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Running is among the most popular sporting hobbies and often chosen specifically for intrinsic psychological benefits. However, up to 40% of runners may experience exercise-induced dyspnoea as a result of cascading physiological phenomena, possibly causing negative psychological states or barriers to participation. Breathing techniques such as slow, deep breathing have proven benefits at rest, but it is unclear if they can be used during exercise to address respiratory limitations or improve performance. While direct experimental evidence is limited, diverse findings from exercise physiology and sports science combined with anecdotal knowledge from Yoga, meditation, and breathwork suggest that many aspects of breathing could be improved via purposeful strategies. Hence, we sought to synthesize these disparate sources to create a new theoretical framework called “Breath Tools” proposing breathing strategies for use during running to improve tolerance, performance, and lower barriers to long-term enjoyment.
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Frontiers in Physiology | 1 March 2022 | Volume 13 | Article 813243
published: 17 March 2022
doi: 10.3389/fphys.2022.813243
Edited by:
Andrea Nicolò,
Foro Italico University of Rome, Italy
Reviewed by:
Annalisa Cogo,
Istituto Pio XII, Italy
Antonella LoMauro,
Politecnico di Milano, Italy
Eric Harbour
Specialty section:
This article was submitted to
Exercise Physiology,
a section of the journal
Frontiers in Physiology
Received: 11 November 2021
Accepted: 28 January 2022
Published: 17 March 2022
Harbour E, Stöggl T,
Schwameder H and
Finkenzeller T (2022) Breath Tools: A
Synthesis of Evidence-Based
Breathing Strategies to Enhance
Human Running.
Front. Physiol. 13:813243.
doi: 10.3389/fphys.2022.813243
Breath Tools: A Synthesis of
Evidence-Based Breathing Strategies
to Enhance Human Running
*, ThomasStöggl
1,2, HermannSchwameder
1 and ThomasFinkenzeller
1 Department of Sport and Exercise Science, University of Salzburg, Salzburg, Austria, 2 Red Bull Athlete Performance Center,
Salzburg, Austria
Running is among the most popular sporting hobbies and often chosen specically
for intrinsic psychological benets. However, up to 40% of runners may experience
exercise-induced dyspnoea as a result of cascading physiological phenomena,
possibly causing negative psychological states or barriers to participation. Breathing
techniques such as slow, deep breathing have proven benets at rest, but it is unclear
if they can beused during exercise to address respiratory limitations or improve
performance. While direct experimental evidence is limited, diverse ndings from
exercise physiology and sports science combined with anecdotal knowledge from
Yoga, meditation, and breathwork suggest that many aspects of breathing could
beimproved via purposeful strategies. Hence, wesought to synthesize these disparate
sources to create a new theoretical framework called “Breath Tools” proposing
breathing strategies for use during running to improve tolerance, performance, and
lower barriers to long-term enjoyment.
Keywords: breathing pattern, coupling, running, techniques, strategies, respiration, ventilation
Breathing is natural and automatic, sustaining life by the simple movement of air. Despite the
apparent simplicity of this process, the understanding of breathing has recently been advanced
extensively through investigations in medicine, sports science, and psychophysiology. e recent
SARS-COVID-19 global epidemic has reminded many of the signicance of breathing and
the consequences of respiratory distress.
Several recent studies have brought renewed attention to the anthropological roots of breathing
and its eect upon overall well-being. Yogic techniques have for millenia utilized breath awareness
and exercises to cultivate “prana” (meaning both “breath” and “life force” in Sanskrit), while
meditation, breathwork practices, and freediving also take advantage of breathing techniques
for calm, focus, and performance. Resonant frequency breathing performed in heart-rate
variability (HRV) biofeedback has signicant positive eects upon HRV itself, overall autonomic
nervous system regulation, and related emotional states such as anxiety and depression (Lehrer
et al., 2020). Performing these breathing techniques at rest has additive eects upon cognitive
function, decision-making, and concentration in sport (Jimenez Morgan and Molina Mora,
2017; De Couck et al., 2019). ese eects are extremely valuable in sports contexts where
both mental and physical performance aect positive psychological states such as perceived
Frontiers in Physiology | 2 March 2022 | Volume 13 | Article 813243
FIGURE1 | Exercise breathing pattern changes during increasing exercise intensity. Note the nonlinear increase in breathing rate and unequal partitioning of EILV
and EELV as intensity increases. TLC, total lung capacity; LOV, lung operating volume; VC, vital capacity; RV, residual volume; EILV, end-inspiratory lung volume;
EELV, end-expiratory lung volume; and VT, tidal volume.
Harbour et al. Breath Tools: Breathing for Runners
ecacy and enjoyment (Ogles et al., 1995). Although slow
breathing is demonstrably ecacious at rest, the utility of slow
breathing during exercise is understudied.
Recent reviews have explored the various mechanisms that
may cause breathing to limit physical performance during
exercise (Amann, 2012; Dempsey et al., 2020), but little work
has attempted to address these mechanisms or improve breathing
directly during exercise. Although running is both one of the
most popular (Statista, 2018) and well-studied physical activities,
very few studies have directly investigated the use of breathing
techniques during running as done during Yoga, meditation,
and cycling (Vickery, 2008; Saoji etal., 2019). Running deserves
special attention not only for its immense global popularity
but also because runners are driven by a complex mix of
psychological and emotional motives (Ogles etal., 1995; Pereira
etal., 2021). Since breathing can heavily aect the psychological
perception of exercise (Laviolette and Laveneziana, 2014),
improving breathing during running may inuence tolerance
or psychological state during activity. Considering the popularity
of running and the diverse benets of breathing strategies in
other contexts, wesought to synthesize the available evidence
to demonstrate how breathing could beused to ease respiratory
distress and improve running performance and
psychological states.
is narrative synthesis has three main goals:
1. Provide an updated overview of exercise breathing pattern,
and identify respiratory limitations to running
2. Dene and describe breathing strategies that provide physical
and mental benets for runners
3. Discuss practical applications and recommendations for
future studies of breathing techniques during running.
e onset of exercise stimulates rapid, characteristic changes
in ventilation (VE) over 20 times greater than that at rest
(hyperpnoea). e increase from an average 6 L/min up to
150 L/min occurs in response to various metabolic, homeostatic,
and peripheral stimuli (Figure 1). While not completely
understood, humans’ precise control of exercise hyperpnoea
is driven by multiple redundant control mechanisms, such as
biochemical feedback loops [especially by the partial pressure
Harbour et al. Breath Tools: Breathing for Runners
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of carbon dioxide (pCO2) and blood pH], central command
(neural feed-forward), and peripheral aerent feedback from
the working limbs (Forster et al., 2012). During steady-state
exercise, the healthy respiratory system precisely tunes VE to
match metabolic rate and maintain equal O2 and CO2 balance
at every level of the system (Ferretti et al., 2017). Above the
respiratory compensation point (RCP; a.k.a., second ventilatory
threshold), VE increases nonlinearly beyond the increase in
CO2 consumption (VCO2). Ventilatory change points are trait-
and state-dependent, continuously adjusting to factors like
anaerobic energy utilization, blood buering, and metabolic
acidosis. Indeed, the respiratory system is remarkable in
responding “just right” to exercise in most scenarios, eciently
managing VE proportional to CO2 production (VCO2). Exercise
VE increases linearly (r2 = 0.99) with inspiratory drive (VT/TI;
measured as mean inspiratory ow), reecting increased neural
drive to the inspiratory musculature (Naranjo et al., 2005).
is is achieved via patterns of breathing rate (BR), depth,
and coordinated muscle activity that maximize O2 perfusion
and minimize the metabolic work of breathing (WOB; Dempsey
etal., 2020). Nevertheless, there is considerable individual and
situational variance in breathing pattern (BP) response to VE
demands (Naranjo et al., 2005; Gravier et al., 2013).
Exercise Breathing Pattern
During exercise, it is thought that individuals intuitively select
the BP that minimizes the metabolic cost of VE (Mead, 1960;
Benchetrit, 2000; Welch etal., 2019). is is termed the “principle
of minimal eort.” e popular denition of BP includes an
inhale, an exhale, and a pause (Tab l e  1 ). It is primarily
determined by four principal variables: inspiratory ow prole
(rate of airow during inhale), inspiratory duration (TI),
expiratory ow prole, and expiratory duration (TE; Tipton
etal., 2017). ese variables determine the typical BP descriptors
of BR (60*TB1, where TB = TE + TI) and depth (tidal volume;
VT). Duty cycle (dc or breath ratio; measured as TI/TB) constrains
ow to determine BP timing, depth, and airway (nose vs.
mouth; Naranjo et al., 2005). ese components are regulated
by multiple overlapping control mechanisms, leading to a variety
of coordinated patterns to achieve respiratory homeostasis.
Unlike other physiological processes, BP can be consciously
altered, for example to befaster or slower. Although sometime
conscious, it is largely unconscious, with bidirectionality between
physiological and psychological mechanisms; this qualies BP
as a “psychophysiological” construct. While VE is ultimately
the product of BR and VT (Equation 1), these determinants
adjust dierently to various regulatory mechanisms, as do
related subcomponents of BP such as timing, coordination,
and coupling, discussed below (Tab l e  1).
Exercise BP is modulated by central and peripheral neural
mechanisms, chemoreex stimulation, attention, and emotions,
and biomechanical rhythms, among other factors. While VE
increase necessitates elevated breathing rate (BR, a.k.a. respiratory
frequency) and/or VT, their increases are independently regulated.
Recent work indicates that during exercise BR is more
“behavioral” and primarily driven by central command (activity
in motor and premotor areas of the brain) and muscle aerents
(Amann et al., 2010; Nicolo et al., 2016, 2017a, 2018). BR
and eort are closely correlated across many dierent exercise
intensities and experimental conditions (Nicolò et al., 2020b)
because perceived exertion is likely signaled by the magnitude
of central command outow (Marcora, 2009). At submaximal
intensities, BR is also aected by cognitive load, emotions,
environmental stress, and exercise rhythm (more on this below;
Homma and Masaoka, 2008; Grassmann et al., 2016; Tipton
et al., 2017). BR is acutely responsive, adjusting almost
immediately to abrupt changes in exercise intensity and stress,
such as anticipatory anxiety, pain, and cold exposure (Masaoka
and Homma, 2001; Tipton et al., 2017). At high relative
intensities above the RCP, continued increases in VE are
accomplished primarily via BR (tachypnoea; fast BR above
~80% peak BR); this point is termed the “tachypnoeic shi
(Sheel and Romer, 2011). e correlation between BR and
perceived eort is particularly strong at these intensities as
BR adjusts independent of absolute workload, metabolism, or
muscular activation (Nicolò et al., 2018; Cochrane-Snyman
et al., 2019). is may be due to increased levels of central
command activity compared with low or moderate-intensity
exercise (Nicolò et al., 2020a). At maximal exertion, peak BR
varies substantially between individuals from 35 to 70breaths
per minute (bpm; Blackie et al., 1991; Naranjo et al., 2005).
While BR responds quickly to “fast” inputs, evidence suggests
that during exercise VT adjusts slowly to optimally match
alveolvar VE to VCO2 (Nicolò et al., 2017a, 2018). In their
“unbalanced interdependence” model, Nicolo and Sacchetti
(2019) propose that VT is secondarily regulated on the basis
of BR to maintain biochemical homeostasis. is dierential
control likely extends across most exercise intensities (Nicolo
etal., 2020). Studies report diverse responses of VT to increasing
exercise intensity; in untrained exercisers, VT tends to increase
until either the rst or second ventilatory threshold, aer which
it either plateaus or declines (Gravier et al., 2013). While this
plateau generally coincides with the tachypnoeic shi, some
elite athletes appear to increase VT beyond the RCP and up
to total exhaustion (Lucía et al., 1999). Generally, VT peaks
around 50%–60% (1.9–2.7 L) of vital capacity (VC; total amount
of air exhaled aer maximal inspiration; Blackie et al., 1991),
although in some untrained persons as low as 35% (Gravier
et al., 2013) and elite athletes as high as 70% VC (Lucía
et al., 1999).
e tachypnoeic shi typical of the RCP cannot entirely
explain VT plateau during normal exercise conditions, since
the plateau occurs before the RCP in some individuals (Gravier
et al., 2013), and not at all in others (Lucía et al., 1999).
Lung mechanoreceptor feedback may explain some of these
disparities. VT limits are likely governed by the principle of
minimal eort, as vagally-mediated aerent feedback from
pulmonary stretch receptors regulates lung operating volumes
[LOV; relative to end-inspiratory (EILV) and end-expiratory
volume (EELV)] to minimize the WOB (Breuer, 1868; Hering,
1868; Clark and von Euler, 1972; Sheel and Romer, 2011).
Harbour et al. Breath Tools: Breathing for Runners
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ese mechanical limitations may interact with pCO2, which
is known to suppress pulmonary stretch receptor outow
(Schelegle and Green, 2001). Clark et al. (1980) observed this
phenomenon with progressive levels of hypercapnia during
incremental exercise increasing VT peak. Nevertheless, despite
higher relative VT peak, CO2 levels are similar or reduced in
elite athletes vs. untrained persons at equivalent absolute work
rates (Lucía etal., 1999). Hence, some of the mechanisms that
aect the VT plateau and tachypnoeic shi during exercise are
not yet entirely clear. Despite large inter-individual dierences
in relative VT peak, it is unclear if this is a xed characteristic
of BP; tness level and training appear to have no eect on
the VT plateau or the VE/VCO2 relationship (Salazar-Martinez
et al., 2016, 2018). It is believed that the attainment of VT
peak is the only circumstance at which VT substantially aects
BR (Sheel and Romer, 2011; Nicolò et al., 2018).
While the tachypnoeic shi is an adaptive, essential response
to maintain respiratory homeostasis at high relative exercise
intensities, it coincides with increased WOB, decreased ventilatory
eciency, and peripheral fatigue (Naranjo et al., 2005; Wa rd,
2007; Gravier et al., 2013). Although exercise below the RCP
triggers near-universal positive aect, there are homogenously
negative psychological changes above the RCP (Ekkekakis etal.,
2011). is may beexplained by the close correlation (r = 0.71)
between tachypnoea and dyspnoea during incremental exercise
(Tsukada etal., 2017). While the mechanisms causing dyspnoea
are complex and varied (Sheel et al., 2011), recent studies
suggest that the psychological “unpleasantness” dimension of
dypsnoea at its onset may contribute substantially to the near-
simultaneous presentation of tachypnoea (Izumizaki etal., 2011;
Tsukada et al., 2017).
Humans generally switch airway from the nose to mouth
as VE increases above 40 L/min (Saibene et al., 1978). Duty
cycle (dc; TI/TB) increases from resting values from about 40%
(slightly longer exhale than inhale) to 50% (equal inhale to
exhale) or greater at maximal intensity (Naranjo et al., 2005;
Ki and Williams, 2007; Salazar-Martinez etal., 2018). Shorter
TE vs. TI implies that mean expiratory ow rate must exceed
mean inspiratory ow rate (rate of airow during breath phase)
in order to maintain constant LOV.
Exercise-induced VE and drive increases trigger altered
ventilatory pump musculature activity and coordination. From
rest to 70% max workload, diaphragmatic pressure increases more
than twofold, accompanied by an increased velocity of shortening,
which contributes 70%–80% of the total inspiratory force (Wallden,
2017). As exercise intensity increases, active exhales (expiratory
muscle activation) lower the inspiratory WOB by reducing
end-expiratory lung volume, modulating lung compliance, and
storing elastic energy in the ventilatory pump musculature (Aliverti,
2016). e primary expiratory muscles are the internal obliques,
which may reach 50% maximum voluntary contraction at maximal
intensity (Ito etal., 2016). e intercostals, parasternals, scalenes,
and neck muscles contribute to ventilation at high intensities by
moderating EILV and airway caliber (e.g., dilation and
inammation). Altogether, the diaphragm and associated ventilatory
pump musculature are remarkably ecient [~3%–5% total O2
consumption (VO2)] and fatigue-resistant at submaximal intensities
(Welch et al., 2019; Sheel et al., 2020).
Locomotor-Respiratory Coupling
Humans are among a large proportion of animals that entrain
BR to movement. e synchronization of locomotion to breath
TABLE1 | List of breathing pattern components and common abbreviations.
