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Natural Antioxidants: Sources, Compounds, Mechanisms of Action, and Potential Applications

M.S. Brewer Abstract: While use of synthetic antioxidants (such as butylated hydroxytoluene and butylated hydroxyanisole) to maintain the quality of ready-to-eat food products has become commonplace, consumer concern regarding their safety has motivated the food industry to seek natural alternatives. Phenolic antioxidants can inhibit free radical formation and/or interrupt propagation of autoxidation. Fat-soluble vitamin E (-tocopherol) and water-soluble vitamin C (L-ascorbic acid) are both effective in the appropriate matrix. Plant extracts, generally used for their avoring characteristics, often have strong H-donating activity thus making them extremely effective antioxidants. This antioxidant activity is most often due to phenolic acids (gallic, protocatechuic, caffeic, and rosmarinic acids), phenolic diterpenes (carnosol, carnosic acid, rosmanol, and rosmadial), avonoids (quercetin, catechin, naringenin, and kaempferol), and volatile oils (eugenol, carvacrol, thymol, and menthol). Some plant pigments (anthocyanin and anthocyanidin) can chelate metals and donate H to oxygen radicals thus slowing oxidation via 2 mechanisms. Tea and extracts of grape seeds and skins contain catechins, epicatechins, phenolic acids, proanthocyanidins, and resveratrol, all of which contribute to their antioxidative activity. The objective of this article is to provide an overview of natural antioxidants, their mechanisms of action, and potential applications.

Introduction
Ultimately, food quality is dened in terms of consumer acceptability: taste, aroma, and appearance characteristics. The increasing demand for convenient foods has led to rapid growth in the ready-to-eat product category (Hofstrand 2008). Many of the food ingredients contain unsaturated fatty acids that are quite susceptible to quality deterioration, especially under oxidative stress. For this reason, efforts to reduce oxidation have increased. Most often, the best strategy is the addition of antioxidants. Synthetic phenolic antioxidants (butylated hydroxyanisole [BHA], butylated hydroxytoluene [BHT], and propyl gallate) effectively inhibit oxidation; chelating agents, such as ethylene diamine tetra acetic acid (EDTA), can bind metals reducing their contribution to the process. Some vitamins (ascorbic acid [AA] and -tocopherol), many herbs and spices (rosemary, thyme, oregano, sage, basil, pepper, clove, cinnamon, and nutmeg), and plant extracts (tea and grapeseed) contain antioxidant components as well (Hinneburg and others 2006). Natural phenolic antioxidants, such as synthetics, can effectively scavenge free radicals, absorb light in the ultraviolet (UV) region (100 to 400 nm), and chelate transition metals, thus stopping progressive autoxidative damage and production of off-odors and off-tastes.
MS 20101442 Submitted 10/22/2010, Accepted 3/8/2011. Author is with the Dept. of Food Science and Human Nutrition, 202 ABL, 1302 W Pennsylvania . Ave., Univ. of Illinois, Urbana, IL 61801, U.S.A. Direct inquiries to author Brewer (E-mail: msbrewer@uiuc.edu).

Since 1994, consumers have expressed concern about the safety of preservatives and additives in their food (Brewer and Russon 1994; Brewer and Prestat 2002; Rojas and Brewer 2008b). More than 12 y ago, Sloan (1999) reported that one of the top 10 trends for the food industry to watch included the sales of natural, organic, and vegetarian foods. There is a clear trend in consumer preference for clean labeling (Hillmann 2010), for food ingredients and additives that are organic/natural with names that are familiar, and that are perceived to be healthy (Joppen 2006). In addition, the call for sustainable sources and environmentally friendly production is forcing the food industry to move in that direction (Berger 2009). Defrancesco and Trestini (2008) estimated that consumers were willing to pay a price premium (up to 70% more) for organic fresh produce (tomatoes) for their health-promoting antioxidant content. Of an estimated $17 billion in sales in the United States, organic foods account for only 3% of total retail food sales. This category has been growing at 7 times the rate of the average food category and has maintained a growth rate of more than 15% per year. However, based on the results of a recent study, Evans and others (2010) concluded that products with physical changes, less processing, with identiable ingredients would also be perceived to be more natural. Consumer expectations about ingredients that may suitably be labeled as natural do not always coincide with current guidelines (Williams and others 2009). A clear denition can guide manufacturers. However, the lack of consumer consensus makes it difcult for them to understand the implications. For consumers, natural

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and clean label are related to what they perceive an ingredient to be. This article provides an overview of naturally occurring antioxidant compounds, their sources, and mechanisms of action. Various different mechanisms may contribute to oxidative processes in complex systems, such as foods. These include reactions that generate reactive oxygen species that target different structures (lipids, proteins, and carbohydrates), and Fenton reactions, where transition metal ions play a vital role. It should be noted that antioxidant activity of food extracts can be determined using a variety of tests (stable free radical scavengers: galvinoxyl, diphenylb-picrylhydrazyl [DPPH]; lipid oxidation: peroxide oxygen, conjugated dienes, Rancimat [measurements of oxygen consumption of a linoleic acid emulsion and oxidation induction period in lard at 100 C], oxygen radical absorbance capacity [ORAC] values ), active oxygen method, iodine value (measure of the change in number of double bonds that bind I), anisidine value (reaction of acetic acid p-anisidine and aldehydes to produce a yellow color that absorbs at 350 nm), measurement of absorbance at 234 nm (conjugated dienes) and 268 nm (conjugated trienes) to assess oxidation in the early stages, and chromatographic methods; however, extraction procedures strongly inuence the composition of the extracts and, therefore, also inuence the antioxidant activity results (Halliwell 1997; Schwarz and others 2001; Trojakova and others 2001). In addition, the effect of the antioxidant compound in a food matrix may be signicantly different than the activity of a puried extract.
Table 1Flavors and aromas associated with volatile compounds resulting from lipid oxidation. Compound Butanoic acid Propanoic acid Pentanal Hexanal Heptanal Octanal Nonanal Decanal Decanal 2-Nonenal 2-Hexenal Nona-2(E)-enal E-2-Hexenal E-2-Octenal E-2-Decenal E,E-Deca-2, 4-dienal E,E-Nona-2, 4-dienal 2-Propanone 3-Hydroxy-2-butanone 2,3-Octanedione Nonenone 2-Heptanone Dimethyl disulde Dimethyl trisulde Methanethiol Flavors and aromas Rancid Pungent, rancid, soy Pungent, malt Green, grassy, tallowy Green, oily, rancid Sweet, fatty, soapy Tallowy, waxy Rancid, burnt Soapy, tallowy Paper Rancid Tallowy, fatty Green, fat, rancid Fatty, nutty, green Green, pungent, Fatty, fried potato, green Green, grassy, fatty Livery Rancid, beany, grassy Oxidized fat or oil Pungent Soapy Onion, cabbage, putrid Sulfur, sh, cabbage Garlic, sulfur

Kerler and Grosch (1996), Yong and others (2000), Ahn and others (2002, 2007), Jensen and others (2002), Jo and others (2003), Mahrour and others (2003), Nam and Ahn (2003), Nam and others (2003), Acree and Arn (2004), Rochat and Chaintreau (2005), Obana and others (2006), and Yancey and others (2006).

Food Lipids
The fatty acids in the lipids of food tissues may be saturated or unsaturated and may be part of the neutral triglyceride fraction (triacylglycerol) or part of the phospholipid fraction. Free fatty acids are electron-decient at the oxygen atom of the carbonyl group (C=O); unsaturated fatty acids are also electron-decient at points of carboncarbon unsaturation (C=C). These electrondecient regions make fatty acids susceptible to attack by a variety of oxidizing and high-energy agents generating free radicals (Nawar 1996). Triglycerides contain straight chains of primarily 16- to 18-carbon fatty acids and minimal amounts of unsaturated fatty acids. Phospholipids in tissue membranes contain up to 15 times the amount of unsaturated fatty acids (C18:4, C20:4, C20:5, C22:5, and C22:6) found in triglycerides. They are much more susceptible to oxidation because of the increase in the number of points of carboncarbon unsaturation (C=C) (Elmore and others 1999).

primary products of lipid oxidation. They are tasteless and odorless; however, in the presence of heat, metal ions, and/or light, they can decompose to compounds that contribute r off-odors and offr tastes. Alkoxy radicals (RO ) can also abstract H from unsaturated fatty acids continuing the chain reaction (see nr 5 below; Decker r 2002; Srinivasan and others 2008). Hydroxyl radicals ( OH) can react with conjugated systems continuing the oxidation process. This chain reaction terminates when 2 radical species combine to form a nonradical species (see nr 6 below). Antioxidants (A:H) r inhibit the chain reaction by donating hydrogen atoms (H ) to radicals (see nr 7 below). The antioxidant free radical may then form a stable peroxy-antioxidant compound (see nr 8 below). (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) R:H + O::O + Initiator R + HOO r r R +r O::O ROO r ROO + R:H ROOH + R r r RO:OHr RO + HO r R::R +r OH R:R-O r Rr + R r R:R R +r ROO rROOR ROOr + ROO ROOR + O2 r ROOr + AH ROOH + A r ROO + A ROOA.
r r

Oxidation

When a hydrogen atom (H ) is abstracted r from an unsaturated fatty acid (R:H) forming an alkyl radical (R ), lipid oxidation is initiated (see nr 1 below). Generation of this lipid radical is thermodynamically unfavorable and r usually initiated by the presence is of other radical compounds (R ), singletstate oxygen (1 O2 ), decomposition of hydroperoxides (ROOH), or pigments that act as r photoensitizers. In order to stabilize, the alkyl radical (R ) usually undergoes a shift in the position of the double bond (cis to trans) r and production of a conjugated diene system. The R r can react with O2 to form a high-energy peroxyl radical (ROO ; see nr 2 below). The peroxyl radical can then abstract a hydrogen atom r (H ) from another unsaturated fatty acid (see nr 3 below) forming r a hydroperoxide (ROOH) and a new, free alkyl radical (R ). This process then propagates to another fatty acid (see nr 4 below; Srinivasan and others 2008). Lipid hydroperoxides (ROOH) are the

Ultimately, oxidation depends on the addition of oxygen to a compound; however, the energy level of the oxygen has a signicant impact on the ease of the oxidation reaction. Singlet state oxygen (1 O2 ) has spin-coupled electrons and is a nonradical, high-energy species (Decker 2002; Min and Boff 2002). It is electrophilic and can react with other electron-rich, nonradical, singlet state compounds containing double bonds (C=C, C=O). However, oxygen in its lowest energy state, triplet state oxygen (3 O2 ), has 2 unpaired, parallel spin electrons. It is very reactive (primarily with radical species). Most food components, such as carbohydrates and proteins, are nonradical (singlet state) and are relatively unreactive with triplet state oxygen (3 O2 ); however, they
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are reactive with singlet state oxygen (1 O2 ) that can be generated in response to temperature change, reduction of activation energy (presence of transition metals), exposure to UV light, and physical damage to tissues. Singlet oxygen and free radicals can cause biological damage to macromolecules and membrane constituents. The presence of natural antioxidants may help control these degradative reactions. Oxidation of unsaturated fatty acids can produce a variety of aldehydes, alkanals, alkenes, and alkanes; many of which contribute off-odors that are perceptible at very low concentrations. Odor detection thresholds for pentanal, hexanal, and heptanal, compounds typically generated from the breakdown of oxidized linoleic acid have been reported to be <34, <38, and 62 ppb, respectively, in a gelatin model system (Vega and Brewer 1995). The odors of a variety of oxidation-generated compounds are shown in Table 1.
Table 2Total ORAC values (m TE/100 g; Prior and others 2003) of selected herbs and spices, berries, roots, and teas. Food Basil (fresh) Marjoram (fresh) Oregano (fresh) Sage (fresh) Savory (fresh) Basil (dried) Cinnamon (ground) Clove (ground) Ginger (ground) Nutmeg (ground) Oregano (dried) Pepper, black Rosemary (dried) Sage (ground) Thyme (fresh) Thyme (dried) Turmeric (ground) Grapes (red, raw) Raspberries (raw) Garlic (raw) Ginger root (raw) Onions, red (raw) Tea brewed Tea, green, brewed Total ORAC 4805 27297 13970 32004 9465 61063 131420 290283 39041 69640 175295 34053 165280 119929 27426 157380 127068 1837 5065 5708 14840 1521 1128 1253 SEM 225 1306 545 1548 436 2280 13867 3292 1835 6859 7683 289 1391 20305 1251 1629 11181 248 205 475 530 69

