Aim: An epidemiological surveillance for Staphylococci contamination of ready-to-eat (RTE) meats from Enugu State, Nigeria, was carried out to determine the prevalence, species distribution, toxigenic potential and antimicrobial susceptibility profile of the organisms and hence the microbiological and toxicological safety of the meats.

Materials and Methods: Isolation and phenotypic Staphylococcus detection were done according to standard microbiological methods. Phenotypic resistance to 17 commonly used antimicrobial agents was determined by disc diffusion method. Molecular characterization of the isolates to species level and detection of selected toxigenic and antimicrobial-resistance genes were done by PCR methods.

Results: Twenty-four (9.4%) of the 255 meat samples investigated were contaminated with Staphylococcus species. Twenty-four Staphylococcus isolates belonging to six species of coagulase-negative Staphylococcus (CoNS) were identified. Four (16.7%) isolates harbored genes coding for exfoliative toxin-A. Ten (41.7%) isolates were multidrug resistant, while mecA, tetK, mphC, ermT and ermC were the antimicrobial-resistance genes detected in the isolates. Meat samples sourced from motor parks (16.7%) and open markets (8.5%) were the most contaminated.

Conclusion: 9.4% of RTE meats sampled were contaminated with toxigenic and multidrug resistance CoNS. Beef was the most contaminated RTE meat type and harbored all the toxigenic and most of the antibiotic-resistant genes detected. Meat samples from motor parks had the highest staphylococcal contamination (16.7%), while those from mechanic village had the least (2.4%). Majority (79.2%) of the isolates were not susceptible to fusidic acid but none exhibited antimicrobial-resistance to chloramphenicol, ciprofloxacin, linezolid or teicoplanin. Food safety authorities in the study area should work proactively to massively improve the hygienic practices of meat vendors; in order to limit staphylococcal contamination of RTE meats and the associated public health problems.

Keywords: antibiotic resistance, food safety, Nigeria, polymerase chain reaction, ready-to-eat meats, Staphylococcus.

1. Ugwu, C.C., Gomez-Sanz, E., Agbo, I.C., Torres, C. and Chah, K.F. (2015) Characterization of mannitol-fermenting methicillin-resistant staphylococci isolated from pigs in Nigeria. Braz. J. Microbiol., 46: 885-892. [Crossref] [PubMed] [PMC]

2. Chah, K.F., Gomez-Sanz, E., Nwanta, J.A., Asadu, B., Agbo, I.C., Lozona, C., Zarazaga, M. and Torres, C. (2014) Methicillin-resistant coagulase-negative Staphylococci from healthy dogs in Nsukka, Nigeria. Braz. J. Microbiol., 45: 215-220. [Crossref] [PubMed] [PMC]

3. Njoga, E.O., Onunkwo, J.I., Okoli, C.E., Ugwuoke, W.I., Nwanta, J.A. and Chah, K.F. (2018) Assessment of antimicrobial drug administration and antimicrobial residues in food animals in Enugu State, Nigeria. Trop. Anim. Health Prod., 50: 897-902. [Crossref] [PubMed]

4. Njoga, E.O., Onunkwo, J.I., Ekere, S.O., Njoga, U.J. and Okoro, W.N. (2018) Seroepidemiology of equine brucellosis and role of horse carcass processors in spread of Brucella infection in Enugu State, Nigeria. Int. J. Curr. Res. Rev., 10:39-45. [Crossref]

5. Ekere, S.O., Njoga, E.O., Onunkwo, J.I. and Njoga, U.J. (2018) Serosurveillance of Brucella antibody in food animals and role of slaughterhouse workers in spread of Brucella infection in Southeast Nigeria, Vet. World., 11(8): 1171-1178.

