Evaluating luminal and post-operative Crohn’s disease activity on magnetic resonance enterography: A review of radiological disease activity scores

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]

STRIDE-II treatment target[1]	Definition
Endoscopic response	> 50% reduction from baseline in CDEIS or SES-CD
Endoscopic healing/remission	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)

STRIDE-II: Selecting therapeutic targets in inflammatory bowel disease-II; CDEIS: Crohn’s disease endoscopic index of severity; SES-CD: Simple endoscopic score for Crohn’s disease; CRP: C-reactive protein; FCP: Faecal calprotectin; MRI: Magnetic resonance imaging; CT: Computed tomography; IUS: Intestinal ultrasound.

Table 2 Defining radiologic findings on magnetic resonance enterography in Crohn’s disease[19,21,28,42,44,97-105]

Radiological item	Definition
Mural thickening[97]	Increased bowel wall thickness; > 3 mm generally considered abnormal
Mural oedema[98]	Mural hyperintensity on T2-weighted fat-suppressed image
Peri-mural oedema/fat stranding[19]	Loss of distinction between the bowel wall and mesentery with edematous changes in the mesenteric fat
Mural contrast enhancement[99]	Qualitative assessment of mural hyperintensity post intravenous contrast administration on T1-weighted image
Mesenteric lymphadenopathy[100]	Enlargement of mesenteric lymph nodes
Ulceration[101]	Presence of intestinal wall discontinuity. Often with transmural involvement
Mural relative contrast enhancement[21]	Quantitative relative measurement of mural intensity post intravenous contrast administration on T1-weighted image
Mural contrast enhancement pattern[98]	Pattern of bowel wall contrast enhancement can be categorised into homogenous, mucosal or layered on post intravenous contrast T1-weighted image
Stricture[19]	Luminal narrowing with pre-stenotic dilatation ≥ 3 cm
Probably stricture[42]	Luminal narrowing without pre-stenotic dilatation
Comb sign[102]	Engorgement of the vasa recta with the appearance resembling a comb
Fistula[101]	Abnormal communication tract between the bowel and another epithelial surface
Diffusion-weighted imaging hyperintensity[28]	Hyperintensity on diffusion-weighted imaging identifies intestinal regions with restricted fluid diffusion
Apparent diffusion coefficient[28]	Quantitative assessment of the regional fluid movement using diffusion-weighted imaging
Abscess[103]	A collection of fluid characterised by border enhancement on post intravenous contrast T1-weighted image and central fluid hyperintensity on T2-weighted image
Pseudopolyps[104]	Islets of normal mucosa bordered by ulcerations
Disease length[44]	Quantitative measurement of the extent of the affected bowel
Creeping fat[19]	Increased presence of adipose tissue surrounding the intestine
Haustral loss[105]	Loss of haustral folds in the colon

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]

MRE disease activity score	MaRIA[21]	Simplified MaRIA[19]	Nancy score[30]	London score[43]	CDMI[43]	Clermont score[18]	MEGS[14]	PICMI[19]	MREI[20]	C-score[21]
Mural2
Mural thickening	Yes1	Yes1	Yes1	Yes1	Yes1	Yes1	Yes1	Yes1	No	Yes1
Mural oedema	Yes1	Yes1	Yes1	Yes1	Yes1	Yes1	Yes1	No	No	No
Ulceration	Yes1	Yes1	Yes1			Yes1		Yes1	Yes1	Yes1
Mural contrast enhancement		No	Yes1	No	Yes1		Yes1	No		No
Mural relative contrast enhancement	Yes1							No	Yes1	No
Mural contrast enhancement pattern				No	No		Yes1	No
Extramural2
Mesenteric lymphadenopathy	No	No		No	No	No	Yes1		No	Yes1
Mesenteric oedema				No	Yes1		Yes1	Yes1	No
Comb sign				No	No		Yes1	Yes1	No
Fistula		No				No	Yes1
Stenosis		No						No
Abscess						No	Yes1
Prestenotic dilatation								No
Fat stranding		Yes1
Creeping fat		No								No
Haustral loss							Yes1
Conglomeration tumor
Technical aspect2
DWI hyperintensity			Yes1			No		Yes1		No
Apparent diffusion coefficient						Yes1				No
Other2
Disease length							Yes1	No		No
Differentiation between mucosa-submucosa complex and the muscularis propria			Yes1
Pseudopolyps	No
Bowel motility								No
Small bowel distortion									No

¹Radiological parameters included in the final scoring formula.

