NATURAL TANNINS WOOD EXTRACTS AS POTENTIAL

Review Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Natural Tannin Wood Extracts as a Potential Food Ingredient in the Food Industry Silvia Molino,† Natalia Andrea Casanova,‡ Jose ́ Á ngel Rufiań Henares,*,†,§ and Mariano Enrique Fernandez Miyakawa‡,∥

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†

Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain ‡ Instituto de Patobiología, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria, Buenos Aires C1033AAE, Argentina § Instituto de Investigación Biosanitaria (ibs.GRANADA), Universidad de Granada, 18071 Granada, Spain ∥ Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires C1425FQB, Argentina ABSTRACT: Wood extracts are one of the most important natural sources of industrially obtained tannins. Their use in the food industry could be one of the biggest (most important) recent innovations in food science as a result of their multiple (many) possible applications. The use of tannin wood extracts (TWEs) as additives directly added in foods or in their packaging meets an ever-increasing consumer demand for innovative approaches to sustainability. The latest research is focusing on new ways to include them directly in food, to take advantage of their specific actions to prevent individual pathological conditions. The present review begins with the biology of TWEs and then explores their chemistry, specific sensorial properties, and current application in food production. Moreover, this review is intended to cover recent studies dealing with the potential use of TWEs as a starting point for novel food ingredients. KEYWORDS: tannins, wood extracts, foods, food supplements, gut microbiota

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INTRODUCTION In 1796, Seguin proposed the term “tannin” to define the extractable substance used to convert animal skin to leather, demonstrating the capacity of these compounds to precipitate gelatin from solution.1 Bate-Smith and Swain in 1962 gave a more specific description of tannins as “water-soluble phenolic compounds having molecular weights between 500−3000 Da and, besides giving the usual phenolic reactions, they have special properties such as the ability to precipitate alkaloids, gelatin and other proteins”.2 According to their structural characteristics (Figure 1), tannins are divided into gallotannins, ellagitannins, condensed tannins, complex tannins, and phlorotannins (from brown algae).3,4 The first two groups are traditionally known as hydrolyzable tannins, because these compounds are hydrolyzed by weak acids to yield sugar (mainly glucose) and acid derivate and gallic and ellagic acids, respectively. Complex tannins are composed by a unit of hydrolyzable tannins bound to a catechin unit.3 Meanwhile, condensed tannins, also referred to as proanthocyanidins, are oligomers or polymers of flavan-3-ols. Tannins are widely distributed in many plant species because they are present in the leaves, buds, stem, bark, wood, roots, fruits, and seeds.5 These compounds are normally present in fruits and vegetables included in the human diet. Nevertheless, only a minority of plants consumed by humans constitute a major source of tannins, because the parts containing these compounds are a small fraction of the edible part (e.g., walnut skin) or because they are not eaten at all. For this reason, tannins extracted from wood and bark, normally applied in the process of leather tanning, are now finding new © XXXX American Chemical Society

relevant applications in the food sector, among others. Furthermore, there is an increasing market demand for more “natural” and “ecological” food products and production processes and a reduced demand for products of chemical synthesis. As a result of their unique chemical properties, tannin wood extracts (TWEs) are used to improve food quality by several modes of actions and in a wide variety of products. Astringency and bitterness are the most recognized and sought-after properties of tannins for food quality, i.e., the perceived mouthfeel occurring in food products, such as aged wines and spirits. Indeed, tannic acid (a commercial available gallotannin) is a European Union (EU) recognized food flavoring.6 On the other hand, new tendencies of food processing are driving the application of green technologies, including the concept of natural food preservatives. In this sense, advantage may be taken of the well-known antioxidant4 and antimicrobial5 properties of tannins to ensure minimal food processing and also protect from spoilage and contamination. Tannin compounds can have a large influence on the nutritive value of many foods eaten by humans as well as feedstuffs eaten by animals. They are considered as bioactive compounds as a result of their capacity to modulate metabolic Special Issue: Advances in Polyphenol Chemistry: Implications for Nutrition, Health, and the Environment Received: Revised: Accepted: Published: A

January 25, 2019 May 17, 2019 May 21, 2019 May 22, 2019 DOI: 10.1021/acs.jafc.9b00590 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry

Figure 1. Classification of tannins.

processes and promote health.7 Different TWEs showed strong biological activities in the form of antitumor, antimutagenic, antidiabetic, antiproliferative, antibacterial, and antimycotic properties, in both humans and animals. For this reason, the tannin−food interaction could be exploited in food systems to benefit human nutrition and health, with technological applications to deliver specific compounds8 or exert specific functions (e.g., to reduce the caloric impact of foods).9 Wood tannins satisfy the characteristics that Lorenzo et al.10 established to be used as food additives. These compounds are economical, ensure stability during processing, extend shelf life, are compatible with foods, and can be effective at low concentrations (to affect the sensory properties of food).10 TWEs are therefore a novel product of interest for not only consumers but also food producers and product developers. The present review focused on all of the results obtained regarding the potential use of TWEs as a starting point for novel food ingredients.

