Antiviral and Virucidal Properties of Essential Oils and Isolated Compounds – A Scientific Approach

Abstract

Essential oils and isolated essential oil compounds are known to exert various pharmacological effects, such as antibacterial, antifungal, antiviral, anti-inflammatory, anti-immunomodulatory, antioxidant, and wound healing effects. Based on selected articles, this review deals with the potential antiviral and virucidal activities of essential oils and essential oil compounds together with their mechanism of action as well as in silico studies involving viral and host cell-specific target molecules that are indispensable for virus cell adsorption, penetration, and replication. The reported in vitro and in vivo studies highlight the baseline data about the latest findings of essential oils and essential oil compounds antiviral and virucidal effects on enveloped and non-enveloped viruses, taking into account available biochemical and molecular biological tests. The results of many in vitro studies revealed that several essential oils and essential oil compounds from different medicinal and aromatic plants are potent antiviral and virucidal agents that inhibit viral progeny by blocking different steps of the viral infection/replication cycle of DNA and RNA viruses in various host cell lines. Studies in mice infected with viruses causing respiratory diseases showed that different essential oils and essential oil compounds were able to prolong the life of infected animals, reduce virus titers in brain and lung tissues, and significantly inhibit the synthesis of proinflammatory cytokines and chemokines. In addition, some in vitro studies on hydrophilic nano-delivery systems encapsulating essential oils/essential oil compounds exhibited a promising way to improve the chemical stability and enhance the water solubility, bioavailabilty, and antiviral efficacy of essential oils and essential oil compounds.

Key words

virus - virion - essential oil - essential oil compound - antiviral activity - virucidal effect

Publication History

Received: 26 January 2021

Accepted after revision: 04 May 2021

Article published online:
18 June 2021

• References

• 1 Zhong P, Agosto LM, Munro JB, Mothes W. Cell-to-cell transmission of viruses. Curr Opin Virol 2013; 3: 44-50
• 2 Nasir A, Romero-Severson E, Claverie JM. Investigating the concept and origin of viruses. Trends Microbiol 2020; 28: 959-967
• 3 Jones JE, Le Sage V, Lakdawala SS. Viral and host heterogeneity and their effects on the viral life cycle. Nat Rev Microbiol 2021; 19: 272-282
• 4 Rumlova M, Ruml T. In vitro methods for testing antiviral drugs. Biotechnol Adv 2018; 36: 557-576
• 5 Louten J. Essential human Virology. Chapter 4: Virus Replication. In: Louten J. Virus Replication. Amsterdam, London: Elsevier, Academic Press; 2016: 49-70
• 6 Aoki-Utsubo C, Chen M, Hotta H. Time-of-addition and temperature-shift assays to determine particular step(s) in the viral life cycle that is blocked by antiviral substance(s). BioProtoc 2018; 8: 1-12
• 7 De Clercq E, Lia G. Approved antiviral drugs over the past 50 years. Clin Microbiol Rew 2016; 29: 695-747
• 8 Bright KR, Gilling DH. Natural virucidal Compounds in Foods. In: Goyal S, Cannon J. eds. Viruses in Foods. Food Microbiology and Food Safety. Cham: Springer; 2016: 449-469
• 9 Jones ST. How materials can beat a virus. J Mater Sci 2020; 55: 9148-9151
• 10 Kumari CBC, Nagaveni HC. Essential oils of aromatic plants with antifungal, antibacterial, antiviral, and cytotoxic properties – an overview. J Pharmacogn Phytochem 2018; 7: 278-282
• 11 Tariq S, Wani S, Rasool W, Bhat M, Prabhakar A, Shalla A, Rather M. A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microb Pathog 2019; 134: 103580
• 12 Ma L, Yao L. Antiviral effects of plant-derived essential oils and their components: An updated review. Molecules 2020; 25: 2627
• 13 Reichling J. Plant-microbe Interaction and secondary Metabolites with antiviral, antibacterial and antifungal Properties. In: Wink W. ed. Functions and Biotechnology of Plant secondary Metabolites. West Sussex, United Kingdom: Wiley-Blackwell; 2010: 214-347
• 14 Swamy MK, Akhtar MS, Sinniah UR. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: An updated review. Evid Based Complement Alternat Med 2016; 2016: 3012462
