Nanoencapsulation of Plant Volatile Organic Compounds to Improve Their Biological Activities

Hakmin Mun; Helen E. Townley

doi:10.1055/a-1289-4505

Planta Medica, Inhaltsverzeichnis

Planta Med 2021; 87(03): 236-251
DOI: 10.1055/a-1289-4505

Formulation and Delivery Systems of Natural Products

Reviews

Nanoencapsulation of Plant Volatile Organic Compounds to Improve Their Biological Activities

Hakmin Mun

¹Nuffield Department of Womenʼs and Reproductive Health, University of Oxford, Oxford, UK

,

Helen E. Townley

¹Nuffield Department of Womenʼs and Reproductive Health, University of Oxford, Oxford, UK

²Department of Engineering Science, University of Oxford, Oxford, UK

› Institutsangaben

Abstract

Plant volatile organic compounds (volatiles) are secondary plant metabolites that play crucial roles in the reproduction, defence, and interactions with other vegetation. They have been shown to exhibit a broad range of biological properties and have been investigated for antimicrobial and anticancer activities. In addition, they are thought be more environmentally friendly than many other synthetic chemicals [1]. Despite these facts, their applications in the medical, food, and agricultural fields are considerably restricted due to their volatilities, instabilities, and aqueous insolubilities. Nanoparticle encapsulation of plant volatile organic compounds is regarded as one of the best strategies that could lead to the enhancement of the bioavailability and biological activity of the volatile compounds by overcoming their physical limitations and promoting their controlled release and cellular absorption. In this review, we will discuss the biosynthesis and analysis of plant volatile organic compounds, their biological activities, and limitations. Furthermore, different types of nanoparticle platforms used to encapsulate the volatiles and the biological efficacies of nanoencapsulated volatile organic compounds will be covered.

Key words

plant volatile organic compounds - essential oil - nanoencapsulation - nanoparticle - antimicrobial activity - anticancer activity

