Food and Bioprocess Technology

, Volume 7, Issue 1, pp 1–20 | Cite as

Biological Aspects in Food Preservation by Ultraviolet Light: a Review

Review
First Online:
Received:
Accepted:

Abstract

The potential to commercialize nonthermal ultraviolet (UV) light technologies as new methods for preserving food products has caught the attention of a food industry that wishes to fulfill consumers' demands for fresh products. Numerous investigations have demonstrated UV light's ability to inactivate a wide range of microorganisms. However, the lack of UV sensitivity data from pathogenic and spoilage bacteria is evident. In addition, the main factors associated with UV light in terms of microbial lethality remain unclear. This review surveys critical factors (process, microbial, and environmental parameters) that determine UV microbial resistance and assess the effects of such factors on the inactivation mechanism and repair pathway efficiency. The effects of some of these factors, such as prior sublethal stresses and post-recovery conditions of UV treatments, may extensively improve the damage repair capacity and thus microbial survivability. Further research is needed to establish adequate control measures pre- and post-UV treatments. Furthermore, the possibility of combining UV light with conventional preservatives and other nonthermal technologies was assessed. The combination of UV light with mild heating or oxidant compounds could offer promising treatments to enhance the safety and stability of minimally processed foods.

Keywords

UV light Bacteria inactivation DNA repair Sub-lethal stress Combined processes 

Abbreviations

6-4PP

Pyrimidine 6–4 pyrimidone photoproduct

8-oxodGuo

8-Oxo-7,8-dihydro-2′-deoxyguanosine

AOP

Advanced oxidation processes

BER

Base excision repair

CPD

Cyclobutan pyrimidine dimer

DewPP

Dewar valence isomers

DSB

Double-strand break

HS

Heat shock

HSP

Heat shock proteins

IR

Infrared radiation

LHR

Liquid holding recovery

LP

Low-pressure mercury vapor lamps

MM

Minimal medium

MP

Medium-pressure mercury vapor lamps

NER

Nucleotide excision repair

ppGpp

Guanosine 5′-diphosphate 3′-diphosphate

PRR

Post-replication repair

PUV

Pulsed UV lamp

PX

Pulsed xenon lamp

RAMER

RecA-mediated excision repair

ROS

Reactive oxygen species

SP

Spore photoproduct

SSB

Single-strand break

TLS

Translesion DNA synthesis

This is a preview of subscription content, log in to check access.

Notes

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. E. G. gratefully acknowledges the financial support for her doctoral studies from the Ministerio de Educación y Ciencia de España.

