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BioMed Research International
Volume 2014, Article ID 485620, 8 pages
http://dx.doi.org/10.1155/2014/485620
Research Article

Mass Spectrometry and Multiplex Antigen Assays to Assess Microbial Quality and Toxin Production of Staphylococcus aureus Strains Isolated from Clinical and Food Samples

1Laboratoire de Biotechnologie et Microbiologie des Aliments, Faculté des Sciences et Technologies des Aliments, Université Nangui Abroguoua, BP 801 Abidjan 02, Cote D’Ivoire
2Laboratoire de Biologie et de Typage Moléculaire en Microbiologie, Faculté des Sciences et Techniques, Université d’Abomey-Calavi, 05 BP 1604 Cotonou, Benin
3Laboratoire de Bactériologie et Virologie, Faculté des Sciences Médicales, Centre Hospitalier et Universitaire de Treichville, BP V3 Abidjan, Cote D’Ivoire
4Université de Strasbourg (CHRU Strasbourg), Fédération de Médecine Translationnelle de Strasbourg, EA 7290 Virulence Bactérienne Précoce, Institut de Bactériologie, 3 rue Koeberlé, 67000 Strasbourg, France
5Department of Biology and Center for Computational and Integrative Biology, Rutgers University, 315 Penn Street, Camden, NJ 08102, USA

Received 8 February 2014; Revised 27 April 2014; Accepted 12 May 2014; Published 29 May 2014

Academic Editor: Himanshu Garg

Copyright © 2014 Paul Attien et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. Tavares, “Bacterias gram-positivas problemas: resistência do estafilococo, do enterococo e do pneumococo aos antimicrobianos,” Revista da Sociedade Brasileira Medicina Tropical, vol. 33, pp. 281–301, 2000. View at Google Scholar
  2. K. B. Crossley, K. K. Jefferson, G. L. Archer, and V. G. Fowler Jr., The Staphylococci in Human Disease, Wiley-Blackwell, West Sussex, UK, 2nd edition, 2009.
  3. N. G. Daver, S. A. Shelburne, R. L. Atmar et al., “Oral step-down therapy is comparable to intravenous therapy for Staphylococcus aureus osteomyelitis,” Journal of Infection, vol. 54, no. 6, pp. 539–544, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. M. P. Jevons, A. W. Coe, and M. T. Parker, “Methicillin resistance in staphylococci,” The Lancet, vol. 281, no. 7287, pp. 904–907, 1963. View at Google Scholar · View at Scopus
  5. O. Lesens, Y. Hansmann, E. Brannigan et al., “Healthcare-associated Staphylococcus aureus bacteremia and the risk for methicillin resistance: is the centers for disease control and prevention definition for community-acquired bacteremia still appropriate?” Infection Control and Hospital Epidemiology, vol. 26, no. 2, pp. 204–209, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. H. F. L. Wertheim, D. C. Melles, M. C. Vos et al., “The role of nasal carriage in Staphylococcus aureus infections,” Lancet Infectious Diseases, vol. 5, no. 12, pp. 751–762, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Zecconi and F. Scali, “Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases,” Immunology Letters, vol. 150, no. 1-2, pp. 12–22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. M. M. Dinges, P. M. Orwin, and P. M. Schlievert, “Exotoxins of Staphylococcus aureus,” Clinical Microbiology Reviews, vol. 13, no. 1, pp. 16–34, 2000. View at Google Scholar · View at Scopus
