J Vet Sci.  2010 Jun;11(2):125-131. 10.4142/jvs.2010.11.2.125.

spa typing and enterotoxin gene profile of Staphylococcus aureus isolated from bovine raw milk in Korea

Affiliations
  • 1Department of Microbiology, College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University, Seoul 151-742, Korea. yhp@snu.ac.kr

Abstract

Staphylococcus aureus is a major etiological pathogen of bovine mastitis, which triggers significant economic losses in dairy herds worldwide. In this study, S. aureus strains isolated from the milk of cows suffering from mastitis in Korea were investigated by spa typing and staphylococcal enterotoxin (SE) gene profiling. Forty-four S. aureus strains were isolated from 26 farms in five provinces. All isolates grouped into five clusters and two singletons based on 14 spa types. Cluster 1 and 2 isolates comprised 38.6% and 36.4% of total isolates, respectively, which were distributed in more than four provinces. SE and SE-like toxin genes were detected in 34 (77.3%) isolates and the most frequently detected SE gene profile was seg, sei, selm, seln, and selo genes (16 isolates, 36.3%), which was comparable to one of the genomic islands, Type I nuSabeta. This is a first report of spa types and the prevalence of the recently described SE and SE-like toxin genes among S. aureus isolates from bovine raw milk in Korea. Two predominant spa groups were distributed widely and recently described SE and SE-like toxin genes were detected frequently.

Keyword

bovine mastitis; enterotoxin; mobile genetic elements; S. aureus; spa typing

MeSH Terms

Animals
Cattle
Cluster Analysis
DNA, Bacterial/chemistry/genetics
Enterotoxins/chemistry/*genetics
Female
Genotype
Mastitis, Bovine/epidemiology/genetics/*microbiology
Microsatellite Repeats
Milk/*microbiology
Polymerase Chain Reaction/veterinary
Prevalence
Republic of Korea/epidemiology
Staphylococcal Infections/epidemiology/microbiology/*veterinary
Staphylococcus aureus/classification/genetics/*isolation & purification

Figure

  • Figure 1 The number of screened herds and collected samples from five provinces of South Korea. The detection rates of S. aureus are shown in boxes and arrows denote each province.


