Yoga is a Sanskrit term meaning “union” or “connection.” More figuratively, it is the union of the soul “atman” with “paramatman,” the absolute or supreme soul (ie, God). It is a combination of physical postures (asana), breathing exercises (pranayama), and meditation (dhyana), performed to attain harmony between the body, mind, and soul, with the ultimate goal of liberation (moksha) of the soul. While the philosophy and practice of yoga date back to the pre-Vedic times in the Hindu tradition, it was introduced to the West only in the late-19th and early-20th centuries. Despite the general acceptance and incorporation of yoga in the West for the last few decades, it remained confined to the realm of alternative medicine until the beginning of the 21st century. Over the last 10 to 15 yr, the concept of yoga has gained increasing attention in the medical scientific community due to a greater recognition and understanding of the mind-body connections in numerous medical disorders. In addition to reigniting the interest in yoga, this has led the medical scientific community to pursue evaluation of the role and benefits of yoga using the current paradigms of evidence-based medicine. This review provides an overview of the emerging evidence assessing the physiologic and clinical effects of yoga on the cardiovascular (CV) system and the potential role of yoga as a component of comprehensive cardiac rehabilitation (CR).1
REVIEW OF RELEVANT LITERATURE
The exact origins and evolution of yoga are unclear and continue to be debated.2 It is the current understanding that yoga originated in ancient India with the earliest descriptions attributed to the Indus valley civilization (3300-1900 BCE).3 Subsequent refinements are attributed to pre-Vedic eastern states of India,4 the Vedic period (1500-500 BCE), and the “sraman.a” movement, an Indian religious movement emphasizing austerity.5 The history of yoga can be conveniently divided into the following 4 broad phases: Vedic yoga (1500-500 BCE), pre-classical yoga (500-200 BCE), classical yoga (200 BCE to 500 CE), and post-classical yoga (500-1500 CE).6 Considered the foundation of Hinduism, the Vedas (“praise of knowledge”) contain early proto-yogic ideas and practices that are vaguely defined. In the pre-classical era, yoga began to take a more definite form with clear documentation of the philosophy and principles in scriptures such as the Upanishads. The Yoga Tattva Upanishad contains explicit discussions of yoga pertaining to posture, breathing exercises, and mental training. It was during this era that the doctrine of Karma yoga (the path of action or ritual) and Jnana yoga (the path of knowledge) originated.7
Patanjali's (∼600-400 BCE) Yoga-Sutra (aphorisms of yoga) is considered the foundation for the current practice of yoga. It has the most extensive commentary on yoga and consists of 196 aphorisms or sutras (threads) that describe the 8-fold path of yoga (also called the 8 limbs of classical yoga). This was the classical period of yoga and is also referred to as the yoga-darshana or raja-yoga. Over time, non-classical schools have led to the development of post-classical yoga.7 The post-classical era resulted in the evolution of many new branches of yoga, such as Tantra yoga, Siddha, and Hatha “body” yoga. Around the dawn of the 20th century, prominent Hindu philosophers and monks such as Swami Vivekananda introduced modern Hinduism, vedantic philosophy, and yoga to the West. Subsequently, noted gurus such as Swami Kuvalayananda and Yogendraji disseminated the systematic practice of yoga more widely. In addition, they established a scientific platform by initiating research and starting centers for learning, research, and dissemination of yoga.
In the last 3 decades, yoga has gained popular acceptance in the United States and hundreds of yoga centers have emerged across the country.8 It is estimated that the number of people who practice some form of yoga in the United States has grown from 4 to 36.7 million between 2001 and 2016, with an estimated $16 billion spent annually.9 In 2014, the United Nations General Assembly approved a resolution establishing June 21 as “International Day of Yoga,” and the first International Day of Yoga was observed in 2015. Multiple types of yoga are currently popular including Iyengar, Bikram, Kundalini, Integral, Yin, Vinyasa, Jivamukti, Anusara, and Vinyoga. A detailed description of the different types of yoga is beyond the scope of this article, but the frequently practiced forms are summarized in Figure 1.
