THE INTERNATIONAL JOURNAL OF MEDICAL ROBOTICS AND COMPUTER ASSISTED SURGERY Int J Med Robotics Comput Assist Surg 2014. Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/rcs.1583
ORIGINAL ARTICLE
Robotic versus laparoscopic rectal resection: is there any real difference? A comparative single center study
Benedetto Ielpo* Riccardo Caruso Yolanda Quijano Hipolito Duran Eduardo Diaz Isabel Fabra Catalina Oliva Sergio Olivares Valentina Ferri Ricardo Ceron Carlos Plaza Emilio Vicente Sanchinarro University Hospital, General Surgery Department, San Pablo University, CEU, Madrid, Spain *Correspondence to: B. Ielpo, Sanchinarro University Hospital, C/Oña nº 10. Madrid 28050, Spain. E-mail: [email protected]
Abstract Introduction Robotic surgery has gained worldwide acceptance in the past decade, and several studies have shown that this technique is safe and feasible. The aim of this study is to compare main outcomes of laparoscopic and robotic rectal resection. Methods In total, 143 consecutive patients treated for rectal cancer in our department with laparoscopic or robotic-assisted surgery from October 2010 to July 2013 were retrospectively analyzed. Results A total of 87 patients underwent laparoscopic rectal resection, and 56 patients were treated using a robotic approach. The conversion rate was 11.5% in the laparoscopic group and 3.5% in the robotics group (P = 0.09). The low rectal cancer conversion rate was significantly lower in the robotic group (1.8%) than in the laparoscopy group (9.2%) (P = 0.04). Mean operation time was 252 min in the laparoscopic group and 309 min in the robotic group (P = 0.023). Conclusions The robotic approach shows a lower conversion rate in low rectal cancer but with a longer operative time compared with the laparoscopic technique. Copyright © 2014 John Wiley & Sons, Ltd. Keywords
rectal cancer; robotic; laparoscopic; low anterior resection
Introduction
Accepted: 15 January 2014
Copyright © 2014 John Wiley & Sons, Ltd.
Within the last few years, robotic surgery has been gaining worldwide acceptance with an increased number of literature reports. To date, several studies have demonstrated the safety and technical feasibility of robotic colorectal resection (1); however, its real benefit is still undefined when compared with the conventional laparoscopic approach. Focusing only on rectal resection, the laparoscopic approach continues to be challenging because of the reduced anatomical space of the pelvis, especially in low rectal cancers that require a complete total mesorectal excision. This may be because the conventional laparoscopic technique has several limitations, such as 2-dimensional view, poor ergonomics, tremor and limited
B. Ielpo et al.
instrument movement. Therefore, the robotic approach could potentially overcome these limitations; nevertheless, in the literature only a few studies are currently available exclusively concerning robotic rectal surgery (2). Most of the reports are case series studies, and few of them only compare laparoscopic versus robotic surgery. The aim of this study is to present the perioperative and short-term outcomes after robotic-assisted rectal resection (RRR) and to compare the outcomes with outcomes associated with the conventional laparoscopic rectal resection (LRR) approach.
Material and Methods Between October 2010 and July 2013, a retrospective chart review was conducted for all consecutive patients with rectal adenocarcinoma who underwent curative resection in our center with minimally invasive techniques (robotic or laparoscopic). Selection of the approach depended on the availability of equipment, patient preference and familiarity of the surgeon with the robotic procedure.
Preoperative study Preoperative work-up included colonoscopy with biopsy, trans-anal endorectal ultrasound and pelvic MRI, whole body CT scan and PET-CT scan. For tumoral stage, the TNM staging system was used (American Joint Committee on Cancer) by choosing the T and N of the worst stage described by any imaging technique. For all T3 and positive lymph node cancers, neoadjuvant chemoradiotherapy was planned, and the previous work-up assessment was repeated when completed. A chemotherapy scheme was personalized for each patient according to the expression and mutations of specific tumor molecular makers analyzed by immunohistochemistry in the tumor biopsy. These patients were treated with 625 to 825 mg/m/12 h of capecitabine in combination with either irinotecan or oxaliplatin, plus either bevacizumab or cetuximab based on the previous molecular status. Radiotherapy consisted of intensity-modulated radiation (50.4 Gy) delivered in 28 fractions. Surgery was scheduled 4–6 weeks after completion of neoadjuvant treatment.
Exclusion criteria Patients were excluded from the study if they had intestinal obstruction, had tumors invading the levator ani or Copyright © 2014 John Wiley & Sons, Ltd.
external sphincter, or had T4 cancers with surrounding tissue invasion.
Data collected Main patient demographic characteristics, pre-operative TNM stage and distance from anal verge (upper rectum: 15–10 cm; mid rectum: 9–5 cm; lower rectum: < 5 cm), SUVmax value, ASA score and BMI were evaluated and compared retrospectively between both groups. Main perioperative and postoperative data, morbidity and mortality were evaluated as well as the mesorectal circumferential margin, specimen margin invasion and histological tumoral regression rate (4). Anastomosis leakage was diagnosed whenever there existed a clinical suspicion (change in the drainage, fever or abdominal pain) and this diagnosis was always corroborated by the extraluminal presence of a contrast enema observed during a control CT.
