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BioMed Research International
Volume 2015, Article ID 786802, 9 pages
http://dx.doi.org/10.1155/2015/786802
Review Article

MRI for Crohn’s Disease: Present and Future

1Department of Internal Medicine, Korea University, Seoul 136-705, Republic of Korea
2Biomedical Research Institute, Chung-Ang University College of Medicine, Seoul 156-756, Republic of Korea
3National Primate Research Center (NPRC), Korea Research Institute of Bioscience and Biotechnology (KRIBB), Ochang 363-883, Republic of Korea

Received 18 August 2014; Revised 9 October 2014; Accepted 11 December 2014

Academic Editor: Takeshi Yokoo

Copyright © 2015 Kichul Yoon 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. D. Corridoni, K. O. Arseneau, and F. Cominelli, “Inflammatory bowel disease,” Immunology Letters, vol. 161, no. 2, pp. 231–235, 2014. View at Publisher · View at Google Scholar
  2. M. W. Laass, D. Roggenbuck, and K. Conrad, “Diagnosis and classification of Crohn's disease,” Autoimmunity Reviews, vol. 13, no. 4-5, pp. 467–471, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. R. D'Iincà and R. Caccaro, “Measuring disease activity in Crohn's disease: what is currently available to the clinician,” Clinical and Experimental Gastroenterology, vol. 7, no. 1, pp. 151–161, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. N. A. Molodecky, I. S. Soon, D. M. Rabi et al., “Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review,” Gastroenterology, vol. 142, no. 1, pp. 46.e42–54.e42, 2012. View at Publisher · View at Google Scholar
  5. L. Peyrin-Biroulet, E. V. Loftus, J.-F. Colombel, and W. J. Sandborn, “The natural history of adult crohn's disease in population-based cohorts,” The American Journal of Gastroenterology, vol. 105, no. 2, pp. 289–297, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. 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
  7. W. R. Best, J. M. Becktel, J. W. Singleton, and F. Kern Jr., “Development of a Crohn's disease activity index. National cooperative Crohn's disease study,” Gastroenterology, vol. 70, no. 3, pp. 439–444, 1976. View at Google Scholar · View at Scopus
  8. D. C. Baumgart and W. J. Sandborn, “Crohn's disease,” The Lancet, vol. 380, no. 9853, pp. 1590–1605, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Sidhu, D. S. Sanders, A. J. Morris, and M. E. McAlindon, “Guidelines on small bowel enteroscopy and capsule endoscopy in adults,” Gut, vol. 57, no. 1, pp. 125–136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Hall, G. Holleran, D. Costigan, and D. McNamara, “Capsule endoscopy: high negative predictive value in the long term despite a low diagnostic yield in patients with suspected Crohn's disease,” United European Gastroenterology Journal, vol. 1, no. 6, pp. 461–466, 2013. View at Publisher · View at Google Scholar
  11. P. B. Wold, J. G. Fletcher, C. D. Johnson, and W. J. Sandborn, “Assessment of small bowel Crohn disease: noninvasive peroral CT enterography compared with other imaging methods and endoscopy—feasibility study,” Radiology, vol. 229, no. 1, pp. 275–281, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. S. L. Triester, J. A. Leighton, G. I. Leontiadis et al., “A meta-analysis of the yield of capsule endoscopy compared to other diagnostic modalities in patients with obscure gastrointestinal bleeding,” American Journal of Gastroenterology, vol. 100, no. 11, pp. 2407–2418, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Fujii, M. Naganuma, Y. Kitazume et al., “Advancing magnetic resonance imaging in crohn's disease,” Digestion, vol. 89, no. 1, pp. 24–30, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. D. J. Brenner and E. J. Hall, “Computed tomography—an increasing source of radiation exposure,” The New England Journal of Medicine, vol. 357, no. 22, pp. 2277–2284, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Bosemani, A. Ozturk, A. Tekes, M. O. Hemker, and T. A. G. M. Huisman, “Feasibility of an optimized MR enterography protocol in the evaluation of pediatric inflammatory bowel disease,” JBR-BTR, vol. 96, no. 4, pp. 196–202, 2013. View at Google Scholar · View at Scopus
