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Prevalence of Helicobacter pylori infection and effectiveness of first-line triple eradication therapy among dyspeptic patients at hospitals in Hawassa City, Ethiopia: a cross-sectional follow-up study

Gut Pathogens volume 16, Article number: 23 (2024) Cite this article

Abstract

Background

Dyspepsia is a common gastrointestinal illness sometimes associated with Helicobacter pylori (H. pylori) infection. Screening and eradicating the bacterium reduces the risk of infection-related complications. The aim of this study was to determine the magnitude of H. pylori infection among dyspeptic patients and the effectiveness of triple eradication therapy at hospitals in Hawassa city, Ethiopia.

Results

The prevalence of H. pylori infection was 48.5%. The H. pylori eradication rate using first-line triple therapy was 83.8%. Eradication therapy failure is associated with previous exposure compared to no exposure (AOR: 4.8, 95% CI: 1.37–10.97), a regimen for 10-days compared to 14-days (AOR: 4.05, 95% CI: 1.42–11.55), and self-reported side effects compared to no report (AOR: 2.5, 95% CI: 1.12–5.97). Based on Morisky-eight scale 230 (79.0%) patients were adherent to their triple therapy. Participants with no reports of adverse effects showed increased odds of adherence to triple therapy compared to those who had reports (AOR = 2.45, 95% CI: 1.29–4.62).

Conclusions

This study demonstrated that about half of adult dyspeptic patients were infected with H. pylori, and moderate eradication was observed. Factors such as previous history of eradication therapy, duration of the eradication regimen, and perception of potential adverse effects are associated with eradication rate and should be considered during the initiation of eradication therapy.

Background

Dyspepsia is a complex disorder with several distinct pathophysiologic mechanisms. 70% of cases of dyspepsia are classified as functional dyspepsia (FD), which is characterized as epigastric discomfort (postprandial fullness, early satiety, and burning) for at least one month without any organic disease evidence discovered during upper endoscopy [1]. The global prevalence of FD was 20.8%, and it ranges from 7 to 45% depending on the dyspepsia definition used, geographical location, environmental risk factors, lifestyle, and socioeconomic status [2, 3]. Among patients with functional gastrointestinal disorders, the magnitude of FD was found to be 48.4% according to the Rome III criteria in Ethiopia [4]. Untreated dyspepsia is associated with patients’ poor quality of life, such as anxiety, depression and somatization [5].

Helicobacter pylori (H. pylori) infection is a well-known risk factor for gastrointestinal disorders, including dyspepsia. It has several virulent factors that promote its survival and cause a range of clinical conditions, such as gastritis, peptic ulcer, gastric carcinoma, and mucosa-associated lymphoid tissue (MALT) lymphoma. The three main pathogenic mechanisms associated with H. pylori virulence factors are immune evasion, disease induction and colonization. The virulence factor that causes colonization are adhesins, flagella, urease and the chemotaxis system. H. pylori are able to remain in the human stomach by evading the host immune clearance through proteins that are responsible for immune escape. Vacuolating-cytotoxin A (vacA) and cytotoxin-associated gene A (cagA) are responsible for direct damage of infected gastric epithelial cells and development of clinical diseases [6, 7]. The infection is acquired in early childhood via family close contact or poor sanitary conditions [8]. A recent systematic review and meta-analysis showed that the global H. pylori pooled prevalence ranges from 24% to70%, being the highest in the developing countries for low socioeconomic reasons and underdevelopment [9,10,11,12]. The prevalence of H. pylori infection in Ethiopia was 52.2% [13].

Eradication of H. pylori is the first-line treatment for infected patients with dyspepsia symptoms, as it can reduce symptoms in the majority of them and minimize the risk of serious complications, including the development of gastric cancer [14]. Different regimens have been used as first-line eradication therapy, such as clarithromycin-based triple therapies, bismuth-free therapies or bismuth-based quadruple therapies (BQT) [15, 16]. The choice of treatment protocol depends on the best local practice, antibacterial resistance patterns, cost, and availability of the drugs. The relative effectiveness of varying combinations of eradication regimens is affected by several factors, and the choice of antibiotics should be localized [17]. In general, as a first-line treatment, 14-days concomitant therapy, or 14-days BQT, is recommended in areas of high clarithromycin resistance (≥ 15%), whereas 14-days triple therapy, or 14-days BQT is recommended in areas of low clarithromycin resistance (< 15%) [18]. The success or failure of treatment is usually determined after a month of completion of the regimen using H. pylori detection techniques such as urea breath test, fecal antigen testing (FAT), or biopsy-based testing [19]. The FAT for H. pylori had good performance and was cost-effective for screening as well as confirmation of eradication [20].

