Laparoscopic versus Open Anterior Resection in Patients with Rectal Cancer: a Review of literature
Dr. Yasser Abbas, MBBCH, M.S, D. MAS, MRCS
Total mesorectal excision has become the gold standard for treating rectal tumors. Controversy exists regarding laparoscopic anterior resection of rectal carcinoma.
To review the literature comparing laparoscopic and open anterior resection of rectum utilizing total mesorectal excision (TME) principles for rectal carcinoma.
A literature search was performed on studies comparing laparoscopic and open anterior resection for rectal cancer on perioperative outcome and quality of life.
Laparoscopic total mesorectal excision of rectal carcinoma is feasible and not inferior to open resection regarding oncologic outcomes. However the learning curve and technical difficulties recommends tackling this problem in specialized centers to optimize the outcome. Long term results and big randomized studies are eagerly awaited.
Laparoscopy – open surgical outcome - Postoperative complications - Rectal cancer - Total mesorectal excision - Quality of life
Advocates of laparoscopic surgery in colon cancer showed a lot of growing evidence of its adequate oncological clearance [1–8], most would not agree with its use in rectal cancer. Early reports on laparoscopic rectal cancer surgery were dominated by sphincter-ablating resection [9–15]. Technical hurdles as well as skepticism on oncological clearance had once confined sphincter preservation to carcinomas located at the rectosigmoid junction or in the upper rectum [8, 16–20]. Progress in technology and skills, however, has finally led to the controversial extension of minimally invasive techniques to distal rectal cancer with sphincter preservation [21–33]. Here we present a review of the clinical outcomes of laparoscopic surgery for rectal cancer in the literature in comparison to conventional open surgery.
A successful TME starts with the proper ligation of the SHA or IMA. As one dissects down toward the sacral promontory, the sympathetic nerve trunks are identified. The dissection plane is just anterior or medial to these nerves. Using the cautery or scissors, the nerves are reflected toward the pelvic sidewall while the mesorectal fascia surrounding the mesorectal fat is kept as an intact unit. The dissection starts posteriorly and then at each level proceeds laterally and then anteriorly. In the mid rectal area along the lateral sidewalls, one can sometimes see the parasympathetic nerves tracing anteriorly toward the hypogastric plexus. The plexus is usually on the anterolateral sidewall of the pelvis, just lateral to the seminal vesicles in the man and the cardinal ligaments in the woman. There is often a tough “ligament” that traverses the mesorectum at this point. It theoretically contains the middle rectal artery. However, in a study by Jones et al.,74 this artery is only present to any significance about 20% of the time. The anterior dissection is perhaps the most difficult. In men, one should try to include the two layers of Denonvillier’s fascia. This fascia is composed of peritoneum that has been entrapped between the seminal vesicles and prostate anterior and the rectum posterior (Figure 1A&B). In woman, the peritoneum at the base of the pouch of Douglas is incised and the rectovaginal septum is then separated.
The patients were placed in a modified lithotomy position, and a pneumoperitoneum was established with a Veress needle, maintaining intraabdominal pressure at 12–15 mm Hg. Four or five trocars were placed. the descent of the splenic flexure was first carried out after placing the patient in the anti-Trendelenburg position with inclination to the right. After the patient was placed in the Trendelenburg position, dissection was performed with ligature of the inferior mesenteric vessels at the site of origin, respecting the left colic vein whenever possible. Dissection was then made by the avascular plane, performing rectosigmoid dissection with TME in tumors of the middle and lower thirds (LAR) and mesorectal excision up to 5 cm below the lesion in tumors of the upper third (AR). After completion of the pelvic dissection, the distal end was sectioned using an EndoGIA-type mechanical suturing device. The assistance incision was made at the suprapubic level (Pfannenstiel incision) with a length of 5–7 cm, according to the size of the tumor. Intracorporal anastomosis was made in all cases under laparoscopic control, and a low-pressure aspirative drain was placed next to the anastomosis. Protective ileostomy was performed in cases with very low anastomoses and in patients who had undergone previous neoadjuvant treatment, although this was always done at the discretion of the surgeon. Conversion was defined as the need to carry out an unplanned incision or an incision of greater than normal size to complete the dissection and/or section of the distal end of the rectum. A Pfannenstiel incision or infraumbilical middle laparotomy was performed at to the discretion of the surgeon.
