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DOI: 10.1055/s-0043-1766122
Capsule Endoscopy in Inflammatory Bowel Disease: A Systematic Review
- Abstract
- Introduction
- Materials and Methods
- Results
- Role of Video Capsule Endoscopy in Inflammatory Bowel Disease
- 4. Discussion
- Conclusion
- References
Abstract
The role of video capsule endoscopy (VCE) in inflammatory bowel disease (IBD) has evolved from small bowel to a panenteric evaluation tool over the past two decades. We systematically reviewed the techniques, applications, outcomes, and complications of VCE in IBD. A systematic literature search was performed using PubMed, Embase, and Medline. All relevant original articles involving VCE in IBD were included from 2003 to July 2022. After screening 3,089 citations, finally 201 references were included. The diagnostic yield of VCE in suspected Crohn's disease (CD) was highly variable (6–80%) with excellent sensitivity (77–93%) and specificity (80–89%). The diagnostic yield in known CD was 52 to 88.3% leading to a change in management (26–75%) and disease reclassification with variable retention rates. VCE was superior to small bowel series, computed tomography (CT) and could be better than magnetic resonance enterography (MRE), especially for proximal and superficial lesions. Colon or panenteric VCE has strong correlation to ileo-colonoscopy (IC) and combined magnetic resonance imaging and IC, respectively. The VCE retention rate in CD is higher in known CD which significantly decreases after the negative patency capsule test or CT/MRE. VCE can identify lesions beyond the reach of IC in postoperative CD. Colon Capsule Endoscopy is a noninvasive monitoring tool in ulcerative colitis (UC) having a strong correlation with IC and may uncover small bowel involvement. VCE is specifically useful in IBD-unclassified (IBD-U) which can lead to the diagnosis of CD in 16.7 to 61.5%. Various scoring systems have been established and validated for small bowel CD (Lewis score and capsule endoscopy CD activity index—CECDAI), UC (capsule scoring of UC: Capsule Scoring of Ulcerative Colitis), panenteric evaluation (Capsule Endoscopy Crohn's Disease Activity Index, Elaikim score), and flare prediction (APEX score). Technological advances include double head, three-dimensional reconstruction, sampling system, panoramic view (344 and 360 degree lateral), and panenteric capsule. Artificial intelligence and software like TOP100 and Quickview can help reduce capsule reading time with excellent sensitivity and specificity. VCE in IBD has widespread application in suspected and known small bowel CD, monitoring of UC, postoperative CD, IBD-U, and for panenteric evaluation. Patency capsule testing helps to reduce retention rates significantly. Artificial intelligence and technical advances can help evolve this novel technology.
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Keywords
video capsule endoscopy - Crohn's disease - ulcerative colitis - inflammatory bowel disease - patency capsuleIntroduction
Video capsule endoscopy (VCE) is a noninvasive, widely available, nonoperator-dependent imaging modality in inflammatory bowel disease (IBD) which avoids any radiation exposure and, hence, has high patient acceptability.[1] [2] Although initially developed for detecting small bowel disease, the role of VCE has evolved to panenteric evaluation.[3] The role of VCE in postoperative Crohn's disease (CD) and treatment follow-up is being increasingly recognized. The drawbacks include risk of retention and inability to procure biopsy and to detect extraluminal disease.[4] The risk of retention can be substantially reduced by the use of patency capsule testing. A new recoverable sampling system (RSS) has shown the technical feasibility of obtaining biopsy with capsule technology, however still not in routine clinical use.[5] As newer methods of deep small bowel total enteroscopy like novel motorized spiral enteroscopy have evolved parallel to the development of capsule endoscopy, the positioning of VCE in the evaluation of IBD needs reconsideration.[6] Hence, we systematically reviewed the literature to understand the current role of VCE in evaluation and monitoring of IBD.
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Materials and Methods
Search Strategy
Data Sources
For the purpose of the review, we used the PubMed, Embase, and Medline databases.
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Study Selection
All relevant original research articles involving VCE in IBD were included for the review from 2003 to July 2022.
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Interventions
We intended to evaluate the current role of VCE in the evaluation and monitoring of IBD. We included articles using keywords such as capsule endoscopy, inflammatory bowel disease, Crohn's disease, ulcerative colitis, indeterminate colitis, panenteric capsule, artificial intelligence, postoperative Crohn's recurrence, patency capsule, Lewis score (LS), and capsule endoscopy Crohn's disease activity index.
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Main Outcome Measures
The role of VCE in suspected and known CD, ulcerative colitis, postoperative CD recurrence, IBD-unclassified (IBD-U), pouchitis, role of various scoring systems, role of artificial intelligence, and technological advances were assessed.
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Results
We screened total 3,089 citations and 502 were screened for full test after the exclusion of articles based on title and abstract and exclusion of duplicates. Finally, 201 citations were included for our review excluding case reports/series/original articles with a small sample size (less than 10 subjects unless they are addressing special circumstances/describing novel technique or an unique complication)/letter to editor/editorials/conference abstracts ([Fig. 1]) and including relevant articles with specific searches and selected cross references.
