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Radiotherapy and Oncology 92 (2009) 22–33

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Radiotherapy and Oncology


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Educational review

Anatomical bases for the radiological delineation of lymph node areas.


Part III: Pelvis and lower limbs
Benoit Lengelé a,*, Pierre Scalliet b
a
Departments of Surgery and Experimental Morphology, Université Catholique de Louvain, Brussels, Belgium
b
Department of Radiation Oncology, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Brussels, Belgium

a r t i c l e i n f o a b s t r a c t

Article history: Cancer spreads locally through direct infiltration into soft tissues, or at a distance by invading vascular
Received 25 September 2008 structures, then migrating through the lymphatic or blood flow. Although cancer cells carried in the blood
Accepted 4 November 2008 can end in virtually any corner of the body, lymphatic migration is usually stepwise, through successive
Available online 16 December 2008
nodal stops, which can temporarily delay further progression. In radiotherapy, irradiation of lymphatic
paths relevant to the localization of the primary has been common practice for decades. Similarly, exci-
Keywords: sion of cancer is often completed by lymphatic dissection.
Lymphatics
Both in radiotherapy and in surgery, advanced knowledge of the lymphatic pathways relevant to any
Pelvic cancer
Lower limb tumors
tumor location is an important information for treatment preparation and execution. The third part of these
Radiotherapy series describes the lymphatics of the pelvis and the lower limb. It Provides anatomical bases for the radio-
CTV logical delineation of lymph nodes areas in the pelvic cavity and in the groin. It also offers the first original
classification for labeling the intrapelvic nodes, grouped in seven paired volumes (called levels I–VII), func-
tionally linked with one another and lower abdominal levels by eight potential drainage pathways.
Ó 2008 Elsevier Ireland Ltd. All rights reserved. Radiotherapy and Oncology 92 (2009) 22–33

The third and last part of these series dedicated to the descrip- The present work is not only an atlas, but also a fine description
tion of updated anatomical bases for delineation of target lymph of lymphatic vessels and nodal stations relevant to the various
node areas in conformal radiotherapy [9–10] discusses the lym- abdominal and pelvic organs. It offers a grouping in functional
phatic drainage of the pelvis and lower limbs. It is of particular levels, common to malignancies arising from a given anatomical
relevance to radiation oncology as about 2/3 of all cancers are region, not unlike the node levels currently in use for head and
localized in the lower abdomen and the pelvis (colo-rectal, pros- neck cancer radiotherapy planning [5]. Furthermore, it helps to
tate and gynaecologic). All these represent important indications better understand the relationship between upper and lower
for radiotherapy, and constitute a challenge regarding normal tis- abdominal lymphatics (see also Part II in [10]). It also clearly indi-
sue (specifically small bowel) tolerance. As in other parts of the cates secondary routes of lymphatic spread, particularly relevant to
body, unambiguous delineation guidelines are desirable, together some specific tumor locations (fundus uteri [14], bladder neck,
with a clear understanding of the dynamics of lymphatic anterior prostate, lower rectum [4]) and to cases with a major
drainage. nodal invasion (f.i. pararectal adenopathies in cervix [7], or pros-
The need for clear guidelines has prompted a series of tate cancer [6,7]).
publications dealing with the lymphatic vessels of the pelvis
[12,16–18,22], as the practice has repeatedly demonstrated in-
ter-observer discrepancies in nodal CTV delineation [11,24,26]. Lymphatics of the pelvis
This reflects the slow learning curve of radiation oncologists,
previously used to define irradiated volumes by external bony Divided into parietal and visceral networks of lymph vessels
landmarks, inaccurate as far as nodal CTV is concerned [1], even and nodes, all the lymphatics of the pelvis drain into successive
if lymphangiograms have helped in the past to shape the relevant groups of nodes located at the level of the pelvic inlet, along the
volumes [3]. arcuate line of the coxal bone and in front of the fifth lumbar ver-
tebra. Mostly associated with the iliac vessels and their branches,
they form several ascending chains which include the external
iliac, internal iliac, common iliac and sacral groups of nodes. Final-
* Corresponding author. Address: Department Experimental Morphology,
Université Catholique de Louvain, Tour Vésale 5251, Avenue E. Mounier, 52, B-
ly, their collecting ducts terminate in the inferior part of the lateral
1200 Bruxelles, Belgium. aortic chain on the corresponding side (Fig. 1, see also Fig. 4 in
E-mail address: benoit.lengele@uclouvain.be (B. Lengelé). [10]).

0167-8140/$ - see front matter Ó 2008 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.radonc.2008.11.007
B. Lengelé, P. Scalliet / Radiotherapy and Oncology 92 (2009) 22–33 23

Fig. 1. Lymphatic node groups and drainage pathways of the pelvis. Medial view of the right female hemipelvis showing the distribution of the pelvic lymph node groups and
their eight connecting pathways, identified by different colors. Abbreviations: DiE: deep inferior epigastric n., G: gonadic n., iCi: intermediate common iliac n., iEi: intermediate
lateral iliac n., iG: inferior gluteal n., ii: interiliac n., Ii: internal iliac n., iM: inferior mesenteric n., IP: internal pudendal n., L: lacunar n., LCi: lateral common iliac n., LEi:
lateroexternal iliac n., LPA: lumbar periaortic n., LS: lateral sacral n., LV: laterovesical n., mCi: medial common iliac n., mEi: medial external iliac n., mR: middle rectal n., MS:
median sacral n., O: obturator n. (Cruveilhier’s), Pm: promontory n., pR: pararectal n., pU: parauterine n., pv: paravaginal n., PV: prevenous n., pV: prevesical n., rV:
retrovesical n., sA: suboartic n., sG: superior gluteal n., SI: superficial inguinal n., SV: subvenous n., sV: subvesical n. Note that the surgical obturator node (*) differs from the
true anatomical obturator node. The major lymphatic pathways of the pelvis are identified as the external iliac (EiP), internal iliac (iiP) and presacral (PSP) pathways and
converge in a common iliac pathway (CIP), ending in the lateral lumbar periaortic nodes. Alternative routes follow the internal pudendal (IPaP), gonadic (GaP), inferior
mesenteric (iMaP) and superficial perineal accessory (SPaP) pathways. The existence of an inguinal accessory pathway (iaP) seems also possible.
24 Delineation of pelvic lymph node areas

