Lo RW, Bhatnagar G, Kutaiba N, Srinivasan AR. Evaluating luminal and post-operative Crohn’s disease activity on magnetic resonance enterography: A review of radiological disease activity scores. World J Gastroenterol 2025; 31(26): 107419 [DOI: 10.3748/wjg.v31.i26.107419]
Corresponding Author of This Article
Ashish R Srinivasan, Associate Professor, Department of Gastroenterology and Hepatology, Eastern Health, 8 Arnold St, Melbourne 3128, Victoria, Australia. ashish.srinivasan@monash.edu
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Review
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Author contributions: Srinivasan AR contributed to the study concept, design and supervision; Lo RW, Srinivasan AR contributed to the drafting of the manuscript; Bhatnagar G, Kutaiba N, Srinivasan AR contributed to the critical review of the manuscript; All authors approved the submitted manuscript.
Conflict-of-interest statement: Bhatnagar G has served as a consultant for Alimentiv, is an employee of Motilent; Owns stocks and shares in Motilent; and owns patent in P295276.US.02, system to characterise topology and morphology of fistulae from medical imaging data; Srinivasan AR has served as a speaker for Sandoz and Arrowtex Pharmaceuticals, and received advisory fees from Abbvie, Amgen, Arrotex Pharmaceuticals, Pfizer, Takeda Pharmaceuticals, and Dr Falk Pharmaceuticals; The remaining authors have no disclosures.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Ashish R Srinivasan, Associate Professor, Department of Gastroenterology and Hepatology, Eastern Health, 8 Arnold St, Melbourne 3128, Victoria, Australia. ashish.srinivasan@monash.edu
Received: March 24, 2025 Revised: April 30, 2025 Accepted: June 25, 2025 Published online: July 14, 2025 Processing time: 110 Days and 18 Hours
Abstract
Magnetic resonance enterography (MRE) is a non-invasive, radiation-free imaging modality that facilitates the assessment of transmural Crohn’s disease activity. It offers advantages over ileo-colonoscopy, which is limited to mucosal-level evaluation, cannot routinely assess small bowel segments proximal to the terminal ileum, and is unable to detect extra-luminal complications. Despite these advantages, the lack of standardised criteria for defining and appraising radiologic disease activity on MRE has contributed to variability in interpretation and clinical application. In response, multiple MRE-based scoring systems have been developed to quantify radiological Crohn’s disease activity in both luminal and post-operative settings. Radiological disease activity scores specific to luminal Crohn’s disease include the magnetic resonance index of activity (MaRIA), simplified MaRIA, Nancy score, London score, Crohn’s disease magnetic resonance imaging (MRI) index, Clermont score, paediatric inflammatory Crohn’s MRE index, MRE global score, MRE index, and modified Clermont score. The MR score and the MRI in Crohn’s disease to predict postoperative recurrence index have been specifically developed to evaluate post-operative disease recurrence in Crohn’s disease. Nevertheless, heterogeneity in scoring parameters, variability in computational complexity, and a lack of consensus regarding optimal score selection, have impeded widespread clinical adoption of radiological disease activity scores. This narrative review aims to summarise the key imaging features of luminal Crohn’s disease, explore their integration into existing MRE scoring indices, and critically compare the structure, strengths, and clinical applicability of each. Furthermore, MRI scores specific to post-operative Crohn’s disease evaluation, and the assessment of cumulative bowel wall damage using the Lemann index will also be discussed.
Core Tip: Magnetic resonance enterography (MRE) offers a non-invasive, radiation-free method of evaluating transmural disease activity and extra-enteric complications of Crohn’s disease. As the role of imaging grows in monitoring Crohn’s disease activity and therapy response, standardised and validated scoring systems are essential. Several MRE-based indices have been developed to quantify radiological Crohn’s disease activity reliably. These tools aim to mirror the role of endoscopic scores by providing reproducible and clinically relevant assessments of Crohn’s disease activity. Integrating these scores into clinical practice and future research promises to enhance objective disease evaluation and support more tailored, evidence-based management of Crohn’s disease.
Citation: Lo RW, Bhatnagar G, Kutaiba N, Srinivasan AR. Evaluating luminal and post-operative Crohn’s disease activity on magnetic resonance enterography: A review of radiological disease activity scores. World J Gastroenterol 2025; 31(26): 107419
Endoscopic remission has been endorsed by the selecting therapeutic targets in inflammatory bowel disease (STRIDE-II) guidelines as the primary treatment objective in Crohn’s disease as part of a treat-to-target approach (Table 1)[1]. However, Crohn’s disease represents a transmural disease process, illuminating potential limitations associated with only evaluating Crohn’s disease activity and therapy response at the mucosal level. Moreover, routine ileo-colonoscopy does not facilitate assessment of small bowel segments proximal to the terminal ileum, and clinical symptoms may not always reliably correlate with small bowel Crohn’s disease activity. These caveats highlight the need for objective assessments of Crohn’s disease activity[2-4]. In light of these limitations, the STRIDE-II guidelines support the use of cross-sectional imaging modalities such as magnetic resonance enterography (MRE), computed tomography enterography, and intestinal ultrasound (IUS), as adjunctive methods of evaluating small bowel Crohn’s disease[1,5,6].
Table 1 Objective treatment targets endorsed by the selecting therapeutic targets in inflammatory bowel disease-II guidelines in adult patients with Crohn’s disease[1].
CDEIS < 3 or SES-CD ≤ 2, and absence of ulceration
Biomarker normalisation
CRP < upper threshold of normal range; FCP < 250 μg/g
Adjunctive target
Transmural healing/remission
Lack of consensus definition of transmural outcomes; Adjunct to endoscopic outcomes assessed using cross-sectional imaging modalities (MRI, CT, IUS)
Obtaining radiological images of the bowel represents an important aspect of Crohn’s disease care. As an incurable disease with a young age of onset, patients with Crohn’s disease typically require frequent imaging over their lifetimes[7]. MRE represents a safe, accurate, and radiation-free imaging modality that is frequently used to document the disease extent and evaluate Crohn’s disease activity, with the benefit of also being able to identify extra-luminal disease complications such as fistulae and abscesses[8]. Unlike ileo-colonoscopy which is only able to evaluate disease activity at a mucosal level, MRE is capable of evaluating disease activity across all layers of the bowel wall in a manner that reflects the transmural nature of Crohn’s disease[9]. Moreover, the clinical utility of evaluating transmural disease activity is supported by data indicating that transmural outcomes may be associated with more favourable long-term clinical outcomes in patients with Crohn’s disease than endoscopic endpoints alone[10,11]. However, the absence of consensus definitions of transmural outcomes, including transmural response and remission, remains an impediment to their widespread adoption and application in the radiological assessment of Crohn’s disease[1,5,11-14].
A standardised and systematic approach to the evaluation of radiological Crohn’s disease activity on MRE remains important and is recognised as best practice, particularly in the context of objectively quantifying Crohn’s disease activity and appraising response to medical therapy[15]. This highlights the need for validated and reproducible methods of evaluating Crohn’s disease activity that correlate with clinically meaningful Crohn’s disease outcomes such as endoscopic remission which have been endorsed by the STRIDE-II guidelines[1]. Akin to endoscopic disease activity scores, such as the Crohn’s disease endoscopic index of severity (CDEIS), and simplified endoscopic activity score for Crohn’s disease (SES-CD), several MRE disease activity scores have been proposed to evaluate radiological disease activity in Crohn’s disease (Figures 1 and 2)[16,17]. This narrative review aims to examine radiological parameters associated with active luminal Crohn’s disease, explore how these parameters have been incorporated into MRE disease activity scores, and compare key characteristics of each MRE disease activity score. Magnetic resonance imaging (MRI) scores specific to the evaluation of post-operative Crohn’s disease, and assessment of bowel wall damage using the Lemann index, will also be examined.
Figure 1 Applying the principles of endoscopic disease activity scores to magnetic resonance enterography in Crohn’s disease.
MRE: Magnetic resonance enterography; CDEIS: Crohn’s disease endoscopic index of severity; SES-CD: Simple endoscopic score for Crohn’s disease; MaRIA: Magnetic resonance index of activity; sMaRIA: Simplified magnetic resonance index of activity.
Figure 2 Endoscopic and radiological disease activity scores in luminal and post-operative Crohn’s disease.
MRE: Magnetic resonance enterography; CDEIS: Crohn’s disease endoscopic index of severity; SES-CD: Simple endoscopic score for Crohn’s disease; MaRIA: Magnetic resonance index of activity; CDMI: Crohn’s disease magnetic resonance imaging index; MEGS: Magnetic resonance enterography global score; PICMI: Paediatric inflammatory Crohn’s magnetic resonance enterography index; MREI: Magnetic resonance enterography index; MR: Magnetic resonance; MONITOR: Magnetic resonance imaging in Crohn’s disease to predict postoperative recurrence.
RADIOLOGICAL PARAMETERS ASSOCIATED WITH CROHN’S DISEASE ACTIVITY ON MRE
Parameters that correlate with Crohn’s disease activity on MRE can be broadly divided into two categories: Those focused on mural abnormalities of the bowel wall, and those that pertain to extra-intestinal and/or peri-mural features of inflammation (Table 2 and Figure 3). The most pertinent mural abnormalities of the bowel wall include thickening, oedema, ulceration, mural enhancement, and mural enhancement patterns, while important extra-luminal or peri-mural parameters include mesenteric oedema and lymphadenopathy. MRE characteristics such as mucosal ulceration and oedema have been associated with more severe endoscopic disease and unfavourable Crohn’s disease outcomes, implying that not all radiological parameters on MRE should be weighted equally[18-20]. This is reflected by the increased weighting of these high-risk parameters in MRE disease activity formulas[19,21-23]. Intravenous (IV) gadolinium-based contrast may also be administered to better appreciate active inflammation. However, clinicians need also be aware that gadolinium-based contrast agents have been associated with rare but serious complications, including nephrogenic systemic fibrosis, intracerebral gadolinium deposition, and hypersensitivity reactions[24-26]. In light of these potential risks, the European Crohn’s and Colitis Organisation and the European Society of Gastrointestinal and Abdominal Radiology guidelines advocate that the administration of IV gadolinium should be evaluated on a case-by-case basis[27].
Figure 3 Radiological findings of Crohn’s disease on magnetic resonance enterography.
A: Mural thickening and oedema of the terminal ileum on T2 sequence; B: Small bowel stricture associated and mural thickening (arrows) with pre-stenotic dilatation (arrowheads) on post-contrast T1 sequence; C: Mesenteric lymphadenopathy on post-contrast T1 sequence; D: Small bowel fistula to the caecum on post-contrast T1.