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Limitations
The limitations include a qualitative review of all study types given the paucity of controlled or comparative studies and preexisting meta-analysis of prospective studies in a few aspects.
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Results
Role of Video Capsule Endoscopy in Inflammatory Bowel Disease
Video Capsule Endoscopy in Suspected Crohn's Disease
Study Selection and Study Characteristics
We have identified 30 original articles (13 prospective) which evaluated the role of VCE in suspected CD[7] [8] [9] [10] [11] [12] [13] [14] [15] [16] [17] [18] [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] [31] [32] [33] [34] [35] [36] ([Table 1]).
Author |
Indication |
Study type |
N |
Diagnostic yield |
Sensitivity |
Specificity |
PPV |
NPV |
Adverse events |
---|---|---|---|---|---|---|---|---|---|
Fireman et al 2003[7] |
Suspected CD, negative conventional imaging |
Prospective |
17 |
71% |
– |
– |
– |
– |
|
Herrerías et al 2003[8] |
Suspected CD, negative conventional imaging |
Prospective |
21 |
43% |
– |
– |
– |
– |
None |
Ge et al 2004[10] |
Suspected CD, negative conventional imaging |
Prospective |
20 |
65% |
– |
– |
– |
– |
– |
De Bona et al 2006[12] |
Suspected CD, negative conventional imaging |
Prospective |
38 |
39.5% (46.2%with symptoms+ biochemical markers of inflammation) |
– |
– |
– |
– |
2.6% |
van Tuyl et al 2006[13] |
Suspected small bowel disorders including CD |
Retrospective |
57 |
49% |
– |
– |
61% |
92% |
– |
May et al, 2007[15] |
Abdominal pain+ diarrhea weight loss/anemia/elevated inflammatory markers |
Prospective |
50 |
54% Additional symptom increased diagnostic yield |
– |
– |
– |
– |
Retention (4%) |
GIrelli et al 2007[14] |
Suspected CD: pain and diarrhea >3 mo + fever/weight loss/anemia/EIM |
Prospective |
27 |
59% |
93% |
84% |
– |
– |
Retention requiring surgery (11.1%) |
Tukey et al 2009[18] |
Suspected CD or pain and/or diarrhea |
Retrospective |
102 |
37% (13% final diagnosis of CD on follow up) |
77% |
89% |
50% (depends on selection criteria) |
96% |
– |
Figueiredo et al 2010[19] |
Suspected CD |
Retrospective |
78 |
39.8% (56% for those with negative ileoscopy) |
93% |
80% |
77% |
94% |
Retention (4%) |
Adler et al 2012[21] |
Perianal disease, normal ileo-colonoscopy/SBFT/CTE/MRE |
Prospective |
26 |
24% |
– |
– |
– |
– |
0% |
Kalla et al 2013[24] |
Suspected CD |
Retrospective |
265 |
12% |
– |
– |
– |
– |
– |
Egnatios et al 2015[27] |
Chronic abdominal pain |
Retrospective |
90 |
24.4% (27.1% with additional symptoms, 19.4% only pain) |
– |
– |
– |
– |
None |
Mitselos et al 2016[29] |
Chronic abdominal pain and/or diarrhea |
Retrospective |
91 |
17.6% |
63.6% |
92.5% |
– |
– |
– |
Lee and Lim 2016[28] |
Symptomatic patients with Isolated ileitis |
Retrospective |
137 |
85.4% (high with ileal ulcer/erosion and high ESR) |
– |
– |
– |
– |
– |
Song et al 2017[30] |
Chronic diarrhea |
Retrospective |
91 |
42.9% (hematochezia and hypoalbuminemia were predictors) |
– |
– |
– |
– |
1% |
Huang et al 2018[32] |
Chronic abdominal pain >3 mo |
Retrospective |
341 |
28.15% (33.3% for abdominal pain + associated symptoms) (half had inflammatory pathology) |
– |
– |
– |
– |
0% |
Magalhaes et al 2019[33] |
Suspected CD |
Prospective |
220 |
44.5% (high CRP, low iron increased yield) |
– |
– |
– |
– |
– |
Min et al 2013[25] |
Suspected CD (pediatric) |
Retrospective |
17 |
6% |
– |
– |
– |
– |
0% |
Gralnek et al 2012[23] |
Suspected CD (pediatric) |
Prospective |
10 |
80% |
– |
– |
– |
– |
0% |
Argüelles-Arias et al 2004[9] |
Suspected CD (pediatric, ≥12–16 y) |
Prospective |
12 |
58.3% |
– |
– |
– |
– |
0% |
Wu et al 2020[34] |
Symptomatic patients (abdominal pain, obscure GI bleed, diarrhea etc.) (Pediatric) |
Retrospective |
825 |
19.9% CD |
– |
– |
– |
– |
Retention requiring surgery (0.4%) |
Nuutinen et al 2011[20] |
Suspected CD (pediatric) (8–188 mo) |
Retrospective |
26 |
62% |
– |
– |
– |
– |
0% |
Moy and Levine 2009[17] |
Suspected CD (pediatric) (growth failure) |
Retrospective |
7 |
57.1% Improvement in height after small bowel CD treatment |
– |
– |
– |
– |
1 retained in stomach |
Cohen et al 2012[22] |
Suspected CD (pediatric) |
Retrospective |
184 |
15% |
– |
– |
– |
– |
1 retention |
Esaki et al 2014[26] |
Suspected CD |
Retrospective |
80 |
72.5% |
– |
– |
– |
– |
6.3% retention |
van Tuyl et al 2007[16] |
Suspected CD |
Retrospective |
22 |
71% definitive diagnosis, 14% probable diagnosis |
– |
– |
– |
– |
– |
Mow et al 2004[11] |
Suspected CD |
Retrospective |
8 |
37.5% |
– |
– |
– |
– |
12.5% |
Eliakim et al 2018[31] |
Suspected CD (panenteric capsule) |
Prospective |
7 |
57.1% |
– |
– |
– |
– |
None |
Broderson et al 2022[36] |
Suspected CD (panenteric capsule) |
Prospective |
59 |
44.8% Better image quality with increased volume of PEG but no change in diagnostic yield (43.9% versus 47.1%) |
– |
– |
– |
– |
Not mentioned clearly |
Tai et al 2020[35] |
Suspected CD (panenteric capsule) |
Prospective |
22 |
13.6% |
– |
– |
– |
– |
0% |
Abbreviations: CD, Crohn's disease; CRP, c-reactive protein; ESR, erythrocyte sedimentation rate; NPV, negative predictive values; PEG, polyethylene glycol; PPV, positive predictive values.