• 15 Setzer WN. Essential oils as complementary and alternative medicines for the treatment of influenza. Am J Essent Oil Nat Prod 2016; 4: 16-22
• 16 Ebenezer KS, Manivannan R, Punniyamoorthy A, Tamilselvan C. Plant secondary metabolites of antiviral properties a rich medicinal source for drug discovery: A mini review. J Drug Deliv Ther 2019; 9: 161-167
• 17 Lelešius R, Karpovaitė A, Mickienė R, Drevinskas T, Tiso N, Ragažinskienė O, Kubilienė L, Maruška A, Šalomskas A. In vitro antiviral activity of fifteen plant extracts against avian infectious bronchitis virus. BMC Vet Res 2019; 15: 178
• 18 Ben-Shabat S, Yarmolinsky L, Porat D, Dahancorresponding A. Antiviral effect of phytochemicals from medicinal plants: Applications and drug delivery strategies. Drug Deliv Transl Res 2020; 10: 354-367
• 19 Ha TKQ, Lee BW, Nguyen NH, Cho HM, Venkatesan T, Doan TP, Kim E, Oh WK. Antiviral activities of compounds isolated from Pinus densiflora (pine tree) against the influenza A virus. Biomolecules 2020; 10: 711
• 20 Kaushik S, Kaushik S, Sharma V, Yadav JP. Antiviral and therapeutic uses of medicinal plants and their derivatives against dengue viruses. Phcog Rev 2018; 12: 177-185
• 21 Patra JK, Das G, Bose S, Banerjee S, Vishnuprasad C, Rodrigues-Torres MP, Shin HS. Star anise (lllicium verum): Chemical compounds, antiviral properties, and clinical relevance. Phytother Res 2020; 34: 1248-1267
• 22 Wink M. Potential of DNA intercalating alkaloids and other plant secondary metabolites against SARS-CoV-2 causing COVID-19. Diversity 2020; 175: 1-12
• 23 Chouhan S, Sharma K, Guleria S. Antimicrobial activity of some essential oils-present status and future perspectives. Medicines 2017; 4: 58
• 24 Paul S, Hmar EBL, Zothantluanga JH, Sharma HK. Essential oils: A review on their salient biological activities and major delivery strategies. Science Vision 2020; 20: 54-71
• 25 Reichling J. Anti-biofilm and virulence-factor reducing activities of essential oils and oil components as possible option for bacterial infection control. Planta Med 2020; 86: 520-537
• 26 Juergens UR, Dethlefsen U, Steinkamp G, Gillissen G, Repges R, Vetter H. Anti-infammatory activity of 1.8-cineol (eucalyptol) in bronchial asthma: A double-blind placebo-controlled trial. Respiratory Med 2003; 97: 250-256
• 27 Juergens LJ, Worth H, Juergens UR. New perspectives for mucolytic, anti-inflammatory and adjunctive therapy with 1,8-cineole in COPD and asthma: Review on the new therapeutic approach. Adv Ther 2020; 37: 1737-1753
• 28 Asif M, Saleem M, Saadullah M, Yaseen HS, Al Zarzour R. COVID-19 and therapy with essential oils having antiviral, anti-inflammatory, and immunomodulatory properties. Inflammopharmacology 2020; 28: 1153-1161
• 29 Sandner G, Heckmann M, Weghuber J. Immunomodulatory activities of selected essential oils. Biomolecules 2020; 10: 1139
• 30 Khezri K, Farahpour MR, Mounesi Rad S. Accelerated infected wound healing by topical application of encapsulated rosemary essential oil into nanostructured lipid carriers. Artif Cells Nanomed Biotechnol 2019; 47: 980-988
• 31 Cagno V, Donalisio M, Civra A, Cagliero C, Rubiolo P, Lembo D. In vitro evaluation of the antiviral properties of Shilajit and investigation of its mechanisms of action. J Ethnopharmacol 2015; 166: 129-134
• 32 Cagno V, Tintori C, Civra A, Cavalli R, Tiberi M, Botta L, Brai A, Poli G, Tapparal C, Lembo D, Botta M. Novel broad spectrum virucidal molecules against enveloped viruses. PLoS One 2018; 13: e0208333
• 33 Gu L, Schneller SW, Li Q. Assays for the identification of novel antivirals against Bluetongue virus. J Vis Exp 2013; 80: e50820
• 34 Kiyohara H, Ichino C, Kawamura Y, Nagai T, Sato N, Yamada H. Patchouli alcohol: In vitro direct anti-influenza virus sesquiterpene in Pogostemon cablin Benth. J Nat Med 2011; 66: 55-61
• 35 Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56: 152-179
• 36 Samji T. Influenza A: Understanding the viral life cycle. Yale J Biol Med 2009; 82: 153-159
• 37 Wu S, Patel KB, Booth LJ, Metcalf JP, Lin HK, Wu W. Protective essential oil attenuates influenza virus infection: An in vitro study in MDCK cells. BMC Complement Altern Med 2010; 10: 69
