Improvements and challenges in intraperitoneal laparoscopic para‐aortic lymphadenectomy: The novel “tent‐pitching” antegrade approach and vascular anatomical variations in the para‐aortic region

Abstract

Introduction

This study introduces and compares a new intraperitoneal laparoscopic para‐aortic lymphadenectomy method to reach the level of the renal vein, the “tent‐pitching” antegrade approach with the retrograde approach in gynecological malignancy surgeries in terms of success rate, complication incidence, and the number of lymph nodes removed. It focuses on the feasibility, safety, and effectiveness. Meanwhile, this article reports on the vascular anatomical variations discovered in the para‐aortic region to enhance surgical safety.

Material and Methods

This was a retrospective cohort study including patients undergone laparoscopic para‐aortic lymphadenectomy at a single center from January 2020 to December 2023 for high‐risk endometrial and early‐stage ovarian cancer. Patient charts were reviewed for mode of operation, perioperative complications, operative details, and histopathology. The patients were divided into anterograde group and retrograde group according to the operation mode. The two groups were further compared based on the success rate of lymph node clearance at the renal vein level, perioperative complications, and the number of removed lymph nodes. Quantitative data were analyzed using the t‐test, non‐normally distributed data using the rank‐sum test, and categorical data using Fisher's exact test and the chi‐square test, with statistical significance defined as P < 0.05.

Results

Among 173 patients, the antegrade group showed higher surgery success (97.5% vs 68.82%), more lymph nodes removed (median 14 vs 7), and less median blood loss. The operation time was shorter in the antegrade group. Postoperative complications like lymphocele and venous thrombosis were lower in the antegrade group. Vascular abnormalities were found in 28.9% of patients, with accessory lumbar vein routing anomaly and accessory renal arteries being most common.

Conclusions

The antegrade approach is feasible, safe, and effective, improving surgical exposure, reducing difficulty without additional instruments or puncture sites, and minimizing organ damage risk. It is effective in achieving better access to the renal vein and removing more para‐aortic lymph nodes than the retrograde method. Recognizing and carefully managing the diverse vascular abnormalities in the para‐aortic area, including variations in renal arteries, veins, and the inferior vena cava, is essential to reduce intraoperative bleeding and the likelihood of converting to open surgery.

The study shows that the “tent‐pitching” antegrade intraperitoneal laparoscopic para‐aortic lymphadenectomy provides better surgical exposure and reduces operation difficulty. The vascular and anatomic variation of the abdominal aorta region are also introduced in this study which should be carefully identified during operation.

Abbreviations

BMI

body mass index

LPAL

laparoscopic para‐aortic lymphadenectomy

SLN

sentinel lymph node

Key message.

The study shows that the “tent‐pitching” antegrade intraperitoneal laparoscopic para‐aortic lymphadenectomy provides better surgical exposure and reduces operation difficulty. The vascular and anatomic variations of the abdominal aorta region are also introduced in this study which should be carefully identified during operation.

1. INTRODUCTION

Comprehensive staging surgery of endometrial cancer includes hysterectomy, bilateral salpingo‐oophorectomy, pelvic washing, and pelvic and para‐aortic lymph node dissection. ¹ However, due to the increased risk of surgical morbidity and lymphedema associated with systematic lymph node dissection, as well as the ongoing controversy regarding its therapeutic efficacy, there is a lack of consensus among gynecologic oncologists regarding the extent of surgical staging. ² , ³ , ⁴ , ⁵ Some randomized clinical trials suggest that systematic lymph node dissection may not provide therapeutic benefits for patients with early‐stage disease. Sentinel lymph node (SLN) mapping can be considered in patients with low to moderate risk of lymph node metastasis, and for lymph node staging in FIGO I/II stage patients, SLN mapping is an acceptable alternative to systematic lymph node dissection. ⁶ Non‐invasive SLN mapping techniques, such as radiomics, have also gained widespread attention in recent years. ⁷ Some scholars have proposed the concept of “cancer field” based on embryo‐logically determined Müllerian compartment and suggested “peritoneal mesometrial resection and targeted compartmental lymphadenectomy” for endometrial cancer. It is recommended to limit “side‐specific” lymph node dissection to the first line nodes only including the cancer field in continuity from tumor to the nodes identified by the indocyanine green stained draining lymphatic channels and sentinel nodes, avoiding systematic pelvic lymph node dissection. This resection technique, by preserving lymphatic channels of non‐risky compartments, can reduce morbidity to the lowest level comparable to SLN dissection. ⁸ , ⁹ However, the treatment challenge lies in avoiding overtreatment of patients with low risk of recurrence while also not underestimating the risk of recurrence. ⁶ , ¹⁰ , ¹¹