Antioxidants
Antioxidants are compounds or systems that delay autoxidation by inhibiting formation of free radicals or by interrupting propagation of the free radical by one (or more) of several mechanisms: (1) scavenging species that initiate peroxidation, (2) chelating metal ions such that they are unable to generate reactive species or der compose lipid peroxides, (3) quenching O2 preventing formation of peroxides, (4) breaking the autoxidative chain reaction, and/or (5) reducing localized O2 concentrations (Nawar 1996). Chain-breaking antioxidants differ in their antioxidative effectiveness depending on their chemical characteristics and physical location within a food (proximity to membrane phospholipids, emulsion interfaces, or in the aqueous phase). The chemical potency of an antioxidant and solubility in oil inuence its accessibility to peroxy radicals especially in membrane, micellar and emulsion systems, and the amphiphilic character required for effectiveness in these systems (Wanatabe and others 2010). Antioxidant effectiveness is related to activation energy, rate constants, oxidationreduction potential, ease with which the antioxidant is lost or destroyed (volatility and heat susceptibility), and antioxidant solubility (Nawar 1996). In addition, inhibitor and chain propagation reactions are both exothermic. As the A:H and R:H bond dissociation energies increase, the activation increases and the antioxidant efciency decreases. Conversely, as these bond energies decrease, the antioxidant efciency increases. The most effective antioxidants are those that interrupt the free radical chain reaction. Usually containing aromatic or phenolic r rings, these antioxidants donate H to the free radicals formed during oxidation becoming a radical themselves (see step nr 7). These radical intermediates are stabilized by the resonance delocalization of the electron within the aromatic ring and formation of quinone structures (Nawar 1996). In addition, many of the phenolics lack positions suitable for molecular oxygen attack. Both synthetic antioxidants (BHA, BHT, and propyl gallate) and natural botanicals contain phenolics (avonoids) function in this manner. Botanical extracts with antioxidant activity generally quench free radical oxygen with phenolic compounds as well. Because bivalent transition metal ions, Fe2+ in particular, can catalyze oxidative processes, leading to formation of hydroxyl radicals, and can decompose hydroperoxides via Fenton reactions, chelating these metals can effectively reduce oxidation (Halliwell and others 1987). Food materials containing signicant amounts of these transition metals (red meat) can be particularly susceptible to metal-catalyzed reactions.
c

The oxygen radical absorbance capacity (ORAC) method is based on the inhibition of the peroxyl-radical-induced oxidation initiated by thermal decomposition of azo compounds. Prior and others (2003) used 2,2 -azo bis (2 amidino propane) dihydrochloride (AAPH) as the azo generator, incubated at 37 C for 30 min with uorescein (14 m) as a uorescent detector. Source: USDA (2010).

Natural Antioxidants
Food tissues, because they are (or were) living, are under constant oxidative stress from free radicals, reactive oxygen species, and prooxidants generated both exogenously (heat and light) and endogenously (H2 O2 and transition metals). For this reason, many of these tissues have developed antioxidant systems to control free radicals, lipid oxidation catalysts, oxidation intermediates, and secondary breakdown products (Nakatani 2003; Agati and others 2007; Brown and Kelly 2007; Chen 2008; Iacopini and others 2008). These antioxidant compounds include avonoids, phenolic acids, carotenoids, and tocopherols that can inhibit Fe3+ /AAinduced oxidation, scavenge free radicals, and act as reductants (Khanduja 2003; Ozsoy and others 2009). Spices and herbs, used in foods for their avor and in medicinal mixtures for their physiological effects, often contain high concentrations of phenolic compounds that have strong H-donating activity (Lugasi and others 1995; Muchuweti and others 2007).
Table 3 Content of redox-active compounds (antioxidants) of selected foods (mmol/100 g). Food Cloves, ground Oregano leaf, dried Ginger, ground Cinnamon, ground Turmeric powder Basil leaf, dried Curry powder Paprika Pepper, black Raspberries Wine, red Cherries, sour Redox-active compound content (mmol/100 g) 125.5 40.3 21.6 17.7 15.7 12.3 10.0 8.6 4.4 2.3 2.1 1.8

Sources: McCormick Institute Antioxidant Comparison (2009) and Halvorsen and others (2006).

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OH

O
COOH

OH

Figure 1Antioxidative phenolic acids (gallic, protochatechuic, p-coumaric acid, caffeic, and rosmarinic) found in plant extracts. All structures generated using ChemBioOfce (2008).

HO OH

OH

HO OH
OH

Gallic acid

Protocatechuic acid

p-Coumaric acid

OH OH

HO

OH

HO OH

HO OH

Caffeic acid

Rosmarinic acid

Many also have high ORAC values (Table 2 and 3). Some plantderived compounds (carnosol, rosmanol, rosmariquinone, and rosmaridiphenol) are better antioxidants than BHA (Richheimer and others 1996; Carvalho and others 2005). The major antioxidative plant phenolics can be divided into 4 general groups: phenolic acids (gallic, protochatechuic, caffeic, and rosmarinic acids; Figure 1), phenolic diterpenes (carnosol and carnosic acid; Figure 2), avonoids (quercetin and catechin; Figure 3), and volatile oils (eugenol, carvacrol, thymol, and menthol; Figure 4; Shan and others 2005). Phenolic acids generally act as antioxidants by trapping free radicals; avonoids can scavenge free radicals and chelate metals as well (Engeseth and Geldof 2001). The common characteristic of the avonoids (avones, avonols, avanols, and avanones) is the basic 15-carbon avan structure (C6 C3 C6 ; Figure 5). These carbon atoms are arranged in 3 rings (A, B, and C). Classes of avonoids differ in the level of saturation of the C ring. Individual compounds within a class dif-

fer in the substitution pattern of the A and B rings that inuence the phenoxyl radical stability and the antioxidant properties of the substances (Wojdyo and others 2007). The free radical-scavenging potential of natural polyphenolic compounds appears to depend on the pattern (both number and location) of free OH groups on the avonoid skeleton (Lupea and others 2008). The B-ring substitution pattern is especially important to free radical-scavenging ability of avonols. Studying the ability of 4 avonols substituted at different points on the B-ring (galangin, kaempferol, quercetin, and myricetin) to quench the intrinsic uorescence of bovine serum albumen, Xiao and others (2008) found that myricetin > quercetin > kaempferol > galangin. Authors interpret these ndings as indicating that hydrogen bond force plays an important role. Flavonoids with multiple hydroxyl groups are more effective antioxidants than those with only one. The presence of the ortho3,4-dihydroxy structure increases the antioxidative activity (Geldof and Engeseth 2002). Flavonoids can dampen transition metal

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CH3 H 3C CH3

CH 3

Figure 2Antioxidative phenolic diterpenes (carnosol, carnosic acid, rosmanol, and rosmarinic acid) found in plants.
OH

CH 3

Diterpene structure

H O O

OH HO COOH

OH OH

OH

Carnosol

Carnosic acid
OH OH

HO O
OH HO CH3 O CH CH 3

O OCH 2CH 3 H 3C CH3

HO OH

Rosmanol
r

Rosmarinic acid
tioning and in H-donating abilities were also hypothesized to have contributed to the structure-activity relationships. Alamed and others (2009) reported that the order of free radicalscavenging activity of a group of polar compounds was ferulic acid > coumaric acid > propyl gallate > gallic acid > AA; the free radical-scavenging activity of a group of nonpolar compounds was rosmarinic acid > BHT, tert-butylhydroquinone (TBHQ) > -tocopherol. Only propyl gallate, TBHQ, gallic acid, and rosmarinic acid inhibited lipid oxidation in an oil-in-water emulsion that may reect the ability of these compounds to orient at the interface of the oil droplet in the emulsion. Evaluating the antioxidative activity of hydroxycinnamic acids with similar structures (caffeic, chlorogenic, o-coumaric, and ferulic acids) in a sh muscle system, Medina and others (2007) found that the capacity of these compounds to donate electrons (bond dissociation energies) appeared to play the most signicant

enhancement of oxidation by donating a H to them, rendering them less proxidative. In addition, avones and some avanones (naringenin) can preferentially bind metals at the 5-hydroxyl and 4-oxo groups (Fernandez and others 2002). Brown and Kelly (2007) evaluated the antioxidative activity of structurally related (poly)phenols, anthocyan(id)ins, and phenolic acids at physiologically relevant concentrations (100 to 1000 nM) using a Cu2+ -mediated low-density lipoprotein oxidation model. (Poly)phenols with an ortho-dihydroxy substituted arrangement (cyanidin-3-glucoside, cyanidin, and protocatechuic acid) were the most effective, while trihydroxy-substituted compounds (gallic acid) had only intermediate efcacy. This was explained, in part, by their ability to chelate Cu2+ ions. It seems likely that the steric relationship of these OH groups and their arrangement on the ring(s) both play a role in the ability of the substance to chelate metal ions. However, differences in lipid/hydrophilic phase parti2011 Institute of Food Technologists

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OH
OH

OH
OH

HO

HO

OH OH
OH O

OH

Epicatechin
OH HO

Quercetin (flavanol)
OH OH

O HO

OH

HO

O OH

O HO O OH

HO

O OH O

HO OH

OH OH

Epicatechin gallate
OH HO

Epigallocatechin gallate

OH

O HO O O OH

HO OH O O

HO

OH OH

Rutin

Figure 3Antioxidative avonoids (epicatechin, quercetin, epicatechin gallate, epigallocatechin gallate, and rutin) found in plant extracts.

