Increasing evidence exists for the safety, efficacy, and

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1 ORIGINAL CONTRIBUTION A Three-Arm (Laparoscopic, Hand-Assisted, and Robotic) Matched-Case Analysis of Intraoperative and Postoperative Outcomes in Minimally Invasive Colorectal Surgery Chirag B. Patel, M.S.E. Madhu Ragupathi, M.D. Diego I. Ramos-Valadez, M.D. Eric M. Haas, M.D. Division of Minimally Invasive Colon and Rectal Surgery, Department of Surgery, University of Texas Medical School at Houston, Houston, Texas PURPOSE: Robotic-assisted laparoscopic surgery is an emerging modality in the field of minimally invasive colorectal surgery. However, there is a dearth of data comparing outcomes with other minimally invasive techniques. We present a 3-arm (conventional, handassisted, and robotic) matched-case analysis of intraoperative and short-term outcomes in patients undergoing minimally invasive colorectal procedures. METHODS: Between August 2008 and October 2009, 70 robotic cases of the rectum and rectosigmoid were performed. Thirty of these were organized into triplets with conventional and hand-assisted cases based on the following 6 matching criteria: 1) surgeon; 2) sex; 3) body mass index; 4) operative procedure; 5) pathology; and 6) history of neoadjuvant therapy in malignant cases. Demographics, intraoperative parameters, and postoperative outcomes were assessed. Pathological outcomes were analyzed in malignant cases. Data were stratified by postoperative diagnosis and operative procedure. RESULTS: There was no significant difference in intraoperative complications, estimated blood loss ( ml overall), or postoperative morbidity and mortality among the groups. Robotic technique Financial Disclosure: None reported. Presented at meeting of The American Society of Colon and Rectal Surgeons, Minneapolis, MN, May 15 to 19, Correspondence: Eric M. Haas, M.D., 7900 Fannin Street, Suite 2700, Houston, TX ehaasmd@houstoncolon.com Dis Colon Rectum 2011; 54: DOI: /DCR.0b013e3181fec377 The ASCRS 2011 required longer operative time compared with conventional laparoscopic (P.01) and hand-assisted (P.001) techniques; however, this difference was not maintained in cases with low pelvic anastomoses. The overall mean length of stay was days with no significant difference between the groups. Pathological analysis of malignant cases revealed a median lymph node extraction of 17 with no significant difference among the 3 modalities. CONCLUSION: In this 3-arm case-matched series, the robotic approach results in short-term outcomes comparable to conventional and hand-assisted laparoscopic approaches for benign and malignant diseases of the rectum and rectosigmoid. With 3- dimensional visualization, additional freedom of motion, and improved ergonomics, this enabling technology may play an important role when performing colorectal procedures involving the pelvic anatomy. KEY WORDS: Colorectal cancer; Laparoscopic surgery; Robotic-assisted surgery; Hand-assisted surgery; Matched-case analysis. Increasing evidence exists for the safety, efficacy, and benefits following minimally invasive surgical techniques including conventional laparoscopic surgery (CLS), hand-assisted laparoscopic surgery (HALS), and robotic-assisted laparoscopic surgery (RALS) in the field of colorectal surgery. Manystudies report the shortterm advantages of CLS compared with open surgery, including reduced intraoperative trauma, postoperative pain, and length of hospital stay (LOS). 1 7 The handassisted technique was developed as an enabling technology for surgeons inexperienced with the CLS approach. 144 DISEASES OF THE COLON & RECTUM VOLUME 54: 2 (2011)

2 DISEASES OF THE COLON & RECTUM VOLUME 54: 2 (2011) 145 FIGURE 1. Location of trocars/ports and extraction site for 3 minimally invasive surgical techniques. (A) Conventional laparoscopic surgery: trocar placement and suprapubic incision for specimen extraction. (B) Hand-assisted laparoscopic surgery: location of three 5-mm trocars and Pfannenstiel incision through which the hand-assist device is placed. (C) Robotic-assisted laparoscopic surgery: extraction site and port placement sites. Since that time, it has been shown to have patient benefits similar to CLS and to result in lower conversion rates in complex procedures. 8 More recently, RALS has been reported to be a safe and feasible approach for various colorectal procedures Although comparative studies of open vs CLS, 1 7 open vs HALS, 8 and CLS vs HALS 12,13 have been reported in the colorectal surgery literature, a limited number of studies have compared RALS with other minimally invasive modalities. 