Antioxidant Potential and Physicochemical Characterization of Yellow, Purple and Orange Passion Fruit

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J Food Sci Technol

https://doi.org/10.1007/s13197-018-3190-2

ORIGINAL ARTICLE

Antioxidant potential and physicochemical characterization


of yellow, purple and orange passion fruit
Luzia Caroline Ramos dos Reis1 • Elizete Maria Pesamosca Facco2 •
Mirian Salvador3 • Simone Hickmann Flôres1 • Alessandro de Oliveira Rios1

Revised: 13 October 2017 / Accepted: 23 April 2018


Ó Association of Food Scientists & Technologists (India) 2018

Abstract This study evaluated yellow, purple and orange pulps and phenolics in general. This research revealed that
passion fruit in pulp, peel, and seed for physicochemical the pulp of passion fruit and his residues have a significant
characteristics, proximate composition, minerals, antioxi- content of bioactive compounds, differing in type accord-
dant capacity (DPPH and ABTS), phenolic compounds, ing the species analyzed.
carotenoids, flavonoids and anthocyanins. Yellow passion
fruit presented higher concentrations of pectin (37.37 g/ Keywords Pectin  Total dietary fiber  Lycopene 
100 g) in peels; high cryptoxanthin, a-carotene, b-car- Quercetin  Anthocyanin
otene, provitamin A, quercetin, and kaempferol in pulps
and higher values of ash and total dietary fiber in seeds.
The purple fruit was highlighted by a great value of Introduction
anthocyanins (103.68 mg/100 g) in peels and seeds and the
orange fruit reported higher levels of ash, carotenoids Passion fruit is a popular name given to several species of
(mainly b-carotene with 21,274 lg/100 g), kaempferol in the genus Passiflora that belongs to Passifloraceae family,
peels, higher contents of total soluble solids, lycopene which there are more than 500 species distributed in
(4405 lg/100 g), lutein, zeaxanthin, total carotenoids in regions of tropical and subtropical climate of the world.
The variety Passiflora edulis Sims fo. flavicarpa, known as
sour or passion fruit, is the most produced and marketed,
and represents 95% of its fruit farm. Its cultivation is pri-
marily focusing on the juice and pulp industry, especially
Electronic supplementary material The online version of this due to its higher acidity and pulp yield. However, the
article (https://doi.org/10.1007/s13197-018-3190-2) contains supple-
mentary material, which is available to authorized users. species Passiflora edulis Sims fo. edulis and Passiflora
caerulea, known as purple and orange passion fruit,
& Alessandro de Oliveira Rios respectively, have the sweetest flavor, so are best con-
alessandro.rios@ufrgs.br sumed as juice or as fresh pulp (Zeraik and Yariwake
1
Instituto de Ciência e Tecnologia de Alimentos, Universidade
2010). These fruits are of interest not only due to the pulps
Federal do Rio Grande do Sul (UFRGS), Av. Bento but also due to its peels and seeds which contain high levels
Gonçalves, 9500, Prédio 43.212, Campus do Vale, of bioactive compounds. Furthermore, regarding species
Porto Alegre, RS CEP 91501-970, Brazil Passiflora caerulea, no research has been reported about
2
Departamento de Bromatologia, Centro de Ciências da saúde, bioactive compounds content.
Universidade de Caxias do Sul (UCS), Rua Francisco Getúlio The ideal condition for the development of passion fruit
Vargas, 1130, Bloco S, Cidade Universitária, Petropólis,
occurs in places where the tropical climate prevails, and it
Caxias do Sul, RS CEP 95070560, Brazil
3
is emphasizing that the water content in the soil is one of
Laboratório de Estresse Oxidativo e Antioxidantes,
the factors that most influences the flowering of passion
Universidade de Caxias do Sul – Instituto de Biotecnologia,
Rua Francisco Getúlio Vargas, 1130, Caxias do Sul, fruit crop. The regions that this fruit is widely using are
RS CEP 95070-560, Brazil American and European countries, due to the favorable

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weather. The best variety known and more used is Passi- (albedo and flavedo) and seed, the parts were packed in
flora edulis, not only because of its pulp but also due of the plastic bags and stored in a freezer at - 18 °C until
infusions made with the leaves (Silva et al. 2013). analysis.
The common consumption of fruit and vegetable in the
diet can protect our organism of Manu chronic diseases Physicochemical and chemical analysis
such as cancer, neurological diseases, cardiovascular dis-
eases, obesity, inflammations and infections (Volp et al. Total soluble solids (TSS) were determined in pulps with a
2009). However, passion fruit appears to be an excellent Brix refractometer. The pH was measured using a pH meter
source of nutrients as carbohydrates, vitamins, and miner- (Quimis, model Q-400A). The yield was calculated by the
als that are essential nutrients for life. The fruit has a high percentage ratio (%) of the weight of the fruit with and
content in nutraceuticals, as phenolic acids, where antho- without seed. The titratable acidity was determined by
cyanins and flavonoids are the majoritarian compounds of titration method using standardized 0.1 M NaOH solution,
this group; carotenoids and b-carotene appear to be the and the results analyzing in g/100 g of citric acid following
principal component, with consequently increased provi- the Analytical Standards Instituto Adolfo Lutz (2008). All
tamin A activity. These nutraceutical compounds have of these analyses were made in triplicate.
biological activities in the health, protective effect against
degenerative and chronic diseases and act as mutagenesis Yield
and carcinogenesis inhibitors. Also, these compounds have
been associated with antiviral, antiallergic, antiplatelet and The yield calculation of the pulp was calculated by weight
anti-inflammatory activities (Morais et al. 2016; Casta- of whole fruit (one by one) and weight of the fruit without
ñeda-Ovando et al. 2009; Tanwar and Modgil 2012; Gon- peel and seed (pulp). The result was expressed as per-
zález-Gallego et al. 2014). centage (%). The average number of passion fruit analyzed
A major problem of passion fruit juice in the manu- was around 30 units.
facturing industry is the amounts of waste generated come
from discarded that are the peels and seeds. These residues Color parameters
are excellent sources of nutrients, bioactive compounds and
studies about your potential can even indicate a future The color was analyzed using a portable colorimeter
application as food ingredients in the formulation of new (Konica Minolta Model CR 400, Singapore) by the Com-
products, encouraging the reutilization of food and offering mission Internationale de l’Eclairage (CIELAB system) by
a nutritious alternative diet at low cost. determining the values of L* (lightness), a* (component
Based on this, the aim of this study was to evaluate the red-green) and b* (yellow-blue component). All of these
physicochemical characteristics, color parameters, pectin, analyses were made in triplicate.
proximate composition, minerals, the content of bioactive
compounds and antioxidant capacity in pulp, peel, and the
seed of yellow, purple and orange passion fruit to future Proximate composition
use of parts as functional ingredients.
All analyses were performed according to AOAC (2000).
Protein content was determined by the Kjeldahl method
Materials and methods with a conversion factor of 5.75. Lipids were obtained by
cold extraction and ash was determined in a muffle furnace
Sample preparation at 550 °C. Total dietary fiber was determined by the
enzymatic–gravimetric method, moisture by gravimetry.
The yellow passion fruit (Passiflora edulis Sims fo. flavi- Carbohydrates were estimated by the difference of 100 per
carpa) samples were obtained CEASA (Central Supply of cent of the sum between proteins, lipids, water and ash.
Rio Grande do Sul), Caxias do Sul, RS, Brazil. The purple The results were expressed as % and the data presented is
(Passiflora edulis Sims fo. edulis) and orange passion fruit the average of triplicate analysis.
(Passiflora caerulea) samples were collected from farmers
in the Criuva District (Caxias do Sul), the Rio Grande do Determination of pectin
Sul, Brazil. The fruits were harvested when fully ripe, with
their skin color (yellow, purple or orange). After the crop, The pectin of peels was extracted using a method of
the fruits were transported immediately to the laboratory Canteri-Schemin et al. (2005) and Seixas et al. (2014) with
where they were cleaned in running water. Then the fruits some modifications. The extraction process was carried out
were cut in half and made a separation of the pulp, peel in beakers (600 mL), followed by heating in a microwave