  16. I. Absah, D. H. Bruining, J. M. Matsumoto et al., “MR enterography in pediatric inflammatory bowel disease: retrospective assessment of patient tolerance, image quality, and initial performance estimates,” American Journal of Roentgenology, vol. 199, no. 3, pp. W367–W375, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. L. Fidler, L. Guimaraes, and D. M. Einstein, “MR imaging of the small bowel,” Radiographics, vol. 29, no. 6, pp. 1811–1825, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. S. A. Anupindi, O. Terreblanche, and J. Courtier, “Magnetic resonance enterography: inflammatory bowel disease and beyond,” Magnetic Resonance Imaging Clinics of North America, vol. 21, no. 4, pp. 731–750, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. B. C. Allen and J. R. Leyendecker, “MR enterography for assessment and management of small bowel crohn disease,” Radiologic Clinics of North America, vol. 52, no. 4, pp. 799–810, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. M. M. Al-Hawary, E. M. Zimmermann, and H. K. Hussain, “MR imaging of the small bowel in crohn disease,” Magnetic Resonance Imaging Clinics of North America, vol. 22, no. 1, pp. 13–22, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. 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
  22. D. D. T. Maglinte, N. Gourtsoyiannis, D. Rex, T. J. Howard, and F. M. Kelvin, “Classification of small bowel Crohn's subtypes based on multimodality imaging,” Radiologic Clinics of North America, vol. 41, no. 2, pp. 285–303, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Laghi, P. Paolantonio, F. Iafrate, F. Altomari, C. Miglio, and R. Passariello, “Oral contrast agents for magnetic resonance imaging of the bowel,” Topics in Magnetic Resonance Imaging, vol. 13, no. 6, pp. 389–396, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Chalian, A. Ozturk, M. Oliva-Hemker, S. Pryde, and T. A. G. M. Huisman, “MR enterography findings of inflammatory bowel disease in pediatric patients,” The American Journal of Roentgenology, vol. 196, no. 6, pp. W810–W816, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. O. Minowa, Y. Ozaki, S. Kyogoku, N. Shindoh, Y. Sumi, and H. Katayama, “MR imaging of the small bowel using water as a contrast agent in a preliminary study with healthy volunteers,” American Journal of Roentgenology, vol. 173, no. 3, pp. 581–582, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Arslan, Ö. Etlik, M. Kayan, M. Harman, Ý. Tuncer, and O. Temizöz, “Peroral CT enterography with lactulose solution: preliminary observations,” American Journal of Roentgenology, vol. 185, no. 5, pp. 1173–1179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. S. Borthne, J. B. Dormagen, K. I. Gjesdal, T. Storaas, I. Lygren, and J. T. Geitung, “Bowel MR imaging with oral Gastrografin: an experimental study with healthy volunteers,” European Radiology, vol. 13, no. 1, pp. 100–106, 2003. View at Google Scholar · View at Scopus
  28. S. Saini, E. Colak, S. Anthwal, P. A. Vlachou, A. Raikhlin, and A. Kirpalani, “Comparison of 3% sorbitol vs psyllium fibre as oral contrast agents in MR enterography,” The British Journal of Radiology, vol. 87, no. 1042, p. 20140100, 2014. View at Publisher · View at Google Scholar