With hydrolyzable tannins, free ellagic and gallic acids (from ellagitannins and gallotannins, respectively) are released after acid hydrolysis. Konishi et al. demonstrated that gallic acid is permeated via the paracellular route in Caco-2 cells.14 No ellagitannins in intact form were detected in human plasma samples, while ellagic acid was detected in human plasma in low concentrations after oral administration.15 A large part of ingested tannins reaches the large intestine, where the gut microbiota converts them into metabolites. More specifically, 5-(30-hydroxyphenyl)-valerolactone, 3-(3hydroxyphenyl)-propionic acid, 3,4-dihydroxyphenylacetic acid, and 3-hydroxyphenylacetic acid are produced from the catabolism of monomeric and oligomeric condensed tannins. Ellagic acid is converted into urolithins.16 Once metabolic products have crossed the intestinal barrier, they reach the liver through the portal vein, where they are further metabolized, to form O-glucuronides, sulfate esters, and O-methyl ether; no free aglycones are found in plasma.13,17 The new conjugates can reach the bloodstream or return to the intestinal tract through bile excretion. Here, gut microbiota may exert enzymatic activity to deconjugate O-glycosides and O-glucuronides and further metabolize the compounds. Several studies reported that the bioactivity of tannin metabolites could differ or be weakened from the functions exerted by parent compounds. Urolithins were determined to have higher physiological activity than ellagitannin and ellagic acid.16

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DIGESTION OF TANNINS The first requisite for a bioactive compound is to be absorbed after digestion or to be unabsorbed and then reach the colon, where it can be further metabolized by the gut microbiota. The absorption and metabolism of each type of tannin differs greatly, and although the gut microbiota has a clear impact on the metabolism of plant tannins, to date little is known of its specific effects.11 As a result of the structure and buffering effect of the food bolus in the gut, condensed tannins are not degraded in acidic conditions of the stomach.12 As a result of digestion in the small intestine, smaller compounds can be more readily absorbed (monomeric, dimeric, and trimeric catechins), which suggests that polymerization impairs intestinal absorption.13

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BIOLOGICAL EFFECTS OF TANNINS The biological effects of tannins, including their antioxidant and radical scavenging, antimutagenic or antigenotoxic, antimicrobial, metabolic, or immunomodulatory properties, among others, are closely related to their chemical structure and degree of polymerization. Moreover, the outcome depends B

DOI: 10.1021/acs.jafc.9b00590 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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The antidiabetic potential of a TWE (Pterocarpus marsupium wood extract) in rats was reported by Mishra et al.36 In particular, among other compounds, the authors identified an active antidiabetic component in epicatechin, which improved the oral glucose tolerance post-sucrose load and exerted regenerative activity on pancreatic β cells. Normal and streptozotocin-induced diabetic rats treated with wood extracts presented a decline in blood glucose and increased insulin levels in diabetic rats. Subsequent results confirm the effects of P. marsupium wood extract, showing dose-dependent antioxidant, antidiabetic, anti-inflammatory and analgesic activities in a mice model.37 Likewise, cinnamtannin, condensed tannin from bay wood, also showed antidiabetic properties by decreasing some complications in type 2 diabetes, such as platelet hyperactivity and hyperaggregability, which lead to the development of micro- and macroangiopathy.38 Other TWEs (bark and wood extracts of Castanea sativa) have been shown to behave as cardioprotective agents in rat culture cells,39 to have antispasmodic action induced by modulation of cholinergic receptors and calcium channels,40 to prevent DNA damage, reducing oxidative stress in pigs,41 and to afford neuroprotection when added to neuroblastoma cells before oxidative-stress-mediated damage.26 Antimicrobial Activity. There are several mechanisms involved in tannin antimicrobial activity, including metal chelation required from microbial growth (mainly iron), interactions with proteins and cell wall/membrane (leading to structural destabilization), and enzyme inhibition.5 Grampositive bacteria are more sensitive to tannins; however, these effects have been proven against Gram-negative bacteria, viruses, and parasites (Table 1). Sweet chestnut (Castanea sativa) and red quebracho ( Schinopsis lorentzii) are representative commercial sources of hydrolyzable and condensed tannins, respectively. Commercial tannins of wood extracts and castalagin (an isolated tannin from chestnut) had antimicrobial effects against food-borne pathogenic bacteria, such as Campylobacter jejuni,42 Salmonella typhymurium,43 Staphylococcus aureus, Salmonella spp., enteropathogenic Escherichia coli, and Vibrio spp.44 Inhibition of S. typhymurium growth in vitro by commercial tannins from chestnut was observed, with no effect in fecal excretion or colonization of internal organs in a pig model.45 Likewise, Min et al.46 reported that hydrolyzable tannins exerted in vitro bacteriostatic and bactericidal effects against E. coli O157:H7 and reduced the shedding of generic E. coli in steers fed tannins. Another Gram-positive bacterium, Clostridium perfringens, was inhibited in a dose-dependent pattern by both types of tannins and their combination, also having antitoxin effects.47 Comparative analysis showed that chestnut-derived tannins exerted a stronger antibacterial effect. These results are in accordance with those obtained by others who observed that chestnut and quebracho extracts were efficient in controlling the proliferation of C. perfringens in vivo and reducing its excretion and the severity of lesions in treated animals with respect to the infected control.48 Antiviral effects of chestnut and quebracho wood extracts49 and isolated tannins of chestnut,50 such as castalagin and vescalagin, were described. Quebracho tannins also exhibited inhibitory effects against parasites, such as helminths51−53 and coccidia.54 Many other tree species were studied in relation to their antimicrobial properties. Tannins from wood and bark of Pterocarpus marsupium,37 Punica granatum, Elaeocarpus sylvestris var. ellipticus,44 Uncaria tomentosa,27 and Ceriops