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oven (Electrolux, ME21S 800 W). Each 2 g of passion The column used was a C30 polymeric reverse phase
fruit peel flour was added to 50 mL of distilled water in a (250 9 4.6 mm ID, 3 lm, YMC, model CT99SO3-
beaker. Then, an addition of a tartaric acidic solution 2546WT). The mobile phase gradient (wa-
(10%), was added to maintain a final pH of 2 for the ter:methanol:MTBE) (JT Baker, CAS Number 04.04.1634,
solutions. The beaker was put in a microwave heating for 99.96% purity) commenced at 5:90:5, reaching 0:95:5 at
3 min. The solution (still warm), was vacuum filtered on a 12 min, 0:89:11 at 25 min, 0:75:25 at 40 min, and finally
filter paper and the filtrate (containing the soluble pectin) 00:50:50 at 60 min. The temperature of column was 33 °C
was cooled to 4 °C. and a flow rate of 1 mL/min (Spectra were obtained at a
To isolate the soluble pectin from the filtrate, the solu- fixed wavelength of 450 nm for carotenoids).
tion was slowly added under magnetic stirring to two Compounds were identified by comparing the sample
volumes of absolute ethyl alcohol. This mixture was stirred retention time’s with the retention times obtained for
for 10 min, after which it was allowed to rest for 30 min to controls. For quantification, a standard curve was con-
facilitate the flotation of the pectin. The pectin was sepa- structed for carotenoids over the following ranges: lutein
rated by vacuum filtration on a filter paper. The extracted 1–65 lg/mL ([ 95%, Sigma-Aldrich); zeaxanthin
pectin in a gel form was immersed in absolute ethyl alcohol 1–40 lg/mL ([ 95%, Sigma-Aldrich); cryptoxanthin
for about 12 h and then was partially dehydrated by 4–100 lg/mL ([ 97%, Sigma-Aldrich); a-carotene
immersion in acetone. The drying pectin was put in an air- 2–25 lg/mL ([ 95%, Sigma-Aldrich); b-carotene
circulated oven at 50 °C until constant weight (approxi- 5–50 lg/mL ([ 97%, Sigma-Aldrich) and lycopene
mately 8 h). The results were expressed as g of pectin/ (C 85% Sigma-Aldrich).
100 g dry peels (triplicate). The limits of detection (LOD) and quantification (LOQ)
were calculated by injecting 10 times the blank of the
Determination of minerals sample at very low level were used for measurement of
LOD and LOQ which were determined as follows:
All the samples (pulp, peel, and seed) of yellow, purple and LOD = mean value ? 3 standard deviation (SD) LOQ =
orange passion fruit were lyophilized (Liotop, L101, Bra- mean value ? 10 SD where, mean value is zero (Ertas
zil) before mineral analysis. The analysis of minerals in the et al. 2007). Lutein: 6.9 9 10-3 and 1.15 9 10-2 lg/g;
passion fruit samples were made in Plant Soil Laboratory zeaxanthin: 9.56 9 10-2 and 1.59 9 10-2 lg/g; cryptox-
Faculty of Agronomy, Federal University of Rio Grande do anthin: 2.11 9 10-2 and 3.51 9 10-2 lg/g; a-carotene:
Sul (UFRGS), according to the methodology of atomic 1.97 9 10-2 and 3.28 9 10-2 lg/g; b-carotene:
emission spectrometry with inductively coupled plasma 6.53 9 10 and 10.89 9 10-2 lg/g and lycopene were
-2

source (ICP–OES) described by Tedesco and Gianello 7 9 10-3 and 33 9 10-3 lg/g.
(2004) This method is compiling in Table 1S (supple- Provitamin A activity was calculated by the biocon-
mentary material). The results were expressed as % and the version factor following Institute of Medicine (2001),
data presented is the average of duplicate analysis. yielding a value of 12 mg of b-carotene with 1 mg of
Retinol Activity Equivalent (RAE). The results were
Determination of carotenoid profile and provitamin expressed as % and the data presented is the average of
A content triplicate analysis.

