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Magnetic resonance imaging in the management of Crohn’s disease: a systematic review and meta-analysis

Abstract

Objectives

Crohn’s disease (CD) is a condition that can occur in any part of the gastrointestinal tract, although usually forms in the colon and terminal ileum. Magnetic resonance imaging (MRI) has become a beneficial modality in the evaluation of small bowel activity. This study reports on a systematic review and meta-analysis of magnetic resonance enterography for the prediction of CD activity and evaluation of outcomes and possible complications.

Methods

Following the PRISMA guidelines, a total of 25 low-risk studies on established CD were selected, based on a QUADAS-II score of ≥ 9.

Results

A sensitivity of 90% was revealed in a pooled analysis of the 19 studies, with heterogeneity of χ2 = 81.83 and I2 of 80.3%. Also, a specificity of 89% was calculated, with heterogeneity of χ2 = 65.12 and I2 of 70.0%.

Conclusion

It was concluded that MRI provides an effective alternative to CT enterography in the detection of small bowel activity in CD patients under supervision of radiologist for assessment of disease activity and its complications. Its advantages include the avoidance of radiation exposure and good diagnostic accuracy.

Key points

  • MRI may be considered as an effective diagnostic technique in moderate to severe CD patients.

  • It plays an increasingly important role as non-invasive and effective method to evaluate the small-bowel involvement and the possible intestinal and extra-intestinal complications, in patients affected by CD.

  • MARIA score found it to be the most sensitive and specific tool.

Introduction

Crohn’s disease (CD) is a form of inflammatory bowel disease (IBD), with an approximate frequency of 20.2 per 100,000 person-years in North America, 12.7 per 100,000 person-years in Europe, and 5 person-years in Asia [1, 2]. Broadly, one-third of CD patients have either colitis, ileocolitis, ileitis, penetrating, or stricturing intestinal (in 50% of cases) complications at the time of diagnosis [3]. While the pathology and etiology of this type of IBD are elusive, a dysregulation of the mucosal immune response is thought to play an important role in the pathogenesis of the disease, together with environmental and genetic factors [4].

An analysis of the medical history and a physical examination of the patient is the first step towards the diagnosis of CD, supported by pathologic, endoscopic, and laboratory data, using a variety of clinical severity indices, such as the Crohn's Disease Activity Index (CDAI), Harvey and Bradshaw Index, Simple Index, Oxford Index, van Hees Index, and Cape Town Index. Clinical disease activity is categorized by the European Crohn’s and Colitis Organization (ECCO) into severe, moderate, and mild [5]. While disease activity generally follows a tripartite classification, there is neither a standardized system of grouping nor a canonical definition of levels. The CDAI is perhaps the most useful and widespread research tool for quantifying the level of disease activity. A score of > 220 is used to recruit patients with active Crohn’s disease in many clinical trials, indicating a moderate to severe disease activity [5].

The Montreal and Paris classifications of CD group patients based on localization, behavior, growth, and onset; the behavior is subdivided into penetrating, non-stricturing/non-penetrating, and stricturing [6]. The most severe prognoses are usually found in the perianal and penetrating form of the disease in comparison with other types [7]. The clinical importance of differentiation according to subtype is shown during the active inflammatory phase of CD, where treatment requires modification when there is a coexistence of extramural disease or if associated fibrostenotic disease occurs with obstructive symptoms [8]. Accordingly, CD is classified clinically into four subtypes: reparative or regenerative (tending to be characterized by regeneration), inflammatory, fibrostenotic, and fistulizing or perforating [9].

There is no consensus about the preferred MRE score and they are not routinely utilized. Several MRE-based indices are common for analysis, including the Clermont score, the magnetic resonance index of activity (MaRIA), the Crohn’s disease magnetic resonance imaging index (CDMI), the Lemann index, and the magnetic resonance enterography global score (MEGS) [10,11,12,13]. This systematic review and meta-analysis focus on the use of MRE to evaluate the types of disease behavior, and to use this information to find possible correlates with clinical findings. This review correlated different MRE methods (Clermont score, MaRIA, CDMI, MEGS) for Crohn disease activity assessment.

