doi: 10.14202/vetworld.2017.1205-1211
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Article history: Received: 21-04-2017, Accepted: 11-09-2017, Published online: 09-10-2017
Corresponding author: A. A. Samy
E-mail: ayman_samy@hotmail.com
Citation: El Seedy FR, Samy AA, Salam HSH, Khairy EA, Koraney AA (2017) Polymerase chain reaction detection of genes responsible for multiple antibiotic resistance Staphylococcus aureus isolated from food of animal origin in Egypt, Veterinary World, 10(10): 1205-1211.Aim: The aim of our study was polymerase chain reaction (PCR) detection of the genes responsible for the multiple antibiotic resistance S. aureus isolated from food of animal origin in Egypt.
Materials and Methods: A total of 125 samples were randomly collected from milk, meat, and their products from Giza and Beni-Suef Governorates markets. The S. aureus isolates were subjected to antimicrobial sensitivity tests using four antibacterial disks (Oxoid), and then the polymerase chain reaction (PCR) was performed for detection of antibiotic resistance genes.
Results: Out of 125 samples, 19 S. aureus isolates were detected. All detected isolates were multiple drug resistance (MDR). The penicillin-, erythromycin-, kanamycin-, and tetracycline-resistant isolates were examined by PCR for resistance genes blaZ, (msrA, ermB, and ermC), aac(6')aph (2''), and tetK. The isolates harbored these resistance genes with percentage of 100% (100%, 0%, and 100%), 62.5%, and 100%, respectively.
Conclusion: Contaminated foods of animal origin may represent a source of MDR S. aureus that can be a major threat to public health.
Keywords: food of animal origin, multiple antibiotic resistance, polymerase chain reaction, resistance genes, Staphylococcus aureus.
1. Hawkey, P.M. and Jones, A.M. (2009) The changing epidemiology of resistance. J. Antimicrob. Chemother., 64 Suppl 1: i3-10. [Crossref] [PubMed]
2. Arenas, N.E., Abril, D.A., Valencia, P., Khandige, S., Soto, C.Y. and Moreno-Melo, V. (2017) Screening food-borne and zoonotic pathogens associated with livestock practices in the Sumapaz region, Cundinamarca, Colombia. Trop. Anim. Health Prod., 49(4): 739-745. [Crossref] [PubMed] [PMC]
3. Threlfall, E.J., Ward, L.R., Frost, J.A. and Willshaw, G.A. (2000) The emergence and spread of antibiotic resistance in food-borne bacteria. Int. J. Food Microbiol., 62: 1-5. [Crossref]
4. Chiu, C.H., Wu, T.L., Su, L.H., Chu, C., Chia, J.H., Kuo, A.J., Chien, M.S. and Lin, T.Y. (2002) The emergence in Taiwan of ?uoroquinolone resistance in Salmonella enterica serotype choleraesuis. N. Engl. J. Med., 346: 413-419. [Crossref] [PubMed]
5. O'Brien, A.M., Hanson, B.M., Farina, S.A., Wu, J.Y., Simmering, J.E. and Wardyn, S.E. (2012), MRSA in conventional and alternative retail pork products. PLoS One, 7(1): 30092. [Crossref]
6. Teuber, M. (2001), Veterinary use and antibiotic resistance. Curr. Opin. Microbiol., 4: 493-499. [Crossref]
7. Leibler, J.H., Jordan, J.A., Brownstein, K., Lander, L., Price, L.B. and Perry, M.J. (2016) Staphylococcus aureus nasal carriage among beef packing workers in a Midwestern United States slaughterhouse. PLoS One, 11(2): e0148789. [Crossref] [PubMed] [PMC]
