Randomized clinical trial of single-incision versus multiport laparoscopic colectomy

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1 Randomized clinical trial Randomized clinical trial of single-incision versus multiport laparoscopic colectomy J. Watanabe 1,M.Ota 2, S. Fujii 2,H.Suwa 2, A. Ishibe 3 and I. Endo 3 1 Department of Surgery, Yokosuka Kyosai Hospital, Yokosuka, 2 Department of Surgery, Gastroenterological Centre, Yokohama City University, and 3 Department of Gastroenterological Surgery, Yokohama City University Graduate School of Medicine, Yokohama, Japan Correspondence to: Dr J. Watanabe, Department of Surgery, Yokosuka Kyosai Hospital, 1 16 Yonegahama Street, Yokosuka , Japan ( nabe-jun@comet.ocn.ne.jp) Background: The efficacy and safety of single-incision laparoscopic colectomy (SILC) for colonic cancer remain unclear. The aim of this study was to determine the outcomes of SILC compared with multiport laparoscopic colectomy (MPLC) for colonic cancer. Methods: Patients with histologically proven colonic carcinoma located in the caecum, ascending, sigmoid or rectosigmoid colon, clinically diagnosed as stage 0 III by CT, were eligible for this study. Patients were randomized before surgery and underwent tumour dissection with complete mesocolic excision. Safety analyses were conducted according to randomization groups. Results: A total of 200 patients were enrolled and randomized to the MPLC (100 patients) or SILC (100 patients) arm. Surgical outcomes were similar between the MPLC and SILC arms, including duration of operation (mean 162 versus 156 min respectively; P = 0 273), blood loss (mean 8 8 versus 21 4ml; P = 0 102), conversion to open laparotomy (2 0 versus 1 0 per cent; P = 0 561), reoperation (3 0 versus 3 0 per cent; P = 1 000), time to first flatus (both median 1 day; P = 0 155) and postoperative hospital stay (both median 6; P = 0 372). The total skin incision length was significantly shorter in the SILC arm (mean 4 4cmversus 6 8cmintheMPLCarm;P < 0 001). The median duration of analgesia use was 5 days in the MPLC and 4 days in the SILC arm (P = 0 485). Overall complication rates were equivalent (15 0 versus 12 0 per cent respecitvely; P = 0 680). Conclusion: SILC is not superior to MPLC. Registration number: UMIN ( Paper accepted 18 April 2016 Published online 10 August 2016 in Wiley Online Library ( DOI: /bjs Introduction Laparoscopic surgery is now an accepted treatment for colonic cancer 1 9. Many small-scale retrospective studies have reported the safety and feasibility of singleincision laparoscopic colectomy (SILC) compared with the short-term results of multiport laparoscopic colectomy (MPLC) However, SILC is limited technically owing to instrument crowding, inline viewing and insufficient countertraction, which can increase the amount of stress experienced by surgeons Meta-analyses 22,23 of comparative studies of SILC versus MPLC have shown the safety, feasibility and effectiveness of SILC when performed by highly skilled laparoscopic surgeons. However, the available SILC data are subject to significant bias because the studies reported were non-randomized and retrospective in design. Additionally, there was significant study population heterogeneity regarding the indications for surgery and use of instruments. The strength of the clinical evidence is weak in the absence of RCTs 24.The aim of this study was to determine the short-term surgical outcomes of SILC compared with MLC for colonic cancer by conducting an RCT. Methods This open-label, multi-institutional, randomized, two-arm (SILC and MPLC) trial was conducted within the framework of the Yokohama Clinical Oncology Group (YCOG) in Japan. Patients were enrolled at three institutions of the YCOG. The study protocol was approved by the Ethical Advisory Committee of Yokohama City University School of Medicine and the institutional review board of each participating hospital before the study was initiated. The trial 2016 BJS Society Ltd BJS 2016; 103:

