Dr. Jordi Rimola Gibert
Hospital Universitari Clínic. Barcelona
II.2.2.1. Computed tomography and magnetic resonance enterography Role in the diagnosis and monitoring of inflammatory bowel disease
The use of imaging techniques to assess patients with Crohn’s disease (CD) has changed dramatically in recent years. Computed tomography (CT enterography) and magnetic resonance (MR enterography) enterography have several advantages over traditional barium radiology tests, such as:
• Better assessment of the location, extent and number of diseased segments.
• Better detection and characterisation of obstructive lesions.
• More accurate assessment of disease activity based on the presence or absence of signs of mural inflammation.
• Added advantage of detecting extramural complications1-3.
The role of CT enterography or MR enterography has been extensively reviewed in different scenarios4. In clinical practice, both techniques enable the non-invasive examination of patients with suspected or diagnosed CD, providing information at the time of diagnosis or during follow-up while complementing clinical and endoscopic findings5. Ultrasound should be included under the umbrella of cross-sectional imaging, but its role in the assessment of CD patients will be discussed in a separate section.
The introduction of CT and MR in the diagnostic algorithm and in the follow-up of patients with CD was largely made possible by the remarkable technological improvements that both approaches have experienced over the past decade. In the field of CT, the advent of multi-detector equipment and its implementation have been crucial for the introduction of CT enterography as a diagnostic tool, allowing faster, more consistent and higher-resolution image acquisition, thus allowing multi-planar reconstruction. Meanwhile, irradiation modulation or reduction systems have also been optimised, an important aspect considering the high number of young patients with CD who may potentially require reassessments of their condition.
Technological advances in the field of MR have allowed improvements in magnetic fields; their increased power now produces high spatial resolution images and rapid acquisition sequences have been developed, which can scan the entire abdominal cavity in a short time and with a very thin thickness.
This chapter describes the current concepts of CD activity and severity using CT and MR, the typical findings yielded by these techniques in the different subtypes of CD, and their potential utility with regard to the therapeutic monitoring and follow-up of these patients, as well as other future prospects.
ROLE OF COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IN THE DIAGNOSIS OF CROHN’S DISEASE AND ITS EXTENSION
The definitive diagnosis of CD relies on endoscopic, histological and radiological findings consistent with the clinical suspicion of CD. There is limited information concerning the utility of cross-sectional imaging techniques in the diagnosis of CD, and these are limited to MR enterography and ultrasound1,6-8. The sensitivity and specificity per patient of MR enterography in the diagnosis of inflammatory lesions in patients ultimately diagnosed with CD were, respectively, 79% and 87.5%3. The severity of inflammatory lesions and their location are two important factors when establishing the image-based diagnosis of CD. The probability of a final diagnosis of CD was higher in patients who showed more severe signs in MRI studies such as mural thickening, greater uptake of intravenous contrast and wall oedema1,7,8.
The accuracy of CT and MR enterography in the diagnosis of CD in patients with inflammatory lesions in the proximal and mid segments of the small intestine is significantly lower than in patients with lesions that are located in the distal or terminal ileum.
In more proximal lesions, capsule endoscopy (CE) or enteroscopy have shown greater diagnostic accuracy in establishing the presence of CD than either CT or MR enterography9,10. However, CT or MR enterography and CE may be regarded as complementary approaches in the diagnosis of Crohn’s disease of the small intestine, since radiological techniques enable the detection of lesions that CE might overlook and vice versa, such as penetrating lesions11. There are no published studies directly comparing MRI and CT in the diagnosis of CD.
The location of inflammatory lesions in CD is very stable and constant over time, in accordance with the disease classification12. The extent of CD in the colon and terminal ilium determined via CT and MR shows a strong correlation with the extension observed via ileocolonoscopy13-15. It is important to note that poor luminal distension of the intestine or colon can lead to errors in the accuracy of CT and MRI in determining the extension of lesions in CD, which may explain the divergent results observed in studies assessing the extension of CD using cross-sectional imaging techniques, which shows a better correlation with endoscopy in series where the colon was intentionally distended16-20.
