Intestinal MRI in Inflammatory Bowel Disease – Literature and Survey-Based Recommendations regarding Reporting by the German Radiological Society (DRG) and the German Competence Network for Inflammatory Bowel Diseases

Key words

abdomen - ileum - MR-imaging - inflammation - small bowel

Introduction

Chronic inflammatory bowel diseases (IBDs) require medication typically for the patientʼs entire life, and surgical treatment is also often required. In Germany, more than 300 000 people have been diagnosed with an IBD [1]. in Germany in the year 2019 alone, approximately 25 500 patients with Crohnʼs disease were treated on an inpatient basis [2].

Imaging has become increasingly important for the treatment of patients with chronic inflammatory bowel diseases for both initial diagnosis and follow-up. In addition to bowel ultrasound, MRI in particular is used for diagnosis and staging and for determining disease activity and severity and complications in IBD [3]. Numerous studies and meta-analyses show the high sensitivity of MR and CT enterography (MRE and CTE) and bowel ultrasound for the detection or exclusion of lesions of the small intestine [4] as well as for the detection of extramural complications [5]. Furthermore, more recent data highlight the significance of cross-sectional imaging for treatment monitoring. Patients with endoscopic mucosal healing and additional transmural healing on MRE have a better clinical outcome [6] [7] [8] [9]. Thus, in patients with Crohnʼs disease, in addition to endoscopic evaluation, imaging of the transmural disease activity (transmural response) is becoming increasingly important a target criterion for anti-inflammatory treatments [10].

The interdisciplinary cooperation of gastroenterologists, radiologists, and surgeons is thus an important requirement for optimal management of IBD patients. This requires common consensus-based understanding with respect to image criteria, interpretation of findings, and evaluation. Previously, reporting standards have been published by individual professional societies [11] [12] [13] [14]. The ECCO (European Crohnʼs and Colitis Organization) and ESGAR (European Society of Gastrointestinal and Abdominal Radiology) recently proposed the first joint reporting standards for MRI, CT, and bowel ultrasound [15]. The goal of comprehensive implementation of standardized reporting has still not been reached in spite of the broad use of imaging in IBD.

The goal of the Work Group for Gastrointestinal/Abdominal Imaging of the Germany Radiological Society and the Imaging Work Group of the Competence Network for Inflammatory Bowel Diseases as national representation of the IBUS initiative (International Bowel Ultrasound Group; https://ibus-group.org) is to address this lack of standardization.

The present study provides recommendations for optimizing and standardizing MRI reports in IBD based on the current literature. The consensus was created by the members of the Work Group for Gastrointestinal/Abdominal Imaging of the German Radiological Society in collaboration with the Imaging Work Group of the Competence Network for Inflammatory Bowel Diseases.

Methods

Representatives of the Imaging Work Group of the Competence Network for Inflammatory Bowel Diseases (T.K., C.M.) as national representation of the IBUS initiative (International Bowel Ultrasound Group; https://ibus-group.org) and the Work Group for Gastrointestinal/Abdominal Imaging (A.S., J.W.) of the German Radiological Society conducted a systematic search of the literature using the key words ((Crohnʼs disease) OR (inflammatory bowel disease) OR (ulcerative colitis)) AND ((imaging) OR (ultrasound) OR (ultrasonography)) OR (mri) AND ((systematic review) OR (score) OR (consensus) OR (guideline) OR (recommendation)) AND ((bowel) OR (intestinal)) AND ((activity) OR (monitor)) AND (constriction, pathologic [Mesh]) OR (stricture) OR (stenosis) AND (fistula) AND (abscess)) in the NLM PubMed, Cochrane Database. Based on this, relevant criteria were defined and provided to the members of the Competence Network and the members of the German Radiological Society for evaluation and voting. Criteria in the categories medical history, examination equipment, patient preparation, quality of the examination, description of the findings, and total evaluation (see appendix 1) were addressed. The resulting criteria were approved in an expert consensus group. 55 gastroenterologists (for ultrasound [16]) and 31 radiologists (for MRE) responded to the questionnaire online. Recommendations and guidelines for MRE were created based on the responses. Only statements with consensus of at least 75 % of the participants were included in the recommendations. As a rule, these statement can only be considered in context with the accompanying texts and an overview of the literature.

