Molecular Epidemiology of Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus in Wild, Captive and Laboratory Rats: Effect of Habitat on the Nasal S. aureus Population

. 2020 Jan 24 ; 12 (2) : . [epub] 20200124

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31991690

Grantová podpora
ESF/14-BMA55-0037/16 European Social Fund - International
FKZ 03ZZ0806B Bundesministerium für Bildung und Forschung - International
01KI1727A Bundesministerium für Bildung und Forschung - International
TTU "emerging infections" Deutsches Zentrum für Infektionsforschung - International

Rats are a reservoir of human- and livestock-associated methicillin-resistant Staphylococcus aureus (MRSA). However, the composition of the natural S. aureus population in wild and laboratory rats is largely unknown. Here, 144 nasal S. aureus isolates from free-living wild rats, captive wild rats and laboratory rats were genotyped and profiled for antibiotic resistances and human-specific virulence genes. The nasal S. aureus carriage rate was higher among wild rats (23.4%) than laboratory rats (12.3%). Free-living wild rats were primarily colonized with isolates of clonal complex (CC) 49 and CC130 and maintained these strains even in husbandry. Moreover, upon livestock contact, CC398 isolates were acquired. In contrast, laboratory rats were colonized with many different S.aureus lineages-many of which are commonly found in humans. Five captive wild rats were colonized with CC398-MRSA. Moreover, a single CC30-MRSA and two CC130-MRSA were detected in free-living or captive wild rats. Rat-derived S. aureus isolates rarely harbored the phage-carried immune evasion gene cluster or superantigen genes, suggesting long-term adaptation to their host. Taken together, our study revealed a natural S. aureus population in wild rats, as well as a colonization pressure on wild and laboratory rats by exposure to livestock- and human-associated S.aureus, respectively.

CEITEC Central European Institute of Technology University of Veterinary and Pharmaceutical Sciences Brno 61242 Brno Czech Republic

Central Core and Research Facility of Laboratory Animals University Medicine Greifswald 17475 Greifswald Germany

Department of Ecology and Diseases of Game Fish and Bees University of Veterinary and Pharmaceutical Sciences Brno 61242 Brno Czech Republic

Department of Immunology University Medicine Greifswald 17475 Greifswald Germany

Department of Microbiology and Immunology Faculty of Pharmacy Alexandria University Alexandria 21521 Egypt

Friedrich Loeffler Institute Federal Research Institute for Animal Health Institute of Novel and Emerging Infectious Diseases 17493 Greifswald Insel Riems Germany

Friedrich Loeffler Institute of Medical Microbiology University Medicine Greifswald 17475 Greifswald Germany

German Cancer Research Center Microbiological Diagnostics 69120 Heidelberg Germany

German Center for Infection Research Partner Site Hamburg Lübeck Borstel Insel Riems 17493 Greifswald Insel Riems Germany

Institute for Medical Microbiology and Hygiene Technical University of Dresden 01307 Dresden Germany

Institute of Geoecology Landscape Ecology and Environmental Systems Analysis Technische Universität Braunschweig 38106 Braunschweig Germany

Institute of Medical Microbiology University Hospital Münster 48149 Münster Germany

Julius Kühn Institute Federal Research Centre for Cultivated Plants Institute for Plant Protection in Horticulture and Forestry Vertebrate Research 48161 Münster Germany

Leibniz Institute of Photonic Technology 07745 Jena Germany

National Reference Centre for Staphylococci and Enterococci Robert Koch Institute Wernigerode Branch 38855 Wernigerode Germany

Outpatient Clinic University of Potsdam 14469 Potsdam Germany

Research and Professional Services Charles River Laboratories Wilmington MA 01887 USA

von Opel Hessische Zoostiftung 61476 Kronberg im Taunus Germany

Zobrazit více v PubMed

Wertheim H.F.L., Melles D.C., Vos M.C., van Leeuwen W., van Belkum A., Verbrugh H.A., Nouwen J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005;5:751–762. doi: 10.1016/S1473-3099(05)70295-4. PubMed DOI

Kaspar U., Kriegeskorte A., Schubert T., Peters G., Rudack C., Pieper D.H., Wos-Oxley M., Becker K. The culturome of the human nose habitats reveals individual bacterial fingerprint patterns. Environ. Microbiol. 2016;18:2130–2142. doi: 10.1111/1462-2920.12891. PubMed DOI

Becker K., Schaumburg F., Fegeler C., Friedrich A.W., Köck R. Staphylococcus aureus from the German general population is highly diverse. Int. J. Med. Microbiol. 2017;307:21–27. doi: 10.1016/j.ijmm.2016.11.007. PubMed DOI