• 38 Brochot A, Guilbot A, Haddioui L, Roques C. Antibacterial, antifungal, and antiviral effects of three essential oil blends. Microbiol Open 2017; 6: 1-6
• 39 Garozzo A, Timpanaro R, Stivala A, Bisignano G, Castro A. Activity of Melaleuca alternifolia (tea tree) oil on influenza virus A/PR/8: Study on the mechanism of action. Antiviral Res 2010; 89: 83-88
• 40 Guinea R, Carrasco L. Concanamycin A blocks influenza virus entry into cells under acidic conditions. FEBS Lett 1994; 349: 327-330
• 41 Guinea R, Carrasco L. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J Virol 1995; 69: 2306-2312
• 42 Li X, Duan S, Chu C, Xu J, Zeng G, Lam AK, Zhou J, Yin Y, Fang D, Reynolds MJ, Gu H, Jiang L. Melaleuca alternifolia concentrate inhibits in vitro entry of influenza virus into host cells. Molecules 2013; 18: 9550-9566
• 43 Wu H, Li B, Wang X, Jin M, Wang G. Inhibitory effect and possible mechanism of action of patchouli alcohol against influenza a (H2N2) virus. Molecules 2011; 16: 6489-6501
• 44 Garman E, Laver G. Controlling influenza by inhibiting the virusʼs neuraminidase. Curr Drug Targets 2004; 5: 119-136
• 45 Yu Y, Zhang Y, Wang S, Liu W, Hao C, Wang W. Inhibition effects of patchouli alcohol against influenza a virus through targeting cellular PI3K/Akt and ERK/MAPK signaling pathways. Virol J 2019; 16: 163
• 46 Paulpandi M, Kannan S, Thangam R, Kaveri K, Gunasekaran P, Rejeeth C. In vitro anti-viral effect of β-santalol against influenza viral replication. Phytomedicine 2012; 19: 231-235
• 47 Furuse Y, Suzuki A, Kamigaki T, Oshitani H. Evolution of the M gene of the influenza A virus in different host species: Large-scale sequence analysis. Virol J 2009; 6: 67
• 48 Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Rämer PC, Lee M, Strowig T, Arrey F, Conenello G, Pypaert M, Andersen J, García-Sastre A, Münz Ch. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009; 6: 367-380
• 49 Wu QF, Wang W, Daia XY, Wang ZY, Shen ZH, Ying HZ, Yuc CH. Chemical compositions and anti-influenza activities of essential oils from Mosla dianthera . J Ethnopharmacol 2012; 139: 668-671
• 50 Dai JP, Zhao XF, Zeng J, Wan Q, Yang JC, Li WZ, Chen XX, Wang GF, Li KS. Drug screening for autophagy inhibitors based on the dissociation of beclin1-Bcl2 complex using BiFC technique and mechanism of eugenol on anti-influenza A virus activity. PLoS One 2013; 8: e61026
• 51 Wang R, Zhu Y, Zhao J, Ren Ch, Li P, Chen H, Jin M, Zhou H. Autophagy promotes replication of influenza A virus in vitro . J Virol 2019; 93: e01984-18
• 52 Liao Q, Qian Z, Liu R, An L, Chen X. Germacrone inhibits early stages of influenza virus infection. Antiviral Res 2013; 100: 578-588
• 53 He YQ, Caib L, Qiana QG, Yanga SH, Chena DL, Zhaoa BQ, Zhongc ZP, Zhoua XJ. Anti-influenza A (H1N1) viral and cytotoxic sesquiterpenes from Carpesium abrotanoides . Phytochem Lett 2020; 35: 41-45
• 54 Li Y, Lai Y, Wang Y, Liu N, Zhang F, Xu P. 1,8-Cineol protect against influenza-virus-induced pneumonia in mice. Inflammation 2016; 39: 1582-1592
• 55 Choi HJ. Chemical constituents of essential oils possessing anti-influenza A/WS/33 virus activity. Osong Public Health Res Perspect 2018; 9: 348-353
• 56 Tellier R. Review of aerosol transmission of influenza A virus. Emerg Infect Dis 2006; 12: 1657-1662
• 57 Richard M, van den Brand JMA, Bestebroer TM, Lexmond P, de Meulder D, Fouchier RAM, Lowen AC, Herfst S. Influenza A viruses are transmitted via the air from the nasal respiratory epithelium of ferrets. Nat Commun 2020; 11: 766
• 58 Usachev EV, Pyankov OV, Usacheva OV, Agranovski IE. Antiviral activity of tea tree and eucalyptus oil aerosol and vapor. J Aerosol Sci 2013; 59: 22-30
• 59 Vimalanathan S, Hudson J. Anti-influenza virus activity of essential oils and vapors. Am J Essent Oil Nat Prod 2014; 2: 47-53
• 60 Vimalanathan S, Hudson J. The activity of cedar leaf oil vapor gainst respiratory viruses: Practical applications. J App Pharm Sci 2013; 3: 011-015
• 61 Pyankov OV, Usachev EV, Pyankova O, Agranovski IE. Inactivation of airborne influenza virus by tea tree and eucalyptus oils. Aerosol Sci Technol 2012; 46: 1295-1302
• 62 Abdel-Moneim AS, Manal AA, El-Kady MF. Isolation and mutation trend analysis of influenza A virus subtype H9N2 in Egypt. Virol J 2012; 9: 173
