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Gynecologic Oncology 116 (2010) 33–37
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Gynecologic Oncology
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y g y n o
Pelvic lymphadenectomy in cervical cancer—surgical anatomy and proposal for a
new classification system
D. Cibula a,⁎, N.R. Abu-Rustum b
a
b
Oncogynecological Centre, Department of Obstetrics and Gynecology, General Faculty Hospital, First Medical Faculty, Charles University, Apolinarska 18 Prague 2, 12000, Czech Republic
Gynecology Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
a r t i c l e
i n f o
Article history:
Received 9 July 2009
Available online 17 October 2009
a b s t r a c t
Background. Pelvic lymphadenectomy is an integral component of gynecologic cancer surgery, yet there
is a lack of standardization in the terminology used, the extent of the procedure, and the definition of
anatomic landmarks. This lack of standardization if corrected will likely facilitate a more clear
communication and analysis of outcomes from various institutions, and reduce confusion to trainees about
the procedure being performed.
Methods. We summarize the anatomic data concerning pelvic lymphatic drainage; describe the procedure
based on clearly defined anatomic landmarks; and finally propose a new classification system to facilitate
standardization, communication, and comparison of results. The accompanying video demonstrates the
anatomic landmarks.
Results. We list and define four commonly used terms related to pelvic lymph node harvesting: sentinel
node mapping, excision of bulky nodes, pelvic lymph node sampling, and systematic pelvic lymphadenectomy.
We list the five specific anatomic regions of the pelvic lymphatic basin: external iliac, obturator, internal
iliac, common iliac, and presacral. We highlight the important neural structures located in regions of the
pelvic lymphadenectomy: genitofemoral nerve, obturator nerve, cranial part of the lumbosacral plexus,
hypogastric plexus, and splanchnic nerves. Finally, we propose a new, four-part classification system of types
of pelvic lymph node dissection.
Conclusion. In this report and video, we demonstrate anatomy and offer a new classification system for
pelvic lymphadenectomy.
© 2009 Elsevier Inc. All rights reserved.
Introduction
Surgery is the least standardized treatment modality in gynecologic oncology. This lack of standardization is due to factors such as
differences in surgical approach, technology used, patient anatomy,
difficulty in measuring and quantitating the extent of procedures, and
also imprecise definitions of the extent of some surgical procedures.
The technique of pelvic lymphadenectomy has been much
discussed in the literature, both in gynecology and urology [1-7].
There are, however, still differences in the terminology used to
describe this procedure. Furthermore, anatomic landmarks are not
clearly defined in all pelvic regions. The total number of lymph nodes
examined in the final pathology report, although highly dependent on
the patient and on the quality and accuracy of the pathologic evaluation, still remains one of the few objective criteria in the assessment
of the procedure's extent and completeness. With the exception of
sentinel node mapping, the larger total lymph node counts are
frequently used as a surrogate for radicality and completeness of
surgery. The number of lymph nodes examined in the final report
varies substantially in the literature, and this variation mirrors a
general lack of standardization in pelvic lymphadenectomy.
The aim of this paper is to contribute to the standardization of
pelvic lymphadenectomy terminology and technique. In particular, we
summarize the anatomic landmarks concerning pelvic lymphatic
drainage that may serve as the rationale for determining the extent of
pelvic lymphadenectomy; describe the procedure in a video based on
clearly defined anatomic landmarks; and finally propose a new
classification system to facilitate standardization, communication,
and comparison of results.
Commonly used terminology
⁎ Corresponding author. Oncogynecological Centre, Department of Obstetrics and
Gynecology, General Faculty Hospital, First Medical Faculty, Charles University,
Apolinarska 18, Prague 2, 120 00, Czech Republic. Fax: +420 224967452.
E-mail address: [email protected] (D. Cibula).
0090-8258/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.ygyno.2009.09.003
Our first step is to identify commonly used terminology relating to
the pelvic lymphadenectomy. In the current literature, several types
of surgical procedures for pelvic lymph node harvest are recognized.
