Early rebleeding rate following endoscopic treatment of colonic diverticular bleeding: a systematic review and meta-analysis
Isha Delaleeuwea*, Jennifer Aounb*, Hendrik Reynaerta, Paraskevas Gkolfakisc^, Pierre Eisendrathb^
UZ Brussel, Jette, Belgium; CHU Saint-Pierre, Brussels, Belgium; “Konstantopoulio-Patision” General Hospital of Nea Ionia, Athens, Greece
aDepartment of Hepatology and Gastroenterology, UZ Brussel, Jette, Belgium (Isha Delaleeuwe, Hendrik Reynaert); bDepartment of Hepatology and Gastroenterology, CHU Saint-Pierre, Brussels, Belgium (Jennifer Aoun, Pierre Eisendrath); cDepartment of Gastroenterology, “Konstantopoulio-Patision” General Hospital of Nea Ionia, Athens, Greece (Paraskevas Gkolfakis)
Abstract
Background Various endoscopic treatment options are available for managing colonic diverticular bleeding (CDB). We conducted a systematic review and meta-analysis to assess the effectiveness of these endoscopic interventions in achieving hemostasis in patients with CDB, focusing on early rebleeding rate (ERR) within 30 days.
Methods A systematic literature search of the PubMed and Cochrane Library databases was performed for articles published between January 2008 and December 2023. Studies evaluating endoscopic clipping, with or without epinephrine injection, endoscopic band ligation (EBL) and endoscopic snare ligation (EDSL) in the treatment of CDB were included. The primary outcome was the overall pooled ERR following successful hemostasis. Secondary outcomes addressed ERRs associated with various hemostatic endoscopic techniques, and pooled ERRs for both direct and indirect clipping methods. Results are presented as pooled rates and odds ratio (OR) with 95% confidence intervals (CI).
Results Sixteen studies were included, comprising 1435 patients with definite CDB of whom 1273 received endoscopic hemostatic treatment. Overall pooled ERR was 14.73% (95%CI 9.33-20.14%). Pooled ERRs were 9.83% (95%CI 7.41-12.26%) in the EBL/EDSL group and 22.32% (95%CI 12.48-32.16%) in the endoscopic clipping group (P=0.02). A subgroup analysis of the clipping group showed a significant difference between the pooled ERRs favoring direct clipping: 12.04% (95%CI 3.06-21.02%) vs. 27.74% (95%CI 18.34-37.14%), P=0.02. The measured effect favors direct over indirect clipping in reducing early rebleeding episodes: OR 0.45, 95%CI 0.24-0.85; P=0.01.
Conclusion In the management of patients presenting with CDB, EBL/EDSL and direct clipping showed significantly lower ERRs compared to indirect clipping.
Keywords Colonic diverticular bleeding, endoscopy, hemostasis, treatment
Ann Gastroenterol 2025; 38 (1): 41-50
Introduction
Colonic diverticular bleeding (CDB) is the most common cause of lower gastrointestinal bleeding (LGIB), accounting for 20-50% of cases worldwide [1]. The prevalence varies in the literature according to the colonic location of diverticular disease. Multicenter studies described a prevalence of CDB of 13% among LGIB in the United Kingdom vs. 63% in Japan, where right-sided diverticulosis, known to be at higher risk of bleeding, is more common [2]. Moreover, the reported incidence varies depending on the modality used for diagnosis [3]. In the absence of consensus about the diagnostic approach to CDB, physicians in Asian countries such as Japan resort more frequently to an endoscopic diagnosis for definite CDB than do those in the United Kingdom, for example (80% vs. 26%, respectively) [4]. Well-established risk factors for CDB include age older than 70 years, use of antithrombotics and nonsteroidal anti-inflammatory drugs (NSAIDs), and atherosclerosis [5]. The vast majority of CDB cases resolve spontaneously; however, some patients require intervention to achieve hemostasis [6]. Studies have shown endoscopic management to be less invasive, with a lower complication rate than transcatheter arterial embolization (TAE) or surgery [7]. Endoscopic treatment modalities, including endoscopic clipping (EC), with or without epinephrine injection, endoscopic band ligation (EBL) and endoscopic snare ligation (EDSL), have been shown to prevent early rebleeding occurrence (within 30 days), notably in the presence of stigmata of recent hemorrhage (SRH) [6]. No randomized control trials comparing the efficacy of the different endoscopic treatments have been published to date [8].
