Open Access
Research (Published online: 29-06-2019)
30. Occurrence, characterization, and antibiogram of Staphylococcus aureus in meat, meat products, and some seafood from Libyan retail markets
Hesham T. Naas, Ramadan A. Edarhoby, Aboubaker M. Garbaj, Salah M. Azwai, Said K. Abolghait, Fatim T. Gammoudi, Ashraf A. Moawad, Ilaria Barbieri and Ibrahim M. Eldaghayes
Veterinary World, 12(6): 925-931

Hesham T. Naas: Department of Food Hygiene and Control, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.
Ramadan A. Edarhoby: Department of Food Hygiene and Control, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.
Aboubaker M. Garbaj: Department of Food Hygiene and Control, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.
Salah M. Azwai: Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.
Said K. Abolghait: Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt.
Fatim T. Gammoudi: Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.
Ashraf A. Moawad: Department of Food Hygiene and Control, Faculty of Veterinary Medicine, Cairo University, 12211 Giza 12211, Egypt.
Ilaria Barbieri: Department of Genetics, The Lombardy and Emilia Romagna Experimental Zootechnic Institute, Via Bianchi 9, Brescia 25124, Italy.
Ibrahim M. Eldaghayes: Department of Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Tripoli, P.O. Box 13662, Tripoli, Libya.

doi: 10.14202/vetworld.2019.925-931

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Article history: Received: 07-03-2019, Accepted: 13-05-2019, Published online: 29-06-2019

Corresponding author: Ibrahim M. Eldaghayes

E-mail: ibrahim.eldaghayes@vetmed.edu.ly

Citation: Naas HT, Edarhoby RA, Garbaj AM, Azwai SM, Abolghait SK, Gammoudi FT, Moawad AA, Barbieri I, Eldaghayes IM (2019) Occurrence, characterization, and antibiogram of Staphylococcus aureus in meat, meat products, and some seafood from Libyan retail markets, Veterinary World, 12(6): 925-931.
Abstract

Aim: The aim of the current investigation was to screen the presence of Staphylococci spp., especially S. aureus in meat, meat products of different animal species, and some seafood sold in some retail markets in Libya using cultural and molecular techniques, and to study their antibiotics resistance profiles.

Materials and Methods: A total of 139 samples from red meat, meat products, and seafood were collected from many areas in Libya. Enumeration and isolation of Staphylococci spp. and S. aureus by normal cultural methods followed by molecular identification using molecular techniques by bacterial DNA extraction and partial sequencing of 16S rDNA.

Results: Out of 139 samples, 112 (80.6%) were contaminated with different species of Staphylococci based on cultural characteristics of Staphylococci on Baird-Parker medium, for which S. aureus was detected in only 32 samples (23%). However, only six out of 18 (33.3%) isolates sent for sequencing were confirmed to be S. aureus using the molecular technique. The six identified isolates of S. aureus were tested for antimicrobial resistance against 24 most commonly used antibiotics. All isolates were resistant to only two antibiotics (cefotaxime and clindamycin). Among these six isolates, only one confirmed to be Methicillin-resistant Staphylococcus aureus.

Conclusion: Results of this study suggest that food of animal origin could be a source of S. aureus with antimicrobial resistance characteristics that can be spread through the food chain, and raise the importance of these results for public health.

Keywords: 16S rDNA, antibiogram, meat products, meat, seafood, Staphylococcus aureus.

References

1. Dai, X.H., Li, H.E., Lu, C.J., Wang, J.F., Dong, J., Wei, J.Y., Zhang, Y., Wang, X., Tan, W., Deng, X.M., Zhao, S.H. and Zhang, M.J. (2013) Liquiritigenin prevents Staphylococcus aureus-mediated lung cell injury via inhibiting the production of alpha-hemolysin. J. Asian Nat. Prod. Res., 15(4): 390-399. [Crossref] [PubMed]

2. Parker, D. and Prince, A. (2012) Immunopathogenesis of Staphylococcus aureus pulmonary infection. Semin. Immunopathol., 34(2): 281-297. [Crossref] [PubMed] [PMC]

