Journal of Food Composition and Analysis 23 (2010) 540–544

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Journal of Food Composition and Analysis

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Original Article

Comparison of antioxidant capacity and phytochemical properties of wild and

cultivated red raspberries (Rubus idaeus L.)
Çetin Çekiç 1,*, Mustafa Özgen 1,*
Department of Horticulture, Faculty of Agriculture, University of Gaziosmanpaşa, 60240 Tokat, Turkey

A R T I C L E I N F O A B S T R A C T

Article history: We investigated some of the chemical properties and antioxidant capacities of 14 wild red raspberry
Received 19 January 2009 accessions selected from northern Turkey. In addition, the cultivars Heritage and Tulameen were
Received in revised form 29 June 2009 included in the study to determine the variation between wild and cultivated raspberries. Total
Accepted 5 July 2009
phenolics (TP), total monomeric anthocyanins (TMA), soluble solids (TSS), individual organic acids and
sugars in the fruit were examined. Antioxidant capacity of fruits was determined by both ferric
Keywords: reducing ability of plasma (FRAP) and trolox equivalent antioxidant capacity (TEAC) assays. The fruit
Red raspberry
color and weight were determined as well. The result of this study indicated that some of the wild
Rubus idaeus L.
Cultivar difference
accessions of red raspberries have higher antioxidant capacity and phytonutrient content than existing
Anthocyanin domesticated cultivars. Moreover, significant variability was found for antioxidant capacity, TP, TMA,
FRAP organic acids and sugars of wild raspberries. Principle component analysis showed that the accessions
Organic acid were divided into three groups: A2, A9, A12, A14 formed the first group with high phytonutrient
Phenolic properties; the cultivars Heritage and Tulameen grouped together with high phytonutrients but low
TEAC color values; and the rest of the accessions formed the final group. The antioxidant capacity among
Biodiversity samples averaged 14.6 and 14.1 mmol TE/gfw using FRAP and TEAC methods, respectively.
Food analysis
ß 2009 Elsevier Inc. All rights reserved.
Food composition

1. Introduction by genetics and environment (Anttonen and Karjalainen, 2005;

Connor et al., 2005a,b; McGhie et al., 2002; Özgen et al., 2008).
Several studies have demonstrated the correlation between Furthermore, Connor et al. (2005a) indicated that having high
consumption of fresh fruits and vegetables with the prevention, bioactive compounds variability among the accessions is impor-
delay or onset of chronic degenerative diseases including cancer tant to obtain superior cultivars, and selection programs are the
(Kaur and Kapoor, 2001; Steinmetz and Potter, 1996). As with important resources.
other fruits, berries may have additional health benefits, as they As an important commercial fruit crop, red raspberries are
are rich sources of micronutrients and phytochemicals such as widely grown in all temperate regions of the world and are
anthocyanins, phenolics and ascorbic acids (Beattie et al., 2005). consumed by local people. Many of the most important modern
In vitro studies indicate that anthocyanins and other polyphenols commercial red raspberry cultivars derive from hybrids or
in berries have a range of potential anti-cancer and heart disease selections from the wild. Northern Turkey is one of the important
properties including antioxidant, anti-inflammatory and cell germplasm centers of this species (Davis, 1982). They grow
regulatory effects (Juranic and Zizak, 2005; Zafra-Stone et al., naturally in high elevations (above 1000 m) and require moist, rich
2007). soils. In some cases, the wild forms of plants may demonstrate
Red raspberries (Rubus idaeus L.), in particular, are known to different phytonutrient profiles and flavors from the cultivated
demonstrate strong antioxidant capacity, mainly as a result of ones. Several researchers have stated that most of the wild species
their high levels of anthocyanins and other phenolic compounds preserve higher antioxidant capacity, richer flavor, and more
(Kafkas et al., 2008; Kähkönen et al., 2001). However, phenolic attractive color, fragrance and aromatic compounds (Halvorsen
compounds and antioxidant capacities can be influenced, mainly et al., 2002; Özgen et al., 2007).
In this study, we investigated the variation of antioxidant
capacity of wild red raspberry accessions in comparison with
* Corresponding authors. Tel.: +90 356 2521616x2110; fax: +90 356 2521488.
representatives of the cultivated raspberries. We also aimed to
E-mail addresses: ccekic@[Link] (Ç. Çekiç), mozgen@[Link] (M. Özgen). identify wild red raspberry accessions with high antioxidant
1
Both the authors have equal contribution. capacity for potential use in cultivar development.

