FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Antibiotics (Basel, Switzerland)2022; 11(2); doi: 10.3390/antibiotics11020221

The Prevalence and Molecular Biology of Staphylococcus aureus Isolated from Healthy and Diseased Equine Eyes in Egypt.

Abstract: This work aimed to characterize S. aureus isolates from the eyes of healthy and clinically affected equines in the Kafrelsheikh Governorate, Egypt. A total of 110 animals were examined for the presence of S. aureus, which was isolated from 33 animals with ophthalmic lesions and 77 healthy animals. We also investigated the antimicrobial resistance profile, oxacillin resistance mechanism, and the major virulence factors implicated in many studies of the ocular pathology of pathogenic S. aureus. The association between S. aureus eye infections and potential risk factors was also investigated. The frequency of S. aureus isolates from clinically affected equine eyes was significantly higher than in clinically healthy equids. A significant association was found between the frequency of S. aureus isolation from clinically affected equine eyes and risk factors including age and season but not with sex or breed factors. Antimicrobial resistance to common antibiotics used to treat equine eyes was also tested. Overall, the isolates showed the highest sensitivity to sulfamethoxazole (100%) and the highest resistance to cephalosporin (90.67%) and oxacillin (90.48%). PCR was used to demonstrate that mecA was present in 100% of oxacillin- and β-lactam-resistant S. aureus strains. The virulence factor genes Spa (x region), nuc, and hlg were identified in 62.5%, 100%, and 56%, of isolates, respectively, from clinically affected equines eyes. The severity of the eye lesions increased in the presence of γ-toxin-positive S. aureus. The phylogenetic tree of the Spa (x region) gene indicated a relationship with human reference strains isolated from Egypt as well as isolates from equines in Iran and Japan. This study provides insight into the prevalence, potential risk factors, clinical pictures, zoonotic potential, antimicrobial resistance, and β-lactam resistance mechanism of S. aureus strains that cause eye infection in equines from Egypt.
Get Full Text
Publication Date: 2022-02-10 PubMed ID: 35203823PubMed Central: PMC8868267DOI: 10.3390/antibiotics11020221Google 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 involves a study of Staphylococcus aureus, a bacterium that was isolated from the eyes of both healthy and diseased horses in the Kafrelsheikh Governorate, Egypt. The study reveals significant details about the bacterium’s prevalence, its antimicrobial resistance profiles, the mechanism of its resistance to oxacillin – a type of antibiotic, its major virulence factors, and the impact of risk factors on equine eye infections.

Study Methodology

  • The researchers examined a total of 110 horses, some with eye infections and others who were healthy.
  • Microbiological analysis allowed for the isolation and identification of Staphylococcus aureus from the eyes of these horses.
  • The effects of risk factors such as age and seasonality on eye infections were also studied, while sex and breed factors were found to be insignificant.
  • Testing was performed to gauge the bacterium’s antimicrobial resistance to commonly used antibiotics in treating equine eye conditions.

Source of Bacterial Resistance

  • The study discovered that the bacterium showed significant resistance to commonly used antibiotics such as cephalosporin and oxacillin – with resistance rates of 90.67% and 90.48% respectively.
  • The mechanism of oxacillin resistance in the bacterium was traced to an enzyme known as β-lactamase, as confirmed by PCR testing.

Role of Virulence Factors

  • A significant aspect of the research was the examination of virulence factors – elements that enhance the bacterium’s ability to infect its host.
  • Three virulence genes – x region, eta, and gamma-toxin – were identified in significant proportions of the pathogenic bacterial isolates from clinically infected horse’s eyes.
  • For instance, the gamma-toxin gene was found in 62.5% of the isolates and was linked to increased severity of eye lesions in horses.

Zoonotic Potential and Genetic Relationships

  • The research also indicated a potential for zoonotic transmission (i.e., the ability for the bacterium to spread from animals to humans), as evidenced by a phylogenetic analysis.
  • The genetic sequence of the x region gene in the isolated bacterial strains showed similarities with human strains from Egypt as well as horse strains from Iran and Japan.

Overall, this study contributes to an understanding of the prevalence and nature of Staphylococcus aureus infections in horses. It provides deeper insights into antibiotic resistance mechanisms, enabling more informed choices about antibiotic therapy in the equine veterinary context, and highlights the potential for zoonotic transmission.

