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Hong Y (ed): Tai Chi Chuan. State of the Art in International Research. Med Sport Sci. Basel, Karger, 2008, vol 52, pp 195­208

Tai Chi Exercise in Patients with Chronic Heart Failure

Gloria Y. Yeha,b, Peter M. Waynea, Russell S. Phillipsa,b

Division for Research and Education in Complementary and Integrative Medical Therapies, Harvard Medical School, and bDivision of General Medicine and Primary Care, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Mass., USA

a

Abstract

Objective: To review the effects of a 12-week Tai Chi program (TC) on exercise capacity, quality of life, neurohormones, autonomic tone, and sleep in patients with heart failure (HF). Methods: We randomized 30 patients with chronic HF (left ventricular ejection fraction 40%) to receive TC plus usual care (n 15), or usual care alone (wait-list control, n 15). Outcome measures included quality of life, exercise capacity, B-type natriuretic peptide, catecholamine levels, heart rate variability, and sleep stability. Results: The mean age ( SD) of patients was 64 13 years, mean baseline ejection fraction ( SD) was 23 7%, and median New York Heart Association Class was 2 (range 1­4). At 12 weeks, patients who participated in TC showed improved quality of life (mean change 17 11 vs. 8 15, Minnesota Living with HF Questionnaire, p 0.001), increased exercise capacity (mean change 85 46 vs. 51 58 m, 6-min walk, p 0.001), and decreased B-type natriuretic peptide (mean change 48 104 vs. 90 333 pg/ml, p 0.03) compared to the control group. Those who participated in TC also showed improvement in sleep stability (increase in high-frequency coupling 0.05 0.10 vs. 0.06 0.09 proportion of estimated total sleep time, p 0.04; reduction in low-frequency coupling 0.09 0.09 vs. 0.13 0.13 proportion of estimated total sleep time, p 0.01), compared to the control group. Conclusion: TC may enhance quality of life, exercise capacity, and sleep stability in patients with chronic HF.

Copyright © 2008 S. Karger AG, Basel

Chronic heart failure (HF) is increasing in prevalence as the population ages and is the most common reason for hospital admission among Medicare patients. Approximately 5 million adults in the US are affected, with 550,000 new cases each year [1]. Despite recent therapeutic advances, patients with HF

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face progressively deteriorating function. Interventions that can improve functional capacity, quality of life, and overall outcome are needed. Reduced physical activity in patients with HF leads to deconditioning and exercise intolerance. Historically, it was thought that initiation of exercise would exacerbate HF symptoms [2]. On the contrary, recent trials have demonstrated benefits of exercise in patients with HF, including improved functional capacity, left ventricular hemodynamics, and quality of life, attenuation of neurohormonal activation and ventricular remodeling, and decreased risk of hospitalization and death. These studies, however, have used varied exercises. Current American Heart Association guidelines do not specify a standard exercise prescription for patients with HF; optimal protocols have yet to be defined [2, 3]. Tai Chi is a mind-body exercise with origins in traditional Chinese martial and healing arts. Reported benefits include increased balance and decreased incidence of falls, increased strength and flexibility, reduced pain and anxiety, improved self-efficacy, and enhanced cardiopulmonary function [4, 5]. Mindbody therapies like Tai Chi are being increasingly recognized in cardiac rehabilitation programs in the US [6]. Unlike conventional treadmill or bicycle exercise, Tai Chi incorporates both physical and meditative elements and emphasizes postural alignment, weight shifting, and low-impact, relaxed circular movements. Exercise intensity has been reported to be 2­4 metabolic equivalents, comparable to mild-moderate aerobic exercise [7, 8]. Trials in HF suggest that lower intensity activity may be just as beneficial as exercise of higher intensity [9]. Because of its mild nature, Tai Chi may be suitable for older or severely deconditioned cardiac patients. Prior randomized clinical trials of Tai Chi in patients with HF are lacking. One prospective, noncontrolled study (n 5) reported improvements in HFspecific quality of life, 6-min walk, and symptoms after a 12-week intervention [6]. Other controlled trials of Tai Chi have reported improvements in blood pressure in patients after myocardial infarction [10] and increases in peak oxygen uptake (VO2) and work rate following coronary bypass surgery [11]. Observational studies of healthy Tai Chi practitioners (compared to agematched sedentary controls) have suggested increased peak VO2, exercise endurance, cardiac output, and decreased peripheral vascular resistance and adrenergic tone [5]. Our objective was to investigate whether Tai Chi is beneficial as an adjunctive treatment to usual care for patients with chronic HF in a prospective randomized controlled trial, and to determine the feasibility of a larger trial. Methods and results of this trial have previously been published in the American Journal of Medicine and Sleep Medicine and are reviewed here [12, 13].

