Plant Foods Hum Nutr DOI 10.1007/s11130-014-0465-2
ORIGINAL PAPER
Effects of Cooking Methods on Phenolic Compounds in Xoconostle (Opuntia joconostle) Rosa María Cortez-García & Alicia Ortiz-Moreno & Luis Gerardo Zepeda-Vallejo & Hugo Necoechea-Mondragón
# Springer Science+Business Media New York 2015
Abstract Xoconostle, the acidic cactus pear fruit of Opuntia joconostle of the Cactaceae family, is the source of several phytochemicals, such as betalain pigments and numerous phenolic compounds. The aim of the present study was to analyze the effect of four cooking procedures (i.e., boiling, grilling, steaming and microwaving) on the total phenolic content (TPC) and antioxidant activity (measured by ABTS, DPPH, reducing power, and BCBA) of xoconostle. In addition, HPLC-DAD analyses were performed to identify and quantify individual phenolic compounds. After microwaving and steaming xoconostle, the TPC remained the same that in fresh samples, whereas both grilling and boiling produced a significant, 20 % reduction (p≤0.05). Total flavonoids remained unchanged in boiled and grilled xoconostle, but steaming and microwaving increased the flavonoid content by 13 and 20 %, respectively. Steaming and microwaving did not produce significant changes in the antioxidant activity of xoconostle, whereas boiling and grilling result in significant decreases. The phenolic acids identified in xoconostle fruits were gallic, vanillic, 4-hydroxybenzoic, syringic, ferulic and protocatechuic acids; the flavonoids identified were epicatechin, catechin, rutin, quercitrin, quercetin and kaempferol. Based on the results, steaming and microwaving are the most R. M. Cortez-García : A. Ortiz-Moreno (*) Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Carpio y Plan de Ayala s/n, Col, Santo Tomás 11340, D.F, Mexico e-mail: [email protected] L. G. Zepeda-Vallejo Departamento de Química Orgánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Carpio y Plan de Ayala s/n, Col, Santo Tomás 11340, D.F, México H. Necoechea-Mondragón Coordinación de Cooperación Académica, Instituto Politécnico Nacional, Avenida Miguel Othón de Mendizábal s/n. Col. La Escalera, Santo Tomás 0778, D.F, Mexico
suitable methods for retaining the highest level of phenolic compounds and flavonoids in xoconostle. Keywords Xoconostle . Cooking . Phenolics . Antioxidant activity . HPLC Abbreviations ABTS 2, 2′-Azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid) BCBA β-Carotene bleaching assay CE Catechin equivalents DPPH 2, 2-Diphenyl-1-picrylhydrazyl DWB Dry weight basis EC50 Half-maximal effective concentration GAE Gallic acid equivalents Rt Retention time TE Trolox (6-hydroxy-2, 5, 7, 8-tetramethychroman-2carboxylicacid) equivalents TFC Total flavonoid content TPC Total phenolic content
Introduction The genus Opuntia belongs to the Cactaceae family and contains approximately 300 species of cactus that produce peartype fruits; approximately 100 of these species are found in Mexico, and 60 of them are endemic [1]. Where O. ficusindica is the cactus species with the highest economic importance worldwide which is cultivated to harvest sweet fruits (cactus pears) and cladodes [2], though there are other Opuntia crops, including xoconostle (O. joconostle) which is important for its production of round, edible acidic fruits with a diameter of 4–5 cm [3]. These plants grow in the semiarid highlands of Central Mexico, are tolerant to poor, stony soils
Plant Foods Hum Nutr
and sparse rainfall and have become a 600 ha standard crop over the last five decades [4]. Xoconostles are characterized by a pink-colored pericarp, a succulent mesocarp and a redcolored endocarp that contains small brown seeds. The fruit is either consumed fresh or is processed into jams, juices, sweetened appetizers and alcoholic beverages [3, 5]. Recently, several processed xoconostle products, such as powders and spicy hot sauces, have attracted the attention of international markets [5]. Previous studies have shown that the regular consumption of xoconostle could be useful for serum glucose control and may help prevent conditions related to metabolic syndrome [6–8]. Research has also revealed that xoconostle is a source of several phytochemicals, such as betalain pigments and phenolic compounds [3, 5]. The phenolic compounds in xoconostle include protocatechuic, gallic, vanillic, 4hydroxybenzoic, caffeic and syringic acids as well as the flavonoids catechin, epicatechin, rutin, and quercetin [3, 5]. The growing interest in phenolic compounds is mainly because of their antioxidant potential and the association between their consumption and the prevention of some diseases [9]. It is common for vegetables and some fruits, including xoconostle, to be cooked in the home prior to consumption, and such traditional domestic processing methods include boiling and grilling processes. Meanwhile, new technologies became available, such as steam and the use of microwaves, which have revolutionized the way home cooking is nowadays done mainly because less time is spent as a result of food processing [10]. Domestic processing of fruits and vegetables can significantly degrade phytochemicals [11]. Nonetheless, food processing provides some beneficial aspects, including the inactivation of detrimental constituents; improved digestibility and bioavailability of nutrients; improved palatability, taste, texture and flavor; and enhanced functional properties [10]. Several studies have been conducted on fresh xoconostle, mainly to quantify the phenolic composition and antioxidant activity of the different parts [3, 5, 12]. However, the available information on the effect of cooking on the phenolic composition and antioxidant activities of this fruit is scarce. Therefore, the aim of this study was to compare the effects of different cooking methods (boiling, grilling, steaming and microwaving) on the phenol content and antioxidant activity of whole xoconostle fruits.
Materials and Methods Fruit and Cooking Procedures Fresh O. joconostle fruits (xoconostles) weighing approximately 50 g and with a uniform shape and maturity were obtained during the month of February from a commercial orchard in San Martin de las Piramides, Mexico, in 2014. The fruits were washed, surface-sterilized and rinsed with
distilled water. For each cooking procedure, eight whole fruits were used (400±8 g), and uncooked fruits were kept as control samples at 4 °C. Two traditional cooking methods utilized by the Mexican population were used, i.e., boiling, and grilling; steaming and microwave cooking was also tested. The cooking conditions were optimized using Design-Expert Software, ver. 7.1.5, with two experimental factors (independent variables) for each cooking procedure. The response factors measured were TPC, betalain content and antioxidant activity, which was measured using the DPPH assay. For all cooking procedures, the minimum time to reach a similar softening [13] (Table 1) for appropriate palatability and taste, according to Mexican eating habits, was used. In addition, the maximization of betalains and phenolic compounds with antioxidant activity in the cooked samples was considered. The boiling of xoconostle was performed for 7.7 min in a covered stainless steel vessel containing 848 mL of water that had just begun to boil. The fruits were grilled on a hot plate at 130 ° C for 44.8 min, with the position of the fruits on the hot plate being changed every 5 min during grilling. For steaming, the fruits were placed on a tray in a steam cooker and were heated for 8.6 min under atmospheric pressure by moderate cooking. The microwaving was conducted in a microwave oven (Panasonic, NN-SN968, Shanghai, China): the xoconostles were placed on a round glass plate and cooked at 297 W for 5.5 min; a 4-channel optical fiber thermometer (OPSense, Temp Sense, USA) was used for temperature monitoring within the samples during microwave cooking. The internal temperature of the xoconostles cooked by the different methods was measured by a digital thermometer (Food Network, mod. 9847–32, IL, USA) at the end of the cooking time (Table 1). The samples were then cooled in ice water and subsequently ground and stored at −40 °C until analysis.