Tong S.Y.C., Davis J.S., Eichenberger E., Holland T.L., Fowler V.G. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 2015;28:603–661. doi: 10.1128/CMR.00134-14. PubMed DOI PMC

Aslam B., Wang W., Arshad M.I., Khurshid M., Muzammil S., Rasool M.H., Nisar M.A., Alvi R.F., Aslam M.A., Qamar M.U., et al. Antibiotic resistance: A rundown of a global crisis. Infect. Drug Resist. 2018;11:1645–1658. doi: 10.2147/IDR.S173867. PubMed DOI PMC

Martens E., Demain A.L. The antibiotic resistance crisis, with a focus on the United States. J. Antibiot. 2017;70:520–526. doi: 10.1038/ja.2017.30. PubMed DOI

McGuinness W.A., Malachowa N., DeLeo F.R. Vancomycin Resistance in Staphylococcus aureus. Yale J. Biol. Med. 2017;90:269–281. PubMed PMC

Redi D., Raffaelli C.S., Rossetti B., de Luca A., Montagnani F. Staphylococcus aureus vaccine preclinical and clinical development: Current state of the art. New Microbiol. 2018;41:208–213. PubMed

Harrison E.M., Weinert L.A., Holden M.T.G., Welch J.J., Wilson K., Morgan F.J.E., Harris S.R., Loeffler A., Boag A.K., Peacock S.J., et al. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. mBio. 2014;5:e00985-13. doi: 10.1128/mBio.00985-13. PubMed DOI PMC

Monecke S., Gavier-Widén D., Hotzel H., Peters M., Guenther S., Lazaris A., Loncaric I., Müller E., Reissig A., Ruppelt-Lorz A., et al. Diversity of Staphylococcus aureus Isolates in European Wildlife. PLoS ONE. 2016;11:e0168433. doi: 10.1371/journal.pone.0168433. PubMed DOI PMC

Mrochen D.M., Schulz D., Fischer S., Jeske K., El Gohary H., Reil D., Imholt C., Trübe P., Suchomel J., Tricaud E., et al. Wild rodents and shrews are natural hosts of Staphylococcus aureus. Int. J. Med. Microbiol. 2018;308:590–597. doi: 10.1016/j.ijmm.2017.09.014. PubMed DOI

Van Alen S., Ballhausen B., Peters G., Friedrich A.W., Mellmann A., Köck R., Becker K. In the centre of an epidemic: Fifteen years of LA-MRSA CC398 at the University Hospital Münster. Vet. Microbiol. 2017;200:19–24. doi: 10.1016/j.vetmic.2016.01.021. PubMed DOI

Köck R., Schaumburg F., Mellmann A., Köksal M., Jurke A., Becker K., Friedrich A.W. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS ONE. 2013;8:e55040. doi: 10.1371/journal.pone.0055040. PubMed DOI PMC

Pantosti A. Methicillin-Resistant Staphylococcus aureus Associated with Animals and Its Relevance to Human Health. Front. Microbiol. 2012;3:127. doi: 10.3389/fmicb.2012.00127. PubMed DOI PMC

Graveland H., Duim B., van Duijkeren E., Heederik D., Wagenaar J.A. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int. J. Med. Microbiol. 2011;301:630–634. doi: 10.1016/j.ijmm.2011.09.004. PubMed DOI

Rothenburger J.L., Himsworth C.G., La Perle K.M.D., Leighton F.A., Nemeth N.M., Treuting P.M., Jardine C.M. Pathology of wild Norway rats in Vancouver, Canada. J. Vet. Diagn. Investig. 2019;31:184–199. doi: 10.1177/1040638719833436. PubMed DOI PMC

Rothenburger J.L., Himsworth C.G., Nemeth N.M., Pearl D.L., Jardine C.M. Environmental Factors Associated with the Carriage of Bacterial Pathogens in Norway Rats. Ecohealth. 2018;15:82–95. doi: 10.1007/s10393-018-1313-x. PubMed DOI

Rothenburger J.L., Rousseau J.D., Weese J.S., Jardine C.M. Livestock-associated methicillin-resistant Staphylococcus aureus and Clostridium difficile in wild Norway rats (Rattus norvegicus) from Ontario swine farms. Can. J. Vet. Res. 2018;82:66–69. PubMed PMC