PHYSIOLOGICAL EFFECTS OF YOGA
An extensive body of literature supports the favorable neurohumoral effects of yoga such as decreased serum cortisol, catecholamine, and aldosterone levels. Chronic activation of the aforementioned pathways has been described in a majority of CV disease states including hypertension and heart failure (HF). In addition, yoga and meditation have been found to increase melatonin, γ-amino butyric acid, and a myriad of other neurotransmitters. Importantly, a decrease in stress markers, such as 8-hydroxydeoxyguanosine, and an increase in endorphin levels with yoga strongly suggest its role in mitigating the effects of stress in humans.10 In addition, the regular practice of yoga is known to attenuate oxidative stress and improve endothelial function by enhancing bioavailability of nitric oxide.11,12 There is now clear evidence regarding the role of inflammation in the pathophysiology of coronary artery disease (CAD) and other vascular diseases. Systemic inflammation is a strong predictor of all-cause mortality.13 Yoga has been shown to have anti-inflammatory and insulin-sensitizing effects by increasing adiponectin levels and decreasing leptin resistance.14 Mindfulness-based meditation can reduce pro-inflammatory response gene profiles,15,16 and yogic meditation appears to reverse nuclear factor-κB-related transcription of pro-inflammatory cytokines.17
Kiecolt-Glaser et al18 assessed CV, inflammatory, and endocrine responses in novice and expert yoga practitioners before, during, and after a Hatha yoga session. These responses were also tested in 2 control conditions (light walking and no activity). The study showed significantly lower serum interleukin-6 levels in experts compared with novice yoga practitioners, and the odds of having detectable high-sensitive C-reactive protein were 4.8 times higher in a novice compared to experts. In a meta-analysis of 34 studies involving 2219 participants assessing the effects of mind-body therapies on the immune system, Morgan et al19 concluded that mind-body therapies may reduce markers of inflammation and favorably influence cell-mediated immune responses. However, this meta-analysis was not limited to yoga alone. The physiologic effects of yoga on the CV system are summarized in Figure 2.
EFFECTS OF YOGA ON CARDIOVASCULAR RISK FACTORS
Several investigators have studied the impact of yoga on the spectrum of traditional CV risk factors such as diabetes, hypertension, hyperlipidemia, and smoking. In a comprehensive meta-analysis of 44 randomized controlled trials (RCTs), Cramer et al20 demonstrated the beneficial effects of yoga (P < .05) on blood pressure (BP), heart rate (HR), abdominal obesity, measures of insulin resistance, and blood lipid levels, when compared with usual care, both in healthy participants and high-risk patients. In the yoga group, systolic blood pressure (SBP) decreased by a mean of 6 mm Hg, diastolic blood pressure (DBP) by 4 mm Hg, HR by 7 beats/min, waist circumference by 2 cm, and hemoglobin A1c by 0.5%. In addition, there were significant improvements in low-density lipoprotein cholesterol, with a mean decrease in total cholesterol of 13 mg/dL, of 6 mg/dL, and triglycerides of 21 mg/dL, as well as an increase in high-density lipoprotein cholesterol of 3 mg/dL. Similar results were reported by Chu et al21 in a systematic review and meta-analysis from 2016. However, in this analysis, the effect of yoga was comparable to exercise therapy. In a “systematic review of systematic reviews” on the effect of complementary and alternative medicine in lowering blood lipid levels, Posadzki et al22 noted an overall positive effect of yoga.
Metabolic syndrome is currently considered a global public health epidemic, and lifestyle modification is the cornerstone of management. Khatri et al23 randomized 101 patients with metabolic syndrome to a control group or a yoga intervention group for 3 mo. At the end of 3 mo, waist circumference, SBP, DBP, fasting blood glucose, HbA1c, serum triglyceride, and serum high-density lipoprotein cholesterol levels improved significantly in the yoga group compared with the control group. Similarly, in 184 pre-hypertensive patients, Thiyagarajan et al24 demonstrated significant improvements in SBP, waist circumference, HR, and fasting blood glucose after 12 wk of a combination of lifestyle measures and yoga therapy compared with lifestyle measures alone. However, a recent 2016 meta-analysis of 7 randomized trials by Cramer et al25 noted that, except for reduction in SBP and waist circumference, no significant improvements were observed in the individual components of metabolic syndrome with yoga practice. Nonetheless, until further evidence is available, yoga should certainly be considered an effective option to reduce waist circumference and SBP in addition to other lifestyle measures.
