Breathing Dysfunction and Screening
Breathing Dysfunction and Screening
Breathing Dysfunction and Screening
ABSTRACT
Introduction: Dysfunctional breathing (DB) has been linked to health conditions including low back pain and neck
pain and adversely effects the musculoskeletal system. Individuals with DB often have decreased pain thresholds and
impaired motor control, balance, and movement. No single test or screen identifies DB, which is multi-dimensional,
and includes biochemical, biomechanical, and psychophysiological components. Several tools assess and test for DB,
but no screen exists to determine whether additional testing and assessment are indicated.
Purpose/Background: The purpose of this study was to develop a breathing screening procedure that could be uti-
lized by fitness and healthcare providers to screen for the presence of disordered breathing. A diagnostic test study
approach was utilized to establish the diagnostic accuracy of the newly developed screen for DB.
Methods: A convenience sample of 51 subjects (27 females, 27.0 years, BMI 23.3) were included. To test for DB
related to the biochemical dimension, end-tidal CO2 (ETCO2) was measured with a capnography unit. To test for DB
related to biomechanical dimension, the Hi-Lo test was utilized. To test for DB related to the psychophysiological
dimension, the Self Evaluation of Breathing Symptoms Questionnaire (SEBQ) and Nijmegen questionnaires were
utilized. Potential screening items that have been shown to be related to DB in previous research and that could be
performed by non-health care personnel were utilized to create the index test including activity level, breath hold
time (BHT), respiration rate, and the Functional Movement Screen (FMS™).
Results: There were no strong correlations between the three measures of DB. Five subjects had normal breathing,
14 failed at least one measure, 20 failed at least two, and 12 failed all three. To develop screening items for each
dimension, data were examined for association with failure. BHT and a four-item mini-questionnaire were identified
as the most closely associated variables with failure of all three dimensions. A BHT of <25 seconds and four questions
were combined and yielded a sensitivity of 0.89 (0.85-0.93) and a specificity of 0.60 (0.18-0.92) for clinical identifica-
tion of DB.
Conclusion: Easily obtained clinical measures of BHT and four questions can be utilized to screen for the presence
of DB. If the screen is passed, there is an 89% chance that DB is not present. If the screen is failed, further assessment
is recommended.
Level of Evidence: 2b
Key Words: Breath holding, disordered breathing, hypocapnia, sensitivity
CORRESPONDING AUTHOR
Kyle Kiesel
1
University of Evansville, Evansville, IN, USA Professor of Physical Therapy
2
Director of Performance, St. Louis Cardinals, St. Louis, MO, University of Evansville
USA 1800 Lincoln Avenue
The Institutional Review Board at the University of Evansville Evansville, Indiana 47722
approved this study
Funding provided through the Ridgway Student Research USA
Award from the University of Evansville E-mail: [email protected]
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 774
DOI: 10.16603/ijspt20170774
INTRODUCTION lumbar multifidus muscles as the posterior border.16
Dysfunctional breathing (DB) is a commonly occur- The function of the inner core is both physiological
ring condition in the general population. It is esti- and mechanical, its main role is to provide the mus-
mated that as high 50-80% of adults have some level cle activation required to sustain respiration, conti-
of DB.1,2 The term DB has been created to identify nence, and segmental spinal stabilization.16 The inner
those individuals who display divergent breathing core receives ongoing subconscious input from the
patterns and have breathing problems that cannot central nervous system (CNS), which automatically
be attributed to a specific medical diagnosis, such maintains respiration,9 continence, and segmental
as asthma.3 Normal breathing, considered to be stabilization in anticipation of a spinal perturbation.
diaphragmatic breathing, includes synchronized This is a highly automated, delicately functioning
motion of the upper rib cage, lower rib cage, and system with the ability to simultaneously regulate
abdomen and requires proper use of the diaphragm.4 physiological functions (respiration and continence)
while allowing for control of translation and shear
DB has been linked to a number of common chronic
forces (segmental stabilization) between spinal seg-
health conditions such as low back pain (LBP),5,6
ments during both low and high load activities.17
neck pain,7 anxiety,8 and depression.2 It has been
reported that approximately 50% of individuals with Core muscle dysfunction, including atrophy and
LBP9 and 83% of individuals with anxiety demon- abnormal activation, has been linked to many com-
strate some form DB.10 A wide-range of individuals mon musculoskeletal problems including LBP,9 ACL
likely possess some level of DB, and currently there injury,18 neck pain,7 and an overall increased injury
is no widely accepted screen or index test that exists risk.19 Subjects with DB have been shown to dem-
to identify these individuals.2 Identification and sub- onstrate concurrent core dysfunction including
sequent intervention for those with DB may be an altered postural responses during limb movements5
important missing component of musculoskeletal and altered inner core muscle activation.9,13 Further,
health care as DB is known to be associated with normal breathing has been described as forming the
many common musculoskeletal conditions and may foundation for all movement patterns12 while DB
also be a risk factor for the development of muscu- has been shown to be related to clinical measures
loskeletal dysfunction.11 DB may be an important of dysfunctional movement with subjects with DB
factor to consider relative to the prevention and scoring lower on the Functional Movement Screen
recurrence of movement oriented dysfunction12 (FMS™) than those with normal breathing.11
and, therefore, may have a place in conditioning and
It is thought that core muscle function is altered in
fitness programs as well.
