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Article
Slow-Paced Breathing: Influence of Inhalation/Exhalation Ratio
and of Respiratory Pauses on Cardiac Vagal Activity
Sylvain Laborde 1,2,*, Maša Iskra 1, Nina Zammit 1, Uirassu Borges 1,3, Min You 4, Caroline Sevoz-Couche 5
and Fabrice Dosseville 6,7
1 Department of Performance Psychology, Institute of Psychology, German Sport University Cologne,
Cologne 50933, Germany; masa.iskra@gmail.com (M.I.); ninazt27@gmail.com (N.Z.)
2 UFR STAPS, EA 4260 CESAMS, Normandie Université, 14000 Caen, France
3 Department of Health & Social Psychology, Institute of Psychology, German Sport University Cologne,
50933 Cologne, Germany; u.borges@dshs-koeln.de
4 UFR Psychologie, EA3918 CERREV, Normandie Université, 14000 Caen, France; you.min14@gmail.com
5 INSERM, Unité Mixte de Recherche (UMR) S1158 Neurophysiologie Respiratoire Expérimentale et Clinique,
Sorbonne Université, 75000 Paris, France; caroline.sevozcouche@gmail.com
6 UMR-S 1075 COMETE, Normandie Université, 14000 Caen, France
7 INSERM, UMR-S 1075 COMETE, 14000 Caen, France; fabrice.dosseville@unicaen.fr
* Correspondence: s.laborde@dshs-koeln.de, +49-221-49-82-57-01
Abstract: Slow-paced breathing has been shown to enhance the self-regulation abilities of athletes
via its influence on cardiac vagal activity. However, the role of certain respiratory parameters (i.e.,
inhalation/exhalation ratio and presence of a respiratory pause between respiratory phases) still
needs to be clarified. The aim of this experiment was to investigate the influence of these respiratory
parameters on the effects of slow-paced breathing on cardiac vagal activity. A total of 64 athletes
(27 female; Mage = 22, age range = 18–30 years old) participated in a within-subject experimental
design. Participants performed six breathing conditions within one session, with a 5 min washout
period between each condition. Each condition lasted 5 min, with 30 respiratory cycles, and each
respiratory cycle lasted 10 s (six cycles per minute), with inhalation/exhalation ratios of 0.8, 1.0, 1.2;
and with or without respiratory pauses (0.4 s) between respiratory phases. Results indicated that
the root mean square of successive differences (RMSSD), a marker of cardiac vagal activity, was
higher when exhalation was longer than inhalation. The presence of a brief (0.4 s) post-inhalation
and post-exhalation respiratory pause did not further influence RMSSD. Athletes practicing slow-
paced breathing are recommended to use an inhalation/exhalation ratio in which the exhalation
phase is longer than the inhalation phase.
Keywords: cardiac vagal activity; slow-paced breathing; respiratory parameters; RMSSD
1. Introduction
During sport competitions, athletes are required to effectively regulate their emo-
tions [1–3] and cope with stressors [4,5]. Among the strategies addressing athletes’ emo-
tional regulation, slow-paced breathing (SPB), the voluntarily slowing down of breathing
frequency, has been increasingly used (e.g., [6,7–9]). However, the effectiveness of varying
certain parameters of SPB, such as the inhalation/exhalation ratio and the presence of a
respiratory pause (i.e., brief cessation of air flow) between respiratory phases, still needs
to be understood. Consequently, the current study aims to further understand the role of
varying these two parameters on the effectiveness of SPB, as measured by cardiac vagal
activity (CVA), an indicator for self-regulation mechanisms [10–16].
SPB is a technique used to decrease overall activation and trigger relaxation [17]. It
involves timed inhalation and exhalation periods (“paced”), at a rate of around six cycles
per minute (cpm), which is at least half as slow than the spontaneous breathing rate,
Citation: Laborde, S.; Iskra, M.;
Zammit, N.; Borges, U.; You, M.;
Sevoz-Couche, C.; Dosseville, F.
Slow-Paced Breathing: Influence
of Inhalation/Exhalation Ratio
and of Respiratory Pauses
on Cardiac vagal activity.
