Shifting concepts in rectal cancer management: A Review of Contemporary Primary Rectal Cancer Treatment Strategies

CA Cancer Journal for Clinicians

Volumn 62, Issue 3, 2012, Pages 173-202

  Kosinski, Lauren ^a   Habr Gama, Angelita ^b   Ludwig, Kirk ^a   Perez, Rodrigo ^b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CAPECITABINE; CARCINOEMBRYONIC ANTIGEN; FLUOROURACIL; FOLINIC ACID; MUCIN; OXALIPLATIN;

ADJUVANT CHEMORADIOTHERAPY; ADJUVANT THERAPY; BRACHYTHERAPY; CANCER CLASSIFICATION; CANCER GRADING; CANCER INVASION; CANCER LOCALIZATION; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER REGRESSION; CANCER SIZE; CANCER STAGING; CANCER SURVIVAL; CLINICAL ASSESSMENT; CLINICAL EXAMINATION; COMORBIDITY; COMPUTER ASSISTED TOMOGRAPHY; DIAGNOSTIC VALUE; DISEASE ACTIVITY; DISEASE FREE SURVIVAL; GASTROINTESTINAL ENDOSCOPY; HUMAN; INTENSITY MODULATED RADIATION THERAPY; INTERMETHOD COMPARISON; INTRAOPERATIVE RADIOTHERAPY; LABORATORY TEST; LAPAROSCOPIC SURGERY; LYMPH NODE METASTASIS; MICROSURGERY; MINIMALLY INVASIVE SURGERY; MULTIMODALITY CANCER THERAPY; NON SPHINCTER SPARING PROCEDURE; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; OVERALL SURVIVAL; POSITRON EMISSION TOMOGRAPHY; PRACTICE GUIDELINE; PRIMARY TUMOR; PRIORITY JOURNAL; PROGNOSIS; RADIATION INJURY; RECTOSCOPY; RECTUM CANCER; RECTUM CARCINOMA; RECTUM RESECTION; RECTUM SURGERY; RECURRENCE RISK; REVIEW; ROBOTICS; SENSITIVITY AND SPECIFICITY; SIGMOIDOSCOPY; SPHINCTER PRESERVING RADICAL RESECTION; STEREOTACTIC BODY RADIATION THERAPY; SURGICAL ANATOMY; SURGICAL APPROACH; SURGICAL TECHNIQUE; THREE DIMENSIONAL IMAGING; TOTAL MESORECTAL EXCISION; TRANSANAL ENDSOCOPIC MICROSURGERY; TREATMENT FAILURE; TREATMENT PLANNING; TREATMENT RESPONSE;

BIOPSY; COMBINED MODALITY THERAPY; DIAGNOSTIC IMAGING; EARLY DIAGNOSIS; HUMANS; NEOPLASM STAGING; OUTCOME ASSESSMENT (HEALTH CARE); PATIENT CARE TEAM; PRACTICE GUIDELINES AS TOPIC; RECTAL NEOPLASMS;

EID: 84860796157     PISSN: 00079235     EISSN: 15424863     Source Type: Journal    
DOI: 10.3322/caac.21138     Document Type: Review

References (195)

1. Eger SA,. Early diagnosis in colon and rectal cancer. CA Cancer J Clin. 1965; 15: 275-277.
2. Burton S, Brown G, Daniels IR, Norman AR, Mason B, Cunningham D,; Royal Marsden Hospital, Colorectal Cancer Network. MRI directed multidisciplinary team preoperative treatment strategy: the way to eliminate positive circumferential margins? Br J Cancer. 2006; 94: 351-357.
3. Palmer G, Martling A, Cedermark B, Holm T,. Preoperative tumour staging with multidisciplinary team assessment improves the outcome in locally advanced primary rectal cancer. Colorectal Dis. 2011; 13: 1361-1369.
4. Nelson H, Petrelli N, Carlin A, et al. National Cancer Institute Expert Panel. Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst. 2001; 93: 583-596.
5. Mohiuddin M, Regine WF, Marks G,. Prognostic significance of tumor fixation of rectal carcinoma. Implications for adjunctive radiation therapy. Cancer. 1996; 78: 717-722.
6. Schoellhammer HF, Gregorian AC, Sarkisyan GG, Petrie BA,. How important is rigid proctosigmoidoscopy in localizing rectal cancer? Am J Surg. 2008; 196: 904-908; discussion 908.
7. Chambers WM, Khan U, Gagliano A, Smith RD, Sheffield J, Nicholls RJ,. Tumour morphology as a predictor of outcome after local excision of rectal cancer. Br J Surg. 2004; 91: 457-459.
8. Leong AF, Seow-Choen F, Tang CL,. Diminutive cancers of the colon and rectum: comparison between flat and polypoid cancers. Int J Colorectal Dis. 1998; 13: 151-153.
9. Rao VS, Ahmad N, Al-Mukhtar A, Stojkovic S, Moore PJ, Ahmad SM,. Comparison of rigid vs flexible sigmoidoscopy in detection of significant anorectal lesions. Colorectal Dis. 2005; 7: 61-64.
10. Kim SH, Milsom JW, Church JM, et al. Perioperative tumor localization for laparoscopic colorectal surgery. Surg Endosc. 1997; 11: 1013-1016.
11. Feingold DL, Addona T, Forde KA, et al. Safety and reliability of tattooing colorectal neoplasms prior to laparoscopic resection. J Gastrointest Surg. 2004; 8: 543-546.
12. Vuong T, Devic S, Podgorsak E,. High dose rate endorectal brachytherapy as a neoadjuvant treatment for patients with resectable rectal cancer. Clin Oncol (R Coll Radiol). 2007; 19: 701-705.