Parietal lymph vessels and nodes ascending drainage pathways, all converging towards the lateral
groups of lumbar aortic nodes (Fig. 1).
The parietal lymphatics collect the lymph from the anterior, lat-
eral, posterior and inferior walls of the pelvis and include superfi- Juxtavisceral nodes
cial and deep networks that drain the integuments of the perineum According to their respective locations, the juxtavisceral nodes
and the muscles covering the pelvic girdle, respectively [2,20,25]. are distinguished as follows [27]:
The superficial parietal vessels are only present on the pelvic
floor. Running under the perineal skin from the coccygeal area to-  Pre-, lateral-, post- and subvesical lymph nodes are located on the
wards the pubis, they cross anteriorly the medial side of the root of corresponding surfaces of the bladder, in the urinary compart-
the thigh around the outer surface of the adductor muscles, and ment of the pelvis.
then join the superomedial group of superficial inguinal nodes.  Paravaginal and parauterine lymph nodes are found, respectively,
Their functional territory comprises all the soft tissues of the per- on the lateral edges of the vagina and the cervix, and occupy the
ineum below the outer fascial sheath of the urogenital diaphragm, parametrial fibrous tissue of the genital compartment of the
but also the distal part of the vagina below the hymen and the infe- female pelvis.
rior part of the anal canal below the ano-cutaneous line [15].  Pararectal lymph nodes are ranged around the right and left
The deep parietal vessels follow the parietal branches of the aspects of the rectum, in the posterior digestive pelvic
external and internal iliac vessels, and thereby make their first re- compartment.
lay into the inferior epigastric, circumflex iliac and sacral groups of
nodes [25]: Afferent vessels to these nodes arise directly from the neighbor-
ing viscera, while the respective routes of the efferent vessels ex-
 The deep inferior epigastric nodes consist of three to six small tend to the external iliac, internal iliac or presacral chains [19].
nodes situated over the lower third of the course of the corre-
sponding artery, behind and along the lateral border of the rec- External iliac nodes
tus abdominis muscle. These nodes may sometimes be absent, Grouped around the external iliac vessels, the external iliac
but when present, they mostly drain the lower part of the ante- nodes are usually nine to ten in number and have a constant
rior abdominal wall but also the retropubic part of the anterior arrangement, forming three distinct chains each consisting of
pelvic wall. Their efferent vessels terminate in the lateral chains about three nodes: the lateral, middle and medial groups of exter-
of external iliac nodes. nal iliac nodes (Fig. 1).
 The deep circumflex iliac nodes are two to four in number but are
frequently absent. Located around the artery which bears the  The lateral chain comprises three nodes which are interposed
same name, they receive afferent vessels arising from the iliac between the medial border of the psoas and the lateral side of
muscle and the parietal peritoneal lining of the iliac fossa. Their the external iliac artery. The lower node is located under the
efferent vessels then extend to the external iliac nodes. inguinal ligament, frequently passes through the femoral sep-
 The sacral groups of nodes are located around the lateral and tum, and is known as the lateral lacunar lymph node [27]. Clo-
median sacral arteries, and constitute three ascending chains sely related to the origin of the deep inferior epigastric and
running, respectively, along the lateral borders of the sacrum deep circumflex iliac arteries, it receives the efferent vessels
and in front of its anterior aspect on the midline. Draining the from the corresponding groups of nodes [19,23].
presacral space between the fascia recti anteriorly and the  The middle or intermediate chain usually comprises two or three
sacrum posteriorly, they send their efferent vessels towards nodes which lie on the anterior aspect of the external iliac vein
the internal iliac nodes laterally and towards the subaortic along the medial side of the artery. The lower node is termed the
nodes in the median area. The largest of these median sacral intermediate lacunar node, but is frequently absent. The middle
nodes usually rests on the anterior aspect of the L5-S1 interver- node, however, is always well developed and rests in front of the
tebral disc, and because of this location it is known as the prom- vein, midway between the inguinal ligament and the bifurcation
ontorial node [14]. of the common iliac artery. The upper node is located in the
angle between the origins of the external and internal iliac arter-
On the lateral pelvic walls, the lymph vessels run along the sur- ies. Known as the interiliac lymph node, the latter is usually cov-
face of the endopelvic fascia and join the external and internal ered by the iliac segment of the ureter [19,20].
chains of iliac nodes above the plane of the levator ani and coccy-  The medial chain includes three to four nodes and is placed on
geal muscles. Below the plane of the levator ani, the muscles and the medial side of the external iliac vein, against the lateral wall
fasciae are drained by the lymphatic vessels that follow the inter- of the pelvic cavity above the obturator nerve [14]. The lower
nal pudendal artery at the surface of the obturatorius internus, in node of this group is located immediately behind the femoral
Alcock’s pudendal canal. These deep lymphatics originate in the septum in contact with Cloquet’s deep inguinal lymph node,
prevesical space, bounded anteriorly by the pubic symphysis and and is commonly termed the medial lacunar lymph node [27].
posteriorly by the umbilicoprevesical fascia. They also collect the The suprajacent node, which is often very large, elongated and
lymph from the ischiorectal fossa, and then pass around the pos- lenticular, tends to separate itself from the vein and descend
terior aspect of the ischial spine and finally join the lower part of downwards into the pelvic cavity. Through this prolapse into
the internal iliac chain [19]. the pelvis, a number of authors regard the medial chain as
belonging to the internal iliac groups of nodes. Nevertheless,
Visceral vessels and nodes its pelvic affluents are relatively few in comparison to the major-
ity of its afferent vessels originating from the lower limb. There-
Like those of the abdomen, the visceral lymphatic vessels of the fore, it has to be considered functionally linked to the external
pelvis usually include several successive relays first located close iliac chain [15]. Furthermore, from the surgeon’s point of view,
to the viscera, then around the different vascular pedicles of each this group of nodes, located in a quadrangular area bounded
organ and finally along the large iliac vessels. At this level, they superiorly by the external iliac vein, posteriorly by the internal
form rich plexuses which are much more developed than in the iliac artery followed by the pelvic part of the ureter, and inferi-
upper part of the abdominal cavity and give rise to multiple orly by the obturator nerve, corresponds to the so-called obtura-
B. Lengelé, P. Scalliet / Radiotherapy and Oncology 92 (2009) 22–33 25