2 Single-incision versus multiport laparoscopic colectomy 1277 Table 1 Study inclusion and exclusion criteria Inclusion criteria Informed consent Clinical stage 0 III adenocarcinoma Curative procedure planned Tumour location in caecum, ascending, sigmoid or rectosigmoid colon Tumour length 4 0cmorless Patient aged years Performance status ECOG 0 1 No previous gastrointestinal surgery apart from appendicectomy No organ dysfunction or blood abnormality White blood cell count 3000/mm 3 and /mm 3 Platelet count /mm 3 Haemoglobin 9 0 g/dl AST and ALT 2 5 times standard upper value Serum total bilirubin 1 5mg/dl Serum creatinine 1 5mg/dl Exclusion criteria Hypersensitivity to flomoxef Multiple cancers (simultaneous or metachronous multiple cancers with disease-free interval 5 years) Active infectious disease Past history of mental disease and/or central nervous system damage Pregnant, lactating or possibility of pregnancy Severe concomitant disease (cardiorespiratory dysfunction, renal failure, intestinal paralysis, intestinal obstruction, uncontrolled diabetes mellitus, liver cirrhosis and chronic hepatitis B and C, etc.) History of organ transplantation Preoperative treatment (chemotherapy, radiation therapy, hormone therapy, etc.) for colorectal cancer Patient judged inappropriate for enrolment in trial by an investigator ECOG, Eastern Cooperative Oncology Group; AST, aspartate aminotransferase; ALT, alanine aminotransferase. was registered with the Japanese Clinical Trials Registry as UMIN ( and all patients provided written informed consent before enrolling in the study. Patients with colonic carcinoma located in the caecum, ascending colon, sigmoid colon or rectosigmoid with histologically proven adenocarcinoma or signet-ring cell carcinoma stage 0 III, according to the UICC TMN classification (7th edition) 25 by CT, were eligible for this study. The inclusion and exclusion criteria are listed in Table 1. Randomization and masking Randomization and data handling were performed by the Department of Biostatistics and Epidemiology Data Centre of Yokohama City University. After confirming the inclusion/exclusion criteria and obtaining written informed consent, patients were randomized by means of computerized randomization following a fax to the data centre on the morning of surgery. The allocated procedure was not concealed from investigators or patients. The sizes of the groups were balanced using the minimization method according to sex, age (less than 65 years, 65 years or more) and clinical stage (stage 0 II, III). Procedure Five surgeons who were qualified based on the endoscopic surgical skill qualification system of the Japan Society for Endoscopic Surgery were accredited by the study chair 26. Before the trial, the surgeons had performed 47, 26, 16, 14 and ten SILCs (median 16 (range 10 47) per surgeon). None had previous experience with other single-incision laparoscopic procedures. In both arms, complete mesocolic excision (CME) with central vascular ligation (CVL) was undertaken. In right hemicolectomy for right-sided colonic cancer, dissection of the entire right mesocolon was performed by ligating the origin of the ileocolic, right colic and middle colic vessels. In operations for left-sided colonic cancer, dissection of the entire sigmoid or rectosigmoid mesocolon was carried out by ligating the origin of the inferior mesenteric artery. In patients with rectosigmoid colonic cancer, the mesorectum at least 5 cm distal to the lesion was removed. The SILC procedure was performed with standard laparoscopic instruments through an initial 2 3-cm extraction incision in the umbilicus. A multichannel access device (EZ Access; Hakko, Nagano, Japan) was fitted into the incision and all trocars (12-mm port used for camera, 2 5-mm ports used for device insertion) were passed through a special platform via a single wound. A multichannel access device was rotated to achieve the ideal operative view and triangulation, and to avoid or resolve crowding of the instruments. An additional 12-mm trocar was placed in the right lower quadrant when it was technically difficult to cut the lower rectum from the umbilicus. A drainage tube was inserted as necessary. Conversion to multiport surgery was defined as the addition of two or more trocars. The MPLC procedure was performed using five ports: a 12-mm port in the umbilical region, 5-mm ports in the upper right, left and lower left quadrants, and a 12-mm port in the lower right quadrant. A 12-mm umbilical trocar was used as a camera port for a rigid scope. Conversion to open surgery was defined by a wound length measuring 8 cm or greater. In both arms, CVL and colon or rectum mobilization were performed laparoscopically. The specimen was extracted through the umbilical port, which was extended