Recommendations regarding reporting in MRE

General recommendations

Standardized reporting for creating MRE reports should be used in order to improve communication with medical practitioners. Reports should include all relevant disease manifestations and be able to be compared to reports by different examiners. The examination quality should also be included (expert consensus of the Work Group for Gastrointestinal/Abdominal Imaging; A.S., J.W. and the Imaging Work Group of the Competence Network for Inflammatory Bowel Diseases: T.K., C.M.).

The report is based on a standardized MRE examination (fasting for at least 4 hours, oral administration of 1.5 L mannitol 2.5 % or methyl cellulose 0.5 %, T2w with and without fat saturation axial and coronal, DWI axial, T1 3 D GRE sequences after gadolinium axial and coronal, optionally TrueFisp cine sequences as well as image acquisition in a prone position to reduce intestinal peristalsis and FOV). In addition to the dedicated indication/medical history, the type and quantity of oral and/or rectal contrast enhancement and the administration of butylscopolamine bromide should be noted in the report. Qualitative limitations on reporting, like insufficient bowel distension or artifacts, as well as a lack of visualization of the anal canal should be mentioned. Distant intestinal segment(s), anastomoses, or pouches should be mentioned at the beginning.

The report should use standard terminology for the description of pathological structures. Disease activity criteria relevant for MRI should be categorized separately in the report as mural, extramural, or extraintestinal. The inflammation status (degree of activity), stenosis status, penetration status (fistulas, abscesses), and complication status (extraintestinal manifestations) should be evaluated on the basis of the reporting criteria and in the clinical context (summarized in [Table 1], [2]).

Table 1 Structured reporting for MR enterography in IBD. Categories of findings and imaging findings/criteria in IBD.

Categories of findings	Imaging findings	Comments
Medical history	HIS search, referring physician data, patient consultation	Known IBD? Perianal fistulas or extraintestinal manifestations known? List relevant bowel surgeries, ascertain anastomosis situation, determine presence of neoterminal ileum Medical question to be examined with MRE: Bowel disease, course/monitoring, which treatment?
Patient preparation	Fasting < 4 h	Document fasting status < or > 4 h Specify type and quantity of oral contrast enhancement (e. g. 1 L 2.5 % Mannitol®) Make a note of Buscopan® administration 1x or 2 × (start of examination/prior to Gd)
Image quality	Likert scale (1–5, very good to insufficient)	Specify patient-side and sequence-side image artifacts affecting the evaluation of findings
	Anal canal fully visualized	Complete visualization of sphincter complex including perianal region
Description of findings
Affected bowel segment	Location	Provide correct anatomical information, particularly position in relation to ligament of Treitz and ileocecal valve. Pay attention to special situations like anastomoses, neoterminal ileum, and pouch. Pay attention to involvement of the appendix
	Length	Short (≤ 5 cm) Segmental (6–40 cm) Long (> 40 cm)
	Wall thickness	Look for sufficient distension, no measurement in collapsed bowel loops Asymmetrical: typical for Crohnʼs disease, mesenteric side, concentric but frequent Symmetrical: nonspecific, consider other differential diagnoses Normal (< 3 mm) Low (3–5 mm) Moderate (> 5–9 mm) Severe (≥ 10 mm) In the case of > 15 mm and/or extension into the mesentery consider carcinoma.
	Stenosis	Criteria: Wall thickening, constriction of the lumen > 50 %, and prestenotic dilation ≥ 3 cm. If prestenotic dilation is absent: qualify as “probable stenosis” Describe location and length of stenosis. Determine inflammatory activity based on criteria described under “intramural manifestations”. Look for penetrating complications in the proximal and middle portions of the stenosis
Intramural manifestations	Hyperenhancement	Compared with enhancement of an immediately adjacent segment without wall thickening. Pay attention to the possibility of false-positive findings in the jejunum and collapsed bowel segments due to increased fold density
	Two/three layers	Can be evaluated in T2w and post-Gd. Two but particularly three layers with submucosal edema (always in connection with T2w images and fat saturation) indicate active IBD
	Transmural homogeneous	No stratification, transmural enhancement, homogeneous to patchy, edema determines activity: absence of edema – mild activity
	Wall edema in T2	Evaluate in T2w with fat saturation, rule out submucosal fat
	Submucosal fat	SI decrease in T2w with fat saturation, high signal intensity in DIXON
	Diffusion restriction	Pay attention to shine-through effects caused by edema, always consult ADC
	Ulcers	Wall defects on the luminal side in T2w and/or post-Gd
	Intramural abscess	Differentiate from ulcers, DWI with diffusion restriction
	Sacculations	Antimesenteric due to shortening along the mesenteric border This can be caused by chronic scarring or more rarely by inflammation
	Loss of haustration	Observed in ulcerative colitis both in the acute inflammation stage and in the regenerative stage.
	Pseudopolyps	Can be large and confused with tumors, e. g., MALT lymphoma.
Extramural manifestations	Comb sign	Dilated vasa recta are seen near the intestinal wall on the mesenteric side. Compare with diameter of an adjacent bowel loop without wall thickening
	Creeping fat	Fibrofatty proliferation typically on the mesenteric side, sometimes also concentric. Pay attention to indirect signs like distancing of small bowel loops, can be better delimited on ultrasound in the case of slightly higher echogenicity and is an expression of inflammatory activity here
	Mesenteric edema	Can be effectively evaluated in T2w with fat saturation and post-Gd, indicates activity
	Free fluid	Interenteric, usually between the serous leaflets of two mesenteric roots = intraperitoneal, not subperitoneal
	Mesenteric lymphadenopathy	> 15 mm SAD Crohnʼs involvement probable, no established activity criterion
Extramural complications	Sinus tracts	Specify origin with clock position, sinus tracts and fistulas occur particularly in the proximal and middle segments of stenoses and in inflammatory bowel segments.
	Internal fistulas
	External perineal fistulas/abscesses	Present, not present
	Abscess	Determine location and size, in addition to T2w pay attention to DWI with diffusion restriction
	Inflammatory mass	Location, T2w without areas with fluid, DWI without abscess-related diffusion restriction
(Extra)intestinal complications	Diverse	Systematically consider typical extraintestinal manifestations/locations of IBD (sacroiliitis, PSC, pancreatitis, cholelithiasis, nephrolithiasis) In particular, pay attention to mesenteric vein thrombosis, can cause venous bowel congestion with hemorrhagic infarction, not to be confused with IBD manifestation Megacolon in ulcerative colitis

