JOURNAL OF LAPAROENDOSCOPIC & ADVANCED SURGICAL TECHNIQUES

Volume 33, Number 5, 2023

ª Mary Ann Liebert, Inc.
DOI: 10.1089/lap.2022.0516

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Laparoscopic Lateral Lymph Node Dissection Based

on Membrane Anatomy for Lower Rectal Cancer:
Surgical Technique and Short-Term Outcomes
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Jiaqi Wang, MS,1,* Yi Chang, MD,1,2,* Hailong Liu, MD,1,2 Wenchao Wang, MD,1 Xuan Tang, MS,1
Huihong Jiang, PhD,1,2 Ajian Li, MD,1 and Moubin Lin, MD1,2

Abstract

Background: Lateral lymph node dissection (LLND) is an effective treatment for metastatic lateral lymph
nodes (LLNs) in lower rectal cancer, but with high complication rates due to a complicated procedure. This
study aimed to introduce a new technique for LLND based on membrane anatomy to simplify the procedure and
report short-term outcomes.
Methods: Twenty-three patients with clinical stage II-III lower rectal cancer underwent three-dimensional (3D)
laparoscopic total mesorectal excision (TME) plus LLND between July 2018 and December 2020. Demo-
graphic data, perioperative variables, and oncologic outcomes were recorded and analyzed. Complications were
graded using the Clavien-Dindo (CD) score.
Results: Based on the theory of ‘‘four fasciae and three spaces,’’ we proposed a fascia-to-space surgical
approach to perform LLND. 3D laparoscopic TME plus LLND was performed successfully in all patients. The
mean operating time was 172 minutes with a mean blood loss of 85 mL. Postoperative complications were
present in 5 (17.4%) patients (CD I–II), including a case of urinary retention. The median number of harvested
LLNs was 9, and positive LLNs were detected in 7 (30.4%) patients. After a median follow-up of 26.5 months,
2 (8.7%) patients developed liver metastases, but no local recurrence.
Conclusions: Laparoscopic LLND based on membrane anatomy is a safe, feasible, and reproducible procedure
and thus worthy of clinical promotion. Further studies with long-term follow-up in larger patient series are still
required.

Keywords: lower rectal cancer, lateral lymph node dissection, membrane anatomy, oncologic outcome,
postoperative complications

Introduction However, the role of LLND still remains controversial

in Western countries because of the complexity of this pro-
cedure and complications it induces.5,6 A Japanese clinical
L ateral lymph node (LLN) metastasis has been esti-
mated to occur in 15%–30% of patients with lower
rectal cancer and is a significant contributor to postoperative
trial ( JCOG0212) reported that even with the introduction
of pelvic autonomic nerve preservation, the rate of urinary
recurrence.1,2 Lateral lymph node dissection (LLND) is an dysfunction following LLND could be as high as 59%.7
effective operation for removing metastatic lymph nodes.3 In In recent years, with the development of membrane anat-
Japan, total mesorectal excision (TME) plus LLND has be- omy in colorectal surgery, more and more surgeons have
come the standard surgical procedure for locally advanced begun to investigate LLND based on membrane anatomy
lower rectal cancer.4 with the aim of improving precision and safety of the
1
Department of General Surgery, Yangpu Hospital, Tongji University School of Medicine, Shanghai, China.
2
Institute of Gastrointestinal Surgery and Translational Medicine, Tongji University School of Medicine, Shanghai, China.
*These authors contributed equally to this work.