tor nodes [19,23]. As previously noted by Cruveilhier and Sappey against the origin of the superior gluteal artery. Intermediate nodes
[20], this surgical terminology should not lead to these nodes are distributed along the initial course of the uterine, internal
becoming confused with the isolated small obturator node which pudendal, inferior gluteal and middle rectal arteries. All these
occupies the internal foramen of the obturator canal in the lower nodes have the same name as the vessel they accompany [15,27].
part of the obturator fossa. The latter indeed drains satellite Afferent vessels of the internal lymph nodes originate from all
lymph vessels running along the obturator artery, and through the pelvic viscera including those from the posterior part of the
its efferents, it is functionally linked to the internal iliac chain. prostate, the lateral and lower parts of the urinary bladder, the
membranous and prostatic segments of the urethra, the seminal
As regards their afferent vessels, the lateral, intermediate and vesicles, the middle and lower parts of the vagina, the body of
medial chains of the external iliac nodes mostly receive collectors the uterus, and the middle part of the rectum [7,19,25].
from the lower limb through the superficial and deep inguinal In addition, the superior gluteal nodes drain the deep regions of
nodes. Furthermore, all these also drain deep lymphatic vessels the buttock, including the gluteal muscles, while the inferior gluteal
arising from the subumbilical part of the abdominal wall and deep nodes similarly collect lymph from the lower part of the gluteal re-
collecting trunks from the glans of the penis or clitoris which pass gion, in continuity with the posterior compartment of the thigh
through the inguinal canal, coursing along the vas deferens in the and the dorsal part of the posterior perineum [25]. The previously
male and along the round ligament of the uterus in the female mentioned internal pudendal lymphatic vessels join the nodes of the
[15]. In addition, the medial chain and to a lesser degree the inter- internal iliac chain in front of the origin of the sciatic nerve just
mediate chain, receive lymphatic satellites of the obturator vessels above the ischial spine, and drain the lymph from the deepest parts
originating from the muscles of the medial compartment of the of the perineum, the ischio-anal fossa and the lower parts of the
thigh and some visceral vessels ascending from the lateral lobes prostate, vagina and rectum [19,23].
of the prostate, the fundus of the urinary bladder, the cervix uteri The efferent vessels of the internal iliac nodes are directed up-
or the upper part of the vagina [2,19,25]. The latter originate from wards and outwards, course within the hypogastric lamina, then
the latero-uterine and laterovaginal juxtavisceral nodes which, as pass underneath the common iliac vein and terminate in the inter-
first described by Lucas Championnière, are located near the corre- mediate group of common iliac lymph nodes [20].
sponding organs, in the base of the broad ligament of the uterus,
alongside the terminal arch of the uterine artery and close to the Common iliac lymph nodes
origin of its upper vaginal branches in the parametrium [7,20]. Usually, ranging from four to seven in number, the common iliac
The fact that these vessels have a long course along the levator nodes are grouped around the common iliac vessels and, according
ani and obturatorius internus muscles before reaching the pelvic to their topographical distribution and afferent vessels, can be dif-
inlet and the fact that they end in the intermediate and medial ferentiated into the lateral, intermediate and medial groups of
chains of external iliac nodes may appear somewhat odd, since nodes [15,27]:
their route would be much shorter if they joined the internal iliac
nodes, over which they are compelled to cross. According to Cuneo  The lateral chain usually consists of two large nodes interposed
and Poirier, this arrangement is in fact explained by their specific between the lateral side of the common iliac artery and the
development [15]. In the fetus indeed, the prostate, vagina and cer- medial border of the psoas. This group forms an extension of
vix uteri are positioned much higher than in the infant or in the the lateral chain of external iliac nodes, and ends without any
adult, and are situated at the level of the pelvic inlet. At this stage, clear delineation in the lateral lumbar aortic chain of nodes [20].
their developing lymph vessels thus create their primary connec-  The middle or intermediate chain comprises three to four nodes
tions with the medial nodes of the external iliac chain and later which are usually concealed on the posteromedial side of the
on, when the organs occupy a lower position within the pelvic cav- artery. On the left side, they can be situated on the anterior
ity, their route then becomes more elongated and complicated. The aspect of the vein. Topographically, these retrovascular nodes
same phenomenon occurs with the lymphatics of the ovary and are located in Cunéo’s and Marcille’s triangular lumbosacral
testis which drain in the lower lateral aortic nodes according to fossa which is bounded medially by the body of the fifth lumbar
their lumbar embryonic origin (abdominal level IIIb in [10]), and vertebra, laterally by the medial border of the psoas and inferi-
which never develop any functional connection with the intrapel- orly by the upper border of the sacral wing. Usually, the com-
vic lymph nodes [23]. mon iliac vessels cross the anterior surface of the fossa which
The efferent vessels of each external chain iliac drain into the is filled with adipose tissue and which contains the nodes supe-
lower nodes of the corresponding common iliac chains. Several riorly and the lumbosacral and obturator nerves inferiorly
anastomosing channels run from the medial to the intermediate [15,23].
and from the intermediate to the lateral chains in such a manner  The medial chain runs along the inner side of the common iliac
that the medial pelvic lymphatic flow mixes progressively with arteries. Together with those of the other side, its nodes consti-
the lateral flow, mostly originating from the lower limb. The peri- tute an uneven group located on the midline just below the aor-
vascular network thus constituted is mostly located on the anterior tic bifurcation, in front of the fifth lumbar vertebra. Usually,
surface of the blood vessels, though some connecting vessels also known as the subaortic group of nodes, the latter is sometimes
cross their posterior aspect [15]. divided into two distinct subgroups [14]: the right subgroup,
which is located below the left common iliac vein, contains
Internal iliac lymph nodes the subvenous nodes; the left subgroup, which lies in front of
Often described as hypogastric nodes, the internal iliac nodes sur- the same vein, contains the prevenous nodes (see Fig. 4 in [10]).
round the internal iliac vessels and are placed near the origin of
their different branches or in the angles formed by their separation Respectively, constituting the terminal routes of the external
(Fig. 1). Most of them combine to form a crescent-shaped chain, and internal iliac chains, the lateral and intermediate common iliac
facing anteriorly and running in front of the sacro-iliac joint down- chains do not receive any direct afferent vessels from the pelvic
wards to the lower part of the greater sciatic foramen. Inferiorly, viscera. On the contrary, some lymphatics originating from the
the most anterior node of the chain is located between the umbil- neck of the bladder, the cervix uteri and the posterior aspect of
ical and obturator arteries below the point where the obturator the rectum directly enter the median group of subaortic nodes
nerve enters its canal. Posteriorly, the most superior node lies [4,7,14]. All these vessels follow the same course in the lower part
26 Delineation of pelvic lymph node areas