Abbreviation Variable (units) Denition
BP Breathing pattern Differential trait and state-dependent control of breathing rhythm and mechanics
BR Breathing rate (bpm) Respiratory frequency; number of breaths taken per minute
Dc Duty cycle, breath ratio (%) Breath timing; relative percentage of inhale time to the complete breath cycle (TI/TB in %)
EELV End-expiratory lung volume Volume of the lungs at the end of an expiration
EID Exercise-induced dyspnoea Excessive perceived breathlessness during activity
EILV End-inspiratory lung volume Volume of the lungs at the end of an inspiration
FR Flow reversal Instant of breath switching; e.g., from inhale to exhale or exhale to inhale
LOV Lung operating volume (%) Mean diaphragm position at a given tidal volume (mean of EELV + EILV as % of TLC)
LRC Locomotor-respiratory coupling (steps:breath) Synchronization between ow reversal and movement; e.g., running footstrike
RV Reserve volume (l) Amount of air that remaining in airway and lungs after maximal expiration
TBBreath cycle time (s) Total breath time from inspiration to next inspiration (TI + TE)
TEExhale time (s) Exhale duration during one breath cycle
TIInhale time (s) Inhale duration during one breath cycle
TLC Total lung capacity (l) Total amount of air present in lungs after maximal inspiration
TLD Thoraco-lumbar depth (%) Ratio of thorax to abdominal expansion contributing to total tidal volume
VC Vital capacity (l) Total amount of air exhaled after maximal inspiration (TLC-RV)
VTTidal volume (l), depth Breathing depth; total amount of air inspired during one breath cycle
VDVentilatory dead space (l) Sum of airway volumes which do not contribute to gas exchange
VEMinute ventilation (L/min) Quantity of air breathed per minute
VO2Oxygen consumption (L/min) Oxygen consumption; difference between oxygen inspired and oxygen expired in a unit of time
WOB Work of breathing Metabolic energy demand of ventilation
- Thoraco-lumbar coordination (s) Breathing coordination; time lag between thoracic and abdominal ow reversal
- Ventilatory drive (l/s) Total output of ventilatory pump; mean inspiratory ow rate (VT/TI)
- Ventilatory efciency Ventilatory pump response to increasing demands, frequently measured as VE/VCO2 slope
Harbour et al. Breath Tools: Breathing for Runners
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is termed “locomotor-respiratory coupling” (LRC), and involves
a dual-synchronization not only of frequency [e.g., BR = step
rate (SR)] but also event phase (e.g., footstrike synchronized
with breath onset; O’Halloran et al., 2012). While most
quadrupedal mammals utilize a 1:1 phase-locked locomotion-
to-breath ratio while running due to mechanical constraints
of the thorax, humans’ upright gait permits BR adjustment
independent of locomotion (Bramble and Carrier, 1983).
Although humans lack this mechnical constraint on breathing,
they have been observed performing LRC during several rhythmic
activities, such as walking, running, cycling, rowing, cross-
country skiing, and even nger-tapping (Bechbache and Dun,
1977; Persegol etal., 1991; Fabre etal., 2007; Bjorklund etal.,
2015; Mathias et al., 2020). Swimming is a prime example of
phase-locked breathing, as swimmers inhale during specic
phases of the stroke when the face is not underwater.
Despite an apparent freedom from quadrupedal thorax
constraints on breathing, LRC in humans is likely aected by
various biomechanical phenomena specic to running. e
“visceral piston” (three-dimensional displacement of the
abdominal mass during locomotion) aects diaphragmatic
contraction via direct ligamentous connections (Daley et al.,
2013). Axial-appendicular dynamics have the potential to
positively or negatively aect VT depending on the phasic
relationship to inhale and exhale (Bramble, 1989). e eect
of footstrike timing and impact forces upon VT is termed
“step-driven ows,” and may aect VE up to 10%–12% (Daley
et al., 2013). is could be detrimental when the timing of
footstrike is out of phase (unsynchronized) with breath onset
(ow reversal; FR) but additive when in-phase (synchronized).
When the inhale is synchronized with peak visceral downward
velocity, it pulls on the diaphragm, increasing the velocity of
shortening. Daley et al. (2013) found that runners naturally
prefer LRC with phase synchronziation at additive (ow-
enhancing) phases, and that ventilatory transitions (change
from inspiration to expiration) were quicker in these conditions
of LRC. ey concluded that the visceral piston and rhythmic
arm movement substantially aect step-driven ows and LRC
has a physiologically signicant mechanical eect on breathing
dynamics. ese ndings suggest that LRC is a result of the
“minimal eort” hypothesis of breathing. If LRC reduces the
WOB, it may contribute to a delayed onset of ventilatory muscle
fatigue, especially at high exercise intensities, long exercise
durations, or in special populations predisposed to respiratory
distress (discussed below; Daley et al., 2013).
Locomotor-respiratory coupling is likely modulated by an
interaction of mechanical, neurological, and metabolic
interactions during running. Recent work indicates that LRC
in humans is probably neurophysiological in origin, as there
is a direct neurological link in humans between the respiratory
and locomotor central pattern generators in the spinal cord
(Le Gal et al., 2014; Del Negro et al., 2018). Group III and
IV aerent feedback from the working limbs appears to aect
LRC, since activities with higher-frequency limb movement
produce higher levels of entrainment (Bechbache and Dun,
1977; Caterini etal., 2016). However, close associations between
limb movement, BR, and pCO2 suggest that chemoreexive
feedback aects the strength of entrainment (Forster et al.,
2012). Cyclical, high-frequency activities such as running are
more likely to induce entrainment vs., for example, walking,
and LRC is most likely to occur at higher intensities near
VO2max (maximal oxygen uptake; Bechbache and Dun, 1977;
Bernasconi and Kohl, 1993). Notably, these studies reported
that increases in velocity of movement aected the strength
of LRC more than intensity increase via load or gradient.
ere appears to be an inuence of training history upon
entrainment, where task preference and experience are positively
associated with LRC onset and strength (Kohl et al., 1981;
Bramble and Carrier, 1983; Stickford et al., 2020). ese
relationships were independent of overall tness, so sport-
specic experience may coincide with LRC as a learned skill
(perhaps unconsciously). Finally, studies utilizing metronomes
to instruct movement appeared to quickly and strongly inuence
LRC (Bechbache and Dun, 1977; Bernasconi et al., 1995).
Entrainment is likely to occur spontaneously and consistently
in the presence of some or all of the above conditions.
Respiration as a Limiting Factor
e respiratory system in healthy individuals is considered to
begenerally well-adapted for the demands of exercise (Amann,
2012; Dempsey etal., 2020). Nevertheless, accumulating evidence
strongly suggests that the respiratory system is “underbuilt”
for the demands of intense exercise. At exercise around or
above 80%–85% VO2max, three primary mechanisms cause the
respiratory system to limit performance: exercise-induced arterial
oxyhemoglobin desaturation, excessive ventilatory muscle work,
and intrathoracic pressure eects on cardiac output (Amann,
2012). Specic scenarios (e.g., hypoxia and cold/dry climates)
expose respiratory system vulnerabilities at submaximal
intensities, and certain populations (e.g., elite athletes, females,
and elderly) are especially susceptible; these phenomena have
been recently detailed in extensive reviews (Dempsey et al.,
2020; Archiza etal., 2021). While the exact limiting mechanisms
dier (structural or functional), these situations and individuals
bring the respiratory system close to its physiological limits.
However, physiological limits do not fully explain the prevalence
of exercise-induced breathlessness (a.k.a dyspnoea; EID).
An estimated 20%–40% of otherwise healthy runners
experience EID even at low absolute exercise intensities
(Johansson et al., 2015; Smoliga et al., 2016; Ersson et al.,
2020). is could bebecause unt or deconditioned individuals
may approach high levels of exertion and experience limb
fatigue at low absolute workloads (Abu-Hasan et al., 2005). It
could also be related to mouth breathing, since mouth-only
breathing at submaximal intensities causes airway irritation,
and possibly subsequent exercise-induced laryngeal obstruction
(EILO; Mangla and Menon, 1981; Johansson etal., 2015). While
the majority of EID prevalence may beexplained by physiological
limitations and deconditioning, the other most likely cause is
dysfunctional breathing (Depiazzi and Everard, 2016). Distinct
from pathology, dysfunctional breathing (DB; suboptimal BP)
can cause otherwise healthy runners to experience premature
onset of fatigue and subsequent EID (Boulding et al., 2016).
Depiazzi and Everard (2016) submit that any BP deviating
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from slow, coordinated, diaphragmatic breathing has the potential
to be “dysfunctional.” Chronic stress (internal or external) or
negative emotional states could cause habitual DB during
exercise (Homma and Masaoka, 2008; Tipton et al., 2017).
Whether caused by physiological or psychological limits, fatigue
and EID could contribute to cessation of exercise, increased
rating of perceived exertion (RPE), or negative emotional states
(Figure 2; Bradley and Clion-Smith, 2009; Weinberger and
Abu-Hasan, 2009). Hence, here we aim to identify three
important shared phenomena that lead to respiration limiting
exercise performance, tolerance, and enjoyment: dynamic
hyperination, blood stealing, and hyperventilation.
FIGURE2 | The “respiratory limiting cycle” cascade of phenomena leading to respiration limiting exercise performance and enjoyment. Increasing exercise intensity
interacts with pre-existing individual constraints, causing an accumulation of respiratory phenomena that ultimately harm performance and cause dyspnoea. Dashed
arrows indicate mechanisms specic to high relative exercise intensities. Adapted with permission from BradCliff® and Bradley and Clifton-Smith (2009).
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Exercise BP may fail to provide the “just right” response
in the presence of ow limitation. During high intensity
exercise, large increases in ventilatory ow may cause narrowing
of the airway related to the Venturi eect and Bernoulli
principle, among other constraints. is is termed “exercise-
induced largyngeal obstruction,” and it is particularly common
in elite athletes who generate large VE at high intensities
(Smoliga et al., 2016). Up to 20% of elite athletes, females,
adolescents, and overweight individuals may experience this
during low-intensity activity (Smith et al., 2017; Dempsey
et al., 2020; Ersson et al., 2020). DB phenotypes including
upper-thoracic-dominant breathing and core muscle
hypertonicity (such as in low back pain compensation) are
also risk factors (Chaitow etal., 2014). Flow limitation could
lead to “breath stacking,” a negative consequence when
subsequent breaths have slightly larger inspiratory than
expiratory ow (Ward, 2007). Breath stacking causes EILV
and EELV to progressively increase, leading to dynamic
hyperination (Figure 3; Sheel et al., 2020). At these higher
LOV, the lungs are stier, less compliant, and require more
muscle work to expand (Sheel et al., 2020). Unfortunately,
dynamic hyperination places the diaphragm in a suboptimal
length for expanding the lungs and managing intrathoracic
pressures, further fatiguing the ventilatory musculature
(Aliverti, 2016).
Diaphragmatic breathing positively aects blood shiing
between the trunk and the extremities during exercise (Aliverti
etal., 2010). However, during heavy exercise above ~80% peak
work rate, increasing intra-thoracic pressure acts like a Valsalva
maneuver, decreasing stroke volume and cardiac output (Aliverti,
2016). Furthermore, at sustained high intensities the diaphragm
fatigues; it demands up to 14%–20% of cardiac output and
10%–16% of VO2 on top of concurrent accessory and expiratory
muscle fatigue (Welch et al., 2019). Ventilatory muscle fatigue
at high intensities triggers the metaboreex, which ensures
that the ventilatory pump maintains adequate perfusion by
shunting blood from the working muscles via sympathetically-
mediated vasocontriction. is competition for oxygen-rich
blood is termed “blood stealing”; a detailed review is available
elsewhere (Sheel et al., 2018). Although its negative
haemodynamic eects generally only occur above 85% VO2max,
its relationship to BP is unclear. Since the tachypnoeic shi
and dynamic ination associated with heavy exercise also elevate
the WOB, it is likely that they contribute to blood stealing
(Amann, 2012).
Exercise hyperpnoea is usually a “just right” respiratory
response to maintaining biochemical homeostasis with increasing
intensity (Dempsey et al., 2020). However, high BR may
bepsychologically disadvantageous, since the tachypnoeic shi
onset is closely associated with EID (Izumizaki et al., 2011;
Tsukada etal., 2017). Some runners may experience tachypnoea
and associated dyspnoea prematurely. Healthy adult females,
for instance, have hormonally-determined lung and airway
limitations that predispose them to higher average BR, lower
VT, and increased risk of EID (Itoh et al., 2007; Dempsey
et al., 2020). During running, VT is constrained more than
in other activities, and the tachypnoeic shi occurs relatively
earlier (Elliott and Grace, 2010; Marko, 2020). is limitation
is partially attributed to competing demands for postural and
ventilatory function upon the diaphragm as well as step-driven
ows (Chaitow et al., 2014; Stickford and Stickford, 2014).
Another factor could be surface inclination; Bernardi et al.
(2017) demonstrated that gradients above 20%–30% decrease
thoraco-lumbar coordination (r = 0.99) and subsequent ventilatory
eciency (r = 0.265). Subsequently, this harmed BP (lower
VT, increased BR), oxygen saturation, and performance. Since
these eects were independent of absolute altitude and fatigue,
they concluded that this was due to trunk inclination limiting
ribcage expansion.
If the tachypnoeic response is early, or inappropriately
dramatic, such as in hyperventilation DB, hypocapnia could
reduce peripheral muscle perfusion via the Bohr eect (Depiazzi
and Everard, 2016). is may accelerate blood stealing and
limb muscle fatigue. Additionally, lower pCO2 is associated
with earlier VT peak (Clark et al., 1980), which could lead to
accelerated increases in BR to increase VE. Hyperventilation
is accompanied by increased ow rates, which could lead to
airway narrowing and ow limitation (Dempsey et al., 2020).
FIGURE3 | Dynamic hyperination occurs when accumulated breath stacking progressively increases lung operating volume. When lung operating volume
approaches total lung capacity, lung stiffness, and suboptimal diaphragm position increase the work of breathing (WOB) and dyspnoea. TLC, total lung capacity;
LOV, lung operating volume; EILV, end-inspiratory lung volume; EELV, end-expiratory lung volume; and VT, tidal volume.
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Hyperventilation, hyperination, and blood stealing might
together form a negative feedback loop if unchecked. If this
cycle is not addressed, it could lead to EID, impaired performance,
or negative emotional aect (Bradley and Clion-Smith, 2009;
Chaitow et al., 2014). If these phenomena could be avoided,
we theorize that individuals could benet from enhanced
performance, reduced perception of fatigue, or prevention of
negative psychological states (Figure 2).
A related, but intensity-independent aspect of respiratory
limitations almost unique to running is exercise-related transient
abdominal pain (ETAP), also known as “side stitch.” First
mentioned by Pliny the Elder, there is still no consensus on
the exact etiology of this unpleasant phenomenon (Morton
and Callister, 2015). Unfortunately, this unpleasant, painful
experience aects up to 70% of runners per year, which is at
best frustrating and at worst a reason for exercise cessation.
Some experts believe that phrenic nerve irritation related to
repeated right footstrike and exhalation synchronization might
bethe cause (Coates and Kowalchik, 2013). Specically, irritation
of the parietal peritoneum is the most likely cause of ETAP,
especially during running and in the right lower quadrant
(Morton and Callister, 2015). It could be that LRC at even
ratios (such as 2:1 strides per breath), leading to ipsilateral
footstrike on expiration, is actually a risk factor for developing
side stitch in runners.
Breathing Patterns Can BeModied and
While breathing usually provides the “just right” response to
the physiological demands of exercise, respiratory limitations
can lead to negative performance or psychological outcomes.
If BP can be “improved” to prevent or delay the onset of
dyspnoea, or to increase ventilatory eciency, then it can
benet not only exercise performance but also the psychological
eects of exercise. Although acute BP modication and longer-
term breathing “retraining” have well-established benets for
human health (Zaccaro et al., 2018; Lehrer et al., 2020), this
eld has only recently gained attention in exercise science. A
recent review addressed this disparity by exploring the utility
of breath retraining for respiratory-limited athletes (Allado
et al., 2021); they found that several targeted techniques (e.g.,
Olin EILOBI breathing) can improve symptoms of ow limitation.