those with DB in a compensatory manner. The phys-
The primary reason to screen for DB in individuals iological drive to maintain respiration leads to core
who are physically active or currently have muscu- muscles functioning to assist breathing to a greater
loskeletal pain is its close relationship with normal extent than during normal functional breathing.16,20
core function.9,13 To better understand core structure This relationship between normal breathing and
and function as it relates to DB, it is important to note core function is so intimately linked that perhaps
the core can be divided into two basic anatomical the most fundamental assessment of core function
units,14 the outer core and the inner core. The outer should start with some type of breathing screen or
core is composed of large multiarticular muscles such test. Core exercises are often prescribed as part of
as the erector spinae, rectus abdominis, and external rehabilitation, fitness, and strength and conditioning
obliques. The function of the outer core is to provide programs with no attention paid to breathing func-
postural stability, resist external load, produce move- tion. It may be desirable for fitness and health care
ment, and transfer rotational energy for activities professionals who prescribe core exercises to uti-
such as throwing and hitting.15 The inner core can be lize a breathing screen to determine if subsequent
conceived as a cylinder made up of the pelvic floor breathing pattern assessment and treatment is nec-
as the base, the diaphragm as the top, the transverse essary in conjunction with planned rehabilitation,
abdominis muscle as the anterior border, and the training, or conditioning.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 775
There is currently no accepted screening procedure breathing strategy at times; however, the system
to identify if a person may have DB and, therefore, does have the ability to function in a normal man-
requires further testing and assessment. Research ner. In such cases, measures of DB can often appear
has shown that DB is multi-dimensional, calling normal during routine clinical testing. Self-reported
for a variety of tests needed for an accurate diag- questionnaires may be useful capture this dimension
nosis.11 Recently, researchers have identified the of DB and include the Nijmegen Questionnaire,27
three most common dimensions or categories of DB and the more recently developed Self Evaluation
which include the biochemical, biomechanical and of Breathing Symptoms Questionnaire (SEBQ). The
psychophysiological dimensions.21 It has been sug- SEBQ was developed, in part, to assess respiratory
gested that any comprehensive assessment for DB symptoms and breathing behaviors reported to be
should include tools that capture all three of these associated with DB for individual who may not dem-
dimensions as they are often found to be indepen- onstrate consistent breathing dysfunction in the bio-
dent from each other. mechanical or biochemical dimensions.21
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 776
METHODS outward direction. The scoring process was as fol-
Subjects: A convenience sample of 51 individuals, lows: Is the upper chest dominant? If yes scores as
including 27 females, (26.5 years, BMI 22.7) and 24 dysfunctional and stop, if no continue. Is the pattern
males (28.3 years, BMI 24.9) consented for participa- paradoxal? If yes score as dysfunctional and stop, if
tion in this study which was approved by the Institu- no continue. Is diaphragm dominant? (greater vol-
tional Review Board at the University of Evansville. ume and diaphragmatic movement is first), if yes
Data for this prospective diagnostic test study were score as functional, if no score as dysfunctional.
collected in a University lab setting from September The Hi-Lo test reliability has been reported by oth-
to November 2015. Potential subjects were excluded ers as acceptable,23 and the researchers in this study
if they were currently participating in rehabilitation achieved 88% agreement with a Kappa = .75 on 43
for any disorder, if they had a neurological or car- subjects assessed during data collection.
