Japanese Journal of Clinical Oncology Advance Access published online on June 25, 2009
Japanese Journal of Clinical Oncology, doi:10.1093/jjco/hyp063
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© The Author (2009). Published by Oxford University Press. All rights reserved
Clinical Evidences of Laparoscopic Versus Open Surgery for Colorectal Cancer
Department of Gastroenterological Surgery, Oita University Faculty of Medicine, Oita, Japan
For reprints and all correspondence: Masafumi Inomata, Department of Gastroenterological Surgery, Oita University Faculty of Medicine, 1-1 Idaigaoka, Hasama-machi, Oita 879-5593, Japan. E-mail: inomata{at}med.oita-u.ac.jp
Received February 18, 2009; accepted May 12, 2009
 |
Abstract |
|---|
TOP
Abstract
INTRODUCTIONLaparoscopic surgery has widely spread in the treatment of colorectal cancer. In Japan, a nation-wide survey has shown that a rate of advanced colorectal cancer has increased gradually and reached 65% of the total cases for colorectal cancer in 2007. For colon cancer, many randomized controlled trials regarding short-term outcome demonstrate that laparoscopic surgery is feasible, safe and has many benefits including reduction in a peri-operative mortality. In terms of long-term outcome, four randomized controlled trials insist that there are no differences in both laparoscopic and open surgeries. However, there are still more important issues including long-term oncological outcome for advanced colon cancer, cost effectiveness and the impact on quality of life of patients. Meanwhile, for rectal cancer, a controversy persists with regard to the appropriateness of laparoscopic surgery because of concerns over the safety of the procedure and a necessity of lateral lymph node dissection for lower rectal cancer. In the present, laparoscopic surgery is acceptable for Stage I colon cancer, whereas there are controversies for Stage II/III colon cancer and each staged rectal cancer because of inadequate clinical evidences. Whether laparoscopic surgery further spreads to be applied for colorectal cancer or not, it would be confirmed by Japanese large-scale phase III trial (JCOG0404) estimating oncological outcome for Stage II/III colon cancer and a Phase II trial estimating the feasibility for Stage 0/I rectal cancer in near future.
Key Words: laparoscopic surgery • colorectal cancer • randomized controlled trial • multicenter study
|
INTRODUCTION |
|---|
Recently, colorectal cancer has been a significant leading cause of death from malignancies in Japan as one of the western countries. Surgery is the mainstay of the treatment, with or without chemotherapy and/or radiotherapy. About 90–92% and 84% of patients with cancer of colon and rectum, respectively, are treated surgically (1–3). Conventional open surgery is associated with significant morbidity and long convalescence. Laparoscopic surgery has been widely used as a minimally invasive surgery to treat diverse benign diseases such as benign gall bladder disease (4,5). Jacobs et al. (6) first reported the technical feasibility of laparoscopic colectomy in 1991. Since then, laparoscopic surgery has been widely operated for various benign colorectal conditions such as polyps (7), diverticular disease (8), inflammatory bowel disease (9), rectal prolapse (5) and now colorectal cancer increasingly.
The benefits of laparoscopic surgery in comparison with open surgery have been suggested with respect to decreased morbidity, decreased pain, faster recovery, shorter hospital stay and possibly reduced immunosuppression (10–12). Laparoscopic colorectal surgery is technically complex as it involves laparoscopic mobilization of colon over a wide area, intracorporeal division of major vessels, extraction of specimen and a bowel anastomosis. There is a steep learning curve to achieve advanced laparoscopic skills, and specialized equipment is required (13). There are concerns with oncological outcome and safety of the laparoscopic procedure in colorectal cancer. There are also controversies with potential port site recurrence (14–16) after curative resection of tumor, hospital cost (17) and the lack of data on long-term oncological outcome.
To address these concerns, several prospective randomized clinical trials have been undertaken with longer follow-up time and larger sample size (18–22). In Japan, a retrospective multicenter study was performed to analyze the clinical outcomes for patients with colorectal cancer (23), and a prospective randomized controlled trial (Phase III) for advanced colon cancer (24) and a prospective feasible study (Phase II) for rectal cancer (25) have been conducted.
