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Journal of Agricultural and Food Chemistry is published by the American ChemicalSociety. 1155 Sixteenth Street N.W., Washington, DC 20036

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Total Antioxidant Capacity of FruitsHong Wang, Guohua Cao, and Ronald L. Prior

J. Agric. Food Chem., 1996, 44 (3), 701-705 DOI: 10.1021/jf950579y Publication Date (Web): 19 March 1996

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chased from Wako Chemicals USA In c. (Richmond, VA).6-Hydroxy-2,5,7,8-tetramethyl-2-carboxylic acid (Trolox) wasobtained from Aldrich (Milwauk ee, WI). Acetone was fromSigma or Aldrich.

S a m p l e P r e p a r a t i o n . All of the fruits except white andred grapes, strawberries, plums, and tomatoes were peeled.The edible portion of the fruit was weighed and then homog-enized by using a blender after deionized water was added(1:2 w/v). The homogenat e was centr ifuged at 4500g for 15min (4 C). The supern ata nt (juice fraction) was r ecoveredand used directly for the ORAC assay after suitable dilutionwith ph osphate buffer (75 mM, pH 7.0). The pulp (insolublefraction) was furt her extracted by u sing pur e acetone (1:7 w/v)with sha king a t r oom te m pe r a tur e f or 30 m in. Ace tone ha sbeen used by other investigators t o extract ant ioxidants fromfruit pu lp (Daniel et al., 1989; Mass et al., 1991). Acetone itselfhas only a very small effect on the ORAC assay (Cao et al. ,1995). The acetone extract was recovered after centr ifugat ion(4500g, 15 min, 4 C), and the sample was used for the ORACassay after suitable dilution with phosphate buffer. The drymat ter of fruit wa s determined by weighing th e water lost afterdrying at 40 C for 1 week.

A u t o m a t e d O R AC A s s a y . The a ut om a te d OR AC a ssa ywas carried out on th e COBAS F ARA II centrifugal a nalyzer(R oche Dia gnostic S yste m I nc. , B r a nc hbur g, NJ) with afluorescence att achment; fluorescent filters were set to passthe l ight with a n e xc ita tion wa ve le ngth of 540 nm a nd a nemission wavelength of 565 nm. The procedur e was based ona pr e vious pa pe r of C a o e t a l . ( 1993), a s m odified for theCOBAS FARA II (Cao et al., 1995). Briefly, in the final a ssaymixtur e (0.4 mL t otal volum e), -PE (1.67 10-8 M) was u sedas a target of free radical damage, AAPH (4 mM) as a peroxylr a dica l ge ne r a tor , a nd Tr olox a s a contr ol sta nda r d. Theanalyzer was programmed t o record the fluorescence every 2min after AAPH addition. Fina l result s were calculat ed usingthe differences of areas under the quenching curves of -P Ebe twe e n a bla nk a nd a sa m ple a nd a r e e xpr e sse d a s m ic r o-moles of Trolox equivalents per gram or m illiliter. The ORACactivity of a fruit was calculated by adding the ORAC activityfrom the juice fraction and the pulp fraction extracted withacetone.

Statistical Analysis. The effect of acetone extraction timeon the ORAC activity of a fruit pulp was analyzed by analysisof var iance (ANOVA) usin g SYSTAT (SYSTAT, Inc., Evan ston ,IL). Pairwise mu ltiple comparisons were evaluated by Tuk eyssignifican t difference (HSD) test used in SYSTAT. Differen cesa t P < 0.05 were considered significant.

