This text was written for the Journal of Functional Morphology and Kinesiology and published on Oct. 3, 2024
Heart Rate Variability, Blood Pressure and Peripheral Oxygen Saturation during Yoga Adham and Mahat Breathing Techniques without Retention in Adult Practitioners
David Catela, Júlia Santos, Joana Oliveira, Susana Franco and Cristiana Mercê
Abstract: Background: Heart rate variability (HRV) is the change in time intervals between heart beats, reflecting the autonomic nervous system’s ability to adapt to psychological and physiological demands. Slow breathing enhances parasympathetic activity, increasing HRV. Pranayama, a yoga breathing technique, affords the conscious regulation of respiration frequency. This study aimed to characterize HRV, blood pressure and peripheral oxygen saturation of basic yoga breathing slow techniques with regular yoga practitioners. Methods: In total, 45 yoga practitioners were included in the study (including 7 males, mean age of 54.04 ± 11.97 years) with varying levels of yoga experi- ence (minimum 3 months, maximum 37 years). Participants performed three breathing conditions: baseline (control) and two yoga techniques (abdominal (adham) and complete (mahat)) breathing, each for 10 min in the supine position (i.e., savasana). For each condition, respiratory frequency, heart rate (HR), blood pressure and peripheral oxygen levels were collected. Results: The findings revealed that both abdominal and complete yoga breathing techniques promoted a decrease in respi- ratory frequency (p < 0.001, r = 0.61; p < 0.001, r = 0.61, respectively), and an increase in peripheral oxygen saturation (p < 0.001, r = 0.50; p < 0.001, r = 0.46, respectively), along with blood pressure decreases in all mean values, and a significant decrease in systolic pressure, considering all conditions (p = 0.034, W = 0.08). There were significant increases in standard deviation of HR during abdominal and complete yoga breathing techniques compared with the baseline (p = 0.003, r = 0.31; p < 0.001, r = 0.47, respectively), indicating enhanced parasympathetic activity. Moreover, the complete breath- ing technique exhibited the greatest variability in HRV measures, with several significant differences compared with abdominal breathing (standard deviation of HR, p < 0.001, r = 0.42; SD2, stan- dard deviation of points perpendicular to the Poincaré parallel line, p < 0.003, r = 0.31; SD1/SD2, p < 0.003, r = 0.31), suggesting a more profound impact on autonomic modulation. Conclusions: simple, inexpensive and non-intrusive abdominal and complete yoga breathing techniques can effectively and momentarily enhance HRV and oxygen saturation in adults, mature adults and the elderly.
1. Introduction
Heart rate (HR) should have the flexibility and the quickness to adapt to sympathetic and parasympathetic modulating activity branches of the autonomous nervous system; the first being related to energy mobilization, and the latter to vegetative and restorative activity. The prolonged dominance of the sympathetic system, with an augmentation in HR frequency and the consequent reduction in heart rate variability (HRV), i.e., the variation of the time interval between heartbeats, is associated with a diversity of health problems, e.g., [1,2]. A healthy high HRV indicates the capacity of autonomic mechanisms to adapt, whereas a low HRV is indicative of an abnormal and/or insufficient capacity for autonomic system adaptation, which is likely to be associated with some form of physiological dysfunction [3]. Heart rate variability (HRV) has been quantified as an index of vagal activity at designated time points and frequencies. In the time domain, the most frequently employed measures are the standard deviation of the intervals between beats, the standard deviation of R-R intervals (SDNN) (R is a peak represented in the electrocardiogram) and the root mean square of successive differences (RMSSD). In the frequency domain, the spectral powers associated with low frequency (LF) and high frequency (HF) are of primary interest [4]. In LF, an oscillation between 0.04 and 0.15 Hz is predominantly related to vasomotor activity, and, in HF, an oscillation between 0.15 and 0.4 Hz is associated with respiratory activity. HF is regarded as an indicator of the predominancy of vagal efferent activity, whereas LF is considered to reflect sympathetic modulation. Nevertheless, it is postulated that LF and HF are the results of a continuous interaction between the sympathetic and parasympathetic branches of the autonomic nervous system (ANS) [5]; it seems plausible that HF and LF components may reflect parasympathetic activity [6]. To allow a comparison across studies, it is recommended to report the LF and the HF in both absolute and normalized forms, i.e., the natural logarithm of LF (LFn) and HF (HFn) absolute values [7]. Given the intricate interplay between the two branches of the autonomic nervous system (ANS), non-linear methodologies were devised to examine the fluctuations in heart rate (HR) in response to external stimuli. Among these techniques, the Poincaré plot has emerged as a prominent analytical tool, e.g., [8]. The scatterplot depicts a present NN interval plotted against its preceding interval, revealing an ellipsoid configuration of points around a diagonal line (the value against itself). The points situated on the aforementioned line represent the instances of HR deceleration, whereas those located below the line indicate the occurrences of HR acceleration [9]. So, the Poincaré plot can not only be analyzed qualitatively but also quantitatively, where, for the shortest radius of the ellipsoid, the standard deviation of points perpendicular to the diagonal line is estimated (SD1), which has been regarded as the equivalent of RMSSD [10]. The short-term (vagal) NN variability is represented by the longest radius of the ellipsoid, which is parallel to the designated line of identity. The standard deviation of the points is estimated (SD2), which is considered equivalent to SDNN [8], and represents the long-term (sympathetic) NN variability. A third index, SD1/SD2, with similar results to the LF/HF ratio, reflects the sympathovagal balance, e.g., [11]. Qualitatively, Poincaré plot shapes are characterized by a “comet tail” in a healthy heart, whereas, in health problems, narrow,“torpedo” and complex clustered shapes occur, e.g., [12,13].
