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http://fst.sagepub.com/ Review: Methods Used to Evaluate the Free Radical Scavenging Activity in Foods and Biological Systems
C. Sánchez-Moreno Food Science and Technology International 2002 8: 121 DOI: 10.1106/108201302026770 The online version of this article can be found at: http://fst.sagepub.com/content/8/3/121

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Review: Methods Used to Evaluate the Free Radical Scavenging Activity in Foods and Biological Systems
´ C. SANCHEZ-MORENO*

´n, Departmento de Metabolismo y Nutricio Instituto del Frı´o, Consejo Superior de Investigaciones Cientı´ficas (CSIC). Ciudad Universitaria, 28040 Madrid, Spain
Free radical generation is directly related with oxidation in foods and biological systems. Therefore, the search for methods to determine free radical scavenging is important. In this work are described the methods used for this purpose in both substrates as well as in specific cases of their application. The main methods comprise superoxide radicals scavenging (O2 À ); hydrogen peroxide scavenging (H2O2); hypochlorous acid scavenging (HOCl); hydroxyl radical scavenging (HO ); peroxyl radical scavenging (ROO ), among them are the methods that use azo-compounds to generate peroxyl radicals, such as the ‘‘TRAP’’ method (Total Radical-Trapping Antioxidant Parameter) and the ‘‘ORAC’’ method (OxygenRadical Absorbance Capacity); the scavenging of radical cation 2,2-azinobis-(3-ethylbenzothiazoline-6sulphonate) or the ABTS or the ‘‘TEAC’’ method (Trolox Equivalent Antioxidant Capacity); the scavenging of stable radical 2,2-diphenyl-1-picrylhydrazyl or DPPH method and the scavenging of radical cation N,N-dimethyl-p-phenylenediamine or DMPD method. At present, in spite of the diversity of methods, there is a great need to standardize measurements of antioxidant activity. The search for more specific assays, giving us chemical information that could be related directly to oxidative deterioration of foods and biological systems could be the objective of future research.

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Key Words: free radical scavenging, antioxidant activity, assays, vegetables, biological systems ´ ´ ´ ´ La generacion de radicales esta directamente relacionada con la oxidacion de lı´ pidos y sustratos biologicos, ´ ´ por tanto, es importante la busqueda de metodos para la determinacion del secuestro de especies radicales. ´ ´ En este trabajo se describen los principales metodos utilizados con este fin en ambos sustratos, ası´ como sus ´ ´ ´ aplicaciones especı´ ficas: secuestro de radicales superoxido (O2 À ), secuestro de peroxido de hidrogeno ´ (H2O2); secuestro de acido hipocloroso (HOCl); secuestro de radicales hidroxilo (HO ); secuestro ´ de radicales peroxilo (ROO ), entre los que destacan los metodos que utilizan azo-compuestos para ´ ´ la generacion de radicales peroxilo, tales como el metodo del ‘‘TRAP’’ (Total Radical-Trapping Antioxidant ´ ´ Parameter) y el metodo del ‘‘ORAC’’ (Oxygen-Radical Absorbance Capacity); secuestro del cation radical ´ 2,2-azinobis-(3-etilbenzotiazolin-6-sulfonato) o metodo del ABTS o del ‘‘TEAC’’ (Trolox Equivalent ´ Antioxidant Capacity); secuestro del radical estable 2,2-difenil-1-picrilhidrazil o metodo del DPPH ´ ´ y secuestro del radical cation N,N-dimetil-p-fenilendiamina o metodo del DMPD. Actualmente, a pesar de ´ ´ la diversidad de metodos existentes, hay una gran necesidad de estandarizar estos metodos para la ´ ´ ´ determinacion de la actividad antioxidante. La busqueda de metodos mas especı´ ficos, que proporcionen ´ ´ una informacion quı´ mica que se directamente relacionada con el deterioro oxidativo de alimentos ´ y muestras biologicas, podrı´ a ser el objetivo de futuras investigaciones.

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´ Palabras Clave: secuestro de radicales libres, actividad antioxidante, metodos, vegetales, sistemas ´ biologicos

INTRODUCTION
The methods used to determine activity of foods and biological antioxidants have evolved from chemical assays with lipid substrates to more complex assays to

*E-mail: csanchezm@if.csic.es Received 10 October 2001; revised 23 March 2002.
Food Sci Tech Int 2002;8(3):121–137 ß 2002 Sage Publications ISSN: 1082-0132 DOI: 10.1106/108201302026770

measure total antioxidant capacity in fluids and biological samples. In the case of foods it is necessary to determine the efficacy of natural antioxidants for food protection against oxidative damage, to avoid deleterious changes and loss of commercial and nutritional value (Halliwell ´ et al., 1995; De la Torre Boronat and Lopez Tamames, 1997; Halliwell, 1997). In addition, a rapid method for determining the potential antioxidant capacity in vegetable foods is necessary. This method could be a useful tool to make a selection among different species, varieties, maturation degree and culture conditions, in order to obtain high content of natural 121

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antioxidants in foods (Fogliano et al., 1999; Leonardi et al., 2000). Thus total antioxidant capacity of an edible vegetable product could be a parameter to evaluate the quality of vegetable foods (Arnao et al., 1998; Cano et al., 1998). In the case of biological systems, oxidative stress, an imbalance between reactive oxygen species and defence and repair antioxidant systems, has been shown to be involved in the development of degenerative diseases. Thus, determination of the antioxidant status in biological systems could contribute to prevention and evaluation of diseases related to aging. In addition to organism defences, the intake of dietary antioxidants and evaluation of the real contribution of foods to antioxidant status in biological systems must be evaluated (Halliwell and Gutteridge, 1989; Namiki, 1990; Jacob, 1995; Gurr, 1996). Many different substrates, system compositions and analytical methods are employed in screening tests to evaluate the effectiveness of antioxidants, evidence that many different methods are necessary to evaluate different antioxidant effects. The methodology for evaluating natural antioxidants must be carefully interpreted according to the system and to the analytical method used to determine the extent and end-point of oxidation (Frankel, 1993; Arnao et al., 1999; Fogliano et al., 1999; Frankel and Meyer, 2000). Antioxidant effectiveness is measured by monitoring the inhibition of oxidation of a suitable substrate. After the substrate is oxidized under standard conditions, the extent of oxidation (an end-point) is measured by chemical, instrumental or sensory methods. Hence, the essential features of any test are a suitable substrate, an oxidation initiator and an appropriate measure of the end-point. The combination of substrate, initiator and end-point which have been used are numerous, and even with the same analytical techniques, several analytical strategies are possible (Arnao et al., 1999; Robards et al., 1999). We could classify antioxidant tests in foods and biological systems into two groups: those assays used to evaluate lipid peroxidation, in which a lipid or lipoprotein substrate under standard conditions is used and the degree of oxidation inhibition is measured ´ (Sanchez-Moreno and Larrauri, 1998), and those assays used to measure free radical scavenging ability. Description of the second group is the objective of this review.

