Comparison of robotic-assisted versus laparoscopy for transperitoneal infrarenal para-aortic lymphadenectomy in patients with endometrial cancer

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1 doi: /jog J. Obstet. Gynaecol. Res. Vol. 44, No. 3: , March 2018 Comparison of robotic-assisted versus laparoscopy for transperitoneal infrarenal para-aortic lymphadenectomy in patients with endometrial cancer Hyun Jung Lee, Yoon Hee Lee, Gun Oh Chong, Dae Gy Hong and Yoon Soon Lee Department of Obstetrics and Gynecology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea Abstract Aim: This study was conducted to evaluate the clinical feasibility of robotic-assisted transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL) in patients with endometrial cancer. Methods: From June 2006 to October 2016, we retrospectively analyzed 42 patients who underwent laparoscopic (n = 16) or robotic-assisted (n = 26) staging operations, including TIPAL for endometrial cancer. Perioperative data including age; body mass index; operation duration; the number of lymph nodes retrieved and the ratio of time to lymph node retrieval during pelvic, infrarenal para-aortic and total lymphadenectomy; estimated blood loss and postoperative complications were compared. Results: The operative duration of pelvic ( vs min; P = 0.002), and total ( vs min; P = 0.010) lymphadenectomy was significantly shorter in the robotic-assisted than the laparoscopic group, whereas there was no statistical difference in the duration of infrarenal para-aortic lymphadenectomy. By contrast, the number of infrarenal para-aortic lymph nodes retreived was significantly higher ( vs ; P = 0.016) in the robotic-assisted group. Consequently, the ratio of time to number of lymph nodes retrieved during infrarenal ( vs ; P = 0.002) and total ( vs ; P = 0.014) lymphadenectomy was lower in the robotic-assisted compared to the laparoscopic group. Conclusions: The robotic-assisted approach took less time per infrarenal para-aortic and total lymph nodes retrieved compared to the conventional laparoscopic approach. Robotic-assisted TIPAL could be feasible and effective for the staging and treatment of patients with endometrial cancer. Key words: endometrial cancer, robotic surgery, transperitoneal infrarenal para-aortic lymphadenectomy. Introduction Comprehensive surgical staging is the mainstay of initial treatment for most patients with endometrial cancer. The results of staging surgery, including pelvic and para-aortic lymphadenectomy, provide a guide for postoperative adjuvant treatment, information about prognosis and biologic features of the disease. The infrarenal lymph nodes have recently received attention as the common sites of nodal metastasis in endometrial cancer, despite negative ipsilateral inframesenteric aortic nodes. 1 3 However, removal of the infrarenal para-aortic nodes up to the renal vein is difficult, sometimes incomplete or unsafe. Since the da Vinci surgical system was approved in 2005 for gynecology, the role of robotic-assisted surgery in endometrial cancer has continued to evolve. The benefits of robotic technology include three-dimensional and high-definition optics, endowrist instruments that allow greater range of motion, the elimination of tremors, higher precision and improved surgeon autonomy without Received: June Accepted: September Correspondence: Professor Yoon Soon Lee, Department of Obstetrics and Gynecology, School of Medicine, Kyungpook National University, 807, Hoguk ro, Buk-gu, Daegu 41404, Republic of Korea. yslee@knu.ac.kr 547

2 H. J. Lee et al. reliance on a trained surgical assistant. 4,5 These advantages have made it possible to overcome difficulties associated with the conventional laparoscopic approach. 6 Several studies have described the perioperative outcomes of robotic-assisted transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL) and concluded that this procedure is feasible, adequate and safe. 7,8 However, studies that have compared robotic-assisted and laparoscopic approaches have included TIPAL as a part of surgical staging but not as an independent procedure. Thus, there are no available data to evaluate this procedure separately using these two approaches. Although minimally invasive surgery in the management of patients with endometrial cancer continues to develop, 9 the role of robotic surgery is even less defined. In the present study, we compared the operative duration, the number of retrieved lymph nodes and the ratio of time to the number of lymph nodes retrieved during pelvic, infrarenal para-aortic and total lymphadenectomy to those of laparoscopy in order