- Email: [email protected]
Three months of Tai Chi Chuan exercise can reduce serum triglyceride and endothelin-1 in the elderly
Complementary Therapies in Clinical Practice 19 (2013) 204e208
Contents lists available at SciVerse ScienceDirect
Complementary Therapies in Clinical Practice journal homepage: www.elsevier.com/locate/ctcp
Three months of Tai Chi Chuan exercise can reduce serum triglyceride and endothelin-1 in the elderly Wan-An Lu a, b, Cheng-Deng Kuo a, * a b
Laboratory of Biophysics, Department of Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Cultural Asset and Reinvention, Fo-Guang University, Yilan, Taiwan
a b s t r a c t Keywords: Tai Chi Chuan Endothelin-1 Exercise Lipid Triglyceride
Endothelin-1 (ET-1) and circulating hormones play important roles in maintaining cardiovascular function. Tai Chi Chuan (TCC) is known to be good for health. This study evaluated the effect of 3 months of TCC training on serum ET-1, blood lipids, and other circulating hormones in the elderly. Twenty-two TCC trainees and 20 normal subjects were included in this study. The TCC trainees practiced classical Yang’s TCC 40 min per session, 7 times per week, for 3 months. The hemodynamics and serum ET-1 and lipids before and after TCC were compared. The percentage change in serum ET-1 and triglyceride (TG) were decreased significantly after 3 months of TCC, as compared to the control group. In the TCC group, the percentage decrease in serum ET-1 and TG after 3 months of TCC were 36.6 (63.4 to 14.0)% and 22.5 (30.7 to 4.9)%, respectively. TCC exercise for 3 months can reduce serum ET-1 and TG in the elderly. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction Endothelial function is a balance between vascular cell protectors and risk factors. Under physiological conditions, vascular endothelium has antithrombogenic potential. While improvement in nitric oxide (NO) vasodilator function has been less frequently found in healthy subjects, a higher level of training may lead to improvement. Exercise training may improve endothelial function by up-regulating endothelial nitric oxide synthase (eNOS) protein expression and phosphorylation. Clinical studies have shown a significant improvement in endothelial dysfunction following lowering of serum cholesterol levels, infusion of nitric oxide donors such as L-arginine and exercise training [22]. Endothelin-1 (ET-1) belongs to a family of potent vasoconstrictor peptides. It was isolated from the culture supernatant of porcine aortic endothelial cell in 1988 by Tomoh Masaki and associates [45]. ET-1 is produced from the biologically inactive 38amino acid intermediate, big ET-1, via cleavage by ET-converting enzyme [44]. Some studies have shown that ET-1 may be involved in the pathogenesis of hypertension and atherosclerosis [24,40]. Elevated plasma level of ET-1 has been observed in patients * Corresponding author. Laboratory of Biophysics, Department of Research and Education, Taipei Veterans General Hospital, No. 210, Sec. 2, Shipai Road, Taipei 112, Taiwan. Tel.: þ886 2 28757745; fax: þ886 2 28710773. E-mail address: [email protected] (C.-D. Kuo). 1744-3881/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ctcp.2013.06.007
with chronic heart failure [15], essential hypertension [17], atherosclerosis [24], chronic renal failure [34], myocardial infarction [30] and diabetes [36]. Takahashi et al. [36] pointed out that circulating ET-1 play an important role as a paracrine factor in the metabolism of blood glucose by modulating insulin levels. One study has showed that both increased plasma ET-1, decreased plasma NOx and diffuse atherosclerosis may cause the decrease in heart rate variability by affecting myocardial blood flow in patients with coronary slow flow [31]. Furthermore, circulating aldosterone may directly affect vascular tone and may be part of the vasoconstriction response [32]. Tostes et al. [38] suggested that renal damage in aldosterone-dependent hypertension is associated with inflammatory processes that are mediated in part via ET-1. Thus, ET-1 and some circulating hormones are involved in the maintenance of the homeostasis of the cardiovascular system. Tai Chi Chuan (TCC) has been shown to be beneficial to the cardiopulmonary function [18,20] balance [42] and strength [20] of the subjects practicing it regularly. TCC is one kind of moving meditations that can reduce tension, anxiety, and mood disturbance [13]. It has also been shown that the short-term effect of TCC was to enhance the vagal modulation and tilt the sympathovagal balance towards deceased sympathetic modulation in older persons [28]. Recent studies have also demonstrated that TCC may be a useful treatment for fibromyalgia [41,46]. Maeda and associates [29] have shown that regular aerobicendurance exercise can reduce plasma ET-1 concentration which
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
may have beneficial effects on the cardiovascular system in older humans. Lewczuk and colleagues [25] demonstrated that ET-1 concentration in plasma is decreased after cycling in healthy men. Since 3 months of TCC training can improve the pulmonary function, glucose availability, blood lipid profile, cytokine production and vagal modulation in elderly subjects [27], it is interesting to know the effects of 3 months of TCC on the cardiovascular system and some circulating hormones of the subjects practicing it. Thus the aim of this study was to examine the effect of 3 months of TCC training on the serum levels of ET-1, aldosterone, fasting serum insulin, lipid profiles and hemodynamics in the elderly. 2. Methods 2.1. Subjects TCC trainees recruited from a TCC training center in Taiwan. The TCC trainees received 3 months of Yang’s TCC training for 1 h each time, 7 times per week. Healthy subjects without TCC experience and smoking history who were recruited from the community were included in this study. All subjects included in this study were over 50 years of age, had no previous experience with TCC, had normal lifestyles, and were capable of daily activities without limitations. Subjects who had major cardiopulmonary disease or were on regular medicine for diabetes mellitus, hypertension, renal or liver disease were not included in the study. The Institute Review Board of the hospital has approved this study, and the procedure was fully explained to the study subjects before the study. The written informed consent was obtained from every participant prior to the study. Before measurements were taken, each subject took a rest in supine position for 5 min. The arterial blood pressure measurement (Omron, HEM-770A) was performed on both controls and TCC trainees before and after 3 months of TCC. The hemodynamic data such as systolic blood pressure (SBP), diastolic blood pressure (DBP), mean arterial blood pressure (MABP), and pulse pressure (PP) were obtained from every subject in the control group and TCC group before TCC training and after 3 months of TCC training. The TCC trainee exercised TCC once per day for 3 months. The subjects included in this study were requested to not take any caffeinated or alcoholic beverages for at least 24 h prior to the study, and they were also requested to not exercise on the day of study. The hemodynamic data were measured after the subject had rested quietly for 5 min, and then a blood sample was withdrawn for later assay. After that, the TCC trainee was advised to exercise the classical Yang’s TCC for 40 min. Each session of Yang’s TCC included a 10-min warm-up exercise (lower back and hamstring stretching, gentle calisthenics, and balance training), a 20-min TCC exercise, and a 10-min cool-down exercise. Each set of Yang’s TCC consists of 64 successive postures. While practicing TCC, the TCC trainee kept the same pace in exercising the different postures of TCC in a sequence according to a pre-recorded tape to ensure that the same pace and sequence of postures were followed. After 3 months of TCC training, which consisted of 40-min exercise per session, 7 times per week, a second hemodynamic measurements and blood sampling were performed using the same procedure. All procedures were performed in a bright and quiet room with a standardized temperature of 24e25 C and a standardized humidity of 54e55%. 2.2. Biochemistry and hormone analysis The biochemistry assays for the quantitative measurements of total cholesterol (TC) (Ektachem Clinical Chemistry Slides, Johnson & Johnson), high-density lipoprotein-cholesterol (HDL-C)
205
(INTEGRA 700, Roche), low-density lipoprotein-cholesterol (LDL-C) (INTEGRA 700, Roche), triglyceride (TG), and fasting blood sugar (FBS) (Ektachem Clinical Chemistry Slides, Johnson & Johnson) were performed on the blood sample obtained from each subject. The radioimmunoassay for the quantitative measurement of insulin (DIAsource INS-IRMA Kit, DIAsource ImmunoAssays SA) and aldosterone (DSL-8600 ACTIVE Aldosterone Coated-Tube Radioimmunoassay Kit, Diagnostic Systems Laboratories, Inc. USA), and the enzyme immunoassay for the quantitative determination of ET-1 (Kit Lot 998C Abl./Exp. 100908. CAT. No. BI-20052, Biomedica Medizinprodukte GmbH & Co. KG, Divischgasse 4, A-1210 Wien, Austria) were also performed on the blood sample from each subject. After 3 months of TCC training, the hemodynamic data, blood biochemistry and serum hormone levels of the TCC trainees were repeated using the same methodology. 2.3. Statistical analysis The ManneWhitney rank sum test (SigmaStat statistical software, SPSS Inc., Chicago, Illinois, USA) was employed to compare the baseline general characteristics, hemodynamics, blood biochemistry, lipid profile and circulating hormone levels between the TCC and control groups. All data are presented as median (25%e 75%). A p < 0.05 is considered statistically significant. To quantify the effect of 3 months of TCC training on the general characteristic, hemodynamics, lipid profile, and hormones in the elderly, the percentage changes in these parameters before and after 3 months of TCC training in each subject were calculated by using the following formula:
%X ¼
h
X3month Xbefore
. i Xbefore 100;
where X denotes the parameter under consideration. Comparisons of the percentage changes in these parameters between the controls and TCC trainees were performed by using the ManneWhitney rank sum test. Correlation analysis was performed to analyze the relationship among the percentage changes in the parameters between before and after 3 months of TCC training. 3. Results 3.1. General characteristics Twenty-two TCC trainees and twenty normal controls were included in this study. There was no significant difference in the baseline characteristics between normal controls and TCC trainees before TCC Training (Table 1). 3.2. Effect of TCC on hormones and lipid profile Table 2 shows the comparison of the percentage changes in general characteristic, hemodynamics, lipid profile and hormone levels between control and TCC groups after 3 months of TCC Training. There were significant decreases in serum level of TG and ET-1 after 3 months of TCC in the TCC group, as compared to those of the control group. In the TCC group, the percentage decrease in the serum levels of ET-1 and TG after 3 months of TCC training were 36.6 (63.4 to 14.0)% and 22.5 (30.7 to 4.9)%, respectively; whereas the percentage increase in the serum levels of insulin and aldosterone after 3 months of TCC training were 95.3 (13.8e212.2)% and 40.0 (18.2 to 169.2)%, respectively. Correlation analysis showed that there were no correlations either between %TG and %ET-1 or between %ET-1 and other parameters in the TCC group after 3 months of TCC.
