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Canadian Journal of Gastroenterology and Hepatology
Volume 2016, Article ID 7857352, 14 pages
http://dx.doi.org/10.1155/2016/7857352
Review Article

Magnetic Resonance Imaging of the Small Bowel in Crohn’s Disease: A Systematic Review and Meta-Analysis

Mount Sinai Hospital Centre for Inflammatory Bowel Disease, University of Toronto, Toronto, ON, Canada M5G 1X5

Received 5 May 2015; Accepted 1 July 2015

Copyright © 2016 Osman Ahmed et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Van Assche, A. Dignass, J. Panes et al., “The second European evidence-based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis,” Journal of Crohn's and Colitis, vol. 4, no. 1, pp. 7–27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. H. J. Steinhardt, K. Loeschke, H. Kasper, K. H. Holtermüller, and H. Schäfer, “European Cooperative Crohn's Disease Study (ECCDS): clinical features and natural history,” Digestion, vol. 31, no. 2-3, pp. 97–108, 1985. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Panés, R. Bouzas, M. Chaparro 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,” Alimentary Pharmacology & Therapeutics, vol. 34, no. 2, pp. 125–145, 2011. View at Publisher · View at Google Scholar
  4. L. C. Cirillo, L. Camera, M. Della Noce, F. Castiglione, G. Mazzacca, and M. Salvatore, “Accuracy of enteroclysis in Crohn's disease of the small bowel: a retrospective study,” European Radiology, vol. 10, no. 12, pp. 1894–1898, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Van Gemert-Horsthuis, J. Florie, D. W. Hommes et al., “Feasibility of evaluating Crohn's disease activity at 3.0 Tesla,” Journal of Magnetic Resonance Imaging, vol. 24, no. 2, pp. 340–348, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. J. M. Peloquin, D. S. Pardi, W. J. Sandborn et al., “Diagnostic ionizing radiation exposure in a population-based cohort of patients with inflammatory bowel disease,” American Journal of Gastroenterology, vol. 103, no. 8, pp. 2015–2022, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Dambha, J. Tanner, and N. Carroll, “Diagnostic imaging in Crohn's disease: what is the new gold standard?” Best Practice and Research: Clinical Gastroenterology, vol. 28, no. 3, pp. 421–436, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Masselli and G. Gualdi, “MR imaging of the small bowel,” Radiology, vol. 264, no. 2, pp. 333–348, 2012. View at Publisher · View at Google Scholar
  9. L. M. Wu, J. R. Xu, H. Y. Gu, J. Hua, and J. Hu, “Is magnetic resonance imaging a reliable diagnostic tool in the evaluation of active Crohn's disease in the small bowel?” Journal of Clinical Gastroenterology, vol. 47, no. 4, pp. 328–338, 2013. View at Publisher · View at Google Scholar
  10. K. Horsthuis, S. Bipat, P. C. F. Stokkers, and J. Stoker, “Magnetic resonance imaging for evaluation of disease activity in Crohn's disease: a systematic review,” European Radiology, vol. 19, no. 6, pp. 1450–1460, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. P. F. Whiting, A. W. S. Rutjes, M. E. Westwood et al., “Quadas-2: a revised tool for the quality assessment of diagnostic accuracy studies,” Annals of Internal Medicine, vol. 155, no. 8, pp. 529–536, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. D. M. Koh, Y. Miao, R. J. S. Chinn et al., “MR imaging evaluation of the activity of Crohn's disease,” American Journal of Roentgenology, vol. 177, no. 6, pp. 1325–1332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Rieber, D. Wruk, S. Potthast et al., “Diagnostic imaging in Crohn's disease: comparison of magnetic resonance imaging and convertional imaging methods,” International Journal of Colorectal Disease, vol. 15, no. 3, pp. 176–181, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Ochsenkühn, K. Herrmann, S. O. Schoenberg, M. F. Reiser, B. Göke, and M. Sackmann, “Crohn disease of the small bowel proximal to the terminal ileum: detection by MR-enteroclysis,” Scandinavian Journal of Gastroenterology, vol. 39, no. 10, pp. 953–960, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Pascu, A. B. Rownowski, H.