A review on the efficacy of essential oils and their nanoencapsulated formulations against aflatoxins contamination of major cereals with emphasis on mode of action

https://doi.org/10.1016/j.bcab.2023.102861Get rights and content

Highlights

  • •
    Fungi and aflatoxins contamination in cereal grains with negative health impact.
  • •
    Essential oils (EOs) for protection of cereal grains against aflatoxins contamination.
  • •
    Nanoencapsulation improves stability, efficacy and delivery of EOs in food system.
  • •
    Biochemical and molecular mechanisms of antifungal and antiaflatoxigenic activity.
  • •
    Safety and regulatory aspect of essential oil nanoformulation as green preservative.

Abstract

Aflatoxins (AFs) contamination in cereal grains like rice, maize and wheat during storage represents a challenging issue to global public health. Different synthetic chemicals are commonly used to mitigate AFs contamination; however, their indiscriminate application adversely affects human health, non-target organisms, and the ecosystem. In this regard, botanical preservatives, especially the plant essential oils (EOs) have been recommended as a novel alternative owing to their high safety, biodegradability, and most importantly proved efficacy against AFs production. However, the main obstacles of EOs concerning their large scale application in food system are volatility, poor water solubility, environmental oxidation, and negative impact on organoleptic properties of foods. Nanoencapsulation has been suggested as an innovative strategy to overcome these limitations. The nanoencapsulated EOs formulations show variable mechanisms of actions against AFs contamination with their controlled delivery and stable interactions. This review aims to provide up-to-date information on AFs contamination in major cereals, their impact on human health, analytical detection methods for AFs, and mitigation strategies using EOs and their nanoencapsulated formulations with particular accent on biochemical and molecular mode of action. Finally, the review deals with safety paradigm of EOs and their nanoformulations for their commercial application in food and agricultural industries.

