(Stroke. 1996;27:247-251.)
© 1996 American Heart Association, Inc.
Articles |
Reduced Heart Rate Variability After Right-Sided Stroke
From the Departments of Neurology (H.K.N., C.B.) and Clinical Neurophysiology (H.K.N., B.G.W.), Institute of Clinical Neuroscience, Sahlgrenska University Hospital, Göteborg, Sweden.
Correspondence to Hans K. Naver, MD, Institute of Clinical Neuroscience, Department of Clinical Neurophysiology, Sahlgrenska University Hospital, S-41345 Göteborg, Sweden.
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Abstract |
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 Top Abstract IntroductionSubjects and Methods Results Discussion References |
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Background and Purpose Recently, asymmetries have been demonstrated in skin sudomotor and vasomotor function after unilateral cerebral lesions. The present study was performed to determine whether other bedside tests reflecting sympathetic and parasympathetic cardiovascular functions would reveal differences with respect to the side of cerebrovascular lesions.
Methods Heart rate variability during deep breathing as well as blood pressure and heart rate changes during tilt and isometric handgrip was measured in a group of patients with a monofocal stroke and compared with similar data from age-matched patients with transient ischemic attack and healthy control subjects.
Results Compared with left-sided stroke and with the control subjects, stroke location on the right side was associated with a reduced respiratory heart rate variability (P>.01), a reflex mainly under parasympathetic control. In contrast, reflexes mainly reflecting peripheral sympathetic function were equal for right- and left-sided lesions.
Conclusions Since an imbalance in cardiac autonomic innervation may be crucial for the generation of cardiac arrhythmias and since reduced heart rate variability has been associated with increased mortality, the findings suggest that the risk of sudden death may be correlated with lateralization and location of the brain infarct after stroke.
Key Words: autonomic nervous system • blood pressure • cerebral infarction • heart rate
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Introduction |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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From animal and human studies, it is well established that anatomic and functional asymmetries exist in autonomic cardiac innervation. The parasympathetic and sympathetic nerves to the heart have parallel courses,1 on the right side mainly to the sinus node (with antagonistic influences on its chronotropic function) and on the left side mainly to the atrioventricular node and the ventricles. The left-sided nerves influence atrioventricular conduction, the ventricular fibrillation threshold, the QT time, and the ST segment of the electrocardiogram (ECG).1 2 3 4 5 6 7 8 9 10 This insight has clinical consequences in that left-sided stellectomy is used in the treatment of malignant ventricular arrhythmias in the long QT syndrome.9 10
Since central autonomic pathways to the heart probably descend uncrossed,11 one should expect a corresponding asymmetry in central nervous control of cardiac function. This assumption is supported by animal studies showing that experimental stroke in the right hemisphere induced more pronounced sympathetic effects than lesions on the left side.12 13 It is well known that central nervous system lesions in humans may induce ECG changes,14 cardiac arrhythmias,15 16 and disturbed cardiovascular reflexes,17 but whether lesions in the left compared with the right side of the brain have different consequences for neural heart rate control in humans is less well known. Clinical observations suggest an association between right hemispheric lesions and supraventricular tachycardia.18 Power spectrum analysis of the ECG has shown a more pronounced reduction of spectral power in the domain of the sinus arrhythmia after right-sided compared with left-sided lesions.19 We have recently found asymmetric sympathetic skin vasomotor reflexes after stroke.20 Against this background, the present study was undertaken to study autonomic reflexes reflecting parasympathetic and sympathetic influence on heart rate and blood pressure in patients with monofocal stroke to determine whether such reflexes are affected differently depending on the side of the lesion. A group of transient ischemic attack (TIA) patients with no central nervous system lesions and a group of healthy subjects served as controls.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Subjects
After giving their informed consent, 23 previously healthy patients with monofocal stroke (aged 59±13 years [mean±SD]) were included consecutively and compared with a group of healthy subjects (n=21; aged 61±12 years) and a group of subjects with a history of one TIA but otherwise previously healthy (n=11; aged 59±16 years). Thirteen patients (aged 62±10 years) had right-sided and 10 (aged 55±15 years) had left-sided lesions. The subjects were taking no medication except for aspirin initiated after the stroke or the TIA. Patients and control subjects who had previously taken medication for cardiovascular disease; with a history of symptoms suggesting cardiac or vascular disease; or with a history of neurological disease, diabetes, or other endocrinologic diseases were excluded as well as all individuals with cardiac arrhythmias. We excluded patients with severe aphasia since they could not give their informed consent. In addition, patients with large lesions who were unable to sit or to stand on a tilt table and patients with a neglect syndrome were not included. The control subjects were contacted through a revenue register and were paid for their participation. The TIA patients were contacted at a follow-up 6 months to 2 years after hospitalization for the TIA at the neurological clinic. The stroke patients were investigated at the end of their hospitalization, 8 to 48 (mean, 18) days after the stroke. The study was approved by the local ethics committee.
