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Ultrasonographic changes and impact factors of diaphragmatic function in patients with obstructive sleep apnea–hypopnea syndrome

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Zhijun Wang
Zhijun Wang
Zhijun Wang
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Jing Li
Jing Li
Jing Li
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Yingchun Zhang
Yingchun Zhang
Yingchun Zhang
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Rui Chen
Rui Chen
Rui Chen
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Abstract and Figures

Purpose Diaphragmatic impairment has been reported in obstructive sleep apnea–hypopnea syndrome (OSAHS) patients. However, the risk factors of diaphragmatic dysfunction are unclear. This study was conducted to evaluate the diaphragmatic function and to investigate impact factors of ultrasonographic changes of the diaphragm in OSAHS patients. Methods This cross-sectional study recruited 150 snoring patients. All patients were divided into the control group (AHI < 5/h, n = 20), the mild-to-moderate OSAHS group (5/h ≤ AHI ≤ 30/h, n = 61), and the severe OSAHS group (AHI > 30/h, n = 69). Diaphragmatic thickness at function residual capacity (TFRC) and total lung capacity (TTLC) were measured by two-dimensional ultrasound, and the diaphragmatic excursion during tidal and deep breath was measured by M-mode ultrasound. The diaphragmatic thickening fraction (TF) was calculated. Spearman analysis and multiple linear stepwise regression analysis were conducted to analyze the impact factors of diaphragmatic function. Results TFRC in the control group, mild-to-moderate OSAHS group, and severe OSAHS group was 1.23 (1.10, 1.39) mm, 1.60 (1.43, 1.85) mm, and 1.90 (1.70, 2.25) mm; TTLC was 2.75 (2.53, 2.93) mm, 3.25 (2.90, 3.55) mm, and 3.60 (3.33, 3.90) mm, and TF was 119.23% (102.94, 155.97), 96.55% (74.34, 119.11), and 85.29% (60.68,101.22). There were across-group significant differences in TFRC, TTLC, and TF (P < 0.05). The oxygen desaturation index was the influencing factor of TFRC, TTLC, and TF (P < 0.05). Conclusion The diaphragm is thickened and diaphragmatic contractility is decreased in OSAHS patients. Nocturnal intermittent hypoxia is a risk factor for diaphragmatic hypertrophy and impaired diaphragmatic contractility.
a The diaphragm was imaged as the non-echogenic muscular layer outlined by the membranes of the peritoneum and diaphragmatic pleura. Diaphragmatic thickness at functional residual capacity was 2.2 mm, and diaphragmatic thickness at total lung capacity was 3.7 mm in an OSAHS patient with AHI = 57.3 events/h. The diaphragmatic thickening fraction was (3.7 − 2.2)/2.2 = 68.18%. b Ultrasound imaging of diaphragmatic excursion during tidal breath(Δm) and deep breath(ΔM) in an OSAHS patient with AHI = 71.4 events /h. The echogenic line is the movement track of the diaphragm and the vertical distance between the wave crest and the wave trough is diaphragmatic excursion
a The diaphragm was imaged as the non-echogenic muscular layer outlined by the membranes of the peritoneum and diaphragmatic pleura. Diaphragmatic thickness at functional residual capacity was 2.2 mm, and diaphragmatic thickness at total lung capacity was 3.7 mm in an OSAHS patient with AHI = 57.3 events/h. The diaphragmatic thickening fraction was (3.7 − 2.2)/2.2 = 68.18%. b Ultrasound imaging of diaphragmatic excursion during tidal breath(Δm) and deep breath(ΔM) in an OSAHS patient with AHI = 71.4 events /h. The echogenic line is the movement track of the diaphragm and the vertical distance between the wave crest and the wave trough is diaphragmatic excursion
… 
A flow chart illustrating the study sample and design. COPD chronic obstructive pulmonary disease, AHI apnea–hypopnea index
A flow chart illustrating the study sample and design. COPD chronic obstructive pulmonary disease, AHI apnea–hypopnea index
… 
Comparison of diaphragmatic parameters. a Comparison of the diaphragmatic thickness at functional residual capacity. b Comparison of the diaphragmatic thickness at total lung capacity. c Comparison of the diaphragmatic thickening fraction. d Comparison of the diaphragmatic excursion during tidal breath. e Comparison of the diaphragmatic excursion during deep breath
