TY - JOUR
AU - MD, David H Bruining,
AB - Abstract Background Ileocolonoscopy and computed tomography (CT) or magnetic resonance (MR) enterography (CTE/MRE) are utilized to evaluate patients with small bowel (SB) Crohn’s disease (CD). The purpose of our study was to estimate the impact of capsule endoscopy (CE) on patient management after clinical assessment, ileocolonoscopy, and CTE/MRE. Methods We prospectively analyzed 50 adult CD patients without strictures at clinically indicated ileocolonoscopy and CTE/MRE exams. Providers completed pre- and post-CE clinical management questionnaires. Pre-CE questionnaire assessed likelihood of active SBCD and management plan using a 5-point level of confidence (LOC) scales. Post-CE questionnaire assessed alteration in management plans and contribution of CE findings to these changes. A change of ≥2 on LOC scale was considered clinically meaningful. Results Of the 50 patients evaluated (60% females), median age was 38 years, median disease duration was 3 years, and median Crohn’s Disease Activity Index (CDAI) score was 238 points. All CTE/MRE studies were negative for proximal disease. CE detected proximal disease in 14 patients (28%) with a median Lewis score of 215 points. CE findings altered management in 17 cases (34%). The most frequent provider-perceived benefits of CE were addition of new medication (29%) and exclusion of active SB mucosal disease (24%). Conclusion CE is a safe imaging modality that alters clinical management in patients with established SBCD by adding incremental information not available at ileocolonoscopy and cross-sectional enterography. Crohn disease/diagnostic imaging, Crohn disease/diagnosis, capsule endoscopy/utilization, enterography INTRODUCTION Crohn’s disease (CD) remains a clinical challenge for health care providers due to nonspecific symptoms and poor correlation between symptoms and disease activity. Furthermore, CD has a special predilection for small intestinal involvement, including regions inaccessible to standard endoscopic techniques. These features have led to the expansion of CD imaging modalities to include computed tomography enterography (CTE), magnetic resonance enterography (MRE), ultrasound, and capsule endoscopy (CE).1–7 It has become apparent that these imaging tools do not replace the need for endoscopy, but rather serve as complementary modalities by detecting small bowel (SB) inflammation and its complications not identified at ileocolonoscopy.8, 9 CTE or MRE are often performed as part of a patient’s initial assessment to determine the extent of SB disease and to assess for complications such as penetrating and stricturing disease. They also are useful to assess response to medical therapy. Several studies show that CTE, MRE, and CE influence or alter inflammatory bowel disease management plans.10–12 These data include studies reporting a change in the perception of the benefit of corticosteroid use and altered therapeutic plans in approximately 50% of patients undergoing CTE at tertiary care centers.5, 6 CE, however, has potential advantages over CTE and MRE including the ability to directly visualize the mucosa, translating into a higher sensitivity for active inflammatory CD particularly in the SB. It may be an attractive alternative to other objective imaging techniques given a lack of ionizing radiation and a high patient tolerance (no need to ingest a large volume of enteric contrast material). There is a paucity of data on how CE can complement enterography and ileocolonoscopy as part of a CD patient assessment, and no estimate of how/if incremental information detected by mucosal assessment of CE changes patient management. The primary focus of our study was to prospectively analyze how CE influenced management plans in patients who were undergoing clinically indicated CTE or MRE and ileocolonoscopy. We hypothesized that when administered safely after cross-sectional enterography, CE alters the therapeutic plans for a substantial proportion of patients with established CD undergoing disease activity assessments. The purpose of our study was therefore to estimate the impact of CE on patient management after clinical assessment, ileocolonoscopy, and CT or MR enterography. METHODS Study Design After approval by our institutional IRB, we prospectively evaluated