Table 1 Cooking time, shear force, softening and temperature reached in xoconostle after processing Cooking method Boiling Time (min) 7.7
Grilling 44.8
Steaming 8.6
Microwaving 5.5
Shear force 16.18±0.92a 16.13±1.58a 15.75±1.58a 16.26±1.11a (N)1 Softening 64.35a 64.46a 65.30a 64.18a (%) Tf (°C) 2 70.33±3.2a 70.33±5.51a 69±7.81a 72±4.36a 3 Means of triplicates in the same row with different letters are significantly different at p≤0.05 1
The shear force of fresh xoconostle was 45.39 N
2
Internal temperature reached after cooking time in xoconostle
3
The average temperature measured by an optical fiber thermometer was 61.16 °C
Plant Foods Hum Nutr
Chemical Analysis Determination of Phenolic Compounds The fresh and thawed cooked samples (500 mg) were homogenized with 5 mL of methanol–water (70:30,v/v) for 30 min, and the sample supernatant was recovered after centrifugation (Hermle, Z326, Wehingen, Germany) at 3000×g [3]. This extraction was repeated once. At the end of the extraction process, the methanol–water supernatants were combined and collected in amber vials, and this constituted the raw extract. The extracts were analyzed immediately to evaluate TPC, TFC and antioxidant activity and were then subjected to HPLC. TPC was determined by a Folin-Ciocalteu colorimetric assay method [3], and the absorbance was measured at 725 nm using a Genesys 10-UV–VIS spectrophotometer. All values are expressed as mg GAE/g DW. TFC was also evaluated using a colorimetric assay [3], with the absorbance measured at 510 nm wavelength. These values are expressed as mg CE/g DW. Analysis of Pigments The pigments were extracted as previously reported [3]. To determine the betalain content, a broad spectral range (350–650 nm) of the pigment extracts was recorded. The red pigment content of xoconostle was referenced as the betanin pigment and was determined using an extinction coefficient of ε =60,000 at 535 nm. The results are expressed as mg of betanin/100 g DW. Determination of Antioxidant Activity The antioxidant activity of the xoconostle extracts was determined using four assays: DPPH, ABTS, reducing power and BCBA. Briefly, the DPPH assay was performed as previously reported [14], and the absorbance was determined at 517 nm; the radicalscavenging activity of the samples is expressed as mmol TE/ 100 g DW. The ABTS assay was performed according to the modified method of Ozgen et al. [15], and the levels of reduced ABTS reactants were measured at 734 nm; the radicalscavenging activity is also expressed in mmol TE/100 g DW. The reducing power assay was performed as previously described by Ak and Gulcin [16]. The extract concentration providing half of the absorbance (EC50) was calculated from the graph of the absorbance at 700 nm versus the extract concentration. The antioxidant activity was also evaluated using the BCBA assay [12]. The absorbance values of all samples at 470 nm were taken at time zero (t=0) and after 2 h of the assay. The extract concentration providing 50 % antioxidant activity (EC50) was calculated by interpolation from the graph of the β-carotene bleaching inhibition percentage versus the extract concentration. Individual Phenolic Compounds (HPLC-DAD) The prepared extracts were used to separate and quantify phenolic compounds [5] using an Agilent 1260 Infinity HPLC with a diode
array detector (HPLC-DAD) and automatic injection. The HPLC was equipped with a 150×4.5 mm i.d., 5μm particle size Zorbax SB-C18 reverse-phase column. The compounds were identified and quantified by comparison of the retention times and absorption spectra of the sample chromatographic peaks with those of authentic standards (Sigma Co.) obtained using the same HPLC operating conditions. Statistical Analysis The optimal cooking conditions were determined by RSM, which was performed using the Design-Expert ver. 7.1.5 software. The complete design consisted of 13 experimental points, including five replications of the central point. For each cooking procedure, eight whole fruits were used (400± 8 g). The experiments for chemical analysis were performed in triplicate. The mean values, standard deviations and analyses of variance were calculated by Sigma Stat software, ver. 3.5. Significant differences between the means were determined using SNK multiple range tests (p≤0.05).
Results and Discussion Whole fresh xoconostle fruits contained 13.08 mg GAE/g DW (1.04 mg GAE/g FW) of total phenols (Table 2), which is slightly lower than the value of 15.01 mg GAE/g DW that was reported by Osorio-Esquivel at al. [3] for whole xoconostles harvested in November 2009. The xoconostle fruits used in the present study were harvested in February 2014, and the differences between the two studies could be largely due to the differences in the harvest time; however, other factors such as climatic and agronomic conditions as well as growing locations cannot be ruled out [11]. After cooking, both the grilling and boiling procedures exhibited a significant reduction (p ≤ 0.05) of nearly 20 % in the xoconostle TPC value. Conversely, the steamed and
Table 2 Total phenolic, flavonoid and betalain contents in cooked xoconostle (DWB) Cooking method
TPC mg GAE/g
Fresh
13.08±0.65a
1.19±0.03a
27.98±0.64a
b
a
21.19±1.41b 20.19±0.92b 20.48±0.51b 23.70±0.33c
Boiling Grilling Steaming Microwaving
TFC mg CE/g
10.54±0.56 10.52±0.71b 12.35±0.91a 13.19±0.26a
Betacyanins mg betanin /100 g
1.12±0.02 1.15±0.05a 1.35±0.07b 1.43±0.04b
Means of triplicates in the same column with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr
microwaved xoconostle did not show significant changes in TPC with respect to the fresh fruit. According to the literature, the TPC level may increase, decrease or remain unchanged after the thermal processing of fruits [10]. In 2005, Turkmen et al. [17] reported that boiling, steaming and microwaving produced the same, significant reduction in the TPC of squash, which may have been due to phenolic breakdown during cooking. Furthermore, a greater loss of zucchini polyphenols was recorded after boiling than after steaming [18]. According to Chuah et al. [19], the TPC was reduced in colored peppers after boiling and microwaving for 5 min, but the decline was statistically significant only in boiled peppers. The authors concluded that microwave heating is superior for ensuring a better retention of the bioactive components in peppers. The TFC found for the fresh xoconostle (Table 2) in this study was 1.19 mg CE/g DW (0.09 mg CE/g FW), which was nearly 2-fold lower than that in the whole, fresh xoconostle surveyed by Osorio-Esquivel et al. [3]. After cooking, the TFC remained unchanged in the boiled and grilled xoconostle compared to the fresh fruit. However, steaming and microwave heating resulted in a significant increase (p≤0.05) in the TFC of xoconostle, increasing by 13 and 20 %, respectively, compared to the initial concentration. This observation is consistent with previous findings reporting that heat treatment increases the level of flavonoids [20]. For instance, Roy et al. [21] found that broccoli steamed for 5 and 10 min resulted in increases in TFC by 2.5-fold and 3.5-fold, respectively. Such an increase in flavonoid content is primarily due to an increased release of phytochemicals from the matrix, which is made more accessible during thermal processing due