Application of Three Types of Cinnamon Essential Oils as Natural Antifungal Preservatives in Wheat Bread
Abstract
:1. Introduction
2. Materials and Methods
2.1. Analyzed EOs
2.2. Assessment of EOs Chemical Profile
2.3. Antioxidant Activity of EOs
2.4. Antifungal Efficacies of EOs
2.4.1. Strains of Fungi
2.4.2. Antifungal (In Vitro) Properties of EOs
2.4.3. Antifungal (In Situ) Properties of EOs
2.4.4. Food Model
2.4.5. Food Model Moisture Content and Water Activity
2.4.6. Microbial Characterization of Bread Loaves during Their Storage
2.4.7. Vapor Contact Method
2.4.8. Fungal Growth Inhibition
2.5. Statistical Analysis
3. Results
3.1. Chemical Profile of EOs
3.2. Antioxidant Activity of EOs
3.3. Antifungal Properties of EOs in In Vitro Conditions
3.4. Technological Properties of Food Model
3.5. Microbiological Characterization of Food Model
3.6. Antifungal Properties of EOs in In-Situ Conditions
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Garcia, M.V.; Bernardi, A.O.; Copetti, M.V. The fungal problem in bread production: Insights of causes, consequences, and control methods. Curr. Opin. Food Sci. 2019, 29, 1–6. [Google Scholar] [CrossRef]
- Day, L. Cereal Food Production with Low Salt. In Reference Module in Food Science; Elsevier: Amsterdam, The Netherlands, 2016. [Google Scholar]
- Garcia, M.V.; Garcia-Cela, E.; Magan, N.; Copetti, M.V.; Medina, A. Comparative growth inhibition of bread spoilage fungi by different preservative concentrations using a rapid turbidimetric assay system. Front. Microbiol. 2021, 12, 678406. [Google Scholar] [CrossRef]
- Melini, V.; Melini, F. Strategies to extend bread and GF bread shelf-life: From Sourdough to antimicrobial active packaging and nanotechnology. Fermentation 2018, 4, 9. [Google Scholar] [CrossRef] [Green Version]
- Axel, C.; Zannini, E.; Arendt, E.K. Mold spoilage of bread and its biopreservation: A review of current strategies for bread shelf life extension. Crit. Rev. Food Sci. Nutr. 2017, 57, 3528–3542. [Google Scholar] [CrossRef] [PubMed]
- Guleria, S.; Tiku, A.K.; Gupta, S.; Singh, G.; Koul, A.; Razdan, V.K. Chemical composition, antioxidant activity and inhibitory effects of essential oil of Eucalyptus teretecornis grown in north-western Himalaya against Alternaria alternata. J. Plant Biochem. Biotechnol. 2012, 21, 44–50. [Google Scholar] [CrossRef]
- Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar, M. Biological effects of essential oil—A review. Food Chem. Toxicol. 2008, 46, 446–475. [Google Scholar] [CrossRef]
- Sánchez-González, L.; Vargas, M.; González-Martínez, C.; Chiralt, A.; Chafer, M. Use of essential oils in bioactive edible coatings: A review. Food Eng. Rev. 2011, 3, 1–16. [Google Scholar] [CrossRef]
- Conde-Hernández, L.A.; Espinosa-Victoria, J.R.; Trejo, A.; Guerrero-Beltrán, J.Á. CO2-supercritical extraction, hydrodistillation and steam distillation of essential oil of rosemary (Rosmarinus officinalis). J. Food Eng. 2017, 200, 81–86. [Google Scholar] [CrossRef]
- Zhuang, X.; Zhang, Z.; Wang, Y.; Li, Y. The effect of alternative solvents to n-hexane on the green extraction of Litsea cubeba kernel oils as new oil sources. Ind. Crops Prod. 2018, 126, 340–346. [Google Scholar] [CrossRef]
- Moon, J.N.; Getachew, A.T.; Haque, A.T.; Saravana, P.S.; Cho, Y.J.; Nkurunziza, D.; Chun, B.S. Physicochemical characterization and deodorant activity of essential oil recovered from Asiasarum heterotropoides using supercritical carbon dioxide and organic solvents. J. Ind. Eng. Chem. 2019, 69, 217–224. [Google Scholar] [CrossRef]
- Aumeeruddy-Elalfi, Z.; Lall, N.; Fibrich, B.; Van Staden, A.B.; Hosenally, M.; Mahomoodally, M.F. Selected essential oils inhibit key physiological enzymes and possess intracellular and extracellular antimelanogenic properties in vitro. J. Food Drug Anal. 2018, 26, 232–243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bona, E.; Cantamessa, S.; Pavan, M.; Novello, G.; Massa, N.; Rocchetti, A.; Gamalero, E. Sensitivity of Candida albicans to essential oils: Are they an alternative to antifungal agents? J. Appl. Microbiol. 2016, 121, 1530–1545. [Google Scholar] [CrossRef] [PubMed]