to evaluate the perioperative outcomes of robotic-assisted TIPAL in endometrial cancer. Therefore, the purpose of this study was to evaluate the clinical feasibility and perioperative outcomes of robotic-assisted TIPAL in endometrial cancer. Methods We retrospectively analyzed the records of 42 patients who underwent laparoscopic (n = 16) or roboticassisted (n = 26) staging operations for endometrial cancer from June 2006 to October 2016 at Kyungpook National University Hospital. Surgical management included total hysterectomy with removal of both adnexa and bilateral pelvic, infrarenal para-aortic lymph node dissection. Aortic node dissection was extended up to the level of the renal vein. Endometrial cancer was staged according to the current guidelines approved by the International Federation of Gynecology and Obstetrics. Demographic data are provided in Table 1. Both groups were statistically homogeneous. A surgeon with 17 years of experience performed all operations. The number of pelvic and para-aortic nodes was based on pathologic reports and included all retrieved lymph nodes, regardless of metastasis. Hospital stay was defined from admission to discharge. Estimated blood loss was based on operative and anesthesiologist notes. We performed robotic-assisted TIPAL using the da Vinci S or Xi Surgical System. All patients underwent bowel preparation and lower extremity mechanical compression, and received perioperative antibiotics. Patients were operated on in the dorsolithotomy position. Table 1 Patient characteristics between robotic versus laparoscopic lymphadenectomy Characteristic Robot Laparoscopy P (n = 26) (n = 16) Age (years) Duration of hospitalization (days) BMI (kg/m 2 ) Tumor grade Tumor stage I II III IV 6 2 Blood loss (ml) Hemoglobin change (g/dl) Perioperative 3 (11.5) 2 (12.5) complications, n (%) 1 Aorta injury, 1 rebleeding, 1 pulmonary embolism 1 Caval injury, 1 chylous ascites BMI, body mass index. 548

3 Robotic para-aortic lymphadenectomy In the robotic-assisted approach, a single port was inserted at the umbilicus for the robotic scope and removal of retrieved lymph nodes, followed by insertion of four additional trocars. Two robotic trocars were placed horizontally at the right side of the umbilicus. Another robotic trocar and one ancillary trocar were placed horizontally at the left side of the umbilicus. The robotic grasps were inserted through the right lateral robotic trocar. The robotic bipolar forceps, the robotic scissors and vessel sealers were inserted through the right medial or the left lateral robotic trocar. The robotic column was positioned in between the patient s legs. An operating table rotation system was used to perform TIPAL after robotic-assisted pelvic surgery in cases using the da Vinci S system. In cases using the da Vinci Xi system, we rotated the arms of the robot system leaving the table at the original position (Fig. 1). In the conventional laparoscopic approach, the primary puncture was made using an 11 mm sharpened triple-edge pyramidal trocar along the lower margin of the umbilicus. Three 5 mm punctures were placed at the lower abdomen (both lateral sides and supra pubic) and one 11 mm trocar was placed to the left upper quadrant. The laparoscopic tower with endoscopic camera system was repositioned from the patients legs to head for para-aortic lymphadenectomy. A similar surgical approach was performed in both laparoscopic and robotic-assisted TIPAL. After left upper traction of the rectosigmoid, a peritoneal incision was made caudad to the inferior mesenteric artery. The rectosigmoid was mobilized, and then the avascular space of the lateral rectal portion was found using upward traction of the rectosigmoid mesentery. Inframesenteric nodes were removed without injury to the ureter and the left common iliac nodes were easily removed because of the upward traction of the rectosigmoid. The superior hypogastric plexus was found overlying the aorta and sacral promontory, and presacral nodes were removed at the subaortic area. A peritoneal traction suture to the right abdomen was required for right para-aortic lymphadenectomy. After right lower para-aortic node dissection, the operator was situated between the patient s legs. After upper traction of the small bowel, left upper para-aortic (infrarenal) nodes were removed. To prevent chylous ascites, we used hemolock or Ligasure application to the upper part of the infrarenal (Fig. 2) and aortocaval nodes (Fig. 3). The infrarenal para-aortic lymphadenectomy margin is from the ureter crossing the common iliac artery at the bifurcation to the level of the branching of the renal veins off of the vena cava superiorly with the psoas posteriorly on the left and the vena cava posteriorly on the right, the peritoneum and duodenum Figure 1 Trocar placement for robotic-assisted (a) pelvic, lower para-aortic and (b) infrarenal lymphadenectomy. Large open circle, single port; small circle, robotic trocars; square, accessory trocar for assistant. 549