of the sacrorectogenitopubic septum and superiorly, in the sacro- spread for malignant tumors of the prostate, the cervix uteri
uterine folds, in the female. Closely linked to the pelvic diaphragm or the proximal part of the anal canal above the ano-cutaneous
at their origin, they then ascend into the sacral concavity and join junction [19].
the lateral sacral chains. Some of them pass through the lymph  The gonadic ascending accessory pelvic pathway runs along the
nodes of the promontory; the others terminate in the subaortic gonadic vessels to reach the inferior group of lateral aortic
nodes [19]. nodes. Located in the front of the psoas muscle, on the lateral
side of the abdominal part of the ureter, this ascending lympha-
Functional drainage pathways tic plexus is the usual route of lymphatic spread for ovarian
tumors. It also represents an alternative pathway of lymph node
Spread around the iliac vessels or closely related to the pelvic involvement for cancers of the uterine fundus, since some
organs, the lymph nodes of the pelvis are connected to one another lymphatics originating from that area run alongside the uterine
by a large number of afferent or efferent vessels which constitute tube in the mesosalpynx and join the ovarian vascular pedicle.
eight different drainage pathways [8]. All these streams which tra- Some other lymph vessels of the uterine tube may also accom-
verse specific perivascular and fatty spaces of the pelvis share the pany the round ligament, thereby resulting in secondary meta-
same main terminal route derived from the efferent pathway of the static nodes in the superficial inguinal area. Finally, it should
lower limbs. Comprising three lateral, intermediate and medial be noted that, at the point where they cross the external iliac
chains, the latter pass successively through the lacunar, external vessels, the lymphatics of the gonadic accessory pathway seem
iliac and common iliac nodes to finally reach the lateral aortic to create several anastomosing channels with the large collec-
nodes and the lumbar trunks entering the lower pole of the cis- tors of the external iliac chain [15]. These few bypass connec-
terna chili [23]. Connected to this common terminal route, the tions may well explain the occasional occurrence of secondary
lymphatic pathways of the pelvis can be described as including lateral aortic metastatic nodes at the L3 level associated with
three main anterior, middle and posterior pelvic pathways and five primarily invaded external iliac nodes, but without any enlarged
accessory pelvic pathways (Fig. 1): nodes in the common iliac or subaortic areas [6,7].
 The inferior mesenteric accessory pelvic pathway only involves the
 The main anterior pelvic pathway is constituted by the lymph drainage of the rectal pelvic compartment. Originating from the
vessels originating from the anterior pelvic viscera which drain upper part of the intramuscular and submucous networks of the
into the medial external iliac nodes. Located in front of the ure- rectum, this lymphatic chain accompanies the inferior mesen-
ter, the vessels and nodes of this external iliac pathway mainly teric vessels on the left side of the abdomen and terminates in
occupy the subperitoneal adipose tissue of the obturator fossa. the preaortic nodes at the L3 level. Its potential neoplastic
Surgically, they correspond to the structures that are excised involvement should be considered in cancers of the rectal
in obturator lymph node clearance. Clinically they are involved ampulla [4].
in the lymphatic spread of tumors of the fundus of the urinary  The superficial perineal accessory pelvic pathway should finally be
bladder, lateral prostatic lobes, cervix uteri and fornix vaginae considered as a route of lymphatic spread for tumors of the per-
[25]. ineal cutaneous part of the anal canal and the vulva. Located
 The main middle pelvic pathway follows the route of the lymph- anteriorly, this subcutaneous pathway ends in the superficial
atics of the internal iliac chain. Topographically located on the inguinal nodes and through the deep inguinal nodes becomes
posterior aspect of the pelvic ureter, this pathway then runs connected to the common terminal pelvic route of the external
superiorly along the sacro-iliac joint, exactly following the and common iliac chains [23].
course of the internal iliac vessels. Its metastatic involvement  According to some observations [19], the superficial inguinal
is common in cases of prostatic and vesical malignancies, but nodes also drain lymph vessels arising from the uterine fundus
also in cancer of the uterine body or of the middle part of the and horns. Running along the round ligament of the uterus,
rectum [19]. these vessels pass through the inguinal canal and so give rise
 The main posterior pelvic pathway follows the presacral chain. to a last inguinal accessory pelvic pathway which ends in the groin
Collecting vessels arising from the posterior parts of the pros- area.
tate, urinary bladder, cervix uteri or from the posterior aspect
of the rectum, this pathway has a fairly regularly curved course Practically, each organ within the pelvis thus contains its own
above the levator ani, along the lateral walls of the rectal com- primary dense submucosal lymphatic plexus which is then relayed
partment, then in front of the sacral concavity, after which it by secondary intramuscular and perivisceral or subperitoneal net-
reaches the lateral, or less frequently, the median sacral nodes. works, the density of which decreases progressively, and which
Because some of its lymphatic vessels originating from the are finally connected to several of the above-mentioned main and
above-mentioned organs terminate in the subaortic nodes, this accessory efferent lymphatic pathways. According to its location
posterior presacral pelvic pathway explains the possible pres- within the pelvic cavity and its vascular connections, each organ
ence of subaortic skip metastases as a primary site of lymph thus has a complex pattern of lymphatic drainage which usually in-
node involvement in the case of pelvic tumors which usually volves at least two major efferent pathways and one or more acces-
first invade the external or internal iliac lymph node groups of sory streams. The lymphatic spread of prostatic cancer may thus
the anterior and middle main pelvic chains [15]. involve four alternative pathways: the external iliac, internal iliac,
 The internal pudendal accessory pelvic pathway follows the course presacral and internal pudendal pathways [8,19]. Tumors of the
of the internal pudendal vessels below the level of the levator rectum preferentially invade the internal iliac and presacral chains,
ani muscle. Originating in Retzius’s prevesical space, it drains but may also spread via the inferior mesenteric and superficial per-
descending lymph vessels arising from the neck of the urinary ineal routes if the lesion extends near its proximal or distal extrem-
bladder, the apex of the prostate and the lower part of the ities [4,20]. Another example is that of uterine carcinomas in which
vagina, which then pass in the narrow space between both med- lymphatic metastases may extend along six possible pathways
ial sides of the puborectalis muscles. Thereafter following the mainly passing through the external iliac and internal iliac lymph
lateral wall of the ischio-anal fossa, this pathway is connected nodes, but also including additional potential relays in the presacral
behind the ischial spine with the middle internal iliac main nodes or along the lymphatic bypasses between the internal puden-
pathway and constitutes an alternative route of lymphatic dal, inguinal and gonadic chains [7,19,23].
B. Lengelé, P. Scalliet / Radiotherapy and Oncology 92 (2009) 22–33 27

Delineation of lymph node areas uterovaginal (G) and pararectal (R) – groups of nodes. These
volumes correspond to the fatty tissue surrounding each organ,
Pelvic lymph node areas cover the anterior, lateral and posterior and their lateral, anterior and posterior boundaries are delin-
walls of the pelvic cavity, and based on the above-described ana- eated by the right and left sacrorectogenitopubic septa, then
tomical facts, we have recently [8] proposed to differentiate them by the successive prevesical, prevaginal, prerectal and sacrorec-
into ten standardized volumes (Fig. 2): tal fasciae.
– The seven lateral paired volumes are present on both sides, and
– The three median volumes occupy the centre of the pelvis and, it is proposed that they should be distinguished as the external
respectively, include the juxtavisceral – perivesical (V), para- iliac, internal iliac, common iliac, subaortic, presacral and

Fig. 2. Radiological delineation of the pelvic lymph node areas. In addition to three central visceral volumes, seven lateral paired areas (levels I–VII) are defined on the pelvic
walls. The corresponding target volumes are indicated by different colors on anatomical and CT sections performed through the upper-female and lower-male parts of the
pelvis and also include additional extrapelvic superficial inguinal (SI) and lower abdominal (IIIA) areas. The key landmarks used to delineate the volumes are as follows: the
ureter (U), internal iliac (iiV) external iliac (EiV), gonadic (GV), inferior mesenteric (IMV) and internal pudendal (IPV) vessels, ischial spine and sacrospinous ligament (SSL),
sacrorectogenitopubic septa (SPS), urogenital diaphragm and the psoas (P), levator ani (LA), obturatorius internus (Oi) and gluteal muscles (G). Legends and colors used to
indicate the node groups are identical to those in Fig. 1, and the cardinal fatty spaces are indicated as ischiorectal (IRF) and lumbosacral (LSF) fossae.
28 Delineation of pelvic lymph node areas

Table 1
Pelvic lymph node levels and corresponding target areas for conformal radiotherapy, with their respective standardized anatomical landmarks.