to the disruption of cell membranes and cell walls, thus releasing phytochemicals that increase the pool of flavonoids [21]. For xoconostle, it is possible that increases in flavonoids could be caused by the release of flavonoids from the seeds because the main phenolic compounds in xoconostle seeds are flavonoids [6]. As stated previously [3], only betacyanin pigments (peaks in the region of 527–530 nm) have been detected in xoconostle, with no betaxanthin pigments being detected in acetonic extracts containing the betalain pigments. In our study, the amount of betacyanins in raw xoconostle was 27.98 mg betanin/100 g DW (2.22 mg/100 g FW). This value is more than 3-fold lower than that reported by OsorioEsquivel et al. [3]. As expected, the betacyanin content decreased significantly (p≤0.05) after cooking in the xoconostle cooked by all the tested methods, though microwave cooking resulted in a higher retention of betacyanins (85 %) (Table 2). Betalains are heat-labile pigments that lose stability at elevated temperatures [22]. In fact, at temperatures above 60 °C, the betalains in xoconostle generally lose color due to probable dehydrogenation and decarboxylation, resulting in neobetanin (yellow) and 17-decarboxy-betanin (orange red) compounds
[23]. In the present study, the temperatures reached during all cooking methods were the same (Table 1), but microwaving required a shorter time to reach the appropriate softness (Table 1) in comparison to other cooking methods, which may improve betalain retention. In this study, four different assays to measure antioxidant activity were performed: the antioxidant activity in uncooked xoconostle and changes after cooking were quantified (Table 3). According to the ABTS assay, the antioxidant activity obtained for uncooked xoconostle was 32.79 mmol TE/ 100 g DW (2.60 mmol TE/100 g FW). This value is consistent with Guzmán-Maldonado et al. [5], who analyzed other xoconostle varieties and found a range of 2–16 mmol TE/ 100 g FW in the methanolic extracts of different parts of O. matudae fruits. As shown in Table 3, the cooking methods that caused a significant decrease (p≤0.05) in the antioxidant activity measured by the ABTS free radical-scavenging assay are listed in descending order: steaming>boiling>grilling. However, with microwave heating, the antioxidant activity was similar to that of the fresh fruit. The antioxidant activity of boiled, grilled and steamed xoconostle determined by the DPPH radical-scavenging method remained the same as that of the fresh samples. In contrast, the DPPH levels were significantly higher using microwave cooking (p≤0.05). This disparate behavior of the DPPH and ABTS radical assays, which has also been observed for other fruit extracts, could be because many antioxidants that react quickly with other radicals may react slowly, or be inert, with DPPH or ABTS due to steric inaccessibility [14]. The xoconostle EC50 values measured by both reducing power and β-carotene bleaching inhibition are shown in Table 3. Unfortunately, the antioxidant activity values determined as EC50 in the fresh samples cannot be compared with those obtained by Morales et al. [12] for O. joconostle fruit pulp because the antioxidant activity in that study is expressed as mg/mL of extract. These authors reported EC50 values of 3.16 and 0.32 mg/mL of extract for O. joconostle fresh fruit pulp according to reducing power and BCBA, respectively, and the EC50 values for boiled and grilled xoconostle in our
Table 3
Antioxidant activity of xoconostle (DWB)
Cooking method
ABTS
DPPH
Reducing BCBA power EC50 (mg/mL)
mmol TE/100 g Fresh Boiling Grilling Steaming Microwaving
32.79±1.42a
4.94±0.64a
8.04±0.52a
3.08±0.29a
b
a
b
4.07±0.42b 4.62±0.29b 3.39±0.14a 3.26±0.20a
26.49±0.37 23.52±0.11c 29.70±0.30d 31.95±0.65a
4.79±0.30 9.47±0.65 4.49±0.22a 10.48±0.15b 4.47±0.27a 8.90±0.18a b 5.81±0.25 8.07±0.68a
Means of triplicates in the same column with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr
study showed a significant increase (p≤0.05) based on these two methods of analysis. Moreover, the results indicate that boiled and grilled xoconostle had lower antioxidant activity than the steamed and microwaved samples, and the antioxidant activity of the steamed and microwaved xoconostle remained unchanged compared with that of the fresh fruit. Overall, the effects on antioxidant activity may indicate that both steaming and microwaving can promote better preservation of antioxidant compounds compared with boiling and grilling. Furthermore, steaming and microwaving may also retain higher TPC and TFC during cooking. Morales et al. [12] related the high antioxidant activity of xoconostle with its high content of phenols and flavonoids. In general, extracts that contain a high amount of phenolic compounds also exhibit high antioxidant activity [14, 24]. HPLC-DAD was employed to separate, identify and quantify thirteen phenolic compounds in fresh and cooked xoconostle (Table 4). The concentrations of phenolic acids (gallic, vanillic, 4-hydroxybenzoic, syringic and protocatechuic acids) and flavonoids (epicatechin, catechin, rutin and quercetin) in fresh xoconostle were found to be similar to previously reported values [3, 5]; however, no literature values are available for ferulic acid and quercitrin concentrations in xoconostle. After all cooking methods, lower concentrations were measured for vanillic, 4-hydroxybenzoic, syringic and protocatechuic acids and the flavonoids epicatechin and quercitrin compared to those in fresh fruit. Furthermore, different degrees of degradation were observed depending on the compound and the processing method. However, the greatest losses were observed during both the boiling and grilling procedures. Conversely, cooking by steaming and microwaving retained higher levels of phenolic Table 4
compounds. With steaming, the vegetable tissue is not placed in direct contact with a hot material (water), the temperature does not exceed 95 °C, and the leaching of hydrophilic compounds into the boiling water is minimized [25]. Likewise, microwaving has also been demonstrated to ensure higher retention of bioactive components [17, 19, 26], mainly when microwave cooking is performed without water and the plant material is heated at low microwave intensity and shorter cooking time [19, 27]. The industrial and domestic use of microwaves has increased dramatically over the past few decades. Moreover, the use of large-scale microwave processes is increasing, recent improvements in the design of highpowered microwave ovens, reduced equipment manufacturing costs and trends in electrical energy costs offer a significant potential for developing new and improved industrial microwave processes [28].
Conclusions The present study shows that the profile of phenolic compounds in xoconostle is modified by different cooking methods. In general, both steaming and microwave heating did not affect TPC and antioxidant activity but produced higher retention of individual phenolic compounds, as observed in the HPLC-DAD analysis. Based on these findings, cooking xoconostle by steaming and microwave heating is recommended to ensure a higher retention of the phenolic compounds and antioxidant constituents, and these methods should be selected to preserve the nutraceutical qualities of xoconostle.
