Bioscience Journal | 2021 | vol. 37, e37086 | ISSN 1981-3163 1 Diego WEBER1 , Jessica Fernanda HOFFMANN2 , Caroline Farias BARRETO3 , Giovana Paula ZANDONÁ4 , Jair Costa NACHTIGAL5 , Fabio Clasen CHAVES6 , Marcelo Barbosa MALGARIM7 ¹ Private Practice, Garopaba, Santa Catarina, Brazil. ² Institute of Technology of Food for Health, São Leopoldo, Rio Grande do Sul, Brazil. ³ Postgraduate Program in Agronomy, Federal University of Pelotas, Capão do Leão, Rio Grande do Sul, Brazil. 4 Postgraduate Program in Food Science and Technology, Federal Universityof Pelotas, Capão do Leão, Rio Grande do Sul, Brazil 5 Embrapa Temperate Agriculture, Pelotas, Rio Grande do Sul, Brazil. 6 Department of Agro-industrial Science and Technology Federal University of Pelotas, Capão do Leão, Rio Grande do Sul, Brazil. 7 Department of Agronomy, Federal University of Pelotas, Pelotas, Rio Grande do Sul, Brazil. Corresponding author: Caroline Farias Barreto Email: carol_fariasb@hotmail.com How to cite: WEBER, D., et al. Bioactive content of six passion fruit genotypes cultivated in southern Brazil. Bioscience Journal. 2021, 37, e37086. https://doi.org/10.14393/BJ-v37n0a2021-54096 Abstract Passion fruit production in Brazil is concentrated in tropical regions, however, recently production has expanded to regions with temperate climate. Cultivar performance in different climate and soil can lead to variation in the contents of bioactive compounds in the juice and rind of the fruit. This study characterized the bioactive content of passion fruit rind and juice of six passion fruit genotypes (‘Catarina Roxo’, ‘Catarina’, ‘Urussanga’, ‘BRS Gigante Amarelo’, ‘BRS Rubi do Cerrado’, and ‘BRS Sol do Cerrado’) cultivated in southern Brazil. Phenolic, flavonoid, anthocyanin, carotenoid, and ascorbic acid contents and the antioxidant potential of each fruit portion from each genotype were evaluated. Fruit composition varied with genotype and evaluated tissue. Bioactive compound contents were greatest in the rind of ‘Urussanga’ and ‘Catarina’, whereas the juice of ‘BRS Sol do Cerrado’ and ‘Catarina Roxo’ had the greatest bioactive content. Given cultivar and tissue variability for bioactive content, postharvest use of passion fruit will determine the choice of cultivar to obtain a product with maximum bioactive compounds. Passion fruit genotypes evaluated in this study have shown to be potential sources of bioactive compounds. Fruit rind has the potential to be explored in the scientific and technological scope, due to its high amounts of phenolic compounds and antioxidant activity. Keywords: Antioxidants. Fruit Rind. Juice. Passiflora spp. Phytochemicals. 1. Introduction Passion fruit is cultivated in tropical regions and in Brazil approximately 550 thousand tons of passion fruit are produced yearly in approximately 51 thousand hectares (IBGE 2019). Passion fruit cultivation has expanded to new regions within Brazil but there is little information on their implementation in such location including Rio Grande do Sul state, where average temperatures are low, and frost may occur during the winter (Weber et al. 2017; Barreto et al. 2019). Passion fruit species vary regarding fruit weight, diameter, color, rind thickness, taste, juice volume, acidity, and, consequently, the quantity of residues generated by the passion fruit processing industry. Such BIOACTIVE CONTENT OF SIX PASSION FRUIT GENOTYPES CULTIVATED IN SOUTHERN BRAZIL https://orcid.org/0000-0003-4118-4208 https://orcid.org/0000-0002-9185-3820 https://orcid.org/0000-0002-5568-5305 https://orcid.org/0000-0002-4025-9039 https://orcid.org/0000-0001-5393-6791 https://orcid.org/0000-0002-5773-0800 https://orcid.org/0000-0002-3584-5228 Bioscience Journal | 2021 | vol. 37, e37086 | https://doi.org/10.14393/BJ-v37n0a2021-54096 2 Bioactive content of six passion fruit genotypes cultivated in southern Brazil residues can be utilized into manufactured products and therefore possess