References

  1. Abshire, R. L., & Dunton, H. (1981). Resistance of selected strains of Pseudomonas-aeruginosa to low-intensity ultraviolet-radiation. Applied and Environmental Microbiology, 41(6), 1419–1423.Google Scholar
  2. Arroyo, C., Cebrián, G., Condón, S., & Pagán, R. (2012a). Development of resistance in Cronobacter sakazakii ATCC 29544 to thermal and nonthermal processes after exposure to stressing environmental conditions. Journal of Applied Microbiology, 112(3), 561–570.Google Scholar
  3. Arroyo, C., Gayán, E., Pagán, R., & Condón, S. (2012b). UV-C inactivation of Cronobacter sakazakii. Foodborne Pathogens and Disease, 9(10), 907–914.Google Scholar
  4. Asad, L., Dealmeida, C. E. B., Dasilva, A. B., Asad, N. R., & Leitao, A. C. (1994). Hydrogen-peroxide induces the repair of UV-damaged DNA in Escherichia-coli—a LexA-independent but UvrA-dependent and RecA-dependent mechanism. Current Microbiology, 29(5), 291–294.Google Scholar
  5. Beauchamp, S., & Lacroix, M. (2012). Resistance of the genome of Escherichia coli and Listeria monocytogenes to irradiation evaluated by the induction of cyclobutane pyrimidine dimers and 6–4 photoproducts using gamma and UV-C radiations. Radiation Physics and Chemistry, 81(8), 1193–1197.Google Scholar
  6. Berney, M., Weilenmann, H. U., Ihssen, J., Bassin, C., & Egli, T. (2006). Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Applied and Environmental Microbiology, 72(4), 2586–2593.Google Scholar
  7. Bhatnagar, D. (1992). Photoprotection of ultraviolet light irradiated E. coli B/r cells. Indian Journal of Pathology & Microbiology, 35(3), 247–250.Google Scholar
  8. Bichara, M., Pinet, I., Lambert, L. B., & Fuchs, R. P. P. (2007). RecA-mediated excision repair: a novel mechanism for repairing DNA lesions at sites of arrested DNA synthesis. Molecular Microbiology, 65(1), 218–229.Google Scholar
  9. Bichara, M., Meier, M., Wagner, J., Cordonnier, A., & Lambert, I. B. (2011). Postreplication repair mechanisms in the presence of DNA adducts in Escherichia coli. Mutation Research-Reviews in Mutation Research, 727(3), 104–122.Google Scholar
  10. Blasius, M., Sommer, S., & Hubscher, U. (2008). Deinococcus radiodurans: what belongs to the survival kit? Critical reviews in biochemistry and molecular biology, 43(3), 221–238.Google Scholar
  11. Bohrerova, Z., & Linden, K. G. (2007). Standardizing photoreactivation: comparison of DNA photorepair rate in Escherichia coli using four different fluorescent lamps. Water Research, 41(12), 2832–2838.Google Scholar
  12. Bradley, D., McNeil, B., Laffey, J. G., & Rowan, N. J. (2012). Studies on the pathogenesis and survival of different culture forms of Listeria monocytogenes to pulsed UV-light irradiation after exposure to mild-food processing stresses. Food Microbiology, 30(2), 330–339.Google Scholar
  13. Bronk, B. V., & Walbridge, D. G. (1980). Sensitivity to ultraviolet-radiation as a function of DNA content in Escherichia-coli B-R. Biophysical Journal, 31(3), 381–392.Google Scholar
  14. Bucheli-Witschel, M., Bassin, C., & Egli, T. (2010). UV-C inactivation in Escherichia coli is affected by growth conditions preceding irradiation, in particular by the specific growth rate. Journal of Applied Microbiology, 109(5), 1733–1744.Google Scholar
  15. Burke, R. M., Upton, M. E., & McLoughlin, A. J. (1990). Influence of pigment production on resistance to ultraviolet-irradiation in Pseudomonas-aeuriginosa ATCC 10145. Irish Journal of Food Science and Technology, 14(1), 51–60.Google Scholar
  16. Casadei, M. A., Mañas, P., Niven, G., Needs, E., & Mackey, B. M. (2002). Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Applied and Environmental Microbiology, 68(12), 5965–5972.Google Scholar
  17. Cairns, B. (2006). UV dose required to achieve incremental log inactivation of bacteria, protozoa and viruses. IUVA News, 8(1), 38–45.Google Scholar
  18. Chan, Y. Y., & Killick, E. G. (1995). The effect of salinity, light and temperature in a disposal environment on the recocery of Escherichia-coli following exposure to ultraviolet-radiation. Water Research, 29(5), 1373–1377.Google Scholar