Himsworth C.G., Miller R.R., Montoya V., Hoang L., Romney M.G., Al-Rawahi G.N., Kerr T., Jardine C.M., Patrick D.M., Tang P., et al. Carriage of methicillin-resistant Staphylococcus aureus by wild urban Norway rats (Rattus norvegicus) PLoS ONE. 2014;9:e87983. doi: 10.1371/journal.pone.0087983. PubMed DOI PMC

Lee M.J., Byers K.A., Donovan C.M., Zabek E., Stephen C., Patrick D.M., Himsworth C.G. Methicillin-resistant Staphylococcus aureus in urban Norway rat (Rattus norvegicus) populations: Epidemiology and the impacts of kill-trapping. Zoonoses Public Health. 2019;66:343–348. doi: 10.1111/zph.12546. PubMed DOI

Van de Giessen A.W., van Santen-Verheuvel M.G., Hengeveld P.D., Bosch T., Broens E.M., Reusken C.B.E.M. Occurrence of methicillin-resistant Staphylococcus aureus in rats living on pig farms. Prev. Vet. Med. 2009;91:270–273. doi: 10.1016/j.prevetmed.2009.05.016. PubMed DOI

Bramble M., Morris D., Tolomeo P., Lautenbach E. Potential role of pet animals in household transmission of methicillin-resistant Staphylococcus aureus: A narrative review. Vector Borne Zoonotic Dis. 2011;11:617–620. doi: 10.1089/vbz.2010.0025. PubMed DOI PMC

De Aires Sousa M. Methicillin-resistant Staphylococcus aureus among animals: Current overview. Clin. Microbiol. Infect. 2017;23:373–380. doi: 10.1016/j.cmi.2016.11.002. PubMed DOI

Sakwinska O., Giddey M., Moreillon M., Morisset D., Waldvogel A., Moreillon P. Staphylococcus aureus host range and human-bovine host shift. Appl. Environ. Microbiol. 2011;77:5908–5915. doi: 10.1128/AEM.00238-11. PubMed DOI PMC

Peton V., Le Loir Y. Staphylococcus aureus in veterinary medicine. Infect. Genet. Evol. 2014;21:602–615. doi: 10.1016/j.meegid.2013.08.011. PubMed DOI

Destoumieux-Garzón D., Mavingui P., Boetsch G., Boissier J., Darriet F., Duboz P., Fritsch C., Giraudoux P., Le Roux F., Morand S., et al. The One Health Concept: 10 Years Old and a Long Road Ahead. Front. Vet. Sci. 2018;5:14. doi: 10.3389/fvets.2018.00014. PubMed DOI PMC

Lindsay J.A., Holden M.T.G. Staphylococcus aureus: Superbug, super genome? Trends Microbiol. 2004;12:378–385. doi: 10.1016/j.tim.2004.06.004. PubMed DOI

Lindsay J.A., Moore C.E., Day N.P., Peacock S.J., Witney A.A., Stabler R.A., Husain S.E., Butcher P.D., Hinds J. Microarrays Reveal that Each of the Ten Dominant Lineages of Staphylococcus aureus Has a Unique Combination of Surface-Associated and Regulatory Genes. J. Bacteriol. 2006;188:669–676. doi: 10.1128/JB.188.2.669-676.2006. PubMed DOI PMC

Xia G., Wolz C. Phages of Staphylococcus aureus and their impact on host evolution. Infect. Genet. Evol. 2014;21:593–601. doi: 10.1016/j.meegid.2013.04.022. PubMed DOI

Richardson E.J., Bacigalupe R., Harrison E.M., Weinert L.A., Lycett S., Vrieling M., Robb K., Hoskisson P.A., Holden M.T.G., Feil E.J., et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat. Ecol. Evol. 2018;2:1468–1478. doi: 10.1038/s41559-018-0617-0. PubMed DOI PMC

Viana D., Blanco J., Tormo-Más M.Á., Selva L., Guinane C.M., Baselga R., Corpa J.M., Lasa Í., Novick R.P., Fitzgerald J.R., et al. Adaptation of Staphylococcus aureus to ruminant and equine hosts involves SaPI-carried variants of von Willebrand factor-binding protein. Mol. Microbiol. 2010;77:1583–1594. doi: 10.1111/j.1365-2958.2010.07312.x. PubMed DOI

Cuny C., Abdelbary M., Layer F., Werner G., Witte W. Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet. Microbiol. 2015;177:219–223. doi: 10.1016/j.vetmic.2015.02.031. PubMed DOI

