Antioxidant properties of fresh and processed cactus pear cladodes ...

South African Journal of Botany 118 (2018) 44–51

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South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb

Antioxidant properties of fresh and processed cactus pear cladodes from selected Opuntia ficus-indica and O. robusta cultivars A. du Toit a,1, M. de Wit b,⁎,1, G. Osthoff b,1, A. Hugo b,1 a b

Department of Consumer Science, University of the Free State, Faculty of Natural and Agricultural Sciences, PO Box 339, Bloemfontein, 9300, South Africa Department of Microbial, Biochemical and Food Biotechnology, University of the Free State, Faculty of Natural and Agricultural Sciences, PO Box 339, Bloemfontein, 9300, South Africa

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Article history: Received 1 September 2017 Received in revised form 6 December 2017 Accepted 12 June 2018 Available online xxxx Edited by OM Grace Keywords: Prickly pear Ascorbic acid Phenolic compounds Carotenes Betalains Chelating activity Radical scavenging

a b s t r a c t If the cactus plant could find applications in the food industry, other than that of fresh fruit, by means of preserving the cladodes, a larger market may emerge, thus making it an economically more viable crop. The aim of this study was therefore to explore the processing of cladodes into different preserved food products and to study the processed products' antioxidant content and -capacity compared to the fresh cladodes. All cultivars demonstrated high antioxidant capacities and consequently, the cladodes of any cultivar could be considered as suitable for processing or preserved to produce healthy products. Processing had a greater influence on the antioxidant content of cactus cladode products than the cultivar. Dried products were the best in terms of antioxidant content and -capacity. © 2018 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction Twenty-two spineless Burbank Opuntia ficus-indica and O. robusta cultivars, developed by Luther Burbank (California, USA) were imported into South Africa in 1914 and established at Grootfontein research station (Middelburg, Cape Province). This collection is unique and South Africa is the only country where these cultivars are still available. These were evaluated and propagated mainly for cladode use in animal fodder (Potgieter and Mashope, 2009). A few cultivars are nowadays cultivated and evaluated for commercial production of the fruit destined for the local and European markets (Joubert, 1993; Coetzer and Fouché, 2015). There is currently a small but well developed commercial sector in South-Africa, but the plant as a whole is mainly under-utilized and under-valued (de Wit and Fouché, 2015). This under-utilization may be, in part, a consequence of the uncertainty that exist regarding the invasive nature of the cactus pear (Shackleton et al., 2011). According to the Conservation of Agricultural Resources Act (1983) (Act No. 43 of 1983), Opuntia ficus-indica (L.) Mill. is categorized as a Category 1 weed, meaning that no plants should be planted, established, maintained, propagated, imported or sold (Beinart and Wotshela, 2013). According to the latest list of invasive plant species, ⁎ Corresponding author. E-mail address: [email protected] (M. de Wit). 1 These authors contributed equally to the work.

https://doi.org/10.1016/j.sajb.2018.06.014 0254-6299/© 2018 SAAB. Published by Elsevier B.V. All rights reserved.

Opuntia ficus-indica (Species No. 218) is a category 1b invasive (DEAT, 2009; Shackleton et al., 2011). The spineless cultivars and selections are however excluded from the Act and invasive species list. The stems or pads (cladodes) of the cactus pear plant (Opuntia ficusindica and Opuntia robusta) are safe for human consumption; they have always been considered an important food and nutritional food source in Latin America (Rodríguez-Felix and Villegas-Ochoa, 1998). In Mexico, the whole cactus stems or pads used for food are known as nopal or pencas, while the young and tender cladodes cut into bite sized pieces is called nopales or nopalitos (Sáenz-Hernández et al., 2002). It is sold in open informal markets or packaged by using modified atmosphere packaging (Guevara et al., 2001). It is prepared and used either raw in dishes such as salads and salsas or cooked by means of boiling or frying (Saenz, 2000). It is used with other ingredients in a variety of traditional culinary dishes including desserts, beverages, snacks, soups, stews, sauces and salads (Saenz, 2000). Nopalitos are also preserved in brine or pickled (Rodriguez-Felix and Cantwell, 1988). There has been increased interest for products derived from the cactus pear plant due to their potential nutraceutical effects (Ruiz Pérez-Cacho et al., 2006). Compounds found in these products are known to combat oxidative stress and chronic diseases (ChavezSantoscoy et al., 2009). The medicinal uses of the cladodes (Feugang et al., 2006) include possible anti-cancer effects and proven antioxidant properties, anti-viral-, anti-inflammatory-, anti-diabetic (type II) effects as well as anti-hyperlipidemia and hypercholesterolemia.

