Thyme essential oil inhibits intracellular replication of CyHV-3 and inactivates extracellular virus. An in vitro study.


Journal

Journal of fish diseases
ISSN: 1365-2761
Titre abrégé: J Fish Dis
Pays: England
ID NLM: 9881188

Informations de publication

Date de publication:
Jun 2023
Historique:
revised: 20 02 2023
received: 30 09 2022
accepted: 23 02 2023
medline: 8 5 2023
pubmed: 15 3 2023
entrez: 14 3 2023
Statut: ppublish

Résumé

Cyprinid herpesvirus 3 (CyHV-3) can induce up to 100% mortality among carp populations. To date, there has been no safe method to prevent the consequences of the activity of CyHV-3. Thyme is widely used in cooking due to its flavour. Both thyme and thyme essential oil (TEO) are used in traditional herbal medicine, mainly to treat respiratory system disorders. In this study, TEO containing predominantly cymene and thymol was applied to explore its antiviral effect. The toxicity of TEO was examined in MTT and crystal violet assays. The anti-CyHV-3 activity of TEO in the intracellular and extracellular stages of the viral replication cycle was explored in a plaque assay and TaqMan qPCR. TEO interfered with the intracellular stages of the CyHV-3 replication cycle with selectivity indexes (SI) of around 5. It also displayed virucidal activity in a dose- and time-dependent manner. Two-hour preincubation of CyHV-3 with TEO generated SI, ranging from 13.37 to 18.47 depending on cell line and method of examination. Preincubation of cells with TEO at a safe concentration did not decrease the intracellular viral DNA copy number, which suggests that TEO does not disturb the attachment of the virus to the cells. Further research regarding the antiviral activity of compounds of TEO is required in order to indicate the most potent molecules that could be considered candidates for application in aquaculture.

Identifiants

pubmed: 36916652
doi: 10.1111/jfd.13777
doi:

Substances chimiques

Oils, Volatile 0
thyme oil 2UK410MY6B
Antiviral Agents 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

663-677

Subventions

Organisme : Institute of Agricultural and Food Biotechnology
Organisme : Polish Ministry of Sciences and Higher Education
Organisme : Polska Akademia Nauk

