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The Importance of Foodborne Enterococci in Terms of Food and Human Health (Turkish with English Abstract)

Year 2011, Volume: 36 Issue: 5, 303 - 310, 01.10.2011

Abstract

Enterococci are bacteria which play an important role in organoleptic properties of many fermented foods through their proteolytic and lipolytic activities; some strains can produce bacteriocin, resistant to pasteurization temperatures and adapt to different growth conditions. In recent years, the reports about enterococci used as starter cultures, co-cultures or probiotics have increased considerably, because of these properties. Although the probiotic benefits of some strains are well established, enterococci are recognized as major nosocomial pathogens that cause bacteraemia, endocarditis, urinary tract and other infections. The pathogenicity of enterococci is related to virulence factors and antibiotic resistance. Antibiotic resistant strains have been found in meat products, dairy products, and ready-to-eat foods, and even within enterococcal strains used as probiotics. In this review, it has been emphasized the general characteristics of enterococci, their isolation and identification methods from foods and also the importance of these bacteria in terms of food and human health.

References

  • Franz CMAP, Holzapfel WH, Stiles ME. 1999. Enterococci at the crossroads of food safety? Review. Int J Food Microbiol, 47, 1–24.
  • Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Review. Microbiol, 155, 1749–1757.
  • Domig KJ, Mayer HK, Kneifel W. 2003. Methods used for the isolation, enumeration, characterization and identification of Enterococcus spp. 1. Media for isolation and enumeration. Review article. Int J Food Microbiol, 88, 147– 164.
  • Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH. 2003. Enterococci in foods - a conundrum for food safety. Review article. Int J Food Microbiol, 88, 105– 122.
  • Klein G. 2003. Taxonomy, ecology and antibiotic resistance of enterococci from food and gastro-intestinal tract. Review. Int J Food Microbiol, 88, 123-131.
  • İşleroğlu H, Yıldırım Z, Demirpençe Y, Yıldırım M. 2008. Enterokoklar: Biyokimyasal, fizyolojik ve fonksiyonel özellikleri ile patojenitesi. Derleme makale. Akademik Gıda, 6(3), 16-26.
  • Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. 2006. The role and application of enterococci in food and health. Review. Int J Food Microbiol, 106, 1 – 24.
  • Belgacem ZB, Abriouel H, Ben Omar N, Lucas R, Martínez-Cañamero M, Gálvez A, Manai M. 2010. Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control, 21, 462–470.
  • Sánchez Valenzuela A, Benomar N, Abriouel H, Martínez-Cañamero M, Gálvez A. 2010. Isolation and identification of Enterococcus faecium from seafoods: Antimicrobial resistance and production of bacteriocin-like substances. Food Microbiol, 27, 955-961.
  • Tunail N. 1999. Microflora of the Intestine/ Biology of the Enterococcus spp. in; Encyclopedia of Food Microbiology. Robinson RK (chief ed), Academic Press, UK, pp 1365-1373.
  • Ruzauskas M, Suziedeliene E, Siugzdiniene R, Seputiene V, Povilonis J. 2010. Antimicrobial resistance of Enterococcus spp. spread in poultry products in Lithuania. J Food Safety, 30, 902–915. 12. Foulquie Moreno MR, Rea MC, Cogan TM, De Vuyst L. 2003. Applicability of a bacteriocin- producing Enterococcus faecium as a co-culture in Cheddar cheese manufacture. Int J Food Microbiol, 81(1), 73-84.
  • Canzek Majhenic A, Rogelj I, Perko B. 2005. Enterococci from Tolminc cheese: Population structure, antibiotic susceptibility and incidence of virulence determinants. Short communication. Int J Food Microbiol, 102, 239-244.
  • Koluman A, Akan LS, Cakiroglu FP. 2009. Occurrence and antimicrobial resistance of enterococci in retail foods. Food Control, 20, 281–283. 15. Ghazi F, Henni DE, Benmechernene Z, Kihal M. 2009. Phenotypic and whole cell protein analysis by SDS-PAGE for identification of dominants lactic acid bacteria isolated from Algerian raw milk. World J Dairy Food Sci, 4 (1), 78-87.
  • Albano H, van Reenen CA, Todorov SD, Cruz D, Fraga L, Hogg T, Dicks LMT, Teixeira P. 2009. Phenotypic and genetic heterogeneity of lactic acid bacteria isolated from ‘‘Alheira", a traditional fermented sausage produced in Portugal. Meat Sci, 82, 389–398.
  • Pangallo D, Drahovska H, Harichova J, Karelova E, Chovanova K, Aradska J, Ferianc P, Turna J, Timko J. 2008. Evaluation of different PCR-based approaches for the identification and typing of environmental enterococci. Anton Leeuw, 93, 193–203.
  • Domig KJ, Mayer HK, Kneifel W. 2003. Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp. 2. Pheno- and genotypic criteria, Review article. J Food Microbiol, 88, 165– 188.