²Radiological parameters included in initial assessment but excluded from the final scoring formula.

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; DWI: Diffusion-weighted imaging; MRE: Magnetic resonance enterography; C-score: Modified Clermont score.

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]

MRE disease activity score	MaRIA[21]	Simplified MaRIA[19]	Nancy score[30]	London score[43]	CDMI[43]	Clermont score[22]	MEGS[14]	PICMI[19]	MREI[20]	C-score[21]	MR score1,2[22]	MONITOR Index1[23]
Oral contrast	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes2	Yes
Intravenous contrast3	Yes	No	Yes	Yes	Yes	No	Yes	No	Yes	No	Yes	Yes
DWI protocol	No	No	Yes	No	No	Yes	No	Yes	No	No	No	No

¹Specific to post-operative Crohn’s disease recurrence.

²Magnetic resonance enteroclysis.

³Gadolinium-based contrast.

MRE: Magnetic resonance enterography; 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; DWI: Diffusion-weighted imaging; C-score: Modified Clermont score; MR: Magnetic resonance; MONITOR: Magnetic resonance imaging in Crohn’s disease to predict postoperative recurrence.

Table 5 Comparison of magnetic resonance enterography disease activity scores in luminal Crohn’s disease[17-21,25-30,43]

MRE disease activity score	MaRIA[18,21]	Simplified MaRIA[19]	Nancy score[30]	London score[43]	CDMI[17]	Clermont score[18,25]	MEGS[14]	PICMI[19]	MREI[20]	C-score[21]
Year	2009, 2011	2019	2010	2012	2012	2013, 2017	2014	2022	2023	2024
Study type	Prospective	Retrospective	Literature review	Retrospective	Retrospective	Prospective	London Score	Prospective	Prospective	Retrospective
Inception cohort (n)	50	98		16	16	31		159	29	274
Reference standard	CDEIS	CDEIS		THAIS	THAIS	MaRIA		RGA, VAS	SES-CD	BDP, Responsiveness
Bowel segments evaluated	Rectum; Sigmoid colon; Descending colon; Transverse colon; Ascending colon; Terminal ileum	Rectum; Sigmoid colon; Descending colon; Transverse colon; Ascending colon; Terminal ileum	Rectum; Sigmoid colon; Left colon; Transverse colon; Right colon; Terminal ileum	Terminal ileum	Terminal ileum	Rectum; Left/sigmoid colon; Transverse colon; Right colon/caecum; Terminal ileum	Rectum; Sigmoid colon; Descending colon; Transverse colon; Ascending colon; Caecum; Terminal ileum; Proximal ileum;Jejunum	Rectum; Sigmoid colon; Descending colon; Transverse colon; Ascending colon/caecum; Terminal ileum; Proximal/distal ileum; Jejunum	Rectum; Sigmoid colon; Descending colon; Transverse colon; Ascending colon; Terminal ileum; Proximal ileum; Jejunum	Rectum; Left/sigmoid colon; Transverse colon; Right colon; Terminal ileum; Distal ileum; Proximal ileum; Distal jejunum; Proximal jejunum
Final radiological components	(1) Ulceration; (2) Mural thickening; (3) Mural oedema; and (4) Mural relative contrast enhancement	(1) Ulceration; (2) Mural thickening; (3) Mural oedema; and (4) Fat stranding	(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) Mural thickening; and (2) Mural oedema	(1) Mural thickening; (2) Mural oedema; (3) Mesenteric oedema; and (4) Mural contrast enhancement	(1) Ulceration; (2) Mural thickening; (3) Mural oedema; and (4) Apparent diffusion coefficient	(1) Mural thickening; (2) Mural oedema; (3) Mural contrast enhancement; (4) Mural contrast enhancement pattern; (5) Mesenteric oedema; (6) Haustral loss; (7) Disease length; (8) Mesenteric lymphadenopathy; (9) Combs sign; (10) Abscess; and (11) Fistula	(1) Mural thickening; (2) Ulceration; (3) DWI hyperintensity; (4) Mesenteric oedema; and (5) Comb sign	(1) Ulceration; and (2) Mural relative contrast enhancement	(1) Ulceration; (2) Mural thickening; and (3) Mesenteric lymphadenopathy
Scoring formula	1.5 × wall thickness (mm) + 0.02 × mural relative contrast enhancement + 5 × presence of oedema + 10 × presence of ulceration	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	1.79 + 1.34 × mural thickness score + 0.94 × mural T2 score	Mural thickness + mural T2 score + perimural T2 signal + mural contrast enhancement	1.321 × apparent diffusion coefficient (mm2/second) + 1.646 × wall thickening (mm) + 8.306 × presence of ulceration + 5.613 × presence of oedema + 5.039	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

