Abstract
Background/Aims
Capsule endoscopy (CE) is widely used for the diagnosis of small bowel diseases. The clinical performance and complications of small bowel CE, including completion rate, capsule retention rate, and indications, have been previously described in Korea. This study aimed at estimating the recent changes in clinical performance and complications of small bowel CE based on 17-year data from a Korean Capsule Endoscopy Registry.
Methods
CE registry data from 35 hospitals were retrospectively analyzed. Clinical information, including completion rate, capsule retention rate, and indications, was collected and analyzed. In addition, the most recent 5-year data for CE examinations were compared with the previous 12-year data.
Results
A total of 4,650 CE examinations were analyzed. The most common indication for CE was obscure gastrointestinal bleeding (OGIB). The overall incomplete examination rate was 16% and the capsule retention rate was 3%. Crohn’s disease was a risk factor for capsule retention. Inadequate bowel preparation was significantly associated with capsule retention and incomplete examination. An indication other than OGIB was a risk factor for incomplete examination. A recent increasing trend of CE diagnosis of Crohn’s disease was observed. The most recent 5-year incomplete examination rate for CE examinations decreased compared with that of the previous 12 years.
Conclusions
The 17-year data suggested that CE is a useful and safe tool for diagnosing small bowel diseases. The incomplete examination rate of CE decreased with time, and OGIB was consistently the main indication for CE. Inadequate bowel preparation was significantly associated with capsule retention and incomplete examination.
Keywords: Capsule endoscopy; Intestine, small; Retention; Bowel preparation
INTRODUCTION
Since Capsule endoscopy (CE) was introduced in 2000, it has been widely used as the main tool for diagnosing small bowel diseases [1]. Although CE is useful for diagnosing small bowel diseases, it has some limitations including incomplete examinations and capsule retention [2-4]. Occasionally, capsules cannot reach the cecum due to various causes, thus leading to incomplete examination of the small bowel. Another problem is capsule retention. Most patients in whom capsule retention occurs are asymptomatic; however, some require surgical or enteroscopic capsule removal [4-9]. The clinical performance and complications of small bowel CE include completion rate, capsule retention rate, and indications [2,3]; these have also been described in Korea [10]. This study aimed to investigate the clinical performance and complications of small bowel CE based on 17-year data from a Korean Capsule Endoscopy Registry. Furthermore, recent changes in the clinical performance and complications of small bowel CE were also evaluated.
METHODS
CE registry data from 35 hospitals, collected between October 2002 and April 2019, were retrospectively analyzed. Clinical information, including demographic data, completion rate, capsule retention rate, indications, CE diagnosis, and bowel preparation data, was collected and analyzed. From September 2014, health insurance benefits were provided to patients with obscure gastrointestinal bleeding (OGIB) in Korea. However, for patients with small bowel tumor(s), Crohn’s disease, and other small bowel diseases, a patient burden of 80% was applied. As such, data from the most recent 5 years (September 2014 to April 2019) were compared with those from the previous 12 years (October 2002 to August 2014).
Indications for CE included OGIB, abdominal pain, chronic diarrhea, small bowel tumor(s), Crohn’s disease, weight loss, protein-losing enteropathy, and screening. OGIB was defined as bleeding of unknown cause that persisted or recurred after initial upper gastrointestinal endoscopy and colonoscopy with negative results [11,12]. In addition to overt bleeding (melena or hematochezia), occult bleeding (persistent iron deficiency anemia or positive stool occult blood) was also considered OGIB [12,13].
Before CE examinations, patients were offered a bowel preparation regimen according to clinician preferences. Options for the bowel preparation included nil per os (NPO), polyethylene glycol (PEG), PEG + ascorbic acid, sodium phosphate (NaP), picosulfate, or others. Bowel preparation quality was categorized by independent examiners as follows: excellent, ≥ 75% of the mucosa visualized; good, 50% to 74% of the mucosa visualized; fair, 25% to 49% of the mucosa visualized; poor, ≤ 24% of the mucosa visualized [14]. For the purpose of study analysis, excellent or good bowel preparation were deemed adequate, and fair or poor preparation were deemed inadequate [15]. Comparison was performed between adequate and inadequate bowel preparation quality.
