Abstract
The bactericidal efficacy of ultraviolet (UV) treatments to fruit juices is limited because of their low UV transmittance; therefore, it is necessary to design combined processes to improve their lethality. This investigation was carried out to determinate the lethal effect of UV-C treatments at mild temperatures (UV-H treatments) on the UV-resistant Escherichia coli strain Spanish Type Culture Collection (STCC) 4201 suspended in apple juice. A synergistic effect was observed and the optimum temperature for the combined process was established. Subsequently, the effect of the optimized treatment on the lethality of an E. coli cocktail (STCC 4201, STCC 471, American Type Culture Collection (ATCC) 27325, ATCC 25922, and O157:H7 Chapman strain) and on freshly squeezed apple juice quality was evaluated. A UV treatment of 20.33 J/mL reached 0.61 ± 0.01, 0.83 ± 0.07, 1.38 ± 0.04, 1.97 ± 0.06, 3.72 ± 0.14, 5.67 ± 0.61, and more than 6 log10 cycles of inactivation at 25.0, 40.0, 50.0, 52.5, 55.0, 57.5, and 60.0 °C, respectively. The optimum conditions for exploiting the synergistic effects were UV doses of 27.10 J/mL, temperature of 55.0 °C, and 3.58 min of treatment time. This treatment guaranteed more of 5 log10 reductions of the cocktail of five strains of E. coli without affecting pH, °Brix, and acidity of freshly squeezed apple juice. The UV-H treatment did not increase the loss of ascorbic acid compared to the same UV treatment at room temperature but approximately doubled the inactivation of polifenoloxidase.
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References
Adzahan, N. (2006). Effects of ultraviolet treatment on water soluble vitamin retention in aqueous model solutions and apple juice. PhD Thesis. Ithaca: Department of Food Technology, Cornell University.
Alonzo, G. (2012). Inactivation of Escherichia coli O157:H7 and spoilage yeasts in germicidal UV-C-irradiated and heat-treated clear apple juice. Food Control, 25(2), 425–432.
Álvarez, I., Mañas, P., Sala, F. J., & Condón, S. (2003). Inactivation of Salmonella enterica serovar enteritidis by ultrasonic waves under pressure at different water activities. Applied and Environmental Microbiology, 69(1), 668–672.
AOAC. (1990a). Acidity (as acid citric). Method 942.15B. Official methods of analysis of the Association of Official Analytical Chemists (15th ed.). Arlington: Association of Official Analytical Chemists.
AOAC. (1990b). Vitamin C (ascorbic acid). Method 967.21.Official methods of analysis of the Association of Official Analytical Chemists (15th ed.). Arlington: Association of Official Analytical Chemists.
Arroyo, C., Condón, S., & Pagán, R. (2009). Thermobacteriological characterization of Enterobacter sakazakii. International Journal of Food Microbiology, 136(1), 110–118.
Arroyo, C., Cebrián, G., Pagán, R., & Condón, S. (2011). Inactivation of Cronobacter sakazakii by ultrasonic waves under pressure in buffer and foods. International Journal of Food Microbiology, 144(3), 446–454.
Basaran, N., Quintero-Ramos, A., Moake, M. M., Churey, J. J., & Worobo, R. W. (2004). Influence of apple cultivars on inactivation of different strains of a Escherichia coli O157:H7 in apple cider by UV irradiation. Applied and Environmental Microbiology, 70(10), 6061–6065.
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(6), 637–645.
Chapman, P. A., Wright, D. J., Norman, P., Fox, J., & Crick, E. (1993). Cattle as a possible source of verocytotoxin-producing Escherichia coli O157 infections in man. Epidemiology and Infection, 111(3), 439–447.
Char, C. D., Mitilinaki, E., Guerrero, S. N., & Alzamora, S. M. (2010). Use of high-intensity ultrasound and UV-C light to inactivate some microorganisms in fruit juices. Food and Bioprocess Technology, 3(3), 797–803.
