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              Open Access  
Copyright: The authors. This article is an open access 
article licensed under the terms of the Creative Commons Attribution License 
 
 
(http://creativecommons.org/licenses/by/2.0) which permits unrestricted use, 
distribution and reproduction in any medium, provided the work is properly 
cited. 
 
              
              
              Research 
              
              
(Published online: 
              26-07-2015) 
              16.  
              
              Prevalence, molecular characterization of 
              Staphylococcus aureus isolated from cheese and in vitro 
              antibacterial activity of silver nanoparticles against such 
              strains - 
              Karima G. Abdel Hameed 
              and Mona A. El-Zamkan 
              
              Veterinary World, 8(7): 908-912   
              
   
                
                
doi: 
              10.14202/vetworld.2015.908-912   Karima 
              G. Abdel Hameed: 
              
              Department of Food Hygiene and Control, Faculty of Veterinary 
              Medicine, South Valley University, Qena, Egypt;
              
              
              karima_galal2004@yahoo.com Mona A. 
              El-Zamkan: Department of Food Hygiene and Control, Faculty of 
              Veterinary Medicine, South Valley University, Qena, Egypt;
              
              Moon_zam@outlook.sa   Received: 
              08-05-2015, Revised: 18-06-2015, Accepted: 26-06-2015, Published 
              online: 26-07-2015   
              
              
              Corresponding author:Karima G. Abdel Hameed, e-mail: karima_galal2004@yahoo.com 
 
              Citation:Abdel Hameed KG, El-Zamkan 
              MA (2015) Prevalence, molecular characterization of 
              Staphylococcus aureus isolated from cheese and in vitro 
              antibacterial activity of silver nanoparticles against such 
              strains, Veterinary World 8(7):908-912. 
 
              Abstract 
 Aim:
              The aim was to investigate cheese samples for the prevalence 
              of Staphylococcus aureus, evaluate multiplex polymerase 
              chain reaction (PCR) methods for S. aureus identification, 
              as well as to determine the antibacterial activity of silver 
              nanoparticles against such strains. 
              Materials and Methods: Total of 100 random locally 
              manufactured cheese samples were collected from Qena dairy 
              markets, Egypt, and examined conventionally for the prevalence of
              S. aureus then, confirmation of these isolates were done 
              using multiplex PCR. The antibacterial activity of silver 
              nanoparticles against such isolates was also checked. 
              Results: Lower prevalence of S. aureus in Damietta 
              cheese (54%) than in Kareish cheese (62%) was recorded. As well 
              lower frequency distribution for both S. aureus (36%) and 
              CNS (8%) was also reported for Damietta cheese. Using of multiplex 
              PCR method for S. aureus identification have been confirmed 
              all 58 S. aureus stains that were identified conventionally 
              by detection of two PCR products on agarose gel: The 791 bp and 
              the 638 bp. The correlation coefficient between conventional and 
              multiplex PCR method was 0.91 and was significant at p≤0.001. 
              Regarding antibacterial activity of silver nanoparticles using 
              disk diffusion method on Baird Parker agar it was found that 
              inhibition zone of silver nanoparticles against S. aureus, 
              was 19.2±0.91 mm and it was higher than that produced by 
              gentamicin (400 units/ml) 15.2±0.89 mm. 
              Conclusions: The present study illustrated the higher 
              prevalence of S. aureus in cheese samples that may 
              constitute a public health hazard to consumers. According to the 
              results, it can be concluded that silver nanoparticles can be used 
              as an effective antibacterial against S. aureus. Thereby, 
              there is a need for an appropriate study for using silver 
              nanoparticles in cleaning and disinfection of equipment and in 
              food packaging. 
              Keywords: antibacterial activity, multiplex 
              polymerase chain reaction, Staphylococcus aureus, silver 
              nanoparticles. 
 
