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Investigation of Escherichia coli O157 in Turkish homemade white cheese

Year 2013, Volume: 72 Issue: 1, 45 - 51, 07.11.2013

Abstract

Verocytotoxin-producing Escherichia coli (VTEC) are important pathogens that cause serious public health risks such as food poisoning. Raw milk and cheeses made from raw or inadequately pasteurized milk remain a potential vehicle for VTEC serotype O157 infections. In this study, the occurrence of E. coli serotype O157 was investigated in a total of 245 Turkish homemade white cheeses, produced in rural areas, which were collected from various open public bazaars. Twenty-one non-sorbitol fermenting colonies were detected as suspicious E. coli O157 isolates on the sorbitol MacConkey Agar supplemented with cefixime and tellurite (CT-SMAC). Presumptive E. coli O157 isolates were tested for agglutination according to the manufacturers' instructions with a commercial E. coli O157 latex test. E. coli O157 was not detected in any of the 245 Turkish homemade white cheeses, popular food consumed by Turkish people. In conclusion, it is pleasing to note the absence of E. coli O157 in all of this popular food. However, it may be advisable to carry out a careful surveillance in such food in view of consumers' health and the possible presence of E. coli O157:H7, an important foodborne pathogen.

Keywords

: Homemade white cheese, Escherichia coli O157, CT-SMAC, Foodborne infection, Latex test.

*Corresponding author:

Seza Arslan (e-mail: arslan_s3@ibu.edu.tr)

(Received: 22.10.2012 Accepted: 04.02.2013)

