jfbc_396 472..483

PHENOLIC COMPOUNDS, TOCOPHEROLS, CAROTENOIDS ANDVITAMIN C OF COMMERCIAL CAPER

NIZAR TLILI1,2,4, NIZAR NASRI1, ABDELHAMID KHALDI2, SAÏDA TRIKI1

and SERGI MUNNÉ-BOSCH3

1Laboratoire de BiochimieDépartement de Biologie

Faculté des Sciences de TunisUniversité Tunis El-Manar

Tunis 2092, Tunisia

2Unité de Recherche Gestion et Valorisation des Ressources ForestièresINRGREF

BP: 10 Ariana 2080, Tunisia

3Departament de Biologia VegetalFacultat de Biologia

Universitat de BarcelonaAvinguda Diagonal 645, E-08028 Barcelona, Spain

Accepted for Publication June 13, 2009

ABSTRACT

The contents of antioxidant compounds were examined in four commer-cial samples of caper, which is one of the most commonly found aromatics inthe Mediterranean kitchen. Analyses were performed by using the colorimetricassay (total phenolic compounds and vitamin C) and high-performance liquidchromatography (rutin, carotenoids and tocopherols). Moreover, vitamin Aactivity (as retinol equivalents) was calculated. Phenolic compound contentsranged from 1151.6 � 19.8 to 2243.96 � 48.2 mg/100 g FW, while rutin con-tents ranged from 150.62 � 5.18 to 732.61 � 10.49 mg/100 g FW. Total toco-pherol content was from 700.23 � 10.49 to 2555.41 � 71.12 mg/100 FW, witha-tocopherol as the predominant isomer in all samples. b-carotene rangedbetween 84.8 � 9.5 and 805.71 � 17.73 mg/100 g FW. Capers also containedan appreciable amount of vitamin C. These results bring attention to theantioxidant vitamin value and nutritional importance of commercialcaper.

4 Corresponding author. TEL: +216-2122-3008; FAX: +216-7188-5480; EMAIL: nizar.tlili@fst.rnu.tn

DOI: 10.1111/j.1745-4514.2010.00396.x

Journal of Food Biochemistry 35 (2011) 472–483.© 2011 Wiley Periodicals, Inc.

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PRACTICAL APPLICATIONS

Results show that caper contain significant amounts of antioxidants (totalphenolic compounds, rutin, tocopherols, carotenoids; and appreciable levels ofvitamin C) as bioactive compounds. Irrespective of the variation betweencountries, commercial caper contained important contents of these com-pounds, thus showing caper has a great interest for its nutritional value. Thecombined contents of these antioxidants in commercial capers encourageconsumers to increase their intake. Also, these results should be useful forresearchers to explore and develop further this plant and its storage conditionsfor human consumption and medicinal uses.

INTRODUCTION

Currently, many researchers and dietary organizations recommended anincrease of the consumption of fruits and vegetables that contain naturalantioxidant vitamins (vitamins P, E, A and C) (Southon 2000; Moure et al.2001; Bazzano et al. 2002; United States Department of Agriculture, U.S.Department of Health and Human Service 2004). Moreover, many authorshave reported adverse potential health risks and toxicity effects of syntheticantioxidants (Ito et al. 1986; Whysner et al. 1994; Williams et al. 1999).Various factors such as ripening time, genotype, cultivation techniques andclimatic conditions that occur during the preharvest period and postharvesthandling practices can affect the phytochemical substances of plant foods, andthey may have a significant role in determining the phenolic and antioxidantcomposition of these compounds (Rodriguez-Amaya 1993; Lee and Kader2000; Imeh and Khokhar 2002).

Numerous investigations support a relationship between the Mediterra-nean diet and a low incidence of several diseases, such as cardiovasculardiseases and cancer (Bester et al. 2008). Caper, as a perennial shrub plant, isone of the most common aromatic plants found in the Mediterranean Basin.Caper shows strong resistance to hard environmental conditions. Differentparts of this plant can be used as drugs or in cosmetics. Spain and Moroccowere the main producer countries (Özcan and Akgül 1998). The fresh aerialparts, especially the flower buds, are stored in salt, vinegar or brine, and usedas an appetizer with olives, cheese and nuts, or as a complement to meat,salads, pasta and other foods. Previous studies on caper have brought attentionto the antioxidant activity and nutritional value of fresh buds (Germano et al.2002; Tlili et al. 2009). Chemical studies have reported the presence of alka-loids and glucosinolates (Brevard et al. 1992), which are naturally occurringproducts belonging to cancer-preventing agents (Mikkelsen et al. 2000).