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Methods

Study Design A total of 30 patients were recruited from advanced HF clinics at Beth Israel Deaconess Medical Center and Brigham and Women's Hospital in Boston, Mass., USA. Patients were assigned randomly to receive either 12 weeks of Tai Chi training in addition to usual care, or to usual care alone, without a formal supervised exercise protocol (wait-list control). Usual care included pharmacologic therapy, dietary counseling, and general exercise advice per American Heart Association guidelines [3]. We used permuted block randomization with variable block size to generate treatment assignments. All patients provided written informed consent. Each institution's human subjects review board approved the study protocol.

Study Population

We included patients with chronic HF and left ventricular ejection fraction 40% by echocardiography in the past year, and those on a stable medical regimen (no major changes in medications in the past 3 months). We excluded patients with unstable angina, myocardial infarction, or cardiac surgery within the past 3 months, uncontrolled cardiac arrhythmias, major structural valvular disease, current participation in a conventional cardiac rehabilitation program, lower extremity amputation, cognitive dysfunction, and inability to speak English.

Intervention

One-hour group Tai Chi classes were held twice weekly for 12 weeks (table 1). Guided by similar interventions used in prior trials with elderly patients and those with limited mobility [14], we developed a standard protocol of meditative warm-up exercises followed by five simplified Tai Chi movements from Master Cheng Man-Ch'ing's Yang-style short form [15]. Warm-up exercises included weight shifting, arm swinging, visualization techniques, and stretches of the neck, shoulders, spine, arms and legs. Exercises focused on releasing tension in the physical body, incorporating mindfulness and imagery into movement, increasing awareness of breathing and promoting overall relaxation of body and mind. Patients were allowed to progress at their own comfort and pace. Classes were supervised by a physician. Patients were encouraged to practice at home three times per week and received a 35-min instructional video that outlined movements presented in class.

Main Outcome Measures All measures were obtained at baseline and 12 weeks. The quality of life assessment, 6-min walk, and neurohormone levels were also obtained at 6 weeks in the event that data at 12 weeks were unavailable.

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Table 1. Outline and overview of the Tai Chi intervention Week Activities Approximate duration, min

1

Introductory session: overview of program 1. Tai Chi principles, philosophies 2. Demonstration of Tai Chi form 3. Expectations of participants 4. Description of class format 5. Participation in warm-up exercises Warm-up exercises (repeated during all sessions) 1. Standing: a. `Drumming the body' b. `Swinging to connect kidney and lungs' c. `Washing the body with qi' d. Standing meditation and breathing 2. Sitting: a. Neck/shoulder stretches b. Arm/leg stretches c. Sitting meditation and breathing Total warm-up time Tai Chi movements 1. `Raising the Power' 2. `Withdraw and Push' (Warm-up and movements 1­2) 3. `Grasp Sparrows Tail' 4. `Brush Knee Twist Step'

15 10 10 5 30

2­5

10­12

Reprinted with permission from Yeh et al. [12].

Quality of Life Quality of life was measured using Minnesota Living with HF Questionnaire, a standardized instrument assessing physical, psychological, and socioeconomic dimensions of illness. Scores range from 0­105, with a lower score denoting a more favorable functional status [16]. Prior studies have reported a score of seven indicates some degree of impaired quality of life and an improvement of five points represents a clinically meaningful change [2]. Exercise Capacity Patients performed a standardized 6-min walk test. This test correlates with peak VO2, and has been used to assess functional capacity and predict survival in HF drug trials [17]. In addition, patients performed a symptom-limited bicycle exercise test to determine peak VO2. Testing was performed by a blinded assessor. Breath-by-breath respiratory gas analysis

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6 3 6 30 5­10 5 per side 5 per side 5 per side (Warm-up and movements 1­4) 5. `Wave Hands Like Clouds' 5­10

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was performed using a Sensormedic metabolic cart (Yorba Linda, Calif., USA). Peak values were averaged from the final 20 s of the test. Peak VO2 has a strong linear correlation with cardiac output and skeletal muscle blood flow and is used to predict when patients with chronic HF should undergo cardiac transplantation [18].

