Abstract
Background and objective
Continuous assessment of disease activity remains a huge challenge during the follow-ups of patients with Crohn’s disease (CD). In this paper, we aimed to evaluate the performance of contrast-enhanced ultrasound (CEUS) by comparing with computed tomography enterography (CTE) in the assessment of disease activity in CD.
Materials and methods
Fifty-two patients diagnosed with CD were included in this study, using the CEUS and CTE as imaging methods for comparison. The selected parameters included the location and thickness of the thickest part of the intestinal wall, mesenteric fat proliferation, mesenteric vessels change, enhancement pattern and the presence of complications. Patients were clinically assessed using the Crohn's disease activity index (CDAI), C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR). Simple endoscopic score for Crohn’s disease (SES-CD) was regarded as the reference standard.
Results
The location of the thickest part of the intestinal wall (κ = 0.653), bowel wall thickness (ICC = 0.795), mesenteric vessels change (κ = 0.692) and complications (κ = 0.796) displayed substantial agreement (0.61–0.80) between CEUS and CTE, while the detection of mesenteric fat proliferation (κ = 0.395) and enhancement pattern (κ = 0.288) showed fair consistency (0.21–0.40) for comparison. In CEUS, bowel wall thickness, mesenteric fat proliferation, enhancement pattern and mesenteric vessels change were statistically significant in assessing CD activity, while bowel wall thickness, mesenteric fat proliferation and mesenteric vessels change in CTE. Bowel wall thickness showed the best diagnostic performance in the assessment of CD activity at CEUS and CTE.
Conclusion
CEUS provides a radiation-free and effective way to assess the CD activity in comparison with CTE, which also avoids frequent colonoscopy examinations, improves tolerance of patients, and reduces the cost of medical care, thereby serving as a useful tool for CD follow-up.
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Abbreviations
- CD:
-
Crohn's disease
- CRP:
-
C-reactive protein
- ESR:
-
Erythrocyte sedimentation rate
- CDAI:
-
Crohn's disease activity index
- SES-CD:
-
Simple endoscopic score for Crohn’s disease
- CEUS:
-
Contrast-enhanced ultrasound
- CTE:
-
Computed tomography enterography
- ICC:
-
Intra-group correlation coefficient
- PPV:
-
Positive predict value
- NPV:
-
Negative predict value
- AUROC:
-
Area under the receiver operating characteristic
References
Gomollon F, Dignass A, Annese V, Tilg H, Van Assche G, Lindsay JO (2017) 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: Part 1: diagnosis and medical management. J Crohns Colitis 11(1):3–25. https://doi.org/10.1093/ecco-jcc/jjw168
Baumgart DC, Sandborn WJ (2012) Crohn’s disease. Lancet 80(9853):1590–1605. https://doi.org/10.1016/S0140-6736(12)60026-9
Feuerstein JD, Cheifetz AS (2017) Crohn disease: epidemiology, diagnosis, and management. Mayo Clin Proc 92(7):1088–1103. https://doi.org/10.1016/j.mayocp.2017.04.010
Tomazoni EI, Benvegnú DM (2018) Symptoms of anxiety and depression, and quality of life of patients with Crohn’s disease. Arq Gastroenterol 55(2):148–153. https://doi.org/10.1590/S0004-2803.201800000-26
Papay P, Ignjatovic A, Karmiris K, Amarante H, Milheller P, Feagan B, Panaccione R (2013) Optimising monitoring in the management of Crohn’s disease: a physician’s perspective. J Crohns Colitis 7(8):653–669. https://doi.org/10.1016/j.crohns.2013.02.005
Vucelic B (2009) Inflammatory bowel diseases: controversies in the use of diagnostic procedures. Dig Dis 27(3):269–277. https://doi.org/10.1159/000228560
Daperno M, D’Haens G, Van Assche G, Baert F, Bulois P, Maunoury V, Rutgeerts P (2004) Development and validation of a new, simplified endoscopic activity score for Crohn’s disease: the SES-CD. Gastrointest Endosc 60(4):505–512. https://doi.org/10.1016/s0016-5107(04)01878-4
