Staphylococcus aureus Host Range and Human-Bovine Host Shift

Abstract

Staphylococcus aureus is a major agent of bovine mastitis. The concomitant emergence of pig-associated methicillin-resistant S. aureus (MRSA) in human carriage and infection requires a reexamination of the host range and specificity of human-and cow-associated S. aureus strains, something which has not been systematically studied previously. The genetic relatedness of 500 S. aureus isolates from bovine mastitis cases, 57 isolates from nasal carriage of farmers, and 133 isolates from nonfarmers was determined by amplified fragment length polymorphism (AFLP) analysis and spa typing. Multilocus sequence typing (MLST) was conducted on a subset of isolates to match AFLP clusters with MLST clonal complexes (CCs). This data set allowed us to study host range and host specificity and to estimate the extent of bovine-tohuman transmission. The genotype compositions of S. aureus isolates from farmers and nonfarmers were very similar, while the mastitis isolates were quite distinct. Overall, transmission was low, but specific genotypes did show increased cow-to-human transmission. Unexpectedly, more than one-third of mastitis isolates belonged to CC8, a lineage which has not been considered to be bovine mastitis associated, but it is well known from human carriage and infection (i.e., USA300). Despite the fact that we did detect some transmission of other genotypes from cows to farmers, no transmission of CC8 isolates to farmers was detected, except for one tentative case. This was despite the close genetic relatedness of mastitis CC8 strains to nonfarmer carriage strains. These results suggest that the emergence of the new bovine-adapted genotype was due to a recent host shift from humans to cows concurrent with a loss of the ability to colonize humans. More broadly, our results indicate that host specificity is a lineage-specific trait that can rapidly evolve.The main niche and the largest reservoir of Staphylococcus aureus are human nares. On average, every third person is colonized with this facultative pathogen, making ca. 2 billion people colonized worldwide. Despite the fact that only a very small fraction of the carriers ever develop staphylococcal disease, its global burden is remarkable (27). Steadily increasing rates of colonization and infections with methicillin-resistant S. aureus (MRSA) are of special concern (20) because of the limited therapeutic options for such infections.Because of their sheer population size, farm animals constitute a potentially enormous reservoir of any pathogen. Even though the largest reservoir of S. aureus is human nares, the second largest may well be cows. The prevalence of S. aureus in bovine mastitis was estimated to be 3 to 5% (28, 34). Given the world's milking cow population of 1.5 billion (31), up to 75 million cows can be infected worldwide. The widespread colonization of pigs with a specific lineage of MRSA, ST398 (2), and emerging infections in humans (10,22,32) showed that the animal reservoir of. S. aureus can have potentially serious consequences for human health care...

Antimicrobial Resistance of Staphylococcus aureus Strains Acquired by Pig Farmers from Pigs

“…Clustering of AFLP data and MLST genotyping of several isolates per AFLP cluster were used to establish the identity of AFLP clusters as previously described (30,32). The genotype composition of S. aureus isolates from pigs and pig farmers and veterinarians was compared to those obtained earlier for healthy volunteers without contact with agriculture and from cow farmers (30,31).…”

Carriage of Staphylococcus aureus by Free-Living Wild Animals in Spain

“…MLST was performed on representative isolates from all spa types found per host. At least one isolate per spa type and host, together with S. aureus with spa types containing less than three repeats (24), were characterized by MLST (n ϭ 88). Based on these results, sequence types (STs) were assigned.…”

Sources of Contamination of Bovine Milk and Raw Milk Cheese by Staphylococcus aureus Using Variable Number of Tandem Repeat Analysis

“…This goes against the results of Hata et al [19] who concluded that pulsotypes isolates found in bulk milk are always different from those isolated from humans, but confirms the identity of certain strains of mastitis and human strains reported by other authors [4,[18][19][20]. These differences can be explained by the fact that isolates submitted to genotyping are taken randomly both in terms of the "time" of the collection and the selection of colonies on the primary isolation medium.…”

“…In their study Sakwinska et al [4] reported that more one third of mastitis isolates belonged to CC8, a clonal complex well known to be of human carriage and infection. They suggest the emergence of a new bovine-adapted genotype due to a recent host shift from human to cow concurrent with a loss of ability to colonize humans.…”

“…Moreover S. aureus is a major pathogen responsible for severe nosocomial and community-associated infections of humans. Livestock strains may have the capacity to colonize humans and humans represent an important source of new pathogenic strains affecting livestock [2][3][4][5][6]. Controlling milk and cheese contamination is an economic and health stake for all raw milk productions.…”