Methods
Brain CTs
In all stroke and TIA
patients, CTs of the brain were performed
acutely and (except for brain stem lesions) again after at least 4
weeks. Stroke patients were excluded from the study if the CT revealed
more than one lesion or a lesion not compatible with the symptoms.
Respiratory Heart Rate Variability
Heart rate
variability was calculated from the variation of the
RR intervals in an ECG recorded with the use of chest electrodes.
The ECG signals were monitored on an electromyographic amplifier (MS92,
Medelec) and processed on a personal computer during a 1-minute
recording period.21 The subjects rested for 15
minutes before registration in a comfortable armchair reclined at
30°. Two recordings were made while the subjects were taking
six maximal breaths per minute, following the pace indicated by the
operator. For each 1-minute registration, the ratio between the longest
and the shortest RR interval during each respiratory cycle
(RRmax/RRmin) was determined, and then
the heart rate variability, expressed as the RR index [mean
(RRmax/RRmin)] for the period, was
calculated.22 The highest value of the two
recordings was chosen.
Orthostatic Test
Although
active standing would be a better procedure to evaluate
sympathetic function, passive tilting was used because of the inability
of many hemiparetic patients to stand up actively. Patients were
secured with three straps to a horizontal table with a 10-cm-thick
cushion under the feet and no pillow under the head to make the
standing position more comfortable. Heart rate and blood pressure were
measured automatically every 30 seconds (Sphygmomanometer 203Y, Nippon
Colin Co), and when measurements had been stable for at least 5
minutes, the subjects were tilted to 80° for 5 minutes while we
continued to take measurements every 30 seconds.
RR intervals were monitored from a continuous ECG recording for 15 seconds before and 45 seconds into the tilt. For each tilt procedure, the mean RR interval of the supine rest period was determined, the shortest RR interval during the first 15 seconds of standing and the longest interval (the brake point of the transient deceleration) during the following 20 seconds were identified, and when possible a brake index [(RRmax-RRmin)/mean RR] was calculated.23
Isometric Handgrip
First
the patient's maximum handgrip power was determined with
a dynamometer. When the blood pressure and heart rate during rest had
been stable for at least 2 minutes, the subject made a handgrip
contraction at 30% of the maximal power for 3 minutes. Blood pressure
and heart rate were measured every 30 seconds for 2 minutes before and
for 3 minutes during the handgrip. All measurements of blood pressure
and heart rate variability were made just before or 3 hours after
lunch.
Statistical Analysis
In
"Results" and in the Figure
, data are presented
as mean±SEM. After we controlled the normal distribution of the
material, differences between groups were evaluated with Student's
t test. When more than one comparison was made, ANOVA
analysis was applied, followed by Duncan's multiple range
test.