Slow-paced breathing has significant immediate (acute) effects on reducing systolic and diastolic blood pressure, albeit modestly [14], with an increasing heart rate variability in the time domain, namely the mean square of successive differences between normal heartbeats (RMSSD) and the standard deviation of NN intervals (SDNN), with a decreasing heart rate [15]. Slow breathing at around six cycles per minute provides synchronisation (resonance) between the respiratory and cardiovascular systems [16], with likely enhancement of the parasympathetic nervous system [17] and maximizing heart rate variability [18] and baroreflex sensitivity [19]. Breathing at a rate of six breaths per minute (0.1 Hz) means that it is in the LF band (0.04–0.15 Hz) of the spectral analysis and that changes should be more apparent, e.g., [20]. At 12 breaths per minute (0.2 Hz), it should be expected to be in the HF band (0.15–0.4 Hz), e.g., [8]. A reduction in the number of breaths per minute from 20 (0.33 Hz) to 15 (0.25 Hz) in the presence of a beta-adrenergic blockade has been observed to result in a decrease in the amplitude of low frequency (LF) and an increase in high frequency (HF) amplitude [21]. Slow breathing techniques have been demonstrated to enhance parasympathetic activity, with increased heart rate variability (HRV), thereby providing emotional control and psychological wellbeing [22]. A cumulative effect on HRV can be achieved within a 30-minute period, comprising 10 6-breaths-per-minute ses- sions [23]. A respiratory sinus arrhythmia of 6 breaths per minute is perceived as indicating lower levels of arousal than a rate of 12 breaths per minute [24]. Side effects (e.g., feeling anxious, having intrusive thoughts, feeling out of control) may also decrease. At a rate of 16 breaths per minute, systolic blood pressure changes, always preceded by RR interval changes, suggesting a baroreflex link independent of the sympathetic drive [25]. Even in patients with chronic heart failure, slow breathing has been shown to be beneficial for the cardiovascular system [26]. Below 10 breaths per minute, blood oxygen saturation increases, with increased baroreceptor sensitivity and significant reduction of systolic blood pressure, even at home [27], probably because slow and deep breathing allows a reduction in the high resting sympathetic tone characteristic of patients with chronic heart failure [28]. Slow deep breathing also has a positive effect on systolic and diastolic blood pressure [29–31]. The regular practice of deep breathing may result in long-term reductions in blood pressure, even when compared with the effects of physical activity [32]. The ma- jority of studies examining the effects of yoga techniques on heart rate variability employ a variety of techniques [33] in accordance with the tenets of yoga philosophy. This approach, however, hinders the ability to discern the individual contributions of each technique, thereby limiting the acquisition of a comprehensive understanding of the specific effects on vital signs. Nevertheless, slow breathing yoga techniques are receiving particular attention, namely their effects on blood pressure. These studies frequently involve advanced yoga procedures, such as nostril or breath hold [34]; although, some studies have tried a more controlled approach with external pacing, namely music, e.g., [35]. Breathing as a meditative practice in yoga and an advanced practice called pranayama, through breath control and expansion with retention, allows the conscious regulation of breathing rate, depth and/or the inhalation/exhalation ratio [36]. Prana means breath, respiration, life, vitality, energy or strength, and ayama means stretch, extension, expansion, length, breadth, regulation, prolongation, restraint or control [37]. In the seminal book of the yogic philosophy, Yoga Sutra (II BC– III), Patanjali describes pranayama as the interruption of inhalation and exhalation, cf., [38], and it is classified as the fourth stage on a scale of eight branches, in which the first three are related to the domain of ethical behavior of the individual in society (yama), personal rules of conduct (niyama) and physical postures (asana). The same is said in the Hatha Yoga texts (Hatha Yoga Pradipika, Gheranda Samhita and Shiva Samhita), dating back to the XIV to XVIII centuries, where pranayama is identified with the notion of kumbhaka (retention). Hatha Yoga Pradipika teaches nine different pranayama, Gheranda Samhita I eight and Shiva Samhita one. In all of these books, pranayama refers to techniques with some degree of complexity, to be practiced under the supervision of an experienced teacher, requiring rigorous and sustained preparation in advance [39]. Pranayama is not regarded as