A. du Toit et al. / South African Journal of Botany 118 (2018) 44–51

The mucilage found in cladodes is a very important source of soluble fiber and products using the whole cladode contain large amounts of both insoluble and soluble fiber that are not absorbed by the human digestive system (Sáenz-Hernández et al., 2002). The cactus cladodes are used to regulate weight, increase fiber intake or manage diabetes mellitus and as a natural source of potassium (Sáenz, 1997). Hfaiedh et al. (2008) found that cladode juice provided highly effective radical scavenger effects. Fresh fruit and cladodes are only ready to be harvested for a few months of the year and storage time is limited (Joubert, 1993). Food technologists are challenged to develop procedures to lengthen the storage life of the cactus pear fruit and cladodes and to diversify the plant by producing different types of preserved products (Joubert, 1993; Piga et al., 2003; Sáenz et al., 2004). Several products could be obtained from processing the fruit and cladodes. Some of the traditional and known products are juices, marmalades, jellies, jams, dried sheets, pickles, candy and alcoholic drinks. Recently developed products include liquid sweeteners, frozen fruit, cladode flour (Sáenz-Hernández et al., 2002; de Wit et al., 2015), oil (from the seeds) (de Wit et al., 2016, 2017, 2018a, 2018b), mucilage (from cladodes) (du Toit, 2016; de Wit et al., 2018a; du Toit et al., 2018a, 2018b), pigments and dietary fiber (from the cladodes) (Saenz, 2000). It is possible that processing could damage and therefore decrease antioxidant content (Tesoriere et al., 2005), however this seems not to be the case. When Jaramillo-Flores et al. (2003) investigated the cladodes for carotene content after thermal treatment, it was found that the carotenoid extractability increased after thermal treatment. It was demonstrated that higher processing temperature caused more carotene to be released from the cell matrix because of thermal denaturation of carotenoid-proteins, softening of tissue and therefore allowing higher penetration of organic solvents into the cells. Rickman et al. (2007b) confirmed that thermal processing methods such as canning improved the extraction of carotene from the cell matrix of cladodes. This effect might be as a result of complexes formed with mucilage because of the high degree of pectin esterification that cannot be detected at pre-gelling temperatures. Medina-Torres et al. (2011) found that bioactive compounds are preserved in cladodes during the dehydration process as 25% of flavonoids, 20% of ascorbic acid and 50% carotene remained intact. Stintzing et al. (2005) demonstrated that betalains maintain their appearance as well as their antioxidant capacity over a large pH spectrum from pH 3 to 7. Rickman et al. (2007b) studied the alleged increase in carotenoids after cooking and found that several authors reported such an increase during cooking of other fresh and frozen vegetables (carrots, broccoli, green beans, spinach and peas) on a wet basis. They also observed that frozen and cooked canned products contained antioxidant values similar to fresh products, regardless of the length of storage time (Rickman et al., 2007a). Rickman et al. (2007b) concluded that vegetables that were initially good sources of carotene remained good sources after processing. The same phenomenon was found by Howard et al. (1999) where microwave cooking resulted in greater solvent extraction of β-carotene in broccoli and carrots. Ryan and Prescott (2010) found that many other authors have reported the same phenomenon and possible explanations were reported as: antioxidant capacity increased because the heat disrupts the cell walls allowing more antioxidant components to be released; heat treatments deactivate oxidative enzymes that would normally destroy antioxidants; as well as heat treatments cause the formation of new structural groups which enhance antioxidant activity. The last explanation was seen by Ryan and Prescott (2010) as the most correct one, as it was found before that antioxidant capacity of gallic acid increased after heat treatment because of the formation of new hydroxyl groups and that structure changes in polyphenols increases antioxidant activity. Therefore Ryan and Prescott (2010) theorized that heat treatment can possibly increase antioxidant capacity by causing slight changes to take place in the structure of the