Several studies have utilized principles of breath retraining at
rest (e.g., slow diaphragmatic breathing) to demonstrate increased
exercise performance (Jimenez Morgan and Molina Mora, 2017;
Bahensky et al., 2021), but it is unclear if these can
beimplemented during exercise, and what psychological benets
result. Whether modifying BP is possible without compromising
the “minimal eort” homeostasis of the respiratory system
requires discussion and more direct study. In fact, one study
examining the eects of internal attentional focus upon breathing
reported no overall benet for movement economy, despite
positive eects upon VE, respiratory quotient, and heart rate
(Schucker etal., 2014). Nonetheless, it is known that breathing
techniques improve positive emotion (Zaccaro et al., 2018),
and that positive emotions can increase running economy
(Brick et al., 2018), so some accommodation might unlock
such performance benets. In fact, doing so during running
might bethe most specic application to maximize adaptations.
Despite a lack of direct evidence, theoretical and experimental
ndings from elds, such as cycling, respiratory medicine, and
Yoga indicate various limiting mechanisms that can beaddressed
with breathing techniques. We hypothesize that breathing
strategies employed during running could improve performance,
attenuate EID, or enhance psychological states.
Renewed attention to breathing techniques has inspired
substantial scientic scrutiny and interest among practioners,
but to our knowledge, no one has yet attempted to summarize
breathing strategies for exercise in an evidence-based, organized
manner. us, the following section is a description of techniques
and “breath tools” with potential benets to the runner. Each
tool is described with an acknowledgement of some historical
and anecdotal perspectives as well as a synthesis of its benets
for running biomechanics, biochemistry, and psychophysiology.
e “advanced” tools are slightly dierent, as they increase
respiratory stress to catalyze positive adaptations via training.
We summarize these strategies in roughly ascending order of
benet, complexity, and risk.
Humans have long known the value of slower BR. While
religious ceremonies, Yoga, and meditation rituals have explored
the practice for thousands of years, recent work has conrmed
the value of slow breathing for biochemical and
psychophysiological benets at rest (Russo etal., 2017; Zaccaro
et al., 2018). Although evidence suggests that sustained high
BR during activity could lead to respiratory limitations (see
“Respiration as a Limiting Factor”), reduced BR has been
understudied as a standalone breathing strategy during running.
Slow BR may reduce the work of accessory respiratory muscles
and subsequent WOB during exercise (Chaitow et al., 2014;
Welch et al., 2019). Perhaps, the most simple advantage is
improved gas exchange. Since BR is inversely proportional to
VT at a given VE (Equation 1), slower breathing implicity induces
greater depth of breathing (Figure 4). Since there is a xed
anatomic dead space (VD; average 150 ml of airway segments
that do not participate in gas exchange), increases in VE via
VT (instead of BR) benecially manipulate relative VD (VD:VT
ratio). For example, in conditions of isoventilation (Equation
1), a BR increase from 20 to 40 bpm at 10 L/min VE causes an
increase of 30% VD relative to VT, and a reduction of 300 ml
in alveolar ventilation (Table 2). In contrast, increasing VE to
20 L/min by only increasing VT (to 1.0 L) has the eect of
halved relative VD (15%) and a 21% increase in alveolar ventilation.
Simplistically, increasing VE via VT (instead of BR) allows for
more oxygen-rich breaths and greater alveolar ventilation.
Several studies have demonstrated remarkable plasticity of
VT in healthy individuals at submaximal intensities (Vickery,
2008; Bahensky etal., 2019; Cleary, 2019; Bahensky etal., 2020).
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ese ndings may stand in contrast to the “minimal eort”
hypothesis. We suspect that since an already-small percentage
of VC is used for normal VT during exercise, an incrementally
larger VT does not undermine the lung volume/pressure
relationship, and the BR/VT relationship may bemore “exible
than previously thought. is is likely not the case above the
RCP, where BR increases are driven substantially by central
command (Nicolò et al., 2018) and most exercisers reach VT
peak (Blackie et al., 1991). We suspect that this strategy is
most appropriate at low relative exercise intensities, and perhaps
not helpful or even harmful at high exercise intensities; future
studies should investigate this dierence.
Given the close association between BR and RPE (Nicolò
et al., 2018; Cochrane-Snyman etal., 2019), we speculate that
slower BR may decrease perceived feelings of eort at a given
exercise intensity. Hypothetically, slower BR may “trick” the
brain into feeling exercise to be easier. Hence, lower perceived
eort might be reected in improved performance or positive
psychological states (Noakes, 2012). Moreover, since BR reects
the physiological response to cognitive and environmental stress
at rest (Grassmann et al., 2016; Tipton et al., 2017), slowing
BR during exercise may improve mental performance and
calmness. As slow BR is known to positively impact autonomic
nervous system balance and vagal tone at rest (Lehrer et al.,
2020), it is possible that there is a similarly “optimal” BR
during running that enhances the pleasant feelings of exercise
(Homma and Masaoka, 2008). One study that manipulated
BR during cycling found lower RPE, suppressed sympathetic
and increased parasympathetic activity when breathing at very
low BR of 10 bpm vs. unconstrained BR (Matsumoto et al.,
2011). More studies are needed to evaluate such ndings
in running.
Another potential application of the “rate” strategy is to
regulate exercise intensity. As BR is closely correlated with
physical eort, wespeculate that constant BR may limit physical
output. Since mechanical limitations partially determine the
comfortable limit of VT, constant “paced” BR therefore has a
theoretical upper limit of VE. Paced BR therefore deterministically
FIGURE4 | Respiratory inductance plethysmography data from our lab showing normal breathing (dashed line) vs. “rate” breathing strategy (solid line). Note longer
breath duration (horizontal) and related larger tidal volume (vertical) for each breath cycle.
TABLE2 | Effect of breathing pattern on alveolar ventilation and dead space in three scenarios. Adapted from Braun (1990).
Breathing pattern Minute ventilation
(VE, L/min)
Breathing rate (BR,
bpm) Tidal volume (VT, L) Dead space volume
(VD, ml)
Alveolar ventilation
rate (L/min) Relative VD (VD/VT, %)
Normal 10 20 0.50 150 7.0 30%
Slow, deep 10 10 1.0 150 8.5 15%
Fast, shallow 10 40 0.25 150 4.0 60%
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limits overexertion since VE cannot easily increase. For example,
given a typical VC of 4 L and assumed VT peak of 60% VC
(Naranjo etal., 2005), running with paced BR at 20 bpm would
limit comfortable VT to 2.4 L and VE to 48 L/m. If the runner
speeds up, increasing metabolic demands but not VE, there
might bea dissociation of the VCO2/VE relationship. Increased
pCO2 could trigger dyspnoea and air hunger (Sheel et al.,
2011); this is a strong cue to “slow down.” In this way, breathing
could beused to deliberately impose a limit on exercise intensity,
potentially aiding in sustainable pacing of exercise. is could
be especially helpful for unt beginner runners to prevent
overexertion. Considering the complex “minimal eort”
regulation of BP, paced BR during exercise could cause adverse
eects such as respiratory discomfort or EID; this requires
more study. Nonetheless, elite athletes express lower levels of
BP variability during exercise vs. healthy sedentary individuals
(Castro et al., 2017), suggesting that decreased BR variability
could beadvantageous. Experimental investigations could address
this topic by including subjective assessment of dyspnoea
intensity and discomfort on top of objective measurement of
physiological performance (Lewthwaite and Jensen, 2021).
Practical application of paced breathing during running
invites scientic exploration. In biofeedback studies, visual
feedback has been used to successfully x BR at specic rates
(Davis et al., 1999; Blum et al., 2019). Auditive feedback may
be especially appropriate for eld running, since over 60% of
runners listen to audio, on average, during their run (Nolan,
2016). We have demonstrated in our lab that runners can
easily follow continuous and periodic auditive BR instruction
during running (van Rheden etal., 2021). e specic parameters
for the “rate” strategy need further denition: there is likely
not an absolute “best” BR for all runners, but rather a relative
decrease that optimizes the benets outlined above. Nicolò
et al. (2017b) suggest monitoring BR as a percentage of an
individual’s peak BR (BR/BRPeak), and this could beused similarly
for the “Rate” strategy. A decrease of 10%–20% is perhaps
prudent as used in previous studies with breathing retraining
(Bahensky et al., 2021).
Given the interdependence of BR and VT, depth of breathing
is largely dependent upon the former. However, equivalent VT
can be achieved with more or less diaphragmatic engagement,
and at variable LOV. Pranayama Yoga, Zen, and Transcedental
meditation practices include conscious diaphragmatic breathing
exercises shown to beeective for improving exercise capacity,
stress reduction, and reducing symptoms of respiratory disease
(Hamasaki, 2020). us, breathing depth ought to beconsidered
distinctly modiable.
Although VT must adjust proportionally with BR to match
VE demands, it can perhaps be altered independently. Elite
athletes have demonstrated ventilatory compensation strategies
favoring VT increases relatively greater than non-elites, especially
in acute hypoxia (Lucía etal., 2001; Tipton etal., 2017). is
may be an adaptive mechanism to aid in the elevated VE
demands of high performance, as lung structure is remarkably
intractable even with training (Dempsey et al., 2020). Not
only is increasing VE via VT preferable and possible (section
“rate”), but this “depth” should come from the abdominal
ribcage (Figure 5).
Upper-thoracic dominant breathing is associated with
increased ow limitation, WOB, hyperventilation, and postural
instability (Nelson, 2012; Chaitow et al., 2014; Depiazzi and
Everard, 2016; Wallden, 2017). Conversely, diaphragmatic
breathing is correlated with various positive health benets,
including reduced resting heart rate, post-exercise oxidative
stress, increased postural control, and baroreex sensitivity
(Hazlett-Stevens and Craske, 2009; Martarelli etal., 2011; Nelson,
2012; Hamasaki, 2020). e eect of diaphragmatic breathing
during exercise on these parameters is unknown. We suspect
that this is due to methodological diculties in measuring
diaphragmatic contribution to breathing noninvasively.
Nonetheless, diaphragmatic deep breathing might help to
attenuate respiratory limitations in vulnerable individuals and
situations. We suspect that this could result in reduced risk
for EID and negative psychophysiological consequences.
Greater depth of breathing can beachieved through exercises
to improve diaphragmatic function, and thoraco-lumbar
coordination. Several publications have provided summaries
of such exercises, which include paced breathing, biofeedback,
and manual therapy (Hazlett-Stevens and Craske, 2009; Saoji
et al., 2019; Hamasaki, 2020). On the other hand, examples
of manipulating breathing depth during exercise are limited.
One simple method is implementing the “rate” strategy to
force VT to increase in response to slow BR (section “rate”).
However, this does not necessarily cue diaphragmatic breathing
as we have described. Some products such as the Buteyko
belt® (Buteyko Clinic International, Galway, Ireland) may bring
awareness to the diagphragm and abdominal ribcage via external
tactile stimulation, but it is unclear if these are suitable during
exercise. Sensors such as the Hexoskin garments (Carre
Technologies, Canada) are capable of measuring abdominal
ribcage expansion, but they experience signicant signal
contamination as a result of so tissue artifact when used
during running (Harbour et al., 2021). Visual and auditive
methods from the eld of biofeedback could be particularly
suitable for cueing this strategy during running.
e nose is the primary point of entry and exit of the airway
during healthy breathing at rest. It is functionally equipped
to humidify, warm, and lter inspired air (Walker et al., 2016).
It also increases nitric oxide production in the airway, and
has positive eects upon pulmonary perfusion (Sanchez Crespo
etal., 2010), head posture (Sabatucci etal., 2015), and cognitive
function (Zelano etal., 2016). Mouth breathing is more common
during exercise and for those with nasal breathing diculties
(Niinimaa, 1983). However, unlike nose breathing, habitual
mouth breathing is linked with DB and numerous pathologies,
including upper respiratory tract infections, rhinitis, and asthma
(Chaitow etal., 2014; Walker etal., 2016). Despite these concrete
advantages at rest, nasal breathing during exercise has seen
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mixed attention and enthusiam as a standalone breathing
strategy. Nose breathing is encouraged during Pranayama Yoga
exercises, and also popularized by authors/bloggers Brian
McKenzie (Sh//.®) and Patrick McKeown (Oxygen Advantage®)
as a psychophysiological state modulator. Humans usually switch
to mouth breathing at VE = 40 L/min, leading to the assumption
that mouth breathing is a requirement during exercise (Saibene
etal., 1978). Despite this assumption, studies have demonstrated
that humans have surprising exibility in airway choice during
exercise (Morton et al., 1995; Dallam and Kies, 2020).
omas et al. (2009) reported that subjects were able to
maintain nasal breathing up to 85% VO2max during exercise
when instructed with a familiarization but no other
accommodation. With an adaptation period, nasal breathing
during exercise may cause reduced BR, reduced hypocapnia,
and increased nitric oxide production (Dallam et al., 2018).
Nitric oxide production is itself benecial as a vasodilator and
bronchodilator (Sanchez Crespo et al., 2010; ornadtsson
et al., 2017), perhaps reducing the risk for ow limitation.
While nasal breathing utilizes a smaller airway, which is a
FIGURE5 | Schematic showing the difference between upper-thoracic dominant breathing (A,C) vs. “deep” diaphragmatic breathing (B,D). (A) Upper-thoracic
breathing elevates and expands the upper ribcage, visible in (C) respiratory inductance plethysmography measurements from our lab showing increased amplitude
in thoracic vs. abdominal bands. (B) Deep breathing attens the diaphragm against the inferior abdominal viscera, expanding the abdominal ribcage via pump- and
bucket-handle mechanisms. Adapted from Isometric angle of diaphragm and ribcage by Chest Heart & Stroke Scotland and Stuart Brett, The University of
Edinburgh 2018 CC BY-NC-SA; arrows added for emphasis.
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limitation at higher exercise intensities, it appears to increase
diaphragmatic function (Trevisan et al., 2015), which could
be a long-term advantage (see section “Deep”). Some studies
have reported favorable performance eects, such as decreased
respiratory exchange ratio, VO2, and increased running economy
and time to exhaustion (Morton et al., 1995; Recinto et al.,
2017). Weestimate that these eects might benecally decrease
RPE or dyspnoeic sensations, although direct study is required.
Conversely, nasal breathing during heavy exercise leads to
higher exercise HR and no dierence in power output or
anaerobic performance, perhaps as a result of greater inspiratory
muscle load (Recinto et al., 2017).
The filtration and humidification functions of the nose
may help at any exercise intensity to prevent EID and
pathogen or particulate inhalation (Mangla and Menon, 1981;
Aydın etal., 2014). The risk for Rhinitis and upper respiratory
tract infections is substantially reduced with nasal breathing
during exercise (Walker et al., 2016). Airway choice also
impacts head posture and glossopharyngeal mechanics (Okuro
et al., 2011; Sabatucci et al., 2015), suggesting that nasal
breathing could be a long-term strategy to prevent EILO.
Although there is limited evidence on the psychophysiological
correlates of nasal breathing during exercise, studies suggest
that nasal breathing at rest leads to improved cognitive
function, emotional appraisal, memory, and lower perception
of fear (Zelano et al., 2016). Hence, we suggest that nasal
breathing is beneficial for its positive effects on performance,
airway quality, and cognitive function during
low-intensity exercise.
Implementing nasal breathing during exercise requires
awareness and accommodation. Anecdotal evidence suggests
that 10–12 weeks are required for meaningful changes in
nasal breathing comfort and relief of airway restriction to
occur, while intervention studies have examined learning
periods of up to 6 months (Dallam et al., 2018). Conversely,
several reports indicate that nasally-restricted breathing causes
nasal airway resistance to drop in days and even minutes
as a result of nitric oxide production and shifting nasal
mucosa (Shturman-Ellstein etal., 1978; McCaffrey and Kern,
1979; Mertz et al., 1984). Rather, nasal breathing is self-
manifesting: performing it encourages subsequent ease. In
fact, nasal airway resistance falls during exercise, regardless
of the airway used (Olson and Strohl, 1987). This is why
the “nose” strategy is indeed an accessible choice for most
runners; barriers to uptake are most likely related to
habituation alone. Nasal breathing requires some adaptation,
but the ideal protocols and individual differences need more
investigation. An understudied aspect is whether diaphragm
fatigue is improved or harmed with nose breathing, given
its active resistance as a smaller airway. Finally, werecommend
exercising caution when performing studies on nasal breathing
in an exercise physiology setting specifically related to
spiroergometry masks and their adverse effects on BP (Gilbert
etal., 1972; Laveneziana etal., 2019). Future studies should
explore nasal breathing in natural running settings with
minimally invasive equipment, and also the details of nasal
breathing accommodation.
