Analyze Diet
BMC veterinary research2022; 18(1); 79; doi: 10.1186/s12917-021-03053-y

Prevalence and WGS-based characteristics of Staphylococcus aureus in the nasal mucosa and pastern of horses with equine pastern dermatitis.

Abstract: Many contributing factors are involved in the development of equine pastern dermatitis (EPD). Among the most frequently suspected is Staphylococcus aureus, known for its pathogenic potential in skin and soft tissue infections. We therefore investigated the association between S. aureus carriage and EPD. Results: One hundred five EPD-affected horses and 95 unaffected controls were examined for the presence of methicillin-resistant and -susceptible Staphylococcus aureus (MRSA and MSSA) on the pastern skin and in the nostrils. S. aureus isolates were cultivated from swab samples on selective MSSA and MRSA chromogenic agar and identified using MALDI-TOF MS. Isolates were analysed by Illumina whole genome sequencing for genetic relatedness (cgMLST, spa typing), and for the presence of antimicrobial resistance and virulence determinants. A markedly higher proportion of samples from EPD-affected horses proved positive for S. aureus, both from the pastern (59.0 % vs. 6.3 % in unaffected horses; P<0.001), and from the nose (59.0 % vs. 8.4 %; P<0.001). Isolates belonged to 20 sequence types (ST) with lineages ST15-t084 (spa) (18 %), ST1-t127 (13 %), and ST1-t1508 (12 %) being predominant. Eight S. aureus were MRSA ST398-t011 and ST6239-t1456, and contained the staphylococcal cassette chromosome SCCmecIVa. Antimicrobial resistance genes were almost equally frequent in pastern and in nasal samples, whereas some virulence factors such as the beta-hemolysin, ESAT-6 secretion system, and some enterotoxins were more abundant in isolates from pastern samples, possibly enhancing their pathogenic potential. Conclusions: The markedly higher prevalence of S. aureus containing specific virulence factors in affected skin suggests their contribution in the development and course of EPD.
Publication Date: 2022-02-24 PubMed ID: 35209904PubMed Central: PMC8867626DOI: 10.1186/s12917-021-03053-yGoogle 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.
  • 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.

This research study investigates the correlation between Staphylococcus aureus, a bacteria commonly implicated in skin and soft tissue infections, and equine pastern dermatitis (EPD) in horses. The team discovered that the presence of this bacteria alongside certain virulence factors was noticeably higher in horses with the disease versus unaffected controls, suggesting that Staphylococcus aureus could be contributing to the development and progress of the ailment.

Objective of the Study

  • This study aimed to determine whether Staphylococcus aureus played a critical role in the onset and progress of equine pastern dermatitis (EPD) in horses. To do this, the team analyzed samples from both EPD-affected and unaffected horses, looking specifically for methicillin-resistant and susceptible strains of this bacteria.

Methodology

  • The researchers amassed swab samples from the pastern skin and nostrils of 105 horses affected by EPD and 95 unaffected horses. They cultured these samples on selective agar to encourage the growth of Staphylococcus aureus.
  • The team identified the resulting bacteria cultures using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS).
  • They then used whole-genome sequencing to study the genetic relatedness of their isolates, as well as to identify the presence of antimicrobial resistance and virulence determinants.

Results

  • The investigation revealed a notably higher positivity rate for Staphylococcus aureus in samples taken from EPD-affected horses, in both skin and nostril swabs.
  • Generated isolates belonged to 20 unique sequence types (ST), with certain types being more predominant than others. Eight of the isolates were found to be methicillin-resistant S. aureus (MRSA) and contained the SCCmecIVa gene.
  • Levels of antimicrobial resistance genes tended to be similar in samples from the pastern and nasal sites. However, certain virulence factors appeared more frequently in pastern sample isolates, suggesting an increased potential for disease induction.

Conclusions

  • The significantly increased presence of Staphylococcus aureus in horses with EPD implies a connection between this bacteria and the disease. Certain virulence factors were found more so in the affected skin samples, further suggesting that the presence of this bacteria might stimulate the progression of EPD.