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compounds. These changes render the antioxidant more stable to pH, allowing it to continue its activity throughout the digestive tract. If the cactus plant could find applications in the food industry, other than that of fresh fruit, by means of preserving the cladodes, a larger market may emerge, thus making it an economically more viable crop. In a previous study (du Toit, 2013; du Toit et al., 2015) different colors of fruit from different cultivars were processed into different food products and evaluated in terms of antioxidant content and -capacity. The highest antioxidant content and -capacity were found in purple (O. robusta Robusta) fruit products, attributed to the high levels of betalains. Orange fruit (O. ficus-indica) products had the second highest levels attributed to ascorbic acid and phenolic compound contents. Betalains were highly retained in processed products; ascorbic acid was mostly preserved in the processed products that involved minimal heat treatments, while carotene and phenolics increased after processing. The aim of this study was to explore the processing of cladodes into different preserved food products, to study the processed products' antioxidant content and -capacity compared to the fresh cladodes as well as to distinguish if fruit color is an indication of antioxidant content and -capacity of cladodes. 2. Materials and methods 2.1. Sample collection and preparation Six-month-old cladodes from the same cultivars used in the study of du Toit et al. (2015) were chosen and collected to represent the four colors of fruit available namely green, orange, pink-red and purple. Cladodes of good quality, without any blemishes, which had not bear any fruit, from four cultivars of O. ficus-indica [Gymno-Carpo (orange), Meyers (red-pink), Nepgen (green), Ofer (orange)] and one from O. robusta [Robusta (purple)] were collected from Waterkloof, an eight year old cactus pear orchard located in the Bloemfontein district of the Free State Province in South Africa. It is 1348 m above sea level and receives 556 mm rainfall on average annually. The GPS coordinates are 29°10′53″ S, 25°58′38″ E. It hosts 40 Opuntia ficus-indica cultivars and two O. robusta cultivars, laid out in a fully randomized design with two replications of each cultivar (de Wit et al., 2010). Each replication consists of five plants. Two cladodes from the first, third and fifth plant of each replication were harvested. Cladodes were all selected to be at the same height of the plant and of equal size. Three cladodes were randomly selected per each replication (thus 6 cladodes per cultivar). For the fresh cladode samples, the cladodes were weighed, cut into pieces and liquidized. Equal weights of water (100%) were added, homogenized and centrifuged at 8000 rpm for 10 min at 4 °C and the supernatant was frozen in aliquots. Cladode juice was prepared by peeling the cladodes, liquidizing the inner soft part, strained (0.5 mm mesh size) and the filtered juice was then pasteurized in a water-bath for 10 min until the internal temperature reached 72 °C, immediately shocked in cold water and then frozen (not longer than one month). For dried cladodes, the cladodes were washed, cut in thin strips and blanched at 80 °C for 5 min. It was dried in a convection oven set at 90 °C for 18 h (Voedselpreservering, 1986), vacuum packed and frozen. Cladodes were also preserved (jarred) in brine according to the steam pressure method (Van Zyl et al., 1987), whereby the cladodes were washed and cut into thin strips of approximately 20 mm × 150 mm, blanched, packed into sterilized hot jars and filled with hot brine solution consisting of 2.5 g salt, 3 g vinegar and 2 g sugar and 500 ml water and sealed. It was pressure cooked for 25 min (Bennion, 1985). For chutney preparation, the cladodes were washed and the pulp was obtained by feeding cladodes through a juicer. The total weight of cladode pulp was obtained and the chutney was further formulated as follows: cladode pulp 65%, sugar 10%, cayenne pepper 0.01%, minced onion 4%, salt 0.2%, powdered ginger 0.2%, powdered mustard 0.06%,

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powdered garlic 0.2% and grape vinegar 10% (Voedselpreservering, 1986). All the ingredients were added to a stainless steel saucepan and allowed to boil slowly until it was thick and dropped off the spoon in flakes and had the consistency of jam. The prepared chutney was poured into hot sterilized jars (350 ml) and sealed, labeled and stored at room temperature (Van Zyl et al., 1987). For pickling, cladodes were weighed, washed and cut into thin strips of approximately 20 mm × 150 mm. It was left for 20 h in brine. The brine, consisting of 500 g salt and 5 l of water, was previously boiled, strained and allowed to cool. After removing the cladodes from the brine they were thoroughly rinsed in cold water and packed into jars up to 20 mm from the rim. The jars were filled with prepared spicy vinegar up to at least 10 mm above the contents to exclude air and avoid discoloration. Jars were sealed and allowed to mature for two months at room temperature. The spicy vinegar consisted of 2 l of vinegar, 9 g mustard seeds, 5 g allspice, 2 g whole cloves and 0.5 g of oil. It was prepared by boiling the ingredients together briefly and allowing it too steep for 2 h (Voedselpreservering, 1986). 2.2. Antioxidant determination Aqueous extracts were prepared from all the processed products for determination of % chelating activity, % DPPH radical scavenging assay, betalain content, ascorbic acid content and total phenolic compound content. For carotenoid determination, a hexane/acetone/ethanol extract was prepared from all the processed products. 2.3. Antioxidant capacity 2.3.1. Percentage chelating activity The method described by Gülçin et al. (2007) was used in the present study in accordance with the study of Sumaya-Martínez et al. (2011) to determine chelating activity. One hundred microliters of the samples were prepared and 50 μl ferric (II) chloride solution (2 mM) and 4.5 ml methanol was added. It was vortexed for 10 s and 200 μl ferrozine (5 mM) was added. It was centrifuged and the absorbance was determined at 562 nm, and the chelating activity was calculated as follows: Ferrous ions chelating effect ð%Þ ¼