Viana D., Comos M., McAdam P.R., Ward M.J., Selva L., Guinane C.M., González-Muñoz B.M., Tristan A., Foster S.J., Fitzgerald J.R., et al. A single natural nucleotide mutation alters bacterial pathogen host tropism. Nat. Genet. 2015;47:361–366. doi: 10.1038/ng.3219. PubMed DOI PMC

Mrochen D.M., Grumann D., Schulz D., Gumz J., Trübe P., Pritchett-Corning K., Johnson S., Nicklas W., Kirsch P., Martelet K., et al. Global spread of mouse-adapted Staphylococcus aureus lineages CC1, CC15, and CC88 among mouse breeding facilities. Int. J. Med. Microbiol. 2018;308:598–606. doi: 10.1016/j.ijmm.2017.11.006. PubMed DOI

Lowder B.V., Guinane C.M., Ben Zakour N.L., Weinert L.A., Conway-Morris A., Cartwright R.A., Simpson A.J., Rambaut A., Nübel U., Fitzgerald J.R. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. Natl. Acad. Sci. USA. 2009;106:19545–19550. doi: 10.1073/pnas.0909285106. PubMed DOI PMC

Moodley A., Espinosa-Gongora C., Nielsen S.S., McCarthy A.J., Lindsay J.A., Guardabassi L. Comparative host specificity of human- and pig- associated Staphylococcus aureus clonal lineages. PLoS ONE. 2012;7:e49344. doi: 10.1371/journal.pone.0049344. PubMed DOI PMC

Walther B., Monecke S., Ruscher C., Friedrich A.W., Ehricht R., Slickers P., Soba A., Wleklinski C.-G., Wieler L.H., Lübke-Becker A. Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2009;47:704–710. doi: 10.1128/JCM.01626-08. PubMed DOI PMC

Vincze S., Stamm I., Monecke S., Kopp P.A., Semmler T., Wieler L.H., Lübke-Becker A., Walther B. Molecular analysis of human and canine Staphylococcus aureus strains reveals distinct extended-host-spectrum genotypes independent of their methicillin resistance. Appl. Environ. Microbiol. 2013;79:655–662. doi: 10.1128/AEM.02704-12. PubMed DOI PMC

Astrup L.B., Skovgaard K., Rasmussen R.S., Iburg T.M., Agerholm J.S., Aalbæk B., Jensen H.E., Nielsen O.L., Johansen F.F., Heegaard P.M.H., et al. Staphylococcus aureus infected embolic stroke upregulates Orm1 and Cxcl2 in a rat model of septic stroke pathology. Neurol. Res. 2019;41:399–412. doi: 10.1080/01616412.2019.1573455. PubMed DOI

Hanses F., Roux C., Dunman P.M., Salzberger B., Lee J.C. Staphylococcus aureus gene expression in a rat model of infective endocarditis. Genome Med. 2014;6:93. doi: 10.1186/PREACCEPT-4819325051343079. PubMed DOI PMC

Power M.E., Olson M.E., Domingue P.A.G., Costerton J.W. A rat model of Staphylococcus aureus chronic osteomyelitis that provides a suitable system for studying the human infection. J. Med. Microbiol. 1990;33:189–198. doi: 10.1099/00222615-33-3-189. PubMed DOI

Trübe P., Hertlein T., Mrochen D.M., Schulz D., Jorde I., Krause B., Zeun J., Fischer S., Wolf S.A., Walther B., et al. Bringing together what belongs together: Optimizing murine infection models by using mouse-adapted Staphylococcus aureus strains. Int. J. Med. Microbiol. 2019;309:26–38. doi: 10.1016/j.ijmm.2018.10.007. PubMed DOI

Sun Y., Emolo C., Holtfreter S., Wiles S., Kreiswirth B., Missiakas D., Schneewind O. Staphylococcal Protein A Contributes to Persistent Colonization of Mice with Staphylococcus aureus. J. Bacteriol. 2018;200 doi: 10.1128/JB.00735-17. PubMed DOI PMC

Holtfreter S., Grumann D., Balau V., Barwich A., Kolata J., Goehler A., Weiss S., Holtfreter B., Bauerfeind S.S., Döring P., et al. Molecular Epidemiology of Staphylococcus aureus in the General Population in Northeast Germany: Results of the Study of Health in Pomerania (SHIP-TREND-0) J. Clin. Microbiol. 2016;54:2774–2785. doi: 10.1128/JCM.00312-16. PubMed DOI PMC