Miles A, Bhatnagar G, Halligan S, Gupta A, Tolan D, Zealley I, Taylor SA (2019) Magnetic resonance enterography, small bowel ultrasound and colonoscopy to diagnose and stage Crohn’s disease: patient acceptability and perceived burden. Eur Radiol 29(3):1083–1093. https://doi.org/10.1007/s00330-018-5661-2
Taylor S, Mallett S, Bhatnagar G, Bloom S, Gupta A, Halligan S, Zealley I (2014) METRIC (MREnterography or ulTRasound in Crohn’s disease): a study protocol for a multicentre, non-randomised, single-arm, prospective comparison study of magnetic resonance enterography and small bowel ultrasound compared to a reference standard in those aged 16 and over. BMC Gastroenterol 14:142. https://doi.org/10.1186/1471-230X-14-142
Siddiki HA, Fidler JL, Fletcher JG, Burton SS, Huprich JE, Hough DM, Mandrekar JN (2009) Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn’s disease. Am J Roentgenol 193(1):113–121. https://doi.org/10.2214/AJR.08.2027
Lee SS, Kim AY, Yang S-K, Chung J-W, Kim SY, Park SH, Ha HK (2009) Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology 251(3):751–761. https://doi.org/10.1148/radiol.2513081184
Allocca M, Fiorino G, Bonifacio C, Furfaro F, Gilardi D, Argollo M, Danese S (2018) Comparative accuracy of bowel ultrasound versus magnetic resonance enterography in combination with colonoscopy in assessing Crohn’s disease and guiding clinical decision-making. J Crohn’s Colitis 12(11):1280–1287. https://doi.org/10.1093/ecco-jcc/jjy093
Hakim A, Alexakis C, Pilcher J, Tzias D, Mitton S, Paul T, Kumar S (2020) Comparison of small intestinal contrast ultrasound with magnetic resonance enterography in pediatric Crohn’s disease. JGH Open 4(2):126–131. https://doi.org/10.1002/jgh3.12228
Yu H, Wang Y, Wang Z, Li J, Lu J, Hu D (2020) Prospective comparison of diffusion-weighted magnetic resonance enterography and contrast enhanced computed tomography enterography for the detection of ileocolonic Crohn’s disease. J Gastroenterol Hepatol 35(7):1136–1142. https://doi.org/10.1111/jgh.14945
Li X-H, Feng S-T, Cao Q-H, Coffey JC, Baker ME, Huang L, Mao R (2021) Degree of creeping fat assessed by computed tomography enterography is associated with intestinal fibrotic stricture in patients with Crohn’s disease: a potentially novel mesenteric creeping fat index. J Crohns Colitis 15(7):1161–1173. https://doi.org/10.1093/ecco-jcc/jjab005
Sakurai T, Katsuno T, Saito K, Yoshihama S, Nakagawa T, Koseki H, Yokosuka O (2017) Mesenteric findings of CT enterography are well correlated with the endoscopic severity of Crohn’s disease. Eur J Radiol 89:242–248. https://doi.org/10.1016/j.ejrad.2016,10(0),pp.22
Limberg B (1999) Diagnosis of chronic inflammatory bowel disease by ultrasonography. Z Gastroenterol 37(6):495–508
Serra C, Menozzi G, Labate AMM, Giangregorio F, Gionchetti P, Beltrami M, Cammarota T (2007) 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 62(1):114–121. https://doi.org/10.1016/j.ejrad.2006.11.027
Balthazar EJ (1991) CT of the gastrointestinal tract: principles and interpretation. Am J Roentgenol 156(1):23–32. https://doi.org/10.2214/ajr.156.1.1898566
Amitai MM, Raviv-Zilka L, Hertz M, Erlich Z, Konen E, Ben-Horin S, Apter S (2015) Main imaging features of Crohn’s disease: agreement between MR-enterography and CT-enterography. Isr Med Assoc J 17(5):293–297
Haber HP, Busch A, Ziebach R, Stern M (2000) Bowel wall thickness measured by ultrasound as a marker of Crohn’s disease activity in children. Lancet 355(9211):1239–1240. https://doi.org/10.1016/S0140-6736(00)02092-4
Novak KL, Kaplan GG, Panaccione R, Afshar EE, Tanyingoh D, Swain M, Wilson S (2017) A simple ultrasound score for the accurate detection of inflammatory activity in Crohn’s disease. Inflamm Bowel Dis 23(11):2001–2010. https://doi.org/10.1097/MIB.000000000001174
