Food Chemistry 134 (2012) 19261931

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Food Chemistry
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Strawberries from integrated pest management and organic farming: Phenolic composition and antioxidant properties
Virgnia C. Fernandes a,b, Valentina F. Domingues b, Victor de Freitas a, Cristina Delerue-Matos b, Nuno Mateus a,
a b

CIQ-Centro de Investigao em Qumica, Departamento de Qumica e Bioqumica, Faculdade de Cincias, Universidade do Porto, Rua do Campo Alegre 687, 4169-007 Porto, Portugal REQUIMTE, Instituto Superior de Engenharia do Porto, Rua Dr Antnio Bernardino de Almeida 431, 4200-072 Porto, Portugal

a r t i c l e

i n f o

a b s t r a c t
Consumer awareness, pesticide and fertilizer contaminations and environmental concerns have resulted in signicant demand for organically grown farm produce. Consumption of berries has become popular among health-conscious consumers due to the high levels of valuable antioxidants, such as anthocyanins and other phenolic compounds. The present study evaluated the inuence that organic farming (OF) and integrated pest management (IPM) practise exert on the total phenolic content in 22 strawberry samples from four varieties. Postharvest performance of OF and IPM strawberries grown in the same area in the centre of Portugal and harvested at the same maturity stage were compared. Chemical proles (phenolic compounds) were determined with the aid of HPLC-DAD/MS. Total phenolic content was higher for OF strawberry extracts. This study showed that the main differences in bioactive phytochemicals between organically and IPM grown strawberries concerned their anthocyanin levels. Organically grown strawberries were signicantly higher in antioxidant activity than were the IPM strawberries, as measured by DPPH and FRAP assays. 2012 Elsevier Ltd. All rights reserved.

Article history: Received 23 February 2012 Received in revised form 22 March 2012 Accepted 27 March 2012 Available online 9 April 2012 Keywords: Strawberries Organic farming Integrated pest management Phenolic content Anthocyanin Antioxidant

1. Introduction Strawberries are a rich source of antioxidants and a common and important fruit in the Mediterranean diet because of their high content of essential nutrients and benecial phytochemicals, which may have relevant biological activity in human health (Giampieri, Tulipani, Alvarez-Suarez, Quiles, Mezzetti, & Battino, 2012). These phytochemicals are essentially avonoids (mainly anthocyanins, with avonols providing a minor contribution), hydrolysable tannins (ellagitannins and gallotannins) phenolic acids (hydroxybenzoic acids and hydroxycinnamic acids), and also condensed tannins (proanthocyanidins) (Cerezo, Cuevas, Winterhalter, Garcia-Parrilla, & Troncoso, 2010). The variety and high content of these compounds make strawberries a very interesting product for studying polyphenols (Kevers, Pincemail, Tabart, Defraigne, & Dommes, 2011). Anthocyanins in strawberries are the major known polyphenolic compounds. Pelargonidin-3-glucoside is the main anthocyanin in strawberries regardless of genetic and environmental factors, and the presence of cyanidin-3-glucoside seems to be constant in strawberries, although only in smaller proportions. Genotypevariety is the major factor in determining fruit nutritional quality, but quality is also affected by crop conditions (environmental and
Corresponding author. Tel.: +351 226082858; fax: +351 226082959.
E-mail address: nbmateus@fc.up.pt (N. Mateus). 0308-8146/$ - see front matter 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2012.03.130

cultivation techniques), ripening season, pre-harvest and postharvest conditions, shelf-life and processing (Giampieri et al., 2012). Inuence of cultivar on phenolic composition (mainly avonols) has been studied previously in onions, pear juices, red raspberry juices, apricot juices and jams, and red wines (Hakkinen & Torronen, 2000). Proponents of organic agriculture often claim that organically produced plant foods promote human health more than those produced using conventional production systems. Others claim the opposite, and many others doubt if there is any difference at all (Amodio, Colelli, Hasey, & Kader, 2007). Previous research has reported that organic fruits and vegetables have higher levels of avonoids and ascorbic acid (Asami, Hong, Barrett, & Mitchell, 2003) than their conventionally produced equivalents. In addition, higher levels of anthocyanins and phenolic compounds, and higher antioxidant capacities were found in some organically cultivated blueberries (You, Wang, Chen, Huang, Wang, & Luo, 2011). Other studies have reported that there is insufcient evidence to draw any valid conclusions, as the scientic research has not proved that organic foods are superior in nutritional quality and safety (Lairon, 2010; Magkos, Arvaniti, & Zampelas, 2003). A recently published scientic status summary by the Institute of Food Technologists (Winter & Davis, 2006) concluded that it is premature to say that either organic or conventional foods are better in terms of safety or nutritional value (Luthria, Singh, Wilson, Vorsa, Banuelos, & Vinyard, 2010).

