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Complementary Therapies in Clinical Practice 28 (2017) 38e46 Contents lists available at ScienceDirect Complementary Therapies in Clinical Practice journal homepage: www.elsevier.com/locate/ctcp The hypotensive effect of Yoga's breathing exercises: A systematic review * Jeniffer Z. Brandani , Julio Mizuno, Emmanuel G. Ciolac, Henrique L. Monteiro ~ Sao Paulo State University (Unesp), School of Sciences, Physical Education Department, Bauru, Brazil articleinfo abstract Article history: Theaimofthisreviewwastoevaluatetheeffectofpranayama(Yoga'sbreathingexercises) on BPand its Received 19 April 2017 applicability in the treatment of hypertension. Thirteen trials, assessing acute (eight studies) and chronic Accepted 8 May 2017 (five studies) BP response to pranayama were included. Significant BP reductions after pranayama were Keywords: found in both acute (2e10 mmHg mean SBP reduction, N ¼ 5 studies; 1 mmHg mean DBP reduction, Cardiovascular diseases N¼1study) and chronic studies (4e21 mmHg mean SBP reduction, N ¼ 3 studies; 4e7 mmHg mean Complementary therapies DBPreduction,N¼2studies).Thepranayama'seffectonBPwerenotrobustagainstselectionbiasdueto Hypertension the low quality of studies. But, the lowering BP effect of pranayama is encouraging. The pranayama with slower rhythms and manipulation of the nostrils, mainly with breaths by the left, present better results when compared with the other types and should be the main pranayama applied when the goal is to reduce blood pressure especially in hypertensive patients. ©2017 Elsevier Ltd. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 38 2. Methods .............. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 39 2.1. Search strategy and study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...........................................39 2.2. Data extraction and analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...........................................39 3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 39 3.1. Study and subject characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...........................................39 3.2. Assessment of BP and secondary outcomes .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .......................................39 3.3. Pranayamas characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...........................................41 3.4. Effects of pranayamas on BP and secondary outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ............................41 4. Discussions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 44 4.1. Implications for clinical practice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . ...........................................45 4.2. Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...................................................45 5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 45 Disclosures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 45 Conflicts of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................ 45 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...................................................45 1. Introduction * Corresponding author. Universidade Estadual Paulista e UNESP, Departamento Hypertension is a highly prevalent disease worldwide and an ~ ~ de Educaçao Física, Av. Engenheiro Luiz Edmundo Carrijo Coube 14-06, Bauru, Sao important risk factor for stroke, coronary artery disease and organ Paulo, 17033-360, Brazil. Tel.: þ55 14 3103 6082. E-mailaddresses:jeniffer_brandani@yahoo.com.br(J.Z. Brandani),juliomizuno@ failure [1]. In Brazil, nearlly 24.4% and 21.6% of adult women and gmail.com (J. Mizuno), ciolac@fc.unesp.br (E.G. Ciolac), heu@fc.unesp.br men are hypertensive, respectively [2]. The regular practice of (H.L. Monteiro). http://dx.doi.org/10.1016/j.ctcp.2017.05.002 1744-3881/© 2017 Elsevier Ltd. All rights reserved. J.Z. Brandani et al. / Complementary Therapies in Clinical Practice 28 (2017) 38e46 39 physical exercise is a well-established non-phamarcological treat- 3. Results mentforhypertension[3e7].Amongthedifferenttypesofexercise, there is increasing evidence suggesting a hypotensive effect of Electronic databases search identified 347 records. Title and regular practice of Yoga [8e12]. abstract screening discharged 219 duplicates, 49 reviews, 43 with Inabroadercontext,Yogaincludestheoreticalandphilosophical no full-text available, 10 with no BP assessment, five with