Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Imaging techniques in IBD and their role in follow-up and surveillance

Nature Reviews Gastroenterology & Hepatology volume 11, pages 722–736 (2014)Cite this article

Subjects

Key Points

  • Ultrasonography, CT enterography (CTE) and magnetic resonance enterography (MRE) are useful tools for assessing Crohn's disease location, activity and extraintestinal complications

  • Ultrasonography, CTE, small-bowel capsule endoscopy (SBCE) and MRE identify mucosal, transmural and extramural inflammation, and thus might change the paradigm of symptom-driven treatment to inflammation-driven treatment of disease

  • Ultrasonography, CTE and MRE are similar to endoscopy in ability to evaluate anastomotic recurrence, with the advantage of detecting Crohn's disease in the proximal small bowel

  • New ultrasonography and MRE techniques might enable evaluation of intestinal fibrosis and guide treatment options

  • Single photon emission CT (SPECT) and hybrid SPECT–CT techniques increase the sensitivity and specificity in the diagnosis of several diseases and are gaining acceptance for new clinical applications in IBD

  • SBCE is a valuable tool for diagnosing or excluding Crohn's disease and might develop into a valuable prognostic modality

Abstract

The assessment of extent and severity of IBD is crucial for directing treatment decisions. Clinical symptoms alone are neither sensitive nor specific for the assessment of lesion severity in IBD. Cross-sectional imaging techniques, as well as small-bowel capsule endoscopy (SBCE) and device-assisted enteroscopy, have a high accuracy for assessing the extent of mucosal lesions, and are reliable alternatives to ileocolonoscopy. New endoscopic techniques and devices are emerging for improved follow-up and surveillance. In this Review, we discuss different imaging techniques that are used to assess IBD activity and to survey patients with IBD, and highlight the latest developments in each area. Moreover, technical improvements and new tools that aim to measure intestinal fibrosis, postoperative recurrence, activity indices and endoscopic features are analysed. All of these imaging techniques are aimed at changing the paradigm from symptom-driven to lesion-driven treatment of IBD.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Ultrasonography images demonstrating fistulous tracts.
Figure 2: Active stenosing Crohn's disease lesions involving the distal ileum and transverse colon.
Figure 3: Intestinal and extraintestinal manifestations in a patient with Crohn's disease.
Figure 4: Fistulizing Crohn's disease.
Figure 5: Examples of fibrostenotic Crohn's disease.
Figure 6: Postoperative recurrence of Crohn's disease.
Figure 7: T2-weighted MRI scan demonstrating active ileal Crohn's disease.
Figure 8: Hybrid SPECT–CT examination in a woman with Crohn's disease.
Figure 9

Similar content being viewed by others

References

  1. Parente, F. et al. Oral contrast enhanced bowel ultrasonography in the assessment of small intestine Crohn's disease. A prospective comparison with conventional ultrasound, x ray studies, and ileocolonoscopy. Gut 53, 1652–1657 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Panes, J. 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. 34, 125–145 (2011).

    Article  CAS  PubMed  Google Scholar 

  3. Ripolles, T. et al. Crohn Disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology 253, 241–248 (2009).

    Article  PubMed  Google Scholar 

  4. Futagami, Y. et al. Development and validation of an ultrasonographic activity index of Crohn's disease. Eur. J. Gastroenterol. Hepatol. 11, 1007–1012 (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Haber, H. P. et al. Ultrasonographic findings correspond to clinical, endoscopic, and histologic findings in inflammatory bowel disease and other enterocolitides. J. Ultrasound Med. 21, 375–382 (2002).

    Article  PubMed  Google Scholar 

  6. Bremner, A. R., Griffiths, M., Argent, J. D., Fairhurst, J. J. & Beattie, R. M. Sonographic evaluation of inflammatory bowel disease: a prospective, blinded, comparative study. Pediatr. Radiol. 36, 947–953 (2006).

    Article  PubMed  Google Scholar 

  7. Parente, F. et al. Role of early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel. Aliment. Pharmacol. Ther. 18, 1009–1016 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Panes, J. et al. Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J. Crohns Colitis 7, 556–585 (2013).

    Article  CAS  PubMed  Google Scholar 

  9. Fraquelli, M. et al. Role of US in detection of Crohn disease: meta-analysis. Radiology 236, 95–101 (2005).

    Article  PubMed  Google Scholar 

  10. Martinez, M. J., Ripolles, T., Paredes, J. M., Blanc, E. & Marti-Bonmati, L. Assessment of the extension and the inflammatory activity in Crohn's disease: comparison of ultrasound and MRI. Abdom. Imaging 34, 141–148 (2009).

