Submitted:
28 April 2025
Posted:
29 April 2025
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Abstract
Keywords:
1. Introduction
2. Imaging Methods Used in Inflammatory Bowel Diseases
- A.
- Colonoscopy remains the gold standard for diagnosis, allowing for direct visualization of the mucosa, biopsy sampling [14], and treatment of some complications. It is superior to other imaging methods in highlighting superficial erosions and ulcerations, mucosal hyperemia, and loss of vascular pattern and detecting colonic polyps [2]. Despite its advantages, it has certain limitations: it is invasive, can be uncomfortable for the patient, and does not allow for visualization of the entire small intestine, requiring the use of additional imaging techniques such as CT, intestinal ultrasound, and MRE [15]. However, a colonoscopic evaluation is necessary if patients have persistent symptoms despite normal MRE results [16]. Colonoscopy also cannot evaluate extraintestinal lesions and may limit the penetration of the endoscope in the presence of stenosis (stricture) [17]. Additionally, during the examination, lesions located in hidden parts of the colon may be missed [18].
- B.
- Video capsule endoscopy is useful in exploring the small intestine, with high sensitivity for early mucosal changes, such as small aphthous lesions[19]. It is also indicated in patients with suspected Crohn's disease and normal endoscopic results[20,21]. Recent studies have shown that video capsule endoscopy is superior to MRE in detecting lesions located in the proximal region of the small intestine[20]. However, it does not allow for in-depth evaluation of the intestinal wall and carries a risk of capsule retention in stenoses and intestinal obstructions.
- C.
- Intestinal ultrasound is a non-invasive, accessible, radiation-free method that does not require prior preparation, except for fasting a few hours before the examination[8]. Firstly, it allows for the detection of wall thickening, with a value over 3 mm considered pathological [8] and a measurement over 7 mm indicating an unfavorable prognosis, with surgical indication within the following year [22]. At the same time, the use of color Doppler or contrast medium (CEUS) allows for evaluation of both the wall perfusion and the intestinal inflammatory status, as well as the presence of complications (fistulas, abscesses, or inflammatory lesions), visualized as hypo or hyperechogenic masses[8]. An increased color Doppler signal is observed in cases of transmural edema present in the active form of Crohn's disease, as evidenced by disrupted mural stratification[23]. Intestinal ultrasound is also useful in detecting the thickening of peri-visceral adipose tissue or fat wrapping [24], as evidenced by increased echogenicity at this level, representing a sign of active disease [23]. Ultrasound images may be unsatisfactory and limited in obese patients, body habitus, or significant abdominal distension that may obscure the intestinal region [23].
- D.
- Computed tomography enterography provides detailed images of both the small intestine—highlighting intestinal wall thickening, hyperemia, submucosal fat deposition, and lymphadenopathy[25,26]—and of extraintestinal, perineural lesions, with greater accuracy in terms of the degree and severity of the disease [27], differentiating the active form from the fibrotic one. At the same time, this imaging technique is frequently used for the detection of complications of inflammatory bowel diseases (fistulas, perforations, and abscesses) [25,26] and in emergencies, such as sepsis or penetrating intra-abdominal lesions requiring surgical intervention [13]. Other advantages of CTE include a shorter scanning time, reduced costs compared to MRE [28], and suitability for patients with contraindications to MRE [13], those who are allergic to gadolinium-based contrast media [8],those who were claustrophobic in prior MR exams, and those with acute symptoms [13]. The main disadvantage is exposure to ionizing radiation, which limits its repeated use in young patients [29,30]. The radiation dose used in CTE for the adult population is between 10 and 20 mSv (milisievert) [31], while that in the pediatric population is between 2.9 and 4 mSv [32]. New protocols propose reducing the radiation dose in adults to 5-7 mSv and the noise produced by CTE during the investigation [33]. At the same time, recent studies have focused their interest on artificial intelligence and radiomics. Li et al. have demonstrated that a radiomics model (RM) based on CTE accurately describes intestinal fibrosis in patients with CD[34].
- E.