Volltext

Referenzen

References
1 EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). Bampidis V, Azimonti G, de Lourdes Bastos M, Christensen H, Kouba M, Kos Durjava M, López-Alonso M, López Puente S, Marcon F, Mayo B, Pechová A, Petkova M, Ramos F, Sanz Y, Villa R, Woutersen R, Brantom P, Chesson A, Kolar B, Beelen PV, Westendorf J, Gregoretti L, Manini P, Dusemund B. Safety and efficacy of an essential oil from Elettaria cardamomum (L.) Maton when used as a sensory additive in feed for all animal species. EFSA J 2019; 17: e05721
2 Pichersky E, Noel JP, Dudareva N. Biosynthesis of plant volatiles: natureʼs diversity and ingenuity. Science 2006; 311: 808-811
3 Schiestl FP. Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytologist 2015; 206: 571-577
4 Effah E, Holopainen JK, McCormick AC. Potential roles of volatile organic compounds in plant competition. Perspect Plant Ecol Evol Syst 2019; 38: 58-63
5 Ameye M, Allmann S, Verwaeren J, Smagghe G, Haesaert G, Schuurink RC, Audenaert K. Green leaf volatile production by plants: a meta-analysis. New Phytologist 2018; 220: 666-683
6 Dong F, Fu X, Watanabe N, Su X, Yang Z. Recent advances in the emission and functions of plant vegetative volatiles. Molecules 2016; 21: 124
7 Bravo Cadena M, Preston GM, Van der Hoorn RAL, Townley HE, Thompson IP. Species-specific antimicrobial activity of essential oils and enhancement by encapsulation in mesoporous silica nanoparticles. Ind Crops Prod 2018; 122: 582-590
8 Li ZH, Cai M, Liu YS, Sun PL, Luo SL. Antibacterial activity and mechanisms of essential oil from Citrus medica L. var. sarcodactylis . Molecules 2019; 24: 1577
9 Naksang P, Tongchitpakdee S, Thumanu K, Oruna-Concha MJ, Niranjan K, Rachtanapun C. Assessment of antimicrobial activity, mode of action and volatile compounds of Etlingera pavieana essential oil. Molecules 2020; 25: 3245
10 Xing M, Zheng L, Deng Y, Xu D, Xi P, Li M, Kong G, Jiang Z. Antifungal activity of natural volatile organic compounds against Litchi Downy Blight pathogen Peronophythora litchii . Molecules 2018; 23
11 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
12 Bezerra DP, Marinho Filho JD, Alves AP, Pessoa C, de Moraes MO, Pessoa OD, Torres MC, Silveira ER, Viana FA, Costa-Lotufo LV. Antitumor activity of the essential oil from the leaves of Croton regelianus and its component ascaridole. Chem Biodivers 2009; 6: 1224-1231
13 Sugier D, Sugier P, Jakubowicz-Gil J, Winiarczyk K, Kowalski R. Essential oil from Arnica Montana L. Achenes: Chemical characteristics and anticancer activity. Molecules 2019; 24: 4158
14 Wu Z, Wei W, Cheng K, Zheng L, Ma C, Wang Y. Insecticidal activity of triterpenoids and volatile oil from the stems of Tetraena mongolica . Pestic Biochem Physiol 2020; 166: 104551
15 Han X, Parker TL. Anti-inflammatory activity of clove (Eugenia caryophyllata) essential oil in human dermal fibroblasts. Pharm Biol 2017; 55: 1619-1622
16 Raafat K, Habib J. Phytochemical compositions and antidiabetic potentials of Salvia sclarea L. essential oils. J Oleo Sci 2018; 67: 1015-1025
17 Abuhamdah S, Abuhamdah R, Howes MJ, Al-Olimat S, Ennaceur A, Chazot PL. Pharmacological and neuroprotective profile of an essential oil derived from leaves of Aloysia citrodora Palau. J Pharm Pharmacol 2015; 67: 1306-1315
18 Pandey A, Bigoniya P, Raj V, Patel KK. Pharmacological screening of Coriandrum sativum Linn. for hepatoprotective activity. J Pharm Bioallied Sci 2011; 3: 435-441
19 de Matos SP, Teixeira HF, de Lima ÁAN, Veiga-Junior VF, Koester LS. Essential oils and isolated terpenes in nanosystems designed for topical administration: A review. Biomolecules 2019; 9: 138
20 Dudareva N, Klempien A, Muhlemann JK, Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 2013; 198: 16-32
21 Champagne A, Boutry M. Proteomics of terpenoid biosynthesis and secretion in trichomes of higher plant species. BBA – Proteins and Proteomics 2016; 1864: 1039-1049
22 Maeda H, Dudareva N. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol 2012; 63: 73-105
23 Deng Y, Lu S. Biosynthesis and regulation of phenylpropanoids in plants. CRC Crit Rev Plant Sci 2017; 36: 257-290
24 Muhlemann JK, Klempien A, Dudareva N. Floral volatiles: from biosynthesis to function. Plant Cell Environ 2014; 37: 1936-1949
25 Feussner I, Wasternack C. The lipoxygenase pathway. Annu Rev Plant Biol 2002; 53: 275-297
26 Babenko LM, Shcherbatiuk MM, Skaterna TD, Kosakivska IV. Lipoxygenases and their metabolites in formation of plant stress tolerance. Ukr Biochem J 2017; 89: 5-21
27 Kotra VSR, Satyabanta L, Goswami TK. A critical review of analytical methods for determination of curcuminoids in turmeric. J Food Sci Technol 2019; 56: 5153-5166