4 H. J. Lee et al. distribution of the variables. Discrete variables were compared using the χ 2 or Fisher s exact tests in the case of small cell comparisons. In addition, linear correlation analysis was performed between the lymph node retrieval time (dependent variable) during surgery with the number of lymph nodes (independent variable 1) and the mode of surgery, such as robotic or laparoscopic surgery (independent variable 2). Statistical significance was defined as P < All computations were performed using commercially available software, SPSS version Results Figure 2 Postoperative view of infrarenal transperitoneal para-aortic lymphadenectomy. The left infrarenal area (dashed line) is bound by the left renal vein (arrow) and the aorta (arrow head). Figure 3 Dissection of the aortocaval area between the vena cava (arrow) and aorta (arrow head), up to the left renal vein (dashed arrow). anteriorly and each of the ureters laterally, divided right and left by the aortocaval margin. TIPAL operative duration was equivalent to console time in robotics and was considered from the peritoneal incision until node extraction in laparoscopy. We analyzed the ratio of time to the number of retrieved lymph nodes to compare the effectiveness of the procedure. Continuous data were analyzed using the t-test for parametric variables or the Mann Whitney U test for non-parametric variables; the Kolmogorov Smirnov test was used to verify Demographic data are provided in Table 1. There was no difference between the groups regarding blood loss and the difference between hemoglobin concentration before and after surgery. The rate of complications was similar in both groups. There were three cases of perioperative complications in the roboticassisted group, consisting of one aorta injury, which was managed robotically, one pulmonary embolism and one rebleeding. In the conventional laparoscopic group, two cases of complications, including one chylous ascites and one caval injury occurred. The operative duration of pelvic ( vs min; P = 0.002) and total ( vs min; P = 0.010) lymphadenectomy was significantly shorter in the robotic-assisted surgery group than in the laparoscopic group, respectively, whereas there was no statistical difference in the duration of infrarenal para-aortic lymphadenectomy ( vs min; P = 0.151) (Table 2). By contrast, the number of infrarenal para-aortic lymph nodes was significantly higher ( vs ; P = 0.016) in the robotic-assisted group. Consequently, the ratio of time to number of lymph nodes retrieved during infrarenal ( vs ; P = 0.002) and total ( vs ; P = 0.014) lymphadenectomy was lower in the robotic-assisted surgery group compared to the laparoscopic group (Table 2, Fig. 4). In linear regression analysis, time was correlated with the number of lymph nodes retrieved during total lymphadenectomy during surgery (R 2 = 0.290, P = 0.003). There were higher R 2 values in the robotic-assisted surgery group for pelvic (0.297 vs 0.020), infrarenal (0.181 vs 0.055) and total (0.338 vs 0.002) lymphadenectomy than in the laparoscopic group (Fig. 5). The mode of surgical approach had an 550

5 Robotic para-aortic lymphadenectomy Table 2 Comparison of surgical results of pelvic, infrarenal para-aortic and total lymphadenectomy between groups Result Robot Laparoscopy P (n = 26) (n = 16) Pelvic lymphadenectomy Number of lymph nodes Time (min) Ratio of time to number Infrarenal para-aortic lymphadenectomy Number of lymph nodes Time (min) Ratio of time to number Total lymphadenectomy Number of lymph nodes Time (min) Ratio of time to number effect on the duration of pelvic (standardized coefficient = 0.47, P = 0.002), infrarenal para-aortic (standardized coefficient = 0.46, P = 0.005) and total (standardized coefficient = 0.52, P = 0.001) lymphadenectomy (Table 3). Discussion Figure 4 Comparison of the ratio of time per total lymph nodes retrieved according to operation mode. As the infrarenal lymph nodes have garnered interest as common sites of nodal metastasis, despite negative ipsilateral inframesenteric aortic nodes, 1 3 para-aortic lymphadenectomy extended up to the infrarenal area is considered an important part of staging and surgical therapy for endometrial cancer. 10 With the introduction of laparoscopic lymphadenectomy, laparoscopic lymphadenectomy is now regarded as a feasible and Figure 5 Linear regression analysis between surgical duration and the number of retrieved lymph nodes in (a) pelvic, (b) infrarenal and (c) total lymphadenectomy, according to surgical method. 551

