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Preventive effect of the bark of Passiflora edulis on obesity-related disorders and oxidative stress in db/db mice

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To verify if the bark of Passiflora edulis prevents obesity-related disorders and oxidative stress in db/db mice. Obese male db/db mice (n = 14 animals) were randomly divided into two groups to receive standard chow and water (obese, n = 7 (OB)) or standard chow with bark of Passiflora edulis (BPe) (obese + BPe, n = 7 (OB + BPe)) for 16 weeks. The evaluated parameters in animals included food and caloric intake, body weight, total body fat and fat deposits, serum glucose, triglycerides, and total cholesterol. Malondialdehyde (MDA) and antioxidant capacity were evaluated in serum and organs (adipose tissue, kidney, liver, and heart). All groups were compared by Student t test, with p < 0.05. The results showed the benefits from BPe by preventing abdominal fat deposition and by reducing the total cholesterol. Moreover, the compound increased the antioxidant capacity from the organs analyzed and reduced the MDA levels in the liver. It is possible to conclude that the consumption of the BPe prevents obesity-related disorders and oxidative stress in db/db mice.
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RESEARCH
Preventive effect of the bark of Passiflora edulis on obesity-related
disorders and oxidative stress in db/db mice
Marielle Fernanda Panelli
1
&Jéssica Leite Garcia
1
&Sérgio Luiz Borges de Souza
1
&Mariane Róvero Costa
1
&
Artur Junio Togneri Ferron
1
&Cristina Schmitt Gregolin
1
&Igor Otávio Minatel
1,2
&Ana Paula Costa Rodrigues Ferraz
1
&
Damiana Tortolero Pierine
1
&Fabiane Valentini Francisqueti- Ferron
1
&Camila Renata Corrêa
1
Received: 25 February 2019 /Accepted: 25 April 2019
#Springer Nature Switzerland AG 2019
Abstract
Purpose To verify if the bark of Passiflora edulis prevents obesity-related disorders and oxidative stress in db/db mice.
Methods Obese male db/db mice (n= 14 animals) were randomly divided into two groups to receive standard chow and water
(obese, n= 7 (OB)) or standard chow with bark of Passiflora edulis (BPe) (obese + BPe, n= 7 (OB + BPe)) for 16 weeks. The
evaluated parameters in animals included food and caloric intake, body weight, total body fat and fat deposits, serum glucose,
triglycerides, and total cholesterol. Malondialdehyde (MDA) and antioxidant capacity were evaluated in serum and organs
(adipose tissue, kidney, liver, and heart). All groups were compared by Student ttest, with p<0.05.
Results The results showed the benefits from BPe by preventing abdominal fat deposition and by reducing the total cholesterol.
Moreover, the compound increased the antioxidant capacity from the organs analyzed and reduced the MDA levels in the liver.
Conclusion It is possible to conclude that the consumption of the BPe prevents obesity-related disorders and oxidative stress in
db/db mice.
Keywords Obesity .Db/db mice .Passion fruit
Introduction
The prevalence of obesity and chronic diseases, such as hy-
pertension, hyperglycemia, and dyslipidemia, has increased
around the world. The literature reports that fat accumulation,
especially abdominal obesity, is related to the development of
obesity-related disorders [16]. Several mechanisms try to
explain the association between obesity and diseases, among
them, higher adiposity, which would induce a redox system
imbalance, characterized by the excess of oxygen reactive
species (ROS) [7]. This condition leads to oxidation of differ-
ent molecules such as lipids, carbohydrates, proteins, and
DNA, which are involved in the development of different
disorders [8,9].
Antioxidants are substances able to protect the organism
against diseases by avoiding molecule oxidation [10,11]. They
are obtained from both endogenous and exogenous sources;
however, the latter is considered the most important since the
nutrients from the diet are indispensable for the endogenous an-
tioxidant synthesis [12]. Based on this, the early introduction of
fruits and vegetables in the diet, which are rich in antioxidants
and bioactive compounds, could be an effective strategy to pre-
vent or delay the obesity-related disorders [1315].