3. Kulhankova, K., King, J. and Salgado-Pabon, W. (2014) Staphylococcal toxic shock syndrome: Superantigen-mediated enhancement of endotoxin shock and adaptive immune suppression. Immunol. Res., 59(1-3): 182-187. [Crossref] [PubMed]

4. Jusko, M., Potempa, J., Kantyka, T., Bielecka, E., Miller, H.K., Kalinska, M., Dubin, G., Garred, P., Shaw, L.N. and Blom, A.M. (2014) Staphylococcal proteases aid in evasion of the human complement system. J. Innate Immun., 6(1): 31-46. [Crossref] [PubMed] [PMC]

5. Doyle, M.E., Hartmann, F.A. and Lee Wong, A.C. (2012) Methicillin-resistant staphylococci: Implications for our food supply? Anim. Health Res. Rev., 13(2): 157-180. [Crossref] [PubMed]

6. Edwards, L.A., O'Neill, C., Furman, M.A., Hicks, S., Torrente, F., Perez-Machado, M., Wellington, E.M., Phillips, A.D. and Murch, S.H. (2012) Enterotoxin-producing staphylococci cause intestinal inflammation by a combination of direct epithelial cytopathy and superantigen-mediated T-cell activation. Inflamm. Bowel Dis., 18(4): 624-640. [Crossref] [PubMed]

7. Gundogan, N., Citak, S., Yucel, N. and Devren, A. (2005) A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci., 69(4): 807-810. [Crossref] [PubMed]

8. Hassanien, A.A. and Abdel-Aziz, N.M. (2017) Staphylococcus aureus and their enterotoxin genes in fast food and food handlers from different food premises in Sohag city, Egypt. Int. J. Agric. Sci. Vet. Med., 5(1): 107-113.

9. Ritter, A.C. and Tondo, E.C. (2014) Foodborne illnesses in Brazil: Control measures for 2014 FIFA World Cup travelers. J. Infect. Dev. Ctries., 8(3): 254-257. [Crossref] [PubMed]

10. Beyene, T., Hayishe, H., Gizaw, F., Beyi, A.F., Abunna, F., Mammo, B., Ayana, D., Waktole, H. and Abdi, R.D. (2017) Prevalence and antimicrobial resistance profile of Staphylococcus in dairy farms, abattoir and humans in Addis Ababa, Ethiopia. BMC Res. Notes, 10(1): 171. [Crossref] [PubMed] [PMC]

11. Schlegelova, J., Napravnikova, E., Dendis, M., Horvath, R., Benedik, J., Babak, V., Klimova, E., Navratilova, P. and Sustackova, A. (2004) Beef carcass contamination in a slaughterhouse and prevalence of resistance to antimicrobial drugs in isolates of selected microbial species. Meat Sci., 66(3): 557-565. [Crossref]

12. Waters, A.E., Contente-Cuomo, T., Buchhagen, J., Liu, C.M., Watson, L., Pearce, K., Foster, J.T., Bowers, J., Driebe, E.M. and Engelthaler, D.M. (2011) Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin. Infect. Dis., 52(10): 1227-1230. [Crossref] [PubMed] [PMC]

13. Otalu, O.J., Junaidu, K., Chukwudi, O.E. and Jarlath, U.V. (2011) Multi-drug resistant coagulase-positive S. aureus from live and slaughtered chickens in Zaria, Nigeria. Int. J. Poult. Sci., 10(11): 871-875. [Crossref]

14. Elshrek, Y.M., Madi, N.S., El-Bakoush, A.A. and El-Tawil, A. (2008) Microbiological studies of spiced beef burgers in Tripoli city, Libyan Arab Jamahiriya. East. Mediterr. Health J., 14(1): 172-178.

15. Naas, H.T., Garbaj, A.M., Elarbed, Z.M., Eshamah, H.L. and Abolghit, S.K. (2009a) Microbial status of beef burgers sold in Tripoli. J. Egypt. Acad. Soc. Environ. Dev., 10(2): 139-144.