This systematic review aims to describe the overall pooled early rebleeding rate (ERR) among patients with definite CDB treated endoscopically. In addition, ERR was compared in relation to the different endoscopic techniques used, including indirect and direct clipping, among others.
Materials and methods
Protocol and registration
This review’s protocol has been registered at the International Prospective Register of Systematic Reviews (PROSPERO) under the registration number CRD42024499363.
Eligibility criteria
A search was conducted based on the PICO model, as follows:
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P: Adults presenting with CDB;
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I: Endoscopic techniques applied for hemostasis, including EC, EBL and EDSL, epinephrine injection;
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C: Not applicable;
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O: ERR after successful endoscopic hemostasis of CDB.
Studies published in the English language as full text, between the years 2008 and 2023, clinical trials, observational prospective studies, retrospective cohort studies and case series with more than 10 patients were included.
Patients under 18 years of age, ex vivo or animal models, LGIB of other etiology, and cases associated with diverticulitis, as well as clinical guidelines, systematic reviews and case reports, were excluded.
Information sources and search strategy
A systematic literature search of the PubMed and Cochrane Library (Cochrane Central Register of Controlled Trials) databases was performed in January 2024. Dedicated search terms were produced: (“Colonic Disease”[Mesh] OR “Colon”[Mesh] OR colon*[TIAB]) AND (diverticul*[TIAB] OR “Diverticulum”[Mesh]) AND (“Hemorrhage”[Mesh] OR hemorrhag*[TIAB] OR bleed*[TIAB]) AND (“Endoscopy, gastrointestinal”[Mesh] OR colonoscop*[TIAB] OR “Hemostasis, endoscopic”[MeSH Terms] OR “Endoscopic Hemostasis”[Text Word] OR clip* [TIAB] OR band*[TIAB] OR Epinephr*[TIAB] OR Snare[TIAB]) AND (2008:2023[pdat]).
Two investigators (ID, JA) independently assessed the potential relevance of the retrieved articles based on title and abstract. Subsequently, the full text of the selected articles was reviewed in the same manner to decide whether they were eligible for inclusion in the study. All references of selected articles were reviewed carefully for additional inclusions. In case of disagreement, the articles were included or not included after a joint discussion with senior investigators (PG, PE). This systematic review was performed according to the updated PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines from 2020 (Supplementary Table 1) [9].
Data collection and analysis
All eligible studies were assessed with the extraction of the following data: name of first author, year of study publication, country of publication, study design, endoscopic treatment modality used, number of patients enrolled, patients’ characteristics (sex, age, comorbidities, use of oral antithrombotics/NSAIDs, past history of diverticular bleeding), bowel preparation, location of CDB, SRH (defined as active bleeding, visible vessel or adherent clot), ERR (defined as any bleeding episode occurring during the first 30 days after initial endoscopic treatment), need for surgery or TAE, adverse events (perforation, diverticulitis).
Outcome measures
The primary outcome was to describe the pooled overall ERRs after successful endoscopic hemostasis of CDB. Secondary outcomes included a comparison of the ERR according to the different endoscopic modalities used for treatment. In addition, the pooled ERRs were calculated for the direct and indirect clipping methods. Direct clipping involves capturing the culprit vessel directly, whereas indirect clipping is defined as closing the diverticular orifice in a zipper-like manner [10].
Quality assessment and risk of bias
Quality assessment was carried out independently by 2 authors (ID, JA) using the National Heart, Lung, and Blood Institute (NHLBI) tool [11].