CE diagnoses were based on CE structured terminology. Complete examination was defined when the capsule reached the cecum during the recording time [2,3]. Capsule retention was defined when the capsule remained in the digestive tract for > 2 weeks [2,10]. Completion and capsule retention rates were calculated, and risk factors affecting incomplete examination and capsule retention were also investigated. Acquisition of informed consent was exempted and the study design was approved by the Institutional Review Board of Seoul Metropolitan Government Seoul National University Boramae Medical Center (approval number: 20190802/10-2019-62/091).
Data are expressed as mean ± standard deviation (SD) for continuous variables and number (%) for categorical variables. Risk factors for incomplete examination and capsule retention were analyzed using logistic regression models. Statistical analysis was performed using SPSS version 20.0 (IBM Corporation, Armonk, NY, USA).
RESULTS
Demographics and indications
A total of 4,650 CE examinations were analyzed. The mean ± SD age of the study population was 53.5 ± 18.8 years, and 60.3% was male. The overall incomplete examination rate was 16.3%, and the capsule retention rate was 3%. The incomplete examination rate of recent CE examinations (from September 2014 to April 2019) decreased compared with that of previous examinations (9.4% vs. 18.9%, p < 0.001) (Table 1). The most common indication for CE was OGIB (64.4%). Patients in whom the indication for CE was OGIB accounted for 68.8% in recent CE examinations and 62.7% in previous CE examinations (p < 0.001) (Table 2).
Table 1.
Demographic information and incomplete examination and retention rates
| Variable | Total | ~Aug. 31, 2014 | Sep. 1, 2014~ |
|---|---|---|---|
| Age | 53.5 ± 18.8 | 53.1 ± 18.1 | 55.0 ± 20.5 |
| Male sex | 2,804 (60.3) | 2,067 (61.1) | 681 (58.2) |
| Incompletion | 678 (16.3) | 570 (18.9) | 108 (9.4)a |
| Retention | 125 (3.0) | 105 (3.2) | 20 (2.6) |
Values are presented as mean ± SD or number (%).
Decreased trend.
Table 2.
Indications for capsule endoscopy
| Variable | Total | ~Aug. 31, 2014 | Sep. 1, 2014~ |
|---|---|---|---|
| Obscure GI bleeding | 2,965 (64.4) | 2,110 (62.7) | 790 (68.8)a |
| Overt | 2,445 (53.1) | 1,755 (52.2) | 638 (55.6) |
| Occult | 520 (11.3) | 355 (10.5) | 152 (13.2) |
| Abdominal pain | 724 (15.7) | 594 (17.7) | 117 (10.2) |
| Crohn’s disease | 212 (4.6) | 119 (3.5) | 86 (7.5)a |
| Small bowel tumor | 166 (3.6) | 122 (3.6) | 42 (3.7) |
| Chronic diarrhea | 171 (3.7) | 118 (3.5) | 51 (4.4) |
| Weight loss | 19 (0.4) | 18 (0.5) | 1 (0.1) |
| Cancer of unknown primary site | 4 (0.1) | 3 (0.1) | 0 |
| Protein-losing enteropathy | 15 (0.3) | 6 (0.2) | 7 (0.6) |
| Behcet’s disease, TB enteritis | 44 (1.0) | 21 (0.6) | 23 (2.0) |
| Ileus | 13 (0.3) | 5 (0.1) | 8 (0.7) |
| Screening | 214 (4.6) | 209 (6.2) | 2 (0.2) |
Values are presented as number (%).
GI, gastrointestinal; TB, tuberculous.
Increased trend.
CE diagnoses
Positive CE diagnosis was obtained in 63.8% CE examinations, while negative (normal) CE diagnosis was obtained in 36.2% CE examinations. Recent CE examinations yielded normal results in 28.4%, which was lower than the normal results in previous CE examinations (38.5%) (p < 0.001). CE diagnoses are summarized in Table 3. A recent increasing trend of CE diagnosis of Crohn’s disease was observed (6.3% vs. 8.5%, p = 0.014). Regarding nonsteroidal anti-inflammatory drug (NSAID) enteropathy, significant changes with time were not observed (5.7% vs. 6.5%, p = 0.305).
Table 3.
