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Evaluation of Steady-State Gaseous Chlorine Dioxide Treatment for the Inactivation of Tulane virus on Berry Fruits

  • David H. Kingsley
  • Bassam A. AnnousEmail author
Original Paper
  • 21 Downloads

Abstract

The effectiveness of steady-state levels of gaseous chlorine dioxide (ClO2) against Tulane virus (TV), a human norovirus surrogate, on berries was determined. The generated ClO2 was maintained at 1 mg/L inside a 269 L glove box to treat two 50 g batches of blueberries, raspberries, and blackberries, and two 100 g batches of strawberries that were immersion coated with TV. The standardized/normalized treatment concentrations of ClO2 ranging from 0.63 to 4.40 ppm-h/g berry were evaluated. When compared to untreated TV contaminated berries, log reductions of TV were in excess of 2.9 log PFU/g for all berry types and conditions tested, indicating that ClO2 was highly effective. In general, the efficacy of all ClO2 treatments on log reductions of TV on all berries was not significantly different (p < 0.05). The average log reduction with strawberries, raspberries, blueberries, and blackberries, treated with the lowest ClO2 concentration, 0.63 ppm-h/g, were 2.98, 3.40, 3.82, and 4.17 log PFU/g, respectively. Overall results suggest that constant levels of ClO2 could be quite effective against foodborne viruses.

Keywords

Norovirus Tulane virus Gaseous chlorine dioxide Blueberry Raspberry Blackberry Strawberry 

Notes

Acknowledgements

We thank Dr. Modesto Olanya, Research Plant Pathologist at the North East Area, Agricultural Research Service, Wyndmoor, PA, for statistical analysis of the results. Mention of trade names or commercial products in this article is solely for providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). USDA is an equal opportunity provider and employer.

