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2Centro de Investigaciones Químicas de la Universidad Autónoma del Estado de Hidalgo (CIQ-UAEH), Pachuca, Hidalgo, México. 3CEPROBI, Carretera ...
Journal of Food Processing and Preservation ISSN 1745-4549

CAROTENOID CONTENT, ANTIOXIDANT ACTIVITY AND SENSORY EVALUATION OF LOW-CALORIE NOPAL (OPUNTIA FICUS-INDICA) MARMALADE jfpp_589

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GONZÁLEZ-CRUZ LEOPOLDO , FILARDO-KERSTUPP SANTIAGO , BELLO-PÉREZ LUIS ARTURO3, GÜEMES-VERA NORMA4 and BERNARDINO-NICANOR AUREA1,5 1

Instituto Tecnológico de Celaya, Departamento de Ingeniería Bioquímica, Celaya, Guanajuato 38010, Mexico Centro de Investigaciones Químicas de la Universidad Autónoma del Estado de Hidalgo (CIQ-UAEH), Pachuca, Hidalgo, México 3 CEPROBI, Carretera Yautepec-Jojutla, Yautepec, Morelos, México 4 Centro de Investigaciones en Ciencia y Tecnología de los Alimentos de la Universidad Autónoma del Estado de Hidalgo (CICyTA-UAEH), Tulancingo, Hidalgo, México 2

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Corresponding author. TEL: +52-461-611-7575; FAX: +52-461-611-7979; EMAIL: [email protected] Accepted for Publication August 10, 2011 doi:10.1111/j.1745-4549.2011.00589.x

ABSTRACT In this study, low-calorie nopal marmalades were analyzed to evaluate the effect of storage conditions on the carotenoids in terms of sensory and chemical properties and antioxidant activity. The results showed that the sensory characteristics of all nopal marmalades were similar to the marmalades that were elaborated with sucrose; the spreadability capacity of the nopal marmalades is better. The concentration of nopal influenced both the chemical characteristics as the concentration and antioxidant activity of carotenoids in the marmalade. The thermal treatment increased the extractability of the carotenoids, principally of b-carotene and lutein. The temperature and storage time led to a decrease in the concentration of b-carotene and lutein, while the concentration of a-cryptoxanthin increased, possibly due to the dehydroxylation of lutein. In conclusion, the antioxidant properties of nopal are maintained in the thermal treatment used for the elaboration of the marmalades, and the product is stable for 3 months.

PRACTICAL APPLICATIONS Nopal is an important vegetable that is used for human consumption in Central American countries for their high content of fiber, carotenoids and soluble carbohydrates. However, it is a seasonal vegetable, and its consumption is restricted to a few months of the year for the elaboration of typical foods. For this reason, low-calorie marmalades can be an option for expanding the consumption of nopal in other countries throughout the entire year without significantly altering its nutraceutical properties (antioxidant activity, fiber benefits and provitamin A). On the other hand, the utilization of low-calorie sweeteners permits this product to be consumed as a nutraceutical pudding without any restrictions.

INTRODUCTION Mexico is the diverse center of the Opuntia genus, where 83 species have thrived and have become an important food in the inhabitants’ diet, particularly in the arid zones. However, the applications of these plants are diverse, including the most

studied medicinal uses that are due to the hypoglycemic effect. In the evaluation of the hypoglycemic effect, different species have been used (Granados and Castañeda 2003), such as the Opuntia ficus-indica (Ibañez-Camacho and Roman-Ramos 1979; Frati-Munari et al. 1989), Opuntia streptacantha (Castañeda-Andrade et al. 1997), Opuntia

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fuliginosa (Trejo-González et al. 1996) and Opuntia megacantha (Bwititi et al. 2000). Additionally, the nopal is also an important fiber source (8.27–21.45% dry matter [DM]) (Scheinvar et al. 2009), and several studies have shown a beneficial effect for hypercholesterolemic individuals (FratiMunari et al. 1983; Cárdenas-Medellin et al. 1998; Galati et al. 2003). Furthermore, three carotenoids, lutein, b-carotene and a-cryptoxanthin (Jaramillo-Flores et al. 2003), have been identified in nopal. These compounds are important in human metabolism because of their antioxidant activities and their role as modulators in processes related to mutagenesis, cell differentiation and proliferation (Reza and Clemens 2001). In addition, the carotenoids can reduce lipid peroxidation, as well as protein, DNA and enzyme damage (Hüsnü 2003). Apparently, the antioxidant activity in carotenoids is due to the presence of conjugated double bonds, and those with more than 11 double bonds (e.g., b-carotene, cryptoxanthin, lutein, lycopene and zeaxanthin) are more efficient (Palace et al. 1999). However, the processing and storage of foods that contain carotenoids can cause losses in antioxidant activity, because of factors such as the processing temperature, water activity, food matrix, light, isomerization promoter acids, antioxidants and pro-oxidants and available oxygen (Rodriguez-Amaya 1997). Considering the great amount of nutraceutical compounds that are present in the nopal, it is important to develop new products that can take advantage of the nutraceutical properties. Thus, the utilization of ingredients that increase the positive effects is important. However, it is also important to consider the effects of diverse treatment used during the processing, because nopal that has undergone heat treatment has a greater hypoglycemic effect than fresh nopal (Frati-Munari et al. 1989), whereas the extractability of carotenoids in thermally treated nopal is greater than that of fresh nopal (Jaramillo-Flores et al. 2003). However, few studies have focused on evaluating this technological process. Therefore, the objective of this study was to evaluate the effect of the elaboration process of low-calorie nopal marmalade on the concentration of carotenoids and their antioxidant activity and access the effect of storage on their chemical and sensory stability.