upon not only the species of plant but also the specific part from which they were derived.4,18,19 Several studies described the beneficial effects of tannin-rich fractions; however, results are sometimes controversial as a result of the use of nonstandardized extracts and techniques.19 Furthermore, information on the activities of tannins derived exclusively from wood is relatively less abundant or accessible from the literature. Antioxidant and Antitumor Properties. At the present moment, the mechanisms by which tannins exert their antioxidant and antitumor activities are not fully elucidated. Some authors suggest that these effects are mainly due to direct impact on cell structures, the modulation of pro-/ antioxidant enzymes (such as superoxide dismutase, catalase, and lipoxygenases), and the scavenging of hydroxyl, superoxide, and peroxyl radicals, which, in turn, decrease protein and lipid oxidation and normalize cell redox balance.20−23 In the case of the antioxidant effects of proanthocyanidins, isolated compounds, such as procyanidins B1 and B3, exhibited stronger antioxidant activity than ascorbic acid and αtocopherol. An increase in antioxidant ability is observed with the low degree of polymerization of proanthocyanidins.24 Tannins derived from wood (casuarictin, castalagin, vescalagin, cinnamtannins B-1 and B-2, grandinin, and epicatechin-3-O-gallate) and proanthocyanidins and procyanidin-rich fractions inhibit cell proliferation and induce apoptosis of neoplastic cells25−27 and prevent this mechanism in normal cells by reducing caspase activation and translocation.28,29 Physiological and Metabolic Activities. Relatively high tannin concentrations may result in potential gastrointestinal problems as a result of the great affinity of tannins for proteins, which may result in an inhibition of digestive enzymes.30,31 Therefore, the property of tannins to bind proteins could interfere with the absorption of nutrients, such as proteins, carbohydrates, and metals.24 However, the ability of tannins to bind gluten proteins could be exploited as a potential therapeutic approach for celiac disease.32 Dias et al.33 revealed that tannins (in particular, epigallocatechin-3-gallate) could have a potential role in modulating some molecular processes associated with celiac disease. In their in vitro transwell cell experiments on Caco-2, they found that epigallocatechin-3gallate reduced the translocation of the immune-reactive peptide involved in celiac pathogenesis, across the simulated intestinal epithelial barrier. In addition, in vitro studies showed the ability of procyanidin B3, procyanidin trimers, procyanidin tetramers, and an oligomeric mixture of high-molecular-weight procyanidins to bind to wheat gliadins.34 Tannins also exert antidiabetic potential as a result of the following: (i) The improvement of the levels of insulin and pro-insulin in blood: The affinity of tannins to bind polysaccharides determines a delay and a decrease of availability of glucose in the gastrointestinal tract. Moreover, several studies reported the potential of inhibition of α-amylase and α-glucosidase activities by hydrolyzable tannins and condensed tannins, respectively.4 (ii) The insulin-like effect on insulin-sensitive tissues: Procyanidins can act on certain specific components of the intracellular insulin-signaling pathway.35 (iii) The regulation of the antioxidant environment of pancreatic β-cells: It is assumed that oxidative stress plays a role in diabetes, because it determines apoptosis of β cells. Furthermore, the expression of genes related with antioxidant enzymes in the pancreas is low. The high antioxidant capacity of tannins can counteract the pathogenesis of diabetes mellitus.4,18 C


