Current Use and Surgical Efficacy of Laparoscopic Colectomy in Colon Cancer

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1 Current Use and Surgical Efficacy of Laparoscopic Colectomy in Colon Cancer Robert P Sticca, MD, FACS, Steven R Alberts, MD, Michelle R Mahoney, MS, Daniel J Sargent, PhD, Lisa M Finstuen, Garth D Nelson, MS, Timothy M Husted, MD, FACS, Jan Franko, MD, FACS, Charles D Goldman, MD, FACS, Barbara A Pockaj, MD, FACS BACKGROUND: The Clinical Outcomes in Surgical Therapy trial demonstrated that laparoscopic colectomy (LC) was equivalent to open colectomy (OC) for 30-day mortality, time to recurrence, and overall survival in colon cancer (CC) patients. Current use of LC for CC is not well known. STUDY DESIGN: Surgical data were reviewed for all patients randomized into a national phase III clinical trial for adjuvant therapy in stage III CC (North Central Cancer Treatment Group trial N0147). Colon resections were grouped as open (traditional laparotomy) or laparoscopic, including laparoscopic; laparoscopic assisted; hand assisted; and laparoscopic converted to OC. Statistical methods included nonparametric methods, categorical analysis, and logistic regression modeling. RESULTS: A total of 3,393 evaluable patients were accrued between 2004 and 2009; 53% were male, median age was 58 years, 86% were white, and 70% had a body mass index >25 kg/m 2. Two thousand one hundred thirteen (62%) underwent OC. One thousand two hundred eighty (38%) were initiated as laparoscopic procedures, 25% (n ¼ 322) were laparoscopic, 32% (n ¼ 410) were laparoscopic assisted, 26% (n ¼ 339) were hand assisted, and 16% (n ¼ 209) were LC converted to OC. Significant predictors of LC (vs OC) in multivariate models were T stage (T1 or T2 vs T3 or T4; p ¼ ), and absence of perforation, bowel obstruction, or adherence to surrounding organs (p < 0.01 each). Increasing rates of LC were observed over time, with LC eclipsing OC in 2009 (p < ). Surgical efficacy, measured by lymph node retrieval, was similar, with the mean number of lymph nodes retrieved higher in the LC group (20.6 vs 19.5 nodes; p ¼ ). CONCLUSIONS: This study demonstrated a steadily increasing use of LC for the surgical treatment of CC between 2004 and 2009, with LC preferred by study completion. Surgical efficacy was similar in stage III CC patients. (J Am Coll Surg 2013;217:56e63. Ó 2013 by the American College of Surgeons) Laparoscopic techniques for colon resection were first reported in ,2 and have demonstrated the advantages commonly attributed to laparoscopic surgery, including less pain, shorter recovery, and quicker return to baseline function. After initial reports demonstrated the feasibility of laparoscopic colectomy (LC) for colon cancer (CC), reports of port-site recurrences questioned the safety and oncologic efficacy of LC for CC. 3-6 Subsequently, CME questions for this article available at Disclosure Information: Authors have nothingto disclose. Timothy J Eberlein, Editor-in-Chief, has nothing to disclose. ClinicalTrials.gov number, NCT This study was conducted as a collaborative trial of the North Central Cancer Treatment Group, Mayo Clinic and was supported in part by Public Health Service grants CA-25224, CA-37404, CA-35103, CA-35113, CA-35272, CA , CA-32102, CA-14028, CA49957, CA21115, CA31946, CA12027, CA37377 from the National Cancer Institute, Department of Health and Human Services. Presented at the Western Surgical Association 120th Scientific Session, Colorado Springs, CO, November Received January 3, 2013; Revised February 19, 2013; Accepted February 19, From the Department of Surgery, University of North Dakota School of Medicine and Health Sciences, Grand Forks, ND (Sticca), Department of Medical Oncology (Alberts) and Cancer Center Clinical Research (Mahoney, Sargent, Finstuen, Nelson), Mayo Clinic, Rochester, MN, Department of Surgery, Toledo Clinic, Toledo, OH (Husted), Department of Surgery, Mercy Medical Center, Des Moines, IA (Franko, Goldman), and Department of Surgery, Section of Surgical Oncology, Mayo Clinic, Scottsdale, AZ (Pockaj). Correspondence address: Robert P Sticca, MD, FACS, Department of Surgery, University of North Dakota, School of Medicine and Health Sciences, 501 North Columbia Rd, Grand Forks, ND robert.sticca@med.und.edu ª 2013 by the American College of Surgeons ISSN /13/$36.00 Published by Elsevier Inc. 56

