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Transanal endoscopic microsurgery for rectal tumors: the St. Mary’s experience
The American Journal of Surgery 194 (2007) 694 – 698
Laparoscopy
Transanal endoscopic microsurgery for rectal tumors: the St. Mary’s experience Emmanouil Zacharakis, M.D., Ph.D., Simon Freilich, M.B.B.S., Sushil Rekhraj, B.Sc., M.B., Ch.B., M.R.C.S., M.Sc., Thanos Athanasiou, M.D., Ph.D., F.E.C.T.S., Paraskeva Paraskeva, Ph.D., F.R.C.S., Paul Ziprin, M.D., F.R.C.S.*, Ara Darzi, K.B.E., Hon.F.R.Eng., F.Med.Sci. Department of Biosurgery and Surgical Technology, Imperial College London, St Mary’s Hospital, 10th Floor, QEQM Wing, St Mary’s Campus, Praed St, London W2 1NY, UK Manuscript received December 21, 2006; revised manuscript March 3, 2007
Abstract Background: The aim of this study is to describe a single institution’s experience in the use of transanal endoscopic microsurgery for rectal tumors. Methods: Between 1996 and 2005, transanal endoscopic microsurgery was performed in 76 patients. The histologic diagnosis was adenoma in 48 and adenocarcinoma in 28 patients. Results: Clear resection margins were achieved in 71 of 74 patients (95.9%). Overall morbidity was 18.9% because 14 patients developed minor (10 patients) or major complications (4 patients). During the follow-up, benign tumor recurrence was detected in 3 patients (6.3%). The recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1%, 42.8%, and 66.6%, respectively. Comments: Transanal endoscopic microsurgery is a safe and feasible technique with low incomplete excision rates and may be the preferred method in patients with benign rectal tumors. Its role in the management of malignant tumors should be limited to selected patients with T1 lesions. © 2007 Excerpta Medica Inc. All rights reserved. Keywords: Local excision; Minimally invasive; Rectal tumors; TEM; TEMS; Transanal endoscopic microsurgery; Transanal excision
Carcinomas and large villous adenomas of the rectum have been traditionally treated by major operations, such as anterior or abdominoperineal resection [1]. Local excision techniques, including the transanal, transsphincteric, or posterior approaches, are well-described alternative methods associated with less postoperative morbidity and mortality [2]. However, for lesions located in the middle and particularly in the upper rectum, the traditional transanal approach is often cumbersome because it allows access to distal tumors only and is associated with high incomplete excision and local recurrence rates [3]. Transanal endoscopic microsurgery (TEMS) is a minimally invasive surgical technique originally designed by Buess et al [4] in the 1980s. TEMS has emerged because it offers several advantages over the traditional transanal ex-
cision by providing improved visualization and exposure, permitting more precise resection of tumors located 2 to 22 cm from the anal verge [5]. This technique is primarily used for selected rectal tumors (both malignant and benign) [6]. However, TEMS may also be used for noncurative treatment in patients who are unfit for major surgery or when the cancer has advanced to a stage at which cure by radical resection is unlikely [6]. Prospective series have shown similar morbidity— but shorter length of stay, lower incomplete excision rates, and fewer recurrences—with transanal excision [7,8]. The aim of this study was to describe a single institution’s experience with the use of TEMS for both treatment of both benign and malignant rectal disease. The goal was to evaluate its feasibility, morbidity, and recurrence rates.
* Corresponding author. Tel.: ⫹011-44 (0) 79449 51160; fax: ⫹011-44 (0) 20788 67950. E-mail address: [email protected]
Materials and Methods Patients undergoing TEMS between 1996 and 2005 at St Mary’s Hospital in London were identified from a prospec-
0002-9610/07/$ – see front matter © 2007 Excerpta Medica Inc. All rights reserved. doi:10.1016/j.amjsurg.2007.03.005
E. Zacharakis et al. / The American Journal of Surgery 194 (2007) 694 – 698 Table 1 TEMS: tumor characteristics and outcome Parameter Size in cm (mean ⫾ SD) Distance from anal verge in cm (mean ⫾ SD) Length of the surgery in min (mean ⫾ SD) Resection margin in mm (mean ⫾ SD) No. with incomplete excision (%) No. with recurrence (%)
Benign tumors (n ⫽ 48) 3.9 ⫾ 1.3 11.1 ⫾ 2.6 78 ⫾ 15 4.4 ⫾ 3 2 (4.2) 3 (6.3)
Malignant tumors (n ⫽ 28) 3.1 ⫾ 1.1
695
annually thereafter. Follow-up examination included complete clinical examination as well as rigid sigmoidoscopy. In addition, patients with malignant tumors underwent periodic metastatic work up, and all patients underwent colonoscopic surveillance as per British Society of Gastroenterology guidelines.