Surgical team The procedures were performed by eight surgeons, all of them with laparoscopic experience. Five of the surgeons had experience with a robotic system and had completed a training program 3 years prior to the initiation of this study. The patients were assigned to each surgeon in a non-randomized way.
Surgical procedure Concerning the robotic procedure, the patient is placed in a modified lithotomy position with legs apart. After achievement of pneumoperitoneum with a Veress needle, a 12 mm trocar is placed through an incision just above the umbilicus. A 30° optic is then introduced through the trocar to perform an abdominal cavity exploration. Three more 8-mm trocars are inserted as showed in Figure 1. The assistant port (12 mm) is placed, then the patient is placed in a 30° Trendelenburg position with the right side down at 15°, completing the docking time (Figure 1). The dissection began with a hook incision of the peritoneum at the origin of the mesosigma on the right side, from the promontory up to the origin of the inferior mesenteric artery. After ligation of the inferior mesenteric artery and vein near its origin using Hemolock, the rectum is suspended entering in the ‘holy plane’; the hypogastric nerves are identified and preserved as well as the ureters. The dissection continues circumferentially along the pelvic sidewall with total mesorectal excision when needed or divided at least 2 cm below the tumor Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
Laparoscopic Vs Robotic rectal resection
distribution, a variance analysis and Student’s t-test were used. For the rest of the variables, both Mann–Whitney and Kruskal–Wallis tests were performed. For categorical variables, a Chi-square test was performed. Results with a P value lower than 0.05 were considered statistically significant.
Results Patient characteristics
Figure 1. Robotic rectal resection. Trocars position
for upper rectum cancers with ligasure. Splenic flexure take down, when needed, was performed completely using robotics. The assistant divided the distal rectum with a reticulating 45 mm linear stapler, and the proximal colon was extracted through a Pfannenstiel incision and then divided proximal to the tumor. An anvil was inserted into the proximal stump, the colon placed back into the abdomen, the pneumoperitoneum restored and, finally, a standard end-to-end anastomosis was performed and tested with the hidro-neumonic technique. Also, 3 handrobotic intracorporeal anastomoses were performed. The laparoscopic technique was performed in a manner similar to the robotic technique. Defunctioning ileostomy was performed based on individual cases.
Post-operative follow-up Postoperative morbidity was stratified according to the Clavien–Dindo classification system (3), and severe morbidity was identified when grade ≥ III. Diagnosis of anastomotic leakage was based on clinical suspicion and confirmed by contrast enema leakage identified via CT scan. Patient follow-up assessment was performed routinely at 15 postoperative days, at month 1, 3 and 6 and finally every 6 months until 5 years postoperative. Colonoscopy was performed at the 1st and 3rd year visits. A chestabdominal-pelvic CT scan was used for the detection of loco regional or systemic recurrence at month 2 and 6 after surgery and then after every 6 months or whenever suspected.
Statistical analysis Data were analyzed using the SPSS statistical program (SPSS Inc. Chicago, IL, USA). To compare the means of the quantitative variables when these followed a normal Copyright © 2014 John Wiley & Sons, Ltd.
In this study, a total of 143 patients underwent rectal resection (87 LRR, 56 RRR). The demographic data for the patients are summarized in Table 1. None of these parameters differed significantly between the groups.
Post-operative outcomes and pathological analysis The mean operating time was significantly lower in the LRR group (mean: 252 min) compared with the RRR group (mean: 312 min) (P = 0.023). Mean intraoperative estimated blood loss and conversion rate are shown in Table 2. Conversion rate according to tumor location was statistically lower in the robotic group (1.8%) compared with the laparoscopic group (9.2%) (P = 0.04) for low rectal cancers (< 5 cm from anal verge). Conversions to an open approach in the LRR group were caused by difficult mesorectal dissection and border tumoral
Table 1. Demographic data
Age (years)a Gender: M/F (%) -2
BMI (kg m ) ASA (%) 1 2 3 Tumor location from anal verge (cm)a (range) Upper rectum Mid rectum Lower rectum TNM stage I II III IV Preoperative CRT: n (%) Preoperative SUVa
Laparoscopy (n = 87)
Robot (n = 56 )
55.7 ± 13.9 39(44.8)/ 48(55.2) 23.7 ± 2.9
43.4 ± 11 25(44.6)/ 31(55.4) 22.8 ± 2.5
16 (18.4) 59 (67.8) 12 (13.8) 7.8 ± 3.2 (1–15) 18 (20) 42 (48) 27 (31)
11 (19.6) 32 (57.1) 11 (19.6) 6.9 ± 2.6 (1–15) 13 (23) 25 (44) 18 (32)
18 (20.7) 32 (36.8) 29 (33.3) 8 (9.2) 70 (80.5) 10.6 ± 5
14 (25) 20 (35.7) 18 (32.1) 4 (7.1) 46 (82.1) 12.4 ± 8.9
P Value 0.83 0.76 0.73 0.64
0.49 0.72 0.67 0.88 0.58
0.56 0.76
BMI: body mass index, ASA: American Society of Anesthesiologists, CRT: chemoradiotherapy Values are means ± standard deviations
a
Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
B. Ielpo et al. Table 2. Operative data
Type of resection LAR LAR with stoma APR Colon Anal Conversion to open surgery Upper rectum Mid rectum Lower rectum Intraoperative blood loss (ml)a (range) Operation time (min)a (range) I period II period III period
Laparoscopy (n = 87) n (%)
Robot (n = 56) n (%)
P value
13 (14,9) 53 (60,9) 20 (23) 1 (1,1) 10 (11,5)
12 (21,4) 28 (50) 15 (26.7) 1 (1,8) 2 (3,5)
0,13 0,31 0,19 0,8 0.75 0,09
1 (1.1) 1 (1.1) 8 (9.2) 240 ± 53.7 (0-4000) 252 ± 90 (180–420)
0 1 (1.8) 1 (1.8) 280 ± 35.3 (0-4000) 309 ± 84 (150–540) 336 ± 37 312 ± 29 280 ± 45
number of hospital stay days was similar in both groups, and there were no mortality cases in either group. Pathologic characteristics are presented in Table 4. The distribution of the specimen TN stage and histological regression grade (4) did not differ significantly between the groups. The mean number of retrieved lymph nodes was 9 and 10 in the LRR and RRR group, respectively (P = 0.97). Tumor size, differentiation grade and specimen circumferential margin affectation did not differ significantly between both groups (Table 4).
