Multivariate Optimization for the Production of OSA-Starch Microcapsules Containing Clove and White Thyme Essential Oils: Antifungal Potential Against Penicillium digitatum
Corresponding Author
Estefania Júlia Dierings de Souza
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Correspondence:
Estefania Júlia Dierings de Souza ([email protected])
Search for more papers by this authorFelipe Nardo dos Santos
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorDianini Hüttner Kringel
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorJaqueline Ferreira de Souza
Laboratory of Technology and Development of Composites and Polymeric Materials (LaCoPol), Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorDanielle Tapia Bueno
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAmanda Fonseca Leitzke
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAndré Ricardo Fajardo
Laboratory of Technology and Development of Composites and Polymeric Materials (LaCoPol), Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorEliezer Avila Gandra
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Center of Chemical, Pharmaceutical and Food Sciences, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorClaudio Martin Pereira de Pereira
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAlvaro Renato Guerra Dias
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorElessandra da Rosa Zavareze
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorCorresponding Author
Estefania Júlia Dierings de Souza
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Correspondence:
Estefania Júlia Dierings de Souza ([email protected])
Search for more papers by this authorFelipe Nardo dos Santos
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorDianini Hüttner Kringel
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorJaqueline Ferreira de Souza
Laboratory of Technology and Development of Composites and Polymeric Materials (LaCoPol), Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorDanielle Tapia Bueno
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAmanda Fonseca Leitzke
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAndré Ricardo Fajardo
Laboratory of Technology and Development of Composites and Polymeric Materials (LaCoPol), Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorEliezer Avila Gandra
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Center of Chemical, Pharmaceutical and Food Sciences, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorClaudio Martin Pereira de Pereira
Center of Chemical, Pharmaceutical and Food Sciences, Innovation and Solutions in Chemistry Laboratory, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorAlvaro Renato Guerra Dias
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorElessandra da Rosa Zavareze
Department of Agroindustrial Science and Technology, Federal University of Pelotas, Pelotas, RS, Brazil
Search for more papers by this authorFunding: This work was supported by Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul, 17/255100009126. Conselho Nacional de Desenvolvimento Científico e Tecnológico, 306378/2015-9. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, 001.
ABSTRACT
The objective of this study was to optimize the conditions for the production of microcapsules based on OSA-starch and clove (CEO) and white thyme (WTEO) essential oils (EOs) obtained by electrospraying. The antifungal activity against the fungus Penicillium digitatum was assessed using both the well diffusion method and volatile release action. The microcapsules were characterized by morphology, loading capacity (LC) presence of functional groups (FTIR), and thermal properties (TGA). Spherical microcapsules were formed in all treatments evaluated, with an average diameter ranging from 0.803 to 1.500 μm. The morphology of the materials was not affected by the variation of the solution parameters (ethanol: 20% and 30%, OSA-starch: 40% and 50%, CEO and WTEO, and EO concentration: 0.2% and 0.4%). The LC ranged from 30.6% to 97.9%, and TGA and FTIR analyses for all treatments confirmed the interaction of EOs with OSA-starch. Microcapsules from OSA-starch with CEO showed greater efficiency in reducing the mycelial growth of P. digitatum through the release of volatiles. These results serve as a basis for future studies to evaluate the technological applicability of these capsules in a food matrix or packaging material for controlling the fungal growth of P. digitatum.
Conflicts of Interest
The authors declare no conflicts of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
- 1M. H. Aminifard and H. Bayat, “Antifungal Activity of Black Caraway and Anise Essential Oils Against Penicillium Digitatum on Blood Orange Fruits,” International Journal of Fruit Science 18 (2018): 307–319, https://doi.org/10.1080/15538362.2017.1409682.
10.1080/15538362.2017.1409682 Google Scholar
- 2M. V. Alvarez, M. B. Pérez-Gago, V. Taberner, L. Settier-Ramírez, V. Martínez-Blay, and L. Palou, “Postharvest Application of Novel Bio-Based Antifungal Composite Edible Coatings to Reduce Sour Rot and Quality Losses of ‘Valencia’ Oranges,” Coatings 13 (2023): 1412, https://doi.org/10.3390/coatings13081412.