diovascular comorbidity known to impair musculo-
skeletal function, or if they could not read or speak Biochemical Dimension
English. To determine if DB was present, reference To determine if a subject had a biochemical breath-
measures were obtained for each of the three dimen- ing problem, capnography was utilized as the ref-
sions of DB. The data collection process was done erence measure. Capnography is a measurement
in the same manner at each data collection session taken via nasal cannula to determine ETCO2. The
with the same three testers performing the same average resting value over a three minute data col-
tests each time in the same order. The reference lection period was utilized to obtain the measure,
measures and the potential screening tests mea- and the standard value of < 35 mmHg was utilized
sures were combined in a manner that was designed as the cut-off for dysfunction.24-26 The capnography
to be as efficient as possible and allowed for blinding unit (CapnoTrainer, Better Physiology Ttd. Boulder,
of the testers to the results of the reference mea- CO, USA) was calibrated according to the manufac-
sures. After consent was obtained, resting capnog- turer recommended procedure prior to each data
raphy data was collected as subjects completed the collection session. Respiration rate in breaths per
questionnaires. Next, the Hi-Lo test was performed, minute was calculated from the capnography data.
followed by the BHT tests and then, lastly, the FMS™
was performed. Psychophysiological Dimension
To address the psychophysiological dimension, two
Reference Measures separate breathing questionnaires were adminis-
Biomechanical Dimension tered. The Nijmegen Questionnaire is a 16-item
To determine if a subject had a biomechanical questionnaire developed in the 1980’s to iden-
breathing problem, the Hi-Lo Breathing Assess- tify patients who have breathing dysfunction that
ment29 was utilized as the reference. The Hi-Lo is emphasizes relationships with common diseases.
a manual assessment to determine if a subject is A cut score of ≥ 22 on the Nijmegen was utilized
in a normal diaphragmatic breathing pattern or if to define DB.30 The Self-Evaluation of Breathing
they are in an abnormal pattern. It was performed Questionnaire (SEBQ), Version 331 is a question-
in the sitting position with the tester standing or naire that includes 25 questions to determine self-
kneeling at the front and slightly to the side of the perception of breathing dysfunction. Test-retest
subject. The tester placed one hand on the subject’s reliability has been shown to be high32 and a cut
sternum and one hand on their upper abdomen to score of ≥ 25 on the SEBQ was utilized to define DB
determine whether thoracic or abdominal motion for this study. The SEBQ is a new tool, and there is
is dominant during breathing. Assessment for par- no established cut-score confirmed in the literature
adoxical breathing is also performed by determin- to define those with this dimension of breathing
ing if the abdomen moves in a direction opposite to dysfunction. Expert opinion suggests a score of 25
the thorax during breathing; this is evident during as an appropriate cut-score. All subjects completed
inhalation if the abdomen moves toward the spine, both questionnaires and scoring above the estab-
and during exhalation if the abdomen moves in an lished cut-score on either questionnaire was used
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 777
as the reference measure for the psychophysiologi- that those with lower activity levels would be more
cal dimension. likely to have DB.
The FMS™ was used as a measure of movement dys-
Screening Tests
function. Previous research has demonstrated that
Clinical tests that the researchers hypothesized may
those scoring lower on the FMS™ (more dysfunc-
be associated with DB were also performed. Tests
tional movement) also had a greater tendency to
administered included those that were most closely
demonstrate signs of DB.11 In the research, Bradley
associated with DB from the current literature. Addi-
and Esformes demonstrated that subjects who scored
tionally, each test had to be easily obtained by a non-
lower on the FMS™ were more likely to demonstrate
healthcare provider so the screen could be employed
an abnormal biomechanical breathing pattern (upper
in a fitness setting.
chest breathing) and more likely to be hypocapnic,
Breath hold time (BHT) was measured by testing demonstrating significantly lower ETCO2 values.
the functional residual capacity, also known as the These findings were present both when the compos-
controlled pause method which is a measure of how ite score with a cut point of ≤ 14 on the FMS™ was
long a subject can hold their breath starting at the utilized to define movement dysfunction and when a
end of a normal exhale until first involuntary mus- “pass/fail” approach (pass = no 0’s and no 1’s, fail =
cle activity was noted by the tester. This BHT test is any score of 0 or 1) was utilized to define movement
described by Courtney and Cohen33 to be the most dysfunction. The FMS™ is a reliable35-41 (ICC val-
reproducible method because involuntary motion of ues ranging from 0.76-0.90 and Kappa values from
the respiratory muscles has been found to be more 0.70-1.0) movement-screening tool created to rank
of a consistent measure of breaking point of breath basic movement patterns. The FMS™ includes seven
holding than the self-report of the sensation of the movements: overhead deep squat, hurdle step, inline
urge to breathe, which is an alternative method to lunge, shoulder mobility, active straight leg raise,
assess BHT. The researches measured inter-tester trunk stability pushup, and rotary stability. Each of
reliability on BHT between two testers and found these patterns is graded on a 0-3 ordinal scale where
the ICC3,2 = 0.88 (0.78-0.93). BHT has been shown 0 represents pain with the movement, 1 represents
to be reduced in those with DB, and it has been sug- dysfunctional movement, 2 represents acceptable
gested that reduced BHT may indicate problems in movement, and 3 represents optimal movement.
