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Yoga for the Management of HIV-Metabolic Syndromes

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Yoga for the Management of HIV-Metabolic Syndromes
  ORIGINAL RESEARCH  Yoga lifestyle intervention reduces blood pressure in HIV-infected adults with cardiovascular disease risk factors *  WT Cade, 1,2  DN Reeds, 1  KE Mondy, 1  ET Overton, 1 J Grassino, 3 S Tucker, 3 C Bopp, 1  E Laciny, 1 S Hubert, 1 S Lassa-Claxton 1 and KE Yarasheski 1,2 1 Department of Medicine, Washington University School of Medicine, 2 Program in Physical Therapy, Washington University School of Medicine and  3 Brentwood Center of Health, St Louis, MO, USA Objective People living with HIV infection are at increased risk for developing cardiovascular disease (CVD).Safe and effective interventions for lowering CVD risk in HIV infection are high priorities. Weconducted a prospective, randomized, controlled study to evaluate whether a yoga lifestyleintervention improves CVD risk factors, virological or immunological status, or quality of life (QOL)in HIV-infected adults relative to standard of care treatment in a matched control group. Methods Sixty HIV-infected adults with mild–moderate CVD risk were assigned to 20 weeks of supervised yoga practice or standard of care treatment. Baseline and week 20 measures were: 2-h oral glucosetolerance test with insulin monitoring, body composition, fasting serum lipid/lipoprotein profile,resting blood pressures, CD4 T-cell count and plasma HIV RNA, and the Medical Outcomes Study Short Form (SF)-36 health-related QOL inventory. Results Resting systolic and diastolic blood pressures improved more ( P  5 0.04) in the yoga group ( À 5 Æ 2and À 3 Æ 1mmHg, respectively) than in the standard of care group ( 1 1 Æ 2 and 1 2 Æ 2mmHg,respectively). However, there was no greater reduction in body weight, fat mass or proatherogeniclipids, or improvements in glucose tolerance or overall QOL after yoga. Immune and virologicalstatus was not adversely affected. Conclusion  Among traditional lifestyle modifications, yoga is a low-cost, simple to administer,nonpharmacological, popular behavioural intervention that can lower blood pressure inpre-hypertensive HIV-infected adults with mild–moderate CVD risk factors. Keywords: cardiometabolic complications, complementary or alternative therapy, hypertension,physical activity   Accepted 8 September 2009 Introduction Infection with HIV and treatment with combinationantiretroviral therapy (cART) have been associated withseveral metabolic and anthropomorphic alterations thatincrease cardiovascular disease (CVD) risk [1,2]. Thesealterations include insulin resistance, dyslipidaemia, visceral adiposity, subcutaneous lipoatrophy, and bonedemineralization, and several are components of thecardiometabolic syndrome. cART has effectively reducedHIV-related morbidity and mortality, but HIV-infectedpeople are living longer with significant CVD risk. HIV service providers are confronted with the challenge of effectively addressing CVD risk, and specifically identify-ing traditional or alternative/complementary therapies thatmay reduce CVD risk in HIV infection.People living with HIV, taking cART, and experiencingcardiometabolic syndromes often use alternative or  *  A preliminary report of these findings was presented at the 9thInternational Workshop on Adverse Drug Reactions and Lipodystrophy inHIV, Sydney, Australia, 19–21 July 2007.Correspondence: Dr Kevin E. Yarasheski, PhD, Washington University School of Medicine, 4940 Parkview Place, Metabolism Division, BOX 8127,St. Louis, MO 63110, USA. Tel: 1 1 314 362 8173; fax: 1 1 314 362 7641;  DOI: 10.1111/j.1468-1293.2009.00801.x r 2010 British HIV Association HIV Medicine  (2010), 11 , 379–388 379  complementary therapies to manage side-effects of HIV or cART [3–7]. Recent surveys estimate that 47–74% of HIV-infected individuals in the United States have used someform of alternative/complementary therapy to improvegeneral health and wellbeing [7]. One potentially safe,effective, low-cost and popular behavioural interventionthat might be employed to manage HIV-associatedcardiometabolic complications is the practice of yoga. Yoga is based on an ancient system of breathing exercises,postures, stretches and meditations founded in Ayurvedicmedicine and Indian philosophy and religion, and it isbelieved