  29. O. Algin, S. Evrimler, E. Ozmen et al., “A novel biphasic oral contrast solution for enterographic studies,” Journal of Computer Assisted Tomography, vol. 37, no. 1, pp. 65–74, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. D. J. Grand, M. Beland, and A. Harris, “Magnetic resonance enterography,” Radiologic Clinics of North America, vol. 51, no. 1, pp. 99–112, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. A. G. Schreyer, A. Geissler, H. Albrich et al., “Abdominal MRI after enteroclysis or with oral contrast in patients with suspected or proven Crohn's disease,” Clinical Gastroenterology and Hepatology, vol. 2, no. 6, pp. 491–497, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Negaard, L. Sandvik, A. E. Berstad et al., “MRI of the small bowel with oral contrast or nasojejunal intubation in Crohn's disease: randomized comparison of patient acceptance,” Scandinavian Journal of Gastroenterology, vol. 43, no. 1, pp. 44–51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. K. P. Murphy, P. D. McLaughlin, O. J. O'Connor, and M. M. Maher, “Imaging the small bowel,” Current Opinion in Gastroenterology, vol. 30, no. 2, pp. 134–140, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. J. R. Dillman, E. A. Smith, S. Khalatbari, and P. J. Strouse, “IV glucagon use in pediatric MR enterography: effect on image quality, length of examination, and patient tolerance,” American Journal of Roentgenology, vol. 201, no. 1, pp. 185–189, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Nozaki, “Single shot fast spin echo (SSFSE),” Nihon Rinsho, vol. 56, no. 11, pp. 2792–2797, 1998. View at Google Scholar · View at Scopus
  36. K. Scheffler and S. Lehnhardt, “Principles and applications of balanced SSFP techniques,” European Radiology, vol. 13, no. 11, pp. 2409–2418, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Courtier, M. Ohliger, S. J. Rhee, O. Terreblanche, M. B. Heyman, and J. D. Mackenzie, “Shooting a moving target: use of real-time cine magnetic resonance imaging in assessment of the small bowel,” Journal of Pediatric Gastroenterology and Nutrition, vol. 57, no. 4, pp. 426–431, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Wakamiya, A. Furukawa, S. Kanasaki, and K. Murata, “Assessment of small bowel motility function with cine-MRI using balanced steady-state free precession sequence,” Journal of Magnetic Resonance Imaging, vol. 33, no. 5, pp. 1235–1240, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Lohan, C. Cronin, C. Meehan, A. N. Alhajeri, C. Roche, and J. Murphy, “MR small bowel enterography: optimization of imaging timing,” Clinical Radiology, vol. 62, no. 8, pp. 804–807, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. D. J. M. Tolan, R. Greenhalgh, I. A. Zealley, S. Halligan, and S. A. Taylor, “MR enterographic manifestations of small bowel crohn disease,” Radiographics, vol. 30, no. 2, pp. 367–384, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Dagia, M. Ditchfield, M. Kean, and A. Catto-Smith, “Feasibility of 3-T MRI for the evaluation of Crohn disease in children,” Pediatric Radiology, vol. 40, no. 10, pp. 1615–1624, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. K. J. Chang, I. R. Kamel, K. J. Macura, and D. A. Bluemke, “3.0-T MR imaging of the Abdomen: comparison with 1.5 T,” Radiographics, vol. 28, no. 7, pp. 1983–1998, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Buisson, A. Joubert, P.-F. Montoriol et al., “Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 37, no. 5, pp. 537–545, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Oto, F. Zhu, K. Kulkarni, G. S. Karczmar, J. R. Turner, and D. Rubin, “Evaluation of diffusion-weighted MR imaging for detection of bowel inflammation in patients with Crohn's disease,” Academic Radiology, vol. 16, no. 5, pp. 597–603, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Kiryu, K. Dodanuki, H. Takao et al., “Free-breathing diffusion-weighted imaging for the assessment of inflammatory activity in crohn's disease,” Journal of Magnetic Resonance Imaging, vol. 29, no. 4, pp. 880–886, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. 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
