Advertisement

Design of biosystems to provide healthy and safe food—part B: effect on microbial flora and sensory quality of orange juice

  • Behnoush Maherani
  • Mohamed Ali Khlifi
  • Stephane Salmieri
  • Monique Lacroix
Original paper
  • 23 Downloads

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.

Keywords

Plant oil extract Organic citrus extract Pathogenic molds and yeast Antifungal activity Microemulsion Sensory analysis 

Notes

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.

Compliance with ethical standards

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.

References

  1. 1.
    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):607–625Google Scholar
  2. 2.
    Mahale DP, Khade RG, Vaidya VK (2008) Microbiological analysis of street vended fruit juices from Mumbai city, India. Internet J Food Saf 10(9):31–34Google Scholar
  3. 3.
    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):1–10Google Scholar
  4. 4.
    FAO (1992) Fruit juices and related products. Codex Alimentarius, RomeGoogle Scholar
  5. 5.
    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):1–10Google Scholar
  6. 6.
    Pawar V, Thaker V (2006) In vitro efficacy of 75 essential oils against Aspergillus niger. Mycoses 49(4):316–323Google Scholar
  7. 7.
    Pitt J (2000) Toxigenic fungi: which are important? Med Mycol 38:17–22Google Scholar
  8. 8.
    Foster T, Vasavada CP (2003) Beverage quality and safety, Microbiology of fruit juice and beverages. CRC Press, Boca RatonGoogle Scholar
  9. 9.
    Ross AIV, Griffiths MW, Mittal GS, Deeth HC (2003) Combining nonthermal technologies to control foodborne microorganisms. Int J Food Microbiol 89(2–3):125–138Google Scholar
  10. 10.
    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):354–359Google Scholar
  11. 11.
    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):391–398Google Scholar
  12. 12.
    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):241–246Google Scholar
  13. 13.
    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 147:209–214Google Scholar
  14. 14.
    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):1–10Google Scholar
  15. 15.
    Robitaille HA, Badenhop AF (1981) Mushroom response to postharvest hyperbaric storage. J Food Sci 46(1):249–253Google Scholar
  16. 16.
    Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46(2):446–475Google Scholar
  17. 17.
    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):466–479Google Scholar
  18. 18.
    Cormier J, Scott R, Janes M (2013) Antibacterial activity of biosecur® citrus extract surface cleaner against vibrio vulnificus. Open Microbiol J 8(7):130–134Google Scholar
  19. 19.
    Choi JS, Yokozawa T, Oura H (1991) Antihyperlipidemic effect of flavonoids from Prunus davidiana. J Nat Prod 54(1):218–224Google Scholar
  20. 20.
    Geleijnse JM, Hollman PC (2008) Flavonoids and cardiovascular health: which compounds, what mechanisms? Am J Clin Nutr 88(1):12–13Google Scholar
  21. 21.
    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):1007–1011Google Scholar
  22. 22.
    Kaul TN, Middleton E, Ogra PL (1985) Antiviral effect of flavonoids on human viruses. J Med Viro 15(1):71–79Google Scholar
  23. 23.
    Nedovic V, Kalusevic A, Manojlovic V, Levic S, Bugarski B (2011) An overview of encapsulation technologies for food applications. Proc Food Science 1:1806–1815Google Scholar
  24. 24.
    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 YorkGoogle Scholar
  25. 25.
    FDA (2017) CFR—Code of Federal Regulations Title 21Google Scholar
  26. 26.
    Hc-sc.gc.ca (2016) Permitted preservatives—lists of permitted food additives—Health CanadaGoogle Scholar
  27. 27.
    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 244:1963–1975Google Scholar
  28. 28.
    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):632–640Google Scholar
  29. 29.
    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 3:1157–1166Google Scholar
  30. 30.
    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 45:156–162Google Scholar
  31. 31.
    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):55–62Google Scholar
  32. 32.
    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 37:292–297Google Scholar
  33. 33.
    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):1184–1192Google Scholar
