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(Stroke. 1996;27:252-259.)
© 1996 American Heart Association, Inc.
Articles |
Sleep-Disordered Breathing and Poor Functional Outcome After Stroke
From the Department of Neurology, Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, NC (D.C.G.), and the Departments of Neurology (D.G., J.W.), Internal Medicine (J.Q.H.), and Statistics and Research Consulting (S.V.), Southern Illinois University School of Medicine, Springfield.
Correspondence to David C. Good, MD, Department of Neurology, Bowman Gray School of Medicine, Wake Forest University, Medical Center Blvd, Winston-Salem, NC 27157-1078.
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Abstract |
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 Top Abstract IntroductionSubjects and Methods Results Discussion References |
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Background and Purpose We objectively evaluated patients with recent stroke to determine the prevalence of sleep-disordered breathing (SDB) and whether SDB was associated with unfavorable clinical outcomes.
Methods Forty-seven patients with recent ischemic stroke (median, 13 days) were studied with computerized overnight oximetry for evidence of arterial oxyhemoglobin desaturation (SaO2). Polysomnography was also performed on 19 patients. Medical history, sleep history, location of stroke, and severity of neurological deficit were recorded, and patients were observed by staff for evidence of snoring and excessive daytime sleepiness. Functional abilities were measured with the use of the Barthel Index (BI). Outcome variables included ability to return home at discharge, continued residence at home at 3 and 12 months, BI at discharge, BI at 3 and 12 months, and death from any cause at 12 months.
Results Mean SaO2 during oximetry
was 94.0±1.7%, and percentage of recording time spent at
<90% SaO2 was 4.3±5.7%. The number of
desaturation events per hour of recording time (desaturation
index [DI]) was 9.5±9.67, with 15 of 47 (32%) having DI
>10 and 6
of 47 (13%) having DI >20. Oximetry measures of SDB correlated with
lower BI scores at discharge and lower BI at 3- and 12-month
follow-ups (P
.05, Pearson coefficients). Oximetry
measures correlated with return home after discharge, but the
association between oximetry measures and living at home was lost at 12
months. Two oximetry variables correlated with death at 1 year.
Brain stem location correlated with higher DI and time at <90%
SaO2, but patients with hemispheric
stroke and oximetry abnormalities also had worse functional outcome. No
correlation was found between oximetry values and sex, age, preexisting
medical conditions (except previous stroke), or severity of
neurological deficit. Oximetry abnormalities were associated with a
history of snoring. Polysomnography on 19 patients confirmed oximetry
evidence of severe SDB. Eighteen of 19 patients (95%) had an
apnea-hypopnea index (AHI) of >10 events per hour of
recording, 13 of 19 (68%) had an AHI >20, and 10 of 19 (53%)
had an AHI >30. Desaturation events were largely due to obstructive
apneas.
Conclusions SDB accompanied by arterial oxyhemoglobin desaturation is common in patients undergoing rehabilitation after stroke and is associated with higher mortality at 1 year and lower BI scores at discharge and at 3 and 12 months after stroke. SDB may be an independent predictor of worse functional outcome. Obstructive sleep apnea appeared to be the most common form of SDB, and the frequent history of snoring suggests that SDB preceded the stroke in most patients.
Key Words: activities of daily living • rehabilitation • sleep apnea syndromes • stroke outcome
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Introduction |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Sleep-disordered breathing is a frequent clinical phenomenon,1 2 and the prevalence increases with age.3 4 5 Sleep apnea, characterized by recurrent cessation of airflow, is the most common type of SDB and may be either obstructive or central, with many patients having both types.6 7 Other periodic breathing patterns, including CSR, also occur during sleep.8 9 Recurrent hypopneas and apneas accompany all forms of SDB, often causing OxyHb desaturation, frequent arousals, and disruption of sleep architecture. Fatigue, inattention, and excessive daytime sleepiness may result. Cardiopulmonary consequences associated with hypoxemia include pulmonary hypertension with right heart failure,2 6 cardiac arrhythmias,2 10 11 12 13 systemic hypertension,2 13 14 15 16 17 18 and ischemic heart disease.13 17
There are several reasons to suspect that the prevalence of SDB is high after stroke, although few studies using objective measures have been reported. Stroke is a condition primarily of the elderly, and OSA, the most common form of SDB,6 increases with age. A history of snoring (which usually accompanies OSA) is more common in stroke patients compared with age- and sex-matched patients admitted for other conditions and is an independent risk factor for stroke.17 19 20 21 22 In a prospective study of 4368 middle-aged men, habitual or frequent snorers had an increased risk of combined heart disease and stroke, even when adjustments were made for age, obesity, history of hypertension, smoking, and alcohol use.23
It is also possible that strokes may cause SDB. Oropharyngeal muscular
dysfunction accompanies both hemispheric and brain stem
stroke.24 25 26 27 During