2 Vol. 217, No. 1, July 2013 Sticca et al Laparoscopic Colectomy in Colon Cancer 57 Abbreviations and Acronyms CC ¼ colon cancer COST ¼ Clinical Outcomes in Surgery Trial LC ¼ laparoscopic colectomy LN ¼ lymph node NCCTG ¼ North Central Cancer Treatment Group OC ¼ open colectomy several studies were published addressing the safety and efficacy of laparoscopic surgery for CC. 7-9 The seminal trial in the United States was the Clinical Outcomes in Surgery Trial (COST), 7 which was reported in This prospective randomized trial evaluating LC for CC performed by credentialed surgeons demonstrated similar rates of overall recurrence, wound recurrence, overall survival, reoperation, 30-day mortality, hospital readmission, and complications. Benefits for the laparoscopic surgery group were shown in the perioperative recovery period with shorter hospital stay and reduced use of narcotics. After the safety and efficacy of LC for CC was established in prospective randomized clinical trials, the procedure was gradually adopted by the surgical community. The rates of acceptance and use of this procedure are not well known and have been questioned. 10 The North Central Cancer Treatment Group (NCCTG) N0147 trial was a large, multi-institutional, prospective, randomized clinical trial designed to evaluate the efficacy of different chemotherapy regimens used in adjuvant therapy for stage III CC. 11 This trial was sponsored by the NCCTG, but was available to other cooperative study groups through the intergroup mechanism. The trial was open to a diverse range of hospitals, including community hospitals, university-affiliated hospitals, and university medical centers. Only patients with pathologically proven stage III CC after surgical resection were eligible for this trial. Surgical data were collected prospectively before randomization and were a mandatory part of the eligibility criteria for entry into the trial. Although the NCCTG N0147 trial was not specifically designed to evaluate surgical methods, the time period in which it was conducted and the complete and prospective nature of the surgical data collection made it an ideal vehicle to study the use and efficacy of LC in the era immediately after the dissemination of the results of the COST study. In addition, an analysis of the factors associated with attempted LC was possible with the data collected for enrollment in this trial. The goals of this study were to evaluate the use and efficacy of LC in the time period after the COST trial and to assess factors associated with the type of procedure attempted. This report describes the use, efficacy, and factors associated with LC for CC using the surgical data for >3,300 stage III CC patients entered into the NCCTG N0147 trial. METHODS The NCCTG N0147 trial was conducted from February 10, 2004 to November 25, 2009 and included patients with histologically proven stage III (any T, N1 or N2, M0) CC after complete surgical resection. Tumors were required to be at least 12 cm from the anal verge and an en bloc resection was required for patients with locally advanced tumors. Other eligibility criteria included age 18 years or older; 1 or more pathologically confirmed involved lymph node (LN); Eastern Cooperative Oncology Group performance status of 0 to 2; and adequate hematologic, hepatic, and renal function. No earlier chemotherapy, immunotherapy, or radiotherapy for CC was allowed. Institutional Review Board approval was required at all of the participating