Predominance of methicillin-resistant Staphylococcus aureus SCCmec type II-CC5 and SCCmec type IV-CC1/CC8 among companion animal clinical isolates in Japan: Findings from phylogenetic comparison with human clinical isolates

Objectives: To characterise the genotypic profiles of methicillin-resistant Staphylococcus aureus (MRSA) clinical isolates from companion animals and to investigate their association with those from humans in Japan. Methods: Non-duplicated MRSA clinical isolates recovered between July 2016 and January 2018 were analysed. The MRSA isolates were typed by polymerase chain reaction (PCR)-based open reading frame (ORF) typing (POT) scores, SCCmec types, multilocus sequence typing, and virulence gene profiles. Phylogenetic comparison of those isolates with previously described human isolates was performed. Results: Among 56 MRSA isolates (33 cats, 20 dogs and three rabbits), 26 isolates with a POT1 score of 93, SCCmec type II mostly belonged to CC5, including ST5. Twenty-six isolates with a POT1 score of 106, SCCmec type IV showed diversity of STs: 15 isolates belonged to CC8, mainly including ST8, and 11 isolates belonged to CC1, including ST1 and newly identified STs 4768, 4775, and 4779. Two cat isolates were ST8-SCCmec type IV possessing pvl/ACME-arcA, presumed to be the hypervirulent community-associated MRSA (CA-MRSA) clone USA300. Notably, all three rabbit isolates belonged to ST4768. The POT1 score 106 CA-MRSA isolates from animals and humans were divided into two large clusters of CC1 and CC8, where host species-specific sub-clusters were not identified within each cluster. A large cluster of POT1 score 93 healthcare-associated MRSA (HA-MRSA) isolates from animals and humans consisted of sub-clusters formed exclusively by the vast majority of human isolates and those formed by animal and human isolates. Conclusion: Companion animals could be potential reservoirs and vehicles for the transmission of CA-MRSA to humans, and could transmit companion animal-adaptive HA-MRSA lineages to humans as their second reservoirs.