8. Munsch-Alatossava, P. and Alatossava, T. (2007) Antibiotic resistance of raw-milk-associated psychrotrophic bacteria. Microbiol. Res., 162(2): 115-123. [Crossref] [PubMed]
9. White, D.G., Zhao, S., Sudler, R., Ayers, S., Friedman, S., Chen, S., McDermott, P.F., McDermott, S., Wagner, D.D. and Meng J. (2001) The isolation of antibiotic-resistant Salmonella from retail ground meats. N. Engl. J. Med., 345(16): 1147-1154. [Crossref] [PubMed]
10. Aarestrup, F.M., Wegener, H.C. and Collignon, P. (2008) Resistance in bacteria of the food chain: Epidemiology and control strategies. Expert Rev. Anti. Infect. Ther., 6(5): 733-750. [Crossref] [PubMed]
11. Khanna, T., Friendship, R., Dewey, C. and Weese, J.S. (2008) Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet. Microbiol., 128: 298-303. [Crossref] [PubMed]
12. Smith, T.C. and Pearson, N. (2011) The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis., 11: 327-339. [Crossref] [PubMed]
13. Morosini, M.I., Garcia-Castillo, M., Coque, T.M., Valverde, A., Novais, A., Loza, E. and Canton, R., (2006) Antibiotic coresistance in extended-spectrum-beta lactamase-producing Enterobacteriaceae and in vitro activity of tigecycline. Antimicrob. Agents Chemother., 50: e2695-e2699. [Crossref] [PubMed] [PMC]
14. El-Jakee, J.K., Nagwa, S.A., Samy, A.A., Bakry, M.A., Elgabry, E.A., Mai, M.K. and Gad El-Said, W.A. (2011) Antimicrobial resistance in clinical isolates of Staphylococcus aureus from bovine and human sources in Egypt. Glob. Vet., 7: 581-586.
15. Quinn, P.J., Markey, B.K., Carter, M.E., Donnelly, W.J.C., Leonard, F.C. and Maguire, D. (2002) Veterinary Microbiology and Microbial Diseases. 1st ed. Published Blackwell Science, Ames.
16. Finegold, S.M. and Martin, W.J. (1982) Baileys and Scotts Diagnostic Microbiology. 6th ed. The C.V. Mosby Company, St. Louis, Toronto, London.
17. Koneman, E., Allen, S.D., Janda, W.M., Schreckenberger, P.C. and Winn, W.C. (1997) Color Atlas and Textbook of Diagnostic Microbiology. 5th ed. Lippincott, Philadelphia, PA, New York.
18. Clinical and Laboratory Standards Institute, CLSI. (2013) Approved Standards: Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard. 11th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
19. Sambrook, X., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloninga Laboratory Manual. 2nd ed. Cold Spring Harbor, New York, Laboratory Press.
20. Duran, N., Ozer, B., Duran, G.G., Onlen, Y. and Demir, C. (2012) Antibiotic resistance genes and susceptibility patterns in staphylococci. Indian J. Med. Res., 135(3): 389-396. [PubMed] [PMC]
21. Schlegelova, J., Vlkova, H., Babak, V., Holasova, M., Jaglic, Z., Stosova, T. and Sauer, P. (2008) Resistance to erythromycin of Staphylococcus spp. Isolates from the food chain. Vet. Med., 53: 307-314.
22. Hill, W.E. (1996) The polymerase chain reaction: Applications for the detection of foodborne pathogens. Crit. Rev. Food Sci. Nutr., 36(1-2): 123-121. [Crossref] [PubMed]
23. Hassanien, F.S. (2004) Bacterial hazards associated with consumption of some meat products. Benha Vet. Med. J., 15: 41-54.
24. El-Jakee, J., Ata-Nagwa, S., Bakry, M., Zouelfakar, S.A., Elgabry, E. and Gad El-Said, W.A. (2008) Characteristics of Staphylococcus aureus strains isolated from human and animal sources. Am. Eur. J. Agric. Environ. Sci., 4(2): 221-229.