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Moreover, it was reported that Capparis spinosa possesses some anti-inflammatory metabolites (Al-Said et al. 1988).

Phenolic compounds may have beneficial effects on human health(Kuntic et al. 1998; Daniel et al. 1999). Rutin, as vitamin P, is one of the mostcommonly found flavonoids in fresh aerial parts of caper (Germano et al.2002), and it has an antioxidative, anti-inflammatory and anticarcinogeniceffect (Ihme et al. 1996). Tocopherols are known as vitamin E and represent animportant class of antioxidants. Burton et al. (1983) reported that vitamin E isan important antioxidant nutrient that can protect cell membranes from oxi-dative damage. Carotenoids are an abundant group of lipid antioxidants.b-carotene is the source of vitamin A, and several studies have linked diets richin this compound with a reduced risk of several chronic and degenerativediseases (Sommer and Davidson 2002; Mozaffarieh et al. 2003). Vitamin Cplays significant roles in the human organism, such as cell defense against freeradicals, conjunctive tissue formation and ion transportation (Barata-Soareset al. 2004). Nearly 90% of vitamin C in the human diet is obtained from fruitsand vegetables as ascorbic and dehydroascorbic acids (Zee et al. 1991).

The aim of this work was to evaluate some antioxidant components (totalphenolic compounds, vitamin P, vitamin E, vitamin C and provitamin A) fromcommercial capers from different countries, to provide information on func-tional food for commercial practices.

MATERIALS AND METHODS

Reagents

Standards: a-tocopherol, g-tocopherol, b-tocopherol, d-tocopherol, rutin,Folin–Ciocalteu reagent, Na2CO3, ascorbate, ferric chloride (FeCl3) and thesolvents (methanol, acetone and hexane) were purchased from Sigma-AldrichChemical Co. (Steinheim, Germany); b-carotene, dithiothreitol (DTT),N-ethylmaleimide (NEM), bipyridyl and trichloroacetic acid (TCA) wereobtained from Fluka Chemical (Buchs, Switzerland).

Samples

Tunisian and Morocco samples were purchased from the Tunisian super-markets (central market). Samples from Spain and Turkey were purchasedfrom local supermarkets in Barcelona (CONDIS and El Corte Ingles,respectively).

Determination of Total Phenolic Content

Phenolic compounds were determined according to the method describedby Germano et al. (2002). In brief, samples were ground to a fine powder in a

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mortar under liquid nitrogen and repeatedly extracted with 100% methanol,using sonication, until the extract was colorless. The resulting extracts werepooled, and an aliquot of the resulting methanolic extract (0.1 mL) was mixedwith 0.2 mL of Folin–Ciocalteu reagent, 2 mL of H2O and 1 mL of 15%Na2CO3, and the absorbance was measured at 765 nm after 2 h incubation atroom temperature. Rutin was used as the standard for the calibration curve,with concentrations ranging between 0 and 1 mg/mL. The total phenolics wereexpressed as milligram of rutin equivalents per 100 g of sample.

Analysis of Rutin Using High-Performance Liquid Chromatography

Rutin content in the methanolic extract was determined by high-performance liquid chromatography (HPLC), using a Hypersil ODS column(Teknokroma, St. Cugat, Spain) and isocratic elution of methanol/acetic acid1% (43:57, v/v) at room temperature at a flow rate of 1 mL/min. Injectionvolume was 5 mL. Rutin was identified by its retention time (6.8 min) and UVspectrum, which was compared with that of an authentic standard. Detectionwas carried out at 355 nm (diode array detector 1000S, Applied Biosystems,Foster City, CA).

