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Clarithromycin-resistant Helicobacter pylori in Africa: a systematic review and meta-analysis

Antimicrobial Resistance & Infection Control volume 14, Article number: 31 (2025) Cite this article

Abstract

Background

In 2022, approximately 56.5% of adults and 47.1% of children and adolescents were affected by Helicobacter pylori (H. pylori) infection in Africa, and clarithromycin-resistant H. pylori (CRHp) strains have become global priority pathogens. Therefore, this study aimed to conduct the first comprehensive systematic review and meta-analysis of CRHp in Africa.

Methods

This investigation was conducted according to the guidelines of the Preferred Reporting Items for Systematic reviews and Meta-Analyses (The PRISMA 2020). Literature search of electronic databases (Google Scholar, African Journals Online, ResearchGate, PubMed, Embase, and Scopus) was performed using keywords “clarithromycin”, “Helicobacter pylori”, “African country name”, “mutation in the 23S rRNA”.

Results

Sixty-five studies involving 5,313 H. pylori strains isolated over 26 years (1997–2022) from 23 African countries were included in this study. The samples from which CRHp was isolated included gastric biopsy (60/63; 95%), and stool (4/63; 6%). The pooled prevalence of CRHp in Africa was 27% (95% CI: 22, 33). There was a steady trend in the prevalence of CRHp isolated in Africa over the 26 years (R2 = 0.0001, p = 0.92, slope coefficient of -0.05x). Ten types of 23S rRNA mutations (conferring clarithromycin resistance) were identified, and included mainly A2143G (465 H. pylori strains out of 1178 tested) and A2142G (344 H. pylori strains out of 1027).

Conclusion

To enhance the accuracy and validity of surveillance data for H. pylori in Africa, there is an urgent need for implementing standardized microbiological methods for resistance detection. The prevalence of CRHp reported in this study was very similar to the overall global prevalence and there is a need for more representative studies on CRHp in Africa. While waiting for this, the treatment of H. pylori infections must be based on the guidelines of the AHMSG first Lagos consensus.

Introduction

Helicobacter pylori, (H. pylori) is responsible for one of the most common human bacterial infections worldwide [1, 2]. In 2022, Africa had the highest prevalence of H. pylori infection compared to other global regions [2]. The prevalence of H. pylori infection in Africa (56.5% for adults and 47.1% for children and adolescents) may be underestimated because of the scarcity of data on asymptomatic H. pylori carriage in most African countries [2, 3]. H. pylori infections are usually associated with poor sanitation and unclean water supplies [4].

H. pylori is also responsible for approximately 90% of the global burden of non-cardiac gastric cancer [5]. In 2020, the International Agency for Research on Cancer has classified H. pylori as a class 1 carcinogen, with a higher incidence of cancer than the human papillomavirus, hepatitis B virus, and hepatitis C virus [6]. To establish and maintain infections, H. pylori strains use several virulence factors such as adhesins (babA), urease (ure operon), vacuolating cytotoxin (vacA), immunodominant antigen (cagA), and the induced by contact with epithelium (iceA), which are most frequently associated with peptic ulceration and increased production of IL-8 [7, 8].

Advances in medicine have improved the treatment of H. pylori infection. In Africa, first-line therapy combines antibiotics (amoxicillin, clarithromycin) with proton pump inhibitors (PPIs), whereas second-line or salvage therapies (levofloxacin-based triple therapy, sequential non-bismuth quadruple therapy, or bismuth-based quadruple therapy) combine antibiotics (amoxicillin, clarithromycin, nitroimidazole, levofloxacin, and tetracycline) with PPIs and bismuth compounds [3].

The antimicrobial resistance has not spared H. pylori strains, with global resistance rates of 24% for levofloxacin, 34% for clarithromycin, and 55% for metronidazole [9]. Clarithromycin inhibits H. pylori protein synthesis by interacting with the peptidyl transferase ring in the V region of the 23S ribosomal RNA (rRNA) subunit of H. pylori strains. Mutations in the 23S rRNA are responsible for clarithromycin resistance [10,11,12]. The resistance of H. pylori to clarithromycin is associated with a seven-fold risk of treatment failure when using a clarithromycin-based regimen [9]. Therefore, in areas with low clarithromycin resistance (< 15%), the treatment algorithm consists of amoxicillin, clarithromycin, and a PPI, whereas second-line therapeutic regimens are used for areas with clarithromycin resistance > 15% [13].

In 2017, the World Health Organization (WHO) released a global priority list of antibiotic-resistant bacteria, and clarithromycin-resistant H. pylori (CRHp) strains were ranked as high-priority pathogens for which new antibiotics are urgently needed [14]. Therefore, from an epidemiological standpoint, monitoring the spread of CRHp has become a priority for global public health authorities.