- 3R. M. Sumalan, R. Kuganov, D. Obistioiu, et al., “Assessment of Mint, Basil, and Lavender Essential Oil Vapor-Phase in Antifungal Protection and Lemon Fruit Quality,” Molecules 25 (2020): 1831, https://doi.org/10.3390/molecules25081831.
- 4F. Chidi, A. Bouhoudan, and M. Khaddor, “Antifungal Effect of the Tea Tree Essential Oil (Melaleuca Alternifolia) Against Penicillium Griseofulvum and Penicillium Verrucosum,” Journal of King Saud University, Science 32 (2020): 2041–2045, https://doi.org/10.1016/j.jksus.2020.02.012.
10.1016/j.jksus.2020.02.012 Google Scholar
- 5J. Wang, F. Zhao, J. Huang, Q. Li, Q. Yang, and J. Ju, “Application of Essential Oils as Slow-Release Antimicrobial Agents in Food Preservation: Preparation Strategies, Release Mechanisms and Application Cases,” Critical Reviews in Food Science and Nutrition 64 (2023): 6272–6297, https://doi.org/10.1080/10408398.2023.2167066.
- 6H. Wu, F. Zhao, Q. Li, J. Huang, and J. Ju, “Antifungal Mechanism of Essential Oil Against Foodborne Fungi and Its Application in the Preservation of Baked Food,” Critical Reviews in Food Science and Nutrition 64 (2022): 2695–2707, https://doi.org/10.1080/10408398.2022.2124950.
- 7A. Rehman, S. M. Jafari, R. M. Aadil, E. Assadpour, M. A. Randhawa, and S. Mahmood, “Development of Active Food Packaging via Incorporation of Biopolymeric Nanocarriers Containing Essential Oils,” Trends in Food Science and Technology 101 (2020): 106–121, https://doi.org/10.1016/j.tifs.2020.05.001.
- 8N. F. Zainal Abiddin, A. Yusoff, and N. Ahmad, “Effect of Octenylsuccinylation on Physicochemical, Thermal, Morphological and Stability of Octenyl Succinic Anhydride (OSA) Modified Sago Starch,” Food Hydrocolloids 75 (2018): 138–146, https://doi.org/10.1016/j.foodhyd.2017.09.003.
- 9L. Altuna, M. L. Herrera, and M. L. Foresti, “Synthesis and Characterization of Octenyl Succinic Anhydride Modified Starches for Food Applications,” A Review of Recent Literature, Food Hydrocoll 80 (2018): 97–110, https://doi.org/10.1016/j.foodhyd.2018.01.032.
- 10S. Ataei, P. Azari, A. Hassan, B. Pingguan-Murphy, R. Yahya, and F. Muhamad, “Essential Oils-Loaded Electrospun Biopolymers: A Future Perspective for Active Food Packaging,” Advances in Polymer Technology 2020 (2020): 1–21, https://doi.org/10.1155/2020/9040535.
- 11E. J. D. de Souza, D. H. Kringel, A. R. G. Dias, and E. R. da Zavareze, “Polysaccharides as Wall Material for the Encapsulation of Essential Oils by Electrospun Technique,” Carbohydrate Polymers 265 (2021): 118068, https://doi.org/10.1016/j.carbpol.2021.118068.
- 12L. M. Fonseca, M. Radünz, H. C. dos Santos Hackbart, et al., “Electrospun Potato Starch Nanofibers for Thyme Essential Oil Encapsulation: Antioxidant Activity and Thermal Resistance,” Journal of the Science of Food and Agriculture 100 (2020): 4263–4271, https://doi.org/10.1002/jsfa.10468.
- 13M. T. Yilmaz, A. Yilmaz, P. K. Akman, et al., “Electrospraying Method for Fabrication of Essential Oil Loaded-Chitosan Nanoparticle Delivery Systems Characterized by Molecular, Thermal, Morphological and Antifungal Properties,” Innovative Food Science and Emerging Technologies 52 (2019): 166–178, https://doi.org/10.1016/j.ifset.2018.12.005.