Introduction

Cereal grains are small seeds of herbaceous plants which are edible in nature and belong to family Poaceae. Among different cereal commodities, rice (Oryza sativa L.), maize (Zea mays L.), and wheat (Triticum aestivum L.) are considered as the important cereals, serving as vital source of carbohydrates, proteins, vitamins, fatty acids, and provides more than 50% calories to the world population (Milani and Maleki, 2014; Sarmast et al., 2021). However, during harvesting, transportation, and especially during storage, these cereal commodities have been frequently contaminated by fungal attack and subsequent mycotoxins production, leading to deterioration of their quality and nutritional values (Chaudhari et al., 2020a). Cereal grains whether effectively dried or slightly moist is alive and respiring, hence has the major chances for fungal and mycotoxin contamination (Magan et al., 2010). Poor storage practices along with favorable climatic conditions such as temperature, humidity, pH, and bacterial as well as insects infestation during storage are the major cause of mycotoxin contamination in major cereal grains (Channaiah and Maier, 2014; Neme and Mohammed, 2017).
To date, around 400 mycotoxins have been reported and verified from different agricultural commodities across the world, among which only few including aflatoxins (AFs), ochratoxins (OTAs), fumonisins (FUMs), trichothecenes (TCs) (including deoxynivalenol (DON)), and zearalenones (ZEAs) are the most thoroughly recognized mycotoxins, presenting severe risks to human and livestock's owing to their potential hepatotoxic, teratogenic, mutagenic, nephrotoxic, immunosuppressive, haemorrhagic, and oestrogenic properties (Ostry et al., 2017; Chaudhari et al., 2019). Because of their toxic properties, many countries have set very strict regulation (4 μg/kg for total AFs, 5 μg/kg for Ochratoxins (OTAs, 2000 μg/kg for FUMs, and 750 μg/kg for DON) to control or restrict their concentration extremely low in cereal grains (Gebremeskel et al., 2019; EU Commission Regulation (EU) 2023/915, 2023). These mycotoxins show great variety of chemical structures, toxicokinetics, and biosynthetic origins.
Among these major mycotoxins, AFs secreted by Aspergillus species namely A. flavus, A. parasiticus and A. nomius are highly toxic (Magan et al., 2011). Currently, more than 18 different forms of AFs have been reported in literature, of which aflatoxin B1 (AFB1) has been acknowledged as the most predominant and toxic ones causing serious risks to human even at very low concentration, and hence has been placed under Class I carcinogen by International Agency for Research on Cancer (IARC, Moss, 2002). Furthermore, there is a cumulative attention on safety of cereal grains against mycotoxin contamination. Further, the ubiquitous nature of AFs producing fungi and high stability of AFs to bind with food components are of immense concern in food safety (Ahlberg et al., 2019).
Different physical as well as chemical approaches have been explored to remove or lessen the AFs level in cereal grains. The physical methods include thermal treatments, UV-treatment, γ-irradiation, ozone treatment, pulse light and adsorption (Mir et al., 2021). However, these methods are still not as much as effective in case of AFB1, because of its high thermal stability (Pankaj et al., 2018). Hence, chemical strategies are the effective controlling measure during large-scale storage. A large number of chemical preservatives viz., citric acid, lactic acid, hydrogen peroxide, and ozonated water are commonly employed for decontamination of cereal grains from AFs contamination. The chemical treatments might convert more toxic form of AFs into less toxic. In a study, Jubeen et al. (2020) also reported conversion of AFB1 into less hazardous form (AFB2) after treatment with lactic acid, probably due to hydrolysis of lactone ring (that contribute toxicity to the AF). Some others like butylated hydroxytoluene, butylated hydroxyanisole, butylated hydroquinone, propyl gallate, potassium sorbate, sodium benzoate, nitrites, and sulphites are utilized by food industries to extend the storage life of cereal grains (da Cruz Cabral et al., 2013; Chaudhari et al., 2019). However, their repetitive use creates harmful effects to the non-target organisms and the environment (Singh et al., 2021; Das et al., 2021a).
Therefore, cumulative efforts have been made in the last few years to replace chemical preservatives with botanical formulations as suitable alternative. Among different botanicals, essential oils (EOs) have been employed as safe preservatives of food commodities owing to its noteworthy antimicrobial, insecticidal, and antioxidant capacities and added beneficial effects on human health (Deepika et al., 2020; Chivandi et al., 2016; Chaudhari et al., 2021a, 2021b). Some EOs based preservatives have been formulated by different food and agricultural industries and are commercially available to the market. Recently, “DMC Base Natural” comprising of 50% EOs from Rosemary, Sage, and Citrus and 50% glycerol have been used as safe food preservative (Burt, 2004). Carvone has been used as “TALENT” (an antifungal agent) in Netherland (Tripathi and Dubey, 2004). EcoPCOR is composed of eugenol and has been introduced by EcoSMART technologies for controlling crawling and flying insects. EcoTrol, containing Rosemary EO has been introduced for horticultural fruits (Dayan et al., 2009). However, the major concerns which limit the large scale application of EOs are high volatility, poor water solubility, intense aroma, and oxidation when come in contact with light, heat, moisture, pH, and oxygen (Hosseini et al., 2013). The oxidation of EOs components is also a major limitation for their practical utilization in the food and agricultural industries. Most importantly, the monoterpene components of EO are oxidized at high humidity forming some skin irritating compounds, which limits their practical applications (Doost et al., 2020). In addition, the lipophilic nature of EOs restricts aqueous phase solubility and reduces the bioefficacy of EOs. Moreover, the direct application of EOs cause changes in organoleptic or sensory properties of stored foods. For these reasons, only few EOs have been successfully implemented as natural antifungal agents in food and agrultural industries.
To avoid such constraint, nanoencapsulation of EOs is an effective and potential strategies, which not only enhances their solubility but also enhances stability and efficacy, thus overall performance in food system (Wen et al., 2016; Chaudhari et al., 2021b). In addition, nanoencapsulation causes controlled release of encapsulated EOs, resulting in their long term effect on food surface without significantly compromising their organoleptic properties (Hosseini and Meimandipour, 2018). Currently, a wide range of encapsulating polymers like chitosan, starch, cyclodextrin, alginate, carrageenans, pullulan, gums, and proteins are available and employed for encapsulation of EOs (Balusamy et al., 2022). Although, AFs contamination is of global concern, their negative impact on human health and life is greater in most of the developing countries of Asia and Africa. The cereal grains and cereal based products of Asian and African countries have been associated with maximum AFs with parallel incidence of hepatocellular carcinoma and aflatoxicosis (Liu and Wu, 2010). Despite being an aflatoxins hotspot, the majority of Asian and African countries are not strictly followed the AFs regulations. Table 1 demonstrates the status of AFs contamination in cereals of Asian and African countries. On the basis of this fact, the review is primarily focused on the AFs contamination of cereals collected from Asian and African countries.
The present review demonstrates a relevant insight on status of AFs contamination in major cereal crops (rice, maize, and wheat) in Asiatic and African countries, their toxic effects on human health, and different analytical techniques for their detection in food system. The review also deals with AFs inhibitory aspect of EOs and their limitations in real food system along with strategies on how to overcome these limitations through nanoencapsulation. Finally, the possible mechanism of action of EOs and their nanoencapsulated nanoformulations at biochemical and molecular levels along with their safety paradigm were reviewed in order to recommend them as novel and smart preservative in food industries and agricultural sectors.