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Ababneh, M., Hananeh, W., & Alzghoul, M. (2020). Mass mortality associated with koi herpesvirus in common carp in Iraq. Heliyon, 6(8), e04827. https://doi.org/10.1016/j.heliyon.2020.e04827
Amoros, M., Simões, C. M., Girre, L., Sauvager, F., & Cormier, M. (1992). Synergistic effect of flavones and flavonols against herpes simplex virus type 1 in cell culture. Comparison with the antiviral activity of propolis. Journal of Natural Products, 55(12), 1732-1740. https://doi.org/10.1021/np50090a003
Armaka, M., Papanikolaou, E., Sivropoulou, A., & Arsenakis, M. (1999). Antiviral properties of isoborneol, a potent inhibitor of herpes simplex virus type 1. Antiviral Research, 43(2), 79-92. https://doi.org/10.1016/s0166-3542(99)00036-4
Astani, A., Reichling, J., & Schnitzler, P. (2010). Comparative study on the antiviral activity of selected monoterpenes derived from essential oils. Phytotherapy Research: PTR, 24(5), 673-679. https://doi.org/10.1002/ptr.2955
Astani, A., Reichling, J., & Schnitzler, P. (2011). Screening for antiviral activities of isolated compounds from essential oils. Evidence-Based Complementary and Alternative Medicine, 2011, 253643. https://doi.org/10.1093/ecam/nep187
Astani, A., & Schnitzler, P. (2014). Antiviral activity of monoterpenes beta-pinene and limonene against herpes simplex virus in vitro. Iranian Journal of Microbiology, 6(3), 149-155.
Awouafack, M. D., McGaw, L. J., Gottfried, S., Mbouangouere, R., Tane, P., Spiteller, M., & Eloff, J. N. (2013). Antimicrobial activity and cytotoxicity of the ethanol extract, fractions and eight compounds isolated from Eriosema robustum (Fabaceae). BMC Complementary and Alternative Medicine, 13, 289. https://doi.org/10.1186/1472-6882-13-289
Bailer, S. M. (2017). Venture from the interior-herpesvirus pUL31 escorts capsids from Nucleoplasmic replication compartments to sites of primary envelopment at the inner nuclear membrane. Cell, 6(4), E46. https://doi.org/10.3390/cells6040046
Balahbib, A., El Omari, N., Hachlafi, N. E., Lakhdar, F., El Menyiy, N., Salhi, N., Mrabti, H. N., Bakrim, S., Zengin, G., & Bouyahya, A. (2021). Health beneficial and pharmacological properties of p-cymene. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 153, 112259. https://doi.org/10.1016/j.fct.2021.112259
Bergmann, S. M., Monro, E. S., & Kempter, J. (2017). Can water disinfection prevent the transmission of infectious koi herpesvirus to naïve carp? - A case report. Journal of Fish Diseases, 40(7), 885-893. https://doi.org/10.1111/jfd.12568
Biron, K. K. (2007). Candidate anti-herpesviral drugs; mechanisms of action and resistance. In A. Arvin, G. Campadelli-Fiume, E. Mocarski, P. S. Moore, B. Roizman, R. Whitley, & K. Yamanishi (Eds.), Human herpesviruses: Biology, therapy, and Immunoprophylaxis. Cambridge University Press. http://www.ncbi.nlm.nih.gov/books/NBK47396/
Boutier, M., Gao, Y., Donohoe, O., & Vanderplasschen, A. (2019). Current knowledge and future prospects of vaccines against cyprinid herpesvirus 3 (CyHV-3). Fish & Shellfish Immunology, 93, 531-541. https://doi.org/10.1016/j.fsi.2019.07.079
Boutier, M., Ronsmans, M., Ouyang, P., Fournier, G., Reschner, A., Rakus, K., Wilkie, G. S., Farnir, F., Bayrou, C., Lieffrig, F., Li, H., Desmecht, D., Davison, A. J., & Vanderplasschen, A. (2015). Rational development of an attenuated recombinant cyprinid herpesvirus 3 vaccine using prokaryotic mutagenesis and in vivo bioluminescent imaging. PLoS Pathogens, 11(2), e1004690. https://doi.org/10.1371/journal.ppat.1004690
Cano, I., Mulhearn, B., Akter, S., & Paley, R. (2020). Seroconversion and skin mucosal parameters during koi herpesvirus shedding in common carp, Cyprinus carpio. International Journal of Molecular Sciences, 21(22), E8482. https://doi.org/10.3390/ijms21228482
Catella, C., Camero, M., Lucente, M. S., Fracchiolla, G., Sblano, S., Tempesta, M., Martella, V., Buonavoglia, C., & Lanave, G. (2021). Virucidal and antiviral effects of Thymus vulgaris essential oil on feline coronavirus. Research in Veterinary Science, 137, 44-47. https://doi.org/10.1016/j.rvsc.2021.04.024