Table 2 Defining radiologic findings on magnetic resonance enterography in Crohn’s disease[19,21,28,42,44,97-105].
A collection of fluid characterised by border enhancement on post intravenous contrast T1-weighted image and central fluid hyperintensity on T2-weighted image
Technical aspects of MRE such as diffusion-weighted imaging (DWI) and parameters such as apparent diffusion coefficient (ADC) have been incorporated into assessments of Crohn’s disease activity on the basis of associations between restricted mural diffusion on DWI and active bowel inflammation[28,29]. Compared to traditional MRE sequences, DWI allows for more rapid image capture and does not require the administration of IV contrast[30]. These advantages have not been shown to impact the diagnostic accuracy (sensitivity = 93%, specificity = 67%) of DWI in detecting terminal ileal inflammation relative to standard MRE sequences[31]. However, studies have documented the limitations of DWI in the assessment of inflammatory activity and drug response[32-34]. The MOTILITY trial documented that DWI lacked adequate specificity and sensitivity in the assessment of response and remission to biologic therapy in small bowel Crohn’s disease, with the study reporting that DWI did not confer any incremental prognostic value over biochemical markers such as C-reactive protein (CRP) and faecal calprotectin (FCP)[35].
Many MRE parameters associated with active Crohn’s disease can be subtle, particularly in the setting of early and/or superficial mucosal Crohn’s disease. This has the potential to lead to greater interobserver variability in how mild radiological Crohn’s disease activity is reported. This has been exemplified by studies demonstrating interobserver variability, even among expert radiologists, in the interpretation of MRE findings associated with the diagnosis, extent, and activity of Crohn’s disease[20,36-40]. Moreover, heterogeneity pertaining to how MRE disease activity parameters are defined and applied across different disease activity scores, accentuates potential shortcomings associated with using individual MRE parameters to inform clinical decision-making. In light of these limitations, standardisation of assessment nomenclature and technical parameters of MRE has been recommended[2,41,42]. In addition, research has focused on identifying the optimal combination of radiological parameters associated with Crohn’s disease activity. This has provided the basis for developing MRE disease activity scores capable of quantifying Crohn’s disease activity, and in some cases also providing a qualitative assessment of disease severity, in a more standardised and reproducible manner.
MRE DISEASE ACTIVITY SCORES IN LUMINAL CROHN’S DISEASE
Several MRE-specific scoring systems have been developed to quantify radiological disease activity in luminal Crohn’s disease. These include the magnetic resonance index of activity (MaRIA), simplified MaRIA (sMaRIA), Nancy score, London score, Crohn’s disease MRI index (CDMI), Clermont score, MRE global score (MEGS), paediatric inflammatory Crohn’s MRE index (PICMI), MRE index (MREI), and modified Clermont score (C-score)[19,21-23,30,43-46]. Most of these scoring indices have been developed using endoscopic or histopathological Crohn’s disease activity as the reference standard, while others have been developed by modifying pre-existing scoring systems. Several radiological parameters were considered for inclusion in the development phase of each of these disease activity scores (Table 3), with those determined to correlate with active Crohn’s disease based on the reference standard, incorporated into the final MRE disease activity formulas. Similarly, each MRE disease activity score has its own imaging protocol that specifies the need for oral and IV contrast, as well as the acquisition of non-standard MRE sequences such as DWI (Table 4). The characteristics of each of these MRE disease activity scores, as they apply to luminal Crohn’s disease, will be reviewed in the following section (Table 5).
Table 3 Radiological parameters evaluated in the construction of magnetic resonance enterography disease activity scores in luminal Crohn’s disease[14,18,19-21,30,43].
Table 4 Comparison of imaging protocols between magnetic resonance imaging disease activity scores for luminal and post-operative Crohn’s disease[14,19-23,30,43].
(1) Ulceration; (2) Mural thickening; (3) Mural oedema; (4) Rapid gadolinium enhancement; (5) DWI hyperintensity; and (6) Differentiation between the mucosa-submucosa complex and the muscularis propria
1 × presence of wall thickness > 3 mm + 1 × presence of wall oedema + 1 × presence of fat stranding + 2 × presence of ulceration
1 × presence of wall thickness > 5 mm + 1 × presence of parietal oedema + 1 × presence of ulceration + 1 × presence of rapid gadolinium enhancement + 1 × presence of DWI hyperintensity + 1 × presence of differentiation between the mucosa-submucosa complex and the muscularis propria
Qualitative or quantitative assessment scores of 11 radiological components
Wall thickness (> 3 mm) × 3 + presence of ulceration × 6 + presence of wall-restricted diffusion × 9 + presence of mesenteric oedema × 6 + presence of comb sign × 9
1.52 × inflamed intestinal T1 signal intensity/adjacent contrast-enhanced normal intestinal T1 signal score + 2.03 × ulceration score
0.2 × (bowel thickness in mm - 3) + 1.5 × presence of mesenteric lymphadenopathy + 2 × presence of ulceration
MaRIA
MaRIA was the first MRE disease activity index created to quantify Crohn’s disease activity and severity using defined radiological parameters. Developed in 2009, MaRIA was developed by correlating endoscopic ulceration seen on ileo-colonoscopy across a prospective cohort of 50 patients with MRE findings of active Crohn’s disease[21]. MaRIA identified mural thickness, mural oedema, relative contrast enhancement (RCE), and ulceration, as independent predictors of active Crohn’s disease activity that correlated with ulceration seen on ileo-colonoscopy[21]. The score is applied on a per bowel segment basis to mirror the application of endoscopic CDEIS scoring against which it was referenced. Crohn’s disease activity is assessed across each of the six bowel segments, namely the rectum, sigmoid colon, descending colon, transverse colon, ascending colon, and terminal ileum. Hence, similar to ileo-colonoscopy, MaRIA does not evaluate Crohn’s disease activity in small bowel segments proximal to the terminal ileum. The inclusion of RCE as a parameter in MaRIA necessitates the routine administration of IV contrast, as well as the meticulous and relatively time-consuming measurement of wall enhancement on pre- and post-contrast MRE sequences.
MaRIA has demonstrated high diagnostic accuracy in detecting active Crohn’s disease (segmental MaRIA ≥ 7, sensitivity = 87%, specificity = 87%), defined as the presence of any endoscopic mucosal lesion[18]. It can also be used to identify severe Crohn’s disease (MaRIA ≥ 11, sensitivity = 96%, specificity = 92%), defined as the presence of any endoscopic ulceration. Multiple studies have affirmed close correlations between MaRIA and validated endoscopic Crohn’s disease activity scores such as SES-CD (r = 0.68-0.787) and CDEIS (r = 0.51-0.82)[18,21,37,38,47,48]. This implies that MaRIA may have utility as a surrogate for ileo-colonoscopy (Figure 4). Moderate concordance (κ = 0.49; r = 0.42-0.56) between MaRIA and the widely used Harvey-Bradshaw index (HBI) also supports the notion that a reduction in MaRIA is also likely to be associated with symptomatic improvement[18,21,49]. However, MaRIA has been shown to correlate poorly to moderately with the Crohn’s disease activity index (CDAI) (r = 0.17-0.421), CRP (r = 0.15-0.53), and FCP (r = 0.230)[18,21,47,48,50]. These findings illuminate inconsistencies associated with comparing clinical, biochemical and radiological assessments of Crohn’s disease activity using MaRIA.
Figure 4 Application of magnetic resonance index of activity and simplified magnetic resonance index of activity scores in luminal Crohn’s disease.
A-C: Baseline magnetic resonance enterography (MRE): Magnetic resonance index of activity (MaRIA) = 21.2, simplified MaRIA = 5; Baseline MRE shows mid small bowel wall thickening (arrows in A and C), mural oedema (arrows in A), transmural ulceration (arrowheads in A and B) and hyperenhancement (arrows in C); D-F: Follow-up MRE: MaRIA = 16.5, simplified MaRIA = 2; Follow-up MRE shows creeping fat (star in D and E) and reduced wall thickening (arrows in D and F). MRE sequences: A and D: Coronal T2 fat-suppressed; B and E: Coronal post contrast T1 fat-suppressed; C and F: Axial post contrast T1 fat-suppressed.
Assessments of Crohn’s disease activity using MaRIA have also been shown to be reproducible, with good intra-rater and inter-rater agreements demonstrated by intraclass correlation coefficients (ICC) of 0.89 and 0.70-0.885, respectively[20,51-53]. However, despite its apparent utility, it has been argued that MaRIA may be impractical for use in routine clinical practice owing to its computational complexity, with one study documenting a median computation time of 12.35 minutes[19,51,54].
sMaRIA
The complexity of MaRIA led to the development of sMaRIA in 2019 from two retrospective cohorts comprising 98 patients with Crohn’s disease[19]. Similar to the original MaRIA, sMaRIA used endoscopic Crohn’s disease activity, adjudicated using CDEIS, as the reference standard[19]. The four MRE parameters evaluated as part of sMaRIA are mural oedema, fat stranding, mucosal ulceration, and bowel wall thickness defined as greater than 3 mm, with the key difference being the substitution of RCE from the original MaRIA with fat stranding in sMaRIA. sMaRIA is applied to the same six bowel segments as the original MaRIA, and thus omits assessment of small bowel segments proximal to the terminal ileum[19].
Despite evaluating the same number of radiological parameters as the MaRIA, sMaRIA is more straightforward to apply. This is objectified by sMaRIA having a median computation time of 4.50 minutes, which is less than half of the time taken to compute the original MaRIA[51]. This is largely attributable to the exclusion of quantitative RCE from sMaRIA, which greatly reduces its complexity and negates the need for IV contrast[51]. Reassuringly, a study evaluating the impact of IV contrast enhancement on the accuracy of sMaRIA in detecting active Crohn’s disease, demonstrated similar diagnostic accuracy to ileo-colonoscopy both with (sensitivity = 95.2%, specificity = 95%) and without (sensitivity = 95%, specificity = 95%) IV contrast[55]. However, this was a small study of 46 patients, of which only 7 had penetrating disease wherein contrast-enhanced sequences are favoured for accurate radiological interpretation.
sMaRIA has demonstrated high diagnostic accuracy in detecting active (segmental sMaRIA ≥ 1, sensitivity = 90%, specificity = 81%) and severe (segmental sMaRIA ≥ 2, sensitivity = 85%, specificity = 92%) Crohn’s disease, defined as the presence of any endoscopic mucosal lesions and any endoscopic ulceration, respectively[19]. Studies have also demonstrated strong correlations between sMaRIA and validated endoscopic scores such as SES-CD [ileal segments (r = 0.94), colonic segments (r = 0.82) and CDEIS (r = 0.72-0.83)][19,48,56]. Similarly, sMaRIA has demonstrated good diagnostic accuracy in assessments of endoscopic response (sensitivity = 73%, specificity = 84%), endoscopic remission (sensitivity = 91%, specificity = 92%) and mucosal healing (sensitivity = 80%, specificity = 88%) following exposure to medical therapy[19].