Table 2 Structured evaluation of MR enterography in IBD. Evaluation of findings on the basis of recommended reporting criteria.

Evaluation categories	Content	Evaluation	MRE criteria
Detection status	Manifestations of Crohnʼs disease?	Nonspecific inflammation	Symmetrical wall thickening, hyperenhancement, other DD possible
		Specific Crohnʼs disease criteria present	Asymmetrical wall thickening on the mesenteric side, antimesenteric sacculation Extramural complications, indicative of skip lesions (also in NSAR)
Inflammatory status	Activity	Crohnʼs disease not active	No signs of activity, minimal wall thickening, and transmural enhancement correspond to mild, non-active changes
		Crohnʼs disease active	Signs of activity present: 1. Ulcerations 2. Increased T2 SI Highly active: Three layers with submucosal edema Active: transmural patchy edema 3. Moderate to severe wall thickening (only use in connection with 1 and/or 2)
		Crohnʼs disease with extramural manifestations	Sinus tracts and/or fistula and/or abscess should be evaluated as signs of activity (active Crohnʼs disease)
	Accuracy of the evaluation Likert scale (1–5, strongly agree to disagree)	1–5	Optional
Stenosis status	Stenosis	No stenosis	< 50 % constriction of the lumen, no prestenotic dilation
		Stenosis probable	> 50 % constriction of the lumen, no prestenotic dilation
		Stenosis not active	No signs of activity
		Stenosis active	Signs of activity (increased intramural T2 SI, particularly in the case of three layers, diffusion restriction, ulcers)
	Obstruction	No obstruction	No or only minor prestenotic dilation
		With obstruction	Moderate to severe prestenotic dilation
	Accuracy of the evaluation Likert scale (1–5, strongly agree to disagree)	1–5	Optional
Penetration status	Extramural complications	None
		Sinus tracts	Location, clock position, association with stenosis or inflammatory bowel segment
		Simple fistulas
		Complex fistulas
		Inflammatory mass	Location, bowel loop involvement
		Abscesses	Location, size, able to be drained with image guidance?
	Accuracy of the evaluation Likert scale (1–5, strongly agree to disagree)	1–5	Optional
Perianal status	External fistulas/abscesses	Not present
		Present	Simple fistulas or complex fistulas, abscess size, mpMRI of the anal canal with St. James classification recommended
Extraintestinal complication status	Extraintestinal manifestations	None	Obtain medical history data, lab results, etc.
		Necrosis of the femoral head
		Sacroiliitis
		PSC
		Pancreatitis
		Mesenteric vein thrombosis
		Cholelithiasis
		Nephrolithiasis
	Accuracy of the evaluation Likert scale (1–5, strongly agree to disagree)	1–5	Optional

