How Should Imaging Direct/Orient Management of Rectal Cancer?

Abstract

Modern rectal cancer management is dependent on preoperative staging, and radiological assessment is a crucial part of this process. Imaging must provide sufficient information to guide preoperative decision-making that is reliable and reproducible. Different methods have been used for local staging; however, magnetic resonance imaging (MRI) has shown to be the most reliable tool for this purpose. MRI offers prognostic information about the patients and guides the decision between neoadjuvant treatment and total mesorectal excision alone. Also, not only the initial staging but also restaging by MRI can provide significant information regarding tumor response that is essential when considering alternative approaches.

Keywords

rectal cancer - magnetic resonance imaging - local staging

• References

• 1 Battersby NJ, Moran B, Yu S, Tekkis P, Brown G. MR imaging for rectal cancer: the role in staging the primary and response to neoadjuvant therapy. Expert Rev Gastroenterol Hepatol 2014; 8 (06) 703-719
• 2 Balyasnikova S, Brown G. Optimal imaging strategies for rectal cancer staging and ongoing management. Curr Treat Options Oncol 2016; 17 (06) 32
• 3 Patel UB, Taylor F, Blomqvist L. , et al. Magnetic resonance imaging-detected tumor response for locally advanced rectal cancer predicts survival outcomes: MERCURY experience. J Clin Oncol 2011; 29 (28) 3753-3760
• 4 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 (06) 1827-1835
• 5 Glynne-Jones R, Harrison M, Hughes R. Challenges in the neoadjuvant treatment of rectal cancer: balancing the risk of recurrence and quality of life. Cancer Radiother 2013; 17 (07) 675-685
• 6 MERCURY Study Group. Diagnostic accuracy of preoperative magnetic resonance imaging in predicting curative resection of rectal cancer: prospective observational study. BMJ 2006; 333 (7572): 779
• 7 MERCURY Study Group. Extramural depth of tumor invasion at thin-section MR in patients with rectal cancer: results of the MERCURY study. Radiology 2007; 243 (01) 132-139
• 8 Salerno G, Daniels IR, Moran BJ, Wotherspoon A, Brown G. Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience. Clin Radiol 2006; 61 (11) 916-923
• 9 Nielsen LB, Wille-Jørgensen P. National and international guidelines for rectal cancer. Colorectal Dis 2014; 16 (11) 854-865
• 10 Brown G. Staging rectal cancer: endoscopic ultrasound and pelvic MRI. Cancer Imaging 2008; 8 Spec No A: S43-S45
• 11 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 (03) 355-364
• 12 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 (03) 351-357
• 13 Brown G, Daniels IR, Richardson C, Revell P, Peppercorn D, Bourne M. Techniques and trouble-shooting in high spatial resolution thin slice MRI for rectal cancer. Br J Radiol 2005; 78 (927) 245-251
• 14 Stoker J, Rociu E, Zwamborn AW, Schouten WR, Laméris JS. Endoluminal MR imaging of the rectum and anus: technique, applications, and pitfalls. Radiographics 1999; 19 (02) 383-398
• 15 Wale A, Brown G. A practical review of the performance and interpretation of staging magnetic resonance imaging for rectal cancer. Top Magn Reson Imaging 2014; 23 (04) 213-223
• 16 Koh DM, Brown G, Temple L. , et al. Distribution of mesorectal lymph nodes in rectal cancer: in vivo MR imaging compared with histopathological examination. Initial observations. Eur Radiol 2005; 15 (08) 1650-1657
• 17 Hunter C, Brown G. Pre-operative staging of rectal cancer: a review of imaging techniques. Expert Rev Gastroenterol Hepatol 2016; 10 (09) 1011-1025
• 18 Bhangu A, Rasheed S, Brown G, Tait D, Cunningham D, Tekkis P. Does rectal cancer height influence the oncological outcome?. Colorectal Dis 2014; 16 (10) 801-808
• 19 Brown G. Thin section MRI in multidisciplinary pre-operative decision making for patients with rectal cancer. Br J Radiol 2005; 78 (Spec No 2): S117-S127