206
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
Table 1 Comparison of characteristics, hemodynamic measures, blood biochemistry, lipid profile and hormone levels between controls and TCC trainees before TCC training.
Age (years) Gender (M/F) Body weight (Kg) Body height (cm) BMI (kg/m2) Waist (cm) SBP (mmHg) DBP (mmHg) MABP (mmHg) PP (mmHg) TG (mg/dl) TC (mg/dl) LDL-C (mg/dl) HDL-C (mg/dl) TC/HDL-C LDL-C/HDL-C FBS (mg/dl) ET-1 (fmol/ml) Insulin (ng/ml) Aldosterone (pg/ml)
Controls (n ¼ 20)
TCC trainees (n ¼ 22)
P value
52 (45e55) 9/11 65 (61e73) 163 (160e168) 23.8 (22.3e26.4) 84.9 (76.2e89.6) 119 (106e127) 68 (58e74) 82 (75e92) 49 (42e55) 138 (115e206) 176 (152e198) 108 (80e124) 46 (42e51) 3.78 (3.03e4.63) 2.37 (1.56e2.79) 92.0 (82.5e104.0) 0.47 (0.36e0.78) 13.6 (8.1e19.2) 64.9 (54.2e103.5)
56 (51e61) 12/10 64 (55e71) 166 (158e170) 23.5 (21.1e24.6) 83.7 (73.7e90.9) 122 (113e129) 71 (64e79) 89 (80e92) 52 (40e59) 124 (80e144) 173 (159e192) 107 (97e123) 52 (45e63) 3.39 (2.79e3.94) 2.29 (1.50e2.61) 90.5 (74.0e159.0) 0.56 (0.41e1.43) 5.5 (2.2e20.7) 60.3 (55.9e73.1)
0.235 0.537 0.569 0.638 0.247 0.574 0.270 0.205 0.198 0.711 0.199 0.990 0.870 0.107 0.284 0.417 0.890 0.195 0.170 0.097
All data are medians (25 percentile w 75 percentile). BMI ¼ body mass index; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; MABP ¼ mean arterial blood pressure; PP ¼ pulse pressure; TG ¼ triglycerides; TC ¼ total cholesterol; LDL-C ¼ low-density lipoproteincholesterol; HDL-C ¼ high-density lipoprotein-cholesterol; TC/HDL-C ¼ ratio of TC over HDL-C; LDL-C/HDL-C ¼ ratio of LDL-C over HDL-C; FBS ¼ fasting blood sugar; ET-1 ¼ Endothelin-1.
4. Discussion Since TCC is a well-known low-intensity and low-impact aerobic exercise, we conducted this study to evaluate the effect of 3 months of TCC training on the lipid profile, endocrine hormone in the elderly people. We found that TCC exercise for 3 months can reduce not only the serum level of TG, but also the serum level of ET-1 in
Table 2 Comparison of percentage changes in general characteristics, hemodynamic measures, blood biochemistry, lipid profile and hormone levels between controls and TCC trainees after 3 months of TCC training.
%BW %BMI %Waist %SBP %DBP %MABP %PP %TG %TC %LDL-C %HDL-C %TC/HDL-C %LDL-C/HDL-C %FBS %ET-1 %Insulin %Aldosterone
Controls (n ¼ 20)
TCC trainees (n ¼ 22)
P value
0.0 0.0 0.1 0.5 8.6 3.5 9.7 0.5 5.0 9.6 6.1 6.2 1.0 6.4 6.3 26.3 4.6
0.0 0.0 0.0 0.9 3.9 1.1 13.9 22.5 2.6 8.3 5.0 3.9 2.2 5.2 36.6 95.3 40.0
0.057 0.115 0.588 0.856 0.513 0.843 0.995 0.023 0.146 0.576 0.990 0.990 0.910 0.734 0.001 0.505 0.148
(0.7 to 1.5) (0.7 to 1.5) (1.3 to 2.6) (10.1 to 7.1) (6.3 to 15.7) (3.9 to 11.6) (15.4 to 4.3) (17.1 to 32.7) (0.5 to 10.3) (4.9 to 30.1) (14.2 to 15.5) (9.9 to 4.2) (9.2 to 12.7) (19.0 to 20.0) (17.5 to 62.0) (50.9 to 288.5) (29.0 to 78.8)
(1.3 to 0.0) (1.3 to 0.0) (1.2 to 0.0) (8.7 to 6.5) (3.9 to 11.1) (5.4 to 7.2) (18.6 to 2.1) (30.7 to 4.9) (9.9 to 11.6) (9.0 to 24.2) (0.3 to 10.0) (13.2 to 2.9) (9.4 to 16.9) (7.4 to 14.3) (63.4 to 14.0) (13.8 to 212.2) (18.2 to 169.2)
All data are medians (25 percentilew75 percentile). %BW ¼ % change in body weight; %BMI ¼ % change in body mass index; %SBP ¼ % change in systolic blood pressure; %DBP ¼ % change in diastolic blood pressure; % MABP ¼ % change in mean arterial blood pressure; %PP ¼ % change in pulse pressure; %TG ¼ % change in triglycerides; %TC ¼ % change in total cholesterol; %LDLC ¼ % change in low-density lipoprotein-cholesterol; %HDL-C ¼ % change in highdensity lipoprotein-cholesterol; %TC/HDL-C ¼ % change in ratio of TC over HDL-C; %LDL-C/HDL-C ¼ % change in ratio of LDL-C over HDL-C; %FBS ¼ % change in fasting blood sugar; %ET-1 ¼ % change in Endothelin-1.