centers and all participants were provided written informed consent. Multiple chemotherapy regimens were compared, including combinations of oxaliplatin, irinotecan, 5FU, leucovorin, and cetuximab for the 3,397 patients enrolled in this trial. Because of reported findings from other studies on adjuvant chemotherapy regimens for stage III CC, which were revealed during the course of the N0147 trial, some of the chemotherapy arms in the N0147 study were adjusted or deleted. The final analysis on the efficacy of the adjuvant chemotherapy regimens from this study reported on 2,686 patients who received leucovorin, 5FU, and oxaliplatin (FOLFOX) with or without cetuximab regimen. 11 Because the surgical resection of the stage III CCs was completed on all enrolled patients before randomization to the different chemotherapy regimens, there was no effect of these regimens on the surgical or demographic data collected in this study. Therefore, the surgical data on all 3,397 patients initially involved in this trial were used for this analysis. The surgical procedure performed was entirely at the discretion of the operating surgeon and had no effect on a patient s entry into the trial. The documentation necessary for entry into the trial included a copy of the surgeon s dictated operative notes, as well as the final pathology report from the resected surgical specimen. The operative and pathology reports were reviewed by a member of the surgery committee of the NCCTG who was knowledgeable in laparoscopic surgery. The reviewing surgeon assigned each operative procedure to a category of LC or open colectomy (OC) as defined in Table 1. For this analysis, all minimally invasive procedures, including laparoscopic, laparoscopic assisted, hand assisted, and

3 58 Sticca et al Laparoscopic Colectomy in Colon Cancer J Am Coll Surg Table 1. Definitions of Surgical Categories Used in N0147 Patients Procedure type Definition Open colectomy Procedure done through a standard laparotomy incision with no laparoscopic or hand assistance Laparoscopic colectomy Procedure done completely laparoscopic with intracorporeal anastomosis Laparoscopic-assisted colectomy Procedure in which the colon was mobilized laparoscopically (with or without vascular dissection and ligation), but the anastomosis was done extracorporeally. Hand-assisted colectomy Procedure in which a hand port is used in conjunction with laparoscopic mobilization, anastomosis done intracorporeally or extracorporeally Laparoscopic colectomy converted to open colectomy Procedure begun with intent to perform laparoscopically but converted to open for any reason. laparoscopic converted to open, were grouped together under the category of LC. The laparoscopic converted to open cases were included in the laparoscopic category because the surgical procedure was initiated laparoscopically. Therefore, the LC group includes all laparoscopic cases both attempted (laparoscopic converted to open category) and completed (laparoscopic, laparoscopic assisted, and hand assisted). Statistical analysis was performed using frequency tables and categorical methods (ie, chi-square and Fisher s exact test) were used to describe the distributions of covariates. Nonparametric methods were used (ie, Wilcoxon test and Kruskal-Wallis test), when appropriate. Univariate and multivariate logistic regression models were used to explore the associations between covariates and the outcomes of having a laparoscopic (vs open) colectomy. Covariates with multiple levels (eg, body mass index and tumor location) were redefined into smaller and more clinically relevant classifications for modeling purposes (eg, eliminating categories with extremely low frequencies). All p values reported are 2-sided and values <0.05 are considered statistically significant. Analyses have not been adjusted for multiple comparisons. RESULTS A total of 3,397 patients underwent colectomy for CC in this trial, of