  9. N. L. Barg and T. Harris, “Toxin-mediated syndromes,” in The Staphylococci in Human Disease, K. B. Crossley and G. L. Archer, Eds., pp. 527–544, Churchill Livingstone, New York, NY, USA, 1997. View at Google Scholar
  10. F. Durupt, L. Mayor, M. Bes et al., “Prevalence of Staphylococcus aureus toxins and nasal carriage in furuncles and impetigo,” British Journal of Dermatology, vol. 157, no. 6, pp. 1161–1167, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Baba-Moussa, H. Ahissou, P. Azokpota et al., “Toxins and adhesion factors associated with Staphylococcus aureus strains isolated from diarrhoeal patients in Benin,” African Journal of Biotechnology, vol. 9, no. 5, pp. 604–611, 2010. View at Google Scholar · View at Scopus
  12. H. Sina, F. Baba-Moussa, T. A. Ahoyo et al., “Antibiotic susceptibility and toxins production of Staphylococcus aureus isolated from clinical samples from benin,” African Journal of Microbiology Research, vol. 5, no. 18, pp. 2797–2803, 2011. View at Google Scholar · View at Scopus
  13. N. Dennaï, B. Kharrati, and M. El Yachioui, “Appréciation de la qualité microbiologique des carcasses de bovins fraîchement abattus,” Annales de Medecine Veterinaire, vol. 145, no. 4, pp. 270–274, 2001. View at Google Scholar · View at Scopus
  14. J. Fosse, C. Magras, and H. Seegers, “Evaluation quantitative des risques biologiques pour le consommateur de viande de porc,” Journees de la Recherche Porcine, vol. 39, pp. 207–214, 2007. View at Google Scholar
  15. S. El Okki, R. El Groud, H. Kenana, and S. Quessy, “Evaluation de la contamination superficielle des carcasses bovines et ovines provenant de l’abattoir municipal de Constantine en Algérie,” The Canadian Veterinary Journal, vol. 200, pp. 638–640, 2005. View at Google Scholar
  16. J.-F. Collobert, F. Dorey, V. Dieuleveux, and N. Quillien, “Microbiological contamination of bovine carcasses,” Sciences des Aliments, vol. 22, no. 3, pp. 327–334, 2002. View at Google Scholar · View at Scopus
  17. J. L. Jouve, “Microbiologie alimentaire et filière des viandes,” Viandes et Produits Carnés, vol. 116, no. 6, pp. 207–213, 1990. View at Google Scholar
  18. J.-F. T. K. Akoachere, R. N. Bughe, B. O. Oben, L. M. Ndip, and R. N. Ndip, “Phenotypic characterization of human pathogenic bacteria in fish from the coastal waters of south west Cameroon: public health implications,” Reviews on Environmental Health, vol. 24, no. 2, pp. 147–156, 2009. View at Google Scholar · View at Scopus
  19. M. Cheesbrough, District Laboratory Practice in Tropical Countries: Part 2, Cambridge University Press, Cambridge, UK, 2004.
  20. A. Mellmann, F. Bimet, C. Bizet et al., “High interlaboratory reproducibility of matrix-assisted laser desorption ionization-time of flight mass spectrometry-based species identification of nonfermenting bacteria,” Journal of Clinical Microbiology, vol. 47, no. 11, pp. 3732–3734, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Prod'Hom, A. Bizzini, C. Durussel, J. Bille, and G. Greub, “Matrix-assisted laser desorption ionization-time of flight mass spectrometry for direct bacterial identification From positive blood culture pellets,” Journal of Clinical Microbiology, vol. 48, no. 4, pp. 1481–1483, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. SFM (Société Française de Microbiologie), Recommandations du Comité de l'Antibiogramme de la Société Française de Microbiologie, 2012.