sleep, functional occlusion of the
airway could result in OSA, especially in persons already predisposed
to this condition. Disruption of central regulatory pathways may result
in CSA, especially in brain stem stroke.28 Finally, CSR
may occur after stroke.8 All three types of SDB (OSA, CSA,
and CSR) may coexist, and all are accompanied by OxyHb desaturation and
arousal. Two studies (both published as abstracts) using objective
measures found that 70% to 72% of patients with recent
ischemic stroke had significant SDB, defined by an AHI of 
10
events per hour.29 30 Another study found a much
higher
prevalence of sleep-related respiratory disturbances in 10
patients less than 1 year after stroke compared with matched control
subjects.31
Regardless of whether SDB precedes or follows a stroke, it may result in daytime sleepiness, inattentiveness, and impaired cognitive functioning. In our clinical experience, apneic spells and snoring are frequently observed on a stroke rehabilitation service. We postulated that SDB might affect ability to participate in a rehabilitation program and contribute to unfavorable outcomes. The purposes of this study were to (1) determine the prevalence of SDB in ischemic stroke patients hospitalized on a rehabilitation service and (2) determine whether SDB was associated with important unfavorable clinical outcomes. Continuous computerized overnight oximetry was used to monitor SaO2, and selected patients also received overnight PSG.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Fifty-five patients with recent ischemic stroke admitted to a stroke rehabilitation ward were asked to participate in the study. Eight patients refused, leaving 47 consenting patients. Median age was 69 years (range, 42 to 87 years), there were 26 men and 21 women, and time from stroke until rehabilitation admission was a median of 13 days (range, 4 to 69 days). The study was approved by the appropriate institutional review committee. None of the patients had clinically evident congestive heart failure or required supplemental oxygen. No patient had a prior diagnosis of SDB. No control subjects were studied. Location of stroke was established with the use of clinical criteria and neuroimaging procedures, which were obtained in all patients. Forty-four of 47 patients (94%) had hemispheric strokes. Stroke location was classified as follows: (1) subcortical, (2) cortical, (3) combined cortical plus subcortical, and (4) brain stem or cerebellar.
Fifteen patients (32%) had a history of previous stroke. Thirty-six (77%) had a history of smoking (mean pack-years, 43.1), but only 7 (15%) had a clinical history of chronic pulmonary disease. Other preexisting medical conditions included hypertension in 25 (53%), diabetes in 17 (36%), and prior myocardial infarction in 13 (28%). All patients had been living at home or with relatives before their stroke. Neurological examination by a board-certified neurologist was performed on all patients, and findings were recorded, including the presence or absence of dysarthria or aphasia. Severity of neurological deficit due to hemispheric stroke was classified in the manner of Reding and Potes32 into pure motor hemiparesis; hemiparesis plus hemisensory loss; and hemiparesis, hemisensory loss, plus homonymous hemianopsia. Patients with brain stem strokes were grouped separately. A Mini-Mental State score33 was obtained in patients without severe aphasia. A history of sleep habits was obtained from the patient and, when possible, the bed partner. This included a history of snoring (never, occasionally, usually, or always), apneic episodes during sleep, and inappropriate daytime sleepiness. Obesity was measured by calculating the body mass index, defined as weight (kilograms) divided by height (meters) squared.
All patients were evaluated for nocturnal SaO2
within 1 week of admission to the rehabilitation ward with the use of
continuous computerized overnight oximetry (Ohmeda Biox 3700 oximeter
with a Laser 128 computer). All hypnotics and nonessential sedating
drugs were discontinued at least 3 days before oximetry testing.
Antihypertensive medications were not stopped, and seven patients
continued to take antidepressants. Computerized (PROFOX)
analysis of oximetry data was performed with every 2-second
real-time data sampling of SaO2,
which provides a time resolution fine enough to reveal stereotypic
patterns of desaturation associated with SDB. A
simultaneous strip chart recording (appropriately
calibrated) was also done to help ensure accuracy. Oximetry
recordings were edited to eliminate data that appeared to be
artifactual (eg, due to probe dislodgment) and might mimic
desaturations due to SDB. The computerized analysis defines a
desaturation event as a 4% change in SaO2
from baseline. A rise of 4% above the nadir of a desaturation event
signals the end of that event. Mean overnight
SaO2, lowest
SaO2, total number of desaturation
events, and percentage of recording time with
SaO2 <90% were recorded. DI was
calculated by dividing the number of desaturation events by the total
recording time. Oximetry strip charts were checked frequently
during recording by certified sleep laboratory technicians for
technical accuracy, and nursing staff observed patients periodically
during the night of recording and recorded snoring, apneic
episodes, and sleep arousals. Therapists and nurses were questioned
weekly regarding the presence of excessive daytime sleepiness.
