Diseases of The Smalllntestine

7
Diseases of the Smalllntestine

E. L. WOLF, P. TAOUREL, B. GALLIX, P. M. BLAYAC, J. M. BRUEL, J. w. A. J. REEDERS, L. E. DERCHI, 0. EKBERG,
C.-H. FLOREN, H. HERLING ER, N. C. GouRTSOYIANNIS, H. JI, R. D. OozE, P. R. Ros, and H. K. HA
7.1
Radiology of Acute and Chronic Small-lntestinallschemia

and Vascular Lesions of the Small Bowel
E. L. WOLF
CONTENTS
Introduction 261
Vascular Anatomy and Collateral Circulation
of the Splanchnic Vessels 261
Pathophysiology 262
7.1.3
Forms of Mesenteric Ischemia
7.1.4
and Clinical Findings 263
Radiographie Findings and Approach to Diagnosis
7.1.5
in Acute Mesenteric Ischemia 264
7.1.5.1 Plain Films 264
7.1.5.2 Computed Tomography 266
7.1.5.3 Sonography 271
7.1.5.4 Angiography 272
7.1.5.5 Barium Studies 273
7.1.5.6 MRI 273
Treatment of Acute Mesenteric Ischemia 274
7.1.6
Focal Mesenteric Ischemia 274
7.1.7
7.1.7.1 Focal Mesenteric Ischemia Due to Bowel
Obstmetion 275
7.1.7.2 Focal Mesenteric Ischemia Due to Radiation 275
7.1.7.3 Focal Mesenteric Ischemia Due to Vaseulitis 276
7.1.8
Chronic Mesenteric Ischemia 276
7.1.9
Celiac Axis Compression Syndrome 277
7.1.10
Vascular Lesions of the Small Bowel 278
7.1.1 0.1 Vascular Ectasia/ Angiodysplasias/ Arteriovenous
Malformation 278
7.1.10.2 Hemangioma 279
7.1.10.3 Varices 279
7.1.11
Conclusion 279
References 279
7.1.1
7.1.2
7 .1.1
lntroduction
Ischemic disease of the small bowel is increasing in
incidence with the aging of the population and as
improved resuscitative measures have saved patients
who would have previously died of cardiovascular
disease but now survive only to develop mesenteric
ischemia as a delayed consequence. In addition, the
E. L. WOLF, MD
Professor, Albert Einstein College of Medicine, Department
of Radiology, Montefiore Medical Center, 111 E 210th Street,
Bronx, NY 10467, USA
diagnosis is being made more frequently, due to an

increased awareness of the various ischemic processes.
Unfortunately, however, the mortality of acute mesenteric ischemia remains high, with rates of over 70%
reported into the late 1990s (VOLTOLINI et al. 1996;
MAMODE et al. 1999). It is estimated that 5% of deaths
in the United States are due to intestinal ischemia
(BRANDT and BOLEY 1993). This high mortality rate
can be attributed to various factors, including delay
in diagnosis, progression of bowel infarction even
after correction of the vascular occlusions has been
clone, and the advanced age of many of these patients.
Since this high mortality is in part due to late diagnosis after intestinal infarction has occurred, it is
important to maintain a high clinical suspicion of
ischemia in the proper clinical setting (the high-risk
groups), to take an aggressive approach in making
the diagnosis by performing early imaging studies,
and to be aware of treatment options in mesenteric
ischemia (WITTENBERG et al.1973; BOLEY et al.1978;
REINUS et al. 1990).
Mesenteric ischemia encompasses a spectrum of
conditions with varied etiologies that range from a
localized transient event to catastrophic necrosis of
majorportians of the gut. The etiology of mesenteric
ischemia is reduced blood flow to the gut. The ischemia may be acute or chronic and due to arterial or
venous occlusion or arterial spasm. Forms of mesenteric ischemia include acute mesenteric ischemia
(AMI), focal mesenteric ischemia, chronic mesenteric
ischemia (CMI), and colanie ischemia.
7.1.2
Vascular Anatomy and Collateral
Circulation of the Splanchnic Vessels
It is necessary to understand the basic anatomy and
collaterals of the splanchnic circulation to understand the events precipitating intestinal ischemia.
(Fig. 7.1.1) The celiac artery, superior mesenteric
artery (SMA), and inferior mesenteric artery supply
N. C. Gourtsoyiannis (ed.), Radiological Imaging of the Small Intestine

Springer-Verlag Berlin Heidelberg 2002
262
E. L. Wolf
areades, with repeated branehing, which serve as eollateral pathways around oeclusions of smaller arterial branehes. Straight vessels arise from the terminal
areade, whieh enter the intestinal wall. These straight
vessels are end vessels, so if oecluded, infaretion may
oeeur.
IUSIMTDIK
COUATI.R.W
H'tP06ASTIK AlTfiT
(JHTfltNAI.IUAC AIITIII'I)
Fig. 7.1.1. Anatomy of the splanchnic circulation and its collaterals. From Haimovici H, et al (eds) (1996), p.985. Reproduced
with permission
IMA. The IMA branehes into the left eolie artery,
whieh supplies the distal transverse and deseending

eolon, has sigmoid branehes, and terminates as the
superior reetal artery.
The eeliae artery and SMA eommunieate via the
panereatieoduodenal areades and, rarely, the artery of
Buhler. The SMA and IMA eommunieate via two main
pathways: (1) the marginal artery of Drummond and
(2) the arc of Riolan. These collaterals open immediately when the SMA or IMA is oecluded and proteet
the bowel from isehemia to varying degrees.
7.1.3
Pathophysiology
The degree and duration of the isehemia, in addition

to the length of bowel involved, will determine the
the vast majority ofblood flow to the gastrointesti- degree of bowel damage. The severity of the injury
nal traet, with the greatest proportion eoming from is inversely related to the blood flow. Various faetors,
including the state of the general cireulation, extent
the SMA.
of eollateral blood flow, response of the mesenterie
to autonomie stimuli, cireulatory vasoaebranehvaseulature
major
three
has
Celiac axis. The eeliae axis
loeal humoral faetors, and the normal
The
substanees,
tive
es: the hepatic, splenie, and left gastrie arteries.
of eellular metabolism before
produets
The
abnormal
and
left gastric supplies a portion of the stomaeh.
the isehemic segment, eonof
reperfusion
after
hepatie artery gives off the gastroduodenal artery, and
intestinal injury (KALEYA
of
severity
the
to
whieh
tribute
whieh divides into the right gastroepiploie,
1995).
BOLEY
supplies part of the stomaeh, and superior panere- and
When a major vessel is occluded, collateral pathatieoduodenal arteries, supplying the panereas and
duodenum. The spienie artery gives offbranches to ways open immediately, and blood flow is maintained
the panereas, the left gastroepiploie artery, and the initially by autoregulation. However, with continued
isehemia, vasoeonstriction develops in the involved
short gastrie arteries.
vaseular bed, whieh elevates the pressure in the
distal bed. This eauses a reduetion in eollateral flow
SMA. The SMA provides the blood flow to the entire and potential eompromise in the bowel vaseularity
small bowel and the aseending and transverse eolon. (KALEYA and OLEY 1995).
As the intestine is deprived of adequate blood flow,
The inferior panereatieoduodenal artery is the first
and morphologie changes develop rapidmetabolie
braneh of the SMA, which anastomoses with brauehes of the superior panereaticoduodenal artery arising ly. Ischemie darnage is produeed both by the hypoxia
from the eeliae artery. This rich anastomosis general- and from reperfusion injury if flow is restored.
ly proteets the duodenum from infaretion. The SMA The initial injury oeeurs at the villus tips of the
then gives rise to the middle eolie artery, right mueosal surface. If the isehemic proeess is mild and
colie artery, ileocolie artery, and has multiple jejunal of short duration, eomplete healing at this stage usuand ileal branehes. These branehes form a series of ally oeeurs. When the isehemia is progressive, howev-
Radiology of Acute and Chronic Small-Intestinal Ischemia and Vascular Lesions of the Small Bowel
er, the necrotic mucosa sloughs, and edema and hemorrhage develop in the lamina propria as the intimal
cells of the end arteries lose their ability to maintain
the integrity of the vessel wall. These submucosal collections of blood and plasma cause thickening of the
mucosal folds and the bowel wall. Coagulation necrosis then advances from the mucosa into the submucosa, and mural infarction develops. At this stage, healing is still possible, although usually with fibrosis and
stricture formation. If the ischemia is more severe
and/or of Ionger duration, coagulation necrosis of
alllayers of the bowel wall develops, and transmural
infarction results (BRANDT and BoLEY 1993; Sc HOLZ
1993; RADBURY et al 1995; LEVINE and JACOBSON
1995).
7.1.4
Forms of Mesenteric lschemia

and Clinical Findings
The spectrum of mesenteric ischemia includes acute
and chronic forms which may be due to arterial or
venous occlusive disease, or nonocclusive ischemia
due to mesenteric vasoconstriction. The etiology of
acute mesenteric ischemia is SMA embolus, SMA
thrombosis, SMV thrombosis, and nonocclusive mesenteric ischemia (NO MI). Regardless of the etiology,
the resultant effect on the bowel is similar.
Retrospective studies have identified patients at high
risk for mesenteric ischemia as those over the age of 50
years, with chronic heart disease, long-standing CHF,
cardiac arrhythmias, previous emboli, recent MI, hypotension, vasculitis, deep vein thrombosis, hypercoagulable states, and sepsis (BOLEY et al. 1973). Ischemia,
especially NOMI, has been increasingly reported after
cardiac surgery (GENNARO et al. 1993), renal dialysis
(DIAMOND et al. 1986), and COCaine use (SUDHAKAR
et al. 1997). However, ischemia can occur in young
patients with no risk factors. A high index of clinical
suspicion of ischemia should be maintained in the
high-risk group with the onset of abdominal pain.
Sudden onset of abdominal pain is found in the
majority of patients, although pain may be atypical or absent in up to 20% of cases (BA TELLIER and
KIENY 1990). Typically, early in the course of the
disease, there is a discrepancy between the degree
of pain and the physical findings, with a paucity of
peritoneal signs and an absence of rebound tenderness or guarding. GIbleeding and abdominal distension are also common, although distension often signals the onset of intestinal infarction. Pain may be
263
absent if infarction has already developed. Laboratory findings, including leukocytosis and metabolic
acidosis, are nonspecific and generally do not develop until after bowel necrosis has occurred. Since clinical and laboratory findings are often inconclusive,
the diagnosis of ischemia may not be made untillate
in the course, after infarction has developed. Since
mesenteric ischemia can progress rapidly, the goal is
to make an early diagnosis of ischemia, before infarction has occurred.
SMA embolism accounts for 40%-50% of cases of
AMI (KALEYA and BoLEY 1995). Patients at risk for
SMA embolism are those with atrial fibrillation or other
cardiac arrhythmias, a history of previous emboli, and
recent myocardial infarction. Emboli usually originate
from mural thrombi in the left atrium or ventricle, or
from cardiac valvular lesions. At least 20% of patients
will have concomitant emboli to other organs at the
time of presentation (BRANDT and BOLEY 1993 ).
SMA thrombosis is commonly seen in patients
with generalized atherosclerosis, but may also be due
to a prothrombin disorder, such as antiphospholipid
syndrome.About 20%-50% of patients have a history
of abdominal pain for weeks to months prior to the
acute episode, in addition to a history of coronary,
cerebrovascular, or peripheral vascular disease. SMA
thrombosis has a high mortality compared with other
causes of AMI (INDERBITZI et al. 1992).
SMV thrombosis is an uncommon cause of mesenteric ischemia, although it is being recognized and
diagnosed more frequently, due to the widespread
use of CT. There are acute, subacute, and chronic
forms. It is reported to be idiopathic in about 20% of
cases, although as more plasma deficiencies are identified, some of these 'idiopathic' cases will probably
be reclassified as due to hypercoagulable states. SMV
thrombosis may be secondary to hypercoagulable
states, neoplasm, postoperative states, especially splenectomy and distal pancreatectomy, local venous
stasis from such conditions as cirrhosis and portal
hypertension, pancreatitis, trauma, peritonitis and
intra-abdominal inflammatory disease. Thrombophlebitis and/or deep vein thrombosis are also risk
factors. It can have a varied presentation, ranging
from asymptomatic cases to acute abdominal pain.
In general, SMV thrombosis has a significantly better
prognosis than the other causes of AMI, since extensive venous collaterals prevent infarction in many
cases (BOLEY et al.1978).
NOMI (low flow) is decreasing in incidence due
to improved resuscitative measures in critical care
units, and possibly also due to the increasing use
of systemic vasodilators, such as the calcium-block-
264
ing agents and nitrates (KALEYA et al1992). Risk factors for NOMI are shock (cardiogenic, hypovolemie,
or septie), dehydration, digitalis, vasopressors, cocaine
use, and open heart surgery. With a decrease in SMA
flow, there is an initial decrease in resistance in the
mesenteric bed, but with continued decreased flow,
the resistance increases. If normal SMA blood flow is
promptly restored, this vasoconstriction is reversible,
but if the blood flow remains low for several hours,
vasoconstriction persists even if the SMA blood flow
returns to normal. Clinieally, the diagnosis of NOMI
may not be suspected, since this group often presents in
an atypical manner, and other medical conditions may
overshadow the ischemic process (HowARD et al. 1996).
Focal segmental ischemia is defined as an ischemic insult to a short segment of intestine in which
there is usually adequate collateral circulation to prevent transmural infarction. Some patients may present acutely, but many present with chronie complaints arising from the sequelae of the acute episode.
Common causes of focal ischemia are strangulation
from small-bowel obstruction or volvulus, collagen
vascular disease, vasculi tis, oral contraceptives, radiation, trauma, and distal emboli. Limited tissue necrosis may result in complete healing, chronic ischemic
enteritis, or stricture formation. If transmural necrosis occurs, perforation or localized peritonitis may
develop.
Chronic mesenterie ischemia is a difficult entity
to diagnose. The dassie presentation is postprandial
epigastric pain, 'fear of food', and weight loss. Symptoms have been attributed to insufficient blood flow
to the gut during periods of maximal intestinal work
load. The primary etiology is atherosclerotie stenosis
of the mesenteric vessels.
7.1.5
Radiographie Findings and Approach
to Diagnosis in Acute Mesenteric lschemia
The diagnosis of acute mesenterie ischemia can be
made or suggested by a variety of imaging modalities,
including plain films, CT, angiography, MRI, ultrasound, and barium studies. The choiee of modality
or modalities will depend on various factors, including availability, expertise, the patient's clinieal evaluation, and the pre-imaging probability of acute mesenteric ischemia. In general, patients with a high
probability of ischemia should undergo angiography
immediately and those in whieh there is a lower suspicion should undergo CT examination.
E. L. Wolf
7 .1.5.1
Plain Films
Plain films of the abdomen are usually obtained in
most patients with abdominal pain and/or suspected ischemia. In ischemia, plain film findings are seen
in a minority of patients, and the findings are often
nonspecific (TOMCHIK et al. 1970; SMITH et al. 1972;
THOMAS 1972; WoLF et al.1992). In addition, positive
plain film findings generally occur late in the course
of the disease process, after infarction has occurred,
and are associated with a high mortality rate (RITZet
al. 1997). Positive plain film findings were identified
in only 30% of patients with proven ischemia in several studies (SMERUD et al. 1990; KLEIN et al. 1995).
Plain films are most useful in ruling out other identifiable causes of abdominal pain, such as bowel perforation and bowel obstruction.
Radiographie plain film findings in ischemie bowel
correlate with the stage of the process and the pathologie and physiologic changes in the bowel wall.
(Table 7.1.1). In the first several hours after the ischemic insult has occurred, plain films will often be
normal. Spasm of the bowel wall is an early physiologie response to ischemia, which causes rapid transit
of the bowel contents and diarrhea, and may produce
a gasless abdomen on plain films. Exudate of blood
and electrolyte-rieh fluid into the bowellumen also
acts to produce fluid-filled, distended, gasless loops.
Submucosal edema and hemorrhage lead to thickened mucosal folds, "pinkyprinting" and/or "thumbprinting" (Fig. 7.1.2). If the ischemia persists, the collections ofblood and edema rupture and slough, and
an ulcerated mucosa develops. Featureless, rigid, or
stiff loops with obliterated valvulae conniventes may
also be identified (Fig. 7.1.3). The muscular layer of
the bowel wallloses its contractile function, and the
bowel becomes atonic and dilated. At this point, plain
films may show an ileus pattern, with an unchanged
loop or loops of bowel on serial radiographs. With
Table 7.1.1. Plain film findings in acute mesenteric ischemia
Generalized or focal paralytic ileus
Gasless abdomen
Bowel wall thickening
Pinkyprinting, thumbprinting
Featureless loops
Rigid or stiff loops with obliterated valvulae
Small-bowel pseudo-obstruction
Unchanging bowelloops
Pneumatosis
Portal venous gas
Pneumoperitoneum
265
Fig. 7.1.2. Thickened folds with pinkyprinting. Supine view of

the abdomen demonstrating thickened folds and pinkyprinting in several small-bowelloops in the left mid-abdomen due
to edema and/or hemorrhage in bowel ischemia
Fig. 7.1.3. Featureless loops. Supine view of the abdomen demonstrates multiple, air-filled loops of small bowel with loss of
the normal valvulae conniventes pattern due to extensive ischemia
extensive small-bowel and right colanie ischemia,

a small-bowel pseudo-obstruction pattern may be
identified (Fig. 7.1.4) (ScHOLTZ 1993). Pneumatosis
may develop when the mucosa sloughs and intraluminal air dissects into the bowel wall (Fig. 7.1.5}.Air
may then dissect further and gain access to the mesenteric and portal veins.
Pneumatosis and portal venous gas are highly suggestive of ischemia in the proper clinical setting, but
both can be seen in other conditions. Pneumatosis
has both 'benign' and 'malignant' forms. The benign
form is associated with conditions such as COPD,
peptic ulcer disease, collagen/vascular disease, and
steroid use (MEYERS et al. 1977} and may be identified in some infections, particularly in the immunosuppressed population. The 'malignant' form is due
to ischemia. The 'benign' form tends to be cystic
or bubbly in appearance, while the 'malignant' form
tends to be linear. However, there is enough overlap
between the two that the appearance of the pneumatosis cannot be relied upon for differentiation.
Pneumatosis is usually a relatively late sign, but does
not necessarily indicate transmural infarction, and in
some cases may be reversible.
Fig. 7.1.4. Pseudo-obstruction pattern. Supine view of the

abdomen demonstrates multiple loops of dilated small bowel
due to loss of contractile fraction and atony of the bowel due
to ischemia
266
E. L. Wolf
Fig. 7.1.5. Pneumatosis. Supine view of the abdomen demonstrates air in the bowel wall (arrows) secondary to dissection of
intraluminal air into the bowel wall due to sloughed mucosa
Fig. 7.1.6. Air in the portal venous system. Branching lucencies

in the liver (arrows) due to air in the portal venous system
On plain films, portal venous gas typically appears

as branching lucencies in the periphery of the liver, as
opposed to gas in the biliary tree which is larger and
more central in location (Fig. 7.1.6}. In some cases,
however, it may difficult to distinguish portal venous
gas from air in the biliary tree. A right-side down
decubitus view may be helpful in distinguishing the
two, as gas in the venous system may shift into the
spienie vein. er has a high er sensitivity for the detection of portal venous gas than plain films. Portal
venous gas detected on plain films has been associated with ischemia in approximately 75% of cases
(LIEB MAN et al.1978}. In the setting of ischemia, portal
venous gas has been associated with a high mortality rate (rEDESCO and STANLEY 1975; GRIFFITHS and
GouGH 1986). Portal venous gas may also be seen
with diverticulitis, gastric ulcer, and other miscellaneous causes. Recent sturlies using er have shown
portal venous gas in a wide variety of circumstances,
with a survival rate of 71% in one series (FABERMAN
and MAYO-SMITH 1997}.
25%-40% of cases in several series (ALPERN et al.

1988; SMERUD et al. 1990). rhis initiallow sensitivity
may in fact be due to technical factors, such as lack
of IV contrast or drip infusion of contrast, thick collimation, noncontiguous slices, and use of first- and
second-generation scanners. With advances in radiologic technology, including helical scanners and rapid
IV contrast bolus techniques, er has become more
sensitive in diagnosing AMI. Recent sturlies have
reported sensitivities of up to 82% (KLEIN et al. 1995;
YAMADA et al. 1998; rAoUREL et al. 1996}. rhe true
sensitivity of er in bowel ischemia is unclear since
the published data are based on retrospective reviews
of er scans in patients with proven ischemia. Some
patients with ischemic bowel may not have er performed, either because they have undergone angiography alone, go directly to surgery, or the diagnosis of
ischemia is not considered. er is also very helpful in
diagnosing other causes of abdominal pain.
7.1.5.2
Computed Tomography
rhe role of er in the diagnosis of AMI is still evolving.

Initially, positive findings were found in only about
7.1.5.2.1
CT Technique
Scanning should be performed using a helical scanner,

using 3- 5 mm collimation and a pitch of 1.5 to 2. Images
should be reconstructed at 1.5- 2.5 mm intervals. Scans
should be obtained in the arterial and venous phases.
A bolus of approximately 130-150 cc of IV contrast
Radiology of Acute and ehronic Small-Intestinal Ischemia and Vascular Lesions of the Small Bowel
should be administered at a rate of between 3 and 5

cc/s. Some recommend a preliminaryunenhanced scan
which permits identification of a high-density acute clot
in the SMA or SMV. Hernarrhage into the bowel wall
may be more easily identified on unenhanced scans as
weil. If there is a high clinical suspicion of ischemia, oral
contrast should not be given, as it interferes with the
evaluation of bowel wall enhancement patterns. Oral
contrast, however, facilitates the identification ofbowel
wall thickening and pneumatosis.
7.1.5.2.2
CTFindings
The CT findings will vary with the extent of bowel

involved and the stage of the ischemic process at
the time of scanning. Many CT findings in AMI correlate with those seen on plain films, but are often
better depicted. Others, such as abnormal bowel wall
enhancement patterns and occlusion of vessels, are
not demonstrated on plain films. CT findings include
bowel distension, bowel wall thickening, pneumatosis, mesenteric and/or portal venous gas, engorgement of the mesenteric veins, mesenteric edema,
ascites, abnormal bowel wall enhancement patterns,
including the target sign or double halo sign, lack
of bowel wall enhancement, reduced or delayed
enhancement, increased or persistent enhancement,
and clots in the SMA or SMV (Table 7.1.2). Emboli
may be identified in other arteries as well, such as
those to the kidney, spleen, or extremities, and associated infarcts may also be seen. Identification of
emboli to other organs increases the suspicion of
mesenteric ischemia, as 20% of patients will present
with concomitant emboli in other areas. Bowel wall
thickening is the most commonly reported finding
267
in ischemia on CT (Fig. 7.1.7) (FEDERLE et al. 1984;

ALPERN et al. 1988; BARTNICKE and ALFE 1994;
YAMADA et al. 1998; RHA et al. 2000). The thickening
is due to submucosal edema and/or hemorrhage and
may be uniform or nodular with pinkyprinting or
thumbprinting. Hemorrhage in the bowel wall may
be high in attenuation (Fig. 7.1.8) and may be better
appreciated on unenhanced scans. Bowel wall thickening alone is nonspecific and may be due to a variety of other causes, including inflammatory, infectious, and neoplastic conditions. Pneumatosis is more
easily identified on CT than on plain films ( CoNNOR
et al. 1984; KELVIN et al. 1984}. On plain films, pneumatosis may be obscured by overlapping bowelloops
or confused with normal bowel gas or with feces in
the colon. CT, due to its cross-sectional nature, has
Fig. 7.1.7. Bowel wall thickening. er scan through the midabdomen showing diffuse thickening of multiple loops of
small bowel due to ischemia
rable 7.1.2. er findings in acute mesenteric ischemia

Bowel dilatation
Bowel wall thickening
Pinkyprinting, thumbprinting
Pneumatosis
Mesenteric and/or portal venous gas
Abnormal bowel wall enhancement patterns:
Target sign
Lack of enhancement
Reduced enhancement
Delayed enhancement
Increased or persistent enhancement
Vascular occlusion
Mesenteric edema
Intramural hemorrhage
Ascites
Pneumaperitoneum
Fig. 7.1.8. Hernarrhage into the bowel wall. er scan at the Ievel
of the pelvis demonstrates thickening and high attenuation in
the bowel wall from bleeding due to ischemia
268
the ability to demonstrate the bowel wall en face or

in profile without overlapping loops, which facilitates
the identification of pneumatosis. Gas in the bowel
wall may be cystic, linear, or curvilinear in appearance (Fig. 7.1.9). Differentiation of pneumatosis from
intraluminal air can be made by identifying the circumferential distribution of the air, paralleling the
bowel wall and/or air in the dependent or peripheral
aspect of the bowel, and the Iack of air fluid or air
contrast Ievels seen with intraluminal air (CoNNOR et
al. 1984). Oral cantrast facilitates the identification of
pneumatosis. Widening the window width (lung windows) is often helpful in detecting intramural air, as
it will become more conspicuous (Fig. 7.1.10).
Fig. 7.1.9. Pneumatosis. CT scan at the Ievel of the mid-abdomen showing pneumatosis with air in a dependent position in
the bowel wall (arrows)
Fig. 7.1.10. Pneumatosis. CT scan at the Ievel of the pelvis using

a wide window width (Jung windows) which facilitates identification of air in the bowel wall. Circumferential collections of
air are identified in multiple bowelloops
E. L. Wolf
Portal venous gas is also more easily identified on

CT than on plain films, especially if a small amount
is present (Figs. 7.1.11 and 7.1.12). As discussed previously, the significance of the identification of portal
gas is changing. It may be identified more frequently
nowadays, and it is no Ionger necessarily the poor
prognostic sign it was once considered tobe (GRAHAM
et al. 1975; TEDESCO and STANLEY 1975; FABERMAN
and MAYO-SMITH 1997; HONG et al. 1997).
In the setting of ischemia, portal venous gas is
almost always, if not always, seen in association with
pneumatosis (SMERUD et al. 1990; TAOUREL et al.
1996). Air may gain access to the mesenteric circulation secondary to dissection of gas from the bowel
wall, and may then continue into the portal vein.
Although there are reports of cases of gas identified
in the IMV on plain film (GRAHAM et al. 1975), CT
is generally necessary to identify mesenteric venous
gas (Fig. 7.1.13). Gas in the mesenteric circulation
may also be identified in other conditions besides
ischemia, particularly sepsis.
Engorgement of mesenteric veins has also been
identified in ischemia (Fig. 7.1.14). This finding is
thought to be due to venous congestion secondary to
stasis (LuNn et al.1988). Infiltration of the mesenteric
fat secondary to mesenteric edema may also be identified, although it is a nonspecific finding.
Occlusion of the SMA and SMV may be identified
on IV contrast-enhanced bolus scanning.An embolus
or thrombosis of the SMA may present as nonenhancement of the SMA, abrupt cutoff of the SMA,
or as an intraluminal filling defect within the SMA
(Fig. 7.1.15). It is important to note that only about
Fig. 7.1.11. Portal venous gas. CT scan through the liver demonstrating branching structures containing air in a peripherallocation due to air in the portal venous system
Fig. 7.1.12. Portal venous gas; small amount. CT scan through

the liver demonstrating a small amount of air in the portal
venous system, not seen on plain film
20o/o of SMA emboli lodge at the origin of the vessel,

while the remainder lodge beyond the origin of the
middle colic artery. It is therefore very important to
scrutinize the entire course of the SMA for evidence
of nonenhancement or cutoff. (Fig. 7.1.16). Occlusion
of the SMA at its origin is typical of SMA thrombosis.
CT angiography with reconstruction of the mesenteric vessels to provide three-dimensional data may
be performed in addition to routine axial images for
further evaluation (NAPEL et al. 1992). On noncantrast examinations, high density due to an acute clot
may be observed in the SMA (NozAKI et al. 1991)
(Fig. 7.1.17). Occlusion of the SMA does not necessarily imply AMI, however, as SMA occlusion may
be seen in asymptomatic patients if the occlusion is
chronic and the collateral circulation is adequate. CT
is not sensitive to mesenteric artery branch occlusions or NOMI, and angiography generally must be
performed to make these diagnoses.
SMV thrombosis (MVT) is readily diagnosed on
CT if an appropriate technique is used. It is necessary to obtain a venous phase in addition to an arterial phase, as venous structures will not be enhanced
during the arterial phase. In addition pseudothrombosis of the SMV may be apparent secondary to
wash in of unopacified blood and other artifacts.
Characteristic findings on CT are low attenuation of
the SMV secondary to a clot in the lumen, with an
enhancing wall secondary to cantrast enhancement
ofthe vasa vasorum (Fig. 7.1.18) (MATos et al. 1986;
KIM et al. 1993). Thrombus may also propagate into
or from the portal vein and/or splenic vein. If noncantrast examination is performed, a high-density
clot may be seen. Rarely, thrombus may be iden-
269
Fig. 7.1.13. Mesenteric venous gas. CT scan at the Ievel of the

kidneys showing gas in the mesenteric venous system (arrows).
Mesenteric venous gas is generally seen in association with pneumatosis
Fig. 7.1.14. Engorgement of mesenteric veins. CT scan at the

Ievel of the mid-abdomen showing engorged mesenteric veins
secondary to stasis. Ascites is also present
Fig. 7.1.15. SMA occlusion. CT scan through the upper abdomen showing nonenhancement of the SMA (arrow) secondary
to embolus
270
E. L. Wolf
Fig. 7.1.16A,B. Embolus to the distal SMA and left renal artery. CT sean at the Ievel of the lower pole of the kidneys shows
nonenhaneement of the left kidney due to embolus with flow in the SMA at that Ievel. B CT sean eaudal to A shows a clot in
the distal SMA (arrow)
Fig. 7.1.17. Aeute clot in SMA on noneoutrast CT examination

(arrow). Noneoutrast CT sean at the Ievel of the proximal SMA
demonstrates high density due to a clot in the SMA. Reprinted
with permission from Nozaki et al. (1991)
Fig. 7.1.18. SMV thrombosis. Contrast-enhaneed CT sean

through the upper abdomen shows low attenuation due to a
clot in the SMV Iumen. The peripheral enhaneement is due to
contrast enhaneement of the vasa vasorum
tified in peripheral branches of the IMV (KIM et

al.l993). CT has been shown to be more sensitive
than angiography in the diagnosis of MVT. Ischemic bowel secondary to SMV thrombosis is typically markedly thickened due to extensive edema
and hemorrhage. The bowel wall may be hyperemic, with persistent enhancement secondary to
slow arterial flow due to increased outflow resistance. These findings correlate with the angiographic findings in SMV thrombosis of prolongation of
the arterial phase with intense opacification of the
bowel wall (BOLEY et al. 1978; CLARK and GALLANT
1984).
Abnormal bowel wall enhancement patterns, attributable to perfusion problems, may also be identified in
ischemia, including the target sign, absent bowel wall
enhancement, poor or reduced enhancement, delayed
enhancement, and increased enhancement. Focal or
diffuse lack of bowel wall enhancement is probably
specific for ischemia and has not been described in
other conditions (TAOUREL et al. 1996) (Fig. 7.1.19).
This may be the only sign of ischemia, early in its
course, before edema, hemorrhage, and bowel wall
thickening develop. Lack of bowel wall enhancement
may be difficult to identify if oral contrast has been
administered. The 'target sign' or 'double halo sign'
of alternating bands of high and low density due to
hyperemia or hemorrhage and edema is commonly
seen, but is not specific for ischemia (Fig. 7.1.20).
Delayed enhancement may be identified if arterial and
venous phases or delayed scans are obtained, presumably due to collateral circulation with slower flow, or
venous outflow obstruction with reflex arterial vasoconstriction (ZALCMAN et al.l996). Reduced enhancement has been described in patients with nonocclusive
ischemia (KLEIN et al. 1995). Persistent enhancement
Fig. 7.1.19. Lack ofbowel wall enhancement. Contrast-enhanced

CT scan at the Ievel of the pelvis shows several loops of small
bowel with Iack ofbowel wall enhancement due to ischemia. This
finding has not been described in other conditions
271
Ultrasound can assess the bowel wall and the mesenteric vessels and may identify air in the portal
venous system. Bowel wall thickening may be readily
appreciated, and differentiation from other causes of
bowel wall thickening may be made in some cases with
Doppler (LEDERMAN et al. 2000). With ischemic bowel
and/or intramural hematoma, symmetric thickening
with reduced or absent peristalsis may be observed
(LEE et al. 1977). Pneumatosis may also be identified,
with hyperechoic regions fixed in the posterior aspect
of the bowel wall. Gas in the portal venous system
can be seen by identifying confluent bright echoes
with or without shadowing, with centripetal movement (Fig. 7.1.21).
The SMA and SMV may also be assessed with uhrasound (PHILLIPS and DIMITRIEVA 1985). Occlusion
and stenosis with intraluminal clot or thrombus may
be identified, and the flow can be assessed with power
or color Doppler. Air in the SMV and portal vein
may be identified as well. Technical difficulties arise
in some cases, however, related to obesity, overlying
bowel gas, and the angle of origin of the SMA. The
sensitivity of sonography in identifying occlusions or
severe stenoses of the splanchnic vessel origins ranges
from 70%-100% (NICOLOFF et al. 1997; LIM et al.
1999). However, most SMA emboli lodge distal to the
origin of the SMA and cannot be detected by Doppler.
Thus, flow may be normal in the proximal SMA with
a distal embolus, and a false-negative study may be
obtained under these conditions. Another limitation
of sonography in the diagnosis of AMI is its inability
to diagnose NOMI.
Fig. 7.1.20. Target sign. Contrast-enhanced CT scan at the Ievel

of the pelvis shows multiple loops with alternating bands of
high and low density. This is a nonspecific finding but, in the
proper clinical setting, highly suggestive of ischemia
of thickened loops of bowel has also been described,

due to slow collateral flow to the bowel or with venous
obstruction (PEREZ et al. 1989).
7.1.5.3
Sonography
Sonography is often the first examination performed
in patients with acute abdominal pain, and the diagnosis of ischemia may first be suggested by ultrasound. Sonography also plays a role in the diagnosis
of chronic mesenteric ischemia, as will be discussed
later.
Fig. 7.1.21. Portal venous gas on ultrasound. Bright echoes due

to air are identified in the liver, which on real time demonstrates centripetal movement
272
E. L. Wolf
7.1.5.4
Angiography
Angiography has been considered the 'gold standard'

in the diagnosis of acute mesenteric ischemia. Boley
and others have shown that the early and extensive
use of angiography, and intra-arterial papaverine
infusion in cases ofNOMI and SMA emboli, improves
survival (BOLEY et al. 1973; ATELLIER and KIENY
1990). In the era of spiral CT, with its ability to diagnosis major vascular occlusions, the role of angiography has been questioned by some. Angiography is
still considered useful (1) as it is the only imaging
study which can reliably establish the diagnosis of
nonocclusive disease (NOMI); (2) to determine the
nature and site of occlusive disease; (3) to evaluate
the perfusion of the vascular bed distal to the occlusion; (4) to provide access for intra-arterial drug
infusion; and (5) to provide a 'roadmap' for revascularization procedures (BAKAL et al. 1992).
Emboli in the SMA typically appear on angiography as sharp, round, or meniscus defects which
usually lodge at branch points and sites of normal
vessel narrowing (Fig. 7.1.22). About 50% of emboli
are found just distal to the origin of the middle colic
artery, with 20% at the origin and the remainder
more distal (Fig. 7.1.23). Boley has classified major
emboli as those proximal to the origin of the ileocolic artery and minor emboli as those distal to that
point or in branches of the SMA. Minor emboli without bowel necrosis have different management and
prognostic implications than major emboli.
SMA thrombosis usually occurs at the origin or
within the first 2 cm of the SMA trunk and appears as
nonfilling of the SMA or as an abrupt vessel cutoff. Since
thrombosis is due to underlying atherosclerotic disease,
except in iatrogenic cases, reconstituted distal vessels
secondary to collateral fiow may be found. Atherosclerosis in other vessels supports the diagnosis.
NOMI may only be diagnosed reliably by angiography. The angiographic findings are diffuse narrowing of the SMA and its branches, localized narrowings
of the origins of multiple SMA branches, alternating
areas of narrowing and dilatation of SMA branches,
spasm of the arcades, and impaired filling of intramural vessels (SIEGELMAN et al. 1974; CLARK and GALLANT 1984; BAKAL et al. 1992) (Fig. 7.1.24). The submucosal 'blush' is absent. The same findings can be
seen in patients in shock or on pressors and in acute
pancreatitis. Selective transcatheter infusion of papaverine into the SMA has been shown to be an effective
means of reversing the vasospasm seen in NOMI
(BOLEY et al. 1973; KALEYA et al. 1992; BAKAL et al.
Fig. 7.1.22. SMA embolus. Film from a selective SMA angiogram demonstrating abrupt termination of the SMA due to
embolus
Inferior
pancreaticoduodendal
Middle
colic
Jejunal
branches
Right
colic
lleocolic
lleal
branches
Fig. 7.1.23. Common sites of SMA emboli. Reprinted with permission from Kaleya et al. (1992)
Radiology of Acute and Chronic Smali-Intestinal Ischemia and Vascular Lesions of the Small Bowel
273
A
Fig. 7.1.24A,B. Nonocclusive mesenteric ischemia. A Selective SMA angiogram shows marked narrowing at the SMA and its
branches. B After papaverine infusion into the SMA, significant improvement in the vasospasm is observed
1992). With this approach, the survival rate has been

shown tobe significantly improved (BoLEY et al. 1973;
eLARK and GALLANT 1984; WARDet al. 1995).
SMV thrombosis may be a difficult diagnosis on
angiography, but is easily diagnosed on er. On selective SMA angiography, reflux of contrast into the
aorta and a prolonged arterial phase is typical. rhe
venous phase may be absent, or venous occlusion
with venous collaterals may be seen. A filling defect
due to a clot within the SMV may be identified.
Barium sturlies correlate with the plain film and er

findings previously described. Dilatation is a nonspecific finding. Submucosal edema and/or hemorrhage may
be manifested initially as thickened folds, which may
progress to a 'stack of coins' or 'picket fence' appearance (Fig. 7.1.25). A scalloped contour to the bowel
wall or frank pinkyprinting or thumbprinting may be
observed. If necrosis and sloughing develop, a shaggy
or ulcerated mucosal pattern develops. Effacement of
the mucosal pattern, rigid loops, and flaccid loops with
prolonged stasis of barium have also been described
(rHOMAS 1972; JOFFE et al. 1977) (Fig. 7.1.26).
7.1.5.5
Barium Studies
7.1.5.6
In the setting of acute mesenteric ischemia, barium
sturlies are generally not indicated, as the findings are
often nonspecific, occur late, and the administration
of barium may interfere with subsequent angiography
and/or er examination. However, they may be performed in patients with atypical presentations and/or
when the diagnosis is not suspected.
MRI
MR is being increasingly used for the evaluation

of the arterial and venous circulation and of intraabdominal pathology. Applications of MRI in mesenteric ischemia have been investigated by Li and others
(LI et al. 1994, 1995, 1999; URKART et al. 1995; HEISS
274
E.L. Wolf
and LI 1998; SHIRKHODA et al. 1998). Both anatomic

and functional information can be obtained. MRA
with gadolinium can demoostrate the mesenteric vasculature to second- and third-order branches, and
abnormal bowel wall enhancement can be observed.
The rate and volume of ftow in the SMA and SMV can
be assessed with eine phase contrast MRA. On Tl- and
T2-weighted MR images, fresh thrombus may be identified in the SMA as a hyperintense signal. MR may
play an increasing role in the diagnosis of AMI in
the future, as technical advances are made and widespread accessibility improves.
7.1.6
Treatment of Acute Mesenteric lschemia
Fig. 7.1.25. Thickened folds due to submucosal edema and/or

hemorrhage. Small bowel series with barium demonstrates
a loop of jejunum with thickened folds, 'stack of coins', and
thumbprinting due to submucosal edema and/or hemorrhage
from ischemia
The treatment of AMI will in part be determined by the

etiology and the stage at which the diagnosis is made.
In patients with peritoneal signs and necrotic bowel,
regardless of the etiology, bowel resection must be
performed. SMA embolism is traditionally treated by
embolectomy. If a major embolus has been identified
on angiography, some advocate papaverine infusion in
addition to embolectomy, since vasoconstriction may
occur in association with an embolus, even after it has
been removed (BAKAL et al. 1992; KALEYA et al. 1992).
Recent reports have described the successful use of
fibrolytic agents in selected patients with SMA embolism (ScHOENBAUM et al. 1992; REGAN et al. 1996). SMA
thrombosis is treated by surgical revascularization with
bypass grafting or reimplantation with thrombectomy.
As previously mentioned, NOMI may be treated by
papaverine infusion into the SMA. If peritoneal signs
are present and/or there is a suspicion of necrotic
bowel, surgical exploration must be performed as weil.
The treatment for SMV thrombosis is evolving. Necrotic bowel should be resected. Surgical thrombectomy
and/or anticoagulation has been the standard therapy.
Thrombolysis, by various methods, has been reported
and is gaining in acceptance as an alternative therapy in
the absence of necrotic bowel (Y ANKES et al. 1988).
7.1.7
Focal Mesenteric lschemia
Fig. 7.1.26. Effacement of the mucosal pattern. Small-bowel

series with barium demonstrates effacement of the mucosal
pattern in the jejunum due to ischemia
Focal segmental ischemia is due to vascular insults to

short segments of the small bowel. Under these circumstances, collateral vessels are usually able to prevent transmural infarction, and the acute life-threat-
ening situation found with more extensive ischemia

is not usually encountered. The etiology of this condition includes minor emboli (those distal to the
ileocolic branch of the SMA), small bowel obstruction, strangulated hernias, closed loop obstruction,
immune complex disorders and vasculitis (lupus),
radiation, oral contraceptives, and blunt abdominal
trauma (BRANDT and BoLEY 1993). In the acute setting, the radiographic findings previously described in
AMI may be identified but are limited to short segments of bowel. If the collaterals are adequate or, as
in the case of obstruction, if the obstruction is relieved
and infarction has not occurred, complete healing
may occur. A chronic enteritis with radiographic findings similar to Crohn's disease may develop in some
cases without complete healing but without transmural
infarction (BRANDT and BOLEY 1993). Some patients
may heal with stricture formation (Fig. 7.1.27).
275
to be fairly sensitive in identifying ischemia using the

criteria previously described, but not very specific, in
that there is an overlap of findings between strangulated and nonstrangulated obstruction. Closed loop
obstruction, which has a high incidence of associated
ischemia, is due to obstruction of a segment ofbowel
at two points. Vascular compromise results from
obstruction to venous outflow, which then induces
a reflex arterial vasoconstriction. Increased intraluminal pressure is another contributory factor in the
development of ischemia (ZALCMAN et al. 1996). The
CT findings suggestive of closed loop obstruction
include ( 1) two adjacent collapsed loops ofbowel with
an isolated conglomerate of a dilated, fluid-filled loop
or loops between them; (2) U-shaped configuration of
a distended, fluid-filled bowelloop; (3) radial distribution ofloops and/or mesenteric vessels converging
toward the point of obstruction; (4) beak sign or serrated beak sign at the site of obstruction; (5) whirl sign
at the point of obstruction; and (6) triangular configuration of the collapsed loop at the site of obstruction,
which is the cross-sectional equivalent of the beak sign
(CHO et al. 1989; MAGLINTE et al. 1991; ZALCMAN et
al. 1996; BALTHAZAR et al. 1992}.
7.1.7.2
Focal Mesenteric lschemia Due to Radiation
Fig. 7.1.27. Focal ischemia with stricture. Small-bowel series

demonstrating stricture formation in the jejunum due to healing of a segment of focal ischemic bowel
7.1.7.1
Focal Mesenteric lschemia Due
to Bowel Obstruction
Many reports in the Iiterature have addressed the
CT findings of bowel ischemia due to small-bowel
obstruction (FRAGER et al. 1996; BALTHAZAR et al.
1997; MAKITA et al.1999). Overall, CT has been shown
Radiation may cause intestinal ischemia due to endarteritis obliterans of the small vessels in the bowel
wall. The incidence of GI complications secondary to
RT is estimated to be between 2o/o and 5%. Doses of
5000 rads are generally necessary to produce radiation darnage to the GI tract.
The small bowel is the most radiosensitive intraabdominal organ. The distal small bowel and terminal
ileum are most commonly affected. RT to the lower
abdomen and pelvis is commonly given for gynecologic malignancy. Patients at increased risk for radiation
darnage are ( 1) those with a history of previous surgery
or peritonitis which could lead to adhesions and fixation ofbowel, (2) those patients, usuallywomen and the
elderly, who have an increased amount of small bowel
in the cul-de-sac (GALLAND and SPENCER 1987} and a
decreased amount of subcutaneous tissue, (3) those with
conditions which may cause vascular narrowing such
as hypertension, diabetes, atherosclerosis, and cardiovascular disease, (4} those receiving chemotherapy, and
(5) those with conditions causing decreased splanchnic
flow, such as congestive heart failure.
There are acute, subacute, and chronic or late phases
of radiation injury to the small bowel (JACOBS et al.
276
1999). In the acute phase, there is suppression of cellular proliferation that primarily affects the mucosal cells.
The subacute phase occurs 2-12 months after radiation
and is due to obiiterative changes in the arterioles in the
submucosa that causes progressive ischemic change.
The late phase may occur up to 25 years later but is usually seen 2-10 years after radiation.
The radiographic findings in radiation enteritis are
nonspecific and are similar to other causes of ischemia
(MASON et al. 1970). In the acute phase, a nonspecific
ileus may be observed. In the subacute phase, bowel
wall thickening, a 'stack of coins', and thumbprinting
due to edema is commonly observed on bariurn studies and CT. Ulceration may also be identified at this
stage. In the chronic stage, fibrosis develops, and stenotic fixed loops may occur, sometimes in association with
fistulae or sinus tracts. Bowel wall thickening and!or
mesenteric involvement Ieads to separation of loops
(Fig. 7.1.28). At this point, the differentiation of radiation enteritis and Crohn's disease may be difficult. CT
may show the 'target sign' or 'double halo sign', bowel
wall thickening, and bowel angulation. The mesentery
is typically thickened and contracted (FISHMAN et
al. 1984; MENDELSON and NoLAN 1985). Intermittent
small-bowel obstruction is a common presentation in
this phase of the process.
E. L. Wolf
7.1.7.3
Focal Mesenteric lschemia Due to Vaseulitis
Vaseulitis can affect blood vessels of all sizes. Large

vessel involvement occurs in such conditions as polyarteritis nodosa and rheumatoid arthritis, may Iead to
AMI, and may be indistinguishable from ischemia due
to acute emboli or thrombosis. In polyarteritis nodosa,
intiammation of mediurn-sized arteries may Iead to
aneurysm formation as weil. The vasa recta and intramural arteries and arterioles may be affected in all vasculitides, including systemic Iupus erythematosus, polyarteritis nodosa, dermatomyositis, Henoch-Schoenlein
purpura, rheumatoid vasculitis, Wegener's granulomatosis, and Churg-Strauss syndrome. The pathologic
changes are generally the result of immune complex
deposition in the vessel wall, leading to perivascular
intiammation, aneurysm formation, vessel perforation,
occlusion, thrombosis, fibrosis, and necrosis (BRANDT
and BOLEY 1993).
The radiographic findings on plain films, CT, and
barium studies are usually indistinguishable from
other causes of ischemia. In Iupus, ischemia has
been shown to be the most common cause of acute
abdominal pain (BYUN et al.1999). Multifocal sites of
involvement of the small bowel were commonly
seen in one study (BYUN et al. 1999). The 'comb
sign', a conspicuous prominence of mesenteric vessels with a palisade or comblike arrangement, has
been described as an early sign of Iupus mesenteric
vasculitis on CT (Ko et al. 1997).
7.1.8
Chronic Mesenteric lschemia
Fig. 7.1.28. Chronic stage radiation enteritis. Small-bowel

series showing multiple, separated, fixed, stenotic loops due to
radiation changes in the chronic stage
Chronic mesenteric ischemia (CMI) is a rare syndrome consisting of postprandial abdominal pain
occurring shortly after meals, gradually increasing
in severity, reaching a plateau and then slowly abating over several hours. The association of pain with
meals Ieads to fear of eating and usually weight loss.
Women are more commonly affected, with a female
to male ratio of ab out 3:1. The cause is almost always
advanced atherosclerosis. Many patients will have a
history of coronary artery disease, peripheral vascular disease, cerebrovascular disease, and/or hypertension. (MOAWAD and GEWERTZ 1997).
This syndrome has also been referred to as 'abdominal angina'. The pain has been attributed to insufficient blood tiow during periods of maximal intestinal work, with the blood supply being insufficient to
meet the metabolic requirements of increased oxygen

demand. Recent studies have suggested, however, that
the pain is due to an increase in demand for gastric
blood ow with eating, which leads to a 'steal' ofblood
ow from the intestine. The subsequent small-bowel
acidosis then causes abdominal pain (PooLE et al.
1987). This explanation better accounts for the temporal relationship of the pain to eating.
The diagnosis of CMI may be difficult, since there
is no specific reliable diagnostic examination, except
possibly for tonometry (BoLEY et al. 1991). The diagnosis has been based on the presence of the typical
symptoms, angiographic demonstration of vascular
occlusions, and exclusion of other causes of pain.
Barium studies in CMI are usually normal,
although a malabsorption pattern may be observed.
Angiography has been considered the most definitive radiologic procedure to establish the diagnosis.
Severe reduction in blood ow, with occlusion or
severe stenosis of at least two of the three splanchnic vessels is necessary before CMI becomes clinically apparent. The demonstration of multiple occlusions in and of itself is not diagnostic of CMI, however, as some patients with occlusions of two or even
three vessels may be asymptomatic, so that anatomic
information alone is insufficient to establish the diagnosis of CMI (RooBOTTOM and DuBBINS 1993).
Duplex Doppler uhrasound can be used as a
screening examination for CMI. Sensitivities as high
as 92%-100% for high-grade SMA stenosis and
87%-100% for high-grade celiac stenosis have been
reported with specificities of approximately 90%
(MoNETA et al. 1991; LIM et al. 1999). Repeat postprandial examinations have been advocated by some
investigators but have not definitively increased the
sensitivity or specificity (GENTILE et al. 1995). Sonography has limitations, however, due to overlying bowel
gas, vessel wall calcification, and interobserver variability.
MRI shows promise in the diagnosis of CMI. Contrast-enhanced MRA of the mesenteric circulation is
an effective noninvasive screening method for the
evaluation of the celiac and SMA origins (MEANEY et
al. 1997; LI et al. 1994). These studies have shown that
the celiac and SMA origins can be reliably evaluated
with gadolinium-enhanced MRA, although technical
difficulties exist. In one study, MR correctly evaluated all normal celiac artery and SMA origins, but
undergraded or overgraded stenoses in 8 of30 arteries
(MEANEY et al. 1997). It can be concluded from these
studies that ifMRA showsnormal arteries, the workup
can stop, and these patients will probably not benefit
from conventional angiography. If MRA is nondiag-
277
nostic or shows stenoses, additional studies are necessary. Li et al. have used eine phase cantrast MRA to
assess the rate and volume of ow in the mesenteric
vessels (LI et al. 1994, 1995). In another study, the
T2 relaxation time of the SMV blood was shown to
decrease in patients with CMI after a meal as compared with healthy controls (LI et al. 1999) This occurs
because with the reduction in blood ow to the small
intestine, the oxygen extraction increases, and the
oxygen Saturation of blood in the SMV decreases.
Paramagnetic substances that are not homogeneously distributed produce T2 shortening. Deoxyhemoglobin in red blood cells is paramagnetic and inhomogeneously distributed, whereas oxyhemoglobin is not
paramagnetic, so an increase in deoxygenated hemoglobin leads to a decrease in blood T2.
Boley et al. have described tonometry as a test for
CMI (BoLEY et al. 1991 ). A tonometer, which measures
intramural pH, is passed per os. In a patient with CMI,
the intramural pH was shown to fall after a test meal
into the stomach, and correlated with symptoms of
abdominal pain. This method also excluded CMI in
others whose postprandial pain proved not to be of
ischemic origin. Boley et al. recommends tonometry
as a screening method for CMI before angiography,
although this has not been widely employed.
Treatment of CMI has traditionally been surgical
revascularization. Percutaneous transluminal angioplasty and/or stents are now alternatives in selected
patients.
7.1.9
Celiac Axis Compression Syndrome
The celiac axis compression syndrome (median arcuate ligament syndrome, Dunbar's syndrome) isarare
cause of CMI. This controversial condition is due to
compression of the celiac axis by the median arcuate
ligament of the diaphragm, resulting in chronic mesenteric ischemia. The median arcuate ligament unites
the crura on either side of the aortic hiatus. It usually
passes posteriorly and inferiorly to the origin of the
celiac axis. It may, however, pass anteriorly and compress the celiac trunk against the aorta. This entity
is controversial because CMI should not theoretically
result from stenosis of one splanchnic vessel, particularly the celiac axis, since there is a rich collateral circulation from the pancreaticoduodenal arcades.
In addition, compression of the celiac axis by
the median arcuate ligament can be demonstrated
in asymptomatic patients as a normal variant in
278
10o/o-24o/o of the population (LINDNER and KEMPRUD