Although accumulating data emphasize the safety and efficacy of the aforementioned techniques, there is still a lack of high‐quality randomized controlled trials comparing their oncologic outcomes with systematic lymph node dissection. Typically, the indications for systematic lymph node dissection are based on the risk of lymph node metastasis. For tumors at high risk of lymph node involvement, complete pelvic and para‐aortic lymph node dissection remains guideline‐recommended. ¹² , ¹³ Comprehensive staging surgery for high‐risk endometrial cancer and early‐stage ovarian cancer necessitates clearing the para‐aortic lymph nodes up to the level of the renal vein. First, lymph node metastasis at the level of the renal vein is also present in early‐stage endometrial/ovarian cancers. Studies have indicated that up to 10% of early‐stage endometrial cancer patients and 14%–20% of early‐stage ovarian cancer patients have metastases to lymph nodes at the renal vein level, ¹⁴ , ¹⁵ , ¹⁶ and removal of lymph nodes at this level can increase the overall survival rate by 10% for endometrial cancer and 21% for ovarian cancer. ¹⁷ , ¹⁸ Second, prospective studies have shown that 77% of patients with para‐aortic lymph node metastases have lesions above the level of the inferior mesenteric artery. ¹⁹ Third, the phenomenon of skip metastases exists. 5% of endometrial and 3% of ovarian cancers can bypass the lymph nodes below the inferior mesenteric artery and directly metastasize to the renal vein level lymph nodes, even at a very early stage. ²⁰ , ²¹ In fact, ultrastaging and pathologic review of negative pelvic lymph nodes of patients with presumed isolated para‐aortic metastasis identified occult pelvic dissemination. ²² Moreover, recurrence of ovarian and endometrial cancers can occur at the renal vein level lymph nodes unless these high‐positioned para‐aortic lymph nodes are removed during staging. ²³

Although documenting the status of para‐aortic lymph nodes at the renal vein level is crucial, and laparoscopic surgery for comprehensive staging of endometrial and early‐stage ovarian cancers has been proven to have fewer postoperative complications and shorter hospital stays compared to open surgery, ²⁴ routine removal of all para‐aortic lymph nodes to the level of the renal vein via intraperitoneal laparoscopy can be quite challenging. A survey in the United States revealed that 50% of gynecologic oncologists typically only remove lymph nodes up to the level of the inferior mesenteric artery when para‐aortic lymphadenectomy is necessary, with only 11% reporting routine removal up to the renal vein level. ² In a retrospective analysis of 206 patients with a body mass index (BMI) greater than 35 with endometrial cancer, the median number of para‐aortic lymph nodes removed by the laparoscopic intraperitoneal group was only 6, ²⁵ indicating that the limitations of laparoscopic intraperitoneal para‐aortic lymphadenectomy are not due to the surgeons but the surgical technique itself. ²⁶ In addition, there are a variety of vascular abnormalities in the abdominal aorta region, and it is difficult to deal with vascular injuries intraperitoneally under endoscopy, which increases the risk and difficulty of surgery. Despite the more familiar anatomical pathway for gynecologists and a shorter learning curve for intraperitoneal surgery, these limitations make doctors reserve minimally invasive surgery only for the most favorable surgical candidates – young, non‐obese patients with few comorbidities, rather than potentially benefiting groups like obese patients.

To improve the laparoscopic para‐aortic lymphadenectomy(LPAL), our center introduces an improved LPAL method reaching the level of the renal vein. It involves merely changing the surgeons' positions of themselves and monitor to optimize access to the para‐aortic region, without the need for additional trocar placements or changes in the positions of existing trocars, and without the need for auxiliary instruments to expose the intestines, thereby reducing the risk of damage to surrounding organs. This position facilitates the lifting of the posterior peritoneum, effectively concealing the intestines, providing good surgical field exposure, reducing surgical difficulty, and opening the posterior peritoneum less, not exceeding the level of the inferior mesenteric artery, thereby reducing postoperative pelvic‐abdominal adhesions. Under physiological conditions, lymphatic drainage is regularly directed from the peripheral to the central venous system. ²⁷ Therefore, for the change of surgical orientation proposed in this paper, we named it anterograde LPAL according to the direction of lymphatic drainage, and correspondingly, the operation mode from the center to the peripheral direction was retrograde LPAL. Additionally, our center compared the improved antegrade LPAL with the intraperitoneal retrograde LPAL to confirm the feasibility, safety, and effectiveness of the new method. This article also introduces the vascular anatomical variations in the para‐aortic region discovered at our center to enhance surgical safety.