Materials and methods

Design and eligibility criteria

This mixed-studies review incorporates a systematic search strategy and quality appraisal method, and is based on the preferred reporting items for systematic reviews and meta-analysis (PRISMA) guidelines for researchers. A comprehensive search strategy was carried out using electronic databases, such as EMBASE, CINAHL, Cochrane Central Register of Controlled Trials, and MEDLINE. All forms of study designs were included with the exception of qualitative studies and management reviews, since the main focus of the review was the quantitative assessment of MRI. Also, all relevant studies were included that examine disease type and activity in patients with CD where MRI was involved as a diagnostic tool. Patients with an established diagnosis of CD were the target population.

Prospective and retrospective studies that were given focus examined subtypes of CD, detection and characterization of the disease using MRE, diagnostic modality (surgery, histopathology, endoscopy, ileocolonoscopy, etc.), and patient population (i.e., established diagnosis of CD). No restrictions were made regarding country, patient’s age, or gender. The review is restricted in terms of the written language of articles, only including those in English. The search was limited to articles published from 1 January 2000 to 1 October 2019.

Extraction

Two independent reviewers reviewed the retrieved studies. Any disagreements were resolved either by a third reviewer or through a consensus approach. The two reviewers extracted the data independently from the selected studies. The data extraction method was established prior to the study commencement and included information on imaging characteristics, such as bowel preparation, radiologist experience, oral and intravenous contrast, MRI strength, and time interval. Also, information on study characteristics were included, comprising age, gender, number of patients, type of study, reference standard, patient population, location studied, year, and country. Particular values were calculated or extracted for the selected studies which provided data regarding individual patients, such as false positive, false negative, true positive and true negative. All outcomes used in the selected articles regarding MRI, CD, clinical examinations, and imaging characteristics were considered as primary for this review. The following keywords were used: (disease type OR behavior type) AND (clinical subtype OR DWI classification OR Clermont Score OR category) AND (Montreal OR Paris) OR (MARIA OR MRI activity index) AND Crohn’s disease.

Risk of bias individuals

The Quality Assessment of Diagnostic Accuracy Studies (QUADAS-II) tool developed for diagnostic studies was used to assess the risk of bias, applicability, and quality. Studies with scores greater than 9 were classified as low risk.

Data analysis

A summary of the results exhibits the effectiveness of MRE in detecting activity, including MARIA, using sensitivity and specificity values for studies that did not provide raw data. For studies that provided raw data, contingency tables were constructed using true positive, true negative, false positive, and false negative information. Likelihood ratios, sensitivity, specificity, and 95% confidence intervals were calculated for each study. Summary receiver-operating characteristic (ROC) curves and forest plots were presented through graphical representation, which were made using the Comprehensive Meta-Analysis software (CMA), version 3 by Biostat, Inc. For a pooled analysis, 0.5 was added to all cells that comprised a value of 0 to include all studies in the analysis. The I2 test was used to assess the heterogeneity.

Results

The preliminary database search yielded 2567 articles. These were reduced further by sorting according to title, resulting in a yield of 252 articles; these were then further reduced to 35 articles based on an appraisal of abstracts. A total of 25 articles fulfilled the inclusion criteria after consideration of the full articles and following contact with authors for missing information [1,2,3,4, 12, 14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30]. Of the 25 included articles, 7 were retrospective studies, 10 were prospective studies, and 8 were unclear with respect to type. The majority of the prospective studies used consecutive patients to restrict the selection bias. These gave sufficient information to constitute a pooled analysis; for instance, 10 studies of the initial 35 selected articles offered only summaries of results. All studies were assessed as low risk, based on QUADAS-II scores of ≥ 9.

In the 25 articles that met the inclusion criteria, a total of 2120 patients took part, out of which, 1470 patients were incorporated into a meta-analysis. The largest sample size among those patients included in the pooled analysis was 305. In an examination of the data of these 1470 patients, 150 underwent endoscopy and MR within 30 days to evaluate the distal ileum condition, which resulted in an MRI pooled specificity of 80% and a sensitivity of 88% in predicting CD activity.