13. Ohdaira T, Konishi F, Nagai H, et al. Intraoperative localization of colorectal tumors in the early stages using a marking clip detector system. Dis Colon Rectum. 1999; 42: 1353-1355.
14. Ohdaira T, Nagai H, Shibusawa H,. Intraoperative localization of early-stage gastrointestinal tumors using a marking clip detector system. Surg Technol Int. 2005; 14: 79-83.
15. American Cancer Society. How is Colorectal Cancer Staged. Available at:. Accessed February 12, 2012.
16. Schaffzin DM, Wong WD,. Endorectal ultrasound in the preoperative evaluation of rectal cancer. Clin Colorectal Cancer. 2004; 4: 124-132.
17. Brown G, Richards CJ, Newcombe RG, et al. Rectal carcinoma: thin-section MR imaging for staging in 28 patients. Radiology. 1999; 211: 215-222.
18. Taylor FG, Swift RI, Blomqvist L, Brown G,. A systematic approach to the interpretation of preoperative staging MRI for rectal cancer. AJR Am J Roentgenol. 2008; 191: 1827-1835.
19. Brown G, Richards CJ, Bourne MW, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003; 227: 371-377.
20. Kim JH, Beets GL, Kim MJ, Kessels AG, Beets-Tan RG,. High-resolution MR imaging for nodal staging in rectal cancer: are there any criteria in addition to the size? Eur J Radiol. 2004; 52: 78-83.
21. Beets-Tan RG, Beets GL, Vliegen RF, et al. Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery. Lancet. 2001; 357: 497-504.
22. Sauer R, Becker H, Hohenberger W, et al. German Rectal Cancer Study Group. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004; 351: 1731-1740.
23. Kwok H, Bissett IP, Hill GL,. Preoperative staging of rectal cancer. Int J Colorectal Dis. 2000; 15: 9-20.
24. Kim JC, Kim HC, Yu CS, et al. Efficacy of 3-dimensional endorectal ultrasonography compared with conventional ultrasonography and computed tomography in preoperative rectal cancer staging. Am J Surg. 2006; 192: 89-97.
25. Muthusamy VR, Chang KJ,. Optimal methods for staging rectal cancer. Clin Cancer Res. 2007; 13 (22 pt 2): 6877s-6884s.
26. Landmann RG, Wong WD, Hoepfl J, et al. Limitations of early rectal cancer nodal staging may explain failure after local excision. Dis Colon Rectum. 2007; 50: 1520-1525.
27. Guillem JG, Diaz-Gonzalez JA, Minsky BD, et al. cT3N0 rectal cancer: potential overtreatment with preoperative chemoradiotherapy is warranted. J Clin Oncol. 2008; 26: 368-373.
28. Brown G, Radcliffe AG, Newcombe RG, Dallimore NS, Bourne MW, Williams GT,. Preoperative assessment of prognostic factors in rectal cancer using high-resolution magnetic resonance imaging. Br J Surg. 2003; 90: 355-364.
29. Quirke P, Steele R, Monson J, et al. MRC CR07/NCIC-CTG CO16 Trial Investigators; NCRI Colorectal Cancer Study Group. Effect of the plane of surgery achieved on local recurrence in patients with operable rectal cancer: a prospective study using data from the MRC CR07 and NCIC-CTG CO16 randomised clinical trial. Lancet. 2009; 373: 821-828.
30. Quirke P, Durdey P, Dixon MF, Williams NS,. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet. 1986; 2: 996-999.
31. MERCURY Study Group. Diagnostic accuracy of preoperative magnetic resonance imaging in predicting curative resection of rectal cancer: prospective observational study. BMJ. 2006; 333: 779.
32. Maizlin ZV, Brown JA, So G, et al. Can CT replace MRI in preoperative assessment of the circumferential resection margin in rectal cancer? Dis Colon Rectum. 2010; 53: 308-314.
33. Vliegen R, Dresen R, Beets G, et al. The accuracy of multi-detector row CT for the assessment of tumor invasion of the mesorectal fascia in primary rectal cancer. Abdom Imaging. 2008; 33: 604-610.
34. Smith NJ, Shihab O, Arnaout A, Swift RI, Brown G,. MRI for detection of extramural vascular invasion in rectal cancer. AJR Am J Roentgenol. 2008; 191: 1517-1522.
35. Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G,. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008; 95: 229-236.
36. Sizer BF, Arulampalam T, Austin R, Lacey N, Menzies D, Motson R,. MRI in predicting curative resection of rectal cancer: defining a "window of opportunity" for laparoscopic surgery. BMJ. 2006; 333: 808-809.
37. American College of Radiology. ACR Appropriateness Criteria. Reston, VA: American College of Radiology; 2007. Available at:. Accessed February 12, 2012.
38. Davey K, Heriot AG, Mackay J, et al. The impact of 18-fluorodeoxyglucose positron emission tomography-computed tomography on the staging and management of primary rectal cancer. Dis Colon Rectum. 2008; 51: 997-1003.
39. Vriens D, de Geus-Oei LF, van der Graaf WT, Oyen WJ,. Tailoring therapy in colorectal cancer by PET-CT. Q J Nucl Med Mol Imaging. 2009; 53: 224-244.
40. Brown G, Davies S, Williams GT, et al. Effectiveness of preoperative staging in rectal cancer: digital rectal examination, endoluminal ultrasound or magnetic resonance imaging? Br J Cancer. 2004; 91: 23-29.
41. Miles WE,. A method of performing abdomino-perineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon (1908). CA Cancer J Clin. 1971; 21: 361-364.
