FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Frontiers in microbiology2018; 9; 2516; doi: 10.3389/fmicb.2018.02516

Equine Methicillin-Resistant Sequence Type 398 Staphylococcus aureus (MRSA) Harbor Mobile Genetic Elements Promoting Host Adaptation.

Abstract: Continuing introduction of multi-drug resistant, zoonotic pathogens such as methicillin-resistant Staphylococcus aureus (MRSA) in horse clinics challenges the biosafety of employees and animal patients. This study was aimed to determine the occurrence of mobile genetic elements facilitating survival in the early stages of invasive infection in different host species, including humans and horses, in MRSA carried by equine patients admitted to a large horse clinic. A total of 341 equine patients were investigated for carriage of MRSA by hygiene screening directly at hospital admission. MRSA were further investigated by antimicrobial susceptibility testing, whole-genome sequencing and genomic composition, including virulence factors involved in immune evasion and host adaption. From a total of 340 validated specimens from equine nostrils, 3.5% yielded positive results for MRSA. All MRSA were found to be closely related belonging to sequence type (ST) 398_t011 with up to four additional antimicrobial resistances. All MRSA harbored a specific Staphylococcal Pathogenicity Island (SaPIbov5) involved in facilitating survival in ruminant and equine plasma. Moreover, a β-hemolysin (hlb) converting ΦSa3 phage encoding the human-specific Immune Evasion Cluster (IEC) was present in 72% of the isolates. An equid-specific leukotoxin encoded by a further temperate phage (Saeq1) was only rarely detected (22%). Despite the absence of β-hemolysin production for all IEC-positive ST398, a prominent hemolysis zone was demonstrable on sheep blood agar. Thus, IEC might remain undetected among the ST398 lineage, since the presence of IEC is commonly associated with reduction of hemolysis in S. aureus belonging to other genetic backgrounds. Here we describe MRSA-ST398 harboring different mobile genetic elements encoding variants of immune evasion factors and toxins previously shown to contribute to S. aureus invasive diseases in specific host species or ecologic niches. We suggest these combinations contribute to the adaptation of MRSA belonging to ST398 with respect to epidemic spread across different habitats and hosts, and may therefore confer a host "generalist" phenotype.
Get Full Text
Publication Date: 2018-10-24 PubMed ID: 30405574PubMed Central: PMC6207647DOI: 10.3389/fmicb.2018.02516Google 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

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.

The research article discusses the investigation into the presence of Methicillin-Resistant Staphylococcus Aureus (MRSA) in horse patients in a clinic, their genetic composition, and how these might contribute to the bacteria’s adaptation in different hosts.

Study Procedure

  • The researchers collected samples from 341 horse patients admitted to a large horse clinic upon their arrival.
  • The aim was to check if these samples were carriers of MRSA, a type of bacteria resistant to several antibiotics.
  • The samples were subjected to antimicrobial susceptibility testing, whole-genome sequencing, and evaluation of their genomic composition.
  • The researchers were specifically interested in investigating the prevalence of virulence factors involved in immune evasion and adaptation to the host.

Findings

  • Out of the 340 validated samples, around 3.5% tested positive for MRSA.
  • All the tested MRSA were found to belong to the sequence type (ST) 398_t011.
  • These MRSA were additionally resistant to approximately four other types of antimicrobial drugs.
  • The researchers detected the presence of a specific Staphylococcal Pathogenicity Island (SaPIbov5) in all the MRSA tested. This genetic element facilitates survival of the bacteria within the blood of ruminants and horses.
  • Furthermore, a phage called ΦSa3, encoding the human-specific Immune Evasion Cluster (IEC), was present in 72% of the samples. The presence of IEC is usually linked with reduced hemolysis (destruction of red blood cells), but this was not the case in the tested samples.
  • A horse-specific leukotoxin was detected only rarely (in 22% of the samples).

Implications

  • The investigators hypothesize that the variety of immune evasion factors and toxins, encoded by mobile genetic elements, could contribute to the bacteria’s ability to cause invasive diseases in different hosts and ecological niches.
  • The presence of such genetic elements might confer a “generalist” phenotype to the ST398 lineage of MRSA, enabling them to adapt and spread across diverse habitats and hosts.
  • This discovery could imply increased risks to the health of both animal patients and human caregivers and on-site staff at animal clinics, indicating the importance of continued attention to hygiene practices.

