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Quality parameters, biocompounds and antioxidant activity in fruits of nine quince (Cydonia oblonga Miller) accessions
Scientia Horticulturae 154 (2013) 61–65
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Quality parameters, biocompounds and antioxidant activity in fruits of nine quince (Cydonia oblonga Miller) accessions Pilar Legua a , María Serrano b,∗ , Pablo Melgarejo a , Daniel Valero c , Juan José Martínez a , Rafael Martínez a , Francisca Hernández a a
Department of Plant Science and Microbiology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain Department of Applied Biology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain c Department of Food Technology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain b
a r t i c l e
i n f o
Article history: Received 27 November 2012 Received in revised form 13 February 2013 Accepted 18 February 2013 Keywords: Antioxidant activity Carotenoids Crude fiber Phenols Quality
a b s t r a c t Quality parameters, as well as bioactive compounds and antioxidant activity were determined in nine quince (Cydonia oblonga Miller) clones belonging to the quince gene bank of the University Miguel Hernández (Alicante, Spain). Significant differences were found among quince clones in fruit weight, firmness, total soluble solids (TSS), total acidity (TA), crude fiber and sensory attributes. Bioactive compound concentration and total antioxidant activity, in both hydrophilic (H-TAA) and lipophilic (L-TAA) extracts, were also found to be different in flesh and skin among quince clones. High correlations were found between total phenolics and H-TAA and total carotenoids and L-TAA, showing that phenolics and carotenoids are the main compounds responsible for hydrophilic and lipophilic antioxidant activity, respectively. The quince clones with the highest content on bioactive compounds and antioxidant activity in the edible portion were AM4, CTM8 and OM6. In addition, AM4 and OM6 accessions had low astringency levels and an equilibrated TSS/TA ratio, leading them also appropriated for fresh consumption. Thus, these accessions could be used, together with other having large fruits as ZM6 accession, to select new cultivars with high yield, and overall fruit quality attributes and specially having high content of bioactive compounds with antioxidant activity and health benefits. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Quince (Cydonia oblonga Miller) is used extensively in Europe as a dwarfing rootstock for pear. Total world production of fresh fruit quince in 2010 was 540.337 tons, from which 14.200 tons were produced in Spain (FAOSTAT, 2012). The quince tree shows high genetic variability, with more than 30 different cultivars in Europe, 19 in USA and 86 in the old USSR being described by Scaramuzzi (1957), which were often mistaken by farmers due to the high number of synonyms, polymorphism of fruits and leaves and the existence of many trees propagated by seeds. Likewise, several authors have studied the genetic variability in this species worldwide (Shao and Lu, 1995; Ercisli et al., 1999; Srivastava et al., 2005; Rodríguez-Guisado et al., 2009). Quince fruit at un-ripe stage is not very appreciated for fresh market due to pulp hardness, bitterness and astringency, but when ripe, quince has pleasant, lasting and powerful flavor. Nevertheless, quince is intended primarily to the manufacture of marmalade, jams, jelly and cakes (Silva et al., 2002, 2005, 2006; Sharma et al.,
∗ Corresponding author. Tel.: +34 966749616; fax: +34 966749678. E-mail address: [email protected] (M. Serrano). 0304-4238/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scienta.2013.02.017
2011). Quince has low fat content and is an important source of organic acids, sugars, crude fiber and minerals like potassium, phosphorous and calcium, as well as of health-promoting constituents, such as phenolic compounds with antioxidant activity (Silva et al., 2004a, 2004b; Fattouch et al., 2007; Rodríguez-Guisado et al., 2009) and it is known to have hypoglycemic, anti-inflammatory, anticarcinogenic, antimicrobial, anti-allergic and antiulcerative properties and act as a tonic for heart and brain (Hamauzu et al., 2006; Fattouch et al., 2007; Shinomiya et al., 2009). Since native quince resources are almost vanished nowadays in Spain, the Plant Science and Microbiology Department (Miguel Hernandez University, UMH) collaborated in the establishment of a gene bank with a total of 87 quince accessions in 1995 (GENRES29CT95) with a wide genetic variability. Thus, the general aim of this research was to perform the morphological and quality characterization of quince fruits from 9 of these accessions, and to determine their content on bioactive compounds (polyphenols and carotenoids) and the total antioxidant activity (TAA), measured by the first time in quince fruit in the hydrophilic (H-TAA) and lipophilic (L-TAA) fractions separately, in the skin and flesh. The results will provide information about the potential interest of these accessions to fresh fruit consumption or to made products such as jam and jelly, with high content on bioactive
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compounds and health benefits. In addition, results would help breeders to select new cultivars based on the overall fruit quality, taking into account not only the external fruit quality or nutritional and organoleptic properties, but also considering the content of bioactive compounds and antioxidant activity, and thus to fulfill consumer’s wishes through the fruits with high health benefits.
following the official methodology established by the Spanish Ministry of Agriculture, Fisheries and Food as described by Rodríguez-Guisado et al. (2009) and results expressed as % in a fresh weight basis.