Selected patients underwent standard overnight PSG (Grass model 78D
12-channel polygraph, scored manually according to established
criteria). PSG was performed in an accredited sleep laboratory within 1
week of oximetry and interpreted by a certified sleep laboratory
physician. Oximetry criteria for performing PSG were arbitrarily
defined and included one or more of the following: (1) any desaturation
to a level 80%, (2) 5% of monitoring time with
SaO2 <90%, and (3) presence of
short-duration, repetitive desaturations. Twenty-four patients
met these criteria, but three subjects refused PSG, and the sleep
laboratory was not available to perform the study within 1 week of
oximetry in two additional patients.
Functional abilities were assessed by the BI, a widely accepted multifaceted scale that measures mobility and activities of daily living.34 BI was scored for all patients on admission and discharge from the rehabilitation unit (median stay, 30 days; range, 8 to 63 days) and by telephone interview at 3 months (±1 week) and 12 months (±1 month) after stroke onset. All personnel scoring BI were blinded to the results of sleep studies. No patients were lost to follow-up.
Primary outcome variables were as follows: (1) ability to return home at discharge, (2) ability to live at home at 3 and 12 months after stroke, (3) BI at discharge, (4) BI at 3 and 12 months after stroke, and (5) death from any cause at 12 months after stroke.
Secondary analysis included assessing the association of OxyHb desaturation with other variables, including age, aspects of medical history, prior stroke, size and location of stroke, and severity of neurological deficit.
A subgroup of 15 patients with the most frequent desaturations (DI >10/h) was also analyzed separately (DI group).
Results were analyzed by 
2 test,
Student's t test, and Pearson correlations. Pearson
correlations were chosen for the primary data analysis because
of our interest in the relationship between variables. Since the
correlation of a continuous variable with a dichotomous
variable is a special case of the Pearson correlation, it was
appropriate for this study. Probability values were used to describe
the strength of relationships, and there was no adjustment for multiple
comparisons.
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Results |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Results of overnight oximetry appear in Table 1
.
The mean overnight SaO2 was 94.0±1.7%. There
was a wide variation in the lowest recorded
SaO2, as shown in Fig 1.
Twenty-six of 47 subjects (55%) had at least one desaturation
event <80%, and 6 of 47 (13%) had at least one event <60%. The
mean number of desaturation events was 65.0±66.3, and this also
exhibited a wide variation. Nine of 47 patients (19%) had >100
desaturation events on the night of recording. The number of
desaturation events per hour of recording time (DI) was
9.5±9.6. The distribution of DI values for all patients is shown in
Fig 2. Fifteen of 47 patients (32%) had >10 events per
hour, and 6 of 47 (13%) had >20 events per hour.
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Mean admission BI was 32.7±13.3 and mean discharge BI
58.3±20.6. At 3
months after stroke onset, mean BI for 44 surviving patients was
70.7±22.8; at 12 months BI was 73.9±23.6 for 42 surviving
patients
(Table 2).
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Correlation between functional status, as measured by BI, and oximetry
measures of SDB was assessed with the use of Pearson correlation
coefficients (Table 3). Although admission BI was
correlated with time at <90% SaO2,
there was no correlation between admission BI and any other oximetry
variable. In contrast, there was a strong correlation between
multiple measures of SDB (including mean
SaO2, time at <90%
SaO2, total number of desaturation
events, and DI) and BI at discharge and improvement in BI between
admission and discharge. The strong correlation between measures of SDB
and BI persisted at 3 and 12 months after stroke. The variable that
correlated least with functional status was the lowest recorded
SaO2.
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At discharge, 35 of 47 patients (74%) had returned home or lived with
relatives. At 3 months after stroke, 34 of 44 surviving patients (77%)
were living at home, and at 12 months 33 of 42 patients (79%) were at
home (Table 2
). There was a correlation (Pearson coefficient)
with
return home at discharge and four oximetry measures: number of
desaturation events (r=.29, P=.05), mean
SaO2 (r=-.35,
P=.02), time spent at <90% SaO2
(r=.42, P=.003), and DI
(r=.29,
P=.05). By 3 months, mean SaO2
(r=-.31, P=.03) and percentage of time
spent at <90% SaO2 (r=.42,
P=.003) correlated with ability to live at home, but by 12
months after stroke, no oximetry measure obtained after stroke
correlated with continued residence at home.
Three of 47 patients died within 3 months after stroke, and a total of
5 patients were dead at the 12-month follow-up (Table 2). Death
by
1 year correlated with mean SaO2
(r=.37, P=.01) and percentage of time spent at
<90% SaO2 (r=-.41,
P=.004).