• 63 Ibrahim NA, El-Hawary SS, Mohammed MMD, Farid MA, Abdel-Wahed NAM, Ali MA, El-Abd EAW. Chemical composition, antiviral against avian influenza (H5N1) virus and antimicrobial activities of the essential oils of the leaves and fruits of Fortunella margarita Lour. Swingle, growing in Egypt. J Appl Pharm Sci 2015; 5: 6-12
• 64 Pourghanbari G, Nili H, Moattari A, Mohammadi A, Iraji A. Antiviral activity of the oseltamivir and Melissa officinalis L. essential oil against avian influenza A virus (H9N2). Virusdisease 2016; 27: 170-178
• 65 Kumosani T, Obeid Y, Shaib H, Abualnaja K, Moselhy SS, Iyer A, Sultan R, Aslam A, Anjum A, Barbour E. Standardization of a protocol for quantitative evaluation of anti-aerosolized influenza virus activity by vapors of a chemically-characterized essential oil blend. Prev Infect Control 2017; 3: 6-14
• 66 Shayeganmehr A, Vasfi Marandi M, Karimi V, Barin A, Ghalyanchilangeroudi A. Zataria multiflora essential oil reduces replication rate of avian influenza virus (H9N2 subtype) in challenged broiler chicks. Br Poult Sci 2018; 59: 389-395
• 67 Chandevar P, Chavhan B, Sahare A, Deshpande P, Kawade D. SARS coronavirus: A review of threat in global world. Inter J Pharm Sci Res 2020; 5: 1-9
• 68 Al-Garawyi AMA, Hussein TA, Jassim MMA. Inhibition of viral infection by using of natural herbal remedies as alternative treatment. Sys Rev Pharm 2020; 11: 416-419
• 69 Merad M, Martin JC. Pathological inflammation in patients with COVID-19: A key role for monocytes and macrophages. Immunology 2020; 20: 355-362
• 70 Antonio AS, Wiedemann LSM, Veiga-Junior VF. Natural productsʼ role against COVID-19. RSC Adv 2020; 10: 23379-23393
• 71 Verma S, Twilley D, Esmear T, Oosthuizen CB, Reid AM, Nel M, Lall N. Anti-SARS-CoV natural products with the potential to inhibit SARS-CoV-2 (COVID-19). Front Pharmacol 2020; 11: 561334
• 72 Silveira D, Prieto-Garcia JM, Boylan F, Estrata O, Fonseca-Bazzo YM, Jamal CM, Magalhaes PO, Pereira EO, Tomczyk M, Heinrich M. COVID-19: Is there evidence for the use of herbal medicines as adjuvant symptomatic therapy?. Front Pharmacol 2020; 11: 581840
• 73 Panyod S, Ho CT, Sheen LY. Dietary therapy and herbal medicine for COVID-19 prevention: A review and perspective. J Tradit Complement Med 2020; 10: 420-427
• 74 Nadjib BM. Effective antiviral activity of essential oils and their characteristic terpenes against coronaviruses: An update. J Pharmacol Clin Toxicol 2020; 8: 1138
• 75 Flouchi R, Fikri-Benbrahim K. Prevention of COVID 19 by aromatic and medicinal plants: A systematic review. J Pharm Sci Res 2020; 12: 1106-1111
• 76 Loizzo MR, Saab AM, Tundis R, Statti GA, Menichini F, Lampronti I, Gambari R, Cinatl J, Doerr HW. Phytochemical analysis and in vitro antiviral activities of the essential oils of seven Lebanon species. Chem Biodivers 2008; 5: 461-470
• 77 Abdelli I, Hassanic F, Brikcic SB, Ghalem S. In silico study the inhibition of angiotensin converting enzyme 2 receptor of COVID-19 by Ammoides verticillata components harvested from Western Algeria. J Biomol Struct Dyn 2021; 39: 3263-3276
• 78 Thuy BTP, Ai My TT, Hai NTT, Hieu LT, Hoa TT, Loan HTP, Triet NT, Van Anh TT, Quy PT, Tat PV, Hue NV, Quang DT, Trung NT, Tung VT, Huynh LK, Nhung NTA. Investigation into SARS-CoV-2 resistance of compounds in garlic essential oil. ACS Omega 2020; 5: 8312-8320
• 79 Da Silva JKR, Figueiredo PLB2 Byler KG, Setzer WN. Essential oils as antiviral agents, potential of essential oils to treat SARS-CoV-2 infection: An in-silico investigation. Int J Mol Sci 2020; 21: 3426
• 80 My TTA, Loan HTP, Hai NTT, Hieu LT, Hoa TT, Thuy BTP, Quang DT, Triet NT, Anh TTV, Dieu NTX, Trung NT, Hue NV, Tat PV, Tung VT, Nhung NTA. Evaluation of the inhibitory activities of COVID-19 of Melaleuca cajuputi oil using docking simulation. ChemistrySelect 2020; 5: 6312-6320
• 81 Kumar KJS, Vani MG, Wang CS, Chen CC, Chen YC, Lu LP, Huang CH, Lai CS, Wang SY. Geranium and lemon essential oils and their active compounds downregulate angiotensin-converting enzyme 2 (ACE2), a SARS-CoV-2 spike receptor-binding domain, in epithelial cells. Plants 2020; 9: 770
• 82 Sharma AD, Kaur I. Eucalyptol (1,8-cineole) from eucalyptus essential oil a potential inhibitor of COVID 19 corona virus infection by molecular docking studies. Preprints 2020; DOI: 10.20944/preprints202003.0455.v1.