The only study that has directly compared CT and MR enterography to evaluate the extension of CD found no significant difference between the two approaches15.
DETECTION OF ACTIVITY AND DETERMINATION OF THE SEVERITY OF THE LESIONS IN CROHN’S DISEASE USING COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING
Detection of inflammatory activity
Signs of activity in CD detected by either CT enterography or MR enterography (Fig. 1) are widely described in the literature and include:
• Intestinal wall thickening.
• Greater mural enhancement after the administration of intravenous contrast.
• Mural stratification.
• Irregular outer edges.
• Perienteric fat involvement.
• Mesenteric congestion of the vessels supplying the diseased bowel segment.
• Lymph node enlargement or increased uptake have likewise often been used as criteria for activity2,5,7,11,13-16,18,20-24.
• Typically, CD may also show multiple zones where healthy-looking segments alternate with diseased ones, which may be at different stages of disease. Some studies suggest that altered motility in the loops of the small intestine, whether qualitative or measured by quantification using specific software, may be useful to detect segments exhibiting inflammatory activity (Video 1)25,26.
The increase in mural attenuation and intestinal wall thickness, perienteric vascularisation and regional lymph node enlargement on CT enterography all correlate with endoscopic and histological findings of inflammatory activity in CD2,27.
In the field of MR enterography, increased mural thickness and uptake of intravenous contrast, whether diffuse or limited to the mucosa, have proven to be independent predictors of inflammatory activity, using endoscopic activity in the terminal ileum and/or colon as an dependent variable19,20,26,28. In order to avoid false positives and negatives, it is worth stressing the importance of proper luminal distension in order to properly assess whether a segment exhibits criteria of activity 17,29. In another study, a hyperintense wall in the diffusion sequence also showed an independent predictive value for detecting inflammatory lesions in an endoscopy. In the same study, a hyperintense signal on diffusion was the most sensitive finding with respect to the detection of inflammatory activity in intestinal segments in CD patients, although its specificity was more limited19. The diffusion sequence reflects the extent of the Brownian motion of water molecules in biological tissues. Said motion may be restricted in tissues with high cell density, such as tumours or inflammatory tissues, which translated into signal enhancement on resonance images. The potential impact of fibrosis deposition in the gut on the diffusion signal is unknown30.
Both CT enterography and MR enterography show high sensitivity and specificity in detecting intestinal segments with inflammatory activity. A recent systematic review of the literature reported a sensitivity and specificity of 79% and 90%, respectively, for CT enterography, vs 70% and 89% for MR enterography3,31. The differences observed between the two techniques may be explained by the fact that only the terminal ileum was included in the CT enterography analysis, whereas MR enterography also encompassed segments of the colon that were not always distended. It is worth noting that in studies directly comparing the two techniques in the same patients, no significant differences were identified in terms of activity detection, nor when individually analysing each of the evaluated findings (Fig. 2)2,15,23.
Determining the severity of the lesions
Determining the severity of lesions is probably the most important factor in establishing the best therapeutic strategy. Treatment adjustments (whether stepping up or stepping down) should be based on objective measures of disease activity, not just on the symptoms. In the field of research, the primary objective set in many recent clinical trials has been mucosal healing rather than symptom control.
The quantification of bowel wall attenuation after the intravenous administration of iodinated contrast in CT enterography correlates with the severity of endoscopic lesions32. The use of MR enterography for the determination of lesion severity has been extensively evaluated by means of multiple indices based on imaging findings11,20,21,25,26,33-37.