potential commercial applications (Ayala-Zavala et al. 2011; Nascimento et al. 2012; Lopez-Vargas et al. 2013; Silva et al. 2014; Coqueiro et al. 2016). The main cultivated passion fruit species are sweet passion fruit (Passiflora alata Curtis), purple passion fruit (Passiflora edulis Sims.), and yellow passion fruit (Passiflora edulis Sims.). Passion fruit is consumed mainly fresh or as juice. Yellow passion fruit, the most cultivated fruit in Brazil, is predominantly utilized in juice processing (Meletti 2011) and this results in a large amount of waste because about 50% of the fruit weight is represented by the rind and seeds (Weber et al. 2016), which are usually discarded after processing. Bioactive compounds extracted from passion fruit juice and from passion fruit processing residues may be applied to pharmaceutical, cosmetics, chemical, and food industries (Oliveira et al. 2009). Processing passion fruit rind into a powder enables it to be mixed with other ingredients such as flours and to be added to baked goods, juices, and vitamins (Cazarini et al. 2014; Silva et al. 2014; Coqueiro et al. 2016). As a result, it contributes to add value to byproducts and impart functional potential to food (Zeraik et al. 2010; Coqueiro et al. 2016). Passion fruit pulp and rind are rich in compounds that may provide significant benefits to human health (Zeraik et al. 2012; Pertuzatti et al. 2015; Araújo et al. 2018). Fruit bioactive content includes fibers and antioxidant compounds, and their consumption has been associated with reduction of chronic- degenerative diseases (Rufino et al. 2010; Chen et al. 2012). Commercial passion fruit varieties are rich in bioactive compounds, including vitamin C, carotenoids, and phenolic compounds (Zeraik et al. 2010). These compounds may be affected by several factors, such as the genotype, edaphoclimatic conditions, cultivation system, and postharvest processing (Pertuzatti et al. 2015; Botelho et al. 2016). In this study fruit of six passion fruit cultivars were separated into juice and rind and each fruit part from each cultivar was evaluated for its bioactive composition. 2. Material and Methods Fruits were harvested from passionfruit vines grown on espaliers at the Centro Agropecuário da Palma (CAP), at Universidade Federal de Pelotas (UFPel), located in Capão do Leão, RS, Brazil. The region has a humid subtropical climate with hot summers, considered “Cfa” in Köppen climate classification. The mean temperature and mean annual rainfall during cultivation were 18.6ºC and 1,844.3 mm, respectively. The soil is moderately deep with medium texture at the A horizon and clay texture at the B horizon, and therefore classified as red-yellow clay soil. The soil consisted of 13% clay, 1.5% organic matter, 4% aluminum saturation, 61% base saturation, cation exchange capacity at pH 7 of 7.9 cmolc/dm³, 50.4 mg/dm3 of P-Mehlich, 65 mg/dm³ of K and pH 5.0. Fertilization was carried out according to the Manual of Fertilization and Liming for the States of Rio Grande do Sul and Santa Catarina (ROLAS, 2004), applying bovine manure at planting, increasing doses of nitrogen (Urea) every 15-20 days until flowering, followed by higher doses of phosphorus (simple superphosphate) and potassium (potassium chloride) divided into five plots, based on soil analysis. Liming was performed with dolomitic limestone (PRNT 85%) performed according to the Shoemaker-McLean-Pratt (SMP) index method, raising the pH to 6.0, according to Rolas (2004). ‘Catarina Roxo’ (Epagri), purple rind; ‘Catarina’ (Epagri), yellow rind; BRS Gigante Amarelo, yellow rind; BRS Rubi do Cerrado, yellow rind; and BRS Sol do Cerrado, yellow rind were all sour passion fruit (Passiflora edulis Sims.) while ‘Urussanga’ (Epagri), yellow rind was the only sweet passion fruit (Passiflora alata Curtis) type. The experimental design was completely randomized, with four replications. Twenty ripe fruits from every treatment were