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Diffusion-Weighted MR Enterography to Monitor Bowel Inflammation after Medical Therapy in Crohn's Disease: A Prospective Longitudinal Study

  • Huh, Jimi (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Kim, Kyung Jo (Department of Gastroenterology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Park, Seong Ho (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Park, So Hyun (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Yang, Suk-Kyun (Department of Gastroenterology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Ye, Byong Duk (Department of Gastroenterology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Park, Sang Hyoung (Department of Gastroenterology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Han, Kyunghwa (Department of Radiology and Research Institute of Radiological Science, Yonsei University College of Medicine) ;
  • Kim, Ah Young (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • Received : 2016.04.30
  • Accepted : 2016.08.10
  • Published : 2017.01.01

Abstract

Objective: To prospectively evaluate the performance of diffusion-weighted imaging (DWI) to monitor bowel inflammation after medical therapy for Crohn's disease (CD). Materials and Methods: Before and following 1-2 years of medical therapy, between October 2012 and May 2015, 18 randomly selected adult CD patients (male:female, 13:5; mean $age{\pm}SD$, $25.8{\pm}7.9years$ at the time of enrollment) prospectively underwent MR enterography (MRE) including DWI ($b=900s/mm^2$) and ileocolonoscopy. Thirty-seven prospectively defined index lesions (one contiguous endoscopy-confirmed inflamed area chosen from each inflamed anatomical bowel segment; 1-4 index lesions per patient; median, 2 lesions) were assessed on pre- and post-treatment MRE and endoscopy. Visual assessment of treatment responses on DWI in 4 categories including complete remission and reduced, unchanged or increased inflammation, and measurements of changes in apparent diffusion coefficient (${\Delta}ADC$), i.e., pre-treatment-post-treatment, were performed by 2 independent readers. Endoscopic findings and CD MRI activity index (CDMI) obtained using conventional MRE served as reference standards. Results: ${\Delta}ADC$ significantly differed between improved (i.e., complete remission and reduced inflammation) and unimproved (i.e., unchanged or increased inflammation) lesions: $mean{\pm}SD$ (${\times}10^{-3}mm^2/s$) of $-0.65{\pm}0.58$ vs. $0.06{\pm}0.15$ for reader 1 (p = 0.022) and $-0.68{\pm}0.56$ vs. $0.10{\pm}0.26$ for reader 2 (p = 0.025). DWI accuracy for diagnosing complete remission or improved inflammation ranged from 76% (28/37) to 84% (31/37). A significant negative correlation was noted between ${\Delta}ADC$ and ${\Delta}CDMI$ for both readers with correlation coefficients of -0.438 and -0.461, respectively (p < 0.05). Conclusion: DWI is potentially a feasible tool to monitor quantitatively and qualitatively bowel inflammation of CD after medical treatment.

