MRI reveals different Crohn’s disease phenotypes in children and adults

  • Francesca MaccioniEmail author
  • Davide Bencardino
  • Valeria Buonocore
  • Fabrizio Mazzamurro
  • Franca Viola
  • Salvatore Oliva
  • Piero Vernia
  • Manuela Merli
  • Anna Rita Vestri
  • Carlo Catalano
  • Salvatore Cucchiara



To identify differences between two cohorts of adult and pediatric patients affected by Crohn’s disease (CD), with regard to lesion location in the small intestine and colon-rectum, lesion activity, and prevalence of perianal disease (PD), using MRI as the main diagnostic tool.


We retrospectively reviewed 350 consecutive MRI examinations performed between 2013 and 2016 in outpatients or inpatients with histologically proven CD, monitored by the Gastroenterology and Pediatric Units of our Hospital. The magnetic resonance enterography (MRE) protocol for adult and pediatric CD patients routinely includes evaluation of nine different intestinal segments (from jejunum to rectum) and of the anal canal. Intestinal activity was also calculated using a validated score. Perianal disease (PD) was staged. Fisher’s exact test was used and the odds ratio (OR) was calculated.


Two hundred and nineteen out of 350 MRI studies (118 adults and 101 children) were included. The prevalence of PD was 34.6% in children and 16.1% in adults (OR = 2.8; p = 0.0017). Pediatric patients showed more frequent rectal involvement (29.7% vs 13.5%, OR = 2.7; p = 0.0045) and higher risk of PD in the presence of rectal disease (p = 0.043; OR = 4.5). In pediatric patients with severe colorectal disease, the prevalence of PD was twofold (86.7% vs 40%; p = 0.072). Using the clinical Montreal classification for lesion location, no significant differences emerged between the two patient populations.


MRI showed a significantly higher prevalence of rectal involvement and perianal disease in the pediatric population. These results may have a relevant clinical impact and deserve further investigation.

Key Points

• To our knowledge, this is the largest morphological comparative study available in the literature using MRI as the main diagnostic tool to compare adult patients and children with Crohn’s disease.

• Our study showed significant differences between adults and children: a higher prevalence of rectal and perianal fistulous disease (PD) in pediatric patients and an increased prevalence of PD in the presence of severe colon-rectum involvement.

• The association of rectal and perianal disease implies a poorer clinical prognosis and a higher risk of disabling complications in pediatric patients.


Magnetic resonance imaging Crohn disease Pediatrics Fistula Anal canal 



Crohn’s disease


Confidence interval


Diffusion-weighted imaging


Half-Fourier acquisition single shot turbo spin echo


High-resolution magnetic resonance imaging


Magnetic resonance enterography global score


Magnetic resonance enterography


Magnetic resonance imaging


Odds ratio


Perianal disease


St. James Hospital


True fast imaging with steady-state free precession


Volumetric interpolated breath-hold examination



The authors state that this work has not received any funding.

Compliance with ethical standards


The scientific guarantor of this publication is Francesca Maccioni.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.


• retrospective

• observational

• performed at one institution

Supplementary material

330_2019_6006_MOESM1_ESM.doc (62 kb)
ESM 1 (DOC 61 kb)