trichloromethyl (CCl3 ), superoxide (O2 À ), hydroxyl (HO ), peroxyl (ROO ), and nitric oxide (NO ) are known to be produced metabolically in living organisms. In addition, some non-radical derivatives of oxygen molecules (hydrogen peroxide (H2O2), hypochlorous acid (HOCl)), can be generated in foods and biological systems. All of these reactive oxygen species participate in the chain reaction of free radicals, thus tests of the ability of a substance to scavenge radical species may be relevant in the evaluation of antioxidant activity (Halliwell, 1990; Halliwell et al., 1995).

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Scavenging of Superoxide Radical (O2 À ) Pathological processes are known to involve complex mechanisms. Xanthine oxidase is one of the main enzymatic sources of reactive oxygen species (ROS) in vivo. Although xanthine oxidase present in normal tissue is a dehydrogenase enzyme that transfers electrons to nicotinamideadeninedinucleotide (NAD), as it oxidizes xanthine or hypoxanthine to uric acid, under certain stress conditions the dehydrogenase is converted to an oxidase enzyme by oxidation of essential thiol groups or by limited proteolysis. Upon this conversion the enzyme reacts with the same electron donors, but reducing oxygen instead of NAD, thus producing superoxide and hydrogen peroxide, and contributing to the initiation and progression of a number of pathological processes (Halliwell and Gutteridge, 1990; Halliwell et al., 1995; Hippeli and Elstner, 1999). The scavenging activity towards O2 À of a wide range of antioxidants is measured in terms of inhibition of generation of O2 À with the hypoxanthine–xanthine oxidase superoxide generating system (HX–XO) (Robak and Gryglewski, 1988; Halliwell, 1990; Mitsuya et al., 1990; Constantino et al., 1992; Minamiyama et al., 1995; Kruedener et al., 1995; Yen and Chen, 1995; Ramanathan et al., 1996; Robak and Sato et al., 1996; Lavelli et al., 1999, 2000; Suh et al., 1999; Saint-Cricq de Gaulejac et al., 1999a,b; Deguchi, 2000; Kubo et al., 2000; Lu and Foo, 2000; Unno et al., 2000; Wang and Jiao, 2000; Yamaguchi et al., 2000a; Calliste et al., 2001; Kweon et al., 2001). To a minor extent, O2 À is generated using a non-enzymatic reaction of phenazine methosulphate in the presence of NADH and molecular oxygen (Nishikimi et al., 1972; Robak and Gryglewski, 1988; Yen and Chen, 1995; Yen and Hsieh, 1995; Yamaguchi et al., 2000b; Barthomeuf et al., 2001). In both strategies, O2 À reduces nitro-blue tetrazolium (NBT) into formazan at pH 7.4 and room temperature, and formazan generation is followed by spectrophotometry at 560 nm. Any added molecule capable of reacting with O2 À , inhibits the production of formazan. Wang and Jiao (2000) used hydroxylammonium chloride as oxidant agent instead of NBT. The consequent nitrile formation from hydroxylammonium is followed by measuring the absorbance due to nitrile at 530 nm. In a

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METHODOLOGIES FOR TESTING RADICAL SCAVENGING SPECIES
A free radical is any species that contains one or more unpaired electrons and is capable of independent existence (Halliwell et al., 1995). Free radicals such as

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similar way as previously, the production of nitrile is inhibited by any added molecule capable of reacting with O2 À . Either in case of NBT or hydroxylammonium, the reduction of the absorbance is estimated as superoxide scavenging activity compared to the value obtained with no test added sample. In the HX–XO reaction system, Kruedener et al. (1995) and Lavelli et al. (1999, 2000) evaluated the inhibition of O2 À production in the presence of -ketomethiolbutyric acid (KMB). The decomposition of KMB by O2 À releases ethene, which is measured by gas chromatography. Other authors using the same HX–XO reaction system (Mitsuya et al., 1990; Sato et al., 1996; Suh et al., 1999; Deguchi et al., 2000; Yamaguchi et al., 2000a; Unno et al., 2000; Calliste et al., 2001) analyzed the O2 À scavenging activity by electron-spin resonance (ESR) spectrometry. The O2 À is trapped with 5,5dimethyl-1-pyrroline N-oxide (DMPO), and the resultant DMPO-OH adduct is detected by ESR using manganese oxide as internal standard. The hydrogen peroxide/sodium hydroxide/dimethyl sulfoxide (DMSO) system is designed to evaluate both water-soluble and oil-soluble free radical scavengers as a non-enzymatic and non-Fenton type ROS generating system in which not only O2 À and hydroxyl radicals, but also methyl radicals are generated (Yamaguchi et al., 2000a). The primary function of the HX–XO system is to oxidize xanthine or hipoxanthine to uric acid. Therefore, the inhibition of the activity of XO is measured by the evaluation of uric acid production, which is formed along with O2 À (Hayashi et al., 1988; Robak and Gryglewski, 1988; Kweon et al., 2001). Based in ESR measurement, Unno et al. (2000) suggested that a likely possible action of certain antioxidants is to scavenge O2 À directly, without inhibiting the function of xanthine oxidase. In order to allow comparison among assays, it is useful to compare the obtained inhibition of the antioxidant with that obtained by the superoxide dismutase enzyme, or by standard antioxidants, such as -tocopherol or ascorbic acid. Measurements of O2 À scavenging should be interpreted with caution, because no equilibrium can be achieved when superoxide radicals are generated continuously during the test (Frankel and Meyer, 2000). The above assay has been applied to flavonoids and vitamins (Hayashi et al., 1988; Robak and Gryglewski, 1988; Ramanathan et al., 1996), gallic acid and derivatives (Aruoma et al., 1993; Gaujelac et al., 1999; Kubo et al., 2000), processed grain foods (Minamiyama et al., 1995), tea extracts (Yen and Chen, 1995), xylose–lysine maillard reaction products (Yen and Hsieh, 1998), berry extracts (Constantino et al., 1992; Wang and Jiao, 2000) seed extracts from Borago officinalis L. (Wettasinghe and Shahidi, 1999), procyanidins from grape-seed and wine extracts (Saint-Cricq de Gaulejac, 1999a), apple pectic oligosaccharides with small molecular weights

