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Review

Magnetic resonance enterography in Crohn’s disease patients: current state of the art and future perspectives

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 657-667 | Received 04 Mar 2021, Accepted 03 Jun 2021, Published online: 30 Jul 2021

References

  • Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2017 Dec 23;390(10114):2769–2778.
  • Thia KT, Sandborn WJ, Harmsen WS, et al. Risk Factors Associated With Progression to Intestinal Complications of Crohn’s Disease in a Population-Based Cohort. Gastroenterology. 2010 Oct;139(4):1147–1155.
  • Cosnes J, Cattan S, Blain A, et al. Long-Term Evolution of Disease Behavior of Crohn’s Disease. Inflamm Bowel Dis. 2002 Jul 8;8(4):244–250.
  • Kroeker KI, Lam S, Birchall I, et al. Patients with IBD are exposed to high levels of ionizing radiation through CT scan diagnostic imaging: a five-year study. J Clin Gastroenterol. 2011 Jan;45(1):34–39.
  • Cicero G, Mazziotti S. Crohn’s disease at radiological imaging: focus on techniques and intestinal tract. Intest Res. 2020 Nov 25. DOI:10.5217/ir.2020.00097.
  • Ripollés T, Rausell N, Paredes JM, et al. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn’s disease: a comparison with surgical histopathology analysis. J Crohns Colitis. 2013 Mar 7;(2): 120–128. Doi: 10.1016/j.crohns.2012.03.002.
  • Mocci G, Migaleddu V, Cabras F, et al. SICUS and CEUS imaging in Crohn’s disease: an update. J Ultrasound. 2017 Jan 2;20(1):1–9.
  • Kucharzik T, Wittig BM, Helwig U, et al., TRUST study group. Use of Intestinal Ultrasound to Monitor Crohn’s Disease Activity. Clin Gastroenterol Hepatol. 2017 Apr;15(4):535–542.e2.
  • Bruining DH, Zimmermann EM, Loftus EV, et al., Society of Abdominal Radiology Crohn’s Disease-Focused Panel. Consensus Recommendations for Evaluation, Interpretation, and Utilization of Computed Tomography and Magnetic Resonance Enterography in Patients With Small Bowel Crohn’s Disease. Radiology. 2018 Mar;286(3):776–799.
  • Cicero G, Ascenti G, Blandino A, et al. Elective surgery outcomes in inflammatory bowel disease: interpretation at magnetic resonance enterography. Jpn J Radiol. 2021 Feb 24. Doi: 10.1007/s11604-021-01103-x.
  • Grand DJ, Guglielmo FF, Al-Hawary MM. MR enterography in Crohn’s disease: current consensus on optimal imaging technique and future advances from the SAR Crohn’s disease-focused panel. Abdom Imaging. 2015 Jun;40(5):953–964.
  • Sturm A, Maaser C, Calabrese E, et al.,European Crohn’s and Colitis Organisation [ECCO] and the European Society of Gastrointestinal and Abdominal Radiology [ESGAR]. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 2: IBD scores and general principles and technical aspects. J Crohns Colitis. 2019 Mar 26; 13: 3. 273–284.
  • Boone D, Taylor SA. Magnetic Resonance of the Small Bowel: how to Do It. Magnetic Resonance Imaging Clinics of North America. 2020 Feb 1;28(1):17–30.
  • Quencer KB, Nimkin K, Mino-Kenudson M, et al. Detecting active inflammation and fibrosis in pediatric Crohn’s disease: prospective evaluation of MR-E and CT-E. Abdom Imaging. 2013 Aug;38(4):705–713.
  • Rimola J, Alvarez-Cofiño A, Pérez-Jeldres T, et al. Increasing efficiency of MRE for diagnosis of Crohn’s disease activity through proper sequence selection: a practical approach for clinical trials. Abdom Radiol (NY). 2017 Dec;42(12):2783–2791.
  • Kim K-J, Lee Y, Park SH, et al. Diffusion-weighted MR Enterography for Evaluating Crohnʼs Disease. Inflamm Bowel Dis. 2015 Jan;21(1):101–109.
  • Soydan L, Demir AA, Ozer S, et al. Can MR Enterography and Diffusion-Weighted Imaging Predict Disease Activity Assessed by Simple Endoscopic Score for Crohn’s Disease? Journal of the Belgian Society of Radiology. 2019 Jan 18;103(1):10.