- Altintas, A.; Tabanca, N.; Tyihák, E.; Ott, P.G.; Móricz, Á.M.; Mincsovics, E.; Wedge, D.E. Characterization of volatile constituents from Origanum onites and their antifungal and antibacterial activity. J. AOAC Int. 2013, 96, 1200–1208. [Google Scholar] [CrossRef] [PubMed]
- Burt, S. Essential oils: Their antibacterial properties and potential applications in foods—A review. Int. J. Food Microbiol. 2004, 94, 223–253. [Google Scholar] [CrossRef]
- Wu, J.; Sun, X.; Guo, X.; Ge, S.; Zhang, Q. Physicochemical properties, antimicrobial activity and oil release of fish gelatin films incorporated with cinnamon essential oil. Aquac. Fish. 2017, 2, 185–192. [Google Scholar] [CrossRef]
- Zhang, Y.; Li, D.; Lv, J.; Li, Q.; Kong, C.; Luo, Y. Effect of cinnamon essential oil on bacterial diversity and shelf-life in vacuum-packaged common carp (Cyprinus carpio) during refrigerated storage. Int. J. Food Microbiol. 2017, 249, 1–8. [Google Scholar] [CrossRef]
- Sriramavaratharajan, V.; Sudha, V.; Murugan, R. Characterization of the leaf essential oils of an endemic species Cinnamomum perrottetii from Western Ghats, India. Nat. Prod. Res. 2016, 30, 1085–1087. [Google Scholar] [CrossRef]
- Singh, N.; Rao, A.S.; Nandal, A.; Kumar, S.; Yadav, S.S.; Ganaie, S.A.; Narasimhan, B. Phytochemical and pharmacological review of Cinnamomum verum J. Presl-a versatile spice used in food and nutrition. Food Chem. 2021, 338, 127773. [Google Scholar] [CrossRef]
- Schmidt, E.; Jirovetz, L.; Buchbauer, G.; Eller, G.A.; Stoilova, I.; Krastanov, A.; Geissler, M. Composition and antioxidant activities of the essential oil of cinnamon (Cinnamomum zeylanicum Blume) leaves from Sri Lanka. J. Essent. Oil Bear. Plants 2006, 9, 170–182. [Google Scholar] [CrossRef]
- Hamidpour, R.; Hamidpour, M.; Hamidpour, S.; Shahlari, M. Cinnamon from the selection of traditional applications to its novel effects on the inhibition of angiogenesis in cancer cells and prevention of Alzheimer’s disease, and a series of functions such as antioxidant, anticholesterol, antidiabetes, antibacterial, antifungal, nematicidal, acaracidal, and repellent activities. J. Tradit. Complement. Med. 2015, 5, 66–70. [Google Scholar]
- Ahmed, H.M.; Ramadhani, A.M.; Erwa, I.Y.; Ishag, O.A.O.; Saeed, M.B. Phytochemical screening, chemical composition and antimicrobial activity of cinnamon verum bark. Int. Res. J. Pure Appl. Chem 2020, 21, 36–43. [Google Scholar] [CrossRef]
- Ribeiro, P.R.E.; Montero, I.F.; Saravia, S.A.M.; Ferraz, V.P.; Santos, R.A.; Marca, J.F.; Linhares, B.M. Chemical composition and antioxidant activity in the essential oil of Cinnamomum zeylanicum Nees with medicinal interest. J. Med. Plant Res. 2020, 14, 326–330. [Google Scholar] [CrossRef]
- Chakraborty, A.; Sankaran, V.; Ramar, M.; Chellappan, D.R. Chemical analysis of leaf essential oil of Cinnamomum verum from Palni hills, Tamil Nadu. Tic 2015, 3, 10. [Google Scholar]
- Farias, A.P.P.; Monteiro, O.D.S.; da Silva, J.K.R.; Figueiredo, P.L.B.; Rodrigues, A.A.C.; Monteiro, I.N.; Maia, J.G.S. Chemical composition and biological activities of two chemotype-oils from Cinnamomum verum J. Presl growing in North Brazil. J. Food Sci. Technol. 2020, 57, 3176–3183. [Google Scholar] [CrossRef]
- Huang, D.F.; Xu, J.G.; Liu, J.X.; Zhang, H.; Hu, Q.P. Chemical constituents, antibacterial activity and mechanism of action of the essential oil from Cinnamomum cassia bark against four food-related bacteria. Microbiology 2014, 83, 357–365. [Google Scholar] [CrossRef]
- Jayaprakasha, G.K.; Rao, L.J.; Sakariah, K.K. Chemical composition of the volatile oil from the fruits of Cinnamomum zeylanicum Blume. Flavour Fragr. J. 1997, 12, 331–333. [Google Scholar] [CrossRef]
- Jayaprakasha, G.K.; Jagan Mohan Rao, L.; Sakariah, K.K. Chemical composition of the flower oil of Cinnamomum zeylanicum Blume. J. Agric. Food Chem. 2000, 48, 4294–4295. [Google Scholar] [CrossRef]
