Systematic review with meta-analysis: Magnetic resonance enterography signs for the detection of inflammation and intestinal damage in Crohn's disease

Alimentary Pharmacology and Therapeutics

Volumn 41, Issue 2, 2015, Pages 153-166

  Church, P C ^a,b   Turner, D ^c   Feldman, B M ^a,b   Walters, T D ^a   Greer, M L ^a   Amitai, M M ^d   Griffiths, A M ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CROHN DISEASE; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIFFUSION COEFFICIENT; DISEASE ASSOCIATION; HUMAN; INTESTINE ABSCESS; INTESTINE FISTULA; INTESTINE INFECTION; INTESTINE INJURY; INTESTINE STENOSIS; MAGNETIC RESONANCE ENTEROGRAPHY; META ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SYMPTOMATOLOGY; SYSTEMATIC REVIEW; ABDOMINAL ABSCESS; CHILD; COMPLICATION; INFLAMMATION; INTESTINAL FISTULA; RECEIVER OPERATING CHARACTERISTIC; SYMPTOM ASSESSMENT;

ABDOMINAL ABSCESS; CHILD; CROHN DISEASE; HUMANS; INFLAMMATION; INTESTINAL FISTULA; MAGNETIC RESONANCE IMAGING; ROC CURVE; SENSITIVITY AND SPECIFICITY; SYMPTOM ASSESSMENT;

EID: 84918589785     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.13024     Document Type: Article

References (91)

1. Cosnes J, Cattan S, Blain A, et al,. Long-term evolution of disease behavior of Crohn's disease. Inflamm Bowel Dis 2002; 8: 244-50.
2. Van Limbergen J, Russell RK, Drummond HE, et al,. Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology 2008; 135: 1114-22.
3. Dubinsky MC, Kugathasan S, Mei L, et al,. Increased immune reactivity predicts aggressive complicating Crohn's disease in children. Clin Gastroenterol Hepatol 2008; 6: 1105-11.
4. D'Haens G, Baert F, van Assche G, et al,. Early combined immunosuppression or conventional management in patients with newly diagnosed Crohn's disease: an open randomised trial. Lancet 2008; 371: 660-7.
5. Markowitz J, Grancher K, Kohn N, Lesser M, Daum F,. A multicenter trial of 6-mercaptopurine and prednisone in children with newly diagnosed Crohn's disease. Gastroenterology 2000; 119: 895-902.
6. Picco MF, Zubiaurre I, Adluni M, Cangemi JR, Shelton D,. Immunomodulators are associated with a lower risk of first surgery among patients with non-penetrating non-stricturing Crohn's disease. Am J Gastroenterol 2009; 104: 2754-9.
7. Wolters FL, Russel MG, Stockbrugger RW,. Systematic review: has disease outcome in Crohn's disease changed during the last four decades? Aliment Pharmacol Ther 2004; 20: 483-96.
8. Etchevers MJ, Aceituno M, Sans M,. Are we giving azathioprine too late? The case for early immunomodulation in inflammatory bowel disease. World J Gastroenterol 2008; 14: 5512-8.
9. Lemann M, Mary JY, Colombel JF, et al,. A randomized, double-blind, controlled withdrawal trial in Crohn's disease patients in long-term remission on azathioprine. Gastroenterology 2005; 128: 1812-8.
10. Tielbeek JA, Lowenberg M, Bipat S, et al,. Serial magnetic resonance imaging for monitoring medical therapy effects in Crohn's disease. Inflamm Bowel Dis 2013; 19: 1943-50.
11. Van Assche G, Herrmann KA, Louis E, et al,. Effects of infliximab therapy on transmural lesions as assessed by magnetic resonance enteroclysis in patients with ileal Crohn's disease. J Crohns Colitis 2013; 7: 950-7.
12. Ordas I, Rimola J, Rodriguez 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: 374-82 e1.
13. Horsthuis K, Bipat S, Stokkers PC, Stoker J,. Magnetic resonance imaging for evaluation of disease activity in Crohn's disease: a systematic review. Eur Radiol 2009; 19: 1450-60.