a cohort of 50 adult outpatients with established CD without SB strictures on clinically indicated ileocolonoscopy and cross-sectional (CT/MR) enterography. Patients were recruited from the Mayo Clinic Inflammatory Bowel Diseases Clinic. Exclusion criteria are listed in Table 1. All study patients provided written informed consent. Table 1: Exclusion Criteria for Study Obstruction •History of obstructive symptoms without surgery to address lesion •Obstruction found CTE or MRE Stricture •History of retained CE •Stricture on ileocolonoscopy •Stricture on CTE or MRE Motility Disorder •History of dysphagia •History of gastrointestinal motility disorder (gastroparesis) Medical Conditions •Implanted electromedical devices •History of abdominal radiation •Pregnancy •Institutionalized or vulnerable adults Severe CD •High confidence from radiologist for any proximal SB disease •Enteric fistulas or sinus tracks (nonperianal) •Intraabdominal abscess(es) Miscellaneous •Prior CE within one 1 year of this study •NSAIDS within last 2 weeks Obstruction •History of obstructive symptoms without surgery to address lesion •Obstruction found CTE or MRE Stricture •History of retained CE •Stricture on ileocolonoscopy •Stricture on CTE or MRE Motility Disorder •History of dysphagia •History of gastrointestinal motility disorder (gastroparesis) Medical Conditions •Implanted electromedical devices •History of abdominal radiation •Pregnancy •Institutionalized or vulnerable adults Severe CD •High confidence from radiologist for any proximal SB disease •Enteric fistulas or sinus tracks (nonperianal) •Intraabdominal abscess(es) Miscellaneous •Prior CE within one 1 year of this study •NSAIDS within last 2 weeks View Large Table 1: Exclusion Criteria for Study Obstruction •History of obstructive symptoms without surgery to address lesion •Obstruction found CTE or MRE Stricture •History of retained CE •Stricture on ileocolonoscopy •Stricture on CTE or MRE Motility Disorder •History of dysphagia •History of gastrointestinal motility disorder (gastroparesis) Medical Conditions •Implanted electromedical devices •History of abdominal radiation •Pregnancy •Institutionalized or vulnerable adults Severe CD •High confidence from radiologist for any proximal SB disease •Enteric fistulas or sinus tracks (nonperianal) •Intraabdominal abscess(es) Miscellaneous •Prior CE within one 1 year of this study •NSAIDS within last 2 weeks Obstruction •History of obstructive symptoms without surgery to address lesion •Obstruction found CTE or MRE Stricture •History of retained CE •Stricture on ileocolonoscopy •Stricture on CTE or MRE Motility Disorder •History of dysphagia •History of gastrointestinal motility disorder (gastroparesis) Medical Conditions •Implanted electromedical devices •History of abdominal radiation •Pregnancy •Institutionalized or vulnerable adults Severe CD •High confidence from radiologist for any proximal SB disease •Enteric fistulas or sinus tracks (nonperianal) •Intraabdominal abscess(es) Miscellaneous •Prior CE within one 1 year of this study •NSAIDS within last 2 weeks View Large Definitions Established CD was defined as a diagnosis of CD after a previous clinical evaluation by a gastroenterologist or colorectal surgeon. Obstructive symptoms were defined as postprandial abdominal pain with nausea or vomiting. A stricture on CTE/MRE was defined a region of lumen narrowing with upstream dilation. An alteration in the management plan was identified as a change of treatment options selected by the treating provider on the pre- and postimaging forms. These changes included the addition or subtraction of a follow-up test, medication or surgical consultation, or a change in the recommended time interval for follow-up imaging. Proximal SB involvement on CTE/MRE was defined as disease in the duodenum or jejunum. A GI radiologist made this determination based on the distance from the ileocecal valve and the SB fold pattern. Extensive SB disease was defined as total disease length (combining all segments) of 10 cm or greater. Pre-Capsule Clinical and Imaging Assessment The investigator documented current symptoms and patients completed the Crohn’s Disease Activity Index (CDAI) questionnaire.13 The treating provider completed a pre-CE questionnaire (Fig. 1) after the patient had undergone an ileocolonoscopy