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METHODS
published: 15 April 2022
doi: 10.3389/fsurg.2022.863078
Frontiers in Surgery | www.frontiersin.org 1April 2022 | Volume 9 | Article 863078
Edited by:
Stefano Cianci,
University of Messina, Italy
Reviewed by:
Carmine Conte,
Agostino Gemelli University Polyclinic
(IRCCS), Italy
Nicolò Bizzarri,
Agostino Gemelli University Polyclinic
(IRCCS), Italy
*Correspondence:
Ying Zheng
zhy_chd@126.com
Specialty section:
This article was submitted to
Obstetrics and Gynecological Surgery,
a section of the journal
Frontiers in Surgery
Received: 26 January 2022
Accepted: 07 March 2022
Published: 15 April 2022
Citation:
Peng S, Zheng Y, Yang F, Wang K,
Chen S and Wang Y (2022) The
Transumbilical Laparoendoscopic
Single-Site Extraperitoneal Approach
for Pelvic and Para-Aortic
Lymphadenectomy: A Technique Note
and Feasibility Study.
Front. Surg. 9:863078.
doi: 10.3389/fsurg.2022.863078
The Transumbilical
Laparoendoscopic Single-Site
Extraperitoneal Approach for Pelvic
and Para-Aortic Lymphadenectomy:
A Technique Note and Feasibility
Study
Shiyi Peng 1,2 , Ying Zheng 1,2
*, Fan Yang1, 2, Kana Wang 1,2 , Sijing Chen 1,2 and Yawen Wang 3
1Department of Gynecology, West China Second Hospital, Sichuan University, Chengdu, China, 2Key Laboratory of
Obstetrics, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second Hospital,
Sichuan University, Chengdu, China, 3Department of Obstetrics and Gynecology, Shanxi Bethune Hospital, Taiyuan, China
Background: Nowadays, lymphadenectomy could be performed by the transperitoneal
or extraperitoneal approach. Nevertheless, each approach has its own advantages
and disadvantages. Under these circumstances, we developed a transumbilical
laparoendoscopic single-site (TU-LESS) extraperitoneal approach for lymphadenectomy.
In this research, the primary goal is to demonstrate the feasibility of the novel approach
in systematic lymphadenectomy and present the surgical process step-by-step.
Methods: Between May 2020 and June 2021, patients who had the indications
of systematic lymphadenectomy underwent lymphadenectomy via the TU-LESS
extraperitoneal approach. This new approach was described in detail, and the clinical
characteristics and surgical outcomes were collected and analyzed.
Results: Eight patients with gynecological carcinoma were included in the research,
including four with high-risk endometrial cancer and four with early-stage ovarian cancer.
The TU-LESS extraperitoneal approach for pelvic and para-aortic lymphadenectomy
was successfully performed in all patients without conversion. In all, a median of 26.5
pelvic lymph nodes (range 18–35) and 18.0 para-aortic lymph nodes (range 7–43) were
retrieved. There was a median of 166.5 min of surgical time (range 123–205). Patients
had speedy recoveries without complications. All patients had positive pain responses
after surgery, as well as satisfactory cosmetic and body image outcomes.
Conclusion: Our initial experience showed that it is feasible to perform systematic
lymphadenectomy with the TU-LESS extraperitoneal approach. And this new approach
may provide a new measure or a beneficial supplement for lymphadenectomy in
gynecologic cancer.
Keywords: extraperitoneal approach, pelvic lymphadenectomy, para-aortic lymphadenectomy, laparoendoscopic
single-site (LESS) surgery, ovarian cancer, endometrial cancer
Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
INTRODUCTION
Lymphadenectomy is paramount for precise staging and
tailoring treatment of gynecological malignancies. Compared
to laparotomy, laparoscopic surgery caused less surgical
trauma and fewer wound complications. The feasibility and
safety of minimally invasive surgery for lymphadenectomy
has been well-investigated and proved (1,2). Currently,
laparoscopic lymphadenectomy is performed either trans- or
extraperitoneally. Dissection of the pelvic lymph nodes (LNs) is
easier with the transperitoneal approach; however, the intestinal
disruption is a major barrier for para-aortic lymphadenectomy
(PALN) (Figure 1). The extraperitoneal approach has been
described as a solution to resolve this problem. Without the
interference of bowels, the extraperitoneal approach provides an
easier access to the infrarenal para-aortic LNs with lower risk of
intestinal and urinary injuries (3). The full exposure of surgical
field achieved a higher para-aortic LN yield compared to the
transperitoneal route (4,5).
Laparoendoscopic single-site (LESS) surgery has emerged as
a minimal invasive surgical approach, which could further
minimize the surgical trauma compared to multi-port
laparoscopy surgery (6). LESS is as safe and effective as the
traditional laparoscopy in the gynecologic surgery (7). Compared
to patients in the multi-port laparoscopy group, patients in the
single-port laparoscopy group attained mild pain with less
analgesic consumption and shorter hospital stay (8–11). The
single-port left iliac extraperitoneal PALN was first described by
Guoy et al. (12). Subsequently, Lambaudie et al. (13) and Beytout
et al. (14) introduced similar single-port lateral approaches.
