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Sleep Apnea in Patients With Hemispheric Stroke
Vahid Mohsenin, AID, Raul Valor, MD
ABSTRACT. Mohsenin V, Valor R. Sleep apnea in patients with hemispheric stroke. Arch Phys Med Rehabil 1995;76:71-6. • Sleep pattern and breathing in humans are altered following cerebrovascular accidents involving the brainstem. Sleep apnea is a well-established complication of stroke involving the brainstem. On the other hand, the effect of cerebral stroke on sleep and breathing has not been well defined. The diffuse cerebral symptoms such as cognitive deficits, depression or fatigue, after hemispheric stroke mimic those present in patients with sleep apnea. To define the breathing pattern in patients with stroke involving cerebral hemispheres without brainstem lesion and without the prior history of sleep-disordered breathing, we studied 10 patients within 1 year of their stroke. The data collected during polysomnography from the stroke patients were compared with a group of subjects matched for age, body mass index, presence of hypertension, and smoking history without stroke. Patients with stroke had an abnormal sleep architecture with significantly lower slow wave sleep and rapid eye movement (REM) sleep when compared with controls. Sleep was fragmented because of the presence of increased respiratory disturbances. Stroke patients had a respiratory disturbance index of 52 _+ 10 events per hour when compared with 3 _ 1 in controls (p < .05). Majorities of respiratory events were obstructive apneas and were associated with arterial oxygen desaturations and arousals. The pathogenic mechanism of sleep-disordered breathing in patients with hemispheric stroke seems to be related to the physiological effect of sleep on already compromised upper airway muscle control. Patients with stroke and diffuse cerebral symptoms should be investigated for the possibility of sleep-disordered breathing. -

© 1995 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation Patients suffering from cerebral infarction often complain of diffuse cerebral symptoms such as impaired memory, inability to concentrate, emotional instability, increased need of sleep, and tiredness. 1 These symptoms have been attributed, in large part, to structural damage to brain tissue. However, many of these symptoms are also noted in patients with sleep disturbances. 2 Indeed, stroke has a profound effect on sleep continuity and architecture because most of the anatomic structures that control sleep are located in the central nervous system. 34 Because the control centers for breathing and upper airway patency are located in the central nervous system as well, it is conceivable that lesions in this area may cause altered breathing pattern and impaired upper airway function during respiration. 6'7 It is not uncommon to encounter a variety of neurological disorders that affect sleep and breathing. It is important to understand not only that the neurological illnesses may affect sleep and breathing, but also that alterations of sleep and breathing may adversely affect the natural history of a neurological disorder. Because centers that control breathing and upper airway function are in the brainstem, lesions in this area have been associated with breathing disorders. 8'9 Lesions in the cerebral hemispheres have been shown to cause periodic breathing. 7'1°
From the Pulmonary and Critical Care Section, Yale University School of Medicine, New Haven, CT; and Gaylord Hospital, Wallingford, CT. Submitted for publication May 31, 1994. Accepted in revised form September 8, 1994. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Vahid Mohsenin, MD, Pulmonary and Critical Care Section, Yale University School of Medicine, PO Box 208057, 333 Cedar Street, New Haven, CT 06520-8057. © 1995 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/95/7601-309653.00/0

More recently, Kapen and colleagues reported a high incidence of obstructive sleep apnea in a group of patients with hemispheric stroke, tt However, because of lack of control for confounding factors such as obesity and presence of hypertension, a definite causal relationship between obstructive sleep apnea and stroke cannot be claimed. Because the implication of these findings in the care and management of patients with cerebral stroke could be extremely important, we sought to study patients with hemispheric stroke to define the effect of stroke on breathing pattern, oxygenation, and sleep architecture. We found a significant number of obstructive sleep apneas with marked arterial desaturations and sleep fragmentation compared with controls.
METHODS

Seventeen patients admitted to a rehabilitation unit with stroke were screened. They were evaluated on the basis of medical history, thorough neurological examination, and brain imaging using computed tomography scan, magnetic resonance imaging or cerebral arteriography. Patients with the prior history of habitual snoring, excessive daytime sleepiness, sleep apnea, obesity (greater than 30kg/m 2 body mass index [BMI]), brainstem stroke or other neurological disorders were excluded. Ten patients out of 17 fulfilled the inclusion criteria and hence were included in the study. We studied 10 additional patients without stroke who were matched for age, gender, and BMI and for the presence of hypertension and smoking as controls. Patients, bed-partners, and caregivers were interviewed for detailed sleep history and symptoms especially about snoring, possible pauses during sleep, daytime sleepiness, memory loss, cognitive function, and affective disorders before the stroke, t2 Polysomnography was performed between 9:00 PM and