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Herein, the compounds are metabolized by microorganisms, resulting in metabolites with different bioavailability, activity, or functional effect compared to the parent molecule. On the other hand, tannins can modulate gut microbial composition and function, selectively inhibiting pathogens and promoting growth of beneficial bacteria.62 Some studies demonstrate the causal effect of gut microbes in chronic pathologies. Tannins may have an indirect impact in these diseases. Mechanisms of these actions are still not completely understood, but it is highly likely that their dietary intake can be beneficial for human health and immunity.63 Ellagitannins from extracts of berries resulted in strong inhibitory compounds, which were effective against Staphylococcus bacteria, but they did not alter probiotic strains, i.e., Lactobacillus rhamnosus.64 The study of Masumoto et al.65 found that, in mice fed a high-fat/highsucrose diet, non-absorbable apple procyanidins induced a decrease of the Firmicutes/Bacteroidetes ratio. On the other hand, the realtive abundances of Verrucomicrobia and, in particular, Akkermansia muciniphila have been recently investigated as markers of a healthy gut because they possess anti-inflammatory properties, increase insulin sensitivity, and boost the gut barrier function.65 Short-chain fatty acids (SCFAs) are produced by metabolism of the gut microbiota and play a critical role in human health. SCFAs can modulate cell metabolism in humans and fine-tune the immune response, in addition to contribuing as an energy source.66 In the study of Molino et al.,67 the application of their in vitro digestion and fermentation model in which quebracho and chestnut TWEs were used gave increased production of SCFAs. A similar release of total SCFAs by grape and apple proanthocyanidins was described by Aura et al.68 Tannins have been proposed as prebiotic subtrates for the gut microbiota as a result of their stimulation of SCFA production, growth-promoting effects for beneficial bacteria, and/or activation of their metabolic functions.16,69 In addition, the combination of proanthocyanidins and polysaccharides (such as pectin) present in the food matrix could result in an additive effect.68 Proanthocyanidins associated with polysaccharides, poorly bioavailable in the upper intestine, reach the colon, where the gut microbiota converts these fermentable substrates into active metabolites, potentially absorbable.31 The conversion rate increases when proanthocyanidins are associated with the food matrix, likely because polysaccharides act as a nutrient for microbiota, which metabolizes more efficiently those proanthocyanidins linked to polysaccharides. Bazzocco and co-workers31 found that proanthocyanidin chain length determines the competition mechanism between the inhibition of microbial enzymes by these molecules and the capacity of colonic microorganisms to metabolize such tannins. With regard to ellagitannins in combination with fructooligosaccharides, the literature is unclear as to whether their role is beneficial or counterproductive in the production of SCFAs in animals.16 Finally, some studies reported that tannins can also promote the adhesion and colonization of probiotic bacteria, resulting in an ulterior beneficial effect. Kawabata and co-workers found that procyanidins and epigallocatechin induced the adhesion of lactic acid bacteria in an in vitro intestinal epitelial tissue model.16 All of the mentioned results suggest a bidirectional relationship between tannins and gut microbiota.

Table 1. Antimicrobial Effects of Tannin Wood Extracts plant species Anadenanthera colubrine (bark) Castanea sativa (wood and bark)

microorganism targeted

57

Clostridium perfringens

47 and 48 43 and 45 42 46

Salmonella typhimurium

Ceriops decandra (wood and bark) Combretum hartmannianum (bark) Commiphora leptophloeos (bark) Elaeocarpus sylvestris var. ellipticus (wood) Myracrodruon urundeuva (bark) Pterocarpus marsupium (wood) Punica granatum (rind) Quercus robur (wood) Schinopsis lorentzii (wood)

Terminalia spp. (wood and bark) Ulmi macrocarpa (cortex) Uncaria tomentosa (wood and bark) Walsura robusta (wood) Xanthoceras sorbifolia (wood) Terminalia spp. (wood and bark)

reference

Pseudomonas aeruginosa

Campylobacter jejuni Escherichia coli and Escherichia coli O157:H7 Staphylococcus aureus, Vibrio spp., Salmonella spp., and enteropathogenic Escherichia coli avian reovirus and metapneumovirus herpes simplex virus Bacillus subtilis, Bacillus coagulans, Escherichia coli, and Proteus vulgaris Porphyromonas gingivalis

44 49 50 55 59


57

Staphylococcus aureus, Vibrio spp., Salmonella spp., and Escherichia coli

44


57

Staphylococcus aureus and Bacillus cereus

37

Staphylococcus aureus, Vibrio spp., Salmonella spp., and Escherichia coli herpes simplex virus

44

Clostridium perfringens Salmonella typhimurium Campylobacter jejuni helminths Eimeria spp. avian reovirus and metapneumovirus Porphyromonas gingivalis

47 43 42 51−53 54 49 59

herpes simplex virus type 2

61

Porphyromonas gingivalis and Treponema denticola Staphylococcus aureus, Enterococcus faecalis, and Pseudomonas aeruginosa Escherichia coli O157:H7

58

human immunodeficiency virus

60

50

27 56

decandra55 showed antibacterial activity against Enterococcus faecalis, S. aureus, and Bacillus spp. With regard to Gramnegative bacteria, condensed and hydrolyzable tannins isolated from woody plants displayed antimicrobial effects against E. coli and E. coli O157:H7,55,56 Pseudomonas aeruginosa,27,57 Proteus vulgaris,55 and Porphyromonas gingivalis.58,59 Antiviral activities were also established for tannins derived from wood of Xanthoceras sorbifolia,60 Quercus robur,50 and Terminalia spp.61 Impact on Gut Microbiota. Tannins exert local and systemic effects owing to interactions between absorbable tannins (low molecular weight) and their metabolites with tissues.21 Non-absorbable tannins (high molecular weight) reach the colonic gut microbiota, exhibiting a prebiotic effect. D


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Figure 2. Scheme of tannin−protein and tannin−polysaccharide interactions.