Acontrol−ðAsample−AblankÞ 100 Acontol DF

Acontrol = absorbance of distilled water used instead of sample with ferric (II) chloride and ferrozine, Asample = absorbance in the presence of the sample and reagents, Ablank = absorbance of sample with dilutants without reagents. 2.3.2. Percentage DPPH scavenging 2,2′-Diphenyl-1-picrylhydrazyl (DPPH) was determined by preparing an ethanolic solution of DPPH (7.4 mg/100 ml) (Morales and Jiménez-Pérez, 2001; Sumaya-Martínez et al., 2011). In each test, 500 μl of the DPPH solution was added to 100 μl of the aqueous samples. It was vortexed for 10 s and left to stand for 1 h. It was then centrifuged at 10,000 rpm for 5 min at 4 °C before the absorbance was measured at 517 nm (Gülçin et al., 2007). DPPH scavenge effectð%Þ ¼

Acontrol−ðAsample−AblankÞ 100 Acontrol DF

Acontrol = absorbance of the reagent, Asample = absorbance of the sample, dilutants and reagent, Ablank = absorbance of sample with dilutants without reagents.

2.4. Antioxidant content 2.4.1. Betalains Betalains were determined according to Castellanos-Santiago and Yahia (2009) and Stintzing et al. (2005). The betalain content (which comprises of the red-violet betacyanins (Bc) and the yellow betaxanthins (Bx)) was calculated according to the following equation. mg Bc=Bx ¼ AðDFÞðMWÞð1000Þ=EðLÞ g A is absorption value at 600 nm, DF = dilution factor, Molecular weight (MW) Bc = 550, Bx = 308, Molar extinction coefficients of betanin (E) = 60,000, indicaxanthin (E) = 48,000, L = pathlength of the cuvette. 2.4.2. Ascorbic acid Ascorbic acid was determined according to James (1995), a 10 fold and 100-fold dilution of the aqueous extract was titrated with 0.04% 2,6 dichlorophenol-indophenol solution. mg ¼ ðT−BÞ=ðSt−BÞð20ÞðDFÞ 100 mg

T = titration value, B = blank, St = standard solution, DF = dilution factor. 2.4.3. Carotenoids Carotenoid content was determined after samples were homogenized with 10 ml hexane:acetone:ethanol (50:25:25, v/v) before being centrifuged at 6500 rpm at 4 °C for 5 min. The top layer of hexane, was recovered and the volume was adjusted to 25 ml with hexane. The absorbance was measured at 450 nm according to the method described by Kuti (2004) and Fernández-López et al. (2010) using an extinction coefficient of β-carotene, E1% = 2590. The results were converted to μg/g (fresh weight). xðμgÞ ¼ A∙yðmLÞ∙106 =A1% 1 cm ∙100 μg xðμgÞ ¼ x g weight of sample X = weight or concentration of carotenoid, A = absorbance, y = volume of solution, A1% 1 cm = 2590 (absorption coefficient). 2.4.4. Total phenolic compounds The total phenolic content was determined using 2 g of the aqueous extract. After the samples had been centrifuged in order to obtain a clear extract, 0.2 ml was combined with 1 ml Folin–Ciocalteu reagent and 0.8 ml sodium carbonate solution concentration. An absorbance reading at 765 nm was done in a Genesys 10 Vis Thermo Spectronic spectrophotometer after 30 min. The polyphenol reading at 765 nm was expressed as mg of gallic acid equivalents per liter (mg/l GAE), following a calibration curve with pure gallic acid at 0, 50, 100, 150, 200, 250, 300, 350 mg/l concentrations (Stintzing et al., 2005). All values were converted to mg/kg (fresh weight).