Sustainability 2021, 13, 7775.
https://doi.org/10.3390/su13147775
Academic Editors: Santos Villafaina,
Juan Pedro Fuentes García and
Daniel Collado-Mateo
Received: 25 May 2021
Accepted: 9 July 2021
Published: 12 July 2021
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Copyright: © 2021 by the authors. Li-
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tribution (CC BY) license (http://crea-
tivecommons.org/licenses/by/4.0/).
Sustainability 2021, 13, 7775 2 of 14
normally ranging between 12 and 20 cpm [18,19]. The exact mechanisms by which SPB
influences emotion regulation are still debated, but they are likely to involve the strength-
ening of the baroreflex, the action on pulmonary afferents, as well as specific oscillations
in brain networks involved in emotion regulation [20–25]. Overall SPB is suggested to
trigger the activation of the vagus nerve [21], the main nerve of the parasympathetic nerv-
ous system which is responsible for rest and digest functions, as well as self-regulation
within the body [11,26,27].
Heart rate variability (HRV), the variation in the time intervals between adjacent
heart beats [10,28,29], is a non-invasive indicator of CVA, as explained by the neurovis-
ceral integration model [11,27]. Among the time domain measures of the HRV parameters
that index CVA, the root mean square of successive differences (RMSSD) is commonly
used. The interpretation of the physiological underpinnings of HRV frequency parame-
ters requires taking into account the respiratory frequency. When breathing frequency is
higher than 9 cpm, CVA is reflected in the high-frequency (HF) band [10,28,29]. However,
when breathing frequency is lower than 9 cpm, CVA is then shifted to low-frequency (LF)
HRV [30]. Given that RMSSD is relatively free from respiratory influences, and more sta-
tistically reliable than frequency-domain indicators [31,32], it is the main outcome of in-
terest in this study.
CVA, whether considering its resting, reactivity, or recovery levels [12], has been
found to be related to different cognitive and physical aspects of sport performance. For
example, morning resting measurements have been used to monitor the effects of training
loads, to adjust training loads, and to predict subsequent performance [33–35]. Addition-
ally, CVA has been linked to executive cognitive performance in athletes [36–40], to their
coping effectiveness with stress and pressure [37,41–46], and to sport performance, such
as shooting [47,48] and dart throwing performance [49]. Consequently, increasing CVA
can be considered an appropriate aim for athletes.
Among the methods used to increase CVA [50–52], SPB has been found to be effective
in athletes, either combined with biofeedback [53,54] or without biofeedback (e.g., [6,7–
9]). Biofeedback includes displaying physiological variables of interest (e.g., heart rate,
heart rate variability, respiratory frequency) to the person being monitored, through real-
time measures realized with a dedicated device, smartphone, or a computer [55]. The use
of biofeedback may contribute to additional motivation through providing positive rein-
forcement to the client [25,55–57]. Additionally, biofeedback can assist in identifying the
breathing pattern that leads to the highest CVA increase [24,25,58,59]. Nonetheless, so far,
no clear evidence has emerged of the physiological benefits of adding biofeedback to SPB
[60]. Consequently, the current study focuses on SPB without biofeedback, given that from
an applied perspective, it requires athletes to use less technology.
SPB without biofeedback has been associated with positive cognitive and physiolog-
ical outcomes in athletes [8,9,61–63]. More specifically, positive effects were found on ex-
ecutive functions such as inhibition in resting conditions [61,62], working memory, and
cognitive flexibility [62], and after physical exertion on inhibition [9]. A robust increase in
CVA during SPB has systematically been found, even if the effects tend to cease immedi-
ately upon stopping SPB [8,62]. Importantly, long-term SPB interventions (15 min per day
for 30 days) seem to trigger increases in resting CVA [63].