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Results
Suspicion of CD is the most common indication of VCE in IBD as per a Spanish physician survey.[37] The diagnostic yield was highly variable (6–80%) across these studies. This wide variability can be explained by the heterogeneity of study design, variable definitions of suspected CD, pretest probability in the subjects studied, and variable age groups (includes pediatric). The probability was higher with an increasing number of symptoms, elevated biochemical markers of inflammation, anemia, and hypoalbuminemia.
Three studies evaluated the sensitivity and specificity of VCE which were excellent (77–93% and 80–89%, respectively). The positive predictive values (PPVs) and negative predictive values (NPVs) varied from 50 to 77% and 92 to 96%, respectively. VCE retention rates varied from 0 to 12.5%. Two meta-analyses have shown that VCE was superior to small bowel follow through (SBFT) and ileo-colonoscopy (IC) and comparable to computed tomography enterography (one meta-analysis showed inferiority to VCE and another comparable to VCE)/MRE in the evaluation of suspected CD (see comparative yield section).[38] [39]
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3.1.1. Capsule Endoscopy Differentiating Crohn's Disease from Mimics (e.g., Small Bowel Tuberculosis)
Capsule endoscopy findings should be interpreted in correlation with other findings to differentiate from other similar appearing lesions like small bowel tuberculosis (SBTB), nonsteroidal anti-inflammatory drugs enteropathy, Behcet's disease, vasculitis, and also normal variation (10%). In a prospective study, out of 37 suspected CD patients on VCE, only 13% were subsequently diagnosed to have CD on 1 year follow-up.[18] On the contrary, 19% patients with nonspecific enteritis develop CD on follow-up. High baseline LS (>135) and clinical suspicion were predictors of the subsequent development of CD.[40]
To address the aforementioned issue, a prospective study from India in which VCE was done in 26 patients after proving bowel patency showed that ileo-cecal valve involvement and aphthous ulceration were universal in SBTB (100% compared with 33% in CD) and CD (100% compared with 25% in SBTB), respectively. Large ulcers were more common in SBTB as compared with CD (75 vs. 47%).[41]
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3.1.2. Factors Affecting Yield of Video Capsule Endoscopy in Suspected Crohn's Disease
Based on clinical symptoms, the combination of abdominal pain and diarrhea was shown to be highly predictive of CD on VCE. Nearly, one-third with the combination of symptoms had CD in this retrospective analysis.[42] The diagnostic yield with only chronic abdominal pain was 20.9% based on a systematic review.[43] The independent predictive factors of proximal small bowel involvement were ileal involvement, stricturing behavior, and significant weight loss.[44] In suspected CD with negative IC and SBFT, the combination of anemia and increased platelet count was a significant predictor of CD on VCE.[45] Fecal calprotectin as a predictor of the lesion in VCE has shown variable results in several studies with variable cutoffs.[46] [47] [48] [49] [50] [51] [52] [53] [54] [55] [56] [57] [58] [59] [60]
Fecal calprotectin level >194 μg/g had a sensitivity and specificity of 47 and 90%, respectively, for diagnosing CD on VCE.[57] On the contrary, fecal calprotectin <50 μg/g had a negative predictive value of 91.8% of having CD on VCE based on a systematic review.[52]
Two studies have evaluated multiple parameters for the prediction of CD. A Spanish multicenter study developed and validated a scoring index based on fecal calprotectin (score 10), c-reactive protein (CRP; score 6), thrombocytosis (score 3), anemia (score 2), leukocytosis (score 2), and high erythrocyte sedimentation rate.[1] Score ranges 0 to 5, 6 to 15, and ≥16 predicted low, intermediate, and high risk of inflammatory lesions on VCE, respectively.[61]
Another elegant study has shown the incremental yield of VCE with an increasing number of International Conference on Capsule Endoscopy (ICCE) criteria. Suspected CD was defined as clinical symptoms (chronic abdominal pain/diarrhea, weight loss, and growth failure) plus any one or more extraintestinal manifestations, inflammatory markers, and abnormal imaging (SBFT/CTE). The prevalence of CD in those with suspected CD not supported by ICCE criteria, two criteria, and three criteria was 21.4, 52.6, and 77.8%, respectively. In those with LS ≥135, 82.6% had CD.[62]
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3.1.3. Value of Repeat Video Capsule Endoscopy in Suspected Crohn's Disease