Similar to MaRIA from which it was derived, sMaRIA has been studied to have high inter-rater reliability (ICC = 0.853-0.96) between reporting radiologists, as well as poor correlation with CDAI (r = 0.22) and CRP (r = 0.08)[19,48,51,53,56]. However, unlike MaRIA, sMaRIA has also demonstrated an excellent correlation with FCP (r = 0.91)[56]. Overall, sMaRIA is simple to use, comparatively quick to compute, does not require IV contrast, and accurately predicts endoscopic outcomes. These favourable operational characteristics imply that sMaRIA may be better suited for clinical practice than the original MaRIA.
Nancy score
The Nancy score was initially developed on the basis of a literature review, and subsequently validated using SES-CD as its reference standard[30]. It was also the first disease activity score to incorporate and validate the use of DWI in the assessment of Crohn’s disease activity[30]. The Nancy score includes six MRE parameters: Bowel wall thickness of more than 5 mm, mural oedema, ulceration, rapid gadolinium enhancement, DWI hyperintensity, and differentiation between bowel wall layers[30]. The score evaluates the same six bowel segments as both MaRIA and sMaRIA, and similar to these scores, does not evaluate small bowel segments proximal to the terminal ileum[30]. The Nancy score requires IV contrast, but unlike other MRE indices, it does not require bowel preparation, which may represent an important advantage in its clinical application[30]. The Nancy score has been documented to have high intra-rater and inter-rater agreements with ICCs of 0.96 and 0.85-0.91, respectively; however, the time taken to compute the Nancy score has not been reported[53,57].
A segmental Nancy score of more than 2 has been associated with active Crohn’s disease, defined by the presence of erythema, oedema, pseudopolyps, aphthoid ulcers or ulceration on ileo-colonoscopy, with a sensitivity of 58.33% and specificity of 84.48%[30]. This may be attributable to the Nancy score having been derived from a literature review rather than an endoscopic reference standard, as well as the heterogeneous diagnostic performance of DWI in detecting Crohn’s disease activity.
A systematic review and meta-analysis reported that DWI identified active inflammation with sensitivities ranging from 68%-100% and specificities from 51%-100%, with lower diagnostic values observed in studies that used endoscopy as the reference standard for evaluating DWI[32]. These findings highlight a potential limitation of relying on DWI for assessing disease activity. Similarly, because the Nancy score was not developed through regression analyses against endoscopic or histopathological reference standards, this likely contributes to its more modest correlation with validated endoscopic Crohn’s disease activity scores such as the SES-CD (r = 0.565) and the CDEIS (r = 0.63)[30,57]. Nevertheless, a segmental Nancy score of less than 2 has been demonstrated to have good diagnostic accuracy for endoscopic mucosal healing [sensitivity = 92%, specificity = 68%, area under receiver operating characteristic curve (AUROC) = 0.8][57]. The inconsistency between the Nancy score’s strong correlation with endoscopic mucosal healing (Nancy < 2), and its comparatively lower diagnostic accuracy and concordance with validated endoscopic indices in active Crohn’s disease (Nancy > 2), underscores the need for further validation studies.
London score and CDMI
The London score and CDMI were developed in 2012, by comparing the transmural histopathological acute inflammation score (AIS) from small bowel resection specimens of the terminal ileum in 16 patients with Crohn’s disease in whom MRE was undertaken within two weeks of resection[43]. By using histopathological assessment of the resected terminal ileum specimens as the reference standard, the London score and CDMI facilitated the comparison of transmural assessment on MRE with transmural assessment on resection specimens. However, the inclusion of patients who required surgery for their Crohn’s disease may reflect that patients with more aggressive Crohn’s disease were included in the development of these scores.
The London score examines two MRE parameters, namely mural thickening, and mural oedema, and requires the administration of both oral and IV contrast. Given that the London score only includes two MRE parameters, it is relatively simple to apply; however, its computational time has not been formally reported. Although the London score was not developed using ileo-colonoscopy as its reference standard, it has demonstrated good concordance with validated endoscopic Crohn’s disease scoring indices such as SES-CD (r = 0.80) when applied to individual bowel segments, albeit a lower correlation with CDEIS (r = 0.51), with a segmental London score of greater or equal to 4.1 shown to correlate with an AIS of greater or equal to 2 with good sensitivity (81%) and moderate specificity (70%)[38,43,48].
CDMI extends the London score by incorporating two additional radiological parameters, namely, mesenteric oedema and mural contrast enhancement. Despite the inclusion of two additional radiological parameters, using a segmental CDMI of 3 or more for active disease was shown to provide only modest improvement in diagnostic accuracy (sensitivity = 87%, specificity = 70%, AUROC = 0.83) over the original London score[43]. Similar to the original London score, the CDMI also demonstrated only moderate concordance with validated endoscopic scores such as CDEIS (0.56-0.59)[37,48]. CDMI also demonstrated a low correlation with FCP (r = 0.39) and did not correlate with clinical disease activity scores such as the CDAI (r = 0.20), and HBI (r = 0.045), nor with CRP (r = 0.144)[44,48]. Poor correlations with CDAI (r = 0.15) and CRP (r = 0.14) were also documented with the original London score[48]. This may be related to inconsistent correlations between biochemical parameters such as FCP and CRP and ileal Crohn’s disease activity from which these scores were developed[58,59].
Both the London score and CDMI have defined cutoffs for radiologically active Crohn’s disease, but have not been configured to provide thresholds for Crohn’s disease severity, including severe disease. The London score and CDMI have also been associated with higher intra-rater agreement (ICC = 0.87; ICC = 0.89) and lower inter-rater agreement (ICC = 0.67-0.72; ICC = 0.70-0.78), respectively, compared to other MRE disease activity scores, which may impact their clinical utility when applied by multiple practitioners[20,38,52].
Clermont score
The Clermont score is another DWI-inclusive MRE disease activity score that was developed by applying MaRIA, which does not include DWI, to 31 patients with Crohn’s disease[22]. The score evaluates four radiological parameters, including DWI sequences on MRE, namely mural thickening, mural oedema, ulceration, and ADC. These parameters are applied to each of the five bowel segments, including the rectum, left/sigmoid colon, transverse colon, caecum/right colon, and terminal ileum[22]. The Clermont score does not require IV contrast but does require oral contrast[22].
A segmental Clermont score of more than 8.4 had moderate sensitivity (54.4%) and high specificity (81.3%) for detecting active Crohn’s disease, defined as the presence of superficial endoscopic ulceration, while a segmental score of more than 12.5 identified severe disease activity, defined as the presence of deep endoscopic ulceration, with high sensitivity (90.9%) and specificity (80.0%)[60]. The lower sensitivity of the Clermont score in detecting active disease may be attributed to its small inception cohort, as well as the heterogeneous performance of DWI in detecting active inflammation in Crohn’s disease[32]. These factors may also impact the generalisability of the score. The score has demonstrated low to moderate correlation with validated endoscopic indices such as SES-CD (r = 0.44-0.68) and CDEIS (r = 0.48), and moderate accuracy in predicting mucosal healing (sensitivity = 50.0%, specificity = 79.4%)[38,60]. The low to moderate endoscopic correlation of the Clermont score is not unexpected, given that its reference standard, MaRIA, has also demonstrated varying degrees of endoscopic correlation[18,21,37,38,47,48]. Nevertheless, the Clermont score has demonstrated good inter-rater agreement (ICC = 0.769), although the complexity of the score, including the non-standardised computation of ADC, illuminates potential challenges associated with its widespread application, including across institutions with different MRE protocols[51]. The complexity of the Clermont score is further highlighted by its median computation time of 14.3 minutes, which exceeds both MaRIA and sMaRIA[51]. These factors may limit the widespread uptake and application of the Clermont score in routine clinical practice.
MEGS
MEGS was developed in 2014 by building upon the London score and utilised clinical (HBI) and biochemical (FCP, CRP) parameters as its validation standard[44]. The score represents the most comprehensive radiological assessment of Crohn’s disease activity on MRE by virtue of including more MRE parameters than any other disease activity score. The 11 MRE parameters incorporated in MEGS include mural thickness, mural oedema, mural contrast enhancement, mesenteric oedema, mural enhancement pattern, haustral loss, disease length, mesenteric lymphadenopathy, comb sign, abscess and fistula[44]. Notably, MEGS includes assessments of disease length and Crohn’s disease complications such as fistulas and abscesses, which are not included in other MRE disease activity scores[44,61,62]. This was likely facilitated by the majority (n = 38) of the 71 patients studied in the validation cohort having stricturing (n = 17) or penetrating (n = 21) Crohn’s disease complications[44].
MEGS evaluates MRE parameters across nine large and small bowel segments, including the terminal ileum, proximal ileum, and jejunum[44]. The score has demonstrated good concordance with validated endoscopic Crohn’s disease activity scores such as SES-CD (r = 0.70), with a segmental MEGS of 6 or more shown to have good diagnostic accuracy (sensitivity = 88%, specificity = 75%) for endoscopic inflammation (SES-CD ≥ 3)[63]. In addition, MEGS has demonstrated favourable interrater agreement (ICC= 0.84) among radiologists. However, the score has yet to designate radiological scoring thresholds pertaining to Crohn’s disease severity, and has demonstrated low to moderate correlation with biochemical parameters such as CRP (r = 0.388) and FCP (r = 0.46), and no correlation with clinical indices such as HBI (r = 0.102), which may be attributable to similar deficiencies in the London score upon which it was based[44]. While MEGS addresses many of the shortcomings of other MRE disease activity scores, its inclusion of up to 11 radiological parameters highlights that its computation time may be longer than other MRE indices, although this remains to be formally evaluated. Comparative studies evaluating the diagnostic accuracy of MEGS are also warranted to better elucidate its performance relative to other MRE-based disease activity scores in luminal Crohn’s disease.
PICMI
PICMI represents the first and only MRE disease activity score designed specifically to evaluate radiological disease activity in paediatric luminal Crohn’s disease. Developed in 2022, PICMI was derived from a multicentre prospective cohort of 159 children (aged 6-18) with Crohn’s disease who had undergone MRE and ileo-colonoscopy within 14 days of each other. The scoring formula was derived using regression analyses against the radiologist global assessment (RGA) [categorical Likert scale from 0 (normal) to 3 (severe inflammation)], and visual analog scale (0 mm-100 mm), of radiological disease activity. In the same study, PICMI was subsequently validated against sMaRIA, RGA, weighted paediatric CDAI (wPCDAI), FCP, erythrocyte sedimentation rate (ESR), CRP and SES-CD across an independent paediatric cohort of 81 patients with Crohn’s disease[46]. PICMI does not require IV gadolinium-based contrast which improves its safety and tolerability in the paediatric population[46].
