Role of Ultrasound Elastography in the Detection of Fibrotic Bowel Strictures in Patients with Crohn’s Disease: Systematic Review and Meta-Analysis

Abstract

Purpose To perform a systematic review with meta-analysis to assess whether ultrasound elastography can have a diagnostic role in detecting fibrotic bowel strictures in patients with Crohn’s disease.

Materials and Methods MEDLINE via the PubMed, Ovid Embase, Scopus and Cochrane Library databases, and abstracts of international conference proceedings were searched up to March 31, 2018. Studies were included if they assessed the performance of abdominal ultrasound elastography in detecting fibrotic bowel strictures in patients with Crohn’s disease using histology or the need for surgery after medical treatment as a reference standard. The quality of the studies was assessed using Quality Assessment of Diagnostic Accuracy Studies.

Results 6 studies including a total of 217 patients with Crohn’s disease and 231 bowel segments, of which 76 were bowel segments with fibrotic stricture, were selected. Three studies used strain ratio and three studies used strain value as parameters of bowel stiffness. Both the pooled standardized mean strain ratio and the pooled standardized mean strain value were higher in bowel segments with fibrotic strictures than in those without fibrotic strictures with a standardized mean difference of 0.85 (95 % confidence level [CI]: 0 to 1.71; p = 0.05) and 1.0 (95 % CI: –0.11 to 2.10; p = 0.08), respectively. There was a high heterogeneity between studies. All studies were at “high risk” or “unclear risk” of bias.

Conclusion Ultrasound elastography could be able to detect fibrotic bowel strictures in patients with Crohn’s disease. Well-designed high quality diagnostic studies with a large sample size are needed.

Zusammenfassung

Ziel Durchführung eines systematischen Reviews mit Meta-Analyse, um zu beurteilen, ob Ultraschall-Elastografie eine diagnostische Rolle beim Erkennen fibrotischer Darmstrikturen bei Patienten mit Morbus Crohn spielen kann.

Material und Methoden Es wurden MEDLINE über die Datenbanken PubMed, Ovid Embase, Scopus und Cochrane Library sowie die Abstracts aus den Tagungsbänden internationaler Konferenzen bis zum 31. März 2018 durchsucht. Aufgenommen wurden Studien, wenn sie die Leistung der abdominalen Ultraschall-Elastografie bezüglich der Erkennung fibrotischer Darmstrikturen bei Patienten mit Morbus Crohn bewerteten und wenn als Referenzstandard eine histologische Untersuchung oder eine notwendige Operation im Anschluss an medizinische Behandlung durchgeführt wurde. Die Qualitätsbeurteilung der Studien erfolgte mittels QUADAS („Quality Assessment of Diagnostic Accuracy Studies“).

Ergebnisse 6 Studien wurden ausgewählt, die insgesamt 217 Patienten mit Morbus Crohn und 231 Darmsegmente, darunter 76 Darmsegmente mit fibrotischer Striktur, einschlossen. 3 Studien verwendeten die Strain-Ratio und die 3 anderen den Strain-Value als Parameter für die Darmsteifigkeit. Sowohl die gepoolte standardisierte mittlere Strain-Ratio als auch der gepoolte standardisierte mittlere Strain-Value waren in Darmsegmenten mit fibrotischen Strikturen höher als in solchen ohne fibrotische Strikturen. Die standardisierte Mittelwertdifferenz betrug mit fibrotischen Strikturen 0,85 (95 % Konfidenzniveau [CI]: 0 bis 1,71; p = 0,05) und ohne Strikturen 1,0 (95 % CI: –0,11 bis 2,10; p = 0,08). Es gab eine große Heterogenität zwischen den Studien. Alle Studien hatten ein „hohes" oder „nicht eindeutiges Risiko“ für Bias.