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OH 3C
HO

HO

Eugenol

Carvacrol

Safrole

H 3C O

OH

OH
O

H2 C

Thymol

Menthol
OH

Myristicin
H 3C CH 3
O

CH3 H3 C O

CH 3

CH3

1,8-Cineol

- Terpineol
O

p-Cymene

Cinnamaldehyde

Piperine
Figure 4Antioxidant volatile oils (eugenol, carvacrol, safrole, thymol, menthol, 1,8-cineole, -terpineol, p-cymene, cinnamaldehyde, myristicin, and piperine) found in plant extracts.

role in delaying rancidity, while the ability to chelate metals and the distribution between oily and aqueous phases were not correlated with inhibitory activities. The latter nding may reect the type of matrix, sh muscle, in which the oxidative activity was studied. Caffeic acid was the most effective of this antioxidant group (similar to propyl gallate).
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Potapovich and Kostyuk (2003) reported that, of a variety of avonoids (rutin, dihydroquercetin, quercetin, epigallocatechin gallate, and epicatechin gallate), the catechins were most effective in inhibiting microsomal lipid peroxidation. All r were able to chelate Fe2+ , Fe3+ , and Cu2+ and were effective O2 scavengers to varying degrees. Authors speculate that the

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B
8 7 6 5 9

A
4 3 2 1

Basic C6, C3, C6 structure

Chalcone

B
HO O

B
O
O

C
OH

OH

Flavone

Flavonol
HO

Flavanone

R1
O OH

3' 4'

R2
O O OH O O

+
R7 7 6 R6 5 R5 3 R4 O 5' R3
HO

HO HO OH OH OH

OH

Anthocyanin (R2= -OH, R4= -OH or H, R5 and R7= -OH or OCH3

Anthocyanidin-3,5-glucoside

Figure 5Flavonoid structure and avonoids (avanones: chalcone, avone, avanol, and avanones; and avans: anthocyanin and anthocyanidin-3,5-glycoside) found in plant extracts.

relative ability to scavenge O2 may be responsible for the relative antioxidative difference among these compounds. Many of the antioxidative avonoid compounds are naturally occurring pigments. It appears that chloroplast-located avonoids r perform a photo-protective role against O2 in plants (Agati and others 2007). Anthocyanins are the glycosides of polyhydroxy or polymethoxy derivatives of the avylium cation. Hydrolysis of the sugar moiety yields an aglycone, anthocyanindin (Figure 5). Anthocyanins and anthocyanindins exhibit visual color because of the extreme mobility of the electrons within the molecular structure (double bonds) in response to light in the visible spectrum (approximately 400 to 700 nm). The pigments are quite water-

soluble and 4 OH groups are bound to the aromatic rings. pH has a signicant effect on anthocyanin pigments. These OH r groups can give up H+ (in a basic solution) or H to an oxidizing r lipid (ROO ). Proanthocyanidins also contain multiple OH groups that can r donate hydrogen, quench O2 , and chelate metals (Shahidi and Wanasundara 1992; Fukumoto and Mazza 2000). Free radicalscavenging ability increases as the number of phenolic OH groups increases (Kondo and others 2001). Some phenols can polymerize into polyphenols that can bind minerals. Proanthocyanidins often occur as oligomers or polymers of monomeric avonoids, polyhydroxy avan-3-ols such as

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H 3C CH3 H CH2
H 2C H

H 3C CH3

CH3 HO

CH2
HO

H 2C

CH3
CH3

O CH 3

H3 C CH3

O CH 3

Alpha tocopherol

Gamma tocopherol
O

OH CH3
CH 2O C (CH2) 14 CH 3

CH OH

HCOH

H C C

O C C O

O O

OH

OH

OH

OH

Ascorbic acid
OH HO OH

Ascorbyl palmitate
OH

HO

OH

Propyl gallate

Resveratrol

Figure 6Natural antioxidants (alpha- and gamma-tocopherol, ascorbic acid, ascorbyl palmitate, propyl gallate, and resveratrol).

[+]-catechin and []-epicatechin (Dixon and others 2005; Figure 3 and 5). The polymeric procyanidins are better antioxidants than the corresponding monomers, catechin, and epicatechin (Ursini and others 2001). Catechin and epicatechin can combine to form esters, such as catechin/epicatechin gallate, or bond with sugars and proteins to yield glycosides and polyphenolic proteins. Glycosylation of avonoids at the 3 OH group usually decreases the antioxidative activity due to the reduction of the number of phenolic groups (quercetin/rutin; Figure 3). Proanthocyanidins with demonstrated antioxidant activity and potential biologically therapeutic effects occur in fruits (apples and
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cherries), some berries (rosehips, raspberries, blackberries, and strawberries), as well as in the leaves (tea), seeds (grape, sorghum, soy, and cocoa bean), and bark of many plants (Dixon and others 2005; Buricova and Reblova 2008; Bak and others 2010).

-Tocopherol -Tocopherol (vitamin E) is a fat-soluble carotenoid whose antioxidative capacity has been studied extensively (Figure 6). -Tocopherol is the major vitamin E compound in plant leaves where it is located in the chloroplast envelope and thylakoid membranes in proximity to phospholipids (Onibi and others 2000). It

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deactivates photosynthesis-derived reactive oxygen species (esr pecially O2 ) and prevents the propagation of lipid peroxidation by scavenging lipid peroxyl radicals in thylakoid membranes (Munn -Bosch 2005). e Trolox is a water-soluble derivative of vitamin E. Structurally related lipid-soluble antioxidants that differ in the number of methyl groups (-tocopherol compared with -tocopherol) have different free radical-scavenging activities and different surface activities (Figure 6; Chaiyasit and others 2005). Giuffrida and others (2007) evaluated the ability of -tocopherol, -tocopherol, ascorbyl palmitate, and propyl gallate (300 mg/kg; Figure 6) to prevent oxidation in sunower oil and high-oleic sunower oil, both rich in di-unsaturated fatty acids, and in partially hydrogenated palm oil containing monounsaturated fatty acids. -Tocopherol was the most effective antioxidant in sunower oil, and propyl gallate was the most effective in the more saturated oils. Yeum and others (2009) reported synergistic effects between AA and -tocopherol in protecting an in vitro biological model system. It may be that AA regenerates -tocopherol after -tocopherol r donates a H to an oxidizing lipid. -Tocopherol can also inhibit oxidation of protein. Est vez and e Heinonen (2010) demonstrated that -tocopherol reduced formation of -aminoadipic and -glutamic semialdehydes from oxidized myobrillar proteins. In general, vitamin E added to water-based food systems using an oil carrier targets the neutral lipid fraction (triacylglycerols) rather than the polar lipid fraction (phospholipids) and is not an effective antioxidant. However, -tocopherol added using a polar carrier can be incorporated into the phospholipid fraction and is an effective antioxidant (Wills and others 2007). In a lard model system, the antioxidative activity of the tocopherols is temperature dependent (Reblova 2006). At 80 C, the antioxidative activity of -tocopherol is about twice that of -tocopherol; however, it decreases as temperature increases. Antioxidative activity of -tocopherol decreases above 110 C, and both lose their activity above 150 C. Dietary supplementation of -tocopherol increases incorporation of the antioxidant into the phospholipid membrane region where the polyunsaturated fatty acids are located. Including -tocopherol in livestock diets has been shown to have signicant effects on the antioxidative activities of their tissues and the stability of meat derived from them (Formanek and others 2001; Swigert and others 2004; Guo and others 2006; Boler and others 2009; Lahucky and others 2010).

Herbs A number of spices and herbs contain compounds that can be removed and added to food systems to prevent oxidation (Lee and Shibamoto 2002; Ahn and others 2007; Rojas and Brewer 2007, 2008a; Sasse and others 2009). Antioxidant (and avor) components of herbs and spices may be removed/concentrated as extracts, essential oils, or resins. Extracts are soluble fractions that can be removed from plant materials by solubilizing the component(s) of interest in an aqueous, lipid, alcohol, solvent, or supercritical CO2 phase then removing it. Essential oils are the volatile oils and often contain isoprenoid compounds. Chemically, essential oils are extremely complex mixtures containing compounds of every major functional group class. Essential oils are isolated by steam distillation, extraction (solvent or CO2 ), or mechanical expression from the plant material. Plants also contain resins that are nonvolatile, high molecular weight, amorphous solids, or semisolids that ow when subjected to heat or stress. They are typically light yellow to dark brown in color, tasteless, odorless or faintly aromatic, and translucent or transparent. Most resins are bicyclic terpenes (alphaand beta-pinene, delta-3 carene, and sabinene), monocyclic terpenes (limonene and terpinolene), and tricyclic sesquiterpenes (longifolene, caryophyllene, and delta-cadinene). They are soluble in most organic solvents but not in water. Resins may contain small amounts of volatile phenolic compounds. Extracts of many members of the Labiatae (Lamiaceae) family (oregano, marjoram, savory, sage, rosemary, thyme, and basil), which are antioxidative, have a high total phenol content (Chen and others 2007). They do not necessarily have a high free radicalscavenging ability but appear to contain components that function by at least 2 different antioxidative mechanisms (Madsen and others 1996). Dorman and others (2003) observed that, while these antioxidant characteristics are not entirely related to the total phenolic contents, they do appear to be strongly dependent on rosmarinic acid, the major phenolic component present. Rosmarinic acid has vicinal OH groups on each of 2 aromatic rings, while carnosic acid, carnosol, and rosmanol each have vicinal OH groups on only 1 aromatic ring (Figure 3). A number of herbs (chamomile, rosehip, hawthorn, and lemon verbena) can enhance the activity of antioxidative enzymes such as superoxide dismutase and catalase in a dose-dependent manner and have been shown to enhance cell viability and provide protective effects against oxidative stress induced by hydrogen peroxide (in lung broblasts; Yoo and others 2008). Rosemary Chen and others (2007) reported that, of several herbs (Psidium guajava L., Camellia sinensis [Gamma Amino Butyric Acid tea], T. sinensis Roem., and Rosemarinus ofcinalis L.), the aqueous extract of rosemary contained the highest concentration of phenolic substances (185 mg/g; FolinCiocalteau) and total avonoids (141 mg/g). This aqueous extract inhibited UVB-induced (100 to 400 nm) oxidation of an erythrocyte ghost system (in vivo model system) at a relatively low concentration (100 g/mL; Chen and others 2007). At 100 mcg/mL, rosemary extract was able to scavenge 39% of the DPPH radicals (0.2 m); at 500 mcg/mL, it scavenged 55%. Rosemary extract (100 mcg/mL) inhibited liposome (egg lecithin with Fe3+/AA/H2 O2 ) oxidation by 98%. The most active antioxidative constituents of rosemary (R. ofcinalis) are phenolic diterpenes (carnosic, carnosol, rosmanol, rosmadial, 12-methoxycarnosic acid, epi-, and iso-rosmanol) and phenolic acids (rosmarinic and caffeic) (Table 4; Figure 1 and 2; Frankel 1991; Frankel and others 1996; Richheimer and others
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Ascorbic acid AA has 4 OH groups that can donate hydrogen to an oxidizing system (Figure 6). Because the OH groups (2 pairs of 2) are on adjacent carbon atoms, AA is able to chelate metal ions r (Fe++ ). It also scavenges free radicals, quenches O2 , and acts as a reducing agent. At high levels (>1000 mg/kg), AA shifts the balance between ferrous (Fe2+ ) and ferric iron (Fe3+ ), acts as an oxygen scavenger, and inhibits oxidation. However, at low levels (<100 mg/kg), it can catalyze oxidation (in muscle tissue; Ahn and others 2007; Yetella and Min 2008). Environmental conditions and the presence of other compounds in the system can alter the antioxidative capacity of AA. Allam and Mohamed (2002) reported that, using the induction period for the oxidation of sunower oil as a measure of antioxidant activity after heating (180 C), ascorbyl palmitate was less thermally stable than mixed tocopherols, propyl gallate, BHT, or BHA. This may be a function of the water solubility of AA.

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Lamiaceae family. Nakatani and Inatani (1981), Arouma and others (1992), Cuvelier and others (1994), Dorman and others (2000, 2003), Ahn and others (2002, 2007), Aoki and Wada (2003), Dorman and others (2003), Thorsen and Hildebrandt (2003), Lee and others (2005), Bozin and others (2006), Carrillo and Tena (2006), Yanishieva and others (2006), Hatzidimitrioua and others (2007), Bitar and others (2008), and Hernandez-Hernandez and others (2009).