  • Barat M, Hoeffel C, Bouquot M, et al. Preoperative evaluation of small bowel complications in Crohn’s disease: comparison of diffusion-weighted and contrast-enhanced MR imaging. Eur Radiol. 2019 Apr;29(4):2034–2044.
  • Seo N, Park SH, Kim K-J, et al. MR Enterography for the Evaluation of Small-Bowel Inflammation in Crohn Disease by Using Diffusion-weighted Imaging without Intravenous Contrast Material: a Prospective Noninferiority Study. Radiology. 2016 Mar;278(3):762–772.
  • Gollifer RM, Menys A, Plumb A, et al. Automated versus subjective assessment of spatial and temporal MRI small bowel motility in Crohn’s disease. Clin Radiol. 2019 Oct;74(10):814.e9–814.e19.
  • Hahnemann ML, Nensa F, Kinner S, et al. Motility mapping as evaluation tool for bowel motility: initial results on the development of an automated color-coding algorithm in cine MRI. J Magn Reson Imaging. 2015 Feb;41(2):354–360.
  • Menys A, Taylor SA, Emmanuel A, et al. Global small bowel motility: assessment with dynamic MR imaging. Radiology. 2013 Nov;269(2):443–450.
  • Lambrou T, Chaudhry NA, Grajo JR, et al. Small bowel stricture is associated with abnormal motility on the cine MRI sequence in patients with Crohn’s disease. Eur J Radiol. 2019Sep;118:264–270.
  • Menys A, Puylaert C, Tutein Nolthenius CE, et al. Quantified Terminal Ileal Motility during MR Enterography as a Biomarker of Crohn Disease Activity: prospective Multi-Institution Study. Radiology. 2018 Nov;289(2):428–435.
  • Dreja J, Ekberg O, Leander P, et al. Volumetric analysis of small bowel motility in an unselected cohort of patients with Crohn’s disease. Neurogastroenterol Motil. 2020 Oct;32(10):e13909.
  • Li X-H, Mao R, Huang S-Y, et al. Characterization of Degree of Intestinal Fibrosis in Patients with Crohn Disease by Using Magnetization Transfer MR Imaging. Radiology. 2018 May;287(2):494–503.
  • Cicero G, Mondello S, Wichmann JL, et al. Fast Magnetic Resonance Enterography Protocol for the Evaluation of Patients with Crohn’s Disease: a Pilot Study. Journal of Clinical Imaging Science. 2020 May 2;10: 25.
  • Jhaveri KS, Sagheb S, Guimaraes L, et al. Evaluation of Crohn Disease Activity Using a Potential Abbreviated MRE Protocol Consisting of Balanced Steady-State Free Precession MRI Only Versus Full-Protocol MRE. AJR Am J Roentgenol. 2020 Dec 9; 1–9. DOI:10.2214/AJR.20.22856.
  • Cronin CG, Dowd G, Mhuircheartaigh JN, et al. Hypotonic MR duodenography with water ingestion alone: feasibility and technique. Eur Radiol. 2009 Jul;19(7):1731–1735.
  • Froehlich JM, Daenzer M, von Weymarn C, et al. Aperistaltic effect of hyoscine N-butylbromide versus glucagon on the small bowel assessed by magnetic resonance imaging. Eur Radiol. 2009 Jun;19(6):1387–1393.
  • Rao A, Sitheeque F, Gustafson S, et al. MR enterography - Impact on image quality between single- versus split-dose Buscopan. J Med Imaging Radiat Oncol. 2020 Jun;64(3):331–337.
  • Cicero G, Mazziotti S. Crohn’s disease at radiological imaging: focus on techniques and intestinal tract. Intest Res. 2020 Nov 25. DOI:10.5217/ir.2020.00097.
  • Rimola J, Rodriguez S, García-Bosch O, et al. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn’s disease. Gut. 2009 Aug;58(8):1113–1120.
  • Ordás I, Rimola J, Alfaro I, et al. Development and Validation of a Simplified Magnetic Resonance Index of Activity for Crohn’s Disease. Gastroenterology. 2019 Aug;157(2):432–439.e1.
  • Buisson A, Joubert A, Montoriol PF, et al. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn’s disease. Aliment Pharmacol Ther. 2013;37(5):537–545.
