Abstract
Background/Aim: We evaluated the clinical feasibility and surgical outcomes of robotic-assisted transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL) in patients with gynecological malignancies. Patients and Methods: The perioperative outcomes in 90 patients with gynecological malignancies who underwent laparoscopic (n=43) or robotic-assisted (n=47) TIPAL were compared retrospectively. Results: The operative time for pelvic and total lymphadenectomy were significantly shorter in the robotic-assisted approach, whereas the time for infrarenal para-aortic lymphadenectomy did not differ statistically. In contrast, the number of infrarenal para-aortic lymph nodes was significantly higher in the robotic-assisted approach. We compared the time per retrieved lymph node in both approaches, and those for pelvic, infrarenal para-aortic, and total lymphadenectomy were significantly shorter in the robotic-assisted approach. Conclusion: In our study, the robotic-assisted TIPAL took less time to retrieve a lymph node than the laparoscopic approach. The robotic-assisted approach for TIPAL is feasible for the staging and treatment of patients with gynecological malignancies.
With the introduction of the da Vinci system (Intuitive Surgical, Sunnydale, CA, USA), the potential benefits of a robotic surgery, such as three-dimensional, high-definition optics, wristed instruments, elimination of tremor, higher precision, and improved surgeon autonomy, have overcome some limitations of conventional laparoscopy (1-3). While the need for evaluating the infrarenal para-aortic area has increased owing to the possibility of metastases without positive inframesenteric lymph node in gynecological malignances, infrarenal para-aortic lymphadenectomy is considered a challenging procedure because of vessel anomalies (4-6). Several observational series that described the outcomes of robotic-assisted transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL) concluded that this procedure is feasible, adequate, and safe (7, 8). However, studies that compared the robotic-assisted approach with laparoscopic approaches analyzed surgical outcomes of TIPAL as a part of surgical staging but not as an independent procedure. Therefore, no data are available to evaluate TIPAL in isolation using these two approaches.
To evaluate the clinical feasibility of robotic-assisted TIPAL in gynecological malignancies, we compared the operative time, number of retrieved lymph nodes, and time per retrieved lymph node in pelvic, infrarenal para-aortic, and total lymphadenectomy with those in conventional laparoscopy.
Materials and Methods
We retrospectively evaluated 90 patients who underwent laparoscopic (n=43) or robotic-assisted TIPAL (n=47) for staging and treatment of gynecological malignancies (44 endometrial, 17 ovarian, and 29 cervical) between June 2006 and October 2016 at Kyungpook National University Hospital. Indications for TIPAL were staging of ovarian cancer in the early stage, staging of high-risk endometrial cancer, and evaluation of the status of the para-aortic nodes to adjust the radiation fields in locally advanced cervical cancer. Disease was staged in accordance with the current guidelines approved by the International Federation of Gynecology and Obstetrics (9, 10). All operations were performed by the same surgeon at same tertiary hospital. Patient and tumor characteristics are presented in Table I. Clinical data, including operative time, were retrieved from hospital records. The numbers of pelvic and para-aortic lymph nodes were based on pathological reports by gynecologic pathologists.
The da Vinci S or Xi Surgical System (Intuitive Surgical, Inc.) was used for robotic-assisted TIPAL. All the patients underwent bowel preparation and lower extremity mechanical compression for prevention of deep vein thrombosis and received perioperative antibiotics. The operation was performed in the reverse Trendelenburg, lithotomy position. In the conventional laparoscopic approach, we used two 11-mm trocars and three 5-mm trocars. The primary 11-mm trocar was inserted in the umbilicus for optics. For the instruments, three 5-mm trocars were placed in the lower abdomen (both lateral sides and supra pubic area) and one 11-mm trocar was placed in the left upper quadrant. After pelvic surgery, the laparoscopic tower was repositioned from the patient's legs to the head for infrarenal para-aortic lymphadenectomy.
Patient demographics and diagnosis.
