FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Toxins (Basel) / Molecular Characterization of Equine Staphylococcus aureus I...
Toxins2019; 11(9); 535; doi: 10.3390/toxins11090535

Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility.

Abstract: The detection of borderline oxacillin-resistant (BORSA) represents a challenge to both, veterinary and human laboratories. Between 2015 and 2017, 19 equine with elevated minimal inhibitory concentrations for oxacillin were detected in routine diagnostics. The aim of this study was to characterize these isolates to identify factors possibly associated with the BORSA phenotype. All were subjected to antimicrobial susceptibility testing and whole genome sequencing (WGS). A quantifiable β-lactamase activity assay was performed for a representative subset of 13 isolates. The WGS data analysis of the 19 BORSA isolates identified two different genomic lineages, sequence type (ST) 1 and ST1660. The core genome multilocus sequence typing (cgMLST) revealed a close relatedness of all isolates belonging to either ST1 or ST1660. The WGS analysis identified the resistance genes , , (L), and/or and Phenotypic resistance to penicillins, aminoglycosides, tetracyclines, fluoroquinolones and sulfamethoxazole/trimethoprim was observed in the respective isolates. For the penicillin-binding proteins 1-4, amino acid substitutions were predicted using WGS data. Since neither transglycosylase nor transpeptidase domains were affected, these alterations might not explain the BORSA phenotype. Moreover, β-lactamase activity was found to be associated with an inducible gene. The lineage-specific differences regarding the expression profiles were noted.
Get Full Text
Publication Date: 2019-09-13 PubMed ID: 31540335PubMed Central: PMC6783909DOI: 10.3390/toxins11090535Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research studies borderline oxacillin-resistant Staphylococcus aureus (BORSA) in horses, examining the related genetic factors and resistance profiles through whole genome sequencing and other techniques.

Background

  • Staphylococcus aureus is a type of bacteria often found in horses. Some of these bacteria have developed resistance to certain antibiotics, including oxacillin.
  • Between 2015 and 2017, the researchers identified 19 such borderline oxacillin-resistant Staphylococcus aureus (BORSA) in routine diagnostics.
  • The research’s goal was to characterize these isolates and identify any factors that might be associated with the BORSA phenotype, which refers to the observable traits and characteristics of the bacteria.

Methods

  • All 19 isolates were put through antimicrobial susceptibility testing and whole-genome sequencing (WGS).
  • A β-lactamase activity assay was also performed on a representative sub-group of 13 of these isolates. β-lactamase is an enzyme produced by bacteria that can break down antibiotics and resist them.

Findings

  • The whole genome sequencing data analysis revealed two distinct genomic lineages, sequence type (ST) 1 and ST1660.
  • The core genome multilocus sequence typing showed a close relatedness of all isolates that belonged to either ST1 or ST1660.
  • The researchers identified resistance genes in the whole genome sequencing analysis.
  • Phenotypic resistance to common drugs like penicillins, aminoglycosides, tetracyclines, fluoroquinolones, and sulfamethoxazole/trimethoprim was observed in some tested isolates.
  • Whole genome sequencing data predicted amino acid substitutions for proteins 1-4 that bind with penicillin. No transglycosylase or transpeptidase domains were affected, suggesting these changes might not explain the BORSA phenotype.
  • The research found β-lactamase activity to be associated with an inducible gene. The differences in expression profiles were also found to depend on lineage.

Significance

  • The study adds to our knowledge about antibiotic-resistant bacteria, particularly the borderline oxacillin-resistant Staphylococcus aureus.
  • The findings might provide important insights for effective antibiotic selection when treating infections in horses.
  • The research also highlights the significance of further investigations into the interplay between genetic and phenotypic factors in determining antibiotic resistance.

Cite This Article

APA
Scholtzek AD, Hanke D, Walther B, Eichhorn I, Stöckle SD, Klein KS, Gehlen H, Lübke-Becker A, Schwarz S, Feßler AT. (2019). Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility. Toxins (Basel), 11(9), 535. https://doi.org/10.3390/toxins11090535

Publication

Toxins
ISSN: 2072-6651
NlmUniqueID: 101530765
Country: Switzerland
Language: English
Volume: 11
Issue: 9
PII: 535

Researcher Affiliations

Scholtzek, Anissa D
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. anissa.scholtzek@fu-berlin.de.
Hanke, Dennis
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. dennis.hanke@fu-berlin.de.
Walther, Birgit
  • Advanced Light and Electron Microscopy (ZBS-4), Robert Koch Institute, 13353 Berlin, Germany. waltherb@rki.de.
Eichhorn, Inga
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. inga.eichhorn@fu-berlin.de.
Stöckle, Sabita D
  • Equine Clinic: Surgery and Radiology, Freie Universität Berlin, 14163 Berlin, Germany. sabita.d.stoeckle@fu-berlin.de.
Klein, Katja-Sophia
  • Equine Clinic: Surgery and Radiology, Freie Universität Berlin, 14163 Berlin, Germany. katjasophia.klein@gmail.com.
Gehlen, Heidrun
  • Equine Clinic: Surgery and Radiology, Freie Universität Berlin, 14163 Berlin, Germany. heidrun.gehlen@fu-berlin.de.
Lübke-Becker, Antina
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. antina.luebke-becker@fu-berlin.de.
Schwarz, Stefan
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. stefan.schwarz@fu-berlin.de.
Feßler, Andrea T
  • Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany. andrea.fessler@fu-berlin.de.

