Abstract
This study investigated the effects of diverse doses (60–3600 mWs/cm2) of ultraviolet radiation (UV-C; 260 nm) on the inactivation of two types of foodborne viruses, the hepatitis A virus (HAV) and murine norovirus-1 (MNV-1; a human norovirus surrogate). Experimentally contaminated fresh chicken breasts were used as substrates, and the effects of UV-C radiation on the physicochemical properties and sensory qualities of chicken breasts were examined. MNV-1 and HAV titers significantly decreased (P < 0.05) when fresh chicken breasts were progressively irradiated with UV-C light. Over 1 log reduction in the titers of MNV-1 (1.23 log) and HAV (1.17 log) was detected when fresh chicken breasts were irradiated with 3600 mWs/cm2 of UV-C light. The calculated D-values for MNV-1 and HAV titers fell in the range of 3138.88–3428.57 and 2854.12–3076.92 mWs/cm2, respectively. Chicken breasts exposed to higher doses of UV-C radiation turned darker, exhibited more redness, and displayed prominent shades of yellow color. These changes strongly correlated with a decrease in the Hunter “L” values and an increase in the Hunter “a” and Hunter “b” values, respectively. This was also accompanied by an increase in the lipid peroxidation of the breast meat, which resulted in higher thiobarbituric acid reactive substance (TBARS) values. However, the UV-C radiation did not induce any pH changes into the food product. Chicken breasts treated with over 1800 mWs/cm2 of UV-C radiation displayed compromised sensory properties, whereas those treated with 60–1200 mWs/cm2 of UV-C witnessed satisfactory consumer acceptance. Therefore, the current study suggests that the use of the 600–1200 mWs/cm2 of UV-C radiation, in combination with other decontamination techniques (such as the hygienic processing of chicken breasts in well-sanitized processing plants), could be very effective in reducing more than 90 % (1 log) of the MNV-1 and HAV counts, without causing any deleterious changes to the physicochemical and sensory qualities of the meat surface.
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Avsaroglu, M. D., Buzrul, S., Alpas, H., Akcelik, M., & Bozoglu, F. (2006). Use of the Weibull model for lactococcal bacteriophage inactivation by high hydrostatic pressure. International Journal of Food Microbiology, 108, 78–83.
Bialka, K., Demirci, A., & Puri, V. M. (2008). Modeling the inactivation of Escherichia coli O157:H7 and Salmonella enterica on raspberries and strawberries resulting from exposure to ozone or pulsed UV-light. Journal of Food Engineering, 85, 444–449.
Bidawid, S., Farber, J. M., Sattar, S. A., & Hayward, S. (2000). Heat inactivation of hepatitis A virus in dairy foods. Journal Food Protection, 4, 522–528.
Bintsis, T., Litopoulou-Tzanetaki, E., & Robinson, R. K. (2000). Existing and potential applications of ultraviolet light in the food industry—a critical review. Journal of the Science of Food and Agriculture, 80, 637–645.
Blactchley, E. R., III, & Peel, M. M. (2001). Disinfection by ultraviolet irradiation. In S. S. Block (Ed.), Disinfection, sterilization, and preservation (5th ed.). Philadelphia, PA: Lea & Febiger.
Buege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310.
Butot, S., Putallaz, T., Amoroso, R., & Sanchez, G. (2009). Inactivation of enteric viruses in minimally processed berries and herbs. Applied and Environmental Microbiology, 75, 4155–4161.
Chouliara, E., Karatapanis, A., Savvaidis, I. N., & Kontomonas, M. G. (2007). Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4 °C. Food Microbiology, 24, 607–617.
Chun, H. H., Kim, J. Y., Lee, B. D., Yu, D. J., & Song, K. B. (2010a). Effect of UV-C irradiation on the inactivation of inoculated pathogens and quality of chicken breasts during storage. Food Control, 21, 276–280.
