Tuberculosis: Frequency of Unusual Radiographic Findings

WALLACE T. MILLER1 AND ROB ROY MacGREGOR2

The changing pattern of the radlologic presentation of are even more likely to overlook the unusual ones.
tuberculosis was noted in a review of 100 consecutive cases Tuberculosis in the adult is more likely to be associated
of pulmonary tuberculosis. Active tuberculosis was not sug- with an unusual radiographic pattern than in the past [4],
gested as a radiologlc diagnosis in 43% of the patients. Of the taking the initial thrust of the diagnosis in a direction
100 cases, only 66 had characteristics of reactivation tuber-
other than tuberculosis. The continuing need for the
culosis (i.e., minimal upper lobe infiftrate or more advanced
proper diagnosis of tuberculosis and especially the
cavitary disease). Of the other 34 patients, 18 had less usual
presentations, making the radiographic diagnosis difficuft.
changing pattern of its radiographic manifestations led
The remaining 16 patients had radiographic pafterns quite un- to this review.
usual for tuberculosis, including masslike densities resem-
Subjects and Methods
bllng carcinoma; chronic infiltrates in a lower lobe; miliary
tuberculosis, either superimposed on diffuse interstitial lung We reviewed 100 consecutive cases of culture-proven pul-
disease or associated with a diffuse lung pattern atypical for monary tuberculosis seen in a 4 year period (1971-1975) at the
miliary disease; and normal chest radiograph. Hospital of the University of Pennsylvania. Criteria for inclusion
were availability of both hospital chart and radiographs and at
Introduction least one positive culture for Mycobacterium tubercu!osis. 5ev-
eral cases of nonpulmonary tuberculosis with negative sputum
Tuberculosis is responsible for considerable morbidity cultures for M. tuberculosis were not included. Two cases of
and mortality in all areas of the world. Careful public scrofula with mediastinal adenopathy, one case of hip tubercu-
health measures and the advent of chemotherapy have losis with positive chest film and sputum culture, and one case
dramatically decreased the incidence of this disease in of meningitis with miliary pulmonary tuberculosis are included.
medically advanced countries. Nonetheless, tuberculo- In this 4 year period, the nonpulmonary tuberculosis cases
sis still exists in such countries, particularly in large encountered were: meningitis, four cases; genitourinary, five
urban populations. There seems to be an increasing (two bladder, three kidney); scrofula, eight; and bone and joint,
two (one spine, one hip).
frequency of misdiagnosis of tuberculosis, possibly due
Of the 100 cases with proven pulmonary tuberculosis, 55
to its decreasing incidence in proportion to other pul-
were men and 45 women; age range was 19-78 years (average
monary disease. for men, 59; for women, 49.6). Blacks constituted 59% of the
In 1953, when national data first became available, the study group; in this hospital population, they represent 42% of
new active tuberculosis rate in the United States was the admissions.
53.0 per 100,000 population. In 1975, this same new Most of the 100 patients in this study were over 40 years of
active case rate was only 15.9 per 100,000 population [1]. age, consistent with the national shift in the incidence of active
A more sensitive index to the decreasing prevalence of pulmonary tuberculosis from predominantly young adults to
tuberculosis in the population is the tuberculin skin test older persons [1 , 5, 6]. Andvord [7] and Frost [8] suggested that
reactivity. In Philadelphia, 16.4% of teenagers had a this shift in the incidence of secondary tuberculosis is a function
of the prevalence of infection during the patients’ youth. Since
positive skin test in 1948, while only 1 .4% were positive
public health measures and chemotherapy have greatly reduced
in 1968 [2].
the incidence of infection in children in the past 35 years, the
Of the new cases of tuberculosis in Philadelphia in greatest numbers of dormant tuberculous foci are in the older
1971 65% were diagnosed
, by nontuberculosis hospitals population.
(55.2%) or private physicians (9.8%) [3]. This demon- Diagnosis in all instances was made by positive culture or
strates the dramatic shift in the care of the tuberculous biopsy. All patients with pulmonary tuberculosis and two of the
patient from the tuberculosis sanatorium to the commu- patients with miliary disease had positive sputum culture. Diag-
nity hospital. In this setting, misdiagnosis of the disease nosis of pulmonary tuberculosis was made by surgical removal