a fundamental tenet of yogic philosophy. It is merely a breathing technique designed to facilitate the introduction of extra oxygen into the lungs. In contrast, pranayama employs breathing as a means of influencing the flow of prana (life force) in the energy channels, the nadis of the energy body, pranamaya kosha [40]. A complete respiratory cycle comprises four distinct phases: inhalation (puraka), lung inflation (antara kumbhaka), exhalation (rechaka) and lung deflation (bahya kumbhaka). Considering the body parts involved, the various breathing techniques can be classified into the following four distinct categories [37]: (i) high or clavicular breathing, which involves activating the upper parts of the lungs through the use of the neck the throat and sternum muscles with the upper ribs and the collar bone pulled upwards [40]; (ii) the mid intercostal thoracic region, where only the central part of the lungs is engaged by the expansion and contraction of the ribcage; (iii) adham pranayama, in the low abdominal/diaphragmatic region, where inhalation involves the diaphragm moving downwards and outwards, while exhalation entails the diaphragm moving upwards and abdominal contents moving inwards [40], with the lower portions of the lungs being primarily activated, whereas the upper and central portions remain less active; (iv) mahat yoga pranayama or dirga pranayama, is a complete practice that combines the three types aforementioned, using the entirety of the lungs in their fullest capacity. Although the publishing about the effects of yoga practices on HRV and blood pres- sure [41] is diverse, an analysis of the acute effect of the control breathing element in accessible yoga calming techniques on HRV, blood pressure and peripheral oxygen sat- uration has not yet been carried out. Consequently, the purpose of this study was to characterize the acute effect of accessible yogic calming breathing control techniques on vital signs (heart rate, breathing frequency, blood pressure, peripheral oxygen saturation) and on heart rate variability. Considering the classification presented above, the low abdom- inal/diaphragmatic and complete techniques were specifically chosen for their simplicity, both without retentions [37,42], as they are easily accessible to regular yoga practitioners, even to beginners. Considering the previous literature of slow-paced breathing, we hy- pothesize that abdominal and complete yoga breathing techniques can promote a decrease in respiratory frequency and blood pressure [41,43], along with an increase in peripheral oxygen saturation and HRV [14,15,17].
2. Materials and Methods
2.1. Sample
The sample size was calculated by G∗Power software (version 3.1). Statistical probability value (α) was set at 0.05, statistical power at 0.95 and the non-sphericity correction = 0.5 [44]; the effect size was set at 0.25, as it represents the cutoff for a medium effect [45]; and the correlation between measures was set at 0.7, based on a previous study that evaluated HRV in the same three breathing conditions, i.e., normal breathing at baseline (control condition without any indication), abdominal (adham) and complete (mahat) yoga breathing. The sample size was calculated to be 44. From an initial sample of 50 volunteers, a withdrawal of 5 participants occurred, 2 of them due to individual time constraints, 2 due to the breathing conditions and 1 due to unwellness, resulting in a final sample size of 45 participants.
In order to recruit the sample, a protocol was made with the Portuguese Yoga Federa- tion (FPY) for scientific partnership purposes, ensuring access to yoga certified instructors and regular practitioners. The recruitment of yoga practitioners was carried out by the instructors in order to ensure that practitioners acquired the two yogic breathing techniques. The convenience sample was composed of yoga practitioners (9.44 ± 9.08 years of practice, min 3 months, max 37 years), over 18 years old (54.04 ± 11.97 years old, min 32 years, max 78 years), both sexes (7 males), without exclusion criteria. Eight participants were on medication for hypertension (17.8%), seven were regular smokers (15.6%), seven had psychiatric support with medication (15.6%), five were on medication for asthma (11.1%), four were receiving hormone treatments (8.9%), three were being monitored and medicated for heart problems (6.7%), three were on medication for cholesterol (6.7%), one was on medication for diabetes (2.2%), one had diagnosed sleep apnea (2.2%), one had varicose veins (2.2%) and another was on medication for joint arthritis (2.2%). As some of the partic- ipants presented with multiple health issues and related medication regimes, a complete characterization is presented below (Table 1).
