In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil
Abstract
:1. Introduction
2. Results and Discussion
2.1. GC/MS Analysis of Essential Oil
2.2. Antioxidant Activity of Essential Oil
2.3. Evaluation of Antiviral Activity
3. Material and Methods
3.1. Essential Oil
3.2. GC/MS Analysis of Essential Oil
3.3. Antioxidant Activity of Essential Oil
3.4. Evaluation of Antiviral Activity
3.4.1. Cells and Viral Culture
3.4.2. Cytotoxicity Assay
3.4.3. Antiviral Assay
3.5. Statistical Analysis
4. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hafidh, R.; Abdulamir, A.; Abu Bakar, F.; Sekawi, Z.; Jahansheri, F.; Jalilian, F. Novel antiviral activity of mung bean sprouts against respiratory syncytial virus and herpes simplex virus −1: An in vitro study on virally infected Vero and MRC-5 cells lines. BMC Complement. Altern. Med. 2015, 15, 179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roy, S.; Chaurvedi, P.; Chowdhary, A. Evaluation of antiviral activity of essential oil of Trachyspermum Ammi against Japanese encephalitis virus. Pharmacogn. Res. 2015, 7, 236–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaur, K.; Kaushal, S. Phytochemistry and pharmacological aspects of Syzygium aromaticum: A review. J. Pharmacogn. Phytochem. 2019, 8, 398–406. [Google Scholar]
- Stringaro, A.; Colone, M.; Angiolella, L. Antioxidant, antifungal, antibiofilm, and cytotoxic activities of Mentha spp. essential oils. Medicines 2018, 5, 112. [Google Scholar] [CrossRef] [Green Version]
- Wani, A.R.; Yadav, K.; Khursheed, A.; Rather, M. An updated and comprehensive review of the antiviral potential of essential oils and their chemical constituents with special focus on their mechanism of action against various Influenza and Coronaviruses. Microb. Pathog. 2021, 152, 104620. [Google Scholar] [CrossRef]
- Singh, I.; Kaur, P.; Kaushal, U.; Kaur, V.; Shekhar, N. Essential oils in treatment and management of dental diseases. Biointerf. Res. Appl. Chem. 2022, 12, 7267–7286. [Google Scholar] [CrossRef]
- Esmaeili, Y.; Paidari, S.; Baghbaderani, S.A.; Nateghi, L.; Al-Hassan, A.A.; Ariffin, F. Essential oils as natural antimicrobial agents in postharvest treatments of fruits and vegetables. J. Food Meas. Charact. 2022, 16, 507–522. [Google Scholar] [CrossRef]
- Angane, M.; Swift, S.; Huang, K.; Butts, C.A.; Quek, S.Y. Essential oils and their major components: An updated review on antimicrobial activities, mechanism of action, and their potential application in the food industry. Foods 2022, 11, 464. [Google Scholar] [CrossRef]
- Ćavar Zeljković, S.; Schadich, E.; Džubák, P.; Hajdúch, M.; Tarkowski, P. Antiviral activity of selected lamiaceae essential oils and their monoterpenes against SARS-CoV-2. Front. Pharmacol. 2022, 13, 893634. [Google Scholar] [CrossRef] [PubMed]
- Vicidomini, C.; Roviello, V.; Roviello, G. Molecular basis of the therapeutical potential of clove (Syzygium aromaticum L.) and clues to its Anti-COVID-19 Utility. Molecules 2021, 26, 1880. [Google Scholar] [CrossRef] [PubMed]
- Chaieb, K.; Zmantar, T.; Ksouri, R.; Hajlaoui, H.; Mahdouani, K.; Abdelly, C.; Bakhrouf, A. Antioxidant properties of the essential oil of Eugenia caryophyllata and its antifungal activity against a large number of clinical Candida species. Mycoses 2007, 50, 403–406. [Google Scholar] [CrossRef] [PubMed]
- d’Avila, F.; Oliveira, P.; Dutra, F.; Fernandes, T.; de Pereira, C.; de Oliveira, S.; Stefanello, F.; Lencina, C.; Barschak, A. Eugenol derivatives as potential antioxidants: Is phenolic hydroxyl necessary to obtain an effect? J. Pharm. Pharmacol. 2014, 66, 733–746. [Google Scholar] [CrossRef] [PubMed]