PICMI assesses five radiological components comprising mural thickening, ulceration, DWI hyperintensity, mesenteric oedema and comb sign. These radiological parameters are evaluated across eight bowel segments, which include the rectum, sigmoid colon, descending colon, transverse colon, ascending colon/caecum, terminal ileum, proximal/distal ileum and jejunum. Despite including a radiological assessment of the upper gastrointestinal tract in its initial evaluation, PICMI ultimately excluded this segment from the final score in view of the suboptimal ability to identify inflammation in this region. Using RGA as the reference standard, PICMI showed high diagnostic accuracies for transmural healing/remission (total PICMI ≤ 10, sensitivity = 97%, specificity = 89%, AUROC = 0.97), mild disease (total PCIMI = 11-55, sensitivity = 85%, specificity = 81%, AUROC = 0.93), moderate disease (total PCIMI = 56-120, sensitivity = 89%, specificity = 86%, AUROC = 0.92), and severe disease (total PCIMI > 120, sensitivity = 89%, specificity = 86%, AUROC = 0.93). Similarly, treatment response, defined as a change in one or more RGA categories, was accurately evaluated by PICMI (total PICMI reduction of > 20, sensitivity = 89%, specificity = 89%, AUROC = 0.96)[46]. PICMI has also demonstrated good reliability with high intra-rater agreement (ICC = 0.81) and moderate to high inter-rater agreement (ICC = 0.65-0.84)[46,64]. Despite involving the assessment of more MRE parameters than sMaRIA, PICMI is faster to calculate, requiring a median time of 2.05 minutes to compute[46].
PICMI showed a high correlation with RGA (r = 0.85) and a fair correlation with SES-CD (r = 0.63) across the validation cohort. PICMI also demonstrated a high correlation with the sMaRIA and a moderate correlation with FCP, although its correlations with wPCDAI, ESR and CRP were reported to be low[46]. However, an independent retrospective study by Romanchuk et al[64] that included 68 children with Crohn’s disease, documented that PCIMI correlated strongly with the PCDAI (P < 0.05) but did not correlate with CDEIS (P > 0.05). This study also reported that the remission/mild and moderate/severe PICMI groups demonstrated no discrimination for the detection of steroid-free remission at 1, 3 and 5 years (P > 0.05). Notably, the group that the PCIMI ascribed to moderate/severe disease activity exhibited a higher likelihood of receiving biologic intervention than the group judged to have remission/mild disease at 1, 3 and 5 years, with incidence rate ratios of 2.17, 2.12 and 2.21, respectively (all P < 0.05)[64]. These contrasting results highlight the need for additional independent studies to validate the clinical utility of PCIMI and compare its diagnostic accuracy in predicting endoscopic outcomes with more established MRE disease activity scores.
MREI
MREI was developed in 2023 by using SES-CD scores from 29 patients with Crohn’s disease as its reference standard[23]. The index evaluates two MRE variables, namely ulceration, and RCE which require IV contrast administration. MREI is applied to five large and three small bowel segments, including the terminal ileum, proximal ileum, and jejunum. A segmental MREI score of 1 or more has been shown to correlate with active endoscopic Crohn’s disease based on SES-CD scoring with excellent sensitivity (96.2%) and moderate specificity (66.7%)[23]. However, scoring thresholds for Crohn’s disease severity, including severe disease, have not yet been designated. MREI has demonstrated highly favourable inter-rater agreement (ICC = 0.921) between reporting radiologists and a high correlation with SES-CD (r2 = 0.770)[23].
The computation time for the MREI has not yet been reported. Although MREI evaluates only two MRE parameters, it incorporates quantitative RCE, which requires intensive computation. As such, the time required for its calculation may impact its clinical applicability in real-world practice[23]. The MREI score also does not define thresholds for Crohn’s disease severity. As a recently derived MRE disease activity index, MREI has not yet undergone external validation. Its initial development cohort was also limited, comprising a single-centre population of only 29 patients with Crohn’s disease. These factors highlight the need for further studies to evaluate its diagnostic accuracy in comparison with other MRE-based disease activity scores.
C-score
The modified Clermont-score, also known as the C-score, was developed in 2024 and represents the most recently developed MRE-based disease activity score in luminal Crohn’s disease[45]. It was devised as part of the DEVISE-CD study, which was designed specifically to build and validate a radiological disease activity score to assess transmural healing and treatment response in patients with Crohn’s disease. The scoring formula was derived from a retrospective single centre cohort of 274 patients with Crohn’s disease who underwent serial MRI, using both bowel damage progression (defined as bowel resection, new or developing stricture, fistula, or abscess), and therapy responsiveness, as reference standards[45]. The C-score incorporates three radiological parameters: Bowel wall thickening, ulceration, and mesenteric lymphadenopathy that are evaluated across nine large and small bowel segments, including the rectum, left colon/sigmoid colon, transverse colon, right colon, terminal ileum, distal ileum, proximal ileum, distal jejunum and proximal jejunum.
Outcomes defined by the C-score include transmural healing, treatment response 50 (TR50) and treatment response 25 (TR25), defined as a segmental C-score of less than 0.5, a decrease of 50% or more from baseline, and a decrease of 25% or more from baseline, respectively. Achieving transmural healing, TR50 and TR25 showed favourable associations with lower risk of bowel damage progression (adjusted hazard ratio = 0.15, 0.36 and 0.46, respectively) and surgery (adjusted hazard ratio = 0.07, 0.31 and 0.28, respectively)[45]. Similarly, achieving transmural healing (specificity = 84.0%, sensitivity = 45.0%), TR50 (specificity = 76.0%, sensitivity = 68.4%) and TR25 (specificity = 68.0%, sensitivity = 73.7%) 12 weeks following therapeutic intervention, exhibited moderate to high diagnostic accuracy in predicting corticosteroid-free remission at 1 year[45].
The C-score represents a novel disease activity score that specifically assesses transmural healing and treatment response, both of which represent clinically important outcomes in the care of patients with Crohn’s disease. Nevertheless, external validation of the C-score remains imperative to provide additional certainty regarding its diagnostic accuracy, particularly in the absence of consensus radiological definitions of transmural healing and treatment response which the score applies. Correlation between the C-score and endoscopic outcomes are also awaited. Similarly, key operational characteristics of the C-score including its reliability, thresholds for Crohn’s disease severity, computational complexity, and comparability with other MRE-based disease activity indices require further investigation.
COMPARING CHARACTERISTICS OF MRE DISEASE ACTIVITY SCORES IN LUMINAL CROHN’S DISEASE
MRE disease activity scores provide a standardized approach for the reporting radiologist to assess, document and communicate radiological Crohn’s disease activity to the treating inflammatory bowel disease (IBD) clinician. However, in view of there being multiple MRE-based disease activity scores, without clear consensus regarding which score to apply, it remains important to compare the clinical and operational characteristics of each score to ascertain their relative strengths and limitations in a real-world context (Table 6).
Table 6 Operational characteristics of magnetic resonance enterography disease activity scores in luminal Crohn’s disease[14,18-21,26,30,37,38,43,47,48,51-53,56,57,60,80].
The STRIDE-II guidelines designate endoscopic remission, defined on the basis of validated endoscopic disease activity scores such as CDEIS and SES-CD, as the consensus treatment target in Crohn’s disease[1]. This implies that MRE disease activity indices that were calibrated against endoscopic assessments of Crohn’s disease should be prioritised, as should radiological scoring systems that have been subsequently shown to correlate favourably with endoscopic disease activity. Most MRE disease activity scores have demonstrated varying correlations with SES-CD (MaRIA: r = 0.68-0.787, sMaRIA: Ileal segments r = 0.94, colonic segments r = 0.84, Nancy score r = 0.565, London score r = 0.80, Clermont score r = 0.44-0.68, MEGS r = 0.70, PICMI r = 0.63, MREI r2 = 0.770)[23,30,38,47,56,60,63]. Similarly, the MaRIA (r = 0.51-0.82), sMaRIA (r = 0.72-0.83), Nancy (r = 0.63), London (r = 0.51), CDMI (r = 0.56-0.59) and Clermont (r = 0.48) scores have also demonstrated varying correlations with CDEIS[18,19,21,37,48,57,60]. Only the C-score, presumably by virtue of being the most recently developed MRE disease activity score, has yet to be correlated with either SES-CD or CDEIS. MaRIA, sMaRIA and MREI have demonstrated the strongest correlations with endoscopic Crohn’s disease activity based on one or both of SES-CD and CDEIS. This may be attributable to these scores having been developed using validated endoscopy scores as their reference standard. Conversely, the Nancy score and Clermont score have only demonstrated moderate correlations with validated endoscopic scoring systems, which may be attributable to their use of reference standards other than endoscopy in their derivation. Despite not using validated endoscopic scoring indices as their reference standard, both the London score (r = 0.80) and MEGS (r = 0.70) have demonstrated good concordance with SES-CD, although another study documented only moderate correlation between the London score and CDEIS (r = 0.51)[43,48,63]. Notably, CDMI has only demonstrated moderate correlations with endoscopic Crohn’s disease activity adjudicated by CDEIS (r = 0.56-0.59)[37,48].
Correlation with biochemical disease activity (FCP, CRP)
The STRIDE-II guidelines designated the normalisation of CRP and FCP as immediate and intermediate treatment targets for Crohn’s disease, respectively. This implies that MRE disease activity scores that are associated with CRP and FCP should be prioritised. With the exception of sMaRIA which showed a high correlation with FCP in a single study (r = 0.91), MRE disease activity scores have largely demonstrated poor and at best, moderate correlations with CRP (MaRIA: r = 0.15-0.53; sMaRIA: r = 0.08; London score: r = 0.14; CDMI: r = 0.144; MEGS: r = 0.388) and FCP (MaRIA: r = 0.230; CDMI: r = 0.39; MEGS: r = 0.46)[18,21,44,47,48,50,56]. The discrepancies are unsurprising in view of demonstrated low correlations (r = 0.28 and r = 0.39, respectively) and poor negative predictive values (24.1% and 20.5%, respectively) of CRP and FCP with small bowel inflammation in patients with Crohn’s disease[65]. This is supported by the observations that 28% of paediatric patients with Crohn’s disease had normal CRP levels, and that FCP may not always reliably predict disease relapse[66,67]. Hence, while FCP is more specific to intestinal inflammation, CRP and FCP may not always be elevated in cases of localised Crohn’s disease activity identified using MRE disease activity scores[68].