  1. 1.
    Benchimol EI, Fortinsky KJ, Gozdyra P, Van den Heuvel M, Van Limbergen J, Griffiths AM (2011) Epidemiology of pediatric inflammatory bowel disease: a systematic review of international trends. Inflamm Bowel Dis 17:423–439CrossRefGoogle Scholar
  2. 2.
    Van Limbergen J, Russell RK, Drummond HE et al (2008) Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology 135:1114–1122CrossRefGoogle Scholar
  3. 3.
    Vernier-Massouille G, Balde M, Salleron J et al (2008) Natural history of pediatric Crohn’s disease: a population-based cohort study. Gastroenterology 135(4):1106–1113CrossRefGoogle Scholar
  4. 4.
    Goodhand J, Hedin CR, Croft NM, Lindsay JO (2011) Adolescents with IBD: the importance of structured transition care. J Crohns Colitis 5:509–519CrossRefGoogle Scholar
  5. 5.
    Duricova D, Burisch J, Jess T, Gower-Rousseau C, Lakatos PL, ECCO-EpiCom (2014) Age-related differences in presentation and course of inflammatory bowel disease: an update on the population-based literature. J Crohns Colitis 8:1351–1361CrossRefGoogle Scholar
  6. 6.
    Kim HJ, Oh SH, Kim DY et al (2017) Clinical characteristics and long-term outcomes of paediatric Crohn’s disease: a single-centre experience. J Crohns Colitis 11(2):157–164CrossRefGoogle Scholar
  7. 7.
    Duricova D, Fumery M, Annese V, Lakatos PL, Peyrin-Biroulet L, Gower-Rousseau C (2017) The natural history of Crohn’s disease in children: a review of population-based studies. Eur J Gastroenterol Hepatol 29(2):125–134CrossRefGoogle Scholar
  8. 8.
    Herzog D, Fournier N, Buehr P et al (2017) Prevalence of intestinal complications in inflammatory bowel disease: a comparison between paediatric-onset and adult-onset patients. Eur J Gastroenterol Hepatol 29(8):926–931CrossRefGoogle Scholar
  9. 9.
    Jakobsen C, Bartek J Jr, Wewer V et al (2011) Differences in phenotype and disease course in adult and paediatric inflammatory bowel disease--a population-based study. Aliment Pharmacol Ther 34(10):1217–1224CrossRefGoogle Scholar
  10. 10.
    Satsangi J, Silverberg MS, Vermeire S, Colombel JF (2006) The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 55(6):749–753CrossRefGoogle Scholar
  11. 11.
    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(6):1314–1321CrossRefGoogle Scholar
  12. 12.
    Müller KE, Lakatos PL, Arató A et al (2013) Incidence, Paris classification, and follow-up in a nationwide incident cohort of pediatric patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 57:576–582CrossRefGoogle Scholar
  13. 13.
    De Bie CI, Paerregaard A, Kolacek S et al (2013) Disease phenotype at diagnosis in pediatric Crohn’s disease: 5-year analyses of the EUROKIDS Registry. Inflamm Bowel Dis 19(2):378–385CrossRefGoogle Scholar
  14. 14.
    Lee YA, Chun P, Hwang EH, Mun SW, Lee YJ, Park JH (2016) Clinical features and extraintestinal manifestations of Crohn disease in children. Pediatr Gastroenterol Hepatol Nutr 19(4):236–242CrossRefGoogle Scholar
  15. 15.
    Assa A, Amitai M, Greer ML et al (2017) ImageKids study group. Perianal pediatric Crohn’s disease is associated with a distinct phenotype and greater inflammatory burden. J Pediatr Gastroenterol Nutr 65(3):293–298CrossRefGoogle Scholar
  16. 16.
    Schwartz DA, Loftus EV Jr, Tremaine WJ et al (2002) The natural history of fistulizing Crohn’s disease in Olmsted County, Minnesota. Gastroenterology 122:875–880CrossRefGoogle Scholar
  17. 17.
    Panés J, Rimola J (2017) Perianal fistulizing Crohn's disease: pathogenesis, diagnosis and therapy. Nat Rev Gastroenterol Hepatol 14(11):652–664CrossRefGoogle Scholar
  18. 18.
    Hellers G, Bergstrand O, Ewerth S, Holmström B (1980) Occurrence and outcome after primary treatment of anal fistulae in Crohn’s disease. Gut 21:525–527CrossRefGoogle Scholar
  19. 19.
    Zwintscher NP, Shah PM, Argawal A et al (2015) The impact of PD in young patients with inflammatory bowel disease. Int J Colorectal Dis 30(9):1275–1279CrossRefGoogle Scholar
  20. 20.
    Safar B, Sands D (2007) Perianal Crohn’s disease. Clin Colon Rectal Surg 20(4):282–293CrossRefGoogle Scholar
  21. 21.
    Kaur M, Panikkath D, Yan X et al (2016) Perianal Crohn’s disease is associated with distal colonic disease, stricturing disease behavior, IBD-associated serologies and genetic variation in the JAK-STAT pathway. Inflamm Bowel Dis 22(4):862–869CrossRefGoogle Scholar
  22. 22.
    Essary B, Kim J, Anupindi S, Katz JA, Nimkin K (2007) Pelvic MRI in children with Crohn disease and suspected perianal involvement. Pediatr Radiol 37(2):201–208CrossRefGoogle Scholar
  23. 23.
    Haggett PJ, Moore NRN, Shearman JD, Travis SP, Jewell DP, Mortensen NJ (1995) Pelvic and perineal complications of Crohn’s disease: assessment using magnetic resonance imaging. Gut 36:407–410CrossRefGoogle Scholar