the elderly. Our result paralleled the results of previous studies that regular aerobic-endurance exercise reduces plasma ET-1 concentration in older people [29], and that ET-1 concentration in plasma is decreased after cycling in healthy men. [25]. Therefore, TCC exercise may be beneficial to the health of elderly people, because the reduction in plasma ET-1 concentration may have beneficial effects on the cardiovascular system in older persons [29]. Channer and associates [2] have shown that an 8-week, lowintensity TCC program was effective for reducing blood pressure in patients with acute myocardial infarction. Lai et al. [18] found that regular TCC can delay the decline of cardiovascular function in the elderly individuals. Lan et al. [20] also demonstrated that a 12month TCC program was effective to improve cardiorespiratory function, muscle strength, and flexibility in the elderly. Lan et al. [19] later showed that TCC could significantly increase the VO2peak and peak work rate in patients with coronary artery bypass surgery. Similarly, Hong et al. [10] reported that long-term regular TCC exercise has favorable effects on the promotion of balance control, flexibility, and cardiovascular fitness in the elderly. Jahnke et al. [12] further pointed out that the strongest and most consistent evidence is demonstrated for effects on bone health, cardiopulmonary fitness, some aspects of physical function, quality of life, selfefficacy, and factors related to prevention of falls. From these studies, it is clear that TCC is a suitable conditioning exercise that can improve the cardiorespiratory function of the elderly. Camsan et al. [1] showed that the baseline ET-1 concentrations of the control subjects were lower than that of patients with slow coronary flow (SCF) and that this difference increased after exercise because post-exercise ET-1 concentrations were significantly higher than baseline in patients with SCF whereas a reduction in the ET-1 concentrations was observed in control subjects. In the present study, we found that 3 months of regular TCC exercise could significantly decrease serum level of ET-1 in the TCC group. Since endothelial dysfunction is associated with advancing age [35] and patients with chronic heart failure [16] and since circulating serum ET-1 is a potent vasoconstrictor that originates mainly from the vascular endothelial cells [5], it is possible that the production of ET-1 by the vascular endothelial cells of elderly subjects in this study was decreased by the remodeling of the vascular endothelium due to regular TCC exercise. Our study seemed to be in accordance with previous studies that aerobic exercise training can reduce plasma ET-1 concentration in older women [29], and that post-exercise ET-1 concentrations were significantly reduced in the control subjects [35]. Since plasma level of ET-1 correlates with disease severity [47], the reduction in serum level of ET-1 after 3 months of TCC suggested that TCC exercise may be beneficial to the cardiovascular system of the elderly subjects. In the present study, we found that regular TCC exercise could significantly increase the fasting serum insulin and aldosterone levels in the elderly. Kirwan et al. [14] have shown that one week of vigorous exercise training can induce significant improvements in insulin action in type 2 diabetes, including increased peripheral insulin sensitivity and responsiveness as well as enhanced suppression of hepatic glucose production. A direct relationship among plasma aldosterone levels, insulin resistance, and hyperinsulinemia exists in hypertensive patients [4]. Insulin also modulates ET-1 levels in vivo [43]. Since ET-1 may impair insulin sensitivity [6], the increased serum insulin after 3 months of regular TCC exercise may be related to the diminished sensitivity and responsiveness of insulin, and the decreased plasma level of ET-1 in the elderly subjects after TCC exercise. It has been shown that 12-month Yang TCC training program decreased triglyceride [21]. Tsai et al. [39] also showed that 12week Tai Chi Chuan exercise resulted in favorable lipid profile changes. Chen et al. [3] demonstrated that Tai Chi exercise practiced
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
by patients who are obese and have type 2 diabetes is efficient and safe when supervised by professionals and helps improve BMI and lipid profile including triglyceride and high density lipoprotein cholesterol. By using quantitative coronary angiography, Hodis et al. [9] further showed that the progression of mild-to-moderate lesions are among the most significant predictors of clinical coronary events, and that lowering triglyceride-rich lipoproteins reduces progression of coronary artery disease to the same degree as the lowering of LDL-cholesterol. Similarly, we found in this study that TCC for 3 months can lower the serum level of TG in the elderly. Thus, TCC for 3 months should be good for the health of the elderly people. Garcés et al. [7] showed that obese 6- to 8-year-old children have elevated levels of TG and insulin and lower levels of HDL-C, which are similar to those found in obese adults. Epidemiologic studies indicated that serum TG level is an important independent risk indicator of coronary heart disease [11,33]. Endogenous hypertriglyceridemia was shown to be the commonly encountered hyperlipidemia in clinical practice, which is characterized by elevation of TG and usually normal levels of TC. [23,37]. The diets which is high in carbohydrate may result in disorder of TG metabolism (excessive production and/or deficient clearance) [26]. Thus, the reduction in serum TG level after 3 months of TCC training indicated that TCC exercise is good for health as far as lipidemia is concerned. Hayakawa et al. [8] pointed out that the mechanisms involved in the endothelial dysfunction induced by hypercholesterolaemia and oxidized lipids may differ among vascular beds. We found no correlations either between %TG and %ET-1 or between %ET-1 and other parameters in the TCC group after 3 months of TCC. The lack of correlation between %TG and %ET-1 suggested that the lowering of serum TG and ET-1 by 3 months of TCC might be via different mechanisms. Also, the lack of correlation between serum ET-1 and other parameters examined in this study suggested that the mechanism leading to the lowering of serum ET1 by 3 months of TCC might not be related to blood sugar, insulin, aldosterone, etc. Further studies are necessary in the future to elucidate the mechanisms responsible for the lowering of ET-1 and TG by 3 months of TCC. The use of an objective measure of physical health and fitness is a major strength of this study as it provides a precise and accurate estimate of the effect of TCC on the TCC trainees. The detailed measures available allowed us to test for the associations among potential determinants such as cardiovascular function and the endocrine activity in the TCC program and allowed adequate exploration of the role of potential confounders in the physical activity of sport medicine. The finding of reduction in the serum levels of endothelin-1 by 3 months of TCC gives supportive evidence to the general notion that TCC is beneficial to the cardiopulmonary function of the subjects practicing it regularly. In conclusion, three months of TCC exercise training can reduce the serum levels of ET-1 and TG in the elderly, and that the lowering of serum TG and ET-1 by 3 months of TCC might be via different mechanisms. TCC for 3 months might be good to health of the elderly subjects as far as cardiovascular diseases are concerned. Conflict of interest statement We certify that all authors have no financial and personal relationships with other people or organizations that could inappropriately influence (bias) their work. Acknowledgments This study was supported by project V91-365-1 of Taipei Veterans General Hospital, project NSC96-2320-B-075-002-MY2 of the National Science Council, and project CCMP97-RD-047 of the
207