34
D. Cibula, N.R. Abu-Rustum / Gynecologic Oncology 116 (2010) 33–37
Sentinel lymph node biopsy (SLN)
The least extensive lymph node harvesting procedure is the
sentinel node (SLN) biopsy. The objective of the SLN is to detect and
remove the first draining lymph node(s) on each side of the pelvis.
Several authors have reported high rates of detection and sensitivity
in cervical cancer (especially small tumors) [8-10]. It is assumed that
SLN mapping will become a standard part of the surgical management
of cervical cancer.
Excision of only bulky nodes
Excision of only bulky nodes is a limited lymphadenectomy targeting enlarged nodes only.
Nevertheless, there have been repeated reports showing low
reliability of palpation of the retroperitonium, and an inadequate
sensitivity of current imaging methods in detection of positive nodes
[11-12].
Pelvic lymph node sampling
Pelvic lymph node sampling is variably defined, either as the
removal of a certain minimal number of lymph nodes, or based on
anatomic criteria [13]. Irrespective on the definition, lymphatic tissue
removal is limited to easily accessible pelvic regions and does not
address all nodal groups. The number of lymph nodes obtained during
sampling procedures is usually very low.
Complete (systematic) pelvic lymphadenectomy
Complete pelvic lymphadenectomy should be defined as the
removal of all fatty lymphatic tissue from the predicted areas of high
incidence of lymph nodes with metastatic involvement. The extent of
the procedure should be standardized, and defined by exact anatomic
landmarks. The aim of the complete pelvic lymphadenectomy is to
remove the majority of lymphatic tissue that drains pelvic organs. The
following regions are the most commonly recognized: common iliac,
external iliac, internal iliac, obturator, and sacral (or presacral). Some
authors further differentiate parametrial and interiliac regions, while
others include tissue from the interiliac region to the external iliac and
obturator regions and remove the tissue from the parametrial region
together with the parametrium during radical hysterectomy.
SLN mapping and distribution of positive pelvic nodes
in cervical cancer
In recent years, there has been a growing interest in SLN mapping
owing to an effort to evaluate reliability and accuracy of SLN biopsy in
cervical cancer. In the largest studies, 75–88% of SLN were found in two
main regions: the obturator fossa and the external iliac region (defined
as interiliac by Marnitz et al. [9]) (Fig. 1) [8-10]. About 5% of SLN were
reported in the presacral region, and 5% in the common iliac region. Data
differ for the internal iliac, paraaortic, and parametrial regions, most
likely due to differences in anatomic boundaries of each region [14-15].
Unfortunately, the majority of studies do not allow for more detailed
anatomical analysis of SLN localization within the regions described
above; such analysis would be beneficial, especially for obturator
(supra- or infraobturator) or common iliac (superficial or deep) regions.
Not surprisingly, localization of metastatically involved SLN corresponds
well with sites of their most frequent detection (Fig. 1) [8-10].
Moreover, the localization of positive pelvic lymph nodes correlates well with data available from SLN mapping (Fig. 1) [16-18]. In
larger studies of early stages cervical cancer, positive lymph nodes
were most frequently detected in the external iliac, obturator, internal
iliac, common iliac, and parametrial regions. Localization in the
paraaortic region (1–4.3%) or in the inguinal nodes (1.9%) was rarely
Fig. 1. Distribution of sentinel nodes / positive sentinel nodes / positive lymph nodes in
% (adopted from [8-10, 16-18]). Regions: CI–common iliac; PS–presacral; EI–external
iliac; OBT–obturator; II–internal iliac.
reported. Some authors have differentiated deep common iliac and
infraobturator (deep obturator) regions, where positive nodes were
found in 7% (1/14) [16]. Large variations in the distribution are again
likely due to the differing anatomic boundaries of individual regions,
mostly including the parametrial or part of the external iliac nodes in
the obturator region.