Figure 1 A&B: peritoneal reflections in male and female
Figure 2 A&B:
Figure 3 : Schematic representation of the correct TME dissection versus an incorrect dissection. The dissection should proceed between the mesorectal fascia and the pelvic wall fascia to ensure a complete” TME.
Figure 4: Transverse diagram of the structures of the mid rectum. The proper dissection proceeds just outside the mesorectal fat and fascia but with sparing of the neurovascular bundle and hypogastric plexus that is located anterolaterally along the pelvic sidewall. One or both layers of Denonvillier’s fascia should be included in males and the equivalent fascial dissection along the back of the vagina in females.
Figure 5: The vascular supply of the sigmoid and rectum. A typical ligation is performed at the junction of the SHA and left colic artery. In patients with a clinical suspicion of positive nodes at the level of the IMA or if vascular mobilization is needed for the left and transverse colon, then a ligation of the IMA is performed at the aorta.
Figure 6: Sagittal view of the rectum, bladder, Denonvillier’s fascia, and the prostate. The dissection should proceed anterior to one or both layers of Denonvillier’s fascia.
Nonrandomized comparative studies shows that laparoscopic and open excision of rectal cancer were found to be equivalent in achieving distal and radial margins [9–12, 18, 24, 28, 33–35]; however, it is unclear whether sphincter preservation during laparoscopic total mesorectal excision (TME) makes the resection Margins less than sufficient.
Small comparative studies found no difference in the distal [28, 33] and radial margins  between open and laparoscopic sphincter-preserving TME. the reported distal margin in laparoscopic sphincter-preserving TME for mid and low rectal cancer ranged from 3 to 4.3 cm, with microscopic involvement in 1% (range 0–2) of cases was shown in four separate studies [27,29,30,33].
Another study reported a 7-mm radial margin with 10% microscopic involvement in 50 rectal tumors within 11 cm of anal verge . In two other series, all 131 patients who had carcinoma within 12 cm of the anal verge had tumor-free radial margins [27, 30].Low rectal cancer, being surrounded by a thin mesorectum, is associated with an increased rate of positive radial margin . Long-term local recurrence rates for laparoscopic sphincter-preserving TME are needed to evaluate the actual place of laparoscopic anterior resection of rectum compared to open surgery; however, there are limited recurrence data available [37, 38].
The adequacy of radical resection can also be measured by the ability to achieve high-ligation, specimen characteristics, and lymph node yield.
In Scheidbach series  successful high ligation of the inferior mesenteric artery reported in 342 (90%) of 380 laparoscopic rectal cancer resections.
Rullier found intact fasica propria in 29 (91%) of 32 laparoscopic TME specimens, and demonstrated quality of excision comparable to open surgery . Laparoscopic excision of rectal cancer was found to yield the same specimen length as open surgery in all comparative studies [10, 24, 33, 35, 41], this was contradicted in one study . lymph node harvest in the resected specimens varied considerably from 5.2 to 25 [9–12,18,24,25,27–29,32–35,39,40,42,43], this was found to be similar to that of open surgery in all comparative studies[9–12,18,24,33–35] except one study done by Anthuber M and colleagues .
From the above mentioned data, evidence exists to support that laparoscopic excision of rectal cancer is as radical as open surgery.
Feasibility and safety:
Evidence exists in the literature confirming the safety and feasibility of laparoscopic rectal cancer surgery. Many studies show that mortality rates were similar [9-12, 24, 28, 34, 40]. Also, no increased overall morbidity when compared with open surgery in most comparative studies [10–12,18,28,33,40,41,44]. Araujo et al’ reported that, there was zero mortality and no difference was observed between the two groups in terms of operative and postoperative complications .
1. Importance of diverting stomas:
When diverting ileostomies are only selectively created, after laparoscopic sphincter-preserving TME [24, 27, 32] the clinical leak rate was comparable to that of open TME and remained significant at 11% to 17% [45,46]. Tsang et al, practice routine protective ileostomy and have not experienced a single case of clinical leak, although 9% of their patients have had asymptomatic minor radiological leaks, as revealed by routine postoperative contrast enema . Bretagnol and coworkers reported a 2% leakage rate with routine protective ileostomy . Many studies clearly shown that anastomotic leaks are less frequent with proximal diversion [24, 27, 32], and when routinely employed following laparoscopic resection, comparable results with open resection can be achieved .
