Advance Access Publication 27 October 27 ecam 27;4(4)511 517 doi:1.193/ecam/nem87 Original Article Iyengar Increases Cardiac Parasympatetic Nervous Modulation Among Healty Practitioners Kerstin Kattab 1, Amed A. Kattab 1, Jasmin Ortak 2, Gert Ricardt 1 and Hendrik Bonnemeier 2 1 Herz-Kreislauf-Zentrum Segeberger Kliniken GmbH, Bad Segeberg and 2 Medizinisce Klinik II, Universitätsklinikum Scleswig-Holstein Campus Lübeck, Lübeck, Germany Relaxation tecniques are establised in managing of cardiac patients during reabilitation aiming to reduce future adverse cardiac events. It as been ypotesized tat relaxationtraining programs may significantly improve cardiac autonomic nervous tone. However, tis as not been proven for all available relaxation tecniques. We tested tis assumption by investigating cardiac vagal modulation during yoga.we examined 11 ealty yoga practitioners (7 women and 4 men, mean age: 43 11; range: 26 58 years). Eac individual was subjected to training units of 9 min once a week over five successive weeks. During two sessions, tey practiced a yoga program developed for cardiac patients by B.K.S. Iyengar. On tree sessions, tey practiced a placebo program of relaxation. On eac training day tey underwent ambulatory 24 Holter monitoring. Te group of yoga practitioners was compared to a matced group of ealty individuals not practicing any relaxation tecniques. Parameters of eart rate variability (HRV) were determined ourly by a blinded observer. Mean RR interval (interval between two R-waves of te ECG) was significantly iger during te time of yoga intervention compared to placebo and to control (P5.1 for bot). Te increase in HRV parameters was significantly iger during yoga exercise tan during placebo and control especially for te parameters associated wit vagal tone, i.e. mean standard deviation of NN (Normal Beat to Normal Beat of te ECG) intervals for all 5-min intervals (SDNNi, P5.1 for bot) and root mean square successive difference (rmssd, P5.1 for bot). In conclusion, relaxation by yoga training is associated wit a significant increase of cardiac vagal modulation. Since tis metod is easy to apply wit no side effects, it could be a suitable intervention in cardiac reabilitation programs. Keywords: yoga Iyengar eart-rate-variability cardiac reabilitation Introduction Heart rate variability (HRV) as been establised as a noninvasive tool to study cardiac autonomic activity. Reduced HRV as been establised as a predictor for increased risk of cardiac mortality and sudden cardiac deat (1 6) especially in patients after myocardial infarction. Several relaxation tecniques ave been establised in te For reprints and all correspondence: Kerstin Kattab, MD, Segeberger Kliniken GmbH, Am Kurpark 1, 23795 Bad Segeberg, Germany. E-mail: kerstinkattab@t-online.de management of patients during cardiac reabilitation aiming to reduce future cardiac events via cardiac autonomic nervous activity. It as been ypotesized tat relaxation training programs may improve te cardiac autonomic nervous tone. However, tis as not been proven for all available relaxation tecniques, suc as yoga. Since more tan 6 years, B.K.S. Iyengar as been working terapeutically wit patients after myocardial infarction. His metod offers more tan oter tecniques for relaxation: te sequence of yoga asanas (postures) and te individuality tey are performed wit, are adjusted to ß 27 Te Autor(s) Tis is an Open Access article distributed under te terms of te Creative Commons Attribution Non-Commercial License (ttp://creativecommons.org/ licenses/by-nc/2./uk/) wic permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided te original work is properly cited.