Correlation between MRE and Crohn disease type and subtype

A sensitivity of 61% for predicting disease type or subtype was revealed in a pooled analysis of 19 studies [1, 2, 4, 12,13,14, 16,17,18,19,20,21,22,23,24, 31,32,33] with a heterogeneity of χ2 = 61.38 and I2 of 60.7%. A specificity of 59% was reported for the pooled analysis with a heterogeneity of χ2 = 65.12 and I2 of 70.0%. The negative predictive ratio was 0.21 and the positive predictive ratio was 6.1 using a random effects model.

Aphthous ulcers in the penetrating type of CD is demonstrated in MRE studies as a high signal intensity nidus, covered by moderate signal intensity area best seen on high-resolution SSFP images with fat suppression [34]. Oral contrast material can outline the transmural ulcers, and thus be observed as linear high-signal intensity seen passing through the gastrointestinal tract. For more accurate evaluation of transmural lesions, along with the associated peri-intestinal inflammatory changes, images must be made on a plane that is perpendicular to the bowel [9]. The penetrating disease that has large sinus tracts with or without fistulas can be evaluated using oral contrast material. This outlines these tracks, enabling them to be seen as high-signal intensity lines that pass through the full thickness of the wall of the bowel to form a small collection adjacent to it, or communicated through an adjacent luminal structure, such as the urinary bladder or another bowel segment [35].

Magnetic resonance enterography (MRE) can detect fibrostenotic disease of stricturing type, observed as a fixed narrowing of the affected segment [36, 37]. Both T1- and T2-weighed images can demonstrate chronic fibrotic strictures, showing inhomogeneous contrast enhancement in post-IV contrast sequences but without the surrounding inflammation of mesentery or obvious edema [36, 38]. The absence of gut motility in active or chronic CD is observed using fast cine sequence (T2-weighted SSFP or echo planar imaging techniques). These images should be obtained before administering the spasmolytic drug, which improves evaluation of the motility of the bowel and enables differentiation between fibrotic and inflammatory strictures [9].

The diagnostic power of the markers was determined through a logistic regression analysis when differentiating between the Montreal behavioral classes (Table 1). Small bowel CD type and various subtypes were diagnosed and presented through forest plots based on sensitivity, specificity, and ROC curves with respect to the use of MRE. The aggregate sensitivity and specificity of MRE in assessing CD type and subtype was 67.78% and 61.88%, respectively, while the aggregate sensitivity and specificity for endoscopy was 64.15% and 62.05%, respectively.

Table 1 Sensitivity and specificity of predicting disease type or subtype

Correlation of MRI with disease activity

The studies presented in Table 2 were added to perform the indices revalidation. Variable outcomes have been shown by validating the studies on the ability of the indices to detect active disease. By contrast, there is considerable inconsistency between gold standards, evaluated bowel segment, and validating studies’ methods, making it difficult to draw firm conclusions on the capacity of these indices to reflect disease activity levels.

Table 2 Sensitivity and specificity of detecting CD activity

Small bowel CD activity determined through the use of MRE was presented through forest plots based on sensitivity, specificity, and ROC curves. The aggregate sensitivity and specificity of MRE in assessing CD activity was 79.25% and 74.25%, respectively.

Discussion

Thia et al. based study on the evolution of Crohn's disease reported 19% of patients with known penetrating or stricturing complications within the first 90 days of diagnosis based on Montreal classification, while patients diagnosed with non-stricturing and non-penetrating disease at baseline had intestinal complication on progression, 76.7% of these patients required bowel resection surgery [3].

Penetrating disease, hospitalization for flares or consequences of the illness, surgery, extra-intestinal manifestations (EIMs) affecting two systems, or poor response to presently available medications are all signs of aggressive CD [41].

The current systematic study is the largest systematic study of MRI for small bowel identification in CD. Previous research and reviews looked at the sensitivity and specificity of MR imaging in detecting small bowel movement [42, 43]. We focused only on the small bowel.

The gold standard diagnostic approach for assessing intra- and extra-luminal CD complications is MR imaging (Fistula, abcess and stenosis). For the identification of stenosis, we discovered a high specificity with a moderate sensitivity. Previously, studies found a high detection rate for stenosis in both small and large bowel illness [24, 44] CT imaging may be beneficial, according to Qiu et al. for fistulas and stenosis detection but with no statistical significance and sensitivity and specificity were comparable to published studies [45, 46]. Qiu et al. found results for stenosis that were similar to ours (sensitivity 65.3%, specificity 94.4%).