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TANNIN INTERACTIONS WITH MACROMOLECULES: RELATIONSHIP WITH SENSORY PROPERTIES Tannins−Polysaccharides. Interactions between tannins, particularly condensed tannins, and polysaccharides have been studied and widely demonstrated in the context of clarification and astringency control of beverages.70 In fact, the most investigated models for tannin−polysaccharide interactions are represented by grapes, apples, and pears (rich in proanthocyanidins) used for the production of ciders and wine.70,71 Proanthocyanidin−polysaccharide associations are spontaneous and quick and direct binding events that occur during vegetable and fruit processing.71,72 These bindings are mediated by hydrogen bonds and hydrophobic interactions, which are boosted by ionic strength and a lower temperature.73 Moreover, a high degree of polymerization corresponds to higher affinities.73 The complexation mechanisms are similar to the aggregation between proanthocyanidins and proteins; nevertheless, both phenomena are distinguished by different kinetics and colloidal consequences.74 Tannins−Proteins. Tannins have a distinctive tendency to bind to proteins, by establishing cross-links with the implication of a different nature of bonds. The main driving forces involved are hydrophobic interactions and hydrogen bonds.75 Model studies suggested that three specific steps determine the combination between tannins and proteins (Figure 2). (1) The earliest interactions are characterized by

hydrogen bonds and hydrophobic interactions, resulting in the generation of protein−tannin complexes. Hydrophobic interactions comprise entropy-driven van der Waals forces, while hydrogen bonds are enthalpy-driven electrostatic interactions. Tannins are able to bind to multiple sites on the protein, leading to a condensation of the protein−tannin complex and resulting in a spherical structure.75,76 (2) Cross-links between protein−tannin complexes determine a self-association, with the formation of bigger structures.75,76 (3) The association of the large aggregates produces colloidal size particles, which induces the precipitation of protein−tannin complexes.75,76 Protein and tannin binding occurs in a specific and selective way. Some factors related to proteins may influence such interactions: protein size, charge, side chains, and conformation. Independent from the protein structure, both tannin molecular weight and degree of galloylation enhance their affinity for proteins, probably because tannin size determines the number of interaction sites. Nevertheless, larger tannin structures can cause steric hindrance and impede access to binding sites, limiting solubility.77 Polysaccharides (i.e., arabic gum, pectin, gellan, polygalacturonic acid, and xanthan) could obstruct the protein−tannin interaction, preventing their precipitation.78 Two mechanisms have been proposed to describe the inhibition of protein− tannin interactions (Figure 2): (i) formation of a ternary soluble complex among protein, tannin, and polysaccharide79 or (ii) encapsulation of tannins by polysaccharides, competing with protein aggregation.80 However, some authors showed E


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Journal of Agricultural and Food Chemistry that the presence of polysaccharides, in particular mannoproteins, inhibits the evolution of tannin aggregate particle size but not their generation.81 In the mouth, salivary tannin−protein interactions are influenced by the concentration of the proteins.82 Several environmental factors, including temperature, pH, and ionic strength, influence the formation of salivary−protein aggregates or their precipitation.82 In saliva, among numerous proteins, there is a predominance of proteins rich in proline (PRPs) and in minor proportion glycine and glutamic/ glutamine residues.83 PRPs are very efficient in complexing tannins and, in particular, the presence of a repeated proline region, increasing binding affinity. It has been reported that histatins 3 and 5, other salivary proteins, increase precipitation of condensed tannins more than histatin 1 as a result of a different content of histidine and phosphoserine.84 Moreover, a study reported that quebracho tannins and tannic acid are more efficiently precipitating salivary histatin 5 than PRP-1, at pH 7.4.75 The tannin−protein binding does not impair the bioavailability of tannins, and some authors suggested proteins as carriers of these bioactive compounds.85,86 Astringency and Bitterness. Tannins contribute directly to several sensorial aspects of food, including astringency and bitter taste. Astringency has been defined as the taste experience corresponding to dryness and puckering mouthfeel all over the oral surface.87 This complex group of sensations results from the interaction between tannins and salivary proteins, leading to physical changes in the salivary mixture, particularly a deep decrease in viscosity. The mechanoreceptors perceive the sensation of roughness as the food comes in contact with the tongue, while the tongue is moving over the palate. This sensation is determined by two types of mechanisms: (i) decrease of saliva viscosity and increase of friction as a result of the interaction between tannins and salivary protein-rich proteins and (ii) perception in the oral texture of the protein−tannin precipitates as discrete particles. The last process determines a drying and grainy sensation that differs on the concentration and dimension of the colloidal aggregates, in addition to the hardness of the precipitate. Astringency is influenced by tannin structure and degree of polymerization, because high-molecular-weight structures favors the interaction with salivary proteins. Several studies highlighted that proanthocyanidins are the major contributors of astringency intensity, while smaller compounds are not considerably astringent, probably because small dimensions do not allow for the formation of cross-linking bonds.88,89 Nevertheless, some authors stated a relationship between low-molecular-weight compounds present in food that could play a role in astringency perception.90,91 As mentioned above, the presence of specific amino acids, such as proline and hydroxyproline, impacts the perception of astringency, being a target for proanthocyanidin reactions.77,92 Some authors highlighted that the astringent sensation is not always necessarily correlated to the precipitation of tannin− protein complexes. Indeed, the study of Obreque-Slier et al.93 showed that soluble aggregates of hydrolyzable tannins and gelatin were perceived with a marked astringent mouthfeel by sensory panelists, but in vitro, they failed to determine precipitation. Moreover, it has been reported that unbound remaining tannins could interact with the epithelial cells of the oral surface, resulting in an increased perceived astringency, especially at lower pH.94

