Document 6602815

Sciknow Publications Ltd.
FBLS 2014, 2(4):90-97
DOI: 10.12966/fbls.12.05.2014
Frontiers of Biological and Life Sciences
©Attribution 3.0 Unported (CC BY 3.0)
24-h Urinary Vanillylmandelic Acid (VMA) is not a Sensitive Parameter to Identify Acute or Chronic Stress Generated by High
Intensity Exercise in Animal Model
Gustavo Puggina Rogatto1,*, Priscila Carneiro Valim-Rogatto1, Ricardo JoséGomes2, JoséAlexandre
Curiacos Almeida Leme3, and Eliete Luciano3
1
Department of Physical Education, Federal University of Lavras, Lavras, Brazil
Department of Biosciences, Federal University of São Paulo, Santos, Brazil
3
Department of Physical Education, São Paulo State University, Rio Claro, Brazil
2
*Corresponding author (Email: [email protected])
Abstract - Vanillylmandelic acid (VMA) is the main urinary end-stage metabolite of epinephrine and norepinephrine. Its concentration can be elevated in some cases of cancer, but also after other stress stimuli. The aim of the study was to investigate the
effect of high intensity physical training (HIPT) and acute exercise on urinary VMA concentration and metabolic aspects related
to glucose metabolism in animal model. Wistar rats underwent four sets of 10 jumps/day supporting a load equivalent to 50% of
body weight, in a water tank for six weeks. A control group was kept in sedentary condition during the same period of time. After
six weeks, sedentary and trained animals underwent an exercise session with the same characteristics of HIPT. Acute high
intensity effort did not change 24-hour urinary VMA concentration in both trained and untrained rats. Both groups increased
glycaemia and lactacidaemia while serum insulin reduced. Acute exercise elevated free fatty acid concentration and decreased
gastrocnemius muscle glycogen content in sedentary animals. It was concluded that high intensity physical training and acute
exercise interfere on glucose metabolism profile without change 24-h VMA.
Keywords - Physical Exercise, Metabolism, Vanillylmandelic Acid, Stress, Rats
1. Introduction
The indication that physical exercise is associated with positive health is not recent or original. Physical training benefitis
associated to correct exercise prescriptions, involving adequate intensity, duration and frequency. Most of experimental
exercise protocols for animal model are based in
low/moderate intensity and long-term (Andrade et al., 2014;
Yoon et al., 2014). Short-term high intensity and intermittent
physical training promotes physiological and morphological
adaptations that differ from those generated by some aerobic
exercise programs, since metabolic demands are dissimilar
(Lemeet al., 2007; Ribeiro et al., 2012).
Exercise intensity is related to stress response influencing
hormonal secretion and substrate consumption. Moreover,
inadequate physical stimulus, generated by erroneous exercise prescription, can result in some undesirable effects such
as those related to overtraining and overreaching. Organisms
exposed to stressful stimuli including exhaustive and/or
prolonged exercise respond with increased secretion of
ACTH and, consequently, elevation of circulating glucocorticoid levels. These hormones exert important effects on
glucose, fat and protein metabolism stimulating catabolic
processes. Other mechanisms involving central nervous
system can also influence metabolic response resulting in
modifications on catecholamine release. Janikowska et al.
(2014) observed that trained road cyclists submitted to
maximum exercise showed increase in plasma epinephrine
but not in norepinephrine concentrations. However, Williams
et al. (2013) observed that recreationally active males presented higher epinephrine and norepinephrine concentrations
when submitted to an acute high-intensity interval exercise
session. Vanillylmandelic acid (VMA) is the main urinary
end-stage metabolite of norepinephrine in the peripheral
sympathetic nervous system (Kopin, 1985). Its measurement
may provide an index of peripheral NE activity.
VMA concentration can be elevated in some cases of
cancer, but also after other stressful stimuli. Physical stress
caused by exercise training can increase the rate of norepinephrine release (Wang et al., 2013). Actually, physical activity has been shown to increase the level of urinary or plasma
NE (Aucouturier et al., 2013; Williams et al., 2013). However,
very few studies have investigated the effects of high intensity
and intermittent physical exercise on VMA secretion and excretion. Tang et al. (1981) investigated the effects of a controlled
Frontiers of Biological and Life Sciences (2014) 90-97
91
exercise program (treadmill walking and bicycle exercise) and
found that VMA levels in plasma increased after acute exercise.