The lack of uniformity of imaging indications suggestive of ongoing illness, especially with the expanding number of sequences available, is one of the challenges in replacing the gold standard with MR imaging. Previous research has shown that wall enhancement, mucosal lesions, and wall T2 hyperintensity are the most reliable indications of inflammation for MR [43, 44]. Additionally, a study by Udayasankar et al. found similar results in both the small and large bowel [45]. Diffusion-weighted MRI sequences have also been demonstrated to have good sensitivity and specificity in previous investigations [46, 47]. Recently, validated scoring systems have been developed, such as the MaRIA (Magnetic Resonance Index of Activity) score for assessing disease activity and severity, and the Lemann score, or Crohn's Disease Digestive Damage Score, which considers a variety of factors (clinical, endoscopic, and imaging findings) and attempts to measure cumulative damage [48, 49].

If the results of MR imaging influence physician management, this is a significant factor. Mendoza et al. found that MR aided decision-making in more than half of patients, particularly when biological treatments and surgery were involved [50]. Messaris et al. showed that 69% of patients had changes to medical and/or surgical management after clinicians were given MR imaging results [51]. Similar results have shown that MR findings influence surgical approaches to managing Crohn's patients [52].

Many researches looked at the use of ultrasound and computed tomography as alternate imaging modalities. Ultrasound has the advantage of avoiding ionising radiation and being very affordable [53]. Previous studies assessing ultrasound have demonstrated high sensitivities and specificities. There is one large-scale trial comparing US and MR currently in progress: the UK-based MR Enterography or Ultrasound in Crohn's disease (METRIC) trial [53,54,55]. Similarly, one meta-analysis has shown similar accuracy between CT and MR. CT has the benefit of being widely available and cost-effective. It, however, also carries the risk of ionizing radiation, especially amongst patients who might require multiple scans throughout the course of their life-long disease [56].

Limitations

This review may be limited in terms of the varied lengths of time between MRI and the reference standard. Thus, some of the findings might be nominally inaccurate in determining disease activity because clinical activity can change relatively quickly, particularly with the use of medication. This article could not differentiate between severity of small bowel activity and other clinical features, owing to a lack of data. A number of other studies have recommended that MRI has better association with CD severity indices [32, 40]. Also, per-segment analysis was not performed, which might have led to an overestimation of MRI accuracy. This may be a product of the use of endoscopy as a reference standard and its unsuitability in assessing added proximal small intestine. Another limitation was that only one complication was analyzed in the studies, and others were not well visualized. This review was not able to determine whether additional advanced MRI may have had an advantage over other methods owing to the small number of studies that provided relevant information.

Conclusion

This review has shown the effectiveness of MRE in detecting CD, and illustrated its considerable accuracy in detecting disease activity: a MARIA score found it to be the most sensitive and specific tool. MRE was able to predict disease types and subtypes to a high degree of accuracy, permitting radiologists to initiate a selection of the disease type or subtype from MRI features. However, radiologists may need to provide the essential characteristics of the disease in arriving at a final diagnosis of disease types and subtypes, because the sensitivity and specificity of MRE are not high enough to determine these accurately, specifically in comparison with endoscopic techniques.

Availability of data and material

The data will be available for review from the corresponding author on request.

Abbreviations

CD:

Chron’s disease

CDAI:

Crohn's Disease Activity Index

CDMI:

Crohn Disease MRI Index

CMA:

Comprehensive meta-analysis software

IBD:

Inflammatory Bowel disease

MaRIA:

Magnetic resonance index of activity

MEGS:

Magnetic resonance enterography global score

MRE:

Magnetic resonance enterography

MRI:

Magnetic resonance imaging

PRISMA:

Preferred reporting items for systematic reviews and meta-analysis

QUADAS:

Quality assessment of diagnostic accuracy studies

ROC:

Receiver-operating characteristic

References

  1. 1.

    Mkoma AE (2013) Inflammatory bowel disease: an expanding global health problem. Clin Med Insights Gastroenterol 6:12731. https://doi.org/10.4137/CGast.S12731

    Article  Google Scholar 

  2. 2.

