Heart failure (HF) is one of the most prevalent chronic illnesses of modern times, with a profound clinical and economic impact on society (4,21,24). The symptoms of the disease significantly reduce quality of life (QoL) among those who live with HF (5). According to the Centers for Disease Control and Prevention, African American (AA) patients on Medicare are hospitalized for HF more frequently than any other medical condition (9). In patients with either systolic or diastolic HF, the symptoms of the disease usually limit functional capacity (34). Previous studies have supported interventions aimed at treating the symptoms of HF, improving QoL, and overall health-related outcomes (37). Physical exercise in the form of yoga has gained immense popularity (17) and may be beneficial in cardiac rehabilitation (8). Despite yoga's widespread appeal, there are limited data on whether the addition of yoga improves symptoms or health-related QoL in patients with chronic HF (29).
Yoga combines structured physical exercises with breathing techniques and meditation to stimulate a sense of well-being. The breathing, relaxation, and meditation components may lead to an improvement in baroreflex sensitivity and a reduction in HR variability as a result of reduced chemoreflex response to hypoxia and hypercapnia (6,7). Decreased sympathetic activation and improvement in baroreflex sensitivity may also affect a reduction in hypertension, which significantly impacts HF and other cardiovascular diseases. Although the exact mechanisms remain hypothetical, a variety of beneficial effects for patients with cardiovascular disease have been reported. For example, studies have demonstrated an improvement in lipid profiles (20), blood pressure (30), psychological well-being, and even regression of atherosclerosis when combined with dietary and other lifestyle modifications (25,36). The clinical application of the previous studies may be limited by the lack of control groups and by the varied style, intensity, and duration of the yoga interventions.
Proinflammatory markers have been associated with unfavorable cardiovascular outcomes in HF (27). Elevated levels of interleukin-6 (IL-6) and high-sensitivity C-reactive protein (hs-CRP) have been adversely associated with HF (10,39); extracellular superoxide dismutase (EC-SOD) activity has been correlated with endothelium-mediated, flow-dependent vasodilatation (19). A search of the medical literature found that the pilot study for this research was the only published investigation on yoga and inflammatory markers (29).
A randomized control group design was used to study the effects of an 8-wk, low-intensity, yoga program on the peak cardiovascular capacity, QoL, and inflammatory markers in a predominantly AA group of patients with systolic and diastolic HF. We also examined the effect of yoga on the flexibility, weight, and girth measurements in these stable HF patients.
Forty patients were recruited prospectively from the outpatient cardiology clinic at Grady Memorial Hospital in Atlanta, GA. All patients had systolic or diastolic HF of ischemic or nonischemic etiology. Patients were randomized to a supervised hospital-based yoga group (YG) or a control group (CG), in addition to standard medical care. Patients were included if they had 1) systolic HF [ejection fraction (EF) ≤45%] or diastolic HF (EF >45%), 2) New York Heart Association (NYHA) class I-III, 3) were able to walk without assistance, and 4) were on stable medical therapy for HF at least 3 months before enrollment.
Patients were excluded if they 1) had a life expectancy <6 months, 2) were unable to walk without an assistive device, 3) were pregnant or breast-feeding, 4) were unable to attend yoga sessions twice a week, or 5) were currently addicted to alcohol or drugs. The study was approved by the Institutional Review Board at Emory University and by the Institutional Review Board of Georgia State University. Patients who were eligible for participation in the study were appropriately screened and enrolled after obtaining informed consent.
Pretest and posttest assessments.
Patients were scheduled for initial assessment at the Vascular Laboratory located at Grady Healthcare System's main hospital in Atlanta, GA. Pretesting and subsequent appointments followed in a timely fashion.