References

  1. Alicea, C., Annous, B. A., Mendez, D. P., Burke, A., & Orellana, L. E. (2018). Evaluation of hot water, gaseous chlorine dioxide, and hypochlorous acid treatments in combination with an edible coating for enhancing safety, quality, and shelf-life of fresh-cut cantaloupes. Journal of Food Protection, 81(4), 534–541.CrossRefGoogle Scholar
  2. Annous, B. A., & Burke, A. (2015). Development of combined dry heat and chlorine dioxide gas treatment with mechanical mixing for inactivation of Salmonella enterica Serovar Montevideo on mung bean seeds. Journal of Food Protection, 78, 868–872.CrossRefGoogle Scholar
  3. Banach, J. L., Sampers, I., Van Haute, S., & Van der Fels-Klerx, H. J. (2015). Effect of disinfectants on preventing the cross-contamination of pathogens in fresh produce washing water. International Journal of Environmental Research and Public Health, 12, 8658–8677.CrossRefGoogle Scholar
  4. Bartsch, S. M., Lopman, B. A., Ozawa, S., Hall, A. J., & Lee, B. Y. (2016). Global economic burden of norovirus gastroenteritis. PLOS ONE.  https://doi.org/10.1371/journal.pone.0151219.Google Scholar
  5. Bernarde, M. A., Israel, B. M., Olivieri, V. P., & Granstrom, M. L. (1976). Kinetics and mechanism of bacterial disinfection by chlorine dioxide. Journal of Applied Microbiology, 15(2), 257.Google Scholar
  6. Butot, S., Putallaz, T., Amoroso, R., & Sánchez, G. (2009). Inactivation of enteric viruses in minimally processed berries and herbs. Applied and Environmental Microbiology, 75, 4155–4161.CrossRefGoogle Scholar
  7. Costantini, V., Morantz, E. K., Browne, H., Ettayebi, K., Zeng, X. L., Atmar, R. L., Estes, M. K., & Vinjé, J. (2018). Human norovirus replication in human intestinal enteroids as model to evaluate virus inactivation. Emerging Infectious Disease, 24, 1453–1464.CrossRefGoogle Scholar
  8. Cromeans, T., Park, G. W., Costantini, V., Lee, D., Wang, Q., Farkase, T., Lee, A., & Vinjé, J. (2014). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environmental Microbiology, 80, 5743–5751.CrossRefGoogle Scholar
  9. Dancho, B. A., Chen, H., & Kingsley, D. H. (2012). Discrimination between infectious and non-infectious human noroviruses using porcine gastric mucin. International Journal of Food Microbiology, 155, 222–226.CrossRefGoogle Scholar
  10. Di Cristo, C., Esposito, G., & Leopardi, A. (2013). Modelling trihalomethanes formation in water supply systems. Environmental Technology, 34, 61–70.CrossRefGoogle Scholar
  11. Ettayebi, K., Crawford, S. E., Murakami, K., Broughman, J. R., Karandikar, U., Tenge, V. R., Neill, F. H., Blutt, S. E., Zeng, X. L., Qu, L., Kou, B., Opekun, A. R., Burrin, D., Graham, D. Y., Ramani, S., Atmar, R. L., & Estes, M. K. (2016). Replication of human noroviruses in stem cell-derived human enteroids. Science, 353, 1387–1393.CrossRefGoogle Scholar
  12. Fan, X., & Sokorai, K. J. (2015). Formation of trichloromethane in chlorinated water and fresh-cut produce and as a result of reacting with citric acid. Postharvest Biology and Technology, 109, 65–72.CrossRefGoogle Scholar
  13. Fraisse, A., Temmam, S., Deboosere, N., Guiller, L., Delobel, A., Maris, P., Viatette, M., Morin, T., & Perelle, S. (2011). Comparison of chlorine and peroxyacetic based acid disinfectant to inactivate feline calicivirus, murine norovirus and hepatitis A virus on lettuce. International Journal of Food Microbiology, 151, 98–104.CrossRefGoogle Scholar
  14. Hall, A. J., Lopman, B. A., Payne, D. C., Patel, M. M., Gastañaduy, P. A., Vinjé, J., & Parashar, U. D. (2013). Norovirus disease in the United States. Emerging Infectious Diseases, 19, 1198–1205.CrossRefGoogle Scholar
  15. Hirneisen, K. A., & Kniel, K. E. (2013). Comparing human norovirus surrogates: Murine norovirus and Tulane virus. Journal of Food Protection, 76, 139–143.CrossRefGoogle Scholar
  16. Keskinen, L. A., & Annous, B. A. (2011). Chlorine dioxide gas. In H. Zhang, G. Barbosa-Canovas, V. M. Balasubramaniam, P. Dunne, D. Farkas, & J. Yuan (Eds.) Nonthermal processing technologies for food (pp. 359–365). Iowa: Blackwell Publishing.CrossRefGoogle Scholar
  17. Kingsley, D. H., Pérez-Pérez, R. E., Niemira, B. A., & Fan, X. (2018). Evaluation of gaseous chlorine dioxide for inactivation of Tulane virus contaminated blueberries. International Journal of Food Microbiology, 273, 28–32.CrossRefGoogle Scholar
  18. Kingsley, D. H., Vincent, E., Meade, G. K., Watson, C., & Fan, X. (2014). Inactivation of human norovirus using chemical sanitizers. International Journal of Food Microbiology, 171, 94–99.CrossRefGoogle Scholar
  19. Kirby, A. E., Streby, A., & Moe, C. L. (2016). Vomiting as a symptom and transmission risk in norovirus illness: Evidence from human challenge studies. PLOS one.  https://doi.org/10.1371/journal.pone.0143759.Google Scholar
  20. Li, X., & Chen, H. (2015). Evaluation of the porcine gastric mucin binding assay for high-pressure-inactivation studies using murine norovirus and Tulane virus. Applied and Environmental Microbiology, 81, 515–521.CrossRefGoogle Scholar
  21. Montazeri, N., Manuel, C., Mooman, E., Khatiwada, J. R., Williams, L. L., & Jaykus, L. (2017). Virucidal activity of fogged chlorine dioxide and hydrogen peroxide disinfectants against human norovirus and its surrogate feline calicivirus on hard to reach surfaces. Frontiers in Microbiology, 8, 1031.CrossRefGoogle Scholar