42. Williams NS, Dixon MF, Johnston D,. Reappraisal of the 5 centimetre rule of distal excision for carcinoma of the rectum: a study of distal intramural spread and of patients' survival. Br J Surg. 1983; 70: 150-154.
43. Heald RJ, Ryall R,. Recurrent cancer after restorative resection of the rectum. Br Med J (Clin Res Ed) 1982; 284: 826-827.
44. Wibe A, Eriksen MT, Syse A, Myrvold HE, Soreide O,; Norwegian Rectal Cancer Group. Total mesorectal excision for rectal cancer-what can be achieved by a national audit? Colorectal Dis. 2003; 5: 471-477.
45. Martling A, Holm T, Rutqvist LE, et al. Impact of a surgical training programme on rectal cancer outcomes in Stockholm. Br J Surg. 2005; 92: 225-229.
46. Adam IJ, Mohamdee MO, Martin IG, et al. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet. 1994; 344: 707-711.
47. Birbeck KF, Macklin CP, Tiffin NJ, et al. Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg. 2002; 235: 449-457.
48. de Haas-Kock DF, Baeten CG, Jager JJ, et al. Prognostic significance of radial margins of clearance in rectal cancer. Br J Surg. 1996; 83: 781-785.
49. Glynne-Jones R, Anyamene N,. Just how useful an endpoint is complete pathological response after neoadjuvant chemoradiation in rectal cancer? Int J Radiat Oncol Biol Phys. 2006; 66: 319-320.
50. Ng IO, Luk IS, Yuen ST, et al. Surgical lateral clearance in resected rectal carcinomas. A multivariate analysis of clinicopathologic features. Cancer. 1993; 71: 1972-1976.
51. Wolpin BM, Meyerhardt JA, Mamon HJ, Mayer RJ,. Adjuvant treatment of colorectal cancer. CA Cancer J Clin. 2007; 57: 168-185.
52. Sayfan J, Averbuch F, Koltun L, Benyamin N,. Effect of rectal stump washout on the presence of free malignant cells in the rectum during anterior resection for rectal cancer. Dis Colon Rectum. 2000; 43: 1710-1712.
53. Tsunoda A, Shibusawa M, Kamiyama G, Takata M, Choh H, Kusano M,. Iodine absorption after intraoperative bowel irrigation with povidone-iodine. Dis Colon Rectum. 2000; 43: 1127-1132.
54. Shihab OC, Brown G, Daniels IR, Heald RJ, Quirke P, Moran BJ,. Patients with low rectal cancer treated by abdominoperineal excision have worse tumors and higher involved margin rates compared with patients treated by anterior resection. Dis Colon Rectum. 2010; 53: 53-56.
55. Stelzner S, Holm T, Moran BJ, et al. Deep pelvic anatomy revisited for a description of crucial steps in extralevator abdominoperineal excision for rectal cancer. Dis Colon Rectum. 2011; 54: 947-957.
56. 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: 3517-3522.
57. Butler CE, Gundeslioglu AO, Rodriguez-Bigas MA,. Outcomes of immediate vertical rectus abdominis myocutaneous flap reconstruction for irradiated abdominoperineal resection defects. J Am Coll Surg. 2008; 206: 694-703.
58. Lefevre JH, Parc Y, Kerneis S, et al. Abdomino-perineal resection for anal cancer: impact of a vertical rectus abdominis myocutaneous flap on survival, recurrence, morbidity, and wound healing. Ann Surg. 2009; 250: 707-711.
59. Schiessel R, Karner-Hanusch J, Herbst F, Teleky B, Wunderlich M,. Intersphincteric resection for low rectal tumours. Br J Surg. 1994; 81: 1376-1378.
60. Schiessel R, Novi G, Holzer B, et al. Technique and long-term results of intersphincteric resection for low rectal cancer. Dis Colon Rectum. 2005; 48: 1858-1865; discussion 1865-1857.
61. Lee WY, Takahashi T, Pappas T, Mantyh CR, Ludwig KA,. Surgical autonomic denervation results in altered colonic motility: an explanation for low anterior resection syndrome? Surgery. 2008; 143: 778-783.
62. Fazio VW, Zutshi M, Remzi FH, et al. A randomized multicenter trial to compare long-term functional outcome, quality of life, and complications of surgical procedures for low rectal cancers. Ann Surg. 2007; 246: 481-488; discussion 488-490.
63. Ulrich AB, Seiler CM, Z'graggen K, Loffler T, Weitz J, Buchler MW,. Early results from a randomized clinical trial of colon J pouch versus transverse coloplasty pouch after low anterior resection for rectal cancer. Br J Surg. 2008; 95: 1257-1263.
64. Brown CJ, Fenech DS, McLeod RS,. Reconstructive techniques after rectal resection for rectal cancer. Cochrane Database Syst Rev. 2008;(2): CD006040.
65. Matthiessen P, Hallbook O, Rutegard J, Simert G, Sjodahl R,. Defunctioning stoma reduces symptomatic anastomotic leakage after low anterior resection of the rectum for cancer: a randomized multicenter trial. Ann Surg. 2007; 246: 207-214.
66. Montedori A, Cirocchi R, Farinella E, Sciannameo F, Abraha I,. Covering ileo- or colostomy in anterior resection for rectal carcinoma. Cochrane Database Syst Rev. 2010;(5): CD006878.
67. Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004; 350: 2050-2059.
68. Guillou PJ, Quirke P, Thorpe H, et al. MRC CLASICC trial group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005; 365: 1718-1726.
69. Lacy AM, Delgado S, Castells A, et al. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg. 2008; 248: 1-7.
70. Colon Cancer Laparoscopic or Open Resection Study Group, Buunen M, Veldkamp R, et al. Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol. 2009; 10: 44-52.
