Food Chemistry 212 (2016) 225233

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Evaluation of nutritional and antioxidant properties of the tropical fruits

banana, litchi, mango, papaya, passion fruit and pineapple cultivated in
Runion French Island
Axelle Septembre-Malaterre a,b, Giovdie Stanislas a,b, Elisabeth Douraguia c, Marie-Paule Gonthier a,b,
a
Inserm, UMR 1188 Diabte athrothrombose Thrapies Runion Ocan Indien, Plateforme CYROI, 97490 Sainte-Clotilde, La Runion, France
b
Universit de La Runion, UFR Sant, 97487 Saint-Denis, La Runion, France
c
Viva Fruit and Vegetable Company, 97410 Saint-Pierre, La Runion, France

a r t i c l e i n f o a b s t r a c t

Article history: Much attention is paid to the beneficial action of fruits against obesity-related oxidative stress. This study
Received 10 January 2016 evaluated nutritional and antioxidant properties of banana, litchi, mango, papaya, passion fruit and
Received in revised form 17 May 2016 pineapple from Runion French Island. Results showed that total amounts of carbohydrates, vitamin C
Accepted 23 May 2016
and carotenoids were 7.767.3 g glucose equivalent, 4.784.9 mg ascorbic acid equivalent and 26.6
Available online 25 May 2016
3829.2 lg b-carotene equivalent/100 g fresh weight, respectively. Polyphenols were detected as the most
abundant antioxidants (33.0286.6 mg gallic acid equivalent/100 g fresh weight) with the highest con-
Keywords:
tent from passion fruit. UPLC-MS analysis led to identify epigallocatechin and quercetin derivatives from
Tropical fruits
Phytochemicals
banana and litchi, ferulic, sinapic, syringic and gallic acids from pineapple and mango, and piceatannol
Antioxidants from passion fruit. Polyphenol-rich extracts protected red blood cells and preadipose cells against oxida-
Polyphenols tive stress. Altogether, these findings highlight nutritional benefits of French tropical fruits and their
Obesity-related oxidative stress possible interest to improve antioxidant capacities of the body during obesity.
2016 Elsevier Ltd. All rights reserved.

1. Introduction adipose tissue may contribute to oxidative stress by inducing an

It is now well established that dietary habits influence several
cardiometabolic risk factors and that the consumption of fruits
reduces the risk of chronic diseases including obesity and diabetes
(Mozaffarian, 2016). The beneficial effects of fruits have been
partly related to their high contents in antioxidant micronutrients
including vitamin C, carotenoids, minerals and polyphenols (Arts &
Hollman, 2005). However, it is also important to consider carbohy-
drate composition and glycemic index of fruits to better manage
their impact on blood glucose level (Parks, 2002). Concerning obe-
sity, it has been reported that excess of fat storage occurring in the
Abbreviations: AAPH, 2,20 -azobis[2-methyl-propionamidin] dihydrochloride;
AUC, area under the curve; DCFH-DA, 20 ,70 -dichlorofluorescein-diacetate; DPPH,
2,2-diphenyl-1-picrylhydrazyl; GAE, gallic acid equivalent; IL-6, interleukin-6;
MTT, 3-(4,5-dimethyl-thiazol-2-yl)-2,5-diphenyltetrazolium bromide; OD, optical
density; ORAC, oxygen radical absorbance capacity; PBS, phosphate buffer saline;
ROS, reactive oxygen species; TNF-a, tumor necrosis factor-a; UPLC-MS, ultra-high
performance liquid chromatography coupled with diode array detection and
electrospray ionization-mass spectrometry.
Corresponding author at: Universit de La Runion, UFR Sant, 97487 Saint-
Denis, La Runion, France.
E-mail address: marie-paule.gonthier@univ-reunion.fr (M.-P. Gonthier).
overproduction of reactive oxygen species (ROS). ROS disrupt adi-
pose cell function and promote the secretion of pro-inflammatory
cytokines such as tumor necrosis factor-a (TNF-a) and interleukin-
6 (IL-6) (Xu et al., 2003) that participate to insulin resistance onset
(Furukawa et al., 2004; Houstis, Rosen, & Lander, 2006). Therefore,
the biological effect of dietary antioxidants is of high interest.
Among the bioactive phytochemicals, polyphenols have been
extensively studied as the most abundant antioxidants provided
by the human diet. More than 8,000 molecules have been identi-
fied and classified into families comprising flavonoids, phenolic
acids, stilbenes and lignans (Scalbert & Williamson, 2000).
Polyphenols may exert a wide range of biological activities includ-
ing antioxidant and anti-inflammatory properties against obesity-
related oxidative stress and chronic inflammation (Siriwardhana
et al., 2013). Polyphenols from tropical fruits may also have bene-
ficial physiological properties, nevertheless due to various resource
limitations, the anti-diabetic and anti-obesity potential of tropical
fruits has been poorly studied. Exotic fruits from India, China,
Africa and South America are gaining popularity in the market
place due to their nutritional and therapeutic values. Noticeably,
pineapple (Ananas comosus) is one of the most consumed tropical