Determination of Vitamin C Content

Content of vitamin C was determined according to the method reportedby Kampfenkel et al. (1995) with some modification. Samples were ground ina mortar (placed on ice) under liquid nitrogen. We added 1 mL of TCA 6% andleft it for 15 min in the ice after sonication for 10 min. Then, we took thesupernatant after spin of 10 min at 4C. Extraction was repeated three times,and the supernatant was adjusted to 10 mL with TCA 6%. To an aliquot of0.2 mL of the extract, we added 0.2 mL DTT, 0.4 mL phosphate buffer (5.44 gacid in 200 mL water with 6.968 g base in 200 mL water mixed up to pH 7.4),0.2 mL NEM (5%), 1 mL TCA (10%), 0.8 mL H3PO4 (42%), 0.8 mL bipyridyl4% (4 g 2,2′-bipiridyl in 100 mL 70% methanol) and 0.4 mL FeCl3 (3%). Thereagents were added in this order and mixed vigorously (strong vortex) imme-diately after adding the FeCl3. Ascorbate was used as the standard for thecalibration curve, with the concentration ranging from 0 to 200 mg/mL. Beforereading the absorbance at 525 nm, the reaction mixture was incubated at 42Cfor 40 min. The absorbance was read using a UV-160A Visible RecordingSpectrophotometer (Shimadzu Scientific Instruments, Columbia, MD).

Analysis of Tocopherols Using HPLC

For tocopherol analysis, an aliquot of the methanolic extract was used.Tocopherols were separated on a Partisil 10 ODS-3 column (250 ¥ 4.6 mm;

475ANTIOXIDANT IN COMMERCIAL CAPER

Scharlau, Barcelona, Spain) at room temperature at a flow rate of 1 mL/min.The solvents consisted of (1) methanol/water (95:5, v/v) and (2) methanol. Thegradient used was: 0–10 min 100% A, 10–15 min decreasing to 0% A,15–20 min 0% A, 20–23 min increasing to 100% A and 23–28 min 100% A.Detection was carried out at 292 nm (diode array detector 1000S, AppliedBiosystems). Tocopherol isomers were identified and quantified by their char-acteristic spectra and by coelution with authentic standards.

Analysis of Carotenoids Using HPLC

Extraction and HPLC analyses of carotenoids were performed asdescribed by Munné-Bosch and Alegre (2003). Samples were repeatedlyextracted with ice-cold 85% (v/v) and 100% acetone using sonication, until theextract was colorless. Carotenoids were separated on a Dupont non-endcappedZorbax ODS-5 mm column (250 ¥ 4.6 mm, 20% C; Scharlau) at 30C at a flowrate of 1 mL/min. The solvents consisted of (1) acetonitrile/methanol (85:15,v/v) and (2) methanol/ethyl acetate (68:32, v/v). The gradient used was:0–14 min 100% A, 14–16 min decreasing to 0% A, 16–28 min 0% A,28–30 min increasing to 100% A and 30–38 min 100% A. Detection wascarried out at 445 nm (diode array detector 1000S; Applied Biosystems).Compounds were identified by their characteristic spectra and by coelutionwith authentic standards.

Calculation of Vitamin A Activity

The vitamin A activity, as retinol equivalents (RE), was calculated basedon the in vivo conversion factor proposed by the World Health Organization(WHO) and the National Research Council (NRC), where 1 RE corresponds to6 mg of b-carotene and 12 mg of a-carotene (WHO 1982; NRC 1989, ch. 7).

Statistical Analysis

The experimental data were analyzed using the analysis of variance usingthe Statistical Analysis System (XLSTAT 2008, Addinsoft, New York, NY).Differences at P � 0.05 were considered statistically significant by Duncan’snew multiple range test. All values were expressed as means � standard devia-tion on at least triplicate samples.

RESULTS AND DISCUSSION

Content of Phenolic Compounds and Rutin

The contents of phenolic compounds and rutin in commercial caperanalyzed in this study are given in Table 1. Results show that commercial

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caper is an excellent source of these compounds. The highest content ofphenolic compounds, as determined by the Folin–Ciocalteu reagent, wasdetected in Tunisian caper with 2,243.96 � 48.2 mg/100 g FW, whereas thelowest value was in Spanish caper with 1,151.6 � 19.8 mg/100 g FW. Tuni-sian caper also showed the highest value of rutin (732.61 � 10.49 mg/100 gFW), while caper from Morocco, Turkey and Spain showed values rangingbetween 150.62 � 5.18 and 223.82 � 13.36 mg/100 g FW. Because severalworks have shown that phenolic compounds are relatively stable with respectto various modes of processing (Makris and Rossiter 2002; Kalt 2005), dif-ferences between countries may be related to variability within the samespecies in different locations.

Phenolic compounds may have beneficial effects on human health. More-over, rutin that belongs to the group of flavonoids displays a remarkable arrayof biological and pharmacological activities. Irrespective of the variationbetween countries, commercial caper contained very high contents of phenoliccompounds, thus showing a great interest in the nutritional value of caper.