Keywords

References

  1. Choi SH, Kim KW, Lee JY, Kim KJ, Park SH. Diffusion-weighted magnetic resonance enterography for evaluating bowel inflammation in Crohn's disease: a systematic review and meta-analysis. Inflamm Bowel Dis 2016;22:669-679 https://doi.org/10.1097/MIB.0000000000000607
  2. 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
  3. Cheifetz AS. Management of active Crohn disease. JAMA 2013;309:2150-2158 https://doi.org/10.1001/jama.2013.4466
  4. Lichtenstein GR, Hanauer SB, Sandborn WJ; Practice Parameters Committee of American College of Gastroenterology. Management of Crohn's disease in adults. Am J Gastroenterol 2009;104:465-483; quiz 464, 484 https://doi.org/10.1038/ajg.2008.168
  5. Ordas I, Feagan BG, Sandborn WJ. Early use of immunosuppressives or TNF antagonists for the treatment of Crohn's disease: time for a change. Gut 2011;60:1754-1763 https://doi.org/10.1136/gutjnl-2011-300934
  6. Sadowski DC, Bernstein CN, Bitton A, Croitoru K, Fedorak RN, Griffiths A; CAG Crohn's Consensus Group. Canadian Association of Gastroenterology Clinical Practice Guidelines: the use of tumour necrosis factor-alpha antagonist therapy in Crohn's disease. Can J Gastroenterol 2009;23:185-202 https://doi.org/10.1155/2009/201430
  7. 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
  8. Buisson A, Hordonneau C, Goutte M, Boyer L, Pereira B, Bommelaer G. Diffusion-weighted magnetic resonance imaging is effective to detect ileocolonic ulcerations in Crohn's disease. Aliment Pharmacol Ther 2015;42:452-460 https://doi.org/10.1111/apt.13287
  9. Tielbeek JA, Ziech ML, Li Z, Lavini C, Bipat S, Bemelman WA, 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;24:619-629 https://doi.org/10.1007/s00330-013-3015-7
  10. Hordonneau C, Buisson A, Scanzi J, Goutorbe F, Pereira B, Borderon C, et al. Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn's disease: validation of quantitative index of activity. Am J Gastroenterol 2014;109:89-98 https://doi.org/10.1038/ajg.2013.385
  11. Caruso A, D'Inca R, Scarpa M, Manfrin P, Rudatis M, Pozza A, et al. Diffusion-weighted magnetic resonance for assessing ileal Crohn's disease activity. Inflamm Bowel Dis 2014;20:1575-1583 https://doi.org/10.1097/MIB.0000000000000128
  12. Ream JM, Dillman JR, Adler J, Khalatbari S, McHugh JB, Strouse PJ, et al. MRI diffusion-weighted imaging (DWI) in pediatric small bowel Crohn disease: correlation with MRI findings of active bowel wall inflammation. Pediatr Radiol 2013;43:1077-1085 https://doi.org/10.1007/s00247-013-2712-3
  13. Neubauer H, Pabst T, Dick A, Machann W, Evangelista L, Wirth C, et al. Small-bowel MRI in children and young adults with Crohn disease: retrospective head-to-head comparison of contrast-enhanced and diffusion-weighted MRI. Pediatr Radiol 2013;43:103-114 https://doi.org/10.1007/s00247-012-2492-1
  14. Buisson A, Joubert A, Montoriol PF, Da Ines D, Hordonneau C, Pereira B, et al. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn's disease. Aliment Pharmacol Ther 2013;37:537-545 https://doi.org/10.1111/apt.12201
  15. Bhatnagar G, Dikaios N, Prezzi D, Vega R, Halligan S, Taylor SA. Changes in dynamic contrast-enhanced pharmacokinetic and diffusion-weighted imaging parameters reflect response to anti-TNF therapy in Crohn's disease. Br J Radiol 2015; 88:20150547 https://doi.org/10.1259/bjr.20150547
  16. Baars JE, Nuij VJ, Oldenburg B, Kuipers EJ, van der Woude CJ. Majority of patients with inflammatory bowel disease in clinical remission have mucosal inflammation. Inflamm Bowel Dis 2012;18:1634-1640 https://doi.org/10.1002/ibd.21925
  17. Peyrin-Biroulet L, Reinisch W, Colombel JF, Mantzaris GJ, Kornbluth A, Diamond R, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn's disease in the SONIC trial. Gut 2014;63:88-95 https://doi.org/10.1136/gutjnl-2013-304984
  18. Catalano OA, Gee MS, Nicolai E, Selvaggi F, Pellino G, Cuocolo A, et al. Evaluation of quantitative PET/MR enterography biomarkers for discrimination of inflammatory strictures from fibrotic strictures in Crohn disease. Radiology 2016;278:792-800 https://doi.org/10.1148/radiol.2015150566
  19. Kovanlikaya A, Beneck D, Rose M, Renjen P, Dunning A, Solomon A, et al. Quantitative apparent diffusion coefficient (ADC) values as an imaging biomarker for fibrosis in pediatric Crohn's disease: preliminary experience. Abdom Imaging 2015;40:1068-1074 https://doi.org/10.1007/s00261-014-0247-1
