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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).
Table 1 Basic structure of phenolic acids identified in some
agro-industrial by-products.
Tabla 1.
Estructura básica de ácidos fenólicos identificados en algunos
subproductos agroindustriales.
| Basic structure | ||||||
|---|---|---|---|---|---|---|
| ||||||
| Phenolic acids identified | ||||||
| Compound | R1 | R2 | R3 | -COOH | Source | Reference |
| p-coumaric acid | H | OH | H | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Apple peel | Łata et al. (2009) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| p-hydroxybenzoic acid | OH | H | H | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Avocado peel, pulp and seed | Rodríguez-Carpena et al. (2011) | |||||
| Citrus seed | Moulehi et al. (2012) | |||||
| Caffeic acid | OH | OH | H | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Apple peel | Łata et al. (2009) | |||||
| Citrus seed | Moulehi et al. (2012) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| Chlorogenic acid | OH | OH | H | Esterified | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Apple peel | Łata et al. (2009) | |||||
| Citrus seed | Moulehi et al. (2012) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| Cinnamic acid | H | H | H | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| Ferulic acid | OCH3 | OH | H | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Citrus seed | Moulehi et al. (2012) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| Gallic acid | OH | OH | OH | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Citrus seed | Moulehi et al. (2012) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
| Protocatechuic acid | H | OH | OH | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Rosmarinic acid | OH | OH | H | Esterified | Citrus seed | Moulehi et al. (2012) |
| Syringic acid | OCH3 | OH | OCH3 | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Citrus seed | Moulehi et al. (2012) | |||||
| Vanillic acid | H | OH | OCH3 | * | Potato peel | Onyeneho and Hettiarachchy (1993) |
| Citrus seed | Moulehi et al. (2012) | |||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||
Table 2 Basic structure of flavonoids identified in some agro-industrial
by-products.
Tabla 2. Estructura básica de
algunos flavonoides identificados en subproductos agroindustriales.
| Basic structure of flavonoids | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| ||||||||||
| Flavonoids identified | ||||||||||
| Compound | R3 | R5 | R7 | R2’ | R3’ | R4’ | R5’ | C2-C3 | Source | Reference |
| Flavones | ||||||||||
| Apigenin | H | OH | OH | H | H | OH | H | + | Citrus seed | Moulehi et al. (2012) |
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||||||
| Chrysin | H | OH | OH | H | H | H | H | + | Apple peel | Balasuriya and Rupasinghe (2012) |
| Flavanols | ||||||||||
| (+) catechin | OH | OH | OH | H | H | OH | OH | - | Apple peel | Łata et al. (2009) |
| Avocado peel, pulp and seed | Rodríguez-Carpena et al. (2011) | |||||||||
| Citrus seed | Moulehi et al. (2012) | |||||||||
| Kaempferol | OH | OH | OH | H | H | OH | H | + | Citrus seed | Moulehi et al. (2012) |
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||||||
| Myricetin | OH | OH | OH | H | OH | OH | OH | + | Tomato peel and seed | Valdez-Morales et al. (2014) |
| Quercetin | OH | OH | OH | H | OH | OH | H | + | Apple peel | Łata et al. (2009) |
| Citrus seed | Moulehi et al. (2012) | |||||||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||||||
| Rutin | Gly | OH | OH | H | OH | OH | H | + | Apple peel | Łata et al. (2009) |
| Citrus seed | Moulehi et al. (2012) | |||||||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||||||
| Flavanones | ||||||||||
| Hesperetin | H | OH | OH | H | OH | OCH3 | H | - | Citrus seed | Moulehi et al. (2012) |
| Naringin | H | OH | OH | H | H | OH | H | - | Apple peel | Balasuriya and Rupasinghe (2012) |
| Citrus seed | Moulehi et al. (2012) | |||||||||
| Tomato peel and seed | Valdez-Morales et al. (2014) | |||||||||
(+) double; (-) single.
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).
Table 3 Obtaining phenolic compounds from agro-industrial by-products
through fungal fermentation-assisted extraction.