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indicates brain stem lesions; 
, hemispheric
lesions). Bars indicate mean±SEM of each column. |
Results |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Location of the Lesion
Of the 23 patients, 14 had hemispheric and 8 had brain stem lesions. Of those with hemispheric lesions, 9 had middle cerebral artery infarcts, 2 subcortical bleedings, and 3 lacunar infarcts, 1 of whom (with a pure sensory lacunar syndrome) had a normal CT. Of those with brain stem lesions, 1 had a hemorrhagic lateral pontine bleeding visible on CT and 7 had typical lateral brain stem infarct syndromes with ipsilateral cranial nerve symptoms, dystaxia, vestibular dysfunction, contralateral temperature and pinprick hypoesthesia, and normal CT.
Resting blood pressure and heart rate did not differ between
the
control groups and the stroke patients, and there was no significant
difference between subgroups of patients with respect to the side of
the lesion (Table 1).
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Respiratory Heart Rate Variability
The mean RR index during
deep breathing and the relationship
between age and RR index did not differ between the stroke patients and
the two control groups. According to regression analysis, the
RR index was reduced 0.005 per year for stroke and TIA patients and
0.004 for control subjects. All individual patients had values within
the range of mean±2 SD of the control subjects. When the entire
patient group was considered, RR variability during deep breathing was
significantly smaller in patients with right-sided lesions compared
with patients with left-sided lesions (P<.01;
Figure
,
Table 2); this difference was also
present between patients with left and right hemispheric lesions
(P<.05). The number of patients with brain stem lesions (6
right, 2 left) was too small to allow a comparison between left- and
right-sided lesions. There was no difference in heart rate
variability between right hemispheric and right brain stem lesions
(1.11±0.03, n=7, and 1.07±0.03, n=6,
respectively).
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Six patients died within a mean of 3 years (range, 12 to 60 months) after the stroke (5 with right and 1 with left hemispheric stroke). They were older than the rest of the patients (mean, 71 versus 55 years; P<.01) and had a lower heart rate variability index during deep breathing (mean, 1.06 versus 1.19; P=.02) and a lower heart rate increase during handgrip (3 versus 9 beats per minute; P=.01).
Isometric Handgrip
Systolic and diastolic blood pressures and
heart rate increased during 3 minutes of handgrip. The changes were
similar in control subjects and patients, and no difference was
observed between left- and right-sided strokes (Table 3).
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Tilt Test
At measurements after 30 seconds in the standing
position, the
healthy control subjects reacted with slight increases in
diastolic blood pressure and heart rate during tilt,
whereas in the stroke and TIA patients systolic blood pressure
was reduced and diastolic blood pressure did not increase
(Table 4). Compared with the healthy control subjects,
there was a greater increase of heart rate in TIA and stroke patients.
The decrease in systolic pressure of the stroke patients was
significant (P<.05) but not the change in
diastolic pressure (Table 4). In healthy control subjects
blood pressure had stabilized after 30 seconds, but for 8 of 23 of the
stroke patients and 4 of 11 of the TIA patients, blood pressure
continued to decrease for an additional 1 to 2 minutes and became
stabilized after 2.5 minutes.
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No brake point, ie, no transient deceleration, could be defined in the RR interval registration after tilting in 1 of 21 control subjects and in 7 of 23 stroke patients (difference not significant, P=.07). For those stroke patients who had a transient heart rate deceleration, the brake index was smaller compared with that of the healthy subjects (P=.02). In 5 of the 7 patients without transient deceleration, blood pressure continued to decrease after the first minute of tilt.
No significant differences in blood pressure or heart rate changes were seen between patients with left- and right-sided stroke.
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Discussion |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Respiratory Heart Rate Variability
Respiratory heart rate variability was significantly smaller in patients with right- compared with those with left-sided cerebral lesions. This asymmetry, which was also significant when hemispheric strokes were considered separately, was probably due to a reduction of heart rate variability in right-sided lesions since the RR variability index in these patients was lower than in the control subjects.
