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Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries

Year 2019, , 38 - 42, 25.03.2019
https://doi.org/10.32707/ercivet.538012

Abstract

Hepatitis A is transferred via fecal-oral route, direct contact from person to person or with ingestion of contaminated food. Foods like, raspberries, strawberries and blueberries are important source of hepatitis A virus (HAV). Frozen retail packaged raspberries are analyzed in this study. Frozen raspberry samples have were obtained from local supermarkets monthly between January and December 2015 in Ankara province, Turkey. The samples were evaluated for HAV contamination using ISO/TS 15216-1:2013 in duplicate and Mengovirus was used for process control. Samples that found to be contaminated with HAV were further analyzed for Enterobacteriaceae Coliform and Escherichia coli. Totally 240 samples were analyzed and 20 (8.33%) were found to be contaminated with HAV. The highest HAV prevalence was on 6th month (25%). On the contrary no HAV was found on 3rd, 4th and 10th months of analyzes. The highest Enterobacteriaceae, Coliform and E. coli counts were found on 2nd month 4.90, 4.84 and, 3.48 log10 cfu/g, respectively. The results indicate that even the food relies with the microbiological criteria, there is no guarantee for viral contamination. Additionally, high cost of virus analyzes is another barrier for routine control which has a direct impact on public health. Additional measures like HACCP, GHP and GMP should be applied strictly from farm to fork to avoid contamination with HAV. 

