Respiratory Physiology & Neurobiology 295 (2022) 103779

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Respiratory Physiology & Neurobiology

journal homepage: www.elsevier.com/locate/resphysiol

Influence of water immersion on the airway impedance measured by forced

oscillation technique
Daisuke Hoshi a, b, Marina Fukuie a, b, Shinsuke Tamai a, Reiko Momma a, Takashi Tarumi b, c,
Jun Sugawara b, c, Koichi Watanabe c, *
a
Doctoral Program in Sports Medicine, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
b
Human Informatics and Interaction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki, Japan
c
Faculty of Health and Sports Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan

A R T I C L E I N F O A B S T R A C T

Edited by Yu Ru Kou Introduction: Few studies have examined the influence of different water depths on the airway impedance
measured by forced oscillation technique in healthy adults.
Keywords: Methods: Eleven healthy men (23.2 ± 1.5 years old) participated in this study. We measured the respiratory
Water immersion impedance assessed with the resistance at frequency of 5 Hz and 20 Hz, the reactance at frequency of 5 Hz, and
Airway impedance
frequency of resonance. To compare the influence of water depths, we carried out one dryland (DL) and two
Forced oscillation technique
water level conditions: clavicle level (CL) and xiphoid appendix level (XA).
Water level
Spirometry Results: The respiratory resistance at frequency of 5 Hz was higher in CL and XA than DL, and at 20 Hz was
significantly higher in CL than DL. The respiratory reactance at 5 Hz was lower in CL and XA than DL, and
frequency of resonance was higher in CL and XA than DL.
Conclusion: These results suggested that water immersion above xiphoid appendix level increase airway
resistance.

1. Introduction
Water immersion causes acute changes in the pulmonary physio­
logical systems. Previous studies have reported that water immersion
cause decreased respiratory function such as forced vital capacity (FVC),
forced expiratory volume in one second (FEV1), and maximal respiratory
muscle pressure (Buono, 1983; de Andrade et al., 2014). Therefore,
these findings suggest that compared with the dryland condition, water
immersion places an extra load on respiratory system and may be used
as a therapeutic method for improving the respiratory function.
Previous research has reported the following two mechanisms that
water immersion can directly and indirectly influence the respiratory
system (e.g., airways, alveolars, and respiratory muscles). First, the in­
crease of hydrostatic pressure on the abdominal and chest cavities in­
duces vertical diaphragm displacement and restricts the thorax (e.g.,
alveolar) expansion. As a result, respiratory muscles contract to over­
come the force of water pressure (Agostoni et al., 1966). Second, hy­
drostatic pressure during water immersion shifts blood from the lower
extremities to the chest cavity and increases venous return and central
blood volume (Carter et al., 2014), which stiffens pulmonary tissue and
decreases lung compliance (Pendergast and Lundgren, 2009). While
there have been many reports of the effects of water immersion on
respiratory muscles and lung compliance, the effects of water immersion
on the airway are not well understood due to methodological limita­
tions. For example, FEV1, a clinical index of airway obstruction
measured by spirometry, decreases with clavicle water immersion.
Water immersion at the neck level has also been shown to increase
closing volume when compared with dryland (Bondi et al., 1976).
However, spirometry data are difficult to evaluate airways indepen­
dently because it provides a comprehensive index of the respiratory
system including respiratory muscle strength and lung compliance. In
addition, closing volume may reflect decreased alveolar contractility
rather than an airway obstruction (Kitaoka and Kawase, 2007). More­
over, these studies have not examined the effect of shallower immersion
levels. The water depth of public swimming pools is set at 1.1–1.5 m and
aquatic therapy and exercise are performed at such shallower water
level. Therefore, further study is necessary to determine the effect of
shallower water immersion on respiratory system.

