Abstract
Balloon-assisted enteroscopy (BAE) is an important diagnostic modality for ongoing obscure gastrointestinal bleeding (OGIB). However, it is difficult to determine the optimal insertion route. We retrospectively analyzed the records of patients with OGIB contained in a multicenter enteroscopy database of 1108 balloon-assisted enteroscopy (BAE) procedures (875 patients) to find out factors affecting BAE route selection in patients with OGIB. A total of 603 BAE procedures in 512 patients were investigated: there were 392 (65.0%) bidirectional and 211 (35.0%) unidirectional procedures. Overt OGIB was more frequent in the latter group (p = 0.024). Computed tomography (CT) was more frequently performed in the unidirectional group (p < 0.001). Capsule endoscopy and a small bowel barium study were performed more frequently in the bidirectional group (p < 0.001 and p = 0.039, respectively). Multivariate analysis showed that occult OGIB, capsule endoscopy and a small bowel barium study were independently associated with use of the bidirectional approach (p = 0.011, p = 0.013 and p = 0.046, respectively). Conversely, CT was associated with use of the unidirectional approach (p < 0.001). Conclusion: CT can aid the selection of an optimal insertion route in OGIB patients. However, capsule endoscopy and small bowel barium study are unhelpful.
Keywords: obscure gastrointestinal bleeding, small bowel bleeding, enteroscopy, capsule endoscopy
1. Introduction
Obscure gastrointestinal bleeding (OGIB), until recently termed small bowel bleeding or potential small bowel bleeding, is relatively rare, accounting for 5–10% of all cases of gastrointestinal (GI) bleeding [1,2,3]. Most OGIB is caused by small bowel bleeding, The American College of Gastroenterology (ACG) recommends that OGIB be reclassified as small bowel bleeding [2]. Recently, various imaging modalities, including video capsule endoscopy (VCE), deep enteroscopy and radiographic imaging have been applied to the small bowel. The utility of these modalities depends on the extent of bleeding and the patient’s condition. Several guidelines have been proposed by various societies [2,4,5,6]. The Japanese guidelines propose that computed tomography (CT) should be considered before capsule endoscopy as the first-line procedure for small bowel evaluation. Device-assisted enteroscopy (DAE) is recommended for patients with persistent overt bleeding or who are OGIB-positive on capsule endoscopy or CT. DAE, including double-balloon [7], single-balloon [8], and spiral enteroscopy [9], enables simultaneous endoscopic tissue sampling and hemostasis. Although DAE is ideal for small bowel evaluation, the use of DAE is very limited given the long procedure times, technical difficulties and need for extensive equipment and several assistants. A recent study introduced a new form of enteroscopy; prototype single-balloon enteroscopy with passive bending and high force transmission that helps deep insertion into the small intestine [10], but the use of DAEs still has technical limitations. One systematic review of double-balloon endoscopy reported that serious complications included perforation, pancreatitis and bleeding, at a rate of 0.72% (95% confidence interval [CI] 0.56–0.90%) [11]. Thus, it is important to consider whether DAE is appropriate and to perform the procedure carefully. An appropriate insertion route is also important, but to the best of our knowledge no study has addressed this topic. Therefore, we aimed to identify factors affecting DAE route selection in OGIB patients by analyzing a large, multicenter enteroscopy database.
2. Materials and Methods
2.1. Patients and Study Design
We extracted data for OGIB patients who underwent enteroscopy from a multicenter, retrospective BAE registry. OGIB was defined as bleeding of unknown origin that persisted or recurred after negative initial or primary upper and lower endoscopy. We obtained data on demographic characteristics and factors affecting the BAE insertion route, including the OGIB type, initial insertion route, use of a unidirectional or bidirectional approach, final diagnosis and diagnostic modality. Patients were divided into unidirectional and bidirectional groups by the oral and/or anal approach. Data collection and analysis were approved by the institutional review board of each participating institution.
2.2. BAE
Enteroscopic examinations were performed using a double-balloon enteroscope (EN-450P5/20, T5/20; Fujinon Inc., Saitama, Japan) and a single-balloon enteroscope (SIF-Q180; Olympus, Tokyo, Japan), which are both available in South Korea. The insertion route was determined based on the clinical features, capsule endoscopy, CT and other imaging modalities. If the oral approach was used, patients fasted for 8–12 h before BAE; if the anal approach was used, patients ingested 2–4 L of polyethylene glycol-electrolyte lavage solution on the day before BAE. All procedures were performed with patients under conscious to deep sedation (established by the endoscopists) according to the sedation protocols of the various centers.