  • Steward MJ, Punwani S, Proctor I, et al. Non-perforating small bowel Crohn’s disease assessed by MRI enterography: derivation and histopathological validation of an MR-based activity index. Eur J Radiol. 2012 Sep;81(9):2080–2088.
  • Makanyanga JC, Pendsé D, Dikaios N, et al. Evaluation of Crohn’s disease activity: initial validation of a magnetic resonance enterography global score (MEGS) against faecal calprotectin. Eur Radiol. 2014 Feb;24(2):277–287.
  • Pariente B, Cosnes J, Danese S, et al. Development of the Crohn’s disease digestive damage score, the Lémann score. Inflamm Bowel Dis. 2011 Jun;17(6):1415–1422.
  • Kitazume Y, Fujioka T, Takenaka K, et al. Crohn Disease: a 5-Point MR Enterocolonography Classification Using Enteroscopic Findings. AJR Am J Roentgenol. 2019 Jan;212(1):67–76.
  • Rozendorn N, Amitai MM, Eliakim RA, et al. A review of magnetic resonance enterography-based indices for quantification of Crohn’s disease inflammation. Therap Adv Gastroenterol. 2018;11:1756284818765956.
  • Mary JY, Modigliani R. Development and validation of an endoscopic index of the severity for Crohn’s disease: a prospective multicentre study. Gut. 1989;30:983–989.
  • Capozzi N, Ordás I, Fernandez-Clotet A, et al. Validation of the Simplified Magnetic Resonance Index of Activity [sMARIA] Without Gadolinium-enhanced Sequences for Crohn’s Disease. J Crohns Colitis. 2020 Sep 7;14(8):1074–1081.
  • Kim JS, Jang HY, Park SH, et al. MR Enterography Assessment of Bowel Inflammation Severity in Crohn Disease Using the MR Index of Activity Score: modifying Roles of DWI and Effects of Contrast Phases. AJR Am J Roentgenol. 2017 May;208(5):1022–1029.
  • Tsai R, Mintz A, Lin M, et al. Magnetic resonance enterography features of small bowel Crohn’s disease activity: an inter-rater reliability study of small bowel active inflammation in clinical practice setting. Br J Radiol. 2019 Jul;92(1099):20180930.
  • Henriksen M, Jahnsen J, Lygren I, et al. Clinical course in Crohn’s disease: results of a five-year population-based follow-up study (the IBSEN study). Scand J Gastroenterol. 2007 May;42(5):602–610.
  • Panés J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther. 2011 Jul;34(2):125–145.
  • Allocca M, Fiorino G, Bonifacio C, et al. Noninvasive Multimodal Methods to Differentiate Inflamed vs Fibrotic Strictures in Patients With Crohn’s Disease. Clin Gastroenterol Hepatol. 2019 Nov;17(12):2397–2415.
  • Zappa M, Stefanescu C, Cazals-Hatem D, et al. Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn’s disease? A retrospective comparison with surgical pathologic analysis. Inflamm Bowel Dis. 2011 Apr;17(4):984–993.
  • Rimola J, Planell N, Rodríguez S, et al. Characterization of inflammation and fibrosis in Crohn’s disease lesions by magnetic resonance imaging. Am J Gastroenterol. 2015 Mar;110(3):432–440.
  • Ippolito D, Lombardi S, Talei Franzesi C, et al. Dynamic Contrast-Enhanced MR with Quantitative Perfusion Analysis of Small Bowel in Vascular Assessment between Inflammatory and Fibrotic Lesions in Crohn’s Disease: a Feasibility Study. Contrast Media Mol Imaging. 2019;2019:1767620.
  • Tielbeek JA, Ziech ML, Li Z, et al. Evaluation of conventional, dynamic contrast enhanced and diffusion weighted MRI for quantitative Crohn’s disease assessment with histopathology of surgical specimens. Eur Radiol. 2014 Mar;24(3):619–629.
  • Kovanlikaya A, Beneck D, Rose M, et al. Quantitative apparent diffusion coefficient (ADC) values as an imaging biomarker for fibrosis in pediatric Crohn’s disease: preliminary experience. Abdom Imaging. 2015 Jun;40(5):1068–1074.
