NITRIC OXIDE is an endothelial-dependent vasodilator. Tai Chi Chuan Training to Enhance Microcirculatory Function in Healthy Elderly Men

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1 1176 Tai Chi Chuan Training to Enhance Microcirculatory Function in Healthy Elderly Men Jong-Shyan Wang, PhD, Ching Lan, MD, May-Kuen Wong, MD ABSTRACT. Wang J-S, Lan C, Wong M-K. Tai Chi Chuan training to enhance microcirculatory function in healthy elderly men. Arch Phys Med Rehabil 2001;82: Objective: To evaluate cutaneous microcirculatory function in geriatric Tai Chi Chuan (TCC) practitioners. Design: Case-control study. Setting: Community setting. Participants: Ten elderly male TCC practitioners (mean age, yr) and 10 sedentary men with matched age and body size (mean age, yr). Intervention: The TCC group had practiced TCC for years (mean standard error of the mean), with an exercise frequency of times weekly. Each session included 20 minutes of warm-up, 24 minutes of TCC practice, and 10 minutes of cool down. Main Outcome Measures: A graded exercise test with gas analysis was conducted on a bicycle ergometer for each subject. Skin blood flow (SkBF), cutaneous vascular conductance, and skin temperature were measured at rest and during exercise testing. Plasma nitric oxide metabolite was analyzed before and immediately after exercise. Results: The TCC group had a 34% higher VO 2 peak than the control group; it also had a higher SkBF, cutaneous vascular conductance, and skin temperature than the control group at rest and during exercise; and it also had a higher level of plasma nitric oxide metabolite than the sedentary group at rest and after exercise. Conclusion: Older TCC practitioners had higher cutaneous microcirculatory function during exercise than did their sedentary counterparts. Moreover, this change may be partially mediated by enhancement of nitric oxide release. Key Words: Elderly; Exercise; Microcirculation; Nitric oxide; Rehabilitation; Skin blood flow; Tai Chi by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation NITRIC OXIDE is an endothelial-dependent vasodilator that has an important role in the regulation of vascular tone 1 ; it also contributes to vasodilatory response during exercise. Although nitric oxide has only a modest role in exercise hyperemia, 2 active cutaneous vasodilation requires functional nitric oxide bioactivity to achieve full expression. 3 Previous From the Department of Physical Therapy, Chang Gung University (Wang); Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital (Wong) Tao-Yuan; and Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital (Lan), Taipei, Taiwan. Accepted in revised form September 25, Supported by the National Science Council (grant no. NSC B ). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Jong-Shyan Wang, PhD, Dept of Physical Therapy, Chang Gung University, 259 Wen-Haw 1st Rd, Kwei-Shan, Tao-Yuan 333, Taiwan, s5492@mail.cgu.edu.tw /01/ $35.00/0 doi: /apmr studies have shown that physical conditioning can enhance vascular responsiveness, 4,5 and hence can relieve the symptoms of intermittent claudication in patients with peripheral vascular disease. 6 Our previous study 7 also indicated that exercise training could increase levels of plasma nitric oxide metabolite at rest and after exercise. The decrease with aging in thermoregulatory response to heat stress can be life threatening to the elderly During exercise, as core temperature rises, skin blood flow (SkBF) increases to facilitate the convective transfer of heat from core to skin. Both the slope of the SkBF-core temperature relationship and the steady-state SkBF achieved are attenuated in older individuals. 11,12 Skin components tend to diminish in size and number with age, and the structural changes in cutaneous vasculature limit vasodilation in the elderly. 13,14 However, exercise training can partially reverse the age-related decline of microcirculation through enhancement of nitric oxide release. Therefore, active older individuals show a greater increase in sweating and SkBF than their sedentary counterparts. 9 Tai Chi Chuan (TCC) is a Chinese conditioning exercise. Recent studies substantiate its benefits on cardiorespiratory function, muscle strength, 18 and posture control. 