Flavonoids

Phenolic acids Simple Rosmarphenolic Caffeic inic acid acids acids X X X X X X X X X X X

1996; Nakatani 2003; Thorsen and Hildebrandt 2003; Carvalho and others 2005). Carnosic acid has several times the antioxidative activity as BHT and BHA (Richheimer and others 1996). The synthetic phenolic antioxidants, BHA and BHT, each have a single aromatic ring with 1 OH group capable of donating r H . While carnosic acid also has ar single aromatic ring, it has 2 OH groups that can serve as H donors. In addition, vicinal OH groups can chelate prooxidative metals thereby preventing oxidation via 2 mechanisms. Hra and others (2000) reported that, in sunower oil, rosemary extract exhibited antioxidant activity superior to -tocopherol. The polyphenol, rosmarinic acid has 2 aromatic r rings, each with 2 OH groups that are capable of donating H and chelating metals. Adding -tocopherol to rosemary can have either an antagonistic effect (Hra and others 2000) or a synergistic effect (Aoki and Wada 2003). This may indicate that there are components in rosemary, other than rosmarinic acid, which make substantial contributions to the antioxidative capacity of the extract. It may also be a function of the solubility of the rosemary fractions used compared to that of -tocopherol with respect to the food system to which it being added. In lipid-based systems, carnosic acid and carnosol effectively chelate iron and scavenge peroxyl radical (Arouma and others 1992). However, free radical-scavenging activity ability does vary among the different compounds: 1,8-cineole = 62.5%, -pinene = 46.2%, and -pinene = 42.7% found in rosemary essential oil (Wang and others 2008). The ethanol extract of rosemary has higher antioxidative activity than do the individual phenolic compounds (carnosic acid, carnosol, 1,8-cineole, -pinene, camphor, camphene, and -pinene) separately (Wang and others 2008; Hernandez-Hernandez and others 2009). Solvents of medium polarity extract higher concentrations of carnosic acid from rosemary and sage than do solvents of higher or lower polarity (Trojakova and others 2001). In addition, different varieties of rosemary, grown in different regions under different conditions may vary in the content of these phenolic compounds.

pCymene X X

Phenylpropanoids

Carv acrol

Eugenol

X X X X X X X X X X X X X

Thymol X X

, pinene X X

Volatiles

Thujene

1,8Cineole X

X X X X X

X X

Table 4Selected antioxidant compounds identied in selected herbs.

Rosmanol X

Oregano Water/ethanol, dichloromethane, and ethanol extracts of oregano (Origanum vulgare L.) also contain high concentrations of phenols, primarily rosmarinic acid, as well as phenolic carboxylic acids and glycosides that are both antioxidative and effective superoxide anion radical scavengers (Kim and Cho 2001; Bendini and others 2002; Nakatani 2003; Hernandez-Hernandez and others 2009; Table 3 and 4). Oregano has a high total phenolic compound concentration (15.8 mg gallic acid equivalent [GAE]/g) and antioxidant activity. Using the reducing power assay, radical-scavenging assay, and the beta-carotene linoleic acid model system, Muchuweti and others (2007) determined that oregano had an antioxidant activity of 58.3% exceeded only by cinnamon (61.8%). Using hexanal as an indicator, Stashenko and others (2002) demonstrated that the essential oils of oregano and rosemary were both more effective at inhibiting Fe2+ -induced oxidation of linoleic acid in a sunower oil model system than vitamin E, Trolox, or BHA. This fraction contained unglycosylated and glycosylated avanones as well as dihydroavonols, all of which have antioxidative activity. Marjoram Of a number of herbs and spices (bay leaves, rosemary, sage, marjoram, oregano, cinnamon, parsley, sweet basil, and mint), marjoram (Origanum majorana L.) has the highest proportion of simple phenolic compounds (96%; Muchuweti and others 2007).
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Carnosol X

Carnosic acid X

X X X X

Phenolic diterpenes

Rosmadial Epi-, isoros manol X

Rosmaridiphenol X Rosemary Oregano Sage Thyme Marjoram Summer savory Bay Leaf Basil X X X

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Marjoram essential oil also contains a signicant amount of both rosmarinic acid and carnosol (Table 4; Figurer 1 and 2). The essential oil can scavenge hydroxyl radicals (OH ). It has antiradical activity exceeding that of the phenolic component thymol. In a linoleic acid model system, at 5 mg/mL, marjoram has a radicalscavenging activity of 92%, inhibits conjugated diene formation by 50%, and formation of secondary oxidation products by 80% (Schmidt and others 2008). Jun and others (2001) isolated a component (T3b) from marjoram, which is likely a phenolic substance, that is a better superoxide anion radical scavenger than -tocopherol, BHA, BHT, AA, epigallocatechin gallate, quercetin, or epicatechin (Figure 3). The inhibitory mechanism of T3b appears to depend on the action of superoxide dismutase, an endogenous enzyme that destroys superoxide anion by converting it to H2 O2 . These authors reported that the methanol extract of marjoram exhibited strong superoxide anion radical-scavenging ability (85.5%). Marjoram essential oil is also rich in terpinen-4-ol, cis-sabinene hydrate, p-cymene, and -terpinene (Vera and Chane-Ming 1999; Edris and others 2003; Nov k and others 2003). The bicyclic a monoterpenes, cis-sabinene hydrate and cis-sabinene hydrate acetate, appear to be responsible for the avor of marjoram (Richter and Schellenberg 2007). To the extent that these aromatic compounds can be separated from marjoram, this herb could be added to foods without adding unwanted avors. number of OH groups appears to coincide with the antioxidant potential of these compounds. Using an aldehyde/carboxylic acid assay, Lee and others (2005) demonstrated that carvacrol and thymol (5 ppm) can inhibit oxidation almost completely for 30 d. The primary aroma compounds in thyme include 1,8-cineole, thymol, carvacrol, and -terpineol (Table 4; Figure 4; Lee and others 2005). Given that thymol is the most effective antioxidative component and also one of the primary aroma compounds in thyme, using extracts of this herb would likely impart unwanted avors to foods to which they are added unless other antioxidative but nonaromatic components can be separated from the extract.

Sage The polar extracts of sage (Salvia ofcinalis) have strong radicalscavenging ability and superoxide anion radical-inhibiting ability (Orhan and others 2007). The antioxidative activity of sage oil compounds, due primarily to the presence of compounds with vicinal OH groups, is correlated with the oxygenated diterpene and sesquiterpene concentrations (Papageorgiou and others 2008). Sage contains some of the same antioxidant phenolic diterpene compounds found in rosemary such as carnosol, rosmanol, and rosmadial, in addition to some not found in rosemary (methyl carnosate, 9-ethylrosmanol ether, epirosmanol, isorosmanol, and galdosol) (Table 4; Figure 1 and 2; Cuvelier and others 1994; Miura and others 2002; Pizzale and others 2002; Nakatani 2003). In model systems, the polar extracts of the Salvia species exhibit excellent antioxidant activities compared to BHT (Tepe and others 2006). However, adding sage (0.05%) to raw pork is a less effective antioxidant than feeding -tocopherol (1000 mg/kg feed) to pigs prior to slaughter in terms of preventing oxidation in cooked pork patties (McCarthy and others 2001). This suggests that there is a component of the polar extract that either locates in the phospholipid membrane, chelates, or reduces free iron or affects Spices endogenous oxidative systems. Like herbs, spices can have signicant antioxidative effects (Suhaj 2006). Wojdyo and others (2007) measured total equivalent anThyme tioxidant capacities and phenolic contents (FolinCiocalteu) of Thymus vulgaris, T. mastichina, T. caespititius, and T. camphorate all 32 spices. Major phenolic acids identied in these spices inhave antioxidative activities comparable to those of -tocopherol cluded caffeic, p-coumaric, ferulic, and neochlorogenic. Predomand BHT (Miguel and others 2004). Thyme essential oil exhibits inant avonoids were quercetin, luteolin, apigenin, kaempferol, very strong free radical-scavenging ability and inhibits lipid oxi- and isorhamnetin. Spices can also have antibacterial effects. Shan and others (2005, dation induced by both Fe2+ /ascorbate and Fe2+ /H2 O2 (Bozin and others 2006). In terms of antioxidative activity, thyme oil > 2007) found that, of 46 spice extracts evaluated, many exhibited thymol > carvacrol > -terpinene > myrcene > linalool > p- antibacterial activity against foodborne pathogens. Gram-positive cymene > limonene > 1,8-cineole > -pinene (Youdim and bacteria were generally more sensitive than Gram-negative bacothers 2002). Carvacrol and thymol each have 1 aromatic ring and teria. Staphylococcus aureus was the most sensitive, while Echerichia 1 OH group, 1-terpineol has 1 OH group, while p-cymene coli was the most resistant. The antibacterial activity of the extracts has 1 aromatic group. The presence of aromatic groups and the was closely associated with their phenolic content.
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Basil In basil, a signicant correlation exists between the total phenolic content and antioxidant activity (Juliani and Simon 2002). Purple basil (Ocimum basilicum) extracts have a higher total phenolic acid content and greater antioxidant activity than do green basil extracts. The essential oil contains <18% eugenol (Figure 4) as a percentage of the total volatiles; however, it is correlated with antioxidant activity. However, the low contribution of the essential oil to the total antioxidant activity (0.05% to 5.9%) suggests that the antioxidant activity of these plants is not due to the presence of the essential oils as such, but to other phenolic compounds in green basil and to anthocyanins in purple basil (Juliani and Simon 2002). The aqueous extract of basil is a concentration-dependent superoxide and hydroxyl radical scavenger (Padurar and others 2008). The antioxidant activity of this extract has been attributed to its polar phenolic compounds. The total phenolic content of water and ethanol extracts of basil (GAE) was reported to be equivalent. Hinneburg and others (2006) reported that hydrodistilled extracts from basil and laurel had the highest antioxidant activities of several herbs (basil, laurel, parsley, juniper, aniseed, fennel, cumin, cardamom, and ginger) but not the greatest iron chelation ability. In a linoleic acid peroxidation assay, basil extract was as effective as Trolox. Basil also exhibited signicant iron-reducing capacity. Rosmarinic acid has been identied as the primary phenolic compound in basil leaves and stems (Lee and Scagel 2009). Linalool, epi--cadinol, and -bergamotene (7.4% to 9.2%) and -cadinene have been identied as the most common compounds in basil essential oil (Hussain and others 2008). Basil essential oil strongly inhibits lipid peroxidation whether induced by Fe2+ ascorbate or by Fe2+ /H2 O2 (Bozin and others 2006). Chicoric acid (caffeic acid derivatized with tartaric acid) has also been identied in substantial quantities (Lee and Scagel 2009). Additional antioxidant compounds found in basil are shown in Table 4.

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Nakatani and Inatani (1981), Arouma and others (1992), Ahn and others (2002, 2007), Dorman and others (2003), Shan and others (2005), Carrillo and Tena (2006), Jirovetz and others (2006), Jukic and others (2006), Schmidt and others (2006), Yanishieva and others (2006), Chaieb and others (2007), Hatzidimitrioua and others (2007), Hernandez-Hernandez and others (2009), and El-Ghorab and others (2010).