0.7 0.04 0.67 0.023
LAR: low anterior resection; APR: abdominalperineal resection Values are means ± standard deviations
a
invasion in nine cases and one case, respectively. The two conversions in the RRR group were due to pneumoperitoneum intolerance and multiple peritoneal adherences. The type of resection is shown in Table 2, and no differences were found.
Discussion In the context of minimally invasive surgery, the robotic approach has clearly demonstrated important advantages over the open approach; however, its use in rectal resection, when compared with the laparoscopic technique, is still under debate. Minimally invasive surgery is still mainly represented by the laparoscopic approach (5); however, the robotic technique is receiving increasing and rapidly growing interest. It provides a 3D-amplified view to the surgeons and an increased ability to control the operative field by manipulating optics, as well as enhanced mobility and precision of instruments. The use of robotic systems in the field of rectal cancer surgery has been attempted to overcome the technical limitations of the laparoscopic approach, due to the deep narrow space where such surgeries are performed.
Post-operative and pathological results Overall post-operative complication rate was similar in both groups (Table 3). Major complications according to the Clavien–Dindo classification did not differ among the groups (5.7%: LRR, 7.1%: RRR, P = 0.73) (Table 3). The overall rate of anastomotic leakage was 4.5% in the LRR group and 9.7% in the RRR group (P = 0.35). Mean
Table 3. Postoperative mortality and morbidity
Postoperative morbidity Anastomic leakage Intraabdominal abscess Wound infection Ileus Clavien ≥ III Length of hospital stay (day)a(range) Reoperation rate Postoperative mortality
Laparoscopy (n = 87) n (%)
Robot (n = 56) n (%)
20 (23) 3 (4.5) 6 (6.9) 5 (5.7) 6 (6.9) 5 (5.7) 10 ± 3.6 (5–16) 3 (3.4) 0
15 (26.8) 4 (9.7) 4 (7.1) 3 (5.3) 4 (7.1) 4 (7.1) 13 ± 10.5 (5–60) 3 (5.3) 0
a
Values are means ± standard deviations
Copyright © 2014 John Wiley & Sons, Ltd.
P value 0.61 0.35 0.87 0.92 0.93 0.73 0.26
Table 4. Pathologic characteristics
pTNM staging Stage I Stage II Stage III No. of retrieved lymph nodesa (rango) Tumor size (cm)a R1 resection CRM ≤1 Tumoral differentiation Well Moderate Poor Tumor regression grade 4 (complete response) 3 2 1 0 (no response)
Laparoscopy (n = 87 ) n (%)
Robot (n = 56) n (%)
19 (21.8) 38 (43.6) 30 (34.5) 9 ± 4.8 (0-17) 2,2 ± 1.1 0 2 (2.3)
14 (25) 21(37.5) 21(37.5) 10 ± 8 (0-29) 2,30 ± 1.9 0 2 (3.6)
44 (50.5) 38 (43.6) 5 (5.7)
23 (41) 29 (51.8) 4 (7.1)
14 (20) 18 (25.7) 21 (30) 11 (15.7) 6 (8.6)
10 (21.7) 13 (28.2) 16 (34.8) 4 (8.7) 3 (6.5)
P value 0.32
0.97 0.49 0.32 0.39
0.73
CRM circumferential resection margin Values are means ± standard deviations
a
Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
Laparoscopic Vs Robotic rectal resection
Some studies have reported main outcomes after robotic rectal resection for cancer, but few of the studies were comparable with the laparoscopic approach (2). Furthermore, most of the studies include less than 50 patients. The main published results are that robotic rectal resection is safe and feasible with a conversion rate ranging from 0 to 9.4% and a complication rate ranging from 1 to 35.9% (2,6). In most of the studies, when robotic approach is compared with the laparoscopic group, the differences were not statistically significant (7–12). To date, the impact of robotic rectal surgery remains understudied. In the current study, we compared the short-term results of patients who underwent RRR and LRR. Results from our study showed the safety and feasibility of RRR as well as the laparoscopic approach. The mean operative time in RRR was significantly longer than that of the LRR approach. Operative time differences seem to be consistent in other studies as well (13). The docking time and the splenic flexure take down are the main causes of longer surgical robotic rectal resection time. Regarding the mobilization of the splenic flexure, our policy is to perform it only when there is difficulty in achieving a tension-free anastomosis. When needed, the splenic flexure take down can be performed with the robot approach, but it needs repositioning of the robotic cart, which increases the robotic operative time procedure. The operating time still represents a disadvantage in robotic surgery, as reported in previous studies. However, we analyzed the mean operative time of the RRR by dividing the number of RRRs into three different groups of 18 patients, each one in three consecutive periods of time, and we notice a remarkably shorter time in the last group (Table 2). Thus, obviously, operative experience quickens RRR. Conversion rate in our series showed a difference in favor of the robotic system with respect to the laparoscopic approach, although it did not reach statistical significance (P = 0.09). This result is consistent with most previous comparative studies in which conversion rate is always higher in patients who underwent laparoscopic rectal resection, although it reached statistically significant values in only a few of them (7–9). However, if we analyze the conversions in relation to tumor location, we find that patients with lower rectal cancer in the robotic group demonstrate significantly lower rates of conversion to open surgery than patients in the laparoscopic group. (P = 0.04). Therefore, RRR may find a legitimate application in the treatment of low rectal cancers. A similar result was reported by Baek et al. (14) in the context of low rectal cancers. One of the main causes of conversion in rectal resection is the inability to perform an oncological pelvic dissection in lower rectal cancers, especially in a deep narrow pelvis with previous radiotherapy; this situation, which can be a Copyright © 2014 John Wiley & Sons, Ltd.
