Skip to main content

Temporal trends of skin and soft tissue infections caused by methicillin-resistant Staphylococcus aureus in Gabon



Methicillin-resistant Staphylococcus aureus (MRSA) is one of the leading causes of mortality due to bacterial antimicrobial resistance. While S. aureus is common in skin and soft tissue infections (SSTI) in Africa, data on MRSA rates are scarce and reports vary widely across the continent (5%-80%). In this study, we describe the proportion of MRSA causing SSTI in Lambaréné, Gabon, over an 11-year period.


We retrospectively analyzed data from 953 bacterial specimens collected from inpatients and outpatients with SSTI at the Albert Schweitzer Hospital, Lambaréné, Gabon, between 2009 and 2019. We determined temporal changes in the prevalence of MRSA and identified risk factors for SSTI with MRSA.


68% of all specimens with bacterial growth yielded S. aureus (n = 499/731), of which 7% (36/497) with antimicrobial susceptibility testing were identified as MRSA. Age above 18 years, admission to the surgical ward, and deep-seated infections were significantly associated with MRSA as the causative agent. After an initial decline from 7% in 2009, there was a marked increase in the proportion of MRSA among all S. aureus from SSTI from 3 to 20% between 2012 and 2019. The resistance rate to erythromycin was significantly higher in MRSA than in methicillin-susceptible S. aureus (73% vs. 10%), and clindamycin resistance was detected exclusively in MRSA isolates (8%).


The increasing proportion of MRSA causing SSTI over the 11-year period contrasts with many European countries where MRSA is on decline. Continuous surveillance of MRSA lineages in the hospital and community along with antibiotic stewardship programs could address the increasing trend of MRSA.


Staphylococcus aureus is a Gram-positive bacterium that is part of the normal human flora and persistently colonizes about 30% of the human population [1]. However, under favorable conditions, including breaching the skin barrier or in hosts with an immature or compromised immune system, S. aureus is capable of causing a wide spectrum of infections [2]. These include skin and soft tissue infections (SSTI), bone and joint infections, pneumonia, endocarditis and sepsis [3].

According to the recent Global Burden of Disease Study 2019, S. aureus was the leading bacterial pathogen, accounting for more than one million deaths worldwide [4], while methicillin-resistant S. aureus (MRSA) was the second leading cause of death worldwide due to antimicrobial resistance [5].

The worldwide proportion of MRSA among S. aureus causing infections varies widely even within countries or regions on different continents. Reported frequencies range from less than 5% in northern Europe to up to 50% in southern Europe, around 50% in the United States, and 56–86% in parts of East Asia [6, 7]. Data from the African continent is mostly available for the Mediterranean region (19–52%), Nigeria (11–31%), and South Africa (24%), but scarce and primarily obtained from single-center studies for other Sub-Saharan countries [8].

In Africa, the high rates of SSTI are closely linked to the prevalence of S. aureus, which is fueled by the tropical climate and high rate of scabies and other skin diseases [9, 10]. It is estimated that the prevalence of MRSA-associated SSTI in Africa may exceed 50% [11,12,13]. In developing countries, such as Gabon, antibiotic resistance poses a major public health threat, but studies investigating the prevalence of antimicrobial resistance are limited [14, 15]. Data on temporal changes in the proportion of MRSA (among all S. aureus) causing SSTI in Gabon are currently not available. This cross-sectional study aimed to evaluate the prevalence of MRSA causing SSTI during 2009–2019 in a secondary care hospital in Lambaréné, Gabon.


Study design

We performed a historical cross-sectional study at the Albert Schweitzer Hospital (ASH) in Lambaréné, Gabon. The ASH has about 150 beds and is annually used by approximately 50,000 people. It offers services including surgery, pediatrics, internal medicine, gynecology, and emergency medicine. Between 2009 and 2019, all cases of SSTI with a specimen sent to the microbiology laboratory were screened for inclusion. From a total of 953 cases, 836 cases were included after excluding duplicate specimen from a patient’s current episode of infection. SSTI were stratified into superficial (impetigo, ecthyma, folliculitis, cellulitis, erysipelas, superficial abscess or wound infections) and deep-seated infections (subcutaneous abscess, pyomyositis, necrotizing fasciitis) as previously described [16].