16. Naas, H.T., Garbaj, A.M., Elarbed, Z.M., Eshamah, H.L. and Abolghit, S.K. (2009b) Microbial status of fresh beef sausage sold in Tripoli. Suez Canal Vet. Med. J., 14(2): 111-118.

17. 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. International Organization for Standardization, Geneva.

18. Kaysner, C.A. and DePaola, A. (2001) Vibrio. In: Downes, F.P. and Ito, K., editor. Compendium of Methods for the Microbiological Examination of Foods. American Public Health Association, Washington, DC. p405-420.

19. Azwai, S.M., Alfallani, E.A., Abolghait, S.K., Garbaj, A.M., Naas, H.T., Moawad, A.A., Gammoudi, F.T., Rayes, H.M., Barbieri, I. and Eldaghayes, I.M. (2016) Isolation and molecular identification of Vibrio spp. by sequencing of 16S rDNA from seafood, meat and meat products in Libya. Open Vet. J., 6(1): 36-43. [Crossref] [PubMed] [PMC]

20. Herlemann, D.P., Labrenz, M., Jurgens, K., Bertilsson, S., Waniek, J.J. and Andersson, A.F. (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J., 5(10): 1571-1579. [Crossref] [PubMed] [PMC]

21. Naas, H.T., Zurghani, M.M., Garbaj, A.M., Azwai, S.M., Eshamah, H.L., Gammoudi, F.T., Abolghait, S.K., Moawad, A.A., Barbieri, I. and Eldaghayes, I.M. (2018) Bacillus cereus as an emerging public health concern in Libya: Isolation and antibiogram from food of animal origin. Libyan J. Med. Sci., 2(2): 56-61. [Crossref]

22. Coyle, B.M. (2005) Manual of Antimicrobial Susceptibility Testing (Book). American Society for Microbiology Press, Washington DC.

23. Jean, B. and Patel, P.D. (2014) Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement (Electronic). Vol. 34. Clinical and Laboratory Standards Institute, Wayne.

24. LNCSM. (2009) Libyan National Center for Standardization and Metrology. LNCSM 600-2009. LNCSM, Libya.

25. Kadariya, J., Smith, T.C. and Thapaliya, D. (2014) Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health. Biomed. Res. Int., 2014: 827965. [Crossref] [PubMed] [PMC]

26. Cohen, N., Ennaji, H., Hassar, M. and Karib, H. (2006) The bacterial quality of red meat and offal in Casablanca (Morocco). Mol. Nutr. Food Res., 50(6): 557-562. [Crossref] [PubMed]

27. Martins, P.D., de Almeida, T.T., Basso, A.P., de Moura, T.M., Frazzon, J., Tondo, E.C. and Frazzon, A.P. (2013) Coagulase-positive staphylococci isolated from chicken meat: Pathogenic potential and vancomycin resistance. Foodborne Pathog. Dis., 10(9): 771-776. [Crossref] [PubMed]

28. Osman, K.M., Amer, A.M., Badr, J.M. and Saad, A.S. (2015) Prevalence and antimicrobial resistance profile of Staphylococcus species in chicken and beef raw meat in Egypt. Foodborne Pathog. Dis., 12(5): 406-413. [Crossref] [PubMed]

29. Goja, A.M., Ahmed, T.A.A., Saeed, S.A.M. and Dirar, H.A. (2013) Isolation and identification of Staphylococcus spp. in fresh beef. Pak. J. Nutr., 12(2): 114-120. [Crossref]

30. Rahimi, E., Nonahal, F. and Salehi, E.A. (2013) Detection of classical enterotoxins of Staphylococcus aureus strains isolated from raw meat in Esfahan, Iran. Health Scope, 2(2): 95-98. [Crossref]

31. Hanson, B.M., Dressler, A.E., Harper, A.L., Scheibel, R.P., Wardyn, S.E., Roberts, L.K., Kroeger, J.S. and Smith, T.C. (2011) Prevalence of Staphylococcus aureus and Methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J. Infect. Public Health, 4(4): 169-174. [Crossref] [PubMed]

