Elsevier

Food Hydrocolloids

Volume 103, June 2020, 105675
Food Hydrocolloids

A peppermint oil emulsion stabilized by resveratrol-zein-pectin complex particles: Enhancing the chemical stability and antimicrobial activity in combination with the synergistic effect

https://doi.org/10.1016/j.foodhyd.2020.105675Get rights and content

Highlights

  • Resveratrol was loaded in zein-pectin particles with partial wettability.

  • Peppermint oil and resveratrol were co-encapsulated in zein-pectin O/W emulsions.

  • Mixture of particles and pectin at the interface decreased size of emulsions.

  • Peppermint oil and resveratrol display synergistic antimicrobial activity.

  • Addition of pectin improved antimicrobial and physicochemical stability.

Abstract

The combination of different antimicrobial agents might produce synergistic effects and has gained increasing interest. Interfacial engineering of emulsion systems has been developed to co-encapsulate and protect bioactive components with different solubility. In this study, peppermint oil and resveratrol display synergistic effect against the Gram-positive bacteria Staphylococcus aureus and the Gram-negative bacteria Salmonella Typhimurium. Partially wettable resveratrol-loaded zein-pectin complex particles with a three-phase contact angle of ~78° were fabricated via a desolvation method. Peppermint oil emulsions with the co-inclusion of resveratrol were successfully prepared by zein-pectin complex particles, showing a high encapsulation efficiency for peppermint oil (~88%) and resveratrol (~99%). Addition of pectin decreased size distribution of the emulsions, improved antimicrobial activity, physical and chemical stability and prolonged antimicrobial efficiency against Staphylococcus aureus and Salmonella Typhimurium. Overall, the current study may have a valuable contribution to develop an efficient antimicrobial system based on the synergistic effect of combined agents and a single emulsion stabilized by protein-polysaccharide complex particles.

Introduction

Essential oils (EOs) are naturally-derived aroma compounds obtained from various parts of edible and medicinal plants and exert strong antibacterial and antifungal activity (Donsi & Ferrari, 2016; Seow, Yeo, Chung, & Yuk, 2014). When two or more agents work together, synergism occurs to produce an effect greater than the sum of individual effects, due to their function on one or more different targets in a metabolic pathway (Seow et al., 2014). For example, the combination of cinnamaldehyde with carvacrol showed synergistic antibacterial effects against both Escherichia coli and Staphylococcus aureus (S. aureus) (Ye et al., 2013). A synergistic antibacterial activity against S. aureus was also observed in nisin combined with cinnamaldehyde in pasteurized milk (Shi et al., 2017). The combination of multiple antibacterial agents has become an important approach to enhance the efficiency of antibacterial therapy and overcome resistance to antibacterial agents. However, poor hydro-solubility and high volatility of EOs limit their application in the pharmaceutical, food and cosmetic industries. It is thus necessary to develop the carriers not only to overcome the limitations but also to enhance the antibacterial activity based on the synergistic effect.

Oil-in-water (O/W) emulsions have been considered to be efficient delivery systems for improving water dispersibility of EOs and preventing their interactions with other food ingredients (Donsi et al., 2016; McClements & Li, 2010). However, the oxidative and physical stability of conventional emulsions is limited due to the high interfacial area and a characteristic porous thin interfacial layer (Berton-Carabin, Sagis, & Schroen, 2018; McClements & Decker, 2018). Recently, interfacial engineering of emulsion systems has been developed to improve the oxidative stability by minimizing interactions between pro-oxidants and bioactive lipids (Berton-Carabin, Ropers, & Genot, 2014; McClements & Decker, 2018). A safflower oil emulsion stabilized by lipid droplets coated by milk protein concentrate (MPC) was prepared, showing slower lipid oxidation than conventional emulsions stabilized by MPC alone. (Okubanjo, Loveday, Ye, Wilde, & Singh, 2019). Resveratrol, as an antioxidant co-emulsifier, can be accumulated at the oil-water interface by interacting with proteins to enhance the oxidative stability (Wan, Wang, Wang, Yuan, & Yang, 2014; Wang, Gao et al., 2016). These provide an opportunity not only to improve the oxidative stability of O/W emulsions but also to co-encapsulate bioactive components with different solubility in the single emulsions.