The introduction of multi-parameter indices that include multiple imaging findings as opposed to merely assessing severity subjectively (visual impression of the radiologist) aims to minimise inter- and intra-reader variability, which will help standardise the assessment of response to pharmacotherapy. Most of these activity indices have been designed based on radiologist experience, with only two MR-based indices being derived from multivariate analysis, using standard technique-based indices (endoscopy or anatomic pathology) as dependent variables 20,26. Of these, only one has been formally validated for the terminal ileum and colon in an independent cohort of patients (MaRIA index). Its criteria for establishing severity include the determination of the mural thickness, the quantification of relative contrast enhancement, and the presence of oedema/ulcers. The combination of these four parameters showed a significant correlation with a CDEIS of 0.8 in both the derivation and the validation cohorts28. The second index (London Score) has been derived specifically for the terminal ileum and includes mural thickness, the T2 mural signal, the extent of mural uptake and the T2 perienteric fat signal. The combination of these four parameters showed a significant correlation with a histological inflammation index of 0.4826.
Overall, no good correspondence was observed between MR-based and clinical indices (e.g. the Crohn’s disease activity index [CDAI]) nor with biomarkers3. Nonetheless, a correlation was found between C-reactive protein (CRP) levels and the identification of perienteric hypervascularisation32.
DETECTION OF COMPLICATIONS DERIVED FROM CROHN’S DISEASE USING COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROGRAPHY
Unlike the location of the lesions, the number of complications, whether stenosing or penetrating, increases over the years after diagnosis of CD12. The detection and characterisation of CD complications represent some of the most important additional information that cross-sectional imaging techniques can provide in the assessment of CD patients; the detection of said complications can affect the therapeutic management of the patient38,39.
The most widely accepted definition of intestinal stenosis is a reduction in the luminal diameter of more than 50%, with or without proximal dilatation5,40. Both CT enterography and MR enterography have an equally high sensitivity, of 89%, in detecting stenoses and both exhibit a high specificity of 99 and 94%, respectively3.
Traditionally, attempts have been made from an imaging perspective to differentiate inflammatory stenoses from fibrotic stenoses. However, in practice, both components (inflammation and fibrosis) often coexist in the same stenosed segment, and only rarely do we find either purely inflammatory or purely fibrotic stenoses (Fig. 3)27,41-43. Both CT and MR enterography have a high capacity for detecting inflammatory tissue, but to date, it has not been possible to characterise fibrosis deposition in the intestine. Two studies have shown a significant positive correlation between the histological degree of inflammation and the histological degree of fibrosis41,43, which further adds to the difficulty of accurately quantifying the degree of fibrosis in a stenosis.
In one study, the histological analysis of stenoses with signs of inflammatory activity on CT enterography showed a high level of fibrosis along with an inflammatory component; by contrast, in stenoses with no signs of inflammatory activity on CT enterography, both components were also identified in the histological examination, although to a lesser degree than in stenoses with signs of activity43. There are also a limited number of studies linking MR enterography findings with histological examination after intestinal resection, and MRI findings that have been associated with fibrosis are discrepant between studies41,42. Analysis of the increase in uptake over time, or the introduction of new abdominal MRI sequences, such as magnetisation transfer, represent potential alternatives to a simple analysis of morphological findings44. Identifying and especially quantifying fibrosis remains important from a clinical perspective, since the stenosing lesions that accompany obstructive symptoms have shown poor response to medical treatment on imaging45.
Finally, apart from yielding a map of the number and location of stenoses, both CT enterography and MR enterography can provide information on their extent and morphology, which is key with regard to selecting patients eligible for endoscopic dilation.
Penetrating complications include fistulas and/or abscesses40. The cumulative incidence of penetrating CD is 33% at 10 years and 50% at 20. The most common fistula in CD is perianal (54%), followed by enteroenteric (24%), rectovaginal (9%) and others (13%)46.
At the advanced stages of inflammation, deep ulcers may progress and penetrate either to the muscular layer or through the actual muscular layer and the serosa, resulting in adjacent perienteric tissue inflammation in the form of blind fistulas, which are precursors to fistulising disease or inflammatory masses. Both situations can be complicated by abscess formation47.
