Natural Tannin Wood Extracts as a Potential Food Ingredient in the

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NATURAL TANNINS WOOD EXTRACTS AS POTENTIAL INGREDIENT IN FOOD INDUSTRY Silvia Molino, Natalia Andrea Casanova, José A. RufiánHenares, and Mariano Enrique Fernandez Miyakawa J. Agric. Food Chem., Just Accepted Manuscript • Publication Date (Web): 22 May 2019 Downloaded from http://pubs.acs.org on May 30, 2019

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Journal of Agricultural and Food Chemistry

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NATURAL TANNINS WOOD EXTRACTS AS POTENTIAL FOOD INGREDIENT IN FOOD INDUSTRY

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Silvia Molinoa, Natalia Andrea Casanovab, José Ángel Rufián Henaresa,c, Mariano Enrique

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Fernandez Miyakawab,d

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a

Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos,

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Centro de Investigación Biomédica, Universidad de Granada, Avda. del Conocimiento S/N,

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Armilla (Granada), Spain

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b Instituto

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de Patobiología, Centro de Investigación en Ciencias Veterinarias y Agronómicas, Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, Argentina

c Instituto

d

de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, Spain.

Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

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*Corresponding Author

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Dr. José Ángel Rufián Henares

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Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos,

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Centro de Investigación Biomédica, Universidad de Granada, Avda. del Conocimiento S/N, 18100,

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Armilla (Granada), Spain

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Tel: 0034 958242841

Fax: 0034 958249577

E-mail address: [email protected]

24 1 ACS Paragon Plus Environment


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Abstract

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Wood extracts are one of the most important natural sources of industrially obtained tannins. Their

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use in the food industry could be one of the biggest (most important) recent innovations in food

28

science due to their multiple (many) possible applications. The use of tannins wood extracts (TWE)

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as additives directly added in foods or in their packaging meets an ever-increasing consumer

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demand for innovative approaches to sustainability. The latest research is focusing on new ways to

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include them directly in food, to take advantage of their specific actions to prevent individual

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pathological conditions. The present review begins with the biology of TWE and then explores their

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chemistry, specific sensorial properties and current application in food production. Moreover, this

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review is intended to cover recent studies dealing with the potential use of TWE as a starting point

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for novel food ingredients.

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Keywords

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Tannins, wood extracts, foods, food supplements, gut microbiota.

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2 ACS Paragon Plus Environment

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INTRODUCTION

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In 1796, A. Seguin proposed the term “tannin” to define the extractable substance used to

42

convert animal skin to leather, demonstrating the capacity of these compounds to precipitate

43

gelatine from solution.1 Bate-Smith and Swain in 1962 gave a more specific description of tannins

44

as “water soluble phenolic compounds having molecular weights between 500-3000 Da and,

45

besides giving the usual phenolic reactions, they have special properties such as the ability to

46

precipitate alkaloids, gelatin and other proteins”.2 According to their structural characteristics

47

(Figure 1), tannins are divided into: gallotannins, ellagitannins, condensed tannins, complex

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tannins, and phlorotannins (from brown algae).3,4 The first two groups are the traditionally known

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as hydrolysable tannins, since these compounds are hydrolysed by weak acids to yield sugar

50

(mainly glucose), and acid derivate, gallic and ellagic acids, respectively. Complex tannins are

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composed by a unit of hydrolysable tannins bound to a catechin unit.3 Meanwhile, condensed

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tannins, also referred as proanthocyanidins, are oligomers or polymers of flavan-3-ols.

53

Tannins are widely distributed in many plant species as they are present in the leaves, buds,

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stem, bark, wood, roots, fruits and seeds.5 These compounds are normally present in fruits and

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vegetables included in the human diet. Nevertheless, only a minority of plants consumed by human

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beings constitute a major source of tannins, since the parts containing these compounds are a small

57

fraction of the edible part (e.g. walnut skin) or because they are not eaten at all. For this reason,

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tannins extracted from wood and bark, normally applied in the process of leather tanning, are now

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finding new relevant applications in the food sector, among others. Furthermore, there is an

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increasing market demand for more “natural” and “ecological” food products and production

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processes, and a reduced demand for products of chemical synthesis.

62

Due to their unique chemical properties, TWE are utilized to improve food quality by

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several modes of actions and in a wide variety of products. Astringency and bitterness are the most

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recognized and sought-after properties of tannins for food quality, i.e., the perceived mouthfeel



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occurring in food products such as aged wines and spirits. Indeed, tannic acid (a commercial

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available gallotannin), is a European Union (EU) recognized food flavouring.6 On the other hand,

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new tendencies of food processing are driving the application of green technologies, including the

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concept of natural food preservatives. In this sense, advantage may be taken of the well-known

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antioxidant4 and antimicrobial5 properties of tannins to ensure minimal food processing, and also

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protect from spoilage and contamination.

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Tannin compounds can have a large influence on the nutritive value of many foods eaten by

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humans, as well as feedstuffs eaten by animals. They are considered as bioactive compounds due to

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their capacity of modulate metabolic process and promote health.7 Different TWE showed strong

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biological activities in the form of anti-tumor, anti-mutagenic, anti-diabetic, anti-proliferative, anti-

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bacterial and anti-mycotic properties, both in human beings and in animals. For this reason, the

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tannin-food interaction could be exploited in food systems to benefit human nutrition and health,

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with technological applications to deliver specific compounds,8 or exert specific functions (e.g. to

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reduce the caloric impact of foods).9

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Wood tannins satisfy the characteristics that Lorenzo et al.10 established in order to be used

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as food additives. These compounds are economical, ensure stability during processing, extend

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shelf-life, are compatible with foods and can be effective at low concentrations (to affect the

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sensory properties of food).10 TWE are therefore not only a novel product of interest for consumers,

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but also for food producers and product developers. The present review focused in all the results

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obtained regarding the potential use of TWE as starting point for novel food ingredients.

85 86

Digestion of tannins

87

The first requisite for a bioactive compound is to be absorbed after digestion, or to be

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unabsorbed and then reach the colon where it can be further metabolized by the gut microbiota. The

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absorption and the metabolism of each type of tannin differs greatly and, although the gut


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microbiota has a clear impact on the metabolism of plant tannins, to date little is known of its

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specific effects.11

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Due to the structure and buffering effect of the food bolus in the gut, condensed tannins are

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not degraded in acidic conditions of the stomach.12 As a result of digestion in the small intestinal,

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smaller compounds can be more readily absorbed (monomeric, dimeric, and trimeric catechins),

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which suggests that polymerization impairs intestinal absorption.13 With hydrolysable tannins, free

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ellagic acid and gallic acid (from ellagitannins and gallotannins, respectively) are released after acid

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hydrolysis. Konishi et al. demonstrated that gallic acid is permeated via the paracellular route in

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Caco-2 cells.14 No ellagitannins in intact form were detected in human plasma samples, while

99

ellagic acid was detected in human plasma in low concentrations after oral administration.15

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A large part of ingested tannins reach the large intestine, where the gut microbiota convert

101

them

into

metabolites.

More

specifically,

5-(30-hydroxyphenyl)-valerolactone,

3-(3-

102

hydroxyphenyl)-propionic acid, 3,4-dihydroxyphenylacetic acid, 3-hydroxyphenylacetic acid are

103

produced from the catabolism of monomeric and oligomeric condensed tannins. Ellagic acid is

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converted into urolithins.16

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Once metabolic products have crossed the intestinal barrier, they reach the liver through the

106

portal vein, where they are further metabolized, to form O-glucuronides, sulphate esters and O-

107

methyl ether; no free aglycones are found in plasma.13,17 The new conjugates can reach the blood

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stream or return to the intestinal tract through bile excretion. Here, gut microbiota may exert

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enzymatic activity to deconjugate O-glycosides and O-glucuronides and further metabolize the

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compounds. Several studies reported that the bioactivity of tannins metabolites could differ or be

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weakened from the functions exerted by parent compounds. Urolithins were determined to have

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higher physiological activity than ellagitannin and ellagic acid.16

113 114

Biological effects of tannins



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The biological effects of tannins, including their antioxidant and radical scavenging,

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antimutagenic or antigenotoxic, antimicrobial, metabolic or immunomodulatory properties, among

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others, are closely related to their chemical structure and degree of polymerization. Moreover, the

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outcome depends not only on the species of plant but also on the specific part from which they were

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derived.4,18,19 Several studies described the beneficial effects of tannin-rich fractions; however,

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results are sometimes controversial due to the use of non-standardized extracts and techniques.19

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Furthermore, information on the activities of tannins derived exclusively from wood is relatively

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less abundant or accessible from the literature.

123 124

Antioxidant and antitumor properties.

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At the present moment the mechanisms by which tannins exert their antioxidant and

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antitumor activities are not fully elucidated. Some authors suggest that these effects are mainly due

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to direct impact on cell structures, the modulation of pro/anti-oxidant enzymes (such as superoxide

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dismutase, catalase and lipoxygenases) and the scavenging of hydroxyl, superoxide and peroxyl

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radicals, which in turn decrease proteins and lipids oxidation and normalize cell redox balance.20–23

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In the case of

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procyanidins B1 and B3 exhibited stronger antioxidant activity than ascorbic acid and α-tocopherol.

132

An increase in antioxidant ability is observed with the low degree of polymerization of

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proanthocyanidins.24

the antioxidant effects of proanthocyanidins, isolated compounds such as

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Tannins derived from wood (casuarictin, castalagin, vescalagin, cinnamtannin B-1 and B-2,

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grandinin, epicatechin 3-O-gallate) as well as proanthocyanidins and procyanidin-rich fractions

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inhibit cell proliferation and induce apoptosis of neoplastic cells,25–27 and prevent this mechanism in

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normal cells by reducing caspase activation and translocation.28,29

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Physiological and metabolic activities.


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Relatively high tannin concentrations may result in potential gastrointestinal problems due

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to the great affinity of tannins for proteins, which may result in an inhibition of digestive

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enzymes.30,31 So, the property of tannins to bind proteins could interfere with the absorption of

143

nutrients such as proteins, carbohydrates and metals.24 However, the ability of tannins to bind

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gluten proteins could be exploited as a potential therapeutic approach for celiac disease.32 Dias et

145

al.33 revealed that tannins (in particular epigallo-catechin-3-gallate) could have a potential role in

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modulating some molecular processes associated with celiac disease. In their in vitro transwell cells

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experiments on Caco-2, they found that epigallo-catechin-3-gallate reduced the translocation of the

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immune reactive peptide involved in celiac pathogenesis, across the simulated intestinal epithelial

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barrier. In addition, in vitro studies showed the ability of procyanidin B3, procyanidin trimers,

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procyanidin tetramers and an oligomeric mixture of high molecular weight procyanidins to bind to

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wheat gliadins.34

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Tannins also exert antidiabetic potential due to: i)

The improvement of the levels of insulin and pro-insulin in blood. The affinity of

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tannins to bind polysaccharides determines a delay and a decrease of availability of

155

glucose in the gastrointestinal tract. Moreover, several studies reported the potential of

156

inhibition of -amylase and -glucosidase activity by hydrolysable tannins and

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condensed tannins, respectively.4

158

ii)

specific components of the intracellular insulin-signaling pathway.35

159 160

The insulin-like effect on insulin-sensitive tissues. Procyanidins can act on certain

iii)

The regulation of the antioxidant environment of pancreatic β-cells. It is assumed that

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oxidative stress plays a role in diabetes, as it determines apoptosis of β-cells.