MRE: Magnetic resonance enterography; 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; DWI: Diffusion-weighted imaging; C-score: Codified Clermont score; CDEIS: Crohn’s disease endoscopic index of severity; THAIS: Transmural histopathological acute inflammation score; RGA: Radiologist global assessment; VAS: Visual analog scale; SES-CD: Simple endoscopic score for Crohn’s disease; BDP: Bowel damage progression.

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]

MRE disease activity score	MaRIA	Simplified MaRIA	Nancy score	London score	CDMI	Clermont score	MEGS	PICMI	MREI
Diagnostic accuracy
Active disease (segmental)	≥ 7	≥ 1	> 2	≥ 4.1	≥ 3	> 8.4	≥ 6	11-551	≥ 1
Sensitivity (%)	87	90	58	81	87	54	88	85	96
Specificity (%)	87	81	84	70	70	81	75	81	66
AUROC	0.93[18]	0.91[19]	0.77[30]	0.76[43]	0.83[43]	0.68[60]	0.81[26]	0.92[19]	0.96[20]
Moderate disease (segmental)								56-1201
Sensitivity (%)								89
Specificity (%)								86
AUROC								0.93[19]
Severe disease (segmental)	≥ 11	≥ 2				> 12.5		> 1201
Sensitivity (%)	92	85				90		89
Specificity (%)	92	92				80		86
AUROC	0.96[18]	0.94[19]				0.86[60]		0.93[19]
Endoscopy index correlation
SES-CD (r)	0.68-0.78[38,47]	0.94 (ileal); 0.82 (colonic)[56]	0.56[30]	0.80[38]		0.44-0.68[38,60]	0.70[26]	0.63[19]
CDEIS (r)	0.51-0.82[18,21,37,48]	0.72-0.83[19,48]	0.63[57]	0.51[48]	0.56-0.59[37,48]	0.48[60]
Intra-rater agreement
ICC coefficient	0.89[20]		0.96[57]	0.87[20]	0.89[20]			0.81[19]
Inter-rater agreement
ICC coefficient	0.70-0.88[20,51-53]	0.85-0.96[19,51,53,56]	0.85-0.91[53,57]	0.67-0.72[20,52]	0.70-0.78[20,37,52]	0.71-0.76[51,52]	0.84[14]	0.65-0.84[19,37]	0.92[20]
Responsiveness to change
Guyatt’s responsiveness index	1.20[80]	1.13[19]	1.18[57]					1.4[19]
Standardised effect size	0.98[48]	1.17[48]		0.85[48]	0.95[48]
Computation time
Minutes (median)	12.35[51]	4.50[51]				14.30[51]		2.05[19]

¹Total score.

MRE: Magnetic resonance enterography; 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; CDEIS: Crohn’s disease endoscopic index of severity; SES-CD: Simple endoscopic score for Crohn’s disease; AUROC: Area under receiver operating characteristic curve; ICC: Intraclass correlation coefficient. Clermont score was not included because comparable parameters were not reported.

