Feasibility of laparoscopic techniques as the surgical approach of choice for primary colorectal cancer

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1 Surg Endosc (2008) 22: DOI /s Feasibility of laparoscopic techniques as the surgical approach of choice for primary colorectal cancer An analysis of 570 consecutive cases Seok-Byung Lim Æ Hyo Seong Choi Æ Seung-Yong Jeong Æ Jae-Gahb Park Received: 17 August 2007 / Accepted: 24 January 2008 / Published online: 6 March 2008 Ó Springer Science+Business Media, LLC 2008 Abstract Background Since the Clinical Outcomes of Surgical Therapy (COST) trial data were reported in May 2004, the laparoscopic technique for primary colorectal cancer has been increasingly used and become the approach of choice at our center. This study aimed to evaluate our laparoscopic experience of 570 consecutive patients between October 2000 and December 2006, and assess the feasibility of this technique as the surgical approach of choice for primary colorectal cancer. Methods The study times were divided into three periods based on the COST trial report and the time when the laparoscopic technique was accepted as the surgical approach of choice at our center (period I: October 2000 to May 2004, II: June 2004 to December 2005, III: January to December 2006). Data regarding clinicopathological, surgical, and perioperative outcomes were collated from registry and compared between periods. Results The use of laparoscopic surgery increased from 2.4% in period I, to 19.2% in period II, to 66.1% in period III. Over the periods, the proportion of rectal cancer and right colon cancer increased (p \ 0.001), T- and N-stage became more advanced (p \ 0.001, p = respectively), and This work supported by National Cancer Center Grant S.-B. Lim H. S. Choi (&) S.-Y. Jeong J.-G. Park Center for Colorectal Cancer, Research Institute & Hospital, National Cancer Center, 809 Madu1-dong, Ilsan-gu, Goyang-si, Gyeonggi-do , Korea hschoi@ncc.re.kr Present Address: J.-G. Park Department of Surgery, Seoul National University College of Medicine, 28 Yongon-dong, Chongno-gu, Seoul , Korea operative time decreased (p \ 0.001). The overall open conversion and morbidity rates were 3.5% and 9.8%, respectively, and these did not differ between periods. Conclusion It was possible to apply laparoscopic approach in two-thirds of primary colorectal cancer patients. The short-term favorable outcomes support the feasibility of laparoscopic technique as surgical approach of choice for colon cancer. Laparoscopic resection for rectal cancer may require a randomized clinical trial prior to gain similar acceptance. Keywords Colon cancer Rectal cancer Laparoscopy The first cases of laparoscopic colorectal resection were reported in 1991 [1]. Despite the procedure being one of the most important recent innovations in surgery, its use in treating colorectal cancer has been controversial due to technical difficulties associated with a steep learning curve [2] and concerns related to oncological safety. While the former issue has been somewhat resolved through new technology and increased operator s experience, oncological safety continues to cause concerns. As such, the National Institute for Clinical Excellence (NICE) stated in 2000 that open rather than laparoscopic resection should be the preferred surgical procedure for colorectal cancer [3]. However, recent randomized controlled trials [4 10] suggest that this recommendation may need amending. The Clinical Outcomes of Surgical Therapy (COST) study group reported in May 2004 that laparoscopic colectomy for colon cancer offers the same oncological outcomes as the open procedure [7]. This report led the American Society of Colon and Rectal Surgeons (ASCRS) and the Society of American Gastrointestinal and Endoscopic

