Evaluation of Non-Invasive Biological Samples to Monitor Staphylococcus aureus Colonization in Great Apes and Lemurs

INTRODUCTION Reintroduction of endangered animals as part of conservational programs bears the risk of importing human pathogens from the sanctuary to the natural habitat. One bacterial pathogen that serves as a model organism to analyze this transmission is Staphylococcus aureus as it can colonize and infect both humans and animals. The aim of this study was to evaluate the utility of various biological samples to monitor S. aureus colonization in great apes and lemurs. METHODS Mucosal swabs from wild lemurs (n=25, Kirindy, Madagascar), feces, oral and genital swabs from captive chimpanzees (n=58, Ngamba and Entebbe, Uganda) and fruit wadges and feces from wild chimpanzees (n=21, Taï National Parc, Côte d'Ivoire) were screened for S. aureus. Antimicrobial resistance and selected virulence factors were tested for each isolate. Sequence based genotyping (spa typing, multilocus sequence typing) was applied to assess the population structure of S. aureus. RESULTS Oro-pharyngeal carriage of S. aureus was high in lemurs (72%, n=18) and captive chimpanzees (69.2%, n=27 and 100%, n=6, respectively). Wild chimpanzees shed S. aureus through feces (43.8, n=7) and fruit wadges (54.5, n=12). Analysis of multiple sampling revealed that two samples are sufficient to detect those animals which shed S. aureus through feces or fruit wadges. Genotyping showed that captive animals are more frequently colonized with human-associated S. aureus lineages. CONCLUSION Oro-pharyngeal swabs are useful to screen for S. aureus colonization in apes and lemurs before reintroduction. Duplicates of stool and fruit wadges reliably detect S. aureus shedding in wild chimpanzees. We propose to apply these sampling strategies in future reintroduction programs to screen for S. aureus colonization. They may also be useful to monitor S. aureus in wild populations.