Phenolic compounds (mg/100 g DWB) detected in cooked xoconostle
Phenolic compound
Gallic acid Vanillic acid 4-Hydroxybenzoic acid Syringic acid Epicatechin Catechin Ferulic acid Rutin Vanillin Protocatechuic acid Quercitrin Quercetin Kaempferol
Rt
Cooking method
(min)
Fresh
Boiling
Grilling
Steaming
Microwaving
2.260 9.533 10.500 10.973 11.347 12.007 15.820 17.353 18.707 20.180 20.507 27.667 30.307
11.35±0.66a 9.96±0.31a 10.42±0.04a 3.39±0.04a 4.65±0.01a 15.81±0.01a 7.00±0.34a 5.36±0.16a 7.87±0.41a 26.56±0.54a 17.3±0.83a 5.19±0.04a 13.90±1.14a
ND 5.30±0.71b 2.96±0.14b 1.12±0.01b 2.04±0.08b 3.36±0.01b 5.15±0.03b 1.34±0.08b ND 2.62±0.02b 3.22±0.13b 5.82±0.09a 9.04±0.30b
7.81±0.41b ND 4.94±0.23c 1.72±0.02c 2.03±0.06b 3.12±0.01b 6.50±0.20a 4.58±0.31c ND 3.59±0.08c 0.84±0.04c 7.55±0.16b ND
6.75±0.04c 4.31±0.39b 3.96±0.23d 1.42±0.02d 2.82±0.16c 17.76±0.38c 7.03±0.18a 4.96±0.13c 5.63±0.10a 4.10±0.02d 0.74±0.04c 7.61±0.02b 10.01±0.47b
12.34±0.04a 0.97±0.04c 4.05±0.21d ND 1.87±0.03b 13.40±0.14d 6.72±0.34a 5.62±0.19a 7.84±0.89b 4.92±0.02e 1.15±0.06d 9.33±0.67c 13.69±1.56a
Means of triplicates in the same row with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr Acknowledgments This research was partly funded by CONACyT scholarship no. 237260, Secretaria de Investigación y Posgrado-IPN Proyect Number 20130428. Conflict of Interest The authors declare that they have no conflict ofinterest.
References 1. Feugang JM, Konarski P, Daming Z et al (2006) Nutritional and medicinal use of cactus pear (Opuntia spp.) cladodes and fruits. Front Biosci 11(1):2574–2589 2. Reyes-Agüero JA, Aguirre-Rivera R, Hernández H (2005) Systematyc notes and a detailed description of O. ficus-indica (L) Mill. (Cactaceae). Agrociencia 39(4):395–408 3. Osorio-Esquivel O, Ortiz-Moreno A, Álvarez V et al (2011) Phenolics, betacyanins and antioxidant activity in Opuntia joconostle fruits. Food Res Int 44(7):2160–2168 4. Gallegos-Vázquez C, Scheinvar L, Núñez-Colín CA, MondragónJacobo (2012) Morphological diversity of xoconostles (Opuntia spp.) or acidic cactus pears: a Mexican contribution to functional foods. Fruits 67(02):109–120 5. Guzmán-Maldonado SH, Morales-Montelongo AL, MondragónJacobo C et al (2010) Physicochemical, nutritional, and functional characterization of fruits xoconostle (Opuntia matudae) pears from central-México region. J Food Sci 75(6):C485–C492 6. Osorio-Esquivel O, Ortiz-Moreno A, Garduño-Siciliano L et al (2012) Antihyperlipidemic effect of methanolic extract from Opuntia joconostle seeds in mice fed a hypercholesterolemic diet. Plant Foods Hum Nutr 67(4):365–370 7. Patel S (2013) Reviewing the prospects of Opuntia pears as low cost functional foods. Rev Environ Sci Biotechnol 12(3):223–234 8. Pimienta-Barrios E, Méndez-Morán L, Ramírez-Hernández B et al (2008) Efecto de la ingestión del fruto de xoconostle (O. joconostle Web.) sobre la glucosa y lípidos séricos. Agrociencia 42:645–653 9. Haminiuk CWI, Maciel GM, Plata-Oviedo MSV, Peralta RM (2012) Phenolic compounds in fruits – an overview. Int J Food Sci Technol 47(10):2023–2044 10. van Boekel M, Fogliano V, Pellegrini N et al (2010) A review on the beneficial aspects of food processing. Mol Nutr Food Res 54(9): 1215–1247 11. Tiwari U, Cummins E (2013) Factors influencing levels of phytochemicals in selected fruit and vegetables during pre- and postharvest food processing operations. Food Res Int 50(2):497–506 12. Morales P, Ramírez-Moreno E, Sanchez-Mata MC et al (2012) Nutritional and antioxidant properties of pulp and seeds of two xoconostle cultivars (O. joconostle F.A.C. Weber ex Diguet and O. matudae Scheinvar) of high consumption in Mexico. Food Res Int 46(1):279–285
13. Ferracane R, Pellegrini N, Visconti A et al (2008) Effects of different cooking methods on antioxidant profile, antioxidant capacity, and physical characteristics of artichoke. J Agric Food Chem 56(18): 8601–8608 14. Fernández-López J, Almela L, Obón J, Castellar R (2010) Determination of antioxidant constituents in cactus pear fruits. Plant Foods Hum Nutr 65(3):253–259 15. Ozgen M, Reese RN, Tulio AZ et al (2006) Modified 2,2azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-diphenyl-1-picrylhydrazyl (DPPH) methods. J Agric Food Chem 54(4):1151–1157 16. Ak T, Gülçin İ (2008) Antioxidant and radical scavenging properties of curcumin. Chem-Biol Interact 174(1):27–37 17. Turkmen N, Sari F, Velioglu YS (2005) The effect of cooking methods on total phenolics and antioxidant activity of selected green vegetables. Food Chem 93(4):713–718 18. Miglio C, Chiavaro E, Visconti A et al (2007) Effects of different cooking methods on nutritional and physicochemical characteristics of selected vegetables. J Agric Food Chem 56(1):139–147 19. Chuah AM, Lee Y-C, Yamaguchi T et al (2008) Effect of cooking on the antioxidant properties of coloured peppers. Food Chem 111(1): 20–28 20. Stewart AJ, Bozonnet S, Mullen W et al (2000) Occurrence of flavonols in tomatoes and tomato-based products. J Agr Food Chem 48(7): 2663–2669 21. Roy MK, Juneja LR, Isobe S, Tsushida T (2009) Steam processed broccoli (Brassica oleracea) has higher antioxidant activity in chemical and cellular assay systems. Food Chem 114(1):263–269 22. Herbach KM, Stintzing FC, Carle R (2006) Betalain stability and degradation—structural and chromatic aspects. J Food Sci 71(4): R41–R50 23. Sanchez-Gonzalez N, Jaime-Fonseca MR, San Martin-Martinez E, Zepeda LG (2013) Extraction, stability, and separation of betalains from Opuntia joconostle cv. using response surface methodology. J Agric Food Chem 61(49):11995–12004 24. Wong SP, Leong LP, William Koh JH (2006) Antioxidant activities of aqueous extracts of selected plants. Food Chem 99(4):775–783 25. Palermo M, Pellegrini N, Fogliano V (2014) The effect of cooking on the phytochemical content of vegetables. J Sci Food Agric 94(6): 1057–1070 26. Song L, Thornalley PJ (2007) Effect of storage, processing and cooking on glucosinolate content of Brassica vegetables. Food Chem Toxicol 45(2):216–224 27. López-Berenguer C, Carvajal M, Moreno DA, García-Viguera C (2007) Effects of microwave cooking conditions on bioactive compounds present in broccoli inflorescences. J Agric Food Chem 55(24):10001–10007 28. Vadivambal R, Jayas DS (2007) Changes in quality of microwavetreated agricultural products—a review. Biosyst Eng 98(1):1–16
ORIGINAL PAPER
Effects of Cooking Methods on Phenolic Compounds in Xoconostle (Opuntia joconostle) Rosa María Cortez-García & Alicia Ortiz-Moreno & Luis Gerardo Zepeda-Vallejo & Hugo Necoechea-Mondragón
