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Early rectal cancer: the European Association for Endoscopic Surgery (EAES) clinical consensus conference

  • Consensus Statement
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Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The last 30 years have witnessed a significant increase in the diagnosis of early-stage rectal cancer and the development of new strategies to reduce the treatment-related morbidity. Currently, there is no consensus on the definition of early rectal cancer (ERC), and the best management of ERC has not been yet defined. The European Association for Endoscopic Surgery in collaboration with the European Society of Coloproctology developed this consensus conference to provide recommendations on ERC diagnosis, staging and treatment based on the available evidence.

Methods

A multidisciplinary group of experts selected on their clinical and scientific expertise was invited to critically review the literature and to formulate evidence-based recommendations by the Delphi method. Recommendations were discussed at the plenary session of the 14th World Congress of Endoscopic Surgery, Paris, 26 June 2014, and then posted on the EAES website for open discussion.

Results

Tumour biopsy has a low accuracy. Digital rectal examination plays a key role in the pre-operative work-up. Magnification chromoendoscopy, endoscopic ultrasound and magnetic resonance imaging are complementary staging modalities. Endoscopic submucosal dissection and transanal endoscopic microsurgery are the two established approaches for local excision (LE) of selected ERC. The role of all organ-sparing approaches including neoadjuvant therapies followed by LE should be formally assessed by randomized controlled trials. Rectal resection and total mesorectal excision is indicated in the presence of unfavourable features at the pathological evaluation of the LE specimen. The laparoscopic approach has better short-term outcomes and similar oncologic results when compared with open surgery.

Conclusions

The management of ERC should always be based on a multidisciplinary approach, aiming to increase the rate of organ-preserving procedures without jeopardizing survival.

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References

  1. Siegel R, Cuesta MA, Targarona E, Bader FG, Morino M, Corcelles R, Lacy AM, Påhlman L, Haglind E, Bujko K, Bruch HP, Heiss MM, Eikermann M, Neugebauer EA, European Association for Endoscopic Surgery (EAES) (2011) Laparoscopic extraperitoneal rectal cancer surgery: the clinical practice guidelines of the European Association for Endoscopic Surgery (EAES). Surg Endosc 25:2423–2440

    CAS  PubMed  Google Scholar 

  2. Monson JR, Weiser MR, Buie WD, Chang GJ, Rafferty JF, Buie WD, Rafferty J, Standards Practice Task Force of the American Society of Colon and Rectal Surgeons (2013) Practice parameters for the management of rectal cancer (revised). Dis Colon Rectum 56:535–550

    CAS  PubMed  Google Scholar 

  3. van de Velde CJ, Boelens PG, Borras JM, Coebergh JW, Cervantes A, Blomqvist L, Beets-Tan RG, van den Broek CB, Brown G, Van Cutsem E, Espin E, Haustermans K, Glimelius B, Iversen LH, van Krieken JH, Marijnen CA, Henning G, Gore-Booth J, Meldolesi E, Mroczkowski P, Nagtegaal I, Naredi P, Ortiz H, Påhlman L, Quirke P, Rödel C, Roth A, Rutten H, Schmoll HJ, Smith JJ, Tanis PJ, Taylor C, Wibe A, Wiggers T, Gambacorta MA, Aristei C, Valentini V (2014) EURECCA colorectal: multidisciplinary management: European consensus conference colon and rectum. Eur J Cancer 50:1.e1–1.e34

    Google Scholar 

  4. Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD (1985) Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology 89:328–336

    CAS  PubMed  Google Scholar 

  5. Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y (1995) Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 38:1286–1295

    CAS  PubMed  Google Scholar 

  6. Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, Kumamoto T, Ishiguro S, Kato Y, Shimoda T, Iwashita A, Ajioka Y, Watanabe H, Watanabe T, Muto T, Nagasako K (2004) Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol 39:534–543

    PubMed  Google Scholar 

  7. Participants in the Paris Workshop (2003) The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 58:S3–S43

    Google Scholar 

  8. Endoscopic Classification Review Group (2005) Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 37:570–578

    Google Scholar 

  9. Kudo S, Lambert R, Allen JI, Fujii H, Fujii T, Kashida H, Matsuda T, Mori M, Saito H, Shimoda T, Tanaka S, Watanabe H, Sung JJ, Feld AD, Inadomi JM, O’Brien MJ, Lieberman DA, Ransohoff DF, Soetikno RM, Triadafilopoulos G, Zauber A, Teixeira CR, Rey JF, Jaramillo E, Rubio CA, Van Gossum A, Jung M, Vieth M, Jass JR, Hurlstone PD (2008) Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc 68:S3–S47

    PubMed  Google Scholar 

  10. Lambert R, Kudo SE, Vieth M, Allen JI, Fujii H, Fujii T, Kashida H, Matsuda T, Mori M, Saito H, Shimoda T, Tanaka S, Watanabe H, Sung JJ, Feld AD, Inadomi JM, O’Brien MJ, Lieberman DA, Ransohoff DF, Soetikno RM, Zauber A, Teixeira CR, Rey JF, Jaramillo E, Rubio CA, Van Gossum A, Jung M, Jass JR, Triadafilopoulos G (2009) Pragmatic classification of superficial neoplastic colorectal lesions. Gastrointest Endosc 70(6):1182–1199

    PubMed  Google Scholar 

  11. Kudo S (1993) Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 25:455–461

    CAS  PubMed  Google Scholar 

  12. Uraoka T, Saito Y, Matsuda T, Ikehara H, Gotoda T, Saito D, Fujii T (2006) Endoscopic indications for endoscopic mucosal resection of laterally spreading tumours in the colorectum. Gut 55:1592–1597

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Petrelli NJ, Létourneau R, Weber T, Nava ME, Rodriguez-Bigas M (1999) Accuracy of biopsy and cytology for the preoperative diagnosis of colorectal adenocarcinoma. J Surg Oncol 71:46–49

    CAS  PubMed  Google Scholar 

  14. Takahashi K, Mori T, Yasuno M (2000) Histologic grade of metastatic lymph nodes an prognosis of rectal cancer. Dis Colon Rectum 43:S40–S46

    CAS  PubMed  Google Scholar 

  15. Gondal G, Grotmol T, Hofstad B, Bretthauer M, Eide TJ, Hoff G (2005) Biopsy of colorectal polyps is not adequate for grading of neoplasia. Endoscopy 37:1193–1197

    CAS  PubMed  Google Scholar 

  16. Absar MS, Haboubi NY (2004) Colonic neoplastic polyps: biopsy is not efficient to exclude malignancy. The Trafford experience. Tech Coloproctol 8(Suppl. 2):s257–s260

    PubMed  Google Scholar 

  17. Moss A, Bourke MJ, Williams SJ, Hourigan LF, Brown G, Tam W, Singh R, Zanati S, Chen RY, Byth K (2011) Endoscopic mucosal resection outcomes and prediction of submucosal cancer from advanced colonic mucosal neoplasia. Gastroenterology 140:1909–1918

    PubMed  Google Scholar 

  18. Kim EK, Han DS, Kim HS (2012) A Biopsy Before the Colorectal ESD—is it Useful? Gastrointest Endosc 75(4S):AB407

    Google Scholar 

  19. Han KS, Sohn DK, Choi DH, Hong CW, Chang HJ, Lim SB, Choi HS, Jeong SY, Park JG (2008) Prolongation of the period between biopsy and EMR can influence the nonlifting sign in endoscopically resectable colorectal cancers. Gastrointest Endosc 67:97–102

    PubMed  Google Scholar 

  20. Fu KI, Sano Y, Kato S, Fujii T, Nagashima F, Yoshino T, Okuno T, Yoshida S, Fujimori T (2004) Chromoendoscopy using indigo-carmine dye-spraying with magnifying observation. Is the most reliable method for differential diagnosis between non-neoplastic and neoplastic colorectal lesions? A prospective study. Endoscopy 36:1089–1093