There are various scores for evaluating inflammatory activity in Crohnʼs disease. For MRE these are partially validated scores like the (global) MaRIA score, simplified MaRIA score, London score, Clermont score, and MEGS score [17] [18] [19] [20] [21] [22]. These semiquantitative scores are based on visual assessment (ulcers, high intramural T2 signal) and quantitative measurements (wall thickness, contrast enhancement, etc.) and differ with respect to the consideration of individual variables (e. g., in the Clermont score it is not necessary to evaluate Gd enhancement) and the weighting of the influencing variables. Most activity scores are currently used in scientific studies due to their reproducibility. It should be noted that these scores do not sufficiently reflect the intraindividual and intersegmental variation in inflammatory activity and thus the dynamic spectrum of IBDs. Therefore, scores are not always helpful with respect to clinical treatment decisions and are not an obligatory part of reporting.

Description of findings

Location

The spectrum of inflammatory activity can vary on an intraindividual basis from location to location. MR enterography is suitable for adequately visualizing the dynamic spectrum and morphological continuum of disease manifestations in IBDs [12]. Affected segments of the small and large intestine should be documented with a description of the location (see [Table 1]) and should be individually interpreted and evaluated. The same is true for special anatomical situations like anastomotic recurrence, neoterminal ileum, and pouch. The disease activity at a certain location is important for the description of the disease classification, for example, according to the Montreal and Paris classifications in pediatrics and is also used to evaluate treatment response.

Length

The extent of the inflammation should be specified in centimeters and classified as short (≤ 5 cm), medium/segmental (6–40 cm), or long (> 40 cm). The affected length of the intestinal wall is not a good individual marker for describing disease activity [23] [24] but can be useful when using scores since some of these are based on the summation of segmental activity scores (“anatomic burden of inflammation”). The Montreal and Paris classifications allow a phenotypical subclassification in various locations of the entire GI tract (non-stricturing/non-penetrating vs. stricturing vs. internally penetrating vs. external perianally penetrating). The length of the affected intestinal wall as well as the inflammatory activity in the affected GI tract segment are not taken into consideration here. Clinically relevant phenotypical overlapping phenomena (e. g. penetrating changes in stenoses) are also only insufficiently addressed.

Wall thickness

Intestinal wall thickness is an important parameter for detecting bowel wall inflammation in IBD [23] [25] [26] [27] [28] [29]. The wall thickness of a sufficiently distended bowel segment should be measured with T1w or T2w MRE. Measurements in collapsed bowel segments can result in false-positive findings or an overestimation of the degree of inflammation of the intestinal wall.

Normal intestinal wall thickness is 2 mm [30]. However, a significant range between 2 mm and 7 mm is stated in the literature [27] [31] [32] [33] [34] [35]. An expert consensus specifies 3 mm as a compromise between sensitivity and specificity to detect active disease [12] [23] [31] [36]. In the sigmoid colon, intestinal wall thicknesses of up to 4 mm can be considered normal in the case of concomitant diverticulosis with hypertrophy of the muscularis propria/mucosae so that 4 mm is preferred by several authors as a cut-off value [35]. When the intestinal wall thickness is measured under standardized conditions, there is good reproducibility for MRE with an ICC = 0.87 (95 % confidence interval 0.82–0.90) and also good agreement with histology [37]. Intestinal wall thickening, contrast enhancement, and diffusion restriction (DWI) ([Fig. 1]) help to detect affected bowel segments. However, they are ambiguous in the case of multisegmental involvement with skip lesions and are nonspecific for IBD [38]. In contrast, asymmetrical wall thickening particularly on the mesenteric side is considered a specific sign of Crohnʼs disease. Inflammatory or fibrotic shortening on the mesenteric side with antimesenteric pseudosacculations significantly increases the specificity [40]. Attention should be paid to concomitant extramural penetrating changes to corroborate the diagnosis of Crohnʼs disease.

Fig. 1 a Moderate wall thickening (5–9 mm) in the ileum without wall edema. b Significant diffusion restriction on DWI that helps with the detection of intestinal wall segments with pathological thickening.