71. Park IJ, Choi GS, Lim KH, Kang BM, Jun SH,. Multidimensional analysis of the learning curve for laparoscopic colorectal surgery: lessons from 1,000 cases of laparoscopic colorectal surgery. Surg Endosc. 2009; 23: 839-846.
72. Tekkis PP, Senagore AJ, Delaney CP, Fazio VW,. Evaluation of the learning curve in laparoscopic colorectal surgery: comparison of right-sided and left-sided resections. Ann Surg. 2005; 242: 83-91.
73. Schlachta CM, Mamazza J, Seshadri PA, Cadeddu M, Gregoire R, Poulin EC,. Defining a learning curve for laparoscopic colorectal resections. Dis Colon Rectum. 2001; 44: 217-222.
74. Dincler S, Koller MT, Steurer J, Bachmann LM, Christen D, Buchmann P,. Multidimensional analysis of learning curves in laparoscopic sigmoid resection: eight-year results. Dis Colon Rectum. 2003; 46: 1371-1378; discussion 1378-1379.
75. Park IJ, Choi GS, Lim KH, Kang BM, Jun SH,. Multidimensional analysis of the learning curve for laparoscopic resection in rectal cancer. J Gastrointest Surg. 2009; 13: 275-281.
76. Anderson C, Uman G, Pigazzi A,. Oncologic outcomes of laparoscopic surgery for rectal cancer: a systematic review and meta-analysis of the literature. Eur J Surg Oncol. 2008; 34: 1135-1142.
77. Hellan M, Anderson C, Ellenhorn JD, Paz B, Pigazzi A,. Short-term outcomes after robotic-assisted total mesorectal excision for rectal cancer. Ann Surg Oncol. 2007; 14: 3168-3173.
78. deSouza AL, Prasad LM, Marecik SJ, et al. Total mesorectal excision for rectal cancer: the potential advantage of robotic assistance. Dis Colon Rectum. 2010; 53: 1611-1617.
79. Baik SH, Kwon HY, Kim JS, et al. Robotic versus laparoscopic low anterior resection of rectal cancer: short-term outcome of a prospective comparative study. Ann Surg Oncol. 2009; 16: 1480-1487.
80. Choi DJ, Kim SH, Lee PJ, Kim J, Woo SU,. Single-stage totally robotic dissection for rectal cancer surgery: technique and short-term outcome in 50 consecutive patients. Dis Colon Rectum. 2009; 52: 1824-1830.
81. Pigazzi A, Luca F, Patriti A, et al. Multicentric study on robotic tumor-specific mesorectal excision for the treatment of rectal cancer. Ann Surg Oncol. 2010; 17: 1614-1620.
82. American College of Surgeons Oncology Group. ACOSOG Z6051. Available at:. Accessed February 12, 2012.
83. National Institute for Health Research. Robotic Versus Laparascopic Resection for Rectal Cancer. Available at:. Accessed February 12, 2012.
84. Nastro P, Beral D, Hartley J, Monson JR,. Local excision of rectal cancer: review of literature. Dig Surg. 2005; 22: 6-15.
85. Buess G, Hutterer F, Theiss J, Bobel M, Isselhard W, Pichlmaier H,. A system for a transanal endoscopic rectum operation [in German]. Chirurg. 1984; 55: 677-680.
86. Moore JS, Cataldo PA, Osler T, Hyman NH,. Transanal endoscopic microsurgery is more effective than traditional transanal excision for resection of rectal masses. Dis Colon Rectum. 2008; 51: 1026-1030; discussion 1030-1031.
87. Mahmoud N, Madoff R, Rothenberger D, Finne C,. Transanal Endoscopic Microsurgery (TEM) Reduces the Incidence of Positive Margins Compared With Transanal Excision for Rectal Tumors. Paper presented at: American Society of Colorectal Surgeons Annual Meeting; June 2-7, 2001; San Diego, CA.
88. Buess G, Kipfmuller K, Ibald R, et al. Clinical results of transanal endoscopic microsurgery. Surg Endosc. 1988; 2: 245-250.
89. Krook JE, Moertel CG, Gunderson LL, et al. Effective surgical adjuvant therapy for high-risk rectal carcinoma. N Engl J Med. 1991; 324: 709-715.
90. O'Connell MJ, Martenson JA, Wieand HS, et al. Improving adjuvant therapy for rectal cancer by combining protracted-infusion fluorouracil with radiation therapy after curative surgery. N Engl J Med. 1994; 331: 502-507.
91. Thomas PR, Lindblad AS,. Adjuvant postoperative radiotherapy and chemotherapy in rectal carcinoma: a review of the Gastrointestinal Tumor Study Group experience. Radiother Oncol. 1988; 13: 245-252.
92. Fisher B, Wolmark N, Rockette H, et al. Postoperative adjuvant chemotherapy or radiation therapy for rectal cancer: results from NSABP protocol R-01. J Natl Cancer Inst. 1988; 80: 21-29.
93. Wolmark N, Wieand HS, Hyams DM, et al. Randomized trial of postoperative adjuvant chemotherapy with or without radiotherapy for carcinoma of the rectum: National Surgical Adjuvant Breast and Bowel Project Protocol R-02. J Natl Cancer Inst. 2000; 92: 388-396.
94. Mohiuddin M, Kramer S,. Adjuvant radiotherapy-preoperative, postoperative, or both: a proposal for a new approach. Cancer Clin Trials. 1978; 1: 93-97.
95. Rullier A, Laurent C, Capdepont M, et al. Lymph nodes after preoperative chemoradiotherapy for rectal carcinoma: number, status, and impact on survival. Am J Surg Pathol. 2008; 32: 45-50.