and CT or MR enterography. Information regarding the patient’s diagnosis, location of disease, indication for imaging, and the pre-CE treatment plan was recorded. Providers also documented their level of confidence (LOC) on a 5-point scale (Fig. 2) for the presence of active SB disease and mucosal ulcerations. A change of 2 points or more on the LOC scale for any of the disease activity parameters was defined as clinically meaningful. After the CE, the treating provider completed a postprocedure questionnaire (Fig. 3) to record the management plan once CE findings were available and contribution of CE to LOC changes. FIGURE 1. View largeDownload slide Preprocedure form. FIGURE 1. View largeDownload slide Preprocedure form. FIGURE 2. View largeDownload slide Level of confidence (LOC). FIGURE 2. View largeDownload slide Level of confidence (LOC). FIGURE 3. View largeDownload slide Postprocedure form. FIGURE 3. View largeDownload slide Postprocedure form. CE CE was performed after a 2 hour fast following CTE or MRE. If CE did not follow CTE/MRE in the same day, it was completed after withholding solid foods for 8 hours, liquids for 4 hours, and pills/capsules for 2 hours. Patients were able to resume a clear liquid diet 2 hours after capsule ingestion and begin light meals 4 hours after capsule ingestion. CD on CE was defined as diffuse erythema and edema, linear or circumferential ulceration(s), the presence of 3 or more aphthous ulcers, or stenosis. CE reports included quality of bowel preparation and a Lewis score.14, 15 The Lewis score is an automated scoring system within RAPID reading program for standardizing CD activity based on the degree and extent of mucosal damage. The SB is divided into tertiles to generate the score. For each tertile, the CE reader reported on villous edema, ulcers, and stenosis to aid in the calculation of the Lewis score. Edema was recorded as focal, patchy, or diffuse. The distribution of edema was reported as short segment (<10% of segment), long segment (10–50%), or extensive (>50%). For ulcers, the number, size, and distribution were reported. Stenosis was described as being present or not, presence of ulceration within the stenotic segment, and if the capsule passed. A score of 135-789 was classified as representing mild small bowel Crohn’s inflammation, and a score of active inflammatory CD of at least mild severity, and a score of ≥ 790 was classified as representing moderate to severe disease. Proximal SB disease was defined as lesions within the first and/or second tertile. Statistical Analysis The primary endpoint was to estimate the proportion of CD patients in which CE influenced the therapeutic plan (ie, change in management plan). Descriptive statistics are reported as number (percent), median (minimum, maximum), and range as appropriate. The Wilcoxon signed rank test was used to assess for statistical significance between groups. RESULTS A total of 434 consecutive patients were screened. The most common reason for exclusion (Fig. 4) was incomplete testing or scheduling conflict followed by disease severity or concern for obstruction (stricturing on imaging, prior intestinal obstruction, and/or current obstructive symptoms). Of the 50 eligible patients evaluated, 60% were females. The median age was 38.0 years (range, 19–72 years), median disease duration was 3 years (range, 0–30 years), median CDAI score was 237.5 points (range, 91.8–431.6), and median hematocrit was 41.05% (range, 28.5–47.2). Serum C-reactive protein was elevated above the upper limit of normal (0.8 mg/dL) in 21 patients (42%). FIGURE 4. View largeDownload slide Flow diagram of study inclusion. FIGURE 4. View largeDownload slide Flow diagram of study inclusion. The most common indication for CTE or MRE imaging was to assess extent of disease (64%; Fig. 5A, B). MRE was ordered more frequently (54%) than CTE as the SB imaging modality. All CTE and MRE studies were negative for proximal SB disease. Active distal SB disease was identified on enterography in 15 patients (30%) with 12 patients having distal ileal disease and 3 patients having ileal disease with terminal ileal skipping (disease affecting proximal ileum with normal terminal ileum). The radiologic severity of the ileal disease was described as mild (13 patients) or moderate (2 patients). There