Skip to main content
Log in

Molecular Typing, Phenotypic and Genotypic Assessment of Antibiotic Resistance and Virulence Factors amongst the Staphylococcus aureus Bacteria Isolated from Raw Chicken Meat

  • EXPERIMENTAL PAPERS
  • Published:
Molecular Genetics, Microbiology and Virology Aims and scope Submit manuscript

Abstract

The present research was performed to evaluate the phenotypic and genotypic properties of antibiotic resistance, virulence factor profiles and molecular typing of Staphylococcus aureus strains isolated from chicken meat. A total of 36 S. aureus strains were isolated from 300 raw chicken meat samples. Phenotypic pattern of antibiotic resistance was assessed by disk diffusion. Distribution of antibiotic resistance and virulence genes was evaluated by PCR. Molecular typing of isolates was performed by the ERIC-PCR. Considering the over than 80% similarity, 36 S. aureus isolates were classified in 9 different profiles with 43 to 100% similarities. S. aureus strains showed the highest incidence of resistance against penicillin (100%), tetracycline (91.66%), cephalothin (100%), ciprofloxacin (75%), erythromycin (75%), mupirocin (63.88%), clindamycin (61.11%) and trimethoprim/sulfamethoxazole (61.11%). The most commonly detected antibiotic resistance genes amid the S. aureus isolates were mecA (100%), tetK (80.55%), tetM (66.66%), aacA (6'')/aphD (2'') (61.11%), msrA (55.55%) and ermA (55.55%). Total distribution of etB, etA, tsst-1, clfA and coa virulence factors amongst the S. aureus strains was 61.11, 58.33, 13.88, 75 and 100%, respectively. Genetic cluster of bacteria affected the antibiotic resistance and virulence characters of S. aureus strains. S. aureus strains with the same ERIC-genetic cluster had similar antibiotic resistance and virulence characters which may show their similar origins. Presence of one or more virulence factors and antibiotic resistance genes amongst the resistant S. aureus strains signifies an important public health threat rendering the consumption of raw or undercooked chicken meat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.

REFERENCES

  1. Abdolmaleki, Z., Mashak, Z., and Dehkordi, F.S., Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches, Antimicrob. Resist. Infect. Control, 2019, vol. 8, no. 1, p. 54.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Adwan, G., Adwan, K., Jarrar, N., and Amleh, A., Molecular detection of nine antibiotic resistance genes in methicillin resistant Staphylococcus aureus isolates, Rom. Arch. Microbiol. Immunol., 2014, vol. 73, nos. 1–2, pp. 9–18.

    CAS  Google Scholar 

  3. Akanbi, O.E., Njom, H.A., Fri, J., Otigbu, A.C., and Clarke, A.M., Antimicrobial susceptibility of Staphylococcus aureus isolated from recreational waters and beach sand in Eastern Cape Province of South Africa, Int. J. Environ. Res. Public Health, 2017, vol. 14, no. 9, p. 1001.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Akbar, A. and Anal, A.K., Prevalence and antibiogram study of Salmonella and Staphylococcus aureus in poultry meat, Asian Pac. J. Trop. Biomed., 2013, vol. 3, no. 2, pp. 163–168.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Akindolire, M.A., Kumar, A., and Ateba, C.N., Genetic characterization of antibiotic-resistant Staphylococcus aureus from milk in the North-West Province, South Africa, Saudi J. Biol. Sci., 2018, vol. 25, no. 7, pp. 1348–1355.

    Article  CAS  PubMed  Google Scholar 

  6. Ali, Y., Islam, M.A., Muzahid, N.H., Sikder, M.O.F., Hossain, M.A., and Marzan, L.W., Characterization, prevalence and antibiogram study of Staphylococcus aureus in poultry, Asian Pac. J. Trop. Biomed., 2017, vol. 7, no. 3, pp. 253–256.

    Article  Google Scholar 

  7. Amoako, D.G., Somboro, A.M., Abia, A.L., Molechan, C., Perrett, K., Bester, L.A., et al., Antibiotic resistance in Staphylococcus aureus from poultry and poultry products in uMgungundlovu district, South Africa, Using the “Farm to Fork” approach, Microb. Drug Resist., 2019, vol. 26, no. 2, pp. 402–411.

