Abstract
Gum arabic stabilised oil-in-water emulsions were prepared through ultrasonication approach for the incorporation of natural, plant-based antimicrobial compounds, geraniol and carvacrol. The oil phase of formulated emulsions was constituted with geraniol and carvacrol, incorporated at various ratios of 1:0, 2:1, 1:1, 1:2, and 0:1 (v/v). The ultrasonication procedure was followed using a frequency of 20 kHz at 40% amplitude for 5 min. These emulsion systems were characterized for mean particle diameter, polydispersity index, ζ-potential, storage stability and creaming index. In addition, emulsion microstructure was studied using confocal laser scanning microscopy (CLSM) and transmission electron microscopy (TEM). Evaluation of antimicrobial activity of the functional emulsions was carried out against Gram-positive bacteria Bacillus cereus MTCC 430 and Gram-negative bacteria Escherichia coli MTCC 443. The results demonstrated that geraniol: carvacrol (1:1) emulsion formulation displayed good stability with particle size (202.7 ± 4.17 nm), polydispersity (0.282 ± 0.001), ζ-potential (− 19.37 ± 0.06 mV) and no visible separation of cream was observed. Furthermore, the CLSM and TEM observations confirmed the presence of stable emulsion. In addition, the antimicrobial susceptibility tests demonstrated collaborative activity and prolonged antibacterial efficacy for the combined essential oil-based emulsion against both the model bacterial pathogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ζ:
-
Zeta potential
References
Abdollahzadeh E, Rezaei M, Hosseini H (2014) Antibacterial activity of plant essential oils and extracts: the role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control 35:177–183. https://doi.org/10.1016/j.foodcont.2013.07.004
Anandan S, Keerthiga M, Vijaya S, Asiri AM, Bogush V, Krasulyaa O (2017) Physicochemical characterization of black seed oil-milk emulsions through ultrasonication. Ultrason Sonochem 38:766–771. https://doi.org/10.1016/j.ultsonch.2016.11.005
Bennett SD, Walsh KA, Gould LH (2013) Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus—United States, 1998–2008. Clin Infect Dis 57:425–433. https://doi.org/10.1093/cid/cit244
Bi L, Yang L, Narsimhan G, Bhunia AK, Yao Y (2011) Designing carbohydrate nanoparticles for prolonged efficacy of antimicrobial peptide. J Control Release 150:150–156. https://doi.org/10.1016/j.jconrel.2010.11.024
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Chang Y, McLandsborough L, McClements DJ (2015) Fabrication, stability and efficacy of dual-component antimicrobial nanoemulsions: essential oil (thyme oil) and cationic surfactant (lauric arginate). Food Chem 172:298–304. https://doi.org/10.1016/j.foodchem.2014.09.081
Chen W, Viljoen AM (2010) Geraniol—a review of a commercially important fragrance material. S Afr J Bot 76:643–651. https://doi.org/10.1016/j.sajb.2010.05.008
Devi KP, Nisha SA, Sakthivel R, Pandian SK (2010) Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 130:107–115. https://doi.org/10.1016/j.jep.2010.04.025
Dickinson E (2009) Hydrocolloids as emulsifiers and emulsion stabilizers. Food Hydrocolloid 23:1473–1482. https://doi.org/10.1016/j.foodhyd.2008.08.005
Dickinson E (2010) Food emulsions and foams: stabilization by particles. Curr Opin Colloid Interface Sci 15:40–49. https://doi.org/10.1016/j.cocis.2009.11.001
Ehling-Schulz M, Fricker M, Scherer S (2004) Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol Nutr Food Res 48:479–487. https://doi.org/10.1002/mnfr.200400055
Epand RM, Epand RF (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta 1788:289–294. https://doi.org/10.1016/j.bbamem.2008.08.023
Food and Drug Administration (2017) Food additives permitted for direct addition to food for human consumption: synthetic flavoring substances and adjuvants. In: Code of federal regulations, Title 21, vol 3, Part 182.20. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=182.20