1971). The diagnosis depends on the typieal clinieal
and radiographie findings and the exclusion of other
causes of abdominal pain. Clinical improvement has
been doeumented after surgery in some patients.
Clinically, this syndrome most often affeets young
women with a female to male ratio of 4:1. The typical
age at presentation is between 20 and 50 years. The
chief complaint is chronic abdominal pain, but the
dassie relation to meals and subsequent 'fear of food'
is variable. An epigastric bruit, which beeomes louder
on expiration, is the hallmark physical examination
finding. This is a nonspecifie finding, however, as epigastrie bruits may be found in normal people as well
(JULIUS and STEWART 1967).
The angiographic findings in celiae axis compression syndrome are eccentric stenosis of the proximal
eeliae trunk whieh is aeeentuated on expiration, poststenotie dilatation of the distal eeliae axis, delayed filling of eeliae branehes via eollateral fl.ow, and laek of
atherosclerotic change in other vessels (Fig. 7.1.29)
(DUNBAR et al. 1965).
The CT findings have been deseribed as effacement
or narrowing of the eeliae trunk by an anterior soft-tissue band, and in some cases, assoeiated dilated peri-
Fig. 7.1.29. Celiac axis compression syndrome. Lateral view

from an abdominal aortic angiogram demonstrating stenosis
of the proximal celiac trunk
E.L. Wolf
panereatie eollateral vessels and poststenotie dilatation

of the eeliae trunk (PATTEN et al. 1991). The eeliae
trunk may appear narrow or effaeed in asymptomatie
patients, however, so the diagnosis depends on the eonstellation of clinical and radiologic findings.
Treatment of the eeliae axis eompression syndrome
is surgieal, with options being eeliae deeompression,
with release of the Iigament, decompression with dilatation, or decompression with reconstruction (reimplantation or bypass) (BECH 1997).
7.1.10
Vascular Lesions of the Small Bowel
7.1.10.1
Vascular Ectasia/Angiodysplasia/Arteriovenous
Malformation
The terms vascular ectasia and angiodysplasia are

used interchangeably and are defined as eetasia
of normal preexisting intestinal submueosal veins,
venules, and overlying mucosal eapillaries. With the
eventual loss of preeapillary sphineter funetions,
an arteriovenous eommunication is created. Congenital arteriovenous malformations are developmental
anomalies, due to embryonie growth defeets.
Vascular lesions of the small bowel are being identified with increasing frequeney as a eause of GI
bleeding. Angiodysplasia of the small bowel aeeounts
for 30o/o-40o/o of eases of GI bleeding of obscure
origin and is the most eommon eause of bleeding
in this group of patients (Fou TCH 1993). Angiodysplasias have been reported to oeeur with higher frequeney in association with renal failure, von Willebrand's disease, aortic stenosis, cirrhosis, and pulmonary disease (FouTCH 1993). The lesions may be
multiple. The jejunum is the most common smallbowel site for AVMs (MEYER et al. 1981).
The diagnosis of vascular lesions has traditionally
been made by angiography (BoLEY et al. 1977; RICHARDSON et al. 1978). The most eommon finding is a late
draining, dilated, tortuous vein, which is observed in
85o/o-90o/o of cases. A vaseular tuft in the arterial phase
may be seen and is found in approximately 70o/o-75o/o
of patients (Fig. 7.1.30). An early filling vein, indicative
of an arteriovenous communication, has been observed
in about 60o/o-80o/o of cases. Similar findings may be
observed, however, in some cases of polyps, cancer, and
Crohn's disease (PRICE 1986). The diagnosis of these
vascular lesions of the small bowel cannot generally be
made on routine small-bowel series because of their
279
sometimes considered tobe a benign neoplasm, hemangiomas are generally thought to be hamartomas.
rhere are cavernous, capillary, and mixed types. Cavernous hemangiomas are composed of dilated, irregular, blood-filled spaces lined by endothelial cells
with walls of fibrous tissue. eapillary hemangiomas
are composed of a proliferation of capillaries separated by very little stroma. Most hemangiomas are
small, less than 2 cm in diameter, although occasionally they may be larger. rhe jejunum is the most
common location. rhe diagnosis can rarely be made
by barium studies or angiography (Ramanujam et al.
1995;Akamatsu et al.1990).
7.1.10.3
Varices
Fig. 7.1.30. Vascular ectasia. Selective SMA angiogram showing a vascular tuft with an early draining vein due to a vascular
ectasia in the jejunum
small size. AVMs are larger than ectasias and may distort adjacent tissues. Enteroclysis has successfully diagnosed some cases of AVMs by demonstrating subtle,
slightly lobulated, focal widening of a part of a small
bowel fold (MacHet al. 1994).
er has also recently been shown to have the ability to
detect AVMs (MINDELZUN and BEAULIED 1997). Multiple AVMs were detected in one patient using the helical er high bolus technique, arterial and venous phase
scans, and water rather than oral contrast. AVMs were
seen on the arterial phase as enhancing dilated vessels
in the bowel wall with the degree of enhancement sirnilar to that of the aorta. During the venous phase, additional lesions were identified, and some seen on the
arterial phase became less conspicuous.
Newer endoscopic techniques for evaluation of the
small bowel, including push enteroscopy and Sonde
enteroscopy, have identified angiodysplasias in up to
40o/o of patients (GOSTOUT et al. 1991; LEWIS et al.
1991 ), although these techniques are not as yet widely
performed.
7.1.10.2
Hemangioma
Hemangiomas are uncommon lesions in the small
bowel and a rare cause of GI bleeding. Although
Portal hypertension causes portosystemic venous

shunting, usually leading to esophageal, hemorrhoidal, and paraumbilical varices. Less commonly seen
are collaterals between the branches of the superior
and inferior mesenteric veins and the subhepatic and
retroperitoneal veins, which may lead to small-bowel
varices. Small-bowel varices may rarely be identified
on routine small-bowel follow through or enterolysis
as serpiginous defects in the bowel wall (FLEMING and
SEAMAN 1968; AGARWAL and SCHOLZ 1981).
7.1.11
Conclusion
Mesenteric ischemia is increasing in incidence and is
being more commonly diagnosed. Mesenteric ischemia
still has a high mortality rate, in part related to late diagnosis, after infarction has occurred. Early diagnosis and
treatment arevital to change this situation.
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7.2 Radiology of Small-lntestinal Obstruction

P. TAOUREL, B. GALLIX, P. M. BLAYAC, J.-M. RUEL
CONTENTS
Diagnosis of Mechanical Obstmetion 283
Clinical Considerations 283
Abdominal Flain Film 284
Findings 284
Fitfalls 285
Aeeuracy 285
Barium Examination 285
Findings 285
Fitfalls 285
Aeeuraey 285
illtrasound 286
CT 286
Findings 286
Fitfalls 286
Aeeuraey 287
Diagnosis of the Site of the Oeclusion 287
Barium Examination 287
illtrasound 287
Computed Tomography 288
Diagnosis of the Cause of the Oeclusion 288
Enteroclysis 289
Findings 289
Fitfalls 290
Aeeuraey 290
Ultrasound 290
Findings 291
Fitfalls 294
Aeeuracy 294
Diagnosis of Complieations
of the Obstmetion 294
7.2.4.1 Clinical Considerations 294
7.2.4.2 Abdominal Flain Film 295
7.2.4.3 Enteroclysis 295
7.2.4.4 illtrasound 295
7.2.4.5 Computed Tomography 296
7.2.4.5.1 Findings 296
7.2.4.5.2 Fitfalls 296
7.2.4.5.3 Aeeuracy 296
Diagnostic Strategy 297
7.2.5
Referenees 297
7.2.1
7.2.1.1
7.2.1.2
7.2.1.2.1
7.2.1.2.2
7.2.1.2.3
7.2.1.3
7.2.1.3.1
7.2.1.3.2
7.2.1.3.3
7.2.1.4
7.2.1.5
7.2.1.5.1
7.2.1.5.2
7.2.1.5.3
7.2.2
7.2.2.1
7.2.2.2
7.2.2.3
7.2.2.4
7.2.2.5
7.2.3
7.2.3.1
7.2.3.2
7.2.3.3
7.2.3.3.1
7.2.3.3.2
7.2.3.3.3
7.2.3.4
7.2.3.5
7.2.3.5.1
7.2.3.5.2
7.2.3.5.3
7.2.4
F. TAOUREL, F.M. BLAYAC

Imagerie Medieale, Hpital Lapeyronie, Montpellier, Franee
B. GALLIX, J.M. BRUEL
Imagerie Medicale, HFital Saint-Eloi, Montpellier, Franee
Small-bowel obstruction (SBO) is responsible for

approximately lSo/o of surgical admissions for acute
abdominal conditions. Because of significant Iimitations in the clinical and initial radiological evaluation, obstruction is still frequently misdiagnosed. The
value of imaging in the assessment of patients with
suspicion of SBO depends on its ability to answer
the questions relevant to their clinical management.
These questions have been defined by MONDOR et al.
(1943) and reviewed by HERLINGERand MAGLINTE
(1989) and are the following:
ls there a mechanical obstruction?
What is the level of the obstruction?
What is the cause of the obstruction?
ls there finding of Strangulation?
ls the recommended management medical or surgical?
The answer to the last question depends on the
answer to the four previous questions.
This chapter examines the findings, the pitfalls
and the accuracy of radiology when answering these
questions, then recommends an approach for the
diagnostic triage of patients with suspected bowel
obstruction.
7.2.1
Diagnosis of Mechanical Obstruction
7.2.1.1
Clinical Considerations
The clinical diagnosis of SBO classically depends

on four cardinal findings: abdominal pain, vomiting,
constipation and abdominal distension. However, the
clinical findings vary with the degree and level of
bowel obstruction and with the vascular status of the
obstructed segment. In typical mechanical obstruction, abdominal pain is crampy and gradually increases in intensity, only to abate and recur. With time,
increasing bowel distension inhibits motility, and
P. Taourel et al.
284
the pain tends to subside (HERLINGER and RUBESIN

1994). On the other hand, crampy abdominal pain
may be present in other causes of acute abdomen
such as renal colic. In the same way, vomiting or
constipation is obviously not specific for mechanical
obstruction.
The differentiation between complete and partial
occlusion is difficult by using only clinical criteria such
as a total arrest of stool and gas for 24 h in complete
obstruction and the conservation of some transit in partial obstruction (MILLAT et al. 1993) because the conservation of transit may be due to the emptying of the
bowel beyond the site of a complete obstruction. Consequently, as defined by SHRAKE et al. (1991), this differentiation is done by using opacification of the bowel
which allows us to categorize complete obstruction,
high-grade and low-grade partial occlusion. The distinction between complete and partial bowel obstruction is a pivotal key for some authors since a conservative treatment by tube decompression is generally sufficient to treat a partial occlusion safely (SNYDER et
al. 1990), whereas surgical intervention is often necessary with complete obstruction. However, a complete
obstruction may be successfully treated by non-operative intubation (PEETZ et al. 1982). Conversely, surgery
may be recommended in partial obstructions because
Strangulation may develop in a partial small-bowel
obstruction, and the obstruction may be due to a surgically treatable lesion. So the distinction between partial
and total small-bowel obstruction may not be decisive
for their management (TAOUREL et al. 1995).
7.2.1.2
Abdominal Plain Film
7.2.1.2.1
Findings
Distended loops of small bowel containing gas
(Fig. 7.2.1) and fluid are usually present within 3-5
h of the onset of complete obstruction. The interface
between gas and fluid forms a straight horizontal
margin in the upright (Fig. 7.2.1b) or lateral decubitus view. Although gas-fluid levels are occasionally
present normally, more than two gas-fluid levels in
b
Fig. 7.2.la,b. Small-bowel obstruction (SBO) findings on abdominal plain film. Supine (a) and upright (b) views demonstrate
!arge amount of gas in dilated Ioop of small bowel. Air-fluid Ievels are well seen on the upright view (b), while valvulae conniventes are weil outlined by air on the supine view (a). Note the absence of gas in the colon
285
Radiology of Small-Intestinal Obstmetion
the small bowel are generally considered to be abnormal. However, gas-fluid levelsarealso very common
in the ileus. The presence of gas-fluid levels at different heights in the same loop has traditionally been
considered strong evidence of mechanical obstruction. However, one study (HARLOW et al. 1993) has
shown that this pattern was insensitive and can also
be demonstrated in some patients with adynamic
ileus. The distinction between partial and complete
obstruction is made by the visualization or not of gas
beyond the presumed site of the obstruction.
However, a major Iimitation to the use of fluoroscopic

small-bowel follow-through is the fact that the lumen
distensibility cannot be assessed. As a result, the presence of low-grade obstruction may not be revealed.
Conversely, enteroclysis with injection of boluses of
oral contrast permits evaluation of the calibre of the
bowel loops, reduces dilution by retained fluid, and
facilitates propulsion toward the site of obstruction.
7.2.1.2.2
Pitfalls
The diagnosis of mechanical obstruction is made

upon visualization of dilated bowel loops proximal
to the site of obstruction and loops decreased in calibre or collapsed distal to the site of obstruction
. The amount of contrast medium beyond the site
of obstruction and the delay in the arrival of contrast at the point of obstruction allows differentiation
between (SHRAKE et al. 1991; MAGLINTE et al. 1993):
- complete obstruction, when there is no passage of
contrast material beyond the site of obstruction,
as shownon delayed radiographs obtained 3-24 h
after the start of the examination
- high-grade partial SBO, when the presence of
retained fluid delays the development of sufficient
barium density above the site of obstruction and
only small amounts of contrast material enter into
the collapsed loops beyond the obstruction
- low-grade partial SBO, when there is no delay
in the arrival of contrast medium at the zone of
obstruction and when there is a suffi.cient flow of
contrast material through the point of obstruction
to readily define the fold patterns in these distal
loops.
The main difficulty lies in the differential diagnosis

between partial obstruction and ileus in patients with
gas-fluid levels and some air in the colon. Abdominal plain film has a better accuracy in diagnosing
complete obstruction. However, even with complete
obstruction, gas-fluid levels may be missing, and gas
and faecal accumulation may be present in the colon
if the examination is performed within the first
few hours of the onset of symptoms. Finally, in
severe complete obstruction, the bowel proximal to
an obstruction can contain no gas but be completely
filled with fluid, producing sausage-shaped waterdensity shadows that can be diffi.cult to diagnose.
This pattern is seen in patients who swallow little air
or have it removed by effective gastric suction.
7.2.1.2.3
Accuracy
It is roughly estimated that plain film findings are diagnostic of SBO in about 50%-60% of cases, equivocal in
about 20%-30%, and normal, non-specifi.c or misleading in 10%-20% of cases (MucHA 1987). In published
studies, the sensitivity of abdominal plain film varies

between 46% (FRAGER et al. 1994) and 80% (EI SENBERG
et al. 1983). This discrepancy is due both to the population included in the study since, as shown by MAGLINTE
et al. {1996), the sensitivity is higher in high-grade than
in low-grade obstruction (86% versus 26%), and to the
modality used as the standard of reference (surgery and
clinical outcome, enteroclysis, etc.).
7.2.1.3.1
Findings
7.2.1.3.2
Pitfalls
The main diffi.culty in the positive diagnosis of SBO

by enteroclysis is in a patient with complete obstruction involves the slow transit of contrast material in
the fluid-filled small bowel loops, making the diagnostic evaluation of the site of obstruction suboptimal
and taking a long time to complete the examination.
7.2.1.3.3
Accuracy
7.2.1.3
Barium Examination
The filling of the small bowel may be performed by
oral ingestion of barium or water-soluble contrast.
Enteroclysis has a very high sensitivity and negative

predictive value. lt allows us to exclude SBO by showing unimpeded flow of barium from the duodenojejunal junction to the right side of the colon. Fur-
P. Taourel et al.
286
thermore, it reveals low-grade SBO.Its ability to both

diagnose low-grade SBO and exclude the possibility
of SBO makes it the reference standard in some studies evaluating different imaging modalities in SBO
(MAGLINTE et al. 1993, 1996).
7.2.1.4
Ultrasound
As for other modalities, the diagnosis of mechanical

obstruction is based on the dilatation of the bowel
proximal to the obstacle with a collapsed bowel distally; there is an increased intestinal content (Fig. 7.2.2)
with visualization of the valvulae conniventes. The
main advantage of uhrasound is to show the increased
bowel peristalsis in real time with rapid progression of
the bowel content. In contrast to mechanical obstruction, paralytic ileus is characterized by dilated small
bowelloops with abundant gas, a colonic lumen filled
with gas, fluid or stool, and the absence of peristaltic
motion during sonography.
Pitfalls in the US diagnosis of obstruction may be
due to the evolution of the obstruction since after
many hours or days of obstruction or after the development of ischemia, small bowelloops may appear completely atonic. Consequently, as noted by ScHMUTZ et
al. (1997), it is important to know the duration of the
obstructive syndrome before concluding that the lack
of peristalsis is due simply to paralytic ileus.
7.2.1.5
Fig. 7.2.2. SBO findings on US . Dilatation of small bowelloops

which are fluid-filled with some gas bubbles
Fig. 7.2.3. Faeces findings on CT. Faecal retentionproximal to

a collapsed small bowelloop (arrow)
Computed Tomography
7.2.1.5.1
Findings
The CT diagnosis of SBO is based on the presence of a

dilated small bowel proximal to a transition zone and
a collapsed distal small intestine or ascending colon
(MEGIBOW et al. 1991; FUKUYA et al. 1992). The small
bowel is considered dilated when its diameter is wider
than 2.5 cm (FUKUY A et al. 1992). The amount of intraluminal air versus fluid and even the degree of dilatation of the small bowel are not reliable criteria to differentiate mechanical obstruction from ileus. Conversely,
a large discrepancy in the calibre of the bowel loops
at the transition zone and a high degree of collapse in
the distalloops are reliable and convincing findings of
mechanical obstruction. In the same way, faecal retention in the small bowel concomitant with a collapsed
colon is a specific finding of SBO (Fig. 7.2.3). Complete
and partial obstruction of the small bowel are theoretically distinguished on CT scans by determining the
degree of collapse and the amount of residual air and
fluid in the collapsed intestinal segments.
7.2.1.5.2
Pitfalls
er has limitations in the diagnosis of intestinal

obstruction, with both false-negative and false-positive results. False-negative findings are mainly due
to low-grade partial occlusion for which a transition
zone is not clearly individualized. In the same way,
the presence of numerous adhesive bands does not
generate a definite transition zone. Location of the
obstructive process at the ileocecal valve with residual faecal content in the colon may also lead to an erroneous diagnosis of ileus. False-positive findings may
be due to ileus with dilatation of the small bowel
287
and the right colon with a totally collapsed distal

colon, which should not lead to a diagnosis of colanie
obstruction unless a colanie lesion is visualized at the
transition zone (MEGIBOW 1994}.
7.2.1.5.3
Accuracy
The value of CT in the diagnosis of SBO relates to

the severity of the obstruction. Reports on patients
with high-grade obstruction show sensitivities equal
or superior to 90% and specificities of about 95%
(MEGIBOW et al. 1991; FUKUYA et al. 1992; TAOUREL
et al. 1995). In contrast, CT has been found to have a
sensitivity of 64%, a specificity of 79% and an accuracy of 67% in patients with mixed grades of obstruction (MAGLINTE et al. 1993}. When these patients were
subdivided, the sensitivity of CT for high-grade SBO
was 82% but only 50% for low-grade obstruction.
However, it must be noted that in studies including a
high number of patients with low-grade obstruction,
the modality used as the gold standard was enteroclysis and not surgery since most patients are not
operated on, when in fact enteroclysis may provide
a false-positive diagnosis of obstruction, and overall
may detect mechanieal obstruction without any clinical significance. As noted by HERLINGERand RUBESIN
(1994), low-grade SBO may occur intermittently, ease
spontaneously, and not require hospital admission.
7.2.2
Diagnosis of the Site of the Occlusion
7.2.2.1
The diagnosis of the site of a mechanieal obstruction is not easily performed with just clinical data,
even if vomiting is more pronounced in proximal
SBO and abdominal distension in distal obstruction.
The accurate determination of the site of the obstruction is not the major point when considering the
management of patients with SBO; however, this may
be useful for a safe laparoscopic division of adhesions
that may be a suitable form of treatment of adhesive
bands. Additionally, it may represent a valuable predietive factor in the management of adhesive SBO,
since it has been shown that most of the patients with
proximal SBO healed with conservative management,
whereas distal SBO more frequently required surgery
(DONCKIER et al. 1998}.
7.2.2.2
The identification of loops of bowel whieh contain

abnormally large amounts of gas is essential to differentiate small- and large-bowel obstruction. Small
bowelloops generally occupy the more central portion of the abdomen, while colanie loops are positioned laterally araund the periphery of the abdomen
or inferiorly in the pelvis. Gas within the lumen of the
bowel also allows one to outline and differentiate the
valvulae conniventes (Fig. 7.2.1) in the small bowel
from the colanie haustra. Valvulae conniventes are
finer and closer tagether than colanie haustra, and
they completely encircle the small bowel, while colanie haustra occupy only a portion of the diameter of
the colon. In SBO, the presence of a few dilated loops
of small bowel located high and slightly to the left
indicates an obstruction in the proximal jejunum,
whereas more extensive involvement suggests a lower
obstruction. The point of obstruction is always distal
to the lowest loop of dilated loop.
7.2.2.3
Barium Examination
An important advantage of enteroclysis compared

with other methods is its ability to accurately detect
the site of a SBO (Fig. 7.2.4), partieularly in lowgrade obstruction. This may be important to clearly
determine the site of fixation resulting from an adhesive obstruction prior to possible laparoscopie lysis
(HERLINGER and RUBESIN 1994}.Another advantage
is its ability to reveal multiple sites of obstructions. In
cantrast to partial obstruction, the dilatation of the
fluid-filled bowelloops in complete obstruction may
alter the progression of the barium and lead to a weak
concentration of cantrast at the site of a distal obstacle.
7.2.2.4
Ultrasound
The level of the obstruction is determined by the

study of both the pattern and the location of the
dilated loops. Small bowelloops are considered jejunal when the valvulae conniventes are prominent and
numerous, and ileal when they are sparse or absent
(Ko et al. 1993). This allowed SCHMUTZ et al. (1997)
to accurately prediet the level of obstruction in 80%
of cases.
288
Fig. 7.2.4. Low-grade partial obstruction of the distal jejunum

on enterodysis. Note the passage of oral contrast distal to the
obstade, demonstrating that the obstruction is partial
7.2.2.5
Computed Tomography
As noted by ALTHAZAR (1994), eT determines the site

of obstruction by detecting the site of the transition
zone and by surveying all the abdominal axial images
and comparing the relative lengths of the prestenotic
versus collapsed intestine. Attempting to determine the
level of the obstruction based solely on the site of transition can be misleading. Jejunalloops can be located in
the pelvis, and ilealloops can be obstructed in the upper
abdomen. When there are multiple levels of obstruction, er encounters great difficulties in determining the
location of the obstruction.
7.2.3
Diagnosis of the Cause of the Occlusion
7.2.3.1
The pattern of major causes of SBO has changed

during the last five decades. Originally, the most
common cause was external hernia. Now postoperative adhesions comprise 50%-80% of the total
P. Taourel et al.
number of SBO in the USA (MUCHA 1987). The

second most common causes are neoplasm and hernias, each counting for 10%-15%. A fourth miscellaneous group of causes includes inammatory
processes, intussusception, volvulus, endometriosis,
ischaemia, haematoma, congenitallesions, gallstones,
foreign bodies or bezoars. However, the prevalence
of the different causes of SBO varies according to the
clinical context. In patients without any past surgery,
adhesions are less common even if congenital bands
may occur. In patients with previously treated cancer,
obstruction is very common. It occurs in up to 28%
of patients with a history of colorectal cancer and
in as many as 42% of patients with ovarian cancer
(TANG et al.1995). Determining the cause of obstruction becomes a1 vexing problern since it may be
benign postoperative adhesions, a focal malignant
deposit, peritoneal carcinomatosis, ischemic stenosis due to raditis enteritis or incisional entrapment.
Malignant lesions represent the most common cause
of obstruction; however, the percentage of benign
causes of obstruction ranges from 18% to 38% on
the basis of the distribution of the primary cancer
(OSTEN et al. 1980; WALSH and SCHOFIELD 1984;
KETCHAM et al. 1986). Benign obstruction is more
likely if pelvic irradiation was used in the management of the primary tumour (WALSH and ScHOFIELD
1984), whereas the risk of malignant obstruction is
increased if the patient had known metastatic cancer
or if the primary cancer was in an advanced stage
or of gynaecological origin (OosTEN et al.1980; KETCHAM et al.1986).
The diagnostic hypothesis for the cause of a SBO
must take these probability data into account; however, systematic evaluation of imaging data must also be
performed by looking for one of the three major categories of SBO, as stated by HERLINGERand RUBESIN
(1994): intraluminal, intrinsic, and extrinsic (Table
7.2.1). Most extrinsic causes obstruct by attening,
twisting or kinking the small bowel; intrinsic lesions
constrict the Iumen by thickening of the bowel wall;
and intraluminal causes abturate the bowellumen.
The practical value of knowing the cause of SBO
before surgery has dramatically improved treatment
in the last decade. The philosophy of never Iet the
sun set or rise on SBO (MucHA 1987) has been
succeeded by management according to the cause
and the severity of the obstruction (TAOUREL et
al. 1995). Most modern surgeons actually recommend an emergent operative management in hernias, a more delayed surgical management in malignant focal tumour, a medical management in most
cases of peritoneal carcinomatosis, radiation enteri-
289

Table 7.2.1. Causes of small-bowel obstruction in adults
Extrinsic lesions
Intrinsic lesions
Intraluminal causes
Adhesions
Hernias
External
Inguinal
Femoral
Obturator
Sciatic
Perineal
Supravesical
Spigelian
Lumbar
Incisional
Umbilical
Interna!
Paraduodenal
Epiploic foramen
Diaphragmatic (traumatic)
Transomental
Transmesenteric
Iliac fossa
Masses
Extrinsic tumours in mesentery
Lymphoma
Peritoneal metastasis
Carcinoid
Desmoid
Abscess
Diverticulitis
Pelvic infiammatory disease
Crohn's disease
Appendicitis
Aneurysm
Haematoma
Endometriosis
Tumours infiltrating wall of small intestine

Adenocarcinoma
Carcinoid tumour
Lymphoma (rare)
Leiomyosarcoma (rare)
Infiammatory conditions
Crohn's disease
Tuberculosis
Potassium chloride stricture
Eosinophilic gastroenteritis
Vascular
Radiation enteropathy
Ischaemia
Haematoma
Post-traumatic
Thrombocytopenia
Anticoagulants
Henoch-Schnlein purpura
Obturation
Gallstone
Bezoar
Foreign body
Ascaris
Meconium
Intussusception
Adhesions
Tumour
Duplication
Inverted Meckel's diverticulum
tis or jejunal haematoma, and a treatment of adhesions, balancing between medical treatment and surgical exploration according to the patient's status, the
location of the adhesions and overall the suspicion of
Strangulation (DONCKIER et al. 1998).
plain film data for diagnosing the causes of SBO is

about 50%. The main diagnostic arguments are given
bythe interrogation and the clinical examination (surgical past consistent with adhesive bands, palpation of
an external hernia, etc.).
7.2.3.2
7.2.3.3
Enteroclysis
Abdominal plain film is of little value in diagnosing

the cause of SBO. In some very rare cases, it can show
a gallstone in the bowellumen responsible for a gallstone ileus or a calcified phytobezoar. It can also
demonstrate an abnormal situation of dilated bowel
loops in external hernias; however, in these cases, clinical examination has generally diagnosed the hernia
already. In our experience (TAOUREL et al. 1995), the
value of the association of clinical and abdominal
7.2.3.3.1
Findings
The features of the different causes of SBO shown by

enteroclysis have been demonstrated in patients with
suspected low-grade obstruction or a history compatible with intermittent obstruction (HERLINGER
and RUBESIN 1994; HERLINGER 1997). An adhesive
band is responsible for a narrow-crossing radiolu-
290
cency, the distended segment above the adhesive

bands generally terminates abruptly with normal
folds extending to its edge, traces of longitudinal
folds may be seen in the narrowed segments, and the
folds are normal again beyond the obstruction. On
the other hand, in the obstruction caused by metastasis, the folds are abruptly cut off above without
any fold seen at the edge, the narrowed segment is
angulated with destruction of the folds, additionally
the space between the narrowed Iumen and adjacent
bowel is widened, and a rounded termination may be
seen demarcating the widened space. The ability to
provide positive findings of adhesive band obstruction is one of the main advantage of enteroclysis; furthermore, the accurate identification of the site of
obstruction resulting from an adhesive obstruction
can facilitate laparoscopie Iysis. In obstructive diseases which involve Ionger segments of bowel such
as inflammatory conditions or radiation enteropathy, enteroclysis may accurately assess the extent of
involved and uninvolved small bowel before resection and bypass surgery.
7.2.3.3.2
Pitfalls
In patients with complete or high-grade SBO, barium
examination may be difficult because of the long time
required to complete the examination. The dilution
ofbarium that occurs proximal to the site of obstruction makes evaluation of this site and diagnosis of the
cause of SBO suboptimaL Moreover, barium retained
in the small bowel will degrade the quality of subsequent CT examinations. Consequently, enteroclysis
is not recommended in patients with acute presentation of SBO. From this fact, as noted by MAGLINTE
et al. (1997), most of the institutions arenot accomplished in the use of enteroclysis in bowel obstruction and may have difficulty using the semiology
drawn by Herlinger to differentiale SBO by bands
from metastases.
P. Taourel et al.
7.2.3.4
Ultrasound
In the literature, the contribution of US in the diagnosis of obstruction has been mainly studied in small
series of patients with specific disease entities (GAINES
et al.1987; TENNENHOUSE and WILSON 1990; DAVIES
et al. 1991; SENER et al. 1991). Intrinsic stenosis due
to inflammatory disease Ieads to a target-like concentric thickening of the bowel wall with pain during
the passage of the probe. This appearance may sometimes mirnie fluid-filled small bowel loops, but realtime sonographie evaluation demonstrates the absence
of modification during peristalsis with thickened or
unidentifiable valvulae conniventes (SCHMUTZ et al.
1997). Stenosis due to tumours Ieads to a more pronounced and asymmetric thickening of the bowel wall.
US allows a confident diagnosis of intussusception by
using the same semiology as for children and shows
both the intraluminal intussusceptum and the intussuscipiens, responsible for a doughnut pattern with a
series of concentric rings and an echogenic centre. The
main advantage of US is a reliable and quick diagnosis of external hernias; furthermore, US is largely
used to characterize a mass in the groin and to identify
bowel inside the mass (Fig. 7.2.5) (VAN DEN BERG
et al. 2000). Finally, adhesions are considered to be
the cause of the obstruction when there are findings
of mechanieal obstruction without any identifiable
cause. However in clinical practice, US remains little
used in the investigation of patients with suspected
SBO, probably because its accuracy for the diagnosis
of cause, whieh varies between 42% (DANSE et al.
1996) and 74% (ScHMUTZ et al. 1997), is inferior to
thatofCT.
7.2.3.3.3
Accuracy
Enteroclysis has been reported as accurate in the diagnosis of the cause of SBO and correctly predicted it
in 86% of cases in the study of SHRAKE et al. (1991).
However, enteroclysis is mainly used in patients with a
suspicion oflow-grade obstruction, for whom medical
treatment with a nasogastrie tube is often sufficient.
This hinders the determination of a gold standard and
the reliable evaluation of enteroclysis.
Fig. 7.2.5. Indirect inguinal hernia on US. Note the dilatation

of the bowelloops inside the hernias and the peritoneal effusion
291
7.2.3.5
Computed Tomography
7.2.3.5.1
Findings
The diagnosis of the cause of a SBO is one of the

more exciting possibilities of CT concerning acute
abdomens. By its ability to show the bowellumen, the
bowel wall as well as the bowel environment, CT may
diagnose intraluminal, intrinsic and extrinsic causes
ofSBO.
- intraluminal objects that cause obstruction include
gallstones (mostly in elderly women) which may be
visible on CT and not with plain radiography (Fig.
7.2.6), faecal impaction in patients with cystic fibrosis, bezoar or various ingested bodies which occur
in mentally disturbed or retarded patients and
occasionally lodge in the small bowel rather than
the oesophagus, stomach and colon. The detection
of a small-bowel foreign body or bezoar requires
looking for an underlying obstructive lesion. Intussusception may be considered an intraluminal
cause of SBO, since it obturates the lumen by pushing a proximal small bowelloop and part of its mesentery into the lumen of the small bowel distal to it,
even if various extrinsic or intrinsic processes may
result in intussusception. The typical CT features of
enteroenteric intussusception include (Fig. 7.2.7): a
distended loop ofbowel (the intussuscipiens) with a
thickened wall, an eccentrically positioned intralu-
minal intussusceptum, and a crescent-shaped area

of fat density representing invaginated fat from the
mesentery of the intussusceptum. CT can also demonstrate the cause of the intussusception by showing the lead mass and suggest its nature by its density: fat -containing lipoma, cystic mass from a mucocoele or solid mass. In some cases, CT may show
multiple polypoid tumours which suggest a diagnosis of metastases, especially from malignant melanoma, or Peutz-Jeghers syndrome. However, as
demonstrated in a recent study (WARSHAUER and
LEE 1999) and contrary to the generally accepted
idea, half of adult cases of enteroenteric intussusception are idiopathic.
- intrinsic causes include tumour, inflammatory disease, ischaemia and haematoma. Tumours that are
responsible for SBO by infiltration of the bowel
wall are mainly adenocarcinoma, primary carcinoid and metastases. Adenocarcinoma presents as
an annular infiltrating lesion located in the duodenum or in the proximal jejunum. Conversely,
peritoneal metastases (for instance from melanoma) usually involve the distal small bowel, and
an annular infiltrative lesion in the distal ileum is
more likely to be a metastasis, especially in the setting of a known primary malignancy. Primary carcinoids obstruct the bowel more by desmoplastic
changes than by the tumour itself, which may be
difficult to visualise. SBO consecutive to inflammatory disease is more often due to Crohn's disease. CT shows circumferential thickening of the
Fig. 7.2.6a,b. Gallstone ileus. Abdominal plain film (a) and CT (b). Big stone in a small bowelloop; despite its size, the stone is
not seen on the plain film because it falls on the sacrum bone. Note also the opacification of the colon by oral contrast
292
Fig. 7.2.7. Enteroenteric intussusception on CT
bowel wall, fibrofatty proliferation and abscess in

some cases. Other primary inflammatory causes
of SBO include tuberculosis, Behcet's disease, both
invading the terminal ileum, and ulcerative jejunoileitis complicating celiac disease and occurring in the
proximal jejunum. ehronic mesenteric ischaemia is
responsible for a thickening of the bowel wall, which
may produce a SBO; radiation enteropathy is a form
of ischaemia since radiation-induced small-vessel
occlusions may produce chronic ischaemia anywhere in the alimentary tract. er shows bowel wall
thickening with occasional visualisation of the target
sign. rhe important clue for the diagnosis is that
bowel changes are confined to the radiation port
(RHA et al. 2000). Spontaneous intramural haematoma is most commonly caused by excessive anticoagulation (Fig. 7.2.8). Other aetiologies include coagulopathy, collagen vascular disease and HenochSchnlein purpura. er shows thickening of the
bowel wall occurring mainly in the duodenum and
in the proximal jejunum, with a characteristic ring
pattern ofhigh attenuation on unenhanced slices.
- extrinsic causes are the most common causes of
SBO. Most extrinsic lesions are adhesions, which
constitute about 60% of SBO causes, or hernias.
rhe er diagnosis of adhesion can be difficult because
the diagnosis is based on exclusion. rhe diagnosis is
assumed when the calibre of the bowellumen changes dramatically with no other explanation (Megibow
et al. 1991; Fukuya et al. 1992). rhin slices and for
some authors (eaoili and Paulson 2000) multiplanar
reformations allow the transition point to be viewed
with more confidence and to individualize a beaklike narrowing without any mass at the transition
zone (Fig. 7.2.9).
P. Taourel et al.
Hernias are the second most common cause of

SBO. Approximately 95% of obstructions caused by
hernias are external. External hernias, which include
inguinal, femoral, umbilical, spigelian and incisional
hernias, consist of a peritoneal sac that protrudes
through a weakness or defect in the muscular layers
of the abdomen. rhe diagnosis of external hernias
is based on the clinical examination, and generally
external hernias are treated before occlusive complications. However, obesity can make the clinical diagnosis difficult, and patients may present with a SBO
of unknown origin. Indirect inguinal hernias are by
far the most common cause of hernias. rhis type of
hernia is localized laterally to the inferior epigastric
vessels and anteromedially to the spermatic cords
and may reach the scrotum. Unlike indirect hernias,
direct hernias are found medial to the epigastric vessels and are separated from the spermatic cord by the
transverse fascia (STABILE IANORA et al. 2000). Femoral hernias are far less common than inguinal hernias; they are encountered in women and generally
reach the superior part of the thigh, at the Ievel of
Scarpa's triangle. When they are small, they may be
difficult to distinguish from inguinal hernias. Umbil-
Fig. 7.2.8a,b. Spontaneous jejunal hematoma on CT. Note the

proximal dilatation of the bowelloops and the thickening of
the wall of a jejunalloop located in the pelvis
ical and subumbilical hernias are the second most

common cause of external hernias and are easily diagnosed by er. Obturator hernias constitute a rarer
form of external hernia for which er has contributed
greatly to the diagnosis (YoKOYAMA et al. 1999}.
In comparison to external hernias, internal hernias are uncommon and remain a vexing problern
for er (ZARVAN et al. 1995). Paraduodenal hernias
Fig. 7.2.9. Beak finding on CT. The transition zone between

dilated loops and collapsed loops (arrowheads) is well individualized with a beak finding
293
account for approximately 50% of all internal hernias; they are congenital and result from an abnormality of gut rotation. rhe small bowel is entrapped
between the posterior peritoneum and the mesocolon in a hernia sac (Fig. 7.2.10). Other internal hernias include herniation through the foramen ofWinslow, hernia through the transverse mesocolon which
occurs after gastric surgery, and pericecal, intersigmoid and transmesenteric hernias.
Extrinsic causes of SBO other than adhesions and
hernias include a wide variety of neoplastic, inflammatory and vascular processes. Extrinsic masses
obstruct by two main mechanisms: compression of
the Iumen by the mass and distortion of the lumen
by a desmoplastic process. rhe most common cause
of extrinsic masses is carcinomatosis, most often
from ovarian carcinoma. However, any peritoneally spread process, such as carcinoid desmoplastic
reaction, tuberculous peritonitis, desmoid tumours,
severe radiation darnage or peritoneal endometriosis from the small bowel serosa, may mirnie peritoneal metastases.
In patients with occlusion and fever, the cause of
the occlusion is often an inflammatory process, and
Fig. 7.2.10a- c. Right paraduodenal hernia on CT. The small

bowel loops are entrapped behind the ascending mesocolon.
Note that the majority of entrapped loops have no wall
enhancement (a, c) whereas some loops still have enhanced
walls (b)
294
P. Taourel et al.
nant intestinal obstruction may develop with implanted miliary lesions not seen on CT (HA et al. 1998).
Another difficulty is posed by low-grade obstruction
since the transition zone is not well individualized.
Lastly, we have shown (TAOUREL et al.1995) that there
are some specific causes of difficult diagnosis such
as internal hernias, for which the abnormality of the
location of the herniated bowel is not obvious on CT
slices and which may be mimicked by anatomic variants, or radiation damage, which has no specific sign.
7.2.3.5.3
Accuracy
a
The accuracy of CT in the diagnosis of the cause of

SBO depends on the population studied. It increases in patients with high-grade obstruction and
decreases in a population with a high rate of adhesive bands or in patients with numerous potential
causes of SBO such as those with a past history
of surgery for malignancy. Consequently in published series, the accuracy of CT varies between 70%
and 95o/o (MEGIBOW et al. 1991; FUKUYA et al. 1992;
MAGLINTE et al. 1993; TAOURELet al. 1995). The
added value of multiplanar reformation remains to
be demonstrated ( CAOILI and PA ULSON 2000 ), even
if it provides nice pictures.
b
Fig. 7.2.1la, b. SBO complicating a perforated sigmoid diverticulitis on CT. Agglutination of small bowelloops in contact
with perforated sigmoid diverticulitis. Note extraluminal air
bubble and diverticula (b)
7.2.4
Diagnosis of Complications
of the Obstruction
7.2.4.1
the mechanism can be associated with a paralytic
ileus and a mechanical obstruction through agglutination of the bowelloops in contact with an inflammatory process, which is most often a sigmoid diverticulitis (Fig. 7.2.11) (KIM et al. 1998) or appendicitis.
7.2.3.5.2
Pitfalls
The main difficulty is that the diagnosis of the most
common cause ofSBO (i.e.adhesive bands) is based on
a negative finding, by not being able to see any mass
or other abnormality at the zone of transition; consequemly, as noted by MEGIBOW (1994), this is disquieting in that we are more comfortable diagnosing an
entity that we can see rather than relying on a diagnosis of exclusion. Besides, it is well known that malig-
Strangulation occurs in about 10% of SBO; it represents the main factor of morbidity and mortality
(FEVANG et al. 2000), with a mortality above 10%. It
is characterized by an impaired vascular circulation
to the obstructed intestine. BALTHAZAR et al. (1992;
BALTHAZAR 1994) have very clearly summarized the
mechanisms which lead to a Strangulation:
- The first event is a closed-loop or incarcerated
intestinal obstruction due to adhesions or hernias,
in which a loop of bowel is occluded at two adjacent points along its course. There is a mechanical
obstruction proximal to the involved bowel segment. The length of the closed loop is variable from
a single to severalloops of bowel. If the length of
the closed loop is sufficient (Fig. 7.2.12), the loop
may twist and produce a volvulus. If the length of
295
The clinical diagnosis of Strangulation is difficult.

Intestinal Strangulation is suspected when the intermittent crampypain becomes continuous and increases in severity, and in patients with tachycardia, fever,
peritoneal irritation and leucocytosis. However, these
findings cannot reliably differentiate simple from
strangulated obstruction, which meant that before the
development of CT, Strangulation was not diagnosed
preoperatively in about 75% of patients with surgically
proved Strangulation (BALTHAZAR 1994).
7.2.4.2
Fig. 7.2.12a, b. Closed-loop obstruction involving a long segment ofbowel on US (a) and CT (b). Note the U pattern of the
involved loop clearly shown by US (a)
Findings of Strangulation on abdominal plain film

are as dassie as they are unreliable. They include
the coffee bean sign, the closed loop assuming the
shape of a coffee bean with the doubled width of the
apposed walls resembling the cleft of the bean, and
the pseudotumour sign reflecting a fluid-filled loop
that is fixed and remains in the same position on
multiple projections. In practice, the only potentially
useful finding is the Iack of air and of an air-fluid
Ievel in patients with obvious clinical findings of SBO.
This means obstruction with a fluid-filled bowel,
reflecting a high degree of obstruction, which carries
a high er risk of Strangulation.
7.2.4.3
Enteroclysis
the closed loop is short (for instance in some external hernias), the bowel proximal to the obstacle
may twist. Volvulus is a common but not invariable
complication of incarcerated loop; it tends to occur
in patients with high degrees of obstruction, but
once developed, it further aggravates the mechanical obstructive process and contributes to the development of mesenteric ischaemia.
- The second event is Strangulation, which is defined
as a closed-loop obstruction associated with intestinal ischaemia. The severity and duration of the
intestinal and mesenteric obstructive process determine the severity of the ischaemia. Initially, the
venous return of blood from the involved bowel
segment is compromised, with congestive changes
affecting the bowel wall and the mesentery, while the
influx of arterial blood continues. Ischaemia may
resolve with an emergent surgical treatment of the
cause. Then, arterial insufficiency follows, aggravating the anoxia and further contributing to the rapid
development of gangrene and perforation.
Even if it can identify features of a closed-loop

obstruction while investigating partial obstruction,
enteroclysis is contraindicated in patients with suspected closed-loop obstruction and of course with
suspected Strangulation.
7.2.4.4
Ultrasound
The diagnosis of Strangulation by US is difficult.

Strangulation may be suspected if the following features are present (Fig. 7.2.13): thickened bowel wall,
localised ascites, thickened leaves of the mesentery
and absence of peristalsis. However, the absence of
peristalsis may be seen in an obstruction of long
duration, and thickening of the bowel wall, localised
ascites or thickened leaves of the mesentery may be
due to the cause of the obstruction and not express
a Strangulation. Duplex and colour Doppler sonog-
296
P. Taourel et al.
7.2.4.5.2
Pitfalls
Fig. 7.2.13a, b. Strangulating obstruction, mesenteric finding

on US (a) and CT (b). Infiltration of the mesenteric fat
raphy, which may demonstrate vascular flow signals

in the vessels of the dilated bowel wall, could theoretically play a role in the detection of strangulation.
However, this evaluation remains difficult because
the bowel wall is a very small area (less than 3 mm),
and the increased peristalsis may cause flow artefact
signal (GIMONDO et al. 1995).
7.2.4.5
Computed Tomography
7.2.4.5.1
Findings
rhey must be divided into two categories: findings

indicative of closed-loop obstruction and findings
indicative of Strangulation.
- elosed-loop obstruction is associated (BALTHAZAR
et al.1992, 1997; HA et al. 1993, 1997) with findings of
incarcerated small bowellike radial distribution and
stretched mesenteric vessels converging toward torsion and a U- or e-shaped dilated bowelloop (Fig.
7.2.12), and at the site oftorsion, the presence oftwo
adjacent, collapsed, round, oval or triangular loops,
the beak sign appearing as a fusiform tapering when
the bowel is imaged in longitudinal section, and a
whirl sign meaning a twist of the mesentery.
- Strangulation is associated (BALTHAZAR et al. 1997;
HA et al. 1997; DONCKIER et al. 1998) with bowel
wall abnormalities like circumferential thickening, increased attenuation, target or halo sign, or in
contrast a Iack of enhancement of the wall of the
incarcerated bowel after intravenous administration of contrast (Fig. 7.2.14) and mesentery abnormalities (Fig. 7.2.13) with blurring, haziness, or
obliteration of the mesenteric vessels, and fluid or
haemorrhage in the mesentery.
rhe main difficulty in the diagnosis of Strangulation

is due to the fact that there is no finding with both
high specificity and sensitivity. rhe most specific
findings of Strangulation are the lack of enhancement of the bowel wall and a diffuse haziness of the
mesentery, but they have sensitivities of about 30 and
50%, respectively (HA et al. 1997). eonsequently, the
diagnosis of Strangulation must be evoked on a
combination of findings. However, even then, strangulation may not be identified in 15%-20% of
patients with strangulated obstruction. eonsequently, as stated by BALTHAZAR et al. (1997), obvious
discrepancies between er and clinical findings in
patients in whom small bowel obstruction and mesenteric infarction are suspected should Iead to exploratory laparotomy.
7.2.4.5.3
Accuracy
By using a combination of findings, HA et al. (1997)

and BALTHAZAR et al. (1997) have found a sensitivity of about 80% and a specificity of about 90% for
the diagnosis of strangulating obstruction. However,
it must be stressed that the results of allsturlies evaluating the efficacy of er in Strangulation are flawed
because of the interval time between er and surgery
since an episode of Strangulation may develop at any
time during obstruction.
Fig. 7.2.14. Strangulating obstruction, bowel wall finding on

CT. Localized Iack of enhancement of the bowel wall (arrow)
297
7.2.5
Diagnostic Strategy
In patients with suspected intestinal obstruction, the

first diagnostic triage is based on clinical, laboratory
and abdominal plain film findings, which allow us to
distinguish schematically four situations (Fig. 7.2.15).
- There is a strong suspicion of paralytic ileus. The
cause of this ileus must be investigated by clinical
and laboratory examinations, and in some cases
byUS or CT.
There is a strong suspicion of a SBO: if there are
findings of Strangulation or if the cause of the SBO
is obvious and needs emergent surgical management, surgery must be performed without waiting for other investigations. In other patients with
acute symptoms, CT must be used to look for
the mechanism and the cause of the occlusion.
In patients with non-acute symptoms (suspicion
of low-grade obstruction), enteroclysis is a good
alternative to CT and should be performed first.
There is a strong suspicion of a large bowel
obstruction (LBO): if the abdominal plain film
shows signs of volvulus, more commonly on the
sigmoid colon than on the cecum, a treatment of
the volvulus must be performed (colonoscopic or
surgical detorsion in sigmoid volvulus, surgery in
cecal volvulus) ; if there is no finding of volvulus,
a stenosis is assumed to be the cause of the LBO,
and CT must be performed to look for the cause
of the stenosis if there are inflammatory findings.
In the absence of inflammatory findings, CT or
contrast enema may be used to search for a colic

tumour responsible for the obstruction.
- There are some doubts between an obstruction
and an ileus or some doubts about the site of an
obstruction, in the small or in the large bowel. CT
should be performed to investigate the nature of
the occlusion, the site of an obstruction, its cause,
and eventual signs of Strangulation.
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Donckier V, Closset J, Van Gansbeke D, Zalcman M, Sy M,

Houben JJ, Larnbilliote JP (1998) Contribution of computed
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Clinical Exam + Plain ftlm abdominal
Sm>~
Ileus
'"'1oom
/~
j j
- suspicion of strangulation Iow grade SBO other cases
the cause:
cause of
obvious treatment
- surgical
- clinical exam
(strangulated
- laboratory
external hernia)
- eventually US CT
surgery
~--------------100~\
l
Doubt
Ileus I mechanichal obstruction
SBO/LBO
colonoscopic
or surgical
detorsion
enteroclysis
CT
presumed
stenosis
presumed
volvulus
CT
/~
inflammatory
findings
no inflammatory
finding
CT or contrast enema
CT
CT if enteroclosys
not informative
Fig. 7.2.15. Algorithm for the diagnostic triage of patients with suspected intestinal obstruction
298
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(1994) CT of small bowel obstruction; value in establishing
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Fukuya T, Hawes DR, Lu CC, Chang PJ, Barloon TJ (1992)
CT diagnosis of small bowel obstruction: efficacy in 60
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Gaines PA, Sanders AJJ, Drake D (1987) Mitgut malrotation
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Gimondo P, LaBella A, Mir KP, Torsoli A (1995) Duplex-doppler
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Ha HK, Park CH, Kim SK, Chun CS, Kim IC, Lee HK, Shinn KS,
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Ha HK, Kim JS, Lee MS, Lee HJ, Jeong YK, Kim PN, Lee
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7.3 Radiology of Crohn's Disease

J. W. A. J. REEDERS and L. E. DERCHI
CONTENTS
7.3.1
7.3.2
7.3.3
7.3.3.1
7.3.3.2
7.3.3.3
7.3.3.4
7.3.4
7.3.4.1
7.3.4.2
7.3.5
7.3.5.1
7.3.5.2
7.3.5.3
7.3.5.4
7.3.6
7.3.7
7.3.8
7.3.9
7.3.10
Introduction 299
Clinical Findings/Symptoms 300
Systemic Extraintestinal Complications 300
Hepatobiliary Complications 302
Pancreatitis 302
Genitourinary Tract Complications 302
Musculoskeletal Complications 302
Morphology 302
Gross Pathology 302
Histopathology 304
Contrast Studies 305
Enteroclysis (Smali-Bowel Enema) 311
Small-Bowel Follow-Through (Peroral or Tubeless
Enterography) 312
The Additional Pneumocolon 313
SBE vs SBFT in Crohn's Disease 314
Ultrasonography 316
Spiral CT Enterography 327
Magnetic Resonance Imaging 328
Nuclear Medicine 332
References 332
7.3.1
lntroduction
Crohn's disease is an idiopathic, chronic, transmural, inflammatory/ulcerative disease of the gastrointestinal tract, affecting particularly the terminal
ileum and characterized by acute exacerbation and
remission. Ulcerative colitis and Crohn's colitis
comprise 90o/o of all cases of chronic inflammatory
bowel disease and are the most important considerations in the differential diagnosis. Both diseases
J. w. A. J. REEDERS, MD, PhD

