ORIGINAL PAPER
Chemical Composition and Nutritional Value of Unripe Banana Flour ( Musa acuminata , var. Nanicão)
Elizabete Wenzel Menezes&Carmen Cecília Tadini&Tatiana Beatris Tribess&
Angela Zuleta&Julieta Binaghi&Nelly Pak&Gloria Vera&Milana Cara Tanasov Dan&
Andréa C. Bertolini&Beatriz Rosana Cordenunsi&Franco M. Lajolo
Published online: 6 July 2011
#Springer Science+Business Media, LLC 2011
Abstract Banana flour obtained from unripe banana (Musa acuminata, var. Nanicão) under specific drying conditions was evaluated regarding its chemical composition and nutritional value. Results are expressed in dry weight (dw). The unripe banana flour (UBF) presented a high amount of total dietary fiber (DF) (56.24 g/100 g), which consisted of resistant starch (RS) (48.99 g/100 g), fructans (0.05 g/100 g) and DF without RS or fructans (7.2 g/100 g).
The contents of available starch (AS) (27.78 g/100 g) and
soluble sugars (1.81 g/100 g) were low. The main phytosterols found were campesterol (4.1 mg/100 g), stigmasterol (2.5 mg/100 g) and β-sitosterol (6.2 mg/
100 g). The total polyphenol content was 50.65 mg GAE/
100 g. Antioxidant activity, by the FRAP and ORAC methods, was moderated, being 358.67 and 261.00μmol of Trolox equivalent/100 g, respectively. The content of Zn, Ca and Fe and mineral dialyzability were low. The procedure used to obtain UBF resulted in the recovery of undamaged starch granules and in a low-energy product (597 kJ/100 g).
Keywords Antioxidant activity. Dietary fiber. Resistant starch . Starch microscopy. Unripe banana flour
Abbreviations
AAPH 2, 2′-azobis (2-amidinopropane)
AS Available starch
DF Dietary fiber
FRAP Ferric reducing antioxidant power GOD/POD/ABTS Glucose-oxidase-peroxidase/2,
2′-Azino-di-[3-ethylbenzthiazoline]
sulfonate
ORAC Oxygen radical absorbance capacity
RS Resistant starch
TS Total starch
UBF Unripe banana flour
Introduction
Bananas are mainly produced in tropical and subtropical developing countries. According to the FAO [1], Brazil is E. W. Menezes
:
M. C. T. Dan:
B. R. Cordenunsi:
F. M. LajoloDepartment of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil
C. C. Tadini
:
T. B. TribessDepartment of Chemical Engineering, Escola Politécnica, University of São Paulo,
São Paulo, Brazil A. Zuleta
:
J. BinaghiFaculty of Pharmacy and Biochemistry, University of Buenos Aires,
Buenos Aires, Argentina N. Pak
:
G. VeraDepartment of Nutrition, Faculty of Medicine, University of Chile,
Santiago, Chile A. C. Bertolini
EMBRAPA Food Technology, Rio de Janeiro, RJ, Brazil E. W. Menezes (*)
Departamento de Alimentos e Nutrição Experimental, FCF, Universidade de São Paulo,
Av. Prof Lineu Prestes, 580, Bl 14, CEP 05508–900, São Paulo, Brazil e-mail: [email protected]
responsible for approximately 9% of the world banana production; it is the fourth largest world producer after India, China and the Philippines. However, Brazil is responsible for only 1.1% (186 thousand tons) of banana exports [2]. Bananas are a very delicate commodity for economic, social, environmental and political reasons.
Nevertheless, Brazil’s share of world banana trade increased slightly over the last decades (from around 18% in the 1960’s and 1970’s to over 22% in the 1990’s and 2000’s).
Since approximately one-fifth of all bananas harvested in Brazil are wasted, UBF could provide a means to minimize losses and increase market share [3]. When bananas are still unripe, they are easily transported and can be stored longer.
Unripe banana has thus been considered an ideal product for industrialization, in addition to its high RS content and low soluble sugar concentrations [4]. An innovative approach has been taken to exploring unripe banana flour as a functional ingredient, and its regular consumption can be expected to confer health benefits in humans [5].
Starch is the main component of unripe banana, corresponding to 60–80 g/100 g (dw) of the fruit, a percentage range similar to that of corn or potatoes [3].
According to Juarez-Garcia et al. [5], UBF produced under specific conditions is composed as follows: 73.4 g/100 g total starch, 17.5 g/100 g RS and 14.5 g/100 g DF content.
