Research progress of ultrasonography for evaluation of Crohn’s disease activity_West China Medical Journal

Authors：

WU Yuting ,  ZHUANG Hua , JING Jigang , LUO Yuan , ZHAO Jieying

Department of Ultrasound, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

ZHUANG Hua, Email: annzhuang@yeah.net

Keywords：

Crohn’s disease; Activity; Ultrasonography

DOI：

10.7507/1002-0179.201902012

Video：

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Abstract Full text Figures/Tables Video References Cited by

Crohn’s disease (CD) is one of inflammatory bowel diseases, characterized by lifelong relapsing-remitting clinical course. The choice of treatment protocols is based on the comprehensive evaluation of the disease. And the treatment protocols should be adjusted according to the response to the treatment and the drug tolerance. Repeated assessment of the activity of intestinal inflammation is very necessary. Each of endoscopy, Crohn’s Disease Activity Index, CT, magnetic resonance enterography, and ultrasonography (US) has its own disadvantages. US is widely used in clinical practice because of its no radiation, convenience, low cost, and high degree of patient tolerance. The two-dimensional ultrasound, Doppler ultrasound, elastosonography, and contrast-enhanced ultrasonography each provides some effective parameters for evaluation of CD activity. Some parameters are of high value, such as bowl wall thichness, bowl wall stratification, color Doppler signal, strain ratio, and relative enhancement, etc. The values of some parameters are disputed, such as the blood flow of superior mesenteric artery, time to peak, etc. Some studies combine several ultrasound parameters and calculate their respective weights to obtain an ultrasound scoring method. US, as a valid tool to evaluate CD activity, provides valuable help in solving clinical problems such as evaluation of therapeutic effect, mucosal healing, and postoperative recurrence.

Citation： WU Yuting, ZHUANG Hua, JING Jigang, LUO Yuan, ZHAO Jieying. Research progress of ultrasonography for evaluation of Crohn’s disease activity. West China Medical Journal, 2019, 34(4): 454-460. doi: 10.7507/1002-0179.201902012 Copy