Comparison of diaphragmatic parameters. a Comparison of the diaphragmatic thickness at functional residual capacity. b Comparison of the diaphragmatic thickness at total lung capacity. c Comparison of the diaphragmatic thickening fraction. d Comparison of the diaphragmatic excursion during tidal breath. e Comparison of the diaphragmatic excursion during deep breath
… 
Heat map of results of correlation analyses of demographic parameters, polysomnographic parameters, and diaphragmatic parameters of 130 OSAHS patients. BMI body mass index, TST total sleep time, NREM non-rapid eye movement, REM rapid eye movement, ODI oxygen desaturation index, MSaO2 Mean arterial oxygen saturation, TS90 percentage of total sleep time at oxygen saturation level < 90%, LSaO2 lowest arterial oxygen saturation, AHI apnea–hypopnea index, RRMAI respiratory-related micro-arousal index, TFRC diaphragmatic thickness at function residual capacity, TTLC diaphragmatic thickness at total lung capacity, TF diaphragmatic thickening fraction, Δm diaphragmatic excursion during tidal breath, ΔM diaphragmatic excursion during deep breath; *P < 0.05; **P < 0.01
Heat map of results of correlation analyses of demographic parameters, polysomnographic parameters, and diaphragmatic parameters of 130 OSAHS patients. BMI body mass index, TST total sleep time, NREM non-rapid eye movement, REM rapid eye movement, ODI oxygen desaturation index, MSaO2 Mean arterial oxygen saturation, TS90 percentage of total sleep time at oxygen saturation level < 90%, LSaO2 lowest arterial oxygen saturation, AHI apnea–hypopnea index, RRMAI respiratory-related micro-arousal index, TFRC diaphragmatic thickness at function residual capacity, TTLC diaphragmatic thickness at total lung capacity, TF diaphragmatic thickening fraction, Δm diaphragmatic excursion during tidal breath, ΔM diaphragmatic excursion during deep breath; *P < 0.05; **P < 0.01
… 
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Vol.:(0123456789)
Sleep and Breathing (2024) 28:1319–1327
https://doi.org/10.1007/s11325-024-03010-7
SLEEP BREATHING PHYSIOLOGY ANDDISORDERS • ORIGINAL ARTICLE
Ultrasonographic changes andimpact factors ofdiaphragmatic
function inpatients withobstructive sleep apnea–hypopnea
syndrome
ZhijunWang1· JingLi2· YingchunZhang2· RuiChen1,3
Received: 20 August 2023 / Revised: 22 January 2024 / Accepted: 19 February 2024 / Published online: 28 February 2024
© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2024
Abstract
Purpose Diaphragmatic impairment has been reported in obstructive sleep apnea–hypopnea syndrome (OSAHS) patients.
However, the risk factors of diaphragmatic dysfunction are unclear. This study was conducted to evaluate the diaphragmatic
function and to investigate impact factors of ultrasonographic changes of the diaphragm in OSAHS patients.
Methods This cross-sectional study recruited 150 snoring patients. All patients were divided into the control group
(AHI < 5/h, n = 20), the mild-to-moderate OSAHS group (5/h ≤ AHI ≤ 30/h, n = 61), and the severe OSAHS group
(AHI > 30/h, n = 69). Diaphragmatic thickness at function residual capacity (TFRC) and total lung capacity (TTLC) were
measured by two-dimensional ultrasound, and the diaphragmatic excursion during tidal and deep breath was measured by
M-mode ultrasound. The diaphragmatic thickening fraction (TF) was calculated. Spearman analysis and multiple linear
stepwise regression analysis were conducted to analyze the impact factors of diaphragmatic function.
Results TFRC in the control group, mild-to-moderate OSAHS group, and severe OSAHS group was 1.23 (1.10, 1.39) mm,
1.60 (1.43, 1.85) mm, and 1.90 (1.70, 2.25) mm; TTLC was 2.75 (2.53, 2.93) mm, 3.25 (2.90, 3.55) mm, and 3.60 (3.33, 3.90)
mm, and TF was 119.23% (102.94, 155.97), 96.55% (74.34, 119.11), and 85.29% (60.68,101.22). There were across-group
significant differences in TFRC, TTLC, and TF (P < 0.05). The oxygen desaturation index was the influencing factor of TFRC,
TTLC, and TF (P < 0.05).