MeSH Terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Drug Resistance, Bacterial / genetics
  • Horse Diseases / microbiology
  • Horses
  • Microbial Sensitivity Tests
  • Oxacillin / pharmacology
  • Phylogeny
  • Staphylococcal Infections / microbiology
  • Staphylococcal Infections / veterinary
  • Staphylococcus aureus / genetics
  • Staphylococcus aureus / isolation & purification
  • Staphylococcus aureus / metabolism
  • Virulence Factors / genetics
  • beta-Lactamases / metabolism

Conflict of Interest Statement

The authors declare no conflict of interest

References

This article includes 87 references
  1. Schwarz S, Feßler A T, Loncaric I, Wu C, Kadlec K, Wang Y, Shen J. Antimicrobial resistance among staphylococci of animal origin. Antimicrobial Resistance in Bacteria from Livestock and Companion Animals 1st ed. American Society for Microbiology; Washington, DC, USA: 2018. pp. 127–157.
  2. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management.. Clin Microbiol Rev 2015 Jul;28(3):603-61.
    doi: 10.1128/CMR.00134-14pmc: PMC4451395pubmed: 26016486google scholar: lookup
  3. Oliveira D, Borges A, Simões M. Staphylococcus aureus Toxins and Their Molecular Activity in Infectious Diseases.. Toxins (Basel) 2018 Jun 19;10(6).
    doi: 10.3390/toxins10060252pmc: PMC6024779pubmed: 29921792google scholar: lookup
  4. Gudiol C, Cuervo G, Shaw E, Pujol M, Carratalà J. Pharmacotherapeutic options for treating Staphylococcus aureus bacteremia.. Expert Opin Pharmacother 2017 Dec;18(18):1947-1963.
    doi: 10.1080/14656566.2017.1403585pubmed: 29115883google scholar: lookup
  5. Khan A, Wilson B, Gould IM. Current and future treatment options for community-associated MRSA infection.. Expert Opin Pharmacother 2018 Apr;19(5):457-470.
    doi: 10.1080/14656566.2018.1442826pubmed: 29480032google scholar: lookup
  6. Kaspar U, von Lützau K, Schlattmann A, Rösler U, Köck R, Becker K. Zoonotic multidrug-resistant microorganisms among non-hospitalized horses from Germany.. One Health 2019 Jun;7:100091.
    doi: 10.1016/j.onehlt.2019.100091pmc: PMC6468158pubmed: 31016221google scholar: lookup
  7. Bino E, Lauková A, Ščerbová J, Kubašová I, Kandričáková A, Strompfová V, Miltko R, Belzecki G. Fecal coagulase-negative staphylococci from horses, their species variability, and biofilm formation.. Folia Microbiol (Praha) 2019 Nov;64(6):719-726.
    doi: 10.1007/s12223-019-00684-5pubmed: 30706301google scholar: lookup
  8. Fouché N, Gerber V, Thomann A, Perreten V. Antimicrobial susceptibility patterns of blood culture isolates from foals in Switzerland.. Schweiz Arch Tierheilkd 2018 Nov;160(11):665-671.
    doi: 10.17236/sat00184pubmed: 30379134google scholar: lookup
  9. Schnellmann C, Gerber V, Rossano A, Jaquier V, Panchaud Y, Doherr MG, Thomann A, Straub R, Perreten V. Presence of new mecA and mph(C) variants conferring antibiotic resistance in Staphylococcus spp. isolated from the skin of horses before and after clinic admission.. J Clin Microbiol 2006 Dec;44(12):4444-54.
    doi: 10.1128/JCM.00868-06pmc: PMC1698435pubmed: 17005735google scholar: lookup
  10. Schwarz S, Roberts MC, Werckenthin C, Pang Y, Lange C. Tetracycline resistance in Staphylococcus spp. from domestic animals.. Vet Microbiol 1998 Oct;63(2-4):217-27.
    doi: 10.1016/S0378-1135(98)00234-Xpubmed: 9851000google scholar: lookup
  11. Cuny C, Witte W. MRSA in equine hospitals and its significance for infections in humans.. Vet Microbiol 2017 Feb;200:59-64.
    doi: 10.1016/j.vetmic.2016.01.013pubmed: 26869097google scholar: lookup
  12. Waqar N, Amin Q, Munir T, Ikram MS, Shahzad N, Mirza A, Ali A, Arshad MI. A cross-sectional study of methicillin-resistant Staphylococcus aureus at the equine-human interface.. Trop Anim Health Prod 2019 Sep;51(7):1927-1933.
    doi: 10.1007/s11250-019-01888-0pubmed: 30972624google scholar: lookup
  13. Walther B, Klein KS, Barton AK, Semmler T, Huber C, Merle R, Tedin K, Mitrach F, Lübke-Becker A, Gehlen H. Equine Methicillin-Resistant Sequence Type 398 Staphylococcus aureus (MRSA) Harbor Mobile Genetic Elements Promoting Host Adaptation.. Front Microbiol 2018;9:2516.
    doi: 10.3389/fmicb.2018.02516pmc: PMC6207647pubmed: 30405574google scholar: lookup
  14. Köck R, Cuny C. [Multidrug-resistant bacteria in animals and humans].. Med Klin Intensivmed Notfmed 2020 Apr;115(3):189-197.
    doi: 10.1007/s00063-018-0487-xpubmed: 30276566google scholar: lookup