  47. C. Hordonneau, A. Buisson, J. Scanzi et al., “Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn's disease: validation of quantitative index of activity,” The American Journal of Gastroenterology, vol. 109, no. 1, pp. 89–98, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Schmid-Tannwald, G. Agrawal, F. Dahi, I. Sethi, and A. Oto, “Diffusion-weighted MRI: role in detecting abdominopelvic internal fistulas and sinus tracts,” Journal of Magnetic Resonance Imaging, vol. 35, no. 1, pp. 125–131, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Satsangi, M. S. Silverberg, S. Vermeire, and J.-F. Colombel, “The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications,” Gut, vol. 55, no. 6, pp. 749–753, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Griffin, L. A. Grant, S. Anderson, P. Irving, and J. Sanderson, “Small bowel MR enterography: problem solving in Crohn's disease,” Insights into Imaging, vol. 3, no. 3, pp. 251–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Maccioni, “Introduction to the feature section on “crohn's disease activity: MRI assessment and clinical implications”,” Abdominal Imaging, vol. 37, no. 6, pp. 917–920, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. G. A. J. Sempere, V. M. Sanjuan, E. M. Chulia et al., “MRI evaluation of inflammatory activity in Crohn's disease,” American Journal of Roentgenology, vol. 184, no. 6, pp. 1829–1835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. R. del Vescovo, I. Sansoni, R. Caviglia et al., “Dynamic contrast enhanced magnetic resonance imaging of the terminal ileum: differentiation of activity of Crohn's disease,” Abdominal Imaging, vol. 33, no. 4, pp. 417–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Zappa, C. Stefanescu, D. Cazals-Hatem et al., “Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn's disease? A retrospective comparison with surgical pathologic analysis,” Inflammatory Bowel Diseases, vol. 17, no. 4, pp. 984–993, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Punwani, M. Rodriguez-Justo, A. Bainbridge et al., “Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features,” Radiology, vol. 252, no. 3, pp. 712–720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Rodriguez, R. Mendez, F. Matute, P. Hernandez, and J. L. Mendoza, “Imaging crohn disease: MR enterography,” Journal of Computer Assisted Tomography, vol. 38, no. 2, pp. 219–227, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Sinha, P. Rajiah, P. Murphy, P. Hawker, and S. Sanders, “Utility of high-resolution MR imaging in demonstrating transmural pathologic changes in Crohn disease,” Radiographics, vol. 29, no. 6, pp. 1847–1867, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. K. A. Herrmann, H. J. Michaely, C. J. Zech, J. Seiderer, M. F. Reiser, and S. O. Schoenberg, “Internal fistulas in Crohn disease: magnetic resonance enteroclysis,” Abdominal Imaging, vol. 31, no. 6, pp. 675–687, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Schill, I. Iesalnieks, M. Haimerl et al., “Assessment of disease behavior in patients with crohn's disease by MR enterography,” Inflammatory Bowel Diseases, vol. 19, no. 5, pp. 983–990, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. 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
  61. F. Maccioni, M. A. Patak, A. Signore, and A. Laghi, “New frontiers of MRI in Crohn's disease: motility imaging, diffusion-weighted imaging, perfusion MRI, MR spectroscopy, molecular imaging, and hybrid imaging (PET/MRI),” Abdominal Imaging, vol. 37, no. 6, pp. 974–982, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Bickelhaupt, J. M. Froehlich, R. Cattin et al., “Software-assisted small bowel motility analysis using free-breathing MRI: feasibility study,” Journal of Magnetic Resonance Imaging, vol. 39, no. 1, pp. 17–23, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. J. L. Cullmann, S. Bickelhaupt, J. M. Froehlich et al., “MR imaging in Crohn's disease: correlation of MR motility measurement with histopathology in the terminal ileum,” Neurogastroenterology and Motility, vol. 25, no. 9, pp. e749–e577, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Bickelhaupt, S. Pazahr, N. Chuck et al., “Crohn's disease: Small bowel motility impairment correlates with inflammatory-related markers C-reactive