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Introduction

Meat and meat products are considered an important source of many essential nutrients in the human diet, including lipids such as fatty acids (mono- or polyunsaturated) and proteins rich in essential amino acids such as isoleucine, leucine, lysine, methionine, phenylalanine, threonine, and valine, which are highly susceptible to oxidation processes (Hammad et al., 2020). Oxidative deterioration of lipids and proteins, and microbial growth are considered the main causes of quality loss in any type of meat or meat products leading to organoleptic and technological changes such as color, odor, flavor, appearance, and texture, as well as water holding capacity and water loss by cooking. In addition, both factors promote nutrient losses and toxic compound formation (Jiang and Xiong, 2016; Aziz and Karboune, 2018). However, the uncontrolled uses of antioxidant and antimicrobial additives to preserve meat and meat products is a practice that generate negative effects on consumer health; thus, strict regulations for their controlled used in foods has been promoted (Poljsak et al., 2013; Aziz and Karboune, 2018).

In previous investigations to reduce lipid and protein oxidation and microbial growth in meat and meat products, extracts rich in phytochemicals have been obtained from plants, herbs, and species, and used instead of synthetic preservatives (Jiang and Xiong, 2016). In addition, the reuse of agro-industrial by-products such as peel pomace and seeds offers an alternative source of additives with antioxidant and antimicrobial properties (Hernández-Carlos et al., 2019).

Moreover, several extraction methods have been developed to obtain bioactive compounds from agro-industrial by-products, such as conventional (maceration and hydrodistillation extraction) and unconventional (ultrasonic, microwave, supercritical fluid, and enzyme extraction) methods. These extraction methods in combination with a solvent system of different polarities, including water, acetone, ethanol, methanol, hexane, and petroleum ether, improve the types of compounds that can be extracted (Azmir et al., 2013; Hernández-Carlos et al., 2019). However, biotechnological methods such as fungal fermentation-assisted extraction (SSF and SCF) has been suggested as an additional alternative to obtain bioactive compounds from agro-industrial by-products (Papaspyridi et al., 2012; Santana-Méridas et al., 2012). In this review, a general description of the uses of fungal fermentation-assisted extraction (SSF and SCF) to obtain phenolic compounds from agro-industrial by-products, and their possible applications as food additives are discussed.

Phenolic Compounds from Agro-Industrial By-Products

The definition of food losses and waste could be associated with a reduction in the availability of food, a decrease in nutritional value and a deterioration in food safety, involving many players in food supply chains, such as farmers and processors. Furthermore, food losses could occur by accidental causes (intrinsic or extrinsic factors), and food waste occurs for reasons of negligence (FAO, 2017). The Mexican normative (NOM-251-SSA1-2009) defines food residue/by-product as ‘waste from processed raw material’. In this regard, the food processing industry generates large amounts of by-products, including pomace, husks, seeds, leaves, stems, and wood (Peanparkdee and Iwamoto, 2019; Rico et al., 2020). In some cases, these by-products are treated to decrease negative environmental impact, making them a useful product with the added benefits of solving a problem and generating additional income (Rico et al., 2020).

Agro-industrial by-products are commonly disposed of, used on-site or used off-site or after pre-treatment. These can be pre-treated by physicochemical (combustion, pyrolysis, and gasification) or biochemical (anaerobic digestion and fermentation) processes, to generate biodiesel and electricity or bio-alcohol and biogas, respectively. In addition, agro-industrial by-products can be pre-treated by bio-reduction to produce animal feed, and by chemical modifications, and by SSF and SCF to obtain bioactive compounds (Santana-Méridas et al., 2012). Thus, agro-industrial by-products are considered a rich source of bioactive compounds, including alkaloids, terpenoids, saponins, essential amino acids and fatty acids, minerals, carotenoids, vitamins, polysaccharides, and phenolic compounds like phenolic acids, and flavonoids (Wijngaard et al., 2012; Azmir et al., 2013; Peanparkdee and Iwamoto, 2019; Rico et al., 2020).