28 Araújo LA, Araújo RG, Gomes FO, Lemes SR, Almeida LM, Maia LJ, Gonçalves PJ, Mrué F, Silva-Junior NJ, Melo-Reis PR. Physicochemical/photophysical characterization and angiogenic properties of Curcuma longa essential oil. An Acad Bras Ciênc 2016; 88: 1889-1897
29 Do TKT, Hadji-Minaglou F, Antoniotti S, Fernandez X. Authenticity of essential oils. Trends Analyt Chem 2015; 66: 146-157
30 Dhifi W, Bellili S, Jazi S, Bahloul N, Mnif W. Essential oilsʼ chemical characterization and investigation of some biological activities: A critical review. Medicines (Basel) 2016; 3: 25
31 Tranchida PQ, Sciarrone D, Dugo P, Mondello L. Heart-cutting multidimensional gas chromatography: a review of recent evolution, applications, and future prospects. Anal Chim Acta 2012; 716: 66-75
32 Turek C, Stintzing FC. Application of high-performance liquid chromatography diode array detection and mass spectrometry to the analysis of characteristic compounds in various essential oils. Anal Bioanal Chem 2011; 400: 3109
33 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
34 Singh G, Maurya S, DeLampasona MP, Catalan CA. A comparison of chemical, antioxidant and antimicrobial studies of cinnamon leaf and bark volatile oils, oleoresins and their constituents. Food Chem Toxicol 2007; 45: 1650-1661
35 Ruberto G, Baratta MT, Deans SG, Dorman HJ. Antioxidant and antimicrobial activity of Foeniculum vulgare and Crithmum maritimum essential oils. Planta Med 2000; 66: 687-693
36 Soković M, Glamočlija J, Marin PD, Brkić D, van Griensven LJ. Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules 2010; 15: 7532-7546
37 Botelho MA, Nogueira NA, Bastos GM, Fonseca SG, Lemos TL, Matos FJ, Montenegro D, Heukelbach J, Rao VS, Brito GA. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Braz J Med Biol Res 2007; 40: 349-356
38 Mahboubi M, Haghi G. Antimicrobial activity and chemical composition of Mentha pulegium L. essential oil. J Ethnopharmacol 2008; 119: 325-327
39 Aridoğan BC, Baydar H, Kaya S, Demirci M, Ozbaşar D, Mumcu E. Antimicrobial activity and chemical composition of some essential oils. Arch Pharm Res 2002; 25: 860-864
40 Lu M, Dai T, Murray CK, Wu MX. Bactericidal property of oregano oil against multidrug-resistant clinical isolates. Front Microbiol 2018; 9: 2329
41 Kim J, Marshall MR, Wei C. Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem 1995; 43: 2839-2845
42 Delaquis PJ, Stanich K, Girard B, Mazza G. Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils. Int J Food Microbiol 2002; 74: 101-109
43 Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils–a review. Food Chem Toxicol 2008; 46: 446-475
44 Knobloch K, Pauli A, Iberl B, Weigand H, Weis N. Antibacterial and antifungal properties of essential oil components. J Essent Oil Res 1989; 1: 119-128
45 Burt SA, van der Zee R, Koets AP, de Graaff AM, van Knapen F, Gaastra W, Haagsman HP, Veldhuizen EJ. Carvacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157:H7. Appl Environ Microbiol 2007; 73: 4484-4490
46 Cox SD, Mann CM, Markham JL, Bell HC, Gustafson JE, Warmington JR, Wyllie SG. The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 2000; 88: 170-175
47 Wińska K, Mączka W, Łyczko J, Grabarczyk M, Czubaszek A, Szumny A. Essential oils as antimicrobial agents–myth or real alternative?. Molecules 2019; 24: 2130
48 Muthaiyan A, Martin EM, Natesan S, Crandall PG, Wilkinson BJ, Ricke SC. Antimicrobial effect and mode of action of terpeneless cold pressed valencia orange essential oil on methicillin-resistant Staphylococcus aureus . J Appl Microbiol 2012; 112: 1020-1033
49 Chung EY, Byun YH, Shin EJ, Chung HS, Lee YH, Shin S. Antibacterial effects of vulgarone B from Artemisia iwayomogi alone and in combination with oxacillin. Arch Pharm Res 2009; 32: 1711-1719
50 Ibrahim NA, El-Sakhawy FS, Mohammed MMD, Farid M, Abdel-Wahed N, Deabes D. Chemical composition, antimicrobial and antifungal activities of essential oils of the leaves of Aegle marmelos (L.) Correa growing in Egypt. J Appl Pharm Sci 2015; 5: 001-005
51 Lopes-Lutz D, Alviano DS, Alviano CS, Kolodziejczyk PP. Screening of chemical composition, antimicrobial and antioxidant activities of Artemisia essential oils. Phytochemistry 2008; 69: 1732-1738
52 Hood JR, Wilkinson JM, Cavanagh HMA. Evaluation of common antibacterial screening methods utilized in essential oil research. J Essent Oil Res 2003; 15: 428-433
53 Unlu M, Ergene E, Unlu GV, Zeytinoglu HS, Vural N. Composition, antimicrobial activity and in vitro cytotoxicity of essential oil from Cinnamomum zeylanicum Blume (Lauraceae). Food Chem Toxicol 2010; 48: 3274-3280
54 Moghadam HD, Sani AM, Sangatash MM. Antifungal activity of essential oil of Ziziphora clinopodioides and the inhibition of aflatoxin B1 production in maize grain. Toxicol Ind Health 2016; 32: 493-499