  15. Aires-de-Sousa M. Methicillin-resistant Staphylococcus aureus among animals: current overview.. Clin Microbiol Infect 2017 Jun;23(6):373-380.
    doi: 10.1016/j.cmi.2016.11.002pubmed: 27851997google scholar: lookup
  16. Hryniewicz MM, Garbacz K. Borderline oxacillin-resistant Staphylococcus aureus (BORSA) - a more common problem than expected?. J Med Microbiol 2017 Oct;66(10):1367-1373.
    doi: 10.1099/jmm.0.000585pubmed: 28893360google scholar: lookup
  17. Becker K, van Alen S, Idelevich EA, Schleimer N, Seggewiß J, Mellmann A, Kaspar U, Peters G. Plasmid-Encoded Transferable mecB-Mediated Methicillin Resistance in Staphylococcus aureus.. Emerg Infect Dis 2018 Feb;24(2):242-248.
    doi: 10.3201/eid2402.171074pmc: PMC5782906pubmed: 29350135google scholar: lookup
  18. Pantosti A. Methicillin-Resistant Staphylococcus aureus Associated with Animals and Its Relevance to Human Health.. Front Microbiol 2012;3:127.
    doi: 10.3389/fmicb.2012.00127pmc: PMC3321498pubmed: 22509176google scholar: lookup
  19. Köck R, Schaumburg F, Mellmann A, Köksal M, Jurke A, Becker K, Friedrich AW. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany.. PLoS One 2013;8(2):e55040.
    doi: 10.1371/journal.pone.0055040pmc: PMC3572123pubmed: 23418434google scholar: lookup
  20. van Duijkeren E, Moleman M, Sloet van Oldruitenborgh-Oosterbaan MM, Multem J, Troelstra A, Fluit AC, van Wamel WJ, Houwers DJ, de Neeling AJ, Wagenaar JA. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks.. Vet Microbiol 2010 Feb 24;141(1-2):96-102.
    doi: 10.1016/j.vetmic.2009.08.009pubmed: 19740613google scholar: lookup
  21. Sieber S, Gerber V, Jandova V, Rossano A, Evison JM, Perreten V. Evolution of multidrug-resistant Staphylococcus aureus infections in horses and colonized personnel in an equine clinic between 2005 and 2010.. Microb Drug Resist 2011 Sep;17(3):471-8.
    doi: 10.1089/mdr.2010.0188pubmed: 21875361google scholar: lookup
  22. Abdelbary MM, Wittenberg A, Cuny C, Layer F, Kurt K, Wieler LH, Walther B, Skov R, Larsen J, Hasman H, Fitzgerald JR, Smith TC, Wagenaar JA, Pantosti A, Hallin M, Struelens MJ, Edwards G, Böse R, Nübel U, Witte W. Phylogenetic analysis of Staphylococcus aureus CC398 reveals a sub-lineage epidemiologically associated with infections in horses.. PLoS One 2014;9(2):e88083.
    doi: 10.1371/journal.pone.0088083pmc: PMC3913741pubmed: 24505386google scholar: lookup
  23. Vincze S, Stamm I, Kopp PA, Hermes J, Adlhoch C, Semmler T, Wieler LH, Lübke-Becker A, Walther B. Alarming proportions of methicillin-resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012.. PLoS One 2014;9(1):e85656.
    doi: 10.1371/journal.pone.0085656pmc: PMC3896405pubmed: 24465637google scholar: lookup
  24. Maddox TW, Clegg PD, Williams NJ, Pinchbeck GL. Antimicrobial resistance in bacteria from horses: Epidemiology of antimicrobial resistance.. Equine Vet J 2015 Nov;47(6):756-65.
    doi: 10.1111/evj.12471pubmed: 26084443google scholar: lookup
  25. Cuny C, Abdelbary MMH, Köck R, Layer F, Scheidemann W, Werner G, Witte W. Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans.. One Health 2016 Dec;2:11-17.
    doi: 10.1016/j.onehlt.2015.11.004pmc: PMC5441336pubmed: 28616471google scholar: lookup
  26. Islam MZ, Espinosa-Gongora C, Damborg P, Sieber RN, Munk R, Husted L, Moodley A, Skov R, Larsen J, Guardabassi L. Horses in Denmark Are a Reservoir of Diverse Clones of Methicillin-Resistant and -Susceptible Staphylococcus aureus.. Front Microbiol 2017;8:543.
    doi: 10.3389/fmicb.2017.00543pmc: PMC5376617pubmed: 28421046google scholar: lookup
  27. Loncaric I, Lepuschitz S, Ruppitsch W, Trstan A, Andreadis T, Bouchlis N, Marbach H, Schauer B, Szostak MP, Feßler AT, Künzel F, Licka T, Springer B, Allerberger F, Monecke S, Ehricht R, Schwarz S, Spergser J. Increased genetic diversity of methicillin-resistant Staphylococcus aureus (MRSA) isolated from companion animals.. Vet Microbiol 2019 Aug;235:118-126.
    doi: 10.1016/j.vetmic.2019.06.013pubmed: 31282369google scholar: lookup
  28. DANMAP. Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Food and Humans in Denmark. DANMAP Statens Serum Institute; Copenhagen, Denmark: 2017.
  29. Toleman MS, Reuter S, Jamrozy D, Wilson HJ, Blane B, Harrison EM, Coll F, Hope RJ, Kearns A, Parkhill J, Peacock SJ, Török ME. Prospective genomic surveillance of methicillin-resistant Staphylococcus aureus (MRSA) associated with bloodstream infection, England, 1 October 2012 to 30 September 2013.. Euro Surveill 2019 Jan;24(4).
