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Alimentary Tract| Volume 53, ISSUE 6, P729-737, June 2021

Bowel contrast-enhanced ultrasound perfusion imaging in the evaluation of Crohn's disease patients undergoing anti-TNFα therapy

Published:September 05, 2020DOI:https://doi.org/10.1016/j.dld.2020.08.005

      Abstract

      Aim

      To evaluate whether changes in bowel perfusion parameters measured by dynamic-CEUS (D-CEUS) can be used for monitoring response to therapy in active Crohn disease (CD).

      Methods

      Fifty-four CD patients were evaluated with d-CEUS before (T0) and after 2 (T1), 6 (T2) and 12 weeks (T3) of anti-TNFα therapy. Variations from baseline were calculated for: peak intensity, PI; area under the curve, AUC; slope of wash in, Pw; time to peak, TP; mean transit time, MTT (median percentage values) and were correlated with combined endoscopic/clinical response after 12 weeks and clinical relapse within 6 months.

      Results

      70% of patients achieved combined endoscopic/clinical response (responders). The reduction in PI, AUC, Pw and MTT between T1 and T0 was higher in responders. Relapsers (21%) showed significantly lower reduction in delta PI and Pw at T1 and T2. At T3 they showed a new increase in PI and lower reduction in delta Pw. In relapsers, AUC showed a significantly lower decrease at T2 and T3, TP showed a significant reduction at T3 and MTT showed a progressive increase at the different time-points, reaching the statistical significance at T3.

      Conclusions

      d-CEUS might become a reliable predictor of combined endoscopic/clinical response and clinical relapse in CD.

      Keywords

      Abbreviations:

      CD (Crohn's disease), US (Ultrasonography), d-CEUS (Dynamic contrast-enhanced ultrasound), CDAI (Crohn's disease activity index), ROI (Region of interest), PI (Peak intensity), TP (Time to peak intensity), AUC (Area under the time-intensity curve), Pw (Slope coefficient of wash in), MTT (Mean transit time), SES-CD (Simplified endoscopic activity score for CD), ICC (Intraclass Correlation Coefficient)
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      References