PSG was performed on 19 patients. AHI, defined as the average number of episodes of apneas and hypopneas per hour of recording, was calculated for all patients. All but 1 patient studied with PSG had an AHI >10, 13 of 19 (68%) had an AHI >20, and 10 of 19 (53%) had an AHI >30. The AHI obtained during PSG was greater than the DI obtained for the same patients during oximetry in 18 of 19 cases. The mean AHI during PSG was 35.6±23.2 compared with a mean DI of 17.7±10.5 for the same group of patients during oximetry. Desaturation events on PSG were largely obstructive in nature, but the proportion of obstructive versus central events differed between hemispheric and brain stem stroke. Of total apneas, 93.3% were obstructive in the 16 patients with hemispheric stroke, but for the 3 patients with brain stem stroke, only 58.3% of the apneas were obstructive, the rest being central. All 3 patients with brain stem stroke had severe SDB, with a mean AHI on PSG of 57.0.
Functional status in those patients with the strongest oximetry
evidence for SDB (DI group) is shown in Fig 3. Admission
BI for the 15 patients constituting the DI group was 30.3±16.7,
discharge BI was 49.3±24.1, BI at 3 months was 56.4±23.6, and BI
at
12 months was 61.2±23.0. BI values measured at the same times for the
other patients were 33.8±11.5, 62.5±17.6, 77.3±19.5, and
79.7±21.9,
respectively. Although there was no statistically significant
difference between the admission BI for the DI group and that for the
other patients, by discharge, the mean BI for the DI group was
significantly lower than that for the other patients
(P<.04, Student's t test). Patients in the DI
group continued to function worse at 3 and 12 months after stroke
compared with the other patients (P<.004 and
P<.02, respectively).
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Brain stem location of stroke correlated with DI calculated during
oximetry (r=.49, P=.0005) and number of
desaturation events (r=.50, P=.0004) but not
with
any other oximetry measures. Because all 3 patients with brain stem
stroke had PSG that demonstrated significant SDB, the data were also
analyzed after these patients were excluded (Table 4). Although
the correlation between oximetry measures
and lower BI is not as great for patients with hemispheric stroke
alone, the association is still statistically significant for mean
SaO2 and percentage of time spent at <90%
SaO2. BI at all time intervals after stroke was
not significantly different between patients with brain stem and
hemispheric strokes.
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For hemispheric strokes, there was no correlation between oximetry measures and location of stroke (cortical, subcortical, or combined cortical and subcortical). No association was found between oximetry measures and degree of neurological deficit (pure motor hemiparesis versus hemiparesis plus hemisensory loss versus hemiparesis plus hemisensory loss plus homonymous hemianopsia). The Mini-Mental State score correlated with the lowest SaO2 (r=.40, P=.04) and percentage of time with SaO2 <90% (r=-.44, P=.02). No association was found between oximetry variables and presence of dysarthria or aphasia.
Oximetry values did not correlate with sex, age, or body mass index. A history of stroke correlated with mean SaO2 (r=.32, P=.03) but no other oximetry variable. No correlation was found between oximetry values and history of any other preexisting medical condition, including prior myocardial infarction and pulmonary disease.
An adequate history of prior sleep habits, usually from the spouse, was obtained in all but 3 patients. Of these, 23 of 44 (52%) were said to usually or always snore, and 10 of 44 (23%) had apneic episodes during sleep. However, a clear history of inappropriate daytime sleepiness was obtained in only 5 patients. By Pearson correlations, a prior history of snoring correlated with the lowest recorded SaO2 (r=-.45, P=.001) and assignment to the DI group (r=-.35, P=.02). A history of previous apneic spells correlated with DI (r=-.45, P=.002) and the number of desaturation events (r=-.46, P=.002). A history of previous inappropriate daytime sleepiness did not correlate with any oximetry variable.
Nursing observations of snoring and apnea during oximetry testing showed less correlation with oximetry results than history from a sleep partner. Nursing staff observed snoring in 25 of 47 patients (53%) during the night of oximetry testing. Nursing observations of snoring did correlate with the number of desaturation events (r=.41, P=.004) and DI (r=.40, P=.005). Apneic episodes were observed by nurses in 10 of 47 patients (21%) but did not correlate with oximetry measures. There was no correlation between oximetry results and weekly reports by nurses or therapists regarding excessive daytime sleepiness, which occurred in only 5 patients.
