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. 2024 Aug;312(2):e233039.
doi: 10.1148/radiol.233039.

Reliability of MR Enterography Features for Describing Fibrostenosing Crohn Disease

Affiliations

Reliability of MR Enterography Features for Describing Fibrostenosing Crohn Disease

Florian Rieder et al. Radiology. 2024 Aug.

Erratum in

  • Erratum for: Reliability of MR Enterography Features for Describing Fibrostenosing Crohn Disease.
    Rieder F, Baker ME, Bruining DH, Fidler JL, Ehman EC, Sheedy SP, Heiken JP, Ream JM, Holmes DR 3rd, Inoue A, Mohammadinejad P, Lee YS, Taylor SA, Stoker J, Zou G, Wang Z, Rémillard J, Carter RE, Ottichilo R, Atkinson N, Siddiqui MT, Sunkesula VC, Ma C, Parker CE, Panés J, Rimola J, Jairath V, Feagan BG, Fletcher JG; Stenosis Therapy and Anti-Fibrosis Research (STAR) Consortium. Rieder F, et al. Radiology. 2024 Oct;313(1):e249020. doi: 10.1148/radiol.249020. Radiology. 2024. PMID: 39470432 Free PMC article. No abstract available.

Abstract

Background Clinical decision making and drug development for fibrostenosing Crohn disease is constrained by a lack of imaging definitions, scoring conventions, and validated end points. Purpose To assess the reliability of MR enterography features to describe Crohn disease strictures and determine correlation with stricture severity. Materials and Methods A retrospective study of patients with symptomatic terminal ileal Crohn disease strictures who underwent MR enterography at tertiary care centers (Cleveland Clinic: September 2013 to November 2020; Mayo Clinic: February 2008 to March 2019) was conducted by using convenience sampling. In the development phase, blinded and trained radiologists independently evaluated 26 MR enterography features from baseline and follow-up examinations performed more than 6 months apart, with no bowel resection performed between examinations. Follow-up examinations closest to 12 months after baseline were selected. Reliability was assessed using the intraclass correlation coefficient (ICC). In the validation phase, after five features were redefined, reliability was re-estimated in an independent convenience sample using baseline examinations. Multivariable linear regression analysis identified features with at least moderate interrater reliability (ICC ≥0.41) that were independently associated with stricture severity. Results Ninety-nine (mean age, 40 years ± 14 [SD]; 50 male) patients were included in the development group and 51 (mean age, 45 years ± 16 [SD]; 35 female) patients were included in the validation group. In the development group, nine features had at least moderate interrater reliability. One additional feature demonstrated moderate reliability in the validation group. Stricture length (ICC = 0.85 [95% CI: 0.75, 0.91] and 0.91 [95% CI: 0.75, 0.96] in development and validation phase, respectively) and maximal associated small bowel dilation (ICC = 0.74 [95% CI: 0.63, 0.80] and 0.73 [95% CI: 0.58, 0.87] in development and validation group, respectively) had the highest interrater reliability. Stricture length, maximal stricture wall thickness, and maximal associated small bowel dilation were independently (regression coefficients, 0.09-3.97; P < .001) associated with stricture severity. Conclusion MR enterography definitions and scoring conventions for reliably assessing features of Crohn disease strictures were developed and validated, and feature correlation with stricture severity was determined. © RSNA, 2024 Supplemental material is available for this article. See also the article by Rieder and Ma et al in this issue. See also the editorial by Galgano and Summerlin in this issue.