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Furthermore, the expression of genes related with antioxidant enzymes in the pancreas is

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low. The high antioxidant capacity of tannins can counteract the pathogenesis of

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diabetes mellitus.4,18



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The antidiabetic potential of a TWE (Pterocarpus marsupium wood extract) in rats was 36.

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reported by Mishra et al.

In particular, among other compounds, the authors identified an

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active antidiabetic component in epicatechin, which improved the oral glucose tolerance post

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sucrose load and exerted regenerative activity on pancreatic  cells. Normal and streptozotocin-

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induced diabetic rats treated with wood extracts presented a decline in blood glucose and

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increased insulin levels in diabetic rats. Subsequent results confirm the effects of P. marsupium

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wood extract showing a dose-dependent antioxidant, antidiabetic, anti-inflammatory and

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analgesic activities in a mice model.37 Likewise, cinnamtannin, condensed tannin from bay

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wood, also showed antidiabetic properties by decreasing some complications in type 2 diabetes,

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such as platelet hyperactivity and hyperaggregability, which lead to the development of micro-

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and macroangiopathy.38

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Other TWE (bark and wood extracts of Castanea sativa) have been shown to behave as

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cardioprotective agents in rat culture cells,39 to have antispasmodic action induced by modulation of

178

cholinergic receptors and calcium channels,40 to prevent DNA damage reducing oxidative stress in

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pigs,41 and to afford neuroprotection when added to neuroblastoma cells before oxidative stress

180

mediated-damage.26

181 182

Antimicrobial activity.

183

There are several mechanisms involved in tannin antimicrobial activity, including metal chelation

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required from microbial growth (mainly iron), interactions with proteins and cell wall/membrane

185

(leading to structural destabilization) and enzymes inhibition.5 Gram-positive bacteria are more

186

sensitive to tannins; however, these effects have been proved against Gram-negative bacteria,

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viruses and parasites (Table 1).

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Sweet chestnut (Castanea sativa) and red quebracho (Schinopsis lorentzii) are a

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representative commercial source of hydrolysable and condensed tannins, respectively. Commercial


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tannins of wood extracts and castalagin (an isolated tannin from chestnut) had antimicrobial effects

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against food-borne pathogenic bacteria such as Campylobacter jejuni,42 Salmonella Typhymurium,43

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S. aureus, Salmonella spp, enteropathogenic E. coli and Vibrio spp44. Inhibition of Salmonella

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Typhymurium growth in vitro by commercial tannins from chestnut was observed, with no effect in

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fecal excretion or colonization of internal organs in a pig model.45 Likewise, Min et al.46 reported

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that hydrolysable tannins exerted in vitro bacteriostatic and bactericidal effects against E. coli

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O157:H7 and reduced the shedding of generic E. coli in steers fed tannins. Another Gram-positive

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bacterium, Clostridium perfringens, was inhibited in a dose-dependent pattern by both types of

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tannins and their combination, having also anti-toxin effects.47 Comparative analysis showed that

199

chestnut derived tannins exerted a stronger antibacterial effect. These results are in accordance with

200

those obtained by others who observed that chestnut and quebracho extracts were efficient in

201

controlling the proliferation of C. perfringens in vivo and in reducing its excretion and the severity

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of lesions in treated animals respect to infected control.48 Antiviral effects of chestnut and

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quebracho wood extracts49 and isolated tannins of chestnut50, such as castalagin and vescalagin,

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were described. Quebracho tannins also exhibited inhibitory effects against parasites like

205

helminthes51–53 and coccidia54.

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Many other tree species were studied in relation to their antimicrobial properties. Tannins

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from wood and bark of Pterocarpus marsupium,37 Punica granatum, Elaeocarpus sylvestris var.

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ellipticus,44 Uncaria tomentosa27 and Ceriops decandra55 showed antibacterial activity against

209

Enterococcus faecalis, S. aureus and Bacillus spp. Regarding Gram negative bacteria, condensed

210

and hydrolysable tannins isolated from woody plants displayed antimicrobial effects against E. coli

211

and E. coli O157:H7,55,56 Pseudomonas aeruginosa,27,57 Proteus vulgaris55 and Porphyromonas

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gingivalis58,59. Antiviral activities were also established for tannins derived from wood of

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Xanthoceras sorbifolia,60 Quercus robur50 and Terminalia spp61.

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Impact on gut microbiota.

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Tannins exert local and systemic effects owing to interactions between absorbable tannins

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(low molecular weight) and their metabolites with tissues.21 Non-absorbable tannins (high

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molecular weight) reach the colonic gut microbiota, exhibiting a prebiotic effect. Herein, the

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compounds are metabolized by microorganisms, resulting in metabolites with different

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bioavailability, activity, or functional effect compared to the parent molecule. On the other hand,

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tannins can modulate gut microbial composition and function, inhibiting selectively pathogens and

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promoting growth of beneficial bacteria.62 Some studies demonstrate the causal effect of gut

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microbes in chronic pathologies. Tannins may have an indirect impact in these diseases.

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Mechanisms of these actions are still not completely understood, but it is highly likely that their

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dietary intake can be beneficial for human health and immunity.63 Ellagitannins from extracts of

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berries resulted in strong inhibitory compounds which were effective against Staphylococcus

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bacteria, but they did not alter probiotic strains, i.e. Lactobacillus rhamnosus.64 The study of

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Masumoto et al.65 found that in mice feed high-fat/high-sucrose diet, non-absorbable apple

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procyanidins induced a decrease of the Firmicutes/Bacteroidetes ratio. On the other hand, the

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realtive abundance of Verrucomicrobia and, in particular, A. muciniphila increased A. muciniphila

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(and more in general Verrucomicrobia) have been recently investigated as markers of healthy gut

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since they possess antinflammatory properties, increase insulin sensitivity and boost the gut barrier

233

function.65

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Short chain fatty acids (SCFAs) are produced by metabolism of the gut microbiota and play

235

a critical role in the human health. SCFAs can modulate cell metabolism in humans and fine tune

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the immune repsonse, in addition to contribuing as an energy source.66 In the study of Molino et

237

al.67 the application of their in vitro digestion and fermentation model in which quebracho and

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chestnut TWE were used gave increased production of SCFAs.A similar release of total SCFAs by

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grape and apple proanthocyanidins was decribed by Aura et al.68. Tannins have been proposed as


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prebiotic subtrates for the gut microbiota, due to their stimulation of SCFAs production, growth-

241

promoting effects for beneficial bacteria, and/or by activation of their metabolic functions.16,69

242

In addition, the combination of proanthocyanidins and polysaccharides (such as pectin)

243

present in the food matrix could result in an additive effect.68 Proanthocyanidins associated with

244

polysaccharides, poorly bioavailable in the upper intestine, reach the colon, where the gut

245

microbiota convert these fermentable substrates into active metabolites, potentially absorbable.31

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The conversion rate increases when proanthocyanidins are associated with the food matrix, likely

247

because polysaccharides act as a nutrient for microbiota, which metabolizes more efficiently those

248

proanthocyanidins

249

proanthocyanidin chain length determinea competition mechanism between the inhibition of

250

microbial enzymes by these molecules and the capacity of colonic microorganisms to metabolize

251

such tannins. As regards ellagitannins in combination with fructooligosaccharides, the literature is

252

unclear as to whether their role is beneficial or counterproductive in the production of SCFAs in

253

animals.16

linked

to

polysaccharides.

Bazzocco

and

co-workers31

found

that

254

Finally, some studies reported that tannins can also promote the adhesion and the

255

colonization of probiotic bacteria resulting in an ulterior beneficial effect. Kawabata and co-workers

256

found that procyanidins and epigallocatechin induced the adhesion of acid lactic bacteria in an in

257

vitro intestinal epitelial tissue model.16 All the mentioned results suggest a bi-directional

258

relationship between tannins and gut microbiota.

259 260

Tannin interactions with macromolecules: relationship with sensory properties

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Tannins – polysaccharides

262

Interactions between tannins, particularly condensed tannins, and polysaccharides have been

263

studied and widely demonstrated in the context of clarification and of astringency control of

264

beverages.70 In fact, the most investigated models for tannin-polysaccharide interactions are



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represented by grapes, apples and pears (rich in proanthocyanidins) used for the production of

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ciders and wine.70,71 Proanthocyanidins-polysaccharides associations are spontaneous, quick and

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direct binding events that occur during vegetables and fruit processing.71,72 These bindings are

268

mediated by hydrogen bonds and hydrophobic interactions, which are boosted by ionic strength and

269

lower temperature.73 Moreover, a high degree of polymerization corresponds to higher affinities.73

270

The complexation mechanisms are similar to the aggregation between proanthocyanidins and

271

proteins; nevertheless, both phenomena are distinguished by different kinetics and colloidal

272

consequences.74

273 274

Tannins - proteins

275

Tannins have a distinctive tendency to bind to proteins, by establishing crosslinks with the

276

implication of different nature of bonds. The main driving forces involved are hydrophobic

277

interactions and hydrogen bonds.75 Model studies suggested that three specific steps determine the

278

combination between tannins and proteins (Figure 2). 1) The earliest interactions are characterized

279

by hydrogen bounds and hydrophobic interactions, resulting in the generation of protein-tannin

280

complexes. Hydrophobic interactions comprise entropy-driven Van der Waals forces, while

281

hydrogen bonds are enthalpy-driven electrostatic interactions. Tannins are able to bind to multiple

282

sites on the protein, leading to a condensation of the protein-tannin complex and resulting in a

283

spherical structure.75,76 2) Cross-links between protein-tannin complexes determine a self-

284

association, so that the formation of bigger structures.75,76 3) The association of the large aggregates

285

produces colloidal size particles, which induces the precipitation of protein-tannin complexes.75,76

286

Proteins and tannins binding occur in a specific and selective way. Some factors related with

287

proteins may influence such interactions: protein size, charge, side chains and conformation.