0889-1575/$ – see front matter ß 2009 Elsevier Inc. All rights reserved.
doi:10.1016/[Link].2009.07.002
 Ç. Çekiç, M. Özgen / Journal of Food Composition and Analysis 23 (2010) 540–544 541

Table 1 2.4. Determination of total antioxidant activity

The altitude, latitude and longitude where the genotypes were collected.

Genotypes Province Altitude (m) Latitude Longitude Total antioxidant activity was estimated by two standard
A1 Trabzon 1505 408 500
9900
398 250
96 00 procedures: ferric reducing ability of plasma (FRAP) and trolox
A2 Trabzon 1506 408 510 0100 398 260 2700 equivalent antioxidant capacity (TEAC) assays. The FRAP assay
A5 Trabzon 1732 408 390 4100 398 400 9100 (Benzie and Strain, 1996) was conducted using three aqueous stock
A8 Trabzon 1718 408 390 4700 398 400 7300 solutions containing 0.1 mol/L acetate buffer (pH 3.6), 10 mmol/L
A9 Trabzon 1123 408 360 4700 408 230 7900
TPTZ [2,4,6-tris(2-pyridyl)-1,3,5-triazine] acidified with concen-
A10 Rize 1486 408 560 4900 418 080 0300
A11 Rize 1584 408 560 1400 418 080 2500 trated hydrochloric acid, and 20 mmol/L ferric chloride. These
A12 Giresun 1381 408 340 7200 388 260 4100 solutions were prepared and stored in the dark under refrigeration.
A13 Ordu 1495 408 410 8100 378 550 4400 Stock solutions were combined ([Link], v/v/v) to form the FRAP
A14 Ordu 1480 408 400 5800 378 550 7600
reagent just prior to analysis. For each assay laboratory duplicate,
A15 Ordu 1730 408 390 9300 378 560 3400
A17 Giresun 1813 408 410 3900 388 150 0600
2.97 mL of FRAP reagent and 30 mL of sample extract were mixed.
A20 Giresun 1681 408 410 3300 388 180 7700 After 10 min, the absorbance of the reaction mixture was
A22 Trabzon 1775 408 510 3500 398 090 0800 determined at 593 nm on a spectrophotometer.
For the standard TEAC assay, ABTS was dissolved in acetate
buffer and prepared with potassium persulfate as described in
2. Materials and methods Rice-Evans et al. (1995) and Özgen et al. (2006). The mixture was
diluted in an acidic medium of 20 mM sodium acetate buffer (pH
2.1. Plant material and extraction 4.5) to an absorbance of 0.700  0.01 at 734 nm for longer stability
(Özgen et al., 2006). For the spectrophotometric assay, 3 mL of the
As result of a national bramble selection program in Turkey, 14 ABTS+ solution and 10 mL of fruit extract were mixed and incubated
superior wild red raspberry (R. idaeus L.) accesions were selected for 10 min and the absorbance was determined at 734 nm. Trolox was
from northern Turkey where they grow naturally in the mountain used as a standard for both assays. The results were expressed as
area between 1120 and 1810 m elevations (Table 1). Commercially mmol trolox equivalent (TE) in gram fw basis.
grown Heritage and Tulameen red raspberry cultivars were also
included in the experiment to compare and contrast antioxidant 2.5. Extraction of individual sugars and organic acids
properties of wild and cultivated red raspberries. Three indepen-
dent samples of fully mature fruits (each weighing about 200 g) For the extractions of individual sugars and organic acids, fruit
were harvested by hand in three separate plastic containers and slurries (5 g) were diluted with purified water or meta-phosphoric
transferred to the laboratory for physical and phytochemical acid (2.5%) solution for individual sugar and organic acid analysis,
analysis. The fruit color was measured using a Minolta portable respectively. The homogenate was centrifuged at 6000 rpm for
chromameter (Minolta, Model CR-400) which provided CIE L*, a* 5 min. Supernatants were filtered through a 0.45-mm membrane