497
 498
procedure.8,9 However, up to now, the detailed anatomy of
fasciae and fascial spaces related to LLND has not been well
described and therefore there is no established standard
surgical procedure.
Based on years of experience in cadaveric dissections, we
conducted an in-depth analysis of the membrane anatomy
related to radical rectal cancer surgery10,11 and proposed
the theory of ‘‘four fasciae and three spaces.’’12 Generally,
the fascia propria of the rectum, urogenital fascia, vesico-
hypogastric fascia, and parietal fascia lie side by side in
a medial–lateral direction and form three spaces (medial,
middle, and lateral) around the rectum. Among them, the
medial space corresponds to the resection area of TME and
the middle and lateral spaces constitute the surgical field
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for LLND.13
According to the theory, we developed a technique of
laparoscopic LLND in two fascial spaces to simplify the
surgical procedure (Fig. 1). In this study, we introduced the
key elements of this procedure and reported its short-term
outcomes.
Materials and Methods
Case–patient
This was a prospective cohort observational study that was
conducted on patients who underwent 3D laparoscopic TME
plus LLND at our hospital between July 2018 and December
2020.
The inclusion criteria were as follows: (1) patients aged
between 18 and 75 years with no sex predominance; (2)
pathologically confirmed rectal adenocarcinoma at clinical
stage II/III; (3) the lower margin of the tumor located at or
below the peritoneal reflection; (4) preoperative evaluation
showing no urinary dysfunction; and (5) clinical suspicion
of LLN metastasis based on magnetic resonance imaging
evaluation. Specifically, LLNs >7 mm in the short-axis di-
ameter before treatment were indicated for LLND, regard-
less of their response to neoadjuvant chemoradiation therapy
(nCRT).14
This study was approved by our local ethics committee
(LL-2020-SCI-001) and performed in accordance with the
FIG. 1. Laparoscopic LLND in ‘‘two fascial spaces’’ based
on membrane anatomy. LLND, lateral lymph node dissection.
WANG ET AL.
Helsinki Declaration.15 The trial was registered at the Chi-
nese Clinical Trial Registry (ChiCTR2200061531), and writ-
ten informed consent was obtained from all patients.
Key surgical procedure
The patient was placed in a modified lithotomy position
under general anesthesia, and a five-trocar placement was
utilized. LLND is performed following TME, with the choice
of unilateral or bilateral LLND depending on the location of
enlarged LLNs.
According to the theory of ‘‘four fasciae and three spaces,’’
the middle and lateral spaces formed by the urogenital fas-
cia, vesicohypogastric fascia, and parietal fascia constitute
the dissection plane for LLND.12,13 We proposed a fascia-to-
space surgical approach to perform LLND (Fig. 1), and key
surgical procedures were as follows:
Step 1: Separation of the urogenital fascia to expose the
medial surface of the middle space. The urogenital fascia
(i.e., visceral fascia) presents as a sandwich-like fascia sheath
and extends posterolaterally to the rectum, containing the
hypogastric nerves (HGNs), ureters, and genital vessels.
Given the close anatomic relationship between the urogenital
fascia and neural structures, separation of urogenital fascia
actually covers the exposure of HGNs, pelvic plexus, and
ureters.
Specifically, the separation of urogenital fascia extends
anteriorly to the level of the vas deferens (male) or the round
ligament of the uterus (female) and deeply into the exposure
of the internal iliac vein (Fig. 2).
Step 2: Separation of the obturator fascia to expose the
lateral surface of the lateral space. The obturator fascia is the
part of the parietal fascia covering the obturator muscle and
its separation is performed along the external iliac vessels.
This process allows removal of external iliac lymph nodes
(#293), common iliac lymph nodes (#273), and abdominal
aortic bifurcation lymph nodes (#280).
During the #293 dissection, special attention should be
paid to protection of the genitofemoral nerve, which runs
along the inner edge of the psoas major muscle and divides
into genital and femoral branches before entering the internal
inguinal ring (Fig. 3).
FIG. 2. Separation of the urogenital fascia to expose the
medial surface of the middle space.
 LAPAROSCOPIC LLND FOR LOWER RECTAL CANCER
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FIG. 3. Separation of the obturator fascia to expose the
lateral surface of the lateral space.