* Corresponding author at: Faculty of Health and Sport Science, University of Tsukuba, 1-1-1, Tennodai, Tsukuba, Ibaraki, 305-0006, Japan.
E-mail address: watanabe.koichi.ga@u.tsukuba.ac.jp (K. Watanabe).

https://doi.org/10.1016/j.resp.2021.103779
Received 17 June 2021; Received in revised form 18 August 2021; Accepted 23 August 2021
Available online 26 August 2021
1569-9048/© 2021 Elsevier B.V. All rights reserved.
D. Hoshi et al.
Forced oscillation technique (FOT) is an airway evaluation method
that can solve the limitations of conventional spirometry measurements.
FOT measurement does not require the breathing effort used in
spirometry tests and can exclude the effects of respiratory muscle and
lung compliance. FOT measures the impedance of the respiratory system
from the spectral relationship between the resultant pressure and
airflow. The impedance is composed of respiratory system resistance
(Rrs) and reactance (Xrs). Rrs reflects the resistance influenced by
airway caliber and Xrs shows elastic and inertial properties of the lung,
which reflects an abnormality in lung parenchyma or airways (Shirai
and Kurosawa, 2016). In the bronchodilator reversibility test, the Rrs
reflects airway reversibility more sensitively than FEV1 when using a
spirometer (Niimi et al., 2003). The frequency dependency of Rrs is
presumed to reflect ventilation inhomogeneity with peripheral airway
lesions (Grimby et al., 1968). Therefore, the FOT is useful evaluation
method to reflect the airway resistance during immersion.
The aim of this study was to evaluate the effects of water immersion
with different water depths on airway impedance. We hypothesized that
the deeper water immersion may present higher airway impedance than
shallower water immersion.
2. Material and methods
2.1. Participants
Eleven healthy young men were recruited (23.2 ± 1.5 years old) in
this study. The participant’s average heights and weights were 171.7 ±
3.6 cm and 65.5 ± 4.7 kg, respectively. The average body mass index
(BMI) was 22.3 ± 1.6 kg/m2. All participants had no presence or history
of pulmonary, cardiovascular, or neuromuscular disease, medication
use, current or a history of smoking. This study was carried out in
accordance with the Declaration of Helsinki and was approved by the
Research Ethics Committee of the University of Tsukuba. All participants
gave informed consent before participation.
2.2. Experimental design
The present study was conducted in randomized crossover design to
compare airway impedance and respiratory function during water im­
mersion at different water depths. All participants were tested in the
dryland (DL) and 2 water immersion conditions in random order:
clavicular immersion (CL) and xiphoid appendix immersion (XA). Water
temperature was maintained at 35.6 ± 0.5 ◦ C, which temperature was
the smallest effect on metabolic system in previous report (Craig and
Dvorak, 1966). Participants were asked to refrain from exercise and
alcohol consumption at least 24 h and caffeine intake at least 12 h before
each experimental condition. Before experiment, participants were
familiarized to the FOT, spirometry, and maximal respiratory muscle
pressures assessments according to the previous studies (Miller et al.,
2005; Oostveen et al., 2003). During experiment, each subject was
instructed to wear swim shorts and sit in a resting position for 10 min to
familiarize themself with the laboratory environment. Then, they
entered the empty bathtub (DL) or bathtub at each water level (XA or
CL) for 10 min and performed airway impedance, respiratory function,
and maximal respiratory muscle pressure measurements. All conditions
started with FOT followed by respiratory function and respiratory
muscle pressure measurements. To exclude the influence of each con­
dition, the interval between each condition was given at least 72 h.
2.3. Respiratory impedance measurements
Respiratory impedance was measured in sitting position with the
FOT (Mostgraph-01; CHEST, Tokyo, Japan). The subjects wore a nose
clip and were asked to perform tidal breathing on the mouthpiece
without leakage. They supported their cheeks to eliminate upper airway