Liu C, Ding S-S, Zhang K, Liu L-N, Guo L-H, Sun L-P, Xu H-X (2020) Correlation between ultrasound consolidated score and simple endoscopic score for determining the activity of Crohn’s disease. Br J Radiol 93(1109):20190614. https://doi.org/10.1259/bjr.20190614
Rimola J, Ordás I, Rodriguez S, García-Bosch O, Aceituno M, Llach J, Panés J (2011) Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis 17(8):1759–1768. https://doi.org/10.1002/ibd.21551
Seo N, Park SH, Kim K-J, Kang B-K, Lee Y, Yang S-K, Ha HK (2016) MR enterography for the evaluation of small-bowel inflammation in Crohn disease by using diffusion-weighted imaging without intravenous contrast material: a prospective noninferiority study. Radiology 278(3):762–772. https://doi.org/10.1148/radiol.2015150809
Nylund K, Sævik F, Leh S, Pfeffer F, Hausken T, Gilja OH (2019) Interobserver analysis of CEUS-derived perfusion in fibrotic and inflammatory Crohn’s disease. Ultraschall In Der Medizin (Stuttgart, Germany: 1980) 40(1):76–84. https://doi.org/10.1055/s-0044-100492
Vogel J, da Luz MA, Baker M, Hammel J, Einstein D, Stocchi L, Fazio V (2007) CT enterography for Crohn’s disease: accurate preoperative diagnostic imaging. Dis Colon Rectum 50(11):1761–1769. https://doi.org/10.1007/s10350-007-9005-6
Mao R, Kurada S, Gordon IO, Baker ME, Gandhi N, McDonald C, Rieder F (2019) The mesenteric fat and intestinal muscle interface: creeping fat influencing stricture formation in Crohn’s disease. Inflamm Bowel Dis 25(3):421–426. https://doi.org/10.1093/ibd/izy331
Medellin-Kowalewski A, Wilkens R, Wilson A, Ruan J, Wilson SR (2016) Quantitative contrast-enhanced ultrasound parameters in Crohn disease: their role in disease activity determination with ultrasound. Am J Roentgenol 206(1):64–73. https://doi.org/10.2214/AJR.15.14506
Fletcher JG, Fidler JL, Bruining DH, Huprich JE (2011) New concepts in intestinal imaging for inflammatory bowel diseases. Gastroenterology 140(6):1795–1806. https://doi.org/10.1053/j.gastro.2011.02.013
Acknowledgements
This work was supported in part from the National Natural Science Foundation of China (Grant 82102048); Shanghai Municipal Health Commission (Grants 2019LJ21 and SHSLCZDZK03502), and the Science and Technology Commission of Shanghai Municipality (Grants 19DZ2251100, and 19441903200), and the Talent Project of Shanghai Tenth People's Hospital (Grant 2021SYPDRC067).
Funding
This work was supported in part from the National Natural Science Foundation of China (Grant 82102048); Shanghai Municipal Health Commission (Grants 2019LJ21 and SHSLCZDZK03502), and the Science and Technology Commission of Shanghai Municipality (Grants 19DZ2251100, and 19441903200), and the Talent Project of Shanghai Tenth People's Hospital (Grant 2021SYPDRC067).
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DSS, LC and XHX were involved in study design; LC, DSS and XXR contributed to patient recruitment, data collection, statistical analysis and data interpretation; DSS was involved in writing of the first draft of the paper; LC and XHX contributed to revision of the manuscript for important intellectual content; ZYF, SLP, LH, XLH, RWW, ZH, FY, SXM and ZK were involved in providing administrative, technical and material support; XHX and XXR contributed to supervising the study.
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Ding, SS., Liu, C., Zhang, YF. et al. Contrast-enhanced ultrasound in the assessment of Crohn’s disease activity: comparison with computed tomography enterography. Radiol med 127, 1068–1078 (2022). https://doi.org/10.1007/s11547-022-01535-z
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DOI: https://doi.org/10.1007/s11547-022-01535-z