2 Surg Endosc (2008) 22: Surgeons (SAGES) to endorse laparoscopic resection for curable colon cancer [11]. As a result, many colorectal surgeons now use this technique as the preferred surgical approach, and its use in colorectal cancer has rapidly increased. At our center, the laparoscopic approach has been increasingly used since the 2004 May COST trial report, and has become the approach of choice. Since 2006, we apply this approach to virtually all-elective surgery for colorectal cancer. The aim of the present study was to evaluate our laparoscopic experience and assess the feasibility of this technique as the surgical approach of choice in primary colorectal cancer. upper rectal cancer cases; during period II (June 2004 to December 2005), laparoscopic surgery was applied more broadly with increasing of experiences: and during period III (January to December 2006), the laparoscopic technique was the surgical approach of choice for primary colorectal cancer. The exclusions for the laparoscopic approach in period III were patients requiring emergency procedures (obstruction, bleeding, perforation), intolerance of a pneumoperitoneum (severe cardiopulmonary insufficiency), history of prior major abdominal surgery, locally far-advanced tumor, participants in the open surgery arm of the randomized trial, and those who opposed the laparoscopic approach. Materials and methods Patients and division of study period From October 2000 to December 2006, 2,820 patients diagnosed with primary colorectal cancer underwent surgery at the Center for Colorectal Cancer, National Cancer Center (Korea). Of those 2,820 patients, 2,250 underwent conventional open surgery and 570 underwent laparoscopic surgery. The records of the 570 consecutive patients who underwent laparoscopic surgery were collected prospectively. The following patient data were collected: age, sex, body mass index (BMI), location of tumor, preoperative workup, preoperative treatment, type of operation, operation time, estimated blood loss, intraoperative adverse events, pathological findings with nodal status, postoperative complications, hospital stay, and recurrence. Conversion to open laparotomy was defined as an early or unplanned need for a midline laparotomy for completion of the operative procedure, and operative mortality was defined a mortality within 1 month postoperatively. Tumor stage was determined using the American Joint Committee on Cancer TNM system [12]. The study times were divided into three periods based on the COST trial report and the time when laparoscopic technique was accepted as the surgical approach of choice at our center in January In January 2006, we launched a prospective randomized phase III trial of laparoscopic surgery for locally advanced rectal cancer with preoperative chemoradiotherapy. The protocol was approved by the local Ethical Committees of the National Cancer Center, Korea. Prior to randomization, informed consent was obtained from participating patients. Different criteria were used to recruit patients in the laparoscopy program in the three study periods: during period I (October 2000 to May 2004), the laparoscopic approach was only applied highly selected early colon and Preoperative workup and therapy To establish the diagnosis and determine the extent and staging of the disease, patients underwent preoperative workups such as digital rectal examination, complete blood count, liver function test, level of carcinoembryonic antigen, colonovideoscopy with biopsy, and computed tomography (CT) scanning of the abdomen and pelvis. Transrectal ultrasonography, chest CT, magnetic resonance scanning of liver and pelvis, and F-18 deoxyfluoroglucose positron emission tomography (FDG- PET) were performed where required. Patient preoperative risk was evaluated using the American Society of Anesthesiologists (ASA) scoring system. A tumor was considered a primary rectal cancer when located within 15 cm of anal verge as determined by rigid sigmoidoscopy. Patients with locally advanced rectal cancer (clinically T3 or T4 stage) and no evidence of distant metastases received preoperative chemoradiation therapy (CRT) involving 50.4 Gy radiation and fluoropyrimidinebased chemotherapy. Of the 187 rectal cancer patients, 58 (31.0%) received CRT prior to laparoscopic surgery. Five obstructive left colonic cancer patients underwent bowel decompression using metal stents, and elective laparoscopic surgery. Surgical preparation and details of procedures Four surgeons experienced in both laparoscopic and conventional open surgery performed all operations, and all patients gave informed consent prior to surgery. Patients received mechanical bowel preparation with 4 L polyethylene glycol on the day prior to surgery. A dose of broadspectrum intravenous antibiotics was administered on call to the operating room and elastic stockings were instituted for antithrombotic prophylaxis. During the study period, a low-molecular-weight heparin had been used for selective