  • Brtkova A, Filipova M, Drahovska H, Bujdakova H. 2010. Characterization of enterococci of animal and environmental origin using phenotypic methods and comparison with PCR based methods. Veterinarni Medicina, 55 (3), 97–105. 20. Canzek Majhenic A. 2006. Enterococci: yin - yang microbes. Mljekarstvo, 56(1) 5-20.
  • Khan H, Flint S, Yu PL. 2010. Enterocins in food preservation. Int J Food Microbiol, 141, 1–10. 25. Alvarez-Cisneros YM, Fernandez FJ, Wacher- Rodarte C, Aguilar MB, del Rosario Sainz Espunes T, Ponce-Alquicira E. 2010. Biochemical characterization of a bacteriocin-like inhibitory substance produced by Enterococcus faecium MXVK29, isolated from Mexican traditional sausage. J Sci Food Agric, 90, 2475–2481.
  • Ghrairi T, Frere J, Berjeaud JM, Manai M. 2008. Purification and characterisation of bacteriocins produced by Enterococcus faecium from Tunisian rigouta cheese. Food Control, 19, 162–169.
  • Cosansu S, Kuleasan H, Ayhan K, Materon L. 2007. Antimicrobial activity and protein profiles of Pediococcus spp. isolated from Turkish "Sucuk". J Food Process Pres, 31, 190–200.
  • Altuntaş EG, Ayhan K. 2009. Purification process and characterization methods of bacteriocins produced by lactic acid bacteria (LAB). TUBITAK-MAM 3rdInternational Congress on Food and Nutrition, 22-25 April 2009, Antalya, Turkey, p. 101
  • Coşansu S, Geornaras I, Ayhan K, Sofos JN. 2009. Control of Listeria monocytogenes on ready-to-eat turkey breast slices by bacteriocin. TUBITAK-MAM 3rdInternational Congress on Food and Nutrition, 22-25 April, Antalya, Turkey, p. 76. 30. Nieto-Arribas P, Seseña S, Poveda JM, Chicón R, Cabezas L, Palop L. 2011. Enterococcus populations in artisanal Manchego cheese: Biodiversity, technological and safety aspects. Food Microbiol, 28, 891-899.
  • Ayhan K, Durlu-Özkaya F. 2007. Biogenic amines in foods. In: Metabolism and Applications of Lactic acid Bacteria. Barbaros Özer (chef ed), Research Signpost, 37/661 (2), Kerela, India. 27p.
  • Hajikhani R, Beyatlı Y, Aslım B. 2007. Antimicrobial activity of enterococci strains isolated from white cheese. Int J Dairy Technol, 60(2), 105-108.
  • Gürses M, Erdogan A. 2006. Identification of lactic acid bacteria isolated from Tulum cheese during ripening period. Int J Food Prop, 9, 551–557.
  • Tuncer Y. 2009. Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese. Afr J Biotechnol, 8(24), 7008-7016.
  • Sırıken B, Ozdemir M, Yavuz H, Pamuk S. 2006. The microbiological quality and residual nitrate/nitrite levels in Turkish sausage (soudjouck) produced in Afyon Province, Turkey. Food Control, 17, 923–928.
  • Erginkaya Z, Yurdakul NE, Karakaş A. 2007. Enterococcus faecium ve Enterococcus faecalis’in starter ve probiyotik kültür özellikleri. GIDA, 32(3), 137-142.
  • Frazzon APG, Gama BA, Hermes V, Bierhals CG, Pereira RI, Guedes AG, d’Azevedo PA, Frazzon J. 2010. Prevalence of antimicrobial resistance and molecular characterization of tetracycline resistance mediated by tet(M) and tet(L) genes in Enterococcus spp. isolated from food in Southern Brazil. World J Microbiol Biotechnol, 26, 365–370.
  • von Wright A, Bruce A. 2003. Genetically modified microorganisms and their potential effects on human health and nutrition. Trends Food Sci Tech, 14, 264-276.
  • Bhardwaj A, Gupta H, Kapila S, Kaur G, Vij S, Malik RK. 2010. Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. Int J Food Microbiol, 141, 156–164.
  • Franz CMAP, Muscholl-Silberhorn AB, Yousif NMK, Vancanneyt M, Swings J, Holzapfel WH. 2001. Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 67(9), 4385–4389.
  • Ogier JC, Serror P. 2008. Safety assessment of dairy microorganisms: The Enterococcus genus. Int J Food Microbiol, 126, 291–301.
  • Jurkovic D, Krizkova L, Dusinsky R, Belicova A, Sojka M, Krajcovic J, Ebringer L. 2006. Identification and characterization of enterococci from bryndza cheese. The Society for Applied Microbiology, Lett Appl Microbiol, 42, 553–559.
  • Cariolato D, Andrighetto C, Lombardini A. 2008. Occurrence of virulence factors and antibiotic resistance in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19, 886-892.
  • Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi LA, Franco BDGM, De Martinis ECP. 2008. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol, 25(5), 668-75.
  • Sánchez Valenzuela A, Ben Omar N, Abriouel H, López RL, Veljovic K, Cañamero MM, Milan Topisirovic KL, Gálvez A. 2009. Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control, 20, 381–385.
  • Özmen Toğay S, Çelebi Keskin A, Açık L, Temiz A. 2010. Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J Appl Microbiol, 109, 1084–1092.
  • Eaton TJ, Gasson MJ. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol, 67(4), 1628-1635.
  • Barbosa J, Gibbs PA, Teixeira P. 2010. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control, 21, 651–656.
  • Carlos AR, Semedo-Lemsaddek T, Barreto- Crespo MT, Tenreiro R. 2010. Transcriptional analysis of virulence-related genes in enterococci from distinct origins. J Appl Microbiol, 108, 1563–1575.

Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi

Year 2011, Volume: 36 Issue: 5, 303 - 310, 01.10.2011

Abstract

Enterokoklar, proteolitik ve lipolitik aktivitelerinden dolayı pek çok fermente gıdanın duyusal özelliklerinde rol oynayan, bazı suşları bakteriyosin üretebilen, pastörizasyon sıcaklıklarına dirençli ve farklı sıcaklıklara ve üreme koşullarına adapte olabilme yeteneğine sahip bakterilerdir. Son yıllarda yapılan çalışmalar bu özelliklerinden dolayı gıda endüstrisinde enterokokların starter, yardımcı kültür ve probiyotik olarak kullanımının arttığını göstermektedir. Bazı suşlarının iyi bilinen yararlı etkilerinin yanında enterokokların bakteriyemi, endokarditis, üriner sistemde ve diğer dokularda enfeksiyonlara neden olan hastane kaynaklı patojen olduğu da bilinmektedir. Enterokokların patojenitesi virülens faktörleri ve antibiyotiklere direnç özellikleri ile ilişkilendirilmektedir. Antibiyotiklere dirençli suşlar et ürünleri, süt ürünleri ve hazır gıdalarda bulunabilmekte, hatta probiyotik olarak kullanılan suşlar dahi antibiyotiklere dirençli olabilmektedir. Bu derlemede enterokokların genel özellikleri, gıdalardan izolasyon ve tanımlama yöntemlerinin yanında gıda ve insan sağlığı açısından önemi üzerinde durulmuştur.