  19. Chang, J. C. H., Ossoff, S. F., Lobe, D. C., Dorfman, M. H., Dumais, C. M., Qualls, R. G., & Johnson, J. D. (1985). UV inactivation of pathogenic and indicator microorganisms. Applied and Environmental Microbiology, 49(6), 1361–1365.Google Scholar
  20. 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(6), 797–803.Google Scholar
  21. Cheigh, C.-I., Park, M.-H., Chung, M.-S., Shin, J. K., & Park, Y.-S. (2012). Comparison of intense pulsed light- and ultraviolet (UVC)-induced cell damage in Listeria monocytogenes and Escherichia coli O157:H7. Food Control, 25(2), 654–659.Google Scholar
  22. Child, M., Strike, P., Pickup, R., & Edwards, C. (2002). Salmonella typhimurium displays cyclical patterns of sensitivity to UV-C killing during prolonged incubation in the stationary phase of growth. Fems Microbiology Letters, 213(1), 81–85.Google Scholar
  23. Courcelle, J., Crowley, D. J., & Hanawalt, P. C. (1999). Recovery of DNA replication in UV-irradiated Escherichia coli requires both excision repair and RecF protein function. Journal of Bacteriology, 181(3), 916–922.Google Scholar
  24. Demirci, A., & Krishnamurthy, K. (2011). Pulsed UV light. In H. Q. Zhang, G. V. Barbosa-Cánovas, V. M. Balasubramaniam, C. P. Dunne, D. F. Farkas, & J. T. C. Yuan (Eds.), Nonthermal processing technologies for food (pp. 249–261). New Jesey: Wiley-Blackwell.Google Scholar
  25. Dicapua, E., Ruigrok, R. W. H., & Timmins, P. A. (1990). Activation of RecA protein—the salt-induced structural transition. Journal of Structural Biology, 104(1–3), 91–96.Google Scholar
  26. Douki, T., Reynaud-Angelin, A., Cadet, J., & Sge, E. (2003). Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. Biochemistry, 42(30), 9221–9226.Google Scholar
  27. Douki, T., Setlow, B., & Setlow, P. (2005). Effects of the binding of alpha/beta-type small, acid-soluble spore proteins on the photochemistry of DNA in spores of Bacillus subtilis and in vitro. Photochemistry and Photobiology, 81(1), 163–169.Google Scholar
  28. Dri, A. M., & Moreau, P. L. (1993). Phosphate starvation and low-temperature as ultraviolet-irradiation transcriptionally induce the Escherichia-coli LexA-controlled gene sfiA. Molecular Microbiology, 8(4), 697–706.Google Scholar
  29. Dykhuizen, D. E. (1999). Experimental studies of natural selection in bacteria. Annual Review of Ecology, Evolution, and Systematics, 21, 373–398.Google Scholar
  30. Eiberger, W., Volkmer, B., Amouroux, R., Dherin, C., Radicella, J. P., & Epe, B. (2008). Oxidative stress impairs the repair of oxidative DNA base modifications in human skin fibroblasts and melanoma cells. DNA Repair, 7(6), 912–921.Google Scholar
  31. Eischeid, A. C., & Linden, K. G. (2007). Efficiency of pyrimidine dimer formation in Escherichia coli across UV wavelengths. Journal of Applied Microbiology, 103(5), 1650–1656.Google Scholar
  32. Farrell, H. P., Garvey, M., Cormican, M., Laffey, J. G., & Rowan, N. J. (2010). Investigation of critical inter-related factors affecting the efficacy of pulsed light for inactivating clinically relevant bacterial pathogens. Journal of Applied Microbiology, 108(5), 1494–1508.Google Scholar
  33. Fine, F., & Gervais, P. (2004). Efficiency of pulsed UV light for microbial decontamination of food powders. Journal of Food Protection, 67(4), 787–792.Google Scholar
  34. Fitt, P. S., & Sharma, N. (1991). Starvation as an inducer of error-free DNA-repair in Escherichia-coli. Mutation Research, 262(2), 145–150.Google Scholar
  35. Fonseca, J. M., & Rushing, J. W. (2006). Effect of ultraviolet-C light on quality and microbial population of fresh-cut watermelon. Postharvest Biology and Technology, 40(3), 256–261.Google Scholar
  36. Foster, P. L. (2007). Stress-induced mutagenesis in bacteria. Critical Reviews in Biochemistry and Molecular Biology, 42(5), 373–397.Google Scholar
  37. 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.Google Scholar