Active Exhale
e benets of long, slow exhales have been long promoted
in Yoga and meditation elds to enhance health and well-being
(Saoji et al., 2019). Some running coaches and experts have
also touted this strategy, suggesting it enhances breathing depth
and aerobic endurance (Jackson, 2002; Coates and Kowalchik,
2013). Although there are few studies directly examining
manipulation of the exhale phase during exercise, combined
evidence from other domains supports several advantages of
“active” exhales.
Longer exhales may exploit respiratory sinus arrythmia to
improve HRV and subjective well-being at rest (Matsumoto
etal., 2008; Van Diest etal., 2014). While inspiration enhances
sympathetic and suppresses parasympathetic activation, during
expiration, the opposite occurs, triggering vagal aerents (Seals
et al., 1993; Hayano etal., 1994). is phenomenon has been
observed during incremental exercise (Blain etal., 2005). Indeed,
breathing may bethe main mechanism responsible for short-
term HR uctuations, especially at higher intensities (Bernardi
et al., 1990; Prigent et al., 2021). Matsumoto et al. (2011)
tested this eect during exercise: longer exhales (33 vs. 50%
dc) caused improved HRV, ventilatory eciency (VE/VCO2
19.1 ± 2.9 vs. 22.1 ± 4.4), and VO2 during incremental cycling.
ese profound results have yet to bereplicated in the literature.
A separate but related approach to exhale manipulation is
conscious recruitment of the expiratory musculature. Although
expiration becomes active by default during exercise, additional
contraction of the abdominals may confer additional benets.
In other words, stronger, forced exhales in combination with
a lower duty cycle make the “active exhale.” Active exhales
cause a fuller upward excursion of the diaphragm, which
generates passive elastic forces, lowers diaphragmatic work, and
assists in postural stabilization (Wuthrich et al., 2014; Wallden,
2017). Greater abdominal recruitment might help to partition
the WOB and delay the onset of ventilatory muscle fatigue
at high intensities, but this aspect is apparently unstudied.
While active exhales are automatic in most situations, the
respiratory limitations outlined above can cause this pattern
to become dysregulated. Hence, in the presence of these
limitations, it is possible that purposeful active exhales could
assist in maintaining optimal LOV (Figure 6). Lower duty
cycle limits inspiratory ow, and allows more time for expiratory
ow; this may reduce expiratory ow limitation. In addition,
the assymetric ow prole accompanying long exhales implies
that peak negative inspiratory pressure exceeds negative expiratory
pressure. is could have net positive eects on intrathoracic
pressure as a limiter to cardiac output during high-intensity
exercise (Amann, 2012). No studies have explored this aspect
yet in the literature.
e mountaineering community has long-touted a version
of active exhales (“rescue breath” or “pressure breath”) for
managing respiratory distress at altitude (Expeditions, 2014).
Ian Jackson’s Breathplay technique highlights this strategy,
claiming a number of benets that were examined by Woj t a
et al. (1987) aer a 3-day training period. e study found
a delayed onset of fatigue, lower HR (1.9%), and longer time
to exhaustion (7.2%) during an incremental cycling test to
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exhaustion. In addition, they reported a substantial delay in
the onset of peak CO2 (40%), presentation of RQ = 1 (60 s
later), and anaerobic threshold (120 s). Replication studies are
needed to conrm these distinct results. Positive expiratory
pressure may contribute to these ergogenic eects; Rupp etal.
(2019) reported that forced exhales benet peripheral and
central circulation and oxygenation, especially in hypoxia, that
is probably caused by increased alveolar pressure and resultant
hyperperfusion. When used intermittently, this may allow
marginal increases in pCO2, which enhance the Bohr Eect.
is may be especially relevant for individuals and situations
predisposed to hypocapnia, such as intense exercise and
hyperventilation DB.
A valuable addition to the active exhale is phonation. For
example, the yogic technique Bhramari Pranayama (humming
during the exhale) may be eective in cueing active exhales
since it not only adds additional airway resistance on the
out-breath, but it profoundly increases free nitric oxide (up
to 15-fold at rest; Weitzberg and Lundberg, 2002; Pramanik
etal., 2009). is may enable nasal breathing at higher intensities,
or ease ow limitation. is unconventional aspect has the
additional benet of amusement for the runner (or those around
them). Future work should clarify whether this technique can
reduce respiratory limitations or if it might adversely irritate
laryngeal structures, especially whether there is an ideal frequency
to perform it.
Performing active exhales during running probably requires
attention, instruction, and habituation. Visual modes of
biofeedback may be especially effective if displaying real-
time LOV. A valuable cue may be to “squeeze all the air
out” (Jackson, 2002) or fully “empty” the lungs before the
inhale (Johnston et al., 2018). Other techniques such as
pursed lips breathing could be combined to exploit the
ergogenic effects of positive expiratory pressure, which is
particularly relevant when exercising at high intensity or
altitude (Rupp etal., 2019). A major limitation to studying
or performing the active exhale is its deviation from the
“minimal effort” BP; duty cycle is remarkably constant in
most healthy exercisers (Naranjo et al., 2005), and it may
require substantial cognitive focus to maintain this technique
for long periods of time.
Locomotor-respiratory coupling, once penned “rhythmic
breathing” by medical doctor Irwin Hance in 1919, has been
the object of much scientic investigation for at least 50 years,
and has wide cultural inuence (Hey etal., 1966; Coates and
Kowalchik, 2013). While bipedalism gives humans exibility
to perform it or not during locomotion, LRC has been observed
at many ratios during running (commonly reported 4:1, 6:1,
8:1, 5:1, and 3:1 steps per breath; Bramble and Lieberman,
2004; Stickford and Stickford, 2014).
FIGURE6 | Respiratory inductance plethysmography (RIP) data from our lab showing normal breathing (dashed line) vs. “active exhale” breathing strategy (solid
line). Note that raw RIP data depict inductance, where signal increases (upward slope) correspond to the exhale phase. Observe the identical breath cycle time, but
shorter relative inhale and longer exhale (smaller breath ratio) as well as lower average lung operating volume throughout the breath cycle (higher signal units
indicating decreased sensor stretch).
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FIGURE7 | Respiratory inductance plethysmography data from our lab showing locomotor-respiratory coupling (LRC). (A) Phase synchrogram and LRC ratio
plotted during 8 min of running at an instructed LRC ratio 3:4 (steps per inhale:steps per exhale). Note the quantity of steps synchronized with inspiration vs.
expiration. All relative phase shifted 90° for visibility. (B) Subsection of 10 s of raw RIP and hip-mounted accelerometer data while running at 3:4 LRC. Dotted lines
added to emphasize step & ow reversal synchronization.
e passive assistance of step-driven ows may assist VE
increases without elevating the WOB (Daley etal., 2013; Stickford
and Stickford, 2014). Several studies report that LRC decreases
VO2, increases running economy, and reduces dyspnoea (Garlando
et al., 1985; Bernasconi et al., 1995; Takano and Deguchi, 1997;
Homann etal., 2012). Some have speculated that active exhales
may further enhance the exhale phase in combination with LRC,
as concentric contraction of the abdominal and pelvic oor
musculature may optimize visceral compressive forces when
synchronized with step-driven ows (Daley etal., 2013; Wallden,
2017). e “free” work granted by step-driven ows may realize
some of the benets of other strategies, since greater VT enables
slower BR and reduced ow velocity at a given VE. If this eases
ow limitation or EID, then it can also lead to associated positive
psychological outcomes.
As noted in section “respiration as a limiting factor,” LRC
at even ratios (e.g., 4:1 or 6:1) could bea risk factor for side
stitch. However, it might also be used to prevent it. Some
experts recommend exhalation on alternate steps specically
to avoid side stitch (Jackson, 2002; Coates and Kowalchik,
2013). Using an odd-numbered LRC ratio (e.g., 5:1 or 7:1;
Figure 7) causes exhales to occur on opposite footstrikes,
potentially limiting parietal peritoneum irritation. is might
avoid such unpleasant pain and discomfort during running.
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Locomotor-respiratory coupling may be energetically
advantageous not only for its synergistic respiratory advantages,
but also as a mediator of BR and running pace. As described
in the “rate” strategy, given the close correlation between BR
and RPE, and also the known stability SR during running
(Van Oeveren et al., 2019), LRC may be an eective way to
stabilize running pace. LRC ratios of 4:1 and 5:1 for a runner
with a preferred SR around 180 (right and le, steps per
minute) would thus correlate to BR of 45 and 36, respectively.
Dierent LRC ratios could thus be utilized as a “gears” system
corresponding to dierent perceptual and physiological levels
of eort.
Since a primary mechanism of LRC during running appears
to be neurological, purposeful performance of LRC may have
additive psychological benets. e immersive
psychophysiological experience of ow is suggested to occur
with the presence of three conditions: an activity with clear
goals and progress, immediate feedback, and balance between
perceived challenges and competence (Snyder et al., 2020).
Entrainment, such as that of breath to step during LRC, is
likely to enhance ow experience in runners (Bood et al.,
2013; Nijs et al., 2020). Indeed, LRC during running satises
the primary conditions for inducing a trance state: physical
exertion, rhythm, and concentration (Damm etal., 2020). Such
rhythmicity is comforting, sedating, and hypnotic, and rhythmic
stability may lower stress on the nervous system by reducing
cognitive fatigue (Ross et al., 2013). Future studies should
explore LRC and ow phenomenology especially as it pertains
to runners.
e practical application of LRC is not trivial. It is possible
that the additional concentration required to execute LRC
during running negates any physiological benet. Nevertheless,
past studies that found no benet for LRC examined it in
untrained individuals or during unfamiliar tasks (Yonge, 1983;
Maclennan et al., 1994). Perhaps some learning and
accommodation is required to realize ergogenic advantages.
Although many elite runners perform it unconsciously
(Bonsignore et al., 1998; McDermott et al., 2003), limited
evidence is available regarding learning this as a deliberate
breathing strategy, especially in sub-elite runners. A notable
exception instructed LRC via haptic feedback (vibration) timed
with footstrikes on either the exhale or inhale (Valsted et al.,
2017). ey found comparable success when the feedback was
periodic (1 min of instruction followed by 2 min or no instruction)
or self-selected vs. continuous. Nonetheless, some runners found
LRC dicult or the instruction annoying. Attention is needed
in this eld to develop intelligent systems for LRC instruction
and feedback, with auditive modes being understudied. Runners
should probably synchronize breath to step, instead of step to
breath, since deviating from individually preferred SR might
beenergetically disadvantageous or increase injury risk (Adams
et al., 2018; De Ruiter et al., 2019). Smart feedback systems
should consider adapting breath instruction to the current SR
to avoid such eects and to maximize entrainment (Bood etal.,
2013; Van Dyck et al., 2015). Practically, runners should use
an odd ratio (such as 5:1 or 7:1) to capture the benets of
longer exhales and side stitch prevention.
Advanced Breath Tools
ese breathing strategies are labeled “advanced” because they
require either special equipment or are especially dicult to
perform. ey also carry some risk, which should beconsidered
in context vs. the potential benets and population of interest.
Nevertheless, they are included here because they have
demonstrated ergogenic benets and are suitable for application
during running.
Respiratory muscle training (RMT) has been extensively studied
as an alternative strategy to improve breathing during exercise.
e use of resistive breathing devices such as the Training
Mask® and POWERbreathe® stress the respiratory system,
resulting in positive changes in ventilatory eciency, muscle
recruitment patterns, oxygen delivery, and reduced WOB and
dyspnoea (Karsten etal., 2018; Shei, 2018; Lorca-Santiago etal.,
2020). Readers are directed to these three recent reviews for
a detailed explanation of these mechanisms. While the majority
of studies leverage these methods at rest, several studies have
examined the eects of concurrent resistive breathing during
exercise (Hellyer et al., 2015; Porcari et al., 2016; Barbieri
etal., 2020). Experts in this eld have suggested that concurrent
RMT is underexplored and may, in fact, bethe most eective
means of transferring the benets of RMT to sport performance
(Karsten et al., 2019). Unfortunately, high-quality studies
examining these scenarios are lacking.
e Olin EILOBI techniques were developed by J. Tod Olin
and colleagues as a variant of inspiratory resistance breathing
specically to address EILO (Johnston etal., 2018). ey were
conceived to be used specically during exercise when EILO
occurs to maximize specicity. Although primarily developed
for clinical applications, the self-resisted nature of this technique
may qualify as RMT and besuitable for other settings. Johnston
et al. (2018) report alleviation of EILO symptoms in 66% of
their participants, and we suspect that this could be valuable
for other runners to prevent ow limitation. While this technique
is complex to learn, some components (emptying, abdominal
ribcage focus) may behelpful for improving breathing mechanics.
We found exactly one study that specically tested RMT
methods during running. Granados etal. (2016) reported that
wearing the Training Mask® (Training Mask LLC; Cadillac,
MI, United States) during running at 60% VO2max induced
hypoxaemia without substantial increases in RPE or anxiety.
ey concluded that incorporation of RMT methods part-time
in a training routine is a convenient, time-ecient approach
to benet from RMT. Nevertheless, more studies are needed
to explore long-term use of such methods. If the muscle
recruitment pattern triggered by resisted breathing is not deep
& diaphragmatic, it may not accumulate adequate stimulus to
induce diaphragmatic hypertrophy, or it may habituate DB
(Karsten et al., 2018, 2019). While many respiratory-limited
individuals could benet substantially from RMT’s subsequent
reduction in EID (Bernardi et al., 2015), females appear less
receptive to its benets (Schaer et al., 2019). Finally, while it
could be dangerous to induce additional respiratory distress
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FIGURE8 | Respiratory inductance plethysmography data from our lab showing normal breathing with one approximate 10 s end-expiratory breath hold. Note the
very long double exhale and brief diaphragm twitch.
during running, the potential ergogenic and psychological
benets suggest that careful protocol development is a key to
making this a viable breathing “strategy” among runners.
Breath holding (BH, also known as hypoventilation, CO2
tolerance, or air hunger training) garnered recent popularity
due to large performance benets reported in swimming and
techniques popularized by freediving (Holfelder and Becker,
2019). e various eects of hypoxia and hypercapnia have
been rigorously studied (Millet etal., 2016; Girard etal., 2020),
and BH is an accessible method for runners to replicate such
benets. In short, BH is a strong metabolic stressor similar
to hypoxic training that causes accelerated muscle deoxygenation,
hypercapnia, and increased muscle activity during exercise
(Kume etal., 2016; Toubekis etal., 2017). BH protocols lasting
3–5 weeks reported performance gains of 3%–4% related to
two acute mechanisms: increased stroke volume (up to 30%)
and haemoglobin concentration (up to 10%; Woorons et al.,
2016; Lapointe et al., 2020; Woorons et al., 2020). ese
ergogenic benets are likely due to increased le ventricular
stroke volume (Woorons et al., 2021b) and post-BH spleen
contraction (Inoue et al., 2013). Only one study was found
that examined the acute eects of BH during running (Woorons
et al., 2021a). ey reported dramatic central and peripheral
deoxygenation when performing maximal end-expiratory BH
at 60%–100% of maximal aerobic velocity, which could provide
adequate stimulus for the aforementioned training eects if
performed systematically.
Characteristics of elite free-divers suggest that long-term
adaptations to BH include reduced CO2 chemosensitivity and
increased lung volume (Bain etal., 2018; Elia etal., 2019). Repeated
hypercapnia (Bloch-Salisbury etal., 1996) and endurance training
(Katayama et al., 1999) cause long-term adaptations to lower
chemosensitivity (measured as the ventilatory response to a given
absolute workload). Moreover, reduced chemosensitivity during
exercise is a characteristic of trained athletes vs. healthy sedentary
individuals (McConnell and Semple, 1996). While increased pCO2
is responsible for the sensation of “air hunger” (Banzett et al.,
1990), it also allows for enhanced O2 transport via the Bohr
Eect. Decreased CO2 sensitivity, therefore, may allow for enhanced
ventilatory eciency and reduced BR. No studies could be found
directly investigating this mechanism in exercise.
Performing BH during running is best in a safe, supervised
environment with prior familiarization with BH techniques at
rest. e cited studies suggest a work:rest ratio of 1:1.5 or 1:2
(e.g., 10 s hold followed by 20 s running) for 10–12 repetitions.