Zein, a major storage protein in corn, contains more than 50% hydrophobic amino acid residues and is soluble in concentrated aqueous ethanol solutions (60–90%) but not in pure water (Shukla & Cheryan, 2001). This property makes zein a suitable material for the encapsulation of bioactive components, such as α-tocopherol, resveratrol and epigallocatechin gallate (Davidov-Pardo, Joye, & McClements, 2015; Donsi, Voudouris, Veen, & Velikov, 2017; Luo, Zhang, Whent, Yu, & Wang, 2011). A Pickering O/W emulsion was successfully produced by bare zein colloidal particles with droplet size in the range of 10–200 μm (de Folter, van Ruijven, & Velikov, 2012). However, the resulting emulsions were unstable against coalescence at low pH due to the poor wettability of the protein. Surface-modified zein particles with water-soluble biopolymers have been utilized to regulate the surface wettability of zein particles and form stable O/W emulsions (Chen et al., 2018; Dai, Sun, Wei, Mao, & Gao, 2018; Feng & Lee, 2016). Pectin, an anionic polysaccharide, belongs to a family of heterogeneous polysaccharides containing mainly α-(1 → 4)-linked partially methyl esterified d-galacturonic acid and rhamnogalacturonan units (Synytsya, Copikova, Matejka, & Machovic, 2003). Zein-pectin core-shell nanoparticles overcome the aggregation problem of bare zein particles and provide better protection for encapsulated molecules than bare zein particles did (Hu et al., 2015; Huang et al., 2017). Additionally, high methoxyl pectin could strongly absorb to the interface of mandarin or lemongrass oil emulsion and improve physical stability against Ostwald ripening (Guerra-Rosas, Morales-Castro, Ochoa-Martinez, Salvia-Trujillo, & Martin-Belloso, 2016).

Peppermint (Mentha piperita) oil is one of the most widely produced and used essential oils in food, flavorings, and pharmaceutical products. Peppermint oil possesses antimicrobial, antiviral and antifungal activities against various types of bacteria and yeasts (Iscan, Kirimer, Kurkcuoglu, Baser, & Demirci, 2002; Mahboubi & Haghi, 2008). Resveratrol, a natural polyphenol, is produced in plants in response to injury and fungal attack (Summerlin et al., 2015). Resveratrol exhibits a broad spectrum of antimicrobial activity across a wide range of microorganisms (Ma et al., 2018), mainly due to the generation of reactive oxygen species causing DNA damage (Subramanian, Soundar, & Mangoli, 2016), oxidative membrane damage (Subramanian, Goswami, Chakraborty, & Jawali, 2014), and metabolic enzyme inhibition (Dadi, Ahmad, & Ahmad, 2009). In this study, resveratrol-fortified zein-pectin particles were prepared to stabilize a peppermint oil emulsion. Physiochemical property of the colloidal particles and emulsions was characterized. Furthermore, antimicrobial efficiency of peppermint oil and resveratrol combination was evaluated against food-borne pathogens.

Section snippets

Materials

Zein (~98%) was purchased from J&K Chemical Co., Ltd. (Shanghai, China). Pectin (50–300 kDa, degree of esterification ≥47.9%) and resveratrol (trans-isomer, ≥98%) were purchased from Sango Biotech Co. (Shanghai, China). Peppermint (M. piperita) oil was obtained from Shanghai Orinno International Business Co., Ltd. (Shanghai, China). The composition of peppermint oil was reported in Table S1. Menthol (≥98%, GC), menthone (≥97%, GC) and Nile red dye were obtained from Sigma-Aldrich Co. (St.

Size and ζ-potential

The size distribution of bare zein particles had a peak around 80 nm (Fig. S1A), which was consistent with a previous report that zein nanoparticles prepared by desolvation method had an average size of 50–200 nm (Kasaai, 2018). The presence of resveratrol at 0.004%, 0.010%, and 0.020% had no impact on the size of zein particles (Fig. S1A). However, a further increase of resveratrol concentration to 0.040% resulted in precipitation to naked eyes. The polyphenol concentration of 0.020% was thus

Conclusions

In the present study, peppermint oil emulsions stabilized by resveratrol-zein-pectin ternary complex particles have been successfully prepared, showing a good encapsulation performance for both resveratrol and peppermint oil. This system has combined the synergistic effect of two antibacterial agents and emulsion-based carrier, which contributes to the improvement of antimicrobial efficiency and chemical stability. These results obtained here should provide the possibility of co-encapsulating

CRediT authorship contribution statement

Hao Cheng: Conceptualization, Investigation, Writing - original draft, Writing - review & editing. Muhammad Aslam Khan: Investigation. Zhenfeng Xie: Investigation. Shengnan Tao: Resources. Yunxing Li: Resources. Li Liang: Conceptualization, Resources, Writing - review & editing, Supervision.

Declaration of competing interest

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

Acknowledgements

This work received supports from the National Natural Science Foundation of China (NSFC Project 31571781), the Fundamental Research Funds for the Central Universities (JUSRP51711B) and the Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX17_1411).

References (74)

  • F. Donsi et al.

    Essential oil nanoemulsions as antimicrobial agents in food

    Journal of Biotechnology

    (2016)
  • F. Donsi et al.

