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Antioxidant activity and phenolic content of leaf infusions of Myrtaceae species from Cerrado (Brazilian Savanna)/Atividade antioxidante e conteudo fenolico de infusoes foliares de especies de Myrtaceae do Cerrado (Savana Brasileira).

1. Introduction

Free radicals and other small reactive molecules have emerged as important regulators of many physiological and pathological processes (Nathan and Ding, 2010). Increased levels of these short-lived reactive molecules can cause oxidative damage to biological macromolecules and disrupt the cellular reduction-oxidation (redox) balance (Dowling and Simmons, 2009). Oxidative stress caused by the accumulation of free radicals in the body is involved in various pathological processes including cardiovascular diseases, cancer, neurodegenerative disorders, and aging (Yoshihara et al., 2010).

An antioxidant is a compound that can delay or inhibit the oxidation of lipids or other molecules by blocking the initiation or propagation of oxidative chain reactions, which prevents or repairs the damage done to the cells by oxygen (Tachakittirungrod et al., 2007). The consumption of natural antioxidants presents potential health benefits (Yoshihara et al., 2010). Thus, there is considerable interest in finding new antioxidants from plant materials. Antioxidant compounds from plants, particularly polyphenols, can inhibit the propagation of free radical reactions and protect the human body from diseases (Perron and Brumaghim, 2009; Lizcano et al., 2010).

Several studies have emphasized the antioxidant activity of species belonging to the Myrtaceae family such as Feijoa sellowiana (Weston, 2010), Psidium guajava (Tachakittirungrod et al., 2007), and Eucalyptus rostrata (Okamura et al., 1993). Furthermore, many members of this family are used in folk medicine, mainly as antidiarrheal, antimicrobial, cleansing, antirheumatic, anti-inflammatory, and cholesterol-lowering agents (Stefanello et al., 2011). However, there are few reports on the antioxidant activity of Myrtaceae species from the Cerrado (Brazilian savanna), although phytochemical studies reveal the presence of quercetin and kaempferol, which are compounds considered to be potent antioxidants (Imatomi et al., 2013). Therefore, in the present study, we aimed to evaluate the antioxidant activity and quantify polyphenols in leaf infusions of 12 Myrtaceae species from the Cerrado.

2. Material and Methods

2.1. Plant materials

Leaves of 12 Myrtaceae species with no signs of herbivory or disease (from at least three individuals per species) were collected in a cerrado sensu stricto area of the Universidade Federal de Sao Carlos (21[degrees]58'5"S and 47[degrees]53'12"W), Sao Carlos, Sao Paulo, Brazil, on July 15, 2013.

Voucher specimens were deposited at the Herbarium of the Universidade Federal de Sao Carlos. The 12 species included Blepharocalyx salicifolius (Kunth) O. Berg (8308), Eugenia bimarginata O. Berg (8310), Eugenia dysenterica DC. (8545), Eugenia klotzschiana O. Berg (8311), Hexachlamys edulis (O. Berg) Kausel & D. Legrand (8546), Myrcia bella Cambess. (8314), Myrcia lingua (O. Berg) Mattos (8315), Myrcia splendens DC. (8317), Myrcia tomentosa DC. (8318), Psidium australe Cambess. (8319), Psidium cinereum Mart. (8320), and Psidium laruotteanum Cambess. (8321). After collection, the leaves were dried at 40[degrees]C for 48 h and ground in an electric mill.

Green tea is commonly used for its antioxidant properties (Senanayake, 2013). Thus, a commercial green tea (dry leaves and stalks of Camellia sinensis (L.) Kuntze) was used for comparison with Myrtaceae species, Yamamatoyama (Midori Industria de Cha Ltda., lot number: 242).

2.2. Chemicals

The reagents used in the experiment were DPPH (2,2-diphenyl-1-picrylhydrazyl) and quercetin from Sigma Aldrich, Folin-Ciocalteu reagent from Haloquimica, gallic acid from Vetec, anhydrous sodium carbonate, and methanol from Synth.

2.3. Infusion extraction

The extraction was performed with 20 g of powdered dry leaves of Myrtaceae or green tea and 200 mL of distilled water for 10 min in a thermostatic water bath at 95[degrees]C. The extracts were filtered through a filter paper (pore size = 3 [micro]m) in a Buchner funnel and lyophilized (Terroni Enterprise I lyophilizer). The yields were calculated on dry weight basis of the plant material.

