The application and prospect of intestinal ultrasound in patients with Crohn’s disease_West China Medical Journal

Authors：

MU Jingxi ,  ZHANG Hu

Department of Gastroenterology & Center of Inflammatory Bowel Disease, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

ZHANG Hu, Email: zhanghu@scu.edu.cn

Keywords：

Crohn’s disease; Intestinal ultrasound; Application prospect

DOI：

10.7507/1002-0179.201812156

Video：

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Crohn’s disease (CD) is a chronic, remitting and segmental inflammatory disease of the gastrointestinal tract, radiological examinations play critical roles in the diagnosis of CD. The common radiological examinations include ultrasound examinations of intestine, computed tomography enterography (CTE), and magnetic resonance enterography (MRE) in clinic. The application of CTE and MRE is limited because of radiation exposure or higher costs. The ultrasound examinations of intestine including conventional intestinal ultrasound, ultrasonic elastography, and contrast-enhanced ultrasound have been studied because of the advantages of non-invasiveness and convenience. The accuracy of the intestinal ultrasound has been already partially validated in assisting diagnosis and evaluating the disease activity and location in CD patients. This review aims at summarizing the diagnostic potency and prospect of the application of ultrasound examinations of intestine in CD patients.

Citation： MU Jingxi, ZHANG Hu. The application and prospect of intestinal ultrasound in patients with Crohn’s disease. West China Medical Journal, 2019, 34(4): 448-453. doi: 10.7507/1002-0179.201812156 Copy