Table 1. Participants with health-confirmed problem characterization
The purpose of such a diversified sample was intentional in order to test the univer- sality of the effects of these yoga techniques with an ample spectrum of ages and health conditions. The percentage distribution among sexes was similar to that found in the Portuguese yoga practitioner census. This project was approved by the research unit ethics committee of the Polytechnique University of Santarém (approval number 2-2023ESDRM), Portugal.
2.2. Experimental Design
This study employed a quasi-experimental design, with subjects serving as their own control, and employed a comparative and associative approach, with a single level of blindness.
2.3. Procedures and Data Treatment
Each volunteer gave informed written consent before this study, in compliance with the Helsinki treaty, and subsequent updates, for human studies. Information about years of yoga practice, health problems and medication were collected. Records were conducted at a Yoga Portuguese Federation center, with subjects in the supine position (i.e., savasana), in a quiet environment, with a room temperature of 19.92◦ (±1.45) and humidity of 56.51% (±8.85). Participants were instructed not to smoke, drink alcohol or coffee 4 h before data collection [4]. The experimental session was structured according to the following sequence: 10 min of rest with normal breathing (control condition without any indication), taken as baseline; and 10 min of each breathing technique: abdominal and complete breathing. The baseline line was always collected first, breathing techniques were alternated among participants (first abdominal = 23; first complete = 22). For the abdominal technique, participants were asked to exhale through their nostrils slowly, while gently contracting their abdomen, and then, to inhale through their nostrils while slowly expanding their abdomen. All the attention remained in the abdominal area. The complete technique was performed by stimulating the release of air through the nostrils in a slow, smooth and complete manner, maintaining the focus of attention from the clavicular region to the abdominal region (exhalation) and then, in the opposite direction, raising awareness from the abdominal region to the clavicular muscle while inhaling slowly, smoothly and completely (inhalation). The RR interval was collected using the Polar©V800 (Polar Electro Oy, Kempele, Finland), which was validated for adults with a combined error rate of 0.086% and an intraclass correlation coefficient (ICC) greater than 0.999 [46], and a chest strap Polar H10, also validated for adults [47]. Data were exported as .txt files and ectopic beats were manually excluded, e.g., [48]. HRV analysis was conducted using gHRV© software, version 1.6 [49]. Blood pressure was recorded at one-minute intervals using a Pic© Solution-Classic Check tensiometer (Grandate, Italy), which fulfils the international protocol requirements, including self-measurement of blood pressure [50]. In accordance with the International Protocol of the European Society of Hypertension [51], the following criteria must be met: age, appropriate cuff size and measurements taken on the left arm at the level of the heart. The frequency of respiratory cycles was observed directly on a minute-by-minute basis, and subsequently validated through the analysis of the respiratory sinus arrhythmia time series for the respiratory techniques. The standard method for respiratory rate measurement is to count the number of movements over a full minute period, observing both the abdominal and chest regions [52]. The counting of respiratory rate for one minute is also a reliable method for infants, e.g., [53]. In the course of our study, the respiratory rate was meticulously recorded at one-minute intervals for a min- imum of ten minutes in each experimental condition. Peripheral oxygen saturation was collected from the index finger of the right hand, using a finger gauge Gima©, Oxi-10 model (Gima SpA, Gessate, Italy; ISO 9001/13485 certificates) [54,55], with a range of 70–100%, an accuracy of ±3% and a perfusion index of 0.2–20%. Gima© models are commonly used as professional wireless fingertip oximeters, and as reference instruments in studies. The peripheral oxygen saturation was recorded for a minimum of 10 min in each of the three conditions, with the data transmitted to a personal computer via wireless Bluetooth technology. Heart rate data were automatically filtered using adaptive thresholds to reject incorrect beats [49]. This method discards beats that exceed the cumulative mean threshold and eliminates data points that fall outside acceptable physiological values. Frequency domain analysis was obtained using a linear interpolation method. As a result, the fil- tered non-equispaced heart rate signal was obtained [56]. The signal was interpolated at a frequency of 4 Hz for the purposes of spectral analysis. The window size and time shift were 120 and 60 s, respectively. For the calculation of non-linear indexes, approximated entropy, SD1 and SD2 were obtained. The normalized power of LF and HF were estimated (e.g., LFn = LF/(VLF + LF + HF)) [23].