# Springer Science+Business Media New York 2015
Abstract Xoconostle, the acidic cactus pear fruit of Opuntia joconostle of the Cactaceae family, is the source of several phytochemicals, such as betalain pigments and numerous phenolic compounds. The aim of the present study was to analyze the effect of four cooking procedures (i.e., boiling, grilling, steaming and microwaving) on the total phenolic content (TPC) and antioxidant activity (measured by ABTS, DPPH, reducing power, and BCBA) of xoconostle. In addition, HPLC-DAD analyses were performed to identify and quantify individual phenolic compounds. After microwaving and steaming xoconostle, the TPC remained the same that in fresh samples, whereas both grilling and boiling produced a significant, 20 % reduction (p≤0.05). Total flavonoids remained unchanged in boiled and grilled xoconostle, but steaming and microwaving increased the flavonoid content by 13 and 20 %, respectively. Steaming and microwaving did not produce significant changes in the antioxidant activity of xoconostle, whereas boiling and grilling result in significant decreases. The phenolic acids identified in xoconostle fruits were gallic, vanillic, 4-hydroxybenzoic, syringic, ferulic and protocatechuic acids; the flavonoids identified were epicatechin, catechin, rutin, quercitrin, quercetin and kaempferol. Based on the results, steaming and microwaving are the most R. M. Cortez-García : A. Ortiz-Moreno (*) Departamento de Ingeniería Bioquímica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Carpio y Plan de Ayala s/n, Col, Santo Tomás 11340, D.F, Mexico e-mail: [email protected] L. G. Zepeda-Vallejo Departamento de Química Orgánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Carpio y Plan de Ayala s/n, Col, Santo Tomás 11340, D.F, México H. Necoechea-Mondragón Coordinación de Cooperación Académica, Instituto Politécnico Nacional, Avenida Miguel Othón de Mendizábal s/n. Col. La Escalera, Santo Tomás 0778, D.F, Mexico
suitable methods for retaining the highest level of phenolic compounds and flavonoids in xoconostle. Keywords Xoconostle . Cooking . Phenolics . Antioxidant activity . HPLC Abbreviations ABTS 2, 2′-Azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid) BCBA β-Carotene bleaching assay CE Catechin equivalents DPPH 2, 2-Diphenyl-1-picrylhydrazyl DWB Dry weight basis EC50 Half-maximal effective concentration GAE Gallic acid equivalents Rt Retention time TE Trolox (6-hydroxy-2, 5, 7, 8-tetramethychroman-2carboxylicacid) equivalents TFC Total flavonoid content TPC Total phenolic content
Introduction The genus Opuntia belongs to the Cactaceae family and contains approximately 300 species of cactus that produce peartype fruits; approximately 100 of these species are found in Mexico, and 60 of them are endemic [1]. Where O. ficusindica is the cactus species with the highest economic importance worldwide which is cultivated to harvest sweet fruits (cactus pears) and cladodes [2], though there are other Opuntia crops, including xoconostle (O. joconostle) which is important for its production of round, edible acidic fruits with a diameter of 4–5 cm [3]. These plants grow in the semiarid highlands of Central Mexico, are tolerant to poor, stony soils
Plant Foods Hum Nutr
and sparse rainfall and have become a 600 ha standard crop over the last five decades [4]. Xoconostles are characterized by a pink-colored pericarp, a succulent mesocarp and a redcolored endocarp that contains small brown seeds. The fruit is either consumed fresh or is processed into jams, juices, sweetened appetizers and alcoholic beverages [3, 5]. Recently, several processed xoconostle products, such as powders and spicy hot sauces, have attracted the attention of international markets [5]. Previous studies have shown that the regular consumption of xoconostle could be useful for serum glucose control and may help prevent conditions related to metabolic syndrome [6–8]. Research has also revealed that xoconostle is a source of several phytochemicals, such as betalain pigments and phenolic compounds [3, 5]. The phenolic compounds in xoconostle include protocatechuic, gallic, vanillic, 4hydroxybenzoic, caffeic and syringic acids as well as the flavonoids catechin, epicatechin, rutin, and quercetin [3, 5]. The growing interest in phenolic compounds is mainly because of their antioxidant potential and the association between their consumption and the prevention of some diseases [9]. It is common for vegetables and some fruits, including xoconostle, to be cooked in the home prior to consumption, and such traditional domestic processing methods include boiling and grilling processes. Meanwhile, new technologies became available, such as steam and the use of microwaves, which have revolutionized the way home cooking is nowadays done mainly because less time is spent as a result of food processing [10]. Domestic processing of fruits and vegetables can significantly degrade phytochemicals [11]. Nonetheless, food processing provides some beneficial aspects, including the inactivation of detrimental constituents; improved digestibility and bioavailability of nutrients; improved palatability, taste, texture and flavor; and enhanced functional properties [10]. Several studies have been conducted on fresh xoconostle, mainly to quantify the phenolic composition and antioxidant activity of the different parts [3, 5, 12]. However, the available information on the effect of cooking on the phenolic composition and antioxidant activities of this fruit is scarce. Therefore, the aim of this study was to compare the effects of different cooking methods (boiling, grilling, steaming and microwaving) on the phenol content and antioxidant activity of whole xoconostle fruits.
Materials and Methods Fruit and Cooking Procedures Fresh O. joconostle fruits (xoconostles) weighing approximately 50 g and with a uniform shape and maturity were obtained during the month of February from a commercial orchard in San Martin de las Piramides, Mexico, in 2014. The fruits were washed, surface-sterilized and rinsed with
distilled water. For each cooking procedure, eight whole fruits were used (400±8 g), and uncooked fruits were kept as control samples at 4 °C. Two traditional cooking methods utilized by the Mexican population were used, i.e., boiling, and grilling; steaming and microwave cooking was also tested. The cooking conditions were optimized using Design-Expert Software, ver. 7.1.5, with two experimental factors (independent variables) for each cooking procedure. The response factors measured were TPC, betalain content and antioxidant activity, which was measured using the DPPH assay. For all cooking procedures, the minimum time to reach a similar softening [13] (Table 1) for appropriate palatability and taste, according to Mexican eating habits, was used. In addition, the maximization of betalains and phenolic compounds with antioxidant activity in the cooked samples was considered. The boiling of xoconostle was performed for 7.7 min in a covered stainless steel vessel containing 848 mL of water that had just begun to boil. The fruits were grilled on a hot plate at 130 ° C for 44.8 min, with the position of the fruits on the hot plate being changed every 5 min during grilling. For steaming, the fruits were placed on a tray in a steam cooker and were heated for 8.6 min under atmospheric pressure by moderate cooking. The microwaving was conducted in a microwave oven (Panasonic, NN-SN968, Shanghai, China): the xoconostles were placed on a round glass plate and cooked at 297 W for 5.5 min; a 4-channel optical fiber thermometer (OPSense, Temp Sense, USA) was used for temperature monitoring within the samples during microwave cooking. The internal temperature of the xoconostles cooked by the different methods was measured by a digital thermometer (Food Network, mod. 9847–32, IL, USA) at the end of the cooking time (Table 1). The samples were then cooled in ice water and subsequently ground and stored at −40 °C until analysis.