Cite This Article

APA
Kaiser-Thom S, Gerber V, Collaud A, Hurni J, Perreten V. (2022). Prevalence and WGS-based characteristics of Staphylococcus aureus in the nasal mucosa and pastern of horses with equine pastern dermatitis. BMC Vet Res, 18(1), 79. https://doi.org/10.1186/s12917-021-03053-y

Publication

ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 18
Issue: 1
Pages: 79

Researcher Affiliations

Kaiser-Thom, Sarah
  • Department of Clinical Veterinary Medicine, Vetsuisse Faculty, Swiss Institute of Equine Medicine (ISME), University of Bern, and Agroscope, Bern, Switzerland.
Gerber, Vinzenz
  • Department of Clinical Veterinary Medicine, Vetsuisse Faculty, Swiss Institute of Equine Medicine (ISME), University of Bern, and Agroscope, Bern, Switzerland.
Collaud, Alexandra
  • Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Hurni, Joel
  • Department of Clinical Veterinary Medicine, Vetsuisse Faculty, Swiss Institute of Equine Medicine (ISME), University of Bern, and Agroscope, Bern, Switzerland.
  • Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
Perreten, Vincent
  • Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Bern, Bern, Switzerland. vincent.perreten@vetsuisse.unibe.ch.

MeSH Terms

  • Animals
  • Anti-Bacterial Agents
  • Dermatitis / veterinary
  • Horse Diseases / epidemiology
  • Horses / genetics
  • Methicillin-Resistant Staphylococcus aureus
  • Microbial Sensitivity Tests / veterinary
  • Nasal Mucosa
  • Prevalence
  • Staphylococcal Infections / epidemiology
  • Staphylococcal Infections / veterinary
  • Staphylococcus aureus
  • Virulence Factors / genetics
  • Whole Genome Sequencing / veterinary

Grant Funding

  • REF-37-075 / Bundesamt für Lebensmittelsicherheit und Veterinärwesen
  • REF-33-890 / ISMEquine Research Fund
  • REF-660-50 / Institute of Veterinary Bacteriology