14. Giles E, Barclay AR, Chippington S, Wilson DC,. Systematic review: MRI enterography for assessment of small bowel involvement in paediatric Crohn's disease. Aliment Pharmacol Ther 2013; 37: 1121-31.
15. Panes 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: 125-45.
16. Wu L-M, Xu J-R, Gu H-Y, Hua J, Hu J,. Is magnetic resonance imaging a reliable diagnostic tool in the evaluation of active Crohn's disease in the small bowel? J Clin Gastroenterol 2013; 47: 328-38.
17. Reitsma JB, Rutjes AWS, Whiting P, Vlassov VV, Leeflang MMG, Deeks JJ,. Chapter 9: Assessing methodological quality. In:, Deeks JJ, Bossuyt PM, Gatsonis C, eds. Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0.0. The Cochrane Collaboration, 2009. Available at: http://srdta.cochrane.org/ (accessed August 2014).
18. Dwamena BA,. MIDAS: Stata module for meta-analytical integration of diagnostic test accuracy studies, 2009. http://EconPapers.repec.org/RePEc:boc:bocode:s456880 (accessed August 2014).
19. Deeks JJ, Macaskill P, Irwig L,. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 2005; 58: 882-93.
20. Rutter CM, Gatsonis CA,. A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat Med 2001; 20: 2865-84.
21. Schiller I, Dendukuri N,. HSROC: Joint meta-analysis of diagnostic test sensitivity and specificity with or without a gold standard reference test. version 2.1.7. Available at http://cran.r-project.org/web/packages/HSROC/index.html/ (accessed May 2014).
22. Leeflang MM, Deeks JJ, Takwoingi Y, Macaskill P,. Cochrane diagnostic test accuracy reviews. Syst Rev 2013; 2: 82.
23. Harbord RM, Whiting P,. metandi: meta-analysis of diagnostic accuracy using hierarchical logistic regression. Stata J 2009; 9: 211-29.
24. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al,. 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 2011; 17: 1073-80.
25. Hyun SB, Kitazume Y, Nagahori M, et al,. Magnetic resonance enterocolonography is useful for simultaneous evaluation of small and large intestinal lesions in Crohn's disease. Inflamm Bowel Dis 2011; 17: 1063-72.
26. Lasocki A, Pitman A, Williams R, Lui B, Kalade AV, Farish S,. Relative efficacy of different MRI signs in diagnosing active Crohn's disease, compared against a histological gold standard. J Med Imaging Radiat Oncol 2011; 55: 11-9.
27. Ziech ML, Bipat S, Roelofs JJ, et al,. Retrospective comparison of magnetic resonance imaging features and histopathology in Crohn's disease patients. Eur J Radiol 2011; 80: e299-305
28. Zappa M, Stefanescu C, Cazals-Hatem D, 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: 984-93.
29. Schmidt S, Guibal A, Meuwly JY, et al,. Acute complications of Crohn's disease: comparison of multidetector-row computed tomographic enterography with magnetic resonance enterography. Digestion 2010; 82: 229-38.
30. 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: 1056-65.
31. Giusti S, Faggioni L, Neri E, 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. Abdom Imaging 2010; 35: 646-53.
32. Froehlich JM, Waldherr C, Stoupis C, Erturk SM, Patak MA,. MR motility imaging in Crohn's disease improves lesion detection compared with standard MR imaging. Eur Radiol 2010; 20: 1945-51.
33. Rottgen R, Grandke T, Grieser C, Lehmkuhl L, Hamm B, Ludemann L,. Measurement of MRI enhancement kinetics for evaluation of inflammatory activity in Crohn's disease. Clin Imaging 2010; 34: 29-35.
34. Punwani S, Rodriguez-Justo M, Bainbridge A, et al,. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features. Radiology 2009; 252: 712-20.