Regarding the characteristics of SPB, it is usually performed with a longer exhalation
than inhalation phase [24,25]. Adapting a longer exhalation phase is suggested to create a
larger increase in CVA, as can be explained through the properties of respiratory sinus
arrhythmia (RSA) [64,65]. RSA reflects the influence of respiration on heart rate—more
specifically, the fact that heart rate increases with inhalation, and decreases with exhala-
tion [66,67]. Inhalation is driven by sympathetic nervous activity, and exhalation by par-
asympathetic nervous activity. Theoretically, a longer exhalation would activate the par-
asympathetic nervous system more strongly. This has been confirmed experimentally in
previous research [64,65], where a longer exhalation phase in comparison to inhalation
was found to provoke larger increases in RSA, as calculated by the difference between
Sustainability 2021, 13, 7775 3 of 14
maximum and minimum cardiac interbeat intervals per breath. Although this way of cal-
culating RSA is suggested to reflect CVA, it does not belong to the classic HRV parameters
recommended to index CVA [10,28,29]. In addition, Strauss-Blasche, Moser, Voica,
McLeod, Klammer and Marktl [65] did not focus on SPB (10 cpm), SPB being characterized
by breathing frequencies lower than 10 cpm [22]. Additionally, the sample sizes used in
those previous studies were rather small, with N = 12 [65] and N = 23 [64]. The inhala-
tion/exhalation ratio was also investigated by Lin, et al. [68]. Contradictory to previous
studies, they concluded that an equal inhalation/exhalation ratio was the most beneficial
regarding HRV. However, this experiment presents several drawbacks: RMSSD was not
reported, and among the variables reported, only LF may have indexed CVA. However,
the findings are difficult to interpret, due to the use of a between-subject design involving
N = 11 or N = 12 in each of the four respiratory patterns (6 cpm 5:5; 6 cpm 4:6; 5.5 cpm 5:5;
and 5.5 cpm 4:6). Finally, Edmonds, Kennedy, Hughes and Calzada [58] investigated the
influence of different breathing patterns around 6 cpm: 1:1 breathing ratio with post-in-
halation and post-exhalation respiratory pauses, 1:1 ratio with no respiratory pauses, 1:2
breathing ratio with no respiratory pauses, 1:2 with post-inhalation and post-exhalation
respiratory pauses, and finally, a condition requiring the participants to breathe in sync
with their heart rate. The focus was not on between-subject analysis, but on within-subject
analysis, and the authors found that for each participant, a specific breathing pattern pro-
duced the highest increase in LF. Moreover, all breathing patterns were found to produce
a descriptive increase in LF; however, no inferential statistics were run at the group level
to investigate differences between breathing patterns. To sum up, given the large interin-
dividual variability of HRV frequency-domain variables [10,69] and the lower reliability
of frequency parameters when breathing characteristics are modified [31,32], we wanted
to address in this study the shortcomings of previous experiments by using a larger sam-
ple size, measuring RMSSD as a robust indicator of CVA, which is relatively free from
respiratory influences, and by using a within-subject design.
The second parameter of interest in this study is the presence of a post-inhalation and
post-exhalation respiratory pause during SPB, an aspect that has received very little at-
tention so far (for an exception, see [70]). In [70], the authors tested the influence of a post-
exhalation respiratory pause on HRV (4 s). In comparison to a condition without post-
exhalation respiratory pause, a post-exhalation respiratory pause showed a higher HF-
HRV, while no differences were found regarding RMSSD and LF-HRV. The authors con-
cluded that a post-exhalation respiratory pause improves CVA and hence self-regulatory
control. However, this interpretation of the results is likely inaccurate, given that HF-HRV
does not reflect CVA when breathing frequency is lower than 9 cpm [10,28,29]. The pattern
of results based on the increase in both RMSSD and LF from baseline in both conditions,
with and without post-exhalation respiratory pause, suggests that they both trigger an
increase in CVA. Finally, the authors did not provide a physiological rationale for having
a post-exhalation respiratory pause besides triggering a higher HF-HRV. Other authors
suggested that a post-inhalation respiratory pause may trigger bradycardia via a rapid
activation of vagal activity, based on the effects of breath-holding [71]. It may be specu-
lated that SPB provokes a certain strain on respiratory muscles due to the forced and pro-
longed inhalation and exhalation phases, and would potentially also result in hyperven-
tilation with increased tidal volume [70]. Consequently, the current study aimed to test
the influence of a brief post-inhalation and post-exhalation respiratory pause on CVA.