Department of Radiology, St. Elisabeth Hospital, Cura~ao,
Netherlands Antilies
L. E. DER CHI, MD
Professor, Department of Radiology, University of Genoa,
Genoa, Italy
are idiopathic since neither their etiology nor their

pathogenesis is completely understood. Each condition is associated with a rather specific but overlapping constellation of clinical, pathologic, endoscopic, and radiographic findings. Socioeconomic
factors do not appear to contribute to the epidemiology or etiology of either condition. Increased
familial occurrence is found in both conditions,
with a range of from 0.6o/o to 16o/o for ulcerative
colitis and approximately 9o/o for Crohn's disease.
Historically, the diagnostic features of Crohn's disease of the small intestine have been delineated by
barium studies, or less frequently by arteriography,
and in the last decade by enteroscopy, ileoscopy,
ultrasound, computed tomography (CT), and magnetic resonance imaging (MRI) (CROHN et al. 1932;
MARSHAKet al. 1963; OIJSON and REUTER 1966;
LUNDERQUIST et al. 1967; BRAHME and LINDSTROM
1970; HERLING ER 1972, 1978; MEYERS 1976; FRAGER
et al. 1983; GOLDBERGet al. 1983; GORE 1989; GORE
et el. 1996; MEYERS and McGUIRE 1995; HALLIGAN
et al. 1998). Ileoscopy and uhrasound play an established role in the evaluation of patients with inflammatory disorders of the terminal ileum.
The indications for diagnostic evaluation of inflammatory bowel disease include:
- determination of the extent and/ or grade of activity
- to rule out cancer or in follow-up after surgery for
cancer
- differentiation from other inflammatory diseases
Detecting these processes by visualizing the full
extent of the patho-anatomic changes is the primary goal of the radiographic examination. Thorough small and large bowel preparation and a good
(double) contrast technique are mandatory, as is an
adequate contrast solution.
Recognizing and distinguishing both conditions
is of therapeutic and prognostic consequence.
Although Crohn's disease is the inflammatory disease most frequently identified by endoscopy or
radiology, underlying infections or identifiable
causes of ileocolitis should be excluded.
J. W. A. J. Reeders and L. E. Derchi
300
7.3.2
Clinical Findings/Symptoms
7.3.3
Systemic Extraintestinal Complications
Four individual stages can be recognized in Crohn's

disease (Fig. 7.3.1):
Early stage
Ulcerative stage (progressive phase)
Recoverystage (proliferative phase)
Advanced stage
Extraintestinal complications develop in 25% of

patients with infl.ammatory bowel disease (IBD).
These complications can be divided into three categories (GORE et al. 1996, LEVINE and LUKAWSKITRUBISH 1995):
- those that are dosely related to the activity or
extent of the disease and that are responsive to
therapy directed at the bowel disease (e.g., arthritis or iritis)
- those whose course is independent of the severity
of the underlying bowel disease (e.g., sderosing
cholangitis or ankylosing spondylitis)
- those that result from inadequate or disordered
intestinal function (e.g., cholelithiasis or nephrolithiasis).
Differentstages of the disease may be present simultaneously in separate segments of the small bowel.
Diarrhea without bleeding is the most common
dinical presentation, found in 66%-90% of cases.
The presence ofblood, pus, or mucus in the stool is
atypical. Occult blood may be seen in up to SO% of
patients. Gradual, progressive development of epigastric or right lower quadrantabdominal pain may
be found in 45%-95% of patients. Fever, anemia,
anorexia, weight loss, nausea, and vomiting are frequently found.
The different extraintestinal manifestations of Crohn's

disease are summarized in Table 7.3.2.
Table 7.3.2. Extra-intestinal manifestations of Crohn's disease (after Reedersand Rosenbusch 1994)
Manifestation
Frequency
Skin:
Erythema nodosum
Pyoderma gangrenosum
1.4o/o
0.16%-l.So/o
Erythema multiforme
Scleroderma
Urticaria
Dermatitis
Exanthema
Fistulas
Psoriasis
Oral mucosa:
Aphthous stomatitis
Ocular:
Conjunctivitis
Iritis
Episcleritis
Uveitis
Corneal ulcers
Keratitis
Retinopathy
Hepatobiliary system:
Fatty infiltration of the liver
Pericholangitis
Cirrhosis
Chronic active hepatitis
Sclerosing cholangitis
Cholangiocarcinoma
Granulomatous hepatitis
Cholelithiasis
Heart:
Perkarditis
Rarely
Rarely
Rarely
Rarely
Rarely
Often
Rarely
Relatively often
Less often
73o/o
<30o/o
2o/o-So/o
Rarely
Rarely
Rarely
Rarely
1Oo/o-SOo/o
Rarely
Manifestation
Lung:
Angiitis
Fibrosing alveolitis
Apical pulmonary fibrosis
Bronchitis
Skeletal system:
Arthralgia
Arthritis
Hypertrophie osteoarthropathy
Sacroiliitis
Osteonecrosis
Genetically associated diseases
Ankylosing spondylitis
Sacroiliitis
Genitourinary tract:
Pyelonephritis
Nephrolithiasis
Amyloidosis (secondary)
Obstructive hydronephrosis
Other:
Clubhing of fingers
Mental retardation in children
and adolescents
Thromboembolism
Multiple sderosis
Malabsorption of fat and vitamin B-12
Myositis
Pancreatitis
Retroperitoneal!psoas abscess
Frequency
3o/o-22o/o
3o/o-22o/o
Rarely
1Oo/o-30o/o
Rarely
3o/o-12.6o/o
18o/o
Rarely
2o/o-10o/o
Rarely
3o/o-7o/o
40o/o-60o/o
Often
Often
Rarely
3o/o-12o/o
Rarely
1o/o-2o/o
Often
301
Radiology of Crohn's Disease
I Crohn's Intestinal Disease
I Stages
IBariumstudies
lneoscopy
Earlystage
Active disease
Preaphthous phase:
Patehy erythema; mueosa intact, but with

foeal edema/intramueosal bleeding
Disturbed mueosal vaseular pattern
Finely nodular mueosa (lymphoid
hyperplasia)
Pathologie regions alternate with normal
1- segments
1-
Aphthous phase:
Seattered ring-shaped, relatively flat

protuberanees with eentral punetate
mueosal defect (aphtoid ulcer <5 mm),
surrounded by normal mueosa
r
Regression
(healing)
Ulcerative
stage
(progressive
phase)
Recovery
stage
(proliferative
phase)
Reversible
Recurrence
during
remission
Preaphthous phase:
Nodular lymphoid hyperplasia (fine,

uniform nodular pattern)
Thickening of the intestinal wall and
semilunar folds (edema)
Prominent innominate line
Aphthous phase:
Aphthoid uleers, seen as punctate

eolleetions of barium with halo (edema),
surrounded by normal mueosa
("dot-halo" or "bull's-eye" sign)
Villous abnormality (granularity)
Spasm
Preserved clistensibility of involved
intestinal wall
Uicerations ofvarying size and depth,

large, eoalescing, deep, linear, longituditypieally linear, oeeasionally serpiginous,
nally and to a lesser degree transversely
eoursing predominantly longitudinally
eoursing, irregular serpiginous ulceration
1- and transition to neighboring normal or 1- at the mesenterie margin
edematous, mounded mueosa
lrregular, nodular eontour of the
("eobblestone" pattern)
intestinal wall
Formation of fissures
Thiekening of the intestinal wall
Coarsely nodular ehanges of the wall

("eobblestone" pattern and/or
pseudopolyps)
Postinflammatory pseudopolyps (foeal;
<1.5 em); some with mueosal bridging
1- Solitary giant polyps
Multiform, deep linear, or serpiginous
eonfluent ulcerations
Thiekening of the interhaustral folds
(fibrosis, sear formation)
1-
Mesenteric border rigidity

Coarsely nodular ehanges of the wall
("eobblestone" pattern)
Postinflammatory pseudopolyps
(foeal; >1.5 em); some with
mueosal bridging
Solitary giant polyps
Deep linear or serpiginous eonfluent
ulcerations, "eollar-button" uleerations
Sealloping of the eontraetile
mesenterie border
Irreversible [
,
Advanced
stage
Characteristic changes
of the intestines
Varying degrees of severity;

disproportional, abrupt t ransitions
to uninvolved tissue
Polymorphie
Segmental (foeal or pate hy)
Asymmetrie, diseontinuo us;
"skip lesions" in 30%
Eeeentric, multieentrie, iso lated
Transmural
Remissionsand exaeerbation
Complications
r
Asymmetrie, irregular, or tubular
strietures (fibrosis) with extensive
inflammatory ehanges (asymmetrie
uleerations)
Coarsely nodular eontour ehanges
("eobblestone" pattern and/or
pseudopolyps)
1- Mueosa of strietures may be
edematous, erythematous, vulnerable
and uleerated; may also be normal
loss of haustration
Saeeulations (false divertieula)
Terminal ileum: extensive asymmetric
uleerations in the area of the ileoeeeal
valve, which may be stenosed
r
Asymmetrie, irregular, tubular strietures
(fibrosis) with or without uleerations
Coarsely nodular eontour ("eobblestone"
pattern and/or pseudopolyps)
Sinustraets/fistula formation
Fixation of eolon and terminal ileum
Saeeulations (false diverticula)
1- Coneave impression on the medial wall
of eeeum due to inflamed terminal ileum
Marked intestinal wall thiekening
longitudinal shortening of the intestines
Segmental or tubular strietures

Interna! fistula: (20-35%)
ileoreetal/sigmoid, ileoeeeal, eolovesieal,
rectovaginal
External fistulas (10-20%) in region
of laparotomy sears; perianal fistulas
(2.5-80%)
1- Fissures
1Vitamin B12 defieieney
Protein loss, abdominal abseesses,
indurations, psoas abseesses
Retroperitoneal fibrosis
Perforation (rare)
Systemie manifestations
Segmental or tubular strictures

Coneave impression on the medial wall
of eeeum due to inflamed terminal ileum
Fistulas (ileoreetal/sigmoid, ileoeecal,
eolovesieal, reetovaginal, perianal
Paraeolie abseesses, perforation
Fig. 7.3.1. Crohn's Intestinal Disease: Stages; findings in ileoscopy and barium sturlies (modified from REEDERS and ROSENBUSCH, 1994)
302
7.3.3.1
Hepatobiliary Complications
The liver and biliary tract are the most frequent sites for
serious complications of extra-intestinal IBD, which do
not correlate with disease activity, duration, or severity,
with the exception of fatty infiltration of the liver. Most
of these complications (cholelithiasis, choledocholithiasis, pericholangitis) can be detected with ultrasound
and!or CT. Hepatic abscesses may occur as the initial
manifestations of Crohn's disease and may be induced
by steroid and immunosuppressive agents, perforations, intra-abdominal abscesses, and anastomotic
leaks. Ultrasound and CT are the premier modalities to
diagnose hepatic abscesses and to guide the percutaneous drainage of suitable collections (GORE et al. 1996).
Septic arthritis of the hip can complicate a psoas

muscle abscess. MRI and CT show these changes
before they can be recognized on plain films. A right
psoas muscle abscess may develop secondary to terminal ileal disease, and a left psoas muscle abscess
can result from sigmoid or jejunal involvement.
Although most patients with psoas muscle abscesses have well established Crohn's disease, it may be
the initial presentation of the disease. CT is the best
technique for the diagnosis and percutaneous management of psoas muscle abscesses (AGHA et al. 1985;
RICCI and MEYER 1985; GORE et al. 1996) (Fig. 7.3.2).
7.3.4
Morphology
7.3.3.2
7.3.4.1
Pancreatitis
Gross Pathology
About 1%-2% of patients with Crohn's disease will

develop pancreatitis. Regardless of the cause (drugs,
choledocholithiasis, fistula, or auto-antibodies against
pancreatic acinar cells), ultrasound and/or CT/MRI
are needed to help confirm the diagnosis of pancreatitis and its complications (GoRE et al. 1996).
In Crohn's disease, different intestinal changes may

be present simultaneously. In the early phase (preaphthous phase), the initial changes are considered to
occur in the mucosallymphoid tissue, in which morphologic abnormality is revealed as aphthous lesions:
scattered, ring-shaped, relatively flat protuberances
with central punctate mucosal defects (<5 mm), surrounded by normal mucosa (aphthous phase) (Fig.
7.3.3). (WATIER et al. 1980; TTO and GEBBERS 1981;
MoRSON and DAWSON 1990; HIZAWA et al. 1994,
1996). Recently, even tinier aphthous lesions have
been reported with magnified endoscopy (MAKIYAMA et al. 1984) or stereomicroscopy (PouLSEN et al.
7.3.3.3
Genitourinary Tract Complications
Between 2% and 10% of patients with Crohn's disease

may develop nephrolithiasis attributable to water and
electrolyte Iosses from diarrhea, malabsorption, and
high ileostomy Output (BANNER 1987; MERINE et al.
1989; GoRE et al. 1996), or obstructive hydronephrosis, due to calculous disease, obstruction due to the
inflammatory effect of an abscess, phlegmon, or the
mass effect (creeping fat) of the mesentery encroaching on the ureter (GORE et al. 1996). Both can be diagnosed easily by uhrasound or CT.
1984).
7.3.3.4
Musculoskeletal Complications
Arthralgia or arthritis (peripheral arthritis, sacroiilitisspondylitis) can be seen in 3%-22% of patients with
Crohn's disease. The radiologic findings can best be
described as usually symmetric joint narrowing with
osseous erosions and sclerosis, more pronounced on
the iliac side of the articulation (Go REet al. 1996).
Fig. 7.3.2. Crohn's disease: multilocular extraperitoneal abscess

(A) among the posteromedial aspect of the right iliopsoas
muscle. Note: transmural thickening (arrow) of an ileal1oop
303
Fig. 7.3.3A. Enteroclysis (SBE): early lesions of Crohn's ileitis

are manifested: scattered, ring-shaped mucosal defects with
central puncta (aphthoid lesions) at the terminal ileum. B Ileoscopy image shows aphthous lesions scattered through the terminal ileum, revealed as tiny erosions with a small red halo
The appearance of only aphthous erosions or

ulcers at radiography is not diagnostic for Crohn's
disease (HAMILTON and MORSON 1985).
The difficulty of differentiating early Crohn's disease from extensive lymphoid hyperplasia (Fig. 7.3.4)
and infectious ileitis (Beh<;et disease or infection with
Yersinia (Fig. 7.3.5), Entamoeba histolytica, Salmonella, Shigella, and the herpes virus) (HrzAWA et al.
1996) is an acknowledged clinical problern (EKBERG
et al. 1984). Therefore, HIZAWA et al. (1996) recommend that if aphthous lesions are encountered,
efforts need to be made to verify the presence of
granulomas in biopsy specimens, especially in those
taken from the terminal ileum.
In patients with overt Crohn's disease, changes in
aphthous lesions are considered to be unpredictable
(JoFFE 1980; Nr and GoLDBERG 1986) and to occur
independently of the disease activity (MoniGLIANI et
al. 1990; KADA et al.1991}.
In the ulcerative stage (progressive phase) of the
disease, large, coalescing, deep, linear, longitudinal,
and to a lesser degree transversally coursing, irregular, serpiginous ulcers can be found (Fig. 7.3.6). The
intestinal wall tends to be irregular, due to 'cobble-
Fig. 7.3.4. SBE: lymphoid hyperplasia; multiple thickened

irregular nodular folds at the terminal ileum, mimicking
Crohn's ileitis
304
Fig. 7.3.5. SBE: Yersinia ileitis: irregularities of the mucosal

margin with distortion of the fold pattern of the terminal
ileum, mimicking Crohn's ileitis
stone formation'. The bowel wall is thickened due to

fibrosis and/or edema.
In the recovery stage (proliferative phase), the
changes in the intestinal wall are coarsely nodular
cobblestone pattern (Fig. 7.3.7). Post-inftammatory Fig. 7.3.6. SBE. Ulcerative stage of Crohn's ileitis: !arge, coalescpseudopolyps (focal >1.5 cm) can be found (Fig. ing, deep, linear, longitudinal, and to a lesser degree transversally coursing, irregular, serpiginous ulcers at the terminal
7.3.8), some with mucosal bridging. Solitary giant
ileum
polyps have been described, causing small-intestinal
intussusception (KoRMAN et al. 2000). Most obvious
are deep, linear, or serpiginous conftuent ulcerations
('collar button' ulcers), thickening of valvulae conniThe grading manifestations of Crohn's disease of
ventes, and tubular narrowing.
the small intestine are summarized in Fig. 7.3.18.
In the advanced stage, asymmetric, irregular, tubular strictures (due to fibrosis) (Fig. 7.3.9) can be
found with or without ulceration. The intestinal wall 7.3.4.2
shows a coarsely nodular contour (cobblestone pat- Histopathology
tern and/or pseudo-polyps), fixation of the terminal
ileum, sacculations (false diverticula) (Fig. 7.3.10), a Mucosal bleeding, focal crypt abscesses, and destrucconcave impression on the medial wall of the cecum tion of crypt epithelium can be found. At times, there
due to the infiamed terminal ileum.
is complete destruction of crypts and the surrounding
Wall thickening, longitudinal shortening and nar- epithelium in regions of former inftammation.
rowing of the terminal ileum are common findings.
Small, non-caseating epitheloid-cell granulomas with
A diverse spectrum of ( entero-colic, entero-entero, or without giant cells of the Langhans type (SOo/o-87%)
entero-vesical, entero-sigmoidal and entero-vaginal) are common findings (Fig. 7.3.19). Focal aggregates of
fistulae can be found (Figs. 7.3.11 - 7.3.17).
lymphocytes with or without germinal centers at the
305
Fig. 7.3.7A-D. SBE (A) ileoscopy (B). Recoverystage of Crohn's

ileitis: cobblestone formation at the terminal ileum, with Separation of bowel loops due to transmural wall thickening,
easily picked up with ultrasonography (C, D) (longitudinal/
transverse view)
mucosa/submucosal interface can be seen. Submucosal

tissue may be seen in the connective tissue of the muscularis propria and beneath the serosal surface.
Transmural infl.ammation with fissures are
common (Fig. 7.3.20). The infl.ammatory infiltration
is often disproportionate, i.e., more marked in the
submucosa than in the mucosa. Fibrotic strictures
with deep ulcerations and fissures into the submucosa may be a late finding.
7.3.5
Contrast Studies
Despite advances in enteroscopy and ileoscopy and
more extensive applications of the new imaging
modalities, i.e., ultrasonography, CT, and MRI, which
prove particularly useful for the investigation of the
intestinal wall thickness, the mesentery and the main
intestinal vasculature, contrast radiography remains
306
Fig. 7.3.8A,B. SBE (A) and additional pneumocolon (B): multiple post-infiammatory pseudo-polyps scattered through the
neo-ileum as late manifestation (recovery stage) of recurrent
Crohn's disease at the ileotransversostomy site
Fig. 7.3.9. SBE. Advanced stage of Crohn's ileitis: asymmetric,

irregular, tubular stricture with prestenotic dilatation at the
terminal ileum after forced infusion
307
B
Fig. 7.3.10A,B. SBE (A): an additional pneumocolon (B). Marked sacculation (false diverticula) of the anti-mesenteric side of
a long, segmental, tubular stricture of the terminal ileum. Note: the impression on the medial wall of the cecum is due to the
transmural infiammation
Fig. 7.3.11. Advanced stage of Crohn's disease. Manifestations
of stenosis are recognized because of prestenotic dilatation

and Iack of distensibility during infusion of cantrast medium.
This differentiates strictures from spasms, which open up
during forced infusion. Scalloping of the anti-mesenteric
border is evident
308
]. W. A. J. Reeders and L. E. Derchi
Fig. 7.3.12. SBE: short segmental stricture at the proximal

ileum with sharp demarcation towards the normal proximal
and distal small bowel mucosa, during forced infusion
Fig. 7.3.13A,B. SBE (A): multiple, tubular, stenosed segments

with acute exacerbation of Crohn's intestinal disease. Full
spectrum of large, coalescing, serpiginous, and deeply penetrating ulcerations and cobblestones can be seen as manifestation of partly ulcerative, partly recovery stage. Macroscopy
(B) shows a sharp demarcation between diseased and normal
mucosa
Fig. 7.3.14. Advanced stage of Crohn's disease of the midileum; multiple, short and long segmental stenoses are seen
with intermittent extreme dilatation of the intestine after
forced infusion (infusion rate 150 cc/min)
Fig. 7.3.15. Oral pneumocolon: multiple, short, segmental

strictures at the terminal ileum with fistulous tracts between
the distal narrowed terminal ileum and mid-transverse colon.
Note: longitudinal indentation of the transverse colon due to
a !arge extraluminal inflammatory mass
309
Fig. 7.3.16. SBE with tube compression shows a multi-fistulous

complex with Separation of the bowelloops and extensive disease of the angulated and narrowed terminal ileum
Fig. 7.3.17. SBE with additional pneumocolon shows a colonicduodenal fistula due to long-standing Crohn's colonic disease.
Note: severe narrowing of the ascending colon at the site of
Bauhin's valve
310
Fig. 7.3.18. Radiologie classification of severity of Crohn's disease of the small intestine. Composite drawing of grading
manifestations. In this classification system, early lesions (1)
are manifested by aphthous ulcerations or villous abnormality
(granularity of the villi) and mild fold thickening. Spasm is
noted fluoroscopically, and the involved intestinal wall shows
preserved distensibility. Increased intraluminal fluid may be
present in the segment immediately proximal to the lesion.
Intermediate (ulcero-proliferative) lesions (2) are characterized by a nodular pattern and by ulcerations and mesenteric
border rigidity with scalloping of the contractile antimesenteric border. Ulcerations are present mostly in the mesenteric
margin. The bowel wall is moderately thickened, and the mesentery may be involved. Advanced lesions (3) are manifested
by an ulcero-nodular pattern in a stiff segment. Stricture formation, deeper ulcers, and sinus tract or fistula formation
indicate advanced stage of the disease. Involvement of the
mesentery and marked thickening of the bowel wall are additional findings ( after ENGELHOLMet al. 1989).
the primary and often the only method for the anatomical investigation of small-bowel Crohn's disease.
More than half of the patients with Crohn's disease have evidence of disease in their distal ileum,
and approximately 25o/o of the patients have disease
restricted to the distal ileum only (GOLDBERG et al.
1979; PODOLSKY 1991; BERNSTEIN et al. 1997). At
present, the mid and distal small bowel is the area
of the gastrointestinal (GI) tract that is not evaluable
with routine endoscopy.
In the past years, changes have altered the order
of priority in the conditions for which an antegrade
small-bowel examination was advocated. However,
the most common indications for small-bowel examination remain the diagnosis of clinically suspected
Crohn's disease and the follow-up of patients with
documented small-bowel and/or colonic Crohn's disease or with suspicion of recurrence after surgery.
For these indications, the sensitivity of the smallbowel studies is high, reaching 93o/o in one series
Fig. 7.3.19. Microscopy, Crohn's disease: numerous macrophages form granulomas with giant cells (arrow)
Fig. 7.3.20. Microscopy: Crohn's disease: characteristic fissure

like ulcerations in the presence of transmural inflammation
(DINER et al. 1984; TT et al. 1985), and its overall

accuracy is well established (NOLAN and GouRTSOYIANNIS 1980; HERLING ER 1982; PRINGOT and BODART
1983; EKBERG 1984).
311
7.3.5.1
Enteroclysis (Smaii-Bowel Enema)
Enteroclysis or small-bowel enema (SBE) relies on

the infusion of barium into the small bowel via a
distal duodenal or jejunal tube, so that the opacification of the small bowel is completed in a short period
of time and combined with an optimal distention
of the loops. The procedure, initially designed as a
single contrast barium study, was proposed by SELLINK in 1983 as a standard method for investigating
the small bowel. The barium suspension used has
a low concentration, usually between 15% and 30%
weight/volume, to facilitate the examination of the
small intestine in the distended condition. The contrast is infused by gravity or via an infusion pump at
a rate of 75-100 ml per minute which is optimal - in
the absence of intestinal hypermotility - to obtain
a distention of the loops while maintaining sufficient
propelling motility in the intestine (OuoKERK 1980).
The flow of barium is fluoroscopically monitored
throughout the examination, and every segment of the
small bowel is studied by fluoroscopy and compres- Fig. 7.3.21. SBE: with forced infusion, extreme saccular dilsion radiography (MAGLINTE and HERLINGER 1984; atation is noted, delineating the short segmental, significant
Crohn's stenosis weil
GELFLAND 1986). Cold barium, metoclopramide, and
Gastrografin added to the barium suspension are used
to quicken the transit time and to avoid pooling of
the barium in the ileum and the consequently delayed
opacification of the terminal ileum (MAGLINTE and
HERLINGER 1984). Balloon catheters have been used
to reduce the amount and incidence of duodeno-gastric reflux during the barium infusion (MAGLINTE
1984; CHABOUIS and BLOCH 1986). The distention of
the small bowel during enteroclysis causes a greater
overlap of the loops, making separation of the individual loops for detailed compression radiography
more difficult and in some cases impossible in the
lower abdomen and pelvis. Water infusion or air
insufflation (Figs. 7.3.21 and 7.3.22) at the end of
the barium infusion as well as bariumfair or barium/
methylcellulose double-contrast small-bowel enema
are used to overcome this technical problem. Doublecontrast sturlies are found to improve the morphological demonstration of the ileum (CLEMENT et al. Fig. 7.3.22. SBE: by forced automatic infusion, sharp demarca1977; SCHMUTZ et al. 1982; TAVERNE and VAN DER tion of a significant Crohn's stricture can be seen at the proxiJAGT 1985) and to reduce the occurrence of false-neg- mal ileum
ative studies (SCHMUTZet al.1981).
The disadvantages of enteroclysis are related to
intubation, which may be difficult and is never instantaneous. Intubation in inexperienced hands may take ly, which means a higher radiation exposure for the
up to 15 min or Ionger (MAGLINTE and HERLINGER patient and the radiologist. Finally, intubation and
1984). The passage of the tube from the stomach into catheter irritation during the infusion of contrast are
the duodenum needs tobe monitored fluoroscopical- the major causes of discomfort for the patient. In
312
most patients, the transnasal instead of the peroral

route reduces the discomfort associated with the procedure (EKBERG 1984).
In the evaluation of patients with suspected
Crohn's disease of the small bowel, enteroclysis (SBE)
provides the clinicians with a sensitive method of
diagnosing the disease and a reliable method to
exclude the disease even in its early stage and allows
the diagnosis of other entities with symptoms that
can mirnie those of Crohn's disease of the small bowel
(NOLAN and GOURTSOYIANNIS 1980; MAGLINTE et
al. 1992). Therefore, SBE has proven tobe an important diagnostic tool in the work-up of patients with
suspected Crohn's disease of the small bowel. At
our institutions, uhrasound and SBE are the primary radiologic methods for examination of the small
bowel.
7.3.5.2
Smaii-Bowel Follow-Through (Peroral or
Tubeless Enterography)
Small-bowelfollow-through (SBFT) examinations are

routine in many radiological departments. Criticism
has been expressed toward this so-called conventional method which often relies too much on serial overhead radiographs instead ofbeing monitored fluoroscopically with the necessarily complementary compression radiographs (GuRIAN et al. 1982; FRASER
and PRESTON 1983). In addition, it is argued that
this method fails to distend the intestinal lumen
adequately and may consequently overlook Crohn's
strictures. Furthermore, the overlapping loops of the
small bowel may obscure disease, particularly when
it is located in loops clumped in the pelvis. Finally, the
examination is time-consuming (90% under 3 h) at
least for the patient. Careful analysis of the diagnostic
errors recorded in the small bowel studies with the
conventional method has shown that missed lesions
are mainly located in the ileum. The reasons for the
deficiency of the examination are mostly technical,
namely due to the failure to obtain adequate compression radiographs demonstrating individual segments of small bowel free from overlap, poor fluoroscopic monitoring of the barium flow through the
small bowel, and to the failure to perform the peroral
pneumocolon examination (MAGLINTE et al. 1982).
Improvement of the technique would result in achieving a detailed small-bowel examination with the peroral method.
Tubeless enterography is a detailed peroral follow-through technique. It relies on the intake by the

patient of large quantities of contrast material and
actively involves the radiologist for the fluoroscopic
and radiographic checks timed during the examination. Only minimal preparation of the patient is
required. The day before the procedure, the patient is
put on a low residue diet and a high fluid intake. The
patient is given a light dinner early in the evening
and no fluid after midnight. Whenever possible, all
medications are discontinued, in particular atonyinducing drugs like anticholinergics, tranquilizers,
and narcotics. Colon cleansing does not decrease the
transit time to the cecum and does not affect the
examination quality (GARVEY et al. 1985). However,
Iaxatives - for example 2-4 tablets of Dulcolax - are
useful in chronically constipated patients to empty
the colon. On the day of the examination, the patient
remains in a fasting state, takes no fluid, and refrains
from smoking, which is believed to increase gastric
secretion. The patient is asked to void his bladder
before entering the X-ray room. A low concentration
barium suspension is used. This eases the demonstration of the mucosal fold pattern and, in most
cases, permits visualization through the superimposed (inflamed) small bowelloops. The amount of
barium administered in an individual patient is variable, depending on the transit time. It varies from 650
ml to more than 1 L.
A detailed examination of the small bowel requires
a high standard of radiographic technique to achieve
adequate visualization of all segments. This can be
achieved by meticulous fluoroscopy, variation in the
positioning of the patient, compression studies, and
possibly special views. The survey views are usually
done for geometrical reasons with the overhead X-ray
tube and the patient in the prone position.
Fluoroscopy and spot filming are performed with
the patient lying supine and - if necessary - prone.
This is more favorable for the separation of the
ilealloops lying in the pelvis, which is important in
Crohn's disease.
For SBE as for SBFT, compression greatly increases the accuracy of the examination by separating the
(inflamed) superimposed loops, and performing a
more precise morphological study of an individual
loop (Figs. 7.3.23 and 7.3.24); it also greatly facilitates
the location and demonstration of the Crohn's lesions
in the terminal ileum. Compression in prone position
with the paddle associated with a head-down tilt of
the X-ray table will lift ileal loops_ out of the pelvis
and uncoil them. However, in some slender patients,
the distalsmall bowelloops in Crohn's disease clump
together in the pelvis and are inaccessible to palpation.
Maneuvers can be used to move these loops out of the
313
Fig. 7.3.23. SBE: zoo angled compression view shows a marked

smooth compression of the inflamed intestinalloop due to an
large extraintestinal mass in Crohn's disease
fluid or air. Angled views of the distalsmall bowel are

obtained with the patient in the prone position and the
X-raytube angled 35-45 towards the feet.
YuE and JaNES (1993) found that a prone-angle
caudad view with suprapubic compression may be
especially valuable in separating overlapping barium-filled loops in the pelvic area andin delineating
the terminal ileum and diseased small bowel. With
this technique rather than with the techniques of
pneumocolon or barium enema examination with
reflux in an attempt to visualize the terminal ileum,
the radiation to these usually young patients can be
diminished (YUE and JaNES 1993).
Radiologists performing detailed sturlies of the
small bowel with the tubeless method have achieved
a satisfactory experience of its diagnostic accuracy in
Crohn's disease.
In Crohn's disease, minimallesions like aphthous
ulcers, fold thickening, and edematous villosity may
be demonstrated (PRINGOT and BonART 1983). In
a series of patients with Crohn's disease, aphthous
ulcers were found to have a prevalence rate of 22%
(PRINGOT et al. 1984).
7.3.5.3
The Additional Pneumocolon
Fig. 7.3.24. SBE: angled compression view shows a kinked

angulated loop prior to a tight inflamed stenosis at the distal
ileum due to Crohn's disease
pelvis, like filling the bladder with fluid by catheterisation or, more comfortably for the patient, by administering 20 mg furosemide i.v., a promptly acting, highly
effective diuretic or distending the rectosigmoid by
In postsurgical recurrent small-bowel Crohn's disease, the pneumocolon or retrograde insuffiation of

air into the terminal ileum via a rectal tube may
be proposed as an adjunct to antegrade small bowel
studies for the demonstration of the ileocecal region
(KELLET et al. 1977) and for double-cantrast sturlies
of the terminal ileum (KELVIN et al. 1982; KRESSEL
et al. 1982) (Fig. 7.3.10). The retrograde passage of
air into the distal ileum is successful in all patients
with small bowel-colonic anastomosis (Figs. 7.3.8
and 7.3.25) and in about 90% of the patients with a
normal anatomic relation. Antispasmodics or glucagon may make the reflux of air easier and increase
the patient's comfort during colon insuffiation. Complementing tubeless enterography with pneumocolon
makes this method biphasic by enabling the demonstration of an exacerbation of Crohn's disease at the
distal ileum in single contrast in the first phase and
in retrograde double contrast in the second phase.
Double-cantrast views improve the anatomical demonstration of the distal ileum and in some cases provide more diagnostic information than single-contrast
views (FITZGERALD et al. 1985). In Crohn's disease,
the intestinal segment affected by pathologic changes
is determined more accurately (WOLF et al. 1985),
314
sion studies or showing a doubtful pattern should

be regarded as indications for biphasic enterography.
However, this latter method should not be performed
systematicallywhen the single-contrast views are diagnostic.
7.3.5.4
SBE vs SBFT in Crohn's Disease
Fig. 7.3.25. SBE with additional pneumocolon shows recurrent

exacerbation of Crohn's disease. Note: early longitudinal and
transverse ulcers in advanced stage of Crohn's disease. Tubular narrowing and anti-mesenteric outpouchings (pseudodiverticula, sacculations) can be seen at the neo-ileo-ascendostomy.
Ileocecal resection was performed at an earlier stage
as weil as the caliber of stenotic lesions (Fig. 7.3.26).

Nondiagnostic single-contrast studies of the distal
ileum, particularly when they are due to overlapping
or clumped loops, accurate demonstration in Crohn's
disease of the disease pattern and its extension,
entero-colonic anastomoses inaccessible by compres-
To date, the Iiterature comparing these two techniques has been mostly biased and retrospective
(FLEGKENSTEIN and PEDERSON 1975; SANDERS and
Ho 1976; VALLANGE 1980; ESETTE et al.1989; CHERNISH et al. 1992; BERNSTEIN et al. 1997). The data
used to support SBE include retrospective analyses
of consecutive radiograph studies, performed with
comparison to historical series of SBFT examination
at the same institution (SANDERS and Ho 1976; VALLANGE 1980; ESETTE et al. 1989; CHERNISH et al.
1992). An obvious major criticism ofthese studies is
the lack of prospective data comparing the two techniques directly in the same patient (AMBERG 1984).
The observed sensitivity, specificity, and accuracy of
SBE in Crohn's disease of the small intestine were
found tobe high in a study by MAGLINTE et al. (1992):
100%, 98.3%, and 99.3%, respectively. There were
no nondiagnostic or failed examinations or complications related to the technique. A retrospective
study performed both techniques in 26 patients: in 9
Fig. 7.3.26A,B. SBE (A) with additional pneumocolon (B) with infiating air retrorectally can better depict
the significance of the short segmental Crohn's Stenosis
patients, SBE added new diagnostic information that

might have changed the clinical management (SANDERS and Ho 1976). Some prospective sturlies compared both techniques in the same group of mostly
normal patients. Enteroclysis was found to be more
accurate than the tubeless method for demonstration
of the intestinal fold pattern, measurement of the fold
thickness being more frequently possible in the enema
sturlies ((FLECKENSTEIN and PEDERSON 1975; TAvERNE and VAN DER JAGT 1985). lt also appeared
in these sturlies that the double-contrast views were
superior to the single-contrast views for fold measurement in the ileum. However, in the terminal ileum,
no superiority of the enema sturlies over the tubeless
sturlies was noted. The diagnostic accuracy achieved by
small-bowel enema sturlies was over 90% (VALLANCE
1980; GURIAN et al. 1982; FRASER and PRESTON 1983).
Therefore, carefully performed enteroclysis by an
experienced gastrointestinal radiologist may often be
definitive. Frequently after enteroclysis, no further
radiologic procedures will be needed. However, overdistension of narrowed areas on SBE may efface submucosal abnormalities and Iead to underreporting of
the disease. In patients with a long segment of diffuse narrowing, the SBE may more clearly identify
the extent of the disease. Clinical sturlies have shown
that the delay between the onset of symptoms and
the diagnosis of Crohn's disease is greatest when the
disease is limited to the small intestine (ADAMS et al.
1980; STEINHARDT et al.1985; MAGLINTE et al.1992).
In 1997, the National Cooperative Crohn Disease
Study reported an average lag time of 36 months
(from onset of symptoms to time of diagnosis) for
small-bowel Crohn's disease ( GoLDBERGet al. 1979),
and the conventional SBFT was the method used for
radiologic examination.
Critics of SBFT often refer to the inadequate definition of the proximal ileum (in 35% of cases), distal
ileum (in 32% of cases), and jejunum (in 24% of
cases), as observed in this study, as a justification to
pursue SBE (BERNSTEIN et al. 1997). However, excellent results with carefully performed SBFT examinations with intermittent fiuoroscopy and compression
in patients with Crohn's disease of the small intestine
have been reported, and therefore some do not advocate the use ofSBE (CARLSON 1986). BERNSTEIN et al.
(1997) performed a prospective randomized comparison between SBE and SBFT in patients with Crohn's
disease. The alternate sturlies were performed within 2
weeks. From this study, it was clear that when Crohn's
disease is absent on SBFT, it is also absent on SBE.
When duodenal Crohn's disease lesions are present,
they may be missed by SBE (Figs. 7.3.27-7.3.29). SBFT
315
was safer in that it was associated with less radiation

than SBE, which is supported by other studies. The
SBFT was the examination preferred by the patients
in thesesturlies (OTT et al. 1985; THOENI and GouLD
1991; BERNSTEIN et al. 1997)
An earlier overview of the radiographic methods
available for small-bowel imaging concluded that
despite the growing interest in SBE, this procedure
has not yet become the prevailing method in Western
countries for diagnosing Crohn's disease (MARUYAMA
1985). We endorse the opinion that the choice of
which of these two methods to use requires ftexibility and depends not only on the clinical indication
for the study but also on the experience of the radiologist, on the referring physician, and on the patient
himself.
B
Fig. 7.3.27A,B. SBE fails to show duodenal disease: doublecantrast barium meal (A) and endoscopy (B) show early aphthoid lesions at the duodenal bulb
316
7.3.6
Ultrasonography
In clinical practice, ultrasonography (US) has recently gained a primary role in the diagnosis and followup of a few pathological conditions of the intestine,
mostly of inflammatory origin, such as acute appendicitis, sigmoid diverticulitis, and Crohn's disease. lt
can identify the presence of Crohn's disease through
the demonstration of bowelloops with pathologically thickened walls (MITTELSTAEDT 1993; SARRAZIN
and WILSON 1996; WILSON 1998; LEDERMANNet al.
2000). Such findings can be seen unexpectedly during
an abdominal uhrasound examination in a patient
with nonspecific symptoms or, more commonly, have
to be accurately researched in a study requested for
suspected inflammatory bowel disease. The examination technique involves both a panoramic exploration of the whole abdomen with a general purpose
abdominal transducer, and a study with a high-frequency probe using the graded compression technique (PUYLAERT 1994). Given the possible involvement of any bowel segment by the disease process,
a complete examination of all abdominal quadrants
is needed, while choice of the appropriate transducer
Fig. 7.3.28. Hypotonic duodenography after intravenous injection of glucagon shows a tight, short Crohn's stricture at the
duodenal bulb, the reason why no SBE could be performed
Fig. 7.3.29. Double-contrast barium meal: advanced stage of

Crohn's disease with an irregular stricture at D 1 of the duoden um with a duodenal biliary fistula (arrow). No Bilbao-Dotter
tube could pass this stricture
frequency will be related to the patient's body habitus. On cross-section, the involved intestinal segments present with a 'target-like' appearance characterized by a preserved layered structure within the
thickened wall (Figs. 7.3.7c and 7.3.30). This latter
finding is commonly regarded as the most important feature indicating the benign nature of the disease process. Furthermore, evaluation of the affected
loops along their longitudinal axis can show the focal
nature of the disease process by revealing adjacent
normal and pathological bowel segments, with gradual transition from one into another. This smooth
transition is considered another important feature
suggesting a benign condition. As regards the upper
Iimit of the normal intestinal wall, reported values
range between 3 and 5 mm, according to different
authors (DI CANDIO et al. 1986; SCHWERK et al. 1992;
BRIGNOLA et al. 1993; LIM et al. 1994; GASCHE et
al. 1999). Since the highest values were encountered
in the earliest studies on this disease, these differences are probably related to technological advances
in uhrasound equipment and/or to increased clinical
experience and better examination techniques. Based
on the demonstration of thickened bowel loops,
317
Fig. 7.3.30A,B. Axial (A) and longitudinal (B) images of the distal ilealloop in a patient with Crohn's disease. The 'target-like'
appearance of the involved loop is clearly evident; as weil as preservation of the layered structure of the thickened wall. There
is an associated slight hyperechogenicity of the inflamed mesenteric fat
uhrasound has shown high diagnostic accuracy in

patients with suspected Crohn's disease. PERA et al.
(1988) have shown 80.8o/o sensitivity and 79.2o/o specificity in a series of 181 patients (89 with Crohn's
disease, 57 with ulcerative colitis, and 35 controls),
and slightly higher values (sensitivity 82o/o, specificity
1OOo/o) have been reported by DI CANDIO et al. (1986)
in a group of 32 patients who had already undergone
one or more intestinal resections and were being
examined to detect possible relapses.
The increase in thickness is not the only finding
that can be encountered at the level of the involved
wall. HATA et al. (1992, 1994) in fact, through clinical
and pathologic-uhrasonographic correlations, have
divided the uhrasound findings of Crohn's disease
into three groups. Group A is characterized by a
bowel wall of normal thickness (<3 mm), but with
absent peristalsis and lack of compressibility of the
loops; group B had a thickened bowel wall (between
5 and 7 mm) and easily dernonstrahle parietallayers;
group C had thicker walls and disappearance of the
layers. Absence of peristalsis and lack of compressibility can then be considered as early signs of parietal involvement and have to be carefully researched,
even if they can be difficult to evaluate and to doc-
ument, involving some degree of subjectivity by

the examiner. Difficulties can be encountered also
in patients with advanced and chronic disease since
identification of the parietallayers can become impossible in these cases, and the thickened wall can present
diffuse and irregular hypoechogenicity (HATA et al.
1992, 1994; SCHWERK et al. 1992). Then, lacking clinical correlation, diagnostic problems can arise in the
differential diagnosis between thickening of benign
and malignant etiology. Furthermore, it must be noted
that thickening of the intestinal wall, even with preserved parietallayers, is not a specific finding and can
be encountered in a variety of benign intestinal diseases. LIM et al. (1994) have used the location of
the involved loops as a differential diagnostic criterion: thickening from Crohn's disease is more commonly encountered in the last ilealloops and ascending
colon, while ulcerative colitis more frequently involves
the rectum and descending colon; the cecal region is
the preferred site of involvement of intestinal tuberculosis, while ischemic colitis is more frequently located at the spienie flexure and descending portion of
the large bowel. Location of the involved loop and the
patient's age have been found to be good predictors
of the nature of the disease process in children with
318
acute bowel disease (SIEGEL et al. 1997). Furthermore,

WORLICEK et al. (1987) have shown that Crohn's disease causes severer thickening of the involved wall,
with values which are, in general, double than in
ulcerative colitis. LIMBERG and OsswALD ( 1994) have
analyzed the structure of the colanie wall after distension of the bowellumen with water and have shown
wall thickening, hypoechogenicity, and disappearance of the normal five-layer structure in patients
with Crohn's disease; in contrast, a normal structural
pattern and moderate thickening were only seen in
ulcerative colitis.
Involvement of the rectal wall by the disease process can be evaluated with the use of transrectal
probes which will accurately show mural changes as
well as perirectal complications within the range of
the transducer's field of view. Probe insertion, however, can cause marked discomfort and pain to subjects with active rectal and anal disease. In female
patients, a transvaginal approach can solve this problern (CHANG et al. 1993; DAMANI and WILSON 1999).
The use of a transvaginal probe angled posteriorly, in
fact, provides imaging of the recto-sigmoid and anal
regions along both axial and sagittal scan planes, and
the proximity of the involved bowel to the vaginal wall
allows the use of high-frequency transducers which
give optimal representation of both the rectum and
surrounding regions. Transvaginal ultrasonography
has also been used to evaluate involved small bowel
segments located deep in the pelvis, postero-superiorly to the Uterus (ADAMS et al. 1994) (Fig. 7.3.31).
The mesentery adjacent to the bowel segments
affected by the disease process becomes edematous

and thickened; it appears as a hyperechogenic structure surrounding the involved loops within which
enlarged hypoechoic lymph nodes may be easily
identified (Fig. 7.3.32). This thick,hyperechoic mass is
often the most striking finding during the uhrasound
examination of the abdomen, and should prompt
accurate evaluation of the adjacent bowel. Thickening of the mesentery is the most direct explanation
of the increased distance between adjacent intestinal
loops visible with conventional radiographic studIes.
In patients with advanced disease, US has a high
sensitivity and specificity for the identification of
Fig. 7.3.31. Transvaginal ultrasonography allows identification

of a thickened small bowel segment deep in the pelvis. The
thickened wall, preserved multilayered structure, and hyperechogenic perienteric fat are weil demonstrated
Fig. 7.3.32A,B. Crohn's disease recurrence after resection and

ileo-colonic anastomosis. A Ultrasonography demonstrates
the thickened ileal loop and two enlarged lymph nodes
(arrows) within the infiamed mesentery. B CT scan during
small-bowel transparent enema shows thickening and contrast enhancement of the involved loop, as weil as of the surrounding lymph nodes (arrow)
complications like strictures, fistulas, and abscesses.

GAseHE et al. {1999) have shown lOOo/o sensitivity in
the detection of strictures and abscesses, with a specificity of 91 o/o and 92%, respectively, and 87o/o sensitivity and 90o/o specificity in the detection of fistulas.
Lower sensitivity in the detection of such complications can be encountered. MACONI et al. {1996), for
instance, reported fistulas in only SOo/o of cases. Different sensitivities can be explained by differences
in the populations examined: patients with a less
advanced stage of the disease can have less severe
lesions, not obviously detectable by ultrasound, while
large lesions are more easily recognized (McLEAN
1999). Furthermore, differences in the definitions of
the US findings can explain the wide range of sensitivities reported by different authors (ARIENTI et al.
2000). As regards the occurrence of stenosis, it must
be noted that the lumen of any involved bowel segment is recognized as a thin echogenic line in the
center of the thickened wall. On this basis, it can be
difficult to differentiate between a collapsed and a
stenotic lumen; however, obstruction is inferred by
the presence of a distended and hyperperistaltic loop
proximal to the stricture (Fig. 7.3.33). Peristaisis and
alternate dilatation and stricture of adjacent loops can
be demonstrated. Fistulas can be seen as linear bands
of variable echogenicity extending from the involved
loops to adjacent abnormal bowel segments, to the
skin, or to the urinary bladder (Fig. 7.3.34). They commonly present with a complex structural pattern, consisting of a hypoechoic center with hyperechogenic
walls. Gas bubbles within the fistula appear as small,
central, echogenic and often mobile spots. The passage of small gas bubbles or solid material into
the urinary bladder can be seen in patients with
a fistula involving the vesical wall (Fig. 7.3.35). A
careful examination technique with a long period of
observation to identify this phenomenon is needed
in patients with pneumaturia and suspected involvement of this organ. It must be noted that fistulas
involving the skin are more easily recognized than
thosewith onlyan intra-abdominal,inter-loop course
which can be obscured by adjacent intraluminal gas.
Abscesses appear as hypoechogenic areas with irregular margins, containing corpusculated fluid, adjacent to involved loops (Figs. 7.3.36 and 7.3.37). They
can be either intra- or extraperitoneal, and can occasionally be difficult to identify and to differentiate
from dilated and hypoperistaltic loops containing corpusculated fluid. Demonstration of extraluminal gas
bubbles can help proper identification; however, large
collections of gas may be either misinterpreted as gas
within the bowellumen or impede a complete exami-
319
nation of the abdomen, thus leading to false-negative

results. When an abscess is easily seen, US can be used
to guide percutaneous drainage (SAFRIT et al. 1987;
LAMBIASE et al. 1988). Although themaneuver cannot
always result in total abscess eure, especially in cases
with associated fistulas, it can provide a temporizing
effect allowing aggressive medical therapy, prolonged
parenteral hyperalimentation, and bowel rest, thus
facilitating closure of fistulas and improving the
patient's nutritional status. It must be noted that when
Fig. 7.3.33A,B. Ultrasonographie demonstration of stenosis. A

Oblique scan with a general purpose probe demonstrates a
dilated loop (asterisk), with tapering of the Iumen and wall
thickening (arrows).A barium study (B) confirms the presence
of the stenosis
320
Fig. 7.3.34. Fistula to the skin. The fistula is seen as a

long linear hypoechoic tract running from the abdominal
cavity to the skin. Subtle movement of a small quantity of
echogenic fluid was appreciated with real-time observation.
Shadowing did not allow identification of the loop from
which the fistula took origin
Fig. 7.3.35. US of the pelvis shows a transmural thickened

intestinalloop (arrow) with a fistulous tract with air entrapped
(arrowhead) to the bladder (B bladder). (Courtesy of Dr. J.
SARRAZIN and Dr. S.R. WILSON 1996)
Fig. 7.3.36. Crohn's disease with phlegmon: US longitudinal

view through a transmural thickened (arrows) intestinalloop
shows a !arge hypoechoic irregular mass, due to a phlegmon
(P) (Courtesy of Dr. J. SARRAZIN and Dr. S.R. WILSON 1996)
the collection is difficult to delineate by US, or when a

safe route for puncture cannot be identified with certainty, er has to be employed for drainage guidance
(CASOLA et al. 1987). Phlegmons can be detected as
hypoechoic areas without a fluid content surrounded
by a hyperechoic halo.
HATA et al. (1992) have shown a direct correlation
between bowel wall thickening and disease activity,
and BRIGNOLA et al. (1993) found one between the
degree of intestinal wall thickening and the severity of
the disease process as measured by nuclear medicine
methods. However, thickened bowelloops can also be
encountered in patients in clinical remission, probably due to persistence of fibrotic changes within the
wall of the involved segments after therapy. In a recent
study, ZAMBONI et al. (1999) have evaluated the prognostic significance of a persistently thickened wall in
patients in clinical remission, showing that patients
with walls thicker than 6 mm had a higher percentage
of recurrence during a follow-up Iasting 18 months.
The hyperdynamic intestinal circulation that develops in infiammatory bowel disease can be evaluated
using the Doppler technique, and the degree of the
measured fiow changes has been related to the activity
of the disease process. The simplest, although subjective, way to demonstrate active infiammatory chang-
es is evaluation of the thickened loops and adjacent

hyperechogenic mesentery with color Doppler ultrasonography (WILSON 1998). Identification of flow
signals within the thickened bowel wall and mesentery is direct evidence of the activity of the disease
(Fig. 7.3.38). Evaluation offlowwithin the mesenteric
arteries and portal vein has been carried out by many
authors, using both quantitative and semiquantitative
321
methods. BoLONDI et al. {1992) have shown increased

flow velocity in the portal vein and a decreased resistance index (RI) within the superior mesenteric artery
(SMA) in patients with active Crohn's disease vs cases
of nonactive disease and controls. A decreased RI
within the SMA in patients with active Crohn's disease was found by VAN OosTAYEN et al. {1994); the
same authors noted a good correlation of flow changes
Fig. 7.3.37A. Thickened loop surrounded by abscess (asterisk) imaged through a transvaginal approach. 8 Transabdominal scan
shows an involved loop and, anteriorly, an abscess containing a small air bubble (arrow)
Fig. 7.3.38A,8. Axial (A) and longitudinal (8) images of the distal ilealloop in two different patients with Crohn's disease
in whom color-Doppler was used to document hypervascularization of the thickened wall
322
at this level with a clinically derived Crohn's disease

activity index (V AN OSTA YEN ET AL. 1997). MACONI
et al. (1998) correlated the presence of flow changes
within the SMA to the site of bowel involvement:
patients with ileal disease had lower RI in the SMA
than those with involvement of the large bowel. MIRK
et al. (1999) have shown that involvement ofthelarge
bowel by the disease process causes lowering of the
RI at the level of the IMA. The study of postprandial
changes in blood flow has demonstrated a variety of
findings. GIOVAGNORIO et al. (1998) have shown that
patients with active disease have a smaller decrease
of resistances within the SMA than those with nonactive disease and normal controls. They suggest that
normal vascular postprandial changes within the SMA
do not occur in these patients since vasodilatation is
already established in the splanchnic system due to the
inflammatory disease, and suggest the use of both
pre- and postprandial measurements as a test to evaluate disease activity, which would be more powerful
than measurements obtained in the fasting state alone.
BRITTON et al. (1998) have found, using volume flow
measurements, that the time interval from food challenge to peak SMA flow rate was significantly lower in
patients with active untreated disease compared with
inactive patients; longitudinal follow-up of active disease demonstrated a prolongation of time to peak flow
following clinical remission. Blood flow measurements
have also been used as a prognostic test: LuowiG et al.
(1999) have shown a relationship between splanchnic
blood flow measurements and early relapse of disease.
They followed up a group of patients with serial Doppler measurement of the SMA and found that a lack
of increase in the pulsatility index (PI) of SMA during
clinical remission was highly indicative of subclinical
persisting disease and early relapse. Patients in whom
the PI increased during clinical remission remained in
good health for at least 6 months.
At present, there are no conclusive data in the literature on the possible role of Doppler imaging in
the clinical management of patients with Crohn's disease. Determining whether the evaluation of hemodynamic changes in the splanchnic vasculature can
influence the clinical assessment of disease activity
and affect the therapeutic approach to the patient
still requires wider and more prolonged experience
in a large series of cases.
The noninvasiveness and general availability of
US have made this technique one of the first-choice
modalities in the study of a large variety of abdominal problems. However, in patients with inflammatory bowel diseases, barium studies, enteroscopy/
ileoscopy, CT, and MRI are still the most frequently

used diagnostic techniques. In fact, although a high
sensitivity and specificity in demonstrating thickening
of the intestinal wall have been demonstrated, there
are still important limitations that do not allow the
use of US for a complete study of the bowel in these
patients. First of all, US is a tomographic technique,
and there are difficulties in exploring the whole course
of the bowel loops. Patients who are obese or have
abundant intestinal gas are difficult to image by this
method, and even if a complete survey of the abdomen is accurately obtained, it is not possible tobe sure
that all bowel segments have been properly explored.
Then, it must be remernbered that although the use of
transrectal and/or transvaginal transducers can greatly help in the study oflesions deep in the pelvis, such
lesions are always difficult to recognize (BAGLEY and
SEMELKA 1994). In addition, US specifically evaluates
the thickness and structure of the bowel wall and
can overlook early pathological changes affecting the
mucosal surface only, which are still better visualized
by enteroscopy/ileoscopy or conventional radiographic procedures (SoL VIG et al. 1995). Furthermore, thickening of the bowel wall is a nonspecific finding, and
even if analysis of the involved bowel segment and of
the preserved parietal layers is taken into account,
it can be difficult to differentiate among its many
possible benign pathologic causes. As regards complications, a different diagnostic accuracy has been
observed in relation to disease severity since advanced
disease can be studied more easily and is more obviously detectable by US (McLEAN 1999).
At present, there is no consensus on the role of
US in relation to other imaging procedures in this
field. However, the lack of radiation and ready availability of US make it an attractive technique, particularly when considering that the disease affects mostly
young patients in the reproductive age, who require
numerous serial examinations. First of all, as suggested by SHERIDAN et al. (1993) and by SOLVIG et al.
(1995), US can be used as a further criterion to select
patients prior to radiological investigations. When
suspicion of disease is low, in fact, anormal US may be
sufficient to avoid radiography; on the contrary, when
US is positive or clinical suspicion is high despite a
normal US exam, further examinations are recommended for a better diagnosis. In addition, although
radiographic studies and/or CT are usually needed for
accurate disease evaluation and for proper surgical
planning, US can be safely employed to follow up the
patient, thus avoiding or at least delaying and reducing the need for more complete and panoramic, but
invasive and less well-accepted imaging procedures.
We believe that a good clinical use of US in this field

requires the cooperation of the radiologist with all the
clinical specialists involved in the care of patients with
Crohn's disease. Close correlation of the US images
with the clinical findings as well as knowledge of the
patient's history and conditions at the time of the
study are of the utmost importance to guide the proper
use and timing of imaging procedures and avoid the
risk of false- negative results.
7.3.7
Computed Tomography
Double-contrast radiographs and endoscopy are the
most common methods of examination in the diagnosis of inflammatory bowel disease. Although these
modalities provide a wealth of information regarding
the mucosa (e.g., the presence of aphthoid lesions,
cobblestoning, pseudopolyps, ulcerations, etc.), US
and CT can provide an important additional diagnostic perspective. It has been proven to be superior
in recognizing intramural, serosal, and mesenteric
changes, including thickening of the intestinal wall or
serosa, fibrofatty proliferation of the mesenteric adipose tissue, inflammatory changes of the surrounding
mesentery (creeping fat), and mesenteric lymphadenopathy (NAHAKAWA et al. 1993; GaRE and GHAHREMANI 1995; JACaBS and BIRNBAUM 1995; KLEIN et al.
1995; GaRE et al. 1996). Clinically, CT is very helpful
in assessing space-occupying masses or displacement
of intestinal segments.
For acutely ill patients, CT is often the only study
required, providing crucial information for both an
accurate diagnosis and management of the many complications associated with inflammatory bowel disease
(IBD) (BALTHAZAR 1991; GaRE and LAUPER 1994).
The characteristics ofiBD, as evaluated by CT, are
listed in Table 7.3.2. GaRE et al. (1996) have reviewed
the value and applications of CT for patients with IBD.
They suggest that complete opacification of a well-distended gut is mandatory for accurate CT evaluation
ofbowel wall thickening and distortion of mural components that are the hallmarks of IBD (GaRE 1994,
GaRE et al. 1996; VECCHIOLI et al. 1994; ScHaLTEN
et al. 1995). Nonopacified bowelloops are potential
sources of diagnostic error because they can simulate
an abscess, mass, or enlarged lymph nodes. The
patient should drink 1000 ml of a 2o/o barium suspension (Readi-CAT 2; EZ-EM, Westbury, NY) the
evening before the CT examination to opacify the
colon by the next day. An additionallOOO ml of dilute
barium suspension is administered orally over a
323
1-h period before the scan to opacify the stomach and
small bowel. Dilute (2o/o), water-soluble contrast material should be used in preoperative and trauma patients
as well as those with suspected bowel perforation.
Iodinated contrast material should be administered
i.v. to all patients, unless contraindicated, because
bowel wall contrast enhancement is an important indicator of the degree of mural inflammation and mesenteric engorgement. They give 150 ml of 60o/o iodinated contrast material, delivered as a monophasic bolus
with apower injector at 2 ml!s.
The standard imaging protocol to obtain scans from
the diaphragm through the perineum uses 10 mm collimation at 10 mm intervals (pitch 1:1). In patients with
known or suspected IBD, this protocol is modified so
Tab1e 7.3.2. Ultrasound and CT findings in Crohn's intestinal
disease (after REEDERSand ROSENBUSCH 1994)
Pathological changes
Frequency
Changes in mucosa and lumen:

