Skip to main content

Advertisement

SpringerLink
Log in

Intestinal ultrasound in inflammatory bowel disease: New kid on the block

  • Narrative review
  • Published:
Indian Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Intestinal ultrasound is an emerging technique for diagnosing and monitoring patients with inflammatory bowel disease (IBD). It is a simple, non-invasive, inexpensive, safe and reliable tool for monitoring patients with IBD. This technique has good diagnostic accuracy in the assessment of the extent and severity of IBD and its complications. The most commonly used parameters are bowel wall thickness, color Doppler flow, bowel wall stratification and peri-bowel inflammation. Various scoring systems have been developed utilizing the above parameters to monitor patients with IBD. It is a good tool to monitor response to therapy and follow-up for post-operative recurrence. Early response on intestinal ultrasound (IUS) predicts long-term clinical remission and mucosal healing in patients with Crohn’s disease. In patients with ulcerative colitis (UC), the response to IUS can be assessed as early as two weeks. Recent data has emerged to predict the response to corticosteroids and colectomy in patients with acute severe UC. Point of care IUS in the outpatient clinic is an excellent tool to follow-up patients and guide clinical decision-making and has good acceptability among patients. It is an underutilized technique in spite of its appeal and the availability of evidence. Underutilization can be attributed to the lack of awareness, expertise and training centres. This review discusses the technical details and the evidence to support the use of IUS in IBD. We aim to increase awareness and use of intestinal ultrasound and build local expertise and data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Flowchart 1

Similar content being viewed by others

Data availability

Yes.

References

  1. Turner D, Ricciuto A, Lewis A, et al. STRIDE-II: an Update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): Determining Therapeutic Goals for Treat-to-Target strategies in IBD. Gastroenterology. 2021;160:1570–83. https://doi.org/10.1053/j.gastro.2020.12.031.

  2. Fernandes SR, Rodrigues RV, Bernardo S, et al. Transmural healing is associated with improved long-term outcomes of patients with Crohn’s disease. Inflamm Bowel Dis. 2017;23:1403–9. https://doi.org/10.1097/MIB.0000000000001143.

  3. Lafeuille P, Hordonneau C, Vignette J, et al. Transmural healing and MRI healing are associated with lower risk of bowel damage progression than endoscopic mucosal healing in Crohn’s disease. Aliment Pharmacol Ther. 2021;53:577–86. https://doi.org/10.1111/apt.16232.

  4. Messadeg L, Hordonneau C, Bouguen G, et al.  Early transmural response assessed using magnetic resonance imaging could predict sustained clinical remission and prevent bowel damage in patients with Crohn’s disease treated with anti-tumour necrosis factor therapy. J Crohns Colitis. 2020;14:1524–34. https://doi.org/10.1093/ecco-jcc/jjaa098.

  5. Piazza O Sed N, Noviello D, Filippi E, et al. Superior predictive value of transmural over endoscopic severity for colectomy risk in ulcerative colitis: a multicenter prospective cohort study. J Crohns Colitis. 2023. https://doi.org/10.1093/ecco-jcc/jjad152.

  6. Asthana AK, Friedman AB, Maconi G, et al. Failure of gastroenterologists to apply intestinal ultrasound in inflammatory bowel disease in the Asia-Pacific: a need for action. J Gastroenterol Hepatol. 2015;30:446–52. https://doi.org/10.1111/jgh.12871.

  7. Kimmey MB, Martin RW, Haggitt RC, Wang KY, Franklin DW, Silverstein FE. Histologic correlates of gastrointestinal ultrasound images. Gastroenterology. 1989;96:433–41. https://doi.org/10.1016/0016-5085(89)91568-0.

  8. Nylund K, Maconi G, Hollerweger A, et al. EFSUMB recommendations and guidelines for gastrointestinal ultrasound. Ultraschall Med. 2017;38:e1–15. https://doi.org/10.1055/s-0042-115853.

  9. Pinto PN, Chojniak R, Cohen MP, Yu LS, Queiroz-Andrade M, Bitencourt AG. Comparison of three types of preparations for abdominal sonography. J Clin Ultrasound. 2011;39:203–8. https://doi.org/10.1002/jcu.20790.

  10. Nylund K, Hausken T, Ødegaard S, Eide GE, Gilja OH. Gastrointestinal wall thickness measured with transabdominal ultrasonography and its relationship to demographic factors in healthy subjects. Ultraschall Med. 2012;33:E225–32. https://doi.org/10.1055/s-0031-1299329.

