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National Institute of Psychiatry and Neurology Epilepsy Centre, National Stroke Centre, Budapest, Hungary Correspondence: Anna Szűcs Received: February 15, 2001 Accepted: July 25, 2001 Key Words:Obstructive sleep apnoea, Haemorrhagic stroke, Ischaemic stroke follow-up, MESAM AbstractFrequency and severity of sleep apnoeas, snoring history, standard clinical stroke scale were assessed in 106 acute (73 ischaemic, 33 haemorrhagic) stroke patients. Thirty-seven patients with ischaemic stroke and 14 patients with cerebral bleeding, each having pathological oxygen desaturation index during sleep, were re-tested in 3 months for sleep apnoeas and clinical stroke scale. In haemorrhagic strokes, the apnoea frequency decreased parallel with clinical improvement; but it remained as frequent as in the acute phase in the ischaemic stroke group (p = 0.0002). Apnoea frequency decreased mostly during the course of posterior stroke (p = 0.0001). It is concluded that pathological sleep apnoea frequency remains stable after ischaemic stroke indicating a concomitant obstructive sleep apnoea syndrome and sleep apnoea is a transitory symptom of haemorrhagic strokes. IntroductionObstructive sleep apnoea syndrome (OSAS) is frequent in the elderly (5–40%) [1–3]. A strong association between OSAS and stroke morbidity is documented [4–11]. Depending on different OSAS criteria, it could be as frequent as 32–71% in acute stroke [12–16]. It is reported that sleep apnoea patients have a less favourable functional outcome of stroke and a higher mortality rate [13]. It is still an open question if OSAS is the cause or consequence [17–19] of cerebrovascular disorders. During the course of OSAS, sequential pathophysiological events occur, which can compromise the brain circulation. Factors which could increase the risk of ischaemic stroke include transient or chronic hypertension [20, 21], decreased blood flow in middle cerebral artery [22–25]; increased blood viscosity [26] and impaired fibrinolysis [27]; decreased venodilatory responsiveness to bradykinin [28]; impaired hypercapnic ventilatory response [29], elevated sympathetic tone [30], increased epinephrine-related platelet activation [31]; increased disposition to atherosclerosis [32, 33], and decreased vascular reactivity [34]. The strong relationship between OSAS and hypertension is well documented [36–39] and it is well known that hypertension is the most important risk factor for haemorrhagic stroke [7, 40]. In most sleep apnoea studies, haemorrhagic and ischaemic stroke patients were included and analysed together. Since in our view a different mechanism of cerebrovascular lesion necessarily implicates also a different relationship to sleep apnoeas and OSAS, we wanted to analyse ischaemic and haemorrhagic stroke patients distinctly. In this study we followed a cohort of acute ischaemic and haemorrhagic stroke patients for sleep apnoeas. Patients and Methods106 patients (73 ischaemic strokes, mean age 67 B 14 years; 45 males and 28 females and 33 haemorrhagic strokes, mean age 60 B 11 years; 25 males and 8 females) were included and screened for sleep apnoeas in 6 days after stroke (test 1). The stroke diagnosis was substantiated by clinical data and neuroimaging (CT or MRI) per- formed within 48 h after admission. Neuroimaging was repeated within 6 weeks in all patients and those with secondary haemorrhagic transformation of ischaemic infarction were excluded. From the initial population, 51 persons (37 ischaemic; mean age 64 ± 11 years; 26 men, 11 women, and 14 haemorrhagic mean age 61 ± 10 years; 11 men and 3 women) with pathological oxygen desaturation index (ODI > 10) were included in the follow-up study. Sleep apnoea screening was repeated 3 months after the first record (test 2). Sleep apnoea assessment was performed by MESAM IV, a portable device developed for home sleep-apnoea screening [41, 42]. We evaluated the main sleeping period, 4 h between midnight and 4 a.m., unless personal observation and/or manual analysis of the MESAM IV records revealed that the sleeping period of a patient occurred at a different time of the night. Then we analysed the MESAM IV record at that period (table 1).