Secondary Outcome Measures Neurohormones B-type natriuretic peptide (BNP) was analyzed on whole blood collected in EDTA using the Biosite Triage BNP Test (San Diego, Calif., USA) fluorescence immunoassay. Levels of this cardiac biomarker correlate positively with degree of left ventricular dysfunction. Serum levels 100 pg/ml support a diagnosis of symptomatic HF [19]. Catecholamine samples were drawn on ice in heparinized tubes after 20-min rest with intravenous catheter in place. After centrifugation, plasma was separated and stored at 70 C. Analyses for norepinephrine, epinephrine, and dopamine were performed using high-performance liquid chromatography/electrochemical detector. Continuous Ambulatory Electrocardiographic Recording and Heart Rate Variability Patients underwent 24-hour ambulatory electrocardiographic (ECG) monitoring to assess cardiac arrhythmias and heart rate variability (HRV). Recordings were performed using Marquette Electronics (Milwaukee, Wisc., USA) series 8500 Holter monitor, digitized at 128 Hz. Annotations were manually verified and edited by a blinded technician. For standard HRV, 27 of 30 patients provided two complete sets of ECG data. Of these, 9 were excluded from analysis: 2 patients had a nonsinus rhythm and 7 patients were paced. In addition to 24-hour analysis, HRV statistics were separately calculated for sleep and waking activity. Sleep was defined as the 6 night-time hours of lowest heart rate (providing estimated total sleep time, ETST). Waking activity was defined as the 6 daytime hours of highest heart rate. Time and frequency domain HRV statistics were calculated, including average of all normal sinus-to-normal sinus NN intervals (AVNN), standard deviation SD of all NN intervals (SDNN), square root of mean of squares of differences between adjacent NN intervals (rMSSD), percentage of differences between adjacent NN intervals greater than 10­50 ms (pNN10­50), LF (0.04­0.15 Hz), HF (0.15­0.4 Hz), and LF/HF ratio [20, 21]. Complete HRV methods are detailed elsewhere [13]. Spectrographic Analysis of Sleep Stability We retrospectively analyzed 24-hour ECG data from the 18 subjects who provided 2 complete sets of data, who were not paced, and who were in sinus rhythm. Using a previously described technique, individual sleep spectrograms describing cardiopulmonary coupling were generated that demonstrate periods of stability and instability [22]. A preponderance of power in the low frequency band is associated with instability and periodic sleep behaviors, while excess power in the high frequency band is associated with physiologic respiratory sinus arrhythmia and stable/deep sleep. Low- and high-frequency coupling regimes have weak correlations with standard sleep staging but more closely follow cyclic alternating pattern (CAP) scoring. Lowfrequency coupling is associated with CAP and high-frequency coupling with non-CAP. Details of the sleep spectrogram technique are reported elsewhere [13].

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Statistical Analysis All statistical analyses were performed on an intention-to-treat basis. Baseline characteristics of the study patients were compared using t tests for continuous variables and Fisher's exact test for nominal variables. Two-sample Wilcoxon rank-sum tests adjusted for baseline scores were used to compare the distribution of changes after 12 weeks between the intervention and control groups. In addition, we compared within-group pre-post HRV statistics using Wilcoxon rank-sum tests. Metabolic stress test and Holter data for 3 patients in the control group were unavailable at 12 weeks. One patient was too debilitated to perform the tests, one refused, and one was only available for phone follow-up. For the latter patient, we were also unable to gather 6-min walk, BNP, and catecholamine measurements at 12 weeks. For these missing data, the last value was carried forward for analysis.