Narrowing of lumen
Thickening of bowel wall
Mural involvement:
Mural thickening
Terminal ileum
Small intestine
Colon
Transmural involvement:
Transmural ulceration
Thickness of wall by CT
Irregular contour:
Inner contour
Outer contour
Thumbprinting'
Submucosal edema ('bull's-eye sign')
Changes in mesentery:
Fibro-fatty proliferation
of the mesentery
Mesenteric abscess/phlegmon
Inflammatory reaction of mesentery
Increased and enlarged
mesenteric lymph nodes
Fistulas and recesses
Abscesses:
Iliopsoas muscle
Periluminal
Subcutaneous
Intramuscular
Liver
Perirectal
Free fluid in peritoneum/seroma
Extraintestinal manifestations:
Fatty infiltration of liver
Hydronephrosis
+>1 cm
+
+ (symmetric)
+ (average
13 mm-3 cm)
+
Inhomogeneous
+
+
+
-
+
+
+
+ (peri-, ischiorectal)
+
+
+
+
+
324
that 5 mm thick scans at 5 mm intervals (pitch 1:1) are

obtained from the iliac crest through the perineum.
This technique should be used in conjunction with
the i.v. administration of glucagon to induce intestinal
hypomotility, which reduces peristaltic artifacts.
If specific intestinal loops are of concern, it is
important to obtain high-resolution, thin-section
images with optimum levels of intravascular cantrast enhancement of the affected areas (Go RE et al.
1996).
In early Crohn's disease (early phase) where the
disease is limited to the mucosa, enlarged lymph
follicles and aphthous ulceration on CT are usually
unremarkable due to the limited spatial resolution.
Although the ulcerative phase may be identified
on CT scan, the assessment of the mucosa is best
clone with barium studies and ileoscopy, which are
more direct and sensitive (FoDERARO et al. 1987;
ARCHIBALD et al. 1988, GaRE et al. 1996). However,
inflamed mucosa and serosa may show significant
cantrast enhancement after bolus i.v. administration
of cantrast material, and the intensity of enhancement
correlates with the clinical activity of the disease.
In the recovery phase, inflammatory and postinflammatory pseudopolyps may be identified on CT
scan. The small bowel may show mural stratification
and often a target or 'double halo' appearance (GOLDBERG et al. 1983; SIMPKINS and GORE 1994; PHILPOTTS et al.1994; HORTON et al. 2000). A ring of softtissue density ( = mucosa) is surrounded by a lowdensity ring with an attenuation near that of water or
fat, corresponding to submucosal edema or fat infiltration respectively, which is surrounded by a higher
density ring (muscularis propria) (JoNES et al. 1986)
(Fig. 7.3.39). The thickness of the wall of the normal,
fully distended small bowel does not exceed 5 mm
with cross-sectional imaging techniques. In Crohn's
disease, the bowel wall thickening, which occurs in
>83% of patients, most frequently at the terminal
ileum, may range from 11 to 13 mm. (GaRE and
GOLDBERG 1982; GOLDBERG et al. 1983; GORE et al.
1984; FISHMAN et al. 1987; PHILPOTTS et al. 1994;
KLEIN et al. 1995, RAPTOPOULOS 1989; RAPTOPOULOS et al. 1997; HORTON et al. 2000).
The mesentery and omenturn normally contain
blood vessels and lymph nodes (<3-5 mm) and fat
(attenuation value -75 to -125 HU) (GaRE 1994; VEcCHIOLI et al. 1994). A higher attenuation value indicates the presence of fluid, cellular infiltrate, edema,
hemorrhage, or fibrosis.
In the advanced phase, transmural fibrosis and
cicatrization are the hallmarks. Due to a loss of mural
stratification, the affected bowel wall shows homoge-
Fig. 7.3.39A. SBE: transition of recovery and advanced stage

of Crohn's intestinal disease, showing recurrent cobblestone
formation and tubular narrowing over a long segment. Ileocecal resection had been performed in an earlier stage. CT (B)
shows the longitudinal and transverse view of the intestinal
marked transmural thickening ('target sign') in a cicatrizing
phase of Crohn's disease
neous attenuation on cantrast-enhanced CT (GaRE et

al. 1996).
In patients with regional enteritis, separation of
bowelloops on small-bowel series is most commonly
caused by mesenteric fibrofatty proliferation ('creeping fat') (GORE and GHAHREMANI 1995; MEYERS and
McGUIRE 1995; GORE et al. 1996) (Fig. 7.3.40). Whereas the CT density of normal mesenteric fat is between
-100 and -160 HU, fibrofatty proliferation shows an
attenuation value of -70 to -90 HU, secondary to the
influx of inflammatory cells and fluid. 'Creeping' mesenteric fat, as observed pathologically, tends to extend
over the serosa towards the anti-mesenteric border
and may encompass the bowel wall (GoLDBERG et al.
1983; RALLS and JEFFREY 1995; MEYERS and McGUIRE
1995).
Fig. 7.3.40. CT showing marked inflammatory changes in periintestinal fat ('creeping fat') around an inflamed intestinal
loop with transmural thickening in the left lower abdominal
region
Mesenteric lymphadenopathy (lymph node size

3-8 mm) - a finding not specific for inflammatory
bowel disease - may be present. If the lymph nodes
are >1 cm, the presence of Iymphoma or carcinoma
must be excluded (FISHMAN et al. 1987; BANSALand
SONNENBERG 1996; GORE et al.1996).
The asymmetry of the disease involvement, which
typically occurs along the mesenteric border of the
intestine, can result in the formation of pseudodiverticula along the anti-mesenteric border. Pseudodiverticula are small outpouchings of the intestinal wall that
occur opposite regions of fibrosis and scarring. Spiral
CT may be used to diagnostic advantage and now often
has the capability of combining the evaluation ofluminal and mural changes and extraluminal pathologywith
vascular alterations (MEYERS and McGUIRE 1995).
Spiral contrast-enhanced CT often shows hypervascularity of the involved mesentery manifesting as
mesenteric arterial dilatation, tortuosity, prominence
and wide spacing, dilatation of the vasa recta (vascular jejunization of the ileum or 'Comb sign') (MEYERS
and MCGUIRE 1995; GORE et al. 1996) (Figs. 7.3.41 and
7.3.42). This vascular pattern of vessel dilatation from
the main mesenteric branches distally to the level
of the vasa recta is a feature of early active Crohn's
disease. It may be useful in differentiating Crohn's
disease from Iymphoma or metastasis (MEYERS and
McGUIRE 1995). Such findings would be unexpected
in chronic disease with its characteristic fibrosis (Lu NDERQUIST et al. 1967; GOLDBERG et al. 1983; HERLINGER and MAGLINTE 1989).
Recent correlative pathologic studies have demonstrated a spectrum of vascular changes, ranging from
mesenteric Vaseulitis (WAKEFIELD et al. 1989; LEWIN
325
et al. 1992) and associated vessel wall granulomas

(LEWIN et al. 1992; MAPSTONE and DIXON 1992) to
obiiterative vascular lesions (KNUTTSON et al. 1968;
LEWIN et al. 1992). Thus, spiral CT angiography,
which allows 2- and 3-dimensional reconstructions
free from the respiratory mis-registration and step
artifacts produced by incremental scanning, may
offer with i.v. cantrast the capability to document
precisely the site of intraluminal extravasation. In
patients with Crohn's disease involving the ileum
and/or ascending colon, spiral CT features of hypervascularity should suggest an acute exacerbation.
Complications of inflammatory intestinal disease
can be imaged with CT; in the case of Crohn's disease,
CT has been shown to affect disease management in
28% of cases (FISHMAN et al. 1987).
Intra-abdominal abscesses or phlegmons (Figs.
7.3.43 and 7.3.44), which develop in 15%-20% of
patients with Crohn's disease, usually result from
sinus tracts, fistulas, perforation, or surgical operations for Crohn's disease (GOLDBERG et al. 1983;
FUKUYA et al. 1991; WILLSet al. 1997).
Although a mass effect, spiculation of the mucosa,
or identification of the fistula on barium studies are
indirect signs of an intra-abdominal abscess, US or
CT is required not only to confirm the diagnosis (as
a circumscribed, round or oval, water-density mass
with attenuation of 10-30 HU, with peripheral cantrast enhancement) and show the full extent and location of the abscess (REL et al. 1987), but also for
US- or CT-guided percutaneous management of intraabdominal abscesses. US allows real-time imaging,
is faster than CT guidance, and avoids unnecessary
exposure to ionizing radiation (HoRTON et al. 2000).
Extraluminal air may be found in 50% of the cases
(HYDE and GERZOF 1994), secondary to sinus tracts
communicating with the skin surface or gastrointestinal tract.
To visualize the full extent of fistulas (entero-enteric, entero-colic, entero-vesical, entero-vaginal, enterocutaneous, entero-spinal) and sinus tracts which may
affect 20o/o-40o/o of the patients with Crohn's disease
(GORE and LAUFER 1994), the usefulness of CT is
controversial (FISHMAN et al. 1987; REL et al. 1987;
KUHLMAN and FISHMAN 1990; RAPTOPOULOS et al.
1997; WILLSet al. 1997). If an entero-vesical fistula is
suspected, it is often helpful to perform CT with oral
or rectal cantrast material but no intravenous cantrast material.
If positive cantrast material is detected in the bladder, it must have originated from the intestine, thus
confirming the presence of an entero-vesical fistula.
If intravenous cantrast material is administered, pos-
326
Fig. 7.3.41A-C. Crohn's disease of distal ileum with hypervascularity. A CT of the right mid-abdomen demonstrates spray of
dilated branches (arrows) rising from an arcade tear. B Extending
distally, the branches areevident as a constellation (arrows) highlighted in the mesentery, which has undergone fibrofatty proliferation. The wall of the distal ilealloop is thickened. An incidental
renal cyst is noted. C Multiple, dilated vasa recta arise in a striking
comblike fashion to enter the mesenteric border of the terminal
ileum ('comb sign'). A halo secondary to submucosal edema is
present within its thickened wall. (Courtesy of Dr. M.A. MEYERS
1995)
Fig. 7.3.42. 'Comb sign' on CT: vascular engorgement of ileal

mesentery associated with active Crohn's disease. CT scan
shows vascular dilatation, tortuosity, and prominence of vasa
recta (solid arrow) on the mesenteric border of the ileum
('comb sign'). Diseased ilealloop shows mural thickening and
target appearance (open arrow). Alsonote prominent mesenteric lymph nodes. (Courtesy of Dr. R.M. GORE 1996)
327
technique usually requires prohing and repositioning

of the catheter during injection. However, in difficult
cases, the fistulous tract can be injected under uoroscopic guidance, and non-enhanced er can then be
performed if necessary (HoRTON et al. 2000)
In chronic erohn's disease, there is an increased
incidence of adenocarcinoma and Iymphoma of the
small bowel, particularly in the bypassed or excluded Segments of the gut (ANSAL and SONNENBERG
1996), which can be seenon barium studies or er.
7.3.8
Spiral CT Enterography
Fig. 7.3.43. CT: Extraperitoneal abscess (A) along the posterior

medial aspect of the right iliopsoas muscle due to Crohn's disease. (Courtesy of Dr. R.M. GoRE et al.l996)
Fig. 7.3.44. Extraperitoneal abscess along the posterior medial

aspect of the right iliopsoas muscle of another patient, which
has been drained under CT guidance
itive cantrast material can reach the bladder via the

ureters or intestine. Other er findings of entero-vesical fistula include air in the bladder and focal bladder wall thickening adjacent to a diseased bowelloop.
Entero-cutaneous, perianal, and recto-vaginal fistulas may be diagnosed by detecting oral or rectal cantrast material within the actual fistulous tract. As an
alternative, for greater sensitivity, positive cantrast
material can be injected into the fistula and its connection to the intestine can be determined. rhis technique is usually more successful when performed
with real-time uoroscopy rather than er, since the
Spiral er enterography, a modified spiral er protocol for bowel imaging, provides bowel opacification
of high diagnostic quality. In patients with erohn's
disease, multiplanar (especially coronal) imaging
improves confidence in assessing the presence and
extent of disease. er enterography is complementary and often superior to conventional barium studies
(RAPTOPOULOS et al.1997; ROLLANDI et al.1999).
Most protocols for abdominal pelvic er scanning
recommend an oral cantrast dose of <1200 cc to
ensure the patient's comfort and compliance (GaRE
et al. 1985; MITCHELL et al.1985; RAPTOPOULOS et al.
1989, 1997). A !arger dose (1500 ml) via a nasogastric
tube has been suggested for adequate bowel opacification and distention (PECHER et al. 1996). In er
enterography, at least 1600 cc is required to produce
consistent bowel opacification. It is performed with
the patient in a prone position to provide better compression and dispersion of the bowelloops.
In the studies by RAPTOPOULOS et al. (1997),
multiplanar renderings improved the perception of
the extent of bowel wall thickening in erohn's disease in a significant number of cases. rhis procedure could obviate the need for additional barium
studies to clarify possible abnormalities or ambiguous er readings and would result in a reduction in
radiation exposure.
RAPTOPOULOS et al. (1997) estimated the average
effective dose equivalent for conventional er of the
abdomen and pelvis as 3.6 mSv. No additional radiation occurs if the technique changes (5 mm collimation and a pitch of 1.5, as used for er enterography) to accommodate image processing and multiplanar or 3-dimensional projectional imaging. rhe
effective dose equivalent for a small-bowel study
can vary greatly from the average figure quoted
(3.9-4.06 mSv), because the exposure factors are
328
patient-, operator-, and even abnormality-dependent (NCRP 1989; NISHIZAWA et al. 1991; RAPTOPOULOS et al. 1997).
of an orally administered, ferromagnetic-based contrast agent to suppress signals of the bowel lumen
has made possible a reproducible evaluation of the
bowel wall. They have adjusted the tissue-contrast
characteristics of MRI to assess bowel wall morphology (thickness) and several functional parameters
7.3.9
including edema (high-signal T2-weighted images)
Magnetic Resonance lmaging
and vascularity (bowel wall enhancement). Their
results demonstrate an excellent agreement between
In the past, MRI was seldom done for Crohn's dis- the BA as defined by positive contrast reactants and
ease. Because of the long acquisition times of spin- the functional parameters of MRI (T2-weighted, fatecho sequences, breath holdingwas not possible, and suppressed wall signal and signal of fibrofatty proimaging of the bowel was blurred.
liferation on T2-weighted, fat-suppressed images).
MRI is an imaging modality similar to CT in that The correlation for anatomic parameters such as wall
images demonstrate overall topography of the abdo- thickness and fatty proliferation was less significant
men (RoLLANDI et al. 1996). It can provide direct (LICHTENSTEIN et al. 2000). Low-field MRI should
multiplanar (coronal) images with a high soft-tissue also be considered a promising non-invasive method
contrast; its lack of ionizing radiation, the ability to in the evaluation of response regarding both disease
do without intubation of the intestinallumen, and extension and activity in Crohn's disease during
the relative ease and lack of overall patient discom- treatment with systemic steroids (MADSON et al.
fort have suggested its use to detect complications 1999) (Fig. 7.3.45).
of Crohn's disease (RAPTOPOULOS et al. 1997; LICHThe continued improvement of MR technology
TENSTEIN et al. 2000). Disadvantages which have with techniques such as HASTE (single-shot fast-spin
generally precluded routine use ofMRI in the inves- echo) and extremely rapid gradient-echo techniques
tigation of bowel disease include motion artifacts, a will make evaluation of the small bowel even faster
lack of spatial resolution (with standard spin-echo and more reliable. Recently, a true FISP sequence has
or gradient-echo sequences), and a lack of a satisfac- been applied successfully for small bowel imaging,
tory oral contrast agent (CHou et al. 1994).
providing clear delineation of intestinal wall, homogCHou et al. (1994) have demonstrated the appear- enaus high-signallumen opacification and demonance of gastrointestinal wall thickening using air stration of the mesenteries (GouRTSOYIANNIS et al.
insuffl.ation and intraluminal contrast agent. The use 2000). The ability to noninvasively monitor the activof i.v. gadolinium chelates has been shown tobe accu- ity of Crohn's disease within the small bowel reprerate in assessing Crohn's disease activity (SEMELKA sents a potentially powerful tool in following Crohn's
et al. 1991; SHOENUT et al. 1993, 1994).
disease patients and an exciting surrogate endpoint
The most widely used measure is the Crohn Dis- for clinical trials of newly proposed therapeutic
ease Activity Index (CDAI), which is of paramount agents (MADSON et al. 1999; LICHTENSTEIN et al.
importance in the management of patients with 2000).
A recent study has shown the value of MRI of the
Crohn's disease and was devised by the National
Cooperative Crohn Disease Study (BEST et al. 1976, abdomen combined with enteroclysis (MRI enterog1979). The CDAI does not have universal acceptance, raphy) in Crohn's disease using oral and intravenous
and other less elaborate forms of statistical analysis gadolinium-DTPA (RIEBER et al. 1998) or oral iron
[Harvey-Bradshaw Index (HBI) and Oxford Index particles (HoLZKNECHT et al. 1998). Intestinal intu(OI)] have been proposed. MACCHIONI et al. (1999) bation with administration of an iso-osomotic water
have considered the evaluation of four acute-phase solution inside the MRI suite provides optimal small
reactants (white blood cell count, ESR, C-reactive bowel distension, ensures delineation of superficial
protein, and orosomucoids) tobe more closely relat- and transmural abnormalities of Crohn's disease
ed to the purpose of MRI, i.e., the determination of (GOURTSOYIANNIS et al. 2000) and allows for fl.uodisease activity. If at least three of these four reac- roscopic sturlies of the small bowel (UMSCHADEN et
tants are positive, this is considered evidence of a sus- al. 2000). Thickening or distortion of valvulae contained infl.ammatory process and thus the gold stan- niventes, linear ulcers, cobblestoning, lumen nardard of biologic activity (BA). By using MRI, MAc- rowing and sinus tracts or fistulas can be easily
CHIONI et al. (1999) have proposed a novel approach depicted employing this technique (PRASSOPOULOS
to monitoring the activity of Crohn' s disease. The use et al. 2001).
329
Fig. 7.3.45A-F. MRI in Crohn's disease: MRI sequences from a patient with active Crohn's disease in the terminal ileum. Examples
ofT2-weighted (A), precontrast Tl-weighted (B), and postcantrast Tl-weighted images (C) from the first MRI when the patient
had high clinical disease activity. Pretreatment images show severely increased signal intensity from the terminal ileum (SI
t2) on T2-weighted images (arrows), indicative of severe edema, and a significant increment of signal intensity in the bowel
wall (%SI tl) on the Tl-weighted images (arrowheads), indicative of inftammation. These findings could not be reproduced
on the images from the second MRI. D-F show corresponding examples from the second MRI (clinical remission). (Courtesy
of Dr. S.M. MADSON et al. 1999)
330
Presently, however, the value ofMR is under investigation, and it is (still) not a primary technique in the
imaging of Crohn's disease or its complications.
However, MRI appears to hold great promise: further directions to develop will probablyinclude i.v. contrast, new sequences (fast spin-echo sequences with
long echo-train, permitting breath holding imaging and
high spatial resolution), regional use ofsurface coils and
oral cantrast agents, which works at all field strengths
and uniformly outline the bowellumen. The application of a contrast-enhanced 3D FLASH Tl-weighted
sequence with fat saturation using 2.5 mm thin slices
and a 512 matrix resulted in excellent image quality
(GOURTSOYIANNIS et al. 2001) and appears promising for the evaluation of morphologic changes and
activity of Crohn's disease.
The current cost-conscious climate makes it imperative to reduce the number of radiologic investigations
performed, especially MRI. LEE and SEMELKA (1998)
introduced MRI of the small bowel using the HASTE
sequence, and ERNST et al. (1998) recently introduced the
fast spin-echo sequence [turbo-spin-echo, hybrid rapid
acquisition with relaxation enhancement (HRARE)] to
evaluate small bowel involvement of Crohn's disease
with a breath holding technique.
Fast imaging is possible with a HRARE technique
using a long echo-train and a short TR. The long echotrain produces a long effective TE (MITCHELL et al.
1994). With such a sequence, ERNST et al. (1998) used
a mixed Tl- and T2-weighted image. Fat gives a high
signal intensity, tissues with short Tl relaxation times
have a low signal intensity. Water, with long Tl and T2
relaxation tim es, has an intermediate signal intensity.
The intestinal wall, with low signal intensity, is well
delineated between the high-signal-intensity mesenteric fat and intermediate-signal-intensity water. Fat

suppression is not suitable with the HRARE sequence,
because its use decreases the cantrast between the
intestinal wall, vessels, lymph nodes, and mesenteric
fat (Figs. 7.3.46 and 7.3.47).
In previous studies (SHOENUT et al. 1994; KETTRITZ
et al. 1995), the measurement of wall thickness was
done on cantrast-enhanced spin-echo images. With the
HRARE sequence, these measurements can be made
without i.v. injection of gadolinium chelate. Furthermore, the use of a HRARE sequence allows a better spatial resolution than a spin-echo sequence as few motion
artifacts occur because of the use of a breath-holding
acquisition. In their series, the ileum wall thickness of
healthy subjects was less than the 3 mm seen on CT
(GoRE 1989). In patients with Crohn's disease, the wall
thickness exceeded 3 mm.
MRI with a HRARE-sequence is able to show
the 'comb sign' (tortuous lines in the mesenteric
fat corresponding to distal mesenteric branches,
distal to the level of the vasa recta). However, in
the future, comparative studies are required to
determine the place of this technique among other
established imaging techniques when investigating
Crohn's disease.
MRI has proved useful in the evaluation of sinus
tracts and fistulas (Figs. 7.3.48 and 7.3.49). On
Tl-weighted MR images, sinus-tracts and fistulas
are hypointense due to their fluid content; on T2weighted images, the signal intensity depends on
their fluid content and the degree of surrounding
fibrosis. On fast multiplanar IR MR images, the fat
signal is suppressed, making it easier to identify the
high signal intensity of sinus tracts and fistula. The
extension of fistula tracts is of particular importance with regard to the surgical approach in affected patients.
Fig. 7.3.46. Ileal Crohn's disease. Fast spin-echo

MR image [577/128(TR/TE): echo train length 23]
reveals thickening of the ileum wall. Fat has a high
signal intensity, the Iumen an intermediate signal
intensity due to water, and intestinal wall a low
signal intensity. (Courtesy of Dr. 0. ERNST et al.
1998)
331
Fig. 7.3.47. Crohn's disease. Fastspin-echo MR image

(552/28; echo train length 23) in coronal plane shows
dilated small bowelloops (arrows) above stricture
of terminal ileum (arrowhead) . (Courtesy of Dr. 0.
ERNST et aJ. 1998)
Fig. 7.3.48. Long fistula resulting from Crohn's disease. Fast SE

T2-weighted MR image shows a curvilinear area of high signal
intensity on the left side of the rectum. This is an example of
an abscess and fistula extending between the infra- and supralevator spaces
Fig. 7.3.49. Axial, fast, multiplanar IR MR image demonstrates

a high signal intensity sinus tract resulting from Crohn's disease, against the black background because of the fat suppression inherent to the imaging sequence, extending into the perianal region
Abscesses resulting from Crohn's disease can be

detected with MRI (LUNNISS et al.l994; O'DoNOVAN
et al. 1997).
Sagittal/axial, fast spin-echo, T2-weighted MRI (or
coronal fast multiplanar) IR MRI may show a hyperintense collection.
7.3.10
Nuclear Medicine
Leucocyte scintigraphy is increasingly being used for

the investigation of inflammatory bowel disease (SAvERYMUTTU et al. 1986; LI et al. 1992a,b, 1994; GIAFFER
332
Fig. 7.3.50. In-labeled granulocyte scan in a patient with ileocolonic Crohn's disease. Abnormal activity in the sigmoid
colon, proximal transverse colon and terminal ileum (courtesy
of Dr. SH Saverymuttu).
1996; ARNDT et al. 1997). Recent results with 111 In and

99Tcm HMPAO-labeled leukocyte scintigraphy have
demonstrated excellent correlation with clinical symptoms, endoscopy, and histopathological findings in
patients with Crohn's disease. lt has proved useful
both for diagnosis inflammation and for estimating its
extent and activity (SAVERYMUTTU et al. 1986; LI et al.
1994) (Fig. 7.3.50).
Radionuclide-labelling leucocyte scintigraphy has
several unique characteristics (abnormal, irregular
uptake in any regional bowel strongly suggests
Crohn's disease) that favor its use as a diagnostic
modality in Crohn's disease. It is noninvasive, requires
no bowel preparation, and is safe in severely ill
patients in whom conventional imaging with barium
enema and endoscopy might be hazardous (WHORWELL and lSAACSON 1981). SAVERYMUTTU et al.
(1986) suggested that mln leucocyte scintigraphy
could distinguish Crohn's disease from ulcerative
colitis using the following criteria: skip lesions, right
side activity, and ileal disease, but this does not

appear to have been adopted into routine practice.
LI et al. (1994) have successfully established accurate diagnostic criteria for the use of 99Tcm-HMPAO
leucocyte scintigraphy in distinguishing Crohn's disease. They compared 99Tcm-HMPAO leucocyte scintigraphy with barium radiology in patients with
Crohn's disease. They found an accuracy for scintigraphy in diagnosing Crohn's disease which was significantly higher than the accuracy of radiology (98%
vs 86%, respectively).
Although radiology is used routinely in the diagnosis of inflammatory bowel disease, some studies
have shown that even high-quality barium examination can miss extensive inflammatory activity
(ELLIOT et al.1982; KINGHAM et al. 1982).
In 1983, SAVERYMUTTU et al., in a prospective study
of the accuracy of radiology and mln granulocyte
scanning in detecting inflammatory bowel disease,
found that 111 In granulocyte scanning was superior
(SAVERYMUTTU et al. 1983). The comparative accuracy of radiology and 99Tcm for Crohn's disease
was also investigated in this study. The accuracy of
99Tcm-HMPAO leucocyte scintigraphywas significantly higher than that of radiology in diagnosing Crohn's
disease. LI et al. (1994) conclude that leucocyte scintigraphy is not only important in the diagnosis of
inflammatory bowel disease and in determining its
event and activity, but also has a major role to play in
distinguishing Crohn's disease from ulcerative colitis.
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7.4 Radiology of Malabsorption

0. EKBERG and C.-H. FLOREN
CONTENTS
7.4.1
7.4.2
7.4.3
7.4.4
7.4.4.1
7.4.5
7.4.6
7.4.7
7.4.7.1
7.4.8
7.4.8.1
7.4.9
7.4.9.1
7.4.10
7.4.10.1
7.4.11
7.4.11.1
7.4.11.2
7.4.12
7.4.13
7.4.13.1
7.4.14
7.4.14.1
7.4.15
7.4.15.1
7.4.16
7.4.16.1
7.4.17
7.4.17.1
7.4.18
7.4.19
7.4.20
7.4.21
7.4.22
7.4.23
7.4.24
Introduction 339
Symptoms and Signs 340
Radiologkai Findings 340
Gastrinoma and Zollinger-Ellison
Syndrome 341
Radiological Findings 341
Bacterial Overgrowth Syndrome 343
Blind Loops 343
Diverticular Disease 344
Intestinal Pseudo-obstruction 344
Systemic Sclerosis 345
Benign Small-Bowel Stricture 345
Adult Celiac Disease 346
Complications of Adult Celiac Disease 348
Tropical Sprue 351
Amyloidosis 351
Whipple's Disease 351
Waldenstrm's Macroglobulinaemia 352
Intestinal Lymphangiectasia 352
Eosinophilic Gastroenteritis 353
Crohn's Disease 353
Ischaemic Disease 353
Radiation Enteritis 353
Short-Bowel Syndrome 355
Pancreatic Disease 355
Biliary Obstmetion 356
Gastroenteric Fistulae 356
References 356
0. EKBERG, MD, PhD

Professor, Department of Diagnostic Radiology, Malm University Hospital, 205 02 Malm, Sweden
C.-H. FLOREN, MD, PhD
Associate Professor, Department of Internat Medicine, University Hospital, 221 85 Lund, Sweden
7.4.1
lntroduction
The integrated processes of digestion and absorption

of nutrients from the small bowellumen can be disturbed at the luminal digestive phase, the mucosal
absorption phase or the removal phase. The word malabsorption is often used to cover two entities, i.e. maldigestion (for example due to pancreatic inefficiency)
and malabsorption (for example due to celiac disease)
(Table 7.4.1). The recognition of such malabsorption
syndromes is based mainly on clinical and biochemical laboratory tests as well as on mucosal biopsies
and histological findings. The intraluminal stage of
Table 7.4.1. Classification of malabsorption syndromes
1) Lack of intraluminal factors (maldigestion)
a) Lack of bile acid
i) Liver insufficiency and/or obstruction of bile flow
ii) Involvement of the terminal ileum
iii) Bacterial overgrowth
b) Lack of pancreatic exocrine function (involves fat and
protein)
i) Chronic pancreatitis
ii) Cystic fibrosis
iii) Obstructed pancreatic duct
iv) Zollinger-Ellison (due to inactivation of enzymes
bylow pH)
2) Abnormalsmall bowel mucosa (true malabsorption)
a) Malabsorption of specific substances
i) Lack of disaccharidases, i.e. lactase insufficiency
b) General malabsorption
i) Short bowel syndrome
ii) Celiac disease
iii) Bacteria and protozoans
( 1) Bacterial overgrowth
(2) Tropical sprue
(3) Whipple's disease
(4) Giardia lamblia
iv) Ischaemic disease
v) Crohn's disease
vi) Eosinophilic gastroenteritis
vii) Radiation enteritis
viii) Intestinallymphangiectasia
ix) Gastroenteric fistulas
x) Amyloidosis
xi) Waldenstrm's macroglobulinaemia
340
0. Ekberg and C.-H. Floren
normal digestion comprises the luminal hydrolysis of

One of the characteristics of malabsorption is the
fat and protein by gastric and pancreatic enzymes. lt presence of excessive amounts of dietary fat in the
also includes the Solubilisation of fat by bile salts. stool, i.e. steatorrhoea. A normal person consumes
The intestinal stage comprises degradation of partial- up to 150 g offat each day. Steatorrhoea is defined
ly hydrolysed carbohydrates by brush border disac- as more than 5 g of triglycerides in the faeces,
charidases and epithelial cell transport of monosac- assuming a dietary intake of 100 g/day. This can be
charides, fatty acids, monoglycerides, small peptides assessed by measuring faecal fat, which is a cumand amino acids.lt also includes the formation of chy- bersome method demanding collecting faeces for
lomicrons from triglycerides and cholesterol in epi- 3 days on a diet containing 100 g fat/day. Instead,
thelial cells. There is also a removal or a lymphatic nowadays, assessment of fat absorption is meatransport stage. This is important for the conveyance sured by the triolein breath test. The procedure is
of nutrients from the intestinal epithelial cells to other simple and involves oral administration of radiolaorgans for storage and metabolism. Diseases which belled triglycerides and subsequent measurement
interrupt any of these three stages can lead to ineffi- of radiolabelled C20 in the breath. The triolein
cient absorption of one or more constituents of food. breath test correlates weil with the results of faecal
fat determination. Mild malabsorption can easily be
handled by the patient by decreasing the amount of
fat in the diet. However, in advanced chronic pancreatitis andin a few instances of treatment-refrac7.4.2
tory celiac disease, passage of 20-40 g of fat per day
Symptoms and Signs
causes problems for the patient.
The main symptom of malabsorption is diarrhoea,
which is characteristically bulky and foul-smelling.
There is also usually weight loss, while in advanced
stages, muscle wasting and oedema may also be pres- 7.4.3
ent. Many patients complain of abdominal pain, flatu- Radiological Findings
lence, borborygmia and abdominal distension. These
symptoms are due to unabsorbed fatty acids, proteins For the diagnosis of specific disease entities causing
and carbohydrates in the Iumen of the small bowel. malabsorption, radiology plays a minor role. The diagParaesthesia, tetany and bone pain may be due to nosis is instead founded on histological examination
decreased vitamin B and calcium absorption. Museie ofbiopsies from the bowel, whether mucosal or transcramps and weakness may be due to excessive potas- mural. It is only of historic interest that flocculation,
sium loss. Decreased vitamin K absorption may i.e. clumping of bariumsulphate particles, was feit to
lead to easy bruisability, petechiae and haematuria. be diagnostic for malabsorption states like celiac disDecreased vitamin B12 and folate and/or iron absorp- ease, etc. (Fig. 7.4.1). Bariumsuspensions at that time
tion may lead to night blindness, glossitis, stomatitis were rather unstable and sensitive to weak acids and
bases. It is true that in many disease entities causing
and cheilosis.
With the use of ultrasound, CT and MRI, it is pos- malabsorption, there is an excessive amount of such
sible to diagnose and characterise disease entities that fluid in the bowellumen. Therefore, this phenomenon
was relatively common. Modern barium suspensions
may cause malabsorption such as pancreatic disease.
What usually brings the patient to a doctor is either use barium particles coated with citrate, which makes
symptoms of generalised malabsorption, e.g. weight them much more stable, as do other additives to the
loss and diarrhoea, or symptoms of specific malab- barium suspension. When flocculation is seen today,
sorption, e.g. paraesthesia due to vitamin B12 defi- it is more likely to be due to an excessive dilution of
ciency. In the clinical situation an astute clinician the barium suspension which per se makes it unstable
can detect signs of malabsorption, e.g. cheilosis, glos- and leads to flocculation.
The radiological barium examination merely serves
sitis, disturbed deep sensation, but he or she may also
detect pathological processes causing the malabsorp- to establish the differential diagnosis or more precisetion, for example a Crohn mass in the lower right ly pinpoint certain characteristics of a disease entity: a
abdomen or signs of alcoholism causing a chronic barium radiology study may serve to diagnose Crohn' s
pancreatitis. The clinical investigation may then be disease, a stricture, blind loops, diverticula, etc. It may
directed at the most plausible pathological conditions also be helpful for diagnosing complications to disease
entities causing malabsorption.
causing the malabsorption.
Radiology of Malabsorption
341
malabsorption is caused by inactivation of pancreatic enzymes by acid.

The diagnosis is usually suspected in patients with
intractable peptic ulcer disease, particularly if malabsorption is also present. Serum levels of gastrin
are elevated, and fasting serum gastrin levels greater
than 1000 pg/ml are diagnostic for the syndrome.
Administration of secretin causes a paradoxical rise
in serum gastrin to >200 pg/ml above the resting
levels in more than 90% of the patients with ZollingerEllison syndrome.
7.4.4.1
Radiological Findings
Gastrinomasare usually small, ranging from 0.1-20.0
cm in diameter. In at least half of the cases, they are
Fig. 7.4.1. Flocculation of barium sulphate suspension due
to excessive amounts of fluid in the small bowel Iumen in a multiple. Up to 75% of the gastrinomas have been
reported to be malignant. They are hypervascular
patient with malabsorption due to celiac disease
on CT. MRI reveals a high signal intensity on Tlweighted and T2-weighted images. They are usually
localised in the tail of the pancreas but may be
localised anywhere (Fig. 7.4.2a).An octreotide nucle7.4.4
ar medicine study is often the most sensitive test for
Gastrinoma and Zollinger-EIIison
detecting these lesions (Fig. 7.4.2b).
Syndrome
Endoscopic retrograde cholangiopancreatography
(ERCP) is no Ionger used for localising these lesions
Gastrinomas are endocrine tumours secreting exces- but may reveal the presence of ductal abnormalities
sive amounts of gastrins that may cause Zollinger- such as stenosis (Fig. 7.4.3a).
Ellison syndrome. This is characterised by severe
Upper gastrointestinal studies using barium or
ulcer disease in the stomach, duodenum and small iodine contrast media usually show large and mulbowel (WOLFE and JENSEN 1987). Increased gastric tiple ulcers in the stomach, duodenum and small
acid secretion is caused by the uncontrolled release of bowel. Mucosal folds in the stomach, duodenum and
gastrins from autonomously functioning non-beta- small bowel are usually thickened and deformed
islet cell tumours, the G-cells. This syndrome has (AMBERG et al. 1964; NELSON and CHRISTOFORIDIS
been estimated to be responsible for 0.1 o/o of all 1968). Perforation and fistulations may also be prespatients with duodenal ulcer. It is most common in ent (Fig. 7.4.3b). Excessive amounts of fluid may
patients between 30 and 50 years of age. Gastrinomas cause air-fluid levels on imaging with horizontal
may be part of the multiple endocrine neoplasia type X-ray beams as well as excessive dilution of contrast
I (MEN I) syndrome.
medium. The diarrhoea is primarily due to the severe
The clinical manifestation of Zollinger-Ellison volume load caused by the secretion of severallitres
syndrome is peptic ulcer disease due to excessive of acid into the intestines.
amounts ofhydrochloric acid in the stomach,duodeThickening of mucosal folds in the stomach and
num and small bowel (MAUSBACH et al. 1968). Such duodenum may also be present in other conditions
ulcers are less responsive to therapy than other ulcers. such as H. pylori gastritis, Menetriere's disease and
The syndrome should be considered in patients who lymphoma. That finding is therefore fairly non-spehave multiple ulcers, and ulcers in unusuallocations. cific. It is the simultaneaus presence of increased
Peptic ulcers occurring distally to the papilla ofVater, amounts of fluid and multiple ulcers that suggests a
especially if multiple and also involving the proximal Zollinger-Ellison syndrome.
duodenum, are highly suggestive of Zollinger-Ellison
syndrome. Complications such as perforation, haemorrhage and reflux disease are common. Secondary
342
Coronal
Fig. 7.4.2a,b. Gastrinoma of the pancreatic head. a Postcantrast CT scan. There is a well-vascularised 4-cm tumour in the
head of the pancreas (arrow). The tail of the pancreas shows
fatty infiltration (open arrow). b Octreotide scan shows uptake
in the tumour (arrow)
Fig. 7.4.3a,b. Zollinger-Ellison syndrome/gastrinoma. A 65-year-old man who presented with abdominal pain, diarrhoea and
weight loss. a ERCP reveals obstruction at the distal tip of the pancreatic duct (arrow). Surgery reveals a 1-cm-sized gastrinoma.
b Endoscopy showed multiple ulcerations. Barium study reveals an ulcer on the greater curvature of the stomach with perforation to the proximal jejunum (arrow). A nasogastric tube is located within the perforation. There are also at least two more
ulcers in the duodenum close to the Iigament of Treitz (open arrow). Mucosal folds in the proximal jejunum are broad and
somewhat irregular
343
7.4.5
7.4.6
There are high amounts of bacteria in the small

bowel, although not so overwhelming as in the
colon, 100,000 and 1 million bacteria per cm2,
respectively. These bacteria are all aerobic. Due to
a relative incompetence of the ileocecal valve, there
are many more bacteria in the distal part of the
ileum. Bacterial growth in the normal small bowel
is suppressed by the presence of gastric acid and
the rapid transportation of the small bowel contents
in the anal direction. Also, the rapid turnover of
enterocytes is counteractive in terms of bacterial
growth. It is calculated that the entire small bowel
mucosa is replaced every 2-4 days. There is also
a prevalent cellular immune defence system in the
small bowel wall, including secretion of antibodies.
When the content of the jejunum contains more
than 106 organisms/ml, this is considered abnormal
and may potentially cause symptoms such as malabsorption. Also, the presence of anaerobic bacteria
may cause symptoms.
The presence of excessive amounts of aerobic or
anaerobic bacteria may cause symptoms by three
mechanisms: (1) increased deconjugation of bile
salts. Conjugated bile salts are important for the
formation of micelies and thereby the absorption
of Iipids and lipid-soluble vitamins; (2) bile salts
and hydroxylated fatty acids per se are irritant to
the mucosa, especially the colonic mucosa, and may
thereby cause fluid and electrolyte secretion from
the intestinal wall; 3) the bacteria may also reduce
absorption of amino acids and carbohydrates. Overgrowth of bacteria may also cause a partial villous
atrophy.
The presence of excessive amounts of bacteria
in the distal small bowel is usually diagnosed by
a breath test measuring deconjugation of radioactively Iabelied conjugated bile salts; alternatively, to
measure a more proximal bacterial overgrowth, a
breath test measuring absorption of a radioactive
pentose (xylose) can be used. On clinical suspicion
of bacterial overgrowth and when an anatomical
defect is present, i.e. duodenal diverticula, antibiotics may be given in order to treat and test. If
the symptoms subside during this treatment, the
assumption is that the patient had a bacterial overgrowth syndrome.
In the bacterial overgrowth syndrome, radiology
plays an important role in order to reveal anatomical
prerequisites for the overgrowth, e.g. diverticula.
Patients who have undergone surgical procedures may

suffer from blind loops, i.e. when part of the small
bowel is excluded from the normal transportation.
Such blind loops may harbour bacteria which, due to
decreased peristalsis, may create an environment that
nourishes their excessive growth. Such a situation may
occur in Crohn's disease but also in patients who have
had different types of bypass operations due to cancers or secondary to metastatic disease.
However, there is also another iatrogenic variety
such as that found in patients after surgery for morbid
obesity. In such patients an anastomosis is created
between the mid-jejunum and distal ileum. In the Payne
procedure, 14 inches of jejunum is anastomosed to 4
inches ofterminalileum (PAYNE et al.1973) (Fig. 7.4.4).
Complications to this by-pass procedure are frequent
Bacterial Overgrowth Syndrome
Blind Loops
Fig. 7.4.4. Bacterial overgrowth, blind loop. A 40-year-old

woman with morbid obesity. She had undergone jejunoileal
by-pass surgery 1 year earlier. She now presented with diarrhoea and malabsorption. There is an anastomosis between
the jejunum and distal ileum (arrow). Contrast medium also
fills the by-passed, blindly ending ileum (curved arrow) that
contains retained material
344
(HocKING et al. 1983). In the excluded or blind loop

made up of the majority of the ileum and distal part
of the jejunum, bacteria may grow in excess.
7.4.7.1
they may also show irregular deformities. They may

be so prevalent that the ordinary small bowellumen
is difficult to identify. There is some correlation
between the total volume of the diverticula and the
prevalence of malabsorption. They may also occasionally perforate but usually only after a foreign
body has been impacted in them. Intestinal peristalsis and thereby transportation of barium or iodine
cantrast medium through the small bowel is usually
severely impaired in patients with jejunal diverticulosis. This may in fact be the cause of the diverticula.
It is extremely rare to have bacterial overgrowth
in a congenital diverticula, i.e. Meckel's diverticula,
although these may be very large. This is likely to be
due to the fact that such diverticula have an intact
muscularis propria and thereby are likely to empty
occasionally.
If the diverticula are limited to a relatively short
segment of the bowel, surgery may be contemplated.
Otherwise, antibiotics are the treatment of choice.
Small bowel radiographs easily visualise this type of

diverticula (Fig. 7.4.5). The diverticula are usually
rounded but may be elongated, and when inflamed
7.4.8
7.4.7
Diverticular Disease
Acquired diverticula of the small bowel are usually
located in the jejunum. They are due to herniations
of mucosa and submucosa at the mesenteric border
where the vasa recta are entering. Such diverticula
become more frequent with increasing age. They
are usually asymptomatic. Bacterial overgrowth may
result from stasis within the diverticula.
Intestinal Pseudo-obstruction
Pseudo-obstruction of the small bowel may be primary or secondary. Malabsorption is only an infrequent
finding in secondary pseudo-obstruction, but can be
highly expressed in primary intestinal pseudo-obstruction. The presenting symptom seems to be abdominal
pain that may vary from mild to severe. Patients with
severe symptoms due to intestinal pseudo-obstruction
may be extremely incapacitated due to the pain. The
cause of primary pseudo-obstruction is a visceral myopathy or neuropathy. Full-thickness biopsy specimens
are required for the diagnosis. Secondary pseudoobstruction has been associated with drugs and metahoHe disorders such as diabetes.
Treatment of intestinal symptoms like malabsorption relies on antibiotics to reduce the number of
bacteria. Surgery is contraindicated.
7.4.8.1
Fig. 7.4.5. Diverticular disease. A 84-year-old woman with

diarrhoea and malabsorption. Enteroclysis shows multiple
diverticula of the small bowel, up to 11 cm !arge, mostly in
the jejunum
The most common finding is that of dilated loops of

small and/or large bowel that contain long air-fluid
levels when images are obtained with horizontal X-ray
beams. During fluoroscopy no or very little peristaltic
activity is observed. The small bowelloops are usually dilated sometimes to an extreme extent (Fig. 7.4.6).
345
a
Fig. 7.4.6a,b. Pseudo-obstruction. A 18-year-old patient with long-standing abdominal pain, diarrhoea and malabsorption. a
Enteroclysis shows normal jejunum but a 1-m-long segment of the ileum is very dilated (arrow) . The terminal 30 cm of the
ileum are normal. b Transition (open arrow) between dilated and normalsmall bowel. The patientwas treated with antibiotics
and became asymptomatic
Thereby, the barium follow-through studyoften shows

an extremely prolonged transit time, often over 24
h. This prompts the prerequisite for bacterial overgrowth, which may lead to malabsorption.
7.4.9
Systemic Sclerosis
In systemic sclerosis small-bowel involvement has
been reported in up to 50% of the patients. The sclerosis of the intestinal wall including destruction of
the muscularis propria leads to a state similar to
pseudo-obstruction. This produces stasis and thereby bacterial overgrowth. However, collagen deposits
may also impair vascularisation of the intestinal wall
and per se cause malabsorption. Systemic sclerosis
also involves other organs like the oesophagus but
also the kidneys, lungs and heart.
In intestinal pseudo-obstruction, treatment of
intestinal symptoms like malabsorption relies on
antibiotics to reduce the number ofbacteria. Surgery
is also contraindicated.
7.4.9.1
The most characteristic finding during barium studies is the hidebound sign of the small intestine (PICKHARnT 1999), characterised by a combination of
lumen dilatation and crowded but normal-appearing
mucosal folds (Fig. 7.4.7). This is usually found in the
duodenum and proximal small bowel. Another characteristic finding is sacculation on the antimesenteric border of the bowel. This is due to muscle atrophy and collagen deposits in the longitudinal fibrous
tissue in the intestinal wall. Other manifestations
of scleroderma are hypomotility of the oesophagus
and/or stomach as well as constipation.
7.4.10
Benign Smaii-Bowel Stricture
Chronic obstruction of the small bowel whether due
to an infection, such as tuberculosis (Fig. 7.4.8}, or
Crohn's disease or any other chronic disease entity
346
Treatment is surgical resection of the affected loop

including both the stenotic and dilated segments.
7.4.10.1
A diagnosis of prestenotic dilated loop of bowel is

usually easy. Sometimes the stenosis per se is difficult
to localise but should be carefully looked for.
7.4.11
Adult Celiac Disease
b
Fig. 7.4.7a,b. Scleroderma with involvement of the small
bowel. a Dilation oflumen and crowded but normal-appearing
mucosal folds. b Sacculation on the antimesenteric border of
the bowel (Courtesy of S RuBESIN, MD, Philadelphia, Penn.,
USA)
(Fig. 7.4.9) may cause stasisproximal to the stenosis.