The profile of carotenoids was determined according to Determination of phenolic compounds


Mercadante and Rodriguez-Amaya (1998). The extraction
of pigments was with acetone and the saponification in a Samples (5 g) were homogenized by exhaustive extraction
KOH solution (10% in methanol) overnight. The extract with 20 mL of ethanol and centrifuged at 15 °C (Cientec,
was rotary evaporated (Fisatom, Model 801) (T \ 25 °C) CTR—5000R, Brazil) at 5000 9 g for 20 min. Then,
and stored in a freezer (- 18 °C) for quantification by 20 lL of supernatant was added to 1.58 mL of water and
high-performance liquid chromatography (HPLC). 100 lL of Folin-Ciocalteu (0.4 mol/L). After reaction
For HPLC (High Performance Liquid Chromatography) (3 min), 300 lL of Na2CO3 was added, and the mixture
analysis, the samples stored in a freezer were diluted with kept at room temperature for 2 h. The absorbance was then
methyl tert-butyl ether (MTBE-JT Baker, CAS. Number read at 765 nm on a UV–visible spectrophotometer (Shi-
1634-04-4, purity 99.96%), sonicated (Unique, Model USC madzu, UV-1700 PharmaSpec, Japan). The ethanol was
1400) for 1 min and filtered (Millex LCR 0.45 lm, used as the blank and gallic acid was used for calibration of
13 mm) for injection into the HPLC (Agilent 1100 Series, the standard curve (0–0.50 mg/L). The results were
Santa Clara, CA, USA), a UV–visible detector and with a expressed as mg of gallic acid equivalent (GAE) per 100 g
quaternary system. of dry sample (triplicates) (Swain and Hillis 1959).

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Determination of quercetin and kaempferol (CAS 528-53-0, [ 95%), aglycone cyaniding (CAS
528-58-5, C 95%), malvidin-3,5-diglucoside (CAS
Quercetin and kaempferol contents were analyzed accord- 643-84-5, C 95%) and aglycone pelargonidin (CAS
ing to Zeraik and Yariwake (2010) with modifications. The 17334-58-6, C 90%). The quantification and identification
sample (10 g) were homogenised in an Ultra-Turrax (T25, of compounds were performed by comparing peak areas
IKA, China) with 30 mL of methanol at room temperature. and retention times with their respective standards under
The extracts were centrifuged at 15,000 9 g, 4 °C for the same chromatographic conditions. The results were
20 min and after in rotary evaporator giving 2 mL of expressed as % and the data presented is the average of
extract. The resulting aqueous solution was filtered through triplicate analysis.
a 0.45 lm Millex-HV PVDF membrane (Millipore, New
Bedford, MA, USA) before HPLC analysis. The samples Determination of antioxidant capacity
were prepared and analyzed in triplicate and the results
were expressed as %. The methodology used to determine antioxidant capacity
The HPLC-/DAD analyses were carried out on a Waters was based on the sequestration of DPPH (2,2-diphenyl-1-
Alliance 2695 (Milford, MA, USA) liquid chromatograph picryl-hydrazyl) and ABTS (2,20 -azino-bis(3-ethylben-
connected to a model 2996 (DAD) diode array detector and zothiazoline-6-sulphonic acid) radicals according to Brand-
controlled by Waters Empower software. The separation Williams et al. (1995). Samples (5 g) were placed in
was performed using a C18 polymer column (250 mm 9 20 mL of ethanol and then centrifuged at 15 °C at
4.6 mm id, 5 lm Vydac, 218TP). The samples were 5000 9 g (Cientec, CTR—5000R, Brazil) for 20 min. The
injected automatically (10.0 lL). A flow rate of 0.8 mL/ liquid was diluted in three concentrations (10, 30, and
min was applied, using a linear gradient of 0.2% formic 100%). For the DPPH assay, aliquots of each concentration
acid in water (solvent A) and 0.2% formic acid in ace- were treated with 2 mL of DPPH (0.06 mM). The absor-
tonitrile (solvent B). The gradients were: 0–10 min, 15% B bance was read at 517 nm (Shimadzu, UV-1700 Phar-
in 85% A and 10–30 min, 20% B in 80% A. The chro- maSpec, Japan). The results were presented as IC
matogram was monitored at 330 nm, and UV spectra of (Effective Concentration of 50% radical inhibition) 50
individual peaks were recorded in the range of (mg/100 mL).
200–400 nm. For the ABTS assay, aliquots of each concentration were
The contents of quercetin and kaempferol were deter- treated with 2 mL of ABTS (7 mM). The absorbance was
mined by comparison with an external standard, injecting a read at 734 nm (Shimadzu, UV-1700 PharmaSpec, Japan).
new standard daily at 30 mg/mL for Quercetin ([ 98%, The results were presented as IC 50 (mg/100 mL).
Sigma-Aldrich) and 4 mg/mL for kaempferol ([ 99%,
Sigma-Aldrich). Statistical analysis

Determination of anthocyanins Data were analyzed by ANOVA and Tukey’s mean com-
parison test with a significance level of 5%, followed by a
The anthocyanins were analyzed according to Zanatta et al. principal component analysis (PCA) using the software
(2005), so 5 g of sample were homogenized in an Ultra- Statistica 12.0 (Statsoft Inc, São Paulo, Brasil). Pearson’s
Turrax (T25, IKA, China) with acidified methanol (HCl correlation was to the results of phenolic compounds and
1%) and then quantified by HPLC (Agilent 1100 Series, antioxidant capacity using Statistica 12.0 (Statsoft, São
Santa Clara, CA, USA) equipped with a quaternary pump Paulo, Brazil).
system solvent and a UV–visible detector was used with a
C18Shim-PakCLC-ODScolumn(5 lm, 250 9 4.6 mm).
The mobile phase was 5% aqueous formic acid/metha- Results and discussion
nol 85:15 (v/v) to 20:80 over 25 min and this isocratic ratio
was maintained for 15 min. The mobile phase flow were Physicochemical analysis
0.8 mL/min, the injection volume was 5 lL, and 29 °C
was the temperature of column. The chromatograms were The results of the physicochemical analysis in pulps of
processed at a fixed wavelength of 520 nm. different species of passion fruit were: 9.10% of TSS (total
The standards were from Sigma-Aldrich (USA): cyani- soluble solids), 9.06% of titratable acidity (citric acid) and
din-3-glucoside (CAS 7084-24-4, C 95.0%), cyanidin-3,5- a pH of 2.66 in yellow passion fruit pulp. For purple pas-
glucoside (CAS 2611-67-8, C 90.0%), delphinidin-3-b- sion fruit the results were 11.60% of TSS, 2.83% of
glucoside (CAS 6906-38-3, C 97%), pelargonidin-3-glu- titratable acidity and a pH of 2.72 and for orange passion
coside (CAS 17334-58-6, C 90%), aglycone delphinidin fruit pulp, we found 12.30% of TSS, 2.21% of

