Abstract
Foodborne pathogens present in food and agricultural systems are recognized as a considerable burden for human health and socioeconomic development. Mānuka essential oil (MEO) exhibits antimicrobial, antiparasitic, photo-protective, and some medicinal effects. However, limitations associated with the use of MEO, such as volatility, instability in complex biological systems, and only being effective at high doses, have significantly affected its large-scale applications in the food and agricultural industry. In this study, we propose to use a rapid and non-thermal vacuum infusion method to facilitate the encapsulation of MEO in yeast microcarriers. The physicochemical properties of encapsulated MEO were characterized and the thermal stability and in vitro release profile of encapsulated MEO were evaluated. The confocal images demonstrated the success of MEO encapsulation. The thermal stability of MEO was significantly improved by approximately 43% due to the presence of yeast microcarriers. The results of the in vitro release assay illustrate the release kinetics of MEO from the microcarriers, demonstrating the controlled release of MEO provided by encapsulation. Spore-forming Bacillus cereus vegetative cells were selected as a model foodborne pathogen. The antimicrobial activity of the encapsulated MEO was tested on B. cereus vegetative cells with and without a high concentration of simulated soluble organic matter (COD = 1000 mg/L). The results suggest that the encapsulated MEO can inactivate 4-log CFU/mL of bacteria after 1-h treatment, regardless of the presence of soluble organic matter, while the non-encapsulated MEO at an equivalent concentration only achieved less than 1-log reduction in the presence of organic content. In summary, this study reveals the potential of using cell-based encapsulation for MEO as an antimicrobial system to treat B. cereus vegetative cells in an organic-rich aqueous environment.
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Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aguilar, C. N., Nevárez-Moorillón, G. V., Fuciños, P., Zekovic, Z. P., Ricci, A., Pellegrini, M., Sterzo, L. C., et al. (2020). Article 14 (2020) Salmonella Enterica control in stick carrots through incorporation of coriander seeds essential oil in sustainable washing treatments. Frontiers in Sustainable Food System, 4, 14. https://doi.org/10.3389/fsufs.2020.00014
Alves, D., Cerqueira, M. A., Pastrana, L. M., & Sillankorva, S. (2020). Entrapment of a phage cocktail and cinnamaldehyde on sodium alginate emulsion-based films to fight food contamination by Escherichia Coli and Salmonella Enteritidis. Food Research International, 128, 108791. https://doi.org/10.1016/j.foodres.2019.108791
Arnesen, S., Lotte, P., Fagerlund, A., & Granum, P. E. (2008). From soil to gut: Bacillus Cereus and its food poisoning toxins. FEMS Microbiology Reviews, 32(4), 579–606. https://doi.org/10.1111/j.1574-6976.2008.00112.x
Bishop, J. R., Nelson, G., Lamb, J. (1998). Microencapsulation in yeast cells. Journal of Microencapsulation. 15(6):761-73. https://doi.org/10.3109/02652049809008259
Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods - A review. International Journal of Food Microbiology, 94(3), 223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Chao, S. C., Gary Young, D., & Oberg, C. J. (2000). Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. Journal of Essential Oil Research, 12(5), 639–649. https://doi.org/10.1080/10412905.2000.9712177
Chang, H-T., Chun-Ya, L., Li-Sheng, H., Shang-Tzen, C. (2021). “Thermal Degradation of Linalool- Chemotype Cinnamomum Osmophloeum Leaf Essential Oil and Its Stabilization by Microencapsulation with β- Cyclodextrin.” Molecules 26 (2): 409. https://doi.org/10.3390/molecules26020409
Clavel, T., Carlin, F., Lairon, D., Nguyen-The, C., & Schmitt, P. (2004). Survival of Bacillus cereus spores and vegetative cells in acid media simulating human stomach. Journal of Applied Microbiology, 97, 214–219. https://doi.org/10.1111/j.1365-2672.2004.02292.x