    Ye Y, Pang Z, Chen W, Ju S, Zhou C (2015) The epidemiology and risk factors of inflammatory bowel disease. Int J Clin Exp Med 12:22529

    Google Scholar 

  3. 3.

    Thia KT, Sandborn WJ, Harmsen WS, Zinsmeister AR, Loftus EV Jr (2010) Risk factors associated with progression to intestinal complications of Crohn’s disease in a population-based cohort. Gastroenterology 139:1147–1155. https://doi.org/10.1053/j.gastro.2010.06.070

    Article  PubMed  Google Scholar 

  4. 4.

    Xu XR, Liu CQ, Feng BS, Liu ZJ (2014) Dysregulation of mucosal immune response in pathogenesis of inflammatory bowel disease. World J Gastroenterol 220:3255–3264. https://doi.org/10.3748/wjg.v20.i12.3255

    CAS  Article  Google Scholar 

  5. 5.

    Peyrin-Biroulet L, Panés J, Sandborn WJ et al (2016) Defining disease severity in inflammatory bowel diseases: current and future directions. Clin Gastroenterol Hepatol 14:348–354. https://doi.org/10.1016/j.cgh.2015.06.001

    Article  PubMed  Google Scholar 

  6. 6.

    Eszter Müller K, Laszlo Lakatos P, Papp M, Veres G (2014) Incidence and Paris classification of pediatric inflammatory bowel disease. Gastroenterol Res Pract. https://doi.org/10.1155/2014/904307

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Li Y, Chen B, Gao X et al (2019) Current diagnosis and management of Crohn’s disease in China: results from a multicenter prospective disease registry. BMC Gastroenterol 19:2–14. https://doi.org/10.1186/s12876-019-1057-2

    CAS  Article  Google Scholar 

  8. 8.

    Bettenworth D, Nowacki TM, Cordes F, Buerke B, Lenze F (2016) Assessment of stricturing Crohn’s disease: current clinical practice and future avenues. World J Gastroenterol 22:1008–1016. https://doi.org/10.3748/wjg.v22.i3.1008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Yoon K, Chang KT, Lee HJ (2015) MRI for Crohn’s disease: present and future. Biomed Res Int. https://doi.org/10.1155/2015/786802

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Moy MP, Sauk J, Gee MS (2016) The role of MR enterography in assessing Crohn’s disease activity and treatment response. Gastroent Res Pract. https://doi.org/10.1155/2016/8168695

    Article  Google Scholar 

  11. 11.

    Rozendorn N, Amitai MM, Eliakim RA, Kopylov U, Klang E (2018) A review of magnetic resonance enterography-based indices for quantification of Crohn’s disease inflammation. Therap Adv Gastroenterol 11:1756284818765956

    Article  Google Scholar 

  12. 12.

    Ye YX, Ju SS, Huang W, Lin WW (2019) The value of Clermont score in detection intestinal mucosal ulcer of Crohn’s disease. Zhonghua Yi Xue Za Zhi 99:2293–2296

    CAS  PubMed  Google Scholar 

  13. 13.

    Williet N, Jardin S, Roblin X (2020) The simplified magnetic resonance index of activity (MARIA) for Crohn’s disease is strongly correlated with the MARIA and Clermont Score: an external validation. Gastroenterology 158:282–283. https://doi.org/10.1053/j.gastro.2019.08.061

    Article  PubMed  Google Scholar 

  14. 14.

    Buisson A, Joubert A, Montoriol PF et al (2013) Diffusion-weighted magnetic resonance imaging for detecting and assessing ileal inflammation in Crohn’s disease. Aliment Pharmacol Ther 37:537–545. https://doi.org/10.1111/apt.12201

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Steward MJ, Punwani S, Proctor I et al (2012) Non-perforating small bowel Crohn’s disease assessed by MRI enterography: derivation and histopathological validation of an MR-based activity index. Eur J Radiol 81:2080–2088. https://doi.org/10.1016/j.ejrad.2011.07.013

    Article  PubMed  Google Scholar 

  16. 16.

