Endoscopic dilation of small-intestine strictures in Crohn’s disease by balloon-assisted enteroscopy: a systematic review and meta-analysis

Vishali Moonda, Vikram Jeet Singh Gilla, Sheza Malikb, Ameya Kasturec, Sandesh Parajulid, Suha Sonie, Saurabh Chandanf, Arkady Broderg, Babu P. Mohanh, Douglas Adleri

Saint Peter’s University Hospital/Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA; Rochester General Hospital, Rochester, New York, USA; Shree Bhausaheb Hire Government Medical College, Dhule, Maharashtra, India; Reading Hospital, PA, USA; University of Texas, Houston - School of Public Health, Houston, Texas, USA; Creighton University School of Medicine, Omaha, USA; Saint Peter’s University Hospital/Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA; Orlando Gastroenterology PA, USA; Center for Advanced Therapeutic Endoscopy, Centura Health, Porter Adventist Hospital, Denver, CO, USA

aDepartment of Internal Medicine, Saint Peter’s University Hospital/Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA (Vishali Moond, Vikram Jeet Singh Gill); bDepartment of Internal Medicine, Rochester General Hospital, Rochester, New York, USA (Sheza Malik); cShree Bhausaheb Hire Government Medical College, Dhule, Maharashtra, India (Ameya Kasture); dDepartment of Internal Medicine, Reading Hospital, PA, USA (Sandesh Parajuli); eUniversity of Texas, Houston - School of Public Health, Houston, Texas, USA (Suha Soni); fDivision of Gastroenterology and Hepatology, Creighton University School of Medicine, Omaha, USA (Saurabh Chandan); gDepartment of Gastroenterology, Saint Peter’s University Hospital/Robert Wood Johnson Medical School, New Brunswick, New Jersey, USA (Arkady Broder); hOrlando Gastroenterology PA, Orlando, USA (Babu P. Mohan); iDirector, Center for Advanced Therapeutic Endoscopy, Centura Health, Porter Adventist Hospital, Denver, CO, USA (Douglas Adler)

Correspondence to: Douglas G. Adler, MD, FACG, FAGA, FASGE, Director, Center for Advanced Therapeutic Endoscopy, Centura Health, Porter Adventist Hospital, Denver, CO, USA, e-mail: dougraham2001@gmail.com
Received 4 Junw 2024; accepted 31 July 2024; published online 22 October 2024
DOI: https://doi.org/10.20524/aog.2024.0920
© 2024 Hellenic Society of Gastroenterology

Abstract

Background Balloon-assisted enteroscopy (BAE) (both single- and double-balloon enteroscopy) has garnered attention in the treatment of small intestine strictures in patients with Crohn’s disease (CD). This study aimed to evaluate the pooled clinical outcomes of BAE-mediated endoscopic dilation of small intestine strictures in patients with CD.

Methods We searched multiple databases for articles reporting outcomes following BAE for small intestinal strictures in patients with CD. Outcomes studied were pooled technical success, clinical success and adverse events. Standard meta-analysis methods were employed using the random-effects model, and heterogeneity was studied using I2 statistics.

Results We analyzed 26 studies, 9 prospective and 17 retrospective, involving 1570 patients. The pooled technical success rate of double-balloon enteroscopy was 87.6% (95% confidence interval [CI] 82.1-91.5; I2=53%) and the pooled therapeutic success rate was 69.7% (95%CI 61.6-76.7; I2=71%). The pooled major complications per procedure were 5.5% (95%CI 3.5-8.4; I2=57%); the risk of bleeding was 2.5% (95%CI 1.4-4.2; I2=28%), and the risk of perforation was 2.7% (95%CI 1.6-4.5; I2=3%). The pooled rate of recurrence after the first dilation was 42.3% (95%CI 16.9-72.5; I2=59%), and the rate of repeat endoscopic balloon dilation was 23.9% (95%CI 14.1%-37.5%; I2=85%), while the pooled rate of repeat surgery was 25.3% (95%CI 11.8%-46.0%; I2=44%].

Conclusion BAE is a good first line approach for patients with CD-induced strictures in an attempt to treat symptoms and potentially avoid surgery.