A descriptive categorization of intestinal wall thickness as normal (< 3 mm), mild (3–5 mm), moderate (5–9 mm), and severe (≥ 10 mm) is useful and has become established. There is no consensus-based correlation between intestinal wall thickness and inflammatory activity. Therefore, acute inflammation and chronic changes in thickened segments of the intestinal wall coexist in IBD. Thus, the measurement of intestinal wall thickness is neither the only nor the best parameter for evaluating inflammatory activity. Other activity parameters (e. g., edema in T2w, stratification phenomena, etc.) should therefore be used in MRE [37] (see below and [Table 1]).

Stenosis

Approximately half of all Crohnʼs disease patients are affected by the stenotic type of the disease [41]. There is currently no consensus regarding the proper definition of stenosis. From an endoscopic perspective, a stenosis that is endoscopically impassable is indicative of stenotic disease. However, the evaluation of “luminal compliance” is limited on MRE. Thus, fixed stenoses can only be conditionally differentiated from strictures caused by spasms (string sign). The established definition of a stenosis ([Fig. 2]) is the combination of 1. wall thickening, 2. constriction of the lumen > 50 %, and 3. prestenotic dilation ≥ 3 cm of the upstream bowel segment [12] [42] [43]. The degree of prestenotic dilation depends on many factors. In addition to the chronicity of the stenosis, this include the individual degree of filling of the bowel loops and the functional or obstructive properties of the stenosis for the mostly liquid content of the intestine. Concomitant fistulas, usually in the proximal part of the stenosis, can also contribute to a prestenotic buildup of pressure. In the case of a proximal (upstream) stenosis with obstructive properties and a distal collapsed bowel (downstream), further aboral stenosis (tandem stenoses) can be masked. The diagnostic requirement of a prestenotic dilation may thus reduce the sensitivity for the detection of stenosis [44] [45] [46] [47] [48]. Stenoses suspected on MRE without verified prestenotic dilation should therefore be described as “probable stenosis”. MRI studies with an adequate reference standard (endoscopy, surgery, or both) showed a sensitivity of 89 % and a specificity of 94 % for the diagnosis of a stenosis [49]. In the same meta-analysis, the sensitivity of bowel ultrasound is 79 % and the specificity is 92 % [49].

Fig. 2 Crohnʼs disease with stenosis (circle) in terms of wall thickening with constriction of the lumen > 50 % and prestenotic dilation. Two layers without significant wall edema. Comb sign-positive, no extramural manifestations.

The detection of stenoses should be supplemented by the characterization of the inflammatory activity. While inflammatory stenoses can initially be treated with medication-based therapy, stenoses that cannot be treated with medication and include scar tissue are treated endoscopically (balloon dilation) or surgically (≤ 5 cm strictureplasty, > 5 cm resection) [50]. Stenoses usually contain both inflammatory and fibrotic components and thus do not correspond histopathologically to an “either-or” situation [51] [52]. In the case of predominant inflammation, areas of fibrosis are also present but are typically centered close around the muscularis propria, while in the case of predominant fibrosis, the fibrotic areas cover the width of the submucosa into the deep subserosa. Hypertrophy of the muscularis propria which is often also present completes the histological picture and contributes to further wall thickening [53].

The selection of optimal treatment depends on which component is dominant [54]. Reliable differentiation cannot be achieved with bowel ultrasound or MRE. Newer technologies like elastography [55] and contrast-enhanced bowel ultrasound may be helpful for determining the degree of fibrosis of a stenosis [56]. However, there are currently no standardized parameters for this. Newer developments in MRE like magnetization transfer or relative Gd enhancement in late acquisitions have also not yet been sufficiently validated for the detection of fibrosis [57].

Penetrating complications in terms of sinus tracts and fistulas often arise from the proximal part of the stenosis, are indicative of inflammatory activity, and should also be documented [43] [58].

In the follow-up, bowel wall thickness, lumen reduction, and prestenotic dilation over the course of the disease can be described and the response to treatment can be characterized [59] [60].

Indications of potential neoplasia, particularly in the case of new stenoses, should be described [61] [62]. Parameters for this are, for example, asymmetry of the stenosis, wall thickening greater than 15 mm, nodular changes, and soft tissue extending into the surrounding tissue [61] [63]. Inflammatory pseudopolyps can sometimes be difficult to differentiate from a carcinoma.

Intramural manifestations

In addition to wall thickness, other parameters like bowel wall edema and intramural ulcerations, determine the disease activity and should be described.

