Single incision vs conventional laparoscopic anterior resection for sigmoid colon cancer: a case-matched study

The American Journal of Surgery (2013) 206, 320-325 Clinical Science Single incision vs conventional laparoscopic anterior resection for sigmoid colon cancer: a case-matched study Seung-Jin Kwag, M.D., Jun-Gi Kim, M.D.*, Seong-Taek Oh, M.D., Won-Kyung Kang, M.D. Department of Surgery, Seoul St. Mary s Hospital, The Catholic University of Korea, Seoul, Korea KEYWORDS: Anterior resection; Laparoscopic colectomy; Sigmoid colon cancer; Single incision; SILS Abstract BACKGROUND: The purpose of the study was to evaluate the safety and effects of single-incision laparoscopic anterior resection (SILAR) for sigmoid colon cancer by comparing it with conventional laparoscopic anterior resection (CLAR). METHODS: Twenty-four patients who underwent SILAR between April 2010 and July 2011 were case matched 1:2 with patients who underwent CLAR, with respect to age, sex, body mass index, tumor location, and history of abdominal surgery. RESULTS: Two patients in the SILAR group and 1 patient in the CLAR group experienced anastomotic leakage. The operative time was longer in the SILAR group than in the CLAR group (251 6 50 vs 237 6 49 minutes; P 5.253). The number of harvested lymph nodes (19.6 6 10.7 vs 20.8 6 7.7; P 5.630) was not different. The postoperative hospital stay was shorter in the SILAR group (7.1 6 3.4 days) than in the CLAR group (8.1 6 3.5 days) (P 5.234). CONCLUSIONS: On the basis of the early outcomes, we conclude that SILAR is feasible and safe. Moreover, the adequate lymph node harvest and free margins support the use of this procedure. Ó 2013 Elsevier Inc. All rights reserved. Laparoscopic procedures have become an accepted method to treat colorectal cancers. 1,2 The benefits of laparoscopic surgery over open surgery are numerous, and advancements in medical science are continuously increasing the superiority of this technique. Reduced postoperative pain, the rapid return of bowel function, shorter hospital stays, and improved cosmesis are well-noted advantages of laparoscopy. 3,4 Recently, minimally invasive techniques such as natural orifice transluminal endoscopic surgery and single-incision laparoscopic surgery (SILS) have been introduced. SILS was rapidly adapted for application in various The authors declare no conflicts of interest. * Corresponding author. Tel.: 182-2-2258-6095; fax: 182-2-595-2822. E-mail address: jgkim@catholic.ac.kr Manuscript received February 23, 2012; revised manuscript September 17, 2012 fields of surgery, such as urologic, gynecologic, and general surgery. 5 In the management of right- or left-sided colon tumors, SILS has recently evolved to a great extent, and its benefits appear to be comparable to those of laparoscopic surgery in many respects. 6,7 The first single-incision laparoscopic colectomy was described for the right colon by Bucher et al 8 and Remzi et al 9 in 2008. Since then, numerous case reports and series have been published to assess the safety and feasibility of this technique. 6,10 13 However, few studies have compared the single incision with conventional methods specifically for sigmoid colon cancer. 7,14,15 SILS has potential advantages because it (1) reduces port-related complications (eg, pain, bleeding, infection, and hernia); (2) promotes an early return of bowel function; and (3) improves cosmetic results. 16,17 However, SILS also has disadvantages, such as prolonged operative time, limited applicability, and a 0002-9610/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.11.007

S.-J. Kwag et al. Single-incision laparoscopic colectomy 321 learning curve for the surgeon performing the procedure. The learning curve, however, appears to be manageable if the surgeon is adaptable and has a great deal of experience in laparoscopic surgery. The primary end point with respect to SILS is the oncologic outcome; no improvement in this technique can be considered useful if oncologic principles are compromised. In our study, we attempted to address the feasibility and applicability of SILS through the comparison with the conventional laparoscopic method. Both techniques were used to perform anterior resections for sigmoid colon cancer, and the short-term surgical outcomes and oncologic results were compared. Methods In this study, we included only patients with sigmoid colon cancer who received single-incision laparoscopic anterior resection (SILAR) or conventional laparoscopic anterior resection (CLAR). The procedures were performed by a single surgeon (J-G.K) at Seoul St. Mary s Hospital between April 2009 and July 2011. Inclusion criteria for a SILAR procedure are the followings: (1) preoperative