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Section snippets

AFs contamination in rice

Rice is recognized as staple cereal grains over 50% of population playing a significant role in agro-economy of the Asiatic and European countries (Reiter et al., 2009). China occupies the top most position in rice production followed by India, Indonesia, Bangladesh, Myanmar, Vietnam, and Thailand (Reiter et al., 2010). Rice is an important source of carbohydrate, protein, minerals (e.g., Mg, Mn, Se, Fe, and P), vitamins (e.g., vitamin B1, B3, and B9), dietary fibers, and bioactive compounds

Toxic effect of AFs on human health

AFs contamination of cereal grains has always been a prime concern worldwide. Owing to its worldwide occurrence, this mycotoxin is considered as a toxic contaminant of foods by the US-FDA. World Health Organization (WHO) has realized AFs as a high-priority concern and placed them at 6 out of 10 top risk factors. Since the discovery of AFs in 1960 with the death of around 100,000 Turkey birds due to bile duct hyperplasia and acute necrosis caused by feeding of A. flavus contaminated groundnuts,

Methods for detection of AFs in major cereals

In compliance with the food safety concern, the analytical processes for the determination of accurate amount of AFs in cereals are of immense importance. To date, several analytical methods have been acquired to detect and quantify AFs levels in foods. For rapid quantification of AFs, sensitive, reproducible and accurate methods are required (Thanushree et al., 2019). Several extraction and cleanup methods have been used for AF detection, which are completely based on the level of

Essential oils (EOs) as food preservatives against AFs contamination in major cereal grains

Several physical and chemical methods have been used to control fungal and AFs contamination in stored cereal grains. AFs are heat stable and difficult to eliminate by thermal treatments. The temperature for decomposition of AFs varies between 237 and 306 °C. Under dry heat condition, AFB1 is stable below its decomposition point. Moreover, heating at this decomposition temperature degrade the nutritional components and emits acrid smell (Lewis, 2004). The use of ozone to mitigate AFs

Challenges of using EOs as preservatives in food system

Although EOs has been recognized to preserve the postharvest agricultural products; however in real food system, their application is not as easy as approaching. This can be attributed to the number of factors including volatility, intense aroma, poor aqueous phase solubility, showing noxious effect on organoleptic properties of the treated food items, and most importantly susceptibility toward degradation under high moisture, temperature, intense light, pH, and oxygen (Donsì et al., 2011).
For

Nanoencapsulation: an effective approach towards optimization of EOs application

Now-a-days, nanoencapsulation is one of the most rapidly growing technologies in the food sectors. This technology creates a renaissance in the food industry for preservation of stored products with improved shelf-life and nutritional status. Nanoencapsulation refers to the encapsulation of bioactive substance in a nanoscale (1 × 10−9 m) range (Quintanilla-Carvajal et al., 2010). Nanoencapsulation has been deployed to protect the EOs from oxidation, improve aqueous solubility, and biological

Application of EOs nanoformulation against AFs contamination in major cereals

Over the last decades, application of encapsulated EOs against AFs contamination and preservation of food commodities is highlighted in the field of agriculture consistency. The preservation encompasses safety issues, environmental sustainability, and in vivo aspect of EOs which can limitedly interact with food components while protecting the foods through controlled delivery. It is worth noting that only few EO nanoformulations has been developed and recommended against fungi and AFs causing

Mechanisms of action of EOs and their nanoformulations against AFs biosynthesis

Before applying EOs or nanoformulations for their application in food system, it has been recommended to unravel their possible mode of action. At present, no reports available in the literature showing the exact mechanism of action of EOs and their nanoformulations; however some experimental outcomes and hypothesis proposed different biochemical and molecular mode of action against AFs biosynthesis. Some of the well known mechanisms against AFs biosynthesis are discussed below.