2.3. Total antioxidant activity determination (TAA) 2. Materials and methods 2.1. Plant material Nine quince clones (AM4, CTM7, CTM8, CTM10, MOM1, OHM4, OM6, ZM4 and ZM6) were used in this research, all of them with high agronomic properties and fruits with high quality, being appropriated for fresh market and processing (unpublished previous results). The selected plant materials belong to the gene bank quince located at the experimental field station of Miguel Hernández University in the province of Alicante, Spain (02◦ 03 50 E, 38◦ 03 50 N, and 25 mals). Trees were planted at a spacing of 4 m × 3 m. Standard cultural practices (pruning, thinning, fertilization and treatments) were performed. The experiment was established in a randomized block design with four single-tree replications and grafted onto quince BA-29 rootstock. Guard rows were used to preclude edge effects. Fruits were harvested at commercial ripening stage at the end of September and first October and 20 homogeneous fruits (based on color, size and absence of defects) were selected from each clone (5 fruits from each tree) for analytical determinations. Thus, since quince trees were under homogeneous growing conditions and fruits harvested at similar ripening stage, results are valid for comparative purposes. The study was conducted twice in the years 2008 and 2009 and results are the mean ± SE of two years. 2.2. Fruit morphological and quality parameters Fruit weight and firmness were determined individually in 20 fruits (in both 2008 and 2009 years) by using a digital balance Sartorius (model BL-600, 0.01 g accuracy, Goettingen, Germany) and a Bertuzzi Penetrometer (model FT-327, Facchini, Alfonsine, Italy), equipped with an 8 mm cylindrical plunger, respectively and data are the mean ± SE. Firmness measurements were performed on two opposite faces in the equatorial zone (where the skin was removed) and results were expressed in kg force (kgf) cm−2 . After that, 4 subsamples of 5 fruits (from the 4 tress or replicates) were performed for the following analytical determinations. They were hand-peeled and skin and pulp were cut in small pieces to obtain homogeneous samples in which the following parameters were determined in duplicate. From pulp samples 10 g were used for total soluble solids (TSS) and total acidity (TA) determination, and 2 g for total fiber quantification. The remaining flesh samples as well as the skin samples were immediately frozen and ground in liquid N2 and stored in freezer at −40 ◦ C until analysis of total phenolics, total carotenoids and total antioxidant activity (TAA) was carried out. For TSS and TA determination 10 g of pulp samples were squeezed using a commercial blender and the extracted juice was later sieved and centrifuged at 8000 × g for 20 min (Sigma 3–18 K, Osterode and Harz, Germany). An aliquot of this supernatant was used to determine TSS with a digital refractometer Atago PAL-1 (Atago Co. Ltd., Tokyo, Japan) at 20 ◦ C, and expressed as percentage (◦ Brix). TA was determined in 1 mL of the above supernatant diluted in 25 mL of distilled water by titration with 0.1 N NaOH up to pH 8.1, using an automatic titration device (877 Titrino plus, Metrohm ion analyses CH9101, Herisau, Switzerland) and results expressed as g of malic L−1 . Maturity index (MI) was calculated as the ratio between TSS and TA. Crude fiber content was quantified
TAA was quantified according to Díaz-Mula et al. (2008) which enables to determine TAA due to both hydrophilic and lipophilic compounds in the same extraction. Briefly, for each sub-sample, 5 g of pulp or 1 g of skin were homogenized in 5 mL of 50 mM phosphate buffer pH = 7.8 and 3 mL of ethyl acetate, then centrifuged at 10,000 × g for 15 min at 4 ◦ C. The upper fraction was used for TAA due to lipophilic compounds (L-TAA) and the lower for TAA due to hydrophilic compounds (H-TAA). In both cases, TAA was determined using the enzymatic system composed of the chromophore 2,2 -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), the horse radish peroxidase enzyme (HRP) and its oxidant substrate (hydrogen peroxide), in which ABTS+• radicals are generated and monitored at 730 nm. The decrease in absorbance after adding the extract was proportional to TAA of the sample. A calibration curve was performed with Trolox ((R)-(+)-6-hydroxy2,5,7,8-tetramethyl-croman-2-carboxylic acid) (0–20 nmol) from Sigma (Madrid, Spain), and results are expressed as mg of Trolox equivalent 100 g−1 .
2.4. Total phenolics and total carotenoids determination Total phenolics were extracted according to Tomás-Barberán et al. (2001) using water:methanol (2:8) containing 2 mM NaF and quantified using the Folin–Ciocalteu reagent (Singleton et al., 1999) and results (mean ± SE) were expressed as mg gallic acid equivalent 100 g−1 fresh weight. Total carotenoids were extracted and quantified as described by Díaz-Mula et al. (2008). Briefly, 1 g of skin or 2 g of flesh tissues were extracted with acetone and shaken with diethyl ether and 10% NaCl to separation of the two phases. The lipophilic phase was washed with Na2 SO4 (2%), saponified with 10% KOH in methanol, and the pigments were subsequently extracted with diethyl ether, evaporated and then made up to 25 ml with acetone. Total carotenoids were estimated by reading the absorbance at 450 nm in a UNICAM Helios-␣ spectrophotometer (Cambridge, UK), and expressed as mg of -carotene equivalent 100 g−1 fresh weight, taking into account the ε1% cm = 2560 and the results were the mean ± SE.
2.5. Sensorial analysis Five fruits from each clone were used to evaluate both pulp astringency and chewiness by a sensory panel of 10 expert tasters. Pulp astringency was evaluated as high or low and chewiness as hard, semi-soft or soft and results expressed as percentage of panelist giving each classification.
2.6. Statistical analysis Statistical analyses were performed using the SPSS 18.0 for Windows (SPSS Science, Chicago, IL, USA). All data were subjected to basic descriptive statistics, and then evaluated by an analysis of variance (ANOVA) for mean comparisons. Fisher’s least significant difference test (LSD at 95.0% of confidence level) was applied for mean values discrimination.
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Table 1 Quality and sensory parameters of quince fruit clones. Results are the mean of data obtained from 2008 to 2009 years. Clone
AM4 CTM7 CTM8 CTM10 MOM1 OHM4 OM6 ZM4 ZM6
Fruit weight (g)
276.0a 331.5bc 269.3a 267.4a 354.1c 280.7ab 265.4a 377.2cd 415.9d
Pulp firmness (Kgf cm−2 )
9.55e 7.76d 4.73a 6.00bc 9.85e 6.56c 5.41ab 6.02bc 5.81bc
TSS (◦ Brix)
18.63e 15.60cd 14.60abc 16.07bcd 16.63d 15.00bc 13.97ab 13.40a 13.53ab
TA (g malic acid L−1 )
9.54d 7.10b 8.56cd 7.65bc 5.28a 6.48ab 7.17bc 7.15bc 6.76b
Crude fiber (%)
1.46cd 1.17ab 1.35bcd 1.63d 1.20abc 1.55d 1.11ab 1.33bcd 0.93a
Pulp astringency (%)
Pulp chewiness (%)
High
Low
Hard
20 50 70 70 60 50 30 30 90
80 50 30 30 40 50 70 70 10
100
Semi-soft
Soft
90 70 80
10 30 20
90 75 80 70
10 25 20 30
100
For each parameter, values within the same columns followed by different letters were significantly different (p < 0.05).