- 14E. P. da Cruz, J. B. Pires, F. N. dos Santos, et al., “Encapsulation of Lemongrass Essential Oil Into Cassava Starch Fibers for Application as Antifungal Agents in Bread,” Food Hydrocolloids 145 (2023): 109105, https://doi.org/10.1016/j.foodhyd.2023.109105.
- 15J. B. Pires, F. N. dos Santos, E. P. da Cruz, et al., “Starch Extraction From Avocado By-Product and Its Use for Encapsulation of Ginger Essential Oil by Electrospinning,” International Journal of Biological Macromolecules 254 (2024): 127617, https://doi.org/10.1016/j.ijbiomac.2023.127617.
- 16B. Biduski, D. H. Kringel, R. Colussi, et al., “Electrosprayed Octenyl Succinic Anhydride Starch Capsules for Rosemary Essential Oil Encapsulation,” International Journal of Biological Macromolecules 132 (2019): 300–307, https://doi.org/10.1016/j.ijbiomac.2019.03.203.
- 17N. Angel, L. Guo, F. Yan, H. Wang, and L. Kong, “Effect of Processing Parameters on the Electrospinning of Cellulose Acetate Studied by Response Surface Methodology,” Journal of Agriculture and Food Research 2 (2020): 100015, https://doi.org/10.1016/j.jafr.2019.100015.
- 18E. J. D. de Souza, F. N. dos Santos, J. B. Pires, et al., “Production and Optimization of Ultrafine Fiber From Yam Starch by Electrospinning Method Using Multivariate Analysis,” Starch 73 (2021): 2000174, https://doi.org/10.1002/star.202000174.
- 19E. J. D. de Souza, D. H. Kringel, I. H. de Lima Costa, et al., “Antifungal Potential of Essential Oils From Different Botanical Sources Against Penicillium Digitatum: Chemical Composition and Antifungal Mechanisms of Action by Direct Contact and Volatile,” Natural Product Research (2024): 1–9, https://doi.org/10.1080/14786419.2024.2405865.
- 20E. J. D. de Souza, D. H. Kringel, T. J. Siebeneichler, et al., “Antifungal Potential of Clove and White Thyme Essential Oils Encapsulated in Electrosprayed Starch-OSA Against Penicillium Digitatum,” European Polymer Journal 215 (2024): 113192, https://doi.org/10.1016/j.eurpolymj.2024.113192.
- 21R. Karami-Osboo, M. Mahboubifar, M. Mirabolfathy, L. Hosseinian, and A. R. Jassbi, “Encapsulated Zataria multiflora's Essential Oil Inhibited the Growth of Aspergillus Flavus and Reduced Aflatoxins Levels in Contaminated Pistachio Nut,” Biocatalysis and Agricultural Biotechnology 51 (2023): 102796, https://doi.org/10.1016/j.bcab.2023.102796.
- 22L. M. Fonseca, M. Radünz, R. L. Crizel, T. M. Camargo, E. A. Gandra, and A. R. G. Dias, “Effect of Carvacrol Encapsulation in Starch-Based Nanofibers: Thermal Resistance and Antioxidant and Antimicrobial Properties,” Journal of Food Processing & Preservation 45 (2021): e15409, https://doi.org/10.1111/jfpp.15409.
- 23F. N. dos Santos, E. J. D. de Souza, J. F. de Souza, et al., “Encapsulation of Anthocyanic Extract of Jambolan (Syzygium cumini (L.)) in Zein Sub-Micron Fibers Produced by Electrospinning,” Food Biophysics 18 (2023): 133–147, https://doi.org/10.1007/s11483-022-09758-3.
10.1007/s11483-022-09758-3 Google Scholar
- 24N. Tao, L. Jia, and H. Zhou, “Anti-Fungal Activity of Citrus reticulata Blanco Essential Oil Against Penicillium Italicum and Penicillium Digitatum,” Food Chemistry 153 (2014): 265–271, https://doi.org/10.1016/j.foodchem.2013.12.070.
- 25C. Y. Chen, J. P. Zheng, C. P. Wan, M. Chen, and J. Y. Chen, “Effect of Carboxymethyl Cellulose Coating Enriched With Clove Oil on Postharvest Quality of “Xinyu” Mandarin Oranges,” Fruits 71 (2016): 319–327, https://doi.org/10.1051/fruits/2016019.