In the robotic-assisted approach, we inserted a single port and four additional trocars. Firstly, the single port (Octoport; Dalim, Seoul, Korea) was inserted in the umbilicus, and the one robotic trocar was placed through the single port for optics. Two robotic trocars were placed horizontally at the right side of the umbilicus, spaced 7 cm apart. An ancillary trocar and a robotic trocar were placed horizontally on the left side, spaced 5 cm apart from the umbilicus. We inserted the robotic instruments differently between the pelvic and lower para-aortic lymphadenectomy and infrarenal para-aortic lymphadenectomy. Robotic grasps (Endowrist ProGrasp Forceps; Intuitive Surgical, Inc.) were through the right lateral robotic trocar in both lymphadenectomy. The robotic bipolar forceps (EndoWrist Fenestrated Forceps; Intuitive Surgical, Inc.), robotic scissors (EndoWrist Hot Shears; Intuitive Surgical, Inc.), and vessel sealers (EndoWrist One vessel sealer; Intuitive Surgical, Inc.) were inserted through the right medial or left lateral robotic trocar depending on the direction of the lymphadenectomy (Figure 1). The robotic column was positioned in between the patient's legs. We rotated the operating table to perform TIPAL after lower para-aortic lymphadenectomy and pelvic surgery in cases where the da Vinci S system was used. In cases with the da Vinci Xi system, we rotated the robotic arms, leaving the operating table in its original position. A similar surgical procedures were performed in both laparoscopic and robotic-assisted TIPAL. After left upper traction of the rectosigmoid, a peritoneal incision was made caudal to the inferior mesenteric artery. The rectosigmoid was mobilized, and then the avascular space of the lateral rectal portion was found by using upward traction of the rectosigmoid mesentery. The superior hypogastric plexus was found overlying the aorta and sacral promontory, and presacral nodes were removed in the subaortic area. Inframesenteric and left common iliac nodes were removed without injury to the ureter. After right lower para-aortic node dissection, the operator positioned between the patient's legs for para-aortic lymphadenectomy. Hemolock or Ligasure (Valleylab, Boulder, CO, USA) was applied to the basin of the infrarenal and aortocaval nodes (Figure 2) to prevent chylous ascites.
Comparison of surgical results of pelvic, infrarenal para-aortic and total lymphadenectomy between robotic-assisted and laparoscopic approaches.
The margins of pelvic lymphadenectomy include the genitofemoral nerve and pelvic sidewall laterally, the obturator nerve posteriorly, the ureter and superior vesical artery medially, the ureter crossing the bifurcation of the common iliac superiorly, and the crossing of the deep circumflex iliac vein over the external iliac artery inferiorly. Infrarenal para-aortic lymphadenectomy starts from the ureter crossing the common iliac artery at the bifurcation. The posterior margin is the psoas muscle and sacrum below the inferior mesenteric artery, and the psoas muscle and vena cava above the inferior mesenteric artery. The anterior margins are the peritoneal lining and duodenum. The lateral margin is the ureter on the left, and the ureter and vena cava on the right side. The superior margin is the branching of the renal veins off the vena cava.
Trocar placement for robotic pelvic, lower para-aortic (A) and infrarenal para-aortic (B) lymphadenectomy. Large open circle: single port, Octoport (Dalim, Seoul, Korea); small circle, robotic trocars; square, accessory port for assistant; open arrow, direction of lymphadenectomy.
The operative time for each lymphadenectomy was considered from the peritoneal incision to the end of nodes retrieval in both approaches. We calculated the specific time consumed for retrieving one lymph node as the operative time divided by the number of retrieved lymph nodes in pelvic, infrarenal, para-aortic, and total lymphadenectomy. For statistical analyses, 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 the distribution of the variables. Discrete variables were compared using the chi-square test or Fisher exact test in the case of small cell comparisons. Statistical significance was defined as a p-value of <0.05. All computations were performed using the commercially available software IBM SPSS Statistics for Windows, version 20 (IBM Corp., Armonk, NY, USA).
Results
The patient and tumor characteristics are presented in Table I. Blood loss during operation and the difference in hemoglobin concentration before and after surgery were not statistically different in both groups. The rate of complications was similar in both groups. Five perioperative complications developed in the robotic-assisted group, consisting of three cases of chylous ascites, one case of pulmonary embolism, and one case of aorta injury, which were managed robotically. In the conventional laparoscopy group, four cases of complications, namely two cases of chylous ascites and two cases of caval injuries occurred.