2. Case selection:
The feasibility of sphincter preservation following laparoscopic resection of distal rectal carcinoma relies not only on skills, but also on case selection. After exclusion of locally advanced tumors that invaded adjacent structures or the external anal sphincter, Tsang et al achieved sphincter preservation in 44 cases of laparoscopic TME for cancers within 10 cm of anal verge, with a stapled anastomosis at 4 cm (range 2.5–5) . Other single-surgeon series of laparoscopic sphincter-preserving TME have exercised similar case selection [27,29,33].
3. Conversion rate:
Feasibility of any laparoscopic procedure is reflected by its associated conversion rates. Conversion during laparoscopic rectal cancer excision varies greatly, from 0% to 33% [9–12,15,24,25,27,29–35,39–41,43,44]. Common reasons for conversion were intraoperative bleeding, bulky or locally advanced tumors, technical difficulties, and adhesions [9–11,24,25,27,29,31,32,34,35,40]. Many authors clearly emphasized that timely conversion, wherever indicated,is of utmost importance in containing harm and should not be perceived as Failure. it also reflects surgical maturity.
4. The operative time factor:
The average operating time for laparoscopic sphincter-preserving TME was more variable, and ranged from 2 to 7 hours in different reports [21, 22, 27, 28]. Although the difference might be due to variation in the surgical technique (stapled versus transanal intersphincteric dissection and hand-sewn anastomosis), case selection and patient body built status.
the relatively long operating time supports the clear fact that laparoscopic excision of low rectal cancer, though feasible, is technically demanding.
Although there is level one evidence showing that laparoscopic colectomy improves ostoperative recovery [1–3,6–8,20,48,49], there is rarity of studies addressing the same in rectal cancer resection and most of these studies are small with conflicting results.
1. Blood loss:
Compared with open surgery, laparoscopic techniques may be associated with less operative blood loss and reduced perioperative transfusions [18, 33]; others show no difference .
2. Hospital stay:
There is also a marginal benefit in the length of hospital stay, with studies showing either similar [18, 24, 33, 41] or shorter hospital stay [9–12, 28, 34, 40]. The absolute reduction in the mean hospital stay was quite dramatic in the latter case, ranging from 4.5 to 7 days [9–12, 28, 34, 40].
3. Postoperative analgesia:
Evidence with regard to postoperative analgesic requirement is also unclear [10,18,24,44].
4. Postoperative Morbidities:
With few exceptions [9, 24], comparative studies showed either lower [11, 33, 40, 44] or similar [10, 12, 18, 28, 41] overall morbidity rates when compared with open surgery.
A. Wound infection and pulmonary complications:
Three comparative studies on rectal cancer surgery reported a similar infection rate between the two techniques [18,24,33].
In the large series by Kockerling and coauthors on low rectal cancer , the incidences of abdominal wound disorders and chest infection were 5.1% and 4.3% respectively, converted cases being included. These figures are certainly significant, and suggest that, as with laparoscopic colectomy, the smaller the size of abdominal wound the less postoperative wound and pulmonary complications.
B. Port-site hernia:
Many studies addressed this complication. However, there were only three port-site hernias (0.3%) [9, 21, 30] among 1026 patients who had received laparoscopic rectal cancer surgery. Thus, port-site hernia is infrequent and should be avoidable with attention to port-site closure .
C. Postoperative bowel obstruction:
Small comparative studies shows that the incidence of small bowel obstruction after laparoscopic rectal cancer excision was either the same  or just barely lower than [12, 18, 24] after open surgery. These studies are small and lack the long-term follow-up. Available evidence does not show clear difference between both groups.
It was first reported in 1993 , and attracted much controversy against laparoscopic colectomy for malignancy. Recent series and randomized trials showed much lower incidence [1, 7, 54, 55]. The overall incidence in the literature is 0.1%. This is comparable to that of wound recurrence in open surgery [56, 57].
TME was introduced by Heald in 1982 and has set the standard for rectal cancer surgery, with a 10-year local recurrence rate of only 4% [37, 60]. This excellent result of open surgery keeps a strong challenge for laparoscopic surgery. The majority of the comparative studies found similar
local recurrence rates for laparoscopic and open rectal cancer excision [9,10,24,34,5], and most were able to achieve a local recurrence rate below 10%. Local recurrence of laparoscopic
sphincter-saving TME were in the range of 0% to 6% [24,27,29–32]. This is similar to that in open surgery [36,60,61].