    PubMed  Google Scholar 

  21. Hewett DG, Kaltenbach T, Sano Y, Tanaka S, Saunders BP, Ponchon T, Soetikno R, Rex DK (2012) Validation of a simple classification system for endoscopic diagnosis of small colorectal polyps using narrow-band imaging. Gastroenterology 143:599–607

    PubMed  Google Scholar 

  22. Hayashi N, Tanaka S, Hewett DG, Kaltenbach TR, Sano Y, Ponchon T, Saunders BP, Rex DK, Soetikno RM (2013) Endoscopic prediction of deep submucosal invasive carcinoma: validation of the narrow-band imaging international colorectal endoscopic (NICE) classification. Gastrointest Endosc 78:625–632

    PubMed  Google Scholar 

  23. Uraoka T, Saito Y, Ikematsu H, Yamamoto K, Sano Y (2011) Sano’s capillary pattern classification for narrow-band imaging of early colorectal lesions. Dig Endosc 23(Suppl. 1):112–115

    PubMed  Google Scholar 

  24. Katagiri A, Fu KI, Sano Y, Ikematsu H, Horimatsu T, Kaneko K, Muto M, Yoshida S (2008) Narrow band imaging with magnifying colonoscopy as diagnostic tool for predicting histology of early colorectal neoplasia. Aliment Pharmacol Ther 27:1269–1274

    CAS  PubMed  Google Scholar 

  25. Ikematsu H, Matsuda T, Emura F, Saito Y, Uraoka T, Fu KI, Kaneko K, Ochiai A, Fujimori T, Sano Y (2010) Efficacy of capillary pattern type IIIA/IIIB by magnifying narrow band imaging for estimating depth of invasion of early colorectal neoplasms. BMC Gastroenterol 10:33

    PubMed Central  PubMed  Google Scholar 

  26. Kato S, Fu KI, Sano Y, Fujii T, Saito Y, Matsuda T, Koba I, Yoshida S, Fujimori T (2006) Magnifying colonoscopy as a non-biopsy technique for differential diagnosis of non-neoplastic and neoplastic lesions. World J Gastroenterol 12:1416–1420

    PubMed Central  PubMed  Google Scholar 

  27. Emura F, Saito Y, Taniguchi M, Fujii T, Tagawa K, Yamakado M (2007) Further validation of magnifying chromocolonoscopy for differentiating colorectal neoplastic polyps in a health screening center. J Gastroenterol Hepatol 22:1722–1727

    PubMed  Google Scholar 

  28. Matsuda T, Fujii T, Saito Y, Nakajima T, Uraoka T, Kobayashi N, Ikehara H, Ikematsu H, Fu KI, Emura F, Ono A, Sano Y, Shimoda T, Fujimori T (2008) Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol 103:2700–2706

    PubMed  Google Scholar 

  29. Kobayashi N, Saito Y, Sano Y, Uragami N, Michita T, Nasu J, Matsuda T, Fu KI, Fujii T, Fujimori T, Ishikawa T, Saito D (2007) Determining the treatment strategy for colorectal neoplastic lesions: endoscopic assessment or the non-lifting sign for diagnosing invasion depth? Endoscopy 39:701–705

    CAS  PubMed  Google Scholar 

  30. Kudo S, Hirota S, Nakajima T, Hosobe S, Kusaka H, Kobayashi T, Himori M, Yagyuu A (1994) Colorectal tumours and pit pattern. J Clin Pathol 47:880–885

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Kudo S, Tamura S, Nakajima T, Yamano H, Kusaka H, Watanabe H (1996) Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 44:8–14

    CAS  PubMed  Google Scholar 

  32. Bretagnol F, Rullier E, George B, Warren BF, Mortensen NJ (2007) Local therapy for rectal cancer: still controversial? Dis Colon Rectum 50:523–533

    CAS  PubMed  Google Scholar 

  33. Brown G, Davies S, Williams GT, Bourne MW, Newcombe RG, Radcliffe AG, Blethyn J, Dallimore NS, Rees BI, Phillips CJ, Maughan TS (2004) Effectiveness of preoperative staging in rectal cancer: digital rectal examination, endorectal ultrasound or magnetic resonance imaging? Br J Cancer 91:23–29

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Rafaelson SR, Kronberg O, Fenger C (1994) Digital rectal examination and transrectal ultrasonography in staging of rectal cancer. A prospective, blind study. Acta Radiol 35:300–304

    Google Scholar 

  35. Thumbe V, Iqbal M, Bhalerao S (2007) Accuracy of digital rectal examination in the estimation of height of rectal lesions. Tech Coloproctol 11:111–113

    CAS  PubMed  Google Scholar 

  36. Nelson RL, Abcarian H, Prasad ML (1982) Iatrogenic perforation of the colon and rectum. Dis Colon Rectum 25:305–308

    CAS  PubMed  Google Scholar 

  37. Baatrup G, Bolstad M, Mortensen JH (2009) Rigid sigmoidoscopy and MRI are not interchangeable in determining the position of rectal cancers. Eur J Surg Oncol 35:1169–1173

    CAS  PubMed  Google Scholar 

  38. Piscatelli N, Hyman N, Osler T (2005) Localizing colorectal cancer by colonoscopy. Arch Surg 140:932–935

    PubMed  Google Scholar 

  39. Schoellhammer HF, Gregorian AC, Sarkisyan GG, Petrie BA (2008) How important is rigid proctosigmoidoscopy in localizing rectal cancer? Am J Surg 196:904–908

    PubMed  Google Scholar 

  40. Taylor FG, Quirke P, Heald RJ, Moran B, Blomqvist L, Swift I, Sebag-Montefiore DJ, Tekkis P, Brown G, MERCURY Study Group (2011) Preoperative high-resolution magnetic resonance imaging can identify good prognosis stage I, II, and III rectal cancer best managed by surgery alone: a prospective, multicenter, European study. Ann Surg 253:711–719

    PubMed  Google Scholar 

  41. Adloff M, Arnaud JP, Bergamaschi R, Schloegel M (1989) Synchronous carcinoma of the colon and rectum: prognostic and therapeutic implications. Am J Surg 157:299–302

    CAS  PubMed  Google Scholar 

  42. Isler JT, Brown PC, Lewis FG, Billingham RP (1987) The role of preoperative colonoscopy in colorectal cancer. Dis Colon Rectum 30:435–439

    CAS  PubMed  Google Scholar 

  43. Barillari P, Ramacciato G, De Angelis R, Gozzo P, Indinnimeo M, Valabrega S, Aurello P, Fegiz G (1990) Effect of preoperative colonoscopy on the incidence of synchronous and metachronous neoplasms. Acta Chir Scand 156:163–166

    CAS  PubMed  Google Scholar 

  44. Chen HS, Sheen-Chen SM (2000) Synchronous and ‘‘early’’ metachronous colorectal adenocarcinoma: analysis of prognosis and current trends. Dis Colon Rectum 43:1093–1099

    CAS  PubMed  Google Scholar 

  45. Fujii T, Rembacken BJ, Dixon MF, Yoshida S, Axon ATR (1998) Flat adenomas in the United Kingdom: are treatable cancers being missed? Endoscopy 30:437–443

    CAS  PubMed  Google Scholar 

  46. Rembacken BJ, Fujii T, Cairns A, Dixon MF, Yoshida S, Chalmers DM, Axon AT (2000) Flat and depressed colonic neoplasms: a prospective study of 1000 colonoscopies in the UK. Lancet 355:1211–1214

