Influence of the breathing pattern on the pulmonary function of endurance-trained athletes

Abstract

Proper functioning of the respiratory system is one of the most important determinants of human health. According to current knowledge, the diaphragmatic breathing pattern seems to be the most favourable. However, recent reports indicate that athletes often have dysfunctional breathing patterns, which may be associated with an increased risk of musculoskeletal injuries. The influence of the type of breathing pattern on the mechanical airways in athletes has not been investigated. The aim of the present study was to determine the characteristics and relationships between breathing patterns and respiratory function in athletes. This study included 69 Polish elite endurance athletes (♂40, ♀29) in different sports disciplines and 44 (♂17, ♀27) healthy nonathletes as a control group. All participants underwent pulmonary function tests (spirometry, plethysmography, diffusion capacity for carbon monoxide) with assessment of breathing patterns by the Hi–Lo test. Inspiratory and expiratory resistance (R) and reactance (X) of the respiratory system at a given frequency (5 Hz, 11 Hz, and 19 Hz) were measured by a noninvasive forced oscillation technique. In this study, almost half of the athletes (44.92%) had dysfunctional breathing patterns, although at a lower rate than that in the control group. Diaphragmatic breathing patterns were characterized by higher spirometric, plethysmographic and DLCO values compared to thoracic or abdominal breathing patterns. Similarly, lower inspiratory reactance at 5 Hz (X5%pred.) was observed in the diaphragmatic pattern compared to the thoracic pattern. A diaphragmatic breathing pattern is associated with better pulmonary function test results. However, this study revealed a dysfunctional breathing pattern in almost half of the athletes. These results suggest that the assessment of breathing patterns and the implementation of breathing exercises in athletes are essential to promote proper breathing patterns.

Full text

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Inuence of the breathing pattern
on the pulmonary function
of endurance‑trained athletes
Marcin Sikora 1*, Rafał Mikołajczyk 2, Olga Łakomy 1, Jakub Karpiński 3,
Aleksandra Żebrowska 1, Sabina Kostorz‑Nosal 4 & Dariusz Jastrzębski 4
Proper functioning of the respiratory system is one of the most important determinants of human
health. According to current knowledge, the diaphragmatic breathing pattern seems to be the
most favourable. However, recent reports indicate that athletes often have dysfunctional breathing
patterns, which may be associated with an increased risk of musculoskeletal injuries. The inuence of
the type of breathing pattern on the mechanical airways in athletes has not been investigated. The
aim of the present study was to determine the characteristics and relationships between breathing
patterns and respiratory function in athletes. This study included 69 Polish elite endurance athletes
(♂40, ♀29) in dierent sports disciplines and 44 (♂17, ♀27) healthy nonathletes as a control group. All
participants underwent pulmonary function tests (spirometry, plethysmography, diusion capacity for
carbon monoxide) with assessment of breathing patterns by the Hi–Lo test. Inspiratory and expiratory
resistance (R) and reactance (X) of the respiratory system at a given frequency (5 Hz, 11 Hz, and 19 Hz)
were measured by a noninvasive forced oscillation technique. In this study, almost half of the athletes
(44.92%) had dysfunctional breathing patterns, although at a lower rate than that in the control
group. Diaphragmatic breathing patterns were characterized by higher spirometric, plethysmographic
and DLCO values compared to thoracic or abdominal breathing patterns. Similarly, lower inspiratory
reactance at 5 Hz (X5%pred.) was observed in the diaphragmatic pattern compared to the thoracic
pattern. A diaphragmatic breathing pattern is associated with better pulmonary function test results.
However, this study revealed a dysfunctional breathing pattern in almost half of the athletes. These
results suggest that the assessment of breathing patterns and the implementation of breathing
exercises in athletes are essential to promote proper breathing patterns.
Proper functioning of the respiratory system is one of the most important factors determining the state of human
health. During exercise, one of the critical functions of the respiratory system is to adapt the ventilation of the
lungs to the increased oxygen demand of the body. Pulmonary function is a determinant of aerobic capacity in
athletes. Exercise training has been shown to increase the functional reserve of the respiratory system1. Improve-
ments in muscular strength and ventilation in response to endurance training appear to be particularly important
in athletes. However, ventilatory work has been found to play a signicant role in the cardiovascular response
during high-intensity exercise1. e main mechanism is the use of inspiratory reserve volume. Exercise training
improves endurance and strength of the respiratory muscles in athletes; it also causes a reduction in bronchial
resistance and increases lung elasticity and alveolar expansion2,3. Studies have also reported increases in lung
volume and capacity in response to exercise2.
Proper breathing, also known as diaphragmatic breathing, involves synchronized movement of the upper tho-
rax, lower thorax, and abdomen4. In addition, proper breathing requires adequate cooperation of the diaphragm
and respiratory muscles5. erefore, the key to achieving a proper exercise capacity is to maintain a proper breath-
ing pattern. On the other hand, the presence of dysfunctional breathing patterns in the patient population, such
as those with asthma, is well documented and is associated with lower pulmonary function test results6,7. To date,
the presence of abnormal breathing patterns in athletes and their impact on pulmonary function test results and
OPEN
1Department of Physiological and Medical Sciences, Institute of Healthy Living, The Jerzy Kukuczka Academy of
Physical Education, 72A Mikolowska Street, Katowice, Poland. 2Department of Physiological and Medical Sciences,
The Jerzy Kukuczka Academy of Physical Education, 72A Mikolowska Street, Katowice, Poland. 3Department of
Exercise and Sport Performance, Institute of Sport Science, The Jerzy Kukuczka Academy of Physical Education,
72A Mikolowska Street, Katowice, Poland. 4Department of Lung Diseases and Tuberculosis, Faculty of Medical
Sciences in Zabrze, Medical University of Silesia, Zabrze, Poland. *email: m.sikora@awf.katowice.pl
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exercise capacity remains uncertain. Recent reports indicate that dysfunctional breathing patterns are relatively
common in athletes and may be associated with an increased risk of musculoskeletal injuries8. Additionally, the
detection of abnormal breathing patterns in athletes is an important step in the prevention of sports injuries8.