96. Pahlman L, Glimelius B,. Pre- or postoperative radiotherapy in rectal and rectosigmoid carcinoma. Report from a randomized multicenter trial. Ann Surg. 1990; 211: 187-195.
97. Cedermark B, Johansson H, Rutqvist LE, Wilking N,. The Stockholm I trial of preoperative short term radiotherapy in operable rectal carcinoma. A prospective randomized trial. Stockholm Colorectal Cancer Study Group. Cancer. 1995; 75: 2269-2275.
98. Improved survival with preoperative radiotherapy in resectable rectal cancer. Swedish Rectal Cancer Trial. N Engl J Med. 1997; 336: 980-987.
99. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001; 345: 638-646.
100. Bujko K, Nowacki MP, Nasierowska-Guttmejer A, Michalski W, Bebenek M, Kryj M,. Long-term results of a randomized trial comparing preoperative short-course radiotherapy with preoperative conventionally fractionated chemoradiation for rectal cancer. Br J Surg. 2006; 93: 1215-1223.
101. Sebag-Montefiore D, Stephens RJ, Steele R, et al. Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCIC-CTG C016): a multicentre, randomised trial. Lancet. 2009; 373: 811-820.
102. Martling A, Holm T, Johansson H, Rutqvist LE, Cedermark B,; Stockholm Colorectal Cancer Study Group. The Stockholm II trial on preoperative radiotherapy in rectal carcinoma: long-term follow-up of a population-based study. Cancer. 2001; 92: 896-902.
103. Ooi BS, Tjandra JJ, Green MD,. Morbidities of adjuvant chemotherapy and radiotherapy for resectable rectal cancer: an overview. Dis Colon Rectum. 1999; 42: 403-418.
104. Birgisson H, Pahlman L, Gunnarsson U, Glimelius B,; Swedish Rectal Cancer Trial Group. Adverse effects of preoperative radiation therapy for rectal cancer: long-term follow-up of the Swedish Rectal Cancer Trial. J Clin Oncol. 2005; 23: 8697-8705.
105. Peeters KC, van de Velde CJ, Leer JW, et al. Late side effects of short-course preoperative radiotherapy combined with total mesorectal excision for rectal cancer: increased bowel dysfunction in irradiated patients-a Dutch colorectal cancer group study. J Clin Oncol. 2005; 23: 6199-6206.
106. Bosset JF, Collette L, Calais G, et al. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med. 2006; 355: 1114-1123.
107. Bosset JF, Calais G, Mineur L, et al. Enhanced tumoricidal effect of chemotherapy with preoperative radiotherapy for rectal cancer: preliminary results-EORTC 22921. J Clin Oncol. 2005; 23: 5620-5627.
108. Roh M, Yothers G, et al. The impact of capecitabine and oxaliplatin in the preoperative multimodality treatment in patients with carcinoma of the rectum: NSABP R-04. J Clin Oncol. 2011; 29.
109. Sanghere P, Wong DW, McConkey CC, Geh JI, Hartley A,. Chemoradiotherapy for rectal cancer: an updated analysis of factors affecting pathological response. Clin Oncol (R Coll Radiol). 2008; 20: 176-186.
110. Gerard JP, Azria D, Gourgou-Bourgade S, et al. Comparison of two neoadjuvant chemoradiotherapy regimens for locally advanced rectal cancer: results of the phase III trial ACCORD 12/0405-Prodige 2. J Clin Oncol. 2010; 28: 1638-1644.
111. Weiss C, Arnold D, Dellas K, et al. Preoperative radiotherapy of advanced rectal cancer with capecitabine and oxaliplatin with or without cetuximab: a pooled analysis of three prospective phase I-II trials. Int J Radiat Oncol Biol Phys. 2010; 78: 472-478.
112. Chau I, Brown G, Cunningham D, et al. Neoadjuvant capecitabine and oxaliplatin followed by synchronous chemoradiation and total mesorectal excision in magnetic resonance imaging-defined poor-risk rectal cancer. J Clin Oncol. 2006; 24: 668-674.
113. Habr-Gama A, Perez RO, Sabbaga J, Nadalin W, Sao Juliao GP, Gama-Rodrigues J,. Increasing the rates of complete response to neoadjuvant chemoradiotherapy for distal rectal cancer: results of a prospective study using additional chemotherapy during the resting period. Dis Colon Rectum. 2009; 52: 1927-1934.
114. Schrag D, Weiser MR, Goodman M, et al. Neoadjuvant FOLFOX-bev, without radiation, for locally advanced rectal cancer. J Clin Oncol. 2010; 28 (suppl): 263s. Abstract 3511.
115. Meyer J, Czito B, Yin FF, Willett C,. Advanced radiation therapy technologies in the treatment of rectal and anal cancer: intensity-modulated photon therapy and proton therapy. Clin Colorectal Cancer. 2007; 6: 348-356.
116. Marijnen CA, Glimelius B,. The role of radiotherapy in rectal cancer. Eur J Cancer. 2002; 38: 943-952.
117. Papillon J, Montbarbon JF, Gerard JP,. Interstitial curietherapy with iridium 192 applied to small cancers of the rectum (author's transl) [in French]. J Radiol Electrol Med Nucl. 1975; 56: 439-442.
118. Gerard JP, Chapet O, Ortholan C, Benezery K, Barbet N, Romestaing P,. French experience with contact X-ray endocavitary radiation for early rectal cancer. Clin Oncol (R Coll Radiol). 2007; 19: 661-673.