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(Tazawa et al., 1999), manufactured tomatoes (Lavelli et al., 1999, 2000), pigments from barley bran-fermented broth (Deguchi et al., 2000), polyphenols from apple pomace (Lu and Foo, 2000) and from onion skin (Suh et al., 1999), catechins from tea (Unno et al., 2000), purified garcinol from Garcinia indica (Yamaguchi et al., 2000a,b), honey and related products (Nagai et al., 2001), a high molecular weight hydroxycinnamatederived polymer (Barthomeuf et al., 2001), bamboo (Kweon et al., 2001), and several plants (Calliste et al., 2001). Scavenging of Hydrogen Peroxide (H2O2) The generation of hydrogen peroxide (H2O2) by activated phagocytes is known to play an important part in the killing of several bacterial and fungal strains. Additionally, H2O2 is generated in vivo by several oxidase enzymes. There is increasing evidence that H2O2, either directly or indirectly via its reduction product OH À, acts as a messenger molecule in the synthesis and activation of inflammatory mediators (Auroma et al., 1989). Hydrogen peroxide-scavenging activity is easily and sensitively measured by using peroxidase-based assay systems. The most common employs horseradish peroxidase, which uses H2O2 to oxidize scopoletin into a nonfluorescent product. In the presence of a putative scavenger, the oxidation of scopoletin is inhibited and the H2O2 scavenging can be monitored (Halliwell, 1990). ´ Following this assay, Martı´ nez-Tome et al. (2001a, b) evaluated the antioxidant activity of broccoli amino acids, and of Mediterranean spices in an aqueous medium. Other assays have been used to a minor extent. The assay for H2O2 in fruit juices of blackberry, raspberry, cranberry, blueberry, and strawberry is carried out measuring the direct reaction of H2O2 and titanium(IV) (Ti). Precipitated Ti–H2O2 complex is dissolved in sulphuric acid and measured at 410 nm (Wang and Jiao, 2000). The ability of tea extracts (Yen and Chen, 1995) to scavenge H2O2 is followed by decay in H2O2 concentration. This is determined spectrophotometrically from absorption at 230 nm using the molar optical density of 81 MÀ1 cmÀ1. The scavenging activity towards H2O2 was estimated in seed extracts from Borago officinalis L. (Wettasinghe and Shahidi, 1999) and in an amino acid fraction from aged garlic extract (Ryu et al., 2001). Scavenging of Hydroxyl Radical (HO ) Hydroxyl radical (HO ) scavenging can often be calculated using the ‘‘deoxyribose assay’’: a mixture of ferric chloride (FeCl3) and ethylenediamine tetraacetic acid (EDTA) in the presence of ascorbate reacts to form iron(II)-EDTA plus oxidized ascorbate, H2O2 then

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reacts with iron(II)-EDTA to generate iron(III)-EDTA plus HO in the so-called Fenton reaction. (Fe2 þ þ H2O2 ! Fe3 þ þ OH À þ HO ). Those radicals not scavenged by other components of the reaction mixture attack the sugar deoxyribose, and degrade it into a series of fragments, some or all of which react on heating with thiobarbituric acid at low pH to give a pink chromogen. Thus the scavenging activity towards HO of a substance added to the reaction mixture is measured on the basis of the inhibition of the degradation of deoxyribose (Halliwell, 1990; Aruoma et al., 1993). This system was used by Ghiselli et al. (1998) to evaluate antioxidant activity of different phenolic fractions separated from red wine, by Tazawa et al. (1999) to evaluate antioxidant activity of apple pectic oligosaccharides with small molecular weights, by Barthomeuf et al. (2001) to evaluate a high molecular weight hydroxycinnamate-derived polymer, and by Martı´ nez´ Tome et al. (2001a,b) to evaluate antioxidant activities of broccoli amino acids, and of certain Mediterranean spices. Hagerman et al. (1998) modified the deoxyribose method by omitting ascorbic acid to evaluate the potential of certain tannins (methyl-gallate) to behave as pro-oxidants. Compounds which act as pro-oxidants are thought to be detrimental since they may enhance oxidative damage. In this modification of the method, pro-oxidants substitute for ascorbic acid in the Fenton reaction and increase color formation over the ascorbic acid-free controls. The generation of HO in the Fenton reaction is due to the presence of the iron ions. Some compounds inhibit color formation in the deoxyribose assay, not by reacting with HO but by chelating iron ions and preventing HO formation. To identify compounds which chelate metal, the deoxyribose assay is performed without EDTA (Aruoma, 1994, Hagerman et al., 1998). In the absence of metal chelating test compounds, iron ions are complexed to deoxyribose and causes ‘‘site specific’’ hydroxyl radical damage. When an iron chelating test substance is present, hydroxyl radical damage and the accompanying color production is diminished. In order to elucidate if the reaction mechanism is the direct radical scavenge and not inhibition of the Fenton reaction by chelation, Yamaguchi et al. (1999, 2000a) evaluated in the H2O2/ NaOH/DMSO system the scavenging activity towards HO of some extracts from Garcinia indica and grape seed. HO are identified because of their ability to form nitroxide adducts from the commonly used DMPO spin trap. This spin trap has a greater ability to trap oxygencentered radicals than other nitrogen spin traps. The adduct DMPO–OH radical exhibits a characteristic ESR response. Moreover, these adducts have relatively long lives, whereas the lifespan of HO is very short. Spin trapping has become a valuable tool to characterize and quantify each oxygen radical (Rimbach, 1999). By