According to data from the INTERHEART study, smoking ranks second only to hypercholesterolemia as the strongest risk factor (3-fold increased risk) for myocardial infarction.26 By targeting stress and behavioral urges associated with craving, yoga is increasingly being recognized as a promising complimentary therapy in addition to conventional medical therapy for smoking cessation. Numerous forms of yoga such as Ashtanga, Hatha, Vinyasa, and Yin yoga, through exercise and movement, enhance mood, reduce negative affect, and decrease the severity of withdrawal symptoms. Bock et al27 studied the efficacy of yoga as a complementary therapy for smoking cessation in 55 women who received an 8-wk group-based cognitive-behavioral therapy and were randomized to either a twice-weekly Vinyasa yoga program or wellness program (control group). Seven-day point-prevalence abstinence rates were significantly higher in the yoga group compared with controls (OR = 4.6). At 6 mo, although the abstinence rates remained higher in the yoga group, the difference did not reach statistical significance. In a 2013 systematic review of 14 clinical trials, including 8 RCTs, on the effect of mind-body interventions on smoking cessation, Carim-Todd et al28 reported favorable changes in smoking behavior and predictors of smoking behavior with these interventions. Of the 14 studies included in this meta-analysis, only 3 assessed the effects of yoga on smoking cessation. Chu et al,29 using published literature on risk factor reductions through diverse lifestyle interventions (ie, walking, Mediterranean diet, and group therapy smoking cessation) found in the base-case analysis, concluded that yoga was associated with the largest 10-yr CV disease risk reduction (maximum absolute reduction 17% for the highest-risk individuals). In summary, all of the above evidence suggests that, in this era of individualized medicine, yoga could potentially be used as a lifestyle modality for effective primary and secondary prevention of CV disease due to its favorable impact on multiple traditional and emerging CV risk factors.
IMPACT OF YOGA IN SPECIFIC CARDIAC DISEASE STATES
Over the last decade, several studies have described the impact of yoga on moderating the effects of various cardiac disease states including autonomic dysfunction, arrhythmias, CAD, and HF.
In addition to the traditional risk factors described earlier, cardiac autonomic dysfunction, as evidenced by reduced HR variability and baroreflex sensitivity, has been identified as an independent predictor of CV mortality and myocardial infarction.30,31 Beyond its effects on the traditional CV risk factors, yoga has been demonstrated to favorably impact autonomic tone. In a systematic review of 59 studies assessing 2358 patients, Tyagi and Cohen32 concluded that yoga increased HR variability, increased vagal output, and decreased sympathetic arousal. Furthermore, given the bidirectional flow of the vagus nerve, it is believed that the practice of yoga directly influences the central nervous system, resulting in favorable emotional, cognitive, and behavioral responses.33
Enhanced automaticity, triggered activity, and re-entry are key factors in the initiation and maintenance of cardiac arrhythmias. Yoga can potentially decrease arrhythmias by reducing sympathetic nervous system activity and promoting parasympathetic output, thereby decreasing automaticity. In the “Yoga My Heart” study, Lakkireddy et al34 prospectively enrolled 52 patients with symptomatic paroxysmal atrial fibrillation to examine the effects of a structured 3-mo yoga program on atrial fibrillation burden, quality-of-life indicators, anxiety, and depression. After a 3-mo control period, an Iyengar yoga intervention was performed twice-weekly for 60 min for 3 additional mo. From the end of control phase to the end of intervention phase, yoga significantly reduced the number of symptomatic (3.8 ± 3 vs 2.1 ± 2.6) and asymptomatic (0.12 ± 0.44 vs 0.04 ± 0.20) atrial fibrillation episodes. Similarly, anxiety and depression scores, BP, and HR significantly improved during this period. This study established yoga as a favorable adjunct to medical therapy for paroxysmal atrial fibrillation. In addition, Wahlstrom et al35 reported improved mental health scores in patients with paroxysmal atrial fibrillation after a 12-wk yoga program involving light movement and deep breathing. The effects of yoga on other forms of atrial fibrillation have not been studied to date. One RCT by Toise et al,36 involving 46 patients treated with implantable cardioverter defibrillator for life-threatening arrhythmias, noted no mortality benefit of yoga at 8-mo follow-up, but the number of nonfatal device-treated ventricular events was lower in these patients compared with the control group. Further research is necessary to establish the significance of yoga as a potential therapeutic option in the management of arrhythmias.