  38. Fredericks, I. N., du Toit, M., & Krügel, M. (2011). Efficacy of ultraviolet radiation as an alternative technology to inactivate microorganisms in grape juices and wines. Food Microbiology, 28(3), 510–517.Google Scholar
  39. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (Eds.). (2006). DNA repair and mutagenesis. Washington: ASN.Google Scholar
  40. Gabriel, A., & Nakano, H. (2009). Inactivation of Salmonella. E. coli and Listeria monocytogenes in phosphate-buffered saline and apple juice by ultraviolet and heat treatments. Food Control, 20(4), 443–446.Google Scholar
  41. Gabriel, A. (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.Google Scholar
  42. 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.Google Scholar
  43. Ganesan, A. K., & Smith, K. C. (1968). Recovery of recombination deficient mutants of Escherichia coli K-12 from ultraviolet irradiation. Cold Spring Harbor Symposia on Quantitative Biology, 33, 235–242.Google Scholar
  44. 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.Google Scholar
  45. Gayán, E., Serrano, M. J., Raso, J., Álvarez, I., & Condón, S. (2012a). Inactivation of Salmonella enterica by UV-C light alone and in combination with mild temperatures. Applied and Environmental Microbiology, 78(23), 8353–8361.Google Scholar
  46. Gayán, E., Serrano, M. J., Monfort, S., Álvarez, I., & Condón, S. (2012b). Combining ultraviolet light and mild temperatures for the inactivation of Escherichia coli in orange juice. Journal of Food Engineering, 113(4), 598–605.Google Scholar
  47. Gayán, E., Mañas, P., Álvarez, & Condón, S. (2013). Mechanism of the synergistic inactivation of E. coli by UV-C light at mild temperatures. Applied and Environmental Microbiology, 79(14), 4465–4473. doi: 10.1128/AEM.00623-13.Google Scholar
  48. Gehr, R., & Wright, H. (1998). UV disinfection of wastewater coagulated with ferric chloride: recalcitrance and fouling problems. Water Science and Technology, 38(3), 15–23.Google Scholar
  49. Gentner, N. E., & Werner, M. M. (1978). Synergistic interaction between UV and ionizing-radiation in wild-type Schizosaccharomyces-pombe. Molecular & General Genetics, 164(1), 31–37.Google Scholar
  50. Girard, P. M., Francesconi, S., Pozzebon, M., Graindorge, D., Rochette, P., Drouin, R., & Sage, E. (2011). UVA-induced damage to DNA and proteins: direct versus indirect photochemical processes. Journal of Physics: Conference Series, 261, 012022.Google Scholar
  51. Goodson, M., & Rowbury, R. J. (1990). Habituation to alkali and increased UV-resistance in DNA repair-deficient strains of Escherichia coli grown at pH 9.0. Letters in Applied Microbiology, 11(3), 123–125.Google Scholar
  52. Görner, H. (1994). Photochemistry of DNA and related biomolecules—quantum yields and consequences of photoionization. Journal of Photochemistry and Photobiology B-Biology, 26(2), 117–139.Google Scholar
  53. Guerrero-Beltrán, J. A., & Barbosa-Cánovas, G. (2006). Reduction of Saccharomyces cerevisae, Escherichia coli and Listeria innocua in apple juice by ultraviolet light. Journal of Food Engineering, 28, 437–452.Google Scholar
  54. Guo, M., Hu, H., Bolton, J. R., & El-Din, M. G. (2009). Comparison of low- and medium-pressure ultraviolet lamps: photoreactivation of Escherichia coli and total coliforms in secondary effluents of municipal wastewater treatment plants. Water Research, 43(3), 815–821.Google Scholar
  55. Ha, J. H., & Ha, S. D. (2010). Synergistic effects of ethanol and UV radiation to reduce levels of selected foodborne pathogenic bacteria. Journal of Food Protection, 73(3), 556–561.Google Scholar
  56. Hallmich, C., & Gehr, R. (2010). Effect of pre- and post-UV disinfection conditions on photoreactivation of fecal coliforms in wastewater effluents. Water Research, 44(9), 2885–2893.Google Scholar
  57. Hartke, A., Bouche, S., Laplace, J. M., Benachour, A., Boutibonnes, P., & Auffray, Y. (1995). UV-inducible proteins and UV-induced cross-protection against acid, ethanol, H2O2 or heat-treatments in Lactococcus lactis subsp lactis. Archives of Microbiology, 163(5), 329–336.Google Scholar