Schulz D., Grumann D., Trübe P., Pritchett-Corning K., Johnson S., Reppschläger K., Gumz J., Sundaramoorthy N., Michalik S., Berg S., et al. Laboratory Mice Are Frequently Colonized with Staphylococcus aureus and Mount a Systemic Immune Response-Note of Caution for In vivo Infection Experiments. Front. Cell. Infect. Microbiol. 2017;7:152. doi: 10.3389/fcimb.2017.00152. PubMed DOI PMC

Sung J.M.-L., Lloyd D.H., Lindsay J.A. Staphylococcus aureus host specificity: Comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology. 2008;154:1949–1959. doi: 10.1099/mic.0.2007/015289-0. PubMed DOI

Van Wamel W.J.B., Rooijakkers S.H.M., Ruyken M., van Kessel K.P.M., van Strijp J.A.G. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 2006;188:1310–1315. doi: 10.1128/JB.188.4.1310-1315.2006. PubMed DOI PMC

Ruiz-Ripa L., Alcalá L., Simón C., Gómez P., Mama O.M., Rezusta A., Zarazaga M., Torres C. Diversity of Staphylococcus aureus clones in wild mammals in Aragon, Spain, with detection of MRSA ST130-mecC in wild rabbits. J. Appl. Microbiol. 2019;127:284–291. doi: 10.1111/jam.14301. PubMed DOI

Ruiz-Ripa L., Gómez P., Alonso C.A., Camacho M.C., de La Puente J., Fernández-Fernández R., Ramiro Y., Quevedo M.A., Blanco J.M., Zarazaga M., et al. Detection of MRSA of Lineages CC130-mecC and CC398-mecA and Staphylococcus delphini-lnu (A) in Magpies and Cinereous Vultures in Spain. Microb. Ecol. 2019;78:409–415. doi: 10.1007/s00248-019-01328-4. PubMed DOI

Ben Said M., Abbassi M.S., Gómez P., Ruiz-Ripa L., Sghaier S., El Fekih O., Hassen A., Torres C. Genetic characterization of Staphylococcus aureus isolated from nasal samples of healthy ewes in Tunisia. High prevalence of CC130 and CC522 lineages. Comp. Immunol. Microbiol. Infect. Dis. 2017;51:37–40. doi: 10.1016/j.cimid.2017.03.002. PubMed DOI

Simpson V.R., Davison N.J., Kearns A.M., Pichon B., Hudson L.O., Koylass M., Blackett T., Butler H., Rasigade J.P., Whatmore A.M. Association of a lukM-positive clone of Staphylococcus aureus with fatal exudative dermatitis in red squirrels (Sciurus vulgaris) Vet. Microbiol. 2013;162:987–991. doi: 10.1016/j.vetmic.2012.10.025. PubMed DOI

Simpson V., Davison N., Hudson L., Whatmore A.M. Staphylococcus aureus ST49 infection in red squirrels. Vet. Rec. 2010;167:69. doi: 10.1136/vr.c3625. PubMed DOI

Mama O.M., Ruiz-Ripa L., Fernández-Fernández R., González-Barrio D., Ruiz-Fons J.F., Torres C. High frequency of coagulase-positive staphylococci carriage in healthy wild boar with detection of MRSA of lineage ST398-t011. FEMS Microbiol. Lett. 2019;366 doi: 10.1093/femsle/fny292. PubMed DOI

Overesch G., Büttner S., Rossano A., Perreten V. The increase of methicillin-resistant Staphylococcus aureus (MRSA) and the presence of an unusual sequence type ST49 in slaughter pigs in Switzerland. BMC Vet. Res. 2011;7:30. doi: 10.1186/1746-6148-7-30. PubMed DOI PMC

Haenni M., Châtre P., Dupieux-Chabert C., Métayer V., Bes M., Madec J.-Y., Laurent F. Molecular Epidemiology of Methicillin-Resistant Staphylococcus aureus in Horses, Cats, and Dogs Over a 5-Year Period in France. Front. Microbiol. 2017;8:2493. doi: 10.3389/fmicb.2017.02493. PubMed DOI PMC

Deplano A., Vandendriessche S., Nonhoff C., Denis O. Genetic diversity among methicillin-resistant Staphylococcus aureus isolates carrying the mecC gene in Belgium. J. Antimicrob. Chemother. 2014;69:1457–1460. doi: 10.1093/jac/dku020. PubMed DOI

Witte W. Selective pressure by antibiotic use in livestock. Int. J. Antimicrob. Agents. 2000;16:19–24. doi: 10.1016/S0924-8579(00)00301-0. PubMed DOI

Lekshmi M., Ammini P., Kumar S., Varela M.F. The Food Production Environment and the Development of Antimicrobial Resistance in Human Pathogens of Animal Origin. Microorganisms. 2017;5:11. doi: 10.3390/microorganisms5010011. PubMed DOI PMC