Committee on Chinese Medicine and Pharmacy, Department of Health, Taipei, TAIWAN. References [1] Camsarl A, Pekdemir H, Cicek D, Polat G, Akkus MN, Döven O, et al. Endothelin-1 and nitric oxide concentrations and their response to exercise in patients with slow coronary flow. Circ J 2003;67:1022e8. [2] Channer KS, Barrow D, Barrow R, Osborne M, Ives G. Changes in hemodynamic parameters following Tai Chi Chuan and aerobic exercise in patients recovering from acute myocardial infarction. Postgrad Med J 1996;72:349e51. [3] Chen SC, Ueng KC, Lee SH, Sun KT, Lee MC. Effect of T’ai Chi exercise on biochemical profiles and oxidative stress indicators in obese patients with type 2 diabetes. J Altern Complement Med 2010;16:1153e9. [4] Colussi G, Catena C, Lapenna R, Nadalini E, Chiuch A, Sechi LA. Insulin resistance and hyperinsulinemia are related to plasma aldosterone levels in hypertensive patients. Diabetes Care 2007;30:2349e54. [5] Dietmann A, Lackner P, Helbok R, Spora K, Issifou S, Lell B, et al. Opposed circulating plasma levels of endothelin-1 and C-type natriuretic peptide in children with Plasmodium falciparum malaria. Malar J 2008;7:253e9. [6] Ferri C, Carlomagno A, Coassin S, Baldoncini R, Faldetta MRC, Laurenti O, et al. Circulating endothelin-1 levels increase during euglycemic hyperinsulinemic clamp in lean NIDDM men. Diab Care 1995;18:226e33. [7] Garcés C, Gutierrez-Guisado J, Benavente M, Cano B, Viturro E, Ortega H, et al. Obesity in Spanish schoolchildren: relationship with lipid profile and insulin resistance. Obes Res 2005;13:959e63. [8] Hayakawa H, Raij L. Relationship between hypercholesterolaemia, endothelial dysfunction and hypertension. J Hypertens 1999;17:611e9. [9] Hodis HN, Mack WJ, Krauss RM, Alaupovic P. Pathophysiology of triglyceriderich lipoproteins in atherothrombosis: clinical aspects. Clin Cardiol 1999;22: II15e20. [10] Hong Y, Li JX, Robinson PD. Balance control, flexibility, and cardiorespiratory fitness among older Tai Chi practitioners. Br J Sports Med 2000;34:29e34. [11] Jacobson TA, Miller M, Schaefer EJ. Hypertriglyceridemia and cardiovascular risk reduction. Clin Ther 2007;29:763e77. [12] Jahnke R, Larkey L, Rogers C, Etnier J, Lin F. A comprehensive review of health benefits of qigong and tai chi. Am J Health Promot 2010;24:e1e25. [13] Jin P. Efficacy of Tai Chi, brisk walking, meditation, and reading in reducing mental and emotional stress. J Psychosom Res 1992;36:361e70. [14] Kirwan JP, Solomon TP, Wojta DM, Staten MA, Holloszy JO. Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 2009;297:E151e6. [15] Kjaer A, Appel J, Hildebrandt P, Petersen CL. Basal and exercise-induced neuroendocrine activation in patients with heart failure and in normal subjects. Eur J Heart Fail 2004;6:29e39. [16] Kobayashi N, Tsuruya Y, Iwasawa T, Ikeda N, Hashimoto S, Yasu T, et al. Exercise training in patients with chronic heart failure improves endothelial function predominantly in the trained extremities. Circ J 2003;67:505e10. [17] Kohno M, Yasunari K, Murakawa KI, Yokokawa K, Horio T, Fukui T, et al. Plasma immunoreactive endothelin in essential hypertension. Am J Med 1990;88:614e8. [18] Lai JS, Lan C, Wong MK, Teng SH. Two-year trends in cardiorespiratory function among older Tai Chi Chuan practitioners and sedentary subjects. J Am Geriatr Soc 1995;43:1222e7. [19] Lan C, Chen SY, Lai JS, Wong MK. The effect of Tai Chi on cardiorespiratory function in patients with coronary artery bypass surgery. Med Sci Sports Exerc 1999;31:634e8. [20] Lan C, Lai JS, Chen SY, Wong MK. 12-month Tai Chi training in the elderly: its effect on health fitness. Med Sci Sports Exerc 1998;30:345e51. [21] Lan C, Su TC, Chen SY, Lai JS. Effect of T’ai chi chuan training on cardiovascular risk factors in dyslipidemic patients. J Altern Complement Med 2008;14:813e9. [22] Laroia ST, Ganti AK, Laroia AT, Tendulkar KK. Endothelium and the lipid metabolism: the current understanding. Int J Cardiol 2003;88:1e9. [23] Lee M, Kim JQ, Kim J, Oh H, Park M. Studies on the plasma lipid profiles, and LCAT and CETP activities according to hyperlipoproteinemia phenotypes (HLP). Atherosclerosis 2001;159:381e9. [24] Lerman A, Edwards BS, Hallett JW, Heublein DM, Sandberg Jr SM, Burnett JC. Circulating and tissue endothelin immunoreactivity in advanced atherosclerosis. N Engl J Med 1991;325:997e1001. [25] Lewczuk P, Söhnchen N, Kele H, Reimers CD, Ehrenreich H. Endothelin-1 concentration in plasma is increased after jogging but decreased after cycling in healthy men. Clin Exp Med 2003;2:166e70. [26] Liu BW. Study on the pathogenesis of endogenous hypoertriglyceridemia. Chin J Atheroscler 1993;1:67e9. [27] Lu WA, Kuo CD. Effect of 3-month Tai Chi Chuan on heart rate variability, blood lipid and cytokine profiles in middle-aged and elderly subjects. Int J Gerontol 2012;6:267e72. [28] Lu WA, Kuo CD. The effect of Tai Chi Chuan on the autonomic nervous modulation in older persons. Med Sci Sports Exerc 2003;35:1972e6. [29] Maeda S, Tanabe T, Miyauchi T, Otsuki T, Sugawara J, Iemitsu M, et al. Aerobic exercise training reduces plasma endothelin-1 concentration in older women. J Appl Physiol 2003;95:336e41.
208
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
[30] Omland T, Lie RT, Aakvaag A, Aarsland T, Dickstein K. Plasma endothelin determination as a prognostic indicator of 1-year mortality after acute myocardial infarction. Circulation 1994;89:1573e9. [31] Pekdemir H, Cicek D, Camsari A, Akkus MN, Cin VG, Doven O, et al. The relationship between plasma endothelin-1, nitric oxide levels, and heart rate variability in patients with coronary slow flow. Ann Noninvasive Electrocardiol 2004;9:24e33. [32] Romagni P, Rossi F, Guerrini L, Quirini C, Santiemma V. Aldosterone induces contraction of the resistance arteries in man. Atherosclerosis 2003;166:345e9. [33] Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, et al. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 western prospective studies. Circulation 2007;115:450e8. [34] Shichiri M, Hirata Y, Ando K, Emori T, Ohta K, Kimoto S, et al. Plasma endothelin levels in hypertension and chronic renal failure. Hypertension 1990;15: 493e6. [35] Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, et al. Aging and endothelial function in normotensive subjects and patients with essential hypertension. Circulation 1995;91:1981e7. [36] Takahashi K, Ghatei MA, Lam HC, O’Halloran DJ, Bloom SR. Elevated plasma endothelin in patients with diabetes mellitus. Diabetologia 1990;33:306e10. [37] Tian L, Fu M. The relationship between high density lipoprotein subclass profile and plasma lipids concentrations. Lipids Health Dis 2010;17:118. [38] Tostes RC, Touyz RM, He G, Chen X, Schiffrin EL. Contribution of endothelin-1 to renal activator protein-1 activation and macrophage infiltration in aldosterone-induced hypertension. Clin Sci (Lond) 2002;103:25Se30S.
[39] Tsai JC, Wang WH, Chan P, Lin LJ, Wang CH, Tomlinson B, et al. The beneficial effects of Tai Chi Chuan on blood pressure and lipid profile and anxiety status in a randomized controlled trial. J Altern Complement Med 2003;9:747e54. [40] Vane JR, Angaard EE, Botting RM. Mechanisms of disease: regulatory functions of the vascular endothelium. N Engl J Med 1990;323:27e36. [41] Wang C, Schmid CH, Rones R, Kalish R, Yinh J, Goldenberg DL, et al. A Randomized trial of Tai Chi for fibromyalgia. N Engl J Med 2010;363: 743e54. [42] Wolfson L, Whipple R, Derby C, Judge J, King M, Amerman P, et al. Balance and strength training in older adults: intervention gains and Tai Chi maintenance. J Am Geriatr Soc 1996;44:498e506. [43] Wolpert HA, Steen SN, Istfan NW, Simonson DC. Insulin modulates circulating endothelin-1 levels in humans. Metabolism 1993;42:1027e30. [44] Xu D, Emoto N, Giaid A, Slaughter C, Kaw S, deWit D, et al. ECE-1: a membrane-bound metalloprotease that catalyzes the proteolytic activation of big endothelin-1. Cell 1994;78:473e85. [45] Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988;332:411e5. [46] Yeh GY, Kaptchuk TJ, Shmerling RH. Prescribing Tai Chi for fibromyalgia d Are we there yet? N Engl J Med 2010;363:783e4. [47] Yoshibayashi M, Nishioka K, Nakao K, Saito Y, Matsumura M, Ueda T, et al. Plasma endothelin concentrations in patients with pulmonary hypertension associated with congenital heart defects: evidence for increased production of endothelin in pulmonary circulation. Circulation 1991;84:2280e5.