3. Results and discussion
3.2. Bioactive compounds and total antioxidant activity (TAA)
3.1. Quality parameters
Total phenolic content, total carotenoid concentration and TAA were measured in flesh and sink, the TAA being measured by the first time separately in hydrophilic (H-TAA) and lipophilic (L-TAA) fractions. Results revealed significant differences among quince accessions and between flesh and skin tissues (Figs. 1–4) showing that plant genetic background is an important factor responsible for differences among quince clones in the concentration of bioactive compounds, according to previous reports in other fruit species, such as plum (Díaz-Mula et al., 2008), loquat (Ercisli et al., 2012) or pomegranate (Caliskan and Bayazit, 2012). Thus, total phenolic concentration ranged from 40 to 100 mg 100 g−1 in the flesh, for M0M1 and AM4 accessions, respectively (Fig. 1) and from 200 to 430 mg 100 g−1 in the skin, for CTM8 and CTM10, respectively (Fig. 2). Thus, given the health beneficial effects of phenolics compounds, those fruits with high phenolics concentration will be advisable for degenerative illness prevention (Haminiuk et al., 2012). These phenolic concentrations are high as compared to that found in other fruits of the Mediterranean diet (Hamauzu et al., 2005; Valero and Serrano, 2010). In quince fruits harvested from different regions of Portugal, the main phenolic compounds in flesh were 5-O-caffeoylquinic (chlorogenic) acid and 3-O-caffeoylquinic (neochlorogenic) acid while in peel the most abundant phenolic was quercitin-3-O-rutinoside (rutin) followed by 3-O- and
Fruit weight ranged from 265 to 416 g, the clones OM6, CTM10, CTM8 and AM4 having the lowest fruit weight and the clone ZM6 the highest (Table 1). Accordingly, a great variability on fruit weight has been reported in other Spanish quince tree clones (RodríguezGuisado et al., 2009) as well as in Turkish (Yarlgac, 2001) and Indian ones (Srivastava et al., 2005). However, the Turkish ‘Katirbasi’ quince showed fruit weight ranging from 470 g to 530 g (Ercisli et al., 1999), similar to that of the clone ZM6 and even fruits weighting from 600 g to 1200 g have been reported in the ‘Jianchuan 1’ Chinese cultivar (Shao and Lu, 1995). Remarkable differences were also found among quince clones in fruit firmness (Table 1). AM4 and MOM1 scored the highest pulp firmness (9.55 and 9.85 kgf cm−2 , respectively) followed by CTM7 (7.76 kgf cm−2 ), while the lowest pulp firmness was scored by CTM8 (4.73 kg cm−2 ). These firmness values are quite high when compared to Turkish cultivars (Ercisli et al., 1999), showing that Spanish clones are firmer than Turkish varieties. However, the content in crude fibber (%) was quite similar among clones (Table 1), the clone ZM6 showing the lowest crude fiber content (0.93%) and the clone CTM10 the highest (1.63%). These values agree with obtained ones for the variety Indian ‘Plate 1’ cultivar (Sharma et al., 2011), while in other Spanish clones fiber content ranged from 1.7 to 8.1% (Rodríguez-Guisado et al., 2009). The evaluation of total soluble solids content (TSS) and total acidity (TA) also established significant differences among evaluated clones (Table 1), with values of TSS ranging from 13.40 (ZM4) to 18.63 ◦ Brix (AM4) and TA ranging from 5.28 (MOM1) to 9.54 g L−1 (AM4), according to previous reports in other quince accessions (Ercisli et al., 1999; Rodríguez-Guisado et al., 2009; Sharma et al., 2011). These variations in TSS and TA led to great differences in ripening index, which ranged from 17.15 in CTM8 clone to 32.22 in MOM1 one, affecting greatly to quince taste and flavor, since they depend more of the TSS/TA ratio that of the TSS or TA considered independently (Crisosto et al., 2007). Glucose and fructose have been reported as the main sugars in quince fruits, followed by sucrose and maltose, while malic plus quinic acids are the main organic acids followed by citric, tartaric, acetic and ascorbic acids in minor concentrations (Silva et al., 2004a, 2005; Rodríguez-Guisado et al., 2009). According to the sensory panel, all evaluated clones were considered as semi-soft with the exception of the clones AM4 and MOM1, which were classified as hard by all the panelists. With respect to pulp astringency, most of the clones were scored as having high astringency, with the exception of the clones AM4, OM6 and ZM4, which were scored as low pulp astringency, by most of the panelists, and therefore they could be considered good for fresh consumption. Rodríguez-Guisado et al. (2009) reported that other Spanish clones were predominantly scored as low pulp astringency and considered as semi-soft pulp.