shunting during measurements (Shirai and Kurosawa, 2016). The
2
Respiratory Physiology & Neurobiology 295 (2022) 103779
measurement started after confirming stable breathing. Forced oscilla­
tions are applied to the airway from the mouth to calculate the respi­
ratory impedance through the spectral relationship between the
resultant pressure and airflow. The oscillatory indices are automatically
calculated from the mean values of five resting ventilations whose res­
piratory flow ranged between 0.5 ~ 1.0 L/s. If unnatural breathing such
as swallowing, glottis closure, leakage around the mouthpiece, incom­
plete sealing with the nose clip, irregular breathing, or acute hyper­
ventilation are observed, the measurements are repeated until obtaining
three or five technically acceptable recordings. We measured the Rrs at 5
Hz and 20 Hz (R5 and R20, respectively), the change in R5 and R20
(R5-R20), the Xrs at 5 Hz (X5), frequency of resonance (Fres), and
low-frequency resonance area (ALX). In general, respiratory impedance
consists of Rrs and Xrs. Rrs reflects the dissipative mechanical properties
of lung such as airway resistance (Raw), respiratory tissue resistance
(Rti), chest wall resistance (Rcw). Rrs sensitively reflects Raw which is a
major part of Rrs. In clinical settings, Rrs is higher level in asthma pa­
tients who have narrowed airway caliber than healthy individuals. Se­
vere asthma patients have higher R5-R20 than healthy individuals by air
trapping. This is called "ventilatory heterogeneity" (Kanda et al., 2010).
Xrs reflects the undissipative mechanical properties such as elasticity
and inertia of the lung and air, respectively. In general, Xrs show
negative value at a low frequency and positive value at a high frequency.
The higher elastic properties indicate more negative Xrs and the higher
inertial properties indicates more positive Xrs. Fres is defined as the
frequency where elasticity and inertia are balanced. Hence Xrs is zero. In
patients with asthma, X5, Fres and ALX were significantly correlate with
FEV1 and exhaled nitric oxide, which suggesting that these measure­
ments may indicate airway obstruction and ventilator unevenness
(Shirai et al., 2013).
2.4. Respiratory function and maximal respiratory muscle pressure
Respiratory function was measured with spirometry (Chestgraph HI-
105; CHEST, Tokyo, Japan). FVC, FEV1, FEV1/FVC, and peak expiratory
flow (PEF) were measured. In accordance with the specifications of the
American Thoracic Society/European Respiratory Society (2005)
(Miller et al., 2005), subjects performed at least three forced respira­
tions, from the total lung capacity to residual volume, with 2 min in­
terval between them, and the highest value was considered. The
maximal respiratory pressure was measured by manometer (Chestgraph
HI-801; CHEST, Tokyo, Japan). Based on the procedures described by
American Thoracic Society/European Respiratory Society (2002),
maximum expiration and inspiration were performed at the total lung
capacity and the residual volume, respectively. Expiration and inspira­
tion were maintained for 3 s and measured three times with 2 min in­
tervals. The highest value was considered as the maximal expiratory
muscle pressure (PEmax) and the maximal inspiratory muscle pressure
(PImax), respectively.
2.5. Statistical analysis
To compare DL, XA, and CL conditions, the repeated one-way anal­
ysis of variance (ANOVA) was conducted. In the case of a significant by
F-test, we used the post-hoc pairwise Bonferroni test. Variables are re­
ported as mean ± standard deviation (SD). Statistical significance was
set a priori at P < 0.05 for two-sided tests, and statistical analyses were
performed by SPSS statistics 26.0 (IBM Inc, Chicago, IL).
3. Results
Due to technical problems erroneous data, such as Fres = 0, were
shown in two subjects. Therefore, nine subjects were analyzed for Fres,
X5 and ALX.
Fig. 1 shows the response of respiratory impedance to water im­
mersion. R5 exhibited significant condition differences (F = 9.882, P =
D. Hoshi et al. Respiratory Physiology & Neurobiology 295 (2022) 103779

