Standards for Local Recurrence Rates in Both Open and Laparoscopic Rectal Cancer Surgery. How do you Measure Up?

Jennifer Liang and James M Church^*

Department of Colorectal Surgery, Digestive Diseases Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, Ohio, USA

*Corresponding Author:

James M Church
Department of Colorectal Surgery
Digestive Diseases Institute
Cleveland Clinic Foundation
9500 Euclid Ave, Cleveland, Ohio, USA
Tel: 216 444 9053
Fax: 216 445 8627
E- mail: churchj@ccf.org

Received date: July 3, 2014; Accepted date: February 25, 2015; Published date: March 4, 2015

Citation: Liang J, Church JM (2015) Standards for Local Recurrence Rates in Both Open and Laparoscopic Rectal Cancer Surgery. How do you Measure Up?. J Gastrointest Dig Syst 5:260. doi:10.4172/2161-069X.1000260

Copyright: © 2015 Liang J, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Visit for more related articles at Journal of Gastrointestinal & Digestive System

Abstract

Local recurrence of rectal cancer is the result either of potentially removable tumor cells left in situ or cells already disseminated to areas where surgery cannot reach them. The first scenario infers inadequate surgery, the second implies unfavorable biology. Surgeons who operate for rectal cancer must know local recurrence rates in their patients, and be able to relate them to outcomes achieved by others. We have performed this study to facilitate such a comparison. Methods: Systematic review of the literature from 1990 to 2010 was performed for publications which reported local recurrence after proctectomy for rectal cancer. Inclusion criteria were: studies of more than 80 patients and local recurrence stratified by histopathologic stage. Pooled local recurrence rates were tabulated by 5 percentile levels, stratified according to TNM stage (I,II,III) and surgical technique (total mesorectal excision or standard), as well as laparoscopic versus open. Results: Thirty-six studies comprising 16425 patients were pooled for final analysis: Mean follow-up is 40.9 months (1.3-188mths). The table shows local recurrence stratified by tumor biology (stage), operative technique (total mesorectal excision vs. standard) and operative approach (open vs. laparoscopic). The percentiles provide standards against which surgeons can compare their own outcomes Conclusion: Oncologic outcome of the treatment of rectal cancer is the result of interaction of therapeutic expertise and tumor biology. The percentile tables allow the use of local recurrence rates as an indirect parameter of surgical quality.

Abstract

Local recurrence of rectal cancer is the result either of potentially removable tumor cells left in situ or cells already disseminated to areas where surgery cannot reach them. The first scenario infers inadequate surgery, the second implies unfavorable biology. Surgeons who operate for rectal cancer must know local recurrence rates in their patients, and be able to relate them to outcomes achieved by others. We have performed this study to facilitate such a comparison.

Methods: Systematic review of the literature from 1990 to 2010 was performed for publications which reported local recurrence after proctectomy for rectal cancer. Inclusion criteria were: studies of more than 80 patients and local recurrence stratified by histopathologic stage. Pooled local recurrence rates were tabulated by 5 percentile levels, stratified according to TNM stage (I,II,III) and surgical technique (total mesorectal excision or standard), as well as laparoscopic versus open.

Results: Thirty-six studies comprising 16425 patients were pooled for final analysis: Mean follow-up is 40.9 months (1.3-188mths). The table shows local recurrence stratified by tumor biology (stage), operative technique (total mesorectal excision vs. standard) and operative approach (open vs. laparoscopic). The percentiles provide standards against which surgeons can compare their own outcomes

Conclusion: Oncologic outcome of the treatment of rectal cancer is the result of interaction of therapeutic expertise and tumor biology. The percentile tables allow the use of local recurrence rates as an indirect parameter of surgical quality.