Choi, L. H., & Nielsen, S. S. (2005). The effect of thermal and non-thermal processing methods on apple cider quality and consumer acceptability. Journal of Food Quality, 28(1), 13–29.
Condón, S., Oria, R., & Trepat, F. J. S. (1987). Heat resistance of microorganisms: an improved method for survival counting. Journal of Microbiological Methods, 7(1), 37–44.
Condón, S., Arrizubieta, M., & Sala, F. J. (1993). Microbial heat resistance determinations by the multipoint system with the thermoresistometer TR-SC. Improvement of this methodology. Journal of Microbiological Methods, 18(4), 357–366.
Duffy, S., & Schaffner, D. W. (2001). Modeling the survival of Escherichia coli O157:H7 in apple cider using probability distribution functions. Journal of Food Protection, 64(5), 599–605
Enache, E., Maathusa, E. C., Elliott, P. H., Black, D. G., Chen, Y. H., Scott, V. N., et al. (2011). Thermal resistance parameters for shiga toxin-producing Escherichia coli in apple juice. Journal of Food Protection, 74(8), 1231–1237.
US Environmental Protection Agency (1997) Final report. A set of scientific issues being considered by the agency in connection with the efficacy testing issues concerning public health antimicrobial issues. Available at: www.epa.gov. Accessed 28 Jan 2012
Espina, L., Somolinos, M., Pagán, R., & García, D. (2010). Effect of citral on the thermal inactivation of Escherichia coli O157:H7 in citrate phosphate buffer and apple juice. Journal of Food Protection, 73(12), 2189–2196.
Falguera, V., Pagán, J., & Ibarz, A. (2011). Effect of UV irradiation on enzymatic activities and physicochemical properties of apple juices from different varieties. LWT–Food. Science and Technology, 44(1), 115–119.
Falguera, V., Pagán, J., Garza, S., Garvín, A., & Ibarz, A. (2012). Inactivation of polyphenol oxidase by ultraviolet irradiation: protective effect of melanins. Journal of Food Engineering, 110(2), 305–309.
Franz, C. M. A. P., Specht, I., Cho, G. S., Graef, V., & Stahl, M. R. (2009). UV-C-inactivation of microorganisms in naturally cloudy apple juice using novel inactivation equipment based on Dean vortex technology. Food Control, 20(12), 1103–1107.
Gachovska, T. K., Kumar, S., Thippareddi, H., Subbiah, J., & Williams, F. (2008). Ultraviolet and pulsed electric field treatments have additive effect on inactivation of E. coli in apple juice. Journal of Food Science, 73(9), M412–M417.
Gayán, E., Monfort, S., Álvarez, I., & Condón, S. (2011). UV-C inactivation of Escherichia coli at different temperatures. Innovative Food Science & Emerging Technologies, 12(4), 531–541.
Geeraerd, A. H., Herremans, C. H., & Van Impe, J. F. (2000). Structural model requirements to describe microbial inactivation during a mild heat treatment. International Journal of Food Microbiology, 59(3), 185–209.
Geeraerd, A. H., Valdramidis, V. P., & Van Impe, J. F. (2005). GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. International Journal of Food Microbiology, 102(1), 95–105.
Geveke, D. J. (2005). UV inactivation of bacteria in apple cider. Journal of Food Protection, 68(8), 1739–1742.
Geveke, D. J. (2008). UV inactivation of E. coli in liquid egg white. Food and Bioprocess Technology, 1(2), 201–206.
Guerrero-Beltrán, J. A., & Barbosa-Cánovas, G. V. (2004). Advantages and limitations on processing foods by UV light. Food Science and Technology International, 10(3), 137–147.
Gui, F., Wu, J., Chen, F., Liao, X., Hu, X., Zhang, Z., et al. (2006). Change of polyphenol oxidase activity, color, and browning degree during storage of cloudy apple juice treated by supercritical carbon dioxide. European Food Research and Technology, 223(3), 427–432.