35. Oto A, Fan X, Mustafi D, et al,. Quantitative analysis of dynamic contrast enhanced MRI for assessment of bowel inflammation in Crohn's disease pilot study. Acad Radiol 2009; 16: 1223-30.
36. Alexopoulou E, Roma E, Loggitsi D, et al,. Magnetic resonance imaging of the small bowel in children with idiopathic inflammatory bowel disease: evaluation of disease activity. Pediatr Radiol 2009; 39: 791-7.
37. Oto A, Zhu F, Kulkarni K, Karczmar GS, Turner JR, Rubin D,. Evaluation of diffusion-weighted MR imaging for detection of bowel inflammation in patients with Crohn's disease. Acad Radiol 2009; 16: 597-603.
38. Lee SS, Kim AY, Yang SK, et al,. Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology 2009; 251: 751-61.
39. Taylor SA, Punwani S, Rodriguez-Justo M, et al,. Mural Crohn disease: correlation of dynamic contrast-enhanced MR imaging findings with angiogenesis and inflammation at histologic examination-pilot study. Radiology 2009; 251: 369-79.
40. Horsthuis K, Nederveen AJ, de Feiter MW, Lavini C, Stokkers PC, Stoker J,. Mapping of T1-values and Gadolinium-concentrations in MRI as indicator of disease activity in luminal Crohn's disease: a feasibility study. J Magn Reson Imaging 2009; 29: 488-93.
41. Rimola J, Rodriguez S, Garcia-Bosch O, et al,. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease. Gut 2009; 58: 1113-20.
42. Gourtsoyianni S, Papanikolaou N, Amanakis E, et al,. Crohn's disease lymphadenopathy: MR imaging findings. Eur J Radiol 2009; 69: 425-8.
43. Udayasankar UK, Martin D, Lauenstein T, et al,. Role of spectral presaturation attenuated inversion-recovery fat-suppressed T2-weighted MR imaging in active inflammatory bowel disease. J Magn Reson Imaging 2008; 28: 1133-40.
44. Malago R, Manfredi R, Benini L, D'Alpaos G, Mucelli RP,. Assessment of Crohn's disease activity in the small bowel with MR-enteroclysis: clinico-radiological correlations. Abdom Imaging 2008; 33: 669-75.
45. Martinez MJ, Ripolles T, Paredes JM, Blanc E, Marti-Bonmati L,. Assessment of the extension and the inflammatory activity in Crohn's disease: comparison of ultrasound and MRI. Abdom Imaging 2009; 34: 141-8.
46. Girometti R, Zuiani C, Toso F, et al,. MRI scoring system including dynamic motility evaluation in assessing the activity of Crohn's disease of the terminal ileum. Acad Radiol 2008; 15: 153-64.
47. Kitazume Y, Satoh S, Hosoi H, Noguchi O, Shibuya H,. Cine magnetic resonance imaging evaluation of peristalsis of small bowel with longitudinal ulcer in Crohn disease: preliminary results. J Comput Assist Tomogr 2007; 31: 876-83.
48. Del Vescovo R, Sansoni I, Caviglia R, et al,. Dynamic contrast enhanced magnetic resonance imaging of the terminal ileum: differentiation of activity of Crohn's disease. Abdom Imaging 2008; 33: 417-24.
49. 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: 2294-301.
50. Negaard A, Sandvik L, Mulahasanovic A, Berstad AE, Klow NE,. Magnetic resonance enteroclysis in the diagnosis of small-intestinal Crohn's disease: diagnostic accuracy and inter- and intra-observer agreement. Acta Radiol 2006; 47: 1008-16.
51. van Gemert-Horsthuis K, Florie J, Hommes DW, et al,. Feasibility of evaluating Crohn's disease activity at 3.0 Tesla. J Magn Reson Imaging 2006; 24: 340-8.
52. Pauls S, Gabelmann A, Schmidt SA, et al,. Evaluating bowel wall vascularity in Crohn's disease: a comparison of dynamic MRI and wideband harmonic imaging contrast-enhanced low MI ultrasound. Eur Radiol 2006; 16: 2410-7.