e breathing pattern can also signicantly inuences cardiac autonomic regulation (i.e., cardiorespiratory
coupling—CRC), which can directly aect sports performance. So far CRC assessment have been proposed to
account for the complex linear and non-linear interactions between respiratory system and heart, as well as their
closed loop relationship with feed-back and feed-forward mechanisms9. According to Elstad etal.10, there are
three types of cardiorespiratory interactions that can determine CRC: respiratory sinus arrhythmia; cardioventila-
tory coupling; and respiratory stroke volume synchronization. CRC coupling appears to provide a great deal of
information regarding the physical performance of athletes by depicting it not only quantitatively by measuring
maximal oxygen uptake, but also by tracking important changes regarding the blood buering system and the
eciency of the gas exchange system11. e results of the present study point to respiratory pattern as another
variable that should be taken into account during CRC analysis.
e forced oscillation technique (FOT) appears to be a potential alternative to traditional methods (spirom-
etry, plethysmography) to assess lung function in athletes. FOT is a non-invasive type of lung function test that
allows the assessment of the mechanical properties of both the bronchi and the lung parenchyma12. Depending
on the frequency of the pressure wave used, impedance provides information on dierent components of the
respiratory system13. In contrast to the gold standard for the examination of respiratory function—spirometry—
oscillometry is a relatively new test method which has already been used successfully in athletes. Studies have
conrmed the high sensitivity of this method in detecting respiratory disorders in athletes14–16. FOT has been
shown to be more sensitive than spirometry in detecting small peripheral airway diseases. e use of oscillometry
in the study of respiratory function in athletes is one of the most important strengths of this work especially as
there has been no work to date assessing the eect of breathing pattern on respiratory impedance.
e inuence of the type of breathing pattern on pulmonary function test results and respiratory impedance
in athletes has not been investigated, which is the main objective of this study.
Aim
e aim of the present study was to determine the characteristics of and the relationship between breathing
patterns and respiratory functions of athletes.
Methods
Subjects
is experimental study evaluated the eect of breathing pattern on lung function and mechanical properties of
the respiratory system in elite Polish endurance athletes is study included 69 Polish elite endurance athletes
(Endurance Athletes Group, EAG) (♂40, ♀29) from dierent sports disciplines and 44 (♂17, ♀27) healthy non-
athlete students from the Academy of Physical Education in Katowice as a control group (CG). Athletes (fourty
males and twenty nine females) volunteered for the study. All participants had valid medical examinations and
showed no contraindications to participating in the study. ey were recruited via contact with the respective
coach of the Polish National Sports Associations. e examinations were performed in a certied laboratory of
the Institute of Healthy Living at the Academy of Physical Education in Katowice. e athletes participated in
a single testing session on a nontraining day. During this session, bronchial mechanical properties, lung func-
tion and breathing patterns were analysed. In addition, body composition was assessed using the bioimpedance
method (In Body220 Biospace, Inc., Seoul, Korea ISO 9001:2015, EN ISO 13485:2016, EN60601-1, EN60601-
1-2). e inclusion criteria for the athlete group were as follows: (1) age over 18years, (2) training endurance
disciplines, (3) training experience of over 6years, (4) good general health (All athletes were qualied for exami-
nation by a sports medicine specialist. Physical examination, blood count, urinalysis, electrocardiography and
echocardiography were used as part of the screening process), (5) nonsmoker status, and (6) signing of consent
to participate in the research. e inclusion criteria for the control group were as follows: (1) age over 18years,
(2) no exercise discipline, (3) good general health, and (4) signing of consent to participate in the study. e
exclusion criteria were as follows: (1) the presence of respiratory diseases; (2) the presence of other diseases,
such as neuromuscular diseases, cardiovascular diseases, and obesity, that aect respiratory tract and lung func-
tion; and (3) a lack of written consent to participate in the study. e group of athletes included 21 swimmers
(Polish national team athletes), 10 ski runners (Polish national team athletes), 15 long-distance runners(Polish
national team athletes), 17 soccer players (Polish Premier League players), and 6 triathletes (master class ath-
letes). Only elite endurance trained athletes (long distance runners, and long distance swimmers, triathletes,
cross-country skiers and soccer players) with a mean training volume (~ 20h/week) were included in this study
as recommended in the paper: McKinney etal.17. e research project was approved of by University Bioethics
Committee for Scientic Research at Jerzy Kukuczka Academy of Physical Education-Opinion No 3/2018 of 19
April 2018and conducted in accordance with the Declaration of Helsinki of the World Medical Association,.
All research was performed in accordance with relevant guidelines/regulations, and include in their manuscript
a statement conrming that informed consent was obtained from all participants and/or their legal guardians.
Moreover study participants gave informed consent to the study.
e average sports experience of the athletes was 7.3 ± 1.1years. e exact characteristics of the tested athletes
are presented in Table1.
e primary outcome was the assessment of lung function in the athletes compared to the control group. e
secondary outcome was to evaluate the combined eect of training and breathing pattern.
