Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Analysis of virulence traits of Staphylococcus aureus isolated from bovine mastitis in semi-intensive and family dairy farms

  • Guzman-Rodriguez, Jaquelina J. (Life Science Division, Postgraduate Program in Bioscience, Irapuato-Salamanca Campus, University of Guanajuato) ;
  • Leon-Galvan, Ma. Fabiola (Life Science Division, Postgraduate Program in Bioscience, Irapuato-Salamanca Campus, University of Guanajuato) ;
  • Barboza-Corona, Jose E. (Life Science Division, Postgraduate Program in Bioscience, Irapuato-Salamanca Campus, University of Guanajuato) ;
  • Valencia-Posadas, Mauricio (Life Science Division, Postgraduate Program in Bioscience, Irapuato-Salamanca Campus, University of Guanajuato) ;
  • Loeza-Lara, Pedro D. (Department of Food Genomics, University of La Cienega of the State of Michoacan de Ocampo) ;
  • Sanchez-Ceja, Monica (Department of Food Genomics, University of La Cienega of the State of Michoacan de Ocampo) ;
  • Ochoa-Zarzosa, Alejandra (Multidisciplinary Center for Biotechnology Studies, Faculty of Veterinary Medicine and Zootechnics, Universidad Michoacana de San Nicolas de Hidalgo) ;
  • Lopez-Meza, Joel E. (Multidisciplinary Center for Biotechnology Studies, Faculty of Veterinary Medicine and Zootechnics, Universidad Michoacana de San Nicolas de Hidalgo) ;
  • Gutierrez-Chavez, Abner J. (Life Science Division, Postgraduate Program in Bioscience, Irapuato-Salamanca Campus, University of Guanajuato)
  • Received : 2020.04.08
  • Accepted : 2020.08.11
  • Published : 2020.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Staphylococcus aureus is one of the main microorganisms that causes bovine mastitis, and its well-known virulence characteristics and interactions with the environment are used to aid the design of more efficient therapies. Objectives: To determine whether the virulence traits, such as antibiotic resistance and biofilm-forming and internalization abilities, of S. aureus isolated from bovine mastitis are related to dairy production system types. Methods: The study was performed in the Mexican states of Guanajuato and Michoacan. Semi-intensive dairy farms (SIDFs) and family dairy farms (FDFs) (454 and 363 cows, respectively) were included. The 194 milk samples from mastitis affected quarters were collected and 92 strains of S. aureus were isolated and identified by biochemical and molecular tests. Antibiotic resistance, biofilm and internalization assays were performed on 30 randomly selected isolated strains to determine virulence traits, and these strains were equally allocated to the 2 dairy production systems. Results: All 30 selected strains displayed a high degree of resistance (50%-91.7%) to the antibiotics tested, but no significant difference was found between SIDF and FDF isolates. S. aureus strains from SIDFs had an average biofilm forming capacity of up to 36% (18.9%-53.1%), while S. aureus strains from FDFs registered an average of up to 53% (31.5%-77.8%) (p > 0.05). Internalization assays revealed a higher frequency of internalization capacity for strains isolated from FDFs (33.3%) than for those isolated from SIDFs (6.7%) (p > 0.05). fnbpA gen was detected in 46.6% of FDF strains and 33.3% of SIDF strains, and this difference was significant (p < 0.05). Conclusions: Our findings show that the virulence traits of S. aureus isolates analyzed in this study, depend significantly on several factors, such as phenotype, genotype, and environmental conditions, which are significantly related to dairy production system type and daily management practices.

Keywords

Acknowledgement

The authors thank students and colleagues at University of Guanajuato for their technical support and express their appreciation to the dairy producers for the contributions they made during this study.