Contents lists available at SciVerse ScienceDirect
Complementary Therapies in Clinical Practice journal homepage: www.elsevier.com/locate/ctcp
Three months of Tai Chi Chuan exercise can reduce serum triglyceride and endothelin-1 in the elderly Wan-An Lu a, b, Cheng-Deng Kuo a, * a b
Laboratory of Biophysics, Department of Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Cultural Asset and Reinvention, Fo-Guang University, Yilan, Taiwan
a b s t r a c t Keywords: Tai Chi Chuan Endothelin-1 Exercise Lipid Triglyceride
Endothelin-1 (ET-1) and circulating hormones play important roles in maintaining cardiovascular function. Tai Chi Chuan (TCC) is known to be good for health. This study evaluated the effect of 3 months of TCC training on serum ET-1, blood lipids, and other circulating hormones in the elderly. Twenty-two TCC trainees and 20 normal subjects were included in this study. The TCC trainees practiced classical Yang’s TCC 40 min per session, 7 times per week, for 3 months. The hemodynamics and serum ET-1 and lipids before and after TCC were compared. The percentage change in serum ET-1 and triglyceride (TG) were decreased significantly after 3 months of TCC, as compared to the control group. In the TCC group, the percentage decrease in serum ET-1 and TG after 3 months of TCC were 36.6 (63.4 to 14.0)% and 22.5 (30.7 to 4.9)%, respectively. TCC exercise for 3 months can reduce serum ET-1 and TG in the elderly. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction Endothelial function is a balance between vascular cell protectors and risk factors. Under physiological conditions, vascular endothelium has antithrombogenic potential. While improvement in nitric oxide (NO) vasodilator function has been less frequently found in healthy subjects, a higher level of training may lead to improvement. Exercise training may improve endothelial function by up-regulating endothelial nitric oxide synthase (eNOS) protein expression and phosphorylation. Clinical studies have shown a significant improvement in endothelial dysfunction following lowering of serum cholesterol levels, infusion of nitric oxide donors such as L-arginine and exercise training [22]. Endothelin-1 (ET-1) belongs to a family of potent vasoconstrictor peptides. It was isolated from the culture supernatant of porcine aortic endothelial cell in 1988 by Tomoh Masaki and associates [45]. ET-1 is produced from the biologically inactive 38amino acid intermediate, big ET-1, via cleavage by ET-converting enzyme [44]. Some studies have shown that ET-1 may be involved in the pathogenesis of hypertension and atherosclerosis [24,40]. Elevated plasma level of ET-1 has been observed in patients * Corresponding author. Laboratory of Biophysics, Department of Research and Education, Taipei Veterans General Hospital, No. 210, Sec. 2, Shipai Road, Taipei 112, Taiwan. Tel.: þ886 2 28757745; fax: þ886 2 28710773. E-mail address: [email protected] (C.-D. Kuo). 1744-3881/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ctcp.2013.06.007
with chronic heart failure [15], essential hypertension [17], atherosclerosis [24], chronic renal failure [34], myocardial infarction [30] and diabetes [36]. Takahashi et al. [36] pointed out that circulating ET-1 play an important role as a paracrine factor in the metabolism of blood glucose by modulating insulin levels. One study has showed that both increased plasma ET-1, decreased plasma NOx and diffuse atherosclerosis may cause the decrease in heart rate variability by affecting myocardial blood flow in patients with coronary slow flow [31]. Furthermore, circulating aldosterone may directly affect vascular tone and may be part of the vasoconstriction response [32]. Tostes et al. [38] suggested that renal damage in aldosterone-dependent hypertension is associated with inflammatory processes that are mediated in part via ET-1. Thus, ET-1 and some circulating hormones are involved in the maintenance of the homeostasis of the cardiovascular system. Tai Chi Chuan (TCC) has been shown to be beneficial to the cardiopulmonary function [18,20] balance [42] and strength [20] of the subjects practicing it regularly. TCC is one kind of moving meditations that can reduce tension, anxiety, and mood disturbance [13]. It has also been shown that the short-term effect of TCC was to enhance the vagal modulation and tilt the sympathovagal balance towards deceased sympathetic modulation in older persons [28]. Recent studies have also demonstrated that TCC may be a useful treatment for fibromyalgia [41,46]. Maeda and associates [29] have shown that regular aerobicendurance exercise can reduce plasma ET-1 concentration which
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
may have beneficial effects on the cardiovascular system in older humans. Lewczuk and colleagues [25] demonstrated that ET-1 concentration in plasma is decreased after cycling in healthy men. Since 3 months of TCC training can improve the pulmonary function, glucose availability, blood lipid profile, cytokine production and vagal modulation in elderly subjects [27], it is interesting to know the effects of 3 months of TCC on the cardiovascular system and some circulating hormones of the subjects practicing it. Thus the aim of this study was to examine the effect of 3 months of TCC training on the serum levels of ET-1, aldosterone, fasting serum insulin, lipid profiles and hemodynamics in the elderly. 2. Methods 2.1. Subjects TCC trainees recruited from a TCC training center in Taiwan. The TCC trainees received 3 months of Yang’s TCC training for 1 h each time, 7 times per week. Healthy subjects without TCC experience and smoking history who were recruited from the community were included in this study. All subjects included in this study were over 50 years of age, had no previous experience with TCC, had normal lifestyles, and were capable of daily activities without limitations. Subjects who had major cardiopulmonary disease or were on regular medicine for diabetes mellitus, hypertension, renal or liver disease were not included in the study. The Institute Review Board of the hospital has approved this study, and the procedure was fully explained to the study subjects before the study. The written informed consent was obtained from every participant prior to the study. Before measurements were taken, each subject took a rest in supine position for 5 min. The arterial blood pressure measurement (Omron, HEM-770A) was performed on both controls and TCC trainees before and after 3 months of TCC. The hemodynamic data such as systolic blood pressure (SBP), diastolic blood pressure (DBP), mean arterial blood pressure (MABP), and pulse pressure (PP) were obtained from every subject in the control group and TCC group before TCC training and after 3 months of TCC training. The TCC trainee exercised TCC once per day for 3 months. The subjects included in this study were requested to not take any caffeinated or alcoholic beverages for at least 24 h prior to the study, and they were also requested to not exercise on the day of study. The hemodynamic data were measured after the subject had rested quietly for 5 min, and then a blood sample was withdrawn for later assay. After that, the TCC trainee was advised to exercise the classical Yang’s TCC for 40 min. Each session of Yang’s TCC included a 10-min warm-up exercise (lower back and hamstring stretching, gentle calisthenics, and balance training), a 20-min TCC exercise, and a 10-min cool-down exercise. Each set of Yang’s TCC consists of 64 successive postures. While practicing TCC, the TCC trainee kept the same pace in exercising the different postures of TCC in a sequence according to a pre-recorded tape to ensure that the same pace and sequence of postures were followed. After 3 months of TCC training, which consisted of 40-min exercise per session, 7 times per week, a second hemodynamic measurements and blood sampling were performed using the same procedure. All procedures were performed in a bright and quiet room with a standardized temperature of 24e25 C and a standardized humidity of 54e55%. 2.2. Biochemistry and hormone analysis The biochemistry assays for the quantitative measurements of total cholesterol (TC) (Ektachem Clinical Chemistry Slides, Johnson & Johnson), high-density lipoprotein-cholesterol (HDL-C)
205
(INTEGRA 700, Roche), low-density lipoprotein-cholesterol (LDL-C) (INTEGRA 700, Roche), triglyceride (TG), and fasting blood sugar (FBS) (Ektachem Clinical Chemistry Slides, Johnson & Johnson) were performed on the blood sample obtained from each subject. The radioimmunoassay for the quantitative measurement of insulin (DIAsource INS-IRMA Kit, DIAsource ImmunoAssays SA) and aldosterone (DSL-8600 ACTIVE Aldosterone Coated-Tube Radioimmunoassay Kit, Diagnostic Systems Laboratories, Inc. USA), and the enzyme immunoassay for the quantitative determination of ET-1 (Kit Lot 998C Abl./Exp. 100908. CAT. No. BI-20052, Biomedica Medizinprodukte GmbH & Co. KG, Divischgasse 4, A-1210 Wien, Austria) were also performed on the blood sample from each subject. After 3 months of TCC training, the hemodynamic data, blood biochemistry and serum hormone levels of the TCC trainees were repeated using the same methodology. 2.3. Statistical analysis The ManneWhitney rank sum test (SigmaStat statistical software, SPSS Inc., Chicago, Illinois, USA) was employed to compare the baseline general characteristics, hemodynamics, blood biochemistry, lipid profile and circulating hormone levels between the TCC and control groups. All data are presented as median (25%e 75%). A p < 0.05 is considered statistically significant. To quantify the effect of 3 months of TCC training on the general characteristic, hemodynamics, lipid profile, and hormones in the elderly, the percentage changes in these parameters before and after 3 months of TCC training in each subject were calculated by using the following formula:
%X ¼
h
X3month Xbefore
. i Xbefore 100;
where X denotes the parameter under consideration. Comparisons of the percentage changes in these parameters between the controls and TCC trainees were performed by using the ManneWhitney rank sum test. Correlation analysis was performed to analyze the relationship among the percentage changes in the parameters between before and after 3 months of TCC training. 3. Results 3.1. General characteristics Twenty-two TCC trainees and twenty normal controls were included in this study. There was no significant difference in the baseline characteristics between normal controls and TCC trainees before TCC Training (Table 1). 3.2. Effect of TCC on hormones and lipid profile Table 2 shows the comparison of the percentage changes in general characteristic, hemodynamics, lipid profile and hormone levels between control and TCC groups after 3 months of TCC Training. There were significant decreases in serum level of TG and ET-1 after 3 months of TCC in the TCC group, as compared to those of the control group. In the TCC group, the percentage decrease in the serum levels of ET-1 and TG after 3 months of TCC training were 36.6 (63.4 to 14.0)% and 22.5 (30.7 to 4.9)%, respectively; whereas the percentage increase in the serum levels of insulin and aldosterone after 3 months of TCC training were 95.3 (13.8e212.2)% and 40.0 (18.2 to 169.2)%, respectively. Correlation analysis showed that there were no correlations either between %TG and %ET-1 or between %ET-1 and other parameters in the TCC group after 3 months of TCC.