Ghosh V, Mukherjee A, Chandrasekaran N (2013) Ultrasonic emulsification of food-grade nanoemulsion formulation and evaluation of its bactericidal activity. Ultrason Sonochem 20:338–344. https://doi.org/10.1016/j.ultsonch.2012.08.010
Goyal A, Sharma V, Upadhyay N, Singh AK, Arora S, Lal D, Sabikhi L (2015) Development of stable flaxseed oil emulsions as a potential delivery system of omega-3 fatty acids. J Food Sci Technol 52:4256–4265. https://doi.org/10.1007/s13197-014-1370-2
Guarda A, Rubilar JF, Miltz J, Galotto MJ (2011) The antimicrobial activity of microencapsulated thymol and carvacrol. Int J Food Microbiol 146:144–150. https://doi.org/10.1016/j.ijfoodmicro.2011.02.011
Hernández-González M et al (2017) Polysuccinimide functionalized with oregano’s essential oil extracts, an antimicrobial extended release bio-material. Mater Lett 191:73–76. https://doi.org/10.1016/j.matlet.2017.01.035
Hu Q, Gerhard H, Upadhyaya I, Venkitanarayanan K, Luo Y (2016) Antimicrobial eugenol nanoemulsion prepared by gum arabic and lecithin and evaluation of drying technologies. Int J Biol Macromol 87:130–140. https://doi.org/10.1016/j.ijbiomac.2016.02.051
Hussein J, El-Bana M, Refaat E, El-Naggar ME (2017) Synthesis of carvacrol-based nanoemulsion for treating neurodegenerative disorders in experimental diabetes. J Funct Foods 37:441–448. https://doi.org/10.1016/j.jff.2017.08.011
Jain A, Thakur D, Ghoshal G, Katare O, Shivhare U (2015) Microencapsulation by complex coacervation using whey protein isolates and gum acacia: an approach to preserve the functionality and controlled release of β-carotene. Food Bioprocess Technol 8:1635–1644. https://doi.org/10.1007/s11947-015-1521-0
Jayme ML, Dunstan DE, Gee ML (1999) Zeta potentials of gum arabic stabilised oil in water emulsions. Food Hydrocoll 13:459–465. https://doi.org/10.1016/S0268-005x(99)00029-6
Jiménez M, Domínguez JA, Pascual-Pineda LA, Azuara E, Beristain C (2017) Elaboration and characterization of O/W cinnamon (Cinnamomum zeylanicum) and black pepper (Piper nigrum) emulsions. Food Hydrocoll. https://doi.org/10.1016/j.foodhyd.2017.11.037
Ju J, Xu X, Xie Y, Guo Y, Cheng Y, Qian H, Yao W (2018) Inhibitory effects of cinnamon and clove essential oils on mold growth on baked foods. Food Chem 240:850–855. https://doi.org/10.1016/j.foodchem.2017.07.120
Khem S, Bansal V, Small DM, May BK (2016) Comparative influence of pH and heat on whey protein isolate in protecting Lactobacillus plantarum A17 during spray drying. Food Hydrocoll 54:162–169. https://doi.org/10.1016/j.foodhyd.2015.09.029
Kowalska M, Zbikowska A, Wozniak M, Kucharczyk K (2017) Long-term stability of emulsion based on rose oil. J Dispers Sci Technol 38:1563–1569. https://doi.org/10.1080/01932691.2016.1262777
Kumar DL, Sarkar P (2017) Encapsulation of bioactive compounds using nanoemulsions. Environ Chem Lett. https://doi.org/10.1007/s10311-017-0663-x
Kwon SJ, Chang Y, Han J (2017) Oregano essential oil-based natural antimicrobial packaging film to inactivate Salmonella enterica and yeasts/molds in the atmosphere surrounding cherry tomatoes. Food Microbiol 65:114–121. https://doi.org/10.1016/j.fm.2017.02.004
Liang R, Xu S, Shoemaker CF, Li Y, Zhong F, Huang Q (2012) Physical and antimicrobial properties of peppermint oil nanoemulsions. J Agric Food Chem 60:7548–7555. https://doi.org/10.1021/jf301129k
Lu WC, Huang DW, Wang CR, Yeh CH, Tsai JC, Huang YT, Li PH (2018) Preparation, characterization, and antimicrobial activity of nanoemulsions incorporating citral essential oil. J Food Drug Anal 26:82–89. https://doi.org/10.1016/j.jfda.2016.12.018
Ma Q, Davidson PM, Zhong Q (2016) Nanoemulsions of thymol and eugenol co-emulsified by lauric arginate and lecithin. Food Chem 206:167–173. https://doi.org/10.1016/j.foodchem.2016.03.065
Martinez-Hernandez GB, Amodio ML, Colelli G (2017) Carvacrol-loaded chitosan nanoparticles maintain quality of fresh-cut carrots. Innov Food Sci Emerg 41:56–63. https://doi.org/10.1016/j.ifset.2017.02.005
McClements DJ, Decker EA, Weiss J (2007) Emulsion-based delivery systems for lipophilic bioactive components. J Food Sci 72:R109–R124. https://doi.org/10.1111/j.1750-3841.2007.00507.x