2.4. Total phenolics determination assay

The total phenolic content (TPC) in the extracts was determined by a modified Folin-Ciocalteu method (George et al., 2005). Extracts were diluted in distilled water (0.4 mg/5 mL) and 0.5 mL of the diluted solutions or distilled water (blank) were each mixed with 2.5 mL of Folin-Ciocalteu reagent (1/10, pre-diluted with distilled water). After allowing the diluted extracts to stand for 2 min at room temperature, 2 mL of aqueous [Na.sub.2]C[O.sub.3] solution (75 g/L) was added to each of them. The mixture was vortexed, incubated for 15 min at 50[degrees]C, and cooled in an ice water bath. Sample absorbances were measured at 760 nm. A calibration curve was prepared with gallic acid (1-8 [micro]g x mL.sup.-1]). TPC was expressed as milligrams of gallic acid equivalents (GAE) per gram of dry extract according to the calibration curve, y = 0.133x + 0.001 ([r.sup.2] = 0.999), where y denotes absorbance and x denotes gallic acid concentration in mg/L.

2.5. Antioxidant activity assay

The antioxidant properties of the samples were assessed by the DPPH method (Scherer and Godoy, 2009). Methanolic solutions of the extracts (0.05 mL) at six different concentrations were added to 1.95 mL of DPPH methanolic solution at 0.08 mM. Methanol PA and 2 commercial antioxidants, gallic acid and quercetin, were used as negative and positive controls, respectively. After 90 min of incubation in the dark at room temperature, the absorbances of the samples were measured at 517 nm (Femto spectrophotometer, model 800XI). Antioxidant activity index (AAI) was calculated as follows: AAI = (final concentration of DPPH in the reaction)/[IC.sub.50], where the final concentration of the reaction was 30.75 [micro]g x mL.sup.-1]. The concentration for 50% inhibition ([IC.sub.50]) was calculated by the linear regression equation between the extract concentration and the corresponding scavenging effect. The scavenging effect was calculated as follows: I% = [([Abs.sub.0] - [Abs.sub.1]/[Abs.sub.0]] x 100, where [Abs.sub.0] indicates absorbance of the negative control, and [Abs.sub.1] is the absorbance with the tested extract at different concentrations. Scherer and Godoy (2009) established the following criteria of AAI values for plant extracts: poor activity < 0.05 < moderate < 1.0 < strong < 2.0 < very strong.

2.6. Data analysis

Assays were performed in triplicates. The data were compared by ANOVA and Tukey test (a = 0.05). Correlations between TPC and AAI values were calculated. Statistical analyses were performed with PAST software, version 2.5 (Hammer et al., 2001).

3. Results

Extraction yields between 10.4% and 29.2% were obtained after the infusion of powdered dry leaves in distilled water and lyophilization (Table 1). There was a high correlation between phenolic contents and antioxidant activities of these extracts. The determination coefficient ([r.sup.2]) between them was 0.767 (Figure 1).

The phenolic contents of these extracts were in the range of 287.98-576.56 mg GAE/g extract (Table 1). P. laruotteanum, B. salicifolius, E. klotzschiana, E. dysenterica, H. edulis, and M. tomentosa showed a significantly higher TPC than that found in green tea. TPC of these species ranged from 412.10 to 576.56 mg GAE/g extract, whereas the value of green tea was 259.53 mg GAE/g extract. The highest TPC was found in P. laruotteanum, which was more than twice the amount obtained for green tea. Phenolics also represented at least one fourth of the extract weights from the remaining five species (287.98-324.72 mg GAE/g extract).

In addition, all infusion extracts presented very strong AAIs (>2) according to the criteria established by Scherer and Godoy (2009) for plant extracts (Table 1). The [IC.sub.50] values were lower than 13 [micro]g x mL.sup.-1], considering a final concentration of DPPH in the reaction of 30.75 [micro]g x mL.sup.-1]. P. laruotteanum was also the most potent antioxidant (AAI = 7.97) with activity close to that of quercetin (AAI = 10.35), corresponding to one third of that of pure gallic acid (AAI = 23.23). Nine species statistically displayed the same antioxidant potential as that of green tea (AAI = 4.13), which was equivalent to half the activity of quercetin.