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Discussion |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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This study confirms our clinical observation that snoring and SDB accompanied by OxyHb desaturation are common in patients undergoing stroke rehabilitation. Several studies have documented a higher prevalence of prior snoring in stroke patients compared with control subjects and have attributed an increased stroke risk to the snoring.19 20 21 22 23 However, only a few other studies used objective measures of SDB in patients with recent stroke,29 30 31 with results similar to ours. In a study of 47 patients published in abstract form,29 72% had an AHI of
10 events per hour, 53% had an AHI >20, and 30% had an AHI
>40. In another study (published in abstract form), PSG evaluations
performed in 20 consecutive patients with acute stroke revealed that 14
(70%) had significant sleep apnea.30 Mohsenin and
Valor31 performed PSG on 10 stroke patients admitted to a
rehabilitation unit and also on 10 control subjects matched for age,
body mass index, presence of hypertension, and smoking history. The AHI
in stroke patients was 52±10 events per hour compared with 3±1
events
per hour in the control group. The majority of the events were
obstructive apneas associated with SaO2
desaturation and arousal. Our study extends previous work by demonstrating that SDB after stroke is associated with higher mortality at 1 year and poor functional outcome in survivors. Only one measure of nighttime OxyHb desaturation was associated with functional abilities on admission to rehabilitation. In contrast, several oximetry variables correlated strongly with lower BI scores at the time of discharge from rehabilitation, and this association remained strong at 3- and 12-month follow-ups. The association between measures of SDB and worse functional outcome was even more dramatic for a subgroup of the study population who had >10 episodes of OxyHb desaturation per hour of recording (DI group). BI on admission for the DI group was no different than that of the other patients, but by discharge, BI was significantly lower for the DI group, a difference that remained significant at 3 and 12 months. Several oximetry measures were also associated with inability to return home after discharge from the rehabilitation program. However, no measure was associated with ability to live at home at 12 months, which is consistent with the frequent observation that ability to live at home depends on many factors, including social support systems.
Vascular mortality is higher in patients with untreated OSA,35 36 which was the most common type of SDB among those patients who received PSG in our study. Spriggs et al20 discovered a definite relationship between mortality at 6 months after stroke and severity of snoring. In our study we found a correlation between death at 1 year and two oximetry measures, which is consistent with earlier studies.
Numerous comparisons were made in this study, and there is potential for observing values of P<.05 by chance alone. However, given the number of oximetry measures that correlated with outcome measures with values of P<.05, this seems unlikely.
The reason for the association between OxyHb desaturation and worse functional outcome is unclear. Since outcome after stroke is multifactorial, we considered the possibility that SDB was a marker for other variables. However, we found no association between oximetry measures and sex, age, location of hemispheric stroke, cognitive impairment, the degree of neurological impairment, history of chronic pulmonary disease, or history of any other preexisting medical condition. We did find an association between one oximetry measure and history of prior stroke, but this is insufficient to establish a causative relationship. It is possible that the small number of patients studied may have been insufficient to demonstrate an association with another important outcome variable or that variables were overlooked. Although oximetry abnormalities were correlated with brain stem stroke, the association between SDB and worse functional outcome was still significant for hemispheric stroke patients.
One possible explanation for the association of measures of SDB and poor outcome is that patients with SDB develop subtle deficits of attention and concentration that impair their abilities to perform activities of daily living and to acquire new skills. We could not demonstrate overt excessive daytime sleepiness in our study population, but the measure used was rather imprecise and consisted of questioning nursing and therapy staff weekly regarding whether any inappropriate daytime sleepiness had been observed. We did not perform more detailed testing of attention and concentration. We did find a weak association with two oximetry readings and Mini-Mental State score. However, we cannot conclude that there was a causal relationship. Another possibility is that changes in arterial oxygen and carbon dioxide saturations that accompany SDB result in local alternations in cerebral blood flow, which in turn inhibit the process of neuronal reorganization. There is ample evidence of decreased cerebral blood flow in patients with OSA during wakefulness as well as sleep.8 37 38 39 Impaired cerebral autoregulation may also accompany OSA.13 Recurrent hypoxemia associated with SDB might be detrimental to cerebral recovery after stroke. At this time, the reason for the association of SDB and worse functional outcome remains speculative. Treatment trials of patients exhibiting SDB after stroke would help determine whether SDB is truly an independent cause of worse outcome and might shed light on the underlying mechanism of this effect.
Computerized overnight oximetry was used to screen for SDB in this
study because it is a convenient, noninvasive procedure that can be
performed easily on elderly stroke patients on a rehabilitation ward.
It is a reliable measure of SaO2 when
SaO2 is >70%.40 A limitation of
oximetry is that it fails to measure respiratory events that cause
sleep fragmentation but not OxyHb desaturation.41
Therefore, PSG remains the standard for the diagnosis of
SDB.1 41 However, oximetry alone can be of
significant
diagnostic value, with sensitivity and specificity values
dependent on the type of data analysis
used.41 42 43 44
Studies comparing the two procedures indicate that oximetry is
sensitive for detecting more severe cases of SDB but not mild
cases.41 45 For those with a high pretest probability
of
disease, finding 15 desaturations of 4% per hour of monitoring is
sufficient to confirm the diagnosis of sleep apnea with a specificity
of 98%.41
The lack of objective information regarding the duration of sleep is regarded by some as a major limitation of oximetry in screening patients for sleep apnea syndrome. However, Douglas and coworkers45 found that the AHI is abnormal in most patients in whom sleep apnea is diagnosed, whether the index is calculated per hour of sleep or per hour in bed. Farney et al46 have shown that a reasonable estimate of the duration of sleep can be made and rapid eye movement and non–rapid eye movement sleep differentiated based on analysis of the oximetry tracing alone.
