Systematic review: Defining, diagnosing and monitoring small bowel strictures in Crohn's disease on intestinal ultrasound.
Journal
Alimentary pharmacology & therapeutics
ISSN: 1365-2036
Titre abrégé: Aliment Pharmacol Ther
Pays: England
ID NLM: 8707234
Informations de publication
Date de publication:
04 Mar 2024
04 Mar 2024
Historique:
revised:
29
12
2023
received:
06
12
2023
accepted:
11
02
2024
medline:
4
3
2024
pubmed:
4
3
2024
entrez:
4
3
2024
Statut:
aheadofprint
Résumé
Stricturing Crohn's disease (CD) occurs most commonly in the terminal ileum and poses a clinical problem. Cross-sectional imaging modalities such as intestinal ultrasound (IUS), computed tomography enterography (CTE), and magnetic resonance enterography (MRE) allow for assessment of the entire bowel wall and associated peri-enteric findings. Radiologic definitions of strictures have been developed for CTE and MRE; their reliability and responsiveness are being evaluated in index development programs. A comprehensive assessment strategy for strictures using IUS is needed. To provide a detailed summary of definitions, diagnosis and monitoring of strictures on IUS as well as technical aspects of image acquisition. We searched four databases up to 6 January 2024. Two-stage screening was done in duplicate. We assessed risk of bias using QUADAS-2. There were 56 studies eligible for inclusion. Definitions for strictures on IUS are heterogeneous, but the overall accuracy for diagnosis of strictures is high. The capability of IUS for characterising inflammation versus fibrosis in strictures is not accurate enough to be used in clinical practice or trials. We summarise definitions for improvement of strictures on IUS, and discuss parameters for image acquisition and standardisation. This systematic review is the first step for a structured program to develop a stricture IUS index for CD.
Sections du résumé
BACKGROUND
BACKGROUND
Stricturing Crohn's disease (CD) occurs most commonly in the terminal ileum and poses a clinical problem. Cross-sectional imaging modalities such as intestinal ultrasound (IUS), computed tomography enterography (CTE), and magnetic resonance enterography (MRE) allow for assessment of the entire bowel wall and associated peri-enteric findings. Radiologic definitions of strictures have been developed for CTE and MRE; their reliability and responsiveness are being evaluated in index development programs. A comprehensive assessment strategy for strictures using IUS is needed.
AIMS
OBJECTIVE
To provide a detailed summary of definitions, diagnosis and monitoring of strictures on IUS as well as technical aspects of image acquisition.
METHODS
METHODS
We searched four databases up to 6 January 2024. Two-stage screening was done in duplicate. We assessed risk of bias using QUADAS-2.
RESULTS
RESULTS
There were 56 studies eligible for inclusion. Definitions for strictures on IUS are heterogeneous, but the overall accuracy for diagnosis of strictures is high. The capability of IUS for characterising inflammation versus fibrosis in strictures is not accurate enough to be used in clinical practice or trials. We summarise definitions for improvement of strictures on IUS, and discuss parameters for image acquisition and standardisation.
CONCLUSIONS
CONCLUSIONS
This systematic review is the first step for a structured program to develop a stricture IUS index for CD.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Authors. Alimentary Pharmacology & Therapeutics published by John Wiley & Sons Ltd.
Références
Thia KT, Sandborn WJ, Harmsen WS, Zinsmeister AR, Loftus EV Jr. Risk factors associated with progression to intestinal complications of Crohn's disease in a population-based cohort. Gastroenterology. 2010;139:1147-1155.
Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 2006;55:749-753.
Lu C, Merrill C, Medellin A, Novak K, Wilson SR. Bowel ultrasound state of the art: grayscale and doppler ultrasound, contrast enhancement, and elastography in Crohn disease. J Ultrasound Med. 2019;38:271-288.
Wilkens R, Novak KL, Maaser C, Panaccione R, Kucharzik T. Relevance of monitoring transmural disease activity in patients with Crohn's disease: current status and future perspectives. Therap Adv Gastroenterol. 2021;14:1-18.
