Variability of respiratory effort in relation to sleep stages in normal controls and upper airway resistance syndrome patients

doi:10.1016/S1389-9457(01)00111-3

Sleep Medicine

Volume 2, Issue 5, September 2001, Pages 397-405

https://doi.org/10.1016/S1389-9457(01)00111-3 Get rights and content

Abstract

Objective: Investigation of the role of sleep states on the respiratory effort of controls and subjects with upper airway resistance syndrome (UARS) using nasal cannula/pressure transducer system and esophageal manometry.

Patients and methods: One night's monitoring of sleep and breathing, including the determination of peak end inspiratory esophageal pressure (respiratory effort) with esophageal manometry and flow limitation with nasal cannula. Analysis of the data, breath-by-breath, using visual inspection and a computerized program. Setting – a university sleep laboratory. Patients were nine men with UARS and nine control men matched for age, ethnicity, and body mass index.

Results: A modulation of respiratory effort by sleep state and stages is seen in all subjects, the lowest noted during REM sleep and the highest associated with Slow Wave Sleep. When total nocturnal breaths are investigated, a significant difference between peak end inspiratory esophageal pressure [(Pes)-considered as an index of respiratory effort] is noted between normal subjects and UARS. Two specific breathing patterns, seen primarily in UARS patients, are NREM sleep stage dependent. Crescendos (defined as more negative peak end inspiratory Pes with each successive abnormal breath) occur mostly during stages 1–2 NREM sleep, while segments consisting of regular and continuous, breath-after-breath, high respiratory efforts are associated with Slow Wave Sleep. Depending on sleep stage, visually scored arousal response displays differences in Pes negativity. The termination of the abnormal breathing pattern, always well defined with Pes, is not necessarily associated with a pattern of ‘flow limitation’ at the nasal cannula tracing, even when a visually scored EEG arousal is present.

Conclusions: UARS patients have significantly more breaths, with more negative peak end inspiratory Pes, than do control subjects. The modulation of peak end inspiratory Pes (an index of respiratory effort) by sleep stage and state differs in UARS patients and control subjects. The nasal cannula/pressure transducer system may not detect all abnormal breathing pattern during sleep. As indicated by the visual sleep scoring, repetitive arousals may lead to more or less severe sleep fragmentation.

Introduction

Sleep disordered breathing has been subdivided into two presentations. The first, exhibiting a significant decrease in airflow lasting for more than 10 s, is associated with drops in oxygen saturation that intermittently reach a level below 90% from baseline supine and above 95% at quiet rest. This polygraphic pattern, when associated with signs and symptoms, has for more than 20 years been called ‘obstructive sleep apnea syndrome’ (OSAS). Its features are coincident with the development of a negative intra-thoracic pressure between −20 and −40 cmH₂O during sleep, and include the partial or complete collapse of the upper airway wall and persistence of obstruction despite the abnormal effort and SaO₂ drop. The termination of the obstructive ‘apnea’ or ‘hypopnea’, with a change in the central EEG lead pattern, may be defined as ‘arousal’ [1] or a switch to a stage 1 NREM sleep.

The second presentation, outlined in the early 1990s and labeled, ‘Upper Airway Resistance Syndrome’ (UARS) [2], is associated with symptoms and signs partially overlapping the above-noted syndrome but occurs with a more common/frequent complaint of ‘nocturnal sleep disruption’ than of daytime sleepiness. The polygraphic pattern presents an abnormal increase in respiratory effort occurring in tandem with some airflow limitation. The impact on tidal volume is only one to, in rare instances, three breaths before returning to normal, usually at a time of peak negative intra-thoracic pressure with very little impact on oxygen saturation (SaO₂). When studied during stage 2 NREM sleep, it was shown to be variably associated with a visually scorable short arousal (3). When not associated with a visual arousal, spectrum analysis of the EEG has shown an increase in delta activity in the central EEG lead [3], demonstrating that the problem can be partially resolved without the need of a cortical arousal (defined as presence of increase of alpha, or alpha and beta EEG waves) and indicating the possibility of reopening the airway with maintenance of sleep and subcortical reflex activation.