288

Independently to the protein structure, both tannins molecular weight and degree of galloylation

289

enhance their affinity for proteins, probably because tannins size determines the number of


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interaction sites. Nevertheless, larger tannin structures can cause steric hindrance and impede the

291

access to binding sites, then limiting solubility.77

292

Polysaccharides (i.e. arabic gum, pectin, gellan, polygalacturonic acid and xanthan) could

293

obstruct protein-tannin interaction, preventing their precipitation.78 Two mechanisms have been

294

proposed to describe the inhibition of protein-tannin interactions (Figure 2): (i) formation of a

295

ternary soluble complex among protein, tannin and polysaccharide,79 or (ii) encapsulation of tannins

296

by polysaccharides, competing with protein aggregation.80 However, some authors showed that the

297

presence of polysaccharides, in particular mannoproteins, inhibits the evolution of tannin aggregates

298

particle size, but not their generation.81

299

In the mouth, salivary tannin-protein interactions are influenced by the concentration of the

300

proteins.82 Several environmental factors, including temperature, pH and ionic strength influence

301

the formation of salivary-protein aggregates or their precipitation.82 In saliva, among numerous

302

proteins, there is a predominance of proteins rich in proline (PRPs) and in minor proportion glycine

303

and glutamic/glutamine residues.83 PRPs are very efficient in complexing tannins and, in particular,

304

the presence of repeated proline region increase binding affinity. It has been reported that histatins 3

305

and 5, other salivary proteins, increase precipitation of condensed tannins more than histatin 1 due

306

to a different content of histidine and phosphoserine.84 Moreover, a study reported that quebracho

307

tannins and tannic acid are more efficiently precipitating salivary histatin 5 than PRP-1, at pH 7.4.75

308

The tannin-protein binding does not impair the bioavailability of tannins and some authors

309

suggested proteins as carriers of these bioactive compounds.85,86

310 311

Astringency and bitterness

312

Tannins contribute directly to several sensorial aspects of food, including astringency and

313

bitter taste. Astringency has been defined as the taste experience corresponding to dryness and

314

puckering mouthfeel all over the oral surface.87 This complex group of sensations results from the



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315

interaction between tannins and salivary proteins, leading to physical changes in the salivary

316

mixture, particularly a deep decrease in viscosity. The mechanoreceptors perceive the sensation of

317

roughness as the food comes in contact with the tongue, while the tongue is moving over the palate.

318

This sensation is determined by two types of mechanisms: i) decrease of saliva viscosity and

319

increasing of friction due to the interaction between tannins and salivary protein-rich proteins; ii)

320

perception in the oral texture of the protein-tannin precipitates as discrete particles. The last process

321

determines a drying and grainy sensation, that differ on the concentration and dimension of the

322

colloidal aggregates, additionally to the hardness of the precipitate.

323

Astringency is influenced by tannins structure and degree of polymerization, since high

324

molecular weight structures favors the interaction with salivary proteins. Several studies highlighted

325

that proanthocyanidins are the major contributors of astringency intensity, while smaller compounds

326

are not considerably astringent, probably because small dimensions don’t allow to form cross-

327

linking bounds.88,89 Nevertheless, some authors stated a relationship between low molecular weight

328

compounds present in food that could play a role in astringency perception.90,91 As mentioned

329

above, the presence of specific amino acids, such as proline and hydroxyproline, impacts the

330

perception of astringency, being a target for proanthocyanidin reactions.77,92

331

Some authors highlighted that the astringent sensation is not always necessarily correlated to

332

the precipitation of tannin-protein complexes. Indeed, the study of Obreque-Slier et al.93 showed

333

that soluble aggregates of hydrolysable tannins and gelatine were perceived with a marked

334

astringent mouthfeel by sensory panelists, but in vitro they failed to determine precipitation.

335

Moreover, it has been reported that unbound remaining tannins could interact with the epithelial

336

cells of the oral surface, resulting in an increased perceived astringency, especially at lower pH.94

337

Some external factors could also impact the astringent mouth feel (like acidic pH) that

338

determines higher puckering sensation.95 The presence of polysaccharides in the food matrix lead to

339

a smoothing of the astringency by inhibiting protein-tannin interactions. In fact, some studies


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340

showed that the presence of water-soluble pectin could prevent the formation of aggregates between

341

tannins and proteins in the mouth, determining an altered astringency response.96,97 In this sense,

342

polysaccharides could be applied in oenology to improve astringent sensation, giving conversely

343

and increase of roundness and sweetness of wine.98

344

In the mouth, tannins could also interact with taste receptors and give a bitter flavor to food.

345

Soares et al.99 showed that bitterness is a matter of combinatorial pattern of TAS2Rs activation.

346

More specifically, the concentration of natural tannins in food is responsible of a different grade of

347

bitter taste by specifically activating TAS2R5 (condensed tannins) or TAS2R7 (hydrolysable

348

ellagitannins). In general, it is well accepted that larger tannins are less bitter than those with a

349

smaller structure, even though some authors obtained conflicting results.99 The bitterness is

350

influenced by different factors and the evaluation of bitterness may vary based on the type of the

351

assay. The absence of salivary proteins in in vitro taste receptor activation assays could determine

352

discrepancies with the taste threshold of sensory assays.99 The authors hypothesize that the presence

353

of saliva (i.e. salivary proteins) could interact with tannins and induce an in vivo decrease of

354

perceived bitterness. The bitter-making potential of tannins could be reduced also by proteins

355

present in food.100 Finally, the interaction with salivary proteins could reduce the activation of

356

TAS2Rs and determine a perception more astringent than bitter of some tannins.101

357 358

Food Industry Applications

359

Wine

360

Natural occurring tannins contribute to the overall taste and mouthfeel in hydroalcoholic

361

beverages like wine and beers, giving bitterness and astringency. These compounds are naturally

362

present in raw ingredients, while the addition of exogenous tannins is a longstanding technological

363

practice, applied at different times and in a number of forms during the processes of production.



Page 16 of 48

364

Exogenous tannins (added to improve food quality) can be added in the form of wood chips, mainly

365

form oak, or as lyophilized extracts, to the grape must or to finished wine.

366

Today’s wine market typically presents a wide range of tannins used for wine making, also

367

called oenotannis or oenological tannins, which are derived from a broad range of plants and wood.

368

Wood commercial preparations are sourced from chestnut, oak and exotic woods (such as

369

quebracho ‘Schinopsis lorentzii’ and ‘Schinopsis balansae’).102 In 1986, Salagoity-Auguste et al.103

370

proposed a classification discriminating the different botanical origin based on the distribution of

371

gallic acid and its derivatives. The different botanical origin and chemical nature of oenotannis

372

determine specific characteristics, so they are added at different stages of winemaking to achieve

373

color stabilization, to improve the organoleptic characteristics, to enhance the aging capacity and

374

the antioxidant capacity, inhibiting the growth of microorganisms and the control of laccase

375

activity.104 The OIV International Oenological Codex stated that procyanthocyanidic oenotannins

376

should contain a catechin equivalent >10 mg/g, while hydrolysable ellagic tannins should have at

377

least 20 mg/g castalagin equivalents. However, the dosage of exogenous tannins should be

378

conscientiously considered. An over-addition of tannins affects negatively mouth feel, resulting in a

379

dramatic increase of perception of sensory characteristics like bitterness, astringency and brown

380

colour.105 Vivas et al.106 estimated the sensory threshold for astringency, which resulted 50 and 80

381

mg/L for oak and chestnut tannin extracts, respectively.

382

The pre-fermentative addition of a small amount of oak and quebracho tannins to young red

383

wines drove to an improvement of the aroma complexity and color stability.107,108 In particular,

384

condensed tannins improve color stabilization by forming anthocyanin-acetaldehyde-flavonoid

385

polymers,109 whilst the role of hydrolysable tannins as color enhancers and stabilizers is still

386

unclear.110 It is also important to underline that exogenous tannins can’t be added as coloring

387

agents.106


Page 17 of 48


388

Several studies using oak wood chips showed that the high concentration of hydrolysable

389

tannins, gave structure to wine (roundness and mouthfeel) and flavor depending upon the chemical

390

composition of the wood.110,111 In fact, it has been reported that oak wood ellagitannins are

391

responsible of the regulation the oxidative process in wine and hasten the condensation between

392

tannins and anthocyanins, that lead to the final sensorial properties of the wine product.

393

Ellagitannins also boost tannin polymerization, decreasing wine astringency.111,112 The addition of

394

oak wood tannins before, or, after fermentation diminishes the floral and fruity notes of wine, while

395

increasing vanilla, spicy, woody or oak-like flavors due to the presence of vanillin, guaiacol, methyl

396

guaiacol and ellagitannins.110–112

397 398

Gelatin

399

Commercial gelatin is a fibrous protein obtained by partial degradation or thermal

400

denaturation of collagen from mammalian skins and bones. However, a growing number of

401

consumers is rejecting gelatins from land animals due to religious or ethical concerns. The

402

occurrence of foot-and-mouth disease (FMD), avian influenza (AI), bovine spongiform

403

encephalopathy (BSE) also contributed to a further skepticism about the use of gelatin-based

404

products of land animal origin. The use of fish processing by-products e.g., swim bladder or fish

405

skins has been suggested as an alternative. These by-products have a downside which is a lower

406

bloom strength, because of their poor imino acid content.113 To overcome the problem, several

407

enzymatic modifications114,115 and physical treatments116 have been applied to improve the

408

properties of fish gelatins. In recent years, polyphenols, in particular tannins, have been proposed as

409

an alternative, as “natural mean” in processing food. Since Balange and Benjakul reported that the

410

addition of tannic acid could increase the gel strength of mackerel surimi,117 the attention focused

411

on natural TWE cutting by-products (kiam tree and bark from cashew tree) or food wastes (coconut

412

husk). Parts of the kiam tree wood and cashew tree bark have been traditionally used in tropical



Page 18 of 48

413

countries to prevent or retard microbial fermentation in palm sap storage.118 Temdee et al.119 found

414

that the addition of a 0.15% of kiam tannin wood extract to surimi (in proportion to the proteins

415

content) improves the product quality since tannins can cross-link with proteins. Another study

416

reported that kiam wood (439 g tannic acid equivalent/kg) and cashew bark extracts (254 g tannic

417

acid equivalent/kg) could improve gel formation through enhancing gel strength and forming large

418

strands with the interconnected structure.120

419

Coconut husk, similar in chemical composition to hard wood, is particularly rich among

420

other phenolics in tannic acid and condensed tannins and its extract contents 460 mg tannin/g

421

approximately.121 The reutilization of this food waste could be used as the alternation protein cross-

422

linker, which strengthens the gel network of gelatin. In a study of the gelatin microstructure, it was

423

found that sardine surimi enriched with coconut husk extract showed an increased strand density

424

and connectivity at a range of concentration % between 0.75 and 0.125, based on protein content,

425

compared to the control gel. The abundance of hydroxyl groups in tannins, could strengthen gel via

426

hydrogen bond and other interactions. In addition to improving the gel breaking force, coconut husk

427

extract increased the acceptability of the product, through the enhancement of sensory and textural

428

characteristics.122 Nevertheless, an excess of tannins could be detrimental and determine a darker

429

color of the gel while decreasing the natural color of the food product.120 In addition, high

430

concentration of tannins from wood extracts could also decrease whiteness.122 While the effects of

431

other light-colored tannins such as tara tannins may have potential in this application, this

432

application will require further study and refinement.