• 20 Taylor FG, Quirke P, Heald RJ. , et al; MERCURY study group. 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 2011; 253 (04) 711-719
• 21 Brown G. Mri IN STaging REctal polyp planes (2015). Available at: http://minstrelstudy.co.uk/downloads/trial-protocol.pdf . Accessed July 2016
• 22 Borstlap WA, Tanis PJ, Koedam TW. , et al. A multi-centred randomised trial of radical surgery versus adjuvant chemoradiotherapy after local excision for early rectal cancer. BMC Cancer 2016; 16 (01) 513
• 23 Lutz MP, Zalcberg JR, Glynne-Jones R. , et al. Second St. Gallen European Organisation for Research and Treatment of Cancer Gastrointestinal Cancer Conference: consensus recommendations on controversial issues in the primary treatment of rectal cancer. Eur J Cancer 2016; 63: 11-24
• 24 Fleming ID, Cooper JS, Henson DE. , et al , eds. AJCC Cancer Staging Manual. 5th ed. Chicago, IL: American Joint Committee on Cancer; 1997
• 25 Compton CC, Greene FL. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 2004; 54 (06) 295-308
• 26 Cawthorn SJ, Parums DV, Gibbs NM. , et al. Extent of mesorectal spread and involvement of lateral resection margin as prognostic factors after surgery for rectal cancer [see comments]. Lancet 1990; 335 (8697): 1055-1059
• 27 Dukes CE, Bussey HJ. The spread of rectal cancer and its effect on prognosis. Br J Cancer 1958; 12 (03) 309-320
• 28 Jass JR, Love SB. Prognostic value of direct spread in Dukes' C cases of rectal cancer. Dis Colon Rectum 1989; 32 (06) 477-480
• 29 Shepherd NA. Mesorectal spread and involvement of lateral resection margin in rectal cancer [letter; comment]. Lancet 1990; 335 (8702): 1402-1403
• 30 Merkel S, Mansmann U, Siassi M, Papadopoulos T, Hohenberger W, Hermanek P. The prognostic inhomogeneity in pT3 rectal carcinomas. Int J Colorectal Dis 2001; 16 (05) 298-304
• 31 Harrison JC, Dean PJ, el-Zeky F, Vander Zwaag R. From Dukes through Jass: pathological prognostic indicators in rectal cancer. Hum Pathol 1994; 25 (05) 498-505
• 32 Brandt WS, Yong S, Abood G, Micetich K, Walther A, Shoup M. The depth of post-treatment perirectal tissue invasion is a predictor of outcome in patients with clinical T3N1M0 rectal cancer treated with neoadjuvant chemoradiation followed by surgical resection. Am J Surg 2014; 207 (03) 357-360 , discussion 360
• 33 Cho SH, Kim SH, Bae JH. , et al; Society of North America (RSNA). Prognostic stratification by extramural depth of tumor invasion of primary rectal cancer based on the Radiological Society of North America proposal. AJR Am J Roentgenol 2014; 202 (06) 1238-1244
• 34 Cianchi F, Messerini L, Comin CE. , et al. Pathologic determinants of survival after resection of T3N0 (Stage IIA) colorectal cancer: proposal for a new prognostic model. Dis Colon Rectum 2007; 50 (09) 1332-1341
• 35 Merkel S, Weber K, Schellerer V. , et al. Prognostic subdivision of ypT3 rectal tumours according to extension beyond the muscularis propria. Br J Surg 2014; 101 (05) 566-572
• 36 Miyoshi M, Ueno H, Hashiguchi Y, Mochizuki H, Talbot IC. Extent of mesorectal tumor invasion as a prognostic factor after curative surgery for T3 rectal cancer patients. Ann Surg 2006; 243 (04) 492-498
• 37 Pollheimer MJ, Kornprat P, Pollheimer VS. , et al. Clinical significance of pT sub-classification in surgical pathology of colorectal cancer. Int J Colorectal Dis 2010; 25 (02) 187-196
• 38 Shin R, Jeong SY, Yoo HY. , et al. Depth of mesorectal extension has prognostic significance in patients with T3 rectal cancer. Dis Colon Rectum 2012; 55 (12) 1220-1228
• 39 Yoshida K, Yoshimatsu K, Otani T, Yokomizo H, Ogawa K. The depth of tumor invasion beyond the outer border of the muscularis propria as a prognostic factor for T3 rectal/rectosigmoid cancer. Anticancer Res 2008; 28 (3B, 3b): 1773-1778
• 40 Smith N, Brown G. Preoperative staging of rectal cancer. Acta Oncol 2008; 47 (01) 20-31