  58. Hassen, A., Mahrouk, M., Ouzari, H., Cherif, M., Boudabous, A., & Damelincourt, J. J. (2000). UV disinfection of treated wastewater in a large-scale pilot plant and inactivation of selected bacteria in a laboratory UV device. Bioresource Technology, 74(2), 141–150.Google Scholar
  59. Hijnen, W. A. M., Beerendonk, E. F., & Medema, G. J. (2006). Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Research, 40(1), 3–22.Google Scholar
  60. Ihssen, J., & Egli, T. (2004). Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology, 150(6), 1637–1648.Google Scholar
  61. Jacobs, A. L., & Schaer, P. (2012). DNA glycosylases: in DNA repair and beyond. Chromosoma, 121(1), 1–20.Google Scholar
  62. Janion, C. (2008). Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli. International Journal of Biological Sciences, 4(6), 338–344.Google Scholar
  63. Jeevan, J., & Ghosh, A. (1995). Induction of heat-shock response in Vibrio-cholerae. Microbiology-UK, 141(9), 2101–2109.Google Scholar
  64. Jung, Y. J., Oh, B. S., & Kang, J.-W. (2008). Synergistic effect of sequential or combined use of ozone and UV radiation for the disinfection of Bacillus subtilis spores. Water Research, 42(6–7), 1613–1621.Google Scholar
  65. Kashimada, K., Kamiko, N., Yamamoto, K., & Ohgaki, S. (1996). Assessment of photoreactivation following ultraviolet light disinfection. Water Science and Technology, 33(10–11), 261–269.Google Scholar
  66. Khaneja, R., Perez-Fons, L., Fakhry, S., Baccigalupi, L., Steiger, S., To, E., Sandmann, G., Dong, T. C., Ricca, E., Fraser, P. D., & Cutting, S. M. (2010). Carotenoids found in Bacillus. Journal of Applied Microbiology, 108(6), 1889–1902.Google Scholar
  67. Koehler, D. R., Courcelle, J., & Hanawalt, P. C. (1996). Kinetics of pyrimidine(6–4)pyrimidone photoproduct repair in Escherichia coli. Journal of Bacteriology, 178(5), 1347–1350.Google Scholar
  68. Koivunen, J., & Heinonen-Tanski, H. (2005). Inactivation of enteric microorganisms with chemical disinfectants, UV irradiation and combined chemical/UV treatments. Water Research, 39(8), 1519–1526.Google Scholar
  69. Koutchma, T., Forney, L. J., & Moraru, C. L. (Eds.). (2009). Ultraviolet light in food technology. Boca Raton: CRC.Google Scholar
  70. Kowalski, W. (Ed.). (2009). Ultraviolet germicidal irradiation handbook. UVGI for air and surface disinfection. New York: Springer.Google Scholar
  71. Krueger, J. H., & Walker, G. C. (1984). groEL and dnaK genes of Escherichia-coli are induced by UV irradiation and nalixilic-acid in an htpr + −dependent fashion. Proceeding of the National Academy of Sciences of the United States of America-Biological Sciences, 81(5), 1499–1503.Google Scholar
  72. Lage, C., Teixeira, P. C. N., & Leitao, A. C. (2000). Non-coherent visible and infrared radiation increase survival to UV (254 nm) in Escherichia coli K12. Journal of Photochemistry and Photobiology, B: Biology, 54(1), 155–161.Google Scholar
  73. Layton, J. C., & Foster, P. L. (2005). Error-prone DNA polymerase IV is regulated by the heat shock chaperone GroE in Escherichia coli. Journal of Bacteriology, 187(2), 449–457.Google Scholar
  74. Liltved, H., & Landfald, B. (1996). Influence of liquid holding recovery and photoreactivation on survival of ultraviolet-irradiated fish pathogenic bacteria. Water Research, 30(5), 1109–1114.Google Scholar
  75. Lin, C. L. G., Kovalsky, O., & Grossman, L. (1997). DNA damage-dependent recruitment of nucleotide excision repair and transcription proteins to Escherichia coli inner membranes. Nucleic Acids Research, 25(15), 3151–3158.Google Scholar
  76. Lindenauer, K. G., & Darby, J. L. (1994). Ultraviolet disinfection of waste-water—effect of dose on subsequent photoreactivation. Water research, 28(4), 805–817.Google Scholar
  77. Little, J. W. (1991). Mechanism of specific LexA cleavage—autodigestion and the role of RecA coprotease. Biochimie, 73(4), 411–422.Google Scholar