These results indicated that the number of para-aortic LNs
retrieved by the single-port lateral extraperitoneal approach
was compatible with that of the multi-port extraperitoneal
route (3,10,13). In spite of this, the most common lateral
extraperitoneal technique restraints access to the obturator
fossa which impedes pelvic lymphadenectomy (PLN) (15)
(Figure 2). Under these circumstances, PLN and other staging
procedures sometimes need extra incisions, which increases
the amount of trauma experienced throughout the operation.
Thus, the TU-LESS extraperitoneal approach, which combines
the strengths of LESS with that of extraperitoneal approach was
developed to achieve PLN and PALN in a minimal invasive way.
This study aims to describe the details of surgical procedures
and present our preliminary experience with the TU-LESS
extraperitoneal approach for PLN and PALN in order to further
evaluate its feasibility.
METHODS
Patients
This study included eight patients from May 2020 to June 2021.
Patients who had indications of systematic lymphadenectomy
and were candidates for LESS surgery were eligible for
inclusion. Clinical data were collected, including demographics,
pathological features, and perioperative outcomes of patients
who had the surgery. The study was approved by the
institutional review board of the West China Second Hospital,
Sichuan University, and all participants provided their written
informed consent to participate in this study. The duration of
lymphadenectomy time was defined as the interval from the first
incision of skin to completion of lymphadenectomy, excluding
subsequent procedures such as hysterectomy. The failure of
the TU-LESS extraperitoneal approach was defined as the
conversion to a transperitoneal approach via laparoscopy or open
surgery; and intraoperative complications included peritoneal
rupture and damage to intestines, bladder, ureters, nerves, or
blood vessels. Postoperative complications included any adverse
event that occurred within 30 days after surgery, including
lymphocysts, thrombosis, infection, and chyle leakage. Visual
analog scoring was used to assess the degree of postoperative
pain of umbilical incision 24 h after surgery in the range of 0–
10, 0 for no pain, 1–3 for mild pain, 4–6 for moderate pain,
and 7–10 for severe pain (16). The body image questionnaire
(BIQ) was administered 7 and 30 days after the surgery to
assess patient satisfaction with the surgical intervention (17). The
BIQ consists of two subscales: body image scale and cosmetic
scale (Supplementary Data Sheet 1). With a score from 5 to 20,
the body image scale measures perception of patients and their
attitude to physical condition. The cosmetic scale evaluates the
satisfaction of patients to their umbilical scars with a score from
3 to 24. The higher the score, the more satisfied the patient was
with body image and cosmetic effect.
Lymphadenectomy Indications
Dissection of LNs should be recommended for endometrial
cancer (EC) patients who are at high risk of recurrence, including
those with deep myometrial invasion, high-grade histology,
lymphatic vascular invasion, or type II tumors (2). For early-stage
EC, the biopsy of sentinel lymph node (SLN) has been proved
to be an accurate and effective alternative to lymphadenectomy.
However, the use of SLN in high-risk group is controversial,
lacking adequate high-level evidences to prove its safety. As a
result, systematic lymphadenectomy was nevertheless conducted
in this trial on individuals who were considered to be at high
risk. In addition, systematic lymphadenectomy was indicated in
patients with stage IA-IIA epithelial ovarian carcinoma (OC),
except for the mucinous type without suspicious LNs), including
those who wished to preserve fertility. Laparoscopy could be
employed for patients with early-stage OC by an experienced
surgeon (1).
Surgical Technique
All surgical procedures were performed by an experienced
gynecologic oncologist. The patient was placed in trendelenburg
position with the primary surgeon on the left and the assistant
on the opposite sides. First, the primary surgeon made a
2 cm umbilical incision and a multichannel single port (Kangji,
Hangzhou, China) was inserted into the intraperitoneal space
(Figure 3). Careful transperitoneal exploration was conducted to
exclude intra-abdominal carcinomatosis and collect peritoneal
washing for cytologic evaluation.
Second, we had to identify the posterior peritoneum above
the aortic bifurcation at first and execute a figure-of-eight suture
subsequently. The surgeon pulled the thread and the sutured
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
FIGURE 1 | The transperitoneal approach for PALN. (A) The placement of trocars. It was difficult to achieve adequate exposure of para-aortic regions for PALN
because of the interference of intestines (B,C). IVC: Inferior vena cava.
FIGURE 2 | The lateral extraperitoneal approach for lymphadenectomy. (A) The lateral incisions. (B) Para-aortic LN dissection. Bilateral obturator fossae were
challenging to reach when performing pelvic lymphadenectomy (C).
FIGURE 3 | (A) Make a 2-cm umbilical incision. (B) The multichannel single port (Kangji). (C) Set up the port into the intraperitoneal space.
posterior peritoneum was gently raised toward the umbilical
incision. Using a purse-string suture, the suspended posterior
peritoneum was held in place and marked. Afterwards, the center
portion of the suspended posterior peritoneum was gently sliced
open (Figure 4,Supplementary Video 1). The third step was
to separate the extraperitoneal soft tissues that attached to the
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
FIGURE 4 | (A) Make a figure-of-eight on the posterior peritoneum above the aortic bifurcation. (B) Raise the sutured posterior peritoneum to the umbilical incision.