http://dx.doi.org/10.1016/j.foodchem.2016.05.147
0308-8146/ 2016 Elsevier Ltd. All rights reserved.
226 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233
fruits and the total production worldwide is 1618 million tons
(Sousa & Correia, 2010). In France, Runion Island based in the
Indian Ocean area constitutes a geographically strategic source of
various tropical fruits including the specific Victoria pineapple cul-
tivar (Septembre-Malaterre et al., 2015). According to the French
Department of Agriculture and Food (DAAF, 2016), Runion Island
produced an estimated 10,000 tons of fruits in 2013 with the fruit
cultivated either for the export market (20%) or local consumption
(80%). Production statistics also indicate that Victoria pineapple,
litchi, mango and banana constitute the most important crops in
world export trade after sugar for which Runion Island is ranked
first for the European trade. However, despite such tropical fruits
are increasingly exported worldwide, Runion Island remains an
unreported geographical area. Importantly, there is still a lack of
data concerning the nutritional properties of tropical fruits
produced from this French region.
We aimed to evaluate the levels of carbohydrates, vitamin C,
carotenoids and polyphenols from six tropical fruits which are
the most cultivated in Runion French Island, namely banana,
litchi, mango, papaya, passion fruit and Victoria pineapple.
Polyphenols extracted from tropical fruits were identified by
UPLC-MS analysis and their free radical-scavenging activities
examined. Then, we determined the protective action of
polyphenol-rich pulp extracts on human red blood cells and 3T3-
L1 preadipose cells against oxidative stress, by measuring cell via-
bility and production of ROS and IL-6 pro-inflammatory cytokine.
2. Materials and methods
2.1. Sample collection
Banana (Musa acuminata), litchi (Litchi sinensis), mango (Mangi-
fera indica L.), papaya (Carica papaya), passion fruit (Passiflora edu-
lis) and Victoria pineapple (Ananas comosus) were provided by
Viva Fruit and Vegetable Company. Two varieties of banana (big
banana or Cavendish and little banana or Dwarf Cavendish),
mango (American and Jos) and papaya (Colombo and Solo) were
sampled. For each fruit, three samples were collected at the same
time during the summer period (from november 2013 to february
2014). Fruits were harvested at optimal eating quality and received
at the laboratory one day after harvest. Pulp samples were ground
at room temperature (Grindomix GM 200). Different portions were
analyzed immediately or stored at 20 C until analysis.
2.2. Determination of carbohydrate, carotenoid, vitamin C and
polyphenol contents
Carbohydrate levels were determined according to the method
described by Hallmann (Hallmann, 2012) with slight modifica-
tions. Briefly, 5 mL of concentrated HCl were added to fruit sample
(5 g) and the mixture was heated for an acid hydrolysis. Then,
20 mL NaOH (2 M) were added and the neutralized solution was
mixed with 10 mL Fehling solution. A calibration curve was built
using a standard solution of glucose (Sigma-Aldrich). Total carbo-
hydrate contents were expressed as g glucose equivalent/100 g of
fresh weight.
For the evaluation of carotenoid contents, the method pub-
lished by Khoo et al. (Khoo, Ismail, Mohd-Esa, & Idris, 2008) was
used and carotenoid levels measured by UVVis spectrophotome-
try at 450 nm (Genesys 10 UV scanning). A calibration curve was
built using a standard solution of b-carotene (Sigma-Aldrich). Total
carotenoid contents were expressed as lg b-carotene equiva-
lent/100 g of fresh weight.
The 2,6-dichloro-phenol-indophenol titrimetric method led to
measure levels of reduced ascorbic acid (JAOAC, 1984). Briefly,
5 g of fruit sample were dissolved in 10 mL of metaphosphoric
acid-acetic acid solution and 10 mL distilled water. The solution
was titrated with 0.01% (v/v) of 2,6-dichloro-phenol-indophenol
solution. The final point was considered when the solution had a
pink color for 15 s. A calibration curve was built using a standard
solution of ascorbic acid (Sigma-Aldrich). Vitamin C contents were
expressed as mg ascorbic acid equivalent/100 g of fresh weight.
For polyphenol analysis, 6 g of fruit were added to 30 mL of
aqueous acetone (70%, v/v) containing HCl 1.2 M. After incubation
at 4 C for 90 min, samples were centrifuged at 3500 rpm for
20 min at 4 C. Polyphenol-rich supernatants were collected and
stored at 80 C until analysis. Folin-Ciocalteu assay led to mea-
sure polyphenol contents (Folin & Denis, 1915). Briefly, 25 lL sam-
ple, 125 lL Folin-Ciocalteus phenol reagent (Sigma-Aldrich) and
100 lL sodium carbonate were added in a 96-well microplate
and incubated at 54 C for 5 min, and then at 4 C for 5 min. The
absorbance was measured at 765 nm (FLUOstar Optima, Bmg Lab-
tech). A calibration curve was built using a standard solution of
gallic acid (Sigma-Aldrich,). Total polyphenol contents were
expressed as mg gallic acid equivalent (GAE)/100 g fresh weight.
Flavonoid contents were determined according to the colori-
metric assay reported by Zhishen et al. (Zhishen, Mengcheng, &
Jianming, 1999) with slight modifications. Briefly, 100 lL of sample
were placed in a 96-well microplate with 6 lL of 5% aqueous
NaNO2. After 5 min, 6 lL of 10% aqueous AlCl3 were added and
the mixture was mixed. Then, after 1 min, 40 lL of 1 M of NaOH
were added. The absorbance was measured at 510 nm (FLUOstar
Optima, Bmg Labtech). A calibration curve was built using a stan-
dard solution of quercetin (Sigma-Aldrich). Total flavonoid con-
tents were expressed as mg quercetin equivalent/100 g of fresh
weight.
Polyphenols extracted from tropical fruits were identified by
ultra-high performance liquid chromatography analysis coupled
with diode array detection and electrospray ionization-mass spec-
trometry (UPLC-MS, Agilent Technologies). Briefly, samples were
diluted, filtered on PTFE (0.45 lm) and injected at 1 lL on C18 col-
umn (1.8 lm, 2.1  100 mm2) for chromatographic separation. The
column was eluted with a gradient mixture of 0.1% formic acid in
water (A) and 0.1% formic acid in acetonitrile (B) at the flow rate
of 0.3 mL/min, with 1% B at 00.4 min, 110% B at 0.42 min, 10
35% B at 26 min, 3550% B at 67 min, 5070% B at 78.8 min,
7092% B at 8.810.8 min, 92100% B at 10.812 min, 1001% B
at 1215.2 min. The column temperature was held at 25 C and
the detection wavelength was set to 280 nm. For the mass spec-
trometer conditions, electrospray ionization source was used.
Nitrogen was used as drying gas. The mass spectrometric condi-
tions were optimized as follows: positive mode, nitrogen flow rate
5 L/min, nebulizer pressure 15 psi, drying gas temperature 325 C,
HV capillary 3700 V, end plate offset 500 V, capillary exit
111.2 V, skimmer 40 V and trap drive 45.9; negative mode, nitro-
gen flow rate 10 L/min, nebulizer pressure 25 psi, drying gas tem-
perature 350 C, HV capillary +3400 V, end plate offset 500 V,
capillary exit 115.3 V, skimmer 40 V and trapdrive 42.9. Spectra
were recorded in the range of m/z 1001400 for full-scan MS anal-
ysis by Agilent MassHunter Workstation with Quantitative
Analysis.
2.3. Evaluation of free radical-scavenging activities of polyphenol-rich
extracts from fruits and their impact on human red blood cells exposed
to oxidative stress
To evaluate free radical-scavenging effects of fruit extracts on
2,20 -diphenyl-1-picrylhydrazyl (DPPH) radical, the method we pre-
viously published was used (Hatia et al., 2014). Briefly, 0.25 mM
DPPH (Sigma-Aldrich) diluted in methanol was incubated with
polyphenol-rich extracts. After 25 min at 25 C, the optical density
 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233 227