to help ‘detoxify’ the body, mitigate chronicfatigue, enhance endurance, and improve organ andimmune functions [8].Several reviews of published studies, in people withoutHIV infection, concluded that the practice of yoga may reduce insulin resistance and related CVD risk factors andimprove clinical outcomes [8–11]. Specifically, reportssuggest that a yoga lifestyle intervention reduces body weight, blood pressures and glucose and cholesterol levels,and improves vascular function; adaptations that shouldreduce CVD risk and improve quality of life (QOL) in HIV-infected people [8,11–33]. Despite the popularity andpotential benefits of yoga, no prospective, randomized,controlled trial has examined the cardiometabolic benefitsof a yoga lifestyle in HIV-infected people with CVD risk factors. The purpose of this randomized, controlled study was to determine whether 20 weeks of supervisedinstruction and practice in yoga asanas (postures) andpranayama (breathing exercises) improves CVD risk factors, including oral glucose tolerance, lipid/lipoproteinlevels, resting blood pressures, body composition, immuneand virological status, and health-related QOL, in HIV-infected men and women relative to standard of care in acontrol group. Methods Participants Participants were recruited from the Washington University  AIDS Clinical Trials Unit and local Infectious DiseasesClinics. Sixty HIV-infected men and women (18–70 yearsold) were randomly assigned (3:2) to receive 20 weeks of individual and group instruction in the practice of yogafrom a certified yoga instructor, or 20 weeks of continuedstandard of care treatment (Fig. 1). Eligibility criteria were:documented HIV status, stable and with no plans to changecurrent cART, CD4 T-cell count 4 200cells/ m L, plasma HIV RNA  o 15000 HIV-1 RNAcopies/mL, and at least one of thefollowing CVD risk factors: dyslipidaemia, central adipos-ity, glucose intolerance/insulin resistance, or hypertension.Dyslipidaemia was defined as low high-density lipoprotein(HDL) cholesterol level ( o 1.0mmol/L for men and o 1.3mmol/L for women), fasting hypertriglyceridaemia( 4 1.7mmol/L), high low-density lipoprotein (LDL) choles-terol level ( 4 2.6mmol/L) or current use of a lipid-loweringagent. Central adiposity was defined as waist circumference 4 102cm for men or  4 88cm for women, or trunk/limbadipose ratio 4 1.0 for men or  4 0.85 for women usingwhole-body dual energy X-ray absorptiometry. Glucoseintolerance/insulin resistance was defined as fasting bloodglucose 5.6–6.9mmol/L, 2-h blood glucose 7.8–11.0mmol/L, fasting insulin level 4 72pmol/L, or current use of ananti-diabetes agent. Hypertension was defined as restingsystolic blood pressure 4 130mmHg, resting diastolicblood pressure 4 85mmHg (on three occasions) or currentuse of an anti-hypertensive agent. Exclusion criteriaincluded: chronic hepatitis B or active hepatitis C virusinfection, diabetes, male hypogonadism ( o 7.0nmol/L),hypo- or hyperthyroidism ( o 0.2 or  4 12 m IU/mL), preg-nancy or plans to become pregnant, prior myocardialinfarction (MI), unstable angina, heart failure, coronary artery disease, resting ST-segment (segment between theS-wave and T-wave on the electrocardiogram) depression 4 1mm, coronary artery bypass graft, stroke and activesubstance abuse. Both groups received monthly nutrition Assessed for eligibility(n = 177)Excluded: Did notmeet inclusion criteria(n = 57); refusedparticipation (n = 60)Randomized (n = 60)Allocated to standard ofcare (n = 26)Allocated to yoga(n = 34)Lost to follow-up (n = 5):2-personal reason1-never attended1-work conflict1-deathLost to follow-up (n = 5):3-personal reason2-never attendedAnalysed (n = 21)Analysed (n = 29) Fig. 1 Flow diagram for participant screening, exclusion, randomi-zation and data analysis. 