3 2590 Surg Endosc (2008) 22: cases with high risk of thrombosis, such as recent history of strokes. No epidural blocks were used. In the operating room, patients were placed in the modified lithotomic position. For left-sided tumors, the operator and the assistant holding the camera stood on the right side of the patient, with the assistant surgeon on the left. For rightsided tumors, the operator stood on the left side of the patient, with the assistant holding the camera stood between the legs of the patient, and the assistant surgeon stood on the right. Five trocars were usually introduced (two or three 5-mm, one 11-mm, and one or two 12-mm). The 30 laparoscope was introduced through an 11-mm umbilical port. A pneumoperitoneum was created using CO 2 gas to a maximum pressure of 12 mmhg, after which laparoscopic exploration was undertaken. Dissection was performed along the avascular plane according to the location of the tumor. Vessels were ligated close to their origin using clips with medial approach, and a complete dissection was performed. For rectal dissection, an assistant drew the sigmoid colon and upper rectum cephalic direction using forceps and the operator separated the mesorectum from the fascia propria of the sacrum. The surgeon performed fine dissection into the presacral space while keeping the proper plane of dissection between the fascia propria of the rectum and the presacral fascia. After dissection proceeds distally into the pelvic cavity, the surgeon dissected Waldeyer s fascia, the lateral side of the rectum, and Denonvilliers fascia in order. Once the rectum was completely mobilized, one or two endoscopic linear stapling devices were introduced through the right lower port and transected the rectum. The diseased colorectum was extracted through a 5-cm skin incision with the abdominal wall protected by a vinyl cover and resected. A bowel anastomosis was performed intracorporeally (anterior or low-anterior resection) or extracorporeally (right hemicolectomy, coloanal anastomosis). Statistical analysis Statistical analysis was performed using Pearson s chisquare test, Fisher s exact test, or Student s t-test depending on the nature of the data. A two-tailed p value \ 0.05 was considered to indicate a significant difference. Results Data analysis was performed for all 570 patients who underwent consecutive laparoscopic surgery for primary colorectal cancer, including those who were converted to open procedure. Of the 570 patients, 569 underwent colorectal resections and 1 underwent palliative ileostomy. Simultaneous combined procedures included cholecystectomy (18 cases), appendectomy (17), hysterectomy (8), bilateral salphingoophorectomy (8), liver resection (7), partial vaginectomy (3), small-bowel resection (3), partial cystectomy (2), splenectomy (1), adrenalectomy (1), gastrectomy (1), and total thyroidectomy (1). Application of laparoscopic techniques to colorectal cancer surgery in each period is shown in Table 1 and Fig. 1. The use of laparoscopic surgery increased over the 6- year study, from 2.4% of patients in period I (October 2000 to May 2004), to 19.2% in period II (June 2004 to December 2005), to 66.1% in period III (January to December 2006). Use of the laparoscopic technique for all types of colorectal cancer surgery increased over the three study periods. During period III, 93% of anterior resections, 64% of low anterior or abdominoperineal resections, and 69% of right hemicolectomies were executed using a laparoscopic approach. In period III, 186 (33.9%) underwent open laparotomy (52 far-advanced tumors invading adjacent organs, 43 simultaneous hepatectomies for hepatic metastasis, 37 Table 1 Use of laparoscopic surgery for colorectal cancer in the three study periods Operation Approach Total Period I (n, %) Period II (n, %) Period III (n,%) AR Open (92.3) 148 (65.2) 9 (7.0) Lapa (7.7) 79 (34.8) 120 (93.0) LAR, APR Open 1, (99.4) 336 (85.9) 74 (35.4) Lapa (0.6) 55 (14.1) 135 (64.6) Rt hemi Open (99.1) 131 (82.4) 32 (30.8) Lapa (0.9) 28 (17.6) 72 (69.2) Others Open (100) 124 (89.9) 71 (67.0) Lapa 49 0 (0) 14 (10.1) 35 (33.0) Total Open 2,250 1,325 (97.6) 739 (80.8) 186 (33.9) Lapa (2.4) 176 (19.2) 362 (66.1) AR, anterior resection; LAR, low anterior resection; APR, abdominoperineal resection; Rt hemi, right hemicolectomy; Lapa, laparoscopic; Others: includes left hemicolectomy, Hartmann s procedure, subtotal colectomy, total proctocolectomy, and ileostomy

