Food and Public Health

p-ISSN: 2162-9412    e-ISSN: 2162-8440

2013;  3(6): 284-288


Nasal Carriage of Enterotoxigenic Staphylococcus aureus and Risk Factors among Food Handlers-Egypt

Moustafa El-Shenawy1, Lobna El-Hosseiny2, Mohamed Tawfeek1, Mohamed El-Shenawy3, Hoda Baghdadi2, Ola Saleh1, J. Mañes4, J. M. Soriano4

1Department of Food Microbiology, National Research Center, Dokki, Cairo, 12311, Egypt

2Department of Environmental Studies, Institute of Graduate Studies and Research, Alexandria University, Egypt

3Department of Microbiology, National Institute of Oceanography and Fisheries, Alexandria, Egypt

4Observatory of Nutrition and Food Safety in Developing Countries, Department of Preventive Medicine and Public Health, Faculty of Pharmacy, University of Valencia, Burjassot, 46100, Spain

Correspondence to: Moustafa El-Shenawy, Department of Food Microbiology, National Research Center, Dokki, Cairo, 12311, Egypt.


Copyright © 2012 Scientific & Academic Publishing. All Rights Reserved.


Food handlers play a major role in the transmission of food borne diseases which represents a global health burden. Carriage of Staphylococcus aureus, in general, and enterotoxigenic strains, in particular, is an important risk factor for the contamination of food. This study was undertaken to determine the prevalence and risk factors associated with nasal carriage of Staphylococcus aureus among 200 food handlers working in 3 different food processing plants in Egypt. Sixty-one (31%) persons were found to be carriers of Staphylococcus aureus of which twenty-one (34.4%) harboured enterotoxigenic staphylococcal strains. The most frequently found enterotoxins were Types A and C (12 isolates each), followed by Type B and Type D (7 isolates, 5 isolates) respectively. A combination of two or three enterotoxins was produced by some of the isolates. The three processing plants recorded statistically significant differences amongst examined personnel in nasal carriage, however neither of the risk factors assessed including age, gender, marital status, education, duration in work, frequency and method of hand wash, incidence of chronic sinusitis and smoking were significant risk determinants of S. aureus nasal carriage. The obtained results should be of public health concern and highlights the need for primary health care and hygiene among food handlers.

Keywords: Enterotoxigenic S. Aureus, Nasal Carriage, Risk Factors, Food Handlers

Cite this paper: Moustafa El-Shenawy, Lobna El-Hosseiny, Mohamed Tawfeek, Mohamed El-Shenawy, Hoda Baghdadi, Ola Saleh, J. Mañes, J. M. Soriano, Nasal Carriage of Enterotoxigenic Staphylococcus aureus and Risk Factors among Food Handlers-Egypt, Food and Public Health, Vol. 3 No. 6, 2013, pp. 284-288. doi: 10.5923/j.fph.20130306.04.

1. Introduction

According to the World Health Organization (WHO), up to 30% of the populations of developed countries are affected by food-borne illness each year. The problem is more widespread in developing countries where most of these cases are not reported, and thus the true dimension of the problem is not known[1]. In these countries, errors made in food processing plants and settlements emerge as important causes of foodborne disease[2].
Food handlers are potential causes of infections by many food borne pathogens since many diseases arecommunicable and caused originally by microorganisms carried into their bodies[3]. It is estimated that 30-50% of the human population carries Staphylococcus aureus and its main habitat is the nasopharynx, a site where strains can persist as transitory or persistent members of the normal microbiota without causing any symptomatology. Accordingly, body carriage of S. aureus by food handlers can be an important source of contamination of the food product via respiratory secretions or direct contact via hands during manufacture and handling of the food product[4].
Staphylococcus aureus is an extraordinary versatile pathogen and the major causative agent of numerous infectious diseases. The disease spectrum includes abscesses, septicemia, endocarditis, osteomyeltis, pneumonia, in addition to various toxin mediated diseases as toxic shock syndrome and staphylococcal food poisoning. The variety of such spectrum of clinical manifestations is mostly dependant on the numerous virulence factors produced by each strain[5]. The ingestion of the preformed toxins produced by enterotoxigenic strains in food often leads to the development of food poisoning. The symptoms typically have a rapid onset (2–6 h) and may include nausea, vomiting, diarrhea and abdominal pain[6].
Consequently, the rising concerns over food safety and the lack of research into the proportion of Egyptian food handlers colonized by S. aureus have formed the impetus for investigation of the incidence and potential risk factors associated with nasal carriage of S. aureus amongst personnel working in three different food processing plants.