    Article  PubMed  Google Scholar 

  8. Bantawa, K., Sah, S.N., Limbu, D.S., Subba, P., and Ghimire, A., Antibiotic resistance patterns of Staphylococcus aureus, Escherichia coli, Salmonella, Shigella and Vibrio isolated from chicken, pork, buffalo and goat meat in eastern Nepal, BMC Res. Notes, 2019, vol. 12, no. 1, pp. 1–6.

    Article  Google Scholar 

  9. Chaalal, W., Chaalal, N., Bourafa, N., Kihal, M., Diene, S.M., and Rolain, J.-M., Characterization of Staphylococcus aureus isolated from food products in Western Algeria, Foodborne Pathog. Dis., 2018, vol. 15, no. 6, pp. 353–360.

    Article  CAS  PubMed  Google Scholar 

  10. Performance Standards for Antimicrobial Susceptibility Testing, 25th Informational Supplement, M100-S25, Wayne, PA: Clinical and Laboratory Standards Institute, 2015.

  11. Codjoe, F.S., Brown, C.A., Smith, T.J., Miller, K., and Donkor, E.S., Genetic relatedness in carbapenem-resistant isolates from clinical specimens in Ghana using ERIC-PCR technique, PLoS One, 2019, vol. 14, no. 9, p. e0222168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Coelho, S.M., Reinoso, E., Pereira, I.A., Soares, L.C., Demo, M., Bogni, C., et al., Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from bovine mastitis in Rio de Janeiro, Pesqui. Vet. Bras., 2009, vol. 29, no. 5, pp. 369–374.

    Article  Google Scholar 

  13. Daka, D. and Yihdego, D., Antibiotic-resistance Staphylococcus aureus isolated from cow’s milk in the Hawassa area, South Ethiopia, Ann. Clin. Microbiol. Antimicrob., 2012, vol. 11, no. 1, p. 26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dehkordi, S.F., Basti, A., Gandomi, H., Misaghi, A., and Rahimi, E., Pathogenic Staphylococcus aureus in hospital food samples; prevalence and antimicrobial resistance properties, J. Food Saf., 2019, vol. 38, article no. E12501 (Retraction).

    Google Scholar 

  15. Feßler, A.T., Kadlec, K., Hassel, M., Hauschild, T., Eidam, C., Ehricht, R., Monecke, S., and Schwarz, S., Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany, Appl. Environ. Microbiol., 2011, vol. 77, no. 20, pp. 7151–7157.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Gomes, R.M., Bomfim, M.R.Q., Trindade, M.J., Farias, L.M., and Santos, S.G., Potential spread of methicillin-resistant Staphylococcus aureus recovered from patients with bloodstream infection, Chemother.: Open Access, 2015, vol. 4, no. 2, p. 1000149.

    Article  Google Scholar 

  17. Govender, V., Madoroba, E., Magwedere, K., Fosgate, G., and Kuonza, L., Prevalence and risk factors contributing to antibiotic-resistant Staphylococcus aureus isolates from poultry meat products in South Africa, 2015–2016, J. S. Afr. Vet. Assoc., 2019, vol. 90, no. 1, pp. 1–8.

    Article  Google Scholar 

  18. Groves, M.D., Crouch, B., Coombs, G.W., Jordan, D., Pang, S., Barton, M.D., et al., Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolated from Australian veterinarians, PLoS One, 2016, vol. 11, no. 1, p. e0146034.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hasanpour Dehkordi, A., Khaji, L., Sakhaei Shahreza, M., Mashak, Z., Safarpoor Dehkordi, F., Safaee, Y., et al., One-year prevalence of antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus recovered from raw meat, Trop. Biomed., 2017, vol. 34, no. 2, pp. 396–404.

    CAS  PubMed  Google Scholar 

  20. Haskell, K.J., Schriever, S.R., Fonoimoana, K.D., Haws, B., Hair, B.B., Wienclaw, T.M., et al., Antibiotic resistance is lower in Staphylococcus aureus isolated from antibiotic-free raw meat as compared to conventional raw meat, PLoS One, 2018, vol. 13, no. 12, p. e0206712.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Heidari, M., Momtaz, H., and Madani, M., Detection of the antibiotic resistance genes in Staphylococcus aureus isolated from human infections and bovine mastitis, Afr. J. Microbiol. Res., 2011, vol. 5, no. 31, pp. 5745–5749.

