Livestock Origin for a Human Pandemic Clone of Community-Associated Methicillin-Resistant Staphylococcus aureus

Abstract

The importance of livestock as a source of bacterial pathogens with the potential for epidemic spread in human populations is unclear. In recent years, there has been a global increase in community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections of healthy humans, but an understanding of the different evolutionary origins of CA-MRSA clones and the basis for their recent expansion is lacking. Here, using a high-resolution phylogenetic approach, we report the discovery of two emergent clones of human epidemic CA-MRSA which resulted from independent livestock-to-human host jumps by the major bovine S. aureus complex, CC97. Of note, one of the new clones was isolated from human infections on four continents, demonstrating its global dissemination since the host jump occurred over 40 years ago. The emergence of both human S. aureus clones coincided with the independent acquisition of mobile genetic elements encoding antimicrobial resistance and human-specific mediators of immune evasion, consistent with an important role for these genetic events in the capacity to survive and transmit among human populations. In conclusion, we provide evidence that livestock represent a reservoir for the emergence of new human-pathogenic S. aureus clones with the capacity for pandemic spread. These findings have major public health implications highlighting the importance of surveillance for early identification of emergent clones and improved transmission control measures at the human-livestock interface.

Livestock-Associated MRSA and Its Current Evolution

“…It is a leading cause of bovine mastitis worldwide [43,77,79,80] and is found occasionally in small ruminants, pigs, and humans. It was determined that the human strains originated from a bovine to human host jump believed to have occurred approximately 40 years ago and subsequently acquired methicillin resistance [81]. MSSA CC97 strains are still circulating in humans [82,83].…”

Methicillin-Resistant Staphylococcus aureus (MRSA) in Food- Producing and Companion Animals and Food Products

“…CC398 is not limited to large livestock animals alone; it has also been reported in poultry [18,122], manure from chicken farms and soil fertilized with this manure [123]. However, the numbers of MRSA ST398-t011-SCCmec V isolated from chickens are lower (0-28%) than in pigs (82-92%) on the same farm [124].…”

“…LA-MRSA S. aureus CC398 is not alone in the ability to adapt. A phylogenetic study of S. aureus CC97 strains that originated from livestock and caused human infections in Asia, Europe, and North and South America indicated that in the process of adapting to the human host, CC97 acquired either the SCCmec IV or V cassete and the φSa3 containing an immune evasion cluster [123]. A more recent study in the United States demonstrated that 22% of 30 veterinary students who were initially MRSA negative became positive after visiting MRSA-positive pig farms in Iowa but were negative again by 24 h after the visit [75].…”

The path of least resistance: Paying for antibiotics in non-human uses

“…These include macrolides, streptogramins, aminoglycosides and tetracyclines, all classified as being of high importance for treating life-threatening human health conditions. [10] According to a growing body of scientific evidence a direct link can be demonstrated between antimicrobial resistance in livestock and in humans [11,12]. A recent study found that 36.6% of industrial livestock workers carried biomarkers associated with methicillinresistant Staphylococcus aureus (MRSA), compared with 19% of workers at antibiotic-free farms [13].…”