2.5. Statistical analysis Data was analyzed using NCCS (2007) statistical software. Analysis of variance (ANOVA) was conducted in order to determine the effect of cultivar and product type on the antioxidant properties of processed cactus pear. The Tukey–Kramer multiple comparison test was used to differentiate between treatment means (NCCS, 2007). In an attempt to visualize the relationship between cultivar and antioxidants of the processed products in a 2 – dimensional space, PCA (Principal Component Analysis) was performed (NCCS, 2007). 3. Results and discussion The influence of cultivar and product type on the antioxidant properties of fresh and processed cactus pear cladodes are indicated in Table 1. Dried cladodes of all cultivars had consistently higher values (81.67– 85. 83%) for chelating activity, while chutney (40.00–75.00%) and preserves (66.67–82.50%) had significantly (p b 0.001) lower values. Cladode juice and pickles had the lowest chelating activity (16.67– 48.33% and 7.33–48.33%, respectively). No single cultivar could be identified as having the best chelating activity in cladodes (Table 1). Chutney and dried cladodes compared well to fresh cladodes in the % DPPH results, as the values did not differ significantly. Values for juice were only slightly lower, while preserved cladodes had the lowest ability to scavenge radicals. For the processed cladodes in general, this trend can be roughly seen when values among products are compared, but no individual cultivar could be highlighted. The fact that the % DPPH did not drop significantly after processing cladodes into different products, indicated that antioxidants in cladodes did not lose their ability to scavenge radicals after processing. This phenomenon was also reported by Jaramillo-Flores et al. (2003), who found that the antioxidant capacity in heat treated young cladodes (nopalitos) increased compared to unprocessed young cladodes. Jaramillo-Flores et al. (2003) demonstrated that fresh carotenoid extracts that measured antioxidant activity of 53% increased to 70% after it was immersed in water at 93 °C for 30 min. For the same product, phenolic content increased from 45% to 54% after the same treatment. The antioxidant activity of the nopalitos increased for both extracts with heat exposure (Jaramillo-Flores et al., 2003). Gallegos-Infante et al. (2009) found low radical scavenging activity in cladodes due to monohydroxylated phenolic compounds that rendered phenols with low activity. This was however not observed in this study since cladodes showed high ability to scavenge radicals in fresh cladodes as well as in dried and chutney products (Table 1). Ascorbic acid levels in dried cladodes were the highest (182.36– 282.14 mg/100 g in Ofer) and the lowest in preserves (14.29– 28.00 mg/100 g) (Table 1). Robusta had the highest ascorbic acid values overall. This result is surprising as Robusta had low ascorbic acid levels in fresh cladodes (24.04 mg/100 g) with Gymno-Carpo (77.40 mg/100 g) and Meyers (67.25 mg/100 g) having the highest values (Table 1). It may however, be possible that ascorbic acid is protected in the Robusta cladode during processing due to its high viscosity mucilage (du Toit, 2016; de Wit et al., 2018a; du Toit et al., 2018a, 2018b). Nepgen and Robusta juice had the highest ascorbic acid content, demonstrating higher levels than all other cultivars (N 50 mg/100 g) (Table 1). Regarding betalains (betacyanins and betaxanthins), the only cultivar standing out was Robusta, where Robusta pickles (19.2 mg/kg) had significantly (p b 0.001) higher betalains than the other cultivars. No statistically significant differences were observed among cultivars in the betalain content for cladode chutney and dried cladodes. In the preserves, the betalain content was generally lower (0.11–0.54 mg/kg) than in the fresh and other products. Jaramillo-Flores et al. (2003) found a carotenoid content of 229 μg/g in a fresh nopalito extract that increased to 379 μg/g after a heat treatment of 93 °C. In this study the highest carotene content was

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found in dried Gymno-Carpo cladodes (254.75 μg/g) and the lowest in Gymno-Carpo chutney (1.36 μg/g) samples. The values in dried cladodes were exceptionally high (103.87–254.75 μg/g) compared to fresh cladodes (6.72–17.87 μg/g). In fact, the carotene content in fresh cladodes was only 7% of the value in dried cladodes. This is due to the concentrating effect of the drying process. Reasons for the observed increase in carotene content after processing was summarized by Rickman et al. (2007b) as higher extraction efficiency, release of protein-bound carotene during heat treatments, degradation of oxidative enzymes and the loss of soluble solids. The values of all other products were statistically similar; in fact, it was very similar to fresh cladodes (Table 1). Gymno-Carpo had the highest carotene content overall and Robusta had the lowest, while in fresh cladodes, both Gymno-Carpo and Meyers had high carotene content (Table 1). Dried cladodes may therefore be a very good source of carotene. Robusta was the cultivar with the lowest phenolic content and Gymno Carpo the cultivar with the highest phenolic content in the fresh product form. The high phenolic content found in fresh cladodes (42.84–270.93 mg/kg) was also seen in processed cladode products, in fact, dried cladodes had phenolic contents similar to that of fresh values (181.11–273.46 mg/kg). In other studies, phenolic values decreased during drying. In a study by Gallegos-Infante et al. (2009) phenolics decreased from 180 mg/g GAE in fresh nopal to 41.0 mg/g GAE in dehydrated nopal at 45 °C and 3 m/s air flow. Phenolic compounds also decreased from 1589 to 287 μg/g in fresh nopalitos exposed to temperatures up to 93 °C (Jaramillo-Flores et al., 2003). The phenolic levels for chutney (104.98–124.81 mg/kg), juice (73.14–102.32 mg/kg) and pickles (91.82–147.12 mg/kg) did differ significantly from fresh and dried cladodes. Preserves had very inconsistent levels for different cultivars (0.44–61.61 mg/kg). The dried cladodes generally had very high antioxidant properties. In the past years, there has therefore been increasing interest in developing foods that contain dried cladodes (Feugang et al., 2006). Drying cladodes for the purpose of making flour has been investigated recently (Sáenz et al., 2000; de Wit et al., 2015). Cladode flour could be used in bread products (such as in tortillas), or in nutritional supplements, in powder, tablet or capsule form (López-Cervantes et al., 2011). It is important to maintain the original properties of cladodes after drying (Gallegos-Infante et al., 2009). It can also be considered to commercially manufacture chutney, juice and pickles from cladodes. Cladodes are suitable for pickling as it has a slightly sour taste (Van Zyl et al., 1987) and pickled cladodes might be an acceptable product to the South African community. It is not cooked therefore the color stays intact, while the flavor is enhanced by the spicy vinegar. Although pickles did not perform well in antioxidant capacity tests, it had high ascorbic acid and phenolic levels, while the carotene levels were similar to fresh cladodes (Table 1). Preserved (jarred) cladodes were the product with the least antioxidants and antioxidant capacity (Table 1). Determining the best cultivar was not clear since Robusta cladodes had the highest ascorbic acid and betalain values, but had the lowest carotene and phenolics contents. Ofer and Gymno-Carpo were the cultivars which had the most consistently high ascorbic acid, phenolic, betalain and the highest carotene values. In the PCA analysis (Fig. 1), F1 and F2 explained 69.48% of the variability. The data clearly indicated that dried products were closely related to carotene, ascorbic acid and phenolic compounds. Percentage DPPH and % chelating activity is closely related to each other and the fresh cladodes from Gymno-Carpo, Nepgen and Meyers as well as to the chutney from Nepgen and Meyers (these products had the highest results for % DPPH and % chelating activity as indicated in Table 1). Not only was the products made from Robusta clustered around the betalains, but Ofer chutney and fresh cladodes from Ofer and Meyers were also clustered together. The other products were also clustered closely together, but did not seem to be associated with the antioxidants tested in this study. It is noteworthy that preserves (all cultivars except Robusta) are located on the far left of the figure, meaning that preserves