References

  • 1. Baert I, Debevere J, Uyttendaele M. The efficacy of preservation methods of inactivate food borne viruses. Int J Food Microbiol 2009; 131: 83-94. 2. Bidawid S, Farber JM, Sattar SA. Rapid concentration and detection of hepatitis A virus from lettuce and strawberries. J Virol Mehtods 2000a; 88: 175-85. 3. Bidawid S, Farber JM, Sattar SA. Contamination of foods by food handlers: Experiments on hepatitis A virus transfer to food and its interruption. Appl Environ Microbiol 2000b; 66 (7): 2759-63. 4. Blaise-Boisseau S, Hennechart-Colette C, Guillier L, Perelle S. Duplex real time qRT-PCR for the detection of hepatitis A virus in water and raspberries using the MS2 bacteriophage as a processcontrol. J Virol Methods 2010; 166: 48-53. 5. Butot S, Putallaz T, Amoroso R, Sanchez G. Inactivation on enteric viruses in minimally processed berries and herbs. Appl Environ Microbiol 2009; 75: 4155-61. 6. Butot S, Putallaz T, Sanchez G. Effects on sanitation, freezing and frozen storage on enteric viruses in berries and herbes. Int J Food Microbiol 2008; 126: 30-5. 7. Calder L, Simmons G, Thornley C, Taylor P, Pritchard K, Greening G, Bishop J. An outberak of hepatitis A associated with consumption of rawbleuberries. Epidemiol Infect 2003; 131: 745-51. 8. Croci L, de Medici D, Scalfaro C, Fiore A, Toti L. The survival of hepatitis A virus in fresh produce. Int J Food Microbiol 2002; 73: 29-34. 9. Deboosere N, Legeay O, Caudrelier Y, Lange M. Modelling effect of physical and chemical parameters on heat inactivation kinetics of hepatitis A virus in a fruit model system. Int J Food Microbiol 2004; 93: 73-85. 10. Deboosere N, Pinon A, Delobel A, Temmam S, Morin T, Merle G, Blaise-Boisseau S, Perelle S, Vialette M. A predictive microbiology approach for thermal inactivation of hepatitis A virus in acidified berries. Food Microbiol 2010; 27: 962-7. 11. European Commission (RASFF Portal). Available at: https://webgate.ec.europa.eu/rasff-window/portal/?event=searchResultList. Accessed: 14.05.2016. 12. Fitzgerald M, Thornton L, O’Gorman J, O’Connor L, Garvey P, Boland M, Part AM, Rogalska J, Coughlan H, MacDiarmada J, Heslin J, Canny M, Finnegan P, Moran J, O’Flanagan D; Hepatitis A Outbreak Control Team. Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013- linked to an international outbreak. Euro Surveill 2014; 19(43): 20942. 13. Gillesberg Lassen S, Soborg B, Midgley SE, Steen A, Vold L, Stene-Johansen K, Rimhanen-Finne R, Kontio M, Löfdahl M, Sundqvist L, Edelstein M, Jensen T, Vestergaard HT, Fischer TK, Molbak K, Ethelberg S. Ongoing multi-strain food-borne hepatitis A outbreak with frozen berries as suspected vehicle: four Nordic countries affected, October 2012 to April 2013. Euro Surveill 2013; 18(17): 20467. 14. Huang Y, Chen H. A novel water-assisted pulsed light processing for decontamination of blueberries. Food Microbiol 2014; 40: 1-8. 15. Hutin YJ, Pool V, Cramer EH, Nainan OV, Weth J, Williams IT, Goldstein ST, Gensheimer KF, Bell BP, Saphiro CN, Alter MJ, Margolis HS. A multistate, foodborne outbreak of hepatitis A. N Eng J Med 1999; 340(8): 595-602. 16. Ishii K, Kiyohara T, Yoshizaki S, Kawabata K, Kanayama A, Yahata Y, Takahashi T, Kinoshita H, Saitou T, Sunagawa T, Oishi K, Uema M, Noda M, Wakita T. Epidomiological and genetic analysis of a 2014 outbreak of hepatitis a in Japan. Vaccine 2015; 33: 6029-36. 17. International Organization for Standardization (ISO) 16649-2: 2001. Microbiology of food and animal feding stuffs – Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli -- Part 2: Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. 2001 18. International Organization for Standardization (ISO) 21528-2: 2004. Microbiology of food and animal feding stuffs—Horizontal methods for the detection and enumeration of Enterobacteriaceae--Part 2: Colony-count method. 2004 19. International Organization for Standardization (ISO) 4832: 2006. Microbiology of food and animal feding stuffs – Horizontal method for the enumeration of coliforms -- Colony-count technique. 2006 20. International Organization for Standardization/Turkish Standards (ISO/TS) 15216-1: 2013. Microbiology of food and animal feed—Horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR--Part 1: Method for quantification. 2013. 21. Koopmans M, Duizer E. Food borne viruses: an emerging problem. Int J Food Microbiol 2004; 90: 23-41. 22. Koopmans M, von Bonsdroff CH, Vinje J, de Medici D, Monroe S. Food borne viruses. FEMS Microbiol Rev 2002; 26: 187-205. 23. Martin-Latil S, Hennechart-Collette C, Gullier L, Perelle S. Comparison of two extraction methods for the detection of hepatitis A virus in semi-dried tomatoes and murine norovirus as a process control by duplex RT-qPCR. Food Microbiol 2012; 31: 246-53. 24. Morales-Rayas R, Wolffs PFG and Griffiths MW. Simultaneous separation and detection of hepatitis A virus and norovirus in produce. Int J Food Microbiol 2010; 139: 48-55. 25. Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse Hl. Food-borne diseases- the challenges of 20 years ago stil persist while new ones continue to emerge. Int J Food Microbiol 2010; 139: 3-15. 26. Nordic Outbreak Investigation Team. Joint analysis by the Nordic countries of hepatitis A outberak, October 2012 to June 2013: frozen strawberries suspected. Euro Surveill 2013; 18(17): 20520. 27. Papafragkou E, Plante M, Mattison K, Bidawid S, Karthikeyan K, Farber JM, Jaykus LA. Rapid and sensitive detection of hepatitis A virus in representative food matrices. J Virol Methods 2008; 147: 177-87. 28. Pebody RG, Leino T, Ruutu P, Kinnunen L, Davidkin I, Nohynek H, Leinikki P. Food borne outbreaks of hepatitis A in a low endemic country: an emerging problem?. Epidemiol Infect 1998; 120: 55-9. 29. Perrin A, Loutreul J, Boudaud N, Bertrand I, Gantzer C. Rapid, simple and efficient method for the detection on viral genomes on raspberries. J Virol Methods 2015; 224: 95-101. 30. Reid TMS, Robinson HG. Frozen raspberries and hepatitis A. Epidemiol Infect 1987; 98: 109-112. 31. Rzezutka A, D’Agostino M, Cook N. An ultracentrifugation-based approach to the detection of hepatitis A virus in soft fruits. Int J Food Microbiol 2005; 108: 315-320.