and b* values. Then, fruit samples were frozen and stored at 30 8C filter (Iwaki Glass) before HPLC analysis, and the mobile phase
for chemical analysis. At the time of analysis, three replicates of solvents were degassed before use. All the samples and standards
fruit samples were thawed at room temperature and homogenized were injected three times each and mean values were used.
in a standard food blender; excess fruits (more than 50 individual The HPLC analyses were carried out using a PerkinElmer HPLC
fruits) were used to minimize naturally occurring fruit-to-fruit system with Totalchrom navigator 6.2.1 software, a pump and UV
variation. Slurries were used to determine total soluble solid (TSS) detector (PerkinElmer, Series-200) (Waltham, MA, USA). The
content by refractometery (Atago, Pal-1). method for separation and determination of organic acids was
modified from Shui and Leong (2002). The separation was carried
2.2. Total phenolic (TP) determination out on an SGE wakosil C18RS 5 mm column (250 mm  4.6 mm
i.d.). Optimum efficiency of separation was obtained using pH 2.5
For the extraction and determination of TP content, a single sulfuric acid solution (solvent A), and methanol (solvent B). Other
extraction procedure was designed to assay phenols (Singleton and parameters adopted were as follows: injection volume, 20 mL;
Rossi, 1965). For each replicate, a 3 g aliquot of slurry was transferred column temperature, 30 8C; and detection wavelength, 215 nm.
to polypropylene tubes and extracted with 20 mL of extraction Analysis of sugars was performed using a refractive index (RI)
buffer containing acetone, water, and acetic acid (70:29.5:0.5, v/v/v) detector (PerkinElmer) (Bartolome et al., 1995). The separation was
for 2 h. After filtration, acetone was removed by rotary evaporation, carried out on an SGE SS Exsil amino column (250 mm  4.6 mm
after which the concentrated samples were brought to a final i.d.). The elution solvent used was 80% acetonitril and 20% deionised
volume of 20 mL with deionised water. Next, Folin–Ciocalteu’s water. The column was operated at 30 8C with 0.9 mL/min flow rate.
phenol reagent and water were incubated for 8 min, followed by the Sample injection volume was 20 mL.
addition of 7% sodium carbonate. After 2 h, the absorbance was
measured by an automated UV–vis spectrophotometer at 750 nm. 2.6. Statistical analysis
Gallic acid was used as standard. The results were expressed as mg
gallic acid equivalent (GAE) in gram fresh weight (fw) basis. Data were analyzed using SAS procedures and software (SAS,
2006). Analysis of variance was constructed using the PROC GLM
2.3. Total monomeric anthocyanins (TMA) procedure. The means were separated using the least significant
difference (LSD) method at 0.01 significance level. PC was
TMA were estimated by a pH differential method (Giusti and performed using PRINCOMP procedure and the accessions were
Wrolstad, 2005) using a UV–vis spectrophotometer (model T60U, plotted on the first three PCs using G3G procedure.
PG Instruments). Absorbance was measured at 533 nm and
700 nm in buffers at pH 1.0 and 4.5 using A = (A533  A700)pH 3. Results and discussion
1.0  (A533  A700)pH 4.5 with a molar extinction coefficient of
30,900. Results were expressed as mg of cyanidin-3-sophoroside Fruit pomological characteristics of selected red raspberries are
equivalent in gram fw basis. presented in Table 2. On average, the fruit weight was 1.3 g. As
542 Ç. Çekiç, M. Özgen / Journal of Food Composition and Analysis 23 (2010) 540–544

Table 2
Several pomological characteristics of red raspberry accessions sampled from Turkey along with two cultivars.