- 26M. Hashemi, A. Ehsani, A. Afshari, M. Aminzare, and M. Raeisi, “Chemical Composition and Antifungal Effect of Echinophora Platyloba Essential Oil Against Aspergillus Flavus, Penicillium Expansum and Fusarium Graminearum,” Journal of Chemical Health Risks 6 (2016): 91–97.
- 27D. H. Kringel, W. M. F. da Silva, B. Biduski, et al., “Free and Encapsulated Orange Essential Oil Into a β-Cyclodextrin Inclusion Complex and Zein to Delay Fungal Spoilage in Cakes,” Journal of Food Processing & Preservation 44 (2020): e14411, https://doi.org/10.1111/jfpp.14411.
- 28L. Vargas-Campos, J. D. de Figueroa-Cárdenas, D. Tochihuitl-Vázquez, R. Ramírez-Bon, J. M. Yáñez-Limón, and J. F. Pérez-Robles, “Study of the Dextrose Equivalent of Maltodextrins in Electrospinning Using an Ethanol/Water Mixture as the Electrospinning Solvent,” Food Hydrocolloids 139 (2023): 108498, https://doi.org/10.1016/j.foodhyd.2023.108498.
- 29S. Wang, J. Ju, S. Wu, et al., “Electrospinning of Biocompatible Alginate-Based Nanofiber Membranes via Tailoring Chain Flexibility,” Carbohydrate Polymers 230 (2020): 115665, https://doi.org/10.1016/j.carbpol.2019.115665.
- 30B. Vafania, M. Fathi, and S. Soleimanian-Zad, “Nanoencapsulation of Thyme Essential Oil in Chitosan-Gelatin Nanofibers by Nozzle-Less Electrospinning and Their Application to Reduce Nitrite in Sausages,” Food and Bioproducts Processing 116 (2019): 240–248, https://doi.org/10.1016/j.fbp.2019.06.001.
- 31Z. Xiao, Y. Kang, W. Hou, Y. Niu, and X. Kou, “Microcapsules Based on Octenyl Succinic Anhydride (OSA)-modified Starch and Maltodextrins Changing the Composition and Release Property of Rose Essential Oil,” International Journal of Biological Macromolecules 137 (2019): 132–138, https://doi.org/10.1016/j.ijbiomac.2019.06.178.
- 32İ. Tarhan, M. R. Bakır, O. Kalkan, M. Yöntem, and H. Kara, “Rapid Determination of Adulteration of Clove Essential Oil With Benzyl Alcohol and Ethyl Acetate: Towards Quality Control Analysis by FTIR With Chemometrics,” Vibrational Spectroscopy 118 (2022): 103339, https://doi.org/10.1016/j.vibspec.2022.103339.
- 33P. Parthipan, M. S. AlSalhi, S. Devanesan, and A. Rajasekar, “Evaluation of Syzygium aromaticum Aqueous Extract as an Eco-Friendly Inhibitor for Microbiologically Influenced Corrosion of Carbon Steel in Oil Reservoir Environment,” Bioprocess and Biosystems Engineering 44 (2021): 1441–1452, https://doi.org/10.1007/s00449-021-02524-8.
- 34X. Yin, Q. Hu, X. Chen, et al., “Inclusion Complexes of Clove Essential Oil With Sodium Caseinate and Gum Arabic Prepared by High-Pressure Homogenization: Characterization and Non-contact Antimicrobial Activity,” Food Control 150 (2023): 109765, https://doi.org/10.1016/j.foodcont.2023.109765.
- 35H. Gao, H. Yang, and C. Wang, “Controllable Preparation and Mechanism of Nano-Silver Mediated by the Microemulsion System of the Clove Oil,” Results in Physics 7 (2017): 3130–3136, https://doi.org/10.1016/j.rinp.2017.08.032.