In this article, we have reviewed clinical studies of laparoscopic surgery versus open surgery for colorectal cancer. We have addressed the important problem whether laparoscopic surgery is acceptable or not for patients with colorectal cancer.
|
NATION-WIDE SURVEY OF LAPAROSCOPIC SURGERY FOR COLORECTAL CANCER IN JAPAN |
|---|
In Japan, laparoscopic surgery for colorectal cancer was introduced in 1992. The Education Committee of Japan Society of Endoscopic Surgery (JSES) conducts a nation-wide survey every 2 years. Until the end of 2007, over 43 000 patients underwent laparoscopic colorectal surgery, and for the year 2007,
9000 operations were carried out in Japan (26). A rate of advanced colorectal cancer has been increased gradually. Particularly, in 2007, 65% of the total cases were advanced cancer (Figure 1).
|
|
RETROSPECTIVE MULTICENTER STUDY OF LAPAROSCOPIC SURGERY FOR COLORECTAL CANCER IN JAPAN |
|---|
A retrospective multicenter study of a large series of patients has been conducted to evaluate long-term results of laparoscopic surgery for colorectal cancer in Japan. The study group comprised 2036 patients undergoing laparoscopic colorectal resection during the period of April 1993–August 2002 in 12 participating surgical units (Japanese Laparoscopic Surgery Study Group). Of the 1495 patients with colon cancer, 781 (59%) had UICC Stage I, 248 (19%) had Stage II and 284 (22%) had Stage III disease. Cancer recurred in 61 (4.1%) of the 1367 curatively treated patients (median follow-up, 32 months; range 6–125 months). The 5-year survival rate was 96.7% for Stage I, 94.8% for Stage II and 79.6% for Stage III disease (Figure 2). Of the 541 patients with rectal cancer, 220 (56%) had Stage I, 62 (16%) had Stage II and 108 (28%) had Stage III disease. Cancer recurred in 30 (5.6%) of the 476 curatively treated patients (median follow-up, 25 months; range 6–102 months). The 5-year survival rate was 95.2% for Stage I, 85.2% for Stage II and 80.8% for Stage III disease. The Japanese data indicate that laparoscopic surgery for colorectal cancer yields an oncological outcome as well as that of conventional open surgery in Japanese Registry (27) for all disease stages.
|
|
CLINICAL EVIDENCES OF LAPAROSCOPIC VERSUS OPEN SURGERY FOR COLON CANCER |
|---|
As searching for all published randomized controlled trials to compare laparoscopic surgery with open surgery for colon cancer, 13 studies were demonstrated in English from 1991 to 2007 (Table 1) (18,19,21,22,28–36). The rate of conversion to open surgery varied widely (0–46.4%) between those studies. There were no significant differences in overall and surgical complication rate, anastomotic leakage rate, re-operation rate and oncological clearance. However, laparoscopic surgery has a significantly lower preoperative mortality, lower wound complications, less blood loss, reduced post-operative pain scores and reduced requirements for narcotic analgesia. After laparoscopic surgery, patients passed flatus earlier and had bowel movement earlier and resumed oral diet sooner than the patients did in open surgery. Prospective randomized controlled trials show that laparoscopic surgery for colon cancer is feasible, safe and has many short-term benefits.
|
Four randomized controlled trials have been reported to clarify long-term outcome of laparoscopic surgery for colon cancer (Table 2) (18–22). These trials were evaluated in the survival, mortality and recurrence of disease associated with two types of surgical procedures with follow-up period of 3.6–5 years. These trials reported an overall mortality rate of 17.9–32% for laparoscopic surgery and 22.2–61% for open surgery. The Clinical Outcomes of Surgical Therapy (COST) Group in USA (19,20), Leung et al. (21) and MRC CLASSICC (22) demonstrated that overall survival rate and the recurrent cancer rate were similar after laparoscopic and open surgery. Only Lacy et al. (18) described significant differences between two surgical methods. In this trial, cancer-related mortality was lower in patients with Stage III disease who underwent LCR, and no significant differences were found with respect to patients with Stage I and II disease. Reza et al. (37) reported that meta-analysis of four randomized controlled trials had not revealed any significant difference in terms of cancer-related mortality and recurrence rates between laparoscopic and open surgery. Transatlantic laparoscopically assisted versus open-colectomy trials study group also reported that meta-analysis demonstrated no significant difference in terms of long-term survival between both surgical procedures (38). Prospective randomized controlled trials and meta-analysis in terms of long-term outcome states that there are no differences in the two surgical procedures. However, these randomized controlled trials in western countries also have several problems such as the criteria including early staged cancer and benign disease, undetermined level of lymph node dissection, unclear indication for adjuvant chemoradiotherapy and no description of quality control of the two surgical procedures.