Fig. 1. Total phenolics (mg 100 g−1 ) and hydrophilic total antioxidant activity (HTAA, mg 100 g−1 ) in the flesh of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
P. Legua et al. / Scientia Horticulturae 154 (2013) 61–65
700
y= 46x -81.56, r =0.927
600
Total Phenolics H-TAA
H-TAA
Phenolics and H-TAA in the Skin (mg 100 g -1)
64
600
500 400 300
C
200
500
200
250
300
c
350
Phenolics
e
400 d
300
A
200
d
D
a a A
b
b B
400
E
D AD
d
B
100
7 8 4 10 0M1 HM4 AM CTM CTM CTM 0 M
6 OM
4 ZM
6 ZM
Fig. 2. Total phenolics (mg 100 g−1 ) and hydrophilic total antioxidant activity (HTAA, mg 100 g−1 ) in the skin of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
5-O-affeoylquinic acids (Silva et al., 2005) as well as in the cv Smyrna from Japan (Hamauzu et al., 2006). Great differences were also found in H-TAA of flesh and skin among quince accessions (Figs. 1 and 2), and high correlations were found between total phenolic concentration and H-TAA (r2 = 0.983 and 0.927, for flesh and skin, respectively), showing that phenolics are the main hydrophilic compounds with antioxidant activity in skin and flesh quince tissues. Specifically, it has been shown that chlorogenic acids and the flavonols quercitine and its 3-O-rutinoside exhibited the highest antioxidant and antiradical scavenging capacity in quince peel and flesh (Silva et al., 2004b; Fiorentino et al., 2008). However, Fattouch et al. (2007) reported that pulp and peel quince extracts had higher antioxidant activity that the sum of those of the individual phenolic compounds, showing the synergistic effect of the individual antioxidants. Moreover, it has been also shown that quince phenolics have antioxidant activity in vivo, since they increased the antioxidant capacity of
Fig. 3. Total carotenoids (mg 100 g−1 ) and lipophilic total antioxidant activity (LTAA, mg 100 g−1 ) in the flesh of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
Fig. 4. Total carotenoids (mg 100 g−1 ) and lipophilic total antioxidant activity (LTAA, mg 100 g−1 ) in the skin of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case of capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
blood after oral administration to rats, as well as suppressed the occurrence of gastric lesions (Hamauzu et al., 2006). In addition, the bacteriostatic and bactericide activities of quince pulp and peel extracts have been also attributed to their main phenolic compounds (Fattouch et al., 2007). Total carotenoid concentration was higher in peel than in flesh and significant differences were found among quince accessions in both tissues. Thus, in flesh tissue, the highest carotenoid concentration in flesh was found in MOM1 accession and the lowest in ZM6, with values ≈0.42 and 0.04 mg 100 g−1 , respectively (Fig. 3), while in skin carotenoid ranged from ≈0.16 mg 100 g−1 in CRM8 to ≈0.86 mg 100 g−1 in AM4 (Fig. 4). Thus, no correlation was found between carotenoid concentration in skin and flesh in these quince accessions, showing that flesh coloration was independent of skin one. However, L-TAA followed the same pattern that carotenoid concentration, and in fact, high correlations were found between both parameters in flesh and skin tissues (Figs. 3 and 4), showing that carotenoids are the main lipophilic compounds with antioxidant activity as previously found in other fruits as sweet cherries, plums, peaches and nectarines (Díaz-Mula et al., 2008; Legua et al., 2011; Valero et al., 2011). In addition, it is interesting to point out that the H-TAA was higher than LTAA in both flesh and skin in all quince accessions, the H-TAA contributing to more than 90% of flesh antioxidant activity in all of them, except in MOM1 in which contributed by 73%, while in skin tissue H-TAA was 80–90% of the total antioxidant activity in all quince accessions. No previous reports are available for comparative purposes, since in previous papers, only antioxidant activity due to hydrophilic compounds has been addressed for quince fruits (Fattouch et al., 2007; Fiorentino et al., 2008; Silva et al., 2004b), and this is the first time that antioxidant activity in both hydrophilic and lipophilic extracts has been measured separately in quince fruits. Finally, it has been indicated that the content of phenolics compounds did not change during jam processing, although caffeoylquinic acid isomeration occurred (Silva et al., 2004b). Thus, those quince clones having fruits with high concentrations of bioactive compounds would lead to jam, jelly or marmalades also enriched with health beneficial compounds. In addition, since in the manufacture processing of these products only pulp is used, the peel and seed could be used as potential sources of antioxidants for use in food and pharmaceutical industry.
P. Legua et al. / Scientia Horticulturae 154 (2013) 61–65
4. Conclusion Taking into account that flesh tissue is the edible portion of quince fruit and that in quince processing to made marmalade, jams or jelly only flesh tissue is used, the quince clones with the highest health beneficial properties due to their content in bioactive compounds and antioxidant activity could be AM4, CTM8 and OM6. In addition, AM4 and OM6 accessions had low astringency levels and an equilibrated TSS/TA ratio, leading them also appropriated for fresh consumption. Thus, these accessions could be used, together with other having large fruits as ZM6 accessions, to select new cultivars with high yield, and overall fruit quality attributes and specially having high content of bioactive compounds with health benefits. References Caliskan, O., Bayazit, S., 2012. Phytochemical and antioxidant attributes of autochthonous Turkish pomegranates. Sci. Hortic. 147, 81–88. Crisosto, G.M., Crisosto, C.H., Echeverría, G., Puy, J., 2007. Segregation of plum and pluot cultivars according to their organoleptic characteristics. Postharvest Biol. Technol. 44, 271–276. Díaz-Mula, H.M., Zapata, P.J., Guillén, F., Castillo, S., Martínez-Romero, D., Valero, D., Serrano, M., 2008. Changes in physicochemical and nutritive parameters and bioactive compounds during development and on-tree ripening of eight plum cultivars. J. Sci. Food Agric. 88, 2499–2507. Ercisli, S., Guleryuz, M., Esitken, A., 1999. A study on the fruit properties of native quince cultivars in Oltu. Anadolu 9, 32–40. Ercisli, S., Gozlekci, S., Sengul, M., Hegedus, A., Tepe, S., 2012. Some phytochemical characteristics, bioactive content and antioxidant capacity of loquat (Eriobotrya japonica (Thunb.) Lindl.) fruits from Turkey. Sci. Hortic. 148, 185–189. FAOSTAT, 2012. Food and Agriculture Organization of the United Nations [FAO]. STATistics 2012. Available at: http://faostat.fao.org/site/339/default.aspx (accessed 19.01.12). Fattouch, S., Caboni, P., Coroneo, V., Tuberoso, C., Angioni, A., Dessi, S., Marzouki, N., Cabras, P., 2007. Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts. J. Agric. Food Chem. 55, 963–969. Fiorentino, A., D’Abrosca, B., Pacifico, S., Mastellone, C., Piscopo, V., Caputo, R., Monaco, P., 2008. Isolation and structure elucidation of antioxidant polyphenols from Quince (Cydonia vulgaris) peels. J. Agric. Food Chem. 56, 2660–2667. Hamauzu, Y., Yasui, H., Inno, T., Kume, C., Omanyuda, M., 2005. Phenolic profile, antioxidant property, and anti-influenza viral activity of Chinese quince (Pseudocydonia sinensis Schneid.), quince (Cydonia oblonga Mill.), and apple (Malus domestica Mill.) fruits. J. Agric. Food Chem. 53, 928–934.