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Forced oscillation technique
e mechanical properties of the respiratory system were assessed using the noninvasive forced oscillation
technique (FOT). FOT was performed with a Resmon Pro Full device (Restech Respiratory Technology SRL,
Milan, Italy, ISO 9001:2015, ISO 13485:2016). e measurements were based on the assessment of resistance (R,
inspiratory, expiratory), reactance (X, inspiratory, expiratory) at frequencies of 5Hz and 11Hz and the dierences
between the inspiratory and expiratory phases of X at 5Hz (∆Xrs). e results were expressed as a percentage
of the predicted values according to Oostveen etal.18. e test was performed during tidal breathing in a sitting
position with the cheeks pressed by the examined athlete. e forced oscillation technique was performed rst
to avoid the likely inuence of forced breathing manoeuvres during spirometry on the quality of the results.
e forced oscillation technique (FOT) is a potential alternative to traditional methods (spirometry, plethys-
mography) that can be used to assess lung function in athletes. FOT is a noninvasive pulmonary function test that
allows evaluation of the mechanical properties of both the airways and the lung parenchyma19. Depending on
the pressure wave frequency used, impedance provides information about dierent components of the respira-
tory system20. FOT has been shown to be more sensitive than spirometry in detecting small peripheral airway
disease. In addition, FOT performed during tidal breathing12 can improve the assessment of the respiratory
system, which consists of resistance (R) and reactance (X). Resistance reects the relationship between pressure
and the ow of air passing through the airways and is therefore mostly dependent on the airway diameter12,13.
e use of dierent frequencies allows airway resistance to be divided into total (R5, at 5Hz), central (R19, at
19Hz) and peripheral (R5-R19) resistance. Reactance expresses the ability of the respiratory system to deform21.
X is determined by the elastic properties that dominate at low frequencies (X5) and the inertial properties of the
lung tissue that dominate at high frequencies (X19)22.
Lung function assessment
e athletes’ lung function was assessed using PulmOne’s MiniBox + (PulmOne Advanced Medical Devices, Ltd,
Ra’ananna, Israel ISO 9001:2015), which is a new device approved by the Food and Drug Administration and
not yet included in the ATS/ERS guidelines. PulmOne’s MiniBox + is a complete pulmonary function testing
(PFT) system including cabinless plethysmography, which has been validated as a reliable method to measure
absolute lung volumes23, as well as spirometry (VC- vital capacity, FVC- forced expiratory volume in one second
and FEV1%VC- forced expiratory volume in one second % of vital capacity) and DLCO testing according to
guidelines24–26. All plethysmographic and spirometric results were expressed in litres and as a percentage of the
predicted values.
Assessment of breathing pattern
e breathing pattern was assessed in the standing position by three independent physiotherapists experienced
in pulmonary rehabilitation (at the same time) using the Hi–Lo test. Hi–Lo is a manual assessment to determine
whether a subject has a normal diaphragmatic breathing pattern or an abnormal pattern. e examiner deter-
mines whether thoracic or abdominal movement is dominant during breathing27. e reliability of the Hi–Lo
test has been reported by others to be acceptable27,28. e Hi–Lo test results were used to categorize observations
as (a) thoracic-dominant pattern (visible abdominal excursion is absent, but visible superior rib cage migration
and shoulder elevation are present), (b) abdominal-only pattern (visible anterior–posterior abdominal expansion
is present, but visible superior rib cage migration and shoulder elevation are present), but visible superior rib
cage migration and shoulder elevation are present), or (c) diaphragmatic breathing pattern (anterior abdominal
expansion followed by anterior chest expansion without superior rib cage migration and shoulder elevation)29.
e graphical characteristics of the Hi–Lo test are illustrated in Fig.1.
Statistical analysis
Microso Excel 2007 (Microso Corp., Washington, USA) and e Statistics Package v.12 (StatSo Poland,
13.3) were used for data processing and analysis, and the results are presented as arithmetic means and standard
deviations. e magnitudes of dierences between the results of the athlete and control groups were expressed
as standardized mean dierences. e eect size (η2) of breathing patterns and dierences between groups were
estimated, and the following interpretation was adopted: 0.01–0.06 denoting a weak eect, 0.06–0.14 denoting
a medium eect, and over 0.14 denoting a strong eect. e eects of breathing pattern on lung function and
Table 1. Somatic characteristics of the study groups (endurance athlete group and control group). Results of
ANOVA analysis of variance, Tukey post hoc test. BMI, body mass index; BSA, body surface area; F, variation
between sample means; p, level of signicance; η2, eect size. *p < 0.05 signicant dierences signicant
dierences in breathing patterns.
Var iable
EAG n = 47; 27M, 20 F CG n = 44; 17M, 27 F
Fpη2
Mean ± SD Mean ± SD
Age (years) 21.05 ± 1.56 22.42 ± 0.98 0.281 0.755 0.007
Body height (m) 1.76 ± 0.09 1.74 ± 0.05 0.23 0.633 0.003
Body mass (kg) 73.27 ± 10.59 69.62 ± 8.87 0.911 0.342 0.011
BMI (kg/m2)23.38 ± 2.01 22.72 ± 1.42 1.646 0.202 0.019
BSA (m2)1.90 ± 0.18 1.83 ± 0.22 2.763 0.197 0.012
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respiratory impedance were determined using analysis of variance (ANOVA) (one-way ANOVA and factorial
ANOVA). e combined eect of gender and breathing pattern and respiratory impedance was examined using
ANOVA analysis of variance(one-way ANOVA and factorial ANOVA). Signicant dierences between groups
and the eects of breathing pattern on lung function and respiratory impedance were analysed using the Tukey
post hoc test.
Results
e tested group of subjects was divided according to their breathing patterns. In the athlete group, 13.04%
of the subjects had an abdominal breathing pattern, 31.88% had a thoracic breathing pattern and 55.07% had
a diaphragmatic breathing pattern. In the CG group, 18.18% of subjects had an abdominal breathing pattern,
29.54% had a thoracic breathing pattern, and 52.27% had a diaphragmatic breathing pattern. e detailed data
are shown in Fig.2.
e analysis of variance allowed us to observe signicantly higher spirometric, plethysmographic and DLCO
values for the diaphragmatic breathing pattern compared to the thoracic breathing pattern in the group of athletes
for VC (F = 9.77; p = 0.000; η2 = 0.307), FVC (F = 9.40; p = 0.001; η2 = 0.299), FEV1 (F = 8.41; p = 0.00; η2 = 0.276),
DLCO mL/min/mmHg (F = 9.48; p = 0.000; η2 = 0.327), IC (F = 9.777; p = 0.001; η2 = 0.307), ERV (F = 15.00;
p = 0.001; η2 = 0.312), ERV%PRED (F = 9.770, p = 0.017; η2 = 0.228), PEF (F = 7.832; p = 0.015; η2 = 0.262), PIF
(F = 10.620; p = 0.001; η2 = 0.330), TLC (F = 6.486; p = 0.003; η2 = 0.227), RV/TLC (F = 4.268; p = 0.019; η2 = 0.162),
VA (F = 10.596; p = 0.001; η2 = 0.352).