Evaluating the extent of Crohn’s disease
All radiological disease activity scores evaluate Crohn’s disease activity on MRE across individual bowel segments in a manner that closely parallels the application of SES-CD and CDEIS, both of which systematically evaluate the terminal ileum and four colonic segments. MaRIA, sMaRIA, Nancy score, and Clermont score incorporate assessments of the terminal ileum and four to five colonic segments, with MEGS, PCIMI, MREI and C-score also incorporating assessments of more proximal small bowel segments[19,21,23,30,44-46,60].
MRE disease activity scores such as MaRIA, sMaRIA, Nancy score, London score, CDMI and Clermont score, omit routine radiological assessments of small bowel segments proximal to the terminal ileum[19,21,22,43]. This reflects that the majority of MRE disease activity scores fail to capitalise on the inherent advantage that MRE has over routine ileo-colonoscopy in its ability to assess small bowel segments inaccessible via traditional ileo-colonoscopy. However, newer scores, such as MEGS, PICMI, MREI, and C-score, have addressed this limitation by incorporating assessments of more proximal small bowel segments, including the proximal terminal ileum and jejenum[23,44-46]. The length of small bowel involvement has been documented as an unfavourable prognostic indicator in Crohn’s disease; however, MEGS remains the only MRE disease activity score to incorporate disease length as a radiological parameter[69-71]. This is likely related to inherent difficulties associated with assessments of Crohn’s disease extent, exemplified by significant interobserver variability in the assessment of Crohn’s disease extent both at diagnosis (43% agreement, κ = 0.14) and in the setting of disease relapse (53% agreement, κ = 0.07)[36].
MRE parameters
The number of radiological parameters incorporated into MRE disease activity scores ranges from two to eleven[19,21-23,30,43-46]. MEGS incorporates eleven radiological parameters, while both the London score and MREI evaluate only two parameters per segment. Nine of the ten MRE scores that evaluate luminal Crohn’s disease activity incorporate assessments of mural thickening, seven appraise mural oedema and/or ulceration, and five evaluate mural contrast enhancement or relative mural contrast enhancement[19,21-23,30,43-46]. Notably, different MRE scoring systems apply varying thresholds for key imaging parameters, which may influence their diagnostic performance. For example, thresholds for bowel wall thickening differ: sMaRIA, London score, CDMI, MEGS, and PICMI all use a 3 mm cut-off, whereas the Nancy score applies a higher threshold of 5 mm. This difference may partly explain the lower sensitivity of the Nancy score, suggesting it may identify a smaller proportion of active Crohn’s disease cases relative to other indices. The Nancy score, Clermont score, and PICMI all incorporate DWI; however, only the Clermont score includes the ADC, a non-standardised, quantitative DWI metric representing regional fluid motion. In contrast, the Nancy score and PICMI use DWI hyperintensity as a qualitative marker of diffusion restriction[22,30,46]. However, the inclusion of DWI may present reproducibility challenges, as DWI protocols in MRE are not standardised, potentially limiting the reliability and broader adoption of these scores across different institutions. All MRE scores require oral contrast with the exception of the Nancy score, while sMaRIA, Clermont score, PICMI, and the C-score do not require IV contrast. Collectively, these differences reflect substantial heterogeneity in the number, type and definitions of radiological parameters included in each MRE disease activity score, as well as differences in MRI contrast protocols and sequences.
Crohn’s disease-related complications such as strictures, fistulas, abscesses, and phlegmons have been well described, and their presence has been shown to correlate with unfavourable clinical outcomes[72-75]. The detection of complications on MRE demonstrates high reliability among radiologists, with excellent inter-observer agreement reported for the presence of strictures (κ = 0.84) and penetrating complications (κ = 0.91), including abscesses (κ = 0.98), in patients with Crohn’s disease[76]. Nevertheless, these findings have been largely excluded from existing MRE disease activity scores. In fact, the MEGS is the only score that explicitly incorporates radiological assessment of fistulae and abscesses; however, Crohn’s disease-related strictures have not yet been included in any MRE-based disease activity index[44,77].
It is noteworthy that MRE assessments of strictures and fistula were included during the construction of sMaRIA, but ultimately excluded from the logistic regression analysis due to the low incidences of these complications among the 98 Crohn’s disease patients from which the score was derived[19]. Similarly, the C-score included radiological evaluation of Crohn’s disease-related strictures and fistula as measures of bowel damage progression, however, these parameters were not included in the final C-score formula in view of the study’s objective of defining outcomes specific to transmural healing rather than bowel damage[45]. This implies that most MRE disease activity scores may be best suited to assess Crohn’s disease activity in uncomplicated inflammatory phenotypes.
The number and complexity of radiological parameters incorporated in each MRE disease activity score, as well as the time taken to input parameters into the disease activity formula and output a final score, are also likely to influence the clinical implementation and application of radiological disease activity scores. Computation time has been formally evaluated across four scores, three of which are directly or indirectly related to MaRIA. sMaRIA was demonstrated to require a median of 4.50 minutes to calculate, which was considerably shorter than both the MaRIA and Clermont scores which required a median of 12.35 minutes and 14.30 minutes, respectively[51]. Therefore, on the basis of significantly shorter computation time and comparable diagnostic accuracy, sMaRIA remains the best-placed MRE disease activity score to apply in adult patients with Crohn’s disease. Of note, PICMI has a shorter median computation time (2.05 minutes) than sMaRIA, indicating that computation time should not represent a significant barrier to its integration into routine radiological assessments of paediatric Crohn’s disease[46].
Diagnostic accuracy, reproducibility and responsiveness
Whilst most MRE indices provide a cut-off for active Crohn’s disease, MaRIA, and its derivatives, specifically sMaRIA and Clermont score, also designate cut-offs for severe Crohn’s disease with a high degree of sensitivity and specificity (AUROC = 0.96, 0.94 and 0.86, respectively)[19,21,22]. PICMI showed very high diagnostic accuracy in discriminating between transmural healing/remission (AUROC = 0.97), mild disease (AUROC = 0.92), moderate disease (AUROC = 0.93) and severe disease (AUROC = 0.93)[46]. Five MRE disease activity scores, MREI (AUROC = 0.968), sMaRIA (AUROC = 0.91), MaRIA (AUROC = 0.93), CDMI (AUROC = 0.83), and MEGS (AUROC = 0.81), have demonstrated very good to excellent ability to distinguish between active and inactive Crohn’s disease[19,21,23,43,44]. Three MRE indices, Nancy score (AUROC = 0.779), London score (AUROC = 0.76) and Clermont score (AUROC = 0.68), have demonstrated a slightly lower albeit acceptable ability to discriminate between radiologically active and inactive Crohn’s disease[30,43,60]. The diagnostic accuracy of the C-score for transmural healing has yet to be reported[45].
The reproducibility of MRE disease activity scores remains another important characteristic. This is particularly important in ensuring that MRE disease activity scores can be reliably reproduced by reporting radiologists. The inter-rater agreement has been evaluated across all MRE scoring indices, apart from the C-score, with intraclass correlation values denoting moderate to good reliability. Conversely, intra-rater agreement has only been evaluated in five of the ten disease activity scores, specifically MaRIA, Nancy score, London score, CDMI, and PICMI, with moderate to excellent reliability[19,20,23,44-46,51,52,57].
Several studies have sought to compare the diagnostic accuracy of different MRE disease activity scores, with MaRIA, sMaRIA, Nancy score, London score and CDMI being most frequently compared (Table 7)[19,38,52,53,60,78,79]. Notably, studies have yet to evaluate the comparative diagnostic accuracy of MEGS, and newer scores such as the PCIMI, MREI, and C-score, against more established MRE indices, and few studies have included comparisons of the Nancy score. However, variability in study methodologies and outcomes illuminates the need for well-designed comparative studies capable of identifying the most accurate, reproducible, and practical MRE disease activity score to apply in the radiological assessment of Crohn’s disease in clinical practice.
Table 7 Studies comparing the diagnostic utility of radiological disease activity scores using magnetic resonance enterography in luminal Crohn’s disease[19,38,52,53,60,78,79].
Active vs inactive disease on high quality MRE; Ileo-colonoscopy: SES-CD ≥ 3
MaRIA ≥ 7: AUROC= 0.838; sMaRIA ≥ 1: AUROC = 0.834; London score ≥ 4.1: AUROC = 0.738; CDMI ≥ 3: AUROC = 0.850; No P value provided
Active vs inactive disease on low quality MRE; Ileo-colonoscopy: SES-CD ≥ 3
MaRIA ≥ 7: AUROC= 0.634; sMaRIA ≥ 1: AUROC = 0.527; London score ≥ 4.1: AUROC = 0.511; CDMI ≥ 3: AUROC = 0.595; No P value provided; Diagnostic performances reduced on low vs high quality MRE (all P < 0.05)
Another important clinical objective of MRE disease activity scores is to facilitate the assessment of radiological change across serial imaging time points in a manner capable of evaluating radiological response to therapy. Nine of the ten disease activity scores, with the exception being MREI, have demonstrated the capacity to evaluate interval change and treatment responsiveness when applied at multiple imaging time points. MaRIA, sMaRIA and Nancy score have demonstrated accuracy and sensitivity in detecting mucosal healing in this context, with Guyatt’s responsiveness indices of 1.20, 1.13, and 1.18, respectively[19,57,80]. The London score, Clermont score, and MEGS have also demonstrated sensitivity in the detection of interval radiological changes reflective of treatment responsiveness in patients with Crohn’s disease[81-83]. Similarly, PICMI showed high diagnostic accuracy for identifying treatment response (Guyatt’s responsiveness index = 1.4) in paediatric Crohn’s disease patients, and the C-score demonstrated moderate to high diagnostic accuracy in predicting corticosteroid-free remission at 1 year[45,46]. A comparative study revealed that sMaRIA was significantly more sensitive to change than the London score, but exhibited similar characteristics to both MaRIA and CDMI, with standardised effect sizes of 1.17, 0.85, 0.98 and 0.95, respectively[48]. While heterogeneity in how radiological response has been defined precludes like-for-like comparisons of responsiveness between MRE disease activity scores, these data imply that MRE disease activity scores have utility in monitoring response to Crohn’s disease therapy in clinical practice. This highlights the need to embed radiological assessments, including the application of MRE disease activity scores, into Crohn’s disease trials in a manner capable of evaluating their clinical utility, endoscopy correlation, and responsiveness across serial imaging time points.