53. Florie J, Wasser MN, Arts-Cieslik K, Akkerman EM, Siersema PD, Stoker J,. Dynamic contrast-enhanced MRI of the bowel wall for assessment of disease activity in Crohn's disease. AJR Am J Roentgenol 2006; 186: 1384-92.
54. Herrmann KA, Michaely HJ, Seiderer J, Ochsenkuehn T, Reiser MF, Schoenberg SO,. The "star-sign" in magnetic resonance enteroclysis: a characteristic finding of internal fistulae in Crohn's disease. Scand J Gastroenterol 2006; 41: 239-41.
55. Maccioni F, Bruni A, Viscido A, 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 2006; 238: 517-30.
56. Florie J, Horsthuis K, Hommes DW, et al,. Magnetic resonance imaging compared with ileocolonoscopy in evaluating disease severity in Crohn's disease. Clin Gastroenterol Hepatol 2005; 3: 1221-8.
57. Pilleul F, Godefroy C, Yzebe-Beziat D, Dugougeat-Pilleul F, Lachaux A, Valette PJ,. Magnetic resonance imaging in Crohn's disease. Gastroenterol Clin Biol 2005; 29: 803-8.
58. Sempere GA, Martinez Sanjuan V, Medina Chulia E, et al,. MRI evaluation of inflammatory activity in Crohn's disease. AJR Am J Roentgenol 2005; 184: 1829-35.
59. Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, Papamastorakis G, Prassopoulos P, Roussomoustakaki M,. Assessment of Crohn's disease activity in the small bowel with MR and conventional enteroclysis: preliminary results. Eur Radiol 2004; 14: 1017-24.
60. Magnano G, Granata C, Barabino A, et al,. Polyethylene glycol and contrast-enhanced MRI of Crohn's disease in children: preliminary experience. Pediatr Radiol 2003; 33: 385-91.
61. Miao YM, Koh DM, Amin Z, et al,. Ultrasound and magnetic resonance imaging assessment of active bowel segments in Crohn's disease. Clin Radiol 2002; 57: 913-8.
62. Potthast S, Rieber A, Von Tirpitz C, Wruk D, Adler G, Brambs HJ,. Ultrasound and magnetic resonance imaging in Crohn's disease: a comparison. Eur Radiol 2002; 12: 1416-22.
63. Koh DM, Miao Y, Chinn RJ, et al,. MR imaging evaluation of the activity of Crohn's disease. AJR Am J Roentgenol 2001; 177: 1325-32.
64. Rieber A, Aschoff A, Nussle K, et al,. MRI in the diagnosis of small bowel disease: use of positive and negative oral contrast media in combination with enteroclysis. Eur Radiol 2000; 10: 1377-82.
65. Schunk K, Kern A, Oberholzer K, et al,. Hydro-MRI in Crohn's disease: appraisal of disease activity. Invest Radiol 2000; 35: 431-7.
66. Maccioni F, Viscido A, Broglia L, et al,. Evaluation of Crohn's disease activity with magnetic resonance imaging. Abdom Imaging 2000; 25: 219-28.
67. Durno CA, Sherman P, Williams T, Shuckett B, Dupuis A, Griffiths AM,. Magnetic resonance imaging to distinguish the type and severity of pediatric inflammatory bowel diseases. J Pediatr Gastroenterol Nutr 2000; 30: 170-4.
68. Ferda J, Mirka H, Kozeluhova J, et al,. Steady-state gadofosveset-enhanced dark lumen MR-enterography. Ceska Radiologie 2009; 63: 315-21.
69. Oto A, Kayhan A, Williams JTB, et al,. Active Crohn's disease in the small bowel: evaluation by diffusion weighted imaging and quantitative dynamic contrast enhanced MR imaging. J Magn Reson Imaging 2011; 33: 615-24.