433 434

Meat production

435

One of the major issues of fresh and processed meat is oxidation. The oxidation of proteins,

436

in particular the heme pigment, leads to a conversion of the initial cherry red color to brown. The

437

deterioration of meat is also strongly related to lipid oxidation, which lead to a decline of the quality


Page 19 of 48


438

of the product and its sensory characteristics.123,124 Lipid oxidation affects in a faster and more

439

intense way the unsaturated fatty acid fraction of the meat in a more rapid and intense manner

440

which is a function on the degree of unsaturation, resulting in hydroperoxides and secondary

441

products.124 Hence, lipid oxidation alters the shelf-life of fresh and processed meats causing off-

442

flavors and altered colour.125 Synthetic antioxidant compounds (e.g. butylated hydroxyanisole and

443

butylated hydroxytoluene) can be added to meat products to prevent or retard these undesirable

444

effects, but they are being examined for their carcinogenic and toxicological effects.126 As a result,

445

producers and consumers are seeking alternative safer natural food additives that can be blended

446

during product formulation, used as a coating or combined into the packaging. Since antioxidants

447

can be used during the period of fattening the animal, there is an increasing proportion of

448

consumers buying meat that prefers the use of natural additives in animal feeds. In this sense, the

449

positive biological effects on animals,127,128 the capacity to maintain meat color stability, extending

450

its self-life129 and the low production costs can make TWE an effective feed additive.

451

Several studies on ruminants and monogastric animals showed that administration of TWE

452

from different sources may improve fatty acid profile by increasing the proportion of PUFA

453

(polyunsaturated fatty acids), in addition to improvements in other meat characteristics such as

454

reduction of cooking weight loss or meat tenderness. Supplementation with chestnut tannins

455

reduced carcass fat deposition in pigs, resulting in a higher proportion of PUFA in fat tissue.130

456

Another study indicated that dietary supplementation with quebracho tree tannins may inhibit lipid

457

peroxidation also in meat of rabbit reared under high temperatures (33 °C).131 Nevertheless,

458

inconsistent findings are found in the scientific literature. Dalle Zotte et al.132 couldn’t demonstrate

459

the effectiveness of dietary addition of tannin in improving oxidative stress or fatty acid profile on

460

raw or cooked rabbit meat. The authors attribute the negative results to the inefficacy of tannins

461

metabolites to reach the target tissue. Even though the doses of 1 and 3% of quebracho tannins in

462

rabbit diets had beneficial effects on live performance, these levels of supplementation did not



Page 20 of 48

463

impact the antioxidant status of meat in this study.133 The addition of pine bark condensed tannins

464

to diets fed to meat goats did not improve meat quality s and fatty acid profile.134 Due to the

465

controversial results present in literature, other authors proposed adding tannins directly to raw meat

466

(during product formulation) in order to create a coating.10 Certainly, more research is needed to

467

better understand the potential of TWE to impact the organoleptic characteristics of meat and

468

enhance shelf life in in the super market.

469 470

Packaging

471

Almost all food products present in markets are wrapped, in direct contact with packaging

472

materials. In this sense, natural products may be a better choice, avoiding the eventual absorption of

473

harmful substances from synthetic materials. Food packaging not only constitutes a simple physic-

474

mechanical barrier, but they are required to provide new features, such as to extend the shelf-life of

475

the products. For this reason these new materials are also called “active packaging”.135 Food

476

packaging is a key component for preservation from external contamination and from physical

477

damage of food products. The shelf life of food depends on many factors like oxidative degradation

478

(due to ultraviolet ‘UV’ light and O2), and/or microbial deterioration. Tannins are recognized by

479

FDA as Generally Recognized As Safe (GRAS) food additives, generally applied to preserve food

480

against microbial spoilage and oxidative degradation.136 Therefore, tannins properties such as

481

antioxidant capacity, antibacterial/antifungal activity and UV-absorption suggest their useful

482

application for functional films in food packaging. In this sense, alternative antioxidant packaging

483

films also resistant to UV radiations have been studied.137 The application of new green materials

484

received a great attention in last years.138 Condensed tannins have been successfully mixed with

485

polylactic acid (PLA), one of the most important polymers in bioplastic engineering.139 In

486

particular, García et al.140 studied the application of tannins from Pinus radiata bark and their

487

modifications. The inclusion of wood tannins resulted in inducing PLA-crystallization in a high


Page 21 of 48


488

extent, influencing the flexural performance and the thermal stability. The modified tannins resulted

489

in higher compatibility with PLA-based blends. Condensed tannins from larch bark have been

490

successfully blended with polyvinyl alcohol (PVA), a high-strength biodegradable polymer,

491

obtaining new membranes with antioxidative ability and anti-UV properties.141 Furthermore, the

492

good compatibility of tannins with PVA allowed to maintain the basic features of PVA membranes,

493

such as the mechanical strength and crystallization properties.

494

A growing interest is focusing also in synthetize new biodegradable gelatin films for meat

495

preservation and commercialization, in order to avoid the synthetic polymeric counterparts. Some

496

authors evaluated the addition of 10% w/w hydrolysable chestnut tannins to gelatin films plasticized

497

by glycerol.142 The incorporation of tannins had a good impact to the tensile properties and water

498

repellence, and more interestingly, enhanced the radical scavenging activity of the films, which

499

exhibited moderate growth-inhibitory microbial activity.

500 501

Future perspectives

502

Due to their numerous biological and chemical properties, TWE have excellent potential for

503

innovative applications in food production. The highly effective antimicrobial activity of wood

504

tannins has been widely documented, as has their use as stabilizing and preservative agents in order

505

of replace those synthetic compounds currently under use of foodstuffs of different origins. A

506

particularly interesting, as yet, not fully explored, field of application could be food preservation.

507

The addition of a tannin bark extract from Albizia myriophylla determined the extension of shelf life

508

stability of “atingba”, a fermented rice beer.143 In addition to increasing the antioxidant activity of

509

the fortified beer, the extract behaved as potent antimicrobial agent by decreasing the growth of

510

Staphylococcus aureus, E. coli, and

511

atingba.143

generally decreasing aerobe count, respectively, in the



Page 22 of 48

512

An issue of relevance for food industry is post-cooking contamination of meat. A possible

513

application of wood tannins could be their incorporation in films. A recent study showed that

514

hydrolysable tannins added to gelatin mitigated E. coli O157:H7 growth.142 Other authors better

515

suggest that bioactive antioxidant compounds be incorporated directly during product formulation,

516

or produce a coating on the food surface.144

517

In support of the beneficial biological activities cited in the prior text, several in vivo studies

518

have reported the effective use of TWE as food supplements in nutraceutical applications. A focal

519

point is the use of tannins in celiac disease, as reported in the studies of Dias et al.

520

sense, TWE could be applied for the formulation of nutraceuticals for special categories, such as

521

celiac patients. Another potential nutraceutical application could aim to control type-2 diabetes.

522

Encapsulation of sorghum condensed tannins in kafirin microparticles showed inhibitory activity

523

against amylase, preventing hyperglycaemia symptoms.33

32–34.

In this

524

Some industries are already commercializing TWE as nutraceuticals, not incorporated in

525

food. The wood extract of the French oak (Quercus robur) Robuvit® French Oak Extract offers a

526

well-documented scientific literature and is offered on Amazon among other vendors. Its

527

formulation is focused on reducing fatigue, boost energy and improve both physical performance

528

and mood. Multiple clinical studies conducted on different classes of population (e.g. elderly

529

individuals, athletes and patients affected by chronic fatigue syndrome) reported that Robuvit® use

530

resulted in an improvement of mental concentration, sleep, and recovery from fatigue and physical

531

performances.145–147 Even though these commercial products present several beneficial effects, they

532

are still considered as dietary supplements taken in form of capsule or tablets, similar to a drug.

533

Since consumers could have an issue with the consumption of a product in this form, future

534

investigations should be directed to the inclusion of TWE in food as a solution and a potential

535

positive factor of acceptance to take advantage of their varied potential health and nutrition effects.

536


Page 23 of 48


537

Abbreviations

538

AI, avian influenza, BSE, Bovine Spongiform Encephalopathy; FDA, Food and Drug

539

Administration; FMD, Foot-and-Mouth Disease; GRAS, Generally Recognized As Safe; OIV,

540

International Organisation of Vine and Wine; PRP, Proteins Rich in Proline; PUFA,

541

Polyunsaturated Fatty Acid; PLA, Polylactic Acid; PVA, Polyvinyl Alcohol; SCFAs, Shortchain

542

Fatty Acidis; TWE, Tannin Wood Extracts.

543 544

Acknowledgements

545

This paper will form part of the doctoral thesis of Silvia Molino, conducted within the context of the

546

‘‘Nutrition and Food Sciences Programme” at the University of Granada.

547 548 549 550 551



552

Page 24 of 48

References

553 554

(1)

555 556

Press, Ed.; Cambridge University Press., 1989. (2)

557 558

Bate-Smith, E. C.; Swain, T. Comparative Biochemistry; Mason, H. S., Florkin, A. M., Eds.; New York: Academic Press, 1962.

(3)

559 560

Haslam, E. Plant Polyphenols: Vegetable Tannins Revisited, 2nd ed.; Cambridge University

Khanbabaee, K.; Ree, T. van. Tannins: Classification and Definition. Nat. Prod. Rep. 2001, 18, 641–649.

(4)

Serrano, J.; Puupponen-Pimiä, R.; Dauer, A.; Aura, A. M.; Saura-Calixto, F. Tannins:

561

Current knowledge of food sources, intake, bioavailability and biological effects. Molecular

562

Nutrition and Food Research. 2009, pp 310–329.

563

(5)

Scalbert, A. Antimicrobial properties of tannins. Phytochemistry 1991, 30, 3875–3883.

564

(6)

EU. EU Guidance to the Commission Regulation (EC) No 2232/1996 of 23 May 1996 on

565 566

Flavouring Substances Used or Intended for Use in or on Foodstuffs; 1996; p L 299/1-200/4. (7)

567 568

Galanakis, E. Chapter 1 - Introduction. In Nutraceutical and Functional Food Components Effects of Innovative Processing Techniques; Academic Press, 2017; pp 1–14.

(8)

Links, M. R.; Taylor, J.; Kruger, M. C.; Naidoo, V.; Taylor, J. R. N. Kafirin microparticle

569

encapsulated sorghum condensed tannins exhibit potential as an anti-hyperglycaemic agent in

570

a small animal model. J. Funct. Foods 2016, 20, 394–399.

571

(9)

Girard, A. L.; Bean, S. R.; Tilley, M.; Adrianos, S. L.; Awika, J. M. Interaction mechanisms

572

of condensed tannins (proanthocyanidins) with wheat gluten proteins. Food Chem. 2018,

573

245, 1154–1162.

