Cross Sectional Study of Skin Carriage and Enterotoxigenicity of Staphylococcus aureus among Food Handlers

Abstract

The prevalence of enterotoxigenic Staphylococcus aureus was investigated among 200 participants working in three different food processing plants in Egypt. Using skin swabs, 75 (38%) of the 200 tested persons were positive for the presence of S. aureus. Of the S. aureus positive persons, 28 (14%) harboured S. aureus produced staphylococcal enterotoxins. The serotypes of these enterotoxins were enterotoxin A (68%), enterotoxin B (36%), enterotoxin C (46%) and enterotoxin D (18%). Some of these isolates produced more than one type of enterotoxins namely AB, AC, BC, BD, ABC and ACD. Analysis of risk factors implicated in skin carriage of S. aureus as age, gender, marital status, education, duration in employment, frequency and method of hand wash and incidence of chronic skin infection revealed insignificant association with staphylococcal skin carriage. The obtained results put forth the risk of food contracting contamination with enterotoxigenic strains of S. aureus owing to skin colonization of S. aureus among food handlers.

Share and Cite:

El-Shenawy, M. , Tawfeek, M. , El-Hosseiny, L. , El-Shenawy, M. , Farag, A. , Baghdadi, H. , Saleh, O. , Mañes, J. and Soriano, J. (2014) Cross Sectional Study of Skin Carriage and Enterotoxigenicity of Staphylococcus aureus among Food Handlers. Open Journal of Medical Microbiology, 4, 16-22. doi: 10.4236/ojmm.2014.41003.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] ECD/WHO (2003) Foodborne Disease in OECD Countries: Present State and Economic Costs. http://dx.doi.org/10.1787/9789264105386-en
[2] FDA (2009) FDA Report on the Occurrence of Foodborne Illness Risk Factors in Selected Institutional Food Service, Restaurant and Retail Food Store Facility Type. http://www.cfsan.fda.gov/~acrobat/retrsk2.pdf
[3] Verkaik, N.J., Benard, M., Boelens, H.A., De Vogel, C.P., Nouwen, J.L., Verbrugh, H.A., Melles, D.C., van Belkum, A. and van Wamel, W.J. (2011) Immune Evasion Cluster Positive Bacteriophages Are Highly Prevalent among Human Staphylococcus aureus Strains, but They Are Not Essential in the First Stages of Nasal Colonization. Clinical Microbiology and Infection, 17, 343-348. http://dx.doi.org/10.1111/j.1469-0691.2010.03227.x
[4] Wertheim, H.F.L., Melles, D.C., Vos, M.C., van Leeuwen, W., van Belkum, A., Verbrugh, H.A. and Nouwen, J.L. (2005) The Role of Nasal Carriage in Staphylococcus aureus Infections. Lancet Infectious Diseases, 5, 751-762. http://dx.doi.org/10.1016/S1473-3099(05)70295-4
[5] Jordá, G.B., Marucci, R.S., Guida, A.M., Pires, P.S. and Manfredi, E.A. (2012) Carriage and Characterization of Staphylococcus aureus in Food Handlers. Revista Argentina de Microbiologia, 44, 101-104.
[6] National Disease Surveillance Centre (NDSC) (2004) Preventing Foodborne Disease: A Focus on the Infected Food Handler. http://www.thehealthwell.info/node/75597
[7] Andargie, G., Kassu, A., Moges, F., Tiruneh, M. and Huruy, K. (2008) Prevalence of Bacteria and Intestinal Parasites among Food-Handlers in Gondar Town, Northwest Ethiopia. Journal of Health, Population and Nutrition, 26, 451-455.
[8] Loeto, D., Matsheka, M.I. and Gashe, B.A. (2007) Enterotoxigenic and Antibiotic Resistance Determination of Staphylococcus aureus Strains Isolated from Food Handlers in Gaborone, Botswana. Journal of Food Protection, 70, 2764-2768.
[9] Talarico, F., Roccia, E. and Nero, D. (1997) Prevalence of Enterotoxigenic Staphylococcus in Food Handlers in the Province of Catanzaro (Italy). Igiene Moderna, 107, 137-142.
[10] Hatakka, M., Björkroth, K.J., Asplund, K., Mäki-Petäys, N. and Korkeala, H.J. (2000) Genotypes and Enterotoxicity of Staphylococcus aureus Isolated from the Hands and Nasal Cavities of Flight-Catering Employees. Journal of Food Protection, 63, 1487-1491.
[11] Figueroa, G., Navarrete, P., Caro, M., Troncoso, M. and Faundez, G. (2002) Carriage of Enterotoxigenic Staphylococcus aureus in Food Handlers. Revista Medica de Chile, 130, 859-864.
[12] Simon, S.S. and Sanjeev, S. (2007) Prevalence of Enterotoxigenic Staphylococcus aureus in Fishery Products and Fish Processing Factory Workers. Food Control, 18, 1565-1568. http://dx.doi.org/10.1016/j.foodcont.2006.12.007