References

  • Franz CMAP, Holzapfel WH, Stiles ME. 1999. Enterococci at the crossroads of food safety? Review. Int J Food Microbiol, 47, 1–24.
  • Fisher K, Phillips C. 2009. The ecology, epidemiology and virulence of Enterococcus. Review. Microbiol, 155, 1749–1757.
  • Domig KJ, Mayer HK, Kneifel W. 2003. Methods used for the isolation, enumeration, characterization and identification of Enterococcus spp. 1. Media for isolation and enumeration. Review article. Int J Food Microbiol, 88, 147– 164.
  • Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH. 2003. Enterococci in foods - a conundrum for food safety. Review article. Int J Food Microbiol, 88, 105– 122.
  • Klein G. 2003. Taxonomy, ecology and antibiotic resistance of enterococci from food and gastro-intestinal tract. Review. Int J Food Microbiol, 88, 123-131.
  • İşleroğlu H, Yıldırım Z, Demirpençe Y, Yıldırım M. 2008. Enterokoklar: Biyokimyasal, fizyolojik ve fonksiyonel özellikleri ile patojenitesi. Derleme makale. Akademik Gıda, 6(3), 16-26.
  • Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. 2006. The role and application of enterococci in food and health. Review. Int J Food Microbiol, 106, 1 – 24.
  • Belgacem ZB, Abriouel H, Ben Omar N, Lucas R, Martínez-Cañamero M, Gálvez A, Manai M. 2010. Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control, 21, 462–470.
  • Sánchez Valenzuela A, Benomar N, Abriouel H, Martínez-Cañamero M, Gálvez A. 2010. Isolation and identification of Enterococcus faecium from seafoods: Antimicrobial resistance and production of bacteriocin-like substances. Food Microbiol, 27, 955-961.
  • Tunail N. 1999. Microflora of the Intestine/ Biology of the Enterococcus spp. in; Encyclopedia of Food Microbiology. Robinson RK (chief ed), Academic Press, UK, pp 1365-1373.
  • Ruzauskas M, Suziedeliene E, Siugzdiniene R, Seputiene V, Povilonis J. 2010. Antimicrobial resistance of Enterococcus spp. spread in poultry products in Lithuania. J Food Safety, 30, 902–915. 12. Foulquie Moreno MR, Rea MC, Cogan TM, De Vuyst L. 2003. Applicability of a bacteriocin- producing Enterococcus faecium as a co-culture in Cheddar cheese manufacture. Int J Food Microbiol, 81(1), 73-84.
  • Canzek Majhenic A, Rogelj I, Perko B. 2005. Enterococci from Tolminc cheese: Population structure, antibiotic susceptibility and incidence of virulence determinants. Short communication. Int J Food Microbiol, 102, 239-244.
  • Koluman A, Akan LS, Cakiroglu FP. 2009. Occurrence and antimicrobial resistance of enterococci in retail foods. Food Control, 20, 281–283. 15. Ghazi F, Henni DE, Benmechernene Z, Kihal M. 2009. Phenotypic and whole cell protein analysis by SDS-PAGE for identification of dominants lactic acid bacteria isolated from Algerian raw milk. World J Dairy Food Sci, 4 (1), 78-87.
  • Albano H, van Reenen CA, Todorov SD, Cruz D, Fraga L, Hogg T, Dicks LMT, Teixeira P. 2009. Phenotypic and genetic heterogeneity of lactic acid bacteria isolated from ‘‘Alheira", a traditional fermented sausage produced in Portugal. Meat Sci, 82, 389–398.
  • Pangallo D, Drahovska H, Harichova J, Karelova E, Chovanova K, Aradska J, Ferianc P, Turna J, Timko J. 2008. Evaluation of different PCR-based approaches for the identification and typing of environmental enterococci. Anton Leeuw, 93, 193–203.
  • Domig KJ, Mayer HK, Kneifel W. 2003. Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp. 2. Pheno- and genotypic criteria, Review article. J Food Microbiol, 88, 165– 188.
  • Brtkova A, Filipova M, Drahovska H, Bujdakova H. 2010. Characterization of enterococci of animal and environmental origin using phenotypic methods and comparison with PCR based methods. Veterinarni Medicina, 55 (3), 97–105. 20. Canzek Majhenic A. 2006. Enterococci: yin - yang microbes. Mljekarstvo, 56(1) 5-20.
  • Khan H, Flint S, Yu PL. 2010. Enterocins in food preservation. Int J Food Microbiol, 141, 1–10. 25. Alvarez-Cisneros YM, Fernandez FJ, Wacher- Rodarte C, Aguilar MB, del Rosario Sainz Espunes T, Ponce-Alquicira E. 2010. Biochemical characterization of a bacteriocin-like inhibitory substance produced by Enterococcus faecium MXVK29, isolated from Mexican traditional sausage. J Sci Food Agric, 90, 2475–2481.
  • Ghrairi T, Frere J, Berjeaud JM, Manai M. 2008. Purification and characterisation of bacteriocins produced by Enterococcus faecium from Tunisian rigouta cheese. Food Control, 19, 162–169.