respiratory control that result in DB.33,34 The BHT
STATISTICAL METHODS
test was performed with the subject in sitting. They
The first step was to dichotomized subjects accord-
were instructed to sit quietly and breathe normally,
ing to their performance on the reference tests for
then, at the end of a normal exhalation, to pinch
DB. Subjects who scored below the stated cut-score
their nose and hold the breath. The time was started
on one or more of the reference tests were classified
when the subject pinched the nose and was stopped
as having DB, and those above the cut score on each
at the first involuntary movement of the respiratory
of the reference tests were classified as having nor-
muscles or when the subject unplugged the nose, as
mal breathing. Next, the data were explored to help
determined by the tester.
determine what index tests should be included as
Respiration rate (RR) was measured in breaths per a screen for DB. One-way ANOVA’s were utilized to
minute. Higher than normal RR have been shown to determine if there were any significant differences
be associated with DB.22 The RR data was obtained between subjects who were classified as DB com-
from the capnography unit data output. pared to those who were not on the clinical tests and
measures obtained to create the index test. The clini-
Activity level was measured using a standard ques- cal tests and measures included activity level, breath
tionnaire. The questionnaire, similar to the Tegner hold time, respiration rate and the FMS™. Next, 2x2
Activity Scale, is scored from a high of 10 (competitive contingency tables and routine diagnostic test statis-
sports) to a low of 1 (sedentary). The questionnaire tics were utilized to test different combinations of the
can be found in Appendix 1. It was hypothesized measures with the goal of identifying those measures
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 778
that would yield the greatest sensitivity relative to an Activity Level
individual subject’s probability of being positive on There was a difference in activity level between
any of the 3 dimensions of DB as described. those who passed (6.78) and failed (4.81), p < 0.01,
the Hi-Lo test. There was a difference in activity
RESULTS level between those who passed (5.53) and those
Five subjects demonstrated normal breathing, 13 who failed (4.25), p = 0.02, the questionnaires. No
failed at least one measure, 21 failed at least two, difference in activity level was found between those
and 12 failed all three. There were no correlations who were above or below the normative value for
between the three measures of DB. ETCO2 of 35 mmHg (p = 0.83) (Tables 1-3).
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 779
Table 4. Mean, standard deviation and ANOVA results between subjects in each dysfunctional
breathing dimension(s) and clinical tests hypothesized to be associated dysfunctional breathing.
Breath Hold Time Table 5. Results from using Pass/Fail on the FMS™
There was not a significant difference in BHT only as a potential screen to predict those with
between those who passed (25.53 seconds) and dysfunctional breathing.
failed (20.88 seconds) the Hi-Lo (p = 0.10). There
were no significant differences in BHT or ETCO2
between those who passed or failed the question-
naires (Tables 1-3).
Functional Movement
There was a difference in composite FMS™ scores
between those who passed (16.0) and failed (13.5)
the Hi-Lo (p < 0.01). There was a difference in
composite FMS™ scores between those who passed
(14.41) and failed (13.5) the questionnaires (p = 13), at least two positive tests (n = 21) and all three
0.03). No difference in composite FMS™ scores was positive tests (n = 12) (Table 4).
found between those above or below the normative
value for ETCO2 of 35 mmHg (p = 0.47) (Tables 1-3). The only clinical test that related in some manner to
When the FMS™ was considered from a pass/fail per- all three dimensions of DB was the FMS™. Although
spective (fail = any 1’s or 0’s), there was a difference a correlation exists between lower scores on the
in ETCO2 between those who passed (36.59 mmHg) FMS™ and DB, when tested as a screen for DB using
and those who failed (33.87 mmHg) the FMS™ (p = the FMS™ Pass/Fail criteria only, the results yielded
0.03). a low sensitivity of 0.52 (Table 5).
