Pediatric Radiology

, Volume 47, Issue 5, pp 565–575 | Cite as

Magnetic resonance enterography has good inter-rater agreement and diagnostic accuracy for detecting inflammation in pediatric Crohn disease

  • Peter C. ChurchEmail author
  • Mary-Louise C. Greer
  • Ruth Cytter-Kuint
  • Andrea S. Doria
  • Anne M. Griffiths
  • Dan Turner
  • Thomas D. Walters
  • Brian M. Feldman
Original Article



Magnetic resonance enterography (MRE) is increasingly relied upon for noninvasive assessment of intestinal inflammation in Crohn disease. However very few studies have examined the diagnostic accuracy of individual MRE signs in children.


We have created an MR-based multi-item measure of intestinal inflammation in children with Crohn disease — the Pediatric Inflammatory Crohn’s MRE Index (PICMI). To inform item selection for this instrument, we explored the inter-rater agreement and diagnostic accuracy of individual MRE signs of inflammation in pediatric Crohn disease and compared our findings with the reference standards of the weighted Pediatric Crohn’s Disease Activity Index (wPCDAI) and C-reactive protein (CRP).

Materials and methods

In this cross-sectional single-center study, MRE studies in 48 children with diagnosed Crohn disease (66% male, median age 15.5 years) were reviewed by two independent radiologists for the presence of 15 MRE signs of inflammation. Using kappa statistics we explored inter-rater agreement for each MRE sign across 10 anatomical segments of the gastrointestinal tract. We correlated MRE signs with the reference standards using correlation coefficients. Radiologists measured the length of inflamed bowel in each segment of the gastrointestinal tract. In each segment, MRE signs were scored as either binary (0-absent, 1-present), or ordinal (0-absent, 1-mild, 2-marked). These segmental scores were weighted by the length of involved bowel and were summed to produce a weighted score per patient for each MRE sign. Using a combination of wPCDAI≥12.5 and CRP≥5 to define active inflammation, we calculated area under the receiver operating characteristic curve (AUC) for each weighted MRE sign.


Bowel wall enhancement, wall T2 hyperintensity, wall thickening and wall diffusion-weighted imaging (DWI) hyperintensity were most commonly identified. Inter-rater agreement was best for decreased motility and wall DWI hyperintensity (kappa≥0.64). Correlation between MRE signs and wPCDAI was higher than with CRP. AUC was highest (≥0.75) for ulcers, wall enhancement, wall thickening, wall T2 hyperintensity and wall DWI hyperintensity.


Some MRE signs had good inter-rater agreement and AUC for detection of inflammation in children with Crohn disease.


Children Crohn disease Diagnostic accuracy Inflammation Magnetic resonance imaging Magnetic resonance enterography 



The authors received funding for this study from an educational grant from the Canadian Association of Gastroenterology and Takeda Canada Inc. The authors are grateful to Karoline Fiedler for assisting in data extraction.

Compliance with ethical standards

Conflicts of interest

The hospital and university research ethics boards approved this study and waived the requirement for informed consent.

Supplementary material

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High resolution image (TIFF 193 kb)
247_2017_3790_MOESM2_ESM.docx (14 kb)
ESM 2 (DOCX 14 kb)