14,15 We present a 3-arm (conventional, hand-assisted, and robotic-assisted laparoscopic surgery) matched-case analysis of intraoperative and short-term postoperative outcomes in patients undergoing minimally invasive colorectal surgery. MATERIALS AND METHODS This study was approved by the institutional review board. Between August 2008 and October 2009, 70 robotic-assisted laparoscopic procedures of the rectum and rectosigmoid were performed. Thirty of the cases were matched into triplets with conventional and hand-assisted laparoscopic procedures based on 6 matching criteria: 1) surgeon (E.M.H.), 2) sex, 3) body mass index, 4) operative procedure: sigmoid resection, low anterior resection, or rectopexy, 5) pathology (benign or malignant), and 6) history of neoadjuvant therapy in malignant cases. Patient demographics, intraoperative parameters, and 30-day postoperative outcomes were assessed. Pathology outcomes were analyzed in malignant cases and included specimen length, lymph node extraction, and surgical margins. Data were stratified by postoperative diagnosis and operative procedure. Surgical Technique The trocar site varied slightly among the minimally invasive surgery (MIS) approaches, whereas the extraction site was suprapubic in all but 3 patients (Fig. 1). In the CLS approach, one 12-mm and three 5-mm trocars were used. The HALS technique used three 5-mm trocars and a handassist device (Gelport, Applied Medical, Rancho Santa Margarita, CA). The robotic approach used three 8-mm and two 12-mm trocars. All MIS procedures were performed in a medial-to-lateral fashion with initial identification and ligation of the inferior mesenteric pedicle. The retroperitoneal plane was established followed by takedown of the splenic flexure (when required) and lateral peritoneal attachments on the left. For the robotic cases, splenic flexure takedown was performed laparoscopically before docking the robot. The time required for splenic flexure mobilization was included in the total operative time for the RALS group. In all techniques, the specimen was extracted with the use of an Alexis wound retractor (Applied Medical, Rancho Santa Margarita, CA). All anastomoses were performed intracorporeally in an end-toend fashion using the ECS29 circular stapling device (Endopath ILS, Ethicon Endo-Surgery, Cincinnati, OH). All patients were placed on the same accelerated postoperative pathway. Statistical Analysis Data analysis was performed using Intercooled Stata version 9.2 (Stata Corporation, College Station, TX). Statistical significance was defined as.05. Categorical data, summarized as percentages, were compared with the 2 test. For quantitative data, paired 2-tailed Student t test was performed for 3-group comparisons (CLS compared with HALS, CLS compared with RALS, and HALS compared with RALS), with Bonferroni correction for multiple comparisons (adjusted.0167). In cases of nonnormally distributed data, Wilcoxon rank-sum analysis was performed. Results are presented as mean SD.

3 146 PATEL ET AL: 3-ARM MATCHED MIS COLORECTAL SURGERY TABLE 1. Unbiased selection of RALS cases Parameter Matched RALS cases All RALS cases (n 70) P Demographics Sex (male) a 19 (63.3%) 33 (47.1%) NS BMI (kg/m 2 ) a NS Prior abdominal or pelvic surgery 17 (56.7%) 40 (57.1%) NS Diagnosis a 22 Benign (73.3%) 47 Benign (67.1%) 8 Malignant (26.7%) 23 Malignant (32.9%) NS Intraoperative Operative procedure a 6 LAR (20.0%) 14 LAR (20.0%) NS 1 RP (3.3%) 5 RP (7.1%) 23 SR (76.7%) 34 SR (48.6%) OT (min) NS EBL (ml) NS Conversion 0% 0% NS Postoperative Morbidity 4 (13.3%) 10 (14.3%) NS LOS (days) NS Malignant cases only Neoadjuvant therapy a 4/8 (50%) 13/23 (56.5%) NS LNE NS Margin status 100% negative 100% negative NS BMI body mass index; EBL estimated blood loss; LAR low anterior resection; LNE lymph node extraction; LOS length of stay; NS not significant; OT total operative time; RP rectopexy; SR sigmoid resection; RALS robotic-assisted laparoscopic surgery. a Matching criterion. RESULTS There was no significant difference in demographic characteristics, intraoperative parameters, or postoperative outcomes between the 30 RALS cases used for this study and the 70 cases comprising our RALS experience (Table 1). A total of 90 patients underwent colorectal surgery with one of 3 MIS techniques: 30 CLS, 30 HALS, and 30 RALS. The matching criteria are summarized in Table 2 and additional preoperative characteristics are summarized in TABLE 2. Matching criteria Parameter CLS HALS RALS Sex (male) 19 (63.3%) 19 (63.3%) 19 (63.3%) BMI (kg/m 2 ) Diagnosis Benign 22 (73.3%) 22 (73.3%) 22 (73.3%) Malignant 8 (26.7%) 8 (26.7%) 8 (26.7%) Neoadjuvant therapy 4 (50.0%) 4 (50.0%) 4 (50.0%) (n 8 malignant cases only) Procedure SR 23 (76.7%) 23 (76.7%) 23 (76.7%) LAR 6 (20.0%) 6 (20.0%) 6 (20.0%) RP 1 (3.3%) 1 (3.3%) 1 (3.3%) BMI body mass index; CLS conventional laparoscopic surgery; HALS handassisted laparoscopic surgery; LAR low anterior resection; RALS robotic-assisted laparoscopic surgery; RP rectopexy; SR sigmoid resection. Table 3. There was no significant difference among the preoperative characteristics. Intraoperative parameters are summarized in Table 4. The total operative time was minutes in the CLS group, minutes in the HALS group, and minutes in the RALS group. The RALS approach required significantly longer operative time compared with the CLS (P.01) and HALS (P.001) approaches. Compared with CLS, HALS required significantly shorter operative time (P.016) for low anterior resection and cases involving malignant pathology. When analyzed in each arm, cases in which a diverting loop ileostomy was performed resulted in significantly longer total operative time in the HALS (P.02) and RALS (P TABLE 3. Preoperative characteristics Parameter CLS HALS RALS P Age (y) NS ASA NS Prior abdominal or 12 (40.0%) 18 (60.0%) 17 (56.7%) NS pelvic surgery Distance to the anal verge (cm), n 8 malignant cases NS ASA American Society of Anesthesiologists; CLS conventional laparoscopic surgery; HALS hand-assisted laparoscopic surgery; NS not significant; RALS robotic-assisted laparoscopic surgery.

4 DISEASES OF THE COLON & RECTUM VOLUME 54: 2 (2011) 147 TABLE 4. Intraoperative parameters Parameter CLS HALS RALS P Diverting loop ileostomy 5 (16.7%) 7 (23.3%) 6 (20%) NS Splenic flexure takedown 9 (30.0%) 11 (36.7%) 8 (26.7%) NS Total operative time (min) All cases CLS vs RALS (P.01) a,b,c,d CLS vs HALS (P.016) c,e HALS vs RALS (P.001) a,b,c,d,e No diverting loop ileostomy HALS (P.02) Diverting loop ileostomy RALS (P.01) No splenic flexure takedown RALS (P.01) Splenic flexure takedown Benign (n 22) RALS (P.01) Malignant (n 8) Estimated blood loss (ml) NS Intraoperative conversion to open or other 0% 0% 0% NS MIS technique Complications 0% 0% 2 (6.7%) NS CLS conventional laparoscopic surgery; HALS hand-assisted laparoscopic surgery; LAR low anterior resection; MIS minimally-invasive surgery; NS not significant; RALS robotic-assisted laparoscopic surgery; SR sigmoid resection. Comparisons were made as follows: a All cases, b SR only, c malignant cases only, d benign cases only, e LAR only..01) groups, with no significant difference in the CLS group (P.08). Splenic flexure takedown resulted in significantly longer operative time in only the RALS group (P.01). There was no significant difference in estimated blood loss between the groups. In regard to intraoperative complications, none occurred in the CLS and HALS groups, whereas 2 complications (6.7%) occurred in the RALS group (P.13). These consisted of a thermal injury and a serosal traction injury of the bowel, both of which were managed with colorrhaphy. In regard to the pathology results for the 8 patients with malignant disease in each group, there was no significant difference in the mean lymph node extraction: 20.9 in the CLS group, 16.3 in the HALS group, and 17.3 in the RALS group. Furthermore, there were no significant differences in other pathology results including specimen length, distal and radial margin status, and staging (Table 5). In regard to postoperative outcomes, overall LOS was days, with no significant difference between the groups. In the subset of patients with malignant disease, the LOS in the RALS ( days) group was significantly shorter than that in the CLS group ( days), P.01. Postoperative complications occurred in 11 of the 90 patients (12.2%) with no significant difference in complication rate noted between the 3 arms. Two patients TABLE 5. Pathology outcomes (malignant cases only) Parameter CLS (n 8) HALS (n 8) RALS (n 8) P Lymph node extraction NS Specimen length (cm) NS Margin status 100% negative 100% negative 100% negative NS T stage T0 2 (25.0%) 1 (12.5%) 1 (12.5%) NS T1 1 (12.5%) 0% 0% T2 1 (12.5%) 3 (37.5%) 4 (50.0%) T3 4 (50.0%) 4 (50.0%) 3 (37.5%) N stage N0 6 (75.0%) 5 (62.5%) 4 (50.0%) NS N1 1 (12.5%) 2 (25.0%) 3 (37.5%) N2 1 (12.5%) 1 (12.5%) 1 (12.5%) Overall stage 0 2 (25.0%) 1 (12.5%) 1 (12.5%) NS I 2 (25.0%) 3 (37.5%) 2 (25.0%) II 2 (25.0%) 1 (12.5%) 1 (12.5%) III 2 (25.0%) 3 (37.5%) 4 (50.0%) CLS conventional laparoscopic surgery; HALS hand-assisted laparoscopic surgery; NS not significant; RALS robotic-assisted laparoscopic surgery.