574

(10)

Lorenzo, J. M.; Pateiro, M.; Domínguez, R.; Barba, F. J.; Putnik, P.; Kovačević, D. B.;

575

Shpigelman, A.; Granato, D.; Franco, D. Berries extracts as natural antioxidants in meat

576

products: A review. Food Res. Int. 2018, 106, 1095–1104.


Page 25 of 48

577

(11)


Carbonell-Capella, J. M.; Buniowska, M.; Barba, F. J.; Esteve, M. J.; Frígola, A. Analytical

578

methods for determining bioavailability and bioaccessibility of bioactive compounds from

579

fruits and vegetables: A review. Compr. Rev. Food Sci. Food Saf. 2014, 13, 155–171.

580

(12)

Rios, L. Y.; Bennett, R. N.; Lazarus, S. A.; Rémésy, C.; Scalbert, A.; Williamson, G. Cocoa

581

procyanidins are stable during gastric transit in humans. Am. J. Clin. Nutr. 2002, 76, 1106–

582

1110.

583

(13)

584 585

polyphenols in the gut and impact on health. Biomed. Pharmacother. 2002, 56, 276–282. (14)

586 587

Scalbert, A.; Morand, C.; Manach, C.; Rémésy, C. Absorption and metabolism of

Konishi, Y.; Kobayashi, S.; Shimizu, M. Transepithelial Transport of p -Coumaric Acid and Gallic Acid in Caco-2 Cell Monolayers. Biosci. Biotechnol. Biochem. 2003, 67, 2317–2324.

(15)

Seeram, N. P.; Lee, R.; Heber, D. Bioavailability of ellagic acid in human plasma after

588

consumption of ellagitannins from pomegranate (Punica granatum L.) juice. Clin. Chim. Acta

589

2004, 348, 63–68.

590

(16)

591 592

Kawabata, K.; Yoshioka, Y.; Terao, J. Role of Intestinal Microbiota in the Bioavailability and Physiological Functions of Dietary Polyphenols. Molecules 2019, 24, 370.

(17)

Santos-Buelga, C.; Scalbert, A. Proanthocyanidins and tannin-like compounds – nature,

593

occurrence, dietary intake and effects on nutrition and health. J. Agric. Food Chem. 2000, 80,

594

109–1117.

595

(18)

596 597

Sieniawska, E.; Baj, T. Pharmacognosy: Fundamentals, Applications and Strategy. In Tannins; Elsevier Inc., 2016; pp 199–232.

(19)

Smeriglio, A.; Barreca, D.; Bellocco, E.; Trombetta, D. Proanthocyanidins and hydrolysable

598

tannins: occurrence, dietary intake and pharmacological effects. British Journal of

599

Pharmacology. 2017.

600 601

(20)

Ricci, A.; Lagel, M. C.; Parpinello, G. P.; Pizzi, A.; Kilmartin, P. A.; Versari, A. Spectroscopy analysis of phenolic and sugar patterns in a food grade chestnut tannin. Food



602 603

Chem. 2016, 203, 425–429. (21)

604 605

Page 26 of 48

Panzella, L.; Napolitano, A. Natural Phenol Polymers: Recent Advances in Food and Health Applications. Antioxidants (Basel, Switzerland) 2017, 6, 30.

(22)

Tuyen, P.; Xuan, T.; Khang, D.; Ahmad, A.; Quan, N.; Tu Anh, T.; Anh, L.; Minh, T.

606

Phenolic Compositions and Antioxidant Properties in Bark, Flower, Inner Skin, Kernel and

607

Leaf Extracts of Castanea crenata Sieb. et Zucc. Antioxidants 2017, 6, 31.

608

(23)

Deáková, Z.; Slezák, P.; Országhová, Z.; Andrezálová, L.; Lehotay, J.; Muchová, J.; Bürki,

609

C.; Ďuračková, Z. Influence of oak wood polyphenols on cysteine, homocysteine and

610

glutathione total levels and PON1 activities in human adult volunteers – a pilot study. Gen.

611

Physiol. Biophys. 2015, 34, 73–80.

612

(24)

613 614

Sieniawska, E. Activities of Tannins--From In Vitro Studies to Clinical Trials. Nat. Prod. Commun. 2015, 10, 1877–1884.

(25)

Kashiwada, Y.; Nonaka, G. I.; Nishioka, I.; Chang, J. J.; Lee, K. H. Antitumor agents, 129.

615

Tannins and related compounds as selective cytotoxic agents. J. Nat. Prod. 1992, 55, 1033–

616

1043.

617

(26)

Brizi, C.; Santulli, C.; Micucci, M.; Budriesi, R.; Chiarini, A.; Aldinucci, C.; Frosini, M.

618

Neuroprotective Effects of Castanea sativa Mill. Bark Extract in Human Neuroblastoma

619

Cells Subjected to Oxidative Stress. J. Cell. Biochem. 2016, 117, 510–520.

620

(27)

Navarro-Hoyos, M.; Lebrón-Aguilar, R.; Quintanilla-López, J.; Cueva, C.; Hevia, D.;

621

Quesada, S.; Azofeifa, G.; Moreno-Arribas, M.; Monagas, M.; Bartolomé, B.

622

Proanthocyanidin Characterization and Bioactivity of Extracts from Different Parts of

623

Uncaria tomentosa L. (Cat’s Claw). Antioxidants 2017, 6, 12.

624

(28)

Bouaziz, A.; Romera-Castillo, C.; Salido, S.; Linares-Palomino, P. J.; Altarejos, J.; Bartegi,

625

A.; Rosado, J. A.; Salido, G. M. Cinnamtannin B-1 from bay wood exhibits antiapoptotic

626

effects in human platelets. Apoptosis 2007, 12, 489–498.


Page 27 of 48

627

(29)


Ouédraogo, M. M.; Charles, C.; Ouédraogo, M. M.; Guissou, I. P.; Stévigny, C.; Duez, P. An

628

overview of cancer chemopreventive potential and safety of proanthocyanidins. Nutr. Cancer

629

2011, 63, 1163–1173.

630

(30)

Zhong, H.; Xue, Y.; Lu, X.; Shao, Q.; Cao, Y.; Wu, Z.; Chen, G. The effects of different

631

degrees of procyanidin polymerization on the nutrient absorption and digestive enzyme

632

activity in mice. Molecules 2018, 23, 1–11.

633

(31)

Bazzocco, S.; Mattila, I.; Guyot, S.; Renard, C. M. G. C.; Aura, A.-M.; Bazzocco, S.; Mattila,

634

A. I.; Aura, A.-M.; Guyot, S.; Renard, C. M. G. C. Factors affecting the conversion of apple

635

polyphenols to phenolic acids and fruit matrix to short-chain fatty acids by human faecal

636

microbiota in vitro. Eur J Nutr 2008, 47, 442–452.

637

(32)

638 639

Dias, R.; Perez-Gregorio, R.; Mateus, N.; De Freitas, V. The interaction between tannins and gliadin derived peptides in a celiac disease perspective. RSC Adv. 2015, 5, 32151–32158.

(33)

Dias, R.; Brás, N. F.; Fernandes, I.; Pérez-Gregorio, M.; Mateus, N.; Freitas, V. Molecular

640

insights on the interaction and preventive potential of epigallocatechin-3-gallate in Celiac

641

Disease. Int. J. Biol. Macromol. 2018, 112, 1029–1037.

642

(34)

Dias, R.; Perez-Gregorio, M. R.; Mateus, N.; De Freitas, V. Interaction study between wheat-

643

derived peptides and procyanidin B3 by mass spectrometry. Food Chem. 2016, 194, 1304–

644

1312.

645

(35)

Pinent, M.; Blay, M.; Bladé, M. C.; Salvadó, M. J.; Arola, L.; Ardévol, A. Grape Seed-

646

Derived Procyanidins Have an Antihyperglycemic Effect in Streptozotocin-Induced Diabetic

647

Rats and Insulinomimetic Activity in Insulin-Sensitive Cell Lines. Endocrinology 2004, 145,

648

4985–4990.

649

(36)

Mishra, A.; Srivastava, R.; Srivastava, S. P.; Gautam, S.; Tamrakar, A. K.; Maurya, R.;

650

Srivastava, A. K.; Chemistry, P. Antidiabetic activity of heart wood of Pterocarpus

651

marsupium Roxb . and. Indian J. Exp. Biol. 2013, 51, 363–374.



652

(37)

Page 28 of 48

Pant, D.; Pant, N.; Saru, D.; Yadav, U.; Khanal, D. Phytochemical screening and study of

653

anti-oxidant, anti-microbial, anti-diabetic, anti-inflammatory and analgesic activities of

654

extracts from stem wood of Pterocarpus marsupium Roxburgh. J. Intercult. Ethnopharmacol.

655

2017, 6, 1.

656

(38)

Bouaziz, A.; Salido, S.; Linares-Palomino, P. J.; Sanchez, A.; Altarejos, J.; Bartegi, A.;

657

Salido, G. M.; Rosado, J. A. Cinnamtannin B-1 from bay wood reduces abnormal

658

intracellular Ca2+ homeostasis and platelet hyperaggregability in type 2 diabetes mellitus

659

patients. Arch. Biochem. Biophys. 2007, 457, 235–242.

660

(39)

Chiarini, A.; Micucci, M.; Malaguti, M.; Budriesi, R.; Ioan, P.; Lenzi, M.; Fimognari, C.;

661

Gallina Toschi, T.; Comandini, P.; Hrelia, S. Sweet chestnut (Castanea sativa Mill.) bark

662

extract: Cardiovascular activity and myocyte protection against oxidative damage. Oxid.

663

Med. Cell. Longev. 2013, 2013.

664

(40)

Budriesi, R.; Ioan, P.; Micucci, M.; Micucci, E.; Limongelli, V.; Chiarini, A. Stop Fitan:

665

Antispasmodic Effect of Natural Extract of Chestnut Wood in Guinea Pig Ileum and

666

Proximal Colon Smooth Muscle. J. Med. Food 2010, 13, 1104–1110.

667

(41)

Frankič, T.; Salobir, J. In vivo antioxidant potential of Sweet chestnut (Castanea sativa Mill.)

668

wood extract in young growing pigs exposed to n-3 PUFA-induced oxidative stress. J. Sci.

669

Food Agric. 2011, 91, 1432–1439.

670

(42)

Anderson, R. C.; Vodovnik, M.; Min, B. R.; Pinchak, W. E.; Krueger, N. A.; Harvey, R. B.;

671

Nisbet, D. J. Bactericidal effect of hydrolysable and condensed tannin extracts on

672

Campylobacter jejuni in vitro. Folia Microbiol. (Praha). 2012, 57, 253–258.

673

(43)

Costabile, A.; Sanghi, S.; Martín, S.; Mueller, I.; Gibson, G.; Rastall, R.; Klinder, A.

674

Inhibition of Salmonella Typhi murium by tannins in vitro. J. Food, Agric. Environ. 2011, 9,

675

119–124.

