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Antiviral Activity of Essential Oils Against Hepatitis A Virus in Soft Fruits

Abstract

Berries have repeatedly been associated with outbreaks of hepatitis A virus (HAV) infection. The fruits are usually minimally processed in the food industry due to their delicate nature. While washing treatments partially remove enteric viruses, the commonly used chemical additives produce toxic by-products. A valid alternative to preserve the food safety of these products could be the use of essential oils (EOs). EOs exert antimicrobial activity and do not interfere with the nutritional characteristics of food products. We investigated the efficacy of four essential oils, lemon (Citrus limon), sweet orange (Citrus sinensis), grapefruit (Citrus paradisi), and rosemary cineole (Rosmarinus officinalis chemotype 1.8 cineole) in reducing viral loads of HAV in soft fruits. Mixed fruit berries were inoculated with 106.74 TCID50/ml of HAV, and treated with four different EOs (0.5% lemon, 0.1% sweet orange and grapefruit, and 0.05% rosemary) for 1 h at room temperature. Virus infectivity was then assessed by titration assays for its ability to grow on cell cultures. A statistically significant reduction in HAV titer on the fruit surface was observed after treating the berries with EOs of lemon (2.84 log TCID50/ml), grapefruit (2.89 log TCID50/ml), and rosemary cineole (2.94 log TCID50/ml). Rosemary cineole was the most effective EO in reducing viral titer on berries, followed by grapefruit EO. These results improve our knowledge about the antiviral activity of these EOs and highlight their potential use in fresh produce sanitation.

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References

  • Baert, L., Debevere, J., & Uyttendaele, M. (2009). The efficacy of preservation methods to inactivate foodborne viruses. International Journal of Food Microbiology, 131(2–3), 83–94.

    CAS  Article  Google Scholar 

  • Burnett, S. L., & Beuchat, L. R. (2001). Human pathogens associated with raw produce and unpasteurized juices, and difficulties in decontamination. Journal of Industrial Microbiology & Biotechnology, 27(2), 104–110.

    CAS  Article  Google Scholar 

  • Butot, S., Putallaz, T., & Sanchez, G. (2008). Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. International Journal of Food Microbiology, 126(1–2), 30–35.

    CAS  Article  Google Scholar 

  • Carter, M. J. (2005). Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection. Journal of Applied Microbiology, 98(6), 1354–1380.

    CAS  Article  Google Scholar 

  • Casteel, M. J., Schmidt, C. E., & Sobsey, M. D. (2008). Chlorine disinfection of produce to inactivate hepatitis A virus and coliphage MS2. International Journal of Food Microbiology, 125(3), 267–273.

    CAS  Article  Google Scholar 

  • Chatziprodromidou, I. P., Bellou, M., Vantarakis, G., & Vantarakis, A. (2018). Viral outbreaks linked to fresh produce consumption: a systematic review. Journal of Applied Microbiology, 124(4), 932–942.

    CAS  Article  Google Scholar 

  • Chouhan, S., Sharma, K., & Guleria, S. (2017). Antimicrobial Activity of Some Essential Oils—Present Status and Future Perspectives. Medicines (Basel), 4(3), 58.

    Article  Google Scholar 

  • EFSA. (2013). Hepatitis A virus infection in four Nordic countries, 15 April 2013. Joint ECDC/EFSA rapid outbreak assessment.

  • Elizaquível, P., Azizkhani, M., Aznar, R., & Sánchez, G. (2013). The effect of essential oils on norovirus surrogates. Food Control, 32(1), 275–278.

    Article  Google Scholar 

  • Fabra, M. J., Castro-Mayorga, J. L., Randazzo, W., Lagarón, J. M., López-Rubio, A., Aznar, R., & Sánchez, G. (2016). Efficacy of cinnamaldehyde against enteric viruses and its activity after incorporation into biodegradable multilayer systems of interest in food packaging. Food and Environmental Virology, 8(2), 125–132.

    CAS  Article  Google Scholar 

  • Felix-Valenzuela, L., Resendiz-Sandoval, M., Burgara-Estrella, A., Hernández, J., & Mata-Haro, V. (2012). Quantitative detection of hepatitis A, rotavirus and genogroup I norovirus by RT-qPCR in fresh produce from packinghouse facilities. Jounal of Food Safety, 32(4), 467–473.