MRE DISEASE ACTIVITY SCORES IN POST-OPERATIVE CROHN’S DISEASE
Ileo-colonoscopy represents the gold standard for monitoring and adjudicating anastomotic recurrence of Crohn’s disease following ileocolonic resection. However, ileo-colonoscopy is invasive, highlighting the need to develop non-invasive alternatives to identify and monitor post-operative Crohn’s disease recurrence. MRE represents a clinically plausible alternative to ileo-colonoscopy for the assessment of post-operative Crohn’s disease recurrence. Two MRE disease activity scores, namely MRI in Crohn’s disease to predict postoperative recurrence (MONITOR) index and MR score, have been specifically designed to evaluate post-operative radiological recurrence in patients with Crohn’s disease (Tables 8 and 9). Both of these radiological disease activity scores use the Rutgeerts score, an endoscopic score widely used to predict the post-operative course of Crohn’s disease following ileocolonic resection, as their reference standard[84].
Table 8 Comparison of magnetic resonance imaging scores to evaluate post-operative recurrence in Crohn’s disease[61,62,85].
MR0: Normal; MR1: Minor mucosal abnormalities: Minor wall thickening or mural contrast enhancement without stenosis; MR2: Moderate recurrence: Major bowel wall thickening or mural contrast enhancement or low-grade stenosis without pre-stenotic dilatation; MR3: Severe recurrence: MR2 plus transmural oedema with T2 hyperintensity and fat stranding or high-grade stenosis with pre-stenostic dilatation or extramural complications
1 × presence of wall thickness; + 1 × presence of mural contrast enhancement; + 1 × presence of T2 hyperintensity; + 1 × presence of DWI hyperintensity; + 1 × presence of mural oedema; + 2.5 × presence of ulceration; + 1 × presence of disease length ≥ 20 mm
Table 9 Operational characteristics of magnetic resonance imaging scores used to evaluate post-operative recurrence in Crohn’s disease[61,62].
The MR score was developed in 2008 with the purpose of evaluating the diagnostic accuracy of MR enteroclysis relative to ileo-colonoscopy for the diagnosis of post-operative Crohn’s disease recurrence. In addition, the authors developed a severity-based MR scoring system capable of appraising post-operative radiological disease recurrence in Crohn’s disease centred around the assessment of the neo-terminal ileum on MRI[62]. Using the Rutgeerts score, applied independently to both the anastomosis and neo-terminal ileum, as the reference standard, the MR score was derived from a prospective cohort of 30 patients who had undergone ileocolonic resection for histologically confirmed Crohn’s disease[62]. All eligible patients underwent post-operative surveillance within 6-24 months of the index surgery which encompassed MR enteroclysis and ileo-colonoscopy within 90 days of each other[62]. One of the key objectives of the MR score was to differentiate between low-grade endoscopic recurrence requiring standard medical therapy, and high-grade endoscopic recurrence requiring incremental immunosuppressive therapy or surgery[62].
The radiological parameters assessed as part of the MR score include mural thickening, mural contrast enhancement, stenosis, pre-stenotic dilatation, mural oedema, fat stranding, fistula, abscess, and conglomeration tumour[84]. These nine radiological parameters are evaluated across two bowel segments, namely the ileocolonic anastomosis and the neo-terminal ileum. MR scores of MR0 (normal, no recurrence), MR1 (minimal mucosal changes), MR2 (moderate recurrence), and MR3 (severe recurrence) were noted to correspond with the Rutgeerts scores of i0, i1-2, i3, and i4, respectively.
While the MR score has demonstrated high inter-rater agreement (κ = 0.893), it exhibited only moderate (κ = 0.673) overall correlation with the Rutgeerts score, yet displayed high diagnostic accuracy (sensitivity 100%, specificity 89%) for moderate to severe radiologic (MR2/3) and endoscopic (Rutgeerts score i3/4) recurrence[62,85]. Follow-up out to 2 years demonstrated that 12.5% (1:8) and 50% (9:18) of patients in MR0/1 and MR2/3 groups, respectively, experienced clinical recurrence[85]. These findings illuminate the potential utility of using the MR score as a non-invasive tool to predict post-operative recurrence; however, the MR score would benefit from validation across larger and independent cohorts. Moreover, despite its potential, the MR score is subject to several limitations, including its computation complexity related to the evaluation of nine radiological parameters albeit across only two bowel segments, and its validation using an MR enteroclysis rather than MR enterography protocol which may not be favoured by patients and clinicians alike.
MONITOR index
The MONITOR index was developed in 2022 with the aim of developing an MRI-based index capable of predicting post-operative anastomotic Crohn’s disease recurrence following ileocolonic resection using an enterography protocol[61]. The score was developed from a cohort of 61 Crohn’s disease patients who underwent ileocolonic resection and were subjected to post-operative surveillance that included both a colonoscopy and MRE within 105 days of each other. The score used the Rutgeerts score as its reference standard, and includes seven radiological parameters, namely wall thickening, mural contrast enhancement, T2 hyperintensity, DWI hyperintensity, mural oedema, ulceration and disease length ≥ 20 mm, each assessed at both the ileocolonic anastomosis and neo-terminal ileum[61].
When applying a Rugeerts score of i2 or more, which has been associated with a higher risk of post-operative Crohn’s disease, as the reference standard, a MONITOR index of 1 or more exhibited moderate to high (sensitivity = 79%-87%, specificity = 55%-75%, AUROC = 0.80) diagnostic accuracy for endoscopic recurrence[61]. The MONITOR index also demonstrated moderate intra-rater (ICC = 0.67) and inter-rater (ICC = 0.67) agreement. However, given the MONITOR index is a recently developed score with only moderate reliability and specificity that ranged from moderate to good, further external validation is awaited to better appreciate the diagnostic accuracy, reliability, and capacity of the MONITOR index to predict post-operative anastomotic recurrence.
ASSESSMENTS OF BOWEL WALL DAMAGE
Unlike the aforementioned MRE disease activity indices, which evaluate Crohn’s disease activity solely on a radiological basis, the Lémann index is a measure of bowel damage that extends beyond radiological Crohn’s disease activity[86,87]. The Lémann index evaluates bowel segments, namely the upper tract (oesophagus, stomach, duodenum), small bowel (divided into 20 cm segments), the colon (ascending, transverse, descending, sigmoid, rectum), and anus, and evaluates and grades (0-3) three specific parameters: Surgical intervention, stricturing lesions, and penetrating lesions, within each bowel segment. Therefore, unlike MRE disease activity scores which primarily focus on an ileocolonic distribution of Crohn’s disease, the Lémann index systematically evaluates the entire gastrointestinal tract. Moreover, the Lémann index is not specific to MRE but rather integrates pan-enteric assessments of Crohn’s disease across each bowel segment, using gastroscopy, colonoscopy, computed tomography imaging, and/or MRE, to formulate an overall Lémann index score. The requirement for multiple imaging and endoscopic modalities to calculate the Lémann index represents a potential limitation that may impede its application in routine clinical practice but likely augments the clinical utility of the score. The Lémann index has been observed to increase with Crohn’s disease duration, with values of 6.3, 14.3, and 19.0, corresponding to Crohn’s disease durations of < 2 years, ≥ 2 to < 10 years, and ≥ 10 years, respectively (all P < 0.001)[87]. This is perhaps unsurprising given that the frequency of surgical intervention, and Crohn’s disease-related complications such as strictures, and penetrating lesions, have been shown to increase with disease duration[88]. Moreover, The Lémann index was not influenced by the CDAI when factoring in Crohn’s disease duration, perhaps cementing its role as an objective long-term measure of Crohn’s disease-mediated bowel damage. The Lémann index has further been shown to be an independent factor in predicting follow-up surgery (hazard ratio = 1.11, P < 0.001) and hospitalisation (hazard ratio = 1.08, P < 0.001) related to Crohn’s disease[89].
CONCLUSION
MRE represents an important non-invasive cross-sectional imaging alternative to ileo-colonoscopy in Crohn’s disease that is capable of evaluating Crohn’s disease activity, response to medical therapy and post-operative anastomotic recurrence[1,5]. There is also accumulating data documenting favourable correlations between Crohn’s disease activity on MRE and ileo-colonoscopy[90]. MRE also has several advantages over ileo-colonoscopy, including its ability to evaluate small bowel segments proximal to the terminal ileum, identify extra-intestinal complications and manifestations of Crohn’s disease, and ability to provide a transmural rather than purely mucosal assessment of Crohn’s disease activity. Nevertheless, the breadth and complexity of radiological Crohn’s disease highlights the need for a more structured, reproducible and objective approach to appraising and reporting radiological disease activity on MRE.
A structured approach should ideally encompass the quantification of radiological Crohn’s disease activity, evaluation of interval radiological change, and adoption of a reporting structure that can be easily applied by radiologists and interpreted by IBD clinicians[15]. This has led to European multi-society guidance endorsing the use of such an approach in routine clinical practice[27,91,92]. These principles can be broadly applied to MRE and IUS, both of which have established themselves as key imaging modalities in the assessment and monitoring of Crohn’s disease[93]. It is, however, important to acknowledge differences in how each modality is reported and interpreted in clinical practice. Allowing for varied practices in some geographical areas, the majority of IUS scans are performed, interpreted, and reported by IBD clinicians; however, the opposite is true of MRE, wherein images are almost exclusively interpreted and reported by radiologists. This highlights that IBD clinicians are likely to be duly reliant on the content and structure of MRE reporting.
MRE disease activity scores (Figure 5) have the potential to provide a structured and reproducible method of evaluating radiological Crohn’s disease; however, several barriers remain to be addressed before they can be integrated into routine IBD care. First, consensus radiological treatment targets in both luminal and post-operative Crohn’s disease need to be defined and validated against comparable endoscopic outcomes in randomised controlled trials. Second, a lack of agreement regarding the optimal number and type of radiological parameters to include in MRE disease activity scores, including how each parameter is defined and interpreted, needs to be resolved. This is particularly important given that the number and complexity of radiological parameters included in each MRE disease activity score are likely to influence its computation time, which represents a critical ‘real-world’ consideration if widespread uptake and application of scoring systems remains the goal. Moreover, apart from being less invasive, one of the inherent advantages that MRE has over ileo-colonoscopy remains its ability to evaluate segments of the small bowel not routinely accessible via ileo-colonoscopy. Several MRE disease activity scores, including both MaRIA and sMaRIA, seemingly failed to take full advantage of this capability, although newer disease activity scores have evolved to include assessments of small bowel segments proximal to the terminal ileum. Moreover, disease activity scores have largely been constructed on the basis of uncomplicated inflammatory ileocolonic Crohn’s disease thus far. This is exemplified by the omission of radiological parameters pertaining to penetrating and stricturing disease complications from all but one MRE disease activity score. As such, variability in the assessment of Crohn’s disease activity in proximal small bowel segments, and non-inclusion of clinically consequent Crohn’s disease parameters including length of bowel involvement and disease complications, raise concerns over the clinical utility of MRE disease activity scores for luminal Crohn’s disease in their current form.