References

  • Akçamlı E. (2008) A study on the presence of enterohemorrhagic Escherichia coli O157:H7 in Blue cheese sold in public markets in Konya province. MSc. dissertation, University of Selçuk, Turkey.
  • Anonymous (1996) VTEC O157 infection in West Yorkshire associated with the consumption of raw milk. Commuicable Disease Report Weekly, 6: 1
  • Ansay S.E. and Kaspar C.W. (1997) Survey of retail cheeses, dairy processing environments and raw milk for Escherichia coli O157:H7. Letters in Applied Microbiology, 25: 131-134.
  • Aslantaş Ö. and Yıldız P. (2002) Isolation of Escherichia coli O157:H7 in animal originated foods in Kars region. Veteriner Bilimleri Dergisi, 18: 107-111.
  • Baz E., Gülmez M., Güven A., Sezer Ç. and Duman B. (2003) Examination of coliforms, E. coli and E. coli O157 in raw milk and ripened white cheese samples sold in Kars-Turkey. Kafkas
  • Universitesi Veteriner Fakültesi Dergisi, 9: 165-1 Bhunia A.K. (2008) Foodborne Microbial
  • Pathogens: Mechanisms and Pathogenesis. Springer, New York, USA. Caro I. and Garcia-Armesto M.R. (2007) Occurrence of Shiga toxin-producing Escherichia coli in a Spanish raw ewe’s milk cheese. International Journal of Food Microbiology, 116: 410-413.
  • Coia J.E., Johnston Y., Steers N.J. and Hanson M.F. (2001) A survey of the prevalence of Escherichia coli O157 in raw meats, raw cow’s milk and raw-milk cheeses in south-east Scotland. International Journal of Food Microbiology, 66: 63-69.
  • Dontorou C., Papadopoulou C., Filioussis G., Economou V., Apostolou I., Zakkas G., Salamoura A., Kansouzidou A. and Levidiotou S. (2003) Isolation of Escherichia coli O157:H7 from foods in Greece. International Journal of Food Microbiology, 82: 273-279.
  • Durch J., Ringhand T., Manner K., Proetor M., Davis J. and Boxrud D. (2000) Outbreak of
  • Escherichia coli O157:H7 infection associated with eating fresh cheese curds. Morbiditiy and Mortality Weekly Report, 49, 911–913. Erkan E.M., Çiftcioğlu G., Vural A. and Aksu H. (2007) Some microbiological characteristics of herbed cheeses. Journal of Food Quality, 30: 228-236.
  • Espie E., Vaillant V., Mariani-Kurkdjian P., Grimont F., Martin-Schaller R., De Valk H. and VernozyRozand C. (2006) Escherichia coli O157 outbreak associated with fresh unpasteurized goats’ cheese. Epidemiology and Infection, 134: 143-1
  • Ewing W.H. (1986) Differentiation of Enterobacteriaceae by biochemical reactions. In: Ewing W.H. (ed.), Edwards and Ewing identification of Enterobacteriaceae. (4th Edn.), Elsevier Science Publishing, New York, pp: 47Gonzalez A.G.M., Rosa A.C.P., Andrade J.R.C. and Tibana A. (2000) Enteropathogenicity markers in Escherichia coli strains isolated from soft white cheese and poultry in Rio de Janeiro, Brazil. Food Microbiolology, 17: 321-328.
  • Govaris A., Koidis P. and Papatheodorou K. (2001) The fate of Escherichia coli O157:H7 in Myzithra, Anthotyros, and Manouri whey cheeses during storage at 2 and 12 °C. Food Microbiolology, 18: 565-570.
  • Govaris A., Papageorgiou D.K. and Papatheodorou K. (2002) Behavior of Escherichia coli O157:H7 during the manufacture and ripening of Feta and Telemes cheeses. Journal of Food Protection, 65: 609-615.
  • Griffin P. and Tauxe R. (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic Escherichia coli and the associated hemolytic uremic syndrome. Epidemiologic Reviews, 13: 60-98.
  • Hancock D.D., Besser T.E., Kinsel M.L., Tarr P.I., Rice D.H. and Paros M.G. (1994) The prevalence of Escherichia coli O157:H7 in dairy and beef cattle in Washington State. Epidemiology and Infection, 113: 199-207.
  • Heuvelink A.E., Bleuminck B., Van den Biggelaar F.L., Te Giffel M.C., Beumer R.R. and De Boer E. (1998) Occurrence and survival of verocytotoxin-producing Escherichia coli O157 in raw cow’s milk in The Netherlands. Journal of Food Protection, 61: 1597-1601.
  • Honish L., Predy G., Hislop N., Chui L., Kowalevska-Grochowska K., Trottier L., Kreplin C. and Zazulak I. (2005) An outbreak E. coli O157:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese. Canadian Journal of Public Health, 96: 182-184.
  • Ingham S.C., Su Y.C. and Spangenberg D.S. (2000) Survival of Salmonella typhimurium and Escherichia coli O157:H7 in cheese brines. International Journal of Food Microbiology, 61:73-79.
  • Jones D.L. (1999) Potential health risks associated with the persistence of Escherichia coli O157 in agricultural environments. Soil Use and Management, 15: 76-83.
  • Karch H., Bielaszewska M., Bitzan M. and Schmidt H. (1999) Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagnostic Microbiology and Infectious Disease, 34: 229-243.
  • Karmali M.A. (1989) Infection by verotoxinproducing Escherichia coli. Clinical
  • Microbiology Reviews, 2: 15-28. Mora A., Leon S.L., Blanco M., Blanco J.E., Lopez C., Dahbi G., Echeita A., Gonzalez E.A. and Blanco J. (2007) Phage types, virulence genes and PFGE profiles of Shiga-toxin-producing
  • Escherichia coli O157:H7 isolated from raw beef, soft cheese and vegetables in Lima (Peru). International Journal of Food Microbiology, 114: 204-210. Öksüz O., Arıcı M., Kurultay S. and Gümüş T. (2004) Incidence of Escherichia coli O157 in raw milk and white pickled cheese manufactured from raw milk in Turkey. Food Control, 15: 453-4
  • Quinto E.J. and Cepeda A. (1997) Incidence of toxigenic Escherichia coli in soft cheese made with raw or pasteurized milk. Letters in Applied Microbiology, 24: 291-295.
  • Ramsaran H., Chen J., Brunke B., Hill A. and Griffiths M.W. (1998). Survival of bioluminescent Listeria monocytogenes and Escherichia coli O157:H7 in soft cheeses. Journal of Dairy Science, 81: 1810-1817.
  • Reuben A., Treminio H., Arias M.L. and Villalobos L. (2002) Isolation of Escherichia coli O157:H7 from Costa Rican food. Revista Biomedica, 13: 273-2
  • Rey J., Sanchez S., Blanco J.E., De Mendoza J.H., De Mendoza M.H., Garcia A., Gil C., Tejero N., Rubio R. and Alonso J.M. (2006) Prevalence, serotypes and virulence genes of shiga toxin-producing Escherichia coli isolated from ovine and caprine milk and other dairy products in Spain. International Journal of Food Microbiology, 107: 212-217.
  • Scheutz F. and Strockbine N.A. (2005) Escherichia.
  • In: Garrity G.M. (ed.), Bergey’s manual of systematic bacteriology. (2nd Edn.), Springer, New York, pp: 607-623. Solomakos N., Govaris A., Angelidis A.S., Pournaras S., Burriel A.R., Kritas S.K. and Papageorgiou D.K. (2009) Occurrence, virulence genes and antibiotic resistance of Escherichia coli O157 isolated from raw bovine, caprine and ovine milk in Greece. Food Microbiology, 26: 8658
  • Tekinşen K.K. and Özdemir Z. (2006) Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese. Food Control, 17: 707-711.
  • Turantaş F., Ünlütürk A. and Göktan D. (1989) Microbiological and compositional status of Turkish White cheese. International Journal of Food Microbiology, 8: 19-24.
  • Upton P.A. and Coia J.E. (1994) Outbreaks of Escherichia coli O157 associated with pasteurised milk supply. Lancet, 344: 1015.
  • Vernozy-Rozand C., Mazuy-Cruchaudet C., Bavai C., Montet M.P., Bonin V., Dernburg A. and Richard Y. (2005) Growth and survival of Escherichia coli O157:H7 during the manufacture and ripening of raw goat milk lactic cheeses. International Journal of Food Microbiology, 105: 83-88.
  • Vivegnis J., El Lioui M., Leclercq A., Lambery B. and Decallonne J. (1999) Detection of Shiga-like toxin producing Escherichia coli from raw milk cheeses produced in Wallonia. Biotechnology, Agronomy, Society and Environment, 3: 1591
  • Vural A., Erkan M.E. and Güran H.Ş. (2010) The examination of the microbiological quality in Örgü cheese (Braided Cheese) samples. Kafkas
  • Universitesi Veteriner Fakültesi Dergisi, 16: 53Zadik P.M., Chapman P.A. and Siddons C. (1993)
  • Use of tellurite for the selection of Escherichia coli O157. Journal of Medical Microbiology, 39: 155-158.