RESULTS

The ORAC activity of a fruit (edible portion) wascalculated by a dding th e ORAC activity from its juicefraction and its pulp fraction extracted with acetone.Thirty minu tes of extra ction with acetone was found tobe sufficient to extra ct the a nt ioxidants contain ed in th epulp of a f r ui t ( str awber r y, or ange, and whi te gr apewere tested in t his stu dy; Table 1). The ORAC activitiesm e a s u r ed i n t h e p u lp of s t r a w b er r i es a n d or a n g esfollowing 2 min of acetone extra ction a t room temper-atur e wer e significantly (P < 0.05) l ower than thosemeasur ed after 30 min of acetone extra ction. However,the ORAC activities measu red in t he pu lp of strawber-ries a nd ora nges following 30 min of acetone extr action

were not significant ly differen t from those mea sur ed byusing a 1 or 4 h a cetone extraction. The ORAC activitymeasured in the pulp of white grapes following 2 minof acetone extraction was not significantly different fromthat measured following 30 min or 1 or 4 h of acetoneextraction (Table 1).

The ORAC activities of 12 fruits are shown in Table2. The ORAC assays of these fr uits wer e car r i ed outon three independent occasions using fruit purchasedon thr ee separa te occasions. The results are presenteda s m e a n ( SE. On th e basis of the wet weight of fruit(edible por tion) , str awber r y had the highest ORAC

activity, followed by plum , orange, r ed gra pe, kiwi fruit,pink gr apef r uit , white gr ape, banana, apple, tomato,pear, an d melon. On th e basis of the dr y weight of fruit,str awberr y also had th e highest ORAC activity followedby plum, orange, pink gra pefruit, tomato, kiwi fru it, redgrape, white grape, apple, honeydew melon, pear, andbanana . I n m ost f r uits, the contr ibution of t he f r ui tpulp fraction (extra cted with a cetone) to the t otal ORACactivity of a fruit was usually less than 10%.

The ORAC activities of five commercial fruit juicesar e shown in Figur e 1. Among the commer cial f r ui t

ju ices tes t ed , gr a pe ju ice ha d th e h igh es t ORAC a cti vit y,followed by grap efruit juice, toma to juice, ora nge juice,an d apple juice. The calculat ed contr ibution of vitam inC t o the total ORAC activity of those commercial fruit

T a b l e 1 . E f fe c t o f A c e t o n e E x t r a c t i o n T i m e o n O R A C

( N a n o m o l e s o f T r o l o x E q u i v a l e n t s p e r G r a m ) M e a s u r e di n F r u i t P u l p

st rawberrya white grapea orangea

2 m in 847 ( 29 (3) 248 ( 22 (3) 3556 ( 154 (3)30 m in 1264 ( 32 (3)* 306 ( 32 (3) 6041 ( 63 (3)*1 h 1116 ( 21 (3)* 340 ( 11 (3) 5782 ( 147 (3)*4 h 1129 ( 113 (3) 398 ( 80 (3) 5572 ( 182 (3)*

a The dat a are present ed as mean ( SE (n ). * denotes P < 0.05using ANOVA in comparison with 2 min extraction.

T a b l e 2 . O R AC o f S e l e c t e d F r u i t s U s i n g A AP H a s a

P e r o x y l R a d i c a l G e n e r a to ra

total ORAC

item

dr ym a t t e r

(%) a s is ba sisb DM basisc

ju iceextractORACb

st r a wber r y 10.0 15.36 ( 2 .3 8 1 53 .6 ( 7 .5 1 2.4 4plu m 12.0 9.49 ( 0.67 79.1 ( 1.9 8.35or a n ge 14.5 7.50 ( 1.01 51.7 ( 2.7 6.82gr a pe, r ed 20.5 7.39 ( 0.48 36.0 ( 1.1 3.99kiwi fr u it 16.5 6.02 ( 0.52 36.5 ( 1.3 5.54gr a pe fr u it , p in k 1 0.0 4.83 ( 0.18 48.3 ( 0.6 4.54

gr a pe, whit e 17.0 4.46 ( 1.06 26.2 ( 2.6 2.89ba n a na 24.5 2.21 ( 0.19 9.0 ( 0.4 2.10a pple 16.5 2.18 ( 0.35 13.2 ( 0.9 1.92t om a t o 5.0 1.89 ( 0.12 37.8 ( 0.5 1.57pea r 14.0 1.34 ( 0.06 9.6 ( 0.2 1.23m elon 7.5 0.97 ( 0.15 12.9 ( 0.5 0.88

a Dat a expressed as means ( SEM of three samples purchasedand analyzed independently. b Data expressed as micromoles ofTrolox equivalents per gram of fruit (as is basis). c Data expressedas micromoles of Trolox equivalents per gram of dry matt er (DM)(DM basis).