Phenolic acids Volatiles Phenylpropanoids p-Hy p-Hy , Van-illic Caffeic Gallic droxy droxy p- Coum , Caro Cur Argen Cam- Lina Gin Piper Cy- Carv CuminCinn-amacid acid acid benzoic acid benz aldehye aric acid Pinene phyllene cumin taene phene lool gerol ine Limonene mene acrol alde hyde alde hyde Cinn-amon X X X X X X X X X X X X X Clove X X X X X X X X X X Nut-meg X X X X X X X X X X Ginger X X X X X Turm-eric X X X X X X X Black pepper X X X X X X X X X

Clove The primary components of clove (Eugenia caryophyllus) essential oil are phenylpropanoids such as eugenol, carvacrol, thymol, and cinnamaldehyde (Figure 4; Chaieb and others 2007). Clove also contains a variety of nonvolatile compounds (tannins, sterols, avonoids, and triterpenes). Jirovetz and others (2006) identied 23 compounds in clove oil including eugenol (76.8%), caryophyllene (17.4%), -humulene (2.1%), and eugenyl acetate (1.2%). A variety of the antioxidative compounds are shown in Table 5. Clove essential oil is inhibitory toward hydroxyl radicals and can chelate iron. Comparing 16 spices, Khatun and others (2006) found that clove had the highest radical-scavenging activity followed by allspice and cinnamon. Eugenol has been reported to have an antioxidative activity equivalent to Trolox, carvacrol (oregano), and thymol (thyme; Dorman and others 2000). The essential oil scavenges free radicals at concentrations lower than those of eugenol, BHT, and BHA alone. Using peroxide values and formation of conjugated dienes, Marinova and others (2008) established that in sunower oil at 100 C, myricetin is a more effective and stronger antioxidant than -tocopherol. Mixtures of
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Flavonoids: kaempferol glycosides, rutin, apigenin, kaempferol, hesperetin, dihydroquercetin, quercetin, and catechins (catechin, epicatechin epigallocatechin gallate, and epicatechin gallate).

Cinnamon Cinnamon (Cinnamonum zeylanicum) contains a number of antioxidative components including vanillic, caffeic, gallic, protochatechuic, p-hydroxybenzoic, p-coumaricd, and ferulic acids and p-hydroxybenzaldehyde (Table 5, Figure 1, 2, 4, and 5; (Muchuweti and others 2007). Of a number of herbs and spices (bay leaves, rosemary, sage, marjoram, oregano, cinnamon, parsley, sweet basil, and mint) evaluated, cinnamon has been reported to have the highest polyphenolic compound concentration (13.7 mg GAE/g; Muchuweti and others 2007). Of 42 commonly used essential oils, cinnamon bark, oregano, and thyme have been reported to have the strongest free radical-scavenging abilities (Wen and others 2009). At 5 mg/mL, cinnamon a radical-scavenging activity of 92% (Muchuweti and others 2007). The major components responsible for this activity were identied as eugenol, carvacrol, and thymol. Jayaprakasha and others (2003) identied 27 compounds in the volatile oil of cinnamon stalks. The volatile oil was 44.7% hydrocarbons and 52.6% oxygenated compounds. Using a -carotene-linoleate model system, the volatile oil inhibited 55.9% and 66.9% of the oxidation at 100 and 200 ppm, respectively, compared to the control. The antioxidant capability of cinnamon essential oil is stronger than its free radical-scavenging capacity (Chen 2008). However, it is a better superoxide radical scavenger than propyl gallate, mint, anise, BHA, licorice, vanilla, ginger, nutmeg, or BHT (Murcia and others 2004). Cinnamon (bark and leaf) oleoresin can signicantly inhibit formation of primary and secondary oxidation products. Singh and others (2007) identied 13 components, which accounted for 100% of the total amount, in cinnamon bark volatile oil. The bark oleoresin contained 17 components that accounted for 92.3% of the total amount. The major component in cinnamon bark oleoresin was (E)-cinnamaldehyde (49.9%). Schmidt and others (2006) identied small amounts of -caryophyllene, benzyl benzoate, linalool, eugenyl acetate, and cinnamyl acetate in cinnamon leaf essential oil. The major component identied in cinnamon leaf oil was eugenol (87.2%). Cinnamon leaf oil has a signicant inhibitory effect on hydroxyl radicals and acts as an iron chelator efciently inhibiting formation of conjugated dienes and generation of secondary products from lipid peroxidation at a concentration equivalent to BHT.
Table 5Selected antioxidant compounds identied in selected spices.

Eug enol X X X

X X

Natural antioxidants . . .
the 2 exhibited a synergistic effect that was optimized in an equal molar ratio of the 2. The antioxidant activity of glycosidically bound volatile compounds in clove essential oil has been reported to be signicantly greater than that of the volatile aglycones (Politeo and others 2010). The glycosides can undergo enzymatic hydrolysis releasing their aglycones, therefore, could be considered as potential antioxidant precursors. Heating at 100 C for up to 6 h increases the peroxy radical-scavenging activity of clove (Khatun and others 2006). out Asia for centuries. Ground turmeric consists primarily of curcumin, dimethoxycurcumin and bis-dimethoxycurcumin, and 2,5-xylenol (Zhang and others 2009). Curcumin is an unsaturated diketone that exhibits keto-enol tautomerism (Anand and others 2008). It is a classical phenolic chain-breaking antioxidant, donatr ing H from the phenolic groups rather than from the CH2 group (Ross and others 2000). Jayaprakashaa and others (2006) reported that the antioxidant activity of the curcuminoids is curcumin > BHT, dimethoxycurcumin > bisdemithoxycurcumin. All of these polyphenolic molecules have limited water solubility. Curcumin is highly effective in neutralizing free radicals (Yu and others 2008). At the same concentration, curcumin has about twice the antioxidative activity of the polyphenol resveratrol (Aftab and Vieira 2009). Turmeric oil has a free radical-scavenging ability comparable to vitamin E and BHT (Yu and others 2008). The major components of turmeric oil responsible for this antioxidant activity are - and -turmerone, curlone, and -terpineol (Carolina and others 2003). Heating dry ginger and turmeric and their essential oils at 120 C results in different degrees of retention of antioxidant activity (Tiwari and others 2006). Antioxidant activity of turmeric oil is higher after heating while that of ginger oil is lower. This may be due to the difference in monoterpene content or to the release of bound antioxidants caused by the heat treatment. A variety of the antioxidant compounds found in ginger and nutmeg are shown in Table 5. Cumin is derived from Cuminum cyminum. The major components in cumin volatile oil are cuminal, -terpinene, and pinocarveol (El-Ghorab and others 2010). Cumin essential oil is better at reducing Fe3+ ions than dried or fresh ginger or cumin.

Nutmeg Jukic and others (2006) isolated glycosidically bound volatiles from nutmeg and identied free aglycones in the essential oil. The glycosidically bound and aglycone fractions had only 2 compounds in common, eugenol and terpinen-4-ol. The aglycone fraction had stronger antioxidant properties than did the free volatiles from the oil. Nutmeg (Myristica fragans and M. argentea) contains argenteane, a avanol diglycoside, which appears to be the primary antioxidative compound (Calliste and others 2010). Bis-erythro argenteane is a di-lignan that has been isolated from nutmeg mace (the lace-like seed membrane of nutmeg). The argenteane central moiety (3,3 -dimethoxy-1,1 -biphenyl-4,4 -diol) appears to owe r its free radical-scavenging ability to its ability to release 1 or 2 H (Chatterjee and others 2007; Calliste and others 2010). Nutmeg also contains signicant amounts of myristicin and safrole that are responsible for the characteristic aroma of nutmeg (Fisher 1992). Myristicin and safrole have similar structures: a 6-membered aromatic ring bound to an oxygenated 5-carbon ring on one side and a hydrocarbon side chain on the other (Figure 4). After heating (180 C, 10 min), nutmeg oil has a signicantly higher free radical-scavenging activity, compared to basil, cinnamon, clove, oregano, and thyme (Tomaino and others 2005). A variety of the Black pepper antioxidant compounds found in nutmeg are shown in Table 5. Black pepper (Piper nigrum) is a highly valued spice for its distinct biting quality that occurs at 1.35 ppm. It has a pungency 150 times Ginger, turmeric, and cumin that of capsaisan (United States Consumer Product Safety ComGinger is derived from the root of Zinger ofcinale. Fresh and mission 1992) due to the alkaloid piperine (Figure 4; Srinivasan dried ginger contain relatively large amounts of the volatile oils 2007). The avor quality is measured by the volatile oil and by the camphene, p-cineole, alpha-terpineol, zingiberene, and pentade- nonvolatile methylene chloride extract, piperine. Piperine stimcanoic acid (Figure 4; Tiwari and others 2006; El-Ghorab and ulates the digestive enzymes of the pancreas, enhances digestive others 2010). The maximum total phenolic contents were ex- capacity, and reduces gastrointestinal food transit time. Piperine tractable with methanol from fresh ginger (95.2 mg/g dry extract) can also quench free radicals and reactive oxygen species. It can followed by hexane extraction of fresh ginger (87.5 mg/g dry ex- protect against oxidative damage in vitro. Piperine acts as a hydroxyl tract). Hydrodistillation produced 23 mg GAE/g (Hinneman and radical scavenger at low concentrations (Mittal and Gupta 2000). others 2006). Ginger extract has been shown to have antioxidant Kapoor and others (2009) reported that black pepper (P. nigrum) activity almost equal to that of synthetic antioxidants (BHA and volatile oil contains 54 components that represent about 97% of BHT; Rehman and others 2003). the total weight. -Caryophylline (30%) is the major compoKikuzaki and Nakatani (2006) reported that 12 of the 5 nent along with limonene (13%), -pinene (7.9%), and sabinene gingerol-related compounds and 8 diarylheptanoids isolated (5.9%). Pepper essential oils also contain - and -pinene, from ginger rhizomes exhibit higher antioxidative activity than cyclohexene, 1-methyl-4-(1-methylethylidene)-2,3-cyclohexen-tocopherol. Authors suggest that this is likely dependent upon 1-ol, limonen-6-ol, (E)-3(10)-caren-4-ol, and t-caryophyllene side chain structures in addition to substitution patterns on the (Liang and others 2010). The major component of both ethanolbenzene ring. Hinneburg and others (2006) have suggested that, and ethyl acetate-extracted oleoresins is piperine (63.9% and for ginger, it may advisable to use extraction media that are able 39.0%, respectively, Liang and others 2010). Using peroxide, pto extract the lipophilic antioxidant compounds. anisidine, and thiobarbituric acid tests, the oil and oleoresins Turmeric is a spice derived from the rhizomes the Cur- have been shown to have stronger antioxidant activity than cuma longa plant, which is a member of the ginger family BHA and BHT (Kapoor and others 2009) but less than that of (Zingiberaceae). Rhizomes are horizontal underground stems propyl gallate. Gurdip and others (2004) reported that, while exthat send out shoots as well as roots. The bright yellow color tracts were predominantly piperine, piperolein B, piperamide, and of turmeric is primarily due to fat-soluble, polyphenolic pig- guineensine, the predominant compounds in essential oils were ments known as curcuminoids, primarily curcumin (diferuloyl caryophyllene, limonene, sabinene, -bisabolene, and -coapene. methane; Priyadarsini and others 2003; Anand and others 2008). Some of the antioxidant compounds found in black pepper are Turmeric has been used as a spice and medicinal herb through- shown in Table 5.
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S O N

OH

Figure 7Antioxidative sulfur-containing compounds (S-allylcysteine sulfoxide, diallyl sulde, allyl trisulde, and allyl-cysteine) in allium plant extracts.
S

S-allyl L-cysteine sulfoxide

Diallyl sulfide
O N OH

S S

Allyl trisulfide
Given that piperine is one of the most effective antioxidative components and also one of the primary aroma compounds in pepper, using extracts of this herb would likely impart unwanted avors to foods to which they are added unless other antioxidative but nonaromatic components can be separated from the extract.