Statistical analysis
Data analysis was performed using the statistical software Review Manager (RevMan 5.3.5, Copenhagen, Denmark, the Nordic Cochrane Centre, the Cochrane Collaboration, 2014). Outcomes were compared using the random-effects model (DerSimonian and Laird method). Heterogeneity among studies was measured using the I2, with lower values representing lower levels of heterogeneity. In case of significant heterogeneity (P<0.1), a predefined sensitivity analysis was performed by repeating the analysis excluding 1 study at a time to assess the potential excessive influence of a single study on the overall significance. Forest plots were created for the visual display of results. Publication bias was assessed by visual inspection of the funnel plots for symmetry. Results are presented as pooled rates with 95% confidence intervals (CI), or as odds ratios (OR) with 95%CI. Finally, we used both overlapping CI inspection and the test for subgroup differences provided by the statistical software to perform a per-endoscopic modality subgroup analysis for ERR.
Ethical approval
This study was a systematic review. Ethics approval or institutional review board approval was not necessary, as the study did not involve patient consent.
Results
Study selection
The initial search produced 550 potentially relevant articles, of which 3 duplicates were removed, leaving 547 articles to be assessed. After records had been screened based on title and abstract, the full texts of 51 articles were reviewed. During this process, a total of 26 articles were excluded for not meeting the inclusion criteria, 5 after a joint discussion with senior investigators (PE and PG). These articles were assessed for overlapping cohorts, defined as the same endoscopic technique applied over the same time course, in the same hospital, and 9 additional articles were excluded. No articles were added after review of the references of the selected articles, resulting in a total of 16 articles that were included in this systematic review. The search methodology, following the PRISMA guidelines, is illustrated in Fig. 1 [9].
Figure 1 PRISMA flow diagram: flowchart of literature search
Characteristics of included studies
A total of 1435 patients with definite CDB were included, from 2 prospective [12,13] and 14 retrospective observational studies [14-27], of whom 1273 patients were treated endoscopically. Five of the 16 studies were multicenter, performed in 2-11 medical centers [12,17,18,21,24]. Studies were published between the years 2012 and 2022. Ten studies evaluated 1 endoscopic technique: EC in 6 studies [14,17-19,24,27], of which 1 study evaluated the over-the-scope-clip [19], EBL in 3 studies [22,25,26], and EDSL in 1 study [12]. Six studies compared 2 of the previously mentioned techniques [13,15,16,20,21,23]. The retrieved articles were mostly from Japan, with only 1 study from the United States of America [18].
The majority of patients from the included studies were male (72%), and the patients’ mean age ranged from 62-77 years. Fifteen articles reported the use of antithrombotics in patients with CDB (38%) [12-25,27], while 12 articles reported the use of NSAIDs (20%) [12-15,17-21,23,25,27]. Most patients (85%) underwent PEG bowel preparation before diagnostic endoscopy. The culprit bleeding diverticulum was identified in 98% of the patients, with missing data points in the remaining 2%. CDB was found in 68% of the cases in the right colon. SRH were described in almost all included studies (14 of 16), with a detection rate of active bleeding of 48% and 44% for visible vessel or adherent clot, while the remaining 8% had missing data. The characteristics of the included studies are summarized in Table 1.
Table 1 Demographics of included patients
Methodological quality and risk of bias
The overall quality of the included observational studies, according to the National Heart, Lung and Blood Institute quality assessment tool, was deemed good (Supplementary Table 2) [11]. Criteria including the research question, study population definition, exposure assessment prior to outcome measurement, sufficient timeframe to see an effect, exposure measures and assessment, outcome measures, and follow-up rate were clearly defined in all 16 included studies. The criterion of uniform eligibility was not met in 1 study [14]. The participation rate was less than 50% in 2 studies [14,18]. Sample size justification was described in the 2 included prospective studies [12,13]. In view of the fact that the exposure of interest, defined as endoscopic treatment modality, is a dichotomous variable, analysis of different levels of exposure was not applicable for the totality of the studies. Similarly, an assessment of repeated exposure was not pertinent in the totality of the studies, since endoscopic treatment was performed only once. Finally, the method of hemostasis was selected according to the physicians’ judgment in the 2 prospective studies [12,13], while no blinding was possible in the other retrospective studies.