Only 19 of our patients had PSG. Although this was performed based on predetermined criteria, it was not performed in 5 patients because of refusal or unavailability of the sleep laboratory. Since our primary goal was to identify a simple way to screen stroke patients for SDB, PSG was done primarily to validate the use of oximetry to identify SDB. Nevertheless, the results are instructive. Although there is no absolute PSG cutoff point for the diagnosis of SDB,1 we chose AHI >10 as a marker for SDB. All but one patient studied with PSG had an AHI >10, 13 of 19 (68%) had an AHI >20, and 10 of 19 (53%) had an AHI >30. These figures are similar to those reported by Kapen and coworkers.29 We also calculated a DI based on the number of OxyHb desaturation events >4% from baseline per hour of oximetry recording for all patients. We presume that most or all of these desaturation events were due to apneas or hypopneas. Other evidence to explain the desaturations (advanced heart/lung disease, morbid obesity) were not present, and oximetry recordings were edited to eliminate artifacts (eg, due to probe dislodgment) that might mimic desaturations due to SDB. The DI during oximetry was lower than the AHI obtained during PSG for 18 of the 19 patients who received both procedures. The mean AHI obtained during PSG for the 19 patients was a striking 35.6 events per hour compared with 17.7 events per hour for the same patients during oximetry. This discrepancy is expected, since apneas and hypopneas with either a >4% desaturation in SaO2 or a sleep arousal were scored on PSG, but only SaO2 desaturations were measured on oximetry. Nevertheless, this difference suggests that oximetry underestimated the severity of SDB in our patient population and that the scope of the problem is much greater than our oximetry data indicate.
The most common form of SDB in this study appears to have been OSA. In the patients undergoing overnight PSG, the vast majority of apneas and hypopneas recorded were obstructive in nature. Although a history of snoring does not always predict OSA documented by objective studies, a history of heavy habitual snoring provided by a sleep partner does appear to be a valid marker for OSA.17 There is suggestive evidence that SDB, particularly OSA, preceded stroke in our patients. Fifty-two percent of our patients in whom an adequate sleep history could be obtained were said to usually or always snore before the stroke, and in almost one quarter a history of apneic episodes during sleep was obtained from the bed partner. Since no age- or sex-matched control subjects were available, this information must be interpreted cautiously. However, our results are comparable to those in the study of Spriggs and coworkers,20 who obtained a history of habitual snoring in 57.7% of 400 stroke victims compared with 30.1% of age- and sex-matched control subjects. In a case-controlled study in which 133 patients with ischemic stroke were compared with control subjects matched for age and sex, Neau et al22 obtained a history of habitual snoring in 23.3% of stroke patients and only 8.3% of control subjects. In the present study, a prior history of habitual snoring and nocturnal apneic episodes correlated with evidence of OxyHb desaturation during oximetry, also suggesting that OSA was a preexisting problem.
Although we believe that SDB in most patients in our study preceded the stroke, it seems possible that the stroke caused SDB in some patients. CSA is well described in association with brain stem stroke.17 28 Brain stem stroke was clearly associated with oximetry measures of SDB in our study. Although only three patients had brain stem stroke, all had significant SDB by both oximetry and PSG measures. All had mixed apnea patterns, but the relative proportion of central apneas was higher in these three patients than in 15 of the 16 patients with hemispheric stroke who had PSG. This observation supports the hypothesis that central regulation of respiration is selectively impaired in patients with brain stem stroke.
Patients with hemispheric strokes might also develop SDB after the stroke. CSR may occur after stroke,8 resulting in a clinical presentation virtually indistinguishable from "traditional" sleep apnea syndromes, including major OxyHb desaturation and sleep fragmentation.9 47 In addition, dysphagia due to impairment of pharyngeal mobility occurs in a high percentage of unilateral hemispheric strokes and is often unsuspected clinically.24 25 26 27 Since the primary mechanism of OSA is functional obstruction of the oral airway, it seems possible that the risk of developing OSA might be higher in stroke patients with pharyngeal muscle dysfunction.31
No age-matched control patients were included in this study, and since the prevalence of SDB increases with age, the results should be interpreted cautiously. However, the frequency of oximetry abnormalities consistent with SDB is quite dramatic, and the association with increased mortality at 1 year and poor long-term functional outcome in survivors warrants further investigation. Although the increased mortality in our patients is consistent with earlier studies, the association with worse functional outcome has not been reported previously. Whether SDB is truly an independent variable associated with worse functional abilities cannot be answered at present.