Türk ev yapımı beyaz peynirlerde Escherichia coli O157’nin araştırılması

Year 2013, Volume: 72 Issue: 1, 45 - 51, 07.11.2013

Abstract

Verositotoksin üreten Escherichia coli (VTEC) gıda zehirlenmeleri gibi ciddi halk sağlığı risklerine neden olan önemli patojendir. Çiğ süt ile çiğ sütten ya da yeterli derecede pastörize edilmemiş sütten yapılan peynirler VTEC serotip E. coli O157 enfeksiyonları için potansiyel bir kaynak teşkil etmektedir. Bu çalışmada, kırsal kesimde üretilen toplam 245 adet Türk ev yapımı beyaz peynir örneği çeşitli açık halk pazarlarından toplanmıştır. Toplanan örnekler E. coli serotip O157’nin varlığı açısıdan araştırılmıştır. Sefiksim-tellürite (CT) ihtiva eden sorbitol MacConkey (CT-SMAC) besiyerinden sorbitolü fermente etmeyen toplam 21 koloni E. coli O157 varlığı açısından şüpheli izolat olarak tespit edildi. E. coli O157 varlığı açısından şüpheli izolatlar ticari E. coli O157 lateks aglütinasyon test kitine üreticinin talimatları doğrultusunda tabi tutuldu. Türk halkı tarafından sevilerek tüketilen toplam 245 Türk ev yapımı beyaz peynirin hiçbirinde E. coli O157 varlığı tayin edilmedi. Sonuç olarak, bu sevilen gıdada E. coli O157’nin yokluğu sevindirici bir tespittir. Bununla beraber, gıdalarda tüketici sağlığı için önemli bir gıda kaynaklı patojen olan E. coli O157:H7’nin varlığına yönelik titiz incelemenin gerçekleştirilmesi tavsiye edilir.