is much more likely to occur [4] for several reasons. The of a pulmonary tuberculoma in two patients: sputum from one
tuberculosis patient is now usually diagnosed and subsequently grew M. tuberculosis. One case of lower lobe
tuberculosis and two cases of miliary tuberculosis were diag-
treated by physicians who do not have a primary interest
nosed by lung biopsy. All cases of tuberculosis adenitis were
in this disease, or even a special interest in pulmonary
diagnosed by biopsy. One case of disseminated tuberculosis
medicine or infectious disease. The recent decreased had positive cultures from the meninges and lung: another had
incidence of tuberculosis has created a group of physi- positive cultures from pleura, lung, and abdominal nodes. Five
cians with little experience in this disease. They may fail patients with mass lesions had tuberculosis in the resected
to recognize the usual manifestations of the disease and specimen with subsequent positive culture from the specimen.

Received August 3, 1977; accepted after revision January 30, 1978.

Presented at the annual meeting of the American Roentgen Ray Society, Boston, September 1977.
‘ Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia. Pennsylvania 19104. Address reprint
requests to W. T. Miller.
a Department of Medicine, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania 19104.

Am J Ro#{149}ntg.nol 130:867-875, May 1978 867 0361 -803X/78/0500-0867 $02.00

© 1978 American Roentgen Ray Society
868 MILLER AND MacGREGOR

TABLE 1

Clinical History

Positive
No. _______________
Symptom .
Questioned
No. I,

Cough 78 62 79
Anorexia, weight loss 76 58 76 .

Fever 75 34 45
Sweats, chills 72 43 60
Fatigue, malaise 63 35 56
Hemoptysis 68 17 25 4
Exposedtotuberculosis 60 13 22
Active tuberculosis in past
Past skin test performed
46
354:
7t
9
15
26
4
.;!.
. Average weight loss. 10 kg.
t An additional four may have had active tuberculosis.
Skin test had been performed on 27 of the 35 questioned.

TABLE 2

Physical Findings on Admission

Positive
No.
Sign
Recorded
No.

Fever 100 15 15
Wasting 83 29 35
Pulmonary rales 88 25 28
Dullness 88 24 27
Fig. 1.-Far advanced tuberculosis in 72-year-old black male with
Adenopathy 12 9 75
fever, hemoptysis, and 18 kg weight loss. Extensive cavitary disease in
Hepatomegaly 85 17 20
left lung with bronchogenic spread to right.
Splenomegaly 84 5 56
. Over 37.8Cc.

TABLE 3

Chest Radiography

Finding
Patients

Usual reactivation tuberculosis:

Extensive, obvious tuberculosis 37
Minimal tuberculosis:
Described as “old” 12
Described as “active” 19
Less usual tuberculosis:
Primary tuberculosis:
Pleural effusion:
Acute 3
Chronic 4
Mediastinal or hilar adenopathy 4
Miliary infiltrates 4
Nodules 3
Pneumothorax 2
Unusual tuberculosis:
Completely clear 3
Masslike density called carcinoma: Fig. 2.-Minimal tuberculosis in 38-year-old female with chronic
Usual location for tuberculosis cough. Prominent infiltrate in right upper lobe. Diagnosis of this type of
2
tuberculosis is generally no problem.
Unusual location for tuberculosis 5
Chronic infiltrate, unusual location for tuberculosis 4
Miliary tuberculosis superimposed upon diffuse in- pulmonary signs and only 35% had a temperature above 37.8CC
terstitial lung disease 1 at any point during hospitalization.
Miliary tuberculosis, atypical pattern 2
Radiographic Findings
The results of chest radiography are listed in table 3.
Symptomatology is shown in table 1 . Cough and weight loss Far Advanced Tuberculosis
were common, seen in more than 75% of all the patients. Fever
was present in less than 50% and hemoptysis in 25% of the There were 37 patients with extensive cavitary tubercu-
patients. Physical findings on admission usually were not help- losis, unilateral or bilateral (fig. 1). These cases are gen-
ful (table 2). Less than one-third of the patients had abnormal erally not a diagnostic problem in a large urban hospital
 UNUSUAL PATTERNS OF TUBERCULOSIS 869