    Article  Google Scholar 

  • 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. Jounal of Food Protection, 71(5), 908–913.

    Article  Google Scholar 

  • Fisher, K., & Phillips, C. (2008). Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends in Food Science & Technology, 19(3), 156–164.

    CAS  Article  Google Scholar 

  • Fitzgerald, M., Thornton, L., O’Gorman, J., O’Connor, L., Garvey, P., Boland, M., Part, A. M., et al. Hepatitis, A., Outbreak Control Team (2014). Outbreak of hepatitis A infection associated with the consumption of frozen berries, Ireland, 2013-linked to an international outbreak. Euro Surveillance, 30(43), pii: 20942. 19 ).

    Google Scholar 

  • Fraisse, A., Temman, S., Deboosere, N., Guillier, L., Delobel, A., Maris, P., Vialette, M., et al. (2001). Comparison of chlorine and peroxyacetic-based disinfectant to inactivate Feline calicivirus, Murine norovirus and hepatitis A virus on lettuce. International Journal of Food Microbiology, 151(1), 98–104.

    Article  Google Scholar 

  • Gavanji, S., Sayedipour, S. S., Larki, B., & Bakhtari, A. (2015). Antiviral activity of some plant oils against herpes simplex virus type 1 in Vero cell culture. Journal of Acute Medicine, 5(3), 62–68.

    Article  Google Scholar 

  • Gil, M. I., Selma, M. V., López-Gálvez, F., & Allende, A. (2009). Fresh-cut product sanitation and wash water disinfection: problems and solutions. International Journal of Food Microbiology, 134(1–2), 37–45.

    CAS  Article  Google Scholar 

  • Gillesberg Lassen, S., Soborg, B., Midgley, S. E., Steens, A., Vold, L., Stene-Johansen, K., Rimhanen-Finne, R., et al. (2013). Ongoing multi-strain food-borne hepatitis A outbreak with frozen berries as suspected vehicle: four Nordic countries affected, October 2012 to April 2013. Euro Surveillance, 18(17), 20467.

    CAS  PubMed  Google Scholar 

  • Gilling, D. H., Kitajima, M., Torrey, J. R., & Bright, K. R. (2014). Antiviral efficacy and mechanisms of action of oregano essential oil and its primary component carvacrol against murine norovirus. Journal of Applied Microbiology, 116(5), 1149–1163.

    CAS  Article  Google Scholar 

  • Hoskins, J. M. (1975). Diagnosi virologica principi e metodi. Milano: Casa Editrice Ambrosiana.

    Google Scholar 

  • Joshi, S. S., Howell, A. B., & D’Souza, D. H. (2016). Reduction of enteric viruses by blueberry juice and blueberry proanthocyanidins. Food and Environmental Virology, 8(4), 235–243.

    CAS  Article  Google Scholar 

  • Kim, Y. W., You, H. J., Lee, S., Kim, B., Kim, D. K., Choi, J. B., Kim, J. A., et al. (2017). Inactivation of norovirus by lemongrass essential oil using a norovirus surrogate system. Jounal of Food Protection, 80(8), 1293–1302.

    CAS  Article  Google Scholar 

  • Kovač, K., Diez-Valcarce, M., Raspor, P., Hernández, M., & Rodríguez-Lázaro, D. (2012). Natural plant essential oils do not inactivate non-enveloped enteric viruses. Food and Environmental Virology, 4(4), 209–212.

    Article  Google Scholar 

  • Lanciotti, R., Gianotti, A., Patrignani, F., Belletti, N., Guerzoni, M. E., & Gardini, F. (2004). Use of natural aroma compounds to improve shelf-life and safety of minimally processed fruits. Trends in Food Science & Technology, 15, 201–208.

    CAS  Article  Google Scholar 

  • Laranjo, M., Fernández-Léon, A. M., Potes, M. E., Agulheiro-Santos, A. C., & Elias, M. (2017). Use of essential oils in food preservation. In Antimicrobial Research: Novel bioknowledge and educational programs (Microbiology Book Series #6) (pp. 177–188). Badajoz: Edited by A. Méndez-Vilas, Formatex Research Center. http://www.microbiology6.org/ebook.php.