It is important to notice that producing UBF with high RS content and considering it a functional ingredient requires the differentiation of the stages of banana ripeness.
Ripeness may influence technical aspects of the processing and results in different chemical compositions.
According to Saura-Calixto [6], the indigestible fraction of foods is made of dietary fiber and other compounds that are resistant to the action of digestive enzymes, such as resistant starch, resistant protein and associated bioactive compounds (polyphenols, carotenoids, phytosterols and others); in tropical fruits, like mango, lime and guava, their indigestible fraction presented high antioxidant activity. In 2009, Goñi et al. [7] showed that a significant quantity of polyphenols is associated to fiber, which contribute to the antioxidant activity of fruits and vegetables, and they are also fermentable substrates to the microbiota. Phytosterols such as campesterol, β-sitosterol, and stigmasterol occur widely in plants, though in variable amounts. Steryl esters and free sterols are the major lipophilic component found in unripe banana peel, while free fatty acids and sterols dominate banana pulp [8], banana is rich in fatty acids, phytosterols and steryl glucosides. Therefore, evaluation of the antioxidant activity and specific bioactive compounds, in unripe bananas is of great interest. Besides the carbohydrates, unripe banana is a source of other nutrients.
Banana contains a considerable amount of mineral elements, and could serve as a source of minerals in human and animal diets [9].
Mainly because of the high banana waste and due to the unripe banana nutritional characteristics, the production of banana flour, in pilot scale, was developed by the University of São Paulo (Patent deposit in July 12, 2007, I.N.P.I./SP—n° 018070044163). Part of the thermal prop- erties of this flour was described by Tribess et al. [10], whereas it is necessary to evaluate its chemical and nutritional properties. The aim of this work was to evaluate the chemical composition and nutritional value of unripe banana flour produced according to the conditions described in the patent.
Material and Methods
Raw Material A pure triploid (AAA group) of Musa acuminata, subgroup Cavendish (called Nanicão in Brazil), consumed as a dessert when ripe, was used for this study.
Banana fruits were grown in Vale do Ribeira, São Paulo, purchased from a local market, characterized as unripe banana at the first stage of maturation [10] and were not submitted to a maturation chamber. The first stage of maturation for this cultivar means values near the following ones: pH (5.3); soluble solids (3.5 °Brix), titratable acidity (0.37 g malic acid/100 g); total solids (33.3 g/100 g) and firmness (25.8 N) [10].
UBF Production It was elaborated according to Tribess et al. [10]. Unripe banana fruits were weighed, rinsed with aseptic solution (sodium hypochlorite 10 g/l), hand peeled and immediately rinsed in citric acid solution (1 g/l). Peeled bananas were cut into about 4 mm-thick slices with a knife on a polyethylene cut board and again rinsed in the same solution. Banana slices were dried at a temperature of 55 °C and an air velocity of 1.0 m/s in a pilot plant-scale tray dryer (Proctor and Schwartz, model K11556, Philadelphia, USA). The air temperature and product weight were controlled during the dehydration process until a constant mass was obtained (for about 6 h). The air temperature was adjusted and controlled to be lower than the starch gelatinization temperature (<68 °C). After dehydration, the slices were ground in an MA 680 mill (Marconi, Piracicaba, Brazil) to 250 μm. Samples of the flour produced were packaged aseptically in aluminized plastic bags (100 g) and stored at ambient temperature until further analysis could be carried out. The thermal and physico-chemical character- istics of UBF obtained by this process were previously evaluated [10].
Chemical Analysis Moisture (925.45), total protein (960.52), fat (920.39) and ash (923.03) contents were determined according to AOAC methods [11]. The conversion factor used for protein determination was N g=100 g6:25.
Atwater factor was used to calculate energy value. The analyses were conducted in triplicate and the results are expressed as means ± SD.
Carbohydrates Soluble sugars were extracted three times with ethanol (80 ml/100 ml) at 80 °C, the supernatants were combined and the ethanol was evaporated under vacuum.
The residues were reconstituted with water, filtered through 0.22 μm membrane filters and analyzed by high- performance anion exchange chromatography coupled with pulsed amperometric detection (HPAE-PAD). The chro- matographic analysis was performed on a Dionex DX 500 instrument equipped with a PAD system (ED 40) (Dionex, Sunnyvale, CA). The analytical column employed was a Carbopac PA1 (250×4 mm, 5μm particle size). The mobile phase was 18 mmol NaOH and the flow rate was kept constant at 1.0 ml/min. Injections (25μl) were made using an AS 500 autosampler. Glucose, fructose, galactose, maltose and sucrose were used as commercially available standard.