6 H. J. Lee et al. Table 3 Linear regression of time for lymphadenectomy according to number of lymph nodes and mode of surgery Mode B (95% CI) β P Pelvic lymphadenectomy Constant 7.48 ( 1.76, 16.72) Mode of surgery 8.56 (3.48, 13.64) Number of lymph nodes 0.30 ( 0.02, 0.617)) Infrarenal paraaortic lymphadenectomy Constant 6.11 ( 21.40, 33.62) Mode of surgery (5.88, 31.47) Number of lymph nodes 0.55 ( 0.05, 1.154)) Total lymphadenectomy Constant ( 13.69, 51.59) Mode of surgery (11.24, 40.34) Number of lymph nodes 0.38 ( 0.11, 0.863) safe procedure because of the higher magnification provided to remove all the lymph nodes in the region compared to laparotomy However, removal of the infrarenal para-aortic nodes up to the renal vein is difficult, sometimes incomplete and unsafe. Generally, the limitation of the laparoscopic approach to the infrarenal area includes a steep learning curve because of the requirement of non-traditional surgical skills, high reliance on trained surgical assistants, patient condition when morbidly obese, a large uterus or significant intra-abdominal adhesions. Many of the limitations related to laparoscopy are overcome by robotic-assisted surgery. The threedimensional, magnified vision combined with wrist instrumentation, the elimination of tremors and motion scaling allow the surgeon to replicate open surgery. Robotic surgery more closely mimics open procedures and is associated with a shorter learning curve. 14 While a skilled robotic bedside assistant is essential, the robotic surgeon has the additional advantage of stable, autonomous and precise control of the camera and instrument movements. Robotics also reduces the poor ergonomics associated with laparoscopy, which can lead to surgeon discomfort and the risk of chronic musculoskeletal injury, particularly during longer procedures. 15 Our study aimed to evaluate the clinical feasibility of robotic assisted TIPAL in patients with endometrial cancer by comparing the perioperative outcomes of the robotic-assisted approach with those of the conventional laparoscopic approach. There is conflicting evidence regarding which of the two surgical approaches takes less intra-operative time (Table 4). Several series have observed a shorter operative duration with the robotic-assisted approach in gynecologic malignancies; however, they compared the total operation duration, not the time related exclusively to TIPAL. Other observational studies have provided operative durations for TIPAL with variable and different results. In our study, we compared the operation duration and the ratio of time to the number of nodes retrieved to compare the exclusive duration of each lymphadenectomy. 7,8,15 23 The operative duration of pelvic and total lymphadenectomy was significantly lower in the robotic assisted group than in the laparoscopic group, whereas there was no statistical difference of the duration of infrarenal para-aortic lymphadenectomy. By contrast, the number of infrarenal para-aortic lymph nodes retrieved was significantly higher in the roboticassisted group. Consequently, the ratio of time to number of lymph nodes retrieved during infrarenal and total lymphadenectomy was lower in the roboticassisted group in comparison to the laparoscopic group. The robotic-assisted approach required less time to retrieve lymph nodes in infrarenal and total lymphadenectomy areas. Moreover, the time for retrieval of lymph nodes was correlated with the number of lymph nodes in the robotic-assisted group. We attributed these relatively constant decreases in time for node retrieval in the robotic-assisted group to the stability of the robotic system and the increased autonomy of the operator, without reliance on an assistant. In addition, a previously experienced advanced surgeon of conventional laparoscopy and a well-trained bedside assistant may be potential factors accounting for the shorter operative durations in the robotic-assisted group. Our study had several limitations. First, our patient selection was not randomized and was retrospective. We retrospectively reviewed all endometrial cancer patients and selected cases that had undergone TIPAL. As robotic-assisted surgery was performed by an experienced surgeon using a conventional laparoscopic 552