MATERIALS AND METHODS Vegetative Material Young cladodes from O. ficus-indica var. Copena F-1 were obtained from Cuautepec, Hidalgo (Mexico). The nopalitos were harvested manually at 8:00 a.m.and selected according to size (about 20 cm long) for a homogeneous state of maturity (Nobel 1998; Granados and Castañeda 2003). The samples were stored at 4C in a refrigerator (LG, Model GR-452SH, LG Electronics México) until used (always less than 24 h).

Marmalade Formulation The cladodes were taken randomly and cut into 1 cm3 cubes, and placed in boiling water for 30 min. The cubes were filtered to eliminate the mucilage and placed in an industrial blender with water in a 50:50 (w/v) ratio, where they were evenly ground to obtain a homogeneous paste (base mix). After adding the ingredients indicated in Table 1 (according to Filardo-Kerstupp et al. 2007), the samples were thermally treated for 35 min at 90C and then packaged in 250 g glass bottles. Lot 1 was analyzed immediately for the time 0 sample, and lots 2 and 3 were used for the study of storage stability. All analyses were performed in triplicate.

Storage Stability The marmalades were stored at 25C and 37C for 90 days, and the chemical changes were evaluated according to the methodology established in the AOAC (1990), and the following were determined: reducing sugars (method 925.36), pH (potentiometer), titratable acidity (method 942.15) and soluble solids in °Brix (method 932.12).

Sensory Analysis The sensory analysis was determined using a multiple comparisons method (discriminate test) by 30 judges who did not receive prior training (Anzaldúa-Morales 2005). The marmalade elaborated with sucrose was used as the standard, and a value of 5 was assigned to this sample. A higher value (6–10)

TABLE 1. MARMALADE FORMULATION Formulation (%)

F1

F2

F3

F4

Base mix Low Methoxyl Pectin (LMP) (Classic AF 710, Herbstreith & Fox, Neuenbürg/Württ, Germany) Modified Starch (Kol-Guard™ 7413; Almidones Mexicanos S.A de C.V., México) Stevia (Esvita®; Promoción Naturista; México) Xylitol (COINA; México) Lactitol (Ferbera; México) Aspartame (Aspartame FCC Powder; COINA, México)

87.40 0.60

79.40 0.60

66.30 0.60

66.00

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2.00 12.00 15.90 4.10

33.00 0.10

31.90 0.10

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was assigned when the judges indicated that the low-calorie marmalade had better sensory characteristics than the standard sample, and a lower value (0–4) was assigned if the sensory characteristics were inferior to the standard sample. Statistical analyses were carried out using the Statistical Analysis System (SAS Institute Inc., Cary, NC) v.8. Differences between the sample means were analyzed by a one-way analysis of Tukey at P ⱕ 0.05.

Extraction and Quantification of Carotenoids The composition of carotenoides in the fresh nopal and marmalades was determined by the method described by Mercadante and Rodriguez-Amaya (1990). Seven grams of fresh nopal and 14 g of marmalade were macerated with Celite® (Johns-Manville Co., Denver, CO) and 45 mL of cold acetone (4C) and vacuum-filtered. The residue was re-extracted twice more with cold acetone. A small portion of the combined filtrates was mixed with 50 mL of petroleum ether in a separatory funnel, and 200 mL of bidistilled water was then added slowly. The water–acetone phase was discarded, and another portion of the acetone extract was added. This operation was repeated until all the extract was transferred into the petroleum ether. The ether phase was washed four times with water to remove all the acetone. The residual water in the ether was eliminated with anhydrous sodium sulphate (RodriguezAmaya 1999). The extract was concentrated to dryness with high purity nitrogen (99.99%). The carotenoids were quantified by high-performance liquid chromatography (HPLC). The equipment consisted of a Beckman System Gold Liquid Chromatograph with a Model 168 UV-Vis detector and a Gold Nouveau V 1.72 Chromatographic Data System (Beckman Coulter, Fullerton, CA). The equipment also included also Prodigy 5 ODS2 column 25 cm ¥ 4.6 mm ID (Phenomenex, Torrance, CA) along with a solvent system consisting of acetonitrile : methanol : tetrahydrofuran (58:35:7) pumped at a flow rate of 1 mL/min for 35 min. Injected solutions consisted of 20 mL of carotenoid extract in 5 mL of acetone, and the visible detection was performed at 450 nm. The quantification was performed using the external standard methods using b-carotene, a-cryptoxanthin and lutein as external standards. The concentrations of these standards were determined spectrophotometrically and later injected into the HPLC, and the areas were measured (Bushway 1985).