To sum up, research points to positive effects of SPB without biofeedback on CVA
[8,9,62,63]. However, the influence of certain characteristics of SPB still needs to be clari-
fied, such as the influence of the inhalation/exhalation ratio, as well as the presence of a
respiratory pause between the respiratory phases. The current study therefore aims to
address these issues. Regarding the inhalation/exhalation ratio, we hypothesize that a
longer exhalation phase in comparison to inhalation would trigger larger increases in
CVA [64,65]. Regarding the respiratory pause, we hypothesized that a brief post-inhala-
tion and post-exhalation respiratory pause may potentially produce a bradycardia and
Sustainability 2021, 13, 7775 4 of 14
reduce the demands on respiratory muscles, therefore resulting in a greater increase in
CVA [70,71].
2. Materials and Methods
2.1. Participants
Regarding sample size, previous research on this topic using a within-subject design
had a rather low sample size, N = 12 for Strauss-Blasche, Moser, Voica, McLeod, Klammer
and Marktl [65], and N = 23 for Van Diest, Verstappen, Aubert, Widjaja, Vansteenwegen
and Vlemincx [64]. Following recommendations for HRV research [10,69], we recruited 66
athletes to take part in this research project. Athletes were here defined as individuals
regularly engaging in sport training. Recruiting a homogenous athletic sample helps to
limit inter-individual differences in HRV that can be found in the general population, en-
abling a better interpretation of the findings [69]. Exclusion criteria were self-reported car-
diovascular diseases and other chronic diseases that might influence breathing or HRV
patterns, such as asthma, diabetes, psychiatric, and neurological diseases [10]. Due to tech-
nical issues, the data of 2 participants had to be excluded, and the final sample comprised
64 athletes (27 female; MAge = 22, age range = 18–30 years old; BMI: M = 23.10, SD = 2.16;
waist-to-hips ratio: M = 0.80, SD = 0.08; number of sport hours per week: M = 7.5 h; SD =
3.2). The experimental protocol was approved by the Ethics Committee of the local uni-
versity (Project Identification Code 06/11/2014).
2.2. Material and Measures
2.2.1. Heart Rate Variability
HRV was measured with an ECG device (Faros 180°, Bittium, Kuopio, Finland) at a
sampling rate of 500 Hz. Two disposable ECG pre-gelled electrodes (Ambu L-00-S/25,
Ambu GmbH, Bad Nauheim, Germany) were used. The negative electrode was placed in
the right infraclavicular fossa (just below the right clavicle) while the positive electrode
was placed on the left side of the chest, below the pectoral muscle in the left anterior axil-
lary line. From ECG recordings, we extracted RMSSD with Kubios (University of Eastern
Finland, Kuopio, Finland). The ECG signal was visually inspected for artefacts and these
were corrected manually in the cases required (<0.001% of the heartbeats), as recom-
mended by Laborde, Mosley and Thayer [10]. In order to provide an overview of the dif-
ferent HRV parameters, following Laborde, Mosley and Thayer [10], we also extracted the
R-R interval, the heart rate, the standard deviation of the NN interval (SDNN) for the
time-domain and the frequency domain with Fast Fourier Transform LF (0.04 to 0.15 Hz),
HF (0.15 to 0.40 Hz), and the LF/HF ratio. Respiratory frequency was computed via the
ECG-derived respiration algorithm of Kubios [72].
2.2.2. Slow-Paced Breathing
Similar to previous research (e.g., [8,73]), SPB was conducted with a video showing
a ball moving up and down at the rate of 6 cpm, based on the EZ-Air software (Thought
Technology Ltd., Montreal, Canada). Participants were instructed to inhale continuously
through the nose while the ball was going up, and exhale continuously with pursed lips
when the ball was going down. The video displayed a 5 min SPB exercise, with six condi-
tions, varying in the inhalation/exhalation ratio (inhalation = exhalation; inhalation > ex-
halation; inhalation < exhalation) and the presence/absence of a respiratory pause (0.4 s)
after both inhalation and exhalation phases (see Figure 1). The inhalation/exhalation ratio
was 4.5 s/5.5 s and 5.5 s/4.5 s, based on Allen and Friedman [74]. The six conditions were
the following: 4.6 s/0.4 s/4.6 s/0.4 s (inhalation/exhalation ratio = 1.0); 4.1 s/0.4 s/5.1 s/0.4 s
(inhalation/exhalation ratio = 0.8); 5.1 s/0.4 s/4.1 s/0.4 s (inhalation/exhalation ratio = 1.2);
5 s/5 s (inhalation/exhalation ratio = 1); 4.5 s/5.5 s (inhalation/exhalation ratio = 0.8); 5.5
s/4.5 s (inhalation/exhalation ratio = 1.2).