206
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
Table 1 Comparison of characteristics, hemodynamic measures, blood biochemistry, lipid profile and hormone levels between controls and TCC trainees before TCC training.
Age (years) Gender (M/F) Body weight (Kg) Body height (cm) BMI (kg/m2) Waist (cm) SBP (mmHg) DBP (mmHg) MABP (mmHg) PP (mmHg) TG (mg/dl) TC (mg/dl) LDL-C (mg/dl) HDL-C (mg/dl) TC/HDL-C LDL-C/HDL-C FBS (mg/dl) ET-1 (fmol/ml) Insulin (ng/ml) Aldosterone (pg/ml)
Controls (n ¼ 20)
TCC trainees (n ¼ 22)
P value
52 (45e55) 9/11 65 (61e73) 163 (160e168) 23.8 (22.3e26.4) 84.9 (76.2e89.6) 119 (106e127) 68 (58e74) 82 (75e92) 49 (42e55) 138 (115e206) 176 (152e198) 108 (80e124) 46 (42e51) 3.78 (3.03e4.63) 2.37 (1.56e2.79) 92.0 (82.5e104.0) 0.47 (0.36e0.78) 13.6 (8.1e19.2) 64.9 (54.2e103.5)
56 (51e61) 12/10 64 (55e71) 166 (158e170) 23.5 (21.1e24.6) 83.7 (73.7e90.9) 122 (113e129) 71 (64e79) 89 (80e92) 52 (40e59) 124 (80e144) 173 (159e192) 107 (97e123) 52 (45e63) 3.39 (2.79e3.94) 2.29 (1.50e2.61) 90.5 (74.0e159.0) 0.56 (0.41e1.43) 5.5 (2.2e20.7) 60.3 (55.9e73.1)
0.235 0.537 0.569 0.638 0.247 0.574 0.270 0.205 0.198 0.711 0.199 0.990 0.870 0.107 0.284 0.417 0.890 0.195 0.170 0.097
All data are medians (25 percentile w 75 percentile). BMI ¼ body mass index; SBP ¼ systolic blood pressure; DBP ¼ diastolic blood pressure; MABP ¼ mean arterial blood pressure; PP ¼ pulse pressure; TG ¼ triglycerides; TC ¼ total cholesterol; LDL-C ¼ low-density lipoproteincholesterol; HDL-C ¼ high-density lipoprotein-cholesterol; TC/HDL-C ¼ ratio of TC over HDL-C; LDL-C/HDL-C ¼ ratio of LDL-C over HDL-C; FBS ¼ fasting blood sugar; ET-1 ¼ Endothelin-1.
4. Discussion Since TCC is a well-known low-intensity and low-impact aerobic exercise, we conducted this study to evaluate the effect of 3 months of TCC training on the lipid profile, endocrine hormone in the elderly people. We found that TCC exercise for 3 months can reduce not only the serum level of TG, but also the serum level of ET-1 in
Table 2 Comparison of percentage changes in general characteristics, hemodynamic measures, blood biochemistry, lipid profile and hormone levels between controls and TCC trainees after 3 months of TCC training.
%BW %BMI %Waist %SBP %DBP %MABP %PP %TG %TC %LDL-C %HDL-C %TC/HDL-C %LDL-C/HDL-C %FBS %ET-1 %Insulin %Aldosterone
Controls (n ¼ 20)
TCC trainees (n ¼ 22)
P value
0.0 0.0 0.1 0.5 8.6 3.5 9.7 0.5 5.0 9.6 6.1 6.2 1.0 6.4 6.3 26.3 4.6
0.0 0.0 0.0 0.9 3.9 1.1 13.9 22.5 2.6 8.3 5.0 3.9 2.2 5.2 36.6 95.3 40.0
0.057 0.115 0.588 0.856 0.513 0.843 0.995 0.023 0.146 0.576 0.990 0.990 0.910 0.734 0.001 0.505 0.148
(0.7 to 1.5) (0.7 to 1.5) (1.3 to 2.6) (10.1 to 7.1) (6.3 to 15.7) (3.9 to 11.6) (15.4 to 4.3) (17.1 to 32.7) (0.5 to 10.3) (4.9 to 30.1) (14.2 to 15.5) (9.9 to 4.2) (9.2 to 12.7) (19.0 to 20.0) (17.5 to 62.0) (50.9 to 288.5) (29.0 to 78.8)
(1.3 to 0.0) (1.3 to 0.0) (1.2 to 0.0) (8.7 to 6.5) (3.9 to 11.1) (5.4 to 7.2) (18.6 to 2.1) (30.7 to 4.9) (9.9 to 11.6) (9.0 to 24.2) (0.3 to 10.0) (13.2 to 2.9) (9.4 to 16.9) (7.4 to 14.3) (63.4 to 14.0) (13.8 to 212.2) (18.2 to 169.2)
All data are medians (25 percentilew75 percentile). %BW ¼ % change in body weight; %BMI ¼ % change in body mass index; %SBP ¼ % change in systolic blood pressure; %DBP ¼ % change in diastolic blood pressure; % MABP ¼ % change in mean arterial blood pressure; %PP ¼ % change in pulse pressure; %TG ¼ % change in triglycerides; %TC ¼ % change in total cholesterol; %LDLC ¼ % change in low-density lipoprotein-cholesterol; %HDL-C ¼ % change in highdensity lipoprotein-cholesterol; %TC/HDL-C ¼ % change in ratio of TC over HDL-C; %LDL-C/HDL-C ¼ % change in ratio of LDL-C over HDL-C; %FBS ¼ % change in fasting blood sugar; %ET-1 ¼ % change in Endothelin-1.