Keywords

Laparoscopic surgery

Introduction

Excellent surgical technique is of particular relevance in the treatment of rectal cancers where clinicians have the greatest impact on the survival outcomes. Cancer recurrence, viewed simply, can be the result of either potentially removable tumour cells that are left in situ at time of surgery or these cells have already disseminated to areas where even the best surgery cannot reach them. The first scenario infers that surgery has been inadequate; the second that biology is unfavorable. The first scenario is likely to lead to potentially resectable local recurrence while the later will lead to unresectable local recurrence unless prevented by appropriate neo adjuvant or adjuvant therapy. The oncologic outcome of treatment of low rectal cancer is therefore the result of the interaction of therapeutic expertise and tumor biology. If treatment is good and biology is good, the result should be a cure. If treatment is good but biology is aggressive, there will be local recurrence but also distant recurrence as cells escape surgery, radiation and chemotherapy. If treatment of good biology tumors is inadequate there will be local recurrence but minimal distant spread. If there is inadequate treatment of aggressive tumors the outcome will be disastrous; high rates of local and distant recurrence with patients dying a terrible death. Fulfilling this responsibility involves knowing the local and distant recurrence rates in their patients, and being able to relate them to outcomes achieved by others. We have performed this study to facilitate such a comparison.

Methods

A systematic review of the literature using MEDLINE and pubmed databases was performed for original papers published between 1990 to 2010 reporting results of local recurrence from rectal cancer surgery. The aim was not to achieve a complete coverage of all the literature but to provide a pool of local recurrence data from large series. Two main inclusion criteria were: studies of more than 80 patients and that local recurrence from these studies had to be stratified into histopathological stages which paralleled tumour’s aggressiveness. Different staging systems were aggregated according to the AJCC Classification system (Table 1).

Table1: Comparison of TNM, AJCC, Dukes, and Astler-Coller Stages.

Surgical techniques were divided into total mesorectal excision (TME) or standard resection (STD) based on the authors’ descriptions. The use of neo-adjuvant or adjuvant therapy was considered to be part of surgical decision making and there for not an inclusion or exclusion criteria. Relevant articles were reviewed and the extracted data include: author, year of publication, study design, number of patients, surgical procedure, laparoscopic or open, length of follow-up, overall LR and DR as well as LR and DR by TNM stage (Table 2).

Table 2: Determinants of oncologic outcome of rectal cancer surgery.

Results

Data from 38 studies comprising of 16425 patients were pooled for final analysis. Twenty-eight were open surgeries only, eight were laparoscopic studies only and two studies included both. 28 retrospective, 7 prospective and 3 randomised controlled trials. The overall laparoscopy conversion rate was 7.5%. Mean follow-up is 40.89 months (1.3-188mths): 58 months (24-120mths) for open surgery and 39 months (26-57mths) for laparoscopic surgery. Type of surgery was described in all of the studies apart from one (72% AR, 33% APR and 2% others) and only 14 studies specified the tumour grade (85% well differentiated and 15% poorly differentiated) (Table 3).

Table 3: Overall local recurrence for lap and open by AJCC Stage.

The data were tabulated in order of LR and stratified by AJCC stage (I-III), surgical technique (Table 4) as well as laparoscopic versus open (Table 5). Percentiles were derived. Stage IV was eliminated from the analysis secondary to paucity of data. Local recurrence rates were then distributed in five percentiles: P10, P25, P50, P75 and P90. This allowed us to develop a simple reference table using LR as an indirect parameter of surgical quality, graded as excellent, very good, good, fair and poor according to each percentile. The 10th percentile represents the top 10% with excellent results and the 90th percentile is the bottom 10% with the poorest surgical results.

Table 4: Local Recurrence for Lap and Open by AJCC Stage and Technique.

Table 5: Local recurrence by surgical approach and AJCC stage.

The overall pooled recurrence rate is 11.3% for stage I to III (range 2-35%) and overall distant recurrence rate is 19.5% (range 8.1-39.3%). The median overall LR for stage I was 2.4% (IQ 0-10%), 9% (IQ 4.1-16.6%) for stage II and 16.1% (IQ10-24.1%) for stage III rectal cancers. For open surgeries, 7583 patients had TME while 7129 patients had standard resection. TME was associated with lower LR for all cancer stages when compared to the STD surgical technique. There is a significant more patients in the open group when compared to the laparoscopic group (14172 patients vs 1713 patients, respectively. While open approach seemed to be associated with higher LR in comparison with laparoscopic surgery at all TNM stage, bear in mind that the open group comprises both TME and STD resection while all patients in the laparoscopic group had TME.