25. El-Jakee, J., Marouf, S.A., Ata, S.N., Abdel-Rahman, H.E., Abd-Elmoez, S., Samy, A.A., El-Sayed, E. and Walaa, E. (2013) Rapid method for detection of Staphylococcus aureus enterotoxins in food. Glob. Vet., 11(3): 335-341.
26. Jamali, H., Paydar, M., Radmehr, B., Ismail, S. and Dadrasnia, A. (2015) Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control. J., 54: 383-388. [Crossref]
27. Imani, F.A.A., Tavakoli, H.R. and Naderi, A. (2010) Detection of enterotoxigenic S. aureus isolates in domestic dairy products. Iran. J. Microbiol., 2(3): 135-144.
28. Song, M., Bai, Y., Xu, J., Qiu, C.M., Shi, C. and Shi, X. (2014) Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai. Int. J. Food Microbiol., 195: 1-8. [Crossref] [PubMed]
29. Gwida, M.M. and El-Gohary, F.A. (2013) Zoonotic bacterial pathogens isolated from raw milk with special reference to Escherichia coli and Staphylococcus aureus in Dakahlia governorate, Egypt. Open Access Sci. Rep., 2(4): 705-708.
30. Hosny, I.M., El-Kholy, W.I., Murad, H.A. and El-Dairouty, R.K. (2011) Antimicrobial activity of curcumin upon pathogenic microorganisms during manufacture and storage of a novel style cheese "Karishcum". J. Am. Sci., 7(5): 611-618.
31. El-Sayed, M.A., Hosny, I.M., El-Kholy, W.I., El-Dairouty, R.K. and Mohamed, S.H.S. (2011) Microbiological evaluation of Egyptian white soft cheeses style. J. Am. Sci., 7(5): 517-526.
32. Fox, A., Pichon, B., Wilkinson, H., Doumith, M., Hill, R.L., McLauchlin, J. and Kearns, A.M. (2017) Detection and molecular characterization of livestock-associated MRSA in raw meat on retail sale in North West England. Lett. Appl. Microbiol., 64(3): 239-245. [Crossref] [PubMed]
33. Pesavento, G., Ducci, B., Comodo, N. and Lo Nostro, A. (2007) Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control., 18: 196-200. [Crossref]
34. Ge, B., Mukherjee, S., Hsu, C.H., Davis, J.A., Tran, T.T., Yang, Q., Abbott, J.W., Ayers, S.L., Young, S.R., Crarey, E.T., Womack, N.A., Zhao, S. and McDermott, P.F. (2017) MRSA and multidrug-resistant Staphylococcus aureus in U.S. Retail meats 2010-2011. Food Microbiol., 62: 289-297. [Crossref] [PubMed]
35. Ali, N.H., Farooqui, A., Khan, A., Khan, A.Y. and Kazmi, S.U. (2010) Microbial contamination of raw meat and its environment in retail shops in Karachi, Pakistan. J. Infect. Dev. Ctries., 4: 382-388.
36. Hassanin, Z.H. (2007) Studies on Food Poisoning Microorganisms in Some Meat Products. M. V. Sc. Thesis, Faculty of Veterinary Medicine, Menoufia University, Sadat Branch.
37. Abdaslam, S.A., Hassan, M.A., Kaheel, H.H., Abobaker, T.M., Alnourain, T.H., Hamdan, H.A., Shankar, S.G. and Thambirajah, J.J. (2014) Isolation of Escherichia coli O157 and other food borne pathogens from meat products and their susceptibility to different antimicrobial agents. Curr. Res. Microbiol. Biotechnol., 2(3): 391-397.