Antioxidant Activity Carotenoid dried extracts from fresh nopal (7 g samples) and marmalade (14 g samples) were suspended in 5 mL of methanol, and 40 mL of this suspension was mixed with 3 mL of a reaction emulsion (300 mg of b-carotene and 40 mg of linoleic acid in 100 mL of 30% hydrogen peroxide). Absor-

CHANGES IN LOW-CALORIE NOPAL MARMALADE

bance readings were performed at 470 nm after 0, 15, 30 and 45 min. This assay tests the ability of the extracts to inhibit oxidation of the b-carotene–linoleate emulsion through the scavenging of peroxyl radicals (Lee et al. 1995). A blank was prepared using 40 mL of methanol.

Statistical Analysis The quantitative data were expressed as the mean ⫾ standard deviation, and the analysis of variance (ANOVA) was carried out followed by a Tukey’s test. SAS software was used for the data analysis, and all experimental determinations were assayed in triplicate.

RESULTS AND DISCUSSION The caloric value in the marmalades, according to the previous work (Filardo-Kerstupp et al. 2007), indicate that the marmalades F1 (426 cal/kg) and F2 (636 cal/kg) can be considered low-calorie products according to the Code of Federal Regulations Title 21(FDA), as they contain less than 800 cal/ kg. However, formulations F3 (942 cal/kg) and F4 (842 cal/ kg) are considered reduced-calorie products because they contain less than 25% of the caloric value of standard marmalade (made with sucrose, 2,380 cal/kg) but contain more than 800 cal/kg (GPO U.S. 2005). The difference in the caloric value of marmalades is due to the concentration of nopal and the type and quantity of sweetener used. Thus, marmalade F3 showed the highest caloric content, while marmalade F1 showed the lowest caloric content. When aspartame was used in the maximum concentration established in the codex alimentarius, it is necessary to increase the lactitol concentration to maintain the sensory characteristics in the marmalades; therefore, the addition of lactitol provides increases of approximately 2 cal/g to the caloric value (Bender and Bender 1999). On the other hand, the combination of sweeteners (xylitol–lactitol) permits a reduction in the quantity of sweeteners,which diminishes the caloric value in marmalade F2 due to the synergetic action of the sugars alcohols. Other studies have reported that the presence of a crystallization inhibitor and texturizer such as maltodextrin can increase the caloric value of marmalades as in the case of the elaborate with Sechium edule (Gajar and Badrie 2001), which showed a higher caloric value (768 cal/kg) than jams F1 and F2 of this study (426 and 636 cal/kg, respectively). The work of Abdullah and Cheng (2001) reports that using acesulfame K and sorbitol in marmalades in combination with tropical fruits, the caloric value of 1,060 cal/kg was also higher than any of the samples obtained with nopal. These results indicate the feasibility of obtaining products with minor caloric value. This allows maximizing the nutraceutical properties of nopal. However, it is important to maintain similar characteristics to the products made with sucrose.

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Sensory Characteristics of Nopal Marmalades The results obtained from the sensory analysis of the lowcalorie marmalades (Table 2) did not show significant variation in odor, flavor and color with respect to the standard marmalades. However, the spreadability was higher in all lowcalorie marmalades compared with the standard marmalade. This behavior indicates that the sweeteners used in all formulations do not have a significant influence on the acceptance parameters. However, the gelling agent used in the elaboration of low-calorie marmalades is a determinant factor in obtaining a product with the best spreadability. Since the addition of LM pectins (F1, F2 and F3) or modified starch (F4) permits a better gel network formation, the LM pectins create cavities between them due their shape, which become occupied by carboxyl and hydroxyl groups. For this reason, the interaction of low methylester pectins with calcium ions from the nopal is favored (Rolin 1993). On the other hand, the presence of water-soluble polysaccharides such as pectin and polysaccharides from nopal mucilage favored the spreadability of marmalade with modified starch elaborated (F4) (Linden and Lorient 2000).This behavior is due to the synergistic effects of the gelling agents and the pectins that are present in the nopal. On the other hand, considering the fact that the pectins present in the nopal are LM pectins (Goycoolea and Cárdenas 2003; Piga 2004), the high concentration of calcium in the nopal is an important factor for maintaining the integrity of the pectin gel network. For this reason, even in sample 4, which utilized modified starch, the pectic substances of nopal generated too much synergy in the gel network formation.