Chun, H. H., Kim, H. J., Won, M., Chung, K. S., & Song, K. B. (2010b). A comparison of kinetic models of foodborne pathogen inactivation by aqueous chlorine dioxide, fumaric acid, and ultraviolet-C. Journal of Applied Biological Chemistry, 53, 243–248.
Cook, A., Odumeru, J., Lee, S., & Pollari, F. (2012). Campylobacter, Salmonella, Listeria monocytogenes, verotoxigenic Escherichia coli, and Escherichia coli prevalence, enumeration, and subtypes on retail chicken breasts with and without skin. Journal of Food Protection, 75, 34–40.
Corrêa, A. A., Carratala, A., Baradi, C. R. M. B., Calvo, M., Girones, E., & Bofill-Mas, S. (2012). Comparative inactivation of murine norovirus, human adenovirus, and human JC polyomavirus by chlorine in seawater. Applied and Environmental Microbiology, 78, 6450–6457.
Cromeans, T., Sobsey, M. D., & Fields, H. A. (1987). Development of a plaque assay for a cytopathic, rapidly replicating isolate of hepatitis A virus. Journal of Medical Virology, 22, 45–56.
de Roda Husman, A. M., Bijkerk, P., Lodder, W., van den Burg, H., Pribil, W., Cabaj, A., Gehringer, P., Sommer, R., & Duizer, E. (2004). Calicivirus inactivation by nonionizing (253.7-nanometer-wavelenght [UV]) and ionizing (gamma) radiation. Applied and Environmental Microbiology, 70, 5089–5093.
de Souza, P. M., & Fernández, A. (2011). Effects of UV-C on physicochemical quality attributes and Salmonella enteritidis inactivation in liquid egg products. Food Control, 22, 1385–1392.
Donnan, E. J., Fielding, J. E., Gregory, J. E., Lalor, K., Rowe, S., Goldsmith, P., Antoniou, M., Fullerton, K. E., Knope, K., Copland, J. G., Bowden, D. S., Tracy, S. L., Hogg, G. G., Tan, A., Adamopoulos, J., Gaston, J., & Vally, H. (2012). A multistate outbreak of hepatitis A associated with semidried tomatoes in Australia, 2009. Clinical Infectious Disease, 54, 775–781.
Fellenberg, M. A., & Speisky, H. (2006). Antioxidants: their effects on broiler oxidative stress and its meat oxidative stability. World's Poultry Science Journal, 62, 53–70.
Fino, V. R., & Kniel, K. E. (2008). UV light inactivation of hepatitis A virus, aichi virus, and feline calicivirus on strawberries, green onions, and lettuce. Journal of Food Protection, 71, 908–913.
Fletcher, D. L. (1999). Broiler breast meat color variation, pH, and texture. Poultry Science, 78, 1323–1329.
Ha, J. H., Lee, Y. S., Na, B. J., Bae, D. D., & Ha, S. D. (2009). Effects of ultraviolet irradiation to reduce the numbers of food-borne pathogenic microorganisms on stainless steel chips. Journal of the Korean Society for Applied Biological Chemistry, 52, 301–304.
Heaton, J. C., & Jones, K. (2008). Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere—a review. Journal of Applied Microbiology, 104, 613–626.
Hong, Y. H., Ku, K. J., Kim, M. K., Won, M. S., Chung, K. S., & Song, K. B. (2008). Survival of Escherichia coli O157:H7 and Salmonella typhimurium inoculated on chicken by aqueous chlorine dioxide treatment. Journal of Microbiology and Biotechnology, 18, 742–745.
Hunter, R. S., & Harold, R. W. (1987). The Measurement of appearance (2nd ed.). New York, NY: Wiley Interscience Publication.
Isohanni, P. M., & Lyhs, U. (2009). Use of ultraviolet irradiation to reduce Campylobacter jejuni on broiler meat. Poultry Science, 88, 661–668.