    doi: 10.2807/1560-7917.ES.2019.24.4.1800215pmc: PMC6351993pubmed: 30696529google scholar: lookup
  30. Pérez-Montarelo D, Viedma E, Larrosa N, Gómez-González C, Ruiz de Gopegui E, Muñoz-Gallego I, San Juan R, Fernández-Hidalgo N, Almirante B, Chaves F. Molecular Epidemiology of Staphylococcus aureus Bacteremia: Association of Molecular Factors With the Source of Infection.. Front Microbiol 2018;9:2210.
    doi: 10.3389/fmicb.2018.02210pmc: PMC6167439pubmed: 30319561google scholar: lookup
  31. Elstrøm P, Grøntvedt CA, Gabrielsen C, Stegger M, Angen Ø, Åmdal S, Enger H, Urdahl AM, Jore S, Steinbakk M, Sunde M. Livestock-Associated MRSA CC1 in Norway; Introduction to Pig Farms, Zoonotic Transmission, and Eradication.. Front Microbiol 2019;10:139.
    doi: 10.3389/fmicb.2019.00139pmc: PMC6376739pubmed: 30800102google scholar: lookup
  32. Güven Gökmen T, Kalayci Y, Yaman A, Köksal F. Molecular characterization of methicillin-resistant Staphylococcus aureus strains by spa typing and pulsed field gel electrophoresis methods.. BMC Microbiol 2018 Oct 24;18(1):155.
    doi: 10.1186/s12866-018-1305-6pmc: PMC6201486pubmed: 30355342google scholar: lookup
  33. Manara S, Pasolli E, Dolce D, Ravenni N, Campana S, Armanini F, Asnicar F, Mengoni A, Galli L, Montagnani C, Venturini E, Rota-Stabelli O, Grandi G, Taccetti G, Segata N. Whole-genome epidemiology, characterisation, and phylogenetic reconstruction of Staphylococcus aureus strains in a paediatric hospital.. Genome Med 2018 Nov 13;10(1):82.
    doi: 10.1186/s13073-018-0593-7pmc: PMC6234625pubmed: 30424799google scholar: lookup
  34. Serra R, Grande R, Butrico L, Rossi A, Settimio UF, Caroleo B, Amato B, Gallelli L, de Franciscis S. Chronic wound infections: the role of Pseudomonas aeruginosa and Staphylococcus aureus.. Expert Rev Anti Infect Ther 2015 May;13(5):605-13.
    doi: 10.1586/14787210.2015.1023291pubmed: 25746414google scholar: lookup
  35. Sisirak M, Zvizdic A, Hukic M. Methicillin-resistant Staphylococcus aureus (MRSA) as a cause of nosocomial wound infections.. Bosn J Basic Med Sci 2010 Feb;10(1):32-7.
    doi: 10.17305/bjbms.2010.2733pmc: PMC5596608pubmed: 20192928google scholar: lookup
  36. Hardy K, Sunnucks K, Gil H, Shabir S, Trampari E, Hawkey P, Webber M. Increased Usage of Antiseptics Is Associated with Reduced Susceptibility in Clinical Isolates of Staphylococcus aureus.. mBio 2018 May 29;9(3).
    doi: 10.1128/mBio.00894-18pmc: PMC5974466pubmed: 29844113google scholar: lookup
  37. Feßler AT, Schug AR, Geber F, Scholtzek AD, Merle R, Brombach J, Hensel V, Meurer M, Michael GB, Reinhardt M, Speck S, Truyen U, Schwarz S. Development and evaluation of a broth macrodilution method to determine the biocide susceptibility of bacteria.. Vet Microbiol 2018 Sep;223:59-64.
    doi: 10.1016/j.vetmic.2018.07.006pubmed: 30173753google scholar: lookup
  38. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Clinical and Laboratory Standards Institute 4th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2018. CLSI supplement VET08. (Print) (Electronic).
  39. CLSI. Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute 29th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2019. CLSI supplement M100. [Print] [Electronic].
  40. Watanabe S, Ito T, Hiramatsu K. Susceptibilities of healthcare- and community-associated methicillin-resistant staphylococci to the novel des-F(6)-quinolone DX-619.. J Antimicrob Chemother 2007 Dec;60(6):1384-7.
    doi: 10.1093/jac/dkm361pubmed: 17890283google scholar: lookup
  41. Hauschild T, Fessler AT, Billerbeck C, Wendlandt S, Kaspar H, Mankertz J, Schwarz S, Kadlec K. Target gene mutations among methicillin-resistant Staphylococcus aureus and methicillin-susceptible S. aureus with elevated MICs of enrofloxacin obtained from diseased food-producing animals or food of animal origin.. J Antimicrob Chemother 2012 Jul;67(7):1791-3.
    doi: 10.1093/jac/dks104pubmed: 22457312google scholar: lookup
  42. Berger-Bächi B, Tschierske M. Role of fem factors in methicillin resistance.. Drug Resist Updat 1998;1(5):325-35.
    doi: 10.1016/S1368-7646(98)80048-4pubmed: 17092813google scholar: lookup
  43. Seidl K, Stucki M, Ruegg M, Goerke C, Wolz C, Harris L, Berger-Bächi B, Bischoff M. Staphylococcus aureus CcpA affects virulence determinant production and antibiotic resistance.. Antimicrob Agents Chemother 2006 Apr;50(4):1183-94.