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Conflict of interest statement

Disclosures of conflicts of interest: F.R. Consulting fees from Adiso Therapeutics, Adnovate, Agomab, Allergan, AbbVie, Arena Pharmaceuticals, AstraZeneca, Bausch & Lomb, Boehringer Ingelheim, Celgene/Bristol-Myers Squibb, Celltrion, Clinical Data Interchange Standards Consortium, Celsius Therapeutics, TD Cowen, Eugit, Ferring Pharmaceuticals, Galapagos, Galmed Pharmaceuticals, Genentech, Gilead, Gossamer Bio, Granite Bio, Guidepoint, Helmsley Charitable Trust, Horizon Therapeutics, Image Analysis Group, InDex Pharmaceuticals, Landos Biopharma, Janssen, Koutif Therapeutics, Mestag Therapeutics, Metacrine, Mirum Pharma, Mopac, Morphic Therapeutic, Myka Labs, Organovo, Origo Biopharma, Palisade Bio, Pfizer, Pliant Therapeutics, Prometheus Biosciences, Receptos, Redx Pharma, Roche, Samsung, Sanofi, Surmodics, Surrozen, Takeda Pharmaceuticals, TECHLAB, Teva Pharmaceuticals, Theravance Biopharma, Thetis Pharmaceuticals, Trlx Bio, UCB, Ysios Capital, and 89Bio, and participation on a data and safety monitoring board or advisory board for Allergan, AbbVie, Celgene, Gilead, Prometheus Biosciences, Receptos, Samsung, Takeda Pharmaceuticals, TECHLAB, Thetis Pharmaceuticals, and UCB. M.E.B. No relevant relationships. D.H.B. No relevant relationships. J.L.F. No relevant relationships. E.C.E. No relevant relationships. S.P.S. No relevant relationships. J.P.H. Grants or contracts from RadMD for clinical trial reads. J.M.R. No relevant relationships. D.R.H. No relevant relationships. A.I. No relevant relationships. P.M. No relevant relationships. Y.S.L. No relevant relationships. S.A.T. Institution received a grant from Takeda Pharmaceuticals, consulting fees from AstraZeneca, chair of NIHR imaging group, stock or stock options from Motilent. J.S. Member of Radiology editorial board. G.Z. No relevant relationships. Z.W. No relevant relationships. J. Rémillard No relevant relationships. R.E.C. No relevant relationships. R.O. No relevant relationships. N.A. No relevant relationships. M.T.S. No relevant relationships. V.C.S Patents planned, issued or pending from MetroHealth Medical Center. C.M. Grants or contracts to institution from AbbVie, Eli Lilly, Ferring Pharmaceuticals, and Pfizer; royalties or licenses from Springer Publishing; consulting fees from AbbVie, Alimentiv, Amgen, AVIR Pharma, Bristol-Myers Squibb, Celltrion, Eli Lilly, Ferring Pharmaceuticals, Fresenius Kabi, Janssen, McKesson, Mylan, Pendopharm, Pfizer, Prometheus Biosciences, Roche, Sanofi, Takeda Pharmaceuticals, and Tillotts Pharma; and payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing, or educational events from AbbVie, Amgen, AVIR Pharma, Alimentiv, Bristol-Myers Squibb, Eli Lilly, Ferring Pharmaceuticals, Fresenius Kabi, Janssen, Organon, Pendopharm, Pfizer, Sanofi, Takeda Pharmaceuticals, and Tillotts Pharma. C.E.P. Employee of Alimentiv. J.P. Consulting fees from AbbVie, Alimentiv, Athos Therapeutics, Atomwise, Boehringer Ingelheim, Celsius Therapeutics, Ferring Pharmaceuticals, Galapagos, Genentech/Roche, GlaxoSmithKline, Janssen, Mirum Pharma, Nimbus Therapeutics, Pfizer, Progenity, Prometheus Biosciences, Protagonist Therapeutics, Revolo Biotherapeutics, Takeda Pharmaceuticals, and Wasserman; and participation on a data and safety monitoring board or advisory board for Sanofi, Sorriso Pharmaceuticals, and Surrozen. J. Rimola Grants or contracts from AbbVie; consulting fees from Janssen, Alimentiv, and Ferring