  1. 1.
    Froslie KF, Jahnsen J, Moum BA et al (2007) Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology 133:412–422CrossRefPubMedGoogle Scholar
  2. 2.
    Baert F, Moortgat L, Van Assche G et al (2010) Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn’s disease. Gastroenterology 138:463–468, quiz e410–461CrossRefPubMedGoogle Scholar
  3. 3.
    Schnitzler F, Fidder H, Ferrante M et al (2009) Mucosal healing predicts long-term outcome of maintenance therapy with infliximab in Crohn’s disease. Inflamm Bowel Dis 15:1295–1301CrossRefPubMedGoogle Scholar
  4. 4.
    De Cruz P, Kamm MA, Prideaux L et al (2013) Mucosal healing in Crohn’s disease: a systematic review. Inflamm Bowel Dis 19:429–444CrossRefPubMedGoogle Scholar
  5. 5.
    Neurath MF, Travis SP (2012) Mucosal healing in inflammatory bowel diseases: a systematic review. Gut 61:1619–1635CrossRefPubMedGoogle Scholar
  6. 6.
    Mazziotti S, Blandino A, Scribano E et al (2013) MR enterography findings in abdominopelvic extraintestinal complications of Crohn’s disease. J Magn Reson Imaging 37:1055–1063CrossRefPubMedGoogle Scholar
  7. 7.
    de Bie CI, Buderus S, Sandhu BK et al (2012) Diagnostic workup of paediatric patients with inflammatory bowel disease in Europe: results of a 5-year audit of the EUROKIDS registry. J Pediatr Gastroenterol Nutr 54:374–380CrossRefPubMedGoogle Scholar
  8. 8.
    Levine A, Koletzko S, Turner D et al (2014) ESPGHAN revised porto criteria for the diagnosis of inflammatory bowel disease in children and adolescents. J Pediatr Gastroenterol Nutr 58:795–806PubMedGoogle Scholar
  9. 9.
    Rimola J, Ordas I, Rodriguez S et al (2014) Accuracy of MRE for assessing mucosal healing: comparison with endoscopy in a multicentric study. Abdom Imaging 39:667Google Scholar
  10. 10.
    Rimola J, Ordas I, Rodriguez S et al (2011) Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis 17:1759–1768CrossRefPubMedGoogle Scholar
  11. 11.
    Hordonneau C, Buisson A, Scanzi J et al (2014) Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn’s disease: validation of quantitative index of activity. Am J Gastroenterol 109:89–98CrossRefPubMedGoogle Scholar
  12. 12.
    Alexopoulou E, Roma E, Loggitsi D et al (2009) Magnetic resonance imaging of the small bowel in children with idiopathic inflammatory bowel disease: evaluation of disease activity. Pediatr Radiol 39:791–797CrossRefPubMedGoogle Scholar
  13. 13.
    Pilleul F, Godefroy C, Yzebe-Beziat D et al (2005) Magnetic resonance imaging in Crohn’s disease. Gastroenterol Clin Biol 29:803–808CrossRefPubMedGoogle Scholar
  14. 14.
    Magnano G, Granata C, Barabino A et al (2003) Polyethylene glycol and contrast-enhanced MRI of Crohn’s disease in children: preliminary experience. Pediatr Radiol 33:385–391CrossRefPubMedGoogle Scholar
  15. 15.
    Durno CA, Sherman P, Williams T et al (2000) Magnetic resonance imaging to distinguish the type and severity of pediatric inflammatory bowel diseases. J Pediatr Gastroenterol Nutr 30:170–174CrossRefPubMedGoogle Scholar
  16. 16.
    Levine A, Griffiths A, Markowitz J et al (2011) Pediatric modification of the Montreal classification for inflammatory bowel disease: the Paris classification. Inflamm Bowel Dis 17:1314–1321CrossRefPubMedGoogle Scholar
  17. 17.
    Hyams JS, Ferry GD, Mandel FS et al (1991) Development and validation of a pediatric Crohn’s disease activity index. J Pediatr Gastroenterol Nutr 12:439–447PubMedGoogle Scholar
  18. 18.
    Turner D, Griffiths AM, Walters TD et al (2010) Appraisal of the pediatric Crohn’s disease activity index on four prospectively collected datasets: recommended cutoff values and clinimetric properties. Am J Gastroenterol 105:2085–2092CrossRefPubMedGoogle Scholar
  19. 19.
    Hyams J, Markowitz J, Otley A et al (2005) Evaluation of the pediatric Crohn disease activity index: a prospective multicenter experience. J Pediatr Gastroenterol Nutr 41:416–421CrossRefPubMedGoogle Scholar
  20. 20.