Safety aspect of EOs and nanoformulations for practical application

Currently, the United States Food and Drug Administration (FDA) and the European Food Safety Authority (EFSA) have set regulatory approaches for application of EOs in foods. These authorities have approved many EOs under high safety category. On the other hand, only limited informations are available for commercialization of nanoformulation. This can be because these nanoparticles equipped with new physico-chemical properties have extremely small in size and hence may cause toxicity to human

Conclusion and future outlook

Different plant essential oils have shown excellent potentiality to mitigate AFs contamination of major cereals during storage along with the reduction of chances to food toxicity and nutritional deterioration. Nanoencapsulation is confirmed as a novel and smart strategy to improve their bio-efficacy with high stability, and controlled delivery showing greater suitability in food industries. The EOs and their nanoformulations are multifaceted in action targeting carbohydrate metabolism,

CRediT authorship contribution statement

Somenath Das: Writing – original draft, Investigation – Review of literature; Reviewing – original draft. Anand Kumar Chaudhari: Conceptualization, Writing – original draft, Reviewing – original draft, visualization, Supervision.

Funding

This article did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of competing interest

No confliict of interest reported by authors.

Acknowledgements

Somenath Das wishes to thank Head, Department of Botany and Principal, Burdwan Raj College, Purba Bardhaman, West Bengal, India for necessary facilities. Anand Kumar Chaudhari is grateful to Principal, Rajkiya Mahila Snatkottar Mahavidyalaya, Ghazipur, Uttar Pradesh, India for providing necessary supports.

References (269)

  • A.K. Chaudhari et al.

    Nanoencapsulation of essential oils and their bioactive constituents: a novel strategy to control mycotoxin contamination in food system

    Food Chem. Toxicol.

    (2021)
  • A.K. Chaudhari et al.

    Unveiling the cellular and molecular mode of action of Melaleuca cajuputi Powell. Essential oil against aflatoxigenic strains of Aspergillus flavus isolated from stored maize samples

    Food Control

    (2022)
  • A.K. Chaudhari et al.

    Improvement of in vitro and in situ antifungal, AFB1 inhibitory and antioxidant activity of Origanum majorana L. essential oil through nanoemulsion and recommending as novel food preservative

    Food Chem. Toxicol.

    (2020)
  • K. Chen et al.

    Microencapsulation of Sichuan pepper essential oil in soybean protein isolate-Sichuan pepper seed soluble dietary fiber complex coacervates

    Food Hydrocolloids

    (2022)
  • E. Chivandi et al.

    Use of essential oils as a preservative of meat

  • P.J. Cotty et al.

    Influences of climate on aflatoxin producing fungi and aflatoxin contamination

    Int. J. Food Microbiol.

    (2007)
  • C. Cucci et al.

    A portable fluorometer for the rapid screening of M1 aflatoxin

    Sensor. Actuator. B Chem.

    (2007)
  • L. da Cruz Cabral et al.

    Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods

    Int. J. Food Microbiol.

    (2013)
  • S. da Silva Gündel et al.

    Basil oil-nanoemulsions: development, cytotoxicity and evaluation of antioxidant and antimicrobial potential

    J. Drug Deliv. Sci. Technol.

    (2018)
  • M.A. Dadzie et al.

    Distribution of Aspergillus flavus and aflatoxin accumulation in stored maize grains across three agro-ecologies in Ghana

    Food Control

    (2019)
  • S. Das et al.

    Chitosan based encapsulation of Valeriana officinalis essential oil as edible coating for inhibition of fungi and aflatoxin B1 contamination, nutritional quality improvement, and shelf life extension of Citrus sinensis fruits

    Int. J. Biol. Macromol.

    (2023)
  • S. Das et al.

    High speed homogenization assisted encapsulation of synergistic essential oils formulation: characterization, in vitro release study, safety profile, and efficacy towards mitigation of aflatoxin B1 induced deterioration in rice samples

    Food Chem. Toxicol.

    (2022)
  • S. Das et al.

    Fabrication, physico-chemical characterization, and bioactivity evaluation of chitosan-linalool composite nano-matrix as innovative controlled release delivery system for food preservation

    Int. J. Biol. Macromol.

    (2021)
  • S. Das et al.

    Eugenol loaded chitosan nanoemulsion for food protection and inhibition of Aflatoxin B1 synthesizing genes based on molecular docking

    Carbohydr. Polym.

    (2021)
  • S. Das et al.

    Nanostructured Pimpinella anisum essential oil as novel green food preservative against fungal infestation, aflatoxin B1 contamination and deterioration of nutritional qualities

    Food Chem.

    (2021)
  • S. Das et al.

    Fabrication, characterization and practical efficacy of Myristica fragrans essential oil nanoemulsion delivery system against postharvest biodeterioration

    Ecotoxicol. Environ. Saf.