Cite This Article

APA
Tahoun A, Elnafarawy HK, El-Sharkawy H, Rizk AM, Alorabi M, El-Shehawi AM, Youssef MA, Ibrahim HMM, El-Khodery S. (2022). The Prevalence and Molecular Biology of Staphylococcus aureus Isolated from Healthy and Diseased Equine Eyes in Egypt. Antibiotics (Basel), 11(2). https://doi.org/10.3390/antibiotics11020221

Publication

Antibiotics (Basel, Switzerland)
ISSN: 2079-6382
NlmUniqueID: 101637404
Country: Switzerland
Language: English
Volume: 11
Issue: 2

Researcher Affiliations

Tahoun, Amin
  • Department of Animal Medicine, Faculty of Veterinary Medicine, Kafrelshkh University, Kafrelsheikh 33511, Egypt.
Elnafarawy, Helmy K
  • Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.
El-Sharkawy, Hanem
  • Department of Poultry and Rabbit Diseases, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh 33511, Egypt.
Rizk, Amira M
  • Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Benha University, Benha 13518, Egypt.
Alorabi, Mohammed
  • Department of Biotechnology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia.
El-Shehawi, Ahmed M
  • Department of Biotechnology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia.
Youssef, Mohamed A
  • Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.
Ibrahim, Hussam M M
  • Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.
El-Khodery, Sabry
  • Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.

Conflict of Interest Statement

The authors declare that they have no conflict of interest.