    CAS  PubMed  Google Scholar 

  47. Neri E, Giusti P, Battolla L, Vagli P, Boraschi P, Lencioni R, Caramella D, Bartolozzi C (2002) Colorectal cancer: role of CT colonography in preoperative evaluation after incomplete colonoscopy. Radiology 223:615–619

    PubMed  Google Scholar 

  48. Marusch F, Koch A, Schmidt U, Zippel R, Kuhn R, Wolff S, Pross M, Wierth A, Gastinger I, Lippert H (2002) Routine use of transrectal ultrasound in rectal carcinoma: results of a prospective multicenter study. Endoscopy 34:385–390

    CAS  PubMed  Google Scholar 

  49. Ptok H, Marusch F, Meyer F, Wendling P, Wenisch HJ, Sendt W, Manger T, Lippert H, Gastinger I (2006) Feasibility and accuracy of TRUS in the pre-treatment staging for rectal carcinoma in general practice. Eur J Surg Oncol 32:420–425

    CAS  PubMed  Google Scholar 

  50. Garcia-Aguilar J, Pollack J, Lee SH, de Anda EH, Mellgren A, Wong WD, Finne CO, Rothenberger DA, Madoff RD (2002) Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum 45:10–15

    PubMed  Google Scholar 

  51. Haji A, Adams K, Bjarnason I, Papagrigoriadis S (2014) High-frequency mini probe ultrasound before endoscopic resection of colorectal polyps–is it useful? Dis Colon Rectum 57:378–382

    PubMed  Google Scholar 

  52. Engelen SM, Maas M, Lahaye MJ, Leijtens JW, van Berlo CL, Jansen RL, Breukink SO, Dejong CH, van de Velde CJ, Beets-Tan RG, Beets GL (2013) Modern multidisciplinary treatment of rectal cancer based on staging with magnetic resonance imaging leads to excellent local control, but distant control remains a challenge. Eur J Cancer 49:2311–2320

    CAS  PubMed  Google Scholar 

  53. Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G (2008) Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg 95:229–236

    CAS  PubMed  Google Scholar 

  54. Beets-Tan RG, Beets GL, Vliegen RF, Kessels AG, Van Boven H, De Bruine A, von Meyenfeldt MF, Baeten CG, van Engelshoven JM (2001) Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery. Lancet 357:497–504

    CAS  PubMed  Google Scholar 

  55. Lambregts DM, Beets GL, Maas M, Kessels AG, Bakers FC, Cappendijk VC, Engelen SM, Lahaye MJ, de Bruïne AP, Lammering G, Leiner T, Verwoerd JL, Wildberger JE, Beets-Tan RG (2011) Accuracy of gadofosveset-enhanced MRI for nodal staging and restaging in rectal cancer. Ann Surg 253:539–545

    PubMed  Google Scholar 

  56. Brown G, Richards CJ, Bourne MW, Newcombe RG, Radcliffe AG, Dallimore NS, Williams GT (2003) Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology 227:371–377

    PubMed  Google Scholar 

  57. Wolberink SV, Beets-Tan RG, de Haas-Kock DF, van de Jagt EJ, Span MM, Wiggers T (2009) Multislice CT as a primary screening tool for the prediction of an involved mesorectal fascia and distant metastases in primary rectal cancer: a multicenter study. Dis Colon Rectum 52:928–934

    PubMed  Google Scholar 

  58. Brush J, Boyd K, Chappell F, Crawford F, Dozier M, Fenwick E, Glanville J, McIntosh H, Renehan A, Weller D, Dunlop M (2011) The value of FDG positron emission tomography/computerised tomography (PET/CT) in pre-operative staging of colorectal cancer: a systematic review and economic evaluation. Health Technol Assess 15:1–4

    CAS  PubMed  Google Scholar 

  59. Beets-Tan RG, Lambregts DM, Maas M, Bipat S, Barbaro B, Caseiro-Alves F, Curvo-Semedo L, Fenlon HM, Gollub MJ, Gourtsoyianni S, Halligan S, Hoeffel C, Kim SH, Laghi A, Maier A, Rafaelsen SR, Stoker J, Taylor SA, Torkzad MR, Blomqvist L (2013) Magnetic resonance imaging for the clinical management of rectal cancer patients: recommendations from the 2012 European Society of Gastrointestinal and Abdominal Radiology (ESGAR) consensus meeting. Eur Radiol 23(9):2522–2531

    PubMed  Google Scholar 

  60. Tominaga K, Fujinuma S, Endo T, Saida Y, Takahashi K, Maetani I (2009) Efficacy of the revised Vienna classification for diagnosing colorectal epithelial neoplasias. World J Gastroenterol 15:2351–2356

    PubMed Central  PubMed  Google Scholar 

  61. Sohn DK, Chang HJ, Park JW, Choi DH, Han KS, Hong CW, Jung KH, Kim DY, Lim SB, Choi HS, Jeong S-Y (2007) Histopathological risk factors for lymph node metastasis in submucosal invasive colorectal carcinoma of pedunculated or semi-pedunculated type. J Clin Pathol 60:912–915

    PubMed Central  PubMed  Google Scholar 

  62. Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H, Kitano S (2007) Risk factors for occult lymph node metastasis of colorectal cancer invading the submucosa and indications for endoscopic mucosal resection. Dis Colon Rectum 50:1370–1376

    PubMed  Google Scholar 

  63. Oh-e H, Tanaka S, Kitadai Y, Shimamoto F, Yoshihara M, Haruma K (2001) Angiogenesis at the site of deepest penetration predicts lymph node metastasis of submucosal colorectal cancer. Dis Colon Rectum 44:1129–1136

    CAS  PubMed  Google Scholar 

  64. Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, Matsukuma S, Kanai T, Kurihara H, Ozawa K, Yoshimura K, Bekku S (2004) Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 127:385–394

    PubMed  Google Scholar 

  65. Cooper HS, Deppisch LM, Kahan EI, Lev R, Manley PN, Pascal RR, Qizilbash AH, Rickert RR, Silverman JF, Wirman JA (1988) Pathology of the malignant colorectal polyp. Hum Pathol 29:15–26

    Google Scholar 

  66. Coverlizza S, Risio M, Ferrari A, Fenoglio-Preiser CM, Rossini FP (1989) Colorectal adenomas containing invasive carcinoma. Pathologic assessment of lymph node metastatic potential. Cancer 64:1937–1947

    CAS  PubMed  Google Scholar 

  67. Glasgow SC, Bleier JI, Burgart LJ, Finne CO, Lowry AC (2012) Meta-analysis of histopathological features of primary colorectal cancers that predict lymph node metastases. J Gastrointest Surg 16:1019–1028

    PubMed  Google Scholar 

  68. Bosch SL, Teerenstra S, de Wilt JH, Cunningham C, Nagtegaal ID (2013) Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 45:827–834

    PubMed  Google Scholar 

  69. Quirke P, Risio M, Lambert R, von Karsa L, Vieth M (2011) QA in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 458:1–19

    PubMed Central  PubMed  Google Scholar 

  70. Ueno H, Hashiguchi Y, Kajiwara Y, Shinto E, Shimazaki H, Kurihara H, Mochizuk H, Hase K (2010) Proposed objective criteria for “grade 3” in early invasive colorectal cancer. Am J Clin Pathol 134:312–322

    PubMed  Google Scholar 

  71. Suzuki A, Togashi K, Nokubi M, Koinuma K, Miyakura Y, Hisanaga H, Lefor AT, Yasuda Y (2009) Evaluation of venous invasion by Elastica van Gieson stain and tumor budding predicts local and distant metastases in patients with T1 stage colorectal cancer. Am J Surg Pathol 33:1601–1607

    PubMed  Google Scholar 

  72. Hase K, Shatney CH, Mochizuki H, Johnson DL, Tamakuma S, Vierra M, Trollope M (1995) Long-term results of curative resection of “minimally invasive” colorectal cancer. Dis Colon Rectum 38:19–26