Discussion

The oncologic outcome is of the utmost importance following rectal cancer surgery, whilst the determinants of local recurrence are multi-factorial they are closely associated with tumour biology and surgical technique. Local recurrence is seldom curable and carries poor prognosis, it also produces incapacitating symptoms which are difficult to palliate [1-6]. Numerous approaches have been used in an attempt to reduce local recurrence rate such as total mesorectal excision (TME) [7], total pelvic lymphadenectomy [8,9], rectal stump irrigation with cytocidal agents, pre and post-operative radiotherapy and adjuvant chemotherapy [10-12]. However, technical ability alone is not the only factor in improving outcome, other components such as knowledge, judgment, training and volume are also crucial. In a multivariate analysis of surgeon-related factors and their effect on the outcomes in rectal cancer, Porter et al. has demonstrated that the risk of local recurrence is lessened with subspecialty training and higher volume of operations performed. Non-colorectal surgeons had a higher local recurrence rate (hazard ratio 2.49, 95% CI 1.43-4.33,p<0.001) and significantly higher risk for local recurrence is demonstrated in surgeons who performed less than 21 resections (hazard ratio 1.80, 95% CI 1.36-2.40, p<0.001) [13].

There is a shift in paradigm in rectal surgery in the last century, abdominoperineal resection, once the gold standard, is now regarded as unnecessary in most patients. The anatomico-pathological studies have showed that the majority of lymph nodes are found parallel to or proximal to the level of primary rectal tumour [14] and distal margins of 2 cm does not compromise survival or local control [15]. The allowance of a close distal margin has led to an increase incidence of sphincter-saving surgery. This has been reflected in our 38 pooled studies where anterior resection is performed at a higher frequency when compared to abdominoperineal resection (72% vs 33% respectively).

Conventional rectal mobilization in either APR or AR by blunt dissection is associated with a high local recurrence. To highlight the importance of surgeon as an independent prognostic factor, the introduction of total mesorectal excision (TME) by Heald in 1982 have significantly reduced the local recurrence rate from approximately 12-20% to 4% [7,16]. Our results have also confirmed such findings, lower local recurrence rates have been seen universally across all AJCC stages when TME is performed. Furthermore, mesorectal excision has been translated into an improvement in overall survival [7,17-19]. Assessment of the quality of TME is done by determining the involvement of tumour at the radial/circumferential margin and distal margin.

The concept of TME involves sharp dissection in the avascular mesorectal plane to keep the visceral layer of the pelvic fascia intact, theoratically it should reduce blood loss and specimen should contain all potential routes of metastatic tumour spread. Deviation from the principle may lead to incomplete TME and may jeopardize oncologic outcome. Moreover, recent studies have suggested TME can be modified according to the tumor distance from the anal verge. For upper rectal cancer, partial mesorectal excision does not compromise oncologic outcomes. However, for middle and low rectal cancer, the complete excision of the mesorectum is deemed necessary [20-24].