Cite This Article

APA
Walther B, Klein KS, Barton AK, Semmler T, Huber C, Merle R, Tedin K, Mitrach F, Lübke-Becker A, Gehlen H. (2018). Equine Methicillin-Resistant Sequence Type 398 Staphylococcus aureus (MRSA) Harbor Mobile Genetic Elements Promoting Host Adaptation. Front Microbiol, 9, 2516. https://doi.org/10.3389/fmicb.2018.02516

Publication

Frontiers in microbiology
ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 9
Pages: 2516

Researcher Affiliations

Walther, Birgit
  • Centre for Infection Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, Germany.
  • Advanced Light and Electron Microscopy (ZBS4), Robert Koch Institute, Berlin, Germany.
Klein, Katja-Sophia
  • Equine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, Germany.
Barton, Ann-Kristin
  • Equine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, Germany.
Semmler, Torsten
  • Microbial Genomics (NG1), Robert Koch Institute, Berlin, Germany.
Huber, Charlotte
  • Microbial Genomics (NG1), Robert Koch Institute, Berlin, Germany.
Merle, Roswitha
  • Institute for Veterinary Epidemiology and Biostatistics, Freie Universität Berlin, Berlin, Germany.
Tedin, Karsten
  • Centre for Infection Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, Germany.
Mitrach, Franziska
  • Faculty of Environment and Natural Sciences, Institute of Biotechnology, Brandenburg University of Technology Cottbus-Senftenberg, Cottbus, Germany.
Lübke-Becker, Antina
  • Centre for Infection Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, Germany.
Gehlen, Heidrun
  • Equine Clinic, Surgery and Radiology, Freie Universität Berlin, Berlin, Germany.