10.5 ⫾ 2 86 ⫾ 10 4.8 ⫾ 4 1 (3.7) 8 (33.3)
tive colorectal database. During this time period, TEMS was performed in 76 patients with rectal tumors. The mean age of the patients was 66.3 (37 to 91) years. The male-tofemale ratio was 48:28. All patients underwent preoperative endoscopic biopsy and radiologic staging by magnetic resonance imaging and/or endoscopic ultrasound. The preoperative histologic diagnosis was benign adenoma in 54 and adenocarcinoma in 22 patients. Criteria for patient selection were mobile tumors ⬍5cm in size, occupying ⬍50% of the rectal circumference, and located 4 to 18 cm from the anal verge. TEMS was applied to 2 groups of patients. The first group included patients with a preoperative diagnosis of benign rectal tumor not amenable to endoscopic removal. The second was comprised of a highly selected group of patients with malignant rectal tumors who were unfit for major surgery because of significant comorbidity or advanced age. Also included were patients who had refused radical surgery. All patients underwent complete bowel preparation before the procedure. Perioperative antibiotic prophylaxis was also administered. The TEMS operative technique was performed as previously described [9 –11] using a 40-mm rectoscope with patients under general anesthesia and positioned so that the lesion was orientated at the inferior aspect of the operative field. Carbon dioxide insufflation was used for the pneumorectum. Lesions were excised circumferentially with at least 10-mm macroscopic margins by way of either full or partial thickness excision when the lesions were located in the intraperitoneal rectum. None of the patients of the study received neoadjuvant chemoradiotherapy. Data prospectively recorded included tumor distance from the anal verge, lesion size, operative time, and final histopathology. Malignant tumors were classified according to the level of extension: Tis ⫽ mucosa; T1 ⫽ submucosa; T2 ⫽ muscularis propria; T3 ⫽ perirectal. Complications, resection margins, incomplete excision, and recurrence rates were also reviewed. The presence of tumor within 1 mm of the specimen’s margin was classified as a positive margin. Local recurrence was defined as the presence of a neoplasm in proximity to the site of the previous excision on follow-up endoscopy. The median follow-up in our series was 37 (6 to 96) months. Regarding follow-up, patients were examined at 6-month intervals for the first 2 years after surgery and
Results Mean operating time was 80.6 (38 –180) minutes, and the mean hospital stay was 3.2 (1 to 51) days. Mortality among the patients in our study was 0%. Overall morbidity was 18.4% because 14 patients developed minor or major complications (4 patients or 5.2%). Three patients had perioperative complications, ie, perforation of the intraperitoneal rectum, and the defect could not be closed primarily by way of the TEMS rectoscope. Two of these patients were treated by conversion to anterior resection and the remaining one by defunctioning transverse loop stoma formation. Major complications also consisted of fecal peritonitis on postoperative day 3 in 1 patient who required laparotomy and defunctioning transverse loop stoma formation. Clinical assessment of sphincter function showed early continence impairment to flatus and soiling in 2 patients, but complete continence was restored within 10 weeks in both. Other minor complications included urinary retention in 6, minor bleeding in 5, and pyrexia in 2 patients. Tumors were located at a mean distance of 10.9 ⫾ 3 cm from the anal verge, with a mean maximal dimension of 3.4 ⫾ 1.5 cm. Postoperative histologic examination of the excised specimens confirmed 48 (63.1%) adenomas and 28 (36.9%) malignant tumors. Six (11.1%) of 54 patients who had a presurgical diagnosis of adenoma had invasive cancer on postoperative histologic examination. Clear resection margins were achieved in 71 of 74 patients (95.9%), whereas the mean resection margin was 4.6 ⫾ 3 mm. The characteristics of the benign and malignant tumours were listed in Table 1. Forty-eight benign lesions were resected. Mean distance for these tumors from the anal verge was 11.1 ⫾ 2.6 cm, and mean size was 3.9 ⫾ 1.3 cm. Of the 48 lesions, 17 were located in the middle rectum (5–10 cm), and 29 were located in the upper rectum (Fig. 1). Mean length of surgery was 78 ⫾ 15 min. In 1 (2.1%) patient, the procedure was converted to laparotomy and low anterior resection because of perforation of the intraperitoneal rectum. The mean re-
Fig. 1. Distance of tumors from the anal verge.
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E. Zacharakis et al. / The American Journal of Surgery 194 (2007) 694 – 698
section margin for benign lesions was 4.4 ⫾ 3 mm, whereas a histologic clear margin was achieved in 45 (95.7%) of 47 patients. In 2 patients with incomplete excision, repeat excision was required. In all, 3 (6.3%) of 47 patients with benign lesion excised with the TEMS technique developed recurrence during follow-up. One patient with benign tumor who was converted to low anterior resection because of intraoperative perforation of the rectum was not counted as part of the denominator when evaluating recurrence after TEMS. There were also 28 cases of rectal carcinoma excised with the TEMS technique. In none of these patients there was intention to cure because this group of patients included highly selective patients not amenable to radical resection because of significant comorbidity or advanced age, both of which contraindicated a major surgery. Six of the 28 patients were thought to have a benign lesion but after TEM surgery were found to have invasive cancer. Of these 6, 3 underwent radical curative-intent surgery; 2 refused recommended additional treatment; and 1 was unfit for further radical resection. In addition, 15 of the remaining 22 patients with malignant tumors were judged to have comorbidities that prohibited radical surgery, and 7 refused radical surgery even although we advised this as preferred option for curative intent. Mean distance for these tumors from the anal verge was 10.5 ⫾ 2 cm, and mean size was 3.1 ⫾ 1.1 cm. Of these lesions, 14 were located in the middle rectum, and 12 were located in the upper rectum (Fig. 1). Mean length of surgery was 86 ⫾ 10 min. Perforation of the intraperitoneal rectum occurred in 2 (7.1%) patients and was treated by conversion to low anterior resection and defunctioning transverse loop stoma formation, respectively. Histologic grading of malignant tumors was T1 in 14, T2 in 11, and T3 in 3 patients. Preoperative diagnosis and further treatment for patients with T1 and T2 tumors are listed in Tables 2 and 3, respectively. The mean resection margin for the malignant lesions was 4.8 ⫾ 4 mm, whereas a histologic clear margin was achieved in 26 (96.3%) of 27 patients. One patient underwent incomplete excision as a palliative procedure; this patient died from metastatic disease 2 months after surgery, and no further action was required. During follow-up, the recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1% (n ⫽ 1), 42.8% (n ⫽ 3) and 66.6% (n ⫽ 2) respectively. One patient with T2 tumor who was converted to low anterior resection because of intraoperative perforation of the rectum, as well as 3 patients with T2 invasive cancer that was diagnosed as adenomas before surgery and who underwent further treatment with low anterior resection, were not counted as part Table 2 Preoperative diagnosis and further treatment for T1 excised tumors No. of patients (N ⫽ 14) 3 11
Preoperative diagnosis
Further treatment
Severe dysplastic adenoma T1 cancer
Refused radical surgery (n ⫽ 2) Comorbidity (n ⫽ 1) Refused radical surgery (n ⫽ 3) Comorbidity (n ⫽ 8)
Table 3 Preoperative diagnosis and further treatment for T2 excised tumors Number of patients Preoperative (N ⫽ 11) diagnosis 3 4 4
Further treatment
Severe dysplastic Anterior resection adenoma T1 cancer Refused radical surgery (n ⫽ 2) Comorbidity (n ⫽ 2) T2 cancer Comorbidity
of the denominator when evaluating the recurrence after TEMS. Comments TEMS is a minimally invasive sphincter-preserving procedure that currently plays an expanding role in the surgical management of rectal tumors. When colonoscopic polypectomy fails to remove large and sessile adenomas because of technical reasons, surgical options include either local resection or major operations, such as low anterior and abdominoperineal resection [1]. The most important factor in avoiding local recurrence after local excision of a rectal adenoma is the complete removal of the tumor, with tumorfree margins [1]. However, the traditional transanal technique leads to variable failure, up to 27%, and high recurrence rates, up to 39% [12]. This may be explained by inadequate intraoperative exposure because this technique is limited to the lower third of the rectum [13]. Buess et al [4] have advocated the TEMS procedure, which enables formal transanal excision and has several advantages over the traditional transanal technique by providing improved exposure, improved vision, and access to the entire rectum. Despite the fact that the technique was initially developed for local excision of benign rectal tumors, it may be an alternative treatment for patients with early rectal cancer or in patients unfit for major surgery [14]. It has been reported that in carefully selected patients with early rectal cancer, local excision combined with chemoradiotherapy may be associated with cure rates equal to the ones achieved after radical excision [15]. However, locoregional treatment of early rectal cancer with the TEMS technique carries the possibility of leaving metastatic lymph node disease, and the selection criteria have not yet been adequately defined [6]. One of the main advantages of TEMS over the traditional major surgery for rectal tumors is that it represents a safe technique with less perioperative mortality [16]. Published mortality for elective abdominal colorectal surgery varies from .6% to 8% [17]. In contrast, Middleton et al [6], in a systematic review of comparative studies and case series of TEMS until 2002, found only 5 perioperative deaths out of a total 1,046 patients who underwent TEMS for benign rectal tumors. In addition, the investigators reported 47 deaths among 599 patients who underwent TEMS for malignant rectal tumors. However, only 15 of these deaths were reported as non-cancer related, whereas no death was clearly reported as a perioperative one [6]. In our study, no postoperative death occurred among 76 patients who underwent TEMS for both benign and malignant rectal lesions.
