Molecular Epidemiology of Staphylococcus aureus in the General Population in Northeast Germany: Results of the Study of Health in Pomerania (SHIP-TREND-0)

Abstract

Population-based studies on Staphylococcus aureus nasal colonization are scarce. We examined the prevalence, resistance, and molecular diversity of S. aureus in the general population in Northeast Germany. Nasal swabs were obtained from 3,891 adults in the large-scale population-based Study of Health in Pomerania (SHIP-TREND). Isolates were characterized using spa genotyping, as well as antibiotic resistance and virulence gene profiling. We observed an S. aureus prevalence of 27.2%. Nasal S. aureus carriage was associated with male sex and inversely correlated with age. Methicillin-resistant S. aureus (MRSA) accounted for 0.95% of the colonizing S. aureus strains. MRSA carriage was associated with frequent visits to hospitals, nursing homes, or retirement homes within the previous 24 months. All MRSA strains were resistant to multiple antibiotics. Most MRSA isolates belonged to the pandemic European hospital-acquired MRSA sequence type 22 (HA-MRSA-ST22) lineage. We also detected one livestock-associated MRSA ST398 (LA-MRSA-ST398) isolate, as well as six livestock-associated methicillin-susceptible S. aureus (LA-MSSA) isolates (clonal complex 1 [CC1], CC97, and CC398). spa typing revealed a diverse but also highly clonal S. aureus population structure. We identified a total of 357 spa types, which were grouped into 30 CCs or sequence types. The major seven CCs (CC30, CC45, CC15, CC8, CC7, CC22, and CC25) included 75% of all isolates. Virulence gene patterns were strongly linked to the clonal background. In conclusion, MSSA and MRSA prevalences and the molecular diversity of S. aureus in Northeast Germany are consistent with those of other European countries. The detection of HA-MRSA and LA-MRSA within the general population indicates possible transmission from hospitals and livestock, respectively, and should be closely monitored.

FIG 1

Mean prevalences (error bars show 95% confidence interval) of S. aureus nasal colonization according to age and gender.

FIG 2

The S. aureus population structure is highly diverse. (A) Minimum spanning tree generated from spa data using the BioNumerics software. Each sphere, or node, represents a unique spa type. The size of each node indicates the number of S. aureus isolates per spa type. The length between two nodes reflects the genetic distance between the two bordering spa types (maximum neighbor distance, 1.00). Nodes are color-coded according the presumptively associated clonal cluster. White circles represent singletons, i.e., strains that were not assigned to any CC. The identification of CCs is based on the BURP algorithm, as implemented in the Ridom StaphType software, aided by MLST sequencing of selected strains. (B) Prevalence of CCs and STs within the SHIP-TREND-0 cohort. spa types marked as excluded were not assigned to clusters, as their repeat sequence included fewer than 5 repeats, and no reliable information about phylogenetic relatedness can be inferred. spa types marked as singletons could not be assigned to a CC. CCs were color-coded in the same manner as in panel A.

FIG 3

S. aureus virulence genes are linked to CCs. Frequency plot depicting the frequency of virulence genes within each S. aureus CC, as illustrated by both color and size of the squares. If a gene occurred in fewer than 5% of isolates per CC, the number of S. aureus isolates positive for the gene is given. Virulence genes are grouped according to their genomic location. agr (agr1 to -4; agr_neg, no agr detected), and egc superantigens (seg, sei, sem, sen, seo, and seu) are core-variable genes. All other virulence genes are located on MGEs. In detail, sea and sep are encoded by the Sa3int phages, tst, sec, and sel as well as seb, sek, and seq are localized on S. aureus pathogenicity islands, while sed, sej, ser, ses, and set are carried on plasmids. eta and etd are located on a phage and plasmid, respectively, while luk-PV is located on a phage. The number of isolates per CC is provided in square brackets. CCs with more than 5 isolates are depicted.