38. Li, G., Wu, C., Wang, X. and Meng, J. (2015) Prevalence and characterization of methicillin susceptible Staphylococcus aureus ST398 isolates from retail foods. Int. J. Food Microbiol., 196: 94-97. [Crossref] [PubMed]
39. 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: 169-174. [Crossref] [PubMed]
40. Gundogan, N., Citak, S. and Turan, E. (2006) Slime production, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurized milk and ice cream samples. Food Control. J., 17(5): 389-392. [Crossref]
41. Al-Zu'Bi, E., Bdour, S. and Shehabi, A.A. (2004) Antibiotic resistance patterns of mecA positive Staphylococcus aureus isolates from clinical specimens and nasal carriage. Microb. Drug Resist. Mech. Epidemiol. Dis., 10(4): 321-324. [Crossref] [PubMed]
42. Ammar, A.M., Attia, A.M., Abd El-Hamid, M.I., El-Shorbagy, I.M. and Abd El-Kader, S.A. (2016) Genetic basis of resistance waves among methicillin resistant Staphylococcus aureus isolates recovered from milk and meat products in Egypt. Cell. Mol. Biol. Noisy-le-Grand, 62(10): 7-15. [PubMed]
43. Zhang, L., Li, Y., Bao, H., Wei, R., Zhou, Y., Zhang, H. and Wang, R. (2016) Population structure and antimicrobial profile of Staphylococcus aureus strains associated with bovine mastitis in China. Microb. Pathog., 97: 103-109. [Crossref] [PubMed]
44. Haran, K., Godden, S., Boxrud, D., Jawahir, S., Bender, J. and Sreevatsan, S. (2012) Prevalence and characterization of Staphylococcus aureus, including methicillin resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. J. Clin. Microbiol., 50(3): 688-695. [Crossref] [PubMed] [PMC]
45. Waters, A.E., Cuomo, T.C., Buchhagen, J., Liu, C.M., Watson, L., Pearce, K., Foster, J.T., Bowers, J., Driebe, E.M., Engelthaler, D.M., Keim, P.S. and Price, L.B. (2011) Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin. Infect. Dis. J., 52: 1227-1230. [Crossref] [PubMed] [PMC]
46. Argudin, M.A., Mendoza, M.C., Gonzalez-Hevia, M.A., Bances, M., Guerra, B. and Rodicioa, M.R. (2012) Genotypes, exotoxin gene content, and antimicrobial resistance of Staphylococcus aureus strains recovered from foods and food handlers. Appl. Environ. Microbiol., 78(8): 2930-2935. [Crossref] [PubMed] [PMC]
47. Tan, S.L., Lee, H.Y. and Mahyudin, N.A. (2014) Antimicrobial resistance of Escherichia coli and Staphylococcus aureus isolated from food handler's hands. Food Control. J., 44: 203-207. [Crossref]
48. Teramoto, H., Salaheen, S. and 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. [Crossref]
49. Millan, L.L., Gonicepero, M.P., Ruiz, J., Zolezzi, P.C., Rubio, C.M.C. and Canales, E.M. (2007) Molecular typing of Staphylococcus aureus clinical isolates by pulsed-field gel electrophoresis, staphylococcal cassette chromosome MEC type determination and dissemination of antibiotic resistance genes. Int. J. Antimicrob. Agents, 30(6): 505-513. [Crossref] [PubMed]
50. Kumar, R., Yadav, B.R. and Singh, R.S. (2010) Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of Mastitic crossbred cattle. Curr. Microbiol., 60(5): 379-386. [Crossref] [PubMed]
51. McCallum, N., Berger-Bachi, B. and Senn, M.M. (2010) Regulation of antibiotic resistance in Staphylococcus aureus. Int. J. Med. Microbiol., 300: 118-129. [Crossref] [PubMed]
52. Gao, J., Ferreri, M., Yu, F., Liu, Xi., Chen, L., Su, J. and Han, B. (2012) Molecular types and antibiotic resistance of Staphylococcus aureus isolates from bovine mastitis in a single herd in China. Vet. J., 192: 550-552. [Crossref] [PubMed]
53. Martineau, F., Picard, F.J., Lansac, N., MeNard, C., Roy, P.H., Ouellette, M. and Bergeron, M.G. (2010) Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob. Agents Chemother., 44(2): 231-238. [Crossref]