Anatomy of the pelvic lymph node drainage
Classical anatomical studies on cadavers described very complex
lymphatic drainage of the cervix, creating three major lymphatic
trunks: lateral, anterior, and posterior. These major trunks terminate
in the interiliac, common iliac, obturator, inferior gluteal, superior
gluteal, superior rectal, or presacral nodes (regions) [19]. Based on
data from surgicopathologic studies on SLN and the distribution of
nodal metastasis, it is obvious that clinical importance of the above
regions is not equal. Specifically, the superior rectal, superior gluteal,
and inferior gluteal regions are rarely involved.
For surgical anatomy, it is important to emphasize that the main
purpose of major lymphatic trunks in the pelvis is to drain the lymph from
lower extremities cranially toward the paracaval and paraaortic lymphatic systems. These trunks receive multiple channels from the midline
gynecological organs. Surgical dissection inside these trunks is more
difficult; it causes bleeding and inevitably leads to incomplete removal of
lymphatic tissue that belongs to highly networked lymphatic trunks.
Two major lymphatic trunks can be identified running on the lateral
pelvic walls, which are involved in drainage of the cervix, with multiple connections between them. Comprehensive demonstration is
available on this paper's accompanying film (supplementary data; film
also available at www.esgo-forum.org/videolibrary). A “superficial
trunk” enters the pelvis through the femoral canal; it courses on the
ventral walls of external iliac vessels, receives lymphatic channels from
parametria, and continues on the ventral wall of the common iliac artery
cranially to precaval and interaortocaval regions (Figs. 2 and Supplementary Fig. 1). A deep trunk enters the pelvis from the femoral canal
as well, medial to external iliac vessels, and surrounds the obturator
nerve as a broad bundle of fatty lymphatic tissue, receiving numerous
channels from lateral parametria (Fig. 3 and Supplementary Fig. 2).
From the obturator fossa it continues cranially to the space between
superior gluteal vessels and the psoas muscle, where it divides into two
parts (Fig. 3). The first one creates a deep common iliac branch that runs
between the psoas muscle and common iliac vein, continuing cranially
D. Cibula, N.R. Abu-Rustum / Gynecologic Oncology 116 (2010) 33–37
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Surgical anatomy of pelvic lymphadenectomy
To facilitate orientation, the pelvic lymphatic basin can be divided
into five specific anatomic regions.
External iliac region (Fig. 4)
Tissue is removed cranially, laterally, and medially from both
external iliac vessels and between them. The medial border is formed
by the opened space of the paravesical fossa, which is bounded
cranially by the course of the umbilical ligament. The lateral border is
the psoas muscle. The ventral border is commonly indicated as the
origin of the deep circumflex iliac vein; however, the origin of this
vessel is variable and other lymph nodes are located more ventrally.
The ventral border should thus be the superior ramus of the pubic bone
and the entry into the femoral canal. Some authors have suggested a
greater risk of lymphedema after removal of these distal external iliac
nodes. The risk of their metastatic involvement is probably low, but
exact data are not available [20]. The dorsal border is the level of the
common iliac artery bifurcation, where it continues as the superficial
common iliac region. Caudally, it is the level of the caudal margin of the
external iliac vein where the tissue proceeds into the obturator region.
Fig. 2. Diagram of pelvic lymphatic drainage - superficial lymphatic trunk (right side)
EIA–external iliac artery; EIV–external iliac vein; IIV–internal iliac vein; IIA–internal
iliac artery; CIA–common iliac artery; CIV–common iliac vein; GN–genitofemoral nerve;
PM–psoas muscle; A–aortic bifurcation SLT–superficial lymphatic trunk; EI–external
iliac region; SCI–superficial common iliac region.
into the paracaval region. The second one, which is often overlooked
during lymphadenectomies, runs medially through a tunnel below the
common iliac vessels into the medial aspect of common iliac vessels,
continuing cranially into the presacral region (Fig. 3 and Supplementary
Fig. 3). From here it crosses, cranially, the left common iliac vessels and
enters mostly interaortocaval and preaortic regions (Supplementary
Fig. 2). This deep trunk receives—on the medial aspect of the common
iliac vessels—a lymphatic branch from the internal iliac region, having
multiple channels from parametria.
