Abstract
Naturally occurring plant-derived flavonoids are reported to have antibacterial, antiviral, and pharmacological activities. The objectives of this study were to determine the antiviral effects of four flavonoids (myricetin, l-epicatechin, tangeretin, and naringenin) on the infectivity of food borne norovirus surrogates after 2 h at 37 °C. The lab-culturable surrogates, feline calicivirus (FCV-F9) at titers of ~7 log10 PFU/ml (high titer) or ~5 log10 PFU/ml (low titer) and murine norovirus (MNV-1) at ~5 log10 PFU/ml, were mixed with equal volumes of myricetin, l-epicatechin, tangeretin, or naringenin at concentrations of 0.5 or 1 mM, and incubated for 2 h at 37 °C. Treatments of viruses were neutralized in cell culture medium containing 10 % heat-inactivated fetal bovine serum, serially diluted, and plaque assayed. Each treatment was replicated thrice and assayed in duplicate. FCV-F9 (low titer) was not found to be reduced by tangeretin or naringenin, but was reduced to undetectable levels by myricetin at both concentrations. Low titer FCV-F9 was also decreased by 1.40 log10 PFU/ml with l-epicatechin at 0.5 mM. FCV-F9 at high titers was decreased by 3.17 and 0.72 log10 PFU/ml with myricetin and l-epicatechin at 0.5 mM, and 1.73 log10 PFU/ml with myricetin at 0.25 mM, respectively. However, MNV-1 showed no significant inactivation by the four tested treatments. The antiviral effects of the tested flavonoids are dependent on the virus type, titer, and dose. Further research will focus on understanding the antiviral mechanism of myricetin and l-epicatechin.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Cheesbrough, J. S., Green, J., Gallimore, C. I., Wright, P. A., & Brown, D. W. G. (2000). Widespread environmental contamination with Norwalk-like viruses (NLV) detected in a prolonged hotel outbreak of gastroenteritis. Epidemiology and Infection, 125(1), 93–98.
Cheng, P. C., & Wong, G. (1996). Honey bee propolis: Prospects in medicine. Bee World, 77(1), 8–15.
Chiang, L. C., Chiang, W., Liu, M. C., & Lin, C. C. (2003). In vitro antiviral activities of Caesalpinia pulcherrima and its related flavonoids. Journal of Antimicrobial Chemotherapy, 52(2), 194–198.
Chu, S. C., Hsieh, Y. S., & Lin, J. Y. (1992). Inhibitory effects of flavonoids on moloney murine leukemia virus reverse transcriptase activity. Journal of Natural Products, 55(2), 179–183.
Cody, V., Middleton, E., & Harborne, J. B. (Eds.). (1986). Plant flavonoids in biology and medicine: Biochemical, pharmacological, and structure–activity relationships. New York: Alan R. Liss, Inc.
Cushnie, T. P. T., & Lamb, A. J. (2005). Antimicrobial activity of flavonoids. International Journal of Antimicrobial Agents, 26(5), 343–356.
Debiaggi, M., Tateo, F., Pagani, L., Luini, M., & Romero, E. (1990). Effects of propolis flavonoids on virus infectivity and replication. Microbiologica, 13(3), 207–213.
D’Souza, D. H., Sair, A., Williams, K., Papafragkou, E., Jean, J., Moore, C., et al. (2006). Persistence of caliciviruses on environmental surfaces and their transfer to food. International Journal of Food Microbiology, 108(1), 84–91.
D’Souza, D. H., & Su, X. W. (2010). Efficacy of chemical treatments against murine norovirus, Feline calicivirus, and MS2 Bacteriophage. Foodborne Pathogens and Disease, 7(3), 319–326.
El Gharras, H. (2009). Polyphenols: Food sources, properties and applications—a review. International Journal of Food Science & Technology, 44(12), 2512–2518.
Jassim, S. A. A., & Naji, M. A. (2003). Novel antiviral agents: A medicinal plant perspective. Journal of Applied Microbiology, 95(3), 412–427.