    CAS  Google Scholar 

  22. Hemmatinezhad, B., Khamesipour, F., Mohammadi, M., Safarpoor Dehkordi, F., and Mashak, Z., Microbiological investigation of O-serogroups, virulence factors and antimicrobial resistance properties of Shiga toxin-producing Escherichia coli isolated from ostrich, turkey and quail meats, J. Food Saf., 2015, vol. 35, no. 4, pp. 491–500.

    Article  CAS  Google Scholar 

  23. Hiroi, M., Kawamori, F., Harada, T., Sano, Y., Miwa, N., Sugiyama, K., et al., Antibiotic resistance in bacterial pathogens from retail raw meats and food-producing animals in Japan, J. Food Prot., 2012, vol. 75, no. 10, pp. 1774–1782.

    Article  CAS  PubMed  Google Scholar 

  24. Hizlisoy, H., Onmaz, N.E., Karadal, F., Serhat, A., Yildirim, Y., Gonulalan, Z., et al., Antibiotic resistance gene profiles of Staphylococcus aureus isolated from foods of animal origin, Kafkas Univ. Vet. Fak. Derg., 2018, vol. 24, no. 2, pp. 243–249.

    Google Scholar 

  25. Jackson, C.R., Davis, J.A., and Barrett, J.B., Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia, J. Clin. Microbiol., 2013, vol. 51, no. 4, pp. 1199–1207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Jamali, H., Paydar, M., Radmehr, B., Ismail, S., and Dadrasnia, A., Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products, Food Control, 2015, vol. 54, pp. 383–388.

    Article  CAS  Google Scholar 

  27. Johler, S., Layer, F., and Stephan, R., Comparison of virulence and antibiotic resistance genes of food poisoning outbreak isolates of Staphylococcus aureus with isolates obtained from bovine mastitis milk and pig carcasses, J. Food Prot., 2011, vol. 74, no. 11, pp. 1852–1859.

    Article  CAS  PubMed  Google Scholar 

  28. Karahan, M., Acik, M.N., and Cetinkaya, B., Investigation of virulence genes by PCR in Staphylococcus aureus isolates originated from subclinical bovine mastitis in Turkey, Pak. Vet. J., 2011, vol. 31, no. 3, pp. 249–253.

    CAS  Google Scholar 

  29. Koosha, R.Z., Fooladi, A.A.I., Hosseini, H.M., and Aghdam, E.M., Prevalence of exfoliative toxin A and B genes in Staphylococcus aureus isolated from clinical specimens, J. Infect. Public Health, 2014, vol. 7, no. 3, pp. 177–185.

    Article  PubMed  Google Scholar 

  30. Kumar, R., Yadav, B., and Singh, R., Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle, Curr. Microbiol., 2010, vol. 60, no. 5, pp. 379–386.

    Article  CAS  PubMed  Google Scholar 

  31. Li, H., Andersen, P., Stegger, M., Sieber, R., Ngmer, H., Staubrand, N., et al., Antimicrobial resistance and virulence gene profiles of methicillin-resistant and -susceptible Staphylococcus aureus from food products in Denmark, Front. Microbiol., 2019, vol. 10, p. 2681.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lin, Q., Sun, H., Yao, K., Cai, J., Ren, Y., and Chi, Y., The prevalence, antibiotic resistance and biofilm formation of Staphylococcus aureus in bulk ready-to-eat foods, Biomolecules, 2019, vol. 9, no. 10, p. 524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lina, G., Quaglia, A., Reverdy, M.E., Leclercq, R., Vandenesch, F., and Etienne, J., Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci, Antimicrob. Agents Chemother., 1999, vol. 43, no. 5, pp. 1062–1066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Louws, F.J., Fulbright, D.W., Stephens, C.T., and De Bruijn, F., Specific genomic fingerprints of phytopathogenic Xanthomonas and Pseudomonas pathovars and strains generated with repetitive sequences and PCR, Appl. Environ. Microbiol., 1994, vol. 60, no. 7, pp. 2286–2295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Martineau, F., Picard, F.J., Lansac, N., Ménard, C., Roy, P.H., Ouellette, M., et al., Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis, Antimicrob. Agents Chemother., 2000, vol. 44, no. 2, pp. 231–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mashak, Z., Jafariaskari, S., Alavi, I., Shahreza, M.S., and Dehkordi, F.S., Phenotypic and genotypic assessment of antibiotic resistance and genotyping of vacA, cagA, iceA, oipA, cagE, and babA2 alleles of Helicobacter pylori bacteria isolated from raw meat, Infect. Drug Resist., 2020, vol. 13, p. 257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Merz, A., Stephan, R., and Johler, S., Staphylococcus aureus isolates from goat and sheep milk seem to be closely related and differ from isolates detected from bovine milk, Front. Microbiol., 2016, vol. 7, p. 319.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Momtaz, H., Davood Rahimian, M., and Safarpoor Dehkordi, F., Identification and characterization of Yersinia enterocolitica isolated from raw chicken meat based on molecular and biological techniques, J. Appl. Poult. Res., 2013, vol. 22, no. 1, pp. 137–145.

