Lymphadenectomy in gynecological cancer is intensively discussed with respect to prognostic, predictive, and therapeutic aspects [
Robotic surgery enables us to develop and dissect structures with extremely increased accuracy, thus allowing to prepare and free the compartments completely of lymphatic tissue without injuring adjacent compartments by respecting the filmy septa at the compartment borders. Due to the excellent 3D/HD visualization surgical technique may be described step by step and may precisely be reproduced and documented in each patient. The authors translated Höckel’s compartment based method of “therapeutic lymphadenectomy,” developed for open surgery of uterine cancer, to a robotically assisted approach, which will be described in the following step by step.
The first author learned the surgical technique of TMMR and tLNE participating in Leipzig School of Surgery in 2006. All radical hysterectomies were consequently performed using the nerve-sparing technique of TMMR and tLNE, if adequate. In 2010, robotically assisted laparoscopic surgery was implemented using a da Vinci Surgical System (Intuitive Surgical Inc., Sunnyvale, CA, USA). The principles of surgical steps were systematically translated to the robotic surgery and optimized to guarantee the same radicalness compared to open surgery but maintain the advantages of an endoscopic approach. The different steps were discussed with Höckel by video sequences. Finally, Höckel participated in the surgery in Essen and confirmed equality of the robotic approach with respect to his operation defined by open surgery. The resulting technique of rtLNE will be described in detail for the firsttime in international literature. The technique with respect to cervicalcancer has been already described in German only, but without reporting anyclinical data [
Patient preparation is identical to laparoscopy with deep Trendelenburg positioning. Trocars are positioned 23–25 cm above the symphysis (camera), two lateral robotic trocars about 5 cm–10 cm above the upper anterior iliac spine, one additional robotic trocar on the left between camera trocar and left lateral trocar, one assistant trocar of 10 mm diameter on the right side between camera trocar and right lateral trocar. The space in between the trocar incisions was at least 10 cm to ensure adequate mobility.
As a first proof of feasibility, 35 patients were treated by rTMMR or rPMMR and rtLNE with cervical cancer FIGO IB-IIa or endometrial cancer FIGO I-III. Therapeutic lymphadenectomy was performed by “robotic surgery” in analogy to the procedure described by Höckel [
Analysis of clinical and histopathological data was performed using and SPSS17.0 for Macintosh (SPSS, Chicago, IL, USA). We conducted a descriptive analysis only, considering the limited number of patients and the explorative character of this study.
The principle of ontogenetically derived surgical compartmental resection may be defined for each organ system. In the following, we will focus on lymphatic basins and the intercalated nodes of the uterus. As outlined by Höckel et al. [
(a) Pelvic lymphatic basins of the uterus (from Hepp et al., Lymphonodektomie in der gynäkologischen Onkologie. Indikation, Technik und Konsequenzen für die Therapieplanung Urban and Schwarzenberg 1988 with permission from ELSEVIER GmbH, Urban and Fischer Verlag) [
Whereas in cervical cancer skip metastases in tertiary and quaternary basins are extremely uncommon, they occur in endometrial cancer due to the different lymph drainage (Figure
Following this concept, the following lymph nodes have to be removed in cervical cancer: Lnn. mesometriales, Lnn. Iliaci externi, interni and communes, Lnn. obturatorii, gluteales superiores et inferiores, pudendales, rectales, praesacrales and subaortici corresponding to the primary and secondary basin. In case of proven node metastases in the primary or secondary basin, the inframesenteric periaortic and pericaval nodes ought to be removed; in case of their involvement, the infrarenal periaortic and pericaval nodes in addition.
In case of high risk endometrial cancer without cervical involvement no metastases may be present in the deep gluteal, pudendal, and rectal nodes. However, all other nodes of level 1–4 have to be removed due to the risk of involvement.
The following steps will illustrate the surgical anatomy and operative technique of robotically assisted therapeutic pelvic and periaortic lymphadenectomy (rtLNE).
First, the robotically assisted pelvic therapeutic lymphadenectomy will be described.
(a) After incision of the parietal peritoneum, the common iliac vessels are exposed. The sigma and mesostigma can be elevated in order to prepare the left iliac vessels further distally. (b) Preparation of the right iliac retroperitoneal space.
(a) Identification of the hypogastric superior plexus at the aortic bifurcation. (b) Preparation of the hypogastric superior plexus, separating its fibers from vessels and lymphatic basins (ci).
Preparation of the left upper iliac retroperitoneum (ci).
Preparation of the right upper iliac retroperitoneum.
(a) Lymphadenectomy of the upper iliac region exposing the aortic bifurcation (ci, ps). (b) Exposition of the promontorium and the presacral region (subaortic nodes, ps). (c) Exposition and preparation of the left iliac bifurcation.