Notably, participant instructions oen include counting cycles
per breath to “pace” BH duration; this is could facilitate use
of the “hold” tool in the eld. Most protocols recommend
end-expiratory BH since it accelerates hypoxaemia and
hypercapnia; this is done by performing a long exhale, and
then another, down to residual volume (Figure8). End-inspiratory
BH and very slow BR trigger similar levels of hypercapnia,
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but not of hypoxaemia required to maximize training eects
(Yamamoto etal., 1988; Holfelder and Becker, 2019). Adverse
eects include hypercapnia-induced headaches, lung injury,
syncope, and neurological harm if performed too oen or
aggressively (Matsuo etal., 2014). “Hold” is likely to beintensely
dicult and psychologically unpleasant since it induces large
feelings of air hunger. is may increase the risk for anxiety
and emotional distress in many individuals (von Leupoldt etal.,
2008). Conversely, if it can betolerated long enough to realize
its dramatic performance benets, it may cause benecial
reductions in EID, especially at high intensities. Important
work is being done to assist the execution and safety of BH
with wearable devices (Vinetti et al., 2020), but this has not
extended to BH during running.
Breathing is Quantiable
e control and expression of breathing pattern is tractibly
understood and every step can be reliably and specically
measured (Del Negro etal., 2018). We suggest measuring and
reporting dyspnoea intensity and discomfort in exercise studies
since these data points assist substantially in identifying
respiratory limitations (Lewthwaite and Jensen, 2021). If a
runner has access to qualied exercise physiology personnel,
cardiopulmonary exercise testing procedures can be especially
useful; we recommend measuring ventilatory thresholds,
tachypnoeic shi onset, VO2max, and approximate representations
of ventilatory eciency (including, but not limited to: running
economy, VE/VCO2 slope, and VT/BR quotient). Voluntary
spirometry measures such as forced expiratory volume and
maximum voluntary ventilation may provide additional insights.
For a detailed description of these laboratory-based procedures,
the reader is directed to recent reviews (Janssens etal., 2013;
Barnes and Kilding, 2015; Laveneziana etal., 2019; Segizbaeva
and Aleksandrova, 2019; Ionescu et al., 2020).
Recent developments in wearable sensors have expanded the
capabilities of respiratory system monitoring outside of the lab.
Non-contact methods such as respiratory inductance
plethysmography and capacitive sensors can provide estimations
of BR, thoraco-lumbar coordination, and the ratio of thoracic-
to-abdominal ribcage breathing (thoraco-lumbar depth) and VT
in the eld (Bernardi et al., 2017; Leutheuser et al., 2017;
Massaroni et al., 2019). Combined FR and step detection in
garments such as the Hexoskin® (Carre Technologies, Canada)
could enable LRC estimation in the eld (Harbour etal., 2021),
although such applications are scarce. When viewed in combination
with performance measures, monitoring BP may therefore reveal
deep individual constraints and context-specic insights that
could be modied or improved with these proposed breath
tools. Alternatively, these BP measurement methods and protocols
could also be used to scientically evaluate the eectiveness of
these strategies during breath retraining interventions.
Using Breath Tools
Although the value and quantity of resources related to breath
retraining at rest is substantial, less is known regarding implementing
breathing strategies during running. While we have provided
some specic recommendations for each strategy, some general
recommendations can bemade. Simple awareness of BP encourages
slow BR and greater depth during running (Schucker etal., 2014;
Schucker and Parrington, 2019). Breathing exercises at rest can
develop awareness of thoraco-lumbar coordination that carries
over into exercise performance (Hagman etal., 2011; Kiesel et al.,
2020). Runners can easily access such exercises in many Yoga
and meditation practices (Ma et al., 2017; Saoji et al., 2019).
A unified theory of breathing strategy prescription would
carefully choose the techniques above specific to the needs
of the runner and scenario (Tab l e 3 ). Wepropose the “Sync”
TABLE3 | Overview of breath tools strategies description and application.
Breath tool Description Primary mechanisms Advantages Disadvantages Applications
Rate and/or paced BR relative VD; ANS regulation perfusion; dyspnoea;
and pacing assistance
VT at less-compliant lung
volumes, initial air hunger
Novice runners; low-intensity
Deep VT via diaphragmatic
BR; abdominal ribcage
contribution to VE
WOB, LOV; postural
Difcult to cue Biofeedback; thoracic-
dominant breathers
Nose Constant or intermittent
nasal breathing
NO; air humidication,
warming, and ltration
airway constriction;
diaphragmatic activation
Difcult at high intensities;
time required for habituation
Low intensity exercise;
extreme climates
Active exhale Longer, forceful exhale
phase with/without
expiratory ow velocity:
abdominal engagement,
expiratory pressure, and NO
ow limitation, LOV;
perfusion; and ANS
relative TI; difcult to cue Constant for calming effects;
intermittent during high
intensity or at altitude
Sync Step & breath
synchronization at whole-
integer ratios
Step-driven ows; rhythmic
WOB; pacing assistance;
Difcult to learn; even ratios
side stitch
Odd ratios for side stitch;
breath awareness
Strength Respiratory muscle
resistance training
ventilatory muscle
activation, metabolic stress
WOB, dyspnoea;
diaphragmatic activation
Special equipment needed;
unclear protocols
Low intensity exercise;
training for competition
Hold Intermittent brief end-
expiratory breath holds
biochemical stress, spleen
cardiovascular performance
Risk of syncope, intense air
hunger unpleasant
Pre-competition; elite sport
Mechanisms, advantages, and disadvantages are based on a mixture of theoretical and empirical evidence as described in the main text. Applications are based on preliminary
subjective ndings of the authors, and do not constitute absolute recommendations. ANS, autonomic nervous system; BR, breathing rate; LOV, lung operating volume; NO, nitric
oxide; TI, inhale time; WOB, work of breathing; VT, tidal volume; and VD, dead space.
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 18 March 2022 | Volume 13 | Article 813243
tool as a near-universal practical recommendation, since it
can be leveraged to manipulate BR, depth, and timing.
However, there is limited knowledge available on how to
learn this skill. Simply counting steps per breath is likely
only suitable for skilled runners with experience in rhythm
(e.g., musicians or dancers). Coates and Kowalchik (2013)
describe a multi-step learning process that may besuitable
for coaches and athletes in field running. This could
becombined with the “gears” system suggested by McKenzie
(2020) to adjust BP to running intensity, or the postural
and verbal cues of Jackson (2002) to maintain active exhales
and proper abdominal engagement. Preliminary data from
our lab suggest that even novice runners can perform this
skill within one session given step-synchronous audio
guidance, although with variable cognitive load.
e eld of Human-Computer Interaction shows immense
promise in learning breathing strategies during running, with
demonstrators such as Strive (Valsted et al., 2017) and
Counterpace® (Constantini et al., 2018) exploiting step-
synchronized feedback modes. Core principles such as multi-
sensory experience, user-centered design, and embodied
interaction can guide the design of future systems to teach
runners how to breathe during running (Wiehr et al., 2017;
Mencarini et al., 2019; van Rheden et al., 2020). We propose
auditive and haptic-based feedback systems that are eld-ready
with real-time learning possibilities regarding the runner’s
current BP and adherence to the desired strategy.
Evidence suggests that breathing strategies such as LRC
might be more eective at relative intensities lesser or greater
than self-selected speeds (Stickford and Stickford, 2014).
Variations away from preferred gait speed tend to increase
the energy cost of transport (Hunter and Smith, 2007); thus,
at metabolically “suboptimal” speeds, breathing strategies have
a greater theoretical benet. At lower intensities, wehypothesize
that most runners could benet from slower, deeper, nose
breathing, which reduces the risk for respiratory limitations.
ese benets may beespecially helpful in extreme environments
(hypoxic, dry, and cold) when the risk for EID is higher (Weiler
et al., 2016). At higher intensities, strategies such as the active
exhale and sync might bemore helpful, as they might improve
gas exchange, optimize trunk kinematics, lower the WOB, and
maintain sustaintable BR. Wespeculate that the greatest benets
would be realized in respiratory-limited runners; this requires
more study.
Although breathing during running is measurable, modiable,
and improvable, several limitations must be addressed before
further study and application. Our review includes a mix of
experimental and theoretical evidence which requires more
direct investigation. Notably, there is a strong hypothesis that
BP manipulation is likely to be ineective or even harmful
when initially employed. If indeed healthy human ventilatory
response is “just right,” and lung structure is not plastic (Dempsey
et al., 2020), then perhaps changing BP will not result in
improved respiratory performance. Ventilatory eciency and
overall BP are considered the result of complexity in a well-
adjusted system (Benchetrit, 2000); any pertubations could
benot only cognitively demanding, but also energetically costly.
On the other hand, studies have shown that positive BP changes
can be habituated over time periods spanning 2–6 months
(Vickery, 2008; Dallam et al., 2018; Bahensky et al., 2019,
2021). It is unknown when exactly BP changes occur and
under what conditions. Some studies have questioned the benet
of internal focus during running, suggesting it leads to technique
breakdown and performance disruption (Beilock et al., 2002;
Hill et al., 2020). us, there may bea switching point when
the mental eort to change BP decreases, perhaps unlocking
resultant benets. Nevertheless, changing BP requires a
suppression of natural reexes and ingrained habits. More work
is needed to clarify if, how, and when BP changes and which
conditions facilitate this.
We have synthesized the evidence to demonstrate how
purposeful breathing strategies might improve running via
specic biochemical, biomechanical, and, ultimately,
psychophysiological mechanisms. Breathing strategies have the
potential to signicantly improve ventilatory eciency and
exercise performance but estimates of eect size are scarce
and variable. It is likely that breathing strategies do not acutely
improve exercise performance but have the potential to increase
it 1%–5% over a longer learning period. Respiratory-limited
individuals have the most to gain by using these techniques.
We theorize that the greatest benets are psychological;
increased exercise tolerance or positive psychological states
might increase runners’ exercise habits and long-term training
adherence. Intervention studies are needed to study these
likely transformative benets in vivo, especially over longer
durations and with populations predisposed to
respiratory limitations.
EH and TF: conceptualization. EH: writing—original dra
preparation and visualization. EH, TF, and TS: writing—review
and editing. TF and HS: supervision and funding acquisition.
HS: project administration. All authors contributed to the article
and approved the submitted version.
is work was partly funded by the Austrian Federal Ministry
for Transport, Innovation and Technology, the Austrian Federal
Ministry for Digital and Economic Aairs, and the federal
state of Salzburg under the research program COMET
Competence Centers for Excellent Technologies—in the project
Digital Motion in Sports, Fitness and Well-being (DiMo).
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 19 March 2022 | Volume 13 | Article 813243
Abu-Hasan, M., Tannous, B., and Weinberger, M. (2005). Exercise-induced
dyspnea in children and adolescents: if not asthma then what? Ann. Allergy
Asthma Immunol. 94, 366–371. doi: 10.1016/S1081-1206(10)60989-1
Adams, D., Pozzi, F., Willy, R. W., Carrol, A., and Zeni, J. (2018). Altering
cadence or vertical oscillation during running: eects on running related
injury factors. Int. J. Sports Phys. er. 13, 633–642. doi: 10.26603/
Aliverti, A. (2016). e respiratory muscles during exercise. Breathe 12, 165–168.
doi: 10.1183/20734735.008116
Aliverti, A., Uva, B., Laviola, M., Bovio, D., Mauro, A. L., Tarperi, C., et al.
(2010). Concomitant ventilatory and circulatory functions of the diaphragm
and abdominal muscles. J. Appl. Physiol. 109, 1432–1440. doi: 10.1152/
Allado, E., Poussel, M., Hily, O., and Chenuel, B. (2021). e interest of
rehabilitation of respiratory disorders in athletes: myth or reality? Ann.
Phys. Rehabil. Med. 65:101461. doi: 10.1016/
Amann, M. (2012). Pulmonary system limitations to endurance exercise
performance in humans. Exp. Physiol. 97, 311–318. doi: 10.1113/
Amann, M., Blain, G. M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., and
Dempsey, J. A. (2010). Group III and IV muscle aerents contribute to
ventilatory and cardiovascular response to rhythmic exercise in humans. J.
Appl. Physiol. 109, 966–976. doi: 10.1152/japplphysiol.00462.2010
Archiza, B., Leahy, M. G., Kipp, S., and Sheel, A. W. (2021). An integrative
approach to the pulmonary physiology of exercise: when does biological
sex matter? Eur. J. Appl. Physiol. 121, 2377–2391. doi: 10.1007/
Aydın, S., Cingi, C., San, T., Ulusoy, S., and Orhan, I. (2014). e eects of
air pollutants on nasal functions of outdoor runners. Eur. Arch. Otorhinolaryngol.
271, 713–717. doi: 10.1007/s00405-013-2610-1
Bahensky, P., Bunc, V., Malatova, R., Marko, D., Grosicki, G. J., and Schuster, J.
(2021). Impact of a breathing intervention on engagement of abdominal,
thoracic, and subclavian musculature during exercise, a randomized trial.
J. Clin. Med. 10:3514. doi: 10.3390/jcm10163514
Bahensky, P., Bunc, V., Marko, D., and Malatova, R. (2020). Dynamics of
ventilation parameters at dierent load intensities and the options to inuence
it by a breathing exercise. J. Sports Med. Phys. Fitness 60, 1101–1109. doi:
Bahensky, P., Malatova, R., and Bunc, V. (2019). Changed dynamic ventilation
parameters as a result of a breathing exercise intervention program. J. Sports
Med. Phys. Fitness 59, 1369–1375. doi: 10.23736/S0022-4707.19.09483-0
Bain, A. R., Drvis, I., Dujic, Z., Macleod, D. B., and Ainslie, P. N. (2018).
Physiology of static breath holding in elite apneists. Exp. Physiol. 103,
635–651. doi: 10.1113/EP086269
Banzett, R. B., Lansing, R. W., Brown, R., Topulos, G. P., Yager, D., Steele, S. M.,
et al. (1990). ‘Air hunger’ from increased PCO2 persists aer complete
neuromuscular block in humans. Respir. Physiol. 81, 1–17. doi:
Barbieri, J. F., Gaspari, A. F., Teodoro, C. L., Motta, L., Castano, L. A. A.,
Bertuzzi, R., et al. (2020). e eect of an airow restriction mask (ARM)
on metabolic, ventilatory, and electromyographic responses to continuous
cycling exercise. PLoS One 15:e0237010. doi: 10.1371/journal.pone.0237010
Barnes, K. R., and Kilding, A. E. (2015). Running economy: measurement,
norms, and determining factors. Sports Med. Open 1:8. doi: 10.1186/
Bechbache, R., and Dun, J. (1977). e entrainment of breathing frequency
by exercise rhythm. Phys. J. 272, 553–561.
Beilock, S. L., Carr, T. H., Macmahon, C., and Starkes, J. L. (2002). When
paying attention becomes counterproductive: impact of divided versus skill-
focused attention on novice and experienced performance of sensorimotor
skills. J. Exp. Psychol. Appl. 8:6. doi: 10.1037/1076-898X.8.1.6
Benchetrit, G. (2000). Breathing pattern in humans: diversity and individuality.
Respir. Physiol. 122, 123–129. doi: 10.1016/S0034-5687(00)00154-7
Bernardi, E., Pomidori, L., Bassal, F., Contoli, M., and Cogo, A. (2015).
Respiratory muscle training with normocapnic hyperpnea improves
ventilatory pattern and thoracoabdominal coordination, and reduces oxygen
desaturation during endurance exercise testing in COPD patients. Int. J.
Chron. Obstruct. Pulmon. Dis. 10, 1899–1906. doi: 10.2147/COPD.S88609
Bernardi, E., Pratali, L., Mandolesi, G., Spiridonova, M., Roi, G. S., and
Cogo, A. (2017). oraco-abdominal coordination and performance during
uphill running at altitude. PLoS One 12:e0174927. doi: 10.1371/journal.
Bernardi, L., Salvucci, F., Suardi, R., Soldá, P. L., Calciati, A., Perlini, S., et al.
(1990). Evidence for an intrinsic mechanism regulating heart rate variability
in the transplanted and the intact heart during submaximal dynamic exercise?
Cardiovasc. Res. 24, 969–981. doi: 10.1093/cvr/24.12.969
Bernasconi, P., Bürki, P., Bührer, A., Koller, E., and Kohl, J. (1995). Running
training and co-ordination between breathing and running rhythms during
aerobic and anaerobic conditions in humans. Eur. J. Appl. Physiol. Occup.