  78. López-Malo, A., & Palou, E. (2005). Ultraviolet light and food preservation. In G. V. Barbosa-Cánovas, M. S. Tapia, & M. P. Cano (Eds.), Novel food processing technologies (pp. 405–421). Madrid: CRC.Google Scholar
  79. Lu, G., Li, C., & Liu, P. (2011). UV inactivation of milk-related microorganisms with a novel electrodeless lamp apparatus. European Food Research and Technology, 233(1), 79–87.Google Scholar
  80. Maclean M, Murdoch LE, Lani MN, MacGregor SJ, Anderson JG & Woolsey GA (2008c) Photoinactivation and photoreactivation responses by bacterial pathogens after exposure to pulsed UV-light. In: IEEE international power modulators and high voltage conference, Proceedings of the 2008, May 2008, Las Vegas.Google Scholar
  81. Mamane-Gravetz, H., & Linden, K. G. (2005). Relationship between physiochemical properties, aggregation and u.v. inactivation of isolated indigenous spores in water. Journal of Applied Microbiology, 98(2), 351–363.Google Scholar
  82. Massier, S., Rince, A., Maillot, O., Feuilloley, M. G. J., Orange, N., & Chevalier, S. (2012). Adaptation of Pseudomonas aeruginosa to a pulsed light-induced stress. Journal of Applied Microbiology, 112(3), 502–511.Google Scholar
  83. Matallana-Surget, S., Douki, T., Meador, J. A., Cavicchioli, R., & Joux, F. (2010). Influence of growth temperature and starvation state on survival and DNA damage induction in the marine bacterium Sphingopyxis alaskensis exposed to UV radiation. Journal of Photochemistry and Photobiology, B: Biology, 100(2), 51–56.Google Scholar
  84. McKinney, J. M., Williams, R. C., Boardman, G. D., Eifert, J. D., & Sumner, S. S. (2009). Effect of acid stress, antibiotic resistance, and heat shock on the resistance of Listeria monocytogenes to UV light when suspended in distilled water and fresh brine. Journal of Food Protection, 72(8), 1634–1640.Google Scholar
  85. Moeller, R., Horneck, G., Facius, R., & Sstackebrandt, E. (2005). Role of pigmentation in protecting Bacillus sp endospores against environmental UV radiation. Fems Microbiology Ecology, 51(2), 231–236.Google Scholar
  86. Moeller, R. T., Douki, T., Cadet, J., Stackebrandt, E., Nicholson, W. L., Rettberg, P., Reitz, G., & Horneck, G. (2007). UV-radiation-induced formation of DNA bipyrimidine photoproducts in Bacillus subtilis endospores and their repair during germination. International Microbiology, 10(1), 39–46.Google Scholar
  87. 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.Google Scholar
  88. Nair, S., & Finkel, S. E. (2004). Dps protects cells against multiple stresses during stationary phase. Journal of Bacteriology, 186(13), 4192–4198.Google Scholar
  89. Nicholson, W. L., & Law, J. F. (1999). Method for purification of bacterial endospores from soils: UV resistance of natural Sonoran desert soil populations of Bacillus spp. with reference to B. subtilis strain 168. Journal of Microbiological Methods, 35(1), 13–21.Google Scholar
  90. Oguma, K., Katayama, H., & Ohgaki, S. (2002). Photoreactivation of Escherichia coli after low- or medium-pressure UV disinfection determined by an endonuclease sensitive site assay. Applied and Environmental Microbiology, 68(12), 6029–6035.Google Scholar
  91. Oguma, K., Katayama, H., & Ohgaki, S. (2004). Photoreactivation of Legionella pneumophila after inactivation by low- or medium-pressure ultraviolet lamp. Water Research, 38(10), 2757–2763.Google Scholar
  92. 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.Google Scholar
  93. Pardasani, D., & Fitt, P. S. (1989). Strain-dependent induction by heat-shock of resistance to ultraviolet-light in Escherichia-coli. Current Microbiology, 18(2), 99–103.Google Scholar
  94. Pattison, D. I., & Davies, M. J. (2006). Actions of ultraviolet light on cellular structures. Cancer: Cell Structures, Carcinogens and Genomic Instability, 96, 131–157.Google Scholar
  95. Peccia, J., Werth, H. M., Miller, S., & Hernandez, M. (2001). Effects of relative humidity on the ultraviolet induced inactivation of airborne bacteria. Aerosol Science and Technology, 35(3), 728–740.Google Scholar