Step 3: Separation of the vesicohypogastric fascia to ex-
pose the medial surface of the lateral space. The vesicohy-
pogastric fascia is a triangle-shaped fascia bounded by the
umbilical artery, the tendinous arch of the pelvic fascia, and
the bladder sidewall. The urogenital fascia and vesicohypo-
gastric fasciae blend with each other in the tendinous arch of
the pelvic fascia and present as a ‘‘V’’ shape.
The umbilical artery is the first branch of the internal iliac
artery and is an important anatomical landmark for separation
of the vesicohypogastric fascia. The separation is performed
along the lateral side of the branches of the internal iliac
vessels until the bladder sidewall is reached (Fig. 4).
Step 4: Lymph node dissection in the lateral space. Ac-
cording to the principle of membrane anatomy, space dis-
section is performed following the establishment of fascia
planes. The lateral space lies between the vesicohypogastric
fascia and parietal fascia and is where the obturator lymph
nodes (#283) are located. In addition to #283, removal of
lateral sacral lymph nodes (#260) can also be done in this
space.
Due to establishment of the vesicohypogastric fascia
plane, the lateral space mostly contains not only the neural
structures but also the obturator artery and vein. Therefore,
space dissection mainly includes three steps: proximal and
distal ligation of obturator vessels, release of the obturator
nerve, and exposure of the sacral plexus.
Step 5: Lymph node dissection in the middle space. The
middle space is located between the urogenital fascia and
vesicohypogastric fascia. The anterior trunks of internal iliac
vessels and most of their branches run in this space, including
the uterine artery, middle rectal artery, and superficial and
deep uterine veins. Therefore, the middle space dissection
is actually dissection of internal iliac vessels. To completely
remove the internal iliac lymph nodes (#263) and median
sacral lymph nodes (#270) in this space, the vesicohypo-
gastric fascia is dissected during this process.
Data collection and follow-up
Clinical data were prospectively documented from pa-
tients’ medical records, including demographic character-
istics (age, sex, and body–mass index [BMI]), pathological
features (tumor stage, number of LLNs, and resection
499
FIG. 4. Separation of the vesicohypogastric fascia to ex-
pose the medial surface of the lateral space.
margin), and perioperative variables (operating time, blood
loss, length of hospital stay, and postoperative complications).
Tumor was staged according to the eighth edition of
the American Joint Committee on Cancer (AJCC) Manual
for Staging of Cancer. Complications were defined as any
deviation from the normal postoperative course occurring
within 30 days of surgery and graded according to the
Clavien-Dindo (CD) classification.16
All patients underwent regular follow-up evaluation for
at least 18 months after surgery to assess for tumor recur-
rence, including physical examination, serum tumor markers,
chest X-ray, abdominopelvic computed tomography scan,
and colonoscopy. In addition, urinary function was evaluated
by measurement of residual urine volume preoperatively and
7–14 days postoperatively. The residual urine volume was
generally measured by catheterization or ultrasound, and
values >50 mL were considered as urinary dysfunction.17
Results
Patient characteristics and perioperative outcomes
A total of 23 (17 males and 6 females) patients with lower
rectal cancer were included in this study, with a mean age of
59 – 6.8 years. The BMI was 25.2 – 1.4 and 21.4 – 0.6 in
males and females, respectively. Of these, 9 patients received
neoadjuvant chemoradiation therapy before surgery and 6 of
them (66.7%) had a reduction in LLN size after treatment.
The 3D laparoscopic TME plus LLND was successfully
performed in all patients without conversion to laparotomy,
including 21 cases of unilateral and 2 cases of bilateral
LLND.
The mean operating time and blood loss for LLND were
172 – 47 minutes and 85 – 22 mL, respectively. The mean
postoperative hospital stay was 10 – 3.6 days, and there were
no perioperative deaths.
Postoperative complications
The overall postoperative complication rate was 17.4%
(5/23), including a case of small bowel obstruction
(CD grade II), a case of lymph leakage (CD grade II), a case of
urinary dysfunction (CD grade II), and a case of lower limb
pain (CD grade I). These patients recovered after conservative
treatment without surgical intervention.
 500 WANG ET AL.

