Abstract
Background and Aims:
Slow, deep breathing (SDB) lowers blood pressure (BP) though the underlying mechanisms are unknown. Redox improvements could facilitate hemodynamic adjustments with SDB though this has not been investigated. The purpose of this randomized, sham-controlled trial was to examine the acute effects of SDB on oxidative stress and endothelial function during a physiological perturbation (high-fat meal) known to induce oxidative stress.
Methods and Results:
Seventeen males (ages 18–35 years) were enrolled, and anthropometric measurements and 7-day physical activity monitoring were completed. Testing sessions consisted of 24-hour diet recalls (ASA24), blood sample collection for superoxide dismutase (SOD) and thiobarbituric acid reactive substances (TBARS) analysis, and flow-mediated dilation (FMD). High-fat meals were ingested and 2-minute breathing exercises (SDB or sham control breathing) were completed every 15 minutes during the 4-hour postprandial phase. Blood sample collection and FMD were repeated 1-, 2-, and 4-hours post meal consumption. Mean body mass index and step counts were 25.6 ± 4.3 kg/m2 and 8165 ± 4405 steps per day, respectively. Systolic and diastolic BP and nutrient intake 24 hours prior were similar between conditions. No time or time by condition interaction effects were observed for FMD. The total area under the curve (AUC) for SOD was significantly lower during SDB compared to the sham breathing condition (p<0.01). No differences were observed in TBARS AUC (p=0.538).
Conclusions:
Findings from the current investigation suggest that SDB alters postprandial redox in the absence of changes in endothelial function in young, healthy males. Clinical trial registration number: NCT04864184.
Keywords: Slow breathing, endothelial function, oxidative stress
Introduction
Slow, deep breathing (SDB) is the second most practiced complementary health approach according to National Health Interview Survey (NHIS) data1 and an emerging intervention of interest in hypertension. Brief bouts of SDB have lowered blood pressure (BP) in hypertensive adults2 and longer 8-week SDB interventions exerted sustained effects reducing clinic3–5 and ambulatory6 BPs while attenuating exercise-induced pressor responses in older adults with isolated systolic hypertension3. Due to mounting evidence supporting the BP-lowering efficacy of SDB, the American Heart Association (AHA) recommended device-guided slow breathing as an adjunctive, non-pharmaceutical means of reducing BP7.
The mechanisms underlying SDB’s hemodynamic effects are not well understood. Results from recent studies suggest involvement of the autonomic nervous system as reductions in sympathetic burst frequency during a bout of SDB have been observed in normotensive8 and hypertensive adults5 as well as individuals with COPD9. Eight weeks of SDB also attenuated the sympathetic response to stress in adults with PTSD10. While these studies used device-guided SDB, slow breathing in the absence of device-guided assistance also elicited immediate declines in salivary pro-inflammatory cytokines in healthy adults 11. As sympathetic innervation is linked with an increase in inflammation, it is likely these mechanisms are intertwined.
While sympathetic neurons exert direct effects on vascular tone increasing peripheral vascular resistance via alpha-adrenergic receptor-mediated vasoconstriction, increased production of reactive oxygen species (ROS) is also a byproduct of sympathetic upregulation12. This increase in ROS leads to nitric oxide scavenging and diminished endothelium-dependent vasodilation. Thus, if SDB reduces SNS activity, it is plausible this practice could also reduce oxidative stress and improve endothelium-dependent vasodilation. Reductions in oxidative stress has been postulated as a potential mechanism inducing physiological alterations with SDB previously13. Moreover, recent pilot work from our lab suggests an increase in relative cutaneous vascular conductance, a previously established NO-dependent measure of microvascular function14, following a 4-week SDB intervention in patients with irritable bowel syndrome15.