• 83 Sharma AD, Kaur I. Jensenone from eucalyptus essential oil as a potential inhibitor of COVID 19 corona virus infection. Res Rev Biotech Biosci 2020; 7: 59-66
• 84 Kumar A, Choudhir G, Shukla SK, Sharma M, Tyagi P, Bhushan A, Rathore M. Identification of phytochemical inhibitors against main protease of COVID-19 using molecular modeling approaches. J Biomol Struct Dyn 2020; DOI: 10.1080/07391102.2020.1772112.
• 85 Walls AC, Park YJ, Tortorici MA, Wall A, McGuire AT, Veesler D. Structure function and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 2020; 181: 281-292
• 86 Kulkarni SA, Nagarajan SK, Ramesh V, Palaniyandi V, Selvam SP, Madhavan T. Computational evaluation of major components from plant essential oils as potent inhibitors of SARS-CoV-2 spike protein. J Mol Struct 2020; 1221: 128823
• 87 De Jesus M, Gaza JT, Junio H, Nellas R. Molecular docking studies of aromatherapy oils against SARS-CoV-2. Preprint 2020; 15: 26
• 88 Feng J, Bai X, Cui T, Zhou H, Chen Y, Xie J, Shi Q, Wang H, Zhang G. In vitro antiviral activity of germacrone against porcine reproductive and respiratory syndrome virus. Curr Microbiol 2016; 73: 317-323
• 89 Fabros DM, Kankeaw U, Ruansit W, Tonlek B, Theenongsang S, Charerntantanakul W. Evaluation of antiviral potential of cinnamon essential oil and its derived benzimidazole against porcine reproductive and respiratory syndrome virus. J Agric Res Ext 2018; 35 (Suppl.) 21-31
• 90 Pilau MR, Alves SH, Weiblen R, Arenhart S, Cueto AP, Lovato LT. Antiviral activity of the Lippia graveolens (Mexican oregano) essential oil and its main compound carvacrol against human and animal viruses. Braz J Microbiol 2011; 42: 1616-1624
• 91 Reichling J. Antibacterial and antiviral Effects of aromatic Plant-derived essential Oils – a scientific and medicinal Approach. In: Rai M, Cordell GA, Martinez JL, Marinoff M, Rastrelli L. eds. Medicinal Plants – Biodiversity and Drugs. Boca Raton: CRC Press; 2012: 622-640
• 92 Cagno V, Sgorbini B, Sanna C, Cagliero C, Ballero M, Civra A, Donalisio M, Bicchi C, Lembo D, Rubioloet P. In vitro anti-herpes simplex virus-2 activity of Salvia desoleana Atzei & V. Picci essential oil. PLoS One 2017; 12: e0172322
• 93 Schnitzler P. Essential oils for the treatment of herpes simplex virus infections. Chemotherapy 2019; 64: 1-7
• 94 Álvarez DM, Castillo E, Duarte LF, Arriagada J, Corrales N, Farías MA, Henríquez A, Agurto-Muñoz C, González PA. Current antivirals and novel botanical molecules interfering with herpes simplex virus infection. Front Microbiol 2020; 11: 139
• 95 Schnitzler P, Schumacher A, Reichling J. Melissa officinalis oil affects infectivity of enveloped herpesviruses. Phytomedicine 2008; 15: 734-740
• 96 Schnitzler P, Astani A, Reichling J. Antiviral Effects of Plant-derived essential Oils and pure Oil Components. In: Halldor T. ed. Lipids and essential Oils as antimicrobial Agents. West Sussex, United Kingdom: John Wiley & Sons, Ltd.; 2011: 239-254
• 97 Brand YM, Roa-Linares VC, Betancur-Galvis LA, Durán-García DC, Stashenko E. Antiviral activity of Colombian labiatae and verbenaceae family essential oils and monoterpenes on human herpes viruses. J Essent Oil Res 2016; 28: 130-137
• 98 Walaszek R, Marszalek A, Kasperczyk T, Walaszek K, Burdacki M. The efficacy of aromatherapy in prevention of herpes simplex virus infections. Ind J Trad Knowledge 2018; 17: 425-429
• 99 Siddiqui YM, Ettayebi M, Haddad AM, Al-Ahdal MN. Effect of essential oils on the enveloped viruses: Antiviral activity of oregano and clove oils on herpes simplex virus type 1 and Newcastle disease virus. Med Sci Res 1996; 24: 185-186
• 100 Lai WL, Chuang HS, Lee MH, Wei CL, Lin CF, Tsai YC. Inhibition of herpes simplex virus type 1 by thymol-related monoterpenoids. Planta Med 2012; 78: 1636-1638