real challenge to address if only laparoscopic instruments are available, can be improved with a robotic system according to our series and to a recent meta-analysis (15). Regarding anastomotic leakage, we found it to be slightly higher in the robotic group, however, without a significant difference (LRR: 4.5%; RRR: 9.7 P = 0.35). Nevertheless, all four of the anastomotic leaks were present in the first 20 RRR cases inside the expected learning curve; indeed, after those, no more anastomotic leaks have been recorded. It suggests that with greater experience, there is the potential for reducing technical complications. Notably, the four leaks reported occurred in male patients, in patients with low rectal tumors (< 5 cm from anal verge), and in patients with previous radiation therapy and with a minimum histological regression rate According to the literature, medians of 7.6% anastomotic leak in the robotic procedure and 7.3% in the laparoscopy procedure have been identified, without significant differences (2). However, three comparative studies found a lower rate of anastomotic leakage in the robotic group, even though it did not reached a statistically significant difference (2). Limitations of the present study were a lack of an economic comparative study, a lack of determining quality of life and the retrospective case control design, which increased the possibility of bias. Despite the results of the present and reported studies, the real benefits of RRR have yet to be ruled out. We underline that the robotic technique has to be considered as a system, allowing the integration of further applications, such as immunofluorescence (16) and the identification of sentinel lymph nodes (17) that may potentially enhance the oncological results of RRR. Moreover, the robotic system may simplify the use of other minimally invasive procedures, such as SILS and TEM (18,19). Once these future applications have been studied, we think we will finally find the real advantages of the robotic approach in rectal cancer resection. The ongoing international ROLARR (Robotic versus laparoscopic resection for rectal cancer) (20) study aims to clarify these issues. In conclusion, given the previous results, RRR has proved to be as safe as the conventional LRR approach. The operating time represents a disadvantage for robotic surgery; however, our results show that this might be overcome with increased experience. Furthermore, RRR shows a lower conversion rate when a tumor is located 5 cm below the anal verge.
Acknowledgements Thanks to Pablo Ruiz and Isabel de Salas for their contribution. Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
B. Ielpo et al.
Conflict of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
Funding No specific funding.
References 1. Baek SK, Carmichael JC, Pigazzi A. Robotic surgery: colon and rectum. Cancer J 2013; 19: 140–146. 2. Scarpinata R, Aly EH. Does robotic rectal cancer surgery offer improved early postoperative outcomes? Dis Colon Rectum 2013; 56: 253–262. 3. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004; 240: 205–213. 4. Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis 1997; 12: 19–23. 5. Halabi WJ, Kang CY, Jafari MD, et al. Robotic-assisted colorectal surgery in the United States: a nationwide analysis of trends and outcomes. World J Surg 2013; (Epub ahead of print). 6. Du XH, Shen D, Li R, et al. Robotic anterior resection of rectal cancer: technique and early outcome. Chinese Med J 2013; 126: 51–54. 7. Baek JH, Pastor C, Pigazzi A. Robotic and laparoscopic total mesorectal excision for rectal cancer: a case-matched study. Surg Endosc 2011; 25: 521–525. 8. Baik SH, Kwon HY, Kim JS. Robotic versus laparoscopic low anterior resection of rectal cancer: short-term outcome of a prospective comparative study. Ann Surg Oncol 2009; 16: 1480–1487.
Copyright © 2014 John Wiley & Sons, Ltd.
