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1 REVIEW ARTICLE Debate and update issues for surgical treatment of mid and lower rectal cancer Professor Department of Surgery Yonsei University College of Medicine Seoul, Korea Nam Kyu Kim, M.D. Debate and update issues for surgical treatment of mid and lower rectal cancer 9

2 Table 1. Selected Series of Local Excision Alone for T1 Rectal Cancers Study Number of patients patients 5-year local recurrence rate(%) 5-year disease free survival rate(%) Chakravartl et al(1999) [7] Steele et al(1999) [8] Garcla-Agullar et al(2000) [9] Paty et al(2002) [10] Nascimbeni et al(2004) [11] Madbouly et al(2005) [12] Endreseth et al(2007) [13] You et al(2007) [14] Ptok et al(2007) [15] Nam Kyu Kim

3 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: Table 2. Selected Series of Local Excision Alone for T2 Rectal caner Study Number of patients patients 5-year local recurrence rate(%) 5-year disease free survival rate(%) Garcla-Agullar et al(2000) [9] Paty et al(2002) [10] Gao et al(2003) [16] You et al(2007) [15] Table 3. Results of Retrospective Series Comparing Local Excision with Radical Surgery for T1 Rectal caner Study 5 year local recurrence rate(%) 5 year overall survival rate(%) Median Follow up(years) Local Excision Radical Resection Local Excision Radical Resection Mellgren et al(2000) [18] Nascimbeni et al(2004) [11] Endreseth et al(2005) [13] Range 2-8 Bentrem et al(2005) [17] You et al(2007) [14] Ptok et al(2007) [15] Folkesson et al(2007) (Mix of T1 and T2) [19] Not reported Nash et al(2009) [20] Debate and update issues for surgical treatment of mid and lower rectal cancer 11

4 Table 4. Transanal Endoscopic Microsurgery versus Radical Surgery for T1 and T2 Rectal cancer TEM Radical resection T stage Local recurrence Overall survival Local recurrence Overall survival Follow-up(months) rate(%) rate(%) rate(%) rate(%) Winde et al(1996) [22] Heintz et al(1998) [23] 1(low risk) (high risk) Lee et al(2003) [24] q 96 De Graaf(2009) [26] Fig. 1. Transanal Endoscopic Operation (TEO) 12 Nam Kyu Kim

5 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: Table 5. Transanal excision with adjuvant treatment for rectal cancer Study Number of patients Follow-up(months) 5-year local recurrence rate(%) 5-year disease free survival rate(%) Coco et al(1992) [28] Fortunato et al(1995) [29] Steele et al(1999) [30] (6 year) Le Voyer et al(1999) [31] (DFS) Russell et al(2000) [32] (DFS) YUHS et al(2007) [33] (pT1, with RT) 76(pT1, without RT) 75(pT2) Table 6. Outcome of patients with rectal cancer undergoing local excision after achieving pathological T0 following neoadjuvant chemoradiation Study Patients with pt0 Follow up median(range) Local recurrence n(%) Distant recurrence n(%) Schell et al(2002) [35] 8 48(18-105) 0 1(12) Ruo et al(2002) [36] 3 29(2-89) 0 0 Hershman et al(2003) [37] 7 33(3-120) 0 0 Bonnen et al(2004) [38] 14 42(5-109) 0 1 Stipa et al(2004) [39] 7 37(18-118) 0 NR Caricato et al(2006) [40] Borschitz et al(2007) [41] 1 24(12-79) 0 0 Lezoche et al(2008) [42] 11 84(72-96) 0 0 Nair et al(2008) [43] 19 64(6-153) 1(5) 1(5) YUHS et al(2008) [44] 4 91(50-127) 0 1(25) Yulia et al(2010) [34] 14 48(5-123) 0 0 Debate and update issues for surgical treatment of mid and lower rectal cancer 13