Vitamin C Content

The level of vitamin C (Table 2) was much lower, ranging between0.4 � 0.03 mg/100 g FW in caper from Morocco and 0.44 � 0.02 mg/100 gFW in Tunisian caper. These values were probably associated not only with theoriginal concentrations in the different samples but also with the storageconditions. Zee et al. (1991) reported that this compound is sensitive to lightand oxygen, and may decompose under normal transport and storage condi-tions, resulting in a reduction of the nutritional value of the foodstuffs. VitaminC plays significant roles, such as in ion transportation, conjunctive tissueformation and cell defense against free radicals (Barata-Soares et al. 2004).

TABLE 1.CONTENTS OF PHENOLIC COMPOUNDS AND RUTIN

(mg/100 g FW) OF COMMERCIAL CAPER FROM DIFFERENTCOUNTRIES

Samples Phenolic compounds Rutin

Tunisia 2,243.96 � 48.2* 732.61 � 10.49*Morocco 1,930.29 � 23.15 150.62 � 5.18Turkey 1,306.77 � 20.2 223.82 � 13.36Spain 1,151.6 � 19.8 164.9 � 4.94Mean 1,658.07 � 477.2 318.02 � 257.58

Values are mean of three repetitions � standard deviation.* Values are significantly higher than the mean at P � 0.05.

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Tocopherol Content

Variations in tocopherol levels are shown in Table 3. The tocopherol poolin commercial caper was distinguished by the content of both a- andg-tocopherols. Total tocopherols ranged between 700.23 � 10.49 mg/100 gFW (Morocco) and 2,555.41 � 71.12 mg/100 g FW (Spain). The mainisomer was a-tocopherol with more than 59%, with a difference betweensamples from 413.52 � 5.06 mg/100 g FW in caper from Morocco to1,925.99 � 47.55 mg/100 g FW in Spanish caper. g-Tocopherol was presentwith less than 40.95%; the highest amount was found in Spanish caper with629.42 � 37.7 mg/100 g FW, whereas the amounts in the samples fromTurkey, Morocco and Tunisia were 363.59 � 11.43, 286.71 � 14.54 and286.20 � 6.57 mg/100 g FW, respectively. These differences were probablybecause of cultivars and storage conditions, as cited by other authors(Rodriguez-Amaya 1993; Kim et al. 2007). Recently, vitamin E has attractedmuch attention. It has been widely studied for its antiaging, anticancer andanti-atherosclerosis effects (Brigelius-Flohé and Traber 1999). In addition,g-tocopherol receives, nowadays, a big attention because of its potent cancer

TABLE 2.CONTENT OF VITAMIN C (mg/100 g FW) OF COMMERCIAL

CAPER FROM DIFFERENT COUNTRIES

Samples Vitamin C

Tunisia 0.44 � 0.02Morocco 0.4 � 0.03Turkey 0.43 � 0.01Spain 0.42 � 0.01Mean 0.42 � 0.02

Values are mean of three repetitions � standard deviation.

TABLE 3.VITAMIN E CONTENT (mg/100 g FW) AND PERCENTAGE OF DIFFERENT ISOMERS IN

DIFFERENT COMMERCIAL BUDS

Samples a-tocopherol % g-tocopherol % Total tocopherols

Tunisia 467.77 � 24.64 62.05 286.20 � 6.57 37.95 753.98 � 29.14Morocco 413.52 � 5.06 59.06 286.71 � 14.54 40.94 700.23 � 10.49Turkey 887.62 � 82.02 70.94 363.59 � 11.43 29.06 1,251.21 � 81.36Spain 1,925.99 � 47.55* 75.36 629.42 � 37.7* 24.64 2,555.41 � 71.12*Mean 923.35 � 649.36 391.35 � 150.92 1,314.98 � 799.29

Values are mean of three repetitions � standard deviation.* Values are significantly higher than the mean at P � 0.05.

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chemopreventive properties and its important role in cardiovascular disease(Hensley et al. 2004). The predominant isomer consumed in Mediterraneancountries is probably a-tocopherol present in olive oil that is one of the typicalMediterranean diets (Psomiadon et al. 2000). With the combined content of a-and g-tocopherol, caper can also be considered as an interesting natural sourceof these compounds. Moreover, Table 4 shows that levels of tocopherolisomers were mostly higher than those in other fermented vegetables (cubedradish, Chinese cabbage, radish leaf and cucumber), as reported previously(Kim et al. 2007).