1.	Cosnes J, Gower Rousseau C, Seksik P, et al. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology, 2011, 140(6): 1785-1794.
2.	Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology, 2017, 152(2): 313-321.
3.	Aloi M, Di Nardo G, Romano G, et al. Magnetic resonance enterography, small-intestine contrast US, and capsule endoscopy to evaluate the small bowel in pediatric Crohn’s disease: a prospective, blinded, comparison study. Gastrointest Endosc, 2015, 81(2): 420-427.
4.	Solberg IC, Vatn MH, Høie O, et al. Clinical course in Crohn’s disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol, 2007, 5(12): 1430-1438.
5.	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, 2016, 11(1): 3-25.
6.	Maconi G, Nylund K, Ripolles T, et al. EFSUMB recommendations and clinical guidelines for intestinal ultrasound (GIUS) in inflammatory bowel diseases. Ultraschall Med, 2018, 39(3): 304-317.
7.	Lu C, Merrill C, Medellin A, et al. Bowel ultrasound state of the art: grayscale and doppler ultrasound, contrast enhancement, and elastography in crohn disease. J Ultrasound Med, 2019, 38(2): 271-288.
8.	Fraquelli M, Colli A, Casazza G, et al. Role of US in detection of Crohn disease: meta-analysis. Radiology, 2005, 236(1): 95-101.
9.	Nylund K, Maconi G, Hollerweger A, et al. EFSUMB recommendations and guidelines for gastrointestinal ultrasound. Ultraschall Med, 2017, 38(3): e1-e15.
10.	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(5): 991-998.
11.	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.
12.	Colli A, Fraquelli M, Casazza G, et al. The architecture of diagnostic research: from bench to bedside--research guidelines using liver stiffness as an example. Hepatology, 2014, 60(1): 408-418.
13.	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(1): 26-33.
14.	Parente F, Greco S, Molteni M, 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, 2004, 53(11): 1652-1657.
15.	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(2): 125-145.
16.	Horsthuis K, Bipat S, Bennink RJ, et al. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology, 2008, 247(1): 64-79.
17.	Maconi G, Bolzoni E, Giussani A, et al. Accuracy and cost of diagnostic strategies for patients with suspected Crohn’s disease. J Crohns Colitis, 2014, 8(12): 1684-1692.
18.	Parente F, Greco S, Molteni M, et al. Role of early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel. Aliment Pharmacol Ther, 2003, 18(10): 1009-1016.
19.	Kucharzik T, Maaser C. Intestinal ultrasound and management of small bowel Crohn’s disease. Therap Adv Gastroenterol, 2018, 11: 1756284818771367.
20.	Calabrese E, Zorzi F, Onali S, et al. Accuracy of small-intestine contrast ultrasonography, compared with computed tomography enteroclysis, in characterizing lesions in patients with Crohn’s disease. Clin Gastroenterol Hepatol, 2013, 11(8): 950-955.
21.	Gasche C, Moser G, Turetschek K, et al. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut, 1999, 44(1): 112-117.
22.	Maconi G, Bollani S, Bianchi PG. Ultrasonographic detection of intestinal complications in Crohn’s disease. Dig Dis Sci, 1996, 41(8): 1643-1648.
23.	Parente F, Maconi G, Bollani S, et al. 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(4): 490-495.
24.	Biancone L, Calabrese E, Petruzziello C, et al. Wireless capsule endoscopy and small intestine contrast ultrasonography in recurrence of Crohn’s disease. Inflamm Bowel Dis, 2007, 13(10): 1256-1265.
25.	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(2): 139-145.
26.	Thompson JS, Iyer KR, Dibaise JK, et al. Short bowel syndrome and Crohn’s disease. J Gastrointest Surg, 2003, 7(8): 1069-1072.
