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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 blood volume (Carter et al., 2014), which stiffens pulmonary tissue and
decreases lung compliance (Pendergast and Lundgren, 2009). While
Water immersion causes acute changes in the pulmonary physio there have been many reports of the effects of water immersion on
logical systems. Previous studies have reported that water immersion respiratory muscles and lung compliance, the effects of water immersion
cause decreased respiratory function such as forced vital capacity (FVC), on the airway are not well understood due to methodological limita
forced expiratory volume in one second (FEV1), and maximal respiratory tions. For example, FEV1, a clinical index of airway obstruction
muscle pressure (Buono, 1983; de Andrade et al., 2014). Therefore, measured by spirometry, decreases with clavicle water immersion.
these findings suggest that compared with the dryland condition, water Water immersion at the neck level has also been shown to increase
immersion places an extra load on respiratory system and may be used closing volume when compared with dryland (Bondi et al., 1976).
as a therapeutic method for improving the respiratory function. However, spirometry data are difficult to evaluate airways indepen
Previous research has reported the following two mechanisms that dently because it provides a comprehensive index of the respiratory
water immersion can directly and indirectly influence the respiratory system including respiratory muscle strength and lung compliance. In
system (e.g., airways, alveolars, and respiratory muscles). First, the in addition, closing volume may reflect decreased alveolar contractility
crease of hydrostatic pressure on the abdominal and chest cavities in rather than an airway obstruction (Kitaoka and Kawase, 2007). More
duces vertical diaphragm displacement and restricts the thorax (e.g., over, these studies have not examined the effect of shallower immersion
alveolar) expansion. As a result, respiratory muscles contract to over levels. The water depth of public swimming pools is set at 1.1–1.5 m and
come the force of water pressure (Agostoni et al., 1966). Second, hy aquatic therapy and exercise are performed at such shallower water
drostatic pressure during water immersion shifts blood from the lower level. Therefore, further study is necessary to determine the effect of
extremities to the chest cavity and increases venous return and central 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. Respiratory Physiology & Neurobiology 295 (2022) 103779
Forced oscillation technique (FOT) is an airway evaluation method measurement started after confirming stable breathing. Forced oscilla
that can solve the limitations of conventional spirometry measurements. tions are applied to the airway from the mouth to calculate the respi
FOT measurement does not require the breathing effort used in ratory impedance through the spectral relationship between the
spirometry tests and can exclude the effects of respiratory muscle and resultant pressure and airflow. The oscillatory indices are automatically
lung compliance. FOT measures the impedance of the respiratory system calculated from the mean values of five resting ventilations whose res
from the spectral relationship between the resultant pressure and piratory flow ranged between 0.5 ~ 1.0 L/s. If unnatural breathing such
airflow. The impedance is composed of respiratory system resistance as swallowing, glottis closure, leakage around the mouthpiece, incom
(Rrs) and reactance (Xrs). Rrs reflects the resistance influenced by plete sealing with the nose clip, irregular breathing, or acute hyper
airway caliber and Xrs shows elastic and inertial properties of the lung, ventilation are observed, the measurements are repeated until obtaining
which reflects an abnormality in lung parenchyma or airways (Shirai three or five technically acceptable recordings. We measured the Rrs at 5
and Kurosawa, 2016). In the bronchodilator reversibility test, the Rrs Hz and 20 Hz (R5 and R20, respectively), the change in R5 and R20
reflects airway reversibility more sensitively than FEV1 when using a (R5-R20), the Xrs at 5 Hz (X5), frequency of resonance (Fres), and
spirometer (Niimi et al., 2003). The frequency dependency of Rrs is low-frequency resonance area (ALX). In general, respiratory impedance
presumed to reflect ventilation inhomogeneity with peripheral airway consists of Rrs and Xrs. Rrs reflects the dissipative mechanical properties
lesions (Grimby et al., 1968). Therefore, the FOT is useful evaluation of lung such as airway resistance (Raw), respiratory tissue resistance
method to reflect the airway resistance during immersion. (Rti), chest wall resistance (Rcw). Rrs sensitively reflects Raw which is a
The aim of this study was to evaluate the effects of water immersion major part of Rrs. In clinical settings, Rrs is higher level in asthma pa
with different water depths on airway impedance. We hypothesized that tients who have narrowed airway caliber than healthy individuals. Se
the deeper water immersion may present higher airway impedance than vere asthma patients have higher R5-R20 than healthy individuals by air
shallower water immersion. trapping. This is called "ventilatory heterogeneity" (Kanda et al., 2010).