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Quality parameters, biocompounds and antioxidant activity in fruits of nine quince (Cydonia oblonga Miller) accessions Pilar Legua a , María Serrano b,∗ , Pablo Melgarejo a , Daniel Valero c , Juan José Martínez a , Rafael Martínez a , Francisca Hernández a a
Department of Plant Science and Microbiology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain Department of Applied Biology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain c Department of Food Technology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain b
a r t i c l e
i n f o
Article history: Received 27 November 2012 Received in revised form 13 February 2013 Accepted 18 February 2013 Keywords: Antioxidant activity Carotenoids Crude fiber Phenols Quality
a b s t r a c t Quality parameters, as well as bioactive compounds and antioxidant activity were determined in nine quince (Cydonia oblonga Miller) clones belonging to the quince gene bank of the University Miguel Hernández (Alicante, Spain). Significant differences were found among quince clones in fruit weight, firmness, total soluble solids (TSS), total acidity (TA), crude fiber and sensory attributes. Bioactive compound concentration and total antioxidant activity, in both hydrophilic (H-TAA) and lipophilic (L-TAA) extracts, were also found to be different in flesh and skin among quince clones. High correlations were found between total phenolics and H-TAA and total carotenoids and L-TAA, showing that phenolics and carotenoids are the main compounds responsible for hydrophilic and lipophilic antioxidant activity, respectively. The quince clones with the highest content on bioactive compounds and antioxidant activity in the edible portion were AM4, CTM8 and OM6. In addition, AM4 and OM6 accessions had low astringency levels and an equilibrated TSS/TA ratio, leading them also appropriated for fresh consumption. Thus, these accessions could be used, together with other having large fruits as ZM6 accession, to select new cultivars with high yield, and overall fruit quality attributes and specially having high content of bioactive compounds with antioxidant activity and health benefits. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Quince (Cydonia oblonga Miller) is used extensively in Europe as a dwarfing rootstock for pear. Total world production of fresh fruit quince in 2010 was 540.337 tons, from which 14.200 tons were produced in Spain (FAOSTAT, 2012). The quince tree shows high genetic variability, with more than 30 different cultivars in Europe, 19 in USA and 86 in the old USSR being described by Scaramuzzi (1957), which were often mistaken by farmers due to the high number of synonyms, polymorphism of fruits and leaves and the existence of many trees propagated by seeds. Likewise, several authors have studied the genetic variability in this species worldwide (Shao and Lu, 1995; Ercisli et al., 1999; Srivastava et al., 2005; Rodríguez-Guisado et al., 2009). Quince fruit at un-ripe stage is not very appreciated for fresh market due to pulp hardness, bitterness and astringency, but when ripe, quince has pleasant, lasting and powerful flavor. Nevertheless, quince is intended primarily to the manufacture of marmalade, jams, jelly and cakes (Silva et al., 2002, 2005, 2006; Sharma et al.,
∗ Corresponding author. Tel.: +34 966749616; fax: +34 966749678. E-mail address: [email protected] (M. Serrano). 0304-4238/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scienta.2013.02.017
2011). Quince has low fat content and is an important source of organic acids, sugars, crude fiber and minerals like potassium, phosphorous and calcium, as well as of health-promoting constituents, such as phenolic compounds with antioxidant activity (Silva et al., 2004a, 2004b; Fattouch et al., 2007; Rodríguez-Guisado et al., 2009) and it is known to have hypoglycemic, anti-inflammatory, anticarcinogenic, antimicrobial, anti-allergic and antiulcerative properties and act as a tonic for heart and brain (Hamauzu et al., 2006; Fattouch et al., 2007; Shinomiya et al., 2009). Since native quince resources are almost vanished nowadays in Spain, the Plant Science and Microbiology Department (Miguel Hernandez University, UMH) collaborated in the establishment of a gene bank with a total of 87 quince accessions in 1995 (GENRES29CT95) with a wide genetic variability. Thus, the general aim of this research was to perform the morphological and quality characterization of quince fruits from 9 of these accessions, and to determine their content on bioactive compounds (polyphenols and carotenoids) and the total antioxidant activity (TAA), measured by the first time in quince fruit in the hydrophilic (H-TAA) and lipophilic (L-TAA) fractions separately, in the skin and flesh. The results will provide information about the potential interest of these accessions to fresh fruit consumption or to made products such as jam and jelly, with high content on bioactive
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compounds and health benefits. In addition, results would help breeders to select new cultivars based on the overall fruit quality, taking into account not only the external fruit quality or nutritional and organoleptic properties, but also considering the content of bioactive compounds and antioxidant activity, and thus to fulfill consumer’s wishes through the fruits with high health benefits.
following the official methodology established by the Spanish Ministry of Agriculture, Fisheries and Food as described by Rodríguez-Guisado et al. (2009) and results expressed as % in a fresh weight basis.
