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Vol. 83, Issue 6, 2080-2085, December 1997
Department of Physiology, National Cheng-Kung University Medical College, Tainan, Taiwan 701, Republic of China
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Wang, Jong-Shyan, Chauying J. Jen, and Hsiun-Ing Chen.
Effects of chronic exercise and deconditioning on platelet
function in women. J. Appl. Physiol.
83(6): 2080-2085, 1997.
To investigate the effects of chronic
exercise and deconditioning on platelet function in women, 16 healthy
sedentary women were divided into control and exercise groups. The
exercise group cycled on an ergometer at 50% maximal oxygen
consumption for 30 min/day, 5 days/wk, for two consecutive menstrual
cycles and then were deconditioned for three menstrual cycles. During
this period, platelet adhesiveness on a fibrinogen-coated surface,
ADP-induced platelet aggregation and intracellular calcium
concentration elevation, guanosine 3
,5-cyclic monophosphate (cGMP) content in platelets, and plasma nitric oxide metabolite levels were measured before and immediately after a progressive exercise test in the midfollicular phase. Our
results indicated that, after exercise training,
1) resting heart rates and blood
pressures were reduced, and exercise performance was improved;
2) resting platelet function was
decreased, whereas plasma nitrite and nitrate levels and platelet cGMP
contents were enhanced; and 3) the
potentiation of platelet function by acute strenuous exercise was
decreased, whereas the increases in plasma nitrite and nitrate levels
and platelet cGMP contents were enhanced by acute
exercise. Furthermore, deconditioning reversed these training effects. This implies that training-induced platelet functional changes in women in the midfollicular phase may be mediated
by nitric oxide.
platelet adhesion; aggregation; nitric oxide; midfollicular phase; guanosine 3 INTRODUCTION REGULAR EXERCISE and physical conditioning may reduce
the risk of major vascular thrombotic events and protect individuals against cardiovascular diseases (2, 24). Because platelets play a key role in thrombus formation, the protective effect of exercise against cardiovascular diseases may be partially due to
alterations of platelet function. Results from our previous study of
men indeed suggest that platelet adhesiveness and aggregability are
suppressed by moderate intensities of acute exercise and exercise training (31, 32). However, similar studies in which women subjects
were used have not been carried out, perhaps because of inconsistent
results regarding the platelet function during different phases of the
menstrual cycle (MC) (21, 23). We recently found that platelet function
of women subjects in the midfollicular phase, but not in the midluteal
phase, was affected by acute exercise (33). It is plausible to
hypothesize that exercise training may also affect platelet function in
women during the midfollicular phase.
In 1987, Busse et al. (4) reported that endothelium-derived relaxing
factor (EDRF) could inhibit platelet activation. Recently, we found
that exercise training could enhance agonist-stimulated EDRF release in
rabbit or rat aortas (6-8). It is possible that exercise training
in humans may also modulate platelet activities via altered EDRF
release. Because EDRF has been identified as nitric oxide (NO) and its
action is mediated by guanosine 3 MATERIALS AND METHODS ,5-cyclic monophosphate
,5-cyclic monophosphate
(cGMP) (3), we, therefore, assessed plasma NO metabolite (nitrite and
nitrate) levels and platelet cGMP content to clarify the possible
mechanisms for exercise-training effects on platelet function.
O2 max), which was
estimated by heart rates, for 30 min/day, 5 days/wk, for two MCs, and
this was then followed by three MCs of deconditioning.
Exercise test and blood collection.
At the beginning of the study, a progressive exercise test was
performed by each subject at the midfollicular phase. During the
experimental period, exercise tests were repeated every cycle in the
training group until the end of deconditioning. In contrast, the
control group performed exercise tests at the midfollicular phase
twice, one at the beginning and the other at two MCs later. To avoid
the short-term exercise effects, the training subjects performed
exercise tests at least 48 h after training.
On the testing days, subjects arrived our laboratory at 1:00 PM to
avoid possible diurnal influence (30). After a 30-min rest, 35 ml of
blood samples in total were collected from a forearm vein for
measurements of resting platelet function and plasma NO metabolites as
described below. Immediately after the exercise test, another blood
sample was drawn for the measurements of postexercise parameters.
Sodium citrate (0.106 M, 
of blood volume) was added as an
anticoagulant in the samples for platelet-function evaluation, and
heparin (20 IU/ml) was used in the samples for measurement of plasma NO
metabolites.
A progressive exercise test, described in detail in a previous study
(31), was conducted at 3:30 PM. The exercise protocol consisted of
2-min unloaded pedaling, followed by a continuous increment of
workload, 10-20 W every 3 min, until exhaustion. During the
exercise test, the electrocardiogram was continuously monitored and
converted to the heart rate. Resting blood pressure was measured by a
sphygmomanometer. Subjects' minute ventilation, O2 consumption, and
CO2 production for every minute
were obtained as described previously (5).