(C) Cut open the suspended posterior peritoneum. (D) Reset the port into the retroperitoneal space.
FIGURE 5 | The establishment of the retroperitoneal space. IVC, inferior vena
cava.
anterior peritoneum with blunt-finger dissection in order to
expand the extraperitoneal space. Subsequently, the port was
repositioned into the retroperitoneal space with the purse-string
suture tightened and secured. The microvessels were coagulated
by a harmonic scalpel (HARMONIC, Ethicon, America), and
carbon dioxide was insufflated at the maximum pressure of 14–
20 mmHg to establish the retropneumoperitoneum (Figure 5,
Supplementary Video 1).
Procedures were carried out for systematic PLN that
included removal of the common iliac, external iliac,
internal iliac, obturator, and deep inguinal nodes (Figure 6,
Supplementary Video 1). During PALN operations, the surgeon
stood between the legs of the patient and the assistant on the
right. Para-aortic LNs were dissected from the aortic bifurcation
to the left renal vein (RV) (Figure 7,Supplementary Video 1).
All surgical specimens were taken out in bags in time to prevent
the spillage of tumor cells. And the surgeon sprayed the porcine
fibrin sealant kit (Bioseal, Guangzhou, China) onto the surgical
field to prevent lymphatic leakage and lymphocyst (18).
After the extraperitoneal surgery, the port was reset into
the intraperitoneal space for other transperitoneal procedures
(i.e., hysterectomy, omentectomy, or salpinx oophorectomy)
according to the different types of tumor.
RESULTS
Patient Information
A total of eight patients underwent lymphadenectomy via
the TU-LESS extraperitoneal approach. Half of patients were
suffering from high-risk EC (one dedifferentiated carcinoma, two
grade 3 serous carcinoma with deep myometrial infiltration, and
one clear cell carcinoma). The other four patients were diagnosed
with early-stage epithelial OC (two serous carcinoma, one clear
cell carcinoma, and one endometrioid carcinoma), and three
of them opted for fertility-sparing surgery (i.e., preservation of
the uterus and contralateral adnexa). The median age was 44
years (range 22–64), and the median BMI was 23.1 kg/m2(range
20.7–28.4). According to the Chinese criteria, two patients were
classified as obese (BMI =28.2 and 28.4 kg/m2) (19). In this
group, half had a history of abdominal surgery, and one even had
undergone four surgeries. The clinical characteristics of patients
are summarized in Table 1.
Surgical Outcomes
Table 2 displays the operative outcomes. The upper limit of
PALN for all patients was at the renal vascular level. The
median time of LN dissection was 166.5 min (range 123–205).
During the procedure, no intraoperative complications were
observed and no conversion to transperitoneal approach or
multiport laparoscopic surgery occurred. The median blood
loss was 100 ml (range 100–300) and no patient required
blood transfusion. Concerning the LN yields, the median
count of para-aortic LNs was 18 (range of 7–30), and the
retrieved pelvic LNs was 26.5 (range 18–35). Three EC patients
had positive LNs, two with pelvic nodal metastasis and one
with para-aortic nodal involvement. Furthermore, there was
no evidence of LN metastasis in OC patients. The median
flatus time was 23.0 h (range 16.0–38.0) and the median
hospital duration was 3 days (range of 2–4). All patients felt
mild pain for 24 h after surgery with a median score of 2
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
FIGURE 6 | Anatomical overview of pelvic area after PLN. (A) The aortic bifurcation and inferior vena cava. (B) The right obturator fossa. (C) The left obturator fossa.
(D) The view of presacral area.
FIGURE 7 | Anatomical overview of para-aortic area. (A) Lymphadenectomy up to the left renal vein. (B) The right para-aortic region. (C) Dissection of the
interaortocaval and retrocaval lymph nodes. (D) The infrarenal region after PALN.
(range 1–3). The median satisfaction value for body image
was 17 (range 16–19) 7 days after surgery and increased
to 19.5 (range 18–20) a month after surgery; while the
median score of cosmetic effects was 18 (range 15–19) 1 week
after surgery and improved to 22.5 (range 21–23) after 30
days (Figure 8).
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
TABLE 1 | Patient characteristics.
Case Age, y BMI, kg/m2Histologic type FIGO staging Number of previous
abdominal surgeries
Conversion
1 48 21.0 Dedifferentiated EC IIIC 0 N
2 54 23.0 Serous EC IB 0 N
3 29 28.2 Serous OC IC 1 N
4 50 26.0 Serous EC IB 1 N
5 22 22.5 Endometrioid OC IA 1 N
6 64 28.4 Clear cell EC IIIC 0 N
7 40 20.7 Serous OC IA 4 N
8 28 23.1 Clear cell OC IC 0 N
TABLE 2 | Surgical and postoperative information.