2.3. Total antioxidant activity determination (TAA) 2. Materials and methods 2.1. Plant material Nine quince clones (AM4, CTM7, CTM8, CTM10, MOM1, OHM4, OM6, ZM4 and ZM6) were used in this research, all of them with high agronomic properties and fruits with high quality, being appropriated for fresh market and processing (unpublished previous results). The selected plant materials belong to the gene bank quince located at the experimental field station of Miguel Hernández University in the province of Alicante, Spain (02◦ 03 50 E, 38◦ 03 50 N, and 25 mals). Trees were planted at a spacing of 4 m × 3 m. Standard cultural practices (pruning, thinning, fertilization and treatments) were performed. The experiment was established in a randomized block design with four single-tree replications and grafted onto quince BA-29 rootstock. Guard rows were used to preclude edge effects. Fruits were harvested at commercial ripening stage at the end of September and first October and 20 homogeneous fruits (based on color, size and absence of defects) were selected from each clone (5 fruits from each tree) for analytical determinations. Thus, since quince trees were under homogeneous growing conditions and fruits harvested at similar ripening stage, results are valid for comparative purposes. The study was conducted twice in the years 2008 and 2009 and results are the mean ± SE of two years. 2.2. Fruit morphological and quality parameters Fruit weight and firmness were determined individually in 20 fruits (in both 2008 and 2009 years) by using a digital balance Sartorius (model BL-600, 0.01 g accuracy, Goettingen, Germany) and a Bertuzzi Penetrometer (model FT-327, Facchini, Alfonsine, Italy), equipped with an 8 mm cylindrical plunger, respectively and data are the mean ± SE. Firmness measurements were performed on two opposite faces in the equatorial zone (where the skin was removed) and results were expressed in kg force (kgf) cm−2 . After that, 4 subsamples of 5 fruits (from the 4 tress or replicates) were performed for the following analytical determinations. They were hand-peeled and skin and pulp were cut in small pieces to obtain homogeneous samples in which the following parameters were determined in duplicate. From pulp samples 10 g were used for total soluble solids (TSS) and total acidity (TA) determination, and 2 g for total fiber quantification. The remaining flesh samples as well as the skin samples were immediately frozen and ground in liquid N2 and stored in freezer at −40 ◦ C until analysis of total phenolics, total carotenoids and total antioxidant activity (TAA) was carried out. For TSS and TA determination 10 g of pulp samples were squeezed using a commercial blender and the extracted juice was later sieved and centrifuged at 8000 × g for 20 min (Sigma 3–18 K, Osterode and Harz, Germany). An aliquot of this supernatant was used to determine TSS with a digital refractometer Atago PAL-1 (Atago Co. Ltd., Tokyo, Japan) at 20 ◦ C, and expressed as percentage (◦ Brix). TA was determined in 1 mL of the above supernatant diluted in 25 mL of distilled water by titration with 0.1 N NaOH up to pH 8.1, using an automatic titration device (877 Titrino plus, Metrohm ion analyses CH9101, Herisau, Switzerland) and results expressed as g of malic L−1 . Maturity index (MI) was calculated as the ratio between TSS and TA. Crude fiber content was quantified
TAA was quantified according to Díaz-Mula et al. (2008) which enables to determine TAA due to both hydrophilic and lipophilic compounds in the same extraction. Briefly, for each sub-sample, 5 g of pulp or 1 g of skin were homogenized in 5 mL of 50 mM phosphate buffer pH = 7.8 and 3 mL of ethyl acetate, then centrifuged at 10,000 × g for 15 min at 4 ◦ C. The upper fraction was used for TAA due to lipophilic compounds (L-TAA) and the lower for TAA due to hydrophilic compounds (H-TAA). In both cases, TAA was determined using the enzymatic system composed of the chromophore 2,2 -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), the horse radish peroxidase enzyme (HRP) and its oxidant substrate (hydrogen peroxide), in which ABTS+• radicals are generated and monitored at 730 nm. The decrease in absorbance after adding the extract was proportional to TAA of the sample. A calibration curve was performed with Trolox ((R)-(+)-6-hydroxy2,5,7,8-tetramethyl-croman-2-carboxylic acid) (0–20 nmol) from Sigma (Madrid, Spain), and results are expressed as mg of Trolox equivalent 100 g−1 .
2.4. Total phenolics and total carotenoids determination Total phenolics were extracted according to Tomás-Barberán et al. (2001) using water:methanol (2:8) containing 2 mM NaF and quantified using the Folin–Ciocalteu reagent (Singleton et al., 1999) and results (mean ± SE) were expressed as mg gallic acid equivalent 100 g−1 fresh weight. Total carotenoids were extracted and quantified as described by Díaz-Mula et al. (2008). Briefly, 1 g of skin or 2 g of flesh tissues were extracted with acetone and shaken with diethyl ether and 10% NaCl to separation of the two phases. The lipophilic phase was washed with Na2 SO4 (2%), saponified with 10% KOH in methanol, and the pigments were subsequently extracted with diethyl ether, evaporated and then made up to 25 ml with acetone. Total carotenoids were estimated by reading the absorbance at 450 nm in a UNICAM Helios-␣ spectrophotometer (Cambridge, UK), and expressed as mg of -carotene equivalent 100 g−1 fresh weight, taking into account the ε1% cm = 2560 and the results were the mean ± SE.
2.5. Sensorial analysis Five fruits from each clone were used to evaluate both pulp astringency and chewiness by a sensory panel of 10 expert tasters. Pulp astringency was evaluated as high or low and chewiness as hard, semi-soft or soft and results expressed as percentage of panelist giving each classification.
2.6. Statistical analysis Statistical analyses were performed using the SPSS 18.0 for Windows (SPSS Science, Chicago, IL, USA). All data were subjected to basic descriptive statistics, and then evaluated by an analysis of variance (ANOVA) for mean comparisons. Fisher’s least significant difference test (LSD at 95.0% of confidence level) was applied for mean values discrimination.
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Table 1 Quality and sensory parameters of quince fruit clones. Results are the mean of data obtained from 2008 to 2009 years. Clone
AM4 CTM7 CTM8 CTM10 MOM1 OHM4 OM6 ZM4 ZM6
Fruit weight (g)
276.0a 331.5bc 269.3a 267.4a 354.1c 280.7ab 265.4a 377.2cd 415.9d
Pulp firmness (Kgf cm−2 )
9.55e 7.76d 4.73a 6.00bc 9.85e 6.56c 5.41ab 6.02bc 5.81bc
TSS (◦ Brix)
18.63e 15.60cd 14.60abc 16.07bcd 16.63d 15.00bc 13.97ab 13.40a 13.53ab
TA (g malic acid L−1 )
9.54d 7.10b 8.56cd 7.65bc 5.28a 6.48ab 7.17bc 7.15bc 6.76b
Crude fiber (%)
1.46cd 1.17ab 1.35bcd 1.63d 1.20abc 1.55d 1.11ab 1.33bcd 0.93a
Pulp astringency (%)
Pulp chewiness (%)
High
Low
Hard
20 50 70 70 60 50 30 30 90
80 50 30 30 40 50 70 70 10
100
Semi-soft
Soft
90 70 80
10 30 20
90 75 80 70
10 25 20 30
100
For each parameter, values within the same columns followed by different letters were significantly different (p < 0.05).