Primary endpoint – overall pooled ERR
Data from 16 studies, including 1273 endoscopically treated patients for definite CDB, showed an overall pooled ERR of 14.73% (95%CI 9.33-20.14%) (Fig. 2). Visual inspection of the funnel plot did not reveal any publication bias (Supplementary Fig. 1).
Figure 2 Overall early rebleeding rate
SE, standard error; CI, confidence interval
Secondary endpoints
A pooled ERR was calculated for the different endoscopic modalities, regrouping EDSL and EBL in 1 group [12,13,15,20-23,25,26] and EC in the other group [13-21,23,24,27]. The pooled ERRs were 9.83% (95%CI 7.41-12.26%) in the EBL/EDSL group, and 22.32% (95%CI 12.48-32.16%) in the EC group. The test for subgroup differences showed that ERR was significantly lower in the endoscopic ligation group compared to clipping (P=0.02) (Fig. 3). No publication bias was detected (Supplementary Fig. 2).
Figure 3 Early rebleeding rate per modality of endoscopic treatment
SE, standard error; CI, confidence interval
A subgroup analysis of 5 studies was performed, comparing direct vs. indirect clipping [13,16,17,20,23]. A total of 21 of 226 patients treated with direct clipping experienced early rebleeding, vs. 47 of 272 patients treated with indirect clipping. The pooled ERRs were 12.04% (95%CI 3.06-21.02%) vs. 27.74% (95%CI 18.34-37.14%) in the direct and indirect clipping groups, respectively. This difference was statistically significant (P=0.02; Fig. 4). The measured effect favors direct over indirect clipping as a means to reduce early rebleeding episodes (OR 0.45, 95%CI 0.24-0.85; P=0.01), with almost no heterogeneity (I2=5%; Fig. 5). Visual inspection did not reveal any publication bias (Supplementary Fig. 3, 4).
Figure 4 Early rebleeding rate per clipping type
SE, standard error; CI, confidence interval
Figure 5 Probability of early rebleeding according to clipping type
SE, standard error; CI, confidence interval
Discussion
In this systematic review and meta-analysis, we evaluated the ERR of definite CDB, both overall and according to the different endoscopic techniques used to achieve hemostasis. Analysis of data from 1273 patients with definite CDB in 16 individual studies showed an overall ERR of 14.73%, regardless of the endoscopic modality used for treatment. Moreover, our results showed a statistically significant advantage of EBL/EDSL over EC in terms of ERR. A subgroup analysis of the EC category (direct vs. indirect clipping) showed significantly lower ERRs for the direct clipping group, suggesting that indirect clipping might be contributing to the higher ERRs in the EC group compared to EBL/EDSL.
According to existing data in the literature, the different endoscopic techniques discussed above have both strengths and limitations. EBL and EDSL are the primary endoscopic ligation techniques studied for achieving hemostasis in CDB. Both methods are comparable as regards their technique for obliteration of the underlying bleeding vessel by mechanical compression. EBL seems to be an effective technique to treat CDB, with a successful hemostasis rate of 99% and relatively low ERRs of 9% reported in the literature, comparable to the results found in our analysis (9.83%) [28]. However, the need for scope re-insertion makes this technique more time-consuming, making EBL a less attractive choice of therapy, particularly for right-sided CDB, or in elderly patients with comorbidities [3]. Moreover, with an O-ring attached to the endoscope tip, the field of view is narrowed, and finding the binding site is considered more difficult with EBL compared to other modalities [15].
Simple to execute, EDSL has the advantage of not needing a ligation device or re-insertion of the scope. Besides, the transparent hood used in EDSL keeps the field of view relatively wide [15]. However, EDSL remains a recent technique, insufficiently studied for the treatment of CDB. In this systematic review, only 2 studies used EDSL [12,15], compared to 8 studies using EBL as a hemostatic technique [13,15,20-23,25,26].