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In the past 10 years, some review studies of the scientic literature comparing the nutritional quality of organic and conventional foods have been published. Some of those studies (Lairon, 2010; Rembialkowska, 2007) found evidence of organic food being more nutritious, whereas two review articles concluded that there were no consistent nutritional differences between organic and conventional foods (Bourn & Prescott, 2002; Dangour, Dodhia, Hayter, Allen, Lock, & Uauy, 2009). Therefore, additional research comparing organic foods with conventional products is needed to aid in further evaluations (Jin, Wang, Wang, & Zheng, 2011). IPM is an ecological approach to agricultural pest control. Compared with conventional practices of pest control, the big differences are the strict conditions of pesticide use and the biological and mechanical control practices. Although there are some studies that show differences between products produced by organic and conventional farming, there are no studies that show differences between strawberries grown using IPM and OF regimes. In the present study, strawberries grown under IPM and OF were compared in terms of their polyphenolic composition, namely avonoids. Additionally, the antiradical capacity and the reducing power of these samples were assessed using DPPH and FRAP assays, respectively. 2. Materials and methods 2.1. Reagents AAPH, DPPH, FeCl3, Na2CO3, gallic acid and Trolox were purchased from SigmaAldrich (Madrid, Spain); 2,4,6-tripyridyl-striazine (TPTZ) was purchased from Fluka (Madrid, Spain), and FolinCiocalteu reagent was purchased from Merck (Darmstadt, Germany). 2.2. Sampling Each eld pair consisted of two adjacent elds, one organic and one IPM. Fields chosen in each pair had the same microclimate, soil prole, soil type and strawberry variety. Sampling was carried out over 3 years and was performed by the authors. Strawberry samples were collected from OF and IPM elds located in the centre of Portugal. 22 strawberry samples were harvested at commercial ripeness, specically when 75% of the surface was red. Strawberries were harvested on rst week of May in 2009, 2010 and 2011. 1 kg of fruit was randomly sampled and samples were stored at 20 C until analysed. Different varieties of strawberries were collected, including siba, camarosa, festival and san andreas. 2.3. Crude phenolic extracts Phenolic compounds were extracted from 30 g of frozen strawberry samples in 30 mL of ethanol. Each extraction was performed using an Ultra Turrax (Janke & Kunkel, Germany) for 1 min. Homogenates were then centrifuged at 3000 rpm for 10 min (Orto Alresa, Spain). Each extract was concentrated with a rotary evaporator (Heidolph, Germany) at low temperature (37 C) and nally diluted in 50 mL of distiled water. 2.4. Procyanidin extracts A mixture of 20 mL of the aqueous phenolic extract and 10 mL of ethyl acetate was used for a liquidliquid extraction. The organic phase was separated and collected. The procedure was repeated three times. The 30 mL of combined organic phase was concentrated with a rotary evaporator at low temperature (37 C) and nally diluted in 1.5 mL of distiled methanol.

Folin Ciocalteau
120 100

OF IPM

GAE (M g-1 FW)

*
80 60 40 20 0

Crop Type
Fig. 1. Total phenolic content of strawberry extracts from OF and IPM. Columns represent mean standard deviation. Differences between column means are statistically signicant p < 0.05. GAE Gallic acid equivalents.