which surgical data were complete for 3,393 (99.9%), which form the basis for this analysis. Demographic data for these patients are listed in Table 2. Mean age was 57.6 years (range 19 to 86 years), 52.5% of patients were male, 85.9% were white, and the majority (70.1%) were overweight or obese with a body mass index >25. There were no statistically significant differences between the patients who had LC or OC for these demographic characteristics. The majority of patients were insured with private or governmentsponsored insurance. Table 3 shows the characteristics of the resected pathology specimens for the patients in this study. Most (73.3%) tumors were T3, with a majority (59.1%) having between 1 and 3 LNs involved. The number of LNs removed was significantly higher in the LC group (p ¼ ). The 2 most common tumor locations were the right colon (41.2%) and sigmoid colon (39.3%), with a statistically significant difference between LC and OC for tumors in the cecum (p ¼ ), transverse colon (p ¼ ), and descending colon (p ¼ ). Multivariate analysis of factors associated with LC (Table 4) revealed that patients who had bowel perforation, obstruction, or adherence to a surrounding organ were less likely to undergo a laparoscopic procedure. Additionally, the year in which the patient was operated on was significantly associated with the type of procedure that was performed. The types of procedures performed are shown in Figure 1. The change in the laparoscopic compared with open procedures over time are shown in Figure 2. The increase in laparoscopic procedures over time was highly statistically significant (p < ), with the laparoscopic approach eclipsing the open approach by the end of the study (2009). DISCUSSION In the United States, use of laparoscopic surgery for different applications in general surgery has evolved rapidly since it was first described for cholecystectomy in Initially, there was skepticism about the use of laparoscopic surgery for bowel resection, especially when malignancy was the reason for resection. 3-6 This skepticism was gradually replaced with enthusiasm for LC after the safety and efficacy of this procedure was demonstrated by multiple randomized clinical trials. 7-9 The N0147 trial was started April 10, 2004, one month before the report of the COST trial 7 (May 13, 2004), which documented the outcomes and benefits of LC for CC. Because the N0147 trial started almost simultaneously with the most important report on the safety and efficacy of LC in the United States, we believed that the surgical data from N0147 would be ideal for evaluating the acceptance and use of laparoscopic surgery

4 Vol. 217, No. 1, July 2013 Sticca et al Laparoscopic Colectomy in Colon Cancer 59 Table 2. Patient Characteristics by Procedure Type Characteristic Laparoscopic (n ¼ 1,280) Open (n ¼ 2,113) Total (n ¼ 3,393) p Value Age, y Mean (SD) 57.3 (10.9) 57.8 (11.2) 57.6 (11.1) Median Range 19.0e e e86 Sex, male, n (%) 655 (51.2) 1,127 (53.3) 1,782 (52.5) Race, n (%) White 1,082 (84.5) 1,832 (86.7) 2,914 (85.9) Black or African American 97 (7.6) 143 (6.8) 240 (7.1) Native Hawaiian or Pacific Islander 4 (0.3) 12 (0.6) 16 (0.5) Asian 66 (5.2) 83 (3.9) 149 (4.4) American Indian or Alaska Native 7 (0.5) 9 (0.4) 16 (0.5) Not reported: patient refused or not available 18 (1.4) 20 (0.9) 38 (1.1) Unknown: patient unsure 6 (0.5) 14 (0.7) 20 (0.6) BMI Missing, n BMI <20, underweight, n (%) 49 (3.8) 91 (4.3) 140 (4.1) 20 BMI <25, normal, n (%) 322 (25.3) 547 (26.0) 869 (25.7) 25 BMI <30, overweight, n (%) 470 (36.9) 740 (35.1) 1,210 (35.8) 30 BMI <35, obese, n (%) 254 (19.9) 427 (20.3) 681 (20.1) 35 BMI, obese, n (%) 179 (14.1) 301 (14.3) 480 (14.2) Health insurance Missing, n Private or Medicare/private, n (%) 957 (74.8) 1,446 (68.5) 2,403 (70.9) Medicaid or Medicare/Medicaid, n (%) 44 (3.4) 79 (3.7) 123 (3.6) Medicare, n (%) 98 (7.7) 184 (8.7) 282 (8.3) No means or self pay (no