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Diagnostic accuracy of different cross-sectional imaging techniques for disease location and activity in Crohn’s disease and external validation and comparison of MARIAs and IBUS-SAS

  • Special Section: Crohn Disease
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Abstract

Purpose

The comparative accuracy of cross-sectional imaging techniques for evaluating Crohn’s disease (CD) remains uncertain. This study aimed to assess diagnostic accuracy of disease location and activity in different cross-sectional images and validate and compare International Bowel Ultrasound Segmental Activity Score (IBUS-SAS) and Simplified Magnetic Resonance Index of Activity (MARIAs).

Methods

CD patients were retrospectively included from August 2018 to May 2021. We compared accuracy of B-mode intestinal ultrasound (B-IUS), computed tomography enterography (CTE), and magnetic resonance enterography (MRE) for the identification of disease location. Meanwhile, disease activity was compared on B-IUS, color Doppler imaging, CTE, and MRE. ROC analyses were used to validate MARIAs and IBUS-SAS. Spearman rank correlation was performed to evaluate the relationships between MARIAs/IBUS-SAS and CDAI, SES-CD, and inflammatory indicators.

Results

A total of 115 CD patients were evaluated. The diagnostic accuracy of MRE in detecting small bowel disease was superior to that of B-IUS/CTE, showing sensitivity (89.3%), specificity (71.4%), and AUC (0.820). B-IUS had the highest sensitivity (81.2%), specificity (84.8%), and AUC (0.830) for detecting terminal ileal lesions. The diagnostic accuracy for colonic disease and disease activity was not significantly different among these techniques. In the validation of IBUS-SAS, the AUC was 0.860, with an optimal cutoff value to predict active disease of 46.7. MARIAs and IBUS-SAS showed no significant differences in the correlations of CDAI, SES-CD, and inflammatory indicators.

Conclusion

MRE and B-IUS are more sensitive for detecting small bowel CD and terminal ileal CD, respectively. IBUS-SAS has potential for precisely defining CD activity.

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References

  1. Allocca M, Danese S, Laurent V, et al. Use of Cross-Sectional Imaging for Tight Monitoring of Inflammatory Bowel Diseases. Clin Gastroenterol Hepatol.2020;18(6):1309-1323.

    Article  PubMed  Google Scholar 

  2. GBD 2017 Inflammatory Bowel Disease Collaborators. The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol.2020;5:17–30.

  3. 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(2):144-164.

    Article  PubMed  Google Scholar 

  4. Ran Z, Wu K, Matsuoka K, et al. Asian Organization for Crohn's and Colitis and Asia Pacific Association of Gastroenterology practice recommendations for medical management and monitoring of inflammatory bowel disease in Asia. J Gastroenterol Hepatol.2021;36(3):637-645.

    Article  PubMed  Google Scholar 

  5. Bollegala N, Griller N, Bannerman H, et al. Ultrasound vs Endoscopy, Surgery, or Pathology for the Diagnosis of Small Bowel Crohn's Disease and its Complications. Inflamm Bowel Dis.2019;25(8):1313-1338.

    Article  PubMed  Google Scholar 

  6. Rispo A, Imperatore N, Testa A, et al. Diagnostic Accuracy of Ultrasonography in the Detection of Postsurgical Recurrence in Crohn's Disease: A Systematic Review with Meta-analysis. Inflamm Bowel Dis.2018;24(5):977-988.

    Article  PubMed  Google Scholar 

  7. Sævik F, Eriksen R, Eide GE, et al. Development and Validation of a Simple Ultrasound Activity Score for Crohn's Disease. J Crohns Colitis.2021;15(1):115-124.

    Article  PubMed  Google Scholar 

  8. Gower-Rousseau C, Sarter H, Savoye G, et al. Validation of the Inflammatory Bowel Disease Disability Index in a population-based cohort. Gut.2017;66(4):588-596.

    Article  PubMed  Google Scholar 

  9. Rimola J, Rodriguez, S, Garcia-Bosch O, et al. Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease. Gut.2009;58(8):1113-1120.

    Article  CAS  PubMed  Google Scholar 

  10. Ordás I, Rimola J, Alfaro I, et al. Development and Validation of a Simplified Magnetic Resonance Index of Activity for Crohn's Disease. Gastroenterology.2019; 157(2):432-439.

    Article  PubMed  Google Scholar 

  11. Roseira J, Ventosa, AR, de Sousa HT, et al. The new simplified MARIA score applies beyond clinical trials: A suitable clinical practice tool for Crohn's disease that parallels a simple endoscopic index and fecal calprotectin. United European Gastroenterol J. 2020;8(10):1208-1216.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hoffmann T, Fusco S, Blumenstock G, et al. Evaluation of bowel wall thickness by ultrasound as early diagnostic tool for therapeutic response in Crohn's disease patients treated with ustekinumab. Z Gastroenterol.2020.