computed tomographic scan showing tumor size less than 4 cm and T stage less than 4; (2) no evidence of distant metastasis; (3) no history of median laparotomy; and (4) patient consent to perform the SILAR. Twenty-four SILARs were performed between April 2010 and July 2011. We retrospectively case matched in a ratio of 1:2 for all the SILAR patients with 48 of 105 patients who received CLAR between April 2009 and July 2011. The groups were matched in terms of age, sex, body mass index, tumor location, and history of abdominal surgery. Cases performed in an emergency, such as patients with obstructions or perforated lesions, or both, were excluded in both groups. This project was approved by the Institutional Review Board of Seoul St. Mary s Hospital, the Catholic University of Korea on October 8, 2011 (KC11RGSI0583). The intraoperative parameters that were compared were the length of the incisions, the operative time, the estimated blood loss, the conversion rate (to conventional laparoscopic method or to open method), and any intraoperative complications. The postoperative parameters that were compared were the return of bowel function (defined as first passage of flatus), the time taken to resume a soft oral diet, the number of analgesics and their duration of use, the duration of the hospital stay, and postoperative morbidity. The oncologic adequacy was assessed by the number of lymph nodes harvested, the specimen length, and the incidence of positive resection margins (including proximal and distal margins). All the data were retrieved from our electronic medical record system, and a retrospective analysis was performed. Statistical analyses were performed using PASW Statistics, version 18.0 (SPSS Inc, Chicago, IL). The chi-square and Student t tests were used to compare the data for each group. P less than.05 was considered statistically significant. Operative technique Single-incision laparoscopic anterior resection. The patient was placed in a low lithotomy position. The surgeon and his assistant stood on the right side of the patient, with the assistant to the left of the surgeon. An incision of approximately 2.5 cm was made through the umbilicus. The peritoneum was entered, and an ALEXIS wound retractor (Applied Medical, Rancho Santa Margarita, CA) was inserted into the peritoneal cavity. A SILS port (Covidien, Norwalk, CT), which can accommodate 3 5-mm cannulas, was then inserted into the retractor. The 3 5-mm cannulas were inserted soon after. The EndoEYE (5-mm, 30 ) rigid telescope (Olympus, Tokyo, Japan) and traditional laparoscopic instruments were used. For the first 7 cases, 1 additional 5-mm trocar was inserted in the left lower quadrant of the abdominal cavity. Pneumoperitoneum was established and the abdominal cavity was explored. The patient was moved into the Trendelenburg and right-tilted position. The small bowel and omentum were gently swept out of the pelvis away from the surgical field. Rather than the medial-to-lateral dissection used in the conventional method, for the SILAR, we first performed the lateral-to-medial dissection. After mobilization was initiated from the medial side, we began the medial-to-lateral dissection and continued in this direction throughout the procedure. It is important to extend the peritoneal incision from the promontory level to the level of the inferior mesenteric artery along the abdominal aorta while preserving the hypogastric plexus. The tissue dissection was generally performed using a combined blunt dissection tool with suction and a sharp dissection tool with monopolar diathermy (Surgiwand II; Covidien). The inferior mesenteric pedicle was divided at its origin using a surgical metal clip and the LigaSure sealing system (Covidien). The divided pedicle was elevated, and the avascular retroperitoneal plane was established up to the inferior border of the pancreas in the cranial direction and laterally to the colon. To obtain the proper distal margin and handling, the upper rectum was mobilized. This procedure was followed by division of the mesorectum to expose the rectal wall to facilitate anastomosis. One 5-mm trocar was replaced by a 12-mm trocar. A laparoscopic bulldog clip (Aesculap AG, Tuttlingen, Germany) was used at the proximal portion of the denuded rectum to ensure that cancer cells did not migrate into the undiseased rectum. After thorough irrigation of the distal portion of the rectum with normal saline, the rectum was transected using 1 or 2 ENDO GIA ROTICULATOR 60 staples (Covidien). The proximal colon with the tumor was extracorporealized through the ALEXIS wound retractor. A purse-string suture was subsequently applied 10 to 15 cm proximal to the cancer before the division of the colon.