Both CT and MR enterography have proven more sensitive than clinical, endoscopic and barium studies in detecting penetrating complications. The sensitivity of CT enterography and MR enterography in detecting fistulas was 78 and 85%, respectively, and the specificity was 97 and 99%. Most studies directly comparing the two techniques found no differences in their ability to detect penetrating lesions 2,15,48; however, MR enterography appeared slightly more accurate than CT enterography in the study by Siddiki23. At approximately 95%, the two approaches were likewise highly and similarly accurate in terms of abscess detection3.
MONITORING OF THERAPEUTIC RESPONSE AND CROHN’S DISEASE
The evaluation of mucosal healing has prognostic value, since it has been reported that patients who achieved it on endoscopy showed more sustained clinical remission during follow-up than those who had not. Moreover, the first group required fewer surgical procedures and hospitalisations than the second49. CT enterography and MR enterography can detect improvements in intestinal wall lesions (wall thinning, improvement of stratification, disappearance of oedema and reduction in wall enhancement) until the intestinal wall fully returns to normal.
A retrospective study by Hara et al., which included 20 patients with CD, found a correlation between changes observed on CT enterography (relating to mural thickness, mucosal enhancement, and stenosing and penetrating complications) and changes in symptoms in 80% of subjects50. In another retrospective study by Bruning et al., changes were retrospectively analysed in 67 patients with lesions in 105 segments treated with infliximab. The radiological evolution based on changes in uptake, hypervascularisation, stratified uptake, segment length and fat proliferation, showed a poor correlation with symptoms, endoscopic appearance and biomarkers (such as CRP)
(κ = 0.26, 0.07 and 0.30, respectively)51.
In a recent multi-centre study, MR enterography was used to analyse changes in the ileum after treatment with infliximab at two weeks and six months using a predefined index in 20 patients with active ileal CD and elevated CRP. While ileal obstructive lesions showed no improvement after treatment, in the remaining segments, changes were already identifiable at two weeks. A correlation with CDAI was identified at both two weeks and six months, but this was not the case with CRP45. The preliminary results of another study that used the MaRIA index to predict endoscopic mucosal healing in colon segments and the terminal ileum over 12 weeks of treatment with anti-TNF drugs or corticosteroids found MR enterography to have a sensitivity and specificity of 84% and 82% for endoscopic remission, and 85% and 78%, respectively, for the absence of lesions52.
In the context of research, the use of objective indices to determine disease activity and severity, treatment response and long-term results is an absolute requirement. In trials assessing the therapeutic benefits for the treatment of active disease, the results should ensure the inclusion of patients who exhibit active inflammation of a certain severity; also, excluding patients with symptoms that do not relate to the presence of inflammation would enable the recruitment of a homogeneous population while reducing the placebo effect. For research purposes, the inclusion of CT or MR enterography may provide relevant additional information compared with endoscopy. Given the low sensitivity and specificity of the clinical symptoms of stenotic lesions, detection via imaging techniques can also be key to avoiding the inclusion of patients whose symptoms may be attributable to obstructive lesions. It is also important to detect penetrating lesions, which may affect between 5–16% of the population with CD, so as to allow for the exclusion of patients with such lesions, which can deteriorate under intense immunosuppression38,39,53.
Follow-up should take into consideration that CD is a chronic and destructive disease that causes the progressive loss of intestinal structures and their function.
An international cooperation initiative is currently actively developing a tool capable of measuring cumulative intestinal damage, which takes into account the location of the damage and its severity, extension, progression and reversibility, as measured by CT and MR enterography54. This index is expected to allow disease progression to be measured from the time of diagnosis (Lemann index). This type of measurement is necessary for the development of long-term trials intended to assess the ability of a therapeutic strategy to alter the course of the disease, separating the beneficial short-term effects on symptoms that a certain treatment can provide.
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