55 Tullio V, Roana J, Scalas D, Mandras N. Evaluation of the antifungal activity of Mentha x Piperita (Lamiaceae) of Pancalieri (Turin, Italy) essential oil and its synergistic interaction with azoles. Molecules 2019; 24: 3148
56 Bona E, Cantamessa S, Pavan M, Novello G, Massa N, Rocchetti A, Berta G, Gamalero E. Sensitivity of Candida albicans to essential oils: are they an alternative to antifungal agents?. J Appl Microbiol 2016; 121: 1530-1545
57 Kalemba D, Kunicka A. Antibacterial and antifungal properties of essential oils. Curr Med Chem 2003; 10: 813-829
58 Adams S, Kunz B, Weidenbörner M. Mycelial deformations of Cladosporium herbarum due to the application of Eugenol or Carvacrol. J Essent Oil Res 1996; 8: 535-540
59 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
60 Hammami S, Jmii H, El Mokni R, Khmiri A, Faidi K, Dhaouadi H, El Aouni MH, Aouni M, Joshi RK. Essential oil composition, antioxidant, cytotoxic and antiviral activities of Teucrium pseudochamaepitys growing spontaneously in Tunisia. Molecules 2015; 20: 20426-20433
61 Brochot A, Guilbot A, Haddioui L, Roques C. Antibacterial, antifungal, and antiviral effects of three essential oil blends. Microbiology open 2017; 6: e459
62 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
63 Tariq S, Wani S, Rasool W, Shafi K, Bhat MA, Prabhakar A, Shalla AH, Rather MA. 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
64 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
65 Venturi CR, Danielli LJ, Klein F, Apel MA, Montanha JA, Bordignon SA, 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
66 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 Microbiol Antimicrob 2007; 6: 10
67 Schuhmacher A, Reichling J, Schnitzler P. Virucidal effect of peppermint oil on the enveloped viruses herpes simplex virus type 1 and type 2 in vitro . Phytomedicine 2003; 10: 504-510
68 Li YC, Peng SZ, Chen HM, Zhang FX, Xu PP, Xie JH, He JJ, Chen JN, Lai XP, Su ZR. Oral administration of patchouli alcohol isolated from Pogostemonis Herba augments protection against influenza viral infection in mice. Int Immunopharmacol 2012; 12: 294-301
69 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
70 García CC, Talarico L, Almeida N, Colombres S, Duschatzky C, Damonte EB. Virucidal activity of essential oils from aromatic plants of San Luis, Argentina. Phytother Res 2003; 17: 1073-1075
71 Gautam N, Mantha AK, Mittal S. Essential oils and their constituents as anticancer agents: a mechanistic view. Biomed Res Int 2014; 2014: 154106
72 Fitsiou E, Pappa A. Anticancer activity of essential oils and other extracts from aromatic plants grown in Greece. Antioxidants (Basel) 2019; 8: 290
73 Liju VB, Jeena K, Kuttan R. Chemopreventive activity of turmeric essential oil and possible mechanisms of action. Asian Pac J Cancer Prev 2014; 15: 6575-6580
74 Di Sotto A, Evandri MG, Mazzanti G. Antimutagenic and mutagenic activities of some terpenes in the bacterial reverse mutation assay. Mutat Res Genet Toxicol Environ Mutagen 2008; 653: 130-133
75 Aras A, Iqbal MJ, Naqvi SK, Gercek YC, Boztas K, Gasparri ML, Shatynska-Mytsyk I, Fayyaz S, Farooqi AA. Anticancer activity of essential oils: targeting of protein networks in cancer cells. Asian Pac J Cancer Prev 2014; 15: 8047-8050
76 Yu GJ, Choi IW, Kim GY, Hwang HJ, Kim BW, Kim CM, Kim WJ, Yoo YH, Choi YH. Induction of reactive oxygen species–mediated apoptosis by purified Schisandrae semen essential oil in human leukemia U937 cells through activation of the caspase cascades and nuclear relocation of mitochondrial apoptogenic factors. Nutr Res 2015; 35: 910-920
77 Pavithra PS, Mehta A, Verma RS. Induction of apoptosis by essential oil from P. missionis in skin epidermoid cancer cells. Phytomedicine 2018; 50: 184-195
78 Zito P, Labbozzetta M, Notarbartolo M, Sajeva M, Poma P. Essential oil of Cyphostemma juttae (Vitaceae): Chemical composition and antitumor mechanism in triple negative breast cancer cells. PLoS One 2019; 14: e0214594
79 Russo A, Cardile V, Graziano ACE, Avola R, Bruno M, Rigano D. Involvement of Bax and Bcl-2 in induction of apoptosis by essential oils of three Lebanese salvia species in human prostate cancer cells. Int J Mol Sci 2018; 19: 292
80 Seal S, Chatterjee P, Bhattacharya S, Pal D, Dasgupta S, Kundu R, Mukherjee S, Bhattacharya S, Bhuyan M, Bhattacharyya PR, Baishya G, Barua NC, Baruah PK, Rao PG, Bhattacharya S. Vapor of volatile oils from Litsea cubeba seed induces apoptosis and causes cell cycle arrest in lung cancer cells. PLoS One 2012; 7: e47014
81 Zuo HX, Jin Y, Wang Z, Li MY, Zhang ZH, Wang JY, Xing Y, Ri MH, Jin CH, Xu GH, Piao LX, Ma J, Jin X. Curcumol inhibits the expression of programmed cell death-ligand 1 through crosstalk between hypoxia-inducible factor-1α and STAT3 (T705) signaling pathways in hepatic cancer. J Ethnopharmacol 2020; 257: 112835