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Table 1 The effect of cultivar and product type on the antioxidant properties of fresh and processed cactus pear cladodes. Cultivar

Chelating activity %

DPPH %

Ascorbic acid mg/100 g

Betacyanins mg/kg

Betaxanthins mg/kg

Betacyanins + betaxanthins mg/kg

Carotene μg/g

Phenolics mg/kg

Fresh

Gymno C Meyers Nepgen Ofer Robusta Gymno C Meyers Nepgen Ofer Robusta Gymno C Meyers Nepgen Ofer Robusta Gymno C Meyers Nepgen Ofer Robusta Gymno C Meyers Nepgen Ofer Robusta Gymno C Meyers Nepgen Ofer Robusta

77.50 ± 2.50hijk 80.83 ± 2.89ijk 89.17 ± 1.44k 80.83 ± 7.22ijk 70.00 ± 9.01ghij 75.00 ± 6.61hijk 40.00 ± 2.50cde 46.67 ± 1.44def 62.50 ± 2.50fgh 53.33 ± 3.82efg 82.50 ± 2.50ijk 83.33 ± 5.20ijk 85.83 ± 3.82jk 82.50 ± 2.50ijk 81.67 ± 1.44ijk 31.67 ± 11.27bcd 48.33 ± 8.04def 38.33 ± 11.27cde 37.50 ± 11.46cde 16.67 ± 3.82ab 7.33 ± 6.43a 28.33 ± 10.10bc 48.33 ± 6.29def 25.83 ± 1.44bc 18.33 ± 1.44ab 66.67 ± 2.89ghi 82.50 ± 2.50ijk 75.83 ± 1.44hijk 76.67 ± 1.44hijk 66.67 ± 1.44ghi 58.69 24.62 41.96 p b 0.001

95.53 ± 0.15k 92.74 ± 3.27ijk 94.49 ± 1.37jk 83.77 ± 10.41efghi 92.50 ± 0.91ijk 94.98 ± 0.43k 95.15 ± 0.03k 93.55 ± 0.26jk 92.19 ± 0.37ijk 90.16 ± 1.28hijk 93.10 ± 1.17jk 89.31 ± 3.19ghijk 89.54 ± 1.53hijk 94.12 ± 0.30jk 88.67 ± 2.20ghijk 92.21 ± 6.60ijk 94.53 ± 2.64k 93.40 ± 1.99jk 85.29 ± 1.22fghij 80.18 ± 4.19efg 70.34 ± 0.99bcd 67.97 ± 3.13bc 82.08 ± 0.11efgh 75.49 ± 0.79cde 77.75 ± 1.46def 61.30 ± 1.37ab 63.47 ± 0.42ab 63.81 ± 2.81ab 57.84 ± 0.74a 76.68 ± 2.49cdef 84.07 11.88 14.13 p b 0.001