We questioned whether REM sleep and NREM sleep stages play a role in the negative peak end inspiratory esophageal pressure [(Pes), taken as an index of respiratory effort] noted during sleep in patients defined as having ‘UARS’ based on clinical presentation and a diagnostic nocturnal polygraphic recording. We looked at the associated nasal flow pattern measured with a nasal cannula and a pressure transducer [4]. For the purpose of comparison, an age, gender, and body mass index (BMI) matched group of non-complaining normal subjects was also investigated.

Section snippets

Patients

Nine men with a mean age of 40.2±4 years (an age range of 35–50) were included in the study. They were recruited from successively seen UARS patients who fulfilled the following inclusion criteria: male subjects with an age range of 35–50 years, body mass index below 26 kg/m², absence of drug intake or other sleep disorders, and with a signed, informed consent approved by the Internal Review Board. They reported heavy snoring at night which disturbed their own sleep and that of their bed

Polysomnography

Our nine UARS patients presented a mean total sleep time of 371±28 min, while our normal subjects slept 345±25 min with a non-significant but clear trend for normal subjects to have a shorter total sleep time. The mean stage 1 NREM was 14±2.6%, stage 2 NREM was 6.6±3.2%, stages 3–4 NREM were 13± 2.1%. REM sleep was 12.9±3% in complainers. The mean stage 1 was 16±3%, stage 2 was 52±3.5%, stages 3–4 were 12.6±3%, and REM sleep was 14±4% in controls. The mean apnea–hypopnea index (A.H.I.) was

Discussion

Our study compared well-matched normal subjects to subjects defined as UARS [2]. None had the breathing problems associated with a significant drop in oxygen saturation, but patients did have a more negative peak end inspiratory Pes (i.e. an increase in an index of respiratory effort) that was often terminated with a visually scorable EEG arousal. The abnormal breathing pattern, monitored by a nasal cannula/pressure transducer system, was not necessarily associated with a pattern of flow

Acknowledgements

Dr Guilleminault is the recipient of an Academic Award from the Center for Sleep Research of the National Heart, Lung, and Blood Institute of the NIH. Dr Dalva Poyares was supported by a fellowship from FAPESP, Sao-Paulo, Brazil.

References (20)

C Guilleminault et al.
A cause of excessive daytime sleepiness: the upper airway resistance syndrome
Chest
(1993)
C Guilleminault et al.
Clinical Investigation of obstructive sleep apnea syndrome and upper airway resistance syndrome patients
Sleep Med
(2000)
C Guilleminault et al.
Upper airway resistance syndrome: Oral–maxillo–facial
Clin N Am
(1995)
T Shiomi et al.
Leftward shift of the interventricular septum and pulsus paradoxus in OSAS
Chest
(1991)
C Guilleminault et al.
Normal pregnancy, daytime sleepiness, snoring and blood pressure
Sleep Med
(2000)
J Gaches
Activites periodiques en EEG
Rev EEG Neurophysiol
(1971)
M.G Terzano et al.
The cyclic alternating pattern sequences in the dynamic organization of sleep
Electroenceph Clin Neurophysiol
(1988)
J.E Black et al.
Upper airway resistance syndrome: Central EEG power and changes in breathing effort
Am J Resp Care Med
(2000)
J.J Hosselet et al.
Detection of flow limitation with a nasal cannula/pressure transducer system
Am J Respir Crit Care Med
(1998)

There are more references available in the full text version of this article.

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Original articleVariability of respiratory effort in relation to sleep stages in normal controls and upper airway resistance syndrome patients

Abstract

Introduction

Section snippets

Patients

Polysomnography

Discussion

Acknowledgements

Chest

Sleep Med

Clin N Am

Chest

Sleep Med

Rev EEG Neurophysiol

Electroenceph Clin Neurophysiol

Upper airway resistance syndrome: Central EEG power and changes in breathing effort

Am J Resp Care Med

Detection of flow limitation with a nasal cannula/pressure transducer system

Am J Respir Crit Care Med

Original article
Variability of respiratory effort in relation to sleep stages in normal controls and upper airway resistance syndrome patients