Xrs reflects the undissipative mechanical properties such as elasticity
2. Material and methods 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.
2.1. Participants The higher elastic properties indicate more negative Xrs and the higher
inertial properties indicates more positive Xrs. Fres is defined as the
Eleven healthy young men were recruited (23.2 ± 1.5 years old) in frequency where elasticity and inertia are balanced. Hence Xrs is zero. In
this study. The participant’s average heights and weights were 171.7 ± patients with asthma, X5, Fres and ALX were significantly correlate with
3.6 cm and 65.5 ± 4.7 kg, respectively. The average body mass index FEV1 and exhaled nitric oxide, which suggesting that these measure
(BMI) was 22.3 ± 1.6 kg/m2. All participants had no presence or history ments may indicate airway obstruction and ventilator unevenness
of pulmonary, cardiovascular, or neuromuscular disease, medication (Shirai et al., 2013).
use, current or a history of smoking. This study was carried out in
accordance with the Declaration of Helsinki and was approved by the 2.4. Respiratory function and maximal respiratory muscle pressure
Research Ethics Committee of the University of Tsukuba. All participants
gave informed consent before participation. Respiratory function was measured with spirometry (Chestgraph HI-
105; CHEST, Tokyo, Japan). FVC, FEV1, FEV1/FVC, and peak expiratory
2.2. Experimental design flow (PEF) were measured. In accordance with the specifications of the
American Thoracic Society/European Respiratory Society (2005)
The present study was conducted in randomized crossover design to (Miller et al., 2005), subjects performed at least three forced respira
compare airway impedance and respiratory function during water im tions, from the total lung capacity to residual volume, with 2 min in
mersion at different water depths. All participants were tested in the terval between them, and the highest value was considered. The
dryland (DL) and 2 water immersion conditions in random order: maximal respiratory pressure was measured by manometer (Chestgraph
clavicular immersion (CL) and xiphoid appendix immersion (XA). Water HI-801; CHEST, Tokyo, Japan). Based on the procedures described by
temperature was maintained at 35.6 ± 0.5 ◦ C, which temperature was American Thoracic Society/European Respiratory Society (2002),
the smallest effect on metabolic system in previous report (Craig and maximum expiration and inspiration were performed at the total lung
Dvorak, 1966). Participants were asked to refrain from exercise and capacity and the residual volume, respectively. Expiration and inspira
alcohol consumption at least 24 h and caffeine intake at least 12 h before tion were maintained for 3 s and measured three times with 2 min in
each experimental condition. Before experiment, participants were tervals. The highest value was considered as the maximal expiratory
familiarized to the FOT, spirometry, and maximal respiratory muscle muscle pressure (PEmax) and the maximal inspiratory muscle pressure
pressures assessments according to the previous studies (Miller et al., (PImax), respectively.
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 2.5. Statistical analysis
familiarize themself with the laboratory environment. Then, they
entered the empty bathtub (DL) or bathtub at each water level (XA or To compare DL, XA, and CL conditions, the repeated one-way anal
CL) for 10 min and performed airway impedance, respiratory function, ysis of variance (ANOVA) was conducted. In the case of a significant by
and maximal respiratory muscle pressure measurements. All conditions F-test, we used the post-hoc pairwise Bonferroni test. Variables are re
started with FOT followed by respiratory function and respiratory ported as mean ± standard deviation (SD). Statistical significance was
muscle pressure measurements. To exclude the influence of each con set a priori at P < 0.05 for two-sided tests, and statistical analyses were
dition, the interval between each condition was given at least 72 h. performed by SPSS statistics 26.0 (IBM Inc, Chicago, IL).
Respiratory impedance was measured in sitting position with the Due to technical problems erroneous data, such as Fres = 0, were
FOT (Mostgraph-01; CHEST, Tokyo, Japan). The subjects wore a nose shown in two subjects. Therefore, nine subjects were analyzed for Fres,
clip and were asked to perform tidal breathing on the mouthpiece X5 and ALX.
without leakage. They supported their cheeks to eliminate upper airway Fig. 1 shows the response of respiratory impedance to water im
shunting during measurements (Shirai and Kurosawa, 2016). The mersion. R5 exhibited significant condition differences (F = 9.882, P =
2
D. Hoshi et al. Respiratory Physiology & Neurobiology 295 (2022) 103779
differences (F = 6.513, Р = 0.007 and F = 8.038, Р = 0.003, respec Data are presented in mean ± standard deviation (SD). *vs. Dry land condition.
tively), and they were significantly lower in CL than DL (P = 0.029 and P P-value are calculated by the repeated one-way analysis of variance. ANOVA =
= 0.010, respectively). FEV1/FVC and PEF did not show significant analysis of variance. FVC = Forced vital capacity, FEV1 = Forced expiratory
difference between conditions (F = 0.420, P = 0.663 and F = 0.332, P = volume in one second, PEF = Peak expiratory flow, PImax = Maximal inspira
0.722, respectively). Furthermore, PImax and PEmax did not exhibit tory muscle pressure, PEmax = Maximal expiratory muscle pressure.
significant difference between conditions (F = 1.182, P = 0.327 and F =
2.233, P = 0.133, respectively). immersion above the xiphoid appendix than in the dryland condition.