In a letter to the editor, Robertson et al have reported findings of 18 patients with suspected CD who underwent repeat VCE on follow-up. Those with nonspecific inflammation on initial VCE (33%) were more likely to have repeat VCE suggestive of CD (33%) along with those with higher fecal calprotectin levels.[63]
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3.1.4. Role of Video Capsule Endoscopy in Presymptomatic Patients
VCE has been used in first-degree relatives of CD patients to identify those with subclinical small bowel inflammation. A cross-sectional study in 2017 by Teshima et al showed increased intestinal permeability, and small bowel ulceration (≥3) was seen in 30 and 24% of the first-degree relatives (n = 223) with CD. However, increased intestinal permeability did not correlate with small bowel inflammation.[64] Later, another study by Taylor et al in 2019 involving 480 asymptomatic first-degree relatives of CD has shown a risk tool comprising family history of CD, genetic variants associated with CD, and high level of fecal calprotectin predicted risk of presymptomatic small bowel inflammation.[65]
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Role of Video Capsule Endoscopy in Spondyloarthropathy
Three prospective studies have shown a high yield of VCE (12.5–42.2%) to diagnose CD in the established case of spondyloarthropathy (SpA) with bowel symptoms.[66] [67] [68] Elevated fecal calprotectin (>100 µg/g) was the predictor of small bowel CD (odds ratio = 4.5).[68] In a case series of three juvenile idiopathic arthritis, all cases were diagnosed to have CD.[69]
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Video Capsule Endoscopy in Known Crohn's Disease
Study Selection and Study Characteristics
A total of 29 original articles were identified (12 prospective) evaluating the role of VCE in known CD.
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Results
Overall diagnostic yield varied from 52 to 88.3%. The yield was high for symptomatic CD (highest for diarrhea—73%), whereas it was 21.1 and 4.7% only in those with clinical remission and clinico-biochemical remission, respectively.[16] [20] [22] [23] [24] [25] [26] [31] [35] [70] [71] [72] [73] [74] [75] [76] [77] [78] [79] [80] [81] [82] [83] [84] [85] [86] [87] [88] The incremental yield over SBFT was 32 to 32.7% and 7% over IC. In a prospective study in pediatric CD, the diagnostic yield of VCE (41%) was higher than magnetic resonance imaging (MRI)/small intestinal contrast ultrasonography (SICUS; 18.2%).[75] The incremental yield in the proximal small bowel was 28 to 50%.[23] [83] [85] The overall change in management after VCE varied from 21 to 71% which included treatment escalation, deescalation, initiation of new medications (biologics/immunomodulators), and decision for surgery.[16] [24] [85] [87] Other implications of VCE in known CD are reclassification of disease phenotype (11%), assessment of mucosal healing posttherapy, and prediction of relapse (higher with jejunal disease).[78] [82] [84] Clinical and biochemical improvement can predict mucosal healing in less than half (none at 2 weeks, 42% at 52 weeks) of the patients.[89] [90] [91] The rate of retention varied from 2.1 to 18.6% ([Table 2]).
Abbreviations: BMI, body mass index; CD, Crohn's disease; CRP, c-reactive protein; ESR, erythrocyte sedimentation rate; HBI, harvey bradshaw index; MRI, magnetic resonance imaging; NPV, negative predictive values; PEG, polyethylene glycol; PPV, positive predictive values; SBFT, small bowel follow through; SICUS, small intestinal contrast ultrasonography; VCE, video capsule endoscopy.
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3.3. Video Capsule Endoscopy Compared with Other Imaging Technologies in Suspected or Known Crohn's Disease
Study Selection and Study Characteristics
In total, 9 studies including 378 patients compared the diagnostic yield of VCE with various other modalities (IC, SBFT, CTE, MRE, SICUS) in suspected CD.
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Results
VCE was better than all the other modalities with regard to diagnostic yield except MRE ([Table 3])[29] [92] [93] [94] [95] [96] [97] [98]. An earlier meta-analysis and a recent meta-analysis have also shown the same for both suspected and established CD.
Abbreviations: AUC, area under the curve; CD, Crohn's disease; IC, ileo-colonoscopy; CTMRI, magnetic resonance imaging; IUS, intestinal ultrasound; MRE, magnetic resonance enterography; PCCE, panenteric colon capsule endoscopy; SES- CD, simple endoscopic score Crohn's disease; SICUS, small intestinal contrast ultrasonography.