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2.	Gomollón F, Dignass A, Annese V, et al. 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis, 2017, 11(1): 3-25.
3.	Bernstein CN, Eliakim A, Fedail S, et al. World gastroenterology organisation global guidelines inflammatory bowel disease: update August 2015. J Clin Gastroenterol, 2016, 50(10): 803-818.
4.	中华医学会消化病学分会炎症性肠病学组. 建立全国通用的炎症性肠病诊治过程的关键性质量控制指标的共识意见. 中华炎性肠病杂志, 2017, 1(1): 12-19.
5.	Landi B, Anh TN, Cortot A, et al. Endoscopic monitoring of Crohn’s-disease treatment: a prospective, randomized clinical-trial. Gastroenterology, 1992, 102(5): 1647-1653.
6.	Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn’s disease in the SONIC trial. Gut, 2014, 63(1): 88-95.
7.	Lahiff C, Safaie P, Awais A, et al. The Crohn’s disease activity index (CDAI) is similarly elevated in patients with Crohn’s disease and in patients with irritable bowel syndrome. Aliment Pharmacol Ther, 2013, 37(8): 786-794.
8.	Rimola J, Ordás I, Rodríguez S, et al. Imaging indexes of activity and severity for Crohn’s disease: current status and future trends. Abdom Imaging, 2012, 37(6): 958-966.
9.	Qiu Y, Mao R, Chen BL, et al. Systematic review with meta-analysis: magnetic resonance enterography vs. computed tomography enterography for evaluating disease activity in small bowel Crohn’s disease. Aliment Pharmacol Ther, 2014, 40(2): 134-146.
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36.	Byrne MF, Farrell MA, Abass S, et al. Assessment of Crohn’s disease activity by Doppler sonography of the superior mesenteric artery, clinical evaluation and the Crohn’s disease activity index: a prospective study. Clin Radiol, 2001, 56(12): 973-978.
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1. 吴开春, 梁洁, 冉志华, 等. 炎症性肠病诊断与治疗的共识意见(2018 年•北京). 中国实用内科杂志, 2018, 38(9): 796-813.
2. Gomollón F, Dignass A, Annese V, et al. 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis, 2017, 11(1): 3-25.
3. Bernstein CN, Eliakim A, Fedail S, et al. World gastroenterology organisation global guidelines inflammatory bowel disease: update August 2015. J Clin Gastroenterol, 2016, 50(10): 803-818.
4. 中华医学会消化病学分会炎症性肠病学组. 建立全国通用的炎症性肠病诊治过程的关键性质量控制指标的共识意见. 中华炎性肠病杂志, 2017, 1(1): 12-19.
5. Landi B, Anh TN, Cortot A, et al. Endoscopic monitoring of Crohn’s-disease treatment: a prospective, randomized clinical-trial. Gastroenterology, 1992, 102(5): 1647-1653.
6. Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn’s disease in the SONIC trial. Gut, 2014, 63(1): 88-95.
7. Lahiff C, Safaie P, Awais A, et al. The Crohn’s disease activity index (CDAI) is similarly elevated in patients with Crohn’s disease and in patients with irritable bowel syndrome. Aliment Pharmacol Ther, 2013, 37(8): 786-794.
8. Rimola J, Ordás I, Rodríguez S, et al. Imaging indexes of activity and severity for Crohn’s disease: current status and future trends. Abdom Imaging, 2012, 37(6): 958-966.
9. Qiu Y, Mao R, Chen BL, et al. Systematic review with meta-analysis: magnetic resonance enterography vs. computed tomography enterography for evaluating disease activity in small bowel Crohn’s disease. Aliment Pharmacol Ther, 2014, 40(2): 134-146.
10. Vilela EG, Torres HO, Martins FP, et al. Evaluation of inflammatory activity in Crohn’s disease and ulcerative colitis. World J Gastroenterol, 2012, 18(9): 872-881.
11. Magarotto A, Orlando S, Coletta M, et al. Evolving roles of cross-sectional imaging in Crohn’s disease. Dig Liver Dis, 2016, 48(9): 975-983.
12. Eliakim R, Magro F. Imaging techniques in IBD and their role in follow-up and surveillance. Nat Rev Gastroenterol Hepatol, 2014, 11(12): 722-736.
13. Panes J, Bouhnik Y, Reinisch W, et al. Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis, 2013, 7(7): 556-585.
14. 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(8): 1425-1433.
15. 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(5): 1168-1183.
16. Novak KL, Wilson SR. The role of ultrasound in the evaluation of inflammatory bowel disease. Semin Roentgenol, 2013, 48(3): 224-233.
17. Poza-Cordón J, Ripollés-González T. Utility of abdominal ultrasonography in the diagnosis and monitoring of inflammatory bowel disease. Rev Esp Enferm Dig, 2014, 106(6): 395-408.
18. Mosli M, Al Beshir M, Al-Judaibi B, et al. Advances in the diagnosis and management of inflammatory bowel disease: challenges and uncertainties. Saudi J Gastroenterol, 2014, 20(2): 81-101.
19. Chiorean L, Schreiber-Dietrich D, Braden B, et al. Ultrasonographic imaging of inflammatory bowel disease in pediatric patients. World J Gastroenterol, 2015, 21(17): 5231-5241.
20. Allgayer H, Braden B, Dietrich CF. Transabdominal ultrasound in inflammatory bowel disease. Conventional and recently developed techniques--update. Med Ultrason, 2011, 13(4): 302-313.
21. Calabrese E, Zorzi F, Pallone F. Ultrasound in Crohn’s disease. Curr Drug Targets, 2012, 13(10): 1224-1233.
22. Kucharzik T, Wittig BM, Helwig U, et al. Use of intestinal ultrasound to monitor Crohn’s disease activity. Clin Gastroenterol Hepatol, 2017, 15(4): 535-542.
23. Calabrese E, Kucharzik T, Maaser C, et al. Real-time interobserver agreement in bowel ultrasonography for diagnostic assessment in patients with Crohn’s disease: an international multicenter study. Inflamm Bowel Dis, 2018.
24. Bartram C, Herlinger H. Bowel wall thickness as a differentiating feature between ulcerative colitis and Crohn’s disease of the colon. Clin Radiol, 1979, 30(1): 15-19.
25. Fraquelli M, Colli A, Casazza G, et al. Role of US in detection of Crohn disease: meta-analysis. Radiology, 2005, 236(1): 95-101.
26. Na Y, Zhou J, Xiao XM, et al. Assessment of Crohn’s disease activity by doppler sonography. Saudi Med J, 2017, 38(4): 391-395.