27.	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.
28.	Ripollés T, Paredes JM, Martinez-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(10): 2465-2473.
29.	Sigrist RMS, Liau J, Kaffas AE, et al. Ultrasound elastography: review of techniques and clinical applications. Theranostics, 2017, 7(5): 1303-1329.
30.	Pecere S, Holleran G, Ainora ME, et al. Usefulness of contrast-enhanced ultrasound (CEUS) in inflammatory bowel disease (IBD). Dig Liver Dis, 2018, 50(8): 761-767.
31.	Pita I, Magro F. Advanced imaging techniques for small bowel Crohn’s disease: what does the future hold?. Therap Adv Gastroenterol, 2018, 11: 1756283X18757185.
32.	Pescatori LC, Mauri G, Savarino E, et al. Bowel sonoelastography in patients with Crohn’s disease: a systematic review. Ultrasound Med Biol, 2018, 44(2): 297-302.
33.	Chen YJ, Mao R, Md XL, et al. Real-time shear wave ultrasound elastography differentiates fibrotic from inflammatory strictures in patients with Crohn’s disease. Inflamm Bowel Dis, 2018, 24(10): 2183-2190.
34.	Lu C, Gui X, Chen W, et al. Ultrasound shear wave elastography and contrast enhancement: effective biomarkers in Crohn’s disease strictures. Inflamm Bowel Dis, 2017, 23(3): 421-430.
35.	Serafin Z, Bialecki M, Bialecka 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.
36.	Migaleddu V, Quaia E, Scanu D, et al. Inflammatory activity in Crohn’s disease: CE-US. Abdom Imaging, 2011, 36(2): 142-148.
37.	Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J roentgenol, 2016, 206(1): 64-73.
38.	Saevik F, Nylund K, Hausken T, et al. Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn’s disease. Inflamm Bowel Dis, 2014, 20(11): 2029-2037.
39.	Quaia E, Sozzi M, Angileri R, et al. Time-intensity curves obtained after microbubble injection can be used to differentiate responders from nonresponders among patients with clinically active crohn disease after 6 weeks of pharmacologic treatment. Radiology, 2016, 281(2): 606-616.
40.	Ripollés T, Martínez-Pérez MJ, Paredes JM, et al. Contrast-enhanced ultrasound in the differentiation between phlegmon and abscess in Crohn’s disease and other abdominal conditions. Eur J Radiol, 2013, 82(10): e525-e531.
41.	Piscaglia F, Nolsøe C, Dietrich CF, et al. The EFSUMB guidelines and recommendations on the clinical practice of contrast enhanced ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med, 2012, 33(1): 33-59.
42.	Ripollés T, Martinez MJ, Paredes JM, et al. Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology, 2009, 253(1): 241-248.
43.	Maconi G, Parente F, Bollani S, et al. Factors affecting splanchnic haemodynamics in Crohn’s disease: a prospective controlled study using Doppler ultrasound. Gut, 1998, 43(5): 645-650.
44.	Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J Roentgenol, 2016, 206(1): 64-73.
45.	Esteban JM, Maldonado L, Sanchiz V, et al. Activity of Crohn’s disease assessed by colour Doppler ultrasound analysis of the affected loops. Eur Radiol, 2001, 11(8): 1423-1428.
46.	Limberg B. Diagnosis of chronic inflammatory bowel disease by ultrasonography. Z Gastroenterol, 1999, 37(6): 495-508.
47.	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(5): 585-593.
48.	Calabrese E, Zorzi F, Zuzzi S, et al. Development of a numerical index quantitating small bowel damage as detected by ultrasonography in Crohn’s disease. J Crohns Colitis, 2012, 6(8): 852-860.
49.	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.
50.	Sturm A, Maaser C, Calabrese E, et al. ECCO-ESGAR guideline for diagnostic assessment in IBD Part 2: IBD scores and general principles and technical aspects. J Crohns Colitis, 2018, 13(3): 273-284.