E. Zacharakis et al. / The American Journal of Surgery 194 (2007) 694 – 698
Regarding the complication rates, it has been reported that overall morbidity for conventional transanal surgery varies from 0% to 14.5% [18]. The alternatives for treatment of tumors in the middle and the upper part of the rectum include, apart from the traditional abdominal surgery, the transsphincteric and posterior approaches [2]. However, both abdominal surgery and the above-mentioned local resection techniques are associated with remarkable morbidity rates, 42% and 22%, respectively [13,19 –21]. In contrast, Middleton et al [6], in a systematic review of case series using TEMS, found a typical complication rate for adenomas resection that ranged from 3% to 7%. The relevant rate among patients who underwent TEMS for malignant lesions varied from 0% to 28%, with a median of 19% [6]. Similarly, in our study, overall morbidity was 18.4%, whereas major complications were observed in only 5.2% of our patients. Complications specific related to TEMS may include perforation into the peritoneal cavity and anal incontinence. The intraperitoneal perforation rate during TEMS excision varies in reported series from 1.3% to 8% [1,5,13,22,23]. However, perforation into the peritoneal cavity does not always necessitate the conversion to open laparotomy because primary endoscopic repair without postoperative consequences has also been described [12,24]. In our series of 76 patients, we report 3 (3.9%) intraperitoneal perforations, but the defect could not be closed primarily by way of the TEMS rectoscope in any of these patients. TEMS is a sphincter-preserving procedure, but prolonged anal dilatation with the 40-mm rectoscope may induce sphincter function problems after surgery. Demartines et al [5] reported a 12% incontinence rate with full postoperative recovery after 3 months. Similarly, Lev-Chelouche et al [1] reported mild anal incontinence in 5 (6.6%) of 75 patients who underwent TEMS. However, persistent mild anal leakage was observed in 2 of these 5 patients. This is in accordance with the results of Floyd et al [23], who also found permanent fecal soilage in 1.3% of their patients. In contrast, Palma et al [13] reported postoperative transitory grade II incontinence in 65 of 100 patients, but full recovery was observed in 98% of them. In our series, early continence impairment to flatus and soiling was detected in 2 of 76 patients, but complete continence was restored within 10 weeks in both. These results indicate that incontinence after TEMS is a minor problem, whereas relevant studies that included continence scores did not imply a change in treatment strategy. The effects of anal dilatation indicated decreased sphincter tone, varying from 25% to 37% of predilatation pressure, with full recovery within 6 to 16 weeks [25,26]. One should also take into consideration the risk of incontinence in conventional transanal surgery by using the Parks retractor if this is to be the alternative procedure [27]. TEMS is clearly applicable in benign lesions of the rectum. The malignant potential of adenomas, which is directly related to size and histologic type, necessitates their early removal. The first line of treatment for adenomatous polyps of the rectum should be the colonoscopic resection. However, for rectal lesions that are too large and sessile to be removed endoscopically, transanal surgical techniques and other options exist. It has been stated that for villous adenomas located in low or middle rectum, transanal exci-
697
sion can be as effective as TEM and has similar recurrence rates [28]. However, for lesions of the middle and upper rectum, transanal excision is difficult and often impossible to reach with conventional instrumentation. TEMS is particularly advantageous for this kind of tumor, offering a preferable alternative to transabdominal surgery. In a review article summarizing the series of transanal excision for rectal tumors, the reported recurrence rates varied between 8% and 33% [29]. In contrast, Middleton et al [6], in a systematic review of case series using the TEMS technique, found median local recurrence rate of 5.1% (range 0% to 15.8%). In our study, 3 (6.3%) of 47 patients with benign lesion excised with TEMS developed recurrence during follow-up. It is believed that the magnified optics at the tip of the rectoscope during the TEMS technique allow improved visualization and more complete excision, justifying the low recurrence rates compared with the traditional transanal excision technique [22]. Local excision of rectal cancers remains a matter of debate, and we do not routinely advocate this approach. Local recurrence after abdominoperineal resection for T1 rectal cancer has been reported to be low, with rates varying from 0% to 10% in some studies [30]. Outcomes after conventional transanal excision of T1 disease have been questioned because local recurrence rates range from 0% to 33% [15,31]. More recently, Madbouly et al [32] reported actuarial local recurrence of 29% after local excision of T1 rectal cancers without adjuvant therapy. The high local recurrence rates after conventional local excision have generated concern about the safety of this form of treatment [23]. In contrast, the TEMS approach is considered by some investigators to offer oncologic results for T1 rectal tumors comparable with those with the more traditional formal resection techniques [16]. However, published case series on TEMS have reported recurrence rates for malignant disease that range from 0% to 50%, but most of these studies are heterogeneous according to selection criteria and use of adjuvant therapy [33]. The only prospective randomized trial for TEMS versus anterior resection reported that the TEMS group had 1 local recurrence (4%), whereas the anterior resection group had 1 patient die from distant metastasis (4%); the 5-year survival probability was 96% for both groups [20]. Local excision of T2 and T3 tumors is less controversial because these cancers are accompanied by high risk of lymph node metastasis, approximately 17% and 50%, respectively [34]. Transanal excision of T2 rectal tumors has been reported to result in high local failure rates, from 28% to 48% [35]. In contrast, the use of postoperative adjuvant radiotherapy has been shown to decrease the incidence of local recurrence on the order to 10% [36]. Moreover, Lezoche et al [37], in a prospective study of 35 patients with T2 rectal cancers who underwent preoperative radiotherapy and TEMS, found that after median follow-up of 38 months, the local recurrence rate was only 2.85%. However, it is believed that the routine use of the TEMS for T2 and T3 stage lesions is not an oncologically curative excision because of significant risk of missing nodal involvement [16]. In our study, 28 rectal carcinomas were excised using the TEMS technique. In none of these cases was there intention to cure because this group of patients included a highly selective group of patients who were not
