Intest Res.  2016 Apr;14(2):120-126. 10.5217/ir.2016.14.2.120.

Magnetic resonance enterography for the evaluation of the deep small intestine in Crohn's disease

• Ohtsuka K
• Takenaka K
• Kitazume Y
• Fujii T
• Matsuoka K
• Kimura M
• Nagaishi T
• Watanabe M

• KMID: 2425284
• DOI: http://doi.org/10.5217/ir.2016.14.2.120

Abstract

For the control of Crohn's disease (CD) a thorough assessment of the small intestine is essential; several modalities may be utilized, with cross-sectional imaging being important. Magnetic resonance (MR) enterography, i.e., MRE is recommended as a modality with the highest accuracy for CD lesions. MRE and MR enteroclysis are the two methods performed following distension of the small intestine. MRE has sensitivity and specificity comparable to computed tomography enterography (CTE); although images obtained using MRE are less clear compared with CTE, MRE does not expose the patient to radiation and is superior for soft-tissue contrast. Furthermore, it can assess not only static but also dynamic and functional imaging and reveals signs of CD, such as abscess, comb sign, fat edema, fistula, lymph node enhancement, less motility, mucosal lesions, stricture, and wall enhancement. Several indices of inflammatory changes and intestinal damage have been proposed for objective evaluation. Recently, diffusion-weighted imaging has been proposed, which does not need bowel preparation and contrast enhancement. Comprehension of the characteristics of MRE and other modalities is important for better management of CD.

Keyword

Magnetic resonance enterography; Computed tomography enterography; Capsule endoscopy; Balloon-assisted enteroscopy; Diffusion magnetic resonance imaging

MeSH Terms

Abscess
Capsule Endoscopy
Comprehension
Constriction, Pathologic
Crohn Disease*
Diffusion Magnetic Resonance Imaging
Edema
Fistula
Humans
Intestine, Small*
Lymph Nodes
Sensitivity and Specificity

Reference

1. Neurath MF, Travis SP. Mucosal healing in inflammatory bowel diseases: a systematic review. Gut. 2012; 61:1619–1635. PMID: 22842618.

2. Ng SC, Tang W, Ching JY, et al. Incidence and phenotype of inflammatory bowel disease based on results from the Asia-pacific Crohn's and colitis epidemiology study. Gastroenterology. 2013; 145:158–165. PMID: 23583432.

3. Iddan G, Meron G, Glukhovsky A, Swain P. Wireless capsule endoscopy. Nature. 2000; 405:417. PMID: 10839527.

4. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001; 53:216–220. PMID: 11174299.

5. Cheriyan DG, Slattery E, McDermott S, et al. Impact of magnetic resonance enterography in the management of small bowel Crohn's disease. Eur J Gastroenterol Hepatol. 2013; 25:550–555. PMID: 23325284.

6. Panes J, Bouhnik Y, Reinisch W, et al. Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis. 2013; 7:556–585. PMID: 23583097.

7. Lang G, Schmiegel W, Nicolas V, Brechmann T. Impact of small bowel MRI in routine clinical practice on staging of Crohn's disease. J Crohns Colitis. 2015; 9:784–794. PMID: 26071412.

8. Kim SH. Computed tomography enterography and magnetic resonance enterography in the diagnosis of Crohn's disease. Intest Res. 2015; 13:27–38. PMID: 25691841.

9. Masselli G, Casciani E, Polettini E, Gualdi G. Comparison of MR enteroclysis with MR enterography and conventional enteroclysis in patients with Crohn's disease. Eur Radiol. 2008; 18:438–447. PMID: 17899102.

10. Schreyer AG, Geissler A, Albrich H, et al. Abdominal MRI after enteroclysis or with oral contrast in patients with suspected or proven Crohn's disease. Clin Gastroenterol Hepatol. 2004; 2:491–497. PMID: 15181618.

11. Negaard A, Paulsen V, Sandvik L, 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. Eur Radiol. 2007; 17:2294–2301. PMID: 17483955.

12. Lawrance IC, Welman CJ, Shipman P, Murray K. Small bowel MRI enteroclysis or follow through: which is optimal? World J Gastroenterol. 2009; 15:5300–5306. PMID: 19908338.

13. Negaard A, Sandvik L, Berstad AE, et al. MRI of the small bowel with oral contrast or nasojejunal intubation in Crohn's disease: randomized comparison of patient acceptance. Scand J Gastroenterol. 2008; 43:44–51. PMID: 18158695.