- Das, M.; Roy, S.; Guha, C.; Saha, A.K.; Singh, M. In vitro evaluation of antioxidant and antibacterial properties of supercritical CO2 extracted essential oil from clove bud (Syzygium aromaticum). J. Plant Biochem. Biotechnol. 2020, 30, 387–391. [Google Scholar] [CrossRef]
- Gülçin, I.; Elmastaş, H.; Aboul-Enein, H.Y. Antioxidant activity of clove oil: A powerful antioxidant source. Arab. J. Chem. 2012, 5, 489–499. [Google Scholar] [CrossRef] [Green Version]
- Kasai, H.; Shirao, M.; Ikegami-Kawai, M. Analysis of volatile compounds of clove (Syzygium aromaticum) buds as influenced by growth phase and investigation of antioxidant activity of clove extracts. Flavour Fragr. J. 2015, 31, 178–184. [Google Scholar] [CrossRef]
- Rani, R.; Kumar, M. Clove (Syzygium aromaticum): Beneficial effects on human health. Plant Arch. 2021, 21, 1967–1972. [Google Scholar] [CrossRef]
- Lane, T.; Anantpadma, M.; Freundlich, J.; Davey, R.; Madrid, P.; Ekins, S. The natural product eugenol is an inhibitor of the Ebola virus in vitro. Pharm. Res. 2019, 36, 104. [Google Scholar] [CrossRef]
- Dai, J.; Zhao, X.; Zeng, J.; Wan, Q.; Yang, J.; Li, W.; Chen, X.; Wang, G.; Li, K. 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Oliveira, A.; Gazolla, P.; da Oliveira, A.; Pereira, W.; Viol, L.; da Maia, A.; Santos, E.; da Silva, Í.; de Mendes, T.; da Silva, A. Discovery of novel West Nile Virus protease inhibitor based on isobenzonafuranone and triazolic derivatives of eugenol and indan-1,3-dione scaffolds. PLoS ONE 2019, 14, e0223017. [Google Scholar] [CrossRef]
- Behbahani, M.; Mohabatkar, H.; Soltani, M. Anti-HIV-1 activities of aerial parts of Ocimum basilicum and its parasite cuscuta campestris. J. Antivir. Antiretrovir. 2013, 5, 057–061. [Google Scholar] [CrossRef] [Green Version]
- Haro-González, J.; Castillo-Herrera, J.; Martínez-Velázquez, M.; Espinosa-Andrews, H. Clove essential oil (Syzygium aromaticum L. Myrtaceae): Extraction, chemical composition, food applications, and essential bioactivity for human health. Molecules 2021, 26, 6387. [Google Scholar] [CrossRef]
- Jimoh, S.; Arowolo, L.; Alabi, K. Phytochemical screening and antimicrobial evaluation of Syzygium aromaticum extract and essential oil. Int. J. Curr. Microbiol. Appl. Sci. 2017, 6, 4557–4567. [Google Scholar] [CrossRef]
- Alma, M.; Ertaş, M.; Nitz, S.; Kollmannsberger, H. Chemical composition and content of essential oil from the bud of cultivated Turkish clove (Syzygium aromaticum L. ) BioResources 2007, 2, 265–269. [Google Scholar] [CrossRef]
- Rodríguez, O.; Sánchez, R.; Verde, M.; Núñez, M.; Ríos, R.; Chávez, A. Obtaining the essential oil of Syzygium aromaticum, identification of eugenol and its effect on Streptococcus mutans. J. Oral Res. 2014, 3, 218–224. [Google Scholar] [CrossRef] [Green Version]
- Kaur, K.; Kaushal, S.; Rani, R. Chemical composition, antioxidant and antifungal potential of clove (Syzygium aromaticum) essential oil, its major compound and its derivatives. J. Essent. Oil-Bear. Plants 2019, 22, 1195–1217. [Google Scholar] [CrossRef]
- Tomaino, A.; Cimino, F.; Zimbalatti, V.; Venuti, V.; Sulfaro, V.; De Pasquale, A.; Saija, A. Influence of heating on antioxidant activity and the chemical composition of some spice essential oils. Food Chem. 2005, 89, 549–554. [Google Scholar] [CrossRef]
- Lee, K.; Shibamoto, T. Antioxidant property of aroma extract isolated from clove buds (Syzygium aromaticum L.) Merr. et Perry. Food Chem. 2001, 74, 443–448. [Google Scholar] [CrossRef]
- Arslan, N.; Gürbüz, B.; Sarıhan, E.O. Variation in essential oil content and composition in Turkish anise (Pimpinella anisum L.) populations. Turk. J. Agric. For. 2004, 28, 173–177. [Google Scholar]