2. Materials and Methods

This work was done over a period of 10 months (Jan. 2012-Nov.2012). Two-hundred food handlers, working in three different food processing plants, participated in this work. These include 42 personnel working in milk and dairy products plant, 67 working in meat and poultry products plants and 91 working in frozen/canned juices and vegetables processing plant. Prior to sample collection a demographic data sheet was collected from each participant.
The Staphylococcus spp. nasal carriage study was carried out using sterile swabs, which were inserted in both anterior nares and transferred to a tube containing sterile brain heart infusion broth. Tubes were incubated at 37℃ for 24 h, streaked onto the surface of Baird-Parker Agar Base plates (Oxoid CM0275, Basinggstoke, Hants, UK) supplemented with egg-yolk tellurite emulsion (Oxoid SR 0054) and aerobically incubated at 37℃ for 24-48 h. Three colonies per sample, showing typical colonial morphology of coagulase- positive Staphylococci, were subjected to Gram staining, coagulase and catalyse tests. Gram, coagulase and catalyse positive strains were confirmed with an agglutination Staphyloccci Plus test (Oxoid) thereafter biochemically identified with API staph identification System for Staphylococcus aureus (bioMerieux Marcy – I'Etoile, France). Definitive identification was based on the presence of DNA using DN-ase test, the presence of protein A and clumping factor using SLIDEX Staph plus (bioMerieux Marcy – I'Etoile, France). A strain of S. aureus NCTC 10788 (obtained from food science department, University of Wisconsin-Madison, US) was used as a reference strain.
Only one identified isolate per positive samples was investigated using an immunological technique to verify its ability to synthesize staphylococcal enterotoxins. The strains were grown in 10 ml of tryptone soya broth (CM0219B, Oxoid) by shaking aerobically for 16-18 h at 37℃. After centrifugation at 9000 x g for 20 min at 4℃, the supernatant was tested for presence of staphylococcal enterotoxins and typed using Staphylococcal Enterotoxin Test Reversed Passive Latex Agglutination (SET-RPLA) (TD900 Oxoid Basinkstoke, Hampshire, UK) as recommended by the manufacturer's protocol. Negative controls were used with all the tested samples.
Data collected were statistically analysed using SAS version 8 (SAS Institute, Cary, NC, US). Proportions were compared using Pearson Chi-Square tests. The level of statistical significance was set at a P-value ≤ 0.05.