In the early development phase of laparoscopic surgery for colorectal cancer, serious concerns are raised regarding the adequacy of oncologic clearance and a high port site recurrence rate of 21% [25]. These concerns have been addressed by results of major comparative studies and randomized controlled trials that have reported no difference in resection margin, lymph node collection, tumor recurrence, and mid- to long-term survival between the open and laparoscopic approach [26]. Port site recurrence is now found to be 2.4% for laparoscopic colorectal cancer cases with 5 years follow up [27] and 1.3% in a more recent randomized controlled trial [28]. Published data from Cochrane review [29], showed there is no difference in recurrence at the site of the primary cancer 7.2% vs 7.7%; OR (fixed) 0.81 (95% CI 0.45 to 1.43) (P = 0.46). Similar cancer-related mortality was found after laparoscopic surgery compared to open surgery, 9.2% vs 10.0%; OR (fixed) 0.66 (95% CI 0.37 to 1.19) (P=0.16). However, Laurent et al. has shown a better 5-year survival in the laparoscopic group, the exact mechanism remains unknown but the author has suggested that mediators of immunologic response (TNF alpha, IL1-6, CRP) are decreased after laparoscopic surgery leading to less immunosuppression in the post operative period [30]. Another possible reason is better exposure and hence better surgery. During laparoscopic surgery, the positive pressure of the pneumoperitoneum can open up the alveolar plane that separates the parietal and visceral fascia of the mesorectum. The optics of laparoscopy provides a clear and magnified view of the pelvis to facilitates sharp TME and identification of important pelvis structures, including blood vessels, pelvic nerves, seminal vesicles, or the posterior vaginal wall.

In contrast to Laurent et al. [30], our data suggested similar local recurrence rates was seen between the laparoscopic TME group when compared to open TME group, this is however limited by a much smaller numbers of patients in the laparoscopic group and a shorter follow-up. Laparoscopic technique is a relatively new entity, the length of follow-up may not be adequate to detect all local recurrences yet.

Tumor biology strongly correlates to tumor stage. The widely used AJCC staging system is a reliable prognostic indicator and lymph node metastasis is an independent risk factor for recurrence and survival in rectal cancer patients [31]. For correct nodal staging, postoperative specimens must be examined thoroughly, and an adequate number of lymph nodes must be obtained. Experts now recommends the use of at least 12 lymph nodes for diagnosis of node-negative disease in colorectal cancer [32-35]. An insufficient number of retrieved nodes from a TME specimen can cause understaging of nodal status which can affect the use of adjuvant therapy.

Incomplete resection, local spillage of tumor cells or just bad technique may compromise the chance of local control of the rectal tumor. Salvage surgery represents a difficult clinical problem and the success rates are not very encouraging, but approximately 30% of patients may benefit from the procedure [36]. Recently Boyle et al. reports that 51% of patients whom has had a potentially curative excision of the local recurrence does not develop a second recurrence during the follow up period. This can be used as an indirect evidence that in approximately half of the patients local failure is related to the primary surgical treatment itself. In the other half, tumor biology is an important prognostic factor that no matter how skilful the surgeon is, it is impossible to eliminate all microscopic spread and local recurrence is inevitable [37].

Under these circumstances, the use neo adjuvant or adjuvant therapy may be more of use to eliminate the microscopic disease. For clinical T3 or T4 or node-positive disease, preoperative chemoradiotherapy is superior to postoperative chemoradiotherapy in reducing local recurrence rates and enhancing anal sphincter preservation. However, chemotherapy is expensive and can cause significant morbidity such as haemorrhagic proctitis, cystitis, radiation enteritis with fistula and tenesmus and severe dermatitis. Kuster et al. [38] has randomized 713 patients into RT+ TME and 704 into TME alone. The overall 5-year local recurrence is 4.6% in the RT+TME group and 11% in the TME group. Knowing one’s own local recurrence rate for various AJCC stage is of particular importance here, because if local recurrence rate of 10% or less can be achieved with surgery alone, pre-operative radiotherapy or adjuvant chemotherapy may not greatly extend eventual outcome. On the other hand, if such result is not consistently achievable, the judicious use of neo-adjuvant and adjuvant therapy lies with the surgeon’s own knowledge of their limitation.

Finally we would like to acknowledge the lack of methodological uniformity and the variability in the definition of curative surgery and local recurrence among rectal cancer studies, which may play a role of the wide variation of local recurrence rates present in the literature. The diversity in patients’ inclusion/exclusion criteria with possible patient or tumor selection bias, and different protocols for the selection of patients for neo or adjuvant therapy may also influences our results. The intention of this study was not to address methodological issues in reporting local recurrence rates but the aim is to provide standards of acceptable rates that one should aim for. However, since these rates are from large series therefore results may not be achievable in lower volume cetres.