F i g u r e 1 . ORAC (micromoles of Trolox equivalent per mil-liliter) of common commer cial fruit juices. Th e ORAC contrib-ute d by vita m in C in a c om m e r c ia l juic e wa s ba se d on theORAC activity of vitamin C (Cao et al., 1993) and the contentof vitamin C obtained from t he commercial juice label. No datawe r e a va ila ble f or a pple juice . Vita m in C in tom a to juice

account ed for 0.02 mol of Trolox equivalent/mL.

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ju ices wa s less t h a n 30 %. Da t a on vit a m in C con t en tof the commercial juices were from their labels exceptfor apple juice, which h ad n o such da tum . The ORACactivity of 1.0 mol of vitamin C is 0.52 mol of Tr oloxequiv (Cao et al., 1993).

DISCUSSION

Reactive oxygen species (ROS) are constantly gener-ated in vivo, both by accidents of chemistry and for

specific purposes. To countera ct ROS and t o preventtheir possible damage to biological molecules, especiallyt o DNA, l ipi ds and pr oteins, al l oxygen-consumingorganisms are endowed with well-integrated an tioxidantsyst ems, whi ch include enzymes such as super oxidedismuta se, cat alase, and glutat hione per oxidase, an dmacromolecules, such as albumin, ceruloplasmin, andfe r r it i n , a n d a n a r r a y of s m a l l m ol ecu l es , s u c h a sascorbic acid, R-tocopherol, -car otene, a nd r educedglutathione.

There ar e ma ny different ant ioxidant components inanimal and plant tissues, and it is relatively difficultt o measur e each antioxidant component separ ately.Therefore, several methods (Cao et al., 1993; Glazer,1990; Miller et al., 1993; Wayner et al., 1985; Whitehead

et al . , 1992) have been developed in r ecent year s toevaluate t he total ant ioxidant capacity of biol ogicalsam ples. In th ese methods, the inhibition of free radicalaction by an an tioxidant conta ins two components: theinhibition time and the inh ibition degree. We used theORAC ass ay system becau se it combines both inhibitiontime and inhibition degree into a single quantity (Caoet a l ., 1993, 1995). Al l other met hods use eit her thei n h ib it i on t i m e a t a fi xe d i n h ib it i on d e gr e e or t h ei n h ib it i on d e gr e e a t a fi xe d t i m e a s t h e b a s is forquant itating t he r esults.

Fru its are good sources of an tioxidant s. Considera bleattention ha s been focused on the vitamin C, vit aminE, and -carotene cont ent of fruits. However, fruits a lsocontain many other substances that have antioxidantactivit ies. By usi ng the ORAC assay, we ha ve mea-sured, for the first time, the total antioxidant capacityof some common fruits. On th e basis of the da ta fromUSDA han dbooks (USDA, 1986) th e vitam in C cont entsof kiwi fruit, str awberry, orange, gra pefruit, honeydewmelon, and tomato ar e 5.0, 2.9, 2.7, 1.8, 1.3, a nd 0.9mol/g (wet wt), resp ectively. The other fru its includingplum, r ed gr ape, white gr ape, banana, a pple, and pearcontain less than 0.49 mol of vitamin C/g (wet wt). TheORAC activity of 1.0 mol of vitamin C is 0.52 mol ofTr olox equiv (Cao et al ., 1993). Ther efor e, i t wascalculat ed tha t th e contribution of vitamin C to the t otalORAC a ctivi ty of a f r uit was usually less t han 15%except for kiwi fruit a nd h oneydew melon. This sug-

gests that the major source of antioxidant capacity ofmost fruits a nd commercial fru it juices ma y be not fromvitamin C.

