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Journal of Exercise Physiologyonline
June 2017
Volume 20 Number 3
Editor-in-Chief
Official Research Journal of
Tommy
the American
Boone, PhD,
Society
MBA
of
Review
Board
Exercise
Physiologists
Todd Astorino, PhD
Julien Baker,
ISSN 1097-9751
PhD
Steve Brock, PhD
Lance Dalleck, PhD
Eric Goulet, PhD
Robert Gotshall, PhD
Alexander Hutchison, PhD
M. Knight-Maloney, PhD
Len Kravitz, PhD
James Laskin, PhD
Yit Aun Lim, PhD
Lonnie Lowery, PhD
Derek Marks, PhD
Cristine Mermier, PhD
Robert Robergs, PhD
Chantal Vella, PhD
Dale Wagner, PhD
Frank Wyatt, PhD
Ben Zhou, PhD
Official Research Journal
of the American Society of
Exercise Physiologists
ISSN 1097-9751
JEPonline
Swimming Exercise Did Not Ameliorate the Adverse
Effects of High-Sugar Diet in Young Rats
Mariana A. V. Carmo1, Angélica B. G. Pinto1, Karina B. Queiroz2,
Renata G. Sá2, Marcelo E. Silva3, Wanderson G. Lima4, Emerson C.
Oliveira1, Lenice K. Becker1
1Laboratory
of Exercise Physiology (LABFE), 2Laboratory of
Biochemistry and Molecular Biology (LBBM), 3Laboratory of
Experimental Nutrition (LABNEX), 4Laboratory of Morphopathology
(LMP) - Federal University of Ouro Preto, Ouro Preto, Brazil
ABSTRACT
Carmo MAV, Pinto ABG, Queiroz KB, Sá RG, Silva ME, Lima
WG, Oliveira EC, Becker LK. Swimming Exercise Did Not
Ameliorate the Adverse Effects of High-Sugar Diet in Young Rats.
JEPonline 2017;20(3):177-183. The purpose of this study was to
investigate the effects of a swimming exercise (SE) in young rats fed
with a high-sugar diet (HSD). Rats fed with a standard diet or a HSD
were simultaneously subjected to SE or not (sedentary group) for 8
wks. The results showed that the HSD decreased calorie intake and
body weight, but increased body adiposity index, total cholesterol,
HDL-cholesterol, and LDL-cholesterol. The SE reduced the total
cholesterol and LDL-cholesterol. Interaction between HSD and SE
was detected based on body adiposity index measurements, on
VLDL-cholesterol and triglycerides levels, and on citrate synthase
activity. Blood pressure and heart rate did not change significantly
among the different groups. The HSD negatively affected the
majority of the biological parameters while the SE improved body
adiposity index and the levels of some lipoproteins. In conclusion,
the SE did not attenuate the adverse effects of HSD in young rats.
Key Words: Blood Pressure, High-Sugar Diet, Swimming Exercise,
Young Rats
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INTRODUCTION
Children and adolescents often consume high-sugar foods (cakes, cookies, etc.). Added
sugars are consumed very frequently; the most common sources of added sugars in the
United States are soft drinks (14). Sucrose is widely used in processed foods, and its high
usage can be a causative factor for increased blood pressure. This hypothesis is supported
by meta-analyses of randomized controlled trials suggesting that sugar is strongly related to
the increase in blood pressure in humans (23).
Regular physical exercise is beneficial to one’s health because it helps to prevent obesity,
hypertension, dyslipidemia, and cardiovascular complications (17,21), and it reduces blood
pressure (18). Several diet models (high-fat, high-sugar, or a combination of each) highlight
the important role of exercise in reducing their side effects. Exercise has been shown to
reduce the accumulation of fat in the liver in sucrose-enriched choline-deficient diet (nonalcoholic fatty liver disease) (1). Additionally, exercise restored pancreatic function and
autonomic nervous system activity in obese rats, which were reduced by a high-fat diet (13).
The combination of high-sugar consumption and regular exercise attenuates hypertension in
rats (20).
It is crucial to start exercising at an early age to avoid the deleterious metabolic effects
induced by different diets. Low-intensity swimming exercise after weaning considerably
inhibits the obesity induced by neonatal treatment with monosodium L-glutamate in mice.
Exercise helps reduce hyperglycemia, maintains insulin sensitivity, and protects against
deterioration effects in tissues (2). Voluntary post-weaning exercise completely reversed the
metabolic effects of maternal obesity in chow-fed offspring, by reducing adiposity, plasma
leptin, and triglyceride levels (19).
Since children are more physically active by nature, it is commonly thought that the adverse
effects associated with the ingestion of high-sugar foods would be attenuated. However,
there are few studies focusing on the possible association of high-sugar diets with physical
exercise at a young age. Therefore, this study aims to evaluate the effect of regular physical
exercise on biological parameters of young rats fed with a HSD.