Apart from local recurrence rates, other parameters of good surgery such as anastomotic leak rates, urinary bladder and sexual dysfunction need to be addressed. Despite serious efforts to preserve nerves during open TME approximately, prospective study has demonstrated that 10% of patients continued to have bladder dysfunction beyond 6 months and 30% of the preoperatively potent men had sexual dysfunction postoperatively [39].

Before trying to set new standards for local control in rectal cancer it is important to have in mind that the goal of every surgeon is to overcome the tumor biology and surgical technical issues to achieve the lowest local recurrence possible. Therefore, the 10% benchmark for local recurrence, commonly used today, seems to underestimate our capacity to achieve better results especially in early stage rectal cancer. With the use of the reference table we challenge that surgeons to push their limits and strive to achieve LR rates at least in the lower 50th percentile (Table 6).

Table 6: Design of laparoscopic operations.

Conclusion

Oncologic outcome of the treatment of rectal cancer is the result of interaction of therapeutic expertise and tumor biology. The percentile tables allow the use of local recurrence rates as an indirect parameter of surgical quality (Table 6).

References

1. Kirwan WO, O'Riordain MG, Waldron R (1989) Declining indications for abdominoperineal resection. Br J Surg 76: 1061-1063.
2. Williams NS1 (1989) Changing patterns in the treatment of rectal cancer. Br J Surg 76: 5-6.
3. Balslev I, Pedersen M, Teglbjaerg PS, Hanberg-Soerensen F, Bone J, et al. (1986)Postoperative radiotherapy in Dukes' B and C carcinoma of the rectum and rectosigmoid. A randomized multicenter study. Cancer 58:22-28.
4. Gunderson LL, Sosin H (1974) Areas of failure found at reoperation (second or symptomatic look) following "curative surgery" for adenocarcinoma of the rectum. Clinicopathologic correlation and implications for adjuvant therapy. Cancer 34: 1278-1292.
5. Pilipshen SJ, Heilweil M, Quan SH, Sternberg SS, Enker WE (1984) Patterns of pelvic recurrence following definitive resections of rectal cancer. Cancer 53: 1354-1362.
6. Cohen AM, Minsky BD (1990) Aggressive surgical management of locally advanced primary and recurrent rectal cancer. Current status and future directions. Dis Colon Rectum33:432-438.
7. Heald RJ, Husband EM, Ryall RD (1982) The mesorectum in rectal cancer surgery--the clue to pelvic recurrence? Br J Surg 69: 613-616.
8. Hojo K, Sawada T, Moriya Y (1989) An analysis of survival and voiding, sexual function after wide iliopelvic lymphadenectomy in patients with carcinoma of the rectum, compared with conventional lymphadenectomy. Dis Colon Rectum 32: 128-133.
9. Enker WE, Pilipshen SJ, Heilweil ML, Stearns MW Jr, Janov AJ, et al. (1986) En bloc pelvic lymphadenectomy and sphincter preservation in the surgical management of rectal cancer. Ann Surg 203: 426-433.
10. Dahl O, Horn A, Morild I, Halvorsen JF, Odland G, et al. (1990) Low-dose preoperative radiation postpones recurrences in operable rectal cancer. Results of a randomized multicenter trial in western Norway. Cancer 66:2286-2294
11. Fisher B, Wolmark N, Rockette H, Redmond C, Deutsch M, et al. (1988) Postoperative adjuvant chemotherapy or radiation therapy for rectal cancer: results from NSABP protocol R-01. J Natl Cancer Inst 80: 21-29.
12. [No authors listed] (1985) Prolongation of the disease-free interval in surgically treated rectal carcinoma. Gastrointestinal Tumor Study Group. N Engl J Med 312: 1465-1472.