• 41 Al-Sukhni E, Milot L, Fruitman M. , et al. Diagnostic accuracy of MRI for assessment of T category, lymph node metastases, and circumferential resection margin involvement in patients with rectal cancer: a systematic review and meta-analysis. Ann Surg Oncol 2012; 19 (07) 2212-2223
• 42 Bissett IP, Fernando CC, Hough DM. , et al. Identification of the fascia propria by magnetic resonance imaging and its relevance to preoperative assessment of rectal cancer. Dis Colon Rectum 2001; 44 (02) 259-265
• 43 Battersby NJ, How P, Moran B. , et al; MERCURY II Study Group. Prospective validation of a low rectal cancer magnetic resonance imaging staging system and development of a local recurrence risk stratification model: The MERCURY II study. Ann Surg 2016; 263 (04) 751-760
• 44 Xie H, Zhou X, Zhuo Z, Che S, Xie L, Fu W. Effectiveness of MRI for the assessment of mesorectal fascia involvement in patients with rectal cancer: a systematic review and meta-analysis. Dig Surg 2014; 31 (02) 123-134
• 45 Wibe A, Rendedal PR, Svensson E. , et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg 2002; 89 (03) 327-334
• 46 Adam IJ, Mohamdee MO, Martin IG. , et al. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet 1994; 344 (8924): 707-711
• 47 Taylor FG, Quirke P, Heald RJ. , et al; Magnetic Resonance Imaging in Rectal Cancer European Equivalence Study Study Group. Preoperative magnetic resonance imaging assessment of circumferential resection margin predicts disease-free survival and local recurrence: 5-year follow-up results of the MERCURY study. J Clin Oncol 2014; 32 (01) 34-43
• 48 Gaertner WB, Kwaan MR, Madoff RD, Melton GB. Rectal cancer: An evidence-based update for primary care providers. World J Gastroenterol 2015; 21 (25) 7659-7671
• 49 Weiser MR, Fichera A, Schrag D, Boughey JC, You YN. Progress in the PROSPECT trial: precision treatment for rectal cancer?. Bull Am Coll Surg 2015; 100 (04) 51-52
• 50 Taylor FG, Quirke P, Heald RJ. , et al; MERCURY study group. One millimetre is the safe cut-off for magnetic resonance imaging prediction of surgical margin status in rectal cancer. Br J Surg 2011; 98 (06) 872-879
• 51 Cedermark B, Dahlberg M, Glimelius B, Påhlman L, Rutqvist LE, Wilking N. ; Swedish Rectal Cancer Trial. Improved survival with preoperative radiotherapy in resectable rectal cancer. N Engl J Med 1997; 336 (14) 980-987
• 52 Bondeven P, Hagemann-Madsen RH, Laurberg S, Pedersen BG. Extent and completeness of mesorectal excision evaluated by postoperative magnetic resonance imaging. Br J Surg 2013; 100 (10) 1357-1367
• 53 Hermanek P, Merkel S, Fietkau R, Rödel C, Hohenberger W. Regional lymph node metastasis and locoregional recurrence of rectal carcinoma in the era of TME [corrected] surgery. Implications for treatment decisions. Int J Colorectal Dis 2010; 25 (03) 359-368
• 54 Yano H, Moran BJ, Watanabe T, Sugihara K. Lateral pelvic lymph-node dissection: still an option for cure. Lancet Oncol 2010; 11 (02) 114 , author reply 114–115
• 55 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 (02) 371-377
• 56 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 (01) 78-83
• 57 Arii K, Takifuji K, Yokoyama S. , et al. Preoperative evaluation of pelvic lateral lymph node of patients with lower rectal cancer: comparison study of MR imaging and CT in 53 patients. Langenbecks Arch Surg 2006; 391 (05) 449-454
• 58 Dworak O. Morphology of lymph nodes in the resected rectum of patients with rectal carcinoma. Pathol Res Pract 1991; 187 (08) 1020-1024
• 59 Park JS, Jang YJ, Choi GS. , et al. Accuracy of preoperative MRI in predicting pathology stage in rectal cancers: node-for-node matched histopathology validation of MRI features. Dis Colon Rectum 2014; 57 (01) 32-38
• 60 Heijnen LA, Lambregts DM, Mondal D. , et al. Diffusion-weighted MR imaging in primary rectal cancer staging demonstrates but does not characterise lymph nodes. Eur Radiol 2013; 23 (12) 3354-3360
• 61 Lambregts DM, Maas M, Riedl RG. , et al. Value of ADC measurements for nodal staging after chemoradiation in locally advanced rectal cancer-a per lesion validation study. Eur Radiol 2011; 21 (02) 265-273