2. MATERIAL AND METHODS

2.1. Study design and patient selection

This is a retrospective study comparing the outcome of the antegrade and retrograde intraperitoneal LPAL groups with high‐risk endometrial and early‐stage ovarian cancer from January 2020 to December 2023 at the Second Xiangya Hospital of Central South University, in Changsha, China. This study involved a total of 166 patients diagnosed with endometrial cancer and 7 patients diagnosed with ovarian cancer. Patients were enrolled into either the improved antegrade LPAL group (antegrade group) or the retrograde LPAL group (retrograde group), depending on the procedure they had performed. A single surgical team, including two identical gynecologic oncology specialists, performed the surgeries, which included LPAL. The equipment used was the same for both groups. All pathological analyses were conducted by an experienced pathologist and reviewed by at least two pathologists. All patients met inclusion criteria.

Inclusion criteria for the patients were as follows: (1) newly diagnosed patients who had not received combined adjuvant therapy, including chemotherapy, radiotherapy, and hormone therapy, and had not been diagnosed with any other malignancies within 2 years prior; (2) high‐risk endometrial cancer (lymphovascular space invasion, positive pelvic lymph nodes, deep myometrial invasion, grade 3 histology, and high‐risk histopathology) and ovarian cancer (stages IA‐II); (3) patients with an expected survival time of more than 3 months. Exclusion criteria included: (1) patients with recurrent endometrial cancer not undergoing lymphadenectomy; (2) those with extensive pelvic and abdominal metastasis or distant metastasis; (3) patients diagnosed with endometrial stromal sarcoma or other malignancies; or (4) patients with severe underlying diseases (cardiac, liver, lung, kidney, etc.). This study complied with the Declaration of Helsinki. All patients provided informed consent regarding potential complications and the possibility of conversion to open surgery before the procedure. The study was approved by the Ethics Committee of the Second Xiangya Hospital of Central South University.

2.2. Surgical technique

Patient Positioning and Trocar Insertion: During the procedure, the patient is placed under general anesthesia in a head‐down, feet‐up Trendelenburg position. The trocar insertion for both the antegrade and retrograde methods is the same, requiring five trocars (Figure 1A): (1) a 10 mm trocar at the midpoint between the umbilicus and the xiphoid (Lee–Huang point) for the camera (A point); (2) two 5 mm trocars are placed at the lateral border of the rectus abdominis on each side (B and C points); (3) a 5 mm trocar is placed on the right side of the midline above the pubic symphysis (D point); (4) a 10 mm trocar is placed on the left side of the midline above the pubic symphysis (E point).

FIGURE 1.

Setting of puncture holes and surgical stations for retrograde approach. (A) Setting of the puncture hole. (B) Surgical stance during retrograde approach to para‐abdominal aortic lymph node dissection.

Surgeon Positioning: For the surgeries prior to PAL, both the retrograde and antegrade group surgeons stand on the patient's left side, with the first assistant on the right, facing the monitor positioned at the patient's feet. The Lee–Huang point is used for the camera (A point), and the remaining points are used by the surgeon. For PAL, in the retrograde group, the surgeon continues in the original position and operative approach. For the antegrade group, the surgeon and first assistant switch positions; the surgeon stands on the patient's right and the first assistant on the left, with the monitor rotated 180 degrees toward the patient's head. The trocar above the pubic symphysis on the left side (E point) is used for the camera, while those on the right midline above the pubic symphysis (D point) and right lateral rectus border (B point) are used by the surgeon. The Lee–Huang point (A point) and the left lateral rectus border (C point) are used by the first assistant, with the antegrade group positioning shown in Figure 1B.

2.3. LPAL procedure

The retrograde LPAL procedure is as follows: The posterior peritoneum is opened along the abdominal aorta, the Treitz ligament is cut, and the duodenum is overturned and mobilized (Figure 2A), fully exposing the underlying renal vein. The left renal vein is dissected laterally and downward, revealing the left ovarian vein. The vascular sheath over the inferior vena cava is cut to reveal the right ovarian vein entering the inferior vena cava. Both ureters are retracted to expose the bilateral psoas major and iliopsoas muscles, defining the surgical boundary. The lymph nodes between the inferior vena cava, its right side, the surface of the abdominal aorta, and between the inferior vena cava and the abdominal aorta are cleared from the renal vein downward. The inferior mesenteric artery is skeletonized from the base of the abdominal aorta, and the left ovarian vein is dissected medially and downward from below the left renal vein until all lymphatic tissue on the left side of the abdominal aorta is completely removed.