Gordon IO, Bettenworth D, Bokemeyer A, Srivastava A, Rosty C, de Hertogh G, et al. International consensus to standardise histopathological scoring for small bowel strictures in Crohn's disease. Gut. 2021;71:479-486.
Allocca M, Fiorino G, Bonifacio C, Furfaro F, Gilardi D, Argollo M, et al. 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;12:1280-1287.
Allocca M, Furfaro F, Fiorino G, Peyrin-Biroulet L, Danese S. Point-of-care ultrasound in inflammatory bowel disease. J Crohns Colitis. 2021;15:143-151.
Rieder F, Bettenworth D, Ma C, Parker CE, Williamson LA, Nelson SA, et al. An expert consensus to standardise definitions, diagnosis and treatment targets for anti-fibrotic stricture therapies in Crohn's disease. Aliment Pharmacol Ther. 2018;48:347-357.
Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page M, et al., editors. Cochrane handbook for systematic reviews of interventions version 6.2. (updated February 2021) 2021.
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffman TC, Mulrow CD, et al. The PRISMA statement: an updated guideline for reporting systematic reviews. BMJ (Clinical Research Ed). 2020;2021:372.
Calabrese E, Petruzziello C, Onali S, Condino G, Zorzi F, Pallone F, et al. Severity of postoperative recurrence in Crohn's disease: correlation between endoscopic and sonographic findings. Inflamm Bowel Dis. 2009;15:1635-1642.
Livne M, Amitai MM, Klang E, Ben Horin S, Ungar B, Levartovsky A, et al. Qualitative sonographic assessment of transmural ileal inflammation in Crohn's disease: a comparison with MRI activity score. Eur J Gastroenterol Hepatol. 2020;33:961-966.
Pallotta N, Barberani F, Hassan N-A, Guagnozzi D, Vincoli G, Corazziari E. Effect of infliximab on small bowel stenoses in patients with Crohn's disease. World J Gastroenterol. 2008;14:1885-1890.
Pallotta N, Vincoli G, Montesani C, Chirletti P, Pronio A, Caronna R, et al. Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in crohn's disease: a prospective comparative study versus intraoperative findings. Inflamm Bowel Dis. 2012;18:74-84.
Pallotta N, Vincoli G, Candeloro L, Calarco R. In Crohn's disease (CD) patients small bowel prestenotic dilatation is not related to severity degree of stricture. Gastroenterology. 2014;146:S-203.
Calabrese E, La Seta F, Buccellato A, Virdone R, Pallotta N, Corazziari E, et al. Crohn's disease: a comparative prospective study of transabdominal ultrasonography, small intestine contrast ultrasonography, and small bowel enema. Inflamm Bowel Dis. 2005;11:139-145.
Calabrese E, Kucharzik T, Maaser C, Maconi G, Strobel D, Wilson SR, 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;24:2001-2006.
Ding S-S, Fang Y, Wan J, Zhao CK, Xiang LH, Liu H, et al. Usefulness of strain elastography, ARFI imaging, and point shear wave elastography for the assessment of Crohn disease strictures. J Ultrasound Med. 2019;38:2861-2870.
Fraquelli M, Branchi F, Cribiù FM, Orlando S, Casazza G, Magarotto A, et al. The role of ultrasound elasticity imaging in predicting ileal fibrosis in Crohn's disease patients. Inflamm Bowel Dis. 2015;21:2605-2612.
Gaitini D, Kreitenberg AJ, Fischer D, Maza I, Chowers Y. Color-coded duplex sonography compared to multidetector computed tomography for the diagnosis of crohn disease relapse and complications. J Ultrasound Med. 2011;30:1691-1699.
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;44:112-117.
Horjus Talabur Horje CS, Bruijnen R, Roovers L, Groenen MJM, Joosten FBM, Wahab PJ. Contrast enhanced abdominal ultrasound in the assessment of ileal inflammation in Crohn's disease: a comparison with MR Enterography. PLoS ONE. 2015;10:e0136105.
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.
Kratzer W, von Tirpitz C, Mason R, Reinshagen M, Adler G, Möller P, et al. Contrast-enhanced power Doppler sonography of the intestinal wall in the differentiation of hypervascularized and hypovascularized intestinal obstructions in patients with Crohn's disease. J Ultrasound Med. 2002;21:149-157.
