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ABSTRACT
Objective: The purpose of this study was to determine the feasibility of performing a larger study to determine if
training in diaphragmatic breathing influences static and dynamic balance.
Methods: A group of 13 healthy persons (8 men, 5 women), who were staff, faculty, or students at the University of
Western States participated in an 8-week breathing and balance study using an uncontrolled clinical trial design.
Participants were given a series of breathing exercises to perform weekly in the clinic and at home. Balance and breathing
were assessed at the weekly clinic sessions. Breathing was evaluated with Liebenson’s breathing assessment, static balance
with the Modified Balance Error Scoring System, and dynamic balance with OptoGait’s March in Place protocol.
Results: Improvement was noted in mean diaphragmatic breathing scores (1.3 to 2.6, P b .001), number of single-leg
stance balance errors (7.1 to 3.8, P = .001), and tandem stance balance errors (3.2 to 0.9, P = .039). A decreasing
error rate in single-leg stance was associated with improvement in breathing score within participants over the 8 weeks
of the study (–1.4 errors/unit breathing score change, P b .001). Tandem stance performance did not reach statistical
significance (–0.5 error/unit change, P = .118). Dynamic balance was insensitive to balance change, being error free
for all participants throughout the study.
Conclusion: This proof-of-concept study indicated that promotion of a costal-diaphragmatic breathing pattern may
be associated with improvement in balance and suggests that a study of this phenomenon using an experimental design
is feasible. (J Manipulative Physiol Ther 2017;40:169-175)
Key Indexing Terms: Diaphragm; Respiration; Postural Balance; Exercise; Breathing Exercises
The purpose of this preliminary study is to explore the Static Balance Assessment. The Modified Balance Error
feasibility of performing a study to measure a potential link Scoring System (SCAT3: Sport Concussion Assessment
between breathing patterns and balance. We had 2 hypotheses: Tool, 3rd ed) is a standardized, objective test used to assess
(1) breathing exercises that promote increased costodiaphrag- balance and postural stability following head trauma. 19,20
matic movement and decrease upper thoracic movement alter The Balance Error Scoring System has been reported to
breathing patterns to be more diaphragmatic in nature; and have good to excellent interrater and test-retest reliability
(2) as breathing biomechanics become more diaphragmatic in for the evaluation of healthy young adults 21 and some
nature, balance will increase correspondingly. evidence of criterion validity in young healthy athletes. 22
Subjects performed the test wearing shorts or pants
rolled up and with shoes removed. Assessors provided
METHODS scripted instructions as each subject performed a single trial
of a double-leg stance (DLS), single-leg stance (SLS), and
Design
tandem stance (TS). For the SLS, participants stood on their
This study was a prospective clinical trial using 1 cohort
nondominant foot. For the TS, the nondominant foot was in
without control. The study was conducted in Portland,
the front. Each trial was performed, with subjects’ eyes
Oregon, between April and June 2015.
closed, for 20 seconds while the examiner counted the
number of errors. Types of errors included hands lifting off
Participants iliac crests; eyes opening; a step, stumble, or fall; moving
Participants were recruited from the students, staff, and the hip into more than 30° abduction; lifting forefoot or
faculty at the University of Western States. The assessors in heel; and remaining out of the test position longer than 5
this study were four doctor of chiropractic students who seconds. Scores for each test were calculated as the number
were also enrolled in the Master of Sports Science program. of errors. If a participant committed multiple errors
Assessors were in their final year of both programs. simultaneously, only 1 error was recorded. 23 Participants
Participants were included if they were at least 21 years were told to reset and start again if they lost their balance.
old, literate in English, ambulatory, and willing to attend 8 Scores were generated by the same assessor for all
visits and complete the prescribed breathing exercises. participants each week in an attempt to improve reliability.