FIGURE 2.

Diagrams of the forward and backward operation. (A) Antegrade approach to expose the renal veins: 1. Duodenum, 2. renal vein. (B) “tenting” approach to retrograde exposure of the duodenum and retroperitoneal vessels: 1. duodenum, 2. inferior vena cava, 3. abdominal aorta.

The antegrade LPAL procedure is as follows: The posterior peritoneum is opened along the abdominal aorta to just below the level of the inferior mesenteric artery; the first assistant lifts the posterior peritoneum to create a “tent effect,” obscuring the intestines (Figure 2B). Detailed procedure of the antegrade LPAL is shown in Video S1. It is crucial to ensure that the incision in the posterior peritoneum does not exceed the level of the inferior mesenteric artery to maintain the tenting effect. The loose space below the duodenum is opened to expose the renal vein. Dissection is carried out leftward and downward along the left renal vein, revealing the left ovarian vein. The sigmoid mesocolon is lifted, opening the loose space and exposing the left ureter. The right peritoneum is lifted to expose the right ureter and right ovarian vein, defining the surgical boundary. The vascular sheath is opened at the midpoint of the right common iliac vein, dissected upward, fully skeletonizing the inferior mesenteric artery and clearing lymph nodes up to the level of the renal vein.

2.4. Outcome measures

The primary outcome measure was the ability of LPAL to reach the level of the renal vein. A successful surgery is defined by completely excising all fatty and lymphatic tissues around the abdominal aorta, inferior vena cava, and renal vessels according to the LPAL surgical boundaries: cephalad to the left renal vein, caudad to the midpoint of the common iliac vein, and bilaterally from the ureters to the psoas major muscles. Comprehensive and complete visualization of the origins of ovarian vessels, inferior mesenteric artery, lumbar vessels, and accessory vessels should be achieved, as well as full exposure of the anterior longitudinal ligament, anterior and lateral parts of the vertebrae, psoas major muscles, and anterior sacrum.

Secondary outcome measures include the number of para‐aortic lymph nodes removed, surgical complications, LPAL time, and estimated blood loss. Additional recorded data include the patient's diagnostic age, histological classification, degree of differentiation, clinical staging, and BMI index. In this study, surgical complications encompass ureteral damage, vascular damage, lymphocele, and deep vein thrombosis. LPAL time refers to the time taken from peritoneal incision at the iliac artery–ureter crossing to lymphadenectomy up to the level of the left renal vein or inferior mesenteric artery. Estimated blood loss is estimated based on the volume of blood in the suction canister.

2.5. Statistical analyses

Statistical analyses were conducted using R studio version 4.2.2. Quantitative data are presented as mean ± standard deviation and were compared between groups using the t‐test for normally distributed data and the median for non‐normally distributed data, with comparisons using the rank‐sum test. Categorical data were compared between groups using the chi‐square test and Fisher's exact test. P‐value of <0.05 was considered statistically significant.

3. RESULTS

Over a 48‐month period, a total of 166 endometrial cancer and 7 ovarian cancer patients were included in the study. Among them, 76 endometrial cancer and 4 ovarian cancer patients underwent the improved antegrade LPAL, while 90 endometrial cancer and 3 ovarian cancer patients underwent the retrograde LPAL. For endometrial cancer, 120 patients underwent extraperitoneal hysterectomy with bilateral salpingo‐oophorectomy; 44 underwent subextensive hysterectomy with bilateral salpingo‐oophorectomy; 18 underwent omentectomy, and 2 patients, who had previously undergone hysterectomy, received laparoscopic pelvic lymphadenectomy and para‐aortic lymphadenectomy. For ovarian cancer, six patients underwent comprehensive staging surgery, including laparoscopic hysterectomy, bilateral salpingo‐oophorectomy, omentectomy, multiple peritoneal biopsies, and/or appendectomy. One patient underwent fertility‐sparing comprehensive staging surgery.

There were no significant differences between the antegrade and retrograde groups in median age (53 ± 7.47 vs 52.09 ± 8.06; p = 0.448), histological classification (p = 0.697), tumor differentiation (p = 0.483), or clinical staging (p = 0.071). The BMI of the antegrade group (24.29 ± 4.3) was higher than that of the retrograde group (22.99 ± 3.07) (p = 0.023), possibly due to better exposure of the surgical field in the antegrade group, which is more favorable for patients with higher BMI. Baseline characteristics of the patients are detailed in Table 1.

TABLE 1.

General condition of patients in retrograde and antegrade groups.