        • Migaleddu V.
        • Quaia E.
        • Scanu D.
        • et al.
        Inflammatory activity in Crohn's disease: CE-US.
        Abdom Imaging. 2011; 36 ([published Online First: Epub Date]|): 142-148https://doi.org/10.1007/s00261-010-9622-8
        • Best W.R.
        • Becktel J.M.
        • Singleton J.W.
        • et al.
        Development of a Crohn's disease activity index. National cooperative Crohn's disease study.
        Gastroenterology. 1976; 70: 439-444
        • Onali S.
        • Calabrese E.
        • Pallone F.
        Measuring disease activity in Crohn's disease.
        Abdom Imaging. 2012; 37 ([published Online First: Epub Date]|): 927-932https://doi.org/10.1007/s00261-012-9877-3
        • Huprich J.E.
        • Fletcher J.G.
        CT enterography: principles, technique and utility in Crohn's disease.
        Eur J Radiol. 2009; 69 ([published Online First: Epub Date]|): 393-397https://doi.org/10.1016/j.ejrad.2008.11.014
        • Maaser C.
        • Sturm A.
        • Vavricka S.R.
        • et al.
        ECCO-ESGAR guideline for diagnostic assessment in inflammatory bowel disease.
        J Crohns Colitis. 2018; ([published Online First: Epub Date]|)https://doi.org/10.1093/ecco-jcc/jjy113
        • Dietrich C.F.
        • Averkiou M.A.
        • Correas J.M.
        • et al.
        An EFSUMB introduction into dynamic contrast-enhanced ultrasound (DCE-US) for quantification of tumour perfusion.
        Ultraschall in der Medizin. 2012; 33 ([published Online First: Epub Date]|): 344-351https://doi.org/10.1055/s-0032-1313026
        • Wong D.D.
        • Forbes G.M.
        • Zelesco M.
        • et al.
        Crohn's disease activity: quantitative contrast-enhanced ultrasound assessment.
        Abdom Imaging. 2012; 37 ([published Online First: Epub Date]|): 369-376https://doi.org/10.1007/s00261-011-9792-z
        • Girlich C.
        • Schacherer D.
        • Jung E.M.
        • et al.
        Comparison between a clinical activity index (Harvey-Bradshaw-Index), laboratory inflammation markers and quantitative assessment of bowel wall vascularization by contrast-enhanced ultrasound in Crohn's disease.
        Eur J Radiol. 2012; 81 ([published Online First: Epub Date]|): 1105-1109https://doi.org/10.1016/j.ejrad.2011.02.054
        • Serra C.
        • Menozzi G.
        • Labate A.M.
        • et al.
        Ultrasound assessment of vascularization of the thickened terminal ileum wall in Crohn's disease patients using a low-mechanical index real-time scanning technique with a second generation ultrasound contrast agent.
        Eur J Radiol. 2007; 62 ([published Online First: Epub Date]|): 114-121https://doi.org/10.1016/j.ejrad.2006.11.027
        • Migaleddu V.
        • Scanu A.M.
        • Quaia E.
        • et al.
        Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn's disease.
        Gastroenterology. 2009; 137 ([published Online First: Epub Date]|): 43-52https://doi.org/10.1053/j.gastro.2009.03.062
        • Ripolles T.
        • Martinez-Perez M.J.
        • Blanc E.
        • et al.
        Contrast-enhanced ultrasound (CEUS) in Crohn's disease: technique, image interpretation and clinical applications.
        Insights Imaging. 2011; 2 ([published Online First: Epub Date]|): 639-652https://doi.org/10.1007/s13244-011-0124-1
        • De Franco A.
        • Di Veronica A.
        • Armuzzi A.
        • et al.
        Ileal Crohn disease: mural microvascularity quantified with contrast-enhanced US correlates with disease activity.
        Radiology. 2012; 262 ([published Online First: Epub Date]|): 680-688https://doi.org/10.1148/radiol.11110440
        • Guidi L.
        • De Franco A.
        • De Vitis I.
        • et al.
        Contrast-enhanced ultrasonography with SonoVue after infliximab therapy in Crohn's disease.
        Eur Rev Med Pharmacol Sci. 2006; 10: 23-26
        • Quaia E.
        • Migaleddu V.
        • Baratella E.
        • et al.
        The diagnostic value of small bowel wall vascularity after sulfur hexafluoride-filled microbubble injection in patients with Crohn's disease. Correlation with the therapeutic effectiveness of specific anti-inflammatory treatment..
        Eur J Radiol. 2009; 69 ([published Online First: Epub Date]|): 438-444https://doi.org/10.1016/j.ejrad.2008.10.029
        • Quaia E.
        • Cabibbo B.
        • De Paoli L.
        • et al.
        The value of time-intensity curves obtained after microbubble contrast agent injection to discriminate responders from non-responders to anti-inflammatory medication among patients with Crohn's disease.
