Beyond Histologic Staging: Emerging Imaging Strategies in Colorectal Cancer with Special Focus on Magnetic Resonance Imaging

 

 Buy Article Permissions and Reprints

Abstract

Imaging plays an increasingly important role in the staging and management of colorectal cancer. In recent years, magnetic resonance imaging (MRI) has supplanted transrectal ultrasound as the preferred modality for the locoregional staging of rectal cancer. Furthermore, the advent of both diffusion-weighted imaging and hepatobiliary contrast agents has significantly enhanced the ability of MRI to detect colorectal liver metastases. In clinical practice, MRI routinely provides prognostic information, helps to guide surgical strategy, and determines the need for neoadjuvant therapies related to both the primary tumor and metastatic disease. Expanding on these roles for MRI, positron emission tomography (PET)/MRI is the newest clinical hybrid imaging modality and combines the metabolic information of PET with the high soft tissue contrast of MRI. The addition of PET/MRI to the clinical staging armamentarium has the potential to provide comprehensive state-of-the-art colorectal cancer staging in a single examination.

• References

• 1 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015; 65 (1) 5-29
  CrossrefPubMedGoogle Scholar
• 2 Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier A-M. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg 2006; 244 (2) 254-259
  CrossrefPubMedGoogle Scholar
• 3 Alberts SR, Poston GJ. Treatment advances in liver-limited metastatic colorectal cancer. Clin Colorectal Cancer 2011; 10 (4) 258-265
  CrossrefPubMedGoogle Scholar
• 4 Berri RN, Abdalla EK. Curable metastatic colorectal cancer: recommended paradigms. Curr Oncol Rep 2009; 11 (3) 200-208
  CrossrefPubMedGoogle Scholar
• 5 Wagman LD. Importance of response to neoadjuvant therapy in patients with liver-limited mCRC when the intent is resection and/or ablation. Clin Colorectal Cancer 2013; 12 (4) 223-232
  CrossrefPubMedGoogle Scholar
• 6 Folprecht G, Grothey A, Alberts S, Raab H-R, Köhne C-H. Neoadjuvant treatment of unresectable colorectal liver metastases: correlation between tumour response and resection rates. Ann Oncol 2005; 16 (8) 1311-1319
  CrossrefPubMedGoogle Scholar
• 7 Abdalla EK, Vauthey J-N, Ellis LM , et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004; 239 (6) 818-825 , discussion 825–827
  CrossrefPubMedGoogle Scholar
• 8 Foxtrot Collaborative Group. Feasibility of preoperative chemotherapy for locally advanced, operable colon cancer: the pilot phase of a randomised controlled trial. Lancet Oncol 2012; 13 (11) 1152-1160
  CrossrefPubMedGoogle Scholar
• 9 Glynne-Jones R, Tan D, Goh V. Pelvic MRI for guiding treatment decisions in rectal cancer. Oncology (Williston Park) 2014; 28 (8) 667-677
  PubMedGoogle Scholar
• 10 Nogué M, Salud A, Vicente P , et al; AVACROSS Study Group. Addition of bevacizumab to XELOX induction therapy plus concomitant capecitabine-based chemoradiotherapy in magnetic resonance imaging-defined poor-prognosis locally advanced rectal cancer: the AVACROSS study. Oncologist 2011; 16 (5) 614-620
  CrossrefPubMedGoogle Scholar
• 11 Velenik V, Ocvirk J, Music M , et al. Neoadjuvant capecitabine, radiotherapy, and bevacizumab (CRAB) in locally advanced rectal cancer: results of an open-label phase II study. Radiat Oncol 2011; 6: 105