  23. V. Gauduchon, S. Werner, G. Prévost, H. Monteil, and D. A. Colin, “Flow cytometric determination of Panton-Valentine leucocidin S component binding,” Infection and Immunity, vol. 69, no. 4, pp. 2390–2395, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Prevost, P. Couppie, P. Prevost et al., “Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins,” Journal of Medical Microbiology, vol. 42, no. 4, pp. 237–245, 1995. View at Google Scholar · View at Scopus
  25. A. Gravet, D. A. Colin, D. Keller, R. Girardot, H. Monteil, and G. Prévost, “Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family,” FEBS Letters, vol. 436, pp. 202–208, 1998. View at Google Scholar
  26. O. Joubert, D. Keller, A. Pinck, H. Monteil, and G. Prévost, “Sensitive and specific detection of staphylococcal epidermolysins A and B in broth cultures by flow cytometry-assisted multiplex immunoassay,” Journal of Clinical Microbiology, vol. 43, no. 3, pp. 1076–1080, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Zdolec, I. Rači, A. Vujnović et al., “Antimicrobial resistance of coagulase-negative staphylococci isolated from spontaneously fermented sausages,” Food Technology and Biotechnology, vol. 51, no. 2, pp. 240–246, 2013. View at Google Scholar · View at Scopus
  28. R. Talon and S. Leroy, “Diversity and safety hazards of bacteria involved in meat fermentations,” Meat Science, vol. 89, no. 3, pp. 303–309, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Seitter, C. Nerz, R. Rosenstein, F. Götz, and C. Hertel, “DNA microarray based detection of genes involved in safety and technologically relevant properties of food associated coagulase-negative staphylococci,” International Journal of Food Microbiology, vol. 145, no. 2-3, pp. 449–458, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Martín, M. Garriga, M. Hugas, S. Bover-Cid, M. T. Veciana-Nogués, and T. Aymerich, “Molecular, technological and safety characterization of Gram-positive catalase-positive cocci from slightly fermented sausages,” International Journal of Food Microbiology, vol. 107, no. 2, pp. 148–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. G. Bonomo, A. Ricciardi, T. Zotta, M. A. Sico, and G. Salzano, “Technological and safety characterization of coagulase-negative staphylococci from traditionally fermented sausages of Basilicata region (Southern Italy),” Meat Science, vol. 83, no. 1, pp. 15–23, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Marty, J. Buchs, E. Eugster-Meier, C. Lacroix, and L. Meile, “Identification of staphylococci and dominant lactic acid bacteria in spontaneously fermented Swiss meat products using PCR-RFLP,” Food Microbiology, vol. 29, no. 2, pp. 157–166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Zdolec, M. Hadžiosmanović, L. Kozačinski et al., “Microbial and physicochemical succession in fermented sausages produced with bacteriocinogenic culture of Lactobacillus sakei and semi-purified bacteriocin mesenterocin Y,” Meat Science, vol. 80, no. 2, pp. 480–487, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. G. Bonomo, A. Ricciardi, and G. Salzano, “Influence of autochthonous starter cultures on microbial dynamics and chemical-physical features of traditional fermented sausages of Basilicata region,” World Journal of Microbiology and Biotechnology, vol. 27, no. 1, pp. 137–146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Simeoni, L. Rizzotti, P. Cocconcelli, S. Gazzola, F. Dellaglio, and S. Torriani, “Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities,” Food Microbiology, vol. 25, no. 1, pp. 196–201, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Even, S. Leroy, C. Charlier et al., “Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented foodstuffs,” International Journal of Food Microbiology, vol. 139, no. 1-2, pp. 87–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Attien, H. Sina, W. Moussaoui et al., “Prevalence and antibiotic resistance of Staphylococcus strains isolated from meat products sold in Abidjan streets (Ivory Coast),” African Journal of Microbiology Research, vol. 7, no. 26, pp. 3285–3293, 2013. View at Google Scholar
  38. N. Y. Zinzendorf, A. Krizo, L. Baba-Moussa, V. Edoh, and Y. G. Loukou, “Molecular characteristics of Staphylococcus aureus from Military Hospital in Abidjan, Côte d'Ivoire,” Bulletin of Environment, Pharmacology and Life Sciences, vol. 1, no. 7, pp. 54–58, 2012. View at Google Scholar