- Cheng, S.S.; Liu, J.Y.; Hsui, Y.R.; Chang, S.T. Chemical polymorphism and antifungal activity of essential oils from leaves of different provenances of indigenous cinnamon (Cinnamomum osmophloeum). Bioresour. Technol. 2006, 97, 306–312. [Google Scholar] [CrossRef]
- Ooi, L.S.; Li, Y.; Kam, S.L.; Wang, H.; Wong, E.Y.; Ooi, V.E. Antimicrobial activities of cinnamon oil and cinnamaldehyde from the Chinese medicinal herb Cinnamomum cassia Blume. Am. J. Chin. Med. 2006, 34, 511–522. [Google Scholar] [CrossRef]
- Akrami, S.; Amin, M.; Saki, M. In Vitro evaluation of the antibacterial effects of Cinnamomum zeylanicum essential oil against clinical multidrug-resistant Shigella isolates. Mol. Biol. Rep. 2021, 48, 2583–2589. [Google Scholar] [CrossRef]
- Bermúdez-Capdevila, M.; Cervantes-Huamán, B.R.H.; Rodríguez-Jerez, J.J.; Ripolles-Avila, C. Repeated sub-inhibitory doses of cassia essential oil do not increase the tolerance pattern in Listeria monocytogenes cells. LWT 2022, 165, 113681. [Google Scholar] [CrossRef]
- Soliman, K.M.; Badeaa, R.I. Effect of oil extracted from some medicinal plants on different mycotoxigenic fungi. Food Chem. Toxicol. 2002, 40, 1669–1675. [Google Scholar] [CrossRef]
- Matan, N.; Rimkeeree, H.; Mawson, A.J.; Chompreeda, P.; Haruthaithanasan, V.; Parker, M. Antimicrobial activity of cinnamon and clove oils under modified atmosphere conditions. Int. J. Food Microbiol. 2006, 107, 180–185. [Google Scholar] [CrossRef] [PubMed]
- Rashid, Z.; Khan, M.R.; Mubeen, R.; Hassan, A.; Saeed, F.; Afzaal, M. Exploring the effect of cinnamon essential oil to enhance the stability and safety of fresh apples. J. Food Process. Preserv. 2020, 44, e14926. [Google Scholar] [CrossRef]
- Xing, Y.; Li, X.; Xu, Q.; Yun, J.; Lu, Y. Antifungal activities of cinnamon oil against Rhizopus nigricans, Aspergillus flavus and Penicillium expansum in vitro and in vivo fruit test. Int. J. Sci. 2020, 45, 1837–1842. [Google Scholar]
- Jokar, A.; Barzegar, H.; Maftoon Azad, N.; Shahamirian, M. Effects of cinnamon essential oil and Persian gum on preservation of pomegranate arils. Food Sci. Nutr. 2021, 9, 2585–2596. [Google Scholar] [CrossRef]
- He, S.; Wang, Y. Antimicrobial and Antioxidant Effects of Kappa-Carrageenan Coatings Enriched with Cinnamon Essential Oil in Pork Meat. Foods 2022, 11, 2885. [Google Scholar] [CrossRef]
- Morshdy, A.E.M.; Al-Mogbel, M.S.; Mohamed, M.E.; Elabbasy, M.T.; Elshafee, A.K.; Hussein, M.A. Bioactivity of essential oils for mitigation of Listeria monocytogenes isolated from fresh retail chicken meat. Foods 2021, 10, 3006. [Google Scholar] [CrossRef]
- Ogwaro, B.A.; O’Gara, E.A.; Hill, D.J.; Gibson, H. A Study of the Antimicrobial Activity of Combined Black Pepper and Cinnamon Essential Oils against Escherichia fergusonii in Traditional African Yoghurt. Foods 2021, 10, 2847. [Google Scholar] [CrossRef]
- Bandyopadhyay, S.; Saha, N.; Zandraa, O.; Pummerová, M.; Sáha, P. Essential oil based PVP-CMC-BC-GG functional hydrogel sachet for ‘cheese’: Its shelf life confirmed with anthocyanin (Isolated from red cabbage) bio stickers. Foods 2021, 9, 307. [Google Scholar] [CrossRef] [Green Version]
- Tantakasem, S. Effect of cinnamon and clove essential oils for extended shelf life of bread. Warasan Ahan 2005, 9, 51–57. [Google Scholar]
- Rodriguez, A.; Nerín, C.; Batlle, R. New cinnamon-based active paper packaging against Rhizopus stolonifer food spoilage. J. Agric. Food Chem. 2008, 56, 6364–6369. [Google Scholar] [CrossRef] [PubMed]
- Cazella, L.N.; Glamoclija, J.; Soković, M.; Gonçalves, J.E.; Linde, G.A.; Colauto, N.B.; Gazim, Z.C. Antimicrobial activity of essential oil of Baccharis dracunculifolia DC (Asteraceae) aerial parts at flowering period. Front. Plant Sci. 2020, 10, 27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Valková, V.; Ďúranová, H.; Vukovic, N.L.; Vukic, M.; Kluz, M.; Kačániová, M. Assessment of Chemical Composition and Anti-Penicillium Activity of Vapours of Essential Oils from Abies Alba and Two Melaleuca Species in Food Model Systems. Molecules 2022, 27, 3101. [Google Scholar] [CrossRef] [PubMed]
