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

Kerri L Novak, Kim Nylund, Christian Maaser, Frauke Petersen, Torsten Kucharzik, Cathy Lu, Mariangela Allocca, Giovanni Maconi, Floris de Voogd, Britt Christensen, Rose Vaughan, Carolina Palmela, Dan Carter, Rune Wilkens, Kerri L Novak, Kim Nylund, Christian Maaser, Frauke Petersen, Torsten Kucharzik, Cathy Lu, Mariangela Allocca, Giovanni Maconi, Floris de Voogd, Britt Christensen, Rose Vaughan, Carolina Palmela, Dan Carter, Rune Wilkens

Abstract

Background and aims: Intestinal ultrasound [IUS] is an accurate, patient-centreed monitoring tool that objectively evaluates Crohn's disease [CD] activity. However no current, widely accepted, reproducible activity index exists to facilitate consistent IUS identification of inflammatory activity. The aim of this study is to identify key parameters of CD inflammation on IUS, evaluate their reliability, and develop an IUS index reflecting segmental activity.

Methods: There were three phases: [1] expert consensus Delphi method to derive measures of IUS activity; [2] an initial, multi-expert case acquisition and expert interpretation of 20 blinded cases, to measure inter-rater reliability for individual measures; [3] refinement of case acquisition and interpretation by 12 international experts, with 30 blinded case reads with reliability assessment and development of a segmental activity score.

Results: Delphi consensus: 11 experts representing seven countries identified four key parameters including: [1] bowel wall thickness [BWT]; [2] bowel wall stratification; [3] hyperaemia of the wall [colour Doppler imaging]; and [4] inflammatory mesenteric fat. Blind read: each variable exhibited moderate to substantial reliability. Optimal, standardised image and cineloop acquisition were established. Second blind read and score development: intra-class correlation coefficient [ICC] for BWT was almost perfect at 0.96 [0.94-0.98]. All four parameters correlated with the global disease activity assessment and were included in the final International Bowel Ultrasound Segmental Activity Score with almost perfect ICC (0.97 [0.95-0.99, p <0.001]).

Conclusions: Using expert consensus and standardised approaches, identification of key activity measurements on IUS has been achieved and a segmental activity score has been proposed, demonstrating excellent reliability.

Keywords: Ultrasound; activity index; monitoring; reliability.

© The Author(s) 2020. Published by Oxford University Press on behalf of European Crohn’s and Colitis Organisation.

Figures

Figure 1.
Figure 1.
Measurement of bowel wall thickness. Measures of the bowel wall occur in two orientations: cross-section and longitudinal. The calipers are placed perpendicular to the wall, with two individual measures taken in each orientation, at least 1 cm apart in longitudinal and more than 90° in cross section, in the segment of bowel most affected by disease. The caliper placement occurs from the interface of the mucosa and muscularis mucosae, to the serosa [interface between the serosa and muscularis propria]. All four measures are averaged. Yellow double-headed arrow is the first measurement. Green double-headed arrows are valid second measurements, where red double-headed arrows are invalid caliper placements.
Figure 2.
Figure 2.
The association between scan quality and rater confidence. Quality and confidence scored on a 5-point Likert scale. Red line is the linear association, grey lines are confidence intervals.
Figure 3.
Figure 3.
The association between physician global disease activity assessment and individual intestinal ultrasound parameters. Associations between A] mean activity and bowel wall thickness [top left], B] mean activity and inflammatory fat [top right], C] mean activity and colour Doppler imaging [bottom left], and D] mean activity and bowel wall stratification.
Figure 4.
Figure 4.
Application of the segmental activity and severity scores. Applying the scores: Bowel wall thickness [BWT] = [7.8 + 7.1 + 8.5 + 8.4] / 4 = 7.95 ≈ 8.0. Blood flow/ colour Doppler signal [CDS] = 0 [no signals]. Inflammatory fat [i-fat] = 2 [certain]. Bowel wall stratification [BWS] = 2 [focal disruption · 4 + 2 · 15 + 0 · 7 + 2 · 4 = 70.