Cardiovascular parameters included resting systolic blood pressure in right and left arms, 12-lead ECG, and treadmill stress test. The sit-and-reach test for flexibility (best of three attempts), girth measurements, the Minnesota Living with Heart Failure Questionnaire (MLwHFQ), and venipuncture for serum biomarkers (IL-6, hs-CRP, and EC-SOD) were also obtained during the assessment visits. Serum markers were drawn before the treadmill test in a resting state. Patients were asked to take medications as usual and fast for 2 h before the pretest and posttest appointments. Both groups received HF patient education, and a brochure with instructions for following a home walk progression (standard medical treatment). Documentation of current exercise behavior and exercise history was recorded during the initial visit and on completion of the study. Investigators responsible for assessment of outcomes were blinded to the treatment assignment.
One-hour yoga sessions were conducted twice per week in a quiet room located within Emory University's Vascular Laboratory. Patients randomized to yoga were given a yoga mat and strap for their personal use. Blood pressure and HR were recorded before and after each class. Patients attended a total of 16 supervised sessions during an 8- to 10-wk period. During each session, subjects completed the following: a 5-min warm-up phase including breathing exercises (pranayama), a 40-min period of standing and/or seated yoga postures (asanas), and finally, a 15-min relaxation phase. On completion of the first four classes, patients were given a handout of the 18 yoga postures taught during class (28). The YG patients were asked to practice at home with a goal of three yoga sessions per week. The yoga sessions were conducted by a Registered Yoga Teacher (RYT-Yoga Alliance®) and certified by the American College of Sports Medicine (ACSM Registered Clinical Exercise Physiologist®), with more than 20 yr of experience in the field of cardiac rehabilitation. The yoga asanas for this study included traditional hatha yoga postures including combinations of forward and backward bends, twists, and balance poses. Modifications were made on an individual basis according to individual medical and orthopedic limitations. Chairs were used for patients unable to get up from the floor unassisted, and a wall was incorporated during the standing balance postures, as needed.
Breathing exercises consisted of slow, deep inhalation and exhalation through the nasal passageways in a one-to-longer-than-one ratio, without breath retention. Inhalation was taught to begin with sequential involvement of the abdomen, lower chest, and then upper chest, with the same sequence in reverse, during exhalation. Meditation and relaxation were performed in a supine or seated position according to the patient's comfort level.
All patients performed a graded exercise test at baseline (pretest) and at the conclusion of the 2-month study period to determine exercise capacity (Model: Case12 EKG and Marquette 2000 treadmill; Marquette Electronics, Inc., Milwaukee, Wisconsin). V˙O2peak was estimated on the basis of the workload at peak exertion using the ACSM's standard formula for treadmill walking (38):
A 1-min-per-stage ramp protocol treadmill test was used for all pretreadmill and posttreadmill tests (29).
Additional baseline and posttest measurements included EKG, blood pressure, flexibility (sit-and-reach test), and girth. Waist circumference was measured at the narrowest part of the torso, and hip circumference was obtained at the maximum extension of the buttocks.
Measurement of soluble levels of IL-6, hs-CRP, and EC-SOD.
Venipuncture was performed at baseline and at the conclusion of the study. Plasma samples were centrifuged and stored at −80°C. An aliquot was drawn, and enzyme immunoassay (Cayman Chemical, Ann Arbor, MI) for serum IL-6, hs-CRP, and EC-SOD was performed on each sample in triplicate. A total of 50 µL of serum was used for analysis, and enzyme immunoassay was performed as previously described (15). The levels of total serum IL-6, hs-CRP, and EC-SOD were determined on a plate reader at an optical density of 420 nm.
QoL was assessed with the MLwHFQ (15). This disease-specific questionnaire is the most widely used and validated assessment of QoL in patients with HF. The MLwHFQ is composed of 21 questions addressing physical function, symptoms of HF, and psychosocial issues. The participants completed the questionnaire at enrollment and again at the end of the study.