Coronary Artery Disease
Patients with established CAD are at increased risk for future coronary events and death. Secondary prevention, which includes medications and lifestyle modifications, has been shown to reduce this risk significantly. Pal et al37 randomized 170 patients with CAD to either yoga (35-40 min/d, 5 d/wk) or non-yoga routine care in a 1:1 fashion for 6 mo and demonstrated significant reductions in body mass index, SBP, DBP, HR, total cholesterol, triglycerides, and low-density lipoprotein. However, the sample size and follow-up duration of the study limited the assessment of the impact of yoga on recurrent coronary events. A systematic review of 4 RCTs involving 510 patients with CAD by Cramer et al38 in 2015 concluded that there was no significant evidence supporting mortality benefits of yoga in CAD when added to conventional medical therapy. Of the 4 RCTs, 1 RCT reported significant reduction in the number of episodes of angina per week and 1 other RCT found a larger increase in exercise time in the yoga group compared with the control group.38 In another report, transcendental meditation was shown to significantly reduce risk of mortality, myocardial infarction, and stroke in African Americans with CAD in a randomized control trial comparing health education and routine medical therapy to yoga in addition to routine medical therapy and education.39 Lastly, a 2015 Cochrane database review by Kwong et al40 could not identify any statistically significant benefits of yoga with respect to all-cause mortality, CV mortality, CV-related hospital admissions, or quality of life in patients with established CAD. Thus, despite the beneficial effects of yoga on numerous CV risk factors, there is currently no evidence demonstrating reduction in major clinical events like myocardial infarction and mortality with yoga.
Increased neurohormonal activation via the sympathetic nervous system and the renin-angiotensin system is key factors in the progression of HF. Drugs blocking these systems have been shown to have mortality benefit in patients with chronic HF. Through its modulatory effects on the autonomic nervous system, yoga is known to reduce HR and BP in patients with HF.41 In addition, yoga programs have been shown to improve physical function measures such as balance, strength and endurance, and symptoms in patients with chronic HF.42
Krishna et al,43 in an RCT of 130 patients with systolic and/or diastolic HF (left ventricular ejection fraction 30%-50%), demonstrated significantly greater improvements in left ventricular function with 12 wk of yoga compared with standard medical therapy without yoga. Two RCTs from Pullen et al,44,45 involving a total of 59 patients with chronic HF (New York Heart Association I-III), did not find any significant difference in mortality when yoga was added to conventional medical therapy for a period of 8 wk. However, exercise time was longer and maximal oxygen consumption was greater in the yoga group compared with the conventional medical therapy-only group. Nonetheless, the long-term effects of yoga in HF, particularly on hospitalization and mortality, have not been adequately studied. The Table summarizes the effects of yoga in specific cardiac disease states.
APPLICATION TO PRACTICE
INCORPORATION OF YOGA INTO CURRENT MEDICAL PRACTICE AND CARDIAC REHABILITATION
Despite the fall in mortality rates over recent decades, there are still over 610 000 deaths associated with heart disease every year, with CAD and HF contributing to the majority of these. CR is a comprehensive mix of patient education, risk factor modification, stress management, and exercise training tailored to individual patient needs. The American Heart Association and the American College of Cardiology guidelines have endorsed CR in the management of CAD, and systolic HF,46 and the American Association of Cardiovascular and Pulmonary Rehabilitation has produced 5 editions of guidelines for CR programs since 1991, describing processes leading to program effectiveness. Because of its holistic, mind-body approach to decreasing stress, favorably impacting CV risk factors, and improving an overall sense of well-being, yoga is a potentially invaluable tool in the armamentarium of CR programs. Figure 3 depicts a schematic model for comprehensive CR that includes yoga.
In a single-blind, prospective randomized, parallel 2-arm active control study involving 250 male post-coronary artery bypass grafting patients aged 35 to 65 yr attending CR, patients randomized to the yoga group showed significant improvement in left ventricular ejection fraction at 1 yr compared with the control (standard CR).47 In the intervention group, patients performed yoga for 30 min/d with the help of a trainer in 3 different phases: deep relaxation for first 6 wk; Sukshma vyayama (subtle yoga) from the 6th wk to the 6th mo; and yogic breathing exercises, asanas, and other postures from the 6th to 12th mo. Pharmacotherapy and conventional post-operative rehabilitation practices were common to both groups.47 However, this study did not include female patients and patients with ejection fraction <35%. A 5-yr follow-up of the same study noted better improvements in quality-of-life measures and stress reduction levels with the addition of long-term yoga-based lifestyle programming to the conventional CR.48 As of now there is no consensus as to when and how yoga can be incorporated into CR post-cardiac bypass surgery, but this study demonstrated that incorporating a structured yoga program immediately post-surgery and extending it for up to 5 yr is safe and can improve outcomes.