    CAS  PubMed  Google Scholar 

  73. Puppa G, Senore C, Sheahan K, Vieth M, Lugli A, Zlobec I, Pecori S, Wang LM, Langner C, Mitomi H, Nakamura T, Watanabe M, Ueno H, Chasle J, Conley SA, Herlin P, Lauwers GY, Risio M (2012) Diagnostic reproducibility of tumor budding in colorectal cancer: a multicentre, multinational study using virtual microscopy. Histopathology 61:562–575

    PubMed  Google Scholar 

  74. Kodama Y, Inokuchi K, Soejima K, Matsusaka T, Okamura T (1983) Growth patterns and prognosis in early gastric carcinoma. Superficially spreading and penetrating growth types. Cancer 51:320–326

    CAS  PubMed  Google Scholar 

  75. Tateishi Y, Nakanishi Y, Taniguchi H, Shimoda T, Umemura S (2010) Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol 23:1068–1072

    PubMed  Google Scholar 

  76. Leong KJ, Beggs A, James J, Morton DG, Matthews GM, Bach SP (2014) Biomarker-based treatment selection in early-stage rectal cancer to promote organ preservation. Br J Surg 101:1299–1309

    PubMed Central  CAS  PubMed  Google Scholar 

  77. Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR (2002) Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 45:200–206

    PubMed  Google Scholar 

  78. Yamamoto S, Watanabe M, Hasegawa H, Baba H, Yoshinare K, Shiraishi J, Kitajima M (2004) The risk of lymph node metastasis in T1 colorectal carcinoma. Hepatogastroenterology 51:998–1000

    PubMed  Google Scholar 

  79. Smith KJE, Jones PF, Burke DA, Treanor D, Finan PJ, Quirke P (2011) Lymphatic vessel distribution in the mucosa and submucosa and potential implications for T1 colorectal tumors. Dis Colon Rectum 54:35–40

    PubMed  Google Scholar 

  80. Saraste D, Gunnarsson U, Janson M (2013) Predicting lymph node metastases in early rectal cancer. Eur J Cancer 49:1104–1108

    PubMed  Google Scholar 

  81. Casadesus D (2009) Surgical resection of rectal adenoma: a rapid review. World J Gastroenterol 15:3844–3851

    Google Scholar 

  82. Suppiah A, Maslekar S, Alabi A, Hartley JE, Monson JR (2008) Transanal endoscopic microsurgery in early rectal cancer: time for a trial? Colorectal Dis 10:314–327

    CAS  PubMed  Google Scholar 

  83. Gavagan JA, Whiteford MH, Swanstrom LL (2004) Full-thickness intraperitoneal excision by transanal endoscopic microsurgery does not increase short-term complications. Am J Surg 187:630–634

    PubMed  Google Scholar 

  84. Ramwell A, Evans J, Bignell M, Mathias J, Simson J (2009) The creation of a peritoneal defect in transanal endoscopic microsurgery does not increase complications. Colorectal Dis 11:964–966

    CAS  PubMed  Google Scholar 

  85. Baatrup G, Borschitz T, Cunningham C, Qvist N (2009) Perforation into the peritoneal cavity during transanal endoscopic microsurgery for rectal cancer is not associated with major complications or oncological compromise. Surg Endosc 23:2680–2683

    PubMed  Google Scholar 

  86. Morino M, Allaix ME, Famiglietti F, Caldart M, Arezzo A (2013) Does peritoneal perforation affect short- and long-term outcomes after transanal endoscopic microsurgery? Surg Endosc 27:181–188

    PubMed  Google Scholar 

  87. Eyvazzadeh DJ, Lee JT, Madoff RD, Mellgren AF, Finne CO (2014) Outcomes after transanal endoscopic microsurgery with intraperitoneal anastomosis. Dis Colon Rectum 57:438–441

    PubMed  Google Scholar 

  88. Marks JH, Frenkel JL, Greenleaf CE, D’Andrea AP (2014) Transanal endoscopic microsurgery with entrance into the peritoneal cavity: is it safe? Dis Colon Rectum 57:1176–1182

    PubMed  Google Scholar 

  89. Bach SP, Hill J, Monson JR, Simson JN, Lane L, Merrie A, Warren B, Mortensen NJ, Association of Coloproctology of Great Britain and Ireland Transanal Endoscopic Microsurgery (TEM) Collaboration (2009) A predictive model for local recurrence after transanal endoscopic microsurgery for rectal cancer. Br J Surg 96:280–290

    CAS  PubMed  Google Scholar 

  90. Morino M, Allaix ME, Caldart M, Scozzari G, Arezzo A (2011) Risk factors for recurrence after transanal endoscopic microsurgery for rectal malignant neoplasm. Surg Endosc 25:3683–3690

    PubMed  Google Scholar 

  91. Peng J, Chen W, Sheng W, Xu Y, Cai G, Huang D, Cai S (2011) Oncological outcome of T1 rectal cancer undergoing standard resection and local excision. Colorectal Dis 13:e14–e19

    CAS  PubMed  Google Scholar 

  92. Greenberg JA, Shibata D, Herndon JE 2nd, Steele GD Jr, Mayer R, Bleday R (2008) Local excision of distal rectal cancer: an update of cancer and leukemia group B 8984. Dis Colon Rectum 51:1185–1191

    PubMed  Google Scholar 

  93. Borschitz T, Wachtlin D, Möhler M, Schmidberger H, Junginger T (2008) Neoadjuvant chemoradiation and local excision for T2–3 rectal cancer. Ann Surg Oncol 15:712–720

    PubMed  Google Scholar 

  94. Lezoche E, Baldarelli M, Lezoche G, Paganini AM, Gesuita R, Guerrieri M (2012) Randomized clinical trial of endoluminal locoregional resection versus laparoscopic total mesorectal excision for T2 rectal cancer after neoadjuvant therapy. Br J Surg 99:1211–1218

    CAS  PubMed  Google Scholar 

  95. Suzuki T, Sadahiro S, Mukoyama S, Ishikawa K, Yasuda S, Tajima T, Makuuchi H, Murayama C (2003) Risk of lymph node and distant metastases in patients with early invasive colorectal cancer classified as Haggitt’s level 4. Dis Colon Rectum 46:203–208

    PubMed  Google Scholar 

  96. Choi PW, Yu CS, Jang SJ, Jung SH, Kim HC, Kim JC (2008) Risk factors for lymph node metastasis in submucosal invasion colorectal cancer. World J Surg 32:2089–2094

    PubMed  Google Scholar 

  97. Kaneko I, Tanaka S, Oka S, Kawamura T, Hiyama T, Ito M, Yoshihara M, Shimamoto F, Chayama K (2007) Lymphatic vessel density at the site of deepest penetration as a predictor of lymph node metastasis in submucosal colorectal cancer. Dis Colon Rectum 50:13–21

    PubMed  Google Scholar 

  98. Sakuragi M, Togashiki K, Konishi F, Koinuma K, Kawanura K, Okada M, Nagai H (2003) Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum 46:1626–1632

    PubMed  Google Scholar 

  99. Tanaka S, Yokota T, Saito D, Okamoto S, Oguro Y, Yoshida S (1995) Clinicopathologic features of early rectal carcinoma and indications for endoscopic treatment. Dis Colon Rectum 39:959–963

    Google Scholar 

  100. Tominaga K, Nakanishi Y, Nimura S, Yoshimura K, Sakai Y, Shimoda T (2005) Predictive histopathologic factors for lymph node metastasis in patients with nonpedunculated submucosal invasive colorectal carcinoma. Dis Colon Rectum 48:92–100