Platelet adhesiveness.
Platelet-rich plasma (PRP) was used for the determination of platelet
adhesiveness and aggregability. It was prepared by centrifugation of
10-ml citrated blood samples at 120 g
for 10 min at room temperature. Platelet-poor plasma was obtained as
the supernatant after recentrifugation at 1,600 g for 10 min.
Platelet adhesiveness was determined by using a tapered parallel-plate
chamber as described previously (31). PRP was gently infused into the
chamber and was allowed to settle on the fibrinogen-coated surface for
12 min. The flow chamber was then flushed with
Tyrode-N-2-hydroxyethylpiperazine-N-2-ethanesulfonic acid (HEPES) buffer (0.128 M NaCl, 2.7 mM KCl, 0.5 mM
MgCl2, 0.36 mM
NaH2PO4,
12 mM NaHCO3, and 10 mM HEPES, pH
7.4) for 5 min at a flow rate of 0.027 ml/s, which provided a
shear-stress range from 55 to 0 dyn/cm2. Ten field locations along
the central line were observed at intervals of 5 mm from the downstream
end with approximately zero shear stress, and the number of remaining
platelets per 0.16 mm2 was counted
at each location. A simple linear regression line for adherent
platelets along with various shear-stress fields was obtained. The
slope of this regression line was used as an index of platelet
adhesiveness; i.e., the less negative the slope, the greater the
platelet adhesiveness.
Platelet aggregability.
ADP-induced platelet aggregation was evaluated by the percentage of
reduction in single platelet count as described in our previous study
(32). Briefly, the kinetics of platelet aggregation in PRP was assessed
with a platelet aggregometer (Hema Tracer 2, Niko Bioscience) after
addition of various concentrations of ADP (Sigma
Chemical). After the optical density had reached a steady
value for at least 1 min, the test tube was then removed from the
aggregometer and left undisturbed for 90 min to allow sedimentation of
platelet aggregates. Forty microliters of plasma from the
upper suspension were used to measure a single platelet count. Results
were expressed as the percent ratio of aggregated platelets to total
platelets.
Measurement of platelet intracellular
Ca2+
concentration
([Ca2+]i).
Platelets were labeled with the
Ca2+-sensitive fluorescent dye
fura 2-acetoxymethyl ester (AM) (Molecular Probes) as described in our
previous study (16). Briefly, PRP was mixed with calcium-free HEPES
buffer, which contained 0.05 IU/ml apyrase (Sigma Chemical) and 0.05 IU/ml hirudin (Sigma Chemical), and was added to a polypropylene tube
with 0.4 g/ml albumin at the bottom to act as a cushion. After
centrifugation, platelet pellets were incubated with calcium-free HEPES
buffer containing fura 2-AM (4 mM), apyrase (0.05 IU/ml), and hirudin
(0.05 IU/ml) at 37°C for 40 min. These fura-2-AM-loaded platelets
were used to measure their basal and ADP-induced
[Ca2+]i by
using a dual-wavelength fluorescence spectrophotometer (Hitachi, excitation wavelength 340/380 nm, emission wavelength 510 nm) (29).
Measurement of platelet cGMP contents.
Platelet cGMP contents were determined by enzyme-linked immunosorbant
assay (ELISA) by using a commercially available kit (Cayman) (15). In
brief, citrated PRP containing
10
4 M of
3-isobutyl-1-methylxanthine (a phosphodiesterase inhibitor; Sigma
Chemical) was mixed with ice-cold HEPES buffer and centrifuged at 6,500 g at 4°C for 5 min. The pellet was
vortexed with ice-cold trichloroacetic acid (TCA; 6%) for 2 min. After
centrifugation (10,000 g, 4°C, 15 min), TCA was removed by washing four times with five volumes of water
saturated ether. The extracted samples were stored at 
80°C
until measurement.
Determination of plasma NO metabolites (nitrite and nitrate).
NO metabolites in plasma were determined by the Griess reagent-based
colorimetric method (13) by using commercially available assay kits
(Cayman). First, plasma nitrate was reduced to become nitrite. Then,
nitrite was converted into a deep purple azo compound with an
absorbance at 550 nm. Measured values represented the total amount of
plasma NO metabolites, i.e., nitrite plus nitrate.
Measurement of plasma progesterone.
Plasma progesterone levels were measured by using a progesterone ELISA
kit (Cayman) to confirm the menstrual phases.
Statistics.
The statistical software package of StatView 4.0 (Macintosh) was used
for analyses of our data. The comparison of variables between trained
and control groups at the beginning and 2 MCs later were analyzed by
analysis of variance (ANOVA), followed by Fisher's multiple-range
test. To compare the differences of various parameters in the trained
group along with the experimental period, data were analyzed by the
randomized-block ANOVA and Tukey's multiple-range test. Differences
were considered significant at P < 0.05. The results are expressed as means ± SE.
RESULTS
It was confirmed that all the experiments were performed in the midfollicular phase, because resting plasma progesterone levels in all subjects were low (<2.6 ng/ml) on the experimental days. The length of MCs did not differ between control and trained groups either before or after training; i.e., 31 ± 1 and 30 ± 1 days/cycle for control and trained groups before training and 30 ± 1 and 30 ± 2 days/cycle for control and trained after training, respectively.
Heart rates and blood pressures. Figure 1 shows that before training, resting heart rates, systolic and diastolic blood pressures, and maximal heart rates were not significantly different between control and trained groups. However, the trained group had significantly lower resting heart rates and blood pressures than did the control group after training (Fig. 1; P < 0.05). Moreover, the trained group had lower resting heart rates and blood pressure compared with pretraining values. After one MC of deconditioning, the training effects disappeared (Fig. 1).
Exercise performance. The trained subjects improved their exercise performance, including elevating time to exhaustion, maximal workload, maximal minute ventilation,
O2 max,
and maximal CO2 production, after exercise training (Fig. 2;
P < 0.05). However, the training
effects were reversed back to the pretraining state after
deconditioning (Fig. 2). They also had significantly greater exercise
performance than did their controls after training (Fig. 2;
P < 0.05). In contrast, the control
group did not alter exercise performance after two MCs (Fig. 2).
max, maximal minute ventilation;
O2 max, maximal O2 consumption;
CO2 max,
maximal CO2 production.
* P < 0.05 compared with
pretraining data in trained group.
# P < 0.05, trained vs. control.
Platelet adhesiveness and aggregability. Our results showed that resting and postexercise platelet adhesiveness decreased after one or two MCs of training in the trained group (Fig. 3; P < 0.05). On the contrary, the control group did not alter platelet adhesiveness after two MCs (Fig. 3). Moreover, the trained group had significantly lower platelet adhesiveness than did the control after two MCs of training (Fig. 3; P < 0.05). The training effects on platelet adhesiveness, however, were reversed back to the pretraining state after deconditioning (Fig. 3). Before training, acute severe exercise would increase platelet adhesiveness. This acute effect, however, no longer existed after training.
Figure 4 demonstrates that ADP-induced platelet aggregation was decreased by training. In contrast, the control group did not alter ADP-induced platelet aggregation (Fig. 4). Moreover, the trained group had lower resting and postexercise platelet aggregability did than the control after two MCs of training (Fig. 4; P < 0.05). This training effect was reversed back to the pretraining state after deconditioning. Although a short-term strenuous exercise increased platelet aggregation induced by 0.25 µM ADP at the beginning of this study, this acute exercise effect did not exist after training.
Platelet [Ca2+]i. Basal and ADP (0.5 or 2 µM)-evoked platelet [Ca2+]i values were decreased by training (Fig. 5; P < 0.05). These training effects were reversed back to the pretraining state after deconditioning. Conversely, they were not altered in the control group after two MCs of experimental period (Fig. 5). It was also noticed that the trained group had lower basal and ADP-evoked platelet [Ca2+]i than did the control after training (Fig. 5; P < 0.05).
Although a single bout of strenuous exercise enhanced basal and ADP-evoked platelet [Ca2+]i at the beginning of this study (Fig. 5; P < 0.05), this phenomenon did not happen after training. In contrast, it consistently existed in the controls throughout the experiment (Fig. 5; P < 0.05). Platelet cGMP. Figure 6 shows that resting and postexercise platelet cGMP contents were increased after training in the trained group (P < 0.05). These training effects were reversed back to the pretraining state after deconditioning. Conversely, platelet cGMP contents were not altered in the control group (Fig. 6). The trained group also had higher resting and postexercise platelet cGMP contents than the control after training (Fig. 6; P < 0.05).
Although platelet cGMP content was not changed by a single bout of strenuous exercise at the beginning, it was significantly increased by short-term strenuous exercise after training and was reversed back to the pretraining state by deconditioning (Fig. 6; P < 0.05). In controls, platelet cGMP content was not significantly changed by severe exercise throughout the experimental period (Fig. 6). NO metabolites (nitrite and nitrate) in plasma. Figure 7 shows that before training, resting or postexercise plasma nitrite and nitrate levels did not differ between control and trained groups. However, they were increased in the trained group after training (Fig. 7; P < 0.05). This training effect was reversed back to the pretraining state after deconditioning. Conversely, plasma nitrite and nitrate levels were not altered in the control group (Fig. 7).
DISCUSSION
Our results demonstrated that, in the follicular phase, two MCs of chronic moderate exercise training 1) increased female subjects' aerobic capacities; 2) decreased platelet adhesiveness, ADP-induced platelet aggregation, and [Ca2+]i elevation; 3) increased platelet cGMP contents and plasma nitrite and nitrate levels; and 4) eliminated the acute severe exercise effects on platelet function. We also found that deconditioning reversed these training effects back to the pretraining state.
It is well known that the risk of primary cardiac arrest is transiently increased during vigorous exercise, whereas habitual physical exercise decreases the risk of primary cardiac arrest (9, 28). We have previously used male subjects to show that, whereas acute strenuous exercise enhances platelet adhesiveness and aggregability, acute moderate exercise and exercise training suppress these platelet-function parameters (31, 32). The present study is the first report to clearly demonstrate that platelets in women at the midfollicular phase, like those in men, can be suppressed by chronic exercise and be reversed back to the pretraining state after deconditioning. Based on this study and previous reports (31-33), exercise effects on cardiovascular diseases, being either protective or antagonistic, can be partially explained by the differential effects due to various intensities and durations of exercise. In addition, we also observed that acute exercise affected platelet function in women only at the midfollicular phase and not at the midluteal phase (33). This may be one possible reason to explain the epidemiological observation that premenopausal women have lower incidences of cardiovascular diseases than do men (17).
NO has potent antiplatelet effects. It stimulates platelet guanylate cyclase, elevates platelet cGMP levels, reduces agonist-induced rise of platelet [Ca2+]i, and suppresses agonist-induced platelet aggregation (4). By similar mechanisms, NO also suppresses platelet adhesion (10, 15). Animal studies indicated that exercise training could enhance agonist-stimulated NO release (6-8). Whether chronic exercise can enhance NO release in humans has not been reported before. Our results showed that exercise training in women at the midfollicular phase could enhance plasma nitrite and nitrate and platelet cGMP levels and could suppress basal and ADP-induced platelet [Ca2+]i elevation. Therefore, exercise training apparently can increase endogenous NO release and elevate cGMP contents in platelets, which in turn may suppress platelet reactivity.
There are several possible explanations for the training-induced NO release. First, exercise training in animals increases norepinephrine (NE)-induced NO release (6, 8). Therefore, this NE-stimulated NO release may in turn diminish the NE-evoked platelet activation (25). This is consistent with our finding that training is able to prevent platelet activation by a single bout of strenuous exercise, which should be accompanied with NE elevation (19, 22). Second, increased blood flow during repetitive exercise may increase NO release. Augmentation of femoral arterial flow induced by peripheral vasodilation or by arteriovenous shunt can elicit vasodilation in vivo (26). Besides, in vitro studies demonstrate that blood vessel segments can release NO in response to either increased steady blood flow rate (27) or increased pulsatile frequency (14). However, whether vessels subjected to periodic elevation of blood flow, simulating the local blood flow change in exercise training, release more NO has not been investigated. Finally, low-density lipoprotein inactivates or inhibits EDRF release (1, 12) and chronic exercise decreases plasma low-density lipoprotein level (11, 34). Therefore, a third possibility is that exercise training changes the lipid pattern in favor of EDRF release, which inactivates platelets. Moreover, our results showed that deconditioning reversed the training effects on platelet function back to the pretraining state. This may be explained by the attenuation of blood flow (18) and the reversed alteration of lipoprotein patterns (20), which lower EDRF release after deconditioning.
In conclusion, platelet adhesiveness on fibrinogen-coated surface and ADP-induced platelet aggregation and [Ca2+]i elevation in women during the midfollicular phase can be desensitized by chronic exercise. Moreover, acute exercise-enhanced platelet activity decreases after training. These changes are likely to be mediated by NO. However, these training effects are reversible after deconditioning. Our findings give new insight into the possible protective effects of exercise training against the risk of cardiovascular disease in women.
ACKNOWLEDGEMENTS
The authors thank the volunteers for their enthusiastic participation in this study. They also express their appreciation to Drs. L. Y. C. Wing and H. L. Lee for their advice in the scientific discussion and stastistical assistance.
FOOTNOTES
Address for reprint requests: H.-I. Chen, Dept. of Physiology, National Cheng-Kung University Medical College, Tainan, Taiwan 701, Republic of China (E-mail: hichen{at}mail.ncku.edu.tw).
Received 25 March 1997; accepted in final form 28 July 1997.
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H. Ikarugi, T. Taka, S. Nakajima, T. Noguchi, S. Watanabe, Y. Sasaki, S. Haga, T. Ueda, J. Seki, and J. Yamamoto Norepinephrine, but not epinephrine, enhances platelet reactivity and coagulation after exercise in humans J Appl Physiol, January 1, 1999; 86(1): 133 - 138. [Abstract] [Full Text] [PDF]
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