- Valková, V.; Ďúranová, H.; Galovičová, L.; Borotová, P.; Vukovic, N.L.; Vukic, M.; Kačániová, M. Cymbopogon citratus Essential Oil: Its Application as an Antimicrobial Agent in Food Preservation. Agronomy 2022, 12, 155. [Google Scholar] [CrossRef]
- Valková, V.; Ďúranová, H.; Štefániková, J.; Miškeje, M.; Tokár, M.; Gabríny, L.; Kowalczewski, P.L.; Kačániová, M. Wheat bread with grape seeds micropowder: Impact on dough rheology and bread properties. Appl. Rheol. 2020, 30, 138–150. [Google Scholar] [CrossRef]
- Kunová, S.; Sendra, E.; Haščík, P.; Vuković, N.L.; Vukić, M.D.; Hsouna, A.B.; Mnif, W.; Kačániová, M. Microbiological Quality of Deer Meat Treated with Essential Oil Litsea cubeba. Animals 2022, 12, 2315. [Google Scholar] [CrossRef]
- Wan, J.; Zhong, S.; Schwarz, P.; Chen, B.; Rao, J. Physical properties, antifungal and mycotoxin inhibitory activities of five essential oil nanoemulsions: Impact of oil compositions and processing parameters. Food Chem. 2019, 291, 199–206. [Google Scholar] [CrossRef]
- Miguel, M.G. Antioxidant activity of medicinal and aromatic plants. A review. Flavour Fragr. J. 2010, 25, 291–312. [Google Scholar] [CrossRef]
- Kim, J.E.; Lee, J.E.; Huh, M.J.; Lee, S.C.; Seo, S.M.; Kwon, J.H.; Park, I.K. 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 2019, 9, 561. [Google Scholar] [CrossRef] [Green Version]
- Li, C.; Luo, Y.; Zhang, W.; Cai, Q.; Wu, X.; Tan, Z.; Zhang, L. A comparative study on chemical compositions and biological activities of four essential oils: Cymbopogon citratus (DC.) Stapf, Cinnamomum cassia (L.) Presl, Salvia japonica Thunb. and Rosa rugosa Thunb. J. Ethnopharmacol. 2021, 280, 114472. [Google Scholar] [CrossRef] [PubMed]
- Chahbi, A.; Nassik, S.; El Amri, H.; Douaik, A.; Maadoudi, E.; Haj, E.; El Hadrami, E.M. Chemical composition and antimicrobial activity of the essential oils of two aromatic plants cultivated in Morocco (Cinnamomum cassia and Origanum compactum). J. Chem. 2020, 2020, 1628710. [Google Scholar] [CrossRef]
- Alizadeh Behbahani, B.; Falah, F.; Lavi Arab, F.; Vasiee, M.; Tabatabaee Yazdi, F. Chemical composition and antioxidant, antimicrobial, and antiproliferative activities of Cinnamomum zeylanicum bark essential oil. Evid.-Based Complement. Altern. Med. 2020, 2020, 5190603. [Google Scholar] [CrossRef] [PubMed]
- Unlu, M.; Ergene, E.; Unlu, G.V.; Zeytinoglu, H.S.; Vural, N. Composition, antimicrobial activity and in vitro cytotoxicity of essential oil from Cinnamomum zeylanicum Blume (Lauraceae). Food Chem. Toxicol. 2010, 48, 3274–3280. [Google Scholar] [CrossRef] [PubMed]
- Gende, L.B.; Floris, I.; Fritz, R.; Eguaras, M.J. Antimicrobial activity of cinnamon (Cinnamomum zeylanicum) essential oil and its main components against Paenibacillus larvae from Argentine. Bull. Insectology 2008, 61, 1. [Google Scholar]
- Monteiro, I.N.; dos Santos Monteiro, O.; Costa-Junior, L.M.; da Silva Lima, A.; de Aguiar Andrade, E.H.; Maia, J.G.S.; Mouchrek Filho, V.E. Chemical composition and acaricide activity of an essential oil from a rare chemotype of Cinnamomum verum Presl on Rhipicephalus microplus (Acari: Ixodidae). Veter. Parasit. 2017, 238, 54–57. [Google Scholar] [CrossRef]
- Wołosiak, R.; Drużyńska, B.; Derewiaka, D.; Piecyk, M.; Majewska, E.; Ciecierska, M.; Pakosz, P. Verification of the Conditions for Determination of Antioxidant Activity by Abts and Dpph Assays—A Practical Approach. Molecules 2021, 27, 50. [Google Scholar] [CrossRef]
- Gholamhosseinpour, A.; Hashemi, S.M.B.; Jafarpour, D. Nanoemulsion of Satureja sahendica bornm essential oil: Antibacterial and antioxidant activities. J. Food Meas. Charact. 2022, 2022, 1–7. [Google Scholar] [CrossRef]
- Sanjay, S.S.; Shukla, A.K. Potential Therapeutic Applications of Nano-Antioxidants; Springer: Berlin/Heidelberg, Germany, 2021. [Google Scholar]
- Higgins, C.L.; Filip, S.V.; Afsar, A.; Colquhoun, H.M.; Hayes, W. From food to mobility: Investigating a screening assay for new automotive antioxidants using the stable radical DPPH. Chem. Sel. 2021, 6, 9179–9184. [Google Scholar] [CrossRef]
