Genetic diversity and virulence potential of staphylococcus aureus isolates from raw and processed food commodities in Shanghai

International Journal of Food Microbiology

Volumn 195, Issue , 2015, Pages 1-8

  Song, Minghui ^a   Bai, Yalong ^a   Xu, Jie ^a   Carter, Michelle Qiu ^b   Shi, Chunlei ^a   Shi, Xianming ^a,c  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Shanghai Jiao Tong University   (China)

^c WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

Agr typing; Food commodities; MecA; Multi locus sequence typing (MLST); Staphylococcus aureus; Toxin genes

Indexed keywords

STAPHYLOCOCCUS AUREUS;

BACTERIAL TOXIN; VIRULENCE FACTOR;

CHINA; FOOD CONTROL; FOOD HANDLING; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; RAW FOOD; STAPHYLOCOCCUS AUREUS; VIRULENCE;

BACTERIAL TOXINS; CHINA; FOOD HANDLING; FOOD MICROBIOLOGY; GENETIC VARIATION; RAW FOODS; STAPHYLOCOCCUS AUREUS; VIRULENCE; VIRULENCE FACTORS;

EID: 84914159268     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.11.020     Document Type: Article

References (46)

1. Alibayov B., Baba-Moussa L., Sina H., Zdenkova K., Demnerova K. Staphylococcus aureus mobile genetic elements. Mol. Biol. Rep. 2014, 41:5005-5018.
2. Argudin M.A., Mendoza M.C., Rodicio M.R. Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2010, 2:1751-1773.
3. Aydin A., Sudagidan M., Muratoglu K. Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int. J. Food Microbiol. 2011, 148:99-106.
4. Bania J., Dabrowska A., Bystron J., Korzekwa K., Chrzanowska J., Molenda J. Distribution of newly described enterotoxin-like genes in Staphylococcus aureus from food. Int. J. Food Microbiol. 2006, 108:36-41.
5. Bergdoll M.S., Crass B.A., Reiser R.F., Robbins R.N., Davis J.P. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet 1981, 1:1017-1021.
6. Boyle-Vavra S., Daum R.S. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab. Investig. 2007, 87:3-9.
7. Brakstad O.G., Aasbakk K., Maeland J.A. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol. 1992, 30:1654-1660.
8. Cafiso V., Bertuccio T., Santagati M., Demelio V., Spina D., Nicoletti G., Stefani S. agr-genotyping and transcriptional analysis of biofilm-producing Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 2007, 51:220-227.
9. Casagrande Proietti P., Coppola G., Bietta A., Luisa Marenzoni M., Hyatt D.R., Coletti M., Passamonti F. Characterization of genes encoding virulence determinants and toxins in Staphylococcus aureus from bovine milk in Central Italy. J. Vet. Med. Sci. 2010, 72:1443-1448.
10. Cha J.O., Lee J.K., Jung Y.H., Yoo J.I., Park Y.K., Kim B.S., Lee Y.S. Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J. Appl. Microbiol. 2006, 101:864-871.
11. Cheung G.Y., Wang R., Khan B.A., Sturdevant D.E., Otto M. Role of the accessory gene regulator agr in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. Infect. Immun. 2011, 79:1927-1935.
12. Chini V., Petinaki E., Foka A., Paratiras S., Dimitracopoulos G., Spiliopoulou I. Spread of Staphylococcus aureus clinical isolates carrying Panton-Valentine leukocidin genes during a 3-year period in Greece. Clin. Microbiol. Infect. 2006, 12:29-34.
13. Cui S., Li J., Hu C., Jin S., Li F., Guo Y., Ran L., Ma Y. Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. J. Antimicrob. Chemother. 2009, 64:680-683.
14. Enright M.C., Day N.P., Davies C.E., Peacock S.J., Spratt B.G. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 2000, 38:1008-1015.
15. Feil E.J., Li B.C., Aanensen D.M., Hanage W.P., Spratt B.G. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 2004, 186:1518-1530.
16. Gilot P., Lina G., Cochard T., Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J. Clin. Microbiol. 2002, 40:4060-4067.
17. Graveland H., Duim B., van Duijkeren E., Heederik D., Wagenaar J.A. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int. J. Med. Microbiol. 2011, 301:630-634.
18. Harmsen D., Claus H., Witte W., Rothganger J., 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.
19. Hata E., Katsuda K., Kobayashi H., Uchida I., Tanaka K., Eguchi M. Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. J. Clin. Microbiol. 2010, 48:2130-2139.
20. He W., Chen H., Zhao C., Zhang F., Li H., Wang Q., Wang X., Wang H. Population structure and characterisation of Staphylococcus aureus from bacteraemia at multiple hospitals in China: association between antimicrobial resistance, toxin genes and genotypes. Int. J. Antimicrob. Agents 2013, 42:211-219.
21. Karahan M., Acik M.N., Cetinkaya B. Investigation of toxin genes by polymerase chain reaction in Staphylococcus aureus strains isolated from bovine mastitis in Turkey. Foodborne Pathog. Dis. 2009, 6:1029-1035.
22. Kerouanton A., Hennekinne J.A., Letertre C., Petit L., Chesneau O., Brisabois A., De Buyser M.L. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int. J. Food Microbiol. 2007, 115:369-375.