Arch Phys Med Rehabil Vol 76, January 1995

Comparison of age. The frequency of the respiratory events was higher in REM sleep than NREM sleep in both control and stroke patients indicating the worsening of sleep-disordered breathing in REM. 7 On the other hand. Six of the strokes were on the left side and four on the fight side. Lee and coworkers found a Cheyne-Stokes pattern of breathing in patients with extensive bilateral pontine lesions. The latter is a milder form of partial obstructive apnea where arousal is the predominant polysomnographic feature. and one ACA. gender. was associated with thoracoabdominal wall movements. Mixed apneas that were counted as obstructive apneas comprised a small fraction of apneas. The respiratory events were defined according to the Diagnostic and Coding Manual of The International Classification of Sleep Disorders.72 SLEEP APNEA IN PATIENTS WITH STROKE. arousal index. All variables were recorded simultaneously and continuously on a 16-channel polygraph. An electrocardiogram was recorded continuously. or sleep apnea. The arousal index of stroke patients was significantly higher than the controls. was within the normal range but shorter than the control group. The respiratory disturbances were associated with arterial oxygen desaturations as shown in figure 4. b Leg movements were monitored with two channels of EMG. Hypopneas and central apneas were infrequent except for patient AB who had predominantly central apneas. RESULTS The anthropometric characteristics and clinical features of patients with stroke and the control group are shown in table 1. None of the patients had prior history of habitual snoring. 7'1°'17'~8 The breathing pattern was attributed to heightened central responsiveness to c02. There are a few scattered reports of sleep complaints after stroke and several anecdotal and uncontrolled reports of sleep-related breathing disorders after cerebral infarction. and one channel submental electromyogram (EMG). two channels of electrooculogram. Statistics Comparisons between groups were performed using Wilcoxon's signed-ranks test. BMI. The slow wave sleep (SWS) and REM sleep were significantly shorter in stroke patients than controls. had very few episodes of oxygen desaturation. Hypopnea was defined as a reduction in amplitude of airflow or thoracoabdominal wall movement of greater than 50% of the baseline measurement for more than 10 seconds and accompanied by greater than 4% arterial o2 desaturation (no time limit). Eight of the 10 patients with stroke were found to have significant sleep apnea (fig 2). nocturnal sleep disruption. excessive daytime sleepiness. Sleep state was recorded with one channel electroencephalogram (C3/A2 or C4/A1). Six percent of the oxygen desaturations were below SaO2 79%. The control subjects had few hypopneas and apneas with a normal respiratory disturbance index (RDI). a Arterial oxygen saturation was measured using a Biox oximeter. a measure of hypersonmolence. and nasal and oral flows using thermisters. Nine of the patients had thromboembolic stroke and one had fight basal ganglia bleed. ~3 Calculated sleep variables were sleep stages as percentage of total sleep period time (SPT). RDI was calculated for both sleep phases.. Mixed apneas had both central and obstructive components and were included in the results as obstructive apneas. The majority of patients had predominantly obstructive sleep apnea. atrial fibrillation in one.007. and the presence of hypertension between patients with stroke and controls showed no significant difference. 14 An apnea was defined as cessation of airflow for at least 10 seconds. ~5 Data are reported as mean + SE. The sleep latency. There were 36 _+ 16 episodes between SaOz 85% to 89% and 6 + 3 episodes between SaO2 80% to 84%. Breathing was assessed by monitoring chest wall and abdominal movements using bellow pneumographs.05 was considered significant. Mohsenin 7:00 AM. The risk factors for stroke included hypertension in five. All patients had intact brainstem function and no evidence of lesion in this area on brain imaging. The quality of sleep was generally poor with awake time accounting for 42% of SPT in stroke patients. January 1995 . for a minimum of 10 sec0nds. Sleep recordings were scored in 30-second epochs and staged according to standard criteria. A p value of <. The overall RDI in stroke patients was 52 _+ 10 events per hour sleep and was significantly higher than the control group of 3 _+ 1 per hour. p -. DISCUSSION The results of this study show that patients with hemispheric stroke may develop sleep-disordered breathing. Nocturnal sleep latency was calculated from "lights out" to the first three consecutive epochs of nonrapid eye movement (NREM) sleep or one epoch of rapid eye movement (REM) sleep. one MCA and anterior cerebral artery (ACA). Central apneas were defined as those without accompanying thoracoabdominal wall movements. the number of apneas and hypopneas per hour of sleep) and number find degree of arterial o2 desaturations. Table 2 and figure 1 show the effect of stroke on sleep architecture and arousals. The control patients who were either normal or had a mild chronic obstructive pulmonary disease or hypertension. 19 Central apnea was noted as Arch Phys Med Rehabil Vol 76. An obstructive apnea was defined when cessation of airflow. and sleep efficiency (total sleep time/SPT). Figure 3 shows the respiratory events expressed per hour sleep as RDI. To determine the effect of REM and NREM sleep on the respiratory disturbances. There was no evidence for polysomnographic features of increased upper airway resistance ~6 in either group. Plum and coworkers noted that the major effect of cerebral hemispheric disease on respiration in sleep was in the form of Cheyne-Stokes respiration or long-cycle Cheyne-Stokes breathing associated with hypocapnia. Calculated respiratory variables included respiratory disturbance index (respiratory disturbance index [RDI]. patients with stroke had 99 _+ 25 episodes of oxygen desaturations (greater than 4%) during the course of the night. smoking history. As a group. but both groups had a history of mild and nonhabitual snoring. Eight of the strokes were in the middle cerebral artery (MCA) distribution. and cigarette smoking in four. This patient had clinical features similar to other patients with a thrombotic stroke involving left frontoparietal region with right hemiparesis.