The mean age of study patients was 64 13 years. There was an equal gender distribution. The mean left ventricular ejection fraction was 23 7% (table 2). Most patients were on consensus-guided medical therapy. There were no statistically significant differences between the groups with regard to demographics, clinical factors, and rates of cardiovascular-related disease. Rates of other comorbid conditions were also similar, with the exception of arthritis, which was more prevalent in the intervention group (60 vs. 7%, p 0.01). Anxiety/depression was relatively common ( 40% both groups). There were no significant differences between the overall study population and the subset of patients examined in HRV and sleep analyses (n 18). At baseline, 77% of patients reported some regular physical activity at home, such as walking (range 5­65 min, 1­7 times per week).

Those who participated in Tai Chi (n 15) showed significantly improved quality of life score ( 17 11 vs. 8 15, p 0.01), 6-min walk distance (85 46 m vs. 51 58 m, p 0.01) and serum BNP levels ( 48 104 vs. 90 333, p 0.03) compared to the control group (n 15). Changes in peak oxygen uptake did not reach statistical significance, although the intervention group showed almost 1 ml/kg/min improvement, while the control group showed 0.7 ml/kg/min deterioration (table 3). There were no significant trends seen in resting catecholamine levels.

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Subject Characteristics Quality of Life, Exercise Capacity, and Neurohormones

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Table 2. Baseline characteristics of the study sample Tai Chi (n Demographic factors Age, years Men Race: Black White Asian Clinical factors Baseline ejection fraction, % New York Heart Association class score Class I Class II Class III Class IV Medications: Angiotensin-converting enzyme inhibitor -Blocker Loop diuretic Digoxin Spironolactone Cholesterol-lowering agent HF etiology Idiopathic dilated Ischemic Alcohol-related Hypertensive Peripartum Adriamycin-induced Cardiovascular-related comorbidities Coronary artery disease Implanted cardiac device1 Arrhythmia Valvular heart disease Hypertension Diabetes 15) Control (n 15) p value

66 12 10 (67) 7 (47) 8 (53) 0 24 7 2.2 1.0 4 (27) 6 (40) 3 (20) 2 (13)

61 14 9 (60) 4 (27) 9 (60) 2 (13) 22 8 2.2 0.6 1 (6.6) 9 (60) 5 (33) 0

0.67 0.71 0.28

0.43 0.19

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13 (87) 14 (93) 13 (87) 11 (73) 4 (27) 5 (33) 14 (93) 13 (87) 15 (100) 8 (53) 4 (27) 6 (40) 8 (53) 4 (27) 1 (7) 1 (7) 0 1 (7) 9 (60) 4 (27) 1 (7) 0 1 (7) 0 4 (27) 6 (40) 10 (67) 7 (47) 11 (73) 3 (20) 7 (47) 4 (27) 6 (40) 3 (20) 9 (60) 5 (33)

0.54 0.54 0.48 0.45 1.00 0.70 0.79

0.45 0.70 0.27 0.25 0.70 0.68

Reprinted with permission from Yeh et al. [12]. Values in parentheses indicate percentages. Values for age, baseline ejection fraction and New York Heart association class score are expressed as mean SD. 1 Automatic implanted cardiac defibrillator and/or pacemaker.

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Table 3. Comparison of the effects of Tai Chi versus control on mean change in outcome ( SD) during the 12-week trial Outcome measure

Minnesota Living with Heart Failure2 6-min walk, m Peak oxygen uptake, ml/kg/min Serum BNP2, pg/ml Plasma norepinephrine, ng/ml

Reprinted with permission from Yeh et al. [12]. Imputation methods (last value carried forward) were used for missing 12-week data, affecting 1 patient in the control group for Minnesota Living with Heart Failure score and serum BNP, and 3 patients in the control group for peak oxygen uptake. 2 For these variables a lower value is better. Thus, a negative between-group difference in change suggests improvement in Minnesota Living with Heart Failure score and B-type natriuretic peptide, while a positive value suggests improvement in 6-min walk.

