Abstract
This study was performed to determine the antifungal activity of plant oil extracts (1% of lemongrass and oregano, 1:1) in combination with organic citrus fruit extract (BIOSECUR F440D®) with a ratio of 1:3 (W/W) against pathogenic molds (Aspergillus niger, Penicillium chrysogenum) and yeast (Saccharomyces cerevisiae). Synthetic commercial preservatives such as sodium benzoate (E211) and potassium sorbate (E202) were used as references. Antifungal formulation-loaded microemulsion was prepared by microfluidization for in situ analysis in orange juice. Antifungal formulation-loaded microemulsion (AFF-MM) led to a total inhibition of targeted fungi during the first days of storage and their populations stayed below detection limit until the end of storage (35 days). AFF-MM presented a higher antifungal activity compared to synthetic preservatives even at a concentration of 10 times lower than optimized concentration. Indeed, microemulsion increased the bioactivity and bioavailability of plant oil/citrus extracts compared to coarse emulsion by increasing the surface area of droplets induced by size decrement. Finally, the sensory analysis showed the panelists acceptance of orange juice in presence of antifungal-loaded microemulsion.
Similar content being viewed by others
References
Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV (1999) Food-related illness and death in the United States. Emerg Infect Dis 5(5):607–625
Mahale DP, Khade RG, Vaidya VK (2008) Microbiological analysis of street vended fruit juices from Mumbai city, India. Internet J Food Saf 10(9):31–34
Nicolas B, Razack BA, Yollande I, Aly S, Tidiane OCA, Philippe NA, De Souza C, Sababénédjo TA (2007) Street-vended foods improvement: contamination mechanisms and application of food safety objective strategy: critical review. Pak J Nutr 6(1):1–10
FAO (1992) Fruit juices and related products. Codex Alimentarius, Rome
Essien E, Monago C, Edor E (2011) Evaluation of the nutritional and microbiological quality of kunun (a cereal based non-alcoholic beverage) in rivers State, Nigeria. Internet J Nutr Wellness 10(2):1–10
Pawar V, Thaker V (2006) In vitro efficacy of 75 essential oils against Aspergillus niger. Mycoses 49(4):316–323
Pitt J (2000) Toxigenic fungi: which are important? Med Mycol 38:17–22
Foster T, Vasavada CP (2003) Beverage quality and safety, Microbiology of fruit juice and beverages. CRC Press, Boca Raton
Ross AIV, Griffiths MW, Mittal GS, Deeth HC (2003) Combining nonthermal technologies to control foodborne microorganisms. Int J Food Microbiol 89(2–3):125–138
Wu T, Cheng D, He M, Pan S, Yao X, Xu X (2014) Antifungal action and inhibitory mechanism of polymethoxylated flavones from Citrus reticulata Blanco peel against Aspergillus niger. Food Control 35(1):354–359
Lu J, Pua X-H, Liu C-T, Chang C-L, Cheng K-C (2014) The implementation of HACCP management system in a chocolate ice cream plant. J Food Drug Anal 22(3):391–398
Deliza R, Rosenthal A, Abadio FBD, Silva CHO, Castillo C (2005) Application of high pressure technology in the fruit juice processing: benefits perceived by consumers. J Food Eng 67(1–2):241–246
Queiros RP, Santos MD, Fidalgo LG, Mota MJ, Lopes RP, Inacio RS, Delgadillo I, Saraiva JA (2014) Hyperbaric storage of melon juice at and above room temperature and comparison with storage at atmospheric pressure and refrigeration. Food Chem 147:209–214
Fernandes PA, Moreira SA, Fidalgo LG, Santos MD, Queirós RP, Delgadillo I, Saraiva JA (2015) Food preservation under pressure (hyperbaric storage) as a possible improvement/alternative to refrigeration. Food Eng Rev 7(1):1–10
Robitaille HA, Badenhop AF (1981) Mushroom response to postharvest hyperbaric storage. J Food Sci 46(1):249–253
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46(2):446–475
Tripoli E, La Guardia M, Giammanco S, Di Majo D, Giammanco M (2007) Citrus flavonoids: molecular structure, biological activity and nutritional properties: a review. Food Chem 104(2):466–479
Cormier J, Scott R, Janes M (2013) Antibacterial activity of biosecur® citrus extract surface cleaner against vibrio vulnificus. Open Microbiol J 8(7):130–134
Choi JS, Yokozawa T, Oura H (1991) Antihyperlipidemic effect of flavonoids from Prunus davidiana. J Nat Prod 54(1):218–224
Geleijnse JM, Hollman PC (2008) Flavonoids and cardiovascular health: which compounds, what mechanisms? Am J Clin Nutr 88(1):12–13
Hertog MG, Feskens EJ, Kromhout D, Hollman P, Katan M (1993) Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly Study. The Lancet 342(8878):1007–1011
Kaul TN, Middleton E, Ogra PL (1985) Antiviral effect of flavonoids on human viruses. J Med Viro 15(1):71–79
Nedovic V, Kalusevic A, Manojlovic V, Levic S, Bugarski B (2011) An overview of encapsulation technologies for food applications. Proc Food Science 1:1806–1815
Weiss J, Gaysinsky S, Davidson M, McClements J (2009) Global issues in food science and technology. In: Barbosa-Cánovas G, Lineback D, Spiess W, Buckle K, Colonna P (eds) Nanostructured encapsulation systems—food antimicrobials. Academic Press, New York
FDA (2017) CFR—Code of Federal Regulations Title 21
Hc-sc.gc.ca (2016) Permitted preservatives—lists of permitted food additives—Health Canada
Maherani B, Khlifi MA, Salmieri S, Lacroix M (2018) Design of biosystems to provide healthy and safe food. Part A: effect of emulsifier and preparation technique on physicochemical, antioxidant and antimicrobial properties. Eur Food Res Technol 244:1963–1975
Maherani B, Arab-Tehrany E, Kheirolomoom A, Cleymand F, Linder M (2012) Influence of lipid composition on physicochemical properties of nanoliposomes encapsulating natural dipeptide antioxidant l-carnosine. Food Chem 134(2):632–640
Bevilacqua A, Corbo M, Campaniello D, D’Amato D, Gallo M, Speranza B, Sinigaglia M (2011) Shelf life prolongation of fruit juices through essential oils and homogenization: a review. Sci Against Microb Pathogens Commun Curr Res Technol Adv 3:1157–1166
Hossain F, Follett P, Vu KD, Salmieri S, Senoussi C, Lacroix M (2014) Radiosensitization of Aspergillus niger and Penicillium chrysogenum using basil essential oil and ionizing radiation for food decontamination. Food Control 45:156–162
Pérez-Conesa D, Cao J, Chen L, McLandsborough L, Weiss J (2011) Inactivation of Listeria monocytogenes and Escherichia coli O157: H7 biofilms by micelle-encapsulated eugenol and carvacrol. J Food Prot 74(1):55–62
Salvia-Trujillo L, Rojas-Graü MA, Soliva-Fortuny R, Martín-Belloso O (2014) Impact of microfluidization or ultrasound processing on the antimicrobial activity against Escherichia coli of lemongrass oil-loaded nanoemulsions. Food Control 37:292–297
Hunter DR, Segel IH (1973) Effect of weak acids on amino acid transport by Penicillium chrysogenum: evidence for a proton or charge gradient as the driving force. J Bacteriol 113(3):1184–1192
Gutierrez J, Barry-Ryan C, Bourke P (2009) Antimicrobial activity of plant essential oils using food model media: efficacy, synergistic potential and interactions with food components. Food Microbiol 26(2):142–150
Lück E (1990) Food applications of sorbic acid and its salts. Food Addit Contam 7(5):711–715
Liewen MB, Marth EH (1984) Inhibition of penicillia and aspergilli by potassium sorbate. J Food Prot 47(7):554–556
Liewen MB, Marth EH (1985) Growth and inhibition of microorganisms in the presence of sorbic acid: a review. J Food Prot 48(4):364–375
Qian C, McClements DJ (2011) Formation of nanoemulsions stabilized by model food-grade emulsifiers using high-pressure homogenization: factors affecting particle size. Food Hydrocoll 25(5):1000–1008
McClements DJ (2015) Food emulsions: principles, practices, and techniques. CRC press, New York
Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Pérez-Álvarez J (2008) Antifungal activity of lemon (Citrus lemon L.), mandarin (Citrus reticulata L.), grapefruit (Citrus paradisi L.) and orange (Citrus sinensis L.) essential oils. Food Control 19(12):1130–1138
Lucini E, Zunino M, López M, Zygadlo J (2006) Effect of monoterpenes on lipid composition and sclerotial development of Sclerotium cepivorum Berk. J Phytopathol 154(7-8):441–446
Salvia-Trujillo L, Rojas-Graü A, Soliva-Fortuny R, Martín-Belloso O (2015) Physicochemical characterization and antimicrobial activity of food-grade emulsions and nanoemulsions incorporating essential oils. Food Hydrocoll 43:547–556
Schweizer HP (2012) Understanding efflux in Gram-negative bacteria: opportunities for drug discovery. Expert Opinion Drug Discov 7(7):633–642
Ortuño A, Báidez A, Gómez P, Arcas M, Porras I, García-Lidón A, Del Rio J (2006) Citrus paradisi and Citrus sinensis flavonoids: their influence in the defence. Food Chem 98(2):351–358
Bouhdid S, Abrini J, Zhiri A, Espuny M, Manresa A (2009) Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil. J Appl Microbiol 106(5):1558–1568