3 1278 J. Watanabe, M. Ota, S. Fujii, H. Suwa, A. Ishibe and I. Endo Randomized n = 200 Enrolment Allocation Allocated to MPLC n = 100 Received allocated intervention n = 100 Conversion to open surgery n = 2 Did not receive allocated intervention n = 0 Allocated to SILC n = 100 Received allocated intervention n = 100 Additional trocar n = 9 Conversion to open surgery n = 1 Did not receive allocated intervention n = 0 Follow-up Lost to follow-upn = 0 Discontinued intervention n = 0 Lost to follow-up n = 0 Discontinued intervention n = 0 Analysis Analysed n = 100 Analysed n = 100 Fig. 1 CONSORT diagram for the trial. MPLC, multiport laparoscopic colectomy; SILC, single-incision laparoscopic colectomy to approximately 2 5 cm. To avoid contamination, a wound protector was used in each patient. For anterior resection, an Endo GIA TM Universal (Covidien, Norwalk, Connecticut, USA), an Endo GIA TM Radial Reload (Covidien) or an Echelon TM 60 (Ethicon Endo-Surgery, Cincinnati, Ohio, USA) stapler was used for distal colon transection. Anastomosis was performed with a double-stapling technique with an ILS TM (Ethicon Endo-Surgery) intracorporeally. In the other colectomies, a functional end-to-end anastomosis was constructed using the Endo GIA TM Universal or Echelon TM 60 device extracorporeally. Perioperative care Admission was scheduled for the day before surgery. Preoperative mechanical bowel preparation was not performed. The duration of preoperative fasting was 2 h for liquids and 6 8 h for solids. One dose of prophylactic intravenous antibiotics (flomoxef; Shionogi, Osaka, Japan) was administered during induction of anaesthesia, and an additional dose after 3 h of surgery if needed. Intermittent pneumatic compression was carried out during surgery and continued until the patient was fully ambulatory in order to prevent deep vein thrombosis. The nasogastric tube was removed within 24 h of operation. Postoperative oral liquid intake was typically authorized from the day after surgery and a normal diet was resumed on postoperative day 2. The intravenous catheter was removed when enteral feeding was possible without nausea and vomiting. Mobilization of patients was promoted on postoperative day 1. Endpoints The primary outcome of this study was the incidence of postoperative complications within 30 days. Secondary outcomes were duration of surgery, blood loss, wound length, conversion rate, proximal margin, distal margin, number of lymph nodes dissected, time to first flatus, defaecation and dietary intake, analgesic use up to postoperative day 5, length of postoperative hospital stay, reoperation, mortality and disease-free survival 5 years after surgery. Disease-free survival 5 years after surgery will be reported after termination of follow-up. Statistical analysis A power analysis determined that 95 patients would be required to demonstrate a reduction in the incidence of postoperative complications within 30 days from 25 to 10 per cent at a significance level of 5 per cent and power of 80 per cent. Continuous data are presented as mean(s.d.) or median (i.q.r.). Differences between categorical variables were compared with Pearson s χ 2 test, and differences between continuous variables were analysed using the Mann Whitney U test. P < was considered statistically significant. Statistical analysis was performed using the SPSS statistical software program (IBM, Armonk, New York, USA). Results Between 1 March 2012 and 31 March 2015, a total of 200 patients were enrolled in the study, 100 to each arm