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amenable to radical resection because of significant comorbidity or advanced age, both of which precluded major surgery. Three patients who were diagnosed to have a benign lesion before surgery underwent radical resection after surgery, whereas the remaining 7 refused to undergo radical treatment. During the follow-up, the recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1%, 42.8%, and 66.6%, respectively. We believe that because of heterogeneity of the existing evidence, a multicenter phase 2 TEM and radiotherapy trial would be necessary first to obtain preliminary data and then to compare TEM with best currently available treatment of the low anterior resection in a phase 3 trial. Only then could the role of TEMS in the treatment of rectal cancer be adequately justified. In conclusion, TEMS is a safe and feasible technique with low incomplete excision rates and may be the preferred method in patients with benign tumors of the mid- and upper rectum. Its role in the management of malignant rectal tumors should be limited to selected patients with T1 tumors, although its role in combination with adjuvant or neoadjuvant chemoradiotherapy warrants further investigation. References [1] Lev-Chelouche D, Margel D, Goldman G, et al. Transanal endoscopic microsurgery. Experience with 75 rectal neoplasms. Dis Colon Rectum 2000;43:662– 8. [2] Grigg M, McDermott FT, Pihl EA, et al. Curative local excision in the treatment of carcinoma of the rectum. Dis Colon Rectum 1984;27: 81–3. [3] Parks AG. A technique for excising extensive villous papillomatous changes in the lower rectum. Proc R Soc Med Lond 1968;61:441–2. [4] Buess G, Theiss R, Gunther M, et al. Endoscopic operative procedure for the removal of rectal polyps. Coloproctology 1984;84:254 – 61. [5] Demartines N, von Flue M, Harder F. Transanal endoscopic microsurgical excision of rectal tumors: Indications and results. World J Surg 2001;25:870 –5. [6] Middleton P, Sutherland L, Maddern G. Transanal endoscopic microsurgery: a systematic review. Dis Colon Rectum 2005;48:270 – 84. [7] Saclarides TJ. Transanal endoscopic microsurgery: a single surgeon’s experience. Arch Surg 1998;133:595–9. [8] Lee W, Lee D, Choi S, et al. Transanal endoscopic microsurgery and radical surgery for T1 and T2 rectal cancer. Surg Endosc 2003;17: 1283–7. [9] Buess G, Mentges B, Manncke K, et al. Technique and results of transanal endoscopic microsurgery in early rectal cancer. Am J Surg 1992;163:63–70. [10] Buess GF, Raestrup H. Transanal endoscopic microsurgery. Surg Oncol Clin North Am 2001;10:709 –31. [11] Benoist S, Taffinder N, Gould S, et al. Transanal endoscopic microsurgery: a forgotten minimally invasive technique [French]. Gastroenterol Clin Biol 2001;25:369 –74. [12] Pigot F, Bouchard D, Mortaji M, et al. Local excision of large rectal villous adenomas. Long-term results. Dis Colon Rectum 2003;46: 1345–50. [13] Palma P, Freudenberg S, Samel S, et al. Transanal endoscopic microsurgery: indications and results after 100 cases. Colorectal Dis 2004;6:350 –55.
[14] Endreseth BH, Wibe A, Svinsas M, et al. Postoperative morbidity and recurrence after local excision of rectal adenomas and rectal cancer by transanal endoscopic microsurgery. Colorectal Dis 2005;7:133–7. [15] Sengupta S, Tjandra JJ. Local excision of rectal cancer: what is the evidence? Dis Colon Rectum 2001;44:1345– 61. [16] Neary P, Makin GB, White TJ, et al. Transanal endoscopic microsurgery: a variable operative alternative in selected patients with rectal lesions Ann Surg Oncol 2003;10:1106 –11. [17] Mella J, Biffin A, Radcliffe AG, et al. Population based audit of colorectal cancer management in two UK health regions. Br J Surg 1997;84:1731– 6. [18] Sakamoto GD, MacKeigan JM, Senagore AJ. Transanal excision of large rectal villous adenomas. Dis Colon Rectum 1991;34:880 –5. [19] Westbook KC, Lang NP, Broadwater JR, et al. Posterior approaches to the rectum. Ann Surg 1982;195:677– 85. [20] Winde G, Nottberg H, Keller R, et al. Surgical cure for early rectal carcinomas (T1). Transanal endoscopic microsurgery vs. anterior resection. Dis Colon Rectum 1996;39:1116 –21. [21] Kanellos I, Zacharakis E, Christoforidis E, et al. Low anterior resection without protective colostomy. Tech Coloproctol 2002;6:153–7. [22] Guerrieri M, Baldarelli M, Morino M, et al. Transanal endoscopic microsurgery in rectal adenomas: Experience of six Italian centres. Dig Liver Dis 2006;38:202–7. [23] Floyd ND, Saclarides TJ. Transanal endoscopic microsurgical resection of pT1 rectal tumors. Dis Colon Rectum 2005;49:164 – 8. [24] Gavagan JA, Whiteford MH, Swanstrom LL. Full thickness intraperitoneal excision by transanal endoscopic microsurgery does not increase short-term complication. Am J Surg 2004;187:360 – 4. [25] Kennedy ML, Lubowski DZ, King DW. Transanal endoscopic microsurgery excision. Is anorectal function compromised? Dis Colon Rectum 2002;45:601– 4. [26] Heminway D, Flett M, McKee RF, et al. Sphincter function after transanal endoscopic microsurgical excision of rectal tumors. Br J Surg 1996;83:51– 6. [27] Van Tets WF, Kuijpers JH, Tran K, et al. Influence of Parks anal retractor on anal sphincter pressures. Dis