Uribe S, Ramirez J, Peña A (1985) Effects of beta-pinene on yeast membrane functions. J Bacteriol 161(3):1195–1200
Tserennadmid R, Tako M, Galgoczy L, Papp T, Pesti M, Vagvolgyi C, Almassy K, Krisch J (2011) Anti-yeast activities of some essential oils in growth medium, fruit juices and milk. Int J Food Microbiol 144(3):480–486
Belletti N, Kamdem SS, Patrignani F, Lanciotti R, Covelli A, Gardini F (2007) Antimicrobial activity of aroma compounds against Saccharomyces cerevisiae and improvement of microbiological stability of soft drinks as assessed by logistic regression. Appl Environ Microbiol 73(17):5580–5586
Khan A, Ahmad A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N (2010) Ocimum sanctum essential oil and its active principles exert their antifungal activity by disrupting ergosterol biosynthesis and membrane integrity. Res Microbiol 161(10):816–823
Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L (2009) Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol 58(11):1454–1462
Tzortzakis NG, Economakis CD (2007) Antifungal activity of lemongrass (Cymbopogon citratus L.) essential oil against key postharvest pathogens. Innov Food Sci Emerg Technol 8(2):253–258
Stratford M (2006) Food and beverage spoilage yeasts. In: Querol A, Fleet GH (eds) The yeast handbook, yeasts in food and beverages. Springer, Berlin
Mollapour M, Piper PW (2001) The ZbYME2 gene from the food spoilage yeast Zygosaccharomyces bailii confers not only YME2 functions in Saccharomyces cerevisiae but also the capacity for catabolism of sorbate and benzoate, two major weak organic acid preservatives. Mol Microbiol 42(4):919–930
Stratford M, Plumridge A, Archer DB (2007) Decarboxylation of sorbic acid by spoilage yeasts is associated with the PAD1 gene. Appl Environ Microbiol 73(20):6534–6542
Walker M, Phillips CA (2008) The effect of preservatives on Alicyclobacillus acidoterrestris and Propionibacterium cyclohexanicum in fruit juice. Food Control 19(10):974–981
Leyva J, Peinado J (2005) ATP requirements for benzoic acid tolerance in Zygosaccharomyces bailii. J Appl Microbiol 98(1):121–126
Wallis AA (2013) Inhibition of spoilage yeasts using spice essential oils and their components. Master thesis, University of Tennessee
Kurtzman CP (2001) Yeasts: Characteristics and Identification. In: Barnett JA, Payne RW, Yarrow D (eds) The quarterly review of biology. Cambridge University Press, Cambridge
Thomas DS (1993) Yeasts as spoilage organisms in beverages. In: Rose AH, Harrison JS (eds) The yeasts, yeast technology, 2nd edn. Academic press, London
Loureiro V, Querol A (1999) The prevalence and control of spoilage yeasts in foods and beverages. Trends Food Sci Technol 10(11):356–365
Baranauskaite J, Kubiliene A, Marksa M, Petrikaite V, VitkeviIius K, Baranauskas A, Bernatoniene J (2017) The influence of different oregano species on the antioxidant activity determined Using HPLC postcolumn DPPH method and anticancer activity of carvacrol and rosmarinic acid. Biomed Res Int. https://doi.org/10.1155/2017/1681392
Nazzaro F, Fratianni F, Coppola R, De Feo V (2017) Essential oils and antifungal activity. Pharmaceuticals 10(86):1–20
Tzortzakis N, Economakis C (2007) Antifungal activity of lemongrass (Cympopogon citratus L.) essential oil against key postharvest pathogens. Innov Food Sci Emerg Technol 8(2):253–258
de Bona da Silva C, Guterres SS, Weisheimer V, Schapoval EES (2008) Antifungal activity of the lemongrass oil and citral against Candida spp. Braz J Infect Dis 12(1):63–66
Baines D, Seal R (2012) Natural food additives, ingredients and flavorings, First edn. Woodhead Publishing, Sawston
Acknowledgements
This work was financially supported by the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ) (Innov’Action Project #IA 115316) and Biosecur Lab Inc. Also, the members of RESALA laboratory appreciate the Biosecur Lab for providing Biosecur products.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Compliance with ethics requirements
This article does not contain any studies with human or animal subjects.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Maherani, B., Khlifi, M.A., Salmieri, S. et al. Design of biosystems to provide healthy and safe food—part B: effect on microbial flora and sensory quality of orange juice. Eur Food Res Technol 245, 581–591 (2019). https://doi.org/10.1007/s00217-018-03228-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-018-03228-2