Jean, J., Morales-Rayas, R., Anoman, M. N., & Lamhoujeb, S. (2011). Inactivation of hepatitis A virus and norovirus surrogate in suspension and on food-contact surfaces using pulsed UV light (pulsed light inactivation of food-borne viruses). Food Microbiology, 28, 568–572.
Karst, S. M., Wobus, C. E., Lay, M., Davidson, J., & Virgin, H. W., IV. (2003). STAT1-dependent innate immunity to a Norwalk-like virus. Science, 299, 1575–1578.
Kim, T., Silva, J., & Chen, T. (2002). Effects of UV irradiation on selected pathogens in peptone water and on stainless steel and chicken meat. Journal of Food Protection, 65, 1142–1145.
Kingsley, D. H., Holliman, D. R., Calci, K. R., Chen, H., & Flick, G. J. (2007). Inactivation of a norovirus by high-pressure processing. Applied Environmental Microbiology, 73, 581–585.
Ko, J. K., Ma, Y. H., & Song, K. B. (2005). Effect of chlorine dioxide treatment on microbial growth and qualities of chicken breast. Journal of Food Science and Nutrition, 10, 122–129.
Koopmans, M., & Duizer, E. (2004). Foodborne viruses: an emerging problem. International Journal of Food Microbiology, 90, 23–41.
Lebovka, N. I., & Vorobiev, E. (2004). On the origin of the deviation from the first-order kinetics in inactivation of microbial cells by pulsed electric fields. International Journal of Food Microbiology, 91, 83–89.
Lenes, D., Deboosere, N., Menard-Szczebara, F., Jossent, J., Alexandre, V., Machinal, C., & Vialette, M. (2010). Assessment of the removal and inactivation of influenza viruses H5N1 and H1N1 by drinking water treatment. Water Research, 44, 2473–2486.
Lyon, S. A., Fletcher, D. L., & Berrang, M. E. (2007). Germicidal ultraviolet light to lower numbers of Listeria monocytogenes on broiler breast fillets. Poultry Science, 86, 964–967.
Lynch, M. F., Tauxe, R. V., & Hedberg, C. W. (2009). The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiology and Infection, 137, 307–315.
Malek, M., Barzilay, E., Kramer, A., Camp, B., Jaykus, L. A., Escudero-Abarca, B., Derrick, G., White, P., Gerba, C., Higgins, C., Vinje, J., Glass, R., Lynch, M., & Widdowson, M. A. (2009). Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clinical Infectious Disease, 48, 31–37.
Noda, M., Fukuda, S., & Nishio, O. (2008). Statistical analysis of attack rate in norovirus foodborne outbreaks. International Journal of Food Microbiology, 122, 216–220.
Nwachuku, N., Gerba, C. P., Oswald, A., & Mashadi, F. D. (2005). Comparative inactivation of adenovirus serotypes by UV light disinfection. Applied and Environmental Microbiology, 71, 5633–5636.
Park, G. W., Linden, K. G., & Sobsey, M. D. (2011). Inactivation of murine norovirus, feline calicivirus and echo 12 as surrogates for human norovirus (NoV) and coliphage (F+) MS2 by ultraviolet light (254 nm) and the effect of cell association on UV inactivation. Letters in Applied Microbiology, 52, 162–167.
Praveen, C., Dancho, B. A., Kingsley, D. H., Calci, K. R., Meade, G. K., Mena, K. D., & Pillai, S. D. (2013). Susceptibility of murine norovirus and hepatitis A virus to electron beam irradiation in oysters and quantifying the reduction in potential infection risks. Applied and Environmental Microbiology, 79, 3796–3801.
Ray, B. (2000). Factor influencing microbial growth in food. In B. Ray (Ed.), Fundamental food microbiology (3rd ed.). Washington: CRC Press.
Renerre, M. (1990). Review : Factors involved in the discoloration of beef meat. International Journal of Food Science and Technology, 25, 613–630.
Robesyn, E., De Schrijver, K., Wollants, E., Top, G., Verbeeck, J., & Van Ranst, M. (2009). An outbreak of hepatitis A associated with the consumption of raw beef. Journal of Clinical Virology, 44, 207–210.