no- concepts(yamasandniyamas),bodytechniques(asanas),breathing pranayamas intervention, one editorial and one experience exercises (pranayamas), concentration (dharana) and meditation report. Full text screening discharged one study with participants [13]. Among these techniques, pranayamas (breathing exercises of with age <18 years and three studies that pranyama was not the varied time and pace that may be performed with or without air only intervention. Finally, thirteen articles assessing the acute retentioninthelungs)appearstohaveabetterrisk/benefitratiofor (eight studies) [9,10,19e24] and chronic (five studies) [25e29] ef- lowering blood pressure (BP) [14]. Moreover, pranayamas practice fects of pranayamas were included in this review (Fig. 1). doesnothavecostswithspecificequipmentandplaces,whichmay increase its applicability. The main mechanism for its lowering ef- 3.1. Study and subject characteristics fect on BP appears to be the improvementin baroceptorsensitivity, which changes the autonomic balance with an increase in para- General description of each study included is shown in Table 1. sympathetic and decrease in sympathetic modulation [15,16]. Twelve studies were conducted in India and one in UK. Subjects Although there are systematic reviews and meta-analyzes sup- with hypertension were included in six of them [9,10,20,23,25,26]. porting the hypotensive effects of Yoga [14,17,18], the broad variety Eight studies assessed the acute effect of pranayamas (BP response of techniques performed in each individual study (i.e. some studies to a single exercise session) [9,10,19e24], which had a sample size useonlyonetechniquewhileothersusedtwoormoretechniques) ranging 20 to 90 participants (totaling 266 participants), and difficults the interpretation of pranaymas lowering BP effect. included only men [24,26], or both men and women Therefore, the aim of this review was to evaluate the effect of [9,10,19e21,23]. Five studies assessed the chronic effect of pra- pranayamas on BP and its applicability in the treatment of nayamas(BPresponsetoanexerciseprogram)[25e29],whichhad hypertension. a sample size ranging 11 to 90 participants (totaling 239 partici- pants), and included only men [28,29], and both men and women [25,26] however, one study have no information about sex of par- 2. Methods ticipants [27]. Only three studies assessing the chronic effect of pranaymas 2.1. Search strategy and study selection were randomized controlled trial (RCT) [23,27,28], and only one study assessing the pranaymas acute effect had a control inter- PubMed/Medline,ScopusandBiremeelectronicdatabaseswere vention[24].Finally,moststudieswereofpoorquality.Themedian searched for articles about pranayamas effects on BP. Search was PEDro score was z3, with a range from 1 to 7 (Table 2). performed by crossing the terms ‘yoga/Yoga’, ‘yogue/yogi’, ‘pra- nayama’ or ‘breathing’ with ‘blood pressure’, ‘hypertension’ or 3.2. Assessment of BP and secondary outcomes ‘systolic/diastolic BP’. The present systematic review included only clinical trials, In the studies evaluating the acute effects of pranayamas, BP published between January 2006 and August 2016, that investi- assessment was performed by means of semiautomatic non- gated the effect of pranayamas on BP in adult individuals (age 18 invasive [9,10,20], continuous non-invasive [21,24], digital [19] ys), with or without comorbidities. There were no imposed sex or and standard mercury sphygmomanometer [22,23]. In the studies language restrictions. Because of the variability of existing breathingtechniques,onlyexplicitlylabeledinterventionswiththe term “Yoga” were included. Methodologic or observational (descriptiveonly)articles,studieswithpranayamasassociatedwith other intervention were not included. Clinical trials that did not have the full text available were also not included. Two indepen- dent reviewers (J. Z. B. and J. M.) performed the literature search and study assessment. 2.2. Data extraction and analysis Data on study source, sample size, participant's characteristics (e.g. age, sex, baseline BP and physical activity levels, comorbidities …), method used to measure BP, characteristics of breathing exer- cise (i.e. type, frequency and duration of breath, breath techinique) and control interventions (i.e. type, frequency and duration), out- comes and limitations of the included studies were extracted independently by two authors (J. Z. B. and J. M.). When there was discrepancy between reviewers, a third reviewer (H. L. M.) was consulted to solve the discrepancy. Methodological quality of included studies was assessed using the Physiotherapy Evidence Database (PEDro) scale (www.pedro.org.au). The results of the systematicreviewarepresenteddescriptively(e.g.means,standard deviations, and minimum and maximumvalues). Fig. 1. Flowchart of the results of the literature search. 