    doi: 10.1128/AAC.50.4.1183-1194.2006pmc: PMC1426959pubmed: 16569828google scholar: lookup
  44. Sadykov MR, Hartmann T, Mattes TA, Hiatt M, Jann NJ, Zhu Y, Ledala N, Landmann R, Herrmann M, Rohde H, Bischoff M, Somerville GA. CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis.. Microbiology (Reading) 2011 Dec;157(Pt 12):3458-3468.
    doi: 10.1099/mic.0.051243-0pmc: PMC3352278pubmed: 21964732google scholar: lookup
  45. Griffiths JM, O'Neill AJ. Loss of function of the gdpP protein leads to joint β-lactam/glycopeptide tolerance in Staphylococcus aureus.. Antimicrob Agents Chemother 2012 Jan;56(1):579-81.
    doi: 10.1128/AAC.05148-11pmc: PMC3256080pubmed: 21986827google scholar: lookup
  46. Argudín MA, Roisin S, Nienhaus L, Dodémont M, de Mendonça R, Nonhoff C, Deplano A, Denis O. Genetic Diversity among Staphylococcus aureus Isolates Showing Oxacillin and/or Cefoxitin Resistance Not Linked to the Presence of mec Genes.. Antimicrob Agents Chemother 2018 Jul;62(7).
    doi: 10.1128/AAC.00091-18pmc: PMC6021684pubmed: 29661881google scholar: lookup
  47. Commichau FM, Heidemann JL, Ficner R, Stülke J. Making and Breaking of an Essential Poison: the Cyclases and Phosphodiesterases That Produce and Degrade the Essential Second Messenger Cyclic di-AMP in Bacteria.. J Bacteriol 2019 Jan 1;201(1).
    doi: 10.1128/JB.00462-18pmc: PMC6287462pubmed: 30224435google scholar: lookup
  48. Huynh TN, Woodward JJ. Too much of a good thing: regulated depletion of c-di-AMP in the bacterial cytoplasm.. Curr Opin Microbiol 2016 Apr;30:22-29.
    doi: 10.1016/j.mib.2015.12.007pmc: PMC4821758pubmed: 26773214google scholar: lookup
  49. Uddin MJ, Ahn J. Associations between resistance phenotype and gene expression in response to serial exposure to oxacillin and ciprofloxacin in Staphylococcus aureus.. Lett Appl Microbiol 2017 Dec;65(6):462-468.
    doi: 10.1111/lam.12808pubmed: 28977678google scholar: lookup
  50. Chen FJ, Lauderdale TL, Lee CH, Hsu YC, Huang IW, Hsu PC, Yang CS. Effect of a Point Mutation in mprF on Susceptibility to Daptomycin, Vancomycin, and Oxacillin in an MRSA Clinical Strain.. Front Microbiol 2018;9:1086.
    doi: 10.3389/fmicb.2018.01086pmc: PMC5980971pubmed: 29887848google scholar: lookup
  51. Rowland SJ, Dyke KG. Tn552, a novel transposable element from Staphylococcus aureus.. Mol Microbiol 1990 Jun;4(6):961-75.
    doi: 10.1111/j.1365-2958.1990.tb00669.xpubmed: 2170815google scholar: lookup
  52. Vincze S. Staphylococcus aureus in Companion Animals: An Infection Source for the Community?. Ph.D. Thesis. Freie Universität Berlin; Berlin, Germany: 2015.
  53. Gharsa H, Ben Sallem R, Ben Slama K, Gómez-Sanz E, Lozano C, Jouini A, Klibi N, Zarazaga M, Boudabous A, Torres C. High diversity of genetic lineages and virulence genes in nasal Staphylococcus aureus isolates from donkeys destined to food consumption in Tunisia with predominance of the ruminant associated CC133 lineage.. BMC Vet Res 2012 Oct 29;8:203.
    doi: 10.1186/1746-6148-8-203pmc: PMC3538696pubmed: 23107174google scholar: lookup
  54. Battisti A, Franco A, Merialdi G, Hasman H, Iurescia M, Lorenzetti R, Feltrin F, Zini M, Aarestrup FM. Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings.. Vet Microbiol 2010 May 19;142(3-4):361-6.
    doi: 10.1016/j.vetmic.2009.10.008pubmed: 19914010google scholar: lookup
  55. Franco A, Hasman H, Iurescia M, Lorenzetti R, Stegger M, Pantosti A, Feltrin F, Ianzano A, Porrero MC, Liapi M, Battisti A. Molecular characterization of spa type t127, sequence type 1 methicillin-resistant Staphylococcus aureus from pigs.. J Antimicrob Chemother 2011 Jun;66(6):1231-5.
    doi: 10.1093/jac/dkr115pubmed: 21447518google scholar: lookup
  56. Alba P, Feltrin F, Cordaro G, Porrero MC, Kraushaar B, Argudín MA, Nykäsenoja S, Monaco M, Stegger M, Aarestrup FM, Butaye P, Franco A, Battisti A. Livestock-Associated Methicillin Resistant and Methicillin Susceptible Staphylococcus aureus Sequence Type (CC)1 in European Farmed Animals: High Genetic Relatedness of Isolates from Italian Cattle Herds and Humans.. PLoS One 2015;10(8):e0137143.
    doi: 10.1371/journal.pone.0137143pmc: PMC4556339pubmed: 26322785google scholar: lookup
  57. Wang W, Lin X, Jiang T, Peng Z, Xu J, Yi L, Li F, Fanning S, Baloch Z. Prevalence and Characterization of Staphylococcus aureus Cultured From Raw Milk Taken From Dairy Cows With Mastitis in Beijing, China.. Front Microbiol 2018;9:1123.