Lenze F, Wessling J, Bremer J, Ullerich H, Spieker T, Weckesser M, et al. Detection and differentiation of inflammatory versus fibromatous Crohn's disease strictures: prospective comparison of 18F-FDG-PET/CT, MR-enteroclysis, and transabdominal ultrasound versus endoscopic/histologic evaluation. Inflamm Bowel Dis. 2012;18:2252-2260.
Lu C, Gui X, Chen W, Fung T, Novak K, Wilson SR. Ultrasound shear wave elastography and contrast enhancement: effective biomarkers in Crohn's disease strictures. Inflamm Bowel Dis. 2017;23:421-430.
Ma C, Huang P-L, Kang N, Zhang J, Xiao M, Zhang JY, et al. The clinical value of multimodal ultrasound for the evaluation of disease activity and complications in inflammatory bowel disease. Annal Palliat Med. 2020;9:4146-4155.
Maconi G, Bollani S, Bianchi PG. Ultrasonographic detection of intestinal complications in Crohn's disease. Dig Dis Sci. 1996;41:1643-1648.
Maconi G, Carsana L, Fociani P, Sampietro GM, Ardizzone S, Cristaldi M, et al. Small bowel stenosis in Crohn's disease: clinical, biochemical and ultrasonographic evaluation of histological features. Aliment Pharmacol Ther. 2003;18:749-756.
Neye H, Ensberg D, Rauh P, Peitz U, Mönkemüller K, Treiber G, et al. Impact of high-resolution transabdominal ultrasound in the diagnosis of complications of Crohn's disease. Scand J Gastroenterol. 2010;45:690-695.
Onali S, Calabrese E, Petruzziello C, Zorzi F, Sica G, Fiori R, et al. Small intestine contrast ultrasonography vs computed tomography enteroclysis for assessing ileal Crohn's disease. World J Gastroenterol. 2012;18:6088-6095.
Parente F, Maconi G, Bollani S, Anderloni A, Sampietro G, Cristaldi M, 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;50:490-495.
Quaia E, Gennari AG, Cova MA, van Beek EJR. Differentiation of inflammatory from fibrotic ileal strictures among patients with Crohn's disease based on visual analysis: feasibility study combining conventional B-mode ultrasound, contrast-enhanced ultrasound and strain elastography. Ultrasound Med Biol. 2018;44:762-770.
Quaia E, Gennari AG, van Beek EJR. Differentiation of inflammatory from fibrotic ileal strictures among patients with Crohn's disease through analysis of time-intensity curves obtained after microbubble contrast agent injection. Ultrasound Med Biol. 2017;43:1171-1178.
Sconfienza LM, Cavallaro F, Colombi V, Pastorelli L, Tontini G, Pescatori L, 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;42:855-863.
Serra C, Rizzello F, Pratico' C, Felicani C, Fiorini E, Brugnera R, et al. Real-time elastography for the detection of fibrotic and inflammatory tissue in patients with stricturing Crohn's disease. J Ultrasound. 2017;20:273-284.
Schulberg JD, Wright EK, Holt BA, Hamilton AL, Sutherland TR, Ross AL, et al. Intensive drug therapy versus standard drug therapy for symptomatic intestinal Crohn's disease strictures (STRIDENT): an open-label, single-centre, randomised controlled trial. Lancet Gastroenterol Hepatol. 2022;7:318-331.
Wilkens R, Liao DH, Gregersen H, et al. Biomechanical properties of strictures in Crohn's disease: can dynamic contrast-enhanced ultrasonography and magnetic resonance Enterography predict stiffness? Diagnostics (Basel, Switzerland). 2022;12:1370.
Allocca M, Dal Buono A, D'Alessio S, Spaggiari P, Garlatti V, Spinelli A, et al. Relationships between intestinal ultrasound parameters and histopathologic findings in a prospective cohort of patients with Crohn's disease undergoing surgery. J Ultrasound Medi. 2023;9999:1-12.
