Retroperitoneal Sentinel Lymph Node Biopsy by Vaginally Assisted Natural Orifices Endoscopic Transluminal Endoscopic Surgery in Early Stage Endometrial Cancer: Description of Technique and Surgeon’s Perspectives after the First Experience

Endometrial cancer is the most diagnosed gynecological malignancy in the USA and in developed countries and represents up to 90% of all uterine corpus cancers. Often diagnosed at early stages because of abnormal uterine bleeding, its incidence increased in the last years by an average of 0.5% per year with life expectancy, sedentary life, and obesity [1].

Surgery is the mainstay treatment for endometrial cancer patients, followed by radiation and/or chemotherapy based on the stage of the disease. Technical progresses and results of randomized studies allowed a shift from traditional open surgery toward minimally invasive approaches for management of early endometrial cases [2]. In patients with apparent uterus confined disease and low-grade tumors, the current recommendations state that minimally invasive surgery (laparoscopic and robotic) is the preferred approach when technically feasible. Sentinel node biopsy is an alternative option for retroperitoneal staging in these patients [3, 4]. Furthermore, laparoscopy offers a higher identification rate of the sentinel node, with less morbidity and lower false-negative rate than open surgery [5-7].

Natural orifices endoscopic transluminal endoscopic surgery (NOTES) is a minimally invasive surgical procedure that utilizes natural orifices to access to the peritoneal cavity. Several advantages compared to standard laparoscopy are described such as faster postoperative recovery, reduced pain, decreased postoperative wound infections, and no abdominal trocar port complications [8]. The benefits and feasibility of the vaginal NOTES (vNOTES) approach for benign gynecological pathologies including hysterectomy, benign ovarian, or tubal pathologies have already been proven by a series of randomized controlled trial [9-12]. In 2014, the first vNOTES case for early stage endometrial cancer FIGO IA G1 with transperitoneal lymphadenectomy was described, with no intra- or postoperative complications [13]. We hereby present our first experience with VNOTES sentinel node biopsy by retroperitoneal access in early stage G1 endometrial cancer.

Data statement: respecting the SCARE 2020 criteria, we collected the following data of 1 patient operated in October 2021.

A 64-year-old patient, nonobese, with postmenopausal bleeding presented to our institution. Endometrial biopsy identified a G1 endometrioid adenocarcinoma and the MRI concluded for superficial myometrial invasion with no abnormal lymph node. We performed a total hysterectomy with bilateral adnexectomy and retroperitoneal sentinel node biopsy by vNOTES.

The patient was placed in dorsal lithotomy position with her legs resting on knee supports. Draping allowed conversion to standard laparoscopy if needed. After injecting 4 mL of 1.25 mg/mL ICG at 3 and 9 o’clock superficial and deep into the cervix, a paracervical incision was made in the lateral vaginal fornix with a cold scalpel (Fig. 1). Sharp and afterward blunt digital dissection through this incision allowed the access to the obturator fossa after the opening of sacrogenital fascia. A 7.5-cm Gelpoint vPath small (Applied Medical) was inserted through this incision to create a retroperitoneal space by insufflating CO₂. The optic and all endoscopic instruments were inserted transvaginally through the Gelpoint. We entered transvaginally to the caudal part of the left obturator fossa and started by identifying the obturator nerve, artery, and vein. The left retroperitoneal space was further developed, and the sentinel node was identified using fluorescence imaging with a rigid 30° 10 mm telescope. As endoscopic instruments, a standard reusable 5-mm bipolar grasper and a 44-cm Caiman Vessel Sealing System (Aesculap, Inc.) were used.

The afferent lymph vessel was identified and the sentinel node was isolated from the surrounding tissues by careful dissection. Similar to the laparoscopic approach, two left sentinel nodes were resected and removed transvaginally on the left side. The same procedure was performed on the right side with identification of one lymph node, confirmed by anatomopathological examination. We were able to clip both uterine arteries before leaving the retroperitoneal space, which allowed almost no bleeding during the hysterectomy.

Vaginal fornix closure was made using a Polyglactin 910 simple continuous suture (Vicryl 2.0). Afterward, we performed a circumcision of the cervix with an electrosurgical scalpel. After opening of the vesicouterin space and the Douglas pouch, we transected the uterosacral ligaments. A 9.5-cm Gelpoint vPath was inserted, and we performed a simple hysterectomy with bilateral adnexectomy. All specimens were removed transvaginally, and vaginal closure was made with a unidirectional continuous autolocking suture (Stratafix Spiral PDS Plus 0). A urinary catheter was removed at the end of the surgery. We encountered no complication and blood loss was less than 100 mL. The total procedure time was 1 h 53 min.

