Transanal endoscopic operation for rectal cancer after neoadjuvant therapy1 1 Research performed at Department of Surgery and Anatomy, Ribeirão Preto Medical School, University of São Paulo (FMRP-USP), Ribeirão Preto-SP, Brazil.

José Joaquim Ribeiro da Rocha Mário Vinícius Angelete Alvarez Bernardes Marley Ribeiro Feitosa Camila Perazzoli Vanessa Foresto Machado Fernanda Maris Peria Harley Francisco de Oliveira Omar Feres About the authors

Abstract

PURPOSE:

In this paper we report the oncological outcomes from clinical series of patients with rectal cancer submitted to local excision after neoadjuvant therapy and discuss the indications for local excision in partial clinical responders.

METHODS:

We analysed a prospective database of 39 patients submitted to a transanal endoscopic operation for rectal cancer after neoadjuvant chemoradiation between 2006 and 2015, comparing clinical and pathological variables, perioperative complications, recurrence rate and overall survival.

RESULTS:

We obtained 15.4% ypT0, 17.9% ypT1, 35.9% ypT2 and 28.2% ypT3. After a median follow-up of 24 months, tumoral recurrence was observed in 4 patients, one of them with isolated pulmonary metastasis. R0 resection was achieved in 79.5%, and postoperative complications were observed in 30.2% patients and no perioperative mortality occur. Compromise surgical margins do not affect recurrence rate, and 94.9% of patients are alive nowadays.

CONCLUSION:

Local excision could be associated with low recurrence rate and good overall survival. Short hospitalization time and low level of serious complications observed could be an interesting option for patients who would not tolerate a radical procedure or for those who declined a total mesorectal excision. A strict long-term follow-up must be warranted to detect early tumoral recurrence.

Rectal Neoplasms; Rectum; Neoadjuvant Therapy; Natural Orifice Endoscopic Surgery; Neoplasm Recurrence


Introduction

Worldwide, colorectal cancer (CRC) is the third most common cancer in men and the second most common cancer in women, with more than 1 million cases yearly11. Stewart BW, Wild CP. World cancer report 2014. Lyon. 2014.. In Brazil, almost 32600 new cases are expected in 201522. Instituto Nacional de Câncer José Alencar Gomes da Silva (INCA). Estimativa 2014: Incidência de câncer no Brasil. In Vigilância CdPe, editor. Rio de Janeiro: INCA; 2014..

Neoadjuvant Chemoradiation (NCR) followed by rectosigmoidectomy with total mesorectal excision (TME) is the cornerstone of rectal cancer treatment and significantly reduced local recurrence from 8.2% to 2.4% compared with surgery alone33. Benson AB 3rd, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, Enzinger PC, Fakih MG, Fuchs CS, Grem JL, Hunt S, Leong LA, Lin E, Martin MG, May KS, Mulcahy MF, Murphy K, Rohren E, Ryan DP, Saltz L, Sharma S, Shibata D, Skibber JM, Small W Jr,Sofocleous CT, Venook AP, Willett CG, Freedman-Cass DA, Gregory KM. Rectal cancer. J Natl Compr Canc Netw. 2012;10(12):1528-64. PMID:23221790.,44. Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, Wiggers T, Rutten HJ, Pahlman L, Glimelius B, van Krieken JH, Leer JW, van de Velde CJ; Dutch Colorectal Cancer Group. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345(9):638-46. PMID:11547717.. However, a significant functional impact is associated with radical resection, like urinary retention or incontinence, sexual dysfunction and changes in bowel habit55. Walma MS, Kornmann VN, Boerma D, de Roos MA, van Westreenen HL. Predictors of fecal incontinence and related quality of life after a total mesorectal excision with primary anastomosis for patients with rectal cancer. Ann Coloproctol. 2015;31(1):23-8. PMID:25745623.. Moreover, no difference has been observed in overall survival66. Bosset JF, Collette L, Calais G, Mineur L, Maingon P, Radosevic-Jelic L, Daban A, Bardet E, Beny A, Ollier JC; EORTC Radiotherapy Group Trial 22921. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006;355(11):1114-23. PMID16971718..