2.4. Statistical Treatment
Data were statistically treated with the program IBM-SPSS, version 27. A Shapiro–Wilk test was used to verify data normal distribution. For descriptive statistics, minimum value (min), maximum value (max), mean (mean), error of the mean (error) and standard deviation are presented. For comparisons, the Friedman test was used, with the Monte Carlo test, with effect size Kendall’s W estimation (0.1, small; 0.3, medium; greater than 0.5, strong); followed by the Wilcoxon test, with the Monte Carlo test and Bonferroni correction, in order to conduct a paired group comparison, with effect size r estimation. In the case of associations, the Spearman test (rho) was employed, with 95% confidence intervals (CI). Only those results that were significant and exhibited the same sign within CI were considered.
3. Results
3.1. Temperature and Humidity
Residual associations were found between humidity and vital signs collected. Tempera- ture revealed inverse associations with systolic pressure, in baseline condition (rho = −0.333, p = 0.025, CI [−0.577; −0.035]); with breathing cycles per minute and peripheral oxygen saturation in the abdominal technique condition (rho = −0.331, p = 0.026, CI [−0.575; −0.032]; rho = −0.316, p = 0.039, CI [−0.569; −0.008], respectively).
3.2. Sex
No significant differences were identified between the sexes, except for systolic pres- sure at the baseline (Z = 2.317, p = 0.02, r = 1.64), which was observed to be lower in the female group (108.36 ± 13.45) than in the male group (121.07 ± 10.33). However, it is important to note that the sample size was very small, with only a few males included.
3.3. Age
As anticipated, both systolic and diastolic pressure increased with age in all condi- tions, except for diastolic pressure at baseline. Additionally, peripheral oxygen saturation decreased at baseline and in abdominal conditions. For breathing frequency, a significant inverse association was observed exclusively during the abdominal condition (Table 2, baseline condition).
Table 2. Association (rho, p; confidence intervals, CI 95%) between age and vital signs collected, per condition (baseline; abdominal technique; complete technique).
3.4. Breathing Frequency
Breathing frequency (Table 3) was significantly different between conditions (χr2(45,2) = 69.53, p < 0.001, W = 0.77). Paired comparisons revealed difference among all conditions (complete baseline T = 5.819, p < 0.001, r = 0.61; complete abdominal T = 3.309, p < 0.001, r = 0.35; abdominal baseline T = 5.757, p < 0.001, r = 0.61).
Table 3. Descriptive statistics for vital signs for each condition.
3.5. Blood Pressure
There was a notable discrepancy in systolic pressure (Table 3) across the various conditions (χr2(45,2) = 6.782, p = 0.034, W = 0.08). However, when paired comparisons were conducted with the Bonferroni correction, the results did not reach statistical significance. Nevertheless, the mean systolic pressure was observed to be lower during the practice of yoga breathing techniques. A 62-year-old woman with a confirmed diagnosis of sleep apnea exhibited elevated mean systolic pressure, positioning her as a moderate outlier within the abdominal condition cohort. No significant differences were observed in diastolic pressure (Table 3) between the various conditions (χr2(45,2) = 0.483). A 66-year-old woman exhibited a moderate outlier (higher mean diastolic pressure) in the abdominal condition. Indeed, the two female subjects who were identified as moderate outliers had 12 and 20 years of declared yoga practice, respectively, and were not registered as having probable hypertension. However, it was observed that there was an augmentation in both the mean systolic and diastolic pressures during the breathing yoga techniques in comparison with the baseline measurements. A detailed characterization of this phenomenon is presented in the table below (Table 4).
Table 4. Mean of systolic and diastolic pressures (mean breathing cycles per minute) for each condition in the two women moderate outliers.
3.6. Peripheral Oxygen Saturation
Due to technical problems, the data of peripheral oxygen saturation of two participants were lost.A significant difference was observed in peripheral oxygen saturation between the various conditions (χr2(43.2) = 22.68, p < 0.001, W = 0.26). Paired comparisons revealed no significant difference between the two yoga techniques (complete abdominal T = 0.350, p = 0.726). However, there were significant differences between these breathing techniques and the baseline (complete baseline T = 4.245, p < 0.001, r = 0.46; abdominal baseline T = 4.595, p < 0.001, r = 0.50). The breathing techniques demonstrated greater mean values of peripheral oxygen saturation, reinforced by higher minimum and maximum values, along with a lower standard deviation (Table 3).
3.7. Heart Rate Variability
No significant differences were identified between the sexes with regard to heart rate variability. There was an inverse association between age and almost all estimated temporal parameters, both in baseline and abdominal breath conditions. However, this pattern became less pronounced during complete breathing conditions (Table 5).
Table 5. Association (rho, p; confidence intervals, CI 95%) between age and estimated temporal parameters per condition (baseline; abdominal technique; complete technique).