  96. 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.Google Scholar
  97. Ramos, R. J., Miotto, M., Lagreze Squella, F. J., Cirolini, A., Ferreira, J. F., & Werneck Vieira, C. R. (2012). Depuration of oysters (Crassostrea gigas) contaminated with Vibrio parahaemolyticus and Vibrio vulnificus with UV light and chlorinated seawater. Journal of Food Protection, 75(8), 1501–1506.Google Scholar
  98. Rastogi, R. P., Richa, K. A., Tyagi, M. B., & Sinha, R. P. (2010). Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. Journal of Nucleic Acids, 2010, 592980.Google Scholar
  99. Ravanat, J.-L., Douki, T., & Cadet, J. (2001). Direct and indirect effects of UV radiation on DNA and its components. Journal of Photochemistry and Photobiology, B: Biology, 63(1–3), 88–102.Google Scholar
  100. Riesenman, P. J., & Nicholson, W. L. (2000). Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Applied and Environmental Microbiology, 66(2), 620–626.Google Scholar
  101. Rodrigues, F., Ludovico, P., Sousa, M. J., Steensma, H. Y., Corte-Real, M., & Leao, C. (2003). The spoilage yeast Zygosaccharomyces bailii forms mitotic spores: a screening method for haploidization. Applied and Environmental Microbiology, 69(1), 649–653.Google Scholar
  102. Rodriguez-Romo, L. A., & Yousef, A. E. (2005). Inactivation of Salmonella enterica serovar enteritidis on shell eggs by ozone and UV radiation. Journal of Food Protection, 68(4), 711–717.Google Scholar
  103. Ross, A. I. V., Griffiths, M. W., Mittal, G. S., & Deeth, H. C. (2003). Combining nonthermal technologies to control foodborne microorganisms. International Journal of Food Microbiology, 89(2–3), 125–138.Google Scholar
  104. Rude, J., & Alper, T. (1972). Changes in UV survival curves of Escherichia coli B/r concomitant with changes in growth conditions. Photochemistry and Photobiology, 15(1), 51–60.Google Scholar
  105. Sastry, S. K., Datta, K., & Worobo, R. W. (2000). Ultraviolet light. Journal of Food Safety, 65(5), 90–92.Google Scholar
  106. Schenk, M., Guerrero, S., & Alzamora, S. M. (2008). Response of some microorganisms to ultraviolet treatment on fresh-cut pear. Food and Bioprocess Technology, 1(4), 384–392.Google Scholar
  107. Schenley, R. L., Fisher, W. D., & Swenson, P. A. (1976). Primidine dimer excision in surviving and non-surviving cells of ultraviolet irradiated cultures of Escherichia-coli. Journal of Bacteriology, 126(2), 985–989.Google Scholar
  108. Sedliakova, M. (1998). A non-excision uvr-dependent DNA repair pathway of Escherichia coli (involvement of stress proteins). Journal of Photochemistry and Photobiology, B: Biology, 45(2–3), 75–81.Google Scholar
  109. Setlow, P. (2001). Resistance of spores of Bacillus species to ultraviolet light. Environmental and Molecular Mutagenesis, 38(2–3), 97–104.Google Scholar
  110. Setlow, P. (2006). Spores of Bacillus subtilis: their resistance ot and killing by radiation, heat and chemicals. Journal of Applied Microbiology, 101(3), 514–525.Google Scholar
  111. Sinha, R. P., & Hader, D. P. (2002). UV-induced DNA damage and repair: a review. Photochemical & Photobiological Sciences, 1(4), 225–236.Google Scholar
  112. Slieman, T. A., & Nicholson, W. L. (2000). Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA. Applied and Environmental Microbiology, 66(1), 199–205.Google Scholar
  113. Slieman, T. A., & Nicholson, W. L. (2001). Role of dipicolinic acid in survival of Bacillus subtilis spores exposed to artificial and solar UV radiation. Applied and Environmental Microbiology, 67(3), 1274–1279.Google Scholar
  114. Sommer, R., Lhotsky, M., Haider, T., & Cabaj, A. (2000). UV inactivation, liquid-holding recovery, and photoreactivation of Escherichia coli O157 and other pathogenic Escherichia coli strains in water. Journal of Food Protection, 63(8), 1015–1020.Google Scholar