Studies on survival data in laparoscopic rectal cancer surgery are scanty in the literature with short follow-up. In a multicenter study on 288 patients with a mean follow-up of 24.8 months, Scheidbach et al  reported 4-year overall survival rates of 86.6% and 71.7% after curative laparoscopic APR and anterior resection respectively. Morino and colleagues  reported 74% 5-year overall survival following curative laparoscopic TME, with a median follow-up of 46 months. With a mean follow-up of 3 years, Leroy and coworkers  reported a slightly lower 5-year figure of 65%. Several small comparative studies of laparoscopic versus open rectal cancer excision demonstrated no survival difference, but follow-up time was short in all these reports [9,18,24,34,35,44].
Apparently laparoscopic TME does not show difference regarding early local disease recurrence and survival rate. Further randomized controlled trials and long-term outcomes needed to support this believe.
In COLOR (colon cancer open or laparoscopic resection) trial, there was no difference in the total cost by laparoscopic or open surgery group within 12 weeks of surgery. In another study there was no difference in the cost for both procedures . In general, laparoscopic surgery is more costly compared to open surgery even though laparoscopic surgery shows shorter hospital stay and comparable operative time in some studies. The importance of cost-effectiveness in overall assessment of laparoscopic role in rectal cancer management cannot be overemphasized; therefore cost analysis studies are needed in the future.
Relation between Laparoscopic rectal cancer excision and genitourinary dysfunction is shown in few reports with conflicting results. One study by Rullier reported one (3.1%) long-term bladder dysfunction in 32 patients after Laparoscopic TME and a 44% sexual dysfunction rate among male patients . On the other hand, Watanabe et al  reported no genitourinary dysfunction in a small series of laparoscopic TME comprising only 7 patients. In Tsang‘series, although no patient suffered from long-term bladder dysfunction, 2 (9.5%) male patients complained of erectile dysfunction at follow-up visits . Theoretically, with the magnified view and improved visualization of deep pelvic structures under the laparoscope, laparoscopic rectal cancer excision should yield functional outcomes at least comparable to, if not better than, open surgery [7,21,33].
Quality of life:
In spite that Open surgery is considered more invasive than laparoscopic surgery; studies could not show significant difference in quality of life between both procedures. Breukink et al, in a recent prospective study evaluating quality of life and sexual dysfunction after laparoscopic TME excision concluded that one year after laparoscopic TME patients reported improvement in some quality of life outcomes .
Available literature comparing laparoscopic and open rectal cancer surgery is limited, non- randomized and contains case series. Laparoscopic TME is safe in experienced hands but requires a steep learning curve and an oncological clearance comparable to that of the open counterpart. Realistic case selection and timely conversion are crucial for success and avoiding harm. Overall morbidity looks similar. Laparoscopic surgery offers less abdominal wound infection and pulmonary complications.
Regarding genitourinary dysfunction after laparoscopic rectal cancer excision data are very limited, and future studies needed to address this problem .from oncological point of view port-site metastasis is rare. Laparoscopic surgery also does not seem to confer any disadvantage in early local disease recurrence and survival figures of rectal cancer. Having no adverse influence on postoperative and early oncological outcomes, laparoscopic rectal cancer surgery therefore deserves further evaluation, in the context of large randomized studies, to determine its functional and financial outcomes as well as long-term oncological outcomes.
 Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P, et al. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trial. Lancet 2002; 359(9325):2224–9.
 The Clinical Outcomes of Surgical Therapy Study Group. Comparison of laparoscopically Assisted and open colectomy for colon cancer. N Engl J Med 2004; 350(20):2050–9.
 Franklin ME Jr, Rosenthal D, Abrego-Medina D, Dorman JP, Glass JL, Norem R, et al. Prospective comparison of open vs. laparoscopic colon surgery for carcinoma. Five-year results. Dis Colon Rectum 1996; 39(Suppl 10):S35–46.
 Hartley JE, Mehigan BJ, MacDonald AW, Lee PWR, Monson JRT. Patterns of recurrence
and survival after laparoscopic and conventional resections for colorectal carcinoma. AnnSurg 2000;232(2):181–6.
 Patanker SK, Larach SW, Ferrara A, Williamson PR, Gallagher JT, DeJesus S, et al.
