Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Is the Mixed Use of Magnetic Resonance Enterography and Computed Tomography Enterography Adequate for Routine Periodic Follow-Up of Bowel Inflammation in Patients with Crohn's Disease?

  • Jiyeon Ha (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Seong Ho Park (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Jung Hee Son (Department of Radiology, Inje University Haundae Paik Hospital) ;
  • Ji Hun Kang (Department of Radiology, Hanyang University Guri Hospital) ;
  • Byong Duk Ye (Inflammatory Bowel Disease Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • So Hyun Park (Department of Radiology, Gil Medical Center, Gachon University College of Medicine) ;
  • Bohyun Kim (Department of Radiology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Sang Hyun Choi (Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Sang Hyoung Park (Inflammatory Bowel Disease Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Suk-Kyun Yang (Inflammatory Bowel Disease Center, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2021.01.21
  • Accepted : 2021.06.30
  • Published : 2022.01.01
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Abstract

Objective: Computed tomography enterography (CTE) and magnetic resonance enterography (MRE) are considered substitutes for each other for evaluating Crohn's disease (CD). However, the adequacy of mixing them for routine periodic follow-up for CD has not been established. This study aimed to compare MRE alone with the mixed use of CTE and MRE for the periodic follow-up of small bowel inflammation in patients with CD. Materials and Methods: We retrospectively compared two non-randomized groups, each comprising 96 patients with CD. One group underwent CTE and MRE (MRE followed by CTE or vice versa) for the follow-up of CD (interval, 13-27 months [median, 22 months]), and the other group underwent MRE alone (interval, 15-26 months [median, 21 months]). However, these two groups were similar in clinical characteristics. Three independent readers from three different institutions determined whether inflammation had decreased, remained unchanged, or increased within the entire small bowel and the terminal ileum based on sequential enterography of the patients after appropriate blinding. We compared the two groups for inter-reader agreement and accuracy (terminal ileum only) using endoscopy as the reference standard for enterographic interpretation. Results: The inter-reader agreement was greater in the MRE alone group for the entire small bowel (intraclass correlation coefficient [ICC]: 0.683 vs. 0.473; p = 0.005) and the terminal ileum (ICC: 0.656 vs. 0.490; p = 0.030). The interpretation accuracy was higher in the MRE alone group without statistical significance (70.9%-74.5% vs. 57.9%-64.9% in individual readers; adjusted odds ratio = 3.21; p = 0.077). Conclusion: The mixed use of CTE and MRE was inferior to MRE alone in terms of inter-reader reliability and could probably be less accurate than MRE alone for routine monitoring of small bowel inflammation in patients with CD. Therefore, the consistent use of MRE is favored for this purpose.