References

This article includes 54 references
  1. Acton DS, Plat-Sinnige MJT, van Wamel W, de Groot N, van Belkum A. Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact?. Eur. J. Clin. Microbiol. Infect Dis. 28, 115–127.
    doi: 10.1007/s10096-008-0602-7pubmed: 18688664google scholar: lookup
  2. Bartels MD, Petersen A, Worning P, Nielsen JB, Larner-Svensson H, Johansen HK. Comparing whole-genome sequencing with Sanger sequencing for spa typing of methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 52, 4305–4308.
    doi: 10.1128/JCM.01979-14pmc: PMC4313303pubmed: 25297335google scholar: lookup
  3. Christie R, Atkins NE, Munch-Petersen E. A note on a lytic phenomenon shown by group B streptococci. Aust. J. Exp. Biol. 22, 197–200.
    pubmed: 21006102
  4. Claassen-Weitz S, Shittu AO, Ngwarai MR, Thabane L, Nicol MP, Kaba M. Fecal carriage of Staphylococcus aureus in the hospital and community setting: a systematic review. Front. Microbiol. 7:449.
    doi: 10.3389/fmicb.2016.00449pmc: PMC4861718pubmed: 27242671google scholar: lookup
  5. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-first Informational Supplement M100-S21. 2011.
  6. Clinical and Laboratory Standards Institute. Vet01-S2 Performance Standards for Antimicrobial Disk and Dilution Susceptibility for Bacteria isolated from Animals. Second International Supplement. 2013.
  7. Cuny C, Abdelbary M, Layer F, Werner G, Witte W. Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet. Microbiol. 177, 219–223.
    doi: 10.1016/j.vetmic.2015.02.031pubmed: 25778546google scholar: lookup
  8. Cuny C, Kuemmerle J, Stanek C, Willey B, Strommenger B, Witte W. Emergence of MRSA infections in horses in a veterinary hospital: strain characterisation and comparison with MRSA from humans. Euro Surveill. 11, 44–47.
    doi: 10.2807/esm.11.01.00595-enpubmed: 16484728google scholar: lookup
  9. Cuny C, Strommenger B, Witte W, Stanek C. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. Microb. Drug Resist. 14, 307–310.
    doi: 10.1089/mdr.2008.0845pubmed: 19025385google scholar: lookup
  10. de Jong NWM, Vrieling M, Garcia BL, Koop G, Brettmann M, Aerts PC. Identification of a staphylococcal complement inhibitor with broad host specificity in equid S. aureus strains. J. Biol. Chem. 293, 4468–4477.
    doi: 10.1074/jbc.RA117.000599pmc: PMC5868266pubmed: 29414776google scholar: lookup
  11. Diene SM, Corvaglia AR, Francois P, van der Mee-Marquet N, Regional Infection Control Group of the Centre Region. Prophages and adaptation of Staphylococcus aureus ST398 to the human clinic. BMC Genomics 18:133.
    doi: 10.1186/s12864-017-3516-xpmc: PMC5294865pubmed: 28166723google scholar: lookup
  12. Everitt RG, Didelot X, Batty EM, Miller RR, Knox K, Young BC. Mobile elements drive recombination hotspots in the core genome of Staphylococcus aureus. Nat. Commun. 5:3956.
    doi: 10.1038/ncomms4956pmc: PMC4036114pubmed: 24853639google scholar: lookup
  13. Feßler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J. Antimicrob. Chemother. 65, 619–625.
    doi: 10.1093/jac/dkq021pubmed: 20164198google scholar: lookup
  14. Fessler AT, Zhao Q, Schoenfelder S, Kadlec K, Brenner MG, Wang Y. Complete sequence of a plasmid from a bovine methicillin-resistant Staphylococcus aureus harbouring a novel ica-like gene cluster in addition to antimicrobial and heavy metal resistance genes. Vet. Microbiol. 200, 95–100.