harvested. Fruits were washed, the pulp was separated from the rind and the juice was strained, packaged in plastic bags and frozen at -20ºC until analysis. The rind was oven dried at 60°C for 24 hours until the humidity content reached 10%. Then, it was ground using an industrial blender so that the powder had uniform particle size of 1 mm. Ground samples were stored in brown paper bags at room temperature (24°C) until analysis. For the analyses of phenolic compounds, flavonoids, and antioxidant capacity, either 2 g dry and ground rind or 2 mL of juice were extracted with 20 mL methanol. The mixture was homogenized by Bioscience Journal | 2021 | vol. 37, e37086 | https://doi.org/10.14393/BJ-v37n0a2021-54096 3 WEBER, D., et al. ultraturrax (7,500 rpm) for 1 min and centrifuged at 9,900 x g for 15 min at 15ºC. The supernatant was collected in 15 mL polypropylene tubes. Total phenolic compound content was determined according to the methodology proposed by Singleton and Rossi (1965) and results were expressed as mg gallic acid equivalent (GAE) per 100 g fresh weight. Total flavonoid content was determined by spectrophotometry (Zhishen et al. 1999) and results were expressed as mg catechin equivalent per 100 g fresh weight. Total anthocyanin content was determined according to the methodology proposed by Lees and Francis (1972) and results were expressed as mg cyaniding-3-glucoside equivalent per 100 g fresh weight. L-Ascorbic acid content was determined by high performance liquid chromatography (HPLC), using a Shimadzu HPLC system equipped with an automatic injector and a UV-Vis detector (254 nm), following a method adapted from Vinci et al. (1995) and results were expressed as mg L-Ascorbic acid equivalent per 100 g fresh weight. Carotenoid content was determined using the modified AOAC (2005) method 970.64 and results were expressed as mg β-carotene equivalent per 100 g fresh weight. Antioxidant potential was determined by the method proposed by Brand-Williams et al. (1995), with the use of the free radical 2,2-diphenyl-1-picrylhydrazyl (DPPH) and results were expressed as percentage (%) of DPPH radical remaining. Data were submitted to an analysis of variance (ANOVA). When the effect of the treatment was significant means were compared by Tukey’s test (p ≤ 0.05). To determine the correlation between the measured variables antioxidant potential, anthocyanin, ascorbic acid, carotenoids, flavonoids, and phenolic compounds, Pearson's correlation coefficients were calculated (p ≤ 0.05). 3. Results and Discussion Contents of total phenolic compounds found in passion fruit and rind (ranged from 118.6 to 192.3 mg GAE 100 g-1) did not differ (p≤0.05) among ‘Catarina Roxo’, ‘Catarina’, ‘BRS Gigante Amarelo’, and ‘Urussanga’ genotypes, and were higher than those found in ‘BRS Sol do Cerrado’ and ‘BRS Rubi do Cerrado’ genotypes (Table 1). Table 1. Phenolic, flavonoid, and anthocyanin contents of passion fruit juice and rind. Genotypes Phenolic compounds1 Flavonoids2 Anthocyanins3 Rind Juice Rind Juice Rind Juice Catarina Roxo 192.3±10.8a 36.7±5.4bc 48.5±4.1ab 5.0±1.2a 3.5±0.1c nd Gigante Amarelo 173.3±10.3a 28.3±2.0bc 39.4±3.3bc 3.7±1.0ab 5.5±0.5b nd Urussanga 190.4±20.7a 49.1±8.0a 56.0±3.4a 2.9±1.2b 9.1±0.7a nd Rubi do Cerrado 118.6±14.9b 26.1±2.4c 31.0±2.3c 3.1±1.1ab 5.6±1.3b nd Catarina 175.4±19.0a 27.9±5.0bc 54.0±9.8a 5.0±1.2a 7.2±1.2ab nd Sol do Cerrado 128.8±26.9b 36.7±5.4bc 62.0±10.0a 3.7±1.0ab 7.4±0.5ab nd Means followed by the same lowercase letter within a column do not differ from each other based on Tukey’s test (p ≤ 0.05). nd = not detected. 