  • Cosansu S, Kuleasan H, Ayhan K, Materon L. 2007. Antimicrobial activity and protein profiles of Pediococcus spp. isolated from Turkish "Sucuk". J Food Process Pres, 31, 190–200.
  • Altuntaş EG, Ayhan K. 2009. Purification process and characterization methods of bacteriocins produced by lactic acid bacteria (LAB). TUBITAK-MAM 3rdInternational Congress on Food and Nutrition, 22-25 April 2009, Antalya, Turkey, p. 101
  • Coşansu S, Geornaras I, Ayhan K, Sofos JN. 2009. Control of Listeria monocytogenes on ready-to-eat turkey breast slices by bacteriocin. TUBITAK-MAM 3rdInternational Congress on Food and Nutrition, 22-25 April, Antalya, Turkey, p. 76. 30. Nieto-Arribas P, Seseña S, Poveda JM, Chicón R, Cabezas L, Palop L. 2011. Enterococcus populations in artisanal Manchego cheese: Biodiversity, technological and safety aspects. Food Microbiol, 28, 891-899.
  • Ayhan K, Durlu-Özkaya F. 2007. Biogenic amines in foods. In: Metabolism and Applications of Lactic acid Bacteria. Barbaros Özer (chef ed), Research Signpost, 37/661 (2), Kerela, India. 27p.
  • Hajikhani R, Beyatlı Y, Aslım B. 2007. Antimicrobial activity of enterococci strains isolated from white cheese. Int J Dairy Technol, 60(2), 105-108.
  • Gürses M, Erdogan A. 2006. Identification of lactic acid bacteria isolated from Tulum cheese during ripening period. Int J Food Prop, 9, 551–557.
  • Tuncer Y. 2009. Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese. Afr J Biotechnol, 8(24), 7008-7016.
  • Sırıken B, Ozdemir M, Yavuz H, Pamuk S. 2006. The microbiological quality and residual nitrate/nitrite levels in Turkish sausage (soudjouck) produced in Afyon Province, Turkey. Food Control, 17, 923–928.
  • Erginkaya Z, Yurdakul NE, Karakaş A. 2007. Enterococcus faecium ve Enterococcus faecalis’in starter ve probiyotik kültür özellikleri. GIDA, 32(3), 137-142.
  • Frazzon APG, Gama BA, Hermes V, Bierhals CG, Pereira RI, Guedes AG, d’Azevedo PA, Frazzon J. 2010. Prevalence of antimicrobial resistance and molecular characterization of tetracycline resistance mediated by tet(M) and tet(L) genes in Enterococcus spp. isolated from food in Southern Brazil. World J Microbiol Biotechnol, 26, 365–370.
  • von Wright A, Bruce A. 2003. Genetically modified microorganisms and their potential effects on human health and nutrition. Trends Food Sci Tech, 14, 264-276.
  • Bhardwaj A, Gupta H, Kapila S, Kaur G, Vij S, Malik RK. 2010. Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. Int J Food Microbiol, 141, 156–164.
  • Franz CMAP, Muscholl-Silberhorn AB, Yousif NMK, Vancanneyt M, Swings J, Holzapfel WH. 2001. Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 67(9), 4385–4389.
  • Ogier JC, Serror P. 2008. Safety assessment of dairy microorganisms: The Enterococcus genus. Int J Food Microbiol, 126, 291–301.
  • Jurkovic D, Krizkova L, Dusinsky R, Belicova A, Sojka M, Krajcovic J, Ebringer L. 2006. Identification and characterization of enterococci from bryndza cheese. The Society for Applied Microbiology, Lett Appl Microbiol, 42, 553–559.
  • Cariolato D, Andrighetto C, Lombardini A. 2008. Occurrence of virulence factors and antibiotic resistance in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19, 886-892.
  • Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi LA, Franco BDGM, De Martinis ECP. 2008. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol, 25(5), 668-75.
  • Sánchez Valenzuela A, Ben Omar N, Abriouel H, López RL, Veljovic K, Cañamero MM, Milan Topisirovic KL, Gálvez A. 2009. Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control, 20, 381–385.
  • Özmen Toğay S, Çelebi Keskin A, Açık L, Temiz A. 2010. Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J Appl Microbiol, 109, 1084–1092.
  • Eaton TJ, Gasson MJ. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol, 67(4), 1628-1635.
  • Barbosa J, Gibbs PA, Teixeira P. 2010. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control, 21, 651–656.
  • Carlos AR, Semedo-Lemsaddek T, Barreto- Crespo MT, Tenreiro R. 2010. Transcriptional analysis of virulence-related genes in enterococci from distinct origins. J Appl Microbiol, 108, 1563–1575.
There are 41 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Sine Özmen Toğay This is me