Similar results were found in known CD (10 articles and 2 meta-analysis)[3] [99] [100] [101] [102] [103] [104] [105] [106] [107]. However, SICUS had comparable sensitivity (90%) and specificity (93%) to VCE for small bowel involvement in pediatric CD.[102] Panenteric colon capsule endoscopy (PCCE) has been compared with MRE plus IC and was found that MRE + IC had 100% sensitivity (94% with VCE) but low specificity (22% compared with 74% with PCCE).[106] PCCE has been compared with reference endoscopic standard (bidirectional double balloon enteroscopy), and diagnostic accuracy was 88.3 and 77.1% for small and large bowel, respectively.[3] Compared with colonoscopy, the sensitivity and specificity of CCE were 86 and 40%, respectively.[101] Moreover, risk prediction for future flare was better with the VCE LS (AUC—area under the curve: 0.79) compared with MRE risk prediction (AUC: 0.71). Among 11 studies (n = 439) comprising both suspected and known CD, VCE had higher sensitivity compared with CTE, IC, and SBFT but lower specificity (53% compared with 100% with others).[108] [109] [110] [111] [112] [113] [114] [115] [116] [117] [118] Comparing the specificity of VCE according to the regions of small intestine, the specificity of VCE was lower in jejunum (61%) and proximal/mid-ileum (74%), but higher in terminal ileum (90%) compared with MRE and SICUS ([Table 3]).[117] VCE was better compared with MRE for proximal and superficial lesions.
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3.4. Risk of Retention in Suspected or Known Crohn's Disease
The risk of retention of VCE is 13% in established CD and 1.6% in suspected CD based on the earlier retrospective study by Cheifetz et al.[119] The overall retention rate in CD is 3.32% (2.35% suspected CD and 4.63% known CD) based on an updated systematic review and meta-analysis.[120] This is the reason why VCE is not generally preferred in established CD except for patients with anemia, obscure GI bleed, or assessment of mucosal healing. Retention rates were lower in pediatric CD (1.64%) compared with adult CD (3.49%).[120]
3.4.1. Predictors of Capsule Retention
Negative patency capsule testing and negative CT/MRE are negative predictors of capsule retention. The retention rates of patency capsule varied between 15.2 and 28% in known CD.[121] [122] A retrospective study showed that the retention rates after positive and negative patency capsule testing were 11 and 2.1%, respectively.[123] Similarly a prospective study showed 28.9% retention rates with active inflammation on MRE.[122] Based on meta-analysis, the retention rates in established CD remained 2.88% even after patency capsule testing and 2.32% after CT/MRE. The risk of retention is reduced after CT/MRE by 50%. MRE has a sensitivity of 92.3% and specificity of 59% to evaluate capsule retention as compared with 97 and 83%, respectively, for patency capsules. MRE tends to overdiagnose the risk of capsule retention. If only MRE is used to predict retention instead of patency capsule, nearly 40% patients (specificity—59%) would not undergo VCE due to fear of capsule retention.[122]
Other predictors were obstructive symptoms, stricturing/penetrating disease, BMI≤ 5th percentile, suspected stenosis on SBFT, restricted diffusion on diffusion-weighted MRI, extensive small bowel thickening on small bowel ultrasound, longer stricture length and higher number of prestenotic dilatations, high CRP, and history of abdominal surgery according to several studies[119] [120] [121] [122] [123] [124] [125] [126] [127] [128] [129] [130] [131] [132] [133] [134] [135] [136] ([Supplementary Table S1], available in the online version).
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3.4.2. Management of Retained Capsule
Capsule retention is asymptomatic in 85% which can be managed conservatively with enteroscopy-guided removal electively. Partial air complete small bowel obstruction occurs in the rest which requires endoscopic retrieval with or without balloon dilation. There are several reports of retrieval by double-balloon enteroscope (success rate 80–92%) and recently novel motorized spiral enteroscopy which can avoid surgery in the majority.[137] [138] [139] Moreover, it can help take surgical decisions as some of the patients may require surgery even after capsule removal for treating the underlying disease.
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3.4.3. Other Complications of Video Capsule Endoscopy
Although known CD substantially increases the risk of capsule retention, other complications of VCE like swallow disorder, aspiration, and technique failure can be substantial and clinically important. However, we could not find specific citations pertaining to IBD with regard to this. Meta-analysis, which included IBD patients, showed that the pooled rates of aspiration, technical failure, and swallow disorders were 0, 0.94, and 0.75%, respectively.[140]
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3.4. Video Capsule Endoscopy in postoperative Crohn's Disease
Study selection and study characteristics
Five prospective and one retrospective study including 313 patients have compared VCE with colonoscopy in postoperative CD ([Supplementary Table S2], available in the online version).
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Results
Except for the one retrospective study,[141] all the studies concluded that the yield of VCE was higher than colonoscopy in detecting postoperative recurrence especially for proximal involvement out of the reach of the colonoscopy.[142] [143] [144] [145] [146] [147] Another prospective study has compared capsule endoscopy or no capsule endoscopy in postoperative settings and has shown that VCE arm had lower hospitalization or surgery[147] ([Supplementary Table S2], available in the online version).