Statistical evaluation also revealed higher spirometric values, plethysmographic values and DLCO for the
abdominal breathing pattern compared to the thoracic breathing pattern in the group of athletes for VC (F = 9.77;
p = 0.011; η2 = 0.307), FVC (F = 9.40; p = 0.011; η2 = 0.299), FEV1 (F = 8.41; p = 0.006; η2 = 0.276) and DLCO
mL/min/mmHg (F = 9.48; p = 0.030; η2 = 0.327), IC (F = 9.777; p = 0.011; η2 = 0.307), ERV (F = 15.00; p = 0.001;
η2 = 0.312), ERV%PRED (F = 9.770, p = 0.002; η2 = 0.228), PEF (F = 7.832; p = 0.001; η2 = 0.262), PIF (F = 10.620;
p = 0.001; η2 = 0.330), TLC (F = 6.486; p = 0.044; η2 = 0.227), VA (F = 10.596; p = 0.038; η2 = 0.352).
Figure1. Graphic presentation of the Hi–Lo test.
Figure2. e number of people in the study groups in terms of the occurrence of the breathing pattern.
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Dierences between diaphragmatic and abdominal breathing patterns in spirometric, plethysmographic,
and DLCO values were not statistically signicant. Detailed results of the statistical analyses are presented in
Table2. Furthermore, the analysis of variance did not indicate an eect of gender for certain breathing patterns
in the athlete study group.
Analysis of variance revealed signicantly lower values of inspiratory reactance at 5Hz for the diaphrag-
matic breathing pattern compared to the thoracic breathing pattern (inspiratory %pred—96.41% vs. 128.72%).
Detailed data on the dierences in respiratory impedance with respect to the observed breathing patterns are
presented in Table3.
In addition, the factorial analysis of variance also indicated the combined eect of regular training and
breathing pattern on spirometric values. Compared to the control group, athletes had signicantly higher values
for VC (diaphragmatic breathing pattern, p = 0.007), FVC (diaphragmatic breathing pattern, p = 0.001), FEV1
(diaphragmatic breathing pattern, p = 0.001), and VC %pred (all breathing patterns abdominal p = 0.023, thoracic
p = 0.001, and diaphragmatic p = 0.027). No combined eect of training and breathing pattern on respiratory
impedance was observed. Detailed results of the analysis are presented in Table4.
Table 2. Breathing pattern dierences in spirometry, plethysmography, and DLCO in endurance athletes.
Results of ANOVA analysis of variance, Tukey post hoc test All data are presented as the mean ± SD. VC,
vital capacity; IC, inspiratory capacity; ERV, expiratory reserve volume; FVC, forced vital capacity; FEV1,
forced expiratory volume in one second; MEF, maximal expiratory ow; PEF, peak expiratory ow; PIF, peak
inspiratory ow; TLC, total lung capacity; RV, residual volume; DLco, diusion lung capacity for carbon
monoxide; VA, alveolar volume. *p < 0.05 signicant dierences signicant dierences in breathing patterns.
Variables
EAG breathing pattern
FpEta2
Post hoc
oracic ± SD
(n = 22, 13♂, 9♀)Diaphragmatic ± SD
(n = 38, 20♂, 18♀)Abdominal ± SD
(n = 9, 7♂, 2♀)Diaphragmatic
versus oracic Abdominal versus
oracic Diaphragmatic
versus Abdominal
VC (L) 4.05 ± 0.95 5.495 ± 1.13 5.49 ± 0.95 9.777 0.000 0.307 0.001* 0.011* 0.984
IC (L) 2.99 ± 0.79 3.76 ± 0.87 3.31 ± 0.77 6.08 0.003 0.155 0.009* 0.698 0.489
ERV (L) 1.06 ± 0.56 1.73 ± 0.62 2.18 ± 0.45 15.00 0.000 0.312 0.001* 0.001* 0.243
VC (%pred.) 91.213 ± 10.56 106.42 ± 14.10 104.37 ± 9.61 0.075 0.927 0.003 0.991 0.959 0.920
IC%PRED 106.36 ± 16.80 113.40 ± 20.37 97.14 ± 14.24 3.107 0.051 0.086 0.426 0.548 0.160
ERV%PRED 70.37 ± 34.48 96.44 ± 29.83 120.46 ± 22.07 9.770 0.000 0.228 0.017* 0.002* 0.226
FEV1/FVC 85.17 ± 5.06 79.60 ± 18.39 79.59 ± 16.37 2.080 0.136 0.086 0.156 0.991 0.371
FEV1/FVC (%pred.) 97.65 ± 6.01 95.99 ± 7.23 92.71 ± 18.58 0.690 0.507 0.030 0.638 0.962 0.580
FVC (L) 4.85 ± 0.95 6.18 ± 1.18 6.03 ± 0.95 9.400 0.000 0.299 0.001* 0.011* 0.996
FVC (%pred.) 111.27 ± 11.39 113.18 ± 12.75 108.33 ± 9.18 0.037 0.963 0.001 0.997 0.961 0.972
FEV1 (L) 4.14 ± 0.88 5.13 ± 1.01 4.69 ± 0.85 8.415 0.000 0.276 0.001* 0.006* 0.879
FEV1 (%pred.) 107.68 ± 8.91 104.39 ± 8.43 106.62 ± 11.22 0.651 0.526 0.028 0.510 0.960 0.821
PEF (L) 7.59 ± 1.64 9.25 ± 1.93 10.41 ± 1.46 7.832 0.001 0.262 0.015* 0.001* 0.256
PEF% (%pred.) 97.25 ± 11.84 95.82 ± 16.72 105.37 ± 15.03 1.236 0.300 0.053 0.954 0.427 0.275
MEF 50 (l/min) 5.04 ± 1.21 5.21 ± 1.30 6.02 ± 1.87 1.426 0.250 0.060 0.922 0.238 0.334
MEF 50 (%pred.) 103.43 ± 19.28 92.78 ± 20.28 106.00 ± 31.81 1.611 0.211 0.068 0.313 0.961 0.324
PIF (L) 6.25 ± 1.43 8.30 ± 1.42 8.86 ± 2.20 10.620 0.000 0.330 0.001* 0.001* 0.670
TLC (L) 5.75 ± 0.80 7.01 ± 1.33 6.96 ± 1.03 6.486 0.003 0.227 0.003* 0.044* 0.991
TLC (%pred.) 105.87 ± 8.49 101.65 ± 11.72 99.50 ± 10.77 1.201 0.310 0.051 0.443 0.353 0.873
RV (L) 1.14 ± 0.25 1.07 ± 0.55 1.08 ± 0.32 0.126 0.881 0.005 0.876 0.946 0.998
