Nocturnal Birds of Prey as Carriers of Staphylococcus aureus and Other Staphylococci: Diversity, Antimicrobial Resistance and Clonal Lineages

Abstract

Owls are nocturnal predators that inhabit urbanized and farmlands. They are in direct contact with other animals, both livestock and small wild rodents that they mostly feed on. Staphylococci can be both commensal and pathogenic bacteria that are widespread across the various ecological niches. We aimed to isolate staphylococci from owls and to characterize their antimicrobial resistance, virulence factors and genetic lineages. Swab samples were collected from the throat and cloaca of 114 owls admitted to two rehabilitation centers in Portugal. The identification of staphylococci species was performed by MALDI-TOF. Staphylococci antimicrobial resistance and virulence genes were investigated by means of the disk diffusion method and PCR. Staphylococcus aureus isolates were characterized by MLST, agr and spa-typing. Of the tested animals, 66 isolates were recovered, including 10 different species of staphylococci, of which 25 were coagulase-positive (CoPS) and 41 were coagulase-negative (CoNS). Twenty-three S. aureus were isolated, of which one mecC-MRSA was identified. The isolates were mainly resistant to penicillin, aminoglycosides, clindamycin and tetracycline. mecC-MRSA belonged to ST1245 and spa-type t843 and the remaining S. aureus were ascribed to 12 STs and 15 spa types. A high diversity of clonal lineages was identified among the S. aureus isolated from wild owls. Owls feed mainly on small rodents often exposed to waste and anthropogenic sources, which may explain the moderate prevalence of S. aureus in these animals.

Antimicrobial Resistance and Clonal Lineages of Staphylococcus aureus from Cattle, Their Handlers, and Their Surroundings: A Cross-Sectional Study from the One Health Perspective

“…S. aureus ST6-t16615 was the most prevalent lineage in cows and was not detected in human samples. This lineage has been reported among wild rats and owls in Portugal [ 57 , 65 ] and as the main lineage in livestock in Algeria [ 66 ]. Although considered a human clone with relatively high prevalence in Asian countries, this lineage seems to be widely disseminated among animals [ 67 ].…”

“…S. aureus ST30-t012 isolate may be related to the Southwest Pacific clone and was the most prevalent clone among community and hospital settings in Portugal between 1992 and 2011 [ 56 ]. ST30-t9413 has only been reported in Portugal in strains isolated from wild owls, superficial waters and one farm worker with close contact with cattle, and all studies were conducted in the same region as this study [ 19 , 32 , 57 ]. spa -type t9413 may be cattle-associated and the ST30-t9413 isolated from farm workers in this study may have an animal origin.…”

“…S. aureus ST133 and ST2328 belonging to CC133 and ST1 (CC1) are known to be livestock-associated and lately have emerged as important zoonotic lineages [ 68 ]. CC133 lineage is regarded as mostly ungulate-animal specific, but it has also been detected in wild animals and surface waters [ 19 , 57 , 69 ]. In fact, S. aureus CC133 has been reported as the most prevalent in bovine mastitis milk [ 70 , 71 ].…”

Antimicrobial Resistance and Molecular Epidemiology of Staphylococcus aureus from Hunters and Hunting Dogs

“…ST30 is an international successful clone since it has been found in Australia, Europe and Asia [ 61 ]. This lineage is primarily associated with humans, but it has been also found among animals and in the environment [ 55 , 62 ]. Moreover, ST30-MSSA-t012 has been detected in hospitalized humans and livestock workers in Portugal, in the same region where the samples of this study were collected [ 63 , 64 ].…”

“…Interestingly, in our study, one ST718-t11333 MSSA strain was also isolated from a hunter (Case 8) which shows the adaptability of this lineage. S. aureus ST718-t11333 has been identified among animals in only one study that was conducted with owl samples in Portugal [ 62 ]. Since hunters and their hunting dogs are in direct contact with wild game animals, transmission may also occur, especially between dogs and wild game animals.…”