Within that usually moderately and eventually severely dilated loop ofbowel, stasis of content may appear.
This may form the prerequisite for bacterial overgrowth.
Adult celiac disease is a gluten-induced enteropathy

characterised by malabsorption due to lesions of
the small intestine caused by certain cereals in the
diet. The condition is diagnosed by a small-intestinal biopsy which reveals flattening and broadening
of the villi, sometimes to the extent of complete loss.
Lymphocytes, plasma cells and eosinophils infiltrate
the Iamina propria. The proximal jejunum is characteristically the segment most involved. The diagnosis
is confirmed by giving the patient a gluten-free diet,
which should be followed by resolution of the symptoms. Usually a follow-up biopsy is also done. lt is
the gliadin fraction of gluten that causes the disease.
Adult celiac disease is often associated with the gene
HLA-BR3. Antiendomycial antibodies can also be
detected in virtually all patients with celiac disease,
and such serological tests are now used for screening
for the disease. Adult celiac disease is common in the
Netherlands, Scandinavia and Ireland.lt is extremely
uncommon in Africans, Japanese and Chinese. Celiac
disease has a prevalence of 1:10,000 in ltaly and 1:200
in Denmark (CATASSI et al.1994; Boo and GuDMAND-HYER 1996)
The clinical diagnosis is that described above.
However, two-thirds of the patients with celiac disease have unusual or even misleading symptoms
(LosowsKY 1984). The presence of antiendomycial
antibodies is almost 100% specific for celiac disease. For a more precise diagnosis a mucosal biopsy
is mandatory. However, such a biopsy, when positive, is highly suggestive of celiac disease but is not
pathognomonic. lt may also be encountered in
bacterial overgrowth syndrome, Zollinger-Ellison
syndrome, different entities associated with AIDS
and also non-specific but severe infection (tropical
sprue).
347
7.4.11.1
Fig. 7.4.8. Tuberculosis. A 28-year-old man from Pakistan who

had had chronic pulmonary disease. He now presented with
abdominal pain, diarrhoea and malabsorption. There is a high
grade of obstruction at the ileocecal valve and caecum. The
caecum is minuscule. There is a prestenotic dilatation of the
terminal ileum. Surgery revealed tuberculosis
Most patients with non-tropical sprue (celiac disease)

have a normal small-bowel examination. Radiology
seldom plays a role in the diagnosis; however, in a
symptomatic patient sent for radiologic examination,
it is important that the radiologist recognise the features that may suggest the correct diagnosis (RUBESIN
et al. 1989). Radiology is mandatory in the diagnosis of
complications to celiac disease (RuBESIN et al. 1989).
The findings during the small-bowel followthrough include distension of the jejunum to more
than 3 cm across. This is a non-specific finding. As
described above, an excess of luminal fluid may cause
ft.occulation. This is also non-specific.
Dilatation of jejunalloops that appear atonic and
featureless and increased fold thickenings may occur
but is non-specific and usually indicates hypoalbuminaemia. During ft.uoroscopy, transient, painless intussusception has been reported (COHEN and LINTOTT
1978). When an enteroclysis is performed and causes
luminal distension, a separation or even absence of
mucosal folds in the jejunum is often noted. Five or
more folds per inchisanormal finding in the proximal jejunum. In three-quarters of the patients with
celiac disease, there are three or fewer folds per
inch of the distended proximal jejunum as revealed
during enteroclysis (HERLINGER and MAGLINTE
Fig. 7.4.9a,b. Non-specific stricture. A 80-year-old woman after

several episodes of mechanical obstruction of the small bowel.
She also had malabsorption. a Follow-through shows dilated jejunum with retained material. b Enteroclysis shows a tight stricture (arrow). Resection showed a non-specific, benign ulcer with
fibrosis and stricture, probably due to the use of NSAID
348
1986) (Fig. 7.4.10a). The duodenum may also be

affected in celiac disease (Fig. 7.4.10b ). The folds may
be fewer in number and also appear irregular.
In adult celiac disease the ileal folds are usually
more prominent and more numerous per inch than
normally seen. This has been called jejunisation of
the ileum (BovA et al. 1985). This fold pattern has
also been reported on CT examinations (ToMEI et al.
2000).
A mosaic pattern has been reported in adult celiac
disease. It is characterised on enteroclysis by a network of barium-containing growth, separating areas
1-3 mm in size (HERLING ER and MAGLINTE 1986).
Endoscopy may show the same abnormalities as
radiology, i.e. reduced or absent folds, scalloped folds,
mosaic appearance and mucosal fissures (GREEN et
al. 2000) (Fig. 7.4.11).
Patients who respond to a gluten-free diet usually
reverse their radiographic abnormalities and appear
with normal enteroclysis. Similarly, it has been reported that non-responders do not normalise radiographically. Enteroclysis has even been reported tobe more
reliable than biopsy in the evaluation of a response to
a gluten-free diet in adults with celiac disease (VAN
DEN BoscH et al. 1996).
Patients with refractory celiac disease, i.e. those
who do not respond to a gluten-free diet, may present with a variety of radiological findings, including
thick and irregular folds and a thickened bowel wall
(Fig. 7.4.12).
It has been shown that enteroclysis can contribute

significantly to the diagnosis of celiac disease and has
a high accuracy for the diagnosis. This is especially
true in the differentiation of celiac disease from
other mucosal abnormalities like viral enteritis, bacterial overgrowth, giardiasis, hypergammaglobulinaemia andlymphoma (RUBESIN et al.1992). Most important is, however, a small bowel examination for the
diagnosis of possible complications of celiac disease.
7.4.11.2
Complications of Adult Celiac Disease
Ulcerative jejunoileitis (Fig. 7.4.13) is usually seen in

the duodenum and proximal jejunum. It is thought
tobe due to vascular impairment of a particular segment of the small bowel. This may cause multiple penetrating ulcers, which may eventually lead to stricture
formation. These strictures may cause severe prestenotic dilatation and thereby symptoms of obstruction. Patients with adult celiac disease may even have
such strictures as the presenting symptom. This may
make the correct diagnosis difficult. Other simultaneaus features of celiac disease may lead to the correct diagnosis during the radiological studies.
Lymphoma is another complication of adult celiac
disease (Fig. 7.4.14).Small-bowel non-Hodgkin's Iymphoma is the most common malignancy complicating celiac disease. The characteristic feature of
Fig. 7.4.10a,b. Celiac disease. A 53-year-old man who presented with diarrhoea, weight loss and malabsorption. There is a
decreased number of mucosal folds in the jejunum (a) as weil as in the duodenum (b)
349
Fig. 7.4.lla-d. Celiac disease. Endoscopy of the duodenum in a patient with celiac disease shows: a reduced or absent folds, b
scalloped folds, c mucosal fissures, d the mosaic pattern which appears more clearly after indigo carmine application. (Courtesy
of E ToTH, MD, Malm, Sweden)
patients with this complication is that for years they

have been asymptomatic on a gluten-free diet. They
then suddenly present with abdominal pain and diarrhoea. These symptoms are difficult to distinguish
from symptoms that may be caused by a less strict
gluten-free diet.
Radiologically, these Iymphomas may be very difficult to diagnose. They are usually superficial. They
are usually overlooked at radiological examination.
When large and polypoid, they are easier to diagnose. These non-Hodgkin's Iymphomas may present
with only a large and irregular fold pattern. A stricture caused by ulcerative jejunoileitis may also mirnie
lymphoma.
Adenocarcinomas in the small bowel as well as in
other parts of the gastrointestinal tract are seen more
frequently in patients with celiac disease. Also, these
patients may present with symptoms indistinguish-
350
Fig. 7.4.13. Complications to celiac disease. A 55-year-old

woman with a long history of celiac disease. She became
asymptomatic on a gluten-free diet. The last couple of months
she has had epigastric pain, diarrhoea and intermittent vomiting. Barium examination of the upper gastrointestinal tract
shows massive dilatation of the horizontal part of the duodenum due to a stricture (arrow). There is a Iot of foreign material proximal to the stenosis
Fig. 7.4.12a,b. A 50-year-old man with refractory celiac disease.

a Enteroclysis shows broad mucosal folds with clubhing in the
jejunum. b CT shows thickening of the bowel wall (arrow)
able from celiac disease, including abdominal pain

and diarrhoea. However, recurrence of malabsorption is not present. Therefore, a carefully performed
small bowel examination is indicated in all patients
with known celiac disease who present with new
or recurrent symptoms, especially when they had
adhered to a gluten-free diet.
The cavitation of mesenteric lymph nodes represents
a rare complication of celiac disease whose pathogenesis is unknown. It has been reported especially in late
onset of the disease (BARDELLA et al. 1999). Histologically, the hypertrophic lymph nodes have a cystic centre
and milky exudate surrounded by normal lymphoid
tissue. On CT these lymph nodes appear enlarged and
hypodense (BARDELLA et al. 1999).
Fig. 7.4.14. Lymphoma. Patient with celiac disease who presented with abdominal pain and mild diarrhoea. Enteroclysis
shows 3-cm-long relative narrowing of the mid-ileum (ar row).
There are broadened and irregular mucosal folds. Surgery
revealed non-Hodgkin's Iymphoma
351
7.4.12
Tropical Sprue
7.4.14
Whipple's Disease
Tropical sprue can be a life-threatening acute condition. It affects individuals who are severely infected
with different gastrointestinal bacterial pathogens.
It is assumed that the bacteria are growing in large
parts of the small bowel lumen and that different
pathogenic bacteria are present. Patients may present
with malabsorption including megaloblastic anaemia. The radiographic finding in tropical sprue may
show lumen dilatation, thickened folds and flocculation. These findings are non-specific (CALDWELL and
BAlLES 1965}. Patients usually respond well to broadspectrum antibiotics.
Whipple's disease is an uncommon disease that may

affect virtually any organ system in the body. In
the majority of cases, the small bowel is involved
(RAMAIAH and BoYNTON 1998}. It is caused by the
organism Tropheryma whippelii, which is a grampositive actinomycete. The disease is characterised by
febrile illness, cachexia, malabsorption, increased skin
pigmentation, anaemia, lymphadenopathy, arthralgia, pleuritis, pericarditis, valvular endocarditis and
central nervous system symptoms (SWARTZ 2000).
This organism is found in glycoprotein-laden macrophages with characteristically small, rod-shaped,
gram-positive bacilli that are not acid-fast. Earlier,
the clinical course ofWhipple's disease generallyprogressed to a fatal outcome. The institution of appropriate antibiotic therapy induces prompt remission.
7.4.13
Amyloidosis
Patients with chronic inflammatory conditions like
rheumatoid arthritis may suffer from secondary amyloid deposition. Also, other chronic inflammatory
diseases like Crohn's disease may result in secondary
amyloidosis. In amyloidosis an eosinophilic glycoprotein that is insoluble is produced in high amounts.
The gastrointestinal tract is, however, infrequently
affected in secondary amyloidosis, but when present
it may cause pseudo-obstruction. In primary amyloidosis the gastrointestinal tract is involved in 70%
of patients. Primary amyloidosis can also affect the
tongue, heart, joints and kidneys.
7.4.13.1
Radiographie findings are uncommon. It has been

reported that a micronodular mucosal surface pattern can be found. Also larger polypoid protrusions
several centimetres in size have been reported occasionally in the small bowellumen (ARAOZ et al. 2000)
(Fig. 7.4.15). CT findings are non-specific but typically include symmetric wall thickening of the affected
small bowel (HORTON and FISCHMAN 1998}.
Fig. 7.4.15. Amyloidosis. A 84-year-old woman with chronic

rheumatoid arthritis. She has now developed amyloidosis of
the kidneys. She also has malabsorption. The mucosal folds of
the small bowel are broad and polypoid (Courtesy of A Kruse,
MD, Aarhus, Denmark)
7.4.14.1
The radiographic features of Whipple's disease

include thickening of the small-bowel folds and a
diffuse, patchy, micronodular pattern, predominantly in the duodenum and jejunum (Fig. 7.4.16). The
352
7.4.15.1
Radiologkai findings have been reported to include

thickening of the small bowel wall including distension
of mucosal folds (AsPELIN et al. 1989) (Fig. 7.4.17).
Other findings are hepatosplenomegaly and lymphadenopathy, including stranding of mesenteric and retroperitoneal fat.
7.4.16
Intestinal Lymphangiectasia
Fig. 7.4.16. Whipple's disease. Follow-through examination in

a patient with Whipple's disease. There is a diffuse pattern
of 1-2 mm sized micronodules (Courtesy of S. RuBESIN, MD,
Philadelphia, Penn., USA)
Lymphangiectasia may be due to a primary congenital malformation of the lymphatics that usually
involves various organs and affects the bowel. As a
result, the removal of nutrients from the intestine
into the portal and systemic circulation is impaired.
Lymph is leaking from the gut surface back into the
bowellumen. Secondary intestinallymphangiectasia
can be caused by several conditions that obstruct the
lymph fl.ow, such as retroperitoneal fibrosis or malignant infiltration of the retroperitoneum.
7.4.16.1
ileum appears normal. CT examination may reveal

low attenuation lymph nodes in the mesentery and
retroperitoneum.
Patients respond favourably to antibiotics, although
this must be prolonged for 1 year or more. Trimethoprim sulphamethoxazole is usually the most effective regimen.
The radiological diagnosis of intestinallymphangiectasia is non-specific and includes thickened folds

with numerous 2 mm or larger micronodules. The
folds may be distorted, and the bowel wall may be
thickened. A differential diagnosis between primary
7.4.15
Waldenstrm's Macroglobulinaemia
Waldenstrm's macroglobulinaemia is characterised
by a proliferation of malignant cells of lymphocytic
origin. The cell secretes a very high molecular weight
monoclonal immunoglobulin, which is an !gM-type
macroglobulin sometimes precipitating at low temperatures (cryoglobulin). Malabsorption is usually
not the predominant symptom. Symptoms are usually due to an increased plasma viscosity due to the
cryoglobulin. Patients usually present with general
fatigue and mental symptoms, visual disturbances
and Raynaud's phenomenon.
Fig. 7.4.17. Macroglobulinaemia. CT of the upper abdomen

in a patient with Waldenstrm's macroglobulinaemia showing multiple, enlarged, right para-aortic and mesenteric lymph
nodes (ASPELIN et al. 1989)
353
and secondary intestinallymphangectasias will need

to be based on abdominal ultrasound, CT and MRI
findings (HERLINGER 2000).
7.4.17
Eosinophilic Gastroenteritis
Eosinophilic infiltration of the mucosa may affect
the oesophagus, stomach, small bowel and colon.
Symptoms include malabsorption, but protein loss
can be apredominant feature, resulting in hypoalbuminaemia.
7.4.17.1
Radiographie features may include thickening of

small bowel folds that may be straight or rarely nodular. The distribution of the disease may be regional
or general. Another form of eosinophilic enteritis has
been described as involving predominantly the muscularis propria. This may cause narrowing of bowel
Iumen, simulating carcinoma, Iymphoma or Crohn's
disease (HERLING ER 2000).
Fig. 7.4.18. Crohn's disease. A 41-year-old woman with abdominal pain and diarrhoea with signs of malabsorption. Smallbowel follow-through shows widespread abnormalities of the
small bowel that involves almost the entire small bowel except
the proximal jejunum. There are broadened and fiattened
mucosal folds. Biopsy revealed Crohn's disease
7.4.18
Crohn's Disease
Patients with extensive Crohn's disease may develop
malabsorption. This may be due to widespread disease involving the jejunum and/or ileum (Fig. 7.4.18).
Other patients with Crohn's disease may present with
fistula formation. Such fistulae may cause blind loop
syndromes, which may Iead to bacterial overgrowth.
In patients with fistulae between the proximal or midsmall bowel and colon, malabsorption may be due to
the shorter contact time within the small bowel. Finally, Crohn's disease may cause obstruction, which may
Iead to bacterial overgrowth in the prestenotic dilated
loop ofbowel (Fig. 7.4.19; see chapter 7.3).
7.4.19
lschaemic Disease
Patients with severe and widespread intestinal vascular disease may suffer from extensive necrosis of the
mucosa and may end up with a non-functioning small

bowel (Fig. 7.4.20). This may be due to recurrent episodes of ischaemia such as in atrial fibrillation. Other
causes of chronic embolic disease may also Iead to this
uncommon situation. See chapter 7.1.
7.4.20
Radiation Enteritis
Patients who have undergone extensive radiation
therapy to the abdominal cavity may eventually end
up with severe darnage to the small bowel. Such a
radiation-induced intestinal disease may be acute
during the radiation therapy or occur years after
when the arterial supply of the bowel has been
impaired. This gives rise to mucosal ischaemia and
may Iead to severe transmural fibrosis (Fig. 7.4.21).
See chapter 7.1.
354
Fig. 7.4.19. Crohn's disease. Widespread Crohn's disease with

malabsorption. There are multiple stenoses leading to luminal
stasis and bacterial overgrowth
a
Fig. 7.4.20a,b. Ischaemic disease. Patient with polyarteritis nodosa with
manifestations from different organs. She also had severe malabsorption. a Small-bowel follow-through shows that both the jejunum and
ileum are without normal mucosal folds and there is a general narrowing of the bowellumen. b Angiography shows small aneurysms in the
branches of the superior mesenteric artery. There is also a larger aneurysm in a branch from the superior mesenteric artery to the liver
355
with ca+2 , and oxalate is absorbed, producing oxalate

stones in the urinary tract. Radiological findings may
reveal signs of adaptation which can include luminal
dilatation and thickened and irregular mucosal folds.
7.4.22
Pancreatic Disease
In patients with chronic pancreatitis, the exocrine
function of the pancreas may be severely impaired.
This may cause decreased pancreatic enzyme and
bicarbonate release. This is also the case in patients
with obstruction of the pancreatic duct due to carcinoma of the pancreas, while pancreatic enzymes
may be equally depleted in patients with cystic fibrosis. Patients with adult cystic fibrosis may therefore
develop malabsorption. The cause of the malabsorption is again that the exocrine pancreatic secretion is
viscous and low in bicarbonates and enzymes.
Fig. 7.4.21. Radiation enteritis. A 74-year-old woman who many

years previously had undergone radiotherapy due to carcinoma
of the ovaries. She now presented with malabsorption. There is
extensive involvement with radiation enteritis in the ileum. The
mucosal folds are broadened and somewhat irregular. There is
also narrowing in a segment of the ileum
7.4.21
Short-Bowel Syndrome
Patients who have undergone major resection of the
small bowel due to Crohn's disease, severe ischaemia
or any other cause may end up with short-bowel syndrome (Fig. 7.4.22). Whether or not the patient has
an intact colon is a crucial aspect. With a preserved
colon, the minimallength can be only 50-70 cm. In
case of total colectomy, 150 cm of small bowel is necessary (GOUTTEBEL et al.1989.)
If the jejunum is resected, the ileum may adapt and
take over some of the jejunal function. This is in
contrast to when the ileum is resected. This loss of
ileum cannot be metabolically replaced. Resection of
more than 40-50 cm of the distal ileum interrupts
the enterohepatic circulation of bile salts, which may
cause choleretic diarrhoea. Urinary stones of calcium
oxalate may arise when a long segment (over 100
cm) of ileum is resected. The fatty acids form soaps
Fig. 7.4.22. Short-bowel syndrome. The patient had undergone

ileocolectomy 2 years earlier due to widespread Crohn's disease. She developed malabsorption after surgery. There is only
1 m of jejunum left. The mucosal folds are normal
356
Radiological findings in patients with malabsorption due to pancreatic disease will include pancreatic
atrophy, chronic pancreatitis and pancreatic carcinoma. Patients with cystic fibrosis may have an atrophic
pancreas with dilated pancreatic ducts, filled with
viscous 'material.
7.4.23
Biliary Obstruction
In patients with long-standing biliary obstruction such as
in sclerosing cholangitis, an insufficient amount of bile
reaches the bowel. This severely disrupts the enterohepatic circulation and thereby causes malabsorption. The
radiographic findings are those ofbiliary obstruction.
7.4.24
Gastroenteric Fistulae
In patients with fistula formation between the stomach and the small bowel, rapid transit of nutrition
from the stomach into the small bowel may cause malabsorption (Fig. 7.4.23 and 7.4.24). The mechanism
is that the nutrients by-pass the pancreatic secretion
of enzymes, thereby causing inappropriate mixing of
enzymes and food. If such a condition cannot be surgi-
Fig. 7.4.24. Gastroenteric fistula. A 83-year-old woman who

presents with diarrhoea and malnutrition. Upper GI study
reveals a fistula between the postbulbar part of the duodenum
and colon. Fistula (long arrow), duodenal bulb (open arrow),
antrum (curved arrow), colon (small arrow)
cally repaired, the patient may be treated with pancreatic enzymes.
References
Fig. 7.4.23. Gastroenteric fistula. The patient presents with

diarrhoea and malabsorption. Upper GI study shows fistula
formation ( arrow) between the antrum of the stomach and the
jejunum. Endoscopy reveals a !arge benign ulceration
Amberg JR, Ellison EH, Wilson SD, et al (1964) Roentgenographic observations in the Zollinger-Ellison syndrome.
JAMA 190: 185-187
Araoz PA, Batts KP, MacCarty RL (2000) Amyloidosis of the
alimentary canal: radiologic-pathologic correlation of CT
findings. Abdom Imaging 25: 38-44
Aspelin P, Adielsson G, Dimitrov N, et al (1989) Abdominal
computed tomography in macroglobulinemia (Waldenstrm's disease).Acta Radiol30: 197- 199
Bardella MT, Troyalo C, Corbe D (1999) Mesenteric lymph
node cavitation: a rare hallmark of celiac disease. Scand J
Bod S, Gudmand-Hyer E (1996) Incidence and prevalence
of adult coeliac disease within a defined geographic area in
Denmark. Scand J Gastroenterol31: 694- 699
Bosch HCM van den, Tjon A Tham RT, Gooszen AW, et al
(1996) Celiac disease: Small-bowel enteroclysis findings in
adult patients treated with a gluten-free diet. Radiology
201:803-808
Bova JG, Friedman AC, Weser E, et al (1985) Adaptation of
the ileum in non-tropical sprue. Reversal of jejunoileal fold
pattern.AJR 144:299-392
Caldwell VL, Balles TN (1965) The importance and reliability
of the roentgenographic examination of the small bowel in
tropical sprue. Radiology 84: 227-240
Catassi C, Rtsch IM, Fabiani E (1994) Coeliac disease in the
year 2000: exploring the iceberg. Lancet 343: 200-203
Cohen MD, Lintott BJ (1978) Transient small bowel intussusception in adult celiac disease. Clin Radiol29: 529-534
Gouttebel MC, Saint Aubert D, Colette C, et al (1989) Intestinal
adaptation in patients with short bowel syndrome. Dig Dis
Sei 34: 709-715
Green PHR, Shane E, Rotterdam H (2000) Significance of
unsuspected celiac disease detected at endoscopy. Gastrointestinal Endosc 51: 60-65
Herlinger H (2000) Malabsorption. In: Gore RM, Levine MS
(eds) Textbook of gastrointestinal radiology, 2nd edn. Saunders, Philadelphia
Herlinger H, Maglinte DDT (1986) Jejunal fold separation in
adult celiac disease: relevance of enteroclysis. Radiology
158: 605-611
Hocking MP, Duerson MC, O'Leary JP, et al (1983) Jejunoileal
bypass for morbid obesity. Late follow-up in 100 cases.
NEJM 308: 995-999
Horton KM, Fishman EK (1998) Uncommon inflammatory
diseases of the small bowel: CT findings. AJR 170: 385-388
Losowsky MS (1984) The protean clinical manifestations of
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celiac disease. In: Ferguson A (ed) Advanced medicine.
Pitman, London, pp 48-60
Mausbach CM II, Wilkins RM, Dobbins WO, et al (1968) Intestinal mucosal function and structure in the steatorrhea of
Zollinger-Ellison syndrome. Arch Intern Med 121: 487-494
Nelson SW, Christoforidis AJ (1968) Roentgenologic features of
the Zollinger-Ellison syndrome: ulcerogenic tumor of the
pancreas. Semin Roentgenol3: 254-266
Payne JH, DeWind L, Schwab CE (1973) Surgical treatment of
morbid obesity: sixteen years of experience. Arch Surg 106:
432-437
Pickhardt PJ (1999) The "hide-bound" bowel sign. Radiology
213: 837-838
Ramaiah C, Boynton RF (1998) Whipple's disease. Gastroenterol Clin North Am 27: 683-695
Rubesin SE, Herlinger H, Sau! SH, et al (1989) Adult celiac disease and its complications. Radiographics 9: 1045-1966
Rubesin SE, Rubiner RA, Herlinger H (1992) Small bowel malabsorption: clinical perspectives. Radiology 184:297-305
Swartz MN (2000) Whipple's disease- past, present and future.
N Eng! J Med 342: 648-650
Tomei E, Marini M, Messineo D, et al (2000) Computed tomography of the small bowel in adult celiac disease: the jejunoileal fold pattern reversal. Eur RadiollO: 119-122
Wolfe MM,Jensen RT (1987) Zollinger-Ellison syndrome: current concepts in diagnosis and management. N Eng! J Med
317: 1200-1209
7.5 Radiology of Immunologie Disorders

H. HERLINGER
CONTENTS
Aspects of Immunology 359
T Lymphocytes 359
B Lymphocytes and Immunoglobulins 360
Natural Killer Cells 360
Cytokines 360
Gut-Associated Lymphoid Tissues 360
Peyer's Patches
and the Maturational Journey 360
7.5.1.7 Lamina Propria 360
7.5.1.8 Immunoglobulin Secretion 361
7.5.1.9 Intraepithelial Lymphocytes 361
Immune Deficiency Diseases 361
7.5.2
Primary Disorders of Immunity 361
7.5.3
7.5.3.1 Selective IgA Deficiency 361
7.5.3.2 Common Variable
Hypogammaglobulinemia 362
Secondary/Acquired Immune Disorders 363
7.5.4
7.5.4.1 Graft-versus-Host Disease 363
7.5.4.1.1 The Induction Protocol 363
7.5.4.1.2 Acute GvHD 363
7.5.4.1.3 Chronic GvHD 364
7.5.4.2 Smali-Bowel Transplantation 364
7.5.4.3 Post-Transplant Lymphoproliferative
Disorder 365
7.5.4.4 Immunoproliferative Small-Intestinal
Disease 366
7.5.4.5 Lymphangiectasia 367
Acquired Immune Deficiency Disease 367
7.5.5
7.5.5.1 Introduction 367
7.5.5.2 HIV Enteritis 369
7.5.5.3 Definition of AIDS 369
AIDS-Defining Infections 370
7.5.6
7.5.6.1 Cryptosporidiosis 370
7.5.6.2 Isosporiasis 370
7.5.6.3 Microsporidiosis 371
7.5.6.4 Cytomegalovirus Infection 371
7.5.6.5 Mycobacterium avium-intracellulare
Complex 371
7.5.6.6 Mycobacterium Tuberculosis 375
7.5.6.7 Bacillary Angiomatosis 375
7.5.6.8 Invasive Candidiasis 376
7.5.6.9 Extrapulmonary Pneumocystosis 376
7.5.1
7.5.1.1
7.5.1.2
7.5.1.3
7.5.1.4
7.5.1.5
7.5.1.6
7.5.7
7.5.7.1
7.5.7.2
7.5.7.3
AIDS-Related Tumors 376

Kaposi's Sarcoma 377
Non-Hodgkin's Lymphoma 377
Primary Effusion Lymphoma 380
References 380
7.5.1
Aspects of lmmunology
The epithelium of the small intestine covering its
villi and microvilli represents the hody's largest surface area in which host and environment interact.
To cope effectively with this task, the gut-associated
lymphoid tissue (GALT) has evolved into the largest
immunologic compartment of the hody. GALT is also
linked to other mucosal surfaces, such as hreast, lung,
and hiliary tracts, to form a common mucosa-associated lymphoid tissue (MALT).
Two types of immunity can he distinguished, the
natural and acquired forms. Natural immunity relies
on a numher of harriers such as gastric acid, hile
acids, intestinal mucus, the tight junctions hetween
epithelial cells, and on rapidly availahle cellular elements like phagocytes and natural killer cells. Specific immunity is composed of humoral and cellular
elements. Humoral immunity relies on B-cell-derived
antihoclies with mainly extracellular duties. Cellular
immunity is hased on T lymphocytes to protect the
system from harmful intracellular events. The ahility
to differentiate hetween foreign and self-antigens is
highly important, to exclude and remove the former
and talerate the latter.
7 .5.1.1
T Lymphocytes
MD
Professor of Radiology (Emeritus), Department of Radiology, University of Pennsylvania Medical Center, University of
Pennsylvania School of Medicine, Hospital of the University of
Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104-4283,
USA
H. HERLING ER,
T lymphocytes derive from pluripotential stem cells

in the hone marrow and migrate to the thymus for
Prepared by Prof. Gourtsoyiannis
360
H. Herlinger
further maturation. Antigens or antigen fragments

associated with components of the major histocompatibility complex (MHC) are recognized by T cells
when on the surface of antigen-presenting cells. The
antigen specific T-cell surface receptors are immunoglobulin-like heterodimeric glycoproteins. T cells can
be divided into those that express a CD4 glycoprotein
and recognize peptides of dass II MHC and those
that express CD8 glycoprotein and respond to dass I
MHC molecules.
can be autocrine, paracrine, or endocrine. Various

combinations of cytokines are produced with overlapping patterns of activity. For exaniple, interferon-a/b derived from macrophages or fibroblasts can
increase cellular natural immunity. Lymphocyte regulation, their growth and antibody synthesis, the activation of inflammatory cells, and the growth and
activation ofleukocytes are among the further effects
of cytokines.
7 .5.1.2
Gut-Associated Lymphoid Tissues
7.5.1.5
B Lymphocytes and lmmunoglobulins
B cells develop from hemopoietic stem cells in the

hone marrow and fetal liver. Expressed on the surface of B lymphocytes, immunoglobulin molecules
become donotypic receptors.After binding their cognate antigens, the surface immunoglobulins cause
activation and proliferation of the B cells, with the
generation of plasma cells which can secrete high
Ievels of immunoglobulins. Secreted immunoglobulins function as antibodies, traveling through tissue
fluids to bind to antigenic molecules identical to
those that originated their production.
Immunoglobulins expressed by B lymphocytes
contain two identicallight chains linked by disulfide
bridges to two identical heavy chains also linked to
each other by disulfide bridges. Hypervariable sectians within the chains permit somatic mutation of
gene sequences for interaction with a wide variety of
antigens.
7.5.1.3
Natural Killer Cells
Natural killer cells form about 10% of peripheral

blood lymphocytes and are an important part of
the natural immune system. By means of cell-mediated cytotoxicity, they are involved in the elimination
of tumor cells and in the inhibition of intracellular
pathogens. Their activity can be influenced by T-cellderived cytokines such as interleukin 2 (IL-2).
7.5.1.4
Cytokines
Cytokines are protein hormones secreted by a variety of cells of the immune system and by others such
as endothelium and smooth musde. Their functions
GALT tend to be divided into organized compartments - Peyer's patches and follide-associated epithelium- and a non-organized distribution through
the Iamina propria. A third immune compartment is
formed by the T-cell population of the epithelium.
7.5.1.6
Peyer's Patches and the Maturational Journey
Clusters ofM cells contained within the special epithelium overlying Peyer's patches and lymphoid
follides facilitate the transepithelial transport of
microorganisms and antigens to start a specific
mucosal immune response by lymphocytes and
macrophages (FREY and NEUTRA 1997; BLOOM and
BoEDEKER 1996). Naive T lymphocytes migrate
into Peyer's patches in search of an antigen
encounter. Activated lymphocytes start on a maturational journey towards the mesenteric lymph
nodes, and pass through the thoracic duct into the
peripheral blood to enter the Iamina propria as
B lymphoblasts. Under the influence of antigenactivated T lymphocytes that have completed their
own maturational journey, the lymphoblasts are
changed into immunoglobulin A (IgA)-secreting
plasma cells.
7.5.1.7
Lamina Propria
The effector portion of the Iamina propria consists

of T cells, B cells, plasma cells. natural killer cells,
phagocytes, and mast cells. About 60% of lymphocytes are T cells, including memory cells. B cells and
their progeny, plasma cells, are mostly concerned
with IgA synthesis and less with the production of
IgM, IgG, and IgE.
361
Radiology of Immunologie Disorders
7.5.1.8
7.5.3
lmmunoglobulin Secretion
Primary Disorders of lmmunity
Dimeric IgA is the major antibody secreted for the

immune protection of the intestinal tract (BLUMBERG 1999). IgA occurs in two subclasses, IgA1 and
IgA2. Because of its high er resistance against bacterial proteases, IgA2 is the subdass predominantly
found in intestinal secretions. Plasma-cell-derived
IgA can occur as a monomer but is more often
found in dimeric form, in which a polypeptide
called J-chain joins the two monomers. IgM can
also be found in dimeric form. A secretory piece
produced by epithelial cells selectively binds to the
J-chain containing polymerk immunoglobulins IgA
and IgM. The entire complex of secretory piece
and immunoglobulin (SigA or SlgM) is transported through the epithelial cell and released into the
intestinallumen. The secretory component protects
the immunoglobulin from degradation by proteolytic enzymes and other hostile substances (MEsTECKY et al. 1999). SigA is also secreted across
hepatocytes into the bile for the protection of the
mostproximal intestine. SlgA has antibacterial and
antiviral properties. It also blocks the absorption of
antigens.
With rare exceptions, adults are affected in only two

of this group of diseases; in these conditions, diagnostic radiology can be of at least limited value.
7.5.3.1
Selective lgA Deficiency
Up to 1 in 500 births have this more common primary immune defect. Most patients lack both serum
and secretory IgA1 and IgA2. However, the majority
of affected persons remain asymptomatic, mainly
because of the compensatory presence of an increased
number of IgM- and IgG-secreting cells. However,
chronic sinopulmonary infections are more common
than in the general population; the incidence of giardiasis is only minimally increased. Nodular lymphoid
hyperplasia (NLH) is the usual radiologic finding
(Fig. 7.5.1).
7.5.1.9
Intraepithelial Lymphocytes
Intraepithelial lymphocytes (IELs) are T lymphocytes located between epithelial cells; they normally
secrete cytokines to regulate epithelial cell function.
When activated, the T cells assume cytolytic capabilities for the immune surveillance of malfunctioning epithelial cells. The number of IELs is greatly
increased in conditions like graft-versus-host disease or gluten-sensitive enteropathy andin infections
such as cryptosporidiosis.
7.5.2
Immune Deficiency Diseases
Immune deficiency diseases can result from defects

(1) in the cellular portion of the immune system or
(2) in the quality or number of secretory products
or (3) in a combination of the two. These abnormalities can be congenital (primary) or acquired (secondary). Radiology plays a more significant function in
the latter group of immune disorders.
Fig. 7.5.1. Selective IgA deficiency, enteroclysis. Here 2- 3 mm

nodules separated by normal mucosa are seen throughout the
distal ileum. Reproduced with permission from HERLINGE&
et al. (1999)
362
H. Herlinger
7.5.3.2
Common Variable Hypogammaglobulinemia
Common variable hypogammaglobulinemia (CVH)

includes a group of deficiencies, most of them related to abnormal terminal differentiation of B lymphocytes into immunoglobulin-secreting cells (SMITH
and JANOFF 1999). As a result, levels of IgG, IgM, and
IgA are much reduced. Symptoms appear in the 2nd
or 3rd decade and affect about 1 in 100,000 of the
general population. Respiratory infections predominate. Diarrhea is a frequent feature and is usually due
to infection with Giardia lamblia. Anti-lamblia treatment may be effective, but recurrence of giardiasis
is usual. Other parasitic infections include Campylobacter (C. jejuni and C. fetus ), cryptosporidiosis,
strongyloidiasis, and salmonellosis. Cytomegalovirus infection during childhood continuing in a latent
state may reactivate to cause severe disease (DocKE
et al. 1994). Bacterial overgrowth with an increase
of anaerobes can be a further cause of diarrhea/
malabsorption. Splenomegaly occurs in 70% of
patients.
Sprue can be a presentation of CVH. The diagnosis
can be made by duodenojejunal endoscopic biopsy
to reveal villous atrophy together with a scarcity or
absence of plasma cells in the lamina propria, the
endoscopic hallmark of CVH. The condition is unresponsive to gluten withdrawal. A few cases of gluten-sensitive enteropathy have also been reported in
patients with CVH (BILLet al. 1997). About one-third
of patients with CVH develop atrophic gastritis and
pernicious anemia and are at high risk of developing
gastric Cancer (HERMASZEWSKI and WEBSTER 1993).
The increased rate of malignancies compared with
the general population has been estimated to be
47-fold for stomach cancer and 30-fold for lymphoma
(KINLEN et al. 1985). Secondaryamyloidosis has complicated several cases of CVH {SANCHEZ-POBRE et al.
1987).
Radiology. Nodular lymphoid hyperplasia is the

usual finding during small-bowel barium radiology.
The nodules are numerous, may extend through
much of the small bowel, are usually up to 5 mm in
diameter and occasionally larger (Fig. 7.5.2). NonHodgkin's lymphoma may co-exist with extensive
NLH (AGUILAR et al. 1987). The potential for malignant change of NLH was indicated by the demonstration of similarity in the monoclonal pattern
shared by the lymphoma with adjacent NLH (CAsTELLANI et al. 1992). Given this or a similar suitable
clinical setting, a radiologic diagnosis of associated
Fig. 7.5.2a,b. Patients with common variable hypogammaglobulinemia presenting with sinopulmonary infections. a Inverted
image of crowded 2-5 mm nodules extending through the
distal ileum, at times obscuring intervening mucosa or appearing to become fused (arrows). b More pronounced Iumen distention together with fold thickening demonstrates multiple
nodules tangentially on the side of folds in a somewhat flattened state (small arrows); a few nodules are almost 1 cm
in diameter (open arrows). a, b Reproduced with permission
from HERLINGER et aJ. (1999)
giardiasis can be suggested by enteroclysis (Fig.

7.5.3). Duodenal and proximal jejunal folds are
mildly thickened with marked irritability that allows
only brief periods of lumen distention.
Fig. 7.5.3. In another patient with hypogammaglobulinemia,

giardiasis was radiologically suggested by intense irritability
that allowed only brief Iumen distention by enteroclysis with
the demonstration of nodularity (small arrows); note pronounced fold thickening in the duodenum (arrow). Reproduced with permission from HERLING ER et al. (1999)
7.5.4
Secondary/Acquired Immune Disorders
7.5.4.1
Graft-versus-Host Disease
Bone marrow for transplantation - the graft - is usually obtained by repeated aspiration from the posterior iliac crest of the donor for subsequent intravenous
injection into the recipient - the host. The purpose is
to re-establish hone marrow function. Graft-versushost disease (GvHD) is its all too frequent complication. GvHD reactions are primarily due to mature
donor T cells within the graft that recognize as foreign and attack the recipient's major histocompatibility complex (SHANAHAN and TARGAN 1999}. Material
used for transplantation is usually allogeneic, donor
derived. Rarely will the donor be an identical twin a synergeic transplantation- or an HLA-matched sibling. Alternatively, an unmatched donor will have to
be used, in which case the prior removal of donor T
cells from the graft may improve the prognosis of the
transplantation (FERRARA and DEEG 1991). However,
the therapeutic potential of the hone marrow transplantation may have to depend on a specific graft-versus-leukemia reaction which would be negated by the
elimination of donor T cells and natural killer cells
(HILL et al. 1999).
363
Autologaus transplantation implies the use of

the patient's own marrow. This technique may have
its place in patients with advanced malignancies
in whom preliminary high-dose radiochemotherapy
has destroyed much of the tumor cellload. Hematopoietic stem cells derived from peripheral blood or
from hone marrow are purged of malignant cells and
are then re-infused (SACHA et al. 1999}.
Indications for marrow transplantation include
aplastic anemia, severe childhood immunodeficiency
disorders, the lymphoblastic and myelogenous leukemias, non-Hodgkin's lymphoma, Hodgkin's disease,
multiple myeloma, and disseminated breast carcinoma. Adverse reactions tend to be more intense with
advancing age, and marrow transplantations are usually contraindicated for a patient over the age of 60
years. However, autologous hematopoietic transplantations may be extended to older patients.
7.5.4.1.1
The lnduction Protocol
High-dose chemotherapy with or without radiation

is used to ablate tumor cells within the hone marrow
and to prevent or reduce host-versus-graft reactions.
The induction protocol, however, also causes acute
necrosis of the intestinal epithelium, clinically presenting with abdominal pain and diarrhea. Bacterial, viral, or fungal contaminations may occur at this
stage. The intestinal epithelium is usually re-established by the end of 3 weeks.
7.5.4.1.2
AcuteGvHD
Acute GvHD may begin 3-4 weeks after transplantation. It consists of a combination of enteritis with
desquamation, a maculopapular rash over the trunk,
palms, and feet, and liver darnage indicated by elevated bilirubin levels. Bleeding due to ulceration in the
stomach, esophagus, or intestine is likely to be CMV
infection related. Prophylactic administration of acyclovir has been shown to reduce the incident of this
complication (MEYERS et al. 1988). Protein loss from
the gut may cause hypoalbuminemia.
Radiology. Barium studies and CT have shown the

ileum to be more severely affected than the jejunum,
with wall and fold thickening, lumen narrowing, and
likelyulcerations (Fig. 7.5.4). Changes mayextendinto
the colon. Mucosal sloughing can be pronounced and
extensive. A consequence of severe ulceration in the
small bowel as weil as colon may be the incorporation
364
H. Herlinger
Fig. 7.5.4a-c. Acute graft-versus-host disease (GvHD). Inverted

bariurn follow-through irnage shows (a) irregular fold thickening in the jejunurn and (b) reduced Iumen diarneter with
loss of fold pattern and likely shallow ulceration (arrows) in
the distal ileurn. c In the sarne patient, CT with intravenous
contrast shows in cross-section and longitudinally enhancernent of the rnucosa and serosal area with rnarked wall
thickening (arrows). a-c Reproduced with perrnission frorn
HERLINGER et aJ. (1999)
of barium underneath reforming mucosa, producing

persistent coating shown by plain films or CT (JoNES
et al. 1988; HoRTON et al. 2000) (Fig. 7.5.5). The same
effect has also been described following ulceration in
ischemic colitis (GREVES et al.1976).
Endoscopy. Biopsies from the stomach or duodenum

may demonstrate crypt epithelial apoptosis, crypt
destruction, and lymphocytic infiltration. More severe
changes such as mucosal sloughing are likely to be
found more distally (PoNEC et al. 1999).
tures are now a mucositis of the oral cavity and the

presence of fibrosis and bandlike stricturing in the
proximal esophagus. Dysmotility and fibrotic changes are seen in the small intestine and can be associated with bacterial overgrowth. Late complications
include a 10-fold increase over the general population of carcinomas of the oral cavity, esophagus, and
thyroid (KOLB et al. 1999).
7.5.4.2
Smaii-Bowel Transplantation
7.5.4.1.3
Chronic GvHD
Chronic GvHD makes its appearance 80-400 days

after the transplant. It may develop in continuity with
a subacute extension of the acute disease or may
occur without prior indication of GvHD. The skin,
liver, and intestinal tract are affected, but major fea-
The number of small-bowel transplantations is steadily

increasing with improvement of the rate of graft survival. Two-thirds of the patients are children or teenagers (GRANT 1999). Cadaver jejunum forms the more
usually transplanted material, but occasionally living
donor jejunum has been used (GRUESSNER and SHARP
1997). The major cause of transplantation-related prob-
365
Fig. 7.5.5a,b. GvHD, acute stage. a Barium follow-through and

b CT demonstrate barium coating 48 h after its administration; denudation of the mucosa seems to be the associated
pathology. a Reproduced with permission from HERLING ER et
al.(l999)
lems are graft rejection, possibly associated with infection, and the post-transplant lymphoproliferative disorder (PTLD) (SHANAHAN and TARGAN 1999). lnfecting agents include CMV and Epstein-Barr virus, the
latter also related to the development of PTLD.
The main indication for small-bowel transplants
is irreversible intestinal failure in patients in whom
total parenteral nutrition has become impossible. The
small bowel may be transplanted alone or in combination with the liver. The use of the immunosuppressant tacrolimus has increased transplant and patient
survival (THOMPSON 1999). A world survey has shown
intestinal graft survival to be 69%, and 66% when
combined with liver transplantation; 77% of the survivors could resume oral nutrition (GRANT 1999).
7.5.4.3
Post-Transplant Lymphoproliferative Disorder
Heart and heart/lung post-transplant patients have a
higher incidence of lymphoproliferative complications
than do liver or kidney transplantations. Between 3%
and 5% of solid organ transplantations develop PTLD
about 4-6 months after surgery. Patients rece1vmg

cyclosporine as the immunosuppressant are more likely
to develop the lymphoproliferative disorder. Most
patients with this complication testpositive for EpsteinBarr virus (EBV). Cyclosporine inhibits the suppressive
action of cytotoxic T lymphocytes directed against the
lymphoproliferative stimulus of active EBV (STARZL et
al. 1984). Regression or even resolution of the lymphoproliferation can follow a reduction or discontinuation
of the use of cyclosporine (STARZL et al. 1984) or its
replacement by tacrolimus. Lymph nodes, the GI tract,
lungs, liver, and spieen are likely tobe involved. Ulceration of GI lesions with bleeding and even perforation
will necessitate surgical intervention.
Radiology. Among 15 patients who developed PTLD,

barium studies have demonstrated ileal changes
in 3 - submucosal masses and pneumoperitoneum
(TUBMAN et al. 1983). A more recent paper (PICKHARDT and SIEGEL 1999) reports that in about half
the cases of PTLD, the lesions were confined to
the abdomen and could be outlined by CT. Liver
lesions and abdominal nodal metastases predominated. Unlike lymphoma in immunocompetent patients,
366
PTLD involvement of the small bowel exceeds or

equals that of the stomach (PICKHARDT and SIEGEL
1999). In a report of PTLD following liver transplantation in a patient who presented with abdominal pain, bleeding, obstruction, and perforation, CT
demonstrated a distended jejunum with gas-containing masses that extended through part of the bowel
wall (CHEZMAR 1997) (Fig. 7.5.6a); of interest are the
highly vascular tumor nodules shown in the mucosa
of the resected loop of jejunum (Fig. 7.5.6b ). Following cardiac transplantation, a further patient developed duodenal and gastric antral masses together
with multiple tumors in the liver (Fig. 7.5.6c, d).
7.5.4.4
lmmunoproliferative Small-lntestinal Disease
Immunoproliferative small-intestinal disease (IPSID)

is the term proposed by the World Health Organiza-
H. Herlinger
tion in a report on alpha-heavy-chain disease (WHO

1975). The disease was first recognized in the Middle
East and affected patients of Arab and Mediterranean
Jewish origin and smaller numbers of other people
living around the Mediterranean shore. Substandard
Ievels of hygiene cause intestinal colonization with
a microbial and parasite Ioad which appears to be
a stimulus towards the formation of a diffuse lymphoplasmacytic intestinal infiltrate (KHOJASTEH et
al. 1983). This infiltrate may already be associated
with IgA heavy-chain protein secreted by plasma
cells in the Iamina propria and detectable by immunofiuorescence (FINE and STONE 1999). Eventually,
the cellular infiltrate includes an increasing number
of malignant lymphocytes and extends into all the
layers of the bowel wall and into the mesentery to
constitute the Mediterranean form of Iymphoma.
Alpha-heavy chains produced by the neoplastic B
lymphocytes are a characteristic feature of Mediterranean Iymphoma. Table 7.5.1 indicates some of the
c
Fig. 7.5.6a- d. Post-transplant lymphoproliferative disorder (PTLD). a CT after liver transplantation. Dilated jejunum contains
blood and gas bubbles; tumor and gas extend into and through the bowel wall (arrows). b Postsurgical specimen reveals several
hemorrhagic tumor nodules studding the mucosal surface. (Courtesy of ]. L. CHEZMAR, MD). In a further patient in whom
PTLD developed after cardiac transplantation, CT demonstrates tumor formations (c) in the duodenum and gastric antrum
and (d) in the liver. (Courtesy of E. ]. BALTHAZAR, MD)
367
clinical differences between Mediterranean and nonHodgkin's lymphoma.

Treatment can be successful if the disease is recognized in the pre-lymphoma stage. An unusual case
already at the lymphoma stage with alpha-heavychain disease was associated with Helicobacter pylori-related MALT lymphoma of the duodenum and
regressed completely after repeated chemotherapy
(FISCHBACH et al.1997).
Radiology. Enteroclysis used in the diagnosis of a Japanese patient demonstrated a micronodular mucosal
pattern indicating lamina propria infiltration with distention of the villi, in that case a feature of IPSID in
the pre-lymphoma phase (MATSUMOTO et al. 1990).
CT and barium studies - follow-through and enteroclysis- recording the progress of IPSID in an American patient showed extensive nodularity getting more
irregular and larger, later with fold thickening and
increasing separation of bowelloops (Fig. 7.5.7); the
histology changed from polyclonallymphoid nodular
hyperplasia to monoclonal non-Hodgkin's lymphoma.
Barium studies of established Mediterranean Iymphoma are characterized by significant bowel loop displacement by mesenteric tumor masses (Fig. 7.5.8).
7.5.4.5
Lymphangiectasia
Intestinal and serosal lymphatic channels become

dilated as a result of an obstruction to lymph flow
through the mesentery. This may be a primary condition and part of generalized lymphatic hypoplasia,
or secondary to flow obstruction by fibrosis, tumors,
and other conditions affecting the mesenteric or retroperitoneallymph nodes. The primary form appears
in late childhood or early adult life. In addition to
protein loss, lymphoenteric fistulae may form with
outflow of lymphocytes, mostly T cells, thus interrupting their recirculation. This will be accompanied by hypoproteinemia, hypoalbuminemia, and
marked hypogammaglobulinemia with impairment
ofhumoral-mediated immunity.
Table 7.5.1. Western versus Mediterranean Iymphoma
Western
Iymphoma
Patients 5th-6th decade, M>F, segmental

may be multiple, early metastases to liver,
spleen, lymph nodes
Mediterranean Patients 2nd-3rd decade, M=F, diffuse infillymphoma

trate, extraintestinal involvement unusual.
Alpha-heavy-chain disease
Radiology. Lymph flow obstruction produces bowel

edema with widening of the submucosa and associated fold thickening. It also causes dilatation of the lacteals within the villi, to produce villous enlargement
and a micronodular surface pattern of the mucosa
best shown by enteroclysis (AoYAGI et al. 1994) (Fig.
7.5.9). CT will demonstrate the causes of secondary
lymphangiectasia.
7.5.5
Acquired Immune Deficiency Disease
7 .5.5.1
lntroduction
In the USA, the widespread availability of the highly

active retroviral therapy has slowed the rise in
the incidence of AIDS. The high cost of this treatment, however, has rendered it largely unavailable to
patients in sub-Saharan Africa, the most important
endemic area for AIDS.
The mucosa of the genital area remains the most
frequent mode of entry ofHIV-1 (KAHN and WALKER
1998). The lower GI tract is the usual portal of entry
for HIV -1 in homosexuals. The massive lymphoid
organ in the mucosa of the upper gastrointestinal
tract becomes the site of entry for the macrophagespecific HIV-1 when introduced with donor-contaminated material; it also becomes an important environment for HIV-1 replication (ORTIZ et al. 1999) and
seems to be the primary site for the decline of CD4+ T
lymphocytes (MuSEY et al. 1997). The GI tract is also a
major site for opportunistic infections and malignancies that characterize this disease.
Detectable viremia follows infection within 4-11
days (KAHN and WALKER 1998). Plasma levels of
HIV-1 RNA were high within 120 days after acquisition and then declined at a rate of about 6.5o/o per
week (ScHACKER et al. 1998). The CD4 cell count
decreases to a median of 500 cells/mm3 during 40
months following seroconversion (ScHACKER et al.
1998). However, there is wide variability in these early
virologic and cellular events. Generally, patients with
high er plasma levels of HIV1-RNA after day 120 from
acquisition were likely to show a more rapid decline
in the CD4 cell count.
An acute seroconversion syndrome develops in
30o/o-60o/o of patients and resembles infectious mononucleosis (SCHACKER et al. 1998). Diarrhea, esophageal ulcers, lymphadenopathy, and a maculopapular
368
H. Herlinger
d
.i
Fig. 7.5.7a...d. Immuneproliferative small-intestinal disease (IPSID). A 44-year-old female patient presented with a 2-month
history of diarrhea.and weight loss. a CT after barium and intravenous centrast demonstrated a thickened small bowel with
nodularities; no significant lymph node enlargement was seen. b Barium follow-through 1 month later revealed diffuse nodularity in the 2-3 mm size range; endoscopic biopsy demonstrated nodular lymphoid hyperplasia of polyclonal type. c After 2
months of treatment, enteroclysis showed more pronounced crowding of 2-4 mm nodules. d After 3 months of treatment,
enteroclysis outlined !arger nodules with pronounced fold thickening; the surgical biopsy was now interpreted as non-Hodgkin's
Iymphoma. (Courtesy of K. C. CHo, MD)
rash may be clinical features of this syndtorne and

rnay be a consequence of dissernination of HIV-1 ;
of an inadequate immune response, and/or of the
expression of cytokines (KAHN and WALKER 1998).
In the course of its dissemination, glycoprotein
120 of the AIDS virus is bound to the CD4 rnolecule
on the surface of helper T lyrnphocytes and also of
rnacrophages and rnicroglial cells (BLOOM and BoE-
DEKER 1996). The virus then gains entry into these

cells, rnultiplies within them to release large nurnbers of virions about one and a half days later, causing cell death. lt has been estirnated that sorne 10
billion virions are produced every day during active
disease, destroying about 2 billion CD4+ lyrnphocytes to cause their significant depletion (PERELsoN et al. 1996); as CDs+ T cells are only slightly
369
7.5.5.2
HIV Enteritis
This entity which presents with diarrhea of short or

more prolonged duration is part of the acute seroconversion syndrome, may be its only clinical expression,
or may be associated with other HIV-associated conditions like esophageal ulceration or aseptic meningitis. To attach to it the diagnosis ofHIV enteritis, the
diarrhea should be associated with the tissue presence
of HIV -associated core protein p24 (KOTLER et al.
1993), and tests for other causative organisms should
be negative. Radiology has rarely contributed to the
diagnosis of HIV enteritis; however, a CT study has
shown features of extensive enteric mural edema,
intraluminal fluid increase, and the presence of numerous, barely enlarged mesenteric nodes (Fig. 7.5.10}.
7.5.5.3
Fig. 7.5.8. Patient from Israel with proven Mediterranean
Iymphoma. Barium study demonstrates irregular nodularity
throughout the small bowel with a !arge mass in the ileocecal
region (arrows)
Definition of AIDS
There can be no sharp boundarybetween HIV-1 disease and the commencement of AIDS. AIDS can be
defined as a further deterioration of immune deficiency characterized by significant infections caused
by normally opportunistic contaminants and by certain tumors such as Kaposi's sarcoma. AIDS-defining
disorders have been listed by the World Health Organization and by the Center for Disease Control and
Prevention (CDC).Although additional diseases have
been added over the years, a recent paper has suggested further widening of the scope of AIDS-defin-
Fig. 7.5.9. Patient with primary lymphangiectasia unchanged

from an enteroclysis done 4 years earlier. There is slight fold
thickening together with grouped nodules in the 2 mm range
(open arrows to some of them). Reproduced with permission
from HERLINGE R et al. (1999)
decreased, a reduced ratio of CD4+ to CD8+ T cells

results. Surviving CD4+ T cells show an impairment
of function, with inadequate differentiation into
IgA-secreting cells (SMITH and MAI 1992}. Once the
number of CD4+ T cells has been reduced to about
200 per mm3 , numerous normally nonpathogenic
organisms become capable of causing AIDS-defining clinical infections.
Fig. 7.5.10. CT of enteritisinan HIV-positive patient with fluid

within the bowellumen. Numerous lymph nodes about 1 cm in
size are seen in the mesentery. (Courtesy of S. D. WALL, MD)
370
H. Herlinger
ing diseases to take account of the global expansion

of this disease (ALBRECHT 1997).
7.5.6
AIDS-Defining lnfections
Chronic diarrhea with watery stools lasting a month
or Ionger is often associated with cramps, fever, and
wasting. Such patients have low levels of CD4 T lymphocytes, and cases with only 50 CD4 T lymphocytes
per mm 3 arenot unusual.
7.5.6.1
Cryptosporidiosis
Thick-walled oocysts of Cryptosporidium parvum pass

through the stomach unaffected by its acid environment. The unicellular protozoan excysts in the small
bowel to reside outside the cytoplasm of the intestinal
epithelium in a parasitophorous vacuole formed by the
cell membranes (SMITH and WILCOX 1999). Waterborne outbreaks or zoonotic infections from calves
causing an acute diarrhea of 1-2 weeks' duration are
examples of infection by C. parvum in immunocompetent persons. In AIDS patients, cryptosporidiosis produces a cholera-like illness with passage of up to 20 L of
nonmucoid fluid.
The distribution of C. parvum in affected AIDS
patients was found to vary between panenteric, duodenal, ileocolic, or mid-enteric (KELLY et al.1998). In an in
vitro model, the disruption of the epithelial cell barrier
by the oocysts of C. parvum (Fig. 7.5.11) was shown to
be a cause for the clinical features of the disease (ADAMS
et al. 1994). Biliary tract infection by C. parvum is a
frequent complication of intestinal cryptosporidiosis in
AIDS patients (VERDON et al. 1998). Stool examination
for cryptosporidia is frequently positive in more severe
disease. Endoscopic biopsy from the terminal ileum has
been reported to be more sensitive than when taken
from the duodenum (GREENBERG and CELLO 1996).
However, an enzyme-linked immunosorbent assay of
stool specimens for Cryptosporidium was reported to
have a sensitivity of 100% (PARIS! and TIERNO 1995).
No reliably effective medical therapy is presently standardized, although the use of paromomycin is usually
recommended. Colostrum-derived bovine immunoglobulin concentrate, when used in powder form in
AIDS patients with severe diarrhea due to C. parvum,
was reported to have caused a significant decrease in
stool weight and frequency (CRABB 1998).
Fig. 7.5.11. Magnified view of oocysts of C. parvum (arrows)

occupying almost the entire epithelial surface of a villus
Radiology. Barium studies are not appropriate in
acute disease, when er may demonstrate extensive

enteric edema, wall thickening, and luminal fluid.
In less severe disease, barium follow-through examinations have shown fluid-containing bowel with
thickened folds, a nonspecific finding. Ultrasound
may demonstrate dilation and wall thickening of
the bile ducts and gallbladder when affected by
cryptosporidiosis.
7.5.6.2
lsosporiasis
The protozoan parasite Isospora belli passes through

an alternating sexual and asexuallife cycle. Unlike C.
parvum, it enters into the cytoplasm of enteric epithelial
cells, and humans are its only known reservoir (SMITH
and WlLCOX 1999). Isosporiasis is infrequently responsible for chronic diarrhea in European patients with
AIDS. In African countries, it is a common cause of
AIDS-related chronic diarrhea and weight loss ('slim
disease') (FISSEHA et al. 1998; DIENG et al. 1994). A case
report describes a unique black female patient who died
of AIDS-related chronic diarrhea and was found to have
I. belli tissue cysts in her lymph nodes, spieen, and liver
371
(MICHIELS et al. 1994). The diagnosis can be made from

stool sarnples by flotation technique after 1-2 days'
incubation at room temperature to promote maturation of the tiny oocysts. The radiologic findings resemble those in cryptosporidiosis.
7.5.6.3
Microsporidiosis
Microsporidia are intracellular, spore-forming protozoa and are ubiquitous in nature. Microsporidia are an
infrequent cause of traveler's diarrhea, usually in persons returning from tropical countries (LoPEZ-VELEZ
et al. 1999). Such infections are self-limited in immunocompetent persons. More significant and much
more frequent is microsporidial contamination of the
small intestine in immunodeficient patients, especially in AIDS. There are 4 genera of microsporidia of
which Enterocytozoon bieneusi and E. intestinalis can
be a cause of intestinal disease. E. bieneusi can also be
associated with biliary disease, and E. intestinalis can
disseminate widely (KOTLER and RENSTEIN 1998).
Microsporidia have been identified in up to 50%
of AIDS patients with chronic diarrhea (KoTLER and
RENSTEIN 1994). Microsporidial enteritis then presents with weight loss, abdominal pain, fever, and diarrhea, a result of microsporidia entering intestinal
cells to cause extensive cell death. Due to the small
size of the microsporidia, fecal staining with modified trichrome blue is needed for identification by
light microscopy (LEDER et al. 1998). Endoscopic
biopsy specimens and brush cytology can also be
used for the microscopic identification of microsporidia in stained preparations. Intestinal radiology has
little to offer towards the specific diagnosis.
7.5.6.4
Cytomegalovirus lnfection
Human cytomegalovirus (CMV) can enter into and

multiply within epithelial and endothelial cells, fibroblasts, circulating leukocytes, smooth muscle cells,
and hepatocytes (SINZGER et al. 1995). The initial
infection is often asymptomatic in the immunocompetent host and tends to continue in a state of latency over many years (SMITH and WILCOX 1999). Any
deterioration of the immune status, especially AIDS
with CD4levels below 200/mm3, leads to their reactivation, with the production by macrophages of cytokines including tumor necrosis factor (TNF)-a, and
to viral penetration into most of the cellular compo-
nents of the intestinal mucosa. Viral inclusion bodies

are more often found in mesenchymal and endothelial cells than in the epithelium of the mucosa. CMV
infection can involve the entire GI tract from the
esophagus to the colon and rectum. The presence of
cellular inclusion bodies, both intranuclear and cytoplasmic, characterizes CMV disease. Bleeding, ulcerations, and perforation are frequent complications of
intestinal tract involvement. CMV disease can also
affect the biliary system, causing sclerosing cholangitis, papillary stenosis, or acalculous cholecystitis.
Diagnosis based on endoscopic biopsy may demonstrate typical intranuclear inclusions surrounded by
a clear space, an 'owl's eye' appearance. Inflammatory
changes are associated, and there may be vasculitis.
Polymerase chain reaction provides a highly sensitive diagnostic test.
Radiology. Barium studies of the small bowel may

demonstrate segmental changes with erosions or
extensive, penetrating, even giant ulcers. The ulcers,
the typical finding of CMV enterocolitis, are likely to
result from a combination of epithelial and vascular
endothelial involvement by CMV causing focal ischemia and possible necrosis (Fig. 7.5.12a). CMV ulcers
tend to be most pronounced in the ileocecal region
(Fig. 7.5.12b). CT has demonstrated wall thickening
and ulcerations (ALTHAZAR and MARTINO 1996)
(Fig. 7.5.12c,d).
7.5.6.5
Mycobacterium avium-intracellulare Complex