insurance), n (%) 43 (3.4) 101 (4.8) 144 (4.2) Military/veteran/other, n (%) 137 (10.7) 302 (14.3) 439 (12.9) BMI, body mass index (calculated as kg/m 2 ). for CC in the initial 5 years after it was shown to be safe and beneficial. In addition, because this trial involved multiple types of institutions across North America, the surgical data should be representative of the surgical techniques used for CC in a broad spectrum of institutions, therefore, providing an accurate reflection of the use of LC for CC in North America during that time. Data from this study indicate a significant change in the use of laparoscopic surgery for CC during this time period. The percentage of CCs resected laparoscopically increased steadily each year during the study and by the end of the study the majority of the cancers were resected laparoscopically. As one would expect, the number of cases attempted laparoscopically was significantly lower when there was bowel obstruction, perforation, or adherence to an adjacent organ. This likely represents the surgeon s judgment that LC was not appropriate when these locally advanced tumors were encountered. Additionally, the significantly higher rate of open resection of tumors of the transverse and left colon and laparoscopic resection of cecal tumors is consistent with recommendations for LC at that time. As surgeons have gained experience in LC and the techniques and equipment have improved, tumors in all locations in the colon are now believed to be appropriate for minimally invasive techniques. Although the efficacy of a surgical procedure for malignancy depends on many factors, including the intraoperative ability to assess for metastatic disease, complete resection of the tumor with a negative margin, and the immediate and long-term outcomes of the surgery, many of these factors can be difficult to evaluate in a clinical trial. A surrogate marker for efficacy that has been used is the number of LNs retrieved in the resected specimen. These data give an indication of the completeness of resection, as an incomplete resection of the colonic mesentery would yield a lower number of LNs. Previously published prospective randomized trials comparing LC with OC have demonstrated the number of LNs removed in LC was

5 60 Sticca et al Laparoscopic Colectomy in Colon Cancer J Am Coll Surg Table 3. Tumor Characteristics by Procedure Type Characteristic Laparoscopic (n ¼ 1,280) Open (n ¼ 2,113) Total (n ¼ 3,393) p Value T stage < Missing, n T1 or T2, n (%) 243 (19.1) 265 (12.5) 508 (15.0) T3, n (%) 908 (70.9) 1,580 (74.8) 2,488 (73.3) T4, n (%) 129 (10.1) 267 (12.6) 396 (11.7) Lymph node involvement, n (%) e3 750 (58.6) 1,254 (59.3) 2,004 (59.1) (41.4) 859 (40.7) 1389 (40.9) No. of nodes examined, mean (SD) 20.6 (11.5) 19.5 (11.0) 19.9 (11.2) Tumor location, n (%) Cecum 313 (24.5) 453 (21.5) 766 (22.6) Ascending colon 247 (19.3) 382 (18.1) 629 (18.6) Hepatic flexure 72 (5.6) 111 (5.3) 183 (5.4) Transverse colon 87 (6.8) 221 (10.5) 308 (9.1) Splenic flexure 47 (3.7) 104 (4.9) 151 (4.5) Descending colon 63 (4.9) 157 (7.4) 220 (6.5) Sigmoid colon 510 (39.9) 822 (39.0) 1,332 (39.3) equivalent to OC. Two prospective randomized trials from Europe (Barcelona, Spain, 8 and COLOR [Colon Cancer Laparoscopic or Open Resection] trial 9 )demonstrated an equivalent number of LNs retrieved from both the LC and OC arms. Our data demonstrated a statistically significant (p < ) higher number of LNs from specimens of patients who had LC (20.6 vs 19.5), confirming that LC is equivalent to OC for this measure of surgical efficacy. Although the difference in the number of LNs retrieved was statistically significant, this significance is a result of the large sample size and, for all practical purposes, the difference of 1 LN in the LC specimens is not clinically meaningful. Rea and colleagues studied the use of LC for CC through the Nationwide Inpatient Sample database during the time periods 