Cos, P., Vlietinck, A. J., Berghe, D. V., & Maes, L. (2006). Anti-infective potential of natural products: How to develop a stronger in vitro ‘proof-of-concept’. Journal of Ethnopharmacology, 106(3), 290-302. https://doi.org/10.1016/j.jep.2006.04.003
Davison, A. J., Eberle, R., Ehlers, B., Hayward, G. S., McGeoch, D. J., Minson, A. C., Pellett, P. E., Roizman, B., Studdert, M. J., & Thiry, E. (2009). The order Herpesvirales. Archives of Virology, 154(1), 171-177. https://doi.org/10.1007/s00705-008-0278-4
Eide, K. E., Miller-Morgan, T., Heidel, J. R., Kent, M. L., Bildfell, R. J., LaPatra, S., Watson, G., & Jin, L. (2011). Investigation of koi herpesvirus latency in koi▿. Journal of Virology, 85(10), 4954-4962. https://doi.org/10.1128/JVI.01384-10
El Euony, O. I., Elblehi, S. S., Abdel-Latif, H. M., Abdel-Daim, M. M., & El-Sayed, Y. S. (2020). Modulatory role of dietary Thymus vulgaris essential oil and Bacillus subtilis against thiamethoxam-induced hepatorenal damage, oxidative stress, and immunotoxicity in African catfish (Clarias garipenus). Environmental Science and Pollution Research International, 27(18), 23108-23128. https://doi.org/10.1007/s11356-020-08588-5
European Medicines Agency. (2020a). Assessment report on Thymus vulgaris L., Thymus zygis L., aetheroleum. https://www.ema.europa.eu/en/documents/herbal-report/final-assessment-report-thymus-vulgaris-l-thymus-zygis-l-aetheroleum-revision-1_en.pdf
European Medicines Agency. (2020b). European Union herbal monograph Thymus vulgaris L., Thymus zygis L., aetheroleum. https://www.ema.europa.eu/en/documents/herbal-monograph/final-european-union-herbal-monograph-thymus-vulgaris-l-thymus-zygis-l-aetheroleum-revision-1_en.pdf
Feriotto, G., Marchetti, N., Costa, V., Beninati, S., Tagliati, F., & Mischiati, C. (2018). Chemical composition of essential oils from Thymus vulgaris, Cymbopogon citratus, and Rosmarinus officinalis, and their effects on the HIV-1 tat protein function. Chemistry & Biodiversity, 15(2), e1700436. https://doi.org/10.1002/cbdv.201700436
Foe, F. M. C., Nyegue, M. A., Kamdem, S. L. S., Essama, R. H. S., & Etoa, F. (2016). Chemical composition, antioxidant effects and antimicrobial activities of some spices' essential oils on food pathogenic bacteria. African Journal of Biotechnology, 15(16), 649-656. https://doi.org/10.4314/ajb.v15i16
Food and Drug Administration Agency. (2023). Code of Federal Regulations, Title 21, Chapter I, Subchapter B, Part 182, § 182.20 Substances Generally Recognized as Safe. https://www.ecfr.gov/current/title-21/chapter-I/subchapter-B/part-182/subpart-A/section-182.20
Ghafarifarsani, H., Hoseinifar, S. H., Javahery, S., & Van Doan, H. (2022). Effects of dietary vitamin C, thyme essential oil, and quercetin on the immunological and antioxidant status of common carp (Cyprinus carpio). Aquaculture, 553, 738053. https://doi.org/10.1016/j.aquaculture.2022.738053
Ghafarifarsani, H., Kachuei, R., & Imani, A. (2021). Dietary supplementation of garden thyme essential oil ameliorated the deteriorative effects of aflatoxin B1 on growth performance and intestinal inflammatory status of rainbow trout (Oncorhynchus mykiss). Aquaculture, 531, 735928. https://doi.org/10.1016/j.aquaculture.2020.735928
Giannenas, I., Triantafillou, E., Stavrakakis, S., Margaroni, M., Mavridis, S., Steiner, T., & Karagouni, E. (2012). Assessment of dietary supplementation with carvacrol or thymol containing feed additives on performance, intestinal microbiota and antioxidant status of rainbow trout (Oncorhynchus mykiss). Aquaculture, 350-353, 26-32. https://doi.org/10.1016/j.aquaculture.2012.04.027
Gilad, O., Yun, S., Adkison, M. A., Way, K., Willits, N. H., Bercovier, H., & Hedrick, R. P. (2003). Molecular comparison of isolates of an emerging fish pathogen, koi herpesvirus, and the effect of water temperature on mortality of experimentally infected koi. The Journal of General Virology, 84(Pt 10), 2661-2667. https://doi.org/10.1099/vir.0.19323-0