119. Willett CG, Czito BG, Tyler DS,. Intraoperative radiation therapy. J Clin Oncol. 2007; 25: 971-977.
120. Kim MS, Choi C, Yoo S, et al. Stereotactic body radiation therapy in patients with pelvic recurrence from rectal carcinoma. Jpn J Clin Oncol. 2008; 38: 695-700.
121. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A, eds. AJCC Cancer Staging Manual. 7th ed. New York: Springer; 2009.
122. Deniaud-Alexandre E, Touboul E, Tiret E, et al. Results of definitive irradiation in a series of 305 epidermoid carcinomas of the anal canal. Int J Radiat Oncol Biol Phys. 2003; 56: 1259-1273.
123. Francois Y, Nemoz CJ, Baulieux J, et al. Influence of the interval between preoperative radiation therapy and surgery on downstaging and on the rate of sphincter-sparing surgery for rectal cancer: the Lyon R90-01 randomized trial. J Clin Oncol. 1999; 17: 2396.
124. Kalady MF, de Campos-Lobato LF, Stocchi L, et al. Predictive factors of pathologic complete response after neoadjuvant chemoradiation for rectal cancer. Ann Surg. 2009; 4: 582-589.
125. Tulchinsky H, Shmueli E, Figer A, Klausner JM, Rabau M,. An interval > 7 weeks between neoadjuvant therapy and surgery improves pathologic complete response and disease-free survival in patients with locally advanced rectal cancer. Ann Surg Oncol. 2008; 15: 2661-2667.
126. Mignanelli ED, de Campos-Lobato LF, Stocchi L, Lavery IC, Dietz DW,. Downstaging after chemoradiotherapy for locally advanced rectal cancer: is there more (tumor) than meets the eye? Dis Colon Rectum. 2010; 53: 251-256.
127. Pucciarelli S, Capirci C, Emanuele U, et al. Relationship between pathologic T-stage and nodal metastasis after preoperative chemoradiotherapy for locally advanced rectal cancer. Ann Surg Oncol. 2005; 12: 111-116.
128. Bujko K, Nowacki MP, Nasierowska-Guttmejer A, et al. Polish Colorectal Study Group. Prediction of mesorectal nodal metastases after chemoradiation for rectal cancer: results of a randomised trial: implication for subsequent local excision. Radiother Oncol. 2005; 76: 234-240.
129. Kim DW, Kim DY, Kim TH, et al. Is T classification still correlated with lymph node status after preoperative chemoradiotherapy for rectal cancer? Cancer. 2006; 106: 1694-1700.
130. Zmora O, Dasilva GM, Gurland B, et al. Does rectal wall tumor eradication with preoperative chemoradiation permit a change in the operative strategy? Dis Colon Rectum. 2004; 47: 1607-1612.
131. Kerr SF, Norton S, Glynne-Jones R,. Delaying surgery after neoadjuvant chemoradiotherapy for rectal cancer may reduce postoperative morbidity without compromising prognosis. Br J Surg. 2008; 95: 1534-1540.
132. Radu C, Berglund A, Pahlman L, Glimelius B,. Short-course preoperative radiotherapy with delayed surgery in rectal cancer-a retrospective study. Radiother Oncol. 2008; 87: 343-349.
133. Habr-Gama A, Perez RO, Wynn G, Marks J, Kessler H, Gama-Rodrigues J,. Complete clinical response after neoadjuvant chemoradiation therapy for distal rectal cancer: characterization of clinical and endoscopic findings for standardization. Dis Colon Rectum. 2010; 53: 1692-1698.
134. Perez RO,. Role of biopsies in patients with residual rectal cancer following neoadjuvant chemoradiation after downsizing colon can they rule out persisting disease. Colorectal Dis. 2011. In press.
135. Jang NY, Kang SB, Kim DW, et al. The role of carcinoembryonic antigen after neoadjuvant chemoradiotherapy in patients with rectal cancer. Dis Colon Rectum. 2011; 54: 245-252.
136. Perez RO, Sao Juliao GP, Habr-Gama A, et al. The role of carcinoembriogenic antigen in predicting response and survival to neoadjuvant chemoradiotherapy for distal rectal cancer. Dis Colon Rectum. 2009; 52: 1137-1143.
137. Engelen SM, Beets-Tan RG, Lahaye MJ, et al. MRI after chemoradiotherapy of rectal cancer: a useful tool to select patients for local excision. Dis Colon Rectum. 2010; 53: 979-986.
138. Lambregts DM, Vandecaveye V, Barbaro B, et al. Diffusion-weighted MRI for selection of complete responders after chemoradiation for locally advanced rectal cancer: a multicenter study. Ann Surg Oncol. 2011; 18: 2224-2231.
139. Mak D, Joon DL, Chao M, et al. The use of PET in assessing tumor response after neoadjuvant chemoradiation for rectal cancer. Radiother Oncol. 2010; 97: 205-211.
140. Calvo FA, Domper M, Matute R, et al. 18F-FDG positron emission tomography staging and restaging in rectal cancer treated with preoperative chemoradiation. Int J Radiat Oncol Biol Phys. 2004; 58: 528-535.
141. Guillem JG, Puig-La Calle J Jr, Akhurst T, et al. Prospective assessment of primary rectal cancer response to preoperative radiation and chemotherapy using 18-fluorodeoxyglucose positron emission tomography. Dis Colon Rectum. 2000; 43: 18-24.
142. Capirci C, Rubello D, Pasini F, et al. The role of dual-time combined 18-fluorodeoxyglucose positron emission tomography and computed tomography in the staging and restaging workup of locally advanced rectal cancer, treated with preoperative chemoradiation therapy and radical surgery. Int J Radiat Oncol Biol Phys. 2009; 74: 1461-1469.
