Steinig, Eike, Aglua, Izzard, Duchene, Sebastian, Meehan, Michael T., Yoannes, Mition, Firth, Cadhla, Jaworski, Jan, Drekore, Jimmy, Urakoko, Bohu, Poka, Harry, Wurr, Clive, Ebos, Eri, Nangen, David, Muller, Elke, Mulvey, Peter, Jackson, Charlene, Blomfeldt, Anita, Vangstein Aamot, Hege, Laman, Moses, Manning, Laurens, Earls, Megan, Coleman, David C., Greenhill, Andrew, Ford, Rebecca, Stegger, Marc, Ali Syed, Muhammad, Jamil, Bushra, Monecke, Stefan, Ehricht, Ralf, Smith, Simon, Pomat, William, Horwood, Paul, Tong, Steven Y.C., and McBryde, Emma (2022) Phylodynamic signatures in the emergence of community-associated MRSA. Proceedings of the National Academy of Sciences of the United States of America, 119 (45). e2204993119.

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Abstract

Community-associated, methicillin-resistant Staphylococcus aureus (MRSA) lineages have emerged in many geographically distinct regions around the world during the past 30 y. Here, we apply consistent phylodynamic methods across multiple community-associated MRSA lineages to describe and contrast their patterns of emergence and dissemination. We generated whole-genome sequencing data for the Australian sequence type (ST) ST93-MRSA-IV from remote communities in Far North Queensland and Papua New Guinea, and the Bengal Bay ST772-MRSA-V clone from metropolitan communities in Pakistan. Increases in the effective reproduction number (Re) and sustained transmission (Re > 1) coincided with spread of progenitor methicillin-susceptible S. aureus (MSSA) in remote northern Australian populations, dissemination of the ST93-MRSA-IV genotype into population centers on the Australian East Coast, and subsequent importation into the highlands of Papua New Guinea and Far North Queensland. Applying the same phylodynamic methods to existing lineage datasets, we identified common signatures of epidemic growth in the emergence and epidemiological trajectory of community-associated S. aureus lineages from America, Asia, Australasia, and Europe. Surges in Re were observed at the divergence of antibiotic-resistant strains, coinciding with their establishment in regional population centers. Epidemic growth was also observed among drug-resistant MSSA clades in Africa and northern Australia. Our data suggest that the emergence of community-associated MRSA in the late 20th century was driven by a combination of antibiotic-resistant genotypes and host epidemiology, leading to abrupt changes in lineage-wide transmission dynamics and sustained transmission in regional population centers.

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