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titratable acidity and a pH of 3.97. So, the pulp of orange Table 1 Yield color parameters and pectin in different species of
passion fruit is sweeter because it showed the higher con- passion fruit (mean and standard deviation)
tent of total soluble solids (TSS), pH and consequently, Yellow Purple Orange
lower content of acidity. The pulp of yellow passion fruit
Yield (%)
showed higher acidity and lower pH and TSS and then it is
more acid. Some factors such as soil type, fertilization, Pulp 27.71 ± 1.00a 25.23 ± 1.02c 26.54 ± 0.98b
a b
climate, irrigation and genetic traits of the cultivar can Peel 64.05 ± 2.03 62.11 ± 1.90 57.28 ± 2.05c
c b
explain the variations between the physicochemical Seed 8.24 ± 0.05 12.66 ± 0.12 16.18 ± 0.08a
parameters. Color L*
Kishore et al. (2011) evaluated the physicochemical Pulp 58.05 ± 0.64b 77.65 ± 0.57a 26.90 ± 0.17c
attributes as TSS and titrable acidity in purple passion fruit Peel 43.16 ± 1.47a 21.58 ± 2.15c 36.94 ± 0.45b
pulp (Passiflora edulis Sims) who the values were 15.30 Seed 33.86 ± 0.80a 28.16 ± 0.78b 26.96 ± 0.49b
and 3.80%, respectively. These results were higher when Color a*
compared to purple passion fruit pulp of this research. In Pulp 8.44 ± 0.01b 0.29 ± 0.08c 10.78 ± 0.11a
b b
another study realized by Souza et al. (2012), who analysed Peel 2.29 ± 0.25 2.20 ± 0.22 13.23 ± 0.49a
the pH, titratable acidity and total soluble solids in sweet Seed 1.91 ± 0.09b 0.30 ± 0.08c 8.25 ± 0.24a
passion fruit pulp (Passiflora alata Dryand), the results Color b*
were 3.31, 2.00, and 13.33%, respectively. These values Pulp 42.83 ± 1.28a 17.18 ± 1.08b 6.08 ± 0.07c
b c
were more similar to specie Passiflora caeurea analysed by Peel 31.33 ± 0.53 3.83 ± 1.75 35.78 ± 1.64a
a c
us that was the passion fruit sweeter. Janzantti et al. (2012) Seed 19.36 ± 0.45 5.90 ± 0.21 8.89 ± 0.55b
did a research with yellow passion fruit pulp (P. edulis Pectin
Sims f. flavicarpa Deg.) and the higher values were 4.32% Peel 37.67 ± 0.97a 32.85 ± 1.20b 21.55 ± 0.55c
for titratable acidity, 14.71% soluble solids and 3.53 for a,b,c
Different superscript letters in the same row indicate statistically
pH, different values found by us when compared to yellow significant difference (p \ 0.05)
passion fruit. López-Vargas et al. (2013) evaluated the pH
in pulp and seed of yellow passion fruit (Passiflora edulis
var. flavicarpa) and the results were 3.75. They found former retain the greater part of the variance present in the
higher values of pH in relation to the same variety (yellow original variables.
passion fruit) of our research. Pongener et al. (2013) found The three passion fruits were evaluated for the color
the highest total soluble solids of 16.2° Brix in purple parameters, proximate composition, minerals, carotenoids,
passion fruit pulp (Passiflora edulis Sims) and titrat- flavonoids, phenolic compounds, antioxidant capacity and
able acidity of 2.34 g citric acid/100 mL extract. These the results are showed in Fig. 1.
values were different both for total soluble solids and By analyzing the components, the variance of the data
titratable acidity when compared to purple passion fruit was accounted for the significant contributions of 47.29%
pulp analysed in this study. for the first principal component representing variable ash,
The yield of different species of passion fruit was color b and color L and 25.77% for the second principal
evaluated, and the results are shown in Table 1. As components representing other variables (Fig. 1a).
expected, pulp and peel of yellow passion fruit presented
higher yield when compared to purple and orange passion Color
fruit, but for seed, orange passion fruit showed higher
yield. Thus, it appears that the residues that represent most The passion fruit was evaluated within the context of color
of the fruit should be characterized to indicate the possible parameters (Fig. 1a). It was observed that for color L*, the
applications and uses. For example, replacing wheat flour pulp of purple passion fruit showed higher brightness. For
in some formulations such as pasta, breads, cakes, biscuits, color a* that indicates the intensity of colors red-green,
which will have a higher content of fibers and bioactive orange passion fruit showed higher levels for pulp, peel,
compounds. and seed when compared to yellow and purple passion
PCA (Principal Component Analysis) is a statistical fruit. For color b*, which indicates the intensity of colors
technique used to reduce the dimensionality of a data set yellow-blue, both for pulp and seed, yellow passion fruit
containing a large number of inter-related variables. The presented more intensity, and for the peel, orange passion
analysis is performed to maintain the maximum variance fruit showed more intensity when compared to other spe-
present in the data. This reduction produces a new reduced cies of passion fruit. The differences in the color
and uncorrelated set of variables, called principal compo-
nents. These components are then chosen to ensure that the