References

This article includes 58 references
  1. Hsiao C.-H., Chuang C.-C., Tan H.Y., Ma D.H.K., Lin K.-K., Chang C.-J., Huang Y.C.. Methicillin-resistant Staphylococcus aureus ocular infection: A 10-year hospital-based study. Ophthalmology 2012;119:522–527.
    doi: 10.1016/j.ophtha.2011.08.038pubmed: 22176801google scholar: lookup
  2. Parhizgari N., Khoramrooz S.S., Hosseini S.A.A.M., Marashifard M., Yazdanpanah M., Emaneini M., Gharibpour F., Mirzaii M., Darban-Sarokhalil D., Moein M.. High frequency of multidrug-resistant Staphylococcus aureus with Scc, Mec, Type III, and Spa types T037 and T631 isolated from burn patients in southwest Iran. Apmis 2016;124:221–228.
    doi: 10.1111/apm.12493pubmed: 26709106google scholar: lookup
  3. Paschalis-Trela K., Cywinska A.. The prevalence of ocular diseases in Polish Arabian horses. BMC Vet. Res. 2017;13:319.
    doi: 10.1186/s12917-017-1252-8pmc: PMC5678559pubmed: 29115950google scholar: lookup
  4. Gilger B.C., Deeg C.. Equine Ophthalmology. Elsevier; Amsterdam, The Netherlands: 2011. Equine recurrent uveitis; pp. 317–349.
  5. Johns I.C., Baxter K., Booler H., Hicks C., Menzies-Gow N.. Conjunctival bacterial and fungal flora in healthy horses in the UK. Vet. Ophthalmol. 2011;14:195–199.
    doi: 10.1111/j.1463-5224.2010.00867.xpubmed: 21521444google scholar: lookup
  6. Foti M., Fisichella V., Giacopello C.. Detection of methicillin-resistant Staphylococcus aureus (MRSA) in the microbial flora from the conjunctiva of healthy donkeys from Sicily (Italy). Vet. Ophthalmol. 2013;16:89–92.
    doi: 10.1111/j.1463-5224.2012.01028.xpubmed: 22520064google scholar: lookup
  7. Camargo I.L.B.C., Gilmore M.S.. Staphylococcus aureus—Probing for host weakness?. J. Bacteriol. 2008;190:2253–2256.
    doi: 10.1128/JB.00043-08pmc: PMC2293175pubmed: 18223088google scholar: lookup
  8. Wieler L.H., Ewers C., Guenther S., Walther B., Lübke-Becker A.. Methicillin-resistant staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)-producing enterobacteriaceae in companion animals: Nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. Int. J. Med. Microbiol. 2011;301:635–641.
    pubmed: 22000738
  9. Walther B., Tedin K., Lübke-Becker A.. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet. Microbiol. 2017;200:71–78.
    doi: 10.1016/j.vetmic.2016.05.017pubmed: 27291944google scholar: lookup
  10. Baptiste K.E., Williams K., Willams N.J., Wattret A., Clegg P.D., Dawson S., Corkill J.E., O’Neill T., Hart C.A.. Methicillin-resistant staphylococci in companion animals. Emerg. Infect. Dis. 2005;11:1942.
    doi: 10.3201/eid1112.050241pmc: PMC3367626pubmed: 16485485google scholar: lookup
  11. Vengust M., Anderson M.E.C., Rousseau J., Weese J.S.. Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Lett. Appl. Microbiol. 2006;43:602–606.
    doi: 10.1111/j.1472-765X.2006.02018.xpubmed: 17083704google scholar: lookup
  12. Weese J.S., Rousseau J., Traub-Dargatz J.L., Willey B.M., McGeer A.J., Low D.E.. Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. J. Am. Vet. Med. Assoc. 2005;226:580–583.
    doi: 10.2460/javma.2005.226.580pubmed: 15742700google scholar: lookup
  13. Leonard F.C., Markey B.K.. Methicillin-resistant Staphylococcus aureus in animals: A review. Vet. J. 2008;175:27–36.
    doi: 10.1016/j.tvjl.2006.11.008pubmed: 17215151google scholar: lookup
  14. Strommenger B., Kehrenberg C., Kettlitz C., Cuny C., Verspohl J., Witte W., Schwarz S.. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. J. Antimicrob. Chemother. 2006;57:461–465.
    doi: 10.1093/jac/dki471pubmed: 16387748google scholar: lookup
  15. van Duijkeren E., Moleman M., van Oldruitenborgh-Oosterbaan M.M.S., Multem J., Troelstra A., Fluit A.C., Van Wamel W.B.J., Houwers D.J., De Neeling A.J., Wagenaar J.A.. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: An investigation of several outbreaks. Vet. Microbiol. 2010;141:96–102.
    doi: 10.1016/j.vetmic.2009.08.009pubmed: 19740613google scholar: lookup
  16. Waqar N., Amin Q., Munir T., Ikram M.S., Shahzad N., Mirza A., Ali A., Arshad M.I.. A cross-sectional study of methicillin-resistant Staphylococcus aureus at the equine-human interface. Trop. Anim. Health Prod. 2019;51:1927–1933.
    doi: 10.1007/s11250-019-01888-0pubmed: 30972624google scholar: lookup
  17. Plummer C.E.. Corneal response to injury and infection in the horse. Vet. Clin. Equine Pract. 2017;33:439–463.
    doi: 10.1016/j.cveq.2017.07.002pubmed: 28985985google scholar: lookup
  18. Walther B., Wieler L.H., Friedrich A.W., Hanssen A.M., Kohn B., Brunnberg L., Lübke-Becker L.. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations. Vet. Microbiol. 2008;127:171–178.
    doi: 10.1016/j.vetmic.2007.07.018pubmed: 17804179google scholar: lookup
  19. Vincze S., Stamm I., Kopp P.A., Hermes J., Adlhoch C., Semmler T., Wieler L.H., 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:e85656.
    doi: 10.1371/journal.pone.0085656pmc: PMC3896405pubmed: 24465637google scholar: lookup
  20. Diene S.M., Corvaglia A.R., François F., van der Mee-Marquet N.. Prophages and adaptation of Staphylococcus aureus St398 to the human clinic. BMC Genom. 2017;18:133.
    doi: 10.1186/s12864-017-3516-xpmc: PMC5294865pubmed: 28166723google scholar: lookup