-P. Müller, A. Adler, B. Wiedenmann, and A. U. Dignass, “Clinical relevance of transabdominal ultrasonography and magnetic resonance imaging in patients with inflammatory bowel disease of the terminal ileum and large bowel,” Inflammatory Bowel Diseases, vol. 10, no. 4, pp. 373–382, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. A. G. Schreyer, H. C. Rath, R. Kikinis et al., “Comparison of magnetic resonance imaging colonography with conventional colonoscopy for the assessment of intestinal inflammation in patients with inflammatory bowel disease: a feasibility study,” Gut, vol. 54, no. 2, pp. 250–256, 2005. View at Publisher · View at Google Scholar
  17. F. Maccioni, A. Bruni, A. Viscido et al., “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, vol. 238, no. 2, pp. 517–530, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Negaard, L. Sandvik, A. Mulahasanovic, A. E. Berstad, and N.-E. Klöw, “Magnetic resonance enteroclysis in the diagnosis of small-intestinal Crohn's disease: diagnostic accuracy and inter- and intra-observer agreement,” Acta Radiologica, vol. 47, no. 10, pp. 1008–1016, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Negaard, V. Paulsen, L. Sandvik et al., “A prospective randomized comparison between two MRI studies of the small bowel in Crohn's disease, the oral contrast method and MR enteroclysis,” European Radiology, vol. 17, no. 9, pp. 2294–2301, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Seiderer, K. Herrmann, H. Diepolder et al., “Double-balloon enteroscopy versus magnetic resonance enteroclysis in diagnosing suspected small-bowel Crohn's disease: results of a pilot study,” Scandinavian Journal of Gastroenterology, vol. 42, no. 11, pp. 1376–1385, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. H. A. Siddiki, J. L. Fidler, J. G. Fletcher et al., “Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn's disease,” American Journal of Roentgenology, vol. 193, no. 1, pp. 113–121, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. S. S. Lee, A. Y. Kim, S.-K. Yang et al., “Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques,” Radiology, vol. 251, no. 3, pp. 751–761, 2009. View at Google Scholar
  23. J. C. Gallego, A. I. Echarri, A. Porta, and V. Ollero, “Ileal Crohn's disease: MRI with endoscopic correlation,” European Journal of Radiology, vol. 80, no. 2, pp. e8–e12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Giusti, L. Faggioni, E. Neri et al., “Dynamic MRI of the small bowel: usefulness of quantitative contrast-enhancement parameters and time-signal intensity curves for differentiating between active and inactive Crohn's disease,” Abdominal Imaging, vol. 35, no. 6, pp. 646–653, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. C. A. Parisinos, V. E. D. McIntyre, T. Heron et al., “Magnetic resonance follow-through imaging for evaluation of disease activity in ileal Crohn's Disease: an Observational, Retrospective cohort Study,” Inflammatory Bowel Diseases, vol. 16, no. 7, pp. 1219–1226, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Fiorino, C. Bonifacio, L. Peyrin-Biroulet et al., “Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn's disease,” Inflammatory Bowel Diseases, vol. 17, no. 5, pp. 1073–1080, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. S. B. Hyun, Y. Kitazume, M. Nagahori et al., “Magnetic resonance enterocolonography is useful for simultaneous evaluation of small and large intestinal lesions in Crohn's disease,” Inflammatory Bowel Diseases, vol. 17, no. 5, pp. 1063–1072, 2011. View at Publisher · View at Google Scholar
  28. M. D. Jensen, T. Nathan, S. R. Rafaelsen, and J. Kjeldsen, “Diagnostic accuracy of capsule endoscopy for small bowel Crohn's disease is superior to that of MR enterography or CT enterography,” Clinical Gastroenterology and Hepatology, vol. 9, no. 2, pp. 124–129, 2011. View at Publisher · View at Google Scholar