Figure 5 Summary of radiological disease activity scores.
A: Luminal Crohn’s disease; B: Post-operative Crohn’s disease. MaRIA: Magnetic resonance index of activity; MEGS: Magnetic resonance enterography global score; CDMI: Crohn’s disease magnetic resonance imaging index; PICMI: Paediatric inflammatory Crohn’s magnetic resonance enterography index; MREI: Magnetic resonance enterography index; MR: Magnetic resonance; MONITOR: Magnetic resonance imaging in Crohn’s disease to predict postoperative recurrence.
The development and application of MR disease activity scores in the post-operative setting remains comparatively underdeveloped compared to luminal Crohn’s disease, with only two scores described thus far. The most clinically useful aspect of MRE disease activity scores in the post-operative setting pertains to their ability to differentiate between mild and moderate to high-risk anastomotic recurrence in a manner that correlates with the Rutgeerts score on ileo-colonoscopy[62]. MRE is also capable of evaluating extra-mural Crohn’s disease complications, and appraising segments of the neo-terminal ileum that may not be readily accessible in the setting of an anastomotic stricture. Many of these benefits equally apply to IUS which is also emerging as a useful clinical imaging modality to apply in the post-operative setting[94,95].
MRE assessments of Crohn’s disease activity have also traditionally focused on structural rather than functional abnormalities. Functional bowel assessments, such as motility MRI (mMRI), have demonstrated clinical utility and correlation with small bowel inflammation in Crohn’s disease. However, findings from the MOTILITY trial indicate that although mMRI effectively identifies inflammation, early changes on mMRI may not reliably predict radiologic response or remission at 12 months in patients undergoing biologic therapy[96]. This implies that the clinical role of mMRI requires further study, with studies evaluating its utility as a radiological biomarker in stricturing Crohn’s disease eagerly awaited.
Finally, the routine application of MRE disease activity scores in the evaluation of radiological Crohn’s disease requires buy-in from both reporting radiologists and IBD clinicians[15]. This emphasises the need for cross-disciplinary collaboration to improve how radiological assessments of Crohn’s disease activity are integrated into existing models of multidisciplinary Crohn’s disease care to improve clinical and patient-reported outcomes.
Footnotes
Provenance and peer review: Invited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Gastroenterology and hepatology
Country of origin: Australia
Peer-review report’s classification
Scientific Quality: Grade B, Grade B
Novelty: Grade B, Grade C
Creativity or Innovation: Grade B, Grade C
Scientific Significance: Grade B, Grade B
P-Reviewer: Khan U; Wang S S-Editor: Fan M L-Editor: A P-Editor: Lei YY
Turner D, Ricciuto A, Lewis A, D'Amico F, Dhaliwal J, Griffiths AM, Bettenworth D, Sandborn WJ, Sands BE, Reinisch W, Schölmerich J, Bemelman W, Danese S, Mary JY, Rubin D, Colombel JF, Peyrin-Biroulet L, Dotan I, Abreu MT, Dignass A; International Organization for the Study of IBD. STRIDE-II: An Update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): Determining Therapeutic Goals for Treat-to-Target strategies in IBD.Gastroenterology. 2021;160:1570-1583.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 473][Cited by in RCA: 1585][Article Influence: 396.3][Reference Citation Analysis (1)]
Bruining DH, Zimmermann EM, Loftus EV Jr, Sandborn WJ, Sauer CG, Strong SA; Society of Abdominal Radiology Crohn’s Disease-Focused Panel. Consensus Recommendations for Evaluation, Interpretation, and Utilization of Computed Tomography and Magnetic Resonance Enterography in Patients With Small Bowel Crohn's Disease.Radiology. 2018;286:776-799.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 120][Cited by in RCA: 206][Article Influence: 29.4][Reference Citation Analysis (0)]
Laterza L, Piscaglia AC, Minordi LM, Scoleri I, Larosa L, Poscia A, Ingravalle F, Amato A, Alfieri S, Armuzzi A, Cammarota G, Gasbarrini A, Scaldaferri F. Multiparametric Evaluation Predicts Different Mid-Term Outcomes in Crohn's Disease.Dig Dis. 2018;36:184-193.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 16][Cited by in RCA: 35][Article Influence: 5.0][Reference Citation Analysis (0)]
Efthymiou A, Viazis N, Mantzaris G, Papadimitriou N, Tzourmakliotis D, Raptis S, Karamanolis DG. Does clinical response correlate with mucosal healing in patients with Crohn's disease of the small bowel? A prospective, case-series study using wireless capsule endoscopy.Inflamm Bowel Dis. 2008;14:1542-1547.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 78][Cited by in RCA: 80][Article Influence: 4.7][Reference Citation Analysis (36)]
Fernandes SR, Rodrigues RV, Bernardo S, Cortez-Pinto J, Rosa I, da Silva JP, Gonçalves AR, Valente A, Baldaia C, Santos PM, Correia L, Venâncio J, Campos P, Pereira AD, Velosa J. Transmural Healing Is Associated with Improved Long-term Outcomes of Patients with Crohn's Disease.Inflamm Bowel Dis. 2017;23:1403-1409.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 93][Cited by in RCA: 138][Article Influence: 17.3][Reference Citation Analysis (115)]
Lafeuille P, Hordonneau C, Vignette J, Blayac L, Dapoigny M, Reymond M, Rouquette O, Sollelis E, Boube M, Magnin B, Pereira B, Buisson A. Transmural healing and MRI healing are associated with lower risk of bowel damage progression than endoscopic mucosal healing in Crohn's disease.Aliment Pharmacol Ther. 2021;53:577-586.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 40][Reference Citation Analysis (0)]
Kucharzik T, Tielbeek J, Carter D, Taylor SA, Tolan D, Wilkens R, Bryant RV, Hoeffel C, De Kock I, Maaser C, Maconi G, Novak K, Rafaelsen SR, Scharitzer M, Spinelli A, Rimola J. ECCO-ESGAR Topical Review on Optimizing Reporting for Cross-Sectional Imaging in Inflammatory Bowel Disease.J Crohns Colitis. 2022;16:523-543.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 9][Cited by in RCA: 64][Article Influence: 21.3][Reference Citation Analysis (0)]
Ferrante M, Colombel JF, Sandborn WJ, Reinisch W, Mantzaris GJ, Kornbluth A, Rachmilewitz D, Lichtiger S, D'Haens GR, van der Woude CJ, Danese S, Diamond RH, Oortwijn AF, Tang KL, Miller M, Cornillie F, Rutgeerts PJ; International Organization for the Study of Inflammatory Bowel Diseases. Validation of endoscopic activity scores in patients with Crohn's disease based on a post hoc analysis of data from SONIC.Gastroenterology. 2013;145:978-986.e5.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 124][Cited by in RCA: 142][Article Influence: 11.8][Reference Citation Analysis (1)]
Jairath V, Ordas I, Zou G, Panes J, Stoker J, Taylor SA, Santillan C, Horsthuis K, Samaan MA, Shackelton LM, Stitt LW, Hindryckx P, Khanna R, Sandborn WJ, D'Haens G, Feagan BG, Levesque BG, Rimola J. Reliability of Measuring Ileo-Colonic Disease Activity in Crohn's Disease by Magnetic Resonance Enterography.Inflamm Bowel Dis. 2018;24:440-449.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 39][Cited by in RCA: 51][Article Influence: 7.3][Reference Citation Analysis (0)]
Sturm A, Maaser C, Calabrese E, Annese V, Fiorino G, Kucharzik T, Vavricka SR, Verstockt B, van Rheenen P, Tolan D, Taylor SA, Rimola J, Rieder F, Limdi JK, Laghi A, Krustiņš E, Kotze PG, Kopylov U, Katsanos K, Halligan S, Gordon H, González Lama Y, Ellul P, Eliakim R, Castiglione F, Burisch J, Borralho Nunes P, Bettenworth D, Baumgart DC, Stoker J; European Crohn’s and Colitis Organisation [ECCO] and the European Society of Gastrointestinal and Abdominal Radiology [ESGAR]. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 2: IBD scores and general principles and technical aspects.J Crohns Colitis. 2019;13:273-284.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 319][Cited by in RCA: 293][Article Influence: 48.8][Reference Citation Analysis (1)]
Seo N, Park SH, Kim KJ, Kang BK, Lee Y, Yang SK, Ye BD, Park SH, Kim SY, Baek S, Han K, Ha HK. 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. 2016;278:762-772.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 96][Cited by in RCA: 116][Article Influence: 11.6][Reference Citation Analysis (0)]
Hameed M, Taylor SA, Ahmed N, Chowdhury K, Patel A, Helbren E, Bhagwanani A, Hyland R, Bhatnagar G, Sidhu H, Lambie H, Franklin J, Mohsin M, Thomson E, Boone D, Tolan D, Rahman S, Sakai NS, Moran GW, Hart A, Bloom S, Menys A, Jacobs I, Halligan S, Plumb AA; MOTILITY Trial Investigators. Diffusion-weighted imaging to predict longer-term response in Crohn's disease patients commencing biological therapy: results from the MOTILITY trial.Br J Radiol. 2025;98:527-534.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 1][Reference Citation Analysis (0)]
Bhatnagar G, Mallett S, Quinn L, Beable R, Bungay H, Betts M, Greenhalgh R, Gupta A, Higginson A, Hyland R, Ilangovan R, Lambie H, Mainta E, Patel U, Pilcher J, Plumb A, Porté F, Sidhu H, Slater A, Tolan D, Zealley I, Halligan S, Taylor S. Interobserver variation in the interpretation of magnetic resonance enterography in Crohn's disease.Br J Radiol. 2022;95:20210995.