Cited by  2 articles

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Reference

1. Aires-de-Sousa M, Parente CE, Vieira-da-Motta O, Bonna IC, Silva DA, de Lencastre H. Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro State, Brazil. Appl Environ Microbiol. 2007. 73:3845–3849.
Article
2. Annemüller C, Lämmler C, Zschöck M. Genotyping of Staphylococcus aureus isolated from bovine mastitis. Vet Microbiol. 1999. 69:217–224.
3. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet. 2002. 359:1819–1827.
Article
4. Balaban N, Rasooly A. Staphylococcal enterotoxins. Int J Food Microbiol. 2000. 61:1–10.
Article
5. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol. 1992. 30:1654–1660.
Article
6. Cha JO, Lee JK, Jung YH, Yoo JI, Park YK, Kim BS, Lee YS. Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J Appl Microbiol. 2006. 101:864–871.
Article
7. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev. 2000. 13:16–34.
8. Deringer JR, Ely RJ, Monday SR, Stauffacher CV, Bohach GA. Vβ-dependent stimulation of bovine and human T cells by host-specific staphylococcal enterotoxins. Infect Immun. 1997. 65:4048–4054.
Article
9. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000. 38:1008–1015.
Article
10. Ferens WA, Goff WL, Davis WC, Fox LK, Deobald C, Hamilton MJ, Bohach GA. Induction of type 2 cytokines by a staphylococcal enterotoxin superantigen. J Nat Toxins. 1998. 7:193–213.
11. Fitzgerald JR, Meaney WJ, Hartigan PJ, Smyth CJ, Kapur V. Fine-structure molecular epidemiological analysis of Staphylococcus aureus recovered from cows. Epidemiol Infect. 1997. 119:261–269.
Article
12. Fitzgerald JR, Hartigan PJ, Meaney WJ, Smyth CJ. Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J Appl Microbiol. 2000. 88:1028–1037.
Article
13. Frénay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, Mooi FR. Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis. 1996. 15:60–64.
Article
14. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol. 2005. 187:2426–2438.
Article
15. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003. 41:5442–5448.
Article
16. Hu DL, Omoe K, Inoue F, Kasai T, Yasujima M, Shinagawa K, Nakane A. Comparative prevalence of superantigenic toxin genes in meticillin-resistant and meticillin-susceptible Staphylococcus aureus isolates. J Med Microbiol. 2008. 57:1106–1112.
Article
17. Hwang SY, Kim SH, Jang EJ, Kwon NH, Park YK, Koo HC, Jung WK, Kim JM, Park YH. Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. Int J Food Microbiol. 2007. 117:99–105.
Article
18. Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol. 2001. 166:669–677.
Article
19. Kapur V, Sischo WM, Greer RS, Whittam TS, Musser JM. Molecular population genetic analysis of Staphylococcus aureus recovered from cows. J Clin Microbiol. 1995. 33:376–380.
Article
20. Katsuda K, Hata E, Kobayashi H, Kohmoto M, Kawashima K, Tsunemitsu H, Eguchi M. Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Vet Microbiol. 2005. 105:301–305.
Article
21. Kenny K, Reiser RF, Bastida-Corcuera FD, Norcross NL. Production of enterotoxins and toxic shock syndrome toxin by bovine mammary isolates of Staphylococcus aureus. J Clin Microbiol. 1993. 31:706–707.
Article
22. Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JM, Kreiswirth BN. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol. 2004. 42:792–799.
Article
23. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y, Lian J, Ito T, Kanamori M, Matsumaru H, Maruyama A, Murakami H, Hosoyama A, Mizutani-Ui Y, Takahashi NK, Sawano T, Inoue R, Kaito C, Sekimizu K, Hirakawa H, Kuhara S, Goto S, Yabuzaki J, Kanehisa M, Yamashita A, Oshima K, Furuya K, Yoshino C, Shiba T, Hattori M, Ogasawara N, Hayashi H, Hiramatsu K. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet. 2001. 357:1225–1240.
24. Mellmann A, Weniger T, Berssenbrügge C, Keckevoet U, Friedrich AW, Harmsen D, Grundmann H. Characterization of clonal relatedness among the natural population of Staphylococcus aureus strains by using spa sequence typing and the BURP (based upon repeat patterns) algorithm. J Clin Microbiol. 2008. 46:2805–2808.
Article
25. Miles H, Lesser W, Sears P. The economic implications of bioengineered mastitis control. J Dairy Sci. 1992. 75:596–605.
Article
26. Moon JS, Lee AR, Kang HM, Lee ES, Joo YS, Park YH, Kim MN, Koo HC. Antibiogram and coagulase diversity in staphylococcal enterotoxin-producing Staphylococcus aureus from bovine mastitis. J Dairy Sci. 2007. 90:1716–1724.
Article
27. Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K. Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun. 2003. 71:6088–6094.
Article
28. Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K. Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett. 2005. 246:191–198.
Article
29. Omoe K, Imanishi K, Hu DL, Kato H, Fugane Y, Abe Y, Hamaoka S, Watanabe Y, Nakane A, Uchiyama T, Shinagawa K. Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect Immun. 2005. 73:5540–5546.
Article
30. Orden JA, Goyache J, Hernández J, Doménech A, Suárez G, Gómez-Lucía E. Detection of enterotoxins and TSST-1 secreted by Staphylococcus aureus isolated from ruminant mastitis. Comparison of ELISA and immunoblot. J Appl Bacteriol. 1992. 72:486–489.
Article
31. Park YK, Koo HC, Kim SH, Hwang SY, Jung WK, Kim JM, Shin S, Kim RT, Park YH. The analysis of milk components and pathogenic bacteria isolated from bovine raw milk in Korea. J Dairy Sci. 2007. 90:5405–5414.
Article
32. Peck KR, Baek JY, Song JH, Ko KS. Comparison of genotypes and enterotoxin genes between Staphylococcus aureus isolates from blood and nasal colonizers in a Korean hospital. J Korean Med Sci. 2009. 24:585–591.
Article
33. Ruzin A, Lindsay J, Novick RP. Molecular genetics of SaPI1--a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol. 2001. 41:365–377.
Article
34. Saei HD, Ahmadi M, Mardani K, Batavani RA. Molecular typing of Staphylococcus aureus isolated from bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Vet Microbiol. 2009. 137:202–206.
Article
35. Schmidt H, Hensel M. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev. 2004. 17:14–56.
Article
36. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol. 1999. 37:3556–3563.
Article
37. Srinivasan V, Sawant AA, Gillespie BE, Headrick SJ, Ceasaris L, Oliver SP. Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathog Dis. 2006. 3:274–283.
Article
38. Stephan R, Annemüller C, Hassan AA, Lämmler C. Characterization of enterotoxigenic Staphylococcus aureus strains isolated from bovine mastitis in north-east Switzerland. Vet Microbiol. 2001. 78:373–382.
Article
39. Strommenger B, Kettlitz C, Weniger T, Harmsen D, Friedrich AW, Witte W. Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol. 2006. 44:2533–2540.
Article
40. Su YC, Wong AC. Identification and purification of a new staphylococcal enterotoxin, H. Appl Environ Microbiol. 1995. 61:1438–1443.
Article
41. Thomas DY, Jarraud S, Lemercier B, Cozon G, Echasserieau K, Etienne J, Gougeon ML, Lina G, Vandenesch F. Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun. 2006. 74:4724–4734.
Article
42. Yarwood JM, McCormick JK, Paustian ML, Orwin PM, Kapur V, Schlievert PM. Characterization and expression analysis of Staphylococcus aureus pathogenicity island 3. Implications for the evolution of staphylococcal pathogenicity islands. J Biol Chem. 2002. 277:13138–13147.
Article
43. Zhang S, Iandolo JJ, Stewart GC. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol Lett. 1998. 168:227–233.
Article
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