Articles
Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study

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Summary

Background

Information about the prevalence of Staphylococcus aureus resistance to antimicrobial drugs has mainly been obtained from invasive strains, although the commensal microbiota is thought to be an important reservoir of resistance. We aimed to compare the prevalence of nasal S aureus carriage and antibiotic resistance, including meticillin-resistant S aureus (MRSA), in healthy patients across nine European countries.

Methods

In this cross-sectional study, nasal swabs were obtained from 32 206 patients recruited by family doctors participating in existing nationwide family doctor networks in Austria, Belgium, Croatia, France, Hungary, Spain, Sweden, the Netherlands, and the UK. Eligible patients were aged 4 years or older (≥18 years in the UK) and presented with a non-infectious disorder. Swabs were sent to national microbiological laboratories for identification and isolation of S aureus. Antibiotic resistance testing was done at one central microbiological laboratory. We established the genotypic structure of the isolated MRSA strains with the spa typing method.

Findings

S aureus was isolated from 6956 (21·6%) of 32 206 patients swabbed. The adjusted S aureus prevalence for patients older than 18 years ranged from 12·1% (Hungary) to 29·4% (Sweden). Except for penicillin, the highest recorded resistance rate was to azithromycin (from 1·6% in Sweden to 16·9% in France). In total, 91 MRSA strains were isolated, and the highest MRSA prevalence was reported in Belgium (2·1%). 53 different spa types were detected—the most prevalent were t002 (n=9) and t008 (n=8).

Interpretation

The prevalence of S aureus nasal carriage differed across the nine European countries assessed, even after correction for age, sex, and family doctor. Generally, the prevalence of resistance, including that of MRSA, was low. The MRSA strains recorded showed genotypic heterogeneity, both within and between countries.

Funding

European Commission, 7th Framework Programme (grant agreement 223083).

Introduction

Staphylococcus aureus forms part of the human microbiota, and the most consistent body site from which it can be isolated is the anterior nares.1, 2 In addition to the commensal role of this bacterium, S aureus can cause various infections in human beings, ranging from minor skin infections to severe pneumonia.3

The potential of S aureus to acquire resistance has been exemplified by the rapid emergence of resistance to penicillin and meticillin. The high rates of meticillin-resistant S aureus (MRSA) reported during the past few decades have been especially concerning because of the paucity of alternative treatment options. MRSA is the most important cause of antibiotic-resistant health-care-associated infections worldwide.4 Antibiotic use is believed to be the main driver for antibiotic resistance.5

Studies of the prevalence of S aureus resistance have so far mainly focused on invasive isolates, often obtained from patients admitted to hospital with bloodstream infections.6 Because of the scarcity of resistance data from the outpatient setting, the prevalence of resistance in invasive strains has been translated into guidelines for empirical antibiotic treatment of community-acquired infections, which will promote excessive use of broad-spectrum antibiotics in outpatients.6 An individual's commensal microbiota is thought to be the reservoir for antibiotic resistance genes and, therefore, resistance in this microbiota usually precedes the acquisition of resistance in pathogens.7 For these reasons, the amount of resistance in the commensal microbiota should be taken into account in clinical guidelines for general practitioners for the control of antibiotic resistance at the source.8

In our study (Appropriateness of Prescribing Antibiotics in Primary Health Care in Europe with Respect to Antibiotic Resistance; APRES), one of the main objectives was to establish the prevalence of antibiotic resistance to commensal S aureus, including rates of MRSA, in nine European countries with different rates and patterns of antibiotic prescription behaviour,9 to get an indication of the selection pressure that antibiotics exert on the general population.8 We also aimed to assess whether differences exist in the prevalence of nasal S aureus carriage in the nine participating countries. Additionally, the population structure of the isolated MRSA strains was to be established with spa typing to detect possible clustering of specific MRSA strains within one or more countries.

Section snippets

Study design

The APRES study design has been described elsewhere.9 Therefore, we will only briefly mention the methods used. The participating family doctors (with an aim for 20 per country) were recruited from existing national networks of family doctors in Austria, Belgium, Croatia, France, Hungary, Spain, Sweden, the Netherlands, and the UK from November, 2010, to August, 2011. Every family doctor was asked to collect nasal swabs from 200 patients, aged 4 years or older (or ≥18 years in the UK because of

Results

Table 1 shows the baseline characteristics of the APRES patient population. The number of patients recruited per country ranged from 3132 (Belgium) to 4017 (Hungary), constituting a total of 32 770 patients (table 1). Patients who did not meet the age inclusion criterion (people aged <18 years in the UK or <4 years in the other participating countries), incompleteness of data (missing patient background or laboratory data), or incorrect sampling (no bacterial growth recorded at laboratory

Discussion

This study included samples from more than 32 000 patients who did not have traditional risk factors for antibiotic resistance (an infectious disease at inclusion, recent antibiotic use, or recent admission to hospital) and is the first study in which standardised methods have been used to compare the prevalence and antibiotic resistance of commensal S aureus within and between countries (panel). The use of a central microbiological laboratory to do the antibiotic resistance analyses removes

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