Allyl-cysteine

The antioxidative effects of shallots are related primarily to their phenol content (Leelarungrayub and others 2006). According to Nuutila and others (2003), methanol extracts of onions have signicantly higher radical-scavenging activities than garlic and red onion has higher activity than yellow onion. Quercetin content is highest in red onions (Gorinstein and others 2008). The radicalscavenging activities are positively correlated with the total pheGarlic and related herbs Garlic (Allium sativum L.) has been widely used as a foodstuff nolics in these extracts. since antiquity. It has acquired a reputation as a therapeutic agent and herbal remedy in many cultures to prevent and treat heart and Tea extracts metabolic diseases, such as atherosclerosis, thrombosis, hypertenThe 3 primary types of tea, green, black, and oolong, are prosion, dementia, cancer, and diabetes (Tyler 1993). duced by different processing procedures. Of these types, green tea Garlic and shallots (Allium ascalonicum) have antioxidant and extracts have the highest total phenolics content, 94% of which free radical-scavenging characteristics and identiable odors at are avonoids (catechins; Duh and others 2004). Oolong tea conlow concentrations. They contain 2 main classes of antioxi- tains about 18% total phenolics and 4.4% avonoids. Theaavins dant compounds: avonoids (avones and quercetins; Figure 3) and thearubigins predominate in black tea. Black tea also conand sulfur-containing compounds (allyl-cysteine, diallyl sulde, tains chlorogenic, caffeic, p-coumaric, and quinic acids (Figure 1; and allyl trisulde; Figure 7). The sulfur-containing amino acid Kiehne and Engelhardt 1996). Some of the antioxidant comderivative, alliin (S-allyl-L-cystein sulfoxide), can be converted pounds found in tea are shown in Table 6. into allicin (diallyldisulde-S-oxide), the compound commonly Much of the antioxidative activity of green tea (C. sinensis) associated with garlic odor, by the enzyme alliinase. Thiosul- appears to be due to natural avonoids, tannins, and some vitamins nates, such as allicin, give garlic its characteristic odor; however, (Abdullin and others 2001). The antioxidant activity is linearly they are not necessarily responsible for all of the various antiox- related to the phenol content (Apak and others 2006) that has idative and health benets attributed to it (Amagase 2006). Okada been reported to be about 450 mg/g (Peschel and others 2007). and others (2005) have suggested that a combination of the allyl Catechins in green tea consist primarily of gallic acid derivatives group (CH2 CH=CH2 ) and the S(O)S group is necessary (Chen and others 2007). Catechin avanols appear to account for for the antioxidant action of thiosulnates in garlic extracts. S- more than 80% of the total antioxidant activity of green tea but allylcysteine, S-allyl mercaptocysteine, and nonsulfur compounds, less than 60% of that of black tea (Gardner and others 1998). The such as saponins, may contribute to the health benets (hy- radical-quenching ability of green tea has been shown to be more polipidemic, antiplatelet, procirculatory, immune enhancement, than 20% more effective than that of black tea in both aqueous anticancer, and chemopreventive activities) associated with garlic. and lipophilic systems. In tea extracts, the strongest antioxidant and H2 O2 -scavenging Gorinstein and others (2008) reported that trans-hydroxycinnamic acid (caffeic, p-coumaric, ferulic, and sinapic acids) concentrations activity is due to phenols, with 3 OH groups bonded to the in garlic were twice that in onions. Some of the antioxidant com- aromatic ring, adjacent to each other (Sroka and Cisowski 2003). pounds found in garlic are shown in Table 6, and sulfur-containing Epigallocatechin, which has 3 adjacent OH substitutions on compounds are shown in Figure 7. the B ring, has the highest antioxidant activity (Figure 3). In
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Rutin
Nakatani and Inatani (1981), Arouma and others (1992), Cuvelier and others (1994), Kiehne and Engelhardt (1996), Dorman and others (2000, 2003), Ahn and others (2002, 2007), Okada and others (2005), Carrillo and Tena (2006), Yanishieva and others (2006), Chen and others (2007), Hatzidimitrioua and others (2007), Gorinstein and others (2008), Iacopini and others (2008), Hernandez-Hernandez and others (2009), and Calliste and others (2010).

Table 6Selected antioxidant compounds identied in garlic, tea, and grapeseed extract.

Epi catechin

addition to a avonoid ring, a 3 ,4 ,5 -trihydroxy (galloyl) group are required for Fe++ binding in catechins (Khokhar and OwusuApenten 2003). These polyphenolic avonoids are particularly effective free radical scavengers (Figure 3; Lien and others 2008). The primary catechin polyphenol [()-epigallocatechin-3-gallate] is also the primary peroxyl-radical-scavenging compound in tea extracts (Caldwell 2001; Cabrera and others 2003). In terms of free radical-scavenging ability, epicatechin gallate > epigallocatechin > epicatechin (Guo and others 1996). The rst 2 compounds have 3 ,4 ,5 -trihydroxy (galloyl) groups while the last does not. Both their iron-chelating and free radical-scavenging activities appear to be responsible for the ability of these compounds to protect membranes from Fe2+ /Fe3+ -initiated lipid oxidation. In an ironmediated reaction, Grey and Adlercreutz (2006) demonstrated that catechin inhibited oxidation better than AA. They concluded that catechins chelating ability, rather than its radical-scavenging mechanism alone, is responsible for the observed antioxidative activity. In more complex food systems, tea catechins can have varying effects. Mitsumoto and others (2005) found that adding tea catechins to raw beef (200 or 400 mg/kg) inhibited (P < 0.05) lipid oxidation to a greater extent than vitamin C (200 or 400 mg/kg); however, they increased discoloration in cooked beef and chicken meat. Chen and others (1998) reported that green tea catechin extract, consisting primarily of 4 epicatechin isomers, was much more antioxidative than rosemary extract when added to canola oil, pork lard, and chicken fat. In maize (corn) oil triglycerides, Huang and Frankel (1997) found that epigallocatechin (140 M), epigallocatechin gallate, and epicatechin gallate were better antioxidants than either epicatechin or catechin. Both gallic acid and propyl gallate were more effective than epicatechin and catechin. However, in a maize oil-in-water emulsion, all tea catechins, gallic acid, and propyl gallate were prooxidative (5 and 20 M) accelerating hydroperoxide and hexanal formation. The improved antioxidant activity of tea catechins in liposomes, compared with emulsions, may be due to the greater afnity of the polar catechins toward the polar surface of the lecithin bilayers, thus affording better protection (Hatzidimitrioua and others 2007). In a model system mixture of the avanols, in the same concentrations as they occur in the tea extracts, the antioxidant potential has been shown to be a simple summation of the activity of the individual components with no apparent synergism or antagonism occurring (Gardner and others 1998). Alkyl compounds with double bond(s), such as 3,7-dimethyl1,6-octadien-3-ol in green tea extracts and heterocyclic compounds (furfural) in roasted green tea extracts, are major volatile constituents that also exhibit some antioxidative activity (Yanagimoto and others 2003).

Others Myre cetin

Res veratrol

Epi gallo catechin gallate

Sulfur-containing compounds Allyl Diallyl Tri cysteine sulde sulde X X X Flavonoids Epi catechin gallate X X X X X

Hydrocinnamic acids pCaffeic Coumaric Ferulic X X X X X X X

Grape seed extract Because red wines are produced from red grapes, the antioxidant capacity and chemical composition are related to the grapes. The antioxidant activity of red wines is associated with the content of polyphenols such as avonoids, phenolic acids, stilbenes, coummarines, and lignoids (Radovanovic and others 2009). The phenolic composition varies greatly due to grape variety, environmental and climate conditions, soil type, degree of ripeness, and winemaking process (Table 6; Jayaprakasha and others 2001; Hatzidimitrioua and others 2007; Lachman and others 2007; Iacopini and others 2008; Rababah and others 2008; Xu and others 2010;). Touns and others (2009) reported wide variations in the contents of total phenols (122 to 441 mg GAE/g), avonoids
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Quer cetin X X X

Cate quin X X X

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17 to 48 mc epicatechin [EC]/g), and tannins (15 to 37 mc EC/g) in the methanolic extracts from seeds of 3 varieties of grapes. Phenolic compounds in grape seeds and skins include catechins, epicatechins, epicatechin-3-O-gallate, phenolic acids, caffeic acid, quercetin, myricetin, proanthocyanidins, and resveratrol (Figure 1, 3, and 4; Jayaprakasha and others 2001; Hatzidimitrioua and others 2007). Many have strong antiradical activity. Most of the phenolic compounds found in red wines are derived from the condensation of avan-2-ol into oligomers (proanthocyanidins) and polymers (condensed tannins). Resveratrol, quercetin, and rutin are generally found in grape skin extracts, while catechin and epicatechin are found in the seeds (Figure 3 and 6). The phenolic content of grape seeds defatted with hexane then extracted with methanol and dried under vacuum has been reported to be about 5 mg/100 g, while the anthocyanin content is between 0.14 and 0.68 g/100 g (Rababah and others 2008). Iacopini and others (2008) assessed the antioxidant activity of the extracts and pure compounds using 2 different in vitro tests: scavenging of the stable DPPH radical and of authentic peroxynitrite (ONOO). Antioxidant activities of grape seed extract ranged from 66.4% to 81.4%, compared to vitamin E that ranges from 90.3% to 94.7%. Monophenols, quercetin, rutin, and resveratrol may act either synergistically or antagonistically depending on their concentrations and the reaction temperature. Grape seed extract has been shown to inhibit both lipid hydroperoxide and propanal formation in an emulsion system (Hu and Skibsted 2002). Oligomeric procyanidins may be better antioxidants than their monomeric counterparts due to their ability to concentrate where the oxidative reaction is likely to occur. Resveratrol (trans-3,4 ,5-trihydroxystilbene), produced primarily in the grapevine, is present in various parts of the grape, including the skin. It has strong antioxidant activity exceeding that of propyl gallate, vanillin, phenol, BHT, and -tocopherol (Murcia and Martinez-Tome 2001). This may be because it has more phenolic rings (2 compared with 1) than propyl gallate, phenol, and BHT, and because it has more OH groups than -tocopherol (3 compared with 1). Resveratrol inhibits peroxidation in a concentration-dependent manner. However, it does not scavenge hydroxyl radicals or does it react with H2 O2 , making it an inefcient catalyst of subsequent oxidation (Murcia and MartinezTome 2001). Some of the antioxidant compounds found in grape seed extract are shown in Table 6. Soares and others (2003) demonstrated that resveratrol, vitamins C and E, BHT, and propyl gallate were all able to signicantly inhibit the oxidation of -carotene by hydroxyl free radicals. Polyphenolic fractions from grape pomace can repair -tocopherol by reducing the -tocopheroxyl radical (Pazos and others 2009). Most of the phenolic compounds in fresh wine are derived from condensation of avan-3-ol into oligomers (proanthocyanidins) and polymers (tannins; Granato and others 2011). Granato and others (2011) reported that the primary phenolics exerting antioxidant effects (DPPH and ORAC assays) in Brazilian red wines were nonanthocyanin avonoids. Anthocyanins present in these wines were present solely in their monomeric form and ranged from about 9 to 237 mg/mL. Flavonoid content varied from 520 to 1795 mg catechin equivalents [CTE]/L. However, after evaluating 80 Spanish red wines, Rivero Perez and others (2008) found that the free anthocyanin fraction is the primary fraction responsible for antioxidant capacity and is correlated with electron transfer processes. Pazos and others (2006) evaluated the effectiveness of a grape phenol fraction, isolated grape procyanidins, hydroxytyrosol (from
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olive oil), and propyl gallate in inhibiting lipid oxidation in a sh (hake) microsomal model system. Oxidation was initiated by hemoglobin, enzymatic NADH iron and nonenzymatic ascorbate iron. The relative antioxidant efciency was independent of the prooxidant system and was isolated grape procyanidin > propyl gallate > grape phenolic extract > hydroxytyrosol. Antioxidative effectiveness was positively correlated with incorporation of the substance into microsomes. However, polarity appeared to play less of a role in inhibition of hemoglobin oxidation by phenolics underscoring the fact that an exogenous antioxidant must be incorporated into membranes where unsaturated fatty acids and iron-reducing enzymes are located in order to be effective. Poiana and others (2008) demonstrated that during the ageing of red wine, polymeric anthocyanins increased from about 9% to over 75% after 6 mo, while monomeric anthocyanins decreased from over 75% to less than 24%. Total antioxidant capacity decreased and was highly correlated with the monomeric anthocyanin fraction (r > 0.98); however, free radical-scavenging ability increased and was highly correlated with the polymeric anthocyanin fraction. Granato and others (2010) also evaluated the antioxidant activity and the phenolic content of red wines and veried that ORAC values correlated well to avonoid content (r = 0.47; P = 0.01), total phenolics (r = 0.44), and DPPH (r = 0.67). DPPH values also correlated well to the content of avonoids (r = 0.69), total phenolic compounds (r = 0.60), and nonavonoid compounds (r = 0.46) (in beers; Granato and others 2011).