512 Antidiabetic compounds from banaba te severity of myocardial infarction, te stage of recovery and te clinical condition of te patient. Props are used, so tat te strain of exercise can be regulated or stopped if desired. We investigated weter tis metod as a positive influence on te cardiac vagal modulation compared to a similar setting of conventional relaxation and exercise tecniques among ealty yoga practitioners. Metods Subjects We examined 11 ealty yoga practitioners (7 women and 4 men, mean age: 43 11; age range: 26 58 years). Tey were experienced practitioners wit at least 3 years of regular practice of Iyengar ; four of tem were certified teacers of Iyengar. Eac individual was subjected to five training units eac of 9 min at te same time of te day (around 12. 13.3 p.m.) once a week over five successive weeks. During two sessions, tey practiced Iyengar ; on tree sessions tey practiced a placebo program of relaxation tat consisted of resting on te floor and park walking. To avoid misinterpretations of our findings due to interindividual and circadian variability (7), te yoga practitioners temselves served as an intraindividual control group. Te group of yoga practitioners was also compared to an age and gender matced group of ealty individuals witout evidence of cardiovascular disease wo ave not been practicing any relaxation tecniques (n ¼ 11), to identify long-term effects. All volunteers gave informed consent for scientific use of teir Holter information. Intervention Before te actual examination started, te yoga practitioners ad 3 5 sessions were tey practiced te sequence of yoga asanas cosen for te intervention to make tem familiar wit te program. Since te yoga practitioners were experienced, te program, wic was taken from te work of B.K.S. Iyengar, addressed patients after myocardial infarction already at an advanced stage of recovery. Te program started wit about 15 min resting poses, continued by 6 min standing poses, backbends and inverted poses and ended wit anoter 15 min of resting poses. Te sequence of asanas is sown in Table 1. Usually a training program for cardiac patients ends wit te asana Bismacaryasana; ere owever we canged te series to end te program wit Savasana (lying on te floor) to simulate te final resting pase of te placebo program. Asanas were conducted by a certified teacer for Iyengar (K.K.). All asanas of B.K.S. Iyengar s work wit cardiac patients after myocardial infarction focus on opening te cest; terefore in standing poses a trestle Table 1. Sequence of asanas (yoga-postures) performed by 11 yoga students during time of intervention Savasana wit support (corpse pose, see Fig. 1a) Supta Badda Konasana wit support (supine, bound angle pose) Purvottanasana on benc and support (intense stretc of te front of te body, see Fig. 1b) Trikonasana wit a trestle (triangular standing pose) Parsvakonasana wit a trestle (lateral angle standing pose) Arda Candrasana wit a trestle (alf moon standing pose, see Fig. 1c) Prasarita Pardottasasana, concave back (spread legs, intensely streced) Baradvajasana, sitting on cair, ands on trestle (twisting pose named after Baradvaja) Ado Muka Svanasana wit ropes (downward facing dog pose) Sirsasana (eadstand) Viparita Dandasana wit benc (inverted stick pose) Danurasana wit or witout support (upward bow pose, see Fig. 1d) Sarvangasana wit cair (soulderstand) Halasana wit support (ploug pose) Bismacaryasana wit support (backbend named after Bisma, see Fig. 1e) Setubanda Sarvangasana wit support (bridge pose) Viparita Karani on Setubanda Benc (inverted lake pose) Savasana wit support (corpse pose, see Fig. 1a) was used and in supine position a special support for te toracic spine was applied (e.g. wooden plank and small eart brick), see Fig. 1 a e. Te exact description of te exercises is beyond te scope of tis article. Details ave been described by B.K.S. Iyengar elsewere (8 9). Te placebo program was designed to be comparable to te yoga intervention and consisted of about 15 min resting on te floor in supine position, 6 min park walking and again 15 min of resting on te floor. Te group was familiar wit tis kind of activity. During park walking or resting, te trainees were also under guidance of te yoga instructor, and were taugt to relax certain muscle groups. Data Collection During five successive weeks, once a week all volunteers underwent 24- ambulatory ECG monitoring wit two-cannel time-tracking Holter recorders (Tracker II, Reynolds, Herford, UK). Te Holter Recording was initiated between 11 a.m. and 12 p.m. At around 12 p.m., te intervention program started. During tree sessions, tey underwent te placebo program; during two sessions te yoga program was conducted. All Holter recordings were manually edited by an experienced pysician (H.B.) for exclusion of artifacts and premature beats. Te pysician was unaware of te group and te intervention. One RR interval (interval between two R waves of te ECG) before and five-rr intervals after an atrial or ventricular premature beat were eliminated from te analysis. A minimum of 22 of analyzable data and a minimum of 9% of analyzable NN (Normal Beat to Normal Beat of te ECG) intervals were required for a tape to be accepted as valid. Te median duration of te recordings was 24, wit 96% of valid analyzable NN intervals. Tere was no drop out.