Kadlec K., Entorf M., Peters T. Occurrence and Characteristics of Livestock-Associated Methicillin-Resistant Staphylococcus aureus in Quarter Milk Samples from Dairy Cows in Germany. Front. Microbiol. 2019;10:1295. doi: 10.3389/fmicb.2019.01295. PubMed DOI PMC

Köck R., Ballhausen B., Bischoff M., Cuny C., Eckmanns T., Fetsch A., Harmsen D., Goerge T., Oberheitmann B., Schwarz S., et al. The impact of zoonotic MRSA colonization and infection in Germany. Berl. Munch. Tierarztl. Wochenschr. 2014;127:384–398. PubMed

Guinane C.M., Ben Zakour N.L., Tormo-Mas M.A., Weinert L.A., Lowder B.V., Cartwright R.A., Smyth D.S., Smyth C.J., Lindsay J.A., Gould K.A., et al. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol. Evol. 2010;2:454–466. doi: 10.1093/gbe/evq031. PubMed DOI PMC

Messenger A.M., Barnes A.N., Gray G.C. Reverse zoonotic disease transmission (zooanthroponosis): A systematic review of seldom-documented human biological threats to animals. PLoS ONE. 2014;9:e89055. doi: 10.1371/journal.pone.0089055. PubMed DOI PMC

Tomas J., Langella P., Cherbuy C. The intestinal microbiota in the rat model: Major breakthroughs from new technologies. Anim. Health Res. Rev. 2012;13:54–63. doi: 10.1017/S1466252312000072. PubMed DOI

Mulcahy M.E., McLoughlin R.M. Host-Bacterial Crosstalk Determines Staphylococcus aureus Nasal Colonization. Trends Microbiol. 2016;24:872–886. doi: 10.1016/j.tim.2016.06.012. PubMed DOI

Zipperer A., Konnerth M.C., Laux C., Berscheid A., Janek D., Weidenmaier C., Burian M., Schilling N.A., Slavetinsky C., Marschal M., et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 2016;535:511–516. doi: 10.1038/nature18634. PubMed DOI

Piewngam P., Zheng Y., Nguyen T.H., Dickey S.W., Joo H.-S., Villaruz A.E., Glose K.A., Fisher E.L., Hunt R.L., Li B., et al. Pathogen elimination by probiotic Bacillus via signalling interference. Nature. 2018;562:532–537. doi: 10.1038/s41586-018-0616-y. PubMed DOI PMC

De Haas C.J.C., Veldkamp K.E., Peschel A., Weerkamp F., van Wamel W.J.B., Heezius E.C.J.M., Poppelier M.J.J.G., van Kessel K.P.M., van Strijp J.A.G. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J. Exp. Med. 2004;199:687–695. doi: 10.1084/jem.20031636. PubMed DOI PMC

Gladysheva I.P., Turner R.B., Sazonova I.Y., Liu L., Reed G.L. Coevolutionary patterns in plasminogen activation. Proc. Natl. Acad. Sci. USA. 2003;100:9168–9172. doi: 10.1073/pnas.1631716100. PubMed DOI PMC

Holtfreter S., Bröker B.M. Staphylococcal superantigens: Do they play a role in sepsis? Arch. Immunol. Ther. Exp. 2005;53:13–27. PubMed

Rooijakkers S.H.M., Ruyken M., Roos A., Daha M.R., Presanis J.S., Sim R.B., van Wamel W.J.B., van Kessel K.P.M., van Strijp J.A.G. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 2005;6:920–927. doi: 10.1038/ni1235. PubMed DOI

Hashimoto M., Watanabe S., Oiwa K., Ohta Y., Kishi T., Okamoto T., Giddings J.C., Yamamoto J. Enhanced thrombolysis induced by argatroban or activated protein C in the presence or absence of staphylokinase, measured in an in vivo animal model using mesenteric arterioles. Haemostasis. 2001;31:80–89. doi: 10.1159/000048048. PubMed DOI

Katayama Y., Baba T., Sekine M., Fukuda M., Hiramatsu K. Beta-hemolysin promotes skin colonization by Staphylococcus aureus. J. Bacteriol. 2013;195:1194–1203. doi: 10.1128/JB.01786-12. PubMed DOI PMC

