| More

Prevalence and distribuion of staphylococcal enterotoxin genes among Staphylococcus aureus isolates from chicken and turkey carcasses in Algeria

Views: 413 Downloads: 321
F. Mebkhout, L. Mezali, T. M. Hamdi, Z. Cantekin, Y. Ergun, N. Ramdani-Bouguessa, P. Butaye
F. Mebkhout, L. Mezali, T. M. Hamdi, Z. Cantekin, Y. Ergun, N. Ramdani-Bouguessa, P. Butaye


This study is aimed to determine the prevalence of staphylococcus aureus (S.aureus) by biochemical tests in poultry carcasses. It is also intend to detect the distribution of genes for classical staphylococcal enterotoxins A, B, C, D and E (sea, seb, sec, sed and see) and for gene femA, specific for S.aureus species, using multiplex PCR. A total of 385 samples of neck skins from fresh poultry carcasses were collected during the period 2012-2013 from 16 different slaughterhouses located in the region of Algiers, Algeria. The overall prevalence of S.aureus in freshly slaughtered poultry carcasses was 41.56%, with an individual prevalence of 40.63% and 45.71% for chicken and turkey respectively. From the 95 strains of S.aureus identified by biochemical tests, 82 (86.32%) isolates were femA positive using multiplex PCR. The investigation has also revealed the presence of both enterotoxins B and D, with a predominance of seb (13.33%) followed by sed (1.67%), in the chicken carcasses while in turkey only sed was detected (4.55%) It has been found that strains of S.aureus of poultry origin can be enterotoxigenic with the predominance of genes encoding for enterotoxins seb in chicken and sed in turkey. As enterotoxins can be produced in adequate amounts to induce foodborne illnesses, these potential dangers must be considered in terms of a real risk to public health.


Staphylococcus aureus; Poultry carcasses; Staphylococcal entérotoxine; Algiers

Full Text:



Achi O, Madubuik C (2007) Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from retail ready-to-eat food in Nigeria. Res J Microbiol 2: 516-523.

Adams BW, Mead GC (1983) Incidence and properties of Staphylococcus aureus associated with turkeys during processing and further-processing operations. J Hyg (Lond) 91: 479-490.

Alloui N, Guergueb N, Ayachi A (2013) Relationship between the slaughtering hygienic practices and bacterial contamination of poultry carcass in the Biskra region (Algeria). Actes des 10èmes Journées de la Recherche Avicole et Palmipèdes à Foie Gras . ITAVI, La Rochelle, France., pp. 480-484.

Argudín MÁ, Mendoza MC, Rodicio MR (2010) Food Poisoning and Staphylococcus aureus Enterotoxins. Toxins 2: 1751-1773.

Aycicek H, Cakiroglu S, Stevenson TH (2005) Incidence of Staphylococcus aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control 16: 531-534.

Aydin 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. Int J Food Microbiol 148: 99-106.

Azelmad K, Hamadi F, Mimouni R, Amzil K, Latrache H, Mabrouki M, El Boulani A (2017) Adhesion of Staphylococcus aureus and Staphylococcus xylosus to materials commonly found in catering and domestic kitchens. Food Control 73: 156-163.

Benhamed N (2014) Evaluation de la qualité microbiologique et sanitaire du lait cru de vache dans la région d’Oran, Algérie : Etude du profil moléculaire virulent des Staphylococcus aureus impliquées dans les mammites bovines., Biologie. Université d’Oran, Oran, Algerie, p. 122.

Bergdoll MS (1991) Symposium on microbiology update: old friends and new enemies. Staphylococcus aureus. J Assoc Off Anal Chem 74: 706-710.

Bystron J, Molenda J, Bania J, Kosek-Paszkowska K, Czerw M (2005) Occurrence of enterotoxigenic strains of Staphylococcus aureus in raw poultry meat. Pol J Vet Sci 8: 37-40.

Chiang YC, Liao WW, Fan CM, Pai WY, Chiou CS, Tsen HY (2008) PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 121: 66-73.

Citak S, Duman T (2011) Staphylococcus aureus and coagulase-negative Staphylococcus from raw chicken samples in Turkey: Prevalence and antimicrobial resistance. Journal of Food, Agriculture & Environment 9: 156-158.

da Silva ER, do Carmo LS, da Silva N (2005) Detection of the enterotoxins A, B, and C genes in Staphylococcus aureus from goat and bovine mastitis in Brazilian dairy herds. Vet Microbiol 106:103-107.

El Allaoui A, Rhazi Filali F, Oumokhtar B (2013) Prevalence and Antibiogram Study of Escherichia coli and Staphylococcus aureus in turkey meat in Morocco. Anal Pharmaceut Acta 4: 270.

Escudero-Gilete ML, González-Miret ML, Temprano RM, Heredia FJ (2007) Application of a multivariate concentric method system for the location of Listeria monocytogenes in a poultry slaughterhouse. Food Control 18: 69-75.

Genigeorgis CA (1989) Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol 9: 327-360.

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

Hazariwala A, Sanders Q, Hudson CR, Hofacre C, Thayer SG, Maurer JJ (2002) Distribution of staphylococcal enterotoxin genes among Staphylococcus aureus isolates from poultry and humans with invasive staphylococcal disease. Avian Dis 46: 132-136.

ISO (2004) NF EN ISO 6888-1/A1, 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.

Jorgensen HJ, Mork T, Hogasen HR, Rorvik LM (2005) Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol 99: 158-166.