322 The American Journal of Surgery, Vol 206, No 3, September 2013 Table 1 Clinical characteristics Characteristic SILAR (n 5 24) CLAR (n 5 48) P value Age (y) 59.5 6 14.5 59.0 6 13.8.898 Male/female 9/15 18/30 1 Body mass index (kg/m 2 ) 24.4 6 3.0 24.0 6 2.9.564 Distance from anal verge (cm) 21.3 6 4.5 21.9 6 3.6.572 History of abdominal surgery 2 4 1 Preoperative CEA (ng/ml) 2.95 6 0.79 5.13 6 1.86.286 Postoperative CEA (ng/ml) 1.19 6 0.98 1.41 6 1.10.475 CEA 5 carcinoembryonic antigen; CLAR 5 conventional laparoscopic anterior resection; SILAR 5 single-incision laparoscopic anterior resection. After the anvil of a DST EEA 31 stapler (Covidien) was secured at the end of the proximal bowel, the bowel was returned to the peritoneal cavity and pneumoperitoneum was re-established. A primary end-to-end circular stapled colorectal anastomosis was then performed. The port was removed and the wound was closed in layers. In the first 7 cases, in which the additional 5-mm trocar was inserted through the left lower quadrant of the abdomen, a suction tube drain was inserted through the same hole from which the trocar was removed. In the cases performed using only the SILS procedure, the wound was closed without a drain. Conventional laparoscopic anterior resection. Most of the surgical steps for the CLAR were the same as those described for the SILAR. The primary difference was that at the beginning of the procedure, the dissection was made in the medial-to-lateral direction, eliminating the need for mobilizing the colon. One 11-mm camera port was inserted just above the umbilicus, and 4 additional working ports were placed in the abdominal quadrants. The size of the right lower quadrant port was 12 mm, whereas the remaining ports were 5 mm. After the laparoscopic division of the rectum, the proximal colon was extracorporealized by extending the camera port incision using the OCTO Port (DalimSurgNET, Seoul, Korea) or the ALEXIS wound retractor (Applied Medical). The remainder of the procedure was performed in a manner similar to that of the SILAR. We kept a closed suction tube drain in the pelvic cavity through the left lower quadrant port site for all CLARs. Results Between April 2009 and July 2011, 24 SILARs were performed by a single surgeon (J-G.K.) to treat patients with sigmoid colon cancer. During this period, the surgeon performed a total of 228 laparoscopic colorectal resections for sigmoid and rectal cancer. Among these cases, 105 patients received CLAR for sigmoid colon cancer. The sex ratio was the same for both groups. The average age was 60 years in both groups. The mean body mass index was similar: 24.4 6 3.0 (range, 18.6 to 31.2) kg/m 2 in the SILAR group and 24.0 6 2.9 (range, 18 to 32) kg/m 2 in the CLAR group. The mean pre- and postoperative carcinoembryonic antigen levels were not significantly different between the 2 groups. There were 2 cases of previous intra-abdominal surgery in the SILAR group (1 laparoscopic cholecystectomy and 1 hysterectomy). In the CLAR group, there were 2 previous appendectomies and 2 previous cholecystectomies. However, no severe adhesions that could interrupt the procedure was encountered in either group. The other clinical data are shown in Table 1. In the SILAR group, the initial 7 cases required 1 additional port, but there was no conversion to open surgery or conventional laparoscopic surgery. There was no conversion to open surgery in the CLAR group. The mean operative time was longer in the SILAR group than in the CLAR group (251 6 50 minutes vs 237 6 49 minutes; P 5.253). There was no difference in the median estimated blood loss between the groups: 135 6 28 ml (range, 20 to 300 ml) for the SILAR group vs 144 6 22 ml (range, 20 to 500 ml) for the CLAR group (P 5.788). There were no intraoperative complications in either group (Table 2). The postoperative recovery with respect to the return of bowel function (defined as the first flatus passage) and the return to an oral diet was faster in the SILAR group than in the CLAR group (1.7 6.6 vs 2.2 6 1.1 days; P 5.043 and 2.8 6 1.0 vs 3.6 6 1.4 days; P 5.015). The postoperative hospital stay was shorter in the SILAR group (7.1 6 3.4 days) than in the CLAR group (8.1 6 3.5 days); however, this difference was not statistically significant. No 30-day mortality or readmissions occurred after the operation for either group, and the difference between the groups in terms of the incidence of postoperative complications was minimal (8.3% for the SILAR group vs 