protein and calprotectin,” Neurogastroenterology and Motility, vol. 25, no. 6, pp. 467–473, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Menys, S. A. Taylor, A. Emmanuel et al., “Global small bowel motility: assessment with dynamic MR imaging,” Radiology, vol. 269, no. 2, pp. 443–450, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Jadvar and P. M. Colletti, “Competitive advantage of PET/MRI,” European Journal of Radiology, vol. 83, no. 1, pp. 84–94, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. J. K. Nicholson, J. C. Lindon, and E. Holmes, ““Metabonomics”: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data,” Xenobiotica, vol. 29, no. 11, pp. 1181–1189, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. K. Pinker, A. Stadlbauer, W. Bogner, S. Gruber, and T. H. Helbich, “Molecular imaging of cancer: MR spectroscopy and beyond,” European Journal of Radiology, vol. 81, no. 3, pp. 566–577, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. M. E. Mullins, “MR spectroscopy: truly molecular imaging; past, present and future,” Neuroimaging Clinics of North America, vol. 16, no. 4, pp. 605–618, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. A. W. J. M. Glaudemans, F. Maccioni, L. Mansi, R. A. J. O. Dierckx, and A. Signore, “Imaging of cell trafficking in Crohn's disease,” Journal of Cellular Physiology, vol. 223, no. 3, pp. 562–571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. R. J. Gillies and D. L. Morse, “In vivo magnetic resonance spectroscopy in cancer,” Annual Review of Biomedical Engineering, vol. 7, pp. 287–326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Ludwig and M. R. Viant, “Two-dimensional J-resolved NMR spectroscopy: review of a key methodology in the metabolomics toolbox,” Phytochemical Analysis, vol. 21, no. 1, pp. 22–32, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. A. M. Weljie, J. Newton, P. Mercier, E. Carlson, and C. M. Slupsky, “Targeted pofiling: quantitative analysis of 1H NMR metabolomics data,” Analytical Chemistry, vol. 78, no. 13, pp. 4430–4442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. E. M. Lenz, J. Bright, I. D. Wilson, S. R. Morgan, and A. F. P. Nash, “A 1H NMR-based metabonomic study of urine and plasma samples obtained from healthy human subjects,” Journal of Pharmaceutical and Biomedical Analysis, vol. 33, no. 5, pp. 1103–1115, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. E. M. Lenz, J. Bright, I. D. Wilson et al., “Metabonomics, dietary influences and cultural differences: a 1H NMR-based study of urine samples obtained from healthy British and Swedish subjects,” Journal of Pharmaceutical and Biomedical Analysis, vol. 36, no. 4, pp. 841–849, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. U. Sharma, R. R. Singh, V. Ahuja, G. K. Makharia, and N. R. Jagannathan, “Similarity in the metabolic profile in macroscopically involved and un-involved colonic mucosa in patients with inflammatory bowel disease: an in vitro proton ((1)H) MR spectroscopy study,” Magn Reson Imaging, vol. 28, no. 7, pp. 1022–1029, 2010. View at Google Scholar
  77. F. Fathi, L. Majari-Kasmaee, A. Mani-Varnosfaderani et al., “1H NMR based metabolic profiling in crohn's disease by random forest methodology,” Magnetic Resonance in Chemistry, vol. 52, no. 7, pp. 370–376, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. J. R. Marchesi, E. Holmes, F. Khan et al., “Rapid and noninvasive metabonomic characterization of inflammatory bowel disease,” Journal of Proteome Research, vol. 6, no. 2, pp. 546–551, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Storr, H. J. Vogel, and R. Schicho, “Metabolomics: is it useful for inflammatory bowel diseases?” Current Opinion in Gastroenterology, vol. 29, no. 4, pp. 378–383, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Fathi, F. Ektefa, M. Hagh-Azali, and H. A. Aghdaie, “Metabonomics exposes metabolic biomarkers of Crohn's disease by 1HNMR,” Gastroenterology and Hepatology from Bed to Bench, vol. 6, supplement 1, pp. S19–S22, 2013. View at Google Scholar · View at Scopus