Takeuchi K, Inokuchi T, Takahara M, Ohmori M, Yasutomi E, Oka S, et al. Usefulness of intestinal ultrasound to detect small intestinal stenosis in patients with Crohn's disease. J Ultrasound Med. 2023;42:373-383.
De Cristofaro E, Montesano L, Lolli E, et al. Echopattern parameter as an aid to profile Crohn's disease patients. Dig Liver Dis. 2023;55:1652-1657.
Fraquelli M, Sarno A, Girelli C, Laudi C, Buscarini E, Villa C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn's disease. Dig Liver Dis. 2008;40:860-866.
Matsumoto H, Hata J, Yo S, Sasahira M, Misawa H, Oosawa M, et al. Serial changes in intestinal stenotic stiffness in patients with Crohn's disease treated with biologics: a pilot study using ultrasound shear wave elastography. Turk J Gastroenterol. 2023;34:1006-1013.
Nylund K, Jirik R, Mezl M, Leh S, Hausken T, Pfeffer F, et al. Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn's disease. Ultrasound Med Biol. 2013;39:1197-1206.
Calabrese E, Zorzi F, Onali S, Stasi E, Fiori R, Prencipe 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;11:950-955.
Carter D, Eliakim R. Feasibility of bedside bowel ultrasound performed by a gastroenterologist for detection and follow-up of inflammatory bowel disease. Isr Med Assoc J. 2017;19:139-142.
Ripolles T, Rausell N, Paredes JM, Grau E, Martinez MJ, Vizuete J. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn's disease: a comparison with surgical histopathology analysis. J Crohns Colitis. 2013;7:120-128.
Ripollés T, Paredes JM, Martínez-Pérez MJ, Rimola J, Jauregui-Amezaga A, Bouzas R, 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;22:2465-2473.
Schirin-Sokhan R, Winograd R, Tischendorf S, Wasmuth HE, Streetz K, Tacke F, et al. Assessment of inflammatory and fibrotic stenoses in patients with Crohn's disease using contrast-enhanced ultrasound and computerized algorithm: a pilot study. Digestion. 2011;83:263-268.
Sey MSL, Gregor J, Chande N, Ponich T, Bhaduri M, Lum A, et al. Transcutaneous bowel sonography for inflammatory bowel disease is sensitive and specific when performed in a nonexpert low-volume north American center. J Ultrasound Med. 2013;32:1413-1417.
Yuksel I, Kilincalp S, Coskun Y, Akinci H, Hamamci M, Alkan A. Diagnostic accuracy of intestinal ultrasound and magnetic resonance enterography for the detection of endoscopy-based disease activity in ileocolonic Crohn's disease. Eur J Gastroenterol Hepatol. 2019;31:809-816.
Chen Y-J, Mao R, Li X-H, Cao QH, Chen ZH, Liu BX, et al. Real-time shear wave ultrasound elastography differentiates fibrotic from inflammatory strictures in patients with Crohn's disease. Inflamm Bowel Dis. 2018;24:2183-2190.
Baumgart DC, Müller HP, Grittner U, Metzke D, Fischer A, Guckelberger O, et al. US-based real-time elastography for the detection of fibrotic gut tissue in patients with Stricturing Crohn disease. Radiology. 2015;275:889-899.
Chatu S, Pilcher J, Saxena SK, Fry DH, Pollok RCG. Diagnostic accuracy of small intestine ultrasonography using an oral contrast agent in Crohn's disease: comparative study from the UK. Clin Radiol. 2012;67:553-559.
Orlova L, Samsonova T, Khali I, Shapina M. Strain elastography and differential diagnosis of inflammatory and fibrotic strictures in Crohn's disease. United Eur Gastroenterol J. 2017;5:A161-A836.
Bhatnagar G, Rodriguez-Justo M, Higginson A, Bassett P, Windsor A, Cohen R, et al. Inflammation and fibrosis in Crohn's disease: location-matched histological correlation of small bowel ultrasound features. Abdom Radiol. 2021;46:144-155.
Kumar S, Hakim A, Alexakis C, Chhaya V, Tzias D, Pilcher J, et al. Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn's disease: correlation with intraoperative findings and magnetic resonance enterography. J Gastroenterol Hepatol. 2015;30:86-91.