  34. 34.
    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):142–150Google Scholar
  35. 35.
    Lück E (1990) Food applications of sorbic acid and its salts. Food Addit Contam 7(5):711–715Google Scholar
  36. 36.
    Liewen MB, Marth EH (1984) Inhibition of penicillia and aspergilli by potassium sorbate. J Food Prot 47(7):554–556Google Scholar
  37. 37.
    Liewen MB, Marth EH (1985) Growth and inhibition of microorganisms in the presence of sorbic acid: a review. J Food Prot 48(4):364–375Google Scholar
  38. 38.
    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):1000–1008Google Scholar
  39. 39.
    McClements DJ (2015) Food emulsions: principles, practices, and techniques. CRC press, New YorkGoogle Scholar
  40. 40.
    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):1130–1138Google Scholar
  41. 41.
    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):441–446Google Scholar
  42. 42.
    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 43:547–556Google Scholar
  43. 43.
    Schweizer HP (2012) Understanding efflux in Gram-negative bacteria: opportunities for drug discovery. Expert Opinion Drug Discov 7(7):633–642Google Scholar
  44. 44.
    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):351–358Google Scholar
  45. 45.
    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):1558–1568Google Scholar
  46. 46.
    Uribe S, Ramirez J, Peña A (1985) Effects of beta-pinene on yeast membrane functions. J Bacteriol 161(3):1195–1200Google Scholar
  47. 47.
    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):480–486Google Scholar
  48. 48.
    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):5580–5586Google Scholar
  49. 49.
    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):816–823Google Scholar
  50. 50.
    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):1454–1462Google Scholar
  51. 51.
    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):253–258Google Scholar
  52. 52.
    Stratford M (2006) Food and beverage spoilage yeasts. In: Querol A, Fleet GH (eds) The yeast handbook, yeasts in food and beverages. Springer, BerlinGoogle Scholar
  53. 53.
    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):919–930Google Scholar
  54. 54.
    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):6534–6542Google Scholar
  55. 55.
    Walker M, Phillips CA (2008) The effect of preservatives on Alicyclobacillus acidoterrestris and Propionibacterium cyclohexanicum in fruit juice. Food Control 19(10):974–981Google Scholar
  56. 56.
    Leyva J, Peinado J (2005) ATP requirements for benzoic acid tolerance in Zygosaccharomyces bailii. J Appl Microbiol 98(1):121–126Google Scholar
  57. 57.
    Wallis AA (2013) Inhibition of spoilage yeasts using spice essential oils and their components. Master thesis, University of TennesseeGoogle Scholar
  58. 58.
    Kurtzman CP (2001) Yeasts: Characteristics and Identification. In: Barnett JA, Payne RW, Yarrow D (eds) The quarterly review of biology. Cambridge University Press, CambridgeGoogle Scholar
  59. 59.
    Thomas DS (1993) Yeasts as spoilage organisms in beverages. In: Rose AH, Harrison JS (eds) The yeasts, yeast technology, 2nd edn. Academic press, LondonGoogle Scholar
  60. 60.
    Loureiro V, Querol A (1999) The prevalence and control of spoilage yeasts in foods and beverages. Trends Food Sci Technol 10(11):356–365Google Scholar
  61. 61.
    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 Google Scholar
  62. 62.
    Nazzaro F, Fratianni F, Coppola R, De Feo V (2017) Essential oils and antifungal activity. Pharmaceuticals 10(86):1–20Google Scholar
  63. 63.
    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):253–258Google Scholar
  64. 64.
    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):63–66Google Scholar
  65. 65.
    Baines D, Seal R (2012) Natural food additives, ingredients and flavorings, First edn. Woodhead Publishing, SawstonGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Behnoush Maherani
    • 1
  • Mohamed Ali Khlifi
    • 1
  • Stephane Salmieri
    • 1
  • Monique Lacroix
    • 1
  1. 1.Research Laboratories in Sciences Applied to Food, Canadian Irradiation CenterINRS-Institut Armand-Frappier, Institute of Nutraceutical and Functional FoodsLavalCanada

Personalised recommendations