Active properties of edible marine polysaccharide-based coatings containing Larrea nitida polyphenols enriched extract

https://doi.org/10.1016/j.foodhyd.2019.105595Get rights and content

Highlights

  • Polyphenolic plant extracts were used for the development of active edible coatings.

  • Larrea nitida extract showed the greatest antioxidant and antimicrobial properties.

  • Ln extract was not toxic or genotoxic at the concentration used (500 μg/mL).

  • Antioxidant and antimicrobial coatings were formed with agar, alginate and Ln extract.

  • Ln containing coatings reduced the titers of MNV in artificially contaminated berries.

Abstract

The aim of this work was to develop active edible coatings based on marine polysaccharide matrices and polyphenols-enriched native plant extracts from arid and semiarid regions of Argentina. Initially, five plant extracts were characterized in terms of antioxidant, antibacterial and antiviral activity and the one with better biological properties and no toxicity or genotoxicity, Larrea nitida (Ln) extract, was incorporated into agar, alginate or agar/alginate matrices. The Ln extract-containing films were characterized in terms of physicochemical and polyphenols release performance in food simulants. The incorporation of Ln extract provided darker films, with a more saturated orange-brownish color and with negligible effects on mechanical and barrier properties. Additionally, all the coatings showed antiviral activity when applied to blueberries against murine norovirus (MNV), a cultivable norovirus surrogate. The coatings of agar and Ln extract was able to reduce the infectivity of MNV below the limit of detection after over-night (ON) incubation at 25 °C and after 4 days at 10 °C storage.

These edible polysaccharides coatings containing Ln extract could be an alternative to reduce or eliminate foodborne viruses and protect the food against oxidative process.

Introduction

Fresh and minimally processed vegetables and fruits market has grown up exponentially because of the changes in consumer's lifestyle. Consumer's preferences towards fresher products with natural additives have made the food industry to focus its efforts on the development of innovative preservation technologies to reduce the growth of both spoilage and foodborne pathogens such as bacteria and human enteric viruses (Dilmaçünal & Kuleaşan, 2018; Prakash, Baskaran, Paramasivam, & Vadivel, 2018). In this regard, edible coatings have recently emerged as one of the most promising technologies for controlling the quality and safety of fresh products while extending their shelf life (Fabra, Falcó, Randazzo, Sánchez, & López-Rubio, 2018; Falcó, Randazzo, Sánchez, López-Rubio, & Fabra, 2019; Guo, Yadav, & Jin, 2017; Majid, Nayik, Dar, & Nanda, 2018).

Edible coatings are based on biodegradable, biocompatible and food-grade polymers from natural sources, which include polysaccharides, proteins, and lipids. Among these materials, polysaccharides have been widely studied and used for the development of edible coatings due to good film forming availability as well as suitable mechanical and gas barrier properties (Hou et al., 2019). More concretely, research interest in the use of marine polysaccharides (Hou et al., 2019; Kanmani & Whan Rhim, 2014; Shankar & Rhim, 2017; Tavassoli-Kafrani, Shekarchizadeh, & Masoudpour-Behabadi, 2015) such as carrageenan, agar and alginate as biopolymer matrices has increased as they are highly abundant, inexpensive, absorbent, non-toxic and non-immunogenic (Fabra et al., 2018; Oliveira Filho et al., 2019; Shankar & Rhim, 2017). Marine polysaccharides are also attracting great attention because, some of them, have unique antiviral properties to assure the food safety (Falcó et al., 2019). Furthermore, polysaccharide-based coatings present a high potential to serve as vehicles to incorporate active compounds, which greatly contribute to extend product shelf life and to reduce the risk of pathogen growth on food surface (Bhardwaj, Alam, & Talwar, 2019). In fact, several works have been carried out in the last decades dealing with active biopolymer matrices containing essential oils and/or natural extracts (Ganiari, Choulitoudi, & Oreopoulou, 2017; Moghimi, Aliahmadi, & Rafati, 2017). Polyphenolic-enriched plant extracts represent an interesting ingredient for the development of edible coatings, mainly due to their natural origin and phytochemical properties, which allows obtaining active materials with the aim of extending the shelf life and the value to the products (Luchese, Brum, Piovesana, Caetano, & Flôres, 2017; Mir, Dar, Wani, & Shah, 2018).

