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POST-HARVEST QUALITY, PHYTOCHEMICALS AND ANTIOXIDANT
CAPACITY IN ORGANIC AND CONVENTIONAL KIWIFRUIT (ACTINIDIA
DELICIOSA, CV. HAYWARD)
L. D’EVOLI 1, S. MOSCATELLO 2, A. BALDICCHI 3 , M. LUCARINI 1, J. G.
CRUZ-CASTILLO4, A. AGUZZI 1, P. GABRIELLI 1, S. PROIETTI 2, A.
BATTISTELLI 2, F. FAMIANI 3, V. BÖHM 5 AND G. LOMBARDI-BOCCIA 1*
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National Research Institute on Food and Nutrition – Via Ardeatina 546, Roma (Italy);
Institute of Agro-environmental and Forestry Biology, CNR – V.le Marconi 2, Porano
(Italy); 3Department of Agricoltural and Environmental Science, University of Perugia –
Borgo XX Giugno 74, (Italy); 4Universidad Autónoma Chapingo. Huatusco -Veracruz
(Mexico); 5Institute of Nutrition, Friedrich Schiller University – Jena (Germany)
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Corresponding author:
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*Dr. Ginevra Lombardi-Boccia
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National Research Institute on Food and Nutition
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Via Ardeatina 546 , 00178 – Roma (Italy)
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e-mail: lombardiboccia@inran.it
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Tel. 06 51494 446; Fax: 06 51494 550
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ABSTRACT
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Quality attributes, bioactive molecules, antioxidant capacity of organic and conventional
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kiwifruit grown in 2 localities (Velletri, Cori) of PGI “Kiwi-Latina” area were studied.
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Despite organic orchards showed a lower yield than conventional ones, fruit quality
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characteristics (weight, firmness, soluble solids, titratable acidity, carbohydrates) were
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better in organic kiwifruit. Higher concentrations (p<0.05) of lutein (Velletri orchard) and
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ß-carotene (Cori orchard) were detected in organic kiwifruit compared to the conventional
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ones. Tocopherols content was similar in both the cultvation systems. Ascorbic acid
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content was significantly higher (p<0.001) in organic kiwifruit. The antioxidant capacity
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was significantly higher (p<0.001) in organic kiwifruit, mirroring the trend reported for
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ascorbic acid content.
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Key words: antioxidant capacity, carotenoids, cultivation systems, kiwifruit, oxalic acid,
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tocopherols.
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INTRODUCTION
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Kiwifruit [Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var deliciosa,
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cultivar Hayward] is grown in both the northern and southern hemispheres and Italy is the
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world's largest producer (TESTOLIN and FERGUSON, 2009). Kiwifruit is extensively
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grown in central Italy (Lazio region), characterized by a temperate climate, favourable
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environmental conditions and high light radiation. The soil is without lime, has a neutral
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pH and is rich in nutrients and organic matter. Indeed, about 37% of the Italian kiwifruit
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production is concentrated in the Lazio region, which corresponds to about 10% of the
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world’s production (TESTOLIN and FERGUSON, 2009). The high quality and peculiarity
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of kiwifruit grown in this area led to the designation of Protected Geographical Indication
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(PGI) “Kiwi Latina” by the European Union (EU). Therefore, since 2004, it has been
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possible to certify kiwifruit produced in this area as “Kiwi Latina”. This implies that the
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fruit meets the specifications required (e.g., size, absence of visible defects and the amount
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of production: yield must be < 33 t/ha). The geographical area is thus highly suitable to
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kiwifruit cultivation which makes it easy to apply low input cultivation systems. In this
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area about 10% of the kiwifruit orchards are cultivated according to organic agricultural
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practices.
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Few data are available in the literature comparing kiwifruit quality from organic and
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conventional growing systems and the data reported are not unequivocal: HASEY et al.