Fig. 3.-Chronic pleural tuberculosis with radiographically stable pulmonary infiltrate in 45-year-old black male with 2.3 kg weight loss and night
sweats. No apparent change in chest films 6 years apart. Three sputum cultures were positive for M. tuberculosis. Despite unchanging character of
loculated pleural collection, fluid was present in pleural space and pleural biopsy was positive.

where tuberculosis is seen frequently. Nonetheless, in Primary Tuberculosis

several instances, the diagnosis of tuberculosis was not
suggested. In retrospect, many of these cases were Although primary tuberculosis has long been con-
rather obvious far advanced tuberculosis. Misdiagnosis sidered a disease of childhood, this is no longer an
of this type of disease occurred most commonly in accurate concept in the United States [4, 10-12]. Only a
patients who were quite ill and often admitted to the small percentage of patients have a positive skin test as
intensive care unit. The extensive infiltration was thought adults, indicating that they are susceptible to the de-
to represent aspiration pneumonia or lung abscess. Two velopment of the primary disease process. The hallmark
of these patients died from respiratory failure, presum- of primary tuberculosis is hilar or mediastinal
ably secondary to their far advanced disease. adenopathy or pleural effusion (10 patients, figs. 4-7).
Many of the cases of lower lobe infiltration or masslike
Minimal Tuberculosis
densities, which are considered unusual characteristics
Nineteen patients were correctly diagnosed as having of tuberculosis, may also represent primary tuberculosis.
minimal active tuberculosis (fig. 2). However, 12 patients If these cases are included, then a full 19% of our cases
who were thought to have old or stable tuberculosis represent primary tuberculosis. In a recent report em-
subsequently proved to have active disease. These pa- phasizing the unusual radiographic appearance of the
tients were identified through a tuberculin skin test and disease, Kahn et al. [4] found that 13.5% of their patients
one or more sputum specimens. These cases illustrate a had primary tuberculosis.
very important point in the radiographic reporting of Adenopathy. Four cases had mediastinal and hilar
apical scarring. Without films dating back at least 6 adenopathy, two bilateral and two unilateral. One patient
months, an accurate statement regarding the stability of also had a pulmonary infiltrate and pleural effusion, and
a tuberculous lesion cannot be made: all of these lesions tuberculosis was suspected. The other three cases were
should be reported as ‘tuberculosis, ‘ activity indetermi- diagnosed as sarcoidosis. One of these patients (fig. 5)
nate.” Even in patients with unchanging radiographic subsequently developed a pneumonialike infiltrate in the
tuberculous scars, active tuberculous infection can still right lower lobe which did not clear on antibiotic therapy.
be present on sputum culture. Consequently, these pa- Diagnosis was made by mediastinal biopsy in two pa-
tients should be reported as radiographically ‘ ‘ stable” tients and by sputum smear in the other two.
rather than “inactive” [9]. Three cases in this series had Sarcoidosis is a common disease usually associated
positive cultures for M. tuberculosis despite radio- with mediastinal adenopathy. However, tuberculosis may
graphically stable lesions (fig. 3). show a similar pattern [12]. Tuberculosis should be
 870 MILLER AND MacGREGOR

Fig. 4.-Mediastinal adenopathy in 38-year-old black male with 6.8 kg Fig. 6.-Pleural tuberculosis in 26-year-old black male heroin addict
weight loss. Original diagnosis was sarcoid, but mediastinal node biopsy with fever and 6.8 kg weight loss. Pleural biopsy and culture from left
and cultures were positive for tuberculosis. pleural effusion were positive for M. tuberculosis.

