Physical Activity and TAC across an Adult Lifespan of Men
Physical Activity and TAC across an Adult Lifespan of Men
This is the first study assessing simultaneously the potential influence of current and historical PA on TAC in a large age-heterogeneous population of men. We used three different measures of current PA, a well-validated questionnaire for historical PA together with the two leading measures of TAC, and a set of the most important risk factors for cardiovascular and metabolic diseases, including exercise testing with aerobic fitness measurements. Our results show that both current and historical PA counteract the age-related deterioration of the cardiometabolic diseases risk profile. Nevertheless, this effect is not detectable for TAC. In fact, an adverse relationship between PA/fitness and TAC was observed. Furthermore, in this population of men, TAC did not decline with age and was directly related to overweight/obesity and laboratory markers of metabolic syndrome.
One would expect that systematic PA will lead, in addition to increased physical capacity and protective effects on the cardiovascular system, to greater protective effects of redox compounds on the human system. Available data from the literature discussing the influence of physical exercise on antioxidant capacity are ambiguous and often do not determine precisely the volume of PA. Some studies show the effects of moderate PA on increasing TAC or activity of antioxidant enzymes. For example, both single intense exertion (half-marathon run) and regular endurance training were connected with higher antioxidant capacity. Cesari et al. also found a positive correlation between the concentration of antioxidants in the blood serum and the level of physical performance in the elderly. The results of other studies do not confirm any positive relation between PA and TAC. There is also strong evidence that a high-intensity single exertion or exercise training period may lead to a reduction in antioxidant capacity and an increased concentration of malondialdehyde in blood.
Discrepancies in the available literature are probably associated with the variety of techniques for TAC determination and depend on whether TAC is the result of a single exercise or training process. It is recommended to use at least two methods of determining TAC because of the differences in the tests used for investigation. The TAC-DPPH method analyzes the ability to reduce the radical cation and determines the decrease in absorbance, whereas the TACFRAS assay measures the formed ferrous ions by increased absorbance. DPPH, used in TAC-DPPH assay, is a relatively stable free radical. TAC-FRAS measures the ferric reducing ability of a sample, and there are no free radicals or oxidants applied in the assay. The correlation between the used methods (r = 0.44, P < 0.0001) is higher than among others allowing the assessment of TAC, e.g., FRAP and OXY-ADSORBENT test (Diacron, Italy) (r = 0.22) and FRAP and oxygen radical absorbance capacity (r = 0.35). In the present study, we evaluated the relationship of longterm PA of varying volume to the actual TAC of blood serum by FRAS and DPPH methods. A generally negative correlation was observed between TAC and the current level of PA or fitness. This association was similar across the whole examined adult lifespan. Current PA data were further corroborated with historical PA. Historical PA had a favorable effect on actual BMI, WHR, waist circumference, percentage of body fat, and laboratory markers of metabolic syndrome, including uric acid levels. In contrast, no relationship with actual TAC could be evidenced. Therefore, regular PA and better fitness do not associate with better TAC throughout the adult lifespan of men.
Advancing age and several diseases have been associated with increased oxidative stress and an impaired antioxidant defense system. In our male subjects, age had no influence on TAC. These results, although contradicting the common understanding of free radicals in aging research, are in agreement with a few previous studies. In one population study involving 1600 subjects, a positive relationship was found between antioxidant potential and age in women. In a second study examining 2828 subjects from the Framingham Heart Study, an inverse relationship was found between age and urinary creatinine– indexed levels of 8-epi-PGF2 (a marker of systemic oxidative stress). Therefore, from the present and previous studies involving larger populations, it seems that in free-living relatively healthy subjects, TAC does not decrease with advancing age. Several explanations are plausible for why regular PA and better fitness as well as advancing age had no expected effect on TAC levels. One possible explanation may be based on the concept of hormesis that has been recently extended to the ROS-generating effects of exercise. Moderate exercise has been shown to increase expression of mitochondrial antioxidant enzymes, being recognized per se as an antioxidant. Therefore, one may assume that subjects with regular PA had lower exposition of tissue structures to endogenous oxidants and it is not necessary to maintain high levels of circulating low– molecular weight antioxidants. Uric acid contributes to about half of total plasma antioxidant activity. A regular moderate exercise training program may decrease serum levels of uric acid. Also, in the present study, physically active men were characterized by a lower concentration uric acid. These may explain why regular PA and better fitness were associated with lower TAC values. We did not observe significant differences of serum uric acid levels across the subjects' age. Moreover, aerobic fitness was previously described to decrease the mitochondrial rate of hydrogen peroxide production and to attenuate age-related DNA damage. These can be explanations of similar TAC values in subgroups with different ages noted in our study.