  115. Suss, J., Volz, S., Obst, U., & Schwartz, T. (2009). Application of a molecular biology concept for the detection of DNA damage and repair during UV disinfection. Water Research, 43(15), 3705–3716.Google Scholar
  116. Takeshita, K., Shibato, J., Sameshima, T., Fukunaga, S., Isobe, S., Arihara, K., & Itoh, M. (2003). Damage of yeast cells induced by pulsed light irradiation. International Journal of Food Microbiology, 85(1–2), 151–158.Google Scholar
  117. Todo, T., Yonei, S., & Kato, M. (1983). The modulating influence of the fluidity of cell-membrane on excision repair of DNA in UV-irradiated Escherichia-coli. Biochemical and Biophysical Research Communications, 110(2), 609–615.Google Scholar
  118. Tosa, K., & Hirata, T. (1999). Photoreactivation of enterohemorrhagic Escherichia coli following UV disinfection. Water Research, 33(2), 361–366.Google Scholar
  119. Truglio, J. J., Croteau, D. L., Van Houten, B., & Kisker, C. (2006). Prokaryotic nucleotide excision repair: the UvrABC system. Chemical Reviews, 106(2), 233–252.Google Scholar
  120. Turtoi, M., & Nicolau, A. (2007). Intense light pulse treatment as alternative method for mould spores destruction on paper-polyethylene packaging material. Journal of Food Engineering, 83(1), 47–53.Google Scholar
  121. Tyrrell, R. M., Moss, S. H., & Davies, D. J. G. (1972). The variation in UV sensitivity of four K12 strains of Escherichia coli as a function of their stage of growth. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 16(1), 1–12.Google Scholar
  122. Tyrrell, R. M., Webb, R. B., & Brown, M. S. (1973). Destruction of photoreactivating enzyme by 365 nm radiation. Photochemistry and Photobiology, 18(4), 249–254.Google Scholar
  123. 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.Google Scholar
  124. Van der Veen, S., & Abee, T. (2011). Bacterial SOS response: a food safety perspective. Current Opinion in Biotechnology, 22(2), 136–142.Google Scholar
  125. Velez-Colmenares, J. J., Acevedo, A., & Nebot, E. (2011). Effect of recirculation and initial concentration of microorganisms on the disinfection kinetics of Escherichia coli. Desalination, 280(1–3), 20–26.Google Scholar
  126. Vulic, M., & Kolter, R. (2001). Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics, 158(2), 519–526.Google Scholar
  127. Wassmann, M., Moeller, R., Reitz, G., & Rettberg, P. (2011). Growth phase-dependent UV-C resistance of Bacillus subtilis: data from a short-term evolution experiment. Archives of Microbiology, 193(11), 823–832.Google Scholar
  128. Wekhof, A. (2000). Disinfection with flash lamps Pda. Journal of Pharmaceutical Science and Technology, 54(3), 264–276.Google Scholar
  129. Wekhof A, Trompeter FJ & Franken O (2001) Pulsed UV-disintegration (PUVD): a new sterilization mechanism for packaging and broad medical-hospital applications. In: Proceedings of the first international conference on ultraviolet technologies, 14–16 June, Washington DCGoogle Scholar
  130. Wu, D., You, H., Zhang, R., Chen, C., & Lee, D.-J. (2011). Ballast waters treatment using UV/Ag-TiO2 + O−3 advanced oxidation process with Escherichia coli and Vibrio alginolyticus as indicator microorganisms. Chemical Engineering Journal, 174(2–3), 714–718.Google Scholar
  131. Zimmer-Thomas, J. L., & Slawson, R. (2002). Potential repair of Escherichia coli DNA following exposure to UV radiation from both medium- and low-pressure UV sources used in drinking water treatment. Applied and Environmental Microbiology, 68(7), 3293–3299.Google Scholar
  132. Zou, Y., Crowley, D. J., & Van Houten, B. (1998). Involvement of molecular chaperonins in nucleotide excision repair—DnaK leads to increased thermal stability of UvrA, catalytic UvrB loading, enhanced repair, and increased UV resistance. Journal of Biological Chemistry, 273(21), 12887–12892.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Elisa Gayán
    • 1
  • Santiago Condón
    • 1
  • Ignacio Álvarez
    • 1
  1. 1.Tecnología de los Alimentos, Facultad de VeterinariaUniversidad de ZaragozaZaragozaSpain

Personalised recommendations