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 65 references
  1. Yu AA. Equine pastern dermatitis. Vet Clin North Am Equine Pract 2013;29:577–88.
    pubmed: 24267676
  2. Scott DW, Miller WH Jr. Pastern Dermatitis. In: Scott DW, Miller WH, eds. Equine Dermatology, 2nd ed. Maryland Heights: Saunders Elsevier 2011; 260–261.
  3. Marsella R. Clinical approach to pastern dermatitis. Manual of Equine Dermatology. Wallingford: CAB International; 2019. pp. 110–8.
  4. Tong SYC, Davis JS, Eichenberger E, Holland TL, Fowler VG. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015;28:603–61.
    pmc: PMC4451395pubmed: 26016486
  5. Peton V, Le Loir Y. Staphylococcus aureus in veterinary medicine. Infect Genet Evol 2014;21:602–15.
    pubmed: 23974078
  6. Poulakou G, Lagou S, Tsiodras S. What’s new in the epidemiology of skin and soft tissue infections in 2018?. Curr Opin Infect Dis 2019;32:77–86.
    pubmed: 30664027
  7. Colles CM, Colles KM, Galpin JR. Equine pastern dermatitis. Equine Vet Educ 2010;22:566–70.
  8. Watson R. Wet skin conditions: the scourge of the UK winter. Equine Health 2017;2017:34–6.
  9. Nagase N, Sasaki A, Yamashita K, Shimizu A, Wakita Y, Kitai S. Isolation and species distribution of staphylococci from animal and human skin. J Vet Med Sci 2002;64:245–50.
    pubmed: 11999444
  10. Sangiorgio D, Hilty M, Kaiser-Thom S, Epper P, Ramseyer A, Overesch G. The influence of clinical severity and antibiotic treatment on bacteriological culture and the microbiota of equine pastern dermatitis. Vet Dermatol 2021;32(2):173-e41.
    pmc: PMC8048527pubmed: 33417744
  11. Busscher JF, Van Duijkeren E, Sloet Van Oldruitenborgh-Oosterbaan MM. The prevalence of methicillin-resistant staphylococci in healthy horses in the Netherlands. Vet Microbiol 2006;113:131–6.
    pubmed: 16303264
  12. Weese JS. Methicillin-resistant Staphylococcus aureus in horses and horse personnel. Vet Clin North Am Equine Pract 2004;20:601–13.
    pubmed: 15519821
  13. Wertheim HFL, Melles DC, Vos MC, Van Leeuwen W, Van Belkum A, Verbrugh HA. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5(12):751–62.
    pubmed: 16310147
  14. 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 2017;8:543.
    pmc: PMC5376617pubmed: 28421046
  15. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 1999;67:5427–33.
    pmc: PMC96900pubmed: 10496925
  16. Yoong P, Torres VJ. The effects of Staphylococcus aureus leukotoxins on the host: Cell lysis and beyond. Curr Opin Microbiol 2013;16:63–9.
    pmc: PMC3670676pubmed: 23466211
  17. Anderson M, Aly KA, Chen YH, Missiakas D. Secretion of atypical protein substrates by the ESAT-6 Secretion System of Staphylococcus aureus. Mol Microbiol 2013;90:734–43.
    pmc: PMC3951145pubmed: 24033479
  18. Mietrach N, Damián-Aparicio D, Mielich-Süss B, Lopez D, Geibel S. Substrate interaction with the EssC coupling protein of the type VIIb secretion system. J Bacteriol 2020;202:646–65.
    pmc: PMC7167477pubmed: 31964696
  19. Lindsay JA. Staphylococci. Evolving Genomes. Gram-Positive Pathog Washington, DC, USA: ASM Press; 2019. pp. 485–98.
  20. Monaco M, Pimentel de Araujo F, Cruciani M, Coccia EM, Pantosti A. Worldwide epidemiology and antibiotic resistance of Staphylococcus aureus. Curr Top Microbiol Immunol 2017;409:21–56.
    pubmed: 27025380
  21. Peacock SJ, Paterson GK. Mechanisms of methicillin resistance in Staphylococcus aureus. Annu Rev Biochem 2015;84:577–601.
    pubmed: 26034890
  22. Lakhundi S, Zhang K. Methicillin-resistant Staphylococcus aureus: Molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 2018;31(4):e00020-18.
    pmc: PMC6148192pubmed: 30209034
  23. Watkins RR, Holubar M, David MZ. Antimicrobial resistance in methicillin-resistant Staphylococcus aureus to newer antimicrobial agents. Antimicrob Agents Chemother 2019;63(12):e01216-19.
    pmc: PMC6879266pubmed: 31527033
  24. Fowler PW, Cole K, Gordon NC, Kearns AM, Llewelyn MJ, Peto TEA. Robust Prediction of resistance to trimethoprim in Staphylococcus aureus. Cell Chem Biol 2018;25:339.
    pubmed: 29307840
