Antibiotic resistance and enterotoxin gene profiles of Staphylococcus aureus isolated from raw milk in Iran

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Δημοσιευμένα: Apr 12, 2023
Εκδόσεις:
2023-04-12 (1)
DOI: https://doi.org/10.12681/jhvms.29671
M Shariatifar
Department of Food Hygiene and Aquaculture, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
https://orcid.org/0000-0002-6093-1064
M Salavati-Hamedani
Department of Food Hygiene and Aquaculture, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
https://orcid.org/0000-0002-4416-861X
R Rezaeian-Doloei
Department of Agricultural Sciences, Faculty of Sciences, Mashhad Branch, Islamic Azad University, Mashhad, Iran
https://orcid.org/0000-0002-1911-1216
M Rezaeigolestani
Department of Food Hygiene and Aquaculture, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
https://orcid.org/0000-0002-6417-0565
M Mohsenzadeh
a:1:{s:5:"en_US";s:30:"Ferdowsi University of Mashhad";}
https://orcid.org/0000-0002-7829-039X
Περίληψη

Staphylococcus aureus is a food-borne pathogen frequently isolated from raw milk in different parts of the world. The emergence of antibiotic resistant strains of S. aureus has become an important global public health issue. In spite of this problem, the contamination rate of raw milk with enterotoxigenic antibiotic resistant S. aureus strains has been rarely evaluated in Iran. This study aimed to evaluate the prevalence and antibiotic resistance of coagulase positive S. aureus strains isolated from bulk tank milk samples in Mashhad, and to analyze the frequency of genes encoding the staphylococcal enterotoxins (SEs). 250 milk samples were tested for S. aureus by the conventional plating method and PCR. The disc diffusion method was used to assess the antibiotic susceptibility of the isolated S. aureus. Finally, the frequency of the SEs encoding genes was determined by the PCR method. S. aureus was detected in 18.4% of the tested milk samples at mean concentrations of 3.5 × 105 CFU/ml. The results showed that 86.95% of the isolates were resistant to at least one antibiotic and the highest resistance was observed against penicillin, ampicillin and methicillin. In total, 71.74% of the studied bacteria had at least one of the SEs encoding genes, and sec and sea genes were the most prevalent ones. In conclusion, the prevalence of enterotoxigenic antibiotic-resistant S. aureus in the milk samples collected from Mashhad dairy farms proves that additional efforts must be devoted to implementing hygienic processes in dairy farms and controlling antibiotic usage as well.

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Αναφορές
Abera, M, Demie, B, Aragaw, K, Regassa, F, & Regassa, A (2010) Isolation and identification of Staphylococcusaureus from bovine mastitic
milk and their drug resistance patterns in Adama town, Ethiopia. J Vet
Med Anim Heal 2 (3) : 29-34.
Carfora, V, Caprioli, A, Marri, N, Sagrafoli, D, Boselli, C, Giacinti, G,
Giangolini, G, Sorbara, L, Dottarelli, S, Battisti, A, & Amatiste, S
(2015) Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcusaureus isolated from milk and dairy products in Central Italy. Int Dairy J 42: 12-15.
Chen, Q, & Xie, S (2019) Genotypes, Enterotoxin Gene Profiles, and
Antimicrobial Resistance of Staphylococcusaureus Associated with
Foodborne Outbreaks in Hangzhou, China. In Toxins (Vol. 11, Issue
.
Cho, YS, Lee, MK, & Hwang, SH (2019) Toxin gene profiles, genetic
diversity, antimicrobial resistance, and coagulase type of Staphylococcusaureus from cream-filled bakery products. Food Sci Nutr 7 (5)
: 1727-1734.
CLSI (2018) M100 Performance Standards for Antimicrobial Susceptibility Testing. In Clinical and Laboratory Standards Institute.
Eid, HM, El-Mahallawy, HS, Mohammed, SR, Mohammed, NEY, & Eidaroos, NH (2022) Multidrug-resistant and enterotoxigenic methicillin-resistant Staphylococcusaureus isolated from raw milk of cows
at small-scale production units. J Adv Vet Anim Res 9 (1) : 113-121.
Fagundes, H, Barchesi, L, Filho, A, Menezes, F, & Oliveira, C (2010)
Occurrence of Staphylococcusaureus in raw milk produced in dairy
farms in São Paulo state, Brazil. Brazilian J Microbiol 41:.
Fooladi, AAI, Tavakoli, HR, & Naderi, A (1970) Detection of enterotoxigenic Staphylococcus aureus isolates in domestic dairy products. Iran
J Microbiol 2 (3 SE-Articles) :
Giacinti, G, Carfora, V, Caprioli, A, Sagrafoli, D, Marri, N, Giangolini, G,
Amoruso, R, Iurescia, M, Stravino, F, Dottarelli, S, Feltrin, F, Franco,
A, Amatiste, S, & Battisti, A (2017) Prevalence and characterization
of methicillin-resistant Staphylococcus aureuscarrying mecAor mecC
and methicillin-susceptible Staphylococcus aureus in dairy sheep
farms in central Italy. J Dairy Sci 100 (10) : 7857-7863.
Haghi, F, Daneshamooz, S, Parsadanians, A, & Zeighami, H (2019) The
Frequency of Staphylococcusaureus Classical Enterotoxin Genes in
Raw Milk Samples in Zanjan, Iran TT -. 5 (1) : 32-35.
Hait, J, Tallent, S, Melka, D, Keys, C, & Bennett, R (2014) Prevalence of
enterotoxins and toxin gene profiles of Staphylococcus aureus isolates recovered from a bakery involved in a second staphylococcal
food poisoning occurrence. J Appl Microbiol 117 (3) : 866-875.
Hemamalini, V, Kavitha, V, & Ramachandran, S (2015) In vitro antibiogram pattern of Staphylococcusaureus isolated from wound infection and molecular analysis of mecA gene and restriction sites in
methicillin resistant Staphylococcus aureus. J Adv Pharm Technol
Res 6 (4) : 170-175.
Hwang, SY, Kim, SH, Jang, EJ, Kwon, NH, Park, YK, Koo, HC, Jung,
WK, Kim, JM, & Park, YH (2007) Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application
to raw meat isolates in Korea. Int J Food Microbiol 117 (1) : 99-105.
Johler, S, Weder, D, Bridy, C, Huguenin, M-C, Robert, L, Hummerjohann,
J, & Stephan, R (2015) Outbreak of staphylococcal food poisoning
among children and staff at a Swiss boarding school due to soft
cheese made from raw milk. J Dairy Sci 98 (5) : 2944-2948.
Johnson, WM, Tyler, SD, Ewan, EP, Ashton, FE, Pollard, DR, & Rozee,
KR (1991) Detection of genes for enterotoxins, exfoliative toxins,
and toxic shock syndrome toxin 1 in Staphylococcusaureus by the
polymerase chain reaction. J Clin Microbiol 29 (3) : 426-430.
Jørgensen, HJ, Mathisen, T, Løvseth, A, Omoe, K, Qvale, KS, & Loncarevic, S (2005) An outbreak of staphylococcal food poisoning caused
by enterotoxin H in mashed potato made with raw milk. FEMS Microbiol Lett 252 (2) : 267-272.
Khairullah, AR, Sudjarwo, SA, Effendi, MH, Harijani, N, Tyasningsih,
W, Rahmahani, J, Permatasari, DA, Ramandinianto, SC, Widodo, A,
& Riwu, KHP (2020) A review of methicillin-resistant Staphylococcusaureus (MRSA) on milk and milk products: Public health importance. Syst Rev Pharm 11 (8) : 59-69.
Lawrynowicz-Paciorek, M, Kochman, M, Piekarska, K, Grochowska,
A, & Windyga, B (2007) The distribution of enterotoxin and enterotoxin-like genes in Staphylococcusaureus strains isolated from nasal
carriers and food samples. Int J Food Microbiol 117 (3) : 319-323.
Mehrotra, M, Wang, G, & Johnson, WM (2000) Multiplex PCR for detection of genes for Staphylococcusaureus enterotoxins, exfoliative
toxins, toxic shock syndrome toxin 1, and methicillin resistance. J
Clin Microbiol 38 (3) : 1032-1035.
Mohsenzadeh, M, Ghazvini, K, & Azimian, A (2015) Frequency of specific agr groups and antibiotic resistance in Staphylococcusaureus
isolated from bovine mastitis in the northeast of Iran. Vet Res Forum
an Int Q J 6 (4) : 295-299.
Monistero, V, Barberio, A, Biscarini, F, Cremonesi, P, Castiglioni, B, Graber, HU, Bottini, E, Ceballos-Marquez, A, Kroemker, V, Petzer, IM,
Pollera, C, Santisteban, C, Veiga Dos Santos, M, Bronzo, V, Piccinini, R, Re, G, Cocchi, M, & Moroni, P (2020) Different distribution
of antimicrobial resistance genes and virulence profiles of Staphylococcusaureus strains isolated from clinical mastitis in six countries. J
Dairy Sci 103 (4) : 3431-3446.
Morandi, S, Brasca, M, Lodi, R, Cremonesi, P, & Castiglioni, B (2007)
Detection of classical enterotoxins and identification of enterotoxin
genes in Staphylococcusaureus from milk and dairy products. Vet
Microbiol 124 (1) : 66-72.
Nazari, R, Godarzi, H, Rahimi Baghi, F, & Moeinrad, M (2014) Enterotoxin gene profiles among Staphylococcusaureus isolated from raw
milk. Iran J Vet Res 15 (4) : 409-412.
Omoe, K, Ishikawa, M, Shimoda, Y, Hu, D-L, Ueda, S, & Shinagawa, K
(2002) Detection of seg, seh, and sei genes in Staphylococcu alence of Staphylococcusaureus and of methicillin-resistant S. aureus
(MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol 69: 43-50.
Pelisser, MR, Klein, CS, Ascoli, KR, Zotti, TR, & Arisi, ACM (2009)
Ocurrence of Staphylococcusaureus and multiplex pcr detection of
classic enterotoxin genes in cheese and meat products. Braz J Microbiol 40 (1) : 145-148.
Rahbar Saadat, Y, Imani Fooladi, AA, Shapouri, R, Hosseini, MM, & Deilami Khiabani, Z (2014) Prevalence of enterotoxigenic Staphylococcusaureus in organic milk and cheese in Tabriz, Iran. Iran J Microbiol
(5) : 345-349.
Rahimi, E (2013) Enterotoxigenicity of Staphylococcusaureus isolated
from traditional and commercial dairy products marketed in Iran.
Braz J Microbiol 44 (2) : 393-399.
Rahimi, E, & Safai, HG (2010) Detection of classical enterotoxins of
Staphylococcusaureus strains isolated from bovine subclinical mastitis in Isfahan, Iran. Vet Microbiol 141 (3-4) : 393-394.
Regasa, S, Mengistu, S, & Abraha, A (2019) Milk Safety Assessment, Isolation, and Antimicrobial Susceptibility Profile of Staphylococcus aureus in Selected Dairy Farms of Mukaturi and Sululta Town, Oromia
Region, Ethiopia. Vet Med Int 2019: 3063185.
Riva, A, Borghi, E, Cirasola, D, Colmegna, S, Borgo, F, Amato, E, Pontello, MM, & Morace, G (2015) Methicillin-resistant Staphylococcusaureus in raw milk: Prevalence, SCCmec typing, enterotoxin
characterization, and antimicrobial resistance patterns. J Food Prot
(6) : 1142-1146.
Riyaz-Ul-Hassan, S, Verma, V, & Qazi, GN (2008) Evaluation of three
different molecular markers for the detection of Staphylococcusaureus by polymerase chain reaction. Food Microbiol 25 (3) : 452-459.
Sahebekhtiari, N, Nochi, Z, Eslampour, M, Dabiri, H, Bolfion, M,
Khoramian, B, Zali, M, & Emaneini, M (2011) Characterization of
Staphylococcusaureus strains isolated from raw milk of bovine subclinical mastitis in Tehran and Mashhad. Acta Microbiol Immunol
Hung 58: 113-121.
Song, M, Bai, Y, Xu, J, Carter, MQ, Shi, C, & Shi, X (2015) Genetic
diversity and virulence potential of Staphylococcusaureus isolates
from raw and processed food commodities in Shanghai. Int J Food
Microbiol 195: 1-8.
Titouche, Y, Hakem, A, Houali, K, Meheut, T, Vingadassalon, N, Ruiz-Ripa, L, Salmi, D, Chergui, A, Chenouf, N, Hennekinne, JA, Torres, C,
& Auvray, F (2019) Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products
in the Tizi Ouzou area of Algeria. J Dairy Sci 102 (8) : 6876-6884.
Zhao, X, Yuan, X, Hu, M, Zhang, Y, Li, L, Zhang, Q, Yuan, X, Wang, W, &
Liu, Y (2021) Prevalence and characterization of Staphylococcusaureus and methicillin-resistant Staphylococcusaureus isolated from
bulk tank milk in Shandong dairy farms. Food Control 125: 107836.