Ayhan Temiz This is me

Publication Date October 1, 2011
Published in Issue Year 2011 Volume: 36 Issue: 5

Cite

APA Toğay, S. Ö. ., & Temiz, A. . (2011). Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi. Gıda, 36(5), 303-310.
AMA Toğay SÖ, Temiz A. Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi. The Journal of Food. October 2011;36(5):303-310.
Chicago Toğay, Sine Özmen, and Ayhan Temiz. “Gıda Kaynaklı Enterokokların Gıda Ve İnsan Sağlığı Yönünden Önemi”. Gıda 36, no. 5 (October 2011): 303-10.
EndNote Toğay SÖ, Temiz A (October 1, 2011) Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi. Gıda 36 5 303–310.
IEEE S. Ö. . Toğay and A. . Temiz, “Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi”, The Journal of Food, vol. 36, no. 5, pp. 303–310, 2011.
ISNAD Toğay, Sine Özmen - Temiz, Ayhan. “Gıda Kaynaklı Enterokokların Gıda Ve İnsan Sağlığı Yönünden Önemi”. Gıda 36/5 (October 2011), 303-310.
JAMA Toğay SÖ, Temiz A. Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi. The Journal of Food. 2011;36:303–310.
MLA Toğay, Sine Özmen and Ayhan Temiz. “Gıda Kaynaklı Enterokokların Gıda Ve İnsan Sağlığı Yönünden Önemi”. Gıda, vol. 36, no. 5, 2011, pp. 303-10.
Vancouver Toğay SÖ, Temiz A. Gıda Kaynaklı Enterokokların Gıda ve İnsan Sağlığı Yönünden Önemi. The Journal of Food. 2011;36(5):303-10.

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