  CrossrefPubMedGoogle Scholar
• 12 Herzog U, von Flüe M, Tondelli P, Schuppisser JP. How accurate is endorectal ultrasound in the preoperative staging of rectal cancer?. Dis Colon Rectum 1993; 36 (2) 127-134
  CrossrefPubMedGoogle Scholar
• 13 Jochem RJ, Reading CC, Dozois RR, Carpenter HA, Wolff BG, Charboneau JW. Endorectal ultrasonographic staging of rectal carcinoma. Mayo Clin Proc 1990; 65 (12) 1571-1577
  CrossrefPubMedGoogle Scholar
• 14 Snady H, Merrick MA. Improving the treatment of colorectal cancer: the role of EUS. Cancer Invest 1998; 16 (8) 572-581
  CrossrefPubMedGoogle Scholar
• 15 Waizer A, Zitron S, Ben-Baruch D, Baniel J, Wolloch Y, Dintsman M. Comparative study for preoperative staging of rectal cancer. Dis Colon Rectum 1989; 32 (1) 53-56
  CrossrefPubMedGoogle Scholar
• 16 Yimei J, Ren Z, Lu X, Huan Z. A comparison between the reference values of MRI and EUS and their usefulness to surgeons in rectal cancer. Eur Rev Med Pharmacol Sci 2012; 16 (15) 2069-2077
  PubMedGoogle Scholar
• 17 Jürgensen C, Teubner A, Habeck J-O, Diener F, Scherübl H, Stölzel U. Staging of rectal cancer by EUS: depth of infiltration in T3 cancers is important. Gastrointest Endosc 2011; 73 (2) 325-328
  CrossrefPubMedGoogle Scholar
• 18 Badger SA, Devlin PB, Neilly PJD, Gilliland R. Preoperative staging of rectal carcinoma by endorectal ultrasound: is there a learning curve?. Int J Colorectal Dis 2007; 22 (10) 1261-1268
  CrossrefPubMedGoogle Scholar
• 19 Fernández-Esparrach G, Ayuso-Colella JR, Sendino O , et al. EUS and magnetic resonance imaging in the staging of rectal cancer: a prospective and comparative study. Gastrointest Endosc 2011; 74 (2) 347-354
  CrossrefPubMedGoogle Scholar
• 20 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 (10) 1520-1525
  CrossrefPubMedGoogle Scholar
• 21 Bhattacharjya S, Bhattacharjya T, Baber S, Tibballs JM, Watkinson AF, Davidson BR. Prospective study of contrast-enhanced computed tomography, computed tomography during arterioportography, and magnetic resonance imaging for staging colorectal liver metastases for liver resection. Br J Surg 2004; 91 (10) 1361-1369
  CrossrefPubMedGoogle Scholar
• 22 Balthazar EJ, Megibow AJ, Hulnick D, Naidich DP. Carcinoma of the colon: detection and preoperative staging by CT. AJR Am J Roentgenol 1988; 150 (2) 301-306
  CrossrefPubMedGoogle Scholar
• 23 Zerhouni EA, Rutter C, Hamilton SR , et al. CT and MR imaging in the staging of colorectal carcinoma: report of the Radiology Diagnostic Oncology Group II. Radiology 1996; 200 (2) 443-451
  CrossrefPubMedGoogle Scholar
• 24 Ju H, Xu D, Li D, Chen G, Shao G. Comparison between endoluminal ultrasonography and spiral computerized tomography for the preoperative local staging of rectal carcinoma. Biosci Trends 2009; 3 (2) 73-76
  PubMedGoogle Scholar
• 25 Perez RO, Pereira DD, Proscurshim I , et al. Lymph node size in rectal cancer following neoadjuvant chemoradiation—can we rely on radiologic nodal staging after chemoradiation?. Dis Colon Rectum 2009; 52 (7) 1278-1284
  CrossrefPubMedGoogle Scholar
• 26 Kim SH, Lee JM, Lee MW, Kim GH, Han JK, Choi BI. Diagnostic accuracy of 3.0-Tesla rectal magnetic resonance imaging in preoperative local staging of primary rectal cancer. Invest Radiol 2008; 43 (8) 587-593
  CrossrefPubMedGoogle Scholar