Fig. 3. Diagram of pelvic lymphatic drainage–deep lymphatic trunk (right side) EIV–
external iliac vein; EIA–external iliac artery; IIV–internal iliac vein; IIA–internal iliac
artery; CIA–common iliac artery; CIV–common iliac vein; GN–genitofemoral nerve;
PM–psoas muscle; A–lymphatic passage below common iliac vessels DLT–deep
lymphatic trunk; OBT–obturator region; II–internal iliac region; DCI–deep common
iliac region.
Obturator region (Fig. 5)
Tissue is removed from the obturator fossa. The cranial border is
the caudal wall of the external iliac vein. The dorsal border is the level
of the bifurcation of the common iliac vessels, medial the paravesical
space, formed by the lateral wall of the urinary bladder. The ventral
border is the pubic bone together with the levator ani and obturator
muscles, where the obturator nerve leaves the pelvis through the
obturator canal. The lateral border is formed by the obturator internal
muscle; caudal anatomical landmarks are obturator vessels.
Fig. 4. Anatomic landmarks of external iliac (EI), superficial common iliac (SCI), internal
iliac (II) and presacral (PS) regions B–deep iliac circumflex vein; ON–obturator nerve;
UL–umbilical ligament; PVS–paravesical space; IIA–internal iliac artery; IIV–internal
iliac vein; SN–splanchnic nerves; SHP–superior hypogastric plexus; U–ureter; MU–
mesoureter; SB–sacral bone; A–aortic bifurcation; EIA–external iliac artery; EIV–
external iliac vein; PM–psoas muscle; GN–genitofemoral nerve; CIV–common iliac
vein; CIA–common iliac artery; IVC–inferior vena cava.
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D. Cibula, N.R. Abu-Rustum / Gynecologic Oncology 116 (2010) 33–37
by the course of both common iliac vessels, on the left side partially
by the mesoureter [21]. The caudal border is formed by the sacral
bone, and the ventral by the level of the right common iliac vessels
bifurcation.
Anatomic considerations of neural structures encountered during
pelvic lymphadenectomy
Awareness of anatomic location of nerve structures in all regions of
pelvic lymphadenectomy is essential for the safety of procedure. Care
must be taken to avoid any harm to nerves, either direct injury or
indirect thermal damage caused by electrosurgery.
Genitofemoral nerve (Figs. 2 and 4)
Runs in the common iliac region on the cranial aspect of the
psoas muscle. This nerve often forms two branches in the
external iliac region: one branch continues on the psoas muscle,
while the second joins the superficial lymphatic trunk on the
cranial aspect of external iliac artery, where it can be easily cut
or injured.
Obturator nerve (Fig. 5)
Runs in the middle of obturator fossa, surrounded by fatty lymphatic tissue. It leaves the pelvis ventrally through the obturator canal,
and is exposed also in the deep common iliac region between the
psoas muscle and common iliac vein, where it runs from below the
psoas muscle.
Fig. 5. Anatomic landmarks of deep common iliac (DCI) and external iliac (EI) regions
PVS–paravesical space; EIA–external iliac artery; EIV–external iliac vein; UL–umbilical
ligament; OA–obturator artery; OV–obturator vein; OM–obturator muscle; ON–obturator
nerve; SGV–superior gluteal vein; LST–lumbosacral nerve trunk; SB–sacral bone; CIA–
common iliac artery; CIV–common iliac vein; ILV–iliolumbal vein; PM–psoas muscle.
Internal iliac region (Fig. 4)
Tissue is removed medially from the internal iliac vein. The ventral
border is the level of the uterine vein origin; medially it is the
mesoureter (a thin layer, coursing caudally from the ureter to the sacral
bone, forming the boundary between the pararectal fossa medially, and
lympho-fatty tissue and large vessels laterally; containing the
hypogastric plexus), cranially and laterally it is the course of the
internal iliac vessels, caudally it is the sacral bone, and dorsally it is the
level of the bifurcation of the common iliac vessels.