Rönnqvist, M., Mikkelä, A., Tuominen, P., Salo, S., & Maunula, L. (2014). Ultraviolet light Inactivation of murine morovirus and human norovirus GII: PCR may overestimate the persistence of noroviruses even when combined with pre-PCR treatments. Food and Environmental Virology, 6, 48–57.
Schmid, D., Stüger, H. P., Lederer, I., Pichler, A. M., Kainz-Arnfelser, G., Schreier, E., & Allerberger, F. (2007). A foodborne norovirus outbreak due to manually prepared salad, Austria 2006. Infection, 35, 232–239.
Siebenga, J. J., Vennema, H., Zheng, D. P., Vinje, J., Lee, B. E., Pang, X. L., Ho, E. C., Lim, W., Choudekar, A., Broor, S., Halperin, T., Rasool, N. B., Hewitt, J., Greening, G. E., Jin, M., Duan, Z. J., Lucero, Y., O'Ryan, M., Hoehne, M., Schreier, E., Ratcliff, R. M., White, P. A., Iritani, N., Reuter, G., & Koopmans, M. (2009). Norovirus illness is a global problem: emergence and spread of norovirus GII. 4 variants, 2001–2007. Journal of Infectious Diseases, 200, 802–812.
Smirnov, Y. M., Rodrigues-Molto, M., & Famada, M. (1983). Protein RNA interaction in encephalomyocarditis virus as revealed by UV light-induced covalent linkages. Journal of Virology, 45, 1048–1055.
Stermer, R. A., Lasater-Smith, M., & Brasington, C. F. (1987). Ultraviolet radiation—an effective bactericide for fresh meat. Journal of Food Protection, 50, 108–111.
Suzuki, H., & Yamamoto, S. (2009). Campylobacter contamination in retail poultry meats and by-products in the world: a literature survey. Journal of Veterinary Medical Science, 71, 255–261.
Turcios, R. M., Widdowson, M. A., Sulka, A. C., Mead, P. S., & Glass, R. I. (2006). Reevaluation of epidemiological criteria for identifying outbreaks of acute gastroenteritis due to norovirus : United States, 1998–2000. Clinical Infectious Diseases, 42, 964–969.
US Food and Drug Administration. (2007). Irradiation in the production, processing and handling of food: 21CFR. Part 179.39. Code of Federal Regulations, 3, 439–440.
Wallner-Pendleton, E. A., Sumner, S. S., Froning, G., & Stetson, L. (1994). The use of ultraviolet radiation to reduce Salmonella and psychrotrophic bacterial contamination on poultry carcasses. Poultry Science, 73, 1327–1333.
Wobus, C. E., Karst, S. M., Thackray, L. B., Chang, K. O., Sosnovtsev, S. V., Belliot, G., Krug, A., Mackenzie, J. M., Green, K. Y., & Virgin, H. W. (2004). Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biology, 2, 2076–2084.
Woods, J. W., & Burkhardt, W., III. (2010). Occurrence of norovirus and hepatitis A virus in US oysters. Food Environmental Virology, 2, 176–182.
Wright, A. C., Danyluk, M. D., & Otwell, W. S. (2009). Pathogens in raw foods: what the salad bar can learn from the raw bar. Current Opinion Biotechnology, 20, 172–177.
Acknowledgments
This research was supported by “Cooperative Research Program for Agriculture Science & Technology Development (Project No. 009221),” Rural Development Administration, Republic of Korea.
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Park, S.Y., Ha, SD. Ultraviolet-C Radiation on the Fresh Chicken Breast: Inactivation of Major Foodborne Viruses and Changes in Physicochemical and Sensory Qualities of Product. Food Bioprocess Technol 8, 895–906 (2015). https://doi.org/10.1007/s11947-014-1452-1
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DOI: https://doi.org/10.1007/s11947-014-1452-1