    Article  CAS  PubMed  Google Scholar 

  11. Dong J, Wang H, Zhao J, et al.  Ultrasound as a diagnostic tool in detecting active Crohn’s disease: a meta-analysis of prospective studies. Eur Radiol. 2014;24:26–33. https://doi.org/10.1007/s00330-013-2973-0.

  12. Sasaki T, Kunisaki R, Kinoshita H, et al. Use of color Doppler ultrasonography for evaluating vascularity of small intestinal lesions in Crohn’s disease: correlation with endoscopic and surgical macroscopic findings. Scand J Gastroenterol. 2014;49:295–301. https://doi.org/10.3109/00365521.2013.871744.

  13. Limberg B. Diagnosis of chronic inflammatory bowel disease by ultrasonography. Z Gastroenterol. 1999;37:495–508.

    CAS  PubMed  Google Scholar 

  14. Rigazio C, Ercole E, Laudi C, et al. Abdominal bowel ultrasound can predict the risk of surgery in Crohn’s disease: proposal of an ultrasonographic score. Scand J Gastroenterol. 2009;44:585–93. https://doi.org/10.1080/00365520802705992.

  15. Maconi G, Greco S, Duca P, et al. Prevalence and clinical significance of sonographic evidence of mesenteric fat alterations in Crohn’s disease. Inflamm Bowel Dis. 2008;14:1555–61. https://doi.org/10.1002/ibd.20515.

  16. Maconi G, Di Sabatino A, Ardizzone S, et al. Prevalence and clinical significance of sonographic detection of enlarged regional lymph nodes in Crohn’s disease. Scand J Gastroenterol. 2005;40:1328–33. https://doi.org/10.1080/00365510510025746.

  17. 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;19:991–8. https://doi.org/10.1097/MIB.0b013e3182802b87.

  18. Ripollés T, Martínez-Pérez MJ, Paredes JM, Vizuete J, García-Martínez E, Jiménez-Restrepo DH. Contrast-enhanced ultrasound in the differentiation between phlegmon and abscess in Crohn’s disease and other abdominal conditions. Eur J Radiol. 2013;82:e525–31. https://doi.org/10.1016/j.ejrad.2013.05.043.

  19. Calabrese E, Maaser C, Zorzi F, et al. Bowel ultrasonography in the management of Crohn’s disease. A review with recommendations of an international panel of experts. Inflamm Bowel Dis. 2016;22:1168–83. https://doi.org/10.1097/MIB.0000000000000706.

  20. 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;34:125–45. https://doi.org/10.1111/j.1365-2036.2011.04710.x.

  21. Taylor SA, Mallett S, Bhatnagar G, et al. Diagnostic accuracy of magnetic resonance enterography and small bowel ultrasound for the extent and activity of newly diagnosed and relapsed Crohn’s disease (METRIC): a multicentre trial. Lancet Gastroenterol Hepatol. 2018;3:548–58. https://doi.org/10.1016/S2468-1253(18)30161-4.

  22. Allocca M, Fiorino G, Bonovas S, et al. Accuracy of Humanitas Ultrasound Criteria in assessing disease activity and severity in ulcerative colitis: a prospective study. J Crohns Colitis. 2018;12:1385–91. https://doi.org/10.1093/ecco-jcc/jjy107.

  23. Pascu M, Roznowski AB, Müller HP, Adler A, Wiedenmann B, Dignass AU. Systematic review: clinical utility of gastrointestinal ultrasound in the diagnosis, assessment and management of patients with ulcerative colitis. J Crohns Colitis. 2020;14:465–79. https://doi.org/10.1093/ecco-jcc/jjz163.

  24. Pascu M, Roznowski, Dignass AU. Clinical relevance of transabdominal ultrasonography and magnetic resonance imaging in patients with inflammatory bowel disease of the terminal ileum and large bowel. Inflamm Bowel Dis. 2004;10:373–82. https://doi.org/10.1097/00054725-200407000-00008.

  25. Kakkadasam Ramaswamy P, Vizhi NK, Yelsangikar A, Krishnamurthy AN, Bhat V, Bhat N. Utility of bowel ultrasound in assessing disease activity in Crohn’s disease. Indian J Gastroenterol. 2020;39:495–502. https://doi.org/10.1007/s12664-020-01019-w.