Dondurulmuş Ahududularda Hepatit A Virüs, Enterobacteriaceae, Koliform ve Escherichia coli Kontaminasyonunun Belirlenmesi

Year 2019, , 38 - 42, 25.03.2019
https://doi.org/10.32707/ercivet.538012

Abstract

 Hepatit A virüsü (HAV), genellikle fekal-oral yolla, kişiden kişiye direkt temas veya kontamine gıda ve suyun alınmasıyla bulaşmaktadır. Dondurulmuş ahududu, çilek ve yabanmersini gibi üzümsü meyveler kategorisinde yer alan ürünler, HAV kontaminasyonu açısından önemli kaynaklar arasında yer almaktadır. Bu çalışmada piyasada paketli olarak satılan dondurulmuş ahududu örnekleri kullanılmıştır. Dondurulmuş ahududu örnekleri, 2015 yılında Ankara’da bulunan marketlerden Ocak-Aralık ayları arasında her ay 20 tane olacak şekilde toplanmıştır. Çalışma konusunu oluşturan ahududu örneklerinde HAV analizi ISO/TS 15216-1:2013 uygun olacak şekilde iki paralel olarak yapılmıştır ve proses kontrolü için Mengovirüs kullanılmıştır. HAV pozitif bulunan örneklerde Enterobacteriaceae, Koliform bakteri ve E. coli sayımları gerçekleştirilmiştir. Toplam 240 adet ahududu örneğinin 20 adetinin (%8,33) HAV pozitif olduğu tespit edilmiştir. En yüksek prevalansın 6. ayda (%25) olduğu tespit edilirken, 3, 4 ve 10. aylarda alınan örneklerde ise HAV bulunmamıştır. En yüksek Enterobacteriaceae, koliform ve E. coli sayılarının 2. ayda olduğu ve bu ayda sırasıyla 4,90, 4,84 ve 3,48 log10 kob/g bakteri olduğu tespit edilmiştir. Bu sonuçlar gıdaların mikrobiyolojik kriterlere göre bakteriyel ajanlar bakımından yeterli koşulları sağlıyor olduğunu gösteriyor olmasına rağmen, viral etkenler bakımından herhangi bir garanti sağlamadığını göstermektedir. Ayrıca yüksek maliyetli virüs analizleri, halk sağlığı üzerinde doğrudan etkisi olan rutin kontrollerin yapılması için bir engel oluşturmaktadır. HACCP, GHP ve GMP gibi ilave önlemler, HAV ile bulaşmayı önlemek için kesinlikle çiftlikten çatala kadar uygulanmalıdır