- Diniz do Nascimento, L.; Moraes, A.A.B.D.; Costa, K.S.D.; Pereira Galúcio, J.M.; Taube, P.S.; Costa, C.M.L.; Faria, L.J.G.D. Bioactive natural compounds and antioxidant activity of essential oils from spice plants: New findings and potential applications. Biomolecules 2020, 10, 988. [Google Scholar] [CrossRef]
- Wang, W.; Wu, N.; Zu, Y.G.; Fu, Y.J. Antioxidative activity of Rosmarinus officinalis L. essential oil compared to its main components. Food Chem. 2008, 108, 1019–1022. [Google Scholar] [CrossRef] [PubMed]
- Ulanowska, M.; Olas, B. Biological Properties and prospects for the application of eugenol—A review. Int. J. Mol. Sci. 2021, 22, 3671. [Google Scholar] [CrossRef] [PubMed]
- Castañeda, C.B.; Ramos, Q.F.; Ibáñez, V.L. Evaluation of the antioxidant capacity of seven Peruvian medicinal plants. J. Med. Hor. 2008, 8, s56–s78. [Google Scholar]
- Yang, C.H.; Li, R.X.; Chuang, L.Y. Antioxidant activity of various parts of Cinnamomum cassia extracted with different extraction methods. Molecules 2012, 17, 7294–7304. [Google Scholar] [CrossRef] [Green Version]
- Alavi-Samani, S.M.; Kachouei, M.A.; Pirbalouti, A.G. Growth, yield, chemical composition, and antioxidant activity of essential oils from two thyme species under foliar application of jasmonic acid and water deficit conditions. Hortic. Environ. Biotechnol. 2015, 56, 411–420. [Google Scholar] [CrossRef]
- Okpala, E.O.; Onocha, P.A.; Ali, M.S. Antioxidant activity of phytol dominated stem bark and leaf essential oils of Celtis zenkeri Engl. Trends Phytochem. Res. 2022, 6, 137–144. [Google Scholar]
- Mancianti, F.; Ebani, V.V. Biological activity of essential oils. Molecules 2020, 25, 678. [Google Scholar] [CrossRef]
- Bassolé, I.H.N.; Juliani, H.R. Essential oils in combination and their antimicrobial properties. Molecules 2012, 17, 3989–4006. [Google Scholar] [CrossRef] [Green Version]
- Jeong, E.J.; Lee, N.K.; Oh, J.; Jang, S.E.; Lee, J.S.; Bae, I.H.; Jeong, Y.S. Inhibitory effect of cinnamon essential oils on selected cheese-contaminating fungi (Penicillium spp.) during the cheese-ripening process. Food Sci. Biotech. 2014, 23, 1193–1198. [Google Scholar] [CrossRef]
- El-Baroty, G.S.; Abd El-Baky, H.H.; Farag, R.S.; Saleh, M.A. Characterization of antioxidant and antimicrobial compounds of cinnamon and ginger essential oils. Afr. J. Biochem. Res. 2010, 4, 167–174. [Google Scholar]
- Ji, H.; Kim, H.; Beuchat, L.R.; Ryu, J.H. Synergistic antimicrobial activities of essential oil vapours against Penicillium corylophilum on a laboratory medium and beef jerky. Int. J. Food Microbiol. 2019, 291, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Guynot, M.E.; Ramos, A.J.; Seto, L.; Purroy, P.; Sanchis, V.; Marin, S. Antifungal activity of volatile compounds generated by essential oils against fungi commonly causing deterioration of bakery products. J. Appl. Microbiol. 2003, 94, 893–899. [Google Scholar] [PubMed]
- Shreaz, S.; Wani, W.A.; Behbehani, J.M.; Raja, V.; Irshad, M.; Karched, M.; Hun, L.T. Cinnamaldehyde and its derivatives, a novel class of antifungal agents. Fitoterapia 2016, 112, 116–131. [Google Scholar] [CrossRef] [PubMed]
- Liang, D.; Xing, F.; Selvaraj, J.N.; Liu, X.; Wang, L.; Hua, H.; Liu, Y. Inhibitory effect of cinnamaldehyde, citral, and eugenol on aflatoxin biosynthetic gene expression and aflatoxin B1 biosynthesis in Aspergillus flavus. J. Food Sci. 2015, 80, M2917–M2924. [Google Scholar] [CrossRef]
- Usta, J.; Kreydiyyeh, S.; Barnabe, P.; Bou-Moughlabay, Y.; Nakkash-Chmaisse, H. Comparative study on the effect of cinnamon and clove extracts and their main components on different types of ATPases. Hum. Exp. Toxicol. 2003, 22, 355–362. [Google Scholar]
- Wang, P.; Ma, L.; Jin, J.; Zheng, M.; Pan, L.; Zhao, Y.; Xing, F. The anti-aflatoxigenic mechanism of cinnamaldehyde in Aspergillus flavus. Sci. Rep. 2019, 9, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Xie, X.M.; Fang, J.R.; Xu, Y. Study of antifungal effect of cinnamaldehyde and citral on Aspergillus flavus. Food Sci. 2004, 25, 32–34. [Google Scholar]
- Abbaszadeh, S.; Sharifzadeh, A.; Shokri, H.; Khosravi, A.R.; Abbaszadeh, A. Antifungal efficacy of thymol, carvacrol, eugenol and menthol as alternative agents to control the growth of food-relevant fungi. J. Mycol. Med. 2014, 24, e51–e56. [Google Scholar] [CrossRef]