This characteristic, in addition to the sensory characteristics provided by the sweeteners, increases the acceptability of the marmalades. On the other hand, low pH values increase the shelf life of the marmalades because the development of microorganisms is inhibited at pH values below 4. Thus, considering this chemical characteristic, the best formulations are F1 and F2 (Fig. 1A). However, the formulations F3 and F4 are in the pH range that is adequate for diminished microorganism development. On the other hand, the pH value is important in the gelation process because the low methoxyl pectins need a pH value between 2.8 and 6. Therefore, characteristics obtained in all formulations of nopal marmalades were evaluated, such as the unnecessary addition of acid in comparison with S. edule marmalades to which acid was added for a diminished pH value of 6.3 to 3.6 (Gajar and Badrie 2001). However, it is important to have an appropriate calcium concentration to allow the interactions between the methoxy groups of the pectins (Thakur et al. 1997). This condition is

Effect of the Storage Time on the Changes in the Chemical Characteristics of the Marmalades In general, all marmalades had acidic pH values; this is possibly due to the fact that the nopal tissues tend to release acids during the heat treatment (Granados and Castañeda 2003).

TABLE 2. SENSORY CHARACTERISTICS IN LOW-CALORIE MARMALADES Sample

Color

Odor

Flavor

Spreadability

Standard marmalade F1 F2 F3 F4

5.00a,b 4.50b 4.70b 5.63a 4.33b

5.00a,b 4.70b 5.50a 4.86a,b 4.80a,b

5.00a 5.90a 5.66a 5.83a 5.13a

5.00c 6.96b 7.33a,b 6.93b 7.66a

Different letters in each column indicate significant statistical differences (P ⱕ 0.05).Higher scores mean better sensory characteristics. Scores above 5 meant that samples tasted/scored better than the reference sample.

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FIG. 1. CHEMICALS CHANGES IN MARMALADES AFTER STORAGE TIME AT 25C AND 37C IN COMPARISON WITH TIME 0 SAMPLE (INITIAL) (A) pH. (B) Soluble solids.

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fulfilled by the nopal since the calcium concentration has been reported to be between 1.5 to 5.9% in the DM (Guzmán and Chávez 2007; Rodríguez-Garcia et al. 2007). This is because unlike blackberry (Rubus irasuensis Lebm) marmalades (Acosta et al. 2006), calcium addition was not necessary for the gel formation. However, it is important to control the amount of acid, because high concentrations of pectin in foods with a pH above 4 may cause pectin precipitation (Thakur et al. 1997). However, the soluble solids in the marmalades were apparently not an important parameter in the stability of nopal marmalades. Therefore, the soluble solids were kept constant during storage time (Fig. 1B), and this was different from the behavior seen in marmalades made with vegetables with minor quantities of pectin and calcium. This was the case of S. edule marmalades, in which a reduction in the pH and soluble solids values were observed after 28 days (Gajar and Badrie 2001), causing syneresis. In the nopal marmalades, this behavior was not observed, due to the concentration of pectin present in the nopal (13.8 % DM) (Granados and Castañeda 2003), which permits a better gel formation; similar results were obtained in marmalades with different fruits pulps (Singh et al. 2009).

Extraction and Quantification of Carotenoids Three major carotenoids were identified in the fresh nopal and marmalades: lutein, b-carotene and a-cryptoxanthin (Fig. 2). The total carotenoid content in the fresh nopal (Fig. 2A) was determined by chromatography to be 247.8 ⫾ 3.69 mg/g in DM, and these values correspond to 36 % of b-carotene, 19 % of a-cryptoxanthin and 45 % of lutein. The content of these pigments were higher than the ones reported by Jaramillo-Flores et al. (2003) (231.8 mg/g DM). These differences can be due to the variety and the location where the nopal was cultivated, because these two variables can influence their concentration (Rodriguez-Amaya 1993). On the other hand, the thermal treatment originates changes in the chromatographic pattern (Fig. 2B). This is due to the isomerization in some carotenoids. Therefore, compounds that are not present in the fresh nopal appear in the marmalade. However, two compounds that were present in the fresh nopal disappeared, which indicates that it is important to evaluate the effects of a production process on the raw materials so that the food quality of the new products can be determined. Due to the thermal treatment, the total carotenoid concentration was higher in the marmalades than the fresh nopal, in particular, b-carotene and lutein (Tables 3 and 4). These changes may be due to a diminished interference of the mucilage on the carotenoid determination, because the carotenoids can form complexes with some components that are present in the mucilaginous compounds (Rock and Swend-