              References 
 
                
                  | 1. EL-Kholy, A.M., EL-Shinawy, S.H., Meshref, A.M. and Korany, 
                  A.M. (2014) Microbiological quality of domiati cheese and the 
                  influence of probiotics on the behavior of Staphylococcus 
                  aureus and Eescherichia coli O157: H7 in domiati cheese. J. 
                  Food Safety, 34(4): 396-406. http://dx.doi.org/10.1111/jfs.12157
 |  
                  |  |  
                  | 2. Mohammed, A.S. (2010) Sanitary evaluation of some dairy 
                  products in qena markets, M.V.Sc. Thesis, Faculty of 
                  Veterinary Medicine South Valley University. |  
                  |  |  
                  | 3. Yan, X., Wang, B., Tao, X., Hu, Q., Cui, Z., Zhang, J., 
                  Lin, Y., You, Y., Shi, X. and Hajo G. (2012) Characterization 
                  of Staphylococcus aureus strains associated with food 
                  poisoning in shenzhen, China. Appl. Environ. Microb., 78(18): 
                  6637-6642. http://dx.doi.org/10.1128/AEM.01165-12
 PMid:22798367 PMCid:PMC3426705
 |  
                  |  |  
                  | 4. William, J.M., Jon, S.B., Karen, B., Noroyono, W., Neelum, 
                  O. and Mark, S.S. (2001) Multiplex PCR protocol for the 
                  diagnosis of Staphylococcal infection. J. Clin. Microbiol., 
                  39(9): 3332-3338. http://dx.doi.org/10.1128/JCM.39.9.3332-3338.2001
 PMCid:PMC88340
 |  
                  |  |  
                  | 5. Yeo, S.Y., Lee, H.J. and Jeong, S.H. (2003) Preparation of 
                  nanocomposite fibers for permanent antibacterial effect. J. 
                  Mater. Sci., 38: 2143-2147. http://dx.doi.org/10.1023/A:1023767828656
 |  
                  |  |  
                  | 6. Azlin-Hasim, S., Cruz-Romero, M.C., Ghoshal, T., Morris, 
                  M.A., Cummins, E. and Kerry, J.P. (2014) Application of silver 
                  nanodots for potential use in antimicrobial packaging 
                  applications. Innov. Food Sci. Emerg., 27: 136-143. http://dx.doi.org/10.1016/j.ifset.2014.10.012
 |  
                  |  |  
                  | 7. Finegold, S.H. and Martin, W.J. (1982) Diagnostic 
                  Microbiology, Bailly and Scott. 6th ed. Mosby Co., St., Louis, 
                  Toronto, London. |  
                  |  |  
                  | 8. Bennett, R.W. and Lancette, G.A. (1995) Staphyloccus 
                  aureus. In: Food and Drug Administration Bacteriological 
                  Analytical Manual. 8th ed., Ch. 12. AOAC International, 
                  Gaithersburg, MD. p12.01-12.05. |  
                  |  |  
                  | 9. Hameid, A.K.G., Sender, G., Prusak, B., Ryniewicz, Z. 
                  (2004) Multiplex PCR protocol for the diagnosis of 
                  Staphylococcus aureus udder infections of Polish Black and 
                  White cows. Anim. Sci. Pap. Rep., 22(4): 679-685. |  
                  |  |  
                  | 10. Lee, K.J., Park, S.H., Govarthanan, M., Hwang, P., Seo, 
                  Y.S., Cho, M., Lee, W.H., Lee, J.Y., Kannan, S.K. and Oh, B.T. 
                  (2013) Synthesis of silver nanoparticles broad using cow milk 
                  and their antifungal activity against phytopathogens. Mater. 
                  Lett., 105: 128-131. http://dx.doi.org/10.1016/j.matlet.2013.04.076
 |  
                  |  |  
                  | 11. Clinical and Laboratory Standards Institute (CLSI). (2002) 
                  Performance Standards for Antimicrobial Disk and Dilution 
                  Susceptibility Tests for Bacterial Isolated from Animals; 
                  Approved Standard, M31-A2. 4th ed. CLSI, Wayne, PA. |  
                  |  |  
                  | 12. Cheruiyot, K.R., Olila, D. and Katerega, J. (2009) 
                  In-vitro antibacterial activity of selected medicinal plants 
                  from Longisa region of Bomet District, Kenya. Afr. Health 
                  Sci., 9: S42-S46. PMid:20589160 PMCid:PMC2890996
 |  
                  |  |  
                  | 13. Frazier, W.C. and Westhoff, D.C. (1988) Food Microbiology. 
                  4th ed. Mc-Graw Hill Publ. Co. Ltd., New York. |  
                  |  |  
                  | 14. Saad, A.M. (2010) Study on microorganisms of public health 
                  hazards in locally manufactured cheese at Aswan city. M.V.Sc. 
                  Thesis, Faculty of Veterinary Medicine South Valley 
                  University. |  
                  |  |  
                  | 15. Jay, A.M. (1996) Modern Food Microbiology. 5th ed. Chapman 
                  and Hall Inc., New York, USA. http://dx.doi.org/10.1007/978-1-4615-7473-6
 |  
                  |  |  
                  | 16. Mcdevitt, D., Francois, P., Vaudaux, P. and Foster, T.J. 
                  (1994) Molecular characterisation of the clumping factor 
                  (fibrinogen receptor) of Staphylococcus aureus. Mol. 
                  Microbiol., 11(2): 237-248. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00304.x
 |  
                  |  |  
                  | 17. Smeltzer, M.S., Gillaspy, A.F., Pratt, F.L., Thames, M.D. 
                  and Landolo, J.J. (1997) Prevalence and chromosomal map 
                  location of Staphylococcus aureus adhesion genes. J. Genet., 
                  196: 249-259. |  
                  |  |  
                  | 18. Stutz, K., Stephan, R. and Tasara, T. (2011) SpA, ClfA, 
                  and FnbA genetic variations lead to Staphaurex test-negative 
                  phenotypes in bovine mastitis Staphylococcus aureus isolates. 
                  J Clin Microbiol., 49(2): 638-646. http://dx.doi.org/10.1128/JCM.01148-10
 PMid:21147952 PMCid:PMC3043514
 |  
                  |  |  
                  | 19. Kelvin, K., Vincent, C., Jasper, F., Amy, C., Sandy, C., 
                  Flora, H., Shirly, O., Susanna, K., Kwok, Y. and Patrick, Y. 
                  (2011) Molecular characterization of a catalase - Negative 
                  Staphylococcus aureus subsp. aureus strain collected from a 
                  patient with mitral valve endocarditis and pericarditis 
                  revealed a novel nonsense mutation in the kat Agene. J. Clin. 
                  Microbiol., 49(9): 3398-3402. http://dx.doi.org/10.1128/JCM.00849-11
 PMid:21715584 PMCid:PMC3165592
 |  
                  |  |  
                  | 20. Da Silva, E.R., Sigueira, A.P., Martins, J.C.D., Ferreria, 
                  W.P.B. and Silva, N. (2005) Hemolysin production by 
                  Staphylococcus aureus species isolated from mastitic goat milk 
                  in Brazilian dairy herds. Small Rumin. Res., 56: 271-275. http://dx.doi.org/10.1016/j.smallrumres.2004.04.011
 |  
                  |  |  
                  | 21. Shrivastava, S., Bera, T., Roy, A., Singh, G., 
                  Ramachandrarao, P. and Dash, D. (2007) Characterization of 
                  enhanced antibacterial effects of novel silver nanoparticles. 
                  Nanotechnology, 18: 225103, 1-6. http://dx.doi.org/10.1088/0957-4484/18/22/225103
 |  
                  |  |  
                  | 22. Hameed, A.K.G. and El-Malt, M.L. (2009) Public health 
                  hazard of Staphylococcus aureus isolated from raw milk and ice 
                  cream in Qena governorate. Assiut Vet. Med. J., 55(121): 
                  191-200. |  
                  |  |  
                  | 23. Dehkordi, S.H., Fatemeh, H. and Azizollah, E.K. (2011) An 
                  in vitro evaluation of antibacterial effect of silver 
                  nanoparticles on Staphylococcus aureus isolated from bovine 
                  subclinical mastitis, Afr. J. Biotechnol., 10(52): 
                  10795-10797. |  
                  |  |  
                  | 24. Kazemi, J., Malahat, A., Habib, D., Saei, M. and Adib, H. 
                  (2014) Antibacterial effect of silver nanoparticles along with 
                  protein synthesis-inhibiting antibiotics on Staphylococcus 
                  aureus isolated from cattle mastitis. Biol. J. Micro., 8: 
                  15-22. |  
                  |  |  
                  | 25. Seil, J.T. and Webster, T.J. (2012) Antimicrobial 
                  applications of nanotechnology: Methods and literature. Int. 
                  J. Nanomed., 7: 2767-2781. PMid:22745541 PMCid:PMC3383293
 |  
                  |  |  
                  | 26. Appendini, P. and Hotchkiss, J.H. (2002) Review of 
                  antimicrobial food packaging. Innov. Food Sci. Emerg., 3: 
                  113-126. http://dx.doi.org/10.1016/S1466-8564(02)00012-7
 |  
                  |  |  
                  | 27. Zarei, M., Jamnejad, A. and Khajehali, E. (2014) 
                  Antibacterial effect of silver nanoparticles against four 
                  foodborne pathogens. Jundishapur J. Microbiol., 7(1): 8720. http://dx.doi.org/10.5812/jjm.8720
 |  |