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3.5. Video Capsule Endoscopy in UC
Study Selection and Study Characteristics
In total, 14 prospective and 3 retrospective studies involving 612 patients have evaluated the role of VCE in ulcerative colitis (UC) ([Table 4]).[11] [20] [23] [31] [75] [148] [149] [150] [151] [152] [153] [154] [155] [156] [157] [158] [159]
Abbreviation: CD, Crohn's disease.
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Results
Overall results indicate that VCE had an excellent correlation with colonoscopy for severity/extent of inflammation and is better than fecal biomarkers. Patient acceptability was better than colonoscopy. Small bowel involvement in UC with VCE is variable (4.8–80%) and is dependent on the pretest probability (80% for those with suspicion of CD in a small series).[11] [23] [31] [149] [150] [156] In postproctocolectomy cases, extensive colitis, pouchitis, and age less than 20 years were predictors of small bowel involvement.[150] Active UC was also a predictor of small bowel involvement (40% compared with overall 36.6%).[150] No adverse events are reported except those related to bowel preparation and one case of retention due to unexpected rectal tumor ([Table 4]).[157] Bowel preparation was acceptable in 62 to 90% cases ([Table 4]).
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3.5.1. Role of Video Capsule Endoscopy in Pouchitis
A single-center prospective study has shown that all of the patients with chronic antibiotic refractory pouchitis have small bowel lesions from duodenum to ileum detectable on VCE which ranges from aphthous to deep, fissuring ulcers. None of the patients have any prior evidence of CD on review of surgical biopsy. These patients need to be followed up further, and the significance of such lesions is still unknown.[160] In a retrospective study, small bowel capsule endoscopy in pouchitis showed positive findings in 65.2%. Initiation of new IBD medications was noted in 56.5%, and small bowel resection was done in 4.4% following VCE.[76]
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3.6. Video Capsule Endoscopy in Inflammatory Bowel Disease-Unclassified
Study Selection and Study Characteristics
VCE could be particularly helpful in the IBD unclassified subgroup, where up to 16.7 to 50% patients can be diagnosed with CD after undergoing VCE as per four retrospective and five prospective studies in 177 adult and pediatric patients ([Supplementary Table S3], available in the online version).[23] [24] [25] [75] [148] [161] [162] [163] [164]
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Results
However, VCE can miss a diagnosis of CD as five of the aforementioned studies have shown that 0 to 16.7% patients develop CD on follow-up.[23] [148] [161] [162] [164] A change in existing treatment after CD diagnosis may not be necessary in all the patients as the reported change in treatment after CD diagnosis was seen in 0 to 100%.[24] [163] [164] A confirmed diagnosis of UC after exclusion of small bowel involvement in IBD-U can occur in 5.5 to 59.3%.[23] [161] [162] [163] [164] No change in diagnosis of IBD-U can occur in 0 to 75% cases ([Supplementary Table S3], available in the online version). LS >135 is a predictor of CD diagnosis with a sensitivity and specificity of 90 and 100%, respectively.[164]
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3.7. Scoring Systems for Video Capsule Endoscopy
Scoring systems in VCE may help predict disease severity and disease course similar to conventional endoscopic scoring. There are various validated scores for small bowel, colon, and panenteric evaluation.
3.7.1. Lewis Score
Study Selection and Study Characteristics
Total 9 studies (2 prospective) including 811 patients evaluated the role of the LS alone.[62] [165] [166] [167] [168] [169] [170] [171] [172]
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Results
LS was initially developed by Gralnek et al based on edema, ulceration, and stenosis in three tertiles with the establishment of cut-off values ([Table 5]; [Fig. 2]).[165] Later, the incremental number of ICCE criteria was found to be the predictive factor of significant inflammatory activity (LS > 135) on VCE.[62] LS ≥ 135 was shown to have a positive predictive value of 73.9%, and a score <135 had a negative predictive value of 91.8%.[168] Similar findings were seen in another validation study. A strong agreement was seen for global as well as for each tertile score in interobserver study.[166] Recent studies have evaluated the prognostic role of LS to predict CD-related emergency hospitalization and risk of cumulative relapse.[171] [172] Correlation of VCE with disease activity and small bowel transit time was weak in adults, whereas correlation with inflammatory markers was moderate in both pediatric age group and adults.[169] LS score correlates well with the MRE global score (r = 0.71) except the proximal LS score (r = 0.55).[170]
![](https://www.thieme-connect.de/media/10.1055-s-00043283/202303/thumbnails/10-1055-s-0043-1766122-i22120004-2.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Abbreviations: CD, Crohn's disease; CECDAIic, Capsule Endoscopy Crohn's Disease Activity Index; CRP, c-reactive protein; ICCE, International Conference on Capsule Endoscopy; LS, Lewis score; MRE, magnetic resonance enterography.