    doi: 10.3389/fmicb.2018.01123pmc: PMC6024008pubmed: 29988423google scholar: lookup
  58. Seinige D, Von Altrock A, Kehrenberg C. Genetic diversity and antibiotic susceptibility of Staphylococcus aureus isolates from wild boars.. Comp Immunol Microbiol Infect Dis 2017 Oct;54:7-12.
    doi: 10.1016/j.cimid.2017.07.003pubmed: 28916003google scholar: lookup
  59. Cunningham SA, Chia N, Jeraldo PR, Quest DJ, Johnson JA, Boxrud DJ, Taylor AJ, Chen J, Jenkins GD, Drucker TM, Nelson H, Patel R. Comparison of Whole-Genome Sequencing Methods for Analysis of Three Methicillin-Resistant Staphylococcus aureus Outbreaks.. J Clin Microbiol 2017 Jun;55(6):1946-1953.
    doi: 10.1128/JCM.00029-17pmc: PMC5442552pubmed: 28404677google scholar: lookup
  60. Xu SX, McCormick JK. Staphylococcal superantigens in colonization and disease.. Front Cell Infect Microbiol 2012;2:52.
    doi: 10.3389/fcimb.2012.00052pmc: PMC3417409pubmed: 22919643google scholar: lookup
  61. Pettersson H, Forsberg G. Staphylococcal enterotoxin H contrasts closely related enterotoxins in species reactivity.. Immunology 2002 May;106(1):71-9.
    doi: 10.1046/j.1365-2567.2002.01409.xpmc: PMC1782703pubmed: 11972634google scholar: lookup
  62. Koop G, Vrieling M, Storisteanu DM, Lok LS, Monie T, van Wigcheren G, Raisen C, Ba X, Gleadall N, Hadjirin N, Timmerman AJ, Wagenaar JA, Klunder HM, Fitzgerald JR, Zadoks R, Paterson GK, Torres C, Waller AS, Loeffler A, Loncaric I, Hoet AE, Bergström K, De Martino L, Pomba C, de Lencastre H, Ben Slama K, Gharsa H, Richardson EJ, Chilvers ER, de Haas C, van Kessel K, van Strijp JA, Harrison EM, Holmes MA. Identification of LukPQ, a novel, equid-adapted leukocidin of Staphylococcus aureus.. Sci Rep 2017 Jan 20;7:40660.
    doi: 10.1038/srep40660pmc: PMC5247767pubmed: 28106142google scholar: lookup
  63. de Jong NWM, Vrieling M, Garcia BL, Koop G, Brettmann M, Aerts PC, Ruyken M, van Strijp JAG, Holmes M, Harrison EM, Geisbrecht BV, Rooijakkers SHM. Identification of a staphylococcal complement inhibitor with broad host specificity in equid Staphylococcus aureus strains.. J Biol Chem 2018 Mar 23;293(12):4468-4477.
    doi: 10.1074/jbc.RA117.000599pmc: PMC5868266pubmed: 29414776google scholar: lookup
  64. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O'Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan HL, Weber S, Ehricht R. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus.. PLoS One 2011 Apr 6;6(4):e17936.
    doi: 10.1371/journal.pone.0017936pmc: PMC3071808pubmed: 21494333google scholar: lookup
  65. Schwarz S, Silley P, Simjee S, Woodford N, van Duijkeren E, Johnson AP, Gaastra W. Assessing the antimicrobial susceptibility of bacteria obtained from animals.. Vet Microbiol 2010 Feb 24;141(1-2):1-4.
    doi: 10.1016/j.vetmic.2009.12.013pubmed: 20042302google scholar: lookup
  66. Ghuysen JM. Serine beta-lactamases and penicillin-binding proteins.. Annu Rev Microbiol 1991;45:37-67.
    doi: 10.1146/annurev.mi.45.100191.000345pubmed: 1741619google scholar: lookup
  67. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis.. FEMS Microbiol Rev 2008 Mar;32(2):234-58.
    doi: 10.1111/j.1574-6976.2008.00105.xpubmed: 18266856google scholar: lookup
  68. Sauvage E, Terrak M. Glycosyltransferases and Transpeptidases/Penicillin-Binding Proteins: Valuable Targets for New Antibacterials.. Antibiotics (Basel) 2016 Feb 17;5(1).
    doi: 10.3390/antibiotics5010012pmc: PMC4810414pubmed: 27025527google scholar: lookup
  69. Morroni G, Brenciani A, Brescini L, Fioriti S, Simoni S, Pocognoli A, Mingoia M, Giovanetti E, Barchiesi F, Giacometti A, Cirioni O. High Rate of Ceftobiprole Resistance among Clinical Methicillin-Resistant Staphylococcus aureus Isolates from a Hospital in Central Italy.. Antimicrob Agents Chemother 2018 Dec;62(12).
    doi: 10.1128/AAC.01663-18pmc: PMC6256782pubmed: 30275082google scholar: lookup
  70. Kim CK, Milheiriço C, de Lencastre H, Tomasz A. Antibiotic Resistance as a Stress Response: Recovery of High-Level Oxacillin Resistance in Methicillin-Resistant Staphylococcus aureus "Auxiliary" (fem) Mutants by Induction of the Stringent Stress Response.. Antimicrob Agents Chemother 2017 Aug;61(8).
    doi: 10.1128/AAC.00313-17pmc: PMC5527599pubmed: 28630179google scholar: lookup