    Pariente B, Cosnes J, Danese S et al (2011) Development of the Crohn’s disease digestive damage score, the Lemann score. Inflamm Bowel Dis 17:1415–1422

    Article  Google Scholar 

  17. 17.

    Hoggard N, Wilkinson ID, Griffiths PD (2001) The imaging of ischaemic stroke. Clin Radiol 56:171–183. https://doi.org/10.1053/crad.2000.0619

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Oto A, Zhu F, Kulkarni K et al (2009) Evaluation of diffusion-weighted mr imaging for detection of bowel inflammation in patients with Crohn’s disease. Acad Radiol 16:597–603. https://doi.org/10.1016/j.acra.2008.11.009

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Ninivaggi V, Missere M, Restaino G et al (2016) MR-enterography with diffusion weighted imaging: ADC values in normal and pathological bowel loops, a possible threshold ADC value to differentiate active from inactive Crohn’s disease. Eur Rev Med Pharmacol Sci 20:4540–4546

    CAS  PubMed  Google Scholar 

  20. 20.

    Dohan A, Taylor S, Hoeffel C et al (2016) Diffusion-weighted MRI in Crohn’s disease: current status and recommendations. J Magn Reson Imaging 44:1381–1396. https://doi.org/10.1002/jmri.25325

    Article  PubMed  Google Scholar 

  21. 21.

    Klang E, Kopylov U, Eliakim R et al (2017) Diffusion-weighted imaging in quiescent Crohn’s disease: correlation with inflammatory biomarkers and video capsule endoscopy. Clin Radiol 72(798):e7–e13. https://doi.org/10.1016/j.crad.2017.04.006

    Article  Google Scholar 

  22. 22.

    Kim JS, Jang HY, Park SH et al (2017) MR enterography assessment of bowel inflammation severity in Crohn disease using the MR index of activity score: modifying roles of DWI and effects of contrast phases. AJR Am J Roentgenol 208:1022–1029. https://doi.org/10.2214/ajr.16.17324

    Article  PubMed  Google Scholar 

  23. 23.

    Hordonneau C, Buisson A, Scanzi J et al (2014) Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn’s disease: validation of quantitative index of activity. Am J Gastroenterol 109:89–98. https://doi.org/10.1038/ajg.2013.385

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Rimola J, Alvarez-Cofino A, Perez-Jeldres T et al (2017) Comparison of three magnetic resonance enterography indices for grading activity in Crohn’s disease. J Gastroenterol 52:585–593. https://doi.org/10.1007/s00535-016-1253-6

    Article  PubMed  Google Scholar 

  25. 25.

    Lunder AK, Jahnsen J, Bakstad LT et al (2018) Bowel damage in patients with long-term Crohn’s disease, assessed by magnetic resonance enterography and the Lemann Index. Clin Gastroenterol Hepatol 16:75-82.e5. https://doi.org/10.1016/j.cgh.2017.06.053

    Article  PubMed  Google Scholar 

  26. 26.

    Tielbeek JA, Makanyanga JC, Bipat S et al (2013) Grading Crohn disease activity with MRI: interobserver variability of MRI features, MRI scoring of severity, and correlation with Crohn disease endoscopic index of severity. AJR Am J Roentgenol 201:1220–1228. https://doi.org/10.2214/ajr.12.10341

    Article  PubMed  Google Scholar 

  27. 27.

    Rimola J, Alvarez-Cofino A, Perez-Jeldres T et al (2017) Increasing efficiency of MRE for diagnosis of Crohn’s disease activity through proper sequence selection: a practical approach for clinical trials. Abdom Radiol (NY) 42:2783–2791. https://doi.org/10.1007/s00261-017-1203-7

    Article  Google Scholar 

  28. 28.

    Pomerri F, Al Bunni F, Zuliani M et al (2017) Assessing pediatric ileocolonic Crohn’s disease activity based on global MR enterography scores. Eur Radiol 27:1044–1051

    Article  Google Scholar 

  29. 29.

    Kang B, Choi SY, Chi S et al (2017) Baseline wall thickness is lower in mucosa-healed segments 1 year after infliximab in pediatric Crohn disease patients. J Pediatr Gastroenterol Nutr 64:279–285. https://doi.org/10.1097/mpg.0000000000001222

    Article  PubMed  Google Scholar 

  30. 30.