In some cases, local excision (LE) of early rectal adenocarcinomas has been performed to reduce morbimortality. The indications of LE are usually limited to patients with well-differentiated, small (< 4cm), T1 rectal adenocarcinomas that exhibit no lymphovascular and perineural invasion, located within 15 cm of the anal verge77. Heidary B, Phang TP, Raval MJ, Brown CJ. Transanal endoscopic microsurgery: a review. Can J Surg. 2014;57(2):127-38. PMID:24666451.. Nevertheless, patients with T2 and T3 lesions who are reluctant to undergo radical resection could benefit from LE88. Baatrup G, Breum B, Qvist N, Wille-Jorgensen P, Elbrond H, Moller P, Hesselfeldt P. Transanal endoscopic microsurgery in 143 consecutive patients with rectal adenocarcinoma: results from a Danish multicenter study. Colorectal Dis. 2009;11(3):270-5. PMID:18573118.. In patients with elevated surgical risk, LE showed lower recurrence rates, fewer post-operative complications and less anorectal, urinary and sexual dysfunctions compared to conventional procedures 99. Balani A, Turoldo A, Braini A, Scaramucci M, Roseano M, Leggeri A. Local excision for rectal cancer. J. Surg. Oncol. 2000;74(2):158-62. doi: 10.1002/1096-9098(200006)74:2<158::AID-JSO15>3.0.CO;2-E., 1010. Nastro P, Beral D, Hartley J, Monson JR. Local excision of rectal cancer: review of literature. Dig Surg. 2005;22(1-2):6-15. PMID:15761225..

Choosing the appropriate treatment requires weighing of some factors: overall survival optimization, local recurrence reduction and prevention of genitourinary and intestinal dysfunctions. Attention must be paid in the elderly patients, with higher operation risks1111. Habr-Gama A, São Julião GP, Perez RO. Nonoperative management of rectal cancer: identifying the ideal patients. Hematol Oncol Clin North Am. 2015;29(1):135-51. PMID:25475576., and in the economically active younger patients1212. You YN. Local excision: is it an adequate substitute for radical resection in T1/T2 patients? Semin Radiat Oncol. 2011;21(3):178-84. PMID:21645862..

In the past 10 years, there has been a 21% increase in the number people older than 65 years old, with a consequent increase in the number of surgical procedures in the elderly1313. Neuman MD, Bosk CL. The redefinition of aging in American surgery. Milbank Q. 2013;91(2):288-315. PMID:23758512.,1414. U.S. partment of Health and Human Services. A profile of older americans: 2014. Available from: http://www.aoa.gov/Aging_Statistics/Profile/2013/2.aspx.
http://www.aoa.gov/Aging_Statistics/Prof...
. A significant portion of geriatric patients, show a complex and not completely understood syndrome of frailty. This vulnerability to a stressful event has been suggested as a risk predictor and is associated with substantial morbidity and mortality1515. Soreide K, Desserud KF. Emergency surgery in the elderly: the balance between function, frailty, fatality and futility. Scand J Trauma Resusc Emerg Med. 2015;23:10. PMID:25645443.

16. Kristjansson SR, Nesbakken A, Jordhoy MS, Skovlund E, Audisio RA, Johannessen HO, Bakka A, Wyller TB. Comprehensive geriatric assessment can predict complications in elderly patients after elective surgery for colorectal cancer: a prospective observational cohort study. Crit Rev Oncol Hematol. 2010;76(3):208-17. PMID:20005123.
-1717. Beets GL, Figueiredo NL, Habr-Gama A, van de Velde CJ. A new paradigm for rectal cancer: Organ preservation: Introducing the International Watch & Wait Database (IWWD). Eur J Surg Oncol. 2015;41(12):1562-4. PMID:26493223..

There is limited information regarding LE after NCR in our country. The main objective of the present study is to present the oncological results from a group of patients with rectal cancer submitted to transanal endoscopic operation (TEO) after NCR.

Methods

Patient selection

A prospective database of patients submitted to TEO for rectal adenocarcinoma after neoadjuvant chemoradiation between 2006 and 2015 was analyzed after approval from the Institutional Review Board. The patients were selected according to the previously mentioned indications for local excision77. Heidary B, Phang TP, Raval MJ, Brown CJ. Transanal endoscopic microsurgery: a review. Can J Surg. 2014;57(2):127-38. PMID:24666451.. We also included patients with T1 lesions exhibiting lymphovascular invasion and those with T2 or T3 tumors who refused or could not tolerate radical surgery due to frailty. Patients submitted to palliative surgery were not considered candidates.

