Staphylococcus aureus, a Gram-positive prokaryote, is the most common human pathobiont, capable of asymptomatic colonization and infection in the majority of the human population. S. aureus causes infections in both healthy and hospitalized individuals, with a markedly high rate of recurrence. Colonization of host by the pathogen serves as a primary risk factor for initial and recurrent infections. Host individuals can be colonized with S. aureus across multiple body sites, commonly shed the organism in their local environment, and transmit S. aureus to nearby contacts. Multiple epidemiological and statistical studies have indicated that efficient prevention of S. aureus skin and soft tissue infections (SSTIs), as well as invasive infections, requires a deeper understanding of S. aureus colonization dynamics in the community and especially in the household. In order to provide the most comprehensive picture to date of S. aureus colonization dynamics, we have followed 150 households, comprising 692 individuals over a 12-month period. We recorded the history of S. aureus infection in these individuals, pairing information about host demographics and behavior with temporal colonization status at three body sites, pathogen environmental sampling, and molecular typing. We specifically traced the appearance and distribution of the S. aureus strains causing previous and interval SSTIs in the household and found these strains commonly present on household members and their local environment months after the initial infection. By combining this information with family pedigrees, we have further found that both colonization and infection risk are nearly evenly split between genetic and behavioral factors. Through our analysis, three major household S. aureus colonization dynamics types have been delineated and defined: (1) introductions, the appearance of a novel strain types across one or more individuals and environmental sites, (2) transmissions, the acquisition of a new strain type on a household member previously present within the household, and (3) persistence events, the continued presence of a strain type on an individual. These distinct phenomena share partially overlapping behavioral and hygiene-related factors, many of which were previously reported as risk factors for S. aureus colonization. We propose that colonization risk can be represented as the combination of individual susceptibility factors to these dynamics. Successful S. aureus colonization and infection intervention strategies must accordingly embrace a comprehensive set of prevention methods that are tailored to both individual and household attributes.




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