    Article  CAS  Google Scholar 

  39. Momtaz, H., Dehkordi, F.S., Rahimi, E., Asgarifar, A., and Momeni, M., Virulence genes and antimicrobial resistance profiles of Staphylococcus aureus isolated from chicken meat in Isfahan province, Iran, J. Appl. Poult. Res., 2013, vol. 22, no. 4, pp. 913–921.

    Article  CAS  Google Scholar 

  40. Momtaz, H., Rahimi, E., and Tajbakhsh, E., Detection of some virulence factors in Staphylococcus aureus isolated from clinical and subclinical bovine mastitis in Iran, Afr. J. Biotechnol., 2010, vol. 9, no. 25, pp. 3753–3758.

    CAS  Google Scholar 

  41. Moon, J.S., Lee, A.R., Kang, H.M., Lee, E.S., Kim, M.N., Paik, Y., et al., Phenotypic and genetic antibiogram of methicillin-resistant staphylococci isolated from bovine mastitis in Korea, J. Dairy Sci., 2007, vol. 90, no. 3, pp. 1176–1185.

    Article  CAS  PubMed  Google Scholar 

  42. Oksuz, L., Dupieux, C., Tristan, A., Bes, M., Etienne, J., and Gurler, N., The high diversity of MRSA clones detected in a university hospital in Istanbul, Int. J. Med. Sci., 2013, vol. 10, no. 12, p. 1740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Osman, K., Badr, J., Al-Maary, K.S., Moussa, I.M., Hessain, A.M., Girah, Z., et al., Prevalence of the antibiotic resistance genes in coagulase-positive- and negative-Staphylococcus in chicken meat retailed to consumers, Front. Microbiol., 2016, vol. 7, p 1846.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Paludi, D., Vergara, A., Festino, A.R., Di Ciccio, P., Costanzo, C., Conter, M., et al., Antimicrobial resistance pattern of methicillin-resistant Staphylococcus aureus in the food industry, J. Biol. Regul. Homeostatic Agents, 2011, vol. 25, no. 4, p. 671.

    CAS  Google Scholar 

  45. Pehlivanoğlu, F. and Yardımcı, H., Detection of methicillin and vancomycin resistance in Staphylococcus strains isolated from bovine milk samples with mastitis, Kafkas Univ. Vet. Fak. Derg., 2012, vol. 18, no. 5, pp. 849–855.

    Google Scholar 

  46. Pekana, A. and Green, E., Antimicrobial resistance profiles of Staphylococcus aureus isolated from meat carcasses and bovine milk in abattoirs and dairy farms of the Eastern Cape, South Africa, Int. J. Environ. Res. Public Health, 2018, vol. 15, no. 10, p. 2223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Puah, S.M., Chua, K.H., and Tan, J.A.M.A., Virulence factors and antibiotic susceptibility of Staphylococcus aureus isolates in ready-to-eat foods: detection of S. aureus contamination and a high prevalence of virulence genes, Int. J. Environ. Res. Public Health, 2016, vol. 13, no. 2, p. 199.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Rahi, A., Kazemeini, H., Jafariaskari, S., Seif, A., Hosseini, S., and Dehkordi, F.S., Genotypic and phenotypic-based assessment of antibiotic resistance and profile of staphylococcal cassette chromosome mec in the methicillin-resistant Staphylococcus aureus recovered from raw milk, Infect. Drug Resist., 2020, vol. 13, p. 273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rahimi, E., Yazdanpour, S., and Dehkordi, F., Detection of Toxoplasma gondii antibodies in various poultry meat samples using enzyme linked immuno sorbent assay and its confirmation by polymerase chain reaction, J. Pure Appl. Microbiol., 2014, vol. 8, no. 1, pp. 421–427.

