Skip to main content

Advertisement

Log in

MRI texture analysis of T2-weighted images is preferred over magnetization transfer imaging for readily longitudinal quantification of gut fibrosis

  • Gastrointestinal
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To investigate the value of magnetization transfer (MT) MRI and texture analysis (TA) of T2-weighted MR images (T2WI) in the assessment of intestinal fibrosis in a mouse model.

Methods

Chronic colitis was induced in mice by cyclic administration of dextran sodium sulphate (DSS) resulting in chronic inflammation and progressive bowel fibrosis. Mice underwent 7-T MR imaging at various time points. Bowel wall MT ratio (MTR) and textural features (skewness, kurtosis, entropy), extracted by a filtration histogram technique, were correlated with histopathology. Performance of both techniques were validated using antifibrotic therapy. Finally, a retrospective study was conducted in five patients with Crohn’s disease (CD) who underwent bowel surgery.

Results

MTR and texture entropy correlated with histopathological fibrosis (r = .85 and .81, respectively). Entropy was superior to MTR for monitoring bowel fibrosis in the presence of coexisting inflammation (linear regression R2 = .93 versus R2 = .01). Furthermore, texture entropy was able to assess antifibrotic therapy response (placebo mice versus treated mice at endpoint scan; Δmean = 0.128, p < .0001). An increase in entropy was indicative of fibrosis accumulation in human CD strictures (inflammation: 1.29; mixed strictures: 1.4 and 1.48; fibrosis: 1.73 and 1.9).

Conclusion

MT imaging and TA of T2WI can both noninvasively detect established intestinal fibrosis in a mouse model. However, TA is especially useful for the longitudinal quantification of fibrosis in mixed inflammatory-fibrotic tissue, as well as for antifibrotic treatment response evaluation. This accessible post-processing technique merits further validation as the benefits for clinical practice as well as antifibrotic trial design would be numerous.

Key Points

• Magnetization transfer MRI and texture analysis of T2-weighted MR images can detect established bowel fibrosis in an animal model of gut fibrosis.

• Texture entropy is able to identify and monitor bowel fibrosis progression in an inflammatory context and can assess the response to antifibrotic treatment.

• A proof-of-concept study in five patients with Crohn’s disease suggests that texture entropy can detect and grade fibrosis in human intestinal strictures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CD:

Crohn’s disease

DAI:

Disease Activity Index

DSS:

Dextran sulfate sodium

IncrEn:

Incremental entropy

MRE:

MR enterography

MT:

Magnetization transfer

MTR:

Magnetization transfer ratio

NormEn:

Normalized entropy

T2WI:

T2-weighted images

TA:

Texture analysis

TI:

Terminal ileum

References

  1. Zhong YK, Lu BL, Huang SY et al (2020) Cross-sectional imaging for assessing intestinal fibrosis in Crohn’s disease. J Dig Dis 21(6):342–350

    Article  PubMed  Google Scholar 

  2. Higgins PD (2017) Measurement of fibrosis in Crohn’s disease strictures with imaging and blood biomarkers to inform clinical decisions. Dig Dis 35(1–2):32–37

    Article  PubMed  Google Scholar 

  3. Rieder F, Latella G, Magro F et al (2016) European Crohn’s and Colitis Organisation topical review on prediction, diagnosis and management of fibrostenosing Crohn’s disease. J Crohns Colitis 10(8):873–885

    Article  PubMed  Google Scholar 

  4. Bettenworth D, Bokemeyer A, Baker M et al (2019) Assessment of Crohn’s disease-associated small bowel strictures and fibrosis on cross-sectional imaging: a systematic review. Gut 68(6):1115–1126

    Article  CAS  PubMed  Google Scholar 

  5. Maaser C, Sturm A, Vavricka SR et al (2019) ECCO-ESGAR guideline for diagnostic assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis 13(2):144–164