• 27 Rafaelsen SR, Vagn-Hansen C, Sørensen T, Pløen J, Jakobsen A. Transrectal ultrasound and magnetic resonance imaging measurement of extramural tumor spread in rectal cancer. World J Gastroenterol 2012; 18 (36) 5021-5026
  CrossrefPubMedGoogle Scholar
• 28 Phang PT, Gollub MJ, Loh BD , et al. Accuracy of endorectal ultrasound for measurement of the closest predicted radial mesorectal margin for rectal cancer. Dis Colon Rectum 2012; 55 (1) 59-64
  CrossrefPubMedGoogle Scholar
• 29 Li JCM, Liu SYW, Lo AWI , et al. The learning curve for endorectal ultrasonography in rectal cancer staging. Surg Endosc 2010; 24 (12) 3054-3059
  CrossrefPubMedGoogle Scholar
• 30 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 (1) 132-139
  CrossrefPubMedGoogle Scholar
• 31 Del Vescovo R, Trodella LE, Sansoni I , et al. MR imaging of rectal cancer before and after chemoradiation therapy. Radiol Med (Torino) 2012; 117 (7) 1125-1138
  CrossrefPubMedGoogle Scholar
• 32 Kim SH, Lee JM, Park HS, Eun HW, Han JK, Choi BI. Accuracy of MRI for predicting the circumferential resection margin, mesorectal fascia invasion, and tumor response to neoadjuvant chemoradiotherapy for locally advanced rectal cancer. J Magn Reson Imaging 2009; 29 (5) 1093-1101
  CrossrefPubMedGoogle Scholar
• 33 Purkayastha S, Tekkis PP, Athanasiou T, Tilney HS, Darzi AW, Heriot AG. Diagnostic precision of magnetic resonance imaging for preoperative prediction of the circumferential margin involvement in patients with rectal cancer. Colorectal Dis 2007; 9 (5) 402-411
  CrossrefPubMedGoogle Scholar
• 34 Videhult P, Smedh K, Lundin P, Kraaz W. Magnetic resonance imaging for preoperative staging of rectal cancer in clinical practice: high accuracy in predicting circumferential margin with clinical benefit. Colorectal Dis 2007; 9 (5) 412-419
  CrossrefPubMedGoogle Scholar
• 35 Wieder HA, Rosenberg R, Lordick F , et al. Rectal cancer: MR imaging before neoadjuvant chemotherapy and radiation therapy for prediction of tumor-free circumferential resection margins and long-term survival. Radiology 2007; 243 (3) 744-751
  CrossrefPubMedGoogle Scholar
• 36 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
  CrossrefPubMedGoogle Scholar
• 37 Chang GJ, You YN, Park IJ , et al. Pretreatment high-resolution rectal MRI and treatment response to neoadjuvant chemoradiation. Dis Colon Rectum 2012; 55 (4) 371-377
  CrossrefPubMedGoogle Scholar
• 38 Hunter CJ, Garant A, Vuong T , et al. Adverse features on rectal MRI identify a high-risk group that may benefit from more intensive preoperative staging and treatment. Ann Surg Oncol 2012; 19 (4) 1199-1205
  CrossrefPubMedGoogle Scholar
• 39 Hofheinz R-D, Wenz F, Post S , et al. Chemoradiotherapy with capecitabine versus fluorouracil for locally advanced rectal cancer: a randomised, multicentre, non-inferiority, phase 3 trial. Lancet Oncol 2012; 13 (6) 579-588
  CrossrefPubMedGoogle Scholar
• 40 Loos M, Quentmeier P, Schuster T , et al. Effect of preoperative radio(chemo)therapy on long-term functional outcome in rectal cancer patients: a systematic review and meta-analysis. Ann Surg Oncol 2013; 20 (6) 1816-1828
  CrossrefPubMedGoogle Scholar
• 41 Engelen SME, Maas M, Lahaye MJ , et al. 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 2013; 49 (10) 2311-2320
  CrossrefPubMedGoogle Scholar
• 42 Taylor FGM, 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 (4) 711-719
  CrossrefPubMedGoogle Scholar
• 43 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