Wall edema: A high T2 wall signal in terms of intramural wall edema is predictive for high inflammatory activity [17] [64] [65] [66] [67]. In the case of homogeneous wall thickening, edema can have a patchy appearance in the affected bowel segments. In the case of stratification phenomena, particularly with three layers, the edema is distributed concentrically in the submucosa ([Fig. 3a]). Edema is detected in T2w sequences with fat saturation. Otherwise, it can be confused with submucosal fat. The latter is evidence of chronic inflammation without activity ([Fig. 3a]).

Fig. 3 a Segmental wall thickening (circle) in Crohnʼs disease with three layers and signs of active inflammation. a In T1w+contrast enhancement of mucosa and muscularis propria/serosa with submucosa with relatively low signal intensity. The submucosa has high signal intensity in T2w without FS. In T2w with FS, confirmation of submucosal edema. Diffusion restriction on DWI that follows the stratification pattern. b Segmental wall thickening in Crohnʼs disease. The arrows mark linear ulcers to be considered signs of inflammatory activity in addition to the submucosal edema. c Segmental wall thickening (circle) in Crohnʼs disease with three layers and signs of a mild course and submucosal fat in terms of chronification. In T1w+contrast enhancement of mucosa and muscularis propria/serosa with submucosa with relatively low signal intensity. The submucosa has high signal intensity in T2w without FS. In T2w with FS, submucosa with low signal intensity in terms of submucosal fat. In DIXON confirmation of submucosal fat with bands of high signal intensity in the submucosa.

Ulcers: Ulcerations are typically linear (the term penetrating ulcer should be avoided) and are seen on MRE as small focal interruptions in the surface of the mucosa with defect-like extension (containing air or fluid) into the intestinal wall ([Fig. 3b]). Ulcerations correlate endoscopically with high inflammatory activity [21].

Diffusion restriction: Diffusion restriction with a high B-factor should be documented as present or not present. Due to edema-based T2 shine-through effects, comparison with ADC maps is needed. DWI has moderate sensitivity and specificity for the detection of skip lesions in Crohnʼs disease ([Fig. 1], [3a]) [68] [69] [70]. The possibility of false-positive findings due to insufficient bowel distension or an increased physiological fold density in the jejunum must be taken into consideration [71]. DWI as a single criterion for inflammatory activity is of no significance. In contrast, a hyperintense T2 signal and simultaneous diffusion restriction correlate with moderate to high inflammatory activity [71] [72] [73] [74]. If further criteria are met, diffusion restriction supports the assumption of high inflammatory activity [67] [75].

Contrast enhancement: Neoangiogenesis and thus bowel wall vascularization is an important pathophysiological mechanism in chronic intestinal inflammation and contributes significantly to disease activity [31] [76] [77]. Various semiquantitative color Doppler scores (particularly Limberg score IBUS-CDS) correlate with the histological and endoscopic disease activity [78] [79] [80]. In contrast to IBD-induced neovascularization that can be detected on ultrasound, mural gadolinium enhancement in the late arterial (= enteric) to the portal venous phase [11] on MRE is subject to additional physiological and technical influencing factors. Mural enhancement on MRE is fundamentally also associated with disease activity. However, if no quantitative parameters (perfusion parameters like k_trans etc.) are used, a gradual evaluation of disease activity does not make sense [81]. The detection of mural enhancement on MRE is not specific for IBD in the absence of wall thickening. However, if wall thickening (particularly asymmetrical) is present, the sensitivity and specificity for the detection of IBD increase [27] [28] [29] [40].

Bowel wall pattern: In bowel wall segments with thickening, there are three basic contrast enhancement patterns. However, these are not specific for Crohnʼs disease. More or less homogeneous transmural enhancement indicates mild inflammatory activity depending on the wall thickness and given a lack of edema [72]. Stratification of the intestinal wall ([Fig. 3a]) occurs in fat-saturated contrast-enhanced T1 sequences in two or three layers. In the case of two layers, there is pronounced concentric hyperenhancement on the lumen side or on the inner wall while hyperenhancement of the outer wall is additionally seen in the case of three layers. The term “mucosal hyperenhancement” of the inner wall should be avoided in the case of a mucosa that is mostly destroyed on endoscopy. The submucosa appears in both cases with intermediate to hypoechoic signal behavior after Gd administration ([Fig. 3a]). It is currently not clinically relevant to differentiate between the two stratification phenomena. The signal behavior of the submucosa varies in the two stratification phenomena depending on the quality of the infiltrate. Edema has high signal intensity in T2w with fat saturation and indicates high inflammatory activity. A fatty submucosa has low signal intensity in T2w with fat saturation (or has high signal intensity in the DIXON technique) and indicates chronification of the IBD regardless of other inflammatory activity ([Fig. 3c]). A predominantly inflammatory infiltrate tends to have an intermediate signal behavior in T2w.