    Article  PubMed  Google Scholar 

  6. Rimola J, Planell N, Rodriguez S et al (2015) Characterization of inflammation and fibrosis in Crohn’s disease lesions by magnetic resonance imaging. Am J Gastroenterol 110(3):432–440

    Article  PubMed  Google Scholar 

  7. Adler J, Swanson SD, Schmiedlin-Ren P et al (2011) Magnetization transfer helps detect intestinal fibrosis in an animal model of Crohn disease. Radiology 259(1):127–135

    Article  PubMed  PubMed Central  Google Scholar 

  8. Pazahr S, Blume I, Frei P et al (2013) Magnetization transfer for the assessment of bowel fibrosis in patients with Crohn’s disease: initial experience. MAGMA 26(3):291–301

    Article  CAS  PubMed  Google Scholar 

  9. Adler J, Rahal K, Swanson SD et al (2013) Anti-tumor necrosis factor alpha prevents bowel fibrosis assessed by messenger RNA, histology, and magnetization transfer MRI in rats with Crohn’s disease. Inflamm Bowel Dis 19(4):683–690

    Article  PubMed  Google Scholar 

  10. Dillman JR, Swanson SD, Johnson LA et al (2015) Comparison of noncontrast MRI magnetization transfer and T2 -weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model. J Magn Reson Imaging 42(3):801–810

    Article  PubMed  Google Scholar 

  11. Li XH, Mao R, Huang SY et al (2018) Characterization of degree of intestinal fibrosis in patients with Crohn disease by using magnetization transfer MR imaging. Radiology 287(2):494–503

    Article  PubMed  Google Scholar 

  12. Meng J, Huang S, Sun C et al (2020) Comparison of three magnetization transfer ratio parameters for assessment of intestinal fibrosis in patients with Crohn’s disease. Korean J Radiol 21(3):290–297

    Google Scholar 

  13. Fang ZN, Li XH, Lin JJ et al (2020) Magnetisation transfer imaging adds information to conventional MRIs to differentiate inflammatory from fibrotic components of small intestinal strictures in Crohn’s disease. Eur Radiol 30(4):1938–1947

    Article  PubMed  PubMed Central  Google Scholar 

  14. Makanyanga J, Ganeshan B, Rodriguez-Justo M et al (2017) MRI texture analysis (MRTA) of T2-weighted images in Crohn’s disease may provide information on histological and MRI disease activity in patients undergoing ileal resection. Eur Radiol 27(2):589–597

    Article  PubMed  Google Scholar 

  15. Bhatnagar G, Makanyanga J, Ganeshan B et al (2016) MRI texture analysis parameters of contrast-enhanced T1-weighted images of Crohn’s disease differ according to the presence or absence of histological markers of hypoxia and angiogenesis. Abdom Radiol (NY) 41(7):1261–1269

    Article  Google Scholar 

  16. Tabari A, Kilcoyne A, Jeck WR, Mino-Kenudson M, Gee MS (2019) Texture analysis of magnetic resonance enterography contrast enhancement can detect fibrosis in Crohn disease strictures. J Pediatr Gastroenterol Nutr 69(5):533–538

    Article  PubMed  Google Scholar 

  17. Miles KA, Ganeshan B, Hayball MP (2013) CT texture analysis using the filtration-histogram method: what do the measurements mean? Cancer Imaging 13(3):400–406

    Article  PubMed  PubMed Central  Google Scholar 

  18. Goh V, Ganeshan B, Nathan P, Juttla JK, Vinayan A, Miles KA (2011) Assessment of response to tyrosine kinase inhibitors in metastatic renal cell cancer: CT texture as a predictive biomarker. Radiology 261(1):165–171

    Article  PubMed  Google Scholar 

  19. Ng F, Ganeshan B, Kozarski R, Miles KA, Goh V (2013) Assessment of primary colorectal cancer heterogeneity by using whole-tumor texture analysis: contrast-enhanced CT texture as a biomarker of 5-year survival. Radiology 266(1):177–184