Pharmaceuticals; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing, or educational events from Takeda Pharmaceuticals and Janssen; and participation on a data and safety monitoring board or advisory board for Janssen, Agomab Therapeutics, and Boehringer Ingelheim. V.J. Consulting fees from AbbVie, Alimentiv, Arena Pharmaceuticals, Asahi Kasei Pharma, Asieris Pharmaceuticals, AstraZeneca, Avoro Capital, Bristol-Myers Squibb, Celltrion, Eli Lilly, Endpoint Health, Enthera, Ferring Pharmaceuticals, Flagship Pioneering, Fresenius Kabi, Galapagos, Gilde Healthcare, GlaxoSmithKline, Genentech, Gilead, Innomar Strategie, JAMP Pharma, Janssen, Merck, Metacrine, Mylan, Pandion, Pendopharm, Pfizer, Protagonist Therapeutics, Prometheus Biosciences, Reistone Biopharma, Roche, Roivant, Sandoz, Second Genome, Sorriso Pharmaceuticals, Synedgen, Takeda Pharmaceuticals, TD Securities, Teva Pharmaceuticals, TopiVert, Ventyx Biosciences, and Vividion Therapeutics; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing, or educational events from AbbVie, Ferring, Bristol-Myers Squibb, Galapagos, Janssen/Pfizer/Shire, Takeda Pharmaceuticals, and Fresenius Kabi. B.G.F. Consulting fees from AbbVie, Agomab Therapeutics, AllianThera Biopharma, Amgen, AnaptysBio, Applied Molecular Transport, Arena Pharmaceuticals, Azora Therapeutics, BIOJAMP, Biora Therapeutics, Boehringer Ingelheim, Boston Pharmaceuticals, Boxer, Celgene/Bristol-Myers Squibb, Connect Biopharma, Cytoki Pharma, Disc Medicine, Duality Biologics, EcoR1 Capital, Everest Clinical Research, Eli Lilly, Equillium, Ermium Therapeutics, Ferring Pharmaceuticals, FirstWave BioPharma, Galapagos, Galen/Atlantica, Genentech/Roche, Gilead, Glenmark Pharmaceuticals, Gossamer Bio, GlaxoSmithKline, Hoffmann-LaRoche, Hot Spot Therapeutics, InDex Pharmaceuticals, Imhotex, ImmuNext, Immunic Therapeutics, Intact Therapeutics, JAK Academy, Janssen, Japan Tobacco, Kaleido Biosciences, Landos Biopharma, Leadiant Biosciences, LifeSci Capital, Lument, Merck/Millennium, MiroBio, Morphic Therapeutic, Mylan, OM Pharma, Origo Biopharma, Orphagen Pharmaceuticals, Otsuka, Pandion Therapeutics, Pfizer, Prometheus Biosciences, PlayToKnow, Progenity, Protagonist Therapeutics, PTM Therapeutics, Q32 Bio, Rebiotix, RedHill Biopharma, Redx Pharma, Roche, Sandoz, Sanofi, Seres Therapeutics, Silverback Therapeutics, Surrozen, Takeda Pharmaceuticals, Teva Pharmaceuticals, Thelium, Theravance Biopharma, TiGenix, Tillotts Pharma, UCB Pharma, VHsquared, Viatris, and Zealand Pharma; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing, or educational events from AbbVie, Takeda Pharmaceuticals, Janssen, Pfizer, Eli Lilly, Sanofi, and Tillotts Pharma; support for attending meetings and/or for travel from Takeda Pharmaceuticals, AbbVie, Eli Lilly, Pfizer, Janssen, Bristol-Myers Squibb, and Sanofi; and scientific advisory board member for AbbVie, Amgen, Boehringer Ingelheim, Celgene/Bristol-Myers Squibb, Genentech/Roche, Janssen, Novartis, Origo Biopharma, Pfizer, Prometheus Biosciences, Takeda Pharmaceuticals, Tillotts Pharma, Teva Pharmaceuticals, Progenity, InDex Pharmaceuticals, EcoR1 Capital, Morphic Therapeutic, and GlaxoSmithKline. J.G.F. Grants or contracts to institution from the Helmsley Charitable Trust, Siemens Healthineers, Alimentiv, Pfizer, Takeda Pharmaceuticals, and Medtronic; consulting fees to institution from Alimentiv, Genentech, Boehringer Ingelheim, GlaxoSmithKline, Janssen, Medtronic, Redx Pharma, and Takeda Pharmaceuticals; and president of the Society of Abdominal Radiology (2021–2022).