Case Operative
time, min
Aortic
dissection
level
Para-
aortic
LNs, n
Pelvic
LNs, n
Blood
loss, ml
Complications Flatus
time, h
Postoperative
pain score,
24 h
Body image
scale (range
5–20) 7/30
days
Cosmetic
scale (range
3–24), 7/30
days
Hospital
duration,
days
1 205 Infrarenal 14 33 100 N 38 2 16/18 18/22 4
2 173 Infrarenal 43 18 100 N 21 2 17/20 17/23 2
3 163 Infrarenal 12 35 200 N 22 2 18/20 19/23 3
4 165 Infrarenal 19 27 100 N 18 1 19/20 17/23 4
5 175 Infrarenal 30 20 300 N 16 3 16/19 15/22 4
6 168 Infrarenal 17 23 100 N 27 1 16/20 18/22 3
7 158 Infrarenal 21 28 200 N 24 2 17/19 19/21 2
8 123 Infrarenal 7 26 100 N 26 2 18/19 18/23 3
Median 166.5 / 18.0 26.5 100 / 23 2 17/19.5 18/22.5 3
DISCUSSION
Lymph node status evaluation is a critical component of
thorough surgical staging for ovarian and EC (20–22).
Laparoscopic lymphadenectomy has been proven safe for
surgical staging in EC and early-stage OC patients with less
complications and faster recovery (1,2,23). Previous studies
have shown that extraperitoneal lymphadenectomy is superior
to the transperitoneal approach for PALN, because it could
avoid intestinal interference and allow an easier access to
supramesenteric LNs (5,24,25). We initially attempted to
employ the TU-LESS extraperitoneal approach in the surgical
staging procedures for a patient with advanced cervical cancer in
order to accurately delineate the radiographic field. The PALN
and right enlarged obturator LN biopsy were performed easily
via this novel technique (26). Further exploration and practice of
this technique were conducted, and the primary findings of our
study confirmed that the TU-LESS extraperitoneal approach is
feasible for systematic PLN and PALN.
Compared to the node counts of laparoscopic transperitoneal
procedure (range 14–22) (11,13,27–29), our method yielded
a comparable number of pelvic LNs. The median count of
para-aortic LNs (18, range 7–30) in our investigation was
equivalent to that of the largest case series of single-port lateral
extraperitoneal approach reported by Guoy (median 18, range
2–47) (3), but was higher than that of left-sided extraperitoneal
approach using multiport laparoscopy (range 9.5–15) (3,5,
14,30). Despite the left extraperitoneal approach being viable
for completing the aortic nodal dissection, Dargent asserted
that the number of right-sided aortic sampling had reduced
compared to bilateral extraperitoneal approach (p<0.01) (31).
Furthermore, being limited in access to the deep obturator
fossae was one of major technical difficulties of the left-sided
approach, which was mainly due to the poor angle of view
(13,15,32) (as Figure 2C shows). Some technique modifications
were made to overcome this difficulty, such as addition of
different incisions. Querleu added two incisions on the basis
of the left-sided extraperitoneal approach in order to achieve
obturator node sampling for patients with locally advanced
cervical cancer (32). However, whether this technique could
be applied in systematic PLN remains to be verified, and the
authors further noted that right obturator fossa was obviously
difficult to reach with this technique. Other methods for pelvic
LN dissection were also reported, such as combining a right
extraperitoneal approach (33). Nonetheless, these modifications
would increase surgical trauma, and there were few studies
that investigated the feasibility for systematic PLN. One of the
greatest merits of the TU-LESS extraperitoneal approach is that
it allows equal access to the bilateral pelvic and para-aortic areas
through the same extraperitoneal approach because the umbilical
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
FIGURE 8 | The umbilical incisions of the TU-LESS extraperitoneal approach. (A) The preoperative appearance. (B) The postoperative appearance. (C) The
appearance 3 months after surgery.
incision is centrally located, which facilitates the obturator and
infrarenal LN dissection (Figures 6,7). Additionally, careful
contrast of Figures 2C,6,7showed that the anatomic angles
during the lateral extraperitoneal procedures were altered, adding
to identification complexity for surgeons. However, surgeons did
not need to readapt to the changing anatomic angles with the TU-
LESS extraperitoneal approach, since the angle of view was the
same as the transperitoneal approach or laparotomy which many
surgeons have been accustomed to.
Reducing intraperitoneal adhesion is another significant
advantage of the extraperitoneal approach. Occelli et al.
compared the adhesion rate of laparoscopic transperitoneal vs.
extraperitoneal PALN on pigs. The results showed that the
extraperitoneal group had a lower adhesion formation rate than
the transperitoneal group (p=0.04) (15). Abdominal adhesion
is likely to increase the morbidity associated with radiotherapy
and may result in adnexal adhesion or even infertility (34,35).