However, urinary VMA concentration did not present any
change when compared to rest condition.
week (beforelactate test, urine collection and euthanasia).
Studies on metabolic and hormonal responses using intermittent high intensity physical exercise with animal model
are even rarer. Thus, it becomes clear need for studies on the
effects of this kind of physical exercise on metabolic and
hormonal adaptations generated by exercise training in longitudinal design. The aim of the present study was to investigate the effect of high intensity physical training (six weeks)
and acute exercise on urinary VMA concentration and metabolic aspects related to glucose metabolism in animal
model.
2.3.1. Body measurements
At the beginning of the experiment and during the following
six weeks all rats were measured and weighted weekly. The
body mass was evaluated with an analytical scale with rats in
fast condition. Nose-anal length was measured with an anthropometrical measuring tape from animal tip of the snout to
its base of the tail. Body weight and length of each rat was
recorded every seven days.
2. Subjects and Methods
2.1. Animals
Forty young male Wistarrats (Rattusnorvegicusalbinus) were
supplied from Animal Care Unit within São Paulo State
University (UNESP), Botucatu. They were maintained at
25±1oC on a 12-h light-dark cycle, with free access to standard rat chow and water. Animal care and all experimental
procedures used were in accordance with those detailed in the
Guide for Care and Use of Laboratory Animals, which was
published by U. S. Department of Health and Human Services
and were analyzed by university ethics Committee on the use
of animals (Protocol 063/2013 - CEUA –Federal University
of Lavras). Animals were selected randomly and distributed
in two groups: sedentary (S) and trained (T, animals submitted to exercise training sessions for six weeks). In the experiments using acute exercise, rats were subdivided in four
groups: sedentary kept in rest (SR), sedentary acutely exercised (SE), trained kept in rest (TR) and trained acutely exercised (TE).
2.2. Exercise training
The physical exercise session consisted of 4 sets of 10
jumps/day in water, supporting a load (compact lead cube)
equivalent to 50% of each animal body mass attached to
thorax by elastic bands (Rogatto & Luciano, 2001a). Rats
were previously familiarized to the jump exercise, performing
sets of exercise with progressive intensity (loads equivalent to
0%, 5%, 10%, 20% and 40% of body mass). Jumps were
performed inside a PVC (poly-vinyl-chloride) tube with a
diameter of 250mm. The bottom of the tube was perforated to
keep rat inside the tube and to permit water to way in and to
draw off. The tube was inserted in a 100cm x 70cm asbestos
tank filled with water at depth corresponding to 150% of rat
individual body length (Rogatto & Luciano, 2001a). The
water temperature was kept at 31±1oC (Gobatto et al., 2001).
Training loads were adjusted every week to promote physiological adaptations. This exercise protocol was performed
during six weeks by TR and TE rats. SE and TE rats performed the exercise session acutely at the end of the sixth
2.3. “In vivo” assessments
2.3.2. Lactate test
At the end of the sixth week rats from sedentary and trained
groups underwent lactate test to evaluate acute responses to
high intensity effort. Test execution was according training
regimen (4 sets of 10 jumps supporting a load equivalent to 50%
of body weight and with water at depth corresponding to 150%
of body length). Blood samples (25l) were collected from a
small cut of tip tail at different times: rest (R), at the end of the
first (F1), second (F2), third (F3) and fourth exercise sets (F4),
as well was at three (A3), five (A5) and 10 minutes (A10)
after the last jump set. Blood samples were stored in Eppendorfs tubes with NaF (1%), for posterior analysis in a lactimeter(YSL 2300 STAT, Yellow Spring, Inc. E.U.A.).
2.3.3. Urinary Vanillylmandelic acid (VMA)
Rats from trained and sedentary groups, in both rest and
acutely exercised condition, were kept at individual metabolic
cages to 24-h urine collection.Previously to urine collection,
100l of chloridric acid were added to the urine collection
containers to acidify and stabilize VMA concentration. After
24 hours rat urine was removed from metabolic cage and
analyzed bymethod proposed by Doles reagents (Doles Reag.