82 Chung KS, Hong JY, Lee JH, Lee HJ, Park JY, Choi JH, Park HJ, Hong J, Lee KT. β-Caryophyllene in the essential oil from Chrysanthemum Boreale induces G₁ phase cell cycle arrest in human lung cancer cells. Molecules 2019; 24: 3754
83 Chidambara Murthy KN, Jayaprakasha GK, Patil BS. D-limonene rich volatile oil from blood oranges inhibits angiogenesis, metastasis and cell death in human colon cancer cells. Life Sci 2012; 91: 429-439
84 Manjamalai A, Kumar MJM, Grace VMB. Essential oil of Tridax procumbens L induces apoptosis and suppresses angiogenesis and lung metastasis of the B16F-10 cell line in C57BL/6 mice. Asian Pac J Cancer Prev 2012; 13: 5887-5895
85 Baldwin IT. Plant volatiles. Curr Biol 2010; 20: R392-R397
86 Nguyen H, Campi EM, Roy Jackson W, Patti AF. Effect of oxidative deterioration on flavour and aroma components of lemon oil. Food Chem 2009; 112: 388-393
87 Neuenschwander U, Guignard F, Hermans I. Mechanism of the aerobic oxidation of α-pinene. ChemSusChem 2010; 3: 75-84
88 Turek C, Stintzing FC. Stability of essential oils: A review. Compr Rev Food Sci Food Saf 2013; 12: 40-53
89 El Asbahani A, Miladi K, Badri W, Sala M, Aït Addi EH, Casabianca H, El Mousadik A, Hartmann D, Jilale A, Renaud FN, Elaissari A. Essential oils: from extraction to encapsulation. Int J Pharm 2015; 483: 220-243
90 Russo M, Rigano F, Arigò A, Sciarrone D, Calabrò ML, Farnetti S, Dugo P, Mondello L. Rapid isolation, reliable characterization, and water solubility improvement of polymethoxyflavones from cold-pressed mandarin essential oil. J Sep Sci 2016; 39: 2018-2027
91 Lee YH, Lee J, Min DB, Pascall MA. Effect of riboflavin on the photo-oxidative stability of vegetable oil in salad dressing. Food Chem 2014; 152: 349-354
92 Beltrame JM, Angnes RA, Chiavelli LUR, da Costa WF, da Rosa MF, da Silva Lobo V, Pomini AM. Photodegradation of essential oil from marjoram (Origanum majorana L.) studied by GC-MS and UV-VIS spectroscopy. Rev latinoam de química 2013; 41: 81-88
93 Turek C, Stintzing FC. Impact of different storage conditions on the quality of selected essential oils. Food Res Int 2012; 46: 341-353
94 Dimarco Palencia FCD, Muñoz VA, Posadaz AC, Cifuente DA, Miskoski S, Ferrari GV, García NA, Montaña MP. Oregano essential oil interactions with photogenerated singlet molecular oxygen. Photochem Photobiol 2020; 96: 1005-1013
95 Olmedo RH, Asensio CM, Grosso NR. Thermal stability and antioxidant activity of essential oils from aromatic plants farmed in Argentina. Ind Crops Prod 2015; 69: 21-28
96 Hădărugă DI, Hădărugă NG, Costescu CI, David I, Gruia AT. Thermal and oxidative stability of the Ocimum basilicum L. essential oil/β-cyclodextrin supramolecular system. Beilstein J Org Chem 2014; 10: 2809-2820
97 Chandran J, Nayana N, Roshini N, Nisha P. Oxidative stability, thermal stability and acceptability of coconut oil flavored with essential oils from black pepper and ginger. J Food Sci Technol 2017; 54: 144-152
98 Asensio CM, Nepote V, Grosso NR. Chemical stability of extra-virgin olive oil added with oregano essential oil. J Food Sci 2011; 76: S445-S450
99 Olmedo R, Ribotta P, Grosso NR. Oxidative stability, affective and discriminative sensory test of high oleic and regular peanut oil with addition of oregano essential oil. J Food Sci Technol 2018; 55: 5133-5141
100 Velasco J, Dobarganes C. Oxidative stability of virgin olive oil. Eur J Lipid Sci Technol 2002; 104: 661-676
101 Sharifi-Rad M, Varoni EM, Iriti M, Martorell M, Setzer WN, Del Mar Contreras M, Salehi B, Soltani-Nejad A, Rajabi S, Tajbakhsh M, Sharifi-Rad J. Carvacrol and human health: A comprehensive review. Phytother Res 2018; 32: 1675-1687
102 Sharifi-Rad J, Sureda A, Tenore GC, Daglia M, Sharifi-Rad M, Valussi M, Tundis R, Sharifi-Rad M, Loizzo MR, Ademiluyi AO, Sharifi-Rad R, Ayatollahi SA, Iriti M. Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules 2017; 22: 70
103 Samperio C, Boyer R, Eigel WN, Holland KW, McKinney JS, OʼKeefe SF, Smith R, Marcy JE. Enhancement of plant essential oilsʼ aqueous solubility and stability using alpha and beta cyclodextrin. J Agric Food Chem 2010; 58: 12950-12956
104 Shin J, Na K, Shin S, Seo SM, Youn HJ, Park IK, Hyun J. Biological activity of thyme white essential oil stabilized by cellulose nanocrystals. Biomolecules 2019; 9: 799
105 Sagalowicz L, Leser ME. Delivery systems for liquid food products. Curr Opin Colloid Interface Sci 2010; 15: 61-72
106 Zhang X, Xing H, Zhao Y, Ma Z. Pharmaceutical dispersion techniques for dissolution and bioavailability enhancement of poorly water-soluble drugs. Pharmaceutics 2018; 10: 74