    Article  PubMed  Google Scholar 

  11. Rimola, J., Ordas, I., Rodriguez, S., Ricart, E. & Panes, J. Imaging indexes of activity and severity for Crohn's disease: current status and future trends. Abdom. Imaging 37, 958–966 (2012).

    Article  PubMed  Google Scholar 

  12. Calabrese, E. et al. Development of a numerical index quantitating small bowel damage as detected by ultrasonography in Crohn's disease. J. Crohns Colitis 6, 852–860 (2012).

    Article  PubMed  Google Scholar 

  13. Xu, H.-X. Contrast-enhanced ultrasound: the evolving applications. World J. Radiol. 1, 15–24 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Migaleddu, V., Quaia, E., Scano, D. & Virgilio, G. Inflammatory activity in Crohn disease: ultrasound findings. Abdom. Imaging 33, 589–597 (2008).

    Article  PubMed  Google Scholar 

  15. Quaia, E. et al. The value of small bowel wall contrast enhancement after sulfur hexafluoride-filled microbubble injection to differentiate inflammatory from fibrotic strictures in patients with Crohn's disease. Ultrasound Med. Biol. 38, 1324–1332 (2012).

    Article  PubMed  Google Scholar 

  16. Malago, R. et al. Contrast-enhanced ultrasonography (CEUS) vs. MRI of the small bowel in the evaluation of Crohn's disease activity. Radiol. Med. 117, 268–281 (2012).

    Article  CAS  PubMed  Google Scholar 

  17. Girlich, C., Schacherer, D., Jung, E. M., Schreyer, A. & Buettner, R. Comparison between a clinical activity index (Harvey-Bradshaw-Index), laboratory inflammation markers and quantitative assessment of bowel wall vascularization by contrast-enhanced ultrasound in Crohn's disease. Eur. J. Radiol. 81, 1105–1109 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Ripolles, T. et al. Contrast-enhanced ultrasound in the differentiation between phlegmon and abscess in Crohn's disease and other abdominal conditions. Eur. J. Radiol. 82, E525–E531 (2013).

    Article  PubMed  Google Scholar 

  19. Thomson, M., Rao, P., Berger, L. & Rawat, D. Graded compression and power Doppler ultrasonography versus endoscopy to assess paediatric Crohn disease activity pre- and posttreatment. J. Pediatr. Gastroenterol. Nutr. 54, 404–408 (2012).

    Article  PubMed  Google Scholar 

  20. Kruschewski, M., Busch, C., Dorner, A. & Lierse, W. Vascular architecture of the colon in Crohns disease and ulcerative colitis—light-microscopy and scanning electron-microscopy study with special reference to the morphology of the normal colon. Langenbecks Archiv. Fur Chirurgie. 380, 253–259 (1995).

    CAS  PubMed  Google Scholar 

  21. Nylund, K. et al. Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn's disease. Ultrasound Med. Biol. 39, 1197–1206 (2013).

    Article  PubMed  Google Scholar 

  22. Ripolles, T. et al. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn's disease: a comparison with surgical histopathology analysis. J. Crohns Colitis 7, 120–128 (2013).

    Article  PubMed  Google Scholar 

  23. Kim, K. et al. Noninvasive ultrasound elasticity imaging (UEI) of Crohn's disease: animal model. Ultrasound Med. Biol. 34, 902–912 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Stidham, R. W. et al. Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn's disease. Gastroenterology 141, 819–826 (2011).

    Article  PubMed  Google Scholar 

  25. Calabrese, E. et al. Severity of postoperative recurrence in Ccrohn's disease: correlation between endoscopic and sonographic findings. Inflamm. Bowel Dis. 15, 1635–1642 (2009).

    Article  PubMed  Google Scholar 

  26. Rispo, A. et al. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn's disease. Inflamm. Bowel Dis. 12, 486–490 (2006).

    Article  PubMed  Google Scholar 

  27. Castiglione, F. et al. Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohn's disease. Inflamm. Bowel Dis. 14, 1240–1245 (2008).

    Article  PubMed  Google Scholar 

  28. Paredes, J. M. et al. Non-invasive diagnosis and grading of postsurgical endoscopic recurrence in Crohn's disease: usefulness of abdominal ultrasonography and 99mTc-hexamethylpropylene amineoxime-labelled leucocyte scintigraphy. J. Crohns Colitis 4, 537–545 (2010).

    Article  PubMed  Google Scholar 

  29. Paredes, J. M. et al. Contrast-enhanced ultrasonography: usefulness in the assessment of postoperative recurrence of Crohn's disease. J. Crohns Colitis 7, 191–201 (2013).

    Article  Google Scholar 

  30. Cammarota, T. et al. Role of bowel ultrasound as a predictor of surgical recurrence of Crohn's disease. Scand. J. Gastroenterol. 48, 552–555 (2013).