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seid 1992; Jaramillo-Flores et al. 2003). On the other hand, an increase in the temperature causes destabilization from the nopal mucilage structure and allows the cell to rupture (Cárdenas et al. 2008). Other events can also occur such as thermal denaturation of the carotenoid–protein complexes and tissue softening and changes in the morphology, which allow a higher penetration of the organic solvents into the cells and enhances the extraction (Khachik et al. 1992; Jaramillo-Flores et al. 2003; Mayer-Miebach and Behsnilian 2006). As regards the individual carotenoid content, the bcarotene in the marmalades showed significant differences that increases in the range of 80 to 130% compared with the initial marmalades.With respect to lutein,the range is between 90 and 143%. This corroborates that the thermal treatment causes rupture in the carotenoid complexes, which leads to the release of more carotenoids from the nopal matrix. On the other hand, the thermal treatment caused a decrease in the concentration of a-cryptoxanthin in three marmalades samples F2, F3 and F4 (Table 5). This behavior can be due to the water concentration in the formulation in addition to the thermal treatment used. A similar behavior was reported for maize (Scott and Eldridge 2005); however, the water concentration is apparently the determining factor because this behavior was not observed in the sample with low water concentration (F1). These results suggest that a-cryptoxanthin is more susceptible to hydrolysis in the oxidation processes (Rodriguez-Amaya 1999) than lutein or b-carotene. The carotenoid content in nopal marmalade can be considered a contribution that complements the requirements for vitamin A (3 mg/day or 2 mg/day for men or women, respectively), because the samples F1 and F3 contain 0.345 mg and 0.276 mg, respectively (considering a conversion factor of b-carotene to vitamin A of 12:1) (de Pee et al. 1998). However, the contribution by portion of marmalades is only 10 and 15% of the daily requirements for men or women, respectively, and is lower than some types of green leaves that can contribute up to 53% of the daily requirement (Weinberger and Msuya 2004). However, considering that this product comes in the form of a pudding, the contribution of vitamin A is important. The storage has a significant effect on the concentration of carotenoids from the marmalade, causing a reduction in the b-carotene and lutein concentration in the ranges of 13.49– 18.03% and 1.71–24.41%, respectively. In comparison with the initial sample, these data are consistent with those reported for carrot juice (stored at 25 and 35C). In this study, it is most evident that there is greater destruction of carotenoids at 25C and 35C than at 4C (Chen et al. 1996). On the other hand, the storage conditions can also cause isomerization reactions. The principal factors of these reactions are light, content or activity of water and enzymatic or

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FIG. 2. CHROMATOGRAPHIC PROFILE OF CAROTENOID (A) Nopal fresh. (B) Processing (marmalade). b, b-carotene; a, a-cryptoxanthin; L, lutein.

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Table 3. b-CAROTENE CONCENTRATION (mg/g DRY MATTER, Mean ⫾ SD n = 3)

CHANGES IN LOW-CALORIE NOPAL MARMALADE

Treatment Fresh nopal Initial 25C* 37C*

F1

F2 c

90.40 + 0.02 207.32 + 1.80a 207.36 + 2.19a 179.52 + 4.56b

F3 c

90.40 + 0.03 195.82 + 3.66a 161.83 + 4.46b 160.51 + 4.26b

F4 c

90.40 + 0.04 166.61 + 6.18a 148.74 + 4.10b 140.55 + 4.22b

90.40 + 0.05d 166.64 + 2.49b 175.82 + 1.66a 142.98 + 4.92c

* Storage time = 90 days. Different letters in each column indicate significant statistical differences (P ⱕ 0.05).

TABLE 4. LUTEIN CONCENTRATION (mg/g DRY MATTER, MEAN ⫾ SD n = 3)

Treatment Fresh nopal Initial 25C* 37C*

F1

F2 c

111.03 + 1.23 270.58 + 0.06a 273.75 + 1.82a 265.94 + 2.43b

F3 c

111.03 + 1.24 240.01 + 0.53a 223.93 + 3.69b 214.21 + 8.52b

F4 d

111.03 + 1.25 248.30 + 1.44a 230.82 + 2.31b 187.68 + 4.57c

111.03 + 1.26d 212.90 + 0.49a 193.82 + 0.51b 175.89 + 1.36c

* Storage time 90 days. Different letters in each column indicate significant statistical differences (P ⱕ 0.05).

TABLE 5. a-CRYPTOXANTHIN CONCENTRATION (mg/g DRY MATTER, MEAN ⫾ SD n = 3)

Treatment Fresh nopal Initial 25C* 37C*

F1

F2 c

46.37 + 2.43 77.71 + 1.90a 57.74 + 0.91b 54.34 + 2.88b

F3 b

46.37 + 2.44 32.25 + 0.71c 44.72 + 1.96b 54.28 + 1.20a

F4 c

46.37 + 2.45 34.88 + 0.64d 51.51 + 1.77b 62.91 + 1.27a

46.37 + 2.46b 36.87 + 0.77c 51.17 + 0.24a 54.30 + 1.96a

* Storage time 90 days. Different letters in each column indicate significant statistical differences (P ⱕ 0.05).

nonenzymatic oxidations. These conditions can originate isomerization of the trans-carotenoids to the cis-carotenoids or carotenoid fragmentations, leading to the formation of small molecular weight compounds (Rodriguez-Amaya 1993, 1999; Chen et al. 1996). The concentration of a-cryptoxanthin showed an increase between 23.5 and 80.3% compared with the initial sample, which can be attributed to the dehydroxylation of lutein, because it has demonstrated that it is one of the previous reactions to the fragmentation and subsequent generation of aromatic compounds (Sánchez-Contreras et al. 2000).