O2 saturation values (sampling in every 2 s), snoring sound, heart rate (sampling in every second both) and body position were recorded. From the available parameters ODI: number of desaturation events of at least 3%/h; ratio of sleeping time spent below 90% haemoglobin saturation (T90), and minimal oxyhaemoglobin saturation value during sleeping time (MINSAT) were chosen to characterize breathing during sleep. All patients had a detailed medical history including risk-profile assessment. NIH stroke scale (NIHSS) was used to quantify neurological deficits at the time of the first and second sleep analysis. Snoring history was gathered from the patients or bed partners. Statistical Evaluation To assess the effects of stroke parameters and risk factors observed at test 1 on sleep apnoea parameters and NIHSS at test 2, general linear models were developed. In each model one of the four outcome measures served as dependent variable (i.e. change in DESAT, MINSAT, T90, and NIHSS). Localization of stroke (brainstem-cerebellar vs. other), stroke type (haemorrhagic or ischaemic), gender, age and risk factors as hypertension, ResultsTen patients of the initial acute stroke population (9%) died in the observational period, 7 of them had an ODI > 20/h. In the ischaemic stroke group, loud snoring before stroke was more frequent than in the haemorrhagic group (44% of men and 25% of women in the ischaemic group, 20% of men and 0% of women in the haemorrhagic group). Risk profiles of the ischaemic and haemorrhagic patients’ group were similar, except for hypercholesterolaemia, being more frequent in the ischaemic population (p = 0.002). Risk profiles of patients with pathological (ODI > 10/h) versus those with normal (ODI ≤ 10) sleep apnoea frequency were different in the ischaemic group. Those with pathological apnoea frequency snored more often before stroke (p = 0.002); there were more patients with arterial hypertension (p = 0.002) than in the nonapnoeic group. In the haemorrhagic group there was no important difference between those with pathological and ‘normal’ sleep apnoea frequency. Seventy percent of the acute ischaemic and 64% of the acute haemorrhagic stroke group had a sleep apnoea frequency characterized by ODI > l0; 45% of the ischaemic and 40% of the haemorrhagic stroke patients had a sleep apnoea frequency with an ODI > 20. Localization of stroke had no effect on sleep apnoea frequency in the acute phase. In the follow-up group improvement of NIHSS was similar in the ischaemic and haemorrhagic groups, however, changing of sleep apnoea parameters (ODI, T90, and MINSAT) was different: ODI of ischaemic stroke patients did not change, but there was a significant improvement of ODI in the haemorrhagic group (p = 0.0002) (fig. 1). Also the MINSAT and T90 values improved less in ischaemic than in haemorrhagic stroke (NS). There was no correlation between the improvement of sleep apnoea parameters and the change of NIHSS in ischaemic stroke, but there was a tendency of correlation between them in haemorrhagic stroke. MINSAT improved best (p = 0.0001) in posterior circulation haemorrhagic strokes.
There was no significant difference in the acute phase (test 1) in NIHSS values in those with normal versus those with pathologic sleep apnoea frequency, and there was no negative correlation between ODI measured in test 1 and the change of NIHSS on follow-up. DiscussionIn this study we registered pathological sleep apnoea frequency in 64–70% of acute stroke patients. Similar data were also found in other studies [12–17]. This apnoea frequency greatly exceeds prevalence values of OSAS in any age group of the general population [1–3, 43]. Three months after the acute stroke, in spite of the global clinical improvement, sleep apnoea frequency and severity were unchanged in most ischaemic stroke patients. Loud snoring, a strong indicator for OSAS [6, 44, 45], was frequent before stroke in this group. Sleep apnoea frequency and severity greatly improved in haemorrhagic strokes, tending to move along with clinical improvement; loud snoring was infrequent before stroke. We can speculate that the two major stroke types have a different relationship to pathological sleep apnoea frequency. Most cerebral bleeding is likely to cause ‘de novo’ sleep apnoeas, improving along with other symptoms. On the other hand, high sleep apnoea frequency would be a concomitant phenomenon in most ischaemic strokes that pre-existed to the cerebrovascular event, remaining unchanged, while clinical stroke symptoms improve. A recent study [46] found that central apnoeas improve on 3 months’ follow-up after acute ischaemic and haemorrhagic strokes while obstructive apnoeas remain stable. Interpreting those results together with ours we are presuming that haemorrhagic strokes lead more often to central apnoeas, and ischaemic strokes are characteristically accompanied by OSAS as a probable risk factor [5–9]. Our data suggest that for patients with pathological sleep apnoea frequency detected in the acute phase of ischaemic stroke, long-term treatment for OSAS will be necessary. In contrast, sleep apnoeas in acute haemorrhagic stroke may temporarily need special care, but would probably improve along with global clinical improvement. Our follow-up tendencies did not confirm those experiences [13] that the functional outcome after stroke is less favourable in patients having higher ODI. On the other hand, high frequency of severe sleep apnoea among those deceased after test 1, suggests an increased vulnerability in the pathological sleep apnoea group. The small study population and the great number of factors taken into account is one of the main limitations of this study. To avoid erroneous interpretations, we set the critical p value to as low as 0.0005. However, sparse data in this field induced us to report also tendencies. The MESAM IV system is a widely used tool for sleep apnoea screening. It has been is validated with polysomnography. According to these tests it has a sensitivity of 92% and a specificity of 97% in detecting sleep apnoeas [47–51]. 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