Cossu, A., Ercan, D., Tikekar, R. V., et al. (2016). Antimicrobial effect of photosensitized rose bengal on bacteria and viruses in model wash water. Food and Bioprocess Technology, 9, 441–451. https://doi.org/10.1007/s11947-015-1631-8
Dorman, H. J. D., & Deans, S. G. (2000). Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88(2), 308–316. https://doi.org/10.1046/j.1365-2672.2000.00969.x
Dou, F., Huang, K., & Nitin, N. (2021). Targeted photodynamic treatment of bacterial biofilms using curcumin encapsulated in cells and cell wall particles. ACS Applied Bio Materials, 2021, 522. https://doi.org/10.1021/acsabm.0c01051
Espina, L., Condón, S., Pagán, R., & García-Gonzalo, D. (2014). Synergistic effect of orange essential oil or (+)-limonene with heat treatments to inactivate Escherichia Coli O157:H7 in orange juice at lower intensities while maintaining hedonic acceptability. Food and Bioprocess Technology, 7(2), 471–481. https://doi.org/10.1007/s11947-013-1076-x
Farag, N. F., Sherweit H. E-A., Enas, H., Abdelrahman, A. N., Hartwig, S., Shadia M. A., El Sayeda, A. E-K. (2018). “Characterization of Essential Oils from Myrtaceae Species Using ATR-IR Vibrational Spectroscopy Coupled to Chemometrics.” Industrial Crops and Products 124 (November): 870– 77. https://doi.org/10.1016/j.indcrop.2018.07.066
Griffiths, P. R., & De Haseth, J. A. (2007) Fourier transform infrared spectrometry (Vol. 171). John Wiley & Sons, page 324
Gutierrez, J., Barry-Ryan, C., Bourke, P. (2008). “The Antimicrobial Efficacy of Plant Essential Oil Combinations and Interactions with Food Ingredients.” International Journal of Food Microbiology 124 (1): 91–97. https://doi.org/10.1016/j.ijfoodmicro.2008.02.028
Huang, K., Dou, F., & Nitin, N. (2019). Biobased sanitizer delivery system for improved sanitation of bacterial and fungal biofilms. ACS Applied Materials and Interfaces, 11(19), 17204–17214. https://doi.org/10.1021/acsami.9b02428
Huang, K., & Nitin, N. (2020). Food-grade microscale dispersion enhances UV stability and antimicrobial activity of a model bacteriophage (T7) for reducing bacterial contamination (Escherichia Coli) on the plant surface. Journal of Agricultural and Food Chemistry, 68(39), 10920–10927. https://doi.org/10.1021/acs.jafc.0c02795
Hemmatkhah, F., Zeynali, F., & Almasi, H. (2020). Encapsulated cumin seed essential oil-loaded active papers: Characterization and evaluation of the effect on quality attributes of beef hamburger. Food and Bioprocess Technology, 13(3), 533–547. https://doi.org/10.1007/s11947-020-02418-9
Kavetsou, E., Koutsoukos, S., Daferera, D., Polissiou, M. G., Karagiannis, D., Perdikis, D. C., & Detsi, A. (2019). Encapsulation of Mentha pulegium essential oil in yeast cell microcarriers: An approach to environmentally friendly pesticides. Journal of Agricultural and Food Chemistry, 67(17), 4746–4753. https://doi.org/10.1021/acs.jafc.8b05149
Kujur, A., Kumar, A., Singh, P. P., & Prakash, B. (2021). Fabrication, characterization, and antifungal assessment of jasmine essential oil-loaded chitosan nanomatrix against aspergillus flavus in food system. Food and Bioprocess Technology, 14(3), 554–571. https://doi.org/10.1007/s11947-021-02592-4
Lin, P. C., Lin, S., Wang, P. C., & Sridhar, R. (2014). Techniques for physicochemical characterization of nanomaterials. Biotechnology Advances, 32(4), 711–726. https://doi.org/10.1016/j.biotechadv.2013.11.006
Lee, C. H., Woo, H. J., Kang, J. H., & Song, K. B. (2021). Electrostatic Spraying of Passion Fruit (Passiflora Edulis L.) Peel extract for inactivation of Escherichia Coli O157:H7 and Listeria monocytogenes on fresh-cut lollo rossa and beetroot leaves. Food and Bioprocess Technology, 14 (5): 898–908. https://doi.org/10.1007/s11947-021-02608-z