References

  • 1. Baert I, Debevere J, Uyttendaele M. The efficacy of preservation methods of inactivate food borne viruses. Int J Food Microbiol 2009; 131: 83-94. 2. Bidawid S, Farber JM, Sattar SA. Rapid concentration and detection of hepatitis A virus from lettuce and strawberries. J Virol Mehtods 2000a; 88: 175-85. 3. Bidawid S, Farber JM, Sattar SA. Contamination of foods by food handlers: Experiments on hepatitis A virus transfer to food and its interruption. Appl Environ Microbiol 2000b; 66 (7): 2759-63. 4. Blaise-Boisseau S, Hennechart-Colette C, Guillier L, Perelle S. Duplex real time qRT-PCR for the detection of hepatitis A virus in water and raspberries using the MS2 bacteriophage as a processcontrol. J Virol Methods 2010; 166: 48-53. 5. Butot S, Putallaz T, Amoroso R, Sanchez G. Inactivation on enteric viruses in minimally processed berries and herbs. Appl Environ Microbiol 2009; 75: 4155-61. 6. Butot S, Putallaz T, Sanchez G. Effects on sanitation, freezing and frozen storage on enteric viruses in berries and herbes. Int J Food Microbiol 2008; 126: 30-5. 7. Calder L, Simmons G, Thornley C, Taylor P, Pritchard K, Greening G, Bishop J. An outberak of hepatitis A associated with consumption of rawbleuberries. Epidemiol Infect 2003; 131: 745-51. 8. Croci L, de Medici D, Scalfaro C, Fiore A, Toti L. The survival of hepatitis A virus in fresh produce. Int J Food Microbiol 2002; 73: 29-34. 9. Deboosere N, Legeay O, Caudrelier Y, Lange M. Modelling effect of physical and chemical parameters on heat inactivation kinetics of hepatitis A virus in a fruit model system. Int J Food Microbiol 2004; 93: 73-85. 10. Deboosere N, Pinon A, Delobel A, Temmam S, Morin T, Merle G, Blaise-Boisseau S, Perelle S, Vialette M. A predictive microbiology approach for thermal inactivation of hepatitis A virus in acidified berries. Food Microbiol 2010; 27: 962-7. 11. European Commission (RASFF Portal). Available at: https://webgate.ec.europa.eu/rasff-window/portal/?event=searchResultList. Accessed: 14.05.2016. 12. Fitzgerald M, Thornton L, O’Gorman J, O’Connor L, Garvey P, Boland M, Part AM, Rogalska J, Coughlan H, MacDiarmada J, Heslin J, Canny M, Finnegan P, Moran J, O’Flanagan D; Hepatitis A Outbreak Control Team. Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013- linked to an international outbreak. Euro Surveill 2014; 19(43): 20942. 13. Gillesberg Lassen S, Soborg B, Midgley SE, Steen A, Vold L, Stene-Johansen K, Rimhanen-Finne R, Kontio M, Löfdahl M, Sundqvist L, Edelstein M, Jensen T, Vestergaard HT, Fischer TK, Molbak K, Ethelberg S. Ongoing multi-strain food-borne hepatitis A outbreak with frozen berries as suspected vehicle: four Nordic countries affected, October 2012 to April 2013. Euro Surveill 2013; 18(17): 20467. 14. Huang Y, Chen H. A novel water-assisted pulsed light processing for decontamination of blueberries. Food Microbiol 2014; 40: 1-8. 15. Hutin YJ, Pool V, Cramer EH, Nainan OV, Weth J, Williams IT, Goldstein ST, Gensheimer KF, Bell BP, Saphiro CN, Alter MJ, Margolis HS. A multistate, foodborne outbreak of hepatitis A. N Eng J Med 1999; 340(8): 595-602. 16. Ishii K, Kiyohara T, Yoshizaki S, Kawabata K, Kanayama A, Yahata Y, Takahashi T, Kinoshita H, Saitou T, Sunagawa T, Oishi K, Uema M, Noda M, Wakita T. Epidomiological and genetic analysis of a 2014 outbreak of hepatitis a in Japan. Vaccine 2015; 33: 6029-36. 17. International Organization for Standardization (ISO) 16649-2: 2001. Microbiology of food and animal feding stuffs – Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli -- Part 2: Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. 2001 18. International Organization for Standardization (ISO) 21528-2: 2004. Microbiology of food and animal feding stuffs—Horizontal methods for the detection and enumeration of Enterobacteriaceae--Part 2: Colony-count method. 2004 19. International Organization for Standardization (ISO) 4832: 2006. Microbiology of food and animal feding stuffs – Horizontal method for the enumeration of coliforms -- Colony-count technique. 2006 20. International Organization for Standardization/Turkish Standards (ISO/TS) 15216-1: 2013. Microbiology of food and animal feed—Horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR--Part 1: Method for quantification. 2013. 21. Koopmans M, Duizer E. Food borne viruses: an emerging problem. Int J Food Microbiol 2004; 90: 23-41. 22. Koopmans M, von Bonsdroff CH, Vinje J, de Medici D, Monroe S. Food borne viruses. FEMS Microbiol Rev 2002; 26: 187-205. 23. Martin-Latil S, Hennechart-Collette C, Gullier L, Perelle S. Comparison of two extraction methods for the detection of hepatitis A virus in semi-dried tomatoes and murine norovirus as a process control by duplex RT-qPCR. Food Microbiol 2012; 31: 246-53. 24. Morales-Rayas R, Wolffs PFG and Griffiths MW. Simultaneous separation and detection of hepatitis A virus and norovirus in produce. Int J Food Microbiol 2010; 139: 48-55. 25. Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse Hl. Food-borne diseases- the challenges of 20 years ago stil persist while new ones continue to emerge. Int J Food Microbiol 2010; 139: 3-15. 26. Nordic Outbreak Investigation Team. Joint analysis by the Nordic countries of hepatitis A outberak, October 2012 to June 2013: frozen strawberries suspected. Euro Surveill 2013; 18(17): 20520. 27. Papafragkou E, Plante M, Mattison K, Bidawid S, Karthikeyan K, Farber JM, Jaykus LA. Rapid and sensitive detection of hepatitis A virus in representative food matrices. J Virol Methods 2008; 147: 177-87. 28. Pebody RG, Leino T, Ruutu P, Kinnunen L, Davidkin I, Nohynek H, Leinikki P. Food borne outbreaks of hepatitis A in a low endemic country: an emerging problem?. Epidemiol Infect 1998; 120: 55-9. 29. Perrin A, Loutreul J, Boudaud N, Bertrand I, Gantzer C. Rapid, simple and efficient method for the detection on viral genomes on raspberries. J Virol Methods 2015; 224: 95-101. 30. Reid TMS, Robinson HG. Frozen raspberries and hepatitis A. Epidemiol Infect 1987; 98: 109-112. 31. Rzezutka A, D’Agostino M, Cook N. An ultracentrifugation-based approach to the detection of hepatitis A virus in soft fruits. Int J Food Microbiol 2005; 108: 315-320.
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Details