6 Table 7. Oncologic outcomes after ultra low anterior resection with coloanal anastomosis Study Follow up median(months) Local recurrence n(%) Distant recurrence n(%) Drake et al(1987) [57] Cavaliere et al(2002) [58] Parc et al(2003) [59] Huguet et al(2004) [60] Hautefeuille et al(2004) [61] YUHS et al(2006) [62] YUHS et al(robotic CAA) (2012) [63] NR 14 Nam Kyu Kim

7 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: Table 8. Oncological outcomes following intersphincteric resection for low rectal cancer. Median R0 Local 5-year survival (%) Operative Overall Continence Study n follow-up resection recurrence Overall Disease-free mortality morbidity (mean bowel (months) (%) (%) (%) (%) movements in 24 h) Braun et al(1992) [53] NR Bannon et al(1995) [54] NR NR 1 10 NR Kohler et al(2000) [55] NR Rullier et al(2005) [56] NR Schiessel et al(2005) [57] NR Saito et al(2006) [58] NR Chamlou et al(2007) [59] Akasu et al(2008) [60] NR Krand et al(2009) [61] Han et al(2009) [62] NR Saito et al(2009) [63] NR Weiser et al(2009) [64] NR Yamada et al(2009) [65] Debate and update issues for surgical treatment of mid and lower rectal cancer 15

8 Fig. 2. Intersphincteric resection after neoadjuvant chemoradiation 16 Nam Kyu Kim

9 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: REFERENCES 1. Heald RJ, Husband EM, Ryall RD. The mesorectum in rectal cancer surgery-the clue to pelvic recurrence? Br J Surg 1982;69: Chessin DB, Guillem JG. Surgical issues in rectal cancer: a 2004 update. Clin Colorectal Cancer 2004;4: Jeong SY, Chessin DB, Guillem JG. Surgical treatment of rectal cancer: radical resection. Surg Oncol Clin N Am 2006;15: Urban M, Rosen HR, Hölbling N, Feil W, Hochwarther G, Hruby W, et al. MR imaging for the preoperative planning of sphinctersaving surgery for tumors of the lower third of the rectum: use of intravenous and endorectal contrast materials. Radiology 2000;214: Rullier E, Sebag-Montefiore D. Sphincter saving is the primary objective for local treatment of cancer of the lower rectum. Lancet Oncol 2006;7: NCCN (National Comprehensive Cancer Network) Guidelines Version 3,2012 Rectal cancer. 7. Chakravarti A, Compton CC, Shellito PC, et al. Long-term followup of patients with rectal cancer managed by local excision with and without adjuvant irradiation. Ann Surg 1999; 230: Steele GD Jr, Herndon JE, Bleday R, et al. Sphincter-sparing treatment for distal rectal adenocarcinoma. Ann Surg Oncol 1999; 6: Garcia-Aguilar J, Mellgren A, Sirivongs P, et al. Local excision of rectal cancer without adjuvant therapy: a word of caution. Ann Surg 2000; 231: Paty PB, Nash GM, Baron P, et al. Long-term results of local excision for rectal cancer. Ann Surg 2002; 236: Nascimbeni R, Nivatvongs S, Larson DR, et al. Long-term survival after local excision for T1 carcinoma of the rectum [published erratum appears in: Dis Colon Rectum 2005; 48: ] Dis Colon Rectum 2004; 47: Madbouly KM, Remzi FH, Erkek BA, et al. Recurrence after transanal excision of T1 rectal cancer: should we be concerned? Dis Colon Rectum 2005; 48:711-9; discussion Endreseth BH, Myrvold HE, Romundstad P, et al. Transanal excision vs. major surgery for T1 rectal cancer. Dis Colon Rectum 2005; 48: You YN, Baxter NN, Stewart A, et al. Is the increasing rate of local excision for stage I rectal cancer in the United States justified?: a nationwide cohort study from the national cancer database. Ann Surg 2007; 245: Ptok H, Marusch F, Meyer F, et al. Oncological outcome of local vs. radical resection of low-risk pt1 rectal cancer. Arch Surg 2007; 142: Gao JD, Shao YF, Bi JJ, et al. Local excision carcinoma in early stage. World J Gastroenterol 2003; 9: Bentrem DJ, Okabe S, Wong WD, et al. T1 adenocarcinoma of the rectum: transanal excision or radical surgery? Ann Surg 2005; 242:472-7; discussion Mellgren A, Sirivongs P, Rothenberger DA, et al. Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum 2000; 43: ; discussion Folkesson J, Johansson R, Pahlman L, et al: Population-based study of local surgery for rectal cancer. Br J Surg 94: , Nash GM, Weiser MR, Guillem JG, et al: Long-term survival after transanal excision of T1 rectal cancer. Dis Colon Rectum 52: , Jesse S. Moore, Peter A. Cataldo, Turner Osler et al: Transanal Endoscopic Microsurgery is more effective than traditional transanal excision for resection of rectal masses. Dis Colon Debate and update issues for surgical treatment of mid and lower rectal cancer 17