- Massodi, E.; Mime, L.; Fogang, D.; Djikeng, T.; Karuna, M.; Womeni, H.M. Chemical composition and antioxidant activity of Syzygium aromaticum and Monodora myristica essential oils from Cameroon. J. Food. Stab 2018, 1, 1–13. [Google Scholar]
- Ćavar, S.; Maksimović, M.; Šolić, M.E.; Jerković-Mujkić, A.; Bešta, R. Chemical composition and antioxidant and antimicrobial activity of two satureja essential oils. Food Chem. 2008, 111, 648–653. [Google Scholar] [CrossRef]
- Adefegha, S.; Oboh, G.; Ejakpovi, I.; Oyeleye, S. Antioxidant and antidiabetic effects of gallic and protocatechuic acids: A structure–function perspective. Comp. Clin. Pathol. 2015, 24, 1579–1585. [Google Scholar] [CrossRef]
- Marmouzi, I.; Karym, E.; Alami, R.; El Jemli, M.; Kharbach, M.; Mamouch, F.; Attar, A.; Faridi, B.; Cherrah, Y.; Faouzi, M. Modulatory effect of Syzygium aromaticum and Pelargonium graveolens on oxidative and sodium nitroprusside stress and inflammation. Orient. Pharm. Exp. Med. 2019, 19, 201–210. [Google Scholar] [CrossRef]
- Shahbazi, Y. Antioxidant, antibacterial, and antifungal properties of nanoemulsion of clove essential oil. J. Nanomed. Res. 2019, 4, 204–208. [Google Scholar]
- Dahham, S.; Tabana, Y.; Iqbal, M.; Ahamed, M.; Ezzat, M.; Majid, A. The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-Caryophyllene from the essential oil of Aquilaria crassna. Molecules 2015, 20, 11808–11829. [Google Scholar] [CrossRef] [PubMed]
- Dundar, Y.; Aslan, R. Antioxidative stress. East. J. Med. 2000, 5, 45–47. [Google Scholar]
- Pilau, M.; Alves, S.; Weiblen, R.; Arenhart, S.; Cueto, A.; Lovato, L. 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schnitzler, P. Essential oils for the treatment of herpes simplex virus infections. Chemotherapy 2019, 64, 1–7. [Google Scholar] [CrossRef]
- Cermelli, C.; Fabio, A.; Fabio, G.; Quaglio, P. Effect of eucalyptus essential oil on respiratory bacteria and viruses. Curr. Microbiol. 2008, 56, 89–92. [Google Scholar] [CrossRef]
- Koch, C.; Reichling, J.; Schneele, J.; Schnitzler, P. Inhibitory effect of essential oils against herpes simplex virus type 2. Phytomedicine 2008, 15, 71–78. [Google Scholar] [CrossRef]
- Ocazionez, R.; Meneses, R.; Torres, F.; Stashenko, E. Virucidal activity of Colombian Lippia essential oils on dengue virus replication in vitro. Mem. Inst. Oswaldo Cruz 2010, 105, 304–309. [Google Scholar] [CrossRef] [Green Version]
- Benencia, F.; Courreges, M. In vitro and in vivo activity of eugenol on human herpesvirus. Phytother. Res. 2000, 14, 495–500. [Google Scholar] [CrossRef] [PubMed]
- Battistini, R.; Rossini, I.; Ercolini, C.; Goria, M.; Callipo, M.R.; Maurella, C.; Pavoni, E.; Serracca, L. Antiviral activity of essential oils against hepatitis A virus in soft fruits. Food Environ. Virol. 2019, 11, 90–95. [Google Scholar] [CrossRef]
- Jama-Kmiecik, A.; Sarowska, J.; Wojnicz, D.; Choroszy-Król, I.; Frej-Mądrzak, M. Natural products and their potential anti-HAV activity. Pathogens 2021, 10, 1095. [Google Scholar] [CrossRef] [PubMed]
- Schuhmacher, A.; Reichling, J.; Schnitzler, P. Virucidal effect of peppermint oil on the enveloped virus’s herpes simplex virus type 1 and type 2 in vitro. Phytomedicine 2003, 10, 504–510. [Google Scholar] [CrossRef] [Green Version]
- Saddi, M.; Sanna, A.; Cottiglia, F.; Chisu, L.; Casu, L.; Bonsignore, L.; De Logu, A. Antiherpevirus activity of Artemisia arborescens essential oil and inhibition of lateral diffusion in Vero cells. Ann. Clin. Microb. Antimicrob. 2007, 6, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Francomano, F.; Caruso, A.; Barbarossa, A.; Fazio, A.; La Torre, C.; Ceramella, J.; Mallamaci, R.; Saturnino, C.; Iacopetta, D.; Sinicropi, M.S. β-Caryophyllene: A sesquiterpene with countless biological properties. Appl. Sci. 2019, 9, 5420. [Google Scholar] [CrossRef] [Green Version]