1mg gallic acid equivalent 100 g-1 fresh weight (fw); 2 mg catechin equivalent 100 g-1 fw; ³ mg cyanidin-3-glycoside equivalent 100 g-1 fw. Phenolic compound variation among passion fruit varieties depends on genetic and environmental factors as well as their interaction (Herrera 2012). Previous studies also reported variation in the phenolic contents of different passion fruit genotypes (Ramaiya et al. 2013; Casierra-Posada and Jarma-Orozco 2016). Ideal temperature for passion fruit cultivation ranges from 23°C to 27°C (Andrade Neto et al. 2015). Fruit evaluated in this study came from plants grown under summer months temperature ranging from 22°C to 25°C and winter months temperature ranging from 12 °C to 15 °C (Barreto et al. 2019). At lower temperature and higher altitude fruit production is delayed and fruit development takes longer (Fischer et al. 2018), which in turn may affect phenolic compound metabolism (Malheiro et al. 2015). Higher amounts of phenolic compounds found in passion fruit rind than in juice, direct a potential application of this residue into a product with health promoting appeal to due to the phenolics’ capacity of preventing various processes associated with oxidative stress (Chandrasekhar et al. 2019). Cazarin et al. (2014) studied Passiflora edulis Sims. passion fruit produced in Torre de Pedra, São Paulo and found contents of total phenolic compounds which ranged from 206 to 253 mg GAE 100 g -1 rind Bioscience Journal | 2021 | vol. 37, e37086 | https://doi.org/10.14393/BJ-v37n0a2021-54096 4 Bioactive content of six passion fruit genotypes cultivated in southern Brazil (fresh weight). It’s possible that the drying process at 60ºC for 24 h may have led to the degradation of phenolics, which explains the low contents found in this study (118 to 192 mg GAE 100 g-1). On the other hand, other studies with passion fruit grown in the states of Santa Catarina, Paraná, and Pernambuco found even lower total phenolic contents ranging from 20 to 83 mg GAE 100 g-1 fresh weight in passion fruit pulp (Kuskpski et al. 2006; Melo et al. 2008; Rotili et al. 2013). The highest content of phenolic compounds was found in the juice extracted from the ‘Urussanga’ genotype, which belongs to the group of sweet passion fruits (Table 1). Likewise, Cohen et al. (2008a) also found higher contents of phenolic compounds in sweet passion fruits than in sour ones ranging from 46 to 60 mg GAE 100 g-1; similar contents were observed in the current study. There seems to be a correlation between sugars and phenolic compounds. Positive correlation between glucose, fructose, and total sugar with the content of phenolic compounds has already been reported in passion fruit juice (Ramaiya et al. 2012). Flavonoid content in passion fruit rind ranged from 31.0 to 62.0 mg catechin 100 g-1. ‘BRS Sol do Cerrado’, ‘Urussanga’, ‘Catarina’, and ‘Catarina Roxo’ genotypes had higher flavonoid content than both ‘BRS Rubi do Cerrado’ and ‘BRS Gigante Amarelo’ genotypes (Table 1). In oven dried peel of passion fruit, was found a flavonoid concentration of 35.13 mg equivalent of quercetin 100 g-1 (Morais et al. 2015). The content of flavonoids found in passion fruit rind in this study was higher than those reported by Morais et al. (2015), with the exception of Rubi do Cerrado. Flavonoid content in passion fruit juice varied from 2.9 to 5.0 mg catechin 100 g-1 and ‘Catarina Roxo’ and ‘Catarina’ genotypes had the highest content in relation to ‘Urussanga’ (Table 1). Similar values were found by Cohen et al. (2008b), who found values between 3.0 to 4.73 mg 100 g-1 of flavonoids in the passion fruit pulp. Anthocyanins were not detected in passion fruit juice of the evaluated genotypes. The highest anthocyanin contents were found in the rind of ‘Urussanga’, ‘BRS Sol do Cerrado’, and ‘Catarina’ genotypes (Table 1). Kuskoski et al. (2006) also did not find anthocyanins in passion fruit juice, what is expected, since the fruit flesh of all genotypes are yellow, which indicates the presence of carotenoids, not anthocyanins (Acero et al. 2019). On the other hand, the peel of some passion fruits, as in the case of ‘Catarina Roxo’ has red / purple colors which is usually associated with the accumulation of anthocyanins. Throughout fruit development occurs degradation of