6. Onunkwo, J.I., Njoga, E.O., Nwanta, J.A., Shoyinka, S.V.O., Onyenwe, I.W. and Eze, J.I. (2011) Serological survey of porcine Brucella infection in Southeast, Nigeria. Nigerian Vet. J., 32: 60-62. [Crossref]

7. Onunkwo, J.I., Njoga, E.O., Njoga, U.J., Ezeokafor, E and Ekere, S.O. (2018) Brucella seropositivity in chicken and risk factors for Brucella infection at the animal-human inter-face in Anambra State, Nigeria. Int. J. One Health., 4:28-34. [Crossref]

8. Bukar, A., Uba, A. and Oyeyi, T.I. (2010) Occurrence of some enteropathogenic bacteria in some minimally and fully processed ready-to-eat foods in Kano metropolis, Nigeria. Afr. J. Food Sci., 4: 32-36.

9. El-Seedy, F.R., Samy, A.A., Salam, H.S.H., Khairy, E.A. and Koraney, A.A. (2017) Polymerase chain reaction detection of genes responsible for multiple antibiotic resistance Staphylococcus aureus isolated from food of animal origin in Egypt. Vet. World, 10: 1205-1211. [Crossref]

10. Kluytmans, J.A. (2012) Methicillin-resistant Staphylococcus aureus in food products: Cause for concern or case for complacency. Clin. Microbiol. Infect., 16: 11-15. [Crossref] [PubMed]

11. Osman, K.M., Abd El-Razik, K.A., Marie, H.S.H. and Arafa, A. (2016) Coagulase-negative Staphylococci collected from bovine milk: Species and antimicrobial gene diversity. J. Food Saf., 36: 89-99. [Crossref]

12. Razmyar, J., Jamshidi, A., Khanzadi, S. and Kalidari, G. (2017) Toxigenic Clostridium difficile in retail packed chicken meat and broiler flocks in northeastern Iran. Iranian J. Vet. Res., 18: 271-274. [PubMed] [PMC]

13. Felgo, P. and Sakyi, K. (2012) Bacterial contamination of street vending food in Kumasi, Ghana. J. Med. Biomed. Sci., 1: 1-8.

14. Nyenje, E.M., Odjadjare, C.E., Tanih, N.F. and Green, E. (2012) Foodborne pathogens recovered from ready-to-eat foods from roadside cafeterias and retail Outlets in Alice, Eastern Cape province, South Africa: Public health implications. Int. J. Environ. Res. Pub. Health, 9: 2608-2619. [Crossref]

15. Salihu, M.D., Junaidu, A.U., Magaji, A.A., Aliyu, R.M. and Yakubu, I. (2010) Bacteriological quality of traditionally prepared ground beef (Dambun Nama) in Sokoto, Nigeria. Adv. J. Food. Sci. Tech., 2: 145-147.

16. Egbebi, O.A. and Muhammad, A.A. (2016) Microbiological analysis of ready-to-eat suya meat sold in Owo, Ondo State. Int. J. Innov. Biochem. Microbiol. Res., 4: 11-15.

17. Uzeh, R.E., Ohenhen, R.E. and Adeniji, O.O. (2006) Bacterial contamination of tsire-suya-a Nigerian meat product. Pak. J. Nut., 5: 458-460. [Crossref]

18. Orji, J., Ugbo, E., Ejikeugwu, C., Okonkwo, E., Nwuzo, A., Moses, I., Nwakaeze, E., Agumah, N. and Ogene, L. (2015) Microbial contamination of ready-to-eat fried chicken meat sold in two selected motor garage points in Abakaliki, Ebonyi State, Nigeria. Int. J. Pure Appl. Biosci., 3: 271-275.

19. Olimpia, P., Giuseppe, B., Francesca, B., Marilena, A., Maria, A. and Francesco, V. (2006) Staphylococcus aureus and staphylococcal enterotoxin A in breaded chicken products: Detection and behavior during the cooking process. Appl. Environ. Microbiol., 72: 7057-7062. [Crossref] [PubMed] [PMC]

20. Mashak, Z., Ali, L.M., Ali, E., Ayub, E.F. and Ashkan, I. (2015) Microbiological quality of ready-to-eat foods of Tehran province. Afr. J. Food Sci., 9: 257-261. [Crossref]

21. Scharff, R.L. (2012) Economic burden from health losses due to foodborne illness in the United States. J. Food Prot., 75: 123-131. [Crossref] [PubMed]