Some external factors could also impact the astringent mouth feel (such as acidic pH) that determines higher puckering sensation.95 The presence of polysaccharides in the food matrix leads to a smoothing of the astringency by inhibiting protein−tannin interactions. In fact, some studies showed that the presence of water-soluble pectin could prevent the formation of aggregates between tannins and proteins in the mouth, determining an altered astringency response.96,97 In this sense, polysaccharides could be applied in oenology to improve astringent sensation, conversely giving an increase of roundness and sweetness of wine.98 In the mouth, tannins could also interact with taste receptors and give a bitter flavor to food. Soares et al.99 showed that bitterness is a matter of the combinatorial pattern of TAS2R activation. More specifically, the concentration of natural tannins in food is responsible for a different grade of bitter taste by specifically activating TAS2R5 (condensed tannins) or TAS2R7 (hydrolyzable ellagitannins). In general, it is wellaccepted that larger tannins are less bitter than those with a smaller structure, even though some authors obtained conflicting results.99 The bitterness is influenced by different factors, and the evaluation of bitterness may vary based on the type of assay. The absence of salivary proteins in in vitro taste receptor activation assays could determine discrepancies with the taste threshold of sensory assays. 99 The authors hypothesize that the presence of saliva (i.e., salivary proteins) could interact with tannins and induce an in vivo decrease of perceived bitterness. The bitter-making potential of tannins could also be reduced by proteins present in food.100 Finally, the interaction with salivary proteins could reduce the activation of TAS2Rs and determine a perception more astringent than bitter of some tannins.101

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FOOD INDUSTRY APPLICATIONS Wine. Natural occurring tannins contribute to the overall taste and mouthfeel in hydroalcoholic beverages, such as wine and beer, giving bitterness and astringency. These compounds are naturally present in raw ingredients, while the addition of exogenous tannins is a longstanding technological practice, applied at different times and in a number of forms during the processes of production. Exogenous tannins (added to improve food quality) can be added in the form of wood chips, mainly from oak, or as lyophilized extracts to the grape must or finished wine. Today’s wine market typically presents a wide range of tannins used for wine making, also called oenotannis or oenological tannins, which are derived from a broad range of plants and wood. Wood commercial preparations are sourced from chestnut, oak, and exotic woods (such as quebracho Schinopsis lorentzii and Schinopsis balansae).102 In 1986, Salagoity-Auguste et al.103 proposed a classification discriminating the different botanical origin based on the distribution of gallic acid and its derivatives. The different botanical origin and chemical nature of oenotannis determine specific characteristics; therefore, they are added at different stages of winemaking to achieve color stabilization, improve the organoleptic characteristics, and enhance the aging capacity and antioxidant capacity, inhibiting the growth of microorganisms and the control of laccase activity.104 The International Organisation of Vine and Wine (OIV) International Oenological Codex stated that procyanthocyanidic oenotannins should contain a catechin equivalent of >10 mg/g, while hydrolyzable ellagic tannins should have at least F


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Journal of Agricultural and Food Chemistry 20 mg/g of castalagin equivalents. However, the dosage of exogenous tannins should be conscientiously considered. An overabundance of tannins negatively affects mouthfeel, resulting in a dramatic increase of perception of sensory characteristics, such as bitterness, astringency, and brown color.105 Vivas et al.106 estimated the sensory threshold for astringency, which resulted in 50 and 80 mg/L for oak and chestnut tannin extracts, respectively. The prefermentative addition of a small amount of oak and quebracho tannins to young red wines drove to an improvement of the aroma complexity and color stability.107,108 In particular, condensed tannins improve color stabilization by forming anthocyanin−acetaldehyde−flavonoid polymers,109 while the role of hydrolyzable tannins as color enhancers and stabilizers is still unclear.110 It is also important to underline that exogenous tannins cannot be added as coloring agents.106 Several studies using oak wood chips showed that the high concentration of hydrolyzable tannins gave structure to wine (roundness and mouthfeel) and flavor depending upon the chemical composition of the wood.110,111 In fact, it has been reported that oak wood ellagitannins are responsible for the regulation the oxidative process in wine and hasten the condensation between tannins and anthocyanins that lead to the final sensorial properties of the wine product. Ellagitannins also boost tannin polymerization, decreasing wine astringency.111,112 The addition of oak wood tannins before or after fermentation diminishes the floral and fruity notes of wine while increasing vanilla, spicy, woody, or oak-like flavors as a result of the presence of vanillin, guaiacol, methyl guaiacol, and ellagitannins.110−112 Gelatin. Commercial gelatin is a fibrous protein obtained by partial degradation or thermal denaturation of collagen from mammalian skins and bones. However, a growing number of consumers is rejecting gelatins from land animals as a result of religious or ethical concerns. The occurrence of foot-andmouth disease (FMD), avian influenza (AI), and bovine spongiform encephalopathy (BSE) also contributed to further skepticism about the use of gelatin-based products of land animal origin. The use of fish-processing byproducts, e.g., swim bladder or fish skins, has been suggested as an alternative. These byproducts have a downside, which is a lower bloom strength, because of their poor imino acid content.113 To overcome the problem, several enzymatic modifications114,115 and physical treatments116 have been applied to improve the properties of fish gelatins. In recent years, polyphenols, in particular tannins, have been proposed as an alternative, as a “natural mean” in processing food. Since Balange and Benjakul reported that the addition of tannic acid could increase the gel strength of mackerel surimi,117 the attention focused on natural TWE cutting byproducts (kiam tree and bark from cashew tree) or food wastes (coconut husk). Parts of the kiam tree wood and cashew tree bark have been traditionally used in tropical countries to prevent or retard microbial fermentation in palm sap storage.118 Temdee et al.119 found that the addition of 0.15% kiam tannin wood extract to surimi (in proportion to the protein content) improves the product quality because tannins can cross-link with proteins. Another study reported that kiam wood (439 g of tannic acid equivalent/kg) and cashew bark (254 g of tannic acid equivalent/kg) extracts could improve gel formation through enhancing gel strength and forming large strands with the interconnected structure.120