676

(44)

Taguri, T.; Tanaka, T.; Kouno, I. Antimicrobial Activity of 10 Different Plant Polyphenols


Page 29 of 48

677 678


against Bacteria Causing Food-Borne Disease. Biol. Pharm. Bull 2004, 27, 1965–1969. (45)

Van Parys, A.; Boyen, F.; Dewulf, J.; Haesebrouck, F.; Pasmans, F. The use of tannins to

679

control salmonella typhimurium infections in pigs. Zoonoses Public Health 2008, 57, 423–

680

428.

681

(46)

Min, E. R.; Pinchak, W. E.; Anderson, R. C.; Callaway, T. R. Effect of tannins on the in vitro

682

growth of Escherichia coli O157:H7 and in vivo growth of generic Escherichia coli excreted

683

from steers. J. Food Prot. 2007, 70, 543–550.

684

(47)

Elizondo, A. M.; Mercado, E. C.; Rabinovitz, B. C.; Fernandez-Miyakawa, M. E. Effect of

685

tannins on the in vitro growth of Clostridium perfringens. Vet. Microbiol. 2010, 145, 308–

686

314.

687

(48)

Tosi, G.; Massi, P.; Antongiovanni, M.; Buccioni, A.; Minieri, S.; Marenchino, L.; Mele, M.

688

Efficacy test of a hydrolysable tannin extract against necrotic enteritis in challenged broiler

689

chickens. Ital. J. Anim. Sci. 2013, 12, 386–389.

690

(49)

Lupini, C.; Cecchinato, M.; Scagliarini, A.; Graziani, R.; Catelli, E. In vitro antiviral activity

691

of chestnut and quebracho woods extracts against avian reovirus and metapneumovirus. Res.

692

Vet. Sci. 2009, 87, 482–487.

693

(50)

Quideau, S.; Varadinova, T.; Karagiozova, D.; Jourdes, M.; Pardon, P.; Baudry, C.; Genova,

694

P.; Diakov, T.; Petrova, R. Main structural and stereochemical aspects of the antiherpetic

695

activity of nonahydroxyterphenoyl-containing C-glycosidic ellagitannins. Chem. Biodivers.

696

2004, 1, 247–258.

697

(51)

698 699

N.L.Butter; J.M.Dawson; D.Wakelin; P.J.Buttery. Effect of dietary condensed tannins on gastrointestinal. J. Agric. Sci. Cambridge 2001, 137, 461–469.

(52)

Marzoni, M.; Castillo, A.; Romboli, I. Dietary inclusion of Quebracho (Schinopsis lorentzii)

700

tannins on productive performances of growing pheasant females. Ital. J. Anim. Sci. 2016, 4,

701

507–509.



702

(53)

703 704

Page 30 of 48

Athanasiadou, S.; Kyriazakis, I.; Jackson, F.; Coop, R. L. Effects of short-term exposure to condensed tannins on adult Trichostrongylus colubriformis. Vet. Rec. 2000, 146, 728–732.

(54)

Cejas, E.; Pinto, S.; Prosdócimo, F.; Batallé, M.; Barrios, H.; Tellez, G.; de Franceschi, M.

705

Evaluation of quebracho red wood (Schinopsis lorentzii) polyphenols vegetable extract for

706

the reduction of coccidiosis in broiler chicks. International Journal of Poultry Science. 2011,

707

pp 344–349.

708

(55)

Simlai, A.; Roy, A. Analysis of and correlation between phytochemical and antimicrobial

709

constituents of Ceriops decandra, a medicinal mangrove plant, from Indian Sundarban

710

estuary. J. Med. Plants Res. 2012, 6, 4755–4765.

711

(56)

Min, B. R.; Pinchak, W. E.; Merkel, R.; Walker, S.; Tomita, G.; Anderson, R. C.

712

Comparative antimicrobial activity of tannin extracts from perennial plants on mastitis

713

pathogens. Sci. Res. Essay 2008, 3, 66–73.

714

(57)

Trentin, D. S.; Silva, D. B.; Amaral, M. W.; Zimmer, K. R.; Silva, M. V.; Lopes, N. P.;

715

Giordani, R. B.; Macedo, A. J. Tannins Possessing Bacteriostatic Effect Impair Pseudomonas

716

aeruginosa Adhesion and Biofilm Formation. PLoS One 2013, 8, e66257.

717

(58)

Song, S.; Choi, B.; Kim, S.; Yoo, Y.; Kim, M.; Park, S.; Roh, S.; Kim, C.; Kim, S.; Yoo, Y.;

718

et al. Inhibitory effect of procyanidin oligomer from elm cortex on the matriz

719

metalloproteinases and proteases of periodontopathogens. J. Periodontal Res. 2003, 38, 282–

720

289.

721

(59)

Mohieldin, E. A. M.; Muddathir, A. M.; Mitsunaga, T. Inhibitory activities of selected

722

Sudanese medicinal plants on Porphyromonas gingivalis and matrix metalloproteinase-9 and

723

isolation of bioactive compounds from Combretum hartmannianum (Schweinf) bark. BMC

724

Complement. Altern. Med. 2017, 17, 1–11.

725 726

(60)

Ma, C. M.; Nakamura, N.; Hattori, M.; Kakuda, H.; Qiao, J. C.; Yu, H. L. Inhibitory effects on HIV-1 protease of constituents from the wood of Xanthoceras sorbifolia. J. Nat. Prod.


Page 31 of 48

727 728

2000, 63, 238–242. (61)

729 730


Cheng, H. Y.; Lin, C. C.; Lin, T. C. Antiherpes simplex virus type 2 activity of casuarinin from the bark of Terminalia arjuna Linn. Antiviral Res. 2002, 55, 447–455.

(62)

Ozdal, T.; Sela, D. A.; Xiao, J.; Boyacioglu, D.; Chen, F.; Capanoglu, E. The reciprocal

731

interactions between polyphenols and gut microbiota and effects on bioaccessibility.

732

Nutrients 2016, 8, 1–36.

733

(63)

734 735

Hogervorst Cvejić, J.; Atanacković Krstonošić, M.; Bursać, M.; Miljić, U. Polyphenols. Nutraceutical Funct. Food Components 2017, 203–258.

(64)

Oksman-Caldentey, K.-M.; Heinonen, M.; Hartmann-Schmidlin, S.; Nohynek, L.;

736

Puupponen-Pimia, R.; Kahkonen, M.; Maatta-Riihinen, K. Berry phenolics selectively inhibit

737

the growth of intestinal pathogens. J. Appl. Microbiol. 2005, 98, 991–1000.

738

(65)

Masumoto, S.; Terao, A.; Yamamoto, Y.; Mukai, T.; Miura, T.; Shoji, T. Non-absorbable

739

apple procyanidins prevent obesity associated with gut microbial and metabolomic changes.

740

Sci. Rep. 2016, 6, 31208.

741

(66)

Koh, A.; De Vadder, F.; Kovatcheva-Datchary, P.; Bäckhed, F. From Dietary Fiber to Host

742

Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell 2016, 165, 1332–

743

1345.

744

(67)

Molino, S.; Fernández-Miyakawa, M.; Giovando, S.; Rufián-Henares, J. Á. Study of

745

antioxidant capacity and metabolization of quebracho and chestnut tannins through in vitro

746

gastrointestinal digestion-fermentation. J. Funct. Foods 2018, 49, 188–195.

747

(68)

Aura, A.-M.; Ismo, M.; Hyötyläinen, T.; Peddinti, G.; Cheynier, V.; Souquet, J.-M.; Magali,

748

B.; Le Bourvellec, C.; Guyot, S.; Orešič, M. Characterization of microbial metabolism of

749

Syrah grape products in an in vitro colon model using targeted and non-targeted analytical

750

approaches. Eur J Nutr 2013, 52, 833–846.

751

(69)

Gibson, G. R.; Hutkins, R.; Sanders, M. E.; Prescott, S. L.; Reimer, R. A.; Salminen, S. J.;



Page 32 of 48

752

Scott, K.; Stanton, C.; Swanson, K. S.; Cani, P. D.; et al. Expert consensus document: The

753

International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus

754

statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017,

755

14, 491–502.

756

(70)

757 758

Li, S.; Wilkinson, K. L.; Bindon, K. A. Compositional variability in commercial tannin and mannoprotein products. Am. J. Enol. Vitic. 2018, 69, 176–181.

(71)

Brahem, M.; Renard, C. M. G. C.; Bureau, S.; Watrelot, A. A.; Le Bourvellec, C. Pear

759

ripeness and tissue type impact procyanidin-cell wall interactions. Food Chem. 2019, 275,

760

754–762.

761

(72)

Symoneaux, R.; Chollet, S.; Bauduin, R.; Le Quéré, J. M.; Baron, A. Impact of apple

762

procyanidins on sensory perception in model cider (part 2): Degree of polymerization and

763

interactions with the matrix components. LWT - Food Sci. Technol. 2014, 57, 28–34.

764

(73)

McManus, J. P.; Davis, K. G.; Beart, J. E.; Gaffney, S. H.; Lilley, T. H.; Haslam, E.

765

Polyphenol interactions. Part 1. Introduction; some observations on the reversible

766

complexation of polyphenols with proteins and polysaccharides. J. Chem. Soc. Perkin Trans.

767

2 1985, 0, 1429.

768

(74)

Carn, F.; Guyot, S.; Baron, A.; Pe, J.; Buhler, E.; Zanchi, E. Structural Properties of

769

Colloidal Complexes between Condensed Tannins and Polysaccharide Hyaluronan.

770

Biomacromolecules 2012, 13, 751–759.

771

(75)

772 773

Victor de Freitas; Nuno Mateus. Protein/Polyphenol Interactions: Past and Present Contributions. Mechanisms of Astringency Perception. Curr. Org. Chem. 2012, 16, 724–746.

(76)

Renard, C. M. G. C.; Watrelot, A. A.; Le Bourvellec, C. Interactions between polyphenols

774

and polysaccharides: Mechanisms and consequences in food processing and digestion.

775

Trends Food Sci. Technol. 2017, 60, 43–51.

776

(77)

Baxter, N. J.; Lilley, T. H.; Haslam, E.; Williamson, M. P. Multiple Interactions between


Page 33 of 48


777

Polyphenols and a Salivary Proline-Rich Protein Repeat Result in Complexation and

778

Precipitation †. Biochemistry 1997, 36, 5566–5577.

779

(78)

Escot, S.; Feuillat, M.; Dulau, L.; Charpentier, C. Release of polysaccharides by yeasts and

780

the influence of released polysaccharides on colour stability and wine astringency. Aust. J.

781

Grape Wine Res. 2001, 7, 153–159.

782

(79)

Mateus, N.; Carvalho, E.; Luı́s, C.; de Freitas, V. Influence of the tannin structure on the

783

disruption effect of carbohydrates on protein–tannin aggregates. Anal. Chim. Acta 2004, 513,

784

135–140.