The Stereochemistry of Flavanones


Enantiomers are molecules that are mirror images of each another but cannot be superimposed onto one another. Molecules exhibit stereoisomerism (enantiomers) because they have one or more chiral centers. A chiral center results from the presence of an assymetrical carbon atom, that is, one that is attached to 4 different atoms or 4 different groups of atoms (making its mirror image nonsuperimposable). Enantiomers rotate the plane of polarized light in opposite directions. Enantiomer names use the R/S system. This system involves no reference but labels each chiral center R or S using a system in which its substituents are each assigned a priority, according to the Cahn-Ingold-Prelog priority rules (Cahn and others 1966), based on atomic number. If the center is oriented so that the lowest priority of the 4 substituents is pointed away from a viewer, the viewer will then see 2 possibilities: if the priority of the remaining 3 substituents decreases in a clockwise direction, it is labeled R (rectus), and if it decreases in a counterclockwise direction, it is S (sinister). Flavanones can have chiral carbon atoms; therefore, they can exist as S- and R-enantiomers. These enantiomers can be produced in different quantities in different plant materials under different growing conditions (Yanez and others 2005, 2008, 2007). They can have different effects in both biological and inorganic systems. For these reasons, separating and quantifying them has been of interest to the medical, biological, and agricultural industries in the recent past. The avanone glycosides naringin and neohesperidin found in some citrus species have a chiral center in the C-2 position of the avanone moiety (Uchiyama and others 2008; Figure 8). The avanone hesperetin, the aglycone of hesperidin and major avonoid in oranges, contains a chiral C-atom, so it can also exist as an S- and R-enantiomer. The 2S-herperidin and its Shesperitin aglycone predominate in nature (Uchiyama and others 2008).

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OH

OH HO

HO

OH

HO O O OH O O OH

OH

O O
O OH OH

OH

Hesperitin

Naringen
OH OH

O HO OH

HO

O O O O O

OH

HO OH OH

OH

Neohesperidin
O HO OH O O O O O

OH OH

OH OH

HO OH OH

OH

Hesperidin
Figure 8Natural antioxidants that exist as stereoisomers (hesperitin, naringin, neohesperidin, and hesperidin).

Enantiomers can react with other compounds or other enantiomers in different ways or at different rates. Brand and others (2010) have demonstrated small, but signicant, differences in the metabolism and transport characteristics, and bioactivity between S- and R-hesperetin. Naringin, the major avanone7-O-glycoside of sour orange, is responsible for the bitter taste of the fruit (Caccamese and others (2010). The relative ratios of naringin and neohesperidin to their C-2 epimers varies depend-

ing on species, maturity, and processing. Separation of naringin from neohesperidin is complicated by the presence of stereoisomers (Belboukhari and others 2010). Takemoto and others (2008) developed a high-performance liquid chromatography (HPLC) method using UV detection for the stereospecic analysis of the avan, sakuranetin, found in grapefruit and oranges. Stereospecic HPLC methods have been developed for separation of epimers in tea, grapes, orange juice, and C-2 epimers from other sources

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and others 2001). Three primary extraction techniques are used for polyphenols: solvents, solid-phase extraction, and supercritical extraction. Using a Soxhlet apparatus combines percolation and immersion that increases extraction efciency. Several extractions can be accomplished with solvents having different polarities (petrol ether, toluene, acetone, ethanol, methanol, ethyl acetate, and water). Methanol/water/HCl (70:29:1, v/v/v) has been shown to be the best among several solvents evaluated for extracting phenolics from grape seed (Xu and others 2010). Grinding in a mortar in liquid nitrogen provides uniform particle size allowing for a more consistent extraction. Ultrasound can be used to assist liquid solvent extraction. Xu and others (2010) reported that sequential sonication was a preferred to mechanical agitation as an extraction method for assessing phenolic content in grapeseed. Supercritical CO2 extraction can also be used (Schwarz and others 2001). Hydrodistillation of plant materials has several advantages. The essential oils that carry the intrinsic avor of a spice can be removed and polyphenols, primary antioxidant compounds, are concentrated. In addition, the hydrodistilled compounds are generally more soluble in aqueous media than are those extracted using organic solvents. They are often more soluble than synthetic antioxidants as well. Hydrodistillation also avoids potential residues from organic solvents. Hydrodistilled extracts have also been reported to have a variety of functional effects in foods and in human health (Hinneburg and others 2006). Optimizing the extraction process could lead to even better results. The distillation process can also concentrate antioxidant components. Naz and others (2011) found that deodorizer distillates from sunower oil processing were richer in tocopherols than the Effects of Processing Endogenous antioxidant systems (enzymatic) can be damaged deodorized oil itself. The implication is that, while the distillation during food processing (particle size reduction and heating), by process removes unwanted materials from the oil, it may, in fact, certain ingredients (salts and organic acids), and by storage con- concentrate some of the antioxidants. ditions (presence of oxygen) such that they are ineffective (Chen and others 1998). NaCl, in particular, reduces the activity of the Heat treatment When we think of processing, heat treatment is often the rst antioxidant enzymes catalase, glutathione peroxidase, and superoxide dismutase that reduces their capacity to perform antioxidative process that comes to mind. Antioxidative activity of a given compound may increase, defunctions (Lee and others 1997). Ingredients, such as AA and citric crease, or remain unchanged as a function of temperature. Stability acid, can work synergistically with avonoid antioxidants. Spices and herbs can be added to foods in various forms: whole, of an antioxidant to heat is advantageous in the food industry, since ground, or as isolates from their extracts. Extracting antioxidant many fat- and oil-containing foods are heated during processing components from a complex matrix depends on the solubility of and since heat is often the initiator of lipid oxidation. At 80 C, the extractant, the solvent, and the presence of other substances the antioxidative activity of -tocopherol is about twice that of that may compete with the extraction process, and the extraction tocopherol; however, it decreases as temperature increases from 80 process itself (vacuum, distillation, pressure, and so on). Because to 150 C. Antioxidative activity of -tocopherol remains fairly these substances are aromatic, pungent food ingredients, they may constant between 80 and 110 C, decreasing only at tempera or may not be desirable in a nonavoring (antioxidant or other) tures above 110 C. Neither retains their antioxidative activity at application (Ruberto and others 2000; Teissedre and Waterhouse 150 C. Ginger extract has good thermal stability and inhibits more 2000). For example, even at low concentrations, some components of rosemary essential oil (verbenone, borneol, and camphor) can than 85% of linoleic acid peroxidation when heated at 185 C for impart a rosemary odor to foods (Carrillo and Tena 2006). Solid 120 min (Rehman and others 2003). Heating (120 C) dry ginger rosemary extract can contain >356 g/g verbenone, 190 g/g and turmeric essential oils results in different degrees of antioxidant activity retention. The antioxidant activity of turmeric oil is higher borneol, and >135 g/g camphor (Carrillo and Tena 2006). after heating (120 C), unlike ginger oil that loses antioxidant activity (Tiwari and others 2006). Turmeric oil contains a higher Extraction Because many antioxidants are unstable to oxygen and endoge- concentration of monoterpenes than does ginger oil; however, nous enzymes, most are extracted from freeze-dried plant materi- release of bound antioxidants by the heat treatment should not be als. Selecting an appropriate extraction procedure can increase the ruled out. concentration of the antioxidant compound. Extraction using edible oil or fat is relatively simple. Herbs and spices can be mixed with Adding antioxidants to livestock diets fats, oils, or medium-chain triglycerides, allowed to extract under Including herb distillates into livestock diets can have positive dened time/temperature control, then ltered for use (Pokorny effects. Moclino and others (2008) found that feeding a steam (Uchiyama and others 2008; Caccamese and others 2010; VegaVillas and others 2008; Kim and others 2009; Belboukhari and others 2010). Si-Ahmed and others (2010) reported that different mobile phases in different ratios are required to accomplish enantiomeric and diastereomeric separation of a variety of avanones (avanone, 2 -hydroxyavanone, 4 -hydroxyavanone, 6-hydroxyavanone, 7-hydroxyavanone, 4 -methoxyavanone, 6-methoxyavanone, 7-methoxyavanone, hesperetin, hesperidin, naringenin, and naringin). Others have reported similar differences in chiral discrimination ability (toward avanones) depending on the buffer and alcohol modier enantioselectivity (Cirilli and others 2008). Abbate and others (2009) described a method for assessing congurational and conformational properties (of naringenin) using vibrational circular dichroism. The stereoselectivity of chiral avanones and epimers has signicant biological effects in terms of their pharmacological activity and disposition in humans and livestock. Gardana and others (2009) reported that some human intestinal bacteria can transform diadzein to equol, O-desmethylangolensin, or dihydrodaidzein. Diet has a clear effect. A diet lower in ber, vegetables, and cereals and higher in lipids from animal sources increases production of equol. These stereoselective differences in the chiral forms of avonone antioxidants may result in differences in antioxidative effects of the various epimers depending on the matrix and oxidizing group. For these reasons, a concerted effort is being made to separate these chiral compounds and to evaluate their specic characteristics under dened conditions.
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distilled rosemary by-product to ewes increased rosmarinic acid, carnosol, and carnosic acid content in the meat. Fresh meat from these animals had higher total ferric reducing antioxidant power and lower DPPH values than controls indicating that the rosemary distillate partitioned into the meat tissues and reduced susceptibility to oxidation. McCarthy and others (2001) have shown similar results with pigs. Boler and others (2009) found that feeding vitamin E to pigs increased pork stability during storage. Simitzis and others (2008) found that meat from lambs fed a feed that had been sprayed with oregano essential oil (1 mL/kg) was much more stable to lipid oxidation during both refrigerated and frozen storage than that from controls. Gobert and others (2010) found that adding antioxidants to diets of cattle fed a polyunsaturated fatty acid (PUFA)-rich diet improved lipid stability in steaks; the combination of vitamin E and plant extracts rich in polyphenols was more efcient than vitamin E alone indicating some synergism between the 2. cluded that the nature and conformation of the proteins as well as the chemical structure of the phenols inuenced the overall effect. Antioxidant content of raw materials can change over time and are likely related to storage conditions. Hatzidimitrioua and others (2007) reported that total phenol content of grape seeds decreases during storage. Changes were minor for samples stored at less than 55% relative humidity; however, high humidity (75%) accelerated degradation resulting in a 50% reduction of total phenol content. Based on the continuous gallic acid release, authors suggested that this degradation was related to hydrolytic reactions. Modications of the storage process would be expected to enhance retention of antioxidative compounds in grape seeds. Ingredients, such as salt, can act as prooxidants in food systems; however, antioxidants can help reduce it. Brannan (2008) found that grape seed extract helps to mitigate the prooxidative effects of NaCl in stored ground chicken without affecting moisture content or pH. The author suggests that grapeseed extract may alter the effect of NaCl on protein solubility in salted chicken patties. Whether it affects physicochemical interactions in cooked meat quality remains to be assessed. Akarpat and others (2008) demonstrated that adding a hot water extract of rosemary (10%) to ground beef containing salt (1.5%) protected color and preserved oxidative quality during frozen storage (120 d). Fasseas and others (2008) found that essential oils from oregano and sage added to ground beef and pork (3% w/w) reduced oxidation. The effect was even more dramatic in cooked meat than in raw meat. The antioxidant components of rosemary, sage, basil, black pepper, garlic, and onion appear to be relatively stable. Microwave treatment of these herbs has no effect on reducing power or ironchelating capacity (Bertelli and others 2004). However, the effects on other components, such as avor components and pigments, are unknown. Marinating and cooking (chicken) signicantly reduces the antioxidant activities of marinating sauces and consequently reduces the amounts of antioxidant available (Thomas and others 2010). Marinating chicken (in herb and spice-based marinades) prior to cooking reduced the total antioxidant activity (45% to 70%) originally present in the sauce. This may be due to the ionic effects of various salts typically included in marinades, the effects of reduced pH on the phenolic components of the marinades, and/or to the interactions between antioxidants or between antioxidants and protein. Loss of antioxidant activity due to cooking may reect the protective action of antioxidants on proteins (which are denatured by heating) or their protective action toward other components (vitamins). In addition to reducing lipid oxidation, antioxidants may have other benets in food systems. Adding rosemary essential oil and/or citrus ber washing water to bologna has been shown to lower the levels of residual nitrite (Viuda-Martos and others 2010). Flavonoids, hesperidin, and narirutin were identied in the bologna with hesperidin concentrations being higher than narirutin concentrations. The preferred (sensory) sample was that which contained 50 g/kg citrus ber water and 200 mg/kg rosemary essential oil. There are many types of food matrices to which these antioxidant compounds might be added and many types of processing that the product might then undergo. There are currently no general guidelines as to what/when to use plant extracts in food matrices. More studies are necessary to elucidate that substances are effective in what systems and under what condition.
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Effects of the food matrix and ingredients Natural plant antioxidants can protect food components from oxidation under the stress of heating and storage. However, the inherent characteristics (ionic strength and pH) of the food, the food matrix (emulsion, foam, aqueous, and protein), and ingredients can inuence antioxidant effectiveness. Vitamin E added to water-based food systems in an oil carrier concentrates in the neutral lipid fraction rather than the polar lipid fraction and is not an effective antioxidant. However, -tocopherol added using a polar carrier can be incorporated into the phospholipid fraction and is an effective antioxidant (Wills and others 2007). In a lard model system, the antioxidative activity of the tocopherols is temperature dependent (Reblova 2006). Wanatabe and others (2010) demonstrated that, in a methyl lineoleate/water emulsion, the effectiveness of AA and acyl ascorbates depended on whether the oxidation process was initiated by an oil-soluble prooxidant or a water-soluble prooxidant. The AA concentrated in the aqueous phase and suppressed oxidation to a greater degree at the oil/water interface when the prooxidant was water soluble. Docecanoyl and hexadecanoyl ascorbates dissolved in the oil phase and suppressed oxidation the oil phase (droplets) rather than at the interface. Increasing the pH appeared to enhance the electron-donating ability of AA in the water phase ultimately affecting oxidation. Hexadecanoyl ascorbate in the oil phase was not susceptible to these pH effects. Authors suggest that another explanation may be destabilization of the emulsion through occulation and coalescence of the oil droplets at low pH. Thymol can prevent loss of -tocopherol (in oil) following heating at 180 C for 10 min (Tomaino and others 2005). Using a lipophilic model system, Lee and Shibamoto (2002) demonstrated that volatile extracts of thyme (and basil) inhibited the oxidation of hexanal for 40 d. These extracts also inhibited methyl linoleate deterioration at 40 C. In sunower oil, aroma detection thresholds of carvacrol, thymol, and p-cymene 2,3-diol have been reported to be 30, 124, and 794 ppm, respectively (Bitar and others 2008). pCymene 2,3-diol at 335 ppm imparted no negative avor changes and reduced oxidation by more than 46%. Estevez and others (2008) evaluated several phenols (gallic acid, cyanidin-3-glucoside, (+)-epicatechin, chlorogenic acid, genistein, and rutin) and -tocopherol in terms of anti- or prooxidative effects of oil-in-water emulsions containing myobrillar proteins (1%). Gallic acid, cyanidin-3-glucoside, and genistein were the most efcient inhibitors of lipid and protein oxidation. They con-