Equip. para Laboratório Ltda®, Goiânia, Brazil). Urine samples were also utilized to evaluated urinary creatinine concentration using Doles Reagents Creatinine kit (Doles Reag.
Equip. para LaboratórioLtda®, Goiânia, Brazil).
2.4. Euthanasia and biological material collection and
analysis
At the end of the experimental period the SR and TR animals
were maintained to 48h resting and 12h fasting and were
euthanized by decapitation. SE and TE rats were sacrificed
after exercise session. Blood samples were collected in tubes
without anticoagulant for posterior analysis of the biochemical parameters (glucose, insulin and free fatty acids) by specific kits. Glucose was determined by enzymatic glucose
peroxidase method (Henry et al., 1974). Insulin was dosed
using DPC insulin radioimmunoassay kit (Diagnostic Products Corporation®, Los Angeles, EUA). Free fatty acids
concentration was determined according to Nogueira et al.
(1990). Gastrocnemius muscle was removed and its white
portion was excised to analyze muscle glycogen concentration according to Sjörgreen et al. (1938) and Dubois et al.
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Frontiers of Biological and Life Sciences (2014) 90-97
(1956).
3. Results
2.5. Statistical analysis
All experimental results were first evaluated with Shapiro-Wilks normality test to establish the necessity for using
parametric statistics. The data were determined to have a
normal distribution. Results were analyzed by ANOVA
followed by a post-hoc Bonferroni test when necessary.
Results are presented as mean ±standard deviation and for all
analysis p<0.05 was considered significant.
All results are expressed as mean and standard deviation.
Figure 1 shows animals’ body weight and nose-anal length
following six weeks of experiment. Both sedentary and
trained rats presented progressive weight gain from the
second to the fifth week (Figure 1-A). However, no significant differences were observed in body mass between experimental groups.Body growth was determined by measuring
the nose-anal length of each rat. Body length evolution is
presented in figure 1-B. Animals from both groups presented
body growth at 1st and 3rd week of the experimental period
(p<0.05). No significant diferences were observed between
groups.
†‡
400
Sedentary
350
†‡
Trained
Sedentary
23
†
Trained
22
250
Length (cm)
Weight (g)
300
24
†‡
200
150
100
A
50
†π
†
†π
†π
†π
†
21
20
19
B
18
17
0
Time 0
1th
2nd
3rd
Weeks
4rd
5th
Time 0
6th
1th
2nd
3rd
Weeks
4rd
5th
6th
Note. †different from Time 0.‡different from previous week.π different from 1st week.No significant differences between groups
Fig. 1. Rats body weight (graphic A, left) and length (graphic B, right) during the experimental period
Figure 2 shows blood lactate concentration of sedentary
and trained rats during the lactate test. Blood lactate concentration during the test presented immediately elevation after
2nd(F2) and 3rd(F3) jumps sets in sedentary and trained animals respectively (p<0.05). At the end of 4th (F4) and last
exercise set both groups continued elevating blood lactate
concentration. Blood lactate concentration was still elevating
at three (A3) and five (A5) minutes after last exercise set
(F4).At 10th minute after exercise (A10) trained animal began
to decrease blood lactate. However, no significant differences
were observed in lactacidaemia when sedentary and trained
groups were compared.
12
Sedentary
Lactate (mmol/L)
10
†‡π
Trained
8
†
6
4
†
†
†‡π
†‡π
†‡
†‡π
†‡π
†‡π
A3
A5
A10
†‡
2
0
R
F1
F2
F3
F4
Time
Note. †different from R. ‡ different from F1.π different from F2. different from F3. No significant differences between groups
Fig. 2. Blood lactate during the lactate test [Blood collection at rest (R), at the end of 1st (F1), 2nd (F2), 3rd (F3) and 4th (F4) sets of
jump, and at 3rd (A3), 5th (A5) and 10th minutes after the last exercise set]
Frontiers of Biological and Life Sciences (2014) 90-97
Figure 3 shows urinary creatinine (3-A) and vanillylmandelic acid (3-B) concentrations of sedentary and trained
rats at rest and acutely exercised. Both exercise and physical
training did not result in changes in urinary creatinine and
VMA concentrations. Table 1 shows serum glucose, insulin
and free fatty acids, and muscle glycogen concentration of
sedentary and trained rats at rest and after the exercise session.