77.40 ± 11.34abcd 67.25 ± 18.65abcd 26.78 ± 1.01ab 58.74 ± 11.14abcd 24.04 ± 7.44a 115.81 ± 5.45cdef 50.60 ± 6.93abc 52.57 ± 8.67abcd 58.17 ± 2.37abcd 115.23 ± 12.51cdef 182.36 ± 34.07fgh 222.94 ± 49.40hi 159.73 ± 31.93efgh 282.14 ± 31.42i 191.57 ± 64.44gh 39.00 ± 9.34ab 48.56 ± 7.34abc 53.48 ± 8.75abcd 35.16 ± 7.43ab 52.05 ± 10.36abc 123.62 ± 13.71defg 95.90 ± 26.25bcde 71.65 ± 27.14abcd 111.79 ± 34.53cdef 157.69 ± 16.59efgh 14.29 ± 9.59a 16.74 ± 6.46a 25.40 ± 17.70ab 17.00 ± 1.45a 28.00 ± 8.16ab 85.85 69.66 81.14 p b 0.001

3.17 ± 2.24abc 7.54 ± 1.97cd 4.74 ± 0.39abc 3.17 ± 2.24abc 17.18 ± 7.74e 5.37 ± 1.31abc 5.44 ± 2.57abc 3.65 ± 1.18abc 8.16 ± 1.98cd 8.71 ± 0.39cd 5.02 ± 0.28abc 8.80 ± 0.09cd 6.12 ± 2.07bcd 8.21 ± 0.77cd 4.57 ± 0.46abc 0.46 ± 0.06ab 0.71 ± 0.14ab 0.24 ± 0.05a 0.55 ± 0.12ab 3.64 ± 1.05abc 0.40 ± 0.20ab 0.66 ± 0.24ab 1.38 ± 0.09ab 0.67 ± 0.23ab 11.30 ± 0.95d 0.09 ± 0.02a 0.32 ± 0.15a 0.42 ± 0.06ab 0.06 ± 0.06a 0.15 ± 0.08a 4.03 4.34 107.67 p b 0.001

2.22 ± 1.56abc 5.28 ± 1.38cd 3.32 ± 0.27abc 16.98 ± 1.26f 12.02 ± 5.42e 3.76 ± 0.91abc 3.81 ± 1.80abc 2.55 ± 0.82abc 5.71 ± 1.39cd 6.10 ± 0.28cd 3.52 ± 0.19abc 6.16 ± 0.06cd 4.28 ± 1.45bcd 5.75 ± 0.54cd 3.20 ± 0.32abc 0.32 ± 0.04ab 0.50 ± 0.10ab 0.17 ± 0.04a 0.39 ± 0.09ab 2.55 ± 0.73abc 0.28 ± 0.14a 0.46 ± 0.17ab 0.97 ± 0.07ab 0.47 ± 0.16ab 7.91 ± 0.67d 0.06 ± 0.01a 0.22 ± 0.11a 0.29 ± 0.04a 0.05 ± 0.04a 0.11 ± 0.05a 3.31 3.96 119.62 p b 0.001

5.40 ± 3.80abc 12.82 ± 3.34cde 8.07 ± 0.66abc 20.15 ± 2.78ef 29.20 ± 13.16f 9.13 ± 2.22abc 9.25 ± 4.36abc 6.20 ± 2.00abc 13.86 ± 3.37cde 14.80 ± 0.67cde 8.54 ± 0.47abc 14.96 ± 0.15cde 10.40 ± 3.51bcd 13.96 ± 1.31cde 7.76 ± 0.79abc 0.77 ± 0.10a 1.21 ± 0.24ab 0.40 ± 0.09a 0.94 ± 0.21ab 6.18 ± 1.78abc 0.68 ± 0.34a 1.12 ± 0.40ab 2.35 ± 0.16ab 1.14 ± 0.40ab 19.20 ± 1.62de 0.15 ± 0.04a 0.54 ± 0.26a 0.71 ± 0.10a 0.11 ± 0.10a 0.26 ± 0.13a 7.34 7.74 105.41 p b 0.001

17.87 ± 1.30bcd 18.15 ± 7.2cd 6.72 ± 1.50abc 17.87 ± 1.30bcd 11.29 ± 3.04abcd 1.36 ± 0.18a 5.02 ± 0.27abc 3.57 ± 0.22abc 3.22 ± 0.17ab 4.19 ± 0.72abc 254.75 ± 4.46h 145.56 ± 5.36f 179.95 ± 8.13g 182.08 ± 8.47g 103.87 ± 1.73e 3.28 ± 0.20abc 9.06 ± 4.18abc 4.57 ± 2.01abc 1.93 ± 0.10a 3.33 ± 0.05abc 24.38 ± 18.39d 14.75 ± 2.83abcd 13.26 ± 2.41abcd 15.72 ± 1.77abcd 11.48 ± 1.01abcd 11.74 ± 2.37abcd 8.71 ± 0.36abc 8.80 ± 0.44abc 13.02 ± 2.05abcd 7.54 ± 0.56abc 36.90 64.96 176.05 p b 0.001