The H. pylori drug resistance is increasing globally and has resulted in the failure of both first-line and second-line eradication therapy, which urges local surveillance network to select an appropriate eradication regimen [21]. There are a few studies in Ethiopia regarding H. pylori drug resistance. The trends of resistance against commonly used antimicrobial metronidazole was 5.26% (in 1999), 76% (in 2004), and 91.6% (in 2023); clarithromycin was 0% (in 2004), and 66.7% (in 2023); amoxicillin was 6% (in 2004), and 91.6% (in 2023); tetracycline was 0% (in 2004), and 37.5% (in 2023) [22,23,24]. This condition is significant, especially for the clarithromycin-based triple therapy. The key antibiotic clarithromycin becomes ineffective because of prior exposure to or use of other macrolides for treatment of infections [25]. Based on the status of clarithromycin resistance, regimens are optimized to maximize eradication rate. Moreover, evaluation of the current regimens and implementing evidence-guided eradication therapy improve the overall eradication rate and cure.

Very few studies are available on the effectiveness of H. pylori first-line eradication therapy among dyspeptic patients in Ethiopia. In addition, the recurrence rate of dyspepsia after taking eradication therapy is very common. The present study is significant because it addresses the public health issue on the effectiveness of H. pylori eradication therapy. Given the different regimens used to eradicate H. pylori infection, an assessment of the relative effectiveness of each regimen is critical for optimizing treatments and revision of protocols. The study benefits those patients whose eradication failed using the first-line eradication regimen to seek the second-line eradication regimen. Moreover, this study will contribute to the existing literature by providing factors that may affect H. pylori eradication.

Therefore, the aim of this study was to determine the prevalence of H. pylori infection and the effectiveness of eradication therapy among adult dyspeptic patients visiting gastroenterology outpatient departments in Hospitals in Hawassa city, Ethiopia.

Methods

Sampling, questionnaires, and dyspepsia screening

The study was conducted in Hospitals in Hawassa city. Hawassa is the capital city of the Sidama region of Ethiopia. The study participants were recruited from five hospitals: four government hospitals (Hawassa comprehensive and specialized, Adare general, Motite Fura primary, and Millenium primary), and one private hospital (Abem primary hospital of internal medicine and cardiology unit). Most of the participants were from Hawassa and environs, for improved follow-up. A facility-based cross-sectional follow-up study was conducted among adult (age ≥ 18 years) dyspeptic patients who visited the gastroenterology outpatient departments from February to June 2023. The sample size to determine the prevalence of H. pylori infection among dyspeptic patients was calculated by considering a previous study done in Ethiopia, which was 51.4% [26]. Using the single population proportion and a margin of error of 4%, 600 participants were invited to participate in the study. Out of the 600 study participants, 309 were H. pylori-negative on H. pylori fecal antigen test and excluded from the follow-up. For the follow-up study, a total of 291 H. pylori-positive patients were followed to investigate the effectiveness of eradication therapy and drug adherence based on the previous study [27] and sample size calculation for the cohort study [28]. After getting their full consent, convenience sampling techniques were employed to invite them. The details of the recruitment of the study participants are presented in Fig. 1.

Fig. 1
figure 1

Recruitment of dyspeptic patients and selection of H. pylori-positive participants for follow-up of eradication therapy

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Study subjects were patients with functional dyspepsia who experienced the upper gastrointestinal disorder with the chief complaint of pain or burning in the stomach, bloating, excessive belching, or nausea after a meal and visited the outpatient department (OPD) during the study period. Patient selection and screening were performed by an experienced gastroenterologist or internist at the baseline. Data regarding the sociodemographic and clinical variables were recorded using structured questionnaires.