METHODS
Animals
Wistar rats (21 days old) were randomly divided into four groups: sedentary and exercised
rats fed with a standard chow diet (S-STD, n = 10), (E-STD n = 10); sedentary and exercised
rats fed with HSD (S-HSD n = 10), (E-HSD n = 10). The Ethics Committee for Animal Use of
the Federal University of Ouro Preto approved the study (25/2013).
Diet and Nutritional Parameters
The animals were fed a HSD (68% carbohydrates) that consisted of 33% standard chow
(Nuvilab, Curitiba, Brazil), 33% condensed milk, and 7% sucrose by weight (the remainder
was water) (9). The control groups were fed with a standard chow (STD). The composition of
each diet has been previously published (11). Rats had their calorie intake and body weight
measured once a week during the experimental period. The weekly food intake was
multiplied by the energy density for the STD (12.22 kJ/g) and the HSD (13.31 kJ/g), to
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calculate the energy intake. The Lee index was used to evaluate the development of obesity.
It was calculated as cubic root of body weight (g) divided by the naso-anal length in
millimeters × 10 (15).
Exercise
The exercised rats swam in collective tanks containing water at 31 ± 1 °C, 1-hr·d-1 and 5
d·wk-1. For the 1st 2 wks, the rats swam without a workload. During the 3rd and 4th wks, the
rats swam supporting a lead weight tied to the tail base that created a workload of 2% of the
rat’s body weight, well above the aerobic/anaerobic metabolic transition that occurs at a
workload of approximately 5% of the rat’s body weight (3). During the 5th wk and until the
end of the experiment, the workload was weekly adjusted to 3% of the rat’s body weight, still
above the aerobic/anaerobic metabolic transition.
Arterial Pressure Measurements
Blood pressure and heart rate were measured in awake rats 48 hrs after the last exercise
section and 12 hrs after their last meal using a pressure transducer coupled to an acquisition
system (PowerLab System; ADInstruments, Dunedin, New Zealand). The data were analyzed
by LabChart 7 software for Windows (16).
Statistical Analyses
Statistical analyses were performed using Graph Pad Prism. The KS test was used to verify
the normality of the data, which were expressed as mean ± standard deviation. We also used
analysis of variance (two-way ANOVA). P values ≤0.05 were considered statistically
significant.
RESULTS
Main Effects of Diet or Exercise
The HSD induced lower calorie intake and reduced body weight. However, body adiposity
index, total cholesterol, HDL and LDL levels were increased. Exercise reduced total
cholesterol and LDL levels (Table 1).
Table 1. Parameters Measured for Rats Fed with an STD or an HSD Subjected to
Swimming Exercise or Not for an 8-Wk Period.
Groups
E-STD
S-STD
Calorie intake (kJ)
367.10 ± 58.03
352.83 ± 56.73
265.05 ± 44.68
264.51 ± 38.39
p = 0.0001
p = 0.7149
p = 0.7349
Body weight (g)
329.90 ± 44.08
323.00 ± 31.08
270.10 ± 17.27
267.00 ± 21.74
p < 0.0001
p = 0.5721
p = 0.6207
1.01 ± 0.22
0.90 ± 1.15
1.70 ± 0.44
1.41 ± 0.22
p < 0.0001
p = 0.0916
p = 0.4514
Total cholesterol (mg·dL-1)
76.89 ± 9.76
65.51 ± 9.96
111.90 ± 15.98
91.12 ± 20.22
p < 0.0001
p = 0.0036
p = 0.3633
HDL cholesterol (mg·dL-1)
22.43 ± 2.80
21.75 ± 1.47
32.17 ± 11.24
29.19 ± 8.10
p = 0.0029
p = 0.4928
p = 0.6658
LDL cholesterol (mg·dL-1)
46.47 ± 13.00
36.35 ± 5.11
64.19 ± 10.48
43.63 ± 10.24
p = 0.0020
p = 0.0003
p = 0.1665
Body Adiposity index
S-HSD
E-HSD
Two-Way ANOVA (P values)
Diet
Training
Interaction
Parameters
Data expressed as means ± SD; Statistical differences were determined using a two-way ANOVA to examine the effects
of diet and/or training and/or interaction, followed by Bonferroni post hoc test; S-STD = sedentary + standard diet; E-STD
= exercised + standard diet; S-HSD = sedentary + high-sugar diet; E-HSD = exercised + high-sugar diet.
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Interactions Between Diet and Dxercise
The interaction between diet and exercise for the Lee index (adiposity index) contributed to
equalizing E-HSD to the control group (S-STD) (Figure 1). The HSD increased the VLDL
cholesterol levels while exercise had the opposite effect. Therefore, the interaction between
the HSD diet and exercise equalized E-HSD to the control group (S-STD) for VLDL values
(Figure 1). Diet and exercise interaction did not affect triglycerides levels (Figure 1) because
HSD blocked the exercise-induced decrease in triglycerides levels. Citrate synthase activity
in the E-HSD group was increased compared to that in the control group (S-STD) (Figure 1),
which indicates that the HSD did not prevent the adaptation to physical training.
1 .8
b
S e d e n ta ry
S t a n d a r d D ie t
a
( m g /d L )
T r ig ly c e r id e s
b
c
40
S e d e n ta ry
20
T ra in e d
0
H ig h S u g a r D ie t
S e d e n ta ry
T ra in e d
0
a
80
S t a n d a r d D ie t
c
10
S t a n d a r d D ie t
100
60
15
H ig h S u g a r D ie t
4
120
b
5
T ra in e d
1 .6
3
a ,b
( m g /d L )
a ,b
b
a
25
20
H ig h S u g a r D ie t
80
a
70
a
60
( a c t iv it y )
L e e in d e x
( a r b it r a r y u n it s )
a
V L D L c h o le s t e r o l
2
C it r a t e S y n t h a s e
1
50
40
b
30
b
20
S e d e n ta ry
10
T ra in e d
0
S t a n d a r d D ie t
H ig h S u g a r D ie t
Figure 1. Interaction of Diet and Exercise Showed by Two Way ANOVA for (1) Lee Index (P = 0.0119), (2)
VLDL cholesterol (P = 0.0493), (3) Triglycerides (P = 0.0132) and (4) Citrate Synthase (P = 0.0069) are
Represented by Different Letters According to Bonferroni post hoc Test.
Systolic, Diastolic Blood Pressure, and Heart Rate
There were no statistically significant differences in systolic blood pressure (S-HSD = 120.9 ±
16.8 mmHg; E-HSD = 107.5 ± 9.5 mmHg), diastolic blood pressure (S-HSD = 97.1 ± 16.3
mmHg; E-HSD 97.0 ± 11.5 mmHg), and heart rate (S-HSD 394 ± 33.1 beats·min-1; E-HSD
369 ± 43.6 beats·min-1).
DISCUSSION
Animals fed with the HSD did not develop high blood pressure or changes in heart rate.
Some studies have reported a positive correlation between sugar consumption and the
increase in arterial pressure (4,5) while others found no correlation (8). It is noteworthy that
rats used in the present study were young. It is possible that this intervention period of 8 wks
was not long enough to induce an alteration in blood pressure.
181
Studies that provided the HSD to weaning rats observed that the alterations in weight gain
were delayed, thus suggest a perturbation in animal growth (9). Previous findings from our
group indicate that HSD induced elevated adiposity indices and hyperplasia of brown adipose
tissue indicates that dietary stimulus can effectively induce obesity (11). However, consistent
with other studies, the S-HSD and E-HSD rats showed high body adiposity index (6,11).
Hypertriglyceridemia was observed in animals that received a diet rich in simple
carbohydrates owing to hepatic lipogenesis and hepatic VLDL secretion, resulting in elevated
serum triglycerides levels (6,10,21).
The lower food intake of the groups that received the HSD may be associated with an
increase in plasma levels of leptin (10,21). Leptin is a hormone secreted by adipocytes, and
its circulating levels are correlated with the amount of fat stored in the body. Leptin levels
increase when an individual adds body fat and, together with other hormones, leptin
regulates appetite control (6,12). Physical training had no effect in weight, calorie intake, and
Lee index in animals that received HSD. Botezelli et al. (3) also studied the combinatorial
effect of the HSD and exercise and showed that exercise did not affect body weight in young
rats.
The combination of the HSD and exercise improved markers of non-alcoholic fatty liver
disease, indicating the beneficial role of exercise (3). Low intensity exercise was not effective
in preventing abdominal adiposity or the increase in plasma and liver triglycerides associated
with sucrose consumption (7). On the contrary, studies using high-intensity and high
frequency training for rats fed with the HSD showed improvement in cholesterol and glucose
homeostasis (3,20). In the current study, exercise training was of submaximal intensity.
The activity of mitochondrial enzymes was used to confirm training-induced elevation of the
oxidative capacity of skeletal muscles (22). Regardless of the diet followed, physical exercise
on a treadmill improved the oxidative capacity of trained animals when compared with their
respective controls (11). In the current study, we observed an increase in the citrate synthase
activity in both HSD- and STD-fed trained groups.
CONCLUSIONS
The HSD negatively affected the majority of the biological parameters, except for blood
pressure and heart rate. Also, while exercise improved the body adiposity index and the
levels of some lipoproteins, it did not prevent the side effects caused by the HSD in young
rats.
ACKNOWLEDGMENTS
Financial support by Capes and CNPq. INCT-Nanobiofar and Pronex CNPQ/FAPEMIG
CCBB-APQ-04758-10 grants. PROPP-UFOP.
Address for correspondence: Emerson Cruz de Oliveira, PhD, Universidade Federal de
Ouro Preto (UFOP) - Centro Desportivo da UFOP (CEDUFOP), Morro do Cruzeiro, zip-code:
35.400-000, Ouro Preto – Minas Gerais, Brazil. E-mail: [email protected]
182
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