380 W Todd Cade et al . r 2010 British HIV Association HIV Medicine  (2010) 11 , 379–388  counselling (American Heart Association (AHA) guidelines[34]) from a research dietician. Standard of care includedregular routine visits to the participant’s infectious diseasephysician, no added physical activity, no changes in cARTand no added medications for hyperglycaemia, hyperlipi-daemia or hypertension. All participants signed aninformed consent document and the study was approvedby the Human Research Protection Office at WashingtonUniversity School of Medicine. Measurements  At baseline and 20 weeks, participants were examined by aphysician-investigator. Waist circumference was measured atthe midpoint between the costal margin and the anterior superior iliac crest. After an overnight fast (8–10h), restingelectrocardiogram (EKG) and blood pressures (average of three resting measures), serum lipid/lipoprotein levels (totaland HDL cholesterol, triglyceride, and calculated LDL andnon-HDL cholesterol levels), a comprehensive metabolicpanel (e.g. liver and kidney function tests), CD4 T-cell count(flow cytometry), plasma HIV RNA level (Roche Amplicor  t HIV-1 Monitor Test; Roche, Branchburg, NJ, USA) and a75-g, 2-h oral glucose tolerance test (oGTT) with plasmaglucose and insulin monitoring at 0, 30, 60, 90 and 120minwere obtained. Whole-body and regional body compositionwere quantified using enhanced-array whole-body dualenergy X-ray absorptiometry (software v12.4; HologicDiscovery, Waltham, MA, USA). Participants completed theMedical Outcomes Study (MOS) Short Form (SF)-36 health-related QOL (HIV-QOL) inventory and a 3-day diet record toevaluate energy, macro- and selected micronutrient intakes.Fasting serum lipid/lipoproteins were quantified asdescribed previously [35]. The accuracy of these analyticalmethods has been verified and standardized by participa-tion in the Centers for Disease Control and Prevention(CDC) Lipid Standardization Program, the CDC CholesterolReference Method Laboratory Network, and the College of  American Pathologists external proficiency programme.Blood glucose levels were quantified using the glucoseoxidase reaction (Yellow Springs Instruments, YellowSprings, OH, USA). Plasma insulin levels were quantifiedusing a chemiluminescent immunometric method (Immu-lite; Siemens, Los Angeles, CA, USA). The plasma insulinassay range is 12–1800pmol/L and the inter-assay coefficient of variation is 4% in the low (63pmol/L) andhigh (331pmol/L) insulin concentration ranges. The home-ostasis model assessment for insulin resistance wascalculated as [baseline glucose (mmol/L) Â baseline insulin( m U/mL)]/22.5 [36]. The MOS SF-36 [37] inventory has been validated for assessing health-related QOL inHIV-infected people [38,39]. The 3-day diet records wereprocessed and analysed by a research dietician using NUTRITIONIST PRO t nutrient analysis software (Axxya Sys-tems, Stafford, TX, USA). For each participant, 3-day average intakes for fat (including saturated and trans fats),protein, carbohydrate, fibre, cholesterol, vitamin D,sodium, calcium and caffeine were calculated.  Yoga intervention  Ashtanga Vinyasa (the co-ordination and integration of breath with movement) yoga was taught and practised. This yoga style follows progressive steps that require adherence,self-control, mental focus, self-awareness and physicalresilience. It encourages body alignment and balance, iseasily reproducible, is adaptable to participants’ limita-tions, and can be delivered safely and with optimal time for learning. All sessions emphasized the proper use of alignedpostures (asanas), controlled breathing (pranayama),focused gaze (drishti), and the regulation of prana(a source of energy that maintains the body) through theuse of bandhas (stabilizing muscle locks), strength building,increased flexibility, large muscle movement, asymmetricalmovements and restorative relaxation. The practice wasmodified to accommodate participants’ limitations (range of motion, spine or joint discomfort and peripheral neuropathy)by allowing for more time between position transitions andby linking breath to movement.The yoga sessions were standardized to optimizeconsistency among participants. They were held two or three times per week for  $ 60min per session andparticipants were enrolled for 20 weeks. As participantsprogressively improved, the respirations (ujjayi) were usedto adjust the timing and transitions of the sequences. Themaximum rate of respirations would last 35–45s per staticpose (asana). Participants initially received individualizedinstruction, but once familiarized and proficient (at $ 9weeks) they were encouraged to attend group sessions. Inaddition to participating in the structured sessions,participants were encouraged to practise at home (at leastone session per week). The yoga sequence was designed for people with no previous yoga exposure. Each session beganwith feedback from the participants about their previoussession. Each session