Levels Lymph nodes and Vascular landmarks Bone landmarks Muscle landmarks Anterior Posterior
vessels boundary boundary
Level I External iliac Around external iliac vessels Medial side of iliopubic branch Medial edge of psoas, Femoral septum Pelvic ureter
lymph nodes and obturator foramen levator ani
Level II Internal iliac Around internal iliac vessels Medial side of ischium and Piriformis, levator ani, Pelvic ureter Lat. sacral edge,
lymph nodes and their branches greater sciatic aperture obturat. int. sacro-iliac joint
Level III Common iliac Around common iliac vessels Lateral side of L5 vertebral Medial edge of psoas Sacro-iliac joint Sacral wing
lymph nodes body
Level IV Presacral Along median sacral vessels Anterior aspect of sacrum None Fascia recti Sacral bone
lymph nodes concavity
Level V Subaortic Below aortic bifurcation Anterior aspect of L5 vertebral None Posterior L5 vertebra
lymph nodes peritoneal lining
Level VI Internal pudendal Along internal Medial side of ischiopubic branch Obturator internus, Pubic symphisis Ischial spine
lymph vessels pudendal vessels and obturator foramen ischiorectal fossa
Level VII Gonadic lymph Along gonadic vessels From iliac wing to upper plate Anterior aspect of psoas Posterior Psoas, lateral to
vessels of L3 vertebra peritoneal lining lumbar ureter

internal pudendal areas. On transverse CT or MR sections, their lumbosacral fossa which is bounded laterally by the medial
boundaries can be described as follows [8]. edge of the psoas muscle and medially by the lateral aspect
 The external iliac lymphatic area (level I) comprises a pyramidal of the L5 vertebra. Usually the blood vessels run along the
volume with the external iliac vessels circumscribing its base. anterior limit of this pyramidal volume which is based caudally
Laterally it is bounded by the medial side of the psoas muscle on the upper surface of the sacral wing and contains the com-
and medially by the peritoneal lining of the pelvic inlet. Its pos- mon latero- and retrovascular iliac lymph nodes as well as the
terior border is delineated by the pelvic part of the ureter, and lumbosacral nervous trunk and the origin of the obturator
anteriorly its limit corresponds to the femoral septum where it nerve. Superiorly, the apex of this area meets the central part
continues within the deep inguinal lymphatic area. Down- of the lower abdominal volume, in front of the L3 vertebra
wards, this area extends into the pelvis, on the inner surface (abdominal level IIIa).
of the iliopubic branch, of the upper part of the obturatorius  The presacral lymphatic area (level IV) corresponds to a triangu-
internus and of the levator ani. Its lowest narrow part corre- lar strongly curved volume which posteriorly faces the presacral
sponds to the inferior free edge of the levator ani. This area concavity. Bounded anteriorly by the fascia recti, its extends lat-
contains the external iliac artery and vein as well as the lym- erally towards the lateral borders of the sacrum where it
phatic vessels and nodes of the main anterior pelvic pathway, encounters the posterior limit of the internal iliac volume. Its
and also includes the proximal part of the gonadic accessory apex is directed caudally and corresponds to the coccyx, while
pathway, the anterior parietal branches of the internal iliac ves- its base is delineated by the sacral promontory. Within this vol-
sels and the obturator nerve. The so-called ‘obturator’ lymph ume, run the median and lateral sacral vessels, the lymphatics of
nodes are located at its centre and, on the left side of the pelvis, the presacral chains, the anterior branches of the sacral nerves
the interiliac nodes occupy its highest narrow apical part. On and the inferior hypogastric plexus.
the right pelvic walls, this node is placed behind the ureter  The subaortic lymphatic area (level V) continues superiorly the
which crosses the iliac vessels more anteriorly than on the left previous one and extends along the anterior aspect of the body
side [15]. However it belongs to the external iliac chain, the of the L5 vertebra. Its apex is in the narrow space superiorly
right interiliac node becomes thus included in the next radio- between both crura of the aortic bifurcation and its base, located
logical volume. at the upper border of S1, is contiguous with that of the presa-
 The internal iliac lymphatic area (level II) is located immediately cral area. This short triangular almost planar volume includes
behind the former one. It is also triangular in shape, is centred the origin of the median sacral artery, the subaortic group of
on the internal iliac artery and becomes enlarged caudally nodes and the superior sympathetic hypogastric plexus.
around its different visceral branches. Anteriorly, this volume  The internal pudendal lymphatic area (level VI) includes the pre-
is bounded by the pelvic part of the ureter and its posterior limit vesical fatty space and courses along the corresponding artery,
runs along the lateral edge of the sacrum then along the sacro- on the lateral wall of the ischio-anal fossa in the narrow angle
iliac joint. Inferiorly, the base of the triangle corresponds to between the levator ani and the obturatorius internus muscles.
the lower free edge of the levator ani, downwards to the apex Its posterior limit is marked by the ischial spine where it joins
of the coccyx dorsally. The lateral wall is lined superiorly by the middle part of the internal iliac lymphatic area.
the ischium, then by the medial surface of the piriformis and  The gonadic lymphatic area (level VII) finally occupies the lateral
levator ani more caudally. Its medial wall extends towards the aspect of the common iliac area. Located in front of the psoas
plane of the sacrorectogenitopubic septum. This area contains, muscle, on the lateral side of the ureter, it extends from the L5
in the adipose tissue surrounding the internal iliac vessels, most vertebra inferiorly, upwards to the L3 vertebra, where it fuses
of their posterior parietal and visceral branches but also the with the lateral part of the lower abdominal level IIIb [10]. Cen-
lymphatic pathways of the middle main pelvic pathway, the tered on the gonadic vessels, this volume contains the distal part
proximal part of the posterior presacral pathway, the efferent of the gonadic accessory pelvic pathway and includes also the
pelvic nerves of the hypogastric plexus and the origin of the sci- proximal course of the genitofemoral nerve and of the lateral
atic nerve. cutaneous nerve of the thigh.
 The common iliac lymphatic area (level III) is an upward exten-
sion of the two above-mentioned volumes, around the common At the end of the inferior mesenteric, inguinal and superficial
iliac vessels. Its three-dimensional space corresponds to the perineal accessory pathways, two extrapelvic areas have also to
B. Lengelé, P. Scalliet / Radiotherapy and Oncology 92 (2009) 22–33 29