References

  1. Argaw A. Review on epidemiology of clinical and subclinical mastitis on dairy cows. Food Sci Qual Manag. 2016;52(6):56-65.
  2. Monistero V, Graber HU, Pollera C, Cremonesi P, Castiglioni B, Bottini E, et al. Staphylococcus aureus isolates from bovine mastitis in eight countries: genotypes, detection of genes encoding different toxins and other virulence genes. Toxins (Basel). 2018;10(6):247. https://doi.org/10.3390/toxins10060247
  3. Thiran E, Di Ciccio PA, Graber HU, Zanardi E, Ianieri A, Hummerjohann J. Biofilm formation of Staphylococcus aureus dairy isolates representing different genotypes. J Dairy Sci. 2018;101(2):1000-1012. https://doi.org/10.3168/jds.2017-13696
  4. Dhanawade NB, Kalorey DR, Srinivasan R, Barbuddhe SB, Kurkure NV. Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis. Vet Res Commun. 2010;34(1):81-89. https://doi.org/10.1007/s11259-009-9326-0
  5. Pereyra EA, Picech F, Renna MS, Baravalle C, Andreotti CS, Russi R, et al. Detection of Staphylococcus aureus adhesion and biofilm-producing genes and their expression during internalization in bovine mammary epithelial cells. Vet Microbiol. 2016;183:69-77. https://doi.org/10.1016/j.vetmic.2015.12.002
  6. Alva-Murillo N, Lopez-Meza JE, Ochoa-Zarzosa A. Nonprofessional phagocytic cell receptors involved in Staphylococcus aureus internalization. Biomed Res Int. 2014;2014:538546. https://doi.org/10.1155/2014/538546
  7. Cote-Gravel J, Malouin F. Symposium review: features of Staphylococcus aureus mastitis pathogenesis that guide vaccine development strategies. J Dairy Sci. 2019;102(5):4727-4740. https://doi.org/10.3168/jds.2018-15272
  8. Val-Arreola D, Kebreab E, France J. Modeling small-scale dairy farms in central Mexico using multi-criteria programming. J Dairy Sci. 2006;89(5):1662-1672. https://doi.org/10.3168/jds.S0022-0302(06)72233-0
  9. Ministry of Agriculture, Livestock, Rural Development, Fisheries and Food (MX). Current Situation and Perspectives of Milk Production in Mexico: Economic Edition. Mexico City: SAGARPA; 2001.
  10. Ramirez-Rivera EJ, Rodriguez-Miranda J, Huerta-Mora IR, Cardenas-Cagal A, Juarez-Barrientos JM. Tropical milk production systems and milk quality: a review. Trop Anim Health Prod. 2019;51(6):1295-1305. https://doi.org/10.1007/s11250-019-01922-1
  11. Hogan JS, Gonzales RN, Harmon RJ, Nickerson SC, Oliver SP, Pankey JW, et al. Laboratory Handbook on Bovine Mastitis. New Prague: National Mastitis Council; 2009.
  12. Ochoa-Zarzosa A, Loeza-Lara PD, Torres-Rodriguez F, Loeza-Angeles H, Mascot-Chiquito N, Sanchez-Baca S, et al. Antimicrobial susceptibility and invasive ability of Staphylococcus aureus isolates from mastitis from dairy backyard systems. Antonie Van Leeuwenhoek. 2008;94(2):199-206. https://doi.org/10.1007/s10482-008-9230-6
  13. House HK, Anderson NG. Maximizing comfort in tiestall housing. Vet Clin North Am Food Anim Pract. 2019;35(1):77-91. https://doi.org/10.1016/j.cvfa.2018.10.004
  14. Metzger SA, Hernandez LL, Skarlupka JH, Suen G, Walker TM, Ruegg PL. Influence of sampling technique and bedding type on the milk microbiota: results of a pilot study. J Dairy Sci. 2018;101(7):6346-6356. https://doi.org/10.3168/jds.2017-14212
  15. Abebe R, Hatiya H, Abera M, Megersa B, Asmare K. Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at Hawassa milk shed, South Ethiopia. BMC Vet Res. 2016;12(1):270-281. https://doi.org/10.1186/s12917-016-0905-3
  16. Vakkamaki J, Taponen S, Heikkila AM, Pyorala S. Bacteriological etiology and treatment of mastitis in Finnish dairy herds. Acta Vet Scand. 2017;59(1):33-42. https://doi.org/10.1186/s13028-017-0301-4
  17. Varela-Ortiz DF, Barboza-Corona JE, Gonzalez-Marrero J, Leon-Galvan MF, Valencia-Posadas M, Lechuga-Arana AA, et al. Antibiotic susceptibility of Staphylococcus aureus isolated from subclinical bovine mastitis cases and in vitro efficacy of bacteriophage. Vet Res Commun. 2018;42(3):243-250. https://doi.org/10.1007/s11259-018-9730-4
  18. Ferreira AM, Martins KB, Silva VR, Mondelli AL, Cunha ML. Correlation of phenotypic tests with the presence of the blaZ gene for detection of beta-lactamase. Braz J Microbiol. 2017;48(1):159-166. https://doi.org/10.1016/j.bjm.2016.10.011
  19. Shrivastava N, Sharma V, Nayak A, Shrivastava AB, Sarkhel BC, Shukla PC, et al. Prevalence and characterization of methicillin-resistant Staphylococcus aureus (MRSA) mastitis in dairy cattle in Jabalpur, Madhya Pradesh. J Anim Res. 2017;7(1):77-84. https://doi.org/10.5958/2277-940X.2017.00011.0