included the following.1. Alignment of muscle locks (bandhas) and controlledbreathing (ujjayi).2. Warm-up (5min).3. Sun salute A x3, salute B x1 (surya namaskara) (7min).4. Standing asanas (25min).5. Seated asanas (10min).6. Lying supine asanas (5min).7. Cool-down (restorative breathing techniques) (7min). HIV, CVD prevention and yoga 381 r 2010 British HIV Association HIV Medicine  (2010) 11 , 379–388  Statistical analyses The mean Æ standard error (SE) is reported except wherenoted. For categorical variables, w 2 tests were used to testbetween-group differences, or Fisher exact tests when thenumber of observations per statistical cell was o 5. For continuous variables, t  -tests were used to test between-group differences. When baseline values differed betweengroups, analysis of covariance was used to adjust and makebetween-group comparisons. Paired t  -tests were used for within-group comparisons. Nonnormally distributed out-come variables (area under the curve for glucose andinsulin) were log-transformed before making any compar-isons. Integrated insulin and glucose areas under the curvewere measured using the trapezoidal method. All other outcomes were normally distributed. Spearman rank correlation coefficients were used to evaluate associationsbetween variables. P  o 0.05 (two-tailed) was consideredsignificant. Results Fifty participants completed the intervention, and atbaseline the two groups were matched for age, gender,race, years known to be HIV infected, immune and virological status, current use of cART, past medical history of CVD, diabetes, hypertension, and alcohol and tobaccouse (Table 1). None of the participants changed cARTduring the study. At baseline, 38% of participants wereusing tobacco, 26% had a history of hypertension, 42% hadpre-hypertension (120–139/80–89mmHg; AHA criteria[40]) and 24% had impaired glucose tolerance (AmericanDiabetes Association (ADA) criteria [41]), and although theaverage per cent body fat was normal (23–24%), theaverage waist circumference was high (men, 97 Æ 21cm;women, 100 Æ 14cm), suggesting that most of the body fatwas located centrally. The baseline Framingham CVD risk score was similar between the groups, and indicated mild–moderate 10-year CVD risk. However, 14% of theparticipants in each group had baseline Framingham CVDrisk scores that were 4 10% (moderate–high risk).On average, yoga participants attended 33 Æ 7 sessions;the minimum number of sessions attended was 14 and themaximum was 45 during the 20-week yoga programme. After 20 weeks, CD4 T-cell count and HIV RNA levels wereunchanged in the yoga (495 Æ 155 to 507 Æ 134cells/ m L;90–83% undetectable) and standard of care groups(570 Æ 256 to 592 Æ 268cells/ m L; 90–90% undetectable). Average baseline glucose and insulin levels and home-ostasis model assessment (HOMA) (Table 1) were normaland not different between groups. Oral glucose toleranceand insulin action were not improved after the yogaintervention (Fig. 2). HOMA index, glucose and insulinlevels and area under the curve during the oGTT were notdifferent between the groups and did not change in either group after the interventions. Insulin levels and area under the curve during the oGTT tended to be lower after yoga(12%), but differences compared with the standard of caregroup were not statistically significant ( P  5 0.46).Baseline serum triglycerides and total and non-HDLcholesterol levels were higher in the yoga group than in thestandard of care group (Fig. 3; P  o 0.04). After adjusting for baseline differences between groups, reductions in theselipid/cholesterol parameters observed in the yoga group (5–24%) were not statistically greater than those in thestandard of care group ( P  4 0.48).Baseline body weight, body fat and lean mass, and trunk and limb fat mass were not different between the groups(Table 2). Weight, fat and lean mass were not changed after either intervention.Baseline resting systolic and diastolic blood pressureswere not different between the groups (Fig. 4). The yogaintervention reduced resting systolic ( À 5 Æ 2mmHg) anddiastolic ( À 3 Æ 1mmHg) blood pressures, while no Table 1 Baseline characteristics for participants who completed thetrial CharacteristicStandard of care Yoga P  -value n (% women) 21 (29) 29 (24) 0.72Race (% African American) 52 35 0.21Age (years) (mean Æ SD) 45 Æ 10 45 Æ 6 0.96Waist circumference (cm) (mean Æ SD) 98 