1

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Tai Chi (n 15) Control (n 15)1 Baseline 12-week 26 412 11.4 281 1.9 Baseline 44 340 11.1 285 1.2 43 327 10.5 329 1.3 21 106 3 377 0.7 23 116 3 365 2.3 20 117 6 340 0.8 52 289 10.4 375 1.4

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12-week 25 165 6 429 0.7

Between group difference in change (95% CI) 25 ( 36, 14) 135 ( 85, 185) 1.6 ( 0.2, 3) 138 ( 257, 19) 0.35 ( 0.84, 1.54)

p value

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0.001 0.001 0.08 0.03 0.77

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Continuous ECG Recordings Standard HRV Twenty-four-hour Holter monitoring revealed no clinically important intraindividual differences in incidence of arrhythmia at baseline and 12 weeks. There were no statistically significant changes seen in the 24-hour HRV analyses. However, the Tai Chi group showed trends toward increased pNN values during sleep that were not seen in the control group. There was a marginally significant increase in pNN30 ( 10.2 12.1, p 0.049) in the Tai Chi group with pNN10, pNN20 and pNN40 approaching significance at p 0.079, 0.060 and 0.054, respectively.

Safety/Compliance

No adverse events occurred during class sessions. During the study period, 1 patient in the Tai Chi group and 4 patients in the control group were hospitalized for HF exacerbation; no deaths occurred. We did not detect any significant changes in mean blood pressure (119/72 mm Hg before vs. 117/72 after) or heart rate (75 beats per min before vs. 73 after) immediately before and after a Tai Chi session. Patients in the Tai Chi group attended 83% of classes, and 93% reported home practice (mean duration 85.5 min per week). All patients rated the classes highly (4 on a 0­4 visual analog scale for enjoyment), and 14 of 15 patients planned to continue Tai Chi after the study.

Discussion

There is a growing interest in the application of Tai Chi for patients with HF. According to a recent report on National Institutes of Health research perspectives,

Tai Chi Exercise in Patients with Chronic Heart Failure

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Sleep Spectrograms After 12 weeks, in the Tai Chi group, statistically significant improvements were seen in sleep stability, with increases in high-frequency coupling (stable sleep state: 0.05 0.10 vs. 0.06 0.09 proportion of ETST, p 0.04) and reductions in low-frequency coupling (unstable sleep state: 0.09 0.09 vs. 0.13 0.13 proportion of ETST, p 0.01), as compared to the control group. Figure 1 illustrates the effect of Tai Chi on the ECG-derived sleep spectrogram of a representative patient, with an increase in high-frequency coupling following 12 weeks of Tai Chi.

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Lo/Hi ratio

W/R C NC 0.5

0.4

HFC

Freq (Hz)

0.3

0.2

LFC

0.1

a

b

Fig. 1. Effect of Tai Chi on the sleep spectrogram. a ECG-derived sleep spectrogram at baseline for a single patient. Note high-frequency (stable sleep state) and low-frequency (unstable sleep state) cardiopulmonary coupling and spontaneous switching between states. b Increase in high-frequency coupling following the Tai Chi exposure. This change is evident across the night, and is thus distinctly different from the type of information that can be obtained from standard sleep scoring approaches. Specifically, slow-wave (delta) sleep is an increasingly small percentage of total sleep time in older adults and would thus be less useful in this assessment. C Cyclic alternating pattern; LFC low-frequency coupling;

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0 0 1 2 3 4 5 Time (h) W/R C NC 0.5 0.4

HFC

Lo/Hi ratio Freq (Hz)

0.3

0.2

0.1

LFC

0

0

1

2

3

4

5

Time (h)

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NC noncyclic alternating pattern; HFC high-frequency coupling; W/R wake or REM sleep, all derived from a single channel of ECG [5]. As polysomnographic data were not available, the sleep period was defined as the 6 night-time hours of the 24-hour period with the lowest mean heart rate. Reprinted with permission from Yeh et al. [13].