Socio-demographic and clinical data were collected from the microbiology laboratory and medical records. Patients below 18 years were considered as children. Outpatients and non-admitted patients from other hospital settings were considered as from the community. Empirical antimicrobial therapy was defined as prescription of antimicrobial agents for the patient’s current episode of infection prior to specimen collection or pending microbiological diagnostics. Empirical therapy and the number of previously prescribed antibiotics were obtained from the laboratory request form.

Culture and identification

Samples from SSTI (e.g., swabs, pus) were cultured on Columbia blood agar (Oxoid, Basingstoke, Hampshire, United Kingdom) for 24–48 h at ambient air. Colonies suggestive for S. aureus were tested for catalase (BD BBL Catalase, Becton Dickinson, Franklin Lakes, NJ, USA), coagulase (BD BBL Coagulase Plasma, BD) and a slide agglutination test (Pastorex Staph Plus, Bio-Rad, Hercules, France) according to the manufacturer´s instructions.

MRSA identification and antimicrobial susceptibility testing

Antimicrobial susceptibility testing was performed using disc diffusion test according to the Clinical Laboratory Standards Institute (CLSI) guidelines and inhibition zone diameters were interpreted with CLSI breakpoints [17]. Intermediate results were considered non-susceptible along with the resistant isolates in this study.

MRSA was screened using cefoxitin disks (30 µg, Oxoid, USA) and methicillin resistance was confirmed by the detection of the Penicillin-binding Protein-2a (PBP2a) using a slide latex agglutination assay (Oxoid) following the manufacturer’s instruction.

As part of a clinical trial requirement, the microbiology laboratory successfully participates in regular external quality assurance (EQA) programs, addressing species identification and susceptibility testing. The EQA is part of the WHO/NICD Proficiency Testing Scheme and is organized by the Contract Laboratory Services (CLS), Johannesburg, South Africa.

Data analysis

All data analyses were performed using the software ‘‘R’’ (, Version: 4.3.1). Pearson’s chi-square test or Fisher’s exact test were used to analyze categorical data, t-test to analyze continuous data. Due to the retrospective nature of our data collection, we were unable to obtain certain missing patient information. Therefore, we report both absolute numbers and percentages of observed events, calculated based on the total number of events for which data were available.


Out of 836 non-duplicate specimens obtained from SSTI between 2009 and 2019, 87.4% (731/836) yielded bacterial growth of which 68.3% (499/731) were identified as S. aureus. The median age of SSTI patients with a positive culture was 6 (0–89) years and the majority of cases were in children (432/678). Infection with S. aureus was significantly associated with young age, highlighted by S. aureus constituting the causative agent in 77% (334/432) of SSTI cases in children (OR 2.9, 95% CI 2.1–4.1, p < 0.001). SSTI with S. aureus was more prevalent in patients without empirical antimicrobial therapy (70%, 301/429), and previous prescription of more than two antibiotics was associated with a decrease in S. aureus SSTI (43%, 9/21; OR 0.3, 95% CI 0.1–0.8, p = 0.013). More than half of the cases (54%, 268/499) were categorized as community-acquired.

Two of the 499 identified S. aureus isolates were excluded from subsequent analyses due to a lack of antimicrobial susceptibility testing. This reduced the number of isolates to 497. The overall proportion of MRSA among all S. aureus isolates collected during the study period was 7.2% (36/497). The proportion of MRSA in SSTI initially declined from 7 to 3% between 2009 in 2012, followed by a marked increase to 20% in 2019 (Fig. 1).

Fig. 1
figure 1

Temporal trends of the proportion of methicillin-resistant Staphylococcus aureus (MRSA) in S. aureus skin and soft tissue infection (SSTI) samples from 2009 to 2019. Stacked bars show the number of MRSA (grey) or methicillin-susceptible S. aureus (MSSA, white) isolates per year. Green line with error bars shows the proportion of MRSA among S. aureus (as percentage with 95% confidence interval) for each year. It should be noted that the peak in the total number of S. aureus from SSTI in 2011 and 2012 may be attributed to an increased number of detected SSTI cases among participants in a malaria vaccine trial conducted at the study site between 2009 and 2013

Methicillin resistance rates were four times higher in isolates from adults than children (16% vs. 4%, p < 0.001) with a median age of patients with MRSA-associated SSTI of 24 (range: 0–76) years (Table 1).