785

(80)

Brandão, E.; Silva, M. S.; García-Estévez, I.; Williams, P.; Mateus, N.; Doco, T.; de Freitas,

786

V.; Soares, S. The role of wine polysaccharides on salivary protein-tannin interaction: A

787

molecular approach. Carbohydr. Polym. 2017, 177, 77–85.

788

(81)

789 790

wine—effect of wine polysaccharides. Food Hydrocoll. 2002, 16, 17–23. (82)

791 792

Riou, V.; Vernhet, A.; Doco, T.; Moutounet, M. Aggregation of grape seed tannins in model

Kawamoto, H.; Nakatsubo, F. Effects of environmental factors on two-stage tannin-protein co-precipitation. Phytochemistry 1997, 46, 479–483.

(83)

Sarni-Manchado, P.; Canals-Bosch, J.-M.; Mazerolles, E.; Eronique Cheynier, V. Influence

793

of the Glycosylation of Human Salivary Proline-Rich Proteins on Their Interactions with

794

Condensed Tannins. J. Agric. Food Chem. 2008, 56, 9563–9569.

795

(84)

796 797

Human Salivary Histatins. J. Agric. Food Chem. 1999, 47, 2229−2234. (85)

798 799

Livney, Y. D. Milk proteins as vehicles for bioactives. Curr. Opin. Colloid Interface Sci. 2010, 15, 73–83.

(86)

800 801

Naurato, N.; Wong, P.; Lu, Y.; Wroblewski, K.; Bennick, A. Interaction of Tannin with

van het Hof, K. H.; Kivits, G. A.; Weststrate, J. A.; Tijburg, L. B. Bioavailability of catechins from tea: the effect of milk. Eur. J. Clin. Nutr. 1998, 52, 356–359.

(87)

Lee, C. B.; Lawless, H. T. Time-course of astringent sensations. Chem. Senses 1991, 16,



802 803

Page 34 of 48

225–238. (88)

Silva, M. S.; García-Estévez, I.; Brandão, E.; Mateus, N.; De Freitas, V.; Soares, S.

804

Molecular Interaction between Salivary Proteins and Food Tannins. J. Agric. Food Chem.

805

2017, 65, 6415–6424.

806

(89)

807 808

Brossaud, F.; Cheynier, V.; Noble, A. C. Bitterness and astringency of grape and wine polyphenols. Aust. J. Grape Wine Res. 2001, 7, 33–39.

(90)

Ferrer-Gallego, R.; Brás, N. F.; García-Estévez, I.; Mateus, N.; Rivas-Gonzalo, J. C.; de

809

Freitas, V.; Escribano-Bailón, M. T. Effect of flavonols on wine astringency and their

810

interaction with human saliva. Food Chem. 2016, 209, 358–364.

811

(91)

812 813

Peleg, H.; Gacon, K.; Schlich, P.; Noble, A. C. Bitterness and astringency of flavan-3-ol monomers, dimers and trimers. J. Sci. Food Agric. 1999, 79, 1123–1128.

(92)

Pascal, C.; Paté, F.; Cheynier, V.; Delsuc, M.-A. Study of the interactions between a proline-

814

rich protein and a flavan-3-ol by NMR: Residual structures in the natively unfolded protein

815

provides anchorage points for the ligands. Biopolymers 2009, 91, 745–756.

816

(93)

Obreque-Slier, E.; Lopez-Solis, R.; Peña-Neira, Á.; Zamora-Marín, F. Tannin-protein

817

interaction is more closely associated with astringency than tannin-protein precipitation:

818

Experience with two oenological tannins and a gelatin. Int. J. Food Sci. Technol. 2010, 45,

819

2629–2636.

820

(94)

821 822

seed procyanidins with oral epithelial cells. Food Chem. 2009, 115, 551–557. (95)

823 824

Payne, C.; Bowyer, P. K.; Herderich, M.; Bastian, S. E. P. Interaction of astringent grape

Llaudy, M. C.; Canals, R.; Canals, J. M.; Roz??s, N.; Arola, L.; Zamora, F. New Method for Evaluating Astringency in Red Wine. J. Agric. Food Chem. 2004, 52, 742–746.

(96)

Carvalho, E.; Mateus, N.; Plet, B.; Pianet, I.; Dufourc, E.; De Freitas, V. Influence of Wine

825

Pectic Polysaccharides on the Interactions between Condensed Tannins and Salivary

826

Proteins. J. Agric. Food Chem. 2006, 54, 8936–8944.


Page 35 of 48

827

(97)

828 829

Ozawa, T.; Lilley, T. H.; Haslam, E. Polyphenol interactions: astringency and the loss of astringency in ripening fruit. Phytochemistry 1987, 26, 2937–2942.

(98)

830 831


García-Estévez, I.; Pérez-Gregorio, R.; Soares, S.; Mateus, N.; De Freitas, V. Oenological perspective of red wine astringency. J. Int. des Sci. la Vigne du Vin 2017, 51, 237–249.

(99)

Soares, S.; Silva, M. S.; García-Estevez, I.; Groβmann, P.; Brás, N.; Brandão, E.; Mateus, N.;

832

De Freitas, V.; Behrens, M.; Meyerhof, W. Human Bitter Taste Receptors Are Activated by

833

Different Classes of Polyphenols. J. Agric. Food Chem. 2018, 66, 8814–8823.

834

(100) Bohin, M. C.; Roland, W. S. U.; Gruppen, H.; Gouka, R. J.; Van Der Hijden, H. T. W. M.;

835

Dekker, P.; Smit, G.; Vincken, J.-P. Evaluation of the Bitter-Masking Potential of Food

836

Proteins for EGCG by a Cell-Based Human Bitter Taste Receptor Assay and Binding

837

Studies. J. Agric. Food Chem. 2013, 61, 10010–10017.

838 839

(101) Hufnagel,

J.

C.;

Hofmann,

T.

Quantitative

Reconstruction

of

the

Nonvolatile

Sensometabolome of a Red Wine. J. Agric. Food Chem. 2008, 56, 9190–9199.

840

(102) OIV. International Oenological Codex, Oenological Tannins INS N°: 181; 2009.

841

(103) Salagoity-Auguste, M.; Tricard, C.; Marsal, F.; Sudraud, P. Preliminary Investigation for the

842

Differentiation of Enological Tannins According to Botanical Origin: Determination of

843

Gallic Acid and Its Derivatives. Am. J. Enol. Vitic. 1986, 37, 301–303.

844

(104) Bautista-Ortín, A. B.; Martínez-Cutillas, A.; Ros-García, J. M.; López-Roca, J. M.; Gómez-

845

Plaza, E. Improving colour extraction and stability in red wines: The use of maceration

846

enzymes and enological tannins. Int. J. Food Sci. Technol. 2005, 40, 867–878.

847

(105) Harbertson, J. F.; Parpinello, G. P.; Heymann, H.; Downey, M. O. Impact of exogenous

848

tannin additions on wine chemistry and wine sensory character. Food Chem. 2012, 131, 999–

849

1008.

850

(106) Vivas, N., Vivas De Gaulejac, N. and Nonier, M. F. (2002). Mise au point sur les tanins

851

oenologiques et bases d’une nouvelle définition qualitative. Setting up enological tannins and



852 853 854

Page 36 of 48

bases for a new qualitative definition. Bull. O.I.V. 2002, 853–854, 175–185. (107) Rinaldi, A.; Moio, L. Effect of enological tannin addition on astringency subqualities and phenolic content of red wines. J. Sens. Stud. 2018, 33, 1–11.

855

(108) Chen, K.; Escott, C.; Loira, I.; Del Fresno, J. M.; Morata, A.; Tesfaye, W.; Calderon, F.;

856

Benito, S.; Suárez-Lepe, J. A. The effects of pre-fermentative addition of oenological tannins

857

on wine components and sensorial qualities of red wine. Molecules 2016, 21, 1–17.

858

(109) Cheynier, V.; Dueñas-Paton, M.; Salas, E.; Maury, C.; Souquet, J. M.; Sarni-Manchado, P.;

859

Fulcrand, H. Structure and properties of wine pigments and tannins. Am. J. Enol. Vitic. 2006,

860

57, 298–305.

861

(110) Kyraleou, M.; Teissedre, P. L.; Tzanakouli, E.; Kotseridis, Y.; Proxenia, N.; Chira, K.; Ligas,

862

I.; Kallithraka, S. Addition of wood chips in red wine during and after alcoholic

863

fermentation: Differences in color parameters, phenolic content and volatile composition. J.

864

Int. des Sci. la Vigne du Vin 2016, 50, 209–222.

865 866

(111) Baiano, A.; De Gianni, A. Timing of the treatment with oak chips: the case of Nero di Troia wine. Eur. Food Res. Technol. 2016, 242, 1343–1353.

867

(112) García-Carpintero, E. G.; Gómez Gallego, M. A.; Sánchez-Palomo, E.; González Viñas, M.

868

A. Sensory descriptive analysis of Bobal red wines treated with oak chips at different stages

869

of winemaking. Aust. J. Grape Wine Res. 2011, 17, 368–377.

870

(113) Grossman, S.; Bergman, M. Process for the production of gelatin from fish skins, 1992.

871

(114) Kaewudom, P.; Benjakul, S.; Kijroongrojana, K. Properties of surimi gel as influenced by

872

fish gelatin and microbial transglutaminase. Food Biosci. 2013, 1, 39–47.

873

(115) Oujifard, A.; Benjakul, S.; Ahmad, M.; Seyfabadi, J. Effect of bambara groundnut protein

874

isolate on autolysis and gel properties of surimi from threadfin bream (Nemipterus bleekeri).

875

LWT - Food Sci. Technol. 2012, 47, 261–266.

876

(116) Chambi, H.; Grosso, C. Edible films produced with gelatin and casein cross-linked with


Page 37 of 48

877 878 879


transglutaminase. Food Res. Int. 2006, 39, 458–466. (117) Balange, A.; Benjakul, S. Enhancement of gel strength of bigeye snapper (Priacanthus tayenus) surimi using oxidised phenolic compounds. Food Chem. 2009, 113, 61–70.

880

(118) Chanthachum, S.; Beuchat, L. R. Inhibitory effect of kiam (Cotylelobium lanceotatum craih).

881

Wood extract on gram-positive food-borne pathogens and spoilage micro-organisms. Food

882

Microbiol. 1997, 14, 603–608.

883 884 885 886

(119) Balange, A. K.; Benjakul, S. Use of kiam wood extract as gel enhancer for mackerel ( Rastrelliger kanagurta ) surimi. Int. J. Food Sci. &Technology 2009, 44, 1661–1669. (120) Temdee, W.; Benjakul, S. Effect of oxidized kiam wood and cashew bark extracts on gel properties of gelatin from cuttle fi sh skins. Food Biosci. 2014, 7, 95–104.

887

(121) Buamard, N.; Benjakul, S. Ethanolic coconut husk extract: In vitro antioxidative activity and

888

effect on oxidative stability of shrimp oil emulsion. Eur. J. Lipid Sci. Technol. 2017, 119,

889

1700131.