4 Surg Endosc (2008) 22: Fig. 1 The use of laparoscopic surgery in colorectal cancer. Period I (October 2000 to May 2004): laparoscopic surgery was used only in highly selected early cancer cases (pre-cost trial). Period II (June 2004 to December 2005): laparoscopic surgery was applied more broadly with increase of experiences. Period III (January to December 2006): laparoscopic surgery was the approach of choice. Note that use of laparoscopic surgery for all types of colorectal cancer surgery increased over the study time participated in open surgery arm of randomized trial, 30 obstructive tumors, 14 history of previous laparotomy, 4 intolerant pneumoperitoneum, 3 perforated tumors, 2 refused laparoscopic surgery, and 1 situs inversus). Changes in clinicopathological findings according to each period are shown in Table 2. The patients in each study period were similar in terms of age, sex ratio, BMI, ASA score, and history of abdominal surgery (excluded simple appendectomy). Over the study period, the proportion of patients with rectal cancer and right colon cancer undergoing laparoscopic surgery increased, while the proportion with sigmoid colon cancer decreased (p \ 0.001). The size of tumors became larger (p = 0.008) and more advanced in terms of T-stage and N- stage (p \ 0.001, p = respectively). The mean number of harvested lymph nodes increased over the three study periods (p \ 0.001), and was 25.1 overall. For rectal cancer patients, the mean length of distal resection margins (DRM) and circumferential resection margins (CRM) were 2.5 cm and 12.2 mm, respectively, and did not differ for each study period. Changes in perioperative outcomes of patients according to each period are shown in Table 3. There were three major intraoperative adverse events requiring conversion to open laparotomy: one hemorrhage from the superior mesenteric vein (period II), one hemorrhage from the inferior epigastric artery (period III), and one left ureter injury (period III). For the two intraoperative hemorrhage cases, the bleeding sites were controlled using nonabsorbable stitches after open laparotomy. The overall conversion rate to open laparotomy was 3.5% (20/570), and was similar for each period. Outside of the three major intraoperative events, the causes of conversion were tumor invasion to adjacent structures (12 cases), a narrow pelvis (4 cases), and severe bowel dilatation (1 case). The mean postoperative hospital stay was 9.5 days, and this was affected by postoperative morbidities. Statistical analysis found that the morbidity rates were similar for each period, being 12.5% in period I, 11.4% in period II, and 8.8% in period III (p = 0.570). Postoperative complications occurred in 56 cases. There was one anastomotic leak (period III), which occurred in a patient with rectal cancer, diabetes, and ischemic heart disease, and who was treated with a diverting stoma. Seven complications (1.2%) involved postoperative bleeding, of which two required reoperations, one of which subsequently resulted in postoperative death. The other five postoperative bleeding cases were treated conservatively. There were two mortalities (0.4%) in period II, and no mortalities in period I or III. One was the result of bleeding on postoperative day 9 in a sigmoid colon cancer patient with multiple hepatic metastases. The other was the result of hepatic failure on postoperative day 13 in a rectal cancer patient with multiple hepatic metastases. Minor complications included intestinal obstructions, incisional hernias, anastomotic strictures, urinary dysfunctions, and wound problems. Patients were followed up for a mean 10.3 months (range, 3 62 months). During the follow-up periods, no port-site metastases were observed. Of 570 patients, 528 (528/570, 92.6%) underwent curative intended R0 resection and 7 had recurrences (6 systemic, 1 local). Discussion The present study clearly portrays the radical effects new technology can have on an established surgical practice, in