107 de Matos SP, Lucca LG, Koester LS. Essential oils in nanostructured systems: Challenges in preparation and analytical methods. Talanta 2019; 195: 204-214
108 Matshetshe KI, Parani S, Manki SM, Oluwafemi OS. Preparation, characterization and in vitro release study of β-cyclodextrin/chitosan nanoparticles loaded Cinnamomum zeylanicum essential oil. Int J Biol Macromol 2018; 118: 676-682
109 Narayan R, Nayak UY, Raichur AM, Garg S. Mesoporous silica nanoparticles: A comprehensive review on synthesis and recent advances. Pharmaceutics 2018; 10: 118
110 Garcia-Bennett AE. Synthesis, toxicology and potential of ordered mesoporous materials in nanomedicine. Nanomedicine (Lond) 2011; 6: 867-877
111 Yamamoto E, Kuroda K. Preparation and controllability of mesoporous silica nanoparticles. Enzymes 2018; 44: 1-10
112 Das S, Horváth B, Šafranko S, Jokić S, Széchenyi A, Kőszegi T. Antimicrobial activity of chamomile essential oil: Effect of different formulations. Molecules 2019; 24: 4321
113 Jin L, Teng J, Hu L, Lan X, Xu Y, Sheng J, Song Y, Wang M. Pepper fragrant essential oil (PFEO) and functionalized MCM-41 nanoparticles: formation, characterization, and bactericidal activity. J Sci Food Agric 2019; 99: 5168-5175
114 Ebadollahi A, Sendi JJ, Aliakbar A. Efficacy of Nanoencapsulated Thymus eriocalyx and Thymus kotschyanus Essential Oils by a Mesoporous Material MCM-41 Against Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 2017; 110: 2413-2420
115 Mody VV, Siwale R, Singh A, Mody HR. Introduction to metallic nanoparticles. J Pharm Bioallied Sci 2010; 2: 282-289
116 Abbasi E, Milani M, Fekri Aval S, Kouhi M, Akbarzadeh A, Tayefi Nasrabadi H, Nikasa P, Joo SW, Hanifehpour Y, Nejati-Koshki K, Samiei M. Silver nanoparticles: Synthesis methods, bio-applications and properties. Crit Rev Microbiol 2016; 42: 173-180
117 Manju S, Malaikozhundan B, Vijayakumar S, Shanthi S, Jaishabanu A, Ekambaram P, Vaseeharan B. Antibacterial, antibiofilm and cytotoxic effects of Nigella sativa essential oil coated gold nanoparticles. Microb Pathog 2016; 91: 129-135
118 Sheny DS, Mathew J, Philip D. Synthesis characterization and catalytic action of hexagonal gold nanoparticles using essential oils extracted from Anacardium occidentale . Spectrochim Acta A Mol Biomol Spectrosc 2012; 97: 306-310
119 Sundararajan B, Ranjitha Kumari BD. Novel synthesis of gold nanoparticles using Artemisia vulgaris L. leaf extract and their efficacy of larvicidal activity against dengue fever vector Aedes aegypti L. J Trace Elem Med Biol 2017; 43: 187-196
120 Hosseinzadeh N, Shomali T, Hosseinzadeh S, Raouf Fard F, Pourmontaseri M, Fazeli M. Green synthesis of gold nanoparticles by using Ferula persica Willd. gum essential oil: production, characterization and in vitro anti-cancer effects. J Pharm Pharmacol 2020; 72: 1013-1025
121 Sutthanont N, Attrapadung S, Nuchprayoon S. Larvicidal activity of synthesized silver nanoparticles from Curcuma zedoaria essential oil against Culex quinquefasciatus . Insects 2019; 10: 27
122 Veisi H, Dadres N, Mohammadi P, Hemmati S. Green synthesis of silver nanoparticles based on oil-water interface method with essential oil of orange peel and its application as nanocatalyst for A3 coupling. Materials Science and Engineering: C 2019; 105: 110031
123 Sebaaly C, Jraij A, Fessi H, Charcosset C, Greige-Gerges H. Preparation and characterization of clove essential oil-loaded liposomes. Food Chem 2015; 178: 52-62
124 Coimbra M, Isacchi B, van Bloois L, Torano JS, Ket A, Wu X, Broere F, Metselaar JM, Rijcken CJ, Storm G, Bilia R, Schiffelers RM. Improving solubility and chemical stability of natural compounds for medicinal use by incorporation into liposomes. Int J Pharm 2011; 416: 433-442
125 Kfoury M, Landy D, Ruellan S, Auezova L, Greige-Gerges H, Fourmentin S. Nootkatone encapsulation by cyclodextrins: Effect on water solubility and photostability. Food Chem 2017; 236: 41-48
126 Kumar S, Pooja. Trotta F, Rao R. Encapsulation of Babchi oil in cyclodextrin-based nanosponges: physicochemical characterization, photodegradation, and In Vitro cytotoxicity studies. Pharmaceutics 2018; 10: 169
127 Pereira KC, Quintela ED, da Silva DJ, do Nascimento VA, da Rocha DVM, Silva JFAE, Forim MR, Silva FG, Cazal CM. Characterization of nanospheres containing Zanthoxylum riedelianum fruit essential oil and their insecticidal and deterrent activities against Bemisia tabaci (Hemiptera: Aleyrodidae). Molecules 2018; 23: 2052
128 Christofoli M, Costa ECC, Bicalhoc KU, de Cássia Domingues V, Fernandes Peixoto M, Fernandes Alves CC, Araújo WL, Cazal CM. Insecticidal effect of nanoencapsulated essential oils from Zanthoxylum rhoifolium (Rutaceae) in Bemisia tabaci populations. Ind Crops Prod 2015; 70: 301-308