Antioxidant Activity The antioxidant activities in all the nopal marmalades were higher than those of the fresh nopal, which is attributed to the increase in the concentration of carotenoids from 68 to 124% Table 6. EFFECT OF THE STORAGE CONDITIONS ON THE ANTIOXIDANT ACTIVITY IN FRESH NOPAL AND NOPAL MARMALADES

by the effect of thermal treatment (Table 6). However, it is important to consider the storage conditions because they may decrease the antioxidant activity considerably as in the case of the samples stored to 37C. On the other hand, the marmalade composition is also an important factor, whereas the samples with the highest nopal concentration (F1 and F2) showed a minor decrease in the antioxidant activity (40%) with respect to the marmalades with lower concentration of nopal (F3 and F4), in which the reduction was 50%. The reduction in the antioxidant activity in the marmalades that were stored for 90 d at 37C can be due to the decrease in the total content of carotenoids in all marmalade samples in the range between 9 and 14%. This behavior is in concordance with the previous results that indicate that the decrease in the content of carotenoids is minor at lower temperatures compared to temperatures higher than 20C (Blessington et al. 2010).

Treatment

F1

F2

F3

F4

Fresh nopal Initial 25C* 37C*

30.38 + 1.19c 54.53 + 1.78a 54.73 + 1.74a 39.09 + 3.57b

30.38 + 1.19b 53.21 + 2.08a 51.67 + 2.63a 37.08 + 4.59b

30.38 + 1.19b 47.05 + 1.95a 47.21 + 4.71a 24.52 + 5.16b

30.38 + 1.19b 39.63 + 1.09a 42.99 + 3.49a 19.47 + 3.75c

* Storage time 90 days. Different letters in each column indicate significant statistical differences (P ⱕ 0.05).

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CONCLUSIONS Two of the obtained nopal marmalades can be considered low-calorie products (426 cal/kg and 636 cal/kg), with similar sensory characteristics of color, odor and flavor to the standard marmalade standard. However, the spreadability was higher in all low-calorie samples. The chemical characteristics of the marmalades were influenced by the nopal concentration used in the formulation. The thermal processing used to obtain the nopal marmalades increased the b-carotene and lutein extraction; nevertheless, a decrement in the a-cryptoxanthin concentration was observed. The storage caused a decrease in the b-carotene and lutein concentrations and an increase in the a-cryptoxanthin concentration. The increment in cryptoxanthin may have been due to the dehydroxylation of lutein, which is a reaction that occurs during aroma formation. The thermal processing in the marmalade elaboration increases the extractability of carotenoids, which caused an increase in the antioxidant activity in comparison with the fresh nopal. However, the storage temperature generates changes in the carotenoid structure, which caused a reduction in their antioxidant activity, most evidently at 37C.

REFERENCES ABDULLAH, A. and CHENG, C.T. 2001. Optimization of reduced calorie tropical mixed fruits jam. Food Qual. Pref. 12(1), 63–68. ACOSTA, O., VÍQUEZ, F., CUBERO, E. and MORALES, I. 2006. Ingredient levels optimization and nutritional evaluation of a low-calorie Blackberry (Rubus irasuensis Liebm) jelly. J. Food Sci. 71(5), S390–S394. ANZALDÚA-MORALES, A. 2005. La Evaluación Sensorial de los Alimentos en la Teoría y la Práctica. 82, Acribia. Barcelona, España. AOAC 1990. Official Methods of Analysis, 15th Ed., Association of Official Analytical Chemists, Arlington, VA. BENDER, A.D. and BENDER, E.A. 1999. Benders’ Dictionary of Nutrition and Food Technology, 7th Ed., Cambridge, England. 463 p. BLESSINGTON, T., NZARAMBA, M.N., SCHEURING, D.C., HALE, A.L., REDDIVAR, L. and MILLER, J.C. 2010. Cooking methods and storage treatment of potato: effects on carotenoids antioxidant activity and phenolics. Am. J. Pot. Res. 87, 479–491. BUSHWAY, R.J. 1985. Separation of carotenoids in fruits and vegetables by High Performance Liquid Chromatography. J. Liq. Chromatogr. 8, 1527–1547. BWITITI, P., MUSABAYANE, C.T. and NHACHI, C.F. 2000. Effects of Opuntia megacantha on blood glucose and kidney function in streptozotocin diabetic rats. J. Ethnopharmacol. 69(3), 247–252.