27. Martínez MJ, Ripollés T, Paredes JM, et al. Assessment of the extension and the inflammatory activity in Crohn’s disease: comparison of ultrasound and MRI. Abdom Imaging, 2009, 34(2): 141-148.
28. Ripollés T, Martínez MJ, Paredes JM, et al. Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology, 2009, 253(1): 241-248.
29. Migaleddu V, Scanu AM, Quaia E, et al. Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn’s disease. Gastroenterology, 2009, 137(1): 43-52.
30. Haber HP, Busch A, Ziebach R, et al. Bowel wall thickness measured by ultrasound as a marker of Crohn’s disease activity in children. Lancet, 2000, 355(9211): 1239-1240.
31. Rispo A, Bucci L, Pesce G, et al. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm Bowel Dis, 2006, 12(6): 486-490.
32. 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(11): 2001-2010.
33. Karoui S, Nouira K, Serghini M, et al. Assessment of activity of Crohn’s disease by Doppler sonography of superior mesenteric artery flow. J Crohns Colitis, 2010, 4(3): 334-340.
34. Sjekavica I, Barbarić-Babić V, Krznarić Z, et al. Assessment of Crohn’s disease activity by doppler ultrasound of superior mesenteric artery and mural arteries in thickened bowel wall: cross-sectional study. Croat Med J, 2007, 48(6): 822-830.
35. Thomson M, Rao P, Berger L, et al. Graded compression and power Doppler ultrasonography versus endoscopy to assess paediatric Crohn disease activity pre-and posttreatment. J Pediatr Gastroenterol Nutr, 2012, 54(3): 404-408.
36. Byrne MF, Farrell MA, Abass S, et al. Assessment of Crohn’s disease activity by Doppler sonography of the superior mesenteric artery, clinical evaluation and the Crohn’s disease activity index: a prospective study. Clin Radiol, 2001, 56(12): 973-978.
37. Neye H, Voderholzer W, Rickes S, et al. Evaluation of criteria for the activity of Crohn’s disease by power Doppler sonography. Dig Dis, 2004, 22(1): 67-72.
38. Moreno N, Ripollés T, Paredes JM, et al. Usefulness of abdominal ultrasonography in the analysis of endoscopic activity in patients with Crohn’s disease: changes following treatment with immunomodulators and/or anti-TNF antibodies. J Crohns Colitis, 2014, 8(9): 1079-1087.
39. Drews BH, Barth TF, Hänle MM, et al. Comparison of sonographically measured bowel wall vascularity, histology, and disease activity in Crohn’s disease. Eur Radiol, 2009, 19(6): 1379-1386.
40. Rieder F, Fiocchi C. Intestinal fibrosis in IBD--a dynamic, multifactorial process. Nat Rev Gastroenterol Hepatol, 2009, 6(4): 228-235.
41. Giannetti A, Matergi M, Biscontri M, et al. Real-time elastography in Crohn’s disease: feasibility in daily clinical practice. J Ultrasound, 2017, 20(2): 147-155.
42. Dillman JR, Stidham RW, Higgins PD, et al. US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model. Radiology, 2013, 267(3): 757-766.
43. Dillman JR, Stidham RW, Higgins PD, et al. Ultrasound shear wave elastography helps discriminate low-grade from high-grade bowel wall fibrosis in ex vivo human intestinal specimens. J Ultrasound Med, 2014, 33(12): 2115-2123.
44. Baumgart DC, Müller HP, Grittner U, et al. US-based real-time elastography for the detection of fibrotic gut tissue in patients with stricturing Crohn disease. Radiology, 2015, 275(3): 889-899.
45. Fraquelli M, Branchi F, Cribiù FM, et al. The role of ultrasound elasticity imaging in predicting ileal fibrosis in Crohn’s disease patients. Inflamm Bowel Dis, 2015, 21(11): 2605-2612.
46. Havre RF, Leh S, Gilja OH, et al. Strain assessment in surgically resected inflammatory and neoplastic bowel lesions. Ultraschall Med, 2014, 35(2): 149-158.
47. Sconfienza LM, Cavallaro F, Colombi V, et al. In-vivo axial-strain sonoelastography helps distinguish acutely-inflamed from fibrotic terminal ileum strictures in patients with Crohn’s disease: preliminary results. Ultrasound Med Biol, 2016, 42(4): 855-863.
48. Fufezan O, Asavoaie C, Tamas A, et al. Bowel elastography-a pilot study for developing an elastographic scoring system to evaluate disease activity in pediatric Crohn’s disease. Med Ultrason, 2015, 17(4): 422-430.
49. Robotti D, Cammarota T, Debani P, et al. Activity of Crohn disease: value of color-power-Doppler and contrast-enhanced ultrasonography. Abdom Imaging, 2004, 29(6): 648-652.
50. De Pascale A, Garofalo G, Perna M, et al. Contrast-enhanced ultrasonography in Crohn’s disease. Radiol Med, 2006, 111(4): 539-550.
51. Serafin Z, Białecki M, Białecka A, et al. Contrast-enhanced ultrasound for detection of Crohn’s disease activity: systematic review and meta-analysis. J Crohns Colitis, 2016, 10(3): 354-362.
52. Ma X, Li Y, Jia H, et al. Contrast-enhanced ultrasound in the diagnosis of patients suspected of having active Crohn’s disease: meta-analysis. Ultrasound Med Biol, 2015, 41(3): 659-668.
53. Paredes JM, Ripollés T, Cortés X, et al. Contrast-enhanced ultrasonography: usefulness in the assessment of postoperative recurrence of Crohn’s disease. J Crohns Colitis, 2013, 7(3): 192-201.
54. Liu C, Xu XR, Xu HX, et al. Conventional ultrasound and contrast-enhanced ultrasound in evaluating the severity of Crohn’s disease. Int J Clin Exp Med, 2015, 8(1): 123-134.
55. Horjus Talabur Horje CS, Bruijnen R, Roovers L, et al. Contrast enhanced abdominal ultrasound in the assessment of ileal inflammation in crohn’s disease: a comparison with MR enterography. PLoS One, 2015, 10(8): e0136105.
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West China Medical Journal

Research progress of ultrasonography for evaluation of Crohn’s disease activity

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