Q J Med 2000; 93: 647-654
© 2000 Association of Physicians
Review |
Snoring, sleep apnoea and stroke: chicken or scrambled egg?
From the Department of Respiratory Medicine, Freeman Hospital, Newcastle upon Tyne, UK
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Introduction |
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 Top Introduction Obstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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Several case-control studies1–6 have suggested that snoring is one of the factors associated with an increased risk of stroke. Snoring is, of course, a cardinal feature of the obstructive sleep apnoea syndrome (OSA), leading some authors1,4,7 to conclude that any risk associated with snoring is likely attributable to the minority of subjects in the snoring population who have OSA. Whether snoring and/or OSA independently increase the risk of stroke remains contentious, mainly because of potential confounding of the association by well-established risk factors such as obesity and hypertension.
Other studies have shown a high prevalence of sleep apnoea shortly after stroke.8–12 To what extent is this a consequence of the stroke, and how much does it reflect pre-existing sleep apnoea? Furthermore, in view of the dearth of information in healthy subjects of the appropriate age, are the post-stroke findings as abnormal as they seem?
Snoring and the risk of stroke
In case-control studies of the risk factors for stroke, patients (and usually family members) are asked whether they snored before the stroke, using the simple question ‘how often do you snore?’ with the possible answers: always or almost always, often, occasionally or never. Comparisons are made with answers from a similarly-aged control group, either paired or non-paired, and recruited either from the same community as the index cases or from other hospital in-patients. The results of six such retrospective studies1–6,13 are summarized in Figure 1
in terms of odds ratios. In each of these studies, snoring was primarily categorized as present with answers ‘always’, ‘almost always’ or ‘often’ and as absent with answers ‘occasionally’ or ‘never’. On univariate analysis, the results are generally consistent, with five of the six studies showing a significantly increased likelihood of stroke in snorers. Of note, the two studies6,13 which included only patients with first-ever strokes showed the lowest odds ratios, a point which may be relevant in light of the reports of sleep apnoea post stroke.8–12 In three of the case-control studies3–5 the odds ratio was adjusted for possible confounding factors such as obesity and hypertension. Although the values fell (Figure 1), they remained statistically significant.
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Statistical adjustment for potential confounding factors is open to criticism, however, notably if adjustment is made for factors which may themselves be on the putative ‘causal pathway’. This applies particularly to hypertension as, if snoring and/or sleep apnoea are truly independent risk factors for stroke, hypertension offers a likely mechanism. Removal of its effect might then ‘over-adjust’ the apparent risk and conceal a real cause and effect relationship.
Case-control studies are inevitably dependent on retrospective information and possible recall bias, and other types of study have suggested a weaker association between snoring and stroke (Figure 1
). For example, the only published cross-sectional prevalence study14 showed no apparent association, and one prospective cohort incidence study15 with follow up over 3 years showed a relative risk of stroke in snorers of 1.40, which was not statistically significant. In a second prospective study over 7 years,16 the relative risk of snorers developing a stroke was 1.75 (95% CI 1.02–3.0) but, after adjustment for possible confounding factors, this fell to a non-significant value of 1.26.
More convincing prospective, observational evidence comes from the large (71 779 female subjects) Nurses Health Study.17 A recent report based on this cohort has demonstrated an age-adjusted relative risk (RR) of stroke of 1.60 (1.21–2.12) for occasional snorers and 1.88 (1.62–2.53) for regular snorers. When corrected for body mass index and other co-variates, this remained significant for occasional snorers, with an RR of 1.42 (1.07–1.89) but became non significant for regular snorers, RR 1.35 (0.91–1.99).
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Obstructive sleep apnoea and the risk of stroke |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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The balance of evidence therefore clearly shows an association between ‘snoring’ and stroke. Of further interest is whether, within the snoring population, it is the minority with OSA who account for the apparently increased risk. It should, however, be borne in mind that snoring and OSA represent a continuum, within which patients are categorized by arbitrary criteria. Increasingly it is recognized that many patients have breathing-related sleep disturbance with frequent transient arousals, yet with objective findings falling short of the conventional definitions of OSA. Such individuals with the so-called ‘upper airway resistance syndrome’ may have similar symptoms and similar recurrent nocturnal surges of autonomic activity causing transient hypertension18 to those seen in patients with ‘classical’ OSA.