Gilad, O., Yun, S., Zagmutt-Vergara, F. J., Leutenegger, C. M., Bercovier, H., & Hedrick, R. P. (2004). Concentrations of a koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Diseases of Aquatic Organisms, 60(3), 179-187. https://doi.org/10.3354/dao060179
Hedrick, R. P., Gilad, O., Yun, S., Spangenberg, J., Marty, G. D., Nordhausen, R. W., Kebus, M., Bercovier, H., & Eldar, A. (2000). A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Journal of Aquatic Animal Health, 12, 44-57. https://doi.org/10.1577/1548-8667(2000)012<0044:AHAWMM>2.0.CO;2
Hudaib, M., Speroni, E., Di Pietra, A. M., & Cavrini, V. (2002). GC/MS evaluation of thyme (Thymus vulgaris L.) oil composition and variations during the vegetative cycle. Journal of Pharmaceutical and Biomedical Analysis, 29(4), 691-700. https://doi.org/10.1016/s0731-7085(02)00119-x
Ilouze, M., Dishon, A., & Kotler, M. (2012). Down-regulation of the cyprinid herpesvirus-3 annotated genes in cultured cells maintained at restrictive high temperature. Virus Research, 169(1), 289-295. https://doi.org/10.1016/j.virusres.2012.07.013
Kaloustian, J., Abou, L., Mikail, C., Amiot, M. J., & Portugal, H. (2005). Southern French thyme oils: Chromatographic study of chemotypes. Journal of the Science of Food and Agriculture, 85(14), 2437-2444. https://doi.org/10.1002/jsfa.2274
Kim, J.-E., Lee, J.-E., Huh, M.-J., Lee, S.-C., Seo, S.-M., Kwon, J. H., & Park, I.-K. (2019). Fumigant antifungal activity via reactive oxygen species of Thymus vulgaris and Satureja hortensis essential oils and constituents against Raffaelea quercus-mongolicae and Rhizoctonia solani. Biomolecules, 9(10), 561. https://doi.org/10.3390/biom9100561
Kong, Y.-D., Li, M., Xia, C.-G., Zhao, J., Niu, X., Shan, X.-F., & Wang, G.-Q. (2021). The optimum thymol requirement in diets of Channa argus: Effects on growth, antioxidant capability, immune response and disease resistance. Aquaculture Nutrition, 27(3), 712-722. https://doi.org/10.1111/anu.13217
Kowalczyk, A., Przychodna, M., Sopata, S., Bodalska, A., & Fecka, I. (2020). Thymol and thyme essential oil-new insights into selected therapeutic applications. Molecules (Basel, Switzerland), 25(18), E4125. https://doi.org/10.3390/molecules25184125
Lai, W.-L., Chuang, H.-S., Lee, M.-H., Wei, C.-L., Lin, C.-F., & Tsai, Y.-C. (2012). Inhibition of herpes simplex virus type 1 by thymol-related monoterpenoids. Planta Medica, 78(15), 1636-1638. https://doi.org/10.1055/s-0032-1315208
Madia, V. N., Toscanelli, W., De Vita, D., De Angelis, M., Messore, A., Ialongo, D., Scipione, L., Tudino, V., D'Auria, F. D., Di Santo, R., Garzoli, S., Stringaro, A., Colone, M., Marchetti, M., Superti, F., Nencioni, L., & Costi, R. (2022). Ultrastructural damages to H1N1 influenza virus caused by vapor essential oils. Molecules, 27(12), 3718. https://doi.org/10.3390/molecules27123718
Marchese, A., Arciola, C. R., Barbieri, R., Silva, A. S., Nabavi, S. F., Tsetegho Sokeng, A. J., Izadi, M., Jafari, N. J., Suntar, I., Daglia, M., & Nabavi, S. M. (2017). Update on monoterpenes as antimicrobial agents: A particular focus on p-cymene. Materials (Basel, Switzerland), 10(8), E947. https://doi.org/10.3390/ma10080947
Marzec, M., Polakowski, C., Chilczuk, R., & Kolodziej, B. (2010). Evaluation of essential oil content, its chemical composition and price of thyme (Thymus vulgaris L.) raw material available in Poland. Herba Polonica, 56(3), 37-52. http://agro.icm.edu.pl/agro/element/bwmeta1.element.agro-60dd1776-d464-47e7-99ca-ffd68ef59bb7
McGimpsey, J. A., Douglas, M. H., Van Klink, J. W., Beauregard, D. A., & Perry, N. B. (1994). Seasonal variation in essential oil yield and composition from naturalized Thymus vulgaris L. in New Zealand. Flavour and Fragrance Journal, 9(6), 347-352. https://doi.org/10.1002/ffj.2730090613
Miwa, S., Ito, T., & Sano, M. (2007). Morphogenesis of koi herpesvirus observed by electron microscopy. Journal of Fish Diseases, 30(12), 715-722. https://doi.org/10.1111/j.1365-2761.2007.00850.x
Miyazaki, T., Kuzuya, Y., Yasumoto, S., Yasuda, M., & Kobayash, I. T. (2008). Histopathological and ultrastructural features of koi herpesvirus (KHV)-infected carp Cyprinus carpio, and the morphology and morphogenesis of KHV. Disease of Aquatic Organisms, 80, 1-11. https://doi.org/10.3354/dao01929