    Article  PubMed  Google Scholar 

  31. Maconi, G. et al. Preoperative characteristics and postoperative behavior of bowel wall on risk of recurrence after conservative surgery in Crohn's disease—a prospective study. Ann. Surg. 233, 345–352 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Siddiki, H. A. et al. Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn's disease. AJR Am. J. Roentgenol. 193, 113–121 (2009).

    Article  PubMed  Google Scholar 

  33. Jensen, M. D., Ormstrup, T., Vagn-Hansen, C., Ostergaard, L. & Rafaelsen, S. R. Interobserver and intermodality agreement for detection of small bowel Crohn's disease with MR enterography and CT enterography. Inflamm. Bowel Dis. 17, 1081–1088 (2011).

    Article  PubMed  Google Scholar 

  34. Maglinte, D. D. T., Sandrasegaran, K., Lappas, J. C. & Chiorean, M. CT enteroclysis. Radiology 245, 661–671 (2007).

    Article  PubMed  Google Scholar 

  35. Engin, G. Computed tomography enteroclysis in the diagnosis of intestinal diseases. J. Comput. Assist. Tomogr. 32, 9–16 (2008).

    Article  PubMed  Google Scholar 

  36. Mazzeo, S. et al. Multidetector CT of the small bowel: evaluation after oral hyperhydration with isotonic solution. Radiologia Medica 109, 516–526 (2005).

    CAS  PubMed  Google Scholar 

  37. Minordi, L. M., Vecchioli, A., Mirk, P. & Bonomo, L. CT enterography with polyethylene glycol solution vs CT enteroclysis in small bowel disease. Br. J. Radiol. 84, 112–119 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hassan, C., Cerro, P., Zullo, A., Spina, C. & Morini, S. Computed tomography enteroclysis in comparison with ileoscopy in patients with Crohn's disease. Int. J. Colorectal Dis. 18, 121–125 (2003).

    PubMed  Google Scholar 

  39. Andersen, K. et al. Multi-detector CT-colonography in inflammatory bowel disease: prospective analysis of CT-findings to high-resolution video colonoscopy. Eur. J. Radiol. 58, 140–146 (2006).

    Article  PubMed  Google Scholar 

  40. Bodily, K. D. et al. Crohn disease: Mural attenuation and thickness at contrast-enhanced CT enterography—correlation with endoscopic and histologic findings of inflammation. Radiology 238, 505–516 (2006).

    Article  PubMed  Google Scholar 

  41. Solem, C. A. et al. Small-bowel imaging in Crohn's disease: a prospective, blinded, 4-way comparison trial. Gastrointest. Endosc. 68, 255–266 (2008).

    Article  PubMed  Google Scholar 

  42. Chiorean, M. V. et al. Correlation of CT enteroclysis with surgical pathology in Crohn's disease. Am. J. Gastroenterol. 102, 2541–2550 (2007).

    Article  PubMed  Google Scholar 

  43. Tong, J. L. et al. Computed tomography enterography versus balloon-assisted enteroscopy for evaluation of small bowel lesions in Crohn's disease. J. Gastroenterol. Hepatol. 28, 1180–1186 (2013).

    Article  PubMed  Google Scholar 

  44. Lee, S. S. et al. CT of prominent pericolic or perienteric vasculature in patients with Crohn's disease: correlation with clinical disease activity and findings on barium studies. AJR Am. J. Roentgenol. 179, 1029–1036 (2002).

    Article  PubMed  Google Scholar 

  45. Wu, Y.-W., Tao, X.-F., Tang, Y.-H., Hao, N.-X. & Miao, F. Quantitative measures of comb sign in Crohn's disease: correlation with disease activity and laboratory indications. Abdom. Imaging 37, 350–358 (2012).

    Article  PubMed  Google Scholar 

  46. Pariente, B. et al. Development of the Crohn's Disease Digestive Damage Score, the Lemann Score. Inflamm. Bowel Dis. 17, 1415–1422 (2011).

    Article  PubMed  Google Scholar 

  47. Samuel, S. et al. Endoscopic skipping of the distal terminal ileum in Crohn's disease can lead to negative results from ileocolonoscopy. Clin. Gastroenterol. Hepatol. 10, 1253–1259 (2012).

    Article  PubMed  Google Scholar 

  48. Maconi, G. et al. Contrast radiology, computed tomography and ultrasonography in detecting internal fistulas and intra-abdominal abscesses in Crohn's disease: a prospective comparative study. Am. J. Gastroenterol. 98, 1545–1555 (2003).

    Article  PubMed  Google Scholar 

  49. Adler, J. et al. Computed tomography enterography findings correlate with tissue inflammation, not fibrosis in resected small bowel Crohn's disease. Inflamm. Bowel Dis. 18, 849–856 (2012).