Verkaik N.J., Benard M., Boelens H.A., de Vogel C.P., Nouwen J.L., Verbrugh H.A., Melles D.C., van Belkum A., van Wamel W.J.B. Immune evasion cluster-positive bacteriophages are highly prevalent among human Staphylococcus aureus strains, but they are not essential in the first stages of nasal colonization. Clin. Microbiol. Infect. 2011;17:343–348. doi: 10.1111/j.1469-0691.2010.03227.x. PubMed DOI

Markham N.P., Markham J.G. Staphylococci in man and animals. Distribution and characteristics of strains. J. Comp. Pathol. 1966;76:49–56. doi: 10.1016/0021-9975(66)90047-8. PubMed DOI

Grumann D., Scharf S.S., Holtfreter S., Kohler C., Steil L., Engelmann S., Hecker M., Völker U., Bröker B.M. Immune cell activation by enterotoxin gene cluster (egc)-encoded and non-egc superantigens from Staphylococcus aureus. J. Immunol. 2008;181:5054–5061. doi: 10.4049/jimmunol.181.7.5054. PubMed DOI

Holbrook M.R., Young K.E., Gibbon L.G., Webster C.A., Tranter H.S., Arbuthnott J.P., Todd I. Stimulation of rat spleen cells by staphylococcal enterotoxins. FEMS Immunol. Med. Microbiol. 1993;7:169–174. doi: 10.1111/j.1574-695X.1993.tb00396.x. PubMed DOI

Van Loo I., Huijsdens X., Tiemersma E., de Neeling A., van de Sande-Bruinsma N., Beaujean D., Voss A., Kluytmans J. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg. Infect. Dis. 2007;13:1834–1839. doi: 10.3201/eid1312.070384. PubMed DOI PMC

Becker K., Ballhausen B., Kahl B.C., Köck R. The clinical impact of livestock-associated methicillin-resistant Staphylococcus aureus of the clonal complex 398 for humans. Vet. Microbiol. 2017;200:33–38. doi: 10.1016/j.vetmic.2015.11.013. PubMed DOI

Gibbs S.G., Green C.F., Tarwater P.M., Mota L.C., Mena K.D., Scarpino P.V. Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ. Health Perspect. 2006;114:1032–1037. doi: 10.1289/ehp.8910. PubMed DOI PMC

Gibbs S.G., Green C.F., Tarwater P.M., Scarpino P.V. Airborne antibiotic resistant and nonresistant bacteria and fungi recovered from two swine herd confined animal feeding operations. J. Occup. Environ. Hyg. 2004;1:699–706. doi: 10.1080/15459620490515824. PubMed DOI

Himsworth C.G., Parsons K.L., Jardine C., Patrick D.M. Rats, cities, people, and pathogens: A systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis. 2013;13:349–359. doi: 10.1089/vbz.2012.1195. PubMed DOI

Wobeser G., Campbell G.D., Dallaire A., McBurney S. Tularemia, plague, yersiniosis, and Tyzzer’s disease in wild rodents and lagomorphs in Canada: A review. Can. Vet. J. 2009;50:1251–1256. PubMed PMC

Strand T.M., Lundkvist Å. Rat-borne diseases at the horizon. A systematic review on infectious agents carried by rats in Europe 1995–2016. Infect. Ecol. Epidemiol. 2019;9 doi: 10.1080/20008686.2018.1553461. PubMed DOI PMC

Taylor K.D. Range of Movement and Activity of Common Rats (Rattus norvegicus) on Agricultural Land. J. Appl. Ecol. 1978;15:663–677. doi: 10.2307/2402767. DOI

Reid R.A., Reid A.K. Route finding by rats in an open arena. Behav. Processes. 2005;68:51–67. doi: 10.1016/j.beproc.2004.11.004. PubMed DOI

Young D.M., Harris H.W., Charlebois E.D., Chambers H., Campbell A., Perdreau-Remington F., Lee C., Mankani M., Mackersie R., Schecter W.P. An epidemic of methicillin-resistant Staphylococcus aureus soft tissue infections among medically underserved patients. Arch. Surg. 2004;139:947–951. doi: 10.1001/archsurg.139.9.947. PubMed DOI

Luedicke C., Slickers P., Ehricht R., Monecke S. Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur. J. Clin. Microbiol. Infect. Dis. 2010;29:457–463. doi: 10.1007/s10096-010-0884-4. PubMed DOI

Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., et al. Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in livestock. mBio. 2012;3:e00305-11. doi: 10.1128/mBio.00305-11. PubMed DOI PMC

Van Alen S., Ballhausen B., Kaspar U., Köck R., Becker K. Prevalence and Genomic Structure of Bacteriophage phi3 in Human-Derived Livestock-Associated Methicillin-Resistant Staphylococcus aureus Isolates from 2000 to 2015. J. Clin. Microbiol. 2018;56 doi: 10.1128/JCM.00140-18. PubMed DOI PMC