Tabla
3. Obtención de compuestos fenólicos de subproductos
agroindustriales mediante extracción-asistida por fermentación
fúngica.
| Substrate | Fungi | Fermentation | Relevant results | Reference |
| Black rice bran | Aspergillus awamori and Aspergillus oryzae | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▼ Total phenolic and anthocyanin content, in the order A. awamori > A. oryzae ▲ Total phenolic content obtained by decomposing anthocyanin content ▲ Protocatechuic, OH-benzoic, vanillic, caffeic, p-coumaric and ferulic acids ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• radical-scavenging activity |
Shin et al. (2019) |
| Peanut press cake | Aspergillus awamori | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Total phenolic, flavonoid and tannin content ‘Fungal fermentation effect on bioactivity’ ▲ ABTS•+ and DPPH• radical-scavenging activity ▲ Metal chelating activity |
Sadh et al. (2018) |
| Rice bran extract | Aspergillus oryzae and Rhizopus oryzae | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Ferulic, caffeic, and protocatechuic acids, by A. oryzae ▲ Sinapic, vanillic, caffeic, syringic, protocatechuic, and 4-hydroxybenzoic acids, by R. oryzae ‘Fungal fermentation effect on bioactivity’ ▲ FRAP, by both fungi ● DPPH• radical-scavenging activity |
Razak et al. (2017) |
| Corncob, pea pod, rice straw, sugarcane bagasse, and wheat straw | Aspergillus terreus and Penicillium citrinum | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Total phenolic content, by both fungi ‘Fungal fermentation effect on bioactivity’ ▲DPPH• and NO• radical-scavenging activity, by both fungi ▲ Fe2+ scavenging activity, by both fungi ▲ FRAP, by both fungi |
Chandra and Arora (2016) |
| Plum fruit | Aspergillus niger and Rhizopus oligosporus | SSF | Plum
pomace ‘Fungal fermentation effect on phenolic compounds’ ▲ Total phenolic and flavonoid content, in a similar manner for both fungi ▲ Chlorogenic acid, isoquercetin, and rutin ▼ neochlorogenic acid, isorhamnetin-3-galactoside, Isorha-3-gluc, isorhamnetin-3-glucoside, cyaniding-3-glucoside, and cyaniding-3-rutinoside ● Quercetin-3-galactoside ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• radical-scavenging activity, in a similar manner for both fungi Waste from plum brandy production ‘Fungal fermentation effect on phenolic compounds’ ▲ Total phenolic and flavonoid content, in a similar manner for both fungi ▲ Neochlorogenic acid, chlorogenic acid, isoquercitrin, quercetin-3-galactoside, and rutin ▼ Isorhamnetin-3-galactoside ● Isorhamnetin-3-glucoside, and cyaniding-3-glucoside and cyaniding-3-rutinoside ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• radical-scavenging activity, in a similar manner for both fungi |
Dulf et al. (2016) |
| Substrate | Fungi | Fermentation | Relevant results | Reference |
| Apple pomace | Rhizopus oryzae | SSF and SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Fumaric acid production, by both culture methods |
Das et al. (2015) |
| Orchid | Fusarium avenaceum and Fusarium oxysporum | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Total phenolic content ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• and ABTS•+ radical-scavenging activity, as well as reducing power ▲ Inhibition of Staphylococcus aureus and Bacillus subtilis growth |
Dong et al. (2015) |
| Peanut shell | Inonotus obliquus | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Phenolic compounds such as epigallocatechin-3-gallate, epicatechin-3-gallate, phelligridin G, davallialactone, and inoscavin B ▼ Phenolic acid, including gallic and ferulic acids ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• and •OH radical-scavenging activity |
Xu et al. (2014) |
| Algae | Candida utilis | SCF |
‘Fungal fermentation effect on
bioactivity’
▲ Inhibition of methicillin-resistant Staphylococcus aureus |
Eom et al. (2013) |
| Herbal residues | Aspergillus oryzae | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Gallic acid formation ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• radical-scavenging activity and reducing power ▲ Inhibition of Bacillus cereus, Listeria monocytogenes, Staphylococcus aureus, and Escherichia coli |