General characteristics	Antegrade group (N = 80 cases)	Retrograde group (N = 93 cases)	p‐value
Age at diagnosis	53 ± 7.47	52.09 ± 8.06	0.448
Histological classification			0.697
Endometrioid adenocarcinoma	71	82
Plasma breast cancer	2	4
Clear cell carcinoma	0	2
Mixed cancer	3	2
Ovarian and fallopian tube cancer	4	3
Degree of differentiation			0.483
G1	20	31
G2	38	40
G3	22	22
Clinical staging			0.071
I	67	66
II	5	16
III	8	11
BMI	24.29 ± 4.3	22.99 ± 3.07	0.023

The success rate of surgery in the antegrade group was 97.5% (78/80), with one patient not achieving renal vein level due to high BMI (BMI 29.5) and another due to a horseshoe kidney. The success rate in the retrograde group was 68.82% (64/93), with 29 patients unable to reach the renal vein level due to poor exposure of the infra‐renal vein area and terminating the surgery at the level of the inferior mesenteric artery.

The rates of intraoperative complications such as vascular and peripheral organ damage (p = 0.249) were not statistically different between the two groups. However, it should be noted that there were no instances of vascular or peripheral organ damage in the antegrade group, whereas the retrograde group had two cases of vascular injury and one case of duodenal injury. Of the vascular injuries, one was minor bleeding from a superficial vein on the inferior vena cava, which was controlled with pressure, and the other was bleeding from an accessory lumbar vein entering the left renal vein, which was successfully controlled with laparoscopic suturing. The patient with duodenal injury was repaired by a gastrointestinal surgeon and recovered postoperatively. There were no urinary tract injuries in either group. The estimated median blood loss was less in the antegrade group than in the retrograde group (p = 0.001). The median operative time for PAL in the retrograde group (50 min; range 40–80 min) was longer than in the antegrade group (35 min; range 30–60 min) (p < 0.001). Neither group required conversion to open surgery. Postoperative complications, including lymphocele or lymphocyst and lower limb venous thrombosis combined, were lower in the antegrade group compared to the retrograde group (2 vs 11 cases; p = 0.042). The antegrade group had one case of mild chylous ascites, while the retrograde group had eight cases of chylous ascites. The incidence of chylous fistula was lower in the antegrade group compared to the retrograde group (1.25% vs 8.6%), and all cases were cured with conservative treatment such as a low‐fat diet. One patient in the antegrade group and three in the retrograde group developed deep vein thrombosis, all of which were post‐tibial vein thromboses and were cured with immobilization and anticoagulation treatment. There was no significant difference in postoperative hospital stay days between the two groups (p = 0.055). Patients were discharged on average 7 days post‐surgery. Postoperative management is determined based on pathological findings: clinical follow‐up or radiotherapy or chemotherapy.

The median number of para‐aortic lymph nodes obtained in the antegrade group was 14 (range: 4–25), while in the retrograde group it was 7 (range: 2–31), with a statistically significant difference (p < 0.001). Among the entire study population, six patients (3.47%) were confirmed to have para‐aortic lymph node metastasis, all of whom were endometrial cancer patients. Among the endometrial cancer patients with para‐aortic lymph node metastasis, one (16.7%) had para‐aortic lymph node metastasis with negative pelvic lymph nodes, and five (83.3%) had both para‐aortic and positive pelvic lymph node metastases. Two (33.3%) endometrial cancer patients were confirmed to have both pelvic and para‐aortic lymph node metastases, but with less than 50% myometrial invasion. Perioperative data for the two groups are detailed in Table 2.

TABLE 2.

Perioperative data for the retrograde and antegrade groups.

General characteristics	Antegrade group (N = 80 cases)	Retrograde group (N = 93 cases)	p‐value
LPAL time (min)			<0.001
Median	35	50
Interval section	30 ~ 60	40 ~ 80
Intraoperative blood loss (mL)			<0.001
Moderate (<200 mL)	72	71
Heavy (>200 mL)	8	22
Number of aortic lymph nodes (nos.)			<0.001
Median	10	7
Interval section	1 ~ 25	2 ~ 31
Intraoperative complications	0	3	0.249
Vascular damage	0	2
Duodenal injury	0	1
Length of postoperative hospitalization (days)			0.055
Median	7	7
Interval section	4 ~ 14	5 ~ 20
Postoperative complication	2	11	0.042
Lymphatic fistula/cyst	1	8
Deep vein thrombosis	1	3