32. Alaboudi, A.R., Jaradat, Z.W. and Shatnawi, M.M. (2012) Biotypes and enterotoxigenicity of staphylococci isolated from camel's meat in Jordan. Br. Microbiol. Res. J., 2(1): 23-35. [Crossref]

33. Greeson, K., Suliman, G.M., Sami, A., Alowaimer, A. and Koohmaraie, M. (2013) Frequency of antibiotic-resistant Salmonella, Escherichia coli, Enterococcus, and Staphylococcus aureus in meat in Saudi Arabia. Afr. J. Microbiol. Res., 7(4): 309-316. [Crossref]

34. Sun, D.W. (2011) Handbook of Frozen Food Processing and Packaging. 2nd ed. CRC Press, Boca Raton, FL.

35. Mensah, P., Yeboah-Manu, D., Owusu-Darko, K. and Ablordey, A. (2002) Street foods in Accra, Ghana: How safe are they? Bull. World Health Organ., 80(7): 546-554.

36. Nimri, L., Abu Al-Dahab, F. and Batchoun, R. (2014) Foodborne bacterial pathogens recovered from contaminated shawarma meat in Northern Jordan. J. Infect. Dev. Ctries., 8(11): 1407-1414. [Crossref] [PubMed]

37. Nespolo, N.M., Martineli, T.M. and Rossi, O.D Jr. (2012) Microbiological quality of salmon (Salmo salar) sold in cities of the state of Sao Paulo, Brazil. Braz. J. Microbiol., 43(4): 1393-1400. [Crossref]

38. Hammad, A.M., Watanabe, W., Fujii, T. and Shimamoto, T. (2012) Occurrence and characteristics of methicillin-resistant and-susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish. Int. J. Food Microbiol., 156(3): 286-289. [Crossref] [PubMed]

39. Sergelidis, D., Abrahim, A., Papadopoulos, T., Soultos, N., Martziou, E., Koulourida, V., Govaris, A., Pexara, A., Zdragas, A. and Papa, A. (2014) Isolation of Methicillin-resistant Staphylococcus spp. from ready-to-eat fish products. Lett. Appl. Microbiol., 59(5): 500-506. [Crossref] [PubMed]

40. Atanassova, V., Meindl, A. and Ring, C. (2001) Prevalence of Staphylococcus aureus and staphylococcal enterotoxins in raw pork and uncooked smoked ham-a comparison of classical culturing detection and RFLP-PCR. Int. J. Food Microbiol., 68(1-2): 105-113. [Crossref]

41. Tarabees, R.Z., Hassanin, Z.H. and EL Bagoury, A. (2015) Polymerase chain reaction (PCR): An alternative rapid method for detection of some microbial contamination of meat products. Alexandria J. Vet. Sci., 45(1): 91-98. [Crossref]

42. Tassew, H., Abdissa, A., Beyene, G. and Gebre-Selassie, S. (2010) Microbial flora and food borne pathogens on minced meat and their susceptibility to antimicrobial agents. Ethiop. J. Health Sci., 20(3): 137-143. [Crossref] [PubMed]

43. Hiroi, M., Kawamori, F., Harada, T., Sano, Y., Miwa, N., Sugiyama, K., Hara-Kudo, Y. and Masuda, T. (2012) Antibiotic resistance in bacterial pathogens from retail raw meats and food-producing animals in Japan. J. Food Prot., 75(10): 1774-1782. [Crossref] [PubMed]

44. de Boer, E., Zwartkruis-Nahuis, J.T., Wit, B., Huijsdens, X.W., de Neeling, A.J., Bosch, T., van Oosterom, R.A., Vila, A. and Heuvelink, A.E. (2009) Prevalence of Methicillin-resistant Staphylococcus aureus in meat. Int. J. Food Microbiol., 134(1-2): 52-56. [Crossref] [PubMed]

45. Boost, M., Ho, J., Guardabassi, L. and O'Donoghue, M. (2013) Colonization of butchers with livestock-associated Methicillin-resistant Staphylococcus aureus. Zoonoses Public Health, 60(8): 572-576. [Crossref] [PubMed]