Accession and cultivar Fruit weight (g) Dry matter (%) Brix (%) L* a* b*

A1 0.9 d 18.2 h 10.4 gh 43.4 de 35.8 c–e 17.0 e–g

A2 1.7 c 23.3 a 12.7 d 49.6 a 40.2 a–c 18.8 c–g
A5 1.2 cd 17.6 i 10.5 gh 41.6 de 40.3 a–c 20.4 a–f
A8 1.1 cd 19.4 f 12.9 cd 43.3 de 42.8 a 21.0 a–e
A9 1.1 d 19.7 f 11.4 f 45.0 b–d 41.5 ab 23.7 ab
A10 1.2 cd 20.6 e 10.1 hi 47.8 ab 38.0 a–d 17.3 d–g
A11 0.9 d 19.4 f 10.2 hi 48.2 ab 34.5 de 15.7 f–g
A12 1.2 cd 23.1 a 13.4 b 43.3 de 36.4 b–e 17.5 c–g
A13 1.1 d 18.8 g 9.6 ij 44.2 c–e 32.2 e 15.7 g
A14 0.7 d 21.4 d 12.2 e 42.2 de 41.3 ab 24.1 a
A15 1.2 cd 21.9 c 13.1 bc 47.0 a–c 40.9 a–c 22.0 a–c
A17 1.1 d 22.9 a 10.8 g 40.5 ef 38.2 a–d 19.4 b–g
A20 1.0 d 22.3 b 10.0 ij 42.5 de 40.2 a–c 21.8 a–d
A22 1.2 cd 20.8 e 13.3 bc 41.7 de 40.7 a–c 21.0 a–e
Heritage 2.5 b 16.6 j 11.8 ef 36.1 g 34.4 de 16.9 e–g
Tulameen 2.8 a 20.9 e 14.7 a 37.9 fg 33.4 de 16.5 e–g

LSD0.01 0.43 0.68 0.73 3.37 4.48 4.03

LSD0.01: Least significant differences at 0.01 level.