High-fat meals instigate a metabolic milieu associated with compromised endothelium-dependent vasodilation16,17 and oxidative stress18. These perturbations are associated with postprandial increases in sympathetic nervous system activation19,20, persist up to 4 hours post meal ingestion in healthy adults, and are more likely to occur in males compared to females21. Such an experimental condition could be useful in detecting changes in oxidative stress and endothelial function attributable to SDB. Accordingly, using a high-fat meal as a stimulus for increased ROS and attenuated endothelium-dependent vasodilation, our primary aims were 1) to determine if SDB could attenuate high-fat meal-induced oxidative stress and 2) to ascertain whether proposed improvements in redox homeostasis with SDB would be linked with preserved endothelial function post-high-fat meal ingestion. We hypothesized that SDB would prevent high-fat meal-induced oxidative stress and declines in FMD.
Methods
Study procedures were approved by the Texas State University Institutional Review Board (Protocol #6275) prior to any data collection and this study was indexed on clinicaltrials.gov April 28, 2021 (Identifier: NCT04864184). Healthy males between the ages of 18 and 35 years were recruited via flyers posted on campus and university-wide mass emails. Exclusion from participation was based upon the presence of any of the following criteria: (i) infection within the previous 4 weeks; (ii) renal disorders; (iii) any cardiovascular disorders such as prior myocardial infarction, known coronary artery disease, personal history of stroke, heart failure, cardiac arrhythmias; (iv) chronic obstructive pulmonary disease; (v) diabetes; (vi) inflammatory bowel disease, HIV, rheumatoid arthritis, chronic or other inflammatory conditions; (vii) current use of blood pressure, statin, steroid or other anti-inflammatory medications; (viii) regular usage of nonsteroidal anti-inflammatory drugs; (ix) smoking; (x) stage 2 hypertension or higher (defined as a systolic BP of ≥140 mm Hg or a diastolic BP ≥ 90 mm Hg); or (xi) lactose intolerance (high-fat meals were dairy-based). All data were collected during the COVID-19 pandemic and participants and members of the investigative team wore facemasks throughout all testing procedures including the slow and sham breathing exercises.
Participants completed 3 sessions after enrollment. Session 1 consisted of BP assessment using an automated cuff (Welch Allyn, Auburn, NY) to ensure participants did not have BPs within the stage 2 hypertension category or higher and distribution of an ActivPal accelerometer (Glasgow, Scotland) for the measurement of physical activity as exercise training status has been demonstrated to affect postprandial responses 22. Participants wore the accelerometers for 7 days prior to returning for sessions 2 and 3. All testing took place in the Cardiovascular Physiology Lab at Texas State University in quiet, temperature-controlled conditions. Participants were asked to fast (water only) for 8 hours and abstain from vitamin C, E, and ᾳ-lipoic acid supplementation at least 3 days, and avoid caffeine, alcohol, and physical exercise 12 hours prior to sessions 2 and 3.
Sessions 2 and 3 were completed at least 7 days apart and consisted of height and body mass measurements, BP assessment using an automated cuff, an antecubital blood draw for later assessment of oxidative stress markers, completion of the ASA24-hour dietary recall (prior dietary intake may influence postprandial responses), and flow-mediated dilation (FMD). Blood pressure was assessed in triplicate while the subject was seated upright after a 5-minute resting period. Blood samples were obtained after 5 minutes (min) of supine rest, clotted at room temperature for 25 min, then centrifuged at 4°C for 20 min prior to serum aliquot storage at −80°C.
After 15 min of supine rest, simultaneous brachial artery diameter and blood flow velocity acquisition ensued using a Doppler ultrasound machine (Samsung, Danvers, MA) equipped with a high-resolution linear array transducer according to current recommendations23. A probe holder secured the ultrasound probe on the upper arm of each participant to obtain a longitudinal image 5–10 centimeters proximal to the right antecubital fossa while maintaining consistency in insonation angles (≤60–70°) and depths between measurements. Measurement sites were marked to ensure consistency in location for each subsequent FMD assessment. After a 1-minute baseline assessment, a forearm cuff was inflated to 50 mmHg above resting systolic BP for 5 min. After cuff deflation, brachial artery diameters and blood flow velocity were measured continuously for 3 min and FMD results were quantified using Quipu software (Pisa, Italy) and expressed as a percentage change in arterial diameter from baseline during the 3-minute reactive hyperemia phase.
