Research Article
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Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers

Year 2023, Volume: 7 Issue: 2, 618 - 627, 31.05.2023

Nesrin Çakıcı Nükhet Nilüfer Demirel Zorba Alper Akçalı

https://doi.org/10.30621/jbachs.1137869

Abstract

To determine the enterotoxigenic Staphylococcus aureus carriage rates and personal hygiene practices a total of 300 food workers participated, with 228 working in food businesses and 72 in hospital kitchens in Canakkale, Turkey.
Participants completed a questionnaire about sociodemographic characteristics, hygiene practices, and food safety. Hand/nasal swabs were collected from the food workers. Inoculums were seeded on Baird Parker Agar. Multiplex PCR and ELISA methods were used.
The enterotoxigenic S. aureus carriage rate was 14% of food workers. Out of the 125 S. aureus strains, 42 (33.6%) were positive for one or more SE genes. Furthermore, sea, seb, sec, sed, and sea+sed were found in 16.0%, 6.4%, 9.6%, 6.4%, and 4.8% respectively. SEA, SEB, SEC, SED, and SEE were found at rates of 14.4%, 7.2%, 12.8%, 11.2%, and 20.8%. It was determined that as the education level of food workers increased, the S. aureus carrier rate decreased. The carrier rate was found to be higher in those who use gloves than those who do not. Hand carriers were determined more in nasal carriers (p<0.05).
Food workers who are carriers of enterotoxigenic S. aureus are a risk factor for food contamination. Training food workers on personal hygiene can be effective in preventing food poisoning.

Keywords

Food workers Enterotoxine Staphylococcus aureus carriage Hygiene practices.

Supporting Institution

TUBİTAK

Project Number

113S562

Thanks

Prof. Dr. Ömer Akineden TUBITAK (The Scientific And Technological Research Council of Turkey

References

  • Acco, M., Ferreira, F. S., Henriques, J. A. P., & Tondo, E. C. (2003). Identification of Multiple Strains of Staphylococcus aureus Colonizing Nasal Mucosa of Food Handlers. Food Microbiology, 20, 489–493.
  • Akineden O, Hassan A. A, Schneider E, Usleber E. (2008). Enterotoxigenic properties of Staphylococcus aureus isolated from goats’ milk cheese. International Journal of Food Microbiology, 124, 211-216.
  • Al Bustan M. A, Udo E. E, Chugh T. D. (1996). Nasal Carriage of Enterotoxin Producing Staphylococcus aureus Among Restaurant Workers in Kuwait City. Epidemiology and Infection, 116 (3): 319-322.
  • Alhashimi, H. M. M., Ahmed, M. M., & Mustafa, J. M. (2017). Nasal carriage of enterotoxigenic Staphylococcus aureus among food handlers in Kerbala city. Karbala International Journal of Modern Science, 3, 69-74.
  • Aydın, A., Sudagidan, M., & Muratoglu, K. (2011). Prevalence of Staphylococcal Enterotoxins, Toxin Genes and Genetic-Relatedness of Foodborne Staphylococcus aureus Strains Isolated in the Marmara Region of Turkey. International Journal of Food Microbiology, 148(2), 99–106.
  • Baş, M., Ersun, A. Ş. & Kıvanç G., (2006). The Evaluation of Food Hygiene Knowledge, Attitudes, and Practices of Food Handlers in Food Businesses in Turkey. Food Control, 17(4), 317–322.
  • Cha, J. O., Lee, J. K., Jung, Y. H., Yoo, J. I., Park, Y. K., Kim, B. S., et al. (2006). Molecular Analysis of Staphylococcus aureus Isolates Associated with Staphylococcal Food Poisoning in South Korea. Journal of Applied Microbiology, 101, 864–871.
  • Cakici, N., Demirel-Zorba, N.N., Akçali, A. (2015). Food industry employees and staphylococcal food poisoning. Turkish Bulletin of Hygiene and Experimental Biology, 72 (4) 337-350.
  • Campos A. K. C., Cardonha A. M. S., Pinheiro L. B. G., Ferreira N. R., Azevedo P. R. M. & Stamford T. L. M. (2009). Assessment of Personal Hygiene and Practices of Food Handlers in Municipal Public Schools of Natal, Brazil. Food Control, 20(9), 807-810.
  • Dagnew, M., Moges, T., Feleke, M. & Zinaye, T. (2012). Survey of Nasal Carriage of Staphylococcus aureus and Intestinal Parasites among Food Handlers Working at Gondar University, Northwest Ethiopia. BMC Public Health, 12(1): 837-844.
  • Figueroa G, Navarrete P, Caro M, Troncoso M, Faundez, G. (2002). Carriage of Enterotoxigenic Staphylococcus aureus in Food Handlers. Revista Medica de Chile, 130(8): 859-64.
  • Ho, J., O'Donoghue, M. M., & Boost, M. V. (2014). Occupational Exposure to Raw Meat: A Newly-Recognized Risk Factor for Staphylococcus aureus Nasal Colonization Amongst Food Handlers. International Journal Hygiene Environmental Health, 217, 347-353.
  • Loeto, D., Matsheka, M. I., & Gashe, B. A. (2007). Enterotoxigenic and Antibiotic Resistance Determination of Staphylococcus aureus Strains Isolated from Food Handlers in Gaborone, Botswana. Journal of Food Protection, 12, 2764-2768.
  • Lovseth, A., Loncarevic, S., & Berdal, K. G. (2004). Modified Multiplex PCR Method for Detection of Pyrogenic Exotoxin Genes in Staphylococcal Isolates. Journal of Clinical Microbiology, 42(8), 3869–3872.
  • Lynch, R. A., Phillips, M. L., Elledge, B. L., Hanumanthaiah, S., & Boatright, D. T. (2005). A preliminary evaluation of the effect of glove use by food handlers in fast food restaurants. Journal of Food Protection, 68, 187–190.
  • Monday, S. R., & Bohach, G. A. (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. Journal of Clinical. Microbiology. 37, 3411–3414.
  • Rall, V. L. M., Sforcin, J. M., Augustini, V. C. M., Watanabe, M. T., Fernandes Jr A., Rall R. et al. (2010). Detection of Enterotoxin Genes of Staphylococcus spp Isolated from Nasal Cavities and Hands of Food Handlers. Brazilian Journal of Microbiology, 41, 59-65.
  • Soriano, J. M., Font, G., Molto, J. C., & Manes, J. (2002). Enterotoxigenic Staphylococci and Their Toxins in Restaurant Foods. Trends in Food Science & Technology, 13, 60–67.