2.5. Total Phenolic content The total polyphenol content of the extracts was determined following the FolinCiocalteu method adjusted to a microscale (Arnous, Makris, & Kefalas, 2001). In an Eppendorf tube, 610 lL of distiled water, 15 lL of sample extract dissolved in methanol, and 75 lL of FolinCiocalteu reagent were mixed. After 30 s, 300 lL of aqueous 20% Na2CO3 and 300 lL of distiled water were added, and the mixture was mixed (30 s) and allowed to stand at room temperature in the dark for 30 min. The absorbance was read at 750 nm, and the total polyphenol concentration was calculated from a calibration curve, using gallic acid as standard. The results were expressed as gallic acid equivalents (GAE) per gram (g) sample fresh weight (FW). 2.6. HPLC-DAD analysis 2.6.1. Anthocyanin HPLC anthocyanin analysis of the extracts was performed on an Elite Lachrom system (L-2130) equipped with a 250 4.6 mm i.d. reversed phase C18 column (Merck, Darmstadt); detection was

Total anthocyanins
40

IP M

OF
30

IPM

M g-1 FW

20

10

Crop Type
Fig. 2. Average total anthocyanin concentration (lM) in strawberries grown using organic farming and IPM practices. Columns represent mean standard deviation. Differences between column means are statistically signicant p < 0.05.

IP

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500

DAD-520 nm 1a_3

DAD-CH1 520 nm 2A_2

400

Plg-3-Gluc

400

300

300

mAU

200

200

100

Cy-3-Gluc

Plg-3-Rut

100

b a
0

10

15

20

25

30

35

40

45

50

55

60

65

70

Minutes
Fig. 3. General anthocyanin prole of strawberry extract. (a) Organic farming strawberries and (b) Integrated pest management strawberries.

carried out at 520 nm using a diode array detector (L-2455). The solvents were A, H2O/HCOOH (9:1), and B, H2O/CH3CN/HCOOH (6:3:1). The gradient consisted of 20% B for 70 min, 85% B for 5 min, and 100% B for 10 min at a ow rate of 1.0 mL min1. The column was washed with 100% B for 10 min and then stabilized at the initial conditions for another 10 min. Detected peaks were scanned between 200 and 600 nm. Compounds were identied according to retention time and UVvis spectra. 2.6.2. Procyanidin HPLC procyanidin analysis of the extracts was performed on an Elite Lachrom system (L-2130) equipped with a 250 4.6 mm i.d. reversed phase C18 column (Merck, Darmstadt); detection was carried out at 280 nm using a diode array detector (L-2455). The solvents were A, H2O/CH3COOH (7.5:2.5), and B, H2O/CH3CN/ CH3COOH (1.5:8:0.5). The gradient consisted of 7% B for 5 min, 20% B for 85 min, and 100% B for 5 min at a ow rate of 1.0 mL min1. The column was washed with 100% B for 10 min and then stabilized at the initial conditions for another 10 min. Compounds were identied according to retention time and UV vis spectra. 2.7. LC-DAD/ESI-MS analysis A Finnigan Surveyor series liquid chromatograph equipped with a Thermo Finnigan (Hypersil Gold) reversed-phase column (150 mm 4.6 mm, 5 lm, C18) thermostatted at 25 C was used. The samples were analysed using the same solvents, gradients, injection volume, and ow rate referred to above for HPLC analysis. Double online detection was done by a photodiode spectrophotometer and mass spectrometry. The mass detector was a Finnigan LCQ DECA XP MAX (Finnigan Corp., San Jose, CA) quadrupole ion trap equipped with an atmospheric pressure ionisation (API) source, using an electrospray ionisation (ESI) interface. The vaporiser and capillary voltages were 5 kV and 4 V, respectively. The capillary temperature was set at 325 C. Nitrogen was used as both sheath and auxiliary gas at ow rates of 90 and 25,

respectively (in arbitrary units). Spectra were recorded in positive-ion mode between m/z 250 and 1500. 2.8. Ferric reducing/antioxidant power (FRAP) The FRAP assay developed by Benzie & Strain (Benzie & Strain, 1996) was performed with some modications. The reaction was performed in a microplate reader of 96 well plates (Biotek