2.3. Definitions
The bidirectional approach was both oral and anal, while the unidirectional approach was oral or anal. We divided OGIB into overt and occult types. Overt OGIB was associated with the passage of visible blood (melena or hematochezia) from a bleeding source in the small bowel, while occult OGIB referred to iron-deficiency anemia with or without a positive fecal occult blood test. The final diagnosis was broadly classified as tumorous disease (benign or malignant tumors and polyposis, non-tumorous disease (vascular and inflammatory lesions), lesions of the stomach and duodenum, or lesions of the colon.
2.4. Statistical Analysis
The t-test and chi-squared test were used to compare data between the unidirectional and bidirectional groups. Variables that were significant, or showed a trend toward significance, in the univariate analysis were included in a multivariate (binary logistic regression) analysis. SAS software (ver. 9.0; SAS Institute, Cary, NC, USA) was used for all analyses. A p-value < 0.05 was considered to indicate statistical significance.
3. Results
3.1. Baseline Characteristics of the Study Subjects
We reviewed a total of 1108 BAEs performed on 875 patients. Of these, 603 BAEs of 512 patients with OGIB were included in the final analysis (Figure 1). The unidirectional and bidirectional groups contained 392 (65.0%) and 211 (35.0%) BAEs, respectively. The mean patient age did not differ between the two groups (52.2 ± 18.5 vs. 49.4 ± 18.1 years, p = 0.731). Overt OGIB was more common in the unidirectional than bidirectional group (p = 0.024). The initial insertion route and final diagnosis did not differ between the two groups. Other patient characteristics are summarized in Table 1.
Figure 1.
Flow diagram of the present study. BAE, balloon-assisted enteroscopy; OGIB, obscure gastrointestinal bleeding.
Table 1.
Patient characteristics (Univariate analysis).
| Total (n = 603) |
Unidirectional Group (n = 392) |
Bidirectional Group (n = 211) |
p-Value | |
|---|---|---|---|---|
| Age | 52.2 ± 18.5 | 49.4 ± 18.1 | 0.731 | |
| Sex | 0.807 | |||
| Male | 379 (62.8) | 245 (62.5) | 134 (63.5) | |
| Female | 224 (37.2) | 147 (37.5) | 77 (36.5) | |
| OGIB | 0.024 | |||
| Overt | 528 (87.6) | 352 (89.8) | 176 (83.4) | |
| Occult | 75 (12.4) | 40 (10.2) | 35 (16.6) | |
| Medical History | ||||
| DM | 92 (15.3) | 65 (16.6) | 27 (12.8) | 0.218 |
| HTN | 162 (26.9) | 100 (25.5) | 62 (29.4) | 0.306 |
| LC | 28 (4.6) | 21 (5.4) | 7 (3.3) | 0.256 |
| ESRD | 22 (3.7) | 19 (4.9) | 3 (1.4) | 0.039 |
| Crohn’s disease | 19 (3.2) | 12 (3.1) | 7 (3.3) | 0.864 |
| Behcet disease | 6 (1.0) | 1 (0.3) | 5 (2.4) | 0.022 |
| Medication | ||||
| Aspirin | 99 (16.4) | 68 (17.4) | 31 (14.7) | 0.401 |
| Antiplatelet agent | 35 (5.8) | 26 (6.6) | 9 (4.3) | 0.236 |
| Anticoagulant | 21 (3.9) | 12 (3.1) | 9 (4.3) | 0.442 |
| Laboratory finding | ||||
| Hemoglobin(g/dL) | 9.2 ± 2.6 | 9.0 ± 2.4 | 0.463 | |
| Platelet | 231.6 ± 103.6 | 248.5 ± 99.8 | 0.059 | |
| BUN | 19.1 ± 16.4 | 16.3 ± 13.8 | 0.036 | |
| Creatinine | 1.2 ± 1.9 | 0.9 ± 0.4 | 0.001 | |
| Protein | 5.8 ± 1.0 | 6.1 ± 1.0 | 0.004 | |
| Albumin | 3.4 ± 0.7 | 3.5 ± 0.7 | 0.054 | |
| Initial | 0.134 | |||
| Insertion Route | ||||
| Oral approach | 359 (59.5) | 242 (61.7) | 117 (55.5) | |
| Anal approach | 244 (40.5) | 150 (38.3) | 94 (44.6) | |
| Final diagnosis | 0.848 | |||
| Tumorous | 67 (11.1) | 46 (11.7) | 21 (10.0) | |
| Non-tumorous | 515 (85.4) | 333 (85.0) | 182 (86.3) | |
| UGI | 17 (2.8) | 11 (2.8) | 6 (2.8) | |
| Colon | 4 (0.7) | 2 (0.5) | 2 (1.0) |
Values are presented as mean ± SD or n (%). OGIB, obscure gastrointestinal bleeding; DM, diabetes mellitus; HTN, hypertension; LC, liver cirrhosis; ESRD, end-stage renal disease; UGI, upper gastrointestinal track.
