https://orcid.org/0000-0002-5272-9122
Abstract
Pharmacists are essential for developing pharmacotherapy plans, conducting clinical assessments, and overseeing drug monitoring. Their interventions help prevent medication errors and adverse drug events and enhance medication safety. This study aimed to systematically review pharmacist-led interventions for managing medication-related issues in patients receiving anti-ulcer treatments. A systematic review and meta-analysis was performed to explore four databases for studies published from 1904 up to June 2024. Nine studies were reviewed, including four retrospective, three case-control, one mixed-method, and one prospective pre-post study involving 34,099 participants. The average age of the patients was 61 years, and 50.23% were male. The study quality was high, with an average score of 6.22/7 on the modified Newcastle-Ottawa scale. All studies involved direct interactions between pharmacists and patients or physicians, and data were primarily collected from hospital electronic records. Pooled analysis demonstrated that pharmacist interventions significantly improved the rational use of anti-ulcer medications (OR: 4.5; 95% CI: 0.97 to 20.80; I2 = 89%, P = 0.05), as reported by studies. Pharmacist interventions have a significant impact on improving rational drug use, reducing costs and treatment duration, and enhancing appropriate medication use. These interventions also positively influenced medication adherence and the correction of irrational drug use.
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Citation: Sapkota B, Pandey B, Sapkota B, Dhakal K, Aryal B (2025) A systematic review and meta-analysis on pharmacist-led interventions for the management of peptic ulcer disease. PLoS ONE 20(3): e0320181. https://doi.org/10.1371/journal.pone.0320181
Editor: Obed Kwabena Offe Amponsah, Kwame Nkrumah University of Science and Technology Faculty of Pharmacy and Pharmaceutical Sciences, GHANA
Received: October 5, 2024; Accepted: February 15, 2025; Published: March 25, 2025
Copyright: © 2025 Sapkota et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interest exist.
Introduction
Peptic ulcer disease (PUD) is characterized by damage to the lining of the gastrointestinal (GI) tract and is primarily caused by gastric acid and pepsin. While it commonly affects the stomach and upper duodenum, it can also affect the lower esophagus, distal duodenum, and jejunum [1]. Patients with stomach ulcers typically experience epigastric discomfort 15-30 minutes after eating, whereas those with duodenal ulcers feel pain 2-3 hours post-meal. All patients with PUD should undergo Helicobacter pylori testing, and endoscopy may be necessary for a definitive diagnosis, especially in cases with symptoms. Most patients respond favorably to a triple therapy regimen involving proton pump inhibitors (PPIs) [2,3]. PUD is a worldwide health concern, with a 5%-10% lifetime risk [4,5]. Successful treatment requires appropriate medication use and oversight by healthcare professionals, including doctors, nurses, and pharmacists.
According to Gary H. Smith’s 1971 pharmacist study has significant importance as a healthcare practitioner in the management of patients with peptic ulcers. Pharmacists can provide individual patient instructions on prescribed prescription usage and collaborate with physicians on drug therapy, including drug selection, potential side effects, and drug interactions [6]. Thus, pharmaceutical intervention care is crucial for disease-treatment procedures. Pharmacists play a recognized role in the selection of pharmacotherapies and in making judgments regarding the assessment of clinical parameters and monitoring of medication [7,8]. Pharmacist interventions are crucial in preventing medication errors (MEs) and adverse drug events (ADEs), thereby improving medication safety. Additionally, their involvement in intensive care units (ICUs) and collaboration with ICU physicians have been shown to lower drug consumption, leading to reduced drug therapy costs, shorter hospital stays, and prevention of inappropriate drug use or ADEs, thereby avoiding associated expenses [9,10].
To date, no systematic study has been published that highlighted the changing role of pharmacists in the management of peptic ulcers. Therefore, this study aimed to thoroughly review and summarize pharmacist interventions to address medication-related issues in patients receiving anti-ulcer treatments. Based on the evidence from this review, healthcare systems may benefit from integrating pharmacists into care teams for peptic ulcer management.
Methods
Protocol and registration
This systematic review was prospectively registered with PROSPERO (registration no. CRD 42024525479). It follows the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [11,12].
Eligibility criteria
Studies were included if they met the following criteria: (a) observational research (e.g., cohort, case-control, cross-sectional, and case series studies) and retrospective studies with clear, extractable data on patient interventions; (b) involved pharmacist-led interventions, either individually or as part of a multidisciplinary team (including medication review, pharmaceutical care, patient education, or counseling); (c) targeted adult patients aged ≥ 18 years; and (d) included patients who were using at least one anti-ulcer medication. All study designs were included in this study.