Table 1 Individual and total anthocyanin contents of 22 strawberry samples. Samples Anthocyanins (lM malv-3-gluc/g FW)a Mean SD Crop type Festival 09 Festival 10 Festival 11 Camarosa 09 Camarosa 10 Camarosa 11 Siba 09 Siba 10 Siba 11 San Andreas 10 San Andreas 11 OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM Cy-3gluc 2.3 0.4 1.8 0.2 2.2 0.5 1.3 0.1 2.4 0.3 1.2 0.3 3.9 0.6 2.4 0.2 4.6 0.9 2.0 0.1 5.4 1.1 4.3 0.8 2.5 0.3 1.1 0.3 3.7 0.4 1.1 0.2 2.5 0.3 1.1 0.2 2.1 0.3 1.6 0.3 1.0 0.2 0.4 0.1 Plg-3gluc 25.2 4.2 20.5 3.2 27.8 4.7 21.7 3.7 13.8 2.8 10.4 1.5 28.8 5.2 13.8 2.5 24.2 4.6 15.2 2.8 23.1 4.2 19.8 3.6 12.5 2.1 10.0 1.7 38.0 6.9 10.0 2.0 13.9 2.6 10.2 1.5 33.3 6.2 15.0 4.0 17.1 2.9 14.4 2.7 Plg-3rut 2.3 0.3 2.4 0.5 1.7 0.2 2.3 0.3 2.1 0.2 0.7 0.1 4.8 1.1 2.1 0.4 3.4 0.6 2.3 0.2 5.1 1.0 1.1 0.2 0.7 0.2 0.8 0.1 4.8 1.0 0.8 0.2 1.0 0.2 0.7 0.1 0.9 0.2 2.2 0.8 2.1 0.4 1.7 0.4 Totalb 29.9 5.9 24.7 4.6 31.7 6.1 25.3 4.3 18.3 2.6 12.3 2.2 37.5 5.6 18.3 3.5 32.1 6.7 19.4 3.5 33.5 5.2 25.2 6.1 15.7 3.3 11.8 2.1 46.5 9.1 11.8 1.9 17.5 3.8 11.9 3.1 36.2 7.1 18.9 3.1 20.2 5.0 16.5 3.1

a Data expressed as micromolar of malvidine-3-glucoside (malv-3-gluc) per gram of fresh weight (FW). b Differences between OF and IPM total anthocyanin contents are statistically signicant (p < 0.05).

mAU

V.C. Fernandes et al. / Food Chemistry 134 (2012) 19261931 Table 2 Retention time and MS spectral data of the major phenolic compounds detected in strawberry extracts (both IPM and OF). Compounds Flavonols Kaempferol-3-acetylglucoside Quercetin-3-glucuronide Kaempferol-3-coumaroylglucoside Hydroxycinnamic acid derivates p-Coumaroylhexose Ferulic acid hexose derivative Flavan-3-ols Proanthocyanidin dimer Catechin Proanthocyanidin trimer Ellagitannins Ellagic acid deoxyhexoside Rt (min) 25.29 29.08 31.17 14.77 24.23 10.52;12.22 14.05 17.07 33.38 MS (m/z) 489 [M-H]477 [M-H]593 [M-H]325 [M-H]449 [M-H]577 [M-H]289 [M-H]865 [M-H]447 [M-H]MS2 (m/z) 285 301 447 163 431 269 245 695 357

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contribution at this absorbance. The reaction for scavenging DPPH radicals was performed in a microplate reader of 96 well plates (Biotek Powerwave XS). The reaction was carried out in the plate wells at a temperature of 25 C. A solution of 60 lM DPPH was prepared in methanol. 270 lL of this solution was added to each well together with 30 lL of antioxidant. Extracts tested were at a nal concentration of 10 lM. The decrease in absorbance was measured at 515 nm, at t = 0 and every 10 min, for 30 min. For the nal analysis, the 020 min reaction time range was used. Antiradical activity was expressed as lM TE per g sample FW. The antiradical activity was calculated from the equation determined from linear regression after plotting known solutions of Trolox with different concentrations.

2.10. Statistical analysis All tests were conducted at least in triplicate. Values are expressed as means standard deviation. Data were analysed using the GraphPad software 5 (unpaired two tailed t-test with Welch correction) and P < 0.05 was considered signicant.

Powerwave XS). The reaction was carried out on the plate wells at a temperature of 37 C. In short, FRAP reagent (10 vol. of 300 mM acetate buffer, pH 3.6 + 1 vol. of 10 mM TPTZ in 40 mM HCl + 1 vol. of 20 mM FeCl3) was diluted to one-third with acetate buffer. 270 lL of this solution was added to each well along with 30 lL of extract. The control assay was performed using 270 lL of FRAP reagent and 30 lL of methanol. The extracts to be tested were dissolved in methanol and used at a nal concentration of 10 lM. The absorbance at 593 nm was measured at time 0 and 4 min. The results were expressed as Trolox equivalents (TE) per g sample FW.