10.1016/j.rinp.2017.08.032 Google Scholar
- 36J. Rojas, S. Cabrera, J. Benavides, Y. Lopera, and C. J. Yarce, “Lipidic Matrixes Containing Clove Essential Oil: Biological Activity, Microstructural and Textural Studies,” Molecules 26 (2021): 2425, https://doi.org/10.3390/molecules26092425.
- 37M. Volić, I. Pećinar, D. Micić, et al., “Design and Characterization of Whey Protein Nanocarriers for Thyme Essential Oil Encapsulation Obtained by Freeze-Drying,” Food Chemistry 386 (2022): 132749, https://doi.org/10.1016/j.foodchem.2022.132749.
- 38P. Sharma, A. Ahuja, A. M. Dilsad Izrayeel, P. Samyn, and V. K. Rastogi, “Physicochemical and Thermal Characterization of Poly (3-Hydroxybutyrate-Co-4-Hydroxybutyrate) Films Incorporating Thyme Essential Oil for Active Packaging of White Bread,” Food Control 133 (2022): 108688, https://doi.org/10.1016/j.foodcont.2021.108688.
- 39Z. Du, H. Lv, C. Wang, et al., “Organic Solvent-Free Starch-Based Green Electrospun Nanofiber Mats for Curcumin Encapsulation and Delivery,” International Journal of Biological Macromolecules 232 (2023): 123497, https://doi.org/10.1016/j.ijbiomac.2023.123497.
- 40X. Li, X. Wang, H. Zhang, L. Gong, X. Meng, and B. Liu, “OSA-Starch Stabilized EPA Nanoliposomes: Preparation, Characterization, Stability and Digestion In Vitro and In Vivo,” Food Chemistry 419 (2023): 136040, https://doi.org/10.1016/j.foodchem.2023.136040.
- 41W. Wang, C. Liu, H. Zhang, et al., “Properties of OSA-Modified Starch and Emulsion Prepared With Different Materials: Glutinous Rice Starch, Japonica Rice Starch, and Indica Rice Starch,” Food Research International 161 (2022): 111845, https://doi.org/10.1016/j.foodres.2022.111845.
- 42H. Cetin Babaoglu, A. Bayrak, N. Ozdemir, and N. Ozgun, “Encapsulation of Clove Essential Oil in Hydroxypropyl Beta-Cyclodextrin for Characterization, Controlled Release, and Antioxidant Activity,” Journal of Food Processing & Preservation 41 (2017): e13202, https://doi.org/10.1111/jfpp.13202.
- 43M. M. Volić, N. S. Obradović, V. B. Djordjević, N. D. Luković, Z. D. Knežević-Jugović, and B. M. Bugarski, “Design of Biopolymer Carriers Enriched With Natural Emulsifiers for Improved Controlled Release of Thyme Essential Oil,” Journal of Food Science 85 (2020): 3833–3842, https://doi.org/10.1111/1750-3841.15499.
- 44A. Amoozegaran, H. Dehghan, S. S. Homami, and S. A. Hashemi, “Efficacy of an Edible Coating, Containing Thyme Essential Oil, to Control Fusarium Oxysporum and the Quality of Tomato Fruits,” Journal of Food Measurement and Characterization 16 (2022): 3760–3767, https://doi.org/10.1007/s11694-022-01424-z.
10.1007/s11694-022-01424-z Google Scholar
- 45P. Fincheira, I. Jofré, J. Espinoza, et al., “The Efficient Activity of Plant Essential Oils for Inhibiting Botrytis Cinerea and Penicillium Expansum: Mechanistic Insights Into Antifungal Activity,” Microbiological Research 277 (2023): 127486, https://doi.org/10.1016/j.micres.2023.127486.
- 46T. Hou, S. S. Sana, H. Li, et al., “Essential Oils and Its Antibacterial, Antifungal and Anti-Oxidant Activity Applications: A Review,” Food Bioscience 47 (2022): 101716, https://doi.org/10.1016/j.fbio.2022.101716.
- 47H. Lv, S. Huo, L. Zhao, et al., “Preparation and Application of Cinnamon-Litsea cubeba Compound Essential Oil Microcapsules for Peanut Kernel Postharvest Storage,” Food Chemistry 415 (2023): 135734, https://doi.org/10.1016/j.foodchem.2023.135734.