It was noted that all patients had no obvious urinary

dysfunction preoperatively, with a median residual urine
volume of <50 mL, and the urinary catheter was generally
removed on the fourth postoperative day after bladder exer-
cise. However, 1 (4.3%) patient suffered from urinary reten-
tion with postvoid residual urine volume of 220 mL and
intermittent catheterization was performed for one more week.

Oncologic outcomes
Postoperative pathology showed that 8 cases were at stage
II and 15 cases were at stage III. The resection margins were
all negative, and a minimum distance of 1 cm distally was
maintained. The median number of harvested mesenteric
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lymph nodes and LLNs was 13 (range 11–18) and 9 (range 6–

12), respectively. LLN metastases were present in 7 (30.4%)
patients, and all positive LLNs were internal iliac lymph FIG. 5. The internal iliac vessels and most of their bran-
nodes (#263) and/or obturator lymph nodes (#283). Among ches run in the middle space.
them, 6 patients had both mesenteric lymph nodes and LLN
metastases, and 1 had only LLN metastases.
During the median follow-up period of 26.5 months (range ternal iliac artery have certain distinguishing characteristics
18–36 months), 2 (8.7%) patients developed liver metastases (Fig. 5). The umbilical artery is the first branch of the internal
and received further treatment, but no anastomotic recurrence iliac artery and often shares a common trunk with the supe-
or regional lymph node metastasis was observed. rior vesical artery, with a constant anatomical location. The
vessels crossing above and below the ureter are the uterine
Discussion artery and deep uterine vein, respectively. The vesical veins
mainly course laterally along the bladder, uterus, or vagina in
The Japanese Guidelines for the Treatment of Colorectal
Cancer in 2019 stated that for patients with T3–T4 lower a sagittal plane.
rectal cancer, LLND can enhance local control and reduce Both the inferior gluteal artery and internal pudendal ar-
distant spread, leading to an improved 5-year overall survival tery enter the lesser sciatic foramen eventually, and the latter
rate.18 However, because of the complicated procedure and is also called the terminal branch of the internal iliac artery.
high complication rate, LLND has so far not been widely The inferior vesical artery is the site where the internal iliac
used in clinical practice.6,19 Therefore, establishment of a lymph nodes are prone to metastasis. It is the last branch of
simple, safe, and reproducible surgical procedure is key to the internal iliac artery and located above the infra-piriformis
popularizing its application. foramen and is therefore deemed as the distal end of vessel
According to the Japanese Classification of Colorectal dissection.
Cancer (Version 9), the extent of LLNs was sorted as iliac In addition, it is very important to accurately locate the
artery series and numbered as #263, #273, #283, #293, #260, internal iliac vein in LLND as its bleeding can be tricky. After
#270, and #280.20 Clinical studies have demonstrated that extensive cadaveric dissection and surgical observation, we
LLN metastases are mainly confined to the internal iliac determined that the internal iliac vein was located between
lymph nodes (#263) and obturator lymph nodes (#283), and the inferior gluteal artery and the internal pudendal artery
the incidence of metastasis in other sites was only 7.7%,19 (Fig. 6), which can act as a useful anatomical landmark in
which was also confirmed in our study. surgery.13
On the basis of the theory of ‘‘four fasciae and three
spaces,’’ we proposed a fascia-to-space surgical approach to
perform LLND.12 Specifically, we first dissect the urogenital
fascia, vesicohypogastric fascia, and parietal fascia to build
the fascial planes and develop fascial spaces, and this process
allows the removal of #293, #273, and #280. Then, we per-
form space dissection to remove #263 and #270 in the middle
space and #283 and #260 in the lateral space.13
Thereby, our proposed surgical procedure can successfully
finish the LD2 or LD3 dissection according to the LLN status
recommended by the Japanese Society for Cancer of the
Colon and Rectum ( JSCCR) guidelines.21 Our preliminary
experience showed that it significantly improved surgical
safety while ensuring oncologic outcomes, with the advan-
tages of easy identification of the surgical plane and clear
location of nerves and vessels.
The middle space corresponds to the Latzko’s pararectal
space22 in the traditional anatomy. The contents of this FIG. 6. The internal iliac vein lies between the inferior
space are mainly blood vessels, and the branches of the in- gluteal artery and the internal pudendal artery.
 LAPAROSCOPIC LLND FOR LOWER RECTAL CANCER
The lateral space corresponds to the paravesical space23 in
the traditional anatomy and mainly contains neural structures
(including the lumbosacral trunk, sciatic plexus, obturator
nerve, and sciatic nerve) in addition to the obturator vessels.
The lateral space dissection can begin with cleaning of superior
inguinal lymph nodes, which although not included in LLND,
is conducive to exposure of the obturator nerve and vessels.
When ligating the distal end of the obturator vessel, special
attention should be paid to the lateral corona mortis (also
known as crown of death) and medial vesical veins to avoid
accidental bleeding. The sacral plexus is located ventrally to
the piriformis muscle and covered with the parietal fascia
(i.e., piriformis fascia).
The sacral plexus constitutes the dorsal boundary of ob-
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turator lymph node dissection in the lateral space. In addition,
the dorsal penile nerve emanates from the pudendal nerve, the
branches of the sacral plexus. As a result, it is another key
structure that needs to be identified and adequately protected
in LLND.
Our anatomical study showed that the sacral plexus was
usually located below the origin of the obturator artery from
the internal iliac artery (Fig. 6).
Conclusions
In conclusion, our short-term outcomes showed that lap-
aroscopic LLND based on membrane anatomy is a safe and
effective procedure for treatment of locally advanced lower
rectal cancer. This technique is feasible and reproducible and
thus worthy of clinical promotion.
However, further studies with larger sample sizes and lon-
gitudinal follow-up are still needed to strengthen the promising
evidence.
Patient Consent
All study participants, or their legal guardians, provided
informed written consent before study enrollment.
Ethical Approval
This study was reviewed and approved by the Yangpu
Hospital Institutional Review Board (LL-2020-SCI-001).
Disclosure Statement
No competing financial interests exist.
Funding Information
This work was supported by the National Natural Science
Foundation of China under grant 81874201; Shanghai Pu-
jiang Program under grant 21PJD066; Science and Tech-
nology Commission of Shanghai Municipality under grant
20Y11908300; and Shanghai Municipal Health Commission
under grant 202040122.
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