Figures

None
Graphical abstract
Flowchart of selection of the development group. The development phase
included baseline and follow-up MR enterography examinations from 100
patients with Crohn disease who had symptomatic terminal ileal strictures.
IPAA = ileal pouch-anal anastomosis, TI = terminal ileum. 1Stricture was
defined by the inclusion criteria (3-cm maximal associated small bowel
dilation or the inability of a colonoscope to pass). 2As part of the
consensus review process, 108 potential MR enterography examinations were
re-reviewed by two senior radiologists at their respective institutions to
ensure that there was no potential adhesive disease, prior strictureplasty,
and/or image quality issues. If issues were identified by the respective
central readers, the examination was excluded. Eight patients were
ultimately excluded. 3Strictureplasty change proximal to neo-TI stricture
interfered with measurement of proximal dilation (as detected by central
readers and confirmed by senior radiologists not participating in the
imaging interpretation). 4One patient was excluded during independent
assessment (most distal stricture measured at baseline and follow-up was not
the same stricture).
Figure 1:
Flowchart of selection of the development group. The development phase included baseline and follow-up MR enterography examinations from 100 patients with Crohn disease who had symptomatic terminal ileal strictures. IPAA = ileal pouch-anal anastomosis, TI = terminal ileum. 1Stricture was defined by the inclusion criteria (3-cm maximal associated small bowel dilation or the inability of a colonoscope to pass). 2As part of the consensus review process, 108 potential MR enterography examinations were re-reviewed by two senior radiologists at their respective institutions to ensure that there was no potential adhesive disease, prior strictureplasty, and/or image quality issues. If issues were identified by the respective central readers, the examination was excluded. Eight patients were ultimately excluded. 3Strictureplasty change proximal to neo-TI stricture interfered with measurement of proximal dilation (as detected by central readers and confirmed by senior radiologists not participating in the imaging interpretation). 4One patient was excluded during independent assessment (most distal stricture measured at baseline and follow-up was not the same stricture).
Baseline MR enterography images in a 26-year-old male patient depict a
long-segment naive stricture with marked inflammation and multiple areas of
narrowing. Top row: Stricture length measurements made in the development
phase by each central reader. The dotted lines indicate three-dimensional
spline tool annotations, which are superimposed onto the two-dimensional
image and correspond to the location of the stricture lumen on images that
are outside of the imaging plane. Central readers created markings along the
lumen of the stricture from the proximal to the distal end. Bottom row:
Maximal associated small bowel dilation measurements made in the development
phase by each central reader.
Figure 2:
Baseline MR enterography images in a 26-year-old male patient depict a long-segment naive stricture with marked inflammation and multiple areas of narrowing. Top row: Stricture length measurements made in the development phase by each central reader. The dotted lines indicate three-dimensional spline tool annotations, which are superimposed onto the two-dimensional image and correspond to the location of the stricture lumen on images that are outside of the imaging plane. Central readers created markings along the lumen of the stricture from the proximal to the distal end. Bottom row: Maximal associated small bowel dilation measurements made in the development phase by each central reader.
Baseline MR enterography images in a 39-year-old female patient with a
short naive stricture with inflammation involving the ileocecal valve and
terminal ileum. Left, top and bottom: Coronal true fast imaging with
steady-state precession images with fat saturation. Arrows point to a single
stricture that was assessed by all four central readers. Top row:
Variability in pulse sequences selected for length measurements and
annotations from each of the four central readers in the development phase.
Bottom row: Variability in pulse sequences selected for maximum small bowel
dilation measurements and annotations from each of the four central readers.
Stricture length, maximal associated small bowel dilation, and visual analog
scale (VAS) evaluations made by each central reader are presented below the
annotations. Stricture severity was rated with a VAS using a 100-mm
continuous horizontal line that ranged from 0 (completely normal) to 100
(worst disease ever seen). Max = maximum.