Physiol. 70, 387–393. doi: 10.1007/BF00618488
Bernasconi, P., and Kohl, J. (1993). Analysis of co-ordination between breathing
and exercise rhythms in man. Phys. J. 471, 693–706.
Bjorklund, G., Holmberg, H. C., and Stoggl, T. (2015). e eects of prior
high intensity double poling on subsequent diagonal stride skiing characteristics.
Springerplus 4:40. doi: 10.1186/s40064-015-0796-y
Blackie, S. P., Fairbarn, M. S., Mcelvaney, N. G., Wilcox, P. G., Morrison, N. J.,
and Pardy, R. L. (1991). Normal values and ranges for ventilation and breathing
pattern at maximal exercise. Chest 100, 136–142. doi: 10.1378/chest.100.1.136
Blain, G., Meste, O., and Bermon, S. (2005). Inuences of breathing patterns
on respiratory sinus arrhythmia in humans during exercise. Am. J. Physiol.
Heart Circ. Physiol. 288, H887–H895. doi: 10.1152/ajpheart.00767.2004
Bloch-Salisbury, E., Shea, S. A., Brown, R., Evans, K., and Banzett, R. B. (1996).
Air hunger induced by acute increase in PCO2 adapts to chronic elevation
of PCO2 in ventilated humans. J. Appl. Physiol. 81, 949–956.
Blum, J., Rockstroh, C., and Goritz, A. S. (2019). Heart rate variability biofeedback
based on slow-paced breathing with immersive virtual reality nature scenery.
Front. Psychol. 10:2172. doi: 10.3389/fpsyg.2019.02172
Bonsignore, M. R., Morici, G., Abate, P., Romano, S., and Bonsignore, G.
(1998). Ventilation and entrainment of breathing during cycling and running
in triathletes. Med. Sci. Sports Exerc. 30, 239–245. doi:
Bood, R. J., Nijssen, M., Van Der Kamp, J., and Roerdink, M. (2013). e
power of auditory-motor synchronization in sports: enhancing running
performance by coupling cadence with the right beats. PLoS One 8:e70758.
doi: 10.1371/journal.pone.0070758
Boulding, R., Stacey, R., Niven, R., and Fowler, S. J. (2016). Dysfunctional
breathing: a review of the literature and proposal for classication. Eur.
Respir. Rev. 25, 287–294. doi: 10.1183/16000617.0088-2015
Bradley, D., and Clion-Smith, T. (2009). BradCli® Manual. Auckland,
New Zealand: Writers Inc.
Bramble, D. M. (1989). Axial-appendicular dynamics and the integration of
breathing and gait in mammal. Am. Zool. 29, 171–186. doi: 10.1093/
Bramble, D. M., and Carrier, D. R. (1983). Running and breathing in mammals.
Science 219, 251–256. doi: 10.1126/science.6849136
Bramble, D. M., and Lieberman, D. E. (2004). Endurance running and the
evolution of homo. Nature 432, 345–352. doi: 10.1038/nature03052
Braun, S. R. (1990). Respiratory Rate and Pattern. Stoneham, MA, USA:
Butterworth Publishers, 226–230
Breuer, J. (1868). Die Selbststeuerung der Athmung durch den Nervus vagus.
Sitzungsberichte der kaiserlichen Akademie der Wissenschaen. Mathematisch–
naturwissenschaliche Classe, Wien, 1868, 58 Band, II. Abtheilung, 909–937.
Brick, N. E., Mcelhinney, M. J., and Metcalfe, R. S. (2018). e eects of facial
expression and relaxation cues on movement economy, physiological, and
perceptual responses during running. Psychol. Sport Exerc. 34, 20–28. doi:
Castro, R. R. T., Lima, S. P., Sales, A. R. K., and Nobrega, A. (2017). Minute-
ventilation variability during cardiopulmonary exercise test is higher in
sedentary men than in athletes. Arq. Bras. Cardiol. 109, 185–190. doi: 10.5935/
Caterini, J. E., Dun, J., and Wells, G. D. (2016). Limb movement frequency
is a signicant modulator of the ventilatory response during submaximal
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 20 March 2022 | Volume 13 | Article 813243
cycling exercise in humans. Respir. Physiol. Neurobiol. 220, 10–16. doi:
Chaitow, L., Bradley, D., and Gilbert, C. (2014). Recognizing and Treating
Breathing Disorders. London: Elsevier Health Sciences.
Clark, J. M., Sinclair, R. D., and Lenox, J. B. (1980). Chemical and nonchemical
components of ventilation during hypercapnic exercise in man. J. Appl.
Physiol. 48, 1065–1076. doi: 10.1152/jappl.1980.48.6.1065
Clark, F., and Von Euler, C. V. (1972). On the regulation of depth and rate
of breathing. Phys. J. 222, 267–295.
Cleary, S. (2019). e Eects of Deep Breathing on Exercise Performance in
Humans. PhD thesis. Dublin City University.
Coates, B., and Kowalchik, C. (2013). Runner’s World Running on Air: e
Revolutionary Way to Run Better by Breathing Smarter. New York: Rodale Books.
Cochrane-Snyman, K. C., Housh, T. J., Smith, C. M., Hill, E. C., and Jenkins, N. D.
(2019). Treadmill running using an RPE-clamp model: mediators of perception
and implications for exercise prescription. Eur. J. Appl. Physiol. 119, 2083–2094.
doi: 10.1007/s00421-019-04197-4
Constantini, K., Stickford, A. S. L., Bleich, J. L., Mannheimer, P. D., Levine, B. D.,
and Chapman, R. F. (2018). Synchronizing gait with cardiac cycle phase
alters heart rate response during running. Med. Sci. Sports Exerc. 50,
1046–1053. doi: 10.1249/MSS.0000000000001515
Daley, M. A., Bramble, D. M., and Carrier, D. R. (2013). Impact loading
and locomotor-respiratory coordination signicantly inuence breathing
dynamics in running humans. PLoS One 8:e70752. doi: 10.1371/journal.
Dallam, G., and Kies, B. (2020). e eect of nasal breathing versus oral and
oronasal breathing during exercise: a review. J. Sports Res. 7, 1–10. doi:
Dallam, G., Mcclaran, S., Cox, D., and Foust, C. (2018). Eect of nasal versus
oral breathing on vo2max and physiological economy in recreational runners
following an extended period spent using nasally restricted breathing. Int.
J. Kinesiol. Sports Sci. 6:22. doi: 10.7575/aiac.ijkss.v.6n.2p.22
Damm, L., Varoqui, D., De Cock, V. C., Dalla Bella, S., and Bardy, B. (2020).
Why do we move to the beat? A multi-scale approach, from physical
principles to brain dynamics. Neurosci. Biobehav. Rev. 112, 553–584. doi:
Davis, A. M., Ottenweller, J. E., Lamanca, J., Reisman, S. S., Findley, T. W.,
and Natelson, B. H. (1999). A simple biofeedback digital data collection
instrument to control ventilation during autonomic investigations. J. Auton.
Nerv. Syst. 77, 55–59. doi: 10.1016/S0165-1838(99)00035-1
De Couck, M., Caers, R., Musch, L., Fliegauf, J., Giangreco, A., and Gidron, Y.
(2019). How breathing can help you make better decisions: two studies on
the eects of breathing patterns on heart rate variability and decision-making
in business cases. Int. J. Psychophysiol. 139, 1–9. doi: 10.1016/j.
De Ruiter, C. J., Van Daal, S., and Van Dieen, J. H. (2019). Individual optimal
step frequency during outdoor running. Eur. J. Sport Sci. 20, 1–9. doi:
Del Negro, C. A., Funk, G. D., and Feldman, J. L. (2018). Breathing matters.
Nat. Rev. Neurosci. 19, 351–367. doi: 10.1038/s41583-018-0003-6
Dempsey, J. A., La Gerche, A., and Hull, J. H. (2020). Is the healthy respiratory
system built just right, overbuilt, or underbuilt to meet the demands imposed
by exercise? J. Appl. Physiol. 129, 1235–1256. doi: 10.1152/
Depiazzi, J., and Everard, M. L. (2016). Dysfunctional breathing and reaching
one’s physiological limit as causes of exercise-induced dyspnoea. Breathe
12, 120–129. doi: 10.1183/20734735.007216
Ekkekakis, P., Partt, G., and Petruzzello, S. J. (2011). e pleasure and displeasure
people feel when they exercise at dierent intensities. Sports Med. 41, 641–671.
doi: 10.2165/11590680-000000000-00000
Elia, A., Wilson, O. J., Lees, M., Parker, P. J., Barlow, M. J., Cocks, M., et al.
(2019). Skeletal muscle, haematological and splenic volume characteristics
of elite breath-hold divers. Eur. J. Appl. Physiol. 119, 2499–2511. doi: 10.1007/
Elliott, A. D., and Grace, F. (2010). An examination of exercise mode on
ventilatory patterns during incremental exercise. Eur. J. Appl. Physiol. 110,
557–562. doi: 10.1007/s00421-010-1541-4
Ersson, K., Mallmin, E., Malinovschi, A., Norlander, K., Johansson, H., and
Nordang, L. (2020). Prevalence of exercise-induced bronchoconstriction and
laryngeal obstruction in adolescent athletes. Pediatr. Pulmonol. 55, 3509–3516.
doi: 10.1002/ppul.25104
Expeditions (2014). Moving Air: Breathing For Performance. Mountaineering
Training [Online]. Available at:
mountaineering_training_moving_air_breathing_for_performance (Accessed
October 15, 2021).
Fabre, N., Perrey, S., Arbez, L., and Rouillon, J.-D. (2007). Neuro-mechanical
and chemical inuences on locomotor respiratory coupling in humans. Respir.
Physiol. Neurobiol. 155, 128–136. doi: 10.1016/j.resp.2006.04.015
Ferretti, G., Fagoni, N., Taboni, A., Bruseghini, P., and Vinetti, G. (2017). e
physiology of submaximal exercise: e steady state concept. Respir. Physiol.
Neurobiol. 246, 76–85. doi: 10.1016/j.resp.2017.08.005
Forster, H. V., Haouzi, P., and Dempsey, J. A. (2012). Control of breathing
during exercise. Compr. Physiol. 2, 743–777. doi: 10.1002/cphy.c100045
Garlando, F., Kohl, J., Koller, E., and Pietsch, P. (1985). Eect of coupling the
breathing-and cycling rhythms on oxygen uptake during bicycle ergometry.
Eur. J. Appl. Physiol. Occup. Physiol. 54, 497–501. doi: 10.1007/BF00422959
Gilbert, R., Auchincloss, J. Jr., Brodsky, J., and Boden, W. A. (1972). Changes
in tidal volume, frequency, and ventilation induced by their measurement.
J. Appl. Physiol. 33, 252–254. doi: 10.1152/jappl.1972.33.2.252
Girard, O., Brocherie, F., Goods, P. S. R., and Millet, G. P. (2020). An updated
panorama of “living low-training high” altitude/hypoxic methods. Front.
Sports Act. Living 2:26. doi: 10.3389/fspor.2020.00026
Granados, J., Gillum, T. L., Castillo, W., Christmas, K. M., and Kuennen, M. R.
(2016). “Functional” respiratory muscle training during endurance exercise
causes modest hypoxemia but overall is well tolerated. J. Strength Cond.
Res. 30, 755–762. doi: 10.1519/JSC.0000000000001151
Grassmann, M., Vlemincx, E., Von Leupoldt, A., Mittelstadt, J. M., and Van
Den Bergh, O. (2016). Respiratory changes in response to cognitive load:
a systematic review. Neural Plast. 2016:8146809. doi: 10.1155/2016/8146809
Gravier, G., Delliaux, S., Delpierre, S., Guieu, R., and Jammes, Y. (2013). Inter-
individual dierences in breathing pattern at high levels of incremental
cycling exercise in healthy subjects. Respir. Physiol. Neurobiol. 189, 59–66.
doi: 10.1016/j.resp.2013.06.027
Hagman, C., Janson, C., and Emtner, M. (2011). Breathing retraining—a ve-
year follow-up of patients with dysfunctional breathing. Respir. Med. 105,
1153–1159. doi: 10.1016/j.rmed.2011.03.006
Hamasaki, H. (2020). Eects of diaphragmatic breathing on health: a narrative
review. Medicine 7:65. doi: 10.3390/medicines7100065
Harbour, E., Lasshofer, M., Genitrini, M., and Schwameder, H. (2021). Enhanced
breathing pattern detection during running using wearable sensors. Sensors
21:5606. doi: 10.3390/s21165606
Hayano, J., Mukai, S., Sakakibara, M., Okada, A., Takata, K., and Fujinami, T.
(1994). Eects of respiratory interval on vagal modulation of heart rate.
Am. J. Physiol. Heart Circ. Physiol. 267, H33–H40. doi: 10.1152/
Hazlett-Stevens, H., and Craske, M. G. (2009). “Breathing retraining and
diaphragmatic breathing techniques,” in Cognitive Behavior erapy: Applying
Empirically Supported Techniques in your Practice. eds. W. T. O’donohue,
J. E. Fisher and S. C. Hayes (Hoboken, New Jersey: John Wiley & Sons),
Hellyer, N. J., Folsom, I. A., Gaz, D. V., Kakuk, A. C., Mack, J. L., and Ver
Mulm, J. A. (2015). Respiratory muscle activity during simultaneous stationary
cycling and inspiratory muscle training. J. Strength Cond. Res. 29, 3517–3522.
doi: 10.1097/JSC.0000000000000238
Hering, K. E. K. (1868). Die Selbststeuerung der Athmung durch den Nervus
vagus. Sitzungsberichte der kaiserlichen Akademie der Wissenschaen.
Mathematisch–naturwissenschaliche Classe, Wien, 1868, 57 Band, II.
Abtheilung, 672–677.
Hey, E., Lloyd, B., Cunningham, D., Jukes, M., and Bolton, D. (1966). Eects
of various respiratory stimuli on the depth and frequency of breathing in
man. Respir. Physiol. 1, 193–205. doi: 10.1016/0034-5687(66)90016-8
Hill, A., Schücker, L., Wiese, M., Hagemann, N., and Strauß, B. (2020). e
inuence of mindfulness training on running economy and perceived ow
under dierent attentional focus conditions–an intervention study. Int. J.
Sport Exerc. Psychol. 19, 1–20. doi: 10.1080/1612197X.2020.1739110
Homann, C. P., Torregrosa, G., and Bardy, B. G. (2012). Sound stabilizes
locomotor-respiratory coupling and reduces energy cost. PLoS One 7:e45206.
doi: 10.1371/journal.pone.0045206
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 21 March 2022 | Volume 13 | Article 813243
Holfelder, B., and Becker, F. (2019). Hypoventilation training: a systematic
review. Sports Exerc. Med. Switzerland. 66. doi: 10.34045/SSEM/2018/23
Homma, I., and Masaoka, Y. (2008). Breathing rhythms and emotions. Exp.
Physiol. 93, 1011–1021. doi: 10.1113/expphysiol.2008.042424
Hunter, I., and Smith, G. A. (2007). Preferred and optimal stride frequency,
stiness and economy: changes with fatigue during a 1-h high-intensity
run. Eur. J. Appl. Physiol. 100, 653–661. doi: 10.1007/s00421-007-0456-1
Inoue, Y., Nakajima, A., Mizukami, S., and Hata, H. (2013). Eect of breath
holding on spleen volume measured by magnetic resonance imaging. PLoS
One 8:e68670. doi: 10.1371/journal.pone.0068670
Ionescu, M. F., Mani-Babu, S., Degani-Costa, L. H., Johnson, M., Paramasivan, C.,
Sylvester, K., et al. (2020). Cardiopulmonary exercise testing in the assessment
of dysfunctional breathing. Front. Physiol. 11:620955. doi: 10.3389/
Ito, K., Nonaka, K., Ogaya, S., Ogi, A., Matsunaka, C., and Horie, J. (2016).
Surface electromyography activity of the rectus abdominis, internal oblique,
and external oblique muscles during forced expiration in healthy adults. J.
Electromyogr. Kinesiol. 28, 76–81. doi: 10.1016/j.jelekin.2016.03.007
Itoh, M., Ueoka, H., Aoki, T., Hotta, N., Kaneko, Y., Takita, C., et al. (2007).
Exercise hyperpnea and hypercapnic ventilatory responses in women. Res pir.