Obviously, a major question resulting from this study is whether treatment trials using continuous positive airway pressure for stroke patients with SDB might prevent the worse outcome seen in SDB patients. This study did not address treatment, although we did counsel patients regarding weight loss and use of sedative drugs and notified primary care physicians about the results. Only one patient was subsequently treated with nasal continuous positive airway pressure. This patient refused further treatment after a short time. Our own anecdotal experience suggests that continuous positive airway pressure is not well tolerated by elderly patients with recent stroke. In this sense, they are very different than patients presenting with excessive daytime sleepiness or other overt clinical manifestations of SDB. Despite ample evidence of the deleterious effects of SDB, our observation has been that most stroke patients, their physicians, and their families do not consider SDB a problem significant enough to warrant what they perceive as the nuisance of treatment. However, the results of this study strongly indicate that SDB associated with stroke should be studied further and that trials of treatment for SDB associated with stroke should be undertaken.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The authors thank Steve Todd for his technical assistance, Cathy Galloway for her assistance in patient recruitment and follow-up, and Teresa Hire for her help in preparing this manuscript.
Received September 1, 1995; revision received November 21, 1995; accepted November 21, 1995.
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References |
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1. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230-1235.
2. Westbrook PR. Sleep disorders and upper airway obstruction in adults. Otolaryngol Clin North Am.. 1990;23:727-743. [Medline] [Order article via Infotrieve]
3. Lavie P. Incidence of sleep apnea in a presumably healthy working population: a significant relationship with excessive daytime sleepiness. Sleep. 1983;6:312-318. [Medline] [Order article via Infotrieve]
4. Gislason T, Almquist M, Eriksson G, Taube A, Bowman G. Prevalence of sleep apnea syndrome among Swedish men: an epidemiologic study. J Clin Epidemiol.. 1988;41:571-576. [Medline] [Order article via Infotrieve]
5.
Carskadon MA, Dement WC. Respiration during
sleep in the aged human. J Gerontol. 1981;36:420-423.
6.
Hall JB. The cardiopulmonary
failure of sleep-disordered breathing.
JAMA.. 1986;255:930-933.
7. Guilleminault C, Quera-Salva MA, Nino-Murcia G, Partinen M. Central sleep apnea and partial obstruction of the upper airway. Ann Neurol. 1987;21:465-469. [Medline] [Order article via Infotrieve]
8.
Hudgel DW, Devadatta P, Quadri M, Sioson ER, Hamilton
H. Mechanism of sleep-induced periodic breathing in
convalescing stroke patients and healthy elderly subjects.
Chest. 1993;104:1503-1510.
9. Dowdell WT, Javaheri S, McGinnis W. Cheyne-Stokes respiration presenting as sleep apnea syndrome. Am Rev Respir Dis. 1990;141:871-879. [Medline] [Order article via Infotrieve]
10.
Shepard JW, Garrison MW, Grither DA, Dolan GF.
Relationship of ventricular ectopy to oxyhemoglobin
desaturation in patients with obstructive sleep apnea.
Chest. 1985;88:335-340.
11. Guilleminault C, Connolly SJ, Winkle RA. Cardiac arrhythmia and conduction disturbances during sleep in 400 patients with sleep apnea syndrome. Am J Cardiol. 1983;52:490-494. [Medline] [Order article via Infotrieve]
12. Miller WP. Cardiac arrhythmias and conduction disturbance in the sleep apnea syndrome: prevalence and significance. Am J Med. 1982;73:317-321. [Medline] [Order article via Infotrieve]
13. Shapard JW. Hypertension, cardiac arrhythmias, myocardial infarction, and stroke in relation to obstructive sleep apnea. Clin Chest. 1992;13:437-458.
14. Koskenvuo M, Kaprio J, Partinen M, Langinvaino H, Sarna S, Heikkila K. Snoring as a risk factor for hypertension and angina pectoris. Lancet. 1985;1:893-896.[Medline] [Order article via Infotrieve]
15. Lugaresi E, Cirignotta F, Coccagna G, Piana C. Some epidemiologic data on snoring and cardiocirculatory disturbances. Sleep. 1980;3:221-224. [Medline] [Order article via Infotrieve]
16. Norton PG, Dunn EV. Snoring as a risk factor for disease: an epidemiological survey. Br Med J. 1985;291:630-632.
17. Palomäki H, Partinen M, Erkinjuntti T, Kaste M. Snoring, sleep apnea syndrome and stroke. Neurology. 1992;42(suppl 6):75-82.
18.
Hla KM, Young JB, Bidwell T, Palta M, Skatrud JB,
Dempsey J. Sleep apnea and hypertension: a population-based
study. Ann Intern Med. 1994;120:382-388.
19. Partinen M, Palomäki H. Snoring and cerebral infarction. Lancet. 1985;2:1325-1326. [Medline] [Order article via Infotrieve]
20. Spriggs DA, French JM, Murdy JM, Curless RH, Bates D, James OFW. Snoring increases the risk of stroke and adversely affects prognosis. Q J Med.. 1992;84:555-562.
21.
Palomäki H. Snoring and the risk of
ischemic brain infarction. Stroke. 1991;22:1021-1025.