10 Rectum 51: , Dimitrios Christoforidis, Hyeon-Min Cho, Matthew R. Dixon et al. Transanal endoscopic microsurgery versus conventional transanl excision for patients with early rectal cancer. Annals of Surgery 249, Number 5, May 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: Heintz A, Morschel M, Junginger T. Comparison of results after transanal endoscopic microsurgery and radical resection for T1 carcinoma of the rectum. Surg Endosc 1998; 12: Lee W, Lee D, Choi S, et al. Transanal endoscopic microsurgery and radical surgery for T1 and T2 rectal cancer. Surg Endosc 2003; 17: De Graaf EJ, Doornebosch PG, Tollenaar RA, et al: Transanal endoscopic microsurgery versus total mesorectal excision of T1 rectal adenocarcinomas with curative intention. Eur J Surg Oncol 35: , Kitajima K, Fujimori T, Fujii S et al: Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol 2004 Jun; 29(6): Coco C, Magistrelli P, Granone P, Roncolini G, Picciocchi A. Conservative surgery for early cancer of the distalrectum. Dis Colon Rectum 1992;35: Fortunato L, Ahmad NR, Yeung RS, Coia LR, Eisenberg BL, Sigurdson ER, et al. Long-term follow-up of local excision and radiation therapy for invasive rectal cancer. Dis Colon Rectum 1995;38: Steele GD Jr, Herndon JE, Bleday R, Russell A, Benson A 3rd, Hussain M, et al. Sphincter sparing treatment for distal rectal adenocarcinoma. Ann Surg Oncol 1999;6: Le Voyer TE, Hoffrnan JP, Cooper H, Ross E, Sigurdson E, Eisenberg B. Local excision and chemoradiation for low rectal T1 and T2 cancers is an effective treatment. Am Surg 1999;65: Russell AH, Harris J, Rosenberg PJ, Sause WT, Fisher BJ, Hoffman JP, et al. Anal sphincter conservation for patients with adenocarcinoma of the distal rectum: longterm results of radiation therapy oncology group protocol Int J Radiat Oncol Biol Phys 2000;46: Min BS, Kim NK, Ko YT, Lee KY, Baek SH, Cho CH, et al. Long-term oncologic results of patients with distal rectal cancer treated by local excision with or without adjuvant treatment. Int J Colorectal Dis 2007;22: Yulia Kundel, Ronen Brenner, Ofer Purim et al: Is local excision after complete pathological response to neoadjuvant chemoradiation for rectal cancer an acceptable treatment option? Dis Colon Rectum 2010; 53: Schell SR, Zlotecki RA, Mendenhall WM, Marsh RW, Vauthey JN, Copeland EM III. Transanal excision of locally advanced rectal cancers downstaged using neoadjuvant chemoradiotherapy.j Am Coll Surg. 2002;194: Ruo L, Guillem JG, Minsky BD, Quan SH, Paty PB, Cohen AM. Preoperative radiation with or without chemotherapy and fullthickness transanal excision for selected T2 and T3 distal rectal cancers. Int J Colorectal Dis. 2002;17: Hershman MJ, Myint AS, Makin CA. Multi-modality approach in curative local treatment of early rectal carcinomas. Colorectal Dis. 2003;5: Bonnen M, Crane C, Vauthey JN, et al. Long-term result using local excision after preoperative chemoradiation among selected T3 rectal cancer patients. Int J Radiat Oncol Biol Phys. 2004;60: Stipa F, Lucandri G, Ferri M, Casula G, Ziparo V. Local excision of rectal cancer with transanal endoscopic microsurgery (TEM). Anticancer Res. 2004;24: Caricato M, Borzomati D, Ausania F, et al. Complementary use of local excision and transanal endoscopic microsurgery for rectal cancer after neoadjuvant chemoradiation. Surg Endosc. 2006; 20: Borschitz T, Wachtlin D, Möhler M, Schmidberger H, Junginger T. Neoadjuvant chemoradiation and local excision for T2 3 rectal cancer. Ann Surg Oncol. 2008;15: Lezoche G, Baldarelli M, Guerrieri M, et al. A prospective randomized study with a 5-year minimum follow-up evaluation of transanal endoscopic microsurgery versus laparoscopic total mesorectal excision after neoadjuvant therapy. Surg Endosc. 2008;22: Nair RM, Siegel EM, Chen DT, et al. Long-term results of transanal excision after neoadjuvant chemoradiation for T2 and T3 adenocarcinomas of the rectum. J Gastrointest Surg. 2008; 12(10): Huh JW, Jung EJ, Park YA, Lee KY, Sohn SK. Preoperative chemoradiation followed by transanal excision for rectal cancer. J Surg Res. 2008;148: Habr-Gama A, de Souza PM, Ribeiro U, et al. Low rectal cancer: impact of radiation and chemotherapy on surgical treatment. Dis Colon Rectum 1998;41: Habr-Gama A, de Souza PM, Ribeiro U, et al. Multimodality therapy in low rectal cancer: long-term outcome of complete responders. Dis Colon Rectum 2001;44:A Habr-Gama A, Perez RO, Nadalin W, et al: Operative versus nonoperative treatment for stage 0 distal rectal cancer following chemoradiation therapy: Long-term results. Ann Surg 240: , 2004; discussion Nam Kyu Kim