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 780
Because BHT of <20 seconds has been described in often scored at the higher levels of dysfunction. The
the literature as a clinical measure related to those SEBQ is scored on a four-level ordinal scale (0- never/
with DB, it was tested alone as a possible screen at not true at all; 1- occasionally/a bit true; 2- frequently-
two different cut points. When using BHT alone with mostly true; and 3- very frequently/very true) so any
a 20 second cut-off the sensitivity was 0.54 (0.49-0.58) question from the SEBQ scored as a 2 or 3 was utilized.
and specificity was 0.60 (0.18-0.92) (Table 6). Then The Nijmegen is scored on a similar five-point ordinal
the cut score of BHT at 25 seconds was assessed, and scale but it is scaled 0-4 (0- Never, 1- Rare, 2- Sometimes,
the sensitivity improved to 0.74 (0.69-0.77) (Table 7). 3- Often, and 4- Very Often) so any question scored as
a 3 or 4 was utilized. Frequency counts of those ques-
The BHT cut score of 25 seconds improved the sen- tions that subjects most often scored at these higher
sitivity but there were still a fairly high number levels of dysfunction were calculated and it was deter-
of false negatives, 12 subjects that were above the mined that SEBQ questions #5 and #25 and Nijmegen
cut-score on the BHT of 25 seconds but were still questions #2 and #14 were the most important ques-
diagnosed by the reference as having at least one tions to ask to help to identify those who have some
dimension of DB present. level of DB. Those subjects who answered at least one
of the four questions at this higher level, did have a
Next, the data from the questionnaires were analyzed
statistically significant relationship, Chi-Square = 0.03
to determine if adding in one or more questions could
(see Appendix 2). Because of this significant relation-
help to strengthen the proposed breathing screen.
ship, a mini-questionnaire was created that consisted
Each question from the questionnaires was investi-
of these four questions and added this to the 25 sec-
gated by identifying those questions that were most
ond BHT cut-off to see if the sensitivity improved with
the addition of the questions. With the combination of
Table 6. Results from using only the
breath hold test (BHT) <20 seconds as a the BHT cut-score of 25 and the mini-questionnaire
potential screen to predict those with DB. as the reference test, the sensitivity increased to 0.89
(0.85-.093) with LR- = 0.18 and a specificity of 0.60
(0.18-0.92) with LR+ = 2.33 (Table 8).
DISCUSSION
In this study, four questions and a breath hold time
test, used in combination, were found to be highly
sensitive to identify those with some dimension of
dysfunctional breathing. Only tests that could be
performed by non-healthcare personnel were con-
sidered, to allow the screen to have utilization in fit-
ness applications as well as the rehabilitation fields.
When screening for a possible measureable disorder,
Table 7. Results from using the breath hold time
(BHT) of < 25 as a potential screen to predict those
with dysfunctional breathing. Table 8. Results for the final screen for
dysfunctional breathing including breath hold
time of <25 seconds and/or any one question
positive from the mini-questionnaire.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 781
the tool used should be highly sensitive, that is, when if any, are present. These data are in agreement with
the screen is negative you are fairly confident that Bradley11 as well where they showed a relationship
the disorder is not present. It is important to real- between two of the three dimensions of DB but that
ize when the results of a highly sensitive screen are all three were not closely correlated, again suggest-
positive, it may not confirm the disorder, rather, it ing the need to assess for all three dimensions. The
suggests further testing or assessment is warranted. current study did show a relationship between AL
It is recommended that in those individuals, either and two of the three dimensions, biomechanical and
fitness or rehabilitation clients who are positive on breathing symptoms. The BHT was not significantly
this screen, further testing and assessment for DB be correlated with any dimension of DB from a univari-
performed by a qualified healthcare provider. ate perspective, but did contribute to the final screen.