    PubMed  Google Scholar 

  101. Gopaul D, Belliveau P, Vuong T, Trudel J, Vasilevsky CA, Corns R, Gordon PH (2004) Outcomes of local excision of rectal carcinoma. Dis Colon Rectum 47:1780–1788

    CAS  PubMed  Google Scholar 

  102. Gao JD, Shao YF, Bi JJ, Shi SS, Liang J, Hu YH (2003) Local excision carcinoma in early stage. World J Gastroenterol 9:871–873

    PubMed  Google Scholar 

  103. Bleday R, Breen E, Jessup JM, Burgess A, Sentovich SM, Steel G Jr (1997) Prospective evaluation of local excision for small rectal cancers. Dis Colon Rectum 40:388–392

    CAS  PubMed  Google Scholar 

  104. Watanabe T, Itabashi M, Shimada Y, Tanaka S, Ito Y, Ajioka Y, Hamaguchi T, Hyodo I, Igarashi M, Ishida H, Ishiguro M, Kanemitsu Y, Kokudo N, Muro K, Ochiai A, Oguchi M, Ohkura Y, Saito Y, Sakai Y, Ueno H, Yoshino T, Fujimori T, Koinuma N, Morita T, Nishimura G, Sakata Y, Takahashi K, Takiuchi H, Tsuruta O, Yamaguchi T, Yoshida M, Yamaguchi N, Kotake K, Sugihara K, Japanese Society for Cancer of the Colon and Rectum (2012) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol 17:1–29

    PubMed  Google Scholar 

  105. Puli SR, Bechtold ML, Reddy JB, Choudhary A, Antillon MR, Brugge WR (2009) How good isendoscopic ultrasound in differentiating various T stages of rectal cancer? Meta-analysis and systematic review. Ann Surg Oncol 16:254–265

    PubMed  Google Scholar 

  106. Marusch F, Ptok H, Sahm M, Schmidt U, Ridwelski K, Gastinger I, Lippert H (2011) Endorectal ultrasound in rectal carcinoma—do the literature results really correspond to the realities of routine clinical care? Endoscopy 43:425–431

    CAS  PubMed  Google Scholar 

  107. Ashraf S, Hompes R, Slater A, Lindsey I, Bach S, Mortensen N, Cunningham C, Association of Coloproctology of Great Britain and Ireland Transanal Endoscopic Microsurgery (TEM) Collaboration (2012) A critical appraisal of endorectal ultrasound and transanal endoscopic microsurgery and decision-making in early rectal cancer. Colorectal Dis 14:821–826

    CAS  PubMed  Google Scholar 

  108. Baron PL, Enker WE, Zakowski MF, Urmacher C (1995) Immediate vs. salvage resection after local treatment for early rectal cancer. Dis Colon Rectum 38:177–181

    CAS  PubMed  Google Scholar 

  109. Hahnloser D, Wolff BG, Larson DW, Ping J, Nivatvongs S (2005) Immediate radical resection after local excision of rectal cancer: an oncologic compromise? Dis Colon Rectum 48:429–437

    PubMed  Google Scholar 

  110. Borschitz T, Heintz A, Junginger T (2006) The influence of histopathologic criteria on the long-term prognosis of locally excised pT1 rectal carcinomas: results of local excision (transanal endoscopic microsurgery) and immediate reoperation. Dis Colon Rectum 49:1492–1506

    PubMed  Google Scholar 

  111. Lee WY, Lee WS, Yun SH, Shin SH, Chun HK (2007) Decision for salvage treatment after transanal endoscopic microsurgery. Surg Endosc 21:975–979

    PubMed  Google Scholar 

  112. Floyd ND, Saclarides TJ (2006) Transanal endoscopic microsurgical resection of pT1 rectal tumors. Dis Colon Rectum 49:164–168

    PubMed  Google Scholar 

  113. Borschitz T, Heintz A, Junginger T (2007) Transanal endoscopic microsurgical excision of pT2 rectal cancer: results and possible indications. Dis Colon Rectum 50:292–301

    PubMed  Google Scholar 

  114. Gagliardi G, Newton TR, Bailey HR (2013) Local excision of rectal cancer followed by radical surgery because of poor prognostic features does not compromise the long term oncologic outcome. Colorectal Dis 15:e659–e664

    CAS  PubMed  Google Scholar 

  115. Russell AH, Harris J, Rosenberg PJ, Sause WT, Fisher BJ, Hoffman JP, Kraybill WG, Byhardt RW (2000) Anal sphincter conservation for patients with adenocarcinoma of the distal rectum: long-term results of radiation therapy oncology group protocol 89-02. Int J Radiat Oncol Biol Phys 46(2):313–322

    CAS  PubMed  Google Scholar 

  116. Chakravarti A, Compton CC, Shellito PC, Wood WC, Landry J, Machuta SR, Kaufman D, Ancukiewicz M, Willett CG (1999) Long-term follow-up of patients with rectal cancer managed by local excision with and without adjuvant irradiation. Ann Surg 230:49–54

    PubMed Central  CAS  PubMed  Google Scholar 

  117. Nakajima T, Saito Y, Tanaka S, Iishi H, Kudo SE, Ikematsu H, Igarashi M, Saitoh Y, Inoue Y, Kobayashi K, Hisasbe T, Matsuda T, Ishikawa H, Sugihara K (2013) Current status of endoscopic resection strategy for large, early colorectal neoplasia in Japan. Surg Endosc 27:3262–3270

    PubMed  Google Scholar 

  118. Saito Y, Uraoka T, Yamaguchi Y, Hotta K, Sakamoto N, Ikematsu H, Fukuzawa M, Kobayashi N, Nasu J, Michida T, Yoshida S, Ikehara H, Otake Y, Nakajima T, Matsuda T, Saito D (2010) A prospective, multicenter study of 1111 colorectal endoscopic submucosal dissections (with video). Gastrointest Endosc 72:1217–1225

    PubMed  Google Scholar 

  119. Kiriyama S, Saito Y, Matsuda T, Nakajima T, Mashimo Y, Joeng HK, Moriya Y, Kuwano H (2011) Comparing endoscopic submucosal dissection with transanal resection for non-invasive rectal tumor: a retrospective study. J Gastroenterol Hepatol 26:1028–1033

    PubMed  Google Scholar 

  120. Kiriyama S, Saito Y, Yamamoto S, Soetikno R, Matsuda T, Nakajima T, Kuwano H (2012) Comparison of endoscopic submucosal dissection with laparoscopic-assisted colorectal surgery for early-stage colorectal cancer: a retrospective analysis. Endoscopy 44:1024–1030

    CAS  PubMed  Google Scholar 

  121. Saito Y, Fukuzawa M, Matsuda T, Fukunaga S, Sakamoto T, Uraoka T, Nakajima T, Ikehara H, Fu KI, Itoi T, Fujii T (2010) Clinical outcome of endoscopic submucosal dissection versus endoscopic mucosal resection of large colorectal tumors as determined by curative resection. Surg Endosc 24:343–352

    PubMed  Google Scholar 

  122. Allaix ME, Arezzo A, Arolfo S, Caldart M, Rebecchi F, Morino M (2013) Transanal endoscopic microsurgery for rectal neoplasms. How I do it. J Gastrointest Surg 17:586–592

    PubMed  Google Scholar 

  123. Lee TG, Lee SJ (2014) Transanal single-port microsurgery for rectal tumors: minimal invasive surgery under spinal anesthesia. Surg Endosc 28:271–280

    PubMed  Google Scholar 

  124. Barendse RM, Dijkgraaf MG, Rolf UR, Bijnen AB, Consten EC, Hoff C, Dekker E, Fockens P, Bemelman WA, de Graaf EJ (2013) Colorectal surgeons’ learning curve of transanal endoscopic microsurgery. Surg Endosc 27:3591–3602

