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Intestinal Conventional Ultrasonography, Contrast-Enhanced Ultrasonography and Magnetic Resonance Enterography in Assessment of Crohn’s Disease Activity: A Comparison with Surgical Histopathology Analysis

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Abstract

Background and Aims

Contrast-enhanced ultrasonography (CEUS) is a potential interesting method for assessing accurately Crohn’s disease (CD) activity. We compared the value of intestinal ultrasonography (US) coupled with contrast agent injection with that of magnetic resonance enterography (MRE) in the assessment of small bowel CD activity using surgical histopathology analysis as reference.

Methods

Seventeen clinically active CD patients (14 women, mean age 33 years) requiring an ileal or ileocolonic resection were prospectively enrolled. All performed a MRE and a US coupled with contrast agent injection (CEUS) less than 8 weeks prior to surgery. Various imaging qualitative and quantitative parameters were recorded and their respective performance to detect disease activity, disease extension and presence of complications was compared to surgical histopathological analysis.

Results

The median wall thickness measured by US differed significantly between patients with non-severely active CD (n = 5) and those with severely active CD (n = 12) [7.0 mm, IQR (6.5–9.5) vs 10.0 mm, IQR (8.0–12.0), respectively; p = 0.03]. A non-significant trend was found with MRE with a median wall thickness in severe active CD of 10.0 mm, IQR (8.0–13.7) compared with 8.0 mm, IQR (7.5–10.5) in non-severely active CD (p = 0.07). The area under the ROC curve (AUROC) of the wall thickness assessed by US and MRE to identify patients with or without severely active CD on surgical specimens were 0.85, 95% CI (0.64–1.04), p = 0.03 and 0.80, 95% CI (0.56–1.01), p = 0.07, respectively. Among the parameters derived from the time-intensity curve during CEUS, time to peak and rise time were the two most accurate markers [AUROC = 0.88, 95% CI (0.70–1.04), p = 0.02 and 0.86, 95% CI (0.68–1.04), p = 0.03] to detect patients with severely active CD assessed on surgical specimens.

Conclusion

The accuracy of intestinal CEUS is close to that of conventional US to detect disease activity. A thickened bowel and shortened time to peak and rise time were the most accurate to identify CD patients with severe histological disease activity.

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Abbreviations

CEUS:

Contrast-enhanced ultrasonography

MRE:

Magnetic resonance enterography

CD:

Crohn’s disease

CRP:

C-reactive protein

AUROC:

Area under the receiver operating characteristic curve

ROC:

Receiver operating characteristic

SB:

Small bowel

CT:

Computed tomography

US:

Ultrasonography

HBI:

Harvey-Bradshaw Index

SD:

Standard deviation

Min:

Minutes

Sec:

Seconds

A.U.:

Arbitrary unit

I.V.:

Intravenous

ROI:

Region of interest

Sen:

Sensitivity

IQR:

Interquartile range

Spe:

Specificity

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Authors and Affiliations

  1. Department of Gastroenterology, Lyon-Sud Hospital, Hospices Civils de Lyon, 165 Chemin du Grand Revoyet, 69495, Pierre-Bénite, France

    L. Servais, G. Boschetti, C. Meunier, C. Gay, M. Chauvenet, A. L. Charlois, B. Flourié & S. Nancey

  2. INSERM U1111, International Center for Research in Infectiology, Lyon, France

    G. Boschetti, C. Meunier, A. Rozieres, B. Flourié & S. Nancey

  3. Department of Digestive Surgery, Lyon-Sud Hospital, Hospices Civils de Lyon, Pierre-Bénite, France

    E. Cotte & Y. François

  4. Department of Pathology, Lyon-Sud Hospital, Hospices Civils de Lyon, Pierre-Bénite, France

    J. Fontaine, S. Isaac & A. Traverse-Glehen

  5. Department of Radiology, Lyon-Sud Hospital, Hospices Civils de Lyon, Pierre-Bénite, France

    L. Cuminal & P. J. Valette

  6. Department of Gastroenterology, CHU Saint-Etienne, Saint-Etienne, France

    X. Roblin

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  1. L. Servais
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Corresponding author

Correspondence to S. Nancey.

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Conflict of interest

Laure Servais: None. Gilles Boschetti: consulting fees from Merck, Abbvie, Takeda, Janssen Cilag, Hospira, Takeda. Camille Meunier: None. Claire Gay: None. Eddy Cotte: consulting fees from Takeda, Abbvie. Yves François: None. Aurore Rozieres: None; Juliette Fontaine: None. Lydie Cuminal: None. Marion Chauvenet: None. Anne-Laure Charlois: None. Sylvie Isaac: None. Alexandra Traverse-Glehen: None. Xavier Roblin served as a speaker, a consultant and/or an advisory board member for MSD, Pfizer, Janssen, Takeda, Abbvie, Amgen, Biogen, Gilead, Roche, Gilead, Theradiag. Bernard Flourié served as a speaker, a consultant and/or an advisory board member for MSD, Abbvie, Ferring, Norgine, Biocodex. Pierre-Jean Valette: None. Stéphane Nancey served as a speaker, a consultant and/or an advisory board member for Merck, Abbvie, Takeda, Ferring, Norgine, Vifor Pharma, Novartis, Janssen Cilag, Hospira, Takeda and HAC-Pharma.

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10620_2021_7074_MOESM1_ESM.jpg

Various quantitative perfusion parameters from the modeled time-intensity curve from the Vuebox analysis of CEUS. Peak enhancement: maximum intensity of the time-intensity curve; rise time: time from arrival of contrast to the peak enhancement; wash-in area under the curve: area under the time-intensity curve from the time of first contrast uptake to the peak enhancement; wash-out area under the curve: area under the time-intensity curve from the peak enhancement to the end of the curve; fall time: time from the peak enhancement to a point at the x-axis where the minimum slope tangent crosses (JPG 42 kb)

10620_2021_7074_MOESM2_ESM.jpg

Representative intensity of contrast enhancement (top), respectively in inactive and active CD assessed by CEUS. Representative time-intensity curves (down) in inactive, moderately and severely active CD by CEUS (JPG 75 kb)

10620_2021_7074_MOESM3_ESM.jpg

Representative wall thickness and intensity of contrast enhancement, respectively in non-severely active (A and B) and severely active (C and D) CD assessed by MRE (JPG 98 kb)

10620_2021_7074_MOESM4_ESM.jpg

Representative small bowel pathologic section analysis in inactive CD (grade 0 of inflammatory score) (A), in inactive CD with transmural fibrosis (grade 2 of fibrosis score) (B), in severely active CD (grade 2 of inflammatory score) with transmural fibrosis (grade 2 of fibrosis score) complicated by fistula (C) and in moderately active CD (grade 1 of inflammatory score) with superficial ulceration and minimal fibrosis limited to submucosa (grade 0 of fibrosis score) (D). Hematoxylin-phloxin-saffron (HPS) staining and magnification X 20 (JPG 115 kb)

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Servais, L., Boschetti, G., Meunier, C. et al. Intestinal Conventional Ultrasonography, Contrast-Enhanced Ultrasonography and Magnetic Resonance Enterography in Assessment of Crohn’s Disease Activity: A Comparison with Surgical Histopathology Analysis. Dig Dis Sci 67, 2492–2502 (2022). https://doi.org/10.1007/s10620-021-07074-3

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