    Article  PubMed  Google Scholar 

  50. Hara, A. K. & Swartz, P. G. CT enterography of Crohn's disease. Abdom. Imaging. 34, 289–295 (2009).

    Article  PubMed  Google Scholar 

  51. Hara, A. K. et al. Iterative reconstruction technique for reducing body radiation dose at CT: feasibility study. AJR Am. J. Roentgenol. 193, 764–771 (2009).

    Article  PubMed  Google Scholar 

  52. Prakash, P. et al. Reducing abdominal CT radiation dose with adaptive statistical iterative reconstruction technique. Invest. Radiol. 45, 202–210 (2010).

    Article  PubMed  Google Scholar 

  53. Kambadakone, A. R. et al. Low-dose MDCT and CT enterography of patients with Crohn disease: feasibility of adaptive statistical iterative reconstruction. AJR Am. J. Roentgenol. 196, W743–W752 (2011).

    Article  PubMed  Google Scholar 

  54. Hardie, A. D., Horst, N. D. & Mayes, N. Preliminary evaluation of ultra-high pitch computed tomography enterography. Acta Radiologica 53, 1088–1091 (2012).

    Article  PubMed  Google Scholar 

  55. Guimaraes, L. S. et al. Feasibility of dose reduction using novel denoising techniques for low kV (80 kV) CT enterography: optimization and validation. Acad. Radiology 17, 1203–1210 (2010).

    Article  Google Scholar 

  56. Lee, S. J. et al. A prospective comparison of standard-dose CT enterography and 50% reduced-dose CT enterography with and without noise reduction for evaluating Crohn disease. AJR Am. J. Roentgenol. 197, 50–57 (2011).

    Article  PubMed  Google Scholar 

  57. O'Neill, S. B. et al. A prospective feasibility study of sub-millisievert abdominopelvic CT using iterative reconstruction in Crohn's disease. Eur. Radiol. 23, 2503–2512 (2013).

    Article  PubMed  Google Scholar 

  58. Paparo, F. et al. Crohn's disease: prevalence of intestinal and extraintestinal manifestations detected by computed tomography enterography with water enema. Abdom. Imaging. 37, 326–337 (2012).

    Article  CAS  PubMed  Google Scholar 

  59. Soyer, P. et al. Small bowel adenocarcinoma in Crohn disease: CT-enterography features with pathological correlation. Abdom. Imaging 37, 338–349 (2012).

    Article  PubMed  Google Scholar 

  60. Malgras, B. et al. Accuracy of imaging for predicting operative approach in Crohn's disease. Br. J. Surg. 99, 1011–1020 (2012).

    Article  CAS  PubMed  Google Scholar 

  61. Soyer, P. et al. Suspected anastomotic recurrence of Crohn disease after ileocolic resection: evaluation with CT enteroclysis. Radiology 254, 755–764 (2010).

    Article  PubMed  Google Scholar 

  62. Paparo, F. et al. Crohn's disease recurrence in patients with ileocolic anastomosis: value of computed tomography enterography with water enema. Eur. J. Radiol. 82, E434–E440 (2013).

    Article  PubMed  Google Scholar 

  63. Mao, R. et al. CT enterography in evaluating postoperative recurrence of Crohn's disease after ileocolic resection: complementary role to endoscopy. Inflamm. Bowel Dis. 19, 977–982 (2013).

    Article  PubMed  Google Scholar 

  64. Hara, A. K. et al. Using CT enterography to monitor Crohn's disease activity: a preliminary study. AJR Am. J. Roentgenol. 190, 1512–1516 (2008).

    Article  PubMed  Google Scholar 

  65. Wu, Y. W., Tang, Y. H., Hao, N. X., Tang, C. Y., Miao, F. Crohn's disease: CT enterography manifestations before and after treatment. Eur. J. Radiol. 81, 52–59 (2012).

    Article  PubMed  Google Scholar 

  66. Bruining, D. H. et al. Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with Crohn's disease. Clin. Gastroenterol. Hepatol. 9, 679–683 (2011).

    Article  PubMed  Google Scholar 

  67. Bruining, D. H. & Loftus, E. V. Jr. Technology Insight: new techniques for imaging the gut in patients with IBD. Nat. Clin. Pract Gastroenterol. Hepatol. 5, 154–161 (2008).

    Article  PubMed  Google Scholar 

  68. Cipriano, L. E., Levesque, B. G., Zaric, G. S., Loftus, E. V. Jr & Sandborn, W. J. Cost-effectiveness of imaging strategies to reduce radiation-induced cancer risk in Crohn's disease. Inflamm. Bowel Dis. 18, 1240–1248 (2012).