2001 to 2003 and 2005 to Their study of >740,000 elective colectomies demonstrated that, despite an almost 3-fold increase (2.3% vs 8.9%) in LC for CC between these 2 time Table 4. Multivariate Cox Models for Factors Associated with Laparoscopic Colectomy Variable Odds ratio (95% CI) Wald p value Overall Wald p value Adherence 0.68 (0.54e0.85) Bowel obstruction 0.39 (0.31e0.49) < < Bowel perforation 0.59 (0.40e0.88) Stage T (0.62e0.93) T (0.57e1.05) Payment method Medicare/Medicaid 1.16 (0.75e1.79) Military 0.93 (0.60e1.44) Private 1.42 (0.96e2.10) Surgery year < (1.28e3.25) (2.92e6.12) (3.22e6.38) (4.39e8.84) < (6.42e13.06) <0.0001

6 Vol. 217, No. 1, July 2013 Sticca et al Laparoscopic Colectomy in Colon Cancer 61 print & web 4C=FPO print & web 4C=FPO Figure 1. Colectomy procedure type (n ¼ 3,393). periods, the absolute rate of LC for CC was low. The authors state that there is clear lack of adoption of LC in the United States. Our study refutes this assertion, demonstrating a predominance of LC for stage III CC by the 5 th year after the COST trial (2009). There might be multiple reasons for this difference, but it seems that the Rea study did not collect data for sufficient time after the publication of the COST trial to demonstrate that surgeons had adopted laparoscopic surgery for colon resection in CC. Considering the time for adoption of other new surgical procedures (eg, breast-conservation surgery for breast cancer), it appears as though the use of LC for CC has occurred fairly quickly. Our study does have limitations, which include the limited stage of disease (stage III only), which was available for study in this database. These data might not Figure 2. Laparoscopic colectomy vs open colectomy, by year. represent the overall use of laparoscopic techniques for CC at the participating institutions, but it seems reasonable to assume that if its use is increasing for stage III disease, the same trend would be seen in earlier stages of CC, because tumors that are stage I and II are usually more amenable to laparoscopic techniques than stage III tumors. Additional analysis of these data for trends in conversion to open procedures, as well as outcomes by type of surgery, is planned. CONCLUSIONS This study demonstrates a steadily increasing and statistically significant increase in use of laparoscopic surgery for colectomy in CC after publication of the COST trial. Laparoscopic surgery might now be the predominant procedure for surgical resection of CC when the appropriate conditions are present. Author Contributions Study conception and design: Sticca, Pockaj Acquisition of data: Sticca, Alberts, Finstuen, Husted, Franko, Goldman, Pockaj Analysis and interpretation of data: Sticca, Alberts, Mahoney, Sargent, Nelson, Pockaj Drafting of manuscript: Sticca, Mahoney, Nelson, Pockaj Critical revision: Sticca, Alberts, Mahoney, Sargent, Finstuen, Nelson, Husted, Franko, Goldman, Pockaj REFERENCES 1. Fowler DL, White SA. Laparoscopy-assisted sigmoid resection. Surg Laparosc Endosc 1991;1:183e Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc 1991;1:144e Berends FJ, Kazemier G, Bonjer HJ, Lange JF. Subcutaneous metastases after laparoscopic colectomy. Lancet 1994; 344: Reilly WT, Nelson H, Schroeder G, et al. Wound recurrence following conventional treatment of colorectal cancer: a rare but perhaps underestimated problem. Dis Colon Rectum 1996;39:200e Vukasin P, Ortega AE, Greene FL, et al. Wound recurrence following laparoscopic colon cancer resection. Results of the American Society of Colon and Rectal Surgeons Laparoscopic Registry. Dis Colon Rectum 1996;39[Suppl]:S20eS Johnstone PAS, Rohde DC, Swartz SE, et al. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol 1996;14:1950e The Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 2004;350:2050e Lacy AM, Garcia-Valdecasas JC, Delgado S, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trial. Lancet 2002;359:2224e2229.