|
|
CLINICAL EVIDENCES OF LAPAROSCOPIC VERSUS OPEN SURGERY FOR RECTAL CANCER |
|---|
The results of multicenter randomized controlled trial to evaluate laparoscopic versus open surgery for rectal cancer have seldom been reported either in Japan or any other foreign countries, yet there is a report to present the fact that there is no significant difference between laparoscopic and open surgery in oncological short-term prognosis (22). There are not many reports regarding prognosis of laparoscopic surgery for advanced rectal cancer. However, there are some reports that an incidence of complications such as anastomotic leakage and pelvic abscess in laparoscopic surgery is the same as, or higher than that in open surgery (39–42). In 2007, CLASICC trial group targeted 794 patients with colon and rectal cancer in multicenter randomized clinical trial of laparoscopic versus open surgery (22). There was no significant difference in 3-years' local recurrence and overall survival rates after curative resection between both the groups. Though there was 5% in mortality rate in each group, a positive rate of circumferential resection margin in laparoscopic group was higher than that in open group. Short-term results of laparoscopic surgery for rectal cancer were shown in Table 3 (43–47). In retrospective studies, tumors were located at 0–15 cm away from the anal verge, and a conversion rate to open surgery was 3–12%. A rate of postoperative complications was 21–36%, and a rate of anastomotic leakage was 5.8–17.3%. In these reports from western countries, pre- or post-operative chemoradiotherapy was treated for 40% of patients with T3 or deeper rectal cancer. Because a standard treatment for advanced rectal cancer is different from the one in Japan, further detailed study would surely be required about the adaptation of laparoscopic surgery.
|
|
A PROSPECTIVE RANDOMIZED CONTROLLED TRIAL FOR COLON CANCER IN JAPAN |
|---|
In Japan, we have conducted a randomized controlled trial to compare laparoscopic surgery with open surgery to evaluate oncological outcome for advanced colon and recto-sigmoid cancer (24). This study has been supported in part by a Grant-in-Aid for Cancer Research from the Japanese Ministry of Health, Labor and Welfare. The Clinical Trial Review Committee of the Japan Clinical Oncology Group (JCOG) approved the protocol in September 2004, and the study (JCOG0404) has started in November 2004 to elucidate the optimal treatment for T3 or deeper colorectal cancer. Surgeons at 27 specialized institutions will recruit 1050 patients. The primary endpoint is the overall survival rate. Secondary endpoints are relapse-free survival rate, short-term clinical outcomes, adverse events and a rate of conversion from laparoscopic surgery to open surgery. The short-term clinical outcomes are the proportion of the use of analgesics, the duration from operation to flatus, the highest body temperature during hospitalization and the highest body temperature during 3 days after operation. In both arms, resection of colon or rectum with D3 lymphadenectomy is performed according to the Japanese Classification of Colorectal Carcinoma (48). The patients are randomized by the minimization method of balancing the groups according to the location of the tumor and the institution (Figure 3). This Japanese randomized controlled trial has characteristic designs comparing with other western trials such as inclusion criteria of only advanced cancer (T3, T4), lymph node dissection, adjuvant chemotherapy and the quality control. In the case of pathological Stage III colorectal carcinoma, three cycles of adjuvant chemotherapy with fluorouracil and L-leucovorin are administered. To control the quality of operation, central review of surgical procedure was done by using photographs of all patients. A registration of the patients in this trial will be accomplished in March 2009.
|
|
A PROSPECTIVE STUDY FOR RECTAL CANCER IN JAPAN |
|---|
To examine technical and oncological feasibility of laparoscopic surgery for rectal cancer, a Phase II trial (Lap-RC) started to be applied to patients with a preoperative diagnosis of Stage 0/I rectal cancer under the direction of the Japan Society of Laparoscopic Colorectal Surgery (26). Surgeons at 39 specialized institutions will recruit 350 patients. The primary endpoint at the first stage is an anastomotic leakage rate by double-stapling technique and the one at the second stage is an overall survival rate. Secondary endpoints are relapse-free survival rate, short-term clinical outcome, adverse events, the rate of histologically curative operation, the proportion of completion of laparoscopic and the conversion rate. To control the quality of operation, central review of surgical procedure was done by using photographs of all patients.