  CrossrefPubMedGoogle Scholar
• 44 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
  CrossrefPubMedGoogle Scholar
• 45 Doyon F, Attenberger UI, Dinter DJ, Schoenberg SO, Post S, Kienle P. Clinical relevance of morphologic MRI criteria for the assessment of lymph nodes in patients with rectal cancer. Int J Colorectal Dis 2015; 30 (11) 1541-1546
  CrossrefPubMedGoogle Scholar
• 46 Koh D-M, George C, Temple L , et al. Diagnostic accuracy of nodal enhancement pattern of rectal cancer at MRI enhanced with ultrasmall superparamagnetic iron oxide: findings in pathologically matched mesorectal lymph nodes. AJR Am J Roentgenol 2010; 194 (6) W505-13
  PubMedGoogle Scholar
• 47 Shihab OC, Taylor F, Bees N , et al; MERCURY Study Group. Relevance of magnetic resonance imaging-detected pelvic sidewall lymph node involvement in rectal cancer. Br J Surg 2011; 98 (12) 1798-1804
  CrossrefPubMedGoogle Scholar
• 48 Mahnken AH, Pereira PL, de Baère T. Interventional oncologic approaches to liver metastases. Radiology 2013; 266 (2) 407-430
  CrossrefPubMedGoogle Scholar
• 49 Cance WG, Cohen AM, Enker WE, Sigurdson ER. Predictive value of a negative computed tomographic scan in 100 patients with rectal carcinoma. Dis Colon Rectum 1991; 34 (9) 748-751
  CrossrefPubMedGoogle Scholar
• 50 Numminen K, Isoniemi H, Halavaara J , et al. Preoperative assessment of focal liver lesions: multidetector computed tomography challenges magnetic resonance imaging. Acta Radiol 2005; 46 (1) 9-15
  CrossrefPubMedGoogle Scholar
• 51 Zorzi D, Laurent A, Pawlik TM, Lauwers GY, Vauthey J-N, Abdalla EK. Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br J Surg 2007; 94 (3) 274-286
  CrossrefPubMedGoogle Scholar
• 52 Ramos E, Valls C, Martinez L , et al. Preoperative staging of patients with liver metastases of colorectal carcinoma. Does PET/CT really add something to multidetector CT?. Ann Surg Oncol 2011; 18 (9) 2654-2661
  CrossrefPubMedGoogle Scholar
• 53 Shin SS, Jeong YY, Min JJ, Kim HR, Chung TW, Kang HK. Preoperative staging of colorectal cancer: CT vs. integrated FDG PET/CT. Abdom Imaging 2008; 33 (3) 270-277
  CrossrefPubMedGoogle Scholar
• 54 Spatz J, Holl G, Sciuk J, Anthuber M, Arnholdt HM, Märkl B. Neoadjuvant chemotherapy affects staging of colorectal liver metastasis—a comparison of PET, CT and intraoperative ultrasound. Int J Colorectal Dis 2011; 26 (2) 165-171
  CrossrefPubMedGoogle Scholar
• 55 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 (5) 1461-1469
  CrossrefPubMedGoogle Scholar
• 56 Niekel MC, Bipat S, Stoker J. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology 2010; 257 (3) 674-684
  CrossrefPubMedGoogle Scholar
• 57 Zech CJ, Herrmann KA, Reiser MF, Schoenberg SO. MR imaging in patients with suspected liver metastases: value of liver-specific contrast agent Gd-EOB-DTPA. Magn Reson Med Sci 2007; 6 (1) 43-52
  CrossrefPubMedGoogle Scholar
• 58 Scharitzer M, Ba-Ssalamah A, Ringl H , et al. Preoperative evaluation of colorectal liver metastases: comparison between gadoxetic acid-enhanced 3.0-T MRI and contrast-enhanced MDCT with histopathological correlation. Eur Radiol 2013; 23 (8) 2187-2196
  CrossrefPubMedGoogle Scholar
• 59 Muhi A, Ichikawa T, Motosugi U , et al. Diagnosis of colorectal hepatic metastases: comparison of contrast-enhanced CT, contrast-enhanced US, superparamagnetic iron oxide-enhanced MRI, and gadoxetic acid-enhanced MRI. J Magn Reson Imaging 2011; 34 (2) 326-335