Participants were excluded if they had a current or previous Dynamic Balance Assessment. This was assessed using
diagnosis of attention deficit disorder or attention deficit OptoGait’s March in Place protocol (MicroGait Corp,
hyperactivity disorder, vascular disease, central nervous Mahopac, NY). 24 By marching in place, the body is
system disorder, benign paroxysmal positional vertigo, performing a dynamic movement in which balance is needed
cancer, posttraumatic stress disorder, anxiety, depression, to provide a base of support. OptoGait’s software measures
chronic pain, hypertension, congestive heart failure, or spinal flight and contact time on the left and right sides. OptoGait
stenosis. Participants who had had a concussion or brain states that as balance improves, contact time and the
injury in the previous year or a lower body injury or ear percentage difference between right and left contact times
infection that required treatment in the past month or who will decrease.
were currently or trying to become pregnant were excluded. Participants were asked to stand between the OptoGait’s
All participants had to confirm that they could perform the sensors with shoes off facing the assessor. They were read a
breathing assessment pain free and were not participating in script asking them to “march in place with a purpose, quickly,
any other balance-specific training. Participants’ blood but comfortably, for 40 seconds.” They were instructed to try
pressure and pulse were taken prior to initiating exercise to and get their knees to 90° and that they would be doing this
screen for any underlying cardiovascular risk factors. 2 times, the first time with their eyes open and the second time
This study was reviewed and approved by University of with their eyes closed. In the event that the participant
Western States institutional review board. Informed consent marched out of the testing area, the test was redone
was given by all participants prior to participation in the study. immediately. 25 This protocol has not yet been reported to
be a valid measurement of dynamic balance.
Breathing Assessment. This test was taken from a full-body
Outcome Measurements assessment of functional movement by Leibenson. 17 It was
Breathing and balance assessments were conducted used in this study as a marker to monitor response to training
before each breathing-exercise training session for 8 for conversion from apical to diaphragmatic breathing.
weeks. To improve the reliability of scoring, all assessments Breathing assessment (BA) has not been assessed for
were scripted and performed by the same evaluator every reliability but has face validity in that the mechanics that
week for each of the participants. The dynamic balance was distinguish breathing styles can be observed.
measured by a computer, but the instructions to participants Participants were asked to lay on their backs in the 90/90/
were read from a script by the same assessor every week. 90 position (hips and knees 90° flexed with feet dorsiflexed).
The following assessments were made: Their legs were supported by the assessor while their anterior
Journal of Manipulative and Physiological Therapeutics Stephens et al 171
Volume 40, Number 3 Effect of Breathing Type on Balance
inferior rib cage was brought into a caudal position, supporting and crocodile breathing; progression 4: seated breathing and
their thoracolumbar junction. They were asked to maintain that 90/90/90 breathing; progression 5: Seated breathing with
position while breathing predominantly with their diaphragm. Theraband and 90/90/90 breathing with belt.
They were cued to “fill” their inferior abdomen and posterior Supine Breathing. Patients were instructed to lay supine,
chest wall. Palpatory cues were used by the assessor. knees bent with arms wherever it felt comfortable. They were
Participants were then asked to support their legs in the 90/ cued to focus on breathing with their diaphragm, the breath
90/90 position while the assessor released support. Breathing filling into their lower abdomen and posterior chest wall. They
score were based on the patient’s ability to maintain breathing were cued to keep their ribs depressed and thoracolumbar
biomechanics and posture after their legs had been released. junction supported and to keep their shoulders and neck relaxed.
Scores ranged from 0 to 3, where 0 indicates the Crocodile Breathing. Patients were instructed to lay prone
participant is having pain performing the test (and will no with their hands in a diamond shape supporting their
longer be eligible to participate in this study); 1 indicates the forehead. They were cued to try and focus on pushing their
participant is not able to complete the exercise with proper ribs out laterally and trying to breathe all the way down to the
form; 2 indicates the participant is able to complete the sacrum. During meetings, pressure was added to their sacrum
exercise but with compensation; and 3 indicates the by the examiner, with permission, to help cue this.
participant is able to complete the exercise with proper form. Seated Breathing. Participants were seated on a hard
Participants scored a 1 if they had paradoxical respiration surface with their knees, hip, and ankles all at 90°. They were
(chest moving inward with inspiration), were unable to told to sit tall, as if a “string was pulling them up from the top
stabilize their ribs when cued, or were unable to stabilize their of their head,” while maintaining all previously discussed
ribs when released. Participants scored a 2 if they had chest breathing cues: preventing lower rib flair, breathing deeply,
breathing predominately on inhalation or a lower rib cage that and relaxing their shoulders, neck and arms.
did not widen laterally, or if release of their legs caused 90/90/90 Breathing. Participants were returned to the 90/90/
anterior inferior rib cage flair. This scale has not been tested 90 assessment position, but were asked to hold their legs
for reliability, validity, or sensitivity to change. while maintaining all previously discussed breathing cues:
Participant Monitoring. Participants were asked to report controlling their ribs and thoracolumbar junction, breathing
on their activity levels in the 6 months prior to initiating deeply and relaxing their shoulders, neck, and arms.