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]

Ref.	MRE disease activity scores	Patients	Reference standard	Outcome
Rimola et al[38]	MaRIA; Clermont score; London score	43	Active disease; Ileo-colonoscopy: SES-CD ≥ 2	MaRIA ≥ 7: Sensitivity = 88%, specificity = 97%, AUROC = 0.92; Clermont score > 8.4: Sensitivity = 89%, specificity = 78%, AUROC = 0.84; London score ≥ 4.1: Sensitivity = 71%, specificity = 99%, AUROC = 0.85; MaRIA superior (all P < 0.05)
Buisson et al[60]	MaRIA; Clermont score	44	Active disease; Ileo-colonoscopy: Presence of superficial ulceration	MaRIA ≥ 7: Sensitivity = 51.8%, specificity = 82.1%, AUROC = 0.67; Clermont score > 8.4: Sensitivity = 54.4%, specificity = 81.3%, AUROC = 0.68; No significant differences between scores (P > 0.05)
			Severe disease; Ileo-colonoscopy: Presence of deep ulceration	MaRIA ≥ 11: Sensitivity = 90.9%, specificity = 82.0%, AUROC = 0.86; Clermont score > 12.5: Sensitivity = 90.9%, specificity = 80.0%, AUROC = 0.86; No significant differences between scores (P > 0.05)
Puylaert et al[52]	MaRIA; Clermont score; London score; CDMI	98	Active disease; Ileo-colonoscopy: CDEIS ≥ 3	MaRIA ≥ 7: Sensitivity = 80%-84%, specificity = 62%-65%; Clermont score > 8.4: Sensitivity = 83%-85%, specificity = 64%; London score ≥ 3.4: Sensitivity = 79%-82%, specificity = 68%-71%; CDMI ≥ 3: Sensitivity = 77%-82%, specificity = 68%-71%; No significant differences between scores (all P > 0.05)
			Ulcerating disease; Ileo-colonoscopy: Presence of ulceration	MaRIA ≥ 11: Sensitivity = 76%-83%, specificity = 66%-68%; Clermont score > 12.5: Sensitivity = 79%-83%, specificity = 67%; London score ≥ 3.8: Sensitivity = 80%-83%, specificity = 61%-63%; No significant differences between scores (P > 0.05)
Ordás et al[19]	MaRIA; sMaRIA	98	Active disease; Ileo-colonoscopy: Presence of any lesion	MaRIA ≥ 7: Sensitivity = 81%, specificity = 89%, AUROC = 0.89; sMaRIA ≥ 1: Sensitivity = 90%, specificity = 81%, AUROC = 0.91; No significant differences between scores (P > 0.05)
			Ulcerating disease; Ileo-colonoscopy: Presence of ulceration	MaRIA ≥ 11: Sensitivity = 95%, specificity = 91%, AUROC = 0.97; sMaRIA ≥ 2: Sensitivity = 85%, specificity = 82%, AUROC = 0.94; No significant differences between scores (P > 0.05)
Kumar et al[78]	sMaRIA; London score; CDMI	111	Active disease-HAI cutoff > 0; Biopsy of terminal ileum on ileo-colonoscopy	sMaRIA ≥ 1: Sensitivity= 83%, specificity = 41%; London score ≥ 4.1: Sensitivity = 76%, specificity = 64%; CDMI ≥ 3: Sensitivity = 81%, specificity = 41%; No P value provided
			Active disease-HAI cutoff > 1; Biopsy of terminal ileum on ileo-colonoscopy	sMaRIA ≥ 1: Sensitivity = 90%, specificity: 31%; London score ≥ 4.1: Sensitivity = 86%, specificity: 46%; CDMI ≥ 3: Sensitivity = 88%, specificity = 33%; No P value provided
Lee et al[53]	MaRIA; sMaRIA; Nancy score	61	Active disease; Ileo-colonoscopy: SES-CD ≥ 2	MaRIA ≥ 8.46: Sensitivity = 63.3%, specificity = 87.6%, AUROC = 0.752; sMaRIA ≥ 1: Sensitivity = 64.2%, specificity = 85.0%, AUROC = 0.764; Nancy > 1: Sensitivity = 65.1%, specificity = 83.8%, AUROC = 0.765; No significant differences between scores (all P > 0.05)
			Sub-analysis: Crohn’s disease diagnosis; Active vs inactive disease; Ileo-colonoscopy: SES-CD ≥ 2 vs < 2	MaRIA ≥ 8.46: AUROC = 0.826; sMaRIA ≥ 1: AUROC = 0.802; Nancy > 1: AUROC = 0.847; All scores able to differentiate (all P < 0.05)
			Sub-analysis: Disease monitoring; Active vs inactive disease; Ileo-colonoscopy: SES-CD ≥ 2 vs < 2	MaRIA ≥ 8.46: AUROC = 0.721; sMaRIA ≥ 1: AUROC = 0.741; Nancy > 1: AUROC = 0.652; MaRIA/sMaRIA able (both, P < 0.05) vs Nancy unable (P > 0.05) to differentiate
			Sub-analysis: Flare up or complication assessment; Active and inactive disease differentiation; Ileo-colonoscopy: SES-CD ≥ 2	MaRIA ≥ 8.46: AUROC = 0.761; sMaRIA ≥ 1: AUROC = 0.761; Nancy > 1: AUROC = 0.754; All scores able to differentiate (all P < 0.05)
Bohra et al[79]	MaRIA; sMaRIA; London score; CDMI	137	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)