The TU-LESS extraperitoneal approach also theoretically has
this advantage, because it could minimize peritoneal injury and
leave the peritoneal cavity intact after surgery. For these reasons,
in our research, the TU-LESS extraperitoneal approach was
considered to be an optimal treatment for young patients who
wish to preserve their fertility. Three patients with epithelial OC
received the fertility preservation surgery. All of them completed
the comprehensive assessment of LNs and dissected lesions
with little peritoneal damage. While peritoneal cavity could
remain intact with our technique, however, the fertility outcomes
ought to be followed. Additionally, patients who underwent
abdominal surgeries might potentially benefit from the TU-
LESS extraperitoneal approach since it avoids adhesiolysis, and
thus it could reduce the risk of intra-abdominal organ injury.
In our analysis, half of the patients had surgical history, and
none of them had intraperitoneal complications. To sum up,
different approaches for lymphadenectomy have their own
strengths and limitations; and the concerned summarization
from our current exploration and prior studies are presented
in Table 3.
In previous studies, the lymphadenectomy time of the lateral
extraperitoneal approach was varied (range 125–339.5 min)
(3,25,30,36). The time required for lymphadenectomy
TABLE 3 | Advantages and limitations of three approaches for lymphadenectomy.
Transperitoneal
approach
Lateral
extraperitoneal
approach
TU-LESS
extraperitoneal
approach
(current work)
PLN Easy Difficult Easy
PALN(RV
level)
Difficult Easy Easy
Risk of
abdominal
adhesion
Increase Decrease Decrease
Changes in
anatomic
recognition
No change Change No change
Surgical
trauma
Small Small Minimal
RV, renal vein.
in this study was in concordance with the prior findings,
but it was less than the time of early practice of the single-
port extraperitoneal approach for PALN (average 240 min,
range 180–270 min) described by Guoy et al. (37). However,
our lymphadenectomy time was somewhat longer than the
single-port transperitoneal approach for PLN and PALN
(range 60–185 min) (13), which might be explained by the
extra time needed to establish the retropneumoperitoneum.
The operation time may decrease when the learning
curve climbs.
In our research, there were no complications during or
after surgery, nor was there a conversion to the transperitoneal
route. The procedural failure of the extraperitoneal approach
was attributed to the peritoneal rupture (38). Peritoneal rupture
occurred in seven patients (16%) during the lateral single-
port extraperitoneal lymphadenectomy according to Beytout
(14). Neither a peritoneal rupture nor any other technical
problems have ever caused abortion of extraperitoneal operation
in our series.
Additionally, some studies indicated that the extraperitoneal
approach may be an optimal option for patients with a high
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Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
BMI. Dowdy et al. (39) and Pakish et al. (25) confirmed that
patients with BMI >35 kg/m2, who had extraperitoneal PALN,
harvested more para-aortic nodes than those who underwent
abdominal or transperitoneal PALN. BMI had no effect on the
duration of surgery, and the area of visceral adipose tissues did
not affect the extraperitoneal approach of PALN (40). According
to earlier studies, the maximum BMI of patients who underwent
the extraperitoneal lymphadenectomy was ranging from 31 to 40
kg/m2(1,3,9,11,20). Nonetheless, we successfully performed the
TU-LESS extraperitoneal technique on two obese patients who
satisfied Chinese diagnostic criteria (BMI ≥28 kg/m2). However,
since this was a primary exploration with a limited number
of patients, we did not try to use this measure for systematic
lymphadenectomy in patients with BMI more than 30 kg/m2. We
were exploring an easier method for establishing extraperitoneal
space in obese patients. The feasibility and safety of robotic
technology for lymphadenectomy in gynecologic cancer have
been validated, with the benefits of a three-dimensional vision,
scaled movement, and short learning curves (41). Gallotta
demonstrated that the robotic technology is conducive for PALN.
The results showed that aortic LN yields were comparable
when patients with BMI >30 kg/m2were compared with those
with BMI <30 kg/m2(42).The robotic surgery was likely to
be a preferable approach for obese patients, and the node
counts were not affected by increasing BMI (43). Combining
robotic technology and the TU-LESS extraperitoneal approach
for lymphadenectomy may provide a potential and feasible
option for obese patients. Robotic technology may facilitate in
shortening the learning curve of the TU- LESS extraperitoneal
approach and implementing it.
CONCLUSION
In conclusion, the TU-LESS extraperitoneal approach for pelvic
and PALN is feasible with a practical application. It significantly
improves the exposure and visualization for PLN and PALN,
while causing minimal surgical trauma. Depending on the
results of our study, this innovative approach may become an
effictive alternative measure to the transperitoneal and lateral
extraperitoneal approach. However, further studies are required
to compare the surgical outcomes like LN yields, surgical trauma,
cosmesis, and other index among three approaches. Additionally,
based on the current research, a long-term clinical application on
a larger sample would be required to evaluate the effects in a more
objective manner.
DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included
in the article/Supplementary Material, further inquiries can be
directed to the corresponding author.
ETHICS STATEMENT
The studies involving human participants were reviewed
and approved by the Medical Institutional Review Board
of West China Second Hospital of Sichuan University. The
patients/participants provided their written informed consent to
participate in this study. Written informed consent was obtained
from the individual(s) for the publication of any potentially
identifiable images or data included in this article.
AUTHOR CONTRIBUTIONS
SP contributed to writing the manuscript and drawing pictures.