The major by-products of fruit processing are peel and seed, and in a minor proportion, pulp (Santana-Méridas et al., 2012). However, the extraction, identification and uses of phenolic compounds are widely investigated in commercial sectors such as the pharmaceutical, chemical, and food industries (Azmir et al., 2013; Santana-Méridas et al., 2012). In this context, table 1 compiled literature reports of these residues as an important source of phenolic acids, including peel (apple, potato, and tomato), pulp (avocado) and seeds (avocado, citrus, and tomato). In addition, table 2 demonstrate that by-products also are a significant source of flavones, flavonols, and flavanones compounds. It has been reported that phenolic compounds are present ubiquitously in all parts of plants such as wood, leaves, roots, and fruits (Vermerris and Nicholson, 2008; Rico et al., 2020). In this regard, these compounds are commonly trapped or bound to the dietary fiber of plant material, through hydrogen bonds between the phenol hydroxyl group (HO^•) of the phenolic component, hydrophobic interactions, and covalent bonds like ester bond between phenolic acids and polysaccharides (Quirós-Sauceda et al., 2011).

Chemical structure plays a key role in the bioactivity of phenolic compounds, which have been associated with several key factors such as OH-group location in the benzene ring, the substitution patterns by the OH-group (ortho-, meta-, para-, meta-tri-, vic-tri-), the presence of glycosylation, and double bounds in the benzene structure (Vermerris and Nicholson, 2008; Rico et al., 2020). However, the types of phenolic compounds obtained, and their bioactivity are closely associated with the extraction method employed (Azmir et al., 2013).

Extraction Methods

Phenolic compounds are widely found as a mixture of different components in a solid, and for extraction that are dispersed in a liquid phase, which allows their separation from the solid phase. This process is known as liquid-solid extraction, and to increase the diffusion rate of the solvent in the solute and yields, it is necessary to dry and reduce the particle size of the solid or plant material (fruits, leaves, stem, roots, wood, flowers or seeds) (Pinelo et al., 2007; Pronyk and Mazza, 2009; Orphanides et al., 2013).

Furthermore, several methods are frequently employed to obtained phenolic compounds, including rustic methods (extraction by cooking, percolation, and infusion), conventional methods (extraction by maceration, Soxhlet, and hydrodistillation) and unconventional methods, including enzymes-assisted extraction, microwave-assisted extraction, pressurized liquid-assisted extraction, supercritical fluids-assisted extraction, and ultrasound-assisted extraction (Wijngaard et al., 2012; Azmir et al., 2013). However, the solvent type, solvent-solid ratio, number of extractions, pH, temperature, time, vacuum and fermentation process, among other conditions used, influences phenolic yields (Spigno et al., 2007; Ramírez-Rojo et al., 2018).

Fungal Culture Fermentation

SSF involves the fermentation of solids or semi-solids in the absence of water, where the substrate used to be the source of moisture to support microbial growth (Pandey, 2003; Castañeda-Casasola et al., 2018), while in SCF, microorganisms grow submerged with an excess of water and limited oxygen (Castañeda-Casasola et al., 2018). In this context, fungal mycelia is widely produced in SSF using substrates such as grains, sawdust or wood from different plant species (Yang and Liau, 1998). Nevertheless, it has been reported that SCF improves potential advantage than SSF, because inoculums can be uniformly dispersed in the substrate, and the time and/or harvest speed are reduced (Yang and Liau, 1998; Xu and Zhu, 2011; Xu et al., 2015).

Moreover, fungal mycelia production during the fermentation process varies extensively, depending on the species of fungus and environmental or culture conditions used (temperature, initial pH, surface-aeration, aeration rate, rotating speed, and stimulatory agents, among others), which consequently affect phytochemical extraction from the substrate (Yang and Liau, 1998; Xu and Zhu, 2011; Xu et al., 2015).