Extramural manifestations

Creeping fat: Perienteric inflammation usually presents as fibrofatty proliferation, partially also with edema or free mesenteric fluid [21] ([Fig. 4]). The adipose tissue reaction described as “creeping fat” is associated with increased inflammatory activity and is usually seen on the mesenteric side of the bowel and is sometimes circumferential [21]. Mesenteric adipose tissue reactions are significantly more common in the small intestine than in the large intestine and are more common in Crohnʼs disease than in ulcerative colitis [21]. The quantitative representation of a mesenteric adipose tissue reaction is difficult so that it should only be described as “present” or “absent”.

Fig. 4 Crohnʼs disease with extramural manifestations. a Dilated vasa recta (arrow) in terms of “comb sign”. b In T2w with fat saturation, mesenteric, perienteric edema with contrast enhancement after gadolinium administration (T1 post-Gd). c Pronounced fibrofatty proliferation on the mesenteric side (stars) with distancing of the small bowel loops in terms of a “creeping fat sign”.

Mesenteric edema: Perienteric mesenteric inflammatory reactions should be described in the report ([Fig. 4]). This is usually seen perirectally with circumferential extension in the mesorectal fat tissue.

Comb sign: Inflammation with enlarged and engorged vasa recta (comb sign) are directly adjacent to the affected bowel loop ([Fig. 4]). Since this sign can be seen both in acute inflammation and chronic mild inflammation, it should only be evaluated in conjunction with other activity markers [83].

Lymphadenopathy: There is currently no consensus regarding the number and size of regional lymph nodes associated with chronic bowel inflammation. Enlarged mesenteric lymph nodes with a short-axis diameter > 15 mm should be documented. A short-axis diameter of 10–15 mm can be viewed as normal in Crohnʼs disease.

Motility: The reduction of motility due to inflammation is a very subjective criterion that currently cannot be evaluated in a standardized manner and, at present, is not part of official activity indices [31] [84]. In “balanced steady state free precession” cine MRE sequences, a correlation with inflammatory activity could be shown [85] [86].

Extramural complications

Penetrating complications of Crohnʼs disease are the result of transmural inflammation and include fistulas, sinus tracts, abscesses, and inflammatory masses [87] [88]. In approximately one third of Crohnʼs patients, transmural inflammation with deep fissural ulcerations exceed the muscularis propria or serosa. Extramural extension of inflammation is the precursor to the formation of sinus tracts and fistulas.

Sinus tracts: Sinus tracts are blind-ending ducts, e. g. in the mesenteric adipose tissue ([Fig. 5]) or in the abdominal wall, without a connection to other organ structures [88]. Sinus tracts often result in angulation or kinking or outpouching of the affected bowel loop at the origin of the sinus tract. Origin with clock position and length should be described.

Fig. 5 Crohnʼs disease with extramural manifestations. a Sinus tract at 11 o'clock (arrow). b Enterovesical fistula (arrow). c Complex fistula system with inflammatory tumor in the specimen. d Retained pararectal fluids, left side (star) with diffusion restriction in terms of an abscess.

Fistulas: In contrast to blind-ending sinus tracts, internal fistulas are connected to other epithelialized surfaces. A simple fistula is a simple extra-enteric connection to another bowel segment, the skin, or another hollow organ ([Fig. 5]). A complex fistula is comprised of various extra-enteric ducts involving multiple structures [89] [90]. Complex fistulas result in multiple angulations and adhesions of the adjacent bowel loops with a star-shaped appearance [90]. In addition to the possible formation of abscesses between the bowel loops, inflammatory masses without a well-defined fluid component can form (see below). The type of fistula should be described including origin (clock position) and end (e. g. enterocutaneous, enteroenteric, enterovesical). Nonsterile fistulas connected to a sterile hollow organ (e. g. enterovesical, enterobiliary fistulas, etc.) are associated with an increased risk of septic complications and typically require surgical intervention [91]. Penetrating manifestations are typically seen in the middle or proximal portion of stenoses with transmural inflammatory activity [51] [58]. Therefore, stenoses should be carefully evaluated with respect to penetrating complications. Conversely, the origin of a fistula should be followed back to a segment with wall thickening and stenosis [92] [93]. In contrast, in the case of anastomoses, postoperative insufficiencies should be primarily considered.