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this method the scavenging effect towards HO of flavonoids from onion skin is evaluated (Suh et al., 1999), various tea extracts (Yen and Chen et al., 1995), and certain plant extracts of different polarities (Calliste et al., 2001), naturally furan fatty acids (Okada et al., 1996), garcinol from Garcinia indica fruit (Yamaguchi et al., 2000a), grape seed (Yamaguchi et al., 1999) and garlic (Yang et al., 1994). Saint-Cricq de Gaulejac et al. (1999b) evaluated the scavenging effect of grape seed extracts towards HO in an in vitro system called 3D (damaged DNA detection). In this system HO , generated by Fenton’s reaction, induced some strand breaks, modifications, or loss of bases in plasmid DNA. The protective power of a potential antioxidant on DNA is measured in terms of percentage of repair ratio of damaged DNA.

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Scavenging of Hypochlorous Acid (HOCl) Another source of strong oxidants in vivo is neutrophil myeloperoxidase (MPO), which catalyzes oxidation of chloride ions by H2O2, resulting in hypochlorous acid (HOCl) production. The cytotoxicity of this reaction contributes to the killing of bacteria in the host defence system. However, HOCl generated by MPO might also inactivate 1-antiproteinase and contribute to proteolytic damage of healthy human tissues in inflammatory disease (Halliwell and Gutteridge, 1990; Hippeli and Elstner, 1999). Antioxidants can be tested for their potential to interfere with tissue damage caused by HOCl. Many compounds can act as HOCl scavengers and are tested using this assay, such as, ascorbic acid, albumin (Halliwell, 1990), gallic acid and derivatives (Aruoma et al., 1993) and carotenoids (Lavelli et al., 2000). Scavenging of HOCl can be examined using MPO/ H2O2/sodium chloride as a source of this substance. In this reaction system, Lavelli et al. (1999, 2000) evaluated the inhibition by tomato extracts of different polarities of HOCl production in the presence of 1-aminocyclopropane-1-carboxylic acid (ACC). The reaction is followed by measurement by GLC of ethene release from ACC by HOCl. Scavenging of HOCl can be examined in a system in which HOCl is generated immediately by adjusting sodium hypochlorous to pH 6.2, with dilute sulphuric acid. At the end of the reaction with test antioxidant, 1-antiproteinase is added to the reaction mixture. The inactivation of this enzyme by HOCl is followed by adding elastase, which is inactivated by any remaining 1-antiproteinase. The remaining elastase activity is measured using elastase substrate (Nsuccinyltriala-p-nitroanilide) and monitoring increases in absorbance at 410 nm. This assay was used by ´ Martı´ nez-Tome et al. (2001a,b) to evaluate the antioxidant activity of broccoli amino acids and of Mediterranean spices.

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Scavenging of Peroxynitrite (ONOO ) Peroxynitrite (ONOOÀ) is formed by the reaction of nitric oxide and superoxide. ONOOÀ is a cytotoxic reactive species that can be generated by endothelial cells, neutrophils, and macrophages (Balvoine and Geletti, 1999). ONOOÀ scavenging by the oxidation of dihydrorhodamine 123 to fluorescent rhodamine 123 is measured in the presence of potential antioxidant with a microplate fluorescent spectrophotometer with excitation and emission wavelength of 485 and 530 nm, respectively. The assay measures the potency of marine algae and green tea tannin extracts in the inhibition of DHR 123 oxidation by ONOOÀ (Chung et al., 1998, 2001). Scavenging of Peroxyl Radical (ROO ) The peroxyl radical is a common free radical found in biological substrates and used in antioxidants assays. This is slightly less reactive than HO and thus possesses an extended half-life of seconds instead of nanoseconds (Halliwell et al., 1995). Assays of examining peroxyl radical scavenging using azo-compounds are extensively used. Naguib (2000) has used a method using 4,4-difluoro-3,5-bis-(4-phenyl-1,3butadienyl)-4-bora-3a,4a-diaza-s-indacine as an indicator, and 2,20-azobis-2,4-dimethylvaleronitril as generator of peroxyl radicals, to evaluate the antioxidant activity of astaxanthin and related carotenoids. Terao et al. (1994) have evaluated the protective effect of several polyphenols such as catechin, epigallocatechin, and quercetin in the induced lipid peroxidation of liposomes by 2,20-diazobis-(2-amidinopropane) dihydrochloride (ABAP). Natella et al. (1999) have determined the scavenging ability of benzoic and cinnamic acids following absorbance decay at 443 nm of a mixture of crocin and ABAP. Yokozawa et al. (2000) have studied the antioxidant protection of green tea extracts and a mixture of tannins from green tea in a culture of epithelial kidney cells (cell line LLC-PK1), using ABAP azo-compound as generator of peroxyl radical at constant rate. Rigo et al. (2000) have studied the scavenging ability of Italian red wines using 2,20-azobis-(2-(2imidazolin-2-yl)propane as generator of peroxyl radicals and linoleic acid as oxidable substrate. The assay was validated using gallic acid as standard. Chun et al. (2000) evaluated the antioxidant activity of bamboo by measuring conjugated diene in a peroxidation liposome model initiated by peroxyl radical induced by 2,20azobis-(2-amidinopropane) dihydrochloride (AAPH).