    Stoppino LP, Della Valle N, Rizzi S et al (2016) Magnetic resonance enterography changes after antibody to tumor necrosis factor (anti-TNF) alpha therapy in Crohn’s disease: correlation with SES-CD and clinical-biological markers. BMC Med Imaging 16:37. https://doi.org/10.1186/s12880-016-0139-7

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Makanyanga JC, Pendsé D, Dikaios N et al (2014) Evaluation of Crohn’s disease activity: initial validation of a magnetic resonance enterography global score (MEGS) against faecal calprotectin. Eur Radiol 24:277–287. https://doi.org/10.1007/s00330-013-3010-z

    Article  PubMed  Google Scholar 

  32. 32.

    Rimola J, Ordas I, Rodriguez S et al (2011) Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis 17:1759–1768. https://doi.org/10.1002/ibd.21551

    Article  PubMed  Google Scholar 

  33. 33.

    Baliyan V, Das CJ, Sharma R et al (2016) Diffusion weighted imaging: technique and applications. World J Radiol 8:785–798. https://doi.org/10.4329/wjr.v8.i9.785

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Masselli G, Perrone G, Kinkel K et al (2016) Are second trimester apparent diffusion coefficient values of the short uterine cervix associated with impending preterm delivery? Radiology 280(3):897–904

    Article  Google Scholar 

  35. 35.

    Lee JK, Stein SL (2014) Radiographic and endoscopic diagnosis and treatment of enterocutaneous fistulas. Clin Colon Rect Surg 23:149–160

    Article  Google Scholar 

  36. 36.

    Mantarro A, Scalise P, Guidi E, Neri E (2017) Magnetic resonance enterography in Crohn’s disease: how we do it and common imaging findings. World J Radiol 9:46–54. https://doi.org/10.4329/wjr.v9.i2.46

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Ahmed O, Rodrigues DM, Nguyen GC (2016) Magnetic resonance imaging of the small bowel in Crohn’s disease: a systematic review and meta-analysis. Can J Gastroenterol Hepatol. https://doi.org/10.1155/2016/7857352

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Laass MW, Roggenbuck D, Conrad K (2014) Diagnosis and classification of Crohn’s disease. Autoimmun Rev 13:467–471. https://doi.org/10.1016/j.autrev.2014.01.029

    Article  PubMed  Google Scholar 

  39. 39.

    Sinha R, Verma R, Verma S, Rajesh A (2011) MR enterography of Crohn disease: part 1, rationale, technique, and pitfalls. AJR Am J Roentgenol 197(1):76–79

    Article  Google Scholar 

  40. 40.

    Ordás I, Rimola J, Alfaro I et al (2019) Development and validation of a simplified magnetic resonance index of activity for Crohn’s disease. Gastroenterology 157:432–439

    Article  Google Scholar 

  41. 41.

    Lewis JD, Chuai S, Nessel L et al (2008) Use of the noninvasive components of the Mayo score to assess clinical response in ulcerative colitis. Inflamm Bowel Dis 14:1660–1666

    Article  Google Scholar 

  42. 42.

    Wu LM, Xu JR, Gu HY et al (2013) Is magnetic resonance imaging a reliable diagnostic tool in the evaluation of active Crohn’s disease in the small bowel? J Clin Gastroenterol 47(4):328–338. https://doi.org/10.1097/MCG.0b013e31825d5034

    Article  PubMed  Google Scholar 

  43. 43.

    Church P, Turner D, Walters T et al (2012) A systematic review of MR enterography signs of inflammation and damage in Crohn’s disease. J Crohns Colitis 6(supplement 1):S84. https://doi.org/10.1016/S1873-9946(12)60208-6

    Article  Google Scholar 

  44. 44.

    Lasocki A, Pitman A, Williams R et al (2013) Relative efficacy of different MRI signs in diagnosing active Crohn’s disease, compared against a histological gold standard. J Med Imaging Radiat Oncol 55(1):11–19. https://doi.org/10.1111/j.1754-9485.2010.02223.x

    Article  Google Scholar 

  45. 45.