Colon Rectum 1997;40: 1042–5. [28] Featherstone JM, Grabham JA, Fozard JB. Per-anal excision of large rectal villous adenomas. Dis Colon Rectum 2004;48:86 –9. [29] Cocilovo C, Smith LE, Stahl T, et al. Transanal endoscopic excision of rectal adenomas. Surg Endosc 2003;17:1461–3. [30] Sticca RP, Rodriguez-Bigas M, Penetrante RB, et al. Curative resection for stage I rectal cancer: natural history, prognostic factors, and recurrence patterns. Cancer Invest 1996;14:491–7. [31] Wagman RT, Minsky BD. Conservative management of rectal cancer with local excision and adjuvant therapy. Oncology 2001;15:513–9. [32] Madbouly KM, Remzi FH, Erker BA, et al. Recurrence after transanal excision of T1 rectal cancer: should we be concerned? Dis Colon Rectum 2005;48:711–21. [33] Ganai S, Kanumuri P, Rao R, et al. Local recurrence after transanal endoscopic microsurgery for rectal polyps and early cancers. Ann Surg Oncol 2006;13:547–56. [34] Killingback M. Local excision of carcinoma of the rectum: indications. World J Surg 1992;16:437– 6. [35] Garcia-Aguilar J, Mellgren A, Sirivongs P, et al. Local excision of carcinoma of the rectum without adjuvant therapy: a word of caution. Ann Surg 2000;231:345–51. [36] Minsky BD, Enker WE, Cohen AM, et al. Clinicopathological features in rectal cancer treated by local excision and postoperative radiation therapy. Radiat Med 1995;13:235– 41. [37] Lezoche E, Guerrieri M, Paganini A, et al. Long term results of patients with pT2 rectal cancer treated by radiotherapy and transanal endoscopic microsurgical excision. World J Surg 2002;26:1170 – 4.
Laparoscopy
Transanal endoscopic microsurgery for rectal tumors: the St. Mary’s experience Emmanouil Zacharakis, M.D., Ph.D., Simon Freilich, M.B.B.S., Sushil Rekhraj, B.Sc., M.B., Ch.B., M.R.C.S., M.Sc., Thanos Athanasiou, M.D., Ph.D., F.E.C.T.S., Paraskeva Paraskeva, Ph.D., F.R.C.S., Paul Ziprin, M.D., F.R.C.S.*, Ara Darzi, K.B.E., Hon.F.R.Eng., F.Med.Sci. Department of Biosurgery and Surgical Technology, Imperial College London, St Mary’s Hospital, 10th Floor, QEQM Wing, St Mary’s Campus, Praed St, London W2 1NY, UK Manuscript received December 21, 2006; revised manuscript March 3, 2007
Abstract Background: The aim of this study is to describe a single institution’s experience in the use of transanal endoscopic microsurgery for rectal tumors. Methods: Between 1996 and 2005, transanal endoscopic microsurgery was performed in 76 patients. The histologic diagnosis was adenoma in 48 and adenocarcinoma in 28 patients. Results: Clear resection margins were achieved in 71 of 74 patients (95.9%). Overall morbidity was 18.9% because 14 patients developed minor (10 patients) or major complications (4 patients). During the follow-up, benign tumor recurrence was detected in 3 patients (6.3%). The recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1%, 42.8%, and 66.6%, respectively. Comments: Transanal endoscopic microsurgery is a safe and feasible technique with low incomplete excision rates and may be the preferred method in patients with benign rectal tumors. Its role in the management of malignant tumors should be limited to selected patients with T1 lesions. © 2007 Excerpta Medica Inc. All rights reserved. Keywords: Local excision; Minimally invasive; Rectal tumors; TEM; TEMS; Transanal endoscopic microsurgery; Transanal excision
Carcinomas and large villous adenomas of the rectum have been traditionally treated by major operations, such as anterior or abdominoperineal resection [1]. Local excision techniques, including the transanal, transsphincteric, or posterior approaches, are well-described alternative methods associated with less postoperative morbidity and mortality [2]. However, for lesions located in the middle and particularly in the upper rectum, the traditional transanal approach is often cumbersome because it allows access to distal tumors only and is associated with high incomplete excision and local recurrence rates [3]. Transanal endoscopic microsurgery (TEMS) is a minimally invasive surgical technique originally designed by Buess et al [4] in the 1980s. TEMS has emerged because it offers several advantages over the traditional transanal ex-
cision by providing improved visualization and exposure, permitting more precise resection of tumors located 2 to 22 cm from the anal verge [5]. This technique is primarily used for selected rectal tumors (both malignant and benign) [6]. However, TEMS may also be used for noncurative treatment in patients who are unfit for major surgery or when the cancer has advanced to a stage at which cure by radical resection is unlikely [6]. Prospective series have shown similar morbidity— but shorter length of stay, lower incomplete excision rates, and fewer recurrences—with transanal excision [7,8]. The aim of this study was to describe a single institution’s experience with the use of TEMS for both treatment of both benign and malignant rectal disease. The goal was to evaluate its feasibility, morbidity, and recurrence rates.
* Corresponding author. Tel.: ⫹011-44 (0) 79449 51160; fax: ⫹011-44 (0) 20788 67950. E-mail address: [email protected]
Materials and Methods Patients undergoing TEMS between 1996 and 2005 at St Mary’s Hospital in London were identified from a prospec-
0002-9610/07/$ – see front matter © 2007 Excerpta Medica Inc. All rights reserved. doi:10.1016/j.amjsurg.2007.03.005
E. Zacharakis et al. / The American Journal of Surgery 194 (2007) 694 – 698 Table 1 TEMS: tumor characteristics and outcome Parameter Size in cm (mean ⫾ SD) Distance from anal verge in cm (mean ⫾ SD) Length of the surgery in min (mean ⫾ SD) Resection margin in mm (mean ⫾ SD) No. with incomplete excision (%) No. with recurrence (%)
Benign tumors (n ⫽ 48) 3.9 ⫾ 1.3 11.1 ⫾ 2.6 78 ⫾ 15 4.4 ⫾ 3 2 (4.2) 3 (6.3)
Malignant tumors (n ⫽ 28) 3.1 ⫾ 1.1
695
annually thereafter. Follow-up examination included complete clinical examination as well as rigid sigmoidoscopy. In addition, patients with malignant tumors underwent periodic metastatic work up, and all patients underwent colonoscopic surveillance as per British Society of Gastroenterology guidelines.