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3.7.2. Capsule Endoscopy Crohn's Disease Activity Index
Capsule Endoscopy Crohn's Disease Activity Index (CECDAI) or Niv score was also developed at the same time as the LS (2008) which was simpler and based on severity of inflammation, extent of disease, and narrowing in proximal and distal small bowel. Interobserver agreement was strong (k = 0.87) in single center and good between different centers (k = 0.767).[173] [174] The score has been validated by Ponte et al in 2018 which showed that the corresponding cut-off value of CECDAI for LS between 135 and 790 was 7.7 to 10.3.[175] Another study showed the cut-off value to be 3.8 to 5.8 which also showed that LS better correlates with fecal calprotectin (<100 μg/g) than CECDAI.[176] [177] In comparison to LS, a retrospective study has shown that CECDAI may better predict intestinal inflammation. Those with high LS and normal CECDAI may reflect strictures rather than active inflammation.[58]
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3.7.3. Panenteric Capsule Endoscopy Scores
As panenteric evaluation became feasible with VCE, panenteric scores were developed. The first one was CECDAlic which was an extension of CECDAI score into colon. Inflammation, extent of disease, and narrowing were evaluated in proximal small bowel, distal small bowel, right colon, and left colon. The concordance was high for small bowel (Kendell's coefficient: k = 0.85) and panenteric evaluation (k = 0.77) except for strictures in proximal small intestine and distal colon.[178] Later, it was validated and was shown to have excellent interobserver agreement (k = 0.94).[179]
The second panenteric score was based on novel PillCam Crohn's (PCC) (Medtronic, Dublin, Ireland) capsule. Panenteric scores were calculated from five areas: three tertiles of small intestine, right, and left colon. Each subscore was calculated using most common lesion (1), most severe lesion (2), extent of disease (3), and stricture (4) (each parameter rated from 0 to 3). Each segmental score was ([A + B] × C) +D. This score also named as the Elaikim score was shown to have an excellent correlation with LS and had excellent interobserver agreement (k = 0.9).[180]
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3.7.4. Capsule Scoring of Ulcerative Colitis
Similar to ulcerative colitis endoscopic activity index (UCEIS), Capsule Scoring of Ulcerative Colitis (CSUC) is based on parameters like vascular pattern (0: none, patchy obliteration[1] <30%, obliterated[2] >30%), bleeding (0: none, automated suspected blood indicator <10 = 1, >10 = 2), and erosions/ulcers (0: none, 1: <5 mm erosion, 2: >5 mm superficial ulcer, 3: excavated deep ulcer ± excavation/raised margins) in second-generation colon capsule endoscopy. Each item was subdivided into proximal and distal parts with the reference point being the splenic flexure. The total score was 0 to 14. Its correlation with fecal calprotectin, CRP, and clinical Lichtiger index was similar to UCEIS.[181]
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3.7.5 APEX Score
This is based on age (≤30 years) (+3), platelet count (≥280 × 103/L) (+2), and extraintestinal manifestations (+2) which were shown to predict risk of 1 year relapse after achieving mucosal healing in small bowel CD based on a recent retrospective study.[182]
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3.8. Interobserver Agreement in Diagnosing Small Bowel Crohn's Disease with Video Capsule Endoscopy
There is substantial interobserver agreement (IOA) for the detection of small bowel CD with VCE (k = 0.68). IOA was moderate for localization (k = 0.44) and only fair for aphthous ulcers (k = 0.38). Although small bowel CD can be diagnosed confidently with VCE, diagnosis can be observer dependent in those with few lesions. Differentiating ileal from cecal lesions can be difficult in a minority of patients.[183]
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3.9. Artificial Intelligence
Study Selection and Study Characteristics
We found nine original articles on the use of artificial intelligence in VCE related to IBD.
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Results
AI technology was used for Pillcam SB 3, panenteric capsule, and colon capsule. A variable number of training images (469–483,444) were used to develop the various AI technology followed by validation. The sensitivity and specificity of the AI models were 80 to 97.1% and 89 to 98.1%, respectively[184] [185] [186] [187] [188] [189] [190] [191] [192] ([Supplementary Table S4], available in the online version). Hence, AI can significantly reduce the examination time with excellent sensitivity and specificity.
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3.10 Novel Techniques and Future Directions
Study Selection and Study Characteristics
We found eight original articles describing various technical advances for VCE in IBD[5] [193] [194] [195] [196] [197] [198] [199]([Table 6]).
Abbreviations: CD, Crohn's disease; IBD, inflammatory bowel disease.
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Results
To increase the visibility and diagnostic yield, double head capsule and 344 degree panoramic view capsules have been developed.[198] For rapid review, the QuickView mode of RAPID capsule view software can reduce the reading time with excellent diagnostic accuracy up to 98%.[194] 3D reconstruction can help in the estimation of size of lesions.[197]
A novel RSS capsule technology has been developed which may allow noninvasive sampling, preservation, and storage of analytes found in gastrointestinal fluids which can correlate with inflammation and gut permeability. The preservative contained in the novel capsule stabilizes DNA and proteins for analysis after expulsion.[5]
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3.11. Cleansing Regimen
A randomized controlled trial in pediatric patients has shown that 25 mL/kg of polyethylene glycol (PEG) solution plus 20 mL (376 mg) of oral simethicone was superior to high volume PEG (50 mL/kg), oral simethicone, and low-dose PEG alone (25 mL/kg) with regard to better visualization but not diagnostic yield.[200] According to a prospective study, the addition of 15 mL of castor oil to 1 L of Moviprep and 10 mg bisacodyl significantly improved colon capsule endoscopy completion rates (87 vs. 73%) and polyp detection (82 vs. 44%)[201].