ecam 27;4(4) 513 (a) (b) (c) (d) (e) Figure 1. (a) Savasana/corpse pose. (b) Purvottanasana on benc and support/intense stretc of te front of te body. (c) Arda Candrasana wit a trestle/alf moon standing pose. (d) Urdva Danurasana wit support/upward bow pose. (e) Bismacaryasana wit support/backbend named after Bisma. Analysis of HRV For eac subject, time-domain HRV was measured according to te Task Force of ESC and NASPE (2) using a Patfinder digital analysis system (Delmar Reynolds). Mean RR interval and te following HRV parameters were calculated as ourly values and as 24- values: square root of te mean of te sum of te squares of differences between adjacent NN intervals (rmssd), standard deviation of NN intervals (SDNN), mean standard deviation of NN intervals for all 5-min segments (SDNNi), standard deviation of te averages of NN intervals for all 5-min segments (SDANN), absolute count of adjacent successive NN intervals differing by 45 ms/ (snn5) and geometrical triangular index (TI). Statistical Analysis Statistical analyses were conducted wit a commercially available software package (SPSS version 12.; SPSS Inc). Comparisons between groups were performed utilizing a Mann Witney U-test. Multiple comparisons were done by Bonferroni corrected analysis of variance for repeated measures. Consecutively, an alpa corrected paired Student s t-test was performed for interval-tointerval comparisons. HRV-parameters were tested for normal distribution wit te Komolgorov Smirnov
514 Antidiabetic compounds from banaba Table 2. Baseline criteria of ealty yoga practitioners subjected to yoga or placebo and teir matced ealty controls goodness-of-fit test for normality. All parameters but snn5 were normally distributed. Altoug natural logaritmic transformation could diminis te skewness of te distributions of snn5, data was not transformed wit regard to te lack of comparability wit previous publised data. HRV-data are presented as mean values standard deviation. Statistical significance was set up at P5.5. Results practitioners (n ¼ 11) (s n ¼ 11) Male (%) 36.4 36.4 Age range (years) 26 58 26 57 Smoker, ypertension, diabetes, istory of cardiovascular disease (%) HRV Parameters Outside Intervention Time Te baseline criteria of yoga practitioners and te matced control group are sown in Table 2. Tere were no significant differences regarding ourly mean values of RR interval and parameters of HRV outside te intervention time. RR Interval and Parameters Associated to te Vagal Tone During Intervention Mean RR interval was significantly iger during te time of yoga intervention compared to placebo and to control (865 119 ms; 746 86 ms; 753 115 ms, respectively, P5.1 for bot). Increase in te parameters of HRV was significantly iger during yoga exercise tan during te placebo program and control especially for parameters associated to vagal tone [mean standard deviation of NN intervals for all 5-min intervals (SDNNi) 86.9 16 versus 62.9 53.3 18 (P5.1 for bot); root mean square successive difference rmssd 37.3 1 versus 3.1 9 versus 24.1 12 (P5.1 for bot)]. Estimates of Overall HRV and Parameters Associated wit Pysical Activity During Intervention Estimates of overall HRV were significantly iger regarding te geometrical TI during yoga compared to placebo and control at time of intervention (26.5 6 versus 24.6 8 versus 17.6 6; P5.1 for bot). Standard deviation of NN interval (SDNN) was not significantly different during yoga exercise compared to te placebo program, but was significant for bot compared to te control at time of intervention (129.6 22 versus 13.7 32 versus 78.7 26 P5.1). Standard Deviation of te averages of NN intervals for all 5 min segments (SDANN) a long-term parameter associated wit pysical activity was iger during te placebo program of resting and park walking compared to te yoga program (9.8 32 versus 116.6 33.5; P5.1) and significantly iger for bot yoga and placebo compared to te control (P5.1), results are demonstrated in Fig. 2 a g and Table 