Preparation of the lateral part of upper paravisceral basin (pv) and lower common iliac basin (ci), dissecting all lymphatic tissue.
Preparation of the right external iliac vessels (ei).
Preparation of lateral part of paravisceral basin (exposition of obturator nerve).
Lymphadenectomy in between right external iliac artery and vein (ei).
Caudal pelvic preparation on the right side exposing the pubic bone (ei).
Development of the paravisceral space by medialization of the vesical mesenteric septum and dissection down to the endopelvic fascia (pv).
Clearing of the lateral and medial part of the paravisceral basin down to the pubococcygeal and iliococcygeal muscles and up to the internal iliac vessels (pv).
Preparation of the right prespinal region with corresponding lymph basins (pv).
Deep pelvic preparation on the left side (ei, pv).
(a) Exposition of the superior gluteal artery and lumbosacral nerve roots (pv). (b) Visualization of the N. ischiadicus and the Vasa pudenda (upper paravisceral basin).
Steps 10–12 correspond to steps 7–9 on the left side.
Following preparation of the branches of the anterior internal iliac artery (Figure
Left lower paravisceral basin (pv).
Left vascular mesometrium (mm) with exposed uterine vessels.
Left iliac bifurcation, border to common iliac basin (ci, line).
In case of indication for periaortic lymphadenectomy two different situations have to be addressed: primary tumor involves uterine corpus and/or adnexa or the cervix only.
In the first situation lymph drainage follows the vascular mesometrium and the infundibulopelvic ligament; therefore primary lymph basins are pelvic and periaortic, simultaneously, and therefore have to be removed entirely. In the second situation periaortic lymph basins are of third or forth order and may be maintained in case of histologically proven negative pelvic nodes.
In case of tumor involvement of the uterine corpus or the adnexa in addition to the vascular mesometrium also the network for vascular and lymphatic anastomoses between uterus and adnexa has to be removed, best covered by the peritoneal leaves of the broad ligament (PMMR). The vascular and lymphatic drainage system along the ovarian vessels has to be removed in analogy to the vascular mesometrium up to its connection to the periaortic and pericaval lymph basins. Whereas the vascular anastomoses to the mesenteric vessel system (ascendant and descendant colon) are dissected the connections to the periaortic lymph basins are preserved and removed together “en bloc.”
On the other hand, if tumor is located in uterine corpus, exclusively, the deep gluteal, pudendal, and rectal nodes may be preserved, since usually there will be no “upstream drainage” in such situation except for clinically suspicious nodes. On the other hand, if it is located in uterine cervix only, periaortic lymphadenectomy has only to be performed in case of positive pelvic nodes, and resection of the ovarian vessel system is not mandatory.
Preparation of the left inframesenteric lymph nodes (im).
Preparation of the lower periaortic region exposing the inferior mesenteric artery (im).
Interaortocaval region with vertebral vessels (ir and im).
Upper periaortic region with right ovarian vessels (ir).
(a) Preparation of the ovarian vessels next to the ureter. (b) Separation of the left ovarian vessel system from the mesostigma.
Upper periaortic region, mobilization of the duodenum.
(a) Preparation and dissection of the right ovarian vein (ir). (b) Exposition of the right ovarian artery at its origin (ir). (c) Preparation of the left ovarian vein (ir). (d) Exposition of the left ovarian artery (ir).
Separation of the left periaortic lymphatic tissue together with the left infundibulopelvic ligament from the inferior mesenteric system (im).
Preparation of the left periaortic lymphatic tissue with special attention to fibers of the superior hypogastric plexus.
Fibers of the inferior mesenteric and superior hypogastric plexus are clearly visible; they are mobilized together with the mesostigma (ir).
En bloc mobilization of the left infundibulopelvic ligament through the “sigmoid tunnel.”
If resection of the ovarian vessel drainage system is not necessary—in case of cervical cancer—the procedure can be performed identically following dissection of connecting vessels to the periaortic drainage system and lateralization of the ovarian vessels.
During the preparation care should be taken to mobilize the entire lymphatic basins of interest and concomitantly preserve the autonomic nerve fibers and the ureteral supplying vessels as thoroughly as possible.
This compartment defined lymphadenectomy in therapeutic intention is combined by compartment defined local surgery, for example, TMMR (total mesometrial resection) or FMMR (fertility-preserving mesometrial resection) for cervical cancer, PMMR (peritoneal mesometrial resection) for endometrial cancer or salpingo-oophorectomy with resection of ovarian vascular/lymphatic vessel system in early ovarian cancer. It is aimed to facilitate locoregional tumor control without additional radiotherapy.