Bezzio C, Monteleone M, Friedman A, Furfaro F, Fociani P, Sampietro GM, et al. P158 real-time strain elastography accurately differentiates between inflammatory and fibrotic strictures in Crohn's disease. J Crohn's Colitis. 2013;7:S72.
Stidham RW, Xu J, Johnson LA, Kim K, Moons DS, McKenna BJ, et al. Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn's disease. Gastroenterology. 2011;141:819-826.e1.
Stidham R, Dillman J, Rubin JM. Shear wave velocity measurement in bowel wall using ARFI ultrasound for prediction of response to medical therapy in Crohn's disease. Inflamm Bowel Dis. 2013;19:S87-S88.
Stidham R, Dillman J, Rubin J. Using stiffness imaging of the intestine to predict response to medical therapy in obstructive Crohn's disease. Inflamm Bowel Dis. 2016;22:S44-S45.
Zhang M, Xiao E, Liu M, Mei X, Dai Y. Retrospective cohort study of shear-wave elastography and computed tomography enterography in Crohn's disease. Diagnostics (Basel). 2023;13:1980.
Pallotta N, Vincoli G, Montesani C, Chirletti P, Pronio A, Caronna R, et al. Small intestine contrast ultrasonography (SICUS) in the preoperative assessment of patients with Crohn's disease of the small bowel. Gastroenterology. 2011;140:S689.
Quaia E, De Paoli L, Stocca T, Cabibbo B, Casagrande F, Cova MA. 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. 2012;38:1324-1332.
Wilkens R, Hagemann-Madsen RH, Peters DA, Nielsen AH, Nørager CB, Glerup H, et al. Validity of contrast-enhanced ultrasonography and dynamic contrast-enhanced MR Enterography in the assessment of transmural activity and fibrosis in Crohn's disease. J Crohns Colitis. 2018;12:48-56.
Rispo A, Imperatore N, Testa A, Mainenti P, de Palma GD, Luglio G, et al. Bowel damage in Crohn's disease: direct comparison of ultrasonography-based and magnetic resonance-based Lemann index. Inflamm Bowel Dis. 2017;23:143-151.
Calabrese E, Maaser C, Zorzi F, Kannengiesser K, Hanauer SB, Bruining DH, 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;22:1168-1183.
Kirshner B, Guyatt G. A methodological framework for assessing health indices. J Chronic Dis. 1985;38:27-36.
Kucharzik T, Tielbeek J, Carter D, Taylor SA, Tolan D, Wilkens R, et al. ECCO-ESGAR topical review on optimizing reporting for cross-sectional imaging in inflammatory bowel disease. J Crohns Colitis. 2022;16:523-543.
Novak KL, Nylund K, Maaser C, Petersen F, Kucharzik T, Lu 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;15:609-616.
Bruining DH, Zimmermann EM, Loftus EV Jr, et al. Consensus recommendations for evaluation, interpretation, and utilization of computed tomography and magnetic resonance enterography in patients with small bowel Crohn's disease. Radiology. 2018;286:776-799.
Bettenworth D, Bokemeyer A, Baker M, Mao R, Parker CE, Nguyen T, et al. Assessment of Crohn's disease-associated small bowel strictures and fibrosis on cross-sectional imaging: a systematic review. Gut. 2019;68:1115-1126.
Dal Buono A, Faita F, Peyrin-Biroulet L, Danese S, Allocca M. Ultrasound elastography in inflammatory bowel diseases: a systematic review of accuracy compared with histopathological assessment. J Crohn's Colitis. 2022;16:1637-1646.
Xu C, Jiang W, Wang L, Mao X, Ye Z, Zhang H. Intestinal ultrasound for differentiating fibrotic or inflammatory stenosis in Crohn's disease: a systematic review and meta-analysis. J Crohn's Colitis. 2022;16:1493-1504.
Bhatnagar G, Quinn L, Higginson A, et al. Observer agreement for small bowel ultrasound in Crohn's disease: results from the METRIC trial. Abdom Radiol. 2020;45:3036-3045.