Nagoor Meeran, M. F., Javed, H., Al Taee, H., Azimullah, S., & Ojha, S. K. (2017). Pharmacological properties and molecular mechanisms of thymol: Prospects for its therapeutic potential and pharmaceutical development. Frontiers in Pharmacology, 8, 380. https://doi.org/10.3389/fphar.2017.00380
Navarrete, P., Toledo, I., Mardones, P., Opazo, R., Espejo, R., & Romero, J. (2010). Effect of Thymus vulgaris essential oil on intestinal bacterial microbiota of rainbow trout, Oncorhynchus mykiss (Walbaum) and bacterial isolates. Aquaculture Research, 41(10), e667-e678. https://doi.org/10.1111/j.1365-2109.2010.02590.x
Patil, S. M., Ramu, R., Shirahatti, P. S., Shivamallu, C., & Amachawadi, R. G. (2021). A systematic review on ethnopharmacology, phytochemistry and pharmacological aspects of Thymus vulgaris Linn. Heliyon, 7(5), e07054. https://doi.org/10.1016/j.heliyon.2021.e07054
Pavela, R., Vrchotová, N., & Tríska, J. (2009). Mosquitocidal activities of thyme oils (Thymus vulgaris L.) against Culex quinquefasciatus (Diptera: Culicidae). Parasitology Research, 105(5), 1365-1370. https://doi.org/10.1007/s00436-009-1571-1
Poulose, A. J., & Croteau, R. (1978). Biosynthesis of aromatic monoterpenes: Conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L. Archives of Biochemistry and Biophysics, 187(2), 307-314. https://doi.org/10.1016/0003-9861(78)90039-5
Rakus, K., Ouyang, P., Boutier, M., Ronsmans, M., Reschner, A., Vancsok, C., Jazowiecka-Rakus, J., & Vanderplasschen, A. (2013). Cyprinid herpesvirus 3: An interesting virus for applied and fundamental research. Veterinary Research, 44(1), 1-16. https://doi.org/10.1186/1297-9716-44-85
Rakus, K. Ł., Irnazarow, I., Adamek, M., Palmeira, L., Kawana, Y., Hirono, I., Kondo, H., Matras, M., Steinhagen, D., Flasz, B., Brogden, G., Vanderplasschen, A., & Aoki, T. (2012). Gene expression analysis of common carp (Cyprinus carpio L.) lines during cyprinid herpesvirus 3 infection yields insights into differential immune responses. Developmental and Comparative Immunology, 37(1), 65-76. https://doi.org/10.1016/j.dci.2011.12.006
Reichling, J. (2022). Antiviral and Virucidal properties of essential oils and isolated compounds-A scientific approach. Planta Medica, 88(8), 587-603. https://doi.org/10.1055/a-1382-2898
Reichling, J., Suschke, U., Schneele, J., & Geiss, H. K. (2006). Antibacterial activity and irritation potential of selected essential oil components - Structure-activity relationship. Natural Product Communications, 1(11), 1934578X0600101. https://doi.org/10.1177/1934578X0600101116
Riss, T. L., Moravec, R. A., Niles, A. L., Duellman, S., Benink, H. A., Worzella, T. J., & Minor, L. (2013). Cell viability assays. In S. Markossian, A. Grossman, K. Brimacombe, M. Arkin, D. Auld, C. P. Austin, J. Baell, T. D. Y. Chung, N. P. Coussens, J. L. Dahlin, V. Devanarayan, T. L. Foley, M. Glicksman, M. D. Hall, J. V. Haas, S. R. J. Hoare, J. Inglese, P. W. Iversen, S. C. Kales, et al. (Eds.), Assay guidance manual (pp. 1-31). Eli Lilly & Company and the National Center for Advancing Translational Sciences. http://www.ncbi.nlm.nih.gov/books/NBK144065/
Romanenko, E. P., & Tkachev, A. V. (2006). Identification by GC-MS of cymene isomers and 3,7,7-trimethylcyclohepta-1,3,5-triene in essential oils. Chemistry of Natural Compounds, 42(6), 699-701. https://doi.org/10.1007/s10600-006-0256-6
Ronen, A., Perelberg, A., Abramowitz, J., Hutoran, M., Tinman, S., Bejerano, I., Steinitz, M., & Kotler, M. (2003). Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine, 21, 4677-4684. https://doi.org/10.1016/S0264-410X(03)00523-1
Saotome, K., Morita, H., & Umeda, M. (1989). Cytotoxicity test with simplified crystal violet staining method using microtitre plates and its application to injection drugs. Toxicology in Vitro: An International Journal Published in Association with BIBRA, 3(4), 317-321. https://doi.org/10.1016/0887-2333(89)90039-8