    Hyams J, Crandall W, Kugathasan S et al (2007) Induction and maintenance infliximab therapy for the treatment of moderate-to-severe Crohn’s disease in children. Gastroenterology 132:863–873CrossRefPubMedGoogle Scholar
  21. 21.
    Levine A, Kori M, Dinari G et al (2009) Comparison of two dosing methods for induction of response and remission with oral budesonide in active pediatric Crohn’s disease: a randomized placebo-controlled trial. Inflamm Bowel Dis 15:1055–1061CrossRefPubMedGoogle Scholar
  22. 22.
    Turner D, Griffiths AM, Walters TD et al (2012) Mathematical weighting of the pediatric Crohn’s disease activity index (PCDAI) and comparison with its other short versions. Inflamm Bowel Dis 18:55–62CrossRefPubMedGoogle Scholar
  23. 23.
    Reinisch W, Wang Y, Oddens BJ et al (2012) C-reactive protein, an indicator for maintained response or remission to infliximab in patients with Crohn’s disease: a post-hoc analysis from ACCENT I. Aliment Pharmacol Ther 35:568–576CrossRefPubMedGoogle Scholar
  24. 24.
    Levine A, Turner D, Pfeffer Gik T et al (2014) Comparison of outcomes parameters for induction of remission in new onset pediatric Crohn’s disease: evaluation of the porto IBD group “growth relapse and outcomes with therapy” (GROWTH CD) study. Inflamm Bowel Dis 20:278–285CrossRefPubMedGoogle Scholar
  25. 25.
    Church PC, Greer M-L, Griffiths AM et al (2014) Development of MRE based multi item measures of inflammation and intestinal damage in paediatric Crohn’s disease: the ImageKids study. J Crohns Colitis 8:S33–S34CrossRefGoogle Scholar
  26. 26.
    Makanyanga JC, Pendse D, Dikaios N et al (2014) Evaluation of Crohn’s disease activity: initial validation of a magnetic resonance enterography global score (MEGS) against faecal calprotectin. Eur Radiol 24:277–287CrossRefPubMedGoogle Scholar
  27. 27.
    Fleiss JL, Levin B, Paik MC (2003) Statistical methods for rates and proportions. Wiley series in probability and statistics. J. Wiley, Hoboken, p xxviiCrossRefGoogle Scholar
  28. 28.
    Campbell MJ, Swinscow TDV (1997) Statistics at square one. BMJ, LondonGoogle Scholar
  29. 29.
    Hyun SB, Kitazume Y, Nagahori M et al (2011) Magnetic resonance enterocolonography is useful for simultaneous evaluation of small and large intestinal lesions in Crohn’s disease. Inflamm Bowel Dis 17:1063–1072CrossRefPubMedGoogle Scholar
  30. 30.
    Rimola J, Rodriguez S, Garcia-Bosch O et al (2009) Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn’s disease. Gut 58:1113–1120CrossRefPubMedGoogle Scholar
  31. 31.
    Horsthuis K, de Ridder L, Smets AM et al (2010) Magnetic resonance enterography for suspected inflammatory bowel disease in a pediatric population. J Pediatr Gastroenterol Nutr 51:603–609CrossRefPubMedGoogle Scholar
  32. 32.
    Grand DJ, Kampalath V, Harris A et al (2012) MR enterography correlates highly with colonoscopy and histology for both distal ileal and colonic Crohn’s disease in 310 patients. Eur J Radiol 81:e763–e769CrossRefPubMedGoogle Scholar
  33. 33.
    Fiorino G, Bonifacio C, Peyrin-Biroulet L et al (2011) Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn’s disease. Inflamm Bowel Dis 17:1073–1080CrossRefPubMedGoogle Scholar
  34. 34.
    Ziech ML, Bipat S, Roelofs JJ et al (2011) Retrospective comparison of magnetic resonance imaging features and histopathology in Crohn’s disease patients. Eur J Radiol 80:e299–e305CrossRefPubMedGoogle Scholar
  35. 35.
    Schmidt S, Guibal A, Meuwly JY et al (2010) Acute complications of Crohn’s disease: comparison of multidetector-row computed tomographic enterography with magnetic resonance enterography. Digestion 82:229–238CrossRefPubMedGoogle Scholar
  36. 36.
    Oussalah A, Laurent V, Bruot O et al (2010) Diffusion-weighted magnetic resonance without bowel preparation for detecting colonic inflammation in inflammatory bowel disease. Gut 59:1056–1065CrossRefPubMedGoogle Scholar
  37. 37.
    Negaard A, Paulsen V, Sandvik L et al (2007) A prospective randomized comparison between two MRI studies of the small bowel in Crohn’s disease, the oral contrast method and MR enteroclysis. Eur Radiol 17:2294–2301CrossRefPubMedGoogle Scholar