Keywords Crohn’s disease, endoscopic dilation, balloon-assisted enteroscopy, stricture

Ann Gastroenterol 2024; 37 (6): 682-694

Introduction

Crohn’s disease (CD) is a type of inflammatory bowel disease (IBD) characterized by sporadic areas of transmural inflammation within the gastrointestinal tract; it has an incidence of 3-20.2 per 100,000 person-years in North America [1,2]. According to the Montreal classification, CD can be divided into: (1) non-stricturing, non-penetrating disease; (2) penetrating; and (3) stricturing [3]. Throughout their illness, individuals with CD may exhibit 1 or more of these disease phenotypes; they frequently go from an inflammatory stage to a stricturing or penetrating stage [4], while approximately 20-40% of CD patients develop stricturing disease within 10 years of disease diagnosis [5-7].

The most common area for stricture development is the ileocecal region, accounting for up to half of cases, which can be primary or anastomotic [5]. The treatment of CD strictures of the small bowel is challenging [8-10]. Medical treatment modalities are being used; however, the CREOLE trial demonstrated that nearly 40% of patients with symptomatic stenoses required either endoscopic balloon dilation (EBD) or surgery [11]. Surgical therapy includes bowel resection and strictureplasty, whereas endoscopic therapies include EBD and endoscopic stricturotomy. Given the high histological and clinical recurrence rates and complications associated with surgery, EBD has emerged as a valuable adjunct and alternative to surgery [8,10-12].

EBD is included in the current guideline recommendations for treating ileal CD strictures [11,13]. Most studies in the existing literature have assessed EBD for terminal ileal and ileocolic anastomotic strictures, which are reachable via standard colonoscopy; however, little is known about EBD for small bowel strictures, which can only be reached by balloon-assisted enteroscopy (BAE) [8,10,13,14].

Recently, various reports on EBD for small bowel strictures using BAE have emerged [15-18]. However, all of these reports have involved small cohorts, and the long-term efficacy was not sufficiently evaluated. Moreover, there is a need to update the adverse outcomes that are associated with these procedures [16,19-42]. The current literature reports a variety of clinical outcomes and complications in this patient cohort. This study aimed to evaluate the pooled clinical outcomes of BAE-mediated endoscopic dilation of small intestine strictures in patients with CD.

Materials and methods

Search strategy

We conducted a comprehensive search of several databases and conference proceedings, including PubMed, EMBASE, and Web of Science databases (earliest inception to December 2023). An experienced medical librarian using inputs from the study authors helped with the literature search to identify studies reporting BAE. The detailed literature search strategy is provided in Appendix A. Two authors (VM, VJSG) independently reviewed the titles and abstracts of studies identified in the primary search and excluded studies that did not address the research question, based on pre-specified exclusion and inclusion criteria. The full text of the remaining articles was reviewed to determine whether it contained relevant information. Any discrepancy in article selection was resolved by consensus, and in discussion with a co-author (BPM). The bibliographic section of the selected articles, as well as the systematic and narrative articles on the topic, were manually searched for additional relevant articles.

We adhered to the Preferred Reporting items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and Meta-analysis Of Observational Studies in Epidemiology (MOOSE) checklist (checklists provided in supplementary materials: Appendices B and C, respectively) [44,45].

Study selection

In this meta-analysis, we included studies that evaluated patients with CD strictures endoscopically treated by BAE, irrespective of inpatient/outpatient setting and geography, as long as they provided data needed for the analysis. Eligible studies enrolled adult patients (age >18 years) with a confirmed diagnosis of CD, strictures of the small intestine (including jejunum and ileum) associated with CD, dilated via BAE using through-the-scope EBD. The following were our exclusion criteria: (1) studies presented as conference abstracts; (2) studies in the pediatric population (age <18 years); (3) studies not published in the English language; (4) case reports and small case series with less than 8 patients per study; and (5) the dilated stricture was located in a non-small-bowel location. In cases of multiple publications from the same cohort and/or overlapping cohorts, data from the most recent and/or most appropriate comprehensive report were included.

Data abstraction and quality assessment

Data on study-related outcomes in the individual studies were abstracted onto a standardized form by at least 2 authors (VM, VJSG), while 2 authors (SP, AK) did the quality scoring independently. The Newcastle-Ottawa scale for cohort studies was used to assess the quality of studies [46]. This quality score consists of 8 questions, the details of which are provided in Supplementary Table 1.