Perianal fistulas: External perianal fistulas should not be subsumed under the term “penetrating complications” since there are relevant differences with respect to their etiology and biology [94]. Approximately 25 % of Crohnʼs patients have anal fistulas before or at the time of diagnosis. The anal canal including the sphincter complex should therefore be used for orientation in the MRE examination and the perianal status (fistula/abscesses present or absent) should be noted in the report. A detailed examination of the course of the fistula is not necessary or is not expedient with MRE. Therefore, in the case of suspicion of fistulas, inconclusive findings, and prior to therapy, dedicated multiparametric MRI of the anal canal should be additionally performed [95]. Classification should preferably be performed according to the AGA criteria (simple vs. complex fistulas) or according to the St. James classification [96].

Abscesses: Rim enhancement after Gd application is typical in MRE. DWI often shows diffusion restriction and also helps to differentiate smaller intramural abscesses or interloop abscesses from intestinal fluid with high T2 signal intensity [43] ([Fig. 5]). The size, location, and feasibility of interventional drainage (ultrasound or CT-guided) should be documented [97] [98] [99].

Inflammatory mass: An inflammatory mass is seen on MRE as a mesenteric, ill-defined soft-tissue mass in the case of penetrating Crohnʼs manifestations ([Fig. 5]). However, MRE shows soft-tissue segments and fatty inclusions but not any significant T2w equivalents [99]. The term mesenteric phlegmon should be avoided.

Extraintestinal involvement

Sacroiliitis: In addition to possible erosion or fusion, bands of subchondral signal changes near the iliosacral joint or enhancement that is often asymmetrical and affects only one side is seen in the T2w sequence with FS, on DWI, and on post-Gd images.

PSC: Discontinuities of the intrahepatic bile ducts usually with intrahepatic and extrahepatic bile ducts with a normal width are typically seen. Advanced stages are characterized by wall thickening and segmental dilation of the bile ducts ([Fig. 6]). In the case of suspicion of a PSC on MRE, MRCP should be additionally performed.

Fig. 6 IBD with extraintestinal complications. a Stenosis on MRE in the distal common bile duct. In the subsequent MRCP confirmation of stenosis and multiple intrahepatic bile duct strictures (arrow) consistent with PSC. b Mesenteric vein thrombosis (star) in the vascular territory of the superior mesenteric vein.

Avascular bone necrosis: Hip pain and/or steroid therapy can be seen in some cases as corresponding signal changes of the anterior femoral head circumference on MRE.

Pancreatitis: In addition to medication-induced and stone-induced pancreatitis, type II autoimmune pancreatitis must be considered. DWI MRE shows corresponding signal changes with a diffuse or focal character.

Mesenteric vein thrombosis: In particular, active chronic inflammatory bowel disease is associated with an increased risk of thromboembolic complications ([Fig. 6]), including mesenteric and portalvenous thromboses [100]. Thromboembolic complications should be documented with MRE. Pronounced three-layer phenomena of the intestinal wall can indicate venous bowel congestion with hemorrhagic infarction and should not be misinterpreted on MRE as a manifestation of active inflammatory Crohnʼs disease.

Cholelithiasis and nephrolithiasis are sometimes seen as corresponding signal losses on the T2w MRE images.

Evaluation of findings

The phenotypical subclassifications according to the Paris and Montreal classifications do not take the intraindividual dynamics of the disease course of IBD into consideration. According to Cosnes and Lemann [101] [102] [103], strictures and extramural complications can develop over the course of the disease from intestinal segments with active inflammation. The reversibility of visible morphological surrogate parameters of inflammatory activity can be observed during treatment. On the basis of defined image and reporting criteria, systematic manifestations and the extent of an IBD should be determined based on inflammatory status, stenosis status, penetration status, perianal status, and extraintestinal complication status (summary in [Table 2]).

Conclusion

The present study on MRE in IBD provides practice-oriented recommendations as to which criteria should be taken into consideration in reporting and the interpretation of findings. An improvement of the collection as well as documentation of MRE findings in IBD can help to further improve care for IBD patients. The standardization of image and evaluation criteria for MRE in IBD patients requires ongoing scientific evaluation. This manuscript does not claim to be a guideline but rather can be used as the foundation for the further development of interdisciplinary consensus in this area.

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