References

  • Akçamlı E. (2008) A study on the presence of enterohemorrhagic Escherichia coli O157:H7 in Blue cheese sold in public markets in Konya province. MSc. dissertation, University of Selçuk, Turkey.
  • Anonymous (1996) VTEC O157 infection in West Yorkshire associated with the consumption of raw milk. Commuicable Disease Report Weekly, 6: 1
  • Ansay S.E. and Kaspar C.W. (1997) Survey of retail cheeses, dairy processing environments and raw milk for Escherichia coli O157:H7. Letters in Applied Microbiology, 25: 131-134.
  • Aslantaş Ö. and Yıldız P. (2002) Isolation of Escherichia coli O157:H7 in animal originated foods in Kars region. Veteriner Bilimleri Dergisi, 18: 107-111.
  • Baz E., Gülmez M., Güven A., Sezer Ç. and Duman B. (2003) Examination of coliforms, E. coli and E. coli O157 in raw milk and ripened white cheese samples sold in Kars-Turkey. Kafkas
  • Universitesi Veteriner Fakültesi Dergisi, 9: 165-1 Bhunia A.K. (2008) Foodborne Microbial
  • Pathogens: Mechanisms and Pathogenesis. Springer, New York, USA. Caro I. and Garcia-Armesto M.R. (2007) Occurrence of Shiga toxin-producing Escherichia coli in a Spanish raw ewe’s milk cheese. International Journal of Food Microbiology, 116: 410-413.
  • Coia J.E., Johnston Y., Steers N.J. and Hanson M.F. (2001) A survey of the prevalence of Escherichia coli O157 in raw meats, raw cow’s milk and raw-milk cheeses in south-east Scotland. International Journal of Food Microbiology, 66: 63-69.
  • Dontorou C., Papadopoulou C., Filioussis G., Economou V., Apostolou I., Zakkas G., Salamoura A., Kansouzidou A. and Levidiotou S. (2003) Isolation of Escherichia coli O157:H7 from foods in Greece. International Journal of Food Microbiology, 82: 273-279.
  • Durch J., Ringhand T., Manner K., Proetor M., Davis J. and Boxrud D. (2000) Outbreak of
  • Escherichia coli O157:H7 infection associated with eating fresh cheese curds. Morbiditiy and Mortality Weekly Report, 49, 911–913. Erkan E.M., Çiftcioğlu G., Vural A. and Aksu H. (2007) Some microbiological characteristics of herbed cheeses. Journal of Food Quality, 30: 228-236.
  • Espie E., Vaillant V., Mariani-Kurkdjian P., Grimont F., Martin-Schaller R., De Valk H. and VernozyRozand C. (2006) Escherichia coli O157 outbreak associated with fresh unpasteurized goats’ cheese. Epidemiology and Infection, 134: 143-1
  • Ewing W.H. (1986) Differentiation of Enterobacteriaceae by biochemical reactions. In: Ewing W.H. (ed.), Edwards and Ewing identification of Enterobacteriaceae. (4th Edn.), Elsevier Science Publishing, New York, pp: 47Gonzalez A.G.M., Rosa A.C.P., Andrade J.R.C. and Tibana A. (2000) Enteropathogenicity markers in Escherichia coli strains isolated from soft white cheese and poultry in Rio de Janeiro, Brazil. Food Microbiolology, 17: 321-328.
  • Govaris A., Koidis P. and Papatheodorou K. (2001) The fate of Escherichia coli O157:H7 in Myzithra, Anthotyros, and Manouri whey cheeses during storage at 2 and 12 °C. Food Microbiolology, 18: 565-570.
  • Govaris A., Papageorgiou D.K. and Papatheodorou K. (2002) Behavior of Escherichia coli O157:H7 during the manufacture and ripening of Feta and Telemes cheeses. Journal of Food Protection, 65: 609-615.
  • Griffin P. and Tauxe R. (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic Escherichia coli and the associated hemolytic uremic syndrome. Epidemiologic Reviews, 13: 60-98.
  • Hancock D.D., Besser T.E., Kinsel M.L., Tarr P.I., Rice D.H. and Paros M.G. (1994) The prevalence of Escherichia coli O157:H7 in dairy and beef cattle in Washington State. Epidemiology and Infection, 113: 199-207.
  • Heuvelink A.E., Bleuminck B., Van den Biggelaar F.L., Te Giffel M.C., Beumer R.R. and De Boer E. (1998) Occurrence and survival of verocytotoxin-producing Escherichia coli O157 in raw cow’s milk in The Netherlands. Journal of Food Protection, 61: 1597-1601.
  • Honish L., Predy G., Hislop N., Chui L., Kowalevska-Grochowska K., Trottier L., Kreplin C. and Zazulak I. (2005) An outbreak E. coli O157:H7 hemorrhagic colitis associated with unpasteurized Gouda cheese. Canadian Journal of Public Health, 96: 182-184.