The previous pooled prevalences of CRHp determined in Africa should be taken cautiously since the studies were only limited to a few African countries [9, 15]. To address the lack of quality data on CRHp in Africa, this study aimed to conduct the first comprehensive systematic review and meta-analysis of CRHp in Africa.

Methods

This systematic review and meta-analysis was conducted according to the guidelines of the Preferred Reporting Items for Systematic reviews and Meta-Analyses (The PRISMA 2020) [16].

Literature review

A comprehensive literature search of electronic databases (Google Scholar, African Journals Online, ResearchGate, PubMed, Embase, and Scopus) was performed using keywords “clarithromycin”, “Helicobacter pylori”, “Africa”, “African country name”, “mutation in the 23S rRNA”). The database search was conducted from March 23, 2024, to April 30, 2024, and the studies written in French and English were included in this systematic review and meta-analysis.

Eligibility criteria

This systematic review and meta-analysis included original peer-reviewed research articles and theses reporting CRHp in African countries. Studies reporting CRHp using both genotypic and phenotypic methods, were included. After identification, duplicate articles were excluded. Reviews, commentaries, perspectives, and non-peer-reviewed articles, reporting CRHp in Africa were also excluded. Furthermore, peer-reviewed research articles and theses on H. pylori strains isolated from outside Africa were also excluded.

Quality assessment

Two authors performed the article quality assessment using the Joanna Briggs Institute (JBI) Prevalence Critical Appraisal Tool [17]. The results of the article quality assessment are presented in the Additional file 1. The JBI prevalence appraisal tool includes 10 questions for each article to be answered Yes (Y) or No (N). A positive answer (Y) was worth 10%, and the total number of points that could be obtained for an article was 100%. Studies with a score of ≥ 50% were considered of good quality and were included in the analyses (Additional file 1).

Data extraction

For each study included in this systematic review and meta-analysis, the following data were extracted: country, authors and references, sample collection period, study design, sample from which the H. pylori strains were isolated, methods used to assess clarithromycin resistance, total number of H. pylori strains studied, number of CRHp strains, mutations within the 23S rRNA conferring clarithromycin resistance and virulence genes. Two authors conducted the data extraction, and disagreements were resolved by discussion, data cross-checking, and validation.

Data analysis

The pooled prevalences and their p-values, forest plots and their p-values, funnel plot, and meta-regression were obtained using Stata v17.0 with commands such as ‘metaprop’, ‘metafunnel’, ‘metabias’, and ‘meta regress’. The pooled prevalence were presented with a 95% CI, corresponding p-value and forest plot. Funnel plot symmetry and Egger’s test statistics were used to evaluate prevalence publication bias [18, 19]. Microsoft Excel 2016 v2.0, was used to perform the remaining statistical analyses, and draw associated graphs. The p-values obtained using Microsoft Excel were calculated based on the chi-square proportion comparison test. The level of significance for all statistical tests was set at p < 0.05.

Selection of studies

A literature search of public databases (Google Scholar, ResearchGate, African Journals Online, PubMed, Embase, and Scopus), generated 923 studies. Subsequently, 426, 327, 19, 46, and 40 studies were excluded for duplication, data outside Africa, other types of studies (reviews, commentaries, non-peer-reviewed articles and perspective articles), studies reporting bacteria other than H. pylori, and studies without any data on clarithromycin resistance, respectively. The remaining 65 studies (64 research articles and one thesis) were included in this systematic review and meta-analysis (Fig. 1). Table 1 shows the data collected from the 65 studies.

Fig. 1
figure 1

PRISMA search flow diagram

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Table 1 Characteristics of the 65 studies included in this study
Full size table

Results

Characteristics of included studies

The article quality assessment using the JBI prevalence critical appraisal tool provided an overall risk of bias assessment score of 89.5% (Additional file 1). A total of 5,313 H. pylori strains were studied across 65 studies and were isolated over 26 years (1997–2022) from 23 African countries (Fig. 2). Thirty-two studies mentioned the type of study, including 18 (56%) cross-sectional studies, 10 (31%) prospective studies, three (9%) observational studies, and one (3%) case-control study. The number of studies on CRHp per year has increased over the years in Africa (Fig. S1).

Fig. 2
figure 2

Map of Africa showing the number of study on CRHp in Africa

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Samples carrying CRHp

Sixty-three studies (97%) specified the samples from which CRHp was isolated, including gastric biopsy (60/63; 95%), and stool (4/63; 6%).