4 Single-incision versus multiport laparoscopic colectomy 1279 Table 2 Clinicopathological characteristics MPLC (n = 100) SILC (n = 100) Age (years)* 66 6(8 9) 66 7(8 8) Sex ratio (M : F) 56 : : 44 BMI (kg/m 2 )* 23 2(3 3) 23 1(3 3) ECOG performance status 0 97 (97 0) 99 (99 0) 1 3 (3 0) 1 (1 0) 2 0 (0) 0 (0) 3 0 (0) 0 (0) ASA grade I 22 (22 0) 29 (29 0) II 78 (78 0) 71 (71 0) III 0 (0) 0 (0) Albumin (g/dl)* 4 4(0 3) 4 4(0 3) Tumour diameter (mm)* 27 7(17 8) 27 5(17 1) Location Caecum 9 (9 0) 16 (16 0) Ascending colon 21 (21 0) 21 (21 0) Sigmoid colon 54 (54 0) 49 (49 0) Rectosigmoid 16 (16 0) 14 (14 0) UICC stage 0 I 54 (54 0) 56 (56 0) II 25 (25 0) 16 (16 0) III 21 (21 0) 28 (28 0) Values in parentheses are percentages unless indicated otherwise; *values are mean(s.d.). MPLC, multiport laparoscopic colectomy; SILC, single-incision laparoscopic colectomy; ECOG, Eastern Cooperative Oncology Group. Table 3 Surgical data and outcomes MPLC (n = 100) SILC (n = 100) P Duration of operation (min)* 162(36) 156(37) Blood loss (ml)* 8 8(19 3) 21 4(74 6) Wound length (cm)* Umbilical incision 4 3(1 2) 4 2(2 4) Total incision 6 8(1 3) 4 4(2 5) < Additional trocar Yes 9 (9 0) No 91 (91 0) Conversion Yes 2 (2 0) 1 (1 0) No 98 (98 0) 99 (99 0) Proximal margin (mm)* 102(45) 108(48) Distal margin (mm)* 92(54) 99(53) No. of lymph nodes 24 1(11 0) 25 5(11 4) harvested* Time to first flatus (days) 1(1 2) 1(1 2) Time to first defaecation 3(2 4) 3(2 3) (days) Time to dietary intake (days) 2(2 3) 2(2 3) Analgesia use until POD Yes 43 (43 0) 33 (33 0) No 57 (57 0) 67 (67 0) Duration of analgesia use 5(2 7) 4(2 7) (days) Length of postoperative hospital stay (days) 6(6 7) 6(6 7) Values in parentheses are percentages unless indicated otherwise; values are *mean(s.d.) and median (i.q.r.). MPLC, multiport laparoscopic colectomy; SILC, single-incision laparoscopic colectomy; POD, postoperative day. χ 2 test, except Mann Whitney U test. Table 4 Postoperative complications MPLC (n = 100) SILC (n = 100) P* Postoperative complication Any 15 (15 0) 12 (12 0) Grade III 5 (5 0) 8 (8 0) Wound infection 3 (3 0) 0 (0 0) Anastomotic leakage 4 (4 0) 2 (2 0) Anastomotic bleeding 0 (0 0) 1 (1 0) Small bowel 1(1 0) 1 (1 0) obstruction Lymphorrhoea 2 (2 0) 0 (0 0) Thrombosis 1 (1 0) 1 (1 0) Urinary 0 (0) 1 (1 0) Cardiovascular 0 (0) 0 (0 0) Pneumonia 0 (0) 0 (0 0) Wound dehiscence 0 (0) 0 (0 0) Reoperation 3 (3 0) 3 (3 0) Death 0 (0) 0 (0) Values in parentheses are percentages. MPLC, multiport laparoscopic colectomy; SILC, single-incision laparoscopic colectomy. *χ 2 test. (Fig. 1). The clinicopathological characteristics of the 200 patients are presented in Table 2. Baseline factors were well balanced between the arms. The surgical procedure and outcomes are summarized in Table 3. The duration of operation, blood loss, rate of conversion to open laparotomy, reoperation rate, length of proximal and distal margins, and number of lymph nodes harvested were similar in the MPLC and SILC arms. In the SILC arm, nine patients (9 0 per cent) required an additional 12-mm trocar for insertion of a linear stapler for intracorporeal distal colon transection during anterior resection. The umbilical incision length did not differ significantly between the two groups. The total skin incision in the SILC arm was significantly shorter than that in the MPLC arm (P < 0 001). Regarding postoperative recovery, there were no significant differences in time to first flatus or first defaecation and length of postoperative hospital stay. The median duration of analgesia use (MPLC arm 5 days, SILC arm 4 days; P = 0 485) and the rate of analgesic use after 5 postoperative days (43 0 and33 0 per cent respectively; P = 0 145) were similar in the two arms. Postoperative complications are shown in Table 4.The overall complication rates were nearly equivalent in the two arms (MPLC 15 0 per cent, SILC 12 0 per cent; P = 0 680). There were no marked differences in grade III IV adverse events (5 0 and 8 0 per cent respectively; P = 0 568), and there were no deaths in either group (P = 1 000). Additionally, there was no significant difference in the incidence of anastomotic leakage, wound infection or small bowel obstruction. Six patients (MPLC 4, SILC 2) developed an anastomotic leak. Emergency