chlorophyll and synthesis of pigments, such as yellow carotenoids and purple anthocyanins in the rind (Silva et al. 2008). Contents of ascorbic acid in the rind were higher in ‘Catarina’, ‘Urussanga’ and ‘BRS Gigante Amarelo’ genotypes (Table 2). Ascorbic acid content of passion fruit juice varied from 5.1 (Catarina) to 9.7 mg of L- ascorbic acid 100 g-1 (Catarina Roxo) (Table 2). Ascorbic acid is a very labile compound susceptible degradation by heat and oxidation and is usually utilized as quality control marker. Table 2. Ascorbic acid and carotenoid contents and antioxidant potential of passion fruit juice and rind. Genotypes Ascorbic acid1 Carotenoids2 Antioxidant potential3 Rind Juice Rind Juice Rind Juice Catarina Roxo 7.0±1.3b 9.7±2.1a 2.5±0.3b 8.8±2.2bc 49.1±2.9b 12.7±1.3ab Gigante Amarelo 6.8±3.0b 6.7±1.8bc 2.3±0.2b 11.0±2.7b 52.2±2.8ab 10.7±1.5b Urussanga 9.9±2.6ab 5.9±2.6bc 19.8±5.7a 5.0±1.4c 62.9±2.5a 7.3±1.7c Rubi 8.9±0.6ab 6.6±2.5bc 1.9±0.1b 9.6±2.9bc 33.1±3.5c 11.2±1.4b Catarina 12.1±1.4a 5.1±1.1c 3.7±1.4b 10.1±1.6b 54.2±2.7ab 10.9±1.5b Sol do Cerrado 2.7±0.4c 8.2±2.0ab 1.6±0.1b 18.1±0.7a 48.7±2.9b 13.9±1.3a Means followed by the same lowercase letter within a column do not differ from each other based on Tukey’s test (p ≤ 0.05). 1 mg L-ascorbic acid equivalent 100g-1 fresh weight (fw); 2 mg β-carotene equivalent 100 g-1 fw. 3 % of DPPH radical remaining. Total carotenoid content of fruit rind varied from 1.6 (Sol do Cerrado) to 19.8 mg equivalent β- carotene 100 g-1 (Urussanga) (Table 2). Rind of ‘Urussanga’ genotype had the highest carotenoid content of all genotypes meanwhile ‘Urussanga’ juice had the lowest carotenoid content (along with Rubi and Catarina Roxo) (Table 2). Sepúlveda et al. (1996) observed 1.57 to 3.22 mg equivalent β-carotene 100 g-1 in passion fruit (Passiflora edulis) and that the harvest season influences carotenoid content, with fruit grown during winter months yielding greater carotenoid content than those grown during summer months. Therefore, the Bioscience Journal | 2021 | vol. 37, e37086 | https://doi.org/10.14393/BJ-v37n0a2021-54096 5 WEBER, D., et al. cultivation of passion fruit in the southern colder regions has the potential to yield juices with more intense colors and higher contents of carotenoids. The rind of ‘Urussanga’, ‘Catarina’, and ‘BRS Gigante Amarelo’ genotypes had the highest antioxidant capacity (Table 2). Cazarin et al. (2014) found yellow passion fruit antioxidant capacity measured as inhibition % of the radical DPPH ranging from 46.4% and 29.6%, similar to the ones of the ‘BRS Rubi do Cerrado’ and ‘BRS Sol do Cerrado’ genotypes (Table 2). Regarding the antioxidant capacity of the juice, ‘BRS Sol do Cerrado’ and ‘Catarina Roxo’ genotypes had the highest values, whereas the ‘Urussanga’ genotype had the lowest ones (Table 2). It is possible that the highest antioxidant potential found in passion fruit rind may be in part due to anthocyanins do not present in the fruit juice (Zeraik 2010). Positive and strong correlation was observed between phenolic content and antioxidant potential (r=0.8092), positive and moderate correlations were observed between both flavonoid (r=0.6108) and carotenoid (r=0.5406) contents with antioxidant potential, and positive and low correlation was observed between anthocyanin and antioxidant potential (r=0.4084) in passion fruit rind (Table 3). In addition, antioxidant potential of fruit rind was negatively correlated with ascorbic acid content (r= - 0.4121) (Table 3). Table 3. Pearson's correlation coefficients (r) comparison of variables measured in passion fruit juice. Ascorbic acid Carotenoid Flavonoid Phenolic compounds Antioxidant potential Ascorbic acid 1.0000 0.3435 0.5331* 0.1674 0.6748* Carotenoid 1.0000 0.4723* -0.1801 0.7094* Flavonoid 1.0000 0.0705 0.4765* Phenolic 1.0000 -0.2324 Antioxidant potential 1.0000 * Significant at p ≤ 0.05. In passion fruit juice the antioxidant potential was