5 2592 Surg Endosc (2008) 22: Table 2 Clinicopathological findings for each study period Total Period I (10/ /2004) Period II (6/ /2005) Period III (1/ /2006) p-value No. of laparoscopic surgeries Age, years, mean (SD) 59.0 (10.9) 55.9 (10.5) 58.8 (11.3) 59.4 (10.8) Male proportion, n (%) 329 (57.7) 18 (56.3) 105 (59.7) 206 (56.9) BMI, kg/m 2, mean (SD) 23.6 (3.1) 24.0 (3.1) 23.6 (2.9) 23.6 (3.3) ASA score of I II, n (%) 540 (94.7) 31 (96.9) 167 (95.0) 342 (94.5) Previous abdominal surgery, n (%) 46 (8.1) 2 (6.3) 9 (5.1) 35 (9.7) Tumor location, n (%) Ascending 87 (15.3) 1 (3.1) 21 (11.9) 65 (18.0) \0.001 Sigmoid 247 (43.3) 26 (81.3) 96 (54.5) 125 (34.5) Rectum 187 (32.8) 4 (12.5) 45 (25.6) 138 (38.1) Others 49 (8.6) 1 (3.1) 14 (8.0) 34 (9.4) Differentiation, n (%) WD/MD 521 (91.4) 30 (93.8) 159 (90.3) 332 (91.7) PD/mucinous/signet 44 (7.7) 1 (3.1) 15 (8.5) 28 (7.7) Unknown 5 (0.9) 1 (3.1) 2 (1.1) 2 (0.6) T-stage, n (%) T0/Tis/T1/T2 183 (32.1) 25 (78.1) 48 (27.3) 110 (30.4) \0.001 T3/T4 387 (67.9) 7(13.7) 128 (72.7) 252 (69.6) N-stage, n (%) a N0 293 (51.5) 24 (75.0) 81 (46.3) 188 (51.9) N1/N2 276 (48.5) 8 (25.0) 94 (53.7) 174 (48.1) M-stage, n (%) M0 515 (90.4) 32 (100.0) 159 (90.3) 324 (89.5) M1 55 (9.6) 0 (0) 17 (9.7) 38 (10.5) Harvested lymph nodes, mean (SD) 25.1 (13.5) 11.2 (8.0) 24.6 (12.0) 26.5 (13.9) \0.001 Tumor size, cm, mean (SD) 4.2 (2.3) 2.4 (1.3) 4.4 (2.4) 4.3 (2.3) Length of DRM, cm, mean (SD) b 2.5 (1.5) 3.0 (1.7) 2.7 (1.6) 2.4 (1.5) Length of CRM, cm, mean (SD) c 12.2 (11.0) 24.0 (22.6) 13.1 (19.3) 11.7 (7.1) WD, well differentiated; MD, moderately differentiated; PD, poorly differentiated; SD, standard deviation; BMI, body mass index; ASA, American Society of Anesthesiologists score a One patient underwent palliative ileostomy, N-stage not known b Distal resection margin (DRM), data available for all 187 rectal cancer patients c Circumferential resection margin (CRM), data available for 126 rectal cancer patients Table 3 Perioperative outcomes for each study period Total Period I (10/2000 5/2004) Period II (6/ /2005) Period III (1/ /2006) p-value No. of laparoscopic surgeries Operation time, min, mean (SD) (104.2) (94.2) (114.2) (96.2) \0.001 EBL, ml, mean (SD) (175.8) 70.3 (47.3) (115.5) (205.9) Transfusion, n (%) 51 (9.0) 0 (0) 9 (5.2) 42 (11.6) Open conversion, n (%) 20 (3.5) 1 (3.1) 7 (4.0) 12 (3.3) Hospital morbidity, n (%) 56 (9.8) 4 (12.5) 20 (11.4) 32 (8.8) In 30-day mortality, n (%) 2 (0.4) 0 (0) 2 (1.1) 0 (0) Oral intake, days, mean (SD) 3.9 (1.3) 3.7 (0.7) 4.0 (1.1.) 3.9 (1.4) Hospital stay, days, mean (SD) 9.5 (4.8) 8.6 (1.6) 8.8 (3.4) 9.9 (5.5) SD, standard deviation; EBL, estimated blood loss a relatively short period of time. The study population consisted of all types of primary colorectal cancer. It did not exclude low-lying rectal cancer, transverse colon cancer, splenic flexure colon cancer, synchronous colon cancer or locally advanced cancers, which have been excluded in the majority of previous studies, and found that the laparoscopic approach was possible in 66.1% of primary colorectal cancer patients (period III data). It is now

6 Surg Endosc (2008) 22: Table 4 Published outcomes following laparoscopic surgery for colorectal cancers Study Year n Disease EBL (ml) Op. time (min) Conversion (%) No. of LNs BM (days) Hosp stay (days) Morbidity (%) Mortality (%) Braga et al. [4] Colon ca 66% Benign 34% Lacy et al. [5] Colon ca Hasegawa et al. [6] Colon ca 92%; RS colon ca 8% COST [7] Colon ca COLOR [8] Colon ca CLASICC [9] Colon ca 52%; rectal ca 48% Leung et al. [10] RS colon ca Kim et al. [19] Rectal ca Present study Total Colon ca (67%) Rectal ca (33%) EBL: estimated blood loss, Op.: operation, LNs: lymph nodes, BM: bowel movement, Hosp: hospital, ca: cancer, RS: rectosigmoid accepted that the indications for laparoscopic surgery are the same as those for open surgery [13], and that all types of open transabdominal operations on the colon and rectum can now be performed laparoscopically [14]. However, many studies reported on outcomes of laparoscopic colorectal cancer surgery involved cancers confined to one segment of the colon, ultimately making those findings applicable only to patients requiring right- or left-sided colonic resection, or high anterior resection involving not more than one bowel segment [15]. In contrast, the patient population used in the present study indicates that laparoscopic techniques can be used as the surgical approach of choice in