  71. de Lencastre H, de Jonge BL, Matthews PR, Tomasz A. Molecular aspects of methicillin resistance in Staphylococcus aureus.. J Antimicrob Chemother 1994 Jan;33(1):7-24.
    doi: 10.1093/jac/33.1.7pubmed: 8157576google scholar: lookup
  72. Giannouli S, Labrou M, Kyritsis A, Ikonomidis A, Pournaras S, Stathopoulos C, Tsakris A. Detection of mutations in the FemXAB protein family in oxacillin-susceptible mecA-positive Staphylococcus aureus clinical isolates.. J Antimicrob Chemother 2010 Apr;65(4):626-33.
    doi: 10.1093/jac/dkq039pubmed: 20156801google scholar: lookup
  73. Bizzini A, Entenza JM, Moreillon P. Loss of penicillin tolerance by inactivating the carbon catabolite repression determinant CcpA in Streptococcus gordonii.. J Antimicrob Chemother 2007 Apr;59(4):607-15.
    doi: 10.1093/jac/dkm021pubmed: 17327292google scholar: lookup
  74. Cabral DJ, Wurster JI, Belenky P. Antibiotic Persistence as a Metabolic Adaptation: Stress, Metabolism, the Host, and New Directions.. Pharmaceuticals (Basel) 2018 Feb 1;11(1).
    doi: 10.3390/ph11010014pmc: PMC5874710pubmed: 29389876google scholar: lookup
  75. Maalej SM, Rhimi FM, Fines M, Mnif B, Leclercq R, Hammami A. Analysis of borderline oxacillin-resistant Staphylococcus aureus (BORSA) strains isolated in Tunisia.. J Clin Microbiol 2012 Oct;50(10):3345-8.
    doi: 10.1128/JCM.01354-12pmc: PMC3457433pubmed: 22814459google scholar: lookup
  76. Staude MW, Frederick TE, Natarajan SV, Wilson BD, Tanner CE, Ruggiero ST, Mobashery S, Peng JW. Investigation of signal transduction routes within the sensor/transducer protein BlaR1 of Staphylococcus aureus.. Biochemistry 2015 Mar 3;54(8):1600-10.
    doi: 10.1021/bi501463kpmc: PMC4691190pubmed: 25658195google scholar: lookup
  77. Olsen JE, Christensen H, Aarestrup FM. Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci.. J Antimicrob Chemother 2006 Mar;57(3):450-60.
    doi: 10.1093/jac/dki492pubmed: 16449305google scholar: lookup
  78. Liu P, Xue H, Wu Z, Ma J, Zhao X. Effect of bla regulators on the susceptible phenotype and phenotypic conversion for oxacillin-susceptible mecA-positive staphylococcal isolates.. J Antimicrob Chemother 2016 Aug;71(8):2105-12.
    doi: 10.1093/jac/dkw123pubmed: 27154864google scholar: lookup
  79. Schug A R, Feßler A T, Scholtzek A D, Meurer M, Brombach J, Hensel V, Schwarz S. Determination of biocide susceptibility: Development of a broth microdilution method. National Symposium on Zoonoses Research 2018, Program and Abstracts National Symposium on Zoonoses Research 2018, Berlin, Germany, 17–19 October 2018. Volume A22. German Research Platform for Zoonoses; Berlin, Germany: 2018; pp. 158–159.
  80. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y, Stepanauskas R, Clingenpeel SR, Woyke T, McLean JS, Lasken R, Tesler G, Alekseyev MA, Pevzner PA. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products.. J Comput Biol 2013 Oct;20(10):714-37.
    doi: 10.1089/cmb.2013.0084pmc: PMC3791033pubmed: 24093227google scholar: lookup
  81. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology.. BMC Genomics 2008 Feb 8;9:75.
    doi: 10.1186/1471-2164-9-75pmc: PMC2265698pubmed: 18261238google scholar: lookup
  82. Seemann T. Prokka: rapid prokaryotic genome annotation.. Bioinformatics 2014 Jul 15;30(14):2068-9.
    doi: 10.1093/bioinformatics/btu153pubmed: 24642063google scholar: lookup
  83. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  84. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. Identification of acquired antimicrobial resistance genes.. J Antimicrob Chemother 2012 Nov;67(11):2640-4.
    doi: 10.1093/jac/dks261pmc: PMC3468078pubmed: 22782487google scholar: lookup
  85. Jünemann S, Sedlazeck FJ, Prior K, Albersmeier A, John U, Kalinowski J, Mellmann A, Goesmann A, von Haeseler A, Stoye J, Harmsen D. Updating benchtop sequencing performance comparison.. Nat Biotechnol 2013 Apr;31(4):294-6.
    doi: 10.1038/nbt.2522pubmed: 23563421google scholar: lookup
  86. Leopold SR, Goering RV, Witten A, Harmsen D, Mellmann A. Bacterial whole-genome sequencing revisited: portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes.. J Clin Microbiol 2014 Jul;52(7):2365-70.
    doi: 10.1128/JCM.00262-14pmc: PMC4097726pubmed: 24759713google scholar: lookup
  87. DVG. Richtlinien für die Prüfung von Desinfektionsverfahren und Chemischen Desinfektionsmitteln. Verlag der DVG Service GmbH 4th ed. Verlag der DVG Service GmbH; Gießen, Germany: 2007.