References

    1. Peyrin-Biroulet L, Sandborn W, Sands BE, et al. . Selecting Therapeutic Targets in Inflammatory Bowel Disease [STRIDE]: determining therapeutic goals for treat-to-target. Am J Gastroenterol 2015;110:1324–38.
    1. Dulai PS, Jairath V. How do we treat inflammatory bowel diseases to aim for endoscopic remission? Clin Gastroenterol Hepatol 2020;18:1300–8.
    1. Bryant RV, Friedman AB, Wright EK, et al. . Gastrointestinal ultrasound in inflammatory bowel disease: an underused resource with potential paradigm-changing application. Gut 2018;67:973–85.
    1. 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;22:1168–83.
    1. Maaser C, Sturm A, Vavricka SR, et al. . ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis 2019;13:144–64.
    1. Taylor SA, Mallett S, Bhatnagar G, et al. ; METRIC study investigators. Diagnostic accuracy of magnetic resonance enterography and small bowel ultrasound for the extent and activity of newly diagnosed and relapsed Crohn’s disease [METRIC]: a multicentre trial. Lancet Gastroenterol Hepatol 2018;3:548–58.
    1. Rajagopalan A, Sathananthan D, An YK, et al. . Gastrointestinal ultrasound in inflammatory bowel disease care: patient perceptions and impact on disease-related knowledge. JGH Open 2020;4:267–72.
    1. Brenner DJ, Doll R, Goodhead DT, et al. . Cancer risks attributable to low doses of ionizing radiation: assessing what we really know. Proc Natl Acad Sci U S A 2003;100:13761–6.
    1. Jairath V, Ordas I, Zou G, et al. . Reliability of measuring ileo-colonic disease activity in Crohn’s disease by magnetic resonance enterography. Inflamm Bowel Dis 2018;24:440–9.
    1. Miles A, Bhatnagar G, Hallian S, et al. . Magnetic resonance enterography, small bowel ultrasound and colonoscopy to diagnose and stage Crohn’s disease: patient acceptability and perceived burden. Eur Radiol 2019;29:1083–93.
    1. Novak K, Tanyingoh D, Petersen F, et al. . Clinic-based point of care transabdominal ultrasound for monitoring Crohn’s disease: impact on clinical decision making. J Crohns Colitis 2015;9:795–801.
    1. Bots S, Nylund K, Löwenberg M, Gecse K, Gilja OH, D’Haens G. Ultrasound for assessing disease activity in IBD patients: a systematic review of activity scores. J Crohns Colitis 2018;12:920–9.
    1. Nylund K, Maconi G, Hollerweger A, et al. . EFSUMB Recommendations and Guidelines for gastrointestinal ultrasound. Ultraschall Med 2017;38:e1–15.
    1. Maconi G, Carsana L, Fociani P, et al. . Small bowel stenosis in Crohn’s disease: clinical, biochemical and ultrasonographic evaluation of histological features. Aliment Pharmacol Ther 2003;18:749–56.
    1. Pallotta N, Vincoli G, Montesani C, 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.
    1. Greenup AJ, Bressler B, Rosenfeld G. Medical imaging in small bowel Crohn’s disease-computer tomography enterography, magnetic resonance enterography, and ultrasound: “Which One Is the Best for What?”. Inflamm Bowel Dis 2016;22:1246–61.
    1. 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 Multicentre Study. Inflamm Bowel Dis 2018;24:2001–6.
    1. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 2016;15:155–63.
    1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–74.
    1. Fraquelli M, Sarno A, Girelli C, et al. . Reproducibility of bowel ultrasonography in the evaluation of Crohn’s disease. Dig Liver Dis 2008;40:860–6.
    1. Goodsall TM, Nguyen TM, Parker CE, et al. . Systematic review: gastrointestinal ultrasound scoring indices for inflammatory bowel disease. J Crohns Colitis 2020, Jul 2. doi: 10.1093/ecco-jcc/jjaa129. Online ahead of print.