Statistical analyses were conducted using the Statistical Package for Social Sciences 16 (SPSS, Inc., Chicago, IL). Means and SD were computed for continuous variables, and paired t-test comparisons for within-groups analyses of pretest and posttest findings were conducted. A one-way ANOVA was conducted on all measured variables between groups for comparisons of pretest to posttest differences. Confounding factors were adjusted for at baseline.
The study was concluded after subjects completed 16 yoga sessions, which typically required 8-10 wk. The primary end points were a change in estimated V˙O2peak for the YG compared with the CG, derived from the ramp protocol treadmill test and the time to peak exertion. The secondary end points were improvement in inflammatory markers, flexibility, and QoL indicators. We hypothesized that YG would fare favorably over CG on these primary and secondary findings.
Ninety-one patients were interviewed initially regarding study participation. Fifty-one patients did not meet various eligibility criteria or declined to participate. Forty patients (17 females and 23 males) enrolled in the study, with an age of 31-76 yr. Twenty-one patients were randomized to the YG, and 19 were randomized to the CG. Three YG patients did not complete the study, and three CG patients did not return for posttesting. All of the YG patients who completed the study attended 16 yoga sessions within 8-10 wk of their initial class. Two of the YG patients were not AA, a female Asian and a male Caucasian, and were included in the statistical analysis.
There were no significant differences between the groups in age, left ventricular EF, resting HR, blood pressure, body weight, body mass index, flexibility, treadmill test time, V˙O2peak, QoL scores, or biomarkers at baseline. Of subjects completing the study, 1 (6%) of 18 of the YG had diastolic dysfunction, whereas 17 (94%) of 18 had systolic dysfunction. For the CG patients (n = 16) who completed the study, 3 (19%) of 16 had diastolic dysfunction and the remaining 13 (81%) of 16 patients had systolic dysfunction. Nonischemic HF was the dominant diagnosis on the basis of clinical history (Table 1).
Pretest to posttest differences between the groups were significant for treadmill time and V˙O2peak (P = 0.002, P = 0.003; Figs. 1 and 2). The YG increased their treadmill time by 22% after the yoga intervention, whereas the CG's time decreased by 5% (Table 2).
Soluble inflammatory markers.
There were statistically significant differences within group improvements in the plasma serum levels of the three biomarkers for YG patients (Table 3). IL-6 decreased from a mean value of 19.6 ± 2.5 to 16.0 ± 2.1 mg·dL−1 (P < 0.001, n = 21) and hs-CRP decreased from 2.4 ± 0.58 to 1.9 ± 0.4 mg·dL−1 (P < 0.001). Levels of EC-SOD increased from 509 ± 71.9 to 610 ± 86.2 U·mL−1 (P < 0.001). Furthermore, between-group comparisons from pretest to posttest were significant for YG improvements (IL-6, P < 0.001; hs-CRP, P = 0.001; and EC-SOD, P < 0.001; Table 2).
There was a significant change from pretest to posttest for the total scores and physical subscale scores for the MLwHFQ within the YG (Table 3). No significant changes were found in the paired samples analysis for the CG. Other significant improvements within the YG from pretest to posttest were for improved flexibility (P = 0.002).
Despite significant advances in medical and surgical management of HF, the 1-yr mortality rate for patients with advanced HF remains approximately 35% (24). Prognosis may be better in patients within the early stages of HF, but patients continue to experience considerable symptoms, deterioration in functional status, and a poor QoL (5). Psychosocial factors and reduced QoL contribute to recurrent HF exacerbations and hospitalizations (26,40). The present study is unique in that there were no yoga studies in the medical or scientific literature that used a randomized control design while examining the clinical effects of yoga on HF patients. There are few data on the unconventional techniques of mind-body medicine specific to HF patients.