23. Koeck R., Schaumburg F., Mellmann A., Koksal M., Jurke A., Becker K., Friedrich A.W. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS One 2013, 8:e55040.
24. Li J., Wang L., Ip M., Sun M., Sun J., Huang G., Wang C., Deng L., Zheng Y., Fu Z., Li C., Shang Y., Zhao C., Yu S., Yao K., Yang Y., Shen X. Molecular and clinical characteristics of clonal complex 59 methicillin-resistant Staphylococcus aureus infections in Mainland China. PLoS One 2013, 8:e70602.
25. Malachowa N., DeLeo F.R. Mobile genetic elements of Staphylococcus aureus. Cell. Mol. Life Sci. 2010, 67:3057-3071.
26. Montanaro L., Speziale P., Campoccia D., Pirini V., Ravaioli S., Cangini I., Visai L., Arciola C.R. Polymorphisms of agr locus correspond to distinct genetic patterns of virulence in Staphylococcus aureus clinical isolates from orthopedic implant infections. J. Biomed. Mater. Res. A 2010, 94:825-832.
27. Neela V., Mohd Zafrul A., Mariana N.S., van Belkum A., Liew Y.K., Rad E.G. Prevalence of ST9 methicillin-resistant Staphylococcus aureus among pigs and pig handlers in Malaysia. J. Clin. Microbiol. 2009, 47:4138-4140.
28. Novick R.P. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 2003, 49:93-105.
29. Novick R.P., Christie G.E., Penades J.R. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 2010, 8:541-551.
30. Omoe K., Hu D.L., 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.
31. Omoe K., Hu D.L., Ono H.K., Shimizu S., Takahashi-Omoe H., Nakane A., Uchiyama T., Shinagawa K., Imanishi K. Emetic potentials of newly identified staphylococcal enterotoxin-like toxins. Infect. Immun. 2013, 81:3627-3631.
32. Ono H.K., Omoe K., Imanishi K., Iwakabe Y., Hu D.L., Kato H., Saito N., Nakane A., Uchiyama T., Shinagawa K. Identification and characterization of two novel staphylococcal enterotoxins, types S and T. Infect. Immun. 2008, 76:4999-5005.
33. Otto M. MRSA virulence and spread. Cell. Microbiol. 2012, 14:1513-1521.
34. Pereira V., Lopes C., Castro A., Silva J., Gibbs P., Teixeira P. Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol. 2009, 26:278-282.
35. Perez-Roth E., Claverie-Martin F., Villar J., Mendez-Alvarez S. Multiplex PCR for simultaneous identification of Staphylococcus aureus and detection of methicillin and mupirocin resistance. J. Clin. Microbiol. 2001, 39:4037-4041.
36. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., Gillece J., Driebe E., Liu C.M., Springer B., Zdovc I., Battisti A., Franco A., Zmudzki J., Schwarz S., Butaye P., Jouy E., Pomba C., Porrero M.C., Ruimy R., Smith T.C., Robinson D.A., Weese J.S., Arriola C.S., Yu F., Laurent F., Keim P., Skov R., Aarestrup F.M. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3.
37. Sugiyama Y., Okii K., Murakami Y., Yokoyama T., Takesue Y., Ohge H., Sueda T., Hiyama E. Changes in the agr locus affect enteritis caused by methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2009, 47:1528-1535.
38. Uhlemann A.C., Porcella S.F., Trivedi S., Sullivan S.B., Hafer C., Kennedy A.D., Barbian K.D., McCarthy A.J., Street C., Hirschberg D.L., Lipkin W.I., Lindsay J.A., DeLeo F.R., Lowy F.D. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 2012, 3.
39. van Belkum A., Melles D.C., Peeters J.K., van Leeuwen W.B., van Duijkeren E., Huijsdens X.W., Spalburg E., de Neeling A.J., Verbrugh H.A. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg. Infect. Dis. 2008, 14:479-483.
40. Varshney A.K., Mediavilla J.R., Robiou N., Guh A., Wang X., Gialanella P., Levi M.H., Kreiswirth B.N., Fries B.C. Diverse enterotoxin gene profiles among clonal complexes of Staphylococcus aureus isolates from the Bronx, New York. Appl. Environ. Microbiol. 2009, 75:6839-6849.
41. Walther B., Monecke S., Ruscher C., Friedrich A.W., Ehricht R., Slickers P., Soba A., Wleklinski C.G., Wieler L.H., Lubke-Becker A. Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2009, 47:704-710.
42. Wang X., Meng J., Zhang J., Zhou T., Zhang Y., Yang B., Xi M., Xia X. Characterization of Staphylococcus aureus isolated from powdered infant formula milk and infant rice cereal in China. Int. J. Food Microbiol. 2012, 153:142-147.
43. Waters A.E., Contente-Cuomo T., Buchhagen J., Liu C.M., Watson L., Pearce K., Foster J.T., Bowers J., Driebe E.M., Engelthaler D.M., Keim P.S., Price L.B. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin. Infect. Dis. 2011, 52:1227-1230.
44. Xie Y., He Y., Gehring A., Hu Y., Li Q., Tu S.I., Shi X. Genotypes and toxin gene profiles of Staphylococcus aureus clinical isolates from China. PLoS One 2011, 6:e28276.
45. Yan X., Wang B., Tao X., Hu Q., Cui Z., Zhang J., Lin Y., You Y., Shi X., Grundmann H. Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China. Appl. Environ. Microbiol. 2012, 78:6637-6642.
46. Yu F., Chen Z., Liu C., Zhang X., Lin X., Chi S., Zhou T., Chen X. Prevalence of Staphylococcus aureus carrying Panton-Valentine leukocidin genes among isolates from hospitalised patients in China. Clin. Microbiol. Infect. 2008, 14:381-384.