10.4% for the CLAR group; P 5.778). Two patients in the SILAR group and 1 patient in the CLAR group had anastomotic leaks and required reoperation using the conventional laparoscopic method. In the SILAR group, 2 of 11 patients (18.2%) who underwent transection at the rectum with 2 linear staples had anastomotic leakage. In the CLAR group, 1 patient who underwent transection at the rectum with 3 linear staples had anastomotic leakage. In the CLAR group, chylous leakage was discovered through the drain in 3 patients without abdominal pain after eating. They were treated with parenteral nutrition for 2 to 3 days and a low-fat diet was given afterward. There was no difference between the

S.-J. Kwag et al. Single-incision laparoscopic colectomy 323 Table 2 Intraoperative outcomes Variable SILAR (n 5 24) CLAR (n 5 48) P value Open conversion 0 0 Operative time (min) 251 6 50 237 6 49.253 Estimated blood loss (ml) 135 6 28 144 6 22.788 Size of incision (cm) 3.4 6 1.1 7.3 6 1.6,.01 Complication 0 0 Amount of gas (L) 462 6 182 425 6 168.747 Number of linear staples.077 1 13 (54.2%) 37 (77.1%) 2 11 (45.8%) 10 (20.8%) 3 0 1 (2.1%) CLAR 5 conventional laparoscopic anterior resection; SILAR 5 single-incision laparoscopic anterior resection. groups with respect to the amount of analgesics given (Table 3). All the resections in both groups were performed to remove a malignancy. The pathologic characteristics were comparable in both groups in terms of the length of the specimen and the distance between the proximal resection margin and the cancer. Although the length of the distal resection margin was shorter in the SILAR group than in the CLAR group (7.5 6 2.5 cm vs 9.2 6 4.0 cm; P 5.072), a length of 7.5 cm was sufficient to provide an adequate safety margin. In the SILAR group, there were more stage T1 and stage T2 cases than in the CLAR group. In addition, tumor size was significantly smaller in the SILAR group. No significant difference was observed with respect to the number of harvested lymph nodes: 19.6 6 10.7 in the SILAR group and 20.8 6 7.7 in the CLAR group. Results related to the pathologic features are shown in Table 4. Comments Laparoscopic surgery is the principal operative method used to treat colorectal cancers in our institute and at other major tertiary health care centers worldwide. The benefits of laparoscopy include reduced postoperative pain, faster return of bowel function, shorter hospital stay, and improved cosmesis. Each port site wound, however, contributes to postoperative pain and carries the potential risk of hemorrhage, infection, hernia, and adhesion. 18 Thus, use of SILS would theoretically lower the rate of port site related complications and strengthen the benefits of laparoscopic surgery. This study was designed to investigate the safety and efficacy of SILS compared with conventional laparoscopic surgery in cases of sigmoid colon cancer. Our data reveal that most intraoperative outcomes and short-term measures of convalescence were equivalent between the SILAR and CLAR groups. In the SILAR group, the average operative time for the first case to the seventh case, using an additional port, was 289 minutes, which was 52 minutes longer than the 237 minutes required for the CLAR. For the latter 17 SILAR cases, however, we achieved an average operative time of 236 minutes without using an additional port for assistance. This fact indicates that using an additional port improves the surgeon s learning curve, which eventually shortens the operative time without violating oncologic principles. The average operative time for the SILAR procedure in our study was longer than that in other studies, 7,19,20 which may be related to our principle of dissecting the precise embryologic plane and performing high ligation of the mesenteric pedicles with extra caution. In every case, adequate dissection of the lymph node near the origin of the inferior mesenteric artery was performed, and the artery was then ligated using clips shortly thereafter. The inferior mesenteric vein was ligated Table 3 Postoperative outcomes Variable SILAR (n 5 24) CLAR (n 5 48) P value Postoperative complication 2 (8.3%) 4 (8.3%) 1 Anastomotic leakage 2 1 Chylous ascites 0 3 Other 0 0 Duration of analgesic use (d) 0.7 6 0.3 0.8 6 0.2.860 Passage of flatus (d) 1.7 6 0.6 2.2 6 1.1.043 Diet (d) 2.8 6 1.0 3.6 6 1.4.015 Hospital stay (d) 7.1 6 3.4 8.1 6 3.5.234 CLAR 5 conventional laparoscopic anterior resection; SILAR 5 single-incision laparoscopic anterior resection.