Total starch was determined as follows: the starch from samples was solubilized in 0.5 mol/l NaOH and neutralized with 0.5 mol/l acetic acid. An aliquot was precipitated with 80 ml/100 ml ethanol. The precipitated starch was hydrolyzed with amyloglucosidase (Sigma A-7255, 28 U/ml) and the resultant glucose was determined with the GOD/POD/ABTS (Sigma Chemical Co. St. Louis, MO) mixture as described by Cordenunsi & Lajolo [4]. Wheat starch (S-1514) from Sigma Chemical Co., St. Louis, MO, was used as commercially available standard and total starch was calculated as glucose
× 0.9. Available starch was calculated as the difference between the content of total starch and RS.
The RS analysis was conducted according to AOAC method 2002.02 [12, 13]. A sample of boiled beans was used as in-house reference material. Glucose was quantified in the supernatants with a GOD/POD/ABTS mixture as described for total starch.
The fructans were determined according to AOAC method 999.03 [14] using a Megazyme fructan HK kit (Megazyme International Ireland Ltd., Wicklow, Ireland).
DF was quantified by the enzymatic-gravimetric method according to AOAC method 991.43 [15] with modifications.
The modifications were proposed by McCleary & Rossiter [16] in order to exclude RS and fructans from the DF. Total DF was determined as the sum of the DF (without fructans and/or RS), fructans and RS.
Minerals and Mineral Dialyzability Total mineral content was analyzed by flame atomic absorption spectroscopy (AAS, Analyst 400, Perkin Elmer Shelton, CT, USA) after washing with HNO3-HCLO4(50:50). Lanthanum (0.5 g/100 ml) was added to all samples analyzed for Ca to prevent possible phosphate interference [17].
The dialyzability of iron, zinc and calcium (FeD%, ZnD%, and CaD%) were determined as a modification of the widespread in vitro Miller’s method [18] according to Wolfgor et al. [19]. Aliquots (50 g) of homogenized samples were adjusted to pH 2.0, and after the addition of 1.6 mL of pepsin digestion mixture, they were incubated at 37 °C in a shaking water bath for 2 h. At the end of the pepsin digestion, two aliquots of the digest (15 g) were placed in wide-necked 100 ml flasks with dialysis bags containing 18.75 ml of PIPES buffer (Piperazine-N,N′-bis [2-ethane- sulfonic acid] disodium salt). Next, samples were incubated in a shaking water bath at 37 °C for 50 min.
A pancreatin-bile mixture was then added to each flask, and the incubation continued for an additional 2 h. The bag contents were transferred to weighed flasks, weighed and analyzed for mineral content by flame atomic absorption spectroscopy. Mineral dialyzability was calculated from dialyzable mineral %ð Þ ¼½D=ðWAÞ 100, where D is the amount of dialyzed mineral (μg), W is the weight of the pepsin digestion mixture (g), and A is the concentration of each mineral in the pepsin digestion mixture (μg/g).
Polyphenol and Phytosterol Contents and Antioxidant Activity The content of polyphenols was determined according to the method proposed by Kim et al. [20] with methanol/water (70/30) extraction. The results were expressed as mg of gallic acid equivalents (GAE)/100 g dw.
The phytosterols were extracted by adding 10 ml of 3 g/
100 ml KOH to 0.3 g of sample followed by heating in a water bath at 50 °C for 3 h. After cooling, hexane was used to extract phytosterols (four times) and recovered fractions were dried under a N2 flow. An aliquot of 1 ml of dihydrocholesterol (used as internal standard) was added to dried samples [21]. The amount of extracted phytosterols was quantified by capillary GC on an HP 6890 (Hewlett- Packard, Palo Alto, CA) equipped with a flame ionization detector and an HP-5MS capillary column (30 m, 0.25 mm i.d., 0.25 μm). Analysis conditions were modified accord- ing to Schmarr et al. [22], splitless injection was performed at 250 °C, and column temperature was programmed from 150 °C (0.1 min hold) to 300 °C (10 min hold) at 100 °C/min.
Helium was used as the carrier gas at a constant inlet pressure of 140 kPa. The phytosterols were identified and quantified by comparison with a standard mix (recovery of 78%). Results were expressed as mg of phytosterols/100 g dw.