  25. Schindler BD, Kaatz GW. Multidrug efflux pumps of Gram-positive bacteria. Drug Resist Updat 2016;27:1–13.
    pubmed: 27449594
  26. Devriese LA, Nzuambe D, Godard C. Identification and characteristics of staphylococci isolated from lesions and normal skin of horses. Vet Microbiol 1984;10:269–77.
    pubmed: 3159146
  27. Chiers K, Decostere A, Devriese LA, Haesebrouck F. Bacteriological and mycological findings, and in vitro antibiotic sensitivity of pathogenic staphylococci in equine skin infections. Vet Rec 2003;152:138–41.
    pubmed: 12585601
  28. Knottenbelt D. A frustrating condition - pastern dermatitis syndrome. Equine Heal 2013;2013:27–30.
  29. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 1997;10:505–20.
    pmc: PMC172932pubmed: 9227864
  30. von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med 2001;344:11–6.
    pubmed: 11136954
  31. Kamus LJ, Theoret C, Costa MC. Use of next generation sequencing to investigate the microbiota of experimentally induced wounds and the effect of bandaging in horses. PLoS One 2018;13:1–18.
    pmc: PMC6261015pubmed: 30475922
  32. Ross AA, Rodrigues Hoffmann A, Neufeld JD. The skin microbiome of vertebrates. Microbiome 2019;7:1–14.
    pmc: PMC6533770pubmed: 31122279
  33. Kaiser-Thom S, Hilty M, Axiak S, Gerber V. The skin microbiota in equine pastern dermatitis: a case‐control study of horses in Switzerland. Vet Dermatol 2021 Apr 8. Epub ahead of print.
    pmc: PMC9290916pubmed: 33830562doi: 10.1111/vde.12955google scholar: lookup
  34. Wertheim HFL, Vos MC, Ott A, Van Belkum A, Voss A, Kluytmans JAJW. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 2004;364:703–5.
    pubmed: 15325835
  35. Weese JS, Archambault M, Willey BM, Dick H, Hearn P, Kreiswirth BN. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002. Emerg Infect Dis 2005;11:430–5.
    pmc: PMC3298236pubmed: 15757559
  36. Dastmalchi Saei H, Safari E. Methicillin resistance and clonal diversity of Staphylococcus aureus isolated from nasal samples of healthy horses in Iran. Ann Microbiol 2019;69:923–31.
  37. Mama OM, Gómez P, Ruiz-Ripa L, Gómez-Sanz E, Zarazaga M, Torres C. Antimicrobial resistance, virulence, and genetic lineages of staphylococci from horses destined for human consumption: High detection of S. aureus isolates of lineage ST1640 and those carrying the lukPQ gene. Animals 2019;9:900.
    pmc: PMC6912640pubmed: 31683871
  38. 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;17:471–8.
    pubmed: 21875361
  39. Scholtzek H, Walther E, Stöckle K. Molecular characterization of equine Staphylococcus aureus isolates exhibiting reduced oxacillin susceptibility. Toxins 2019;11:535.
    pmc: PMC6783909pubmed: 31540335
  40. Grinberg A, Biggs PJ, Zhang J, Ritchie S, Oneroa Z, O’Neill C. Genomic epidemiology of methicillin-susceptible Staphylococcus aureus across colonisation and skin and soft tissue infection. J Infect 2017;75:326–35.
    pubmed: 28782565
  41. Vali L, Dashti AA, Mathew F, Udo EE. Characterization of heterogeneous MRSA and MSSA with reduced susceptibility to chlorhexidine in Kuwaiti hospitals. Front Microbiol 2017;8:1359.
    pmc: PMC5517409pubmed: 28775716
  42. Franco A, Hasman H, Iurescia M, Lorenzetti R, Stegger M, Pantosti A. Molecular characterization of spa type t127, sequence type 1 methicillin-resistant Staphylococcus aureus from pigs. J Antimicrob Chemother 2011;66:1231–5.
    pubmed: 21447518
  43. Porrero MC, Mentaberre G, Sánchez S, Fernández-Llario P, Gómez-Barrero S, Navarro-Gonzalez N. Methicillin resistant Staphylococcus aureus (MRSA) carriage in different free-living wild animal species in Spain. Vet J 2013;198:127–30.
    pubmed: 23846031
  44. Earls MR, Kinnevey PM, Brennan GI, Lazaris A, Skally M, O’Connell B. The recent emergence in hospitals of multidrug-resistant community-associated sequence type 1 and spa type t127 methicillin-resistant Staphylococcus aureus investigated by whole-genome sequencing: Implications for screening. PLoS One 2017;12:e0175542.
    pmc: PMC5388477pubmed: 28399151
  45. Aspiroz C, Lozano C, Vindel A, Lasarte JJ, Zarazaga M, Torres C. Skin lesion caused by ST398 and ST1 MRSA, Spain. Emerg Infect Dis 2010;16:157–9.