3.2. Diagnostic Modalities
The diagnostic modalities used before BAE included CT, capsule endoscopy, a barium study, a bleeding scan and an angiographic Meckel scan. CT was more frequently performed in the unidirectional group (p < 0.001). Capsule endoscopy and a small bowel barium study were more frequently performed in the bidirectional group (p < 0.001 and p = 0.039, respectively). The diagnostic modalities are listed in Table 2.
Table 2.
Diagnostic modalities (univariate analysis).
| Total (n = 603) N (%) |
Unidirectional Group (n = 392) N (%) |
Bidirectional Group (n = 211) N (%) |
p-Value | |
|---|---|---|---|---|
| CT | <0.001 | |||
| No | 197 (32.7) | 99 (25.3) | 98 (46.5) | |
| Yes | 406 (67.3) | 293 (74.7) | 113 (53.6) | |
| Capsule | <0.001 | |||
| No | 407 (67.5) | 286 (73.0) | 121 (57.4) | |
| Yes | 196 (32.5) | 106 (27.0) | 90 (42.6) | |
| Barium study | 0.039 | |||
| (small bowel) | ||||
| No | 393 (65.2) | 267 (68.1) | 126 (59.7) | |
| Yes | 210 (34.8) | 125 (31.9) | 85 (40.3) | |
| Bleeding Scan | 0.747 | |||
| No | 459 (76.1) | 300 (76.5) | 159 (75.4) | |
| Yes | 144 (23.9) | 92 (23.5) | 52 (24.6) | |
| Angiography | 0.186 | |||
| No | 448 (74.3) | 298 (76.0) | 150 (71.1) | |
| Yes | 155 (25.7) | 94 (24.0) | 61 (28.9) | |
| Meckel scan | 0.878 | |||
| No | 553 (91.7) | 359 (91.6) | 194 (91.9) | |
| Yes | 50 (8.3) | 33 (8.4) | 17 (8.1) |
Values are presented as n (%). CT, computed tomography.
3.3. Factors Associated with the Bidirectional Approach
On univariate analysis, occult OGIB, low blood urea nitrogen (BUN) and creatinine levels, high protein and albumin levels, no CT examination, capsule endoscopy and a small bowel barium study were associated with the bidirectional approach. Multivariate analysis (Table 3) showed that occult OGIB was independently associated with the bidirectional approach. Of the diagnostic modalities, capsule endoscopy and a small bowel barium study were associated with the bidirectional approach (p = 0.013 and p = 0.046, respectively). Conversely, CT was associated with the unidirectional approach (p < 0.001). On univariate analysis, we found no significant correlation between the bidirectional approach and a low BUN or high albumin level.
Table 3.
Factors affecting DAE route selection in OGIB patients (Multivariate analysis).
| Estimated Value | Standard Error | Odds Ratio | 95% CI | p-Value | |
|---|---|---|---|---|---|
| Age | −0.002 | 0.006 | 0.075 | 0.988–1.009 | 0.784 |
| Sex | 0.087 | 0.202 | 0.184 | 0.734–1.622 | 0.668 |
| OGIB (Occult) | 0.704 | 0.278 | 6.433 | 1.174–3.485 | 0.011 |
| CT | –0.923 | 0.203 | 20.590 | 0.267–0.592 | <0.001 |
| Capsule | 0.506 | 0.204 | 6.137 | 1.112–2.477 | 0.013 |
| Barium study (small bowel) | 0.405 | 0.203 | 3.983 | 1.007–2.230 | 0.046 |
| BUN | –0.008 | 0.007 | 1.310 | 0.977–1.006 | 0.252 |
| Albumin | 0.180 | 0.147 | 1.494 | 0.987–1.598 | 0.222 |
DAE, device-assisted enteroscopy; CI, confidence interval; OGIB, obscure gastrointestinal bleeding; CT, computed tomography.