    Article  PubMed  Google Scholar 

  69. Rieber, A., Nussle, K., Reinshagen, M., Brambs, H. J. & Gabelmann, A. MRI of the abdomen with positive oral contrast agents for the diagnosis of inflammatory small bowel disease. Abdom. Imaging 27, 394–399 (2002).

    Article  CAS  PubMed  Google Scholar 

  70. Lauenstein, T. C. et al. Optimization of oral contrast agents for MR imaging of the small bowel. Radiology 228, 279–283 (2003).

    Article  PubMed  Google Scholar 

  71. Fidler, J. L., Guimaraes, L. & Einstein, D. M. MR imaging of the small bowel. Radiographics 29, 1811–1826 (2009).

    Article  PubMed  Google Scholar 

  72. Horsthuis, K., Bipat, S., Stokkers, P. C. F. & Stoker, J. Magnetic resonance imaging for evaluation of disease activity in Crohn's disease: a systematic review. Eur. Radiol. 19, 1450–1460 (2009).

    Article  PubMed  Google Scholar 

  73. Maccioni, F. et al. MR imaging in patents with Crohn disease: value of T2-versus T1-weighted gadolinium-enhanced MR sequences with use of an oral superparamagnetic contrast agent. Radiology 238, 517–530 (2006).

    Article  PubMed  Google Scholar 

  74. Masselli, G. & Gualdi, G. MR imaging of the small bowel. Radiology 264, 333–348 (2012).

    Article  PubMed  Google Scholar 

  75. Rimola, J. et al. Magnetic resonance imaging for evaluation of Crohn's disease: validation of parameters of severity and quantitative index of activity. Inflamm. Bowel Dis. 17, 1759–1768 (2011).

    Article  PubMed  Google Scholar 

  76. Gourtsoyiannis, N. et al. Assessment of Crohn's disease activity in the small bowel with MR and conventional enteroclysis: preliminary results. Eur. Radiol. 14, 1017–1024 (2004).

    Article  PubMed  Google Scholar 

  77. Steward, M. J. 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. 81, 2080–2088 (2012).

    Article  PubMed  Google Scholar 

  78. Fiorino, G. 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. 17, 1073–1080 (2011).

    Article  CAS  PubMed  Google Scholar 

  79. Rimola, J. et al. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease. Gut 58, 1113–1120 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Buisson, A. et al. Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn's disease. Aliment. Pharmacol. Ther. 37, 537–545 (2013).

    Article  CAS  PubMed  Google Scholar 

  81. Ream, J. M. et al. MRI diffusion-weighted imaging (DWI) in pediatric small bowel Crohn disease: correlation with MRI findings of active bowel wall inflammation. Pediatr. Radiol. 43, 1077–1085 (2013).

    Article  PubMed  Google Scholar 

  82. Oto, A. 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 33, 615–624 (2011).

    Article  PubMed  Google Scholar 

  83. Hordonneau, C. et al. Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn's disease: validation of quantitative index of activity. Am. J. Gastroenterol. 109, 89–98 (2014).

    Article  CAS  PubMed  Google Scholar 

  84. Bickelhaupt, S. et al. Crohn's disease: small bowel motility impairment correlates with inflammatory-related markers C-reactive protein and calprotectin. Neurogastroenterol. Motil. 25, 467–473 (2013).

    Article  CAS  PubMed  Google Scholar 

  85. Bickelhaupt, S. et al. Differentiation between active and chronic Crohn's disease using MRI small-bowel motility examinations—initial experience. Clin. Radiol. 68, 1247–1253 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Maccioni, F., Staltari, I., Pino, A. R. & Tiberti, A. Value of T2-weighted magnetic resonance imaging in the assessment of wall inflammation and fibrosis in Crohn's disease. Abdom. Imaging 37, 944–957 (2012).

    Article  CAS  PubMed  Google Scholar 

  87. Punwani, S. et al. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features. Radiology 252, 712–720 (2009).

    Article  PubMed  Google Scholar 

  88. Breynaert, C. et al. Unique gene expression and MR T-2 relaxometry patterns define chronic murine dextran sodium sulphate colitis as a model for connective tissue changes in human Crohn's disease. PLoS ONE 8, e68876 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Adler, J. et al. Magnetization transfer helps detect intestinal fibrosis in an animal model of Crohn disease. Radiology 259, 127–135 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Larsson, A. E. et al. Magnetic resonance imaging of experimental mouse colitis and association with inflammatory activity. Inflamm. Bowel Dis. 12, 478–485 (2006).