Mycobacterium avium-intracellulare complex (MAI),
which includes the two closely related organisms M.
avium and M. intracellulare, has been isolated throughout the world from soil, house dust, animal feed, and
other materials. MAI disease presents with fever, weight
loss, and, less often, diarrhea. The liver, spieen, and
lymph nodes tend to be involved. Bulky abdominal
lymph nodes are seen at a later stage of the infection
(ARELLANO and SADEGHI 2000). Hepatomegaly, splenomegaly, and enlargement of mesenteric and retroperitoneallymph nodes are usual findings on CT. By the
time MAI complicates AIDS, CD4+ T-cell counts have
fallen to the 50 per mm3 range, and other AIDS-defining
infections either have preceded or accompany the disease. Infection of humans occurs mostly by ingestion
of contarninated food or water and only exceptionally
by human to human transmission. After ingestion, bacteria enter into the intestinal mucosa and are phagocytosed by growing numbers of macrophages that are
372
H. Herlinger
c
Fig. 7.5.12a-d. Cytomegalovirus (CMV) infection. a CMV enteritis. Numerous ulcers (arrows) are seen in the distal ileum. b
In a patient with ileocecal CMV infection, a barium follow-through study demonstrates penetrating ulcers (arrows) and an
increased thickness of the wall of the terminal ileum. c In the same patient, CT with intravenous contrast reveals enhancement of the thickened wall of the terminal ileum and demonstrates penetrating ulcers (arrows); d a further CT study with
peroral contrast reveals wall thickening in both the terminal ileum and cecum (arrows). a-d Reproduced with permission
from HERLINGER et aJ. (1999)
incapable of digesting them. Multiplying bacteria distend the macrophages to cause a widening of the
Iamina propria and enlargement of the villi. Chylous
ascites isarare complication (KEAVENY et al. 1999).
The presence of acid-fast organisms can be determined in stool or endoscopic biopsy specimens. A full
diagnosis can be made by culture, but this implies a
2-week delay. A rapid identification of the organisms
by the polymerase chain reaction makes possible an

early start with anti-mycobacterial drug combinations
(DE FRANCESCO et al. 1996).
Radiology. Radiology can significantly contribute to

the diagnosis of MAC. Barium studies, preferably
enteroclysis, can demoostrate a fine nodular mucosal surface pattern (Fig. 7.5.13) representing villi
373
Fig. 7.5.13a-c. Infection with Mycobacterium aviumintra-ce/lulare complex (MAI). a Enteroclysis demonstrates groups
of micronodules (1-2 mm in diameter) within an oval space
(open arrows). bIn a further patient with MAI, enteroclysis
outlines extensive micronodularity, mostly in the jejunum
(arrows); c follow-through examination shows numerous
micronodules in the non-distended jejunum (arrows) and
fold thickening in the distal bowel, likely due to hypoalbuminemia. a, b Reproduced with permission from HERLING ER
et al. (1999)
dilated by their thickened core of lamina propria

(HERLINGER 1999). CT can outline grouped or fused
enlarged mesenteric and/or retroperitoneal lymph
nodes typically with low density centers (PANTONGRAG-BROWN et al. 1998)(Fig. 7.5.14). A similar
appearance of micronodularity and low attenuation
nodal masses is found in Whipple's disease; however,

the association of MAI with AIDS and its very low
T-lymphocyte count provide a clinical background
for a correct interpretation.
The small bowel can be extrinsically affected by an
MAI abscess, for examp1e in the omenturn (Fig. 7.5.15).
374
H. Herlinger
Fig. 7.5.14a-c. Value of CT in MAI infection. a CT after intravenous contrast outlines seemingly matted mesenteric and retroperitoneal nodal mass containing areas of low attenuation
(arrows); b a similar but more pronounced low attenuation
pattern is demonstrated in enlarged nodes (arrows); c in a further patient with MAI infection, CT presents fused para-aortic
and para-SMA nodal masses with low attenuation centers and
mild peripheral enhancement (arrows). a, b Reproduced with
permission from HERLINGER et al. (1999)
Fig. 7.5.15a,b. MAI abscess deforming the jejunum. a Extrinsic

type deformity of two loops of jejunum (open arrows). b MAI
abscess in the omenturn (arrow) was the cause. In this case, the
small bowel was not infected by MAI. a, b Reproduced with
permission from HERLINGER et al. (1999)
375
7.5.6.6
Mycobacterium Tuberculosis
Mycobacterium tuberculosis (MTb) unrelated to HIV

disease can present with lymphopenia below 1000
per mm3, usually with equal reduction of CD4+
and CD8+ T cells (CURRAN et al.1985).AIDS-associated tuberculosis occurs with greater frequency than
in the immunocompetent population; in one series
more than 40% of AIDS patients had gastrointestinal
MTb (SHAFER et al.1991). AIDS-related MTb is more
likely to present with mesenteric nodal involvement
and may have miliary or meningitic spread (SHAFER
et al.199l). Tuberculous enteritis can resemble infection by MAI but usually occurs at lymphocyte counts
above 200 per mm3 (ARELLANO and SADEGHI 2000).
Radiology. Radiologie diagnosis by means of a
barium series or enteroclysis may demonstrate
bowel wall thickening with multiple scattered ulcers
which may extend to become circumferential. Ulcers
may perforate and fistulae between bowelloops are
not unusual. The terminal ileum, often associated
with the cecum, is most likely tobe involved, usually with extensive ulceration and possible abscess
formation (Fig. 7.5.16). Contrast-enhanced CT may
outline multiple, enlarged, mesenteric or peripancreatic lymph nodes with peripheral density
increase and lower density centers, a result of caseation necrosis (HosSEIN et al. 1997). A periduodenal tuberculous cavity formation has been demonstrated (Fig. 7.5.17).
7.5.6.7
Bacillary Angiomatosis
Bacillary angiomatosis, almost confined to AIDS

patients, relates to infection by Bartonella henselae or
B. quintana. B. henselae infection derives from cats
or cat fleas and causes bacillary peliosis, focal vascular proliferations in the liver or spieen (KoEHLER et
al. 1997). B. quintana infection is a possible cause of
focal bacillary lesions in the skin and bowel wall that
resemble Kaposi's sarcoma but are unrelated to the
Kaposi's sarcoma-associated human herpes virus-8
(HHV-8) (RELMAN et al. l999).
Radiology. Radiology has demonstrated abdominal
adenopathy and soft-tissue masses, lesions in the
liver and spieen, all showing intense enhancement
with injections of contrast (MooRE et al. 1995).
Fig. 7.5.16a,b. Ileocecal tuberculosis in an AIDS patient. a

Barium follow-through examination indicates a mass separating the distal portion of the terminal ileum from the cecum
(open arrows). The affected terminal ileum is narrowed and
ulcerated. b CT study reveals a low attenuation mass medial to
the cecum ( arrows), likely caused by caseation necrosis. (Courtesy of E. J. BALTHAZAR, MD)
H. Hertinger
376
graft-versus-host disease, leukemias, AIDS {Josu1 et

al. 1981; DIBAISE and QuiGLEY 1997). Intestinal ulcerations can be a feature of candidiasis and be associated
with bleeding and perforation; however, biopsy evidence is required to confirm focal invasiveness of Candida as the cause (PRESCOTT et al. 1992).
7.5.6.9
Extrapulmonary Pneumocystosis
Fig. 7.5.17. Duodenum-related tuberculous cavitary extension.

Entry ofbarium into a debris-containing space (arrows) at the
medial border of the descending duodenum. (Courtesy of K.
C.CHo,MD)
Extrapulmonary pneumocystosis (EP) isarare complication of Pneumocystis carinii pneumonia (PCP).

About 90 cases of EP complicating AIDS were reported up to 1997 (NG et al. 1997). It has been suggested
that aerolyzed pentamidine used in the treatment of
PCP, though locally effective, produced insufficient
serum concentrations which aided the dissemination
Pneumocystis carinii. Viscera} calcifications (a 'starry
sky' pattern) are a feature of disseminated pneumocystosis and have been demonstrated in the liver
and spieen by uhrasound (RADIN et al. 1990) and
er (LUBAT et al. 1990) (Fig. 7.5.19). Histoplasmosis,
sickle cell disease, hemochromatosis, and previous
injections of mercury or thorotrast can produce a
similar pattern of calcifications.
7.5.6.8
lnvasive Candidiasis
Candida albicans, a yeastlike fungus, is a normal colonizer of the gastrointestinal tract. Interaction with HIV -1
has been shown to promote its virulence (GRUBER et
al. 1998). Intestinal invasive candidiasis (Fig. 7.5.18) has
occasionally been reported in patients with immune
deficiencies of various backgrounds - transplantation,
7.5.7
AIDS-Related Tumors
Kaposi's sarcoma and, to a lesser degree, non-Hodgkin's Iymphoma have been found to occur with
increased frequency in patients with AIDS.
a
Fig. 7.5.18a,b. Invasive candidiasis in AIDS. a Gas-rimmed, fluid-containing bowelloop (open arrows) and pneumoperitoneum
(arrows) . b Gas-fittedportal venous channels. lnvasive candidiasis-related perforation is likely tobe due to associated ischemia.
(Courtesy of E. J. BALTHAZAR, MD)
377
Fig. 7.5.19. Extrapulmonary disseminated pneumocystosis in

AIDS. 'Starry sky' pattern of calcifications throughout liver
and spieen shown by CT. (Courtesy of E. J. BALTHAZAR, MD)
7.5.7.1
Kaposi's Sarcoma
In 1882 Moritz Kaposi, a noted Viennese dermatologist, described an incurable and lethal disease with
multiple, pigmented, sarcomatous skin lesions and
tumors in the gastrointestinal tract and the liver
(BREIMER 1994). The disease, named after him, now
occurs in four subgroups, the classic, endemic, epidemic, and iatrogenic forms. Classie Kaposi's sareoma (KS) initially affected mostly elderly European men, many of them Jews from Eastern Europe.
Although patterned on Kaposi's description of the
disease, it now runs a mostly indolent course
(STRATIGOS et al. 1999) with some 5000 cases from
Europe, the Mediterranean countries, and the Americas reported up to 1998 (IsovicH et al. 2000). Endemie KS has its maximal incidence in equatorial Africa,
with a decrease towards the north and south. Males
of an average age of 32 years are predominantly
affected. The disease comprises cutaneous, osseous, lymphatic, and gastrointestinal involvement
(GIGASE 1984). Epidemie KS refers to the now
predominant facet of the disease, its association
with AIDS. The term iatrogenie KS mostly refers to
transplantation-associatedimmunosuppression. Solid
organ transplantation-related KS follows either
reactivation of human herpes virus-8 within the
recipient or results from the presence of the virus in
the transplanted tissue. This type of KS is likely to
be highly aggressive (ANTMAN and eHANG 2000).
In terms of etiology, all four subtypes have shown
a relationship to the HHV -8. Monocytes and B
lymphocytes have been found to be reservoirs for
HHV -8 in asymptomatic persons, but HHV -8 is

found in the spindie cells and the microvascular
endothelium of KS tumors. The presence of HHV -8
antiborlies at the time of HIV seroconversion carries an increased risk of KS development. These
observations strongly support the causal relationship of HHV -8 to the development of KS (ANTMAN
and eHANG 2000; ANGELONI et al. 1998; FFERMAN 1999; RENWieK et al. 1998). The homosexual
transmission of HHV -8 increases with the nurober
ofmale sexual partners (NGENDAHAYO et al. 1989).
Although its AIDS-related incidence has decreased
in recent years, KS remains the mostfrequent AIDSdefining neoplasm, especially in homosexual men.
KS lesions are formed by neovascular structures
with endothelium-derived spindie cells and infiltrating leukocytes.
Improvement of the immune status with highly
active antiretroviral drug therapy (HAART) usually
suffices to reduce the presence of KS lesions and of
the HHV-8load (SATAMBROGIO et al. 1998). Patients
with widespread visceraland mucocutaneous KS may
benefit from Paclitaxel, as a well-tolerated secondline therapy (GILL et al. 1999).
Radiology. Radiology can demonstrate KS involvement

of the gastrointestinal tract with the aid of ingested or
infused barium Suspensions. Multicentric KS lesions,
found more often in the stomach, duodenum, and
colon, are shown as centrally umbilicated, submucosal
polypoid elevations (HERLINGER 1999) (Fig. 7.5.20a).
When the mesenteric small bowel is involved, barium
studies are most likely to demonstrate the multiple polypoid lesions (Fig. 7.5.20b,c). At times er may be able
to demonstrate some of the scattered KS lesions of the
small bowel (Fig. 7.5.20d). The usually associated presence of violaceous papular skin lesions aids the interpretation of the abdominallesions as KS. er may outline clusters ofbarely enlarged mesenteric and retroperitoneallymph nodes (Fig. 7.5.21a). Only infrequently
are individual nodes found to be as large as 1.5 cm in
diameter. The liver and spieen are often found tobe
enlarged, but individual KS infiltrates are only rarely
shown by er (Fig. 7.5.21b), MRI or ultrasound.
7.5.7.2
Non-Hodgkin's Lymphoma
AIDS patients are at increased risk for developing nonHodgkin's Iymphoma (NHL) of B-cell origin. Small,
non-cleaved, Burkitt-like and diffuse, large-celllymphomas predominate (PENKOWA and HANSEN 1998)
378
H. Herlinger
a
b
Fig. 7.5.20a-d. Small-bowel lesions in AIDS-related Kaposi's sarcoma (KS). a Two centrally ulcerated, round, and elevated,
submucosal-type KS lesions are seen in the duodenum (arrows). b Multiple 'target' KS lesions are demonstrated (arrows) against
a barium-revealed background of thick folds and, more distally, of segmental clumping of barium, a result of an association
with cryptosporidiosis. c A few typical KS lesions (arrows) in the jejunum; additionallesions were present in the duodenum, a
morefrequent location. d Courtesy of E. J. BALTHAZAR, MD, an infrequent example of multiple small-bowel KS tumor nodules
demonstrated by CT (open arrows)
and occur with about 60 times greater incidence than

in the non-AIDS population (TULPULE and LEVINE
1999).
There is a preponderance for extranodal involvement, with the central nervous system being the most
typical site, with an up to So/o occurrence (ScHABET
1999). The Epstein-Barr virus (EBV), a B-lymphotropic
herpesvirus that is widespread in human populations
is strongly related to the increase of lymphoproliferative diseases. NHL and also Hodgkin's disease can
occur after years of EBV dormancy, triggered or supported by viral reactivation (PAGANO 1999). The more
common sites of non-Hodgkin's involvement of the

digestive tract have been the colon (46%}, ileum (39% ),
and stomach (23%} (BECK et al. 1996).
Radiology. Radiology has demonstrated solid organ

involvement (liver, spieen, kidneys, adrenals) in 22%
of AIDS and 10% of immunocompetent NHL patients.
Barium studies have demonstrated widespread smallbowel involvement with CT outlining multiple segments of circumferential or more focal wall thickening
with mesenteric and retroperitoneal lymphadenopathies (Fig. 7.5.22), all this without a significant differ-
379
b
Fig. 7.5.2la,b. Two examples of KS extension from the GI tract. a Involvement of mesenteric and retroperitoneallymph nodes
causes only a slight increase in their size (arrows). Reproduced with permission from HERLINGER et al. (1999). b Courtesy of
E. J. BALTHAZAR, MD, a case of KS metastasizing to the liver
c
Fig. 7.5.22a-c. Non-Hodgkin's Iymphoma (NHL). Widespread involvement ofthe small bowel byNHL isamorefrequent finding
when related to AIDS. a Barium follow-through examination demonstrates numerous segments with Iumen reduction, ulceration,
and destruction of fold patterns. b, c CT demonstrates extensive and focally massive wall thickening (open arrows) involving many
bowelloops. Mesenteric nodal enlargement is demonstrated. (Courtesy ofE. J. BALTHAZAR, MD)
380
ence between AIDS and non-AIDS patients (BALTHAZAR et al. 1997). Cavitary NHL masses may occur more
frequently in AIDS patients and are readily depicted by
barium and imaging techniques (Fig. 7.5.23).
7.5.7.3
Primary Effusion Lymphoma
Primary effusion lymphoma (PEL) isarare and distinctive form of AIDS-related B-celllymphoma and is associated with both HHV-8 and EBV (IBRAHIMBACHA et
al. 1999). lt usually evolves in the pleural space but may
also occur in the pericardiac or peritoneal spaces. There
is no associated tumor mass, but the cytology confirms
its B-celllymphoma origin. CT scans demonstrate the
presence of effusions, confirm the absence of a mass,
and may show slight thickening of the serosal lining
(MoRASSUT et al. 1997). A unique case of PEL in a
homosexual AIDS patient was located in the subarachnoid space with otherwise typical cytomorphology plus
HHV-8 and EBV association (ELY et al. 1999).
H. Herlinger
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7.6 Benign Small-lntestinal Neoplasms

N. C. GouRTSOYIANNIS, H. JI, R.D.
DZE,
P.R. Ras
CONTENTS
7.6.1
7.6.2
7.6.3
7.6.4
7.6.5
7.6.6
7.6.7
7.6.8
7.6.9
7.6.10
7.6.11
Incidence and Clinical Presentation

Adenoma 386
Leiomyoma 387
Neurogenie Tumors 388
Lipoma 390
Peutz-Jeghers Harnartoma 392
Pancreatic Heterotopia 393
Brunner's Gland Lesions 393
Inflammatory Fibroid Polyp 395
Differential Diagnosis of Benign
Small-Intestinal Neoplasms 396
Conclusion 397
References 398
385
7.6.1
lncidence and Clinical Presentation
Benign small-bowel tumors account for approximately 0.5o/o-2o/o of all gastrointestinal tract tumors
( Gooo 1963 ). Histologically, neoplastic tumors of the
small bowel are classified as epithelial, lymphoid,
or mesenchymal depending on the predominant
cell type, as indicated in Table 7.6.1. Among all
N.C. GOURTSOYIANNIS, MD
Professor & Chairman, Department of Radiology, University
Hospital of Iraklion, P.O. Box 1352, 711 10 Iraklion, Crete,
Greece
H. JI, MD, PhD
Research Fellow, Department of Radiology, Brigham and
Women's Hospital, Harvard Medical School, Boston, Massachusetts
R.D. DZE, MD, FRCP
Director, Gastrointestinal Pathology Service, Department of
Pathology, Brigham and Women's Hospital, Boston, Massachusetts, USA and Associate Professor of Pathology, Harvard
Medical School, Boston, Massachusetts, USA
P.R. Ros, MD, MPH
Executive Vice Chairman, Department of Radiology, Brigham
and Women's Hospital, Boston, Massachusetts, USA and
Professor of Radiology, Harvard Medical School, Boston,
Massachusetts, USA
types, adenomas and carcinoid tumors are the most

common, while mesenchymal tumors are less frequently encountered (GARVIN et al. 1979; OLMSTED
et al. 1987).
However, it is of importance to note that nonneoplasticsmall-intestinal tumors, such as congenital rests, heterotopic lesions, and hamartomas, may
Table 7.6.1. Types of small-bowel tumors

Tissue of origin
Benign
Malignant
1. Neoplastic
Epithelium
Adenoma
Adenocarcinoma
metastasis
Carcinoid
Lymphoma
Lymphoid tissue
Smooth muscle
tissue
Vascular tissue
Lymphoid
hyperplasia
Leiomyoma
Hemangioma
Lymphangioma
Connective tissue Fibroma
Leiomyosarcoma
Angiosarcoma
Kaposi sarcoma
Fibrosarcoma
Gastrointestinal
stromal tumor (GIST)
Malignant peripheral
nerve sheath tumor
(MPNST)
Neural tissue
Neurofibroma
Adipose tissue
Schwannoma
(neurilemmoma)
GangHoneuroma
Paraganglioma
Gangliocytic
paraganglioma
Lipoma
Liposarcoma
2. Non-neoplastic
Peutz-Jeghers
hamartoma
Pancreatic
heterotopia
Brunner's gland
lesions
- hyperplasia
- hamartoma
- adenoma
Inflammatory
fibroid polyp
386
demonstrate similar radiologic findings to benign

small-intestinal neoplasms and are, in fact, more
common.
Clinically, benign neoplasms may be asymptomatic or symptomatic, which depends more on the size
and location of the tumor rather than on the specific
histologic type. Occult GI bleeding, anemia, and/or
abdominal pain are the most common presenting
symptoms, whereas intestinal obstruction, intussusception, and/or weight loss are less common. Approximately 50% of patients are asymptomatic (ASLEY
and WELLS 1988). Thus, a higher than usual index
of clinical suspicion is needed in order to diagnose
these lesions successfully (GouRTSOYIANNIS et al.
1993).
The radiologic appearance of benign neoplasms
often mirrors the gross pattern of growth, which may be
endoluminal, intramural, or both. As noted below, filling
defects are the most common radiographic feature.
N. C. Gourtsoyiannis
culated, that produce a lobulated, cauliflower-like filling defect, with multiple radiolucent striations interspersed with frond-like projections (CHo 1997}. On
er scan adenomas appear as a sharply demarcated
soft-tissue mass confined within the boundaries of
the intestinallumen and with homogenous, moderate contrast enhancement.
The differential diagnosis of adenomas includes
adenocarcinoma, Brunner's gland lesions (hyperplasia, adenoma), hamartomatous polyps (Peutz-Jeghers
7.6.2
Adenoma
Adenomas account for up to 20% of benign smallbowel neoplasms. Approximately two-thirds of adenomas are found at autopsy, while only one-quarter
of them cause clinical symptoms. Presenting symptoms depend primarily on their location, size, and
the presence or absence of a pedicle. Typical symptoms include mild, crampy abdominal pain, intestinal
obstruction, or intermittent, often obscure GI hemorrhage (PERZIN and BRIDGE 1981}.
Pedunculated or large adenomas may lead to intussusception. However, it is their propensity to bleed
that often brings patients to clinical attention. Pathologically, adenomas may be single or multiple, occur
most often in the duodenum, and consist of dysplastic columnar epithelium arranged either in a tubular,
tubulovillous, or villous growth pattern (Fig. 7.6.1}.
On enteroclysis, adenomatous polyps usually
appear as intraluminal filling defects of small size,
averaging less than 2 cm. The filling defects have a
smooth outline and are typically round, sessile, oval,
or slightly lobulated in shape (GOURTSOYIANNIS and
MAKO 1997}. They may be solitary or multiple. When
multiple, adenomas usually affect a single bowel segment (Fig. 7.6.2). This is in contrast to patients with
familial polyposis, where filling defects are usually
distributed throughout the entire small bowel and
colon. Villous adenomas are often large in size, possibly greater than 2 cm in size, broad-based, or pedun-
Fig. 7.6.1A,B. Adenomatous polyp. A Enteroclysis shows a

large, solitary, oval-shaped, sharply demarcated, intraluminal
filling defect in the duodenum. B CT scan demonstrates a
homogeneous, intraluminal, weil marginated mass in the same
patient. (With permission from GOURTSOYIANNIS and MAKO
1997)
387
Benign Small-Intestinal Neoplasms
Fig. 7.6.2. Multiple adenomatous polyps. Two

oval-shaped, smoothly outlined filling defects,
size over 1 cm, with short pedicles (arrow).
(With permission from GOURTSOYIANNIS and
MAKO
syndrome), inammatory fibroid polyps, and, rarely,

pancreatic heterotopia and hemangiomas (GouRTSOYIANNIS et al. 1993). Radiologically, it is not possible to differentiate an adenoma from one that contains adenocarcinoma.
7.6.3
Leiomyoma
Leiomyoma is defined as a benign mesenchymal

tumor of smooth muscle origin. Leiomyoma is the
most frequently encountered benign mesenchymal
neoplasm, with a reported incidence that ranges from
20% to 40%, and occurs in all age groups ( Garvin et
al.1979; Good 1963; Gourtsoyiannis et al.1993). Leiomyomas also represent the most common symptomatic, benign small-bowel neoplasm. Patients typically
present with hemorrhage, anemia, and/or abdominal
pain/discomfort as the main clinical manifestations.
Leiomyomas may develop from the muscularis
mucosa or muscularis propria. They may be single or
multiple and occur in the jejunum or ileum in over 80%
of cases. Pathologically, these tumors typically show
a bland, relatively hypercellular parenchyma of elongated smooth muscle cells without significant atypia,
mitoses, or necrosis. Four radiologic growth patterns
have been identified: (1) intramural, (2) intraluminal
(most common), (3) extraluminal (subserosal), and (4)
bidirectional (dumbbell-shaped). Intramuralleiomyomas are usually very small in size and, thus rarely, if
ever, produce clinical symptoms. Therefore, the intrarnmal type has not been described radiologically.
On barium studies, intraluminalleiomyomas often
appear as a smooth, round, or semilunar filling defect,
1997)
demarcated by a sharp angle to the intestinal wall (Fig.

7.6.3). Hypervascular intraluminalleiomyomas may be
associated with hemorrhage and ulceration, which can
be demonstrated radiologically in almost one-third of
cases. They usually present as a single, well-defined,
round or linear lesion, often associated with a shallow
ulcer. However, ulceration is more often associated with
leiomyosarcomas, the malignant counterpart of leiomyomas, and largely in the form of cavitation.
Extraluminal (subserosal) leiomyomas are usual~
ly larger in size and typically produce a mass effect
or a 'blank' space between neighboring bowelloops
(Fig. 7.6.4). Displacement of the intestinal wall with
stretching and attening of the overlying mucosa, or
a tenting deformity, indicative of the site of attachment of the tumors,may also be present (GouRTSOYIANNIS et al. 1992).
Leiomyomas with a bidirectional growth pattern
may appear dumbbell shaped with combined features
of both an intraluminal and an extraintestinal mass.
Typical CT findings of leiomyomas include a round
or semilunar, smoothly outlined, homogeneous soft-tissue mass. The tumors appear associated with the intestinal wall, showing marked homogeneous or rim contrast
enhancement and an absence of mesenteric changes
or metastases (MEGIBOW 1997). A peripheral crescentshaped type of necrosis of the tumor mass, shown on
contrast enhanced CT as well as on US and MRI, has
found to be additionally suggestive of a leiomyomatous
(stromal) tumor (RIOUX and MAILLOUX 1997).
The radiologic differential diagnosis of leiomyoma includes leiomyosarcoma as well as other tumors
such as neurogenic tumors and carcinoid tumors.
Unfortunately, there are no characteristic radiological differences between benign (leiomyomas) and
malignant (leiomyosarcomas) lesions.
388
Fig. 7.6.3A-C. Leiomyoma of the small bowel in a patient with

occult GI bleeding. A Small-bowel follow-through (SBFf) demonstrates a smooth, oval mass in the jejunum. B Superior mesenteric arteriogram shows a hypervasewar small-bowel tumor
(arrow). C Gross specimen demonstrates submucosal mass with
hemorrhagic necrosis on the peripheral portion of the tumor
Although quite rare, intestinal neurogenic tumors

should be included in the differential diagnosis, since
their presenting symptoms, pattern of growth, and
radiologic features are similar to benign leiomyomas.
In contrast, a rather broad spectrum of radiological signs have been described in patients with primary
ileal carcinoid tumors. These include solitary or multiple filling defects, annular constriction or the appearance of kinking of the bowellumen, as weil as extraluminal extension that causes separation of adjacent
bowelloops (JEFFREE et al. 1984). When small, carcinoids may appear as round, smooth, solitary, intraluminal filling defects (GOURTSOYIANNIS 1997a).
In patients with acquired immunodeficiency syndrome (AIDS), multiple leiomyomas should be differentiated from Kaposi's sarcoma. The radiologic
appearance of Kaposi's sarcoma includes thickening
of the valvulae conniventes, mural thickening, submucosal nodularity, coalescent plaque-like lesions,
and large polypoid filling defects (WALLet al. 1986).
c
7.6.4
Neurogenie Tumors
Neurogenie tumors develop from subserosal nerve
sheaths or the Auerbach or Meissner plexus. They
are usually polypoid masses, mostly located on the
antimesenteric serosal border, and rarely exhibit malignant potential. They account for 2%-6% of all benign
small-bowel neoplasms (GARVIN et al. 1979). Five different types have been described (GouRTSOYIANNIS
1997b). The two mostfrequent are schwannoma (neurilemmoma), a mostly solitary and encapsulated neoplasm, and neurofibroma, which is the hallmark lesion
in neurofibromatosis (von Recklinghausen disease).
The other three forms, ganglioneuroma, paraganglioma, and gangliocytic paraganglioma (GP), are rare
tumors (SIVAK et al. 1975) (Fig. 7.6.5). Most of these
lesions, except for GP, may be multiple.
The principal clinical manifestation of neuragenie tumors is hemorrhage. Hernarrhage may be acute
389
Fig. 7.6.4A.B. Leiomyoma. A Enteroclysis demonstrates a !arge

subserosalleiomyoma extending outside the intestinal wall of
the jejunum. B Corresponding pathological specimen. (With
permission from GOURTSOYIANNIS and MAKO 1997)
Fig. 7.6.5A,B. Gangliocytic paraganglioma in a patient with

upper GI bleeding. A Small-bowel examination demonstrates
a smooth, 3 cm mass and thickening of the second and third
portions of the duodenum. B Pathologie examination showed
the mass to contain ganglion cells, Schwann cells, and neuroendocrine cells (H&E stain)
390
or ehronic or reeurrent. Patients may present with

melena, hematemesis, or hematoehezia (SIVAK et al.
1975).Abdominal pain may also be present.
Radiologieally, neuragenie tumors typieally appear
as smooth-surfaeed, well-defined, oeeasionally ulcerated, polypoid masses (Fig. 7.6.6). Lesions that protrude into the Iumen are easily deteeted, while subserosal or smalllesions may be diffieult to reeognize.
Dumbbell-shaped tumors may also oeeur (GouRTsoYIANNIS et al. 1993). The preoperative distinetion
of solitary neuragenie tumors from intestinal leiomyomas is extremely diffieult, sinee their presenting
symptoms, pattern of growth, and radiologieal
appearanees may be quite similar. Moreover, the
intramuralloeation and small size of the lesions often
seen in intestinal neurofibromatosis may result in a
failure to identify the lesion in up to one-third of
eases (RUNETON et al. 1984).
7.6.5
Lipoma
Lipomas arewell-cireumseribed proliferations of adipoeytes that usually grow intraluminally but may, on
oeeasion, extend outwards onto the serosal surfaee.
In some series, it forms the seeond most eommon,
benign small-bowel neoplasm (GARVIN et al. 1979).
Affected patients are usually in their 6th or 7th
deeade of life. Lipomas may be solitary or, less frequently, multiple and usually measure 1-6 em in size.
The ileum is the mostfrequent site (50%) of involvement, followed by the duodenum. Symptoms oeeur
in up to one-third of eases. Larger lesions may eause
obstruction, intussuseeption, or bleeding.
Radiologically, Iipomas appear as a solitary, sharply demareated, sessile lesions that may produee 3-4
em, intraluminal filling defeets (TAYLOR et al. 1990)
(Fig. 7.6.7). Interestingly, their shape often eonforms
to that of the small-bowel Iumen, and it is easily
deformed by eompression or peristalsis. A "pseudopedicle" eonfiguration at its distal end isarather eonstant feature (HADJIDAKIS et al. 1995).
Radiologie signs of intussuseeption may be present as well. Ulceration is less eommon (Fig. 7.6.8).
Lipomas are relatively easy to diagnose with the
use of CT. In this setting, they appear as well-cireumseribed, intraluminal, homogeneaus masses with
attenuation values between -80 and -120 HU (MEGIBOW et al. 1979; HEIKEN et al.1982).
Fig. 7.6.6A,B. Neurofibroma. A Enteroclysis shows a small, well-demarcated

mass encroaching on the intestinal
Iumen (arrow). B Corresponding pathology specimen demonstrates a small,
intraluminally protruding mass with
ulceration
391
Fig. 7.6.7A-D. Lipoma of the duodenal bulb. A Upper GI series demonstrates a smooth, well-demarcated mass in the duodenum.
B Histologie section shows focal submucosal fatty accumulation producing polyp (H&E stain, _40). C Axial CT scan shows low
attenuation mass in the duodenum. The attenuation of this mass does not correspond with typical fat because the tumor is not
of sufficient size. D Tl-weighted MR image demonstrates high signal intensity tumor consistent with fat (arrow)
B
Fig. 7.6.8A,B. Lipoma that was the lead point of an intussusception. A Axial CT image shows a fat density mass in the lead point
of an intussusception (arrow). Note the eccentric location of mesenteric fat in the intussusceptum (arrowhead). B Axial CT of
the more caudal portion of the intussusceptum clearly shows the fat attenuation value of this mass, suggesting lipoma
392
7.6.6
Peutz-Jeghers Harnartoma
Harnartomas are non-neoplastic tumors that consist
of a mixture of cell types that are normally present
for the anatomic site of growth, but are arranged
in an unusual pattern. Harnartomas may occur sporadically or associated with a familial syndrome.
For instance, Peutz-Jeghers hamartomas are the hallmark of Peutz-Jeghers syndrome {PJS) (PERZIN and
BRIDGE 1982). PJS is a hereditary GI syndrome characterized by the presence of multiple intestinal hamartomas in conjunction with mucocutaneous melanin pigmentation. Hamartomatous polyps in this
syndrome typically develop during early childhood
or adolescence and occur predominantly in the jejunum. Approximately 25o/o-30o/o of patients with PJS
have synchronaus gastric or colorectal polyps. The
natural history of PJS is marked by multiple episodes
of obstruction and/or GI bleeding. Recurrent episodes of colicky abdominal pain, due to intermittent
intussusception, are the most frequent clinical signs.
Melena or rectal bleeding may develop, although most

patients eventually develop anemia due to chronic
blood loss (GOURTSOYIANNIS and NOLAN 1997a).
Pathologically, Peutz-Jeghers hamartomas are
composed of a branched smooth muscle core tissue,
lined by normal-appearing epithelial cells (ELSAYED
and SoBIN 1997) (Fig. 7.6.9). They may be small, sessile or large, pedunculated polyps. Malignant transformation of a Peutz-Jeghers polyp is rare (PERZIN
and BRIDGE 1982; ELSAYED and SOBIN 1997).
Radiologically, Peutz-Jeghers hamartomas appear
as multiple, discrete, sessile or pedunculated, intraluminal filling defects, round or oval in shape when
small and coarsely lobulated when larger than 1.5 cm
in size (GOURTSOYIANNIS et al. 1993) (Fig. 7.6.10).
Larger lesions or those that grow in a conftuent mass
may cause intussusception. Smaller lesions may be
difficult to recognize. Solitary lesions are difficult to
diagnose (GouRTSOYIANNIS and NoLAN 1997a). In
this setting, the differential diagnosis includes adenomatous polyps, other intraluminal benign neoplasms, or even malignancy (BucK et al. 1992).
Fig. 7.6.9A-C. Peutz-Jeghers hamartoma. A Enteroclysis demonstrates a discrete, lobulated, intraluminal filling defect. B, C
Gross and low power microscopic pictures show the lobulated polypoid mass with smooth muscle core with branching radial
extensions, lined by normal epithelium
393
Fig. 7.6.IOA,8. Peutz-Jeghers hamartoma. A Enteroclysis shows

a large, typically lobular, intraluminal filling defect in a proximal ileal loop. 8 Corresponding appearance of the resected
lesion, exhibiting coarse lobulation. (With permission from
GOURTSOYIANNIS et al. 1993)
7.6.7
7.6.8
Also referred to as "ectopic pancreas" or "myoepithelial hamartoma", this is a congenital abnormality that
is characterized by the presence of pancreatic ductal,
acinar, and /or islet cell tissue in the small intestine
(LMSTED et al. 1987). Male and female patients
are equally affected. Pancreatic heterotopia is always
solitary and usually less than 3 cm in size. The majority of pancreatic heterotopias occur in the gastric
antrum, within 5- 6 cm from the pylorus, although
a few have been reported in the more distal small
bowel as well (GOURTSOYIANNIS et al. 1993; BRACKE
et al. 1991). They are usually asymptomatic except
when large in size, in which case they may cause discomfort (BRUNETON et al. 1990).
Radiologically, pancreatic heterotopia appear as
a smooth, solitary, nonpedunculated, intraluminal
filling defect that closely resembles an adenoma
(GOURTSOYIANNIS and NOLAN 1997b) (Fig. 7.6.11).
Occasionally, these lesions may show central umbilication (RUNETON et al. 1990).
Brunner's gland lesions represent an abnormal

growth ofbranched acinotubular submucosal glands,
which are normally most prominent in the fi.rst portion of the duodenum (OLMSTED et al. 1987). Their
etiology remains obscure; they are classified either
as hyperplastic lesions or as hamartomatous tumors,
and exhibit a benign course with no malignant predisposition (LMSTED et al. 1987; GOURTSOYIANNIS
and NOLAN 1997b).
Three different types of Brunner's gland lesions
have been recognized (FEYRTER 1934): hyperplasia,
hamartoma, and adenoma. Brunner's gland hyperplasia is the most common, occurring in up to 1o/o of
the population (FARKAS et al. 1980). Lesions are usually multiple, measuring less than 1 cm in size. Harnartomas and adenomas are exclusively rare. Most are
asymptomatic but may cause bleeding or obstruction.
The radiologic appearance of Brunner's gland
lesions is nonspecific. Large, solitary lesions may
Pancreatic Heterotopia
Brunner's Gland Lesions
394
Fig. 7.6.11A,B. Pancreatic heterotopia (ectopic pancreas). A Upper GI study shows smooth-surfaced, intraluminal filling defect
in the duodenum. No umbilication is noted in this case. B Smooth muscle, ductal, and pancreatic acinar tissue (bottom) are
needed to make this diagnosis (H&E stain, _60). Note the intact mucosal epithelium
Fig. 7.6.12A,B. Brunner's gland adenoma. A Upper GI series shows a sharply demarcated mass in the duodenum. This lesion is
somewhat atypical, being located in the third portion of the duodenum. Brunner's gland adenoma is usually found in the first
or second portion of the duodenum. B CT scan accompanying barium study demonstrates the submucosal tumor encroaching
on the duodenal Iumen (arrow)
395
appear as a smooth, mostly sessile, sharply marginated, intraluminal filling defects (OLMSTED et al. 1987;
GOURTSOYIANNIS et al. 1990) (Fig. 7.6.12A). Large
Brunner's gland lesions may be associated with surface erosions or superficial shallow ulcerations that
are difficult to recognize on barium studies or endoscopy (GOURTSOYIANNIS et al. 1990; SBORNE et al.
1973), whereas deep ulcers often seen with nodular
hyperplasia are easily demonstrated (PONTORIERO et
al.l988). Pliability of the duodenal wall, hypermotility of the proximal segment of the GI tract, and
the fluoroscopic appearance of a space-occupying
lesion floating loose within the bowellumen or causing incomplete obstruction may represent additional findings (GouRTSOYIANNIS et al. 1990). The CT
appearance is also nonspecific. Findings include a
round, weil defined, sharply demarcated mass of
homogenous density that projects into the duodenum (Fig. 7.6.12B).
7.6.9
lnflammatory Fibroid Polyp

Inflammatory fibroid polyps (IFPs) are benign, reactive lesions that occur in all age groups, although with
an increased incidence in the 6th and 7th decades of
life. They are more frequently located in the stomach
(OLMSTED et al. 1987). IFPs are usually solitary and
tend to occur more often in the ileum.
IFPs are submucosal growths composed of edematous, fibroblast-rich connective tissue with scattered
eosinophils and blood vessels (ELSAYED and SoBIN
1997). Their etiology is uncertain, but most believe
that they represent reactive inflammatory lesions
(SHIMER and HELWIG 1984). Patients present mostly
with obstructive symptoms due to intussusception.
Anemia or bleeding is an uncommon mode of presentation.
Radiologically, IFPs may appear as a solitary,
round, intraluminal filling defect that may be sessile or
pedunculated (GouRTSOYIANNIS and NoLAN 1997b)
(Fig. 7.6.13). Their usual size is 2- 6 cm, although
larger or elongated lesions have been reported (LMSTED et al. 1987). Signs of intussusception are often
Fig. 7.6.13A,B. Infiammatory fibroid polyp. A Enteroclysis

demonstrates a !arge, round, sessile, intraluminal filling defect,
proximal dilatation of the Iumen, and signs of intussusception.
B Corresponding resected specimen with the fibroid polyp as
the leading cause of intussusception
396
Fig. 7.6.14A-C. Infiammatory fibroid polyp of the ileum that was the lead point of intussusception. A Ultrasonogram shows
dassie target appearance of intussusception. 8 Axial CT scan demonstrates the intraluminal tumor causing intussusception
(arrowheads). C On gross specimen, disected tumor shows whitish yellow, fibroblastic stroma. Ileum is the dassie location for
this tumor when it affects the small intestine
present, whereas ulceration is rare (Fig. 7.6.14). Helpful diagnostic hints include a predominantly ileal
location, solitary growth pattern, and occurrence in
later life.
7.6.10
Differential Diagnosis of Benign Smalllntestinal Neoplasms
The specifi.c preoperative diagnosis of benign smallbowel tumors is diffi.cult based on radiologic grounds
alone. It is often necessary to interpret the radiologic features in conjunction with clinical data, such as
patient age, anatomic site, location, size and number
of lesions, to narrow down the differential diagnosis
(LMSTED et al.1987).
With respect to patient age, hamartomas and
Brunner's gland lesions usually occur earlier in life.
Conversely, lipoma and IFPs are often discovered
later in life. In fact, almost all IFPs occur in the 6th
and 7th decade. With regard to size, although many of
the lesions previously described are usually 2-3 cm
in diameter, some may be notably larger in size. For

instance, leiomyomas, lipomas, and IFPs may grow to
larger sizes.
Anatomie location may be helpful as well. The
duodenum is the preferred location for Brunner's
gland lesions, pancreatic heterotopia, adenomatous
polyps, and gangliocytic paraganglioma. The jejunum is the preferred site of growth of Peutz-Jeghers
hamartoma, leiomyoma, and schwannoma. The ileum
is the most common location of lipomas, Peutz-Jeghers hamartomas, IFPs, and, less frequently, leiomyomas and neurogenic tumors (GouRTSOYIANNIS et al.
1993).
As to the number of lesions, leiomyoma, lipoma,
pancreatic heterotopia, Brunner's gland adenoma,
IFP, and neurogenic tumors, apart from neurofi.bromatosis, are usually solitary. Peutz-Jeghers hamartomas, adenomatous polyps, hemangiomas, and Brunner's gland lesions are typically multiple.
Good quality radiologic studies combined with a
familiarity with the gross morphology help establish
an accurate diagnosis. For instance, features such
as broad-based, round or semilunar fi.lling defects,
with a crescent-type peripheral necrosis or uker-
397
ation, encroachment of the lumen or intussusception,

displacement of neighboring loops, and/or a tenting
deformity of the intestinal wall and effacement of the
overlying mucosa are highly suggestive of a leiomyoma. In contrast, the appearance of a small, finely
demarcated, oval-shaped, solitary or multiple, sessile
or pedunculated, intraluminal filling defect is most
suggestive of an adenoma. Multiple filling defects
of different sizes, combined with coarse lobulation,
a broad distribution with or without coalescence,
and/or synchronous tumors in the stomach or colon
are findings suggestive of PJS. Solitary, large, smoothly lobulated, often pedunculated, filling defects in the
second portion of the duodenum are highly suggestive of a Brunner's gland lesion. Finally, lesions with
a solitary, sharply marginated, ovoid filling defect,
with a pseudopedicle at its tip, and easily deformed
by compression or peristalsis are highly characteristic of a lipoma (Table 7.6.2).
7.6.11
Conclusion
Preoperative radiological diagnosis of symptomatic,
benign small-bowel tumors may be rewarding, especially when the prompt application of sensitive techniques is available, and a high index of clinical suspicion is utilized. Experience has shown that enteroclysis and er can adequately depict the individual
characteristics of such tumors, so that subtle differences may lead to a correct diagnosis in the majority
of cases.
Table 7.6.2. Differential diagnosis of benign small-intestinal neoplasms

Neoplasm
Clinical data
Age
Leiomyoma
Morphology
Size
Commonsite
Number
3cm
occasionally
Jejunum, ileum
(less often)
Solitary
Adenoma
Broad-based, round or semilunar

filling defect with peripheral necrosis
or ulceration, effacement of overlying
mucosa, and/or tenting deformity
Duodenum,
Multiple
jejunum (less often)
Small, finely demarcated, oval,

sessile or pedunculated nodule( s)
Gangliocytic
paraganglioma
Duodenum, ileum
(less often)
Solitary
Same as leiomyoma
Schwannoma
Jejunum, ileum
(less often)
Ileum, duoderrum
(less often)
Solitary
Sharply marginated, usually solitary,

ovoid nodule with pseudopedicle,
easily deformed by compression or
peristalsis, fat attenuation coefficient
Peutz-Jeghers hamartoma Younger
Ileum, jejunum
Multiple
Multiple nodules of different sizes,

usually exhibiting coarse lobulation,
a broad distribution, and coalescence
with synchronous tumors in stomach
and colon
Pancreatic heterotopia
Younger
Duodenum
Brunner's gland lesion
Younger
Duodenum
(second portion)
Multiple
Small, smoothly lobulated, often

pedunculated
Infiammatory
Later
(6th-7th
decade)
Ileum
Solitary
Round or ovoid filling fibroid polyp

defect causing intussusception
Neurogenie tumor:
Lipoma
Later
(6th-7th
decades)
3cm
occasionally
3cm
occasionally
398
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Heiken JP, Forde KA, Gold RP ( 1982) Computed tomography as
a definite method for diagnosing gastrointestinallipomas.
Jeffree ~A~ Barter SJ, Heminway AP, Nolan DJ (1984) Primary
carcm01d tumors of the ileum: the radiologic appearances.
Clin Radiol35:451-454
Megibow A (1997) Computed tomography. In: Gourtsoyiannis
NC, Nolan DJ (eds) Imaging of small intestinal neoplasms.
Elsevier,Amsterdam, pp 347-371
Megibow AJ, Redmond PE, Bosniak MA, Horowitz L (1979)
Diagnosis of gastrointestinal lipomas by CT. AJR
133:743-745
Olmsted WW, Ros PR, Hjermstad BM, McCarty MJ, Dachman
AH (1987) Tumors of the small intestine with little or no
malignant predisposition: a review of the literature and
report of 56 cases. Gastroint Radiol 12:231-239
Osborne R, Toffier R,Lowman RM (1973) Brunner's gland adenoma of the duodenum. Am J Dig Dis 18:689-694
Perzin KH, Bridge MF ( 1981) Adenomas of the small intestine:
a clinicopathologic review of 51 cases and a study of their
relationship to carcinoma. Cancer 48:799-819
Perzin KR, Bridge MF ( 1982) Adenomataus and carcinomatous
changes in hamartomatous polyps of the small intestine
(Peutz-Jeghers syndrome): report of a case and review of
the literature. Cancer 49:971-983
Pontoriero MA, Khan MY, Spillert CR, Lazaro EJ (1988) Brunner's gland adenoma: case report and literature review. Dig
Surg 5:177-180
Rioux M, Mailloux C (1997) Crescent-shaped necrosis: a new
imaging sign suggestive of stromal tumour of the small
bowel. Abdom Imaging 22:376-380
Shimer GR, Helwig EB (1984) Inflammatory fibroid polyps of
the intestine.Am J Clin Pathol81:708-713
Sivak MV, Sullivan Bh, Farmer RG (1975) Neurogenietumors
of the small intestine: review of the literature and report
of a case with endoscopic removal. Gastroenterology
68:374-380
Taylor AJ, Stewart ET, Dodds WJ (1990) Gastrointestinal
lipomas: a radiologic and pathologic review. AJR
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7.7 Malignant Small-lntestinal Neoplasms