Acute exercise increased serum glucose and decreased insu-
120
4.5
B
4
3.5
100
VMA (mg/L)
Creatinine (mg/dL)
linaemia in sedentary and trained rats (p<0.05). Free fatty
acids concentration did not alter by acute effort or exercise
training. Chronic exercise increased white gastrocnemius
muscle glycogen content. Acute exercise reduced muscle
glycogen concentration only in sedentary rats. Trained animals showed higher post exercise muscle glycogen concentration than sedentary group (table 1).
A
140
93
80
60
40
3
2.5
2
1.5
1
20
0.5
0
0
SR
TR
Time
SE
TE
SR
TR
Time
SE
TE
Note. No significant differences between groups
Fig. 3. Urinary creatinine (graphic A, left) and urinary vanillylmandelic acid (VMA) (graphic B, right) in sedentary (S) and
trained (T) rats kept in rest (R) or submitted to acute exercise (E).
Table 1. Serum glucose, insulin and free fatty acids concentration and gastrocnemius muscle glycogen content of sedentary and
trained rats submitted or not to acute exercise († different from sedentary equivalent group; ‡ different from rest condition)
Experimental
groups
Sedentary rest
(n=10)
Trained rest
(n=10)
Sedentary exercised
(n=10)
Trained exercised
(n=10)
Glucose
(mg/dL)
Insulin
(UI/mL)
Free Fatty Acids
(mEq/L)
Glycogen
(mg/100mg)
102.1 ±4.7
16.5 ±3.9
123.0 ±26.6
0.43 ±0.07
91.1 ±5.6
16.1 ±2.4
140.5 ±23.7
0.60 ±0.08†
152.5 ±15.7‡
8.7 ±2.5‡
207.2 ±50.2‡
0.31 ±0.07‡
148.8 ±12.8‡
8.3 ±0.5‡
138.0 ±25.6†
0.56 ±0.02†
4. Discussion
Exercise has been regarded by some authors as a promoter of
wellness and health to its practitioners, contributing favorably
with circulatory, respiratory, immune and other physiological
systems, and reducing the risk of disorders related to sedentary behavior (Ästrand, 1991; Radak et al., 1999; Rogatto &
Luciano, 2001a).
Studies on the effects of physical exercise through experimental models in laboratory animals allows deeper examination about physical activity on exercised organisms,
enabling new discoveries and ways of treating and preventing
diseases. In our study we analyzed some endocrine-metabolic
adaptations of rats submitted to high-intensity physical
training, assessing the interrelationships of these adaptations
in acute and chronic exercise.
Numerous studies have investigated the effects of regular
physical exercise at different levels of analysis. Chronic
physical activity may result in benefits, since oriented and
applied properly. On the other hand, exercises performed
improperly, either by inadequate intensity, frequency and/or
duration may result in damage and even affect growth and
development of different organs and tissues. Such characteristics may be related to overtraining condition, compromising the performance and physical health and generating stress
to the exercised organism (Selye, 1965; Tabata et al., 1991;
Watanabe et al., 1991;Sothmann et al., 1992; Azevedo, 1994;
Wittert et al., 1996).
Much of experimental models of physical training for
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Frontiers of Biological and Life Sciences (2014) 90-97
animals have been based on aerobic activity, long-lasting, and
moderate intensity. This fact leaves a gap on the possibilities
for study high intensity physical activity.
Weight loss and/or impairment of body growth may be
useful indicatives to identify the inadequacy of physical
exercise for the animals. In the current study any impairment
in these variables were observed, since exercise trained rats,
as well as the animals in the sedentary group showed significant gains in weight and body length in relation to the beginning of the trial. In addition, no significant differences in
body growth between S and T groups were detected which
confirms the idea that exercise training did not negatively
affect the animals. Moreover, urinary creatinine levels did not
change by acute or chronic exercise training showing that
physical effort did not compromise renal function.
The lactate test allowed us not only to detect level of
conditioning of animals subjected to chronic exercise, but also
to report the anaerobic characteristics of the exercise model
proposed. Thus, we observed that physical training used in the
present study can be termed as intense, given the significant
and large increase in blood lactate concentrations during the
test. Blood lactate levels of sedentary and trained animals
were not different from each other, which could indicate a
possible inefficiency of physical training in modifying this
substrate production and/or removal. However, cannot be
disregarded the fact that other metabolic adjustments occurred
as increased energy reserves and modulation of hormonal
secretions.
At the end of six weeks of experiment, animals of trained
and sedentary groups were euthanized at rest and after acute
exercise performance.
Given that physical exercise is a condition in which there
is rapid energy mobilization and redistribution to guarantee
muscle activity, numerous changes in hormonal secretion and
metabolism become necessary for the maintenance of organic
homeostasis (Martin, 1996; Marliss et al., 2000). The reduction of serum glucose concentrations at rest could indicate a
metabolic adaptation to increased uptake of this substrate by
peripheral tissues (Reaven & Chang, 1981; Tan et al., 1982;
Plourde et al., 1991.). However, in our study, no significant
differences in serum glucose concentrations of sedentary and
trained animals at rest were detected. This fact is possibly due
to similar levels of glucose uptake and insulin secretion from
animals’ pancreas. However, during acute exercise, glucose
uptake can increase dramatically, reaching levels 7-20 times
above baseline (Felig & Wahren, 1975; Koivisto et al., 1980;
Ivy, 1987; Lapman & Schteingart, 1991).
When submitted to acute exercise session, both sedentary
and trained rats showed elevation of blood glucose compared
to resting values.This glycemic increase possibly due to
hepatic gluconeogenesis and glycogenolysis that are important factors to preserve homeostasis during exercise. The
occurrence of these events can be related to increased levels
of some hormones such as glucagon, glucocorticoids and
catecholamines among others.
Only sedentary rats showed significant increase in serum
free fatty acids (FFA) concentration after acute effort. This
acute metabolic response resulted in differences between
sedentary and trained groups in post-exercise condition. The
observation of such occurrence may be due to some metabolic
adaptation promoted by physical training, which can have
contributed to free fatty acid uptake into mitochondria for
oxidation during the course of acute exercise.
Insulin secretion is another variable that can be altered by
chronic physical exercise and thus influence the energy distribution in the body. Physical exercise can reduce insulin
levels both at rest and in acute post-exercise condition. In our
study, we found that at rest serum insulin concentrations did
not differ between animals from sedentary and trained groups
which is possibly related to the observation of similar glucose
levels at rest. After the single exercise session, only animals
from sedentary group showed lower levels of serum insulin.
In a previous study (Rogatto & Luciano, 2000a) we observed
that acute exercise reduced insulinaemia in 50% in both
sedentary and trained individuals. Similar phenomenon was
observed by Nakatani et al. (1997), where rats subjected to
endurance training showed significant reduction in plasma
insulin levels immediately after the completion of a workout.
In the present study, the reduction of insulin after the completion of acute exercise observed in sedentary animals may
be due to a "protection mechanism" of the organism in order
to promote the maintenance of glucose homeostasis, since
glucose uptake can present increased after exercise performance, resulting in hypoglycemia. However, Nakatani et al.
(1997) reported that after completion of acute exercise, both
trained and sedentary animals showed progressive increase in
insulin until a period of 48 hours post-exercise, which can
promote increase in glucose uptake. This metabolic response
can favor the accumulation of glycogen in post-exercise
period. In the present study, increases in glucose uptake may
also have occurred in the post-exercise, in view of the observation of increased muscle glycogen stores, even considering similar concentrations of insulin. This fact has been
observed by our group in previous studies using the same
model of physical training (Rogatto & Luciano, 1999, 2000a,
2001b, 2001c).
Chronic physical exercise induces several biochemical
adaptations in different organic levels, as in muscle and liver
tissues, facilitating the mobilization and oxidation of triacylglycerols and favoring removal of lactate produced during the
performance of physical exertion (Saitoh et al., 1983; Kudelska et al., 1996; Hickner et al., 1997; Murakami et al.,
1997). Besides favor aerobic metabolism, increasing number
and size of mitochondria, long-term and moderate intensity
physical training promotes, among other positive adaptations,
increase in energy reserves in different organs and tissues
(Donovan & Brooks, 1983; Henriksson, 1992; Luciano &
Mello, 1999). Such adaptation contributes to the ability of the
organism to develop and maintain muscle work, thus improving performance.
The increase of glycogen content in skeletal muscle may
be due to, among other, an increase in glycogenesis by
Frontiers of Biological and Life Sciences (2014) 90-97
overcompensation mechanism, where after complete depletion of this energy substrate, intense activation of glycogen
synthase (GS) enzyme occurs. Numerous studies have shown
depletion of glycogen content in skeletal muscle after acute
exercise (Nakatani et al., 1997) with subsequent increase in its
concentration after 48 hours of resting (Lamb et al., 1969).
Furthermore, increased peripheral insulin sensitivity observed
in post-exercise may persist for a prolonged period of time
(Cartee et al., 1989; Nakatani et al., 1997). The glucose
uptake during exercise can also occur independently of insulin action, resulting from mechanical stimulation from muscle
contraction process (Rodnick et al., 1992; Young & Balon,
1997), and increased translocation of glucose transporters
"GLUT 4" in muscle (Host et al., 1998ab).
In the present study, high-intensity physical training contributed for trained animals present higher muscle glycogen
levels. Previous studies have found that increased glycogen
storage by post-exercise overcompensation mechanism has
been higher in trained animals (Lamb et al., 1969; Tan et al.,
1984; Nakatani et al., 1997).
Furthermore, increase in muscle glycogen in trained group,
even with similar serum glucose and insulin levels in both
groups at rest, may also be due to increased glucose uptake
and/or peripheral insulin sensitivity arising the last training
session. This adaptation, mainly observed after acute performance of physical activity, may improve glucose tolerance.
Luciano & Mello (1998), studying diabetic rats submitted to
aerobic swimming training, observed increase in glycogen
reserves after four weeks of exercise training. The same
physiological adaptation was observed in our previous studies
(Rogatto & Luciano, 2000b, 2000c, 2001b) where rats were
submitted to high intensity and intermittent exercise training.
Muscle glycogen accumulation can also occurred by increase
in glucose uptake by repeated muscle contractions mechanism,
or by reducing the "turnover" of muscle glycogen during
exercise (Rodnick et al., 1992; Azevedo et al., 1998).
The overcompensation observed after glycogen depletion
may also be due to higher glucose transporters "GLUT 4"
activity and glycogen synthase (GS) enzyme, which favor the
repletion of muscle glycogen (Kristiansenet al., 2000). Other
datasets have suggested depletion of muscle glycogen after
performing intense physical effort (Kudelska et al., 1996;
Murakami et al., 1997; Rogatto & Luciano, 1999). This fact
may influence the activation mechanism of overcompensation.
The depletion of muscle glycogen by acute exercise may
be due to, among other factors, the activation of adrenal
medulla. In the present study, we observed no significant
changes in urinary vanillylmandelic acid concentration.
However, this may not be reflecting adrenal activity and
catecholamine secretion in time of stress generated by performing physical exercise.Actually, very few studies have
investigated the effects of physical exercise on VMA secretion and excretion. Tang et al. (1981) investigated the effects
of a controlled exercise program (treadmill walking and
bicycle ergometry exercise) and found that VMA levels in
95
plasma increased after acute exercise. However, urinary
VMA concentration did not present any change when compared to rest condition. For those authors, the lack of change
in the corresponding urinary metabolite, despite significant
changes in plasma levels, clearly suggests that factors such as
renal clearance and/or metabolism of this metabolite or their
precursors attenuate or dampen any activity-dependent
changes. On the other hand, Pequignot et al. (1979) observed
increase in VMA excretion in men submitted to short-term
(15 min) exercise. These findings confirm that the VMA is
influenced by different factors which hamper its use as a
screening parameter of the stress effects caused by exercise.
Our findings suggest that high intensity and intermittent
physical training did not impactrats´body growth and favored
muscle glycogen storage. Acute exercise acted on metabolic
profile reducing circulating insulin and muscle glycogen
content and increasing serum glucose and free fatty acid.
Moreover, urinary VMA is not a sensitive parameter to detect
stress stimulus generated by acute and chronic exercise.
Acknowledgment
Authors would like to thank FAPESP for financial support.
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