70. Ziech MLW, Lavini C, Caan MWA, et al,. Dynamic contrast-enhanced MRI in patients with luminal Crohn's disease. Eur J Radiol 2012; 81: 3019-27.
71. Jensen MD, Kjeldsen J, Rafaelsen SR, Nathan T,. Diagnostic accuracies of MR enterography and CT enterography in symptomatic Crohn's disease. Scand J Gastroenterol 2011; 46: 1449-57.
72. Rimola J, Ordas I, Rodriguez S, et al,. Magnetic resonance imaging for evaluation of Crohn's disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis 2011; 17: 1759-68.
73. Grieser C, Denecke T, Steffen IG, et al,. Magnetic resonance enteroclysis in patients with Crohn's disease: fat saturated T2-weighted sequences for evaluation of inflammatory activity. J Crohns Colitis 2012; 6: 294-301.
74. Pozza A, Scarpa M, Lacognata C, et al,. Magnetic resonance enterography for Crohn's disease: what the surgeon can take home. J Gastrointest Surg 2011; 15: 1689-98.
75. 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: 2494-501.
76. Gallego JC, Echarri AI, Porta A, Ollero V,. Ileal Crohn's disease: MRI with endoscopic correlation. Eur J Radiol 2011; 80: e8-12.
77. Papadia C, Maffei E, Del Rio P, et al,. Sensitivity and specificity of magnetic resonance enterography in the clinical management of fistulizing Crohn's disease. Inflamm Bowel Dis 2013; 19: 1896-903.
78. Bickelhaupt S, Froehlich JM, Cattin R, et al,. Differentiation between active and chronic Crohn's disease using MRI small-bowel motility examinations-initial experience. Clin Radiol 2013; 68: 1247-53.
79. Fiorino G, Bonifacio C, Padrenostro M, et al,. 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 2013; 58: 3246-55.
80. Sinha R, Murphy P, Sanders S, et al,. Diagnostic accuracy of high-resolution MR enterography in Crohn's disease: comparison with surgical and pathological specimen. Clin Radiol 2013; 68: 917-27.
81. Lenze F, Wessling J, Bremer J, 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. Inflamm Bowel Dis 2012; 18: 2252-60.
82. Tielbeek JAW, Ziech MLW, Li Z, 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: 619-29.
83. Fallis SA, Murphy P, Sinha R, et al,. Magnetic resonance enterography in Crohn's disease: a comparison with the findings at surgery. Colorectal Dis 2013; 15: 1273-80.
84. Cullmann JL, Bickelhaupt S, Froehlich JM, et al,. MR imaging in Crohn's disease: correlation of MR motility measurement with histopathology in the terminal ileum. Neurogastroenterol Motil 2013; 25: 749-e577.
85. 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 e3.
86. Rimola J, Ordas I, Rodriguez S, Ricart E, Panes J,. Accuracy of MRE for assessing mucosal healing: comparison with endoscopy in a multicentric study. Abdom Imaging 2014; 39: 667.
87. Buisson A, Joubert A, Montoriol PF, et al,. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn's disease. Aliment Pharmacol Ther 2013; 37: 537-45.
88. Hordonneau C, Buisson A, Scanzi J, 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.
89. Macaskill P, Gatsonis C, Deeks JJ, Harbord RM, Takwoingi Y,. Chapter 10: analysing and presenting results. In:, Deeks JJ, Bossuyt PM, Gatsonis C, eds. Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0. The Cochrane Collaboration, 2010. Available at: http://srdta.cochrane.org/ (accessed October 2014).
90. Menke J, Larsen J,. Meta-analysis: accuracy of contrast-enhanced magnetic resonance angiography for assessing steno-occlusions in peripheral arterial disease. Ann Intern Med 2010; 153: 325-34.
91. Dinnes J, Deeks J, Kirby J, Roderick P,. A methodological review of how heterogeneity has been examined in systematic reviews of diagnostic test accuracy. Health Technol Assess 2005; 9: 1-113, iii.