A standardized postoperative protocol was performed corresponding to rapid mobilization, preventive anticoagulation, normal diet, simple analgesia such as paracetamol and ibuprofen. The patient was discharged on day 2 with no complications after 3-month follow-up.

The final histopathology did not identify any node metastasis and confirmed a G1 endometrial adenocarcinoma with superficial myometrial invasion, but proximal focal cervical stroma infiltration pT2 pN0, FIGO II. The patient underwent an adjuvant radio- and brachytherapy.

Kalloo et al. [14] first described NOTES surgery in 2004 in the porcine model using the transgastric endoscopic approach to the peritoneal cavity. Feasibility of transvaginal extraperitoneal lymphadenectomy by vNOTES was first assessed in porcine models in 2008 [15], and vNOTES was introduced in gynecology in 2012 for benign ovarian pathology. Since then, the technique developed exponentially and was implemented by many gynecologist surgeons for various procedures: hysterectomy, myomectomy, adnexal surgery, colposuspension, etc. (Fig. 2).

An international expert base statement guides surgeons with safe adoption of vNOTES approach and focuses on oncological applications of vNOTES surgery in order to collect outcomes and feasibility data. Consensus was reached in all domains except that of patients’ selection [16].

Contraindications to vNOTES are not totally established but may include history of inflammatory disease, active lower genital tract infection, obliterated pouch of the Douglas, rectovaginal endometriosis, history of a rectal surgery or mesh sacrocolpoplexy, ovarian cancer, history of pelvic radiotherapy, multiple cesarean sections, or virginity [9, 16]. An enlarged uterus or the previous laparoscopic surgery has no contraindications.

The surgical approach for vNOTES to perform lymphadenectomy can be intra- or retroperitoneal, before or after hysterectomy [17-19]. A recent Chinese retrospective study assessed a prospective study about standard laparoscopy versus vNOTES for early stage endometrial cancer. Between 2017 and 2020, 23 out of 74 patients underwent VNOTES hysterectomy with sentinel node biopsy. The sentinel nodes were harvested transperitoneally, after the hysterectomy, using carbons nanoparticles injected 15 min before surgery. If no stained node was identified in the pelvic and para-aortic area, a side-specific pelvic lymphadenectomy was performed by vNOTES. The authors concluded to the absence of difference in sentinel node detection and perioperative outcome between the two groups, but a decrease of hospital stay, a better cosmetic result, and a faster recovery for the vNOTES approach [2]. No conversion to classic laparoscopy was reported.

In case of vNOTES sentinel node biopsy or lymphadenectomy, the spatial orientation of the anatomical structures is different compared to the standard laparoscopy or the open surgery. However, because of the very little anatomical variation of pelvic vessels and nerves, an experimented surgeon adapts without difficulty to the new point of view [20]. Main limitations of vNOTES are the restricted surgical access in case of a narrowed vagina, instrument-optic conflicts, and difficult triangulation that may be circumvented by a curved scope or instruments [2].

For our patient, the access to the obturator fossa was easy. After the incision of the sacrogenital fascia and introduction of the v-path, we identified the obturator nerve, vein, and artery. Following the course of the obturator nerve, we identified the arterial and venous iliac bifurcation. The ureter, umbilical, and uterine artery were subsequently identified. Because the access is next to the cervix, the afferent lymphatic vessels are directly seen and the true sentinel node (the closest dyed node to the tumor) was identified.

In standard laparoscopy, the obturator fossa is accessed cranially and we approach the tumor and the sentinel node on the opposite direction of the lymphatic drainage. We frequently see multiple dyed nodes and should follow the dyed lymphatic vessels and nodes until the cervix to assure that the true sentinel node is identified. By this access, parallel to the lymphatic vessels and close to the tumor, vNOTES allows to follow the afferent vessels and to easily identify the first dyed node. As in 85% of cases, the sentinel node is located below the iliac vessels, and this approach offers an excellent access [2]. The retroperitoneal vNOTES approach might have thus an additional advantage to reduce the number of harvested lymph nodes by limiting the number of secondary lymph nodes, which has no sentinel node.

About lymphatic nodes situated above the iliac vessels, at the aortic bifurcation, or in the para-aortic region, the vaginal approach seems more difficult, but feasible according to the Chinese team and Baekelandt. Baekelandt proposed this new retroperitoneal transvaginal vNOTES approach as it enables a better exposure of retroperitoneal structures and less indocyanine leakage than transperitoneal [21]. Exposure of the major vessels and anatomic landmarks is critical to success [22].