13. Porter GA, Soskolne CL, Yakimets WW, Newman SC (1998) Surgeon-related factors and outcome in rectal cancer. Ann Surg 227: 157-167.
14. Wood W WD (1933) Carcinoma of the rectum. An anatomico-pathological study. Edinb Med J 40:321.
15. Pollett WG, Nicholls RJ (1983) The relationship between the extent of distal clearance and survival and local recurrence rates after curative anterior resection for carcinoma of the rectum. Ann Surg 98:159-163.
16. Heald RJ (1995) Rectal cancer: the surgical options. Eur J Cancer 31A: 1189-1192.
17. Enker WE, Thaler HT, Cranor ML, Polyak T (1995) Total mesorectal excision in the operative treatment of carcinoma of the rectum. J Am CollSurg 181: 335-346.
18. MacFarlane JK, Ryall RD, Heald RJ (1993) Mesorectal excision for rectal cancer. Lancet 341: 457-460.
19. Sebag-Montefiore D, Stephens RJ, Steele R, Monson J, Grieve R, et al. (2009) Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCIC-CTG C016): a multicentre, randomised trial. Lancet373:811-820.
20. Zaheer S, Pemberton JH, Farouk R, Dozois RR, Wolff BG, et al. (1998) Surgical treatment of adenocarcinoma of the rectum. Ann Surg 227: 800-811.
21. Bokey EL, Ojerskog B, Chapuis PH, Dent OF, Newland RC, et al. (1999) Local recurrence after curative excision of the rectum for cancer without adjuvant therapy: role of total anatomical dissection. Br J Surg86:1164-1170.
22. Lopez-Kostner F, Lavery IC, Hool GR, Rybicki LA, Fazio VW (1998) Total mesorectal excision is not necessary for cancers of the upper rectum. Surgery 124: 612-617.
23. Ono C, Yoshinaga K, Enomoto M, Sugihara K (2002) Discontinuous rectal cancer spread in the mesorectum and the optimal distal clearance margin in situ. Dis Colon Rectum 45: 744-749.
24. Scott N, Jackson P, al-Jaberi T, Dixon MF, Quirke P, et al. (1995) Total mesorectal excision and local recurrence: a study of tumour spread in the mesorectum distal to rectal cancer. Br J Surg 82: 1031-1033.
25. Wexner SD, Cohen SM (1995) Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg 82: 295-298.
26. Ströhlein MA, Grützner KU, Jauch KW, Heiss MM (2008) Comparison of laparoscopic vs. open access surgery in patients with rectal cancer: a prospective analysis. Dis Colon Rectum 51: 385-391.
27. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, et al. (2010) Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97: 1638-1645.
28. Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, et al. (2009)Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 10:44-52.
29. Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008) Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev : CD003432.
30. Laurent C, Leblanc F, Gineste C, Saric J, Rullier E (2007) Laparoscopic approach in surgical treatment of rectal cancer. Br J Surg 94: 1555-1561.
31. Romano G, Rotondano G, D'Alessandro V, Esposito P, Novi A, et al. (1997) Pelvic recurrence following resection of rectal cancer: a multivariate predictive model. IntSurg 82: 67-71.
32. Compton CC, Fielding LP, Burgart LJ, Conley B, Cooper HS, et al. (2000) Prognostic factors in colorectal cancer. College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med 124: 979-994.
33. Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99: 433-441.
34. Tepper JE, O'Connell MJ, Niedzwiecki D, Hollis D, Compton C, et al. (2001) Impact of number of nodes retrieved on outcome in patients with rectal cancer. J ClinOncol 19: 157-163.
35. http://www.qualityforum.org/pdf/cancer/txAppA-Specifications_web.pdf
36. Spiliotis J, Datsis A (2004) The surgical approach to locally recurrent rectal cancer. Tech Coloproctol 8 Suppl 1: s33-35.