There is no standardized and well-accepted clini- The results from the current study were similar to
cal assessment for DB. A comprehensive review by Bradley11 in that we both showed a relationship
CliftonSmith and Rowley42 stated that the lack of a between being a predominately thoracic breather
definitive assessment tool makes diagnosing breath- and having poor movement. While Bradley reported
ing disorders difficult. They suggest that a compre- a correlation between lower ETCO2 and lower FMS™
hensive assessment should include a wide variety of scores, the data from this study was analyzed differ-
measures including an accurate medical history and ently. When the FMS™ was considered as a pass/fail
understanding of the subjects musculoskeletal status, variable, there was a relationship with lower ETCO2
a visual and hands on assessment of breathing and and failing the FMS™, but when the FMS™ was ana-
muscle status, self-reported questionnaires, a breath- lyzed as a continuous variable there were not differ-
ing hold time, peak expiratory flow rate and pulse ences in FMS™ scores between those above or below
oximetry. Additionally, spirometry and capnography the normative value for ETCO2 of 35 mmHg (p =
may be used if available. As the awareness of DB 0.47). Because the FMS™ mean scores for most popu-
grows there will be a need to standardize assessment lations have a small range, normally between 13-15
tools for both rehabilitation and fitness settings. on the composite score, and the composite score in
and of itself may not be that useful, the recommen-
Several authors have demonstrated that breath- dation is to consider FMS™ information on a pass/
ing re-training programs are effective,43-45 but the fail basis as much as possible. One can conclude an
outcome tools utilized and the populations stud- individual failing the FMS™ is more likely to be a tho-
ied vary widely making it challenging to become racic breather and have a lower ETCO2. Additionally,
widely accepted in the medical literature. It would scoring lower on the FMS™ from a composite per-
be ideal to standardize a breathing screen, tests, and spective will more likely be associated with failing
an assessment to better understand which interven- the SEBQ, demonstrating the presence of breathing
tion approach is most effective for each type of DB. symptoms. But, taken together, using only the FMS™
To do this will require an approach similar to the score to screen for DB yielded a sensitivity of only
treatment based classification system utilized for 0.52 and, therefore, is not recommended. In this case,
patients with acute low back pain where clinically although the FMS™ had a statistical relationship with
captured data allows for the creation of diagnostic DB, it yielded a low sensitivity because there were
categories.46,47 Establishing diagnostic categories of 22 subjects who passed the FMS™, but did have some
DB may serve to clarify the complex nature DB and dimension of DB. These were false negatives that
help to standardize future research efforts. lowered the sensitivity. From these data, the FMS™
alone should not be used as a screen for breathing.
Data from this study are similar to those of Courtney
et al21 who demonstrated that DB has three distinct While there was a univariate trend in lower BHT
dimensions and that they often do not correlate well, being related to the biomechanical dimension, when
suggesting a need to screen for the condition of DB BHT was applied with a cut score of 25 seconds,
overall and then have further assessments that can the sensitivity strengthened substantially; along
be performed to identify which dimension(s) of DB, with adding in the mini-questionnaire, all three
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 782
dimensions of DB were captured. A breath hold 5. Kolar P, Sulc J, Kyncl M, et al. Postural function of
time of 20 seconds has been proposed as a cut-off to the diaphragm in persons with and without chronic
identify those with hyperventilation syndrome. Jack low back pain. J Orthop Sports Phys Ther.
2012;42(4):352-362.
et al34 reported a mean BHT of 20 (SD 12) seconds
6. Smith MD, Russell A, Hodges PW. Disorders of
in individuals with known breathing dysfunction
breathing and continence have a stronger
which compares closely to the mean of 21.9 (SD 9.3) association with back pain than obesity and physical
seconds from the current study in those who were activity. Aust J Physiother. 2006;52(1):11-16.
considered positive on any one or more of the refer- 7. McLaughlin L, Goldsmith CH, Coleman K. Breathing
ence tests used for DB. evaluation and retraining as an adjunct to manual
therapy. Man Ther. 2011;16(1):51-52.
A limitation to this study is that the sample size is
8. Hagman C, Janson C, Emtner M. A comparison
considered small to establish a new screening tool. between patients with dysfunctional breathing and
The next step is to perform a validation study of patients with asthma. Clin Respir J. 2008;2(2):86-91.
the breathing screen with another sample of sub- 9. Whittaker JL. Ultrasound imaging of the lateral
jects. Additionally, only five subjects passed all the abdominal wall muscles in individuals with
tests performed for DB indicating a high incidence lumbopelvic pain and signs of concurrent
(90%) of DB in this population, which is higher than hypocapnia. Man Ther. 2008;13(5):404-410.
expected. The threshold of 25 seconds is challenging 10. Courtney R, Cohen M, van Dixhoorn J. Relationship
to achieve and it will take further research in more between dysfunctional breathing patterns and ability
to achieve target heart rate variability with features
diverse samples to determine if this threshold can of “coherence” during biofeedback. Altern Ther
be validated. Also, the activity level questionnaire Health Med. 2011;17(3):38-44.
utilized in the current research is a modified version 11. Bradley H, Esformes J. Breathing pattern disorders
of the Tegner Activity Scale.48 Although similar, this and functional movement. Int J Sports Phys Ther.
tool has not been validated in the literature to date. 2014;9(1):28-39.
12. Lewit K. Relation of faulty respiration to posture,
CONCLUSION with clinical implications. J Am Osteopath Assoc.
Easily obtained clinical measures of BHT and four 1980;79(8):525-529.
questions can be utilized to screen for the presence of 13. Hodges PW, Sapsford R, Pengel LH. Postural and
DB. If the screen is passed, there is a 89% chance that respiratory functions of the pelvic floor muscles.