14. Ognibene NM, Basile M, Di Maurizio M, Petrillo G, De Filippi C. Features and perspectives of MR enterography for pediatric Crohn disease assessment. Radiol Med. [published online ahead of print February 2, 2016]. DOI: 10.1007/s11547-015-0613-2.

15. Qiu Y, Mao R, Chen BL, 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. PMID: 24912799.

16. Desmond AN, O'Regan K, Curran C, et al. Crohn's disease: factors associated with exposure to high levels of diagnostic radiation. Gut. 2008; 57:1524–1529. PMID: 18443021.

17. Towbin AJ, Sullivan J, Denson LA, Wallihan DB, Podberesky DJ. CT and MR enterography in children and adolescents with inflammatory bowel disease. Radiographics. 2013; 33:1843–1860. PMID: 24224581.

18. Duigenan S, Gee MS. Imaging of pediatric patients with inflammatory bowel disease. AJR Am J Roentgenol. 2012; 199:907–915. PMID: 22997386.

19. Heye T, Stein D, Antolovic D, Dueck M, Kauczor HU, Hosch W. Evaluation of bowel peristalsis by dynamic cine MRI: detection of relevant functional disturbances–initial experience. J Magn Reson Imaging. 2012; 35:859–867. PMID: 22267053.

20. Quencer KB, Nimkin K, Mino-Kenudson M, Gee MS. Detecting active inflammation and fibrosis in pediatric Crohn's disease: prospective evaluation of MR-E and CT-E. Abdom Imaging. 2013; 38:705–713. PMID: 23361877.

21. Amitai MM, Ben-Horin S, Eliakim R, Kopylov U. Magnetic resonance enterography in Crohn's disease: a guide to common imaging manifestations for the IBD physician. J Crohns Colitis. 2013; 7:603–615. PMID: 23122965.

22. Church PC, Turner D, Feldman BM, et al. Systematic review with meta-analysis: magnetic resonance enterography signs for the detection of inflammation and intestinal damage in Crohn's disease. Aliment Pharmacol Ther. 2015; 41:153–166. PMID: 25403954.

23. Coimbra AJ, Rimola J, O'Byrne S, et al. Magnetic resonance enterography is feasible and reliable in multicenter clinical trials in patients with Crohn's disease, and may help select subjects with active inflammation. Aliment Pharmacol Ther. 2016; 43:61–72. PMID: 26548868.

24. Rimola J, Rodriguez S, García-Bosch O, et al. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease. Gut. 2009; 58:1113–1120. PMID: 19136510.

25. Scardapane A, Ambrosi A, Salinaro E, et al. Assessment of disease activity in small bowel Crohn's disease: comparison between endoscopy and magnetic resonance enterography using MRIA and modified MRIA score. Gastroenterol Res Pract. 2015; 2015:159641. DOI: 10.1155/2015/159641. PMID: 26759554.

26. Ordás I, Rimola J, Rodríguez S, 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. PMID: 24177375.

27. Takenaka K, Ohtsuka K, Kitazume Y, et al. Correlation of the endoscopic and magnetic resonance scoring systems in the deep small intestine in Crohn's disease. Inflamm Bowel Dis. 2015; 21:1832–1838. PMID: 26020602.

28. Steward MJ, Punwani S, Proctor I, 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. PMID: 21924572.

29. Makanyanga JC, Pendsé D, Dikaios N, et al. Evaluation of Crohn's disease activity: initial validation of a magnetic resonance enterography global score (MEGS) against faecal calprotectin. Eur Radiol. 2014; 24:277–287. PMID: 24026620.

30. Pariente B, Mary JY, Danese S, et al. Development of the Lémann index to assess digestive tract damage in patients with Crohn's disease. Gastroenterology. 2015; 148:52–63. PMID: 25241327.

31. Takenaka K, Ohtsuka K, Kitazume Y, et al. Comparison of magnetic resonance and balloon enteroscopic examination of the small intestine in patients with Crohn's disease. Gastroenterology. 2014; 147:334–342. PMID: 24732015.

32. Seastedt KP, Trencheva K, Michelassi F, et al. Accuracy of CT enterography and magnetic resonance enterography imaging to detect lesions preoperatively in patients undergoing surgery for Crohn's disease. Dis Colon Rectum. 2014; 57:1364–1370. PMID: 25380001.