Outcomes assessed

The primary analysis of this study focused on calculating the pooled rate of technical success, clinical success, adverse events, rates of repeat dilation, rates of recurrence of strictures, and surgery required during the follow up with BAE. Pooled rates were calculated for commonly encountered adverse event subcategories with BAE: namely, perforation, bleeding, small bowel obstruction (SBO), localized peritonitis, pancreatitis, and hyperamylasemia associated with the procedure. Additionally, when possible, the adverse events were categorized based on the American Society for Gastrointestinal Endoscopy (ASGE) lexicon and pooled rates were determined for mild, moderate, severe, and fatal adverse events [47].

Statistical analysis

We used meta-analysis techniques to calculate the pooled estimates in each case, following the methods suggested by DerSimonian and Laird [48] and using the random-effects model. When the incidence of an outcome was zero in a study, a continuity correction of 0.5 was added to the number of incident cases before statistical analysis [49]. We assessed heterogeneity between study-specific estimates using the Cochran Q statistical test for heterogeneity, the 95% prediction interval (PI), which deals with the dispersion of the effects, and the I2 statistics [50, 51], in which values of <30%, 30-60%, 61-75%, and >75% are suggestive of low, moderate, substantial, and considerable heterogeneity, respectively [52]. Publication bias was ascertained, qualitatively, by visual inspection of the funnel plot, and quantitatively, by the Egger test. When publication bias was present, further statistics using the fail-Safe N and Duval and Tweedie’s “Trim and Fill” tests were used to ascertain the impact of the bias [53]. Three levels of impact were reported based on the concordance between the reported results and the actual estimate if there was no bias. The impact was reported as minimal if both versions were estimated to be the same, modest if the effect size changed substantially but the final finding would remain the same, and severe if the basic final conclusion of the analysis was threatened by the bias [54]. All analyses were performed using Comprehensive Meta-Analysis (CMA) software, version 3 (BioStat, Englewood, NJ).

Results

Search results and population characteristics

From a total of 2246 citations identified from databases (PubMed, EMBASE, Web of Science), 1996 records were screened after the removal of 250 duplicate records. Of these, 516 reports were assessed for eligibility. Reports were excluded for the following reasons: review articles and editorials (n=318), case reports and case series (n=54), studies not exclusive to Crohn’s disease (n=66), possible cohort overlaps (n=15), studies not published as full manuscripts (n=19), and studies that did not meet the inclusion criteria (n=18). Therefore, a total of 26 BAE studies (with a total of 1576 patients) were included in the final analysis [16,19-43]. The schematic diagram of study selection is illustrated in Supplementary Fig. 1.

A total of 26 publications, including 9 prospective studies and 17 retrospective studies, were analyzed. Technical success was defined as the ability to successfully reach and dilate the target stricture. Clinical success was defined as the improvement or relief of symptoms of intestinal obstruction. Major adverse events were defined as perforation, bleeding, dilation-related surgery, small bowel obstruction (SBO), localized peritonitis, pancreatitis, and hyperamylasemia associated with the procedure. Secondary outcomes were defined as need for surgery, at the site of the dilated stricture only and not in other parts of the intestine. Detailed definitions, degree of adverse events and reintervention, were defined in accordance with the ASGE report.

Symptom recurrence was only assessed in subjects where clinical efficacy was achieved after endoscopic dilation, and follow-up time was defined as months from initial dilation to time of symptom recurrence; subjects were censored at the time of re-dilation, surgery or last follow-up visit if they had no recurrence of symptoms. For time to surgery, follow-up time was defined as months from the first dilation to time of surgery; patients were censored at the time of last follow-up visit if they did not have surgery. For first re-intervention, follow-up time was defined as the months from the first dilation to either first re-dilation or surgery; patients were censored at the time of last follow-up visit if they did not have a re-intervention.

Continuous outcomes reported as median with minimum and maximum limits, or with 95% confidence interval (CI) or interquartile range (IQR) were converted to mean values using the method suggested by Luo et al, and the corresponding standard deviation (SD) was calculated using the method suggested by Wan et al.

Characteristics and quality of included studies

The meta-analysis included 26 independent cohort studies with a total of 1570 patients [16,19-43], described in Table 1. None of the studies were population-based. All of the included studies reported clear information on the technical success, clinical success and adverse event rates, including the subcategory of the adverse events. None of the studies had patients lost to follow up. Eighteen studies were considered to be of high quality and 8 as medium quality. No studies were considered low quality. Supplementary Table 1 details the study quality assessment.