RV (%pred.) 83.81 ± 19.91 69.43 ± 34.13 70.75 ± 20.58 1.331 0.274 0.057 0.266 0.533 0.992
RV/TLC 20.12 ± 4.64 15.08 ± 6.45 15.58 ± 3.44 4.268 0.020 0.162 0.019* 0.146 0.972
RV/TLC (%pred.) 78.81 ± 16.91 66.39 ± 27.81 70.62 ± 15.06 1.403 0.256 0.059 0.227 0.687 0.893
VC (%pred.) 91.213 ± 10.56 106.42 ± 14.10 104.37 ± 9.61 0.075 0.927 0.003 0.991 0.959 0.920
DLco mL/min/
mmHg 25.73 ± 5.91 36.31 ± 8.10 34.57 ± 7.43 9.484 0.000 0.327 0.001* 0.030* 0.849
DLco (%pred.) 103.86 ± 11.77 113.40 ± 16.53 109.14 ± 14.65 1.805 0.177 0.084 0.152 0.714 0.788
VA (L) 5.31 ± 1.06 7.34 ± 1.56 6.83 ± 0.86 10.596 0.000 0.352 0.001* 0.038* 0.655
VA%pred 102.66 ± 13.00 110.65 ± 26.68 110.85 ± 7.45 0.748 0.479 0.036 0.492 0.657 0.999
DLco/VA (ml/min/
mmHg/L) 4.86 ± 0.58 4.95 ± 0.53 5.05 ± 0.80 0.259 0.773 0.013 0.885 0.769 0.932
DLco/VA%pred 101.13 ± 11.48 97.60 ± 9.52 98.28 ± 14.30 0.452 0.639 0.022 0.623 0.841 0.989
Respiratory fre-
quency (br/min) 13.84 ± 2.52 12.92 ± 2.38 13.33 ± 2.47 0.347 0.739 0.457 0.991 0.838 0.961
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Discussion
One of the main novelties of this work is the use of the technique of forced oscillations to study the dierences
between the breathing patterns used by athletes. Interestingly, in the group of athletes, signicantly lower reac-
tance values (5Hz %pred) were observed in subjects using the diaphragmatic breathing pattern compared to
the thoracic pattern. Reactance is determined by the elastic properties of the lung tissue, which dominate at low
frequencies (X5), and the inertial properties of the lung tissue, which dominate at high frequencies (X19)22. Nev-
ertheless, X5 is also lower in the presence of heterogeneity in airway diameter distribution, which can be present
in obstructive lung disease, most commonly when small airways collapse. Regardless of the mechanism, such a
decrease in reactance in the group of athletes underlines the advantage of the diaphragmatic breathing pattern,
expressed in the improvement of lung function. However, it should be remembered that the observed results
are still within the normal range for healthy people, and we only present the tendency to change the elasticity of
the lung parenchyma or the communication between dierent parts of the lung under the inuence of training.
ese results are in agreement with previously published studies that indicate an increase in lung elasticity as a
result of physical training13,21. us far, scientic reports only explain the occurrence of obstructive disorders in
athletes, especially winter sports activity, which puts athletes at risk of asthma and exercise-induced bronchoc-
onstriction. is is thought to be the result of repeated dehydration of the small airways when large volumes of
cold air are inhaled30. Exercise-induced bronchospasm, which occurs aer vigorous exercise, may be triggered by
intense exercise, cold dry environments, chronic asthma, or a variety of air pollutants31. e scientic literature
indicates that physical exercise increases the endurance and strength of the respiratory muscles; it also causes
a reduction in bronchial resistance and increases the elasticity of the lung tissue, allowing free expansion of the
alveoli32. However, previous studies were mainly based on the analysis of spirometric values, the results of which
can only suggest an increase in the elasticity of the lung tissue. e main advantage of this research is the use
of the forced oscillation technique, which is considered a much more sensitive research tool. e signicantly
lower X5 (%pred.) is in line with other better pulmonary function test results observed in athletes and conrms
the positive eect of the diaphragmatic pattern on the functioning of the respiratory system.
Another important observation of this study is the high prevalence of dysfunctional/unfavourable breathing
patterns both in the group of endurance athletes (44.92%) and in the control group (47.73%) of physically active
young healthy people. According to our results, the diaphragmatic breathing pattern is characterized by better
lung function test results. In addition, we found that athletes had higher spirometric and plethysmographic results
than the control group. At the same time, no eect of physical activity was observed on oscillometric results,
which seems to be independent of respiratory muscle and diaphragm function. ese results conrm the eect
of training on the diaphragm only observed in pulmonary function tests requiring forced expiratory manoeuvres
and therefore demonstrate the advantage of the diaphragmatic breathing pattern over the others. A particularly
common but undesirable pattern, especially in athletes, is the thoracic one. Endurance athletes have higher VC,
FEV1, FVC and VC due to the eect of training on the diaphragm and respiratory muscles.