Capsule endoscopic diagnosis
| Variable | Total | ~Aug. 31, 2014 | Sep. 1, 2014~ |
|---|---|---|---|
| Normal | 1,647 (36.2) | 1,285 (38.5) | 322 (28.4)a |
| Vascular lesions | |||
| Angiodysplasia, telangiectasia, Dieulafoy’s lesion | 442 (9.7) | 349 (10.4) | 87 (7.7) |
| Bleeding of unidentified origin | 234 (5.1) | 122 (3.7) | 109 (9.6) |
| Varices | 12 (0.3) | 10 (0.3) | 2 (0.2) |
| Inflammatory lesions | |||
| Erosion, not signified | 365 (8.0) | 233 (7) | 130 (11.5) |
| Ulcer, not signified | 469 (10.3) | 352 (10.5) | 112 (9.9) |
| Hemorrhagic enteropathy | 31 (0.7) | 28 (0.8) | 3 (0.3) |
| Congestive enteropathy | 13 (0.3) | 13 (0.4) | 6 (0.5) |
| H-S purpura, vasculitis | 11 (0.2) | 10 (0.3) | 1 (0.1) |
| Ischemic enteritis | 9 (0.2) | 6 (0.2) | 3 (0.3) |
| NSAID enteropathy | 267 (5.9) | 190 (5.7) | 74 (6.5) |
| TB enteritis | 30 (0.7) | 16 (0.5) | 12 (1.1) |
| Behcet’s enteritis | 33 (0.7) | 22 (0.7) | 11 (1.0) |
| Radiation enteritis | 9 (0.2) | 8 (0.2) | 0 |
| Eosinophilic enteritis | 18 (0.4) | 10 (0.3) | 6 (0.5) |
| Crohn’s disease | 316 (6.9) | 211 (6.3) | 96 (8.5)b |
| CMUSE | 3 (0.1) | 1 (0) | 2 (0.2) |
| Tumor lesions | |||
| Lymphoid hyperplasia | 25 (0.5) | 22 (0.7) | 3 (0.3) |
| Lymphangiectasia | 30 (0.7) | 17 (0.5) | 12 (1.1) |
| Malignant tumor | 50 (1.1) | 40 (1.2) | 9 (0.8) |
| Submucosal tumor | 146 (3.2) | 120 (3.6) | 24 (2.1) |
| Polyp, adenomatous | 25 (0.5) | 21 (0.6) | 4 (0.4) |
| Polyp, non-neoplastic | 134 (2.9) | 105 (3.1) | 25 (2.2) |
| Peutz-Jeghers syndrome | 10 (0.2) | 7 (0.2) | 3 (0.3) |
| Hemangioma | 4 (0.1) | 2 (0.1) | 2 (0.2) |
| Lymphangioma | 3 (0.1) | 2 (0.1) | 1 (0.1) |
| Others | 220 (4.8) | 138 (4.1) | 82 (7.2) |
Values are presented as number (%).
H-S, Henoch–Schönlein; NSAID, nonsteroidal anti-inflammatory drug; TB, tuberculous; CMUSE, cryptogenic multifocal ulcerous stenosing enteritis.
Decreased trend.
Increased trend.
Factors associated with incomplete examination and capsule retention
Factors associated with incomplete examination included inadequate bowel preparation and an indication other than OGIB (Table 4). Crohn’s disease was a risk factor for capsule retention, and inadequate bowel preparation was significantly associated with capsule retention (Table 5). The capsule retention rate was the highest among patients with Crohn’s disease (Table 6).
Table 4.
Factors associated with incomplete examination
| Variable | Crude |
Age and sex adjusted |
||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p value | OR | 95% CI | p value | |
| Age | 1.005 | 1.001–1.009 | 0.026 | |||
| Male sex | 0.911 | 0.771–1.076 | 0.274 | |||
| Indication for capsule endoscopy | ||||||
| OGIB vs. others | 0.761 | 0.642–0.902 | 0.002 | 0.712 | 0.597–0.850 | < 0.001 |
| Crohn’s disease vs. others | 0.864 | 0.574–1.301 | 0.484 | 0.966 | 0.636–1.467 | 0.871 |
| Small bowel tumor vs. others | 0.827 | 0.523–1.308 | 0.418 | 0.868 | 0.548–1.375 | 0.548 |
| Bowel preparation | ||||||
| Inadequate vs. adequate | 1.757 | 1.479–2.086 | < 0.001 | 1.750 | 1.472–2.080 | < 0.001 |
OR, odds ratio; CI, confidence interval; OGIB, obscure gastrointestinal bleeding.
Table 5.
