Nocturnal swallowing and arousal threshold in individuals with chronic spinal cord injury

Abstract

Respiratory complications are potential causes of death in patients with spinal cord injury (SCI). Nocturnal swallowing could be related to transient arousals and could lead to fragmented sleep in SCI patients. However, the impact of nocturnal swallowing on breathing and sleep physiology in SCI is unknown. The objectives of this study were 1) to determine whether nocturnal swallowing is more common in SCI than in able-bodied (AB) subjects, 2) to determine the role of nocturnal swallowing on arousal threshold (ArTh) in SCI individuals with sleep-disordered breathing (SDB), and 3) to determine the effect of continuous positive airway pressure (CPAP) treatment on nocturnal swallowing. A total of 16 SCI and 13 AB subjects with SDB completed in-laboratory polysomnography with a pharyngeal catheter. A swallowing event (SW) was defined as a positive spike in pharyngeal pressure and was used to calculate the swallow index (SI) defined as a number of SW/total sleep time. Each SW was assessed for a relationship to the sleep stages and respiratory cycle phases, and associated arousals and ArTh were calculated. SI was higher in the SCI group compared with AB subjects during wake and different sleep stages ( P < 0.05). SWs were found to be significantly higher in the late expiratory phase in the group with SCI compared with the other respiratory phases and were eliminated by CPAP ( P < 0.05). ArTh for the subjects with SCI was significantly lower ( P < 0.05) compared with the AB subjects. Nocturnal swallowing is more common in SCI than in AB individuals who have SDB, particularly during the expiratory phase. The ArTh is significantly lower in SCI (indicating increased arousal propensity), which may contribute to the mechanism of sleep disturbances in SCI. NEW & NOTEWORTHY Nocturnal swallowing is common in patients with chronic spinal cord injury (SCI) and is associated with frequent arousals from sleep. The lower arousal threshold during sleep in SCI may contribute to the mechanism of sleep disturbances that are commonly found in cervical and high thoracic SCI. Continuous positive airway pressure may play a therapeutic role in alleviating nocturnal swallowing, which may contribute to reduced risk of aspiration.

Keywords: arousal; arousal threshold; sleep; sleep-disordered breathing; spinal cord injury; swallowing.

Fig. 1.

A representative polygraph record in an able-bodied subject during wake demonstrating alignment of supraglottic pressure and submentalis electromyogram (EMG) with instructed swallowing. Swallows are represented by a spike in supraglottic pressure. A disruption of the flow signal can be observed during expiratory phase at the time of the swallows. $\mathrm{P}\mathrm{E}{\mathrm{T}}_{\mathrm{C}{\mathrm{O}}_{\mathrm{2}}}$; end-tidal pressure of carbon dioxide.

Fig. 2.

A representative polygraph record of a swallow with an AS during sleep in an able-bodied subject. A: brain electrical activity during sleep in two separate EEG channels, EEG(c) [records brain activity from electrode attached to the scalp near central (top) portion of the brain] and EEG(o) [records brain activity from electrode attached to the scalp near occipital (back) portion of the brain], respectively. A also shows muscle tension in the body during sleep via activity in the chin channel. B: respiratory parameters (flow, volume, and SaO₂) during sleep along with the supraglottic pressure channel, which is the main channel to depict swallow (a positive spike on the supraglottic pressure channel) during sleep. C: magnification of the highlighted portion of the P_SG channel of B to calculate the delta pressure change (Δ₁ = a–b) for the breath before arousal preceding a swallow. A and B are representatives of a sleep segment recorded on two separate sleep systems, which are time matched. AS, arousal preceding the swallow; EEG(c), electroencephalogram (central); EEG(o), electroencephalogram (occipital); SaO₂, oxygen saturation.

Fig. 3.

A representative polygraph record of a swallow with an AS during sleep in an SCI subject. A: brain electrical activity during sleep in two separate EEG channels, EEG(c) [records brain activity from electrode attached to the scalp near central (top) portion of the brain] and EEG(o) [records brain activity from electrode attached to the scalp near occipital (back) portion of the brain], respectively. A also shows measure of muscle tension in the body during sleep via activity in the chin channel. B: respiratory parameters (flow, volume, and SaO₂) during sleep along with the supraglottic pressure channel, which is the main channel to depict swallow (a positive spike on the supraglottic pressure channel) during sleep. C: magnification of the highlighted portion of the supraglottic pressure channel of B to calculate the delta pressure change (Δ₂ = a–b) for the breath before AS. A and B are representatives of a sleep segment recorded on two separate sleep systems, which are time-matched. AS arousal preceding the swallow; SCI, spinal cord injury; EEG(c), electroencephalogram (central); EEG(o), electroencephalogram (occipital); SaO₂, oxygen saturation.

Fig. 4.

A representative summary of the index of total swallows (hr⁻¹) for each sleep phase (W, N1, N2, N3, and R) in the subjects with SCI (n = 16) vs. able-bodied (AB; n = 13) subjects. *Number of swallows in the W phase is significantly higher in the subjects with SCI compared with the AB subjects (P < 0.05). ╪Wake phase is significantly higher (P < 0.001) than other event phases. The statistical test used is two-way repeated measures ANOVA (F = 76.1, P = 0.001 for sleep phase factor). All representative data are mean ± SE. N1, non-REM stage1; N2, non-REM stage2; N3, non-REM stage3; R, REM; REM, rapid eye movement; SCI, spinal cord injury; W, Wake.

Fig. 5.

A representative summary of the percent of total swallows (%) for each phase of respiration (1–4) in the subjects with SCI (n = 16) vs. able-bodied (n = 13) subjects. ╪Number of swallows is significantly higher for the phase 4 (late expiratory phase; P < 0.05), but no significant difference is noted between the subjects with SCI and able-bodied subjects. The statistical test used is two-way repeated measures ANOVA (F = 15.7, P < 0.05 for respiratory cycle phase factor). All representative data are mean ± SE. 1, beginning of inspiration to peak of inspiration; 2,  peak of inspiration to end of inspiration; 3, beginning of expiration to peak of expiration; 4, peak of expiration to end of expiration; SCI, spinal cord injury.

Fig. 6.

A summary of the delta (Δ) supraglottic pressure in the SCI (n = 6) vs. able-bodied (n = 8) subjects. *Δ supraglottic pressure is significantly reduced in the SCI subjects compared with able-bodied subjects (P < 0.05). Statistical test used is unpaired t-test (t = 2.9, P < 0.05). All representative data are mean ± SE. SCI, spinal cord injury.