High-Fat Meal
Participants were given vanilla milkshakes consisting of Breyer’s French vanilla ice cream, heavy whipping cream, and whole milk. This milkshake recipe has previously been demonstrated to evoke oxidative stress24. Milkshake ingredient quantities were adjusted based on the participant’s body mass. For subjects weighing 70 kilograms (kg), recipes consisted of 2 cups of ice cream, 1 cup of whole milk, and 2 tablespoons of heavy cream. Ice cream quantities were increased by 0.25 cups per 5 kg increase in body mass. Whole milk measurements remained consistent up to a body mass of 100 kg, where the quantity was then increased to 1.25 cups with no further increases. Three tablespoons of heavy cream were used up to a body mass of 75 kg with 1-, 1.5-, and 2-tablespoon increases at 80 kg, 95 kg, and 110 kg, respectively. Participants were given 5 minutes to fully ingest the milkshakes after baseline blood draws and FMD.
Device-Guided Breathing Interventions
Fifteen min after milkshake ingestion, breathing exercises were initiated. Breath frequency/protocol selection was based upon random number generation using randomizer.org. Participants were not given details about the slow breathing focus of the trial and told instead that purpose of the study was “to learn whether different breathing styles affect blood vessel function and other molecular changes after ingesting a high-fat meal.” No further information was given until study completion to avoid the influence of subject expectations or biases on study outcomes.
The Breathing App which uses audio and visual cues to guide users through inhalation and exhalation cycles was used to guide participants through 2-minute breathing exercises every 15 min after high-fat meal ingestion. During the SDB session, The Breathing App was set to a 4:6 inhale/exhale ratios resulting in a respiratory rate of 6 breaths per minute. During the sham breathing session, the app was set to a 2:3 inhale/exhale ratio (12 breaths per minute). Respective breathing exercises were completed every 15 min throughout the 4-hour post-prandial period. We adapted this protocol previously used which implemented relaxation breathing bouts every 10 minutes during an oral glucose tolerance test showing a significant reduction in blood glucose concentrations during SDB25.
Postprandial Measurements
Postprandial measurements of FMD and venipuncture were completed during both SDB and sham breathing sessions 1, 2, and 4 hours post-meal ingestion.
Oxidative Stress Markers
Serum aliquoted from whole blood samples was stored at −80°C prior to later analysis of superoxide dismutase (SOD: 0.005 U/ml minimum detectable concentration) and thiobarbituric acid reactive substances (TBARS: 0.0625 μM minimum detectable concentration). SOD activity and TBARS were measured via commercially available assay kits (Cayman Chemical Company, Item No. 706002 & 700870) according to the manufacturer’s instructions. SOD is an enzyme which catalyzes the dismutation of superoxide to hydrogen peroxide. The assay kit used measures SOD activity via the dismutation of superoxide generated by xanthine oxidase and hypoxanthine and values were expressed as U/mL/mg of protein. Lipid peroxidation is a consequence of oxidative stress resulting in the formation of malondialdehyde (MDA). The TBARS TCA method kits measure MDA through controlled reactions with TBARS and MDA concentrations were expressed as μM. Absorbance was determined using a colorimetric plate reader (BioTek, Winooski, VT). The intra- and inter-assay %CV was <10% for all assays. In addition, the total area under the curve (AUC) was calculated for SOD and MDA using the trapezoid method.
Statistical Analysis
Data normality was assessed using Shapiro-Wilk tests. Data were normally distributed and thus, parametric statistical tests were deployed for all analyses. Paired samples t-tests were used to compare ASA 24-hour recall results, step counts per day, baseline BP, brachial artery diameter, FMD, SOD, and MDA, and the total AUCs for SOD and MDA between breathing conditions. Repeated measures ANOVAs with time and condition (sham or SDB) as within- and between-subjects factors, respectively, were used to compare changes in means from baseline and at 1, 2, and 4 hours post-meal ingestion for baseline brachial artery diameter, FMD, SOD, and MDA.
