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Effectiveness of eradication therapy for Helicobacter pylori infection in Africa: a systematic review and meta-analysis

Abstract

Background

The effectiveness of Helicobacter pylori (H. pylori) eradication depends on the treatment protocol. This study investigates the H. pylori eradication rate in Africa using the best available evidence from databases.

Methods

Databases were searched and results were pooled together. Heterogeneity between studies was assessed using I2 test statistics. Stata version 13 software was employed to compute the pooled eradication rate. In the subgroup analysis comparison, the finding is considered significant when the confidence intervals did not overlap.

Results

Twenty-two studies from 9 African countries with a total population of 2,163 were included in this study. The pooled eradication rate of H. pylori was 79% (95% CI: 75%-82%), heterogeneity (I2 = 93.02%). In the subgroup analysis by study design, a higher eradication rate was reported from observational studies (85%, 95% CI: 79%-90%), compared to randomized control trials (77%, 95% CI: 73%-82%); by the duration of therapy, higher eradication rate was reported in 10-days regimen (88%, 95% CI: 84%-92%), compared to 7-days regimen (66%, 95% CI: 55%-77%); by country, the highest eradication rate was found in Ethiopia (90%; 95% CI: 87%-93%) and the lowest eradication rate was reported in Ivory Coast (22.3%; 95% CI:15%-29%); by type of H. pylori test, the highest eradication rate was reported when rapid urease test coupled with histology (88%, 95% CI: 77%-96%), and the lowest eradication rate was reported with histology alone (22.3%; 95% CI:15%-29%). Significant heterogeneity was observed with pooled prevalence (I2 = 93.02%, P < 0.000).

Conclusions

In Africa, the first-line therapy showed a variable eradication rate for H. pylori. This study demonstrates the necessity to optimize current H. pylori treatment regimens in each country, taking into account the antibiotic susceptibility. Future RCT studies with standardized regimens are warranted.

Peer Review reports

Background

Helicobacter pylori (H. pylori) is a microaerophilic, Gram-negative, spiral-shaped motile bacterial pathogen that colonizes the gastric mucosa of approximately half of the world’s population. H. pylori infection is associated with gastritis, peptic ulcer, atrophic gastritis, gastric adenocarcinoma, and mucosa-associated lymphoid tissue lymphoma (MALT). The presentation of a range of clinical conditions is primarily determined by bacterial virulence, host genetics, and the individual’s lifestyle [1,2,3,4]. The prevalence of H. pylori infection varies globally, with Africa being the highest infection rate [5]. The bacterium is primarily acquired during early childhood under low socioeconomic conditions and close family contact [6].

According to the Maastricht VI/Florence consensus report 2022, individuals with or without clinical evidence of H. pylori infection are recommended to receive first-line eradication therapy to prevent the development of infection-associated complications, such as gastritis and cancer [7]. Moreover, large-scale eradication of H. pylori in a population reduced the incidence and mortality of gastric cancer [8]. In light of this, guidelines have been developed as a national or regional first-line eradication protocol that consists of different antibiotic combinations, including triple therapies, bismuth-free therapies (sequential, concomitant, or hybrid regimens), and bismuth-based quadruple therapy [9]. The effectiveness of eradication therapy has been assessed based on the pre-protocol analysis and categorized as excellent (≥ 95% success), good (≥ 90% success), borderline acceptable (85–89% success), or unacceptable (< 85% success) [10]. The presence of H. pylori resistance to one or more antimicrobial agents or poor medication adherence increases the likelihood of treatment failure, even with excellent regimens.

H. pylori eradication rate differs in different settings based on the type of regimen employed, duration of therapy, and local antibacterial susceptibility pattern. According to a recent systematic review and meta-analysis, first-line treatment had a 98% global H. pylori eradication rate, with a subcontinental success rate of 98% in Asia, 94% in Africa, 94% in Europe, 93% in South America, and 84% in North America. In this report, five African countries with a total of 7 studies comprising 1021 patients were included, Morocco (n = 3), Egypt (n = 1), Kenya (n = 1), Nigeria (n = 1), and Tunisia (n = 1) [11].