40 Table 1 General characteristics of included studies. Author, year and Design of study Nunber/age/sex and characteristics of Experimental intervention/ Control group/ Mesures of blood pressure/kind of country participants Duration/ intervention device Adhana et al. (2013) 1 group 38adults(8excluded)/menandwomen Pranayama2:1/twiceadayfor5e7min Nocontrol intervention Aresting measure pre intervention and (India) [25] (20e50 years)/recently diagnosed for 3 months. weekly measures of BP/automated hypertension digital Sphygmomanometer Bhavanani et al. (2011) 1 group 23 adults (11 men)/55.13 ± 1.54 years/ Sukha pranayama/5 min Nocontrol intervention Onemeasured pre and post (India) [9] with hypertension intervention/Semiautomatic Bhavananietal.(2012)a 1 group 22 adults (12 men)/58,14 ± 1,69 years/ Chandra Nadi Pranayama/5 min Nocontrol intervention Onemeasured pre and post (India) [10] with hypertension intervention/Semiautomatic J.Z. Bhavananietal.(2012)b 1 group 29 adults (16 men)/49,34 ± 2,36 years/ Pranva Pranayama 1:3/5 min Nocontrol intervention Onemeasured pre and post Bra (India) [19] with hypertension intervention/Digital ndani Bhavanani et al. (2014) 1 group 20 adults (13 women)/34,10 ± 13,62 Surya pranayama vs. chandra Nocontrol intervention Onemeasured pre and post (India) [20] years/8 healthy, 12 reported conditions pranayama vs. surya bhedana vs. intervention/Semiautomatic et such as hypertension, hypothyroidism, chandra bhedana vs. nadi shuddhi vs. al. / type 2 diabetes mellitus, polycystic normal breathing/5min for each Complementary ovary syndrome, bipolar affective pranayama (6 sessions) disorder and others. Critchley et al. (2015) 1 group Twenty-three healthy volunteer Slowbreathingandnormalbreathing/1 Nocontrol intervention Continuous monitoring/Non-invasive (Reino Unido) [21] participants (8 women 12 men; session z 28min. monitor 34.5 ± 10.4 yrs) Goyal, 2014 (India) [26] 2 groups 50 adults with hypertension/ GP: Nadi shodana þ Chadar bhedi, GC: No intervention Onemeasured pre and post Ther Pranayama group (n ¼ 25) and Control Bhramari þ Omkar chanting/6 intervention/Standard apies group (n ¼ 25)/20e50 years/women weeks z 40 min sphygmomanometer and men in Raghuraj et al. 1 group 21 healthy men/27,5 ± 6,3 years right, left, alternate nostril, breath Nocontrol intervention Onemeasured pre and post each Clinical (2008)(India) [22] awareness and normal breathing/5 session/Manual sessions of 40 min Pr Sharma et al. (2013) Randomized/3 90 healthy subjects/without G1:Slowbreathing;G2:Fastbreathing/ GC: No intervention Three BP and HR recordings at 1min actice (India) [27] groups informationonsex/agebetween18and 30 min a day, 3 times per week for 12 intervals were taken and the lowest of 25 years weeks these values was included for the 28 present study/Semi-automatic Telles et al. (2013) Randomized/ 90 adults (60 men)/with hypertension/ G1: Anuloma-villoma pranayama/G2: GC:reading, 10 min per Onemeasured pre and post each (20 1 7 (India) [23] Double Blinded/3 49.7 ± 9.5 years breath awareness/10 min per session session session/Standard mercury ) 3 groups sphygmomanometer 8 e Telles et al. (2014) 2 groups 41 healthy men/PG n ¼ 26 (23.8 ± 3.5 GP: alternate nostril yoga breathing or GC: breathing Continuous monitoring/Non-invasive 46 (India) [24] years) e CG n ¼ 15 (26.1 ± 4.0 years) anulom-vilompranayamaand(b)breath normally/1 session e monitor awareness/2 sessions 25 min 25 min Turankar et al. Randomized, 2 11 healthy males aged between PG: AnulomaViloma technique of CG: normal breathing/ Measuting on the end of all stages/ (2013)(India) [28] groups (27.83 ± 0.91 years)/Pranayama group pranayama with Kumbhak (alternative two sessions of 20 Automatic BP measuring apparatus n ¼ 6, non-pranayama group n ¼ 5 nostril breathing with breath holding)/ mineachdayfor seven two sessions of 20 days mineachdayfor seven days Veerabhadrappa et al. 1 group 50 healthy men/between 18 and 25 MukhBhastrika/30min a day, 5 times Nocontrol intervention Twomeasuredpreandpost (2011) (India) [29] years per week for 12 weeks intervention/Postural Maneuver (supine-standing)/Automatic non-invasive monitor. AbbreviationsRCT: Randomized controlled