  26. Futagami Y, Haruma K, Hata J, et al. Development and validation of an ultrasonographic activity index of Crohn’s disease. Eur J Gastroenterol Hepatol. 1999;11:1007–12. https://doi.org/10.1097/00042737-199909000-00010.

  27. Novak KL, Kaplan GG, Panaccione R, et al. A simple ultrasound score for the accurate detection of inflammatory activity in Crohn’s disease. Inflamm Bowel Dis. 2017;23:2001–10. https://doi.org/10.1097/MIB.0000000000001174.

  28. Neye H, Voderholzer W, Rickes S, Weber J, Wermke W, Lochs H. Evaluation of criteria for the activity of Crohn’s disease by power Doppler sonography. Dig Dis. 2004;22:67–72. https://doi.org/10.1159/000078737.

    Article  PubMed  Google Scholar 

  29. Allocca M, Craviotto V, Bonovas S, et al. Predictive value of bowel ultrasound in Crohn’s disease: a 12-month prospective study. Clin Gastroenterol Hepatol. 2022;20:e723–40. https://doi.org/10.1016/j.cgh.2021.04.029.

  30. Novak KL, Nylund K, Maaser C, et al. Expert Consensus on Optimal Acquisition and Development of the International Bowel Ultrasound Segmental Activity Score [IBUS-SAS]: A reliability and inter-rater variability study on intestinal ultrasonography in Crohn’s disease. J Crohns Colitis. 2021;15:609–16. https://doi.org/10.1093/ecco-jcc/jjaa216.

  31. Ramaswamy KP, Yelsangikar A, Nagarajan KV, Nagar A, Bhat N. P154 Development of a novel ultrasound based score for assessing disease activity in ulcerative colitis: preliminary results. J Crohns Colitis. 2019;13:S166. https://doi.org/10.1093/ecco-jcc/jjy222.278.

  32. Civitelli F, Di Nardo G, Oliva S, et al. Ultrasonography of the colon in pediatric ulcerative colitis: a prospective, blind, comparative study with colonoscopy. J Pediatr. 2014;165:78-84.e2. https://doi.org/10.1016/j.jpeds.2014.02.055.

  33. Hashimoto Y, Kume N, Sato K, et al. Development of a novel transabdominal ultrasound disease activity score in patients with ulcerative colitis (UCUS score). J Crohn’s Colitis. 2018;12:S269. https://doi.org/10.1093/ecco-jcc/jjx180.458.

  34. Parente F, Molteni M, Marino B, et al. Are colonoscopy and bowel ultrasound useful for assessing response to short-term therapy and predicting disease outcome of moderate-to-severe forms of ulcerative colitis?: a prospective study. Am J Gastroenterol. 2010;105:1150–7. https://doi.org/10.1038/ajg.2009.672.

  35. Ishikawa D, Ando T, Watanabe O, et al. Images of colonic real-time tissue sonoelastography correlate with those of colonoscopy and may predict response to therapy in patients with ulcerative colitis. BMC Gastroenterol. 2011;11:29. https://doi.org/10.1186/1471-230X-11-29.

  36. Bots S, Nylund K, Löwenberg M, Gecse K, D'Haens G. Intestinal ultrasound to assess disease activity in ulcerative colitis: development of a novel UC-ultrasound index. J Crohns Colitis. 2021;15:1264–71. https://doi.org/10.1093/ecco-jcc/jjab002.

  37. Goodsall TM, Nguyen TM, Parker CE, et al. Systematic review: gastrointestinal ultrasound scoring indices for inflammatory bowel disease. J Crohns Colitis. 2021;15:125–42. https://doi.org/10.1093/ecco-jcc/jjaa129.

  38. Maconi G, Bollani S, Bianchi Porro G. Ultrasonographic detection of intestinal complications in Crohn’s disease. Dig Dis Sci. 1996;41:1643–8. https://doi.org/10.1007/BF02087914.

  39. Kohn A, Cerro P, Milite G, De Angelis E, Prantera C. Prospective evaluation of transabdominal bowel sonography in the diagnosis of intestinal obstruction in Crohn’s disease: comparison with plain abdominal film and small bowel enteroclysis. Inflamm Bowel Dis. 1999;5:153–7.

  40. Gasche C, Moser G, Turetschek K, Schober E, Moeschl P, Oberhuber G. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut. 1999;44:112–7. https://doi.org/10.1136/gut.44.1.112.