_‘i’ 1

.‘

II ...

Fig. 5.-Mediastinal adenopathy and right lower lobe infiltrate in 24- Fig. 7. - Pleural tuberculosis with bronchopleural fistula in 62-year-old
year-old black female with uveitis. Initially. patient had only mediastinal black male. Long-standing fibrothorax on left with extensive pleural
adenopathy but developed right lower lobe infiltrate 3 weeks later. thickening and pleural calcification. Air-fluid level (arrow) developed at
Sarcoidosis was thought to be likely diagnosis. After pulmonary infiltrate left base 1 year after his last film. Pleural biopsy and culture revealed
appeared, sputum became positive for M. tuberculosis. M. tuberculosis.

suspected when the adenopathy involves only one hilum. adenopathy as well as cervical adenitis. Six additional
All diagnoses of sarcoid should be confirmed by biopsy patients had cervical adenitis only diagnosed by lymph
to show that noncaseating rather than caseating node biopsy; sputum cultures were negative for M.
granulomata are present: culture of the surgical speci- tuberculosis. Therefore, these six cases are not included
men is also important, since not all tuberculous nodes in this review, although some may represent primary
will show caseation. tuberculosis.
Two other patients had coexisting mediastinal Pleural Effusion. Seven cases in this study had unilat-
 UNUSUAL PATTERNS OF TUBERCULOSIS 871

Fig. 8.-Miliary tuberculosis in 64-year-old female Fig. 9.-Miliary tuberculosis in 72-year-old male with cardiac and
with cough, low grade fever, and 4.5 kg weight loss. At pulmonary failure. Patient had prior interstitial lung disease and was felt
this stage, miliary tuberculosis is relatively easy to to have pneumonia and/or pulmonary edema. Autopsy revealed miliary
recognize. tuberculosis.

eral pleural effusion (figs. 6 and 7), including five cases diagnosed by lung biopsy (two cases) or autopsy (one
in which it was the only radiographic finding. Pleural case). The diagnosis was quite difficult because of the
effusion is generally considered to be a manifestation of underlying preexisting lung disease. In each case, there
primary tuberculosis [4, 10, 13, 14]. However, two of our was a change in the sequential chest film to a miliary
patients with pleural effusion had a long-standing history pattern which could be identified in retrospect as conSis-
of pleural disease with Ioculated effusions that were tent with miliary tuberculosis.
stable for years and thought to represent old pleural The radiographs in one of these patients improved
thickening. One of these patients subsequently de- somewhat after therapy for tuberculosis but did not
veloped pulmonary infiltration and one a bronchopleural revert completely to normal. The other two patients
fistula. Both had M. tuberculosis cultured from loculated expired from miliary tuberculosis. These three cases
pleural collection. Thus, although we have included all emphasize the importance of suspecting miliary tuber-
cases of pleural effusion as primary tuberculosis, it is culosis in chronically ill patients. The radiographic ap-
likely that some cases, especially if loculated and long pearance of early miliary tuberculosis may be overlooked
standing, represent secondary disease. unless searched for carefully. Conversely, the patient
with very extensive miliary tuberculosis may show such
Miliary Tuberculosis
an unusual lung pattern (fig. 9) that miliary tuberculosis
Seven patients had miliary tuberculosis (figs. 8 and 9). is not suspected. One patient with miliary tuberculosis in
One patient, admitted with the diagnosis of schizo- this series was on immunosuppressive drugs, and this
phrenia, was found to have meningeal tuberculosis. The type of disease must be suspected in such patients.
chest film was originally interpreted as normal but in
retrospect showed multiple miliary nodules. In two other Pneumo thorax
cases, miliary tuberculosis was strongly suspected. In a
fourth case, tuberculosis was considered but thought to One patient had a pneumothorax and unsuspected
be less likely than hypersensitivity lung disease. Tuber- tuberculosis (fig. 10). A second patient had a
culosis was subsequently proven in all four cases and all pneumothorax associated with far advanced tuber-
cases responded to drug therapy. culosis. Tuberculosis is a known albeit unusual etiology
Three patients had a rather unusual radiologic pattern of pneumothorax. On films after reexpansion of a
for miliary tuberculosis. All three had initial respiratory pneumothorax, an apical infiltrate should be searched
failure and extensive diffuse interstitial lung disease for for carefully. Such an infiltrate was identified in the one
several weeks to several months. These were compli- case with unsuspected tuberculosis, but was incorrectly
cated by superimposed miliary tuberculosis which was interpreted as an ‘ ‘old scar.’ ‘ Again the necessity of
872 MILLER AND MacGREGOR