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TRAP assay (Total Radical-Trapping Antioxidant Parameter) Ingold group (Wayner et al., 1985) introduced this assay for the determination of the antioxidant status of

human plasma. Peroxyl radicals are generated at a controlled rate by the thermal decomposition of a watersoluble ‘‘azo-initiator’’, such as ABAP. After adding ABAP to the plasma, the oxidation of the oxidizable materials is monitored by measuring the oxygen consumed during the reaction. The induction period, in which oxidation is inhibited by the antioxidants in the plasma, is compared to that of Trolox (6-hydroxyl2,5,7,8-tetramethylchroman-2-carboxylic acid) (hydrosoluble vitamin E analogue) used as reference water-soluble antioxidant, and then quantitatively related to the antioxidant capacity of plasma. This method was later modified (Wayner et al., 1987) and allowed the formed peroxyl radical to react with a lipid (e.g., a suspension of linoleic acid or an ester), whereupon it caused peroxidation. Studies of the ability to protect lipid substrates against peroxidation by ABAP derived radicals have shown that ascorbic acid is an excellent scavenger of water-soluble peroxyl radicals (Halliwell, 1990). The Ingold group has given the contribution of several different antioxidants (ascorbate > thiols > bilirrubin > urate > vitamin E) in plasma to total TRAP value (Wayner et al., 1987). This assay was later modified by Delange and Glazer (1989), replacing the lipid substrate with R-phycoerythrin (R-PE) or -phycoerythrin ( -PE), a phycobiliprotein containing a red photoreceptor pigment, and correlated the fluorescent decay of R-PE with the activity of an antioxidant (excitation wavelength 495 nm, emission wavelength 575 nm). Ghiselli et al. (1995) proposed some modifications to the assay of Delange and Glazer (1989), measuring plasma antioxidant activity and taking into account several aspects such as interference from lipids and proteins, contribution of several different antioxidants from plasma to total TRAP value, synergistic effects of thiols and ascorbic acid, interference of metal ions, and effect of plasma storage to TRAP value. This method served to analyze the influence of the consumption of tea and red wine (Serafini et al., 1994, 1996, 1998) and tomato (Pellegrini et al., 1999) on the antioxidant activity of human plasma was evaluated, following oxidation kinetics through the decay of fluorescent of R-PE at a specific time (90 min). The lag phase inducted by plasma is compared to that of Trolox, and expressed as TRAP value (mM) (Trolox micromoles having the same antioxidant activity towards peroxyl radicals as one liter of plasma). Alho and Leinonen (1999) reviewed this method and concluded that the measurement of plasma TRAP might not be valid, since free radical production would have to be sufficiently extensive to disturb the steady state level of antioxidants and disrupt the compartmentalization protection afforded by cell membranes. This assay has been applied to compare the effects of dietary olive and soybean oil in antioxidant defenses in rats (Lespine et al., 2001), and to evaluate the effects of ethyl alcohol and wine on

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the TRAP value in plasma. Wollny et al. (1999) showed that red wine induced a three-fold increase in total radical-trapping antioxidant parameter of rat plasma compared to controls, while white wine and alcohol did not show any effect. This assay could be also be applied in vitro to the evaluation of antioxidant activity of beverages and foods. Thus, it has been used to study green tea and red wine, expressing the results as Trolox equivalents, that is, Trolox micromoles that have the same scavenging peroxyl radical ability as one liter of beverage (Serafini et al., 1996, 1997; Ghiselli et al., 1998; Pietta et al., 1998a, b). In oil samples subjected to peroxyl radical attack by the lipophilic azo compound 2,20-azobis(2,4dimethylvaleronitrile) (AMVN), the total antioxidant capacity of the oil is determined by oxygen consumption measured with a Clark-type electrode. In this method, TRAP is determined by measuring the length of time that oxygen uptake is inhibited (Cabrini et al., 2001). ORAC assay (Oxygen-Radical Absorbance Capacity) The ORAC assay is based largely on the work reported by Glazer’s laboratory (Delange and Glazer, 1989) and depends on the unique properties of phycoerytrin, which is used as a target of free radicals. In the ORAC assay the antioxidant capacity is quantified by calculating the net protection area under the time recorded flurorescence decay curve of R-PE or -PE in the presence of antioxidant or serum. AAPH as a peroxyl radical generator (ORACROOÁ ) or copper(II)-H2O2 as mainly a hydroxyl radical generator (ORACHOÁ ), or copper(I) as a transition metal oxidant (ORACCu) are used. The ORAC assay combines both inhibition time and inhibition percentage of free radical action by antioxidants using an area under curve technique for quantification. This assay expresses the results as ORAC units or Trolox equivalents, which correspond to the amount of Trolox micromoles that have the same antioxidant activity as one liter of the tested solution (Cao et al., 1993, 1995). In the case of copper(II) alone used as an oxidant in the assay, Trolox cannot be used as an antioxidant standard since Trolox may act as a prooxidant in the presence of copper(II). Therefore, in this case the antioxidant action is expressed as antioxidant units (1 unit equals the antioxidant activity which increases the area under the -PE decay curve by 100%). In the case of plasma or enriched protein samples, an interference in the scavenging of peroxyl radicals by protein thiol groups may occur (Ghiselli et al., 1995). Recently, a modification has been introduced in the ORAC assay to eliminate protein content with trichloroacetic acid (Prior and Cao, 1999b). An improved method of ORAC assay has been developed and validated using fluorescein as the