- Giovannini, P.P.; Catani, M.; Massi, A.; Sacchetti, G.; Tacchini, M.; de Oliveira, D.; Lerin, L.A. Continuous production of eugenol esters using enzymatic packed-bed microreactors and an evaluation of the products as antifungal agents. Flavour Fragr. J. 2019, 34, 201–210. [Google Scholar] [CrossRef]
- Pinto, S.M.L.; Rivera, Y.; Sandoval, L.V.H.; Lizarazo, J.C.; Rincón, J.J.; Méndez, L.Y.V. Semisynthetic eugenol derivatives as antifungal agents against dermatophytes of the genus Trichophyton. J. Med. Microbiol. 2019, 68, 1109–1117. [Google Scholar] [CrossRef]
- Chami, N.; Bennis, S.; Chami, F.; Aboussekhra, A.; Remmal, A. Study of anticandidal activity of carvacrol and eugenol in vitro and in vivo. Oral Microbiol. Immunol. 2005, 20, 106–111. [Google Scholar] [CrossRef] [PubMed]
- Gill, A.O.; Holley, R.A. Disruption of Escherichia coli, Listeria monocytogenes and Lactobacillus sakei cellular membranes by plant oil aromatics. Int. J. Food Microbiol. 2009, 108, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Weegels, P.L. The future of bread in view of its contribution to nutrient intake as a starchy staple food. Plant Foods Hum. Nut. 2019, 74, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Molina, F.; López-Acedo, E.; Tabla, R.; Roa, I.; Gómez, A.; Rebollo, J.E. Improved detection of Escherichia coli and coliform bacteria by multiplex PCR. BMC Biotechnol. 2015, 15, 48. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fisher, K.; Phillips, C.A. The effect of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J. Appl. Microb. 2006, 101, 1232–1240. [Google Scholar] [CrossRef] [PubMed]
- Munhuweyi, K.; Caleb, O.J.; Lennox, C.L.; van Reenen, A.J.; Opara, U.L. In Vitro and In Vivo antifungal activity of chitosan-essential oils against pomegranate fruit pathogens. Postharv. Biol. Technol. 2017, 129, 9–22. [Google Scholar] [CrossRef]
- Lucia, A.; Guzmán, E. Emulsions containing essential oils, their components or volatile semiochemicals as promising tools for insect pest and pathogen management. Adv. Colloid Interface Sci. 2021, 287, 102330. [Google Scholar] [CrossRef]
- Tyagi, A.K.; Malik, A. Antimicrobial potential and chemical composition of Eucalyptus globulus oil in liquid and vapour phase against food spoilage microorganisms. Food Chem. 2011, 126, 228–235. [Google Scholar] [CrossRef]
- Laird, K.; Phillips, C. Vapour phase: A potential future use for essential oils as antimicrobials? Lett. Appl. Microbiol. 2012, 54, 169–174. [Google Scholar] [CrossRef]
- Lorenzo-Leal, A.C.; Palou, E.; López-Malo, A. Evaluation of the efficiency of allspice, thyme and rosemary essential oils on two foodborne pathogens in in-vitro and on alfalfa seeds, and their effect on sensory characteristics of the sprouts. Int. J. Food Microbiol. 2019, 295, 19–24. [Google Scholar] [CrossRef]
- Valková, V.; Ďúranová, H.; Galovičová, L.; Vukovic, N.L.; Vukic, M.; Kačániová, M. In Vitro antimicrobial activity of lavender, mint, and rosemary essential oils and the effect of their vapours on growth of Penicillium spp. in a bread model system. Molecules 2021, 26, 3859. [Google Scholar] [CrossRef] [PubMed]
- Clemente, I.; Aznar, M.; Nerín, C. Synergistic properties of mustard and cinnamon essential oils for the inactivation of foodborne moulds in vitro and on Spanish bread. Int. J. Food Microbiol. 2019, 298, 44–50. [Google Scholar] [CrossRef] [PubMed]
No. | Compound a | Sample | RI e (calc.) | RI f (lit.) | ||
---|---|---|---|---|---|---|
EO1 b | EO2 c | EO3 d | ||||
% g | ||||||
1 | α-thujene | tr h | / j | tr | 926 | 930 |
2 | α-pinene | 0.6 | 0.8 | 1.8 | 938 | 939 |
3 | camphene | 0.1 | 0.2 | 0.2 | 948 | 954 |
4 | benzaldehyde | 0.9 | 0.2 | 0.2 | 958 | 960 |
5 | sabinene | tr | tr | 0.2 | 977 | 975 |
6 | β-pinene | 0.3 | 0.3 | 0.4 | 980 | 979 |
7 | β-myrcene | tr | 0.2 | 0.3 | 992 | 990 |
8 | α-phellandrene | / | 0.2 | 0.6 | 1004 | 1002 |
9 | δ-3-carene | / | / | tr | 1009 | 1011 |
10 | α-terpinene | / | 0.4 | 0.1 | 1016 | 1017 |