- Magnetic resonance enterography (MRE) has become the gold standard [8] in the evaluation of inflammatory bowel disease, providing simultaneously detailed images of the intestinal wall and adjacent structures and inflammatory lesions [23], differentiating inflammation from fibrosis in both the small and large intestine submucosa and the perineal area [35,36]. MRE also has high accuracy in staging small bowel inflammatory bowel disease [30], in monitoring treatment response and relapse [23], and in detecting and classifying isolated forms of colonic involvement [37]. This imaging modality is preferred in complex cases with evidence of penetrating, fistulizing, and stenosing lesions [23], as well as in fistulas and perianal sepsis [13]. Fat smudging, fecal sign, fluid level, gaseous distension, comb sign (related vascular congestion), and lymphadenopathy are elements mainly visualized/detected by MRE [2]. Another advantage—perhaps the most important—is that MRE is an imaging method that can be used to evaluate the activity of Crohn's disease and ulcerative colitis in both adults and young people [38], without the use of ionizing radiation [2]. Taylor et al. have shown that MRE has a sensitivity of 97% for detecting inflammatory bowel diseases, over 90% for fibro-inflammatory strictures, and specificity of over 95% [30].
3. Technical Principles of MRE
3.1. Standardized Protocol for MRE
3.2. Relevant Imaging Features in Magnetic Resonance Enterography
- a.
- Mural thickening :
- Is mild (<5 mm), moderate (<9mm) and severe (> 10 mm)
- Commonly occurs in active areas of inflammation (Figure 1).
- b.
- Mural hyperenhancement
- Asymmetric distribution in CD or ontinuous and concentric distribution in extensive ulcerative colitis[44]
- Stratified uptake: “double layer” (submucosa is thickened by edema and inflammation) or “trilaminar layer” (when serosa is also involved) [8]
- Homogeneous, hypovascular uptake in (chronic) fibrosis
- Correlates with clinical and biological activity scores [44]
- Evaluated on post-gadolinium T1 fat-sat sequences, in dynamics [50]
- c.
- Intramural edema
- Is detected as T2 hyperintense signal
- d.
- Restricted diffusion
- DWI hypersignal + low ADC in acute inflammation
- e.
- Ulceration
- Focal defects, fine disruptions of the mucosal contour - small signs of T2 hyposignal or intense post-contrast enhancement[50]
- Requires adequate distension of the small bowel (Figure 4 ).
- f.
- Mesenteric lymphadenopathy
- g.
- Comb sign
- h.
- Fibrofatty proliferation
- Also called “creeping fat”
- i.
- Fistulas
- They may be enteroenteric, enterocolic, enterovesical, or perianal [8]
- Fistulae occur following advanced penetrating disease [8]
- j.
- Abcesses
- Abscesses are found in the abdominal cavity, intestinal wall, or perianal area[8]
- k.
- Stenosis
- May be inflammatory (with edema and entrapment) or fibrotic (without inflammatory signs)(Figure 7)
4. Applicability of MRE in Inflammatory Bowel Diseases
4.2. Differentiating Between Active Inflammation and Fibrosis
4.3. Screening/Detection of Complications
- ➢
- Enteroenteric, enterocutaneous, perianal fistulas: MRE can distinguish between simple and complicated fistulas, guiding the decision between conservative treatment and surgical drainage;
- ➢
- Intra-abdominal abscesses;
- ➢
- Fibrous stenosis with dilation of the upstream loops;
- ➢
- Mesenteric adenopathies and changes in perenteric fat;
- ➢
- Toxic megacolon—a rare but severe complication of ulcerative colitis [29].
4.4. Monitoring Response to Treatment
4.5. Complementarity with Other Methods
- ➢
- Exploration of jejunal and ileal loops;
- ➢
- Transmural and extramural evaluation;
- ➢
- Therapeutic guidance in the absence of obvious colonic lesions.
4.6. Role in Staging and Imaging Scores
- Standardized imaging scores in Magnetic Resonance Enterography
- The most widely studied scoring system that assesses Crohn's disease activity on MRE is the magnetic resonance index activity (MaRIA) score. The score is calculated using the following equation:
- MaRIA score=1.5 x wall thickness + 0.02 x RCE (relative contrast enhancement) + 5 x edema + 10 x ulceration [61];
- ➢
- Normal: 0-6;
- ➢
- Moderate disease: ≥ 7-11;
- ➢
- Severe disease: ≥ 11 [23].
- 2.