Med. 101, 446–452. doi: 10.1016/j.rmed.2006.07.011
Izumizaki, M., Masaoka, Y., and Homma, I. (2011). Coupling of dyspnea
perception and tachypneic breathing during hypercapnia. Respir. Physiol.
Neurobiol. 179, 276–286. doi: 10.1016/j.resp.2011.09.007
Jackson, I. (2002). e benet of breathing out and in, instead of in and out.
Healing Breath 4:2.
Janssens, L., Brumagne, S., Mcconnell, A. K., Raymaekers, J., Goossens, N.,
Gayan-Ramirez, G., et al. (2013). e assessment of inspiratory muscle
fatigue in healthy individuals: a systematic review. Respir. Med. 107, 331–346.
doi: 10.1016/j.rmed.2012.11.019
Jimenez Morgan, S., and Molina Mora, J. A. (2017). Eect of heart rate variability
biofeedback on sport performance, a systematic review. Appl. Psychophysiol.
Biofeedback 42, 235–245. doi: 10.1007/s10484-017-9364-2
Johansson, H., Norlander, K., Berglund, L., Janson, C., Malinovschi, A., Nordvall, L.,
et al. (2015). Prevalence of exercise-induced bronchoconstriction and exercise-
induced laryngeal obstruction in a general adolescent population. orax
70, 57–63. doi: 10.1136/thoraxjnl-2014-205738
Johnston, K. L., Bradford, H., Hodges, H., Moore, C. M., Nauman, E., and
Olin, J. T. (2018). e Olin EILOBI breathing techniques: description and
initial case series of novel respiratory retraining strategies for athletes with
exercise-induced laryngeal obstruction. J. Voic e 32, 698–704. doi: 10.1016/j.
Karsten, M., Ribeiro, G. S., Esquivel, M. S., and Matte, D. L. (2018). e
eects of inspiratory muscle training with linear workload devices on the
sports performance and cardiopulmonary function of athletes: A systematic
review and meta-analysis. Phys. er. Sport 34, 92–104. doi: 10.1016/j.
Karsten, M., Ribeiro, G. S., Esquivel, M. S., and Matte, D. L. (2019). Maximizing
the eectiveness of inspiratory muscle training in sports performance: A
current challenge. Phys. er. Sport 36, 68–69. doi: 10.1016/j.ptsp.2019.01.004
Katayama, K., Sato, Y., Morotome, Y., Shima, N., Ishida, K., Mori, S., et al.
(1999). Ventilatory chemosensitive adaptations to intermittent hypoxic exposure
with endurance training and detraining. J. Appl. Physiol. 86, 1805–1811.
doi: 10.1152/jappl.1999.86.6.1805
Kiesel, K., Burklow, M., Garner, M. B., Hayden, J., Hermann, A. J., Kingshott, E.,
et al. (2020). Exercise intervention for individuals with dysfunctional breathing:
a matched controlled trial. Int. J. Sports Phys. er. 15, 114–125. doi: 10.26603/
Ki, J., and Williams, E. M. (2007). e respiratory time and ow prole at
volitional exercise termination. J. Sports Sci. 25, 1599–1606. doi:
Kohl, J., Koller, E., and Jäger, M. (1981). Relation between pedalling-and breathing
rhythm. Eur. J. Appl. Physiol. Occup. Physiol. 47, 223–237. doi: 10.1007/
Kume, D., Akahoshi, S., Yamagata, T., Wakimoto, T., and Nagao, N. (2016).
Does voluntary hypoventilation during exercise impact EMG activity?
Springerplus 5:149. doi: 10.1186/s40064-016-1845-x
Lapointe, J., Paradis-Deschenes, P., Woorons, X., Lemaitre, F., and Billaut, F.
(2020). Impact of hypoventilation training on muscle oxygenation, myoelectrical
changes, systemic [k(+)], and repeated-sprint ability in basketball players.
Front. Sports Act. Living 2:29. doi: 10.3389/fspor.2020.00029
Laveneziana, P., Albuquerque, A., Aliverti, A., Babb, T., Barreiro, E., Dres, M.,
et al. (2019). ERS statement on respiratory muscle testing at rest and during
exercise. Eur. Respir. J. 53:1801214. doi: 10.1183/13993003.01214-2018
Laviolette, L., and Laveneziana, P. (2014). Dyspnoea: a multidimensional and
multidisciplinary approach. Eur. Respir. J. 43, 1750–1762. doi:
Le Gal, J. P., Juvin, L., Cardoit, L., oby-Brisson, M., and Morin, D. (2014).
Remote control of respiratory neural network by spinal locomotor generators.
PLoS One 9:e89670. doi: 10.1371/journal.pone.0089683
Lehrer, P., Kaur, K., Sharma, A., Shah, K., Huseby, R., Bhavsar, J., et al. (2020).
Heart rate variability biofeedback improves emotional and physical health
and performance: a systematic review and meta analysis. Appl. Psychophysiol.
Biofeedback 45, 109–129. doi: 10.1007/s10484-020-09466-z
Leutheuser, H., Heyde, C., Roecker, K., Gollhofer, A., and Eskoer, B. M.
(2017). Reference-free adjustment of respiratory inductance plethysmography
for measurements during physical exercise. IEEE Trans. Biomed. Eng. 64,
2836–2846. doi: 10.1109/TBME.2017.2675941
Lewthwaite, H., and Jensen, D. (2021). Multidimensional breathlessness assessment
during cardiopulmonary exercise testing in healthy adults. Eur. J. Appl.
Physiol. 121, 499–511. doi: 10.1007/s00421-020-04537-9
Lorca-Santiago, J., Jimenez, S. L., Pareja-Galeano, H., and Lorenzo, A. (2020).
Inspiratory muscle training in intermittent sports modalities: a systematic
review. Int. J. Environ. Res. Public Health 17:4448. doi: 10.3390/ijerph17124448
Lucía, A., Carvajal, A., Calderón, F. J., Alfonso, A., and Chicharro, J. L. (1999).
Breathing pattern in highly competitive cyclists during incremental exercise.
Eur. J. Appl. Physiol. Occup. Physiol. 79, 512–521.
Lucía, A., Hoyos, J., Pardo, J., and Chicharro, J. L. (2001). Eects of endurance
training on the breathing pattern of professional cyclists. Jpn. J. Physiol.
51, 133–141. doi: 10.2170/jjphysiol.51.133
Ma, X., Yue, Z. Q., Gong, Z. Q., Zhang, H., Duan, N. Y., Shi, Y. T., et al.
(2017). e eect of diaphragmatic breathing on attention, negative aect
and stress in healthy adults. Front. Psychol. 8:874. doi: 10.3389/fpsyg.2017.00874
Maclennan, S. E., Silvestri, G. A., Ward, J., and Mahler, D. A. (1994). Does
entrained breathing improve the economy of rowing? Med. Sci. Sports Exerc.
26, 610–614
Mangla, P., and Menon, M. (1981). Eect of nasal and oral breathing on
exercise-induced asthma. Clin. Exp. Allergy 11, 433–439. doi:
Marcora, S. (2009). Perception of eort during exercise is independent of aerent
feedback from skeletal muscles, heart, and lungs. J. Appl. Physiol. 106,
2060–2062. doi: 10.1152/japplphysiol.90378.2008
Marko, D. (2020). “Comparison of results of spiroergometry on running and
bicycle ergometer of athletes with running and cycling specialization.” in
Proceedings of the 12th International Conference on Kinanthropology. November
7-9, 2019.
Martarelli, D., Cocchioni, M., Scuri, S., and Pompei, P. (2011). Diaphragmatic
breathing reduces exercise-induced oxidative stress. Evid. Based Complement.
Alternat. Med. 2011:932430. doi: 10.1093/ecam/nep169
Masaoka, Y., and Homma, I. (2001). e eect of anticipatory anxiety on
breathing and metabolism in humans. Respir. Physiol. 128, 171–177. doi:
Massaroni, C., Nicolò, A., Lo Presti, D., Sacchetti, M., Silvestri, S., and Schena, E.
(2019). Contact-based methods for measuring respiratory rate. Sensors 19:908.
doi: 10.3390/s19040908
Mathias, B., Zamm, A., Gianferrara, P. G., Ross, B., and Palmer, C. (2020).
Rhythm complexity modulates behavioral and neural dynamics during
auditory–motor synchronization. J. Cogn. Neurosci. 32, 1864–1880. doi:
Matsumoto, T., Masuda, T., Hotta, K., Shimizu, R., Ishii, A., Kutsuna, T., et al.
(2011). Eects of prolonged expiration breathing on cardiopulmonary responses
during incremental exercise. Respir. Physiol. Neurobiol. 178, 275–282. doi:
Matsumoto, T., Matsunaga, A., Hara, M., Saitoh, M., Yonezawa, R., Ishii, A.,
et al. (2008). Eects of the breathing mode characterized by prolonged
expiration on respiratory and cardiovascular responses and autonomic nervous
activity during the exercise. Jpn. J. Phys. Fit. 57, 315–326. doi: 10.7600/
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 22 March 2022 | Volume 13 | Article 813243
Matsuo, R., Kamouchi, M., Arakawa, S., Furuta, Y., Kanazawa, Y., and
Kitazono, T. (2014). Magnetic resonance imaging in breath-hold divers
with cerebral decompression sickness. Case Rep. Neurol. 6, 23–27. doi:
Mccarey, T. V., and Kern, E. B. (1979). Response of nasal airway resistance
to hypercapnia and hypoxia in man. Ann. Otol. Rhinol. Laryngol. 88, 247–252.
doi: 10.1177/000348947908800217
Mcconnell, A. K., and Semple, E. (1996). Ventilatory sensitivity to carbon
dioxide: the inuence of exercise and athleticism. Med. Sci. Sports Exerc.
28, 685–691. doi: 10.1097/00005768-199606000-00007
Mcdermott, W. J., Van Emmerik, R. E., and Hamill, J. (2003). Running training
and adaptive strategies of locomotor-respiratory coordination. Eur. J. Appl.
Physiol. 89, 435–444. doi: 10.1007/s00421-003-0831-5
Mckenzie, B. (2020). “e Gears,” (ed.) Sh//Ft. (Vimeo).
Mead, J. (1960). Control of respiratory frequency. J. Appl. Physiol. 15, 325–336.
doi: 10.1152/jappl.1960.15.3.325
Mencarini, E., Rapp, A., Tirabeni, L., and Zancanaro, M. (2019). Designing
wearable systems for sports: a review of trends and opportunities in human–
computer interaction. IEEE Trans. Hum. Mach. Syst. 49, 314–325. doi: 10.1109/
Mertz, J. S., Mccarey, T. V., and Kern, E. B. (1984). Role of the nasal airway
in regulation of airway resistance during hypercapnia and exercise. Otolaryngol.
Head Neck Surg. 92, 302–307. doi: 10.1177/019459988409200311
Millet, G. P., Debevec, T., Brocherie, F., Malatesta, D., and Girard, O. (2016).
erapeutic use of exercising in hypoxia: promises and limitations. Front.
Physiol. 7:224. doi: 10.3389/fphys.2016.00224
Morton, D., and Callister, R. (2015). Exercise-related transient abdominal pain
(ETAP). Sports Med. 45, 23–35. doi: 10.1007/s40279-014-0245-z
Morton, A., King, K., Papalia, S., Goodman, C., Turley, K., and Wilmore, J.
(1995). Comparison of maximal oxygen consumption with oral and nasal
breathing. Aust. J. Sci. Med. Sport 27, 51–55
Naranjo, J., Centeno, R. A., Galiano, D., and Beaus, M. (2005). A nomogram
for assessment of breathing patterns during treadmill exercise. Br. J. Sports
Med. 39, 80–83. doi: 10.1136/bjsm.2003.009316
Nelson, N. (2012). Diaphragmatic breathing: the foundation of core stability.
Strength Cond. J. 34, 34–40. doi: 10.1519/SSC.0b013e31826ddc07
Nicolò, A., Girardi, M., Bazzucchi, I., Felici, F., and Sacchetti, M. (2018).
Respiratory frequency and tidal volume during exercise: dierential control
and unbalanced interdependence. Phys. Rep. 6:e13908. doi: 10.14814/phy2.13908
Nicolò, A., Girardi, M., and Sacchetti, M. (2017a). Control of the depth and
rate of breathing: metabolic vs. non-metabolic inputs. J. Physiol. 595, 6363–6364.
doi: 10.1113/JP275013
Nicolo, A., Marcora, S. M., and Sacchetti, M. (2016). Respiratory frequency is
strongly associated with perceived exertion during time trials of dierent
duration. J. Sports Sci. 34, 1199–1206. doi: 10.1080/02640414.2015.1102315
Nicolo, A., Marcora, S. M., and Sacchetti, M. (2020). Last word on viewpoint:
time to reconsider how ventilation is regulated above the respiratory
compensation point during incremental exercise. J. Appl. Physiol. 128:1456.
doi: 10.1152/japplphysiol.00285.2020
Nicolò, A., Marcora, S. M., and Sacchetti, M. (2020a). Time to reconsider how
ventilation is regulated above the respiratory compensation point during
incremental exercise. J. Appl. Physiol. 128, 1447–1449. doi: 10.1152/
Nicolò, A., Massaroni, C., and Passeld, L. (2017b). Respiratory frequency
during exercise: the neglected physiological measure. Front. Physiol. 8:922.
doi: 10.3389/fphys.2017.00922
Nicolò, A., Massaroni, C., Schena, E., and Sacchetti, M. (2020b). e importance
of respiratory rate monitoring: from healthcare to sport and exercise. Sensors
20:6396. doi: 10.3390/s20216396
Nicolo, A., and Sacchetti, M. (2019). A new model of ventilatory control during
exercise. Exp. Physiol. 104, 1331–1332. doi: 10.1113/EP087937
Niinimaa, V. (1983). Oronasal airway choice during running. Respir. Physiol.
53, 129–133. doi: 10.1016/0034-5687(83)90021-X
Nijs, A., Roerdink, M., and Beek, P. J. (2020). Cadence modulation in walking
and running: pacing steps or strides? Brain Sci. 10:273. doi: 10.3390/
Noakes, T. D. (2012). Fatigue is a brain-derived emotion that regulates the
exercise behavior to ensure the protection of whole body homeostasis. Front.
Physiol. 3:82. doi: 10.3389/fphys.2012.00082
Nolan, A. (2016). e State of the American Runner [Online]. Runner’s World.
Available at:
state-of-the-american-runner-2016/ (Accessed 11 October 2021).
O’halloran, J., Hamill, J., Mcdermott, W. J., Remelius, J. G., and Van Emmerik, R. E.
(2012). Locomotor-respiratory coupling patterns and oxygen consumption
during walking above and below preferred stride frequency. Eur. J. Appl.
Physiol. 112, 929–940. doi: 10.1007/s00421-011-2040-y
Ogles, B., Masters, K., and Richardson, S. (1995). Obligatory running and
gender: an analysis of participative motives and training habits. Int. J. Sport
Psychol. 26, 233–248.
Okuro, R. T., Morcillo, A. M., Sakano, E., Schivinski, C. I. S., Ribeiro, M. Â.
G. O., and Ribeiro, J. D. (2011). Exercise capacity, respiratory mechanics
and posture in mouth breathers. Braz. J. Otorhinolaryngol. 77, 656–662.
doi: 10.1590/S1808-86942011000500020
Olson, L. G., and Strohl, K. P. (1987). e response of the nasal airway to
exercise. Am. Rev. Respir. Dis. 135, 356–359. doi: 10.1164/arrd.1987.135.2.356
Pereira, H. V., Palmeira, A. L., Encantado, J., Marques, M. M., Santos, I.,
Carraa, E. V., et al. (2021). Systematic review of psychological and behavioral
correlates of recreational running. Front. Psychol. 12:624783. doi: 10.3389/
Persegol, L., Jordan, M., and Viala, D. (1991). Evidence for the entrainment
of breathing by locomotor pattern in human. J. Physiol. 85, 38–43
Porcari, J. P., Probst, L., Forrester, K., Doberstein, S., Foster, C., Cress, M. L.,
et al. (2016). Eect of wearing the elevation training mask on aerobic
capacity, lung function, and hematological variables. J. Sports Sci. Med. 15,
Pramanik, T., Sharma, H. O., Mishra, S., Mishra, A., Prajapati, R., and Singh, S.