33. Hirai F, Beppu T, Takatsu N, et al. Long-term outcome of endoscopic balloon dilation for small bowel strictures in patients with Crohn's disease. Dig Endosc. 2014; 26:545–551. PMID: 24528293.

34. Gibson DJ, Murphy DJ, Smyth AE, et al. Magnetic resonance enterography findings as predictors of clinical outcome following antitumor necrosis factor treatment in small bowel Crohn's disease. Eur J Gastroenterol Hepatol. 2015; 27:956–962. PMID: 26049706.

35. Eder P, Katulska K, Krela-Kaźmierczak I, et al. The influence of anti-TNF therapy on the magnetic resonance enterographic parameters of Crohn's disease activity. Abdom Imaging. 2015; 40:2210–2218. PMID: 26048698.

36. Plumb AA, Menys A, Russo E, et al. Magnetic resonance imaging-quantified small bowel motility is a sensitive marker of response to medical therapy in Crohn's disease. Aliment Pharmacol Ther. 2015; 42:343–355. PMID: 26059751.

37. Mino JS, Gandhi NS, Stocchi LL, et al. Preoperative risk factors and radiographic findings predictive of laparoscopic conversion to open procedures in Crohn's disease. J Gastrointest Surg. 2015; 19:1007–1014. PMID: 25820486.

38. Greener T, Klang E, Yablecovitch D, et al. The impact of magnetic resonance enterography and capsule endoscopy on the reclassification of disease in patients with known Crohn's disease: a prospective Israeli IBD Research Nucleus (IIRN) study. J Crohns Colitis. [published online ahead of print January 8, 2016]. DOI: 10.1093/ecco-jcc/jjw006.

39. Rozendorn N, Klang E, Lahat A, et al. Prediction of patency capsule retention in known Crohn's disease patients by using magnetic resonance imaging. Gastrointest Endosc. 2016; 83:182–187. PMID: 26142554.

40. Panés J, Bouzas R, Chaparro M, 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. Aliment Pharmacol Ther. 2011; 34:125–145. PMID: 21615440.

41. Dillman JR, Smith EA, Sanchez R, et al. Prospective cohort study of ultrasound-ultrasound and ultrasound-MR enterography agreement in the evaluation of pediatric small bowel Crohn disease. Pediatr Radiol. 2016; 46:490–497. PMID: 26718197.

42. Castiglione F, Mainenti PP, De Palma GD, et al. Noninvasive diagnosis of small bowel Crohn's disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis. 2013; 19:991–998. PMID: 23429465.

43. Taylor S, Mallett S, Bhatnagar G, 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 Gastroenterol. 2014; 14:142. DOI: 10.1186/1471-230X-14-142. PMID: 25110044.

44. Grand DJ, Guglielmo FF, Al-Hawary MM. MR enterography in Crohn's disease: current consensus on optimal imaging technique and future advances from the SAR Crohn's disease-focused panel. Abdom Imaging. 2015; 40:953–964. PMID: 25666967.

45. Oussalah A, Laurent V, Bruot O, et al. Diffusion-weighted magnetic resonance without bowel preparation for detecting colonic inflammation in inflammatory bowel disease. Gut. 2010; 59:1056–1065. PMID: 20525970.

46. 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. PMID: 26457380.

47. Kovanlikaya A, Beneck D, Rose M, 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. PMID: 25248794.

48. Rosenbaum DG, Rose ML, Solomon AB, Giambrone AE, Kovanlikaya A. Longitudinal diffusion-weighted imaging changes in children with small bowel Crohn's disease: preliminary experience. Abdom Imaging. 2015; 40:1075–1080. PMID: 25808716.

49. Menys A, Atkinson D, Odille F, et al. Quantified terminal ileal motility during MR enterography as a potential biomarker of Crohn's disease activity: a preliminary study. Eur Radiol. 2012; 22:2494–2501. PMID: 22661057.

50. Menys A, Helbren E, Makanyanga J, et al. Small bowel strictures in Crohn's disease: a quantitative investigation of intestinal motility using MR enterography. Neurogastroenterol Motil. 2013; 25:967–e775[975]. PMID: 24028647.

51. Pazahr S, Blume I, Frei P, et al. Magnetization transfer for the assessment of bowel fibrosis in patients with Crohn's disease: initial experience. MAGMA. 2013; 26:291–301. PMID: 23138635.