Contamination rate, antibiotic susceptibility profile, biofilm formation and presence of TSST-1 gene in Staphylococcus aureus isolates
Subject Areas : Food Science and TechnologyK. Ebrahimzadeh 1 , S. Hanifian 2
1 - M.Sc Graduate in Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran
2 - Assistant Professor of Department of Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran
Biotechnology Research Center, Tabriz Branch, Islamic Azad University, Tabriz, Iran
Keywords: Biofilm, Staphylococcus aureus, Antibiotic resistance, traditional Dairy products, TSST-1 gene,
Abstract :
This study aimed to investigate the prevalence of Staphylococcus aureus in raw milk and traditional dairy products of West-Azerbaijan Province and also to evaluate the presence of TSST-1 virulence gene, antibiotic resistance and biofilm formation of the isolates. Using stratified random method, a total of 80 raw milk and traditional dairy products (including traditional cheese, cream and curd) together with 20 nasal swab samples of the dairy products’ manufacturers were collected. S. aureus strains were isolated and identified by conventional culture methods. Afterwards, the isolates were subjected to PCR analysis to detect the presence of TSST-1 gene. According to the findings, 35% of the samples were contaminated by S. aureus. Moreover TSST-1 gene was recognized in 1 cheese and 2 swab samples. Antibiotic resistance profile revealed that most of S. aureus isolates were resistant towards vancomycin, penicillin, and methicillin and sensitive towards co-trimoxazole, gentamicin, rifampin, oxacillin, and cephalothin. Moreover, 2.85%, 17.15%, and 80% of the isolates were capable to form high, moderate and low amounts of biofilm. High occurrence of S. aureus in milk and dairy products which harbor TSST-1 virulence gene, and the strains that demonstrated resistant to several antibiotics and capable of biofilm formation, could be considered a health threat to the consumers of these products.
● Appelbaum, P.C. (2007). Microbiology of antibiotic resistance in Staphylococcus aureus. Clinical Infectious Diseases, 45: 165–170.
● Archer, N.K., Mazaitis, M.J., Costerton, J.W., Leid, J.G., Powers, M.E. and Shirtliff, M.E. (2011). Staphylococcus aureus biofilms, properties, regulation and roles in human disease. Virulence, 2(5), 445–459.
● Barrow, G.I. and Feltham, R.K.A. (2003). Cowan and Steel’s Manual for the Identification of Medical Bacteria. 3rd Edition. Cambridge University Press. pp. 54–57.
● Bennett, R.W. and Monday, S.R. (2003). Staphylococcus aureus. In: Miliotis, M.D. and Bier, J.W. (Editors), International Handbook of Foodborne Pathogens. Marcel Dekker, Inc. pp. 41–59.
● Dastmalchi, H., Ahmadi, M., Mardani, K. and Batavani, R.A. (2009). Molecular typing of Staphylococcus aureus isolated form bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Veterinary Microbiology, 137: 202–206.
● Djordjevic, D., Wiedmann, M. and McLandsborough, L.A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6): 2950–2958.
● Duran, N., Ozer, B., Gulbol Duran, G., Onlen, Y. and Demir, C. (2012). Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian Journal of Medical Research, 135: 389–396.
● El-Ghodban. A., Ghenghesh, K.S., Marialigeti, K., Esahli, H. and Tawil, A. (2006). PCR detection of toxic shock syndrome toxin of Staphylococcus aureus from Tripoli, Libya. Journal of Medical Microbiology, 55(2): 179–182.
● Ertas, N., Gonulalan, Z., Yildirim, Y. and Kum, E. (2010). Detection of Staphylococcus aureus Enterotoxins in Sheep Cheese and Dairy Desserts by Multiplex PCR Technique. International Journal Food Microbiology, 142(1-2): 74–77.
● Eshraghi, S., Salehipour, Z., Pourmand, M.R., Rahimi Forushani, A., Zahraei Salehi, M.T., Agha Amiri, S., et al. (2009). Prevalence of tst, entC, entA and entA/C genes in Staphylococcus aureus strains isolated from different foods. Tehran University Medical Journal, 67(7): 470–476 [In Persian].
● Farahmand-Azar, S., Ahmadi, M., Dastmalchi Saei, H. and Anassori, E. (2013). Identification of Toxic Shock Syndrome Toxin-1 (TSST-1) gene in Staphylococcus aureus isolated from bovine mastitis milk. Archives of Razi Institute, 68(1): 17–22.
● Fueyo, J.M., Mendoza, M.C., Rodicio, M.R., Muniz, J., Alvarez, M.A. and Martin, M.C. (2005). Cytotoxin and pyrogenic toxin superantigen gene profiles of Staphylococcus aureus associated with subclinical mastitis in dairy cow and relationships with macrorestriction genomic profiles. Journal of Clinical Microbiology, 43(3): 1278–1284.
● Hoerlle, J.L. and Brandelli, A. (2009). Antimicrobial resistance of Staphylococcus aureus isolated from the intensive care unit of a general hospital in southern Brazil. The Journal of Infection in Developing Countries, 3(7): 504–510.
● Imani-Fooladi, A.A., Riazipour, M. and Sattari, M. (2010). Molecular and serological detection of Enterotoxigenic Staphylococcus aureus from traditionally dairy products. Journal of Shahrekord University of Medical Sciences, 11(4): 19–26 [In Persian].
● Khakpoor, M., Ezzati, M., Mahmoodi, K., Khalaji Pirbaluti, M., Khaksar, R. (2013). Prevalence of coagulase-positive Staphylococcus aureus in local cheese in West Azerbaijan with culture and PCR method. Iranian Journal of Nutrition Sciences & Food Technology, 7(5): 237–242.
● Khalifezadeh, S., Sadeghi Zali, M.H. and Nahaee, M.R. (2015). Prevalence and antibiotics susceptibility of Staphylococcus aureus in traditional Kouzeh cheese at Saqqez retails. Journal of Food Hygiene, 4(16), 1–10 [In Persian].
● Khoramian, B., Emaneini, M.E., Bolourchi, M., Eslampour, M.A., Niasari-Naslaji, A., Aligholi, M. et al., (2009). Evaluation of the biofilm-forming ability of Staphylococcus aureus isolates from bovine mastitis in Iran. Journal of Comparative Pathobiology, 6(4), 109-114.
● Lancette, G.A. and Bennet, R.W. (2001). Staphylococcus aureus and Staphylococcal Enterotoxins, In: Pouch Downes, F., Ito, K. (Editors), Compendium of methods for the microbiological examination of foods, 3rd edition, American Public Health Association, Washington DC. pp. 387–400.
● Lindqvist, R., Sylvén, S. and Vågsholm, I. (2002). Quantitative microbial risk assessment exemplified by Staphylococcus aureus in unripened cheese made from raw milk. International Journal of Food Microbiology, 78: 155–170.
● Mehrotra, M., Wang, G. and Johnson, W.M. (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(3): 1032–1035.
● Mirzaei, H., Javadi, A., Farajli, M., Shah-Mohammadi, A.R., Monadi, A.R. and Barzegar, A. (2012). Prevalence of Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city of Tabriz, Iran. Journal of Veterinary Research, 67(1): 65–70 [In Persian].
● Molla Abbaszadeh, H., Mobaiyen, H. and Mirzaei, H. (2011). Determination of prevalence rate and antibiotic resistance pattern in Staphylococcus aureus strains isolated from in-patients of Imam Reza and Shohada hospitals, Tabriz. Journal of Microbial Biotechnology, 3(9): 45–50 [In Persian].
● Molla Abaszadeh, H. and Haji Sheikhzadeh, B. (2014). Surveying the contamination rate, sensibility and antimicrobial resistance patterns in Staphylococcus aureus isolated from traditional cheese consumed in Qotur of Khoy province. Journal of Fasa University of Medical Science, 4(2): 209–217 [In Persian].
● Moroni, P., Pisoni G., Cremonesi, P. and Castiglioni, B. (2010). Staphylococcus. In: Liu, D. (Editor), Molecular Detection of Foodborne Pathogens. CRC Press, New York, pp. 245–246.
● Nagao, M., Okamoto, A., Yamada, K., Hasegawa, T., Hasegawa, Y. and Ohta, M. (2009). Variations in amount of TSST-1 produced by clinical methicillin resistant Staphylococcus aureus (MRSA) isolates and allelic variation in accessory gene regulator (agr) locus. BMC Microbiology, 9: 52.
● Norouzi, J, Goudarzi, G., Pakzad, P. and Razavipour, R. (2012). The Isolation and detection of Staphylococcus aureus enterotoxins A-E and TSST-1 genes from different sources by PCR Method. Qom University of Medical Sciences Journal, 6(3): 78–85.
● Parsonnet, J., Goering, R.V., Hansmann, M.A., Jones, M.B., Ohtagaki, K., Davis, C.C. and Totsuka, K. (2008). Prevalence of toxic shock syndrome toxin 1 (tsst-1)-producing strains of Staphylococcus aureus and antibody to tsst-1 among healthy Japanese women. Journal of Clinical Microbiology, 46(8): 2731–2738.
● Periasamy, S., Joo, H.S., Duong, A.C., Bach, T.H.L., Tan, V.Y., Chatterjee, S.S. and et al. (2011). How Staphylococcus aureus biofilms develop their characteristic structure. Proceedings of the National Academy of Sciences, 109: 1281–1286.
● Pourshafie, N., Shayegh, J. and Mobayen, H. (2015). Identification of toxic shock syndrome toxin-1 genes of Staphylococcus aureus isolated from local cheese and cow’s milk in Tabriz city. Journal of Food Microbiology, 2(6): 81–87.
● Quinn, P.J., Carter, M.E. and Barkey, B. (1994). Veterinary Microbiology, Elsevier, p. 118.
● Rahimi, F., Katouli, M. and Pourshafie, M.R. (2014). Characteristics of hospital-and community-acquired meticillin-resistant Staphylococcus aureus in Tehran, Iran. Journal of Medical Microbiology, 63(6): 796–804.
● Rahimi, F. (2015). Biofilm production among Staphylococcus aureus strains isolated from healthy people. Iranian Journal of Infectious Diseases, 68, 21–29 [In Persian].
● Rahimi, F., Bouzari, M., Katouli, M. and Pourshafie, M.R. (2013). Antibiotic resistance pattern of methicillin resistant and methicillin sensitive Staphylococcus aureus isolates in Tehran, Iran. Jundishapur Journal of Microbiology, 6(2): 144–149.
● Rahimi, E. and Alian, F. (2013). Presence of enterotoxigenic Staphylococcus aureus in cow, camel, sheep, goat and buffalo bulk tank milk. Veterinarski Arhiv, 83(1): 23–30.
● Rahimi, F., Bouzari, M., Vandyousefi, J., Maleki, Z., Saberi kashani, S. and Davoudi, S. (2008). Analysis of antibiotic resistance and detection of mecA gene in Staphylococcus aureus isolated from hospitals and medical laboratories in Tehran. Iranian Biological Journal, 21: 64–74.
● Schweizer, M.L., Perencevich, E.N., Eber, M.R., Cai, X., Shardell, M.D., Braykov, N. and Laxminarayan, R. (2013). Optimizing antimicrobial prescribing: Are clinicians following national trends in methicillin-resistant staphylococcus aureus (MRSA) infections rather than local data when treating MRSA wound infections. Antimicrobial Resistance and Infection Control, 2: 28.
● Scherrer, D., Corti, S., Muehlherr, J.E., Zweifel, C. and Stephan, R. (2004). Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep.Veterinary Micriobiology, 101: 101–107.
● Secor, P.R., James, G.A., Fleckman, P., Olerud, J.E, McInnerney, K. and Stewart, P.S. (2011). Staphylococcus aureus biofilm and planktonic cultures differentially impact gene expression, mapk phosphorylation, and cytokine production in human keratinocytes. BMC Microbiology, 11: 143.
● Singh, P. and Prakash A. (2010). Prevalance of coagulase positive pathogenic Staphylococcus aureus in milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta Agriculturae Slovenica, 96(1): 37–41.
● Srey, S., Jahid, I.K. and Ha, S.D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31: 572–585.
● Stepanović, S., Vuković, D., Dakić, I., Savić, B. and Švabić-Vlahović, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40: 175–179.
● Teyhoo, M., Mobin, H., Mozafari, N.A., Moadab, S.R., Sedigh Bayan, K.H. and Mones Rast, S.H. (2011). The prevalence of toxic shock syndrome toxin (TSST-1) producing clinical isolates of Staphylococcus aureus strains isolated from Shohada hospital in Tabriz, Iran. Medical Laboratory Journal, 5(1): 38–44 [In Persian].
● Udobi, C.E., Obajuluwa, A.F. and Onaolapo J.A. (2013). Prevalence and antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus from an orthopaedic hospital in Nigeria. BioMed Research International, 860467, 4 pages.
● Wikler, M.A., Cockeril, F.R., Craig, W.A., Dudley, M.N., Eliopoulos, G.M., Hecht, D.W. and et al. (2007). Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Information Supplement. Clinical and Laboratory Standards Institute (CLSI), 27(1): 44–51.
_||_● Appelbaum, P.C. (2007). Microbiology of antibiotic resistance in Staphylococcus aureus. Clinical Infectious Diseases, 45: 165–170.
● Archer, N.K., Mazaitis, M.J., Costerton, J.W., Leid, J.G., Powers, M.E. and Shirtliff, M.E. (2011). Staphylococcus aureus biofilms, properties, regulation and roles in human disease. Virulence, 2(5), 445–459.
● Barrow, G.I. and Feltham, R.K.A. (2003). Cowan and Steel’s Manual for the Identification of Medical Bacteria. 3rd Edition. Cambridge University Press. pp. 54–57.
● Bennett, R.W. and Monday, S.R. (2003). Staphylococcus aureus. In: Miliotis, M.D. and Bier, J.W. (Editors), International Handbook of Foodborne Pathogens. Marcel Dekker, Inc. pp. 41–59.
● Dastmalchi, H., Ahmadi, M., Mardani, K. and Batavani, R.A. (2009). Molecular typing of Staphylococcus aureus isolated form bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Veterinary Microbiology, 137: 202–206.
● Djordjevic, D., Wiedmann, M. and McLandsborough, L.A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6): 2950–2958.
● Duran, N., Ozer, B., Gulbol Duran, G., Onlen, Y. and Demir, C. (2012). Antibiotic resistance genes & susceptibility patterns in staphylococci. Indian Journal of Medical Research, 135: 389–396.
● El-Ghodban. A., Ghenghesh, K.S., Marialigeti, K., Esahli, H. and Tawil, A. (2006). PCR detection of toxic shock syndrome toxin of Staphylococcus aureus from Tripoli, Libya. Journal of Medical Microbiology, 55(2): 179–182.
● Ertas, N., Gonulalan, Z., Yildirim, Y. and Kum, E. (2010). Detection of Staphylococcus aureus Enterotoxins in Sheep Cheese and Dairy Desserts by Multiplex PCR Technique. International Journal Food Microbiology, 142(1-2): 74–77.
● Eshraghi, S., Salehipour, Z., Pourmand, M.R., Rahimi Forushani, A., Zahraei Salehi, M.T., Agha Amiri, S., et al. (2009). Prevalence of tst, entC, entA and entA/C genes in Staphylococcus aureus strains isolated from different foods. Tehran University Medical Journal, 67(7): 470–476 [In Persian].
● Farahmand-Azar, S., Ahmadi, M., Dastmalchi Saei, H. and Anassori, E. (2013). Identification of Toxic Shock Syndrome Toxin-1 (TSST-1) gene in Staphylococcus aureus isolated from bovine mastitis milk. Archives of Razi Institute, 68(1): 17–22.
● Fueyo, J.M., Mendoza, M.C., Rodicio, M.R., Muniz, J., Alvarez, M.A. and Martin, M.C. (2005). Cytotoxin and pyrogenic toxin superantigen gene profiles of Staphylococcus aureus associated with subclinical mastitis in dairy cow and relationships with macrorestriction genomic profiles. Journal of Clinical Microbiology, 43(3): 1278–1284.
● Hoerlle, J.L. and Brandelli, A. (2009). Antimicrobial resistance of Staphylococcus aureus isolated from the intensive care unit of a general hospital in southern Brazil. The Journal of Infection in Developing Countries, 3(7): 504–510.
● Imani-Fooladi, A.A., Riazipour, M. and Sattari, M. (2010). Molecular and serological detection of Enterotoxigenic Staphylococcus aureus from traditionally dairy products. Journal of Shahrekord University of Medical Sciences, 11(4): 19–26 [In Persian].
● Khakpoor, M., Ezzati, M., Mahmoodi, K., Khalaji Pirbaluti, M., Khaksar, R. (2013). Prevalence of coagulase-positive Staphylococcus aureus in local cheese in West Azerbaijan with culture and PCR method. Iranian Journal of Nutrition Sciences & Food Technology, 7(5): 237–242.
● Khalifezadeh, S., Sadeghi Zali, M.H. and Nahaee, M.R. (2015). Prevalence and antibiotics susceptibility of Staphylococcus aureus in traditional Kouzeh cheese at Saqqez retails. Journal of Food Hygiene, 4(16), 1–10 [In Persian].
● Khoramian, B., Emaneini, M.E., Bolourchi, M., Eslampour, M.A., Niasari-Naslaji, A., Aligholi, M. et al., (2009). Evaluation of the biofilm-forming ability of Staphylococcus aureus isolates from bovine mastitis in Iran. Journal of Comparative Pathobiology, 6(4), 109-114.
● Lancette, G.A. and Bennet, R.W. (2001). Staphylococcus aureus and Staphylococcal Enterotoxins, In: Pouch Downes, F., Ito, K. (Editors), Compendium of methods for the microbiological examination of foods, 3rd edition, American Public Health Association, Washington DC. pp. 387–400.
● Lindqvist, R., Sylvén, S. and Vågsholm, I. (2002). Quantitative microbial risk assessment exemplified by Staphylococcus aureus in unripened cheese made from raw milk. International Journal of Food Microbiology, 78: 155–170.
● Mehrotra, M., Wang, G. and Johnson, W.M. (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(3): 1032–1035.
● Mirzaei, H., Javadi, A., Farajli, M., Shah-Mohammadi, A.R., Monadi, A.R. and Barzegar, A. (2012). Prevalence of Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city of Tabriz, Iran. Journal of Veterinary Research, 67(1): 65–70 [In Persian].
● Molla Abbaszadeh, H., Mobaiyen, H. and Mirzaei, H. (2011). Determination of prevalence rate and antibiotic resistance pattern in Staphylococcus aureus strains isolated from in-patients of Imam Reza and Shohada hospitals, Tabriz. Journal of Microbial Biotechnology, 3(9): 45–50 [In Persian].
● Molla Abaszadeh, H. and Haji Sheikhzadeh, B. (2014). Surveying the contamination rate, sensibility and antimicrobial resistance patterns in Staphylococcus aureus isolated from traditional cheese consumed in Qotur of Khoy province. Journal of Fasa University of Medical Science, 4(2): 209–217 [In Persian].
● Moroni, P., Pisoni G., Cremonesi, P. and Castiglioni, B. (2010). Staphylococcus. In: Liu, D. (Editor), Molecular Detection of Foodborne Pathogens. CRC Press, New York, pp. 245–246.
● Nagao, M., Okamoto, A., Yamada, K., Hasegawa, T., Hasegawa, Y. and Ohta, M. (2009). Variations in amount of TSST-1 produced by clinical methicillin resistant Staphylococcus aureus (MRSA) isolates and allelic variation in accessory gene regulator (agr) locus. BMC Microbiology, 9: 52.
● Norouzi, J, Goudarzi, G., Pakzad, P. and Razavipour, R. (2012). The Isolation and detection of Staphylococcus aureus enterotoxins A-E and TSST-1 genes from different sources by PCR Method. Qom University of Medical Sciences Journal, 6(3): 78–85.
● Parsonnet, J., Goering, R.V., Hansmann, M.A., Jones, M.B., Ohtagaki, K., Davis, C.C. and Totsuka, K. (2008). Prevalence of toxic shock syndrome toxin 1 (tsst-1)-producing strains of Staphylococcus aureus and antibody to tsst-1 among healthy Japanese women. Journal of Clinical Microbiology, 46(8): 2731–2738.
● Periasamy, S., Joo, H.S., Duong, A.C., Bach, T.H.L., Tan, V.Y., Chatterjee, S.S. and et al. (2011). How Staphylococcus aureus biofilms develop their characteristic structure. Proceedings of the National Academy of Sciences, 109: 1281–1286.
● Pourshafie, N., Shayegh, J. and Mobayen, H. (2015). Identification of toxic shock syndrome toxin-1 genes of Staphylococcus aureus isolated from local cheese and cow’s milk in Tabriz city. Journal of Food Microbiology, 2(6): 81–87.
● Quinn, P.J., Carter, M.E. and Barkey, B. (1994). Veterinary Microbiology, Elsevier, p. 118.
● Rahimi, F., Katouli, M. and Pourshafie, M.R. (2014). Characteristics of hospital-and community-acquired meticillin-resistant Staphylococcus aureus in Tehran, Iran. Journal of Medical Microbiology, 63(6): 796–804.
● Rahimi, F. (2015). Biofilm production among Staphylococcus aureus strains isolated from healthy people. Iranian Journal of Infectious Diseases, 68, 21–29 [In Persian].
● Rahimi, F., Bouzari, M., Katouli, M. and Pourshafie, M.R. (2013). Antibiotic resistance pattern of methicillin resistant and methicillin sensitive Staphylococcus aureus isolates in Tehran, Iran. Jundishapur Journal of Microbiology, 6(2): 144–149.
● Rahimi, E. and Alian, F. (2013). Presence of enterotoxigenic Staphylococcus aureus in cow, camel, sheep, goat and buffalo bulk tank milk. Veterinarski Arhiv, 83(1): 23–30.
● Rahimi, F., Bouzari, M., Vandyousefi, J., Maleki, Z., Saberi kashani, S. and Davoudi, S. (2008). Analysis of antibiotic resistance and detection of mecA gene in Staphylococcus aureus isolated from hospitals and medical laboratories in Tehran. Iranian Biological Journal, 21: 64–74.
● Schweizer, M.L., Perencevich, E.N., Eber, M.R., Cai, X., Shardell, M.D., Braykov, N. and Laxminarayan, R. (2013). Optimizing antimicrobial prescribing: Are clinicians following national trends in methicillin-resistant staphylococcus aureus (MRSA) infections rather than local data when treating MRSA wound infections. Antimicrobial Resistance and Infection Control, 2: 28.
● Scherrer, D., Corti, S., Muehlherr, J.E., Zweifel, C. and Stephan, R. (2004). Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep.Veterinary Micriobiology, 101: 101–107.
● Secor, P.R., James, G.A., Fleckman, P., Olerud, J.E, McInnerney, K. and Stewart, P.S. (2011). Staphylococcus aureus biofilm and planktonic cultures differentially impact gene expression, mapk phosphorylation, and cytokine production in human keratinocytes. BMC Microbiology, 11: 143.
● Singh, P. and Prakash A. (2010). Prevalance of coagulase positive pathogenic Staphylococcus aureus in milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta Agriculturae Slovenica, 96(1): 37–41.
● Srey, S., Jahid, I.K. and Ha, S.D. (2013). Biofilm formation in food industries: A food safety concern. Food Control, 31: 572–585.
● Stepanović, S., Vuković, D., Dakić, I., Savić, B. and Švabić-Vlahović, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40: 175–179.
● Teyhoo, M., Mobin, H., Mozafari, N.A., Moadab, S.R., Sedigh Bayan, K.H. and Mones Rast, S.H. (2011). The prevalence of toxic shock syndrome toxin (TSST-1) producing clinical isolates of Staphylococcus aureus strains isolated from Shohada hospital in Tabriz, Iran. Medical Laboratory Journal, 5(1): 38–44 [In Persian].
● Udobi, C.E., Obajuluwa, A.F. and Onaolapo J.A. (2013). Prevalence and antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus from an orthopaedic hospital in Nigeria. BioMed Research International, 860467, 4 pages.
● Wikler, M.A., Cockeril, F.R., Craig, W.A., Dudley, M.N., Eliopoulos, G.M., Hecht, D.W. and et al. (2007). Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Information Supplement. Clinical and Laboratory Standards Institute (CLSI), 27(1): 44–51.