Fig. 3. Lymphatic pathways and target volumes of the lower limbs. Anterior and posterior anatomical views of the lower limb showing the distribution of lymph vessels and
nodes. Node groups are identified as follows: superficial inguinal (SI), deep inguinal (DI), superficial popliteal (SP), middle popliteal (MP), deep popliteal (DP) and anterior
tibial (AT) nodes. Collecting vessels of the superficial system give rise to the medial (MA), inferior lateral (ILA) and superior lateral (SLA) ascending pathways and to the medial
(MG) and lateral gluteal (LG) pathways. The inguinal target volume is delineated on anatomical and CT sections of the groin area. Key anatomical landmarks indicating its
boundaries are as follows: the femoral vessels (FV), great saphenous vein (GSV), cribriformis (FC) and superficialis (FS) fasciae, and the pectineus (P), adductor longus (AL),
sartorius (S), rectus femoris (RF), gluteus (G) and iliopsoas (ip) muscles.

be considered as target volumes in the treatment of intrapelvic the above-described functional levels, their main vascular, bone
tumors: and soft tissue landmarks.

 The first one is the inferior mesenteric area. Arising from the
upper limit of the rectal visceral volume, it follows the infe- Lymphatics of the lower limbs
rior mesenteric vessels within the left mesocolon, and con-
tinues itself superiorly with the central part of the lower The lymphatic vessels of the lower limbs consist of two net-
abdominal volume, in front of the L3 vertebra. (abdominal works, one superficial and one deep, which are segregated by
level IIIa). the deep fascia and remain completely independent of one an-
 The second extrapelvic area corresponds to the superficial other although they finally converge in the popliteal fossa and
inguinal volume described with the lymphatics of the lower proximally in the groin area. During their course, they are inter-
limb. Located in the groin, it contains the superficial peri- rupted by several groups of nodes which are fewer in number
neal lymph vessels, in the lengthening of the soft tissues in the lower limbs than elsewhere. The terminal groups, located
of the perineum, below the muscles of the urogenital on the anterior root of the thigh, comprise the superficial and
diaphragm. deep inguinal lymph nodes. The outlying nodes, deeply located
on the interosseous membrane of the leg or on the posterior as-
Table 1 summarizes the anatomical principles for the CTV delin- pect of the knee, are known as the anterior tibial and popliteal
eation of the pelvic lymph nodes areas, and emphasizes for each of nodes (Fig. 3).
30 Delineation of pelvic lymph node areas

Lymph node groups uated against the femoral vein just below the point where the ter-
minal arch of the great saphenous vein opens into its anterior wall.
The superficial inguinal lymph nodes constitute one of the most When present, the highest node occupies the medial part of the
important lymphatic centres of the body. They are usually from femoral ring. It can often protrude into the pelvis, and is known
ten to twelve in number and are frequently larger than nodes from as Cloquet’s node by French authors [2,19,20] and is referred to
other lymphatic areas. They are all scattered in front of Scarpa’s as Rosenmüller’s node in the German literature [27]. Afferent ves-
femoral triangle in a space which is bounded superiorly by the sels to the deep inguinal nodes mostly issue from the terminal col-
inguinal ligament, laterally by the medial border of the sartorius lectors of the deep network of nearly the whole lower limb, which
muscle, and medially by the upper border of the adductor longus. accompany the femoral vessels. Nevertheless, they also receive
Topographically, the nodes are situated under the subcutaneous some afferents from the superficial inguinal nodes and few lym-
tissue and the superficialis fascia, and lie posteriorly on the cribri- phatic vessels from the glans penis in the male and from the clito-
form fascia which separates them from the femoral vessels and ris in the female. Their efferents penetrate the pelvis through the
nerve, and from the nodes of the deep inguinal group [23]. Due femoral canal, and join the lacunar nodes of the external iliac
to their large number, the extensive space they occupy and their group.
different drainage territories, they are usually divided into two The popliteal lymph nodes are from four to six in number, always
groups and four subgroups [15]. A horizontal line drawn through small in size and are embedded in the loose adipose tissue within
the terminal arch of the great saphenous vein separates the supe- the popliteal fossa. Mainly located around the popliteal vessels,
rior and inferior superficial inguinal groups. The latter groups are they form a chain around the vertical axis of the losangic space
then subdivided into two secondary subgroups, i.e., a medial and bounded superiorly by the hamstring muscles and inferiorly by
a lateral group. In the former group, the nodes are usually arranged the medial and lateral heads of the gastrocnemius. From the upper
in a chain of five to six nodes parallel to the inguinal ligament. On to the lower part, these nodes usually occupy three distinct loca-
the contrary, the latter group includes four to five elongated nodes tions [25,27]:
set vertically along the terminal part of the great saphenous vein.
According to several authors, additional small round nodes located  The most superficial node is situated just beneath the popliteal
in the saphenous opening are interposed between the previous fascia, against the termination of the small saphenous vein
nodes and constitute a supplementary central group [19,20]. How- and its entry into the popliteal vein. Invariably located on the
ever, although this subdivision may have certain clinical implica- medial side of the tibial nerve, it drains the superficial lymphatic
tions, it remains purely relative from an anatomical point of view vessels of the calf and those of the lateral edge of the foot [20].
since a large number of connections are present between the nodes  The middle nodes are spread around the popliteal vessels, either
from different subgroups, and also since their preferential tributar- on their lateral side or on their medial edge. Mainly linked to the
ies are subject to numerous variations [25]. popliteal vein, they drain the deep lymphatic collectors originat-
ing from the foot and the leg, coursing alongside the anterior tib-
 The afferent vessels of the superolateral group originate from the ial, posterior tibial and fibular vessels [15].
integuments of the gluteal region and the adjacent lateral part of  The deepest node is located on the anterior aspect of the popli-
the lower anterior abdominal wall, below the umbilicus. teal artery and lies against the oblique popliteal ligament. In
 The lymph nodes of the superomedial group receive afferent ves- close relation with the knee, it receives lymphatics from the
sels from the hypogastric area of the abdominal wall, but also a joint, which accompany the genicular arteries [19].
large number of collecting vessels originating from the external
genitalia including the skin of the penis, the scrotum, the vulva The efferent vessels of the popliteal nodes mainly follow the
and the distal parts of the vagina and anal canal below the ano- popliteal vessels, pass through the adductor canal and then course
cutaneous junction. As previously stated, they constitute the ter- alongside the femoral vessels before ending in the deep inguinal
minal relay of the superficial perineal alternative pathway for nodes. Some efferent vessels, however, remain at a more superfi-
the lymphatic drainage of the lower pelvis. Furthermore, they cial level and have a different outcome. Running alongside anasto-
also receive some afferent vessels from the uterine horns that motic veins which unite the small saphenous vein with the great
run through the inguinal canal with the round ligament of the saphenous vein, they terminate in the inferomedial group of super-
uterus. ficial inguinal nodes. This route is not as important as the former
 In the lower groups, both inferomedial and inferolateral nodes and may frequently be absent [15,19].
drain the terminal superficial lymphatic vessels of the lower The anterior tibial lymph node is usually unique and lies close to
limb, except those from the lateral edge of the foot and the pos- the anterior tibial vessels on the anterior aspect of the interosseous
terolateral aspect of the leg. membrane of the leg. Receiving afferents from the ascending col-
lectors of the dorsum of the foot and the muscles of the anterior
Efferent vessels from all the groups of superficial inguinal nodes crural compartment, it gives off a single efferent channel which
converge towards the central nodes when these are present, then terminates in the middle popliteal lymph nodes [23].
extend towards the deep inguinal nodes. To reach them, they usu-
ally pass through the saphenous opening along the saphenous vein, Functional drainage pathways
while others pass through the cribriform fascia, thereby creating its
multiperforated aspect. Among the efferent vessels arising from The superficial lymphatic vessels of the lower limbs originate
the lower nodes, some large collectors directly enter the pelvic cav- from a dense subcutaneous network which shows its maximum
ity through the femoral ring. Running alongside the femoral ves- development in the foot. The collecting trunks arising from this
sels, either in front of them, but with the majority on the inner plexus all converge in the groin, but follow three distinct pathways
side of the vein, they end in the lower pole of the lateral and inter- according to their respective origins (Fig. 3):
mediate lacunar nodes [15].
The deep inguinal lymph nodes, which are embedded in the sub-  The lymphatics originating from the medial side of the foot fol-
fascial adipose tissue of the femoral canal, are located on the med- low an ascending course on the medial side of the leg, which is
ial side of the femoral vein. They vary in number from one to three, closely related to that of the great saphenous vein. Thereby giv-
and when three of them are present, the lowest node is always sit- ing rise to the medial superficial lymphatic pathway of the lower
B. Lengelé, P. Scalliet / Radiotherapy and Oncology 92 (2009) 22–33 31