Tai Chi Exercise in Patients with Chronic Heart Failure

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application of complementary therapies to cardiovascular diseases is a funding priority, and Tai Chi is listed among areas of interest [23]. This chapter presents previously published data from the only randomized controlled trial to date on Tai Chi exercise in patients with HF. In summary, we found that a 12-week Tai Chi program can enhance the quality of life and functional capacity in patients with chronic HF who are already managed with standard medical therapy. Patients who participated in Tai Chi improved their 6-min walk distances and quality of life scores compared to patients who did not practice Tai Chi. We also observed a decrease in BNP levels, suggesting an improvement in cardiac filling pressures after Tai Chi. With traditional HRV measures, there was a trend towards increased shortterm HRV during sleep in the Tai Chi group, suggesting an improvement in cardiac vagal modulation. In patients with comparable HF severity, similar changes in exercise tolerance have been shown with conventional exercise. Trials using step aerobics, treadmill, bicycle, arm or rowing ergometer have reported increases of 10­20% in 6-min walk distance and increases of 12­31% in peak VO2 [24], With Tai Chi, we report a comparable increase of 25% in 6-min walk distance. Results of quality of life measures in conventional exercise trials have been mixed [24, 25], while we report significant improvements. Similar to our findings, conventional exercise trials have failed to show consistent changes in resting norepinephrine and epinephrine [24, 26]. In the retrospective sleep analysis, we found that a 12-week Tai Chi program can improve sleep stability. An increase in stable sleep may be a robust marker of overall improved sleep quality. For patients with HF, unstable sleep may cause excessive hemodynamic stress through respiratory and nonrespiratory mechanisms, and may be associated with ventricular arrhythmias [27]. In contrast, stable sleep is associated with stable respiration and hemodynamics and may protect from triggered arrhythmias. Improvements in sleep stability may have potentially important restorative effects on chronic HF pathophysiology. Sleep stability has not previously been described with Tai Chi, although one prior trial reported improvements in sleep quality, latency, and duration after 24 weeks of Tai Chi compared to conventional low-impact exercise [28]. Changes in sleep quality have also been demonstrated with other meditative practices, such as mindfulness-based stress reduction and yoga [29, 30].

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Tai Chi appears to be a safe alternative to conventional exercise. Adverse events in the Tai Chi literature are lacking. In conventional exercise trials, cases of worsened HF, arrhythmias, and hypotension have been reported, and minor musculoskeletal injuries are common [2]. In contrast, Tai Chi encourages patients to move fluidly with less strain and may be beneficial for patients with musculoskeletal conditions [5]. While we report encouraging preliminary results, we recognize important study limitations. First, our sample was small and likely underpowered to detect differences in certain measures, e.g. peak VO2 and standard HRV. With a wait-list control, patients were not blinded to treatment assignment, and we were unable to control for social interaction. Any social effect on mood or perceived quality of life, however, would be unlikely to account for the magnitude of change we observed in exercise capacity. For the retrospective sleep analysis, polysomnographic data were not available to correlate our results. In many ways, Tai Chi appears to be an optimal exercise for patients with HF. Tai Chi's gentle, low-impact, nonstrenuous movements may be suitable for persons with a wide range of functional capacities, including the elderly and more severely deconditioned, e.g. NYHA Class IV patients. Emphases on efficient breathing and stress reduction also address important cardiorespiratory processes. Further, Tai Chi can be practiced in any environment, and requires no equipment, possibly offering a cost advantage. Despite this favorable profile and promising preliminary evidence, the exact mechanisms of Tai Chi are not well understood. Ongoing investigations at Harvard Medical School and Beth Israel Deaconess Medical Center in Boston continue to explore the role of Tai Chi exercise in the care of patients with HF. Currently, a larger randomized controlled trial is underway that includes an attention-matched comparison, controlling for group social effect. In addition to exercise capacity and quality-of-life, an expanded list of outcomes includes left ventricular hemodynamics, serum biomarkers of cardiac and immune function, mood, and exercise self-efficacy. Other investigations are comparing Tai Chi with conventional aerobic exercise, and qualitative analyses are exploring patient experiences, expectations, and belief systems. Further studies might also define the population most likely to benefit from meditative exercise and investigate whether benefits can be sustained or increased. Clearly, Tai Chi is a rich, complex, multimodal intervention. The challenge will be to design research studies that can appropriately study such an intervention and provide us meaningful insights regarding meditative exercise and its potential application in a clinical setting.

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Gloria Y. Yeh, MD, MPH Harvard Medical School Osher Institute 401 Park Drive, Suite 22A Boston, MA 02215 (USA) Tel. 1 617 384 8550, Fax 1 617 384 8555, E-Mail [email protected] Yeh/Wayne/Phillips

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