were no cases of severe disease found on cross-sectional imaging but 2 patients did have extensive disease (15 cm). FIGURE 5. View largeDownload slide A,B, CTE of luminal narrowing and early penetrating disease. The arrow points to ileal disease found on CT imaging. FIGURE 5. View largeDownload slide A,B, CTE of luminal narrowing and early penetrating disease. The arrow points to ileal disease found on CT imaging. Review of the ileocolonoscopy reports revealed the largest subset of patients had normal mucosa (23 patients; 46%). The next most common finding from the ileocolonoscopy was ileocolonic disease (36%). For the remaining patients, ileocolonoscopy identified proctitis (8%), right-sided only colonic disease (4%), proctosigmoiditis (2%), anastomotic ulcer (2%), and proctocolectomy with ileal pouch-anal anastomosis (2%). Pathology reports found 27 patients (54%) to have normal colonic or ileal mucosa. Fifteen patients (30%) had mild colitis or ileitis. Only 7 patients (14%) had moderate colitis or ileitis. The final patient had severe ileocolonic disease. The CE reader rated the visualization as fair to excellent in 47/50 patients. In the 3/50 patients with poor preparation, fluid and bubbles obscured SB mucosa. CE detected proximal disease in 14 patients (28%; Fig. 6A, B) with a median Lewis score of 214.5 points (range, 8-1404) and 6 patients had extensive SB disease with a median Lewis score of 519.5 points (range, 112–2140). There was only 1 adverse event with CE ingestion that occurred when a patient developed acute dysphagia after swallowing CE and then regurgitated the CE. This patient was excluded from the study but had no adverse medical complications from the event. FIGURE 6. View largeDownload slide A,B, CE positive for SB mucosal disease. The arrow points to small bowel mucosal disease found on capsule endoscopy. FIGURE 6. View largeDownload slide A,B, CE positive for SB mucosal disease. The arrow points to small bowel mucosal disease found on capsule endoscopy. CE findings altered management in 17 cases (34%; Table 2). Of those 17 cases, 12 (71%) had a normal cross-sectional imaging. The most frequent provider-perceived changes were addition of new medication (29%) and exclusion of active SB mucosal disease (24%). LOC changes were related to CE in 82% of cases with clinically meaningful LOC changes observed in 56% of encounters. The LOC changes were statistically significant when comparing those with a change in management and those without a change for both active disease (P = 0.049) and SB mucosal ulcerations (P = 0.03). Providers indicated they would have ordered a CE for 13 patients even without enrollment in the study. Table 2: CE Altered Management Management Change Total Patients (no. = 17) CDAI <150 CDAI ≥150 to <220 CDAI ≥220 to ≤450 CDAI >450 Addition of New Medication 5 2 1 2 0 Escalation of Therapy Cancelled 4 0 1 3 0 Discontinue Medication 2 1 0 1 0 Dose Change 2 0 1 1 0 Surgical Referral 1 1 0 0 0 Continue Current Management Plan 2 0 0 2 0 Other: Evaluate in shorter time interval 1 0 0 1 0 Management Change Total Patients (no. = 17) CDAI <150 CDAI ≥150 to <220 CDAI ≥220 to ≤450 CDAI >450 Addition of New Medication 5 2 1 2 0 Escalation of Therapy Cancelled 4 0 1 3 0 Discontinue Medication 2 1 0 1 0 Dose Change 2 0 1 1 0 Surgical Referral 1 1 0 0 0 Continue Current Management Plan 2 0 0 2 0 Other: Evaluate in shorter time interval 1 0 0 1 0 View Large Table 2: CE Altered Management Management Change Total Patients (no. = 17) CDAI <150 CDAI ≥150 to <220 CDAI ≥220 to ≤450 CDAI >450 Addition of New Medication 5 2 1 2 0 Escalation of Therapy Cancelled 4 0 1 3 0 Discontinue Medication 2 1 0 1 0 Dose Change 2 0 1 1 0 Surgical Referral 1 1 0 0 0 Continue Current Management Plan 2 0 0 2 0 Other: Evaluate in shorter time interval 1 0 0 1 0 Management Change Total Patients (no. = 17) CDAI <150 CDAI ≥150 to <220 CDAI ≥220 to ≤450 CDAI >450 Addition of New Medication 5 2 1 2 0 Escalation of Therapy Cancelled 4 0 1 3 0 Discontinue Medication 2 1 0 1 0 Dose Change 2 0 1 1 0 Surgical Referral 1 1 0 0 0 Continue Current Management Plan 2 0 0 2 0 Other: Evaluate in shorter time interval 1 0 0 1 0 View Large The follow-up recommendation given to the majority of patients (56%) was to return at 6 months to be assessed by the provider. Follow-up imaging (CE or CTE/MRE) was recommended to be completed within 6 months for 12 patients (24%; 2 CE) and within 12 months for 10 patients (20%; 2 CE). DISCUSSION Determining the location, extent, and severity of CD at the time of diagnosis is an important part of the clinical assessment to establish prognosis and determine optimal, individualized management and monitoring strategies. A complete evaluation of SBCD activity requires a multimodality approach with optical and radiologic imaging studies. Cross-sectional imaging (CTE/MRE) is superior to ileocolonoscopy and CE for assessing SB strictures, penetrating complications, transmural disease, and extraluminal disease. However, the addition of CE allows an assessment of SB mucosal disease that is below the diagnostic threshold of CTE/MRE and is beyond the reach of standard endoscopy. This prospective study affirms that CE alters the management plans in up to a third of patients with CD undergoing CTE/MRE and ileocolonoscopy. Our data suggest that for every 50 patients with CE performed after CTE/MRE and colonoscopy, 17 would have a management change. Thus, to achieve 1 patient with a change in management, 1.94 patients would undergo testing without a plan change (33/17). The most frequent management changes were addition of a new medication and ability to exclude active SB mucosal disease. This is consistent with prior studies that have reported CE as having a high diagnostic yield for detection of SB mucosal erosions and aphthae.16, 17 Detection of proximal SB disease is prognostically significant since it has been associated with worse clinical outcomes.18, 19 In addition, our study is congruent with prior studies showing identification of proximal SB lesions has led to medical management changes.20–22 Lastly, these results suggest the greatest benefit may occur in patients with a history of SBCD but with a normal CTE / MRE. Capsule retention is a known risk of the CE procedure. As evident in our study, careful screening of patients clinically and radiographically can dramatically reduce the risk of SB retention of CE. In a large retrospective study of all CE completed over a 10-year span, retention only occurred in 0.3% of cases.23 CE retention was more likely to occur in the setting of SB anastomosis and strictures, but not necessarily CD alone. Overall, the procedure is well tolerated by patients especially when a bowel preparation is not required before capsule ingestion. Several limitations should be acknowledged with this analysis. This includes its small sample size and a referral bias as a tertiary care center. The results, however, were prospectively obtained and consistent with a growing body of evidence that SB imaging complements ileocolonoscopy. This is the first prospective study to assess the additional benefit of CE in CD patients undergoing both CTE / MRE and ileocolonoscopy. In conclusion, CE is a valuable, safe, radiation-free imaging modality that can alter management plans and provider LOC by detecting SB inflammation in patients with established CD after strictures are excluded by CTE or MRE. These findings further support the use of CE in SBCD diagnostic management algorithms. Further studies are needed to determine if CE has a vital role in monitoring SB mucosal healing and to determine situations where CE can be used in place of cross-sectional imaging as a first-line diagnostic modality for assessing the burden of SB disease. Conflicts of Interest: Stephanie L. Hansel, MD, MS,Medtronic, grant support and David H. Bruining, MD, Medtronic, consultant and grant support. All other authors do not have relevant disclosures. Supported by: study was funded by a research grant from Medtronic. REFERENCES 1. Booya F , Fletcher JG , Huprich JE , et al. Active Crohn disease: CT findings and interobserver agreement for enteric phase CT enterography . 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TI - Clinical Benefit of Capsule Endoscopy in Crohn’s Disease: Impact on Patient Management and Prevalence of Proximal Small Bowel Involvement
JO - Inflammatory Bowel Diseases
DO - 10.1093/ibd/izy050
DA - 2018-05-17
UR - https://www.deepdyve.com/lp/oxford-university-press/clinical-benefit-of-capsule-endoscopy-in-crohn-s-disease-impact-on-hHmdT0l4rr
SP - 1
EP - 1588
VL - Advance Article
IS - 7
DP - DeepDyve
ER -