22. Neau J-P, Meaurice J-C, Paquereau J, Chavagnat J-J, Ingrand P, Gil R. Habitual snoring as a risk factor for brain infarction. Acta Neurol Scand. 1995;92:63-68. [Medline] [Order article via Infotrieve]
23. Koskenvuo M, Kaprio J, Telakivi T, Partinen M, Heikkila K, Sarna S. Snoring as a risk factor for ischaemic heart disease and stroke in men. Br Med J. 1987;294:16-19.
24. Robbins J, Levine RL. Swallowing after unilateral stroke of the cerebral cortex: preliminary experience. Dysphagia. 1988;3:11-17.[Medline] [Order article via Infotrieve]
25.
Barber DH. The natural history and functional
consequences of dysphagia after hemispheric stroke.
J Neurol Neurosurg Psychiatry.. 1989;52:236-241.
26. Veis SL, Logemann JA. Swallowing disorders in persons with cerebrovascular accident. Arch Phys Med Rehabil. 1985;66:372-375. [Medline] [Order article via Infotrieve]
27.
Horner J, Massey EW, Riski JE, Lathrop DL, Chase
KN. Aspiration following stroke: clinical correlates and
outcome. Neurology. 1988;38:1359-1362.
28.
Askenasy JJM, Godhammer I. Sleep apnea as a
feature of bulbar stroke. Stroke. 1988;19:637-639.
29. Kapen S, Goldberg J, Wynter J. The incidence and severity of obstructive sleep apnea in ischemic cerebrovascular disease. Neurology. 1991;41(suppl 1):125. Abstract.
30. Dyken ME, Somers VK, Yamada T, Adams HP, Zimmerman MB. Investigating the relationship between sleep apnea and stroke. Sleep Res. 1992;21:30. Abstract.
31. Mohsenin V, Valor R. Sleep apnea in patients with hemispheric stroke. Arch Phys Med Rehabil. 1995;76:71-76. [Medline] [Order article via Infotrieve]
32.
Reding MJ, Potes E. Rehabilitation outcome
following initial unilateral hemispheric stroke: life table
analysis approach. Stroke. 1988;19:1354-1358.
33. Folstein MF, Folstein SE, McHugh PR. Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189-198. [Medline] [Order article via Infotrieve]
34. Mahoney FI, Barthel DW. Functional evaluation of the Barthel Index. Md Med J. 1965;14:61-65.
35.
Partinen M, Guilleminault C. Daytime sleepiness
and vascular morbidity at seven-year follow-up in obstructive
sleep apnea patients. Chest. 1990;97:27-32.
36.
He J, Kryger M, Zorick F, Conway W, Roth T.
Mortality and apnea index in obstructive sleep apnea.
Chest. 1988;94:9-14.
37. Daly JA, Giombetti R, Miller B, Garrett K. Impaired awake cerebral perfusion in sleep apnea. Am Rev Respir Dis. 1990;141:A376. Abstract.
38. Meyer JS, Ishikawa Y, Hata T, Karacan I. Cerebral blood flow in normal and abnormal sleep and dreaming. Brain Cogn. 1987;6:266-294. [Medline] [Order article via Infotrieve]
39.
Fisher AQ, Chaudhary BA, Taormina MA, Akhtar B.
Intracranial hemodynamics in sleep apnea.
Chest. 1992;102:1402-1406.
40.
Tobin MJ. Respiratory monitoring.
JAMA.. 1990;264:244-251.
41. Gyulay S, Olson LG, Hensley MJ, King MT, Allen KM, Saunders NA. A comparison of clinical assessment and home oximetry in the diagnosis of obstructive sleep apnea. Am Rev Respir Dis. 1993;147:50-53. [Medline] [Order article via Infotrieve]
42.
Series F, Marc I, Cormier Y, LaForge J. Utility
of nocturnal home oximetry for case finding in patients with suspected
sleep apnea hypopnea syndrome. Ann Intern Med. 1993;119:449-453.
43.
Williams AJ, Yu G, Santiago S, Stein M.
Screening for sleep apnea using pulse oximetry and a clinical
score. Chest. 1991;100:631-635.
44. Allan MA, Fitzpatrick MF, Molly J, Douglas NJ. Correlation between oximetry and polysomnography in patients with the sleep apnea/hypopnea syndrome. Am Rev Respir Dis. 1990;141:A858. Abstract.
45. Douglas NJ, Thomas S, Jan MA. Clinical value of polysomnography. Lancet. 1992;339:347-350. [Medline] [Order article via Infotrieve]
46.
Farney RJ, Walker LE, Jensey RL, Walker JM. Ear
oximetry to detect apnea and differentiate rapid eye movement (REM) and
non-rapid eye movement (NREM) sleep: screening for sleep apnea
syndrome. Chest. 1986;89:533-539.
47. Alex CG, Önal E, Lopata M. Upper airway occlusion during sleep in patients with Cheyne-Stokes respiration. Am Rev Respir Dis. 1986;133:42-45.[Medline] [Order article via Infotrieve]
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