37. Boyle KM, Sagar PM, Chalmers AG, Sebag-Montefiore D, Cairns A, et al. (2005) Surgery for locally recurrent rectal cancer. Dis Colon Rectum 48: 929-937.
38. Kusters M, Marijnen CA, van de Velde CJ, Rutten HJ, Lahaye MJ, et al. (2010) Patterns of local recurrence in rectal cancer; a study of the Dutch TME trial. Eur J SurgOncol 36: 470-476.
39. Sterk P, Shekarriz B, Gunter S, Nolde J, Keller R, et al. (2005)Voiding and sexual dysfunction after deep rectal resection and total mesorectal excision: prospective study on 52 patients. IntJ Colorectal Dis 20:423-427.
40. Amato A, Pescatori M, Butti A (1991) Local recurrence following abdominoperineal excision and anterior resection for rectal carcinomaDis Colon Rectum34:317-322.
41. Bissett IP, McKay GS, Parry BR, Hill GL (2000) Results of extrafascial excision and conventional surgery for rectal cancer at Auckland Hospital. Aust N Z J Surg 70: 704-709.
42. Bonadeo FA, Vaccaro CA, Benati ML, Quintana GM, Garione XE, et al. (2001) Rectal cancer: local recurrence after surgery without radiotherapy. Dis Colon Rectum 44: 374-379.
43. Cecil TD, Sexton R, Moran BJ, Heald RJ (2004) Total mesorectal excision results in low local recurrence rates in lymph node-positive rectal cancer. Dis Colon Rectum47:1145-1149.
44. Dehni N, McFadden N, McNamara DA, Guiguet M, Tiret E, et al. (2003) Oncologic results following abdominoperineal resection for adenocarcinoma of the low rectum. Dis Colon Rectum 46: 867-874.
45. Ferulano GP, Dilillo S, La Manna S, Forgione A, Lionetti R, et al. (2000) Influence of the surgical treatment on local recurrence of rectal cancer: a prospective study (1980-1992). J SurgOncol 74: 153-157.
46. Havenga K, Enker WE, Norstein J, Moriya Y, Heald RJ, et al. (1999) Improved survival and local control after total mesorectal excision or D3 lymphadenectomy in the treatment of primary rectal cancer: an international analysis of 1411 patients. Eur J SurgOncol25:368-374.
47. Jatzko GR, Jagoditsch M, Lisborg PH, Denk H, Klimpfinger M, et al. (1999) Long-term results of radical surgery for rectal cancer: multivariate analysis of prognostic factors influencing survival and local recurrenceEur J SurgOncol25:284-291.
48. Kapiteijn E, Marijnen CA, Colenbrander AC, Klein Kranenbarg E, Steup WH, et al. (1998) Local recurrence in patients with rectal cancer diagnosed between 1988 and 1992: a population-based study in the west Netherlands. Eur J SurgOncol24:528-535.
49. Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, et al. (2001) Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 345: 638-646.
50. Killingback M, Barron P, Dent OF (2001) Local recurrence after curative resection of cancer of the rectum without total mesorectal excision. Dis Colon Rectum 44: 473-483.
51. Lavery IC,Lopez-Kostner F, Fazio VW, Fernandez-Martin M, Milsom JW, (1997) Chances of cure are not compromised with sphincter-saving procedures for cancer of the lower third of the rectum. Surgery 122:779-784.
52. Law WL, Chu KW (2002) Local recurrence following total mesorectal excision with double-stapling anastomosis for rectal cancers: analysis of risk factors. World journal of surgery 26:1272-1276.
53. Manfredi S, Benhamiche AM, Meny B, Cheynel N, Rat P, et al. (2001) Population-based study of factors influencing occurrence and prognosis of local recurrence after surgery for rectal cancer. Br J Surg 88: 1221-1227.
54. Morino M, Allaix ME, Giraudo G, Corno F, Garrone C (2005) Laparoscopic versus open surgery for extraperitoneal rectal cancer: a prospective comparative study. SurgEndosc 19: 1460-1467.
