Received for publication: 29 October, 2013. Accepted for publication: 19 March, 2014. 1 Department of Chemistry, Faculty of Sciencies, Universidad Nacional de Colombia. Bogota (Colombia). cenarvaezc@unal.edu.co Agronomía Colombiana 32(2), 232-237, 2014 Antioxidant capacity and total phenolic content of air-dried cape gooseberry (Physalis peruviana L.) at different ripeness stages Capacidad antioxidante y contenido total de fenoles de uchuva (Physalis peruviana L.) secada al aire en diferentes estados de maduración Carlos Eduardo Narváez-Cuenca1, Ángela Mateus-Gómez1, and Luz Patricia Restrepo-Sánchez1 ABSTRACT RESUMEN Because the use of drying at high temperatures might negatively affect the functional properties of fruits, the effect of air-drying at 60°C on the total phenolic content (TPC) and antioxidant capacity (AOC) of cape gooseberry fruit was evaluated at three ripeness stages. The AOC was evaluated with 2,2’-azino-bis(3- ethylbenzothiazoline-6-sulfonic acid) (ABTS), ferric reduc- ing ability of plasma (FRAP), 1,1-diphenyl-2-picrylhydrazyl (DPPH), and β-carotene-linoleate assays. The TPC and AOC increased in the fresh fruit as the ripeness stage increased. The TPC increased from 401.8±19.8 to 569.3±22.3 mg GAE/100 g dry weight (DW). The AOC values obtained with ABTS in the fresh fruit (ranging from 79.4±4.5 to 132.7±12.9 µmol trolox/g fruit DW) were comparable to those obtained with FRAP (rang- ing from 82.9±16.3 to 153.9±31.7 µmol trolox/g fruit DW). The values assessed with DPPH ranged from 21.0±3.2 to 34.1±5.1 µmol trolox/g fruit DW. The β-carotene-linoleate assay gave values ranging from 5.8±1.1 to 12.7±2.0 µmol α-tocoferol/g fruit DW. Air-drying the cape gooseberry fruit had a small inf lu- ence on the TPC. The air-dried fruit had AOC values ranging from 27 to 164% of the value of the fresh fruit. While the ABTS assay produced higher values in the air-dried fruit than in the fresh fruit, the FRAP, DPPH, and β-carotene-linoleate assays resulted in lower values in the air-dried fruit. Debido a que el secado a altas temperaturas puede afectar nega- tivamente las propiedades funcionales de las frutas, se evaluó el efecto del secado con aire a 60°C sobre el contenido total de fenoles (CTF) y la capacidad antioxidante (CAO) de frutos de uchuva en tres estados de madurez. CAO se evaluó por los métodos ácido 2,2’-azino-bis(3-etilbenzotiazolin-6-sulfonico) (ABTS), habilidad reductora de hierro en plasma (FRAP), 1,1-difenil-2-picrilhidrazil (DPPH) y β-caroteno-linoleato. En la fruta fresca los valores de CTF y CAO se incrementaron al aumentar el estado de madurez. CTF se incrementó desde 401,8±19,8 hasta 569,3±22,3 mg GAE/100 g peso seco, PS. Los valores de CAO obtenidos por ABTS en la fruta fresca (desde 79,4±4,5 hasta 132,7±12,9 µmol trolox/g fruta PS) fueron simil- ares a los obtenidos por FRAP (desde 82,9±16,3 hasta 153,9±31,7 µmol trolox/g fruta PS). Los valores obtenidos por DPPH variaron entre 21,0±3,2 a 34,1±5,1 µmol trolox/g fruta PS. El ensayo de β-caroteno-linoleato arrojó valores entre 5,8±1,1 a 12,7±2,0 µmol α-tocoferol/g fruta PS. El secado con aire tuvo una inf luencia pequeña en los valores de CTF. La fruta seca tuvo valores de CAO que representaron entre 27 a 164% de los valores obtenidos en la fruta fresca, con valores mayores en la fruta seca que en la fresca para ABTS y valores menores para FRAP, DPPH y β-caroteno-linoleato. Key words: tropical fruit, functional food, polyphenols. Palabras clave: fruta tropical, alimento funcional, polifenoles. POSTHARVEST PHYSIOLOGY AND TECHNOLOGY Introduction The cape gooseberry (Physalis peruviana L.), native to the Andean region, is a berry with an ovoid shape and 1.2-2.5 cm diameter, containing 100-300 seeds in a calyx- covered fruit (Fischer et al., 2011). The cape gooseberry is a climacteric fruit grown in countries such as Colombia, Peru, Venezuela, Egypt, South Africa, and Australia, among others (Ramadan, 2011). The cape gooseberry is the second most exported fruit from Colombia, after the banana, with European countries as the main customers: 3,225 t being exported to The Netherlands, 1,610 t to Germany, 966 t to Belgium, 115 t to Luxemburg, 214 t to Sweden, and 130 t to France (Fischer et al., 2011). In Colombia, an area of 1,000 ha is estimated to be dedicated to cape gooseberry plantations, with fresh fruit production ranging from 15 to 28 t ha-1 (Fischer et al., 2011). The cape gooseberry is commercialized in the domestic and international Colombian markets as fresh fruit. In Colombia, the cape gooseberry fruit is sold at three differ- ent ripeness stages according to the color of the peel (light orange, stage 4; orange, stage 5; and deep orange, stage 6) (Icontec, 1999). Commercialization of the air-dried fruit is a 233Narváez-Cuenca, Mateus-Gómez, and Restrepo-Sánchez: Antioxidant capacity and total phenolic content of air-dried cape gooseberry (Physalis peruviana L.)... growing marketing niche. Air-drying fruits and vegetables is a relatively inexpensive technique that extends shelf-life due to the reduction of water activity. As a negative effect, air-drying fruits and vegetables can negatively affect their nutritional and sensorial characteristics (Santos and Silva, 2008). A recent study showed that both oven drying and drum drying of frozen-stored whole fruit and frozen- stored slurry of the cape gooseberry fruit reduce the total phenolic content and the antioxidant activity as measured with a DPPH assay (Valdenegro et al., 2013). Air-drying fresh cape gooseberry at temperatures ranging from 50 to 100°C changed the total phenolic content and the antioxi- dant capacity as measured with DPPH and FRAP assays (Izli et al., 2014; López et al., 2013). No attempts on gaug- ing the effect of air-drying fresh cape gooseberry fruit at different ripeness stages on the antioxidant activity have been made. The objective of this research was, therefore, to evaluate the effect of air-drying cape gooseberry fresh fruit in three different ripeness stages (light orange, stage 4; orange, stage 5; and deep orange, stage 6) on the total phenolic content and antioxidant capacity. Materials and methods Reagents All trans-β-carotene; α-tocopherol; 6-hydroxy-2,5,7,8- tetramethylchroman-2-carboxylic acid (Trolox); 2,2′-azin- obis-(3-3-ethylbenzothiazoline-6-sulfonic acid) (ABTS); dithiothreitol; 2,2-diphenyl-1-picrylhydrazyl (DPPH); 2,4,6-tripyridyl-S-triazine (TPTZ); and Folin Ciocalteau- phenol reagents were supplied by Sigma (St. Louis, MO) and were used as they were received. Other chemicals came from Panreac Quimica (Barcelona, Spain). Plant material The cape gooseberry fruits were randomly collected from a commercial plantation in the municipality of Ramiriqui (Boyaca department), located in the central part of Colom- bia, 148 km northeast of Bogota, at 2,313 m a.s.l. with an av- erage temperature of 16°C. The cape gooseberry fruits were visually selected at three degrees of ripeness, according to the color of the peel. This selection was based on the color specifications given in the Colombian Technical Standard NTC 4580 (Instituto Colombiano de Normas Técnicas y Certificación, Icontec, 1999). The fruits were allowed to mature on the plants and harvested at the ripeness stages: 4, light orange; 5, orange; and 6, deep orange. The samples were immediately transported to Bogota and processed. Preparation of samples and processing The calyces were carefully removed from the fruit by hand. The fruit samples were washed with tap water and gently wiped with paper tissue. Fresh samples (without cutting them, 500 g fruit) were placed on 40 x 30 cm stainless steel food trays and loaded into a tangential air-flow cabinet. Nat- ural gas-heated air at 60°C, at a f low of 1,200-1,500 m3 h-1, with a relative humidity ranging from 40 to 60%, was used. The samples were removed