    Zein-based colloidal particles for encapsulation epigallocatechin gallate and delivery of epigallocatechin gallate

    Food Hydrocolloids

    (2017)
  • Q. Fan et al.

    Partition and stability of resveratrol in whey protein isolate oil-in-water emulsion: Impact of protein and calcium concentrations

    International Dairy Journal

    (2017)
  • Y.M. Feng et al.

    Surface modification of zein colloidal particles with sodium caseinate to stabilize oil-in-water pickering emulsion

    Food Hydrocolloids

    (2016)
  • R.V.D. Fernandes et al.

    Cashew gum and inulin: New alternative for ginger essential oil microencapsulation

    Carbohydrate Polymers

    (2016)
  • V. Filip et al.

    Resveratrol and its antioxidant and antimicrobial effectiveness

    Food Chemistry

    (2003)
  • M.I. Guerra-Rosas et al.

    Long-term stability of food-grade nanoemulsions from high methoxyl pectin containing essential oils

    Food Hydrocolloids

    (2016)
  • S. Gursul et al.

    Antioxidant efficacy of thymol and carvacrol in microencapsulated walnut oil triacylglycerols

    Food Chemistry

    (2019)
  • X.L. Huang et al.

    Resveratrol encapsulation in core-shell biopolymer nanoparticles: Impact on antioxidant and anticancer activities

    Food Hydrocolloids

    (2017)
  • K. Hu et al.

    Core-shell biopolymer nanoparticle delivery systems: Synthesis and characterization of curcumin fortified zein-pectin nanoparticles

    Food Chemistry

    (2015)
  • O.G. Jones et al.

    Effect of polysaccharide charge on formation and properties of biopolymer nanoparticles created by heat treatment of beta-lactoglobulin-pectin complexes

    Food Hydrocolloids

    (2010)
  • M.R. Kasaai

    Zein and zein-based nano-materials for food and nutrition applications: A review

    Trends in Food Science & Technology

    (2018)
  • Y.C. Luo et al.

    Preparation and characterization of zein/chitosan complex for encapsulation of alpha-tocopherol, and its in vitro controlled release study

    Colloids and Surfaces B: Biointerfaces

    (2011)
  • M. Mahboubi et al.

    Antimicrobial activity and chemical composition of Mentha pulegium L. essential oil

    Journal of Ethnopharmacology

    (2008)
  • H. Majeed et al.

    Bactericidal action mechanism of negatively charged food grade clove oil nanoemulsions

    Food Chemistry

    (2016)
  • M. Matos et al.

    O/W emulsions stabilized by OSA-modified starch granules versus non-ionic surfactant: Stability, rheological behaviour and resveratrol encapsulation

    Journal of Food Engineering

    (2018)
  • D.J. McClements et al.

    Structured emulsion-based delivery systems: Controlling the digestion and release of lipophilic food components

    Advances in Colloid and Interface Science

    (2010)
  • R. Melgosa et al.

    Omega-3 encapsulation by PGSS-drying and conventional drying methods. Particle characterization and oxidative stability

    Food Chemistry

    (2019)
  • H. Mirhosseini et al.

    Influence of pectin and CMC on physical stability, turbidity loss rate, cloudiness and flavor release of orange beverage emulsion during storage

    Carbohydrate Polymers

    (2008)
  • C.S. Romano et al.

    Synergistic antioxidant and antibacterial activity of rosemary plus butylated derivatives

    Food Chemistry

    (2009)
  • C. Shi et al.

    Synergistic interactions of nisin in combination with cinnamaldehyde against Staphylococcus aureus in pasteurized milk

    Food Control

    (2017)
  • R. Shukla et al.

    Zein: The industrial protein from corn

    Industrial Crops and Products

    (2001)
  • M. Subramanian et al.

    Resveratrol induced inhibition of Escherichia coli proceeds via membrane oxidation and independent of diffusible reactive oxygen species generation

    Redox Biology

    (2014)
  • N. Summerlin et al.

    Resveratrol nanoformulations: Challenges and opportunities

    International Journal of Pharmaceutics

    (2015)
  • A. Synytsya et al.

    Fourier transform Raman and infrared spectroscopy of pectins

    Carbohydrate Polymers

    (2003)
  • L. Wang et al.

    Effect of resveratrol or ascorbic acid on the stability of alpha-tocopherol in O/W emulsions stabilized by whey protein isolate: Simultaneous encapsulation of the vitamin and the protective antioxidant

    Food Chemistry

    (2016)
  • L.J. Wang et al.

    Fabrication and characterization of Pickering emulsions and oil gels stabilized by highly charged zein/chitosan complex particles (ZCCPs)

    Food Chemistry

    (2016)
  • Cited by (0)

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