many types of colorectal cancer. As a single-institution series, the present study has the advantages of relatively standardized uniform laparoscopic techniques and similar experiences between involving surgeons. The major problems in multicenter trials are difference in surgical techniques among institutions and surgeons experiences. While some major multicenter studies [7 9] only participated surgeons who had performed at least 20 laparoscopic-assisted colorectal operations based on studies examining the learning curve of laparoscopic surgery [16], this number may be underestimated [9, 10], and the difference of laparoscopic techniques was not considered. The differences in techniques and experiences in multicenter trials may affect laparoscopic surgical outcomes including conversion rates, morbidity rates or harvested lymph node yields. These advantages may have resulted in favorable short-term outcomes of the present study. Especially, an anastomotic leak occurred in only 1 of 182 patients undergoing low anterior resection (0.5%); this rate is much lower than those of previous studies ( %) [13, 17, 18]. Although this rate may be associated with the selective fecal diversion with a loop ileostomy (37.4%, 68/182 low anterior resection cases), we thought that the standardized laparoscopic techniques and experience could influence the morbidity. Other perioperative outcomes in the present study are comparable to previous studies (Table 4) [4 10, 19]. Besides standardized technique and experience, selection criteria of laparoscopic surgery could also influence postoperative outcomes including low conversion or complication rates of present study. During period III, we did not provide the laparoscopic approach for patients requiring emergency procedures, those intolerant of a pneumoperitoneum, or those with a history of prior major abdominal surgery or locally far-advanced tumor, as described above. Usually, the laparoscopic surgery for such patients is very difficult, and postoperative outcomes such as conversion or complication rates are eventually not good. Various studies have shown that conversion rate, morbidity, and mortality rates decreased with increasing experience [20, 21]. However, postoperative outcome and conversion rate were similar for the three study periods in present study (Table 3). We did not demonstrate a reduction in the conversion and morbidity rate, and on the contrary, estimated blood loss and number of blood transfusion were increased despite a significant reduction in the operating time. These results, we thought, were caused by the combination of different selection criteria for laparoscopy in each period and experience for this approach. At period I, we the applied laparoscopic approach only to early cancer cases, which were performed laparoscopic surgery without great difficulty. With increasing experience, we applied laparoscopic approach to more advanced

7 2594 Surg Endosc (2008) 22: and complex cases, and the shift was significant (Table 2), thus resulting in an overall stable morbidity and conversion rate. Similar findings were reported by several reports [20, 22]. The long-term results of large multicenter trials indicate that the laparoscopic approach is safe to use in curable colon cancer providing that it is undertaken by experienced surgeons adhering to standard oncological principles [5, 7 9]. Recently, the COST study group reported with 5-year data of the prospective randomized trial that laparoscopic colectomy for curable colon cancer is not inferior to open surgery based on disease-free 5-year survival (open 68.4% versus laparoscopic 69.2%, p = 0.94) and overall 5-year survival (open 74.6% versus laparoscopic 76.4%, p = 0.93) [23]. Since the laparoscopic technique was actively applied in our center only after the COST trial confirmed its oncological safety [7], long-term data from our patients are not yet available. However, for colon cancer, perioperative outcomes in the present study are comparable to previous studies (Table 4); there is no reason to expect long-term oncological outcomes to be inferior. The present study involved four surgeons experienced in both laparoscopy and oncologic colorectal surgery, with one being the first surgeon to perform laparoscopic colon surgery in Korea (J.