  22. Nowak, P., Topping, J. R., Fotheringham, V., Gallimore, C. I., Gray, J. J., Iturriza-Gomara, M., & Knight, A. I. (2011). Measurement of the virolysis of human GII.4 norovirus in response to disinfectants and sanitizers. Journal of Virological Methods, 174, 7–11.CrossRefGoogle Scholar
  23. Olaimat, A. N., & Holley, R. A. (2012). Factors influencing the microbial safety of fresh produce: A review. Food Microbiology, 32, 1–19.CrossRefGoogle Scholar
  24. Ortega, Y. R., Mann, A., Torres, M. P., & Cama, V. (2008). Efficacy of gaseous chlorine dioxide as a sanitizer against Cryptosporidium parvum, Cyclospora cayetanensis, and Encephalitozoon intestinalis on produce. Journal of Food Protection, 71, 2410–2414.CrossRefGoogle Scholar
  25. Oxenford, J. L. (1995). Disinfection by-products: Current practices and future directions. In R. A. Minear and G. L. Amy (Eds.), Disinfection by-products in water treatment: The chemistry of their formation and control. Boca Raton, FL.Google Scholar
  26. Parish, M. E., Beuchat, L. R., Suslow, T. V., Harris, L. J., Farber, J. N., & Busta, F. F. (2003). Methods to reduce or eliminate pathogens from fresh and fresh-cut produce. Comprehensive Reviews of Food Science and Food Safety, 2, 161–173.CrossRefGoogle Scholar
  27. Park, S. H., Kim, W. J., & Kang, D. H. (2018). Effect of relative humidity on inactivation of foodborne pathogens using chlorine dioxide gas and its residues on tomatoes. Letters in Applied Microbiology, 67, 154–160.CrossRefGoogle Scholar
  28. Popa, I., Hanson, E. J., Todd, E. C. D., Schilder, A. C., & Ryser, E. T. (2007). Efficacy of chlorine dioxide gas sachets for enhancing the microbial safety and quality of blueberries. Journal of Food Protection, 70, 2084–2088.CrossRefGoogle Scholar
  29. Prado-Silva, L., Cadavez, V., Gonzales-Barron, U., Rezende, A. C. B., & Sant’Ana, A. S. (2015). Meta-analysis of the effects of sanitizing treatments on Salmonella, Escherichia coli O157:H7 and Listeria monocytogenes inactivation in fresh produce. Applied and Environmental Microbiology, 81, 8008–8021.CrossRefGoogle Scholar
  30. Prodduk, V., Annous, B. A., Liu, L., & Yam, K. L. (2014). Evaluation of chlorine dioxide gas treatment to inactivate Salmonella enterica on mungbean sprouts. Journal of Food Protection, 77, 1876–1881.CrossRefGoogle Scholar
  31. Richards, G. P., Watson, M. A., Meade, G. K., Hovan, G. L., & Kingsley, D. H. (2012). Resilience of norovirus GII.4 to freezing and thawing: Implications for virus infectivity. Food and Environmental Virology, 4, 192–197.CrossRefGoogle Scholar
  32. Rulis, A. M. (2001) Agency response letter GRAS Notice No. GRN 000062. Retrieved July 26, 2018, from http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm153971.htm.
  33. Saade, C., Annous, B. A., Gualtieri, A. J., Schaich, K. M., Liu, L.-S., & Yam, K. L. (2018). System feasibility: designing a chlorine dioxide self-generating package label to improve fresh produce safety part II: Solution casting approach. Innovative Food Science and Emerging Technologies, 47, 110–119.CrossRefGoogle Scholar
  34. Shirasaki, Y., Matsuura, A., Uekusa, M., Ito, Y., & Hayashi, T. (2016). A study of the properties of chlorine dioxide gas as a fumigant. Experimental Animals, 65, 303–310.CrossRefGoogle Scholar
  35. Sun, X., Bai, J., Ference, C., Wang, Z., Zhang, Y., Narciso, J., & Zhou, K. (2014). Antimicrobial activity of control-release chlorine dioxide gas on fresh blueberries. Journal of Food Protection, 77, 1127–1132.CrossRefGoogle Scholar
  36. Sy, K. V., McWatters, K. H., & Beuchat, L. R. (2005). Efficacy of gaseous chlorine dioxide as a sanitizer for killing Salmonella, yeasts, and molds on blueberries, strawberries, and raspberries. Journal of Food Protection, 68, 1165–1175.CrossRefGoogle Scholar
  37. Tian, P., Yang, D., Quigley, C., Chou, M., & Jiang, X. (2013). Inactivation of the Tulane virus, a novel surrogate for the human norovirus. Journal of Food Protection, 76, 712–718.CrossRefGoogle Scholar
  38. Tung, G., Macinga, D., Abrogast, J., & Jaykus, L. A. (2013). Efficacy of commonly used disinfectants for inactivation of human norovirus and their surrogates. Journal of Food Protection, 76, 1210–1217.CrossRefGoogle Scholar
  39. Verhoef, L., Hewitt, J., Barclay, L., Ahmed, S. M., Lake, R., Hall, A. J., Lopman, B., Kroneman, A., Vennema, H., Vinjé, J., & Koopmans, M. (2015). Norovirus genotype profiles associated with foodborne transmission, 1999–2012. Emerging Infectious Diseases, 21, 592–599.CrossRefGoogle Scholar
  40. Wu, V. C., & Kim, B. (2007). Effect of simple chlorine dioxide method for controlling five foodborne pathogens, yeasts and molds on blueberries. Food Microbiology, 24, 794–800.CrossRefGoogle Scholar
  41. Yang, X., Zhang, X., Fu, M., Chen, Q., & Muzammil, J. M. (2018). Chlorine dioxide fumigation generated by a solid releasing agent enhanced the efficiency of 1-MCP treatment on the storage quality of strawberry. Journal of Food Science & Technology, 55, 2003–2010.CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  1. 1.Food Safety and Intervention Technologies Research Unit, U.S. Department of Agriculture, Agricultural Research ServiceDelaware State UniversityDoverUSA
  2. 2.Food Safety and Intervention Technologies Research Unit, U.S. Department of Agriculture, Agricultural Research ServiceEastern Regional Research CenterWyndmoorUSA

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