from the air-f low cabinet after 16 h, allowed to cool to room temperature, packed in poly- ethylene bags, and stored at -20°C until the analyses. The fruits were also analyzed before air-drying. Compositional indexes Water content, total titratable acidity (TTA), and total soluble solids (TSS, °Brix) were measured in the fresh fruit. Water content was determined using the official AOAC (2000) method 934.06.27. TTA was measured by titrating the samples (2 g of homogenate plus 25 mL of CO2-free distilled water) with standardized 0.1 M NaOH to pH 8.2 using an Orion Advanced pH meter, model Orion 2-Star (Thermo Scientific, Boston, MA). Because citric acid is the main non-volatile carboxylic acid in the cape gooseberry (Fischer et al., 2000), the TTA was expressed as mg of citric acid/100 g of fruit fresh weight (FW). The TSS was assessed using a digital refractometer Abbe II (Reichert-Jung, Leica Inc., Buffalo, NY). The TSS/TTA ratio was calculated. Total phenolic content and antioxidant capacity The extraction was performed according to previous stud- ies (Restrepo-Sánchez et al., 2009). A 1 g fruit sample was placed in a f lask, equipped with a ref lux condenser, and extracted with 20 mL of 50% (v/v) aqueous methanol by stirring on a magnetic stir plate for 30 min at 50°C. After cooling to room temperature, the mixture was centrifuged (4,000 x g, 10 min, 4 °C) and the supernatant was kept at 4°C. The pellet was extracted four times with 5 mL of 70% (v/v) aqueous acetone for 30 min at 50°C. The five super- natants were mixed, the volume was graduated to 50 mL in a volumetric f lask with distilled water, and used for the analysis of the total phenolic content (TPC) and antioxidant capacity (AOC). The TPC was determined using the Folin-Ciocalteu (FC) method as described by Velioglu et al. (1998). A 100 µL extract was mixed with 750 µL of 10% (v/v) FC reagent. After 5 min, 750 µL of a 6% (w/v) Na2CO3 solution were added. After 90 min, the absorbance of the reaction mixture was measured at 725 nm. The results were expressed as gallic acid equivalents (mg GAE/100 g of dry weight (DW) of fruit). Calibration curves for gallic acid were performed in concentrations ranging from 0.01 to 0.30 mg mL-1 (five data points, r2 = 0.996). 234 Agron. Colomb. 32(2) 2014 The AOC of the extracts was measured by the ABTS, FRAP, DPPH, and β-carotene-linoleate bleaching assays. The ABTS assay was based on Re et al. (1999). A mixture of 7.0 mM ABTS and 2.45 mM potassium persulphate was prepared and stored in dark conditions for 16 h. The result- ing ABTS+• solution was diluted with ethanol to reach an absorbance of 0.70 at 734 nm. Aliquots of 10 µL of extracts were incubated with 1,000 µL of the ABTS+• solution at 30°C and the absorbance was monitored at 734 nm every 5 s over a period of 60 min. The FRAP assay was carried out according to the method described by Benzie and Strain (1996). The FRAP reagent was prepared by mixing 25.0 mL of a 300 mM sodium acetate buffer (pH 3.6) with 2.5 mL of 10 mM TPTZ in 40 mM HCl, and 2.5 mL of 20 mM ferric chloride. The FRAP reagent (900 µL), distilled water (90 µL), and extract (30 µL) were mixed. The mixture was incubated at 37°C and the absorbance was monitored at 593 nm every 5 s over a period of 45 min. The DPPH assay was performed according to Sánchez- Moreno et al. (1998). A methanolic stock solution of 50 mM DPPH was diluted with methanol to obtain a work- ing DPPH solution with absorbance of 1.10 at 515 nm. The extract (25 µL) was mixed with 975 µL of working DPPH solution. The mixture was incubated at 20°C and its absorbance was measured every 5 s for 1 h at 515 nm. The scavenging effect (in percentage) was calculated as (A1-A2/A0)*100, where A0 was the absorbance of the control (without extract), A1 was the absorbance in the presence of the extract once the steady state plateau was reached, and A2 was the absorbance without DPPH. In the