Occurrence and relatedness of vancomycin-resistant enterococci in animals, humans, and the environment in different European regions

Abstract

Vancomycin-resistant enterococci (VRE) in Europe are thought to have emerged partly due to the use of the glycopeptide avoparcin in animal husbandry. We compared the occurrence of VRE in geographical regions of Europe in which until 1997 large amounts of avoparcin were used (Spain, United Kingdom, and Denmark) with the occurrence of VRE in Sweden, where avoparcin was banned in 1986. We also studied the relatedness between VRE strains from different regions and habitats. In total, 2,580 samples were collected from humans, animals, and the environment (soil, sewage, recipient water). VRE resistant to 20 microg/ml vancomycin were identified in 8.2% of the samples and were found most frequently in raw and treated urban sewage samples (means, 71% and 36% of the samples, respectively), pig manure (17%), and hospital sewage (16%). The proportions of VRE-positive sewage samples were similar in Sweden, Spain, and the United Kingdom, whereas pig feces and manure were more often positive in Spain than in Sweden (30% versus 1%). Most VRE were Enterococcus faecium carrying vanA, and computerized biochemical phenotyping of the isolates of different ecological origins showed a high degree of polyclonality. In conclusion, it seems that animal-associated VRE probably reflect the former use of avoparcin in animal production, whereas VRE in human-associated samples may be a result of antibiotic use in hospitals. Since there seems to be a reservoir of the resistance genes in all countries studied, precautions must be taken to limit the use of antibiotics and antibiotic-like feed additives.

FIG. 1.

Dendrogram showing the results of a cluster analysis (unweighted-pair group method using average linkages) of PhP-FS typing data for 127 isolates confirmed to be enterococci, having vancomycin MICs of ≥32 μg/ml, and representing diverse clusters (only one isolate per PhP-RF type and sample was included). The dotted line indicates the identity level that was determined by the reproducibility of the typing method (25). Isolates that show similarity to each other higher than this level were assigned to the same PhP type. Solid circles indicate isolates of animal origin, open circles indicate isolates of human origin, and no mark indicates isolates having other or mixed origins. The arrows indicate the only two PhP types that comprise isolates of both human origin and animal origin.

FIG. 2.

Dendrogram showing the results of a cluster analysis (unweighted-pair group method using average linkages) of PhP-FS typing data for 32 E. faecium isolates and four E. hirae isolates of animal origin having vancomycin MICs of ≥32 μg/ml. The isolates included isolates from broilers from slaughterhouses (SB), from cattle from slaughterhouses (SC), from pigs from slaughterhouses (SP), from pig feces (PF), and from pig manure (PM). SE, Sweden; DK, Denmark; ES, Spain. Shading indicates a cluster of identical E. faecium isolates having different origins.

FIG. 3.

Dendrogram showing the results of a cluster analysis (unweighted-pair group method using average linkages) of PhP-FS typing data for 72 E. faecium isolates of presumed human origin (urban and hospital sewage isolates, clinical isolates) having vancomycin MICs of ≥32 μg/ml. Shading indicates isolates showing high similarity to the ampicillin- and ciprofloxacin-resistant clone FMSE1 previously found nationwide in Sweden. SE, Sweden; ES, Spain; UK, United Kingdom; sew., sewage.