• 101 Civitelli L, Panella S, Marcocci ME, De Petris A, Garzoli S, Pepi F, Vavala E, Ragno R, Nencioni L, Palamara AT, Angiolella L. In vitro inhibition of herpes simplex virus type 1 replication by Mentha suaveolens essential oil and its main component piperitenone oxide. Phytomedicine 2014; 21: 857-865
• 102 Venturi CR, Danielli LJ, Klein F, Apel MA, Montanha JA, Bordignon SAL, Roehe PM, Fuentefria AM, Henriques AT. Chemical analysis and in vitro antiviral and antifungal activities of essential oils from Glechon spathulata and Glechon marifolia . Pharm Biol 2015; 53: 682-688
• 103 Astani A, Reichling J, Schnitzler P. Comparative study on the antiviral activity of selected monoterpenes derived from essential oils. Phytother Res 2010; 24: 673-679
• 104 Astani A, Reichling J, Schnitzler P. Screening for antiviral activities of isolated compounds form essential oils. Evid Based Complement Alternat Med 2011; 2011: 253643
• 105 Astani A, Schnitzler P. Antiviral activity of monoterpenes beta-pinene and limonene against herpes simplex virus in vitro . Iran J Microbiol 2014; 3: 150-155
• 106 El-Baz FK, Mahmoud K, El-Senousy WM, Darwesh OM, El Gohary AE. Antiviral–antimicrobial and schistosomicidal activities of Eucalyptus camaldulensis essential oils. Int J Pharm Sci Rev Res 2015; 31: 262-268
• 107 Gavanji S, Sayedipour SS, Larki B, Bakhtaric A. Antiviral activity of some plant oils against herpes simplex virus type 1 in Vero cell culture. J Acute Med 2015; 5: 62-68
• 108 Sharifi-Rad J, Salehi B, Schnitzler P, Ayatollahi SA, Kobarfard F, Fathi M, Eisazadeh M, Sharifi-Rad M. 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. Cell Mol Biol (Noisy le Grand) 2017; 63: 41-46
• 109 Kamalabadi M, Astani A, Nemati F. Antiviral effect and mechanism of carvacrol on herpes simplex virus type 1. Int J Med Lab 2018; 5: 113-122
• 110 Camero M, Lanave G, Catella C, Capozza P, Gentile A, Fracchiolla G, Britti D, Martella V, Buonavoglia C, Tempesta M. Virucidal activity of ginger essential oil against caprine alphaherpesvirus-1. Vet Microbiol 2019; 230: 150-155
• 111 Douek DC, Roederer M, Koup RA. Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 2009; 60: 471-484
• 112 Das AT, Harwig A, Berkhout B. The HIV-1 Tat protein has a versatile role in activating viral transcription. J Virol 2011; 85: 9506-9516
• 113 Feriotto G, Marchetti N, Costa V, Beninati S, Tagliati F, Mischiati C. Chemical composition of essential oils from Thymus vulgaris, Cymbopogon citratus, and Rosmarinus officinalis, and their effects on the HIV-1 Tat protein function. Chem Biodivers 2018; 15: e1700436
• 114 Kaushik S, Kaushik S, Sharma V, Yadav JP. Antiviral and therapeutic uses of medicinal plants and their derivatives against dengue viruses. Phcog Rev 2018; 12: 177-185
• 115 Kadir SLA, Yaakop H, Zulkiffi RM. Potential anti-dengue medicinal plants: A review. J Nat Med 2013; 67: 677-689
• 116 García CC, Acosta EG, Carro AC, Belmonte MCF, Bomben R, Duschatzky CB, Perotti M, Schuff C, Damonte EB. Virucidal activity and chemical composition of essential oils from aromatic plants of central west argentina. Nat Prod Commun 2010; 5: 1307-1310
• 117 Ocazionez RE, Meneses R, Torres FA, Stashenko E. Virucidal activity of Colombian Lippia essential oils on dengue virus replication in-vitro . Mem Inst Oswaldo Cruz 2010; 105: 304-309
• 118 Pajaro-Castro N, Flechas MC, Ocazionez R, Stashenko E, Olivero-Verbel J. Potential interaction of components from essential oils with dengue virus proteins. Bol Latinoam Caribe Plant Med Aromat 2015; 14: 141-155
• 119 Flechas MC, Ocazionez RE, Stashenko EE. Evaluation of in vitro antiviral activity of essential oil compounds against dengue virus. Pharmacogn J 2018; 10: 55-59
• 120 Vogt MV, Sutil SB, Escobar FM, Sabini MC, Cariddi LN, Torres CV, Zanon SM, Sabini LI. Minthostachys verticillata essentials oil and its major components: Antiherpetic selective action in HEp-2 cells. Mol Med Chem 2010; 21: 117-120