ABTS, FRAP, and DPPH assays, standard curves were generated with trolox in concentrations ranging from 100 to 1,500 µM (five data points, r2 = 0.999, 0.989, 0.975, respectively). In all cases, the absorbance reached the steady state within the given incubation time. Results from the ABTS, FRAP, and DPPH assays were expressed as µmol of trolox/g of DW fruit. The β-carotene-linoleate bleaching assay was performed according to Velioglu et al. (1998). First, 500 µL of a 0.4 mg/mL β-carotene solution in chloroform was placed in a 100 mL plastic container and dried under N2. Next, 20 µL of linoleic acid, 200 µL of Tween® 20, 200 µL of the extract, and 50.0 mL of water saturated with air were added. The mixture was vigorously shaken, sonicated at 36 kHz for 10 min (Ultrasonic LC60H, Elma GmbH & Co., Singen, Ger- many), and incubated at 50°C for 2 h. The absorbance of the mixture was measured at 470 nm every 10 min during the given incubation time. The absorbance was plotted versus incubation time and the slope was calculated. A zero order kinetics was observed, which indicates that the depletion on the absorbance was caused by β-carotene bleaching and not by β-carotene precipitation (first order kinetics). The bleaching assay was also tested with a 50 µM α-tocoferol solution. The antioxidant activity of the extracts measured by the β-carotene-linoleate bleaching assay was expressed as µmol α-tocoferol/g of DW fruit. Statistical analyses The statistical analyses were performed using Statgraphics Plus® 5.1 for Windows (Manugistics, Rockville, MD). The mean values and their standard deviations were reported. One-way analyses of variance were performed for the com- positional index results. Two-way analyses of variance were performed for the TPC and AOC. Comparisons among means were performed by Tukey’s-test (P≤0.05). Results and discussion Compositional indexes As shown in Tab. 1, as the ripeness stage of the cape goose- berry increased (evaluated by its color), the TSS increased and the TTA decreased. The TSS/TTA ratio of each stage was in agreement with the specifications given in NTC 4580 (Icontec, 1999). The TSS values of the cape gooseberry fruit were comparable to those of the tropical fruits mango (Mangifera indica) (14.2-21.7°Brix, depending on cultivar and storage temperature) and papaya (Carica papaya) (8.8-14.3 °Brix, depending on cultivar and geographical location), but the TTA values were higher than those of the mentioned fruits (0.03-0.42 g citric acid/100 g FW in mango and 0.09-0.19 g citric acid/100 g FW in papaya) (Vazquez-Salinas and Lakshminarayana, 1985; Wall, 2006; Schweiggert et al., 2012). The relatively high TSS/TTA ratio of the cape gooseberry agrees with the high-sour/low-sweet taste of the fruit. TABLE 1. Compositional indexes of the cape gooseberry fruit. Compositional index Ripeness stage 4 5 6 TSS1 14.5±0.2 b 15.0±0.1 a 15.4±0.6 a TTA2 1.85±0.01 a 1.76±0.02 b 1.68±0.04 c TSS/ TA 7.8±0.1 c 8.5±0.1 b 9.2±0.5 a Water content3 79.6±1.7 b 85.0±2.9 a 85.0±2.5 a 1 Total soluble solids (TSS), expressed as °Brix. 2 Titratable acidity, expressed in g citric acid/100 g fresh weight. 3 Expressed in g water/100 g fresh weight. Means with different letters in the same row indicate significant differences according to the Tukey test (P≤0.05). 235Narváez-Cuenca, Mateus-Gómez, and Restrepo-Sánchez: Antioxidant capacity and total phenolic content of air-dried cape gooseberry (Physalis peruviana L.)