    PubMed  Google Scholar 

  125. Moore JS, Cataldo PA, Osler T, Hyman NH (2008) Transanal endoscopic microsurgery is more effective than traditional transanal excision for resection of rectal masses. Dis Colon Rectum 51:1026–1031

    PubMed  Google Scholar 

  126. de Graaf EJR, Burger JWA, van Ijsseldijk ALA, Tetteroo GWM, Dawson I, Hop WCJ (2011) Transanal endoscopic microsurgery is superior to transanal excision of rectal adenomas. Colorectal Dis 13:762–767

    PubMed  Google Scholar 

  127. Langer C, Liersch T, Süss M, Siemer A, Markus P, Ghadimi BM, Füzesi L, Becker H (2003) Surgical cure for early rectal carcinoma and large adenoma: transanal endoscopic microsurgery (using ultrasound or electrosurgery) compared to conventional local and radical resection. Int J Colorectal Dis 18:222–229

    CAS  PubMed  Google Scholar 

  128. Christoforidis D, Cho HM, Dixon MR, Mellgren AF, Madoff RD, Finne CO (2009) Transanal endoscopic microsurgery versus conventional transanal excision for patients with early rectal cancer. Ann Surg 249:776–782

    PubMed  Google Scholar 

  129. Rimonda R, Arezzo A, Arolfo S, Salvai A, Morino M (2013) TransAnal minimally invasive surgery (TAMIS) with SILS™ port versus transanal endoscopic microsurgery (TEM): a comparative experimental study. Surg Endosc 27:3762–3768

    PubMed  Google Scholar 

  130. Albert M, Atallah S, deBeche-Adams TC, Izfar S, Larach SW (2013) Transanal minimally invasive surgery (TAMIS) for local excision of benign neoplasms and early-stage rectal cancer: efficacy and outcomes in the first 50 patients. Dis Colon Rectum 56:301–307

    PubMed  Google Scholar 

  131. Park SU, Min YW, Shin JU, Choi JH, Kim YH, Kim JJ, Cho YB, Kim HC, Yun SH, Lee WY, Chun HK, Chang DK (2012) Endoscopic submucosal dissection or transanal endoscopic microsurgery for nonpolypoid rectal high grade dysplasia and submucosa-invading rectal cancer. Endoscopy 44:1031–1036

    CAS  PubMed  Google Scholar 

  132. Kawaguti FS, Nahas CS, Marques CF, da Costa Martins B, Retes FA, Medeiros RS, Hayashi T, Wada Y, de Lima MS, Uemura RS, Nahas SC, Kudo SE, Maluf-Filho F (2014) Endoscopic submucosal dissection versus transanal endoscopic microsurgery for the treatment of early rectal cancer. Surg Endosc 28:1173–1179

    PubMed  Google Scholar 

  133. Arezzo A, Passera R, Saito Y, Sakamoto T, Kobayashi N, Sakamoto N, Yoshida N, Naito Y, Fujishiro M, Niimi K, Ohya T, Ohata K, Okamura S, Iizuka S, Takeuchi Y, Uedo N, Fusaroli P, Bonino MA, Verra M, Morino M (2014) Systematic review and meta-analysis of endoscopic submucosal dissection versus transanal endoscopic microsurgery for large noninvasive rectal lesions. Surg Endosc 28:427–438

    PubMed  Google Scholar 

  134. Hoerske C, Weber K, Goehl J, Hohenberger W, Merkel S (2010) Long-term outcomes and quality of life after rectal carcinoma surgery. Br J Surg 97:1295–1303

    CAS  PubMed  Google Scholar 

  135. Morino M, Parini U, Allaix ME, Monasterolo G, Contul RB, Garrone C (2009) Male sexual and urinary function after laparoscopic total mesorectal excision. Surg Endosc 23:1233–1240

    PubMed  Google Scholar 

  136. Marijnen CAM, Kapiteijn E, van de Velde CJ, Martijn H, Steup WH, Wiggers T, Kranenbarg EK, Leer JW, Cooperative Investigators of the Dutch Colorectal Cancer Group (2002) Acute side effects and complications after short-term preoperative radiotherapy combined with total mesorectal excision in primary rectal cancer: report of a multicenter randomized trial. J Clin Oncol 20:817–825

    CAS  PubMed  Google Scholar 

  137. Wallner C, Lange MM, Bonsing BA, Maas CP, Wallace CN, Dabhoiwala NF, Rutten HJ, Lamers WH, Deruiter MC, van de Velde CJ, Cooperative Clinical Investigators of the Dutch Total Mesorectal Excision Trial (2008) Causes of fecal and urinary incontinence after total mesorectal excision for rectal cancer based on cadaveric surgery: a study from the cooperative clinical investigators of the Dutch total mesorectal excision trial. J Clin Oncol 26:4466–4472

    PubMed  Google Scholar 

  138. Hendren SK, O’Connor BI, Liu M, Asano T, Cohen Z, Swallow CJ, Macrae HM, Gryfe R, McLeod RS (2005) Prevalence of male and female sexual dysfunction is high following surgery for rectal cancer. Ann Surg 242:212–223

    PubMed Central  PubMed  Google Scholar 

  139. Ho P, Law WL, Chan SC, Lam CK, Chu KW (2003) Functional outcome following low anterior resection with total mesorectal excision in the elderly. Int J Colorectal Dis 18:230–233

    PubMed  Google Scholar 

  140. 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 (2001) Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 345:638–646

    CAS  PubMed  Google Scholar 

  141. Sauer R, Becker H, Hohenberger W, Rödel C, Wittekind C, Fietkau R, Martus P, Tschmelitsch J, Hager E, Hess CF, Karstens JH, Liersch T, Schmidberger H, Raab R, German Rectal Cancer Study Group (2004) Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 351:1731–1740

    CAS  PubMed  Google Scholar 

  142. Sebag-Montefiore D, Stephens RJ, Steele R, Monson J, Grieve R, Khanna S, Quirke P, Couture J, de Metz C, Myint AS, Bessell E, Griffiths G, Thompson LC, Parmar M (2009) Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCIC-CTG C016): a multicentre, randomised trial. Lancet 373:811–820

    PubMed Central  PubMed  Google Scholar 

  143. Pettersson D, Cedermark B, Holm T, Radu C, Påhlman L, Glimelius B, Martling A (2010) Interim analysis of the Stockholm III trial of preoperative radiotherapy regimens for rectal cancer. Br J Surg 97:580–587

    CAS  PubMed  Google Scholar 

  144. O’Neill BD, Brown G, Heald RJ, Cunningham D, Tait DM (2007) Non-operative treatment after neoadjuvant chemoradiotherapy for rectal cancer. Lancet Oncol 8:625–633

    PubMed  Google Scholar 

  145. Patel UB, Brown G, Rutten H, West N, Sebag-Montefiore D, Glynne-Jones R, Rullier E, Peeters M, Van Cutsem E, Ricci S, Van de Velde C, Kjell P, Quirke P (2012) Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 19:2842–2852

    PubMed  Google Scholar 

  146. Bhangu A, Brown G, Nicholls RJ, Wong J, Darzi A, Tekkis P (2013) Survival outcome of local excision versus radical resection of colon or rectal carcinoma: a surveillance, epidemiology, and end results (SEER) population-based study. Ann Surg 258:563–569

    PubMed  Google Scholar 

  147. Finlayson E, Zhao S, Varma MG (2012) Outcomes after rectal cancer surgery in elderly nursing home residents. Dis Colon Rectum 55:1229–1235

    PubMed  Google Scholar 

  148. Mamidanna R, Almoudaris AM, Faiz O (2012) Is 30-day mortality an appropriate measure of risk in elderly patients undergoing elective colorectal resection? Colorectal Dis 14:1175–1182