Coconut husk, similar in chemical composition to hard wood, is particularly rich among other phenolics in tannic acid and condensed tannin and its extract contents of 460 mg of tannin/g approximately.121 The reutilization of this food waste could be used as the alternation protein cross-linker, which strengthens the gel network of gelatin. In a study of the gelatin microstructure, it was found that sardine surimi enriched with coconut husk extract showed an increased strand density and connectivity at a range of concentration between 0.75 and 0.125% based on protein content compared to the control gel. The abundance of hydroxyl groups in tannins could strengthen gel via hydrogen bond and other interactions. In addition to improving the gel breaking force, coconut husk extract increased the acceptability of the product, through the enhancement of sensory and textural characteristics.122 Nevertheless, an excess of tannins could be detrimental and determine a darker color of the gel while decreasing the natural color of the food product.120 In addition, a high concentration of tannins from wood extracts could also decrease whiteness.122 While the effects of other light-colored tannins, such as tara tannins, may have potential in this application, this application will require further study and refinement. Meat Production. One of the major issues of fresh and processed meat is oxidation. The oxidation of proteins, in particular the heme pigment, leads to a conversion of the initial cherry red color to brown. The deterioration of meat is also strongly related to lipid oxidation, which leads to a decline of the quality of the product and its sensory characteristics.123,124 Lipid oxidation affects the unsaturated fatty acid fraction of the meat in a more rapid and intense manner, which is a function on the degree of unsaturation, resulting in hydroperoxides and secondary products.124 Hence, lipid oxidation alters the shelf life of fresh and processed meats, causing off-flavors and altered color.125 Synthetic antioxidant compounds (e.g., butylated hydroxyanisole and butylated hydroxytoluene) can be added to meat products to prevent or retard these undesirable effects, but they are being examined for their carcinogenic and toxicological effects.126 As a result, producers and consumers are seeking alternative, safer, natural food additives that can be blended during product formulation, used as a coating, or combined into the packaging. Because antioxidants can be used during the period of fattening the animal, there is an increasing proportion of consumers buying meat that prefers the use of natural additives in animal feeds. In this sense, the positive biological effects on animals,127,128 the capacity to maintain meat color stability, extending its self-life,129 and the low production costs can make TWEs an effective feed additive. Several studies on ruminants and monogastric animals showed that administration of TWEs from different sources may improve the fatty acid profile by increasing the proportion of polyunsaturated fatty acids (PUFAs), in addition to improvements in other meat characteristics, such as reduction of cooking weight loss or meat tenderness. Supplementation with chestnut tannins reduced carcass fat deposition in pigs, resulting in a higher proportion of PUFAs in fat tissue.130 Another study indicated that dietary supplementation with quebracho tree tannins may inhibit lipid peroxidation also in meat of rabbit reared under high temperatures (33 °C).131 Nevertheless, inconsistent findings are found in the scientific literature. Dalle Zotte et al.132 could not demonstrate the effectiveness of dietary addition of tannin in improving G