... Total phenolic content (TPC) As shown in Fig. 1, the TPC (in mg GAE/100 g DW) increa- sed in the fresh fruit as the ripeness stage increased, from 401.8±19.8 (stage 4) to 569.3±22.3 (stage 6). When expressed in fresh weight (FW), the TPC (in mg GA/100 g FW) was 82.0±4.0 (stage 4), 81.0±2.8 (stage 5), and 85.4±3.3 (stage 6). The TPC values obtained in the current research were lower than those previously reported in cape gooseberry grown in Peru (154±3 mg GAE/100 g FW) (Repo and En- cina, 2008), comparable to that grown in Ecuador (87±19 mg GAE/100 g FW) (Vasco et al., 2008), and greater than previous reports for Colombia (39±5 mg GAE/100 g FW) (Restrepo, 2008) and Chile (321.0±31.4 mg GAE/100 g DW) (López et al., 2013). The higher values reported here might be related, in addition to differences in geographic origin, to the extraction method. Besides a methanolic extraction, a more lipophilic extraction solvent, 70% (v/v) aqueous acetone, was also used. The increase in the TPC as the ripeness stage increased was in agreement with previous results for some mango cultivars (Sulaiman and Ooi, 2012). FIGURE 1. Total phenolic content of fresh (white bars) and dried (grey bars) cape gooseberry fruit Maturity stage 4, light orange; 5, orange; 6, deep orange. Means with different letters in the same row indicate sig- nificant differences according to the Tukey test (P≤0.05) (n=3). Error bars indicate standard error. Air-drying the cape gooseberry fruit had a small inf luence, but statistically significant (P≤0.05), on the TPC. These values were reduced to 95, 86, and 92% of the original values after air-drying of the fruit at stages 4, 5, and 6, respectively. The moderate reduction in the TPC after air-drying the cape gooseberry was in contrast to the strong reduction in the TPC after air-drying in previous results on the type of fruit grown in Turkey (ripeness stage not reported) (Izli et al., 2014) and Chile (López et al., 2013), red pepper (Cap- sicum annuum) (Vega-Gálvez et al., 2009), saskatoon fruit (Amelanchier alnifolia) (Kwok et al., 2004), and apricots (Prunus armeniaca) (Madrau et al., 2009). Interestingly, López et al. (2013) reported that the modification of the TPC of air-dried cape gooseberry is temperature-depen- dant in a way that its content can be decreased but also increased. Furthermore, the stability in the air-drying of phenolic compounds observed in the cape gooseberry does not agree with the expected heat-degradation of the f lavonols rutin (quercetin-3-O-rutinoside), myricetin, and kaempferol present in cape gooseberry fruit (Licodiedoff et al., 2013). It has been shown that rutin and other phenolics (e.g. chlorogenic acid and catechin) are susceptible to high temperatures (55°C) during the air-drying of apricots (Madrau et al., 2009). Likewise, the air-drying of mulberry (Morus alba) leaves (Katsube et al., 2009) at 70°C induces degradation of rutin, a kaempferol glycoside, and other phe- nolics. We hypothesize that the low reduction in the TPC of the air-dried fruit might be explained by the presence of other compounds, different from the aforementioned phenolics, that are stable under heat treatments and renct- ing to the FC reagent or that degradation products of the native phenolic compounds after air-drying have similar reactivity towards the FC reagent. Antioxidant capacity (AOC) Figure 2 shows the AOC of the cape gooseberry fruit as measured by the ABTS, FRAP, DPPH, and β-carotene- linoleate assays. The AOC values (expressed as µmol trolox/g fruit DW) obtained by ABTS in the fresh fruits (ranging from 79.4±4.5 in ripeness stage 4 to 132.7±12.9 in ripeness stage 6) were comparable to those obtained by FRAP (ranging from 82.9±16.3 in ripeness stage 4 to 153.9±31.7 in ripeness stage 6). In contrast, those values assessed by DPPH (ranging from 21.0±3.2 in ripeness stage 4 to 34.1±5.1 in ripeness stage 6) were much lower. When the AOC was evaluated by the β-carotene-linoleate assay, values ranging from 5.8±1.1 (ripeness stage 4) to 12.7±2.0 µmol α-tocoferol/g fruit DW (ripeness stage 6) were obtained. Furthermore, the AOC measured by the ABTS, FR AP, DPPH, and β-carotene-linoleate assays increased as the ripeness stage of the fruit increased. The increase in the AOC observed as the ripeness stage of the cape gooseberry increased agrees with results of AOC- FRAP measured in papaya fruits during ripening when stored at 25°C (Ong et al., 2013). The greater antioxidant activity as the ripeness stage advanced observed in the cape gooseberry fruit was opposite to the trend described in guava and durian fruits (Arancibia-Avila et al., 2008; Gull et al., 2012). As a result of air-drying, the AOC measured by the FRAP, DPPH, and β-carotene-linoleate assays decreased, con- trasting with the increase observed when the AOC was e e ab d bc a 0 100 200 300 400 500 600 G al lic a ci d (m g/ 10 0 g fr ui t D W ) Maturity stage 4 5 6 236 Agron. Colomb. 