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b Fig. 1 Principal component analysis of yellow, purple and orange Table 2 Proximate composition of different species of passion fruit
passion fruit in pulp, peel, and seed: proximate composition and color (g/100 g of dry weight—except for moisture) with mean and standard
parameters (a); minerals (b); carotenoids, phenolic compounds and deviation
flavonoids (c). Legend: YPU: yellow passion fruit pulp; YPE: yellow
passion fruit peel; YSE: yellow passion fruit seed; PPU: purple Yellow Purple Orange
passion fruit pulp; PPE: purple passion fruit peel; PSE: purple passion
fruit seed; OPU: orange passion fruit OPE: orange passion fruit peel; Moisture
OSE: orange passion fruit seed; Moist: moisture; Ptn: protein; Lip: Pulp 90.06 ± 0.00a 83.44 ± 0.99b 88.18 ± 0.87a
lipids; Carb: carbohydrates; TF: total fibre; N: nitrogen; P: phospho- Peel 87.14 ± 3.29 b
87.02 ± 1.22 b
94.25 ± 0.26a
rus; K: potassium; Ca: calcium; Mg: magnesium; S: sulphur; Cu:
Seed 57.09 ± 2.36a 45.91 ± 0.97b 58.46 ± 0.38a
copper; Zn: zinc; Fe: iron; Mn: manganese; B: boron; So: sodium;
Lut: lutein; Zea: Zeaxanthin; Cryp: Cryptoxanthin; a-car: a-carotene; Proteins
b-car: b-carotene; Lycop: lycopene; Provit A: provitamin A; TC: total Pulp 8.57 ± 0.10b 6.53 ± 0.23c 9.90 ± 0.35a
carotenoids; PC: phenolic compounds; Quer: quercetin; Kaemp: Peel 3.40 ± 0.06 c
6.47 ± 0.04 b
11.60 ± 0.44a
kaempferol b b
Seed 13.07 ± 0.12 13.23 ± 0.48 15.84 ± 0.15a
Lipids
Pulp 1.11 ± 0.04b 1.09 ± 0.04b 2.92 ± 0.09a
parameters can be explained mainly the species, soil and Peel 4.20 ± 0.03 c
4.89 ± 0.07 b
10.25 ± 0.12a
harvesting period are different. Seed 12.31 ± 0.78 c
14.94 ± 0.41 b
19.64 ± 0.30a
Ash
Proximate composition Pulp 6.94 ± 0.01a 2.95 ± 0.14b 7.31 ± 0.22a
Peel 6.62 ± 0.24c 7.93 ± 0. 05b 13.29 ± 0.41a
By principal component analysis (Fig. 1a) can be seen that Seed 3.56 ± 0.05 a
1.85 ± 0.06 c
3.23 ± 0.18b
the orange passion fruit stands out for its red coloration in Carbohydrates
the peel, high ash content present in the pulp and peel and
Pulp 83.37 ± 0.00b 89.42 ± 0.00a 79.87 ± 0.00c
the high content of proteins and lipids in the seeds. The
Peel 85.78 ± 0.00a 80.71 ± 0.00b 64.86 ± 0.00c
yellow passion fruit, in turn, showed a high content of
Seed 71.07 ± 0.00a 69.98 ± 0.00a 61.38 ± 0.00b
carbohydrates in the peel, probably due to the high content
Total fibre
of pectin (37.37 g/100 g) in this species. The total fiber
Pulp 7.15 ± 0.07a 1.40 ± 0.18c 2.17 ± 0.11b
content in the pulp was greater in this species compared a a
Peel 61.16 ± 1.02 61.68 ± 1.31 62.14 ± 2.62a
with others. The purple passion fruit highlights to have a a b
Seed 65.60 ± 0.52 55.06 ± 0.35 51.47 ± 0.60c
high content of carbohydrates in the pulp compared with
a,b,c
orange and yellow passion fruit (Table 2). Different superscript letters in the same row indicate statistically
Souza et al. (2012) analyzed the proximate composition significant difference (p \ 0.05)
in sweet passion fruit pulp (Passiflora alata Dryand), and
the results were (dry weight, except for moisture): 84.12%
of moisture, 8.50% proteins, 0.63% lipids, 82.17% carbo- of pectin from passion fruit peel. Kulkarni and Vijayanand
hydrates, 4.40% dietary fiber and 4.28% ash. The results of (2010) also conducted a study to evaluate the pectin con-
proteins and carbohydrates were similar with yellow pas- tent of passion fruit peel (Passiflora edulis f. flavicarpa L.)
sion fruit analyzed in this study, but for moisture, lipids, yellow variety. The passion fruit peels were dehydrated for
dietary fiber, and ash we found higher values. pectin extraction experiments. The conditions for the
Thereby, the peels and seeds of yellow, purple and extraction of pectin from the passion fruit peel promoted a
orange passion fruit showed to be richer in total dietary yield of 14.80 g/100 g of the dried peel. In another
fiber, proteins (seeds) and lipids, which should have an research carried out by Seixas et al. (2014), pectin
unsaturated origin. extraction was investigated from the passion fruit peel
(Passiflora edulis f. flavicarpa). The highest yield was
Pectin found to be 18.20%. Different species of passion fruit of
this study showed better results compared to the yield of
As it can be seen in Table 1, the peel of yellow passion pectin compared to all kinds of passion fruit analyzed.
fruit showed higher levels of pectin when compared to the
purple and orange passion fruit (the latter presented the Minerals
lowest content).
Liew et al. (2014) evaluated the production of pectin The minerals content of passion fruit is shown in Fig. 1B.
yellow passion fruit peel (Passiflora edulis f. flavicarpa) in By analyzing the components, the variance of the data was
extraction with citric acid. The authors found 14.60% yield accounted for the significant contributions of 42.66% for

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the first and 24.95% for the second principal components. Table 3 Mineral composition of different species of passion fruit
It can be observed that pulps of three species have high (mg/100 g of dry weight) with mean and standard deviation
calcium, potassium, and boron. The yellow and orange Yellow Purple Orange
passion fruit peels showed high zinc, manganese, copper,
Zinc
phosphorus, and sulfur. As for the purple passion fruit peel,
Pulp 5.20 ± 0.10b 2.10 ± 0.05c 6.50 ± 0.12a
these minerals had low content. Regarding seeds, orange b c
Peel 1.00 ± 0.02 0.90 ± 0.01 5.80 ± 0.05a
passion fruit presented a considerable amount of copper c b
Seed 4.10 ± 0.09 4.60 ± 0.05 8.90 ± 0.04a
followed by yellow passion fruit (Table 3). Iron
Gondim et al. (2005) determined the mineral concen- Pulp 5.50 ± 0.03a 2.90 ± 0.02c 3.20 ± 0.01b
tration in yellow passion fruit peels (Passiflora edulis). Peel 3.20 ± 0.04 c
4.60 ± 0.03 a
3.90 ± 0.02b
They found 44.51 mg of calcium, 0.89 mg of iron, Seed 5.20 ± 0.02 a
4.30 ± 0.03 c
4.50 ± 0.03b
43.77 mg sodium, 27.82 magnesium, 0.32 mg zinc, Boron
0.04 mg copper and 178.40 mg potassium in 100 g of fresh Pulp 0.70 ± 0.02a 0.20 ± 0.01b 0.70 ± 0.02a
sample. These values were lower (except for sodium) when Peel 1.30 ± 0.03 c
1.40 ± 0.03 b
1.60 ± 0.04a
b a
compared to the yellow passion fruit peel analyzed in this Seed 0.40 ± 0.01 0.50 ± 0.02 0.50 ± 0.02a
research due to they did not present the values in dry basis. Manganese
Souza et al. (2012) evaluated the mineral content Pulp 1.20 ± 0.05a 0.40 ± 0.01b 1.20 ± 0.01a
(phosphorus, potassium, calcium, magnesium and iron) in Peel 0.50 ± 0.0c 0.70 ± 0.02b 7.30 ± 0.02a
passion fruit pulp (Passiflora alata Dryand). The authors Seed 2.20 ± 0.05c 2.30 ± 0.03b 8.90 ± 0.01a