4. Discussion
BAE yields tissue samples for diagnosis and allows endoscopic hemostasis in OGIB patients. The diagnostic rate is 60–80% and the treatment success rate 40–73% [12,13,14]. In 40–50% of patients, BAE findings influence the treatment strategy [15]. Recently, urgent BAE (<72 h) of OGIB patients has been reported to improve the diagnostic rate compared to non-urgent BAE (70% vs. 30%, p < 0.050); the treatment rate was also improved (54% vs. 15%, p < 0.001) [16]. However, BAE can cause various complications. The procedure-related mortality rate is 0.01% and care is required in these cases [11]. In addition, BAE takes a relatively long time and several medical personnel are needed, including nurses, assistant doctors and radiologists. Therefore, it is very important to determine the optimal insertion route.
We found that CT identified the optimal insertion route and the bidirectional approach became unnecessary. This supports the Japanese guideline, which states that CT is essential in the absence of a contra-indication such as renal failure or contrast allergy [5,17,18]. The American, European and Korean guidelines suggest that capsule endoscopy should be the first choice diagnostic modality [2,4,6]. Differences in the modalities used have been attributed to CT availability [18]. However, CT is quicker than capsule endoscopy and identifies tumors and bleeding foci. DAE combined with abdominal CT is a simple and effective method for the diagnosis of intestinal vascular malformation bleeding [19]. Therefore, CT should be performed to determine the BAE insertion route.
Capsule endoscopy and a small bowel barium study can also locate OGIB foci. The diagnostic rate and positive and negative predictive rates, of capsule endoscopy for OGIB are 60–83%, 94–97% and 83–100%, respectively. Recent studies have shown that the capsule transit time was useful for determining the DBE route [20,21]. This contrasts with our findings that capsule endoscopy and a small bowel barium study were associated with the bidirectional route. There are several possible explanations. First, BAE can be performed without prior capsule endoscopy in patients with overt OGIB. In such cases, the optimal insertion route can be selected by reference to the bleeding pattern (hematochezia or melena). We found that the optimal insertion route was determined more often in patients with overt than occult OGIB. Second, capsule endoscopy may serve as the first-choice diagnostic modality for occult OGIB, where it may be difficult to locate the bleeding focus. A recent study indicated that the failure rates of capsule endoscopy were 18.9%, 5.9% and 0.5% for small bowel tumors, vascular disease and ulcers, respectively [22], suggesting that it may be difficult to determine the optimal insertion route for BAE. Third, the small bowel barium studies had low diagnostic OGIB rates (3–17%) [23,24,25,26] and was, thus, not recommended for evaluation of OGIB [2].
Several limitations of this study should be addressed. First, it was a retrospective registry study. In addition, BAEs were performed by several endoscopists in various centers, so technical differences in BAE implementation were inevitable. However, that the study included a large number of OGIB BAEs from a large, multicenter enteroscopy database.
5. Conclusions
An optimal BAE insertion route in OGIB is important; CT is invaluable in this regard. Unlike previous studies, we found that capsule endoscopy and small intestinal imaging were unhelpful in selecting an optimal BAE insertion route. In patients with overt (in contrast to occult) OGIB, it may be easier to determine the optimal insertion route. Although CT availability varies among countries, CT scan is most commonly used than capsule endoscopy and maybe it is the most cost-effective initial imaging strategy. Thus, a country-specific prospective study of CT efficacy prior to BAE in OGIB patients is required.
Author Contributions
S.H.J. and D.H.B. planned and designed the review. E.R.K., J.K., D.-H.Y., S.R.J., H.J.J., S.J.P. and J.P.I. carried out data collection. Data analysis was performed by S.H. and D.H.B. under the supervision of C.S.E. and S.H.J. supervised the writing of the manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HI19C1298).
Institutional Review Board Statement
This study was approved by the Institutional Review Board of the Catholic University of Korea (XC21RCDI0121, approved on 16 September 2021).
Informed Consent Statement
Not applicable.
Data Availability Statement
The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.
Conflicts of Interest
The authors declare that they have no competing interest.
Footnotes
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.