    doi: 10.1016/j.vetmic.2016.07.010pubmed: 27476981google scholar: lookup
  15. Foster TJ. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3, 948–958.
    doi: 10.1038/nrmicro1289pubmed: 16322743google scholar: lookup
  16. Harrison EM, Weinert LA, Holden MT, Welch JJ, Wilson K, Morgan FJ. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. MBio 5:e00985–e00913.
    doi: 10.1128/mBio.00985-13pmc: PMC4030480pubmed: 24825010google scholar: lookup
  17. Islam MZ, Espinosa-Gongora C, Damborg P, Sieber RN, Munk R, Husted L. Horses in Denmark are a reservoir of diverse clones of methicillin-resistant and -susceptible Staphylococcus aureus. Front. Microbiol. 8:543.
    doi: 10.3389/fmicb.2017.00543pmc: PMC5376617pubmed: 28421046google scholar: lookup
  18. Jongerius I, Kohl J, Pandey MK, Ruyken M, van Kessel KP, van Strijp JA. Staphylococcal complement evasion by various convertase-blocking molecules. J. Exp. Med. 204, 2461–2471.
    doi: 10.1084/jem.20070818pmc: PMC2118443pubmed: 17893203google scholar: lookup
  19. Jung P, Abdelbary MM, Kraushaar B, Fetsch A, Geisel J, Herrmann M. Impact of bacteriophage Saint3 carriage on the immune evasion capacity and hemolytic potential of Staphylococcus aureus CC398. Vet. Microbiol. 200, 46–51.
    doi: 10.1016/j.vetmic.2016.02.015pubmed: 26923248google scholar: lookup
  20. Kadlec K, Schwarz S. Identification of the novel dfrK-carrying transposon Tn559 in a porcine methicillin-susceptible Staphylococcus aureus ST398 strain. Antimicrob Agents Chemother. 54, 3475–3477.
    doi: 10.1128/AAC.00464-10pmc: PMC2916295pubmed: 20498309google scholar: lookup
  21. Katayama Y, Baba T, Sekine M, Fukuda M, Hiramatsu K. Beta-hemolysin promotes skin colonization by Staphylococcus aureus. J. Bacteriol. 195, 1194–1203.
    doi: 10.1128/JB.01786-12pmc: PMC3592002pubmed: 23292775google scholar: lookup
  22. Kinnevey PM, Shore AC, Brennan GI, Sullivan DJ, Ehricht R, Monecke S. Extensive genetic diversity identified among sporadic methicillin-resistant Staphylococcus aureus isolates recovered in Irish hospitals between 2000 and 2012. Antimic. Agents Chemoth. 58, 1907–1917.
    doi: 10.1128/AAC.02653-13pmc: PMC4023797pubmed: 24395241google scholar: lookup
  23. Köck R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur. J. Clin. Microbiol. Infect. Dis. 28, 1375–1382.
    doi: 10.1007/s10096-009-0795-4pmc: PMC2772956pubmed: 19701815google scholar: lookup
  24. 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 8:e0055040.
    doi: 10.1371/journal.pone.0055040pmc: PMC3572123pubmed: 23418434google scholar: lookup
  25. Koop G, Vrieling M, Storisteanu DM, Lok LS, Monie T, van Wigcheren G. Identification of LukPQ, a novel, equid-adapted leukocidin of Staphylococcus aureus. Sci. Rep. 7:40660.
    doi: 10.1038/srep40660pmc: PMC5247767pubmed: 28106142google scholar: lookup
  26. Kraushaar B, Hammerl JA, Kienol M, Heinig ML, Sperling N, Dinh Thanh M. Acquisition of virulence factors in livestock-associated MRSA: Lysogenic conversion of CC398 strains by virulence gene-containing phages. Sci. Rep. 7:2004.
    doi: 10.1038/s41598-017-02175-4pmc: PMC5435737pubmed: 28515479google scholar: lookup
  27. Larsen J, Petersen A, Sorum M, Stegger M, van Alphen L, Valentiner-Branth P. Meticillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Euro. Surv. 20, 5–13.
    doi: 10.2807/1560-7917.ES.2015.20.37.30021pmc: PMC4902279pubmed: 26535590google scholar: lookup