270.93 ± 117.99j 257.25 ± 60.00j 241.53 ± 32.75j 239.47 ± 17.12ij 42.84 ± 18.92abcd 120.85 ± 3.45defg 121.85 ± 5.91defg 124.81 ± 2.00defg 116.16 ± 4.57cdefg 104.98 ± 11.99bcdef 203.18 ± 17.22ghij 228.89 ± 24.01ij 181.11 ± 18.26fghij 273.46 ± 30.28j 224.71 ± 23.71hij 79.28 ± 8.68abcde 102.32 ± 30.22bcdef 82.29 ± 6.26abcde 85.97 ± 11.01abcde 73.14 ± 27.12abcde 108.82 ± 12.24cdef 131.79 ± 29.03defgh 123.07 ± 12.66defg 147.12 ± 6.15efghi 91.82 ± 2.85abcdef 61.61 ± 5.32abcde 41.47 ± 15.62abcd 12.59 ± 13.40ab 0.44 ± 0.76a 22.81 ± 5.88abc 130.55 82.33 63.07 p b 0.001

Chutney

Dried

Juice

Pickles

Preserves (jarred in brine)

AVG STD CV Significance level

Means with different superscripts in the same column differ significantly.


Product


49

Fig. 1. Principal component analysis of product and cultivar on the antioxidant content and capacity of cactus pear cladodes.

had a weak association with all the antioxidants and antioxidant potential results. It was observed from the PCA of the cladodes that the different processed products seem to cluster together, instead of fruit color or cultivar effects, except for the purple Robusta cultivar products that are closely associated with betalains. These results may also be, in part, ascribed to the different levels of concentration and therefore moisture contents in the different products and processes. Dried products were the best in terms of antioxidant content and capacity. This is in agreement with the findings of Vinson et al. (2005) who found that dried products have a greater nutrient density and significantly more phenol antioxidant content than fresh products. Dried products also have a longer shelf life, contain complex carbohydrates and are high in fiber. Due to the lifestyle of modern people, convenience foods are becoming more popular. Consequently, dried products are extremely popular because of the light weight, shelfstability and small size (Sharma et al., 2011). Dried cladodes retain antioxidant activity after the heat induced dehydration process (Medina-Torres et al., 2011), after being ground into cladode flour and are used in baked products (Ayadi et al., 2009; Santos-Zea et al., 2011). Phenolic levels were higher in cladodes than in fruit (du Toit, 2013; du Toit et al., 2015). Fresh cladodes had the highest levels and drying was the best process for preserving phenolics. Thus, fresh or dried cladodes would be the choice for high phenolics content in the cactus pear plant. Antioxidant capacity in processed cactus cladode products were exceptionally high, in fact some processed products were comparable to or higher than the fresh counterparts. This was seen before in studies concerning processed fruit by Rickman et al. (2007a, 2007b), Ryan and Prescott (2010) and Jaramillo-Flores et al. (2003). Though cladodes are not used as food in South Africa, processed cladodes are excellent sources of antioxidants: in fact, processed cladodes are a better source than fresh cladodes probably because mucilage present in cladodes captures antioxidants. These are, however released with the heat treatments required in processing techniques (Jaramillo-Flores et al., 2003).

Purple fruit cultivar cladodes tested the highest in % DPPH, % chelating activity, betalains, carotene and phenolics. In orange and pink fruit cultivar cladodes, it was ascorbic acid that dominated. Purple (first) and orange (second) were therefore the colors of cactus fruit cultivars that could be the best choice in terms of antioxidant content. In cladodes, Robusta had the highest ascorbic acid and betalain content, but had the lowest carotene and phenolic content. Ofer and GymnoCarpo were the cultivars that had the most consistently high antioxidant contents in cladodes, as it had fairly high ascorbic acid, phenolic and betalain values and the highest carotene values. Ofer cladode products were determined in this study to be the best choice in terms of high antioxidant cladode products. Processing had a greater influence on the antioxidant content of cactus cladode products than the influence of cultivar or color.

4. Conclusions From this study no specific cultivar emerged as one with outstanding antioxidant properties, content or capacity. All cultivars demonstrated high antioxidant capacities and consequently, the cladodes of any cultivar could be considered as suitable for processing or preserved to produce healthy products. Regarding fruit color, the highest antioxidant content and -capacity were found in cladodes from orange and purple fruit bearing cultivars. Processing had a greater influence on the antioxidant content of cactus cladode products than the influence of cultivar. Dried products were the best in terms of antioxidant content and capacity. Processed cladodes, more than fresh cladodes, from all the cultivars, were concluded to provide an excellent source of antioxidants and could be suggested for products such as cladode flour and pickles. Based according to the data, the following recommendations can be made: dried products made from cladodes of any cultivar/color as well as pickles from cladodes of any cultivar.

50


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