Kuusi, M., Nuorti, J. P., Maunula, L., Minh, N. N. T., Ratia, M., Karlsson, J., et al. (2002). A prolonged outbreak of Norwalk-like calicivirus (NLV) gastroenteritis in a rehabilitation centre due to environmental contamination. Epidemiology and Infection, 129(1), 133–138.
Kwon, H. J., Kim, H. H., Ryu, Y. B., Kim, J. H., Jeong, H. J., Lee, S. W., et al. (2010). In vitro anti-rotavirus activity of polyphenol compounds isolated from the roots of Glycyrrhiza uralensis. Bioorganic & Medicinal Chemistry, 18(21), 7668–7674.
Liu, A. L., Wang, H. D., Lee, S. M. Y., Wang, Y. T., & Du, G. H. (2008). Structure-activity relationship of flavonoids as influenza virus neuraminidase inhibitors and their in vitro anti-viral activities. Bioorganic & Medicinal Chemistry, 16(15), 7141–7147.
Lyu, S. Y., Rhim, J. Y., & Park, W. B. (2005). Antiherpetic activities of flavonoids against herpes simplex virus type 1 (HSV-1) and type 2 (HSV-2) in vitro. Archives of Pharmacal Research, 28(11), 1293–1301.
Matias, A. A., Serra, A. T., Silva, A. C., Perdigao, R., Ferreira, T. B., Marcelino, I., et al. (2010). Portuguese winemaking residues as a potential source of natural anti-adenoviral agents. International Journal of Food Sciences and Nutrition, 61(4), 357–368.
Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., et al. (1999). Food-related illness and death in the United States. Emerging Infectious Diseases, 5(5), 607–625.
Mukoyama, A., Ushijima, H., Nishimura, S., Koike, H., Toda, M., Hara, Y., et al. (1991). Inhibition of rotavirus and enterovirus infection by tea extract. Japanese Journal of Medical Science and Biology, 44(4), 181–186.
Ramachandran, K. V. (1956). On the Tukey test for the equality of means and the HARTLEY test for the equality of variances. Annals of Mathematical Statistics, 27(3), 825–831.
Regal, R. R. (1986). PC statistician PC ANOVA. American Statistician, 40(2), 164–167.
Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States–major pathogens. Emerging Infectious Disease, 17(1), 7–15.
Siebenga, J. J., Vennema, H., Zheng, D. P., Vinje, J., Lee, B. E., Pang, X. L., et al. (2009). Norovirus illness is a global problem: Emergence and spread of Norovirus GII.4 variants, 2001–2007. Journal of Infectious Diseases, 200, 802–812.
Su, X., & D’Souza, D. H. (2011). Grape seed extract for the control of human enteric viruses. Applied Environmental Microbiology, 77, 3982–3987.
Su, X., Howell, A. B., & D’Souza, D. H. (2010a). The effect of cranberry juice and cranberry proanthocyanidins on the infectivity of human enteric viral surrogates. Food Microbiology, 27(4), 535–540.
Su, X. W., Sangster, M. Y., & D’Souza, D. H. (2010b). In Vitro Effects of Pomegranate Juice and Pomegranate Polyphenols on Foodborne Viral Surrogates. Foodborne Pathogens and Disease, 7(12), 1473–1479.
Tait, S., Salvati, A. L., Desideri, N., & Fiore, L. (2006). Antiviral activity of substituted homoisoflavonoids on enteroviruses. Antiviral Research, 72(3), 252–255.
Wobus, C. E., Karst, S. M., Thackray, L. B., Chang, K. O., Sosnovtsev, S. V., Belliot, G., et al. (2004). Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biology, 2(12), 2076–2084.
Yao, L. H., Jiang, Y. M., Shi, J., Tomas-Barberan, F. A., Datta, N., Singanusong, R., et al. (2004). Flavonoids in food and their health benefits. Plant Foods for Human Nutrition, 59(3), 113–122.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Su, X., D’Souza, D.H. Naturally Occurring Flavonoids Against Human Norovirus Surrogates. Food Environ Virol 5, 97–102 (2013). https://doi.org/10.1007/s12560-013-9106-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12560-013-9106-4