11 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: 48. Habr-Gama A, Perez RO, Proscurshim I, et al: Patterns of failure and survival for nonoperative treatment of stage c0 distal rectal cancer following neoadjuvant chemoradiation therapy. J Gastrointest Surg 10: , 2006; discussion Maas M, Beets-Tan RG, Lambregts DM, Lammering G, Nelemans PJ, Engelen SM et al.wait-and-see policy for clinical complete responders after chemoradiation for rectal cancer. J Clin Oncol 2011; 29: Kraske P. Zur extirpation hochsitzender mastdarmkrebse. Verch Dtsch Ges Chirurgie 1885;14: Parks AG, Pery JP. Resection and sutured coloanal anastomosis for rectal carcinoma. Br J Surg 1982;69: Williams NS, Price R, Johnston D. The long term effect of sphincter preserving operations for rectal carcinoma on function of the anal sphincter in man. Br J Surg 1980; 67: Ho YH, Tan M, Seow-Choen F. 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J Gastrointest Surg 2005;9: Kang JH, Hur H, Min BS, Lee KY, Kim NK et al: Roboti coloanal anastomosis with or without intersphincteric resection for low rectal cancer: starting with the perianal approach followed by Robotic procedure. Ann Surg Oncol (2012) 19: Moore HG, Riedel E, Minsky BD, Saltz L, Paty P, Wong D, et al. Adequacy of 1-cm distal margin after restorative rectal cancer resection with sharp mesorectal excision and preoperative combined-modality therapy. Ann Surg Oncol 2003;10: Braun J, Treutner KH,Winkeltau G, Heidenreich U, Lerch MM, Schumpelick V. Results of intersphincteric resection of the rectum with direct coloanal anastomosis for rectal carcinoma. Am J Surg 1992; 163: Bannon JP, Marks GJ, Mohiuddin M, Rakinic J, Jian NZ, Nagle D. Radical and local excisional methods of sphincter-sparing surgery after high-dose radiation for cancer of the distal 3 cm of the rectum. Ann Surg Oncol 1995; 2: Köhler A, Athanasiadis S, Ommer A, Psarakis E. 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12 Weiser MR, Quah HM, Shia J, Guillem JG, Paty PB, Temple LK et al. Sphincter preservation in low rectal cancer is facilitated by preoperative chemoradiation and intersphincteric dissection. Ann Surg 2009; 249: Yamada K, Ogata S, Saiki Y, Fukunaga M, Tsuji Y, Takano M. Long-term results of intersphincteric resection for low rectal cancer. Dis Colon Rectum 2009; 52: Bozzeitti F, Mariani L, Miceli R, Doci R, Montalto F, Andreola S, et al. Cancer of the low and middle rectum: local and distant recurrences, and survival in 350 radically resected patients. J Surg Oncol 1996;62: Zaheer S, Pemberton JH, Farouk R, Dozois RR, Wolff BG, Ilstrup D. Surgical treatment of adenocarcinoma of the rectum. Ann Surg 1998;227: Kim JS, Lee CR, Kim NK, Hur H, Min BS et al: Intersphincteric resection and colonanal anastomosis for very low lying rectal cancer. J Korean Surg Soc 2009; 76: Kim JS, Hur H, Kim NK et al: Oncologic Outcomes After Radical Surgery Following Preoperative Chemoradiotherapy for Locally Advanced Lower Rectal Cancer: Abdominoperineal Resection Versus Sphincter-Preserving Procedure Ann Surg Oncol (2009) 16: Heald RJ, Smedh RK, Kald A, Sexton R, Moran BJ. Abdominoperineal excision of the rectum an endangered operation. Norman Nigro Lectureship. Dis Colon Rectum 1997;40: Law WL, Chu KW. Abdominoperineal resection is associated with poor oncological outcome. Br J Surg 2004;91: Marr R, Birbeck K, Garvican J, et al. The modern abdominoperineal excision: the next challenge after total mesorectal excision. Ann Surg 2005;242: Wibe A, Møller B, Norstein J, et al. A national strategic change in treatment policy for rectal cancer implementation of total mesorectal excision as routine treatment in Norway. A national audit. Dis Colon Rectum 2002;45: Nagtegaal ID, van de Velde CJ, Marijnen CA, van Krieken JH, Quirke P. Pathology review committee low rectal cancer: a call for a change of approach in abdominoperineal resection. J Clin Oncol 2005;23: J. Braun, K. H. Treutner, G.Winkeltau, U. Heidenreich, M. M. Lerch, and V. Schumpelick, Results of intersphincteric resection of the rectum with direct coloanal anastomosis for rectal carcinoma, The American Journal of Surgery, vol. 163, no. 4, pp , Swedish Rectal Cancer Trial, Improved survival with preoperative radiotherapy in resectable rectal cancer, The New England Journal of Medicine, vol. 336, no. 14, pp , L. J. Kuo, C. S. Hung, C. H. Wu et al., Oncological and functional outcomes of intersphincteric resection for low rectal cancer, Journal of Surgical Research, vol. 170, pp. e93 e98, Chambers W, Khan A, Waters R, Lindsey I, George B, Mortensen N et al. Examination of outcome following Abdominoperineal Resection for adenocarcinoma in Oxford. Colorectal Dis 2010;12: Ueno M, Oya M, Azekura K, Yamaguchi T, Muto T. Incidence and prognostic significance of lateral lymph node metastasis in patients with advanced low rectal cancer. Br J Surg 2005;92: Eriksen MT, Wibe A, Syse A, Haffner J, Wiig JN, Norwegian Rectal Cancer Group. Inadvertent perforation during rectal cancer resection in Norway. Br J Surg 2004;91: Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol 2008;26: West NP, Finan PJ, Anderin C, Lindholm J, Holm T, Quirke P. Evidence of the oncologic superiority of cylindrical abdominoperineal excision for low rectal cancer. J Clin Oncol 2008; 26: G. Portier1, L. Ghouti1, S. Kirzin1, R. Guimbaud1 et al ; Oncological outcome of ultra-low coloanal anastomosis with and without intersphincteric resection for low rectal adenocarcinoma. British Journal of Surgery 2007; 94: Holbling. Shirouzu K, Ogata Y, Araki Y, Kishimoto Y, Sato Y. A new ultimate anus-preserving operation for extremely low rectal cancer and for anal canal cancer. Tech Coloproctol 2003;7: Nam Kyu Kim