the study, as well as their physical activity outside of the Breathing With Theraband. A Theraband was added around
study while completing the breathing exercises. Participants the lower ribs to help promote lateral excursion. It was applied
completed daily homework logs and returned them at the end to progress supine, crocodile, or seated breathing exercises.
of the 8 weeks to confirm they had completed the required Breathing With Belt. A Theraband was laid flat on the
exercises. In the final interview, participants were also asked ground to look like a belt. It was added in the final exercise
to give their subjective impressions of the benefits of the progression to help cue caudal rib position. With all the cues
program on their physical activities. from previous exercises, a Theraband or belt was placed
under the patient’s thoracolumbar junction. The patient was
instructed to not let the examiner pull the belt away. At home,
Intervention patients were instructed to tie the Theraband around a table or
Participants were assigned 2 exercises a week. They were chair and leave tension in it to simulate the effect of pulling.
asked to complete each breathing exercise for 5 minutes, twice
daily, for a total of 20 minutes a day at least 5 days per week.
Instruction and feedback were given to participants on Statistical Analysis
assessment days. A YouTube video of their prescribed The primary analysis consisted of Friedman’s analysis of
exercises was emailed to them weekly. All exercises were variance for nonparametric repeated-measures data to test
prescribed in a sequential order and were dependent on the whether there were any differences between scores over the
patient's ability to maintain proper form. All participants 8 weeks of the study. The analysis was conducted separately
started at progression 1. They were asked to record their for breathing assessment, SLS, and TS scores only. This was
homework in a provided log. Participants were instructed to because no errors were recorded for any baseline or follow-up
do exercises for only as long as they could maintain proper data for the DLS, and equipment failure was suspected for the
posture. If they were not able to hold the posture for the full dynamic balance measurements. A nonparametric analysis
5 minutes, they were instructed to take breaks and work up to was chosen to avoid distribution concerns in smaller samples.
the 5 minutes. In a secondary analysis, the linear relationship between the
Five exercise progressions were designed for the purposes 3 variables and time was determined by regression of each of
of this study: progression 1: supine breathing and crocodile the variables on time, using generalized estimating equations
breathing; progression 2: supine breathing with Theraband (with an exchangeable correlation structure) to account
(The Hygenic Corp, Akron, OH) and crocodile breathing for correlation of variables within subjects. The 2 balance
with Theraband; progression 3: supine breathing with belt variables were then regressed on the breathing score using
172 Stephens et al Journal of Manipulative and Physiological Therapeutics
Effect of Breathing Type on Balance March/April 2017
7.5 2.6
6 2
5.5 1.8
5 1.6
4.5 1.4
4 1.2
3.5 1
Week 1 Week 2 Week 3 Week 4 Week 5 Week 6 Week 7 Week 8
Mean Single Leg Stance Balance Errors Mean Breathing Score (0-3)
Fig 1. Mean single-leg stance errors versus mean breathing scores over 8-week breathing intervention.
3.5 2.6
Mean Tandem Stance Balance Errors
2.4
3
2 1.8
1.6
1.5
1.4
1
1.2
0.5 1
Week 1 Week 2 Week 3 Week 4 Week 5 Week 6 Week 7 Week 8
Fig 2. Mean tandem stance errors versus mean breathing scores over 8-week breathing intervention.
diaphragmatic breathing style suggests increased movement Possible explanations for the increase in balance include,
through the lateral inferior ribs and abdomen. 16 As there is but are not limited to, the following reasons. There may
likely increased movement in the deep abdominal muscula- have been an increase in muscle firing, proprioception, and
ture, it is reasonable to assume that there is also increased strength through the diaphragm and deep core musculature.
muscle firing and proprioception of the deep core musculature These changes may have been associated with a diaphrag-
and diaphragm. Furthermore, it is not unlikely that increased matic breathing pattern or breathing exercised independent
strength would have resulted from increased muscle firing of breathing style. Alternatively, there may have been a
over an 8-week period. learning effect from the weekly balance testing over the
The improvement in balance was indicated by a decrease in course of the study.