10.5 ⫾ 2 86 ⫾ 10 4.8 ⫾ 4 1 (3.7) 8 (33.3)
tive colorectal database. During this time period, TEMS was performed in 76 patients with rectal tumors. The mean age of the patients was 66.3 (37 to 91) years. The male-tofemale ratio was 48:28. All patients underwent preoperative endoscopic biopsy and radiologic staging by magnetic resonance imaging and/or endoscopic ultrasound. The preoperative histologic diagnosis was benign adenoma in 54 and adenocarcinoma in 22 patients. Criteria for patient selection were mobile tumors ⬍5cm in size, occupying ⬍50% of the rectal circumference, and located 4 to 18 cm from the anal verge. TEMS was applied to 2 groups of patients. The first group included patients with a preoperative diagnosis of benign rectal tumor not amenable to endoscopic removal. The second was comprised of a highly selected group of patients with malignant rectal tumors who were unfit for major surgery because of significant comorbidity or advanced age. Also included were patients who had refused radical surgery. All patients underwent complete bowel preparation before the procedure. Perioperative antibiotic prophylaxis was also administered. The TEMS operative technique was performed as previously described [9 –11] using a 40-mm rectoscope with patients under general anesthesia and positioned so that the lesion was orientated at the inferior aspect of the operative field. Carbon dioxide insufflation was used for the pneumorectum. Lesions were excised circumferentially with at least 10-mm macroscopic margins by way of either full or partial thickness excision when the lesions were located in the intraperitoneal rectum. None of the patients of the study received neoadjuvant chemoradiotherapy. Data prospectively recorded included tumor distance from the anal verge, lesion size, operative time, and final histopathology. Malignant tumors were classified according to the level of extension: Tis ⫽ mucosa; T1 ⫽ submucosa; T2 ⫽ muscularis propria; T3 ⫽ perirectal. Complications, resection margins, incomplete excision, and recurrence rates were also reviewed. The presence of tumor within 1 mm of the specimen’s margin was classified as a positive margin. Local recurrence was defined as the presence of a neoplasm in proximity to the site of the previous excision on follow-up endoscopy. The median follow-up in our series was 37 (6 to 96) months. Regarding follow-up, patients were examined at 6-month intervals for the first 2 years after surgery and
Results Mean operating time was 80.6 (38 –180) minutes, and the mean hospital stay was 3.2 (1 to 51) days. Mortality among the patients in our study was 0%. Overall morbidity was 18.4% because 14 patients developed minor or major complications (4 patients or 5.2%). Three patients had perioperative complications, ie, perforation of the intraperitoneal rectum, and the defect could not be closed primarily by way of the TEMS rectoscope. Two of these patients were treated by conversion to anterior resection and the remaining one by defunctioning transverse loop stoma formation. Major complications also consisted of fecal peritonitis on postoperative day 3 in 1 patient who required laparotomy and defunctioning transverse loop stoma formation. Clinical assessment of sphincter function showed early continence impairment to flatus and soiling in 2 patients, but complete continence was restored within 10 weeks in both. Other minor complications included urinary retention in 6, minor bleeding in 5, and pyrexia in 2 patients. Tumors were located at a mean distance of 10.9 ⫾ 3 cm from the anal verge, with a mean maximal dimension of 3.4 ⫾ 1.5 cm. Postoperative histologic examination of the excised specimens confirmed 48 (63.1%) adenomas and 28 (36.9%) malignant tumors. Six (11.1%) of 54 patients who had a presurgical diagnosis of adenoma had invasive cancer on postoperative histologic examination. Clear resection margins were achieved in 71 of 74 patients (95.9%), whereas the mean resection margin was 4.6 ⫾ 3 mm. The characteristics of the benign and malignant tumours were listed in Table 1. Forty-eight benign lesions were resected. Mean distance for these tumors from the anal verge was 11.1 ⫾ 2.6 cm, and mean size was 3.9 ⫾ 1.3 cm. Of the 48 lesions, 17 were located in the middle rectum (5–10 cm), and 29 were located in the upper rectum (Fig. 1). Mean length of surgery was 78 ⫾ 15 min. In 1 (2.1%) patient, the procedure was converted to laparotomy and low anterior resection because of perforation of the intraperitoneal rectum. The mean re-
Fig. 1. Distance of tumors from the anal verge.