Neurourol Urodyn. 2007;26(3):362-371.
DB is not present. If the screen is failed, further assess-
14. Kiesel KB, Knox T. Core stability for the running
ment is recommended to determine if DB breathing is
athlete. In: O’Connor F, Wilde R, eds. Running
present and if so, which dimension is affected. Addi- Medicine. 2nd ed. Montaray, CA: Healthy Learning;
tionally, these findings help to validate previous find- 2014:1801-1825.
ings that link movement and breathing dysfunction. 15. Kiesel K, Burton S, Cook E. Mobility screening for
the core. Athl Ther Today. 2004;9(5):42-45.
REFERENCES 16. Hodges PW, Gandevia SC. Changes in intra-
1. Courtney R, van Dixhoorn J, Greenwood KM, et al. abdominal pressure during postural and respiratory
Medically unexplained dyspnea: partly moderated activation of the human diaphragm. J Appl Physiol
by dysfunctional (thoracic dominant) breathing (1985). 2000;89(3):967-976.
pattern. J Asthma. 2011;48(3):259-265. 17. Richardson CA, Jull GA, Hodges PW, et al.
2. Thomas M, McKinley RK, Freeman E, et al. Therapeutic Exercise for Spinal Segmental Stabilization
Prevalence of dysfunctional breathing in patients in Low Back Pain; Scientific Basis and Clinical
treated for asthma in primary care: cross sectional Approach. Edinburgh: Churchill Livingstone; 1999.
survey. BMJ. 2001;322(7294):1098-1100. 18. Zazulak BT, Hewett TE, Reeves NP, et al. Deficits in
3. Lowhagen O. [Asthma--a disease difficult to define. neuromuscular control of the trunk predict knee
Patients can receive correct treatment by means of injury risk: a prospective biomechanical-epidemiologic
differential diagnosis criteria]. Lakartidningen. study. Am J Sports Med. 2007;35(7):1123-1130.
2005;102(50):3872-3873, 3875-3878. 19. Peate WF, Bates G, Lunda K, et al. Core strength:
4. Pryor JA PSC. Physiotherapy for Respiratoryand a new model for injury prediction and prevention.
Cardiac Problems. Edinburgh, UK: Livingstone; 2002. J Occup Med Toxicol. 2007;2:3.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 783
20. O’Sullivan PB, Grahamslaw KM, Kendell M, et al. 34. Jack S, Rossiter HB, Warburton CJ, et al. Behavioral
The effect of different standing and sitting postures influences and physiological indices of ventilatory
on trunk muscle activity in a pain-free population. control in subjects with idiopathic hyperventilation.
Spine (Phila Pa 1976). 2002;27(11):1238-1244. Behav Modif. 2003;27(5):637-652.
21. Courtney R, Greenwood KM, Cohen M. 35. Gulgin H, B. H. The Functional Movement Screening
Relationships between measures of dysfunctional (FMS)™: an inter-rater reliability study between
breathing in a population with concerns about their raters of varied experience. Int J Sports Phys Ther.
breathing. J Bodyw Mov Ther. 2011;15(1):24-34. 2014;9(1):14-20.
22. Chaitow L BD, Gilbert C. Multidisciplinary 36. Smith C, Chimera N, Wright N, et al. Interrater and
Approaches to Breathing Pattern Disorders. London, intrarater reliability of the Functional Movement
UK: Churchill Livingstone; 2002. Screen. J Strength Cond Res. 2013;27(4):982-987.
23. Roussel NA, Nijs J, Truijen S, et al. Low back pain: 37. Gribble PA, Brigle J, Pietrosimone BG, et al.
clinimetric properties of the Trendelenburg test, Intrarater reliability of the Functional Movement
active straight leg raise test, and breathing pattern Screen. J Strength Cond Res. 2013;27(4):978-981.
during active straight leg raising. J Manipulative 38. Teyhen DS, Shaffer SW, Lorenson CL, et al. The
Physiol Ther. 2007;30(4):270-278. Functional Movement Screen: a reliability study.
24. Gardner WN. The pathophysiology of J Orthop Sports Phys Ther. 2012;42(6):530-540.
hyperventilation disorders. Chest. 1996;109(2):516- 39. Onate JA, Dewey T, Kollock RO, et al. Real-time
534. intersession and interrater reliability of the
Functional Movement Screen. J Strength Cond Res.
25. Miner JR, Heegaard W, Plummer D. End-tidal carbon
2012;26(2):408-415.
dioxide monitoring during procedural sedation. Acad
Emerg Med. 2002;9(4):275-280. 40. Minick KI, Kiesel KB, Burton L, et al. Interrater
reliability of the Functional Movement Screen.
