Transmission of Antimicrobial-Resistant Staphylococcus Aureus Clonal Complex 9 Between Pigs and Humans, United States

Pranay R. Randad; Jesper Larsen; Hülya Kaya; Nora Pisanic; Carly Ordak; Lance B. Price; Maliha Aziz; Maya L. Nadimpalli; Sarah Rhodes; Jill R. Stewart; Dave C. Love; David Mohr; Meghan F. Davis; Lloyd S. Miller; Devon Hall; Karen C. Carroll; Trish M. Perl; Christopher D. Heaney

Disclosures

Emerging Infectious Diseases. 2021;27(3):740-748. 

In This Article

Abstract and Introduction

Abstract

Transmission of livestock-associated Staphylococcus aureus clonal complex 9 (LA-SA CC9) between pigs raised on industrial hog operations (IHOs) and humans in the United States is poorly understood. We analyzed whole-genome sequences from 32 international S. aureus CC9 isolates and 49 LA-SA CC9 isolates from IHO pigs and humans who work on or live near IHOs in 10 pig-producing counties in North Carolina, USA. Bioinformatic analysis of sequence data from the 81 isolates demonstrated 3 major LA-SA CC9 clades. North Carolina isolates all fell within a single clade (C3). High-resolution phylogenetic analysis of C3 revealed 2 subclades of intermingled IHO pig and human isolates differing by 0–34 single-nucleotide polymorphisms. Our findings suggest that LA-SA CC9 from pigs and humans share a common source and provide evidence of transmission of antimicrobial-resistant LA-SA CC9 between IHO pigs and humans who work on or live near IHOs in North Carolina.

Introduction

Livestock-associated Staphylococcus aureus (LA-SA) has emerged among pigs raised in industrial hog operations (IHOs) and persons who work on or live near IHOs globally, including in the United States.[1–4] IHO workers who are occupationally exposed to pigs are at increased risk for intranasal carriage of S. aureus, including methicillin-resistant S. aureus (MRSA), multidrug-resistant S. aureus (MDRSA), and LA-SA.[3,5] Furthermore, persons exposed to LA-SA are at risk of developing mild-to-severe infections, including skin and soft tissue infections (SSTIs), pneumonia, endocarditis, osteomyelitis, and bacteremia.[5–8] Recent evidence supports emergence of diverse clones associated with IHOs. S. aureus clonal complex 9 (CC9), for example, has been reported as a dominant LA-SA lineage in Asia and has been described as an emerging clone in some areas with intensive industrial livestock production in the United States.[9–11]

The population structure and transmission dynamics of emerging LA-SA CC9 strains in the United States remains poorly understood. Previous epidemiologic studies in the top 10 pig-producing counties in North Carolina, the second leading US pig-producing state, showed a high prevalence of LA-SA CC9 nasal carriage among IHO pigs and IHO workers.[3,12] Epidemiologic findings provide support for potential transmission of LA-SA CC9 between IHO workers and their household contacts, including minor children (<18 years of age; IHO minors), based on nasal carriage of LA-SA CC9 with concordant spa types at the same time point.[3] Epidemiologic studies have also identified instances of LA-SA CC9 nasal carriage among community residents with no known exposure to livestock in high-density IHO areas of North Carolina.[2] Whole-genome sequencing (WGS) analysis provides an opportunity to characterize the population structure and transmission dynamics of LA-SA CC9 in the United States. The objectives of this study were to use WGS and phylogenetic analyses to elucidate the population structure of S. aureus CC9 from various regions in North America, South America, Europe, and Asia and to investigate potential transmission of antimicrobial-resistant LA-SA CC9 among IHO pigs and humans who work on or live near IHOs in North Carolina.

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