    CAS  PubMed  Google Scholar 

  149. Mamidanna R, Eid-Arimoku L, Almoudaris AM, Burns EM, Bottle A, Aylin P, Hanna GB, Faiz O (2012) Poor 1-year survival in elderly patients undergoing nonelective colorectal resection. Dis Colon Rectum 55:788–796

    PubMed  Google Scholar 

  150. Clark AJ, Stockton D, Elder A, Wilson RG, Dunlop MG (2004) Assessment of outcomes after colorectal cancer resection in the elderly as a rationale for screening and early detection. Br J Surg 91:1345–1351

    CAS  PubMed  Google Scholar 

  151. Rutten H, den Dulk M, Lemmens V, Nieuwenhuijzen G, Krijnen P, Jansen-Landheer M, van de Poll Franse L, Coebergh JW, Martijn H, Marijnen C, van de Velde C (2007) Survival of elderly rectal cancer patients not improved: analysis of population based data on the impact of TME surgery. Eur J Cancer 43:2295–2300

    PubMed  Google Scholar 

  152. Lezoche G, Baldarelli M, Guerrieri M, Paganini AM, De Sanctis A, Bartolacci S, Lezoche E (2008) 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 22:352–358

    CAS  PubMed  Google Scholar 

  153. Garcia-Aguilar J, Shi Q, Thomas CR Jr, Chan E, Cataldo P, Marcet J, Medich D, Pigazzi A, Oommen S, Posner MC (2012) A phase II trial of neoadjuvant chemoradiation and local excision for T2N0 rectal cancer: preliminary results of the ACOSOG Z6041 trial. Ann Surg Oncol 19:384–391

    PubMed  Google Scholar 

  154. Marks JH, Valsdottir EB, DeNittis A, Yarandi SS, Newman DA, Nweze I, Mohiuddin M, Marks GJ (2009) Transanal endoscopic microsurgery for the treatment of rectal cancer: comparison of wound complication rates with and without neoadjuvant radiation therapy. Surg Endosc 23:1081–1087

    PubMed  Google Scholar 

  155. Perez RO, Habr-Gama A, São Julião GP, Proscurshim I, Neto AS, Gama-Rodrigues J (2011) Transanal endoscopic microsurgery for residual rectal cancer after neoadjuvant chemoradiation therapy is associated with significant immediate pain and hospital readmission rates. Dis Colon Rectum 54:545–551

    PubMed  Google Scholar 

  156. Bujko K, Richter P, Smith FM, Polkowski W, Szczepkowski M, Rutkowski A, Dziki A, Pietrzak L, Kołodziejczyk M, Kuśnierz J, Gach T, Kulig J, Nawrocki G, Radziszewski J, Wierzbicki R, Kowalska T, Meissner W, Radkowski A, Paprota K, Polkowski M, Rychter A (2013) Preoperative radiotherapy and local excision of rectal cancer with immediate radical re-operation for poor responders: a prospective multicentre study. Radiother Oncol 106:198–205

    PubMed  Google Scholar 

  157. Bökkerink GMJ, de Graaf EJR, Punt CJA, Nagtegaal ID, Rütten H, Nuyttens JJ, van Meerten E, Doornebosch PG, Tanis PJ, Derksen EJ, Dwarkasing RS, Marijnen CA, Cats A, Tollenaar RA, de Hingh IH, Rutten HJ, van der Schelling GP, Ten Tije AJ, Leijtens JW, Lammering G, Beets GL, Aufenacker TJ, Pronk A, Manusama ER, Hoff C, Bremers AJ, Verhoef C, de Wilt JH (2011) The CARTS study: chemoradiation therapy for rectal cancer in the distal rectum followed by organ-sparing transanal endoscopic microsurgery. BMC Surg 11:34

    PubMed Central  PubMed  Google Scholar 

  158. TREC study (2012) http://www.controlled-trials.com/isrctn 14422743. (Accessed 25 Sept 2012)

  159. Wu Y, Wu YY, Zhu BS, Zhao K, Yang XD, Xing CG (2011) TEM and conventional rectal surgery for T1 rectal cancer: a meta-analysis. Hepatogastroenterology 58:364–368

    PubMed  Google Scholar 

  160. Heintz A, Mörschel M, Junginger T (1998) Comparison of results after transanal endoscopic microsurgery and radical resection for T1 carcinoma of the rectum. Surg Endosc 12:1145–1148

    CAS  PubMed  Google Scholar 

  161. Lee W, Lee D, Choi S, Chun H (2003) Transanal endoscopic microsurgery and radical surgery for T1 and T2 rectal cancer. Surg Endosc 17:1283–1287

    CAS  PubMed  Google Scholar 

  162. Bentrem DJ, Okabe S, Wong WD, Guillem JG, Weiser MR, Temple LK, Ben-Porat LS, Minsky BD, Cohen AM, Paty PB (2005) T1 adenocarcinoma of the rectum: transanal excision or radical surgery? Ann Surg 242:472–479

    PubMed Central  PubMed  Google Scholar 

  163. Mellgren A, Sirivongs P, Rothenberger DA, Madoff RD, García-Aguilar J (2000) Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum 43:1064–1071

    CAS  PubMed  Google Scholar 

  164. Friel CM, Cromwell JW, Marra C, Madoff RD, Rothenberger DA, Garcia-Aguílar J (2002) Salvage radical surgery after failed local excision for early rectal cancer. Dis Colon Rectum 45:875–879

    PubMed  Google Scholar 

  165. Levic K, Bulut O, Hesselfeldt P, Bülow S (2013) The outcome of rectal cancer after early salvage TME following TEM compared with primary TME: a case-matched study. Tech Coloproctol 17:397–403

    CAS  PubMed  Google Scholar 

  166. Morino M, Allaix ME, Arolfo S, Arezzo A (2013) Previous transanal endoscopic microsurgery for rectal cancer represents a risk factor for an increased abdominoperineal resection rate. Surg Endosc 27:3315–3321

    PubMed  Google Scholar 

  167. Vennix S, Pelzers L, Bouvy N, Beets GL, Pierie JP, Wiggers T, Breukink S (2014) Laparoscopic versus open total mesorectal excision for rectal cancer. Cochrane Database Syst Rev 4:CD005200. doi:10.1002/14651858.CD005200.pub3

    PubMed  Google Scholar 

  168. Arezzo A, Passera R, Scozzari G, Verra M, Morino M (2013) Laparoscopy for rectal cancer reduces short-term mortality and morbidity: results of a systematic review and meta-analysis. Surg Endosc 27:1485–1502

    PubMed  Google Scholar 

  169. Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, Heath RM, Brown JM, MRC CLASICC Trial Group (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365:1718–1726

    PubMed  Google Scholar 

  170. Kang SB, Park JW, Jeong SY, Nam BH, Choi HS, Kim DW, Lim SB, Lee TG, Kim DY, Kim JS, Chang HJ, Lee HS, Kim SY, Jung KH, Hong YS, Kim JH, Sohn DK, Kim DH, Oh JH (2010) Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol 11:637–645

    PubMed  Google Scholar 

  171. van der Pas MH, Haglind E, Cuesta MA, Fürst A, Lacy AM, Hop WC, Bonjer HJ, COlorectal cancer Laparoscopic or Open Resection II (COLOR II) Study Group (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218

    PubMed  Google Scholar 

  172. Kennedy RH, Francis EA, Wharton R, Blazeby JM, Quirke P, West NP, Dutton SJ (2014) Multicenter randomized controlled trial of conventional versus laparoscopic surgery for colorectal cancer within an enhanced recovery programme: EnROL. J Clin Oncol 32:1804–1811

    PubMed  Google Scholar 

  173. Green BL, Marshall HC, Collinson F, Quirke P, Guillou P, Jayne DG, Brown JM (2013) Long-term follow-up of the medical research council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 100:75–82