Conclusion The diaphragm is thickened and diaphragmatic contractility is decreased in OSAHS patients. Nocturnal intermit-
tent hypoxia is a risk factor for diaphragmatic hypertrophy and impaired diaphragmatic contractility.
Keywords Obstructive sleep apnea· Diaphragm· Ultrasound· Intermittent hypoxia
Introduction
Obstructive sleep apnea–hypopnea syndrome (OSAHS) is
a sleep disorder characterized by repeated collapse of the
upper airway during sleep, resulting in hypoxia, hypercap-
nia, and sleep arousals [1]. OSAHS affects up to 13.6% of
adults aged between 30 and 69years worldwide and 23.6%
in China [2]. It is strongly associated with cardiovascular
events, cognitive impairment, and metabolic dysfunction [1].
It is reported that OSAHS may also cause diaphragmatic
impairment [3, 4]. However, further studies are needed to
assess the impact of OSAHS on diaphragmatic function.
The diaphragm is the primary dome-shaped respiratory
muscle that accounts for 70% of the inspired tidal volume
[5]. Some studies have suggested that airway obstruction,
obesity, and hypoxia, which are features of OSAHS, are
potential factors leading to diaphragmatic dysfunction [6–8].
Zhijun Wang and Jing Li contributed equally to this work.
* Rui Chen
chenruigood@126.com
1 Department ofRespiratory andCritical Care Medicine, The
Second Affiliated Hospital ofSoochow University, 1055
Sanxiang Road, Suzhou, Jiangsu, China
2 Department ofUltrasound, The Second Affiliated Hospital
ofSoochow University, 1055 Sanxiang Road, Suzhou,
Jiangsu, China
3 Department ofSleeping Center, The Second Affiliated
Hospital ofSoochow University, 1055 Sanxiang Road,
Suzhou, Jiangsu, China
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Chen et al. [20] studied the characteristics of diaphragms in OSA patients and noted that patients with higher AHI tend to have thicker diaphragms with more stiffness. The main influencing factor was found to be the oxygen desaturation index, suggesting that nocturnal intermittent hypoxia was a risk factor for diaphragmatic hypertrophy and impaired diaphragmatic contractility [20]. ...
... Chen et al. [20] studied the characteristics of diaphragms in OSA patients and noted that patients with higher AHI tend to have thicker diaphragms with more stiffness. The main influencing factor was found to be the oxygen desaturation index, suggesting that nocturnal intermittent hypoxia was a risk factor for diaphragmatic hypertrophy and impaired diaphragmatic contractility [20]. Lim et al. [21] evaluated breath volumes and found that when subjects were exposed to small negative pressure at −3 cmH 2 O to induce upper airway collapsibility, their decrease in their breath volume correlated with an increase in AHI severity. ...
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We aimed at testing M-mode ultrasound diaphragmatic thickness reproducibility and its clinical correlates in healthy volunteers. Sixty-six consecutive healthy volunteers were considered eligible, and enrolled in the study. During a single visit, all participants received three M-mode and B-mode ultrasound evaluations of Diaphragmatic Thickness (DT). We then proceeded to calculate the thickness difference and assess the association of ultrasonographic measurements with demographic and anthropometric data. Variables associated through univariate analyses were entered in multivariable models, and Intraclass Correlation Coefficient (ICC) was performed in order to determine intra- and inter-observer reproducibility. Intra- and inter-observer agreements showed to be excellent through Cronbach's Alpha, ranging from 0.81 - 0.91 and 0.86 - 0.92, respectively. Mean diaphragmatic thickness measurements were: 2.6 (±0.5) mm at inhalation and 1.8 (±0.4) mm at exhalation. The results we obtained significantly varied according to gender, showing diaphragmatic motion, inspiratory/expiratory thickness and fractional thickening to be significantly lower in women. Moreover, a significantly reduced expiratory diaphragmatic thickness emerged in the subgroup of subjects having a sedentary work (p = 0.045). The crude association between expiratory thickness and active work produced a B coefficient of 0.19 (95% CI: 0.04-0.38; p = 0.045), which was confirmed after adjustments considering age and sex (B = 0.20; 95% CI: 0.01- 0.39; P = 0.037). Diaphragmatic thickness measurements using M-mode are reproducible. Intra and inter-observer agreement is high enough to support the precision of this measurement and provide a further analytic tool for a wider application in clinical practice.
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