(OD) was read at 517 nm. Free radical-scavenging activity was To evaluate the cellular inflammatory response, culture media
expressed as the inhibition percentage and calculated as: were collected from 3T3-L1 cells exposed to polyphenol-rich fruit
extracts (25 lM GAE) in the presence or not of H2O2 (200 lM) dur-
Antioxidant capacity % OD control ing 24 h, and analyzed using Mouse IL-6 ELISA kit (eBioscience).
Absolute values were normalized according to total cellular protein
 OD sample=OD control  100:
contents assessed by Bradford test (Bradford, 1976).
Free radical-scavenging activities of fruit extracts were also
assessed by oxygen radical absorbance capacity (ORAC) test, 2.5. Statistical analysis
according to the method previously described (Hatia et al., 2014).
Peroxyl radical was generated using 2,20 -azobis[2-methyl-propio Data were expressed as means SEM of three independent
namidin] dihydrochloride (AAPH) (Sigma-Aldrich) and fluorescein experiments with triplicate analysis. Statistical analysis was per-
(Sigma-Aldrich) was used as the substrate. Briefly, 25 lL sample formed using Prism software. Significant differences (p < 0.05)
diluted 40 times in phosphate buffer saline (PBS, pH 7.4) and between the means were determined by either the Bonferroni or
150 lL of 8.4  105 mM fluorescein were placed in a 96-well Dunnett tests.
black plate, and after 15 min at 37 C, 25 lL of 153 mM AAPH rad-
ical were added to each well. Then, the fluorescence was measured 3. Results and discussion
for 1 h 40 min at an excitation wavelength of 485 nm and an emis-
sion wavelength of 530 nm (Infinite 200, Tecan). Values were cal- This study characterized the nutritional properties of six tropi-
culated based on net area under the curve (AUC) by subtracting cal fruits which are the most produced from Runion Island in
the AUC of the blank from that of samples and compared to Trolox France and increasingly exported worldwide, comprising banana,
standard curve. litchi, mango, papaya, passion fruit and Victoria pineapple.
The capacity of polyphenol-rich fruit extracts to inhibit free
radical-induced hemolysis was measured as previously described
3.1. Carbohydrate, carotenoid, vitamin C and polyphenol contents
(Hatia et al., 2014). Red blood cells were obtained from 11 subjects
from tropical fruits
aged 2040 years-old, according to the authorization from the
Committee for the Protection of Persons and Guidelines from La
As reported on Table 1, carbohydrate levels ranged from
Runion University Hospital. Cells were washed and suspended
7.7 0.7 to 67.3 10.5 g glucose equivalent/100 g. Little banana
in 0.15 M NaCl, pH 7. After three washes with NaCl, they were
exhibited the highest carbohydrate amount whereas carbohydrate
incubated with 50 mM AAPH and polyphenol-rich fruit extracts
contents measured from all other fruits were not statistically dif-
(25 lM GAE) for 18 h at 37 C. Cell lysis was determined by spec-
ferent. Except for little banana, carbohydrate amounts detected
trophotometric measures at 450 nm at 10 min intervals (FLUOstar
were close to those reported for orange, apple or cherry as well
Optima, Bmg Labtech).
as tropical fruits such as mango, passion fruit, guava, litchi and
banana (11.922.8 g/100 g) (Rios de Souza et al., 2014; USDA,
2010). The highest carbohydrate level depicted for little banana
2.4. Evaluation of the effect of polyphenol-rich extracts from fruits on
as compared to that measured for big banana led to suggest varia-
3T3-L1 preadipose cells exposed to oxidative stress
tions according to banana cultivar. Considering that different levels
of dietary carbohydrates give rise to different glycemic responses,
3T3-L1 cells were obtained from American Type Culture Collec-
the knowledge of carbohydrate pattern in these tropical fruits is
tion and grown in Dulbeccos Modified Eagles Medium supple-
of great importance from a nutritional point of view. Indeed, a diet
mented with 25 mM glucose, 10% heat-inactivated fetal bovine
inducing high increments of blood glucose usually leads to an
serum, L-glutamin (5 mM), streptomycin (2 lg/mL) and penicillin
increase in insulin secretion, and high insulinemia has been corre-
(50 lU/mL). Cells were maintained at 37 C with 5% CO2. For viabil-
lated to the stimulation of lipogenesis and the deregulation of
ity measurement, MTT (3-(4-5-dimethylthiazol-2-yl)-2,5-diphenyl
lipoprotein metabolism (Parks, 2002).
tetrazolium bromide) assay was performed according to the
Consumption of fruits and vegetables has been reported to play
method previously described (Hatia et al., 2014). Cells were plated
an essential role in the prevention of diseases, partly due to the
in 96-well plate at a density of 5  103 cells/well. After 24 h, the
presence of antioxidants such as carotenoids, vitamin C and
culture medium was removed and cells exposed to polyphenol-
polyphenols. Carotenoids are lipophilic compounds abundant in
rich fruit extracts (25 lM GAE) in the presence or not of H2O2
considerable tropical fruit species (Pierson et al., 2011). They are
(200 lM) (Sigma-Aldrich) for 24 h. Five hours before the end of
the experiment, 20 lL of sterile filtered MTT solution (5 mg/mL) Table 1
(Sigma-Aldrich) prepared in PBS were added to each well and the Carbohydrate, carotenoid and vitamin C contents from tropical fruits.
plate was incubated at 37 C. Then, the unreacted dye was
Fruit Carbohydrate Total carotenoid Vitamin C content
removed by centrifugation, the insoluble formazan crystals were content content (mg ascorbic acid
dissolved in 200 lL/well dimethyl sulfoxide and the absorbance (g glucose (lg b-carotene equivalent/100 g)
was measured at 560 nm (FLUOstar Optima, Bmg Labtech). equivalent/100 g) equivalent/100 g)
The level of intracellular ROS was assessed by measuring the Papaya Colombo 7.7 0.7a 1922.43 95.0b 51.5 4.7b
oxidation of 20 ,70 -dichlorofluorescein-diacetate (DCFH-DA) accord- Mango American 13.2 0.7a 2806.8 141.7c 18.2 0.9a
ing to the method published (Hatia et al., 2014). Briefly, cells were Passion fruit 13.7 0.1a 3829.2 237.9d 44.4 2.9b
Pineapple 14.3 0.7a 52.6 5.6a 28.9 7.4a
cultured in 96-well black plate (5  103 cells/well) for 24 h. Then,
Papaya Solo 15.7 2.3a 1573.4 153.2b 84.9 4.4c
the medium was removed and replaced by PBS containing 10 lM Litchi 20.6 2.1a 571.4 117.2a 10.1 2.2a
of DCFH-DA (Sigma-Aldrich), and cells were kept in a humidified Big banana 23.9 0.5a 26.6 6.2a 4.7 0.8a
atmosphere (5% CO2, 37 C) for 45 min. Next, cells were exposed Mango Jos 26.3 4.8a 572.6 23.9a 6.0 0.3a
to polyphenol-rich fruit extracts (25 lM GAE) in the presence or Little Banana 67.3 10.5b 45.5 20.1a 5.9 1.2a

