Abstract
We investigated the presence of enterotoxigenic and methicillin-resistant Staphylococcus aureus (MRSA) in a kitchen of a catering firm by collecting 100 food samples and 100 utensil-equipment samples after sanitation. Additional 186 samples in total were collected by swabbing the mouths, noses and hands of 62 kitchen staff members during working hours. The isolation of S. aureus was performed using a culture method and verified by using a genetic method (PCR). The presence of toxin genes and the toxic shock syndrome gene (tst) was analyzed by PCR. ELISA was used to investigate whether the isolates bearing a toxin gene that produces enterotoxin or not. In this research we obtained 1930 isolates from 386 samples. Using molecular typing by PCR, 842 Staphylococcus spp. were found of which 307 (36.4 %) were identified as S. aureus. 198 (64.4 %) of the S. aureus strains were identified as CoA positive and 89 (28.9 %) as MRSA. Our data demonstrate the presence of MRSA and enterotoxigenic S. aureus in a catering kitchen providing daycare and hospital refectories. Given the facts that the rate of kitchen staff members contaminated with enterotoxigenic strains was rather high and that the kitchen contained S. aureus even after sanitation and that there was uneducated staff and insufficient hygiene practices aroused suspicions of the presence of biofilms and/or multi-resistant strains which could manifest a serious public health concern.
Similar content being viewed by others
References
Anonymous (1999) International Organization for Standardization. ISO 6888-1:1999, Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species)-Part 1: Technique using Baird-Parker agar medium. ISO, Geneva, Switzerland
Anonymous (2004) International Organization for Standardization. ISO 18593:2004, Microbiology of food and animal feeding stuffs—horizontal methods for sampling techniques from surfaces using contact plates and swabs. ISO, Geneva, Switzerland
Anonymous (2012) Food and Drug Administration. FDA. Staphylococcus aureus. Bad Bug Book: Foodborne Pathogenic Microorganisms and Natural Toxins Handbook Staphylococcus aureus. Accessed 28 July 2014
Asghar A, Zafar T, Momenah A (2006) Bacteriological and serological survey of infectious diseases among food handlers in Makkah. Ann Saudi Med 26:141–144
Avorn JL, Barrett JF, Davey PG, McEwen SA, O’Brien TF, Levy SB (2001) Antibiotic resistance: synthesis of recommendations by expert policy groups. Alliance for the Prudent Use of Antibiotics. World Health Organization. WHO/CDS/CSR/DRS/2001.10. Accessed 25 March 2014
Aydin A, Muratoglu K, Sudagidan M, Bostan K, Okuklu B, Harsa S (2011a) Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne Pathog Dis 8:63–69
Aydin A, Sudagidan M, Muratoglu K (2011b) 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 148:99–106
Becker K, Roth R, Peters G (1998) Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene. J Clin Microbiol 36:2548–2553
Bennett RW, Lancette GA (2001) Staphylococcus aureus. In: FDA Bacteriological Analytical Manual Online, chapter. 12. http://www.cfsan.fda.gov/. Accessed 30 Jan 2014
Bergdoll MS (1983) Enterotoxins. In: Easmon CSF, Adlam C (eds) Staphylococci and staphylococcal infections. Academic Press, London, pp 559–598
Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43:2163–2176
Can HY, Çelik TH (2012) Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control 24:100–103
Carfora V, Capriol A, Marri N, Sagrafoli D, Boselli C, Giacinti G, Giangolini G, Sorbara L, Dottarelli S, Battisti A, Amatiste S (2015) Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy. Int Dairy J 42:12–15
Cha JO, Lee JK, Jung YH, Yoo JI, Park YK, Kim BS, Lee YS (2006) Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J Appl Microbiol 101:864–871
El-Shenawy M, El-Hosseiny L, Tawfeek M, El-Shenawy M, Baghdadi H, Saleh O, Manes J, Soriano JM (2013) Nasal carriage of enterotoxigenic Staphylococcus aureus and risk factors among food handlers- Egypt. Food Public Health. 3:284–288
Harrigan WF (1998) Laboratory methods in food microbiology, 3rd edn. Academic Press, California
Ho J, O’Donoghue MM, Boost MV (2014) Occupational exposure to raw meat: a newly-recognized risk factor for Staphylococcus aureus nasal colonization amongst food handlers. Int J Hygiene Environ Health 217:347–353
Kamal RM, Bayoumi MA, Abd El Aal SFA (2013) MRSA detection in raw milk, some dairy products and hands of dairy workers in Egypt, a mini-survey. Food Control 33:49–53
Mehrotra M, Wang G, Johnson WM (2000) Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 38:1032–1035
Moretro T, Langsrud S, Heir E (2013) Bacteria on Meat Abattoir Process Surfaces after Sanitation: characterisation of survival properties of Listeria monocytogenes and the commensal bacterial flora. Adv Microbiol 3:255–264
Omoe K, Ishikawa M, Shimoda Y, Hu DL, Ueda S, Shinagawa K (2002) Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harboring seg, seh or sei genes. J Clin Microbiol 40:857–862
Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K (2005) Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett 15:191–198
Pereira V, Lopes C, Castro A, Silva J, Gibbs P, Teixeira P (2009) Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol 26:278–282
Perillo J, Ceccarelli D, Spagnoletti M, Lollai S, Cappuccinelli P, Colombo MM (2012) Molecular characterization of enterotoxigenic and borderline oxacillin resistant Staphylococcus strains from ovine milk. Food Microbiol 32:265–273
Schlegelova J, Babak V, Holasova M, Tantinova LK, Necidova L, Sisak F, Vlkova H, Roubal P, Jaglic Z (2010) Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants. Czech J Food Sci 28:450–461
Sharma M, Anand SK (2002) Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol 19:627–636
Sivaraman K, Venkataraman N, Cole AM (2009) Staphylococcus aureus nasal carriage and its contributing factors. Future Microbiol 4:999–1008
Udo EE, Al-Mufti S, Albert MJ (2009) The prevalence of antimicrobial resistance and carriage of virulence genes in Staphylococcus aureus isolated from food handlers in Kuwait City restaurants. BMC Res Notes 108:2–6
Uzunoviç S, Ibrahimagiç A, Kamberoviç F, Rijnders MIA, Stobberingh EE (2013) Molecular characterization of methicillin-susceptible and methicillin-resistant Staphylococcus aureus in Food handlers in Bosnia and Herzegovina. Open Infect Dis J 7:15–20
Vazquez-Sanchez D, Lopez-Cabo M, Saa-Ibusquiza P, Rodriguez-Herrera JJ (2012) Incidence and characterization of Staphylococcus aureus in fishery products marketed in Galicia (Northwest Spain). Int J Food Microbiol 157:286–296
Veras JF, do Carmo LS, Tong LC, Shupp JW, Cummings C, Dos Santos DA, Cerqueira MM, Cantini A, Nicoli JR, Jett M (2008) A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais. Braz Int J Infect Dis 12:410–415
Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, Gregson DB, Louie T, Conly JM (2004) New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol 42:4947–4955
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sezer, Ç., Özgür, Ç., Aksem, A. et al. Food handlers: a bridge in the journey of enterotoxigenic MRSA in food. J. Verbr. Lebensm. 10, 123–129 (2015). https://doi.org/10.1007/s00003-015-0939-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00003-015-0939-7