The operative time for pelvic and total lymphadenectomy were significantly shorter in the robotic-assisted approach than in the laparoscopic approach (both p≤0.001), but infrarenal para-aortic lymphadenectomy (p=0.142) showed no statistically significant difference. No significant difference in the number of retrieved pelvic nodes (p=0.734) were found between the two approaches. However, the numbers of lymph nodes retrieved in infrarenal para-aortic and total lymphadenectomy were significantly higher in the robotic-assisted approach (Table II). We compared the time per lymph node according to procedure, and those for pelvic (p≤0.001), infrarenal para-aortic (p≤0.001), and total lymphadenectomy (p≤0.001) were significantly lower in the robotic-assisted approach than in the laparoscopic approach (Figure 3). The F test revealed that the standard deviations for the time per retrieved node for pelvic, infrarenal para-aortic, and total lymphadenectomy were smaller in the robotic-assisted approach (p<0.001).
The operative time for pelvic (Figure 4A), infrarenal para-aortic (Figure 4B), and total lymphadenectomy (Figure 4C) correlated with the number of retrieved lymph nodes in both groups. The number of lymph nodes correlated with body mass index (BMI) in pelvic (R2=0.043, p=0.051) and infrarenal para-aortic areas (R2=0.21, p=0.169), and the total number of resected lymph nodes (R2=0.56, p=0.025). The operative time per retrieved lymph node in total lymphadenectomy (p=0.008) correlated reversely with BMI in the laparoscopic group, whereas BMI did not influence the time in the robotic group (p=0.910). Surgical approach influenced the linear regression between the ratio and the BMI during pelvic (p<0.001; Figure 5A), infrarenal para-aortic (p=0.025; Figure 5B), and total lymphadenectomy (p<0.001; Figure 5C). Linear regression analysis for pelvic, infrarenal para-aortic, and total lymphadenectomy revealed that the number of lymph nodes and the surgical method were a significant determinant of the duration of surgery (Table III).
View of transperitoneal infrarenal para-aortic lymphadenectomy showing the left infrarenal (A) and aortocaval areas (B). The left renal vein (arrow) extends over the aorta (arrowhead). The aortocaval area was dissected between the vena cava (dashed arrow) and aorta (arrowhead) up to the left renal vein (arrow). Hemolock (dashed circle) were applied to the basin of the infrarenal (A) and aortocaval (B) nodes to prevent chylous ascites.
Discussion
The need to evaluate the infrarenal para-aortic area has increased owing to the possibility of metastases without positive inframesenteric lymph nodes in gynecological malignances (4-6). However, infrarenal para-aortic lymphadenectomy is considered a challenging procedure because of their location. The potential vessel anomalies and critical vessels make TIPAL up the renal vein the most difficult, sometimes incomplete, or unsafe procedure.
Although laparoscopic lymphadenectomy is now considered a feasible and safe procedure (11-13), the left infrarenal para-aortic area accessed via the laparoscopic approach remains a difficult and unsafe area. Several limitations of the laparoscopic approach, such as the steep learning curve due to the non-traditional surgical skills required, high reliance on adept surgical assistants, patient‘s condition (morbidly obese), or significant intra-abdominal adhesions, make it difficult to approach the infrarenal para-aortic area. With the introduction of the robotic-assisted approach, these limitations are overcoming. Robotic-assisted surgery more closely imitate open procedures and is associated with a shorter learning curve (14). The three-dimensional, magnified vision combined with wristed instrumentation, elimination of tremor, and motion scaling allows the surgeon to replicate open surgery. The robotic surgeon has the additional advantages of stable, autonomous, and precise control of the camera and instrument movements. Robotics also reduces the poor ergonomics associated with laparoscopy, which leads to surgeon's discomfort and risk of chronic musculoskeletal occupational injury, particularly during longer procedures (15).
Linear regression of time for lymphadenectomy according to number of lymph nodes retrieved, body mass index (BMI) and method of approach.
Comparisons of the operative time per retrieved lymph node according to surgical approach in pelvic (A), infrarenal para-aortic (B), and total lymphadenectom y (C). LPS: Laparoscopic.
Linear regression analysis between the number of retrieved lymph nodes and operative time in pelvic (A), infrarenal para-aortic (B), and total lymphadenectomy (C). LPS: Laparoscopic.