TAC data from our study was directly related to common cardiometabolic risk factor measures. Positive correlations of TAC with blood pressure, indices of overweight/obesity, and laboratory indices of metabolic syndrome together with a negative correlation with HDL-C were found. One plausible explanation for these findings may be related to PA/fitness data. TAC of blood serum, determined by both the FRAS and DPPH methods, reached higher values in participants with lower PA and fitness levels. Less physically active subjects were characterized by higher values of anthropometric overweight/obesity indicators (BMI, WHR, waist circumference, and percentage of body fat) and higher values of blood pressure. Physically active men were characterized by a lower concentration of TG, TC, and uric acid but higher levels of HDL-C. Another explanation may be related to oxidant/antioxidant balance in different diseases. The risk of CHD increases with obesity and physical inactivity. Lower levels of TAC in the course of many diseases may be due to the depletion of the antioxidant barrier as an effect of long-term oxidative stress. In early stages, in the presence of risk factors, the antioxidant defense system may increase its activity in response to sustained oxidative stress. Similar observations have been reported in some earlier studies. Vassalle et al. observed higher TAC in patients with hypertension compared with peers with normal blood pressure. In a population study involving 1600 subjects, a positive relationship was found between antioxidant potential and BMI in women. On the other hand, in one study, an inverse relationship between body fat or central fat and TAC was found in both males and females.
Among laboratory findings of particular interest are the correlations found for uric acid. Uric acid is the strongest antioxidant of human serum, which prevents oxidative inactivation of endothelial enzymes (cyclooxygenase, angiotensin-converting enzyme) and preserves the ability of the endothelium to mediate vascular dilatation in the face of oxidative stress. On the other hand, uric acid is considered to be an independent risk factor of cardiovascular diseases. Hyperuricemia is associated with several components of metabolic syndrome. Uric acid levels have been found to be not correlated or only weakly associated with PA, those associations being mediated by obesity measures. Therefore, the two-directional activity of uric acid, as both a potent antioxidant and a cardiovascular risk factor, requires further studies.
Several shortcomings of the present study should be acknowledged. This is a cross-sectional study performed in either sedentary or endurance-trained men. Patterns of declines may be different in longitudinal comparisons. Our subjects were more physically active and healthy than a random sample would be. Active well-educated subjects in good health are more prone to participate in such studies and especially to undergo exercise testing. Nevertheless, they may overestimate recent and either forget to report or underestimate historical PA. This may explain lower PA reported in early as compared with advanced adulthood. Correlation coefficients of TAC to selected patients characteristics were relatively modest and reached higher values for TAC-FRAS (Table 3). Although both TAC-DPPH and TAC-FRAS measure total antioxidant activity of serum, they reflect somewhat different physiological properties. Some loss of serum antioxidants related to serum deproteinization with acetonitrile in the TAC-DPPH method and higher coefficient of variation across the triplicate measurements noted for TAC-DPPH could explain these differences. We used fasting glucose concentration as the most important measure of CHO metabolism and cardiometabolic risk factor. However, fasting insulin concentration and glycated hemoglobin are other important indicators of insulin sensitivity and CHO metabolism status.
In conclusion, men with disadvantageous risk factor values for cardiovascular and metabolic diseases (BMI, WHR, waist circumference, high blood pressure, low HDL-C) showed higher TAC. PA, both actual and historical, has a positive effect on the elimination of risk factors of cardiovascular disease but does not affect the increase in TAC, as revealed by the FRAS and DPPH methods. Age has no influence on TAC. Therefore, present data strongly suggest that the known beneficial effects of PA alleviating the age-related decline in health and performance do not seem to be directly mediated through increased serum antioxidant status.