  81. Y.-S. Hong, Y.-T. Ahn, J.-C. Park et al., “1H NMR-based metabonomic assessment of probiotic effects in a colitis mouse model,” Archives of Pharmacal Research, vol. 33, no. 7, pp. 1091–1101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Schicho, R. Shaykhutdinov, J. Ngo et al., “Quantitative metabolomic profiling of serum, plasma, and urine by 1H NMR spectroscopy discriminates between patients with inflammatory bowel disease and healthy individuals,” Journal of Proteome Research, vol. 11, no. 6, pp. 3344–3357, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Baur, F.-P. Martin, L. Gruber et al., “Metabolic phenotyping of the Crohn's disease-like IBD etiopathology in the TNFΔARE/WT mouse model,” Journal of Proteome Research, vol. 10, no. 12, pp. 5523–5535, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Balasubramanian, S. Kumar, R. R. Singh et al., “Metabolism of the colonic mucosa in patients with inflammatory bowel diseases: an in vitro proton magnetic resonance spectroscopy study,” Magnetic Resonance Imaging, vol. 27, no. 1, pp. 79–86, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. N. S. Stephens, J. Siffledeen, X. Su, T. B. Murdoch, R. N. Fedorak, and C. M. Slupsky, “Urinary NMR metabolomic profiles discriminate inflammatory bowel disease from healthy,” Journal of Crohn's and Colitis, vol. 7, no. 2, pp. e42–e48, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. H. R. T. Williams, I. J. Cox, D. G. Walker et al., “Characterization of inflammatory bowel disease with urinary metabolic profiling,” The American Journal of Gastroenterology, vol. 104, no. 6, pp. 1435–1444, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. B. C. te Boekhorst, G. A. van Tilborg, G. J. Strijkers, and K. Nicolay, “Molecular MRI of inflammation in atherosclerosis,” Current Cardiovascular Imaging Reports, vol. 5, no. 1, pp. 60–68, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. L. E. Paulis, T. Geelen, M. T. Kuhlmann et al., “Distribution of lipid-based nanoparticles to infarcted myocardium with potential application for MRI-monitored drug delivery,” Journal of Controlled Release, vol. 162, no. 2, pp. 276–285, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. S. A. Sargsyan and J. M. Thurman, “Molecular imaging of autoimmune diseases and inflammation,” Molecular Imaging, vol. 11, no. 3, pp. 251–264, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. J. L. Gaglia, A. R. Guimaraes, M. Harisinghani et al., “Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients,” Journal of Clinical Investigation, vol. 121, no. 1, pp. 442–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. M. E. Kool, V. C. Cappendijk, K. B. J. M. Cleutjens et al., “Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging,” Circulation, vol. 107, no. 19, pp. 2453–2458, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. M. F. Kircher, J. R. Allport, E. E. Graves et al., “In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors,” Cancer Research, vol. 63, no. 20, pp. 6838–6846, 2003. View at Google Scholar · View at Scopus
  93. J. Barkhausen, W. Ebert, C. Heyer, J. F. Debatin, and H.-J. Weinmann, “Detection of atherosclerotic plaque with gadofluorine-enhanced magnetic resonance imaging,” Circulation, vol. 108, no. 5, pp. 605–609, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. W. J. M. Mulder, G. J. Strijkers, G. A. F. van Tilborg, A. W. Griffioen, and K. Nicolay, “Lipid-based nanoparticles for contrast-enhanced MRI and molecular imaging,” NMR in Biomedicine, vol. 19, no. 1, pp. 142–164, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. R. Weissleder, K. Kelly, E. Y. Sun, T. Shtatland, and L. Josephson, “Cell-specific targeting of nanoparticles by multivalent attachment of small molecules,” Nature Biotechnology, vol. 23, no. 11, pp. 1418–1423, 2005. View at Publisher · View at Google Scholar · View at Scopus