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(1997) found organic kiwifruit firmer than the conventional, whereas no differences were
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observed in the soluble solids content. BENGE et al. (2000) reported that conventional
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kiwifruit at harvest, even with the same firmness as organic fruit, had higher soluble solids
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contents, whereas softening and incidence of decay did not differ between the two
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cultivation systems. Recently, AMODIO et al. (2007) found lower flesh firmness and
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higher soluble solids contents in organically grown fruit with respect to those
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conventionally grown in California (USA). Furthermore, organic kiwifruit was richer in
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minerals, ascorbic acid and total phenols than conventional kiwifruit, whereas there were
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no differences in sugar and other organic acid content (AMODIO et al. 2007). The
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physicochemical features (BELTRAMO et al., 2007) and the nutritional quality in relation
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to vine training system and genotype (D’EVOLI et al., 2009) of kiwifruit conventionally
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grown in the Lazio region (area of PGI “Kiwi Latina”) have already been described. At
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present, however, no data are available on the quality of kiwifruit organically grown in the
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PGI “Kiwi Latina” Area. This study was designed to analyse the yield and the
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physicochemical characteristics (weight, firmness, soluble solids, titratable acidity) of
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kiwifruit (cv. Hayward) and to define a comprehensive profile of the major phytochemicals
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of organic kiwifruit grown in the “Kiwi Latina” PGI area (Velletri, Cori), comparing them
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with those conventionally grown in the same area. Kiwifruit were analysed for their
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proximate composition, carbohydrate profile, organic acids (citric, malic, ascorbic, oxalic)
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and oxalic acid content; furthermore the concentration of bioactive molecules like
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carotenoids (lutein and ß-carotene), tocopherols (α-tocopherol, γ-tocopherol, γ-tocotrienol)
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and ascorbic acid was also quantified. Kiwifruit from both cultivation systems were also
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evaluated for the expression of their antioxidant capacity.
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MATERIALS AND METHODS
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Vine and orchard characteristics and management
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The study was carried out in two kiwifruit farms of organic and conventional kiwifruit
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orchards in the locality of Velletri and Cori, in the PGI “Kiwi Latina” area. The area is
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very suitable for the cultivation of kiwifruit because the climate is mild (frost is rare during
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spring and autumn) and temperatures during winter are never dangerous for the vines.
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Yearly rainfall ranges from 800 to 1200 mm. The wind speed is rarely dangerous. The soils
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of both orchards were fertile and suitable for kiwi production. They were of medium-clay
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texture in Velletri and of clay texture in Cori, and all of them had a pH around neutrality,
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absence of limestone or present in trace amounts and medium-high nutrient (N, K, P, Mg,
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Ca, Fe) levels.
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Both organic and conventional orchards were made up of mature vines of the cv. Hayward,
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with cv. Matua as pollinizer. The vines were trained to the pergolette system. In both
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orchards, vines were irrigated with a drip irrigation system, ensuring full resupplying of
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evapo-transpiration (Etc). Cultural practices in conventional and organic orchards differed
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for the fertilisers used, and for the use in conventional cultivation of “Dormex” (hydrogen
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cyanamide), to enhance bud breaking. Moreover, in the Velletri conventional orchard
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CPPU [N-(2-chloro-4-pyridyl)-N'-phenylurea - a synthetic cytokinin-like substance] was
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also used to promote fruit growth. Fertilization was carried out to ensure a full resupplying
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of the nutrients taken up, by use of chemical fertilisers in conventional orchards and
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organic fertilisers in organic orchards.
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Harvesting and post-harvest storage of kiwifruit
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At harvesting (end of October), the yield/orchard (expressed as t/ha) was determined and
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recorded when the fruit soluble solids content was around 7 °Brix. After harvesting,
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kiwifruit was stored in normal atmosphere at T = 00.5 °C and RH > 90% for about 5
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months.
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Fruit weight, flesh firmness and soluble solids content
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Fruit weight was determined by weighing 100 fruits per orchard. Fruit flesh firmness was
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determined on 100 fruits per orchard with a hand-held penetrometer (Effe.gi, Ravenna,
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Italy) with an 8 mm plunger, after removal of about 1 cm2 of skin. The same 100 fruits
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were also used to determine the soluble solids content, as °Brix, by taking a juice sample
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from the equatorial part of each fruit using a hand-held refractometer (Model M, Atago,
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Japan). Fruit dry matter content was determined on 40 fruits by drying them at 105 °C in a
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forced air oven to constant weight (AOAC, 1996).
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Preparation of fruit powder
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A fruit powder was prepared for titratable acidity, carbohydrates, oxalic acid, citric and
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malic acids analyses. Four samples per orchard were prepared, each composed of sub-
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samples (segments) of 8 fruits: hair and epidermis were removed by scratching the surface
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of each fruit with a sharp knife, then a segment representative of all the fruit tissues (outer
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and inner pericarp and columella) was removed from each fruit and rapidly frozen in liquid
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N2. Samples were stored at -80°C. The frozen samples were ground to a fine powder under
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liquid N2 (nitrogen powder) in a pre-cooled mortar and stored at -80 °C until analysis.
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Titratable acidity
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Five grams of the fruit powder were dissolved in 10 mL of distilled water. Titratable
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acidity was determined by titrating the solution with 0.1 N NaOH to a pH of 8.2; results
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are expressed as g of citric acid per kg of fruit.