7 Robotic para-aortic lymphadenectomy Table 4 Perioperative outcomes of TIPAL in published series Source Approach No. of patients Site of cancer Operative duration (min) for TIPAL No. of TIPAL-nodes Intraoperative Postoperative complications complications Magrina et al. 7 Robotic 33 Ovary, cervix, endometrium, vagina, peritoneum Lambaudie et al. 8 Robotic 53 Ovary, cervix, endometrium aorta injury, 1 inferior mesentery artery injury 1 lymphocyst caval injury, 1 inferior 2 lymphocysts, 1 abscess, mesenteric artery injury 1 hematoma Seamon et al. 15 Laparoscopy 76 Endometrium ND 11 2 caval and aortic injuries 1 thromboembolic disease Robotic 105 Endometrium ND 10 None None Boggess et al. 16 Laparoscopy 81 Endometrium ND caval injury 1 lymphocyst Robotic 103 Endometrium ND 12 None 1 lymphocyst, 1 thromboembolic disease Cardenas-Goicoechea Laparoscopy 173 Endometrium ND 7.2 None 3 lymphocysts et al. 17 Robotic 102 Endometrium ND 9 None 1 lymphocyst, 1 thromboembolic disease DeNardis et al. 20 laparotomy 106 Endometrium ND 6.6 None 1 lymphocyst Robotic 56 Endometrium ND 6.5 None None Gehrig et al. 21 Laparoscopy 32 Endometrium ND 7.03 None 1 lymphocyst Robotic 49 Endometrium ND 10.3 None 1 lymphocyst Magrina et al. 22 Laparoscopy 37 Endometrium ND caval injury 1 deep venous thrombosis Robotic 67 Endometrium ND 8.7 None 1 deep venous thrombosis Coronado et al. 19 Laparoscopy 8 Endometrium ND 6.4 None 1 lymphocyst Robotic 4 Endometrium ND 5.8 None None Coronado et al. 18 Laparoscopy 32 Ovary, cervix, endometrium Robotic 30 Ovary, cervix, endometrium Ponce et al. 23 Robotic 50 Ovary, cervix, endometrium Total, No. Laparoscopy 439 ND 8.1 Robotic 652 ND None None inferior mesenteric artery injury None caval injury 2 chylous ascites, 1 ileus, 1 death Complications probably related to transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL). and ND, no data relative to TIPAL. 553

8 H. J. Lee et al. approach, it could have affected the reduced operative duration in the robotic-assisted group. It may also be of concern that results from a single surgeon s experience in the same hospital might not be easily reproduced in a different setting. However, the merits of this study include that it has significant consistency with all cases represented. Well-designed, large randomized controlled trials are needed to determine more precisely the feasibility and safety of roboticassisted surgery. Second, the total operation duration was not compared. There are disadvantages with the robotic system for infrarenal para-aortic lymphadenectomy, in particular, the requirement for table or robotic arm rotation, although these steps do not seem to delay patient recovery. Table rotation requires coordination between the operating team and anesthesia department. Finally, our study did not enroll a large enough number of patients to evaluate clinical outcomes, such as major complications. The occurrence of major vessel injury in the presented study (3.8%) was lower than that reported using inframesenteric paraaortic lymphadenectomy. 7,10 Control of major vessel bleeding is facilitated by robotic instrumentation. The robotic grasper can be left in situ to secure bleeding while vascular suture preparations for hemostasis can be made. The patient s thighs must be further lowered to prevent restriction of the robotic arm and the possibility of injury related to this position can be increased. Other disadvantages include increased costs, the need for a trained and supportive team and experienced assistant and limitations to the extent of movements of the robotic arms. According to the results of this study, a higher number of infrarenal para-aortic lymph nodes were retrieved in less time in the robotic-assisted group. In summary, the perioperative results of transperitoneal para-aortic infrarenal lymphadenectomy in our study were different to other studies: the number of retrieved infrarenal para-aortic lymph nodes was higher in the robotic-assisted group, but pelvic lymph nodes were similar in both groups. Lymph node retrieval took less time in the robotic-assisted group during infrarenal para-aortic and total lymphadenectomy. In conclusion, robotic-assisted TIPAL could be feasible and effective for the staging and treatment of patients with endometrial cancer. Disclosure No authors declare any conflict of interest. Author contributions All authors have read and approved the final version of the manuscript. References 1. Mariani A, Dowdy SC, Cliby WA et al. Prospective assessment of lymphatic dissemination in endometrial cancer: A paradigm shift in surgical staging. Gynecol Oncol 2008; 109: Gil-Moreno A, Magrina JF, Pérez-Benavente A et al. 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