4. Discussion

Extract's yield and chemical composition are determined by the extraction method (Dai and Mumper, 2010). Water infusion is a simple, fast, cheap, and non-toxic procedure to extract phenolic compounds efficiently because of their water polarity. Therefore, this method was used in our study, resulting in high extraction yields of phenolics.

Phenolics are the most abundant secondary metabolites in plants (Dai and Mumper, 2010). Myrtaceae species have the ability to accumulate phenolics (Salvador et al., 2011). These organic compounds are important defense antioxidants (Pietta, 2000), which are more potent than Vitamin C and E and carotenoids (Rice-Evans et al., 1996). Some authors reported phenolic contents in leaves of other Myrtaceae species. Coutinho et al. (2008) found a TPC of 7.2-21.2 mg GAE/g extract in Campomanesia adamantium. Salvador et al. (2011) reported high values for Eugenia chlorophylla, Eugenia pyriformis, Myrcia laruotteana, and Myrcia obtecta (343.7-429.3 mg GAE/g extract). In these studies, the extraction methods were different. They used organic solvents such as hexane, chloroform, methanol, and ethanol. However, some of our TPC values were still higher than these results.

Phenolic content and antioxidant activity are parameters of quality for tea pertaining to its biological properties (Anesini et al., 2008). For this reason, several studies have been performed to evaluate these parameters and their functional properties (e.g., anti-inflammatory or anticarcinogenic activity) (Yao et al., 2006; Chan et al., 2007; Anesini et al., 2008; Nishiyama et al., 2010; Senger et al., 2010). In our study, green tea was used as another reference (in addition to the pure substances, quercetin, and gallic acid) due to its abundance of flavonoids, including catechins and their derivatives, which may constitute up to 30% of its dry weight (Lorenzo et al., 2013). In our study, leaf infusions of Myrtaceae species showed phenolic concentrations similar to or even higher than those of green tea.

AAI by the DPPH method was used because it is considered appropriate for comparing extracts and pure compounds. There is no difference in AAI values when different solutions of DPPH and concentrations of the compounds/extracts are used (Scherer and Godoy, 2009).

The relation of extraction yield, TPC and antioxidant activity must be taken into account in the analysis of results. One species can display high TPC and AAI values but low yield. Others may display lower antioxidant activity but higher extraction yield. The understanding of the balance between these factors is necessary for further studies and their application. Despite this variation, the studied species displayed high antioxidant activities and can be considered as promising for future studies. Psidium laruotteanum was the most potent, possessing the highest phenolic content and antioxidant activity.

To the best of our knowledge, this is the first comparative survey on the antioxidant potential of Myrtaceae leaf infusions from the Cerrado. The focus of antioxidant studies in the Myrtaceae family from Brazil has been on edible fruits (Marin et al., 2008; Rufino et al., 2009, 2010; Pereira et al., 2012) with few reports on leaves (Coutinho et al., 2008; Salvador et al., 2011). Thus, our results contribute valuable knowledge about the bioactive properties of native Myrtaceae species.

Further studies should be conducted to isolate, characterize, and understand the mode of action of these phenolic compounds. Likewise, evaluation of the effect of environmental abiotic factors, such as temperature and humidity, on the production and concentration of these compounds is desirable.

http://dx.doi.org/10.1590/1519-6984.03314

Acknowledgements

We are grateful to CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico) for providing a scholarship to the first author and for funding the Research Productivity Grant of the third author.

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L. K. Takao (a) *, M. Imatomi (b) and S. C. J. Gualtieri (a)

(a) Programa de Pos-Graduacao em Ecologia e Recursos Naturais, Universidade Federal de Sao Carlos--UFSCar, Rodovia Washington Luis, km 235, CP 676, CEP 13565-905, Sao Carlos, SP, Brazil

(b) Departamento de Botanica, Universidade Federal de Sao Carlos--UFSCar, Rodovia Washington Luis, km 235, CP 676, CEP 13565-905, Sao Carlos, SP, Brazil

* e-mail: lktakao@gmail.com

Received: February 19, 2014--Accepted: April 16, 2014--Distributed: November 30, 2015

(With 1 figure)

Table 1. Antioxidant activity index (AAI) and total phenolic
content (TPC) of leaf infusions from 12 Myrtaceae species.