19,20 To our knowledge, the effect of TCC training on cutaneous microcirculation and release of nitric oxide induced by acute exercise in elderly individuals has not been studied. This study compared cutaneous microcirculatory responsiveness to acute exercise in elderly TCC practitioners and sedentary individuals. In addition, subjects plasma nitric oxide metabolites (nitrite plus nitrate) were measured to explore the potential enhancing effect of TCC training on the release of nitric oxide. METHODS Subjects Ten TCC men (mean age, yr) were recruited from a Tai Chi club and 10 sedentary men (mean age, yr) were recruited from a senior citizens center. Medical and activity histories were obtained by questionnaire. Subjects with histories of significant cardiovascular, pulmonary, metabolic, or musculoskeletal disease were excluded. The men in the TCC group had been regularly practicing Yang TCC for an average of years, and the men in the sedentary group had not engaged in any regular physical activity for at least 5 years. All subjects were community dwellers, led normal lifestyles, and were capable of daily activities without limitations. An institutional committee for the protection of human subjects approved the study protocol. Procedures followed were in accord with institutional guidelines, and informed consent to participate was given by all subjects. Before the study, subjects were familiarized with exercising on a bicycle ergometer a to eliminate the novel effect of a new experience. TCC Training Subjects practiced classical Yang TCC at least 3 times weekly. Each session included a 20-minute warm-up (low back and hamstrings stretching, gentle calisthenics, balance training), a 24-minute TCC session, and 10-minute cool down. Each

2 TAI CHI CHUAN AND MICROCIRCULATORY FUNCTION, Wang 1177 Table 1: Subjects Baseline Anthropometric Characteristics Group TCC (n 10) Control (n 10) Age (yr) Height (cm) Weight (kg) Body mass index (kg/m 2 ) Resting blood pressure (mmhg) 141 9/ /77 2 NOTE. Values are mean SEM. TCC set included 108 postures, with some repeated sequences. During the TCC session, subjects were led by a Tai Chi instructor and imitated the motions and postures at the same speed. Subjects performed each posture according to a taperecorded form sequence to ensure the same time course. Exercise Testing Protocol The exercise test was conducted in an air-conditioned laboratory with an atmospheric temperature of 22 C to 25 C, a barometric pressure of 755 to 770torr, and relative humidity of 55% to 65%. After the subject had rested for 30 minutes, blood samples were drawn from a forearm vein. The first 2mL of blood was discarded, and the remaining blood sample was used to measure resting plasma nitric oxide metabolite. The exercise protocol consisted of 2 minutes of unloaded pedaling, followed by a continuous increment of workload of 10 to 15W every 3 minutes until exhaustion. Another blood sample was obtained immediately after exercise for the measurements of postexercise plasma nitric oxide metabolite. Heart rate (HR), minute ventilation (V E), oxygen consumption (V O2 ), and carbon dioxide production (V CO2 ) were measured during the exercise with an automated system. b Blood pressure was monitored every 3 minutes by an automatic blood pressure system. c Mean arterial pressure (MAP) was calculated as the diastolic pressure plus one third of the pulse pressure, and oxygen pulse values as V O2 divided by HR. Peak oxygen uptake (VO 2 peak) was defined as the peak VO 2, according to at least 3 of the following 4 criteria: (1) the increase of V O2 was less than 2mL kg 1 min 1 in the last 2 minutes of exercise 21 ; (2) HR exceeded the maximal predicted HR; (3) the respiratory exchange ratio exceeded ; and (4) venous lactate concentration after the termination of exercise exceeded 50mg/dL. 23 SkBF and Temperature Regional cutaneous blood flow during exercise was estimated by laser Doppler flowmetry (LDF). 24,d The laser Doppler incorporates a low-power solid-state infrared laser diode as a source of coherent light. Variables of frequency and power of the reflected photons are analyzed to yield estimates of blood volume and flow velocity. The probe head was applied to the skin over the right upper back. The subject was then asked to take deep breaths to verify stability of the signal and to ensure that movement artifacts did not influence the readings. 25 Cutaneous vascular conductance was calculated as MAP divided by LDF and expressed as the blood perfusion unit (BPU) per millimeters of mercury. Skin temperature was measured using a thermistor e taped to the upper back. Plasma Nitric Oxide Metabolites Nitric oxide is rapidly oxidized to a stable end-product, nitrite and nitrate. Therefore, nitrite plus nitrate have been used as a biochemical marker of endogenous nitric oxide production. Blood samples were put into a polypropylene tube containing sodium citrate (3.8g/dL; 1 vol for 9 vol of blood). The plasma was obtained by centrifugation at 10,000g for 30 minutes at 4 C. Nitrite plus nitrate in plasma was measured by fluorometric assay kit. 26,f The first step was the conversion of nitrate to nitrite by using nitrate reductase. The second step was the addition of 2,3-diaminonaphthalene followed by sodium hydroxide, which coverted nitrite into a fluorescent compound in which nitrite concentration could be determined. The fluorescent intensity was measured using a microplate fluorometer g with excitation at 375nm and emission at 415nm. Statistical Analysis Data were expressed as means standard errors of the mean (SEMs). The parametric differences