9. Patriti A, Ceccarelli G, Bartoli A, et al. Short- and medium-term outcome of robot-assisted and traditional laparoscopic rectal resection. JSLS 2009; 13: 176–183. 10. Bianchi PP, Ceriani C, Locatelli A, et al. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a comparative analysis of oncological safety and short-term outcomes. Surg Endosc 2010; 24: 2888–2894. 11. Park JS, Choi GS, Lim KH, et al. Robotic-assisted versus laparoscopic surgery for low rectal cancer: case-matched analysis of short-term outcomes. Ann Surg Oncol 2010; 17: 3195–3202. 12. Kwak JM, Kim SH, Kim J, et al. Robotic vs laparoscopic resection of rectal cancer: short-term outcomes of a case-control study. Dis Colon Rectum 2011; 54: 151–156. 13. Erguner I, Aytac E, Boler DE, et al. What have we gained by performing robotic rectal resection? Evaluation of 64 consecutive patients who underwent laparoscopic or robotic low anterior resection for rectal adenocarcinoma. Surg Laparosc Endosc Percutan Technol 2013; 23: 316–319. 14. Baek SJ, Al-Asari S, Jeong DH, et al. Robotic versus laparoscopic coloanal anastomosis with or without intersphincteric resection for rectal cancer. Surg Endosc 2013; 25 (Epub ahead of print). 15. Ortiz-Oshiro E, Sánchez-Egido I, Moreno-Sierra J, et al. Robotic assistance may reduce conversion to open in rectal carcinoma laparoscopic surgery: systematic review and meta-analysis. Int J Med Robot 2012; 8: 360–370. 16. Jafari MD, Lee KH, Halabi WJ, et al. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 2013; 27: 3003–3008. 17. Marano A, Priora F, Lenti LM, et al. Application of fluorescence in robotic general surgery: review of the literature and state of the art. World J Surg 2013; 4: (Epub ahead of print). 18. Gonzalez AM, Rabaza JR, Donkor C, et al. Single-incision cholecystectomy: a comparative study of standard laparoscopic, robotic, and SPIDER platforms. Surg Endosc 2013; (Epub ahead of print). 19. Bardakcioglu O. Robotic transanal access surgery. Surg Endosc 2013; 27: 1407–1409. 20. Collinson FJ, Jayne DG, Pigazzi A, Tsang C, et al. An international, multicentre, prospective, randomized, controlled, unblinded, parallel-group trial of robotic-assisted versus standard laparoscopic surgery for the curative treatment of rectal cancer. Int J Color Dis 2012; 27: 233–241.
Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
ORIGINAL ARTICLE
Robotic versus laparoscopic rectal resection: is there any real difference? A comparative single center study
Benedetto Ielpo* Riccardo Caruso Yolanda Quijano Hipolito Duran Eduardo Diaz Isabel Fabra Catalina Oliva Sergio Olivares Valentina Ferri Ricardo Ceron Carlos Plaza Emilio Vicente Sanchinarro University Hospital, General Surgery Department, San Pablo University, CEU, Madrid, Spain *Correspondence to: B. Ielpo, Sanchinarro University Hospital, C/Oña nº 10. Madrid 28050, Spain. E-mail: [email protected]
Abstract Introduction Robotic surgery has gained worldwide acceptance in the past decade, and several studies have shown that this technique is safe and feasible. The aim of this study is to compare main outcomes of laparoscopic and robotic rectal resection. Methods In total, 143 consecutive patients treated for rectal cancer in our department with laparoscopic or robotic-assisted surgery from October 2010 to July 2013 were retrospectively analyzed. Results A total of 87 patients underwent laparoscopic rectal resection, and 56 patients were treated using a robotic approach. The conversion rate was 11.5% in the laparoscopic group and 3.5% in the robotics group (P = 0.09). The low rectal cancer conversion rate was significantly lower in the robotic group (1.8%) than in the laparoscopy group (9.2%) (P = 0.04). Mean operation time was 252 min in the laparoscopic group and 309 min in the robotic group (P = 0.023). Conclusions The robotic approach shows a lower conversion rate in low rectal cancer but with a longer operative time compared with the laparoscopic technique. Copyright © 2014 John Wiley & Sons, Ltd. Keywords
rectal cancer; robotic; laparoscopic; low anterior resection
Introduction
Accepted: 15 January 2014
Copyright © 2014 John Wiley & Sons, Ltd.
Within the last few years, robotic surgery has been gaining worldwide acceptance with an increased number of literature reports. To date, several studies have demonstrated the safety and technical feasibility of robotic colorectal resection (1); however, its real benefit is still undefined when compared with the conventional laparoscopic approach. Focusing only on rectal resection, the laparoscopic approach continues to be challenging because of the reduced anatomical space of the pelvis, especially in low rectal cancers that require a complete total mesorectal excision. This may be because the conventional laparoscopic technique has several limitations, such as 2-dimensional view, poor ergonomics, tremor and limited
B. Ielpo et al.
instrument movement. Therefore, the robotic approach could potentially overcome these limitations; nevertheless, in the literature only a few studies are currently available exclusively concerning robotic rectal surgery (2). Most of the reports are case series studies, and few of them only compare laparoscopic versus robotic surgery. The aim of this study is to present the perioperative and short-term outcomes after robotic-assisted rectal resection (RRR) and to compare the outcomes with outcomes associated with the conventional laparoscopic rectal resection (LRR) approach.
Material and Methods Between October 2010 and July 2013, a retrospective chart review was conducted for all consecutive patients with rectal adenocarcinoma who underwent curative resection in our center with minimally invasive techniques (robotic or laparoscopic). Selection of the approach depended on the availability of equipment, patient preference and familiarity of the surgeon with the robotic procedure.