Primary Language English
Journal Section Articles
Authors

Gökhan Kürşad Incılı 0000-0003-1178-3365

Publication Date March 25, 2019
Submission Date April 10, 2018
Acceptance Date August 2, 2018
Published in Issue Year 2019

Cite

APA Incılı, G. K. (2019). Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 16(1), 38-42. https://doi.org/10.32707/ercivet.538012
AMA Incılı GK. Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries. Erciyes Üniv Vet Fak Derg. March 2019;16(1):38-42. doi:10.32707/ercivet.538012
Chicago Incılı, Gökhan Kürşad. “Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia Coli Contamination of Frozen Raspberries”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16, no. 1 (March 2019): 38-42. https://doi.org/10.32707/ercivet.538012.
EndNote Incılı GK (March 1, 2019) Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16 1 38–42.
IEEE G. K. Incılı, “Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries”, Erciyes Üniv Vet Fak Derg, vol. 16, no. 1, pp. 38–42, 2019, doi: 10.32707/ercivet.538012.
ISNAD Incılı, Gökhan Kürşad. “Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia Coli Contamination of Frozen Raspberries”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16/1 (March 2019), 38-42. https://doi.org/10.32707/ercivet.538012.
JAMA Incılı GK. Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries. Erciyes Üniv Vet Fak Derg. 2019;16:38–42.
MLA Incılı, Gökhan Kürşad. “Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia Coli Contamination of Frozen Raspberries”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 16, no. 1, 2019, pp. 38-42, doi:10.32707/ercivet.538012.
Vancouver Incılı GK. Determination of Hepatitis A Virus, Enterobacteriaceae, Coliform and Escherichia coli Contamination of Frozen Raspberries. Erciyes Üniv Vet Fak Derg. 2019;16(1):38-42.