the elderly. Our result paralleled the results of previous studies that regular aerobic-endurance exercise reduces plasma ET-1 concentration in older people [29], and that ET-1 concentration in plasma is decreased after cycling in healthy men. [25]. Therefore, TCC exercise may be beneficial to the health of elderly people, because the reduction in plasma ET-1 concentration may have beneficial effects on the cardiovascular system in older persons [29]. Channer and associates [2] have shown that an 8-week, lowintensity TCC program was effective for reducing blood pressure in patients with acute myocardial infarction. Lai et al. [18] found that regular TCC can delay the decline of cardiovascular function in the elderly individuals. Lan et al. [20] also demonstrated that a 12month TCC program was effective to improve cardiorespiratory function, muscle strength, and flexibility in the elderly. Lan et al. [19] later showed that TCC could significantly increase the VO2peak and peak work rate in patients with coronary artery bypass surgery. Similarly, Hong et al. [10] reported that long-term regular TCC exercise has favorable effects on the promotion of balance control, flexibility, and cardiovascular fitness in the elderly. Jahnke et al. [12] further pointed out that the strongest and most consistent evidence is demonstrated for effects on bone health, cardiopulmonary fitness, some aspects of physical function, quality of life, selfefficacy, and factors related to prevention of falls. From these studies, it is clear that TCC is a suitable conditioning exercise that can improve the cardiorespiratory function of the elderly. Camsan et al. [1] showed that the baseline ET-1 concentrations of the control subjects were lower than that of patients with slow coronary flow (SCF) and that this difference increased after exercise because post-exercise ET-1 concentrations were significantly higher than baseline in patients with SCF whereas a reduction in the ET-1 concentrations was observed in control subjects. In the present study, we found that 3 months of regular TCC exercise could significantly decrease serum level of ET-1 in the TCC group. Since endothelial dysfunction is associated with advancing age [35] and patients with chronic heart failure [16] and since circulating serum ET-1 is a potent vasoconstrictor that originates mainly from the vascular endothelial cells [5], it is possible that the production of ET-1 by the vascular endothelial cells of elderly subjects in this study was decreased by the remodeling of the vascular endothelium due to regular TCC exercise. Our study seemed to be in accordance with previous studies that aerobic exercise training can reduce plasma ET-1 concentration in older women [29], and that post-exercise ET-1 concentrations were significantly reduced in the control subjects [35]. Since plasma level of ET-1 correlates with disease severity [47], the reduction in serum level of ET-1 after 3 months of TCC suggested that TCC exercise may be beneficial to the cardiovascular system of the elderly subjects. In the present study, we found that regular TCC exercise could significantly increase the fasting serum insulin and aldosterone levels in the elderly. Kirwan et al. [14] have shown that one week of vigorous exercise training can induce significant improvements in insulin action in type 2 diabetes, including increased peripheral insulin sensitivity and responsiveness as well as enhanced suppression of hepatic glucose production. A direct relationship among plasma aldosterone levels, insulin resistance, and hyperinsulinemia exists in hypertensive patients [4]. Insulin also modulates ET-1 levels in vivo [43]. Since ET-1 may impair insulin sensitivity [6], the increased serum insulin after 3 months of regular TCC exercise may be related to the diminished sensitivity and responsiveness of insulin, and the decreased plasma level of ET-1 in the elderly subjects after TCC exercise. It has been shown that 12-month Yang TCC training program decreased triglyceride [21]. Tsai et al. [39] also showed that 12week Tai Chi Chuan exercise resulted in favorable lipid profile changes. Chen et al. [3] demonstrated that Tai Chi exercise practiced
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
by patients who are obese and have type 2 diabetes is efficient and safe when supervised by professionals and helps improve BMI and lipid profile including triglyceride and high density lipoprotein cholesterol. By using quantitative coronary angiography, Hodis et al. [9] further showed that the progression of mild-to-moderate lesions are among the most significant predictors of clinical coronary events, and that lowering triglyceride-rich lipoproteins reduces progression of coronary artery disease to the same degree as the lowering of LDL-cholesterol. Similarly, we found in this study that TCC for 3 months can lower the serum level of TG in the elderly. Thus, TCC for 3 months should be good for the health of the elderly people. Garcés et al. [7] showed that obese 6- to 8-year-old children have elevated levels of TG and insulin and lower levels of HDL-C, which are similar to those found in obese adults. Epidemiologic studies indicated that serum TG level is an important independent risk indicator of coronary heart disease [11,33]. Endogenous hypertriglyceridemia was shown to be the commonly encountered hyperlipidemia in clinical practice, which is characterized by elevation of TG and usually normal levels of TC. [23,37]. The diets which is high in carbohydrate may result in disorder of TG metabolism (excessive production and/or deficient clearance) [26]. Thus, the reduction in serum TG level after 3 months of TCC training indicated that TCC exercise is good for health as far as lipidemia is concerned. Hayakawa et al. [8] pointed out that the mechanisms involved in the endothelial dysfunction induced by hypercholesterolaemia and oxidized lipids may differ among vascular beds. We found no correlations either between %TG and %ET-1 or between %ET-1 and other parameters in the TCC group after 3 months of TCC. The lack of correlation between %TG and %ET-1 suggested that the lowering of serum TG and ET-1 by 3 months of TCC might be via different mechanisms. Also, the lack of correlation between serum ET-1 and other parameters examined in this study suggested that the mechanism leading to the lowering of serum ET1 by 3 months of TCC might not be related to blood sugar, insulin, aldosterone, etc. Further studies are necessary in the future to elucidate the mechanisms responsible for the lowering of ET-1 and TG by 3 months of TCC. The use of an objective measure of physical health and fitness is a major strength of this study as it provides a precise and accurate estimate of the effect of TCC on the TCC trainees. The detailed measures available allowed us to test for the associations among potential determinants such as cardiovascular function and the endocrine activity in the TCC program and allowed adequate exploration of the role of potential confounders in the physical activity of sport medicine. The finding of reduction in the serum levels of endothelin-1 by 3 months of TCC gives supportive evidence to the general notion that TCC is beneficial to the cardiopulmonary function of the subjects practicing it regularly. In conclusion, three months of TCC exercise training can reduce the serum levels of ET-1 and TG in the elderly, and that the lowering of serum TG and ET-1 by 3 months of TCC might be via different mechanisms. TCC for 3 months might be good to health of the elderly subjects as far as cardiovascular diseases are concerned. Conflict of interest statement We certify that all authors have no financial and personal relationships with other people or organizations that could inappropriately influence (bias) their work. Acknowledgments This study was supported by project V91-365-1 of Taipei Veterans General Hospital, project NSC96-2320-B-075-002-MY2 of the National Science Council, and project CCMP97-RD-047 of the
207