    Article  PubMed  Google Scholar 

  91. Mustafi, D. et al. High-resolution magnetic resonance colonography and dynamic contrast-enhanced magnetic resonance imaging in a murine model of colitis. Magn. Reson. Med. 63, 922–929 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Pazahr, S. et al. Magnetization transfer for the assessment of bowel fibrosis in patients with Crohn's disease: initial experience. Magn. Reson. Mat. Phys. Biol. Med. 26, 291–301 (2013).

    Article  CAS  Google Scholar 

  93. Menys, A. et al. Small bowel strictures in Crohn's disease: a quantitative investigation of intestinal motility using MR enterography. Neurogastroenterol. Motil. 25, 967–e775 (2013).

    Article  CAS  PubMed  Google Scholar 

  94. Van Assche, G. 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 7, 950–957 (2013).

    Article  PubMed  Google Scholar 

  95. Ordás, I. et al. Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn's disease. Gastroenterology 146, 374–382 (2014).

    Article  CAS  PubMed  Google Scholar 

  96. Cheriyan, D. G. et al. Impact of magnetic resonance enterography in the management of small bowel Crohn's disease. Eur. J. Gastroenterol. Hepatol. 25, 550–555 (2013).

    Article  PubMed  Google Scholar 

  97. Sailer, J. et al. Anastomotic recurrence of Crohn's disease after ileocolic resection: comparison of MR enteroclysis with endoscopy. Eur. Radiol. 18, 2512–2521 (2008).

    Article  PubMed  Google Scholar 

  98. Koilakou, S. et al. Endoscopy and MR enteroclysis: equivalent tools in predicting clinical recurrence in patients with Crohn's disease after ileocolic resection. Inflamm. Bowel Dis. 16, 198–203 (2010).

    Article  PubMed  Google Scholar 

  99. Basu, S. et al. Functional imaging of inflammatory diseases using nuclear medicine techniques. Semin. Nucl. Med. 39, 124–145 (2009).

    Article  PubMed  Google Scholar 

  100. Gotthardt, M., Bleeker-Rovers, C. P., Boerman, O. C. & Oyen, W. J. G. Imaging of inflammation by PET, conventional scintigraphy, and other imaging techniques. J. Nucl. Med. 51, 1937–1949 (2010).

    PubMed  Google Scholar 

  101. ICRP. Annex C Biokinetic models and dose tables. Ann. ICRP 38, 51–162 (2008).

  102. Love, C. & Palestro, C. J. Radionuclide imaging of inflammation and infection in the acute care setting. Semin. Nucl. Med. 43, 102–113 (2013).

    Article  PubMed  Google Scholar 

  103. Lee, B. F. et al. Use of Tc-99m (V) DMSA scintigraphy in the detection and localization of intestinal inflammation: comparison of findings at colonoscopy and biopsy. Radiology 220, 381–385 (2001).

    Article  CAS  PubMed  Google Scholar 

  104. Koutroubakis, I. E. et al. Active inflammatory bowel disease: Evaluation with 99mTc (V) DMSA scintigraphy. Radiology 229, 70–74 (2003).

    Article  PubMed  Google Scholar 

  105. Stathaki, M. I. et al. Active inflammatory bowel disease: head-to-head comparison between Tc-99m-hexamethylpropylene amine oxime white blood cells and Tc-99m(V)-dimercaptosuccinic acid scintigraphy. Nucl. Med. Commun. 29, 27–32 (2008).

    Article  PubMed  Google Scholar 

  106. Ercan, M. T. et al. Evaluation of Tc-99m(V) DMSA for imaging inflammatory lesions: an experimental study. Ann. Nucl. Med. 10, 419–423 (1996).

    Article  CAS  PubMed  Google Scholar 

  107. Papantoniou, V. et al. Imaging in situ breast carcinoma (with or without an invasive component) with technetium-99m pentavalent dimercaptosuccinic acid and technetium-99m 2-methoxy isobutyl isonitrile scintimammography. Breast Cancer Res. 7, R33–R45 (2005).

    Article  CAS  PubMed  Google Scholar 

  108. Bai, L., Collins, J. F. & Ghishan, F. K. Cloning and characterization of a type IIINa-dependent phosphate cotransporter from mouse intestine. Am. J. Physiol. Cell Physiol. 279, C1135–C1143 (2000).

    Article  CAS  PubMed  Google Scholar 

  109. Spier, B. J., Perlman, S. B. & Reichelderfer, M. FDG-PET in inflammatory bowel disease. Q. J. Nucl. Med. Mol. Imaging. 53, 64–71 (2009).

    CAS  PubMed  Google Scholar 

  110. Halpenny, D. F., Burke, J. P., Lawlor, G. O. & O'Connell, M. Role of PET and combination PET/CT in the evaluation of patients with inflammatory bowel disease. Inflamm. Bowel Dis. 15, 951–958 (2009).