Wen et al. (2013) |
| Sugarcane bagasse | Inonotus obliquus | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Phenolic compounds such as epicatechin-3-gallate, epigallocatechin-3-gallate, and phelligridin G ‘Fungal fermentation effect on bioactivity’ ▲ DPPH• and •OH radical-scavenging activity |
Zhu and Xu (2013) |
| Coffee silverskin and coffee grounds | Aspergillus ustus, Aspergillus niger, Neurospora crassa, and Penicillium purpurogenum | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Total phenolic content |
Machado et al. (2012) |
| Pineapple and guava | Rhizopus oligosporus | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Total phenolic content ‘Fungal fermentation effect on bioactivity’ ▼ DPPH• radical-scavenging activity |
Sousa and Correia (2012) |
| Corn cob | Yarrowia lipolytica | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Ferulic acid production |
Huang et al. (2011) |
| Cashew husk | Aspergillus oryzae | SSF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Gallic acid production |
Lokeshwari and Reddy (2010) |
| Citrus peel | Cordyceps sinensis | SCF | ▲ Total phenolic and flavonoids content ▲ ABTS•+ radical-scavenging activity | Choi et al. (2010) |
| Wheat bran | Agrocybe chaxingu, Auricularia auricula-judae, Cordyceps militaris, Hericium erinaceus, and Pleurotus ostreatus | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Ferulic acid production, in the order H. erinaceus > P. ostreatus > C. militaris |
Xie et al. 2010 |
| Valonia acorns extract | Aspergillus oryzae and Trichoderma reesei | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Ellagic acid production, in the order A. oryzae > T. reesei |
Huang et al. (2007) |
| Shrimp and crab shell powder | Monascus purpureus | SCF |
‘Fungal fermentation effect on
bioactivity’
▲ Antimicrobial effect against Bacillus subtilis, Bacillus cereus, Pseudomonas aeruginosa, Staphylococcus aureus and Escherichia coli |
Wang et al. (2002) |
| Tannic acid | Aspergillus awamori | SCF |
‘Fungal fermentation effect on
phenolic compounds’
▲ Gallic acid production |
Seth and Chand (2000) |
(▲), significant increase with respect to the control group; (▼), significant reduction with respect to the control group; (●), without significant differences with respect to the control group.
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).
Table 4 Uses of phenolic compounds as additives for meat and meat
products.
Tabla 4. Usos de compuestos fenólicos
como aditivos para carne y productos cárnicos.
| As an antioxidant additive | |||
|---|---|---|---|
| Phenolic compounds | Conditions | Relevant results | References |
|
Flavonoids: catechin
Phenolic acids: tannic, caffeic, and gallic |
Product: Minced camel meat
Storage: 4 °C for 9 days Addition level: 200 ppm |
▲ Inhibition of lipid oxidation (catechin 72.7%, as well as tannic
95.5%, caffeic 80%, and gallic acids 70% approximately)
▲ Red color, 1 point in sensory score for all phenolic compounds |
Maqsoo et al. (2015) |
| Phenolic acids: caffeic, t-cinnamic, p-coumaric, ferulic, gallic, p-hydroxybenzoic, gentisic, sinapic, and syringic |
Product: Beef
Storage: 4 °C for 6 days Addition level: 0.05 mmol/kg |
▲ Inhibition of lipid oxidation precooked beef in the order sinapic acid > caffeic acid > ferulic acid > gentisic acid > syringic acid > t-cinnamic acid > p-coumaric acid > p-hydroxybenzoic acid | Brettonnet et al. (2010) |
| Phenolic compounds | Conditions | Relevant results | References |
| Flavonoids: quercetin and rutin |
Product: beef patties
Storage: 2 °C for 11 days Addition level: 1 and 5 mM |
▼ L* values in concentration dependence (quercetin 1.9%; rutin 3.0%)
▼ C values in concentration dependence (quercetin 12.3%; rutin 16.6%) ▲ h values in concentration dependence (quercetin 8.9%; rutin 16.4%) ▲ Inhibition of metmyoglobin formation in concentration dependence (quercetin 47.0% approximately; rutin 66.0% approximately) ▲ Inhibition of lipid oxidation in concentration dependence (quercetin 14.3%) ▼ Inhibition of lipid oxidation (rutin -23.8%) |
Bekhit et al. (2004) |
| Flavonoids: quercetin |
Product: cook-chill chicken
Storage: 5 °C for 5 days