Systemic hypertension offers a plausible mechanism for an association between OSA and stroke but the relation between OSA and hypertension has itself been a matter of considerable controversy. This has centred in particular around whether sleep apnoea contributes to sustained daytime hypertension (over and above the clearly demonstrable surges of blood pressure during sleep associated with the autonomic effects of periodic transient arousal). A recent prospective study19 has demonstrated a ‘dose-related’ association between the severity of sleep apnoea and the development of hypertension in the 4 years following the sleep study. This and related epidemiological20 and experimental studies21 have produced convincing evidence that sleep apnoea is an independent risk factor for hypertension. Other factors that might contribute to an association between OSA and stroke include the effects of apnoeas on cerebral perfusion22 and possible effects of adrenergic stimulation on platelet function23 and the fibrinolytic system.24
In some of the case-control studies of snoring discussed above, the authors have attempted to identify within their populations those snoring subjects more likely to have OSA. One approach is to reclassify subjects by their answers to the simple snoring question in order to identify those with ‘habitual’ snoring, on the basis that they are more likely than intermittent snorers to have OSA. To this end, habitual snoring is defined by the responses ‘always’ or ‘almost always’. Other clues to pre-existing OSA include identifying snorers who also have either witnessed apnoeas or daytime sleepiness.
In two of the case control-studies1,6 where snoring subjects were reclassified, the odds ratios associated with ‘habitual’ snoring increased considerably in comparison with the simple yes/no definition. Categorization of the subjects in other ways, however, has given conflicting results: the addition of witnessed apnoeas to snoring increased the odds ratio in one study1 but had only a marginal effect in two others4,6 while in one study,4 the odds ratio increased only slightly for snorers who also had daytime sleepiness.
Other potentially useful pieces of evidence include the time of day at which the stroke occurred and the type of stroke, whether cerebral haemorrhage or infarct. Although in one study4 snoring was associated more closely with sleep related strokes than with strokes later in the day, this was not confirmed in two other studies.3,6 If systemic hypertension were the link between snoring and/or sleep apnoea and stroke, it might be expected that snoring would be associated with an excess of haemorrhagic strokes in comparison with infarcts but in one study25 this proved not to be the case.
The evidence on snoring and/or sleep apnoea as independent risk factors for stroke therefore remains inconclusive. It seems unlikely that non-habitual snoring carries a significant risk, but the evidence on habitual snoring (which may be a marker of OSA) is more persuasive. A similar conclusion that any risk of snoring was probably attributable to OSA was reached in a review 10 years ago,7 and it is unlikely that further retrospective studies will clarify the situation. Long-term prospective studies with objective measurements of sleep apnoea in large populations are required in order to assess the true risk of stroke in subjects with snoring and OSA. Such a study is underway in the United States and hopefully should answer this potentially important question within the next few years.
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Stroke and sleep |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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The initiation and maintenance of sleep is a complex process involving structures in the brainstem, diencephalon and forebrain and influenced by afferent impulses from all areas of the brain. It is therefore not surprising that any lesion causing significant brain injury may have an effect on sleep.
No large studies of the effects of acute stroke on sleep pattern have been reported. Reasons include the heterogeneous nature of stroke, reducing the generalizability of observations, and practical problems of polysomnography in patients who may be agitated and confused. Elderly subjects, in particular, undergoing polysomnography frequently suffer from a ‘first night effect’ with increased sleep disruption.26 Consequently interpretation of results in the unstable period shortly after stroke is particularly problematical. The difficulties of interpretation are highlighted by the report27 of one interesting patient who coincidentally suffered a large stroke in the left middle cerebral artery territory immediately after undergoing polysomnography for other indications. There was complete loss of rapid eye movement (REM) sleep in both hemispheres during the first two nights post-stroke, with reduction in duration and frequency of REM episodes for a week. EEG waveforms became slower and flatter, and the authors reported an increase in slow-wave sleep. Whether the latter is a correct interpretation, or whether the increase in slow waves actually reflected brain injury, is questionable. Sleep stage classification became difficult immediately after the stroke, as at times the patient appeared to show different sleep stages in each hemisphere. Indeed, on occasion the uninvolved hemisphere was reported asleep while the infarcted side was awake.