such as in hemispheric cerebral stroke. min) Total sleep time (min) Sleep latency (min) Awake (% SPT) Stage I (% SPT) Stage II (% SPT) Stage I I I + IV (% SPT) REM (% SPT) Arousal index (/h) * p < .0 24.7 26. 2m2 We hypothesize two pathogenic mechanisms in the development of sleepbreathing abnormalities in patients with hemispheric stroke. though. a definite causal relationship between obstructive sleep apnea and stroke cannot be claimed. 26'27 In support of this. the patency of the upper airway becomes compromisedY '23 However. Our results confirm the report by Kapen and coworkers on the presence of obstructive sleep apnea in some patients with cerebral stroke. attributed to continual neuromuscular input by the higher nervous system. however it has been shown that it may cause a transient contralateral loss of tone or weakness in these muscles. when this control of the pharyngeal airways by the higher nervous system is disrupted. because of associated risk factors such as obesity and hypertension in most of these patients.7 15. and palatal muscle weakness contralateral Arch Phys Med Rehabil Vol 76. In hemispheric stroke with hemiplegia and. depending on the site and extent of the stroke.05 when compared with control.3 1 2 1 3. January 1995 . The fact that the pharyngeal airway is open during wakefulness but occludes during sleep implicates a neural component dependent on the state of vigilance.0 25.2 20. should not cause any significant weakness of the muscle.2 L R L L L R L R L R ACA MCA MCA MCA MCA MCA thalamic MCA MCA.2 30 26. we excluded patients with previous complaints of sleep disorders and obesity and matched for the presence of hypertension. dysphagia. 356 271 22 26 8 45 9 14 20 _+ 21 _+ 26 _+ 6 _+ 4 _+ 1 _+ 3 -4. During sleep.9 26. of lymphatic tissue (tonsils and adenoids). 24 The second and potentially important factor is the dimension of the upper airway itself. a unilateral upper motor neuron lesion. smoking Hypertension Hypertension m m E 2 8 1 1 12 2 0. tongue weakness. and/or mucosal swelling reduces airway patencyY Because of bilateral upper motor neuron innervation of pharyngeal and laryngeal muscles from the corticobulbar pathways. when the activation of pharyngeal dilator muscles occurs. hypertrophy.9 23. Mohsenin Table 1: Patients Characteristics and Clinical Features Controls FB CB SF AG LK WL MQ LB EG EH Mean SE Patients AM DG GB MM JR RP RO JK AB DZ Mean SE 73 Age (yr) 55 49 47 56 66 64 35 27 78 62 54 5 58 78 51 33 68 50 61 72 44 41 56 5 Sex F M M F M M M F F F --F F M M M M M M M M --- BMI (Kg/m 2) 25. 28 The impaired upper airway control as a result of upper motor neuron dysfunction may be caused by a required and highly complex neuronal control of a nasopharyngeal and pharyngolaryngeal muscles.8 21.2 28. Kapen and associates reported a high incidence of obstructive sleep apnea in hemispheric stroke patients.4 23. Narrowing of the upper airway by obesity. adequate airway lumen is promoted so no airway obstruction occurs in a healthy person.1 21. the patient may have dysarthria. Robbins and coworkers showed that patients with hemispheric infarctions were more likely to exhibit pharyngeal muscle dysfunction with impaired swallowing. smoking Hypertension Hypertension.2 22.8 25.SLEEP APNEA IN PATIENTS WITH STROKE.5 26. which controls the action of pharyngeal muscles and ensures a patent pharynx.5 25.8 22. The lack of optimal tone of the muscles may lead to a highly compliant upper airway with a propensity to narrowing and collapse.8 1. The pharyngeal patency during Table 2: Sleep Architecture and Arousal in Controls and Stroke Patients Control Sleep period time (SPT. l~ In our casecontrol study.0 21. One is the physiological effect of sleep on upper airway control and the second is the flaccidity of upper airway muscles as a result of stroke.9 26. in large part.3 2.5 26.2 _+ 2 _+ 3 Stroke 370 227 13 42 12 36 4 7 64 _+ 21 _+ 35 _+ 5 +_ 9 _+ 3 _+ 6 +_ 2* _+ 3* _+ 16" wakefulness is. A C A MCA the predominant form of apnea in patients with brainstem lesionsY ° In contrast to these studies. We speculate that the maintenance of upper airway tone and function requires a dual upper motor neuron control.0 1.5 Age of Stroke (month) Site of Stroke Clinical Features Mild COPD Hypertension Normal Mild COPD Mild COPD Hypertension Normal Normal Mild COPD Hypertension --R hemiparesis L hemiparesis R hemlparesis R hemiparesis R hemiparesis L hemiparesis Expressive aphasia L hemiparesis R hemiparesis L hemi ~aresis Other Problems Smoking _ _ m _ _ m m m _ _ m m m _ _ m Smoking None Seizures Smoking None Smoking Smoking --Coronary heart disease Hypertension None Smoking Smoking ARDS.