Committee on Chinese Medicine and Pharmacy, Department of Health, Taipei, TAIWAN. References [1] Camsarl A, Pekdemir H, Cicek D, Polat G, Akkus MN, Döven O, et al. Endothelin-1 and nitric oxide concentrations and their response to exercise in patients with slow coronary flow. Circ J 2003;67:1022e8. [2] Channer KS, Barrow D, Barrow R, Osborne M, Ives G. Changes in hemodynamic parameters following Tai Chi Chuan and aerobic exercise in patients recovering from acute myocardial infarction. Postgrad Med J 1996;72:349e51. [3] Chen SC, Ueng KC, Lee SH, Sun KT, Lee MC. Effect of T’ai Chi exercise on biochemical profiles and oxidative stress indicators in obese patients with type 2 diabetes. J Altern Complement Med 2010;16:1153e9. [4] Colussi G, Catena C, Lapenna R, Nadalini E, Chiuch A, Sechi LA. Insulin resistance and hyperinsulinemia are related to plasma aldosterone levels in hypertensive patients. Diabetes Care 2007;30:2349e54. [5] Dietmann A, Lackner P, Helbok R, Spora K, Issifou S, Lell B, et al. Opposed circulating plasma levels of endothelin-1 and C-type natriuretic peptide in children with Plasmodium falciparum malaria. Malar J 2008;7:253e9. [6] Ferri C, Carlomagno A, Coassin S, Baldoncini R, Faldetta MRC, Laurenti O, et al. Circulating endothelin-1 levels increase during euglycemic hyperinsulinemic clamp in lean NIDDM men. Diab Care 1995;18:226e33. [7] Garcés C, Gutierrez-Guisado J, Benavente M, Cano B, Viturro E, Ortega H, et al. Obesity in Spanish schoolchildren: relationship with lipid profile and insulin resistance. Obes Res 2005;13:959e63. [8] Hayakawa H, Raij L. Relationship between hypercholesterolaemia, endothelial dysfunction and hypertension. J Hypertens 1999;17:611e9. [9] Hodis HN, Mack WJ, Krauss RM, Alaupovic P. Pathophysiology of triglyceriderich lipoproteins in atherothrombosis: clinical aspects. Clin Cardiol 1999;22: II15e20. [10] Hong Y, Li JX, Robinson PD. Balance control, flexibility, and cardiorespiratory fitness among older Tai Chi practitioners. Br J Sports Med 2000;34:29e34. [11] Jacobson TA, Miller M, Schaefer EJ. Hypertriglyceridemia and cardiovascular risk reduction. Clin Ther 2007;29:763e77. [12] Jahnke R, Larkey L, Rogers C, Etnier J, Lin F. A comprehensive review of health benefits of qigong and tai chi. Am J Health Promot 2010;24:e1e25. [13] Jin P. Efficacy of Tai Chi, brisk walking, meditation, and reading in reducing mental and emotional stress. J Psychosom Res 1992;36:361e70. [14] Kirwan JP, Solomon TP, Wojta DM, Staten MA, Holloszy JO. Effects of 7 days of exercise training on insulin sensitivity and responsiveness in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 2009;297:E151e6. [15] Kjaer A, Appel J, Hildebrandt P, Petersen CL. Basal and exercise-induced neuroendocrine activation in patients with heart failure and in normal subjects. Eur J Heart Fail 2004;6:29e39. [16] Kobayashi N, Tsuruya Y, Iwasawa T, Ikeda N, Hashimoto S, Yasu T, et al. Exercise training in patients with chronic heart failure improves endothelial function predominantly in the trained extremities. Circ J 2003;67:505e10. [17] Kohno M, Yasunari K, Murakawa KI, Yokokawa K, Horio T, Fukui T, et al. Plasma immunoreactive endothelin in essential hypertension. Am J Med 1990;88:614e8. [18] Lai JS, Lan C, Wong MK, Teng SH. Two-year trends in cardiorespiratory function among older Tai Chi Chuan practitioners and sedentary subjects. J Am Geriatr Soc 1995;43:1222e7. [19] Lan C, Chen SY, Lai JS, Wong MK. The effect of Tai Chi on cardiorespiratory function in patients with coronary artery bypass surgery. Med Sci Sports Exerc 1999;31:634e8. [20] Lan C, Lai JS, Chen SY, Wong MK. 12-month Tai Chi training in the elderly: its effect on health fitness. Med Sci Sports Exerc 1998;30:345e51. [21] Lan C, Su TC, Chen SY, Lai JS. Effect of T’ai chi chuan training on cardiovascular risk factors in dyslipidemic patients. J Altern Complement Med 2008;14:813e9. [22] Laroia ST, Ganti AK, Laroia AT, Tendulkar KK. Endothelium and the lipid metabolism: the current understanding. Int J Cardiol 2003;88:1e9. [23] Lee M, Kim JQ, Kim J, Oh H, Park M. Studies on the plasma lipid profiles, and LCAT and CETP activities according to hyperlipoproteinemia phenotypes (HLP). Atherosclerosis 2001;159:381e9. [24] Lerman A, Edwards BS, Hallett JW, Heublein DM, Sandberg Jr SM, Burnett JC. Circulating and tissue endothelin immunoreactivity in advanced atherosclerosis. N Engl J Med 1991;325:997e1001. [25] Lewczuk P, Söhnchen N, Kele H, Reimers CD, Ehrenreich H. Endothelin-1 concentration in plasma is increased after jogging but decreased after cycling in healthy men. Clin Exp Med 2003;2:166e70. [26] Liu BW. Study on the pathogenesis of endogenous hypoertriglyceridemia. Chin J Atheroscler 1993;1:67e9. [27] Lu WA, Kuo CD. Effect of 3-month Tai Chi Chuan on heart rate variability, blood lipid and cytokine profiles in middle-aged and elderly subjects. Int J Gerontol 2012;6:267e72. [28] Lu WA, Kuo CD. The effect of Tai Chi Chuan on the autonomic nervous modulation in older persons. Med Sci Sports Exerc 2003;35:1972e6. [29] Maeda S, Tanabe T, Miyauchi T, Otsuki T, Sugawara J, Iemitsu M, et al. Aerobic exercise training reduces plasma endothelin-1 concentration in older women. J Appl Physiol 2003;95:336e41.
208
W.-A. Lu, C.-D. Kuo / Complementary Therapies in Clinical Practice 19 (2013) 204e208
[30] Omland T, Lie RT, Aakvaag A, Aarsland T, Dickstein K. Plasma endothelin determination as a prognostic indicator of 1-year mortality after acute myocardial infarction. Circulation 1994;89:1573e9. [31] Pekdemir H, Cicek D, Camsari A, Akkus MN, Cin VG, Doven O, et al. The relationship between plasma endothelin-1, nitric oxide levels, and heart rate variability in patients with coronary slow flow. Ann Noninvasive Electrocardiol 2004;9:24e33. [32] Romagni P, Rossi F, Guerrini L, Quirini C, Santiemma V. Aldosterone induces contraction of the resistance arteries in man. Atherosclerosis 2003;166:345e9. [33] Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, et al. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 western prospective studies. Circulation 2007;115:450e8. [34] Shichiri M, Hirata Y, Ando K, Emori T, Ohta K, Kimoto S, et al. Plasma endothelin levels in hypertension and chronic renal failure. Hypertension 1990;15: 493e6. [35] Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, et al. Aging and endothelial function in normotensive subjects and patients with essential hypertension. Circulation 1995;91:1981e7. [36] Takahashi K, Ghatei MA, Lam HC, O’Halloran DJ, Bloom SR. Elevated plasma endothelin in patients with diabetes mellitus. Diabetologia 1990;33:306e10. [37] Tian L, Fu M. The relationship between high density lipoprotein subclass profile and plasma lipids concentrations. Lipids Health Dis 2010;17:118. [38] Tostes RC, Touyz RM, He G, Chen X, Schiffrin EL. Contribution of endothelin-1 to renal activator protein-1 activation and macrophage infiltration in aldosterone-induced hypertension. Clin Sci (Lond) 2002;103:25Se30S.
[39] Tsai JC, Wang WH, Chan P, Lin LJ, Wang CH, Tomlinson B, et al. The beneficial effects of Tai Chi Chuan on blood pressure and lipid profile and anxiety status in a randomized controlled trial. J Altern Complement Med 2003;9:747e54. [40] Vane JR, Angaard EE, Botting RM. Mechanisms of disease: regulatory functions of the vascular endothelium. N Engl J Med 1990;323:27e36. [41] Wang C, Schmid CH, Rones R, Kalish R, Yinh J, Goldenberg DL, et al. A Randomized trial of Tai Chi for fibromyalgia. N Engl J Med 2010;363: 743e54. [42] Wolfson L, Whipple R, Derby C, Judge J, King M, Amerman P, et al. Balance and strength training in older adults: intervention gains and Tai Chi maintenance. J Am Geriatr Soc 1996;44:498e506. [43] Wolpert HA, Steen SN, Istfan NW, Simonson DC. Insulin modulates circulating endothelin-1 levels in humans. Metabolism 1993;42:1027e30. [44] Xu D, Emoto N, Giaid A, Slaughter C, Kaw S, deWit D, et al. ECE-1: a membrane-bound metalloprotease that catalyzes the proteolytic activation of big endothelin-1. Cell 1994;78:473e85. [45] Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988;332:411e5. [46] Yeh GY, Kaptchuk TJ, Shmerling RH. Prescribing Tai Chi for fibromyalgia d Are we there yet? N Engl J Med 2010;363:783e4. [47] Yoshibayashi M, Nishioka K, Nakao K, Saito Y, Matsumura M, Ueda T, et al. Plasma endothelin concentrations in patients with pulmonary hypertension associated with congenital heart defects: evidence for increased production of endothelin in pulmonary circulation. Circulation 1991;84:2280e5.