Mirhosseini H, Amid BT (2012) A review study on chemical composition and molecular structure of newly plant gum exudates and seed gums. Food Res Int 46:387–398. https://doi.org/10.1016/j.foodres.2011.11.017
Mirhosseini H, Tan CP, Hamid NSA, Yusof S (2008) Optimization of the contents of Arabic gum, xanthan gum and orange oil affecting turbidity, average particle size, polydispersity index and density in orange beverage emulsion. Food Hydrocoll 22:1212–1223. https://doi.org/10.1016/j.foodhyd.2007.06.011
Moon H, Rhee MS (2016) Synergism between carvacrol or thymol increases the antimicrobial efficacy of soy sauce with no sensory impact. Int J Food Microbiol 217:35–41. https://doi.org/10.1016/j.ijfoodmicro.2015.10.009
Niu F, Pan W, Su Y, Yang Y (2016) Physical and antimicrobial properties of thyme oil emulsions stabilized by ovalbumin and gum arabic. Food Chem 212:138–145. https://doi.org/10.1016/j.foodchem.2016.05.172
Noshad M, Mohebbi M, Shahidi F, Koocheki A (2015) Freeze–thaw stability of emulsions with soy protein isolate through interfacial engineering. Int J Refrig 58:253–260. https://doi.org/10.1016/j.ijrefrig.2015.05.007
Oussalah M, Caillet S, Saucier L, Lacroix M (2007) Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157: H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 18:414–420. https://doi.org/10.1016/j.foodcont.2005.11.009
Pol IE, Smid EJ (1999) Combined action of nisin and carvacrol on Bacillus cereus and Listeria monocytogenes. Lett Appl Microbiol 29:166–170. https://doi.org/10.1046/j.1365-2672.1999.00606.x
Salvia-Trujillo L, Rojas-Grau MA, Soliva-Fortuny R, Martin-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. https://doi.org/10.1016/j.foodcont.2013.09.015
Salvia-Trujillo L, Rojas-Grau A, Soliva-Fortuny R, Martin-Belloso O (2015) Physicochemical characterization and antimicrobial activity of food-grade emulsions and nanoemulsions incorporating essential oils. Food Hydrocoll 43:547–556. https://doi.org/10.1016/j.foodhyd.2014.07.012
São José JFBd, Andrade NJd, Ramos AM, Vanetti MCD, Stringheta PC, Chaves JBP (2014) Decontamination by ultrasound application in fresh fruits and vegetables. Food Control 45:36–50. https://doi.org/10.1016/j.foodcont.2014.04.015
Sarkar P, Bhunia AK, Yao Y (2017) Impact of starch-based emulsions on the antibacterial efficacies of nisin and thymol in cantaloupe juice. Food Chem 217:155–162. https://doi.org/10.1016/j.foodchem.2016.08.071
Shah B, Ikeda S, Michael Davidson P, Zhong Q (2012) Nanodispersing thymol in whey protein isolate-maltodextrin conjugate capsules produced using the emulsion–evaporation technique. J Food Eng 113:79–86. https://doi.org/10.1016/j.jfoodeng.2012.05.019
Sharma M, Mann B, Sharma R, Bajaj R, Athira S, Sarkar P, Pothuraju R (2017) Sodium caseinate stabilized clove oil nanoemulsion: physicochemical properties. J Food Eng 212:38–46. https://doi.org/10.1016/j.jfoodeng.2017.05.006
Silva-Angulo AB, Zanini SF, Rosenthal A, Rodrigo D, Klein G, Martinez A (2015) Combined effect of carvacrol and citral on the growth of Listeria monocytogenes and Listeria innocua and on the occurrence of damaged cells. Food Control 53:156–162. https://doi.org/10.1016/j.foodcont.2015.01.028
Sivapratha S, Sarkar P (2018) Multiple layers and conjugate materials for food emulsion stabilization. Crit Rev Food Sci Nutr 58:877–892. https://doi.org/10.1080/10408398.2016.1227765
Sosa N, Schebor C, Pérez OE (2014) Encapsulation of citral in formulations containing sucrose or trehalose: emulsions properties and stability. Food Bioprod Process 92:266–274. https://doi.org/10.1016/j.fbp.2013.08.001
Sugumar S, Ghosh V, Nirmala MJ, Mukherjee A, Chandrasekaran N (2014) Ultrasonic emulsification of eucalyptus oil nanoemulsion: antibacterial activity against Staphylococcus aureus and wound healing activity in Wistar rats. Ultrason Sonochem 21:1044–1049. https://doi.org/10.1016/j.ultsonch.2013.10.021
Tontul I, Topuz A (2014) Influence of emulsion composition and ultrasonication time on flaxseed oil powder properties. Powder Technol 264:54–60. https://doi.org/10.1016/j.powtec.2014.05.002