• 121 He W, Zhai X, Su J, Ye R, Zheng Y, Su S. Antiviral activity of germacrone against pseudorabies virus in vitro . Pathogens 2019; 8: 258
• 122 Khodakaram-Tafti A, Faranikish GH. Persistent bovine viral diarrhea virus (BVDV) infection in cattle herds. Iran J Vet Res 2017; 18: 154-163
• 123 Kubiça TF, Alves SH, Weiblen R, Lovato LT. In vitro inhibition of the bovine viral diarrhoea virus by the essential oil of Ocimum basilicum (basil) and monoterpenes. Brazilian J Microbiol 2014; 45: 209-214
• 124 Roy S, Chaurvedi P, Chowdhary A. Evaluation of antiviral activity of essential oil of Trachyspermum ammi against Japanese encephalitis virus. Pharmacognosy Res 2015; 7: 263-267
• 125 Monath TP, Barrett AD. Pathogenesis and pathophysiology of yellow fever. Adv Virus Res 2003; 60: 343-395
• 126 Meneses R, Ocazionez RE, Martínez JR, Stashenko EE. Inhibitory effect of essential oils obtained from plants grown in Colombia on yellow fever virus replication in-vitro . Ann Clin Microbiol Antimicrob 2009; 8: 8
• 127 Gómez LA, Stashenko E, Ocazionez RE. Comparative study on in vitro activities of citral, limonene and essential oils from Lippia citriodora and L. alba on yellow fever virus. Nat Prod Commun 2013; 8: 249-252
• 128 Mohammadi A, Mosleh N, Shomali T, Ahmadi M, Sabetghadam S. In-vitro evaluation of antiviral activity of essential oil from Zataria multiflora Boiss. against Newcastle disease virus. J Herb Med Pharmacol 2015; 4: 71-74
• 129 Zamora AP, Edmonds JH, Reynolds MJ, Khromykh AA, Ralph SJ. The in vitro and in vivo antiviral properties of combined monoterpene alcohols against West Nile virus infection. Virology 2016; 495: 18-32
• 130 Samuel MA, Diamond MS. Pathogenesis of West Nile virus infection: A balance between virulence, innate and adaptive immunity, and viral evasion. J Virol 2006; 80: 9349-9360
• 131 Zeedan GSG, Abdalhamed AM, Ottai ME, Abdelshafy S, Abdeen E. Antimicrobial, antiviral activity and GC-MS analysis of essential oil extracted from Achillea fragrantissima plant growing in Sinai Peninsula, Egypt. J Microbial Biochem Technol 2014; S8: 006
• 132 Ralambondrainy M, Belarbi E, Viranaicken W, Baranauskienė R, Venskutonis PR, Desprès P, Roques P, El Kalamouni C, Selambarom J. In-vitro comparison of three common essential oils mosquito repellents as inhibitors of the Ross River virus. PLoS One 2018; 13: e0196757
• 133 Haddad JG, Picard M, Bénard S, Desvignes C, Desprès P, Diotel N, El Kalamouni C. Ayapana triplinervis essential oil and its main component thymohydroquinone dimethyl ether inhibit Zika virus at doses devoid of toxicity in zebrafish. Molecules 2019; 24: 3447
• 134 Lane T, Anantpadma M, Freundlich JS, Davey RA, Madrid PB, Ekins S. The natural product eugenol is an inhibitor of the ebola virus in-vitro . Pharm Res 2019; 36: 104
• 135 Garozzo A, Timpanaro R, Bisignano B, Furneri PM, Bisignano G, Castro A. In vitro antiviral activity of Melaleuca alternifolia essential oil. Lett Appl Microbiol 2009; 49: 806-808
• 136 Kovac K, Diez-Valcarce M, Raspor P, Hernándes M, Rodriques-Lazáro D. Natural plant essential oils do not inactivate non-enveloped enteric viruses. Food Environ Virol 2012; 4: 209-212
• 137 Rouis Z, Abid N, Koudja S, Yangui T, Elaissi A, Cioni PL, Flamini G, Aouni M. Evaluation of the cytotoxic effect and antibacterial, antifungal, and antiviral activities of Hypericum triquetrifolium Turra essential oils from Tunisia. BMC Complement Altern Med 2013; 13: 24
• 138 Gilling DH, Kitajima M, Torrey JR, Bright KR. Antiviral efficacy and mechanisms of action of oregano essential oil and its primary component carvacrol against murine norovirus. J Appl Microbiol 2014; 116: 1149-1163