3. Discussion Tis study demonstrates tat relaxation by yoga training is associated wit a significant increase of cardiac vagal modulation among ealty yoga practitioners. Since tis metod is easy to apply wit no side effects, and leads to a deep pysical and mental relaxation, it could be a suitable intervention during cardiac reabilitation to sift te autonomic balance towards an increase of vagal activity and possibly decrease cardiac mortality. La Rovere et al. (1) sowed tat exercise training by bicycle ergometry, an establised training metod in cardiac reabilitation programs, increases vagal activity in patients after myocardial infarction, investigating baroreflex sensitivity as an autonomic marker. However, tey reported tat exercise training alone does not seem to be te only determinant of improved Figure 2. (a) Mean ourly results of RR-interval ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te yoga group ( or ). *** versus P5.1, ** versus P5.1. (b) Mean ourly results of SDNN ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). *** versus P5.1, *** versus P5.1. (c) Mean ourly results of SDNNi ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). *** versus P5.1, *** versus P5.1. * versus P5.5. (d) Mean ourly results of SNN5 ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). ** versus P5.1, ** versus P5.1. (e) Mean ourly results of SDANN ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). ** versus P5.1, *** versus P5.1, *** versus P5.1. (f) Mean ourly results of rmssd ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). ** versus. P5.1, ** versus P5.1, * versus P5.5. (g) Mean ourly results of TI ECG-recordings among 11 students and a matced control group. Te red arrow marks time of intervention of te group ( or ). *** versus P5.1, *** versus P5.1, * versus P5..
RR Interval 5 55 6 65 7 75 8 85 9 95 1 15 11 115 12 1 2 1 2 1 2 1 2 1 2 1 2 ms *** ** SDNN 2 4 6 8 1 12 14 16 18 *** *** SDNNi 2 4 6 8 1 12 *** *** * SNN5 2 4 6 8 1 12 14 16 ** ** SDANN 2 4 6 8 1 12 14 16 ** ** * ** * rmssd 1 2 3 4 5 6 7 1 2 ** ** * Triangular Index 5 1 15 2 25 3 35 4 *** *** * (a) (b) (c) (d) (e) (f) (g) ecam 27;4(4) 515
516 Antidiabetic compounds from banaba Table 3. Results during time of intervention mean SD mean SD mean SD Significance yoga versus placebo Significance yoga versus control Significance placebo versus control RR Interval 864.5 119 746.4 86 743.6 115 P5.1 P5.1 n.s. SDNN 129.6 22 13.7 32 78.7 26 n.s. P5.1 P5.1 SDNNi 86.9 16 62.9 29 53.9 18 P5.1 P5.1 P5.5 SNN5 58.3 41 48.7 371 246.1 3 P5.1 P5.1 n.s. SDANN 9.8 32 116.6 33.5 49.7 25.9 P5.1 P5.1 P5.1 rmssd 37.3 1 3.1 9 24.1 12 P5.1 P5.1 P5.5 TI 26.5 6 24.6 8 17.6 6 P5.1 P5.1 P5.5 survival. It was only te combination of exercise wit an increase in baroreflex sensitivity tat predicted better survival. From experiments wit dogs, Billmann et al. (11) considered te possibility tat even independently from pysical training, increased baroreflex sensitivity would be associated wit a reduced risk for cardiac mortality after myocardial infarction. Also in experiments wit dogs after ealed myocardial infarction, Kukielka et al. (12) reported tat submaximal long-duration exercise reduced cardial vagal regulation initially, but furter exercise training attenuated te initially exercise-induced reductions in eart rate variability, suggesting a maintained iger cardiac vagal activity during exercise in te trained state. On te oter and, Duru et al. (13) found no significant effect of ig-intensity exercise training on HRV indexes among patients wit new-onset left ventricular dysfunction after myocardial infarction after 1, 2 and 12 monts of training in a reabilitation center, despite beneficial effects on clinical variables. Tese findings suggest, tat after myocardial infarction wit resulting left ventricular dysfunction wic makes up most of post-infarction patients, exercise training remains of limited value on HRV improvements. Furtermore, it seems tat in a previously untrained condition, te