129 Shetta A, Kegere J, Mamdouh W. Comparative study of encapsulated peppermint and green tea essential oils in chitosan nanoparticles: Encapsulation, thermal stability, in-vitro release, antioxidant and antibacterial activities. Int J Biol Macromol 2019; 126: 731-742
130 Woranuch S, Yoksan R. Eugenol-loaded chitosan nanoparticles: I. Thermal stability improvement of eugenol through encapsulation. Carbohydr Polym 2013; 96: 578-585
131 Almeida KB, Ramos AS, Nunes JBB, Silva BO, Ferraz ERA, Fernandes AS, Felzenszwalb I, Amaral ACF, Roullin VG, Falcão DQ. PLGA nanoparticles optimized by Box-Behnken for efficient encapsulation of therapeutic Cymbopogon citratus essential oil. Colloids Surf B Biointerfaces 2019; 181: 935-942
132 Lv Y, Yang F, Li X, Zhang X, Abbas S. Formation of heat-resistant nanocapsules of jasmine essential oil via gelatin/gum arabic based complex coacervation. Food Hydrocoll 2014; 35: 305-314
133 da Rosaa CG, de Oliveira Brisola Maciel MV, de Carvalho SM, Zapelini de Melo AP, Jummes B, da Silva T, Martelli SM, Villetti MA, Cleber Bertoldi F, Barreto PLM. Characterization and evaluation of physicochemical and antimicrobial properties of zein nanoparticles loaded with phenolics monoterpenes. Colloids Surf A Physicochem Eng Asp 2015; 481: 337-344
134 Donsì F, Annunziata M, Vincensi M, Ferrari G. Design of nanoemulsion-based delivery systems of natural antimicrobials: effect of the emulsifier. J Biotechnol 2012; 159: 342-350
135 Shi F, Zhao JH, Liu Y, Wang Z, Zhang YT, Feng NP. Preparation and characterization of solid lipid nanoparticles loaded with frankincense and myrrh oil. Int J Nanomedicine 2012; 7: 2033-2043
136 Qiu C, Chang R, Yang J, Ge S, Xiong L, Zhao M, Li M, Sun Q. Preparation and characterization of essential oil-loaded starch nanoparticles formed by short glucan chains. Food Chem 2017; 221: 1426-1433
137 da Cunha JA, de Ávila Scheeren C, Fausto VP, de Melo LDW, Henneman B, Frizzo CP, de Almeida Vaucher R, Castagna de Vargas A, Baldisserotto B. The antibacterial and physiological effects of pure and nanoencapsulated Origanum majorana essential oil on fish infected with Aeromonas hydrophila . Microb Pathog 2018; 124: 116-121
138 Cui H, Li W, Li C, Vittayapadung S, Lin L. Liposome containing cinnamon oil with antibacterial activity against methicillin-resistant Staphylococcus aureus biofilm. Biofouling 2016; 32: 215-225
139 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
140 Mokarizadeh M, Kafil HS, Ghanbarzadeh S, Alizadeh A, Hamishehkar H. Improvement of citral antimicrobial activity by incorporation into nanostructured lipid carriers: a potential application in food stuffs as a natural preservative. Res Pharm Sci 2017; 12: 409-415
141 Bravo Cadena M, Preston GM, Van der Hoorn RAL, Flanagan NA, Townley HE, Thompson IP. Enhancing cinnamon essential oil activity by nanoparticle encapsulation to control seed pathogens. Ind Crops Prod 2018; 124: 755-764
142 Chan AC, Bravo Cadena M, Townley HE, Fricker MD, Thompson IP. Effective delivery of volatile biocides employing mesoporous silicates for treating biofilms. J R Soc Interface 2017; 14: 20160650
143 Hasheminejad N, Khodaiyan F, Safari M. Improving the antifungal activity of clove essential oil encapsulated by chitosan nanoparticles. Food Chem 2019; 275: 113-122
144 Beyki M, Zhaveh S, Khalili ST, Rahmani-Cheratic T, Abollahi A, Bayat M, Tabatabaei M, Mohsenifar A. Encapsulation of Mentha piperita essential oils in chitosan–cinnamic acid nanogel with enhanced antimicrobial activity against Aspergillus flavus . Ind Crops Prod 2014; 54: 310-319
145 Seibert JB, Viegas JSR, Almeida TC, Amparo TR, Rodrigues IV, Lanza JS, Frézard FJG, Soares RDOA, Teixeira LFM, de Souza GHB, Vieira PMA, Barichello JM, Dos Santos ODH. Nanostructured systems improve the antimicrobial potential of the essential oil from Cymbopogon densiflorus leaves. J Nat Prod 2019; 82: 3208-3220
146 Nasseri M, Golmohammadzadeh S, Arouiee H, Jaafari MR, Neamati H. Antifungal activity of Zataria multiflora essential oil-loaded solid lipid nanoparticles in-vitro condition. Iran J Basic Med Sci 2016; 19: 1231-1237
147 Fazly Bazzaz BS, Khameneh B, Namazi N, Iranshahi M, Davoodi D, Golmohammadzadeh S. Solid lipid nanoparticles carrying Eugenia caryophyllata essential oil: the novel nanoparticulate systems with broad-spectrum antimicrobial activity. Lett Appl Microbiol 2018; 66: 506-513
148 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 Farmacog 2018; 28: 495-502
149 Sinico C, De Logu A, Lai F, Valenti D, Manconi M, Loy G, Bonsignore L, Fadda AM. Liposomal incorporation of Artemisia arborescens L. essential oil and in vitro antiviral activity. Eur J Pharm Biopharm 2005; 59: 161-168