Discussion
This is the first study assessing simultaneously the potential influence of current and historical PA on TAC in a large age-heterogeneous population of men. We used three different measures of current PA, a well-validated questionnaire for historical PA together with the two leading measures of TAC, and a set of the most important risk factors for cardiovascular and metabolic diseases, including exercise testing with aerobic fitness measurements. Our results show that both current and historical PA counteract the age-related deterioration of the cardiometabolic diseases risk profile. Nevertheless, this effect is not detectable for TAC. In fact, an adverse relationship between PA/fitness and TAC was observed. Furthermore, in this population of men, TAC did not decline with age and was directly related to overweight/obesity and laboratory markers of metabolic syndrome.
One would expect that systematic PA will lead, in addition to increased physical capacity and protective effects on the cardiovascular system, to greater protective effects of redox compounds on the human system. Available data from the literature discussing the influence of physical exercise on antioxidant capacity are ambiguous and often do not determine precisely the volume of PA. Some studies show the effects of moderate PA on increasing TAC or activity of antioxidant enzymes. For example, both single intense exertion (half-marathon run) and regular endurance training were connected with higher antioxidant capacity. Cesari et al. also found a positive correlation between the concentration of antioxidants in the blood serum and the level of physical performance in the elderly. The results of other studies do not confirm any positive relation between PA and TAC. There is also strong evidence that a high-intensity single exertion or exercise training period may lead to a reduction in antioxidant capacity and an increased concentration of malondialdehyde in blood.
Discrepancies in the available literature are probably associated with the variety of techniques for TAC determination and depend on whether TAC is the result of a single exercise or training process. It is recommended to use at least two methods of determining TAC because of the differences in the tests used for investigation. The TAC-DPPH method analyzes the ability to reduce the radical cation and determines the decrease in absorbance, whereas the TACFRAS assay measures the formed ferrous ions by increased absorbance. DPPH, used in TAC-DPPH assay, is a relatively stable free radical. TAC-FRAS measures the ferric reducing ability of a sample, and there are no free radicals or oxidants applied in the assay. The correlation between the used methods (r = 0.44, P < 0.0001) is higher than among others allowing the assessment of TAC, e.g., FRAP and OXY-ADSORBENT test (Diacron, Italy) (r = 0.22) and FRAP and oxygen radical absorbance capacity (r = 0.35). In the present study, we evaluated the relationship of longterm PA of varying volume to the actual TAC of blood serum by FRAS and DPPH methods. A generally negative correlation was observed between TAC and the current level of PA or fitness. This association was similar across the whole examined adult lifespan. Current PA data were further corroborated with historical PA. Historical PA had a favorable effect on actual BMI, WHR, waist circumference, percentage of body fat, and laboratory markers of metabolic syndrome, including uric acid levels. In contrast, no relationship with actual TAC could be evidenced. Therefore, regular PA and better fitness do not associate with better TAC throughout the adult lifespan of men.
Advancing age and several diseases have been associated with increased oxidative stress and an impaired antioxidant defense system. In our male subjects, age had no influence on TAC. These results, although contradicting the common understanding of free radicals in aging research, are in agreement with a few previous studies. In one population study involving 1600 subjects, a positive relationship was found between antioxidant potential and age in women. In a second study examining 2828 subjects from the Framingham Heart Study, an inverse relationship was found between age and urinary creatinine– indexed levels of 8-epi-PGF2 (a marker of systemic oxidative stress). Therefore, from the present and previous studies involving larger populations, it seems that in free-living relatively healthy subjects, TAC does not decrease with advancing age. Several explanations are plausible for why regular PA and better fitness as well as advancing age had no expected effect on TAC levels. One possible explanation may be based on the concept of hormesis that has been recently extended to the ROS-generating effects of exercise. Moderate exercise has been shown to increase expression of mitochondrial antioxidant enzymes, being recognized per se as an antioxidant. Therefore, one may assume that subjects with regular PA had lower exposition of tissue structures to endogenous oxidants and it is not necessary to maintain high levels of circulating low– molecular weight antioxidants. Uric acid contributes to about half of total plasma antioxidant activity. A regular moderate exercise training program may decrease serum levels of uric acid. Also, in the present study, physically active men were characterized by a lower concentration uric acid. These may explain why regular PA and better fitness were associated with lower TAC values. We did not observe significant differences of serum uric acid levels across the subjects' age. Moreover, aerobic fitness was previously described to decrease the mitochondrial rate of hydrogen peroxide production and to attenuate age-related DNA damage. These can be explanations of similar TAC values in subgroups with different ages noted in our study.