Lim, J. S., & Ha, J. W. (2021). Growth-inhibitory effect of X-ray irradiation on gram-negative and gram-positive pathogens in apple, orange, and tomato juices. Food and Bioprocess Technology, 1, 1–11. https://doi.org/10.1007/s11947-021-02686-z
Mathew, C., Tesfaye, W., Rasmussen, P., Peterson, G. M., Bartholomaeus, A., Sharma, M., & Thomas, J. (2020). Mānuka oil—a review of antimicrobial and other medicinal properties. Pharmaceuticals, 13(11), 343. https://doi.org/10.3390/ph13110343
Meneses, R., Ocazionez, R. E., Martínez, J. R., & Stashenko, E. E. (2009). Inhibitory effect of essential oils obtained from plants grown in colombia on yellow fever virus replication in vitro. Annals of Clinical Microbiology and Antimicrobials, 8(March), 8–8. https://doi.org/10.1186/1476-0711-8-8
Moghadam, N., Maryam, A. J., Bazzaz, B. B. S. F., Azizzadeh, M., & Movaffagh, J. (2020a). Saccharomyces Cerevisiae as a delivery system of Zataria multiflora Boiss. Essential Oil as a Natural Preservative for Food applications: Encapsulation of Iranian Zataria multiflora Boiss. Essential Oil. Journal of the Science of Food and Agriculture, 101, 2006–2013. https://doi.org/10.1002/jsfa.10818
Nakhaee Moghadam, M., Movaffagh, J., Fazli Bazzaz, B. S., Azizzadeh, M., & Jamshidi, A. (2020). Encapsulation of Zataria multiflora essential oil in Saccharomyces Cerevisiae: Sensory evaluation and antibacterial activity in commercial soup. Iranian Journal of Chemistry and Chemical Engineering, 39 (2): 233–42. https://doi.org/10.30492/IJCCE.2020.34020
Nakhaee, M., Maryam, A. J., Bi Bi, S. F. B., Mohammad, A., Jebrail, M. (2020). “Saccharomyces Cerevisiae as a Delivery System of Zataria Multiflora Boiss. Essential Oil as a Natural Preservative for Food Applications: Encapsulation of Iranian Zataria Multiflora Boiss. Essential Oil.” Journal of the Science of Food and Agriculture, no. August. https://doi.org/10.1002/jsfa.10818
Ngamakeue, N., & Chitprasert, P. (2016). Encapsulation of holy basil essential oil in gelatin: Effects of palmitic acid in carboxymethyl cellulose emulsion coating on antioxidant and antimicrobial activities. Food and Bioprocess Technology, 2016 9:10 9 (10): 1735–45. https://doi.org/10.1007/S11947-016-1756-4
Perdana, M. I., Ruamcharoen, J., Panphon, S., & Leelakriangsak, M. (2021). Antimicrobial activity and physical properties of starch/chitosan film incorporated with lemongrass essential oil and its application. LWT, 141, 110934. https://doi.org/10.1016/j.lwt.2021.110934
Prosser, J. A., Woods, R. R., Horswell, J., & Robinson, B. H. (2016). The potential in-situ antimicrobial ability of Myrtaceae plant species on pathogens in soil. Soil Biology and Biochemistry, 96, 1–3. https://doi.org/10.1016/j.soilbio.2015.12.007
Park, J. B., Kang, J. H., & Song, K. B. (2018). Geranium essential oil emulsion containing benzalkonium chloride as a wash solution on fresh-cut vegetables. Food and Bioprocess Technology, 11(12), 2164–2171. https://doi.org/10.1007/s11947-018-2177-3
Park, C. G., Miyeon, J., Eunsik, S., Junheon, K. (2017). “Myrtaceae Plant Essential Oils and Their β-Triketone Components as Insecticides against Drosophila Suzukii.” Molecules 22 (7). https://doi.org/10.3390/molecules22071050
Rather, I. A., Koh, W. Y., Paek, W. K., & Lim, J. (2017). The sources of chemical contaminants in food and their health implications. Frontiers in Pharmacology, 8, 830. https://doi.org/10.3389/fphar.2017.00830
Rai, R., Caroline, M., Wallace, Y., Nitin, N. (2021). “Infusion of Trans-Resveratrol in Micron-Scale Grape Skin Powder for Enhanced Stability and Bioaccessibility.” Food Chemistry 340 (March): 127894. https://doi.org/10.1016/j.foodchem.2020.127894
Romdhane, S., Devers-Lamrani, M., Martin-Laurent, F., Jrad, A. B., Raviglione, D., Salvia, M. V., & Barthelmebs, L. (2018). Evidence for photolytic and microbial degradation processes in the dissipation of leptospermone, a natural β-triketone herbicide. Environmental Science and Pollution Research, 25(30), 29848–29859.