not of H2O2 (200 lM) for 1 h. Fluorescence was measured at an Results are means SEM of three independent experiments with triplicate analysis.
excitation wavelength of 492 nm and an emission wavelength of For each nutrient family, means with different letters (ad) are significantly
520 nm (FLUOstar Optima, Bmg Labtech). different (p < 0.001).
228 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233
vitamin A precursors and act as strong antioxidants able to protect
cell membrane lipids from free radicals. Carotenoids are also
extensively used as antioxidant preservatives and colorants in
the food industry (Rufino et al., 2010). As indicated on Table 1, total
carotenoid contents from the tropical fruits analyzed on the pre-
sent study greatly varied depending on the food matrix. Passion
fruit, American mango and papaya exhibited carotenoid levels sig-
nificantly higher than those from Jos mango, litchi, pineapple and
banana. Levels measured from passion fruit, mango, papaya and
litchi were higher than those reported by literature data (USDA,
2010). The abundance of carotenoids in plants such as tropical
fruits has been associated to changes in the expression of genes
involved in carotenoid biosynthesis pathways, in response to envi-
ronmental stimuli integrating photo-oxidative stress and light-
signaling cascades. Carotenoids such as b-carotene exert a benefi-
cial photo-protective action by quenching excited chlorophyll
molecules as well as antioxidant effects in stabilizing membrane
lipids against photo-damage. In tropical fruits particularly colored
such as papaya, lycopene, b-cryptoxanthin and b-carotene are the
main carotenoids that have been identified (Gayosso-Garca
Sancho, Yahia, & Gonzlez-Aguilar, 2010). Here, our data showed
that carotenoid content varied according to mango cultivar as the
level measured for American mango was 5-fold higher than that
found for Jos mango. Similar high variations have been reported
for fruits such as Prunus species (including plums and mirabelles).
Factors comprising environmental stimuli like temperatures or
solar radiation, and agricultural practices such as soil irrigation fre-
quency or cultivation mode on open/shade sites, may also influ-
ence carotenoid composition (Rodriguez-Amaya, Kimura, Godoy,
& Amaya-Farfan, 2008).
Vitamin C is a hydrophilic vitamin provided by many fruits
under L-ascorbic and oxidized L-dehydroascorbic acid forms.
L-ascorbic acid is known as the main biologically active form of
vitamin C and is a powerful antioxidant due to its ability to trap
hydroxyl and superoxide radicals (Almeida et al., 2011). Interest-
ingly, from a methodological point of view, a positive correlation
has been reported between L-ascorbic acid amounts measured by
the 2,6-dichloro-phenol-indophenol titrimetric assay and those
obtained by HPLC method which helps to separately quantify both
L-ascorbic and L-dehydroascorbic acids (Hernandez, Lobo, &
Gonzalez, 2006). Considering that L-dehydroascorbic acid accounts
for less than 10% of total vitamin C in fruits, several authors did not
take it into consideration when reporting vitamin C levels (Lee &
Kader, 2000). Here, through the titrimetric method, we found that
vitamin C levels ranged from 4 to 84 mg ascorbic acid equiva-
lent/100 g depending on the tropical fruit considered, and identi-
fied Solo papaya as the most abundant source (Table 1). Levels
measured from papaya were similar to those published for papaya
from Malaysia (Lim, Lim, & Tee, 2007). Interestingly, Ramful et al.
(Ramful, Tarnus, Aruoma, Bourdon, & Bahorun, 2011) classified
tropical fruits from Mauritius Island according to their vitamin C
contents into three categories, including low (<30 mg/100 g), med-
ium (3050 mg/100 g) and high (>50 mg/100 g) sources. Taking
into account this classification, papaya sample analyzed in the pre-
sent work could be considered as a rich source of vitamin C with
levels close to those reported for orange (70 mg/100 g) which is
referred as one of the most abundant sources of vitamin C com-
monly consumed (USDA, 2010). In contrast, banana, mango, and
litchi samples tested here could be considered as less abundant
sources of vitamin C. As observed above for carbohydrates and car-
otenoids, vitamin C levels may also be influenced by factors such as
genotypic differences. Indeed, Solo papaya exhibited vitamin C
amount significantly higher than that of Colombo papaya. This
agrees with data from other authors reporting the impact of culti-
vars as well as environmental conditions and agricultural practices
on vitamin C composition (Lee & Kader, 2000).
Table 2
Total polyphenol and flavonoid contents from tropical fruits.
Fruit Total polyphenol Total flavonoid content
content (mg gallic (mg quercetin
acid equivalent/100 g) equivalent/100 g)
Pineapple 33.0 2.3a 2.0 0.3a
Papaya Colombo 33.4 3.1a 1.5 0.2a
Mango Jos 41.1 0.4a 6.4 2.0a
Papaya Solo 41.3 5.5a 1.7 0.0a
Mango American 49.0 6.7a 5.3 0.2a
Little Banana 148.5 2.9b 9.1 1.5 a
Big banana 174.4 14.5b 9.9 2.8a
Litchi 178.0 34.7b 53.3 5.9b
Passion fruit 286.6 20.4c 70.1 0.5c
Results are means SEM of three independent experiments with triplicate analysis.
For each nutrient family, means with different letters (ac) are significantly
different (p < 0.001).
Polyphenols are reported as the most abundant antioxidant
micronutrients provided by the human diet with a daily intake
estimated at 1 g (Scalbert & Williamson, 2000). Total polyphenol
content can be used as a relevant indicator of the antioxidant
capacity of a food matrix, and as a preliminary marker for any plant
product expected to be selected as a natural source of antioxidants
for functional foods (Viuda-Martos et al., 2011). Here, we found
that total polyphenol contents significantly varied depending on
the tropical fruit considered (Table 2). Passion fruit was identified
as the richest source of polyphenols, followed by litchi and banana.
Comparatively, pineapple, papaya and mango exhibited a 5-fold
lower polyphenol level. Total polyphenol contents measured from
pineapple and passion fruit were similar to those reported in the
literature (Almeida et al., 2011). However, the amount detected
for mango was lower than that reported by Chen et al. (78 mg
GAE/100 g) (Chen et al., 2014). Interestingly, total polyphenol level
found for banana from Runion Island was higher than that pub-
lished for banana from China and Malaysia (56 mg GAE/100 g)
(Chen et al., 2014; Lim et al., 2007). Considering that flavonoids
may account for about two thirds of the total polyphenol intake
(Scalbert & Williamson, 2000), flavonoid contents from tropical
fruits were also determined in the present study (Table 2). We
found a great variation of flavonoid amounts depending on the
fruit considered, and both passion fruit and litchi were identified
as the most abundant sources (5370 mg quercetin equiva-
lent/100 g), followed by banana (9 mg quercetin equivalent/100 g).
Quantities detected for passion fruit, banana and pineapple were in
accordance with those reported by other studies (Ribeiro da Silva
et al., 2014). For mango and papaya, amounts were lower than
those measured by Luximon-Ramma et al. (28 and 37 mg quercetin
equivalent/100 g, respectively) while levels we measured from
litchi were higher than those reported by the same authors (9 mg
quercetin equivalent/100 g) (Luximon-Ramma, Bahorun, &
Crozier, 2003). Such variations could be related to several factors
influencing levels of bioactive compounds in fruits, such as culti-
vars, climatic conditions, cultural practices and harvest conditions
(Deng, West, & Jensen, 2010).
By UPLC-MS analysis, we identified polyphenol compounds
from pineapple, Colombo papaya, Jos mango, big banana, litchi
and passion fruit (Fig. 1). Derivatives of ferulic, sinapic, gallic and
syringic acids were detected from pineapple and Jos mango while
flavonoids including epigallocatechin 3-O-gallate and quercetin
derivatives were depicted in banana and litchi, respectively. More-
over, both piceatannol and its dimeric form were found in passion
fruit. Several of these compounds from the phenolic acid and flavo-
noid families have been commonly reported in fruits and vegeta-
bles (Scalbert & Williamson, 2000). Piceatannol from the stilbene
family has been poorly detected, except for some sources compris-
ing passion fruit, berry, grape and wine. It is a resveratrol analogue
 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233 229