Sustainability 2021, 13, 7775 5 of 14
.
Figure 1. The six breathing conditions, realized in a randomized order during the experiment. Note: ascending arrows
depict the inhalation phase and descending arrows depict the exhalation phase; I: inhalation, E: exhalation; time indicated
in seconds.
2.2.3. Procedure
Participants were recruited via flyers on the campus of the local university and via
posts on social network groups linked to the local university. In line with recommenda-
tions for psychophysiological experiments involving HRV measurements [10], partici-
pants were instructed to follow their usual sleep routine the night prior to the experiment,
not to consume alcohol or engage in strenuous physical activity in the previous 24 h, nor
drink or eat 2 h before taking part in the experiment. All participants gave written in-
formed consent before participation, and were informed that they could withdraw from
the study at any time without explanation and without any consequences. The partici-
pants attended the lab once in accordance with the within-subject design. The whole ses-
sion lasted 90 min (the protocol is described in Figure 2). After being welcomed to the lab,
they were asked to fill out an informed consent form and a demographic questionnaire
regarding variables potentially influencing HRV [10,51,52]. The ECG device was attached,
and participants watched a 15 min familiarization video to get acquainted with SPB. The
participants started with a 5 min rest period (baseline), where they were breathing spon-
taneously, with open eyes. After the 5 min rest period, they performed the six breathing
conditions in a randomized order, with a 5 min washout period between each respiratory
condition, similarly to Russell, Scott, Boggero and Carlson [70]. The washout period char-
acteristics were similar to those of the baseline. At the end of the experiment, the ECG
device was detached, and participants were thanked and debriefed.
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Figure 2. Experimental protocol.
2.3. Data Analysis
HRV variables were exported from the Kubios output. Data were checked for nor-
mality and outliers. Regarding outliers, 0.002% of the cases were found to be univariate
outliers (>2 SD, z-scores higher than 2.58; none were found being >3 SD, with z-scores
higher than 3.29). Running the analyses without them did not change the pattern of re-
sults; therefore, they were kept in the analysis. As the RMSSD data were non-normally
distributed, a log-transformation was applied, as is usually recommended for HRV re-
search [10].
As a manipulation check, we first checked whether the participants were breathing
at 6 cpm during the different conditions, and whether the breathing frequencies differed
among conditions, by conducting a repeated-measures ANOVA. Further, we conducted
a series of t-tests (two-tailed) to show whether the breathing conditions differed from
baseline, with log RMSSD as the dependent variable, with Bonferroni correction (0.05/6 =
0.008). We conducted a repeated-measures ANOVA, with inhalation/exhalation ratio (in-
halation = exhalation; inhalation > exhalation; inhalation < exhalation) and respiratory
pause (with/without) as independent variables, and log RMSSD as the dependent varia-
ble.
3. Results
Descriptive statistics are presented in Table 1 for all study variables. The first manip-
ulation check revealed that participants followed the 6 cpm breathing frequency, ranging
Sustainability 2021, 13, 7775 7 of 14
from 6.48 (SD = 0.20) to 6.55 (SD = 0.26). A repeated-measures ANOVA with the Green-
house–Geisser correction was conducted, and showed no significant effect of condition on
breathing frequency, with F (4.401, 277.232) = 0.696, p = 0.608, and partial η2 = 0.01.