  CrossrefPubMedGoogle Scholar
• 60 Kulemann V, Schima W, Tamandl D , et al. Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI?. Eur J Radiol 2011; 79 (2) e1-e6
  PubMedGoogle Scholar
• 61 Valls C, Andía E, Sánchez A , et al. Hepatic metastases from colorectal cancer: preoperative detection and assessment of resectability with helical CT. Radiology 2001; 218 (1) 55-60
  CrossrefPubMedGoogle Scholar
• 62 Bruegel M, Gaa J, Waldt S , et al. Diagnosis of hepatic metastasis: comparison of respiration-triggered diffusion-weighted echo-planar MRI and five t2-weighted turbo spin-echo sequences. AJR Am J Roentgenol 2008; 191 (5) 1421-1429
  CrossrefPubMedGoogle Scholar
• 63 Parikh T, Drew SJ, Lee VS , et al. Focal liver lesion detection and characterization with diffusion-weighted MR imaging: comparison with standard breath-hold T2-weighted imaging. Radiology 2008; 246 (3) 812-822
  CrossrefPubMedGoogle Scholar
• 64 Holzapfel K, Eiber MJ, Fingerle AA, Bruegel M, Rummeny EJ, Gaa J. Detection, classification, and characterization of focal liver lesions: Value of diffusion-weighted MR imaging, gadoxetic acid-enhanced MR imaging and the combination of both methods. Abdom Imaging 2012; 37 (1) 74-82
  CrossrefPubMedGoogle Scholar
• 65 Brouquet A, Abdalla EK, Kopetz S , et al. High survival rate after two-stage resection of advanced colorectal liver metastases: response-based selection and complete resection define outcome. J Clin Oncol 2011; 29 (8) 1083-1090
  CrossrefPubMedGoogle Scholar
• 66 Shindoh J, Loyer EM, Kopetz S , et al. Optimal morphologic response to preoperative chemotherapy: an alternate outcome end point before resection of hepatic colorectal metastases. J Clin Oncol 2012; 30 (36) 4566-4572
  CrossrefPubMedGoogle Scholar
• 67 Bischof DA, Clary BM, Maithel SK, Pawlik TM. Surgical management of disappearing colorectal liver metastases. Br J Surg 2013; 100 (11) 1414-1420
  CrossrefPubMedGoogle Scholar
• 68 Knowles B, Welsh FKS, Chandrakumaran K, John TG, Rees M. Detailed liver-specific imaging prior to pre-operative chemotherapy for colorectal liver metastases reduces intra-hepatic recurrence and the need for a repeat hepatectomy. HPB (Oxford) 2012; 14 (5) 298-309
  CrossrefPubMedGoogle Scholar
• 69 Paspulati RM, Partovi S, Herrmann KA, Krishnamurthi S, Delaney CP, Nguyen NC. Comparison of hybrid FDG PET/MRI compared with PET/CT in colorectal cancer staging and restaging: a pilot study. Abdom Imaging 2015; 40 (6) 1415-1425
  CrossrefPubMedGoogle Scholar
• 70 Brendle C, Schwenzer NF, Rempp H , et al. Assessment of metastatic colorectal cancer with hybrid imaging: comparison of reading performance using different combinations of anatomical and functional imaging techniques in PET/MRI and PET/CT in a short case series. Eur J Nucl Med Mol Imaging 2016; 43 (1) 123-132
  CrossrefPubMedGoogle Scholar
• 71 Donati OF, Hany TF, Reiner CS , et al. Value of retrospective fusion of PET and MR images in detection of hepatic metastases: comparison with 18F-FDG PET/CT and Gd-EOB-DTPA-enhanced MRI. J Nucl Med 2010; 51 (5) 692-699
  CrossrefPubMedGoogle Scholar
• 72 Cascini GL, Avallone A, Delrio P , et al. 18F-FDG PET is an early predictor of pathologic tumor response to preoperative radiochemotherapy in locally advanced rectal cancer. J Nucl Med 2006; 47 (8) 1241-1248
  PubMedGoogle Scholar