324 The American Journal of Surgery, Vol 206, No 3, September 2013 Table 4 Pathologic characteristics Variable SILAR (n 5 24) CLAR (n 5 48) P value Tumor extent.257 T1 9 (37.5%) 15 (31.3%) T2 6 (25.0%) 5 (10.4%) T3 9 (37.5%) 27 (56.3%) T4 0 0 Length of specimen (cm) 20.1 6 3.8 21.3 6 4.6.242 Tumor size (cm) 2.6 6 1.3 3.4 6 1.9.033 Proximal free margin (cm) 11.2 6 3.9 11.4 6 4.1.758 Distal free margin (cm) 7.5 6 2.5 9.2 6 4.0.072 Harvested lymph nodes (n) 19.6 6 10.7 20.8 6 7.7.630 Positive margin 0 0 CLAR 5 conventional laparoscopic anterior resection; SILAR 5 single-incision laparoscopic anterior resection. just below the lower border of the pancreas. To preserve the integrity of the mesocolon, it was separated from the parietal plane with care. The splenic flexure was sufficiently mobilized to obtain tension-free colorectal anastomosis. 21 In contrast to the conventional procedure, the lateral peritoneal reflection is mobilized first so that it becomes more feasible to apply traction on the vascular pedicle from the medial side with a single instrument. The rate of postoperative complications was similar in both groups. In terms of anastomotic leakage, which is the most risky complication in colorectal surgery, the rate in the SILAR group (8.3%) was higher than that in the CLAR group (2.1%). When transecting the rectum with SILS, placing the transverse staple line is difficult because of the acute angle, which caused an oblique staple line for SILAR. This result indicates a higher probability of using 2 linear staples in the SILAR group compared with the CLAR group. 22 The tip on the bowel segment that resulted from the oblique staple line might have contributed to the leakage; however, we tried to use this area for the anastomosis using a circular staple to remove the possible ischemic tip. The learning curve for SILAR is also a possible reason for the leakage; however, there were only 24 cases of SILAR in this study. Thus, further studies with a large number of cases are necessary. The chylous leakage appeared only in the CLAR cases, even though the operative instruments and extent of surgery were identical in both groups. The incidence rate of chylous leakage in the CLAR group was 6.25%, which is relatively higher compared with other studies, 23 but these cases of leakage were solved without any serious problems. A possible cause for chylous leakage may be the extensive dissection needed for removing the cancer-bearing area on the sigmoid colon using electrocautery. In contrast, the lack of leakage in the SILAR group and the possible reason for the result is the limited number of patients (only 7 of 24) who had a drain inserted; thus leakage that occurred in patients without a drain might had been overlooked. In our study, the patients who underwent SILAR were discharged earlier than those in the CLAR group: 7.1 6 3.4 days vs 8.1 6 3.5 days (P 5.234). The patients in the SILAR group were able to eat earlier than the patients in the CLAR group. This finding is very promising and should be demonstrated in larger series. Also, a recent study indicates that single-incision laparoscopic colectomy significantly reduces the postoperative pain and is associated with shorter hospital stay for colonic neoplasms. 24 However, contrary to our expectations, there was no reduction in the number of analgesics used for the patients in the SILAR group. We did not examine the postoperative pain score, which could be considered a weak point of our study. Further studies are required to investigate whether SILS reduces the pain after surgery. Maintaining the surgical oncologic principle is the most important factor for the treatment of cancer regardless of the approach. The principles of high vascular ligation, the notouch technique, and anatomic dissection were maintained in this series. No gross or microscopic positive resection margins were observed in either group. The average number of harvested lymph nodes was 19.6 in the SILAR group, which exceeded the acceptable 12 nodes. 25 This study has limitations including its small sample size and its reliance on retrospective review of medical records. In addition, the patients included were not randomly selected. However, we expect that this initial comparison study will lead to larger randomized prospective studies that will conclusively demonstrate SILAR to be the next step in sigmoid colon cancer operating procedures. In conclusion, our results demonstrate that SILAR is a feasible and safe procedure and results in immediate oncologic outcomes that are comparable to those of conventional laparoscopic surgery, with potentially better postoperative outcomes. Although there is a learning curve for this technique, SILAR may become an alternative approach for selected patients with sigmoid colon cancer. Whether SILAR will be as successful as conventional laparoscopy is unknown, but a large randomized study will be crucial to assess the feasibility and advantages of this approach, as well as its efficacy with respect to long-term oncologic outcomes.

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