The antioxidant activity was measured by two methods and the dehydrated samples were extracted with 70%
methanol in water (v,v). The ferric reducing antioxidant power (FRAP) method was used [23] and the content was expressed asμmol of Trolox equivalent/100 g dw. Oxygen radical absorbance capacity (ORAC) method was per- formed according to Dávalos et al. [24], adapted to individual cubets. Fluorescein (40 nM) (Sigma Chemical
Co. St. Louis, Mo) was used as a target of free radical damage and AAPH (53 mM) as a peroxyl radical generator, with Trolox as a control standard. The fluorescence measurements were made using an espectrophotometer (Hitachi F-3010, Tokio, Japan) with an excitation wave- length of 485 nm and an emission wavelength of 520 nm.
The antioxidant activity was expressed asμmol of Trolox equivalent/100 g of dw.
High-Resolution Scanning Electron MicroscopyThe sam- ples were fixed in stubs with double-faced tape and coated with a 10-nm thick layer of platinum in a Bal-tec MED-020 Coating System. Samples were examined on a high-resolution scanning electron microscope by FEI Quanta 600 FEG (FEI, Eindhoven, Netherlands). The images were obtained from secondary electrons operating at 10, 5 and 2 kV.
Results and Discussion
The UBF produced presented a light colored and smooth surface as seen in Fig.1.
The carbohydrate profile of UBF is shown in Table1. It presented a small amount of soluble sugars (1.81 g/100 g) which is in accordance with the maturity stage of the fruit [25]. The amount of fructans was negligible. Most of the total starch was RS; the available starch (AS) represented only 28 g/100 g. The low content of soluble sugars in UBF is in accordance with foods that produce low increase in the post prandial glycemic response and return of the glycemia to the fast level after 120 min [26]. Foods classified as having a low glycemic index (GI) generally present a low concentration of soluble sugars and a high concentration of unavailable carbohydrates [27,28]. For example, oat bran (dw), which contains 1 g/100 g total soluble sugars and 46 g/100 g AS, produces a glycemic index of 28% and a glycemic load of 1.2, which are both considered low [29]. At the same time, the UBF energy value (597 kJ/100 g dw) was very low if compared to oat bran (1,443 kJ/100 g dw) [29].
In relation to the RS content, the process used for flour production resulted in a product with a high RS content
(48.99 g/100 g). The TS, AS and RS contents were similar to those found by Ovando-Martinez et al. [30] and the RS content was more than two times that observed by Juarez- Garcia [5].
Remarkably, this flour is a very good source of RS. RS can be used as a source of DF, once it presents physiological effects that are similar to those produced by DF [31]. The studied flour represents a concentrated form of total DF (56.24 g/100 g of DF, RS and fructans) when compared to oat bran (19.9 g/100 g of DF and fructans) [29], which is considered rich in dietary fiber. Menezes et al. [28] observed that the flour obtained from the cooked pulp of unripe bananas (Musa acuminata, var. Nanicão), the same cultivar of the present study but using heating during its production, presents high in vitrofermentability due to the high content of unavailable carbohydrates (RS and/or DF). RS has received much attention during the last two decades for its potential health benefits (similar to soluble DF), once it positively influences the functioning of the digestive tract, microbiota, blood cholesterol level, glycemic index and assists in the control of diabetes [31].
Therefore, the high content of total DF (DF, RS and fructans) and low content of available carbohydrates of UBF highlight the potential of this ingredient to promote intestinal health; however, its physiological effects and profile of fermentation need to be evaluated.
The mineral dializability (D%) and mineral content were evaluated in the flour. The D%Fe (6.3 ±0.9) of UBF presented a lower value than wheat flour (9.8). This result may be due to the presence of phenolic compounds in UBF, which inhibits iron dializability. The D%Ca (24.6±1.6) was lower in UBF than in wheat flour (44.1), although the D%
Zn (28.1±1.7) of UBF was higher than wheat flour (10.1).
On the other hand, when compared to other similar grains like amaranth, banana flour has better mineral availability [32]. The contents (mg/100 g dw) of Zn (0.22±0.02), Ca (16.26 ±0.52) and Fe (0.19±0.02) were low in UBF. The concentrations of zinc obtained in this work are in the same range as those described by other authors, but the contents of Ca and Fe were very different from those described for bananas in other parts of the world [9].