These findings suggested that even a water immersion at xipohid level
4. Discussion used in public swimming pool may place a load on respiratory system.
Below we discuss the potential mechanisms and clinical implications of
The main findings from this study are as follows. Respiratory our findings.
impedance (R5, X5 and Fres) was significantly higher during water
3
D. Hoshi et al. Respiratory Physiology & Neurobiology 295 (2022) 103779
4.1. Airway impedance measured with those reported in previous studies (de Andrade et al., 2014). Based
on the literature, the effect of hydrostatic pressure decreases the total
R5 were higher in water immersion conditions than a land condition. lung capacity but does not change the residual volume which is the
These changes may be explained by following two mechanisms. Firstly, respiratory dead space (Buono, 1983). Thus, the decreased FVC can be
the displacement of the diaphragm during water immersion acts to assist explained by the decreased vital capacity out of total lung capacity. FEV1
expiration. In previous research, water immersion at the cervical level is mainly used to assess intrathoracic airway obstruction and is adapted
markedly reduces expiratory reserve volume (Agostoni et al., 1966; to bronchodilator and bronchoconstriction responses in clinical settings.
Buono, 1983). Thus, the alveolar size at the end of tidal expiration is However, water immersion may cause a decrease in total lung volume,
smaller during water immersion than on dryland, which may decrease airway obstruction, and loss of lung elasticity, and these factors can
the expiratory residual volume. Secondly, increased venous return explain the decreased FEV1 in the present study.
during water immersion causes increased cardiac output and central Maximal inspiratory muscle pressure tended to decrease with
blood volume, which decreases lung compliance and vital capacities increasing water depth, but there was no significant difference between
(Bréchat et al., 2013; Johansen et al., 1997; Pendergast and Lundgren, conditions. From a mechanical perspective, the pressure of the abdom
2009). The accumulation of blood in the chest cavity may suppress the inal cavity is higher than that of the thoracic cavity during water im
expansion of the lung and the recovery from the decreased functional mersion because the deeper the water level, the higher the pressure.
residual volume at the inspiration phase. Collectively, these factors not Therefore, the diaphragm, which separates the thoracic and abdominal
only may decrease lung capacity and alveolar size but also may narrow cavities, is displaced to vertical direction, and interfered with inspira
the airway caliber. tion. In previous studies, water immersion up to the neck significantly
Interestingly, although previous studies and our result have reported reduces or tends to reduce inspiratory muscle strength (de Andrade
that respiratory function measured by spirometry is remarkably et al., 2014; Schoenhofer et al., 2004). Our results may be due to dif
decreased in neck water immersion (Dahlbäck et al., 1978; de Andrade ferences in sample size from previous studies and magnitude of mea
et al., 2014), airway resistance such as R5, X5 and Fres in the present surement variability between subjects by the difficulty of measurement.
study was significantly higher in the water immersion at xiphoid level
than dryland condition. In addition, there was no significant difference 4.3. Conclusions
in airway resistance between the clavicular and xiphoid appendix water
immersion conditions. These different results may be because FEV1 The present study demonstrated that the airway impedance
measured by spirometry is mainly influenced by vital capacity, whereas measured by FOT during water immersion above xiphoid appendix level
airway resistance may be influenced by increased central blood. was higher than non-immersion condition.
Decreased vital capacity was caused by at least in neck water immersion.
During immersion in xiphoid water level, while the effect of hydrostatic Funding
pressure on the diaphragm is estimated at -4.5 cmH2O, which relatively
lower than neck water immersion (-14 cmH2O) (Agostoni et al., 1966), This work was supported by the Japan Society for the Promotion of
the central blood volume associated with the venous return is signifi Science [grant numbers 20K11303, KW]. The data in this study are
cantly enhanced even in xiphoid water immersion (Carter et al., 2014). presented clearly, honestly, and without fabrication, falsification, or
Suggesting that higher airway resistance during shallower water im inappropriate data manipulation.
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 Declaration of Competing Interest
two water immersion conditions showed high R5 as well as high R20.
Therefore, R5-R20 was a low value in water immersion conditions and The authors declare that they have no potential conflict of interest.
exhibited no significant differences between all conditions. Suggesting
that the water immersion in present study may not cause ventilatory Acknowledgements
heterogeneity in healthy adults. This finding may provide new insights
into underwater exercise therapy. However, further study is necessary to The authors would like to thank all participants who took in this
determine whether water immersion causes ventilatory heterogeneity in study.
elderly or patients with respiratory diseases because the subjects in
present study were healthy men. References
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