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Carbohydrates
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Fifty mg of the fruit powder were extracted as described by FAMIANI et al. (2009).
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Samples were then centrifuged and the supernatant was immediately analysed for glucose,
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fructose and sucrose and the pellet, containing starch, was re-suspended and processed as
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described in ANTOGNOZZI et al. (1996) in order to completely hydrolyse the starch to
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glucose. Contents of glucose, fructose and sucrose were determined using an enzyme-
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coupled spectrophotometric method as described by JONES et al. (1977), with minor
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modifications as described by ANTOGNOZZI et al. (1996).
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Citric and malic acids
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The citric and malic acid contents were determined using an enzyme-coupled
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spectrophotometric method as described by LOWRY and PASSONNEAU (1972) using
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the same extracts used to determine the soluble sugars content.
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Oxalic acid
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One hundred mg of the fruit powder were extracted in 1.5 mL of distilled water. Samples
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were then processed as describes by PROIETTI et al. (2010) in order to extract both
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soluble and insoluble oxalic acid. Oxalic acid was determined using the enzymatic assay
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described by BEUTLER et al. (1980).
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Proximate analysis
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Protein, lipid and ash were determined according to AOAC methods (1996). The analyses
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were carried out on triplicate.
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Total dietary fiber
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Total dietary fiber was determined following the method of PROSKY et al. (1988). The
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analyses were carried out on triplicate.
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Minerals and bioactive molecules
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For minerals, micronutrients (trace elements, carotenoids, tocopherols, ascorbic acid) and
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antioxidant capacity analyses, it was necessary to make up a pool (GREENFIELD and
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SOUTHGATE, 2003). About 5 kg of kiwifruit from each orchard were transported to the
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laboratory. Equal amounts of defect-free kiwifruit were randomly grouped into 4 batches
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per orchard. Each batch was homogenized and aliquots were taken for subsequent
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analyses.
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Minerals and trace elements: minerals (Ca, Mg, Na, K, P) and trace element (Fe, Zn, Cu,
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Mn, Se) content were determined by ICP-Plasma (Optima 3200 - Perkin-Elmer) following
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liquid ashing (4 mL HNO3+1 mL H2O2) of the samples in a microwave digestion system
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(Milestone, 1200 Mega). Standard Reference Materials: Mixed diet (NBS 8431, National
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Bureau of Standards, Gathersburg, MD 20899) and Wholemeal flour (BCR 189,
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Community Bureau of Reference, Brussels) were analysed as a check on the accuracy of
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the analysis.
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Carotenoids: ß-carotene and lutein were extracted and quantified by HPLC following the
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method of SEYBOLD et al. (2004).
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Tocopherols: α-tocopherol, γ-tocopherol, γ-tocotrienol were extracted and quantified using
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a HPLC/fluorescence detector as described by BALTZ et al. (1992).
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Ascorbic acid: was determined according to the method of VALLS et al. (2002). Total
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ascorbic acid was determined and quantified by HPLC on an Alltima NH2 column
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(0.46x25cm, Alltech) at 248 nanometers with a photodiode array detector (HPLC/PDA)
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referring to the ascorbic acid standard calibration curve.
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Antioxidant capacity: the antioxidant capacity of kiwifruit was determined by FRAP assay
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(BENZIE and STRAIN, 1996). Results are expressed as mmol Trolox equivalent (TE) kg.
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To evaluate the antioxidant capacity a kiwifruit crude extract was prepard as described by
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MEYERS et al. (2003).
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Statistics
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Data are reported as the MeanStandard Deviation of at least three independent analyses.
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Statistical analysis was performed utilizing the Student’s t-test to compare organic and
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conventional samples; only results significant at p<0.05 are discussed.
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RESULTS AND DISCUSSION
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Yield, physicochemical characteristics and proximate composition of kiwifruit from both
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organic and conventional orchards are reported in Table 1. The organic growing system
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showed a lower yield than that of the conventional one: 30.0 vs 56.0 t ha-1 in Velletri and
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17.0 vs 33.5 t ha-1 in Cori (Table 1). A lower yield from the organic system compared to
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the conventional one was also observed by AMODIO et al. (2007), even if to a lower
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extent (-16%). This has also been reported for other fruit species such as apple and olive
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(PECK et al., 2006; NINFALI et al., 2008; ROUSSOS and GASPARATOS, 2010). The
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lower yields may be attributed to the restrictions in the use of agronomical inputs in
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organic cultivation. Indeed, in the present study the use of Dormex in conventional
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orchards (not allowed in organic cultivation) was probably the factor that greatly improved
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fruit production by increasing bud-breaking (INGLESE et al., 1998). Moreover, in Velletri,
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the use of CCPU (a synthetic cytokinin-like substance able to strongly increase fruit
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growth), contributed in increasing the orchard’s yield. Fruit weight was similar in both
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organic and conventional orchards in Cori, whereas it was higher in the conventional
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orchards in Velletri (Table 1). The higher fruit weight of the conventional Kiwifruit in
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Velletri, despite the highest yield ha-1 of this orchard (which is generally inversely related
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to fruit weight), can be explained by the use of CPPU (Antognozzi et al., 1996; Famiani et
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al., 1999). Dry matter and soluble solids contents, total titratable acidity and flesh firmness
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were significantly higher (p<0.05) in organic kiwifruit than in conventional fruit (Table 1).