                                 [r.sup.2]
DPPH: 30.75
[micro]g x [mL.sup.-1]     I        II        III

Gallic acid              0.996     0.998     0.997
Quercetin                0.994     0.998     0.993
Psidium laruotteanum     0.997     0.997     0.998
Blepharocalyx            0.998     0.995     0.997
  salicifolius
Eugenia klotzschiana     0.996     0.996     0.961
Eugenia dysenterica      0.990     0.991     0.996
Hexachlamys edulis       0.991     0.989     0.997
Psidium australe         0.987     0.990     0.994
Green tea                0.984     0.982     0.982
Myrcia tomentosa         0.988     0.993     0.999
Myrcia bella             0.995     0.988     0.998
Myrcia lingua            0.984     0.971     0.988
Psidium cinereum         0.993     0.970     0.993
Myrcia splendens         0.996     0.994     0.995
Eugenia bimarginata      0.945     0.992     0.996

                         Mean [IC.sub.50]
DPPH: 30.75                 ([micro]g x
[micro]g x [mL.sup.-1]     [mL.sup.-1])      Mean AAI [+ or -] SD

Gallic acid                    1.33          23.23 [+ or -] 1.14   a
Quercetin                      2.99          10.35 [+ or -] 0.92   b
Psidium laruotteanum           3.86           7.97 [+ or -] 0.36   c
Blepharocalyx                  6.24           4.95 [+ or -] 0.39   d
  salicifolius
Eugenia klotzschiana           6.40           4.81 [+ or -] 0.26   de
Eugenia dysenterica            6.83           4.52 [+ or -] 0.37   de
Hexachlamys edulis             6.93           4.44 [+ or -] 0.23   de
Psidium australe               7.10           4.35 [+ or -] 0.30   de
Green tea                      7.45           4.13 [+ or -] 0.01   de
Myrcia tomentosa               7.46           4.13 [+ or -] 0.17   de
Myrcia bella                   7.73           3.99 [+ or -] 0.24   de
Myrcia lingua                  7.80           3.95 [+ or -] 0.16   de
Psidium cinereum               8.75           3.52 [+ or -] 0.21   ef
Myrcia splendens               12.48          2.47 [+ or -] 0.14   f
Eugenia bimarginata            12.83          2.40 [+ or -] 0.05   f

                                  Mean TPC [+ or -] SD
DPPH: 30.75
[micro]g x [mL.sup.-1]    (mg GAE/g dry extract)   yield   Extraction
                                                   (%) *

Gallic acid                        --                          --
Quercetin                          --                          --
Psidium laruotteanum      576.56 [+ or -] 21.82      a        22.6
Blepharocalyx             431.70 [+ or -] 10.63     bc        23.2
  salicifolius
Eugenia klotzschiana      461.50 [+ or -] 12.38      b        25.3
Eugenia dysenterica       412.10 [+ or -] 17.20      b        25.6
Hexachlamys edulis        422.10 [+ or -] 44.16     bcd       10.4
Psidium australe          359.26 [+ or -] 11.91    bcdef      29.2
Green tea                 259.53 [+ or -] 4.30       f        16.2
Myrcia tomentosa          463.69 [+ or -] 54.42      b        18.0
Myrcia bella              312.99 [+ or -] 8.60      ef        19.4
Myrcia lingua             318.93 [+ or -] 47.69     def       25.8
Psidium cinereum          324.72 [+ or -] 3.28      def       22.6
Myrcia splendens          287.98 [+ or -] 55.66      f        19.4
Eugenia bimarginata       318.93 [+ or -] 57.43     def       24.3

Gallic acid and quercetin: reference antioxidants. Green tea:
reference antioxidant infusion. [r.sup.2]: determination
coefficient of free radical scavenging effect on the
concentration of the substance-extract I, II, and III (three
repetitions). [IC.sub.50]: concentration for 50% inhibition. SD:
standard deviation. Different letters: significant difference
(p < 0.05). GAE: gallic acid equivalents. --: not evaluated.
*: dry weight basis.
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Title Annotation:Original Article
Author:Takao, L.K.; Imatomi, M.; Gualtieri, S.C.J.
Publication:Brazilian Journal of Biology
Date:Nov 1, 2015
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