    pmc: PMC2874358pubmed: 20031071
  46. Lozano C, Aspiroz C, Lasarte JJ, Gómez-Sanz E, Zarazaga M, Torres C. Dynamic of nasal colonization by methicillin-resistant Staphylococcus aureus ST398 and ST1 after mupirocin treatment in a family in close contact with pigs. Comp Immunol Microbiol Infect Dis 2011;34:e1–7.
    pubmed: 20663559
  47. Pilla R, Castiglioni V, Gelain ME, Scanziani E, Lorenzi V, Anjum M. Long-term study of MRSA ST1, t127 mastitis in a dairy cow. Vet Rec Case Reports 2013;1:e100510.
    pubmed: 22383329
  48. Sekizuka T, Niwa H, Kinoshita Y, Uchida-Fujii E, Inamine Y, Hashino M. Identification of a mecA/mecC-positive MRSA ST1-t127 isolate from a racehorse in japan. J Antimicrob Chemother 2020;75:292–5.
    pubmed: 31691809
  49. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS. Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in livestock. MBio 2012;3:1–6.
    pmc: PMC3280451pubmed: 22354957
  50. Huber H, Koller S, Giezendanner N, Stephan R, Zweifel C. Prevalence and characteristics of meticillin-resistant Staphylococcus aureus in humans in contact with farm animals, in livestock, and in food of animal origin, Switzerland, 2009. Eurosurveillance 2010;15:7–10.
    pubmed: 20430001
  51. Abdelbary MMH, Wittenberg A, Cuny C, Layer F, Kurt K, Wieler LH. Phylogenetic Analysis of Staphylococcus aureus CC398 reveals a sub-lineage epidemiologically associated with infections in horses. PLoS One 2014;9:e88083.
    pmc: PMC3913741pubmed: 24505386
  52. Korea CG, Balsamo G, Pezzicoli A, Merakou C, Tavarini S, Bagnoli F. Staphylococcal Esx proteins modulate apoptosis and release of intracellular Staphylococcus aureus during infection in epithelial cells. Infect Immun 2014;82:4144–53.
    pmc: PMC4187876pubmed: 25047846
  53. Burts ML, Williams WA, DeBord K, Missiakas DM. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci U S A 2005;102:1169–74.
    pmc: PMC545836pubmed: 15657139
  54. Katayama Y, Baba T, Sekine M, Fukuda M, Hiramatsu K. Beta-hemolysin promotes skin colonization by Staphylococcus aureus. J Bacteriol 2013;195:1194–203.
    pmc: PMC3592002pubmed: 23292775
  55. Thomas D, Chou S, Dauwalder O, Lina G. Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 2007;93:24-41.
    pubmed: 17369698
  56. Ortega E, Abriouel H, Lucas R, Gálvez A. Multiple roles of Staphylococcus aureus enterotoxins: Pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins 2010;2:2117–31.
    pmc: PMC3153285pubmed: 22069676
  57. Sau S, Bhasin N, Wann ER, Lee JC, Foster TJ, Lee CY. The Staphylococcus aureus allelic genetic loci for serotype 5 and 8 capsule expression contain the type-specific genes flanked by common genes. Microbiology 1997;143:2395–405.
    pubmed: 9245821
  58. Morinaga N, Kaihou Y, Noda M. Purification, cloning and characterization of variant luke-lukd with strong leukocidal activity of staphylococcal bi-component leukotoxin family. Microbiol Immunol 2003;47:81–90.
    pubmed: 12636257
  59. Laarman AJ, Ruyken M, Malone CL, van Strijp JAG, Horswill AR, Rooijakkers SHM. Staphylococcus aureus metalloprotease aureolysin cleaves complement C3 to mediate immune evasion. J Immunol 2011;186:6445–53.
    pubmed: 21502375
  60. Vandenesch F, Lina G, Henry T. Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors?. Front Cell Infect Microbiol 2012;2:12.
    pmc: PMC3417661pubmed: 22919604
  61. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–20.
    pmc: PMC4103590pubmed: 24695404
  62. 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;52:2365–70.
    pmc: PMC4097726pubmed: 24759713
  63. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C, Francisco AP. GrapeTree: Visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018;28:1395–404.
    pmc: PMC6120633pubmed: 30049790
  64. Letunic I, Bork P. Interactive Tree of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res 2019;47:W256–9.
    pmc: PMC6602468pubmed: 30931475
  65. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2018. Available online at https://www.R-project.org/.