Magnetic resonance enterography, small bowel ultrasound and colonoscopy to diagnose and stage Crohn’s disease: patient acceptability and perceived burden

Cross-sectional imaging plays a crucial role in the diagnosis and follow-up of Crohn’s disease (CD), and is fundamental to determine disease extent, activity and complications [1]. Although many techniques are available, emphasis is placed on MR enterography (MRE) and small bowel ultrasound (US) given the potential detrimental effects of repeated ionising radiation exposure associated with CT [1, 2]. Meta-analyses suggest that MRE and US are largely equivalent in terms of accuracy, although most comparative studies to date have been relatively small and single site [3‐5], and implementation has been governed largely by availability, local expertise and clinician preference [6, 7]. However the results of the METRIC trial, a large prospective multicentre diagnostic accuracy study, have shown that although both MRE and US have high accuracy for the extent and activity of small bowel Crohn’s disease, MRE is superior to US when tested in a national health service setting [8, 9].

Patient experience and acceptability will influence test utility. While MRE and US avoid radiation, they have their own specific attributes which may impact on tolerance. For example, patients must ingest large volumes of oral contrast for MRE, and US requires abdominal compression. Patients’ perceptions of test “burden” (levels of physical and psychological discomfort) can impact on compliance, even if the test is diagnostically superior to alternatives, as exemplified by low uptake of colorectal cancer screening colonoscopy [10]. This diminishes test utility. Indeed, patients may delay seeking medical attention, fearing the discomfort associated with procedures such as colonoscopy [11]. To date little data reports imaging test preferences amongst patients with CD, and available data largely compares now largely obsolete investigations such as barium enema and enteroclysis [1].

The purpose of our study was to compare the perceived burden and acceptability of MRE to US, and to other enteric investigations in patients recruited to the METRIC trial [8], to identify predictors of scan preference and to determine the perceived importance of different scan attributes.

Ethical approval for the METRIC trial (including the current study) was obtained from the National Health Service Research Ethics Committee (NHS REC) in September 2013 (ref: 13/SC/0394).

Participant characteristics are shown in Table 1. Just under half of participants who consented to complete a questionnaire actually did so (159/ 324, 49%). Participants completing the questionnaire were significantly older than non-responders (mean age, 38.2 vs. 33.8 years; t = 2.603, p = 0.010), but there were no gender differences between groups (chi-square = 1.606, p = 0.205) or whether the patient was newly diagnosed or relapsing (chi-square = 1.763, p = 0.184).

There were no significant differences in demographics, educational level, ethnicity, presence of comorbidities or prevalence of significant psychological distress between those with newly diagnosed CD or suspected relapse. Overall, rates of psychological distress were high, with 48% reporting clinically significant levels (Table 1).

The median number of days between patients undergoing the MRE scan and completing the questionnaire was 7 (range 0–326; 46.6 weeks). The median number of days between patients undergoing the US scan and completing the questionnaire was 6 (range 0–326). The proportion who completed the questionnaire less than 5 weeks after their MRE and US scan was 61% (n = 70) and 61% (n = 71) respectively.

The number and percentage of patients who completed the questions about scan experience across the different imaging modalities are shown in Supplementary Table 1.

While our primary focus was MRE and US, we collected data on other small bowel investigations performed as part of usual clinical care in recruited patients. Recovery time for MRE was significantly longer than for CTE. However, we found no significant difference in recovery time compared to BaFT. This finding may be secondary to lack of statistical power contingent on small numbers undergoing BaFT, but it is possible that the constipating effects of barium contributed to slower recovery.

In general, MRI is a challenging test for patients. Relatively long scan times, claustrophobic scanner bore and associated noise all influence patient experience negatively [17]. Using a very similar questionnaire to the present study in a sample of 115 patients [15], patient burden during whole-body MRI (WB-MRI) cancer staging was reported as actually a little better than we found for MRE (2.21 vs. 2.72) [15]. Interestingly, both studies reported that high levels of emotional distress predicted increased MRI burden, although the current study found that younger age was also associated. Indeed, a very large proportion of participants in the current study reported significant psychological distress, comparable with high rates of anxiety recently among patients with active CD [18], and reaching levels more typically reported by patients being investigated for suspected cancer [19].