Spahr C., Knauf-Witzens T., Vahlenkamp T., Ulrich R.G., Johne R. Hepatitis E virus and related viruses in wild, domestic and zoo animals: A review. Zoonoses Public Health. 2018;65:11–29. doi: 10.1111/zph.12405. PubMed DOI

Holtfreter S., Bauer K., Thomas D., Feig C., Lorenz V., Roschack K., Friebe E., Selleng K., Lövenich S., Greve T., et al. egc-Encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect. Immun. 2004;72:4061–4071. doi: 10.1128/IAI.72.7.4061-4071.2004. PubMed DOI PMC

Holtfreter S., Grumann D., Schmudde M., Nguyen H.T.T., Eichler P., Strommenger B., Kopron K., Kolata J., Giedrys-Kalemba S., Steinmetz I., et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J. Clin. Microbiol. 2007;45:2669–2680. doi: 10.1128/JCM.00204-07. PubMed DOI PMC

Völzke H., Alte D., Schmidt C.O., Radke D., Lorbeer R., Friedrich N., Aumann N., Lau K., Piontek M., Born G., et al. Cohort profile: The study of health in Pomerania. Int. J. Epidemiol. 2011;40:294–307. doi: 10.1093/ije/dyp394. PubMed DOI

Zhang K., Sparling J., Chow B.L., Elsayed S., Hussain Z., Church D.L., Gregson D.B., Louie T., Conly J.M. New Quadriplex PCR Assay for Detection of Methicillin and Mupirocin Resistance and Simultaneous Discrimination of Staphylococcus aureus from Coagulase-Negative Staphylococci. J. Clin. Microbiol. 2004;42:4947–4955. doi: 10.1128/JCM.42.11.4947-4955.2004. PubMed DOI PMC

Strommenger B., Kettlitz C., Weniger T., Harmsen D., Friedrich A.W., Witte W. Assignment of Staphylococcus Isolates to Groups by spa Typing, SmaI Macrorestriction Analysis, and Multilocus Sequence Typing. J. Clin. Microbiol. 2006;44:2533–2540. doi: 10.1128/JCM.00420-06. PubMed DOI PMC

Enright M.C., Day N.P., Davies C.E., Peacock S.J., Spratt B.G. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 2000;38:1008–1015. doi: 10.1128/JCM.38.3.1008-1015.2000. PubMed DOI PMC

Harmsen D., Claus H., Witte W., Rothgänger J., Claus H., Turnwald D., Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J. Clin. Microbiol. 2003;41:5442–5448. doi: 10.1128/JCM.41.12.5442-5448.2003. PubMed DOI PMC

Goerke C., Pantucek R., Holtfreter S., Schulte B., Zink M., Grumann D., Bröker B.M., Doskar J., Wolz C. Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J. Bacteriol. 2009;191:3462–3468. doi: 10.1128/JB.01804-08. PubMed DOI PMC

Jean B., Mpw P., Eliopoulos G.M., Jenkins S.G. M100: Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI; Wayne, PA, USA: 2018.

Schwendener S., Cotting K., Perreten V. Novel methicillin resistance gene mecD in clinical Macrococcus caseolyticus strains from bovine and canine sources. Sci. Rep. 2017;7:43797. doi: 10.1038/srep43797. PubMed DOI PMC

Cuny C., Layer F., Strommenger B., Witte W. Rare occurrence of methicillin-resistant Staphylococcus aureus CC130 with a novel mecA homologue in humans in Germany. PLoS ONE. 2011;6:e24360. doi: 10.1371/journal.pone.0024360. PubMed DOI PMC

Becker K., van Alen S., Idelevich E.A., Schleimer N., Seggewiß J., Mellmann A., Kaspar U., Peters G. Plasmid-Encoded Transferable mecB-Mediated Methicillin Resistance in Staphylococcus aureus. Emerg. Infect. Dis. 2018;24:242–248. doi: 10.3201/eid2402.171074. PubMed DOI PMC

Sperber W.H., Tatini S.R. Interpretation of the Tube Coagulase Test for Identification of Staphylococcus aureus. Appl. Microbiol. 1975;29:502–505. doi: 10.1128/AEM.29.4.502-505.1975. PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Staphylococcus ratti sp. nov. Isolated from a Lab Rat

. 2022 Jan 01 ; 11 (1) : . [epub] 20220101

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace