Enterotoxin gene profiles among multi-drug resistance Staphylococcus aureus isolated from traditional dairy products in Fars providence
Subject Areas : Food Microbiology
Maryam Beygi
1
,
Mohammad Kargar
2
1 - Department of Microbiology, Jahrom Branch, Islamic Azad University, Jahrom, Iran
2 - Department of Microbiology, Jahrom Branch, Islamic Azad University, Jahrom
Keywords: Staphylococcus aureus, dairy products, Enterotoxigenic, Multi-drug resistance,
Abstract :
Background & Objectives: Staphylococcus aureus is one of the most importantfactors of food poisoning in the world. The objective of this research is to investigate the frequency amount of enterotoxin genes in traditional dairy products with multidrug resistance isolates in Fars province. Materials and Methods: This cross-sectional descriptive study was performed on 300 samples of traditional dairy products. In order to identify Staphylococcus aureus isolates in addition to standard biochemical tests, according to PCR method, nuc and 23S rRNA genes proliferation were confirmed. Enterotoxin genes were identified by using of the multiple PCR method. The susceptibility of the isolates for 16 antibiotics was investigated by using of the disk diffusion method according to CLSI criteria. Results: 120 isolates (40%) were identified as Staphylococcus aureus. The highest frequency of contamination is related to Cheese with 38 samples (31.66%) and its lowest relates to Doogh with 10 samples (8.33%). 91 samples (75.83%) of contaminated isolates were included of the enterotoxin gene, the highest frequency of enterotoxin gene was related to sea (54.17%) and its following, seb, seg, see, sed and sec respectively were included the frequency 50%, 33.33%. 28%, 16.67%, 4.17% and 3.50%. Also out of 64 strains of Staphylococcus aureus (56.33%) with multidrug resistance, 54 isolates (84.38%) had enterotoxin genes. Conclusion: The finding indicated that a significant frequency of Staphylococcus aureus isolates with enterotoxin producing multidrug resistance. Therefore, continuous molecular monitoring of Staphylococcus aureus isolates and also evaluation of the association of genetic profiles with clinical specimens is recommended.
References:
Eslami M, Koohi MK, adehashem E, Khadiri B, Keshavarz H. Survey the Presence of
Coagulase Positive Staphylococcus aureus in Cottage Cheeses Produced from Sheep Milk and
Sold in Marand County. J Food Sci Tech. 2015; 12(46): 211-218.
2. Alizadeh S, Amini K. Determining the Presence of irulence Genes Panton alentine
Leukocidin Pvl and Methicillin Resistance Gene Meca in Staphylococcus aureus Strains
Isolated from Food Samples by Multiplex PCR and Antibiotic Resistance. J Rafsanjan Univ
Med Sci. 2015; 14(5): 27-34[In persian].
3. Mahdavi S. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. J Food Hygiene. 2014; 3(4):
1-7.
4. Tavakoli H R, jodayi A A, Imani Foladi A A, sarshar M, Rafati H, Asadi bagh asiab B.
Comman Types Of Staphylococcus Aureus Enterotoxin In Meaty Foods. Iran J Clin Infect Dis
Trop Med. 2013; 17(59): 9-15.
5. Podkowik M, Park J, Seo K, Bystroń J, Bania J. Enterotoxigenic potential of
coagulase-negative staphylococci. International. J food microbiol. 2013; 163: 34-40.
6. Luss JP, antonder I. The occurrence of indicator bacteria on hands and aprons of food
handlers in the delicatessen sections of a retail group. J Food Control. 2007; 18(4): 326-332.
7. Ahmadi , Tajbakhsh E, Momtaz H. Detection of the Antibiotic Resistance Pattern in
Staphylococcus aureus Isolated from Clinical Samples Obtained from Patients Hospitalised in
Imam Reza Hospital, Kermanshah. J Microbial World. 2014; 6(4): 209-311.
8. Magiorakos A. Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Olsson‐Liljequist B.
Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international
expert proposal for interim standard definitions for acquired resistance. Clin microbiol infect.
2012; 18(3): 268-281.
9. Mirzaei H, Javadi A, Farajli M, Shah-Mohammadi A, Monadi A, Barzegar A. Prevalence of
Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city
of Tabriz, Iran. J et Res. 2012; 1.70-65 :)76(
10. Brown DFJ, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ, Wren MW.
Guidelines for the laboratory diagnosis and susceptibility testing of Methicillin-Resistant
Staphylococcus aureus (MRSA). J Antimicrob Chemother. 2005; 56: 1000-1018.
11. Mollaei M, Rashki A. The Prevalence of Adhesive Surface Encoding Genes in
Staphylococcus aureus Isolated from Hospitalized Patients in abol-Iran by Multiplex PCR. J
Fasa Univ Med Sci. 2016; 6(3): 296-302.
12. Chapaval L, Moon D, Gomes J, Duarte F, Tsai S. Use of PCR to Detect Classical
Enterotoxins Genes and Toxic Shock Syndrom Toxin-1 Gene (tst) in Staphylococcus aureus
Isolated from Crude Milk and Determination of Toxin Productivites of S.aureus. Arq Inst Biol,
Sao Paulo. 2006; 73(2): 165-169.
13. Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, imercati C, Agnellini D,
Caramenti G, Moroni P, Castiglioni B. Development of a multiplex PCR assay for the
identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy
products. Mol Cell Probes. 2005; 19: 299-305.
14. Mahdiyoun, S M, Ahanjan M, Goudarzi M, Rezaee R. Prevalence of Antibiotic Resistance in
Methicillin-Resistant Staphylococcus aureus and Determining Aminoglycoside Resistance
Gene by PCR in Sari and Tehran Hospitals. J Mazandaran Univ Med Sci. 2015; 25(128):
97-107 [In persian].
15. Nazari R, Godarzi H, Rahimi Baghi F, Moeinrad M. Enterotoxin Gene Profiles among
Staphylococcus aureus Isolated from Raw Milk. Iran J et Res. 2014; 15(4): 409.
16. Alni, R, Mohammadzadeh A, Mahmoodi P, Alikhani M. Detection of Toxic Shock Syndrome
Toxin (tsst) Gene Among Staphylococcus aureus Isolated from Patients and Healthy Carriers.
Avicenna J Clin Microbiol Infect. 2018; 5(1): 1-5.
17. MahdaviS. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. Journal of Food Hygiene. 2014;
3(4): 1-7.
18. CLSI, Performance Standards for Antimicrobial Susceptibility Testing 30th ed. CLSI
Supplement M100, CLSI, Wayne, Pa, USA; 2020.
19. Ghazavi N, Rahimi E, Esfandiari , Shakerian A. Enterotoxigencity, distribution of
enterotoxigenic genes and antibiotic resistance pattern of Staphylococcus aureus isilated from
traditional sweet. Tropical Biomedicine. 2018; 35(4): 880-892.
20. Shekarforoush SS, N Rokni, G Karim, Rohani Razavi SM, Kiaie S M M, Abbasvali M. Study
on the Overview on Food Borne Bacteria in Foodstuffs with Animal Origin in Iran, Part Two:
Meat and Meat Products. J Food Hyg. 2012; 2(3): 1-14.
21. Sadeghi, M R. The prevalence of Enterotoxigenic Isolates of Staphylococcus aureus in Bovine and Sheep Bulk Tank Milk Samples of Maku. J et Microbiol. 2015; 11(1): 27-38.
22. Imani-Fooladi A.A, Riazipour M, Sattari M. Molecular and serological detection of
Enterotoxigenic Staphylococcus aureus from traditionally dairy products. J Shahrekord Univ
Med Sci. 2010; 11(4): 19–26. [persian]
23. Singh P, Prakash A. Prevalance of coagulase positive pathogenic Staphylococcus aureus in
milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta
Agriculturae Slovenica. 2010; 96(1): 37–41.
24. Mohammadi Sani A. The survey of the distributed cheese to listeria monocytogen,
Staphylococcus aureus and Ecoli pathogens in Mashhad and Ghochan. Twelf th national
congress of Iran environment health, Shahid Beheshti medical sciences university. 522-533.
25. Molla Abaszadeh H, Haji Sheikhzadeh B. Surveying the contamination rate, sensibility and
antimicrobial resistance patterns in Staphylococcus aureus isolated from Traditional cheese
consumed in Qotur of Khoy province. J Fasa univ med sci. 2014; 4(2): 209-217.
26. Abbasi S, Taei S, amanzad B. The prevalence of methicillin-resistant Staphylococcus aureus
strains producing enterotoxin A and B. Tehran Univ Med J. 2016; 73(11):778-83 [In persian].
27. Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B. Detection of classical enterotoxins
and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products.
et microbiol. 2007; 124: 66-72.
28. icosa GN, Le Loir A, Le Loir Y, de Carvalho AF, Nero LA. egc characterization of
enterotoxigenic Staphylococcus aureus isolates obtained from raw milk and cheese. Int J Food
Microbiol. 2013; 165: 227-30.
29. Mashouf R, Hosseini S.M, Mousavi S.M. Arabestani M. Prevalence of Enterotoxin Genes and
Antibacterial Susceptibility Pattern of Staphylococcus aureus Strains Isolated from Animal
Originated Foods in West of Iran. Oman med j. 2015; 30 (4): 283.
30. Adwan G, Abu-Shanab B, Adwan K. Enterotoxigenic Staphylococcus aureus in raw milk in
the North of Palestine. Turk J Biol. 2005; 29: 229-232.
31. Ahmadi E, Ghuzivandi A, Ebrahim Pourbaser, K, Karimi Dareabi, H. Identification of sea and
seb frequency in Staphylococcus aureus isolated from cow, sheep and goat mastitic milk
samples in Sanandaj city. Iran et J. 2018; 14(2): 5-13.
32. Imani Fooladi A.A, Tavakoli H.R, Naderi A. Detection of enterotoxigenic Staphylococcus
aureus isolates in domestic dairy products. Iran J Microbiol. 2010; 2(3): 137–142.
33. Khazaei S, Pourtahmaseby P, Kanani M, Madani S.H, Malekianzadeh E. Staphylococcus
aureus Resistance to ancomycin: A Six Years Survey,(2006-2012). Med J Tabriz Univ Med
Sci Health Services. 2013; 35(5): 40-45.
34. Ma Y, hao Y, Tang J, Tang C, Chen J, Liu J. Antimicrobial susceptibility and presence of
resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CyTA-J
Food. 2018; 16(1): 76-84.
35. huge S.Y, Tan D.M, Li .G. Research on Staphylococcus aureus enterotoxin property and
drug resistance in quick frozen flour product in Guangxi. Mod Prev Med. 2015; 42: 1765-1767.
36. Teyhoo M, Mobin M, Mozafari NA, Moadab SR, Sedigh Bayan KH, Mones Rast SH. The
prevalence of Toxic shock syndrome toxin -1 (TSST-1) producing clinical isolates of
Staphylococcus aureus strain isolated from shohada hospital in Tabriz, Iran. Med lab j. 2011; 5
(1): 38-44.[persian]
37. Kumar R, Yadav B, Singh R. Antibiotic Resistance and Pathogenicity Factors in
Staphylococcus aureus Isolated from Mastitic Sahiwal Cattle. J of biosciences. 2011; 36(1):
175-88.
38. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. Staphylococcus aureus biofilms: Structures,
antibiotic resistance, inhibition, and vaccines. Gene Reports.2020; 20, 100739.
39. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. A synergistic association between
adhesion-related genes and multidrug resistance patterns of Staphylococcus aureus isolates
from different patients and healthy individuals. Journal of Global Antimicrobial
Resistance.2020; 22: 379-385.
40. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Multiplex touchdown PCR assay to
enhance specificity and sensitivity for concurrent detection of four foodbornepathogens in raw
milk. Journal of Applied Microbiology.2019; 127:262-273.
41. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Developing a multiplex real-time PCR
with anew pre-enrichment to simultaneously detect four foodborne bacteria in milk. Future
Microbiol. 201914(10):885–898.
42. Dahyot S, Lbeurre J, Argemi , Francois P, Lemee L, Prevost G, et al. Multiple-Locus
ariable Number Tandem Repeat Analysis (ML A) and Tandem Repeat Sequence Typing
(TRST), helpful tools for subtyping Staphylococcus lugdunensis. Sci Rep. 2018; 8: 1-11.
_||_
Eslami M, Koohi MK, adehashem E, Khadiri B, Keshavarz H. Survey the Presence of
Coagulase Positive Staphylococcus aureus in Cottage Cheeses Produced from Sheep Milk and
Sold in Marand County. J Food Sci Tech. 2015; 12(46): 211-218.
2. Alizadeh S, Amini K. Determining the Presence of irulence Genes Panton alentine
Leukocidin Pvl and Methicillin Resistance Gene Meca in Staphylococcus aureus Strains
Isolated from Food Samples by Multiplex PCR and Antibiotic Resistance. J Rafsanjan Univ
Med Sci. 2015; 14(5): 27-34[In persian].
3. Mahdavi S. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. J Food Hygiene. 2014; 3(4):
1-7.
4. Tavakoli H R, jodayi A A, Imani Foladi A A, sarshar M, Rafati H, Asadi bagh asiab B.
Comman Types Of Staphylococcus Aureus Enterotoxin In Meaty Foods. Iran J Clin Infect Dis
Trop Med. 2013; 17(59): 9-15.
5. Podkowik M, Park J, Seo K, Bystroń J, Bania J. Enterotoxigenic potential of
coagulase-negative staphylococci. International. J food microbiol. 2013; 163: 34-40.
6. Luss JP, antonder I. The occurrence of indicator bacteria on hands and aprons of food
handlers in the delicatessen sections of a retail group. J Food Control. 2007; 18(4): 326-332.
7. Ahmadi , Tajbakhsh E, Momtaz H. Detection of the Antibiotic Resistance Pattern in
Staphylococcus aureus Isolated from Clinical Samples Obtained from Patients Hospitalised in
Imam Reza Hospital, Kermanshah. J Microbial World. 2014; 6(4): 209-311.
8. Magiorakos A. Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Olsson‐Liljequist B.
Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international
expert proposal for interim standard definitions for acquired resistance. Clin microbiol infect.
2012; 18(3): 268-281.
9. Mirzaei H, Javadi A, Farajli M, Shah-Mohammadi A, Monadi A, Barzegar A. Prevalence of
Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city
of Tabriz, Iran. J et Res. 2012; 1.70-65 :)76(
10. Brown DFJ, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ, Wren MW.
Guidelines for the laboratory diagnosis and susceptibility testing of Methicillin-Resistant
Staphylococcus aureus (MRSA). J Antimicrob Chemother. 2005; 56: 1000-1018.
11. Mollaei M, Rashki A. The Prevalence of Adhesive Surface Encoding Genes in
Staphylococcus aureus Isolated from Hospitalized Patients in abol-Iran by Multiplex PCR. J
Fasa Univ Med Sci. 2016; 6(3): 296-302.
12. Chapaval L, Moon D, Gomes J, Duarte F, Tsai S. Use of PCR to Detect Classical
Enterotoxins Genes and Toxic Shock Syndrom Toxin-1 Gene (tst) in Staphylococcus aureus
Isolated from Crude Milk and Determination of Toxin Productivites of S.aureus. Arq Inst Biol,
Sao Paulo. 2006; 73(2): 165-169.
13. Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, imercati C, Agnellini D,
Caramenti G, Moroni P, Castiglioni B. Development of a multiplex PCR assay for the
identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy
products. Mol Cell Probes. 2005; 19: 299-305.
14. Mahdiyoun, S M, Ahanjan M, Goudarzi M, Rezaee R. Prevalence of Antibiotic Resistance in
Methicillin-Resistant Staphylococcus aureus and Determining Aminoglycoside Resistance
Gene by PCR in Sari and Tehran Hospitals. J Mazandaran Univ Med Sci. 2015; 25(128):
97-107 [In persian].
15. Nazari R, Godarzi H, Rahimi Baghi F, Moeinrad M. Enterotoxin Gene Profiles among
Staphylococcus aureus Isolated from Raw Milk. Iran J et Res. 2014; 15(4): 409.
16. Alni, R, Mohammadzadeh A, Mahmoodi P, Alikhani M. Detection of Toxic Shock Syndrome
Toxin (tsst) Gene Among Staphylococcus aureus Isolated from Patients and Healthy Carriers.
Avicenna J Clin Microbiol Infect. 2018; 5(1): 1-5.
17. MahdaviS. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. Journal of Food Hygiene. 2014;
3(4): 1-7.
18. CLSI, Performance Standards for Antimicrobial Susceptibility Testing 30th ed. CLSI
Supplement M100, CLSI, Wayne, Pa, USA; 2020.
19. Ghazavi N, Rahimi E, Esfandiari , Shakerian A. Enterotoxigencity, distribution of
enterotoxigenic genes and antibiotic resistance pattern of Staphylococcus aureus isilated from
traditional sweet. Tropical Biomedicine. 2018; 35(4): 880-892.
20. Shekarforoush SS, N Rokni, G Karim, Rohani Razavi SM, Kiaie S M M, Abbasvali M. Study
on the Overview on Food Borne Bacteria in Foodstuffs with Animal Origin in Iran, Part Two:
Meat and Meat Products. J Food Hyg. 2012; 2(3): 1-14.
21. Sadeghi, M R. The prevalence of Enterotoxigenic Isolates of Staphylococcus aureus in Bovine and Sheep Bulk Tank Milk Samples of Maku. J et Microbiol. 2015; 11(1): 27-38.
22. Imani-Fooladi A.A, Riazipour M, Sattari M. Molecular and serological detection of
Enterotoxigenic Staphylococcus aureus from traditionally dairy products. J Shahrekord Univ
Med Sci. 2010; 11(4): 19–26. [persian]
23. Singh P, Prakash A. Prevalance of coagulase positive pathogenic Staphylococcus aureus in
milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta
Agriculturae Slovenica. 2010; 96(1): 37–41.
24. Mohammadi Sani A. The survey of the distributed cheese to listeria monocytogen,
Staphylococcus aureus and Ecoli pathogens in Mashhad and Ghochan. Twelf th national
congress of Iran environment health, Shahid Beheshti medical sciences university. 522-533.
25. Molla Abaszadeh H, Haji Sheikhzadeh B. Surveying the contamination rate, sensibility and
antimicrobial resistance patterns in Staphylococcus aureus isolated from Traditional cheese
consumed in Qotur of Khoy province. J Fasa univ med sci. 2014; 4(2): 209-217.
26. Abbasi S, Taei S, amanzad B. The prevalence of methicillin-resistant Staphylococcus aureus
strains producing enterotoxin A and B. Tehran Univ Med J. 2016; 73(11):778-83 [In persian].
27. Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B. Detection of classical enterotoxins
and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products.
et microbiol. 2007; 124: 66-72.
28. icosa GN, Le Loir A, Le Loir Y, de Carvalho AF, Nero LA. egc characterization of
enterotoxigenic Staphylococcus aureus isolates obtained from raw milk and cheese. Int J Food
Microbiol. 2013; 165: 227-30.
29. Mashouf R, Hosseini S.M, Mousavi S.M. Arabestani M. Prevalence of Enterotoxin Genes and
Antibacterial Susceptibility Pattern of Staphylococcus aureus Strains Isolated from Animal
Originated Foods in West of Iran. Oman med j. 2015; 30 (4): 283.
30. Adwan G, Abu-Shanab B, Adwan K. Enterotoxigenic Staphylococcus aureus in raw milk in
the North of Palestine. Turk J Biol. 2005; 29: 229-232.
31. Ahmadi E, Ghuzivandi A, Ebrahim Pourbaser, K, Karimi Dareabi, H. Identification of sea and
seb frequency in Staphylococcus aureus isolated from cow, sheep and goat mastitic milk
samples in Sanandaj city. Iran et J. 2018; 14(2): 5-13.
32. Imani Fooladi A.A, Tavakoli H.R, Naderi A. Detection of enterotoxigenic Staphylococcus
aureus isolates in domestic dairy products. Iran J Microbiol. 2010; 2(3): 137–142.
33. Khazaei S, Pourtahmaseby P, Kanani M, Madani S.H, Malekianzadeh E. Staphylococcus
aureus Resistance to ancomycin: A Six Years Survey,(2006-2012). Med J Tabriz Univ Med
Sci Health Services. 2013; 35(5): 40-45.
34. Ma Y, hao Y, Tang J, Tang C, Chen J, Liu J. Antimicrobial susceptibility and presence of
resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CyTA-J
Food. 2018; 16(1): 76-84.
35. huge S.Y, Tan D.M, Li .G. Research on Staphylococcus aureus enterotoxin property and
drug resistance in quick frozen flour product in Guangxi. Mod Prev Med. 2015; 42: 1765-1767.
36. Teyhoo M, Mobin M, Mozafari NA, Moadab SR, Sedigh Bayan KH, Mones Rast SH. The
prevalence of Toxic shock syndrome toxin -1 (TSST-1) producing clinical isolates of
Staphylococcus aureus strain isolated from shohada hospital in Tabriz, Iran. Med lab j. 2011; 5
(1): 38-44.[persian]
37. Kumar R, Yadav B, Singh R. Antibiotic Resistance and Pathogenicity Factors in
Staphylococcus aureus Isolated from Mastitic Sahiwal Cattle. J of biosciences. 2011; 36(1):
175-88.
38. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. Staphylococcus aureus biofilms: Structures,
antibiotic resistance, inhibition, and vaccines. Gene Reports.2020; 20, 100739.
39. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. A synergistic association between
adhesion-related genes and multidrug resistance patterns of Staphylococcus aureus isolates
from different patients and healthy individuals. Journal of Global Antimicrobial
Resistance.2020; 22: 379-385.
40. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Multiplex touchdown PCR assay to
enhance specificity and sensitivity for concurrent detection of four foodbornepathogens in raw
milk. Journal of Applied Microbiology.2019; 127:262-273.
41. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Developing a multiplex real-time PCR
with anew pre-enrichment to simultaneously detect four foodborne bacteria in milk. Future
Microbiol. 201914(10):885–898.
42. Dahyot S, Lbeurre J, Argemi , Francois P, Lemee L, Prevost G, et al. Multiple-Locus
ariable Number Tandem Repeat Analysis (ML A) and Tandem Repeat Sequence Typing
(TRST), helpful tools for subtyping Staphylococcus lugdunensis. Sci Rep. 2018; 8: 1-11.
Coagulase Positive Staphylococcus aureus in Cottage Cheeses Produced from Sheep Milk and
Sold in Marand County. J Food Sci Tech. 2015; 12(46): 211-218.
2. Alizadeh S, Amini K. Determining the Presence of irulence Genes Panton alentine
Leukocidin Pvl and Methicillin Resistance Gene Meca in Staphylococcus aureus Strains
Isolated from Food Samples by Multiplex PCR and Antibiotic Resistance. J Rafsanjan Univ
Med Sci. 2015; 14(5): 27-34[In persian].
3. Mahdavi S. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. J Food Hygiene. 2014; 3(4):
1-7.
4. Tavakoli H R, jodayi A A, Imani Foladi A A, sarshar M, Rafati H, Asadi bagh asiab B.
Comman Types Of Staphylococcus Aureus Enterotoxin In Meaty Foods. Iran J Clin Infect Dis
Trop Med. 2013; 17(59): 9-15.
5. Podkowik M, Park J, Seo K, Bystroń J, Bania J. Enterotoxigenic potential of
coagulase-negative staphylococci. International. J food microbiol. 2013; 163: 34-40.
6. Luss JP, antonder I. The occurrence of indicator bacteria on hands and aprons of food
handlers in the delicatessen sections of a retail group. J Food Control. 2007; 18(4): 326-332.
7. Ahmadi , Tajbakhsh E, Momtaz H. Detection of the Antibiotic Resistance Pattern in
Staphylococcus aureus Isolated from Clinical Samples Obtained from Patients Hospitalised in
Imam Reza Hospital, Kermanshah. J Microbial World. 2014; 6(4): 209-311.
8. Magiorakos A. Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Olsson‐Liljequist B.
Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international
expert proposal for interim standard definitions for acquired resistance. Clin microbiol infect.
2012; 18(3): 268-281.
9. Mirzaei H, Javadi A, Farajli M, Shah-Mohammadi A, Monadi A, Barzegar A. Prevalence of
Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city
of Tabriz, Iran. J et Res. 2012; 1.70-65 :)76(
10. Brown DFJ, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ, Wren MW.
Guidelines for the laboratory diagnosis and susceptibility testing of Methicillin-Resistant
Staphylococcus aureus (MRSA). J Antimicrob Chemother. 2005; 56: 1000-1018.
11. Mollaei M, Rashki A. The Prevalence of Adhesive Surface Encoding Genes in
Staphylococcus aureus Isolated from Hospitalized Patients in abol-Iran by Multiplex PCR. J
Fasa Univ Med Sci. 2016; 6(3): 296-302.
12. Chapaval L, Moon D, Gomes J, Duarte F, Tsai S. Use of PCR to Detect Classical
Enterotoxins Genes and Toxic Shock Syndrom Toxin-1 Gene (tst) in Staphylococcus aureus
Isolated from Crude Milk and Determination of Toxin Productivites of S.aureus. Arq Inst Biol,
Sao Paulo. 2006; 73(2): 165-169.
13. Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, imercati C, Agnellini D,
Caramenti G, Moroni P, Castiglioni B. Development of a multiplex PCR assay for the
identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy
products. Mol Cell Probes. 2005; 19: 299-305.
14. Mahdiyoun, S M, Ahanjan M, Goudarzi M, Rezaee R. Prevalence of Antibiotic Resistance in
Methicillin-Resistant Staphylococcus aureus and Determining Aminoglycoside Resistance
Gene by PCR in Sari and Tehran Hospitals. J Mazandaran Univ Med Sci. 2015; 25(128):
97-107 [In persian].
15. Nazari R, Godarzi H, Rahimi Baghi F, Moeinrad M. Enterotoxin Gene Profiles among
Staphylococcus aureus Isolated from Raw Milk. Iran J et Res. 2014; 15(4): 409.
16. Alni, R, Mohammadzadeh A, Mahmoodi P, Alikhani M. Detection of Toxic Shock Syndrome
Toxin (tsst) Gene Among Staphylococcus aureus Isolated from Patients and Healthy Carriers.
Avicenna J Clin Microbiol Infect. 2018; 5(1): 1-5.
17. MahdaviS. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. Journal of Food Hygiene. 2014;
3(4): 1-7.
18. CLSI, Performance Standards for Antimicrobial Susceptibility Testing 30th ed. CLSI
Supplement M100, CLSI, Wayne, Pa, USA; 2020.
19. Ghazavi N, Rahimi E, Esfandiari , Shakerian A. Enterotoxigencity, distribution of
enterotoxigenic genes and antibiotic resistance pattern of Staphylococcus aureus isilated from
traditional sweet. Tropical Biomedicine. 2018; 35(4): 880-892.
20. Shekarforoush SS, N Rokni, G Karim, Rohani Razavi SM, Kiaie S M M, Abbasvali M. Study
on the Overview on Food Borne Bacteria in Foodstuffs with Animal Origin in Iran, Part Two:
Meat and Meat Products. J Food Hyg. 2012; 2(3): 1-14.
21. Sadeghi, M R. The prevalence of Enterotoxigenic Isolates of Staphylococcus aureus in Bovine and Sheep Bulk Tank Milk Samples of Maku. J et Microbiol. 2015; 11(1): 27-38.
22. Imani-Fooladi A.A, Riazipour M, Sattari M. Molecular and serological detection of
Enterotoxigenic Staphylococcus aureus from traditionally dairy products. J Shahrekord Univ
Med Sci. 2010; 11(4): 19–26. [persian]
23. Singh P, Prakash A. Prevalance of coagulase positive pathogenic Staphylococcus aureus in
milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta
Agriculturae Slovenica. 2010; 96(1): 37–41.
24. Mohammadi Sani A. The survey of the distributed cheese to listeria monocytogen,
Staphylococcus aureus and Ecoli pathogens in Mashhad and Ghochan. Twelf th national
congress of Iran environment health, Shahid Beheshti medical sciences university. 522-533.
25. Molla Abaszadeh H, Haji Sheikhzadeh B. Surveying the contamination rate, sensibility and
antimicrobial resistance patterns in Staphylococcus aureus isolated from Traditional cheese
consumed in Qotur of Khoy province. J Fasa univ med sci. 2014; 4(2): 209-217.
26. Abbasi S, Taei S, amanzad B. The prevalence of methicillin-resistant Staphylococcus aureus
strains producing enterotoxin A and B. Tehran Univ Med J. 2016; 73(11):778-83 [In persian].
27. Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B. Detection of classical enterotoxins
and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products.
et microbiol. 2007; 124: 66-72.
28. icosa GN, Le Loir A, Le Loir Y, de Carvalho AF, Nero LA. egc characterization of
enterotoxigenic Staphylococcus aureus isolates obtained from raw milk and cheese. Int J Food
Microbiol. 2013; 165: 227-30.
29. Mashouf R, Hosseini S.M, Mousavi S.M. Arabestani M. Prevalence of Enterotoxin Genes and
Antibacterial Susceptibility Pattern of Staphylococcus aureus Strains Isolated from Animal
Originated Foods in West of Iran. Oman med j. 2015; 30 (4): 283.
30. Adwan G, Abu-Shanab B, Adwan K. Enterotoxigenic Staphylococcus aureus in raw milk in
the North of Palestine. Turk J Biol. 2005; 29: 229-232.
31. Ahmadi E, Ghuzivandi A, Ebrahim Pourbaser, K, Karimi Dareabi, H. Identification of sea and
seb frequency in Staphylococcus aureus isolated from cow, sheep and goat mastitic milk
samples in Sanandaj city. Iran et J. 2018; 14(2): 5-13.
32. Imani Fooladi A.A, Tavakoli H.R, Naderi A. Detection of enterotoxigenic Staphylococcus
aureus isolates in domestic dairy products. Iran J Microbiol. 2010; 2(3): 137–142.
33. Khazaei S, Pourtahmaseby P, Kanani M, Madani S.H, Malekianzadeh E. Staphylococcus
aureus Resistance to ancomycin: A Six Years Survey,(2006-2012). Med J Tabriz Univ Med
Sci Health Services. 2013; 35(5): 40-45.
34. Ma Y, hao Y, Tang J, Tang C, Chen J, Liu J. Antimicrobial susceptibility and presence of
resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CyTA-J
Food. 2018; 16(1): 76-84.
35. huge S.Y, Tan D.M, Li .G. Research on Staphylococcus aureus enterotoxin property and
drug resistance in quick frozen flour product in Guangxi. Mod Prev Med. 2015; 42: 1765-1767.
36. Teyhoo M, Mobin M, Mozafari NA, Moadab SR, Sedigh Bayan KH, Mones Rast SH. The
prevalence of Toxic shock syndrome toxin -1 (TSST-1) producing clinical isolates of
Staphylococcus aureus strain isolated from shohada hospital in Tabriz, Iran. Med lab j. 2011; 5
(1): 38-44.[persian]
37. Kumar R, Yadav B, Singh R. Antibiotic Resistance and Pathogenicity Factors in
Staphylococcus aureus Isolated from Mastitic Sahiwal Cattle. J of biosciences. 2011; 36(1):
175-88.
38. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. Staphylococcus aureus biofilms: Structures,
antibiotic resistance, inhibition, and vaccines. Gene Reports.2020; 20, 100739.
39. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. A synergistic association between
adhesion-related genes and multidrug resistance patterns of Staphylococcus aureus isolates
from different patients and healthy individuals. Journal of Global Antimicrobial
Resistance.2020; 22: 379-385.
40. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Multiplex touchdown PCR assay to
enhance specificity and sensitivity for concurrent detection of four foodbornepathogens in raw
milk. Journal of Applied Microbiology.2019; 127:262-273.
41. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Developing a multiplex real-time PCR
with anew pre-enrichment to simultaneously detect four foodborne bacteria in milk. Future
Microbiol. 201914(10):885–898.
42. Dahyot S, Lbeurre J, Argemi , Francois P, Lemee L, Prevost G, et al. Multiple-Locus
ariable Number Tandem Repeat Analysis (ML A) and Tandem Repeat Sequence Typing
(TRST), helpful tools for subtyping Staphylococcus lugdunensis. Sci Rep. 2018; 8: 1-11.
_||_
Coagulase Positive Staphylococcus aureus in Cottage Cheeses Produced from Sheep Milk and
Sold in Marand County. J Food Sci Tech. 2015; 12(46): 211-218.
2. Alizadeh S, Amini K. Determining the Presence of irulence Genes Panton alentine
Leukocidin Pvl and Methicillin Resistance Gene Meca in Staphylococcus aureus Strains
Isolated from Food Samples by Multiplex PCR and Antibiotic Resistance. J Rafsanjan Univ
Med Sci. 2015; 14(5): 27-34[In persian].
3. Mahdavi S. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. J Food Hygiene. 2014; 3(4):
1-7.
4. Tavakoli H R, jodayi A A, Imani Foladi A A, sarshar M, Rafati H, Asadi bagh asiab B.
Comman Types Of Staphylococcus Aureus Enterotoxin In Meaty Foods. Iran J Clin Infect Dis
Trop Med. 2013; 17(59): 9-15.
5. Podkowik M, Park J, Seo K, Bystroń J, Bania J. Enterotoxigenic potential of
coagulase-negative staphylococci. International. J food microbiol. 2013; 163: 34-40.
6. Luss JP, antonder I. The occurrence of indicator bacteria on hands and aprons of food
handlers in the delicatessen sections of a retail group. J Food Control. 2007; 18(4): 326-332.
7. Ahmadi , Tajbakhsh E, Momtaz H. Detection of the Antibiotic Resistance Pattern in
Staphylococcus aureus Isolated from Clinical Samples Obtained from Patients Hospitalised in
Imam Reza Hospital, Kermanshah. J Microbial World. 2014; 6(4): 209-311.
8. Magiorakos A. Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, Olsson‐Liljequist B.
Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international
expert proposal for interim standard definitions for acquired resistance. Clin microbiol infect.
2012; 18(3): 268-281.
9. Mirzaei H, Javadi A, Farajli M, Shah-Mohammadi A, Monadi A, Barzegar A. Prevalence of
Staphylococcus aureus resistant to methicillin in traditional cheese and cream: a study in city
of Tabriz, Iran. J et Res. 2012; 1.70-65 :)76(
10. Brown DFJ, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ, Wren MW.
Guidelines for the laboratory diagnosis and susceptibility testing of Methicillin-Resistant
Staphylococcus aureus (MRSA). J Antimicrob Chemother. 2005; 56: 1000-1018.
11. Mollaei M, Rashki A. The Prevalence of Adhesive Surface Encoding Genes in
Staphylococcus aureus Isolated from Hospitalized Patients in abol-Iran by Multiplex PCR. J
Fasa Univ Med Sci. 2016; 6(3): 296-302.
12. Chapaval L, Moon D, Gomes J, Duarte F, Tsai S. Use of PCR to Detect Classical
Enterotoxins Genes and Toxic Shock Syndrom Toxin-1 Gene (tst) in Staphylococcus aureus
Isolated from Crude Milk and Determination of Toxin Productivites of S.aureus. Arq Inst Biol,
Sao Paulo. 2006; 73(2): 165-169.
13. Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, imercati C, Agnellini D,
Caramenti G, Moroni P, Castiglioni B. Development of a multiplex PCR assay for the
identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy
products. Mol Cell Probes. 2005; 19: 299-305.
14. Mahdiyoun, S M, Ahanjan M, Goudarzi M, Rezaee R. Prevalence of Antibiotic Resistance in
Methicillin-Resistant Staphylococcus aureus and Determining Aminoglycoside Resistance
Gene by PCR in Sari and Tehran Hospitals. J Mazandaran Univ Med Sci. 2015; 25(128):
97-107 [In persian].
15. Nazari R, Godarzi H, Rahimi Baghi F, Moeinrad M. Enterotoxin Gene Profiles among
Staphylococcus aureus Isolated from Raw Milk. Iran J et Res. 2014; 15(4): 409.
16. Alni, R, Mohammadzadeh A, Mahmoodi P, Alikhani M. Detection of Toxic Shock Syndrome
Toxin (tsst) Gene Among Staphylococcus aureus Isolated from Patients and Healthy Carriers.
Avicenna J Clin Microbiol Infect. 2018; 5(1): 1-5.
17. MahdaviS. Prevalence of Six Genes Encoding Enterotoxins Production of Staphylococcus
aureus Isolated from White-Brined-Cheese by Multiplex PCR. Journal of Food Hygiene. 2014;
3(4): 1-7.
18. CLSI, Performance Standards for Antimicrobial Susceptibility Testing 30th ed. CLSI
Supplement M100, CLSI, Wayne, Pa, USA; 2020.
19. Ghazavi N, Rahimi E, Esfandiari , Shakerian A. Enterotoxigencity, distribution of
enterotoxigenic genes and antibiotic resistance pattern of Staphylococcus aureus isilated from
traditional sweet. Tropical Biomedicine. 2018; 35(4): 880-892.
20. Shekarforoush SS, N Rokni, G Karim, Rohani Razavi SM, Kiaie S M M, Abbasvali M. Study
on the Overview on Food Borne Bacteria in Foodstuffs with Animal Origin in Iran, Part Two:
Meat and Meat Products. J Food Hyg. 2012; 2(3): 1-14.
21. Sadeghi, M R. The prevalence of Enterotoxigenic Isolates of Staphylococcus aureus in Bovine and Sheep Bulk Tank Milk Samples of Maku. J et Microbiol. 2015; 11(1): 27-38.
22. Imani-Fooladi A.A, Riazipour M, Sattari M. Molecular and serological detection of
Enterotoxigenic Staphylococcus aureus from traditionally dairy products. J Shahrekord Univ
Med Sci. 2010; 11(4): 19–26. [persian]
23. Singh P, Prakash A. Prevalance of coagulase positive pathogenic Staphylococcus aureus in
milk and milk products collected from unorganized sector of Agra. Journal Guide-Acta
Agriculturae Slovenica. 2010; 96(1): 37–41.
24. Mohammadi Sani A. The survey of the distributed cheese to listeria monocytogen,
Staphylococcus aureus and Ecoli pathogens in Mashhad and Ghochan. Twelf th national
congress of Iran environment health, Shahid Beheshti medical sciences university. 522-533.
25. Molla Abaszadeh H, Haji Sheikhzadeh B. Surveying the contamination rate, sensibility and
antimicrobial resistance patterns in Staphylococcus aureus isolated from Traditional cheese
consumed in Qotur of Khoy province. J Fasa univ med sci. 2014; 4(2): 209-217.
26. Abbasi S, Taei S, amanzad B. The prevalence of methicillin-resistant Staphylococcus aureus
strains producing enterotoxin A and B. Tehran Univ Med J. 2016; 73(11):778-83 [In persian].
27. Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B. Detection of classical enterotoxins
and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products.
et microbiol. 2007; 124: 66-72.
28. icosa GN, Le Loir A, Le Loir Y, de Carvalho AF, Nero LA. egc characterization of
enterotoxigenic Staphylococcus aureus isolates obtained from raw milk and cheese. Int J Food
Microbiol. 2013; 165: 227-30.
29. Mashouf R, Hosseini S.M, Mousavi S.M. Arabestani M. Prevalence of Enterotoxin Genes and
Antibacterial Susceptibility Pattern of Staphylococcus aureus Strains Isolated from Animal
Originated Foods in West of Iran. Oman med j. 2015; 30 (4): 283.
30. Adwan G, Abu-Shanab B, Adwan K. Enterotoxigenic Staphylococcus aureus in raw milk in
the North of Palestine. Turk J Biol. 2005; 29: 229-232.
31. Ahmadi E, Ghuzivandi A, Ebrahim Pourbaser, K, Karimi Dareabi, H. Identification of sea and
seb frequency in Staphylococcus aureus isolated from cow, sheep and goat mastitic milk
samples in Sanandaj city. Iran et J. 2018; 14(2): 5-13.
32. Imani Fooladi A.A, Tavakoli H.R, Naderi A. Detection of enterotoxigenic Staphylococcus
aureus isolates in domestic dairy products. Iran J Microbiol. 2010; 2(3): 137–142.
33. Khazaei S, Pourtahmaseby P, Kanani M, Madani S.H, Malekianzadeh E. Staphylococcus
aureus Resistance to ancomycin: A Six Years Survey,(2006-2012). Med J Tabriz Univ Med
Sci Health Services. 2013; 35(5): 40-45.
34. Ma Y, hao Y, Tang J, Tang C, Chen J, Liu J. Antimicrobial susceptibility and presence of
resistance & enterotoxins/enterotoxin-likes genes in Staphylococcus aureus from food. CyTA-J
Food. 2018; 16(1): 76-84.
35. huge S.Y, Tan D.M, Li .G. Research on Staphylococcus aureus enterotoxin property and
drug resistance in quick frozen flour product in Guangxi. Mod Prev Med. 2015; 42: 1765-1767.
36. Teyhoo M, Mobin M, Mozafari NA, Moadab SR, Sedigh Bayan KH, Mones Rast SH. The
prevalence of Toxic shock syndrome toxin -1 (TSST-1) producing clinical isolates of
Staphylococcus aureus strain isolated from shohada hospital in Tabriz, Iran. Med lab j. 2011; 5
(1): 38-44.[persian]
37. Kumar R, Yadav B, Singh R. Antibiotic Resistance and Pathogenicity Factors in
Staphylococcus aureus Isolated from Mastitic Sahiwal Cattle. J of biosciences. 2011; 36(1):
175-88.
38. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. Staphylococcus aureus biofilms: Structures,
antibiotic resistance, inhibition, and vaccines. Gene Reports.2020; 20, 100739.
39. Parastan R, Kargar M, Solhjoo K,Kafilzadeh F. A synergistic association between
adhesion-related genes and multidrug resistance patterns of Staphylococcus aureus isolates
from different patients and healthy individuals. Journal of Global Antimicrobial
Resistance.2020; 22: 379-385.
40. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Multiplex touchdown PCR assay to
enhance specificity and sensitivity for concurrent detection of four foodbornepathogens in raw
milk. Journal of Applied Microbiology.2019; 127:262-273.
41. Moezi P, Kargar M, Doosti A, Khoshneviszadeh M. Developing a multiplex real-time PCR
with anew pre-enrichment to simultaneously detect four foodborne bacteria in milk. Future
Microbiol. 201914(10):885–898.
42. Dahyot S, Lbeurre J, Argemi , Francois P, Lemee L, Prevost G, et al. Multiple-Locus
ariable Number Tandem Repeat Analysis (ML A) and Tandem Repeat Sequence Typing
(TRST), helpful tools for subtyping Staphylococcus lugdunensis. Sci Rep. 2018; 8: 1-11.