Prospective comparison of laparoscopic vs. open resections for colorectal adenocarcinoma
over a ten-year period. Dis Colon Rectum 2003;46(5):601–11.
 Champault GG, Barrat C, Raselli R, Elizalde A, Catheline JM. Laparoscopic versus open
surgery for colorectal carcinoma: a prospective clinical trial involving 157 cases with a mean
follow-up of 5 years. Surg Laparosc Endosc 2002;12(2):88–95.
 Chung CC, Tsang WWC, Kwok SY, Li MKW. Laparoscopy and its current role in the management of colorectal disease. Colorectal Dis 2003;5(6):528–43.
 Leung KL, Kwok SPY, Lau WY, Meng WCS, Lam TY, Kwong KH, et al. Laparoscopicassisted resection of rectosigmoid carcinoma: immediate and medium-term results. Arch Surg 1997;132(7):761–4.
 Fleshman JW, Wexner SD, Anvari M, La Tulippe JF, Birnbaum EH, Kodner IJ, et al. Laparoscopic vs. open abdominoperineal resection for cancer. Dis Colon Rectum 1999;42(7):930–9.
 Ramos JR, Petrosemolo RH, Valory EA, Polania FC, Pecanha R. Abdominoperineal resection: laparoscopic versus conventional. Surg Laparosc Endosc 1997;7(2):148–52.
 Iroatulam AJ, Agachan F, Alabaz O, Weiss EG, Nogueras JJ, Wexner SD. Laparoscopic abdominoperineal resection for anorectal cancer. Am Surg 1998;64(1):12–8.
 Darzi A, Lewis C, Menzies Gow N, Guillou PJ, Monson JR. Laparoscopic abdominoperineal excision of the rectum. Surg Endosc 1995;9(4):414–7.
 Chindasub S, Charntaracharmnong C, Nimitvanit C, Akkaranurukul P, Santitarmmanon B. Laparoscopic abdominoperineal resection. J Laparoendosc Surg 1994;4(1):17–21.
 Larach SW, Salomon MC, Williamson PR, Goldstein E. Laparoscopic assisted abdominoperineal resection. Surg Laparosc Endosc 1993;3(2):115–8.
 Glattli A, Birrer S, Buchmann P, Christen D, Frei E, Klaiber C, et al. Technick und resultate der laparoskopischen rektumexstirpation. (Technique and results of laparoscopic rectum resection.) Schweiz Med Wochenschr Suppl 1996;79:85S–8S.
 Goh YC, Eu KW, Seow-Choen F. Early postoperative results of a prospective series of laparoscopic vs. open anterior resections for rectosigmoid cancers. Dis Colon Rectum 1997;40(7):776–80.
 Rhodes M, Rudd M, Nathanson L, Fielding G, Siu S, Hewett P, et al. Laparoscopic anterior resection: a consecutive series of 84 patients. Surg Laparosc Endosc 1996;6(3):213–7.
 Schwandner O, Schiedeck TH, Killaitis C, Bruch HP. A case-control-study comparing laparoscopic versus open surgery for rectosigmoidal and rectal cancer. Int J Colorectal Dis 1999;14(3):158–63.
 Scheidbach H, Schneider C, Baerlehner E, Konradt J, Koeckerling F. Laparoscopic anterior resection for rectal carcinoma. Results of a registry. Surg Oncol Clin N Am 2001;10(3):599–609.
 Leung KL, Kwok SPY, Lam SCW, Lee JFY, Yiu RYC, Ng SSM, et al. Laparoscopic resection of rectosigmoid cancer: prospective randomized trial. Lancet 2004;363:1187–92.
 Weiser MR, Milsom JW. Laparoscopic total mesorectal excision with autonomic nerve preservation. Semin Surg Oncol 2000;19(4):396–403.
 Watanabe M, Teramoto T, Hasegawa H, Kitajima M. Laparoscopic ultralow anterior resection combined with per anum intersphincteric rectal dissection for lower rectal cancer. Dis Colon Rectum 2000;43(Suppl 10):S94–7.
 Chung CC, Ha JPY, Tsang WWC, Li MKW. Laparoscopic-assisted total mesorectal excision and colonic J pouch reconstruction in the treatment of rectal cancer. Surg Endosc 2001;15(10):1098–101.
 Hartley JE, Mehigan BJ, Qureshi AE, Duthie GS, Lee PWR, Monson JRT. Total mesorectal excision: assessment of the laparoscopic approach. Dis Colon Rectum 2001;44(3):315–21.