  13. Laterza L, Ainora ME, Garcovich M, et al. Bowel contrast-enhanced ultrasound perfusion imaging in the evaluation of Crohn's disease patients undergoing anti-TNFalpha therapy. Dig Liver Dis.2020.

  14. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  16. Maconi G, Greco S, Duca P, et al. Prevalence and clinical significance of sonographic evidence of mesenteric fat alterations in Crohn's disease. Inflamm Bowel Dis.2008;14(11):1555-1561.

    Article  PubMed  Google Scholar 

  17. Deban L, Correale C, Vetrano S, et al. Multiple pathogenic roles of microvasculature in inflammatory bowel disease: a Jack of all trades. Am J Pathol.2008;172(6):1457-1466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Migaleddu V, Scanu AM, Quaia E, et al. Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn's disease. Gastroenterology.2009;137(1):43-52.

    Article  PubMed  Google Scholar 

  19. Limberg B. Diagnosis of chronic inflammatory bowel disease by ultrasonography. Z Gastroenterol.1999;37(6):495-508.

    CAS  PubMed  Google Scholar 

  20. Novak KL, Nylund K, Maaser 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(4):609-616.

    Article  PubMed  Google Scholar 

  21. Daperno M, D'Haens G, Van Assche G, et al. SES-CD-Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD. Gastrointest Endosc.2004;60(4):505-512.

    Article  PubMed  Google Scholar 

  22. Koh D, Miao Y, Chinn R, et al. MR imaging evaluation of the activity of Crohn's disease. AJR Am J Roentgenol.2001;177(6):1325-1332.

    Article  CAS  PubMed  Google Scholar 

  23. Taylor SA, Mallett S, Bhatnagar G, et al. 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(8):548-558.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Elsayes K, Al-Hawary M, Jagdish J, et al. CT enterography: principles, trends, and interpretation of findings. Radiographics.2010;30(7):1955-1970.

    Article  PubMed  Google Scholar 

  25. Ripollés T, Martínez-Pérez M, Paredes J, et al. The Role of Intravenous Contrast Agent in the Sonographic Assessment of Crohn's Disease Activity: Is Contrast Agent Injection Necessary? J Crohns Colitis.2019;13(5):585-592.

    Article  PubMed  Google Scholar 

  26. Jing J, Wu Y, Zhang H, et al. The establishment of a regression model from four modes of ultrasound to predict the activity of Crohn's disease. Sci Rep.2021;11(1):77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hanley JA, Mcneil BJ, et al. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology.1982;143(1):29.

    Article  CAS  PubMed  Google Scholar 

  28. Rimola J, Ordás I, Rodriguez S, et al. Magnetic resonance imaging for evaluation of Crohn's disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis.2011;17(8):1759-1768.

    Article  PubMed  Google Scholar 

  29. Lee S, Kim A, Yang S, et al. Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology.2009;251(3):751-761.

    Article  PubMed  Google Scholar 

  30. Jensen M, Kjeldsen J, Rafaelsen S, et al. Diagnostic accuracies of MR enterography and CT enterography in symptomatic Crohn's disease. Scand J Gastroenterol.2011;46(12):1449-1457.

    Article  PubMed  Google Scholar 

  31. D'Silva A, Fox D, Nasser Y, et al. Prevalence and Risk Factors for Fatigue in Adults With Inflammatory Bowel Disease: A Systematic Review With Meta-Analysis. Clin Gastroenterol Hepatol.2021.

  32. Pascu M, Roznowski A, Müller H, et al. Clinical relevance of transabdominal ultrasonography and magnetic resonance imaging in patients with inflammatory bowel disease of the terminal ileum and large bowel. Inflamm Bowel Dis.2004;10(4):373-382.

    Article  CAS  PubMed  Google Scholar 

  33. Zezos P, Zittan E, Islam S, et al. Associations between quantitative evaluation of bowel wall microvascular flow by contrast-enhanced ultrasound and indices of disease activity in Crohn's disease patients using both bolus and infusion techniques. J Clin Ultrasound.2019;47(8):453-460.

    Article  PubMed  Google Scholar 

  34. Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med.2011;155(8):529-536.

    Article  PubMed  Google Scholar 

  35. Bots S, Nylund K, Löwenberg M, et al. Ultrasound for Assessing Disease Activity in IBD Patients: A Systematic Review of Activity Scores. J Crohns Colitis.2018;12(8):920-929.

    Article  CAS  PubMed  Google Scholar 

  36. 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.

    Article  PubMed  Google Scholar 

  37. Zorzi F, Stasi E, Bevivino G, et al. A sonographic lesion index for Crohn's disease helps monitor changes in transmural bowel damage during therapy. Clin Gastroenterol Hepatol.2014;12(12):2071-2077.