3. Results and discussion 3.1. Total phenolic analysis Strawberry samples (IPM and OF growing conditions) were analysed in terms of total phenolic composition by using the Folin Ciocalteu colorimetric method. OF grown strawberries were found to contain higher amounts of phenolic compounds when compared to IPM grown strawberries, 108 and 81 lM g1 FW GAE, respectively (Fig. 1). This difference is partly due to the presence of anthocyanins that were found to occur in higher amounts in OF strawberries (Fig. 2). Indeed, the average total anthocyanin amounts of the 11 OF extracts analysed was around 29 lM g1 FW while the 11 IPM extracts were found to have ca 18 lM g1 FW. On the other hand, the total average proanthocyanidin amounts in both types of extracts were not found to be statistically different (data not shown).

2.9. Radical DPPH scavenging activity Following the method described in the literature (Bondet, BrandWilliams, & Berset, 1997) with modications, radical activities were determined by using DPPH (2,2-diphenyl-1picrylhydrazyl) as a free radical. The tested extract reacted with DPPH and decreased the absorbance measured at 515 nm, which indicated the scavenging potential of the phenolic compounds. As all extracts tested absorbed at 515 nm, previous control assays were performed with all the samples in order to subtract their

Table 3 Antiradical activity and reducing power of the strawberry extracts assessed by DPPH method and FRAP method. Strawberry varieties Festival 09 Festival 10 Festival 11 Camarosa 09 Camarosa 10 Camarosa 11 Siba 09 Siba 10 Siba 11 San Andreas 10 San Andreas 11
a b

Crop type IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF IPM OF

DPPHb (lM TE/g FW)a 12.4 2.4 18.2 4.8 12.4 2.9 17.1 3.4 12.9 3.1 16.1 4.3 14.1 1.9 16.1 2.6 8.8 1.8 20.1 3.5 10.0 1.9 16.2 2.8 12.4 2.3 19.2 1.5 13.3 4.1 16.2 2.8 14.9 3.1 18.0 2.9 6.4 1.2 16.1 3.5 12.5 2.5 16.1 2.9

FRAPb (lM TE/g FW) 13.2 3.1 28.0 6.8 14.4 3.1 25.7 6.2 14.0 2.3 27.9 7.1 12.9 3.0 28.3 6.1 17.3 4.0 23.5 3.6 18.1 3.6 30.8 6.1 14.4 2.8 22.6 4.3 14.5 3.7 23.9 5.1 15.7 3.5 31.7 5.9 16.3 3.1 22.9 4.2 17.4 3.1 20.1 5.0

Data expressed as micromolar of Trolox (TE) per gram of fresh weight (FW). Differences between OF and IPM FRAP and DPPH assay are statistically signicant (p < 0.05).

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3.2. Anthocyanin analysis HPLC-DAD/MS analysis of the strawberry extracts identied a total of three major anthocyanin compounds: cyanidin-3-glucoside (Cy-3-gluc), pelargonidin-3-glucoside (Plg-3-gluc) and pelargonidin-3-rutinoside (Plg-3-rut). Mass data revealed a [M]+ ion at m/z 449 with a major ion fragment at m/z 287 (loss of hexosyl residue) attributed to Cy-3-gluc. A compound with [M]+ at m/z 433 and a major ion fragment at m/z 271 (loss of a hexosyl residue) was identied as Plg-3-gluc. Finally, pelargonidin-3-rutinoside (Plg-3-rut) was identied at m/z 579 with two major fragments at m/z 433 and m/z 271. Plg-3-gluc was the major anthocyanin followed by Plg-3-rut and Cy-3-gluc, in agreement with previous studies (Kajdzanoska, Petreska, & Stefova, 2011). The general anthocyanin chromatograms of the OF and IPM strawberry extracts are displayed in Fig. 3. The anthocyanin proles of strawberries from Portugal grown under IPM and OF have not previously been reported in the literature. The different anthocyanin contents in all extracts analysed are shown in Table 1. Overall, the amounts of anthocyanins are systematically higher in the OF extracts among the different varieties. 3.3. Polyphenolic characterisation