Keywords

References

  1. Peyrin-Biroulet L, Sandborn W, Sands BE, Reinisch W, Bemelman W, Bryant RV, et al. Selecting therapeutic targets in inflammatory bowel disease (STRIDE): determining therapeutic goals for treat-to-target. Am J Gastroenterol 2015;110:1324-1338 https://doi.org/10.1038/ajg.2015.233
  2. Park SH, Ye BD, Lee TY, Fletcher JG. Computed tomography and magnetic resonance small bowel enterography: current status and future trends focusing on Crohn's disease. Gastroenterol Clin North Am 2018;47:475-499 https://doi.org/10.1016/j.gtc.2018.04.002
  3. Bruining DH, Bhatnagar G, Rimola J, Taylor S, Zimmermann EM, Fletcher JG. CT and MR enterography in Crohn's disease: current and future applications. Abdom Imaging 2015;40:965-974 https://doi.org/10.1007/s00261-015-0360-9
  4. Kim DH, Chang KJ, Fowler KJ, Cash BD, Garcia EM, Kambadakone AR, et al. ACR appropriateness Criteria® Crohn disease. J Am Coll Radiol 2020;17:S81-S99 https://doi.org/10.1016/j.jacr.2020.01.030
  5. Grand DJ, Beland M, Harris A. Magnetic resonance enterography. Radiol Clin North Am 2013;51:99-112 https://doi.org/10.1016/j.rcl.2012.09.007
  6. Qiu Y, Mao R, Chen BL, Li XH, He Y, Zeng ZR, et al. Systematic review with meta-analysis: magnetic resonance enterography vs. computed tomography enterography for evaluating disease activity in small bowel Crohn's disease. Aliment Pharmacol Ther 2014;40:134-146 https://doi.org/10.1111/apt.12815
  7. Liu W, Liu J, Xiao W, Luo G. A diagnostic accuracy meta-analysis of CT and MRI for the evaluation of small bowel Crohn disease. Acad Radiol 2017;24:1216-1225 https://doi.org/10.1016/j.acra.2017.04.013
  8. Ordas I, Rimola J, Rodriguez S, Paredes JM, MartinezPerez MJ, Blanc E, et al. Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn's disease. Gastroenterology 2014;146:374-382.e1 https://doi.org/10.1053/j.gastro.2013.10.055
  9. Tielbeek JA, Lowenberg M, Bipat S, Horsthuis K, Ponsioen CY, D'Haens GR, et al. Serial magnetic resonance imaging for monitoring medical therapy effects in Crohn's disease. Inflamm Bowel Dis 2013;19:1943-1950 https://doi.org/10.1097/MIB.0b013e3182905536
  10. Van Assche G, Herrmann KA, Louis E, Everett SM, Colombel JF, Rahier JF, et al. Effects of infliximab therapy on transmural lesions as assessed by magnetic resonance enteroclysis in patients with ileal Crohn's disease. J Crohns Colitis 2013;7:950-957 https://doi.org/10.1016/j.crohns.2013.01.011
  11. Prezzi D, Bhatnagar G, Vega R, Makanyanga J, Halligan S, Taylor SA. Monitoring Crohn's disease during anti-TNF-α therapy: validation of the magnetic resonance enterography global score (MEGS) against a combined clinical reference standard. Eur Radiol 2016;26:2107-2117 https://doi.org/10.1007/s00330-015-4036-1
  12. Thierry ML, Rousseau H, Pouillon L, Girard-Gavanier M, Baumann C, Lopez A, et al. Accuracy of diffusion-weighted magnetic resonance imaging in detecting mucosal healing and treatment response, and in predicting surgery, in Crohn's disease. J Crohns Colitis 2018;12:1180-1190 https://doi.org/10.1093/ecco-jcc/jjy098
  13. Huh J, Kim KJ, Park SH, Park SH, Yang SK, Ye BD, et al. Diffusion-weighted MR enterography to monitor bowel inflammation after medical therapy in Crohn's disease: a prospective longitudinal study. Korean J Radiol 2017;18:162-172 https://doi.org/10.3348/kjr.2017.18.1.162
  14. Wu YW, Tang YH, Hao NX, Tang CY, Miao F. Crohn's disease: CT enterography manifestations before and after treatment. Eur J Radiol 2012;81:52-59
  15. Bruining DH, Loftus EV Jr, Ehman EC, Siddiki HA, Nguyen DL, Fidler JL, et al. Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with Crohn's disease. Clin Gastroenterol Hepatol 2011;9:679-683.e1 https://doi.org/10.1016/j.cgh.2011.04.025
  16. Lopes S, Andrade P, Afonso J, Cunha R, Rodrigues-Pinto E, Ramos I, et al. Monitoring Crohn's disease activity: endoscopy, fecal markers and computed tomography enterography. Therap Adv Gastroenterol 2018;11:1756284818769075
  17. Park SH, Yang SK, Park SK, Kim JW, Yang DH, Jung KW, et al. Long-term prognosis of Crohn's disease and its temporal change between 1981 and 2012: a hospital-based cohort study from Korea. Inflamm Bowel Dis 2014;20:488-494 https://doi.org/10.1097/01.MIB.0000441203.56196.46
  18. Seo N, Park SH, Kim KJ, Kang BK, Lee Y, Yang SK, 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;278:762-772 https://doi.org/10.1148/radiol.2015150809
  19. Choi IY, Park SH, Park SH, Yu CS, Yoon YS, Lee JL, et al. CT enterography for surveillance of anastomotic recurrence within 12 months of bowel resection in patients with Crohn's disease: an observational study using an 8-year registry. Korean J Radiol 2017;18:906-914 https://doi.org/10.3348/kjr.2017.18.6.906
  20. Bruining DH, Zimmermann EM, Loftus EV Jr, Sandborn WJ, Sauer CG, Strong SA. Consensus recommendations for evaluation, interpretation, and utilization of computed tomography and magnetic resonance enterography in patients with small bowel Crohn's disease. Gastroenterology 2018;154:1172-1194 https://doi.org/10.1053/j.gastro.2017.11.274
