Genomic Evidence for Direct Transmission of mecC-MRSA between a Horse and Its Veterinarian

Methicillin-resistant Staphylococcus aureus bearing the mecC gene (mecC-MRSA) has been reported from animals and humans in recent years. This study describes the first mecC-MRSA isolates of human and equine origin in Hungary (two isolates from horses and one from a veterinarian, who treated one of the infected horses, but was asymptomatic). MRSA isolates were identified by cultivation and PCR detection of the species-specific spa gene and mecA/mecC methicillin resistance genes. The isolates were characterized by antibiotic susceptibility testing, MLST, spa, SCCmec typing, PFGE and whole genome sequencing (WGS). All three isolates belonged to the ST130-t843-SCCmec XI genotype, and carried the mecC and blaZ genes. Apart from beta-lactam drugs, they were sensitive to all tested antibiotics. The isolates of the infected horse and its veterinarian had the same PFGE pulsotype and showed only slight differences with WGS. Hence, this is the first description of direct transmission of a mecC-carrying MRSA between a horse and its veterinarian. The emergence of mecC in the country highlights the importance of the appropriate diagnostics in MRSA identification.

[1]  B. Söderquist,et al.  Evaluation of within-host evolution of methicillin-resistant Staphylococcus aureus (MRSA) by comparing cgMLST and SNP analysis approaches , 2022, Scientific Reports.

[2]  M. Steward,et al.  Prevalence of Staphylococcus aureus in wild hedgehogs (Erinaceus europaeus) and first report of mecC-MRSA in Hungary. , 2022, The Science of the total environment.

[3]  S. Börjesson,et al.  Benzylpenicillin-producing Trichophyton erinacei and methicillin resistant Staphylococcus aureus carrying the mecC gene on European hedgehogs – A pilot-study , 2021, BMC microbiology.

[4]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[5]  U. Höfle,et al.  Genomic Analysis of Staphylococcus aureus of the Lineage CC130, Including mecC-Carrying MRSA and MSSA Isolates Recovered of Animal, Human, and Environmental Origins , 2021, Frontiers in Microbiology.

[6]  L. Calvinho,et al.  Antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis: Systematic review and meta-analysis. , 2021, Preventive veterinary medicine.

[7]  Thomas M. Keane,et al.  Twelve years of SAMtools and BCFtools , 2020, GigaScience.

[8]  H. Castro,et al.  First report of meticillin-resistant Staphylococcus aureus harboring mecC gene in milk samples from cows with mastitis in southeastern Brazil , 2020, Brazilian Journal of Microbiology.

[9]  C. Torres,et al.  Human mecC-Carrying MRSA: Clinical Implications and Risk Factors , 2020, Microorganisms.

[10]  P. Kovács,et al.  Occurrence and characterisation of methicillin-resistant Staphylococcus aureus isolated from bovine milk in Hungary. , 2020, Acta veterinaria Hungarica.

[11]  G. Balka,et al.  Genomic Analysis of Staphylococcus aureus Strains Originating from Hungarian Rabbit Farms Reinforce the Clonal Origin of Various Virulence Types , 2020, Animals : an open access journal from MDPI.

[12]  E. Aklilu,et al.  First mecC and mecA Positive Livestock-Associated Methicillin Resistant Staphylococcus aureus (mecC MRSA/LA-MRSA) from Dairy Cattle in Malaysia , 2020, Microorganisms.

[13]  G. Paterson,et al.  Low prevalence of livestock‐associated methicillin‐resistant Staphylococcus aureus clonal complex 398 and mecC MRSA among human isolates in North‐West England , 2020, Journal of applied microbiology.

[14]  M. Kuroda,et al.  Identification of a mecA/mecC-positive MRSA ST1-t127 isolate from a racehorse in Japan. , 2019, The Journal of antimicrobial chemotherapy.

[15]  V. Perreten,et al.  Outbreaks of a Methicillin-Resistant Staphylococcus aureus Clone ST398-t011 in a Hungarian Equine Clinic: Emergence of Rifampicin and Chloramphenicol Resistance After Treatment with These Antibiotics. , 2019, Microbial drug resistance.