3. Results and discussion
3.2. Bioactive compounds and total antioxidant activity (TAA)
3.1. Quality parameters
Total phenolic content, total carotenoid concentration and TAA were measured in flesh and sink, the TAA being measured by the first time separately in hydrophilic (H-TAA) and lipophilic (L-TAA) fractions. Results revealed significant differences among quince accessions and between flesh and skin tissues (Figs. 1–4) showing that plant genetic background is an important factor responsible for differences among quince clones in the concentration of bioactive compounds, according to previous reports in other fruit species, such as plum (Díaz-Mula et al., 2008), loquat (Ercisli et al., 2012) or pomegranate (Caliskan and Bayazit, 2012). Thus, total phenolic concentration ranged from 40 to 100 mg 100 g−1 in the flesh, for M0M1 and AM4 accessions, respectively (Fig. 1) and from 200 to 430 mg 100 g−1 in the skin, for CTM8 and CTM10, respectively (Fig. 2). Thus, given the health beneficial effects of phenolics compounds, those fruits with high phenolics concentration will be advisable for degenerative illness prevention (Haminiuk et al., 2012). These phenolic concentrations are high as compared to that found in other fruits of the Mediterranean diet (Hamauzu et al., 2005; Valero and Serrano, 2010). In quince fruits harvested from different regions of Portugal, the main phenolic compounds in flesh were 5-O-caffeoylquinic (chlorogenic) acid and 3-O-caffeoylquinic (neochlorogenic) acid while in peel the most abundant phenolic was quercitin-3-O-rutinoside (rutin) followed by 3-O- and
Fruit weight ranged from 265 to 416 g, the clones OM6, CTM10, CTM8 and AM4 having the lowest fruit weight and the clone ZM6 the highest (Table 1). Accordingly, a great variability on fruit weight has been reported in other Spanish quince tree clones (RodríguezGuisado et al., 2009) as well as in Turkish (Yarlgac, 2001) and Indian ones (Srivastava et al., 2005). However, the Turkish ‘Katirbasi’ quince showed fruit weight ranging from 470 g to 530 g (Ercisli et al., 1999), similar to that of the clone ZM6 and even fruits weighting from 600 g to 1200 g have been reported in the ‘Jianchuan 1’ Chinese cultivar (Shao and Lu, 1995). Remarkable differences were also found among quince clones in fruit firmness (Table 1). AM4 and MOM1 scored the highest pulp firmness (9.55 and 9.85 kgf cm−2 , respectively) followed by CTM7 (7.76 kgf cm−2 ), while the lowest pulp firmness was scored by CTM8 (4.73 kg cm−2 ). These firmness values are quite high when compared to Turkish cultivars (Ercisli et al., 1999), showing that Spanish clones are firmer than Turkish varieties. However, the content in crude fibber (%) was quite similar among clones (Table 1), the clone ZM6 showing the lowest crude fiber content (0.93%) and the clone CTM10 the highest (1.63%). These values agree with obtained ones for the variety Indian ‘Plate 1’ cultivar (Sharma et al., 2011), while in other Spanish clones fiber content ranged from 1.7 to 8.1% (Rodríguez-Guisado et al., 2009). The evaluation of total soluble solids content (TSS) and total acidity (TA) also established significant differences among evaluated clones (Table 1), with values of TSS ranging from 13.40 (ZM4) to 18.63 ◦ Brix (AM4) and TA ranging from 5.28 (MOM1) to 9.54 g L−1 (AM4), according to previous reports in other quince accessions (Ercisli et al., 1999; Rodríguez-Guisado et al., 2009; Sharma et al., 2011). These variations in TSS and TA led to great differences in ripening index, which ranged from 17.15 in CTM8 clone to 32.22 in MOM1 one, affecting greatly to quince taste and flavor, since they depend more of the TSS/TA ratio that of the TSS or TA considered independently (Crisosto et al., 2007). Glucose and fructose have been reported as the main sugars in quince fruits, followed by sucrose and maltose, while malic plus quinic acids are the main organic acids followed by citric, tartaric, acetic and ascorbic acids in minor concentrations (Silva et al., 2004a, 2005; Rodríguez-Guisado et al., 2009). According to the sensory panel, all evaluated clones were considered as semi-soft with the exception of the clones AM4 and MOM1, which were classified as hard by all the panelists. With respect to pulp astringency, most of the clones were scored as having high astringency, with the exception of the clones AM4, OM6 and ZM4, which were scored as low pulp astringency, by most of the panelists, and therefore they could be considered good for fresh consumption. Rodríguez-Guisado et al. (2009) reported that other Spanish clones were predominantly scored as low pulp astringency and considered as semi-soft pulp.
Fig. 1. Total phenolics (mg 100 g−1 ) and hydrophilic total antioxidant activity (HTAA, mg 100 g−1 ) in the flesh of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
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700
y= 46x -81.56, r =0.927
600
Total Phenolics H-TAA
H-TAA
Phenolics and H-TAA in the Skin (mg 100 g -1)
64
600
500 400 300
C
200
500
200
250
300
c
350
Phenolics
e
400 d
300
A
200
d
D
a a A
b
b B
400
E
D AD
d
B
100
7 8 4 10 0M1 HM4 AM CTM CTM CTM 0 M
6 OM
4 ZM
6 ZM
Fig. 2. Total phenolics (mg 100 g−1 ) and hydrophilic total antioxidant activity (HTAA, mg 100 g−1 ) in the skin of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
5-O-affeoylquinic acids (Silva et al., 2005) as well as in the cv Smyrna from Japan (Hamauzu et al., 2006). Great differences were also found in H-TAA of flesh and skin among quince accessions (Figs. 1 and 2), and high correlations were found between total phenolic concentration and H-TAA (r2 = 0.983 and 0.927, for flesh and skin, respectively), showing that phenolics are the main hydrophilic compounds with antioxidant activity in skin and flesh quince tissues. Specifically, it has been shown that chlorogenic acids and the flavonols quercitine and its 3-O-rutinoside exhibited the highest antioxidant and antiradical scavenging capacity in quince peel and flesh (Silva et al., 2004b; Fiorentino et al., 2008). However, Fattouch et al. (2007) reported that pulp and peel quince extracts had higher antioxidant activity that the sum of those of the individual phenolic compounds, showing the synergistic effect of the individual antioxidants. Moreover, it has been also shown that quince phenolics have antioxidant activity in vivo, since they increased the antioxidant capacity of
Fig. 3. Total carotenoids (mg 100 g−1 ) and lipophilic total antioxidant activity (LTAA, mg 100 g−1 ) in the flesh of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case o capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
Fig. 4. Total carotenoids (mg 100 g−1 ) and lipophilic total antioxidant activity (LTAA, mg 100 g−1 ) in the skin of different quince fruit clones. Bars (mean value ± SE of data from 2008 to 2009 years) with different case of capital letters showed significant differences among quince clones (p < 0.05). Inset linear regression among both parameters.