Harm, W. (1980). Biological effects of ultraviolet radiation. Cambridge: Cambridge University Press.
Keyser, M., Muller. I., Cillier. P., Nel W., & Gouws, P. (2008). Ultraviolet radiation as a non-thermal treatment for the inactivation of microorganisms in fruit juice. Innovative Food Science & Emerging Technologies 9(3), 348–354.
Komthong, P., Igura, N., & Shimoda, M. (2007). Effect of ascorbic acid on the odours of cloudy apple juice. Food Chemistry, 100(4), 1342–1349.
Koutchma, T., Keller, S., Chirtel, S., & Parisi, B. (2004). Ultraviolet disinfection of juice products in laminar and turbulent flow reactors. Innovative Food Science & Emerging Technologies, 5(2), 179–189.
Koutchma, T., Paris, B., & Patazca, E. (2007). Validation of UV coiled tube reactor for fresh juices. Journal of Environmental Engineering and Science, 6(3), 319–328.
Koutchma, T., Forney, L. J., & Moraru, C. L. (2009). Ultraviolet light in food technology. Boca Raton: CRC.
Leistner, L. (1992). Food preservation by combined methods. Food Research International, 25(2), 151–158.
Liltved, H., & Cripps, S. J. (1999). Removal of particle-associated bacteria by prefiltration and ultraviolet irradiation. Aquaculture Research, 30(6), 445–450.
Manzocco, L., Quarta, B., & Dri, A. (2009). Polyphenoloxidase inactivation by light exposure in model systems and apple derivatives. Innovative Food Science & Emerging Technologies, 10(4), 506–511.
Mazzotta, A. S. (2001). Thermal inactivation of stationary-phase and acid-adapted Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in fruit juices. Journal of Food Protection, 64(3), 315–320.
Müller, A., Stahl, M. R., Graef, V., Franz, C. M. A. P., & Huch, M. (2011). UV-C treatment of juices to inactivate microorganisms using Dean vortex technology. Journal of Food Engineering, 107(2), 268–275.
Muñoz, A., Palgan, I., Noci, F., Morgan, D. J., Cronin, D. A., Whyte, P., et al. (2011). Combinations of high intensity light pulses and thermosonication for the inactivation of Escherichia coli in orange juice. Food Microbiology, 28(6), 1200–1204.
Ngadi, M., Smith, J. P., & Cayouette, B. (2003). Kinetics of ultraviolet light inactivation of Escherichia coli O157: H7 in liquid foods. Journal of the Science of Food and Agriculture, 8(15), 1551–1555.
Noci, F., Riener, J., Walkling-Ribeiro, M., Cronin, D. A., Morgan, D. J. & Lyng, J. G. (2008). Ultraviolet irradiation and pulsed electric fields (PEF) in a hurdle strategy for the preservation of fresh apple Juice. Journal of Food Engineering, 85(1), 141–146.
Oteiza, J. M., Giannuzzi, L., & Zaritzky, N. (2010). Ultraviolet treatment of orange juice to inactivate E. coli O157:H7 as affected by native microflora. Food and Bioprocess Technology, 3(4), 603–614.
Quintero-Ramos, A., Churey, J. J., Hartman, P., Barnard, J., & Worobo, R. W. (2004). Modeling of Escherichia coli inactivation by UV irradiation at different pH values in apple cider. Journal of Food Protection, 67(6), 1153–1156.
Raso, J., & Barbosa-Cánovas, G. V. (2003). Nonthermal preservation of foods using combined processing techniques. Critical Reviews in Food Science and Nutrition, 43(3), 265–285.
Raso, J., Pagán, R., Condón, S., & Sala, F. J. (1998). Influence of temperature and pressure on the lethality of ultrasound. Applied and Environmental Microbiology, 64(2), 465–471.