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Future Perspectives. As a result of their numerous biological and chemical properties, TWEs have excellent potential for innovative applications in food production. The highly effective antimicrobial activity of wood tannins has been widely documented, as has their use as stabilizing and preservative agents to replace those synthetic compounds currently under use in foodstuffs of different origins. A particularly interesting, as yet not fully explored, field of application could be food preservation. The addition of a tannin bark extract from Albizia myriophylla determined the extension of shelf life stability of “atingba”, a fermented rice beer.143 In addition to increasing the antioxidant activity of the fortified beer, the extract behaved as a potent antimicrobial agent by decreasing the growth of S. aureus and E. coli and generally decreasing aerobe count in the atingba.143 An issue of relevance for the food industry is post-cooking contamination of meat. A possible application of wood tannins could be their incorporation in films. A recent study showed that hydrolyzable tannins added to gelatin mitigated E. coli O157:H7 growth.142 Other authors better suggest that bioactive antioxidant compounds be incorporated directly during product formulation or produce a coating on the food surface.144 In support of the beneficial biological activities cited in the prior text, several in vivo studies have reported the effective use of TWEs as food supplements in nutraceutical applications. A focal point is the use of tannins in celiac disease, as reported in the studies of Dias et al.32−34 In this sense, TWEs could be applied for the formulation of nutraceuticals for special categories, such as celiac patients. Another potential nutraceutical application could aim to control type 2 diabetes. Encapsulation of sorghum condensed tannins in kafirin microparticles showed inhibitory activity against amylase, preventing hyperglycaemia symptoms.33 Some industries are already commercializing TWEs as nutraceuticals, not incorporated in food. The wood extract of the French oak (Quercus robur) Robuvit offers welldocumented scientific literature and is offered on Amazon among other vendors. Its formulation is focused on reducing fatigue, boosting energy, and improving both physical performance and mood. Multiple clinical studies conducted on different classes of population (e.g., elderly individuals, athletes, and patients affected by chronic fatigue syndrome) reported that Robuvit use resulted in an improvement of mental concentration, sleep, and recovery from fatigue and physical performances.145−147 Even though these commercial products present several beneficial effects, they are still considered as dietary supplements taken in the form of capsules or tablets, similar to a drug. Because consumers could have an issue with the consumption of a product in this form, future investigations should be directed to the inclusion of TWEs in food as a solution and potential positive factor of acceptance to take advantage of their varied potential health and nutritional effects.

oxidative stress or fatty acid profile on raw or cooked rabbit meat. The authors attribute the negative results to the inefficacy of tannin metabolites to reach the target tissue. Even though the doses of 1 and 3% of quebracho tannins in rabbit diets had beneficial effects on live performance, these levels of supplementation did not impact the antioxidant status of meat in this study.133 The addition of pine bark condensed tannins to diets fed to meat goats did not improve meat quality and fatty acid profile.134 As a result of the controversial results present in the literature, other authors proposed adding tannins directly to raw meat (during product formulation) to create a coating.10 Certainly, more research is needed to better understand the potential of TWEs to impact the organoleptic characteristics of meat and enhance shelf life in the supermarket. Packaging. Almost all food products present in markets are wrapped, in direct contact with packaging materials. In this sense, natural products may be a better choice, avoiding the eventual absorption of harmful substances from synthetic materials. Food packaging not only constitutes a simple physical−mechanical barrier but also is required to provide new features, such as extend the shelf life of the products. For this reason, these new materials are also called “active packaging”.135 Food packaging is a key component for preservation from external contamination and physical damage of food products. The shelf life of food depends upon many factors, such as oxidative degradation [as a result of ultraviolet (UV) light and O2] and/or microbial deterioration. Tannins are recognized by the U.S. Food and Drug Administration (FDA) as generally recognized as safe (GRAS) food additives, generally applied to preserve food against microbial spoilage and oxidative degradation.136 Therefore, tannin properties, such as antioxidant capacity, antibacterial/antifungal activity, and UV absorption suggest their useful application for functional films in food packaging. In this sense, alternative antioxidant packaging films also resistant to UV radiations have been studied.137 The application of new green materials received great attention in the last few years.138 Condensed tannins have been successfully mixed with polylactic acid (PLA), one of the most important polymers in bioplastic engineering.139 In particular, Garciá et al.140 studied the application of tannins from Pinus radiata bark and their modifications. The inclusion of wood tannins resulted in inducing PLA crystallization to a high extent, influencing the flexural performance and thermal stability. The modified tannins resulted in higher compatibility with PLA-based blends. Condensed tannins from larch bark have been successfully blended with poly(vinyl alcohol) (PVA), a highstrength biodegradable polymer, obtaining new membranes with antioxidative ability and anti-UV properties.141 Furthermore, the good compatibility of tannins with PVA allowed for the maintenance of the basic features of PVA membranes, such as the mechanical strength and crystallization properties. A growing interest is focusing also in synthesizing new biodegradable gelatin films for meat preservation and commercialization, to avoid the synthetic polymeric counterparts. Some authors evaluated the addition of 10% (w/w) hydrolyzable chestnut tannins to gelatin films plasticized by glycerol.142 The incorporation of tannins had a good impact on the tensile properties and water repellence and, more interestingly, enhanced the radical scavenging activity of the films, which exhibited moderate growth inhibitory microbial activity.

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AUTHOR INFORMATION

Corresponding Author

*Telephone: 0034-958242841. Fax: 0034-958249577. E-mail: jarufi[email protected]. ORCID

Silvia Molino: 0000-0001-9405-5085 José Á ngel Rufián Henares: 0000-0002-1428-4353 H


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Journal of Agricultural and Food Chemistry Notes

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This paper will form part of the doctoral thesis of Silvia Molino, conducted within the context of the “Nutrition and Food Sciences Programme” at the University of Granada.

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ABBREVIATIONS USED AI, avian influenza; BSE, bovine spongiform encephalopathy; FDA, Food and Drug Administration; FMD, foot-and-mouth disease; GRAS, generally recognized as safe; OIV, International Organisation of Vine and Wine; PRP, protein rich in proline; PUFA, polyunsaturated fatty acid; PLA, polylactic acid; PVA, poly(vinyl alcohol); SCFA, short-chain fatty acid; TWE, tannin wood extract

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