  38. 38.
    Negaard A, Sandvik L, Mulahasanovic A et al (2006) Magnetic resonance enteroclysis in the diagnosis of small-intestinal Crohn’s disease: diagnostic accuracy and inter- and intra-observer agreement. Acta Radiol 47:1008–1016CrossRefPubMedGoogle Scholar
  39. 39.
    Maccioni F, Viscido A, Broglia L et al (2000) Evaluation of Crohn disease activity with magnetic resonance imaging. Abdom Imaging 25:219–228CrossRefPubMedGoogle Scholar
  40. 40.
    Sinha R, Murphy P, Sanders S et al (2013) Diagnostic accuracy of high-resolution MR enterography in Crohn’s disease: comparison with surgical and pathological specimen. Clin Radiol 68:917–927CrossRefPubMedGoogle Scholar
  41. 41.
    Fiorino G, Bonifacio C, Padrenostro M et al (2013) Comparison between 1.5 and 3.0 tesla magnetic resonance enterography for the assessment of disease activity and complications in ileo-colonic Crohn’s disease. Dig Dis Sci 58:3246–3255CrossRefPubMedGoogle Scholar
  42. 42.
    Modigliani R, Mary JY, Simon JF et al (1990) Clinical, biological, and endoscopic picture of attacks of Crohn’s disease. Evolution on prednisolone. Groupe d’Etude Therapeutique des Affections Inflammatoires Digestives. Gastroenterology 98:811–818CrossRefPubMedGoogle Scholar
  43. 43.
    Eklund C, Lehtimaki T, Hurme M (2005) Epistatic effect of C-reactive protein (CRP) single nucleotide polymorphism (SNP) +1059 and interleukin-1B SNP +3954 on CRP concentration in healthy male blood donors. Int J Immunogenet 32:229–232CrossRefPubMedGoogle Scholar
  44. 44.
    Brull DJ, Serrano N, Zito F et al (2003) Human CRP gene polymorphism influences CRP levels: implications for the prediction and pathogenesis of coronary heart disease. Arterioscler Thromb Vasc Biol 23:2063–2069CrossRefPubMedGoogle Scholar
  45. 45.
    Russell AI, Cunninghame Graham DS, Shepherd C et al (2004) Polymorphism at the C-reactive protein locus influences gene expression and predisposes to systemic lupus erythematosus. Hum Mol Genet 13:137–147CrossRefPubMedGoogle Scholar
  46. 46.
    Church PC, Turner D, Feldman BM et al (2015) Systematic review with meta-analysis: magnetic resonance enterography signs for the detection of inflammation and intestinal damage in Crohn’s disease. Aliment Pharmacol Ther 41:153–166CrossRefPubMedGoogle Scholar
  47. 47.
    Ordas I, Rimola J, Rodriguez S et al (2014) Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn’s disease. Gastroenterology 146, e371CrossRefGoogle Scholar
  48. 48.
    Van Assche G, Herrmann KA, Louis E et al (2013) Effects of infliximab therapy on transmural lesions as assessed by magnetic resonance enteroclysis in patients with ileal Crohn’s disease. J Crohns Colitis 7:950–957CrossRefPubMedGoogle Scholar
  49. 49.
    Tielbeek JA, Lowenberg M, Bipat S et al (2013) Serial magnetic resonance imaging for monitoring medical therapy effects in Crohn’s disease. Inflamm Bowel Dis 19:1943–1950PubMedGoogle Scholar
  50. 50.
    Modigliani R (1990) Endoscopic severity index for Crohn’s disease. Gastrointest Endosc 36:637CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Peter C. Church
    • 1
    • 2
    Email author
  • Mary-Louise C. Greer
    • 3
  • Ruth Cytter-Kuint
    • 3
  • Andrea S. Doria
    • 2
    • 3
  • Anne M. Griffiths
    • 1
    • 4
  • Dan Turner
    • 5
  • Thomas D. Walters
    • 1
    • 4
  • Brian M. Feldman
    • 2
    • 6
  1. 1.Division of Gastroenterology, Hepatology & Nutrition, The Hospital for Sick Children, Department of PediatricsUniversity of TorontoTorontoCanada
  2. 2.Institute of Health Policy, Management and EvaluationUniversity of TorontoTorontoCanada
  3. 3.Department of Diagnostic Imaging, The Hospital for Sick Children, Department of Medical ImagingUniversity of TorontoTorontoCanada
  4. 4.SickKids Inflammatory Bowel Disease CenterThe Hospital for Sick ChildrenTorontoCanada
  5. 5.Shaare Zedek Medical CenterJerusalemIsrael
  6. 6.Division of Rheumatology, The Hospital for Sick Children, Department of PediatricsUniversity of TorontoTorontoCanada

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