- The major disadvantage of this score is that it is time-consuming to obtain. Such a limitation led to the development of a simplified new scoring system, the sMaRIA, which requires just 4.5 minutes compared to over 12 minutes for the MARIA [23,61,62]. The sMaRIA was validated by Ordas et al. in 2019, and its most significant advantage is that it does not involve contrast-enhanced imaging [23,63].
- MARIAs = (1 x thickness >3 mm) + (1 x edema) + (1 x fat stranding) + (2 x ulcers)
- ➢
- A score of >1 identifies active disease, with 90% sensitivity and 81% specificity;
- ➢
- 3.
5. Limitations and Challenges of enteroMR
5.1. Accessibility and Costs
- MRE requires modern, high-performance equipment (preferably 1.5T or 3T), specialized software, and trained personnel.
- The limited availability of these resources in some centers may restrict patient access.
- Additionally, the associated costs are higher than those of other investigations, such as ultrasound or CT, which may influence clinical decisions in resource-limited health systems.
- The examination time is longer (30-45 minutes), which can lead to longer waiting lists in congested hospitals.
5.2. The Need for Standardized Protocols and Experience in Interpretation
- There are variations among centers regarding the oral contrast dose scanning technique used and the criteria for interpreting the images, especially in centers without a standardized protocol.
- The lack of correlation with clinical findings and biomarkers can lead to over- or underdiagnosis errors.
- The scores used to assess disease activity (e.g., MaRIA, Clermont, Nancy, and London score) are not always applied uniformly in all centers.
5.3. Patient Preparation and Compliance
- The examination requires specific preparation, including the ingestion of a large volume of oral solution, maintaining immobility for 30-45 minutes, and tolerating possible dyspeptic symptoms. These factors can limit the quality of the examination, especially in children, elderly patients, or patients with severe abdominal pain.
5.4. Artifacts and Technical Limitations
- Respiratory movements and intestinal peristalsis can generate artifacts that degrade image quality, despite the administration of antiperistaltic agents.
- Excessive intestinal gas can affect adequate loop distension and correct interpretation.
- The sensitivity of MRE is lower than that of endoscopy in cases of small, superficial lesions, such as millimeter-sized ulcerations, incipient disease, or subtle inflammatory changes.
5.5. Contraindications and Limitations of use
- Patients with severe claustrophobia or incompatible metallic implants cannot be examined.
- MRE is not indicated in major emergencies, such as perforations or complete occlusions, where CT is preferred for speed.
6. Conclusions and Future Perspectives
6.1. Main Benefits of enteroMRI
6.2. Research and Innovation Directions
Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
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| CROHN DISEASE | ULCERATIVE COLITIS |
| Intestinal preparation before examination | Colonic preparation before examination |
| T2-weighted HASTE/SSFSE axial and coronal | MR images axial plane with entirely colon and rectum[45] |
| Balanced steady state free procession gradient-echo (SSFPGR) – Coronal | T2-weighted coronal postcontrast additional images to verify if there are complications [45] |
| 3D Cinematic bSSFP- Coronal | |
| Delayed 3D T1-weighted post-contrast fat-saturated GRE (gradient recalled echo) - Axial | Sagittal T2-weighted MR images for anastomosis [45] |
| 3D T1-weighted pre-/post-contrast fat-saturated GRE (gradient recalled echo) –Dynamic- Coronal | Thin-section axial fat-suppression T2-weighted images for perianal disease[45] |
| DWI - Axial |
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| Per-segment score | |||||
| MR features | 0 | 1 | 2 | 3 | |
| Mural thickness | <3mm | >3–5mm | >5–7mm | >7mm | |
| Mural T2 signal (oedema) | NORMAL | Minor increase | Moderate increase | Large increase | |
| Perimural T2 signal | NORMAL | Increased signal but no fluid | Small (≤2mm) fluid rim | Large (>2mm fluid rim) | |
| Contrast enhancement: pattern | NORMAL | N/A or homogeneous | Mucosal | Layered | |
| Haustral loss (colon only) | 0–5 cm | 5–15 cm | >15 cm | ||
| Multiplication factor for segmental score | |||||
| X1 | X2 | X3 | |||
| Length of disease in that segment | <5cm | 5-15cm | >15cm | ||
| Per patient score | |||||
| MR features | 0 | 5 | |||
| Lymph nodes | Absent | Present | |||
| Comb sign | Absent | Present | |||
| Abscess | Absent | Present | |||
| Fistula | Absent | Present | |||
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