  41. Neye H, Ensberg D, Rauh P, et al. Impact of high-resolution transabdominal ultrasound in the diagnosis of complications of Crohn’s disease. Scand J Gastroenterol. 2010;45:690–5. https://doi.org/10.3109/00365521003710190.

  42. Parente F, Maconi G, Bollani S. Bowel ultrasound in assessment of Crohn’s disease and detection of related small bowel strictures: a prospective comparative study versus x ray and intraoperative findings. Gut. 2002;50:490–5. https://doi.org/10.1136/gut.50.4.490.

  43. Calabrese E, La Seta F, Buccellato A, et al. Crohn’s disease: a comparative prospective study of transabdominal ultrasonography, small intestine contrast ultrasonography, and small bowel enema. Inflamm Bowel Dis. 2005;11:139–45. https://doi.org/10.1097/00054725-200502000-00007.

  44. Bettenworth D, Bokemeyer A, Baker M, et al. Assessment of Crohn’s disease-associated small bowel strictures and fibrosis on cross-sectional imaging: a systematic review. Gut. 2019;68:1115–26. https://doi.org/10.1136/gutjnl-2018-318081.

  45. Bettenworth D, Bokemeyer A, Baker M, et al. Small bowel stenosis in Crohn’s disease: clinical, biochemical and ultrasonographic evaluation of histological features. Aliment Pharmacol Ther. 2003;18:749–56. https://doi.org/10.1046/j.1365-2036.2003.01673.x.

  46. Rispo A, Imperatore N, Testa A, et al. Diagnostic accuracy of ultrasonography in the detection of postsurgical recurrence in Crohn’s disease: a systematic review with meta-analysis. Inflamm Bowel Dis. 2018;24:977–88. https://doi.org/10.1093/ibd/izy012.

  47. Martínez MJ, Ripollés T, Paredes JM, Moreno-Osset E, Pazos JM, Blanc E. Intravenous contrast-enhanced ultrasound for assessing and grading postoperative recurrence of Crohn’s disease. Dig Dis Sci. 2019;64:1640–50. https://doi.org/10.1007/s10620-018-5432-6.

  48. Kucharzik T, Wittig BM, Helwig U, et al. Use of intestinal ultrasound to monitor Crohn’s disease activity. Clin Gastroenterol Hepatol. 2017;15:535–42.e2. https://doi.org/10.1016/j.cgh.2016.10.040.

  49. Ripollés T, Paredes JM, Martínez-Pérez MJ, et al. Ultrasonographic changes at 12 weeks of anti-TNF drugs predict 1-year sonographic response and clinical outcome in Crohn’s disease: A multicenter study. Inflamm Bowel Dis. 2016;22:2465–73. https://doi.org/10.1097/MIB.0000000000000882.

  50. Castiglione F, Mainenti P, Testa A, et al. Cross-sectional evaluation of transmural healing in patients with Crohn’s disease on maintenance treatment with anti-TNF alpha agents. Dig Liver Dis. 2017;49:484–9. https://doi.org/10.1016/j.dld.2017.02.014.

  51. Maaser C, Petersen F, Helwig U, et al. Intestinal ultrasound for monitoring therapeutic response in patients with ulcerative colitis: results from the TRUST&UC study. Gut. 2020;69:1629–36. https://doi.org/10.1136/gutjnl-2019-319451.

  52. Arienti V, Campieri M, Boriani L, et al. Management of severe ulcerative colitis with the help of high resolution ultrasonography. Am J Gastroenterol. 1996;91:2163–9.

  53. de Voogd F, van Wassenaer EA, Mookhoek A, et al. Intestinal ultrasound is accurate to determine endoscopic response and remission in patients with moderate to severe ulcerative colitis: A longitudinal prospective cohort study. Gastroenterology. 2022;163:1569–81. https://doi.org/10.1053/j.gastro.2022.08.038.

  54. Scarallo L, Maniscalco V, Paci M, et al. Bowel ultrasound scan predicts corticosteroid failure in children with acute severe colitis. J Pediatr Gastroenterol Nutr. 2020;71:46–51. https://doi.org/10.1097/MPG.0000000000002677.

  55. Ilvemark JFKF, Wilkens R, Thielsen P,  et al. Early intestinal ultrasound predicts intravenous corticosteroid response in hospitalised patients with severe ulcerative colitis. J Crohns Colitis. 2022;16:1725–34. https://doi.org/10.1093/ecco-jcc/jjac083.