Seiji, M., & Iwashita, S. (1965). Enzyme inactivation by ultraviolet light and protective effect of melanin. Journal of Biochemistry, 57(3), 457–459.
Sizer, C. E., & Balasubramaniam, V. M. (1999). New intervention processes for minimally processed juices. Food Technology, 53(10), 64–67.
Splittstoesser, D. F., Mclellan, M. R., & Churey, J. J. (1996). Heat resistance of Escherichia coli O157:H7 in apple juice. Journal of Food Protection, 59(3), 226–229.
Tikekar, R. V., Anantheswaran, R. C., & Laborde, L. F. (2011). Ascorbic acid degradation in a model apple juice system and in apple juice during ultraviolet processing and storage. Journal of Food Science, 76(15), H62–H71.
Torkamani, A. E., & Niakousari, M. (2011). Impact of UV-C light on orange juice quality and shelf life. Food Research Journal, 18(4), 1265–1268.
Tran, M. T. T., & Farid, M. (2004). Ultraviolet treatment of orange juice. Innovative Food Science & Emerging Technologies, 5(4), 495–502.
Ukuku, D. O., & Geveke, D. J. (2010). A combined treatment of UV-light and radio frequency electric field for the inactivation of Escherichia coli K-12 in apple juice. International Journal of Food Microbiology, 138(1–2), 50–55.
Ülker-Yerlitürk, F., Arslan, O., Sinan, S., Gencer, N., & Özensoy, O. (2008). Characterization of polyphenol oxidase from wild pear (Pyrus elaegrifolia). Journal of Food Biochemistry, 32(3), 368–383.
Unluturk, S., Atilgan, M. R., Baysal, A. H., & Unluturk, M. S. (2010). Modeling inactivation kinetics of liquid egg white exposed to UV-C irradiation. International Journal of Food Microbiology, 142(3), 341–347.
US Food and Drug Administration. (2000). Irradiation in the production, processing and handling of food. Title 21, part 179. Federal register, 65. Washington: US Food and Drug Administration.
US Food and Drug Administration. (2001). Hazard analysis and critical control points (HACCP): final rule. Federal Register 66. Washington: US Food and Drug Administration.
Vojdani, J. D., Beuchat, L. R., & Tauxe, R. V. (2008). Juice-associated outbreaks of human illness in the United States, 1995 through 2005. Journal of Food Protection, 71(2), 356–364.
Walkling-Ribeiro, M., Noci, F., Cronin, D. A., Riener, J., Lyng, J. G., & Morgan, D. J. (2008). Reduction of Staphylococcus aureus and quality changes in apple juice processed by ultraviolet irradiation, pre-heating and pulsed electric fields. Journal of Food Engineering, 89(3), 267–273.
Webb, R. B., & Brown, M. S. (1976). Sensitivity of strains of Escherichia coli differing in repair capability to far UV, near UV and visible radiations. Photochemistry and Photobiology, 24(5), 425–432.
Wright, J. R., Sumner, S. S., Hackney, C. R., Pierson, M. D., & Zoecklein, B. W. (2000). Efficacy of ultraviolet light for reducing Escherichia coli O157:H7 in unpasteurized apple cider. Journal of Food Protection, 63(5), 563–567.
Acknowledgments
This study has been carried out with financial support from the Ministerio de Ciencia e Innovación de España, EU-FEDER (CIT020000-2009-40) and the Departamento de Ciencia, Tecnología y Universidad del Gobierno de Aragón. S. M., E. G. and M. J. S. gratefully acknowledge the financial support for their doctoral studies from the Ministerio de Educación y Ciencia de España.
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Gayán, E., Serrano, M.J., Monfort, S. et al. Pasteurization of Apple Juice Contaminated with Escherichia coli by a Combined UV–Mild Temperature Treatment. Food Bioprocess Technol 6, 3006–3016 (2013). https://doi.org/10.1007/s11947-012-0937-z
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DOI: https://doi.org/10.1007/s11947-012-0937-z