Skip to main content

Advertisement

SpringerLink
Log in

Prevalence and characterization of Staphylococcus aureus isolated in raw milk from cows in Hokkaido, Japan

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

The aim of this study was to characterize the phenotypes and genotypes of Staphylococcus aureus isolated from raw bovine milk in Hokkaido, Japan. S. aureus isolates were identified in 135 of 436 milk samples from cows with and without signs of mastitis from three farms in Hokkaido. These clinical isolates were characterized for antimicrobial susceptibility patterns, molecular typing using phage-open-reading frame typing (POT), coagulase gene type, virulence genes, and biofilm-associated genes and were evaluated for biofilm-forming ability. Most isolates were susceptible to the antimicrobial agents tested. The highest rate of resistance was to ampicillin. Molecular typing of all S. aureus isolates indicated a predominance of coagulase type VI and 0–17–34 POT type, and virulence genes were highly prevalent in the isolates from all farms. Moreover, a high percentage of the 0-17–34 POT type isolates showed extensive formation of biofilm. These findings will help veterinarians and farmers to understand the epidemiology of S. aureus so that they can monitor the transmission and spread of this pathogen and control it more effectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aslantas, O. and Demir, C., 2016. Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. Journal of Dairy Science, 99, 8607–8613.

    Article  CAS  Google Scholar 

  • Baba, K., Ishihara, K., Ozawa, M., Usui, M., Hiki, M., Tamura, Y. and Asai, T., 2012. Prevalence and mechanism of antimicrobial resistance in Staphylococcus aureus isolates from diseased cattle, swine and chickens in Japan. Journal of Veterinary Medical Science, 74, 561–565.

    Article  CAS  Google Scholar 

  • Barkema, H.W., Schukken, Y.H. and Zadoks, R.N., 2006. Invited review: the role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. Journal of Dairy Science, 89, 1877–1895.

    Article  CAS  Google Scholar 

  • Bentley, S.D. and Parkhill, J., 2015. Genomic perspectives on the evolution and spread of bacterial pathogens. Proceedings of the Royal Society of London. Series B, Biological Sciences, 282, 20150488.

  • Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M. and Beachey, E. H., 1985. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. Journal of Clinical Microbiology, 22, 996–1006.

  • Clinical and Laboratory Standards Institute [CLSI], 2015. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. VET01S. Clinical and Laboratory Standards Institute. Wayne, PA.

  • Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I. and Penades, J. R. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. Journal of Bacteriology 183, 2888–2896.

    Article  CAS  Google Scholar 

  • Cucarella, C., Tormo, M.Á., Úbeda, C., Trotonda, M.P., Monzón, M., Peris, C., Amorena, B., Lasa, Í. and Penadés, J.R., 2004. Role of biofilm-associated protein Bap in the pathogenesis of bovine Staphylococcus aureus. Infection and Immunity, 72, 2177–2185.

    Article  CAS  Google Scholar 

  • Ferens, W.A., Davis, W.C., Hamilton, M.J., Park, Y.H., Deobald, C.F., Fox, L. and Bohach, G., 1998. Activation of bovine lymphocyte subpopulations by staphylococcal enterotoxin C. Infection and Immunity, 66, 573–580.

    Article  CAS  Google Scholar 

  • Gogoi-Tiwari, J., Williams, V., Waryah, C.B., Costantino, P., Al-Salami, H., Mathavan, S., Wells, K., Tiwari, H.K., Hegde, N., Isloor, S., Al-Sallami, H. and Mukkur, T., 2017. Mammary gland pathology subsequent to acute infection with strong versus weak biofilm forming staphylococcus aureus bovine mastitis isolates: A pilot study using non-invasive mouse mastitis model. PLoS One. 12, 1–19.

    Article  Google Scholar 

  • Guimaraes, F.F., Manzi, M.P., Joaquim, S.F., Richini-Pereira, V.B. and Langoni, H., 2017. Short communication: Outbreak of methicillin-resistant Staphylococcus aureus (MRSA)-associated mastitis in a closed dairy herd. Journal of Dairy Science, 100, 726–730.

    Article  CAS  Google Scholar 

  • Hata, E., 2016. Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus New York/Japan clone. Journal of Veterinary Diagnostic Investigation 28, 291–298.

    Article  CAS  Google Scholar 

  • Jarraud, S., Mougel, C., Thioulouse, J., Lina, G., Meugnier, H., Forey, F., Etienne, J., Vandenesch, F. and Nesme, X., 2002. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infection and Immunity, 70, 631–641.

    Article  CAS  Google Scholar 

  • Latasa, C., Solano, C., Penadés, J.R. and Lasa, I., 2006. Biofilm-associated proteins. Comptes Rendus Biologies, 329, 849–857.

    Article  CAS  Google Scholar 

  • Mehrotra, M., Wang, G., Johnson, W.M., 2000. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. Journal of Clinical Microbiology 38, 1032–1035.

    Article  CAS  Google Scholar 

  • Merritt, J. H., Kadouri, D. E. and O'Toole, G. A., 2005. Growing and analyzing static biofilms. Current Protocols in Microbiology. Chapter 1, Unit 1B 1.

  • Nada, T., Yagi, T., Ohkura, T., Morishita, Y., Baba, H., Ohta, M. and Suzuki, M., 2009. Usefulness of phage open-reading frame typing method in an epidemiological study of an outbreak of methicillin-resistant Staphylococcus aureus infections. Japanese Journal of Infectious Diseases, 62, 386–389.