    CAS  PubMed  Google Scholar 

  174. Pollett WG, Nicholls RJ (1983) The relationship between the extent of distal clearance and survival and local recurrence rates after curative anterior resection for carcinoma of the rectum. Ann Surg 198:159–163

    PubMed Central  CAS  PubMed  Google Scholar 

  175. Rullier E, Laurent C, Bretagnol F, Rullier A, Vendrely V, Zerbib F (2005) Sphincter-saving resection for all rectal carcinomas: the end of the 2-cm distal rule. Ann Surg 241:465–469

    PubMed Central  PubMed  Google Scholar 

  176. Morris E, Quirke P, Thomas JD, Fairley L, Cottier B, Forman D (2008) Unacceptable variation in abdominoperineal excision rates for rectal cancer: time to intervene? Gut 57:1690–1697

    CAS  PubMed  Google Scholar 

  177. Ricciardi R, Roberts PL, Read TE, Marcello PW, Schoetz DJ, Baxter NN (2010) Variability in reconstructive procedures following rectal cancer surgery in the United States. Dis Colon Rectum 53:874–880

    PubMed  Google Scholar 

  178. Rullier E, Denost Q, Vendrely V, Rullier A, Laurent C (2013) Low rectal cancer: classification and standardization of surgery. Dis Colon Rectum 56:560–567

    PubMed  Google Scholar 

  179. Banerjee AK, Jehle EC, Kreis ME, Schott UG, Claussen CD, Becker HD, Starlinger M, Buess GF (1996) Prospective study of the proctographic and functional consequences of transanal endoscopic microsurgery. Br J Surg 83:211–213

    CAS  PubMed  Google Scholar 

  180. Kennedy ML, Lubowski DZ, King DW (2002) Transanal endoscopic microsurgery excision: is anorectal function compromised? Dis Colon Rectum 45:601–604

    CAS  PubMed  Google Scholar 

  181. Kreis ME, Jehle EC, Haug V, Manncke K, Buess GF, Becker HD, Starlinger MJ (1996) Functional results after transanal endoscopic microsurgery. Dis Colon Rectum 39:1116–1121

    CAS  PubMed  Google Scholar 

  182. Herman RM, Richter P, Walega P, Popiela T (2001) Anorectal sphincter function and rectal barostat study in patients following transanal endoscopic microsurgery. Int J Colorectal Dis 16:370–376

    CAS  PubMed  Google Scholar 

  183. Jin Z, Yin L, Xue L, Lin M, Zheng Q (2010) Anorectal functional results after transanal endoscopic microsurgery in benign and early malignant tumors. World J Surg 34:1128–1132

    PubMed  Google Scholar 

  184. Cataldo PA, O’Brien S, Osler T (2005) Transanal endoscopic microsurgery: a prospective evaluation of functional results. Dis Colon Rectum 48:1366–1371

    PubMed  Google Scholar 

  185. Doornebosch PG, Gosselink MP, Neijenhuis PA, Schouten WR, Tollenaar RA, de Graaf EJ (2008) Impact of transanal endoscopic microsurgery on functional outcome and quality of life. Int J Colorectal Dis 23:709–713

    PubMed Central  CAS  PubMed  Google Scholar 

  186. Allaix ME, Rebecchi F, Giaccone C, Mistrangelo M, Morino M (2011) Long-term functional results and quality of life after transanal endoscopic microsurgery. Br J Surg 98:1635–1643

    CAS  PubMed  Google Scholar 

  187. Gornicki A, Richter P, Polkowski W, Szczepkowski M, Pietrzak L, Kepka L, Rutkowski A, Bujko K (2014) Anorectal and sexual functions after preoperative radiotherapy and full-thickness local excision of rectal cancer. Eur J Surg Oncol 40:723–730

    CAS  PubMed  Google Scholar 

  188. Coco C, Rizzo G, Mattana C, Gambacorta MA, Verbo A, Barbaro B, Vecchio FM, Pafundi DP, Mastromarino MG, Valentini V (2013) Transanal endoscopic microsurgery after neoadjuvant radiochemotherapy for locally advanced extraperitoneal rectal cancer: short-term morbidity and functional outcome. Surg Endosc 27:2860–2867

    CAS  PubMed  Google Scholar 

  189. Juul T, Ahlberg M, Biondo S, Espin E, Jimenez LM, Matzel KE, Palmer GJ, Sauermann A, Trenti L, Zhang W, Laurberg S, Christensen P (2014) Low anterior resection syndrome and quality of life: an international multicenter study. Dis Colon Rectum 57:585–591

    PubMed  Google Scholar 

  190. Doornebosch PG, Tollenaar RA, Gosselink MP, Stassen LP, Dijkhuis CM, Schouten WR, van de Velde CJ, de Graaf EJ (2007) Quality of life after transanal endoscopic microsurgery and total mesorectal excision in early rectal cancer. Colorectal Dis 9:553–558

    CAS  PubMed  Google Scholar 

  191. Lezoche E, Paganini AM, Fabiani B, Balla A, Vestri A, Pescatori L, Scoglio D, D’Ambrosio G, Lezoche G (2014) Quality-of-life impairment after endoluminal locoregional resection and laparoscopic total mesorectal excision. Surg Endosc 28:227–234

    PubMed  Google Scholar 

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Disclosures

Drs. Mario Morino, Mauro Risio, Simon Bach, Regina Beets-Tan, Krzysztof Bujko, Yves Panis, Bjorn Rembacken, Eric Rullier, Yutaka Saito, Tonia Young-Fadok and Marco Ettore Allaix have no conflicts of interest or financial ties to disclose. Dr. Philip Quirke is funded by Yorkshire Cancer Research.

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Authors and Affiliations

  1. Department of Surgical Sciences, University of Torino, Corso A. M. Dogliotti 14, 10126, Turin, Italy

    Mario Morino & Marco Ettore Allaix

  2. Department of Pathology, Candiolo Cancer Institute - FPO, IRCCS, Candiolo, Italy

    Mauro Risio

  3. Academic Department of Surgery, University of Birmingham, Birmingham, UK

    Simon Bach

  4. Department of Radiology, Maastricht University Medical and Oncology Center, Maastricht, The Netherlands

    Regina Beets-Tan

  5. Department of Radiotherapy, M. Sklodowska-Curie Memorial Cancer Centre, Warsaw, Poland

    Krzysztof Bujko

  6. Colorectal Department Beaujon Hospital, University Paris VII, Paris, France

    Yves Panis

  7. Pathology and Tumour Biology, University of Leeds, Leeds, UK

    Philip Quirke

  8. Leeds Teaching Hospitals NHS Trust, Leeds, UK

    Bjorn Rembacken

  9. Department of Surgery, Saint André Hospital, Bordeaux, France

    Eric Rullier

  10. Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan

    Yutaka Saito

  11. Division of Colon and Rectal Surgery, Department of Surgery, Mayo Clinic College of Medicine, Phoenix, AZ, USA

    Tonia Young-Fadok

Authors
  1. Mario Morino
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  2. Mauro Risio
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  3. Simon Bach
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  4. Regina Beets-Tan
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  5. Krzysztof Bujko
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  6. Yves Panis
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  7. Philip Quirke
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  8. Bjorn Rembacken
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  9. Eric Rullier
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  10. Yutaka Saito
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  11. Tonia Young-Fadok
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  12. Marco Ettore Allaix
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Corresponding author

Correspondence to Mario Morino.

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Morino, M., Risio, M., Bach, S. et al. Early rectal cancer: the European Association for Endoscopic Surgery (EAES) clinical consensus conference. Surg Endosc 29, 755–773 (2015). https://doi.org/10.1007/s00464-015-4067-3

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  • DOI: https://doi.org/10.1007/s00464-015-4067-3

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