  39. H. Belabbès, N. Elmdaghri, K. Hachimi, L. Marih, K. Zerouali, and M. Benbachir, “Antibiotic resistance of Staphylococcus aureus isolated from community and nosocomial infections in casablanca,” Medecine et Maladies Infectieuses, vol. 31, no. 1, pp. 25–28, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. W. Bustamante, A. Alpízar, S. Hernández et al., “Predominance of vanA genotype among vancomycin-resistant Enterococcus isolates from poultry and swine in Costa Rica,” Applied and Environmental Microbiology, vol. 69, no. 12, pp. 7414–7419, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Kruse, B. K. Johansen, L. M. Rørvik, and G. Schaller, “The use of avoparcin as a growth promoter and the occurrence of vancomycin-resistant Enterococcus species in Norwegian poultry and swine production,” Microbial Drug Resistance, vol. 5, no. 2, pp. 135–139, 1999. View at Google Scholar · View at Scopus
  42. J. M. Manson, J. M. B. Smith, and G. M. Cook, “Persistence of vancomycin-resistant enterococci in New Zealand broilers after discontinuation of avoparcin use,” Applied and Environmental Microbiology, vol. 70, no. 10, pp. 5764–5768, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Ladhani, “Understanding the mechanism of action of the exfoliative toxins of Staphylococcus aureus,” FEMS Immunology and Medical Microbiology, vol. 39, no. 2, pp. 181–189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Prévost, P. Couppié, and H. Monteil, “Staphylococcal epidermolysins,” Current Opinion in Infectious Diseases, vol. 16, no. 2, pp. 71–76, 2003. View at Google Scholar · View at Scopus
  45. C. A. Morris, H. D. Conway, and P. H. Everall, “Food-poisoning due to staphylococcal enterotoxin E,” The Lancet, vol. 2, no. 7791, pp. 1375–1376, 1972. View at Google Scholar · View at Scopus
  46. T.-R. Chen, C.-S. Chiou, and H.-Y. Tsen, “Use of novel PCR primers specific to the genes of staphylococcal enterotoxin G, H, I for the survey of Staphylococcus aureus strains isolated from food-poisoning cases and food samples in Taiwan,” International Journal of Food Microbiology, vol. 92, no. 2, pp. 189–197, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. T. Ikeda, N. Tamate, K. Yamaguchi, and S.-I. Makino, “Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H,” Applied and Environmental Microbiology, vol. 71, no. 5, pp. 2793–2795, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. X. Yan, B. Wang, X. Tao et al., “Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China,” Applied and Environmental Microbiology, vol. 78, no. 18, pp. 6637–6642, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J.-A. Hennekinne, M.-L. De Buyser, and S. Dragacci, “Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation,” FEMS Microbiology Reviews, vol. 36, no. 4, pp. 815–836, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Sina, T. A. Ahoyo, W. Moussaoui et al., “Variability of antibiotic susceptibility and toxin production of Staphylococcus aureus strains isolated from skin, soft tissue, and bone related infections,” BMC Microbiology, vol. 13, no. 1, article 188, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Gillet, B. Issartel, P. Vanhems et al., “Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients,” The Lancet, vol. 359, no. 9308, pp. 753–759, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Baba-Moussa, H. Sina, J.-M. Scheftel et al., “Staphylococcal panton-valentine leucocidin as a major virulence factor associated to furuncles,” PLoS ONE, vol. 6, no. 10, Article ID e25716, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. G. P. Gladstone and W. E. Van Heyningen, “Staphylococcal leucocidins,” British Journal of Experimental Pathology, vol. 38, no. 2, pp. 123–137, 1957. View at Google Scholar · View at Scopus
  54. E. Jover, M. Y. Tawk, B.-J. Laventie, B. Poulain, and G. Prévost, “Staphylococcal leukotoxins trigger free intracellular Ca2+ rise in neurones, signalling through acidic stores and activation of store-operated channels,” Cellular Microbiology, vol. 15, no. 5, pp. 742–758, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. G. Prévost, L. Mourey, D. A. Colin, and G. Menestrina, “Staphylococcal pore-forming toxins,” Current Topics in Microbiology and Immunology, vol. 257, pp. 53–83, 2000. View at Google Scholar · View at Scopus