Methods used to assess clarithromycin resistance

Sixty-two studies (95%) specified the methods used to assess clarithromycin resistance. The phenotypic methods (48/62; 77%), included the Kirby-Bauer disc diffusion method (22/62; 36%), E-test (20/62; 32%), and agar dilution method (6/62; 10%). Genotypic methods (38/62; 61%), included real-time polymerase chain reaction (RT-PCR) (17/62; 27%), polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) (9/62; 15%), end-point PCR (5/62; 8%), DNA sequencing (5/62; 8%), and the Genotype Helicobacter DR Kit (2/62; 3%).

Pooled prevalence of CRHp

A total of 5,313 H. pylori strains were studied, of which 1,288 were resistant to clarithromycin. The pooled prevalence of CRHp in Africa was 27% (95% CI: 22, 33). A large discrepancy was reported among the prevalences of CRHp, ranging from 0% (95% CI: 0, 2) to 100% (95% CI: 89, 100), (I2 = 95.3%, p < 0.001) (Fig. S2).

Publication bias

The presence of publication bias on the studies of CRHp in Africa was reported with a bias coefficient of 2.18 (Fig. S3).

Evolution of the prevalence of CRHp over time

Meta-regression of the prevalences of CRHp isolated in Africa over the 26 years did not reveal any significant variation (R2 = 0.0001, p = 0.92), with an insignificant downward trend (slope coefficient of -0.05x).

Mutations within the 23S rRNA conferring clarithromycin resistance

Thirty studies (46%) identified ten types of mutations within the 23S rRNA (Table S1). A2143G (carried by 465 H. pylori strains out of 1178 tested) and A2142G (344 H. pylori strains out of 1027) were by far the most reported 23S rRNA mutations in Africa (p < 0.0001) (Table S1).

There was no difference between the prevalence of A2143G and A2142G in Northern Africa (p = 0.17) and southern Africa (p = 0.08). Nevertheless, the A2143G mutation was significantly more prevalent in Eastern Africa and Central Africa (Table 2). Several studies have reported cases of multiple 23S rRNA mutations in H. pylori strains.

Table 2 Distribution of A2143G and A2142G mutations in African regions
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Virulence genes

Eleven articles (17%) searched and reported H. pylori virulence genes. cagA (10/11; 91%) and vacA (6/11; 55%) were the most reported, followed by iceA1 (1/11; 9%), ureC (1/11; 9%) and babA2 (1/11; 9%).

Discussion

In the reviewed studies, the agar dilution method, considered the gold standard for antimicrobial susceptibility testing (AST) for H. pylori, was used in only 6 of the 65 studies included. In contrast, the Kirby-Bauer disc diffusion method, which is regarded as an unreliable AST method for detecting CRHp, remains the most commonly used method on the African continent (in 22 studies out of 65). This underscores the urgent need for implementing standardized microbiological methods for resistance detection to enhance the accuracy and validity of surveillance data.

The overall pooled prevalence of CRHp reported in this study was 27% (95% CI: 22, 33), and was very similar to the global pooled prevalence of CRHp from 248 articles in 2023 [27.53% (95% CI: 25.41, 29.69)] [20]. The pooled prevalence of CRHp observed in Africa in this systematic review and meta-analysis was slightly lower than that reported for the Asian continent (29.57% and 35.97% in 2023) [85, 86]. However, the CRHp prevalence in Africa was slightly higher than that (22%) reported in the Asia-Pacific region [21], and was the same as that (27%) reported for the Southern Asian region in 2023 [22]. Concerning Europe, the African CRHp pooled prevalence was quite similar to those reported for the European continent, 25% in 2021 [23] and 26.25% in 2023 [20]. The pooled prevalence of CRHp reported in this study was higher than that (23.86%) observed in the American continent in 2023 [20], and was significantly higher than the 10.3% [24] observed for Oceania in 2020 and the 7.02% reported for North America in 2023 [25].

In this study, we reported a steady trend (R2 = 0.0001; p = 0.92) for the prevalence of CRHp in Africa for strains isolated from 1997 to 2022, with a slightly negative slope coefficient of -0.05x. This is contrary to most of the trends observed worldwide. An increase from 24.28% in 2010–2017 to 32.14% in 2018–2021 was reported in a global study that included 248 articles in 2023 [20]. In addition, increases in CRHp prevalence were also observed in the South-East Asian Region (13% in 2006–2008 to 21% in 2012–2016) [9], South Asia (21% in 2003–2012 to 30% in 2013–2022) [22], Oceania (6.4% in 1997–2000 to 16.1% in 2000–2013) [24]. Similar to this study, steady trends of CRHp have been reported for Latin America (11% in 1996–2000, 12% in 2001–2005, 14% in 2006–2011, p = 0.47) [26]. Furthermore, a decreasing trend in CRHp prevalence was noted for the European continent (25% in 2013–2016 to 20% (2017–2020), p = 0.002) [23].