Fig. 1. Identification of polyphenols from tropical fruits. Polyphenol-rich extracts from tropical fruits were analyzed by UPLC-MS method (280 and 320 nm), and compounds
identified according to their retention time (min) and molecular weight (Da). Polyphenols detected from pineapple extract (320 nm) were hydroxyferulic acid-rhamnoside
(3.7/356), sinapic acid-hexoside (4.3/386) and sinapic acid-dihexoside (4.4/548). The compounds eluted at 4.8 and 5.0 min were not identified. Concerning papaya extract
(280 nm), the compound eluted at 2.9 min remained unidentified. Polyphenols detected from mango extract (280 nm) were gallic acid-O-hexoside (2.9/332), syringic acid-
hexoside (3.2/360). Other eluted compounds were not identified. The compound detected at 3.5 min from banana extract (280 nm) was epigallocatechin 3-O-gallate (3.5/
458). Polyphenols detected from litchi extract (320 nm) were quercetin-dirhamnoside-hexoside (4.6/756), isorhamnetin-dirhamnoside-hexoside (4.9/770) and quercetin-
rhamnoside-hexoside (5.0/610). The compound eluted at 4.8 min was not identified. Polyphenols detected from passion fruit extract (320 nm) were piceatannol (5.7/244) and
its dimeric form (6.6/486). The compound eluted at 3.7 remained unidentified.

with an additional hydroxyl group, and may exert strong antioxi-
dant effects contributing to the biological activities attributed to
resveratrol (Tang & Chan, 2014).
3.2. Free radical-scavenging activities of polyphenol-rich extracts from
tropical fruits and their antioxidant effect on human red blood cells
To assess free radical-scavenging activities of polyphenol-rich
extracts from tropical fruits, both DPPH and ORAC tests were per-
formed. The results obtained with DPPH method were presented
on Fig. 2A. In agreement with data obtained above for total
polyphenol contents, we detected the highest antioxidant activity
for passion fruit (64% of DPPH reduced) whereas other fruits
including mango, pineapple, banana and litchi exerted lower free
radical-scavenging activities (4558%). According to our published
data (Hatia et al., 2014), similar antioxidant capacities were
depicted for equimolar solutions of standard polyphenols such as
epigallocatechin gallate, quercetin and gallic acid. The presence
of such compounds in tropical fruits like litchi, banana, mango
and pineapple may partly contribute to explain their free radical-
scavenging capacities. Interestingly, the antioxidant activities mea-
sured for some tropical fruits in the present study were similar to
those found through a DPPH assay for guava (40%), plum (54%),
strawberry (34%) and banana (65%), but were lower than those
published for mango (84%), passion fruit (94%) and pineapple
(87%) (Alothman, Bhat, & Karim, 2009). ORAC is also used as one
of the most reliable and standard assays to check the antioxidant
capacity of food matrix. Here, ORAC values ranged from 1.5 0.3
to 14.1 2.0 lM Trolox equivalent (Fig. 2B). In agreement with
data obtained above through Folin-Ciocalteu and DPPH assays, pas-
sion fruit exerted the highest free radical-scavenging activity
(14.08 1.99 lM Trolox equivalent). Values obtained for litchi,
passion fruit and papaya were similar to those previously
published, whereas those for banana and pineapple were lower
(Isabelle et al., 2010; Wu et al., 2004). Interestingly, ORAC values
depicted here for French tropical fruits were close to those
reported for some fruits and vegetables considered as strong
antioxidant sources, including onion (4.5 lM Trolox equivalent),
230 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233

Fig. 2. Free radical-scavenging activities of polyphenol-rich extracts from tropical fruits and their antioxidant effect on human red blood cells. Free radical-scavenging
activities of polyphenol-rich extracts from tropical fruits were measured (A) through DPPH method and expressed as % DPPH reduced, or (B) by ORAC assay and expressed as
lM Trolox equivalent. (C) Human red blood cells were incubated with 2,20 -azobis(2-amidinopropane) (AAPH) and polyphenol-rich extracts from fruits (25 lM GAE) for 18 h
at 37 C, and cell lysis was determined by spectrophotometric measurements at 450 nm at 10 min intervals. Results are means SEM of three independent experiments with
triplicate analysis. *: p < 0.05, **: p < 0.0, ***: p < 0.001 as compared to corresponding fruits or control cells.