It is perhaps unsurprising that most patients stated that they would choose US over MRE, and indeed MRI scans have been judged to be more challenging than other scans such as PET-CT and contrast-enhanced spectral mammography [20, 21]. One very important finding from the current study is that patients rated several scan attributes as more important than the challenges and discomfort of undergoing scans. Notably, diagnostic accuracy was the most important attribute. This is comparable to data from studies of CT colonography [22]. Patients, at least to some extent, seem tolerant of discomfort if they believe that the test is more accurate than a less arduous alternative. We did not provide differential accuracy data for the tests under investigation, and it is likely that patients assumed they are similar when selecting preferences. The METRIC study has recently reported [9] and shows that when compared prospectively, MRE has significantly higher sensitivity for extent (presence and location) of small bowel Crohn’s disease than US (80% vs. 70%). When viewed in this context, and given their emphasis on diagnostic accuracy, it seems that MRE is an acceptable first-line test for patients; although patients’ experience during MRE was inferior to US, absolute levels of scan burden were relatively low and acceptability ratings reasonable. The performance of US in the METRIC trial was, however, still good, particularly for small bowel disease presence, and the technique still undoubtedly has a major role in managing Crohn’s disease patients. It is clearly a very well tolerated test by patients and completely safe, an important attribute given the potential deleterious effect of gadolinium deposition with repeated MRE [23‐25]. Perhaps surprisingly, patients did not rate radiation exposure as particularly important, although again this may be influenced by their knowledge of this issue.

A very important consideration in questionnaire studies is the timing of the survey post intervention [26]. In a similar study comparing patient preferences for CT colonography verses colonoscopy, van Gelder et al reported that patient preference for CT colonography fell from 71% immediately after the tests to 61% 5 weeks later, and that drivers for preference switched from physical discomfort to relative diagnostic accuracy [16]. In the current study, we instructed patients to complete questionnaires after all their diagnostic tests had been completed rather than using a fixed time point [27]. The median return time in the current study was 1 week, although this ranged widely from 0 to 47 weeks. There was some evidence that after 5 weeks the perceived importance of a few attributes related to scan discomfort declined over time (although no significance was found after statistical correction). The rating of diagnostic accuracy as the priority for patients was not influenced by the time between the tests and questionnaire response, nor was overall patient scan preference, suggesting that our findings are robust.

Overall, it is clear therefore that the choice of imaging investigation should be based on a discussion between the referring clinician, radiologist and patient, considering scan attributes including diagnostic accuracy, patient experiences and priorities, and the exact underlying clinical question.

This study has limitations. Although the largest prospective study of patients’ experiences of cross-sectional imaging in Crohn’s disease to date, questionnaire response rates were under 50% despite the large majority stating that they would participate initially. However, this is consistent with questionnaire studies of similar design (e.g. [15, 28]). Non-responders were significantly younger than those who completed questionnaires, which may restrict generalisability. Postcode data were unavailable so we were unable to examine the influence of deprivation on questionnaire completion rates or scan burden/preference.

Since patients had already consented to the METRIC trial, the cohort sampled were apparently willing to undergo these tests in the first place. It would have been interesting to question those declining participation as to whether prior experience of either test had influenced their decision. We did not specifically record the experience of patients who did not complete or interrupted their imaging examination which would have been informative. In addition, some patients did not complete the questionnaire until weeks after their scan, and their recall of scan experiences may be imperfect. However, as noted above, the effect of such delay on reported experiences did not impact patient preferences. Finally, we used a variety of questionnaires, which, although comprehensive, may not fully capture the subtleties of patient experience.

In summary, both MRE and US are well tolerated generally by patients with CD, and better than colonoscopy. However, patient burden and recovery are significantly inferior for MRE compared to US. Whilst a majority of patients would opt to undergo US rather than MRE, patients rate other scan attributes, notably diagnostic accuracy, as more important than discomfort.