between the TCC group and the sedentary group were analyzed by Student s t test. The association of measurements with other biochemical parameters was assessed by the Spearman rank-correlation test. Differences were considered significant at p less than.05. RESULTS Table 1 lists the anthropometric data for the TCC and the sedentary group. There were no significant differences in age, body height, body weight, and body mass index between the 2 groups. Cardiorespiratory Function Resting HR, systolic and diastolic blood pressures, and MAP did not differ significantly between the TCC and the sedentary group. During the peak exercise, the TCC group was 34% higher in VO 2 peak than the control group. In addition, the TCC group had higher peak oxygen pulse, work rate, and V E than the sedentary group (table 2). At the same relative percentage of VO 2 peak, the TCC group showed similar work rate, HR, and MAP. However, oxygen pulse was higher in the TCC group than in the sedentary group for the same relative exercise intensity (fig 1). Cutaneous Microcirculatory Function During the exercise test, the TCC group had significantly higher SkBF than the sedentary group at the same percentage of VO 2 peak (fig 2). The TCC group also had higher cutaneous vascular conductance and skin temperature than the sedentary group at the same relative workload. Plasma Nitric Oxide Metabolite Table 3 shows that the levels of plasma nitrite plus nitrate correlated positively with SkBF, cutaneous vascular conduc- Table 2: Cardiorespiratory Function at Peak Exercise TCC Control VO 2 peak (ml kg 1 min 1 ) * HR peak (beats/min) Peak O 2 pulse (ml/beat) * RER VE peak (L/min) * WR peak (W) * Double product ( 10 3 ) BP (mmhg) / / NOTE. Values are mean SEM. Abbreviations: RER, respiratory exchange ratio; WR, work rate; BP, blood pressure. *p.05. The differences of parameters between the TCC and the control groups were analyzed by unpaired Student s t test.

3 1178 TAI CHI CHUAN AND MICROCIRCULATORY FUNCTION, Wang Fig 2. Changes in SkBF, cutaneous vascular conductance (CVC), and skin temperature (SkT) during exercise in the TCC and the control groups. *p <.05, TCC vs control. Fig 1. Work rate, MAP, HR, and oxygen pulse at rest and during exercise in the TCC and the sedentary (control) groups. Abbreviation: R, resting. *p <.05, TCC vs control. tance, and skin temperature in the TCC and the sedentary groups. Strenuous exercise increased the level of plasma nitrite plus nitrate in both groups (fig 3). The TCC group had higher levels of plasma nitrite plus nitrate than the sedentary group at rest and immediately after exercise (fig 3). DISCUSSION Aging is associated with a decline in acrobic capacity and vascular responsiveness to exercise. Lower VO 2 peak in older individuals results from lower peak cardiac output and, to a lesser extent, arteriovenous oxygen differences. This lower peak arteriovenous oxygen difference appears to result from a less efficient redistribution of blood flow, rather than a defi- Table 3: Correlation Between Plasma Nitrate Plus Nitrate Levels and SkBF, Cutaneous Vascular Conductance, and Skin Temperature Plasma Nitrite Plus Nitrate Levels r p SkBF (nitrite plus nitrate) CVC (nitrite plus nitrate) SkT (nitrite plus nitrate)

4 TAI CHI CHUAN AND MICROCIRCULATORY FUNCTION, Wang 1179 Fig 3. The effect of strenuous exercise in release of nitric oxide in the TCC and the control group. The TCC group had a higher level of plasma nitrite plus nitrate than the control group at rest and immediately after exercise. *p <.05, rest vs exercise; p <.05, TCC vs control. ciency in oxygen extraction. 27 The change of blood flow is most likely caused by an alteration in the relation between regional vasodilator and vasoconstrictor mechanisms. 27 Endurance training could partially reverse the age-related decline in aerobic power. From the perspective of oxygen transport, the increase of aerobic capacity after exercise training may be attributed to the increase of cardiac output and peripheral blood flow. We have reported 17 that TCC benefited the aerobic capacity of older individuals, 16 and long-term TCC training can significantly increase their VO 2 peak. 17 In this study, older TCC men showed a 34% higher VO 2 peak than did sedentary men. Although peak HR was similar in the 2 groups, the TCC group showed higher peak oxygen pulse than did the sedentary group. Oxygen pulse can be used to predict the cardiac stroke volume, and it shows a progressive decline with age. 28 Our previous study 17 showed that TCC training could significantly increase the peak oxygen pulse of elderly individuals. In this study, the TCC group also showed a 30% higher peak oxygen pulse than the sedentary group. Because the peak cardiac output is calculated as stroke volume multiplied by the HR, the result implies that TCC men have a higher peak cardiac output than their sedentary counterparts. TCC practitioners demonstrated higher SkBF, cutaneous vascular conductance, and skin temperature during exercise than did the sedentary subjects. The results indicated that TCC men had higher peripheral blood flow and heat dissipation during exercise. TCC men also had higher levels of nitric oxide metabolite than sedentary men, and the levels of plasma nitrite plus nitrate correlated positively with SkBF, cutaneous vascular conductance, and skin temperature. This results implies that the increased cutaneous microcirculatory function in older TCC practitioners may be, in part, mediated by nitric oxide. Nitric oxide is a potent vasorelaxant. 