11 | p-cymene | 0.3 | / | / | 1023 | 1024 |
12 | o-cymene | / | 2.2 | 1.7 | 1026 | 1026 |
13 | α-limonene | 0.7 | 1.0 | 1.1 | 1028 | 1029 |
14 | 1,8-cineole | 2.3 | 2.9 | 3.0 | 1033 | 1031 |
15 | salicylic aldehyde | 0.4 | / | / | 1043 | 1044 |
16 | (E)-β-ocimene | / | / | tr | 1047 | 1050 |
17 | γ-terpinene | 0.2 | 0.3 | 0.3 | 1060 | 1059 |
18 | acetophenone | tr | / | / | 1063 | 1065 |
19 | α-terpinolene | tr | 0.1 | tr | 1088 | 1088 |
20 | linalool | / | 2.1 | 2.5 | 1098 | 1096 |
21 | α-thujone | tr | / | / | 1101 | 1102 |
22 | phenyl ethyl alcohol | 0.7 | / | / | 1110 | 1108 |
23 | camphor | 0.2 | tr | tr | 1148 | 1146 |
24 | benzyl acetate | / | tr | tr | 1160 | 1162 |
25 | iso-menthone | / | / | tr | 1162 | 1162 |
26 | benzenepropanal | 0.5 | / | / | 1165 | 1163 |
27 | borneol | tr | tr | / | 1170 | 1169 |
28 | 4-terpinenol | tr | 0.3 | 0.2 | 1178 | 1177 |
29 | p-cymen-8-ol | / | / | tr | 1183 | 1182 |
30 | α-terpineol | tr | 0.6 | 0.3 | 1189 | 1188 |
31 | methyl salicylate | tr | / | / | 1190 | 1191 |
32 | 2-allyl-phenol | / | / | tr | 1193 | 1191 |
33 | 2-methoxy-benzaldehyde | 0.5 | / | / | 1243 | 1245 |
34 | linalool acetate | tr | / | / | 1255 | 1257 |
35 | 2-phenyl ethyl acetate | tr | / | / | 1258 | 1258 |
36 | (E)-cinnamaldehyde | 77.1 | 44.1 | 1.7 | 1269 | 1270 |
37 | safrole | / | 1.1 | 1.1 | 1289 | 1287 |
38 | geranyl formate | / | 0.2 | / | 1299 | 1298 |
39 | carvacrol | / | 0.1 | tr | 1302 | 1299 |
40 | (E)-cinnamyl alcohol | tr | 0.4 | tr | 1303 | 1304 |
41 | α-cubebene | 0.4 | / | / | 1353 | 1351 |
42 | eugenol | / | 23.5 | 70.8 | 1360 | 1359 |
43 | α-ylangene | / | 0.9 | 0.6 | 1379 | 1373 |
44 | (Z)-caryophyllene | / | 0.2 | / | 1415 | 1408 |
45 | (E)-caryophyllene | tr | 3.9 | 3.5 | 1422 | 1419 |
46 | 1,2-benzopyrone | 2.2 | / | / | 1437 | 1434 |
47 | (E)-cinnamyl acetate | 3.0 | 3.0 | 1.5 | 1449 | 1446 |
48 | (E)-cinnamic acid | tr | / | / | 1452 | 1454 |
49 | α-humulene | / | 1.2 | / | 1456 | 1454 |
50 | allo-aromadendrene | tr | / | / | 1465 | 1460 |
51 | α-curcumene | tr | / | / | 1482 | 1480 |
52 | α-amorphene | tr | / | / | 1485 | 1484 |
53 | ledene | / | 0.2 | / | 1498 | 1496 |
54 | α-selinene | / | / | 0.6 | 1499 | 1498 |
55 | α-muurolene | tr | 0.2 | / | 1504 | 1500 |
56 | β-bisabolene | tr | / | / | 1507 | 1505 |
57 | eugenol acetate | / | 0.5 | 2.1 | 1519 | 1522 |
58 | δ-cadinene | / | 0.4 | tr | 1525 | 1523 |
59 | (E)-ο-methoxy cinnamaldehyde | 8.5 | 0.3 | / | 1529 | 1528 |
60 | caryophyllene oxide | / | 0.9 | 0.4 | 1583 | 1583 |
61 | tetradecanal | / | 0.1 | / | 1611 | 1612 |
62 | benzyl benzoate | / | 1.8 | 3.9 | 1755 | 1760 |
total | 98.9 | 94.8 | 99.1 |
Class of Compounds | EO1 a | EO2 b | EO3 c |
---|---|---|---|
% (Number of Compounds) | |||
nonterpenic compounds | |||
aldehydes | / d (0) | 0.1 (1) | /(0) |
aromatic compounds | 93.8 (14) | 50.9 (8) | 8.4 (8) |
subtotal | 93.8 (14) | 51.0 (9) | 8.4 (8) |
monoterpenes | |||
monoterpene hydrocarbons | 2.2 (10) | 5.7 (11) | 6.7 (14) |
summ | 2.2 (10) | 5.7 (11) | 6.7 (14) |
oxygenated monoterpenes | |||
monoterpene alcohols | tr (3) | 3.1 (5) | 3.0 (5) |
monoterpene aldehydes | /(0) | 0.2 (1) | /(0) |
monoterpene ketones | 0.2 (2) | tr (1) | tr (2) |
monoterpene esters | tr (1) | /(0) | /(0) |
monoterpene epoxides | 2.3 (1) | 2.9 (1) | 3.0 (1) |
summ | 2.5 (7) | 6.2 (8) | 6.0 (8) |
subtotal | 4.7 (17) | 11.9 (19) | 12.7 (22) |
phenylpropanoids | /(0) | 24.0 (2) | 72.9 (2) |
subtotal | /(0) | 24.0 (2) | 72.9 (2) |
sesquiterpenes | |||
sesquiterpene hydrocarbons | 0.4 (7) | 7.0 (7) | 4.7 (4) |
summ | 0.4 (7) | 7.0 (7) | 4.7 (4) |
oxygenated sesquiterpenes | |||
sesquiterpene epoxides | /(0) | 0.9 (1) | 0.4 (1) |
summ | /(0) | 0.9 (1) | 0.4 (1) |
subtotal | 0.4 | 7.9 (8) | 5.1 (5) |
total | 98.9 (38) | 94.8 (38) | 99.1 (37) |
EOS | AA (%) | AA (TEAC) |
---|---|---|
CCEO | 29.9 ± 0.6 a | 229.0 ± 3.0 a |
CVBEO | 82.4 ± 0.1 b | 480.0 ± 0.5 b |
CVLEO | 84.0 ± 0.3 c | 488.0 ± 1.2 c |
P. expansum | P. citrinum | P. crustosum | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Con. (µL/L) | 62.5 | 125 | 250 | 500 | 62.5 | 125 | 250 | 500 | 62.5 | 125 | 250 | 500 |