[RCA] [PubMed] [DOI] [Full Text] [Full Text (PDF)][Cited by in Crossref: 14][Cited by in RCA: 16][Article Influence: 5.3][Reference Citation Analysis (0)]
Guglielmo FF, Anupindi SA, Fletcher JG, Al-Hawary MM, Dillman JR, Grand DJ, Bruining DH, Chatterji M, Darge K, Fidler JL, Gandhi NS, Gee MS, Grajo JR, Huang C, Jaffe TA, Park SH, Rimola J, Soto JA, Taouli B, Taylor SA, Baker ME. Small Bowel Crohn Disease at CT and MR Enterography: Imaging Atlas and Glossary of Terms.Radiographics. 2020;40:354-375.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 35][Cited by in RCA: 36][Article Influence: 7.2][Reference Citation Analysis (0)]
Steward MJ, Punwani S, Proctor I, Adjei-Gyamfi Y, Chatterjee F, Bloom S, Novelli M, Halligan S, Rodriguez-Justo M, Taylor SA. Non-perforating small bowel Crohn's disease assessed by MRI enterography: derivation and histopathological validation of an MR-based activity index.Eur J Radiol. 2012;81:2080-2088.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 202][Cited by in RCA: 226][Article Influence: 16.1][Reference Citation Analysis (0)]
Makanyanga JC, Pendsé D, Dikaios N, Bloom S, McCartney S, Helbren E, Atkins E, Cuthbertson T, Punwani S, Forbes A, Halligan S, Taylor SA. Evaluation of Crohn's disease activity: initial validation of a magnetic resonance enterography global score (MEGS) against faecal calprotectin.Eur Radiol. 2014;24:277-287.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 93][Cited by in RCA: 105][Article Influence: 8.8][Reference Citation Analysis (0)]
Focht G, Cytter-Kuint R, Greer MC, Pratt LT, Castro DA, Church PC, Walters TD, Hyams J, Navon D, Martin de Carpi J, Ruemmele F, Russell RK, Gavish M, Griffiths AM, Turner D. Development, Validation, and Evaluation of the Pediatric Inflammatory Crohn's Magnetic Resonance Enterography Index From the ImageKids Study.Gastroenterology. 2022;163:1306-1320.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 3][Cited by in RCA: 19][Article Influence: 6.3][Reference Citation Analysis (0)]
Zhang YN, Liu YB, Xu J, Cao KM, Zhang XX, Wang YB, Liu F, Duan BS, Hu YD, Chu SG. Magnetic resonance Index of Activity (MaRIA) is reliable in assessing response to treatment in patients with Crohn's disease (CD).Clin Radiol. 2024;79:230-236.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 1][Reference Citation Analysis (0)]
Fernàndez-Clotet A, Sapena V, Capozzi N, Rodríguez S, Masamunt MC, Ricart E, Ordás I, Panés J, Rimola J. Avoiding contrast-enhanced sequences does not compromise the precision of the simplified MaRIA for the assessment of non-penetrating Crohn's disease activity.Eur Radiol. 2022;32:3334-3345.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 4][Cited by in RCA: 12][Article Influence: 4.0][Reference Citation Analysis (0)]
Thierry ML, Rousseau H, Pouillon L, Girard-Gavanier M, Baumann C, Lopez A, Danese S, Laurent V, Peyrin-Biroulet L. Accuracy of Diffusion-weighted Magnetic Resonance Imaging in Detecting Mucosal Healing and Treatment Response, and in Predicting Surgery, in Crohn's Disease.J Crohns Colitis. 2018;12:1180-1190.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 22][Cited by in RCA: 29][Article Influence: 4.1][Reference Citation Analysis (0)]
Buisson A, Pereira B, Goutte M, Reymond M, Allimant C, Obritin-Guilhen H, Bommelaer G, Hordonneau C. Magnetic resonance index of activity (MaRIA) and Clermont score are highly and equally effective MRI indices in detecting mucosal healing in Crohn's disease.Dig Liver Dis. 2017;49:1211-1217.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 32][Cited by in RCA: 42][Article Influence: 5.3][Reference Citation Analysis (0)]
Schaefer M, Laurent V, Grandmougin A, Vuitton L, Bourreille A, Luc A, Clerc-Urmes I, Orry X, Frampas E, De Billy M, Pouillon L, Le Berre C, Gay C, Meyer J, Baumann C, Peyrin-Biroulet L. A Magnetic Resonance Imaging Index to Predict Crohn's Disease Postoperative Recurrence: The MONITOR Index.Clin Gastroenterol Hepatol. 2022;20:e1040-e1049.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 8][Cited by in RCA: 19][Article Influence: 6.3][Reference Citation Analysis (0)]
Romanchuk A, Valle C, Ghirardi A, Bonaffini PA, Ippolito D, Sansotta N, Calia M, Zuin G, Marra P, D'Antiga L, Norsa L. Prognostic value of magnetic resonance enterography for children with Crohn's disease: A multicenter, multireader study.Dig Liver Dis. 2025;57:624-629.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 1][Reference Citation Analysis (0)]
Dane B, Qian K, Gauvin S, Ji H, Karajgikar J, Kim N, Chang S, Chandarana H, Kim S. Inter-reader agreement of the Society of Abdominal Radiology-American Gastroenterological Association (SAR-AGA) consensus reporting for key phenotypes at MR enterography in adults with Crohn disease: impact of radiologist experience.Abdom Radiol (NY). 2021;46:5095-5104.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 1][Cited by in RCA: 7][Article Influence: 1.8][Reference Citation Analysis (0)]
Kumar S, Parry T, Mallett S, Bhatnagar G, Plumb A, Walsh S, Scott N, Tandon R, Chong H, du Parcq J, Martinez A, Moorghen M, Rodriguez-Justo M, Halligan S, Taylor SA; METRIC study investigators. Diagnostic Performance of Magnetic Resonance Enterography Disease Activity Indices Compared with a Histological Reference Standard for Adult Terminal Ileal Crohn's Disease: Experience from the METRIC Trial.J Crohns Colitis. 2022;16:1531-1539.
[RCA] [PubMed] [DOI] [Full Text] [Full Text (PDF)][Cited by in Crossref: 3][Cited by in RCA: 15][Article Influence: 5.0][Reference Citation Analysis (0)]
Ordás I, Rimola J, Rodríguez S, Paredes JM, Martínez-Pérez MJ, Blanc E, Arévalo JA, Aduna M, Andreu M, Radosevic A, Ramírez-Morros AM, Pinó S, Gallego M, Jauregui-Amezaga A, Ricart E, Panés J. Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn's disease.Gastroenterology. 2014;146:374-82.e1.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 263][Cited by in RCA: 294][Article Influence: 26.7][Reference Citation Analysis (0)]
Pariente B, Cosnes J, Danese S, Sandborn WJ, Lewin M, Fletcher JG, Chowers Y, D'Haens G, Feagan BG, Hibi T, Hommes DW, Irvine EJ, Kamm MA, Loftus EV Jr, Louis E, Michetti P, Munkholm P, Oresland T, Panés J, Peyrin-Biroulet L, Reinisch W, Sands BE, Schoelmerich J, Schreiber S, Tilg H, Travis S, van Assche G, Vecchi M, Mary JY, Colombel JF, Lémann M. Development of the Crohn's disease digestive damage score, the Lémann score.Inflamm Bowel Dis. 2011;17:1415-1422.
[RCA] [PubMed] [DOI] [Full Text] [Full Text (PDF)][Cited by in Crossref: 412][Cited by in RCA: 459][Article Influence: 32.8][Reference Citation Analysis (1)]
Pariente B, Mary JY, Danese S, Chowers Y, De Cruz P, D'Haens G, Loftus EV Jr, Louis E, Panés J, Schölmerich J, Schreiber S, Vecchi M, Branche J, Bruining D, Fiorino G, Herzog M, Kamm MA, Klein A, Lewin M, Meunier P, Ordas I, Strauch U, Tontini GE, Zagdanski AM, Bonifacio C, Rimola J, Nachury M, Leroy C, Sandborn W, Colombel JF, Cosnes J. Development of the Lémann index to assess digestive tract damage in patients with Crohn's disease.Gastroenterology. 2015;148:52-63.e3.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 214][Cited by in RCA: 246][Article Influence: 24.6][Reference Citation Analysis (0)]
Maaser C, Sturm A, Vavricka SR, Kucharzik T, Fiorino G, Annese V, Calabrese E, Baumgart DC, Bettenworth D, Borralho Nunes P, Burisch J, Castiglione F, Eliakim R, Ellul P, González-Lama Y, Gordon H, Halligan S, Katsanos K, Kopylov U, Kotze PG, Krustinš E, Laghi A, Limdi JK, Rieder F, Rimola J, Taylor SA, Tolan D, van Rheenen P, Verstockt B, Stoker J; European Crohn’s and Colitis Organisation [ECCO] and the European Society of Gastrointestinal and Abdominal Radiology [ESGAR]. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications.J Crohns Colitis. 2019;13:144-164.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 1242][Cited by in RCA: 1144][Article Influence: 190.7][Reference Citation Analysis (0)]
Taylor SA, Mallett S, Bhatnagar G, Baldwin-Cleland R, Bloom S, Gupta A, Hamlin PJ, Hart AL, Higginson A, Jacobs I, McCartney S, Miles A, Murray CD, Plumb AA, Pollok RC, Punwani S, Quinn L, Rodriguez-Justo M, Shabir Z, Slater A, Tolan D, Travis S, Windsor A, Wylie P, Zealley I, Halligan S; METRIC study investigators. 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;3:548-558.
[RCA] [PubMed] [DOI] [Full Text] [Full Text (PDF)][Cited by in Crossref: 133][Cited by in RCA: 172][Article Influence: 24.6][Reference Citation Analysis (0)]
Plumb AA, Moran G, Chowdhury K, Ahmed N, Philpott S, Ahmad T, Bloom S, Hart A, Jacobs I, Menys A, Mooney P, Tolan D, Travis S, Bhagwanani A, Bhatnagar G, Boone D, Franklin J, Gangi-Burton A, Hameed M, Helbren E, Hosseini-Ardehali F, Hyland R, Kilic Y, Kumar S, Lambie H, Mohsin M, Patel A, Rahman S, Sakai N, Sidhu H, Thomson E, Ahmed S, Bannur Chikkeragowda U, Barratt N, Beeston T, Fitzke H, Gibbons N, Godfrey E, Gupta A, Higginson A, Isaac E, Kok KB, Langlands S, Parkes M, Patel J, Patel K, Patel K, Patodi N, Pollok R, Przemiosolo R, Robinson C, Thoua N, Wadke A, Halligan S, Taylor SA; MOTILITY study co-authors. Small Bowel Motility Quantified by Cine MRI to Predict Longer-Term Response in Patients with Crohn's Disease Commencing Biological Therapy: The Motility Study.Inflamm Bowel Dis. 2025;izaf023.
[RCA] [PubMed] [DOI] [Full Text][Cited by in RCA: 3][Reference Citation Analysis (0)]
Punwani S, Rodriguez-Justo M, Bainbridge A, Greenhalgh R, De Vita E, Bloom S, Cohen R, Windsor A, Obichere A, Hansmann A, Novelli M, Halligan S, Taylor SA. Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features.Radiology. 2009;252:712-720.
[RCA] [PubMed] [DOI] [Full Text][Cited by in Crossref: 202][Cited by in RCA: 202][Article Influence: 12.6][Reference Citation Analysis (0)]