1. Cosnes J, Gower Rousseau C, Seksik P, et al. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology, 2011, 140(6): 1785-1794.
2. Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology, 2017, 152(2): 313-321.
3. Aloi M, Di Nardo G, Romano G, et al. Magnetic resonance enterography, small-intestine contrast US, and capsule endoscopy to evaluate the small bowel in pediatric Crohn’s disease: a prospective, blinded, comparison study. Gastrointest Endosc, 2015, 81(2): 420-427.
4. Solberg IC, Vatn MH, Høie O, et al. Clinical course in Crohn’s disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol, 2007, 5(12): 1430-1438.
5. 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, 2016, 11(1): 3-25.
6. Maconi G, Nylund K, Ripolles T, et al. EFSUMB recommendations and clinical guidelines for intestinal ultrasound (GIUS) in inflammatory bowel diseases. Ultraschall Med, 2018, 39(3): 304-317.
7. Lu C, Merrill C, Medellin A, et al. Bowel ultrasound state of the art: grayscale and doppler ultrasound, contrast enhancement, and elastography in crohn disease. J Ultrasound Med, 2019, 38(2): 271-288.
8. Fraquelli M, Colli A, Casazza G, et al. Role of US in detection of Crohn disease: meta-analysis. Radiology, 2005, 236(1): 95-101.
9. Nylund K, Maconi G, Hollerweger A, et al. EFSUMB recommendations and guidelines for gastrointestinal ultrasound. Ultraschall Med, 2017, 38(3): e1-e15.
10. 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(5): 991-998.
11. 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.
12. Colli A, Fraquelli M, Casazza G, et al. The architecture of diagnostic research: from bench to bedside--research guidelines using liver stiffness as an example. Hepatology, 2014, 60(1): 408-418.
13. 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(1): 26-33.
14. Parente F, Greco S, Molteni M, 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, 2004, 53(11): 1652-1657.
15. 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(2): 125-145.
16. Horsthuis K, Bipat S, Bennink RJ, et al. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology, 2008, 247(1): 64-79.
17. Maconi G, Bolzoni E, Giussani A, et al. Accuracy and cost of diagnostic strategies for patients with suspected Crohn’s disease. J Crohns Colitis, 2014, 8(12): 1684-1692.
18. Parente F, Greco S, Molteni M, et al. Role of early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel. Aliment Pharmacol Ther, 2003, 18(10): 1009-1016.
19. Kucharzik T, Maaser C. Intestinal ultrasound and management of small bowel Crohn’s disease. Therap Adv Gastroenterol, 2018, 11: 1756284818771367.
20. Calabrese E, Zorzi F, Onali S, et al. Accuracy of small-intestine contrast ultrasonography, compared with computed tomography enteroclysis, in characterizing lesions in patients with Crohn’s disease. Clin Gastroenterol Hepatol, 2013, 11(8): 950-955.
21. Gasche C, Moser G, Turetschek K, et al. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut, 1999, 44(1): 112-117.
22. Maconi G, Bollani S, Bianchi PG. Ultrasonographic detection of intestinal complications in Crohn’s disease. Dig Dis Sci, 1996, 41(8): 1643-1648.
23. Parente F, Maconi G, Bollani S, et al. 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(4): 490-495.
24. Biancone L, Calabrese E, Petruzziello C, et al. Wireless capsule endoscopy and small intestine contrast ultrasonography in recurrence of Crohn’s disease. Inflamm Bowel Dis, 2007, 13(10): 1256-1265.
25. 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(2): 139-145.
26. Thompson JS, Iyer KR, Dibaise JK, et al. Short bowel syndrome and Crohn’s disease. J Gastrointest Surg, 2003, 7(8): 1069-1072.
27. 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.
28. Ripollés T, Paredes JM, Martinez-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(10): 2465-2473.
29. Sigrist RMS, Liau J, Kaffas AE, et al. Ultrasound elastography: review of techniques and clinical applications. Theranostics, 2017, 7(5): 1303-1329.
30. Pecere S, Holleran G, Ainora ME, et al. Usefulness of contrast-enhanced ultrasound (CEUS) in inflammatory bowel disease (IBD). Dig Liver Dis, 2018, 50(8): 761-767.
31. Pita I, Magro F. Advanced imaging techniques for small bowel Crohn’s disease: what does the future hold?. Therap Adv Gastroenterol, 2018, 11: 1756283X18757185.
32. Pescatori LC, Mauri G, Savarino E, et al. Bowel sonoelastography in patients with Crohn’s disease: a systematic review. Ultrasound Med Biol, 2018, 44(2): 297-302.
33. Chen YJ, Mao R, Md XL, et al. Real-time shear wave ultrasound elastography differentiates fibrotic from inflammatory strictures in patients with Crohn’s disease. Inflamm Bowel Dis, 2018, 24(10): 2183-2190.
34. Lu C, Gui X, Chen W, et al. Ultrasound shear wave elastography and contrast enhancement: effective biomarkers in Crohn’s disease strictures. Inflamm Bowel Dis, 2017, 23(3): 421-430.
35. Serafin Z, Bialecki M, Bialecka 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.
36. Migaleddu V, Quaia E, Scanu D, et al. Inflammatory activity in Crohn’s disease: CE-US. Abdom Imaging, 2011, 36(2): 142-148.
37. Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J roentgenol, 2016, 206(1): 64-73.
38. Saevik F, Nylund K, Hausken T, et al. Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn’s disease. Inflamm Bowel Dis, 2014, 20(11): 2029-2037.
39. Quaia E, Sozzi M, Angileri R, et al. Time-intensity curves obtained after microbubble injection can be used to differentiate responders from nonresponders among patients with clinically active crohn disease after 6 weeks of pharmacologic treatment. Radiology, 2016, 281(2): 606-616.
40. Ripollés T, Martínez-Pérez MJ, Paredes JM, et al. Contrast-enhanced ultrasound in the differentiation between phlegmon and abscess in Crohn’s disease and other abdominal conditions. Eur J Radiol, 2013, 82(10): e525-e531.
41. Piscaglia F, Nolsøe C, Dietrich CF, et al. The EFSUMB guidelines and recommendations on the clinical practice of contrast enhanced ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med, 2012, 33(1): 33-59.
42. Ripollés T, Martinez MJ, Paredes JM, et al. Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology, 2009, 253(1): 241-248.
43. Maconi G, Parente F, Bollani S, et al. Factors affecting splanchnic haemodynamics in Crohn’s disease: a prospective controlled study using Doppler ultrasound. Gut, 1998, 43(5): 645-650.
44. Medellin-Kowalewski A, Wilkens R, Wilson A, et al. Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. AJR Am J Roentgenol, 2016, 206(1): 64-73.
45. Esteban JM, Maldonado L, Sanchiz V, et al. Activity of Crohn’s disease assessed by colour Doppler ultrasound analysis of the affected loops. Eur Radiol, 2001, 11(8): 1423-1428.
46. Limberg B. Diagnosis of chronic inflammatory bowel disease by ultrasonography. Z Gastroenterol, 1999, 37(6): 495-508.
47. 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(5): 585-593.
48. Calabrese E, Zorzi F, Zuzzi S, et al. Development of a numerical index quantitating small bowel damage as detected by ultrasonography in Crohn’s disease. J Crohns Colitis, 2012, 6(8): 852-860.
49. 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.
50. Sturm A, Maaser C, Calabrese E, et al. ECCO-ESGAR guideline for diagnostic assessment in IBD Part 2: IBD scores and general principles and technical aspects. J Crohns Colitis, 2018, 13(3): 273-284.

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