Carotenoids Content

The level of lutein, b-carotene and total carotenoids are presented inTable 5. Results show that, only in Tunisian caper, both b-carotene(84.8 � 9.5 mg/100 g FW) and lutein (202.1 � 16.52 mg/100 g) weredetected. Whereas in the other samples, only b-carotene was detected, with thehighest amount found in caper from Morocco (805.71 � 17.73 mg/100 g FW)and the lowest in caper from Turkey (307.94 � 18.29 mg/100 g FW). Thesedifferences might be, however, related to cultivar differences or differingharvesting techniques, which is in agreement with previous studies(Rodriguez-Amaya 1993; Kim et al. 2007). Carotenoids play an important rolein human nutrition. Lutein has been reported to play a significant role in thehealth of eyes. b-carotene has been reported as provitamin A (Sommer and

TABLE 4.CAROTENOID (mg/100 g FW) AND TOCOPHEROL (mg/100 g

FW) CONTENTS IN COMMERCIAL CAPER FROMDIFFERENT COUNTRIES (THIS STUDY) AND SOME

FERMENTED VEGETABLES (KIM ET AL. 2007)

Samples Carotenoids Tocopherols

b-carotene Lutein a g

Cubed radish* 47.4 7.1 0.19 nmChinese cabbage* 155.4 216.1 0.28 0.1Radish leaf* 530.4 984.4 0.51 0.23Cucumber* 883.2 1408.2 0.27 0.18Tunisian caper† 84.8 202.1 0.46 0.28Morocco caper† 805.7 nd 0.41 0.28Turkish caper† 307.9 nd 0.88 0.36Spanish caper† 406.4 nd 1.92 0.62

* Values published by Kim et al. 2007.† Values from this study.nm, not mentioned; nd, not detected.

479ANTIOXIDANT IN COMMERCIAL CAPER

Davidson 2002; Mozaffarieh et al. 2003). The high amount of carotenoids incommercial caper attests its nutritional value.

In Table 4, we reported a comparison between our results and publishedvalues of Kim et al. (2007) for some fermented vegetables. The highest levelof lutein was in cucumber (1,408.2 mg/100 g). The value in caper from Tunisia(216.1 mg/100 g) was higher than in cubed radish (7.1 mg/100 g). The contentof b-carotene was between 47.4 mg/100 g (cubed radish) and 883.2 mg/100 g(cucumber).

Vitamin A Activity

Vitamin A activity of commercial caper is presented in Table 5. Resultsshow that RE was ranging from 14.13 RE (Tunisian caper) to 134.28 RE(Morocco). Total vitamin A activity was statistically different in capers fromdifferent countries, which was probably because of the variety of concentra-tions in the samples and probably to the storage conditions.

Results show that commercial caper contains important quantities of totalphenolic compounds, rutin (as vitamin P), tocopherols (as vitamin E), caro-tenoids (as pro-vitamin A) and appreciable levels of vitamin C, as bioactivecompounds. The combined contents of these antioxidants in capers encourageconsumers to increase the intake of caper. Also, these results should be usefulfor researchers to explore and develop further this plant and its storage forhuman consumption and medicinal uses.

ACKNOWLEDGMENTS

We are very grateful to the Serveis Cientıfico-Tecnics (University ofBarcelona) for technical assistance. This research was supported by the AECI(project no. A/016255/08).

TABLE 5.b-CAROTENE, LUTEIN, TOTAL CAROTENOIDS (mg/100 g FW) AND VITAMIN A ACTIVITY

IN COMMERCIAL CAPER

Samples Total carotenoids Lutein b-carotene a-carotene Vitamin A activity

Tunisia 286.9 � 16.98 202.1 � 16.52 84.8 � 9.5 nd 14.13†Morocco 805.71 � 17.73* nd 805.71 � 17.73* nd 134.28Turkey 307.94 � 18.29 nd 307.94 � 18.29 nd 51.32Spain 406.49 � 17.07 nd 406.49 � 17.07 nd 67.74Mean 451.13 � 223.52 50.26 � 93.07 400.73 � 278.53

Values are mean of three repetitions � SD.* Values are significantly higher than the mean at P � 0.05.† 1 retinol equivalent = 6 mg b-carotene or 12 mg a-carotene.nd, not detected.

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