The objective of this study was to evaluate the clinical feasibility of robotic-assisted TIPAL by comparing the perioperative outcomes with those of the conventional laparoscopic approach in patients with gynecological malignancies. Evidence for which of the two surgical approaches has a faster intraoperative time is conflicting (16). Several series have reported a shorter operative time with the robotic-assisted approach in gynecological malignancies (15, 17-21), but they compared total operative time instead of specific time related exclusively to TIPAL. Some studies provided the operative times for TIPAL with variable and different results (7, 8, 22, 23). In our study, we compared the specific time for each lymphadenectomy and the time per retrieved lymph node between the two approaches. The robotic-assisted approach showed faster operative time for pelvic, infrarenal, para-aortic, and total lymphadenectomy. The number of retrieved pelvic lymph nodes were similar in both approaches, while the numbers of retrieved pelvic lymph nodes in infrarenal para-aortic and total lymphadenectomy were higher in the robotic-assisted group. The time per retrieved lymph node was significantly longer in the robot-assisted group in each area. Depending on BMI, the time per retrieved node in pelvic, infrarenal para-aortic, and total lymphadenectomy were constant in the robotic-assisted group, compared to laparoscopic group. We attributed the decrease in operative time and constant retrieval time regardless of BMI to the advantages and stability of the robotic system and the increased autonomy and reduced fatigue of the operator. In addition, experienced advanced surgeon through previous conventional laparoscopy and well-trained bedside assistant may be potential factors for reducing operative time in the robotic-assisted group.
Linear regression analysis between body mass index and the operative time per retrieved lymph nodes according to surgical approach in pelvic (A), infrarenal para-aortic (B), and total lymphadenectomy (C). LPS: Laparoscopic.
Six (20.7%) out of the 29 patients with cervical cancer had infrarenal node metastasis. In one patient among them, the pelvic and lower para-aortic lymph nodes were bypassed. Gil Moreno et al. reported similar results, as 16% of patients with locally advanced cervical cancer had infrarenal node involvement (5). Of the patients with endometrial cancer, three (6.9%) had infrarenal lymph node metastasis and one bypassed the lower lymph node metastasis. Meanwhile, Turan et al. reported a 10% infrarenal involvement in early endometrial cancer (25), Abu-Rustum et al. reported only 1.8% (26). Among the 17 patients with early ovarian cancer in our study, one had infrarenal para-aortic metastasis.
Our study had several limitations. Firstly, our patient selection was retrospective and not randomized. We reviewed retrospectively the records of patients with gynecological malignancies and selected the cases for which TIPAL was performed. Secondly, all surgeries were performed by a single surgeon in the same hospital. The experiences from the conventional laparoscopic approach could be a factor for reducing the operative time of the robotic approach. In addition, there is a concern that it might not be easily reproduced in a different setting, despite having significant consistency. Well-designed, prospective randomized trials are necessary for further evaluation of the feasibility and safety of robot-assisted surgery. Thirdly, the number of patients was not enough to evaluate clinical outcomes such as major complications. The prevalence of a major vessel injury in this study (2.13%) was lower than the 4.6% reported with inframesenteric para-aortic lymphadenectomy (7, 24). Control of major vessel bleeding is easier in the robotic-assisted approach. The magnified lesion, wristed instruments, and precise control enable a more comfortable and meticulous vascular suture in the robotic approach. The robotic surgery itself has several limitations based on our experience. The patient's thighs must be further lowered to prevent restriction of the robotic arm, which increases the possibility of nerve injury related with the patient's position. Other limitations include increased costs, the need for a trained and supportive team, and experienced assistant about the robotic system, and the limitations to the extent of movements of the robotic arms. In the present study, we retrieved a higher number of infrarenal para-aortic lymph nodes (up to the renal vein) in a shorter time in the robotic-assisted approach. Differently with other studies, our study showed that robotic-assisted TIPAL retrieved a higher number of infrarenal para-aortic lymph nodes, but a similar number of pelvic lymph nodes was retrieved in both approaches. The robotic-assisted approach also took less operative times for pelvic and total lymphadenectomy than laparoscopy.
In conclusion, robotic-assisted transperitoneal infrarenal para-aortic lymphadenectomy could be feasible for staging and treatment in patients with gynecological malignancies.
- Received September 17, 2017.
- Revision received October 19, 2017.
- Accepted October 23, 2017.
- Copyright© 2017, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
References
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