Common iliac region (Figs. 4 and 5; Supplementary Fig. 5)
Tissue is removed ventrally and laterally from both common iliac
vessels. The lymphatic tissue can be anatomically divided into two parts:
the superficial branch, which continues from the external iliac region,
and the deep branch, which runs deeply between the common iliac vein
and psoas muscle, continuing from the obturator region. The dorsal
border is the level of the aorta bifurcation; medial on the right side is the
medial aspect of common iliac vessels (the tissue medial to the vessels is
removed together with the presacral nodes), while on the left it is the
mesoureter (tissue medial to the vessels should be removed as well).
Lateral border is formed by the psoas muscle, ventral by the bifurcation
of common iliac vessels. The caudal border is formed by the sacral bone,
the cranial part of the lumbosacral trunk (L4 + L5) (medially), and the
obturator nerve (laterally), where it enters under the psoas muscle.
Presacral region (Fig. 4 and Supplementary Fig. 6)
Tissue is removed above the sacral bone below and between
both common iliac veins. The cranial and lateral borders are formed
Cranial part of the lumbosacral plexus (L 4-5)
(Fig. 5 and Supplementary Fig. 5)
Exposed together with the obturator nerve (which is lateral) in a
deep common iliac region.
Hypogastric plexus (Fig. 4)
Runs inside of the mesoureter, which forms a thin tissue layer
between pararectal fossa and large vessels; it is exposed during
dissection of the presacral and internal iliac regions.
Splanchnic nerves (Fig. 4)
Cross the space between the mesoureter and large vessels; are
exposed during dissection of the internal iliac region.
Proposal for a new classification system of types of pelvic lymph
node dissection
We propose a new system to classify types of pelvic lymph node
dissection. The four types are listed below.
• Type SLN:
Only the sentinel lymph nodes detected in the pelvic basin are
removed
• Type I dissection:
External iliac region: removes lymph nodes anterior and medial to
the external iliac vessels, ventrally up to the deep circumflex iliac
vein.
Obturator region: removes obturator nodes above the obturator
nerve.
Common iliac region: removes nodes anterior (superficial common
iliac region) up to the mid common iliac vessels.
• Type II dissection:
D. Cibula, N.R. Abu-Rustum / Gynecologic Oncology 116 (2010) 33–37
This is a type I dissection which also includes all of the following
steps:
External iliac region: removes nodes between the external iliac
vessels and psoas muscle after vessel mobilization and complete
skeletonization; removes distal nodes caudal to deep circumflex
iliac vein.
Internal iliac region: exposes the internal iliac vein and removes
internal iliac nodes.
Obturator region: removes nodes below obturator nerve.
Presacral region: complete removal of presacral nodes.
• Type III dissection:
This is a type II dissection which also includes all of the following
steps:
Common iliac region: removal of superficial common iliac nodes
up to the aortic bifurcation; complete medialization of the
common iliac vessels and removal of deep common iliac nodes
between the lateral aspect of the common iliac vein and the psoas
muscle exposing lumbosacral trunk.
Conclusion
Pelvic lymph node dissection remains an integral component of
gynecologic cancer surgery. In modern surgical practice it is essential to
standardize terminology and the extent of procedures to facilitate clear
communication and analysis of outcomes from various institutions, and
to reduce confusion to trainees about the procedure being performed.
With our increasing knowledge of the patterns of lymphatic drainage
from the emerging SLN mapping data and from anatomic dissections in
the living, we are now able to more accurately map and localize the
anatomic regions most relevant to the diseases we treat and more
precisely target the pelvic regions at risk for nodal metastasis. In spite of
continuing debates about the “therapeutic role” of pelvic lymph node
dissection in some gynecologic malignancies, a pelvic lymphadenectomy will remain a sentinel procedure in gynecologic oncology training
and an important surgical tool for resection of metastatic disease and
for staging of select gynecologic tumors. As gynecologic oncologists, we
should continue to teach this important procedure to residents and
fellows in training and provide them with better anatomic and
oncologic rationale for what we practice. We hope that this article
and video contributes to standardization and classification of one of the
basic procedures in gynecological oncology and improves communication and educational efforts among various training programs.
Conflict of interest statement
The authors have no conflicts of interest to disclose.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.ygyno.2009.09.003.
37
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