Phenolic Compounds Extraction by Fungal Fermentation

In relation to the aforementioned, the use of agro-industrial by-products as substrates in combination with fungal fermentation-assisted extraction (SSF and SCF), are considered an alternative method for the extraction of phytochemicals, including triterpenoids, polysaccharides, and phenolic compounds, which could be obtained through agro-industrial by-products (Xu and Zhu, 2011; Xu et al., 2014; Xu et al., 2015; Dey et al., 2016).

In this context, the extraction of phenolic compounds and triterpenoids from citrus peel like pomelo, lemon, orange, and tangerine, through SCF (25 °C at 100 rpm, 28 d) with Antrodia cinnamomea has been reported (Ma et al., 2014). Also, polysaccharide and triterpenoid extraction from citrus peels, including pomelo, lemon, orange, and grapefruit, using SCF (25 °C at 100 rpm, 28 d) with A. cinnamomea was also demonstrated (Yang et al., 2012). Xu and Zhu (2011) , reported the extraction of phenolic compounds with antioxidant properties (DPPH^• and hydroxyl scavenging activity) from ground corn stover by SCF (28 °C at 150 rpm, 12 d) using Inonotus obliquus. In addition, Vattem and Shetty (2002) demonstrated the extraction of phenolic compounds such as ellagic acid, resveratrol and rosmarinic acid with antioxidant properties (antiradical DPPH^• and β-carotene antioxidant protection factor) from cranberry pomace by SSF (28 °C, 16 d) using Rhizopus oligosporus.

Additionally, table 3 compile literature reports focused on the extraction of phenolic compounds with antioxidant and antibacterial properties, from agro-industrial by-products using fungal fermentation-assisted extraction (SSF and SCF). Mycelial growth during fungal fermentation depends on the nutrient supply (nitrogen, phosphorus and carbon) and any type of energy source or substrate, as well as substrate digestibility, which are essential for extraction of bioactive secondary metabolites (Hölker et al., 2004).

Likewise, an increase in enzyme production (lipases, xylanase, pectinase, proteases, cellulolytic, and ligninolytic enzymes) during fungal fermentation has been demonstrated (Hölker et al., 2004; Sadh et al., 2018). The enzymatic hydrolysis produced during fungal fermentation increase the extraction of phenolic compounds, such as p-coumaric, caffeic, chlorogenic, ferulic, protocatechuic, sinapic, syringic, and vanillic acids, quercetin, and rutin. Also, improve antioxidant activity like antiradical (DPPH^• and ABTS^•+ activity), chelating metal properties, ferric reducing antioxidant power, and nitric oxide chelating properties. As well as antimicrobial activity by microbial growth and foodborne pathogens reduction (Hölker et al., 2004; Das et al., 2015; Dong et al., 2015; Dulf et al., 2016; Razak et al., 2017; Sadh et al., 2018; Shin et al., 2019). Thus, the enzymatic hydrolysis produced during fungal fermentation appears to be an attractive strategy to extract phenolic compounds with potential uses as food additives (Papaspyridi et al., 2012).

Phenolic Compounds as Possible Meat and Meat Product Additives

The NOM-213-SSA1-2002 define a ‘food additive’ as ‘those substances, which added directly to food and beverages during their elaboration, provide or intensify aroma, color, and flavor, to improve stability and conservation’. Also, the FDA (2008) indicate that a ‘Food Additive’ is ‘any substance that when use directly or indirectly, become a component or otherwise affect the characteristics of any food, including any substance intended for use in packaging, production, manufacturing, processing, preparation, treatment, transportation or storage of food; and including any source of radiation intended for such use’. The Codex Alimentarius (2017) defined it as ‘any substance that, regardless of its nutritional value, is intentionally added to a food in controlled quantities for technological purposes’.