 Yamamoto S, Watanabe M, Hasegawa H, Kitajima M. Prospective evaluation of laparoscopic surgery for rectosigmoidal and rectal carcinoma. Dis Colon Rectum 2002;45(12):1648–54.
 Pikarsky AJ, Rosenthal R, Weiss EG, Wexner SD. Laparoscopic total mesorectal excision.Surg Endosc 2002;16(4):558–62.
 Morino M, Parini U, Giraudo G, Salval M, Brachet Contul R, Garrone C. Laparoscopic total mesorectal excision: a consecutive series of 100 patients. Ann Surg 2003;237(3):335–42.
 Rullier E, Sa Cunha A, Couderc P, Rullier A, Gontier R, Saric J. Laparoscopic intersphincteric resection with coloplasty and coloanal anastomosis for mid and low rectal cancer. Br J Surg 2003;90(4):445–51.
 Bretagnol F, Rullier E, Couderc P, Rullier A, Saric J. Technical and oncological feasibility of laparoscopic total mesorectal excision with pouch coloanal anastomosis for rectal cancer.Colorectal Dis 2003;5(5):451–3.
 Tsang WWC, Chung CC, Li MKW. Prospective evaluation of laparoscopic total mesorectal excision with colonic J-pouch reconstruction for mid and low rectal cancers. Br J Surg 2003;90(7):867–71.
 Zhou ZG, Wang Z, Yu YY, Shu Y, Cheng Z, Li L, et al. Laparoscopic total mesorectal excision of low rectal cancer with preservation of anal sphincter: a report of 82 cases. World J Gastroenterol 2003;9(7):1477–81.
 Leroy J, Jamali 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(2):281–9.
 Wu WX, Sun YM, Hua Y, Shen LZ. Laparoscopic versus conventional open resection of rectal carcinoma: a clinical comparative study. World J Gastroenterol 2004;10(8):1167–70.
 Baker RP, White EE, Titu L, Duthie GS, Lee PWR, Monson JRT. Does laparoscopic abdominoperineal resection of the rectum compromise long-term survival? Dis Colon Rectum 2002;45(11):1481–5.
 Feliciotti F, Guerrieri M, Paganini AM, De Sanctis A, Campagnacci R, Perretta S, et al.
Long-term results of laparoscopic versus open resections for rectal cancer for 124 unselected patients. Surg Endosc 2003;17(10):1530–5.
 Wibe A, Syse A, Andersen E, Tretli S, Myrvold HE, Soreide O. Oncological outcomes after total mesorectal excision for cure for cancer of the lower rectum: anterior vs. abdominoperineal resection. Dis Colon Rectum 2004;47(1):48–58.
 Adam IJ, Mohamdee MO, Martin IG, Scott N, Finan PJ, Johnston D, et al. Role of circumferential margin involvement in local recurrence of rectal cancer. Lancet 1994;344(8924):707–11.
 Heald RJ, Husband EM, Ryall RD. The mesorectum in rectal cancer surgery: the clue to pelvic recurrence? Br J Surg 1982;69(10):613–6.
 Scheidbach H, Schneider C, Konradt J, Barlehner E, Kohler L, Wittekind Ch, et al. Laparoscopic abdominoperineal resection and anterior resection with curative intent for carcinoma of the rectum. Surg Endosc 2002;16(1):7–13.
 AnthuberM, Fuerst A, Elser F, Berger R, Jauch KW. Outcome of laparoscopic surgery for rectal cancer in 101 patients. Dis Colon Rectum 2003;46(8):1047–53.
 Araujo SEA, da Silva e Sousa AH Jr, de Campos FGCM, Habr Gama A, Dumarco RB, Caravatto PP de P, et al. Conventional approach x laparoscopic abdominoperineal resection for rectal cancer treatment after neoadjuvant chemoradiation: results of a prospective randomized trial. Rev Hosp Clin Fac Med Sao Paulo 2003;58(3):133–40.
 Barlehner E, Decker T, Anders S, Heukrodt B. Laparoskopische chirurgie desrektumkarzinoms. Onkologische radikalitat und spatergebnisse. (Laparoscopic surgery of rectal carcinoma. Radical oncology and late results.) Zentralbl Chir 2001;126(4):302–6.