7 62 Sticca et al Discussion J Am Coll Surg 9. Veldecamp R, Kuhry E, Hop WC, et al. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomized trial. Lancet Oncol 2005;6: 477e Rea JD, Cone MM, Diggs BS, et al. Utilization of laparoscopic colectomy in the United States before and after the Clinical Outcomes of Surgical Therapy study group trial. Ann Surg 2011;254:282e Alberts SR, Sargent DJ, Nair S, et al. Effect of oxaliplatin, fluorouracil, and leucovorin with or without cetuximab on survival among patients with resected stage III colon cancer. JAMA 2012;307:1383e1393. Discussion INVITED DISCUSSANT: DR JOHN RUSSELL (Albuquerque, NM): It has been more than 21 years since the first case report of a laparoscopic colectomy for a villous adenoma by Cooperman, and the first published series of 20 laparoscopic colectomies by Jacobs, which included 8 colectomies for cancer. Yet, unlike laparoscopic cholecystectomy, for many surgeons, laparoscopic colectomy has not replaced open colectomy as the standard approach for nonemergent colon cancer surgery. Although the patient benefits of laparoscopic surgery would seem obvious, there have been concerns regarding the adequacy of laparoscopic colectomy as a cancer operation in terms of margins of resection and lymph node harvest. Early on, the specter was raised of potential port site tumor implantation. Perhaps the greatest barrier to adoption, especially for the low-volume colon surgeon, was the steep learning curve for the procedure when compared with laparoscopic cholecystectomy. The Clinical Outcomes of Surgical Therapy (COST) trial in 2004 first demonstrated the noninferiority of laparoscopic colectomy compared with open colectomy for management of curable colon cancer. Although the laparoscopic procedures were longer (by an average of 55 minutes), they were associated with shorter hospital stays and less time requiring parenteral narcotics and oral analgesics. Nodal harvest was equivalent with both techniques. The conversion rate from laparoscopic to open technique was 21%. There were no differences in postoperative complications, readmission rates, and 30-day mortality. At 5 years, recurrence and survival rates were also equivalent. Reviews of prospective randomized trials evaluating the short-term benefits of laparoscopic colectomy by Schwenk in 2005, and of the long-term outcomes of laparoscopic colorectal resection for cancer by Kuhry in 2008, confirmed the findings of the COST trial and should put any lingering concerns aside. For the cost of a longer operative procedure (average additional length of 42 minutes), patients undergoing laparoscopic colectomy have less postoperative pain, improved postoperative pulmonary function, quicker return of bowel function, shorter hospital stays, fewer wound infections, and improved quality of life at 30 days postprocedure. The overall rates of postoperative complications and operative mortality are equivalent to those of open surgery. The long-term outcomes of laparoscopic colectomy confirm its adequacy as a cancer operation, although the data are limited for laparoscopic rectal cancer patients. The average number of lymph nodes harvested may be slightly less with laparoscopic colectomy (15 vs 16 lymph nodes), there is no difference with margin adequacy, and cancer outcomes, cancer-related deaths, rates of port site or wound recurrence, and rates of peritoneal recurrence, are equivalent between laparoscopic and open colectomy. The rate of reoperations for late complications, such as hernias and for adhesive disease, was also found to be equivalent. Not all patients are candidates for the laparoscopic technique, and the rate of conversion from laparoscopic to open surgical technique varies with patient selection and institutional experience. Kuhry reported a 24% conversion rate for low-volume hospitals and a 9% conversion rate for high-volume hospitals. This report by Sticca and colleagues of participants in the North Central Cancer Treatment Group (NCCTG) N0147 trial of different adjuvant chemotherapy regimens for stage III colon cancer (any T, N1 or N2, Mx) examined the changing pattern of use of laparoscopic and open colectomy among a diverse group of surgeons and institutions during the period of that trial (2004 to 2009). Randomization to adjuvant chemotherapy occurred after surgery; there was no randomization of surgical technique. The laparoscopic group (38% of total procedures performed), included laparoscopic-only cases (10%), laparoscopic-assisted procedures (12%), hand-assisted procedures (10%), and laparoscopic converted to open procedures (intention to treat as laparoscopic procedures, 6%). The choice of the specific laparoscopic technique reflects surgeon preference. The conversion rate from laparoscopic to open technique was 16% (209 of 1,280 procedures). Other than a slightly higher nodal harvest in the laparoscopic cases (average 20.6 vs 19.5 nodes), comparative patient cancer outcomes between the laparoscopic and open operations were not reported. The authors noted the progressive trend toward laparoscopic surgery as the favored operative approach during the 6 years of the study. In 2004, only 12% of colectomies in the study were done by one of the listed laparoscopic approaches; by 2009, that figure had steadily risen to 53%. During the course of the study, open surgery was used more frequently for larger primary tumors (T3, T4), when adherence to surrounding structures was recognized, when there was bowel obstruction or perforation, and for tumors of the transverse and descending colon, although