Table 1 Study and population characteristics

thumblarge

Meta-analysis outcomes

The study population was comprised of 47.7% males with a mean age of 44.7±15.42 years and a mean follow-up duration of 25±14 months. The mean age at diagnosis of CD was 28.85±11 years, and the mean duration of CD was 13.08±2.5 years, with the disease located mainly in the ileal region (37.69%). The median length of the strictures was 1.60±0.25 cm.

The pooled technical success rate of balloon assisted enteroscopy was 87.6% (95%CI 82.1-91.5; I2= 53%) and the pooled therapeutic success rate was 69.7% (95%CI 61.6-76.7; I2= 71%; Table 1, Fig. 1, 2). The pooled rate of major adverse events per procedure was 5.5% (95%CI 3.5-8.4; I2=57%). The risk of bleeding was 2.5% (95%CI 1.4-4.2; I2=28%), while the risk of perforation was 2.7% (95%CI 1.6-4.5; I2=3%). Other overall adverse events, including SBO, localized peritonitis, pancreatitis, and hyperamylasemia associated with the procedure came to 4.2% (95%CI 1.1-1.44; I2=11%). The results are summarized in Table 2 and the corresponding forest plots are illustrated in Supplementary Figs. 2-5. There were no reported deaths with BAE. The adverse events were further categorized according to the ASGE Lexicon criteria: the pooled mild adverse event rate associated with BAE was 2.3% (95%CI 1.5-3.4; I2=0%), the moderate adverse event rate was 1.9% (95%CI 1.2-2.9; I2=0%), and the severe adverse event rate was 2.9% (95%CI 1.8-4.7; I2=0%), while the fatal adverse event rate was 1.2% (95%CI 0.7-2.1; I2=0%) The corresponding forest plots are illustrated in Supplementary Figs. 6-9.

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Figure 1 Forest plot, technical success of balloon-assisted endoscopy

CI, confidence interval

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Figure 2 Forest plot, clinical success of balloon-assisted endoscopy

CI, confidence interval

Table 2 Summary of pooled rates

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The pooled rate of recurrence after the first dilation was 42.3% (95%CI 16.9-72.5; I2=59%). The pooled rate of patients who required repeat endoscopic balloon dilation was 23.9% (95%CI 14.1-37.5%; I2=85%), while the pooled rate of repeat surgery was 25.3% (95%CI 11.8-46.0%; I2=44%). The corresponding forest plots are illustrated in Supplementary Figs. 10-12.

Validation of meta-analysis results

Sensitivity analysis

To assess whether any single study had a dominant effect on the meta-analysis, we excluded 1 study at a time and analyzed the effect on the main summary estimate. In this analysis, no single study significantly affected the outcome or the heterogeneity.

Heterogeneity

We assessed the dispersion of the calculated rates using the PI and I2 percentage values. The PI gives an idea of the range of the dispersion and I2 tells us what proportion of the dispersion is true rather than chance. Despite high I2 values, the pooled rates of mean sessions of treatment, and mean pre- and post-treatment hemoglobin had narrow prediction intervals, suggesting minimal dispersion of effects. We observed moderate heterogeneity in the rates of technical success and major complications (I2=53% and 57%, respectively). Low heterogeneity was noted for bleeding, perforation and other complication rates (I2=28%, 3% and 11%, respectively). However, there was substantial heterogeneity in the clinical success rates (I2=71%). No heterogeneity (I2=0) was noted for ASGE Lexicon mild, moderate, severe and fatal adverse event rates.

Publication bias

On the basis of visual inspection of the funnel plots, as well as quantitative measurement that used the Egger regression test, there was evidence of publication bias. The funnel plot study scatter indicated the possibility of “small study effect” confounding. Further statistics using the fail-Safe N and Duval and Tweedie’s “Trim and Fill” tests revealed the impact of the possible publication bias to be minimal, not changing the calculated estimate or the conclusion of this meta-analysis. The funnel plot is summarized in Supplementary Fig. 13.