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Synergism
Combining antioxidants may increase their effectiveness. Smet and others (2008) found that dietary synthetic antioxidants combined with -tocopherol were more effective than rosemary, green tea, grape seed, or tomato extracts (100 to 200 ppm) alone or in combination in sparing tocopherols oxidation and in preventing oxidation of fresh frozen chicken patties. It has been proposed that the mixed free radical acceptors involve 2 antioxidants: one that reacts with the peroxy radical (and is consumed) and a 2nd that regenerates the 1st, effectively sparing. Phenolic antioxidants and AA appear to work synergistically in this way (Uri 1961). (1) ROO + A:H = ROO:H + A r r (2) A + B:H = A:H + B .
r r

Regulatory Status of Extracts, Concentrates, and Resins


Synthetic antioxidants (BHA, BHT, and EDTA) are regulated by the Food and Drug Administration (FDA) as direct food additives. They may be used alone or in combination not to exceed 0.02% (2 ppm) of the nal product in specied food products (21CFR172.110). These antioxidants are considered to be safe and suitable ingredients for use in meat, poultry, and egg products, alone or in combination, not to exceed 0.02% of the fat content (FSIS Directive 7120.1. revision 5). Some herb and spice extracts and oleoresins are Generally Recognized As Safe (GRAS). Some are considered to be indirect additives (21 CFR Vol. 3. Part 101); as such, solvents permitted for the extraction process and solvent residues allowed are specied. Some extracts, concentrates, and resins are regulated by the FDA Dietary Supplement Health and Education Act of 1994 and are considered to be one (or more) of several dened dietary ingredients (a vitamin, a mineral, an herb or other botanical, amino acid, a dietary substance for use by man to supplement the diet by increasing the total dietary intake, or a concentrate, metabolite, constituent, extract, or combination of any ingredient described in clause (A), (B), (C), (D), or (E) and is excluded from regulation as a food additive. Extracts, concentrates, and resins are also regulated under the Food Labeling Regulation, Amendments; Food Regulation Uniform Compliance Date; and New Dietary Ingredient Premarket Notication Final Rule (1997). If they are added to cause avor or color changes, they are regulated as such and specic quantities allowable for use in various foods are set forth. Based on the number of various classications under which an extract, concentrate or resin could be covered, allowable use levels vary widely.

Some acidic compounds, such as AA and citric acid, can exert a synergistic effect when added along with polyphenolic antioxidants. These acidic compounds chelate metals. These synergists form an antioxidant radical synergist complex (A:S) such that neir r ther the antioxidant radical (A ) nor the synergist radical (S ) can catalyze oxidation reactions. This chemical association suppresses the antioxidant radicals ability to assist in the breakdown of lipid peroxides (Aurand and Woods 1979). Addition of anthocyanin can prevent oxidation of AA by metal ions such as copper (Sarma and others 1997). Anthocyanin not only chelates metal ions, but also forms an AA (copigment-metalanthocyanin) complex that may be the basis for its antioxidative activity. Because of the number of OH groups on the aromatic rings, and because of their water solubility, anthocyanins are pH-sensitive. In a basic solution, the OH groups can give up r H+; in a more neutral environment, they can donater H to an r oxidizing lipid (ROO ). For this reason, the antioxidative capacity of an anthocyanin is dependent on the anthocyanin itself (number and location of OH groups), the pH of the surrounding environment, and the other components of the system (metals, continuous phase). Lee and others (2005) found that combinations of chelators (sodium tripolyphosphate or sodium citrate) with reductants (erythorbate), and/or free radical scavengers (BHA and rosemary extract) were effective antioxidants. The combination of rosemary and erythorbate was most effective in delaying lipid oxidation in ground beef. The rosemary/citrate/erythorbate combination was most effective in stabilizing color and delaying lipid oxidation. These ndings indicate that combining a reductant with a free radical scavenger is more effective at preventing lipid oxidation than either alone. In a mixture of 3 monophenols (catechin, resveratrol, and/or quercetin) derived from grapeseed, Pinelo and others (2004) found an initial increase in antioxidative activity followed by a subsequent decrease for all solution combinations. They also reported a possible synergy between quercetin, rutin, and resveratrol toward ONOO. The effect was additive for catechin and epicatechin. These compounds may be acting independently, while other combinations may react with each other. Granato and others (2010) found that (in brown ales) avonoids, total phenolics, and nonavonoid phenolics (hydroxycinnamates and hydroxybenzoates), derived from both the malt and the hops, are strongly correlated with antioxidant activity (ORAC and DPPH). Ghiselli and others (2000) have shown that beer increases serum antioxidant capacity. Ethanol increases absorption of phenolic acids. However, the increase in antioxidant capacity is not due to either ethanol or phenolic acids alone, but rather because of a synergistic effect between the 2.
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Summary
Plant and animal tissues contain unsaturated fatty acids, primarily in the phospholipid fraction of cell membranes. These lipids are especially susceptible to oxidation because of their electrondecient double bonds. The breakdown products of oxidation can produce off-odors, new avors, loss of nutrient content, and color deterioration. To manufacture high-quality, stable food products, the most effective solution is often the addition of antioxidants, either synthetic or natural, which can serve as chain breakers, by intercepting the free radicals generated during various stages of oxidation or to chelate metals. Chain-breaking antioxidants are generally the most effective. A common feature of these compounds is that they have one or more aromatic rings (often phenolic) with one or more OH groups capable of donating H to the oxidizing lipid. Synthetic antioxidants, such as BHA, BHT, and propyl gallate, have one aromatic ring. The natural antioxidants AA and -tocopherol each have 1 aromatic ring as well. However, many of the natural antioxidants (avonoids and anthocyanins) have more than 1 aromatic ring. The effectiveness of these aromatic antioxidants is generally proportional to the number of OH groups present on the aromatic ring(s). Depending on the arrangement of the OH groups, these compounds may also chelate prooxidative metals. The facts that they are natural, and have antioxidative activity that is as good or better than the synthetic antioxidants, makes them particularly attractive for commercial food processors because of consumer demand for natural ingredients.
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