Clonally Diverse Methicillin and Multidrug Resistant Coagulase Negative Staphylococci Are Ubiquitous and Pose Transfer Ability Between Pets and Their Owners

Abstract

Sixty-eight owners and 66 pets, from 43 unrelated pet-owning households were screened for methicillin-resistant coagulase negative staphylococci (MRCoNS), potential cases of MRCoNS interspecies transmission (IT), and persistence. MRCoNS isolates were identified by microbiological and molecular tests. MLST-based phylogenetic analysis was performed in Staphylococcus epidermidis isolates. Antimicrobial susceptibility was evaluated using phenotypic and molecular methods. SCC mec type and the presence of biofilm-related ica locus was PCR-tested. Isolates suspected for MRCoNS IT cases were subjected to SmaI -PFGE analysis and individuals from positive households were followed-up for 1 year for carriage dynamics (every 3 months, T0–T4). Nineteen MRCoNS isolates from owners (27.9%) and 12 from pets (16.7%) were detected, coming from 20 households (46.5%). S. epidermidis was predominant (90 and 67% of human and animal strains, respectively), showing high phylogenetic diversity (16 STs among 24 strains). Methicillin-resistant S. epidermidis (MRSE) strains belonged to CC5 (75%), CC11 (12.5%), singleton S556 (8.3%), and S560 (4.17%). Significant host-associated differences were observed for resistance to aminoglycosides, co-trimoxazole, chloramphenicol (higher in animal isolates) and tetracycline (higher among human strains). Multidrug resistance (MDR) was common (68.4%) and associated with human strains. Great diversity of ccr and mec complexes were detected, most strains being non-typeable, followed by SCC mec IV and V. Over one third of isolates (most from owners), carried the ica locus, all MRSE CC5. Two sporadic IT cases (T0) were identified in owners and dogs from two households (4.7%), with diverse interspecies-exchanged clones detected along the sampling year, especially in dogs. A comparative analysis of all MRCoNS, with all nasal coagulase positive staphylococci (CoPS) recovered from the same individuals at T0, revealed that CoPS alone was predominant in owners and pets, followed by co-carriage of CoPS and MRCoNS in owners but single MRCoNS in pets. Statistical analyses revealed that owners are more prone to co-carriage and that co-existence of IT cases and co-carriage are positively interrelated. MRCoNS from healthy owners and their pets are genetically heterogeneous MDR strains that are spread in the community. Therefore, pets also contribute to the dissemination of successful human clones. Owner-pet inhabitancy increases the risk for staphylococcal temporal concomitance with its subsequent risk for bacterial infection and genetic exchange.

Multidrug-Resistant Coagulase-Negative Staphylococci Isolated from Bloodstream in the uMgungundlovu District of KwaZulu-Natal Province in South Africa: Emerging Pathogens

“…However, higher MRCoNS prevalence figures of 86% [ 12 ] and 100% [ 13 ] were detected for CoNS implicated in infections in South Africa. The S. epidermidis group ( S. epidermidis and S. haemolyticus ) is an important cause of nosocomial infections [ 1 ]. S. epidermidis is the most frequently isolated staphylococcal species in humans and considered the most important CoNS species [ 3 ].…”

“…Staphylococci are classified as either coagulase-positive or coagulase-negative, depending on their ability to clot plasma that is facilitated by the enzyme coagulase [ 1 ]. Coagulase-negative staphylococci (CoNS) are the most frequent colonizers of the skin and mucous membranes and the most frequently isolated organisms in microbiology laboratories [ 2 ].…”

“…CoNS are noted for their ability to develop antibiotic resistance against commonly used antibiotic classes such as β-lactams, aminoglycosides, and macrolides, with exceptionally high reported methicillin resistance rates [ 2 ] as well as resistance to antibiotics of last resort such as the glycopeptides [ 7 ]. Antibiotic resistance genes conferring resistance to these antibiotic classes can be transferred between staphylococcal species such as S. aureus and S. intermedius, limiting the therapeutic options available [ 1 , 8 ].…”

Virulence Factors in Coagulase-Negative Staphylococci

“…Additionally, several studies demonstrated that infections caused by these species affect debilitated domestic animals as cats with conjunctivitis, upper respiratory tract and skin or wound infections [16], or dogs with keratitis or urinary tract infections [17,18]. This is especially concerning, since it was already demonstrated that CoNS may be transferred from pets to their owners [19,20]. Moreover, some farm animals such as chickens are known to be the main reservoirs of antimicrobial resistance genes [21].…”

Frequency and Characterization of Antimicrobial Resistance and Virulence Genes of Coagulase-Negative Staphylococci from Wild Birds in Spain. Detection of tst-Carrying S. sciuri Isolates

“…Several studies have investigated the molecular characteristics of CoNS isolated from food items, companion animals, livestock and clinical samples [ 1 , 5 , 8 , 13 , 14 , 15 , 16 , 17 ], but CoNS from wildlife remains largely unattended. In this regard, birds have been postulated as sentinels, reservoirs and potential disseminators of antimicrobial resistance due to their interaction with the human interface, their diverse ecological niches and their capacity to migrate long distances [ 18 ].…”