found values of 34.95 mg for phosphorus, 375.42 mg Copper


Pulp 0.60 ± 0.02b 0.20 ± 0.01c 1.00 ± 0.02a
potassium, 4.76 mg calcium, 19.82 mg magnesium and c b
Peel 0.10 ± 0.01 0.20 ± 0.01 0.30 ± 0.01a
1.06 mg of iron in 100 g of fresh pulp. They found signi- b c
Seed 0.90 ± 0.02 0.70 ± 0.02 1.30 ± 0.03a
ficative amounts of calcium and potassium in pulp com-
Phosphorus
pared to our pulps studied.
Pulp 380 ± 1.98b 150 ± 1.70c 390 ± 2.76a
As example, in adults above 19 years old, a portion of Peel 140 ± 1.30 b
70.00 ± 1.12 c
240 ± 1.71a
100 g of orange passion fruit pulp presents 81 and 59% of Seed 310 ± 2.05 b
63.00 ± 1.19 c
390 ± 2.90a
recommended daily intake of zinc in women and men, Sulfur
respectively; 70 and 55% for magnesium in women and Pulp 170 ± 2.00b 90.00 ± 0.85c 330 ± 3.92a
men; 111% for copper; 55% for phosphorus and 33% for Peel 70.00 ± 0.40 c
160 ± 1.35 b
280 ± 2.80a
calcium. In orange passion fruit peel (100 g), potassium Seed 150 ± 1.23 b
32 ± 0.10 c
230 ± 2.09a
presents 85% of recommended daily intake and manganese Sodium
405 and 317% in women and men. The pulp of yellow Pulp 1.40 ± 0.02c 5.30 ± 0.04b 9.40 ± 0.20a
passion fruit (100 g) gives 30 and 69% of iron recom- Peel 2.20 ± 0.02c 7.30 ± 0.12b 11.50 ± 0.15a
mended daily intake for women and men; the concentra- Seed 3.46 ± 0.07c 4.80 ± 0.03a 4.40 ± 0.05b
tions of boron and sodium of all parts in passion fruit Magnesium
(portion of 100 g) is according to tolerable upper intake Pulp 200 ± 1.23b 120 ± 0.95c 220 ± 1.30a
c b
Peel 120 ± 0.90 130 ± 0.97 140 ± 1.34a
levels from 1 year old; sulphur and nitrogen not appears in c a
Seed 150 ± 1.10 290 ± 1.80 200 ± 1.22b
recommended daily intake and tolerable upper intake
Nitrogen
levels.
Pulp 2400 ± 20.0a 1100 ± 8.0c 1700 ± 12.0b
Thus, it can be seen that from the nutritional matrix, we c b
Peel 620 ± 9.00 920 ± 7.50 940 ± 7.00a
can ingest the recommended daily amount of minerals b c
Seed 1800 ± 15.0 380 ± 1.50 2200 ± 18.5a
through the passion fruit, noting that the pulps have higher Potassium
concentrations of minerals than peels. Pulp 3800 ± 25.5a 1600 ± 16.0c 2900 ± 18.5b
c b
Peel 2600 ± 15.7 2800 ± 16.3 4000 ± 32.0a
Carotenoid profile and provitamin A content Seed 760 ± 6.40 b
112 ± 3.00 c
1000 ± 7.80a
Calcium
The content of carotenoids and provitamin A are shown in Pulp 50.00 ± 0.40a 20.00 ± 0.12c 30.00 ± 0.10b
Fig. 1c. By analyzing the components, the variance of the Peel 250 ± 1.98b 310 ± 1.69a 30.00 ± 0.11c
data was accounted for the significant contributions of Seed 30.00 ± 0.35b 6.00 ± 0.02c 330 ± 1.18a
62.80% for the first and 16.14% for the second principal a,b,c
Different superscript letters in the same row indicate statistically
components. For peel, orange passion fruit stands out to all significant difference (p \ 0.05)
carotenoids evaluated and provitamin A about other spe-
cies of passion fruit, where the majoritarian carotenoid was