However, there is no pooled eradication rate consisting of observational and randomized controlled trials for H. pylori infection in Africa. However, small-scale studies were reported in different countries in Africa. Therefore, African studies differ in study settings, methodology, and other characteristics. In addition, no systematic review or meta-analysis has been conducted on the eradication rate of H. pylori infection in Africa. Therefore, we have undertaken a systematic review to determine the eradication rate of H. pylori in Africa using previously published articles.

Methods

Databases and search strategy

PubMed, Google Scholar, Hinari, Scopus, and the Directory of Open Access Journals (DOAJ) were searched to identify potential articles on H. pylori eradication in Africa. The search was conducted following PRISMA guidelines and checklists [12], Fig. 1.

Fig. 1
figure 1

PRISMA flow chart of studies selection

Quality assessment

The quality of included studies was assessed by using a revised Cochrane risk-of-bias tool for randomized trials (RoB2) and Risk Of Bias in Non-Randomized Studies-of Interventions (ROBINS-I) (Supplementary files 1 and 2). The authors independently assessed the quality of each study, and a consensus was reached on twenty-two studies conducted in nine African countries.

Data extraction

Data were extracted into a customized Microsoft excel spreadsheet. The characteristics of extracted data in each study include: first author name, year of publication, country of study, study design, number of study participants, characteristics of study participants (naïve or nan-naïve), laboratory methods for H. pylori positivity test, number of H. pylori-positive participants, H. pylori eradication regimen, duration of follow up, laboratory methods for H. pylori eradication confirmation, and number of H. pylori eradicated individuals. In addition, graphs of the summary of the risk of bias were developed using RevMan 5.3 (Cochrane Informatics and Knowledge Management Department, London, UK).

Data analysis

Statistical analyses were conducted using Stata version 13.0 (StataCorp, LP, college station, TX). The eradication rate values were pooled using the metaprop command in Stata. The heterogeneity of the studies was assessed using the I2 statistic, and significance was declared at I2 > 50% and Q-test (p < 0.10). Because of high heterogeneity among the studies, the random-effects model (REM) was used to estimate the pooled proportion and 95% CIs using the DerSimonian and Laird methods. The Freeman-Turkey double arcsine transformation was used to avoid missing proportions near or at 0 and 1 from the meta-analysis. Subgroup analysis was done by study design, country, laboratory tests for H. pylori infection, eradication regimen, type of regimen analysis, characteristics of the study population, follow-up duration, and tests employed to confirm eradication. The presence of publication bias was tested using Egger’s test. Forest plots and tables were constructed to display the individual studies and pooled results.

Publication bias and sensitivity analysis

A funnel plot was drawn to evaluate the potential for publication bias. The funnel plots’ gap suggests potential publication bias. In addition, Egger’s regression asymmetry tests were used to assess publication bias, with p < 0.05 considered to indicate potential publication bias. Finally, sensitivity and leave-one-out analysis were done to evaluate the prime determinant of the pooled eradication rate and to detect the possible causes of heterogeneity between studies.

Results

Characteristics of included studies

Twenty-two studies from nine African countries with a total population of 2,163 met the inclusion criteria of the meta-analysis. These studies were published articles from 1992 to 2020, and the number of articles by country is indicated in Table 1. The detailed characteristics of included studies are presented in Table 2. Among the included studies, 8 were observational, and 14 were randomized control trials (RCT). Except for Abd-Elsalam et al., 2016, all study participants were newly diagnosed cases with gastrointestinal disorder. Twelve studies used multiple tests to detect H. pylori, while 10 employed a single test to declare H. pylori infection. Eighteen studies employed a single test, and 4 studies used multiple tests to prove H. pylori eradication. The H. pylori eradication rates in the qualified studies ranged from 22.3% to 90%.

Table 1 Number of articles included in the study by country
Table 2 Lists and characteristics of included 22 studies

The eradication rate and the retrieved studies varies with time. Trend analysis is done to explore the time effect of the study using a scatter plot as indicated in Fig. 2. The trend analysis shows that from 2000 to 2010 there is no eradication study and no variability observed with time.