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4. Discussion
VCE is indicated in suspected small bowel CD after negative IC (nearly 10% of small bowel CD) if there are no obstructive symptoms or known stenosis/history of bowel surgery. If these are present, cross-sectional imaging (CT/MRE) is warranted. In those with positive findings in IC, VCE may still be indicated for mapping of the disease as one-third may have proximal bowel involvement.[44] The inherent limitation of VCE to evaluate the extraluminal involvement can be an additional reason to use cross-sectional imaging upfront especially in tuberculosis endemic regions where distal small bowel involvement often leads to TB and CD dilemma. The long duration of symptoms should also be kept in mind as it may indicate stricturing complications with high risk of retention.[6] VCE is also helpful to exclude differential diagnosis like TB and diagnose CD in presymptomatic patients.
The role of VCE in known CD ranged from diagnosis of active disease (highest in symptomatic patients), change in treatment decisions (escalation or deescalation of treatment and surgical decision), reclassification of disease, assessment of mucosal healing, and prediction of relapse. The yield was noninferior to MRI. However, the risk of retention is higher in known CD. PCCE has high agnostic accuracy in detecting active disease in small and large bowels.
VCE can also be useful in postoperative settings. However, the drawbacks of VCE in postoperative settings are lower yield in neoterminal ileum, inability to perform in those with positive patency testing, and poor correlation of endoscopic activity in VCE and clinical recurrence.
Capsule endoscopy can have role in relatively noninvasive monitoring of disease activity in UC with excellent correlation with colonoscopy. It has the advantage of identifying small bowel involvement although the preparation may be poor in a third of the patients.
VCE scores have a good correlation with cross-sectional imaging (e.g., MRI scores) and can be helpful to establish the extent of small bowel, panenteric, and large bowel involvement with the existing scores (Lewis, CECDAI, Capsule Endoscopy Crohn's Disease Activity Index [CECDAIic], CSUC). Scores like APEX can predict the risk of relapse in small bowel CD.
Technical advances in the form of artificial intelligence, technical modification, and various software packages can reduce reading time with high diagnostic accuracy. Technology like RSS has the potential to guide therapy by disease monitoring and characterization and may also help in developing novel therapeutic targets.
The limitations of the review include qualitative nature and inclusion of primarily uncontrolled, noncomparative studies. The highest quality citations included good-quality prospective studies. Individual meta-analysis of the different outcomes is out of the scope of this broader systematic review. The strength of this review is the inclusion of all relevant articles pertaining to the role of VCE in IBD. The review implies the need for further comparative studies such as comparing MRI with VCE in suspected and known CD or comparison of VCE with other modalities like IC for diagnosing postoperative recurrence. In areas where randomized controlled trials are not available, high-quality prospective studies can give true estimates of VCE yield in scenarios such as IBD-U and pouchitis and their implications in future disease courses.
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Conclusion
Capsule endoscopy is indicated in the evaluation of suspected small bowel CD irrespective of findings of IC to map small intestinal involvement, and the diagnostic yield is superior to other modalities except MRE. Hence, VCE should be the preferred investigation in suspected CD in the absence of obstructive symptoms or known stenosis. A cross-sectional imaging (CTE/MRE) or patency capsule testing should be done prior to CE in suspected stricturing CD or established CD. In known CD, VCE should not be preferred over cross-sectional imaging due to the risk of retention. It can be done in established CD to evaluate unexplained anemia, obscure GI bleed, and sometimes assessment of mucosal healing. Capsule retention is usually asymptomatic, however, symptomatic cases can be treated with balloon or spiral enteroscopy-guided retrieval failing which surgery is warranted. Various scoring systems are available for small bowel, colon, and panenteric evaluation. Scoring systems at VCE can help to determine severity and disease course similar to endoscopic scoring. VCE is useful to assess postoperative CD, IBD-U, and noninvasive monitoring of UC. Artificial intelligence and newer technologies increase the diagnostic yield and reading time of VCE and are the future avenues in this evolving field.
Abbreviations: BMI, body mass index; CD, Crohn's disease; CRP, c-reactive protein; CT, computed tomography; GI, gastrointestinal; MRI, magnetic resonance imaging; SBFT, small bowel follow through.
Abbreviations: CD, Crohn's disease; ICCE, International Conference on Capsule Endoscopy; LS, Lewis score; SICUS, small intestinal contrast ultrasonography.
Abbreviations: CD, Crohn's disease; NSAID, nonsteroidal anti-inflammatory drugs.
Source: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. doi: 10.1136/bmj.n71.
For more information, visit: http://www.prisma-statement.org/
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Conflict of Interest
None declared.
Authors' Contribution
P.P. was responsible for conceptualization, literature review and writing original draft, and illustrations. P.P., R.G., and P.M.R. were responsible for images. M.T., R.B., R.G., P.M.R., and D.N.R. were responsible for proof reading and critical review. M.T., P.P., R.B., R.G., P.M.R., and D.N.R. were responsible for approving final manuscript.
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