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b-carotene because his peel color is orange. This species results were higher when compared to all varieties ana-
also presented in the pulp the highest content of lycopene lyzed in this study.
(Table 4). As an example (Institute of Medicine 2002), pulp of
Souza et al. (2012) analyzed the content of b-carotene yellow passion fruit (100 g) presents 15 and 11% of DRI
and lycopene in sweet passion fruit pulp (Passiflora alata (dietary reference intakes) of vitamin A in women and men
Dryand), and they found 8249 and 5478 lg/100 g dry ([ 14 years old), respectively. A portion of 100 g of
weight, confirming that these results were higher than our orange passion fruit peel could contribute with 233 and
study for both b-carotene and lycopene. Pongener et al. 181% for women and men ([ 14 years old), respectively
(2013) evaluated the total carotenoids in purple passion according to recommended a daily intake of vitamin A.
fruit, and the higher value was 1467 lg/100 mL, being
higher when compared to purple passion fruit analyzed in Phenolic compounds
this research, but lower values compared to yellow and
orange pulps. The presence of phenolic compounds in passion fruit
Silva et al. (2014) evaluated the content of b-carotene makes this fruit an excellent candidate to evaluate several
and lycopene in pulp and peel of yellow passion fruit effects in vivo. As can be seen in Fig. 1c, the pulps and
(Passiflora edulis Sims). They found 1362.07 and 57.93 lg peels revealed the higher content of phenolic compounds,
b-carotene/100 g (dry basis), respectively and lycopene where the orange passion fruit stands out due to the higher
was not detected both in pulp and peel. The values of b- concentrations. Therefore, the peels are residues that can be
carotene were similar to our research for pulp (1333.97 lg/ used and applied in formulations that would enrich the food
100 g dry basis), but for the peel, we detected more content due to the presence of these compounds (Table 5).
of this compound (272.52 lg/100 g dry basis). Silva et al. (2014) measured the total phenolic content in
However, Pertuzatti et al. (2015) analyzed the car- yellow passion fruit (Passiflora edulis Sims). They found
otenoids profile in yellow passion fruit (Passiflora edulis) 765.09 mg gallic acid equivalent/100 g (dry basis) in pulp
and found: for lutein ? zeaxanthin 1 lg/100 g, b-cryp- and 451.06 mg gallic acid equivalent/100 g in peel (dry
toxanthin 24,990 lg/100 g, lycopene 28 lg/100 g and total basis), similar values to our purple pulp. Already
carotenoids 25,100 lg/100 g. The values of b-cryptoxan- Septembre-Malaterre et al. (2016), found 286.6 mg gallic
thin and total carotenoids were much higher than our study, acid equivalent/100 g in passion fruit pulp (Passiflora
but for lutein ? zeaxanthin, we found higher concentra- edulis), different values about our research.
tions in all varieties and for lycopene, the variety ‘orange’ In summary, genotype, geographic effect, crop year,
were higher too. maturation and storage conditions are some characteristics
In another research realized by Septembre-Malaterre that can influence the content of phenolic compounds,
et al. (2016) where the content of b-carotene in passion anthocyanins, flavonoids, carotenoids and other bioactive
fruit pulp (Passiflora edulis) was investigated, the values compounds in all fruit (Souza et al. 2008; Cardeñosa et al.
found were 3829.20 lg b-carotene equivalent/100 g. These 2016).

Table 4 Analysis of carotenoids in different species of passion fruit (lg/100 g dry weight; mean and standard deviation)
Pulp Peel
Yellow Purple Orange Yellow Purple Orange

Lutein 44.28 ± 2.33b 10.68 ± 0.11c 105.36 ± 3.24a 504.97 ± 24.77b 366.88 ± 17.89b 2881 ± 148.7a
b c a b b
Zeaxanthin 65.51 ± 0.86 7.49 ± 0.05 91.22 ± 1.89 65.61 ± 0.22 48.70 ± 2.85 323.98 ± 11.11a
Cryptoxanthin 254.38 ± 3.32a 30.85 ± 0.07b nd 75.31 ± 0.05b 74.56 ± 0.12b 617.23 ± 37.71a
a-carotene 86.43 ± 4.59a 67.65 ± 2.16b nd nd 37.19 ± 1.29b 420.07 ± 15.02a
a c b b b
b-carotene 1334 ± 78.8 171.88 ± 2.12 744.60 ± 15.47 272.52 ± 11.77 716.32 ± 30.65 21,274 ± 676a
a
Lycopene nd nd 4405 ± 135.1 nd nd nd
a c b b b
Provitamin A* 111.16 ± 6.57 14.32 ± 0.18 62.05 ± 1.29 22.71 ± 0.98 59.69 ± 2.55 1773 ± 56.4a
b c a b b
Total carotenoids 1785 ± 81.5 288.56 ± 0.03 5346 ± 145.4 918.41 ± 36.81 1244 ± 52.5 25,516 ± 561.9a
a,b,c
Different superscript letters in the same row indicate statistically significant difference (p \ 0.05)
nd not detected
*Expressed as lg RAE (Retinol Activity Equivalent)

123
123
Table 5 Analysis of phenolic compounds (mg/100 g dry weight), flavonoids (mg/100 g dry weight) and anthocyanins (lg/100 g dry weight) in different species of passion fruit with mean and
standard deviation
Pulp Peel Seed
Yellow Purple Orange Yellow Purple Orange Yellow Purple Orange

Phenolic 1297.31 ± 13.43b 788.93 ± 3.99c 1559.15 ± 5.33a 1061.87 ± 25.00c 1570.80 ± 26.76b 2584.91 ± 96.67a 346.69 ± 6.58b 325.69 ± 1.18c 429.33 ± 0.19a
compounds
Quercetin 506.45 ± 23.79a 229.79 ± 10.99b 16.28 ± 0.19c 760.21 ± 32.07a nd 800.13 ± 24.18a nd nd 120.41 ± 2.82
Kaempferol 199.66 ± 1.10a 12.35 ± 0.08b nd nd 74.70 ± 1.44b 229.27 ± 8.90a 375.32 ± 13.50 nd Nd
Cyanin nd nd nd nd 1477.47 ± 20.85 nd nd nd Nd
Delphinidin-3,5- nd nd nd nd 8679.60 ± 341.32 nd nd nd Nd
Glu
Cyanidin-3-Glu nd nd nd nd 2852.92 ± 177.93 nd nd nd Nd
Pelargonidin-3- nd nd 183.95 ± 6.52 nd 1551.94 ± 239.03 nd nd nd Nd
Glu
Aglycone nd nd nd nd 90,998.72 ± 5218.53 nd nd nd Nd
Delphinidin
Aglycone nd nd nd nd 1237.73 ± 37.68 nd nd nd 159.18 ± 5.92
Cyanidin
Malvidin 3,5-Di nd nd nd nd nd nd 4598.70 ± 119.73b 8232.41 ± 6.54a Nd
Aglycone nd nd nd nd nd nd nd nd 134.18 ± 0.84
Pelargonidin
Total nd nd 183.95 ± 6.52 nd 103,686.48 ± 542.11 nd 4598.70 ± 119.73 8232.41 ± 6.54a 293.36 ± 6.75
anthocyanins
DPPH* 0.20 ± 0.03a 3.32 ± 0.02c 2.41 ± 0.01b 1.69 ± 0.03a 6.98 ± 0.20c 2.45 ± 0.03b 1.18 ± 0.03a 6.30 ± 0.08c 2.68 ± 0.03b
ABTS* 0.82 ± 0.03a 4.59 ± 0.01c 3.72 ± 0.05b 2.22 ± 0.01a 9.37 ± 0.05c 2.95 ± 0.02b 3.84 ± 0.08a 4.76 ± 0.03b 3.87 ± 0.00a
a,b,c
Different superscript letters in the same row and to the same part indicate statistically significant difference (p \ 0.05)
nd not detected
*IC50 (g/100 mL): Effective Concentration of 50% radical inhibition
J Food Sci Technol
J Food Sci Technol