26. Levitsky M. Pulmonary Physiology. New York, J Strength Cond Res. 2010;24(2):479-486.
NY:McGraw Hill; 1995.
41. Frohm A, Heijne A, Kowalski J, et al. A nine-test
27. van Dixhoorn J, Duivenvoorden HJ. Efficacy of screening battery for athletes: a reliability study.
Nijmegen Questionnaire in recognition of the Scand J Med Sci Sports. 2011;22(3):306-315.
hyperventilation syndrome. J Psychosom Res.
42. CliftonSmith T, Rowley J. Breathing pattern
1985;29(2):199-206.
disorders and physiotherapy: inspiration for our
28. Mosby’s Medical Dictionary. 9th ed: Elsevier; 2009. profession. Phys Ther Rev. 2011;16(1):75-86.
29. Courtney R, Cohen M, Reece J. Comparison of the 43. Holloway E, Ram FS. Breathing exercises for asthma.
Manual Assessment of Respiratory Motion (MARM) Cochrane Database Syst Rev. 2004(1):CD001277.
and the hi lo breathing assessment in determining a 44. Hagman C, Janson C, Emtner M. Breathing
simulated breathing pattern. Int J Osteopath Med. retraining - a five-year follow-up of patients with
2009;12(3):86-91. dysfunctional breathing. Respir Med.
30. Vansteenkiste J, Rochette F, Demedts M. Diagnostic 2011;105(8):1153-1159.
tests of hyperventilation syndrome. Eur Respir J. 45. Jones M, Troup F, Nugus J, et al. Does manual
1991;4(4):393-399. therapy provide additional benefit to breathing
31. Courtney R, Greenwood, KM. Preliminary retraining in the management of dysfunctional
investigation of a measure of dysfunctional breathing? A randomised controlled trial. Disabil
breathing symptoms: the Self Evaluation of Rehabil. 2014;37(9):763-770.
Breathing Questionnaire (SEBQ). Int J Osteopath Med. 46. Alrwaily M, Timko M, Schneider M, et al. Treatment-
2009;12(4):121-127. based classification system for low back pain:
32. Mitchell AJ, Bacon CJ, Moran RW. Reliability and revision and update. Phys Ther. 2016;96(7):1057-1066.
determinants of Self-Evaluation of Breathing 47. Fritz JM, Cleland JA, Childs JD. Subgrouping
Questionnaire (SEBQ) score: a symptoms-based patients with low back pain: evolution of a
measure of dysfunctional breathing. Appl classification approach to physical therapy. J Orthop
Psychophysiol Biofeedback. 2016;41(1):111-120. Sports Phys Ther. 2007;37(6):290-302.
33. Courtney R, Cohen M. Investigating the claims of 48. Briggs KK, Lysholm J, Tegner Y, et al. The reliability,
Konstantin Buteyko, M.D., Ph.D.: the relationship of validity, and responsiveness of the Lysholm score
breath holding time to end tidal CO2 and other and Tegner activity scale for anterior cruciate
proposed measures of dysfunctional breathing. ligament injuries of the knee: 25 years later. Am J
J Altern Complement Med. 2008;14(2):115-123. Sports Med. 2009;37(5):890-897.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 784
Appendix 1. Activity rating scale.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 785
Appendix 2
Tabulations of how the mini-questionnaire was developed showing the questions with the highest frequency
counts of subjects who scored either of the 2 higher levels of dysfunction. Each question is scored on a four-
point ordinal scale from each of the self reported questionnaires utilized.
The Nijmegen is scored on a five-point ordinal scale from 0-4 (0- Never, 1- Rare, 2- Sometimes, 3- Often, and
4- Very Often) so any question scored as a 3 or 4 was utilized.
These 2 questions from the Nijmegen were the most frequently scored at the high end of dysfunction (a score
of 3 or 4):
The SEBQ is scored on a 4-point ordinal scale from 0-3. (0- never/not true at all, 1- occasionally/a bit true, 2-
frequently-mostly true, and, 3- very frequently/very true)
so any score of 2 or 3 was utilized. These two questions from the SEBQ were the most frequently scored at the
high end of dysfunction (a score of 2 or 3):
Below is the 2 x 2 table used to calculate the Chi Square demonstrating a significant difference between fre-
quency of subjects scoring the four questions and presence of dysfunctional breathing.
The International Journal of Sports Physical Therapy | Volume 12, Number 5 | October 2017 | Page 786