nectarine (7.2 lM Trolox equivalent), orange (7.5 lM Trolox equiv-
alent), carambola (12.9 lM Trolox equivalent) and broccoli
(14.8 lM Trolox equivalent) (Mahattanatawee et al., 2006; Wu
et al., 2004).
To assess the ability of polyphenol-rich fruit extracts to protect
cells against free radicals, the hemolysis inhibition assay was per-
formed. Indeed, red blood cells are considered as major targets for
free radicals due to the presence of high concentrations of polyun-
saturated fatty acids in cellular membrane and their specific role as
oxygen carriers associated with redox active hemoglobin mole-
cules which are potent sources of ROS (Ajila & Prasada Rao,
2008). Here, AAPH was used as the free radical-initiator to induce
oxidative damage in erythrocytes as it is able to generate peroxyl
radicals that induce the chain oxidation of lipids and proteins
and damage erythrocyte membrane, leading to hemolysis.
Whereas the half-life of control human erythrocytes exposed to
AAPH free radical was 2 h 09 min, polyphenol-rich fruit extracts
protected cells by delaying hemolysis from 2 to 8 h (Fig. 2C). Pas-
sion fruit, big banana and litchi extracts exerted the highest protec-
tive effect by delaying hemolysis to 8 h 13 min, 7 h 36 min and 5 h
39 min, respectively. Little banana exerted the lowest inhibitory
effect, corresponding nonetheless to a half-life which was 2 fold
higher than that of control cells. Several studies have reported
the antioxidant and anti-hemolytic properties of flavonoids,
hypothesizing their localization in the membrane bilayer through
selective bindings with erythrocyte membrane lipids and proteins.
Once compartmentalized into cell membranes, these polyphenols
may inhibit lipid peroxidation and promote membrane integrity
(Cesquini, Torsoni, Stoppa, & Ogo, 2003). In the present study,
the extent of antioxidant capacities depended on the food matrix
and this variation could be related to the polyphenolic composi-
tion. Consistently, our published data demonstrated that antioxi-
dant effects of dietary polyphenols on human erythrocytes
depended on their chemical structure. Quercetin, resveratrol and
epicatechin gallate were found as the most bioactive molecules
and could partly contribute to explain here the strong antioxidant
activity of litchi, passion fruit and banana, respectively. This also
agrees with data reporting polyphenol structure-activity relation-
ships (Rice-Evans, Miller, & Paganga, 1996).
3.3. Antioxidant and anti-inflammatory properties of polyphenol-rich
extracts from tropical fruits on preadipose cells
Adipose tissue development is governed by preadipocyte prolif-
eration and differentiation capacities, and is profoundly altered
during obesity-related oxidative stress (Furukawa et al., 2004). To
evaluate the effect of polyphenol-rich fruit extracts on the viability
of preadipose cells during oxidative stress, 3T3-L1 murine preadi-
pose cells were exposed to polyphenol-rich fruit extracts (25 lM
GAE) in the presence or not of H2O2 (200 lM) during 24 h. Then,
 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233 231

Fig. 3. Effect of polyphenol-rich extracts from tropical fruits on the mitochondrial metabolic activity of 3T3-L1 preadipose cells exposed to H2O2. Cells were exposed to
polyphenol-rich extracts from tropical fruits (25 lM GAE) in the presence or not of H2O2 (200 lM) for 24 h. Then, the mitochondrial metabolic activity was determined by
MTT assay. Results are means SEM of three independent experiments with triplicate analysis. *: p < 0.05, **: p < 0.01, as compared to control, ###: p < 0.001 as compared to
H2O2.

a MTT assay was performed to measure the mitochondrial meta-
bolic activity of cells. As shown on Fig. 3 polyphenol-rich extracts
from litchi, big banana, and little banana enhanced the basal mito-
chondrial metabolic activity (from 100.0 2.2 to 108.7 1.4,
111.2 0.6 and 112.1 3.0%, respectively), and all the other fruit
extracts did not affect it. In contrast H2O2 significantly decreased
it (from 100.0 2.2 to 93.3 0.7%). According to our recent data
H2O2 effect was not attributed to a cell death but to a transient pro-
liferation arrest (Baret et al., 2013; Hatia et al., 2014). Barnouin
et al. (2002) have also demonstrated that dividing cells exposed
to sublethal doses of H2O2 undergo detoxification or repair, and
reinitiate cell cycle progression. Interestingly, except for papaya,

Fig. 4. Effect of polyphenol-rich extracts from tropical fruits on ROS production and IL-6 secretion from 3T3-L1 preadipose cells exposed to H2O2. (A) Cells were exposed to
DCFH-DA (10 lM) for 45 min. Then, they were treated with polyphenol-rich extracts from tropical fruits (25 lM GAE) in the presence or not of H2O2 (200 lM) for 1 h. The
intracellular ROS production was measured by DCFH-DA assay. (B) Cells were exposed to polyphenol-rich extracts from tropical fruits (25 lM GAE) in the presence or not of
H2O2 (200 lM) for 24 h. Then, culture media were collected and IL-6 levels evaluated by ELISA kit. Results are means SEM of three independent experiments with triplicate
analysis. *: p < 0.05, **: p < 0.01, as compared to control, ##: p < 0.01, ###: p < 0.001 as compared to H2O2.
232 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233
all polyphenol-rich extracts from tropical fruits were able to inhibit
H2O2-mediated anti-proliferative action. In a similar previous
study evaluating the protective effect of standard polyphenols on
3T3-L1 preadipose cells exposed to H2O2, we showed through
MTT assay that H2O2 decreased mitochondrial activity and some
of the polyphenols tested such as gallic acid, ferulic acid, daidzein
and genistein did not significantly modulate H2O2 effect. In con-
trast, compounds like epicatechin and caffeic acid were found to
exert a strong protective action. Such results raised the question
about the ability of polyphenols to exert biological activities
depending on their chemical nature, dose, time of exposure and
bioaccessibility extent (Hatia et al., 2014). This may help to explain
the lack of bioactivity for papaya and suggests that it will be of high
interest to determine a possible dose- and time-dependent effect
of polyphenol-rich extracts.
In order to understand the protective role exerted by some trop-
ical fruits against H2O2 action, their impact on the intracellular
production of ROS was evaluated by DCFH-DA fluorescent probe
assay. We found that passion fruit, litchi and American mango
extracts decreased the basal level of ROS (Fig. 4A). While H2O2
increased ROS production (from 100.0 1.9 to 132.9 1.6%,
p < 0.01), all polyphenol-rich fruit extracts counteracted H2O2
action. This antioxidant activity could be partly explained through
the free radical-scavenging activities of fruit polyphenols we
detected above. Furthermore, other mechanisms could be evoked
such as the ability of polyphenols to regulate the activity of
endogenous antioxidant enzymes (Baret et al., 2013; Yen, Chen,
Chang, & Hsu, 2011). Obesity-related oxidative stress is known to
induce an overproduction of pro-inflammatory cytokines such as
IL-6 which may participate to the onset of insulin resistance
(Furukawa et al., 2004). Our results showed that whereas H2O2 sig-
nificantly elevated IL-6 secretion from preadipose cells (from
66.7 5.0 to 133.0 5.8 pg/mg total proteins, p < 0.01),
polyphenol-rich fruit extracts exerted an anti-inflammatory action
by decreasing IL-6 levels to 56.2 6.092.8 6.6 pg/mg total pro-
teins depending on the food matrix (Fig. 4B). We recently reported
the ability of plant polyphenols to regulate Nuclear Factor jappa B
signaling pathway, leading to the reduction of pro-inflammatory
cytokines synthesis from preadipose cells exposed to H2O2-
mediated oxidative stress (Marimoutou et al., 2015). Such a molec-
ular mechanism could contribute to explain the anti-inflammatory
effect of polyphenol-rich fruit extracts. Our previous study also
demonstrated that anti-inflammatory properties of polyphenols
depended on their chemical nature (Hatia et al., 2014). Thus, the
variation of polyphenol composition of tropical fruits may help
to explain the variation of the extent of their anti-inflammatory
action observed here.
4. Conclusion
This study led to the first characterization of the nutritional and
antioxidant properties of six tropical fruits including banana, litchi,
mango, papaya, passion fruit and pineapple cultivated in Runion
French Island. We found that quantities of carbohydrates, vitamin
C, carotenoids and polyphenols varied depending on the food
matrix, and detected polyphenols as the most abundant antioxi-
dants with the highest content from passion fruit. UPLC-MS analy-
sis led to identify phenolic acids from pineapple and mango,
flavonoids from banana and litchi as well as the stilbene piceatan-
nol from passion fruit. Polyphenol-rich pulp extracts exerted free
radical-scavenging capacities and protected human red blood cells
and 3T3-L1 preadipose cells against oxidative stress. Altogether,
these findings should contribute to provide new evidence for the
high interest of polyphenols from tropical fruits for nutritional
strategies aiming to improve antioxidant capacities of the body
during metabolic disorders such as obesity. Further studies will
be needed to evaluate the in vivo effects of polyphenols from trop-
ical fruits in order to better consider their absorption rate,
metabolic fate and ability to target cells in in vivo conditions.
Conflict of interest
The authors declare that there is no conflict of interest.
Acknowledgments
We gratefully acknowledge colleagues from Viva Fruit and
Vegetable Company who provided fruit samples from Runion
French Island. This work was supported by the European Union,
the French Ministry of Education and Research and the Federative
Structure for Environment, Biodiversity and Health from the
University of Runion Island. ASM is a recipient of a Rgion
Runion fellowship.
References
Ajila, C. M., & Prasada Rao, U. J. (2008). Protection against hydrogen peroxide
induced oxidative damage in rat erythrocytes by Mangifera indica L. peel
extract. Food and Chemical Toxicology, 46(1), 303309.
Almeida, M. M. B., de Sousa, P. H. M., Arriaga, . M. C., do Prado, G. M., Magalhaes, C.
E. D. C., Maia, G. A., & de Lemos, T. L. G. (2011). Bioactive compounds and
antioxidant activity of fresh exotic fruits from northeastern Brazil. Food
Research International, 44(7), 21552159.
Alothman, M., Bhat, R., & Karim, A. A. (2009). Antioxidant capacity and phenolic
content of selected tropical fruits from Malaysia, extracted with different
solvents. Food Chemistry, 115(3), 785788.
Arts, I. C., & Hollman, P. C. (2005). Polyphenols and disease risk in epidemiologic
studies. The American Journal of Clinical Nutrition, 81(1 Suppl), 317S325S.
Baret, P., Septembre-Malaterre, A., Rigoulet, M., Lefebvre dHellencourt, C., Priault,
M., Gonthier, M. P., & Devin, A. (2013). Dietary polyphenols preconditioning
protects 3T3-L1 preadipocytes from mitochondrial alterations induced by
oxidative stress. International Journal of Biochemistry & Cell Biology, 45(1),
167174.
Barnouin, K., Dubuisson, M. L., Child, E. S., Fernandez de Mattos, S., Glassford, J.,
Medema, R. H., ... Mann, D. J. (2002). H2O2 induces a transient multi-phase cell
cycle arrest in mouse fibroblasts through modulating cyclin D and p21Cip1
expression. The Journal of Biological Chemistry, 277(16), 1376113770.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of
microgram quantities of protein utilizing the principle of protein-dye binding.
Analytical Biochemistry, 72, 248254.
Cesquini, M., Torsoni, M. A., Stoppa, G. R., & Ogo, S. H. (2003). T-BOOH-induced
oxidative damage in sickle red blood cells and the role of flavonoids.
Biomedicine & Pharmacotherapy, 57(34), 124129.
Chen, G.-L., Chen, S.-G., Zhao, Y.-Y., Luo, C.-X., Li, J., & Gao, Y.-Q. (2014). Total
phenolic contents of 33 fruits and their antioxidant capacities before and after
in vitro digestion. Industrial Crops and Products, 57, 150157.
DAAF (2016). <http://daaf974.agriculture.gouv.fr/Fruits-et-legumes>.
Deng, S., West, B. J., & Jensen, C. J. (2010). A quantitative comparison of
phytochemical components in global noni fruits and their commercial
products. Food Chemistry, 122(1), 267270.
Folin, O., & Denis, W. (1915). A colorimetric estimation of phenols and phenol
derivatives in urine. The Journal of Biological Chemistry, 22, 305308.
Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., ...
Shimomura, I. (2004). Increased oxidative stress in obesity and its impact on
metabolic syndrome. Journal of Clinical Investigation, 114(12), 17521761.
Gayosso-Garca Sancho, L. E., Yahia, E. M., & Gonzlez-Aguilar, G. A. (2010).
Identification and quantification of phenols, carotenoids, and vitamin C from
papaya (Carica papaya L., cv. Maradol) fruit determined by HPLC-DAD-MS/MS-
ESI. Food Research International, 44(5), 12841291.
Hallmann, E. (2012). The influence of organic and conventional cultivation systems
on the nutritional value and content of bioactive compounds in selected tomato
types. Journal of the Science of Food and Agriculture, 92(14), 28402848.
Hatia, S., Septembre-Malaterre, A., Le Sage, F., Badiou-Beneteau, A., Baret, P., Payet,
B., ... Gonthier, M. P. (2014). Evaluation of antioxidant properties of major
dietary polyphenols and their protective effect on 3T3-L1 preadipocytes and red
blood cells exposed to oxidative stress. Free Radical Research, 48(4), 387401.
Hernandez, Y., Lobo, M. G., & Gonzalez, M. (2006). Determination of vitamin C in
tropical fruits: A comparative evaluation of methods. Food Chemistry, 96(4),
654664.
Houstis, N., Rosen, E. D., & Lander, E. S. (2006). Reactive oxygen species have a causal
role in multiple forms of insulin resistance. Nature, 440(7086), 944948.
Isabelle, M., Lee, B. L., Lim, M. T., Koh, W.-P., Huang, D., & Ong, C. N. (2010).
Antioxidant activity and profiles of common fruits in Singapore. Food Chemistry,
123(1), 7784.
 A. Septembre-Malaterre et al. / Food Chemistry 212 (2016) 225233
JAOAC (1984). Official methods of analysis. Vitamin C (ascorbic acid) in vitamin
preparations and juices: 2,6-Dichloroindophenol titrimetric method. Washington,
DC., 844.
Khoo, H., Ismail, A., Mohd-Esa, N., & Idris, S. (2008). Carotenoid content of
underutilized tropical fruits. Plant Foods for Human Nutrition, 63(4), 170175.
Lee, S. K., & Kader, A. A. (2000). Preharvest and postharvest factors influencing
vitamin C content of horticultural crops. Postharvest Biology and Technology, 20
(3), 207220.
Lim, Y. Y., Lim, T. T., & Tee, J. J. (2007). Antioxidant properties of several tropical
fruits: A comparative study. Food Chemistry, 103(3), 10031008.
Luximon-Ramma, A., Bahorun, T., & Crozier, A. (2003). Antioxidant actions and
phenolic and vitamin C contents of common Mauritian exotic fruits. Journal of
the Science of Food and Agriculture, 83(5), 496502.
Mahattanatawee, K., Manthey, J. A., Luzio, G., Talcott, S. T., Goodner, K., & Baldwin, E.
A. (2006). Total antioxidant activity and fiber content of select Florida-grown
tropical fruits. Journal of Agricultural and Food Chemistry, 54(19), 73557363.
Marimoutou, M., Le Sage, F., Smadja, J., Lefebvre dHellencourt, C., Gonthier, M. P., &
Robert-Da Silva, C. (2015). Polyphenol-rich extracts from the medicinal plants
Antirhea borbonica, Doratoxylon apetalum and Gouania mauritiana, protect 3T3-
L1 preadipocytes exposed to oxidative stress by regulating superoxide
dismutase and NF-kappa B. Journal of Inflammation, 115.
Mozaffarian, D. (2016). Dietary and policy priorities for cardiovascular disease,
diabetes, and obesity: A comprehensive review. Circulation, 133, 187225.
Parks, E. J. (2002). Dietary carbohydrates effects on lipogenesis and the relationship
of lipogenesis to blood insulin and glucose concentrations. British Journal of
Nutrition, 87(Suppl 2), S247253.
Pierson, J. T., Dietzgen, R. G., Shaw, P. N., Roberts-Thomson, S. J., Monteith, G. R., &
Gidley, M. J. (2011). Major Australian tropical fruits biodiversity: Bioactive
compounds and their bioactivities. Molecular Nutrition & Food Research, 56(3),
357387.
Ramful, D., Tarnus, E., Aruoma, O. I., Bourdon, E., & Bahorun, T. (2011). Polyphenol
composition, vitamin C content and antioxidant capacity of Mauritian citrus
fruit pulps. Food Research International, 44(7), 20882099.
Ribeiro da Silva, L. M., Teixeira de Figueiredo, E. A., Silva Ricardo, N. M., Pinto Vieira,
I. G., Wilane de Figueiredo, R., Brasil, I. M., & Gomes, C. L. (2014). Quantification
of bioactive compounds in pulps and by-products of tropical fruits from Brazil.
Food Chemistry, 143, 398404.
Rice-Evans, C. A., Miller, N. J., & Paganga, G. (1996). Structure-antioxidant activity
relationships of flavonoids and phenolic acids. Free Radical Biology & Medicine,
20(7), 933956.
Rios de Souza, V., Pereira, P. A. P., da Silva, T. L. T., de Oliveira Lima, L. C., Pio, R., &
Queiroz, F. (2014). Determination of the bioactive compounds, antioxidant
activity and chemical composition of Brazilian blackberry, red raspberry,
strawberry, blueberry and sweet cherry fruits. Food Chemistry, 156, 362368.
233
Rodriguez-Amaya, D. B., Kimura, M., Godoy, H. T., & Amaya-Farfan, J. (2008).
Updated Brazilian database on food carotenoids: Factors affecting carotenoid
composition. Journal of Food Composition and Analysis, 21(6), 445463.
Rufino, M. d. S. M., Alves, R. E., De Brito, E. S., Prez-Jimnezc, J., Saura-Calixto, F., &
Mancini-Filho, J. (2010). Bioactive compounds and antioxidant capacities of 18
non-traditional tropical fruits from Brazil. Food Chemistry, 121(4), 9961002.
Scalbert, A., & Williamson, G. (2000). Dietary intake and bioavailability of
polyphenols. Journal of Nutrition, 130(8S Suppl), 2073S2085S.
Septembre-Malaterre, A., Hatia, S., Lallemand, L., Csari, M., Douraguia, E., Libelle, T.,
& Gonthier, M. P. (2015). Characterization of French Victoria pineapple
antioxidant micronutrients and polyphenol protective effect on preadipose
cells exposed to oxidative stress. International Journal of Food and Nutritional
Sciences, 4(5), 111.
Siriwardhana, N., Kalupahana, N. S., Cekanova, M., LeMieux, M., Greer, B., &
Moustaid-Moussa, N. (2013). Modulation of adipose tissue inflammation by
bioactive food compounds. The Journal of Nutritional Biochemistry, 24(4),
613623.
Sousa, B. A. A., & Correia, R. T. P. (2010). Biotechnological reuse of fruit residues as a
rational strategy for agro-industrial resources. Journal of Technology
Management & Innovation, 5, 104112.
Tang, Y. L., & Chan, S. W. (2014). A review of the pharmacological effects of
piceatannol on cardiovascular diseases. Phytotherapy Research, 28(11),
15811588.
USDA (2010). National nutrient database for standard reference. Release 23.
Retrieved 2010-03-21 from the Nutrient Data Laboratory http://www.nal.
usda.gov/fnic/foodcomp/search.
Viuda-Martos, M., Ruiz-Navajas, Y., Fernndez-Lpez, J., Sendra, E., Sayas-Barber,
E., & Prez-lvarez, J. A. (2011). Antioxidant properties of pomegranate (Punica
granatum L.) bagasses obtained as co-product in the juice extraction. Food
Research International, 44(5), 12171223.
Wu, X., Beecher, G. R., Holden, J. M., Haytowitz, D. B., Gebhardt, S. E., & Prior, R. L.
(2004). Lipophilic and hydrophilic antioxidant capacities of common foods in
the United States. Journal of Agricultural and Food Chemistry, 52(12), 40264037.
Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., ... Sole, J. (2003). Chronic
inflammation in fat plays a crucial role in the development of obesity-related
insulin resistance. Journal of Clinical Investigation, 112(12), 18211830.
Yen, G. C., Chen, Y. C., Chang, W. T., & Hsu, C. L. (2011). Effects of polyphenolic
compounds on tumor necrosis factor-alpha (TNF-alpha)-induced changes of
adipokines and oxidative stress in 3T3-L1 adipocytes. Journal of Agricultural and
Food Chemistry, 59(2), 546551.
Zhishen, J., Mengcheng, T., & Jianming, W. (1999). The determination of flavonoid
contents in mulberry and their scavenging effects on superoxide radicals. Food
Chemistry, 64(4), 555559.