Fig. 10.-Pneumothorax and apical infiltrate in 69-year-old male with

pneumothorax (A). On reexpansion, infiltrate noted in right upper lobe
(B) was considered old tuberculous scar. Patient subsequently expired;
active tuberculosis was cultured from right apical lesion.

segment of an upper lobe. Other patients had nodules in

the upper lobe, but since tuberculosis was already con-
sidered, these were not thought to be diagnostic prob-
ems. Other authors [4, 15] have reported multiple
nodules as diagnostic problems in that they suggest
metastatic tumor. No such cases were encountered in
this review, although some have been seen previously at
this institution.
A solitary nodule requires pathologic identification;
consequently, diagnosis was made in two patients after
surgical removal of the nodule (fig. 11). In the third,
diagnosis was made by a positive smear; treatment with
antituberculous drugs resulted in disappearance of the
nodule.

Masslike Densities

Seven patients had masslike densities (fig. 12) which

were felt to most likely represent carcinoma of the lung.
Five of these were in locations unusual for tuberculosis:
one each in the anterior segment of the upper lobe,
lingula, and middle lobe, and two in the lower lobe.
These five lesions may represent another manifestation
of primary tuberculosis. Two lesions were in the pos-
tenor segment of an upper lobe. Tuberculosis should not
Fig. 11.-Tuberculous nodule in asymptomatic 30-
be suggested for every mass lesion of the chest. How-
year-old female. Nodule in superior segment of right ever, this possibility must be considered in patients with
lower lobe was diagnosed as tuberculosis at surgery. benign pulmonary cytology.

reporting any apical lesion as one of indeterminate Basilar Infiltrates

activity is emphasized.
Four patients had chronic infiltrates in a lower lobe
Tuberculoma representing basilar tuberculosis (fig. 13). These infil-
Three patients had solitary nodules, two in the superior trates were generally thought to represent chronic in-
segment of the lower lobe and one in the anterior flammatory disease or a poorly responsive pneumonia;
 UNUSUAL PATTERNS OF TUBERCULOSIS 873

tuberculosis was not suspected in any case. Diagnosis

was made in one patient by thoracotomy and in the other
three by positive smear and culture. These patients may
also represent primary tuberculosis, although reactiva-
tion tuberculosis may occasionally involve the lower
lobe.
Normal Chest Film

Three patients with positive sputum cultures for M.

tuberculosis had a normal chest film, even in retrospect.
One of these patients had coexisting tuberculosis in a
transplanted
drugs.
and sputum
positive
The other
kidney

cultures
and was on immunosuppressive
two patients had unexplained
for M. tuberculosis
after they left the hospital.
which
These patients
fevers
became
could
-1
conceivably represent primary tuberculosis with a very
minute focus of infection, or they may represent reactiva-
tion tuberculosis with subradiographic pulmonary le- it

sions. Miliary tuberculosis is also a consideration, but

none of the patients subsequently developed diffuse
infiltrates or systemic symptoms of miliary disease.
These three cases illustrate a point in the course of
pulmonary tuberculosis when a radiographically visible Fig. 12.-Masslike density in asymptomatic 79-year-old male. Right
lesion is not yet present and yet the patient has a positive lower lobe mass was diagnosed as tuberculosis at surgery.