Factors associated with capsule retention
| Variable | Crude |
Age and sex adjusted |
||||
|---|---|---|---|---|---|---|
| OR | 95% CI | p value | OR | 95% CI | p value | |
| Age | 0.999 | 0.989–1.008 | 0.814 | |||
| Male sex | 0.83 | 0.580–1.188 | 0.309 | |||
| Indication for capsule endoscopy | ||||||
| OGIB vs. others | 1.083 | 0.745–1.575 | 0.677 | 1.092 | 0.743–1.604 | 0.654 |
| Crohn’s disease vs. others | 2.264 | 1.226–4.182 | 0.009 | 2.380 | 1.258–4.505 | 0.008 |
| Small bowel tumor vs. others | 0.213 | 0.030–1.533 | 0.124 | 0.209 | 0.029–1.506 | 0.120 |
| Bowel preparation | ||||||
| Inadequate vs. adequate | 2.434 | 1.677–3.533 | < 0.001 | 2.412 | 1.657–3.510 | < 0.001 |
OR, odds ratio; CI, confidence interval; OGIB, obscure gastrointestinal bleeding.
Table 6.
Capsule retention rates according to indications for capsule endoscopy
| Indications of capsule endoscopy | No. (%) |
|---|---|
| Obscure GI bleeding | 82 (3.1) |
| Abdominal pain | 20 (3.0) |
| Crohn’s disease | 12 (6.3) |
| Small bowel tumor | 1 (0.7) |
| Screening | 0 |
| Chronic diarrhea | 2 (1.3) |
GI, gastrointestinal.
Bowel preparation
The quality of bowel preparation significantly differed according to bowel preparation regimen (Table 7). When the proportion of adequate bowel preparation after ingesting the bowel preparation regimen was compared pairwise with that after NPO, significant differences were identified for PEG 4 L, PEG + ascorbic acid 2 L, and NaP (p = 0.017, p < 0.001, p = 0.028, respectively). When Bonferroni correction was applied for multiple comparisons (p < 0.0125), the proportion of adequate bowel preparation was different only between PEG + ascorbic acid 2 L and NPO. PEG 2 L was previously the most commonly used regimen (47.9%); however, recently, the PEG + ascorbic acid regimen has become the most popular (58.1%) (Table 8).
Table 7.
Bowel preparation quality according to bowel preparation method
| Variable | NPO | PEG 4 L | PEG 2 L | PEG + Asc 2 L | NaP | p value |
|---|---|---|---|---|---|---|
| Quality | < 0.001 | |||||
| Excellent | 149 (21.4) | 104 (16.1) | 165 (10.8) | 92 (13.5) | 89 (30.3) | |
| Good | 340 (48.9) | 388 (60.1) | 874 (57.5) | 289 (42.6) | 138 (46.9) | |
| Fair | 161 (23.2) | 119 (18.4) | 368 (24.2) | 215 (31.7) | 53 (18.0) | |
| Poor | 45 (6.5) | 35 (5.4) | 114 (7.5) | 83 (12.2) | 14 (4.8) | |
| Acceptability | < 0.001 | |||||
| Adequate | 489 (70.4) | 492a (76.2) | 1,039 (68.3) | 381a (56.1) | 227a (77.2) | |
| Inadequate | 206 (29.6) | 154 (23.8) | 482 (31.7) | 298 (43.9) | 67 (22.8) | |
| p value vs. NPO | Reference | 0.017 | 0.333 | < 0.001 | 0.028 |
Values are presented as number (%).
NPO, nil per os; PEG, polyethylene glycol; Asc, ascorbic acid; NaP, sodium phosphate.
Statistically significant in comparison with NPO (p < 0.05).
Table 8.
Trends in bowel preparation methods
| Variable | Total | ~Aug. 31, 2014 | Sep. 1, 2014~ |
|---|---|---|---|
| NPO | 704 (17.5) | 560 (19.2) | 144 (12.9) |
| PEG 4 L | 658 (16.3) | 546 (18.7) | 111 (10.0) |
| PEG 2 L | 1,553 (38.5) | 1,398 (47.9) | 155 (13.9) |
| PEG + Asc 2 L | 681 (16.9) | 34 (1.2) | 646 (58.1) |
| NaP | 297 (7.4) | 297 (10.2) | 0 |
| Picosulfate | 64 (1.6) | 8 (0.3) | 56 (4.8) |
| Others | 77 (1.9) | 77 (2.7) | 0 |
Values are presented as number (%).
NPO, nil per os; PEG, polyethylene glycol; Asc, ascorbic acid; NaP, sodium phosphate.