Results
Of 65 adult males prescreened for participation, 29 were excluded due to having at least exclusionary criterion, 15 were lost to follow up prior to scheduling the first testing session, and 21 were enrolled. After enrollment, another 4 participants were lost to follow up after completing at least 1 initial testing session, and 17 completed the study. The ethnic and racial demographic data for study participants is as follows: 8 Hispanic/Latinx; 9 Non-Hispanic/Latinx; 9 white; 1 African American; 1 Asian; 1 Pacific Islander; and 3 Other. Randomization of session order resulted in 9 of the 17 subjects completing the SDB condition first.
Baseline anthropometric, hemodynamic, and other selected subject data are presented in Table 1. The mean age and BMI of study participants were 25±4 years and 25.6±4.3 kg/m2, respectively. Twenty-four-hour diet recalls also revealed similar total caloric and fat, protein, and carbohydrate and other nutrient intake the prior to both testing sessions (Table 1). Accelerometer results are shown in Table 2. Participants averaged 8,165±4,405 steps per day indicating moderate levels of physical activity26. Baseline brachial systolic and diastolic BP and FMD were similar between conditions (Table 1; Figure 1; p=0.955, 0.517, & 0.817, respectively). Baseline brachial artery diameters were similar at all timepoints (p= 0.573 for time) and between conditions (p=0.777 for time by condition interaction). No effects of time (p=0.86) or time by condition interaction effects (p=0.853) were observed for brachial artery FMD.
Table 1.
Selected Subject Characteristics
Normal Breathing | Slow Deep Breathing | |
---|---|---|
Age (years) | 25 ± 4 | - |
Height (cm) | 176.8 ± 7.4 | - |
Body Mass (kg) | 80.1 ± 16 | - |
Body Mass Index (kg/m2) | 25.6 ± 4.3 | - |
Systolic Blood Pressure (mm Hg) | 123 ± 9 | 123 ± 10 |
Diastolic Blood Pressure (mm Hg) | 77 ± 9 | 76 ± 9 |
Pulse Pressure (mm Hg) | 46 ± 8 | 48 ± 9 |
Baseline Brachial Artery Diameter (mm) | ||
Before Meal Ingestion | 3.9 ± 0.4 | 3.9 ± 0.5 |
1 hour post | 3.8 ± 0.3 | 3.9 ± 0.5 |
2 hours post | 3.9 ± 0.3 | 3.8 ± 0.6 |
4 hours post | 3.8 ± 0.5 | 3.9 ± 0.5 |
24-Hour Diet Recall Results | ||
Total Energy Intake (kcal) | 1995 ± 777 | 2286 ± 1071 |
Protein (g) | 97 ± 58 | 96 ± 50 |
Fat (g) | 88 ± 42 | 101 ± 57 |
Carbohydrate (g) | 209 ± 74 | 242 ±120 |
Water (g) | 2351 ± 1382 | 2318 ± 1105 |
Sugar (g) | 70 ± 43 | 97 ± 74 |
Fiber (g) | 21 ± 12 | 20 ± 10 |
Cholesterol (mg) | 313 ± 280 | 379 ± 233 |
Sodium (mg) | 3751 ± 2180 | 3633 ± 1683 |
Vitamin C (mg) | 65 ± 65 | 65 ± 68 |
Vitamin E (mcg) | 10 ± 8 | 9 ± 7 |
Data are presented as means ± standard deviations.
Table 2.
Physical Activity Characteristics
Weekday | Weekend | |
---|---|---|
Step Counts (steps/day) | 8030 ± 4070 | 8306 ± 5865 |
Time Seated (hours) | 18.9 ± 3.2 | 19 ± 3 |
Time Standing (hours) | 3.2 ± 2.4 | 3.3 ± 2.4 |
Time Active (hours) | 1.6 ± 0.8 | 1.7 ± 1.2 |
Data are presented as means ± standard deviations.