W e d i d n o t m e a s u r e t h e v i t a m i n C c o n t e n t o f t h efruits directly but used vitamin C data from the USDAhandbooks (USDA, 1986), realizing that this may in-troduce some added variability in the estima te. How-ever, since the estimated contribution of vitamin C tot h e t ot a l O RAC a ct i vi t y i s r e la t i ve ly l ow , w e fe elconfident in concluding th at th is cont ribution is low an dthat other antioxidants in fruits should be consideredas significan t contr ibutors t o the total ORAC activity.The vitamin C values conta ined in th e USDA handbookgener ally wil l r epr esent a diver se sam pling, and thusone would not expect severalfold fluctuations in the

amount of vitamin C concentr a tion in th e f ood. Theob je ct i ve of t h i s s t u d y w a s t o d e t er m i n e t h e t ot a lant ioxidan t capacity (ORAC a ctivity) of fruits and notthe contr ibution of any individual anti oxidant to t hetotal antioxidant capacity. Our da ta in f act indicat ethat some un known a ntioxidants may need to be identi-fied in these fruits.

The total antioxidant capacity var ies consider abl yfrom one kind of fruit t o another. For example, on th eb a sis of t h e w et w eig h t of a fr e sh fr u it , t h e t ot a l

a n t i ox id a n t ca p a ci t y o f s t r a w b er r y w a s 2 t i m es t h ecapacity measured in oran ges or r ed grapes, 7 times thecapacity measur ed in apple and banana, 11 t i mes t hecapacity measured in pears, and 16 times the capacitymeasur ed in honeydew melon. The ant ioxidant capaci-ties of the five commercial fruit juices were not alwayssimilar to those measu red in respective fresh fruits u sedin this stu dy. The commercial grape juice and t omato

ju ice h a d m u ch h igh er ORAC t h a n t h e fr es h r ed gr a pe sand the fr esh tomatoes, while the commer cial or ange

ju ice h a d m u ch lowe r OR AC t h a n t h e fr es h or a n ges.However, the commercial grape juice was made fromConcord grapes which have a dark color and thick skinand which are different from the red gr apes t ested inthis st udy. Red wine h ad a n ORAC activity of 12.34 (0.47 mmol/L (Cao et al., 1995), which is similar to thatmeasu red in grape juice. The varieties of tomatoes andoranges u sed in the commercial juices could a lso havebeen very different from t he fresh tomat oes an d oranges.I n addition, we do not know whether vitami n C wasadded into these commer cial fr uit juices. However ,other commercial processing factors, such as the pro-cedures used for juice preparation (diluting and con-centr ating) and storage, can not be excluded in explain-ing the observed difference.

Par t of the antioxidant capacity of these f r ui t s ma ybe fr om flavonoids. Flavonoids ar e low molecul arweight polyphenolic compound s t ha t a re widely distrib-u t e d i n v eg et a b le s a n d fr u i t s (H e r t og e t a l ., 1 99 2;

Ortun o et al., 1995). Many flavonoids, such as kaem -pherol, quercetin, luteolin, myricetin, eridictyol, andcatechin, h ave been shown to ha ve an t i oxidant (Bor sa n d S a r a n , 1 98 7; B or s e t a l ., 1 9 9 0; H a n a s a k i e t a l .,1994), a nti-inflamm atory, a ntiallergic, ant ican cer, andant ihemorrhagic properties (Das, 1994). Hertog et al.(1992) measured the flavonoid conten t (including k aem-pherol, quercetin, luteolin, and myricetin) of importantfruits, vegetables, an d beverages in the Dut ch diet andr elated t he baseline inta ke of dietar y flavonoids t osubsequent cor onar y hear t disease mor tali t y and t heincidence of myocardial infarction in t he Zutphen Eld-erly Study du ring a 5-year followup per iod. They foun dth at flavonoid inta ke was significan tly inversely related

to mortality from coronary h eart disease an d of border-line significan ce (P < 0.08 for trend) with the incidenceof a first fat al or nonfata l myocar dial infarction (Hertoget al., 1993). This furt her suggests tha t other an tioxi-dants besides vitamins E and C and -carotene a re a lsoresponsible for the protection provided by fruits a ndvegetables against various diseases.