  21. Ferreira A.R.d.A., Santana A.F., Almeida A.C.d.V.R., Sousa R.F., Perecmanis S., Galera P.D.. Bacterial culture and antibiotic sensitivity from the ocular conjunctiva of horses. Ciência Rural 2017;47:19.
    doi: 10.1590/0103-8478cr20160753google scholar: lookup
  22. Kahlmeter G., Brown D.F., Goldstein F.W., MacGowan A.P., Mouton J.W., Odenholt I., Rodloff A., Soussy C.J., Steinbakk M., Soriano F.. European Committee on Antimicrobial Susceptibility Testing (EUCAST) technical notes on antimicrobial susceptibility testing. Clin. Microbiol. Infect. 2006;12:501–503.
    doi: 10.1111/j.1469-0691.2006.01454.xpubmed: 16700696google scholar: lookup
  23. Sauer P., Andrew S.E., Lassaline M., Gelatt K.N., Denis H.M.. Changes in antibiotic resistance in equine bacterial ulcerative keratitis (1991–2000): 65 horses. Vet. Ophthalmol. 2003;6:309–313.
    doi: 10.1111/j.1463-5224.2003.00312.xpubmed: 14641828google scholar: lookup
  24. Wada S., Hobo S., Niwa H.. Ulcerative keratitis in thoroughbred racehorses in Japan from 1997 to 2008. Vet. Ophthalmol. 2010;13:99–105.
    doi: 10.1111/j.1463-5224.2010.00767.xpubmed: 20447028google scholar: lookup
  25. Kuroda T., Kinoshita Y., Niwa H., Mizobe F., Ueno T., Kuwano A., Hatazoe T., Hobo S.. Methicillin-resistant Staphylococcus aureus ulcerative keratitis in a thoroughbred racehorse. J. Equine Sci. 2015;26:95–98.
    doi: 10.1294/jes.26.95pmc: PMC4591416pubmed: 26435683google scholar: lookup
  26. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J.. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  27. Thompson J.D., Higgins D.G., Gibson T.J.. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680.
    doi: 10.1093/nar/22.22.4673pmc: PMC308517pubmed: 7984417google scholar: lookup
  28. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. Mega6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729.
    doi: 10.1093/molbev/mst197pmc: PMC3840312pubmed: 24132122google scholar: lookup
  29. Momtaz H., Dehkordi F.S., Rahimi E., Asgarifar A., Momeni M.. Virulence genes and antimicrobial resistance profiles of Staphylococcus aureus isolated from chicken meat in Isfahan Province, Iran. J. Appl. Poult. Res. 2013;22:913–921.
    doi: 10.3382/japr.2012-00673google scholar: lookup
  30. Gao J., Ferreri M., Liu X.Q., Chen L.B., Su J.L., Han B.. Development of multiplex polymerase chain reaction assay for rapid detection of Staphylococcus aureus and selected antibiotic resistance genes in bovine mastitic milk samples. J. Vet. Diagn. Investig. 2011;23:894–901.
    doi: 10.1177/1040638711416964pubmed: 21908344google scholar: lookup
  31. McClure J.A., Conly J.M., Lau V., Elsayed S., Louie T., Hutchins W., Zhang K.. Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from resistant staphylococci. J. Clin. Microbiol. 2006;44:1141–1144.
    doi: 10.1128/JCM.44.3.1141-1144.2006pmc: PMC1393128pubmed: 16517915google scholar: lookup
  32. Kumar J., Dinesh Y.K.N., Gaur A., Khanna D.. Detection of virulence genes in Staphylococcus aureus isolated from paper currency. Int. J. Infect. Dis. 2009;13:e450–e455.
    doi: 10.1016/j.ijid.2009.02.020pubmed: 19477670google scholar: lookup
  33. 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.42.11.4947-4955.2004pmc: PMC525205pubmed: 15528678google scholar: lookup
  34. Tamilmahan P., Zama M.M.S., Pathak R., Muneeswaran N.S., Karthik K.. A retrospective study of ocular occurrence in domestic animals: 799 cases. Vet. World. 2013;6:274–276.
    doi: 10.5455/vetworld.2013.274-276google scholar: lookup
  35. Scantlebury C.E., Aklilu N., Reed K., Knottenbelt D.C., Gebreab F., Pinchbeck G.L.. Ocular disease in working horses in Ethiopia: A cross-sectional study. Vet. Rec. 2013;172:99.
    doi: 10.1136/vr.100802pubmed: 23155077google scholar: lookup
  36. Vola M.E., Moriyama A.S., Lisboa R., Vola M.M., Hirai F.E., Bispo P.J.M., Höfling-Lima A.L.. Prevalence and antibiotic susceptibility of methicillin-resistant Staphylococcus aureus in ocular infections. Arq. Bras. Oftalmol. 2013;76:350–353.
    doi: 10.1590/S0004-27492013000600006pubmed: 24510081google scholar: lookup
  37. Malalana F., McGowan T.W., Ireland J.L., Pinchbeck G.L., McGowan C.M.. Prevalence of owner-reported ocular problems and veterinary ocular findings in a population of horses aged ≥15 years. Equine Vet. J. 2019;51:212–217.
    doi: 10.1111/evj.13005pubmed: 30080275google scholar: lookup
  38. Ramesh S., Ramakrishnan R., Bharathi M.J., Amuthan M., Viswanathan S.. Prevalence of bacterial pathogens causing ocular infections in South India. Indian J. Pathol. Microbiol. 2010;53:281.
    pubmed: 20551533
  39. Timney B., Macuda T.. Vision and hearing in horses. J. Am. Vet. Med. Assoc. 2001;218:1567–1574.
    doi: 10.2460/javma.2001.218.1567pubmed: 11393366google scholar: lookup
  40. Plata K., Rosato A.E., Wegrzyn G.. Staphylococcus aureus as an infectious agent: Overview of biochemistry and molecular genetics of its pathogenicity. Acta Biochim. Pol. 2009;56:597–612.
    doi: 10.18388/abp.2009_2491pubmed: 20011685google scholar: lookup
  41. Chambers H.F., DeLeo F.R.. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009;7:629–641.
    doi: 10.1038/nrmicro2200pmc: PMC2871281pubmed: 19680247google scholar: lookup