In a further report,28 polysomnography was performed on 18 patients on three successive nights following acute stroke. Nine of these lost all REM episodes in the first 48 h post-stroke and the others showed significant reduction in REM sleep. The patients with complete loss of REM sleep had a worse prognosis than the others. There appears to be gradual recovery of REM sleep over time,28 but reports on longer-term effects of stroke on sleep structure suggest a reduced proportion of REM sleep in right hemisphere strokes,28,30 left hemisphere strokes being associated with less slow-wave sleep.31
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Sleep apnoea following stroke |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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Several authors have reported a high prevalence of sleep apnoea following stroke8–12,31–35 (Table 1
). Many of the studies were uncontrolled, but three of the four with control groups showed a significantly higher AHI in the patients. However in one report33 there was no significant difference in AHI between paired community controls and ‘good outcome’ stroke patients, living independently at 3 months.
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There are important limitations to all of these studies, particularly in relation to patient selection. For example, the overall mean age of stroke is >75 years,36 yet the average age of the patients in most of these studies was <65, implying highly selected populations. This problem of patient selection is, however, often unavoidable in studies of cerebrovascular disease. The prevalence of co-existent respiratory and cardiac disease following stroke is high, so that in order to determine the true relation between acute stroke and sleep apnoea numerous exclusions are necessary, and excluded patients are more likely to be elderly. Cognitive problems may be found in up to 40% of patients in the 10 days following acute stroke and in 20% in the 3 months following.37 This often renders informed consent and detailed sleep study impossible, further reducing the potential population for study and increasing the risk of selection bias.
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Course and significance of sleep apnoea post-stroke |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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The effect of sleep apnoea on morbidity and mortality post-stroke is uncertain. Spriggs et al.3 reported a greater mortality in those with more severe snoring pre-stroke and Good et al.8 found that more severe nocturnal oxygen desaturation following stroke was associated with poorer functional outcome. Since there is also a relation between the extent of neurological impairment post-stroke and sleep apnoea severity,12 it is unclear whether more severe sleep apnoea merely reflects more severe neurological damage and consequently a worse outcome.
Figure 2 summarizes the results of studies of sleep apnoea post-stroke where the average time interval between the stroke and study is available (Because of the overlap of populations in their three papers, only the largest study by Bassetti et al.12 is included). Overall, the results suggest that the prevalence of sleep apnoea decreases with time since the stroke. Bassetti et al.12 however found no difference between sleep apnoea severity in patients with transient ischaemic attack (TIA) and stroke, and for this reason argued that sleep apnoea post-stroke probably predates the event. There was, however, a trend towards greater prevalence and severity of sleep apnoea in the stroke group in this study and furthermore, the classification of patients was clinically based and radiological evidence of cerebrovascular disease was not taken into account. On the other hand, our own data on patients studied on two occasions following stroke showed a reduction in prevalence from 94% to 76% between week 2 and week 6 post-stroke.35 Similarly, Parra et al.38 reported an improvement in sleep apnoea in the 3 months following stroke in a population of relatively non-disabled patients with stroke and TIAs. At first sight, an improvement in the TIA group is surprising, but it may be relevant that up to 36% of patients with a clinical diagnosis of TIA are found to have persistent cerebral ischaemic lesions following apparent full neurological recovery39 and the distinction between TIA, Reversible Ischaemic Neurological Deficit (RIND) and minor stroke may be quantitative rather than qualitative.40 Overall therefore, it seems likely that both pre-existing sleep apnoea and the acute effects of the stroke contribute to the various findings reported.
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Does sleep apnoea post-stroke have the same clinical implications as in patients presenting with symptoms? Probably not, as the frequency of both snoring and daytime sleepiness in patients with sleep apnoea post-stroke9,12,34 are notably less than would be expected in a sleep clinic population. The cause of daytime sleepiness in ‘classical’ OSA is generally thought to be sleep disruption due to repeated transient arousal. There is remarkably little information on arousals in the stroke population, despite several studies employing detailed polysomnography. In two studies31,34 an increased frequency of arousal was reported in stroke patients, but the increases were proportionally less than those in apnoeas and hypopnoeas, and it is not clear whether the arousals were respiratory-related.