fluorescent probe (Ou et al., 2001). This modification provides a direct measure of hydrophilic chain breaking antioxidant capacity against peroxyl radical. However, it is usually not possible to determine directly the contribution of specific phytonutrients to the total ORAC value. A principal drawback of the ORAC method is that it is assumed that the oxidative deterioration and, in turn, the antioxidative mechanism and protection of the fluorescence protein -PE can mimic critical biological substrates (Frankel and Meyer, 2000). The same drawback extends to the TRAP method, which also uses -PE as oxidable substrate. The ORAC assay has provided substantial information regarding the antioxidant capacity of pure compounds such as antocianidins (Wang et al., 1997), flavonoids (Cao et al., 1997a), and caffein (Lee, 2000), food complex matrix such as common vegetables (Cao et al., 1996a; Guo et al., 1997, 1999a,b; Kalt et al., 1999; Caldwell, 2001), fruits (Wang et al., 1996), berries (Wang and Lin, 2000), cocoa and chocolate (Adamson et al., 1999), tea (Cao et al., 1996a; Prior and Cao, 1999a), and oat (Handelman et al., 1999). Also, ORAC is useful to evaluate the influence of cultivar and storage temperatures on the antioxidant activity of cranberries (Wang and Stretch, 2001). ORAC has also been applied to the evaluation of total antioxidant status in animal tissues (Cao et al., 1996b, c, 1999), and plasma of different species (Cao et al., 1997a; Cao and Prior, 1998, 1999a; Ninfali and Alugi, 1998; Chao et al., 1999; Prior and Cao, 1999b), and in bioavailability human studies of vitamin C, carotenoids, anthocyanins, and other phenolic compounds from berries, fruits, vegetables and wine (Cao et al., 1998a, b; Paiva et al., 1998; Cao and Prior, 1999b; Ehlenfeldt and Prior, 2001). Scavenging of Radical Cation 2,2-azinobis-(3-ethylbenzothiazoline-6-sulphonate) (ABTS þ ). TEAC assay (‘‘Trolox Equivalent Antioxidant Capacity’’) or ABTS assay

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The ABTS (2,2-azinobis-(3-ethylbenzothiazoline-6sulphonic acid)) assay is based on the inhibition by antioxidants of the absorbance of the radical cation 2,2azinobis-(3-ethylbenzothiazoline-6-sulphonate) (ABTS þ ), which has a characteristic long-wavelength absorption spectrum showing main absorption maxima at 415 nm, and secondary absorption maxima at 660, 734, and 820 nm. The original method was based on the activation of metmyoglobin, acting as peroxidase, with H2O2 via the formation of the ferrylmyoglobin radical, which then oxidizes the phenothiazine compound ABTS, forming the ABTS þ radical cation. In terms of assay design, several different analytical strategies are used: decolorization and inhibition strategies, in which the absorbance of the reaction mixture is read when the

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color of the incubation mixture is stable or at a fixed time point, respectively, and lag phase strategy, in which the length of lag phase before the antioxidant reaction starts is measured (Miller et al., 1993; Rice-Evans and Miller, 1994). These authors (Rice-Evans and Miller, 1997a) found that results of the metmyoglobin/ABTS assay and ABTS decolorization assay, in which the ABTS þ radical cation is generated directly by chemical reduction by manganese dioxide in the absence of heme protein and H2O2, is very similar. They established that the action of the antioxidant studied acted via scavenging of the ABTS þ radical cation and not by inhibition of its formation through reduction of ferrylmyoglobin or reaction with H2O2. Recently, a modification of this method has been introduced by a decolorization technique in which the radical is generated directly in a stable form using potassium persulphate (Re et al., 1999). Afterwards, the formed radical is mixed with the antioxidant in the reaction medium and the percentage inhibition of absorbance at 734 nm is calculated and plotted as a function of concentration of antioxidants. Arnao and co-workers (Arnao et al., 1996, 1998, 1999, 2001a, b; Cano et al., 1998), introduced some modifications in this assay: the ABTS þ radical cation is generated enzymatically using the system formed by H2O2 and horseradish peroxidase (ABTS/ H2O2/HRP). The reaction is monitored at a wavelength selected between 400 and 750 nm, to avoid exogenous interference. Two strategies may be used: the antioxidant compounds are added previously to the formation of the ABTS þ radical cation and then the lag phase, caused by different antioxidants in the production of the ABTS þ radical cation, is measured. The ABTS þ radical cation is pre-generated and when stable absorbance is obtained the antioxidant sample is added to the reaction medium, and the antioxidant activity is measured in terms of decolorization. Several authors (Campos and Lissi, 1996; Van der Berg et al., 1999) proposed a modification based on pregeneration of the ABTS À radical anions by heating the radical cation 2,2-azinobis-(3-ethylbenzothiazoline6-sulphonate (ABTS2 À) with a thermolabile azo compound ABAP. Generation of radicals before the antioxidants are added prevents interference of compounds, which affect radical formation. This modification makes the assay less susceptible to artefacts and prevents overestimation of antioxidant capacity. The usual use of Trolox as a standard allows the assay to be called TEAC; the results are expressed as Trolox equivalents, that is, the concentration of Trolox solution (mmol/L) with an equivalent antioxidant potential to 1.0 mmol/L solution of the substance under investigation. Since ABTS þ radical cation can be dissolved in aqueous and acidified ethanol medium (Arnao et al., 1998) this assay is capable of testing the antioxidant activity of hydrophilic and lipophilic compounds. In

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order to evaluate the lipophilic compounds, several solvents (dichloromethane, tetrahydrofuran, acetone and Titron X-100) have been tested for their compatibility with both aqueous or ethanol solutions containing ABTS þ (Scalfi et al., 1999; Van der Berg et al., 1999). The metmyoglobin/ABTS assay has been used to evaluate the total plasma antioxidant status of premature neo-nates (Miller et al., 1993). It showed that whereas urate, -tocopherol and ascorbate are as effective as Trolox in their antioxidant activity, desferrioxamine is three times more effective as a scavenger. The interfering substances in this assay are peroxidases, such as heme proteins which, in the presence of H2O2, promote the formation of the ABTS þ radical cation. Drug and other exogenous materials with significant absorption at 734 nm might also be potential sources of positive interference in the assay. Bilirubin is more efficacious than those compounds, whereas albumin is less active. Also with the same assay, relative antioxidant activities in the aqueous phase of plant-derived polyphenolic flavonoids and phenolic acids is measured (Rice-Evans et al., 1995, 1997a; Salah et al., 1995). The relative contributions of ascorbic acid and phenolic antioxidants to the total antioxidant activity of orange, and apple fruit juices and blackcurrant drink was evaluated by the former assay (Miller and Rice-Evans, 1997b). Also, the status of liposoluble antioxidants in patients with Crohn’s disease (Genser et al., 1999), the in vivo antioxidant effect of green tea (Sung et al., 2000) and the effect of a vitamin E and -carotene human supplementation study in total antioxidant plasma (Calzada et al., 1995) has been evaluated. On the basis of the same assay the TEAC values were calculated for polymeric polyphenol compounds (Hagerman et al., 1998), anthocyanins mixtures from red cabbage, black currant, black chokeberry, and roselle (Degenhardt et al., 2000), and methanol extracts of some Yemeni plants (Alzoreky and Nakahara, 2001). On the basis of the ABTS decolorization assay, in which the ABTS þ radical cation is generated by chemical reduction by manganese dioxide, the antioxidant effects of quercetin from onions (McAnlis et al., 1999) and fruit juice intake (Young et al., 1999) was evaluated. The antioxidant capacity of carotenes and xanthophylls (Miller et al., 1996), wines (Fogliano et al., 1999), the water-insoluble fraction from tomatoes (Leonardi et al., 2000; Scalfi et al., 2000), the flavan-3ol fraction from grape seeds (Castillo et al., 2000), and flavonoids from Olea europea L. leaves (BenaventeGarcı´ a et al., 2000) has been measured. Using ABTS/metmyoglobin in the presence of H2O2, the antioxidant activity of phenolic compounds from cereal grains (Zielinski and Kozlowska, 2000), red wine polyphenols (Simonetti et al., 1997; Soleas et al., 1997; Pellegrini et al., 2000), green and black tea (Liebert et al., 1999), selected medicine plants (Pietta et al., 1998),