subject needs to first develop a trained state, before exercise training can ave a positive influence on cardial vagal regulation, and tat during te pase of building-up exercise capacity an unwanted counter effect migt occur. Tere is a risk tat especially young and untrained patients tend to go beyond teir (cardiac) exercise capacity. We also experience patients aving reduced left ventricular function or comorbidities, wo cannot tolerate regular exercise on bicycle ergometry. In tese cases, training by relaxation programs could be a suitable alternative and are already establised in many reabilitation centers as an additional training. A systematic meta-analysis about relaxation terapy for reabilitation and prevention in iscemic eart disease by Van Dixoorn and Wite (14) of 27 controlled trials in wic patients wit myocardial infarction were taugt relaxation terapy revealed tat intense supervised relaxation practice enances recovery from an iscemic cardiac event. Tis meta-analysis included relaxation tecniques suc as progressive muscle relaxation, autogenic training, biofeedback, breat relaxation, ypnosis and psycological training. Among tese 27 controlled trials, tree studies investigated and revealed a positive effect on HRV (15 17). Te applied tecniques of relaxation were progressive muscle relaxation, breat relaxation, deep breating, cue controlled relaxation and biofeedback. In our study, we could sow tat training after te metod of B.K.S. Iyengar among ealty yoga practitioners was superior to a simple relaxation program tat consisted of resting on te floor and mild exercise like park walking. We tink tat is metod migt be superior to oter relaxation tecniques since it is a unique combination of relaxation [acieved by components like muscle stretcing and relaxing, deep breating, awareness (comparable to biofeedback), psycological aspects (18) concentration and meditation] and very exact terapeutical pysical work tat can be tailored for any limiting condition or comorbidity. Te postures for cardiac patients are cosen and modified in a way to improve te loading unloading conditions of te eart, wic could positively influence remodeling and ealing. In every asana, te cest is kept open to improve respiration and acieve a iger oxygenation of blood. Backbending actions give a lengtwise stretc to te mediastinum. Depending on te stage of recovery and condition of te patient, te body is gradually brougt to more inverted postures wic increase venous return to te eart. During yoga, te trainees ad a lower eart rate tan during te alternative program. Even during postures tat build up body tension like standing poses or backbends, using slow and more isometric muscle contraction, te eart rate did not rise muc. A slow eartbeat prolongs te diastolic filling of te eart, decreases myocardial oxygen consumption and increases myocardial perfusion. A study among 24.913 patients by Diaz et al. (19) clearly identified a ig resting eart rate (wic also reflects cardial autonomic imbalance towards sympatetic activity) in patients wit suspected or proved
ecam 27;4(4) 517 coronary artery disease as an independent predictor for total and cardiovascular mortality. Furtermore, a recently publised study introducing deceleration capacity of eart rate a novel Holter-ECG-based marker for vagal activity underlines te crucial role of cardiac vagal modulation regarding cardiovascular mortality in post-infarction patients undergoing modern treatment, particularly treatment involving acute revascularization procedures (2). Furter studies are required to investigate weter te demonstrated positive effect of terapeutic yoga on te cardiac vagal modulation can be transferred to cardiac patients and introduced into cardiac reabilitation programs. Limitations Te coort (regular yoga practitioners) warrants drawing conclusions about long-lasting effects of yoga on HRV parameters. However, te 24 circadian rytm of te yoga practitioners e.g. for SDNNi and rmssd was iger tan in te control group, yet te population was too small to sow a significant difference. Additional studies are required to investigate long-term effects of yoga training on cardiac autonomic nervous modulation. Acknowledgements We like to tank Mr B.K.S. Iyengar for is guidance during tis study. He tailored te sequence of asanas for tis investigation and gave us a glimpse of is knowledge and experience of terapeutic yoga. References 1. Ewing DJ, Neilson JMM, Travis P. New metod for assessing parasympatetic activity using 24 our electrocardiograpms. Br Heart J 1984;52:396 42. 