Fig. 2
figure 2

Trends in H. pylori eradication rate in Africa

Pooled eradication rate of H. pylori

A total of 2,163 people tested positive for H. pylori in Africa. Of which 1,659 confirmed eradication following first-line eradication therapy in the period under review. Our meta-analysis revealed pooled eradication rate of 79% (95% CI: 75%-82%), I2 = 93.02% (Fig. 3). Moreover, the funnel plot for publication bias supported Egger’s regression (p = 0.672) test, which showed no significant publication bias (Fig. 4).

Fig. 3
figure 3

Forest plots of the pooled eradication rates of Helicobacter pylori infection by first-line standard therapy in Africa from 22 studies

Fig. 4
figure 4

Funnel plot showing absence of publication bias with no small study effects, p = 0.672. Publication bias assessment funnel plot; Egger’s regression test (p = 0.672)

Subgroup eradication rate of H. pylori

Subgroup analyses were conducted by country, study design, type of analysis, study population, duration of therapy, outcome measures and regimen. The pooled data were from nine countries. In addition, more studies were conducted in Egypt, which showed an eradication rate of 82%, and almost all countries showed a similar eradication rate except Ivory Coast (22.3%) (Table 3).

Table 3 The subgroup analysis of included studies by country, study design, type of analysis, study population, duration of therapy, outcome measures and regimen from 22 studies in Africa

Discussions

The 22 studies included in our analysis showed the pooled eradication rate in Africa was estimated to be 79% (95% CI: 75–82). This overall eradication rate is lower than reports from Ethiopia (90%), Nigeria (87%), South Africa (86%), Egypt (82%), Morocco (82%), and higher than reports from Tanzania (69%), Kenya (68%) and Ivory Coast (22.3%). These differences might be attributed to methods employed to diagnose H. pylori, type of eradication regimen and duration of therapy, local H. pylori pretreatment resistance,and drug adherence, as stated by previous reports [35,36,37,38,39].

Trend analysis in H. pylori eradication from the 22 studies showed that presence of few studies in the year between 1990s and 2000. There is no relevant study between the year 2000 and 2010. The trend also showed that more publications coming out since 2011. This trend analysis showed that decrease in H. pylori eradication rate. Similar studies indicated that decreasing trends of eradication rate for H. pylori over the years [40]. On the other hand, H. pylori eradication rate consistent in study conducted for a decade [41]. The decrement in eradication rate could be attributed to increasing resistance due to increased antibiotic exposure.

The eradication rate for H. pylori varies in different regions of the world. The overall success of eradication depends on the choice of eradication regimen, duration of the treatment, and local and regional antibiotic resistance pattern of H. pylori. The World Gastroenterology Organization (WGO), in its 2023 guideline, recommended the minimum acceptable eradication rate greater than 80% on an intention-to-treat basis using PPI-clarithromycin plus amoxicillin in areas where clarithromycin resistance is low or moderate [42]. Determining the national and regional eradication rate is fundamental to establish an appropriate eradication protocol for H. pylori infection. Estimating the effectiveness of H. pylori eradication is difficult since factors like pretreatment antibiotic resistance have a profound effect [43,44,45,46]. Some studies consider distinct H. pylori diagnosis or eradication confirmation tests and employ different eradication regimens and/or duration based on the local guideline on the H. pylori treatment [47,48,49]. In the regional context, H. pylori treatment in Africa largely depends on an empirical approach despite the highest infection rate in the world [50, 51].

In the subgroup analysis by country, the highest eradication rate of 90% was from Ethiopia, and the lowest was 22.3% from Ivory Coast, as shown in Table 3. The eradication rate depends on the sensitivity and specificity of tests that detect H. pylori. The sensitivity and specificity of diagnostic or screening techniques depend on the laboratory techniques employed, personal skill to perform the test, and even the brand of reagents and facility standard. In the study from Ivory Coast, the H. pylori pre-and post-eradication detection was based on histological examination of gastric biopsy, which is less sensitive than conventional techniques such as urease test, anti-H. pylori antibody test, and PCR detection of bacterial genome. This finding is consistent with studies showing that treatment efficacy varies with H. pylori detection techniques [52,53,54,55].