22. Cheesbrough, M. (2000) District Laboratory Practice in Tropical Countries. Cambridge University Press, London.

23. Gomez-Sanz, E., Torres, C., Lozano, C., Ferna'ndez-Pe'rez, R., Aspiroz, C., Ruiz-Larrea, F. and Zarazaga, M. (2010) Detection, molecular characterization and clonal diversity of methicillin-resistant Staphylococcus aureus CC398 and CC97 in Spanish slaughter pigs of different age groups. Foodborne Pathog. Dis., 7: 1269-1277. [Crossref]

24. Poyart, C., Quesue, G. and Boumaila, C. (2001) Rapid and accurate species-level identification of coagulase-negative Staphylococci by using the sodA gene as target. J. Clin. Microbiol., 39: 4296-4301. [Crossref] [PubMed] [PMC]

25. Hwang, K.N., Yun, A.R. and Rhee, M.S. (2007) Prevalence and classification of toxigenic Staphylococcus aureus isolated from refrigerated ready-to-eat foods in Korea. J. Appl. Microbiol., 70: 1153-1158.

26. CLSI (Clinical and Laboratory Standards Institute). (2014) Performance Standards for Antimicrobial Susceptibility Testing: Twenty-first Informational Supplement. CLSI Document 34:M100-S24. Clinical and Laboratory Standards Institute, Wayne, PA.

27. Gomez-Sanz, E., Torres, C., Lozano, C. and Zarazaga, M. (2013) High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owning household members: Underestimating normal household contact? Comp. Immunol. Microbiol. Infect. Dis., 36: 83-94. [Crossref] [PubMed]

28. Oyeyi, T.I. and Lum-Nwi, M.E.F. (2008) Bacteriological quality of some street vended foods in Bayero University campuses, Kano, Nigeria. Afr. J. Food Sci., 5: 239-243.

29. Senait, G. and Moorty, A.R.S. (2016) Isolation and identification of Staphylococcus species from ready-to-eat meat products in and around Debre-Zeit, Ethiopia. Int. J. Res. Agric. For., 3: 6-16.

30. Acco, M., Ferreira, P.S., Henriques, J.A.P. and Tondo, E.C. (2003) Identification of multiple strains of Staphylococcus aureus colonizing nasal mucosa of food handlers. Food Microbiol., 20: 489-943. [Crossref]

31. Alimi, R.S. (2013) An analysis of meat demand in Akungba-Akoko, Nigeria. Nigerian J. Appl. Behav. Sci., 1: 96-104.

32. Bello, M., Lawan, M.M., Aluwong, T. and Sanusi, M, (2015) Management of slaughterhouses in northern Nigeria and the safety of meat produced for human consumption. Food Control, 49: 34-39. [Crossref]

33. Nwanta, J.A., Onunkwo, J. and Ezenduka, E. (2010) Analysis of Nsukka Metropolis Abattoir solid waste and its bacterial contents in South Eastern Nigeria: Public Health Implication. Arch. Environ. Occup. Health, 65: 19-23. [Crossref] [PubMed]

34. El-Razik, K.A.A., Arafa, A.A., Hedia, R.H., Ibrahim, E.S. (2017) Tetracycline resistance phenotypes and genotypes of coagulase-negative staphylococcal isolates from bubaline mastitis in Egypt. Vet. World, 10: 702-710. [Crossref] [PubMed] [PMC]

35. Sila, J., Sauer, P. and Kolar, M. (2009) Comparison of the prevalence of genes coding for enterotoxins, exfoliatins, Panton-valentine leukocidin and TSST-1 between methicillin-resistant and methicillin-susceptible isolates of Staphylococcus aureus at the University Hospital in Olomouc. J. Biomed Res., 153: 215-218. [Crossref]

36. Gandhale, D., Kolhe, R., Nalband, S., Deshpande, P., Jagtap, U., Dhandore, C., Bhave, S., Jadhav, S., Muglikar, D. and Kolhe, S. (2017) Molecular types and antimicrobial resistance profile of Staphylococcus aureus isolated from dairy cows and farm environments. Turk. J. Vet. Anim. Sci., 41: 713-724. [Crossref]

---