  • Lee, J. Y., Jang, S., Aguilar, L. E., Park, C. H., & Kim, C. S. (2019). Structural packaging technique using biocompatible nanofiber with essential oil to prolong the shelf-life of fruit. Journal of Nanoscience and Nanotechnology, 19(4), 2228–2231.

    CAS  Article  Google Scholar 

  • Lee, M. H., Lee, B. H., Lee, S., & Choi, C. (2013). Reduction of hepatitis A virus on FRhK-4 cells treated with Korean red ginseng extract and ginsenosides. Journal of Food Science, 78(9), 1412–1415.

    Article  Google Scholar 

  • Li, D., Baert, L., & Uyttendaele, M. (2013). Inactivation of food-borne viruses using natural biochemical substances. Food Microbiology, 35(1), 1–9.

    Article  Google Scholar 

  • Martínez, K., Ortiz, M., Albis, A., Gilma Gutiérrez Castañeda, C., Valencia, M. E., & Grande Tovar, C. D. (2018). The effect of edible chitosan coatings incorporated with Thymus capitatus essential oil on the shelf-life of strawberry (Fragaria × ananassa) during cold storage. Biomolecules. 21,8(4).

  • Maunula, L., Kaupke, A., Vasickova, P., Söderberg, K., Kozyra, I., Lazic, S., van der Poel, W. H., et al. (2013). Tracing enteric viruses in the European berry fruit supply chain. International Journal of Food Microbiology, 167(2), 177–185.

    Article  Google Scholar 

  • Nieto, G. (2017). Biological activities of three essential oils of the Lamiaceae family. Medicines (Basel), 4(3), 63.

    Article  Google Scholar 

  • Nolkemper, S., Reichling, J., Stintzing, F. C., Carle, R., & Schnitzler, P. (2006). Antiviral effect of aqueous extracts from species of the Laminaceae Family against Herpes simplex Virus type 1 and type 2 in vitro. Planta Medica, 72(15), 1378–1382.

    CAS  Article  Google Scholar 

  • Ozogul, Y., Kuley, E., Ucar, Y., & Ozogul, F. (2015). Antimicrobial impacts of essential oils on food borne-pathogens. Recent Patents on Food, Nutrition & Agriculture, 7(1), 53–61.

    CAS  Article  Google Scholar 

  • Piątkowska, E., & Rusiecka-Ziółkowska, J. (2016). Influence of essential oils on infectious agents. Advances in Clinical and Experimental Medicine, 25(5), 989–995.

    Article  Google Scholar 

  • Randazzo, W., Falco, I., Aznar, R., & Sànchez, G. (2017). Effect of green tea extract on enteric viruses and its application as natural sanitizer. Food microbiology, 66, 150–156.

    CAS  Article  Google Scholar 

  • Reed, L. J., & Muench, H. (1938). A simple method of estimating fifty per cent endpoint. American Journal of Hygiene, 27(3), 493–497.

    Google Scholar 

  • Reichling, J., Schnitzler, P., Suschke, U., & Saller, R. (2009). Essential oils of aromatic plants with antibacterial, antifungal, antiviral, and cytotoxic properties: an overview. Forschende Komplementarmedizin, 16(2), 79–90.

    PubMed  Google Scholar 

  • Richardson, S. (1998). Drinking water disinfection by-products. In: Encyclopedia of environmental analysis and remediation. In R. A. Meyers (Ed.), Encyclopedia of environmental analysis and remediation (Vol. 3, pp. 1398–1421). New York: Wiley.

    Google Scholar 

  • Sánchez, C., Aznar, R., & Sánchez, G. (2015). The effect of carvacrol on enteric viruses. International Journal of Food Microbiology, 192, 72–76.

    Article  Google Scholar 

  • Sánchez, G. (2015). Processing strategies to inactivate hepatitis A virus in food products: a critical review. Comprehensive Reviews in Food Science and Food Safety, 14(6), 771–784.

    Article  Google Scholar 

  • Sánchez, G., & Aznar, R. (2015). Evaluation of natural compounds of plant origin for inactivation of enteric viruses. Food and Environmental Virology, 7(2), 183–187.