Passiflora edulis, popularly known as passion fruitor
maracujá,is a fruit that contains several antioxidants in the
pulp, leaves, seeds, and bark, such as phenolics, carotenoids,
vitamin C, and polyamines [16]. In a previous study published
by our group [17], it was demonstrated that the treatment of
obese db/db mice with the BPe reduced the body fat and
improved metabolic and antioxidant parameters. However,
there is a lack of studies regarding the preventive effect of
the BPe. So, the aim of this study was to verify if the BPe
prevents obesity-related disorders and oxidative stress in db/
db mice.
*Fabiane Valentini Francisqueti- Ferron
fabiane_vf@yahoo.com.br
1
São Paulo State University (UNESP), Medical School,
Botucatu, Brazil
2
São Paulo State University (UNESP), Institute of Biosciences,
Botucatu, Brazil
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https://doi.org/10.1186/s41110-019-0101-x
Materials and methods
Animals and experimental protocol
In this study, db/db mice were used, which are animals genet-
ically deficient for the leptin receptor, and considered by the
literature an established model for obesity and type 2 diabetes
[18]. All the animals were acquired from Universidade de São
PauloUSP, Brazil. After weaning (21 days of age), male db/
db mice (n= 14 animals) were randomly divided into two
groups to receive standard chow (Presence for rats and mice,
Presence Nutrição Animal, Brazil) and water (obese, n=7
animals (OB)) or standard chow with BPe ((obese + BPe,
n= 7 animals (OB + BPe)) during 16 weeks.
For all the animals, chow and water were offered ad
libitum.Feed and water consumption were measured daily,
and body weight was measured weekly. Two animals per cage
were kept in an environment with controlled temperature (24
± 2 °C), humidity (55 ± 5%), and light-dark cycle (1212 h).
The study protocol was approved by the Ethics Committee on
Animal Experimentation of the Botucatu Medical School,
Universidade Estadual Paulista-UNESP, (1104/2017) in São
Paulo, Brazil, and followed the recommendations of the Guide
for the Care and Use of Experimental Animals [19]. At the end
of the experiment, the animals were anesthetized with keta-
mine and xylazine and then euthanized by cardiac puncture,
and the organs and blood were collected for analysis.
Preparation of chow with bark of Passiflora edulis
The Passiflora edulis fruits were obtained from a rural pro-
ducer in Presidente Prudente city, São Paulo, Brazil, at the
ripening stage and submitted to selection, washed, cut into
small pieces, and oven-dried at 60 °C for 48 h. After this
process, the dried barks were milled (Logen Scientific,
Diadema São Paulo, Brazil) and added to grounded commer-
cial chow (Presence, Paulínea, São Paulo, Brazil), to reach the
proportion of 7 g of Passiflora edulis bark/kg of chow (corre-
spondent to 1.5 g/kg of body weight per day) [20]. Following
this, the mixture was pelleted again for consumption.
Nutritional parameters
In order to characterize the nutritional profile, the initial body
weight (IBW), final body weight (FBW), total body fat (TF
sum of fat deposits: epididymal, retroperitoneal, visceral, and
subcutaneous), adiposity index (AItotal body fat/final body
weight × 100), and feed intake (g/day) were considered.
Metabolic parameters
After 8-h fasting, serum glucose, triglycerides, and cholesterol
levels (kits from BioClin®, Belo Horizonte, MG, Brazil) were
determined by an automatic enzymatic analyzer system
(Chemistry Analyzer BS-200, Mindray Medical
International Limited, Shenzhen, China).