150 Valenti D, De Logu A, Loy G, Sinico C, Bonsignore L, Cottiglia F, Garau D, Fadda AM. Liposome-incorporated santolina insularis essential oil: preparation, characterization and in vitro antiviral activity. J Liposome Res 2001; 11: 73-90
151 Natrajan D, Srinivasan S, Sundar K, Ravindran A. Formulation of essential oil-loaded chitosan-alginate nanocapsules. J Food Drug Anal 2015; 23: 560-568
152 Onyebuchi C, Kavaz D. Chitosan and N, N, N-trimethyl chitosan nanoparticle encapsulation of Ocimum Gratissimum essential oil: Optimised synthesis, in vitro release and bioactivity. Int J Nanomedicine 2019; 14: 7707-7727
153 Sonia, Komal. Kukreti S, Kaushik M. Exploring the DNA damaging potential of chitosan and citrate-reduced gold nanoparticles: Physicochemical approach. Int J Biol Macromol 2018; 115: 801-810
154 White B, Evison A, Dombi E, Townley HE. Improved delivery of the anticancer agent citral using BSA nanoparticles and polymeric wafers. Nanotechnol Sci Appl 2017; 10: 163-175
155 Celia C, Trapasso E, Locatelli M, Navarra M, Ventura CA, Wolfram J, Carafa M, Morittu VM, Britti D, Di Marzio L, Paolino D. Anticancer activity of liposomal Bergamot Essential Oil (BEO) on human neuroblastoma cells. Colloids Surf B Biointerfaces 2013; 112: 548-553
156 Nirmala MJ, Durai L, Rao KA, Nagarajan R. Ultrasonic nanoemulsification of Cuminum cyminum essential oil and its applications in medicine. Int J Nanomedicine 2020; 15: 795-807
157 Al-Otaibi WA, Alkhatib MH, Wali AN. Cytotoxicity and apoptosis enhancement in breast and cervical cancer cells upon coadministration of mitomycin C and essential oils in nanoemulsion formulations. Biomed Pharmacother 2018; 106: 946-955
158 Ali H, Al-Khalifa AR, Aouf A, Boukhebti H, Farouk A. Effect of nanoencapsulation on volatile constituents, and antioxidant and anticancer activities of Algerian Origanum glandulosum Desf. essential oil. Sci Rep 2020; 10: 2812
159 Liakos IL, Grumezescu AM, Holban AM, Florin I, DʼAutilia F, Carzino R, Bianchini P, Athanassiou A. Polylactic acid–lemongrass essential oil nanocapsules with antimicrobial properties. Pharmaceuticals 2016; 9: 42
160 da Cunha JA, de Ávila Scheeren C, Fausto VP, de Melo LDW, Henneman B, Frizzo CP, de Almeida Vaucher R, Castagna de Vargas A, Baldisserotto B. The antibacterial and physiological effects of pure and nanoencapsulated Origanum majorana essential oil on fish infected with Aeromonas hydrophila . Microb Pathog 2018; 124: 116-121
161 Keawchaoon L, Yoksan R. Preparation, characterization and in vitro release study of carvacrol-loaded chitosan nanoparticles. Colloids Surf B Biointerfaces 2011; 84: 163-171
162 Esmaeili A, Asgari A. In vitro release and biological activities of Carum copticum essential oil (CEO) loaded chitosan nanoparticles. Int J Biol Macromol 2015; 81: 283-290
163 Low WL, Martin C, Hill DJ, Kenward MA. Antimicrobial efficacy of liposome-encapsulated silver ions and tea tree oil against Pseudomonas aeruginosa, Staphylococcus aureus and Candida albicans . Lett Appl Microbiol 2013; 57: 33-39
164 Sonu KS, Mann B, Sharma R, Kumar R, Singh R. Physico-chemical and antimicrobial properties of d-limonene oil nanoemulsion stabilized by whey protein–maltodextrin conjugates. J Food Sci Technol 2018; 55: 2749-2757
165 Xue J, Michael Davidson P, Zhong Q. Antimicrobial activity of thyme oil co-nanoemulsified with sodium caseinate and lecithin. Int J Food Microbiol 2015; 210: 1-8
166 Lei K, Wang X, Li X, Wang L. The innovative fabrication and applications of carvacrol nanoemulsions, carboxymethyl chitosan microgels and their composite films. Colloids Surf B Biointerfaces 2019; 175: 688-696
167 Saporito F, Sandri G, Bonferoni MC, Rossi S, Boselli C, Icaro Cornaglia A, Mannucci B, Grisoli P, Vigani B, Ferrari F. Essential oil-loaded lipid nanoparticles for wound healing. Int J Nanomedicine 2017; 13: 175-186
168 Vilas V, Philip D, Mathew J. Essential oil mediated synthesis of silver nanocrystals for environmental, anti-microbial and antioxidant applications. Mater Sci Eng C 2016; 61: 429-436
169 Chang Y, McLandsborough L, McClements DJ. Physicochemical properties and antimicrobial efficacy of carvacrol nanoemulsions formed by spontaneous emulsification. J Agric Food Chem 2013; 61: 8906-8913
170 Tubtimsri S, Limmatvapirat C, Limsirichaikul S, Akkaramongkolporn P, Inoue Y, Limmatvapirat S. Fabrication and characterization of spearmint oil loaded nanoemulsions as cytotoxic agents against oral cancer cell. Asian J Pharm Sci 2018; 13: 425-437
171 Zielińska A, Martins-Gomes C, Ferreira NR, Silva AM, Nowak I, Souto EB. Anti-inflammatory and anti-cancer activity of citral: Optimization of citral-loaded solid lipid nanoparticles (SLN) using experimental factorial design and LUMiSizer^® . Int J Pharm 2018; 553: 428-440