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section margin for benign lesions was 4.4 ⫾ 3 mm, whereas a histologic clear margin was achieved in 45 (95.7%) of 47 patients. In 2 patients with incomplete excision, repeat excision was required. In all, 3 (6.3%) of 47 patients with benign lesion excised with the TEMS technique developed recurrence during follow-up. One patient with benign tumor who was converted to low anterior resection because of intraoperative perforation of the rectum was not counted as part of the denominator when evaluating recurrence after TEMS. There were also 28 cases of rectal carcinoma excised with the TEMS technique. In none of these patients there was intention to cure because this group of patients included highly selective patients not amenable to radical resection because of significant comorbidity or advanced age, both of which contraindicated a major surgery. Six of the 28 patients were thought to have a benign lesion but after TEM surgery were found to have invasive cancer. Of these 6, 3 underwent radical curative-intent surgery; 2 refused recommended additional treatment; and 1 was unfit for further radical resection. In addition, 15 of the remaining 22 patients with malignant tumors were judged to have comorbidities that prohibited radical surgery, and 7 refused radical surgery even although we advised this as preferred option for curative intent. Mean distance for these tumors from the anal verge was 10.5 ⫾ 2 cm, and mean size was 3.1 ⫾ 1.1 cm. Of these lesions, 14 were located in the middle rectum, and 12 were located in the upper rectum (Fig. 1). Mean length of surgery was 86 ⫾ 10 min. Perforation of the intraperitoneal rectum occurred in 2 (7.1%) patients and was treated by conversion to low anterior resection and defunctioning transverse loop stoma formation, respectively. Histologic grading of malignant tumors was T1 in 14, T2 in 11, and T3 in 3 patients. Preoperative diagnosis and further treatment for patients with T1 and T2 tumors are listed in Tables 2 and 3, respectively. The mean resection margin for the malignant lesions was 4.8 ⫾ 4 mm, whereas a histologic clear margin was achieved in 26 (96.3%) of 27 patients. One patient underwent incomplete excision as a palliative procedure; this patient died from metastatic disease 2 months after surgery, and no further action was required. During follow-up, the recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1% (n ⫽ 1), 42.8% (n ⫽ 3) and 66.6% (n ⫽ 2) respectively. One patient with T2 tumor who was converted to low anterior resection because of intraoperative perforation of the rectum, as well as 3 patients with T2 invasive cancer that was diagnosed as adenomas before surgery and who underwent further treatment with low anterior resection, were not counted as part Table 2 Preoperative diagnosis and further treatment for T1 excised tumors No. of patients (N ⫽ 14) 3 11
Preoperative diagnosis
Further treatment
Severe dysplastic adenoma T1 cancer
Refused radical surgery (n ⫽ 2) Comorbidity (n ⫽ 1) Refused radical surgery (n ⫽ 3) Comorbidity (n ⫽ 8)
Table 3 Preoperative diagnosis and further treatment for T2 excised tumors Number of patients Preoperative (N ⫽ 11) diagnosis 3 4 4
Further treatment
Severe dysplastic Anterior resection adenoma T1 cancer Refused radical surgery (n ⫽ 2) Comorbidity (n ⫽ 2) T2 cancer Comorbidity
of the denominator when evaluating the recurrence after TEMS. Comments TEMS is a minimally invasive sphincter-preserving procedure that currently plays an expanding role in the surgical management of rectal tumors. When colonoscopic polypectomy fails to remove large and sessile adenomas because of technical reasons, surgical options include either local resection or major operations, such as low anterior and abdominoperineal resection [1]. The most important factor in avoiding local recurrence after local excision of a rectal adenoma is the complete removal of the tumor, with tumorfree margins [1]. However, the traditional transanal technique leads to variable failure, up to 27%, and high recurrence rates, up to 39% [12]. This may be explained by inadequate intraoperative exposure because this technique is limited to the lower third of the rectum [13]. Buess et al [4] have advocated the TEMS procedure, which enables formal transanal excision and has several advantages over the traditional transanal technique by providing improved exposure, improved vision, and access to the entire rectum. Despite the fact that the technique was initially developed for local excision of benign rectal tumors, it may be an alternative treatment for patients with early rectal cancer or in patients unfit for major surgery [14]. It has been reported that in carefully selected patients with early rectal cancer, local excision combined with chemoradiotherapy may be associated with cure rates equal to the ones achieved after radical excision [15]. However, locoregional treatment of early rectal cancer with the TEMS technique carries the possibility of leaving metastatic lymph node disease, and the selection criteria have not yet been adequately defined [6]. One of the main advantages of TEMS over the traditional major surgery for rectal tumors is that it represents a safe technique with less perioperative mortality [16]. Published mortality for elective abdominal colorectal surgery varies from .6% to 8% [17]. In contrast, Middleton et al [6], in a systematic review of comparative studies and case series of TEMS until 2002, found only 5 perioperative deaths out of a total 1,046 patients who underwent TEMS for benign rectal tumors. In addition, the investigators reported 47 deaths among 599 patients who underwent TEMS for malignant rectal tumors. However, only 15 of these deaths were reported as non-cancer related, whereas no death was clearly reported as a perioperative one [6]. In our study, no postoperative death occurred among 76 patients who underwent TEMS for both benign and malignant rectal lesions.
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Regarding the complication rates, it has been reported that overall morbidity for conventional transanal surgery varies from 0% to 14.5% [18]. The alternatives for treatment of tumors in the middle and the upper part of the rectum include, apart from the traditional abdominal surgery, the transsphincteric and posterior approaches [2]. However, both abdominal surgery and the above-mentioned local resection techniques are associated with remarkable morbidity rates, 42% and 22%, respectively [13,19 –21]. In contrast, Middleton et al [6], in a systematic review of case series using TEMS, found a typical complication rate for adenomas resection that ranged from 3% to 7%. The relevant rate among patients who underwent TEMS for malignant lesions varied from 0% to 28%, with a median of 19% [6]. Similarly, in our study, overall morbidity was 18.4%, whereas major complications were observed in only 5.2% of our patients. Complications specific related to TEMS may include perforation into the peritoneal cavity and anal incontinence. The intraperitoneal perforation rate during TEMS excision varies in reported series from 1.3% to 8% [1,5,13,22,23]. However, perforation into the peritoneal cavity does not always necessitate the conversion to open laparotomy because primary endoscopic repair without postoperative consequences has also been described [12,24]. In our series of 76 patients, we report 3 (3.9%) intraperitoneal perforations, but the defect could not be closed primarily by way of the TEMS rectoscope in any of these patients. TEMS is a sphincter-preserving procedure, but prolonged anal dilatation with the 40-mm rectoscope may induce sphincter function problems after surgery. Demartines et al [5] reported a 12% incontinence rate with full postoperative recovery after 3 months. Similarly, Lev-Chelouche et al [1] reported mild anal incontinence in 5 (6.6%) of 75 patients who underwent TEMS. However, persistent mild anal leakage was observed in 2 of these 5 patients. This is in accordance with the results of Floyd et al [23], who also found