The first analysis showed that log RMSSD was significantly higher in all the breath-
ing conditions than in the baseline, for inhalation > exhalation (respiratory pause) with t
(63) = 8.693, p < 0.001, Cohen’s d = 1.09; for inhalation < exhalation (respiratory pause) with
t (63) = 10.853, p < 0.001, Cohen’s d = 1.36; for inhalation = exhalation (respiratory pause)
with t (63) = 9.925, p < 0.001, Cohen’s d = 1.24; for inhalation > exhalation (no respiratory
pause) with t (63) = 8.393, p < 0.001, Cohen’s d = 1.05; for inhalation > exhalation (no res-
piratory pause) with t (63) = 9.428, p < 0.001, Cohen’s d = 1.05; and for inhalation > exhala-
tion (no respiratory pause) with t (63) = 8.944, p < 0.001, Cohen’s d = 1.12.
A repeated-measures ANOVA with the Greenhouse–Geisser correction was con-
ducted and showed a significant main effect of inhalation/exhalation ratio, with F (1.996,
125.753) = 8.778, p < 0.001, and partial η2 = 0.12; no main effect of respiratory pause, with F
(1, 63) = 2.495, p = 0.119, and partial η2 = 0.04; and no interaction effect between inhala-
tion/exhalation ratio and respiratory pause, with F (1.676, 105.567) = 0.141, p = 0.832, and
partial η2 = 0. Regarding the main effect of inhalation/exhalation ratio, further post-hoc t-
tests were conducted, applying Bonferroni’s correction with the alpha level adjusted to p
= 0.016 (0.05/3). Log RMSSD was found to be significantly higher in the condition with
inhalation < exhalation in comparison to inhalation > exhalation, with t (63) = 4.059, Co-
hen’s d = 0.51, and p < 0.001; and in comparison to inhalation = exhalation, with t (63) =
2.928, Cohen’s d = 0.37, and p = 0.012. No differences were found between the condition
inhalation > exhalation and inhalation = exhalation, with t (63) = 1.155, Cohen’s d = 0.14,
and p = 0.758. The results of this analysis are presented in Figure 3.
Sustainability 2021, 13, 7775 8 of 14
Table 1. Descriptive statistics.
Conditions HR SDNN RMSSD Log RMSSD LF HF LF/HF Breathing Frequency
M SD M SD M SD M M SD SD M SD M SD M SD
Baseline 67.18 7.97
92.22 37.37 57.14 33.17 1.70 4.09 3.91 0.22 3735.74 6586.00 1266.25 1450.35 11.45 2.03
I > E RP 68.23 6.68
138.11 54.94 85.29 38.95 1.89 17.52 14.53 0.20 14,031.93 10,768.08 1427.02 1473.48 6.55 0.26
I < E RP 68.23 6.53
133.89 45.04 90.27 41.38 1.91 14.30 12.38 0.20 14,587.38 11,754.30 1954.86 1918.53 6.49 0.30
I = E RP 68.37 6.57
132.06 42.74 86.82 39.35 1.89 16.52 12.95 0.21 14,352.57 11,242.16 1664.05 1702.17 6.51 0.22
I > E no RP 68.91 7.06
127.94 39.02 82.44 38.09 1.87 16.92 12.22 0.20 12,761.97 9874.21 1415.16 1621.83 6.52 0.23
I < E no RP 68.59 6.86
161.10 42.80 89.93 41.39 1.91 16.13 13.15 0.20 14,580.16 11,277.36 1602.47 1403.40 6.54 0.32
I = E no RP 68.78 6.30
128.27 38.72 82.94 34.54 1.88 15.91 11.81 0.18 13597.23 9134.12 1465.51 1506.67 6.48 0.20
Note: I: inhalation; E: exhalation; Rest: with post-inhalation and post-exhalation respiratory pauses; SDNN = standard deviation of all RR intervals; RMSSD: root mean square of the
successive differences; LF = low-frequency; HF = high-frequency; RP: respiratory pause.
Sustainability 2021, 13, 7775 9 of 14
Figure 3. Root mean square of successive differences (RMSSD) and inhalation/exhalation ratio.
Note: We display here the raw RMSSD values given that they are more informative for the reader,
as opposed to the log transformed values on which the analyses were based. The main effect of the
inhalation/exhalation ratio is shown here, meaning that the conditions with respiratory pauses and
without respiratory pauses are pooled for each ratio. I: inhalation; E: exhalation.