CCEO | 0.00 ± 0.00 aA | 0.67 ± 0.58 aB | 2.67 ± 1.15 aC | 6.67 ± 0.58 aD | 2.33 ± 0.58 aA | 5.67 ± 1.15 aB | 8.00 ± 1.00 aC | 10.67 ± 0.58 aD | 3.33 ± 0.58 aA | 6.67 ± 0.58 aB | 8.67 ± 0.58 aC | 14.67 ± 1.15 aD |
CVBEO | 0.00 ± 0.00 aA | 1.33 ± 0.58 aB | 4.67 ± 1.15 aC | 8.33 ± 0.58 aD | 1.67 ± 1.15 aA | 5.33 ± 0.58 aB | 5.67 ± 1.15 bB | 11.00 ± 1.73 abC | 3.33 ± 1.15 aA | 6.00 ± 1.73 aB | 9.00 ± 1.00 aC | 13.00 ± 1.73 aD |
CVLEO | 0.00 ± 0.00 aA | 0.00 ± 0.00 bA | 3.33 ± 1.15 aB | 8.00 ± 1.00 bC | 1.67 ± 0.58 aA | 6.33 ± 1.15 aB | 7.33 ± 0.58 abB | 12.33 ± 0.58 bC | 4.00 ± 1.73 aA | 5.67 ± 2.08 aA | 9.67 ± 1.53 aB | 14.33 ± 1.15 aC |
Isolated Microorganisms | 1st Day | 1st Week | 2nd Week | 3rd Week | 4th Week |
---|---|---|---|---|---|
Total count of microorganisms | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 2.71 ± 0.03 b | 2.87 ± 0.05 c | 3.04 ± 0.02 d |
Coliforms bacteria | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a |
Microscopic filamentous fungi | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 2.58 ± 0.04 b | 2.77 ± 0.03 c | 2.86 ± 0.04 d |
Isolated Species | 2nd Week | 3rd Week | 4th Week | Total |
---|---|---|---|---|
Bacillus amyloliquefaciens subsp. plantarum | 5 | 5 | ||
Bacillus cereus | 1 | 1 | ||
Bacillus pumilus | 2 | 1 | 3 | |
Bacillus subtilis | 3 | 1 | 4 | |
Micrococcus luteus | 1 | 1 | ||
Staphylococcus pasteuri | 7 | 1 | 5 | 13 |
Penicillium spp. | 4 | 5 | 5 | 14 |
Total | 12 | 16 | 13 | 41 |
Isolated Species | Genera | Family |
---|---|---|
Bacillus amyloliquefaciens subsp. plantarum | Bacillus | Bacillaceae |
Bacillus cereus | Bacillus | Bacillaceae |
Bacillus pumilus | Bacillus | Bacillaceae |
Bacillus subtilis | Bacillus | Bacillaceae |
Micrococcus luteus | Micrococcus | Micrococcaceae |
Staphylococcus pasteuri | Staphylococcus | Staphylococcaceae |
Penicillium spp. | Penicillium | Aspergillaceae |
Fungi Strains | MGI [%] | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
CCEO (µL/L) | CVBEO (µL/L) | CVLEO (µL/L) | ||||||||||
62.5 | 125 | 250 | 500 | 62.5 | 125 | 250 | 500 | 62.5 | 125 | 250 | 500 | |
P. crustosum | 11.90 ± 1.83 aA | 47.25 ± 8.96 bA | 72.32 ± 6.82 cA | 85.63 ± 4.19 dA | 60.13 ± 2.19 aB | 50.95 ± 3.12 bA | 74.13 ± 5.71 cA | 88.00 ± 9.29 cA | 14.74 ± 5.44 aA | 11.49 ± 2.37 aB | −41.60 ± 3.52 bB | 33.22 ± 9.14 cB |
P. citrinum | 49.14 ± 3.69 aA | 67.43 ± 9.72 bA | 85.01 ± 6.57 cA | 68.04 ± 2.32 bA | 33.27 ± 8.79 aB | 48.43 ± 10.59 acA | 95.23 ± 9.17 bA | 57.54 ± 5.41 cB | 23.01 ± 3.16 aB | 96.78 ± 8.54 bB | 71.21 ± 5.36 cB | 39.30 ± 5.79 dC |
P. expansum | 48.01 ± 7.51 aA | 82.71 ± 8.62 bA | 80.82 ± 9.56 bA | 69.72 ± 9.19 bA | −116.10 ± 10.75 aB | 60.97 ± 8.78 bB | 84.01 ± 6.96 cA | 60.67 ± 8.63 bdA | 5.78 ± 1.49 aC | 24.36 ± 6.89 bC | 26.86 ± 2.85 bB | 69.02 ± 7.31 cA |
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Valková, V.; Ďúranová, H.; Galovičová, L.; Vukovic, N.L.; Vukic, M.; Kowalczewski, P.Ł.; Kačániová, M. Application of Three Types of Cinnamon Essential Oils as Natural Antifungal Preservatives in Wheat Bread. Appl. Sci. 2022, 12, 10888. https://doi.org/10.3390/app122110888
Valková V, Ďúranová H, Galovičová L, Vukovic NL, Vukic M, Kowalczewski PŁ, Kačániová M. Application of Three Types of Cinnamon Essential Oils as Natural Antifungal Preservatives in Wheat Bread. Applied Sciences. 2022; 12(21):10888. https://doi.org/10.3390/app122110888
Chicago/Turabian StyleValková, Veronika, Hana Ďúranová, Lucia Galovičová, Nenad L. Vukovic, Milena Vukic, Przemysław Łukasz Kowalczewski, and Miroslava Kačániová. 2022. "Application of Three Types of Cinnamon Essential Oils as Natural Antifungal Preservatives in Wheat Bread" Applied Sciences 12, no. 21: 10888. https://doi.org/10.3390/app122110888
APA StyleValková, V., Ďúranová, H., Galovičová, L., Vukovic, N. L., Vukic, M., Kowalczewski, P. Ł., & Kačániová, M. (2022). Application of Three Types of Cinnamon Essential Oils as Natural Antifungal Preservatives in Wheat Bread. Applied Sciences, 12(21), 10888. https://doi.org/10.3390/app122110888