  56. Ilvemark JFKF, Hansen T, Goodsall TM, et al. Defining transabdominal intestinal ultrasound treatment response and remission in inflammatory bowel disease: Systematic review and expert consensus statement. J Crohns Colitis. 2022;16:554–80. https://doi.org/10.1093/ecco-jcc/jjab173.

  57. Novak KL, Jacob D, Kaplan GG. Point of care ultrasound accurately distinguishes inflammatory from noninflammatory disease in patients presenting with abdominal pain and diarrhea. Can J Gastroenterol Hepatol. 2016;2016:4023065. https://doi.org/10.1155/2016/4023065.

  58. Bots S, De Voogd F, De Jong M, et al. Point-of-care intestinal ultrasound in IBD patients: disease management and diagnostic yield in a real-world cohort and proposal of a point-of-care algorithm. J Crohns Colitis. 2022;16:606–15. https://doi.org/10.1093/ecco-jcc/jjab175.

  59. Buisson A, Gonzalez F, Poullenot F, et al. Comparative acceptability and perceived clinical utility of monitoring tools: A nationwide survey of patients with inflammatory bowel disease. Inflamm Bowel Dis. 2017;23:1425–33. https://doi.org/10.1097/MIB.0000000000001140.

  60. Allocca M, Fiorino G, Bonifacio C. Comparative accuracy of bowel ultrasound versus magnetic resonance enterography in combination with colonoscopy in assessing Crohn’s disease and guiding clinical decision-making. J Crohns Colitis. 2018;12:1280–7. https://doi.org/10.1093/ecco-jcc/jjy093.

  61. Sagami S, Kobayashi T, Aihara K, et al. Transperineal ultrasound predicts endoscopic and histological healing in ulcerative colitis. Aliment Pharmacol Ther. 2020;51:1373–83. https://doi.org/10.1111/apt.15767.

  62. Sagami S, Kobayashi T, Aihara K, et al. Early improvement in bowel wall thickness on transperineal ultrasonography predicts treatment success in active ulcerative colitis. Aliment Pharmacol Ther. 2022;55:1320–9. https://doi.org/10.1111/apt.16817.

  63. Dolinger MT, Kayal M. Intestinal ultrasound as a non-invasive tool to monitor inflammatory bowel disease activity and guide clinical decision making. World J Gastroenterol. 2023;29:2272–82. https://doi.org/10.3748/wjg.v29.i15.2272.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I wish to acknowledge my mentors in this field. Dr Pradeep Kakkadasam Ramaswamy (Gold Coast University Hospital, Queensland, Australia) for initiating me into intestinal ultrasound, Dr Mariangella Alloca (IRCCS Hospital San Raffaele and University Milan, Italy), Dr Kim Nylund (National Centre for Ultrasound in Gastroenterology, Haukeland University Hospital, Bergen, Norway) and Dr Odd Helge Gilja (Director, National Centre for Ultrasound in Gastroenterology, Haukeland University Hospital, Bergen, Norway) for training and mentoring me in intestinal ultrasound.

Funding

None.

Author information

Authors and Affiliations

  1. Department of Gastroenterology, Hepatology and Clinical Nutrition, Aster CMI Hospital, Bengaluru, 560 092, India

    Kayal Vizhi Nagarajan & Naresh Bhat

Authors
  1. Kayal Vizhi Nagarajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naresh Bhat
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors made substantial contributions to the design of the work. Kayal Vizhi Nagarajan drafted the work and Naresh Bhat revised it critically for important intellectual content.

Corresponding author

Correspondence to Kayal Vizhi Nagarajan.

Ethics declarations

Competing interests

KVN and NB declare no competing interests.

Ethical approval and consent to participate

Not applicable.

Human ethics

Not applicable.

Consent for publication

Not applicable.

Disclaimer

The authors are solely responsible for the data and the contents of the paper. In no way, the Honorary Editor-in-Chief, Editorial Board Members, the Indian Societry of Gastroenterology or the printer/publishers are responsible for the results/findings and content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nagarajan, K.V., Bhat, N. Intestinal ultrasound in inflammatory bowel disease: New kid on the block. Indian J Gastroenterol 43, 160–171 (2024). https://doi.org/10.1007/s12664-023-01468-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12664-023-01468-z

Keywords

Search

Navigation