Preoperative study Preoperative work-up included colonoscopy with biopsy, trans-anal endorectal ultrasound and pelvic MRI, whole body CT scan and PET-CT scan. For tumoral stage, the TNM staging system was used (American Joint Committee on Cancer) by choosing the T and N of the worst stage described by any imaging technique. For all T3 and positive lymph node cancers, neoadjuvant chemoradiotherapy was planned, and the previous work-up assessment was repeated when completed. A chemotherapy scheme was personalized for each patient according to the expression and mutations of specific tumor molecular makers analyzed by immunohistochemistry in the tumor biopsy. These patients were treated with 625 to 825 mg/m/12 h of capecitabine in combination with either irinotecan or oxaliplatin, plus either bevacizumab or cetuximab based on the previous molecular status. Radiotherapy consisted of intensity-modulated radiation (50.4 Gy) delivered in 28 fractions. Surgery was scheduled 4–6 weeks after completion of neoadjuvant treatment.
Exclusion criteria Patients were excluded from the study if they had intestinal obstruction, had tumors invading the levator ani or Copyright © 2014 John Wiley & Sons, Ltd.
external sphincter, or had T4 cancers with surrounding tissue invasion.
Data collected Main patient demographic characteristics, pre-operative TNM stage and distance from anal verge (upper rectum: 15–10 cm; mid rectum: 9–5 cm; lower rectum: < 5 cm), SUVmax value, ASA score and BMI were evaluated and compared retrospectively between both groups. Main perioperative and postoperative data, morbidity and mortality were evaluated as well as the mesorectal circumferential margin, specimen margin invasion and histological tumoral regression rate (4). Anastomosis leakage was diagnosed whenever there existed a clinical suspicion (change in the drainage, fever or abdominal pain) and this diagnosis was always corroborated by the extraluminal presence of a contrast enema observed during a control CT.
Surgical team The procedures were performed by eight surgeons, all of them with laparoscopic experience. Five of the surgeons had experience with a robotic system and had completed a training program 3 years prior to the initiation of this study. The patients were assigned to each surgeon in a non-randomized way.
Surgical procedure Concerning the robotic procedure, the patient is placed in a modified lithotomy position with legs apart. After achievement of pneumoperitoneum with a Veress needle, a 12 mm trocar is placed through an incision just above the umbilicus. A 30° optic is then introduced through the trocar to perform an abdominal cavity exploration. Three more 8-mm trocars are inserted as showed in Figure 1. The assistant port (12 mm) is placed, then the patient is placed in a 30° Trendelenburg position with the right side down at 15°, completing the docking time (Figure 1). The dissection began with a hook incision of the peritoneum at the origin of the mesosigma on the right side, from the promontory up to the origin of the inferior mesenteric artery. After ligation of the inferior mesenteric artery and vein near its origin using Hemolock, the rectum is suspended entering in the ‘holy plane’; the hypogastric nerves are identified and preserved as well as the ureters. The dissection continues circumferentially along the pelvic sidewall with total mesorectal excision when needed or divided at least 2 cm below the tumor Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
Laparoscopic Vs Robotic rectal resection
distribution, a variance analysis and Student’s t-test were used. For the rest of the variables, both Mann–Whitney and Kruskal–Wallis tests were performed. For categorical variables, a Chi-square test was performed. Results with a P value lower than 0.05 were considered statistically significant.
Results Patient characteristics
Figure 1. Robotic rectal resection. Trocars position
for upper rectum cancers with ligasure. Splenic flexure take down, when needed, was performed completely using robotics. The assistant divided the distal rectum with a reticulating 45 mm linear stapler, and the proximal colon was extracted through a Pfannenstiel incision and then divided proximal to the tumor. An anvil was inserted into the proximal stump, the colon placed back into the abdomen, the pneumoperitoneum restored and, finally, a standard end-to-end anastomosis was performed and tested with the hidro-neumonic technique. Also, 3 handrobotic intracorporeal anastomoses were performed. The laparoscopic technique was performed in a manner similar to the robotic technique. Defunctioning ileostomy was performed based on individual cases.
Post-operative follow-up Postoperative morbidity was stratified according to the Clavien–Dindo classification system (3), and severe morbidity was identified when grade ≥ III. Diagnosis of anastomotic leakage was based on clinical suspicion and confirmed by contrast enema leakage identified via CT scan. Patient follow-up assessment was performed routinely at 15 postoperative days, at month 1, 3 and 6 and finally every 6 months until 5 years postoperative. Colonoscopy was performed at the 1st and 3rd year visits. A chestabdominal-pelvic CT scan was used for the detection of loco regional or systemic recurrence at month 2 and 6 after surgery and then after every 6 months or whenever suspected.
Statistical analysis Data were analyzed using the SPSS statistical program (SPSS Inc. Chicago, IL, USA). To compare the means of the quantitative variables when these followed a normal Copyright © 2014 John Wiley & Sons, Ltd.
In this study, a total of 143 patients underwent rectal resection (87 LRR, 56 RRR). The demographic data for the patients are summarized in Table 1. None of these parameters differed significantly between the groups.