- Bezerra, D.; Militão, G.; Morais, M.; Sousa, D. The dual antioxidant/prooxidant effect of eugenol and its action in cancer development and treatment. Nutrients 2017, 9, 1367. [Google Scholar] [CrossRef] [Green Version]
- Furuya, A.; Uozaki, M.; Yamasaki, H.; Arakawa, T.; Arita, M.; Koyama, A. Antiviral effects of ascorbic and dehydroascorbic acids in vitro. Int. J. Mol. Med. 2008, 22, 541–545. [Google Scholar]
- Hassimotto, N.; Genovese, M.; Lajolo, F. Antioxidant activity of dietary fruits, vegetables, and commercial frozen fruit pulps. J. Agric. Food Chem. 2005, 53, 2928–2935. [Google Scholar] [CrossRef]
- Ibrahim, G.; Kiki, M. Chemical composition, antifungal and antioxidant activity of some spice essential oils. J. Life Sci. Pharma Res. 2020, 10, 45–52. [Google Scholar]
- Park, H.; Park, E.; Rim, A.; Jeon, K.; Hwang, J.; Lee, S. Antioxidant activity of extracts from Acanthopanax senticosus. Afr. J. Biotechnol. 2006, 5, 2388–2396. [Google Scholar]
- Vijayan, P.; Raghu, C.; Ashok, G.; Dhanaraj, S.; Suresh, B. Antiviral activity of medicinal plants of Nilgiris. Indian J. Med. Res. 2004, 120, 24–29. [Google Scholar] [PubMed]
- Pinto, R.M.; Diez, J.M.; Bosch, A. Use of the colonic carcinoma cell line CaCo-2 for in vivo amplification and detection of enteric viruses. J. Med. Virol. 1994, 44, 310–315. [Google Scholar] [CrossRef]
- Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55–63. [Google Scholar] [CrossRef]
- Kaul, T.; Middleton, E.; Ogra, P. Antiviral effect of flavonoids on human viruses. J. Med. Virol. 1985, 15, 71–79. [Google Scholar] [CrossRef] [PubMed]
Name | Formula | Retention Time | Area | Area Sum % |
---|---|---|---|---|
α-Cubebene | C15H24 | 21.704 | 914,030.44 | 0.28 |
Eugenol | C10H12O2 | 22.264 | 253,303,146.8 | 76.78 |
α-Copaene | C15H24 | 22.567 | 3,839,412.04 | 1.16 |
β-Caryophyllene | C15H24 | 23.971 | 70,203,334.66 | 21.24 |
β-Caryophyllene oxide | C15H24O | 28.838 | 1,793,977.82 | 0.54 |
Concentrations (µg/mL) | Inhibition (%) ± SD | |||
---|---|---|---|---|
30 | 60 | 90 | 120 | |
50 | 47.6 ± 0.62 | 53.1 ± 0.28 | 57.3 ± 0.24 | 60.1 ± 0.12 |
100 | 73.2 ± 0.22 | 79.2 ± 0.14 | 84.2 ± 0.13 | 88.1 ± 0.23 |
200 | 91.2 ± 0.21 | 93.5 ± 0.32 | 94.5 ± 0.05 | 95.1 ± 0.12 |
400 | 96.1 ± 0.11 | 96.7 ± 0.25 | 97.0 ± 0.17 | 97.2 ± 0.03 |
800 | 98.6 ± 0. 15 | 98.6 ± 0.01 | 98.7 ± 0.21 | 98.7 ± 0.25 |
Sample Concentration (µg/mL) | Viability (%) | Cytotoxicity (%) ± SD |
---|---|---|
0.25 | 97.82 | 2.18 ± 0.46 |
0.5 | 95.66 | 4.34 ± 0.32 |
1 | 89.74 | 10.26 ± 0.52 |
2 | 80.28 | 19.72 ± 0.46 |
3.9 | 72.49 | 27.51 ± 1.03 |
7.8 | 59.17 | 40.83 ± 1.79 |
15.6 | 48.02 | 51.98 ± 1.34 |
31.25 | 34.83 | 65.17 ± 1.29 |
62.5 | 20.95 | 79.05 ± 0.63 |
125 | 8.04 | 91.96 ± 0.28 |
Virus | Cytotoxic Effects CC50 µg/mL ± SD | Antiviral Effects IC50 µg/mL ± SD | Selectivity Index (SI) |
---|---|---|---|
Hepatitis A virus (HAV) | 14.21 ± 0.63 | 0.73 ± 0.25 | 14.46 |
Herpes simplex virus (HSV-1) | 14.21 ± 0.63 | 9.84 ± 0.68 | 1.44 |
Adenovirus | 14.21 ± 0.63 | NA | NA |
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Kiki, M.J. In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil. Molecules 2023, 28, 2421. https://doi.org/10.3390/molecules28062421
Kiki MJ. In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil. Molecules. 2023; 28(6):2421. https://doi.org/10.3390/molecules28062421
Chicago/Turabian StyleKiki, Manal Jameel. 2023. "In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil" Molecules 28, no. 6: 2421. https://doi.org/10.3390/molecules28062421
APA StyleKiki, M. J. (2023). In Vitro Antiviral Potential, Antioxidant, and Chemical Composition of Clove (Syzygium aromaticum) Essential Oil. Molecules, 28(6), 2421. https://doi.org/10.3390/molecules28062421