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AMODIO et al. (2007) reported a soluble solids content similar to those found in this
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study, whereas flesh firmness showed an opposite trend. Other studies did not find
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differences in flesh firmness between organic and conventional kiwifruit (HASEY et al.,
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1997; BENGE et al., 2000). Fruit firmness can be affected by several factors, such as
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fertilization (JOHNSON et al., 1997), light exposure (ANTOGNOZZI et al., 1995) calcium
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content (FRANCESCHI and NAKATA, 2005) and dry matter content (FAMIANI et al.,
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unpublished data). The retaining of higher flesh firmness, shown by organic kiwifruit
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compared with conventional fruit after months of storage, could be due to both their higher
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dry matter content (Table 1), the better lightening (as a result of lower bud-breaking and
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consequently a lower number of shoots/vine caused by not using Dormex) and, in Velletri
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orchards also to the higher Ca content. Flesh firmness can be considered a quality index to
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establish the storability of fruit. During storage, retaining values up to 2.5 N ensures safe
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manipulation of fruit for subsequent marketing (COSTA, 2003). Hence, organic kiwifruit
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seems to have a higher quality in terms of storability. Total carbohydrate content was
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significantly higher (p<0.001) in organic orchards than in conventional ones (Table 1).
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Starch content also was significntly higher (p<0,001) in organic kiwifuit even if in very
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low amount in the ripe fruit, indicating that after 5 months of storage the fruits were fully
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ripened (Table 1). The highest carbohydrates content found in the organic kiwifruit was in
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agreement with their higher percentage of dry matter and higher soluble solids content, and
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accounted for more than 60% of the dry matter content of ripe kiwifruit. Differently from
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our findings, AMODIO et al. (2007) did not report any difference in simple sugar content
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between organic and conventional kiwifruit. Among the organic acids, malic acid content
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was significantly higher (p<0.001) in organic kiwifruit compared to the conventional ones,
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by contrast citric acid was in significanly higher (p<0.001) amount in the Cori organic
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orchard only (Table 1). AMODIO et al. (2007) did not found differences in both citric and
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malic acids content between organic and conventional kiwifruit. Oxalic acid content in
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organic kiwifruit was reported for the first time in this study. Oxalic acid was detected in
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very low amounts, organic and conventional kiwifruit differed significantly (p<0.05) only
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in the insoluble fraction content of Velletri orchards (Table1). Soluble and insoluble
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oxalate in the human and animal diet poses nutritional and health problems (Siener et al
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2003), the amounts detected in both organic and conventional kiwifruit at edible maturity
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were much lower than those found in vegetables.
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The higher values of dry matter, soluble solids, carbohydrate and organic acid (titratable
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acidity) found in organic kiwifruit may be due, at least in part, to the lower yield from this
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cultivation, which may have favoured the accumulation of higher amounts of metabolites
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in the fruit. In this study the differences in yield between organic and conventional
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orchards were considerable and this may have contributed to determining more marked
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differences between organic and conventional kiwifruit than those observed in previous
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studies (HASEY, 1997; BENGE et al., 2000; AMODIO et al., 2007).
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There were no significant differences in protein, lipid, total dietary fiber contents between
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organic and conventional kiwifruit (Tables 1). Organic and conventional kiwifruit
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significantly differed in some mineral contents only in the Velletri orchards: both Ca
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(p<0.001) and Mg (p<0.01) content was higher in organic fruits, by contrast K (p<0.001)
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content was higher in conventional ones (Table 2). Lutein was the most abundant
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carotenoid in kiwifruit (Fig. 1). Differences in lutein content between organic and
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conventional kiwifruit were significant (organic vs. conventional, p<0.05) only for fruits
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grown in the Velletri orchards (Fig. 1). By contrast, ß-carotene content was significantly
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higher (p<0.05) in organic fruits than in conventional ones grown in the Cori orchards
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(Fig. 1). The values found in this study for the carotenoids in kiwifruit were, on average,
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similar to those reported in previous studies (CANO, 1991; D’EVOLI et al., 2009), but
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lower than the values reported by NISHIYAMA (2007). A large variation in the lutein
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content in fruit was already reported by HART and SCOTT (1995). Among the
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tocopherols, α-tocopherol was the most abundant in kiwifruit (Fig. 2). In this study no
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differences in tocopherols content between organic and conventional fruit were found (Fig.