274

CÁRDENAS, A., GOYCOOLEA, M.F. and RINAUDO, M. 2008. On the gelling behaviour of “nopal” (Opuntia ficus indica) low methoxyl pectin. Carbohydr. Polym. 73(2), 212–222. CÁRDENAS-MEDELLIN, M.L., SERNA, S.S.O. and VELAZCO DE LA GARZA, J. 1998. Effect of raw and cooked nopal (Opuntia ficus indica) ingestion on growth and profile of total cholesterol, lipoproteins, and blood glucose in rats. Arch. Latinoam. Nutr. 48(4), 316–323. CASTAÑEDA-ANDRADE, I., GONZÁLEZ-SANCHEZ, J. and FRATI-MUNARI, A.C. 1997. Hypoglycemic effect of an Opuntia streptacanta Lemaire Dialysate. J. PACD. 2, 73–75. CHEN, H.E., PENG, H.Y. and CHEN, B.H. 1996. Stability of carotenoids and vitamin A during storage of carrot juice. Food Chem. 57(4), 497–503. DE PEE, S., WEST, C.E., PERMAESIH, D., MARTUTI, S. and HAUTVAST, J.G. 1998. Orange fruit is more effective than are dark-green, leafy vegetables in increasing serum concentrations of retinol and b-carotene in schoolchildren in Indonesia. Am. J. Clin. Nutr. 68(5), 1058–1067. FILARDO-KERSTUPP, S., SHEINVAR, L., GONZÁLEZ-CRUZ, L., BERNARDINO-NICANOR, A., ZÚÑIGA, E.A., CRUZ, M.B. and ARRIETA, A.M. 2007. Desarrollo de una mermelada de nopal (Opuntia ficus indica) rica en fibra y baja en calorías. Industria Alimentaria. Abril-Mayo. FRATI-MUNARI, A.C., DEL VALLE-MARTÍNEZ, L.M., ARIZA-ANDRACA, C.R., ISLAS-ANDRADE, S. and CHÁVEZ-NEGRETE, A. 1989. Hypoglycemic action of different doses of nopal (Opuntia streptacantha Lemaire) in patients with Type II diabetes mellitus. Arch. Invest. Med. (Mex). 20(2), 197- 201. FRATI-MUNARI, A.C., FERNÁNDEZ-HARP, J.A., DE LA RIVA, H., ARIZA-ANDRACA, R. and DEL CARMEN-TORRES, M. 1983. Effects of nopal (Opuntia sp.) on serum lipids, glycemia and body weight. Arch. Invest. Med. (Mex). 14(2), 117–125. GAJAR, A.M. and BADRIE, N. 2001. Processing and quality evaluation of a low-calorie christophene jam (Sechium edule(Jacq.) Swartz. J. Food Sci. 67(1), 341–346. GALATI, E.M., TRIPODO, M.M., TROVATO, A., D’AQUINO, A. and MONFORTE, M.T. 2003. Biological activity of Opuntia ficus indica cladodes II: effect on experimental Hypercholesterolemia in rats. Pharm. Biol. 41(3), 175–179. GOYCOOLEA, M.F. and CÁRDENAS, A. 2003. Pectins from Opuntia spp: a short review. J. PACD. 5, 17–29. GPO U.S. 2005. Code of federal regulations (CFR). Washington, D.C.:U.S. GPO. Available on the internet http://frwebgate3. access.gpo.gov/cgi-bin/TEXTgate.cgi?WAISdocID=E8NQmj/ 18/1/0&WAISaction=retrieve (accessed July 20, 2009). GRANADOS, S.D. and CASTAÑEDA, A.P. 2003. Historia, Fisiología, Genética e Importancia del Nopal, p. 227, Editorial Trillas, México, DF. GUZMÁN, L.D. and CHÁVEZ, J. 2007. Estudio bromatológico del cladodio de nopal (Opuntia ficus-indica) para el consumo humano. Rev. Soc. Quím. Perú 73(1), 41–45.

Journal of Food Processing and Preservation 36 (2012) 267–275 © 2011 Wiley Periodicals, Inc.

G-C. LEOPOLDO ET AL.