13 Korean Journal of Clinical Oncology Summer 2012;Vol.8,NO.1: Debate and update issues for surgical treatment of mid and lower rectal cancer Department of Surgery, Yonsei University College of Medicine, Seoul, Korea Nam Kyu Kim, M.D. Updates and Debate issues form the surgical treatment of middle or low rectal cancer The main goals for the surgical treatment of rectal cancer were the complete removal of the rectal cancer with surrounding lymphatic draining area, which subsequently result in decreasing the rate of local recurrence as well as prolong patient survival. If the tumor located at the near the anal canal, concerning issues will be whether anal sphincter can be preserved or not and furthermore autonomic pelvic nervous system could be saved or not. Multidisciplinary approach for rectal cancer has been more popular and treatment strategy rapidly changing based on more accurate preoperative local staging finding and minimal invasive surgical techniques become popular too. One of the advance technology is the development of transanal local excision techniques such Transanal endoscopic microsurgery technique such as TEM(transendoscopic microsurgery), TEO(transendoscopic operation) and TAMIS (transanal minimal invasive surgery). Those techniques make us be able to excise early rectal cancer with full thickness as well as unfragmented state, also can be approached to the upper rectum, which can not approach with previous conventional transanal approach method. Local excision for early T1 rectal cancer has been regards as good treatment option because patient can avoid complication related to the radial proctotectomy such as anastomoitc leakage, postoperative sexual and voiding dysfunction and dysregulated bowel movements. Neoadjuvant chemoradiation therapy has been recommended for patient with ct3n0 or ct3 N+ rectal cancer because some clinical trials showed us preoperative chemoradiation therapy showed better local control rate and less toxicities than postoperative chemoradiation treatment. Recent clinical trial both retrospective and prospective showed us a promising results about local excision after neoadjuvant chemoradiation selectively in patients with low rectal cancer. Neoadjuvant chemoradiation therapy for ct2n0 followed by local excision reported excellent oncologic outcomes quite comparable to the radical surgery group. In addition to that, there has been some reports which showed clinical complete remission after neoadjuvant chemoradiation therapy could be wait and see. A couple of observational studies showed wait and see can be possible option of treatment in selective patients. Radial surgery for middle and low rectal cancer still remains a cornerstone of surgical treatment Ultralow anterior resection with or without intersphincteric resection became a more standard surgical method for low rectal cancer. Oncologic and functional outcomes has been reported as safe even functional outcomes study was rare. Furthermore, Abdominoperineal resection has been famous for high intraoperative tumor perforation and positive circumferential resection margin, those factors have been contributed to the high rate of local recurrence and poor survival rate compared with sphincter saving procedures for rectal cancer. Recently, there have been great efforts Debate and update issues for surgical treatment of mid and lower rectal cancer 21

14 for reducing theses problem and total levator excision or extended abdominoperineal resection concepts emerged. Surgeons who advocated this concept recommended perineal dissection under the Jack-knife position. Surgical management for low rectal cancer should be directed for radically and preserving function based on multimodality approach. We need more high level of evidence based on prospective clinical trials for tailored treatment of rectal cancer patients 22 Nam Kyu Kim