Treatment and follow-up

Surgical resection was carried out 8-12 weeks after the end of NCR. The same surgeon performed operations, with a previously described proctoscope1818. Ribeiro da Rocha JJ, Feres O. A new proctoscope for transanal endoscopic operations. Tech Coloproctol. 2008;12(3):241-6. PMID:18679568.. Patients were positioned on the operation table according to the tumor location. Posterior tumors required a lithotomy position while anterior lesions required a prone jack-knife position. The resection was considered as R0 if surgical margins higher than 1 mm were achieved. Follow-up protocol included clinical examination every 3 months with serum CEA during the first 2 years and then annually. A control endoscopic procedure was performed 3 months after TEO, and then every year. Surveillance image exams (thoracic, abdominal and pelvic computed tomography) were repeated annually. Other exams (such as pelvic magnetic resonance imaging, positron emission tomography) were recommended based on the discretion of the treating physician. Patients who developed local recurrence were offered a salvage surgery. Those who refused any major procedure were submitted to a second TEO.

Analysis

Clinicopathological variables were obtained from medical records. Overall and disease-specific survival after TEO was the primary outcome of the study. Statistical analysis of all continuous variables was expressed as mean ± standard deviation (SD). Categorical variables were compared with χ2 tests. A p<0.05 was considered significant. Survival curves were plotted using the Kaplan-Meier method.

Results

The study included 39 patients. Mean age was 65.5±14.4 years. The main characteristics of subjects are summarized in Table 1.

TABLE 1
- Main characteristics of subjects

The average duration of hospital stay was 2 days (1-6 days). Surgery data is summarized in Table 2.

TABLE 2
- Main characteristics of surgical procedures

Mean follow-up of subjects was 24 months (1-110 months). Loss to follow-up rate was 38.5% (n=15). Observed recurrence rate was 10.3% (n=4). Three subjects (75%) developed isolated local recurrence and one subject (25%) was diagnosed with distant metastasis (pulmonary). Patients with local recurrence were submitted to a new TEO in 2 cases (refused radical surgery) and abdominoperineal excision of the rectum in 1 case. The patient with pulmonary metastasis underwent pulmonary segmentectomy. No deaths were observed in the recurrence group. Twelve subjects (30.8%) underwent adjuvant chemotherapy. There was no perioperative mortality, and 5.1% mortality rate observed during follow-up were not cancer-specific. A survival analysis is illustrated in figure 1.

FIGURE 1
- Kaplan-Meier survival function

A univariate analysis was conducted, and no association was found between recurrence and compromised microscope surgical margins, staging, and presence of complications. Table 3 summarizes the univariate analysis results.

TABLE 3
- Univariate analysis for recurrence

Discussion

TME is associated with significant morbidity (10-49%) and mortality (0-9%) rates1919. Heald RJ. The 'Holy Plane' of rectal surgery. J R Soc Med. 1988;81(9):503-8. PMID:3184105.. Moreover, the possibility of permanent or temporary stomas is often associated with unfavorable aesthetic and functional results2020. Alberda WJ, Verhoef C, Nuyttens JJ, Rothbarth J, van Meerten E, de Wilt JH, Burger JW. Outcome in patients with resectable locally recurrent rectal cancer after total mesorectal excision with and without previous neoadjuvant radiotherapy for the primary rectal tumor. Ann Surg Oncol. 2014;21(2):520-6. PMID:24121879.,2121. Kulu Y, Muller-Stich BP, Bruckner T, Gehrig T, Buchler MW, Bergmann F, Ulrich A. Radical surgery with total mesorectal excision in patients with T1 rectal cancer. Ann Surg Oncol. 2015;22(6):2051-8. PMID:25331008.. The relevant morbimortality rates related to the procedure have led to an interest in less invasive procedures.