The antioxidant defense system of the body is com-posed of different an tioxidant component s. The supple-ment ation of one or a few ant ioxidants m ay not be veryeffective. Fru its contain a group of na tu ral an tioxidant stha t could ha ve not only a high a ntioxidant activity butalso a good combina tion or mixtu re of an tioxidan ts. F orexample, 1 lb of fresh str awberries (454 g) ha s a n ORACactivity (6973 mol of Trolox equiv) equal to about 1.7

Total Antioxidant Capacity of Fruits J. Agric. Food Chem., Vol. 44, No. 3, 1996 703

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g of Trolox, 3.0 g ofR-tocopher ol (the ORAC a ctivity of1 mol ofR-tocopherol ) 1 mol of Trolox equiv; Cao etal., 1993) or 2.3 g of vitamin C (the ORAC activity of 1mol of vitamin C ) 0.52 mol of Trolox equ iv; Cao etal., 1993). A high int ake of vitamin C may a ct in somes it u a t i on s a s a p r o-ox id a n t i n t h e b od y w h en fr e et r a n s it ion m e ta ls a r e a va ila b le a t t h e s a m e t im e .Ther efor e, the supplementation of these na tur al anti-oxidants thr ough a balanced diet containing enoughfruits could be mu ch more effective and also economical

tha n th e supplementat ion of an individual antioxidant,such as vitamin C or vitamin E, in protecting the bodyagainst oxidative dama ge un der different conditions.

I n summar y, the total an t ioxidant act ivit ies of 12fruits and 5 commercial fruit juices were measured byusing an au tomated ORAC assa y with a peroxyl radicalg en e r a t or . O n t h e b a s is of t h e w et w ei gh t of fr u i t s(edible por ti on) , str awber r y had t he highest ORACactivity followed by plum, ora nge, red gr ape, kiwi fruit,pink gr apef r uit , white gr ape, banana, apple, t omato,p e a r , a n d h o n e yd e w m e lon . O n t h e b a s is of t h e d r yweight of fruits, st rawberry a lso had t he h ighest ORACactivity followed by plum, or ange, pink gr apefr uit ,t om a t o, k i wi fr u i t , r e d g r a p e, w h it e g r a p e, a p p le ,honeydew melon, pear , and banana . Among the com-

mercial fruit and vegetable juices, grape juice had thehighest antioxidant activity, followed by tomato juice,orange juice, a nd apple juice.

ABBREVIATIONS USED

AAPH, 2,2-azobis(2-am idinopropan e) dihydr ochlo-ride; ORAC, oxygen radical absorbance capacity; -PE,-phycoerythr in; ROS, r eactive oxygen s pecies; Trolox,6-hydroxy-2,5,7,8-tetra met hyl-2-carboxylic acid.

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Received for review August 23, 1995. Revised man uscriptreceived December 4, 1995. Accepted December 18, 1995.X

M ention of a tr a de na m e , pr opr ieta r y pr oduct, or spe cifice qu i pm e n t d oe s n ot con s t it u t e a g u a r a n t ee b y t h e U .S .Department of Agricultur e and does not imply its approval tothe exclusion of other products that may be suitable.

JF950579Y

X Abstract published in Advance ACS Abstracts, Feb-r uar y 1, 1996.

Total Antioxidant Capacity of Fruits J. Agric. Food Chem., Vol. 44, No. 3, 1996 705