Fig. 1. A) The airway resistance at 5 Hz (R5),

B) at 20 Hz (R20), C) the difference between R5
and R20 (R5-R20), D) the reactance at 5 Hz
(X5), E) frequency of resonance (Fres), and F)
low-frequency resonance area (ALX) measured
by forced oscillation technique during water
immersion conditions (clavicle level: CL, xi­
phoid appendix level: XA) and dryland condi­
tion (DL). Circle and error bars are presented
mean ± standard deviation (SD). Gray lines
indicate individual changes. *vs. dryland con­
dition. P-value for the repeated one-way anal­
ysis of variance was < 0.05.

0.001), and was significantly higher in the water immersion conditions

Table 1
(CL and XA) than DL condition (P = 0.005 and P = 0.024, respectively).
Comparison of spirometric data and maximal respiratory muscle pressure be­
R20 exhibited significant condition differences (F = 5.400, P = 0.013).
tween water immersions (clavicle and xiphoid appendix level) and dryland.
Specifically in CL, R20 was significantly higher than DL (P = 0.003),
Clavicle Xiphoid Dry land P-value
whereas R5-R20 did not show significant differences between each
appendix (ANOVA)
condition (F = 2.484, P = 0.109). × 5 showed significant condition
differences (F = 8.591, P = 0.003). The water immersion conditions (CL FVC (L) 4.05 ± 0.39 4.19 ± 0.41 4.37 ± 0.007
* 0.36
and XA) showed significantly lower X5 when compared with DL (P =
FEV1 (L) 3.52 ± 0.47 3.65 ± 0.49 3.82 ± 0.003
0.032 and P = 0.031, respectively). Fres showed significant condition * 0.36
differences (F = 7.965, P = 0.004). In water immersion conditions (CL FEV1/FVC 87.7 ± 7.2 88.3 ± 6.6 88.6 ± 5.7 0.663
and XA), Fres was significantly higher than DL (P = 0.046 and P = 0.010, (%)
PEF (L/s) 9.65 ± 1.90 9.65 ± 2.59 10.01 ± 0.722
respectively). ALX exhibited significant condition differences (F =
0.71
6.108, P = 0.033), and was significantly higher in XA than DL (P = PImax 107.9 ± 114.6 ± 20.1 119.5 ± 0.327
0.028). (cmH2O) 37.6 24.8
Table 1 shows the results of respiratory function and maximal res­ PEmax 118.7 ± 131.2 ± 24.1 127.8 ± 0.133
piratory muscle pressure. FVC and FEV1 exhibited significant condition (cmH2O) 31.6 29.9

differences (F = 6.513, Р = 0.007 and F = 8.038, Р = 0.003, respec­
tively), and they were significantly lower in CL than DL (P = 0.029 and P
= 0.010, respectively). FEV1/FVC and PEF did not show significant
difference between conditions (F = 0.420, P = 0.663 and F = 0.332, P =
0.722, respectively). Furthermore, PImax and PEmax did not exhibit
significant difference between conditions (F = 1.182, P = 0.327 and F =
2.233, P = 0.133, respectively).
4. Discussion
The main findings from this study are as follows. Respiratory
impedance (R5, X5 and Fres) was significantly higher during water
Data are presented in mean ± standard deviation (SD). *vs. Dry land condition.
P-value are calculated by the repeated one-way analysis of variance. ANOVA =
analysis of variance. FVC = Forced vital capacity, FEV1 = Forced expiratory
volume in one second, PEF = Peak expiratory flow, PImax = Maximal inspira­
tory muscle pressure, PEmax = Maximal expiratory muscle pressure.
immersion above the xiphoid appendix than in the dryland condition.
These findings suggested that even a water immersion at xipohid level
used in public swimming pool may place a load on respiratory system.
Below we discuss the potential mechanisms and clinical implications of
our findings.