Tumors located 10 cm from the anal verge are usually amenable to TEO. Full-thickness excision of around mesorectal fat and clear margins are the goal of the procedure. Hemostasis and transverse closure of the resulting rectal defect are also important steps to avoid complications. A clear orientation of the margins is very important to pathological evaluation2222. Althumairi AA, Gearhart SL. Local excision for early rectal cancer: transanal endoscopic microsurgery and beyond. J Gastrointest Oncol. 2015;6(3):296-306. PMID:26029457.. Postoperative pain is usually well managed with oral analgesics and non-steroidal anti-inflammatory drugs. Recovery and return to daily activities are fast2323. Heafner TA, Glasgow SC. A critical review of the role of local excision in the treatment of early (T1 and T2) rectal tumors. J Gastrointest Oncol. 2014;5(5):345-52. PMID:25276407.. Postoperative complications include, rectal bleeding (6%), rectal stenosis (5.5%), urinary retention (1.5%), fecal incontinence (0.5%), and rectovaginal / rectourethral fistulas (<1%) .

TEO is characterized by less surgical stress, short hospital stay, and lower complications. It may be considered as an alternative in older and frail cancer patients2424. Handforth C, Clegg A, Young C, Simpkins S, Seymour MT, Selby PJ, Young J. The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann Oncol. 2015;26(6):1091-101. PMID:25403592.. Younger and active patients concerned with higher complication rates of a radical resection may also be candidates as long as they understand and accept the risks of higher local recurrence.

The rate of R1 resection in the present study was 17.9%, and an elevated rate of tumor fragmentation and compromised tumor margins are related to a poorer surgical outcome in LE. However, compared LE and TEM, no difference in recurrence rates (21% vs. 33%) or overall survival (80% vs. 66%) was found 2323. Heafner TA, Glasgow SC. A critical review of the role of local excision in the treatment of early (T1 and T2) rectal tumors. J Gastrointest Oncol. 2014;5(5):345-52. PMID:25276407..

Adjuvant chemotherapy could reduce the recurrence rates from 19-47% to 5-26%2525. Kajiwara Y, Ueno H, Hashiguchi Y, Mochizuki H, Hase K. Risk factors of nodal involvement in T2 colorectal cancer. Dis Colon Rectum. 2010;53(10):1393-9. PMID:20847621.. For tumors treated by local excision following neoadjuvant therapy, a significant reduction in local recurrence rates from 12% to 4% was achieved2626. Folkesson J, Birgisson H, Pahlman L, Cedermark B, Glimelius B, Gunnarsson U. Swedish Rectal Cancer Trial: long lasting benefits from radiotherapy on survival and local recurrence rate. J Clin Oncol. 2005;23(24):5644-50. PMID:16110023.. The high number of ypT2 and ypT3 operated tumors could explain the 10.3% recurrence rate observed in the present study. Higher recurrence rates in stage II and III patients have previously been observed2727. Perez RO, Habr-Gama A, Sao Juliao GP, Proscurshim I, Coelho AQ, Figueiredo MN, Fernandez LM, Gama-Rodrigues J. Transanal local excision for distal rectal cancer and incomplete response to neoadjuvant chemoradiation - does baseline staging matter? Dis Colon Rectum. 2014;57(11):1253-9. PMID:25285691.,2828. Perez RO, Habr-Gama A, Lynn PB, São Julião GP, Bianchi R, Proscurshim I, Gama-Rodrigues J. Transanal endoscopic microsurgery for residual rectal cancer (ypT0-2) following neoadjuvant chemoradiation therapy: another word of caution. Dis Colon Rectum. 2013;56(1):6-13. PMID:23222274.. Both surgeon and patients should be aware this risk when contemplating any local excision procedure. Moreover, some authors have noted higher rates of unsalvageable recurrence after LE2929. You YN, Roses RE, Chang GJ, Rodriguez-Bigas MA, Feig BW, Slack R, Nguyen S, Skibber JM. Multimodality salvage of recurrent disease after local excision for rectal cancer. Dis Colon Rectum. 2012;55(12):1213-9. PMID:23135578.,3030. Weiser MR, Landmann RG, Wong WD, Shia J, Guillem JG, Temple LK, Minsky BD, Cohen AM, Paty PB. Surgical salvage of recurrent rectal cancer after transanal excision. Dis Colon Rectum. 2005;48(6):1169-75. PMID:15793645..

Conclusion

TEO was characterized by short hospitalization time and was performed with a low level of serious complications. LE could be an option for patients who would not tolerate a radical procedure or for those who declined a low anterior resection or an abdominoperineal excision of the rectum. A strict long-term follow-up must be warranted in all cases since the procedure is related to a higher risk local recurrence.