  29. M. D. Jensen, J. Kjeldsen, S. R. Rafaelsen, and T. Nathan, “Diagnostic accuracies of MR enterography and CT enterography in symptomatic Crohn's disease,” Scandinavian Journal of Gastroenterology, vol. 46, no. 12, pp. 1449–1457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Oto, A. Kayhan, J. T. B. Williams et al., “Active Crohn's disease in the small bowel: evaluation by diffusion weighted imaging and quantitative dynamic contrast enhanced MR imaging,” Journal of Magnetic Resonance Imaging, vol. 33, no. 3, pp. 615–624, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. B. M. Wiarda, P. B. F. Mensink, D. G. N. Heine et al., “Small bowel Crohn's disease: MR enteroclysis and capsule endoscopy compared to balloon-assisted enteroscopy,” Abdominal Imaging, vol. 37, no. 3, pp. 397–403, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Friedrich, A. Fajfar, M. Pawlik et al., “Magnetic resonance enterography with and without biphasic contrast agent enema compared to conventional ileocolonoscopy in patients with Crohn's disease,” Inflammatory Bowel Diseases, vol. 18, no. 10, pp. 1842–1848, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. D. J. Grand, V. Kampalath, A. Harris et al., “MR enterography correlates highly with colonoscopy and histology for both distal ileal and colonic Crohn's disease in 310 patients,” European Journal of Radiology, vol. 81, no. 5, pp. e763–e769, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. H. E. Adamek, W. Schantzen, U. Rinas, M. Goyen, W. Ajaj, and C. Esser, “Ultra-high-field magnetic resonance enterography in the diagnosis of ileitis (Neo-)terminalis: a prospective study,” Journal of Clinical Gastroenterology, vol. 46, no. 4, pp. 311–316, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Castiglione, P. P. Mainenti, G. D. De Palma et al., “Noninvasive diagnosis of small bowel Crohn's disease: direct comparison of bowel sonography and magnetic resonance enterography,” Inflammatory Bowel Diseases, vol. 19, no. 5, pp. 991–998, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. S. A. Fallis, P. Murphy, R. Sinha et al., “Magnetic resonance enterography in Crohn's disease: a comparison with the findings at surgery,” Colorectal Disease, vol. 15, no. 10, pp. 1273–1280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Kumar, A. Hakim, C. Alexakis et al., “Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn's disease: correlation with intraoperative findings and magnetic resonance enterography,” Journal of Gastroenterology and Hepatology, vol. 30, no. 1, pp. 86–91, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Takenaka, K. Ohtsuka, Y. Kitazume et al., “Comparison of magnetic resonance and balloon enteroscopic examination of the small intestine in patients with Crohn's disease,” Gastroenterology, vol. 147, no. 2, pp. 334–342.e3, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Church, D. Turner, T. Walters, M. L. Greer, M. Amitai, and A. Griffiths, “A systematic review of MR enterography signs of inflammation and damage in Crohn's disease,” Journal of Crohn's and Colitis, vol. 6, supplement 1, p. S84, 2012. View at Publisher · View at Google Scholar
  40. N. Gourtsoyiannis, N. Papanikolaou, J. Grammatikakis, and P. Prassopoulos, “MR enteroclysis: technical considerations and clinical applications,” European Radiology, vol. 12, no. 11, pp. 2651–2658, 2002. View at Google Scholar · View at Scopus
  41. I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Small bowel MRI enteroclysis or follow through: which is optimal?” World Journal of Gastroenterology, vol. 15, no. 42, pp. 5300–5306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Lenze, J. Wessling, J. Bremer et al., “Detection and differentiation of inflammatory versus fibromatous Crohn's disease strictures: prospective comparison of 18F-FDG-PET/CT, MR-enteroclysis, and transabdominal ultrasound versus endoscopic/histologic evaluation,” Inflammatory Bowel Diseases, vol. 18, no. 12, pp. 2252–2260, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Qiu, R. Mao, B.