EBL and EDSL present similar efficacy in achieving hemostasis, as well as comparable ERRs at 30 days [15]. For the reasons mentioned above, we decided to combine the 2 techniques for the subgroup analysis. Further studies investigating EDSL in the treatment of CDB are needed to support the existing data in the literature.
On the other hand, EC is a commonly used treatment modality for CDB, given its simplicity and low invasiveness, providing a high technical success rate of 96% [28]. However, hemostasis may be difficult to achieve, particularly in patients with active bleeding or small diverticular orifices [28]. Clipping is largely classified into direct clipping, in which the culprit bleeding vessel is clipped directly, and indirect clipping, where the openings of the diverticula are closed. Inconsistent data are found in the literature comparing the ERRs of direct and indirect clipping. More specifically, Kobayashi et al and Nagata et al found no significant difference in the ERRs between the 2 methods [13,29], whereas Kishino et al showed a significantly lower ERR associated with direct clipping [10,20]. Our results align with the latter publications, showing significantly lower ERR with direct clipping compared to indirect clipping.
Although the larger over-the-scope-clip might be effective as a hemostatic method for CDB, large cohorts comparing it to the existing techniques are lacking [19]. Furthermore, as with EBL, the need for reinsertion leads to a longer examination duration, with the suction cap narrowing the field of view and making it more challenging to identify the bleeding diverticulum [19]. For the purposes of subgroup analysis, we opted to exclude the only study using the over-the-scope-clip for the treatment of CDB [19].
Right-sided diverticular disease (RSD) in Western countries is likely to be underestimated, with recent studies from Italy and France reporting a prevalence of RSD reaching 35% [30]. According to the literature, RSD increases the risk of CDB significantly, with more than two thirds of diverticular bleeding occurring proximal to the splenic flexure [31,32]. This has been attributed to the wider necks and domes of the right-sided diverticula, leaving a greater length of the vasa recta exposed to injury [32]. In our analysis, including predominantly Japanese patients, the culprit diverticulum responsible for the CDB was identified on the right side of the colon in 68% of the patients.
The strength of our analysis is the guarantee of reproducibility by using a predefined registered protocol. Although recently published large multicenter cohort studies [10,28,33] comparing the ERRs among the different endoscopic modalities were not included in our analysis because of overlapping cohorts, we evaluated data from 16 articles, including 1273 patients endoscopically treated for CDB, making it the largest systematic review and meta-analysis to date. In addition, previously published systematic reviews did not compare ERR according to clipping type.
We acknowledge some limitations in our study. High levels of heterogeneity were present among the different included studies. This may be attributed to the different sample sizes, population demographics, study designs and follow-up protocols used. Moreover, the included studies (except 1) were mostly from Japan, creating a sampling bias for the Asian population, and limiting the generalizability of the results. Furthermore, EBL and EDSL were not analyzed separately.
To conclude, results from our analysis favor the superiority of EBL/EDSL and direct clipping over indirect clipping in the endoscopic management of CDB, since these modalities were associated with significantly lower rates of early rebleeding. It needs to be determined whether these data can be extrapolated to right-sided diverticular bleeding in Western countries.
What is already known:
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Most colonic diverticular bleeding (CDB) cases resolve spontaneously; some require intervention to achieve hemostasis
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Endoscopic treatment is an effective first-line treatment for CDB, with fewer complications than transarterial embolization or surgery
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In the absence of randomized controlled trials, there are inconsistent data regarding which endoscopic modality achieves the lowest early rebleeding rate (ERR)
What the new findings are:
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The overall pooled ERR after endoscopic treatment for CDB is 14.73%
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Endoscopic ligation techniques have significantly lower ERRs compared to endoscopic clipping (9.83% vs. 22.32%)
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Compared to direct clipping, indirect clipping shows a 55% higher risk of ERR, implying the need to favor direct over indirect clipping when possible
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