blood after oral administration to rats, as well as suppressed the occurrence of gastric lesions (Hamauzu et al., 2006). In addition, the bacteriostatic and bactericide activities of quince pulp and peel extracts have been also attributed to their main phenolic compounds (Fattouch et al., 2007). Total carotenoid concentration was higher in peel than in flesh and significant differences were found among quince accessions in both tissues. Thus, in flesh tissue, the highest carotenoid concentration in flesh was found in MOM1 accession and the lowest in ZM6, with values ≈0.42 and 0.04 mg 100 g−1 , respectively (Fig. 3), while in skin carotenoid ranged from ≈0.16 mg 100 g−1 in CRM8 to ≈0.86 mg 100 g−1 in AM4 (Fig. 4). Thus, no correlation was found between carotenoid concentration in skin and flesh in these quince accessions, showing that flesh coloration was independent of skin one. However, L-TAA followed the same pattern that carotenoid concentration, and in fact, high correlations were found between both parameters in flesh and skin tissues (Figs. 3 and 4), showing that carotenoids are the main lipophilic compounds with antioxidant activity as previously found in other fruits as sweet cherries, plums, peaches and nectarines (Díaz-Mula et al., 2008; Legua et al., 2011; Valero et al., 2011). In addition, it is interesting to point out that the H-TAA was higher than LTAA in both flesh and skin in all quince accessions, the H-TAA contributing to more than 90% of flesh antioxidant activity in all of them, except in MOM1 in which contributed by 73%, while in skin tissue H-TAA was 80–90% of the total antioxidant activity in all quince accessions. No previous reports are available for comparative purposes, since in previous papers, only antioxidant activity due to hydrophilic compounds has been addressed for quince fruits (Fattouch et al., 2007; Fiorentino et al., 2008; Silva et al., 2004b), and this is the first time that antioxidant activity in both hydrophilic and lipophilic extracts has been measured separately in quince fruits. Finally, it has been indicated that the content of phenolics compounds did not change during jam processing, although caffeoylquinic acid isomeration occurred (Silva et al., 2004b). Thus, those quince clones having fruits with high concentrations of bioactive compounds would lead to jam, jelly or marmalades also enriched with health beneficial compounds. In addition, since in the manufacture processing of these products only pulp is used, the peel and seed could be used as potential sources of antioxidants for use in food and pharmaceutical industry.
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4. Conclusion Taking into account that flesh tissue is the edible portion of quince fruit and that in quince processing to made marmalade, jams or jelly only flesh tissue is used, the quince clones with the highest health beneficial properties due to their content in bioactive compounds and antioxidant activity could be AM4, CTM8 and OM6. In addition, AM4 and OM6 accessions had low astringency levels and an equilibrated TSS/TA ratio, leading them also appropriated for fresh consumption. Thus, these accessions could be used, together with other having large fruits as ZM6 accessions, to select new cultivars with high yield, and overall fruit quality attributes and specially having high content of bioactive compounds with health benefits. References Caliskan, O., Bayazit, S., 2012. Phytochemical and antioxidant attributes of autochthonous Turkish pomegranates. Sci. Hortic. 147, 81–88. Crisosto, G.M., Crisosto, C.H., Echeverría, G., Puy, J., 2007. Segregation of plum and pluot cultivars according to their organoleptic characteristics. Postharvest Biol. Technol. 44, 271–276. Díaz-Mula, H.M., Zapata, P.J., Guillén, F., Castillo, S., Martínez-Romero, D., Valero, D., Serrano, M., 2008. Changes in physicochemical and nutritive parameters and bioactive compounds during development and on-tree ripening of eight plum cultivars. J. Sci. Food Agric. 88, 2499–2507. Ercisli, S., Guleryuz, M., Esitken, A., 1999. A study on the fruit properties of native quince cultivars in Oltu. Anadolu 9, 32–40. Ercisli, S., Gozlekci, S., Sengul, M., Hegedus, A., Tepe, S., 2012. Some phytochemical characteristics, bioactive content and antioxidant capacity of loquat (Eriobotrya japonica (Thunb.) Lindl.) fruits from Turkey. Sci. Hortic. 148, 185–189. FAOSTAT, 2012. Food and Agriculture Organization of the United Nations [FAO]. STATistics 2012. Available at: http://faostat.fao.org/site/339/default.aspx (accessed 19.01.12). Fattouch, S., Caboni, P., Coroneo, V., Tuberoso, C., Angioni, A., Dessi, S., Marzouki, N., Cabras, P., 2007. Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts. J. Agric. Food Chem. 55, 963–969. Fiorentino, A., D’Abrosca, B., Pacifico, S., Mastellone, C., Piscopo, V., Caputo, R., Monaco, P., 2008. Isolation and structure elucidation of antioxidant polyphenols from Quince (Cydonia vulgaris) peels. J. Agric. Food Chem. 56, 2660–2667. Hamauzu, Y., Yasui, H., Inno, T., Kume, C., Omanyuda, M., 2005. Phenolic profile, antioxidant property, and anti-influenza viral activity of Chinese quince (Pseudocydonia sinensis Schneid.), quince (Cydonia oblonga Mill.), and apple (Malus domestica Mill.) fruits. J. Agric. Food Chem. 53, 928–934.
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