Serio, A., Abdulhameed, S., Jiménez-Munguía, M. T., Salgado-Nava, A. A., Hernández-Nava, R., & López-Malo, A. (2020). Antimicrobial Activity of encapsulated Mexican oregano (Lippia Berlandieri Schauer) essential oil applied on bagels. Frontiers in Sustainable Food Systems, 4, 537091. https://doi.org/10.3389/fsufs.2020.537091
Smith, A. E., Zhang, Z., Thomas, C. R. (2000). Wall material properties of yeast cells: Part 1. Cell measurements and compression experiments. Chemical Engineering Science, 55(11): 2031–2041. https://doi.org/10.1016/S0009-2509(99)00500-X
Souza, A. C., Goto, G. E. O., Mainardi, J. A., Coelho, A. C. V., & Tadini, C. C. (2013). Cassava starch composite films incorporated with cinnamon essential oil: Antimicrobial activity, microstructure, mechanical and barrier properties. LWT - Food Science and Technology, 54(2), 346–352. https://doi.org/10.1016/j.lwt.2013.06.017
Stephens, J. M. C., Molan, P. C., & Clarkson, B. D. (2005). A review of Leptospermum Scoparium (Myrtaceae) in New Zealand. New Zealand Journal of Botany, 48(1), 53–68. https://doi.org/10.1080/0028825X.2005.9512966
St Angelo, A. J., John, V., Tom, J., Michael, L. (1996). “Lipid Oxidation in Foods.” Critical Reviews in Food Science and Nutrition 36 (3): 175–224. https://doi.org/10.1080/10408399609527723
Souza, H. J., & Barboza de, Regiane Victória de Barros Fernandes, Soraia Vilela Borges, Pedro Henrique Campelo Felix, Lívia Cássia Viana, Amanda Maria Teixeira Lago, and Diego Alvarenga Botrel. (2018). Utility of blended polymeric formulations containing cellulose nanofibrils for encapsulation and controlled release of sweet orange essential oil. Food and Bioprocess Technology, 11(6), 1188–1198. https://doi.org/10.1007/s11947-018-2082-9
Taha, M., Hassan, M., Essa, S., & Tartor, Y. (2013). Use of Fourier transform infrared spectroscopy (FTIR) spectroscopy for rapid and accurate identification of yeasts isolated from human and animals. International Journal of Veterinary Science and Medicine, 1(1), 15–20. https://doi.org/10.1016/j.ijvsm.2013.03.001
Tao, M., Juhong, C., Kang, H. (2021). “Bio-Based Antimicrobial Delivery Systems for Improving Microbial Safety and Quality of Raw or Minimally Processed Foods.” Current Opinion in Food Science. Elsevier Ltd. https://doi.org/10.1016/j.cofs.2021.04.011
Van Vuuren, S. F., Docrat, Y., Kamatou, G. P. P., & Viljoen, A. M. (2014). Essential oil composition and antimicrobial interactions of understudied tea tree species. South African Journal of Botany, 92, 7–14. https://doi.org/10.1016/j.sajb.2014.01.005
Velasco, J., Carmen, D. (2002). “2 External Variables Influencing the Oxidative Stability of Olive Oils.” European Journal of Lipid Science 104: 661–76
Workman, M. J., Bruno Gomes, Ju., Weng, L., Ista, L. K., Jesus, C. P., David, M. R., Ramalho-Ortigao, M., et al. (2020). Yeast-encapsulated essential oils: A new perspective as an environmentally friendly Larvicide. Parasites and Vectors, 13(1), 19. https://doi.org/10.1186/s13071-019-3870-4
World Health Organization. Food Safety. (2020). https://www.who.int/news-room/fact-sheets/detail/food-safety [Accessed February 15, 2021]
Young, S., Dea, S., & Nitin, N. (2017). Vacuum facilitated infusion of bioactives into yeast microcarriers: Evaluation of a novel encapsulation approach. Food Research International, 100, 100–112. https://doi.org/10.1016/j.foodres.2017.07.067
Young, S., Nitin, N. (2019). “Thermal and Oxidative Stability of Curcumin Encapsulated in Yeast Microcarriers.” Food Chemistry 275 (March): 1–7. https://doi.org/10.1016/J.FOODCHEM.2018.08.121
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This research was supported by K. Huang’s start-up funds and FRDF grants (3720331 and 3722390) at the University of Auckland.
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Shanshan Liu: methodology, data collection and analysis, visualization, writing—original draft. Meihan Tao: data collection and analysis, writing—review and editing. Kang Huang: conceptualization, data collection and analysis, writing—review and editing, supervision.
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Liu, S., Tao, M. & Huang, K. Encapsulation of Mānuka Essential Oil in Yeast Microcarriers for Enhanced Thermal Stability and Antimicrobial activity. Food Bioprocess Technol 14, 2195–2206 (2021). https://doi.org/10.1007/s11947-021-02714-y
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DOI: https://doi.org/10.1007/s11947-021-02714-y