Æ 25 98 Æ 15 0.92 Years HIV positive (mean Æ SD) 11 Æ 6 11 Æ 5 0.92HOMA index (mean Æ SD) 2.1 Æ 1.2 3.1 Æ 3.4 0.21CD4 count (cells/ m L) (mean Æ SD) 570 Æ 256 495 Æ 156 0.21HIV RNA (% undetectable) 90 90 1.0History of hypertension (%) 19 31 0.51History of DM (%) 5 7 1.0Glucose intolerance (%) 24 24 1.0History of CVD (%) 0 3 1.0History of tobacco usePast (%) 29 24 4 0.84Current (%) 33 41Packs/year (range) 0.3–75 2–50History of alcohol usePast (%) 10 21 4 0.66Current (%) 24 21Framingham 10-yr risk (mean Æ SD) 4.3 Æ 5.6 4.8 Æ 4.6 0.73Current cART% on NRTI 95 96 0.93% on NNRTI 57 50 0.88% on PI 48 65 0.72 Undetectable is o 400copies/mL. Glucose intolerance includes impairedfasting glucose (5.6–6.9mmol/L) and impaired glucose tolerance at 2h(7.8–11.0mmol/L) during the oral glucose tolerance test.cART, combination antiretroviral therapy; HOMA, homeostasis modelassessment; NRTI, nucleos(t)ide reverse transcriptase inhibitor; NNRTI,nonnucleoside reverse transcriptase inhibitor; PI, protease inhibitor; CVD,cardiovascular disease; DM, diabetes mellitus; SD, standard deviation. 382 W Todd Cade et al . r 2010 British HIV Association HIV Medicine  (2010) 11 , 379–388  reductions were found in the standard of care group( 1 1 Æ 2 and 1 2 Æ 2mmHg, respectively) ( P  5 0.04 for thedifference between groups). At baseline, 11 participantsassigned to yoga had pre-hypertension and only sixparticipants had pre-hypertension after yoga (45% decline).For the MOS SF-36 inventory (Table 3), the yogaparticipants had a more favourable average baseline painscore than the standard of care group (81 Æ 21 vs . 63 Æ 31,respectively; P  5 0.02). The pain score improved more inthe standard of care group ( 1 10 Æ 22) than in the yogagroup ( À 6 Æ 27; P  5 0.05), suggesting a less favourablepain status at the end of the yoga programme. However, theabsolute SF-36 scores at week 20 were equivalent betweenthe groups (73 Æ 25 vs . 75 Æ 24). There was a trend( P  5 0.06) for a greater improvement in emotional well-being in the yoga group than in the standard of care group. At baseline, average macro- and micronutrient intakeswere similar between the groups (Table 4), except for transfat intake which was higher ( P  5 0.048) in the yoga group,and decreased more in the yoga group after intervention( À 1.6 Æ 2.8 g vs . 1 1.3 Æ 3.3g for the standard of caregroup; P  5 0.03). Baseline differences in fasting totalcholesterol and triglyceride levels (Fig. 3) were notattributed to baseline dietary cholesterol, saturated fat or trans fat intake. Systolic and diastolic blood pressurereductions in the yoga group were not associated withreductions in trans fat intake ( P  5 NS; r  5 0.12). Discussion These findings suggest that practicing yoga for 20 weeksmay lower CVD risk in HIV-infected men and women    P   l  a  s  m  a  g   l  u  c  o  s  e   (  m  m  o   l   /   L   ) of careTime (min)020406080100120140160    I  n  s  u   l   i  n   (  p  m  o   l   /   L   ) 0120240360480600720(a)Yoga    P   l  a  s  m  a  g   l  u  c  o  s  e   (  m  m  o   l   /   L   ) (min)020406080100120140160    I  n  s  u   l   i  n   (  p  m  o   l   /   L   ) 0120240360480600720(b) Fig. 2 Blood glucose and plasma insulin levels, and area under the curve (AUC; mean Æ standard error) during a 75-g 2-h oral glucosetolerance test (oGTT) conducted before and after standard of care (a) or yoga lifestyle intervention (b). No baseline differences in glucose orinsulin levels were noted. Glucose and insulin levels and AUC during the oGTT were not different between the two groups, and the trendtowards a lower insulin AUC after yoga intervention was not significantly different from that in the standard of care group ( P  5 0.46). Table 2 Body composition parameters  VariableStandard of care YogaBetween-groupchange P-value  Baseline Post Baseline Post Body weight (kg) 78.4 Æ 3.4 78.0 Æ 3.6 80.9 Æ 3.1 80.4 Æ 3.2 0.85Body fat (kg) 19.9 Æ 2.2 19.5 Æ 2.3 19.6 Æ 2.1 19.4 Æ 2.1 0.74Limb fat (kg) 8.4 Æ 1.3 8.3 Æ 1.2 7.5 Æ 1.0 7.4 Æ 1.0 0.98Trunk fat (kg) 11.5 Æ 1.1 11.2 Æ 1.3 12.1 Æ 1.2 12.0 Æ 1.2 0.64Lean mass (kg) 57.5 Æ 1.8 57.5 Æ 2.1 60.3 Æ 2.1 57.7 Æ 2.8 0.25Limb lean mass (kg) 24.9 Æ 1.0 24.8 Æ 1.0 25.9 Æ 1.0 26.4 Æ 1.1 0.39  Values are mean Æ standard error. HIV, CVD prevention and yoga 383 r 2010 British HIV Association HIV Medicine  (2010) 11 , 379–388
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