Kiliç S, Kuplulu O (2009) Detection the enterotoxin producing capacity of coagulase positive Staphylococcus by EIA (Enzyme Immuno Assay) isolated from turkey meat . Ankara Üniv Vet Fak Derg, 56, 183-186, 2009

Katsuda K, Hata E, Kobayashi H, Kohmoto M, Kawashima K, Tsunemitsu H, Eguchi M (2005) Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Vet Microbiol 105: 301-305.

Khallaf M, Benbakhta B, Nasri I, Bouchaib S, Senouci S, Ennaji MM (2014) Prevalence of Staphylococcus aureus isolated from chicken meat marketed in Rabat, Morocco. International Journal of Innovation and Applied Studies 7: 1665-1670.

Kitai S, Shimizu A, Kawano J, Sato E, Nakano C, Kitagawa H, Fujio K, Matsumura K, Yasuda R, Inamoto T (2005) Prevalence and characterization of Staphylococcus aureus and enterotoxigenic Staphylococcus aureus in retail raw chicken meat throughout Japan. J Vet Med Sci 67: 269-274.

Kluytmans JAJW, Wertheim HFL (2005) Nasal Carriage of Staphylococcus aureus and Prevention of Nosocomial Infections. Infection 33: 3-8.

Koluman A, Unlu T, Dikici A, Tezel A, Akcelik E, Burkan Z (2011) Presence of staphylococcus aureus and staphylococcal enterotoxins in different foods. Kafkas Univ Vet Fak Derg 17 S55-S60.

Kotula KL, Pandya Y (1995) Bacterial contamination of broiler chickens before scalding. J Food Prot 58: 1326-1329.

Larsen HD, Sloth KH, Elsberg C, Enevoldsen C, Pedersen LH, Eriksen NH, Aarestrup FM, Jensen NE (2000) The dynamics of Staphylococcus aureus intramammary infection in nine Danish dairy herds. Vet Microbiol 71: 89-101.

Letertre C, Perelle S, Dilasser F, Fach P (2003) Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. Journal of Applied Microbiology 95: 38-43.

Lindblad M, Lindmark H, Lambertz ST, Lindqvist R (2006) Microbiological baseline study of broiler chickens at Swedish slaughterhouses. J Food Prot 69: 2875-2882.

Madahi H, Rostami F, Rahimi E, Safarpoor Dehkordi F (2014) Prevalence of Enterotoxigenic Staphylococcus aureus Isolated From Chicken Nugget in Iran. Jundishapur J Microbiol 7: e10237.

Mehrotra M, Wang G, Johnson WM (2000) Multiplex PCR for Detection of Genes for Staphylococcus aureus Enterotoxins, Exfoliative Toxins, Toxic Shock Syndrome Toxin 1, and Methicillin Resistance. Journal of Clinical Microbiology 38: 1032-1035.

Nader YM, Reham MA, Engy FE (2016) Incidence of Staphylococcus aureus and Salmonella in Poultry Meat. Global Veterinaria 16:570-578.

Nemati M (2013) Prevalence of Enterotoxin Genes in Poultry Staphylococcus aureus Isolates. Bull Env Pharmacol Life Sci 3: 277-281.

Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, Santagada G, Firinu A, Crisetti E, Celano GV (2007) Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 115: 290-296.

Orden JA, Goyache J, Hernandez J, Domenech A, Suarez G, Gomez-Lucia E (1992) Detection of enterotoxins and TSST-1 secreted by Staphylococcus aureus isolated from ruminant mastitis. Comparison of ELISA and immunoblot. J Appl Bacteriol 72: 486-489.

Pacholewicz E, Sura Barus SA, Swart A, Havelaar AH, Lipman LJA, Luning PA (2016) Influence of food handlers’ compliance with procedures of poultry carcasses contamination: A case study concerning evisceration in broiler slaughterhouses. Food Control 68: 367-378.

Rosec JP, Guiraud JP, Dalet C, Richard N (1997) Enterotoxin production by staphylococci isolated from foods in France. Int J Food Microbiol 35: 213-221.

Sambrock J, W. Russel D (2001) Molecular Cloning: A Laboratory Manual(3rd edition). Sarrafzadeh Zargar MH, Hosseini Doust R, Mohebati Mobarez A (2014) Staphylococcus aureus Enterotoxin A Gene Isolated From Raw Red Meat and Poultry in Tehran, Iran. Int J Enteric Pathog 2: 2-16085.

Sasidharan S, Prema B, Yoga LL (2011) Antimicrobial drug resistance of Staphylococcus aureus in dairy products. Asian Pacific Journal of Tropical Biomedicine 1: 130-132.

Smyth DS, Hartigan PJ, Meaney WJ, Fitzgerald JR, Deobald CF, Bohach GA, Smyth CJ (2005) Superantigen genes encoded by the egc cluster and SaPIbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry. J Med Microbiol 54: 401-411.

Smyth JA, McNamee PT (2008) Chapter 17 - Staphylococci, streptococci and enterococci A2 - Pattison, Mark. in: McMullin, P.F., Bradbury, J.M., Alexander, D.J. (Eds.), Poultry Diseases (Sixth Edition), W.B. Saunders, Edinburgh: pp. 191-199.

Teramoto H, Salaheen S, Biswas D (2016) Contamination of post-harvest poultry products with multidrug resistant Staphylococcus aureus in Maryland-Washington DC metro area. Food Control 65: 132-135.

Wang X, Tao X, Xia X, Yang B, Xi M, Meng J, Zhang J, Xu B (2013) Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail raw chicken in China. Food Control 29: 103-106.


  • There are currently no refbacks.


Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.