The exclusion criteria were (a) review articles, non-research letters, editorials, commentaries, animal studies, original research with fewer than 10 samples, abstracts from meeting proceedings, and articles not published in English; (b) studies focusing exclusively on children or pregnant women; (c) studies lacking full-text versions; and (d) articles that were not peer-reviewed or not accepted for publication.
Search strategy and selection criteria
A comprehensive systematic literature search was conducted in PubMed, Medline, Europe PMC, and Google Scholar from March 17, 2024, to June 13, 2024, to gather relevant data published from 1904 through June 2024. These databases were searched using the following search terms: (“Peptic ulcer” OR” Peptic ulcer disease” OR” Gastric ulcer” OR “Duodenal ulcer” OR” Gastritis” OR “ Gastroesophageal reflux disease”) AND (“Pharmaceutical care” OR “ Patient counseling” OR “ Medication errors” OR “Drug interactions “OR “ Medication reviews” OR “ Associated factors”) (S1 File). After the initial search, duplicates were deleted, and two reviewer (BS and BP) separately assessed the titles and abstracts for potentially relevant papers. The complete texts of the relevant papers were checked for eligibility requirements. The reference list of acceptable research and pertinent systematic reviews was also examined to reduce literature omissions.
Data extraction and quality assessment
Two reviewers (BS and BP) independently collected the following information from each included study: first author’s name, country of origin, publication year, study location, type of study, data collection dates, gender, age, number of cases in each group, details of the interventions, and study conclusions. A third reviewer (KD) reviewed the article list and verified the extracted data to ensure the absence of duplicate articles or repeated information.
The modified Newcastle Ottawa Scale (NOS) [8] was used to evaluate the risk of bias in the research [13,14]. NOS assesses study quality based on a total of 7 points. A study receiving all seven points was considered to be of high quality, while fewer points indicated lower quality. For each original study included, the quality assessment was performed independently by two reviewers (BS and BA), and any disagreements were resolved through discussion with additional reviewers.
Statistical analysis
A modified version of the DEPICT tool (version 2) [15] was used to categorize pharmacist interventions. The study findings are displayed in tables and elaborated upon in the results section. To assess the three primary outcomes, a meta-analysis was conducted: the effect of pharmaceutical interventions on the rational use of anti-ulcer drugs, anti-ulcer drug use for Stress Ulcer Prophylaxis (SUP), and therapy duration. When comparable outcome data from at least two studies were available, the information was aggregated. Owing to anticipated clinical and methodological heterogeneity, a random-effects model was employed. For categorical variables, results were expressed as odds ratios, whereas standard mean differences (SMD) were used for continuous variables, both with 95% confidence intervals. The I2 statistic was used to evaluate the statistical heterogeneity. Subgroup analyss were performed based on pharmacist activities, rational medication use, and duration of therapy. Review Manager Version 5.4.1 was used for all analyses.
Results
Search results
The study selection process is illustrated in Fig 1. This study followed the PRISMA flow diagram and included four stages: identification, screening, eligibility, and inclusion. The initial database search yielded 5,616 articles; after removing duplicates 5,431 articles remained. The two reviewers evaluated these publications by examining their titles and abstracts. Ultimately, 11 articles were included in the review, although 2 were excluded due to the unavailability of full texts. Finally, nine studies were included in the investigation.
Analysis of included articles
Nine articles were reviewed, including four retrospective studies, three case-control studies, one mixed-method study, and one exploratory prospective pre- and post-study. These studies were conducted in various countries: the United States (n = 3), China (n = 2), Canada (n = 1), Italy (n = 1), France (n = 1), and Iran (n = 1). Eight of the studies were conducted in hospitals, while one was conducted with discharged patients via telephone. The studies collectively involved 34,099 participants, with a median sample size of 502 (range, 58–29,694). The average age of the participants was 61 years and more than half (50.23%) were male. The participants used PPIs, acid suppression treatments (AST), triple or quadruple regimens, and various anti-ulcer medications. The characteristics of the reviewed articles are listed in Table 1. All studies described pharmacist-delivered services and evaluated outcomes related to pharmacist interventions.
Quality of the included articles
The average score of the included articles was 6.22 out of seven, according to the modified NOS (Table 2). All studies were classified as medium- or high-quality studies. Four articles did not meet the criteria for sample representativeness (sample size ≥ 1000 participants). Three articles did not report non-respondents or had a response rate of less than 80%. All other criteria were met by articles. The quality assessment results of this systematic review are presented in Table 2.