A total of 50 vascular anomalies were identified intraoperatively, with an overall incidence of 28.9% (50/173). The incidence of venous system anomalies, in decreasing order of frequency, included accessory lumbar vein routing anomalies in 21 cases (12.1%) (Figure 3A–C), double inferior vena cava in 3 cases (1.7%) (Figure 3D), inferior vena cava transposition in 2 cases (1.2%) (Figure 3E), pre‐aortic inferior vena cava/iliac vein confluence in 2 cases (1.2%) (Figure 3F), dilated ascending lumbar vein in 2 cases (1.2%) (Figure 3G), posterior left renal vein in 1 case (0.6%) (Figure 3H), and circumaortic left renal vein in 1 case (0.6%) (Figure 3I); the incidence of arterial system anomalies, in decreasing order of frequency, included accessory renal artery in 15 cases (8.7%) (Figure 3J), abnormal iliac artery branches in 2 cases (1.2%) (Figure 3K), horseshoe kidney and pre‐caval renal artery in 1 case (0.6%) (Figure 3L).

FIGURE 3.

Vascular variations in some para‐abdominal aortic regions. (A–C) Accessory lumbar veins. White arrows point to different directions of the accessory lumbar veins; black arrows point to the renal arteries. (D) Double inferior vena cava. (E) Left inferior vena cava. (F) Pre‐aortic inferior vena cava/iliac vein confluence. (G) Dilated lumbar ascending vein. (H) Posterior left renal vein. (I) Encircling aortic left renal vein. (J) Accessory renal arteries. (K) Iliac artery branching anomaly: Blue arrow points to the common iliac artery that is branching in advance. (L) Inferior vena cava anterior to the renal artery. The black arrow points to the renal artery. Legend: 1. renal vein, 2. abdominal aorta, 3. inferior vena cava, 4. ovarian vein, 5. inferior mesenteric artery, 6. accessory renal artery, 7. common iliac artery.

4. DISCUSSION

The application of SLN mapping in early‐stage endometrial cancer has been widely accepted by gynecologists and has been supported by numerous prospective and retrospective studies. ²⁸ , ²⁹ In some institutions, it has largely replaced systematic pelvic and para‐aortic lymph node dissection. Among the different techniques proposed for SLN mapping in endometrial cancer, the use of indocyanine green injection into the cervix is the preferred method and is uniformly recommended by the Society of Gynecologic Oncology. ⁵ , ³⁰ , ³¹ However, a major concern and criticism regarding the use of cervical dye injection for SLN mapping is that it may not adequately delineate the para‐aortic region, potentially missing isolated para‐aortic lesions. ³² Kimmig et al. confirmed that SLN mapping with cervical dye injection cannot reach the aortic region and only through uterine body injection can the aortic region be visualized. ³³ The reported overall frequency of para‐aortic lymph node metastasis ranges from 0% to 17%. ³⁴ In a prospective study at MD Anderson Cancer Center, among high‐risk endometrial cancer patients who underwent SLN mapping followed by pelvic and para‐aortic lymph node dissection, one patient was identified with isolated para‐aortic lesions (1 of 101 high‐risk patients) after SLN was not detected. Therefore, isolated para‐aortic involvement is rare but may occur, and high‐risk patients with “undetected” SLN seem to be at risk for this condition. ³⁵ Another concern regarding SLN mapping is that based on the cancer field theory proposed by Kimmig et al., performing SLN dissection or sampling may leave lymphatic tissue and eventually lymph nodes, at risk between tumor and sentinel node in situ since they belong to the locoregional cancer field at risk. A resection of selected nodes only, therefore, violates the therapeutic aspect of compartmental cancer field resection. ⁸ Targeted compartmental lymphadenectomy combined with peritoneal mesometrial resection preserves lymphatic vessels of non‐risky compartments, avoiding systematic pelvic lymph node dissection, and has been preliminarily validated for its effectiveness and safety in high‐risk endometrial cancer patients. ⁹ However, for high‐risk endometrial cancer, such as a deep infiltration of a G2/3 tumor close or into the serosa which may cause isolated paraortic node metastases comparable to ovarian cancer. In these situations, a para‐aortic sentinel node biopsy may be indicated. ²⁷ Therefore, high‐quality data accumulation is still needed for targeted compartmental lymphadenectomy in high‐risk endometrial cancer patients.