N.C. GouRTSOYIANNIS, H. JI, R.D. DZE, P.R. Ros
CONTENTS
7.7.1
7.7.2
7.7.3
7.7.4
7.7.5
7.7.5.1
7.7.5.2
7.7.6
7.7.7
7.7.8
Incidence and Clinical Presentation 399

Adenocarcinoma 400
Carcinoid Tumor 404
Lymphoma 408
Vascular Sarcomas 416
Angiosarcoma 416
Kaposi Sarcoma 416
Gastrointestinal Stromal Tumors 417
Metastasis 420
Conclusion 425
References 425
7.7.1
lncidence and Clinical Presentation
Primary malignant small-bowel neoplasms account

for less than 2% of all primary gastrointestinal
malignancies (BARCLAY and SHAPIRA 1983; GOEL
et al. 1976; GoRE 1997). Thesetumorsoften present
with nonspecific signs and symptoms, which may
result in a delay of diagnosis until the tumors
are advanced. The most common malignancies of
the small bowel include adenocarcinoma, carciN.C. GOURTSOYIANNIS, MD
Professor & Chairman, Department of Radiology,University
Hospital of Irakiion and University of Crete Medical School,
Iraklion, Crete, Greece
H. JI, MD, PhD
Research Fellow, Department of Radiology, Brigham and
Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA
R.D. DZE, MD, FRCP
Director, Gastrointestinal Pathology Service, Department of
Pathology, Brigham and Women's Hospital, Boston, Massachusetts, USA and Associate Professor of Pathology, Harvard
Medical School, Boston, Massachusetts, USA
P.R. Ros, MD, MPH
Executive Vice Chairman, Department of Radiology, Brigham
and Women's Hospital, Boston, Massachusetts, USA and
Professor of Radiology, Harvard Medical School, Boston,
Massachusetts, USA
noid tumor, and lymphoma. Gastrointestinal stromal tumors (GISTs) are increasing in incidence
(Table 7.7.1).
Table 7.7.1. Frequency and prognosis of small-bowel tumors
by histologic type (from GoRE 1997 with permission)
Tumortype
Relative
frequency
5- year survival
Adenocarcinoma
24%-50%
Resectable: 10%- 20%

Unresectable: < 1%
Carcinoid
17%-41%
50%
Primary lymphoma
12%-24%
Resectable: 40%- 50%

Unresectable: <25%
Gastrointestinal stromal 11%- 20%

tumor (leiomyosarcoma)
20%- 25%
The preferred location of small-intestinal malignancies varies according to the specific histological type. For instance, the majority of adenocarcinomas occur in the duodenum or jejunum. Carcinoid tumors and Iymphomas usually develop in
the ileum. GISTs occur with equal frequency in the
jejunum and ileum.
The clinical presentation of malignant smallintestinal neoplasms may also be nonspecific. Occult
GI bleeding, anemia, and/or abdominal pain are the
most common presenting symptoms, whereas intestinal obstruction, intussusception, and/or weight
loss are signs that occur less often.
The cornerstone of diagnosis of primary smallintestinal malignancies is contrast radiology. However, computed tomography (CT), with its high
degree of accuracy and staging capabilities, is a
popular method of evaluating primary small-bowel malignancies (FREEMAN 2001; GouRTSOYIANNIS
1988; JI and Ros 1999; LAURENT et al. 1995; MACClON! et al. 1997; MEGIBOW 1997). Other imaging
modalities, such as ultrasonography, angiography,
and magnetic resonance imaging (MRI), may also
be helpful.
400
7.7.2
N. C. Gourtsoyiannis et al.
majority metastasize early to regionallymph nodes,

liver, or the peritoneum (Ouriel and Adams 1984).
Microscopically, adenocarcinomas may be well to
Primary adenocarcinoma of the small intestine is a poorly differentiated and may be mucinous or conremarkably uncommon neoplasm with an estimated tain signet ring features.
annual incidence of 0.25- 0.4 per 100,000 (BARCLAY
Radiology remains the most effective means of
and SCHAPIRA 1983; ELSAYED and SOBIN 1997). lt preoperative assessment of small-bowel adenocarciaccounts for less than 1% of all primary gastrointes- noma, although enteroscopy can permit direct examtinal malignancies (ADLER et al. 1982; GoRE 1997).
ination and biopsy of the small bowel. Enteroclysis
Adenocarcinomas are usually located in the prox- has been shown to be a sensitive diagnostic method
imal small bowel; approximately 42% occur in the for depicting even subtle characteristics of smallduodenum, 43% in the jejunum, and 15% in the ileum bowel malignancies (BASSETTE et al.1989), and it can
(AsHLEY and WELLS 1988). However, adenocarcino- be the procedure of choice for accurately identifying
mas that develop in Crohn's disease occur in the and localizing small-bowel neoplasms (GouRTSOYileum in >70% of patients (HoFFMAN et al. 1977; IANNIS 1997b).The radiologic appearance of smallMILLER et al. 1987a).
bowel adenocarcinoma is similar to carcinomas that
In the majority of cases, no risk factor is evident involve other parts of the GI tract. It basically reflects
(ARTHAUD and GUINEE 1979), although several con- the growth pattern and characteristically demonditions are associated with a higher incidence of ade- strates annular narrowing or stricture formation, fillnocarcinoma in the small intestine. These include ing defects, the presence of an ulcerated mass, or a
adenomatous polyps and villous adenomas (PERSIN combination of these features.
and BRIDGE 1981), familial adenomatous polyposis
Infiltrating neoplasms are the most common type,
and its variant Gardner syndrome (HEFFEMON et al. which invariably appear as a short, well defined, cir1962; RoTsand MARHJE 1974), and hereditary non- cumferential narrowing of the lumen with shoulderpolyposis colorectal cancer (HNPCC) or Lynch syn- ing of the margins and evidence of mucosal destrucdrome (LYNCH et al. 1993). To a lesser extent, celiac tion (Fig. 7.7.1). The narrowing tends to be symdisease (SwiNSON et al. 1983), long-standing Crohn's metrical and may, at times, be elusive on contrast
disease (CoLLIER et al.1985; MILLER et al.1987a), and radiography or CT examination. Adenocarcinomas
neurofibromatosis (McGLINCHEY et al. 1982) have may, on occasion, induce a marked local desmoalso been associated with a higher risk for small- plastic reaction, which can lead to complete obstruction with prestenotic dilatation (GouRTSOYIANNIS
bowel adenocarcinoma.
Adenocarcinomas are almost always symptomat- 1997b ). Annular, constricting lesions in the distal
ic. However, the presenting symptoms are nonspe- ileum resembling primary adenocarcinomas need to
cific and usually related to intestinal obstruction be considered carefully, as in most of the cases they
or chronic blood loss. Abdominal pain is the most represent either Iymphomas or secondary involveconsistent clinical complaint (ADLER et al. 1982). A ment from carcinoma of the cecum through lymmobile abdominal mass may be palpated in only phatic permeation.
Polypoid-type adenocarcinomas occur primarily
about one-third of patients (ARTHAUD and GuiNEE
1979; BRIDGE and PERS IN 1975; DARLING and WELCH in the duodenum. They appear as large, irregular, pol1959), while recurrent obstruction due to intussus- ypoid filling defects associated with mucosal destrucception, jaundice in cases with duodenal periampul- tion and encroachment on the bowel lumen (Fig.
lary neoplasms, fistula formation, or perforation are 7.7.2). Small, solitary polypoid adenocarcinomas are
other rather rare forms of presentation (ADLER et al. rather rare in the mesenteric small bowel, and dif1982; SAGER 1978; WILSON et al. 1974). The OVerall ferentiation from other, mostly benign neoplasms is
prognosis for adenocarcinoma is poor. Five-year sur- difficult with either enteroclysis or CT scan. Multiple
vival rates range between 15% and 28% in large or larger polypoid masses are less frequently encounseries (ADLER et al. 1982; BRIDGE and PERSIN 1975; tered and may be grossly ulcerated (GouRTSOYIANMILES et al. 1979). Early diagnosis isthebest means NIS and MAKO 1997) (Fig. 7.7.3).
Ulceration is a common finding in adenocarcinoof improving survival in patients with these tumors
mas. Single or multiple ulcers of variable size are
(GOURTSOYIANNIS 1997a).
Grossly, primary adenocarcinomas are usually sol- often present, accompanying infiltrating or polypoiditary, infiltrative, annular, or constrictive lesions. type adenocarcinomas. Ulceration, however, seldom
Polypoid intraluminal growth is less common. The represents the only feature of adenocarcinoma, and
Adenocarcinoma
Malignant Small Intestinal Neoplasms
401
Fig. 7.7.1A,B. Adenocarcinoma of the jejunum. A Short, annular narrowing with mucosal destruction and prestenotic dilatation.
B Corresponding pathology specimen. (Reproduced from GouRTSOYIANNIS 1997b with permission)
Fig. 7.7.2A,B. Adenocarcinoma of the duodenum. A A large,

solitary filling defect with irregular margin encroaches on
the distal end of the common bile duct (BD). B CT shows a
bulky, homogeneous, intraluminal mass with irregular margins. (Reproduced from GouRTSOYIANN IS 1997b with permission)
cases with bulky, ragged, ulcerated masses are indistinguishable from cavitating small-bowel Iymphomas ( GOURTSOYIANNIS 1997b ). Fistulaformation and
intestinal perforation have been reported to complicate ileal adenocarcinomas as well.
er scan may present the best form of radiologic
study initially to detect a primary small-bowel neoplasm in patients referred for evaluation of unusual
or nonspecific abdominal complaints. eertain er
scan patterns may also enable the radiologist to characterize individual tumor types. When complemented with barium radiology, CT scan can also increase
the detection rate of these lesions (LAURENT et al.

1991).
As with other GI tract malignancies, the extent of
tumor spread at the time of diagnosis is the strongest
prognostic factor. Thus, the rNM classification is the
most useful predictor of survival in affected patients
(Table 7.7.2) (ELSAYED and SOBIN 1997; HERMANEK
and SO BIN 1992).er plays an important role in tumor
staging, based on its ability to depict mural and
extraluminal components of the tumors, including
evaluation of lymph nodes, liver, mesenteric, or peritoneal involvement (MEGIBOW 1997). CT may also
402
Fig. 7.7.3A- C. Polypoid adenocarcinoma of the jejunum. A Enteroclysis showing indentation and encroachment on the Iumen
of a jejunalloop by a bilobed mass, displacing adjacent loops. B CT demonstrates a bilobed, polypoid mass. C Corresponding
pathology specimen. (Reproduced from GouRTSOYIANNIS and MAKO 1997 with permission)
Table 7.7.2. TNM clinical classification system for staging of malignant small-bowel tumors (from HERMANEK and So BIN 1992
with perrnission)
Primary tumor (T)
TX
Primary tumor cannot be assessed
TO
No evidence of primary tumor
Tis
Carcinoma in situ
Tumor invades Iamina propria or submucosa
Tl
Tumor invades muscularis propria
T2
Tumor invades through the muscularis propria into
T3
the subserosa or into the nonperitonealized perimuscular tissue (for jejunum and ileum into mesentery) or retroperitoneum (for duodenum in areas
where serosa is lacking) with extension equal to or
less than 2 cm
T4
Tumor perforates the visceral peritoneum or directly
invades the organs or structures (includes other
loops of small intestine, mesentery or retroperitoneum >2 cm and abdominal wall by way of serosa;
for duodenum only, invasion of pancreas)
Regionallymph nodes (N)
NX
Regionallymph nodes cannot be assessed
NO
No regionallymph node metastasis
Nl
Regionallymph node metastasis
Distant metastasis (M)

MX
Presence of distant metastasis cannot be assessed
MO
No distant metastasis
Ml
Distant metastasis
The categories M1 and pM1 may be further specified according to the following notation:
PUL Pulmonary MAR Bone marrow
oss
PLE Pleura
HEP Hepatic
PER Peritoneum
BRA Brain
ADR Adrenals
LYMP Lymph nodes
SKI Skin
OTH Others
Stage grouping
Stage 0
Tis
Stage I
Tl
T2
Stage II
T3
T4
AnyT
Stage III
NO
NO
NO
NO
NO
Nl
MO
MO
MO
MO
MO
MO
Stage IV
AnyN
M1
AnyT
Osseous
demoostrate the degree of extension of the tumor

beyond the bowel wall into the mesenteric fat or the
peritoneal surface, or pick up invasion of neighboring parenchymal argans or mesenteric vessels, indicating unresectability. An accuracy in preoperative
staging of >60o/o has been reported, with er being
particularly helpful in the determination of local
invasion rather than the detection of lymph node
involvement (LAURENT et al.1991). er is additionally
indicated for the detection of disease recurrence after
surgery (rHOMPSON and HALVORSEN 1987).
Radiologically, adenocarcinomas typically appear
on er as solitary, focal, well-defined masses with
thickening of the bowel wall and narrowing of
the lumen, either concentrically or asymmetrically
(Fig. 7.7.4). Lesions are often ulcerated and not infrequently accompanied by dilatation of the proximal
Fig. 7.7.4A,B. Annular carcinoma of the jejunum. A Spot compression radiograph during enteroclysis shows annular constricting lesion (arrow). B Helical CT studywith delayed image
demonstrates focal circumferential thickening of jejunum
403
Fig. 7.7.5. Adenocarcinoma in a patient with small-bowel

obstruction. Axial CT scan shows an irregular occluding mass
involving the jejunum with mesenteric extension. Dilatation
of the proximal bowel segment is obvious
bowel segment (Fig. 7.7.5}. rhe tumor mass may be

homogeneaus or heterogeneaus and usually shows
moderate enhancement after intravenous cantrast
administration (MEGIBOW 1997}. Infiltration of the
mesenteric surfaces and/or adjacent argans is seen
with advanced disease. Associated lymph node
enlargement is encountered in <50% of patients
(MEGIBOW 1997); invaded nodes may be missed
when they are <15 mm in size (LAURENT et al.
1991), whereas bulky adenopathy is less common.
Effective use of er is essential and requires meticulous attention to technique, including completely
uniform opacification of the bowellumen and cantrast enhancement of the bowel wall.
A variety of radiological appearances may be
encountered with small-bowel adenocarcinomas, and
careful barium and/or er studies are essential to
detect and diagnose preoperatively some of the smaller or more distally located lesions. Annular constricting lesions would need to be differentiated from
secondary adenocarcinoma, carcinoid or erohn's
disease, whereas predominantly ulcerated adenocarcinomas may simulate Iymphomas, leiomyosarcomas
or metastatic melanomas. Annular lesions encountered in the small intestine have been found to
be due to metastases in 55o/o of cases (LEVINE et
al. 1987).Unlike primary adenocarcinoma, annular
metastases tend to be larger and cause a more pronounced narrowing and/or angulation, often due to a
desmoplastic reaction. Leiomyosarcoma, Iymphoma,
and metastatic melanoma usually appear as lengthier lesions with wider channels, and usually show
marked ulceration with little or no evidence of
obstruction (LEVINE et al.1987; PAPADOPOULOS and
404
NoLAN 1985). In addition, adenocarcinoma has been

reported to mirnie ileal Crohn's disease radiographieally (GALLEGO et al. 1986; MILMAN et al. 1980;
TRAUBE et al. 1980). The radiologie appearance of
adenocarcinoma complicating ileal Crohn's disease is
essentially indistinguishable from that oflong-standing Crohn's disease (MILLER et al.1987b).
7.7.3
Carcinoid Tumor
Carcinoid tumor is the second most common smallintestinal malignant neoplasm, with an estimated
incidence of 0.28 per 100,000 persons per year (MoERTEL 1987). Almost 90o/o of lesions occur in the distal
ileum; they may be multiple in approximately onethird of cases and may often coexist with other primary malignant neoplasms (KoTHARI and MANGLA
1981; MOERTEL 1987).
Primary small-intestinal carcinoid tumors rarely
produce clinieal symptoms largely due to their small
size and deep mucosal site of origin. Nevertheless,
the most common clinieal presentation is episodie
abdominal pain, often in association with intermittent intestinal obstruction. Gastrointestinal bleeding
is distinctly uncommon and usually associated with
duodenallesions or multiple ileal carcinoids (KREIT
et al. 1986). Infrequently, a palpable abdominal mass
may be the only important physieal finding at initial
examination. The carcinoid syndrome is an unusual
clinical presentation, estimated to occur in 30o/o- 35o/o
of jejunoileal carcinoids that have metastasized to the
liver (MoERTEL et al.1961). Cutaneous flushing, characteristieally triggered by alcohol and diarrhea, are
prominent symptoms. Other manifestations include
hepatomegaly, asthma, valvular heart disease, telangiectasia, or intermittent hypertension. The average
duration of symptoms attributable to small-intestinal carcinoid tumors prior to definite diagnosis is
reported to exceed 2 years (KREIT et al. 1986). The
presence of symptoms has, however, been shown to
have a definite prognostic significance, and lymph
node metastases have been found to accompany 90o/o
of symptomatic patients (MoERTEL et al.1961).
No distinctive histologieal differences are
described between benign and malignant carcinoids.
The pathologie diagnosis of malignancy is based on
the degree of local invasiveness to mesentery and
mesenteric lymph nodes or the presence of distant
metastases, mainly to the liver. Despite their variable
biologic behavior, a definite correlation has been
established between the size of the lesion at presentation, muscle invasion, and metastases, with intestinal
carcinoids smaller than 1 cm exhibiting malignant
behavior only occasionally and those 2 cm or larger
being more consistently malignant (MoERTEL 1987).
Patients with carcinoid tumor have a better overall chance of survival than those with other smallintestinal malignancies. The prognosis appears to be
directly correlated with tumor size and resectability,
and the eure rate appears to be exceedingly high for
patients from whom allvisible malignant disease has
been resected. In patients with metastatie disease,
5-year survival has been reported in 50o/o of those
with incurable abdominal disease and in about 30o/o
of those with hepatie metastases (ASHLEY and WELLS
1988; GOURTSOYIANNIS 1988; MOERTEL 1987).
Carcinoid tumors are believed to arise from endocrine cells within the basal portion of the epithelium, superficial to the muscularis mucosae. They are
composed of small cells with uniform, round nuclei
(BucK and SOBIN 1990). They have a distinctive tendency to extend into the submucosa and infiltrate the
intestinalwalland serosa. Less frequently, intraluminal growth will result in a polypoid lesion. Invasion
through the intestinal wall may give rise to smooth
muscle hypertrophy and fibrosis in the surrounding
submucosa, the mesentery, and mesenterie vessels.
The tumor mass and associated fibrosis may produce wall rigidity, fixation of intestinalloops, angula-'
tion, and kinking, sometimes leading to obstruction
and/or ischemia.
Careful barium examination is essential for providing an accurate preoperative diagnosis. The radiologie signs shown on enteroclysis reflect the stage
that the pathologie process has reached at the time
of examination. They may be those of the primary
lesion, appearing as solitary(Fig. 7.7.6) or multiple,
round, smoothly outlined, intramural or intraluminal filling defects that encroach upon the intestinal
lumen (Fig. 7.7.7); those of a secondary mesenterie
mass causing stretching, rigidity, and fixation of ileal
loops (Fig. 7.7.8); those due to interference with the
ileal blood supply, resulting in thiekening of the valvulae conniventes and chronic ischemie intestinal
changes; or to the effects of fibrosis associated with
tumor spread, presenting as sharp angulation of a
loop or a stellate, spoke-like arrangement of adjacent
intestinalloops (GouRTSOYIANNIS and MAKO 1997;
}EFFREE et al. 1984).
High resolution sonography, if meticulously performed,may be useful in the detection of small-intestinal carcinoids, especially when located in the distal
ileum. The sonographie appearances are not charac-
405
Fig. 7.7.6. Carcinoid tumor. Compression view of an enteroclysis study showing a solitary, small, semilunar, finely demarcated filling defect in the terminal ileum. (Reproduced from
GOURTSOYIANNIS and MAKO 1997 with permission)
Fig. 7.7.7A,B. Multiple ileal carcinoids. A Enteroclysis shows

three adjacent, finely demarcated filling defects in the terminal ileum. (Courtesy of Dr. E. Lambrakos; reproduced from
GOURTSOYIANNIS and MAKO 1997 with permission)
'V
406
Fig. 7.7.8A- C. Carcinoid tumor. A A semilunar intraluminal

filling defect (arrowhead) in an ilealloop, resulting in obstruction and proximal dilatation. B Narrowing, kinking of the
Iumen, and fixation of ileal loops, immediately distal to the
tumor mass are also demonstrated. C CT shows the mesenteric response to small-intestinal carcinoid with a spiculated
mass tethering adjacent intestinal loops. Dystrophie calcification within the mesenteric mass is also seen. (Reproduced
from GOURTSOYIANNIS 1988 with permission)
c
teristic and include a smooth, intraluminal, homogeneously hypoechoic, oval mass with a broad-based
wall attachment interrupting the submucosa. lt may
demoostrate more specific features, like thickening
of the muscularis propria, puckering, wall retraction,
serosal invasion, and mesenteric involvement (Rwux
et al. 1995). Sonography is additionally valuable in
detecting liver metastases, which may have a variable
but often hyperechoic echotexture (MACCIONI et al.
1997).
Carcinoid tumors are recognized best on CT on

the basis of mesenteric findings. Due to their relatively small size, primary tumors are rarely visualized
as soft-tissue nodular masses projecting into an optimally opacified intestinalturnen or as focal intestinal wall thickening (Fig. 7.7.9). Secondary mesenteric
changes include discrete, unifocal, soft-tissue masses
associated, or not, with linear soft-tissue strands radiating into the surrounding mesentery in a stellate
pattern, while displacing adjacent intestinal loops
407
Fig. 7.7.9A- D. Carcinoid tumors involving the small bowel. A

Enteroclysis shows nodular mass involving ileum. B CT demonstrates nodular mass with mural thickening of ileum. C,
D Gross and low power microscopic specimen demonstrates
nodular mass involving mucosal and serosal layer of small
bowel
c
(Fig. 7.7.10). Bulky, conglomerate calcification of the
mesenteric mass is considered a characteristic feature of the tumor (WooDARD et al. 1995). Hypervascular liver metastases (Figs. 7.7.11, 7.7.12), usually hypodense on precontrast scans, mesenteric and
retroperitoneallymph node enlargement, ascites secondary to peritoneal seeding, and occasionally dystrophic calcification in metastatic nodes or in liver
metastases (Figs. 7.7.11, 7.7.12) may be additionally
demonstrated (MEGIBOW 1997; PELAGE et al. 1999).
Despite limitations concerning the detection of
primary carcinoid tumor and metastases to normalsized lymph nodes, CT is considered a reliable means
for evaluating the full extent of disease spread before
surgical exploration. Liver metastases are demonstrated in 60o/o- 65o/o of patients, and optimum examination technique, combining precontrast scans and
intravenous cantrast enhancement, is required for
their detection (Prcus et al. 1984; WooDARD et al.
1995). Mesenteric involvement is shown in 50o/o of

cases, either in the form of nonspecific mesenteric
soft-tissue stranding or of a discrete mesenteric
mass with radiating margins (WooDARD et al.1995).
Enlarged retroperitoneal lymph nodes are reported
in 27o/o- 35o/o of patients, mesenteric lymphadenopathy in 20o/o, and carcinomatosis, manifested by peritoneal studding and/or ascites, in another 20o/o of
reported cases (Picus et al. 1984; Woodard et al.
1995).
The radiologic appearance of carcinoid tumor is
nonspecific, and in the absence of the carcinoid syndrome, none of the individual features described are
diagnostic. The differential diagnosis of primary carcinoid tumors includes any benign tumor that grows
intraluminally, such as leiomyomas. The radiographic findings of carcinoid-induced mesenteric infiltration may be mimicked by inflammatory or neoplastic disorders or chronic ischemia. Perhaps the single
408
Fig. 7.7.10A,B. Mesenteric involvement of carcinoid. A CT reveals a spiculated mesenteric mass tethering adjacent intestinal
loops. B Axial CT shows increased soft-tissue attenuation in the small-bowel mesenterywith calcification (arrow) and stranding
of the mesentery, and tethering of severalloops of small bowel, consistent with carcinoid
Fig. 7.7.11A,B. Duodenal carcinoid and hepatic metastasis in a patient with carcinoid syndrome. A Unenhanced CT demonstrates an exophytic isoattenuated mass on the medial duodenum (arrow). B CT obtained during the early phase of the bolus
shows enhancement of !arge hepatic metastasis
most important differential diagnosis of an ileal carcinoid is Crohn's disease (JEFFREE et al. 1984). Comparative characteristics that should alert the radiologist to the possibility of a carcinoid include multiple
or diverse lesions, sharp angulation, kinking or stellate arrangement of intestinalloops, predominantly
ileal involvement with absence of ulceration, and
a desmoplastic mesenteric mass (GouRTSOYIANNIS
and MAKO 1997).
7.7.4
Lymphoma
Malignant Iymphoma may involve the small intestine
primarily or as a manifestation of a widespread systemic disease process. Primary small-intestinallymphoma has an estimated annual incidence of 0.12 per
100,000 persons (WEISS and YANG 1987), and it represents approximately 20% of primary malignancies
409
Fig. 7.7.12A- D. Carcinoid tumor with carcinoid syndrome.

A Enteroclysis shows a smoothly outlined, semilunar filling
defect encroaching on the intestinallumen of an ilealloop, and

an annular-type stricture in an adjacent ileal segment (white
arrowheads). B CT reveals a spiculated mesenteric mass tethering adjacent intestinal loops. C Hepatic arteriogram demonstrates numerous hypervascular metastases throughout the
liver. D Pathology specimen showing the actual carcinoid
tumor (arrow). (Reproduced from GouRTSOYIANNIS and
MAKO 1997 with permission
of the small intestine (DRAGOSICS et al. 1985). Intestinallymphoma is considered to be primary if the predominant lesion is in the intestine, the initial presenting symptoms are related to intestinal involvement,
and there is no evidence of a generalized or intestinal
predisposing factor (GouRTSOYIANNIS and NoLAN
1988 ). Disordersthat predispose to Iymphoma include
previous extraintestinal Iymphoma, chronic lymphocytic leukemia, celiac disease (SWINSON et al. 1983),
immunoproliferative small intestinal ( a heavy chain)

disease (GouRTSOYIANNIS and NoLAN 1988; KHOJASTEH et al. 1983), and immunologic dysfunction
including acquired immunodeficiency syndrome
(AIDS) (BALTHAZAR et al. 1997). The ileum is the
most frequent location for primary intestinal Iymphomas, particularly the terminal ileum, due to the
increased amount of lymphoid tissue normally present compared with the duodenum and jejunum.
410
Intestinallymphoma has a bimodal age distribution. One peak occurs in patients < 10 years of age and
the other in patients >50 years old. Lymphoma represents the most common neoplasm of the small
intestine in children, although it is far more commonly encountered in adults .The clinical presentation is variable and includes abdominal pain, diarrhea, weight loss, intestinal bleeding and/or anemia,
and a palpable abdominal mass (GouRTSOYIANNIS
and NOLAN 1988). Major complications include massive hemorrhage, perforation complicated by peritonitis, fistula formation, and rarely intestinal obstruction. Fever is uncommon and suggests diffuse involvement. Patients with Mediterranean-type Iymphoma
usually present with diarrhea and malabsorption
(KHOJASTEH et al. 1983).
The prognosis of small-intestinal Iymphomas is
poor and correlates with the degree of tumor differentiation, but mainly with the extent of tumor spread
at presentation. Multiplicity of intestinal involvement
may additionally indicate a poor prognosis (DRAGosrcs et al. 1985). An overall 5-year survival of
approximately 36o/o has been estimated (MAKEPEACE
et al. 1987).
The vast majority of intestinallymphomas are of
the non-Hodgkin type (LEWIN et al. 1978) and arise
from mucosa-associated lymphoid tissue (MALT).
They are typically low-grade small-cell Iymphomas
(ELSAYED and SoBIN 1977). Their gross pathologic
patterns include: (1) nodular or polypoid masses, (2)
focally or diffusely infiltrative (constricting) lesions,
and (3) a combined pattern. Mucosal ulceration may
be present in any of these morphologic patterns of
growth. Multiple sites of involvement, either in the
same segment or widely separated in location, may
occur in 10%- 40o/o of patients (DRAGosrcs et al.
1985; GOURTSOYIANNIS and NOLAN 1988; LEWIN et
al. 1978 ). Spread to the adjacent mesentery and lymph
nodes is not unusual.
Small-bowel Iymphomas demonstrate a broad
spectrum of radiologic appearances that mirror their
variable pathologic patterns of growth. Enteroclysis
will usually define a multiplicity of features (Fig.
7.7.13). In the majority of cases, the lesions are large
and non-obstructing.
Nodular lesions tend to be multiple and <3 cm
in diameter. They appear as mucosal or intraluminal
filling defects of varying size and shape, involving
variable lengths of the small intestine (Figs. 7.7.14,
7.7.15).
Infiltrative forms are reported to represent >50o/o
of all cases (RUNETON and VALETTE 1990), and they
may cause thickening of the bowel wall (Fig. 7.7.16)
without eliciting a desmoplastic reaction. Constricting lesions are less common. When solitary, they may
be indistinguishable from adenocarcinoma or metastatic disease except that they are mostly located distally, and there is no history of a known primary.
Preservation of the patency of the lumen in infiltrative lesions is highly suggestive of an intestinallymphoma. The infrequently seen aneurysmal dilatation
is a characteristic feature of Iymphoma; dilatation
is due to loss of the muscle tone of the intestinal wall
caused by lymphomatous invasion and destruction of
the muscle layers and neural plexuses. These lesions
can reach considerable dimensions and appear as
focal, aperistaltic, ballooned, thick-walled segments
of the intestine filled with barium, with undisturbed
intestinal architecture and with a normal caliber
both proximal and distal to the involved segment
Fig. 7.7.13. Multifocallymphoma. Concentric narrowing with

shouldering of the margins in an ileal loop (black arrow),
distal to a smooth marginal indentation from an enlarged
mesenteric lymph node, encroaching on the intestinal lumen
( white arrowhead). In a proximalloop, a short annular stenosis
with nodular thickening of the mucosal folds (wh ite arrowheads) is also seen. (Reproduced from GouRTSOYIANNIS and
MAKO 1997with permission)
411
Fig. 7.7.14A. CT scan demonstrates multiple polypoid masses with proximal small-bowel dilatation. B Specimen with low power
microscopy demonstrates nodular infiltration of Iymphoma involving small-intestinal submucosa
Fig. 7.7.15A- C. Diffuse nodular infiltration of Iymphoma. A

SBFT demonstrates numerous tiny nodules in the small intestine. B CT shows nodular thickening of mucosal folds (arrow).
C Gross specimen reveals corresponding features of diffuse
nodular infiltration of Iymphoma
c
(BRUNETON and V ALETTE 1990; GOURTSOYIANNIS
and NOLAN 1988; SARTORIS et al.1984) (Fig. 7.7.17).
Ulcerating lesions are encountered in more than
one-third of cases and are often associated with
infiltrating and multinodular forms (BRUNETON and
VALETTE 1990). They represent fairly characteristic
radiologic fi.ndings for intestinallymphoma and are
recognized either as discrete broad-based ulcers
(Fig. 7.7.18) or as large excavating lesions, secondary

to central necrosis of a large neoplastic mass (GouRTSOYIANNIS and NOLAN 1988; SARTORIS et al. 1984)
(Fig. 7.7.19).
Intestinal lymphomas are invariably associated
with enlarged mesenteric lymph nodes, which may
become confluent and cause progressive narrowing
of the lumen of the affected loop. Large extraluminal
412
Fig. 7.7.16A,B. Localized annular infiltrating lymphoma. A CT

shows marked thickening of localized small bowel (arrow).
The attenuation of the thickened wall is relatively homogeneous, which suggests the diagnosis of lymphoma. B Gross
specimen demonstrates annular infiltration of lymphoma
masses that grow in the mesenteric root and may

extend into the retroperitoneum are characteristic of
the mesenteric form of lymphoma. These may result
in displacement, angulation, encapsulation, or a variable degree of narrowing of adjacent barium-filled
loops ofthe intestine (RuBESIN et al.1990).
Fistulas are infrequent, but when they occur, they
often connect to the skin, solid organs, or bladder.
Enteroenteric fistulas are generally associated with
the endoexoenteric type of involvement and may be
difficult to distinguish from an abscess or a conglomerate tumor mass (MEGIBOW 1997). Fistulas arealso
a dassie manifestation of Crohn's disease, but in lymphoma, the communication between adjacent segments is often through a wider channel or a large
Fig. 7.7.17A,B. Primary lymphoma with aneurysmal dilatation. A Enteroclysis (early phase) shows abnormal intraluminal gas collection, separated from adjacent air-filled loops
by soft-tissue thickening. B Enteroclysis (late phase) demonstrates marked dilatation of a jejunal segment with residual contrast. (Reproduced from GOURTSOYIANNIS and NOLAN
1988 with permission)
413
Fig. 7.7.18. Lymphoma with broad-based ulceration. Compression view of an ilealloop demonstrates a narrowed segment
with a !arge, broad-based ulcer (arrowhead). (Reproduced
from GOURTSOYIANNJS and NOLAN 1988 with permission)
cavity (GouRTSOYIANNIS and NoLAN 1988). elinically, fi.stulas in lymphoma are usually asymptomatic,
similar to other malignancies, whereas in inflammatory bowel diseases, they are typically symptomatic.
rhickening of the valvulae conniventes is a less
frequent and nonspecifi.c fi.nding of lymphoma (Fig.
7.7.20). Unlike other types of intestinallymphoma,
thickening of the valvulae, often nodular, involving
long segments of the jejunum is a common and valid
feature of Mediterranean-type lymphoma (RAMOS
et al. 1978). lt is invariably associated with enlarged
mesenteric lymph nodes, which may become confluent and cause progressive narrowing of the lumen of
the affected segment (Fig. 7.7.21).
rhe er appearance of lymphoma is also variable
and includes focal or segmental mural infiltration, cavitation, fi.stula formation, and mesenteric and/or retroperitoneal adenopathy. rhe diagnosis of intestinal
lymphoma may be suggested with a high degree of
confi.dence in the presence of homogeneous focal wall
thickening >2 cm, either nodular or eccentric, in association with an enlarged bowel lumen (LAURENT et
al. 1991) (Figs. 7.7.22, 7.7.23). Pronounced mesenteric
involvement greatly assists in the differential diagnosis. Mesenteric lymphoma may appear as an ill-defi.ned
confluent mass encasing loops of intestine, as bulky
mesenteric adenopathy,a sandwich-like confi.guration,
due to encasement of mesenteric vessels from enlarged
mesenteric lymph nodes, and less often, as a conglomerate mantle of mesenteric/retroperitoneal tissue
(MEGIBOW 1997) (Fig. 7.7.24).
In addition, er has an increasing application in
patients with intestinallymphoma, because accurate
staging is necessary for their management. In most
c
Fig. 7.7.19A- C. Ulcerated Iymphoma. A Amorphaus barium
collection in a jejunal loop, representing a !arge ulcer. B CT
examination shows segmental infiltration and distortion of
the barium-filled Iumen. C Corresponding pathology specimen. (Reproduced from GOURTSOYIANNIS and MAKO 1997
with permission)
patients, er aids in staging the disease, not only by

defi.ning the size and extent of the primary lesion, but
also by allowing noninvasive identifi.cation of mesenteric and retroperitoneal adenopathy or spread to
other intraabdominal organs. Several staging systems
have been applied to primary intestinallymphomas
(HABER and MAYER 1988; HERMANEK and SOBIN
414
B
Fig. 7.7.20A,B. Diffuse small-intestinallymphoma thickening
of mucosal folds. A Enteroclysis demonstrates diffuse thickening of folds of small intestine. B Microscopy demonstrates diffuse submucosal involvement of Iymphoma
1992). It appears that distinction of disease spread from

contiguous regional and noncontiguous lymph node
involvement is an important factor for disease management. Long-term survival has been reported in 60o/o80o/o of patients with tumor confined to the intestine,
in 40%- 60% of patients with regionallymphadenopathy, andin only 10%- 20% of patients who have tumor
spread beyond regional nodes or beyond the abdominal cavity (HABER and MAYER 1988).
Complementary use of detailed barium and CT
examinations enables a diagnosis to be made in most
cases of intestinallymphoma. The differential diagnosis includes mainly Crohn's disease and adenocarcinoma and, less frequently, metastatic melanoma
and leiomyosarcoma. Crohn's disease may demonstrate a strikingly similar pattern to that of Iymphoma (SARTORIS et al.1984}. Features favoring the diag-
Fig. 7.7.21A,B. Mediterranean-type Iymphoma. A Enteroclysis

demonstrates nodular thickening of the mucosal folds of the
jejunum. B CT shows enlarged lymph nodes and marked softtissue attenuation wall thickening of several segments of the
proximal small intestine. (Reproduced from GouRTSOYIANNIS
and MAKO 1997 with permission)
nosis of intestinallymphoma include distallocation,

long segment of involvement, large size, absence of
desmoplastic reaction, which allows for changes in
the shape of lesions with compression, lack of intestinal obstruction, and associated mesenteric involvement with bulky adenopathy (GOURTSOYIANNIS and
MAKO 1997}.
415
Fig. 7.7.22. Lymphoma. Axial CT demonstrates marked mural

thickening of the small bowel with dilatation of involved bowel
Iumen consistent with Iymphoma
B
Fig. 7.7.24A,B. Lymphoma. Mesenteric involvement. A CT
shows confluent mesenteric masses encasing, but not obstructing, barium-filled loops of intestine. B In the same patient
mesenteric vessels are sandwiched between lymphomatous
mesenteric nodal masses. (Reproduced from GouRTSOYIANNIS and MAKO 1997 with permission)
Fig. 7.7.23A,B. Multifocallymphoma. A CT demonstrates a

focal region of wall thickening in a jejunalloop (arrowhead),
representing lymphomatous infiltration. B At a more caudal
Ievel, marked segmental bowel wall thickening, moderately
enhanced after intravenous contrast administration, is demonstrated in an ileal loop with a distended bowel segment.
(Reproduced from GouRTSOYIANNIS 1988 with permission)
416
7.7.5
Vascular Sarcomas
Sarcomas, in general, may be intraluminal, extraluminal, or dumbbell shaped and can grow to a large size.
Patients with intestinal sarcomas are often asymptomatic, which results in a long delay before diagnosis. They often present with massive gastrointestinal
hemorrhage (WALKER 1987). Obstructive symptoms,
sometimes resulting from intussusception, anemia,
and chronic nonspecific abdominal pain are other
less common forms of clinical presentation.
Radiological features of vascular sarcomas
include displacement or encroachment of intestinalloops by large, frequently ulcerated, extraluminal masses, intraluminal filling defects, or infiltrating strictures.
7.7.5.1
Angiosarcoma
Primary angiosarcomas of the small intestine are
extremely unusual, accounting for approximately 3o/o
of all GI tract vascular neoplasms (GouRTSOYIANNIS
et al. 1994). Angiosarcomas are defined as malignant
vascular neoplasms that exhibit morphologic and
functional properties of endothelial cells (WALKER
1987). In the GI tract, they are believed to arise de
novo rather than from pre-existing hemangiomas
(STOUT 1943). Therapeutic pelvic irradiation has
been implicated as a causative factor in a small
nurober of reported cases (NANUS et al.1987; WoLov
et al. 1991).
Patients with intestinal angiosarcomas may present with nonspecific and rather diverse clinical manifestations, including abdominal discomfort, signs of
intestinal obstruction, a palpable abdominal mass,
diarrhea, or undue fatigue and malaise. However, gastrointestinal bleeding, massive or recurrent, and/or
persistent anemia are the most frequently reported
clinical presentations (GOURTSOYIANNIS et al. 1994;
WALKER 1987).
Intestinal angiosarcomas are characteristically
multifocal, occur equally in the jejunum and ileum,
and are usually small in size, although rare lesions
measuring 5 cm in diameter have been reported
(RDONEZ et al.1983).
The radiological appearance of intestinal angiosarcoma is poorly documented. They may appear
as a large, annular, constrictive lesion (RDONEZ et
al. 1983), but more often appear as multiple, small,
sessile, intraluminal polypoid filling defects, invariably accompanied by mucosal ulceration (GouRTSOYIANNIS et al. 1994) (Fig. 7.7.25). The diagnosis
may be difficult, since the appearance of multiple
intraluminal filling defects may be attributed to a
variety of causes, such as multiple adenomas, hemangiomas, Peutz-Jegher hamartomas, the nodular
form of primary lymphoma, and metastases from
malignant melanoma. Furthermore, any of these
conditions may present with gastrointestinal bleeding.
7.7.5.2
Kaposi Sarcoma
Kaposi sarcoma is a systemic, multifocal neoplasm
characterized by pigmented cutaneous lesions and
visceral manifestations. Its incidence in the small
intestine is extremely low and is nearly always
associated with AIDS. Since its first description in
1872 (KAPOS I 1872), three forms of Kaposi sarcoma
have been recognized (GOURTSOYIANNIS 1997b).
The dassie form involves primarily the skin of the
lower limbs, affects mainly elderly European mal es,
and usually exhibits a course that extends over some
15 years. Gastrointestinal involvement is usually a
late development. A second form is an endemic variant that affects African adolescents and is characterized by an aggressive systemic course, early lymph
node and visceral involvement, and a poor prognosis (TAYLOR et al. 1971). AIDS-related Kaposi sarcoma is the third form, sharing the same histogenetic features as the other two and with a similar
clinical behavior to the African form. It is a markedly aggressive and disseminated disorder (RosE et
al. 1982).
Kaposi sarcoma is often asymptomatic in AIDS
patients. However, clinical signs may include gastrointestinal bleeding, intestinal obstruction, and rarely,
intussusception or perforation.
Gastrointestinal involvement is estimated to occur
in 8o/o- 27o/o of patients with AIDS and cutaneous
Kaposi sarcoma (FRAGER et al. 1986; WALL et al.
1986). Gastrointestinal Kaposi sarcoma with no cutaneous or nodal involvement is rare (HANNO et al.
1979). Multifocal involvement, in the form of multiple foci of Kaposi sarcoma, coexistence of tumor and
opportunistic infections, or coexistence ofKaposi sarcoma and non-Hodgkin lymphoma, arenot unusual.
The duodenum is the most common site of gastrointestinal involvement with Kaposi sarcoma (WALL et
al. 1986).
417
Fig. 7.7.25A,B. Angiosarcoma. A Two smoothly outlined, round, sessile, intraluminal filling defects (arrows) in a jejunalloop. B
The resected specimen showing four small-sized nodules (arrows), spread over the mucosa of a 20-cm-long segment of jejunum.
(Reproduced from GouRTSOYIANNI S et al. 1994 with permission)
The radiological features of intestinal Kaposi sarcoma are nonspecific, cover a wide spectrum of
changes, and may show similar findings in the stomach and colon. These include thickening of the valvulae conniventes, mural thickening, submucosal nodularity and/or mucosal irregularity, large polypoid
filling defects, plaque-like lesions that may coalesce,
and less often, a mass effect (WALLet al. 1986) (Fig.
7.7.26). Large lesions may show ulceration or umbilication. In widespread cases, CT may demonstrate
mural thickening, large focal masses associated with
the intestine, or concurrent bulky retroperitoneal
or mesenteric lymphadenopathy and splenomegaly
{JEFFREY et al. 1986).
The differential diagnosis of Kaposi sarcoma
includes Iymphoma, metastases, polyposis syndromes, infiltrating adenocarcinoma, and even
Crohn's disease. Thorough clinical evaluation and not
infrequently fine-needle aspiration cytology may be
necessary for a definite diagnosis.
7.7.6
Gastrointestinal Stroma I Tumors
Gastrointestinal stromal tumors (GIST) are a unique
type of mesenchymal tumors that may occur anywhere in the GI tract, from the esophagus to the
anus. They e:xhibit a wide spectrum of clinical behavior from benign, small, incidentally detected nodules
to frank, malignant tumors. In the earlier literature,
GISTs were categorized as smooth muscle tumors,
including leiomyomas, cellular leiomyomas, leiomyoblastomas, and leiomyosarcomas (APPELMAN 1990).
A better understanding of the ultrastructural and
immunophenotypic characteristics of these tumors
has recently resulted in the use of the histogenetically
neutral designation 'GISTs', to include mesenchymal
tumors of neural differentiation as weil (MAZ UR and
CLARK 1983; MIETTINEN et al.l999b).
The prevalence of GISTs is estimated at 1020/million, according to a recent population-based
418
Fig. 7.7.26A,B. Kaposi sarcorna involving the duodenurn. A

Enteroclysis showsmultiple nodules involving the duodenurn,
causing thurnbprinting or irregular fold thickening (arrows). B
Gross specirnen shows rnultifocal tan discoloration and nodular thickening of folds
study. Of these, 20%- 39o/o are malignant tumors

(FRANQUEMONT 1995). The small intestine is the
second most common location {20o/o- 30o/o) for GISTs.
Malignant GISTs account for less than 15o/o of primary intestinal malignancies, yet they represent the
most common malignant soft-tissue neoplasm of the
small intestine.
Malignant GISTs are single lesions as a rule, most
commonly located in the jejunum and ileum. Their
peak incidence is in the sixth decade. Patients are

almost always symptomatic, with abdominal pain and
gastrointestinal bleeding being the most common
presenting complaints. A palpable abdominal mass
may be encountered in nearly 50o/o of cases. However, partial or complete intestinal obstruction is infrequent despite the large size these tumors usually
attain. The mean duration of clinical symptoms preoperatively is almost 2 years (CHIOTAsso and FAZIO
1982), and the average 5-year survival rate ranges
from 20o/o to 50o/o (AKWARI et al. 1978); a combined
association of symptoms for more than 1 year,
absence of metastases, and a tumor diameter less
than 9 cm favor a better prognosis (CHIOTAsso and
FAZIO 1982).
Histologically, GISTs are typically spindie cell
tumors that have a prominent, nerve sheath tumorlike, nuclear palisading pattern. Other GISTs may
show prominent perinuclear vacuoles. GISTs may
also have an epithelioid appearance, resembling cells
with round nuclei and abundant cytoplasm (MIETTINEN and LASOTA 2001). It is now believed that
GISTs are derived from intestinal cells of Cajal.
Recent application of immunohistochemical sturlies
has revealed strong and uniform expression of the
KIT (CD 117, stem cell factor receptor) protein and
CD34 in GISTs. This offers the possibility to diagnose these tumors accurately and separate them from
other mesenchymal tumors of the GI tract (MIETTINEN and LASOTA 2001).
Malignant GISTs grow slowly, predominantly
extraluminally and eccentrically, and are prone to
develop degenerative changes such as necrosis, hemorrhage, calcification, fistula, or secondary infection.
Determination of the malignant potential of GISTs is
based on factors such as location, tumor size, degree
of cellularity and pleomorphism, and presence or
absence of necrosis. Small-intestinal GISTs less than 5
cm in size are usually benign, regardless of their cellularity. However, GISTs > 10 cm in size and/or with
mitotic counts >5/50 high power field usually behave
in a malignant fashion. Such tumors have a high risk
for liver metastases and/or diffuse intraabdominal
spread. Bone and lung metastases are rare.
The radiologic appearance of malignant GISTs is
fairly characteristic. On barium studies, the rnain feature is frequently a large, extrinsic, nonobstructing
mass displacing or distorting adjacent bariurn-filled
loops of intestine (Fig. 7.7.27). This may be associated
with ulceration, cavitation, or fistula formation. Less
often, they rnay appear as a large cavity filled with
barium, and it may be difficult to identify the connection between the small intestine and the cavity
419
Fig. 7.7.27A- C. Malignant gastrointestinal stromal tumor

(GIST). A Enteroclysis showing a large, nonobstructing, largely
excavated mass, displacing adjacent barium-filled loops of
intestine. B CT demonstrates a large, extraintestinal, inhomogeneous mass. There is no evidence of enlarged lymph nodes.
C Corresponding pathology specimen
c
(GouRTSOYIANNIS and MAKO 1997; SHOJAKU et al.
1997).
er scan may add considerably to the preoperative
evaluation of these tumors (Fig. 7.7.28). lt can accurately demonstrate the size, shape, and extent of the
lesion, uniformity of densities, and enhancing patterns, and it can depict the presence of liver, peritoneal, or other metastases. er is useful in the differen-
a predominantly submucosallocation and/or appear

largely excavated, such as lymphoma or metastatic
melanoma. rhe main differential diagnosis of malignant GISrs, however, includes their benign counterparts, benign smooth muscle or neuragenie tumors.
e r criteria favoring malignancy include an irregular, lobulated, large sized mass (Fig. 7.7.29), heterogeneaus tissue density, centralliquefactive necro-
tiation from other malignant tumors that often have
sis, seen as water density with or without an air-flu-
420
GISTs are distinctive from other malignant smallintestinal neoplasms in that they have a greater tendency to grow extraluminally, to develop large ulcers
and therefore to bleed, and to attain a large size without obstruction; regionallymph node metastases are
unusual for them, and they are accompanied by high
survival rates, even with metastases (GouRTSOYIANNIS and MAKO 1997).
7.7.7
Metastasis
Fig. 7.7.28. Malignant GIST. CT shows a !arge, inhomogeneous, soft-tissue mass, merely hanging from an ileal segment.
Absence of lymph node enlargement
Fig. 7.7.29. Malignant GIST with mesenteric extension. Axial

CT image of a patient with GI bleeding demonstrates a !arge,
exophytic jejunal mass with ulceration (arrowheads)
id level, ulceration, or fistula formation (MEGIBOW