3. Results and Discussion

Table (1) illustrates the number of persons screened for nasal carriage of S. aureus in the investigated food processing plants. The overall prevalence of the pathogen in the two hundred examined personnel was about one third (31%). Subjects working in the milk and dairy processing plant recorded the highest prevalence rate (36%) of colonization by S. aureus followed by the other two processing plants; meat and meat products (31%) and frozen/canned vegetables and juices (27%) plants respectively. The difference in prevalence rates amongst the three study plants were significant (P = -0.028), however this prevalence cannot be exactly compared due to differences in sample size, habits and other environmental conditions that may exist in these plants.
Table 1. Incidence of nasal S. aureus among food-handlers working in food processing plants
The overall prevalence of nasal S. aureus amongst the study population, in the current study, recorded values higher than those registered in other studies conducted at US (23%)[7] and UK (25%)[8] and among food handlers working in Ethiopia (20.5%)[9], Turkey (23.1%)[10] and Brazil (29%)[11] and even hospital personnel in Cameroon (23.7%)[12]. Meanwhile, higher prevalence rates were reported among food handlers of a Chilean (65%)[13] and Botswana (57.5%)[14] studies, as well as, amongst healthy subjects working in an Iranian (35.7%), Indian (37.3%) and Nigerian (50%) hospitals[15]. A study conducted in Sudan for food handlers working in restaurants, bakeries, butcheries and groceries demonstrated that 30.1% of the examined handlers harboured S. aureus in their anterior nares[16]. Results of the current investigation recorded an S. aureus nasal carriage incidence rates that are approximately the same as that of the Sudanese study and within the ranges reported for health personnel (15-56%)[15]. A number of studies estimate the prevalence of S. aureus colonization in the general population to be approximately 20%–32%[17]. In the present study, we found a prevalence of 61 carriers in 200 individuals, corresponding to 31%, which shows good accordance with these general findings. Generally, there exists considerable variation of nasal carriage of S. aureus prevalence within regions, countries and even inside each country. Global trends of staphylococcal nasal carriage demonstrated that nasal carriage is high in developed countries, as compared to underdeveloped and developing countries[18]. However comparison amongst these studies are difficult since most of these studies identify a particular target population (encompassing students, hospital workers, infants in neonatal ward, geriatric patients, food handlers ….etc) and study carriage in that cohort with respect to certain standard variables (viz., age, sex, health status, antibiotic intervention in a given time frame and others) within that group.
Food handlers carrying enterotoxin-producing S. aureus in their noses or on their hands are regarded as the main source of food contamination, via manual contact or through respiratory secretions. The majority of reported Staphylococcal food poisoning outbreaks are associated with classical enterotoxins, SEA-SEE; however enterotoxin A was the most incriminated[19]. Results of the present investigation indicated that 10.5% of the examined persons were found to be carriers of enterotoxigenic S. aureus. Enterotoxin type A being the most prevalent type detected in 12 of the 21 isolates (57%) followed by enterotoxin C (52%), SEB (38%) and SED respectively. Results also indicated that some isolates produced more than one type of toxin as shown in Table 1. Similar findings was observed in other studies, where food handlers in a Botswana's study[14] recorded a 21% of occurrence of enterotoxigenic strains among S. aureus isolates, the most prevalent being type A which accounted for 34.9% of the toxigenic strains. Similarly a Chilean study[20] reported that out of the 34% of S. aureus harbouring individuals, 54% were enterotoxin producers with SEA being the most frequently type detected. On the contrary, another Chilean study reported that out of the 36 food handlers investigated, the most frequently found enterotoxin was type B[13].
Table 2. Risk factors associated with S.aureus nasal carriage amongst study population