Therefore, in staging surgeries for endometrial cancer with high‐risk factors and ovarian cancer, clearing the para‐aortic lymph nodes located below the renal vein holds significant diagnostic and therapeutic value, directly impacting patient outcomes and prognosis. ³⁶ , ³⁷ Currently, laparoscopic surgery is recognized for its minimal invasiveness, clear field of vision, and fewer complications and is recommended for surgical treatment of endometrial cancer. However, it requires meeting the pathological standards of open surgery, meaning all lymphatic regions at risk of tumor invasion must be covered laparoscopically. ³⁸ Yet, performing para‐aortic lymphadenectomy at the renal vascular level laparoscopically is challenging for several reasons: First, surgical field exposure is difficult. The field is mostly obscured by the mesentery and intestines, and exposure is influenced by the patient's BMI, particularly in obese patients. ²⁵ Studies have reported that surgery often ends at the level of the inferior mesenteric artery in patients with a BMI over 35. ³⁹ Second, there are anatomical contraints during the surgery. When the surgeon stands on the patient's left side to operate on the same side lesion, the range of operation motion becomes restricted, and the arms must operate at an angle, complicating the procedure. Third, the presence of anatomical variations significantly increases the risk of damaging surrounding organs during surgery. ⁴⁰

To achieve the goal of laparoscopic para‐aortic lymphadenectomy, many scholars have attempted various approaches, focusing mainly on two aspects: (1) changing the surgical approach to extraperitoneal routes, including single‐port and multi‐port laparoscopy and robot‐assisted extraperitoneal approaches. The extraperitoneal route has clear advantages in terms of good exposure and minimal adhesions but is technically more difficult with a relatively long learning curve, not easily mastered by gynecologic oncologists. ⁴¹ Another challenge is maintaining the integrity of the peritoneum; if the peritoneum is perforated, the extraperitoneal route fails. ²⁶ (2) Improving intraperitoneal surgical methods by changing trocar positions and numbers, ⁴² , ⁴³ , ⁴⁴ altering surgical positioning, rotating the camera, and using other tools to assist in lifting the peritoneum, such as needles and rakes. ⁴¹ , ⁴⁵

Our modified method has several advantages over previous improvements. First, there is no need to add or remove trocars, as increasing trocar numbers can augment trauma to patients. Second, by changing the surgeon's position and the camera's orientation, we successfully overcome the anatomical constraints of traditional laparoscopic para‐aortic lymphadenectomy. With the surgeon and camera repositioned, the surgical field immediately becomes the familiar laparoscopic view for gynecologic oncologists, significantly reducing the difficulty of the operation. Third, no additional surgical instruments are needed, reducing the risk of damage to surrounding organs. The first assistant can entirely lift the posterior peritoneum using the Lee–Huang point and the right McBurney's point trocars, creating a “tent effect.” The key to forming the “tent effect” is to not open the posterior peritoneum excessively; it should not exceed the level of the inferior mesenteric artery. The peritoneum's natural tension and the first assistant's tools can effectively support the omentum and small intestine, clearly exposing the duodenum and the PAL area completely. Fourth, opening the posterior peritoneum less, not exceeding the level of the inferior mesenteric artery, reduces postoperative pelvic‐abdominal adhesions. Finally, our data confirm that our modified technique allows oncologists with laparoscopic and anatomical knowledge to perform LPAL at the renal vein level, without any special training compared to the extraperitoneal approach, and is easily completed.

The number of lymph nodes removed is often the most important oncological parameter in lymphadenectomy. ⁴⁶ Many studies have used the number of lymph nodes as an indicator of successful surgery. Our findings indicate that the antegrade group can obtain a higher number of para‐aortic lymph nodes in patients with higher body mass index. The number of lymph nodes obtained is similar to the results of other modified methods published. ³⁸ However, since the count of lymph nodes is also influenced by pathological computation, the number alone cannot be the sole criterion for successful surgery. Instead, the standard should be whether the surgery can cover all lymphatic regions at risk of tumor invasion laparoscopically. Our results show that when performing lymphadenectomy at the renal vein level using the antegrade method, 97.5% of patients reached the renal vein level, and there were no perioperative vascular injuries, peripheral organ damage, or conversions to open surgery. Even for patients with high BMI, the antegrade group still met the surgical standards, obtaining more para‐aortic lymph nodes, less surgical time and intraoperative blood loss, and a lower rate of postoperative complications.