143. Kristiansen C, Loft A, Berthelsen AK, et al. PET/CT and histopathologic response to preoperative chemoradiation therapy in locally advanced rectal cancer. Dis Colon Rectum. 2008; 51: 21-25.
144. Perez RO, Habr-Gama A, Gama-Rodrigues J, et al. Accuracy of PET/CT and clinical assessment in the detection of complete rectal tumor regression following neoadjuvant chemoradiation. Long-term results of a prospective trial (NCT00254683). Cancer 2011; DOI: 10.1002/cncr.26644 Epub ahead of print.
145. Rosenberg R, Herrmann K, Gertler R, et al. The predictive value of metabolic response to preoperative radiochemotherapy in locally advanced rectal cancer measured by PET/CT. Int J Colorectal Dis. 2009; 24: 191-200.
146. Ota DM, Nelson H,; ACOSOG Group Co-Chairs. Local excision of rectal cancer revisited: ACOSOG protocol Z6041. Ann Surg Oncol. 2007; 14: 271.
147. Rutkowski A, Bujko K, Nowacki MP, Chmielik E, Nasierowska-Guttmejer A, Wojnar A,; Polish Colorectal Study Group. Distal bowel surgical margin shorter than 1 cm after preoperative radiation for rectal cancer: is it safe? Ann Surg Oncol. 2008; 15: 3124-3131.
148. Moore HG, Riedel E, Minsky BD, 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: 80-85.
149. Guillem JG, Chessin DB, Shia J, et al. A prospective pathologic analysis using whole-mount sections of rectal cancer following preoperative combined modality therapy: implications for sphincter preservation. Ann Surg. 2007; 245: 88-93.
150. Rengan R, Paty P, Wong WD, et al. Distal cT2N0 rectal cancer: is there an alternative to abdominoperineal resection? J Clin Oncol. 2005; 23: 4905-4912.
151. Dworak O, Keilholz L, Hoffmann A,. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis. 1997; 12: 19-23.
152. Bateman AC, Jaynes E, Bateman AR,. Rectal cancer staging post neoadjuvant therapy-how should the changes be assessed? Histopathology. 2009; 54: 713-721.
153. Berho M, Oviedo M, Stone E, et al. The correlation between tumour regression grade and lymph node status after chemoradiation in rectal cancer. Colorectal Dis. 2009; 11: 254-258.
154. Vecchio FM, Valentini V, Minsky BD, et al. The relationship of pathologic tumor regression grade (TRG) and outcomes after preoperative therapy in rectal cancer. Int J Radiat Oncol Biol Phys. 2005; 62: 752-760.
155. Bujko K, Kolodziejczyk M, Nasierowska-Guttmejer A, et al. Tumour regression grading in patients with residual rectal cancer after preoperative chemoradiation. Radiother Oncol. 2010; 95: 298-302.
156. Perez RO, Bresciani BH, Bresciani C, et al. Mucinous colorectal adenocarcinoma: influence of mucin expression (Muc1, 2 and 5) on clinico-pathological features and prognosis. Int J Colorectal Dis. 2008; 23: 757-765.
157. Shia J, Guillem JG, Moore HG, et al. Patterns of morphologic alteration in residual rectal carcinoma following preoperative chemoradiation and their association with long-term outcome. Am J Surg Pathol. 2004; 28: 215-223.
158. Smith KD, Tan D, Das P, et al. Clinical significance of acellular mucin in rectal adenocarcinoma patients with a pathologic complete response to preoperative chemoradiation. Ann Surg. 2010; 251: 261-264.
159. de Campos-Lobato LF, Dietz DW, Stocchi L, et al. Clinical implications of acellular mucin pools in resected rectal cancer with pathologic complete response to neoadjuvant chemoradiation. Colorectal Dis. 2012; 14: 62-67.
160. Compton CC,. Updated protocol for the examination of specimens from patients with carcinomas of the colon and rectum, excluding carcinoid tumors, lymphomas, sarcomas, and tumors of the vermiform appendix: a basis for checklists. Cancer Committee. Arch Pathol Lab Med. 2000; 124: 1016-1025.
161. Habr-Gama A, Perez RO, Nadalin W, et al. Long-term results of preoperative chemoradiation for distal rectal cancer correlation between final stage and survival. J Gastrointest Surg. 2005; 9: 90-99; discussion 99-101.
162. Capirci C, Valentini V, Cionini L, et al. Prognostic value of pathologic complete response after neoadjuvant therapy in locally advanced rectal cancer: long-term analysis of 566 ypCR patients. Int J Radiat Oncol Biol Phys. 2008; 72: 99-107.
163. Maas M, Nelemans PJ, Valentini V, et al. Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol. 2010; 11: 835-844.
164. National Comprehensive Cancer Network. Available at:. Accessed February 12, 2012.
165. Blomqvist L, Glimelius B,. The 'good', the 'bad', and the 'ugly' rectal
166. Gerard JP, Rostom Y, Gal J, et al. Can we increase the chance of sphincter saving surgery in rectal cancer with neoadjuvant treatments: lessons from a systematic review of recent randomized trials. Crit Rev Oncol Hematol. 2012; 81: 21-28.
167. Bouchard P, Efron J,. Management of recurrent rectal cancer. Ann Surg Oncol. 2010; 17: 1343-1356.
168. Marijnen CA, Nagtegaal ID, Kapiteijn E, et al. Radiotherapy does not compensate for positive resection margins in rectal cancer patients: report of a multicenter randomized trial. Int J Radiat Oncol Biol Phys. 2003; 55: 1311-1320.