007 control versus CVA for all categories. 5~0 100 150 Number of Respiratory Events 200 250 With apneas occurring in very close clusters continuously throughout the night. Significant increases in systemic arterial pressure occur cyclically with episodes of apnea. and maximal elevation follows arousals and after the resumption of ventilation. Arch Phys Med Rehabil Vol 76. as was shown in this study. this phenomenon would become more pronounced during REM sleep. The RDI was significantly higher in stroke patients than controis. during the night. they may occur. Thus patients with stroke and sleep apnea with oxygen desaturations are at greater potential risk of repeated stroke or incomplete neurological recovery.74 60 SLEEP APNEA IN PATIENTS WITH STROKE.1--I DGAM0 . leading 120 ~ • [] Control CVA . Fig 3 .. X " - O 4020• "5 . These abnormalities are more profound in patients with bilateral upper motor neuron lesions. as in our patients with unilateral involvement. Mohsenin 90 i (/3 o I! _. the global and regional cerebral perfusion is decreased in sleep apnea patients during even wakefulness. severe narrowing or closure of the pharyngeal airway may occur during sleep. 33'34 suggesting altered cerebral blood flow autoregulatory mechanisms.T h e RDI in controls and patients with stroke (CVA). DZ AB.. When the physiological change. predominantly obstructive apneas.T h e number and degree of arterial oxygen desaturations during sleep as a result of apneas and hypopneas in controis as well as patients with stroke. 32'33 Further. cerebral blood flow during sleep is more decreased in patients with apnea than controls.T h e number and type of sleep-disordered breathing during the course of the night in patients with stroke. January 1995 . to the side of the upper motor neuron lesion. elevations may be extreme. often in association with very severe oxygen desaturations. *P < ._J I F ] Control • CVA x "~ ~D 8070- [] • [] NREM RDI REM RDI Overall RDI =o 605o- =g i:~ 40- 30e-~ rr 20- 13- Awake Stage 1 Stage 2 SWS REM Control CVA Fig 1 . decreased upper airway muscle tone. however. 29'3° The pseudobulbar and bulbar palsies predispose patients to obstructive apneas during sleep. Repeated episodes of apneas and oxygen desaturation can also cause multiple awakenings and arousals. 3~ Further.~ E ~ Z Total 89-85% 84-80% 79-70% <70% Fig 2 .m JKF~3RP. occurs superimposed on a background of a narrowed pharyngeal lumen...S l e e p architecture in patients with stroke and controls. Patients with stroke (CVA) had a significantly shorter SWS and REM sleep than the controls. Oxygen Saturation Fig 4 . All but two patients had higher than 32 events. P = . .05._o lOO- • "////~ • [] [] Obstructiveapnea Centralapnea Hypopnea ~ 80- a ~. Arousals to the fully awake state or stage shifts from a deeper to a lighter stage of sleep disrupt the sleep architecture. Because the activities of pharyngeal dilator muscles are virtually absent in REM sleep.E JRMMGB. .

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