  20. Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. Absence of the mecA gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi City, Sudan. Biomed Res Int. 2015;2015:895860. https://doi.org/10.1155/2015/895860
  21. Yang Y, Jiang X, Chai B, Ma L, Li B, Zhang A, et al. ARGs-OAP: online analysis pipeline for antibiotic resistance genes detection from metagenomic data using an integrated structured ARG-database. Bioinformatics. 2016;32(15):2346-2351. https://doi.org/10.1093/bioinformatics/btw136
  22. de Oliveira TL, Cavalcante FS, Chamon RC, Ferreira RB, Dos Santos KR. Genetic mutations in the quinolone resistance-determining region are related to changes in the epidemiological profile of methicillin-resistant Staphylococcus aureus isolates. J Glob Antimicrob Resist. 2019;19:236-240. https://doi.org/10.1016/j.jgar.2019.05.026
  23. Raza A, Muhammad G, Sharif S, Atta A. Biofilm producing Staphylococcus aureus and bovine mastitis: a review. Mol Microbiol Res. 2013;3:1-8.
  24. Balasubramanian D, Harper L, Shopsin B, Torres VJ. Staphylococcus aureus pathogenesis in diverse host environments. Pathog Dis. 2017;75(1):1-13.
  25. Stenz L, Francois P, Whiteson K, Wolz C, Linder P, Schrenzel J. The CodY pleiotropic repressor controls virulence in gram-positive pathogens. FEMS Immunol Med Microbiol. 2011;62(2):123-139. https://doi.org/10.1111/j.1574-695X.2011.00812.x
  26. Falaki B, Mahdavi S. Study of distribution of biofilm producing genes in Staphylococcus aureus isolated from local cheese samples in Maragheh city. Gene Cell Tissue. 2017;4(4):e66970.
  27. Notcovich S, DeNicolo G, Flint SH, Williamson NB, Gedye K, Grinberg A, et al. Biofilm-forming potential of Staphylococcus aureus isolated from bovine mastitis in New Zealand. Vet Sci. 2018;5(1):8. https://doi.org/10.3390/vetsci5010008
  28. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol. 2001;183(9):2888-2896. https://doi.org/10.1128/jb.183.9.2888-2896.2001
  29. Buzzola FR, Alvarez LP, Tuchscherr LP, Barbagelata MS, Lattar SM, Calvinho L, et al. Differential abilities of capsulated and noncapsulated Staphylococcus aureus isolates from diverse agr groups to invade mammary epithelial cells. Infect Immun. 2007;75(2):886-891. https://doi.org/10.1128/IAI.01215-06
  30. Murphy MP, Niedziela DA, Leonard FC, Keane OM. The in vitro host cell immune response to bovine-adapted Staphylococcus aureus varies according to bacterial lineage. Sci Rep. 2019;9(1):6134. https://doi.org/10.1038/s41598-019-42424-2
  31. Ahangari Z, Ghorbanpoor M, Shapouri MR, Gharibi D, Ghazvini K. Methicillin resistance and selective genetic determinants of Staphylococcus aureus isolates with bovine mastitis milk origin. Iran J Microbiol. 2017;9(3):152-159.
  32. Schroeder JW. Mastitis Control Program: Bovine Mastitis and Milking Management. AS-1129. Fargo: North Dakota State University; 1997.
  33. Firth CL, Laubichler C, Schleicher C, Fuchs K, Kasbohrer A, Egger-Danner C, et al. Relationship between the probability of veterinary-diagnosed bovine mastitis occurring and farm management risk factors on small dairy farms in Austria. J Dairy Sci. 2019;102(5):4452-4463. https://doi.org/10.3168/jds.2018-15657
  34. Richert RM, Cicconi KM, Gamroth MJ, Schukken YH, Stiglbauer KE, Ruegg PL. Management factors associated with veterinary usage by organic and conventional dairy farms. J Am Vet Med Assoc. 2013;242(12):1732-1743. https://doi.org/10.2460/javma.242.12.1732
  35. Chaiyabutr N. Control of mammary function during lactation in crossbred dairy cattle in the tropics. In: Milk Production - Advanced Genetic Traits, Cellular Mechanism, Animal Management and Health. London: IntechOpen; 2012, 127-154.
  36. Haltia L, Honkanen-Buzalski T, Spiridonova I, Olkonen A, Myllys V. A study of bovine mastitis, milking procedures and management practices on 25 Estonian dairy herds. Acta Vet Scand. 2006;48(1):22-28. https://doi.org/10.1186/1751-0147-48-22
  37. Hughes K, Watson CJ. The mammary microenvironment in mastitis in humans, dairy ruminants, rabbits and rodents: a one health focus. J Mammary Gland Biol Neoplasia. 2018;23(1-2):27-41. https://doi.org/10.1007/s10911-018-9395-1
  38. Hashem RA, Yassin AS, Zedan HH, Amin MA. Fluoroquinolone resistant mechanisms in methicillin-resistant Staphylococcus aureus clinical isolates in Cairo, Egypt. J Infect Dev Ctries. 2013;7(11):796-803. https://doi.org/10.3855/jidc.3105
  39. Frutis-Murillo M, Sandoval-Carrillo MA, Alva-Murillo N, Ochoa-Zarzosa A, Lopez-Meza JE. Immunomodulatory molecules regulate adhesin gene expression in Staphylococcus aureus: effect on bacterial internalization into bovine mammary epithelial cells. Microb Pathog. 2019;131(131):15-21. https://doi.org/10.1016/j.micpath.2019.03.030