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phenolic compounds from Salvia officinalis (Wang et al., 1998), and beer (Szwajgier and Targonoski, 2000) was determined. On the basis of pre-generation of the ABTS þ radical cation with a thermolabile azo compound ABAP, lipophilic and hydrophilic compounds with antioxidant capacity (Van der Berg et al., 1999), several wines (Campos and Lissi, 1996), and crystal malt extracts (Woffenden et al., 2001) were tested. Also, the effect of moderate consumption of beer, red wine and spirits on plasma antioxidants in middle-aged men was evaluated (Van der Gaag et al., 2000). The antioxidant capacity relative to L-ascorbic acid was measured on the basis of the generation of the ABTS þ radical cation in the ABTS/H2O2/HRP system in terms of lag time, for butylated hydroxytoluene, Trolox, L-cysteine and glutathione compounds, orange juice and grapefruit juice (Arnao et al., 1996). With the same assay, the antioxidant activity in terms of decolorization assay was measured for orange juice and grapefruit juice (Cano et al., 1998), wines (CanoLario et al., 1999), hydrophilic and lipophilic compounds in vegetable soaps (Arnao et al., 2001a), leaf extracts of barley, oat and citrus (Arnao et al., 2001b), pomegranate juice (Gil et al., 2000), lipophilic vitamins (Cano et al., 2000), and the effects of pH, temperature and light conditions in the antiradical activity of betanine from Beta vulgaris L. roots (Pedreno and Escribano, 2001). The antioxidant capacity of fruits (Leong and Shui, 2002), tannin–protein complexes (Riedl and Hagerman, 2001), and walnut polyphenols (Anderson et al., 2001), and the influence of heating in total antioxidant activity of olive oils (Pellegrini et al., 2001) was measured by the technique in which the ABTS þ radical cation is generated directly in a stable form using potassium persulfate.

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with different amounts of Trolox. This method is used to measure hydrophilic compounds. It is worth noting that the high stability of the point fixed for measurement makes the effect of time variation negligible, allowing a high interassay reproducibility (Fogliano et al., 1999). The presence of organic acids, especially citric acid, in some extracts may interfere with the DMPD assay, and so this assay should be used with caution in those extracts rich in organic acids (Gil et al., 2000). This method is used to evaluate the antioxidant capacity of wines (Fogliano et al., 1999), water solublefraction of tomatoes (Scalfi et al., 2000), red wines, green tea infusion and pomegranate juice (Gil et al., 2000). Scavenging of the Stable Radical 2,2-diphenyl-1-picrylhydrazyl – DPPH assay

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Scavenging of Radical Cation from N,N-dimethyl-pphenylenediamine – DMPD assay This assay is similar to that from Re et al. (1999), in which the ABTSþ radical cation is chemically pregenerated. The main difference is the use of the hydrophilic compound N,N-dimethyl-p-phenylenediamine (DMPD). In the presence of a suitable oxidant solution (ferric chloride) at an acidic pH, DMPD is converted to a stable and coloured DMPD radical cation (DMPD þ ). The UV-visible spectrum of this compound shows maximum absorbance at 505 nm. Antioxidant compounds which are able to transfer a hydrogen atom to DMPD þ cause a decolorization of the solution which is proportional to their concentration. This reaction is rapid (less than 10 min) and the end point, which is stable, is taken as a measure of the antioxidant efficiency. Antioxidant ability is expressed as Trolox equivalents using a calibration curve plotted

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This assay is based on the measurement of the scavenging ability of antioxidants towards the stable radical 2,2-diphenyl-1-picrylhydrazyl (DPPH ). The free radical DPPH is reduced to the corresponding hydrazine when it reacts with hydrogen donors ´ (Contreras-Guzman and Strong, 1982). This ability is evaluated using electron spin resonance spectroscopy on the basis that the DPPH signal intensity is inversely related to the test antioxidant concentration and to the reaction time (Scheller et al., 1990; Minamiyama et al., 1994; Noguchi et al., 1994; Yoneda et al., 1995; Chen et al., 2000; Deguchi et al., 2000; Calliste et al., 2001; Wasek et al., 2001; Yu, 2001), but the more frequently used technique is the decoloration assay, which evaluates the absorbance decrease at 515–528 nm produced by the addition of the antioxidant to a DPPH solution in ethanol or methanol. Different authors use different initial radical concentrations and different reaction times. DPPH assay is considered a valid and easy assay to evaluate scavenging activity of antioxidants, since the radical compound is stable and does not have to be generated as in other radical scavenging assays. ´ Sanchez-Moreno et al. (1998, 1999a, b) have proposed a new methodology for the evaluation of the antiradical efficiency towards DPPH . Their procedure takes into account not only the antioxidant concentration but also the reaction time to reach the plateau of the scavenging reaction, a modification that could be an advantage over other methods, which only consider antioxidant con´ centration. De Ancos et al. (2000) and Jimenez-Escrig et al. (2000) have applied this modified procedure to the determination of the scavenging activity of raspberries and cranberries, and carotenoids, respectively. From the methodological point of view the DPPH method is recommended as easy and accurate with regard to measuring the antioxidant activity of fruit and vegetable juices or extracts. The results are highly reproducible and comparable to other free radical