    Google Scholar 

  50. Rahimi, F. and Karimi, S., Characteristics of methicillin resistant Staphylococcus aureus strains isolated from poultry in Iran, Arch. Clin. Infect. Dis., 2015, vol. 10, no. 4, p. e30885.

    Article  Google Scholar 

  51. Rahimi, H., Saei, H.D., and Ahmadi, M., Nasal carriage of Staphylococcus aureus: Frequency and antibiotic resistance in healthy ruminants, Jundishapur J. Microbiol., 2015, vol. 8, no. 10, p. e22413.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Ranjbar, R., Dehkordi, F.S., Shahreza, M.H.S., and Rahimi, E., Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products, Antimicrob. Resist. Infect. Control, 2018, vol. 7, no. 1, p. 53.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Ranjbar, R., Farsani, F.Y., and Dehkordi, F.S., Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk, Antimicrob. Resist. Infect. Control, 2018, vol. 7, no. 1, p. 115.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Ranjbar, R., Masoudimanesh, M., Dehkordi, F.S., Jonaidi-Jafari, N., and Rahimi, E., Shiga (Vero)-toxin producing Escherichia coli isolated from the hospital foods; virulence factors, o-serogroups and antimicrobial resistance properties, Antimicrob. Resist. Infect. Control, 2017, vol. 6, no. 1, p. 4.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Ranjbar, R., Shahreza, M.H.S., Rahimi, E., and Jonaidi-Jafari, N., Methicillin-resistant Staphylococcus aureus isolates from Iranian restaurant food samples: Panton-Valentine Leukocidin, SCCmec phenotypes and antimicrobial resistance, Trop. J. Pharm. Res., 2017, vol. 16, no. 8, pp. 1939–1949.

    Article  CAS  Google Scholar 

  56. Ranjbar, R., Yadollahi Farsani, F., and Safarpoor Dehkordi, F., Antimicrobial resistance and genotyping of vacA, cagA, and iceA alleles of the Helicobacter pylori strains isolated from traditional dairy products, J. Food Saf., 2019, vol. 39, no. 2, p. e12594.

    Article  Google Scholar 

  57. Riva, A., Borghi, E., Cirasola, D., Colmegna, S., Borgo, F., Amato, E., et al., Methicillin-resistant Staphylococcus aureus in raw milk: Prevalence, SCC mec typing, enterotoxin characterization, and antimicrobial resistance patterns, J. Food Prot., 2015, vol. 78, no. 6, pp. 1142–1146.

    Article  CAS  PubMed  Google Scholar 

  58. Safarpoor Dehkordi, F., Gandomi, H., Akhondzadeh Basti, A., Misaghi, A., and Rahimi, E., Phenotypic and genotypic characterization of antibiotic resistance of methicillin-resistant Staphylococcus aureus isolated from hospital food, Antimicrob. Resist. Infect. Control, 2017, vol. 6, no. 1, p. 104.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Sallam, K.I., Abd-Elghany, S.M., Elhadidy, M., and Tamura, T., Molecular characterization and antimicrobial resistance profile of methicillin-resistant Staphylococcus aureus in retail chicken, J. Food Prot., 2015, vol. 78, no. 10, pp. 1879–1884.

    Article  CAS  PubMed  Google Scholar 

  60. Shopsin, B., Gomez, M., Waddington, M., Riehman, M., and Kreiswirth, B., Use of coagulase gene (coa) repeat region nucleotide sequences for typing of methicillin-resistant Staphylococcus aureus strains, J. Clin. Microbiol., 2000, vol. 38, no. 9, pp. 3453–3456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Strommenger, B., Kettlitz, C., Werner, G., and Witte, W., Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus, J. Clin. Microbiol., 2003, vol. 41, no. 9, pp. 4089–4094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Stutz, K., Stephan, R., and Tasara, T., SpA, ClfA, and FnbA genetic variations lead to Staphaurex test-negative phenotypes in bovine mastitis Staphylococcus aureus isolates, J. Clin. Microbiol., 2011, vol. 49, no. 2, pp. 638–646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Sukhumungoon, P., Bunnueang, N., Butsabong, N., Sae-lim, A., and Rattanachuay, P., Characterization of Staphylococcus spp, from meat and ready-to-eat food, Hat Yai city, Songkhla, Thailand, Southeast Asian J. Trop. Med. Public Health, 2018, vol. 49, no. 1, pp. 96–107.