Figure 1. Baseline and postprandial flow-mediated dilation during normal and slow breathing conditions.
Brachial artery endothelial function was preserved following ingestion of the high-fat meal and no differences between conditions were observed. Data are presented as means ± standard error of the mean.
Results from SOD activity and MDA serum concentrations and total areas under the curves are depicted in Figure 2. At baseline SOD activity and MDA concentrations were similar between conditions (p=0.481 & 0.556). No effects of time (p=0.225) or time by condition interaction effects (p=0.19) were observed for SOD. There was a significant effect of time on MDA concentrations (p<0.05) with no time by condition interaction effects evident (p=0.625). The total AUC for SOD was significantly lower during the slow breathing compared to the sham breathing condition (p<0.01). The total AUC for MDA was similar between conditions (p=0.538).
Figure 2. Changes in postprandial oxidative stress parameters during normal and slow breathing conditions.
Lipid peroxidation (MDA) increased during the postprandial phase though no differences were noted between conditions. Superoxide dismutase activity was significantly lower during the slow breathing compared to the normal breathing condition. Data are presented as means ± standard error of the mean.
Discussion
To our knowledge, this is the first sham-controlled study to investigate the effects of SDB on markers of oxidative stress. Moreover, to our knowledge, this is the first examination of the effects of SDB on macrovascular endothelial function. Results showed that repeated bouts of SDB at 6 breaths per minute significantly attenuated SOD activity following ingestion of the high-fat meal. These changes in antioxidant activity during SDB were unaccompanied by significant effects on endothelial function as FMD was preserved throughout the 4-hour postprandial phase in both conditions.
Our hypothesis that SDB would prevent high-fat meal-induced oxidative stress was based upon combined findings showing an immediate reduction in MSNA during SDB in normotensive adults8 and an increase in superoxide after norepinephrine infusion in healthy volunteers12. We anticipated a dampening effect of SDB on markers of oxidative stress following a high-fat meal likely attributed to decreased SNS activation. The lower SOD AUC during the SDB condition compared to normal breathing supports our hypothesis as superoxide production increases SOD activity via redox sensitive pathways. Gomez-Cabrera, et al.27 were among the first to demonstrate this mechanism in rodents showing that reactive oxygen/nitrogen species inhibition via allopurinol prevented the upregulation of SOD protein expression after a bout of exercise. Additional work in rodent models demonstrated a significant increase in SOD activity was associated with increases in MDA concentrations following high-fat, high-fructose diets 28,29. Thus, it is likely the lower SOD activity observed during SDB in the current study reflects an attenuation of reactive oxygen species production.
Lower SOD activity during the slow breathing condition could be attributed to a direct effect of SDB on the vagus nerve. Similarities in the effects of SDB and vagal nerve stimulation have been previously noted. Reductions in sympathetic nerve activity and increased baroreflex sensitivity (BRS) during a bout of SDB9,13,30 mimic the effects of direct vagal stimulation which, in addition to lowering sympathetic activation and improving BRS, has also been demonstrated to reduce reactive oxygen species31–33.
In addition to oxidative stress, inflammation has been shown to accompany the postprandial response. Increases in IL-1β, IL-6, and TNF-ᾳ up to 6 hours post high-fat or high-carbohydrate meal ingestion have been previous observations in the literature34. One study demonstrated reductions in IL-1β and IL-8 up to 20 minutes after a single, 20-minute slow breathing bout in health adults 11. As inflammation triggers the production of free radicals29, it is possible reductions in inflammation with SDB could have facilitated decreased reactive oxygen species production during the postprandial phase. It is important to note that this trial11 implemented non-device-guided breathing though the current study implemented a device-guided breathing protocol. Evidence suggests differential effects of device-guided and non-device-guided breathing on blood pressure35,36. Thus, direct comparisons between SDB studies using device-guided and non-device guided modalities should be made with careful consideration.