Figure 3:
Baseline MR enterography images in a 39-year-old female patient with a short naive stricture with inflammation involving the ileocecal valve and terminal ileum. Left, top and bottom: Coronal true fast imaging with steady-state precession images with fat saturation. Arrows point to a single stricture that was assessed by all four central readers. Top row: Variability in pulse sequences selected for length measurements and annotations from each of the four central readers in the development phase. Bottom row: Variability in pulse sequences selected for maximum small bowel dilation measurements and annotations from each of the four central readers. Stricture length, maximal associated small bowel dilation, and visual analog scale (VAS) evaluations made by each central reader are presented below the annotations. Stricture severity was rated with a VAS using a 100-mm continuous horizontal line that ranged from 0 (completely normal) to 100 (worst disease ever seen). Max = maximum.
Central reader interpretations of four MR enterography features in the
development phase using select images obtained in a 26-year-old male
patient. (A) Coronal diffusion-weighted image. (B) Coronal fat-saturated
postgadolinium image. (C) Coronal true fast imaging with steady-state
precession and coronal single-shot fast spin-echo (inset) images. Arrows
point to sacculation. (D) Coronal single-shot fast spin-echo image with fat
saturation.
Figure 4:
Central reader interpretations of four MR enterography features in the development phase using select images obtained in a 26-year-old male patient. (A) Coronal diffusion-weighted image. (B) Coronal fat-saturated postgadolinium image. (C) Coronal true fast imaging with steady-state precession and coronal single-shot fast spin-echo (inset) images. Arrows point to sacculation. (D) Coronal single-shot fast spin-echo image with fat saturation.
Graphs of central reader measurements for (A) stricture length, (B)
maximal associated small bowel dilation, (C) maximal stricture wall
thickness, and (D) maximal luminal diameter for each patient in the
development phase. Black dots indicate the mean measurement value for each
patient. For each variable, patient values are displayed from the smallest
to largest. The dotted horizontal line in A indicates a stricture length of
5.0 cm. The dotted horizontal line in B indicates maximum small bowel
dilation of 3.0 cm. Note that measurement variability in maximal associated
small bowel dilation remains relatively constant.
Figure 5:
Graphs of central reader measurements for (A) stricture length, (B) maximal associated small bowel dilation, (C) maximal stricture wall thickness, and (D) maximal luminal diameter for each patient in the development phase. Black dots indicate the mean measurement value for each patient. For each variable, patient values are displayed from the smallest to largest. The dotted horizontal line in A indicates a stricture length of 5.0 cm. The dotted horizontal line in B indicates maximum small bowel dilation of 3.0 cm. Note that measurement variability in maximal associated small bowel dilation remains relatively constant.
Coronal single-shot fast spin-echo and postgadolinium images
demonstrate the proximal, mid, and distal aspects of a naive stricture at MR
enterography performed in a 71-year-old female patient. There is a long
inflammatory stricture with multifocal areas of luminal narrowing and
intervening areas of active inflammation involving the terminal ileum. The
four central readers measured this stricture as being 70.1, 69.8, 71.7, and
71.6 cm in length. The visual analog scale estimate of the stricture
severity was rated by the central readers as 65, 90, 80, and 75. The arrows
point to a single stricture that was assessed by all readers. Colored dots
in the left-most and right-most images are reader markings along the lumen
of the stricture. Postgadolinium images are the middle images.
Figure 6:
Coronal single-shot fast spin-echo and postgadolinium images demonstrate the proximal, mid, and distal aspects of a naive stricture at MR enterography performed in a 71-year-old female patient. There is a long inflammatory stricture with multifocal areas of luminal narrowing and intervening areas of active inflammation involving the terminal ileum. The four central readers measured this stricture as being 70.1, 69.8, 71.7, and 71.6 cm in length. The visual analog scale estimate of the stricture severity was rated by the central readers as 65, 90, 80, and 75. The arrows point to a single stricture that was assessed by all readers. Colored dots in the left-most and right-most images are reader markings along the lumen of the stricture. Postgadolinium images are the middle images.

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