the authors commented that during the course of the study surgeons appeared to be more willing to tackle transverse and descending colon lesions. Having private or Medicare/private insurance also appeared to increase the likelihood of laparoscopic colectomy. Temporal trends in technique within the laparoscopic group (for example, laparoscopic-only vs laparoscopic-assisted or hand-assisted techniques ) were not reported. For surgeons offering laparoscopic colectomy to their colon cancer patients, they must demonstrate that they can perform these procedures safely, with equivalent or less short-term patient morbidity when compared with the open surgical approach, and without compromising the adequacy of the tumor resection and lymph node harvest performed. This report would indicate that in clinical practice, an increasing number of patients are being offered this option by their surgeons, presumably with the benefits previously reported in controlled randomized clinical trials. I have several questions for the authors:

8 Vol. 217, No. 1, July 2013 Sticca et al Discussion What should be the medical staff credentialing criteria for laparoscopic colectomy, and how should new medical staff members be proctored in these techniques? 2. Rectal tumors were specifically excluded from both the COST trial and the NCCTG N0147 trial (and therefore from this report), and the Cochrane review notes that long-term data on laparoscopic approaches to tumors of the rectum are limited. What are your thoughts regarding laparoscopic surgical approaches for curable rectal cancers? 3. Finally, as more institutions acquire surgical robots, the interest of surgeons in using robotic surgical approaches for colon and rectal cancer will likely increase. As we have seen from our urologic and gynecologic colleagues, the pelvis should be the ideal anatomic area for robotic surgery. How should robotic surgery fit into the armamentarium of minimally invasive surgical options for colorectal cancer? DR ROBERT STICCA: As far as credentialing for laparoscopic procedures, that s a hard thing to assess. For residents coming out of training who are doing a significant number of these procedures, I honestly don t think it should be any different than 10 or 20 years ago, when we got out and we were able to do open colectomies. For individuals who are learning laparoscopic techniques, established surgeons, I think in that situation, some degree of proctoring and mentoring is probably appropriate. Again, each institution has to decide this on its own. At least in our institution, we have pretty rigorous credentialing criteria for any new procedure. I would hesitate to say at this point that laparoscopic colectomy is a new procedure, since it s been around for at least 10 years that most institutions have been doing it. In regard to rectal cancer, I certainly would agree that at least I know our colorectal surgeons do most of their rectal operations with a total mesorectal excision, and mostly these are done either as hand-assisted or laparoscopic procedures. This question also brings up your final point, which is robotic surgery. As you mention, the pelvis, especially the male pelvis, is an ideal situation for robotic surgery. I think that in the future, if the cost of robotic surgery can come close to what we now have for laparoscopic or open surgery, then I think it will probably be the preferred method in many institutions, especially larger institutions that have the funding to purchase one of these devices. So I think that rectal cancer will certainly be predominantly laparoscopic or minimally invasive. And robotic, I think, is the wave of the future. DR RON GAGLIANO (Honolulu, HI): Looking at your data, I have a question as to whether these were unequal groups. Looking at the proportions of operations, it appeared that there were more right and sigmoid laparoscopic colectomies and more transverse, rectal, complicated cases in the open group. So is this an applesto-oranges comparison? The second part is, you showed a statistically significant difference between a 20.6 and 19.5 average lymph node harvest. I want to know what the clinical significance of that difference is, and is that possibly attributed to an unequal analysis of the groups, or are the groups just uneven because this is a retrospective study? DR ROBERT STICCA: I will answer your second question first. I think that the difference of 19 vs 20 lymph nodes is probably not significant. As you know, for appropriate staging, it s thought that you should have at least 12 lymph nodes. And, actually, one of our statisticians commented that just because of the large number of patients, the p value came out significant. To me, it means that the procedures are being done equivalently and there is just as good a resection of the mesentery in a laparoscopic procedure as an open procedure. In answer to the first question, about the difference in the groups, yes, there were more right colectomies. And I think, as many people begin to do these procedures, the right colon procedures tend to be a little technically easier and would have been done more often. But as more and more people get experience with laparoscopic surgery, I think it s just like with gallbladders, where initially we did only straightforward noninfected gallbladders and now everybody does all sorts of acute cholecystitis. So I think the main thing that we wanted to show in this study was just the increasing incidence of laparoscopic surgery, and that now it predominates as the method of choice for colon cancer.