Demographic characteristics of respondents are presented in table (2). About half of the respondents (57.5%) were females and nearly half were below the age of forty. About half of the investigated food handlers had education above primary school. One third of the respondents was single and has spent more than 5 years in their current employment in the studied food processing plants. Findings related to analysis of demographic variables revealed that neither gender, age, marital status nor level of education had a significant effect with respect to the nasal carriage of S. aureus. Similarly other demographic characteristics as the work experiences and incidence of chronic sinusitis were statistically insignificant in relation to harbouring S. aureus in the anterior nares of the investigated subjects. Surprisingly, personal habits as smoking and hand wash did not significantly seem to affect the colonization of the bacterium in the anterior nares of the respondents.
The current study evaluated the potential risk factors for nasal carriage of S. aureus. The investigated variables included fixed factors as gender, age, education in addition to modifiable elements as smoking, hand wash, incidence of chronic sinusitis. Age was identified in earlier studies as a factor influencing nasal colonization with S. aureus[21]. Newborns have higher rates of S. aureus colonization ranging from 59-100% within a few days of birth and these rates decline to adult carrier rates (10-35%) by 5-6 years of age[22]. This trend towards a decline in S. aureus carriage with advancing age is not the case in this study, as the two age groups, cited almost the same incidence of nasal S. aureus carriage. This difference among the current study and others may be attributed to the differences in age ranges investigated amongst the study populations. Male gender has also been reported in several studies as a risk factor for nasal carriage of S. aureus[21,23]. Unfortunately, the reasons for this association remain unclear. Regarding modifiable characteristics, chronic sinusitis was shown to be a risk factor for nasal carriage of S. aureus[24]. Anatomic alterations of the nasopharynx, long-term antibiotic exposure, or other factors might lead to a predisposition of S. aureus carriage. However, a recent comparison of the bacteriologic flora of patients with and without chronic sinusitis did not reveal a significant difference in colonization rates regarding S. aureus which is in agreement with our present findings where the carriage rate did not significantly differ between both groups with/without a history of chronic sinusitis[25]. The correlation between smoking and nasal carriage of S. aureus in previous studies presented biased results where a cross sectional study involving 346 adults conducted in Malaysia revealed that smokers had higher nasal carriage rates than non-smokers[26]. An earlier study had already revealed that passive smoking is associated with an increased risk of S. aureus colonization, with active smoking being protective against colonization[27]. In the current investigation, smoking seemed to be an insignificant determinant of S. aureus nasal carriage. Food handlers in the current study had the habit of hand wash during their working hours but with a difference in frequency and method of hand wash employed. In a study among 200 food handlers working at Gondar University, Ethiopia[9] an insignificant association was found between different hand washing practices (hand wash after toilet with water, hand wash after toilet with soap and hand wash before preparing food) and nasal carriage of S. aureus, which correlates with the findings in our current investigation.
The discrepancies amongst the findings related to the several factors that are independent risk determinants of nasal carriage of S. aureus are attributed to multiple reasons. One of those applies in our study; the self-administered questionnaire may have led to inaccuracies in the assessment of risk factors. Because the study population had different educational backgrounds, socioeconomic status, perceptions, chronic or more severe diseases were underrepresented and, therefore, might have lacked the statistical power to be detected as risk factors for S. aureus carriage. Since this study targeted host-related factors, somewhat neglecting the role of the microorganism itself, further coherent research is needed into the complex background underlying staphylococcal nasal carriage.