Schlussfolgerung Die Ultraschall-Elastografie könnte fibrotische Darmstrikturen bei Patienten mit Morbus Crohn nachweisen. Erforderlich sind gut konzipierte, qualitativ hochwertige Diagnosestudien mit ausreichender Stichprobengröße.

Key words

ultrasound elastography - Crohn’s disease - fibrotic bowel stricture - gastrointestinal tract

• References

• 1 Freeman HJ. Natural history and long-term clinical course of Crohn’s disease. World J Gastroenterol 2014; 20: 31-36
• 2 Cosnes J, Gower-Rousseau C, Seksik P. et al. Epidemiology and Natural History of Inflammatory Bowel Diseases. Gastroenterology 2011; 140: 1785-1794.e4
• 3 Li C, Kuemmerle JF. Mechanisms That Mediate the Development of Fibrosis in Patients With Crohnʼs Disease. Inflamm Bowel Dis 2014; 20: 1250-1258
• 4 Peyrin-Biroulet L, Loftus EV, Colombel JF. et al. The Natural History of Adult Crohn’s Disease in Population-Based Cohorts. Am J Gastroenterol 2010; 105: 289-297
• 5 Rieder F, Fiocchi C, Rogler G. Mechanisms, Management, and Treatment of Fibrosis in Patients With Inflammatory Bowel Diseases. Gastroenterology 2017; 152: 340-350.e6
• 6 Latella G, Rieder F. Intestinal fibrosis: ready to be reversed. Curr Opin Gastroenterol 2017; 33: 239-245
• 7 Stidham RW, Higgins PD. Imaging of intestinal fibrosis: current challenges and future methods. United Eur Gastroenterol J 2016; 4: 515-522
• 8 Bryant RV, Friedman AB, Wright EK. et al. Gastrointestinal ultrasound in inflammatory bowel disease: an underused resource with potential paradigm-changing application. Gut 2018; 67: 973-985
• 9 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 Crohn’s Colitis 2017; 11: 3-25
• 10 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: 556-585
• 11 Pescatori LC, Mauri G, Savarino E. et al. Bowel Sonoelastography in Patients with Crohn’s Disease: A Systematic Review. Ultrasound Med Biol 2018; 44: 297-302
• 12 Stidham RW, Higgins PD. Imaging of intestinal fibrosis: current challenges and future methods. United Eur Gastroenterol J 2016; 4: 515-522
• 13 Kim K, Johnson LA, Jia C. et al. Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model. Ultrasound Med Biol 2008; 34: 902-912
• 14 Stidham RW, Xu J, Johnson LA. 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
• 15 Handbook for DTA Reviews | Cochrane Screening and Diagnostic Tests n.d. http://methods.cochrane.org/sdt/handbook-dta-reviews (accessed May 29, 2018)
• 16 Bettenworth D, Nowacki TM, Cordes F. et al. Assessment of stricturing Crohn’s disease: Current clinical practice and future avenues. World J Gastroenterol 2016; 22: 1008-1016
• 17 Dietrich CF, Bamber J, Berzigotti A. et al. EFSUMB Guidelines and Recommendations on the Clinical Use of Liver Ultrasound Elastography, Update 2017 (Long Version). Ultraschall in Med 2017; 38: e16-e47
• 18 Whiting PF, Rutjes AWS, Westwood ME. et al. QUADAS-2: A Revised Tool for the Quality Assessment of Diagnostic Accuracy Studies. Ann Intern Med 2011; 155: 529-536
• 19 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177-188
• 20 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: 889-899
• 21 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: 422-430
• 22 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: 855-863
• 23 Giannetti A, Matergi M, Biscontri M. et al. Real-time elastography in Crohn’s disease: feasibility in daily clinical practice. J Ultrasound 2017; 20: 147-155
• 24 Coelho R, Ribeiro H, Maconi G. Bowel Thickening in Crohnʼs Disease. Inflamm Bowel Dis 2017; 23: 23-34