5 1280 J. Watanabe, M. Ota, S. Fujii, H. Suwa, A. Ishibe and I. Endo operation with diverting ileostomy was performed in four of these patients and two were treated with conservative drainage alone. Discussion The outcomes and postoperative complications were similar after SILC and MPLC in this trial. With the exception of the total skin incision length, there were no significant differences between the SILC and MPLC arms in any of the variables studied. Although SILC may be limited by procedural difficulties, such as interference by forceps, insufficient countertraction and inline viewing, there was no significant difference in the duration of surgery, blood loss, proximal or distal surgical margin, or the incidence of postoperative complications when performed by experienced surgeons. Moreover, there was no conversion to MPLC in the SILC arm. Several case-controlled reports and two RCTs 27,28 have compared the short-term results of MPLC with SILC and the feasibility of this procedure. Many groups have reported that SILC has similar postoperative results to MPLC, including operating time, blood loss, complications, hospital stay, number of lymph nodes harvested and resection margin on the specimen. Several studies 10,11,14,16 included patients with diseases other than cancer, such as adenoma, diverticulitis or inflammatory disease. These SILC data are subject to significant biases owing to non-randomization and the retrospective nature of the studies. Additionally, there was significant heterogeneity of the study population in terms of indications for surgery and use of instruments. The two RCTs had very few patients (32 and 50 respectively) and did not performed CME. Two meta-analyses 22,23 revealed a shorter hospital stay following SILC. Some reports have indicated that the length of postoperative hospital stay is shorter in fast-track compared with conventional management. Thus the length of postoperative hospital stay is largely dependent on the type of postoperative management 29. Papaconstantinou and colleagues 13 reported that the decreased pain level after SILC might be a direct result of eliminating the trauma of additional ports at separate sites on the abdominal wall. In present study, the sample size may have been insufficient to show a clinical difference, and incremental pain caused by additional trocars is unlikely to be large. In cancer treatment, better cosmetic and less invasive approaches must not compromise oncological clearance 18. Therefore, the application of SILC for colonic cancer treatment must be considered carefully. From the viewpoint of oncological clearance, there was no difference in the number of lymph nodes dissected between the SILC and MPLC arms (mean 25 5 and24 1 respectively). This study has several limitations. There is a possibility of observational bias as both the patient and the surgeon were aware of study group assignments. The limited power to detect subtle differences in outcomes is acknowledged. Nevertheless, this trial has shown that SILC has no clear advantages over MPLC. Acknowledgements The authors thank M. S. Oba for her statistical contribution to this study. Disclosure: The authors declare no conflict of interest. References 1 Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 2002; 359: Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. NEnglJMed2004; 350: Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM et al.; MRC CLASICC trial group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 2005; 365: Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ et al.; COlon cancer Laparoscopic or Open Resection Study Group (COLOR). Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 2005; 6: Fleshman J, Sargent DJ, Green E, Anvari M, Stryker SJ, Beart RW Jr et al.; Clinical Outcomes of Surgical Therapy Study Group. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg 2007; 246: Lacy AM, Delgado S, Castells A, Prins HA, Arroyo V, Ibarzabal A et al. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. 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