TAC data from our study was directly related to common cardiometabolic risk factor measures. Positive correlations of TAC with blood pressure, indices of overweight/obesity, and laboratory indices of metabolic syndrome together with a negative correlation with HDL-C were found. One plausible explanation for these findings may be related to PA/fitness data. TAC of blood serum, determined by both the FRAS and DPPH methods, reached higher values in participants with lower PA and fitness levels. Less physically active subjects were characterized by higher values of anthropometric overweight/obesity indicators (BMI, WHR, waist circumference, and percentage of body fat) and higher values of blood pressure. Physically active men were characterized by a lower concentration of TG, TC, and uric acid but higher levels of HDL-C. Another explanation may be related to oxidant/antioxidant balance in different diseases. The risk of CHD increases with obesity and physical inactivity. Lower levels of TAC in the course of many diseases may be due to the depletion of the antioxidant barrier as an effect of long-term oxidative stress. In early stages, in the presence of risk factors, the antioxidant defense system may increase its activity in response to sustained oxidative stress. Similar observations have been reported in some earlier studies. Vassalle et al. observed higher TAC in patients with hypertension compared with peers with normal blood pressure. In a population study involving 1600 subjects, a positive relationship was found between antioxidant potential and BMI in women. On the other hand, in one study, an inverse relationship between body fat or central fat and TAC was found in both males and females.
Among laboratory findings of particular interest are the correlations found for uric acid. Uric acid is the strongest antioxidant of human serum, which prevents oxidative inactivation of endothelial enzymes (cyclooxygenase, angiotensin-converting enzyme) and preserves the ability of the endothelium to mediate vascular dilatation in the face of oxidative stress. On the other hand, uric acid is considered to be an independent risk factor of cardiovascular diseases. Hyperuricemia is associated with several components of metabolic syndrome. Uric acid levels have been found to be not correlated or only weakly associated with PA, those associations being mediated by obesity measures. Therefore, the two-directional activity of uric acid, as both a potent antioxidant and a cardiovascular risk factor, requires further studies.
Several shortcomings of the present study should be acknowledged. This is a cross-sectional study performed in either sedentary or endurance-trained men. Patterns of declines may be different in longitudinal comparisons. Our subjects were more physically active and healthy than a random sample would be. Active well-educated subjects in good health are more prone to participate in such studies and especially to undergo exercise testing. Nevertheless, they may overestimate recent and either forget to report or underestimate historical PA. This may explain lower PA reported in early as compared with advanced adulthood. Correlation coefficients of TAC to selected patients characteristics were relatively modest and reached higher values for TAC-FRAS (Table 3). Although both TAC-DPPH and TAC-FRAS measure total antioxidant activity of serum, they reflect somewhat different physiological properties. Some loss of serum antioxidants related to serum deproteinization with acetonitrile in the TAC-DPPH method and higher coefficient of variation across the triplicate measurements noted for TAC-DPPH could explain these differences. We used fasting glucose concentration as the most important measure of CHO metabolism and cardiometabolic risk factor. However, fasting insulin concentration and glycated hemoglobin are other important indicators of insulin sensitivity and CHO metabolism status.
In conclusion, men with disadvantageous risk factor values for cardiovascular and metabolic diseases (BMI, WHR, waist circumference, high blood pressure, low HDL-C) showed higher TAC. PA, both actual and historical, has a positive effect on the elimination of risk factors of cardiovascular disease but does not affect the increase in TAC, as revealed by the FRAS and DPPH methods. Age has no influence on TAC. Therefore, present data strongly suggest that the known beneficial effects of PA alleviating the age-related decline in health and performance do not seem to be directly mediated through increased serum antioxidant status.
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