FAT for H. Pylori infection and eradication confirmation

Stool samples were collected in a sterile plastic container for H. pylori FAT (SD BIOLINE H. pylori Ag, Standard Diagnostics, Inc. Korea). H. pylori-positive participants were given eradication therapy consisting of proton pump inhibitor (PPI)-based triple therapy: omeprazole 40 mg or pantoprazole 40 mg, twice a day for 15 to 30 days; clarithromycin (500 mg); and amoxicillin (1000 mg), each twice a day for 14-days or 10-days. After 4 weeks of completion of the eradication therapy, stool samples were collected and assayed as previously to confirm the success or failure of eradication. Self-reported information was used to estimate the adherence level. Medication adherence was measured by the Morisky Medication Adherence Scale–8 (MMAS-8), a measure of compliance with medication using time, dose, and frequency recommended by the health care provider [29]. A patient who scored seven no answers for the eight MMAS-8 was said to be adherent to triple therapy, while a patient who scored ≥ 2 yes answers for the MMAS-8 was said to be non-adherent to triple therapy.

Statistical analysis

The data were entered, cleaned, and analyzed using SPSS version 25.0 (IBM Cop., Armonk, NY, USA). Descriptive statistics such as percentages, means, and standard deviations were used to describe the data. A Chi-square test was used to assess success-failure differences in H. pylori eradication. Bivariate and multivariable logistic regressions were used as predictors of failure of eradication and adherence rate. A backward stepwise logistic regression model was used during multivariable logistic regression to control confounding effect. The odds ratio with 95% confidence intervals was calculated for each of the independent variables using p-value < 0.05 as the level of significance.

Results

Among 600 adult dyspeptic patients who had clinical signs and symptoms of dyspepsia, 291 were positive for H. pylori FAT giving an overall prevalence of 48.5% (291/600). The 291 H. pylori- positive patients were further consented to for follow-up. Among the 291 consented for the follow-up, 219 were able to came to hospitals to confirm their H. pylori eradication after one month of completion of the eradication therapy, and for the rest of the participants, their H. pylori status was confirmed at their home because of their social condition. The mean age of study subjects was 33.6 (± 12.04) years (range = 18–78 years), with most (38.8%) being between 25 and 34 years of age. Most of the participants were females (65.5%), resulting an overall female-to-male ratio of 1.8:1. Most of the participants live in Hawassa, and the remaining came from the nearby administrative districts. Tables 1 and 2 show the general physical and sociodemographic characteristics of the study participants.

Table 1 General physical characteristics of dyspeptic patients attending selected hospitals in Hawassa city administration, February–June, 2023
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Table 2 Sociodemographic characteristics of dyspeptic patients attending selected hospitals in Hawassa city administration, February–June, 2023
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Medical information and H. pylori prevalence

The study participants were assessed for their medical conditions and tested for H. pylori status and eradication rate after completion of the eradication regimen. Among the subjects, 54.3% had a previous history of gastritis, 12.7% had a history of H. pylori infection, and 36.5% had a history of other illnesses. The clinical characteristics and associated factors are shown in Table 3.

Table 3 Clinical characteristics of dyspeptic patients attending selected hospitals in Hawassa city administration, February–June, 2023
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H. Pylori eradication and associated factors

Binary and multivariable logistic regression were performed to assess factors that are related to the H. pylori eradication rate among dyspeptic patients. Accordingly, after adjusting all the confounders, the previous history of H. pylori eradication and current eradication regimen used were associated with H. pylori eradication failure. Table 4 shows the binary and multivariable logistic regression of H. pylori eradication among the study participants.

Table 4 Binary and multivariable logistic regression of factors associated with H. pylori eradication in the hospitals in Hawassa city, February–June 2023 (n = 291)
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Adherence rate

Based on MMAS-8, 230 (79.0%) patients were adherent to their triple therapy medications, and 61 (21.0%) were non-adherent, Table 5.