Year 2023, Volume: 7 Issue: 2, 618 - 627, 31.05.2023

Nesrin Çakıcı Nükhet Nilüfer Demirel Zorba Alper Akçalı

https://doi.org/10.30621/jbachs.1137869

Abstract

Project Number

113S562

References

  • Acco, M., Ferreira, F. S., Henriques, J. A. P., & Tondo, E. C. (2003). Identification of Multiple Strains of Staphylococcus aureus Colonizing Nasal Mucosa of Food Handlers. Food Microbiology, 20, 489–493.
  • Akineden O, Hassan A. A, Schneider E, Usleber E. (2008). Enterotoxigenic properties of Staphylococcus aureus isolated from goats’ milk cheese. International Journal of Food Microbiology, 124, 211-216.
  • Al Bustan M. A, Udo E. E, Chugh T. D. (1996). Nasal Carriage of Enterotoxin Producing Staphylococcus aureus Among Restaurant Workers in Kuwait City. Epidemiology and Infection, 116 (3): 319-322.
  • Alhashimi, H. M. M., Ahmed, M. M., & Mustafa, J. M. (2017). Nasal carriage of enterotoxigenic Staphylococcus aureus among food handlers in Kerbala city. Karbala International Journal of Modern Science, 3, 69-74.
  • Aydın, A., Sudagidan, M., & Muratoglu, K. (2011). Prevalence of Staphylococcal Enterotoxins, Toxin Genes and Genetic-Relatedness of Foodborne Staphylococcus aureus Strains Isolated in the Marmara Region of Turkey. International Journal of Food Microbiology, 148(2), 99–106.
  • Baş, M., Ersun, A. Ş. & Kıvanç G., (2006). The Evaluation of Food Hygiene Knowledge, Attitudes, and Practices of Food Handlers in Food Businesses in Turkey. Food Control, 17(4), 317–322.
  • Cha, J. O., Lee, J. K., Jung, Y. H., Yoo, J. I., Park, Y. K., Kim, B. S., et al. (2006). Molecular Analysis of Staphylococcus aureus Isolates Associated with Staphylococcal Food Poisoning in South Korea. Journal of Applied Microbiology, 101, 864–871.
  • Cakici, N., Demirel-Zorba, N.N., Akçali, A. (2015). Food industry employees and staphylococcal food poisoning. Turkish Bulletin of Hygiene and Experimental Biology, 72 (4) 337-350.
  • Campos A. K. C., Cardonha A. M. S., Pinheiro L. B. G., Ferreira N. R., Azevedo P. R. M. & Stamford T. L. M. (2009). Assessment of Personal Hygiene and Practices of Food Handlers in Municipal Public Schools of Natal, Brazil. Food Control, 20(9), 807-810.
  • Dagnew, M., Moges, T., Feleke, M. & Zinaye, T. (2012). Survey of Nasal Carriage of Staphylococcus aureus and Intestinal Parasites among Food Handlers Working at Gondar University, Northwest Ethiopia. BMC Public Health, 12(1): 837-844.
  • Figueroa G, Navarrete P, Caro M, Troncoso M, Faundez, G. (2002). Carriage of Enterotoxigenic Staphylococcus aureus in Food Handlers. Revista Medica de Chile, 130(8): 859-64.
  • Ho, J., O'Donoghue, M. M., & Boost, M. V. (2014). Occupational Exposure to Raw Meat: A Newly-Recognized Risk Factor for Staphylococcus aureus Nasal Colonization Amongst Food Handlers. International Journal Hygiene Environmental Health, 217, 347-353.
  • Loeto, D., Matsheka, M. I., & Gashe, B. A. (2007). Enterotoxigenic and Antibiotic Resistance Determination of Staphylococcus aureus Strains Isolated from Food Handlers in Gaborone, Botswana. Journal of Food Protection, 12, 2764-2768.