expected, the weight of cultivated berries was much larger than displayed similar results (Khanizadeh et al., 2009). The result for
wild accessions. A2 had the biggest berries among the wild A2 seems to indicate a rich source of phenolics. The average TMA
accessions, with 1.7 g compared to 2.5 and 2.8 g for Heritage and content was 204.9 mg cy-3-soph/g fw, and A9 had the highest
Tulameen, respectively. Fruit dry matter content ranged from 16.6 anthocyanin content with 296.2 mg cy-3-soph/g fw. A2 displayed
to 23.3%. The average TSS content of berries was 11.7%. In terms of the highest antioxidant capacity for FRAP and TEAC methods,
fruit color, the variation in b* was higher than those of L* and a*. In resulting in 19.8 and 21.5 mmol TE/g fw, respectively. Among all
the chromaticity coordinates, where high b* indicates toward the raspberries tested, A20 had the lowest TP and TMA content
yellow direction and high a* indicates toward red direction, wild with the lowest antioxidant capacity determined by TEAC.
accessions looked darker red and towards to yellowish color. On Previous studies (e.g. Connor et al., 2005a,b; Özgen et al., 2008)
the other hand, the appearance of cultivated red raspberries was a reported strong relationships among measures of TP content,
blue-based lighter red color. The average a* and b* values were 38.2 anthocyanin levels, and antioxidant capacity of Rubus species.
and 19.3, respectively. L* values represent lightness and wild From our data we calculated high correlation coefficients (r)
accessions had higher L* values. between the TP values of red raspberry samples and their
There were significant differences among the accessions for TP, respective antioxidant capacities. Correlation coefficients between
TMA and antioxidant capacity (Table 3). TP ranged from 1486 (A20) TEAC and TP, TMA, FRAP was r = 0.74, 0.73 and 0.81, respectively.
to 3479 (A2), with an average of 2046 mg GAE/g fw. We compared When PC analysis was considered, the first three PC explained
TP values, and except for A2, the other accessions and cultivars 30, 25 and 16% of the variation, making a total of 71% (Table 4).
Among the variables tested, the phytonutrient-related parameters
(TP, TMA, FRAP and TEAC) were highly correlated with PC1. The
Table 3
Variation of total phenolics (TP), total monomeric anthocyanin (TMA), antioxidant highly correlated variables with PCs were color measurements (L*,
capacity (FRAP and TEAC) of red raspberry accessions sampled from Turkey along a*, b*) and fruit weight and dry matter content. Interestingly, while
with two cultivars. dry weight was positively correlated with PC2, fruit weight was
Accession and cultivar TPa TMAb FRAPc TEACd negatively correlated. The highest correlation with PC3 was
calculated from TSS content.
A1 2040 de 258.0 b 13.9 de 13.5 d
A2 3479 a 199.1 de 19.8 a 21.5 a
Based on the PC analysis, the genotypes tested can be divided
A5 1933 d–f 216.1 cd 11.5 fg 13.3 de into three groups, as follows: A2, A9, A12, A14 formed the first
A8 2120 cd 214.0 cd 11.7 fg 11.6 d–f group with high antioxidant capacity, TP, TMA content and darker
A9 2447 b 296.2 a 17.9 b 17.0 c red color (Fig. 1).
A10 1664 gh 137.5 f 11.2 g 11.3 d–f
The cultivars Heritage and Tulameen grouped together and had
A11 2125 cd 179.1 e 12.0 fg 12.9 d–f
A12 2084 cd 237.0 bc 15.2 cd 17.5 bc high phytonutrient content, lighter red color but larger fruit size.
A13 1947 de 214.6 cd 16.0 c 16.2 c
A14 2386 b 239.5 bc 19.7 a 19.3 b Table 4
A15 1684 f–h 197.6 de 13.2 ef 10.6 fg First three principle component (PC) scores of the variables used to evaluate
A17 1625 gh 188.8 de 13.2 ef 11.1 e–g raspberry accessions sampled from Turkey along with two cultivars.
A20 1486 gh 65.6 g 14.4 c–e 8.9 g
Variable PC1 PC2 PC3
A22 1586 gh 200.6 de 11.4 fg 11.1 e–g
Heritage 1795 e–g 239.5 bc 18.1 ab 17.5 bc Fruit weight 0.22 0.40 0.39
Tulameen 2342 bc 195.9 de 14.4 c–e 12.9 d–f Dry weight 0.03 0.36 0.16
Brix 0.26 0.03 0.59
LSD0.01 243.17 27.41 1.69 2.11 L 0.02 0.35 0.49
LSD0.01: Least significant differences at 0.01 level. a 0.03 0.55 0.24
a
TP contents were estimated by the Folin–Ciocalteu assay of Singleton and Rossi b 0.02 0.51 0.30
(1965). Values are expressed as mg GAE/g fw. Total phenolics 0.48 0.14 0.17
b
TMA were determined by the pH-differential method of Giusti and Wrolstad Total anthocyanin 0.37 0.06 0.02
(2005). Values are expressed as mg cy-3-soph/g fw. FRAP 0.48 0.07 0.08
c
FRAP values were determined by the method of Benzie and Strain (1996). TEAC 0.53 0.01 0.22
Values are expressed as mmol of TE/g fw.
d
Eigenvalue 3.03 2.51 1.60
TEAC values were determined by the method of Özgen et al. (2006). Values are
Proportion 0.30 0.25 0.16
expressed as mmol TE/g fw.
[(Fig._1)TD$IG] Ç. Çekiç, M. Özgen / Journal of Food Composition and Analysis 23 (2010) 540–544 543

fruits, particularly berries. The result of our study indicates that

some of the wild accessions of red raspberries have higher
antioxidant capacity and phytonutrient content than existing
domesticated cultivars. Moreover, significant variability was found
for the antioxidant capacity, TP, TMA, organic acids and sugars of
wild raspberries. These findings may help and guide fruit breeders
to develop new cultivars with high antioxidant capacity using wild
types as a resource to help meet recent consumer trends.

Acknowledgements

This study was supported by the Scientific and Technological

Research Council of Turkey (TUBITAK) (Project No. TOVAG-
107O209); we greatly acknowledge the financial support. We
would also like to thank all the project personnel for guiding us and
collecting these valuable materials.

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