permanent fecal soilage in 1.3% of their patients. In contrast, Palma et al [13] reported postoperative transitory grade II incontinence in 65 of 100 patients, but full recovery was observed in 98% of them. In our series, early continence impairment to flatus and soiling was detected in 2 of 76 patients, but complete continence was restored within 10 weeks in both. These results indicate that incontinence after TEMS is a minor problem, whereas relevant studies that included continence scores did not imply a change in treatment strategy. The effects of anal dilatation indicated decreased sphincter tone, varying from 25% to 37% of predilatation pressure, with full recovery within 6 to 16 weeks [25,26]. One should also take into consideration the risk of incontinence in conventional transanal surgery by using the Parks retractor if this is to be the alternative procedure [27]. TEMS is clearly applicable in benign lesions of the rectum. The malignant potential of adenomas, which is directly related to size and histologic type, necessitates their early removal. The first line of treatment for adenomatous polyps of the rectum should be the colonoscopic resection. However, for rectal lesions that are too large and sessile to be removed endoscopically, transanal surgical techniques and other options exist. It has been stated that for villous adenomas located in low or middle rectum, transanal exci-
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sion can be as effective as TEM and has similar recurrence rates [28]. However, for lesions of the middle and upper rectum, transanal excision is difficult and often impossible to reach with conventional instrumentation. TEMS is particularly advantageous for this kind of tumor, offering a preferable alternative to transabdominal surgery. In a review article summarizing the series of transanal excision for rectal tumors, the reported recurrence rates varied between 8% and 33% [29]. In contrast, Middleton et al [6], in a systematic review of case series using the TEMS technique, found median local recurrence rate of 5.1% (range 0% to 15.8%). In our study, 3 (6.3%) of 47 patients with benign lesion excised with TEMS developed recurrence during follow-up. It is believed that the magnified optics at the tip of the rectoscope during the TEMS technique allow improved visualization and more complete excision, justifying the low recurrence rates compared with the traditional transanal excision technique [22]. Local excision of rectal cancers remains a matter of debate, and we do not routinely advocate this approach. Local recurrence after abdominoperineal resection for T1 rectal cancer has been reported to be low, with rates varying from 0% to 10% in some studies [30]. Outcomes after conventional transanal excision of T1 disease have been questioned because local recurrence rates range from 0% to 33% [15,31]. More recently, Madbouly et al [32] reported actuarial local recurrence of 29% after local excision of T1 rectal cancers without adjuvant therapy. The high local recurrence rates after conventional local excision have generated concern about the safety of this form of treatment [23]. In contrast, the TEMS approach is considered by some investigators to offer oncologic results for T1 rectal tumors comparable with those with the more traditional formal resection techniques [16]. However, published case series on TEMS have reported recurrence rates for malignant disease that range from 0% to 50%, but most of these studies are heterogeneous according to selection criteria and use of adjuvant therapy [33]. The only prospective randomized trial for TEMS versus anterior resection reported that the TEMS group had 1 local recurrence (4%), whereas the anterior resection group had 1 patient die from distant metastasis (4%); the 5-year survival probability was 96% for both groups [20]. Local excision of T2 and T3 tumors is less controversial because these cancers are accompanied by high risk of lymph node metastasis, approximately 17% and 50%, respectively [34]. Transanal excision of T2 rectal tumors has been reported to result in high local failure rates, from 28% to 48% [35]. In contrast, the use of postoperative adjuvant radiotherapy has been shown to decrease the incidence of local recurrence on the order to 10% [36]. Moreover, Lezoche et al [37], in a prospective study of 35 patients with T2 rectal cancers who underwent preoperative radiotherapy and TEMS, found that after median follow-up of 38 months, the local recurrence rate was only 2.85%. However, it is believed that the routine use of the TEMS for T2 and T3 stage lesions is not an oncologically curative excision because of significant risk of missing nodal involvement [16]. In our study, 28 rectal carcinomas were excised using the TEMS technique. In none of these cases was there intention to cure because this group of patients included a highly selective group of patients who were not
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amenable to radical resection because of significant comorbidity or advanced age, both of which precluded major surgery. Three patients who were diagnosed to have a benign lesion before surgery underwent radical resection after surgery, whereas the remaining 7 refused to undergo radical treatment. During the follow-up, the recurrence rates among patients with T1, T2, and T3 malignant tumors were 7.1%, 42.8%, and 66.6%, respectively. We believe that because of heterogeneity of the existing evidence, a multicenter phase 2 TEM and radiotherapy trial would be necessary first to obtain preliminary data and then to compare TEM with best currently available treatment of the low anterior resection in a phase 3 trial. Only then could the role of TEMS in the treatment of rectal cancer be adequately justified. In conclusion, TEMS is a safe and feasible technique with low incomplete excision rates and may be the preferred method in patients with benign tumors of the mid- and upper rectum. Its role in the management of malignant rectal tumors should be limited to selected patients with T1 tumors, although its role in combination with adjuvant or neoadjuvant chemoradiotherapy warrants further investigation. References [1] Lev-Chelouche D, Margel D, Goldman G, et al. Transanal endoscopic microsurgery. Experience with 75 rectal neoplasms. Dis Colon Rectum 2000;43:662– 8. [2] Grigg M, McDermott FT, Pihl EA, et al. Curative local excision in the treatment of carcinoma of the rectum. Dis Colon Rectum 1984;27: 81–3. [3] Parks AG. A technique for excising extensive villous papillomatous changes in the lower rectum. Proc R Soc Med Lond 1968;61:441–2. [4] Buess G, Theiss R, Gunther M, et al. Endoscopic operative procedure for the removal of rectal polyps. Coloproctology 1984;84:254 – 61. [5] Demartines N, von Flue M, Harder F. Transanal endoscopic microsurgical excision of rectal tumors: Indications and results. World J Surg 2001;25:870 –5. [6] Middleton P, Sutherland L, Maddern G. Transanal endoscopic microsurgery: a systematic review. Dis Colon Rectum 2005;48:270 – 84. [7] Saclarides TJ. Transanal endoscopic microsurgery: a single surgeon’s experience. Arch Surg 1998;133:595–9. [8] Lee W, Lee D, Choi S, et al. Transanal endoscopic microsurgery and radical surgery for T1 and T2 rectal cancer. Surg Endosc 2003;17: 1283–7. [9] Buess G, Mentges B, Manncke K, et al. Technique and results of transanal endoscopic microsurgery in early rectal cancer. Am J Surg 1992;163:63–70. [10] Buess GF, Raestrup H. Transanal endoscopic microsurgery. Surg Oncol Clin North Am 2001;10:709 –31. [11] Benoist S, Taffinder N, Gould S, et al. Transanal endoscopic microsurgery: a forgotten minimally invasive technique [French]. Gastroenterol Clin Biol 2001;25:369 –74. [12] Pigot F, Bouchard D, Mortaji M, et al. Local excision of large rectal villous adenomas. Long-term results. Dis Colon Rectum 2003;46: 1345–50. [13] Palma P, Freudenberg S, Samel S, et al. Transanal endoscopic microsurgery: indications and results after 100 cases. Colorectal Dis 2004;6:350 –55.
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