    Article  Google Scholar 

  • Sánchez, G., Bosch, A., & Pintó, R. M. (2007). Hepatitis A virus detection in food: current and future prospects. Letters in Applied Microbiology, 45(1), 1–5.

    Article  Google Scholar 

  • Satyal, P., Jones, T. H., Lopez, E. M., McFeeters, R. L., Ali, N. A., Mansi, I., Al-Kaf, A. G., & Setzer, W. N. (2017). Chemotypic characterization and biological activity of Rosmarinus officinalis. Foods, 6(3), 20.

    Article  Google Scholar 

  • Scavia, G., Alfonsi, V., Taffon, S., Escher, M., Bruni, R., Medici, D., Pasquale, S. D., et al. National Italian Task Force On Hepatitis A (2017). A large prolonged outbreak of hepatitis A associated with consumption of frozen berries, Italy, 2013-14. Journal of medical microbiology, 66(3), 342–349.

    Article  Google Scholar 

  • Serrano, M., Martinez-Romero, D., Guillén, F., Valverde, J. M., Zapata, P. J., Castillo, S., & Valero, D. (2008). The addition of essential oils to MAP as a tool to maintain the overall quality of fruits. Trends in Food Science & Technology, 19, 464e471.

    Article  Google Scholar 

  • Sirocchi, V., Devlieghere, F., Peelman, N., Sagratini, G., Maggi, F., Vittori, S., & Ragaert, P. (2017). Effect of Rosmarinus officinalis L. essential oil combined with different packaging conditions to extend the shelf life of refrigerated beef meat. Food Chemistry, 221, 1069–1076.

    CAS  Article  Google Scholar 

  • Su, X., & D’Souza, D. H. (2011). Grape seed extract for control of human enteric viruses. Applied and Environmental Microbiology, 77(12), 3982–3987.

    CAS  Article  Google Scholar 

  • Tavoschi, L., Severi, E., Niskanen, T., Boelaert, F., Rizzi, V., Liebana, E., Dias, G., et al. (2015). Food-borne diseases associated with frozen berries consumption: a historical perspective, European Union, 1983 to 2013. Euro Surveillance, 20(29), 21193.

    CAS  PubMed  Google Scholar 

  • Tullio, V., Mandras, N., Allizond, V., Nostro, V., Roana, J., Merlino, C., Banche, et al. (2012). Positive interaction of Thyme (Red) essential oil with human ply-morphonuclear granulocytes in eradicating intracellular Candida albicans. Planta Medica, 78(15), 1633–1635.

    CAS  Article  Google Scholar 

  • Tzortzakis, N. G. (2007). Maintaining postharvest quality of fresh produce with volatile compounds. Innovative Food Science & Emerging Technologies, 8, 111e116.

    Google Scholar 

  • Ulukanli, Z., & Oz, A. T. (2015). The effect of oleum myrtle on the fruit quality of strawberries during MAP storage. Journal of Food Science and Technology, 52(5), 2860–2868.

    CAS  Article  Google Scholar 

  • Vergis, J., Gokulakrishnan, P., Agarwal, R. K., & Kumar, A. (2015). Essential oils as natural food antimicrobial agents: a review. Critical Review in Food Science & Nutrition, 55(10), 1320–1323.

    CAS  Article  Google Scholar 

  • Vicente, R. A., & Sozzi, G. (2007). Ripening and postharvest storage of ‘soft fruits’. Fruit, Vegetable and Cereal Science and Biotechnology, 1, 95–103.

    Google Scholar 

  • Yezli, S., & Otter, J. (2011). Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment. Food and Environmental Virology, 3(1), 1–30.

    Google Scholar 

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Acknowledgements

This study was supported by Grants from the Italian Ministry of Health (IZS PLV 14/13).

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Correspondence to Laura Serracca.

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Battistini, R., Rossini, I., Ercolini, C. et al. Antiviral Activity of Essential Oils Against Hepatitis A Virus in Soft Fruits. Food Environ Virol 11, 90–95 (2019). https://doi.org/10.1007/s12560-019-09367-3

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  • DOI: https://doi.org/10.1007/s12560-019-09367-3

Keywords

  • Inactivation
  • Berries
  • Hepatitis A virus
  • Essential oils