This systematic review and meta-analysis reported ten types of H. pylori  23S rRNA mutations conferring clarithromycin resistance in Africa. All the reported 23S rRNA mutations have been already observed worldwide [27,28,29]. Our results are similar to those reported in Iran: A2143G (46.6%), A2142G (37.2%), and A2142C (5.5%) [30]. However, other 23S rRNA mutations conferring clarithromycin resistance in H. pylori, such as A2146G, C2772T, C2759T, G2212A, and A2144G, reported in Brazil [31], Mexico [27], Portugal [32], South Korea [33], and Iraq [34] have not been observed in Africa.

Conclusion

The data reported in this systematic review and meta-analysis showed that the pooled prevalence of CRHp in Africa was very similar to the overall pooled prevalence observed globally. In addition, more representative studies on H. pylori are needed in African countries. This can help to appreciate the real extent of antibiotic resistance in H. pylori strains. While waiting for further representative studies of the African population to be carried out, the treatment of H. pylori infections must be based on the guidelines of the AHMSG first Lagos consensus, for which triple therapy was suggested as this could be tenable.

Data availability

Data is provided within the manuscript or supplementary information files.

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Authors and Affiliations

  1. Department of Microbiology, Global Health Research Institute, Lomé, Togo

    Komla Mawunyo Dossouvi

  2. Laboratoire des Sciences Biomédicales Alimentaires et de Santé Environnementale, Ecole Supérieure des Techniques Biologiques et Alimentaires, Université de Lomé, Lomé, Togo

    Tchilabalo Bouyo

  3. Ecole Doctorale des Sciences Juridiques, Politiques, Economiques et de Gestion, Cheikh Anta Diop University, Dakar, Senegal

    Simon Sognonnou

  4. Medical Microbiology division, Medical Laboratory Services, University of Benin Teaching Hospital, Benin City, Nigeria

    Ephraim Ehidiamen Ibadin

  5. State Key Laboratory for Animal Disease Control and Prevention, Guangdong Laboratory for Lingnan Modern Agriculture, College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China

    Lu-chao Lv

  6. World Health Organization Country Office Senegal, Dakar, Senegal

    Bissoume Sambe Ba

  7. Faculté de Médecine, Pharmacie et Odontostomatologie, Cheikh Anta Diop University, Dakar, Senegal

    Abdoulaye Seck

  8. Fundamental Sciences Department, Health Sciences Faculty, Université de Kara, Kara, Togo

    Sika Dossim

  9. Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil

    Fábio Parra Sellera

  10. School of Veterinary Medicine, Metropolitan University of Santos, Santos, Brazil

    Fábio Parra Sellera

  11. Bacteriology-Virology laboratory, National University Teaching Hospital Aristide Le Dantec, Dakar, Senegal

    Makhtar Camara

  12. Department of Botany and Microbiology, Faculty of Science, Suez Canal University, Ismailia, 41522, Egypt

    Amr El Kelish

  13. Department of Biology, College of Science, Imam Muhammad Ibn Saud Islamic University (IMSIU), Riyadh, 11623, Saudi Arabia

    Amr El Kelish

  14. Molecular Biology and Biotechnology Department, Nigerian Institute of Medical Research, Yaba, Lagos, Nigeria

    Stella Ifeanyi Smith

  15. Department of Biological Sciences, Mountain Top University, Prayer, Ogun State, Nigeria

    Stella Ifeanyi Smith

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  1. Komla Mawunyo Dossouvi
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Contributions

K.M.D. conceptualized and designed the study, helped in data acquisition and analysis, and drafted the manuscript. T.B. helped in data acquisition and analysis. S.S. helped in data analysis. L.L., B.S.B., A.S., and S.D. substantively revised the manuscript. E.E.I., F.P.S. and M.C. provided writing assistance and substantively revised the manuscript. A.E.K. supervised the study and substantively revised the manuscript. S.I.S. supervised the study, and substantively revised the manuscript.

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Dossouvi, K.M., Bouyo, T., Sognonnou, S. et al. Clarithromycin-resistant Helicobacter pylori in Africa: a systematic review and meta-analysis. Antimicrob Resist Infect Control 14, 31 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13756-025-01533-6

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Keywords

Antimicrobial Resistance & Infection Control

ISSN: 2047-2994

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