    1. Rimola J, Fernàndez-Clotet A, Capozzi N, et al. . Pre-treatment magnetic resonance enterography findings predict the response to TNF-alpha inhibitors in Crohn’s disease. Aliment Pharmacol Ther 2020;52:1563‐ 73.
    1. Kucharzik T, Wittig BM, Helwig U, et al. ; TRUST study group. Use of intestinal ultrasound to monitor Crohn’s disease activity. Clin Gastroenterol Hepatol 2017;15:535–42.e2.
    1. Wilkens R, Hagemann-Madsen RH, Peters DA, 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.
    1. 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;23:2001–10.
    1. Rimola J, Rodriguez S, García-Bosch O, et al. . Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn’s disease. Gut 2009;58:1113–20.
    1. 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;40:134–46.
    1. Sævik F, Eriksen R, Eide GE, Gilja OH, Nylund K. Development and validation of a simple ultrasound activity score for Crohn’s disease. J Crohns Colitis 2020,. Jun 6. doi: 10.1093/ecco-jcc/jjaa112. Online ahead of print.
    1. Zabotti A, Filippou G, Canzoni M, et al. . OMERACT agreement and reliability study of ultrasonographic elementary lesions in osteoarthritis of the foot. RMD Open 2019;5:e000795.
    1. Kucharzik T, Wittig BM, Helwig U, et al. ; TRUST study group. Use of intestinal ultrasound to monitor Crohn’s disease activity. Clin Gastroenterol Hepatol 2017;15:535–42.e2.
    1. Daperno M, Comberlato M, Bossa F, et al. ; IGIBDEndo Group. Training programs on endoscopic scoring systems for inflammatory bowel disease lead to a significant increase in interobserver agreement among community gastroenterologists. J Crohns Colitis 2017;11:556–61.
    1. Khanna R, Zou G, D’Haens G, et al. . Reliability among central readers in the evaluation of endoscopic findings from patients with Crohn’s disease. Gut 2016;65:1119–25.
    1. Panés J, Feagan BG, Hussain F, Levesque BG, Travis SP. Central endoscopy reading in inflammatory bowel diseases. J Crohns Colitis 2016;10[Suppl 2]:S542–7.
    1. Feagan B, Sandborn WJ, Rutgeerts P, et al. . Performance of Crohn’s disease clinical trial endpoints based upon different cutoffs for patient reported outcomes or endoscopic activity: analysis of EXTEND data. Inflamm Bowel Dis 2018;24:932–42.
    1. Tsai R, Mintz A, Lin M, et al. . Magnetic resonance enterography features of small bowel Crohn’s disease activity: an inter-rater reliability study of small bowel active inflammation in clinical practice setting. Br J Radiol 2019;92:20180930.
    1. Tielbeek JA, Makanyanga JC, Bipat S, et al. . Grading Crohn disease activity with MRI: interobserver variability of MRI features, MRI scoring of severity, and correlation with Crohn disease endoscopic index of severity. AJR Am J Roentgenol 2013;201:1220–8.
    1. Booya F, Akram S, Fletcher JG, et al. . CT enterography and fistulizing Crohn’s disease: clinical benefit and radiographic findings. Abdom Imaging 2009;34:467–75.
    1. Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology 1976;70:439–44.
    1. Mary JY, Modigliani R. Development and validation of an endoscopic index of the severity for Crohn’s disease: a prospective multicentre study. Groupe d’Etudes Thérapeutiques des Affections Inflammatoires du Tube Digestif [GETAID]. Gut 1989;30:983–9.
    1. Pariente B, Cosnes J, Danese S, et al. . Development of the Crohn’s disease digestive damage score, the Lémann score. Inflamm Bowel Dis 2011;17:1415–22.

Source: PubMed

3
Iratkozz fel