Post-operative outcomes and pathological analysis The mean operating time was significantly lower in the LRR group (mean: 252 min) compared with the RRR group (mean: 312 min) (P = 0.023). Mean intraoperative estimated blood loss and conversion rate are shown in Table 2. Conversion rate according to tumor location was statistically lower in the robotic group (1.8%) compared with the laparoscopic group (9.2%) (P = 0.04) for low rectal cancers (< 5 cm from anal verge). Conversions to an open approach in the LRR group were caused by difficult mesorectal dissection and border tumoral
Table 1. Demographic data
Age (years)a Gender: M/F (%) -2
BMI (kg m ) ASA (%) 1 2 3 Tumor location from anal verge (cm)a (range) Upper rectum Mid rectum Lower rectum TNM stage I II III IV Preoperative CRT: n (%) Preoperative SUVa
Laparoscopy (n = 87)
Robot (n = 56 )
55.7 ± 13.9 39(44.8)/ 48(55.2) 23.7 ± 2.9
43.4 ± 11 25(44.6)/ 31(55.4) 22.8 ± 2.5
16 (18.4) 59 (67.8) 12 (13.8) 7.8 ± 3.2 (1–15) 18 (20) 42 (48) 27 (31)
11 (19.6) 32 (57.1) 11 (19.6) 6.9 ± 2.6 (1–15) 13 (23) 25 (44) 18 (32)
18 (20.7) 32 (36.8) 29 (33.3) 8 (9.2) 70 (80.5) 10.6 ± 5
14 (25) 20 (35.7) 18 (32.1) 4 (7.1) 46 (82.1) 12.4 ± 8.9
P Value 0.83 0.76 0.73 0.64
0.49 0.72 0.67 0.88 0.58
0.56 0.76
BMI: body mass index, ASA: American Society of Anesthesiologists, CRT: chemoradiotherapy Values are means ± standard deviations
a
Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
B. Ielpo et al. Table 2. Operative data
Type of resection LAR LAR with stoma APR Colon Anal Conversion to open surgery Upper rectum Mid rectum Lower rectum Intraoperative blood loss (ml)a (range) Operation time (min)a (range) I period II period III period
Laparoscopy (n = 87) n (%)
Robot (n = 56) n (%)
P value
13 (14,9) 53 (60,9) 20 (23) 1 (1,1) 10 (11,5)
12 (21,4) 28 (50) 15 (26.7) 1 (1,8) 2 (3,5)
0,13 0,31 0,19 0,8 0.75 0,09
1 (1.1) 1 (1.1) 8 (9.2) 240 ± 53.7 (0-4000) 252 ± 90 (180–420)
0 1 (1.8) 1 (1.8) 280 ± 35.3 (0-4000) 309 ± 84 (150–540) 336 ± 37 312 ± 29 280 ± 45
number of hospital stay days was similar in both groups, and there were no mortality cases in either group. Pathologic characteristics are presented in Table 4. The distribution of the specimen TN stage and histological regression grade (4) did not differ significantly between the groups. The mean number of retrieved lymph nodes was 9 and 10 in the LRR and RRR group, respectively (P = 0.97). Tumor size, differentiation grade and specimen circumferential margin affectation did not differ significantly between both groups (Table 4).
0.7 0.04 0.67 0.023
LAR: low anterior resection; APR: abdominalperineal resection Values are means ± standard deviations
a
invasion in nine cases and one case, respectively. The two conversions in the RRR group were due to pneumoperitoneum intolerance and multiple peritoneal adherences. The type of resection is shown in Table 2, and no differences were found.
Discussion In the context of minimally invasive surgery, the robotic approach has clearly demonstrated important advantages over the open approach; however, its use in rectal resection, when compared with the laparoscopic technique, is still under debate. Minimally invasive surgery is still mainly represented by the laparoscopic approach (5); however, the robotic technique is receiving increasing and rapidly growing interest. It provides a 3D-amplified view to the surgeons and an increased ability to control the operative field by manipulating optics, as well as enhanced mobility and precision of instruments. The use of robotic systems in the field of rectal cancer surgery has been attempted to overcome the technical limitations of the laparoscopic approach, due to the deep narrow space where such surgeries are performed.
Post-operative and pathological results Overall post-operative complication rate was similar in both groups (Table 3). Major complications according to the Clavien–Dindo classification did not differ among the groups (5.7%: LRR, 7.1%: RRR, P = 0.73) (Table 3). The overall rate of anastomotic leakage was 4.5% in the LRR group and 9.7% in the RRR group (P = 0.35). Mean
Table 3. Postoperative mortality and morbidity
Postoperative morbidity Anastomic leakage Intraabdominal abscess Wound infection Ileus Clavien ≥ III Length of hospital stay (day)a(range) Reoperation rate Postoperative mortality
Laparoscopy (n = 87) n (%)
Robot (n = 56) n (%)
20 (23) 3 (4.5) 6 (6.9) 5 (5.7) 6 (6.9) 5 (5.7) 10 ± 3.6 (5–16) 3 (3.4) 0
15 (26.8) 4 (9.7) 4 (7.1) 3 (5.3) 4 (7.1) 4 (7.1) 13 ± 10.5 (5–60) 3 (5.3) 0
a
Values are means ± standard deviations
Copyright © 2014 John Wiley & Sons, Ltd.