trials; PG: pranayama group; CG: control group; BP: blood pressure. J.Z. Brandani et al. / Complementary Therapies in Clinical Practice 28 (2017) 38e46 41 assessing pranayamas's chronic effects, BP assessment was per- Total 1/102/102/102/102/101/104/102/105/107/103/105/102/10 formed by means of automatic non-invasive monitor [25,28,29], semiautomatic non-invasive [27] and standard sphygmomanom- eter [26]. Seven studies evaluated mean arterial pressure (MAP) 9,10,20,22 [9,10,19,20,22,27,28] by MAP ¼ DBP þ1/3 x PP , 27 28 PointmeasureY Y Y Y Y Y Y Y Y Y Y Y Y MAP¼DBPþPP/3 ,MAP¼[SBPx(1/3)þDBPx(2/3)] andone study didn't report [19]. Eleven studies assessed heart rate (HR) [9,10,19e22,25e29] by semi-automatic non-invasive BP monitor [9,10,19,20,27], electrocardiogram [26,29], photoplethysmogrophic sensors [25], and Portapres [21]. The method for HR assessment was not reported in two studies [23,24]. Six studies presented Between-groupstatisticalcomparisonNNNNNNYNYYYY N values of rate pressure product (RPP; [RPP ¼ HR x SBP/ 100]9,10,19,20,27; or [RPP ¼ HR x SBP x 102]) [26]. Finally, five to [9,10,19,20,27] studies evaluated the double product (DP; [DP ¼ HR 9,10,19,20 27 x MAP/100] or [DP ¼ HR x MAP] ). IntentiontreatNN N N N N N N N N N N N 3.3. Pranayamas characteristics n i f A detailed description of the pranayamas intervention charac- o % teristics for each study included in the present review is shown in outcome85 Table 3. The studies assessing acute pranayamas effects subjects Keymorethe N Y Y Y Y N Y Y Y Y Y Y Y [9,10,19e24]hadsessionslasting5e40min.Inthestudiesassessing chroniceffects[25e29],thepranayamas'sessionslasted5e40min, all and were performed for 1e12 weeks, with frequency of 3e7 days of per week. There was a great variation of interventions, with programs involving up to four types of pranayamas. All studies assessing BlindingassessorsNNNN N N N N N Y N N N acute effect of pranayamas used slow breathing [9,10,19e24], and five used panayamas with manipulation of the nostrils all [10,20,22e24]. Among the studies evaluating the chronic effect of of pranayamas, three used slow breathing [25,26,28] (two with air retention [26,28]), one used rapid breathing with forced expiration BlindingtherapistsNNNN N N N N N Y N N N [29], oneusedbothslowandrapidbreathingwithforcedexpiration [27], and three studies used pranayamas with manipulation of the of nostrils [26e28]. subjects BlindingallN N N N N N N N N N N N N 3.4. Effects of pranayamas on BP and secondary outcomes Themaineffects of pranayamas on BP and secondary outcomes SimilargroupsNN N N N N Y N Y N N Y N of each study are shown in Table 4. All studies with hypertensive subjects showedthatpranayamaswereeffectivetoacutellyreduce systolic BP (mean BP reduction from 2 to 10 mmHg) [9,10,19,23]; was however, the diastolic BP was reduced only in one studies [23] and after only one type of pranayama (mean BP reduction 1 mmHg). In normotensive subjects, two studies showed systolic BP reduction AllocationconcealedNNNNN N N N N Y N N N after an acute pranayamas session [21,24], and one study showed 22 no effects on BP , for diastolic BP one study showed reduces [22] (mean BP reducion 1 mmHg). Finally, one study with subjects were with different chronic diseases showed a varied acute BP response mly (mean BP reduction from 1 to 4 mmHg) according to the pra- SubjectsrandoallocatedNNNNNN N N Y Y N Y N nayamas performed [20]. Amongthestudiesassessing the chronic effects of pranayamas, PEDro systolic BP was reduced in all studies with hypertensive sub- jects [25,26] (mean BP reduction from 12 to 21). However, in the CriteriaEligibilityYYY Y Y Y Y Y Y Y Y Y Y studies with normotensive subjects, systolic BP was reduced in studies. one[29](meanBPreducionof4mmHg),whiletwostudiesshowed no. no effects of pranayamas on BP27,28, the diastolic BP was reduced 2011 N: only in two studies [25,27], one with hypertensive and other included with normotensive subjects, respectively (mean BP reduction the yes; f year 2011201220122014 4e7mmHg). o 2015 2008 2013 e and 2013 2013 HRwasreducedinfourstudiesassessingthechronic[25e27,29] 2014 20132014 and three acute [9,10,19] effects of pranayamas. DP was reduced 2 scor Author Adhana,Bhavanani,Bhavanani,Bhavanani,Bhavanani,Critchley,Goyal,Raghuraj,Sharma,Telles,Telles,Turankar,Veerabhadrappa,only in one chronic study [27] and three acute [9,10,19] and RPP able T PEDro AbbreviationsY: reduce in two chronic studies [26,27] and three acutes [9,10,19].
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