Table 1 Demographic characteristics and clinical data of patients with SSTI caused by S. aureus

We found that patient age above 18 years (OR 4.7, 95% CI 2.3–10.0, p < 0.001), admission to the surgical ward (OR 4.1, 95% CI 1.9–8.9, p < 0.001), and deep-seated infections (OR 7.9, 95% CI 3.0–19.9, p < 0.001) were significantly associated with MRSA as the causative agent (Table 1). We observed that the odds of infection with MRSA increased with the number of previously prescribed antibiotics. However, the association was not statistically significant (Table 1).

The rate of resistance to erythromycin (73% vs. 10%) and gentamicin (15% vs. 3%) was significantly higher in MRSA than in MSSA isolates, and clindamycin resistance was detected exclusively in one MRSA isolate (8%, Table 2). Temporal trends in the antimicrobial resistance profile of MRSA and MSSA are provided in Figure S1.

Table 2 Antibiotic resistance of S. aureus isolates


We performed a historical cross-sectional study on S. aureus SSTI and found an increase in the proportion of MRSA over a period of 11 years.

The majority of SSTI are caused by S. aureus. In our study, 68% (499/731) of all culture-positive SSTI samples yielded S. aureus as the causative agent, which is consistent with findings from Gabon (75%), Kenya (46%) or Switzerland (65%) [18,19,20].

The overall proportion of MRSA among all S. aureus in our study was 7%, while the proportion ranged from 3–8% between 2009 and 2016, followed by a marked increase to 20% in 2019. In line with this, previous studies conducted between 2008 and 2012 in Lambaréné observed MRSA rates of 6–11% [14, 20]. Similarly, a prospective multi-center study conducted between 2016 and 2018 in Gabon found a rate of 16% MRSA among all S. aureus isolates [15]. While the above studies included isolates from all types of infections, a study conducted in several Sub-Saharan African countries, including Gabon, on the management of S. aureus SSTI detected 6.5% MRSA [16]. In this multicenter study, the rate of MRSA was similar in superficial and deep-seated infections which is divergent to our finding of significantly higher MRSA rates in deep-seated compared to superficial infections.

The observed increase in the rate of MRSA in isolates originating from the surgical ward of the hospital (18%) may be attributed to the fact that MRSA patients are more likely to fail empirical antimicrobial therapy and therefore progress to more severe infections requiring surgical intervention. This is supported by the high proportion of MRSA-associated purulent infections in our study, such as abscesses, that require surgical drainage [16]. Alternatively, it might point toward a nosocomial transmission of MRSA on surgical wards. Such a transmission might be further supported by a lower MRSA prevalence on pediatric wards. However, such a nosocomial source has not been investigated yet. Past studies rather suggest multiple sources for MRSA colonization as indicated by S. aureus protein A (spa)-types (t186, t653, t121, t729) or multilocus sequence types (ST5, ST8, ST88) among five MRSA isolates from health care workers, patients and the general population in Lambaréné, Gabon [21]. Noteworthy, these sequence types are also among the major MRSA lineages in Africa [22]. Further updated genotyping analysis of MRSA in our study setting are warranted to identify potential new sources and transmission chains.

A recent survey conducted among healthcare workers in our study area revealed a lack of knowledge on causes for the emergence of antimicrobial resistance and poor antibiotic stewardship [23]. Irrational prescription habits and easy accessibility to antimicrobials without a prescription might underlie the increase in MRSA shown in our study region.

A peak in the incidence of S. aureus SSTI was observed in 2012, while the proportion of MRSA was very low (Fig. 1). A malaria vaccination trial was conducted at our study site from 2009 to 2013 [24]. During the primary vaccination series and follow-up visits, the participants were seen by a physician which may have increased the chance of detecting SSTI that were previously undetected, thus, affecting sample sizes during this period. However, there was no active screening for SSTIs, and specimens were only collected and sent to the microbiology laboratory if there was clinical evidence of an SSTI. There were two age groups in the study, one comprising infants aged 6–12 weeks and the other comprising young infants aged 5–17 months. This may account for the observed proportion of approximately two-thirds of children among SSTI patients in our study and the median age of 4 years among patients with S. aureus SSTI. However, previous studies in Sub-Saharan Africa have shown that the median age of patients with S. aureus infections, including SSTI, can be as low as 3–4 years [12, 16].