limb, some of them are located in front and others behind the of the greater sciatic foramen. Their terminal node usually occu-
medial malleolus, and progressively converge into ten large lon- pies the highest position in the internal iliac chain on the ante-
gitudinal collectors which also receive afferents from the ante- rior aspect of the actual trunk of the superior gluteal artery,
rior and medial aspects of the thigh and terminate in the above the upper edge of the piriformis [19].
lower groups of superficial inguinal nodes [2,20].
 The lymphatics arising from the lateral part of the foot and the Given these anatomical considerations, deep lymphophilic tu-
posterolateral part of the ankle progressively become satellites mors developing in the distal part of the lower limb and in the
of the small saphenous vein. Following this venous channel, anterior compartment of the thigh invade the principal deep chan-
they initially course between the lateral malleolus and the cal- nel with primary metastases in the popliteal and deep inguinal
caneal tendon and then ascend along the posterior aspect of nodes before involving the external iliac chain. The lymphatic
the calf. They thus constitute the lateral superficial lymphatic spread of posteriorly located deep tumors of the thigh or the but-
pathway of the lower limb and converge into three terminal tock on the contrary bypasses this usual route interrupted in the
collectors which perforate the fascia covering the popliteal groin area, and is characterized by the primary involvement of
fossa and then terminate in the superficial and middle popliteal intrapelvic nodes linked to the internal iliac chain.
nodes. From this point, the lymphatic drainage of the postero-
lateral cutaneous cover of the leg and foot follows thus the Delineation of node areas
deep lymphatic pathway, ending in the deep inguinal nodes
[23,25]. However, some superficial subcutaneous lymph vessels The lymph node areas of the lower limbs consist of two main
bypass the popliteal nodes, running alongside anastomosing volumes located, respectively, on the posterior aspect of the knee
veins that connect the great and small saphenous veins. Cross- and in the groin area. They are well circumscribed by the main
ing the medial edge of the thigh, they finally reach the medial muscular groups of the thigh and the calf, and include all the nodes
group of lower superficial inguinal nodes. This rare alternative of the main ascending pathways of the superficial and deep lym-
route mentioned by Sappey [20] can explain that the sentinel phatic streams (Fig. 3). They are easily identifiable on CT or MR
node of a skin tumor located on the lateral edge of the calf transverse sections, and are delineated as follows [8]:
or foot may be identified in the superficial inguinal nodes,
whereas it should theoretically be found among the popliteal  The inguinal volume corresponds to the anatomical boundaries
or deep inguinal nodes. of Scarpa’s femoral triangle. Limited superiorly by the inguinal
 Finally, the collecting trunks from the cutaneous layer of the glu- ligament, it extends laterally to the medial border of the sarto-
teal region are divided into two superficial gluteal pathways. The rius and medially to the lateral border of the adductor longus.
lateral stream usually constitutes the main pathway, drains the Pyramidal in shape, the inguinal volume is bounded on its ante-
ascending lymph vessels from the outer two-thirds of the but- rior surface by the fascia superficialis of the groin area. Posteri-
tock, and turns around the greater trochanter to terminate in orly, its deep walls are constituted by the outer surface of the
the superolateral group of superficial inguinal nodes. The medial iliopsoas muscle, laterally and medially, by the anterior aspect
stream concerns only the inner third of the gluteal area. Joining of the pectineus muscle. The base of the pyramid lies proximally
the lymphatics of the anal region, these vessels course down- and corresponds to the femoral septum. At this point underlined
wards and then forwards, thereby entering the superficial peri- by the upper border of the pubis, it encounters the anterior
neal pathway which ends in the superomedial group of extremity of the external iliac volume of the pelvic lymphatic
superficial inguinal nodes [19,20]. chains (pelvic level I). Caudally, the apex of the inguinal volume
is located in the narrow angle between the sartorius and adduc-
The deep lymphatics of the lower limbs drain the subfascial tis- tor longus muscles. Surgically, the inguinal volume is clearly
sues and course as satellites of the main blood vessels. They thus divided into two topographical compartments, respectively con-
comprise several converging channels which follow the anterior taining the saphenous vein and the superficial inguinal nodes on
tibial, posterior tibial and fibular vessels. Interrupted by the ante- one side, and the femoral blood vessels accompanied by the
rior tibial and middle popliteal nodes, they thereafter run along deep inguinal nodes on the other. The cibriform fascia which
the femoral vessels until they reach the deep inguinal and lacunar covers the femoral canal constitutes the anatomical plane which
external iliac nodes [25]. In addition to this principal deep channel segregates both these superficial and deep compartments which
which drains all the deep tissues of the foot and leg and the ante- are cleared separately or in continuity in an inguinal dissection.
rior compartment of the thigh, deep accessory channels are present Because of its low thickness and its multiple perforations, it is
along the obturator and superior or inferior gluteal arteries usually difficult to recognise this plane on radiological images.
[15,19]: The anterior limit of the inguinal volume therefore remains par-
tially virtual, just as its subdivision into deep and superficial
 Among these, the obturator collecting trunks arise from the compartments. In addition to the femoral artery and vein, the
adductor muscles and drain the medial compartment of the deep part of the inguinal volume contains the deep inguinal
thigh. Passing through the obturator canal with their companion lymph nodes, the origin of the external pudendal, superficial cir-
vessels, they terminate in the true obturator lymph node and cumflex iliac and superficial epigastric vessels, and the common
then in the internal iliac nodes [20]. stem of the femoral nerve that runs on the surface of the ili-
 The inferior deep gluteal lymphatics accompany the inferior glu- opsoas muscle. The superficial part of the inguinal volume
teal blood vessels and mainly drain the hamstring muscles and includes, in the subcutaneous fat, the superficial inguinal nodes,
soft tissues of the posterior compartment of the thigh. Entering the terminal part of the great saphenous vein and the femoral
the pelvis through the lower part of the greater sciatic foramen, branch of the genitofemoral nerve.
they usually end in a specific small node of the internal iliac  The popliteal volume occupies the losangic space of the popliteal
group which is situated on the lower border of the piriformis fossa. Superiorly, it is then bounded by the medial (semitendi-
(Fig. 3). nous and semimembranous) and lateral (biceps femoris) ham-
 The superior deep gluteal lymphatics originate from the gluteal string muscles. Inferiorly, it extends between the medial and
and pelvitrochanteric muscles. They run along the superior glu- lateral heads of the gastronemius. Its anterior aspect corre-
teal vessels and then pass into the pelvis through the upper part sponds to the posterior capsule of the knee joint covered by
32 Delineation of pelvic lymph node areas