|
CONCLUSIONS AND PERSPECTIVES |
|---|
Laparoscopic surgery has widely spread as a less invasive procedure for colorectal cancer in Japan and western countries. A nation-wide survey by JSES revealed that a rate of advanced colorectal cancer has increased gradually and reached two-thirds of total cases in 2007. Many randomized controlled trials demonstrate that laparoscopic surgery for colon cancer is feasible, safe and has many short-term benefits including reduction in peri-operative mortality. There are still more important issues including long-term oncological outcome for advanced colon cancer, cost-effectiveness and the impact on quality of life of patients with colon cancer. Meanwhile, a controversy persists with regard to the appropriateness of laparoscopic surgery for patients with rectal cancer because of concerns over the safety of the procedure, especially in low anterior resections for lower rectal carcinoma. Additionally, lateral lymph node dissection combined with total mesorectal excision remains the standard surgical procedure for patients with advanced lower rectal carcinoma in Japan, but lateral lymph node dissection by laparoscopic surgery is still an unexplored frontier (49–51). In the presence, laparoscopic surgery is acceptable for Stage I disease of colon cancer, also it is generally not acceptable for Stage II/III colon cancer and each staged rectal cancer. However, experienced and trained surgeons may do laparoscopic surgery for Stage II/III colon cancer and early staged rectal cancer with accepting the informed consent from patients because clinical outcomes of laparoscopic surgery are equivalent or superior to open surgery in previous clinical trial reports. Further works are needed to estimate laparoscopic procedures for advancer colon and rectal cancer. Japanese on-going large-scale RCT (JCOG0404) estimating oncological outcome for Stage II/III colon cancer (24) and a prospective feasible study for Stage 0/I rectal cancer (25) would be beneficial to determine the role of laparoscopic surgery as a standard operation for colorectal cancer. General surgeons expect the report of clinical results of Japanese two trials to come out as soon as possible.
|
Funding |
|---|
Health and Labour Sciences Research Grants for Clinical Cancer Research, from the Ministry of Health, Labour and Welfare, Japan.
|
Conflict of interest statement |
|---|
None declared.
|
Acknowledgements |
|---|
We thank Miss Midori Kono for linguistic assistance.
|
References |
|---|
1 Jessup JM, McGinnis LS, Steele GD Jr, Menck HR, Winchester DP. The National Cancer Data Base, report on colon cancer. Cancer (1996) 78:918–26.[CrossRef][Web of Science][Medline]
2 Ota DM. Colon cancer. Cancer Treat Res (1997) 90:347–56.[Medline]
3 Bokey EL, Chapuis PH, Dent OF, Newland RC, Koorey SG, Zelas PJ, et al. Factors affecting survival after excision of the rectum for cancer; a multivariate analysis. Dis Colon Rectum (1997) 40:3–10.[CrossRef][Web of Science][Medline]
4 Anonymous. Gallstones and laparoscopic cholecystectomy. NIH Consensus Development Panel on Gallstones and Laparoscopic Cholecystectomy. Surg Endosc (1993) 7:271–9.[CrossRef][Web of Science][Medline]
5 Tomita H, Marcelo PW, Milsom JW. Laparoscopic surgery of the colon and rectum. World J Surg (1999) 23:397–405.[CrossRef][Web of Science][Medline]
6 Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc (1991) 1:144–50.[Medline]
7 Joo JS, Amarnath L, Wexner SD. Is laparoscopic resection of colorectal polyps beneficial? Surg Endosc (1998) 12:1341–4.[CrossRef][Web of Science][Medline]
8 Liberman MA, Phillips FH, Carroll BJ, Fallas M, Rosenthal R. Laparoscopic colectomy vs traditional colectomy for diverticulitis. Surg Endosc (1996) 10:15–8.[CrossRef][Web of Science][Medline]
9 Young-Fadok TM, Hall LK, McConnell EJ, Gomez Rey G, Cabanela RL. Advantages of laparoscopic resection for ileocolic Crohn's disease. Surg Endosc (2001) 15:450–4.[CrossRef][Web of Science][Medline]
10 Lacy A. Colon cancer; laparoscopic resection. Ann Oncol (2005) 16:88–92.
11 Curet MJ. Laparoscopic-assisted resection of colorectal carcinoma. Lancet (2005) 365:1666–8.[CrossRef][Web of Science][Medline]
12 Motson RW. Laparoscopic surgery for colorectal cancer. Br J Surg (2005) 92:519–20.[CrossRef][Web of Science][Medline]
13 Tekkis PP, Senagore AJ, Delaney CP, Fazio VW. Evaluation of the learning curve in laparoscopic colorectal surgery: comparison right-sided left-sided resections. Ann Surg (2005) 242:83–91.[CrossRef][Web of Science][Medline]