Our study has several limitations. First, since this is a historical cross-sectional study, we exclusively relied on the medical and laboratory records of the patients for whom microbiological testing was requested. Thus, patients who have not undergone microbiological examination could have been missed in our study, possibly underestimating the rate of SSTI in the study area. Due to the limited medical data, the duration of stay, or applied treatment and outcome of the patients was not completely assessed. In addition, we were unable to classify infections according to standard definitions of hospital-acquired, community-acquired, or healthcare-associated infections [25]. The availability of these data would help to elucidate the role of iatrogenic infections, including those associated with healthcare interactions but emerging within the community. Second, we were not able to analyze the genotype of the MRSA isolates regarding the sequence type or clonal complex attribution. Lastly, the inclusion of a single hospital may not be representative of the entire country or Central African region.


In conclusion, the proportion of MRSA among S. aureus SSTI increase steadily over an 11-year period. Continuous surveillance of MRSA lineages in the hospital and community along with antibiotic stewardship programs could address the increasing trend of MRSA in Lambaréné.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.



Skin and soft tissue infections


Methicillin-resistant Staphylococcus aureus


Methicillin-susceptible Staphylococcus aureus


Odds ratio

95% CI:

95% Confidence interval


  1. Becker K, Schaumburg F, Fegeler C, Friedrich AW, Kock R. Prevalence of Multiresistant Microorganisms PMMS. Staphylococcus aureus from the German general population is highly diverse. Int J Med Microbiol. 2017;307(1):21–7.

    Article  CAS  PubMed  Google Scholar 

  2. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28(3):603–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339(8):520–32.

    Article  CAS  PubMed  Google Scholar 

  4. Collaborators GBDAR. Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2022;400(10369):2221–48;

  5. Antimicrobial RC. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55.

    Article  Google Scholar 

  6. Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers. 2018;4:18033.

    Article  PubMed  Google Scholar 

  7. Lakhundi S, Zhang K. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin Microbiol Rev. 2018;31(4);

  8. Falagas ME, Karageorgopoulos DE, Leptidis J, Korbila IP. MRSA in Africa: filling the global map of antimicrobial resistance. PLoS ONE. 2013;8(7):e68024.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Karimkhani C, Dellavalle RP, Coffeng LE, Flohr C, Hay RJ, Langan SM, et al. Global Skin Disease Morbidity and Mortality: An Update From the Global Burden of Disease Study 2013. JAMA Dermatol. 2017;153(5):406–12.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Engelman D, Hofer A, Davis JS, Carapetis JR, Baird RW, Giffard PM, et al. Invasive Staphylococcus aureus Infections in Children in Tropical Northern Australia. J Pediatric Infect Dis Soc. 2014;3(4):304–11.

    Article  PubMed  Google Scholar 

  11. Stryjewski ME, Chambers HF. Skin and soft-tissue infections caused by community-acquired methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2008;46(Suppl 5):S368–77.

    Article  CAS  PubMed  Google Scholar 

  12. Ruffing U, Alabi A, Kazimoto T, Vubil DC, Akulenko R, Abdulla S, et al. Community-Associated Staphylococcus aureus from Sub-Saharan Africa and Germany: A Cross-Sectional Geographic Correlation Study. Sci Rep. 2017;7(1):154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Urban E, Stone GG. Impact of EUCAST ceftaroline breakpoint change on the susceptibility of methicillin-resistant Staphylococcus aureus isolates collected from patients with complicated skin and soft-tissue infections. Clin Microbiol Infect. 2019;25(11):1429 e1-e4.

    Article  CAS  PubMed  Google Scholar 

  14. Schaumburg F, Ngoa UA, Kosters K, Kock R, Adegnika AA, Kremsner PG, et al. Virulence factors and genotypes of Staphylococcus aureus from infection and carriage in Gabon. Clin Microbiol Infect. 2011;17(10):1507–13.