• 62 Kim DJ, Chung JJ, Yu JS, Cho ES, Kim JH. Evaluation of lateral pelvic nodes in patients with advanced rectal cancer. AJR Am J Roentgenol 2014; 202 (06) 1245-1255
• 63 Hida J, Yasutomi M, Fujimoto K, Maruyama T, Okuno K, Shindo K. Does lateral lymph node dissection improve survival in rectal carcinoma? Examination of node metastases by the clearing method. J Am Coll Surg 1997; 184 (05) 475-480
• 64 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 (05) 1517-1522
• 65 Talbot IC, Ritchie S, Leighton MH, Hughes AO, Bussey HJ, Morson BC. The clinical significance of invasion of veins by rectal cancer. Br J Surg 1980; 67 (06) 439-442
• 66 Freedman LS, Macaskill P, Smith AN. Multivariate analysis of prognostic factors for operable rectal cancer. Lancet 1984; 2 (8405): 733-736
• 67 Chand M, Siddiqui MR, Swift I, Brown G. Systematic review of prognostic importance of extramural venous invasion in rectal cancer. World J Gastroenterol 2016; 22 (04) 1721-1726
• 68 Günther K, Dworak O, Remke S. , et al. Prediction of distant metastases after curative surgery for rectal cancer. J Surg Res 2002; 103 (01) 68-78
• 69 Rich T, Gunderson LL, Lew R, Galdibini JJ, Cohen AM, Donaldson G. Patterns of recurrence of rectal cancer after potentially curative surgery. Cancer 1983; 52 (07) 1317-1329
• 70 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 (02) 229-236
• 71 Koh DM, Smith NJ, Swift RI, Brown G. The relationship between MR demonstration of extramural venous invasion and nodal disease in rectal cancer. Clin Med Oncol 2008; 2: 267-273
• 72 Brown G, Kirkham A, Williams GT. , et al. High-resolution MRI of the anatomy important in total mesorectal excision of the rectum. AJR Am J Roentgenol 2004; 182 (02) 431-439
• 73 Sohn B, Lim JS, Kim H. , et al. MRI-detected extramural vascular invasion is an independent prognostic factor for synchronous metastasis in patients with rectal cancer. Eur Radiol 2015; 25 (05) 1347-1355
• 74 Chand M, Evans J, Swift RI. , et al. The prognostic significance of postchemoradiotherapy high-resolution MRI and histopathology detected extramural venous invasion in rectal cancer. Ann Surg 2015; 261 (03) 473-479
• 75 Balyasnikova S, Brown G. Imaging advances in colorectal cancer. Curr Colorectal Cancer Rep 2016; 12: 162-169
• 76 Chand M, Swift RI, Tekkis PP, Chau I, Brown G. Extramural venous invasion is a potential imaging predictive biomarker of neoadjuvant treatment in rectal cancer. Br J Cancer 2014; 110 (01) 19-25
• 77 Beyond TME Collaborative. Consensus statement on the multidisciplinary management of patients with recurrent and primary rectal cancer beyond total mesorectal excision planes. Br J Surg 2013; 100 (08) 1009-1014
• 78 Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer?. J Clin Oncol 2008; 26 (02) 303-312
• 79 Jörgren F, Johansson R, Damber L, Lindmark G. Oncological outcome after incidental perforation in radical rectal cancer surgery. Int J Colorectal Dis 2010; 25 (06) 731-740
• 80 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 (04) 449-457
• 81 Moran BJ. Predicting the risk and diminishing the consequences of anastomotic leakage after anterior resection for rectal cancer. Acta Chir Iugosl 2010; 57 (03) 47-50
• 82 Habr-Gama A, Sabbaga J, Gama-Rodrigues J. , et al. Watch and wait approach following extended neoadjuvant chemoradiation for distal rectal cancer: are we getting closer to anal cancer management?. Dis Colon Rectum 2013; 56 (10) 1109-1117
• 83 Memon S, Lynch AC, Bressel M, Wise AG, Heriot AG. Systematic review and meta-analysis of the accuracy of MRI and endorectal ultrasound in the restaging and response assessment of rectal cancer following neoadjuvant therapy. Colorectal Dis 2015; 17 (09) 748-761
• 84 Yu SK, Tait D, Chau I, Brown G. MRI predictive factors for tumor response in rectal cancer following neoadjuvant chemoradiation therapy--implications for induction chemotherapy?. Int J Radiat Oncol Biol Phys 2013; 87 (03) 505-511