    Article  PubMed  Google Scholar 

  20. Rieder F, Fiocchi C, Rogler G (2017) Mechanisms, management, and treatment of fibrosis in patients with inflammatory bowel diseases. Gastroenterology 152(2):340–50 e6

    Article  PubMed  Google Scholar 

  21. Jairath V, Levesque BG, Vande Casteele N et al (2017) Evolving concepts in phases I and II drug development for Crohn’s disease. J Crohns Colitis 11(2):246–255

    Article  PubMed  Google Scholar 

  22. Van Welden S, De Vos M, Wielockx B et al (2017) Haematopoietic prolyl hydroxylase-1 deficiency promotes M2 macrophage polarization and is both necessary and sufficient to protect against experimental colitis. J Pathol 241(4):547–558

    Article  PubMed  Google Scholar 

  23. Holvoet T, Devriese S, Castermans K et al (2017) Treatment of intestinal fibrosis in experimental inflammatory bowel disease by the pleiotropic actions of a local Rho kinase inhibitor. Gastroenterology 153(4):1054–1067

    Article  CAS  PubMed  Google Scholar 

  24. Kanda T, Nakai Y, Oba H, Toyoda K, Kitajima K, Furui S (2016) Gadolinium deposition in the brain. Magn Reson Imaging 34(10):1346–1350

    Article  CAS  PubMed  Google Scholar 

  25. Li XH, Sun CH, Mao R et al (2015) Assessment of activity of Crohn disease by diffusion-weighted magnetic resonance imaging. Medicine (Baltimore) 94(43):e1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wilkens R, Hagemann-Madsen RH, Peters DA et al (2018) 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 12(1):48–56

    Article  PubMed  Google Scholar 

  27. Catalano OA, Gee MS, Nicolai E et al (2016) Evaluation of quantitative PET/MR enterography biomarkers for discrimination of inflammatory strictures from fibrotic strictures in Crohn disease. Radiology 278(3):792–800

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The antifibrotic compound (REDX08397) that was used in this study was provided by Redx Pharma Plc.

Statistical analyses were performed by Dr Ellen Deschepper (Biostatistics Unit, Ghent University, Ghent, Belgium).

Histopathologic evaluation was co-executed by professor emeritus Dr Karel Geboes (University Hospital KULeuven, Leuven, Belgium).

Figures were partially created with BioRender.

Funding

This study was supported by research grants from the Department of Radiology and Medical Imaging, Ghent University Hospital, Ghent, Belgium. Sophie Van Welden is supported by a fellowship from Ghent University, Ghent, Belgium [BOF20/PDO/047].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Debby Laukens.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Prof Dr Debby Laukens.

Conflict of interest

Peter Bunyard is an employee of Redx Pharma Plc but had no control of the data nor control of information that might present a conflict of interest. The other authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

Dr Ellen Deschepper provided statistical advice for this manuscript and performed statistical analyses.

One of the authors, Simon Bos, has significant statistical expertise.

Informed consent

Written informed consent was waived because of the retrospective nature of the proof-of-concept study.

Ethical approval

The proof-of-concept study was approved by the Ethics Committee of Ghent University Hospital (EC/2018/1493, Belgian study registration number B670201838339). Approval from the institutional animal care committee was obtained.

Methodology

•Animal study: prospective; human proof-of-concept study: retrospective

•Experimental

•Performed at one institution

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Isabelle De Kock and Simon Bos share equal first authorship contribution.

Geert Villeirs and Debby Laukens share equal senior authorship contribution.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 845 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De Kock, I., Bos, S., Delrue, L. et al. MRI texture analysis of T2-weighted images is preferred over magnetization transfer imaging for readily longitudinal quantification of gut fibrosis. Eur Radiol 33, 5943–5952 (2023). https://doi.org/10.1007/s00330-023-09624-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-023-09624-x

Keywords

Navigation