Table 1 Cooking time, shear force, softening and temperature reached in xoconostle after processing Cooking method Boiling Time (min) 7.7
Grilling 44.8
Steaming 8.6
Microwaving 5.5
Shear force 16.18±0.92a 16.13±1.58a 15.75±1.58a 16.26±1.11a (N)1 Softening 64.35a 64.46a 65.30a 64.18a (%) Tf (°C) 2 70.33±3.2a 70.33±5.51a 69±7.81a 72±4.36a 3 Means of triplicates in the same row with different letters are significantly different at p≤0.05 1
The shear force of fresh xoconostle was 45.39 N
2
Internal temperature reached after cooking time in xoconostle
3
The average temperature measured by an optical fiber thermometer was 61.16 °C
Plant Foods Hum Nutr
Chemical Analysis Determination of Phenolic Compounds The fresh and thawed cooked samples (500 mg) were homogenized with 5 mL of methanol–water (70:30,v/v) for 30 min, and the sample supernatant was recovered after centrifugation (Hermle, Z326, Wehingen, Germany) at 3000×g [3]. This extraction was repeated once. At the end of the extraction process, the methanol–water supernatants were combined and collected in amber vials, and this constituted the raw extract. The extracts were analyzed immediately to evaluate TPC, TFC and antioxidant activity and were then subjected to HPLC. TPC was determined by a Folin-Ciocalteu colorimetric assay method [3], and the absorbance was measured at 725 nm using a Genesys 10-UV–VIS spectrophotometer. All values are expressed as mg GAE/g DW. TFC was also evaluated using a colorimetric assay [3], with the absorbance measured at 510 nm wavelength. These values are expressed as mg CE/g DW. Analysis of Pigments The pigments were extracted as previously reported [3]. To determine the betalain content, a broad spectral range (350–650 nm) of the pigment extracts was recorded. The red pigment content of xoconostle was referenced as the betanin pigment and was determined using an extinction coefficient of ε =60,000 at 535 nm. The results are expressed as mg of betanin/100 g DW. Determination of Antioxidant Activity The antioxidant activity of the xoconostle extracts was determined using four assays: DPPH, ABTS, reducing power and BCBA. Briefly, the DPPH assay was performed as previously reported [14], and the absorbance was determined at 517 nm; the radicalscavenging activity of the samples is expressed as mmol TE/ 100 g DW. The ABTS assay was performed according to the modified method of Ozgen et al. [15], and the levels of reduced ABTS reactants were measured at 734 nm; the radicalscavenging activity is also expressed in mmol TE/100 g DW. The reducing power assay was performed as previously described by Ak and Gulcin [16]. The extract concentration providing half of the absorbance (EC50) was calculated from the graph of the absorbance at 700 nm versus the extract concentration. The antioxidant activity was also evaluated using the BCBA assay [12]. The absorbance values of all samples at 470 nm were taken at time zero (t=0) and after 2 h of the assay. The extract concentration providing 50 % antioxidant activity (EC50) was calculated by interpolation from the graph of the β-carotene bleaching inhibition percentage versus the extract concentration. Individual Phenolic Compounds (HPLC-DAD) The prepared extracts were used to separate and quantify phenolic compounds [5] using an Agilent 1260 Infinity HPLC with a diode
array detector (HPLC-DAD) and automatic injection. The HPLC was equipped with a 150×4.5 mm i.d., 5μm particle size Zorbax SB-C18 reverse-phase column. The compounds were identified and quantified by comparison of the retention times and absorption spectra of the sample chromatographic peaks with those of authentic standards (Sigma Co.) obtained using the same HPLC operating conditions. Statistical Analysis The optimal cooking conditions were determined by RSM, which was performed using the Design-Expert ver. 7.1.5 software. The complete design consisted of 13 experimental points, including five replications of the central point. For each cooking procedure, eight whole fruits were used (400± 8 g). The experiments for chemical analysis were performed in triplicate. The mean values, standard deviations and analyses of variance were calculated by Sigma Stat software, ver. 3.5. Significant differences between the means were determined using SNK multiple range tests (p≤0.05).
Results and Discussion Whole fresh xoconostle fruits contained 13.08 mg GAE/g DW (1.04 mg GAE/g FW) of total phenols (Table 2), which is slightly lower than the value of 15.01 mg GAE/g DW that was reported by Osorio-Esquivel at al. [3] for whole xoconostles harvested in November 2009. The xoconostle fruits used in the present study were harvested in February 2014, and the differences between the two studies could be largely due to the differences in the harvest time; however, other factors such as climatic and agronomic conditions as well as growing locations cannot be ruled out [11]. After cooking, both the grilling and boiling procedures exhibited a significant reduction (p ≤ 0.05) of nearly 20 % in the xoconostle TPC value. Conversely, the steamed and
Table 2 Total phenolic, flavonoid and betalain contents in cooked xoconostle (DWB) Cooking method
TPC mg GAE/g
Fresh
13.08±0.65a
1.19±0.03a
27.98±0.64a
b
a
21.19±1.41b 20.19±0.92b 20.48±0.51b 23.70±0.33c
Boiling Grilling Steaming Microwaving
TFC mg CE/g
10.54±0.56 10.52±0.71b 12.35±0.91a 13.19±0.26a
Betacyanins mg betanin /100 g
1.12±0.02 1.15±0.05a 1.35±0.07b 1.43±0.04b
Means of triplicates in the same column with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr
microwaved xoconostle did not show significant changes in TPC with respect to the fresh fruit. According to the literature, the TPC level may increase, decrease or remain unchanged after the thermal processing of fruits [10]. In 2005, Turkmen et al. [17] reported that boiling, steaming and microwaving produced the same, significant reduction in the TPC of squash, which may have been due to phenolic breakdown during cooking. Furthermore, a greater loss of zucchini polyphenols was recorded after boiling than after steaming [18]. According to Chuah et al. [19], the TPC was reduced in colored peppers after boiling and microwaving for 5 min, but the decline was statistically significant only in boiled peppers. The authors concluded that microwave heating is superior for ensuring a better retention of the bioactive components in peppers. The TFC found for the fresh xoconostle (Table 2) in this study was 1.19 mg CE/g DW (0.09 mg CE/g FW), which was nearly 2-fold lower than that in the whole, fresh xoconostle surveyed by Osorio-Esquivel et al. [3]. After cooking, the TFC remained unchanged in the boiled and grilled xoconostle compared to the fresh fruit. However, steaming and microwave heating resulted in a significant increase (p≤0.05) in the TFC of xoconostle, increasing by 13 and 20 %, respectively, compared to the initial concentration. This observation is consistent with previous findings reporting that heat treatment increases the level of flavonoids [20]. For instance, Roy et al. [21] found that broccoli steamed for 5 and 10 min resulted in increases in TFC by 2.5-fold and 3.5-fold, respectively. Such an increase in flavonoid content is primarily due to an increased release of phytochemicals from the matrix, which is made more accessible during thermal processing due