In endometrial cancer with clinical negative lymph nodes, an extemporaneous examination of lymph nodes is not mandatory, as results will not change the course of the surgery or the management of the patient. Two randomized studies confirmed that radical pelvic dissection does not improve the outcome in patients with endometrial cancer, but lymphadenectomy allows the identification of nodal involvement [5]. In patients with apparent uterine confined disease, sentinel node mapping is an alternative to lymphadenectomy [23-25]. Ultrastaging of sentinel lymph nodes can identify metastasis undetected through conventional histology, leading to upstaging in 5–15% cases [26, 27].

Concerns about the contamination of retroperitonal space by malignant cell displaced from the uterine cavity and its impact in late outcomes were raised by some authors [28]. It has been described that vaginal contamination with glandular tumor cells in patients with endometrial cancer occurs either before or during the surgical procedure, leading to vaginal recurrences. Stolnicu et al. [29] propose to wash the vagina before and after the surgical procedure or to use a special device to prevent tumor cell spillage. Before starting the procedure, Tantitamit et al. [30] preconize the suture of the exocervix to prevent tumor’s spreading. We did not find any other suggestion in other studies, but cerclage before the beginning of the procedure might be another option. The question whether these protective maneuvers have sense or not is still not answered. Previous hysteroscopy and curettage or positive peritoneal washing before hysterectomy does not worsen the prognosis of patients with endometrial cancer [31, 32].

Although any surgical approach might be proposed in endometrial cancer (abdominal, vaginal, laparoscopic, robotic), minimal invasive surgery is recommended for uterine confined disease, even for a patient with high-risk carcinomas without compromising oncological outcome [33-35]. Laparotomy remains the preferred option in metastatic disease, large uterus, or patients intolerant to Trendelenburg position or pneumoperitoneum.

vNOTES, such as standard vaginal surgery, offers greater benefits to obese and extreme obese patients [36]. Endometrial cancer patients are often overweight, with metabolic comorbidities and advanced age. This population correlates with a higher risk of vascular injury during surgery, venous thromboembolism, postoperative wound infections, and operative constraints for the surgeon [37-40]. vNOTES enables moderate Trendelenburg position and the pneumoperitoneum is lowered to 8–10 mm Hg, two technical advantages for these patients [41].

Approximately 3–10% of patients suffering from endometrial cancer are unsuitable for surgery [30]. vNOTES could improve this statistics by lowering the complications and surgical morbidity by combining the advantages of minimal invasive surgery, good exposition of the abdominal cavity, and advantages of a vaginal approach without limitation by the nondescent of the uterus [36, 42, 43].

Nevertheless, some patients describe apprehension toward vNOTES, especially younger patients before 36 years old, with only 36% that would favor this approach. This might be due to the concern about their sexual life or future pregnancy. Comprehensive analysis of women’s perception is essential to understand their choice in regard to classic abdominal laparoscopy versus vNOTES and to reassure them with a long-term follow-up about transvaginal surgery, showing no incidence of sexual symptoms or dyspareunia [5-7].

The vaginal access broadens the indications of NOTES surgery for oncological gynecological surgery allowing an accurate staging of endometrial cancer [13]. This new surgical approach may overcome patient-related limits of the standard laparoscopy or laparotomy procedures. It requires technical skills, proficiency, and familiarization with new planes of view. However, the learning curve shows an exponential improvement in surgical performance in hands of skilled surgeon [44]. Nevertheless, it requires to reskill to vaginal surgery a generation of young “laparoscopic only” gynecologists. Further studies are required to corroborate the feasibility of retroperitoneal approach for staging of uterine cancers based on a larger panel of patients.

This is a case report about 1 patient in 2021. Our institution (Hôpital de Sion) exempted us to submit the case from an ethical approval. Written informed consent was obtained from the patient for the publication of this case report and any accompanying images.

The authors have no conflicts of interest to declare.

There was no funding for this case report. All the authors worked in their free time on this paper.

Marie-Pierre Mathey: carried out the structure of the article and the literature review, and corrected the final version. Fabien Romito carried out the description of the surgical procedure. Daniela E. Huber followed the patient, corrected several times, and approved the final version.

The data that support the findings of this study are openly available in Research Registry (https://www.researchregistry.com/browse-the-registry. Guarantor Dr Mathey Marie-Pierre).