  20. Adler J, Punglia DR, Dillman JR, Polydorides AD, Dave M, Al-Hawary MM, et al. Computed tomography enterography findings correlate with tissue inflammation, not fibrosis in resected small bowel Crohn's disease. Inflamm Bowel Dis 2012;18:849-856 https://doi.org/10.1002/ibd.21801
  21. Zappa M, Stefanescu C, Cazals-Hatem D, Bretagnol F, Deschamps L, Attar A, 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;17:984-993 https://doi.org/10.1002/ibd.21414
  22. Kim KJ, Lee Y, Park SH, Kang BK, Seo N, Yang SK, et al. Diffusion-weighted MR enterography for evaluating Crohn's disease: how does it add diagnostically to conventional MR enterography? Inflamm Bowel Dis 2015;21:101-109 https://doi.org/10.1097/MIB.0000000000000222
  23. Lennard-Jones JE. Classification of inflammatory bowel disease. Scand J Gastroenterol Suppl 1989;170:2-6; discussion 16-19
  24. Van Assche G, Dignass A, Panes J, Beaugerie L, Karagiannis J, Allez M, et al. The second european evidence-based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis. J Crohns Colitis 2010;4:7-27 https://doi.org/10.1016/j.crohns.2009.12.003
  25. Colombel JF, Rutgeerts PJ, Sandborn WJ, Yang M, Camez A, Pollack PF, et al. Adalimumab induces deep remission in patients with Crohn's disease. Clin Gastroenterol Hepatol 2014;12:414-422.e5 https://doi.org/10.1016/j.cgh.2013.06.019
  26. Colombel JF, Sandborn WJ, Reinisch W, Mantzaris GJ, Kornbluth A, Rachmilewitz D, et al. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 2010;362:1383-1395 https://doi.org/10.1056/NEJMoa0904492
  27. Rutgeerts P, Van Assche G, Sandborn WJ, Wolf DC, Geboes K, Colombel JF, et al. Adalimumab induces and maintains mucosal healing in patients with Crohn's disease: data from the EXTEND trial. Gastroenterology 2012;142:1102-1111.e2 https://doi.org/10.1053/j.gastro.2012.01.035
  28. Mary JY, Modigliani R. Development and validation of an endoscopic index of the severity for Crohn's disease: a prospective multicentre study. Groupe d'Etudes Therapeutiques des Affections Inflammatoires du Tube Digestif (GETAID). Gut 1989;30:983-989 https://doi.org/10.1136/gut.30.7.983
  29. 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
  30. Tielbeek JA, Makanyanga JC, Bipat S, Pendse DA, Nio CY, Vos FM, et al. Grading Crohn disease activity with MRI: interobserver variability of MRI features, MRI scoring of severity, and correlation with Crohn disease endoscopic index of severity. AJR Am J Roentgenol 2013;201:1220-1228 https://doi.org/10.2214/AJR.12.10341
  31. Yang Z, Zhou M. Weighted kappa statistic for clustered matched-pair ordinal data. Comput Stat Data Anal 2015;82:1-18 https://doi.org/10.1016/j.csda.2014.08.004
  32. Kim SY, Park SH. Reply to what is the role of diffusionweighted imaging in ileocolonic Crohn's disease? Inflamm Bowel Dis 2015;21:E9-E10
  33. Bilgili MY. Reproductibility of apparent diffusion coefficients measurements in diffusion-weighted MRI of the abdomen with different b values. Eur J Radiol 2012;81:2066-2068 https://doi.org/10.1016/j.ejrad.2011.06.045
  34. Braithwaite AC, Dale BM, Boll DT, Merkle EM. Short- and midterm reproducibility of apparent diffusion coefficient measurements at 3.0-T diffusion-weighted imaging of the abdomen. Radiology 2009;250:459-465 https://doi.org/10.1148/radiol.2502080849
  35. Kim SY, Lee SS, Byun JH, Park SH, Kim JK, Park B, et al. Malignant hepatic tumors: short-term reproducibility of apparent diffusion coefficients with breath-hold and respiratory-triggered diffusion-weighted MR imaging. Radiology 2010;255:815-823 https://doi.org/10.1148/radiol.10091706
  36. Kim SY, Lee SS, Park B, Kim N, Kim JK, Park SH, et al. Reproducibility of measurement of apparent diffusion coefficients of malignant hepatic tumors: effect of DWI techniques and calculation methods. J Magn Reson Imaging 2012;36:1131-1138 https://doi.org/10.1002/jmri.23744
  37. Miquel ME, Scott AD, Macdougall ND, Boubertakh R, Bharwani N, Rockall AG. In vitro and in vivo repeatability of abdominal diffusion-weighted MRI. Br J Radiol 2012;85:1507-1512 https://doi.org/10.1259/bjr/32269440
  38. Taouli B, Koh DM. Diffusion-weighted MR imaging of the liver. Radiology 2010;254:47-66 https://doi.org/10.1148/radiol.09090021
  39. Feinstein AR, Cicchetti DV. High agreement but low kappa: I. The problems of two paradoxes. J Clin Epidemiol 1990;43:543-549 https://doi.org/10.1016/0895-4356(90)90158-L

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