[16]  M. Bes,et al.  Persistence and Diffusion of mecC-Positive CC130 MRSA Isolates in Dairy Farms in Meurthe-et-Moselle County (France) , 2019, Front. Microbiol..

[17]  C. Knoop,et al.  Emergence of livestock-associated MRSA isolated from cystic fibrosis patients: Result of a Belgian national survey. , 2019, Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society.

[18]  Emmanuel Paradis,et al.  ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R , 2018, Bioinform..

[19]  A. Cherif,et al.  Prevalence of methicillin-resistant and susceptible coagulase-negative staphylococci with the first detection of the mecC gene among cows, humans, and manure in Tunisia. , 2019, International journal of antimicrobial agents.

[20]  B. Olsen,et al.  Staphylococcus aureus Carrying mecC Gene in Animals and Urban Wastewater , Spain , 2019 .

[21]  Sahreena S. Lakhundi,et al.  Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology , 2018, Clinical Microbiology Reviews.

[22]  O. Lund,et al.  SCCmecFinder, a Web-Based Tool for Typing of Staphylococcal Cassette Chromosome mec in Staphylococcus aureus Using Whole-Genome Sequence Data , 2018, mSphere.

[23]  M. Holmes,et al.  Comparison of Different Phenotypic Approaches To Screen and Detect mecC-Harboring Methicillin-Resistant Staphylococcus aureus , 2017, Journal of Clinical Microbiology.

[24]  Mirko Rossi,et al.  chewBBACA: A complete suite for gene-by-gene schema creation and strain identification , 2017, bioRxiv.

[25]  W. Witte,et al.  MRSA in equine hospitals and its significance for infections in humans. , 2017, Veterinary microbiology.

[26]  B. Lilje,et al.  Report of mecC-carrying MRSA in domestic swine , 2016, The Journal of antimicrobial chemotherapy.

[27]  S. Monecke,et al.  Diversity of Staphylococcus aureus Isolates in European Wildlife , 2016, PloS one.

[28]  D. Trott,et al.  Isolation of mecC MRSA in Australia. , 2016, The Journal of antimicrobial chemotherapy.

[29]  Hing-Fung Ting,et al.  MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. , 2016, Methods.

[30]  K. Becker,et al.  Clinical Significance and Pathogenesis of Staphylococcal Small Colony Variants in Persistent Infections , 2016, Clinical Microbiology Reviews.

[31]  W. Witte,et al.  Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans , 2015, One health.

[32]  Klaus Schliep,et al.  Phylogenetic Analysis in R , 2015 .

[33]  M. Bes,et al.  mecC-positive MRSA in horses. , 2015, The Journal of antimicrobial chemotherapy.

[34]  Nicholas S. Gleadall,et al.  Old Drugs To Treat Resistant Bugs: Methicillin-Resistant Staphylococcus aureus Isolates with mecC Are Susceptible to a Combination of Penicillin and Clavulanic Acid , 2015, Antimicrobial Agents and Chemotherapy.

[35]  P. Worning,et al.  Monitoring meticillin resistant Staphylococcus aureus and its spread in Copenhagen, Denmark, 2013, through routine whole genome sequencing. , 2015, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[36]  M. Holmes,et al.  Detection of mecC-Methicillin-resistant Staphylococcus aureus isolates in river water: a potential role for water in the environmental dissemination. , 2014, Environmental microbiology reports.

[37]  P. Worning,et al.  Comparing Whole-Genome Sequencing with Sanger Sequencing for spa Typing of Methicillin-Resistant Staphylococcus aureus , 2014, Journal of Clinical Microbiology.

[38]  R. Cantón,et al.  Staphylococcus aureus Carrying mecC Gene in Animals and Urban Wastewater, Spain , 2014, Emerging infectious diseases.

[39]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[40]  Ole Lund,et al.  Real-Time Whole-Genome Sequencing for Routine Typing, Surveillance, and Outbreak Detection of Verotoxigenic Escherichia coli , 2014, Journal of Clinical Microbiology.