Zuccagnia punctata Cav., Larrea divaricata Cav., Larrea cuneifolia Cav., Larrea nitida Cav., and Tetraglochin andina Ciald. are shrubs that grow in arid and semiarid regions of Argentina and have demonstrated biological activities such as antifungal (Butassi et al., 2015, 2018; Moreno et al., 2018a, b), antibacterial (Zampini, Cudmani, & Isla, 2012), antigenotoxic (Zampini et al., 2008), antioxidant (Álvarez Echazú et al., 2018; Carabajal, Zampini & Isla, 2017; Moreno et al., 2018a, Moreno et al., 2018b, Moreno et al., 2018c ) and anti-inflammatory (Torres Carro et al., 2017), which have been mainly attributed to their high content in chalcones, flavonoids, phenolic acids, and lignans (Isla et al., 2016; Moreno et al., 2018a, Moreno et al., 2018b, Moreno et al., 2018c ). However, although several biological properties have been studied, the activity of these plant species against foodborne bacteria and viruses of interest in the food industry has not been previously described and there is not existing literature on their application as active edible coatings.

Concretly, this work compares the potential of alginate and agar on the antiviral activity and their synergetic effect when mixed with natural extracts with potential virucide activity. Although both polysaccharides have excellent film-forming properties, agar forms a slightly viscous fluid that can form thermorreversible gels when the temperature is decreased below a certain temperature and thus, temperatures around 40 °C are needed when applied as an edible coating, fact that could partially limit their application on fresh and perishable fruits like berries. To improve handing properties of the agar-based matrices, alginate was used in the mixture and compared to the counterparts prepared with pure polysaccharide matrices.

Therefore, the main aim of this work was: (i) to characterize and evaluate the most relevant active properties, and the toxicity of the extracts obtained from Argentinian medicinal plants; (ii) to investigate the physicochemical properties of edible polysaccharide-based films containing the most bioactive extract; and (iii) to assess the antiviral efficacy when applied onto the surfaces of blueberries at room and refrigeration temperatures.

Section snippets

Reagents

Alginic acid sodium salt from brown algae (medium viscosity), 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), and dimethylsulfoxide (DMSO) were purchased from Sigma-Aldrich. Agar was obtained from Hispanagar S.A. (Burgos, Spain) and glycerol was purchased from Panreac- Aplichem. Mueller Hinton Broth (MHB), Mueller Hinton Agar (MHA), peptone water and Palcam agar were purchased from Scharlab.

Plant material

The used plant parts were leaves and stems (aerial parts), according to

Preparation and characterization of phenolic enriched extracts of medicinal plants

Polyphenolic-enriched extracts are of considerable interest and have received increased attention in recent years due to their bioactive properties. In the first part of this work, the antioxidant and antimicrobial (antiviral and antibacterial) activity against foodborne pathogens (L. innocua, E. coli and MNV) of the five hydroalcoholic extracts, having a content of TPC between 354.7 and 397.9 mg GAE/g dry extract (Moreno et al., 2018a, Moreno et al., 2018b, Moreno et al., 2018c ) were analyzed.

Conclusions

Plant species that grow in arid and semiarid regions of Argentina were proposed as active compounds for the development of active edible coatings for food applications. Amongst them, Ln extract showed the most promising antimicrobial and antioxidant properties, being a potential antiviral compound for foodborne viruses. Furthermore, it was proved not to be toxic or genotoxic at 500 μg/mL, being this concentration selected for the development of antiviral edible coatings based on marine

CRediT authorship contribution statement

María Alejandra Moreno: Formal analysis, Methodology, Writing - original draft. Hylenne Bojorges: Formal analysis, Methodology. Irene Falcó: Methodology. Gloria Sánchez: Data curation, Formal analysis, Investigation, Methodology, Supervision, Writing - review & editing. Gracia López-Carballo: Methodology. Amparo López-Rubio: Conceptualization, Data curation, Supervision, Resources, Writing - review & editing. Iris Catiana Zampini: Methodology. María Inés Isla: Conceptualization, Resources,

Declaration of competing interest

The authors declare that there are no conflicts of interest.

Acknowledgements

This research was supported by grants from Secretaría de Ciencia, Arte e Innovación Tecnológica de la Universidad Nacional de Tucumán, Argentina (PIUNT 637), Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (Proyecto UE-0011, doctoral and postdoctoral scholarship), Agencia Nacional de Promoción Científica y Tecnológica (PICT 3136, PICT 4436), Agencia Estatal de Investigación (AEI, Grant PCI2018-092886) and cofunded by the European Union's Horizon 2020 research and

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