• 25 Serra C, Rizzello F, Pratico’ C. 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
• 26 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: 421-430
• 27 Pita I, Magro F. Advanced imaging techniques for small bowel Crohn’s disease: what does the future hold?. Therap Adv Gastroenterol 2018; 11: 1756283X1875718
• 28 de Sousa HT, Brito J, Magro F. New cross-sectional imaging in IBD. Curr Opin Gastroenterol 2018; 34: 194-207
• 29 Quaia E, Gennari AG, Cova MA. et al. 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
• 30 Orlando S, Fraquelli M, Coletta M. et al. Ultrasound Elasticity Imaging Predicts Therapeutic Outcomes of Patients With Crohn’s Disease Treated With Anti-Tumour Necrosis Factor Antibodies. J Crohn’s Colitis 2018; 12: 63-70
• 31 Branchi F, Caprioli F, Orlando S. et al. Non-invasive evaluation of intestinal disorders: The role of elastographic techniques. World J Gastroenterol 2017; 23: 28-32
• 32 Lo Re G, Picone D, Vernuccio F. et al. Comparison of US Strain Elastography and Entero-MRI to Typify the Mesenteric and Bowel Wall Changes during Crohn’s Disease: A Pilot Study. Biomed Res Int 2017; 2017: 4257987
• 33 Havre R, Gilja OH. Elastography and strain rate imaging of the gastrointestinal tract. Eur J Radiol 2014; 83: 438-441
• 34 Giannetti A, Biscontri M, Matergi M. et al. Feasibility of CEUS and strain elastography in one case of ileum Crohn stricture and literature review. J Ultrasound 2016; 19: 231-237
• 35 Havre R, Leh S, Gilja O. et al. Strain Assessment in Surgically Resected Inflammatory and Neoplastic Bowel Lesions. Ultraschall in Med 2014; 35: 149-158
• 36 Xu J, Tripathy S, Rubin JM. et al. A new nonlinear parameter in the developed strain-to-applied strain of the soft tissues and its application in ultrasound elasticity imaging. Ultrasound Med Biol 2012; 38: 511-523
• 37 Dillman JR, Stidham RW, Higgins PDR. et al. US Elastography–derived Shear Wave Velocity Helps Distinguish Acutely Inflamed from Fibrotic Bowel in a Crohn Disease Animal Model. Radiology 2013; 267: 757-766
• 38 Dillman JR, Stidham RW, Higgins PDR. 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: 2115-2123
• 39 Fraquelli M, Branchi F, Cribiù FM. et al. The Role of Ultrasound Elasticity Imaging in Predicting Ileal Fibrosis in Crohnʼs Disease Patients. Inflamm Bowel Dis 2015; 21: 2605-2612
• 40 Bezzio C, Monteleone M, Friedman A. 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
• 41 Stidham R, Dillman J, Rubin J. et al. P-111 Using Stiffness Imaging of the Intestine to Predict Response to Medical Therapy in Obstructive Crohnʼs Disease. Inflamm Bowel Dis 2016; 22: S44-S45
• 42 Orlova LP, Samsonova TV, Khalif I. et al. P1018 Strain elastography and differential diagnosis of inflammatory and fibrotic strictures in Crohn’s disease. United Eur Gastroenterol J 2017; 5S: A518
• 43 Mao R, Chen Y, Chen B. et al. P204 Ultrasound elastography–derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in patients with Crohn’s disease receiving surgery. J Crohns Colitis 2016; 10: 195
• 44 Chen YJ, Mao R, He Y. et al. Real-time Shear Wave Ultrasound Elastography in distinguishing inflammatory from fibrotic stenosis in Crohn's disease. Journal of Crohn's and Colitis 2015; 9: S192
• 45 Piscaglia F, Salvatore V, Mulazzani L. et al. Differences in liver stiffness values obtained with new ultrasound elastography machines and Fibroscan: A comparative study. Dig Liver Dis 2017; 49: 802-808