Characteristics of pharmacist-delivered services
Table 3 presents an overview of pharmacist-delivered services as outlined in DEPICT version 2 [15,25]. Except for Yailian et al. and Atkins et al., [21] all studies involved direct, one-on-one interactions between pharmacists and patients or physicians throughout the study period. Yailian et al., collected data retrospectively from the French Act IP database, whereas Atkins et al., collected data through telephone communication with discharged patients [17]. The pharmacists’ activities included discontinuing medications, switching therapies, conducting educational sessions on PPI guidelines, and monitoring drug administration. Key tools employed in these interventions included prescription audits, rational drug use software, and PPI review guidelines[16,24].
Outcomes of pharmacist-delivered services
The first significant outcome of pharmacist-delivered services was improvement in the rational use of anti-ulcer drugs. Xin C et al., 96.5%, [16] Chen Q et al., 68.45% [18] and Weng A et al., reported 96. 25% [14] of all interventions detected irrational use of drugs, such as not taking through proper route, proper dose, proper time, and discontinuation with consulting. Pooled estimates of these three studies found that pharmacist involvement improved rational use of anti-ulcer drugs among patients as compared to control (OR: 4.5; 95% CI: 0.97 to 20.80; I2 = 89%, P = 0.05, Fig 2). Subgroup analysis revealed that H. pylori eradication yielded a slightly higher effect (0.18) than non-eradication (0.16). Interventions by pharmacists significantly improved rational medication use, with a greater effect observed in direct patient interventions (risk difference = 9.68) than in lectures (1.49). The age analysis showed higher effects in participants aged < 50 years (7.12) than in those aged > 50 years (1.91) (Table 4).
The size of the data markers represents the weight from the random effects analysis and CI denotes the confidence interval.
The second outcome was a reduction in treatment cost and duration of therapy. Xin C et al., [16] Chen Q et al., [18] and Buckley et al., reported [23] reduction of cost and duration of treatment due to the pharmacist intervention. Pooled estimates of these three studies found that pharmacist involvement decreased the duration of therapy among patients as compared to control (SMD: -0.72; 95% CI: -1.16, -0.29; I2 = 90%, P = 0.001, Fig 3). Subgroup analysis revealed a larger effect in studies within 6 months (SMD = -0.96) and single-center studies (SMD = -0.96). Longer studies (>6 months) and multicenter studies showed moderate effects (SMD = -0.51). Therapy duration was moderately reduced in the general wards (SMD = -0.61), but data for the surgery wards were not estimated (Table 5).
The size of the data markers reflects the weight from the random-effects analysis, and CI denotes the confidence interval.
The third outcome was improvement in the appropriate drug for SUP. Atkins et al., [22] Khalili et al., [21] reported the significant improvement of use of PPI/ acid supression therapy for SUP. Pooled estimates of these two studies found that pharmacist involvement improved rational use of antiulcer drugs among patients as compared to control (OR: 0.71; 95% CI: 0.41 to 1.24; I2 = 0%, P = 0.23, Fig 4). These studies indicated that physicians accepted pharmacist interventions at rates between 79.9% and 89.4% [16,17]. The detailed outcomes of the included studies are presented in Table 6.
The size of the data markers was based on the weight from the random effects analysis, with CI representing the confidence interval.
Discussion
The primary aim of our study was to conduct a systematic review of the literature to examine the nature and extent of research evaluating the effects of pharmacist-provided care in patients taking ulcer medications. Our findings revealed that most pharmacist interventions focused on ensuring rational use for improved patient outcomes. However, the delivery of these interventions varies, including approaches such as medication reviews, implementation of pharmaceutical care plans, adherence to standard guidelines, and the development of evaluation protocols.
Our study underscores the crucial role that pharmacists play in improving the rational use of anti-ulcer drugs. Pharmacist-delivered services significantly enhance appropriate medication use, as reported by Xin et al. (96.5%) and Chen et al. (68.45%) and Weng et al. (96.25%) [16,18,20]. These interventions primarily address irrational drug use, including improper administration routes, incorrect dosages, and discontinuation without consultation. A pooled analysis further supported the positive impact of pharmacist involvement, with an odds ratio of 4.5, demonstrating significant improvement in the intervention group compared with the control group. This aligns with Nassir et al., (2024), in which clinical pharmacists improved the rational use of intravenous paracetamol and reduced hospital costs [26,27]. Despite the wide 95% CI (0.97 to 20.80), likely due to differences in study design, patient populations, or pharmacist interventions [28] and high heterogeneity (I2 = 89%), the findings advocate for standardized approaches in future research. Nonetheless, the pooled analysis provides compelling evidence for the beneficial role of pharmacists in promoting rational anti-ulcer medication use, emphasizing their integration into multidisciplinary healthcare teams to optimize patient outcomes, consistent with Bayraktar et al., 2024 [29].