Topuz OK, Ozvural EB, Zhao Q, Huang Q, Chikindas M, Golukcu M (2016) Physical and antimicrobial properties of anise oil loaded nanoemulsions on the survival of foodborne pathogens. Food Chem 203:117–123. https://doi.org/10.1016/j.foodchem.2016.02.051
Ultee A, Gorris LG, Smid EJ (1998) Bactericidal activity of carvacrol towards the food-borne pathogen Bacillus cereus. J Appl Microbiol 85:211–218. https://doi.org/10.1046/j.1365-2672.1998.00467.x
Ultee A, Kets EP, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65:4606–4610
Ultee A, Bennik M, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 68:1561–1568. https://doi.org/10.1128/AEM.68.4.1561-1568.2002
Visalli MA, Jacobs MR, Appelbaum PC (1996) MIC and time-kill study of activities of DU-6859a, ciprofloxacin, levofloxacin, sparfloxacin, cefotaxime, imipenem, and vancomycin against nine penicillin-susceptible and -resistant pneumococci. Antimicrob Agents Chemother 40:362–366
WHO (2015) WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference grou. World Health Organization, Geneva, pp 2007–2015
Wu JE, Lin J, Zhong QX (2014) Physical and antimicrobial characteristics of thyme oil emulsified with soluble soybean polysaccharide. Food Hydrocoll 39:144–150. https://doi.org/10.1016/j.foodhyd.2013.12.029
Xue J, Michael Davidson P, Zhong Q (2015) Antimicrobial activity of thyme oil co-nanoemulsified with sodium caseinate and lecithin. Int J Food Microbiol 210:1–8. https://doi.org/10.1016/j.ijfoodmicro.2015.06.003
Yao X et al (2013) Physical and chemical stability of gum arabic-stabilized conjugated linoleic acid oil-in-water emulsions. J Agric Food Chem 61:4639–4645. https://doi.org/10.1021/jf400439d
Ye HQ, Shen SX, Xu JY, Lin SY, Yuan Y, Jones GS (2013) Synergistic interactions of cinnamaldehyde in combination with carvacrol against food-borne bacteria. Food Control 34:619–623. https://doi.org/10.1016/j.foodcont.2013.05.032
Ye F, Miao M, Jiang B, Hamaker BR, Jin Z, Zhang T (2017) Characterizations of oil-in-water emulsion stabilized by different hydrophobic maize starches. Carbohydr Polym 166:195–201. https://doi.org/10.1016/j.carbpol.2017.02.079
Yegin Y, Perez-Lewis KL, Zhang M, Akbulut M, Taylor TM (2016) Development and characterization of geraniol-loaded polymeric nanoparticles with antimicrobial activity against foodborne bacterial pathogens. J Food Eng 170:64–71. https://doi.org/10.1016/j.jfoodeng.2015.09.017
Yildirim ST, Oztop MH, Soyer Y (2017) Cinnamon oil nanoemulsions by spontaneous emulsification: formulation, characterization and antimicrobial activity. Lwt-Food Sci Technol 84:122–128. https://doi.org/10.1016/j.lwt.2017.05.041
Zhang Z, Vriesekoop F, Yuan Q, Liang H (2014) Effects of nisin on the antimicrobial activity of d-limonene and its nanoemulsion. Food Chem 150:307–312. https://doi.org/10.1016/j.foodchem.2013.10.160
Zhang W, Chen L, Fang X (2015) Optimizing the preparation conditions for shea butter nanoemulsions via response surface methodology. J Dispers Sci Technol 36:983–990. https://doi.org/10.1080/01932691.2014.942317
Acknowledgements
The authors would like to thank the Science and Engineering Research Board, Govt. of India, for providing financial support for conducting research work through a research grant to Dr. Preetam Sarkar (YSS/2015/000546). The authors would also like to acknowledge technical support extended by Sukanta, Susanta Pradhan, and Subhabrata Chakraborty, National Institute of Technology, Rourkela, for assistance with Zetasizer Nano ZS, confocal laser scanning microscopy imaging and TEM imaging, respectively.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors report no conflict of interest.
Rights and permissions
About this article
Cite this article
Syed, I., Sarkar, P. Ultrasonication-assisted formation and characterization of geraniol and carvacrol-loaded emulsions for enhanced antimicrobial activity against food-borne pathogens. Chem. Pap. 72, 2659–2672 (2018). https://doi.org/10.1007/s11696-018-0501-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11696-018-0501-z