-G. Park) [24], The pathology findings regarding the number of harvested lymph nodes (mean 25.1) and the status of the proximal and distal margins (no margin tumor involvement in all 382 resected colon cancer cases) were similar to those reported elsewhere. Therefore, despite the lack of long-term data, we believe these findings indicate that our laparoscopic technique for colon cancer results in adequate resection. For rectal cancers, many reports have demonstrated that laparoscopic rectal cancer resection promises oncological safety [17 19, 25 27]. As the first multicenter randomized trial to investigate the oncological long-term results of laparoscopic surgery for rectal cancer, the Conventional versus Laparoscopic-Assisted Surgery in Colorectal Cancer (CLASICC) trial reported that total mesorectal excision was undertaken more frequently in the laparoscopic group, and overall CRM positivity rates did not differ significantly between treatments [9]. They also reported that a nonsignificant difference in CRM positivity in patients undergoing anterior resection (open 6% versus laparoscopy 12%) could be associated with a slightly raised risk of local recurrence [9]. Recently, the CLASICC trial group reported that higher positivity of the CRM after laparoscopic anterior resection (AR) did not translate into a difference in 3-year local recurrence rates (open 7.0% versus laparoscopic 7.8%, p = 0.70) and long-term outcomes for patients with rectal cancer were similar in those undergoing abdominoperineal resection (APR) and AR [28]. Although survival data currently remain the best primary endpoint in many clinical trials, this may be a problematic endpoint due to multiple effective lines of systemic therapy obscuring the impact of study treatment upon survival [29]. In addition, it takes a long time to collect survival data. Recently, an alternative early endpoint of a negative CRM was suggested in rectal cancer surgery [29], and the CLASICC trial has also used this endpoint in its short-term analysis [9]. For adequate CRM, a minimum distance of 1 mm appeared to discriminate between a high and low risk of local recurrence [30]. In the present study, a 1 mm distance was used to define CRM involvement, and 4.3% (8/187 rectal cancer patients) of patients were found to not have a negative CRM. The CRM data were available in 126 rectal cancer patients, and of the remaining 61 with no CRM data, 40 had upper rectal cancer with peritonealization on the carcinoma portion, 13 had no residual cancer on the specimen after endoscopic mucosal resection prior to surgery, and 8 showed no tumor cells after preoperative CRT (complete response). The rate of CRM tumor involvement in the present study (4.3%) was comparable to rates reported in previous laparoscopic (4.2 16%) [9, 19, 31] surgery studies, and appears to be another indicator of the oncological safety of our laparoscopic approach for rectal cancer surgery. Until now, the routine use of the laparoscopic approach for rectal cancer has not yet been justified because of lack of proven oncological safety. In January 2006, we commenced a prospective randomized phase III trial addressing this issue. We intend to compare short- and long-term results of laparoscopic surgery for localized advanced mid or distal rectal cancer treated using preoperative CRT with those of open surgery, and we anticipate interim results will be reported soon. In conclusion, the present study found that it was possible to apply laparoscopic techniques as the surgical approach of choice in two-thirds of primary colorectal cancer patients. While the follow-up period is too short for any long-term conclusions, the basic demographics and short-term favorable outcome data join the existing literature in support of the safety and feasibility of laparoscopic techniques as surgical approach of choice for colon cancer. However, laparoscopic resection for rectal cancer may require a randomized clinical trial prior to gaining similar acceptance. Acknowledgments The authors would like to thank Dr. Woon Kyung Jeong, Dr. Sang-Woo Lim, M.D., Dr. Tae-Sung Chung, and Dr. Dong Hyun Choi for their extensive help and assistance in performing laparoscopic surgeries, and the staff at Center for Colorectal Cancer, National Cancer Center for their patience and assistance throughout this study.

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