3
D. Hoshi et al.
4.1. Airway impedance measured
R5 were higher in water immersion conditions than a land condition.
These changes may be explained by following two mechanisms. Firstly,
the displacement of the diaphragm during water immersion acts to assist
expiration. In previous research, water immersion at the cervical level
markedly reduces expiratory reserve volume (Agostoni et al., 1966;
Buono, 1983). Thus, the alveolar size at the end of tidal expiration is
smaller during water immersion than on dryland, which may decrease
the expiratory residual volume. Secondly, increased venous return
during water immersion causes increased cardiac output and central
blood volume, which decreases lung compliance and vital capacities
(Bréchat et al., 2013; Johansen et al., 1997; Pendergast and Lundgren,
2009). The accumulation of blood in the chest cavity may suppress the
expansion of the lung and the recovery from the decreased functional
residual volume at the inspiration phase. Collectively, these factors not
only may decrease lung capacity and alveolar size but also may narrow
the airway caliber.
Interestingly, although previous studies and our result have reported
that respiratory function measured by spirometry is remarkably
decreased in neck water immersion (Dahlbäck et al., 1978; de Andrade
et al., 2014), airway resistance such as R5, X5 and Fres in the present
study was significantly higher in the water immersion at xiphoid level
than dryland condition. In addition, there was no significant difference
in airway resistance between the clavicular and xiphoid appendix water
immersion conditions. These different results may be because FEV1
measured by spirometry is mainly influenced by vital capacity, whereas
airway resistance may be influenced by increased central blood.
Decreased vital capacity was caused by at least in neck water immersion.
During immersion in xiphoid water level, while the effect of hydrostatic
pressure on the diaphragm is estimated at -4.5 cmH2O, which relatively
lower than neck water immersion (-14 cmH2O) (Agostoni et al., 1966),
the central blood volume associated with the venous return is signifi­
cantly enhanced even in xiphoid water immersion (Carter et al., 2014).
Suggesting that higher airway resistance during shallower water im­
mersion may be due to cardiovascular response.
High R5-R20 indicates the ventilation heterogeneity seen in patients
with severe asthma and COPD (Grimby et al., 1968). In this study, the
two water immersion conditions showed high R5 as well as high R20.
Therefore, R5-R20 was a low value in water immersion conditions and
exhibited no significant differences between all conditions. Suggesting
that the water immersion in present study may not cause ventilatory
heterogeneity in healthy adults. This finding may provide new insights
into underwater exercise therapy. However, further study is necessary to
determine whether water immersion causes ventilatory heterogeneity in
elderly or patients with respiratory diseases because the subjects in
present study were healthy men.
Xrs represents the sum of elasticity and inertia at a given frequency.
Elastic properties are causing negative values and inertial components
due to moving air result in positive values. Fres is the point determined
by balancing the elasticity and inertia. Therefore, the lower X5 and the
higher Fres indicates lung elastic resistance (Takeichi et al., 2019). In
water immersion conditions, X5 was significantly lower and Fres was
significantly higher than dryland condition. During immersion, water
pressure enhances venous return, resulting in decreased pulmonary
compliance (Bréchat et al., 2013). The increase in venous return occurs
even at relatively lower water levels such as the xiphoid appendix level
(Carter et al., 2014). Therefore, X5, the elasticity part of Xrs, became
higher in water immersion conditions than land condition, and our re­
sults are consistent with previous studies.
4.2. Respiratory function and maximal respiratory muscle
In this study, the FVC and FEV1 were significantly lower only at the
clavicular level, while the FEV1/FVC and peak expiratory flow did not
show significantly between conditions. These findings are consistent
4
Respiratory Physiology & Neurobiology 295 (2022) 103779
with those reported in previous studies (de Andrade et al., 2014). Based
on the literature, the effect of hydrostatic pressure decreases the total
lung capacity but does not change the residual volume which is the
respiratory dead space (Buono, 1983). Thus, the decreased FVC can be
explained by the decreased vital capacity out of total lung capacity. FEV1
is mainly used to assess intrathoracic airway obstruction and is adapted
to bronchodilator and bronchoconstriction responses in clinical settings.
However, water immersion may cause a decrease in total lung volume,
airway obstruction, and loss of lung elasticity, and these factors can
explain the decreased FEV1 in the present study.
Maximal inspiratory muscle pressure tended to decrease with
increasing water depth, but there was no significant difference between
conditions. From a mechanical perspective, the pressure of the abdom­
inal cavity is higher than that of the thoracic cavity during water im­
mersion because the deeper the water level, the higher the pressure.
Therefore, the diaphragm, which separates the thoracic and abdominal
cavities, is displaced to vertical direction, and interfered with inspira­
tion. In previous studies, water immersion up to the neck significantly
reduces or tends to reduce inspiratory muscle strength (de Andrade
et al., 2014; Schoenhofer et al., 2004). Our results may be due to dif­
ferences in sample size from previous studies and magnitude of mea­
surement variability between subjects by the difficulty of measurement.
4.3. Conclusions
The present study demonstrated that the airway impedance
measured by FOT during water immersion above xiphoid appendix level
was higher than non-immersion condition.
Funding
This work was supported by the Japan Society for the Promotion of
Science [grant numbers 20K11303, KW]. The data in this study are
presented clearly, honestly, and without fabrication, falsification, or
inappropriate data manipulation.
Declaration of Competing Interest
The authors declare that they have no potential conflict of interest.
Acknowledgements
The authors would like to thank all participants who took in this
study.
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