  • Rosenbaum DG, Rose ML, Solomon AB, et al. Longitudinal diffusion-weighted imaging changes in children with small bowel Crohn’s disease: preliminary experience. Abdom Imaging. 2015 Jun;40(5):1075–1080.
  • Caruso A, Angriman I, Scarpa M, et al. Diffusion-weighted magnetic resonance for assessing fibrosis in Crohn’s disease. Abdom Radiol (NY). 2020 Aug;45(8):2327–2335.
  • Peyrin-Biroulet L, Sandborn W, Sands BE, et al. Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): determining Therapeutic Goals for Treat-to-Target. Am J Gastroenterol. 2015 Sep;110(9):1324–1338.
  • Deepak P, Fletcher JG, Fidler JL, et al. Radiological Response Is Associated With Better Long-Term Outcomes and Is a Potential Treatment Target in Patients With Small Bowel Crohn’s Disease. Am J Gastroenterol. 2016 Jul;111(7):997–1006.
  • Ordás I, Rimola J, Rodríguez S, et al. Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn’s disease. Gastroenterology. 2014 Feb;146(2):374–82.e1.
  • Hallé E, Azahaf M, Duveau N, et al. Radiological Response Is Associated with Better Outcomes and Should Be Considered a Therapeutic Target in Crohn’s Disease. Dig Dis Sci. 2020 Sep;65(9):2664–2674.
  • Bouhnik Y, Carbonnel F, Laharie D, et al., GETAID CREOLE Study Group. Efficacy of adalimumab in patients with Crohn’s disease and symptomatic small bowel stricture: a multicentre, prospective, observational cohort (CREOLE) study. Gut. 2018 Jan;67(1):53–60.
  • Amitai MM, Klang E, Levartovsky A, et al. Diffusion-weighted magnetic resonance enterography for prediction of response to tumor necrosis factor inhibitors in stricturing Crohn’s disease. Abdom Radiol (NY). 2018 Dec;43(12):3207–3212.
  • Gordic S, Bane O, Kihira S, et al. Evaluation of ileal Crohn’s disease response to TNF antagonists: validation of MR enterography for assessing response. Initial results. Eur J Radiol Open. 2020 Jan 28;7: 100217.
  • Rimola J, Fernàndez-Clotet A, Capozzi N, et al. Pre-treatment magnetic resonance enterography findings predict the response to TNF-alpha inhibitors in Crohn’s disease. Aliment Pharmacol Ther. 2020 Nov;52(10):1563–1573.
  • Gallego JC, De Juan C, Echarri A, et al. Small-Bowel Crohn Disease Treated With Anti-Tumor Necrosis Factor-α Therapy: MR Enterography Score Changes After 1 Year Predict Long-Term Outcomes. AJR Am J Roentgenol. 2019 Dec;213(6):1240–1246.
  • Kim C, Park SH, Yang SK, et al. Endoscopic Complete Remission of Crohn Disease After Anti-Tumor Necrosis Factor-α Therapy: CT Enterographic Findings and Their Clinical Implications. AJR Am J Roentgenol. 2016 Jun;206(6):1208–1216.
  • Rimola J, Alfaro I, Fernández-Clotet A, et al. Persistent damage on magnetic resonance enterography in patients with Crohn’s disease in endoscopic remission. Aliment Pharmacol Ther. 2018 Dec;48(11–12):1232–1241.
  • Lunder AK, Bakstad LT, Jahnsen J, et al. Assessment of Bowel Inflammation and Strictures by Magnetic Resonance Enterography in Long-term Crohn’s Disease. J Crohns Colitis. 2019 Apr 26;13(5):607–614.
  • Naziroglu RE, Puylaert CAJ, Tielbeek JAW, et al. Semi-automatic bowel wall thickness measurements on MR enterography in patients with Crohn’s disease. Br J Radiol. 2017 Jun;90(1074):20160654.
  • Makanyanga J, Ganeshan B, Rodriguez-Justo M, et al. MRI texture analysis (MRTA) of T2-weighted images in Crohn’s disease may provide information on histological and MRI disease activity in patients undergoing ileal resection. Eur Radiol. 2017 Feb;27(2):589–597.
  • Tabari A, Kilcoyne A, Jeck WR, et al. Texture analysis of magnetic resonance enterography contrast enhancement can detect fibrosis in Crohn disease strictures. J Pediatr Gastroenterol Nutr. 2019 Nov;69(5):533–538.

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