MRE: Magnetic resonance enterography; MaRIA: Magnetic resonance index of activity; sMaRIA: Simplified magnetic resonance index of activity; CDMI: Crohn’s disease magnetic resonance imaging index; CDEIS: Crohn’s disease endoscopic index of severity; SES-CD: Simple endoscopic score for Crohn’s disease; AUROC: Area under receiver operating characteristic curve; HAI: Histological activity index.

Table 8 Comparison of magnetic resonance imaging scores to evaluate post-operative recurrence in Crohn’s disease[61,62,85]

MRE disease activity score	MR score[62,85]	MONITOR Index[61]
Year	2008	2022
MR protocol	MR enteroclysis	MR enterography
Study type	Prospective	Prospective
Inception cohort (n)	30	61
Reference standard	Rutgeerts score	Gwet’s coefficient, Rutgeerts score
Bowel segments evaluated	Anastomosis	Anastomosis
	Neo-terminal ileum	Neo-terminal ileum
Final radiological components	(1) Mural thickening; (2) Mural oedema; (3) Ulceration; (4) Mural contrast enhancement; (5) Fat stranding; (6) Stenosis; (7) Prestenotic dilatation; (8) Fistula; (9) Abscess; and (10) Conglomeration tumor	(1) Mural thickening; (2) Mural oedema; (3) Ulceration; (4) Mural contrast enhancement; (5) T2 hyperintensity; (6) DWI hyperintensity; and (7) Disease length
Scoring formula	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

MRE: Magnetic resonance enterography; DWI: Diffusion-weighted imaging; MR: Magnetic resonance; MONITOR: Magnetic resonance imaging in Crohn’s disease to predict postoperative recurrence.

Table 9 Operational characteristics of magnetic resonance imaging scores used to evaluate post-operative recurrence in Crohn’s disease[61,62]

MRE disease activity score	MR score	MONITOR Index
Diagnostic accuracy
Clinical recurrence	MR2/MR3	≥ 1
Reference standard	Rutgeerts score ≥ i3	Rutgeerts score ≥ i2
Sensitivity (%)	100	79-87
Specificity (%)	89	55-75
AUROC		0.80
Endoscopy index correlation
Rutgeerts score	κ = 0.673[62]
Intra-rater agreement
ICC		0.67[61]
Inter-rater agreement
ICC	κ = 0.893[62]	0.67[61]

MRE: Magnetic resonance enterography; MR: Magnetic resonance; MONITOR: Magnetic resonance imaging in Crohn’s disease to predict postoperative recurrence; ICC: Intraclass correlation coefficient; AUROC: Area under receiver operating characteristic curve.