32(2) 2014 measured by the ABTS assay at ripeness stages 4 and 6. A decrease of the TPC, together with an increase of the AOC has been described when the AOC was evaluated by the DPPH assay during the air-drying of apricots (Madrau et al., 2009), mulberry leaves (Katsube et al., 2009), and red pepper (Vega-Gálvez et al., 2009). It would be possible that reaction products of the Maillard type or degradation products of phenolic compounds were generated during the air-drying and that those compounds, resulting in a low reaction to the FC reagent, contributed to the control- ling power of the ABTS+•. It is unknown, nevertheless, why these compounds enhanced the AOC-ABTS, but decreased the AOC-FRAP, considering the fact that, in both methods, the redox potential involved was similar (Prior et al., 2005). It might be that the compounds re- sponsible for the divergent behavior in these two assays have a differential behavior at the different pH values that each assay involves (Prior et al., 2005). The decrease in the AOC as measured by the DPPH and FRAP methods after air-drying was in agreement with previous results from cape gooseberry fruit (López et al., 2013; Izli et al., 2014). Conclusions The total phenolic content (TPC) as well as the antioxidant capacity (AOC), as measured by the ABTS, FRAP, DPPH, and β-carotene-linoleate assays, increased as the ripeness stage of the cape gooseberry increased. While the TPC in the air-dried fruits represented values ranging from 86 to 95% of the fresh fruit, the AOC in the air-dried fruits produced values ranging from 27 to 164%, with ABTS giv- ing higher values in the air-dried than in the fresh fruits and the FRAP, DPPH, and β-carotene-linoleate assays giving lower values in the air-dried fruits. The differential behavior of the AOC (large variation after air-drying) as compared to the TPC (small variation after air-drying) might indicate a large transformation of phenolic com- pounds, yielding reaction products with different behaviors c bc b b a b c e b e d a c de b d cd a c d b d d a α -t oc of er ol ( µ m ol /g fr ui t D W ) Maturity stage 4 5 64 5 6 D Tr ol ox ( µ m ol /g fr ui t D W ) 4 5 6 Tr ol ox ( µ m ol /g fr ui t D W ) 4 5 6 0 50 100 150 200 250 0 50 100 150 200 BA 0 10 20 30 40 Tr ol ox ( µ m ol /g fr ui t D W ) Maturity stage C 0 5 10 15 FIGURE 2. Antioxidant capacity of fresh (white bars) and dried (grey bars) cape gooseberry fruit. A, ABTS; B, FRAP; C, DPPH; D, β-carotene-linoleate assays. Maturity stage 4, light orange; 5, orange; 6, deep orange. Means with different letters in the same row indicate significant differences ac- cording to the Tukey test (P≤0.05) (n=3). Error bars indicate standard error. 237Narváez-Cuenca, Mateus-Gómez, and Restrepo-Sánchez: Antioxidant capacity and total phenolic content of air-dried cape gooseberry (Physalis peruviana L.)... towards the chemicals used to access the AOC, but with similar reactivity towards the FC reagent. Literature cited AOAC, Association of Official Analytical Chemists International. 2000. Moisture in dried fruits. Method 934.06.27. In: Horowitz, W. (ed.). Official Methods of Analysis of AOAC International. 17th ed. Gaithersburg, MD. Arancibia-Avila, P., F. Toledo, Y.-S. Park, S.-T. Jung, S.-G. Kang, B.G. Heo, S.H. Lee, M. Sajewicz, T. Kowalska, and S. Gorinstein. 2008. 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