Flavonoids purple passion fruit reveals a lot of anthocyanins, among


them: cyanin, delphinidin-3,5-glucoside, cyanidin-3-glu-
Flavonoids were analyzed in all parts of different species of coside, pelargonidin-3-glucoside, aglycone delphinidin (the
passion fruit, but the anthocyanins were analyzed only in majoritarian anthocyanin) and aglycone cyanidin. They
seeds of all species of passion fruit, peel of purple passion were also found pelargonidin-3-glucoside in pulp of orange
fruit (because his color is purple) and pulp of orange pas- passion fruit (his color is red), aglycone cyanidin and
sion fruit (because his color is red). In the other parts, we aglycone delphinidin in seed of orange passion fruit and
did not analyze because contains a negligible amount of malvidin 3,5-diglucoside in seeds of yellow and purple
these compounds. passion fruit, which are the same species (Passiflora edu-
The pulp of yellow passion fruit presented to be richer in lis), the purple showed higher content of this anthocyanin
quercetin and kaempferol that other species; for the peel, when compared to yellow passion fruit (Table 5).
orange passion fruit showed more retention of kaempferol As no data were found in the literature about the content
and for seed, only the species of yellow passion fruit of anthocyanins in purple passion fruit peel, we compared
detected this component. with fruits that have purple color in the peel. In a study
Zeraik and Yariwake (2010) evaluated the total flavo- realized by Todaro et al. (2009), delphinidin-3-rutinoside
noids, expressed as rutin and isoorientin in yellow passion was extracted and identified as the major anthocyanin in
fruit pulp (Passiflora edulis Sims f. flavicarpa Degener) eggplant peel (Solanum melongena var. esculentumpeel).
and found 158.03 mg/L and 16.22 mg/L, respectively, Leite-Legatti et al. (2012) analyzed the content of antho-
suggesting that P. edulis fruits may be comparable with cyanins in jaboticaba peel (Myrciaria jaboticaba). They
other flavonoid food sources such as orange juice or sug- found delphinidin 3-glucoside and cyanidin 3-glucoside
arcane juice. (634.75 and 1963.57 mg/100 g, respectively) as antho-
Li et al. (2011) analyzed the flavonoid composition of cyanins. Cyanidin-3-O-glucoside was the dominant antho-
Passiflora edulis ‘edulis’ and Passiflora edulis ‘flavicarpa’ cyanin with 75.6% of the total anthocyanins.
more known as ‘purple’ and ‘yellow.’ The chromatograms Our results indicate promising perspectives for the
revealed that the six major flavonoids obtained from Pas- exploitation of pulps of passion fruit species and their
siflora edulis ‘flavicarpa’ had not been detected in Passi- residues with significant levels of bioactive substances
flora edulis ‘edulis’ which suggested that the two mainly peels of purple passion fruit which is rich in several
population are originally disparate and that the fruit color is anthocyanins.
closely correlated with some other variabilities of the
species. Antioxidant capacity
Silva et al. (2014) measured the content of yellow fla-
vonoids in pulp and peel of yellow passion fruit (Passiflora The DPPH radical has purple color and ABTS the green
edulis Sims). They found 60.37 and 43.08 mg/100 g (dry color. With the addition of the radical fruit extract, the
basis), respectively, different values when compared to our DPPH and ABTS are reduced, presenting yellow color,
study, because they analyzed by spectrophotometry and us with consequent disappearance of absorption. From the
by high-performance liquid chromatography. results, it determines the percentage of antioxidant activity
In another research realized by Septembre-Malaterre and scavenging of free radicals.
et al. (2016) in which the content of total flavonoid content In the antioxidant capacity, pulp, peel and seed of yel-
in passion fruit pulp (Passiflora edulis) was investigated, low passion fruit has a greater power to scavenge the free
the values found were: 70.10 mg quercetin equivalent/ radicals DPPH and ABTS (Table 5), which means that this
100 g. Our study found different values to yellow fruit has a higher antioxidant capacity when compared to
(506.45 mg/100 g), purple (229.79 mg/100 g) and orange purple and orange passion fruit, except for seeds of yellow
(16.28 mg/100 g). and orange passion fruit in ABTS analysis that no signi-
Consequently, these fruit residues and pulp of passion ficative difference was detected.
fruit analyzed in this study can be regarded as a natural Souza et al. (2012) evaluated the antioxidant capacity of
source of flavonoids and the part (pulp, peel, seed) where different fruit, and they concluded that the smallest
the color will indicate the concentration and type of fla- antioxidant capacity was observed in the jenipapo pulps,
vonoid present in this matrix. followed by sweet passion fruit, soursop, murici and
marolo.
Anthocyanins López-Vargas et al. (2013) also evaluated the antioxi-
dant capacity DPPH in pulp and seed and albedo of yellow
A large variety of anthocyanins were found in each part of passion fruit (Passiflora edulis Sims fo. flavicarpa). They
different species passion fruit. As expected, the peel of concluded that the albedo showed a higher ability to inhibit

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DPPH radical than the pulp and seed samples. Our study Cardeñosa V, Girones-Vilaplana A, Muriel JL, Moreno DA, Moreno-
showed different results because we had higher antioxidant Rojas JM (2016) Influence of genotype, cultivation system and
irrigation regime on antioxidant capacity and selected phenolics
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pene, and quercetin in pulps. Castañeda-Ovando A, Pacheco-Hernández ML, Páez-Hernández ME,
Septembre-Malaterre et al. (2016) concluded that the Rodrı́guez JA, Galán-Vidal CA (2009) Review: chemical studies
of anthocyanins. Food Chem 113:859–871
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(Passiflora edulis) pulp (64% of DPPH reduced) when determination of Sudan dyes and Para Red in red chilli pepper.
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Acknowledgments The authors are grateful to the Brazilian Liew SQ, Chin NL, Yusof A (2014) Extraction and characterization
Research Agency (Coordenação de Aperfeiçoamento de Pessoal de of pectin from passion fruit peels. Agric Agric Sci Procedia
Nı́vel Superior—CAPES) for their financial support. 2:231–236
López-Vargas JH, Fernández-López J, Pérez-Álvarez JA, Viuda-
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