  21. Koulaouzidis A, Sipponen T, Nemeth A, Makins R, Kopylov U, Nadler M, et al. Association between fecal calprotectin levels and small-bowel inflammation score in capsule endoscopy: a multicenter retrospective study. Dig Dis Sci 2016;61:2033-2040 https://doi.org/10.1007/s10620-016-4104-7
  22. Noh SM, Oh EH, Park SH, Lee JB, Kim JY, Park JC, et al. Association of faecal calprotectin level and combined endoscopic and radiological healing in patients with Crohn's disease receiving anti-tumour necrosis factor therapy. J Crohns Colitis 2020;14:1231-1240 https://doi.org/10.1093/ecco-jcc/jjaa042
  23. Hernaez R. Reliability and agreement studies: a guide for clinical investigators. Gut 2015;64:1018-1027 https://doi.org/10.1136/gutjnl-2014-308619
  24. Park JE, Han K, Sung YS, Chung MS, Koo HJ, Yoon HM, et al. Selection and reporting of statistical methods to assess reliability of a diagnostic test: conformity to recommended methods in a peer-reviewed journal. Korean J Radiol 2017;18:888-897 https://doi.org/10.3348/kjr.2017.18.6.888
  25. Park SH. DWI at MR enterography for evaluating bowel inflammation in Crohn disease. AJR Am J Roentgenol 2016;207:40-48 https://doi.org/10.2214/AJR.15.15862
  26. Maaser C, Sturm A, Vavricka SR, Kucharzik T, Fiorino G, Annese V, et al. ECCO-ESGAR guideline for diagnostic assessment in IBD part 1: initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis 2019;13:144-164 https://doi.org/10.1093/ecco-jcc/jjy113
  27. Turner D, Ricciuto A, Lewis A, D'Amico F, Dhaliwal J, Griffiths AM, et al. STRIDE-II: an update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) initiative of the International Organization for the Study of IBD (IOIBD): determining therapeutic goals for treat-to-target strategies in IBD. Gastroenterology 2021;160:1570-1583 https://doi.org/10.1053/j.gastro.2020.12.031
  28. Son JH, Kim SH, Cho EY, Ryu KH. Comparison of diagnostic performance between 1 millisievert CT enterography and half-standard dose CT enterography for evaluating active inflammation in patients with Crohn's disease. Abdom Radiol (NY) 2017;43:1558-1566 https://doi.org/10.1007/s00261-017-1359-1
  29. Gandhi NS, Baker ME, Goenka AH, Bullen JA, Obuchowski NA, Remer EM, et al. Diagnostic accuracy of CT enterography for active inflammatory terminal ileal Crohn disease: comparison of full-dose and half-dose images reconstructed with FBP and half-dose images with SAFIRE. Radiology 2016;280:436-445 https://doi.org/10.1148/radiol.2016151281
  30. Fletcher JG, Hara AK, Fidler JL, Silva AC, Barlow JM, Carter RE, et al. Observer performance for adaptive, image-based denoising and filtered back projection compared to scanner-based iterative reconstruction for lower dose CT enterography. Abdom Imaging 2015;40:1050-1059 https://doi.org/10.1007/s00261-015-0384-1
  31. Murphy KP, Crush L, Twomey M, McLaughlin PD, Mildenberger IC, Moore N, et al. Model-based iterative reconstruction in CT enterography. AJR Am J Roentgenol 2015;205:1173-1181 https://doi.org/10.2214/AJR.14.13321
  32. Johnson E, Megibow AJ, Wehrli NE, O'Donnell T, Chandarana H. CT enterography at 100 kVp with iterative reconstruction compared to 120 kVp filtered back projection: evaluation of image quality and radiation dose in the same patients. Abdom Imaging 2014;39:1255-1260 https://doi.org/10.1007/s00261-014-0156-3
  33. Lee SJ, Park SH, Kim AY, Yang SK, Yun SC, Lee SS, et al. A prospective comparison of standard-dose CT enterography and 50% reduced-dose CT enterography with and without noise reduction for evaluating Crohn disease. AJR Am J Roentgenol 2011;197:50-57 https://doi.org/10.2214/AJR.11.6582
  34. Zakeri N, Pollok RC. Diagnostic imaging and radiation exposure in inflammatory bowel disease. World J Gastroenterol 2016;22:2165-2178 https://doi.org/10.3748/wjg.v22.i7.2165
  35. Rimola J, Rodriguez S, Garcia-Bosch O, Ordas I, Ayala E, Aceituno M, et al. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease. Gut 2009;58:1113-1120 https://doi.org/10.1136/gut.2008.167957
  36. Ordas I, Rimola J, Alfaro I, Rodriguez S, Castro-Poceiro J, Ramirez-Morros A, et al. Development and validation of a simplified magnetic resonance index of activity for Crohn's disease. Gastroenterology 2019;157:432-439.e1 https://doi.org/10.1053/j.gastro.2019.03.051
  37. Steward MJ, Punwani S, Proctor I, Adjei-Gyamfi Y, Chatterjee F, Bloom S, 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;81:2080-2088 https://doi.org/10.1016/j.ejrad.2011.07.013
  38. Oussalah A, Laurent V, Bruot O, Bressenot A, Bigard MA, Regent D, et al. Diffusion-weighted magnetic resonance without bowel preparation for detecting colonic inflammation in inflammatory bowel disease. Gut 2010;59:1056-1065  https://doi.org/10.1136/gut.2009.197665