  28. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL. Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355–1361.
    doi: 10.1128/JCM.06094-11pmc: PMC3318499pubmed: 22238442google scholar: lookup
  29. Makarova O, Johnston P, Walther B, Rolff J, Roesler U. Complete genome sequence of the livestock-associated methicillin-resistant strain Staphylococcus aureus subsp. aureus 08S00974 (Sequence Type 398). Genome Announc 5 e00294–17.
    doi: 10.1128/genomeA.00294-17pmc: PMC5427207pubmed: 28495772google scholar: lookup
  30. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell. Mol. Life Sci. 67, 3057–3071.
    doi: 10.1007/s00018-010-0389-4pmc: PMC2929429pubmed: 20668911google scholar: lookup
  31. McCarthy AJ, Lindsay JA. Staphylococcus aureus innate immune evasion is lineage-specific: a bioinfomatics study. Infect. Genet. Evol. 19, 7–14.
    doi: 10.1016/j.meegid.2013.06.012pubmed: 23792184google scholar: lookup
  32. Ricklin D, Tzekou A, Garcia BL, Hammel M, McWhorter WJ, Sfyroera G. A molecular insight into complement evasion by the staphylococcal complement inhibitor protein family. J. Immunol. 183, 2565–2574.
    doi: 10.4049/jimmunol.0901443pmc: PMC2881335pubmed: 19625656google scholar: lookup
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069.
    doi: 10.1093/bioinformatics/btu153pubmed: 24642063google scholar: lookup
  34. Sharma M, Nunez-Garcia J, Kearns AM, Doumith M, Butaye PR, Argudin MA. Livestock-associated methicillin resistant Staphylococcus aureus (LA-MRSA) Clonal Complex (CC) 398 Isolated from UK Animals belong to European Lineages. Front. Microbiol. 7:1741.
    doi: 10.3389/fmicb.2016.01741pmc: PMC5101578pubmed: 27881973google scholar: lookup
  35. Soimala T, Lübke-Becker A, Schwarz S, Feßler AT, Huber C, Semmler T. Occurrence and molecular composition of methicillin-resistant Staphylococcus aureus isolated from ocular surfaces of horses presented with ophthalmologic disease. Vet. Microbiol. 222, 1–6.
    doi: 10.1016/j.vetmic.2018.06.009pubmed: 30080662google scholar: lookup
  36. Spellerberg B, Brandt C. Streptococcus, in Manual of Clinical Microbiology, 11th Edn, eds Pfaller M., Jorgensen J., Carroll K., Funke G., Landry M., Richter S., Warnock D.. 391–392.
  37. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
    doi: 10.1093/bioinformatics/btu033pmc: PMC3998144pubmed: 24451623google scholar: lookup
  38. Tavares A, Nielsen JB, Boye K, Rohde S, Paulo AC, Westh H. Insights into Alpha-Hemolysin (Hla) Evolution and expression among Staphylococcus aureus clones with hospital and community origin. PLoS ONE 9:e0098634.
    doi: 10.1371/journal.pone.0098634pmc: PMC4102472pubmed: 25033196google scholar: lookup
  39. Thomer L, Schneewind O, Missiakas D. Multiple ligands of von Willebrand factor-binding protein (vWbp) promote Staphylococcus aureus clot formation in human plasma. J. Biol. Chem. 288, 28283–28292.
    doi: 10.1074/jbc.M113.493122pmc: PMC3784736pubmed: 23960083google scholar: lookup
  40. Tokateloff N, Manning ST, Weese JS, Campbell J, Rothenburger J, Stephen C. Prevalence of methicillin-resistant Staphylococcus aureus colonization in horses in Saskatchewan, Alberta, and British Columbia. Can. Vet. J. 50, 1177–1180.
    pmc: PMC2764514pubmed: 20119542
  41. Traber KE, Lee E, Benson S, Corrigan R, Cantera M, Shopsin B. agr function in clinical Staphylococcus aureus isolates. Microbiology 154(Pt 8), 2265–2274.