balance errors in the SLS; such improvement was not observed We believe that the breathing exercises and corresponding
for the TS (Table 2). Our findings suggest that the SLS is a increase in diaphragmatic breathing style may have increased
promising outcome measure for future studies. However, we the strength of the diaphragm and deep core musculature, and
believe there was a floor effect in TS measurements that that this increase in strength and proprioception may have
precluded demonstrable improvement of performance in the contributed to the increase in balance measured. However,
study population. without control groups, we were unable to discern the effects
174 Stephens et al Journal of Manipulative and Physiological Therapeutics
Effect of Breathing Type on Balance March/April 2017
Table 3. Correlation of Balance Scores With Breathing Score a and TS may also be more impressive for various clinical
Week Single-Leg Stance Tandem Stance conditions. Finally, this study could cast no light on the
1 0.07 0.11 usefulness of dynamic balance testing because of suspected
2 –0.28 –0.12 equipment failure, and we could not find any empirical data to
3 0.02 0.00 support the OptoGait protocols.
4 –0.03 0.06 Despite these limitations, the relationship between breathing
5 –0.05 –0.17
and static balance is intriguing and worthy of pursuit with
6 –0.20 0.09
7 –0.23 –0.36 more sophisticated study designs. As these exercises require
8 –0.42 0.02 very limited supplies and can be done almost everywhere,
a
Spearman’s rank-sum correlation coefficient. P N .05.
we believe that they could benefit a large portion of the
population. It would be also be interesting to compare the
effects of breathing exercise with traditional core exercises on
sports performance. In addition to benefiting a healthy athletic
of balance training on diaphragmatic breathing from other population, this information may be helpful for populations
causes such as learning effect and increase in breathing that are at high risk for falls.
musculature independent of breathing style.
During the final assessment participants stated that they
had enjoyed doing the breathing exercises and had noticed
improvements throughout other aspects of their lives that they CONCLUSION
associated with the changes in their breathing patterns. This preliminary study gives proof-of-concept evidence
Benefits included feeling more balanced rock climbing, that there may be a relationship between breathing and
having less low back pain with long road bike rides, and balance. Further research using experimental design needs
feeling stronger while Olympic lifting. The effects of to be conducted to investigate the link between breathing
participation in a research study could not be distinguished patterns and balance. If verified, there might be applications
from the effects of the exercise program on perceived benefits. to sports performance in the future.
Limitations
Ours was a small, uncontrolled clinical trial, and all the FUNDING SOURCES AND CONFLICTS OF INTEREST
usual limitations of such studies apply. The most important
concern is that the relationship observed between balance Theraband donated the Theraband resistance bands for
and breathing was confounded by the possibility of learning this study. No funding sources or conflicts of interest were
effects from the weekly balance testing over the course of reported for this study.
the study. Also, breathing data were collected only once per
week, so the extent of change in breathing pattern could not
be clearly ascertained.
Another limitation is that the BA used to monitor breathing
CONTRIBUTORSHIP INFORMATION
style has not been fully validated. However, the linear Concept development (provided idea for the research):
association of BA with the number of training sessions R.J.S., J.A.S.
(time) gives preliminary evidence for test responsiveness. The Design (planned the methods to generate the results):
association between BA and balance over time supports the R.J.S., J.R.E., J.A.S., A.W.
construct validity for monitoring a breathing training program, Supervision (provided oversight, responsible for organiza-
because it is consistent with the underlying hypothesis tion and implementation, writing of the manuscript): W.L.M.
(construct) that change in breathing style can improve balance. Data collection/processing (responsible for experiments,
We did not specifically screen for stroke and transient patient management, organization, or reporting data): R.J.S.,
ischemic attack, nor did we ask about medication in general W.L.M., J.R.E., J.A.S., A.W.
and those that could affect balance in particular. However, Analysis/interpretation (responsible for statistical analysis,
participants were screened for a history of vascular disease evaluation, and presentation of the results): R.J.S., M.H.
and central nervous system disorders. The participants were Literature search (performed the literature search): R.J.S.,
also young, active, healthy individuals, so that it was unlikely J.R.E., J.A.S.
they were on medications that could affect balance. Writing (responsible for writing a substantive part of the
Our findings in a healthy population should also not be manuscript): R.J.S., W.L.M., M.H.
generalized to clinical populations. In particular, the DLS, Critical review (revised manuscript for intellectual content,
useless here because it was completely error free, may provide this does not relate to spelling and grammar checking):
valuable information for clinical patients. Findings for the SLS R.J.S., M.H.
Journal of Manipulative and Physiological Therapeutics Stephens et al 175
Volume 40, Number 3 Effect of Breathing Type on Balance