  42. Soimala T., Lübke-Becker A., Schwarz S., Feßler A.T., Huber C., Semmler T., Merle R., Gehlen H., Eule J.C., Walther B.. Occurrence and molecular composition of methicillin-resistant Staphylococcus aureus isolated from ocular surfaces of horses presented with ophthalmologic disease. Vet. Microbiol. 2018;222:1–6.
    doi: 10.1016/j.vetmic.2018.06.009pubmed: 30080662google scholar: lookup
  43. Bagga B., Reddy A.K., Garg P.. Decreased susceptibility to quinolones in methicillin-resistant Staphylococcus aureus isolated from ocular infections at a tertiary eye care centre. Br. J. Ophthalmol. 2010;94:1407–1408.
    doi: 10.1136/bjo.2010.179747pubmed: 20576768google scholar: lookup
  44. Schmitz F.J., Krey A., Sadurski R., Verhoef J., Milatovic D., Fluit A.C.. Resistance to tetracycline and distribution of tetracycline resistance genes in European Staphylococcus aureus isolates. J. Antimicrob. Chemother. 2001;47:239–240.
    doi: 10.1093/jac/47.2.239pubmed: 11157916google scholar: lookup
  45. Zilberberg M.D., Shorr A.F., Kollef M.F.. Growth and geographic variation in hospitalizations with resistant infections, United States, 2000–2005. Emerg. Infect. Dis. 2008;14:1756.
    doi: 10.3201/eid1411.080337pmc: PMC2630735pubmed: 18976563google scholar: lookup
  46. Lakshmi V., Ashok R., Susmita J., Shailaja V.V.. Changing trends in the antibiograms of Salmonella isolates at a tertiary care hospital in Hyderabad. Indian J. Med. Microbiol. 2006;24:45–48.
    doi: 10.1016/S0255-0857(21)02470-1pubmed: 16505555google scholar: lookup
  47. Hammad O.M., Hifnawy T., Omran D., Tantawi M.A.E., Girgis N.I.. Ceftriaxone versus chloramphenicol for treatment of acute typhoid fever. Life Sci. J. 2011;8:100–105.
  48. Graille M., Stura E.A., Corper A.L., Sutton B.J., Taussig M.J., Charbonnier J.-B., Silverman G.J.. Crystal structure of a Staphylococcus aureus protein A domain complexed with the Fab fragment of a human IgM antibody: Structural basis for recognition of B-cell receptors and superantigen activity. Proc. Natl. Acad. Sci. USA 2000;97:5399–5404.
    doi: 10.1073/pnas.97.10.5399pmc: PMC25840pubmed: 10805799google scholar: lookup
  49. Keener A.B., Thurlow L.T., Kang S.A., Spidale N.A., Clarke S.H., Cunnion K.M., Tisch R., Richardson A.R., Vilen B.J.. Staphylococcus aureus protein A disrupts immunity mediated by long-lived plasma cells. J. Immunol. 2017;198:1263–1273.
    doi: 10.4049/jimmunol.1600093pmc: PMC5266639pubmed: 28031339google scholar: lookup
  50. Shopsin B., Gomez M., Montgomery S.O., Smith D.H., Waddington M., Dodge D.E., Bost D.A., Riehman M., Naidich S., Kreiswirth B.N.. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J. Clin. Microbiol. 1999;37:3556–3563.
    doi: 10.1128/JCM.37.11.3556-3563.1999pmc: PMC85690pubmed: 10523551google scholar: lookup
  51. Asadollahi P., Farahani N.N., Mirzaii M., Khoramrooz S.S., Van Belkum A., Asadollahi K., Dadashi M., Darban-Sarokhalil D.. Distribution of the most prevalent Spa types among clinical isolates of methicillin-resistant and-susceptible Staphylococcus aureus around the world: A review. Front. Microbiol. 2018;9:163.
    doi: 10.3389/fmicb.2018.00163pmc: PMC5816571pubmed: 29487578google scholar: lookup
  52. Van der Donk C.F.M., Schols J.M.G.A., Schneiders V., Grimm K.-H., Stobberingh E.E.. Antibiotic resistance, population structure and spread of Staphylococcus aureus in nursing homes in the Euregion Meuse-Rhine. Eur. J. Clin. Microbiol. Infect. Dis. 2013;32:1483–1489.
    doi: 10.1007/s10096-013-1901-1pubmed: 23733319google scholar: lookup
  53. Berends E.T.M., Horswill A.R., Haste N.M., Monestier M., Nizet V., von Köckritz-Blickwede M.. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2010;2:576–586.
    doi: 10.1159/000319909pmc: PMC2982853pubmed: 20829609google scholar: lookup
  54. Mann E.E., Rice K.C., Boles B.R., Endres J.L., Ranjit D., Chandramohan L., Tsang L.H., Smeltzer M.S., Horswill A.R., Bayles K.W.. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE 2009;4:e5822.
    doi: 10.1371/journal.pone.0005822pmc: PMC2688759pubmed: 19513119google scholar: lookup
  55. Kiedrowski M.R., Kavanaugh J.S., Malone C.L., Mootz J.M., Voyich J.M., Smeltzer M.S., Bayles K.W., Horswill A.R.. Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS ONE 2011;6:e26714.
    doi: 10.1371/journal.pone.0026714pmc: PMC3214024pubmed: 22096493google scholar: lookup
  56. Hoegh S.V., Skov M.N., Boye K., Worning P., Jensen T.G., Kemp M.. Variations in the Staphylococcus aureus-specific nuc gene can potentially lead to misidentification of methicillin-susceptible and-resistant S. aureus. J. Med. Microbiol. 2014;63:1020–1022.
    doi: 10.1099/jmm.0.076638-0pubmed: 24809385google scholar: lookup
  57. Wang X., Li X., Liu W., Huang W., Fu Q., Li M.. Molecular characteristic and virulence gene profiles of community-associated methicillin-resistant Staphylococcus aureus isolates from pediatric patients in Shanghai, China. Front. Microbiol. 2016;7:1818.
    doi: 10.3389/fmicb.2016.01818pmc: PMC5108810pubmed: 27895635google scholar: lookup
  58. Zarizal S., Yeo C.C., Faizal G.M., Hoong C., Chew Z.A.Z., Al-Obaidi M.M.J., Amin N.S., Nasir M.D.M.. Nasal colonisation, antimicrobial susceptibility and genotypic pattern of Staphylococcus aureus among agricultural biotechnology students in Besut, Terengganu, east coast of Malaysia. Trop. Med. Int. Health. 2018;23:905–913.
    doi: 10.1111/tmi.13090pubmed: 29873865google scholar: lookup