Schmidt, E., Wanner, J., Hiiferl, M., Jirovetz, L., Buchbauer, G., Gochev, V., Girova, T., Stoyanova, A., & Geissler, M. (2012). Chemical composition, olfactory analysis andantibacterial activity of Thymus vulgaris chemotypes geraniol, 4-thujanol/terpinen-4-ol, thymol and linalool cultivated in southern France. Natural ProductCommunications, 7(8), 1095-1098.
Schnitzler, P., Koch, C., & Reichling, J. (2007). Susceptibility of drug-resistant clinical herpes simplex virus type 1 strains to essential oils of ginger, thyme, hyssop, and sandalwood. Antimicrobial Agents and Chemotherapy, 51(5), 1859-1862. https://doi.org/10.1128/AAC.00426-06
Sharifi-Rad, J., Salehi, B., Schnitzler, P., Ayatollahi, S. A., Kobarfard, F., Fathi, M., Eisazadeh, M., & Sharifi-Rad, M. (2017). Susceptibility of herpes simplex virus type 1 to monoterpenes thymol, carvacrol, p-cymene and essential oils of Sinapis arvensis L., Lallemantia royleana Benth. and Pulicaria vulgaris Gaertn. Cellular and Molecular Biology (Noisy-Le-Grand, France), 63(8), 42-47. https://doi.org/10.14715/cmb/2017.63.8.10
Shin, J., Na, K., Shin, S., Seo, S.-M., Youn, H. J., Park, I.-K., & Hyun, J. (2019). Biological activity of thyme white essential oil stabilized by cellulose nanocrystals. Biomolecules, 9(12), 799. https://doi.org/10.3390/biom9120799
Sönmez, A. Y., Bilen, S., Alak, G., Hisar, O., Yanık, T., & Biswas, G. (2015). Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint and thyme oils. Fish Physiology and Biochemistry, 41(1), 165-175. https://doi.org/10.1007/s10695-014-0014-9
Šudomová, M., Berchová-Bímová, K., Mazurakova, A., Šamec, D., Kubatka, P., & Hassan, S. T. S. (2022). Flavonoids target human herpesviruses that infect the nervous system: Mechanisms of action and therapeutic insights. Viruses, 14(3), 592. https://doi.org/10.3390/v14030592
Sutili, F. J., Gatlin, D. M., III, Heinzmann, B. M., & Baldisserotto, B. (2018). Plant essential oils as fish diet additives: Benefits on fish health and stability in feed. Reviews in Aquaculture, 10(3), 716-726. https://doi.org/10.1111/raq.12197
Troszok, A., Kolek, L., Szczygieł, J., Wawrzeczko, J., Borzym, E., Reichert, M., Kamińska, T., Ostrowski, T., Jurecka, P., Adamek, M., Rakus, K., & Irnazarow, I. (2018). Acyclovir inhibits cyprinid herpesvirus 3 multiplication in vitro. Journal of Fish Diseases, 41(11), 1709-1718. https://doi.org/10.1111/jfd.12880
Troszok, A., Napora-Rutkowski, Ł., & Pilarczyk, A. (2021). Experimental methods of an anti-CyHV-3 directed campaign - Prospects, efficiency and safety. Aquaculture, 544, 737090. https://doi.org/10.1016/j.aquaculture.2021.737090
Tsuchiya, Y., Shimizu, M., Hiyama, Y., Itoh, K., Hashimoto, Y., Nakayama, M., Horie, T., & Morita, N. (1985). Antiviral activity of natural occurring flavonoids in vitro. Chemical & Pharmaceutical Bulletin, 33(9), 3881-3886. https://doi.org/10.1248/cpb.33.3881
Uchii, K., Minamoto, T., Honjo, M. N., & Kawabata, Z. (2014). Seasonal reactivation enables cyprinid herpesvirus 3 to persist in a wild host population. FEMS Microbiology Ecology, 87(2), 536-542. https://doi.org/10.1111/1574-6941.12242
Uchii, K., Telschow, A., Minamoto, T., Yamanaka, H., Honjo, M. N., Matsui, K., & Kawabata, Z. (2011). Transmission dynamics of an emerging infectious disease in wildlife through host reproductive cycles. The ISME Journal, 5(2), 244-251. https://doi.org/10.1038/ismej.2010.123
Vimalanathan, S., & Hudson, J. B. (2014). Anti-influenza virus activity of essential oils and vapors. American Journal of Essential Oils and Natural Products, 2, 47-53.
Zambonelli, A., D'Aulerio, A. Z., Severi, A., Benvenuti, S., Maggi, L., & Bianchi, A. (2004). Chemical composition and fungicidal activity of commercial essential oils of Thymus vulgaris L. Journal of Essential Oil Research, 16(1), 69-74. https://doi.org/10.1080/10412905.2004.9698653

Auteurs

Agnieszka Troszok (A)

Polish Academy of Sciences, Institute of Ichthyobiology and Aquaculture in Golysz, Chybie, Poland.

Marek Roszko (M)

Institute of Agricultural and Food Biotechnology, State Research Institute, Warsaw, Poland.

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