culture [16]. There certainly is no way that tuberculosis

can be suspected in this instance.
Radiographic Reports

In reviewing the original radiographic reports issued

on the 100 patients, we found that a positive diagnosis of
active tuberculosis was made in 50 cases. Tuberculosis
was mentioned as a possibility but not a primary diag-
nosis in seven patients. A diagnosis of old tuberculosis
or apical tuberculous scarring was made in 14 patients.
Tuberculosis was not mentioned as a diagnostic possibil-
ity in 29 patients. Of these, three had a normal chest
radiograph, even in retrospect. Thus in 26% of the cases,
the diagnosis of pulmonary tuberculosis was not
suggested by the radiologist in the face of chest radio-
graphic findings which subsequently proved to be tuber-
culosis.
The failure of the radiologist to alert the clinician to the
possibility of pulmonary tuberculosis frequently led to
long delays in the institution of therapy in many of the
patients in this report. Tuberculosis was not suspected
initially by the clinician in 42% of our cases; 20% actually
were discharged from the hospital without any antituber-
culous therapy, since the cultures did not become posi-
tive until after discharge. One patient was told that he
had inoperable carcinoma of the lung; when his cultures
grew M. tuberculosis several weeks later, he was located Fig. 13.-Lower lobe infiltrate in 32-year-old female. Smears and
cultures of chronic right lower lobe infiltrate were positive for M.
in Italy where he was making a “last pilgrimage” before
tuberculosis.
his “impending death.”
In some cases, the cause of the delay could not be
attributed to the radiologist. In several instances. a Discussion
correct diagnosis of active or possibly active tuber-
culosis was suggested by the radiologist but ignored by Concepts of the pathogenesis of ‘‘secondary tubercu-
the referring physician. To prevent this, a mechanism losis” have changed during the past 15 years. Until
has been instituted in our hospital to follow all patients in recently, many believed that secondary tuberculosis re-
whom tuberculosis is suggested on the radiographic suIted from reinfection of a person previously sensitized
report. to tubercle bacillus. This implied a second contact with
874 MILLER AND MacGREGOR

tuberculosis as an adult. Current concepts of the patho- disease becomes more extensive, other pulmonary seg-
genesis of tuberculosis, as elaborated by Stead and ments may subsequently become involved. The early
colleagues [17, 18], are as follows. The primary tubercu- lesion of reactivation tuberculosis is usually a fluffy or
bus lesion nearly always occurs in the well ventilated strandlike infiltrate in an apical portion of the lung,
(lower) portions of the lung. After implantation, the possibly accompanied by pleural thickening.
tubercle bacillus grows and multiplies with little or no As the disease becomes more extensive, cavitation
immediate tissue response. Eventually, a few bacilli frequently develops in the lesion and there is endobron-
reach the circulation through pulmonary veins and lym- chial spread to other areas of the lung, often to the
phatic channels and are widely disseminated. The bacilli superior segment of the contralateral lung. More exten-
implant and multiply in organs with a milieu favorable sive far-advanced tuberculosis is almost invariably ac-
for growth, usually in an area of high oxygen tension. companied by cavitation, although tomography may be
This implantation occurs most commonly in the apices necessary to demonstrate this.
of the lungs, and more rarely in the kidneys, brain, or While these are the accepted radiographic findings in
bone. Lymphatic drainage into the mediastinum also tuberculosis, this study suggests that there are other,
results in tuberculous growth in lymph nodes, and rup- somewhat unusual, manifestations of tuberculosis which
ture of a small tuberculous focus into the pleura may must be considered in the diagnosis of this disease. As
result in a pleural effusion. tuberculosis becomes less common, the radiologist and
The 4-6 week interval between development of the the clinician must remain aware of its existence, partic-
primary and secondary lesions results from the time ularly in the urban population. They also should be
required for the host to develop specific cell mediated aware of the increasing frequency of a radiographic
immunity (delayed hypersensitivity). During this phase, appearance of the disease not generally described in the
organisms disseminate from the primary focus of infec- textbooks.
tion to other susceptible parts of the body. When cell-
mediated immunity develops, these sites attract infiam-
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