Moreover, in the meat and meat products industry, additives are widely employed for preservative purposes (i.e., as antioxidants and antimicrobials). An antioxidant additive, is defined as a ‘substance added to foods to prevent the oxygen present in the air from causing undesirable changes in flavor and color’ (USDA, 2015). In another context, an antimicrobial additive, is defined as ‘a substance that meets the definition of food additive and is used to control microorganisms such as bacteria, viruses, fungi, among others, in food or food contact items’ (FDA, 2008).

The following is a list of additives commonly used in meat and meat products as preservatives are: ɑ-tocopherol (E307), acetic acid (E260), ascorbic acid (E300), citric acid (E300), erythorbic acid (E315), fumaric acid (E297), lactic acid (E270), sorbic acid (E200), tartaric acid (E334), sodium ascorbate (E301), calcium ascorbate (E302), sodium benzoate (E211), butylhydroxyanisole (E320), and butylhydroxytoluene (E321). Also, calcium carbonate (E170i), sodium citrate (E330), potassium citrate (E332), tricalcium citrate (E333iii), trisodium citrate (E331iii), isopropyl citrate (E384), sodium diacetate (E262ii), sodium erythorbate (E316), ethyl lauroyl arginate (E243), propyl gallate (E310), nitrite/sodium nitrate (E250 and E252), tert-butylhydroquinone (E319), potassium sorbate (E202), among others (NOM-122-SSA1-1994; FDA, 2004; European Commission, 2014; FAO, 2018). The preservative compounds mentioned above have phenolic groups in their structure, which in phenolic compounds (phenolic acid and flavonoids) are widely associated with their antioxidant and antimicrobial activity (Sova, 2012).

Moreover, extensive research has demonstrated that lipid oxidation and microbial growth, are the main factors involved in the quality loss of raw and cooked meat products. These factors lead to the formation of some compounds that affect sensory attributes, including changes in texture, odor, flavor, and color, which consequently have an adverse effect on meat acceptability and meat purchase intention (Faustmant et al., 2010; Aziz and Karboune, 2018). Therefore, there have been efforts to obtain antioxidant and antimicrobial compounds from natural sources, including agro-industrial by-products (Faustmant et al., 2010; Jiang and Xiong, 2016).

Table 4 shows the possible uses of phenolic compounds, obtained by SSF and SCF using agro-industrial residues as substrate, including as meat and meat product additives. In this context, it has been demonstrated that phenolic compounds and flavonoids can preserve raw and cooked meat and meat products from different species (beef, camel, chicken, and pork), against undesirable changes caused by lipid oxidation and microbial growth during refrigerated storage (Stojković et al., 2013; Maqsoo et al., 2015). Furthermore, phenolic compounds can act through two pathways: (1) by breaking chain reactions triggered by free radicals, which implies hydrogen atom transfer (HAT), then electron transfer followed by a proton transfer mechanism (SET-PT) and sequential proton-loss electron-transfer (SPLET), and (2) by reducing metals such as copper (Cu²⁺) and iron (Fe³⁺) (Marković et al., 2012). Additionally, phenolic compounds can act against nucleic acid and protein synthesis and alter the components of cellular membranes (Cushnie and Lamb, 2005).

Conclusion

The agro-industrial by-products are an important source of phenolic compounds, including phenolic acids and flavonoids. The uses of agro-industrial residues as substrates (seeds, pulps, and peels) during fungal fermentation-assisted extraction (SSF and SCF), can be used as an alternative or complementary strategy to obtain phenolic compounds like rustic, conventional and unconventional extraction methods. These compounds could be use as antioxidant and antimicrobial additives to extend the shelf life of raw and cooked meat and meat products from different species (beef, camel, chicken, and pork) during refrigerated storage.

Acknowledgements

The authors gratefully acknowledge Cátedras CONACYT for the fellowship of the project (#739).

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Author notes

*Autor para correspondencia: Rey David Vargas Sánchez. Correo electrónico: rey.vargas@ciad.mx

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