  • Ingham S.C., Su Y.C. and Spangenberg D.S. (2000) Survival of Salmonella typhimurium and Escherichia coli O157:H7 in cheese brines. International Journal of Food Microbiology, 61:73-79.
  • Jones D.L. (1999) Potential health risks associated with the persistence of Escherichia coli O157 in agricultural environments. Soil Use and Management, 15: 76-83.
  • Karch H., Bielaszewska M., Bitzan M. and Schmidt H. (1999) Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagnostic Microbiology and Infectious Disease, 34: 229-243.
  • Karmali M.A. (1989) Infection by verotoxinproducing Escherichia coli. Clinical
  • Microbiology Reviews, 2: 15-28. Mora A., Leon S.L., Blanco M., Blanco J.E., Lopez C., Dahbi G., Echeita A., Gonzalez E.A. and Blanco J. (2007) Phage types, virulence genes and PFGE profiles of Shiga-toxin-producing
  • Escherichia coli O157:H7 isolated from raw beef, soft cheese and vegetables in Lima (Peru). International Journal of Food Microbiology, 114: 204-210. Öksüz O., Arıcı M., Kurultay S. and Gümüş T. (2004) Incidence of Escherichia coli O157 in raw milk and white pickled cheese manufactured from raw milk in Turkey. Food Control, 15: 453-4
  • Quinto E.J. and Cepeda A. (1997) Incidence of toxigenic Escherichia coli in soft cheese made with raw or pasteurized milk. Letters in Applied Microbiology, 24: 291-295.
  • Ramsaran H., Chen J., Brunke B., Hill A. and Griffiths M.W. (1998). Survival of bioluminescent Listeria monocytogenes and Escherichia coli O157:H7 in soft cheeses. Journal of Dairy Science, 81: 1810-1817.
  • Reuben A., Treminio H., Arias M.L. and Villalobos L. (2002) Isolation of Escherichia coli O157:H7 from Costa Rican food. Revista Biomedica, 13: 273-2
  • Rey J., Sanchez S., Blanco J.E., De Mendoza J.H., De Mendoza M.H., Garcia A., Gil C., Tejero N., Rubio R. and Alonso J.M. (2006) Prevalence, serotypes and virulence genes of shiga toxin-producing Escherichia coli isolated from ovine and caprine milk and other dairy products in Spain. International Journal of Food Microbiology, 107: 212-217.
  • Scheutz F. and Strockbine N.A. (2005) Escherichia.
  • In: Garrity G.M. (ed.), Bergey’s manual of systematic bacteriology. (2nd Edn.), Springer, New York, pp: 607-623. Solomakos N., Govaris A., Angelidis A.S., Pournaras S., Burriel A.R., Kritas S.K. and Papageorgiou D.K. (2009) Occurrence, virulence genes and antibiotic resistance of Escherichia coli O157 isolated from raw bovine, caprine and ovine milk in Greece. Food Microbiology, 26: 8658
  • Tekinşen K.K. and Özdemir Z. (2006) Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese. Food Control, 17: 707-711.
  • Turantaş F., Ünlütürk A. and Göktan D. (1989) Microbiological and compositional status of Turkish White cheese. International Journal of Food Microbiology, 8: 19-24.
  • Upton P.A. and Coia J.E. (1994) Outbreaks of Escherichia coli O157 associated with pasteurised milk supply. Lancet, 344: 1015.
  • Vernozy-Rozand C., Mazuy-Cruchaudet C., Bavai C., Montet M.P., Bonin V., Dernburg A. and Richard Y. (2005) Growth and survival of Escherichia coli O157:H7 during the manufacture and ripening of raw goat milk lactic cheeses. International Journal of Food Microbiology, 105: 83-88.
  • Vivegnis J., El Lioui M., Leclercq A., Lambery B. and Decallonne J. (1999) Detection of Shiga-like toxin producing Escherichia coli from raw milk cheeses produced in Wallonia. Biotechnology, Agronomy, Society and Environment, 3: 1591
  • Vural A., Erkan M.E. and Güran H.Ş. (2010) The examination of the microbiological quality in Örgü cheese (Braided Cheese) samples. Kafkas
  • Universitesi Veteriner Fakültesi Dergisi, 16: 53Zadik P.M., Chapman P.A. and Siddons C. (1993)
  • Use of tellurite for the selection of Escherichia coli O157. Journal of Medical Microbiology, 39: 155-158.
There are 39 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Seza Arslan This is me

Fatma Özdemir This is me

Publication Date November 7, 2013
Submission Date November 7, 2013
Published in Issue Year 2013 Volume: 72 Issue: 1

Cite

AMA Arslan S, Özdemir F. Investigation of Escherichia coli O157 in Turkish homemade white cheese. Eur J Biol. November 2013;72(1):45-51.