Citations

This article has been cited 17 times.
  1. Krüger-Haker H, Ji X, Hanke D, Fiedler S, Feßler AT, Jiang N, Kaspar H, Wang Y, Wu C, Schwarz S. Genomic Diversity of Methicillin-Resistant Staphylococcus aureus CC398 Isolates Collected from Diseased Swine in the German National Resistance Monitoring Program GERM-Vet from 2007 to 2019.. Microbiol Spectr 2023 Jun 15;11(3):e0077023.
    doi: 10.1128/spectrum.00770-23pubmed: 37154741google scholar: lookup
  2. Tyrnenopoulou P, Fthenakis GC. Clinical Aspects of Bacterial Distribution and Antibiotic Resistance in the Reproductive System of Equids.. Antibiotics (Basel) 2023 Mar 28;12(4).
    doi: 10.3390/antibiotics12040664pubmed: 37107026google scholar: lookup
  3. Bertelloni F, Cagnoli G, Bresciani F, Scotti B, Lazzerini L, Marcucci M, Colombani G, Ebani VV. Antimicrobial Resistant Coagulase-Negative Staphylococci Carried by House Flies (Musca domestica) Captured in Swine and Poultry Farms.. Antibiotics (Basel) 2023 Mar 23;12(4).
    doi: 10.3390/antibiotics12040636pubmed: 37106998google scholar: lookup
  4. Nwobi OC, Anyanwu MU, Jaja IF, Nwankwo IO, Okolo CC, Nwobi CA, Ezenduka EV, Oguttu JW. Staphylococcus aureus in Horses in Nigeria: Occurrence, Antimicrobial, Methicillin and Heavy Metal Resistance and Virulence Potentials.. Antibiotics (Basel) 2023 Jan 24;12(2).
    doi: 10.3390/antibiotics12020242pubmed: 36830153google scholar: lookup
  5. Monecke S, Roberts MC, Braun SD, Diezel C, Müller E, Reinicke M, Linde J, Joshi PR, Paudel S, Acharya M, Chalise MK, Feßler AT, Hotzel H, Khanal L, Koju NP, Schwarz S, Kyes RC, Ehricht R. Sequence Analysis of Novel Staphylococcus aureus Lineages from Wild and Captive Macaques.. Int J Mol Sci 2022 Sep 23;23(19).
    doi: 10.3390/ijms231911225pubmed: 36232529google scholar: lookup
  6. Monecke S, Schaumburg F, Shittu AO, Schwarz S, Mühldorfer K, Brandt C, Braun SD, Collatz M, Diezel C, Gawlik D, Hanke D, Hotzel H, Müller E, Reinicke M, Feßler AT, Ehricht R. Description of Staphylococcal Strains from Straw-Coloured Fruit Bat (Eidolon helvum) and Diamond Firetail (Stagonopleura guttata) and a Review of their Phylogenetic Relationships to Other Staphylococci.. Front Cell Infect Microbiol 2022;12:878137.
    doi: 10.3389/fcimb.2022.878137pubmed: 35646742google scholar: lookup
  7. Schug AR, Scholtzek AD, Turnidge J, Meurer M, Schwarz S, Feßler AT, The Biocide Susceptibility Study Group. Development of Quality Control Ranges for Biocide Susceptibility Testing.. Pathogens 2022 Feb 8;11(2).
    doi: 10.3390/pathogens11020223pubmed: 35215165google scholar: lookup
  8. Kaiser-Thom S, Gerber V, Collaud A, Hurni J, Perreten V. Prevalence and WGS-based characteristics of Staphylococcus aureus in the nasal mucosa and pastern of horses with equine pastern dermatitis.. BMC Vet Res 2022 Feb 24;18(1):79.
    doi: 10.1186/s12917-021-03053-ypubmed: 35209904google scholar: lookup
  9. Feßler AT, Scholtzek AD, Schug AR, Kohn B, Weingart C, Schink AK, Bethe A, Lübke-Becker A, Schwarz S. Antimicrobial and Biocide Resistance among Feline and Canine Staphylococcus aureus and Staphylococcus pseudintermedius Isolates from Diagnostic Submissions.. Antibiotics (Basel) 2022 Jan 19;11(2).
    doi: 10.3390/antibiotics11020127pubmed: 35203730google scholar: lookup
  10. Monecke S, Feßler AT, Burgold-Voigt S, Krüger H, Mühldorfer K, Wibbelt G, Liebler-Tenorio EM, Reinicke M, Braun SD, Hanke D, Diezel C, Müller E, Loncaric I, Schwarz S, Ehricht R. Staphylococcus aureus isolates from Eurasian Beavers (Castor fiber) carry a novel phage-borne bicomponent leukocidin related to the Panton-Valentine leukocidin.. Sci Rep 2021 Dec 22;11(1):24394.
    doi: 10.1038/s41598-021-03823-6pubmed: 34937862google scholar: lookup
  11. Sommer A, Fuchs S, Layer F, Schaudinn C, Weber RE, Richard H, Erdmann MB, Laue M, Schuster CF, Werner G, Strommenger B. Mutations in the gdpP gene are a clinically relevant mechanism for β-lactam resistance in meticillin-resistant Staphylococcus aureus lacking mec determinants.. Microb Genom 2021 Sep;7(9).
    doi: 10.1099/mgen.0.000623pubmed: 34486969google scholar: lookup
  12. Little SV, Hillhouse AE, Lawhon SD, Bryan LK. Analysis of Virulence and Antimicrobial Resistance Gene Carriage in Staphylococcus aureus Infections in Equids Using Whole-Genome Sequencing.. mSphere 2021 Aug 25;6(4):e0019620.
    doi: 10.1128/mSphere.00196-20pubmed: 34346711google scholar: lookup
  13. Mbindyo CM, Gitao GC, Plummer PJ, Kulohoma BW, Mulei CM, Bett R. Antimicrobial Resistance Profiles and Genes of Staphylococci Isolated from Mastitic Cow's Milk in Kenya.. Antibiotics (Basel) 2021 Jun 24;10(7).
    doi: 10.3390/antibiotics10070772pubmed: 34202836google scholar: lookup
  14. Lienen T, Schnitt A, Hammerl JA, Marino SF, Maurischat S, Tenhagen BA. Multidrug-resistant Staphylococcus cohnii and Staphylococcus urealyticus isolates from German dairy farms exhibit resistance to beta-lactam antibiotics and divergent penicillin-binding proteins.. Sci Rep 2021 Mar 16;11(1):6075.
    doi: 10.1038/s41598-021-85461-6pubmed: 33727647google scholar: lookup
  15. Becker K. Methicillin-Resistant Staphylococci and Macrococci at the Interface of Human and Animal Health.. Toxins (Basel) 2021 Jan 14;13(1).
    doi: 10.3390/toxins13010061pubmed: 33466773google scholar: lookup
  16. Fisher JF, Mobashery S. β-Lactams against the Fortress of the Gram-Positive Staphylococcus aureus Bacterium.. Chem Rev 2021 Mar 24;121(6):3412-3463.
    doi: 10.1021/acs.chemrev.0c01010pubmed: 33373523google scholar: lookup
  17. Speck S, Wenke C, Feßler AT, Kacza J, Geber F, Scholtzek AD, Hanke D, Eichhorn I, Schwarz S, Rosolowski M, Truyen U. Borderline resistance to oxacillin in Staphylococcus aureus after treatment with sub-lethal sodium hypochlorite concentrations.. Heliyon 2020 Jun;6(6):e04070.
    doi: 10.1016/j.heliyon.2020.e04070pubmed: 32613099google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.