4. Conclusions

In conclusion, a relatively high prevalence rate of S. aureus nasal carriage was recorded among the investigated food handlers. Moreover, 11% of the investigated carriers harboured enterotoxigenic strains in their anterior nares increasing the likelihood of transmission of the pathogen to the handled food. These findings resurges the imperative need for protective measures including increased public awareness programs, regular monitoring of food handlers for food borne pathogens and intensive training on primary health care and hygiene. Finally, the current findings clearly highlight the significance of implementation of efficient quality control systems in areas of direct contact with food product as good manufacturing practices and standard operational procedures and future research addressing effective methods for sustained eradication of staphylococcal nasal carriage are clearly warranted to reduce the high risk of subsequent infection.


Financial support for this research was provided by the Agencia Espa˜nola de Cooperaci ´on Internacional para el Desarrollo (A/019106/08, A/025113/09 and A1/035779/11).


[1]  WHO (World Health Organization). (2007)[Online]. Available:
[2]  EUFIC (The European Food Information Council). (2010).[Online]. Available:
[3]  Zain, M., and Naing, N., 2002, Sociodemographic characteristics of food handlers and their knowledge, attitude and practice towards food sanitation: a preliminary report. Southeast Asian J. Trop. Med. Public Health, 33, 410-417.
[4]  Scott, E. 2003, Food safety and foodborne diseases in 21st century homes. Can. J. Infect. Dis., 14,277-280.
[5]  Vasconcelos, N.G. and da Cunha, M.R., 2010, Staphylococcal enterotoxins: Molecular aspects and detection methods. J. Public Health Epidemiol. 2, 29-42.
[6]  Hennekinne, J.A., Ostyn, A., Guillier, F., Herbin, S., Prufer, A.L., and Dragacci, S., 2010, How Should Staphylococcal Food Poisoning Outbreaks Be Characterized? Toxins 2, 2106-2116.
[7]  Mainous, A.G., Hueston, W.J., Everett, C.J. and Diaz, V.A., 2006, Nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus in the United States, 2001-2002., Ann. Fam. Med., 4,132–137.
[8]  Wieneke, A.A., Roberts, D., and Gilbertm R.J., 1993, Staphylococcal food poisoning in the United Kingdom, 1969-90., J. Epidemiol. Infect. Dis., 110, 519-531.
[9]  Dagnew, M., Tiruneh, M., Moges, F., and Tekeste, Z., 2012, Survey of nasal carriage of Staphylococcus aureus and intestinal parasites among food handlers working at Gondar University, Northwest Ethiopia., BMC public health, 12,837.
[10]  Simsek, Z., Koruk, I., Kopur, A.C., and Gurses, G., 2009, prevalence of Staphylococcus aureus and intestinal parasites among food handlers in Sanliurfa, Southeastern Anatolia., J. Public Health Manag. Pract., 15, 518-523.
[11]  Carmo, L.S., Dias, R.S., Linardi, V.R., Sena, M.J., and Dos Santos, D.A., 2003, An outbreak of staphylococcal food poisoning in the municipality of Passos, Minas Geralis, Brazil., Braz. Arch. Biol. Technol., 46, 581-586.
[12]  Eyoh, A., Toukam, M., Okomo, M., Fokunang, C., Atashilli, J., Lyonga, E., Ikomey, G., Mukwele, B., Messembe, M., Akongnwi, E., and Ndumbe, P., 2012, Nasal carriage of Staphylococcus aureus by hospital personnel of three health institutions in Yaounde Cameroon. IRJM, 2, 271-274.
[13]  Soto, A., Saldias, M.E., Oviedo, P., and Fernandez, M. 1996, Prevalence of Staphylococcus aureus among food handlers from a metropolitan university in Chile., Rev. Med. Chil., 124, 1142-1146.
[14]  Loeto, D., Matsheka, M.I. and Gashe, B.A., 2007, Enterotoxigenic and antibiotic resistance determination of Staphylococcus aureus strains isolated from food handlers in Gaborne, Botswana., J. food Prot., 70, 2764-2768.
[15]  Kluytmans, J., Van Belkum, A., and Verbrugh, H., 1997, Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms and associated risks. Clin. Microbiol. Rev. 13, 505-520.
[16]  Saeed, H.A., and Hamid, H.H. 2010, Bacteriological and parasitological assessment of food handlers in the Omdurman Area of Sudan., J. Microbiol. Immunol. Infect. 43,70-73.
[17]  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 Infect Dis., 5,751–762.
[18]  Sivaraman, K., Venkataraman, N. and Cole, A.M., 2009, Staphylococcus aureus nasal carriage and its contributing factors. Future Microbiol. 4,999-1008.
[19]  Argudin, M.A., Mendoza, M.C., and Rodicio, M.R., 2010, Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2,1751-1773.
[20]  Figueroa, G., Navarrete, P., Caro, M., Troncoso, M., and Faundez, G., 2002, Carriage of enterotoxigenic Staphylococcus aureus in food handlers. Rev. Med. Chil.,130, 859-864.
[21]  Bischoff, W.E., Wallis, M.L., Tucker, K.B., Reboussin, B.A. and Sherertz RJ., 2004, Staphylococcus aureus nasal carriage in a student community: prevalence, clonal relationships, and risk factors., Infect. Control Hosp. Epidemiol., 25,485-491.
[22]  VandenBergh, M.F.Q. and Verbrugh, H.A., 1999, Carriage of Staphylococcus aureus: epidemiology and clinical relevance., J. Lab. Clin. Med., 133,525-534.
[23]  Riewerts Eriksen N.H., Esperen, F., Thamdrup Rosdahl, V. and Jensen, K., 1995, Carriage of Staphylococcus aureus among 104 healthy persons during a 19-month period., Epidemiol. Infect., 115,51-60.
[24]  Kremer, B., Jacobs, J.A., Soudijn, E.R. and Van der Ven, A.J.A.M., 2001, Clinical value of bacteriological examinations of nasal and paranasal mucosa in patients with chronic sinusitis., Eur. Arch. Otorhinolaryngol., 258,220-225.
[25]  Halablab, M. A., Hijazi, S.M., Fawzi, M.A. and Araj, G.F., 2010., Staphylococcus aureus nasal carriage rate and associated risk factors in individuals in the community. Epidemiol. Infect., 138,702-706.
[26]  Choi, C.S., Yin, C.S., Bakar, A.A., Sakewi, Z., Naing, N.N., Jamal, F. and Othman, N., 2006, Nasal carriage of Staphylococcus aureus among healthy adults. J. Microbiol. Immunol. Infect., 39,458–464.
[27]  Bogaert, D., van Belkum, A., Sluijter, M., Luijendijk, A., de Groot, R., Rümke, H.C., Verbrugh, H.A. and Hermans, P.W.M., 2004, Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 3631871–1872.