Citations

This article has been cited 3 times.
  1. Khalid E, Tartor YH, Ammar AM, Abdelaziz R, Mahmmod Y, Abdelkhalek A. Controlling drug-resistant bacteria in Arabian horses: bacteriophage cocktails for treating wound infections. Front Vet Sci 2025;12:1609955.
    doi: 10.3389/fvets.2025.1609955pubmed: 41169678google scholar: lookup
  2. Okorie-Kanu OJ, Anyanwu MU, Nwobi OC, Tambe-Ebot RY, Ikenna-Ezeh NH, Okolo CC, Obodoechi LO, Ugwu PC, Okosi IR, Jaja IF, Oguttu JW. Prevalence, Antimicrobial Resistance, and Virulence Potential of Staphylococcus aureus in Donkeys from Nigeria. Antibiotics (Basel) 2025 Apr 29;14(5).
    doi: 10.3390/antibiotics14050453pubmed: 40426520google scholar: lookup
  3. Shaheen R, El-Abasy M, El-Sharkawy H, Ismail MM. Prevalence, molecular characterization, and antimicrobial resistance among Escherichia coli, Salmonella spp., and Staphylococcus aureus strains isolated from Egyptian broiler chicken flocks with omphalitis. Open Vet J 2024 Jan;14(1):284-291.
    doi: 10.5455/OVJ.2024.v14.i1.25pubmed: 38633165google scholar: lookup
Subscribe to our newsletter
Join 99,780 horse owners like you who receive our email updates on horse health and nutrition.