DISCUSSION
In this registry-based study including 4,650 CE examinations, the incomplete examination and capsule retention rates were determined. This study revealed an incomplete examination rate of 16%, which is similar to that reported in previous studies [2,3]. The capsule retention rate was 3%, which is slightly higher than that reported in previous studies [2,3]. The incomplete examination rate of recent CE (September 2014 to April 2019) decreased compared with that of previous CE (October 2002 to August 2014). With the extended battery life of newer CE technologies, more capsules have reached the ileocecal valve and cecum, leading to a decrease in the number of incomplete examinations [16,17]. With technical advances in radiological examinations, such as computed tomography enterography and magnetic resonance enterography, more patients with small bowel stricture(s) can be diagnosed before undergoing CE. However, the decrease in capsule retention rate over time was not statistically significant in our study. Moreover, our data lacked radiological examination results and, thus, analysis in this regard was not possible. The most common indication for CE was OGIB (64.4%), which is consistent with results reported in previous studies [2,3,10]. In our study, recent CE examinations had more OGIB indications than previous CE examinations (p < 0.001), which can be explained by the inception of health insurance coverage for patients with OGIB in September 2014.
Recently, the incidence of Crohn’s disease has been found to be increasing in Korea [18]. Our study revealed a recent increasing tendency of indications and CE diagnosis of Crohn’s disease. CE diagnosis of NSAID enteropathy demonstrated an increasing tendency without statistical significance. The increase in NSAID enteropathy can be attributed to the aging population. In our study, the proportion of normal results was smaller in recent CE examinations than in previous examinations. Recent advances in CE technology with improved resolution may have led to more lesion detection and fewer patients diagnosed with normal findings.
Our study revealed that factors associated with incomplete examination were inadequate bowel preparation and indications other than OGIB, which is consistent with the results of a previous study [10]. With adequate bowel preparation, CE is more likely to be completed. Blood materials in patients with gastrointestinal bleeding appear to act as laxatives, thus helping the capsule proceed through the ileocecal valve. In our study, inadequate bowel preparation was significantly associated with capsule retention, which is also consistent with the results of previous studies [2,10]. The presence of stenotic portions in the small bowel may lead to both inadequate bowel preparation and capsule retention. Additionally, fecal materials stuck in the stenotic portion may result in capsule retention. Although causality was difficult to determine, our study revealed that inadequate bowel preparation was significantly associated with capsule retention. Crohn’s disease was a risk factor for capsule retention and the capsule retention rate was the highest among patients with the indication of Crohn’s disease. Special caution or using a patency capsule will be needed in patients with Crohn’s disease.
In this study, bowel preparation quality was affected by the bowel preparation regimen. PEG 4 L or NaP more favorably affected bowel preparation than NPO; however, PEG + ascorbic acid resulted in worse bowel preparation than NPO. In our study, the recent data revealed that PEG + ascorbic acid regimen was the most widely used. This can be explained by the fact that recent guidelines recommend that CE should be performed as soon as possible (generally after colonoscopy) in patients with overt, obscure bleeding [11], and PEG + ascorbic acid has recently become the most popular regimen for colonoscopy in Korea [19]. The time interval from the ingestion of the bowel preparation regimen to performing CE can be delayed because performing colonoscopy and clinician’s decision-making to perform CE after colonoscopy can take time. This time delay may adversely affect bowel preparation quality [20,21], because debris and intestinal fluid can affect preparation of the distal small bowel [22].
Our study had some limitations, the first of which was its retrospective design and, as such, may have been susceptible to selection bias. Moreover, our data may have been susceptible to the under-reporting of complications. Second, our investigation was a multi-center, registry-based study, and the data collection methods used at each institution were not monitored. There was no auditing system to control data collection. However, this was a large study based on 17-year registry data. Time trends were also investigated between recent and previous data.
In conclusion, our 17-year data suggest that CE is a useful and safe tool for diagnosing small bowel diseases. The incomplete examination rate of CE decreased with time and OGIB was consistently the primary indication for CE. Inadequate bowel preparation was significantly associated with capsule retention and incomplete examination.
KEY MESSAGE
1. The incomplete examination rate of capsule endoscopy decreased over time.
2. Obscure gastrointestinal bleeding was consistently the primary indication for capsule endoscopy.
3. Inadequate bowel preparation was significantly associated with capsule retention and incomplete examination.
Acknowledgments
This research was supported by a grant of the Korean Health Technology R & D project through the Korean Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HI19C0665).
Footnotes
No potential conflict of interest relevant to this article was reported.
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