This analysis presented the cumulative eradication rate for Africa and identified factors associated with eradication. In addition, the study included a sub-group analysis of differences in study design, country, treatment regimen, type of analysis, duration of eradication therapy, weeks of outcome measure and tests employed for H. pylori diagnosis and eradication confirmation. Africa contains 54 countries; however, this study has picked up reports only from 9 countries. Moreover, one-third of data are reported from Egypt. The fact might influence the generalization of our findings. Thus, eradication studies in Africa are so rare that more research must be promoted. There are so many regimen subgroups and result could be difficult to comprehend. But the general finding is that there is not significant variability among the regimen subgroups.

The current study included from observational to randomized control trails whereas the previous systematic review and network meta-analysis included only randomized controlled trials [11]. In Africa there is only very few RCT and only 7 articles are included. As a result, paucity of literature landscape in Africa, the current study has included observational study in addition to RCT. This has given a better understanding of eradication rate in Africa than the previous global meta-analysis. The study suffers from heterogeneity and there is no generalizable finding.

Conclusion

In Africa, the first-line therapy showed variable eradication rate for H. pylori. This study demonstrates the need to reassess antibiotic susceptibility in each country and optimize current H. pylori treatment regimens. Antibiotic susceptibility of H. pylori should be investigated in each nation of Africa. Although gastrointestinal disorders and associated H. pylori infections are common problems in Africa, less attention is given to translate the efficiency of eradication and improve the eradication regimen. Future RCT studies with standardized regimens are required.

Availability of data and materials

All data generated or analyzed are included in the result of the manuscript and its supplementary files.

Abbreviations

CI:

Confidence interval

H. pylori :

Helicobacter pylori

OAC:

Omeprazole + Amoxicillin + Clarithromycin

OCM:

Omeprazole + Clarithromycin + Metronidazole

OAM:

Omeprazole + Amoxicillin + Metronidazole

LAC:

Lansoprazole + Amoxicillin + Clarithromycin

PAC:

Pantoprazole + Amoxicillin + Clarithromycin

RAC:

Rabeprazole + Amoxicillin + Clarithromycin

OCN:

Omeprazole + Clarithromycin + Nitazoxacine

OACS:

Omeprazole + Amoxicillin + Clarithromycin + Simvastatin

OLDN:

Omeprazole + Levofloxacin + Doxycycline + Nitazoxanide

DLA:

Dexlansoprazole + Levofloxacin + Amoxicillin

OCT:

Omeprazole + Clarithromycin + Tinidazole

PS:

Prospective study;

RCT:

Randomized control trial

PP:

Per protocol

ITT:

Intention to treat

FAT:

Fecal antigen test

UBT:

Urea breath test

H:

Histology

RUT:

Rapid urease test

C:

Culture

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SF: Conceived and designed the study, analyzed data, and drafted the manuscript. SD: interpret the results and review the manuscript. AG: assess methodological quality and review the manuscript. HI and HY: review the manuscript. SF, SD, AG, HE and SS select and evaluate the quality of studies and extract data. All authors revised, edited, and approved the manuscript.

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Supplementary Information

Additional file 1:

Supplementary file 1. ‘Checklist risk-of-bias assessment for randomized trials (RoB2)’.

Additional file 2:

Supplementary file 2. 'Checklist risk-of-bias in non-randomized studies of intervention (ROBINS-I).'

Additional file 3:

Supplementary file 3. Databases and search strategy.

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Fekadu, S., Engiso, H., Seyfe, S. et al. Effectiveness of eradication therapy for Helicobacter pylori infection in Africa: a systematic review and meta-analysis. BMC Gastroenterol 23, 55 (2023). https://doi.org/10.1186/s12876-023-02707-5

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