5 148 PATEL ET AL: 3-ARM MATCHED MIS COLORECTAL SURGERY TABLE 6. Postoperative outcomes Parameter CLS HALS RALS P Length of stay (d) CLS vs RALS (P.01) a Complications 3 (10%) 4 (13.3%) 4 (13.3%) NS Complications (description) Seroma, n 1 UTI, n 1 Seroma, n 1 Pelvic abscess (IR drainage), n 1 Pelvic abscess (IR drainage), n 2 Presacral abscess (transrectal drainage), n 1 Bowel obstruction (laparoscopic LOA), n 1 Extraction site infection, n 1 Postoperative ileus, n 2 Readmission 2 (6.7%) 2 (6.7%) 1 (3.3%) NS Operative reintervention 1 (3.3%) 0% 0% NS Data presented as mean SD or percent age. CLS conventional laparoscopic surgery; HALS hand-assisted laparoscopic surgery; IR interventional radiology; LOA lysis of adhesions; NS not significant;.rals robotic-assisted laparoscopic surgery; UTI urinary tract infection. Comparisons were made as follows: a malignant cases only. in the HALS group and one patient each in the CLS and RALS groups had a pelvic abscess presumably secondary to a contained anastomotic leak. All were successfully treated without operative intervention. One patient in the CLS group required laparoscopic lysis of adhesions in the early postoperative period for a bowel obstruction at the level of a loop ileostomy. There were no conversions to open or other MIS technique in any arm (Table 6). DISCUSSION Conventional laparoscopic colectomy was first reported in 1991 by Jacobs et al. 16 During this time, laparoscopic colorectal surgery gathered increased interest with escalating enthusiasm for improved patient outcomes (eg, reduced postoperative pain) and reduced cost (eg, reduced LOS). 16,17 Hand-assisted laparoscopic colectomy was first reported in 1996 as a technique facilitating use of the surgeon s hand in the abdomen while maintaining a minimally invasive platform. 18 This technique, providing tactile feedback for retraction and dissection, and has been shown to result in diminished operative times compared with laparoscopic surgery. Each of these techniques has been shown to be safe and feasible for colorectal procedures, with several short-term benefits 1 8 compared with open surgery. In 2002, the first robotic-assisted laparoscopic colectomy was reported. 19 Although RALS has been reported to be a safe and feasible approach for various colorectal procedures, comparative studies with other MIS modalities are limited. 14,15 The robotic platform is an enabling technology affording several potential advantages over CLS and HALS, including improved camera stability, 3-dimensional visualization and magnification of structures, fine motion scaling, tremor elimination, and wristed movements with added freedom of motion. The intraoperative and shortterm benefits of RALS in colorectal surgery have been described for procedures involving the deep and narrow confines of the pelvic anatomy. We aimed to assess the safety and efficacy of RALS compared with CLS and HALS through a matched-case analysis of intraoperative and short-term outcomes between these 3 minimally invasive modalities for colorectal surgery. We selected 30 RALS cases from our experience of 70 cases for the purposes of matching. To ensure no selection bias, we compared key parameters between the 30 selected and 70 total RALS cases. Absence of significant difference in all key parameters demonstrated unbiased selection, and RAL cases were subsequently matched to CLS and HALS cases. Cases were matched on the basis of preoperative characteristics with the intent to eliminate possible confounding factors of the comparative analysis. Exact matches were obtained with sex, pathology (benign or malignant disease), presence of neoadjuvant therapy (malignant cases only), surgical procedure, and surgeon. Body mass index was matched within 5 kg/m 2 within each triplet. Although age was not matched strictly, there was no significant difference in this parameter between the groups. Among all cases, RALS required longer total operative time compared with CLS (P.01) and HALS (P.001). This difference was not maintained in cases with low pelvic anastomoses, such as required for low anterior resection of mid-to-low rectal cancer. Patients with malignant disease who underwent the RALS technique experienced a significantly shorter length of stay compared with those who underwent the CLS approach. These findings are in line with our belief that the benefits of the robotic approach are most realized in those cases requiring dissection and retraction in the deeper and more confined surgical field of the pelvis. The RALS technique may have resulted in reduced intraoperative trauma and subsequent postoperative pain, leading to earlier discharge for this patient subgroup. Larger sample sizes and mesorectal grading in future studies would be important considerations to support or refute these findings.