References

  • 1
    Stewart BW, Wild CP. World cancer report 2014. Lyon. 2014.
  • 2
    Instituto Nacional de Câncer José Alencar Gomes da Silva (INCA). Estimativa 2014: Incidência de câncer no Brasil. In Vigilância CdPe, editor. Rio de Janeiro: INCA; 2014.
  • 3
    Benson AB 3rd, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, Enzinger PC, Fakih MG, Fuchs CS, Grem JL, Hunt S, Leong LA, Lin E, Martin MG, May KS, Mulcahy MF, Murphy K, Rohren E, Ryan DP, Saltz L, Sharma S, Shibata D, Skibber JM, Small W Jr,Sofocleous CT, Venook AP, Willett CG, Freedman-Cass DA, Gregory KM. Rectal cancer. J Natl Compr Canc Netw. 2012;10(12):1528-64. PMID:23221790.
  • 4
    Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, Wiggers T, Rutten HJ, Pahlman L, Glimelius B, van Krieken JH, Leer JW, van de Velde CJ; Dutch Colorectal Cancer Group. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001;345(9):638-46. PMID:11547717.
  • 5
    Walma MS, Kornmann VN, Boerma D, de Roos MA, van Westreenen HL. Predictors of fecal incontinence and related quality of life after a total mesorectal excision with primary anastomosis for patients with rectal cancer. Ann Coloproctol. 2015;31(1):23-8. PMID:25745623.
  • 6
    Bosset JF, Collette L, Calais G, Mineur L, Maingon P, Radosevic-Jelic L, Daban A, Bardet E, Beny A, Ollier JC; EORTC Radiotherapy Group Trial 22921. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006;355(11):1114-23. PMID16971718.
  • 7
    Heidary B, Phang TP, Raval MJ, Brown CJ. Transanal endoscopic microsurgery: a review. Can J Surg. 2014;57(2):127-38. PMID:24666451.
  • 8
    Baatrup G, Breum B, Qvist N, Wille-Jorgensen P, Elbrond H, Moller P, Hesselfeldt P. Transanal endoscopic microsurgery in 143 consecutive patients with rectal adenocarcinoma: results from a Danish multicenter study. Colorectal Dis. 2009;11(3):270-5. PMID:18573118.
  • 9
    Balani A, Turoldo A, Braini A, Scaramucci M, Roseano M, Leggeri A. Local excision for rectal cancer. J. Surg. Oncol. 2000;74(2):158-62. doi: 10.1002/1096-9098(200006)74:2<158::AID-JSO15>3.0.CO;2-E.
  • 10
    Nastro P, Beral D, Hartley J, Monson JR. Local excision of rectal cancer: review of literature. Dig Surg. 2005;22(1-2):6-15. PMID:15761225.
  • 11
    Habr-Gama A, São Julião GP, Perez RO. Nonoperative management of rectal cancer: identifying the ideal patients. Hematol Oncol Clin North Am. 2015;29(1):135-51. PMID:25475576.
  • 12
    You YN. Local excision: is it an adequate substitute for radical resection in T1/T2 patients? Semin Radiat Oncol. 2011;21(3):178-84. PMID:21645862.
  • 13
    Neuman MD, Bosk CL. The redefinition of aging in American surgery. Milbank Q. 2013;91(2):288-315. PMID:23758512.
  • 14
    U.S. partment of Health and Human Services. A profile of older americans: 2014. Available from: http://www.aoa.gov/Aging_Statistics/Profile/2013/2.aspx
    » http://www.aoa.gov/Aging_Statistics/Profile/2013/2.aspx
  • 15
    Soreide K, Desserud KF. Emergency surgery in the elderly: the balance between function, frailty, fatality and futility. Scand J Trauma Resusc Emerg Med. 2015;23:10. PMID:25645443.
  • 16
    Kristjansson SR, Nesbakken A, Jordhoy MS, Skovlund E, Audisio RA, Johannessen HO, Bakka A, Wyller TB. Comprehensive geriatric assessment can predict complications in elderly patients after elective surgery for colorectal cancer: a prospective observational cohort study. Crit Rev Oncol Hematol. 2010;76(3):208-17. PMID:20005123.
  • 17