In total, 35 patients were operated with the diagnosis of endometrial
The majority of endometrial as well as cervical cancer patients were diagnosed with FIGO I.
No transition to open surgery was necessary due to complications or technical problems. We noted complication rates of 13% for endometrial cancer and 21% for cervical cancer. In the group of endometrial cancer patients, one patient had a superficial vein thrombosis, and one had a phase of transitional postoperative aphasia which resolved completely. In the group of cervical cancer patients, there were two reoperations due to formation of an intra-abdominal lymphocele/abscess and one due to postoperative bleeding. One patient had a port infection which was treated by local aseptic measures.
Endometrial cancer patients with tumor stage FIGO III and/or positive lymph nodes were treated with six cycles of adjuvant platinum based chemotherapy. Patients with cervical cancer and positive lymph nodes received an adjuvant platinum based chemotherapy with or without irradiation.
Median followup was 20(22) month (Table
No patient, up to now, neither in cervical nor in endometrial cancer developed isolated locoregional recurrence.
Detailed data on patient characteristics and oncological outcome are depicted in Tables
Detailed information on clinical and perioperative data.
Patients | Age (years) | BMI (kg/m2) | Number of lymph nodes removed | Hospital stay (days) | Blood transfusion | Complication rate | |
---|---|---|---|---|---|---|---|
Endometrial cancer | 16 | 59 (26–78) | 32 (20–57) | 32 (16–52) | 10 (5–25) | 1 |
2 |
Cervical cancer | 19 | 46 (31–71) | 23 (18–33) | 34 (13–68) | 9 (6–33) | 2 |
4 |
Detailed information on oncological data.
Patients | Tumor stage | Grading | Positive lymph nodes | Recurrent disease | Median Follow-up (months) | |||||
---|---|---|---|---|---|---|---|---|---|---|
FIGO I | FIGO II | FIGO III | G1 | G2 | G3 | |||||
Endometrial cancer | 16 | 13 (81%) | 0 | 3 (19%) | 0 | 12 (75%) | 4 (25%) | 4 (25%) | 2 (13%) | 22 (13–28) |
Cervical cancer | 19 | 18 (95%) | 1 (5%) | 0 | 2 (11%) | 14 (74%) | 3 (16%) | 5 (26%) | 1 (5%) | 20 (12–28) |
We were able to show that the principle of compartment based surgery in uterine cancers, which is applied in the techniques of modified radical hysterectomies as TMMR and PMMR, can be translated with respect to the removal of the accordant lymphatic basins, to minimal invasive, robotically assisted procedures.
The method appears to be feasible and safe, especially if we consider that the presented data were collected during the very first learning curve of the authors. Although the followup time of our patients is limited, we are confident that the oncological outcome will be comparable to open surgery. Due to the excellent visibility, the high precision, and control of preparation, the technical radicalness of lymph node dissection can be controlled individually and documented continuously for each single region allowing complete removal of tissue at least comparable to open surgery if not even better.
In our experience, patients grossly benefit from these procedures. First, compartment based surgery oncologically appears to exert excellent locoregional control combined with a lower complication rate especially regarding the autonomous nerve plexus. Second, the translation to a minimal invasive method by robot assistance adds the advantages of minimal invasive surgery, regarding blood loss, mobilization, length of hospitalization, and short-term complications [
In conclusion, we suggest that the minimal invasive approach of compartment based oncologic surgery for uterine cancers by robotic assistance is feasible, safe, and beneficial for patients. To evaluate whether the excellent monocentric data with excellent locoregional tumor control and low morbidity of Höckel in cervical cancer [
However, for surgical studies it is crucial to define exactly the surgical procedure to be done. For “therapeutic lymphadenectomy” the technique described in this publication will be the reference basis, as it could be for other trials referring to “therapeutic lymphadenectomy.” In addition, operative procedure of TMMR and tLNE is exactly defined by surgical videos of open and robotically assisted TMMR and therapeutic lymphadenectomy preceded by education at Leipzig School of Radical Pelvic Surgery and followed by onsite visit to control for the technique. In future, from our point of view, this kind of preparation and auditing of surgical studies could contribute to comparability between different sites, which is not only mandatory in scientific studies but may also beneficial in education and clinical practice. 3 D Vision, HD Quality, magnification of structures, and thus, excellent quality of surgical videos derived from robotic surgery will revolutionize our prospects for education, scientific research, and quality control.
The authors thank Michael Höckel (Head of Department of Gynecology and Obstetrics, University of Leipzig, Head of Leipzig School of Radical Pelvic Surgery, Leipzig, Germany) for his intensive and steady support in helping us to understand ontogenetically derived compartment based radical surgery in uterine cancer and translating it from open to robotically assisted laparoscopic surgery.