    (2020)
  • S. Das et al.

    Antimicrobial activity, antiaflatoxigenic potential and in situ efficacy of novel formulation comprising of Apium graveolens essential oil and its major component

    Pestic. Biochem. Physiol.

    (2019)
  • S. Das et al.

    Encapsulation in chitosan-based nanomatrix as an efficient green technology to boost the antimicrobial, antioxidant and in situ efficacy of Coriandrum sativum essential oil

    Int. J. Biol. Macromol.

    (2019)
  • S. Das et al.

    Co-encapsulation of Pimpinella anisum and Coriandrum sativum essential oils based synergistic formulation through binary mixture: physico-chemical characterization, appraisal of antifungal mechanism of action, and application as natural food preservative

    Pestic. Biochem. Physiol.

    (2022)
  • S. Das et al.

    Myristica fragrans essential oil nanoemulsion as novel green preservative against fungal and aflatoxin contamination of food commodities with emphasis on biochemical mode of action and molecular docking of major components

    LWT (Lebensm.-Wiss. & Technol.)

    (2020)
  • F.E. Dayan et al.

    Natural products in crop protection

    Bioorg. Med. Chem.

    (2009)
  • R.V. de Barros Fernandes et al.

    Effect of solids content and oil load on the microencapsulation process of rosemary essential oil

    Ind. Crop. Prod.

    (2014)
  • Deepika et al.

    Nanoencapsulated Petroselinum crispum essential oil: characterization and practical efficacy against fungal and aflatoxin contamination of stored chia seeds

    Food Biosci.

    (2021)
  • R. Delshadi et al.

    Micro and nano-encapsulation of vegetable and essential oils to develop functional food products with improved nutritional profiles

    Trends Food Sci. Technol.

    (2020)
  • F. Donsì et al.

    Nanoencapsulation of essential oils to enhance their antimicrobial activity in foods

    LWT (Lebensm.-Wiss. & Technol.)

    (2011)
  • A.K. Dwivedy et al.

    Nanoencapsulated Illicium verum Hook. f. essential oil as an effective novel plant-based preservative against aflatoxin B1 production and free radical generation

    Food Chem. Toxicol.

    (2018)
  • L. Fresco

    Rice is life

    J. Food Compos. Anal.

    (2005)
  • D.R. Georgianna et al.

    Genetic regulation of aflatoxin biosynthesis: from gene to genome

    Fungal Genet. Biol.

    (2009)
  • R. Gharib et al.

    Drug-in-cyclodextrin-in-liposomes as a carrier system for volatile essential oil components: application to anethole

    Food Chem.

    (2017)
  • F. Ghasemi-Kebria et al.

    Aflatoxin contamination of wheat flour and the risk of esophageal cancer in a high risk area in Iran

    Cancer Epidemiol.

    (2013)
  • B. Giray et al.

    Aflatoxin levels in wheat samples consumed in some regions of Turkey

    Food control

    (2007)
  • D. Githang'a et al.

    The effects of aflatoxin exposure on Hepatitis B-vaccine induced immunity in Kenyan children

    Curr. Probl. Pediatr. Adolesc. Health Care

    (2019)
  • S. Gu et al.

    Rapid detection of Aspergillus spp. infection levels on milled rice by headspace-gas chromatography ion-mobility spectrometry (HS-GC-IMS) and E-nose

    LWT (Lebensm.-Wiss. & Technol.)

    (2020)
  • S. Gupta et al.

    Nanoencapsulation of essential oils for sustained release: application as therapeutics and antimicrobials

  • M. Hadidi et al.

    Chitosan nanoparticles loaded with clove essential oil: characterization, antioxidant and antibacterial activities

    Carbohydr. Polym.

    (2020)
  • M.D. Hanvi et al.

    Aflatoxins in maize dough and dietary exposure in rural populations of Togo

    Food Control

    (2021)
  • A.S. Hathout et al.

    Incidence and exposure assessment of aflatoxins and ochratoxin A in Egyptian wheat

    Toxicol Rep.

    (2020)
  • K. Hell et al.

    The influence of storage practices on aflatoxin contamination in maize in four agroecological zones of Benin, West Africa

    J. Stored Prod. Res.

    (2000)
  • J. Adamiec et al.

    Analysis of microencapsulation ability of essential oils during spray drying

    Dry. Technol.

    (2006)
  • S. Ahlberg et al.

    Aflatoxin binders in foods for human consumption—can this be promoted safely and ethically?

    Toxins

    (2019)

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