-L. Chen et al., “Systematic review with meta-analysis: magnetic resonance enterography vs. computed tomography enterography for evaluating disease activity in small bowel Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 40, no. 2, pp. 134–146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Papadia, E. Maffei, P. Del Rio et al., “Sensitivity and specificity of magnetic resonance enterography in the clinical management of fistulizing Crohn's disease,” Inflammatory Bowel Diseases, vol. 19, no. 9, pp. 1896–1903, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Panes, Y. Bouhnik, W. Reinisch et al., “Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines,” Journal of Crohn's and Colitis, vol. 7, no. 7, pp. 556–585, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. GR. Lichtenstein, S. B. Hanauer, and W. J. Sandborn, “Management of Crohn's disease in adults,” The American Journal of Gastroenterology, vol. 104, no. 2, pp. 465–483, 2009. View at Publisher · View at Google Scholar
  47. A. Lasocki, A. Pitman, R. Williams, B. Lui, A. V. Kalade, and S. Farish, “Relative efficacy of different MRI signs in diagnosing active Crohn's disease, compared against a histological gold standard,” Journal of Medical Imaging and Radiation Oncology, vol. 55, no. 1, pp. 11–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. U. K. Udayasankar, D. Martin, T. Lauenstein et al., “Role of spectral presaturation attenuated inversion-recovery fat-suppressed T2-weighted MR imaging in active inflammatory bowel disease,” Journal of Magnetic Resonance Imaging, vol. 28, no. 5, pp. 1133–1140, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. J. A. W. Tielbeek, M. L. W. Ziech, Z. Li et al., “Evaluation of conventional, dynamic contrast enhanced and diffusion weighted MRI for quantitative Crohn's disease assessment with histopathology of surgical specimens,” European Radiology, vol. 24, no. 3, pp. 619–629, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Oussalah, V. Laurent, O. Bruot et al., “Diffusion-weighted magnetic resonance without bowel preparation for detecting colonic inflammation in inflammatory bowel disease,” Gut, vol. 59, no. 8, pp. 1056–1065, 2010. View at Publisher · View at Google Scholar
  51. B. Pariente, J. Cosnes, S. Danese et al., “Development of the Crohn's disease digestive damage score, the Lémann score,” Inflammatory Bowel Diseases, vol. 17, no. 6, pp. 1415–1422, 2011. View at Publisher · View at Google Scholar
  52. J. Rimola, S. Rodriguez, O. García-Bosch et al., “Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease,” Gut, vol. 58, no. 8, pp. 1113–1120, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. L. Mendoza, Y. González-Lama, C. Taxonera et al., “Using of magnetic resonance enterography in the management of crohn's disease of the small intestine: first year of experience,” Revista Espanola de Enfermedades Digestivas, vol. 104, no. 11, pp. 578–583, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Messaris, N. Chandolias, D. Grand, and V. Pricolo, “Role of magnetic resonance enterography in the management of Crohn disease,” Archives of Surgery, vol. 145, no. 5, pp. 471–475, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Spinelli, G. Fiorino, P. Bazzi et al., “Preoperative magnetic resonance enterography in predicting findings and optimizing surgical approach in Crohn's disease,” Journal of Gastrointestinal Surgery, vol. 18, no. 1, pp. 83–91, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Florie, K. Horsthuis, D. W. Hommes et al., “Magnetic resonance imaging compared with ileocolonoscopy in evaluating disease severity in Crohn's disease,” Clinical Gastroenterology and Hepatology, vol. 3, no. 12, pp. 1221–1228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Taylor, S. Mallett, G. Bhatnagar et al., “METRIC (MREnterography or ulTRasound in Crohn's disease): a study protocol for a multicentre, non-randomised, single-arm, prospective comparison study of magnetic resonance enterography and small bowel ultrasound compared to a reference standard in those aged 16 and over,” BMC Gastroenterology, vol. 14, no. 1, article 142, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Buisson, A. Joubert, P. F. Montoriol et al., “Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation,” Alimentary Pharmacology & Therapeutics, vol. 37, no. 5, pp. 537–545, 2013. View at Publisher · View at Google Scholar