  24. 24.
    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(6):795–806PubMedGoogle Scholar
  25. 25.
    Panes J, Bouhnik Y, Reinisch W et al (2013) Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis 7:556–585CrossRefGoogle Scholar
  26. 26.
    Civitelli F, Casciani E, Maccioni F et al (2015) Use of imaging techniques in inflammatory bowel diseases that minimize radiation exposure. Curr Gastroenterol Rep 17(7):28CrossRefGoogle Scholar
  27. 27.
    Maccioni F, Al Ansari N, Mazzamurro F et al (2014) Detection of Crohn disease lesions of the small and large bowel in pediatric patients: diagnostic value of MR enterography versus reference examinations. AJR Am J Roentgenol 203(5):W533–W542CrossRefGoogle Scholar
  28. 28.
    Church PC, Greer MC, Cytter-Kuint R et al (2017) Magnetic resonance enterography has good inter-rater agreement and diagnostic accuracy for detecting inflammation in pediatric Crohn disease. Pediatr Radiol 47(5):565–575CrossRefGoogle Scholar
  29. 29.
    Gomollón F, Dignass A, Annese V et al (2017) 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: Part 1: Diagnosis and medical management. J Crohns Colitis 11(1):3–25CrossRefGoogle Scholar
  30. 30.
    Maccioni F, Viscido A, Broglia L et al (2000) Evaluation of Crohn disease activity with magnetic resonance imaging. Abdom Imaging 25(3):219–228CrossRefGoogle Scholar
  31. 31.
    Rimola J, Ordás 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(8):1759–1768CrossRefGoogle Scholar
  32. 32.
    Tielbeek JA, Makanyanga JC, Bipat S et al (2013) 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 201(6):1220–1228CrossRefGoogle Scholar
  33. 33.
    Steward MJ, Punwani S, Proctor I et al (2012) Non-perforating small bowel Crohn’s disease assessed by MRI enterography: derivation and histopathological validation of an MR-based activity index. Eur J Radiol 81(9):2080–2088CrossRefGoogle Scholar
  34. 34.
    Maccioni F, Bruni A, Viscido A et al (2006) MR imaging in patients with Crohn disease: value of T2- versus T1-weighted gadolinium-enhanced MR sequences with use of an oral superparamagnetic contrast agent. Radiology 238(2):517–530 Erratum in: Radiology. 2013 Aug;268(2):614CrossRefGoogle Scholar
  35. 35.
    Prezzi D, Bhatnagar G, Vega R, Makanyanga J, Halligan S, Taylor SA (2015) Monitoring Crohn’s disease during anti-TNF-alpha therapy: validation of the magnetic resonance enterography global score (MEGS) against a combined clinical reference standard. Eur Radiol 26 (7):2107–2117Google Scholar
  36. 36.
    Makanyanga JC, Pendsé 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(2):277–287CrossRefGoogle Scholar
  37. 37.
    Parks AG, Gordon PH, Hardcastle JD (1976) A classification of fistula-in-ano. Br J Surg 63:1–12CrossRefGoogle Scholar
  38. 38.
    Morris J, Spencer JA, Ambrose NS (2000) MR imaging classification of perianal fistulas and its implications for patient management. Radiographics 3:623–635CrossRefGoogle Scholar
  39. 39.
    Maccioni F, Viola F, Carrozzo F et al (2012) Differences in the location and activity of intestinal Crohn’s disease lesions between adult and paediatric patients detected with MRI. Eur Radiol 22:2465–2477CrossRefGoogle Scholar
  40. 40.
    Ye BD, Yang SK, Cho YK et al (2010) Clinical features and long-term prognosis of Crohn’s disease in Korea. Scand J Gastroenterol 45:1178–1185CrossRefGoogle Scholar
  41. 41.
    Ruel J, Ruane D, Mehandru S, Gower-Rousseau C, Colombel JF (2014) IBD across the age spectrum: is it the same disease? Nat Rev Gastroenterol Hepatol 11(2):88–98CrossRefGoogle Scholar
  42. 42.
    Weiser M, Simon JM, Kochar B et al (2018) Molecular classification of Crohn’s disease reveals two clinically relevant subtypes. Gut 67:36–42CrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  • Francesca Maccioni
    • 1
    Email author
  • Davide Bencardino
    • 1
  • Valeria Buonocore
    • 1
  • Fabrizio Mazzamurro
    • 1
  • Franca Viola
    • 2
  • Salvatore Oliva
    • 2
  • Piero Vernia
    • 3
  • Manuela Merli
    • 4
  • Anna Rita Vestri
    • 5
  • Carlo Catalano
    • 1
  • Salvatore Cucchiara
    • 2
  1. 1.Department of Radiological SciencesOncology and Pathology, Sapienza University of Rome, Policlinico Umberto I Hospital RomeItaly
  2. 2.Department of Pediatrics and Pediatric NeuropsychiatrySapienza University of Rome, Policlinico Umberto I HospitalRomeItaly
  3. 3.Department of Internal Medicine and Medical Specialties, Gastroenterology UnitSapienza University of Rome, Policlinico Umberto I HospitalRomeItaly
  4. 4.Gastroenterology, Department of Clinical MedicineSapienza University of Rome, Policlinico Umberto I HospitalRomeItaly
  5. 5.Department of Public Health and Infectious DiseasesSapienza University of RomeRomeItaly

Personalised recommendations