890 891 892 893

(122) Buamard, N.; Benjakul, S. Improvement of gel properties of sardine (Sardinella albella) surimi using coconut husk extracts. Food Hydrocoll. 2015, 51, 146–155. (123) Jiménez-Colmenero, F.; Carballo, J.; Cofrades, S. Healthier meat and meat products: their role as functional foods. Meat Sci. 2001, 59, 5–13.

894

(124) Wood, J. .; Richardson, R. .; Nute, G. .; Fisher, A. .; Campo, M. .; Kasapidou, E.; Sheard, P.

895

.; Enser, M. Effects of fatty acids on meat quality: a review. Meat Sci. 2004, 66, 21–32.

896

(125) Nikmaram, N.; Budaraju, S.; Barba, F. J.; Lorenzo, J. M.; Cox, R. B.; Mallikarjunan, K.;

897

Roohinejad, S. Application of plant extracts to improve the shelf-life, nutritional and health-

898

related properties of ready-to-eat meat products. Meat Sci. 2018, 145, 245–255.

899

(126) Botterweck, A. A. M.; Verhagen, H.; Goldbohm, R. A.; Kleinjans, J.; Van Den Brandt, P. A.

900

Research Section Intake of Butylated Hydroxyanisole and Butylated Hydroxytoluene and

901

Stomach Cancer Risk: Results from Analyses in the Netherlands Cohort Study. Food Chem.



902

Page 38 of 48

Toxicol. 2000, 38, 599–605.

903

(127) Redondo, L. M.; Chacana, P. A.; Dominguez, J. E.; Fernandez Miyakawa, M. E. Perspectives

904

in the use of tannins as alternative to antimicrobial growth promoter factors in poultry. Front.

905

Microbiol. 2014, 5, 1–7.

906 907 908 909

(128) Iji, P. The future of tannins in animal nutrition. In Recent Progress in Medicinal Plants; 2015; pp 335–345. (129) Candan, T.; Aytunga, B. Use of Natural Antioxidants in Poultry Meat. CBU J. Sci. 2017, 13, 279–291.

910

(130) Rezar, V.; Salobir, J.; Levart, A.; Tomažin, U.; Škrlep, M.; Batorek Lukač, N.; Čandek-

911

Potokar, M. Supplementing entire male pig diet with hydrolysable tannins: Effect on carcass

912

traits, meat quality and oxidative stability. Meat Sci. 2017, 133, 95–102.

913

(131) Liu, H.; Zhou, D.; Tong, J.; Vaddella, V. Influence of chestnut tannins on welfare, carcass

914

characteristics, meat quality, and lipid oxidation in rabbits under high ambient temperature.

915

Meat Sci. 2012, 90, 164–169.

916

(132) Dalle Zotte, A.; Cullere, M.; Tasoniero, G.; Gerencsér, Z.; Szendrő, Z.; Novelli, E.; Matics,

917

Z. Supplementing growing rabbit diets with chestnut hydrolyzable tannins: Effect on meat

918

quality and oxidative status, nutrient digestibilities, and content of tannin metabolites. Meat

919

Sci. 2018, 146, 101–108.

920 921 922 923

(133) Dalle Zotte, A.; Cossu, M. Dietary inclusion of tannin extract from red quebracho trees (Schinopsos spp.) in the rabbit meat production. Ital. J. Anim. Sci. 2009, 8, 784–786. (134) Lee, J. H.; Min, B. R.; Lemma, B. B. Quality characteristics of goat meat as influenced by condensed tannins-containing pine bark. Small Rumin. Res. 2017, 146, 28–32.

924

(135) EU. EU Guidance to the Commission Regulation (EC) No 450/2009 of 29 May 2009 on

925

Active and Intelligent Materials and Articles Intended to Come into Contact with Food;

926

2009; Vol. 450, p L 135/3-135/11.


Page 39 of 48


927

(136) Sung, S. H.; Kim, K. H.; Jeon, B. T.; Cheong, S. H.; Park, J. H.; Kim, D. H.; Kweon, H. J.;

928

Moon, S. H. Antibacterial and antioxidant activities of tannins extracted from agricultural by-

929

products. J. Med. Plants Res. 2012, 6, 3072–3079.

930

(137) Lopez De Dicastillo, C.; Ner, C.; Alfaro, P.; On Catal, R.; Gavara, R.; Hern Andez-Mu~

931

Noz, P. Development of New Antioxidant Active Packaging Films Based on Ethylene Vinyl

932

Alcohol Copolymer (EVOH) and Green Tea Extract. J. Agric. Food Chem 2011, 59, 7832–

933

7840.

934 935

(138) Fang, Z.; Zhao, Y.; Warner, R. D.; Johnson, S. K. Active and intelligent packaging in meat industry. Trends Food Sci. Technol. 2017, 61, 60–71.

936

(139) Anwer, M. A. S.; Naguib, H. E.; Celzard, A.; Fierro, V. Comparison of the thermal, dynamic

937

mechanical and morphological properties of PLA-Lignin & PLA-Tannin particulate

938

green composites. Compos. Part B Eng. 2015, 82, 92–99.

939

(140) García, D. E.; Carrasco, J. C.; Salazar, J. P.; Pérez, M. A.; Cancino, R. A.; Riquelme, S. Bark

940

polyflavonoids from pinus radiata as functional building-blocks for polylactic acid (PLA)-

941

based green composites. Express Polym. Lett. 2016, 10, 835–848.

942

(141) Zhai, Y.; Wang, J.; Wang, H.; Song, T.; Hu, W.; Li, S.; Zhai, Y.; Wang, J.; Wang, H.; Song,

943

T.; et al. Preparation and Characterization of Antioxidative and UV-Protective Larch Bark

944

Tannin/PVA Composite Membranes. Molecules 2018, 23, 2073.

945

(142) Peña-Rodriguez, C.; Martucci, J. F.; Neira, L. M.; Arbelaiz, A.; Eceiza, A.; Ruseckaite, R. A.

946

Functional properties and in vitro antioxidant and antibacterial effectiveness of pigskin

947

gelatin films incorporated with hydrolysable chestnut tannin. Food Sci. Technol. Int. 2015,

948

21, 221–231.

949 950 951

(143) Mangang, K. C. S.; Das, A. J.; Deka, S. C. Shelf Life Improvement of Rice Beer by Incorporation of Albizia myriophylla Extracts. J. Food Process. Preserv. 2017, 41, e12990. (144) Horita, C. N.; Baptista, R. C.; Caturla, M. Y. R.; Lorenzo, J. M.; Barba, F. J.; Sant’Ana, A. S.



reformulation,

active

packaging

and

Page 40 of 48

952

Combining

non-thermal

post-packaging

953

decontamination technologies to increase the microbiological quality and safety of cooked

954

ready-to-eat meat products. Trends Food Sci. Technol. 2018, 72, 45–61.

955

(145) Országhová, Z.; Waczulíková, I.; Burki, C.; Rohdewald, P.; Ďuračková, Z. An Effect of Oak-

956

Wood Extract (Robuvit®) on Energy State of Healthy Adults-A Pilot Study. Phytother. Res.

957

2015, 29, 1219–1224.

958

(146) Belcaro, G.; Cornelli, U.; Luzzi, R.; Cesarone, M. R.; Dugall, M.; Feragalli, B.; Hu, S.;

959

Pellegrini, L.; Ippolito, E. Improved management of primary chronic fatigue syndrome with

960

the supplement French oak wood extract (Robuvit®): a pilot, registry evaluation.

961

Panminerva Med. 2014, 56, 63–72.

962

(147) Vinciguerra, M. G.; Belcaro, G.; Cacchio, M. Robuvit® and endurance in triathlon:

963

improvements in training performance, recovery and oxidative stress. Minerva Cardioangiol.

964

2015, 63, 403–409.


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Figure captions Figure 1. Classification of Tannins Figure 2. Scheme of Tannin-Protein and Tannin-Polysaccharide Interactions



Page 42 of 48

Figure 1

TANNINS

Hydrolysable Tannins Ellagitannins Precursor structure

Hexahydroxydiphenic acid

Condensed Tannins

Complex Tannins

Precursor structures (+)-catechin (–)-epicatechin (+)-afzelechin (–)-epiafzelechin (–)-gallocatechin (–)-epigallocatechin

Structures which contain catechin unit bound to either an ellagitannin or a gallotannin unit.

(+)-catechin

Gallotannins Example of complex tannins: Acutissimin A

Precursor structure

Gallic acid


Phlorotannins

Phloroglucinol

Page 43 of 48


Figure 2



Page 44 of 48

Table 1. Antimicrobial Effects Of Tannins Wood Extracts

Plant species

Micro-organism targeted

References

Anadenanthera colubrine (bark)

Pseudomonas aeruginosa

57

Castanea sativa (wood and bark)

Clostridium perfringens

47,48

Salmonella Typhimurium

43,45

Campylobacter jejuni

42

Escherichia coli, Escherichia coli O157:H7

46

Staphylococcus aureus, Vibrio spp, Salmonella spp, enteropathogenic Escherichia coli

44

Avian reovirus and metapneumovirus

49

Herpes simplex virus

50

Ceriops decandra (wood and bark)

Bacillus subtilis, Bacillus coagulans, Escherichia coli, Proteus vulgaris

55

Combretum hartmannianum (bark)

Porphyromonas gingivalis

59

Commiphora leptophloeos (bark)


57

Elaeocarpus sylvestris var. Ellipticus (wood)

Staphylococcus aureus, Vibrio spp, Salmonella spp, Escherichia coli

44

Myracrodruon urundeuva (bark)


57

Pterocarpus marsupium (wood)

Staphylococcus aureus, Bacillus cereus

37

Punica granatum (rind)

Staphylococcus aureus, Vibrio spp, Salmonella spp, Escherichia coli

44

Quercus robur (wood)

Herpes simplex virus

50

Schinopsis lorentzii (wood)

Clostridium perfringens

47

Salmonella Typhimurium

43

Campylobacter jejuni

42

Helminthes

51–53

Eimeria spp

54

Avian reovirus, metapneumoviru

49

Porphyromonas gingivalis

59

Terminalia spp (wood and bark)


Page 45 of 48


Ulmi macrocarpa (cortex)

Herpes simplex virus type 2

61

Uncaria tomentosa (wood and bark)

Porphyromonas gingivalis, Treponema denticola

58

Walsura robusta (wood)

Staphylococcus aureus, Enterococcus faecalis, Pseudomonas aeruginosa

27

Xanthoceras sorbifolia (wood)

Escherichia coli O157:H7

56

Terminalia spp (wood and bark)

Human Immunodeficiency Virus

60



Graphic for Table Of Content


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Page Journal 47 ofof48 Agricultural and Food Chemistry

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Natural Tannin Wood Extracts as a Potential Food Ingredient in the

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