In addition, studies indicate a lower eciency of the respiratory system in subjects with a conrmed dysfunc-
tional breathing pattern. Scientic publications indicate a high prevalence of dysfunctional breathing patterns
(nondiaphragmatic patterns) in the population of healthy, physically active adults29. In addition, lower physical
activity has been observed in subjects with conrmed dysfunctional breathing27. In the work of Shimozawa
etal.8, the prevalence of dysfunctional breathing patterns was even higher (90.6%). Despite the lower number
of dysfunctional breathing patterns observed, the prevalence of dysfunctional breathing patterns in the athletic
population cannot be ignored8, as biomechanical breathing patterns have been associated with various mus-
culoskeletal and psychological conditions and the health status of individuals33–35. In addition, other reports
Table 3. Dierences in respiratory impedance between diaphragmatic, thoracic, and abdominal breathing
patterns in endurance athletes. Results of ANOVA analysis of variance, Tukey post hoc test. All data are
presented as the mean ± SD. R, resistance; X, reactance; insp, inspiratory; exp, expiratory; ∆Xrs, the dierences
between inspiratory and expiratory phases of X at 5Hz. *p < 0.05 signicant dierences signicant dierences
in breathing patterns.
Variables
EAG breathing pattern
FpEta2
Post hoc
oracic ± SD
(n = 22. 13♂. 9♀)) Diaphragmatic ± SD
(n = 38. 20♂. 18♀)Abdominal ± SD
(n = 9. 7♂. 2♀)Diaphragmatic
versus thoracic Abdominal versus
thoracic Diaphragmatic
versus abdominal
Rinsp5 (%pred.) 123.83 ± 28.41 108.15 ± 26.89 117.63 ± 31.81 2.165 0.122 0.061 0.170 0.889 0.762
Rexp5 (%pred.) 138.44 ± 32.19 121.30 ± 33.83 135.80 ± 39.64 1.988 0.144 0.056 0.225 0.985 0.640
Xinsp5 (%pred.) 128.72 ± 44.87 96.41 ± 29.10 91.35 ± 22.67 7.125 0.001 0.177 0.007* 0.061 0.947
Xexp5 (%pred.) 105.52 ± 39.22 82.50 ± 38.19 84.58 ± 49.01 2.409 0.097 0.068 0.144 0.510 0.993
Rinsp11 (%pred.) 113.79 ± 26.03 102.81 ± 24.14 111.99 ± 38.37 1.309 0.276 0.038 0.369 0.988 0.749
Rexp11 (%pred.) 134.87 ± 31.08 120.96 ± 32.56 133.98 ± 40.77 1.446 0.242 0.041 0.352 0.998 0.684
Xinsp11 (%pred.) 222.78 ± 570.40 261.89 ± 709.41 1193.80 ± 2146.00 3.723 0.029 0.101 0.990 0.093 0.112
Xexp11 (%pred.) 275.79 ± 442.44 226.64 ± 451.37 1071.80 ± 2189.11 3.556 0.034 0.097 0.980 0.135 0.106
Rinsp19 (%pred.) 111.32 ± 24.92 100.46 ± 20.88 110.05 ± 36.30 1.572 0.215 0.045 0.312 0.993 0.685
Rexp19 (%pred.) 122.89 ± 24.87 110.64 ± 26.32 123.37 ± 34.84 1.791 0.174 0.051 0.296 0.999 0.580
∆Xrs -0.08 ± 0.21 -0.1 ± 0.19 -0.09 ± 0.23 1 0.97 0.005 0.990 0.982 0.976
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Table 4. Combined eect of training and breathing pattern on spirometric values and respiratory impedance. Results of ANOVA analysis of variance, Tukey post hoc test. All data are
presented as the mean ± SD. VC, vital capacity; IC, inspiratory capacity; ERV, expiratory reserve volume; FVC, forced vital capacity; FEV1, forced expiratory volume in one second; MEF,
maximal expiratory ow; PEF, peak expiratory ow; R, resistance; X, reactance; insp, inspiratory; exp, expiratory; ∆Xrs, the dierences between inspiratory and expiratory phases of X at 5Hz.
*p < 0.05 signicant dierences signicant dierences in breathing patterns.