YZ designed the study and revised the manuscript. FY and KW
analyzed and interpreted the data. SC and YW made the video
and collected the data. All authors contributed to the manuscript
and approved the final manuscript.
FUNDING
This work was supported by the Science and Technology
Program of Sichuan, China (2020YFS0049), and the Chengdu
Science and Technology Bureau (2019-YF05-00473-SN).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fsurg.
2022.863078/full#supplementary-material
Supplementary Video 1 | The TU-LESS extraperitoneal approach for
systematic lymphadenectomy.
Supplementary Data Sheet 1 | The Body Image Questionnaire (BIQ).
REFERENCES
1. Armstrong DK, Alvarez RD, Bakkum-Gamez JN, Barroilhet L, Behbakht
K, Berchuck A, et al. Ovarian cancer, version 2.2020, Nccn clinical
practice guidelines in oncology. J Natl Compr Canc Netw. (2021) 19:191–
226. doi: 10.6004/jnccn.2021.0007
2. Abu-Rustum NR, Yashar CM, Bradley K, Campos SM, Chino J,Chon HS, et al.
Nccn guidelines R
insights: uterine neoplasms, version 3.2021. J Natl Compr
Canc Netw. (2021) 19:888–95. doi: 10.6004/jnccn.2021.0038
3. Gouy S, Uzan C, Scherier S, Gauthier T, Bentivegna E, Kane A, et al.
Single-port laparoscopy and extraperitoneal para-aortic lymphadenectomy
for locally advanced cervical cancer: assessment after 52 consecutive patients.
Surg Endosc. (2014) 28:249–56. doi: 10.1007/s00464-013-3180-4
4. Díaz-Feijoo B, Bebia V, Hernández A, Gilabert-Estalles J,
Franco-Camps S, de la Torre J, et al. Surgical complications
comparing extraperitoneal vs transperitoneal laparoscopic
aortic staging in early stage ovarian and endometrial cancer.
Gynecol Oncol. (2021) 160:83–90. doi: 10.1016/j.ygyno.2020.
10.038
5. Zhang W, Xia L, Han X, Ju X, Wu X, Chen X. Extraperitoneal
laparoscopy for para-aortic lymphadenectomy in endometrial carcinoma
staging: an approach with higher efficiency. World J Surg Oncol. (2021)
19:323. doi: 10.1186/s12957-021-02416-x
6. Spana G, Rane A, Kaouk JH. Is robotics the future of
laparoendoscopic single-site surgery (less)? BJU Int. (2011)
108:1018–23. doi: 10.1111/j.1464-410X.2011.10513.x
Frontiers in Surgery | www.frontiersin.org 8April 2022 | Volume 9 | Article 863078
Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
7. Song T, Kim ML, Jung YW, Yoon BS, Joo WD, Seong SJ.
Laparoendoscopic single-site versus conventional laparoscopic
gynecologic surgery: a metaanalysis of randomized controlled trials.
Am J Obstet Gynecol. (2013) 209:317.e1–9. doi: 10.1016/j.ajog.2013.
07.004
8. Michener CM, Lampert E, Yao M, Harnegie MP, Chalif J, Chambers
LM. Meta-analysis of laparoendoscopic single-site and vaginal natural
orifice transluminal endoscopic hysterectomy compared with multiport
hysterectomy: real benefits or diminishing returns? J Minim Invasive Gynecol.
(2021) 28:698–709.e1. doi: 10.1016/j.jmig.2020.11.029
9. Yuan JB, Chen MF, Qi L, Li Y, Li YL, Chen C, et al. Preservation
of the saphenous vein during laparoendoscopic single-site inguinal
lymphadenectomy: comparison with the conventional laparoscopic
technique. BJU Int. (2015) 115:613–8. doi: 10.1111/bju.12838
10. Hudry D, Cannone F, Houvenaeghel G, Buttarelli M, Jauffret C, Chéreau E,
et al. Comparison of single-port laparoscopy and conventional laparoscopy
for extraperitoneal para-aortic lymphadenectomy. Surg Endosc. (2013)
27:4319–24. doi: 10.1007/s00464-013-3051-z
11. Fagotti A, Boruta DM, 2nd, Scambia G, Fanfani F, Paglia A, Escobar PF.
First 100 early endometrial cancer cases treated with laparoendoscopic single-
site surgery: a multicentric retrospective study. Am J Obstet Gynecol. (2012)
206:353.e1–6. doi: 10.1016/j.ajog.2012.01.031
12. Gouy S, Uzan C, Kane A, Gauthier T, Morice P. Single-port laparoscopy
and extraperitoneal para-aortic lymphadenectomy: 3 consecutive cases.
Int J Gynecol Cancer. (2011) 21:1695–7. doi: 10.1097/IGC.0b013e31822
a0175
13. Lambaudie E, Cannone F, Bannier M, Buttarelli M, Houvenaeghel G.
Laparoscopic extraperitoneal aortic dissection: does single-port surgery offer
the same possibilities as conventional laparoscopy? Surg Endosc. (2012)
26:1920–3. doi: 10.1007/s00464-011-2126-y
14. Beytout C, Laas E, Naoura I, Bendifallah S, Canlorbe G, Ballester M,
et al. Single-port extra- and transperitoneal approach for paraaortic
lymphadenectomy in gynecologic cancers: a propensity-adjusted analysis.