169. Kapiteijn E, Putter H, van de Velde CJ,; Cooperative Investigators of the Dutch ColoRectal Cancer Group. Impact of the introduction and training of total mesorectal excision on recurrence and survival in rectal cancer in The Netherlands. Br J Surg. 2002; 89: 1142-1149.
170. Simunovic M, Sexton R, Rempel E, Moran BJ, Heald RJ,. Optimal preoperative assessment and surgery for rectal cancer may greatly limit the need for radiotherapy. Br J Surg. 2003; 90: 999-1003.
171. van Gijn W, Marijnen CA, Nagtegaal ID, et al. Dutch Colorectal Cancer Group. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer: 12-year follow-up of the multicentre, randomised controlled TME trial. Lancet Oncol. 2011; 12: 575-582.
172. Nagtegaal ID, Quirke P,. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol. 2008; 26: 303-312.
173. Dresen RC, Peters EE, Rutten HJ, et al. Local recurrence in rectal cancer can be predicted by histopathological factors. Eur J Surg Oncol. 2009; 35: 1071-1077.
174. Nagtegaal ID, van de Velde CJ, Marijnen CA, van Krieken JH, Quirke P,; Dutch Colorectal Cancer Group; Pathology Review Committee. Low rectal cancer: a call for a change of approach in abdominoperineal resection. J Clin Oncol. 2005; 23: 9257-9264.
175. 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: 5644-5650.
176. Quah HM, Chou JF, Gonen M, et al. Pathologic stage is most prognostic of disease-free survival in locally advanced rectal cancer patients after preoperative chemoradiation. Cancer. 2008; 113: 57-64.
177. Collette L, Bosset JF, den Dulk M, et al. European Organisation for Research and Treatment of Cancer Radiation Oncology Group. Patients with curative resection of cT3-4 rectal cancer after preoperative radiotherapy or radiochemotherapy: does anybody benefit from adjuvant fluorouracil-based chemotherapy? A trial of the European Organisation for Research and Treatment of Cancer Radiation Oncology Group. J Clin Oncol. 2007; 25: 4379-4386.
178. Mellgren A, Sirivongs P, Rothenberger DA, Madoff RD, Garcia-Aguilar J,. Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum. 2000; 43: 1064-1071; discussion 1071-1074.
179. Greenberg JA, Shibata D, Herndon JE 2nd, Steele GD Jr, Mayer R, Bleday R,. Local excision of distal rectal cancer: an update of cancer and leukemia group B 8984. Dis Colon Rectum. 2008; 51: 1185-1191; discussion 1191-1194.
180. Floyd ND, Saclarides TJ,. Transanal endoscopic microsurgical resection of pT1 rectal tumors. Dis Colon Rectum. 2006; 49: 164-168.
181. Christoforidis D, Cho HM, Dixon MR, Mellgren AF, Madoff RD, Finne CO,. Transanal endoscopic microsurgery versus conventional transanal excision for patients with early rectal cancer. Ann Surg. 2009; 249: 776-782.
182. Doornebosch PG, Ferenschild FT, de Wilt JH, Dawson I, Tetteroo GW, de Graaf EJ,. Treatment of recurrence after transanal endoscopic microsurgery (TEM) for T1 rectal cancer. Dis Colon Rectum. 2010; 53: 1234-1239.
183. Sengupta S, Tjandra JJ,. Local excision of rectal cancer: what is the evidence? Dis Colon Rectum. 2001; 44: 1345-1361.
184. Bonnen M, Crane C, Vauthey JN, et al. Long-term results using local excision after preoperative chemoradiation among selected T3 rectal cancer patients. Int J Radiat Oncol Biol Phys. 2004; 60: 1098-1105.
185. 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: 352-358.
186. Weiser MR, Landmann RG, Wong WD, et al. Surgical salvage of recurrent rectal cancer after transanal excision. Dis Colon Rectum. 2005; 48: 1169-1175.
187. Habr-Gama A, de Souza PM, Ribeiro U Jr, et al. Low rectal cancer: impact of radiation and chemotherapy on surgical treatment. Dis Colon Rectum. 1998; 41: 1087-1096.
188. Habr-Gama A, Perez RO,. Non-operative management of rectal cancer after neoadjuvant chemoradiation. Br J Surg. 2009; 96: 125-127.
189. 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. 2004; 240: 711-717; discussion 717-718.
190. Hiotis SP, Weber SM, Cohen AM, et al. Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients. J Am Coll Surg. 2002; 194: 131-135; discussion 135-136.
191. Glynne-Jones R, Wallace M, Livingstone JI, Meyrick-Thomas J,. Complete clinical response after preoperative chemoradiation in rectal cancer: is a "wait and see" policy justified? Dis Colon Rectum. 2008; 51: 10-19; discussion 19-20.
192. Habr-Gama A, Perez RO, Proscurshim I, et al. Interval between surgery and neoadjuvant chemoradiation therapy for distal rectal cancer: does delayed surgery have an impact on outcome? Int J Radiat Oncol Biol Phys. 2008; 71: 1181-1188.
193. Ghadimi BM, Grade M, Difilippantonio MJ, et al. Effectiveness of gene expression profiling for response prediction of rectal adenocarcinomas to preoperative chemoradiotherapy. J Clin Oncol. 2005; 23: 1826-1838.
194. Rimkus C, Friederichs J, Boulesteix AL, et al. Microarray-based prediction of tumor response to neoadjuvant radiochemotherapy of patients with locally advanced rectal cancer. Clin Gastroenterol Hepatol. 2008; 6: 53-61.
195. Kim IJ, Lim SB, Kang HC, et al. Microarray gene expression profiling for predicting complete response to preoperative chemoradiotherapy in patients with advanced rectal cancer. Dis Colon Rectum. 2007; 50: 1342-1353.