 Kockerling F, Scheidbach H, Schneider C, Barlehner E, Kohler L, Bruch HP, et al. Laparoscopic abdominoperineal resection: early postoperative results of a prospective study involving 116 patients. The Laparoscopic Colorectal Surgery Study Group. Dis Colon Rectum 2000;43(11):1503–11.
 Vorob ev GI, Shelygin Iu A, Frolov SA, Loshinin KV, Syshkov OI. Laparoskopicheskie operatsii u bol’nykh rakom priamoi kishki (sravnitel’nye rezul’taty laparoskopicheskikh otkrytykh perednikh rezektsii). (Laparoscopic surgery of rectal cancer (comparative results of laparoscopic and open abdominal resection).) Khirurgiia (Mosk) 2003;(3):36–42.
 Karanjia ND, Corder AP, Bearn P, Heald RJ. Leakage from stapled low anastomosis after total mesorectal excision for carcinoma of the rectum. Br J Surg 1994;81(8):1224–6.
 Carlsen E, Schlichting E, Guldvog I, Johnson E, Heald RJ. Effect of the introduction of total mesorectal excision for the treatment of rectal cancer. Br J Surg 1998;85(4):526–9.
 Karanjia ND, Corder AP, Holdsworth PJ, Heald RJ. Risk of peritonitis and fatal septicaemia and the need to defunction the low anastomosis. Br J Surg 1991;78(2):196–8.
 Braga M, Vignali A, Gianotti L, Zuliani W, Radaelli G, Gruarin P, et al. Laparoscopic versus open colorectal surgery: a randomized trial on short-term outcome. Ann Surg 2002; 236(6):759–67.
 Chapman AE, Levitt MD, Hewett P, Woods R, Sheiner H, Maddern GJ. Laparoscopicassisted resection of colorectal malignancies: a systematic review. Ann Surg 2001;234(5):590–606.
 Janson M, Bjorholt I, et al. Randomized clinical trial of the costs of open and laparoscopic surgery for colonic cancer. Br J Surg 2004 ;91:409.
 Larach SW, Patankar SK, Ferrara A, Williamson PR, Perozo SE, Lord AS. Complications of laparoscopic colorectal surgery. Analysis and comparison of early vs. latter experience.Dis Colon Rectum 1997;40(5):592–6.
 Reissman P, Teoh TA, Skinner K, Burns JW, Wexner SD. Adhesion formation after laparoscopic anterior resection in a porcine model: a pilot study. Surg Laparosc Endosc 1996;6(2):136–9.
 Alexander RJ, Jaques BC, Mitchell KG. Laparoscopically assisted colectomy and wound recurrence. Lancet 1993;341(8839):249–50.
 Zmora O, Weiss EG. Trocar site recurrence in laparoscopic surgery for colorectal cancer.Myth or real concern? Surg Oncol Clin N Am 2001;10(3):625–38.
 Lacy AM, Delgado S, Garcia Valdecasas JC, Castells A, Pique JM, Grande L, et al. Port site metastasis and recurrence after laparoscopic colectomy. A randomized trial. Surg Endosc 1998;12(8):1039–42.
 Hughes ES, McDermott FT, Polglase AL, JohnsonWR.Tumor recurrence in the abdominal wall scar tissue after large-bowel cancer surgery. Dis Colon Rectum 1983;26(9):571–2.
 Reilly WT, Nelson H, Schroeder G, Wieand HS, Bolton J, O’Connell MJ. Wound recurrence following conventional treatment of colorectal cancer: a rare but perhaps underestimated problem. Dis Colon Rectum 1996;39(2):200–7.
 Falk PM, Beart RW, et al. laparoscopic colectomy: a critical appraisal. Dis Colon Rectum 1993;36:28.
 S.O. Breukink, H,J. Vander Zaag- Loonen, et al. Prospective evaluation of quality of life and sexual functioning after laparoscopic total mesorectal excision . Dis Colon Rectum 2006;50:147-155..
 Heald RJ, Moran BJ, Ryall RD, Sexton R, MacFarlane JK. Rectal cancer: the Basingstoke experience of total mesorectal excision, 1978–1997. Arch Surg 1998; 133(8):894–9.
 Heald RJ, Smedh RK, Kald A, Sexton R, Moran BJ. Abdominoperineal excision of the rectum- an endangered operation. Dis Colon Rectum 1997; 40(7):747–51.