Anatomical variations in the para‐aortic region are the main causes of intraoperative bleeding, thromboembolic events, and preoperative misdiagnosis in LPAL, ⁴⁷ with mechanisms stemming from embryonic development. Reported incidence rates for venous and arterial system anatomical variations vary, with venous system abnormalities between 0.1% and 43%, and arterial system abnormalities between 9% and 31%. ⁴⁰ Among arterial system abnormalities, accessory renal arteries are quite common, affecting up to 30%–40% of the population. ⁴⁷ Accessory renal arteries are functional end arteries. Damage to accessory renal arteries could lead to partial renal ischemic necrosis. Our study found 50 vascular anomalies, including 15 accessory renal arteries, making it the second most common vascular variation. Additionally, the right renal artery is typically described as passing behind the inferior vena cava, yet reports suggest up to 5% of pre‐caval right renal arteries. ⁴⁸ Our study identified one pre‐caval renal artery and two patients with downwardly displaced renal arteries, completely exposed 2–3 cm below the renal vein. Venous system anomalies primarily refer to the number and position of the inferior vena cava and renal veins. Huntington and McLure proposed a classification system for inferior vena cava anomalies based on abnormal regression and the aberrant persistence of various embryonic veins. ⁴⁹ Mark J and others proposed a similar surgical and radiological classification. ⁵⁰ Our study identified all the aforementioned venous system anomalies except for the rare variations like retrocaval ureter and interrupted inferior vena cava with azygos continuation. ⁴⁹ Additionally, we found anatomical variations less commonly reported in the literature, such as dilated ascending lumbar veins and high‐branching ovarian veins. Similarly to Klemm's study conclusion, we found the most common anatomical variation to be various accessory lumbar vein routing anomalies. ⁴⁰ Our center identified 21 cases of accessory lumbar vein routing anomalies, with one incident of intraoperative accessory lumbar vein injury requiring vascular repair. Our center found that an incidence of retroaortic renal vein is 0.6%, similar to previous studies. ⁵¹ Additionally, the general population has up to 0.3% incidence of horseshoe kidneys. ⁵² The isthmus of a horseshoe kidney, located above the abdominal aorta, is a common anatomical anomaly that hinders abdominal and pelvic surgery, particularly para‐aortic lymphadenectomy. Our center identified two cases of horseshoe kidneys, which due to the limitations of the laparoscopic approach did not clear up to the level of the renal vein.

Our cohort study has several weaknesses: (1) with a retrospective design, our study cannot exclude selection bias and undisclosed confounders. However, this paper mainly emphasizes the technical aspects and the perioperative parameters and outcome and eventually description of anatomical variations; therefore, discussion of clinical impact in this paper is of minor relevance. More randomized controlled trials are needed to verify the merits of the new approach. (2) The cases recruited in this study (BMI for the antegrade group: 24.29 ± 4.3) did not include obese women. Obesity might be a significant limitation for our posterior peritoneal “tent effect” method, as excessive fat on the mesocolon could hinder the formation of the “tent effect,” especially in the infra‐renal area. (3) In terms of surgical skills, the requirements for surgeons increase, as the first assistant cannot provide much help in special situations such as vascular injury. (4) Extraperitoneal and robotic surgeries were not compared. (5) The estimation of blood loss includes many other procedures besides comprehensive lymphadenectomy. (6) Lack of follow‐up data.

5. CONCLUSION

This article presents a novel approach for intraperitoneal laparoscopic para‐aortic lymphadenectomy, utilizing a “tent‐pitching” lifting effect formed by lifting the posterior peritoneum, which provides good exposure to the infra‐renal area. Combined with changes in the surgeon's position and the rotation of the laparoscopic video screen, this technique facilitates easier management of upper abdominal and major vascular injuries. This new method aims to overcome the technical difficulties and constraints of traditional intraperitoneal laparoscopic para‐aortic lymphadenectomy, thereby promoting discussion on the clinical value of evaluating para‐aortic lymph nodes and future research. Understanding the anatomical anomalies in this region also provides useful references for adopting this technique, helping to minimize the risk of damage to major vessels and ensuring the completeness of the resection.

AUTHOR CONTRIBUTIONS

Xianqing Wu designed the article. Xiaoshan Chai wrote the manuscript. Xianqing Wu and Hongwen Zhang performed the surgery; Zhaoying Chen conducted the statistical analysis; Tianyu Zhu analyzed the patient data and processed image; Xianqing Wu was responsible for the revision of the manuscript for important intellectual content. All authors contributed to the article and approved the submitted version.

CONFLICT OF INTEREST STATEMENT

The authors declare that they have no conflict of interest.

ETHICS STATEMENT

This study was approved on November 29, 2023, by the Human Ethics Committee of the Second Xiangya Hospital of Central South University (No. 2023(287)). Written informed consent was obtained from the individual for the publication of any potentially identifiable images or data included in this article.

Supporting information

Video S1.

Chai X, Zhu T, Chen Z, Zhang H, Wu X. Improvements and challenges in intraperitoneal laparoscopic para‐aortic lymphadenectomy: The novel “tent‐pitching” antegrade approach and vascular anatomical variations in the para‐aortic region. Acta Obstet Gynecol Scand. 2024;103:1753‐1763. doi: 10.1111/aogs.14916