the popliteus, while its posterior surface extends between the ture for all levels, each level receiving a name firstly defined by
four above-mentioned muscular edges, in order to virtually rep- its location on the trunk (C for cervical, T for thoracic, A for abdom-
resent the anatomical plane of the popliteal fascia. In addition to inal and P for pelvic) and thereafter characterized by its relative
the popliteal lymph nodes within the fatty tissue of the fossa, position along the main or accessory drainage pathway (I to III or
this volume contains the popliteal blood vessels and their artic- VII, in roman numerals). Sublevels, when present, are identified
ular branches, the terminal part of the small saphenous vein and as N a, b or c, according to their specific topography and functional
the tibial nerve. The common fibular nerve, running along the connections with related organs. For example, submandibular and
lower border of the biceps femoris should not be systematically jugulodigastric lymph node groups, draining the oral floor and the
included in the lymphatic volume. As previously stated, the pop- body of the tongue are located in functional levels CII a and CII b,
liteal lymph nodes indeed occupy the central axis of the fossa in respectively. Namely, subcarinal nodes draining cells arising from
the immediate vicinity of the veins. They thus have a close rela- bronchial cancer are included in the upper part of the central medi-
tion with the tibial nerve but are quite distant from the fibular astinal level TII c, in the same functional clinical target volume as
terminal branch of the sciatic nerve. the adjacent bronchopulmonary lymph nodes (see part II in [10]).
Finally, common iliac nodes are resting along the distal part of
the main pelvic pathway in level PIII, and their clinical target vol-
General conclusion: the lymphosome concept ume is contiguous with those of the subaortic area (level PV) and of
the central part of the lower abdominal level (level AIII a).
In the past decade, the fast technical developments registered in As already stressed above and in part II of these series [10],
conformal and intensity modulated radiotherapy and the nearly there is no real anatomical or functional rationale to divide in dis-
simultaneous introduction of the sentinel node concept in oncolog- tinct levels or sublevels the axillary and inguinal volumes which
ical surgery have dramatically changed the management guide- contain the proximal groups of nodes draining the limbs. Though
lines of numerous cancer patients. By the way, both surgery and such divisions have been suggested and commonly used previ-
radiotherapy nowadays tend to become more selective on the tu- ously, they were drawn onto virtual surgical limits, and were thus
mor itself and on the various lymph node stations prone to be in- mostly useful to create a distinction between more or less exten-
vaded depending on the precise location and extension of the sive lymph node dissection procedures. We therefore advocate to
primary lesion. Nevertheless, all these technical developments consider both axillary and inguinal volumes as undivided clinical
have also induced a increased medical need for an updated and target areas in conformal radiation therapy. Nevertheless, segre-
more detailed anatomical knowledge of the dynamic lymphatic gated lymphatic territories exist obviously in the superficial and
networks associated with each part of the human body. In the pres- deep compartments of upper and lower limbs, as they are present
ent series, we have tried to join our combined experiences in the in the integuments and walls of the head, neck and trunk areas
fields of anatomy, surgical oncology and radiotherapy in order to [13]. All these contiguous areas, drained by distinct collectors, also
summarize the essentials to know about the main and accessory behave as dynamic and highly plastic lymphosomes, as suggested
pathways of lymphatic spread potentially involved in the natural by recent experimental investigations [13,21]. Limbs lympho-
evolution of any tumor developing in the head and neck area, on somes, as mapped in Fig. 2 of part II [10] and in Fig. 3 above, are
the limbs, or in the chest, abdomen and pelvis. thus potentially relevant in the treatment of skin cancer, especially
Our second goal was to point out the noticeable discrepancies in melanoma, and provide an anatomical basis for the surgical
that still exist, in several areas of high clinical interest, between application of the sentinel node concept in the management of
functional anatomical facts and some surgical or radiological clas- malignant skin tumors. Nevertheless, functional plasticity of the
sification patterns that are very commonly used for nodal meta- lymphosomes is always to be considered in any CTV treatment
static staging on CT images or pathological specimens. Because planning, since several alternative routes of lymphatic spread cur-
there is consequently a need for using a standardized nomencla- rently coexist in each specific cancer location, especially when the
ture to describe accurately lymph nodes groups, to achieve their tumor has developed on the relative anatomical boundary between
adequate clinical staging and to delineate the corresponding target two neighboring lymphosomes and when surgery has potentially
volumes for surgical lymph node clearance and/or conformal modified their dynamic functional relationships.
radiotherapy, we have also made here an attempt to include all
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