  • Lovseth, A., Loncarevic, S., & Berdal, K. G. (2004). Modified Multiplex PCR Method for Detection of Pyrogenic Exotoxin Genes in Staphylococcal Isolates. Journal of Clinical Microbiology, 42(8), 3869–3872.
  • Lynch, R. A., Phillips, M. L., Elledge, B. L., Hanumanthaiah, S., & Boatright, D. T. (2005). A preliminary evaluation of the effect of glove use by food handlers in fast food restaurants. Journal of Food Protection, 68, 187–190.
  • Monday, S. R., & Bohach, G. A. (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. Journal of Clinical. Microbiology. 37, 3411–3414.
  • Rall, V. L. M., Sforcin, J. M., Augustini, V. C. M., Watanabe, M. T., Fernandes Jr A., Rall R. et al. (2010). Detection of Enterotoxin Genes of Staphylococcus spp Isolated from Nasal Cavities and Hands of Food Handlers. Brazilian Journal of Microbiology, 41, 59-65.
  • Soriano, J. M., Font, G., Molto, J. C., & Manes, J. (2002). Enterotoxigenic Staphylococci and Their Toxins in Restaurant Foods. Trends in Food Science & Technology, 13, 60–67.
There are 18 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Research Article
Authors

Nesrin Çakıcı 0000-0001-8662-7215

Nükhet Nilüfer Demirel Zorba 0000-0001-6851-6474

Alper Akçalı 0000-0003-0325-886X

Project Number 113S562
Publication Date May 31, 2023
Submission Date June 29, 2022
Published in Issue Year 2023 Volume: 7 Issue: 2

Cite

APA Çakıcı, N., Demirel Zorba, N. N., & Akçalı, A. (2023). Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers. Journal of Basic and Clinical Health Sciences, 7(2), 618-627. https://doi.org/10.30621/jbachs.1137869
AMA Çakıcı N, Demirel Zorba NN, Akçalı A. Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers. JBACHS. May 2023;7(2):618-627. doi:10.30621/jbachs.1137869
Chicago Çakıcı, Nesrin, Nükhet Nilüfer Demirel Zorba, and Alper Akçalı. “Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers”. Journal of Basic and Clinical Health Sciences 7, no. 2 (May 2023): 618-27. https://doi.org/10.30621/jbachs.1137869.
EndNote Çakıcı N, Demirel Zorba NN, Akçalı A (May 1, 2023) Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers. Journal of Basic and Clinical Health Sciences 7 2 618–627.
IEEE N. Çakıcı, N. N. Demirel Zorba, and A. Akçalı, “Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers”, JBACHS, vol. 7, no. 2, pp. 618–627, 2023, doi: 10.30621/jbachs.1137869.
ISNAD Çakıcı, Nesrin et al. “Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers”. Journal of Basic and Clinical Health Sciences 7/2 (May 2023), 618-627. https://doi.org/10.30621/jbachs.1137869.
JAMA Çakıcı N, Demirel Zorba NN, Akçalı A. Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers. JBACHS. 2023;7:618–627.
MLA Çakıcı, Nesrin et al. “Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers”. Journal of Basic and Clinical Health Sciences, vol. 7, no. 2, 2023, pp. 618-27, doi:10.30621/jbachs.1137869.
Vancouver Çakıcı N, Demirel Zorba NN, Akçalı A. Carriage of Enterotoxigenic Staphylococcus Aureus and Hygiene Practices of Food Workers. JBACHS. 2023;7(2):618-27.
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