Discussion

As there remains a lack of comprehensive reporting of the clinical outcomes and associated complications linked to BAE for small intestine strictures, we performed the first meta-analysis of good-quality studies consisting of the largest comparative cohort of studies to date reporting the overall pooled rates of the outcomes exclusively for BAE. In this meta-analysis of 26 studies involving 1570 patients, we analyzed the pooled technical success and therapeutic success of BAE for CD-related small intestine strictures, which were 87.6% and 69.7% respectively. The overall rate of major adverse events with BAE was found to be 5.5%. The overall low incidence of major adverse events at 5.5%, particularly perforation (2.7%) and bleeding (2.5%), reinforces the procedure’s safety profile.

These findings confirm BAE as a highly effective modality for managing CD-related small intestine strictures. Our analysis shows that BAE for the treatment of CD-related small intestinal strictures can be performed safely, with a clinical success rate of just under 70%. Unlike prior research, where variations in reporting methods were prevalent, our analysis only encompassed studies with clear and consistent data presentation, with 18 of 26 (70%) studies being graded as high-quality [36,55,56].

A recent review performed by Bettenworth et al, which evaluated 18 clinical studies, reported the technical and short-term clinical efficacy of BAE in this same clinical context to be 94.9% and 82.3%, respectively [54]. However, the results of our study showed that both the technical success and the clinical success rates were much lower, which could be attributed to the different sample sizes in the 2 studies. In this same study, it was reported that 48.3% of patients experienced symptom recurrence during follow up, which was relatively higher than in our study, and 38.8% of the patients required re-dilation, which was also higher compared to our study. The overall adverse event rates were similar (5.5% vs. 5.3%).

The rates of mild, moderate, severe and fatal adverse events were reported to be 2.3%, 1.9%, 2.9% and 1.2%, respectively. The calculated pooled rate of adverse events was as follows: perforation 2.7%, bleeding 2.5%, and other complications, including SBO, localized peritonitis, pancreatitis, and hyperamylasemia associated with the procedure, were 4.2%. This is the first study to report these rates in the BAE population via meta-analysis.

The strengths of this analysis are as follows: systematic literature search with well-defined inclusion criteria, carefully excluding redundant studies, the inclusion of all high-quality studies, detailed extraction of adverse events, their subcategories, technical success and clinical success information, rigorous evaluation of study quality, low to moderate heterogeneity, narrow range of prediction intervals, statistics to establish and/or refute the validity of the results of the analysis. Moreover, an absence of patient loss to follow up in the data retrieval process further bolsters the reliability of our conclusions. The findings of this study offer valuable insights into the efficacy and safety of BAE, reinforcing its role as a minimally invasive alternative to surgery for managing CD-related strictures and potentially guiding future clinical practices and research.

Our study had some limitations. There was an inherent heterogeneity between the different studies in our analysis. Our study relied heavily on prospective studies and retrospective studies, without any major randomized control trials. Despite these limitations, our study provides valuable information on the pooled success rates and adverse outcomes associated with BAE.

In conclusion, the technical and clinical success rates of BAE were 87.6% and 69.7%, respectively. The pooled rate of major adverse events was 5.5%. Our findings are particularly relevant in light of the current trend toward less invasive management of CD strictures, where BAE serves as a less invasive alternative to surgical intervention, which carries a higher risk profile and significant morbidity. The non-surgical approach of BAE, with its less intensive post-procedure recovery and preservation of bowel integrity, is a compelling option for patients and clinicians alike.

Summary Box

What is already known:

  • Crohn’s disease (CD) often leads to the formation of strictures in the small intestine, with a significant percentage of patients requiring intervention

  • Balloon-assisted enteroscopy (BAE) has been used for endoscopic balloon dilation of small intestinal strictures in CD, offering a minimally invasive alternative to surgery

  • Previous studies have reported varied success rates and complications associated with BAE, but data on long-term outcomes and safety are limited

What the new findings are:

  • BAE has a high pooled technical success rate of 87.6% and a clinical success rate of 69.7% in the treatment of small bowel strictures in CD

  • The pooled risk of major complications, including perforation and bleeding, is low, with perforation occurring in 2.7% and bleeding in 2.5% of cases

  • The rate of symptom recurrence after initial dilation is 42.3%, with 23.9% of patients requiring repeat dilation and 25.3% ultimately undergoing surgery

  • BAE offers a safe and effective first-line approach for managing small bowel strictures in CD

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Notes

Conflict of Interest: DGA: Consultant for Boston Scientific; all other authors declare no conflicts of interest.