[41]  M. Holmes,et al.  The emergence of mecC methicillin-resistant Staphylococcus aureus , 2014, Trends in microbiology.

[42]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[43]  C. Walzer,et al.  Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. , 2013, The Journal of antimicrobial chemotherapy.

[44]  S. Monecke,et al.  The diversity of antimicrobial resistance genes among staphylococci of animal origin. , 2013, International journal of medical microbiology : IJMM.

[45]  J. Parkhill,et al.  Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC , 2013, EMBO molecular medicine.

[46]  A. Tomasz,et al.  Properties of a Novel PBP2A Protein Homolog from Staphylococcus aureus Strain LGA251 and Its Contribution to the β-Lactam-resistant Phenotype , 2012, The Journal of Biological Chemistry.

[47]  A. Tomasz,et al.  Guidelines for Reporting Novel mecA Gene Homologues , 2012, Antimicrobial Agents and Chemotherapy.

[48]  S. Rasmussen,et al.  Identification of acquired antimicrobial resistance genes , 2012, The Journal of antimicrobial chemotherapy.

[49]  P. Andersen,et al.  Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[50]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[51]  Christopher A. Miller,et al.  VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. , 2012, Genome research.

[52]  Ole Lund,et al.  Multilocus Sequence Typing of Total-Genome-Sequenced Bacteria , 2012, Journal of Clinical Microbiology.

[53]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[54]  Julian Parkhill,et al.  Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study , 2011, The Lancet. Infectious diseases.

[55]  S. Monecke,et al.  Detection of Staphylococcal Cassette Chromosome mec Type XI Carrying Highly Divergent mecA, mecI, mecR1, blaZ, and ccr Genes in Human Clinical Isolates of Clonal Complex 130 Methicillin-Resistant Staphylococcus aureus , 2011, Antimicrobial Agents and Chemotherapy.

[56]  K. Nagy,et al.  Detection of Staphylococcus aureus nasal carriage in healthy young adults from a Hungarian University. , 2011, Acta microbiologica et immunologica Hungarica.

[57]  Klaus Peter Schliep,et al.  phangorn: phylogenetic analysis in R , 2010, Bioinform..

[58]  J. Caron,et al.  Retrospective multicentre study of methicillin-resistant Staphylococcus aureus infections in 115 horses. , 2009, Equine veterinary journal.

[59]  M. Schijffelen,et al.  Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis , 2010, BMC Genomics.

[60]  J. Szabó,et al.  Phenotypic and genetic characterisation of methicillin-resistant Staphylococcus aureus strains isolated from the university hospitals of Debrecen , 2009, European Journal of Clinical Microbiology & Infectious Diseases.

[61]  W. Witte,et al.  Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. , 2008, Microbial drug resistance.

[62]  H. Goossens,et al.  Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. , 2007, The Journal of antimicrobial chemotherapy.

[63]  W. V. van Wamel,et al.  The Innate Immune Modulators Staphylococcal Complement Inhibitor and Chemotaxis Inhibitory Protein of Staphylococcus aureus Are Located on β-Hemolysin-Converting Bacteriophages , 2006, Journal of bacteriology.

[64]  J. Weese,et al.  Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. , 2005, Journal of the American Veterinary Medical Association.

[65]  J. Weese Methicillin-resistant Staphylococcus aureus: an emerging pathogen in small animals. , 2005, Journal of the American Animal Hospital Association.

[66]  Ronald N. Jones,et al.  Methicillin-Resistant Staphylococcus aureus Outbreak in a Veterinary Teaching Hospital: Potential Human-to-Animal Transmission , 1999, Journal of Clinical Microbiology.

[67]  A. Conde Staphylococcus aureus infections. , 1998, The New England journal of medicine.

[68]  T. Anzai,et al.  Genetic analysis of equine methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis. , 1997, The Journal of veterinary medical science.

[69]  F. Hartmann,et al.  Isolation of methicillin-resistant Staphylococcus aureus from a postoperative wound infection in a horse. , 1997, Journal of the American Veterinary Medical Association.