Preparation of tissues for oxidative stress analysis
Increased reactive oxygen species (ROS) are able to oxidize
biomolecules and to affect the antioxidant capacity, so it was
analyzed in this study: MDA levels, an important lipid perox-
idation biomarker, and the antioxidant capacity in the serum
and tissues (adipose, hepatic, cardiac, and renal). Tissues
(100 mg) were homogenized in 1 mL of cold phosphate saline
buffer (PBS), pH = 7.4, and centrifuged (800×g,4°C,
10 min). The supernatant was used in the following analyses:
Malondialdehyde
One hundred microliters of the homogenate was used for
malondialdehyde (MDA) analysis. Briefly, 700 μLof1%or-
thophosphoric acid and 200 μL of thiobarbituric acid (42 mM)
were added to the samples. Then, the mixture was boiled for
60 min in a water bath, and afterward, it was immediately
cooled on ice. A total of 200 μL was transferred to a 2-mL
tube containing 200-μL sodium hydroxide/methanol
(1:12 v/v). The sample was vortex-mixed for 10 s and centri-
fuged for 3 min at 13,000g. The supernatant (200 μL) was
transferred to a 300-μL glass vial and 50 μL was injected onto
the column. The HPLC was a Shimadzu LC-10AD system
(Kyoto, Japan) equipped with a C18 Luna column (5 μm,
150 × 4.60 mm, Phenomenex Inc., Torrance, CA, USA), a
Shimadzu RF-535 fluorescence detector (excitation 525 nm,
emission 551 nm), and 0.5 mL/min flow of phosphate buffer
(KH2PO4 1 mM, pH 6.8) [10]. The MDA was quantified by
the determination of the peak area in the chromatograms rel-
ative to a standard curve of known concentrations. A calibra-
tion curve was obtained by tetra-ethoxypropane (TEP) solu-
tions [21].
Antioxidant capacity
The hydrophilic antioxidant capacity was determined
fluorometrically as described by Beretta et al. [22] using a
microplate reader (VICTOR X2, Perkin Elmer-Boston, MA,
USA). The antioxidant capacity was quantified by the com-
parison between the areas under the curve relative to the oxi-
dation kinetics of the phosphatidylcholine (PC) suspension,
used as a reference for the biological matrix. The compound
2,2-Azobis (2-aminopropano)-dihydrochloride (AAPH) was
used as the peroxyl radical initiator. The results represent the
percentage of the inhibition of 4,4-difluoro-5-(4-phenyl-1,3-
butadienyl)-4-bora-3a,4a-diaza-s-indacene-3-undecanoic acid
(BODIPY, 581/591) in serum relative to that occurring in the
control sample of BODIPY 581/591 in PC liposome. All
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analyses were performed in triplicate, and the results represent
the percentual of protection.
Statistical analysis
Data were analyzed by the Student ttest or the Mann
Whitney and the results are presented as means ± standard
deviation (SD) or medians (interquartile range). Statistical
analyses were performed using Sigma Stat for Windows ver-
sion 3.5. (Systat Software, Inc., San Jose, CA, USA), and a p
value of 0.05 was considered as statistically significant.
Results
The nutritional parameters are presented in Table 1and it
is possible to verify that BPe was able to prevent the
increase in both visceral and retroperitoneal adipose tis-
sues. Moreover, the treated group (obese + BPe) showed
Table 1 Nutritional parameters
Obese Obese + passiflora
Feed intake (g/day 6.53 ± 0.27 10.8 ± 0.5*
IBW (g) 15.8 ± 2.23 14.3 ± 1.8
FBW (g) 53.8 ± 3.6 49.3 ± 5.4
RAT (g) 1.93 ± 0.29 1.50 ± 0.28*
EAT (g) 3.00 (0.19) 2.93 (0.16)
VAT (g) 1.76 ± 0.13 1.42 ± 0.33*
TAS (g) 9.50 ± 0.89 8.07 ± 1.68
TF (g) 16.3 (1.3) 14.5 (1.6)*
AI (%) 31.1 (2.5) 28.9 (2.4)*
BPe,barkofPassiflora edulis;IBW, initial body weight; FBW,finalbody
weight; RAT, retroperitoneal adipose tissue; EAT, epididymal adipose
tissue; VAT, visceral adipose tissue; SAT, subcutaneous adipose tissue;
TF,totalfat;AI, adiposity index. Data are expressed in mean ± standard
deviation, or median and interquartile range (FBW, RAT, TF, AI).
*Indicates P<0.05
Fig. 1 Serum biochemical parameters for total cholesterol (a), triglycerides (b), and glucose (c). Data are expressed in mean ± standard deviation, or
median. Asterisk indicates p< 0.05. BPe, bark of Passiflora edulis
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lower total body fat and adiposity index than the obese
group.
Figure 1presents the serum biochemical parameters. It is
possible to verify the positive effect of the BPe preventing the
increase in the total cholesterol in the treated group. No effect
was observed on glucose and triglycerides levels.
The antioxidant capacity in serum, liver, kidney, left ven-
tricle, and adipose tissue was analyzed an is presented in
Fig. 2. The BPe was able to increase the antioxidant capacity
in serum, kidney, liver, and adipose tissue. Regarding the ef-
fect on the left ventricle, no change was observed.
Figure 3presents the MDA levels in the kidney, liver, left
ventricle, and adipose tissue. It is possible to verify a lower
level of this marker in the liver. There was no effect on MDA
levels in the kidney, left ventricle, and adipose tissue.
Discussion
The principal findings of this study are that BPe treatment
conferred protection against obesity, reduced levels of total
cholesterol, increased antioxidant defense, and reduced
MDA in the liver. These are important findings since the
BPe was effective to modulate the genome-wide expression
profiling in a classic obesity experimental model [23].
The expansion of the adipose tissue, especially the
visceral fat, is indicated as the central dogma regarding
the physiopathology of obesity disorders [24]. Our re-
sults showed a positive effect from the BPe by
preventing visceral and total fat accumulation in the
treatment group. Studies show that natural bioactive
compounds can prevent obesity development by the
modulation of several pathways [25], among them the
stimulation of the peroxisome proliferatoractivated re-
ceptor gamma (PPAR-γ) synthesis. The increased levels
of PPAR-γinduced by some bioactive compounds would
be responsible for the adipose tissue browning, making it
more metabolic and decreasing its lipid deposition [26].
Once the bark of Passiflora edulis is rich in carotenoids
and flavonoids [17], the compound used in this study
may be able to modulate some of these mechanisms in-
volved in fat accumulation.
According to the literature, the reduction in body fat is
responsible for significant metabolic benefits, as the pre-
vention of insulin resistance, glucose intolerance, type 2
diabetes, and dyslipidemia [27]. In this study, the treated
group presented only lower levels of total cholesterol
compared with the non-treated group. This finding can
be attributed to the pectin, a soluble fiber presented in
the BPe, able to form gels and prevents cholesterol ab-
sorption [28]. No effect was observed in glucose level,
which is an expected result once db/db mice are a genet-
ic rodent model for type 2 diabetes [23]. The absence of
effect on triglycerides levels can be related to insulin
resistance. Increased secretion of triglyceride-enriched
VLDL (very-low-density protein) is the commonest
cause of elevated plasma triglycerides in insulin resis-
tance and diabetes conditions [29].
The imbalance of the redox system is considered one of the
main causes of obesity-related disorder development [30]. In
Fig. 2 Antioxidant capacity in serum (a), kidney (b), liver (c), left ventricle (d), and adipose tissue (e). Data are expressed in mean ± standard deviation,
or median. Asterisk indicates P< 0.05. BPe, bark of Passiflora edulis
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the present study, the BPe increased both systemic and tissues
antioxidant capacity, which can be attributed to the antioxi-
dant activity from the BPe, already described in our previous
study [17]. This property is an important finding that demon-
strates the effectiveness to prevent diseases and modulates
antioxidant response by the bioactive compounds present in
discarded parts from foods.
One consequence of the oxidative stress is the lipid
peroxidation, a free radicalmediated chain of reactions
that result in an oxidative deterioration of polyunsaturat-
ed lipids, which are components of biological mem-
branes and common targets of reactive species [31].
Lipid peroxidation results in MDA production, the most
frequently used biomarker of the oxidative stress in
many health problems such as cancer, chronic obstructive
pulmonary disease, and cardiovascular diseases [32]. Our
results showed that the BPe prevented lipid peroxidation
(MDA production) only in the liver. There are several
potential mechanisms that explain the increased lipid per-
oxidation in hepatic tissue. Higher levels of triglycerides
are deposited inside the hepatocytes, which favors the
occurrence of oxidative stress and the progression of
steatosis to steatohepatitis and fibrosis. Reactive oxygen
species and lipid peroxidation products impair the respi-
ratory chain in hepatocytes, either directly or indirectly,
exposing the mitochondrial genome to oxidative damage.
These features, in turn, lead to the generation of more
ROS, and a vicious cycle may ensue. All groups present
higher levels of TG, and the BPe was able to prevent the
hepatic lipid peroxidation [33].
The absence of effect on MDA in the other organs can
be explained by the duration of the experiment. The oc-
currence of free radical production and consequently lip-
id peroxidation in the heart is associated with the elevat-
ed myocardial work and mechanical overload. In kid-
neys, the lipid peroxidation is responsible for the accu-
mulation of adipose tissue around the kidneys of obese
rats [33]. In adipose tissue, oxidative stress occurs espe-
cially in hypertrophied cells [34]. Probably the obese
group did not develop a level of obesity which is able
to lead to oxidative stress in all organs. However, it
demonstrates that the liver is the primary organ affected
Fig. 3 Malondialdehyde levels (MDA) in the kidney (a), left ventricle (b), liver (c), and adipose tissue (d). Data are expressed in mean ± standard
deviation, or median. Asterisk indicates P< 0.05. BPe, bark of Passiflora edulis
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by the reactive species in obesity condition and the BPe
prevents the lipid peroxidation.
Conclusion
In summary, the results showed that the BPe is a good source
of fiber and phytochemicals and have a wide variety of health
benefits as a protection against obesity. In addition, it is note-
worthy that BPe reduced the total cholesterol and increased
the antioxidant capacity of treated animals. Based on these
results, it is possible to conclude that the BPe consumption
prevents obesity-related disorders and oxidative stress in db/
db mice.
Funding Fundação de Amparo à Pesquisa do Estado de São Paulo
FAPESP (2015/09292-0).
Compliance with ethical standards
The study protocol was approved by the Ethics Committee on Animal
Experimentation of the Botucatu Medical School, Universidade Estadual
Paulista-UNESP, (1104/2017) in São Paulo, Brazil, and followed the
recommendations of the Guide for the Care and Use of Experimental
Animals [19].
Conflict of interest The authors declare that they have no conflict of
interest.
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Nutrire
... However, no changes in glucose levels were observed by P. edulis supplementation (Panelli et al., 2018) as previously have been reported Lima et al. (2016). Panelli et al. (2019) repeated the same in vivo assay, with the difference in the supplemented time, as can be appreciated in Table 2, to verify the anti-obesity effects of bark from P. edulis. The main results were confirmed, such as decrease cholesterol serum, reduced weight and visceral fat accumulation and peroxidation status of visceral fat, liver and ventricule. ...
Article
Background The prevalence of obesity around the world arises nowadays in its maximum number. Passiflora sp. genus (Passifloreace family) is native to Brazil and widely cultivated in other regions of America. The extracts of their leaves and fruits have been reported to show sedative and anxiolytic effects. Furthermore, they have been used as a medicinal plant in many populations worldwide. The Passiflora genus has been tested through in vivo studies to treat and prevent obesity and its complications. Likewise, their use as ingredients for developing probiotic foods has been increased. Scope and approach Therefore, the current review aimed to summarize and analyze the current knowledge about the in vivo effects of the Passiflora genus in preventing and treating obesity and overweight, following the systematic review protocol. Furthermore, an extensive review of the use of passion fruit and its by-products in the development of probiotic foods has been included. Key findings and conclusions Twelve works were selected in which different Passiflora genus parts (leave, seed, fruit) have been tested as anti-obesity agents, mainly in animal male models where obesity was induced through diet. Most evidence showed that Passiflora supplementation prevents body fat accumulation and protects against liver damage. However, more in vivo studies with female representation and a significant number of subjects are needed to confirm these results. Probiotics foods are related to improving health and obesity. An emergent tendency is developing probiotic foods (dairy or non-dairy based) with passion fruit or its by-products. Therefore, these new probiotic foods could be used in the transition from high sugar and fat foods to palatable-healthy foods in obese people to help them in their dietary pattern modifications.
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