4. Discussion
The aim of this study was to investigate the influence of the inhalation/exhalation
ratio and of a respiratory pause on CVA during SPB. Regarding the inhalation/exhalation
ratio, findings showed that CVA is higher when the exhalation phase lasts longer than the
inhalation phase, confirming our hypothesis. Regarding the presence of a respiratory
pause, contrary to our hypothesis, there was no evidence for CVA to be influenced by the
presence of a respiratory pause after the inhalation or exhalation phase.
Findings concerning the inhalation/exhalation ratio are in line with previous research
[64,65], with the exception of Lin, Tai and Fan [68]; however, their study suffered from a
number of methodological issues, regarding sample size, design, and HRV variables re-
ported, as noted in the introduction section. Based on the characteristics of RSA [66,67],
heart rate increases with inhalation and decreases with exhalation. Inhalation is driven by
sympathetic nervous activity and inhibits parasympathetic nervous activity, while exha-
lation reactivates parasympathetic nervous activity. Consequently, we can assume that a
longer exhalation provokes a longer activation of the parasympathetic nervous system,
which is reflected in CVA. It is expected that at slow breathing frequencies, more acetyl-
choline is released during exhalation, due to its longer duration [75]. Due to the time con-
stants of acetylcholine hydrolysis around 1.5 s to 2.0 s [76,77], longer exhalation is sug-
gested to provoke a summation of sinoatrial responses, and hence maximally inhibit sino-
atrial node firing. This longer exhalation in comparison to inhalation was also found to
trigger more benefits, for example in terms of pain perception [78]. However, we have to
note that the inhalation/exhalation ratio range was reduced in this study (0.8–1.2) in com-
parison to other studies, such as 0.5–1 [58]; 0.4–2.3 [64], or 1–3.4 [65]. Our rationale was to
investigate whether slight variations in the ratio would already have an effect on CVA,
but larger ranges may reveal different physiological effects.
With regard to the respiratory pause during SPB, the findings did not show any
changes in CVA with the presence or absence of a respiratory pause. As we mentioned in
the introduction, Russell, Scott, Boggero and Carlson [70] concluded inaccurately that a
0
20
40
60
80
100
120
140
Baseline I > E I < E I = E
RMSSD
*
*
*
*
*
*
Sustainability 2021, 13, 7775 10 of 14
post-exhalation respiratory pause (4 s) increased CVA, drawing conclusions on HF-HRV
during SPB, which in this case does not reflect CVA [30]. Based on previous research
[70,71], we argued that a post-inhalation and post-exhalation respiratory pause may be
less demanding for the participant, by not requiring such a prolonged inhalation and ex-
halation, and that it would additionally trigger a bradycardia. Given that no changes were
observed in CVA, it may be that the respiratory pause we chose in this design (0.4 s) may
have been too short to elicit these effects. Other research used a respiratory pause of 4 s
but had an exhalation phase of 2 s [70], which we deemed too short given that the inhala-
tion phase lasted 4 s, and regarding previous research, a longer exhalation triggers higher
increases in CVA [64,65].
Our study had several strengths, such as a larger sample size than previous inhala-
tion/exhalation ratio-related research [64,65] and the investigation of RMSSD to index
CVA, as it is suggested to be relatively free of respiratory influences [31]. Limitations in-
clude first the sample chosen, comprising only athletes. This limits the generalization of
our findings, given that athletes have higher resting HRV than the general population
[79], and a ceiling effect may appear with SPB. Future research must investigate this re-
search question in different samples. Additionally, demographics related to the sport
practiced were collected. Second, the 5 min washout period between the conditions might
not have been sufficiently long to cancel the effects of previous breathing techniques.