1997). Liver metastases from malignant GISTs are
large, necrotic, or cystic in nature with peripheral
or 'rim' enhancement, whereas peritoneal metastases
may appear as widely distributed, multiple, round,
smoothly outlined, homogeneaus satellite masses
(CHOI et al.1990; HAMA et al. 2001; MIETTINEN et al.
1999a).
The signal intensity on MRI suggests that GISTs
usually have no fibrotic component and that the inner
portion of these tumors does not usually contain
blood products. Their signal intensity on MRI
has been reported to be hyperintense compared
with fat on Tl-weighted imaging. They also show
intense enhancement after gadolinium-chelate injection (HAMA et al. 2001; SEMELKA et al.1996; SHOJAKU
et al. 1997; TERVAHARTIALA and HALAVAARA 1998).
Metastases are the most common malignant lesions of

the small intestine. Neoplasms can spread to involve
the small intestine by direct invasion from adjacent
structures, by lymphatic extension, as embolic bloodborne metastases, and by intraperitoneal seeding
(MEYERS 1981, 1994). More than one mechanism of
spread may be encountered in a particular patient.
Direct invasion of the small intestine from primary colonic, pancreatic, biliary, renal, adrenal, and
gynecological malignancies is not uncommon and
indicates that an aggressive malignant neoplasm has
broken through facial planes that normally separate
the intestine from these organs. The degree of infiltration of the secondary invasion depends on the
desmoplastic response. Intestinal obstruction is a
known presentation of small-intestinal involvement
by recurrent colanie carcinoma (Fig. 7.7.30) and
pelvic malignancies, particularly ovarian carcinoma
(YuHAZ et al. 1985). Such infiltration from the
colon usually involves a shorter segment of intestine
(Fig. 7.7.31), unlike the more intensive involvement
seen with ovarian malignancy (NoLAN 1997). Carcinoma of the hepatic flexure of the colon may invade
the duodenum throughout the first portion of the
transverse mesocolon. Pancreatic tumors can also
infiltrate the duodenum (BUCKLEY and FISHMAN
1998). Duodenal metastases have been associated
with dilatation of the pancreatic or common bile
ducts. Residualtumor may also affect an anastomotic site, leading to narrowing and possible obstruction. Renal and adrenal carcinomas may also metastasize to the small intestine. Especially carcinoma of
the right kidney may invade the descending duodenum and give rise to hypervascularized metastases.
Extension through lymphatic permeation from a
noncontiguous primary carcinoma is rather rare. A
characteristic example is the spread of cecal carcinoma to the terminal ileum. Extensive lymphatic
spread from cecal carcinoma can cause occlusion of
421
Fig. 7.7.30A,B. Secondary invasion by colonic adenocarcinoma. A A long, annular stenosis causing complete obstruction. B
Corresponding pathology specimen. (Reproduced from NoLAN 1997 with permission)
Fig. 7.7.31A,B. Secondary invasion by colonic adenocarcinoma. A Compression view of an ilealloop demonstrates a plaquelike lesion with diffuse nodularity and mucosal distortion, over a short segment of ileum (arrows) B Corresponding pathology
specimen. (A Reproduced from NoLAN 1997 with permission)
the regional pericolic nodal chains and subsequent

retrograde passage in the lymphatics of the ileum,
resulting in progression of the neoplastic process in
the terminal ileum (MOFFAT and GOURLEY 1980).
Narrowing of the Iumen of the terminal ileum, associated with marked thickening of the valvulae conniventes or effacement of the mucosal pattern, is a
characteristic finding seen on barium examination
(NOLAN 1997) (Fig. 7.7.32).
Embolie spread of primary neoplasms is infrequent. Malignant melanomas and carcinomas of the
lung, breast, female genital tract, and kidneys are
the most common malignancies that metastasize to
the small intestine via the bloodstream. Metastatic
deposits tend to be submucosal and are frequently
multiple, although solitary metastases do occur and
may be difficult to differentiate from primary neoplasms of the small intestine (PoTESHMAN 1967).
Central ulceration is a common finding as metastatic
Fig. 7.7.32. Carcinoma of the cecum invading the terminal ileum

via the lymphatics. Compression view of the terminal ileum
showing a short stricture with mucosal destruction. The secondary neoplastic mass was much larger than the primary cecal
carcinoma. (Reproduced from NoLAN 1997 with permission)
422
deposits usually outgrow their blood supply. Gastrointestinal bleeding, obstruction due to intussusception, and occasionally perforation are the usual presenting complaints.
Because of its large blood supply, the small intestine is the most common part of the GI tract to be
involved with metastatic melanoma. In autopsies of
patients who die from this malignancy, the incidence
of metastatic melanoma of the small intestine ranges
from 25.6% to 58% (SHIRKODA and A LBIN 1987; SILVERMAN et al. 1984). Malignant melanoma produces
smooth, round, or polypoid metastases. When multiple, deposits may be either confined to a segment
of intestine or be widespread (Fig. 7.7.33). Ulceration is frequent (Fig. 7.7.34), causing a 'target' or
'bull's eye lesion pattern. Intraluminal growth probably explains the high frequency of transient intestinal intussusception seen with metastatic melanomas (Fig. 7.7.35). The most common CT appearance
of metastatic melanoma is that of a tumor implant
Fig. 7.7.34. Metastatic melanoma. A moderate-sized cavitating

mass is seen, replacing the lumen of a short segment of ileum.
Multiple intraluminal filling defects are present. (Reproduced
from NOLAN 1997 with permission)
Fig. 7.7.33A,B. Melanoma metastases. A Spiral CT demonstrates a homogeneous soft-tissue mass involving the small
bowel. B Axial CT from a patient with known melanoma shows
multiple !arge masses (arrowheads) encroaching on the smallbowellumen
Fig. 7.7.35A,B. Melanoma metastasis in a 30-year-old man

with abdominal pain and small-bowel obstruction. A Barium
study demonstrates small-bowel intussusception. B Resected
specimen shows multifocal, dark-colored melanoma metastasis
or an extrinsic mass or masses (Fig. 7.7.36) that

encroaches on the lumen of the involved segment and
causes an impression on adjacent bowelloops. Concomitant extensive involvement of mesenteric nodes
and metastases to sites other than the small intestine are common (UCKLEY and fiSHMAN 1998;
SHIRKODA and ALBIN 1987).
Metastatic infiltration of the wall of the small
intestine resulting in stricture formation is more frequently seen with breast carcinoma. Although no
desmoplastic response is elicited by breast metastases, the highly cellular submucosal deposits usually
narrow and deform the bowellumen (MEYERS 1994).
There may be a long segment of intestinal narrowing similar to the limitis plastica appearance of breast
carcinoma that has disseminated to the stomach
(Fig. 7.7.37).A feature of metastatic breast carcinoma
isthat the obstruction may be relieved and the symptoms resolved with chemotherapy (NoLAN 1997).
Hematogenous metastases to the small intestine
from bronchogenic carcinoma are rare. Patients usually present with obstruction, bleeding, or perforation, and they carry a poor prognosis. Intestinal
metastases may be single or multiple. Radiologically,
423
they are seen as large mesenteric masses with infiltration of the bowel wall and fixation and angulation of the intestinal segment and mucosal folds
(MEYERS 1994). Occasionally, metastases may feature
as mural rigidity and/or annular constricting lesions
(Fig. 7.7.38). Discrete submucosal deposits with central ulceration are only rarely encountered.
Intraperitoneal seeding of abdominal malignancies to the small intestine may occur as a result of
spread via ascitic fluid, which has a continuous, natural flow within the anatomical pathways of the peritoneal recesses (MEYERS 1973).A primary neoplasm
or even intraabdominallymph node metastases, after
breaking through into the peritoneal cavity, can shed
cells into the ascitic fluid induced (MEYERS 1981).
Sites of predilection for the lodgment and growth
of intraperitoneal seeded metastases clearly follow
the pathways of flow of ascitic fluid and include: the
pouch of Douglas, the terminal portion of the mesentery, the superior aspect of the sigmoid mesocolon,
and the right paracolic gutter. Malignant cells usually implant on the mesenteric border of the small
intestine and incite a fibrotic reaction. The most frequently encountered forms of seeded intraperitoneal
B
Fig. 7.7.36A,B. Metastatic melanoma. Overview (A) and sport view (B) enteroclysis show a solitary, !arge, sharply marginated,
eccentric filling defect, with mucosal destruction and subtle nodularity at its base, in an ilealloop. (B Reproduced from NoLAN
424
Fig. 7.7.37A,B. Metastatic breast carcinoma. AAshort tight stricture is seenon a compression view of a segment of ileum.
BA long segment of narrowing (arrowheads) is additionally seen in a more distal ileal segment. (Reproduced from NoLAN
A
Fig. 7.7.38A,B. Metastatic Jung carcinoma. A Compression view showing an annular-type stenosis with fixation and angulation
of a jejunalloop. B Corresponding pathology specimen. (A Reproduced from NoLAN 1997 with permission)
425
metastases are primary mucinous neoplasms of the

pancreas, colon, and stomach in the male population,
and ovarian carcinoma in the female. The radiological features depend on the size of growth and the
presence and extent of the local desmoplastic reaction (MEYERS 1975). If no significant fibrotic reaction
is elicited as the metastases grow in size, gross extrinsic mass displacement is shown. Discrete separation
of ilealloops, angulated tethering of mucosal folds on
their mesenteric border, and narrowed loops aligned
in a parallel configuration, described as 'palisading'
(MEYERS 1975, 1994) indicate an associated fibrous
response. Multiple, scalloped deflections of adjacent
bowelloops, seen with larger seeded metastases and
marked fixation and angulation of ilealloops in the
right lower quadrant as a result of a severe desmoplastic response, are highly characteristic findings
on barium radiology. CT and MRI can also depict
multiple, small, nodular metastases along the small
bowel serosa, mesentery, and omenturn (Fig. 7.7.39).
lncreased bowel wall thickening, plaque-like thickening of the parietal peritoneum, and mesenteric or
intraperitoneal fat fibrous stranding are additional
findings. As mesenteric masses or stranding are features associated with a number of diseases, such as
Crohn's disease, endometriosis, or carcinoid tumor,
additional imaging findings and clinical history are
mandatory for a confident diagnosis.
7.7.8
Conclusion
Small-intestinal malignant neoplasms are uncommon tumors. The overall survival of patients with
cancer of the small intestine is best for patients discovered with early-stage lesions. This is a challenge
for both the clinician and the radiologist To improve
the prognosis, they should have a high index of suspicion when confronted with nonspecific and/or unexplained gastrointestinal symptoms, such as intermittent pain, episodes of incomplete obstruction, occult
bleeding, or unexplained anemia. Meticulous use of
the sensitive techniques available, familiarity with
imaging findings, and awareness of the importance
of preoperative diagnosis and staging are necessary if
the management of these patients is to be improved.
Fig. 7.7.39A,B. Ovarian metastases. CT (A) and MR (B) images

of a patient with metastatic ovarian carcinoma showmultiple
nodular masses involving terminal ileum and mesentery
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7.8 Parasitic and lnfectious Diseases

of the Smalllntestine
H.K.HA
CONTENTS
7.8.1
7.8.2
7.8.2.1
7.8.2.2
Introduction 429
Infectious Diseases 429
Intestinal Tuberculosis 429
Mycobacterium Avium Intracellulare
Enteritis 433
7.8.2.3 Yersinia Enterocolitica 434
7.8.2.4 Salmonellosis 434
7.8.2.5 Campylobacter Enteritis 435
7.8.2.6 Actinomycosis 436
7.8.2.7 Mucormycosis 438
7.8.2.8 Typhlitis 438
7.8.2.9 Diverticulitis 439
7.8.2.10 Cytomegalovirus Enteritis 439
7.8.3
Parasitic Diseases 440
7.8.3.1 Giardia Lamblia 440
7.8.3.2 Ascaris 440
7.8.3.3 Intestinal Anisakiasis 441
7.8.3.4 Paragonimiasis 442
7.8.3.5 Schistosomiasis Japonica 443
7.8.3.6 Cryptosporidiosis 443
7.8.3.7 Strongyloidiasis 444
References 444
Furthermore, the differentiation of infectious enteritis

from neoplastic and vascular disorders is often difficult. Barium studies offer unique information regarding the mucosal changes, while imaging studies such
as computed tomography (CT) and magnetic resonance imaging (MRI) are advantageaus in demonstrating the mural process and extraluminal pathologies. Therefore, it seems likely that they have a complementary role in assessing the disease characteristics
and extent of the lesion. Because of the nonspecificity
of the radiographic and imaging findings, understanding the clinical and pathological aspects of these diseases may be crucial for establishing the specific diagnosis.
7.8.2
lnfectious Diseases
7.8.2.1
Intestinal Tuberculosis
7.8.1
lntroduction
Enteritis may be caused by various organisms including bacteria, viruses, fungi, and parasites. The patients
infected with these organisms may be asymptomatic
or show a broad spectrum of clinical manifestations.
Adefinite diagnosis requires bacterial or viral cultures
from stool specimens or blood, but the patient's clinical history may sometimes give the clue for a specific
diagnosis, especially in cases of parasitic infections
which are highly prevalent in certain endemic areas.
In many instances, radiographic and imaging findings in these patients overlap to a considerable degree.
H.K.HA,MD
Department of Radiology, Asan Medical Center, University
of Ulsan Medical College, 388-I Poongnag-Dong, Songpa-Ku,
Seoul !38-040, Korea
With the advent of effective antituberculous chemotherapy, the incidence of intestinal tuberculosis had
diminished dramatically by the middle of the century, but it is occurring with increasing frequency in
high-risk populations, such as patients with acquired
immunodeficiency syndrome (AIDS) and other forms
of immunosuppression, intravenous drug abuse, alcoholism, and cirrhosis (HORVATH and WHELAN 1998).
Mycobacterium tuberculosis is the cause of virtually
all cases of intestinal tuberculosis, but Mycobacterium avium-complex (MAC) is also a responsible
agent in AIDS patients. It occurs at any age and is
equally prevalent in male and female patients. The
ehest radiograph shows active disease in only about
one-fifth of patients with intestinal tuberculosis. Several pathogenic mechanisms may be associated with
the development of intestinal tuberculosis: swallowing of infected sputum in active pulmonary tuberculosis; ingestion of contagious milk; hematogenous
spread from the primary focus in other sites; and
430
H. K.Ha
direct extension from adjacent organs (MARSHALL

1993). After the tuberde bacillus enters the gastrointestinal tract, it traverses the mucosa to lodge in
the submucosa. Lymphangitis, endarteritis, and fibrosis ensue, leading to mucosal ulceration, caseating
necrosis, and narrowing of the intestinal tract. Infection often spreads to the mesenteric lymph nodes.
Classically, three forms of intestinal tuberculosis are
recognized: the ulcerative form (60%), hypertrophic
form {10%),and ulcerohypertrophicform (30%). The
affinity of the tuberde bacillus for lymphoid tissue
and areas of physiologic stasis may darify why the
ileocecum is the most common site of disease (MARSHALL 1993).
On barium study, the ulcerative form of tuberculous enteritis may show the ulcers, which are generally transverse and circumferential with a small diameter {3-6 mm) (Fig. 7.8.1). The involved intestinal segment is not long, about 3-7 cm. This orientation of the
ulcers may be related to the arrangement of the submucosal lymphatic structures. The individual ulcers
are round, stellate, or longitudinal (Fig. 7.8.2); they are Fig. 7.8.2. Intestinal tuberculosis. Multiple discrete ulcers
usually superficial and do not penetrate the muscu- (arrows) are scattered through the distal ilealloop with interlaris propria. With progression, the ulcers become vening, normal-appearing mucosal folds on small-bowel folconuent. Although not common, aphthous ulcers low-through
mimicking Crohn's disease can be demonstrated. The
mucosal folds surrounding the ulcers are thickened,
and the mucosal surface may show nodularity caused by the granuloma in the submucosa. The terminal
ileum is commonly narrowed mainly due to spasticity; the ileocecal valve becomes fixed, irregular, gaping,
and incompetent; and the cecum is usually involved,
with a conical and retracted configuration (Fig. 7.8.3).
Accordingly, there is evidence of a wide gap between a
thickened ileocecal valve and a narrowed ileum (Fleischner's sign) and a fibrotic terminal ileum that empties into a rigid contracted cecum (Steirlin's sign). The
shortening of the ascending colon results in an obtuse
angle of the ileocecal valve. The hypertrophic form of
a lesion commonly resulting from a florid inammatory fibroblastic reaction in the submucosa and subserosa occurs predominantly in the ileocecal region and
colon. The involved segment in this form is usually
rigid, with a cobblestone appearance on barium study
(Fig. 7.8.4). In the chronic phase of tuberculous enteritis, multiple, circumferential strictures may develop,
which typically have an hourglass appearance, sometimes causing small-bowel obstruction (Fig. 7.8.5). In
addition to the terminal ileum, the evaluation of other
parts of the small intestine should not be neglected
in the barium study, as we and other researchers
(VAIDYA and SODHI 1978) have experienced that
Fig. 7.8.1. Intestinal tuberculosis. Small-bowel follow-through
about
half of all patients were affected at multiple sites
shows circumferentialluminal narrowing with marginal irreg(40%-50% proximal ileum and pelvic small bowel
ularity (arrows) in the ilealloop
431
Parasitic and Infectious Diseases of the Small Intestine
Fig. 7.8.3. Intestinal tuberculosis. The cecum is markedly

retracted, with marginal irregularity due to ulcers in the terminal ileum and obtuse ileocecal valve (arrow) on double contrast barium enema (from HA et al. 1999)
Fig. 7.8.5. Chronic intestinal tuberculosis. Double contrast

barium enema shows fibrotic stricture (arrowheads) in the
terminal ileum with retracted cecum (arrow) (from HA et al.
1999)
Fig. 7.8.4. Intestinal tuberculosis. Small-bowel follow-through

shows multifocal areas of circumferentialluminal narrowing
(solid arrows) in the ilealloop along with evidence of cobblestone appearance of the mucosa (open arrows) (from HA et
al. 1999)
Fig. 7.8.6. Jejunal tuberculosis with low-grade bowel obstruction. Small-bowel follow-through shows stricture involving the
distal jejunum. A polypoid mass (straight arrows) is seen proximal to the stricture, which was proved to be granuloma on histopathological examination. Focal stricture (curved arrow) is
also noted in the ascending colon (from HA et al. 1999)
432
H. K.Ha
loops and So/o-10% jejunum) (Fig. 7.8.6). The differentiation of ileoeeeal tubereulosis from Crohn's disease may be virtually impossible. However, tubereulosis usually develops on both sides of the ileoeeeal
valve and almost always involves the valve, which
may become widely open and rigid, while the eeeum
beeomes retracted and indented. The superficial uleers
tend to be cireumferential, with the long axis perpendicular to the lumen. In Crohn's disease, the eeeum is
more often intaet, and the ileoeeeal valve may remain
intaet, while the ileum is often involved for a Ionger
length than in tubereulosis (BROMBART and MASSION
1961). In eontrast to Crohn's disease, there have been
limited reports in the Iiterature deseribing the CT features of intestinal tubereulosis. However, in our experienee, CT is very useful for determining the extent
of disease, deteeting eomplieations, and differentiating
it from Crohn's disease. The eommon CT finding of
tubereulous enteritis is bowel wall thickening (Fig.
7.8.7), with a range of 1-2 em in thiekness (HA et al.
1999). The thickened bowel may show homogeneous
attenuation on CT, but mural stratifieation is rarely
seen. Multiple sites of involvement with skipped areas
are eommon. Therefore, there seems to be no speeifie
CT features ofbowel wall involvement patterns in intestinal tubereulosis which ean be used to distinguish it
from Crohn's disease. Bowelloop separation ean be
eaused by mesenteric lymphadenopathy or Iymphadenitis, bowel wall thickening, intraperitoneal fluid eolleetion, and rarely fibrofatty proliferation in the mesentery. Although not always the ease, lymph nodal
involvement patterns differ from those of Crohn's disease. The enlarged lymph nodes are eommonly larger
than 1 em, may have a low attenuation eenter due to
easeating neerosis, commonly involve the peripanereatie nodal ehains, and may eontain ealeifieation (HA et
al. 1996). The ineidenee of peritonitis in patients with
intestinal tubereulosis has not been weil deseribed, but
the presenee of peritonitis on CT seans may favor the
diagnosis of tubereulosis rather than Crohn's disease
in circumstanees where the differentiation between the
two diseases should be made (HA et al. 1996; MAKANJUOLA 1998). The CT findings of tubereulous peritonitis may mirnie those of peritoneal eareinomatosis,
including diffuse omental and mesenteric infiltration
and nodules, peritoneal thickening, and ascites (Fig.
7.8.8) (HA et al. 1996). In addition, the incidenee of
spienie involvement is common in abdominal tubereulosis, which includes splenomegaly, hypoattenuated
nodules, or ealeifieations (HA et al. 1996).
Although intestinal tubereulosis is a ehronic disease, acute onset of abdominal symptoms may develop due to their eomplieations. A broad speetrum of
eomplieations include intestinal obstruetion, bowel
perforation, fistula, gastrointestinal bleeding, enterolithiasis, venous thrombosis, and traetion divertieula
(MARSHALL 1993; BHANSALI 1977; MAKANJUOLA et
al. 1998). Intestinal obstruetion is the most eommon
eomplieation of tubereulous enteritis, with an incidenee of 12o/o-60o/o of patients (MARSHALL 1993).
The meehanisms may include inflammatory thiekening of the bowel wall, especially in eases of hypertrophic or uleero-hypertrophic type with a long length
of strieture or multiple areas of involvement, and
intraperitoneal adhesion (HA et al. 1996). lt should
be noted that this eomplieation eommonly oeeurs
during the medieal therapy. Healing by eieatrization
in the eourse of antitubereulous therapy inereases
Fig. 7.8.7. Intestinal tuberculosis. The bowel wall of both the

ileum (asterisks) and right-sided colon (c) including appendix
is diffusely thickened with marked contrast enhancement on
CT. Note prominent regional mesenteric vessels (hypervascularity) (arrows)
Fig. 7.8.8. Intestinal tuberculosis with peritonitis. Computed

tomography (CT) scan shows concentric bowel wall thickening
(arrowheads) of the ascending colon with target appearance.
Also, diffuse omental and mesenteric infiltration with granular
lesions as weil as peritoneal thickening and ascites are evident
the tendency to develop obstruction, and the use of

modern chemotherapeutic agents, such as rifampicin, also partly plays a role in developing cicatrization
(ANAND et al. 1988). Single or multiple bowel perforations may occur in patients with ulceration proximal to the obstruction (Fig. 7.8.9) (HA et al. 1996).
However, it may be confined to a localized area when
pre-existing adhesive change is present. The incidence of fistulae is lower than that of Crohn's disease
but may result from either bacterial invasion of the
necrotic area in the bowel, a penetrating abscess, or
the sequelae of the confined perforation (PARTEL and
DE 1972).
7.8.2.2
Mycobacterium Avium lntracellulare Enteritis
Mycobacterium avium intracellulare (MAI) is the

most common cause of systemic bacterial infection in
patients with AIDS. lt frequently affects the gastrointestinal tract as weil as the hepatobiliary system (ARMSTRONG et al. 1985; YOUNG et al. 1986). Patents typi-
433
cally present with progressive weight loss, watery diarrhea, malabsorption, fever, and chill. This disease is
often called pseudo-Whippie disease because of the
clinical, histologic, and radiologic similarities (PooRMAN and KATON 1994). The singlemostsensitive test
for the diagnosis of disseminated MAI is the peripheral
blood culture, with a reported sensitivity of 86%-98%
(YouNG et al. 1986). The CD4+ lymphocyte count is
usually less than 60/mm3 The radiographic findings
on small-bowel examination may be nonspecific. The
small-bowel mucosal folds are diffusely and regularly
thickened, with a 'stacked coin' appearance (Fig.
7.8.10) (POORMAN and KATON 1994; VINCENT and
ROBBINS 1985). Various dilatations of the lumen and
increased secretions may be present. These features
are usually most prominent in the duodenum and
jejunum. CT may demonstrate bowel wall thickening,
especially in the jejunum (Fig. 7.8.10). The presence
of low-attenuation mesenteric and retroperitoneal
lymphadenopathy is characteristic. U nlike other infectious processes, the nodes in MAI infection are often
bulky and may be impossible to distinguish from Iymphoma (HoRTON et al. 1999). Hepatosplenomegaly
can also be seen.
a
Fig. 7.8.9a-c. Chronic intestinal tuberculosis. a Multiple strictures (arrowheads) are seen in the distal jejunum, along
with evidence of obliteration (S) of the mucosal folds in the
involved segment. b,c On CT, bowel wall (arrows) at the stricture site of the jejunum is concentrically thickened with proximalloop dilatation (J)
H. K. Ha
434
Fig. 7.8.10a,b. Mycobacterium avium intracellulare enteritis. a

Small-bowel follow-through showsdiffuse mucosal fold thickening (arrows) of the jejunum, as weil as bowel dilatation. b CT
shows fold thickening and bowel wall thickening of the smallbowelloops (arrows) with evidence ofbowel dilatation. Mesenteric lymphadenopathy (curved arrows) is also seen. (Courtesy
of KC Cho, MD, New Jersey, USA)
7.8.2.3
Yersinia Enterocolitica
Yersinioses are primarily diseases of animals caused
by Yersinia enterocolitica, which is an anaerobic,
gram-negative bacillus. However, human infections
are recognized with increasing frequency all over the
world. In man, the alimentary tract is probably the
portal of entry in most cases. The proposed modes
of infection are intake of contaminated food, contact
with infected animals, or person to person transmission. Enteric infection causes mucosal ulcerations in
the terminal ileum, necrotic lesions in Peyer's patches, and enlargement of the mesenteric lymph nodes.
Although most patients are under 5 years of age, the
clinical presentation varies with age, sex, and immunological state of the host; acute enteritis ( <5 years),
mesenteric adenitis (5- 15 years), acute terminal ileitis (10-20 years), gastroenteritis, erythema nodosum, and polyarthritis (adults) (FERRER et al. 1990).
The main clinical symptoms are watery diarrhea, a
low-grade fever, and abdominal pain. Most cases are
self-limited, but complications may include appendicitis, diffuse ulceration, and inflammation of the
small intestine and colon, intestinal perforation, peritonitis, ileocolic intussusception, toxic megacolon,
mesenteric venous thrombosis, and gangrene of the
small bowel (CovER and ABER 1989).A definite diagnosis can be made after the isolation of Y. enterocolitica together with the demonstration of a rising anti-
body titer (VANTRAPPEN et al. 1982). The terminal

ileum is the most common site of involvement, but
the ileocecal valve, cecum, and other parts of the
colon can be involved (MATSUMOTO et al. 1990).
The radiographic findings on barium study include
solitary or multiple aphthoid ulcers to longitudinal
ulcers, diffuse fold thickening, and nodularity predominantly at the terminal ileum (Fig. 7.8.11) (VANTRAPPEN et al. 1982). Aphthoid ulcers may also be
seen in the colon. These radiographic features resemble Crohn's disease, but fibrotic stenosis and fistula
formation are not findings of Yersinia ileitis. In most
patients, the radiographic abnormalities may be normalized on follow-up study. CT and sonography may
detect bowel wall thickening of the distal ileum as
well as enlarged mesenteric lymph nodes (MATSUMOTO et al. 1991).
7.8.2.4
Salmonellosis
Salmonellosis is one of the common causes of acute
gastroenteritis. Salmonella species are gram-negative,
nonspore-forming bacilli, and in humans the disease
is usually contracted by the ingestion of contaminated
foods, notably meat, dairy products, poultry, and eggs.
Susceptibility to infection is heightened in patients
afflicted by sickle cell anemia, hemolytic disease, and
immune deficiency. The terminal ileum may be mainly
Parasitic and Infectious Diseases of the Small lntestine
435
Fig. 7.8.lla,b. Yersiniosis. a Barium enema shows multiple

nodular defects (arrows) at the terminal ileum. b CT scan
shows mesenteric lymphadenopathy (arrows) in the same
patient
affected, although colanie changes are also seen. The

organisms penetrate the wall of the small bowel, invading the lymphoid tissue of Peyer's patches, with the
development of a small, longitudinally oriented ulcer.
Ileal inflammation is usually superficial, involving the
mucosa and lamina propria. Once the patient recovers, intestinal lesions heal with minimal fibrosis, so
that stricture formation is unusual. The diagnosis is
established on bacteriological grounds. Small-bowel
study may show diffuse mucosal fold thickening with
ulceration in the distal ileum (Fig. 7.8.12). Because of
the nonspecificity of radiological findings, the information from clinical findings such as a sudden onset
of nausea, vomiting, fever, crampy abdominal pain,
and diarrhea is important to make a diagnosis. CT
findings include circumferential and homogeneaus
thickening of the terminal ileum over a segment of
10-15 cm (Fig. 7.8.13) (BALTHAZAR et al. 1996). The
colanie wall can also be mildly thickened. Small-bowel perforation with peritonitis can occasionally occur
(Fig. 7.8.13) (FRANCIS and BERK 1974; SAFFOURI et
al. 1979).
7.8.2.5
Campylobacter Enteritis
Campylobacter fetus subspecies (especially jejuni and

fetus), which are small, microaerophilic, oxidase-positive curved, or S-shaped gram-negative bacteria, have
recently been recognized as an important cause of
Fig. 7.8.12. Salmonellosis. Small-bowel follow-through shows

mucosal fold thickening and marginal irregularity (arrows )
due to the presence of mucosal ulcers in the ileal loop
436
Fig. 7.8.13. Perforated salmonellosis. CT scan shows concentric

bowel wall thickening (asterisks) in the ileum as well as in the
ascending colon (arrowheads). Perforated site (curved arrow)
in the involved ilealloop is weil demonstrated with evidence
of pneumoperitoneum (not shown) and ascites
diarrheal illness in humans (Loss et al. 1980). The

transmission of this infection occurs by the fecaloral route through contaminated food and water or
by direct contact with fecal material from infected
animals or persons (BLASER et al. 1979). The sites of
tissue injury primarily include the jejunum and ileum,
but the colon can also be involved (Loss et al. 1980).
The typical clinical syndrome includes acute onset
of diarrhea, abdominal pain, fever, and constitutional
symptoms; this clinical attack follows an incubation
period of 3-5 days (range 1-10 days). In about 50%
of the patients, the acute episode lasts for an average
of 3-4 days (range 24 r to 3 weeks). While the disease
is usually self-limited, relapses occur in about 20%,
which makes it difficult to distinguish this infection
from other inammatory bowel diseases (BRODEY et
al. 1982). The diagnosis is based on a positive stool
culture or a positive blood culture. The radiographic
features are nonspecific and include bowel wall thickening, irregularity, and spiculation along with luminal narrowing (BRODEY et al. 1982). Nodular lymphoid hyperplasia is also seen in the terminal ileum
(RODEY et al. 1982).
7.8.2.6
Actinomycosis
Actinomycosis is a chronic, progressive, suppurative
disease characterized by the formation of multiple
abscesses, draining sinuses, abundant granulation,
and dense fibrous tissue. This infection is considered
to be caused by Actinomyces organisms (most com-
H. K.Ha
monly, A. israelii), which are gram-positive anaerobic bacteria; they are not regarded as virulent human
pathogens and are best considered as opportunistic
pathogens as they are normally present in healthy
individuals, especially in the oral cavity, tonsilar
crypts, and colon (BERADI 1979; BROWN 1973 ). Dental
caries are also common reservoirs of Actinomyces
(BENNHOFF 1984). It has a worldwide distribution
and is present with equal frequency in city and
rural dwellers (BERADI 1979). Although no discernible sex predilection has been reported, the majority
of patients (94%) are female (BERADI 1979; YEGUEZ
et al. 2000). Human actinomycosis commonly occurs
in three distinct forms. The majority of cases is
cervicofacial (55%), with only 20% occurring in an
abdominopelvic form and 15% as the thoracopulmonic form (BENNHOFF 1984; YEGUEZ et al. 2000).
Abdominopelvic actinomycosis has been known tobe
associated with abdominal surgery (such as appendectomy), bowel perforation, or trauma (SHAH et al.
1987; MALONEY and CHo 1983). Recently, the association with a long-standing lUD has been emphasized as a risk factor in young women ( O'CoNNOR et
al. 1989; LAURENT et al. 1996; ASUNCION et al. 1984).
Various abdominal organs can be involved in abdominopelvic actinomycosis, including the gastrointestinal tract, ovaries, liver, gallbladder, and pancreas
(BERADI 1979; NIETHAMMER et al. 1990). In many
instances, the gastrointestinal tract appears to be secondarily involved, and the rectosigmoid colon and
ileocecal region, including the appendix, are most
commonly involved (BERADI 1979; ScHMIDT et al.
1999). The clinical features depend upon which
organs are affected, but common symptoms and signs
include fever and leukocytosis (BERADI 1979; HA et
al. 1993). The presumptive diagnosis is made when
'sulfur granules' are seen in the Papanicolaou smears
of pus in the abscess or discharged material from the
sinus tract (GuPTA et al. 1976). Although histologic
identification of actinomycotic granules or culture of
the Actinomyces or both (BERADI 1979) is important
in order to establish a definite diagnosis, the success
rate is less than 50% (BENNHOFF 1984).
The radiological findings in the colon and small
intestine on barium study include mural invasion
with stricture formation, mass effect with tapered
narrowing of the Iumen, and thickened mucosal
folds (Fig. 7.8.14) (MALONEY and CHO 1983; NIETHAMMER et al. 1990; HA et al. 1993). The use of CT
in patients with abdominopelvic actinomycosis is
important for suggesting the diagnosis and determining the anatomic location and extent of this disease as well as for monitoring the effectiveness of
Parasitic and Infectious Diseases of the Smaii Intestine
437
Fig. 7.8.14a,b. Actinomycosis infection involving the small

intestine and transverse colon. a CT scan shows a poorly
demarcated, weil enhancing, and infiltrative mass (A) in the
omenturn with extension to the abdominal waii and involvement of the jejunum (arrowheads). b Small-bowel followthrough shows focal, tapered, Iumina! narrowing (arrowheads)
of the distal jejunum along with nodular fold thickening. Also
note Iumina! narrowing (arrows) of the mid-transverse colon
(from HA et al. 1993)
treatment and for follow-up in cases of possible

recurrence (LAURENT et al. 1996; HA et al. 1993;
HARRIS et al. 1989). Because of its aggressiveness
and infiltrative nature, this disease can easily be
mistaken for gastrointestinal malignancy on er,
including carcinoid tumor, intestinal tuberculosis,
erohn's disease, diverticulitis, or other complicated gastrointestinal infection. The main er feature
when the gastrointestinal tract is involved is bowel
wall thickening (mostly, concentric). The mean wall
thickness of 1.2 cm and the mean length of 8.3 cm
overlap considerably with those of other inflammatory bowel diseases. However, rather than bowel
wall thickening, the most important er feature for
the correct diagnosis is the presence of a large mass
adjacent to the involved bowel (Fig. 7.8.15); we
noted the mass in 17 of our 18 patients (LEE et al.
2001). Such a mass appears to be predominantly
cystic or solid. The presence of abundant granulation and dense fibrous tissues in the solid components of these masses may cause hyperattenuation
after infusion of contrast material. It should also
be noted that these lesions show an aggressive infiltration pattern with a propensity for crossing the
fascial planes or boundaries, and involve multiple
compartments. These tendencies are attributed to
the proteolytic enzyme produced by A. israelii
(LAURENT et al. 1996). Soft-tissue strandings are
also prominent, surrounding the involved bowel
Fig. 7.8.15. Actinomycosis infection involving the gastrointestinai tract. CT scan shows ill-defined, soft-tissue lesion (arrowheads) occupying the right lower abdomen as weil as evidence of bowel waii thickening of the distal ileum (arrows)
and diffuse infiltration in the regional fat plane (from LEE et
al.2001)
or mass. Because of the size of the bacterium, the

organism of actinomycosis usually does not spread
via the lymphatics, and therefore regional lymphadenopathy is uncommon or develops late (BENNHOFF 1984; YEGUEZ et al. 2000). Early diagnosis
is important in order to minimize the morbidity
of this disease and to avoid unnecessary surgery
because the response to treatment with high doses
438
of penicillin is usually quite favorable (BENNHOFF

1984; HA et al. 1993).
7.8.2.7
Mucormycosis
Mucormycosis is a relatively uncommon, opportunistic infection caused by fungi of the order Mucorales
(CALLE and KLATSKY 1966). The disease is known to
occur especially in association with diabetes mellitus,
leukemia, or Iymphoma (CALLE and KLATSKY 1966).
When the gastrointestinal tract is involved, the stomach is the most common site of involvement, while
the intestinal form has a predilection for the terminal
ileum and cecum (LYON et al. 1979). Gastrointestinal
involvement usually complicates local disease processes such as intractable peptic ulceration, amebic
colitis, persistent peritonitis, and malnutrition (CALLE
and KLATSKY 1966; LEHRER et al. 1980). However,
they pursue a fulminant and rapidly fatal course in
certain instances (LYON et al. 1979). Thesefungi exhibit a remarkable tendency to infiltrate the walls of
blood vessels, especially arteries. They grow profusely
into the vessellumen and initiate acute vasculitis and
thrombosis of major blood vessels. As a result, ischemic infarction can occur in any organ (LEHRER et
al. 1980; HAGSPIEL et al. 1995). In some instances,
venous involvement with thrombosis causes hemorrhagic necrosis (McBRIDE et al. 1960). CT shows
diffuse circumferential wall thickening of the small
bowel, intermingled with areas of both intense and
poor contrast enhancement (Fig. 7.8.16) (LEE et al.
2000). Pathologically, poorly enhanced areas coincide
with places of necrosis and infarction, while intensely
H.K.Ha
enhanced areas represent the regions of edema and

hemorrhage in the submucosa and muscle layers due
to congestive changes. Therefore, such CT findings
might easily be confused with chemotherapy-induced
necrotizing enteropathy if they were seen in patients
with Iymphoma or leukemia who had undergone chemotherapeutic regimens.
7.8.2.8
Typhlitis
Neutropenie colitis is a necrotizing enterocolitis occurring as a complication of acute leukemia or other neutropenie states such as aplastic anemia, systemic Iupus
erythematosus, or cyclic neutropenia. The cecum is
most commonly involved, but the remaining colon
and distal ileum may also be affected. Various factors
account for the predominant cecal involvement by
neutropenie colitis (ABRAMSON et al.1983). The cecum
represents an area of relative stasis of the bowel contents and is easily distensible. Mucosal ulcerations
create a mural port of entry for the resident colonic
microflora and allow the overgrowth ofbacteria, viruses, or fungi, causing edema, thickening, and induration ofthe cecal wall (ABRAMSON et al. 1983; HUNTER
and BJELLAND 1984). Ifleft untreated, it progresses to
transmural necrosis and colonic perforation, resulting
in septicemia and death. Uncomplicated neutropenie
colitis is managed conservatively, but any evidence of
perforation, abscess formation, or significant bleeding
is an indication for surgery (ABRAMSON et al. 1983).
Typical clinical features include fever, watery diarrhea,
abdominal pain, and occasionally a palpable mass. CT
findings are nonspecific and include concentric homo-
Fig. 7.8.16a,b. Bowel perforation due to mucomycosis infection in the gastrointestinal tract. a CT shows diffuse, circumferential, bowel wall thickening with areas ofboth intense (ar rowheads) and poor (arrow) contrast enhancement. b Follow-up
CT scan shows thinning of the bowel wall thickening. However, the bowel wall definition becomes completely lostat multiple
sites of the ileum due to transmural infarct, along with evidence of extraluminal fluid and air collections (arrowh eads).
(From LEE et al. 1999)
439
7.8.2.10
Cytomegalovirus Enteritis
Fig. 7.8.17. Typhlitis developed in a patient with a history

of chemotherapy for Iymphoma. The wall in the cecum and
terminal ileum is heterogeneously thickened (arrows), with a
multilayered appearance due to mural edema
geneous or heterogeneaus thickening of the bowel wall

with intramural edema and necrosis, pericolic fluid,
and pneumatosis intestinalis (Fig. 7.8.17} (FRICK et al.
1984).
7.8.2.9
Diverticulitis
Small diverticula may not be recognized on CT because

the distinction between a diverticulum and bowelloops
is usually impossible. CT findings which may be useful
in identifying small-bowel diverticula include the large
size of a diverticulum (greater than 3 cm), different contents between the diverticulum and adjacent small-bowel
loops, and absence of valvulae conniventes (CHou et al.
1998). The diagnosis of diverticulitis can be suggested on
CT when an inflamrnatory mass containing air and/or
oral contrast material with edema of the adjacent mesentery is detected in an unusuallocation, distant from the
area of the ileocecal valve and from the sigrnoid colon
(Fig. 7.8.18) (GAYER et al. 1999; GREENSTEIN et al. 1986);
the contrast material within a diverticulum may remain
for several days after completing the CT scanning. Diverticulitis may mirnie many other conditions on CT, such
as abdominal abscess associated with appendicitis or
inflamrnatory bowel disease, perforated colon cancer,
and perforated right-sided colonic diverticulitis.
Cytomegalovirus (CMV) is a herpes virus that can

be sexually transmitted or transmitted via infected
organs, blood, or needles. CMV remains in a latent
state in the host after initial infection. With increasing
impairment of cell-mediated immunity, particularly
a CD4 lymphocyte count of less than 100 mm3,
viral reactivation may occur (WALL and JoNES 1992).
Clinically evident CMV infections most commonly
affect immunosuppressed patients, including transplant recipients and patients with AIDS. However, this
infection may occasionally occur in nonimmunosuppressed individuals, which include patients with diabetes mellitus, those who receive corticosteroids or
undergo radiation therapy, and elderly patients (SPIEGEL and ScHWABE 1980}. The clinical manifestations
usually include diarrhea, hematochezia, abdominal
pain, and constitutional symptoms.Although the colon
is the organ most commonly affected, the incidence of
small-bowel involvement is not uncommon (TEXIDOR
et al. 1987; MuRRAY et al. 1995). Radiographie features include ulcers of various sizes and depth along
with mucosal fold thickenings and luminal narrowing
(TEXIDOR et al. 1987}. The ulcers are usually numerous, round or serpiginous, often reaching the muscular layer with subsequently common occurrence of
bowel perforation; CMV inclusions in the capillaries
and venules of the mucosa and submucosa may produce focal ischemias that are responsible for the mucosal ulcerations (GoonMAN and PORTER 1973}. These
features simulate those of inflammatory bowel disease, bacterial or parasitic infection, ischemic bowel
disease, lymphoma, and graft-versus-host disease. CT
Fig. 7.8.18. Jejunal diverticulitis. CT scan shows diffuse inflammatory change (asterisks) in the mesenteric fat and diverticu-
lar abscess (d) (courtesy of KC Cho, New Jersey, USA)
440
H. K. Ha
blia. It is initiated by ingestion of Giardia cysts, and

excystation occurs in the proximal small intestine.
rhe resultant trophozoites then take up a location
in close proximity to the surface epithelium and are
responsible for the diarrhea and malabsorption (PARTHING 1996). Outbreaks have been linked to contaminated water supplies and situations involving personto-person contact. High-risk groups include infants
and young children, travellers, and immunocompromised patients. In infants and young children, nutritional insufficiency can have profound effects on
growth and development. Most cases can be diagnosed by a single stool examination. Radiographie
findings may include nonspecific mucosal fold thickening in the duodenum and jejunum (Fig. 7.8.20)
(HERLING ER 1994). er findings has been reported to
show thickening of the wall of the duodenum and jejunum and mesenteric lymphadenopathy (0RCHARD
and PETORAK 1995).
7.8.3.2
Ascaris
Fig. 7.8.19a,b. Cytomegalovirus enterocoitis. a The circular

folds of the ileum are diffusely thickened (arrowheads) with
spastic narrowing of the Iumen on a single phase study of
enteroclysis. b Bowel wall at the involved segment of the
ileum (asterisk) is minimally thickened with proximal loop
dilatation. Also note diffuse concentric bowel wall thickening
(arrowheads) of the rectosigmoid colon. (Courtesy of DT
Maglinte, MD, Indianapolis, USA)
may demoostrate bowel wall thickening in both the

small and large intestine, lymphadenopathy, and ascites (Fig. 7.8.19) (MURRAY et al. 1995).
7.8.3
Parasitic Diseases
7.8.3.1
Giardia Lamblia
Giardiasis is a small intestinal infection with the protozoan parasite, Giardia intestinalis. Isolates obtained
from humans are commonly given the name G. lam-
Ascaris in man is infection by the nematode Ascaris

lumbricoides. It occurs with the greatest frequency
in moist tropical countries and in overcrowded rural
communities. eontamination of soll by human feces is
a key factor in the spread of this infection. rhis disease
seldom produces any symptoms, but heavy infections
may cause nausea, vomiting, abdominal discomfort,
and anorexia. Although very rare, a bolus of worms
can obstruct the intestine, most commonly at the terminal ileum and at the ileocecal valve. Adult worms
may also invade the appendix, causing acute appendicitis. Serious complications arise when adult worms
migrate into the ampulla of Vater, and thence to the
pancreatic or biliary ducts, resulting in obstructive
jaundice, cholangitis, cholecystitis, and pancreatitis
(PRICE and LEUNG 1988). rhe diagnosis is usually
made by identifying eggs in the feces; however, adult
worms are occasionally found in feces or ernerging
from body orifices. On barium study, ascariasis can
be diagnosed by identifying the tubular filling defect
of the worm within the opacified small-bowellumen
(Fig. 7.8.21). rhe Iumen of the worm's digestive tract is
also frequently barium-filled, thereby confirming the
diagnosis. er may show a long, tubular structure outlined by the contrast-filled small-bowelloop together
with a trace amount of contrast within the worm's gut
(Fig. 7.8.21) (HOMMEYER et al. 1995).
441
b
Fig. 7.8.20a,b. Giardiasis. a Small-bowel follow-through showsdiffuse thickening (arrows) of the duodenaland jejunal mucosal folds. b After effective medical treatment, the mucosal folds in the jejunum become nearly normalized. (Courtesy of DT
Maglinte, MD, Indianapolis, USA)
Fig. 7.8.21a,b. Ascaris. a A long, linear, tubular filling defect

(arrows) is seen in the proximal ilealloop on small-bowel follow-through. b CT scan of the same patient shows a tubular
hypoattenuated lesion (arrows)
7.8.3.3
Intestinal Anisakiasis
Anisakiasis refers to the infestation of humans by
species of marine nematode larvae belanging to the
subfamily Anisakiae. Humans become infected by
ingesting raw or improperly cooked seafood dishes.
Although the starnach is the most common site of
involvement (75%), the small intestine and colon can
be involved in 25% of cases (IKEDA et al. 1989). In cantrast to acute gastric anisakiasis in which acute gastrointestinal symptoms occur 4-6 h after the ingestion of
raw or poorly cooked fresh fish, the clinical symptoms
in intestinal anisakiasis usually occur within 7 days of
ingestion, including diffuse abdominal tenderness or
colicky abdominal pain and sometimes even intestinal
obstruction. Therefore, it can be easily mistaken for
other acute abdominal diseases such as acute appen-
442
H.K.Ha
7.8.3.4
Paragonimiasis
b
Fig. 7.8.22a,b. Jejunal obstruction due to anisakiasis infection. a Concentricalluminal narrowing (arrows) in the proximal jejunum on small-bowel follow-through. b CT scan shows
bowel obstruction (arrow) at the proximal jejunum (f)
dicitis. The radiographic features include irregular

bowel wall thickening together with mucosal edema,
luminal narrowing, and dilatation of the proximal
bowelloops (Fig. 7.8.22) (MATSUI et al. 1985). The
worm itself may manifest as a thread-like or linear
filling defect within the involved intestinal segment
(MATSUI et al. 1985; MATSUMOTO et al. 1992). CT may
show bowel wall thickening, inflammatory infiltrates
in the adjacent mesentery, and ascites. Target sign may
be demonstrated in the involved bowel segment. The
differential diagnosis includes eosinophilic enteritis,
intestinal tuberculosis, erohn's disease, bowel ischemia, and Iymphoma. The correct diagnosis requires
an appropriate history and immunoserological examination (MATSUI et al. 1985).
Paragonimiasis is a parasitic disease caused by the

trematode P. westermani or other species of Parogonimus. Human infection occurs by ingestion of raw or
improperly cooked freshwater crab or crayfish infected with the metacercarcia. Once ingested, the larvae
escape from the cyst in the small intestine, penetrate
the intestinal wall, and enter the peritoneal cavity.
In 3-8 weeks, they penetrate the diaphragm and
pleura and enter the lung (eHAI 1971). Therefore,
the abdominal cavity is the pathway of migration of
this lung fluke after the larvae excyst in the small
intestine. Ectopic lesions appears tobe produced by
wandering adult organisms residing in the abdominal cavity (eHAI 1971), and most of these patients
have associated lung lesions or a history oflung disease (eHA et al. 1994). The diagnosis is made on the
basis of clinical symptoms, absolute eosinophilia,
positive findings on a serologic test, or detection of
ova or worms in the feces or in a pathologic specimen.
er is a valuable tool for determining the presence
and extent of both gastrointestinal tract and intraperitoneal involvement in this infestation (RHA et al.
1999). The er features when this parasite involves the
gastrointestinal tract and peritoneal cavity include
intramural mass formation or bowel wall thickening
of the starnach or small intestine, often simulating
submucosal tumor on barium study. The perienteric
or perigastric space adjacent to the involved bowel
may show a characteristic finding of single or multiple, abscess-like, multisepated cyst masses (Fig.
7.8.23) (RHA et al. 1999); they can be calcified in a
late stage. These masses represent parasitic granulomas containing caseous necrotic debris with scattered Paragonimus ova. The differential diagnosis of
these masses may include intraperitoneal abscess,
pancreatic pseudocyst, and multicystic tumors such
as lymphangioma, mesothelioma, and pancreatic or
ovarian cystic tumors. However, a multiplicity of
multiseptated cystic masses in different locations, a
relatively chronic process, and a low-grade fever help
differentiale parasitic granuloma from other diseases. Moreover, the presence of pleural effusion and
lung cysts suggests paragonimiasis infestation. Other
er findings include nonspecific, localized, granular
infiltration in the perienteric or perigastric space or
in the omentum, minimallymphadenopathy (mostly
less than 1 cm in diameter) in the retroperitoneum
or upper abdomen, and a small amount of ascites
(RHA et al. 1999). However, it should be noted that
Fig. 7.8.23. Parasitic granuloma in the peritoneal cavity due

to paragonimiasis. A cystic mass of parasitic granuloma (P)
simulating a dilated bowelloop causes small-bowel obstruction due to bowel adhesion
443
Fig. 7.8.24. Fascioliasis. A heterogeneous mass (arrowheads)

with cystic and solid components is seen in the right lower
quadrant near the terminal ileum and ascending colon, along
with diffuse infiltration (arrowheads) in the regional fat plane
and omenturn
similar CT features can be produced by the peritoneal involvement of other parasitic infestations such
as sparganosis and fascioliasis (Fig. 7.8.24) (RHA et
al. 1999).
7.8.3.5
Schistosomiasis Japonica
Schistosomiasis japonica is confined to eastern Asia.

Patients are infected by contact with fresh water that
is infested with larvae. The schistosomallarvae penetrate the skin and pass via the systemic circulation
to the portal vein and its tributaries. The eggs are
the chief cause of tissue darnage to the host. An
intense granulomatous reaction is followed by irregular mucosal thickening, formation of granulomataus polyps, and eventually fibrosis. CT characteristically shows curvilinear or nodular calcification in the
colon, appendix, rectum, or small bowel (Fig. 7.8.25)
(LEE et al. 1994; ARAKI et al. 1989). The calcified eggs
are deposited more extensively in the submucosa and
subserosa (LEE et al. 1994).
7.8.3.6
Cryptosporidiosis
Cryptosporidium, a protozoan parasite of the dass

Sporozoa, has been recognized as an inhabitant
of the gastrointestinal tract in numerous animals
including man. Recently, this infestation has been
an important cause of a severe opportunistic infection in patients with disordered immunoregulation
Fig. 7.8.25. Schistosomiasis japonica. CT scan shows diffuse

colonic wall calcification (arrows) in the rectum and sigmoid
colon. (Courtesy of T Araki, MD, Yamanashi University,
associated with AIDS (CENTER FOR DISEASE CoNTROL 1982), but it is also reported to occur in immunologically normal patients (TZIPORI 1983). The
disease can be transmitted to man from vertebrate
animals, but evidence for person-to person transmission, especially during sexual practices, is rapidly increasing (CURRENT et al. 1983). Cryptosporidium attaches to the brush border of the intestinal epithelial cell on electron microscopy (BABB
et al. 1982) and causes enterocolitis in various
animal species. Histologie examination of intestinal biopsies shows partial villous atrophy, lengthened crypts, and cellular infiltration of the lamina
propria of the jejunum and ileum (MA and SoA VE
1983}. Cryptosporidiosis in immunocompetent persons may produce a self-limited, flu-like, gastro-
H. K. Ha
444
intestinal illness. However, the clinical course in

immunocompromised patients contrasts with the
prolonged severe diarrhea (CURRENT et al. 1983),
becoming a cause of morbidity and death in AIDS
patients. The most reliable method for diagnosis
is intestinal biopsy. However, the presence of an
oocyst can also be demonstrated in fecal samples.
The radiographic features of the small intestine in
patients with AIDS include nonspecific mucosal fold
thickening predominantly at the duoden um and jejunum (BERK et al. 1984). Mild hypersecretion and dilatation may be present. These features simulate those
of giardiasis, Strongyloides, Isospora, and cytomegalovirus. Nonspecific bowel wall thickening can be
seenon CT (MEYERS et al. 1990).
and fold thickening of the duodenum and jejunum

(MEDINA et al. 1992). With progression of the infestation, the involved small-bowel segments may show
marked hypotonia and rigidity. In the most cases,
the small-bowellumen is narrowed, and the mucosal folds are flattened or effaced, producing the dassie pipestem or ribbon bowel appearance (MEDINA
et al. 1992). The differential diagnosis of this appearance on barium study may include sprue, Iymphoma,
Crohn's disease, secondary malignancy, and ischemic
or radiation enteritis. Another parasitic disease, isosporiasis caused by Isospora belli, is also reported to
show radiographic features very similar to strongyloidiasis (HIZAWA et al. 1998).
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7

Diseases of the Smalllntestine

Radiology of Acute and Chronic Small-lntestinallschemia

diagnosis is being made more frequently, due to an

N. C. Gourtsoyiannis (ed.), Radiological Imaging of the Small Intestine

IMA. The IMA branehes into the left eolie artery,

whieh supplies the distal transverse and deseending

The degree and duration of the isehemia, in addition

Forms of Mesenteric lschemia

Fig. 7.1.2. Thickened folds with pinkyprinting. Supine view of

extensive small-bowel and right colanie ischemia,

Fig. 7.1.4. Pseudo-obstruction pattern. Supine view of the

Fig. 7.1.6. Air in the portal venous system. Branching lucencies

On plain films, portal venous gas typically appears

25%-40% of cases in several series (ALPERN et al.

rhe role of er in the diagnosis of AMI is still evolving.

Scanning should be performed using a helical scanner,

should be administered at a rate of between 3 and 5

The CT findings will vary with the extent of bowel

in ischemia on CT (Fig. 7.1.7) (FEDERLE et al. 1984;

rable 7.1.2. er findings in acute mesenteric ischemia

the ability to demonstrate the bowel wall en face or

Fig. 7.1.10. Pneumatosis. CT scan at the Ievel of the pelvis using

Portal venous gas is also more easily identified on

Fig. 7.1.12. Portal venous gas; small amount. CT scan through

20o/o of SMA emboli lodge at the origin of the vessel,

Fig. 7.1.13. Mesenteric venous gas. CT scan at the Ievel of the

Fig. 7.1.14. Engorgement of mesenteric veins. CT scan at the

Fig. 7.1.17. Aeute clot in SMA on noneoutrast CT examination

Fig. 7.1.18. SMV thrombosis. Contrast-enhaneed CT sean

tified in peripheral branches of the IMV (KIM et

Fig. 7.1.19. Lack ofbowel wall enhancement. Contrast-enhanced

Fig. 7.1.20. Target sign. Contrast-enhanced CT scan at the Ievel

of thickened loops of bowel has also been described,

Fig. 7.1.21. Portal venous gas on ultrasound. Bright echoes due

Angiography has been considered the 'gold standard'

1992). With this approach, the survival rate has been

Barium sturlies correlate with the plain film and er

MR is being increasingly used for the evaluation

and LI 1998; SHIRKHODA et al. 1998). Both anatomic

Treatment of Acute Mesenteric lschemia

Fig. 7.1.25. Thickened folds due to submucosal edema and/or

The treatment of AMI will in part be determined by the

Focal Mesenteric lschemia

Fig. 7.1.26. Effacement of the mucosal pattern. Small-bowel

Focal segmental ischemia is due to vascular insults to

ening situation found with more extensive ischemia

to be fairly sensitive in identifying ischemia using the

Fig. 7.1.27. Focal ischemia with stricture. Small-bowel series

Vaseulitis can affect blood vessels of all sizes. Large

Chronic Mesenteric lschemia

Fig. 7.1.28. Chronic stage radiation enteritis. Small-bowel

meet the metabolic requirements of increased oxygen

10o/o-24o/o of the population (LINDNER and KEMPRUD

Fig. 7.1.29. Celiac axis compression syndrome. Lateral view

panereatie eollateral vessels and poststenotie dilatation

The terms vascular ectasia and angiodysplasia are

Portal hypertension causes portosystemic venous

Mindelzun RE, Beaulieu CF ( 1997) Using biphasic CT to reveal

7.2 Radiology of Small-lntestinal Obstruction

F. TAOUREL, F.M. BLAYAC

Small-bowel obstruction (SBO) is responsible for

The clinical diagnosis of SBO classically depends