• 85 Patel UB, Brown G, Rutten H. , et al. Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 2012; 19 (09) 2842-2852
• 86 Hole KH, Larsen SG, Grøholt KK, Giercksky KE, Ree AH. Magnetic resonance-guided histopathology for improved accuracy of tumor response evaluation of neoadjuvant treatment in organ-infiltrating rectal cancer. Radiother Oncol 2013; 107 (02) 178-183
• 87 Alcaide J, Funez R, Rueda A. , et al. The role and prognostic value of apoptosis in colorectal carcinoma. BMC Clin Pathol 2013; 13 (01) 24
• 88 Vanagunas A, Lin DE, Stryker SJ. Accuracy of endoscopic ultrasound for restaging rectal cancer following neoadjuvant chemoradiation therapy. Am J Gastroenterol 2004; 99 (01) 109-112
• 89 Pastor C, Subtil JC, Sola J. , et al. Accuracy of endoscopic ultrasound to assess tumor response after neoadjuvant treatment in rectal cancer: can we trust the findings?. Dis Colon Rectum 2011; 54 (09) 1141-1146
• 90 Rau B, Hünerbein M, Barth C. , et al. Accuracy of endorectal ultrasound after preoperative radiochemotherapy in locally advanced rectal cancer. Surg Endosc 1999; 13 (10) 980-984
• 91 Schaefer O, Langer M. Detection of recurrent rectal cancer with CT, MRI and PET/CT. Eur Radiol 2007; 17 (08) 2044-2054
• 92 Denecke T, Rau B, Hoffmann KT. , et al. Comparison of CT, MRI and FDG-PET in response prediction of patients with locally advanced rectal cancer after multimodal preoperative therapy: is there a benefit in using functional imaging?. Eur Radiol 2005; 15 (08) 1658-1666
• 93 Walker AS, Zwintscher NP, Johnson EK. , et al. Future directions for monitoring treatment response in colorectal cancer. J Cancer 2014; 5 (01) 44-57
• 94 Chennupati SK, Quon A, Kamaya A. , et al. Positron emission tomography for predicting pathologic response after neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Am J Clin Oncol 2012; 35 (04) 334-339
• 95 Guillem JG, Ruby JA, Leibold T. , et al. Neither FDG-PET nor CT can distinguish between a pathological complete response and an incomplete response after neoadjuvant chemoradiation in locally advanced rectal cancer: a prospective study. Ann Surg 2013; 258 (02) 289-295
• 96 O'Neill BD, Brown G, Heald RJ, Cunningham D, Tait DM. Non-operative treatment after neoadjuvant chemoradiotherapy for rectal cancer. Lancet Oncol 2007; 8 (07) 625-633
• 97 Dewhurst CE, Mortele KJ. Magnetic resonance imaging of rectal cancer. Radiol Clin North Am 2013; 51 (01) 121-131
• 98 Wu LM, Zhu J, Hu J. , et al. Is there a benefit in using magnetic resonance imaging in the prediction of preoperative neoadjuvant therapy response in locally advanced rectal cancer?. Int J Colorectal Dis 2013; 28 (09) 1225-1238
• 99 Yeo SG, Kim DY, Kim TH. , et al. Tumor volume reduction rate measured by magnetic resonance volumetry correlated with pathologic tumor response of preoperative chemoradiotherapy for rectal cancer. Int J Radiat Oncol Biol Phys 2010; 78 (01) 164-171
• 100 Yeo SG, Kim DY, Park JW. , et al. Tumor volume reduction rate after preoperative chemoradiotherapy as a prognostic factor in locally advanced rectal cancer. Int J Radiat Oncol Biol Phys 2012; 82 (02) e193-e199
• 101 Therasse P, Arbuck SG, Eisenhauer EA. , et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000; 92 (03) 205-216
• 102 Shihab OC, Taylor F, Salerno G. , et al. MRI predictive factors for long-term outcomes of low rectal tumours. Ann Surg Oncol 2011; 18 (12) 3278-3284
• 103 Siddiqui MR, Gormly KL, Bhoday J. , et al. Interobserver agreement of radiologists assessing the response of rectal cancers to preoperative chemoradiation using the MRI tumour regression grading (mrTRG). Clin Radiol 2016; 71 (09) 854-862
• 104 Battersby NJ, Balyasnikova S, Brown G. Guiding post-treatment decisions in rectal cancer: mrTRG is a practical place to start. Oncology (Williston Park) 2014; 28 (08) 677-680