14 Stocchi L, Nelson H. Wound recurrences following laparoscopic-assisted colectomy. Arch Surg (2000) 135:948–58.
15 Tseng LN, Berends FJ, Wittich P, Bouvy ND, Marquet RL, Kazemier G, et al. Port site metastases: impact of local tissue trauma and gas leakage. Surg Endosc (1998) 12:1377–80.[CrossRef][Web of Science][Medline]
16 Lacy AM, Delgado S, Garcia-Valdecasas JC, Castells A, Piqué JM, Grande L, et al. Port site metastases and recurrence after laparoscopic colectomy. A randomized trial. Surg Endosc (1998) 12:1039–42.[CrossRef][Web of Science][Medline]
17 Philipson BM, Bokey EL, Moore JW, Chapuis PH, Bagge E. Cost of open versus laparoscopically assisted right hemicolectomy for cancer. World J Endosc (1998) 12:1039–42.
18 Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer; a randomized trial. Lancet (2002) 359:2224–9.[CrossRef][Web of Science][Medline]
19 The Clinical Outcomes of Surgical Therapy (COST) Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med (2004) 350:2050–9.
20 Fleshman J, Sargent DJ, Green E, for The Clinical Outcomes of Surgical Therapy Study Group. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg (2007) 246:655–62.[CrossRef][Web of Science][Medline]
21 Leung KL, Kwok SP, Lam SC, Lee JF, Yiu RY, Ng SS, et al. Laparoscopic resection of rectosigmoid carcinoma: prospective randomized trial. Lancet (2004) 363:1187–92.[CrossRef][Web of Science][Medline]
22 Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AM, et al, UK MRC CLASICC Trial Group. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol (2007) 25:3061–8.
23 Kitano S, Kitajima M, Konishi F, Kondo H, Satomi S, Shimizu N, Japanese Laparoscopic Surgery Study Group. A multicenter study on laparoscopic surgery for colorectal cancer in Japan. Surg Endosc (2006) 20:1348–52.[CrossRef][Web of Science][Medline]
24 Kitano S, Inomata M, Sato A, Yoshimura K, Moriya Y, Japan Clinical Oncology Group Study. Randomized controlled trial to evaluate laparoscopic surgery for colorectal cancer: Japan Clinical Oncology Group Study JCOG 0404. Jpn J Clin Oncol (2005) 35:475–7.
25 Seiichiro Y, Kenichi Y, Fumio K, Masahiko W. Phase II trial to evaluate laparoscopic surgery for Stage 0/I rectal carcinoma. Jpn J Clin Oncol (2008) 38:497–500.
26 The Education Committee of Japan Society of Endoscopic Surgery. 8th Nationwide Survey of Endoscopic Surgery in Japan. J Jpn Soc Endosc Surg (2006) 5:527–628.
27 Multi-Institutional Registry of Large Bowel Cancer in Japan, Cases Treated in 1994. (2002) Vol. 23. Tokyo, Japan: Japanese Society for Cancer of the Colon and Rectum.
28 Hasegawa H, Kabeshima Y, Watanabe M, Yamamoto S, Kitajima M. Randomized controlled trial of laparoscopic versus open colectomy for advanced colorectal cancer. Surg Endosc (2003) 17:636–40.[CrossRef][Web of Science][Medline]
29 Hewitt PM, Ip SM, Kwok SP, Somers SS, Li K, Leung KL, et al. Laparoscopic-assisted vs. open surgery for colorectal cancer: comparative study of immune effects. Dis Colon Rectum (1998) 41:901–34.[CrossRef][Web of Science][Medline]
30 Milsom JW, Bohm B, Hammerhofer KA, Fazio V, Steiger E, Elson P. A prospective, randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: a preliminary report. J Am Coll Surg (1998) 187:46–55.[CrossRef][Web of Science][Medline]
31 Schwenk W, Jacobi C, Mansmann U, Böhm B, Müller JM. Inflammatory response after laparoscopic and conventional colorectal resections-results of a prospective randomized trial. Langenbecks Arch Surg (2000) 385:2–9.[CrossRef][Web of Science][Medline]
32 Curet MJ, Putrakul K, Pitcher DE, Josloff RK, Zucker KA. Laparoscopically assisted colon resection for colon carcinoma: perioperative results and long-term outcome. Surg Endosc (2000) 14:1062–6.[CrossRef][Web of Science][Medline]
33 Braga M, Vignali A, Zuliani W, Radaelli G, Gianotti L, Martani C, et al. Metabolic and functional results after laparoscopic colorectal surgery: a randomized, controlled trial. Dis Colon Rectum (2002) 45:1070–7.[CrossRef][Web of Science][Medline]
34 Kaiser AM, Kang JC, Chan LS, Vukasin P, Beart RW Jr. Laparoscopy-assisted vs open colectomy for colon cancer: a prospective randomized trial. J Laparoendosc Adv Surg Tech A (2004) 14:329–34.[Web of Science][Medline]
35 The COLOR Study Group. Laparoscopic surgery versus open surgery for colon cancer: short term outcomes of a randomized trial. Lancet Oncol (2005) 6:477–84.[CrossRef][Web of Science][Medline]
36 Liang JT, Huang KC, Lai HS, Lee PH, Jeng YM. Oncologic results of laparoscopic versus conventional open surgery for stage II or III left-sided colon cancers: a randomized controlled trial. Ann Surg Oncol (2007) 14:109–17.[CrossRef][Web of Science][Medline]
37 Reza MM, Blasco JA, Andradas E, Cantero R, Mayol J. Systematic review of laparoscopic versus open surgery for colorectal cancer. Br J Surg (2006) 93:921–8.[CrossRef][Web of Science][Medline]
38 Bonjer HJ, Hop WC, Nelson H, Sargent DJ, Lacy AM, Castells A, et al. Laparoscopically assisted vs open colectomy for colon cancer: a meta-analysis. Arch Surg (2007) 142:298–303.