to the disruption of cell membranes and cell walls, thus releasing phytochemicals that increase the pool of flavonoids [21]. For xoconostle, it is possible that increases in flavonoids could be caused by the release of flavonoids from the seeds because the main phenolic compounds in xoconostle seeds are flavonoids [6]. As stated previously [3], only betacyanin pigments (peaks in the region of 527–530 nm) have been detected in xoconostle, with no betaxanthin pigments being detected in acetonic extracts containing the betalain pigments. In our study, the amount of betacyanins in raw xoconostle was 27.98 mg betanin/100 g DW (2.22 mg/100 g FW). This value is more than 3-fold lower than that reported by OsorioEsquivel et al. [3]. As expected, the betacyanin content decreased significantly (p≤0.05) after cooking in the xoconostle cooked by all the tested methods, though microwave cooking resulted in a higher retention of betacyanins (85 %) (Table 2). Betalains are heat-labile pigments that lose stability at elevated temperatures [22]. In fact, at temperatures above 60 °C, the betalains in xoconostle generally lose color due to probable dehydrogenation and decarboxylation, resulting in neobetanin (yellow) and 17-decarboxy-betanin (orange red) compounds
[23]. In the present study, the temperatures reached during all cooking methods were the same (Table 1), but microwaving required a shorter time to reach the appropriate softness (Table 1) in comparison to other cooking methods, which may improve betalain retention. In this study, four different assays to measure antioxidant activity were performed: the antioxidant activity in uncooked xoconostle and changes after cooking were quantified (Table 3). According to the ABTS assay, the antioxidant activity obtained for uncooked xoconostle was 32.79 mmol TE/ 100 g DW (2.60 mmol TE/100 g FW). This value is consistent with Guzmán-Maldonado et al. [5], who analyzed other xoconostle varieties and found a range of 2–16 mmol TE/ 100 g FW in the methanolic extracts of different parts of O. matudae fruits. As shown in Table 3, the cooking methods that caused a significant decrease (p≤0.05) in the antioxidant activity measured by the ABTS free radical-scavenging assay are listed in descending order: steaming>boiling>grilling. However, with microwave heating, the antioxidant activity was similar to that of the fresh fruit. The antioxidant activity of boiled, grilled and steamed xoconostle determined by the DPPH radical-scavenging method remained the same as that of the fresh samples. In contrast, the DPPH levels were significantly higher using microwave cooking (p≤0.05). This disparate behavior of the DPPH and ABTS radical assays, which has also been observed for other fruit extracts, could be because many antioxidants that react quickly with other radicals may react slowly, or be inert, with DPPH or ABTS due to steric inaccessibility [14]. The xoconostle EC50 values measured by both reducing power and β-carotene bleaching inhibition are shown in Table 3. Unfortunately, the antioxidant activity values determined as EC50 in the fresh samples cannot be compared with those obtained by Morales et al. [12] for O. joconostle fruit pulp because the antioxidant activity in that study is expressed as mg/mL of extract. These authors reported EC50 values of 3.16 and 0.32 mg/mL of extract for O. joconostle fresh fruit pulp according to reducing power and BCBA, respectively, and the EC50 values for boiled and grilled xoconostle in our
Table 3
Antioxidant activity of xoconostle (DWB)
Cooking method
ABTS
DPPH
Reducing BCBA power EC50 (mg/mL)
mmol TE/100 g Fresh Boiling Grilling Steaming Microwaving
32.79±1.42a
4.94±0.64a
8.04±0.52a
3.08±0.29a
b
a
b
4.07±0.42b 4.62±0.29b 3.39±0.14a 3.26±0.20a
26.49±0.37 23.52±0.11c 29.70±0.30d 31.95±0.65a
4.79±0.30 9.47±0.65 4.49±0.22a 10.48±0.15b 4.47±0.27a 8.90±0.18a b 5.81±0.25 8.07±0.68a
Means of triplicates in the same column with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr
study showed a significant increase (p≤0.05) based on these two methods of analysis. Moreover, the results indicate that boiled and grilled xoconostle had lower antioxidant activity than the steamed and microwaved samples, and the antioxidant activity of the steamed and microwaved xoconostle remained unchanged compared with that of the fresh fruit. Overall, the effects on antioxidant activity may indicate that both steaming and microwaving can promote better preservation of antioxidant compounds compared with boiling and grilling. Furthermore, steaming and microwaving may also retain higher TPC and TFC during cooking. Morales et al. [12] related the high antioxidant activity of xoconostle with its high content of phenols and flavonoids. In general, extracts that contain a high amount of phenolic compounds also exhibit high antioxidant activity [14, 24]. HPLC-DAD was employed to separate, identify and quantify thirteen phenolic compounds in fresh and cooked xoconostle (Table 4). The concentrations of phenolic acids (gallic, vanillic, 4-hydroxybenzoic, syringic and protocatechuic acids) and flavonoids (epicatechin, catechin, rutin and quercetin) in fresh xoconostle were found to be similar to previously reported values [3, 5]; however, no literature values are available for ferulic acid and quercitrin concentrations in xoconostle. After all cooking methods, lower concentrations were measured for vanillic, 4-hydroxybenzoic, syringic and protocatechuic acids and the flavonoids epicatechin and quercitrin compared to those in fresh fruit. Furthermore, different degrees of degradation were observed depending on the compound and the processing method. However, the greatest losses were observed during both the boiling and grilling procedures. Conversely, cooking by steaming and microwaving retained higher levels of phenolic Table 4
compounds. With steaming, the vegetable tissue is not placed in direct contact with a hot material (water), the temperature does not exceed 95 °C, and the leaching of hydrophilic compounds into the boiling water is minimized [25]. Likewise, microwaving has also been demonstrated to ensure higher retention of bioactive components [17, 19, 26], mainly when microwave cooking is performed without water and the plant material is heated at low microwave intensity and shorter cooking time [19, 27]. The industrial and domestic use of microwaves has increased dramatically over the past few decades. Moreover, the use of large-scale microwave processes is increasing, recent improvements in the design of highpowered microwave ovens, reduced equipment manufacturing costs and trends in electrical energy costs offer a significant potential for developing new and improved industrial microwave processes [28].
Conclusions The present study shows that the profile of phenolic compounds in xoconostle is modified by different cooking methods. In general, both steaming and microwave heating did not affect TPC and antioxidant activity but produced higher retention of individual phenolic compounds, as observed in the HPLC-DAD analysis. Based on these findings, cooking xoconostle by steaming and microwave heating is recommended to ensure a higher retention of the phenolic compounds and antioxidant constituents, and these methods should be selected to preserve the nutraceutical qualities of xoconostle.