    PubMed  Google Scholar 

  • Nagase, N., Shimizu, A., Kawano, J., Yamashita, K. and Yoshimura, H., 2002. Characterization of Staphylococcus aureus strains isolated from bovine mastitis in Japan. Journal of Veterinary Medical Science, 64, 1169–1172.

    Article  CAS  Google Scholar 

  • Paule, S. M., Pasquariello, A. C., Hacek, D. M., Fisher, A. G., Thomson, R. B., Jr., Kaul, K. L. and Peterson, L. R., 2004. Direct detection of Staphylococcus aureus from adult and neonate nasal swab specimens using real-time polymerase chain reaction. Journal of Molecular Diagnostics, 6, 191–196.

    Article  CAS  Google Scholar 

  • Pol, M. and Ruegg, P.L., 2007. Relationship between antimicrobial drug usage and antimicrobial susceptibility of gram-positive mastitis pathogens. Journal of Dairy Science, 90, 262–273.

    Article  CAS  Google Scholar 

  • Pitkälä, A., Haveri, M., Pyörälä, S., Myllys, V. and Honkanen-Buzalski, T., 2004. Bovine mastitis in Finland 2001—prevalence, distribution of bacteria, and antimicrobial resistance. Journal of Dairy Science, 87, 2433–2441.

    Article  Google Scholar 

  • Rayner, C. and Munckhof, W.J., 2005. Antibiotics currently used in the treatment of infections caused by Staphylococcus aureus. Internal Medicine Journal, 35, Suppl 2, S3–16.

    Article  CAS  Google Scholar 

  • Seegers, H., Fourichon, C. and Beaudeau, F., 2003. Production effects related to mastitis and mastitis economics in dairy cattle herds. Veterinary Research, 34, 475–491.

    Article  Google Scholar 

  • Sinha, M.K., Thombare, N.N. and Mondal, B., 2014. Subclinical mastitis in dairy animals: Incidence, economics, and predisposing factors. Scientific World Journal, 2014, 523984.

    PubMed  Google Scholar 

  • Srinivasan, V., Sawant, AA., Gillespie, B., Headrick, SJ., Ceasaris, L and, Oliver, S., 2006. Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathogens and Disease, 3, 274–283.

  • Suzuki, M., Tawada, Y., Kato, M., Hori, H., Mamiya, N., Hayashi, Y. and Sakae, K. 2006. Development of a rapid strain differentiation method for methicillin-resistant Staphylococcus aureus isolated in Japan by detecting phage-derived open-reading frames. Journal of Applied Microbiology, 101, 938–947.

    Article  CAS  Google Scholar 

  • Vrieling, M., Boerhout, E.M., Van Wigcheren, G.F., Koymans, K.J., Mols-Vorstermans, T.G., De Haas, C.J.C., Aerts, P.C., Daemen, I.J.J.M., Van Kessel, K.P.M., Koets, A.P., Rutten, V.P.M.G., Nuijten, P.J.M., Van Strijp, J.A.G. and Benedictus, L., 2016. LukMF′ is the major secreted leukocidin of bovine Staphylococcus aureus and is produced in vivo during bovine mastitis. Scientific Reports, 6, 1–12.

    Article  Google Scholar 

  • Wang, D., Wang, Z., Yan, Z., Wu, J., Ali, T., Li, J., Lv, Y. and Han, B., 2015. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infection Genetics and Evolution 31, 9–16.

    Article  Google Scholar 

  • Yamada, T., Tochimaru, N., Nakasuji, S., Hata, E., Kobayashi, H., Eguchi, M., Kaneko, J., Kamio, Y., Kaidoh, T. and Takeuchi, S., 2005. Leukotoxin family genes in Staphylococcus aureus isolated from domestic animals and prevalence of lukM-lukF-PV genes by bacteriophages in bovine isolates. Veterinary Microbiology, 110, 97–103.

    Article  CAS  Google Scholar 

  • Yousefi, M., Pourmand, M. R., Fallah, F., Hashemi, A., Mashhadi, R. and Nazari-Alam, A., 2016. Characterization of Staphylococcus aureus biofilm formation in urinary tract infection. Iranian Journal of Public Health, 45, 485–493.

Download references

Funding

This work was financially supported by Rakuno Gakuen University, Hokkaido, Japan.

Author information

Authors and Affiliations

  1. Department of Veterinary Public Health, Faculty of Veterinary Medicine, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, Thailand

    Sukanya Thongratsakul & Chaithep Poolkhet

  2. Laboratory of Food Microbiology and Food Safety, Department of Health and Environmental Sciences, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido, Japan

    Masaru Usui, Tomomi Sato & Yutaka Tamura

  3. Laboratory of Animal Health, Department of Health and Environmental Sciences, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido, Japan

    Hidetoshi Higuchi

  4. Livestock Hygiene, Department of Sustainable Agriculture, College of Agriculture, Rakuno Gakuen University, Ebetsu, Hokkaido, Japan

    Toshihiko Takahashi

Authors
  1. Sukanya Thongratsakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masaru Usui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hidetoshi Higuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toshihiko Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomomi Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chaithep Poolkhet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yutaka Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sukanya Thongratsakul.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thongratsakul, S., Usui, M., Higuchi, H. et al. Prevalence and characterization of Staphylococcus aureus isolated in raw milk from cows in Hokkaido, Japan. Trop Anim Health Prod 52, 1631–1637 (2020). https://doi.org/10.1007/s11250-019-02169-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-019-02169-6

Keywords

Search

Navigation