(2009). Immediate eect of slow pace bhastrika pranayama on blood pressure
and heart rate. J. Altern. Complement. Med. 15, 293–295. doi: 10.1089/
Prigent, G., Aminian, K., Rodrigues, T., Vesin, J. M., Millet, G. P., Falbriard, M.,
et al. (2021). Indirect estimation of breathing rate from heart rate monitoring
system during running. Sensors 21:5651. doi: 10.3390/s21165651
Recinto, C., Ehemeou, T., Boelli, P. T., and Navalta, J. W. (2017). Eects of
nasal or oral breathing on anaerobic power output and metabolic responses.
Int. J. Exerc. Sci. 10, 506–514
Ross, C. F., Blob, R. W., Carrier, D. R., Daley, M. A., Deban, S. M., Demes, B.,
et al. (2013). e evolution of locomotor rhythmicity in tetrapods. Evolution
67, 1209–1217. doi: 10.1111/evo.12015
Rupp, T., Saugy, J. J., Bourdillon, N., Verges, S., and Millet, G. P. (2019).
Positive expiratory pressure improves arterial and cerebral oxygenation in
acute normobaric and hypobaric hypoxia. Am. J. Phys. Regul. Integr. Comp.
Phys. 317, R754–R762. doi: 10.1152/ajpregu.00025.2019
Russo, M. A., Santarelli, D. M., and O’rourke, D. (2017). e physiological
eects of slow breathing in the healthy human. Breathe 13, 298–309. doi:
Sabatucci, A., Raaeli, F., Mastrovincenzo, M., Luchetta, A., Giannone, A., and
Ciavarella, D. (2015). Breathing pattern and head posture: changes in
craniocervical angles. Minerva Stomatol. 64, 59–74
Saibene, F., Mognoni, P., Lafortuna, C. L., and Mostardi, R. (1978). Oronasal
breathing during exercise. Pugers Arch. 378, 65–69. doi: 10.1007/BF00581959
Salazar-Martinez, E., De Matos, T. R., Arrans, P., Santalla, A., and Orellana, J. N.
(2018). Ventilatory eciency response is unaected by tness level, ergometer
type, age or body mass index in male athletes. Biol. Sport 35, 393–398.
doi: 10.5114/biolsport.2018.78060
Salazar-Martinez, E., Terrados, N., Burtscher, M., Santalla, A., and Naranjo
Orellana, J. (2016). Ventilatory eciency and breathing pattern in world-
class cyclists: A three-year observational study. Respir. Physiol. Neurobiol.
229, 17–23. doi: 10.1016/j.resp.2016.04.001
Sanchez Crespo, A., Hallberg, J., Lundberg, J. O., Lindahl, S. G., Jacobsson, H.,
Weitzberg, E., et al. (2010). Nasal nitric oxide and regulation of human
pulmonary blood ow in the upright position. J. Appl. Physiol. 108, 181–188.
doi: 10.1152/japplphysiol.00285.2009
Saoji, A. A., Raghavendra, B. R., and Manjunath, N. K. (2019). Eects of yogic
breath regulation: a narrative review of scientic evidence. J. Ayurveda Integr.
Med. 10, 50–58. doi: 10.1016/j.jaim.2017.07.008
Schaer, C. E., Wuthrich, T. U., Beltrami, F. G., and Spengler, C. M. (2019).
Eects of sprint-interval and endurance respiratory muscle training regimens.
Med. Sci. Sports Exerc. 51, 361–371. doi: 10.1249/MSS.0000000000001782
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 23 March 2022 | Volume 13 | Article 813243
Schelegle, E. S., and Green, J. F. (2001). An overview of the anatomy and
physiology of slowly adapting pulmonary stretch receptors. Respir. Physiol.
125, 17–31. doi: 10.1016/S0034-5687(00)00202-4
Schucker, L., Knopf, C., Strauss, B., and Hagemann, N. (2014). An internal
focus of attention is not always as bad as its reputation: how specic aspects
of internally focused attention do not hinder running eciency. J. Sport
Exerc. Psychol. 36, 233–243. doi: 10.1123/jsep.2013-0200
Schucker, L., and Parrington, L. (2019). inking about your running movement
makes you less ecient: attentional focus eects on running economy and
kinematics. J. Sports Sci. 37, 638–646. doi: 10.1080/02640414.2018.1522697
Seals, D. R., Suwarno, N. O., Joyner, M. J., Iber, C., Copeland, J. G., and
Dempsey, J. A. (1993). Respiratory modulation of muscle sympathetic nerve
activity in intact and lung denervated humans. Circ. Res. 72, 440–454. doi:
Segizbaeva, M. O., and Aleksandrova, N. P. (2019). Assessment of the functional
state of respiratory muscles: methodological aspects and data interpretation.
Hum. Physiol. 45, 213–224. doi: 10.1134/S0362119719010110
Sheel, A. W., Boushel, R., and Dempsey, J. A. (2018). Competition for blood
ow distribution between respiratory and locomotor muscles: implications
for muscle fatigue. J. Appl. Physiol. 125, 820–831. doi: 10.1152/
Sheel, A. W., Foster, G. E., and Romer, L. M. (2011). Exercise and its impact
on dyspnea. Curr. Opin. Pharmacol. 11, 195–203. doi: 10.1016/j.coph.2011.04.004
Sheel, A. W., and Romer, L. M. (2011). Ventilation and respiratory mechanics.
Compr. Physiol. 2, 1093–1142. doi: 10.1002/cphy.c100046
Sheel, A. W., Taylor, J. L., and Katayama, K. (2020). e hyperpnoea of exercise
in health: respiratory inuences on neurovascular control. Exp. Physiol. 105,
1984–1989. doi: 10.1113/EP088103
Shei, R. J. (2018). Recent advancements in our understanding of the ergogenic
eect of respiratory muscle training in healthy humans: a systematic review.
J. Strength Cond. Res. 32, 2665–2676. doi: 10.1519/JSC.0000000000002730
Shturman-Ellstein, R., Zeballos, R., Buckley, J., and Souhrada, J. (1978). e
benecial eect of nasal breathing on exercise-induced bronchoconstriction.
Am. Rev. Respir. Dis. 118, 65–73. doi: 10.1164/arrd.1978.118.1.65
Smith, J. R., Kurti, S. P., Meskimen, K., and Harms, C. A. (2017). Expiratory
ow limitation and operating lung volumes during exercise in older and
younger adults. Respir. Physiol. Neurobiol. 240, 26–31. doi: 10.1016/j.
Smoliga, J. M., Mohseni, Z. S., Berwager, J. D., and Hegedus, E. J. (2016).
Common causes of dyspnoea in athletes: a practical approach for diagnosis
and management. Breathe 12, e22–e37. doi: 10.1183/20734735.006416
Snyder, C. R., Lopez, S. J., Edwards, L. M., and Marques, S. C. (2020). e
Oxford Handbook of Positive Psychology. New York: Oxford university press.
Statista (2018). “Number of participants in running/jogging and trail running
in the U.S. from 2006 to 2017 (in millions).” (Statista: Outdoor Foundation).
Stickford, A. S., and Stickford, J. L. (2014). Ventilation and locomotion in
humans: mechanisms, implications, and perturbations to the coupling of
these two rhythms. Springer Sci. Rev. 2, 95–118. doi: 10.1007/s40362-014-0020-4
Stickford, A. S. L., Stickford, J. L., Fulton, T. J., Lovci, T. L., and Chapman, R. F.
(2020). Attentional focus does not impact locomotor-respiratory coupling
in trained runners. Eur. J. Appl. Physiol. 120, 2477–2486. doi: 10.1007/
Takano, N., and Deguchi, H. (1997). Sensation of breathlessness and respiratory
oxygen cost during cycle exercise with and without conscious entrainment
of the breathing rhythm. Eur. J. Appl. Physiol. Occup. Physiol. 76, 209–213.
doi: 10.1007/s004210050238
omas, S.A., Phillips, V., Mock, C., Lock, M., Cox, G., and Baxter, J. (2009).
“e eects of nasal breathing on exercise tolerance,” in Chartered Society
of Physiotherapy Annual Congress. October 17, 2009.
ornadtsson, A., Drca, N., Ricciardolo, F., and Hogman, M. (2017). Increased
levels of alveolar and airway exhaled nitric oxide in runners. Ups. J. Med.
Sci. 122, 85–91. doi: 10.1080/03009734.2017.1317886
Tipton, M. J., Harper, A., Paton, J. F., and Costello, J. T. (2017). e human
ventilatory response to stress: rate or depth? Phys. J. 595, 5729–5752. doi:
Toubekis, A. G., Beidaris, N., Botonis, P. G., and Koskolou, M. (2017). Severe
hypoxemia induced by prolonged expiration and reduced frequency breathing
during submaximal swimming. J. Sports Sci. 35, 1025–1033. doi:
Trevisan, M. E., Boueur, J., Soares, J. C., Haygert, C. J., Ries, L. G., and
Correa, E. C. (2015). Diaphragmatic amplitude and accessory inspiratory
muscle activity in nasal and mouth-breathing adults: a cross-sectional study.
J. Electromyogr. Kinesiol. 25, 463–468. doi: 10.1016/j.jelekin.2015.03.006
Tsukada, S., Masaoka, Y., Yoshikawa, A., Okamoto, K., Homma, I., and
Izumizaki, M. (2017). Coupling of dyspnea perception and occurrence of
tachypnea during exercise. J. Physiol. Sci. 67, 173–180. doi: 10.1007/
Valsted, F.M., Nielsen, C.V., Jensen, J.Q., Sonne, T., and Jensen, M.M. (2017).
“Strive: exploring assistive haptic feedback on the run.” in Proceedings of
the 29th Australian Conference on Computer-Human Interaction: ACM.
November 28 - December 01, 2017; 275–284.
Van Diest, I., Verstappen, K., Aubert, A. E., Widjaja, D., Vansteenwegen, D.,
and Vlemincx, E. (2014). Inhalation/exhalation ratio modulates the eect
of slow breathing on heart rate variability and relaxation. Appl. Psychophysiol.
Biofeedback 39, 171–180. doi: 10.1007/s10484-014-9253-x
Van Dyck, E., Moens, B., Buhmann, J., Demey, M., Coorevits, E., Dalla Bella, S.,
et al. (2015). Spontaneous entrainment of running cadence to music tempo.
Sports Med. Int. Open 1:15. doi: 10.1186/s40798-015-0025-9
Van Oeveren, B. T., De Ruiter, C. J., Hoozemans, M. J. M., Beek, P. J., and
Van Dieen, H. (2019). Inter-individual dierences in stride frequencies during
running obtained from wearable data. J. Sports Sci. 37, 1996–2006. doi:
Van Rheden, V., Grah, T., and Meschtscherjakov, A. (2020). “Sonication
approaches in sports in the past decade.” in Proceedings of the 15th International
Conference on Audio Mostly. September 16, 2020.
Van Rheden, V., Harbour, E., Finkenzeller, T., Burr, L.A., Meschtscherjakov, A.,
and Tscheligi, M. (2021). “Run, beep, breathe: exploring the eects on
adherence and user experience of 5 breathing instruction sounds while
running,” in Audio Mostly 2021. October 15, 2021.
Vickery, R.L. (2008). e eect of breathing pattern retraining on performance
in competitive cyclists. dissertation/thesis. Auckland University of Technology.
Vinetti, G., Lopomo, N. F., Taboni, A., Fagoni, N., and Ferretti, G. (2020).
e current use of wearable sensors to enhance safety and performance in
breath-hold diving: a systematic review. Diving Hyperb. Med. 50, 54–65.
doi: 10.28920/dhm50.1.54-65
Von Leupoldt, A., Sommer, T., Kegat, S., Baumann, H. J., Klose, H., Dahme, B.,
et al. (2008). e unpleasantness of perceived dyspnea is processed in the
anterior insula and amygdala. Am. J. Respir. Crit. Care Med. 177, 1026–1032.
doi: 10.1164/rccm.200712-1821OC
Walker, A., Surda, P., Rossiter, M., and Little, S. (2016). Nasal function and
dysfunction in exercise. J. Laryngol. Otol. 130, 431–434. doi: 10.1017/
Wallden, M. (2017). e diaphragm–more than an inspired design. J. Bodyw.
Mov. er. 21, 342–349. doi: 10.1016/j.jbmt.2017.03.013
Ward, S. A. (2007). Ventilatory control in humans: constraints and limitations.
Exp. Physiol. 92, 357–366. doi: 10.1113/expphysiol.2006.034371
Weiler, J. M., Brannan, J. D., Randolph, C. C., Hallstrand, T. S., Parsons, J.,
Silvers, W., et al. (2016). Exercise-induced bronchoconstriction update-2016.
J. Allergy Clin. Immunol. 138, 1292–1295.e36. doi: 10.1016/j.jaci.2016.05.029
Weinberger, M., and Abu-Hasan, M. (2009). Perceptions and pathophysiology
of dyspnea and exercise intolerance. Pediatr. Clin. N. Am. 56, 33–48, ix.
doi: 10.1016/j.pcl.2008.10.015
Weitzberg, E., and Lundberg, J. O. (2002). Humming greatly increases nasal nitric
oxide. Am. J. Respir. Crit. Care Med. 166, 144–145. doi: 10.1164/rccm.200202-138BC
Welch, J. F., Kipp, S., and Sheel, A. W. (2019). Respiratory muscles during
exercise: mechanics, energetics, and fatigue. Curr. Opin. Physiol. 10, 102–109.
doi: 10.1016/j.cophys.2019.04.023
Wiehr, F., Kosmalla, F., Daiber, F., and Krüger, A. (2017). “FootStriker: an
EMS-based assistance system for real-time running style correction.” in
Proceedings of the 19th International Conference on Human-Computer Interaction
with Mobile Devices and Services. September 04, 2017; 1–6.
Wojta, D., Flores, X., and Andres, F. (1987). Eect of “breathplay” on the
physiological performance of trained cyclists. Med. Sci. Sports Exerc. 19:S85.
doi: 10.1249/00005768-198704001-00509
Woorons, X., Billaut, F., and Lamberto, C. (2021a). Running exercise with
end-expiratory breath holding up to the breaking point induces large and
early fall in muscle oxygenation. Eur. J. Appl. Physiol. 121, 3515–3525. doi:
Harbour et al. Breath Tools: Breathing for Runners
Frontiers in Physiology | 24 March 2022 | Volume 13 | Article 813243
Woorons, X., Billaut, F., and Vandewalle, H. (2020). Transferable benets of cycle
hypoventilation training for run-based performance in team-sport athletes. Int.
J. Sports Physiol. Perform. 1–6. doi: 10.1123/ijspp.2019-0583 [Epub ahead of print].
Woorons, X., Lemaitre, F., Claessen, G., Woorons, C., and Vandewalle, H.
(2021b). Exercise with end-expiratory breath holding induces large increase
in stroke volume. Int. J. Sports Med. 42, 56–65. doi: 10.1055/a-1179-6093
Woorons, X., Mucci, P., Richalet, J. P., and Pichon, A. (2016). Hypoventilation
training at supramaximal intensity improves swimming performance. Med.
Sci. Sports Exerc. 48, 1119–1128. doi: 10.1249/MSS.0000000000000863
Wuthrich, T. U., Eberle, E. C., and Spengler, C. M. (2014). Locomotor and
diaphragm muscle fatigue in endurance athletes performing time-trials of
dierent durations. Eur. J. Appl. Physiol. 114, 1619–1633. doi: 10.1007/
Yamamoto, Y., Takei, Y., Mutoh, Y., and Miyashita, M. (1988). Delayed appearance
of blood lactate with reduced frequency breathing during exercise. Eur. J.
Appl. Physiol. Occup. Physiol. 57, 462–466. doi: 10.1007/BF00417994
Yonge, R. (1983). Entrainment of breathing in rhythmic exercise. Model. Control
Breath. 197–204.
Zaccaro, A., Piarulli, A., Laurino, M., Garbella, E., Menicucci, D., Neri, B.,
et al. (2018). How breath-control can change your life: a systematic review
on psycho-physiological correlates of slow breathing. Front. Hum. Neurosci.
12:353. doi: 10.3389/fnhum.2018.00353
Zelano, C., Jiang, H., Zhou, G., Arora, N., Schuele, S., Rosenow, J., et al.
(2016). Nasal respiration entrains human limbic oscillations and modulates
cognitive function. J. Neurosci. 36, 12448–12467. doi: 10.1523/
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