P value 0.61 0.35 0.87 0.92 0.93 0.73 0.26
Table 4. Pathologic characteristics
pTNM staging Stage I Stage II Stage III No. of retrieved lymph nodesa (rango) Tumor size (cm)a R1 resection CRM ≤1 Tumoral differentiation Well Moderate Poor Tumor regression grade 4 (complete response) 3 2 1 0 (no response)
Laparoscopy (n = 87 ) n (%)
Robot (n = 56) n (%)
19 (21.8) 38 (43.6) 30 (34.5) 9 ± 4.8 (0-17) 2,2 ± 1.1 0 2 (2.3)
14 (25) 21(37.5) 21(37.5) 10 ± 8 (0-29) 2,30 ± 1.9 0 2 (3.6)
44 (50.5) 38 (43.6) 5 (5.7)
23 (41) 29 (51.8) 4 (7.1)
14 (20) 18 (25.7) 21 (30) 11 (15.7) 6 (8.6)
10 (21.7) 13 (28.2) 16 (34.8) 4 (8.7) 3 (6.5)
P value 0.32
0.97 0.49 0.32 0.39
0.73
CRM circumferential resection margin Values are means ± standard deviations
a
Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
Laparoscopic Vs Robotic rectal resection
Some studies have reported main outcomes after robotic rectal resection for cancer, but few of the studies were comparable with the laparoscopic approach (2). Furthermore, most of the studies include less than 50 patients. The main published results are that robotic rectal resection is safe and feasible with a conversion rate ranging from 0 to 9.4% and a complication rate ranging from 1 to 35.9% (2,6). In most of the studies, when robotic approach is compared with the laparoscopic group, the differences were not statistically significant (7–12). To date, the impact of robotic rectal surgery remains understudied. In the current study, we compared the short-term results of patients who underwent RRR and LRR. Results from our study showed the safety and feasibility of RRR as well as the laparoscopic approach. The mean operative time in RRR was significantly longer than that of the LRR approach. Operative time differences seem to be consistent in other studies as well (13). The docking time and the splenic flexure take down are the main causes of longer surgical robotic rectal resection time. Regarding the mobilization of the splenic flexure, our policy is to perform it only when there is difficulty in achieving a tension-free anastomosis. When needed, the splenic flexure take down can be performed with the robot approach, but it needs repositioning of the robotic cart, which increases the robotic operative time procedure. The operating time still represents a disadvantage in robotic surgery, as reported in previous studies. However, we analyzed the mean operative time of the RRR by dividing the number of RRRs into three different groups of 18 patients, each one in three consecutive periods of time, and we notice a remarkably shorter time in the last group (Table 2). Thus, obviously, operative experience quickens RRR. Conversion rate in our series showed a difference in favor of the robotic system with respect to the laparoscopic approach, although it did not reach statistical significance (P = 0.09). This result is consistent with most previous comparative studies in which conversion rate is always higher in patients who underwent laparoscopic rectal resection, although it reached statistically significant values in only a few of them (7–9). However, if we analyze the conversions in relation to tumor location, we find that patients with lower rectal cancer in the robotic group demonstrate significantly lower rates of conversion to open surgery than patients in the laparoscopic group. (P = 0.04). Therefore, RRR may find a legitimate application in the treatment of low rectal cancers. A similar result was reported by Baek et al. (14) in the context of low rectal cancers. One of the main causes of conversion in rectal resection is the inability to perform an oncological pelvic dissection in lower rectal cancers, especially in a deep narrow pelvis with previous radiotherapy; this situation, which can be a Copyright © 2014 John Wiley & Sons, Ltd.
real challenge to address if only laparoscopic instruments are available, can be improved with a robotic system according to our series and to a recent meta-analysis (15). Regarding anastomotic leakage, we found it to be slightly higher in the robotic group, however, without a significant difference (LRR: 4.5%; RRR: 9.7 P = 0.35). Nevertheless, all four of the anastomotic leaks were present in the first 20 RRR cases inside the expected learning curve; indeed, after those, no more anastomotic leaks have been recorded. It suggests that with greater experience, there is the potential for reducing technical complications. Notably, the four leaks reported occurred in male patients, in patients with low rectal tumors (< 5 cm from anal verge), and in patients with previous radiation therapy and with a minimum histological regression rate According to the literature, medians of 7.6% anastomotic leak in the robotic procedure and 7.3% in the laparoscopy procedure have been identified, without significant differences (2). However, three comparative studies found a lower rate of anastomotic leakage in the robotic group, even though it did not reached a statistically significant difference (2). Limitations of the present study were a lack of an economic comparative study, a lack of determining quality of life and the retrospective case control design, which increased the possibility of bias. Despite the results of the present and reported studies, the real benefits of RRR have yet to be ruled out. We underline that the robotic technique has to be considered as a system, allowing the integration of further applications, such as immunofluorescence (16) and the identification of sentinel lymph nodes (17) that may potentially enhance the oncological results of RRR. Moreover, the robotic system may simplify the use of other minimally invasive procedures, such as SILS and TEM (18,19). Once these future applications have been studied, we think we will finally find the real advantages of the robotic approach in rectal cancer resection. The ongoing international ROLARR (Robotic versus laparoscopic resection for rectal cancer) (20) study aims to clarify these issues. In conclusion, given the previous results, RRR has proved to be as safe as the conventional LRR approach. The operating time represents a disadvantage for robotic surgery; however, our results show that this might be overcome with increased experience. Furthermore, RRR shows a lower conversion rate when a tumor is located 5 cm below the anal verge.
Acknowledgements Thanks to Pablo Ruiz and Isabel de Salas for their contribution. Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
B. Ielpo et al.
Conflict of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
Funding No specific funding.
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Int J Med Robotics Comput Assist Surg 2014. DOI: 10.1002/rcs