Table 5 Morisky-Medication Adherence Predictor Scale-8 (MMAPS-8)
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Factors associated with adherence to triple therapy

The results of multivariate regression are indicated in Table 6. Except for the presence of self-reported adverse effects, no significant association with adherence was observed in both bivariate and multivariate models. Participants who have no reported adverse effects showed 1.80 times increased odds of adherence (COR = 1.80, 95% CI (1.01, 3.21)) to triple therapy as compared to participants who has reported adverse effects. In the multivariate model, those who have no reports of adverse effects showed 2.45 times (AOR = 2.45, 95% CI (1.29–4.62) increased odds of adherence to triple therapy compared to those who have reports of adverse effects, Table 6.

Table 6 Binary and multivariable logistic regression of factors associated with adherence to H. pylori eradication therapy in the hospitals in Hawassa city, February–June 2023 (n = 291)
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Discussions

The prevalence of H. pylori infection among adult dyspeptic patients in this study was 48.5%. A decrease in prevalence was, of course, not a prefect consistency, what was observed in the most recent study reports is comparable with our findings, 51.4% [26]; 51.1% [30]; 49% [31]; 52.4% [32]; 49.2% [33]. Two of the studies with lower findings, 37.6% [34] and 34% [35] than the current study was published in 2017 and 2023. This inconsistency could be due to geographical variation. The oldest reports (published 20-years ago) showed H. pylori prevalence of 81% [36], far from the prevalence of recent publications. The reasons for decrease rate of H. pylori infection with time may be due to improved socioeconomic and personal hygiene [37, 38]. Several other factors could also be in display, such as improved nutritional quality and medical care overtime.

H. pylori infection results in persistent chronic infection, and the presence of other risk factors can lead to severe gastrointestinal diseases such as gastritis, peptic ulcer, and gastric cancer. Therefore, early screening and eradicating the bacteria decrease infection-associated complications [39]. In this study, the H. pylori eradication rate using standard triple therapy was 83.8% (244/291). This result was lower than the eradication rate reported from Northern Ethiopia, which was 90.3% [27] and higher than the study reported from Central Ethiopia, which was 50.0% [40]. Moreover, our findings are comparable with a recent systematic review on eradication rate of African studies, which was 79.0% [41]. Several factors are associated with failure in the eradication rate, such as eradication regimen used, pre-antibiotic resistance, poor drug compliance, and sociodemographic factors [42,43,44,45]. Overall, this eradication rate is acceptable in areas of low clarithromycin resistance (< 15%), one of the core antibiotics for the treatment of H. pylori. However, there is no local data regarding clarithromycin resistance levels, making it unlikely that this regimen will be continued.

In our study, the odds of eradication failure were four times higher in participants with previous exposure to H. pylori eradication therapy compared with those without exposure. This is supported by similar studies conducted elsewhere showing the importance of considering the patient’s antibiotic history before employing first-line eradication therapy [46,47,48]. Exposure to antibiotics indeed accelerated antimicrobial resistance and, thus, treatment failure.

In multivariate logistic regression, patients receiving an eradication regimen consisting of omeprazole, amoxicillin, and clarithromycin for 10-days had four times more eradication failures than patients receiving the same regimen for 14-days. The effectiveness of eradication depends on the regimen and successful adherence to the treatment protocol. Several studies supported the finding that the 14-days treatment showed better eradication compared to the 10-days regimen [49,50,51,52]. However, another study showed no difference in eradication rate was observed in patients taking a 10-days and 14-days triple eradication regimen [53].

The effectiveness of H. pylori eradication depends not only on choosing the right antibiotic combination, but also on the proper taking of those antibiotics and proper counseling on perceived side effects. In our study, those participants who self-reported fewer or no side effects were two times more likely to experience eradication failure compared with those who had no self-reported adverse effects. Most of the eradication regimens have side effects, and adherence to the regimens during the treatment course is the main factor for success of eradication. The pretreatment consultation with physicians regarding the nature and effect of the antibiotics and follow-up during treatment also play a crucial role, as most patients become reluctant to take their medicine at home [54, 55].