Ann Surg Oncol. (2016) 23:952–8. doi: 10.1245/s10434-015-4874-8
15. Occelli B, Narducci F, Lanvin D, Querleu D, Coste E, Castelain B,
et al. De novo adhesions with extraperitoneal endosurgical para-
aortic lymphadenectomy versus transperitoneal laparoscopic para-aortic
lymphadenectomy: a randomized experimental study. Am J Obstet Gynecol.
(2000) 183:529–33. doi: 10.1067/mob.2000.105736
16. Fagotti A, Bottoni C, Vizzielli G, Gueli Alletti S, Scambia G, Marana E,
et al. Postoperative pain after conventional laparoscopy and laparoendoscopic
single site surgery (less) for benign adnexal disease: a randomized trial. Fertil
Steril. (2011) 96:255–9.e2. doi: 10.1016/j.fertnstert.2011.04.006
17. Dunker MS, Stiggelbout AM, van Hogezand RA, Ringers J, Griffioen G,
Bemelman WA. Cosmesis and body image after laparoscopic-assisted and
open ileocolic resection for crohn’s disease. Surg Endosc. (1998) 12:1334–
40. doi: 10.1007/s004649900851
18. Gasparri ML, Ruscito I, Bolla D, Benedetti Panici P, Mueller MD, Papadia A.
The efficacy of fibrin sealant patches in reducing the incidence of lymphatic
morbidity after radical lymphadenectomy: a meta-analysis. Int J Gynecol
Cancer. (2017) 27:1283–92. doi: 10.1097/IGC.0000000000001051
19. Coorperative Meta analysis Group of China Obesity Task Force. Predictive
values of body mass index and waist circumference to risk factors of related
disease in Chinese adult population. Chin J Epidemiol. (2002) 1:10–5.
20. O’Hanlan KA, Sten MS, O’Holleran MS, Ford NN, Struck DM,
McCutcheon SP. Infrarenal lymphadenectomy for gynecological
malignancies: two laparoscopic approaches. Gynecol Oncol. (2015)
139:330–7. doi: 10.1016/j.ygyno.2015.09.019
21. Koo YJ, Kim JE, Kim YH, Hahn HS, Lee IH, Kim TJ, et al. Comparison
of laparoscopy and laparotomy for the management of early-stage ovarian
cancer: surgical and oncological outcomes. J Gynecol Oncol. (2014) 25:111–
7. doi: 10.3802/jgo.2014.25.2.111
22. Kong Q, Wei H, Zhang J, Li Y, Wang Y. Comparison of the survival
outcomes of laparoscopy versus laparotomy in treatment of early-stage
ovarian cancer: a systematic review and meta-analysis. J Ovarian Res. (2021)
14:45. doi: 10.1186/s13048-021-00793-1
23. Gallotta V, Petrillo M, Conte C, Vizzielli G, Fagotti A, Ferrandina G,
et al. laparoscopic versus laparotomic surgical staging for early-stage ovarian
cancer: a case-control study. J Minim Invasive Gynecol. (2016) 23:769–
74. doi: 10.1016/j.jmig.2016.03.006
24. Prodromidou A, Machairas N, Spartalis E, Kostakis ID, Iavazzo C, Moris D,
et al. Transperitoneal versus extraperitoneal laparoscopic lymphadenectomy
for gynecological malignancies: a systematic review and meta-analysis.
Anticancer Res. (2018) 38:4677–81. doi: 10.21873/anticanres.12773
25. Pakish J,Soliman PT, Frumovitz M, Westin SN, Schmeler KM, Reis RD, et al. A
Comparison of extraperitoneal versus transperitoneal laparoscopic or robotic
para-aortic lymphadenectomy for staging of endometrial carcinoma. Gynecol
Oncol. (2014) 132:366–71. doi: 10.1016/j.ygyno.2013.12.019
26. Chen S, Zhou J, Zheng Y, Wang K, Yang X. Para-aortic and right obturator
lymphadenectomy for surgical staging of advanced cervical cancer through
the tu-less extraperitoneal approach. J Minim Invasive Gynecol . 2021)
28:1140. doi: 10.1016/j.jmig.2020.12.014
27. Boruta DM, Fagotti A, Bradford LS, Escobar PF, Scambia G, Kushnir
CL, et al. Laparoendoscopic single-site radical hysterectomy with pelvic
lymphadenectomy: initial multi-institutional experience for treatment of
invasive cervical cancer. J Minim Invasive Gynecol. (2014) 21:394–
8. doi: 10.1016/j.jmig.2013.10.005
28. Paik ES, Baek SH, Kang JH, Jeong SY, Kim MS, Kim WY, et al. Comparison
of laparoscopy and laparotomy for para-aortic lymphadenectomy in women
with presumed stage i-ii high-risk endometrial cancer. Front Oncol. (2020)
10:451. doi: 10.3389/fonc.2020.00451
29. Larciprete G, Casalino B, Segatore MF, Jarvis S, Catarinella V, Cirese
E. Pelvic lymphadenectomy for cervical cancer: extraperitoneal versus
laparoscopic approach. Eur J Obstet Gynecol Reprod Biol. (2006) 126:259–
63. doi: 10.1016/j.ejogrb.2005.09.019
30. Iacoponi S, De Santiago J, Diestro MD, Hernandez A, Zapardiel I.
Single-port laparoscopic extraperitoneal para-aortic lymphadenectomy.