positively correlated with ascorbic acid (r=0.6748), carotenoid (r=0.7094), and flavonoid contents (r=0.4765) (Table 3). No significant correlation was observed between phenolic compounds and antioxidant potential in passion fruit juice. On the other hand, passion fruit rind antioxidant potential was more strongly correlated with total phenolic content (r=0.8092). Melo et al. (2008) and Rotili et al. (2013) had found a weak correlation between fruit phenolic content and antioxidant capacity. However, many other authors have shown a strong positive correlation between total phenolic content and the antioxidant capacity of fruits (Leja et al. 2003; Abdille et al. 2005; Kuskoski et al. 2006; Gruz et al. 2011). The variation observed for the correlation coefficients indicate that the overall antioxidant capacity of the fruit may be better explained from the added contributions from all the different components with antioxidant properties instead of their isolated impact. Table 4. Pearson's correlation coefficients (r) comparison of variables measured in passion fruit rind. Anthocyanin Ascorbic acid Carotenoid Flavonoid Phenolic compounds Antioxidant potential Anthocyanin 1.0000 -0.0373 0.5857* 0.4879* -0.0587 0.4084* Ascorbic acid 1.0000 0.0341 -0.6746* -0.1799 -0.4121* Carotenoid 1.0000 0.2796 0.3588 0.5406* Flavonoid 1.0000 0.3028 0.6108* Phenolic 1.0000 0.8092* Antioxidant potential 1.0000 * Significant at p ≤ 0.05. Bioscience Journal | 2021 | vol. 37, e37086 | https://doi.org/10.14393/BJ-v37n0a2021-54096 6 Bioactive content of six passion fruit genotypes cultivated in southern Brazil 4. Conclusions Differences in contents of bioactive compounds were genotype and tissue dependent and therefore postharvest use of passion fruit will determine the choice of cultivar to obtain a product with maximum bioactive compounds. Authors' Contributions: WEBER, D.: conception and design, acquisition of data, analysis and interpretation of data, drafting the article; HOFFMANN, J.F.: acquisition of data, analysis and interpretation of data, drafting the article; BARRETO, C.F.: conception and design, analysis and interpretation of data, drafting the article; ZANDONA, G.P.: acquisition of data, analysis and interpretation of data, drafting the article; NACHTIGAL, J.C.: drafting the article; CHAVES, F.C.: analysis and interpretation of data, drafting the article; MALGARIM, M.B.: drafting the article. All authors have read and approved the final version of the manuscript. Conflicts of Interest: The authors declare no conflicts of interest. Ethics Approval: Not applicable. Acknowledgments: The authors would like to thank the funding for the realization of this study provided by the Brazilian agencies SDECT (Secretaria de Desenvolvimento Econômico e Turismo do Rio Grande do Sul - Brasil), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil), Finance Code 001. References ABDILLE, M.H., SINGH, R.P., JAYAPRAKASHA, G.K. and JENA, B.S. Antioxidant activity of the extracts from Dillenia indica fruits. Food Chemistry. 2005, 90, 891-896. http://dx.doi.org/10.1016/j.foodchem.2004.09.002 ACERO, N., et al. Comparison of phenolic compounds profile and antioxidant properties of different sweet cherry (Prunus avium L.) varieties. Food Chemistry. 2019, 278(1), 260-271. https://doi.org/10.1016/j.foodchem.2018.12.008 ANDRADE NETO, R. de C., et al. Recomendações técnicas para o cultivo do maracujazeiro-amarelo cvs. BRS Gigante Amarelo e BRS Sol do Cerrado. Comunicado técnico 187. 2015, 1(1), 1-12. ARAÚJO, A.C.M.S., et al. 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Food Chemistry. 1999, 64, 555-559. http://dx.doi.org/10.1016/S0308-8146(98)00102-2 Received: 24 April 2020 | Accepted: 30 October 2020 | Published: 29 December 2021 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. https://doi.org/10.1590/S0102-695X2010000300026 https://doi.org/10.1590/S0100-40422012000300019 http://dx.doi.org/10.1016/S0308-8146(98)00102-2