The adherence rate and the eradication rate in this study showed similar values; however, the finding of the current study did not reveal an association. In this study, adherence to triple therapy was associated with reports of adverse effects. Better adherence was observed among those who did not report adverse effects. Adverse effects can compel patients to compromise treatment adherence and even force them to stop medications. In a previous study, 6.6% of patients on triple therapy with adverse events stopped medication [56]. The eradication rate of H. pylori on triple therapy is influenced by adherence in children [57]. The self-report modified Morisky adherence scale was used to assess medication adherence, which tends to overestimate adherence when compared to other methods such as pill counts, prescription claims or biological assays [58]. It also did not assess the outcome of adherence; future researchers are warranted to corroborate the finding.

The virulence factors, particularly the vacA and cagA status of the infecting H. pylori strain, are important for disease development and response to medical interventions such as eradication therapy. However, because of facility limitations in our study, the cagA and vacA statuses were not determined; hence, the samples were appropriately preserved and stored for future studies.

Conclusions

This study demonstrated that about half of adult dyspeptic patients were infected with H. pylori, and this suggests careful consideration of dyspeptic patients for proper management. Our study also demonstrated a moderate H. pylori eradiation rate, 83.8% using first-line eradiation therapy, and this eradication rate is acceptable in areas of low clarithromycin resistance; however, so far, there is no published data in the study area to recommend that this regimen be continued for H. pylori eradication.

Careful assessment of dyspeptic patients regarding their previous history of eradication therapy, which may have resulted in poor eradication or pre-antibiotic exposure, ultimately leads to eradication failure. In addition, the selection of a longer duration over the shorter regimen, coupled with proper consultation during the course of treatment, promotes the rate of eradication.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

BQT:

Bismuth-based quadruple therapies

FD:

Functional dyspepsia

FAT:

Fecal antigen test

H. pylori :

Helicobacter pylori

MMAS-8:

Morisky Medication Adherence Scale-8

OPD:

Outpatient department

PUD:

Peptic ulcer disease

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Acknowledgements

We would like to thank the study participants for their kind cooperation during the follow-up.

Funding

This work was supported by the Hawassa University office of Vice President for Research and Technology Transfer (VPRTT) under the disciplinary research category.

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Authors and Affiliations

  1. School of Laboratory Sciences, College of Medicine and Health Sciences, Hawassa University, P. O. Box 1560, Hawassa, Ethiopia

    Sintayehu Fekadu

  2. Department of Internal Medicine, College of Medicine and Health Sciences, Hawassa University, P. O. Box 1560, Hawassa, Ethiopia

    Seyife Kibru & Sisay Tesfaye

  3. Internal Medicine and Cardiology Unit, Abem Primary Hospital, P. O. Box 1162, Hawassa, Ethiopia

    Tariku Egeno

  4. School of Public Health, College of Medicine and Health Sciences, Hawassa University, P.O. Box 1560, Hawassa, Ethiopia

    Alemu Tamiso

  5. School of Pharmacy, College of Medicine and Health Sciences, Hawassa University, P. O. Box 1560, Hawassa, Ethiopia

    Hizkel Engiso & Serawit Deyno

Authors
  1. Sintayehu Fekadu
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  2. Seyife Kibru
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  3. Sisay Tesfaye
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  4. Tariku Egeno
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  5. Alemu Tamiso
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  6. Hizkel Engiso
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  7. Serawit Deyno
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Contributions

SF conceived and designed the study; SF, SK, ST, TE, AT, HE & SD contributed in patient recruitment and data collection; SF and SD analyzed the data, interpreted and drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sintayehu Fekadu.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was obtained from the Ethics Committee of Hawassa University College of Medicine and Health Sciences, approved by the chair of the ethics committee, Dawit Jember, with a reference number of IRB/072/14. All participants signed written informed consent in the study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Fekadu, S., Kibru, S., Tesfaye, S. et al. Prevalence of Helicobacter pylori infection and effectiveness of first-line triple eradication therapy among dyspeptic patients at hospitals in Hawassa City, Ethiopia: a cross-sectional follow-up study. Gut Pathog 16, 23 (2024). https://doi.org/10.1186/s13099-024-00618-8

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Keywords

Gut Pathogens

ISSN: 1757-4749