Int J Gynecol Cancer. (2013) 23:1712–6. doi: 10.1097/IGC.00000000000
00006
31. Dargent D, Ansquer Y, Mathevet P. Technical development and results of left
extraperitoneal laparoscopic paraaortic lymphadenectomy for cervical cancer.
Gynecol Oncol. (2000) 77:87–92. doi: 10.1006/gyno.1999.5585
32. Querleu D, Ferron G, Rafii A, Bouissou E, Delannes M, Mery E, et al. Pelvic
lymph node dissection via a lateral extraperitoneal approach: description of a
technique. Gynecol Oncol. (2008) 109:81–5. doi: 10.1016/j.ygyno.2007.12.031
33. Pan XY, Lin H, Wang YN, Zhao YW, Cheng JY, Sun AP.
Feasibility of laparoscopic extraperitoneal pelvic lymphadenectomy
in gynecologic malignancies. Gynecol Oncol. (2011) 122:281–
4. doi: 10.1016/j.ygyno.2011.04.048
34. Vergote I, Pouseele B, Van Gorp T, Vanacker B, Leunen K, Cadron I,
et al. Robotic retroperitoneal lower para-aortic lymphadenectomy in cervical
carcinoma: first report on the technique used in 5 patients. Acta Obstet Gynecol
Scand. (2008) 87:783–7. doi: 10.1080/00016340802146946
35. Mabuchi S, Kimura T. Extraperitoneal radical trachelectomy with
pelvic lymphadenectomy: a novel fertility-preserving option for
early stage cervical cancer patients. Int J Gynecol Cancer. (2017)
27:537–42. doi: 10.1097/IGC.0000000000000918
36. Schuman S, Lucci JA 3rd, Twiggs LB. Laparoendoscopic single-site
extraperitoneal aortic lymphadenectomy: first experience. J Laparoendosc Adv
Surg Tech A. (2011) 21:251–4. doi: 10.1089/lap.2010.0362
37. Gouy S, Uzan C, Kane A, Scherier S, Gauthier T, Bentivegna E, et al. A new
single-port approach to perform a transperitoneal step and an extraperitoneal
para-aortic lymphadenectomy with a single incision. J Am Coll Surg. (2012)
214:e25–30. doi: 10.1016/j.jamcollsurg.2012.02.012
38. Morales S, Zapardiel I, Grabowski JP, Hernandez A, Diestro MD,
Gonzalez-Benitez C, et al. Surgical outcome of extraperitoneal paraaortic
lymph node dissections compared with transperitoneal approach in
gynecologic cancer patients. J Minim Invasive Gynecol. (2013) 20:611–
5. doi: 10.1016/j.jmig.2013.03.009
39. Dowdy SC, Aletti G, Cliby WA, Podratz KC, Mariani A.
Extra-peritoneal laparoscopic para-aortic lymphadenectomy–a
prospective cohort study of 293 patients with endometrial cancer.
Gynecol Oncol. (2008) 111:418–24. doi: 10.1016/j.ygyno.2008.
08.021
40. Nakao K, Sasaki H, Nishimura T, Banno H, Otsuka K, Hirabuki S,
et al. Periaortic abdominal fat area as a predictor of surgical difficulties
Frontiers in Surgery | www.frontiersin.org 9April 2022 | Volume 9 | Article 863078
Peng et al. The TU-LESS Extraperitoneal Lymphadenectomy Approach
during extraperitoneal laparoscopic para-aortic lymphadenectomy. J
Minim Invasive Gynecol. (2020) 27:1377–82. doi: 10.1016/j.jmig.2019.
10.016
41. Gallotta V, Giudice MT, Conte C, Sarandeses AV, D’Indinosante
M, Federico A, et al. Minimally invasive salvage lymphadenectomy
in gynecological cancer patients: a single institution series.
Eur J Surg Oncol. (2018) 44:1568–72. doi: 10.1016/j.ejso.2018.
08.006
42. Gallotta V, Federico A, Gaballa K, D’Indinosante M, Conte C,
Giudice MT, et al. The role of robotic aortic lymphadenectomy in
gynecological cancer: surgical and oncological outcome in a single
institution experience. J Surg Oncol. (2019) 119:355–60. doi: 10.1002/jso.
25335
43. Cunningham MJ, Dorzin E, Nguyen L, Anderson E, Bunn
WD Jr. Body mass index, conversion rate and complications
among patients undergoing robotic surgery for endometrial
carcinoma. J Robot Surg. (2015) 9:339–45. doi: 10.1007/s11701-015-0
538-8
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