Variables
EAG breathing pattern CG breathing pattern
FpEta2
Post hoc (CG vs. EAG)
oracic ± SD
(n = 22, 13♂, 9♀))
SD
Diaphragmatic
(n = 38, 20♂, 18♀)
SD
Abdominal (n = 9,
7♂, 2♀)
SD
oracic (n = 13,
6♂, 7♀))
SD
Diaphragmatic
(n = 23, 8♂, 15♀)
SD
Abdominal (n = 8,
3♂, 5♀)
SD
Abdominal
versus
abdominal
oracic
versus
thoracic
Diaphragmatic
versus
diaphragmatic
VC (L) 4.05 ± 0.95 5.49 ± 1.13 5.49 ± 0.95 3.46 ± 0.72 4.47 ± 0.90 4.13 ± 0.89 0.934 0.396 0.017 0.071 0.634 0.007*
IC (L) 2.99 ± 0.79 3.76 ± 0.87 3.31 ± 0.77 2.90 ± 0.94 3.17 ± 0.75 3.11 ± 0.94 1.017 0.365 0.018 0.996 0.999 0.167
ERV (L) 1.059 ± 0.56 1.73 ± 0.62 2.18 ± 0.45 0.56 ± 0.41 1.30 ± 0.55 1.03 ± 0.37 2.914 0.058 0.051 0.001* 0.191 0.086
VC %pred 91.213 ± 10.56 106.42 ± 14.10 104.37 ± 9.61 70.94 ± 9.03 96.64 ± 4.98 87.52 ± 3.97 2.706 0.071 0.048 0.023* 0.001* 0.027*
IC %pred 106.36 ± 16.80 113.41 ± 20.37 97.14 ± 14.25 90.66 ± 17.65 108.08 ± 16.37 101.04 ± 13.78 1.835 0.164 0.033 0.997 0.224 0.912
ERV % pred 70.38 ± 34.48 96.44 ± 29.83 120.47 ± 22.08 36.87 ± 28.52 81.71 ± 26.67 67.96 ± 28.99 3.017 0.053 0.053 0.007* 0.050 0.539
FEV1/FVC 85.17 ± 5.06 79.60 ± 18.39 79.59 ± 16.37 84.30 ± 0.85 84.30 ± 0.93 84.00 ± 1.07 0.60 0.548 0.011 0.976 0.999 0.763
FEV1/
FVC%pred 97.65 ± 6.01 95.99 ± 7.23 92.71 ± 18.58 96.46 ± 8.14 96.47 ± 7.25 96.25 ± 8.33 0.42 0.656 0.007 0.962 0.999 0.999
FVC (L) 4.85 ± 0.95 6.18 ± 1.18 6.03 ± 0.95 4.83 ± 1.18 4.74 ± 1.12 4.85 ± 0.93 5.46 0.026 0.158 0.262 1.000 0.001*
FVC% pred 111.27 ± 11.39 113.18 ± 12.75 108.33 ± 9.18 102.61 ± 7.04 105.39 ± 10.23 105.75 ± 12.94 8.918 0.005 0.235 0.997 0.368 0.181
FEV1 (L) 4.14 ± 0.88 5.13 ± 1.01 4.69 ± 0.85 3.94 ± 0.87 3.80 ± 1.07 3.68 ± 1.20 3.51 0.033 0.061 0.312 0.996 0.001*
PEF (L) 7.59 ± 1.64 9.25 ± 1.93 10.41 ± 1.46 7.59 ± 1.64 7.67 ± 1.87 7.99 ± 1.79 2.84 0.063 0.062 0.082 1.000 0.037*
PEF%pred 97.25 ± 11.84 95.82 ± 16.72 105.37 ± 22.81 86.61 ± 11.09 89.95 ± 9.11 91.25 ± 4.30 0.75 0.472 0.017 0.221 0.262 0.605
MEF 50 5.04 ± 1.21 5.21 ± 1.30 6.02 ± 1.87 4.62 ± 1.34 4.54 ± 1.44 4.29 ± 0.95 1.28 0.282 0.029 0.119 0.969 0.547
MEF 50%pred 103.43 ± 19.28 92.78 ± 20.28 106.00 ± 31.81 87.92 ± 25.32 88.47 ± 21.94 83.62 ± 8.67 1.23 0.295 0.028 0.323 0.464 0.984
Rinsp5
(%pred.) 123.84 ± 28.41 108.15 ± 26.89 117.63 ± 31.81 108.72 ± 17.28 120.28 ± 28.92 115.55 ± 28.93 2.572 0.081 0.045 0.999 0.730 0.672
Rexp5 (%pred.) 138.45 ± 32.19 121.31 ± 33.83 135.80 ± 39.65 123.45 ± 20.57 133.65 ± 41.56 124.14 ± 33.43 1.928 0.150 0.034 0.984 0.877 0.829
Xinsp5 (%pred.) 128.72 ± 44.87 96.41 ± 29.10 91.36 ± 22.67 143.73 ± 40.89 125.92 ± 38.81 122.76 ± 42.26 0.476 0.622 0.008 0.524 0.901 0.077
Xexp5 (%pred.) 105.53 ± 39.22 82.51 ± 38.19 84.59 ± 49.01 120.72 ± 28.40 106.59 ± 38.15 94.51 ± 40.96 0.281 0.754 0.005 0.995 0.915 0.285
Rinsp11 (%pred.) 113.79 ± 26.03 102.81 ± 24.14 111.99 ± 38.38 94.59 ± 16.42 111.05 ± 29.55 112.25 ± 31.19 2.74 0.069 0.048 1.000 0.452 0.902
Rexp11 (%pred.) 134.87 ± 31.08 120.96 ± 32.56 133.98 ± 40.77 117.48 ± 22.06 133.14 ± 39.93 127.48 ± 37.14 2.07 0.131 0.037 0.998 0.781 0.827
Xinsp11 (%pred.) 222.78 ± 570.40 261.89 ± 709.41 1193.80 ± 2146.01 214.86 ± 280.53 320.13 ± 939.84 256.87 ± 300.52 2.17 0.118 0.039 0.283 1.000 0.999
Xexp11 (%pred.) 275.79 ± 442.44 226.64 ± 451.37 1071.80 ± 2189.11 147.88 ± 232.45 170.79 ± 201.94 195.92 ± 284.41 2.33 0.101 0.041 0.130 0.997 0.999
Rinsp19 (%pred.) 111.32 ± 24.92 100.46 ± 20.88 110.05 ± 36.30 90.35 ± 18.84 105.93 ± 27.00 109.35 ± 28.09 3.00 0.053 0.053 1.000 0.265 0.975
Rexp19 (%pred.) 122.89 ± 24.87 110.64 ± 26.32 123.37 ± 34.85 104.10 ± 20.57 115.87 ± 31.61 116.26 ± 29.47 2.00 0.139 0.036 0.995 0.511 0.987
∆Xrs -0.08 ± 0.21 -0.1 ± 0.19 -0.09 ± 0.23 -0,10 ± 0.20 -0.12 ± 0.21 -0.10 ± 0.21 0.92 0.983 0.003 0.998 0.999 1.000
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indicate that dysfunctional breathing strategies inuence functional movement patterns36. In addition, a study
by Shimozawa etal.8 suggests that dysfunctional breathing patterns may also increase the risk of musculoskeletal
injury during exercise. Although dysfunctional breathing patterns have been observed less frequently in athletes
than in the general population, their high prevalence remains a signicant clinical problem, and therefore, an
assessment of breathing patterns may be necessary to prevent injury in the athletic population. erefore, it seems
necessary to include breathing exercises in athletic training that would allow the formation of a correct breathing
pattern. Previous studies suggested that including respiratory muscle training could optimize the respiratory
pattern and aerobic and aerobic capacity in athletes37–39. Strengthening the inspiratory muscles increases respira-
tory performance, endurance and reduces blood lactate concentration. Contrary, fatigue in respiratory muscle
during exercise limits their optimal physiological function and decreases oxygen supply to working muscle40.