Third, our equipment did not allow us to control precisely the exact duration of the inha-
lation, exhalation, and respiratory pauses, so it is not possible for us to evaluate how ac-
curately the participants performed the breathing techniques. Still, we were able to control
for respiratory frequency, to assure that our participants followed the 6 cpm rhythm, by
using the respiration algorithm of Kubios [72]. Additionally, the experimenter paid close
attention that the participants were following the breathing pacer. Finally, we also
checked the visual display of R-R values with Kubios, given that during slow-paced
breathing, oscillations matching the respiratory frequency can be observed [24]. Nonethe-
less, future research should use a respiratory belt to offer an online measurement of res-
piratory frequency. The fourth limitation is the design of the respiratory pause—future
research should endeavor to disentangle the effects of a post-inhalation and post-exhala-
tion respiratory pauses by investigating them separately, and should also consider respir-
atory pauses of different durations. We originally chose a 0.4 s respiratory pause duration
to enable our participants to avoid switching abruptly from inhalation to exhalation, and
from exhalation to inhalation. However, we acknowledge that this duration is much
shorter than those used in previous studies, such as 4 s in Russell, Scott, Boggero and
Carlson [70], and consequently, future research should investigate whether longer respir-
atory pauses trigger different physiological effects. Additionally, the inhalation/exhala-
tion ratio range was reduced (0.8–1.2), and future research should consider investigating
larger ranges [58,64,65].
Furthermore, the investigation of a respiratory pause should also include gas ex-
change measurement and consider, in particular, end-tidal CO2 values for enhanced un-
derstanding of its consequences on CVA, as well as consider its impact on tidal volume,
given the effects of respiratory pauses on RSA [67,70,71]. Additionally, other variables
related to HRV may be considered, such as the RSA, calculated as the difference between
the maximum and minimum cardiac interbeat interval per breath. The RSA has also been
suggested to index CVA [80–82] and has been used in previous research investigating a
similar research question [64]. Finally, future research should also consider investigating
the inhalation/exhalation ratio at different breathing frequencies [64,68,83] and take into
account the effects on other cardiovascular parameters, such as baroreflex sensitivity [84]
and blood pressure [85]. Authors should discuss the results and how they can be inter-
preted from the perspective of previous studies and of the working hypotheses. The find-
ings and their implications should be discussed in the broadest context possible. Future
research directions may also be highlighted.
Sustainability 2021, 13, 7775 11 of 14
5. Conclusions
In conclusion, the aim of this study was to investigate the role of two characteristics
of SPB on CVA, namely the inhalation/exhalation ratio and the presence of a respiratory
pause. Findings showed that adopting a respiratory pattern with a longer exhalation
phase triggered higher CVA in comparison to respiratory patterns with longer inhalation
than exhalation, or with equal duration of both phases. No changes in CVA were pro-
voked by a respiratory pause, but methodological limitations in our design guarantee fur-
ther scrutiny of this parameter in the future.
Manipulating the autonomic nervous system is often the target of sport psychological
techniques [86,87], with either activating or relaxing purposes, through methods such as
power posing [88] and hypnosis [13]. Within the autonomic nervous system, CVA is a
particularly desirable target for athletes, given its role in self-regulation [10–12,14–16]. In
contrast to other methods that exist to stimulate the vagus nerve, such as transcutaneous
vagus nerve stimulation [89–91], SPB without biofeedback does not require external de-
vices besides a respiratory pacer, and can be easily implemented as an acute [8,9,61,62] or
long-term intervention [63] in athletes. SPB with respiratory patterns involving a longer
exhalation phase compared to inhalation may therefore show potential as a performance
habit [92] in order to trigger the highest possible changes in CVA.
Author Contributions: Conceptualization, S.L. and F.D.; methodology, S.L. and F.D.; formal analy-
sis, S.L. and M.Y.; investigation, S.L. and M.Y.; resources, S.L.; data curation, S.L.; writing—original
draft preparation, S.L., M.I., N.Z., U.B., M.Y., C.S.-C., F.D.; writing—review and editing, S.L., M.I.,
N.Z., U.B., M.Y., C.S.-C., F.D.; visualization, M.I. and N.Z.; supervision, S.L. and F.D.; project ad-
ministration, S.L. and F.D. All authors have read and agreed to the published version of the manu-
script.
Funding: This research received no external funding.
Institutional Review Board Statement: The experimental protocol was approved by the Ethics
Committee of the German University Cologne (Project Identification Code 06/11/2014).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the
study.
Data Availability Statement: Data can be shared by the corresponding author upon reasonable re-
quest.
Conflicts of Interest: The authors declare no conflict of interest.
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