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scavenging methods such as ABTS (Gil et al., 2000). Both radicals show the same stoichiometry with Trolox: 2 moles of ABTS þ (Cano et al., 1998) or 2 moles of DPPH radicals (Leong and Shui, 2002) are scavenged by 1 mol of the hydrosoluble vitamin E analogue. Results using the DPPH method further show that the interaction of a potential antioxidant with DPPH depends on its structural conformation (Kaur and Kapoor, 2001). The DPPH method is not useful for measuring the antioxidant activity of plasma, because protein is precipitated in the alcoholic reaction medium. This assay has been applied to hydrolyzable tannins (Lin et al., 1974; Yoshida et al., 1989), lignans (Filleur et al., 2001), polyphenolic compounds (Brand-Williams et al., 1995; Bondet et al., 1997; Yokozawa et al., 1998), phenolic acids and derivatives (Silva et al., 2000), phenolic acids in oil matrix (Pekkarinen et al., 1999), hydroxycinnamic acid compounds (Chen and Ho, 1997), flavonoids (Lebeau et al., 2000; Madsen et al., 2000; Burda and Oleszek, 2001), hydroxi-flavones (Cotelle et al., 1996), procyanidins (Saint-Cricq de Gaulejac et al., 1999a, b), catechins (Sawai and Sakata, 1998), resveratrol (Wang et al., 1999; Tadolini et al., 2000), conjugated linoleic acids (Yu, 2001), polysaccharides (xanthan, tragacanth gum, methylcellulose) on soybeanoil emulsion (Shimada et al., 1992), fucoxhantin (Nomura et al., 1997), tannins from oriental herbs (Yokozawa et al., 1998), plant phenols from unfermented rooibos tea (Von Gadow et al., 1997), polyphenols from methanol and ethylacetate extracts from Lactuta scarola (Kim, 2001), polyphenols from apple pomace (Lu and Foo, 2000) and from Salvia officinalis (Wang et al., 1998), phenolic acids from fresh orange juices (Rapisarda et al., 2000), non-tannin phenolics from canola hulls (Amarowicz et al., 2000), flavonoids from barley leaves and soy bean (Okawa et al., 2001), gallic acid, catechin and stilbene from Polyginum multiflorum extracts (Chen et al., 1999), quercetin from onion skin (Suh et al., 1999), garcinol from Garcinia indica (Yamaguchi et al., 2000a, b), citrus essential oils (Choi et al., 2000), oil fractions (Espı´ n et al., 2000a; Gordon et al., 2001), waxy mixture from beehives (Scheller et al., 1990), resinous exudates from Heliotropium spp. (Lissi et al., 1999), anthocyanin-based natural colorants from berries (Espı´ n et al., 2000b), curcumin (Noguchi et al., 1994; Sreejayan and Rao, 1996), antibrowning agents (Kubo et al., 2000), Maillard reaction products (Yen and Hsieh, 1995; Chevalier et al., 2001; Morales and ´ ´ Jimenez-Perez, 2001; Tressi et al., 2001), tea (Yen and Chen, 1995; Nanjo et al., 1996), pigments from barley bran-fermented broth (Deguchi et al., 2000), grape pomace (Larrauri et al., 1998), avellana hulls (Moure et al., 2000), berries (De Ancos et al., 2000; Fukumoto and Mazza, 2000), different edible vegetable products (Miller et al., 2000; Du Toit et al., 2001; Leong and Shui, ´ 2001), oils (Jimenez et al., 1993), cognacs (Da Porto et al., 2000), chloroform extract from Cedrus deodara

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Table 1. Antioxidant activity of red wine and green tea measured by several radical scavenging methods.
DPPH Red Wine

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ABTS DMPD (H2O2/HRP) (mmol TE/mL)a

TRAP 7.8 (3250 ppm catechin eq.) 14

7.5 6.0 8.7 (2036 ppm p-coumaric acid eq.) 7.6 6.1 4.4 (1029 ppm p-coumaric acid eq.)

Green Tea
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According to Gil et al. (2000) and Serafini et al. (1996).

(Tiwari et al., 2001), different polarities extracts of leaves and seeds from Rumex crispus (Yildririm et al., 2001), from cardamom (Kikuzaki et al., 2001), and from several plants (Diallo et al., 2001), and edible seaweed ´ (Yan et al., 1998, 1999; Jimenez-Escrig et al., 2001). This assay has been applied to different processed food, such as processed grain foods (Minamiyama et al., 1994), storage red raspberry jams (Zafrilla et al., 2001), storage protein from Dioscorea batata (Hou et al., 2001), processed jam from berries (Amakura et al., 2000), processed pomegranate juice (Gil et al., 2000), and aged red wines (Larrauri et al., 1999). In order to make comparison of radical scavenging activity Table 1 shows the antioxidant activity of red wine and green tea measured by different methods. In conclusion, we might say that in view of the diversity of methods, there is a great need to standardize them for measurement of antioxidant activity. The system composition, the oxidable substrate and the method of inducing oxidation, are factors when evaluating an assay. On the other hand, there are different oxidation sources and oxidation types, hence, firstly, we should define oxidation targets (lipids, protein or DNA) before selecting a method to evaluate antioxidant activity. The search for more specific assays that give us chemical information, which could be related directly to oxidative deterioration of foods and biological systems, should be the objective of future research.

ACKNOWLEDGMENTS
The co-operation of Dr. Charles Boone and Dr. Piotr Szut in critical reviewing of the manuscript is gratefully acknowledged.

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