Fig. 1 Unripe banana slices (Musa acuminata, subgroup Cavendish) dried at 55 °C and the resulting flour
The content of total polyphenols in UBF was 50.65±
0.80 mg GAE/100 g dw. This value was lower than the mixture of fruits (oranges, bananas, apples, pears, others) of Spanish diet (350 mg GAE/100 g dw) [7] and apple with peel (590 mg GAE/100 g dw) [20]. The antioxidant activity of UBF, by FRAP method, was 358.67±0.01 μmols of Trolox equivalent/100 g dw and by ORAC method was 261.00±8.80 μmols of Trolox equivalent/100 g dw. A similar result, with ORAC method, was observed in bananas, but five times higher in plums and five times lower in apples [33]. Adding unripe banana flour to make pasta increase the antioxidant activity due to the high content of polyphenol compounds in the indigestible fraction of banana [30]. The content of different kinds of phenolic compounds in UBF must be investigated.
The major phytosterols (mg/100 g dw) quantified in the samples were stigmasterol (2.5±0.1), campesterol (4.1±
0.1) and β-sitosterol (6.2±0.1); the total amount of these
three phytosterols was 12.8. The phytosterol proportions (stigmasterol:campesterol:β-sitosterol) were 1.0:1.6:2.4.
Cavendish phytosterols represented 8–13 g/100 g dw of the extracted lipophilic components. The proportions of stigmasterol (6.5 mg/100 g), campesterol (7.6 mg/100 g) and β-sitosterol (32.5 mg/100 g) were 1.0:1.2:5.0, respec- tively [8]. Even if the results obtained demonstrate a proportion of stigmasterol:campesterol:β-sitosterol close to that observed previously by Oliveira et al. [8], the total amount of phytosterols found in the UBF was lower than those previously reported inMusa acuminata Colla varpulp extract, (almost 47 mg/100 g dw). The higher amount of phytosterols observed [8] could be due to two factors:
differences in the composition of the two banana cultivars and the sample preparation, and sterol extraction methods, specifically the use of alkaline hydrolysis for phytosterol extraction. Indeed, Oliveira et al. [8] quantified phytosterols before and after alkaline hydrolysis of the samples; it was observed that, after alkaline hydrolysis, the relative propor- tion of phytosterols increased and other phytosterols such as cycloeucalenol, cycloartenol, and 24-methylenecycloartanol could be quantified. However, even if UBF is a source of phytosterols, the banana cultivar as well as the method of phytosterol extraction must be considered when quantifying the amount of phystosterols present.
The scanning electron microscopy of UBF is shown in Fig. 2a and b. Figure 2a shows that UBF is mostly composed of starch and cell wall. In fact, the material that appears on the surface of the granules is most likely to be amyloplast membranes, which enclose starch granules in the banana fruit cell. The starch granules are intact, without fractures, indicating that the process used to obtain UBF was not drastic. However, it has not been established yet which structural property of the banana starch granule is responsible for its resistance to enzymatic attack [34].
Figure 2b presents granules with depressions, indicating that although the fruits were in a mature-green stage, degradation of the granule starch had already been initiated by hydrolytic enzymes.
Table 1 Chemical composition and carbohydrate profile of unripe banana flour
Compound Content (g/100 g dw)
Proteina 3.60±0.19
Asha 3.14±0.02
Lipidsa 0.89±0.04
Total soluble sugars 1.81
Glucosea 0.37±0.02
Fructosea 0.48±0.01
Sucrosea 0.96±0.08
Total starcha 76.77±0.54
Resistant starch (RS)a 48.99±0.40
Available starch 27.78
Total dietary fiber (RS + fructans + DF) 56.24
Fructansa 0.05±0.03
Dietary fiber (DF) (without RS and fructans)a 7.2±0.17 Moisture = 6.9±0.09 (g/100 g wet weight)
aMean ± SD of triplicates
50 µm
a b
Fig. 2 Scanning electron micros- copy of unripe banana flour
The microbial analysis of UBF was also conducted and samples presented good microbiological quality (data not shown), according to ANVISA [35]. Ingestion of this product would constitute no microbiological health hazard since the samples were properly stored.
Conclusions
The process used for preparing UBF obtained from peeled unripe banana (Musa acuminata, var. Nanicão) generated a product with a high amount of total DF, and a particularly significant concentration of RS. At the same time, UBF exhibited undamaged starch granules and low energy value.
Mineral, phytosterols, available carbohydrate and total polyphenol contents were low in UBF, but with moderated antioxidant activity. In conclusion, the carbohydrate profile of UBF indicates that it has characteristics of a potential functional ingredient.
Acknowledgements The authors acknowledge the 106PI0297 CYTED/CNPq project for international cooperation that allowed the scientific interchange between different Ibero-American laboratories as well as CNPq for the scholarships granted to authors Tatiana Beatris Tribess and Milana C. T. Dan.
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