39 Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, et al, MRC CLASICC trial group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicenter randomized controlled trial. Lancet (2005) 365:1718–26.[CrossRef][Web of Science][Medline]
40 Moloo H, Mamazza J, Poulin EC, Burpee SE, Bendavid Y, Klein L, et al. Laparoscopic resections for colorectal cancer: does conversion affect survival? Surg Endosc (2004) 18:732–5.[Web of Science][Medline]
41 Thorpe H, Jayne DG, Guillou PJ, Quirke P, Copeland J, Brown JM, MRC CLASICC Trial Group. Patient factors influencing conversion from laparoscopically assisted to open surgery for colorectal cancer. Br J Surg (2008) 95:199–205.[CrossRef][Web of Science][Medline]
42 Laurent C, Leblanc F, Gineste C, Saric J, Rullier E. Laparoscopic approach in surgical treatment of rectal cancer. Br J Surg (2007) 94:1555–61.[CrossRef][Web of Science][Medline]
43 Morino M, Parini U, Giraudo G, Salval M, Brachet CR, Garrone C. Laparoscopic total mesorectal excision. A consecutive series of 100 patients. Ann Surg (2003) 237:335–42.[CrossRef][Web of Science][Medline]
44 Zhou ZG, Hu M, Li Y, Lei WZ, Yu YY, Cheng Z, et al. Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc (2004) 18:1211–5.[CrossRef][Web of Science][Medline]
45 Leroy J, Jamail F, Forbes L, Smith M, Rubino F, Mutter D, et al. Laparoscopic total mesorectal excision (TME) for rectal cancer surgery: long-term outcomes. Surg Endosc (2004) 18:281–9.[CrossRef][Web of Science][Medline]
46 Dulucq JL, Wintringer P, Stabilini C, Mahajna A. Laparoscopic rectal resection with anal spincter preservation for rectal Cancer. Surg Endosc (2005) 19:1468–74.[CrossRef][Web of Science][Medline]
47 Kim SH, Park IJ, Joh YG, Hahn KY. Laparoscopic resection for rectal cancer: a prospective analysis of thirty-month follow-up outcomes in 312 Patients. Surg Endosc (2006) 20:1197–202.[CrossRef][Web of Science][Medline]
48 Japanese Society for Cancer of the Colon and Rectum. General Rules for Clinical and Pathological Studies on Cancer of the Colon, Rectum and Anus. (2006) 7th edn. in Japanese.
49 Moriya Y, Sugihara K, Akasu T, Fujita S. Importance of extended lymphadenectomy with lateral node dissection for advanced lower rectal cancer. World J Surg (1997) 21:728–32.[CrossRef][Web of Science][Medline]
50 Fujita S, Yamamoto S, Akasu T, Moriya Y. Lateral pelvic lymph node dissection for advanced lower rectal cancer. Br J Surg (2003) 90:1580–5.[CrossRef][Web of Science][Medline]
51 Yamamoto S, Watanabe M, Hasegawa H, Kitajima M. Prospective evaluation of laparoscopic surgery for rectosigmoidal and rectal carcinoma. Dis Colon Rectum (2002) 45:1648–54.[CrossRef][Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||