• 139 Gilling DH, Kitajima M, Torrey JR, Bright KR. Mechanisms of antiviral action of plant antimicrobials against murine norovirus. Appl Environ Microbiol 2014; 80: 4898-4910
• 140 Chung MS. Antiviral activities of Artemisia princeps var. orientalis essential oil and its α-thujone against norovirus surrogates. Food Sci Biotechnol 2017; 26: 1457-1461
• 141 Dalldorf G, Sickles GM. An unidentified, filtrable agent isolated from the feces of children with paralysis. Science 1948; 108: 61-62
• 142 Elaissi A, Rouis Z, Salem NAB, Mabrouk S, Ben Salem Y, Salah KBH, Aouni M, Farhat F, Chemli R, Harzallah-Skhiri F, Khouja ML. Chemical composition of 8 Eucalyptus speciesʼ essential oils and the evaluation of their antibacterial, antifungal and antiviral activities. BMC Complement Altern Med 2012; 12: 81
• 143 Bouazzi S, Jmii H, El Mokni R, Faidi K, Falconieri D, Piras A, Jaïdane H, Porcedda S, Hammami S. Cytotoxic and antiviral activities of the essential oils from Tunisian fern, Osmunda regalis . S Afr J Bot 2018; 118: 52-57
• 144 El Mokni R, Youssef FS, Jmii H, Khmiri A, Bouazzi S, Jlassi I, Jaidane H, Dhaouadi H, Ashour ML, Hammami S. The essential oil of Tunisian Dysphania ambrosioides and its antimicrobial and antiviral properties. J Essent Oil Bear Plants 2019; 22: 282-294
• 145 Chen Y, Dong Y, Jiao Y, Hou L, Shi Y, Gu T, Zhou P, Shi Z, Xu L, Wang C. In vitro antiviral activity of germacrone against porcine parvovirus. Arch Virol 2015; 160: 1415-1420
• 146 Oskuee RK, Behravan J, Ramezani M. Chemical composition, antimicrobial activity and antiviral activity of essential oil of Carum copticum from Iran. Avicenna J Phytomedicine 2011; 1: 83-90
• 147 Behravan J, Ramezani M, Nobandegani EF, Gharaee ME. Antiviral and antimicrobial activity of Thymus transcaspicus essential oil. Pharmacologyonline 2011; 1: 1190-1199
• 148 Wu H, Liu Y, Zu S, Sun X, Liu C, Liu D, Zhang X, Tian J, Qu L. In vitro antiviral effect of germacrone on feline calicivirus. Arch Virol 2016; 161: 1559-1567
• 149 Bilia AR, Guccione C, Isacchi B, Righeschi C, Firenzuoli F, Bergonzi MC. Essential oils loaded in nanosystems: A developing strategy for a successful therapeutic approach. Evid Based Complement Alternat Med 2014; 2014: 651593
• 150 Rai M, Paralikar P, Jogee P, Agarkar G, Ingle AP, Derita M, Zacchino S. Synergistic antimicrobial potential of essential oils in combination with nanoparticles: Emerging trends and future perspectives. Intern J Pharm 2017; 519: 67-78
• 151 De Matos SP, Teixeira HF, de Lima AAN, Veiga-Junior VF, Koester LS. Essential oils and isolated terpenes in nanosystems designed for topical administration: A review. Biomolecules 2019; 9: 138
• 152 Chakravarty M, Vora A. Nanotechnology-based antiviral therapeutics. Drug Deliv Transl Res 2021; 11: 748-787
• 153 Lammari N, Louaer O, Meniai AH, Elaissari A. Encapsulation of essential oils via nanoprecipitation process: Overview, progress, challenges and prospects. Pharmaceutics 2020; 12: 431
• 154 Lai F, Sinico C, De Logu A, Zaru M, Müller RH, Fadda AM. SLN as a topical delivery system for Artemisia arborescens essential oil: In vitro antiviral activity and skin permeation study. Int J Nanomedicine 2007; 2: 419-425
• 155 Almeida KB, Araujo JL, Cavalcanti JF, Romanos MTV, Mourão SC, Amaral ACF, Falcão DQ. In vitro release and anti-herpetic activity of Cymbopogon citratus volatile oil-loaded nanogel. Rev Bras Farmacogn 2018; 28: 495-502
• 156 Vanti G, Ntallis SG, Panagiotidis CA, Dourdouni V, Patsoura C, Bergonzi MC, Lazari D, Bilia AR. Glycerosome of Melissa officinalis L. essential oil for effective anti-HSV type 1. Molecules 2020; 25: 3111
• 157 Junior OT, Kuhn F, Padilha PJM, Nesi CN, Mestres M, Magro JD, Castellvi SDL. Effect of microencapsulated thyme essential oil on white spot virus-infected Litopenaeus vannamei . Aquacult Int 2018; 26: 1459-1468