    doi: 10.1099/mic.0.2007/011874-0pmc: PMC4904715pubmed: 18667559google scholar: lookup
  42. van Alen S, Ballhausen B, Kaspar U, Koeck R, Becker K. Prevalence and genomic structure of bacteriophage phi3 in human derived livestock-associated MRSA from 2000 to 2015. J. Clin. Microbiol. 56, e00140–e00148.
    doi: 10.1128/JCM.00140-18pmc: PMC6113466pubmed: 29976589google scholar: lookup
  43. van Alen S, Ballhausen B, Peters G, Friedrich AW, Mellmann A, Koeck R. In the centre of an epidemic: fifteen years of LA-MRSA CC398 at the University Hospital Munster. Vet. Microbiol. 200, 19–24.
    doi: 10.1016/j.vetmic.2016.01.021pubmed: 26878970google scholar: lookup
  44. van Duijkeren E, Ten Horn L, Wagenaar JA, de Bruijn M, Laarhoven L, Verstappen K. Suspected horse-to-human transmission of MRSA ST398. Emerg. Infect. Dis. 17, 1137–1139.
    doi: 10.3201/eid1706.101330pmc: PMC3358200pubmed: 21749795google scholar: lookup
  45. van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188, 1310–1315.
    doi: 10.1128/JB.188.4.1310-1315.2006pmc: PMC1367213pubmed: 16452413google scholar: lookup
  46. Viana D, Blanco J, Tormo-Mas MA, Selva L, Guinane CM, Baselga R. Adaptation of Staphylococcus aureus to ruminant and equine hosts involves SaPI-carried variants of von Willebrand factor-binding protein. Mol. Microbiol. 77, 1583–1594.
    doi: 10.1111/j.1365-2958.2010.07312.xpubmed: 20860091google scholar: lookup
  47. Vincze S, Stamm I, Kopp PA, Hermes J, Adlhoch C, Semmler T. Alarming proportions of methicillin-resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012. PLoS ONE 9:e85656.
    doi: 10.1371/journal.pone.0085656pmc: PMC3896405pubmed: 24465637google scholar: lookup
  48. von Mentzer A, Connor TR, Wieler LH, Semmler T, Iguchi A, Thomson NR. Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat. Genet. 46, 1321–1326.
    doi: 10.1038/ng.3145pubmed: 25383970google scholar: lookup
  49. Walther B, Klein KS, Barton AK, Semmler T, Huber C, Wolf SA. Extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli and Acinetobacter baumannii among horses entering a veterinary teaching hospital: the contemporary “Trojan Horse”. PLoS ONE 13:e0191873.
    doi: 10.1371/journal.pone.0191873pmc: PMC5790241pubmed: 29381714google scholar: lookup
  50. Walther B, Monecke S, Ruscher C, Friedrich AW, Ehricht R, Slickers P. Comparative molecular analysis substantiates a zoonotic potential of equine Methicillin- resistant Staphylococcus aureus (MRSA). J. Clin. Microbiol. 47, 704–710.
    doi: 10.1128/JCM.01626-08pmc: PMC2650932pubmed: 19109463google scholar: lookup
  51. Walther B, Tedin K, Luebke-Becker A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet. Microbiol. 200, 71–78.
    doi: 10.1016/j.vetmic.2016.05.017pubmed: 27291944google scholar: lookup
  52. Weese JS, van Duijkeren E. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet. Microbiol. 140, 418–429.
    doi: 10.1016/j.vetmic.2009.01.039pubmed: 19246166google scholar: lookup
  53. Wendlandt S, Fessler AT, Monecke S, Ehricht R, Schwarz S, Kadlec K. The diversity of antimicrobial resistance genes among staphylococci of animal origin. Int. J. Med. Microbiol. 303, 338–349.
    doi: 10.1016/j.ijmm.2013.02.006pubmed: 23499306google scholar: lookup
  54. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644.
    doi: 10.1093/jac/dks261pmc: PMC3468078pubmed: 22782487google scholar: lookup