The discrepancy between high AHI values and apparent lack of other features of OSA has parallels in epidemiological studies of sleep-disordered breathing. For example, in a large study of sleep apnoea in the community, Young et al.41 reported that 9% of healthy male adults aged 30–60 years had sleep apnoea (defined as an AHI 
15), yet only about one fifth of these had attributable symptoms. In the elderly, the frequency of such findings is even higher, with AHI>10 in as many as 62% of subjects over 65 years in one study.42 Thus, the very high frequencies reported post-stroke are much less dramatic when considered in the appropriate context.
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Type of apnoea/hypopnoea |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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Although some studies are notably noncommittal when describing apnoea type, published data suggest that the majority of apnoeas recorded after stroke are obstructive, with between 6% and 30% of patients experiencing predominantly central (Cheyne-Stokes breathing) or mixed apnoeas.11,12 Some authors11 admit to difficulty distinguishing between obstructive apnoeas and Cheyne-Stokes breathing, and some patients after stroke show a remarkably high frequency of apnoeas even while awake.12
The mechanisms underlying obstructive and central events post-stroke may actually be similar. In general, an obstructive event (apnoea or hypopnoea) occurs if the force tending to narrow or close the upper airway exceeds that required to maintain its patency. The latter force is supplied with each inspiration by contraction of the pharyngeal dilator muscles. Without effective action of these important muscles the upper airway tends to narrow or close as the intra-airway pressure during inspiration is subatmospheric. Some degree of periodic waxing and waning of respiratory drive during sleep is a normal phenomenon that tends to increase in the elderly. The increase results from slowing of either the circulation or neural conduction, increasing the lag between signal and response and thereby destabilizing respiratory control. The periodic reduction in tone of the upper airway muscles consequent on fluctuating drive causes periodic increases in upper airway resistance. Thus, a primarily ‘central’ phenomenon may result in ‘obstructive’ hypopnoea or even apnoea. Hudgel et al.43 comparing patients with previous strokes and healthy controls of similar age during sleep showed qualitatively similar fluctuations of tidal volume and upper airway resistance but the amplitude of the fluctuations was greater in the stroke patients. They speculated that this might contribute to the high number of apnoeas and hypopnoeas observed in patients after stroke. One factor determining whether a respiratory ‘event’ during sleep appears to be ‘central’ or ‘obstructive’ is the balance of inspiratory activity between the upper airway and respiratory ‘pump’ muscles (mainly the diaphragm).44 Relatively greater suppression of the former interacting with other factors such as pharyngeal size favours airway narrowing and occlusion. Disturbance of this balance has been suggested as a factor determining whether sleep-breathing events appear to be ‘central’ or ‘obstructive’ in other conditions such as generalised respiratory muscle weakness45 and chronic obstructive pulmonary disease.46 In patients after stroke, various combinations of increased instability of respiratory drive and weakness of the upper airway and ‘pump’ muscles would account for the reported findings.
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Conclusions |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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Disentangling the interrelations between snoring, sleep apnoea and stroke remains a challenge, and the clinical significance of the data is still uncertain. Potentially, the topic is of considerable importance in terms of both the risk of developing a stroke and the management of patients after a stroke. Even if the relative risk of stroke associated with snoring and/or sleep apnoea is small, the high incidence of stroke implies that the ‘population attributable’ risk would be considerable. Equally, if the clinical consequences of sleep apnoea post-stroke were similar to those usually seen with OSA, there might be considerable benefits from treatment with continuous positive airway pressure (CPAP). At present, however, there is no indication to treat patients after stroke with CPAP unless they have typical symptoms of OSA, and a randomized controlled trial would be necessary before treatment of stroke patients with asymptomatic sleep apnoea can be recommended.
Several important questions remain in this area—in particular whether sleep apnoea causes stroke or whether stroke causes sleep apnoea and whether, if correct, either is of clinical importance. At present only provisional answers can be given, based on the incomplete data available (Table 2).
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Acknowledgments |
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J.A. Harbison holds a Research Training Fellowship from the NHS Executive.
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Notes |
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Address correspondence to Professor G.J. Gibson, Department of Respiratory Medicine, Freeman Hospital, Newcastle upon Tyne NE7 7DN. e-mail: G.J. Gibson{at}ncl.ac.uk
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References |
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TopIntroductionObstructive sleep apnoea and...Stroke and sleepSleep apnoea following strokeCourse and significance of...Type of apnoea/hypopnoeaConclusionsReferences |
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