HÜSNÜ, C.B.K. 2003. Industrial plants as source of dietary supplements. In Dietary Supplements of Plant Origin. A Nutrition and Health Approach (M. Maffei, ed.) pp. 31–42, Taylor & Francis, New York. IBAÑEZ-CAMACHO, R. and ROMAN-RAMOS, R. 1979. Hypoglycemic effect of Opuntia cactus. Arch. Invest. Med (Mex). 10(4), 223–230. JARAMILLO-FLORES, M.E., GONZÁLEZ-CRUZ, L., DORANTES-ÁLVAREZ, L., GUTIÉRREZ-LÓPEZ, G.F. and HERNÁNDEZ-SÁNCHEZ, H. 2003. Effect to the thermal treatment on the antioxidant activity and content of carotenoids and phenolic compounds of cactus pear cladodes (Opuntia ficus-indica). Food Sci. Tech. Int. 9(4), 271–278. KHACHIK, F., GOLI, M.B., BEECHER, G.R., HOLDEN, J., LUSBY, W.R., TENORIO, M.D. and BARRERA, M.R. 1992. Effect of food preparation on qualitative and quantitative distribution of major carotenoid constituents of tomatoes and several green vegetables. J. Agric. Food Chem. 40(3), 390–398. LEE, Y., HOWARD, L. and VILLALÓN, B. 1995. Flavonoids and antioxidant activity of fresh pepper (Capsicum annum) cultivars. J. Food Sci. 60, 473–476. LINDEN, G. and LORIENT, D. 2000. New Ingredients in Food Processing, pp. 242–262, CRC Press, Boca Raton, FL. MAYER-MIEBACH, E. and BEHSNILIAN, D. 2006. Stability and bioavailability of lycopene, lutein and zeaxanthin in fruits and vegetables as affected by thermal processing. Stewart Postharvest Rev. 5, 13–23. MERCADANTE, A.Z. and RODRÍGUEZ-AMAYA, D.B. 1990. Carotenoid composition and vitamin A value of some native Brazilians green leafy vegetables. Int. J. Food Sci. Tech. 25, 213–219. NOBEL, P.S. 1998. Los incomparables Agaves y Cactos, pp. 59–94, Editorial Trillas, México. PALACE, V.P., KHAPER, N., QIN, Q. and SINGAL, P.K. 1999. Antioxidant potential of vitamin A and carotenoids and their relevance to heart disease. Free Radic. Biol. Med. 26(5–6), 746–761. PIGA, A. 2004. Cactus Pear: a fruit of nutraceutical and functional importance. J. PACD. 6, 9–22. REZA, W.A. and CLEMENS, M.R. 2001. Effect of dietary phytochemicals on cancer development. In Vegetables, Fruits, and Herbs in Health Promotion (R.R. Watson, ed.) pp. 3–20, ed) CRC Press, New York. ROCK, C.L. and SWENDSEID, M.E. 1992. Plasma b-carotene response in humans after meals supplemented with dietary pectin. Am. J. Clin. Nutr. 55, 96–99. RODRIGUEZ-AMAYA, D.B. 1993. Nature and distribution of carotenoids. In Foods. In Shelf Life Studies of Foods and

CHANGES IN LOW-CALORIE NOPAL MARMALADE

Beverages. Chemical, Biological, Physical and Nutritional Aspects (G. Charalambous, ed.) pp. 547–589, Elsevier Science Publishers, Amsterdam. RODRIGUEZ-AMAYA, D.B. 1997. Carotenoides and food preparation: the retention of provitamin A carotenoides in prepared, processed and stored foods, USAID, Brazil. 39–49. RODRIGUEZ-AMAYA, D.B. 1999. Changes in carotenoides during processing and storage of foods. Arch. Latinoam. Nutr. 49(3 Suppl 1), 38S–47S. RODRÍGUEZ-GARCIA, M.E., DE LIRA, C., HERNÁNDEZ-BECERRA, E., CORNEJO-VILLEGAS, M.A., PALACIOS-FONSECA, A.J., ROJAS-MOLINA, I., REYNOSO, R., QUINTERO, L.C., DEL-REAL, A., ZEPEDA, T.A. and MUÑOZ-TORRES, C. 2007. Physicochemical characterization of nopal pads (Opuntia ficus indica) and dry vacuum nopal powders as a function of the maturation. Plant Foods Hum. Nutr. 62(3), 107–112. ROLIN, C. 1993. Pectin. In Industrial Gums: Polysaccharides and Their Derivatives (R.L. Whistler and J.N. Bemiller, eds.) pp. 257–293, Academic Press, New York. SÁNCHEZ-CONTRERAS, A., JIMÉNEZ, M. and SÁNCHEZ, S. 2000. Bioconversion of lutein to products with aroma. Appl. Microbiol. Biotechnol. 54(4), 528–534. SCOTT, C.E. and ELDRIDGE, L.A. 2005. Comparison of carotenoid content in fresh, frozen and canned corn. J. Food Compost. Anal. 18(6), 551–559. SINGH, S., JAIN, S., SINGH, S.P. and SINGH, D. 2009. Quality changes in fruit jams from combinations of different fruit pulps. J. Food Process. Preserv. 33, 41–47. THAKUR, B.R., SINGH, R.K. and HANDA, A.K. 1997. Chemistry and uses of pectin-a review. Crit. Rev. Food Sci. Nutr. 37(1), 47–73. TREJO-GONZÁLEZ, A., GABRIEL-ORTIZ, G., PUEBLA-PÉREZ, A.M., HUÍZAR-CONTRERAS, M.D., MUNGUÍA-MAZARIEGOS, M., MEJÍA-ARREGUÍN, S. and CALVA, E. 1996. A purified extract from prickly pear cactus (Opuntia fuliginosa) controls experimentally induced diabetes in rats. J. Ethnopharm. 55(1), 27–33. WEINBERGER, K. and MSUYA, J. 2004. Indigenous Vegetables in Tanzania. Significance and prospects. AVRDC-The World vegetable Center. Technical Bulletin No. 31. 70 p. AVRDC Publication 04-600. SCHEINVAR, L., FILARDO, K.S., OLALDE, P.G. and SAVALETA, B.P. 2009. Diez especies mexicanas productoras de xoconostles: Opuntia spp. y Cylindropuntia imbricata (Cactaceae), p. 38, Universidad Nacional Autónoma de México, México.

Journal of Food Processing and Preservation 36 (2012) 267–275 © 2011 Wiley Periodicals, Inc.

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