1 Because chronically elevated blood flow can enhance endothelium-derived nitric oxide release and endothelial nitric oxide synthase expression, 29,30 increased cutaneous blood flow during repetitive exercise may alter endothelial function and increase the sensitivity of stimulated endothelium-derived nitric oxide release in skin vasculature. Moreover, a previous study 31 demonstrated that physical conditioning could enhance cutaneous vascular responsiveness to endothelium-dependent vasodilators (ie, nitric oxide). Our previous study 32 also found that moderate exercise training with intensity at 55% VO 2 peak could increase plasma nitric oxide metabolite levels. In this study, TCC also enhanced vascular responsiveness during exercise in older individuals. The higher levels of nitric oxide in older TCC men can decrease the resistance of cutaneous vasculature, thereby increasing SkBF and cutaneous vascular conductance. Therefore, TCC training may increase the total amount of blood distributed to the skin during exercise by decreasing peripheral vascular resistance and increasing cardiac output. Although aging is associated with decreased vascular responsiveness, our results demonstrate that TCC training can slow the rate of decline in cutaneous microcirculatory function. When exercising, the muscles require oxygen to sustain energy metabolism and produce a large quantity of heat. The excessive metabolic heat must be transported by the blood from the deep tissues to the periphery. The change in core temperature during exercise is determined by the relative workload. 33 Thus, a fit person generates more heat at the same percentage of VO 2 peak during exercise, yet still has the same core temperature as their less fit counterparts. At a higher work rate, the excessive metabolic heat is dissipated by increased skin blood flow and sweat output. Previous studies indicated that the ability to dissipate heat during exercise declines with age. 9,34 Tankersley et al 9 also suggested that the decline in heat loss capacity may be related to the decline in VO 2 peak associated with aging. In this study, older TCC men had a higher SkBF, cutaneous vascular conductance, and skin temperature. The result implies that long-term TCC training can significantly improve the cutaneous microcirculatory function. CONCLUSION TCC is a Chinese conditioning exercise and is unique for its slow and graceful movements. From an exercise training perspective, TCC is suitable for the elderly. It is a low-technology approach to conditioning that can be implemented in the community with minimal cost. 35 Additionally, it is well suited for an elderly population because of its slow and structured movements. In our previous studies, 16,17 we have substantiated the benefits of TCC to health-related fitness (eg, cardiorespiratory function, muscular strength, flexibility, body composition). In this study, we have demonstrated that TCC also benefits peripheral microcirculation in the elderly. Although progressive decline in the cutaneous microcirculation with age is a natural course, our data suggest that TCC can attenuate this process. The mechanism of enhanced SkBF induced by TCC may be due to the increase of total blood volume distributed to skin by increasing cardiac output, and decreasing peripheral vascular resistance. In conclusion, TCC training in older individuals is associated with an attenuated decline of cutaneous microcirculatory function, and it may be prescribed as a suitable aerobic exercise for the elderly. References 1. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327: Joyner MJ, Dietz NM. Nitric oxide and vasodilation in human limbs. J Appl Physiol 1997;83: Kellogg DL, Crandall CG, Liu Y, Charkoudian N, Johnson JM. Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol 1998;85:824-9.

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Corival 400; Lode BV, Zernikepark 16, 9747 AN Groningen, The Netherlands. b. Systems 2000; Medical Graphics Corp, 350 Oak Grove Pkwy, St. Paul, MN c. Model 412; Quinton Instrument Co, 3303 Monte Villa Pkwy, Bothell, WA d. LDF 100; Biopac System, 42 Aero Camino, Santa Barbara, CA e. SKT100B; Biopac System, 42 Aero Camino, Santa Barbara, CA f. Cayman Chemical Co, 1180 E Ellsworth Rd, Ann Arbor, MI g. Fluoroskan II; Labsystems Oy, Pulttitie 8, PO Box 8, SF Helsinki, Finland.