6 DISEASES OF THE COLON & RECTUM VOLUME 54: 2 (2011) 149 Of the 90 cases in this study, the 2 with intraoperative complications were in the RALS group. This may be related to the surgeon s early experience with RAL compared with CLS and HALS. The traction injury resulted from the loss of tactile feedback during the RALS approach. In this case, it occurred at the location of a fixed robotic arm that was retracting the colon while countertraction was applied by a secondary arm. With experience, traction injuries are avoided as visual cues are relied on in the absence of tactile feedback. The thermal injury was encountered because of inefficient retraction, which resulted in displacement of the bowel into the operating field. Both injuries were readily recognized and repaired with intracorporeal robotic suture technique without further sequelae. Approximately one-third of patients in this series required splenic flexure takedown. Within the CLS and HALS groups, total operative time in cases with splenic flexure takedown was not significantly different from that of cases without takedown. This was not the case in the RALS group, in which splenic flexure takedown resulted in an additional 68 minutes of operating time. This may have occurred because we did not have a standardized surgical approach for this portion of the procedure in our early experience, which resulted in redocking and repositioning. In addition, the laparoscopic portion itself was cumbersome and prolonged as modification from our existing techniques was required for takedown using the robotic port sites. With regard to the malignant cases (n 8 in each group), the overall median lymph node extraction of 17 exceeded the median value of 12 reported for laparoscopic technique in a national randomized study comparing open with laparoscopic colectomy. 4 The mean lymph node extractions for CLS (20.9), HALS (16.3), and RALS (17.3) technique individually exceeded the previously reported values, and were not significantly different from each other. An additional important finding involved a relatively low postoperative complication rate found among all the modalities in this series (12.2%), which is comparable to previously reported rates for MIS techniques, ranging from 10% to 29%. 1,4,9,20 Although one might anticipate that a new technique such as RALS may initially result in higher complication rates compared with those of established modalities such as CLS and HALS, this was not our experience. In fact, RALS resulted in a comparably low complication rate compared with CLS and HALS, thus indicating the safety of this emerging approach. One of the limitations of this study includes the relatively small number of matched triplets ; however, given that 6 matching criteria were used in the formation of the triplets, a considerable number of possible confounders were removed from this analysis. Indeed, many other potential confounding factors (eg, clinical staging and distance from the anal verge in malignant cases, past abdominal surgical history in all cases, etc) remain. The inclusion of a greater proportion of malignant cases would have improved the heterogeneity of the cases under study as well as allowed for long-term follow-up in regard to disease-free and overall survival. Future studies may consider the inclusion of additional outcomes including mesorectal grading during pathology evaluation, quality-oflife assessment for bladder and sexual function, cost analysis, and long-term patient follow-up. An additional limitation of this study relates to the surgeon s learning curve. Before adopting the RALS technique, the surgeon had performed more than 500 CLS and HALS cases. The robotic cases included in this study occurred during the early part of the surgeon s RALS learning curve, leading one to expect a bias against intraoperative and postoperative outcomes. We included rectopexy because this procedure has been recognized as an applicable procedure for the robotic approach, specifically in regard to placement of transfixing sutures into the longitudinal ligament of the presacral fascia to perform the rectopexy. CONCLUSION RALS for benign and malignant diseases of the pelvis was shown to be safe and feasible, with short-term outcomes comparable to conventional and hand-assisted laparoscopic surgical approaches. With 3-dimensional visualization, increased range of motion, and improved ergonomics, this potentially enabling technology may play an increasingly important role in surgical procedures involving the rectum and rectosigmoid. REFERENCES 1. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350: Bonjer HJ, Hop WC, Nelson H, et al. Laparoscopically assisted vs open colectomy for colon cancer: a meta-analysis. Arch Surg. 2007;142: Buunen M, Veldkamp R, Hop WC, et al. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009;10: Guillou PJ, Quirke P, Thorpe H, et al. 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