    Google Scholar 

  64. Versalovic, J., Schneider, M., de Bruijn, F.J., and Lupski, J.R., Genomic fingerprinting of bacteria using repetitive sequence-based PCR (rep-PCR), Methods Mol. Cell. Biol., 1994, vol. 5, pp. 25–40.

    CAS  Google Scholar 

  65. Waryah, C.B., Gogoi-Tiwari, J., Wells, K., Eto, K.Y., Masoumi, E., Costantino, P., et al., Diversity of virulence factors associated with West Australian methicillin-sensitive Staphylococcus aureus isolates of human origin, BioMed Res. Int., 2016, vol. 2016, p. 8651918.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Wendlandt, S., Schwarz, S., and Silley, P., Methicillin-resistant Staphylococcus aureus: A food-borne pathogen?, Annu. Rev. Food Sci. Technol., 2013, vol. 4, pp. 117–139.

    Article  CAS  PubMed  Google Scholar 

  67. Wu, S., Huang, J., Wu, Q., Zhang, J., Zhang, F., Yang, X., et al., Staphylococcus aureus isolated from retail meat and meat products in China: Incidence, antibiotic resistance and genetic diversity, Front. Microbiol., 2018, vol. 9, p. 2767.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Yadav, R., Sharma, S.K., Yadav, J., and Kataria, A.K., Typing of Staphylococcus aureus obtained from mastitic milk of cattle and buffalo on the basis of two virulence-associated genes (spa and clfA), Vet. World, 2015, vol. 8, no. 3, p. 398.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Yang, X., Yu, S., Wu, Q., Zhang, J., Wu, S., and Rong, D., Multilocus sequence typing and virulence-associated gene profile analysis of Staphylococcus aureus isolates from retail ready-to-eat food in China, Front. Microbiol., 2018, vol. 9, p. 197.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ye, Y., Jiang, Q., Wu, Q., Zhang, J., Lu, J., and Lin, L., The characterization and comparison of Staphylococcus aureus by antibiotic susceptibility testing, enterobacterial repetitive intergenic consensus-polymerase chain reaction, and random amplified polymorphic DNA-polymerase chain reaction, Foodborne Pathog. Dis., 2012, vol. 9, no. 2, pp. 168–171.

    Article  CAS  PubMed  Google Scholar 

  71. Zmantar, T., Chaieb, K., Abdallah, F.B., Kahla-Nakbi, A.B., Hassen, A.B., Mahdouani, K., et al., Multiplex PCR detection of the antibiotic resistance genes in Staphylococcus aureus strains isolated from auricular infections, Folia Microbiol., 2008, vol. 53, no. 4, p. 357.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors would like to thank Dr. Mohammad Zavarshani for his assistance in sample collection. This work was financially supported by the Islamic Azad University, Shahrekord Branch, Shahrekord, Iran.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sepideh Karimi or Hassan Momtaz.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

The research was extracted from the PhD thesis in the field of Microbiology and was ethically approved by the Council of Research of the Faculty of Basic Science, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran (Consent Ref no. IR.IAU.SHK.REC.1398.051). Verification of this research project and the licenses related to sampling process were approved by the Prof. Hassan Momtaz (Approval Ref no. MIC201946).

Conflict of Interest

The authors declare that they have no conflicts of interest.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karimi, S., Momtaz, H. Molecular Typing, Phenotypic and Genotypic Assessment of Antibiotic Resistance and Virulence Factors amongst the Staphylococcus aureus Bacteria Isolated from Raw Chicken Meat. Mol. Genet. Microbiol. Virol. 37, 226–241 (2022). https://doi.org/10.3103/S0891416822040073

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0891416822040073

Keywords:

Navigation