Another important nding of our study was the demonstration of no dierences in the incidence of dierent
breathing patterns between the sexes. However, the literature indicates that the thoracic breathing pattern is more
common in women41,42. is seems to be related to respiratory exercises. Positive changes in breathing patterns
induced by exercise have been reported in COPD patients43. Unfortunately, no similar work has been found in
athletes, even if a change in the dysfunctional breathing pattern seems possible. In addition, importantly, in
highly trained endurance athletes, changes in the training load during the training macrocycle do not have any
eect on the change in the breathing pattern44.
is study also conrms the signicant inuence of the breathing pattern on spirometric results. Signicantly
higher spirometric values were observed in athletes using the diaphragmatic breathing pattern compared to the
thoracic pattern. In addition, a signicantly higher RV/TLC ratio and a lower diusion for carbon monoxide
(DLCO) value were observed in subjects using the thoracic breathing pattern in relation to the diaphragmatic
breathing pattern. ese results conrm the negative impact of dysfunctional breathing patterns on lung function.
is condition appears to be particularly important in the athletic population due to the possibility of decreased
physical performance. It is generally accepted that elite athletes and physically active individuals tend to have
higher spirometric values, which are inuenced by many factors, such as strength, agility, power, speed, and
cardiovascular endurance32,45–47. e reason why athletes have higher spirometric lung volumes than sedentary
controls is mostly due to respiratory adaptations to exercise46,48,49. Interestingly, there are also reports that the
introduction of additional inspiratory muscle training can enhance the training eects on lung function in
athletes and at the same time improve their performance50,51. ese results are consistent with our report, which
showed higher spirometric and plethysmographic results in the group of athletes. However, no eect of training
on lung function was observed in the oscillometric results. ese results conrm the higher sensitivity of FOT
compared to spirometry, which excludes subject-related factors, thus conrming its objectivity.
Recent reports indicate a significant effect of endurance training on spirometric values in athletes.
Hacket1indicated that endurance training experience has yielded greater performance in FVC, FEV1, VC and
MVV. Similar observations were conrmed by the reports of Durmic etal.13 and Lazovic etal.32. e presence
of improved lung function is likely the result of training adaptations to greater and prolonged ventilation to
meet the gas exchange demands of exercise1. ese high demands on the respiratory system during endurance
training and events are reected in the occurrence of hypoxemia in some athletes52. In addition, other studies
have shown that endurance athletes have higher FVC and FEV 1 values but lower FEV 1/FVC values than the
sedentary population53.
Our report shows a higher diusion value for carbon monoxide in athletes breathing with the diaphragmatic
breathing pattern compared to the others. To date, no such relationship has been reported in the scientic
literature. Nevertheless, the results we obtained are consistent with the basis of diusion measurement, as it is
well documented that exercise contributes to an increase in DLCO54. During exercise, the surface area of the
functioning alveoli increases and therefore has greater contact with the pulmonary capillaries. Not surprisingly,
diaphragmatic breathing patterns associated with better lung function are characterized by higher DLCO results.
e reports indicate that the DLCO may double in individuals who exercise regularly in proportion to the
increase in cardiac output55, which may explain the fact that body fat% has no eect on the variability of DLCO in
elite athletes49. Furthermore, there is a report indicating that DLCO is positively correlated with lean body mass56.
In this study, a signicant eect of the breathing pattern on lung function was observed. According to our
results, a dysfunctional breathing pattern was associated with lower lung function test results. To date, there
are no reports describing the inuence of breathing patterns on lung function in a group of endurance athletes.
However, the eect of endurance training on changes in breathing patterns during intense exercise has been
analysed, but no signicant changes were observed44.
Study limitations
e main limitations of this study are the small size of the group of athletes tested and the lack of assessment
of exercise capacity as a determinant of lung function and airway mechanical properties. Despite the relatively
small size of the group, the results based on oscillometry seem to be reliable, if only because of the sensitivity
of the device. However, this is a pioneering study showing the impact of breathing pattern on lung function
tests. Future studies are therefore needed to establish the implementation of breathing pattern assessment in the
individual training of subjects.
Conclusions
A diaphragmatic breathing pattern is characterized by better lung function test results. However, almost half
of the athletes in this study had a dysfunctional breathing pattern. ese results suggest that assessment of
the breathing pattern may be necessary to identify dysfunctional breathing patterns in athletes. It may also be
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important to incorporate breathing exercises into an athlete’s training to help develop a proper breathing pattern
and thus better exercise performance.
Data and/or code availability
Data and publication materials are available upon request to the corresponding author.
Received: 7 September 2023; Accepted: 9 January 2024
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Acknowledgements
e authors thank all athletes who participated in the study.
Author contributions
M.S.: conceptualization; data curation; methodology; writing-original dra; writing-review & editing. A.Ż.:
conceptualization; methodology; validation; writing-original dra. R.M.: data curation; investigation; writing-
original dra. O.Ł.: data curation; formal analysis; writing-original dra. J.K.: methodology; writing review and
editing. S.K-N.: formal analysis; investigation; writing-review and editing. D.J.: data curation; methodology;
project administration; writing-review & editing.
Competing interests
e authors declare no competing interests.
Additional information
Correspondence and requests for materials should be addressed to M.S.
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