Phenolic compounds (mg/100 g DWB) detected in cooked xoconostle
Phenolic compound
Gallic acid Vanillic acid 4-Hydroxybenzoic acid Syringic acid Epicatechin Catechin Ferulic acid Rutin Vanillin Protocatechuic acid Quercitrin Quercetin Kaempferol
Rt
Cooking method
(min)
Fresh
Boiling
Grilling
Steaming
Microwaving
2.260 9.533 10.500 10.973 11.347 12.007 15.820 17.353 18.707 20.180 20.507 27.667 30.307
11.35±0.66a 9.96±0.31a 10.42±0.04a 3.39±0.04a 4.65±0.01a 15.81±0.01a 7.00±0.34a 5.36±0.16a 7.87±0.41a 26.56±0.54a 17.3±0.83a 5.19±0.04a 13.90±1.14a
ND 5.30±0.71b 2.96±0.14b 1.12±0.01b 2.04±0.08b 3.36±0.01b 5.15±0.03b 1.34±0.08b ND 2.62±0.02b 3.22±0.13b 5.82±0.09a 9.04±0.30b
7.81±0.41b ND 4.94±0.23c 1.72±0.02c 2.03±0.06b 3.12±0.01b 6.50±0.20a 4.58±0.31c ND 3.59±0.08c 0.84±0.04c 7.55±0.16b ND
6.75±0.04c 4.31±0.39b 3.96±0.23d 1.42±0.02d 2.82±0.16c 17.76±0.38c 7.03±0.18a 4.96±0.13c 5.63±0.10a 4.10±0.02d 0.74±0.04c 7.61±0.02b 10.01±0.47b
12.34±0.04a 0.97±0.04c 4.05±0.21d ND 1.87±0.03b 13.40±0.14d 6.72±0.34a 5.62±0.19a 7.84±0.89b 4.92±0.02e 1.15±0.06d 9.33±0.67c 13.69±1.56a
Means of triplicates in the same row with different letters are significantly different at p≤0.05
Plant Foods Hum Nutr Acknowledgments This research was partly funded by CONACyT scholarship no. 237260, Secretaria de Investigación y Posgrado-IPN Proyect Number 20130428. Conflict of Interest The authors declare that they have no conflict ofinterest.
References 1. Feugang JM, Konarski P, Daming Z et al (2006) Nutritional and medicinal use of cactus pear (Opuntia spp.) cladodes and fruits. Front Biosci 11(1):2574–2589 2. Reyes-Agüero JA, Aguirre-Rivera R, Hernández H (2005) Systematyc notes and a detailed description of O. ficus-indica (L) Mill. (Cactaceae). Agrociencia 39(4):395–408 3. Osorio-Esquivel O, Ortiz-Moreno A, Álvarez V et al (2011) Phenolics, betacyanins and antioxidant activity in Opuntia joconostle fruits. Food Res Int 44(7):2160–2168 4. Gallegos-Vázquez C, Scheinvar L, Núñez-Colín CA, MondragónJacobo (2012) Morphological diversity of xoconostles (Opuntia spp.) or acidic cactus pears: a Mexican contribution to functional foods. Fruits 67(02):109–120 5. Guzmán-Maldonado SH, Morales-Montelongo AL, MondragónJacobo C et al (2010) Physicochemical, nutritional, and functional characterization of fruits xoconostle (Opuntia matudae) pears from central-México region. J Food Sci 75(6):C485–C492 6. Osorio-Esquivel O, Ortiz-Moreno A, Garduño-Siciliano L et al (2012) Antihyperlipidemic effect of methanolic extract from Opuntia joconostle seeds in mice fed a hypercholesterolemic diet. Plant Foods Hum Nutr 67(4):365–370 7. Patel S (2013) Reviewing the prospects of Opuntia pears as low cost functional foods. Rev Environ Sci Biotechnol 12(3):223–234 8. Pimienta-Barrios E, Méndez-Morán L, Ramírez-Hernández B et al (2008) Efecto de la ingestión del fruto de xoconostle (O. joconostle Web.) sobre la glucosa y lípidos séricos. Agrociencia 42:645–653 9. Haminiuk CWI, Maciel GM, Plata-Oviedo MSV, Peralta RM (2012) Phenolic compounds in fruits – an overview. Int J Food Sci Technol 47(10):2023–2044 10. van Boekel M, Fogliano V, Pellegrini N et al (2010) A review on the beneficial aspects of food processing. Mol Nutr Food Res 54(9): 1215–1247 11. Tiwari U, Cummins E (2013) Factors influencing levels of phytochemicals in selected fruit and vegetables during pre- and postharvest food processing operations. Food Res Int 50(2):497–506 12. Morales P, Ramírez-Moreno E, Sanchez-Mata MC et al (2012) Nutritional and antioxidant properties of pulp and seeds of two xoconostle cultivars (O. joconostle F.A.C. Weber ex Diguet and O. matudae Scheinvar) of high consumption in Mexico. Food Res Int 46(1):279–285
13. Ferracane R, Pellegrini N, Visconti A et al (2008) Effects of different cooking methods on antioxidant profile, antioxidant capacity, and physical characteristics of artichoke. J Agric Food Chem 56(18): 8601–8608 14. Fernández-López J, Almela L, Obón J, Castellar R (2010) Determination of antioxidant constituents in cactus pear fruits. Plant Foods Hum Nutr 65(3):253–259 15. Ozgen M, Reese RN, Tulio AZ et al (2006) Modified 2,2azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2′-diphenyl-1-picrylhydrazyl (DPPH) methods. J Agric Food Chem 54(4):1151–1157 16. Ak T, Gülçin İ (2008) Antioxidant and radical scavenging properties of curcumin. Chem-Biol Interact 174(1):27–37 17. Turkmen N, Sari F, Velioglu YS (2005) The effect of cooking methods on total phenolics and antioxidant activity of selected green vegetables. Food Chem 93(4):713–718 18. Miglio C, Chiavaro E, Visconti A et al (2007) Effects of different cooking methods on nutritional and physicochemical characteristics of selected vegetables. J Agric Food Chem 56(1):139–147 19. Chuah AM, Lee Y-C, Yamaguchi T et al (2008) Effect of cooking on the antioxidant properties of coloured peppers. Food Chem 111(1): 20–28 20. Stewart AJ, Bozonnet S, Mullen W et al (2000) Occurrence of flavonols in tomatoes and tomato-based products. J Agr Food Chem 48(7): 2663–2669 21. Roy MK, Juneja LR, Isobe S, Tsushida T (2009) Steam processed broccoli (Brassica oleracea) has higher antioxidant activity in chemical and cellular assay systems. Food Chem 114(1):263–269 22. Herbach KM, Stintzing FC, Carle R (2006) Betalain stability and degradation—structural and chromatic aspects. J Food Sci 71(4): R41–R50 23. Sanchez-Gonzalez N, Jaime-Fonseca MR, San Martin-Martinez E, Zepeda LG (2013) Extraction, stability, and separation of betalains from Opuntia joconostle cv. using response surface methodology. J Agric Food Chem 61(49):11995–12004 24. Wong SP, Leong LP, William Koh JH (2006) Antioxidant activities of aqueous extracts of selected plants. Food Chem 99(4):775–783 25. Palermo M, Pellegrini N, Fogliano V (2014) The effect of cooking on the phytochemical content of vegetables. J Sci Food Agric 94(6): 1057–1070 26. Song L, Thornalley PJ (2007) Effect of storage, processing and cooking on glucosinolate content of Brassica vegetables. Food Chem Toxicol 45(2):216–224 27. López-Berenguer C, Carvajal M, Moreno DA, García-Viguera C (2007) Effects of microwave cooking conditions on bioactive compounds present in broccoli inflorescences. J Agric Food Chem 55(24):10001–10007 28. Vadivambal R, Jayas DS (2007) Changes in quality of microwavetreated agricultural products—a review. Biosyst Eng 98(1):1–16