    Article  PubMed  Google Scholar 

  111. Perlman, S. B., Hall, B. S. & Reichelderfer, M. PET/CT Imaging of Inflammatory Bowel Disease. Semin. Nucl. Med. 43, 420–426 (2013).

    Article  PubMed  Google Scholar 

  112. Roca, M., de Vries, E. F. J., Jamar, F., Israel, O. & Signore, A. Guidelines for the labelling of leucocytes with In-111-oxine. Eur. J. Nucl. Med. Mol. Imaging 37, 835–841 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  113. de Vries, E. F. J., Roca, M., Jamar, F., Israel, O. & Signore, A. Guidelines for the labelling of leucocytes with Tc-99m-HMPAO. Eur. J. Nucl. Med. Mol. Imaging 37, 842–848 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Watkinson, J. C. et al. Pharmacokinetics, biodistribution and dosimetry of Tc-99m(V)DMSA in humans with squamous-cell carcinoma. Nucl. Med. Commun. 11, 343–359 (1990).

    Article  CAS  PubMed  Google Scholar 

  115. Saboury, B., Torigian, D. A. & Alavi, A. Comment on: “FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging, version 1.0”. Eur. J. Nucl. Med. Mol. Imaging 37, 1430–1431 (2010).

    Article  PubMed  Google Scholar 

  116. Biancone, L. et al. Technetium-99m-HMPAO labeled leukocyte single photon emission computerized tomography (SPECT) for assessing Crohn's disease extent and intestinal infiltration. Am. J. Gastroenterol. 100, 344–354 (2005).

    Article  CAS  PubMed  Google Scholar 

  117. Hillel, P. G., Lorenz, E., Metherall, P. & Tindale, W. B. Tc-99m white-cell imaging in inflammatory bowel disease: a comparison of planar versus SPECT. Nucl. Med. Commun. 32, 591–596 (2011).

    Article  PubMed  Google Scholar 

  118. Mariani, G. et al. A review on the clinical uses of SPECT/CT. Eur. J. Nucl. Med. Mol. Imaging 37, 1959–1985 (2010).

    Article  PubMed  Google Scholar 

  119. Yap, K. S., Patel, C. N., Chowdhury, F. U. & Scarsbrook, A. F. Less commonly used and emerging clinical applications of SPECT-CT in benign and malignant disease. Nucl. Med. Commun. 33, 808–818 (2012).

    Article  PubMed  Google Scholar 

  120. Bailey, D. L. & Willowson, K. P. An evidence-based review of quantitative SPECT imaging and potential clinical applications. J. Nucl. Med. 54, 83–89 (2013).

    Article  PubMed  Google Scholar 

  121. Dionisio, P. M. et al. Capsule endoscopy has a significantly higher diagnostic yield in patients with suspected and established small-bowel Crohn's disease: a meta-analysis. Am. J. Gastroenterol. 105, 1240–1248 (2010).

    Article  PubMed  Google Scholar 

  122. Tukey, M., Pleskow, D., Legnani, P., Cheifetz, A. S. & Moss, A. C. The utility of capsule endoscopy in patients with suspected Crohn's disease. Am. J. Gastroenterol. 104, 2734–2739 (2009).

    Article  PubMed  Google Scholar 

  123. Annese, V. et al. European evidence based consensus for endoscopy in inflammatory bowel disease. J. Crohn's Colitis 7, 982–1018 (2013).

    Article  Google Scholar 

  124. Flamant, M. T. C. et al. The prevalence and outcome of jejunal lesions visualized by small bowel capsule endoscopy in Crohn's disease. Inflamm. Bowel Dis. 19, 1390–1396 (2013).

    Article  PubMed  Google Scholar 

  125. Park, S. K. et al. Long-term prognosis of the jejunal involvement of Crohn's disease. J. Clin. Gastroenterol. 400–408 (2013).

    Article  PubMed  Google Scholar 

  126. Beltrain, V. P. et al. Evaluation of postsurgical recurrence in Crohn's disease: a new indication for capsule endoscopy. Gastrointest. Endosc. 66, 533–540 (2007).

    Article  Google Scholar 

  127. Bourreille, A. et al. Wireless capsule endoscopy versus ileocolonoscopy for the diagnosis of post operative recurrence of Crohn's disease: a prospective study. Gut 55, 978–983 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Maunoury, V. et al. Value of wireless capsule endoscopy in patients with indeterminate colitis (inflammatory bowel disease type unclassified). Inflamm. Bowel Dis. 13, 152–155 (2007).

    Article  PubMed  Google Scholar 

  129. Meister, T. et al. Colon capsule endoscopy versus standard colonoscopy in assessing disease activity in patients with ulcerative colitis: a prospective trial. Gastrointest. Endosc. 75, 641–646 (2012).