The addition of an organized program of yoga for 8 wk to standard medical treatment of HF led to an improvement in V˙O2peak, exercise capacity, flexibility, and reduced inflammatory markers. Mechanisms by which yoga may have improved the clinical parameters in this study are speculative at this time. In addition to hemodynamic dysfunction, an increased neurohormonal activation via the sympathetic nervous system and the renin-angiotensin system has been implicated in the progression of HF (31). Indeed, drugs such as β-blockers and ACE-I/ARB that block this neurohormonal activation, leading to a reduction in morbidity and mortality in patients with HF (1,2). HR, blood pressure, and the respiratory rate interval are all influenced by input from both the parasympathetic and the sympathetic systems. Arterial baroreflex modulates vagal nerve traffic to the sinoatrial node. In postmyocardial infarction patients, it has been observed that if the vagal baroreflex is abnormal, there is an increased risk of fatal events due to ventricular tachycardia (18). In addition, arterial baroreflex insensitivity may lead to ventricular arrhythmias (22). Combining yogic postures with breathing exercises and meditation attenuates sympathetic activation and could lead to a decrease in ventricular filling pressures. This may explain part of the improvement in exercise capacity that was found in this study (on the basis of the significant improvement in treadmill time and estimated V˙O2peak in the YG compared with that in the CG).
Yoga postures, relaxation, and breathing practices may improve patient well-being and retard the pathogenic mechanisms observed in HF. Dyspnea in chronic HF results in muscle fatigue from decreased arterial CO2 (13). Dyspnea requires an increased ventilatory effort, driven by sympathetic activation, which predisposes patients to ventricular arrhythmias. In addition to allowing for a predominance of the parasympathetic state, yoga may also promote effective extraction of oxygen by peripheral tissues. When muscle is stretched, the O2 consumption increases. Studies that examined the health-related aspects of yoga found that an 8-wk yoga training program increased muscular strength by 31%, increased muscular endurance by 57%, increased flexibility by 88%, improved oxygen uptake by 7%, and reduced cardiovascular risk in healthy adults (36). These data seem to support the current study's increase in exercise tolerance in the YG, as reflected by longer treadmill times and an increase in V˙O2peak. Flexibility increased significantly in the current study, which was anticipated because the sit-and-reach test is a replication of one of the yoga postures in the routine. It was encouraging to find that, despite their comorbidities, age, and poor EF, the YG patients were able to improve their flexibility.
Studies of yoga treatment in hypertensive patients have demonstrated mean reductions of systolic and diastolic blood pressure of 10-15 mm Hg (23,30). The insignificant blood pressure and HR changes in this cohort may have been influenced by medications and the fluctuations in body weight noted throughout the study.
In addition to the proposed mechanism of yoga's ability to attenuate the derangements of the autonomic nervous system, and thereby improve symptoms, its effect on psychological well-being may be a benefit as well. Major clinical depression occurs in 25% of patients with HF, and 50% report symptoms consistent with subclinical depression or dysthymia (14), which in turn affect patient QoL and raise mortality (12). Increased serum catecholamine levels due to stress cause deleterious effects on cardiac health and immune function (11,16).
In this study, answers to the well-validated MLwHFQ indicated that patients who participated in yoga perceived it to be beneficial. Statistical significance was reached for total scores and for the physical improvement subscale, which is congruent with a positive QoL effect. The emotional subscale failed to reach significance possibly owing to a few extraneous incidents that occurred to a couple of the YG participants during the study (one patient's brother died unexpectedly and another's husband was placed in a hospital intensive care unit).
The yoga treatment patients reported an improved tolerance for the activities of daily living. Another important factor to consider is that modified yoga postures can be practiced safely by persons with disability, the elderly, and by patients with chronic debilitating illnesses such as arthritis and HF compared with the conventional aerobic forms of exercise that can be too physically demanding. There were no adverse outcomes in patients in the YG, and they tolerated this form of nonaerobic exercise quite well. Interestingly, compliance for the yoga sessions and testing appointments was 85% for both the treatment and control subjects.