    Article  PubMed  Google Scholar 

  38. Ishikawa D, Ando T, Watanabe O, et al. Images of colonic real-time tissue sonoelastography correlate with those of colonoscopy and may predict response to therapy in patients with ulcerative colitis. BMC Gastroenterol.2011;11:29.

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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.

    Article  PubMed  Google Scholar 

  40. Sasaki T, Kunisaki R, Kinoshita H, et al. Use of color Doppler ultrasonography for evaluating vascularity of small intestinal lesions in Crohn's disease: correlation with endoscopic and surgical macroscopic findings. Scand J Gastroenterol.2014;49(3):295-301.

    Article  PubMed  Google Scholar 

  41. Civitelli F, Di Nardo G, Oliva S, et al. Ultrasonography of the colon in pediatric ulcerative colitis: a prospective, blind, comparative study with colonoscopy. J Pediatr.2014;165(1):78-84.e2.

    Article  PubMed  Google Scholar 

  42. Paredes JM, Ripollés T, Cortés X, et al. Contrast-enhanced ultrasonography: usefulness in the assessment of postoperative recurrence of Crohn's disease. J Crohns Colitis.2013;7(3):192-201.

    Article  PubMed  Google Scholar 

  43. Paredes JM, Ripollés T, Cortés X, et al. Non-invasive diagnosis and grading of postsurgical endoscopic recurrence in Crohn's disease: usefulness of abdominal ultrasonography and (99m)Tc-hexamethylpropylene amineoxime-labelled leucocyte scintigraphy. J Crohns Colitis.2010;4(5):537-545.

    Article  PubMed  Google Scholar 

  44. Dragoni G, Innocenti T, Lynch EN, et al. P141 IBUS-SAS for Crohn's disease ultrasound activity: initial validation and research of the optimal cut-off score. J Crohns Colitis.2021(Supplement_1):Supplement_1.

  45. Martínez MJ, Ripollés T, Paredes JM, Blanc E, Martí-Bonmatí L. Assessment of the extension and the inflammatory activity in Crohn's disease: comparison of ultrasound and MRI. Abdom Imaging.2009;34(2):141-148.

    Article  PubMed  Google Scholar 

  46. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al. Prospective comparison of computed tomography enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn's disease. Inflamm Bowel Dis.2011;17(5):1073-1080.

    Article  CAS  PubMed  Google Scholar 

  47. Koplay M, Guneyli S, Cebeci H, et al. Magnetic resonance enterography with oral mannitol solution: Diagnostic efficacy and image quality in Crohn disease. Diagn Interv Imaging.2017;98(12):893-899.

    Article  CAS  PubMed  Google Scholar 

  48. Hollerbach S, Geissler A, Schiegl H, et al. The accuracy of abdominal ultrasound in the assessment of bowel disorders. Scand J Gastroenterol.1998;33(11):1201-1208.

    Article  CAS  PubMed  Google Scholar 

  49. 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.

    Article  CAS  PubMed  Google Scholar 

  50. Amitai M, Raviv-Zilka L, Hertz M, et al. Main Imaging Features of Crohn's Disease: Agreement between MR-Enterography and CT-Enterography. Isr Med Assoc J.2015;17(5):293-297.

    PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge and thank the patients participated in this study and Yali Wang (Department of Ultrasound) and Qing Xu (Department of Radiology) for their clinical support to this work.

Funding

No funding was received.

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Author notes

  1. Chenjing Xu, Linzhen Li, and Yanyan Zhang are co-first authors and contributed equally.

Authors and Affiliations

  1. Department of Gastroenterology, The First Affiliated Hospital of Nanjing Medical University, Nanjing Medical University, Nanjing, Jiangsu, China

    Chenjing Xu, Ruohan Wang & Hongjie Zhang

  2. Department of Gastroenterology, The First Affiliated Hospital of Wannan Medical College, Wuhu, China

    Linzhen Li

  3. Department of Ultrasound, The First Affiliated Hospital of Nanjing Medical University, Nanjing, China

    Yanyan Zhang

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  1. Chenjing Xu
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Contributions

CJX and HJZ involved in substantial contributions to conception and design of the study. CJX, LZL, and YYZ contributed to data curation, analysis and interpretation of the data, and drafting the article. CJX, LZL, YYZ, RHW, and HJZ contributed to making critical revisions related to the important intellectual content of the manuscript and final approval.

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Correspondence to Hongjie Zhang.

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Xu, C., Li, L., Zhang, Y. et al. Diagnostic accuracy of different cross-sectional imaging techniques for disease location and activity in Crohn’s disease and external validation and comparison of MARIAs and IBUS-SAS. Abdom Radiol 48, 821–832 (2023). https://doi.org/10.1007/s00261-022-03751-7

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