55. Nesbakken A, Nygaard K, Westerheim O, Mala T, Lunde OC (2002)Local recurrence after mesorectal excision for rectal cancer. Eur J SurgOncol 28:126-134.
56. Park IJ, Choi GS, Lim KH, Kang BM, Jun SH (2009) Laparoscopic resection of extraperitoneal rectal cancer: a comparative analysis with open resection. SurgEndosc 23: 1818-1824.
57. Paty PB, Enker WE, Cohen AM, Lauwers GY (1994) Treatment of rectal cancer by low anterior resection with coloanal anastomosis. Ann Surg 219: 365-373.
58. Read TE, Ogunbiyi OA, Fleshman JW, Birnbaum EH, Fry RD, et al. (2001) Neoadjuvant external beam radiation and proctectomy for adenocarcinoma of the rectum. Dis Colon Rectum 44: 1778-1790.
59. Ross A, Rusnak C, Weinerman B, Kuechler P, Hayashi A, et al. (1999) Recurrence and survival after surgical management of rectal cancer. Am J Surg 177: 392-395.
60. Rubbini M, Vettorello GF, Guerrera C, Mari C, De Anna D, et al. (1990) A prospective study of local recurrence after resection and low stapled anastomosis in 183 patients with rectal cancer. Dis Colon Rectum 33: 117-121.
61. Rullier E, Laurent C, Carles J, Saric J, Michel P, et al. (1997) Local recurrence of low rectal cancer after abdominoperineal and anterior resection. Br J Surg 84: 525-528.
62. Sauer R1 (2002) Adjuvant and neoadjuvant radiotherapy and concurrent radiochemotherapy for rectal cancer. PatholOncol Res 8: 7-17.
63. (1990 )Preoperative short-term radiation therapy in operable rectal carcinoma. A prospective randomized trial. Stockholm Rectal Cancer Study Group. Cancer. 66:49-55.
64.  (1997) Improved survival with preoperative radiotherapy in resectable rectal cancer. Swedish Rectal Cancer Trial. N Engl J Med 336: 980-987.
65. Van Lingen CP, Zeebregts CJ, Gerritsen JJ, Mulder HJ, Mastboom WJ, et al. (2003) Local recurrence of rectal cancer after total mesorectal excision without preoperative radiotherapy. Int J Gastrointest Cancer.34:129-134.
66. Wibe A, Moller B, Norstein J, Carlsen E, Wiig JN, et al. (2002)A national strategic change in treatment policy for rectal cancer--implementation of total mesorectal excision as routine treatment in Norway. A national audit. Dis Colon Rectum45:857-866.
67. Ng KH, Ng DC, Cheung HY, Wong JC, Yau KK, et al. (2009) Laparoscopic resection for rectal cancers: lessons learned from 579 cases. Ann Surg 249: 82-86.
68. Fukunaga Y, Higashino M, Tanimura S, Takemura M, Fujiwara Y (2010) Laparoscopic rectal surgery for middle and lower rectal cancer. SurgEndosc 24: 145-151.
69. Tsang WW, Chung CC, Kwok SY, Li MK (2006) Laparoscopic sphincter-preserving total mesorectal excision with colonic J-pouch reconstruction: five-year results. Ann Surg 243: 353-358.
70. Morino M, Parini U, Giraudo G, Salval M, BrachetContul R, et al. (2003) Laparoscopic total mesorectal excision: a consecutive series of 100 patients. Ann Surg 237: 335-342.
71. Pugliese R, Di Lernia S, Sansonna F, Scandroglio I, Maggioni D, et al. (2008) Results of laparoscopic anterior resection for rectal adenocarcinoma: retrospective analysis of 157 cases. Am J Surg195:233-238.
72. Anthuber M, Fuerst A, Elser F, Berger R, Jauch KW (2003) Outcome of laparoscopic surgery for rectal cancer in 101 patients. Dis Colon Rectum 46: 1047-1053.
73. Poulin EC, Schlachta CM, Gregoire R, Seshadri P, Cadeddu MO, et al. (2002) Local recurrence and survival after laparoscopic mesorectal resection forrectal adenocarcinoma. SurgEndosc16:989-995.
74. Agha A, Fürst A, Hierl J, Iesalnieks I, Glockzin G, et al. (2008) Laparoscopic surgery for rectal cancer: oncological results and clinical outcome of 225 patients. SurgEndosc 22: 2229-2237.

--