Although clearly changes in inflammatory markers, especially hs-CRP, have been debated, this is not the central focus of this study. However, increased levels of markers of inflammation such as IL-6 and hs-CRP have been associated with higher mortality in cardiac patients (27). These data suggest that yoga may improve endothelial function by decreasing inflammation and oxidative stress at the level of vasculature reactivity. The levels of all three biomarkers improved after 8 wk of yoga compared with the CG. These results are noteworthy: hs-CRP decreased by 20% in the YG compared with 1.6% in the control group; IL-6 decreased by 22% in the YG compared with minimal change from baseline in the CG (Table 2). This is consistent with the effect cardiovascular exercise has on markers of inflammation in patients with chronic HF (3). Both forms of activity may also improve endothelial function by increasing levels of EC-SOD and NO activity (35). Recently, a pilot study demonstrated that after 6 wk of yoga participation, brachial artery reactivity improved only in the CAD patients, as opposed to individuals at risk for CAD (32). Thus, in patients with HF, yoga may improve functional capacity and QoL by lowering sympathetic response to physical activity, leading to a reduction in cytokines and oxidative stress resulting in improved vascular reactivity.
Home walking assessment and compliance were self-reported during the patient interview, at the pretest and posttest visits. The self-reported weekly walking time (n = 10, 5 YG and 5 CG) in minutes revealed a significant increase in walking time from pretest to posttest (P = 0.046) with no significant difference between the YG and CG. This implies that study participation had an independent effect on walking behavior. In future studies of this nature, a pedometer or accelerometer and an activity questionnaire could be used to more objectively measure activity away from the laboratory.
Study limitations included the use of self-report for the assessment of home walking adherence and reliance on the exercise log for the documentation of home activities. These methods have obvious limitations. Patients are required to be disciplined enough to keep accurate records that are not always reliable. Long-term follow-up of the patients' adherence to the yoga and walking would also have been desirable but were not practical using the current protocol.
Ninety-five percent of the study patients were AA because of the makeup of the inner city hospital clinic from which the patients were recruited. The results of this study may have applicability to HF patients in general; a larger study with multiracial HF patients would be helpful toward answering this question. The relatively small number of subjects in this study is also a potential weakness. The decision to include patients with diastolic dysfunction was based on recent findings from the study by Smart et al. (33), who concluded that both patient groups (i.e., patients with diastolic dysfunction and systolic dysfunction) could respond to exercise training favorably with similar improvement in V˙O2peak and also QoL. The significant difference found in the mean values of the EF of the systolic dysfunction only patients is of questionable clinical relevance and may have been due to the smaller number of patients in that analysis.
This study of the effect of yoga on exercise capacity, inflammatory markers, and QoL in predominantly AA HF patients indicates that yoga may provide a beneficial adjunctive therapy and may be safely added to standard medical care under similar circumstances. Markers of inflammation such as IL-6, hs-CRP, and EC-SOD showed a significant improvement with an 8-wk yoga-based program in patients with compensated systolic and diastolic HF. Larger patient groups and longer-term studies that control for physical activity are needed to further delineate the mechanisms of improvement that are unique to yoga. Future investigation with additional measurements of brachial artery reactivity, myocardial contractility, accelerometer recordings, depression inventories, and symptom rating scales, in a head-to-head comparison with exercise therapy, may further delineate the benefits and mechanisms of yoga as an adjunct treatment of HF. The sustained body weight and girth of the study groups not only points to the need to include weight loss interventions in future studies but also implies that the benefits of yoga demonstrated in our findings were independent of weight loss. In conclusion, yoga offered additional benefits to HF patients in regards to, exercise capacity, QoL, inflammatory markers, a precursor of nitric oxide (EC-SOD), and flexibility when compared with a group of HF patients who received standard medical care.
The study was partially funded by the John and Rosalie Weiss research grant from the ACSM.
The authors thank Hugger Mugger Yoga Products, LLC, for donating yoga products to the study. The results of the study do not constitute endorsement by the ACSM. None of the authors have any conflict of interest.
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