Citations

This article has been cited 20 times.
  1. Stöckle SD, Kannapin DA, Merle R, Lübke-Becker A, Gehlen H. Comparison of a Single-Shot Antibiotic Protocol Compared to a Conventional 5-Day Antibiotic Protocol in Equine Diagnostic Laparotomy Regarding Pre- and Postoperative Colonization with Multi-Drug-Resistant Indicator Pathogens. Antibiotics (Basel) 2026 Jan 21;15(1).
    doi: 10.3390/antibiotics15010106pubmed: 41594143google scholar: lookup
  2. Jafari H, Abebe BK, Cong L, Ahmed Z, Zhaofei W, Sun M, Muhatai G, Chuzhao L, Dang R. Review: Genomic insights into the adaptive traits and stress resistance in modern horses. Stress Biol 2026 Jan 12;6(1):5.
    doi: 10.1007/s44154-025-00274-1pubmed: 41521281google scholar: lookup
  3. Dewi DAPR, Khalifa HO, Khandar H, Hisatsune J, Kutuno S, Yu L, Hayashi W, Kayama S, Mason CE, Sugai M, Suzuki H, Matsumoto T. Detection and genetic characterization of multidrug-resistant staphylococci isolated from public areas in an international airport. Sci Rep 2024 Nov 12;14(1):27738.
    doi: 10.1038/s41598-024-79447-3pubmed: 39532959google scholar: lookup
  4. . The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2021-2022. EFSA J 2024 Feb;22(2):e8583.
    doi: 10.2903/j.efsa.2024.8583pubmed: 38419967google scholar: lookup
  5. Werner G, Abu Sin M, Bahrs C, Brogden S, Feßler AT, Hagel S, Kaspar H, Köck R, Kreienbrock L, Krüger-Haker H, Maechler F, Noll I, Pletz MW, Tenhagen BA, Schwarz S, Walther B, Mielke M. [Therapy-relevant antibiotic resistances in a One Health context]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2023 Jun;66(6):628-643.
    doi: 10.1007/s00103-023-03713-4pubmed: 37184673google scholar: lookup
  6. Gehlen H, Klein KS, Merle R, Lübke-Becker A, Stoeckle SD. Does colonization with MRSA, ESBL - producing Enterobacteriaceae, and/or Acinetobacter baumannii - increase the risk for postoperative surgical site infection?. Vet Med Sci 2023 Mar;9(2):729-737.
    doi: 10.1002/vms3.1073pubmed: 36646070google scholar: lookup
  7. Huber C, Wolf SA, Ziebuhr W, Holmes MA, Assmann J, Lübke-Becker A, Thürmer A, Semmler T, Brombach J, Bethe A, Bischoff M, Wieler LH, Epping L, Walther B. How to survive pig farming: Mechanism of SCCmec element deletion and metabolic stress adaptation in livestock-associated MRSA. Front Microbiol 2022;13:969961.
    doi: 10.3389/fmicb.2022.969961pubmed: 36504815google scholar: lookup
  8. Khairullah AR, Sudjarwo SA, Effendi MH, Ramandinianto SC, Widodo A, Riwu KHP. A review of horses as a source of spreading livestock-associated methicillin-resistant Staphylococcus aureus to human health. Vet World 2022 Aug;15(8):1906-1915.
    doi: 10.14202/vetworld.2022.1906-1915pubmed: 36313842google scholar: lookup
  9. Suminda GGD, Bhandari S, Won Y, Goutam U, Kanth Pulicherla K, Son YO, Ghosh M. High-throughput sequencing technologies in the detection of livestock pathogens, diagnosis, and zoonotic surveillance. Comput Struct Biotechnol J 2022;20:5378-5392.
    doi: 10.1016/j.csbj.2022.09.028pubmed: 36212529google scholar: lookup
  10. 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
  11. Yip CH, Mahalingam S, Wan KL, Nathan S. Prodigiosin inhibits bacterial growth and virulence factors as a potential physiological response to interspecies competition. PLoS One 2021;16(6):e0253445.
    doi: 10.1371/journal.pone.0253445pubmed: 34161391google scholar: lookup
  12. Stöckle SD, Kannapin DA, Kauter AML, Lübke-Becker A, Walther B, Merle R, Gehlen H. A Pilot Randomised Clinical Trial Comparing a Short-Term Perioperative Prophylaxis Regimen to a Long-Term Standard Protocol in Equine Colic Surgery. Antibiotics (Basel) 2021 May 16;10(5).
    doi: 10.3390/antibiotics10050587pubmed: 34065712google scholar: lookup
  13. Kauter A, Epping L, Ghazisaeedi F, Lübke-Becker A, Wolf SA, Kannapin D, Stoeckle SD, Semmler T, Günther S, Gehlen H, Walther B. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia coli Isolated From Specimens of Hospitalized Horses. Front Microbiol 2021;12:671676.
    doi: 10.3389/fmicb.2021.671676pubmed: 33936023google scholar: lookup
  14. Kauter A, Epping L, Semmler T, Antao EM, Kannapin D, Stoeckle SD, Gehlen H, Lübke-Becker A, Günther S, Wieler LH, Walther B. The gut microbiome of horses: current research on equine enteral microbiota and future perspectives. Anim Microbiome 2019 Nov 13;1(1):14.
    doi: 10.1186/s42523-019-0013-3pubmed: 33499951google scholar: lookup
  15. Lienen T, Schnitt A, Hammerl JA, Maurischat S, Tenhagen BA. Genomic Distinctions of LA-MRSA ST398 on Dairy Farms From Different German Federal States With a Low Risk of Severe Human Infections. Front Microbiol 2020;11:575321.
    doi: 10.3389/fmicb.2020.575321pubmed: 33488532google scholar: lookup
  16. Huber C, Stamm I, Ziebuhr W, Marincola G, Bischoff M, Strommenger B, Jaschkowitz G, Marciniak T, Cuny C, Witte W, Doellinger J, Schaudinn C, Thürmer A, Epping L, Semmler T, Lübke-Becker A, Wieler LH, Walther B. Silence as a way of niche adaptation: mecC-MRSA with variations in the accessory gene regulator (agr) functionality express kaleidoscopic phenotypes. Sci Rep 2020 Sep 8;10(1):14787.
    doi: 10.1038/s41598-020-71640-4pubmed: 32901059google scholar: lookup
  17. Kittl S, Brodard I, Heim D, Andina-Pfister P, Overesch G. Methicillin-Resistant Staphylococcus aureus Strains in Swiss Pigs and Their Relation to Isolates from Farmers and Veterinarians. Appl Environ Microbiol 2020 Feb 18;86(5).
    doi: 10.1128/AEM.01865-19pubmed: 31836575google scholar: lookup
  18. Scholtzek AD, Hanke D, Walther B, Eichhorn I, Stöckle SD, Klein KS, Gehlen H, Lübke-Becker A, Schwarz S, Feßler AT. Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility. Toxins (Basel) 2019 Sep 13;11(9).
    doi: 10.3390/toxins11090535pubmed: 31540335google scholar: lookup
  19. Espadinha D, Sobral RG, Mendes CI, Méric G, Sheppard SK, Carriço JA, de Lencastre H, Miragaia M. Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages. Front Microbiol 2019;10:1971.
    doi: 10.3389/fmicb.2019.01971pubmed: 31507574google scholar: lookup
  20. 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
Subscribe to our newsletter
Join 99,780 horse owners like you who receive our email updates on horse health and nutrition.