DPPH

a
TE (M g FW)

20

OF IPM

15

*
10

-1

Crop Type
FRAP

b
TE ( M g-1 FW)

30

IP M

OF IPM

Strawberry extracts were also analysed by HPLC-DAD/MS in order to identify the main classes of polyphenols present. Identication of phenolic compounds was based on retention times of the chromatographic peaks and the corresponding UVvis absorption and mass spectral data (Table 2). In addition to the anthocyanins already reported, the major phenolic classes identied in strawberry samples were as follows: avonols (quercetin and Kaempferol conjugates), hydroxycinnamic acid derivates (p-coumaric and ferulic acid derivatives), avan-3-ols (catechin and proanthocyanidins) and ellagitannins (ellagic acid conjugates). LC-MS analysis of the strawberry extract led to characterisation of 10 compounds, as indicated in Table 2. The presence of all these phenolic classes in strawberries have already been reported in the literature (Buendia et al., 2010; Simirgiotis, Theoduloz, Caligari, & Schmeda-Hirschmann, 2009). In agreement with previous observations for proanthocyanidins, the levels of these polyphenol classes were not found to be statistically different between the two types of extracts (data not shown). 3.4. Antioxidant properties of strawberry extracts The free radical scavenging capacity of OF and IPM strawberry extracts was tested using the DPPH method, as described in the Material and Methods section. In this study, all 22 ethanol extracts from the four strawberry varieties investigated displayed radical scavenging activity (Table 3). The OF strawberry extracts systematically showed higher radical scavenging activities than the IPM strawberry extracts. The average values are showed in Fig. 4a (17.2 0.4 and 11.9 0.8 TE lM g1 FW). This result was anticipated because of the higher amounts of total phenolics present in the OF strawberry extracts and because these have been reported to have good free radical scavenging capacities (Azevedo et al., 2010). These extracts were also assayed for their reducing capacity using the FRAP method previously developed by Benzie and Strain (1996) with some modications. The results presented in Table 3 shows a similar trend to that observed for the DPPH assay with higher values obtained for the OF strawberry extracts. Furthermore, the difference between the reducing capacity of OF and IPM strawberry extracts was higher than that of their radical scavenging capacity (Fig. 4). This result may be explained by the fact that some polyphenols, like anthocyanins present in higher

20

*
10

Crop Type
Fig. 4. Average radical scavenging activity (DPPH) and average reducing capacity (FRAP) of OF and IPM strawberry extracts. Columns represent mean standard deviation, p < 0.05. Differences between column means are statistically signicant.

amount in OF strawberry extracts, are more prone to this feature than other compounds. 4. Conclusion The present study clearly shows that the type of agriculture may have important consequences in terms of the phenolic composition and antioxidant features of cultivated crops. This was shown here in the case of strawberries. Varieties grown under different agricultural practices, namely OF and IPM, contain different amounts of phenolic compounds, which has consequences for their resulting antioxidant proles. This outcome agrees with previous reports in the literature dealing with other samples (Navarro, Perez-Lopez, Mercader, Carbonell-Barrachina, & Gabaldon, 2011; Wang, Chen, Sciarappa, Wang, & Camp, 2008). Although several classes of phenolic compounds were detected in all strawberry samples, the levels of anthocyanins were the only phenolics to be signicantly affected by the different agricultural practices tested (OF and IPM). Indeed, strawberries grown under organic farming were found to contain higher levels of anthocyanins than IPM grown strawberries. Also, the radical scavenging ability and the reducing capacity assayed by the DPPH and FRAP methods, respectively, were higher in strawberry extracts grown under organic farming (Simirgiotis, Theoduloz, Caligari, & Schmeda-Hirschmann, 2009). Since the levels of anthocyanins were the only ones to be statistically different between the two

IP M

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types of extracts, it is probable that these compounds play a crucial role in the observed differences in antioxidant features. Acknowledgments This research was supported by a Ph.D. Grant from FCT (Fundao para a Cincia e a Tecnologia- BD/47200/2008) and Grant No. PEst-C/EQB/LA0006/2011. The authors acknowledge the Portuguese farmers for providing strawberry samples. References
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