[13] El-Shenawy, M., El Hosseiny, L., Tawfeek, M., El-Shenawy, M., Baghdadi, H., Saleh, O., Manes, J. and Soriano, J.M. (2013) Nasal Carriage of Enterotoxigenic Staphylococcus aureus and Risk Factors among Food Handlers-Egypt. Food and Public Health, 3, 284-288.
[14] Argudin, M.A., Mendoza, M.C. and Rodicio, M.R. (2010) Food Poisoning and Staphylococcus aureus Enterotoxins. Toxins, 2, 1751-1773. http://dx.doi.org/10.3390/toxins2071751
[15] Pinchuk, I.V., Beswick, E.J. and Reyes, V.E. (2010) Staphylococcal Enterotoxins. Toxins, 2, 2177-2197. http://dx.doi.org/10.3390/toxins2082177
[16] Udo, E.E., Al-Bustan, M.A., Jacob, L.E. and Chugh, T.D. (1999) Enterotoxin Production by Coagulase-Negative Staphylococci in Restaurant Workers from Kuwait City May Be a Potential Cause of Food Poisoning. Journal of Medical Microbiology, 48, 819-823. http://dx.doi.org/10.1099/00222615-48-9-819
[17] Soriano, J.M., Font, G., Molto, J.C. and Males, J. (2002) Enterotoxigenic Staphylococci and Their Toxins in Restaurant Foods. Trends in Food Science and Technology, 13, 60-67. http://dx.doi.org/10.1016/S0924-2244(02)00030-4
[18] van Belkum, A., Melles, D.C., Nouwen, J., van Leeuwen, W.B., van Wamel, W., Vos, M.C., Wertheim, H.F. and Verbrugh, H.A. (2009) Co-Evolutionary Aspects of Human Colonisation and Infection by Staphylococcus aureus. Infections, Genetics and Evolution, 9, 32-47. http://dx.doi.org/10.1016/j.meegid.2008.09.012
[19] Warren, R. (2012) Staphylococcus aureus A Cross Sectional Study of Prevalence and Risk Factors in One General Practice. Australian Family Physician, 41, 325-328.
[20] Ibe, S.N. and Wariso, B.A. (2005) Carriage of Staphylococcus aureus on Armpits of School and University Students in Port Harcourt, Nigeria. African Journal of applied Zoology and Environmental Biology, 7, 125-130.
[21] Zanger, P., Nurjadi, D., Gaile, M., Gabrysch, S. and Kremsner, P.G. (2012) Hormonal Contraceptive Use and Persistent Staphylococcus aureus Nasal Carriage. Clinical Infectious Diseases, 55, 1625-1632. http://dx.doi.org/10.1093/cid/cis778
[22] Donker, G.A., Deurenberg, R.H., Driessen, C., Sebastian, S., Nijs, S. and Stobberingh, E.E. (2009) The Population Structure of Staphylococcus aureus among General Practice Patients from The Netherlands. Clinical Microbiology and Infection, 15, 137-143. http://dx.doi.org/10.1111/j.1469-0691.2008.02662.x
[23] Breuer, K., Haussler, S., Kapp, A. and Werfel, T. (2002) Staphylococcus aureus: Colonizing Features and Influence of an Antibacterial Treatment in Adults with Atopic Dermatitis. British Journal of Dermatology, 147, 55-61. http://dx.doi.org/10.1046/j.1365-2133.2002.04872.x
[24] Sollid, J.U., Furberg, A.S., Hanssen, A.M. and Johannessen, M. (2013) Staphylococcus aureus: Determinants of Human Carriage. Infections, Genetics and Evolution. http://dx.doi.org/10.1016/j.meegid.2013.03.020
[25] Olsen, K., Falch, B.M., Danielsen, K., Johannessen, M., Sollid, J.U., Thune, I., Grimnes, G., Jorde, R., Simonsen, G.S. and Furberg, A.S. (2012) Staphylococcus aureus Nasal Carriage Is Associated with Serum 25-Hydroxyvitamin D Levels, Gender and Smoking Status. The Tromso Staph and Skin Study. European Journal of Clinical Microbiology and Infectious Diseases, 31, 465-473. http://dx.doi.org/10.1007/s10096-011-1331-x
[26] Wang, J.T., Liao, C.H., Fang, C.T., Chie, W.C., Lai, M.S., Lauderdale, T.L., Lee, W.S., Huang, J.H. and Chang, S.C. (2009) Prevalence of and Risk Factors for Colonization by Methicillin-Resistant Staphylococcus aureus among Adults in Community Settings in Taiwan. Journal of Clinical Microbiology, 47, 2957-2963. http://dx.doi.org/10.1128/JCM.00853-09
[27] Maree, C.L., Eells, S.J., Tan, J., Bancroft, E.A., Malek, M., Harawa, N.T., Lewis, M.J., Santana, E. and Miller, L.G. (2010) Risk Factors and Colonization with Community Associated Methicillin Resistant Staphylococcus aureus in the Los Angeles County Jail: A Case Control Study. Clinical Infectious Diseases, 51, 1248-1257. http://dx.doi.org/10.1086/657067
[28] Bieber, T. (2008) Atopic Dermatitis. The New England Journal of Medicine, 358, 1483-1494. http://dx.doi.org/10.1056/NEJMra074081

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.