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2). The ascorbic acid content in kiwifruit is presented in Fig. 3. Other studies reported
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values of ascorbic acid for conventional kiwifruit in the range of those determined in this
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study (LEONG and SHUI, 2002; NISHIYAMA et al., 2004; DU et al., 2009). Organic
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kiwifruit had a significantly higher (p<0.001) content of ascorbic acid than conventional
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fruit (Fig.3) in both the cultivation areas. The use of ‘compost’ (rich in organic not easily
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available nitrogen) as a soil supplement has been shown to enhance ascorbic acid synthesis
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in organic fruit compared to that produced conventionally (ASAMI et al., 2003; WANG
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and LIN, 2003), probably because it induces plants to first synthesize non-nitrogen-
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containing compounds. The larger carbohydrate content in organic kiwifruit may have
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contributed to a greater synthesis of ascorbic acid (LOEWUS, 1999). Higher ascorbic acid
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contents have been found in a number of organically grown fruits (WHORTINGTON,
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2001; AMODIO et al., 2007; DUARTE et al., 2010; REGANOLD et al., 2010). Finally,
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the kiwifruit was also analyzed for expression of their antioxidant capacity measured in
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hydrophilic extracts of the fruit (Fig. 4). Values found in this study for the conventionally
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grown kiwifruit were in the range of those previously reported for kiwifruit of the PGI
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“Kiwi Latina” area (D’EVOLI et al, 2009). The antioxidant capacity mirrored the trend
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reported for ascorbic acid content: the antioxidant activity expressed by organic kiwifruit
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was significantly higher (p<0.001) than that of the conventional fruit in both the orchards
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(Fig.4). Studies carried out on several Actinidia genotypes reported a high direct
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correlation between antioxidant capacity and vitamin C and polyphenols content (DU et
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al., 2009; PARK et al., 2011). Its antioxidative properties in human cells has also been
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described (COLLINS et al., 2001).
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CONCLUSION
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Fruit is an important part of the daily human diet and its consumption greatly contributes to
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the prevention of chronic-degenerative diseases (RIBOLI and NORAT, 2003). Our
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findings showed that kiwifruit consumption could be an excellent dietary vehicle for a
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number of bioactive molecules (e.g. carotenoids, tocopherols, ascorbic acid); in particular
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the results confirmed that kiwifruit (cv. Hayward) is among the fruits with the highest
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content of lutein and its daily consumption provides an adequate vitamin C intake,
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consistent with the Recommended Daily Allowance (RDA). Furthermore, compared to the
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conventional growing system, kiwifruit with higher concentrations of some of the bioactive
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molecules (ß-carotene, ascorbic acid) was obtained in the organic growing system. On the
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other hand the agronomic practices (BOURNE and PRESCOTT, 2002; ASAMI et al,
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2003; D’EVOLI et al., 2010) are among the broad range of factors, like genotype
26
(JAAKOLA et al., 2002) and environmental conditions (THOMAS-BARBERAN et al.
12
1
2001; LOMBARDI-BOCCIA et al., 2004), that affect biosynthesis and accumulation of
2
bioactive molecules in the fruit. The antioxidant capacity is highly dependent on the
3
biological activity of a number of molecules in foods. In this study, ascorbic acid strongly
4
contributed to the highest antioxidant activity showed by organic fruit compared to
5
conventional one, representing a nutritionally active fraction of kiwifruit. Our findings also
6
showed that fruit qualitative parameters were correlated to the cropping system applied.
7
Most of the quality characteristics like flesh firmness, titratable acidity, dry matter, soluble
8
solids and sugar contents, indicated higher performances of the organic kiwifruit compared
9
to the conventional ones in terms of both fruit quality and storability. These characteristics
10
are also key factors related to sweetness and flavour of ripe fruit; thus organic kiwifruit
11
seems to have the potential for a higher sensorial quality and in turn for greater consumer
12
appreciation.
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This study was carried out as part of the Project “QUALKIWI” funded by the Italian
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Ministry for Agricultural, Food and Forestry Politics (MiPAAF).
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ACKNOWLEDGEMENTS
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