CHALLENGES TO INCORPORATING YOGA INTO CARDIAC REHABILITATION
Despite its potential benefits, incorporating yoga into CR lacks standardization. At the center of this issue is the general absence of guidance for standard practices in navigating programs, as well as patients, through this multifactored, mind-body discipline, which may appear seemingly complex, and perhaps impacted by CV disease status.49 The recognition by staff and patients of the value of this holistic approach, rather than as a substitute for exercise, cannot be overstated. Furthermore, the choice of style and intensity of yoga, and the identification of instructors, as well as the specific components of the yoga intervention including dose/delivery, modifications dependent upon patient characteristics, and home programming are critical to the success of this intervention. Moreover, while yoga may be accepted within the urban population, lack of adequate resources, primarily appropriately trained instructors, and patient engagement in rural settings need to be addressed before incorporating yoga as a potential adjunctive modality within CR. The role of instructors is critical for appropriate outcomes, but it may be difficult to assure competence, particularly related to CR patients. CR programs would benefit from utilization of trained staff already participating as CR staff members to deliver yoga instruction, but this approach may be limited due to time constraints and lack of expertise in yoga. Conversely, yoga “instructors” might be engaged/contracted to provide services, dependent upon financial support for doing so, or patients' willingness to pay for services.
The evaluation for and use of yoga in the presence of medical limitations, in this instance, CV disease, center on the actual components of the intervention, given that what is practiced in the West is frequently different from yoga's traditional origins. The average dose of yoga for patients with CV disease in the United States has been described as employing 8 wk, 2 classes/wk, for up to 60 min/session, along with home practice.49 Certainly, the specifics of the activity can be adjusted based upon the participants' yoga experiences and health limitations, as well as facility parameters, and can begin with shorter activity periods (15-30 min) and working up to an additional day per week. The importance of complementing the results of the formal program, by utilizing the practice of yoga at home, should be encouraged. The components of yoga have primarily included postures, breathing, and relaxation, but may include meditation. Questions of additional costs associated with yoga participation within CR have not been sufficiently addressed, and many programs simply incorporate yoga components as appropriate within the CR program. Furthermore, given that many CR participants are older, ≥70 yr of age, individualizing yoga prescription is necessary and can variously focus on upper and lower body strength, balance, and sitting versus standing body position. The recently reported “Yoga Empowers Seniors Study (YESS)” trial demonstrated significant improvements in physical function and muscle-specific lower extremity strength with a modified Hatha yoga program designed for seniors.50 In addition, the use of yoga in the sitting position, initially described in the yoga sutras, the first text on yoga,51 has become popular in programs directed toward older persons. The use of “Chair Yoga” allows participation without having to get down on the floor, while providing stability, including the prevention of loss of balance and potential falls or other injuries.52 An example of chair yoga can be found at https://www.verywellfit.com/chair-yoga-poses-3567189.
SAFETY OF YOGA
As with any form of therapy, yoga can result in adverse events especially when practiced without adequate guidance, instruction, and when extreme forms are practiced. The most important part of yoga practice is choosing the right form and tailoring it to individual needs and limitations; for example, Hatha yoga, if not performed in certain sequences, may lead to gastric discomfort, nausea, and vomiting. Musculoskeletal side effects are also possible if physically intense yoga methods are followed without proper supervision. Kundalini syndrome, characterized by headaches, motor and sensory effects, high BP, increased HR, insomnia and psycho-social issues, may result from performing Kundalini yoga incorrectly or too often.53 Rare adverse events have also been reported with extremes of temperature used in certain types of yoga. Despite these limitations, most studies assessing the safety of yoga have demonstrated very low rates of adverse events. A 2015 meta-analysis of 94 randomized control trials concluded that yoga was not associated with a significant excess of intervention-related, nonserious, or serious adverse events, when compared with usual care or exercise.54
LIMITATIONS AND FUTURE DIRECTIONS
Currently the effect of yoga on CV health is restricted to very low to low-quality evidence. Most studies are limited by small numbers of patients enrolled, short follow-up duration, and observer bias due to lack of adequate blinding. In addition, studies originating in certain geographic areas like India appear to have more favorable results. This could be due to observer and patient bias toward yoga or may be a result of superior delivery of yoga instruction and performance, as yoga has been practiced for a very long time in this part of the world. The various methodological drawbacks in the reviewed studies significantly impact the strength of the conclusions pertaining to the clinical benefits of yoga in CV disease.
Yoga appears to be a relatively safe intervention that can be incorporated into primary and secondary prevention strategies for CV disease. Large well-designed randomized control studies in diverse groups of patients assessing long-term clinical benefits are necessary to definitively establish the benefits of yoga and define its role in the current CV prevention and CR landscape.
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