        Eur Radiol. 2013; 23 ([published Online First: Epub Date]|): 1650-1659https://doi.org/10.1007/s00330-012-2754-1
        • 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 ([published Online First: Epub Date]|): 2029-2037https://doi.org/10.1097/MIB.0000000000000159
        • 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 ([published Online First: Epub Date]|): 1168-1183https://doi.org/10.1097/MIB.0000000000000706
        • Harvey R.F.
        • Bradshaw J.M.
        A simple index of Crohn's-disease activity.
        Lancet. 1980; 1 ([published Online First: Epub Date]|): 514https://doi.org/10.1016/s0140-6736(80)92767-1
        • Strobel D.
        • Goertz R.S.
        • Bernatik T.
        Diagnostics in inflammatory bowel disease: ultrasound.
        World J Gastroenterol. 2011; 17 ([published Online First: Epub Date]|): 3192-3197https://doi.org/10.3748/wjg.v17.i27.3192
        • Zocco M.A.
        • Garcovich M.
        • Lupascu A.
        • et al.
        Early prediction of response to sorafenib in patients with advanced hepatocellular carcinoma: the role of dynamic contrast enhanced ultrasound.
        J Hepatol. 2013; 59 ([published Online First: Epub Date]|): 1014-1021https://doi.org/10.1016/j.jhep.2013.06.011
        • Daperno M.
        • D'Haens G.
        • Van Assche G.
        • et al.
        Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD.
        Gastrointest Endosc. 2004; 60: 505-512
        • Sands B.E.
        • Anderson F.H.
        • Bernstein C.N.
        • et al.
        Infliximab maintenance therapy for fistulizing Crohn's disease.
        N Engl J Med. 2004; 350 ([published Online First: Epub Date]|): 876-885https://doi.org/10.1056/NEJMoa030815
        • Sostegni R.
        • Daperno M.
        • Scaglione N.
        • et al.
        Review article: crohn's disease: monitoring disease activity.
        Aliment Pharmacol Ther. 2003; 17 (-7[published Online First: Epub Date]|): 11https://doi.org/10.1046/j.1365-2036.17.s2.17.x
        • Landis J.R.
        • Koch G.G.
        The measurement of observer agreement for categorical data.
        Biometrics. 1977; 33: 159-174
        • Bland J.M.
        • A D.
        Statistical Methods in Medical Research.
        Stat Methods Med Res. 1999; ([published Online First: Epub Date]|): 135-160https://doi.org/10.1191/096228099673819272
        • Pariente B.
        • Cosnes J.
        • Danese S.
        • et al.
        Development of the Crohn's disease digestive damage score, the Lemann score.
        Inflamm Bowel Dis. 2011; 17 ([published Online First: Epub Date]|): 1415-1422https://doi.org/10.1002/ibd.21506
        • Colombel J.F.
        • Panaccione R.
        • Bossuyt P.
        • et al.
        Effect of tight control management on Crohn's disease (CALM): a multicentre, randomised, controlled phase 3 trial.
        Lancet. 2018; 390 ([published Online First: Epub Date]|): 2779-2789https://doi.org/10.1016/S0140-6736(17)32641-7
        • Coelho R.
        • Ribeiro H.
        • Maconi G.
        Bowel thickening in Crohn's disease: fibrosis or inflammation? diagnostic ultrasound imaging tools.
        Inflamm Bowel Dis. 2017; 23 ([published Online First: Epub Date]|): 23-34https://doi.org/10.1097/MIB.0000000000000997
        • Ripolles T.
        • Martinez M.J.
        • Paredes J.M.
        • et al.
        Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy.
        Radiology. 2009; 253 ([published Online First: Epub Date]|): 241-248https://doi.org/10.1148/radiol.2531082269
        • Socaciu M.
        • Ciobanu L.
        • Diaconu B.
        • et al.
        Non-invasive assessment of inflammation and treatment response in patients with Crohn's disease and ulcerative colitis using contrast-enhanced ultrasonography quantification.
        J Gastrointest Liver Dis: JGLD. 2015; 24 ([published Online First: Epub Date]|): 457-465https://doi.org/10.15403/jgld.2014.1121.244.chr
        • Mocci G.
        • Migaleddu V.
        • Cabras F.
        • et al.
        SICUS and CEUS imaging in Crohn's disease: an update.
        J Ultrasound. 2017; 20 ([published Online First: Epub Date]|): 1-9https://doi.org/10.1007/s40477-016-0230-5
        • 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 ([published Online First: Epub Date]|): 606-616https://doi.org/10.1148/radiol.2016152461
        • Paredes J.M.
        • Ripolles T.
        • Cortes X.
        • et al.
        Contrast-enhanced ultrasonography: usefulness in the assessment of postoperative recurrence of Crohn's disease.
        J Crohns Colitis. 2013; 7 ([published Online First: Epub Date]|): 192-201https://doi.org/10.1016/j.crohns.2012.03.017