    Article  Google Scholar 

  130. Sung, J. et al. The use of Pillcam Colon in assessing mucosal inflammation in ulcerative colitis: a multicenter study. Endoscopy 44, 754–758 (2012).

    Article  CAS  PubMed  Google Scholar 

  131. Schluender, S. J. et al. Does preoperative wireless endoscopic capsule predict long-term outcome after heal pouch-anal anastomosis (IPAA)? Gastroenterology 130, A214 (2006).

    Article  Google Scholar 

  132. Rahmi, G. et al. Multicenter comparison of double-balloon enteroscopy and spiral enteroscopy. J. Gastroenterol. Hepatol. 28, 992–998 (2013).

    Article  PubMed  Google Scholar 

  133. Pasha, S. F. et al. Double-balloon enteroscopy and capsule endoscopy have comparable diagnostic yield in small-bowel disease: a meta-analysis. Clin. Gastroenterol. Hepatol. 6, 671–676 (2008).

    Article  PubMed  Google Scholar 

  134. Esaki, M., Kubokura, T., Kudo, T. & Matsumoto, T. Endoscopic findings under narrow band imaging in ulcerative colitis. Dig. Endosc. 23, 140–142 (2011).

    Article  PubMed  Google Scholar 

  135. Hurlstone, D. P. et al. The role of high-magnificationchromoscopic colonoscopy in hereditary nonpolyposis colorectal cancer screening: a prospective “back-to-back” endoscopic study. Am. J. Gastroenterol. 100, 2167–2173 (2005).

    Article  PubMed  Google Scholar 

  136. Wu, L., Li, P., Wu, J., Cao, Y. & Gao, F. The diagnostic accuracy of chromoendoscopy for dysplasia in ulcerative colitis: meta-analysis of six randomized controlled trials. Colorectal Dis. 14, 416–420 (2012).

    Article  CAS  PubMed  Google Scholar 

  137. Pellisé, M. et al. Narrow-band imaging as an alternative to chromoendoscopy for the detection of dysplasia in long-standing inflammatory bowel disease: a prospective, randomized, crossover study. Gastrointest. Endosc. 74, 840–848 (2011).

    Article  PubMed  Google Scholar 

  138. Kiesslich, R. et al. Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 132, 874–882 (2007).

    Article  PubMed  Google Scholar 

  139. Kiesslich, R. et al. Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease. Gut 61, 1146–1153 (2012).

    Article  CAS  PubMed  Google Scholar 

  140. Buda, A. et al. Confocal laser endomicroscopy for prediction of disease relapse in ulcerative colitis: A pilot study. J. Crohns Colitis 8, 304–311 (2013).

    Article  PubMed  Google Scholar 

  141. Atreya, R. et al. In vivo molecular imaging using fluorescent anti-TNF antibodies and confocal laser endomicroscopy predicts response to anti-TNF therapy in Crohn's disease. Gastroenterology 144, S85–S86 (2013).

    Article  Google Scholar 

  142. Cipolletta, L. et al. Endocytoscopy can identify dysplasia in aberrant crypt foci of the colorectum: a prospective in vivo study. Endoscopy 41, 129–132 (2009).

    Article  CAS  PubMed  Google Scholar 

  143. Gralnek, I. M. et al. A prospective cohort study evaluating a novel colonoscopy platform featuring full-spectrum endoscopy. Endoscopy 45, 697–702 (2013).

    Article  PubMed  Google Scholar 

  144. Gralnek, I. M. et al. Standard forward-viewing colonoscopy versus full-spectrum endoscopy: an international, multicentre, randomised, tandem colonoscopy trial. Lancet Oncol. 15, 353–360 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge L. Guimarães and R. Cunha, from the Department of Radiology, and T. Vieira, from the Department of Nuclear Medicine, Hospital de São João, Porto, Portugal, for their critical review of the article, technical support and image analysis.

Author information

Authors and Affiliations

  1. Department of Gastroenterology, Chaim Sheba Medical Center, Sackler School of Medicine, Tel Hashomer, 5265601, Israel

    Rami Eliakim

  2. Department of Pharmacology & Therapeutics, Faculty of Medicine, Alameda Professor Hernâni Monteiro, Porto, 4200-319, Portugal

    Fernando Magro

Authors
  1. Rami Eliakim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Magro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Both authors contributed to all aspects of this manuscript.

Corresponding author

Correspondence to Rami Eliakim.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eliakim, R., Magro, F. Imaging techniques in IBD and their role in follow-up and surveillance. Nat Rev Gastroenterol Hepatol 11, 722–736 (2014). https://doi.org/10.1038/nrgastro.2014.144

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrgastro.2014.144

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing