Introduction
Described as a set of activities that improve one's
health and help one maintain good health, sports or exercise, in
addition to the protective function, serve as a treatment tool
(1–3).
However, despite its ameliorative effects, exercise (which is also
considered to be a controlled catabolic process) leads to the
destruction of muscle and even bone tissue, to a certain extent
(4,5).
Given the mechanisms of immune responses, it can be argued that
tissue injury in the skeletal muscle resulting from exercise paves
the way for activation of immune reactions (6). However, previous studies indicated that a
cytokine response may be observed even after exercise that is not
strenuous (7). The decisive factor
distinguishing elevation of cytokines in response to the immune
response to infections from the post-exercise elevation of
cytokines is the increase observed in tumor necrosis factor-α
(TNF-α) levels in inflammation. In response to exercise, however,
the first cytokine to increase is interleukin (IL)-6, although the
extent of the increase will depend on the type of exercise and the
level of effort exerted (8). The major
reason behind the increase is that muscle injury caused by exercise
serves as a strong signal for IL-6 response (8,9). While
developing appropriate training programs to increase performance in
physical activity, the dietary alternatives in athlete nutrition
are also given greater emphasis (10–12).
However, when strategies for athlete performance and diet are
devised, one of the major issues that requires consideration is the
elimination of factors that may negatively impact the health of an
athlete (12). It was reported that
regular and mild exercise had a favorable effect on immune
responses (13,14), whereas slow-paced and extended exercise
may impair the T-lymphocyte cell functions and natural killer cell
activation, thus altering the cytokine balance and negatively
influencing immune reactions (13,15). In this
context, the association between exercise and immune system becomes
a significant research topic (13).
Consequently, the present study aims to investigate how a 4-week
exercise program affects the serum values of certain cytokines in
individuals performing Taekwondo.
Subjects and methods
Subjects
The current study involved 10 elite healthy male
Taekwondo athletes (mean age, 20.67±0.24 years; mean weight,
65.45±1.69 kg) studying at the Physical Education and Sports High
School of Selcuk University (Konya, Turkey). The athletes were
informed about this study and they participated in the study with
consent. The study protocol was approved by the ethics committee of
Selçuk University's Physical Education and Sports High School. The
study was performed in June 2014.
Four-week Taekwondo exercise program
The athletes attended Taekwondo training every day
of the week for 4 weeks. The exercise program began with a 20-min
warm-up. Following the warm-up, each athlete was involved in a hand
target practice. Spending maximal effort, the athletes practiced
all techniques on the hand target up to complete exhaustion. The
practice was repeated three times and the training session ended
with a cool-down exercise.
Exhaustion exercise (Bruce protocol)
The athletes were worked to exhaustion on two
occasions; once before and once after the 4-week exercise program.
A common clinical exercise assessment is the Bruce protocol, which
was used as the exhaustion test in the current study. The incline
and speed of the treadmill (Cosmed T150 treadmill) were adjusted
every 3 min until the subject was unable to continue (16).
Collection of blood samples from subjects
Blood samples (5 ml) were collected from the
subjects in four rounds: During rest and upon exhaustion before the
4-week exercise program, and again during rest and upon exhaustion
after the 4-week exercise program. Samples were taken from the
forearm vein at 9:00 a.m. on an empty stomach. The samples were
then centrifuged at 2,000 × g for 10 min at 4°C to separate the
sera and stored at −80°C until the time of analysis.
Biochemical analyses
Interferon-γ (IFN-γ) (LOT:121101/A), IL-2
(LOT:122301), IL-6 (LOT:124802) and TNF-α (LOT:121902A) parameters
were analyzed in the sera using ELISA kits which were purchased
from DIAsource ImmunoAssays (Louvain-la-Neuve, Belgium).
Analyses were performed according to the
manufacturer's instructions. The results are presented in units of
IU/ml for IFN-γ and IL-2, and pg/ml for IL-6 and TNF-α.
Statistical analysis
SPSS 16.0 software package (SPSS, Inc., Chicago, IL,
USA) was used for the statistical evaluation of data. Following
calculation of the arithmetic means and standard deviations of all
parameters, repeated measures variance analysis was used to detect
the differences between the measurements taken at different times,
and the least significant difference test was employed to identify
the time period from which the difference arose. P<0.05 was
considered to indicate a statistically significant difference.
Results
The IFN-γ levels of the subjects did not vary before
and after the 4-week exercise program. When compared with the
levels measured prior to exercise, IL-2 levels were found to be
increased subsequent to the 4-week exercise program (P<0.05).
The highest serum IL-6 value was obtained after exercise to
exhaustion prior to initiation of the 4-week program (P<0.05).
The 4-week exercise program resulted in a decrease in IL-6 levels
(P<0.05). In addition, the TNF-α levels before and after the
4-week exercise program did not differ (Table I).
 | Table I.Serum cytokine levels of the
subjects. |
Table I.
Serum cytokine levels of the
subjects.
| Time-point | IFN-γ (IU/ml) | IL-2 (U/ml) | IL-6 (pg/ml) | TNF-α (pg/ml) |
|---|
| Before exercise
program |
|
|
|
|
| Rest | 0.25±0.05 | 0.53±0.02 | 20.58±4.13 | 4.04±0.98 |
|
Exhaustion | 0.29±0.16 | 0.55±0.07 |
25.05±5.03a | 3.43±0.73 |
| After exercise
program |
|
|
|
|
| Rest | 0.26±0.32 |
0.71±0.10a,b |
16.72±4.72a,b | 4.01±1.07 |
|
Exhaustion | 0.27±0.12 |
0.74±0.15a,b |
16.96±4.62a,b | 4.35±1.97 |
Discussion
Levels of IFN-γ and TNF-α did not differ
significantly in the measurements during rest and exhaustion before
and after the 4-week exercise program. The results of studies
regarding the associated between exercise and cytokines are
inconsistent. It has been shown that a 32-week exercise program did
not affect the TNF-α levels in older individuals (17). Consistently, it was reported that acute
aerobic exercise in humans did not alter the cytokine activity of T
cells (18), and that combined
strength and endurance exercise did not change IFN-γ and TNF-α
levels in individuals with type II diabetes (19). However, it was shown that 12 weeks of
swimming exercise elevated IFN-γ and TNF-α levels in mice (20), and that exercise increased the release
of IFN-γ in horses (21).
Additionally, it was demonstrated that intense physical activity
could disrupt immune responses (22),
and that an 8-week swimming exercise program (duration, 150 min per
session; frequency, 6 days per week) reduced IFN-γ and IL-2 levels
in rats (23). Thus, the results of
the studies investigating the association between exercise and
cytokines are inconsistent. These differences may be attributed to
the variances in exercise type, the duration and intensity of
exercise and the subjects, as well as other aspects of
implementation. The IFN-γ and TNF-α levels of the subjects in the
current study remained unaffected before the exercise program and
after the 4-week Taekwondo exercise program. This result is
consistent with the reports of Marques et al (17), LaVoy et al (18) and Touvra et al (19) all of whom noted that the TGF-β1
cytokine was not affected by exercise.
In comparison to the levels measured before the
program, the IL-2 levels of the subjects after the 4-week Taekwondo
exercise program were found to be elevated. Suzuki et al
(24) reported that there was no
increase in the secretion of cytokines following endurance training
in athletes, and it was demonstrated in another study that IL-2
levels of exercised rats remained unchanged (25). Similarly, Kara et al (6) noted that exercise did not cause any
change in the IL-2 levels of individuals performing wrestling as a
sport. The results of these studies are not consistent with the
elevated IL-2 levels that were observed after the 4-week Taekwondo
training program. However, one-hour strenuous training was shown to
have a marginal effect on cytokine production in male rowers
(26) and it was suggested that
exercise in energy-restricted rats may increase IL-2 production
(27). Another study reported elevated
cytokine levels in cyclists (28),
while Petersen et al (29)
demonstrated that exercise significantly increased CD4+
and CD8+ lymphocytes, and cytokine levels in individuals
who received antioxidant supplementation. Another study examining
the interaction between exercise and cytokines revealed that
exercise in a cold environment elevated IL-2 levels (30). All of these reports suggesting that
exercise increases IL-2 levels are consistent with our finding of
elevated IL-2 levels following a 4-week Taekwondo training
program.
The highest serum IL-6 values in the current study
were identified during the exercise to exhaustion test before the
program; the 4-week Taekwondo exercise program appeared to reduce
the IL-6 levels. Although the extent of the increase may vary
depending on the type and physical load of exercise, the first
cytokine to be elevated in response to exercise is IL-6 (31). It was established that plasma IL-6
level showed an ~100-fold increase following long-term and
strenuous exercise (32). Studies
investigating the factors that cause the post-exercise IL-6
elevation showed that the major factors were the length of exercise
and the muscle mass involved in exercise (31,32).
Consequently, it has been proposed that muscle damage caused by
exercise is a warning signal for IL-6 response (31,32). The
abovementioned studies suggest that the increase that was
established in the present study in the IL-6 values, during
exercise to exhaustion, is an expected outcome. Furthermore, Yfanti
et al (33) demonstrated that
exercise to exhaustion elevated IL-6 levels. Notably, in the
current study, however, the 4-week Taekwondo exercise program
suppressed the IL-6 levels. This finding may be novel, as the
studies cited above indicate that the muscular damage in physical
activity causes an increase in IL-6 levels (31–34).
However, our study demonstrates that a 4-week Taekwondo training
program reduced the IL-6 levels, which had become elevated as a
result of exercise to exhaustion. In addition, it has been reported
in a previous study that regular exercise exerts a regulatory
effect on immune responses (18). In
conclusion, the results of the present study indicate that
long-term regular physical activity serves a regulatory function in
immune responses by elevating serum IL-2 levels and suppressing
serum IL-6 levels. Howevever, this exercise program had no affect
on IFN-γ and TNF-α.
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