    Udayasankar UK, Martin D, Lauenstein T et al (2008) of spectral presaturation attenuated inversion-recovery fat-suppressed T2-weighted MR imaging in active inflammatory bowel disease. J Magn Reson Imaging 28(5):1133–1140. https://doi.org/10.1002/jmri.21574

    Article  PubMed  Google Scholar 

  46. 46.

    Tielbeek JAW, Ziech MLW, Li Z et al (2014) Evaluation of conventional, dynamic contrast enhanced and diffusion weighted MRI for quantitative Crohn’s disease assessment with histopathology of surgical specimens. Eur Radiol 24(3):619–629. https://doi.org/10.1007/s00330-013-3015-7

    Article  PubMed  Google Scholar 

  47. 47.

    Oussalah A, Laurent V, Bruot O et al (2010) Diffusion-weighted magnetic resonance without bowel preparation for detecting colonic inflammation in inflammatory bowel disease. Gut 59(8):1056–1065. https://doi.org/10.1136/gut.2009.197665

    Article  PubMed  Google Scholar 

  48. 48.

    Pariente B, Cosnes J, Danese S et al (2011) Development of the Crohn’s disease digestive damage score, the Lémann score. Inflamm Bowel Dis 17(6):1415–1422. https://doi.org/10.1002/ibd.21506

    Article  PubMed  Google Scholar 

  49. 49.

    Rimola J, Rodriguez S, García-Bosch O et al (2009) Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn’s disease. Gut 58(8):1113–1120. https://doi.org/10.1136/gut.2008.167957

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Mendoza JL, González-Lama Y, Taxonera C et al (2012) Using of magnetic resonance enterography in the management of Crohn’s disease of the small intestine: first year of experience. Rev Esp Enferm Dig 104(11):578–583. https://doi.org/10.4321/s1130-01082012001100005

    Article  PubMed  Google Scholar 

  51. 51.

    Messaris E, Chandolias N, Grand D et al (2010) Role of magnetic resonance enterography in the management of Crohn disease. Arch Surg 145(5):471–475. https://doi.org/10.1001/archsurg.2010.68

    Article  PubMed  Google Scholar 

  52. 52.

    Spinelli A, Fiorino G, Bazzi P et al (2014) (2014) Preoperative magnetic resonance enterography in predicting findings and optimizing surgical approach in Crohn’s disease. J Gastrointest Surg 18(1):83–91. https://doi.org/10.1007/s11605-013-2404-1

    Article  PubMed  Google Scholar 

  53. 53.

    Panés J, Bouzas R, Chaparro M et al (2011) Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther 34(2):125–145. https://doi.org/10.1111/j.1365-2036.2011.04710.x

    Article  PubMed  Google Scholar 

  54. 54.

    Taylor S, Mallett S, Bhatnagar G et al (2014) METRIC (MREnterography or ulTRasound in Crohn’s disease): a study protocol for a multicentre, non-randomised, single-arm, prospective comparison study of magnetic resonance enterography and small bowel ultrasound compared to a reference standard in those aged 16 and over. BMC Gastroenterol. https://doi.org/10.1186/1471-230x-14-142

    Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Buisson A, Joubert A, Montoriol PF et al (2013) weighted magnetic resonance imaging for detecting and assessing ileal inflammation. Aliment Pharmacol Ther 37(5):537–545. https://doi.org/10.1111/apt.12201

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Qiu Y, Mao R, Chen BL et al (2014) Systematic review with meta-analysis: magnetic resonance enterography vs. computed tomography enterography for evaluating disease activity in small bowel Crohn’s disease. Aliment Pharmacol Ther 40(2):134–146

    CAS  Article  Google Scholar 

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Acknowledgements

The authors acknowledge all the associated personnel who contributed in the completion of this study. The authors declare that this study is self-funded and includes no conflicts of interest.

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Ahmad, R., Ajlan, A.M., Eskander, A.A. et al. Magnetic resonance imaging in the management of Crohn’s disease: a systematic review and meta-analysis. Insights Imaging 12, 118 (2021). https://doi.org/10.1186/s13244-021-01064-9

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Keywords

  • Magnetic resonance imaging
  • Radiation
  • Crohn disease
  • Treatment