Addition level: 1.6% and 3.0% |
▲ Inhibition of lipid oxidation (83.9% and 97.3% in concentration dependence) | Karastogiannidou (1999) |
| Flavonoids: (-)-epicatechin (EC), (-)-epigallocatechin (EGC), (-)-epicatechin gallate (ECG), and (-)-epigallocatechin gallate (EGCG) |
Product: ground white muscle of mackerel
Storage: cooked at 75 °C, 4 °C for 7 days Addition level: EC and EGC (200 mg/kg). ECG and EGCG (300 mg/kg) |
▲ Inhibition of lipid oxidation (EC 40.5%; EGC, ECG, and EGCG 65.5%) | He and Shahidi (1997) |
|
Flavonoids: kaempferol, morin, myricetin,
naringenin, naringin, quercetin, and rutin
Phenolic acids: gallic, caffeic, coumaric, ferulic, syringic, vanillic, sinapic, chlorogenic, and tannic |
Product: cooked ground pork
Storage: 4 °C for 4 weeks Addition level: 30 and 200 ppm |
▲ Inhibition of lipid oxidation in concentration dependence Kaempferol (95.3%), morin (96.4%), myricetin (98.7%), naringenin (3.3%), naringin (2.3%), quercetin (98.9%), rutin (33.0%), as well as gallic (73.5%), caffeic (69.3%), coumaric (54.3%), ferulic (56.6%), syringic (55.3%), vanillic (23.6%), sinapic (38.5%), chlorogenic (35.0%), and tannic (98.9%) acids | Shahidi et al. (1993) |
|
Flavonoids: kaempferol, morin, myricetin,
naringenin, naringin, quercetin, and rutin
Phenolic acids: ellagic, gallic, vanillic, syringic, and tannic |
Product: pork model system, cooked at 75
°C Storage: 4 °C for 3 weeks Addition level: 200 ppm |
▲ Inhibition of lipid oxidation Kaempferol (41%), morin (30%), myricetin (1.0%), naringenin (4.7%), naringin (4.7%), quercetin (97%), and rutin (28.4%), as well as ellagic (99.0%), gallic (44.7%), vanillic (21.3%), syringic (39.6%), and tannic (57.0%) acids | Shahidi et al. (1992) |
| As an antimicrobial additive | |||
| Phenolic compounds | Conditions | Relevant results | References |
|
Flavonoids: catechin
Phenolic acids: tannic, caffeic, and gallic |
Product: Minced camel meat
Storage: 4 °C for 9 days Addition level: 200 ppm |
▲ Inhibition of mesophilic bacteria count, 1 log approximately
(catechin and tannic acids) ▲ Inhibition of psychrotrophic bacteria count, 1 log approximately (catechin, tannic, and gallic acids) |
Maqsoo et al. (2015) |
|
Flavonoids: rutin
Phenolic acids: caffeic acid and p-coumaric |
Product: chicken soup
Storage: 4 and 25 °C for 48 h Addition level: 0.2 mg/mL |
▲ Inhibition of Staphylococcus aureus growth (100% by all phenolic compounds) | Stojković et al. (2013) |
| Phenolic acids: benzoic |
Product: Raw and cooked chicken meat
Storage: 4 and 20 °C for 14 days Addition level: 5000 ppm |
▲ Inhibition of Listeria monocytogenes and growth in
raw and cooked meat (1.2 and 3.5 log, respectively)
▲ Inhibition of Salmonella typhimurium and growth in raw and cooked meat (1.2 log by both) |
Ravichandran et al. (2011) |
|
Flavonoids: Mixture of quercetin and
rutin Phenolic acids: Mixture of gallic and caffeic Mixture of gallic and protocatechuic |
Product: meat model system
Storage: 4 °C for 24 h days Addition level: 100 and 200 mg |
▲ Inhibition of Listeria monocytogenes growth in concentration dependence (mixture quercetin and rutin 6.7 log; mixture gallic and caffeic acids 6.3 log; mixture gallic and protocatechuic acids 3.7 log) | Rodríguez-Vaquero et al. (2011) |
| Phenolic acids: carvacrol and thymol |
Product: bovine meat stake
Storage: 7 °C for 96 h Addition level: <1 µL/mL |
▲ Inhibition of Staphylococcus aureus growth of carvacrol and thymol in combination with organic acids (lactic and acetic) | De Oliviera et al. (2010) |
|
Flavonoids: Mixture of quercetin and
rutin Phenolic acids: Mixture of gallic and caffeic Mixture of gallic and protocatechuic |
Product: meat model system
Storage: 20 °C for 14 days Addition level: 100 and 200 mg |
▲ Concentration- and temperature-dependent inhibition of Escherichia coli growth (mixture of quercetin and rutin 100%; mixture of gallic and caffeic acids 100%; mixture of gallic and protocatechuic acids 50% approximately) | Rodríguez-Vaquero et al. (2010) |
(▲), significant increase with respect to the control group; (▼), significant reduction with respect to the control group.
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.