Our analysis revealed that pharmacist interventions reduced both the cost and duration of anti-ulcer therapies. Studies by Xin C et al., Chen Q et al., and Buckley et al., [16,18,23] confirmed these reductions, illustrating the economic and therapeutic benefits of pharmacist involvement. Similarly, Lankford et al., (2021) found that 547 interventions led to cost avoidance of $1,508,131 [30], and another study indicated that pharmacist interventions reduced hospital stay [31]. Pooled estimates showed a significant impact with a standardized mean difference of -0.72 in therapy duration compared to controls, and a 95% CI of -1.16 to -0.29 (P = 0.001) [32]. Despite high heterogeneity (I2 = 90%), likely due to differences in healthcare settings, methods, or patient populations [28], the consistent reduction in therapy duration and costs across studies supports the integration of pharmacists into healthcare teams to optimize resource use and enhance cost-effectiveness of anti-ulcer treatment protocols [31].
The third outcome of our analysis examined the improvement in the appropriate use of drugs for SUP, especially PPIs and other acid-suppressive therapies. Studies by Atkins et al,. and Khalili et al,. [21,22] reported significant enhancements in rational drug use following pharmacist interventions. This underscores the critical role of pharmacists in optimizing anti-ulcer drug selection and usage for SUP based on clinical guidelines. The pooled analysis of these studies showed an odds ratio of 0.71, indicating a positive trend towards improved rational drug use with pharmacist involvement compared to the control group. However, the CI of 0.41 to 1.24 shows no statistical significance (P = 0.23), and the wide range suggests some uncertainty in the effect size. Low heterogeneity (I2 = 0%) indicated consistency across studies. Despite the lack of statistical significance, the consistent improvement implies that pharmacist interventions may still promote more appropriate SUP therapy [28]. Further large-scale studies are needed to confirm these findings and clarify the role of pharmacists in enhancing the rational use of anti-ulcer medications for SUP. These results highlight the potential value of integrating pharmacists into health care teams to improve treatment decisions and reduce inappropriate acid-suppressive therapy use.
Physicians’ acceptance of pharmacist interventions is essential for successful medication management. Two studies in our review showed high acceptance rates of 79.9%–89.4% for pharmacist recommendations, highlighting the collaborative potential in patient care optimization, especially in anti-ulcer therapies. Zaal et al., (2020) similarly reported a 71.2% acceptance rate by physicians for pharmacist interventions [28]. These high rates indicate that physicians value pharmacists’ expertise in addressing medication-related issues, such as drug selection, dosing, and adherence to guidelines. Collaboration is crucial for enhancing patient outcomes by leveraging the complementary skills of healthcare providers. These findings emphasize the need for a multidisciplinary approach in healthcare, integrating pharmacists in medication management, particularly in complex areas, such as peptic ulcer disease [29,30]. Continued collaboration between pharmacists and physicians is vital to improve medication use and patient safety [31].
Strengths and limitations
The study’s rigorous methodology, following the PRISMA guidelines and comprehensive assessment of pharmacist-led interventions for peptic ulcer disease provide valuable insights into their impact on medication use and patient outcomes, while the inclusion of diverse interventions strengthens the findings. This review had several limitations that may affect its applicability and validity. The exclusion of non-English studies potentially introduces bias and reduces generalizability. Heterogeneity is likely increased by variations in study designs, small sample sizes, and diversity in pharmacist interventions. The predominance of observational studies, which are susceptible to selection bias and confounding factors, could also impact the overall reliability of the findings.
Conclusion
This review highlights the significant impact of pharmacist interventions in the management of anti-ulcer therapies, particularly in improving rational drug use, reducing treatment costs and duration, and enhancing appropriate medication use for SUP. Pooled analysis of studies demonstrated that pharmacist involvement resulted in better medication adherence and corrected irrational drug use, with positive trends in therapy duration and cost reduction. Overall, these findings advocate for a more prominent role for pharmacists in peptic ulcer management as their interventions improve clinical outcomes, optimize resource use, and foster a collaborative approach in healthcare settings. Further research using standardized methodologies could strengthen the evidence for these benefits.
Supporting information
S3 File. List of all excluded study with explanation.
https://doi.org/10.1371/journal.pone.0320181.s003
(XLSX)
S4 File. List of all included study with explanation.
https://doi.org/10.1371/journal.pone.0320181.s004
(XLSX)
Acknowledgments
We would like to acknowledge the Madan Bhandari Academy of Health Sciences, Hetauda, Nepal, for supporting us in conducting this study.
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