    Beets GL, Figueiredo NL, Habr-Gama A, van de Velde CJ. A new paradigm for rectal cancer: Organ preservation: Introducing the International Watch & Wait Database (IWWD). Eur J Surg Oncol. 2015;41(12):1562-4. PMID:26493223.
  • 18
    Ribeiro da Rocha JJ, Feres O. A new proctoscope for transanal endoscopic operations. Tech Coloproctol. 2008;12(3):241-6. PMID:18679568.
  • 19
    Heald RJ. The 'Holy Plane' of rectal surgery. J R Soc Med. 1988;81(9):503-8. PMID:3184105.
  • 20
    Alberda WJ, Verhoef C, Nuyttens JJ, Rothbarth J, van Meerten E, de Wilt JH, Burger JW. Outcome in patients with resectable locally recurrent rectal cancer after total mesorectal excision with and without previous neoadjuvant radiotherapy for the primary rectal tumor. Ann Surg Oncol. 2014;21(2):520-6. PMID:24121879.
  • 21
    Kulu Y, Muller-Stich BP, Bruckner T, Gehrig T, Buchler MW, Bergmann F, Ulrich A. Radical surgery with total mesorectal excision in patients with T1 rectal cancer. Ann Surg Oncol. 2015;22(6):2051-8. PMID:25331008.
  • 22
    Althumairi AA, Gearhart SL. Local excision for early rectal cancer: transanal endoscopic microsurgery and beyond. J Gastrointest Oncol. 2015;6(3):296-306. PMID:26029457.
  • 23
    Heafner TA, Glasgow SC. A critical review of the role of local excision in the treatment of early (T1 and T2) rectal tumors. J Gastrointest Oncol. 2014;5(5):345-52. PMID:25276407.
  • 24
    Handforth C, Clegg A, Young C, Simpkins S, Seymour MT, Selby PJ, Young J. The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann Oncol. 2015;26(6):1091-101. PMID:25403592.
  • 25
    Kajiwara Y, Ueno H, Hashiguchi Y, Mochizuki H, Hase K. Risk factors of nodal involvement in T2 colorectal cancer. Dis Colon Rectum. 2010;53(10):1393-9. PMID:20847621.
  • 26
    Folkesson J, Birgisson H, Pahlman L, Cedermark B, Glimelius B, Gunnarsson U. Swedish Rectal Cancer Trial: long lasting benefits from radiotherapy on survival and local recurrence rate. J Clin Oncol. 2005;23(24):5644-50. PMID:16110023.
  • 27
    Perez RO, Habr-Gama A, Sao Juliao GP, Proscurshim I, Coelho AQ, Figueiredo MN, Fernandez LM, Gama-Rodrigues J. Transanal local excision for distal rectal cancer and incomplete response to neoadjuvant chemoradiation - does baseline staging matter? Dis Colon Rectum. 2014;57(11):1253-9. PMID:25285691.
  • 28
    Perez RO, Habr-Gama A, Lynn PB, São Julião GP, Bianchi R, Proscurshim I, Gama-Rodrigues J. Transanal endoscopic microsurgery for residual rectal cancer (ypT0-2) following neoadjuvant chemoradiation therapy: another word of caution. Dis Colon Rectum. 2013;56(1):6-13. PMID:23222274.
  • 29
    You YN, Roses RE, Chang GJ, Rodriguez-Bigas MA, Feig BW, Slack R, Nguyen S, Skibber JM. Multimodality salvage of recurrent disease after local excision for rectal cancer. Dis Colon Rectum. 2012;55(12):1213-9. PMID:23135578.
  • 30
    Weiser MR, Landmann RG, Wong WD, Shia J, Guillem JG, Temple LK, Minsky BD, Cohen AM, Paty PB. Surgical salvage of recurrent rectal cancer after transanal excision. Dis Colon Rectum. 2005;48(6):1169-75. PMID:15793645.

  • Financial source: none
  • 1
    Research performed at Department of Surgery and Anatomy, Ribeirão Preto Medical School, University of São Paulo (FMRP-USP), Ribeirão Preto-SP, Brazil.

Publication Dates

  • Publication in this collection
    2016
Sociedade Brasileira para o Desenvolvimento da Pesquisa em Cirurgia Al. Rio Claro, 179/141, 01332-010 São Paulo SP Brazil, Tel./Fax: +55 11 3287-8814 - São Paulo - SP - Brazil
E-mail: sgolden@terra.com.br