2. Task Force of te European Society of Cardiology and te Nort American Society of Pacing and Electropysiology. Heart rate variability: standards of measurement, pysiological interpretation, and clinical use. Circulation 1996;93:143 65. 3. Malik M, Camm AJ. Heart rate variability. Clin Cardiol 199;13:57 6. 4. Kleiger RE, Miller JP, Gigger JT, Moss AJ, and te Multicenter Post-Infarction Researc Group. Decreased eart rate variability and its association wit increased mortality after acute myocardial infarction. Am J Cardiol 1987;59:256 62. 5. Malik M, Farrell T, Cripps T, Camm AJ. Heart rate variability in relation to prognosis after myocardial infarction. Selection of optimal processing tecniques. Eur Heart J 1989;1:16 74. 6. Bigger JT Jr, Kleiger RE, Fleiss JL, Rolnitzky LM, Steinmann RC, Miller JP, and te Multicenter Post-Infarction Researc Group. Components of eart rate variability measured during ealing of acute myocardial infarction. Am J Cardiol 1988;61:28 15. 7. Bonnemeier H, Wiegand UKH, Brandes A, Kluge N, Katus HA, Ricardt G, et al. Circarian profile of cardiac autonomic nervous modulation in ealty subjects: differing effects of aging and gender on eart rate variability. J Cardiovasc Electropysiol 23;14:1 9. 8. Iyengar BKS. -Te pat to olistic ealt. London: Dorling Kindersley Limited, 21. 9. Iyengar BKS. Ligt on. Great Britain: George Allen & Unwin, 1966. 1. La Rovere MT, Bersano C, Gnemmi M, Speccia G, Scwartz PJ. Exercise-induced increase in baroreflex sensitivity predicts improved prognosis after myocardial infarction. Circulation 22;16:945 9. 11. Billmann GE, Scwartz PJ, Stone HL. Te effects of daily exercise on susceptibility to sudden cardiac deat. Circulation 1984;69:1182 9. 12. Kukielka M, Seals DR, Billmann GE. Cardiac vagal modulation of eart rate during prolonged submaximal exercise in animals wit ealed myocardial infarctions: effects of training. Am J Pysiol Heart Circ Pysiol 25;29:H168 5. 13. Duru F, Candinas R, Dziekan G, Goebbels U, Myers J, Dubac P. Effect of exercise training on eart rate variability in patients wit new-onset left ventricular dysfunction after myocardial infarction. Am Heart J 2;14:157 61. 14. Van Dixoorn J, Wite A. Relaxation terapy for reabilitation and prevention in iscaemic eart disease: a systematic review and metaanalysis. Eur J Cardiovasc Prev Reabil 25;12:193 22. 15. Del Pozo JM, Gervirtz RN, Scer B, Guarneri E. Biofeedback treatment increases eart rate variability in patients wit known coronary artery disease. Am Heart J 24;E11:G1 8. 16. Hase S, Douglas A. Effects of relaxation training on recovery from myocardial infarction. Aust J Adv Nurs 1987;5:18 27. 17. Van Dixoorn J. Cardiorespiratory effects of breating and relaxation in myocardial infarction patients. Biol Psycol 1998;49:123 35. 18. Sapiro D, Cook IA, Davydov DM, Ottaviani C, Leucter AF, Abrams M. as a complementary treatment of depression: effects of traits and moods on treatment outcome. ecam, February 28, 27; doi: doi:1.193/ecam/nel114. 19. Diaz A, Bourassa MG, Guertin MC, Tardif JC. Longterm prognostic value of resting eart rate in patients wit suspected or proven coronary artery disease. Eur Heart J 25;26:943 5. 2. Bauer A, Kantelardt JW, Bartel P, Scneider R, Mäkikallio T, Ulm K, et al. Deceleration capacity of eart rate as a predictor of mortality after myocardial infarction: coort study. Lancet 26;351:478 84. Received October 22, 26; accepted April 23, 27