While MDA concentrations increased slightly following ingestion of the high-fat meal, SDB had no effect on this outcome. Accelerometer-based step counts and self-reported physical activity suggest these participants were moderately active26 which could have contributed to this result. It has previously been demonstrated that postprandial lipid peroxidation is attenuated in exercise trained adults37. Thus, it is possible these participants could have been able to buffer some of the changes in oxidative stress posed by the high-fat meal and that SDB had no additional effects. Future studies should expand on these findings by including additional markers of oxidative stress.
Endothelium-dependent vasodilation was preserved following high-fat meal ingestion. This result is consistent with previous trials in healthy young men and exercise trained adults22,38. It could be that due to training status of the participants in the present trial as indicated by moderate levels of physical activity, the negative effects of high-fat intake on endothelial function could have been prevented. It is also possible the high-fat meal used in the current study, while sufficient to induce oxidative stress, might not have been an adequate stressor to evoke endothelial dysfunction. Meal fat content was a correlate of postprandial declines in FMD according to a recent review21; however, after controlling for confounding variables, the authors found this association not significant at 2 and 4 hours post meal ingestion. Therefore, it is unlikely meal nutrient composition was a significant factor in the current trial21.
While SDB can be practiced in isolation using device-guided or non-device-guided modalities, it is also an integral part of yoga, a discipline consisting of 8 limbs, among them and most practiced in the U.S., are postures (asanas) and regulated breathing (pranayama). Most physical yoga disciplines like vinyasa or hot yoga incorporate some form of regulated breathing. In fact, typical hot yoga classes, which our group has previously demonstrated to improve endothelial function39, begin with approximately 5 minutes of SDB. While no effects of SDB on FMD were observed, our results lend support for the notion that previous observations of improvements in oxidative stress following regular yoga engagement could be mediated by slow breathing alone in the absence of yoga postures40.
Slow breathing is a widely accessible practice given its minimal cost and diversity of locales in which it can be practiced with participants being able to practice at home or any other location. Slow breathing can also be practiced by individuals with a range of physical capabilities requiring minimal to no physical exertion. These facets make it an attractive candidate for therapeutic intervention. Strengths of the current study include the randomized, sham controlled, crossover design, randomization of SDB and sham breathing session order, the assessment of physical activity via accelerometer-based step counts, the assessments of prior nutrient intake before both conditions, and repeated measurements if FMD and oxidative stress over the course of 4 hours. However, the current study also has limitations including the relatively small sample size, the lack of exploration of other oxidative stress markers to obtain a more comprehensive view, and the lack of inclusion of female participants. A recent review 21 concluded that males are more likely to exhibit postprandial declines in FMD compared to males. Thus, the focus on males in the current study seemed appropriate.
In conclusion, results from this investigation show alterations in postprandial oxidative stress with SDB compared to normal sham breathing. Slow breathing was associated with lower postprandial antioxidant enzymatic activity as demonstrated by lower SOD AUC during SDB compared to the sham breathing condition. Endothelium-dependent was preserved throughout the postprandial state during both breathing conditions.
Highlights:
Slow, deep breathing reduced antioxidant enzyme activity after a high-fat meal in young, healthy adult males.
Lipid peroxidation was unaltered by slow or sham breathing during the postprandial state.
Flow-mediated dilation was preserved following high-fat meal ingestion despite a modest increase in lipid peroxidation.
Acknowledgements
We would like to thank all the participants who volunteered for this trial during the COVID-19 pandemic. We would also like to thank Karen A. Lewis, PhD, Mathilde L. Canet, and Isaac H’Luz for their assistance with assays and other study procedures.
Funding
This study was funded by an internal grant from Texas State University. The funding source played no role in the design and conduct of this project.
Footnotes
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Clinical Trials Identifier: NCT04864184
Competing interests
There are no competing interests to disclose.
Conflicts of Interest
The authors have no conflicts to disclose.
Data availability statement
All data used in the generation of results for the current study have been included in the manuscript.
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Associated Data
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Data Availability Statement
All data used in the generation of results for the current study have been included in the manuscript.