    Article  CAS  PubMed  Google Scholar 

  15. Dikoumba A-C, Onanga R, Mbehang Nguema PP, Mangouka L, Iroungou B, Kassa F, et al. Phenotipic Prevalence of Antibiotic Resistance in Gabon. Open Journal of Medical Microbiology. 2021;11:100–18.

    Article  CAS  Google Scholar 

  16. Alabi A, Kazimoto T, Lebughe M, Vubil D, Phaku P, Mandomando I, et al. Management of superficial and deep-seated Staphylococcus aureus skin and soft tissue infections in sub-Saharan Africa: a post hoc analysis of the StaphNet cohort. Infection. 2018;46(3):395–404.

    Article  PubMed  Google Scholar 

  17. CLSI. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—Eleventh Edition. CLSI document M02-A11. Wayne, PA: Clinical and Laboratory Standards Institute; 2012.

    Google Scholar 

  18. Maina EK, Kiiyukia C, Wamae CN, Waiyaki PG, Kariuki S. Characterization of methicillin-resistant Staphylococcus aureus from skin and soft tissue infections in patients in Nairobi. Kenya Int J Infect Dis. 2013;17(2):e115–9.

    Article  CAS  PubMed  Google Scholar 

  19. Bouvet C, Gjoni S, Zenelaj B, Lipsky BA, Hakko E, Uckay I. Staphylococcus aureus soft tissue infection may increase the risk of subsequent staphylococcal soft tissue infections. Int J Infect Dis. 2017;60:44–8.

    Article  PubMed  Google Scholar 

  20. Alabi AS, Frielinghaus L, Kaba H, Kosters K, Huson MA, Kahl BC, et al. Retrospective analysis of antimicrobial resistance and bacterial spectrum of infection in Gabon. Central Africa BMC Infect Dis. 2013;13:455.

    Article  PubMed  Google Scholar 

  21. Ateba Ngoa U, Schaumburg F, Adegnika AA, Kosters K, Moller T, Gaus E, et al. Epidemiology and population structure of Staphylococcus aureus in various population groups from a rural and semi urban area in Gabon. Central Africa Acta Trop. 2012;124(1):42–7.

    Article  PubMed  Google Scholar 

  22. Lawal OU, Ayobami O, Abouelfetouh A, Mourabit N, Kaba M, Egyir B, et al. A 6-Year Update on the Diversity of Methicillin-Resistant Staphylococcus aureus Clones in Africa: A Systematic Review. Front Microbiol. 2022;13:860436.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Adegbite BR, Edoa JR, Schaumburg F, Alabi AS, Adegnika AA, Grobusch MP. Knowledge and perception on antimicrobial resistance and antibiotics prescribing attitude among physicians and nurses in Lambarene region, Gabon: a call for setting-up an antimicrobial stewardship program. Antimicrob Resist Infect Control. 2022;11(1):44.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rts SCTP. Efficacy and safety of the RTS, S/AS01 malaria vaccine during 18 months after vaccination: a phase 3 randomized, controlled trial in children and young infants at 11 African sites. PLoS Med. 2014;11(7):e1001685.

    Article  Google Scholar 

  25. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, et al. Health care–associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med. 2002;137(10):791–7.

    Article  PubMed  Google Scholar 

Download references


Not applicable.


Open Access funding enabled and organized by Projekt DEAL. This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation, grant 404893180). We acknowledge support from the Open Access Publication Fund of the University of Münster.

Author information

Authors and Affiliations



FS, MBBM, ASA and AAA contributed to conception and design of the study. CSG, MAAD and SOOB acquired material and data. CSG and TG analyzed and interpreted data. CSG, FS and TG wrote the first draft of the manuscript. All authors assisted in editing the manuscript and agreed on the final version of the manuscript before submission for peer review.

Corresponding author

Correspondence to Tobias Grebe.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gouleu, C.S., Daouda, M.A., Oye Bingono, S.O. et al. Temporal trends of skin and soft tissue infections caused by methicillin-resistant Staphylococcus aureus in Gabon. Antimicrob Resist Infect Control 13, 68 (2024).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: