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Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar

Year 2022, , 101 - 105, 31.03.2022
https://doi.org/10.30607/kvj.1022250

Abstract

This study aimed to investigate the methicillin and Panton-Valentine leukocidin genes in Staphylococcus aureus strains isolated from clotted cream samples produced and sold in Afyonkarahisar. A total of 110 clotted cream samples sold in public bazaars of Afyonkarahisar were collected between November 2019 and December 2020. Conventional cultural methods achieved the isolation of S. aureus from clotted cream samples. For the confirmation of S. aureus strains isolated from samples and determination of mecA and pvl genes in the strains, PCR was used. In this study, while S. aureus was isolated from 14 of 110 clotted cream samples by standard cultural methods, 13 (11.8%) of 110 samples were typed to be S. aureus by PCR. The mecA and pvl genes were found in none of the 13 S. aureus strains. In this study, in which the pvl gene was investigated for the first time in the S. aureus strains isolated from clotted creams in Turkey, it was thought that more research should be done to determine mecA and pvl genes in this traditional product and other dairy products.

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References

  • Abdeen EE, Mousa WS, Abdelsalam SY, Heikal HS, Shawish RR, Nooruzzaman M, Soliman MM, Batiha GE, Hamad A, Abdeen A. Prevalence and characterization of coagulase positive Staphylococci from food products and human specimens in Egypt. Antibiotics 2021; 10: 75.
  • Algammal AM, Hetta HF, Elkelish A, Alkhalifah DHH, Hozzein WN, Batiha GS, El Nahhas N, Mabrok MA. Methicillin-Resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect. Drug Resist. 2020; 13: 3255-3265. Basanisi MG, La Bella G, Nobili G, Franconieri G, La Salandra G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol. 2017; 62: 141-146.
  • Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab. Invest. 2007; 87(1): 3-9.
  • Choi SM, Kim SH, Kim HJ, Lee DG, Choi JH, Yoo JH, Kang JH, Shin WS, Kang MW. Multiplex PCR for detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. J. Korean Med. Sci. 2003; 18(5): 631-636.
  • Dai J, Wu S, Huang J, Wu Q, Zhang F, Zhang J, Wang J, Ding Y, Zhang S, Yang X, Lei T, Xue L, Wu H. Prevalence and characterization of Staphylococcus aureus isolated from pasteurized milk in China. Front. Microbiol. 2019; 10: 641.
  • Dittmann KK, Chaul LT, Lee SHI, Corassin CH, Fernandes de Oliveira CA, Pereira De Martinis EC, Alves VF, Gram L, Oxaran V. Staphylococcus aureus in some Brazilian dairy industries: Changes of contamination and diversity. Front. Microbiol. 2017; 8: 2049.
  • Garipcin M, Seker E. Nasal carriage of methicillin-resistant Staphylococcus aureus in cattle and farm workers in Turkey. Vet. Arhiv. 2015; 85(2): 117-129.
  • Gezgen C, Seker E. Investigation of methicillin resistance and Panton-Valentine leukocidin in Staphylococci isolated from bovine mastitis. Acta Sci. Vet. 2016; 44: 1373.
  • Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter M, Gauduchon V, Vandenesch F, Etienne J. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 1999; 29(5): 1128-1132.
  • Lo W, Wang C. Panton-Valentine leukocidin in the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection. Pediatr. Neonatol. 2011; 52(2): 59-65.
  • Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, Greco G, Bellacicco AL, Virgilio S, Celano GV. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int. J. Food Microbiol. 2007; 117(2): 219-222.
  • Pamuk S, Yıldırım Y, Seker E, Gürler Z, Kara R. (2012). A survey of the occurrence and properties of methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus intermedius in water buffalo milk and dairy products in Turkey. Int. J. Dairy Technol. 2012; 65(3): 416-422.
  • Quinn PJ, Markey BK, Carter ME, Donnely WJC, Leonard FC. Veterinary Microbiology and Microbial Disease. Blackwell Publishing Professional, Iowa, 2004.
  • Papadopoulos P, Papadopoulos T, Angelidis AS, Boukouvala E, Zdragas A, Papa A, Hadjichristodoulou C, Sergelidis D. Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol. 2018; 69: 43-50.
  • Rahimi E. Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran. Brazil. J. Microbiol. 2013; 44(2): 393-399. Rainard P, Corrales JC, Barrio MB, Cochard T, Poutrel B. Leucotoxic activities of Staphylococcus aureus strains isolated from cows, ewes and goats with mastitis: Importance of LukM/LukF'-PV leucotoxin. Clin. Diagn. Lab. Immunol. 2003; 10(2): 272-277.
  • Sağlam D, Şeker E. First report of Escherichia coli O157 from traditional Turkish dairy product kaymak. Kocatepe Vet J. 2018; 11(1): 11-17.
  • Sağun E, Sancak H, Durmaz H. Van'da kahvaltı salonlarında tüketime sunulan süt ürünlerinin mikrobiyolojik ve kimyasal kaliteleri üzerine bir araştırma. Yüzüncü Yıl Üniv. Vet. Fak. Derg. 2001; 12 (1-2): 108-112.
  • Saka E, Terzi Gülel G. Detection of enterotoxin genes and methicillin-resistance in Staphylococcus aureus isolated from water buffalo milk and dairy products. J. Food Sci. 2018; 83(6): 1716-1722.
  • Singh P, Prakash A. Isolation of Escherichia coli, Staphylococcus aureus and Listeria monocytogenes from milk products sold under market conditions at Agra region. Acta Agric. Slov. 2008; 92(1): 83-88.
  • Strommenger B, Kettlitz C, Werner G, Witte W. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in S. aureus. J. Clin. Microbiol. 2003; 41(9): 4089-4094.
  • Şeker E, Özenç E, Baki Acar D, Yilmaz M. Prevalence of methicillin resistance and Panton-Valentine leukocidin genes in Staphylococci isolated from Pirlak sheep with subclinical mastitis in Turkey. Kocatepe Vet J. 2019; 12(4): 424-429.
  • Thaker HC, Brahmbhatt MN, Nayak JB. Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet. World 2013; 6(1): 10-13.
  • Tunail N. Mikrobiyel Enfeksiyonlar ve İntoksikasyonlar. Gıda Mikrobiyolojisi ve Uygulamaları. Ank. Üniv. Ziraat Fakültesi Gıda Mühendisliği Bölümü Yayını, Genişletilmiş 2. Baskı. Sim Matbaası, Ankara, 2000.
  • Türkyılmaz S, Tekbıyık S, Oryasin E, Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Public Health. 2010; 57: 197-203.
  • Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, Welty D, Long RD, Dorward DW, Gardner DJ, Lina G, Kreiswirth BN, DeLeo FR. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J. Infect. Dis. 2006; 194(12): 1761-1770.
  • Wang D, Wang Z, Yan Z, Wub J, Ali T, Li J, Lv Y, Han B. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect. Genet. Evol. 2015; 31: 9-16.
  • Yilmaz M. Sığır mastitislerinden izole edilen Staphylococcus aureus suşlarında metisilin, vankomisin direnci ve Panton-Valentine lökosidin varlığının araştırılması. Master Thesis, Afyon Kocatepe University, Health Science Institute, Afyonkarahisar, 2019. Zecconi A, Cesaris L, Liandris E, Daprà V, Piccinini R. (2006). Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microb. Pathog. 2006; 40(4): 177-183.

Afyonkarahisar'da Satışa Sunulan Kaymaklardan İzole Edilen Staphylococcus aureus Suşlarında Metisilin ve Panton-Valentine Lökosidin Genlerinin Araştırılması

Year 2022, , 101 - 105, 31.03.2022
https://doi.org/10.30607/kvj.1022250

Abstract

Bu çalışmada, Afyonkarahisar'da üretilen ve satılan kaymak örneklerinden izole edilen Staphylococcus aureus suşlarında metisilin ve Panton-Valentine lökosidin genlerinin araştırılması amaçlandı. Kasım 2019 ile Aralık 2020 tarihleri arasında Afyonkarahisar halk pazarlarında satışa sunulan toplam 110 kaymak örneği toplandı. Kaymak örneklerinden S. aureus izolasyonu konvansiyonel kültür yöntemleri kullanılarak gerçekleştirildi. Örneklerden izole edilen S. aureus suşlarının doğrulanması ve suşlarda mecA ve pvl genlerinin belirlenmesi amacıyla PZR kullanıldı. Çalışmada 110 kaymak örneğinin 14'ünden standart kültürel yöntemlerle S. aureus izole edilirken, 110 örneğin 13'ü (%11,8) PZR ile S. aureus olarak tiplendirildi. On üç S. aureus suşunun hiçbirinde mecA ve pvl genleri bulunmadı. Türkiye'de kaymaklardan izole edilen S. aureus suşlarında ilk kez pvl geninin araştırıldığı bu çalışmada, bu geleneksel ürün ve diğer süt ürünlerinde mecA ve pvl genlerinin belirlenmesi için daha fazla araştırma yapılması gerektiği düşünüldü.

Project Number

-

References

  • Abdeen EE, Mousa WS, Abdelsalam SY, Heikal HS, Shawish RR, Nooruzzaman M, Soliman MM, Batiha GE, Hamad A, Abdeen A. Prevalence and characterization of coagulase positive Staphylococci from food products and human specimens in Egypt. Antibiotics 2021; 10: 75.
  • Algammal AM, Hetta HF, Elkelish A, Alkhalifah DHH, Hozzein WN, Batiha GS, El Nahhas N, Mabrok MA. Methicillin-Resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect. Drug Resist. 2020; 13: 3255-3265. Basanisi MG, La Bella G, Nobili G, Franconieri G, La Salandra G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol. 2017; 62: 141-146.
  • Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab. Invest. 2007; 87(1): 3-9.
  • Choi SM, Kim SH, Kim HJ, Lee DG, Choi JH, Yoo JH, Kang JH, Shin WS, Kang MW. Multiplex PCR for detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. J. Korean Med. Sci. 2003; 18(5): 631-636.
  • Dai J, Wu S, Huang J, Wu Q, Zhang F, Zhang J, Wang J, Ding Y, Zhang S, Yang X, Lei T, Xue L, Wu H. Prevalence and characterization of Staphylococcus aureus isolated from pasteurized milk in China. Front. Microbiol. 2019; 10: 641.
  • Dittmann KK, Chaul LT, Lee SHI, Corassin CH, Fernandes de Oliveira CA, Pereira De Martinis EC, Alves VF, Gram L, Oxaran V. Staphylococcus aureus in some Brazilian dairy industries: Changes of contamination and diversity. Front. Microbiol. 2017; 8: 2049.
  • Garipcin M, Seker E. Nasal carriage of methicillin-resistant Staphylococcus aureus in cattle and farm workers in Turkey. Vet. Arhiv. 2015; 85(2): 117-129.
  • Gezgen C, Seker E. Investigation of methicillin resistance and Panton-Valentine leukocidin in Staphylococci isolated from bovine mastitis. Acta Sci. Vet. 2016; 44: 1373.
  • Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter M, Gauduchon V, Vandenesch F, Etienne J. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 1999; 29(5): 1128-1132.
  • Lo W, Wang C. Panton-Valentine leukocidin in the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection. Pediatr. Neonatol. 2011; 52(2): 59-65.
  • Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, Greco G, Bellacicco AL, Virgilio S, Celano GV. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. Int. J. Food Microbiol. 2007; 117(2): 219-222.
  • Pamuk S, Yıldırım Y, Seker E, Gürler Z, Kara R. (2012). A survey of the occurrence and properties of methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus intermedius in water buffalo milk and dairy products in Turkey. Int. J. Dairy Technol. 2012; 65(3): 416-422.
  • Quinn PJ, Markey BK, Carter ME, Donnely WJC, Leonard FC. Veterinary Microbiology and Microbial Disease. Blackwell Publishing Professional, Iowa, 2004.
  • Papadopoulos P, Papadopoulos T, Angelidis AS, Boukouvala E, Zdragas A, Papa A, Hadjichristodoulou C, Sergelidis D. Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol. 2018; 69: 43-50.
  • Rahimi E. Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran. Brazil. J. Microbiol. 2013; 44(2): 393-399. Rainard P, Corrales JC, Barrio MB, Cochard T, Poutrel B. Leucotoxic activities of Staphylococcus aureus strains isolated from cows, ewes and goats with mastitis: Importance of LukM/LukF'-PV leucotoxin. Clin. Diagn. Lab. Immunol. 2003; 10(2): 272-277.
  • Sağlam D, Şeker E. First report of Escherichia coli O157 from traditional Turkish dairy product kaymak. Kocatepe Vet J. 2018; 11(1): 11-17.
  • Sağun E, Sancak H, Durmaz H. Van'da kahvaltı salonlarında tüketime sunulan süt ürünlerinin mikrobiyolojik ve kimyasal kaliteleri üzerine bir araştırma. Yüzüncü Yıl Üniv. Vet. Fak. Derg. 2001; 12 (1-2): 108-112.
  • Saka E, Terzi Gülel G. Detection of enterotoxin genes and methicillin-resistance in Staphylococcus aureus isolated from water buffalo milk and dairy products. J. Food Sci. 2018; 83(6): 1716-1722.
  • Singh P, Prakash A. Isolation of Escherichia coli, Staphylococcus aureus and Listeria monocytogenes from milk products sold under market conditions at Agra region. Acta Agric. Slov. 2008; 92(1): 83-88.
  • Strommenger B, Kettlitz C, Werner G, Witte W. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in S. aureus. J. Clin. Microbiol. 2003; 41(9): 4089-4094.
  • Şeker E, Özenç E, Baki Acar D, Yilmaz M. Prevalence of methicillin resistance and Panton-Valentine leukocidin genes in Staphylococci isolated from Pirlak sheep with subclinical mastitis in Turkey. Kocatepe Vet J. 2019; 12(4): 424-429.
  • Thaker HC, Brahmbhatt MN, Nayak JB. Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet. World 2013; 6(1): 10-13.
  • Tunail N. Mikrobiyel Enfeksiyonlar ve İntoksikasyonlar. Gıda Mikrobiyolojisi ve Uygulamaları. Ank. Üniv. Ziraat Fakültesi Gıda Mühendisliği Bölümü Yayını, Genişletilmiş 2. Baskı. Sim Matbaası, Ankara, 2000.
  • Türkyılmaz S, Tekbıyık S, Oryasin E, Bozdogan B. Molecular epidemiology and antimicrobial resistance mechanisms of methicillin resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Public Health. 2010; 57: 197-203.
  • Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, Welty D, Long RD, Dorward DW, Gardner DJ, Lina G, Kreiswirth BN, DeLeo FR. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J. Infect. Dis. 2006; 194(12): 1761-1770.
  • Wang D, Wang Z, Yan Z, Wub J, Ali T, Li J, Lv Y, Han B. Bovine mastitis Staphylococcus aureus: Antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect. Genet. Evol. 2015; 31: 9-16.
  • Yilmaz M. Sığır mastitislerinden izole edilen Staphylococcus aureus suşlarında metisilin, vankomisin direnci ve Panton-Valentine lökosidin varlığının araştırılması. Master Thesis, Afyon Kocatepe University, Health Science Institute, Afyonkarahisar, 2019. Zecconi A, Cesaris L, Liandris E, Daprà V, Piccinini R. (2006). Role of several Staphylococcus aureus virulence factors on the inflammatory response in bovine mammary gland. Microb. Pathog. 2006; 40(4): 177-183.
There are 27 citations in total.

Details

Primary Language English
Subjects Veterinary Sciences
Journal Section RESEARCH ARTICLE
Authors

Aliye Horasan Yakan This is me 0000-0002-9649-6308

Esra Şeker 0000-0003-0969-5286

Project Number -
Publication Date March 31, 2022
Acceptance Date February 25, 2022
Published in Issue Year 2022

Cite

APA Horasan Yakan, A., & Şeker, E. (2022). Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar. Kocatepe Veterinary Journal, 15(1), 101-105. https://doi.org/10.30607/kvj.1022250
AMA Horasan Yakan A, Şeker E. Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar. kvj. March 2022;15(1):101-105. doi:10.30607/kvj.1022250
Chicago Horasan Yakan, Aliye, and Esra Şeker. “Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus Aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar”. Kocatepe Veterinary Journal 15, no. 1 (March 2022): 101-5. https://doi.org/10.30607/kvj.1022250.
EndNote Horasan Yakan A, Şeker E (March 1, 2022) Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar. Kocatepe Veterinary Journal 15 1 101–105.
IEEE A. Horasan Yakan and E. Şeker, “Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar”, kvj, vol. 15, no. 1, pp. 101–105, 2022, doi: 10.30607/kvj.1022250.
ISNAD Horasan Yakan, Aliye - Şeker, Esra. “Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus Aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar”. Kocatepe Veterinary Journal 15/1 (March 2022), 101-105. https://doi.org/10.30607/kvj.1022250.
JAMA Horasan Yakan A, Şeker E. Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar. kvj. 2022;15:101–105.
MLA Horasan Yakan, Aliye and Esra Şeker. “Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus Aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar”. Kocatepe Veterinary Journal, vol. 15, no. 1, 2022, pp. 101-5, doi:10.30607/kvj.1022250.
Vancouver Horasan Yakan A, Şeker E. Investigation of Methicillin and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Strains Isolated from Clotted Creams Sold in Afyonkarahisar. kvj. 2022;15(1):101-5.

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