The asymmetry was probably not an effect of age since the age-related variations were similar between the groups. Since reduced compliance would be more common after left hemispheric lesions due to apraxia and aphasia than after right hemispheric lesions, this seems to be a less likely explanation for the asymmetry. The low heart rate variability also seen in the patients with right-sided brain stem lesions supports our contention that this is not due to low compliance.
Reduced heart rate variability and heart rate response to the Valsalva maneuver have been demonstrated previously in the acute phase of stroke,17 but the influence of the side of the stroke was not reported. However, our results agree with both the side differences observed by spectral analysis of the ECG19 and the observation that patients with right hemispheric lesions had reduced heart rate responses to attention-demanding stimuli.24 The studies on cardiac effects during electric insular cortex stimulation25 and during unilateral hemispheric amobarbital narcosis26 confirm a lateralization of the cerebral cardiac control and suggest a predominance of the right hemispheric cortex in tachycardia mechanisms. This is consistent with our results.
Since respiratory heart rate variability predominantly reflects parasympathetic mechanisms,22 27 the reduced variability after right-sided lesions is probably due to impaired vagal function. Whether this is a consequence of a direct lesion of central parasympathetic pathways or due to a sympathetic lesion with secondary effects on vagal function is unclear. The central organization that controls interactions between the two limbs of the autonomic nervous system is complex; reciprocal as well as nonreciprocal patterns of cardiac sympathetic and vagal activities may be induced during hypothalamic electric stimulation in dogs.28
What are the putative consequences of reduced heart rate variability in right-sided stroke? A low heart rate variability after cardiac infarction is known to be related to an increased risk of sudden death,29 30 perhaps because an imbalance between cardiac parasympathetic and sympathetic innervation may induce ventricular arrhythmias more easily in a damaged myocardium. However, this is unlikely to be the only explanation since low heart rate variability may also be associated with an increased risk of sudden death in patients without a history of cardiac infarction.31 32 Cerebral mechanisms may be important since the risk is also increased after cerebral lesions in subjects with diseased as well as with normal hearts.33 Against this background, our results make it likely that patients with right-sided stroke should have a higher risk for sudden death compared with patients with left-sided stroke. Whether the mechanism would be ventricular or other arrhythmias is, however, obscure. A left/right imbalance favoring the left vagal tone might lead to atrioventricular and ventricular electrophysiological abnormalities in parallel with the effect of unilateral changes in sympathetic tone.6 Alternatively, a right parasympathetic/sympathetic imbalance might primarily lead to supraventricular tachyarrhythmias. That patients with right-sided stroke have been shown to have an increased frequency of supraventricular tachycardia18 agrees with this hypothesis. No conclusions can be made regarding whether cardiac arrhythmias were involved in the cause of death in the five deceased patients with right-sided stroke. A larger prospective study is needed to examine the relationship between the risk of malignant arrhythmias and the location of the brain infarct after stroke.
Orthostatic Test and Isometric Handgrip
The variations in
blood pressure in these tests are commonly
used as measures of sympathetic function.34 35
Compared
with the healthy control subjects, our stroke patients showed
pathological blood pressure and heart rate responses to tilt. On the
other hand, the response of the patients to isometric handgrip was
similar to those of the control groups, and no test showed differences
with respect to the side of the lesions. Thus, our findings are
conflicting: the response to isometric handgrip but not the
orthostatic systolic hypotension indicates
preserved sympathetic function. However, since the results of the tilt
test were similar for stroke and TIA patients, it seems more likely
that the fall in blood pressure during the tilt test was due to
nonspecific factors rather than to a stroke-induced defect of
sympathetic vasoconstrictor activity. The relationship between the tilt
responses in our TIA and stroke patients on the one hand and the
healthy control subjects on the other hand is similar to that found
previously36 between elderly and young healthy subjects
and is explained primarily by abnormalities in the circulatory system
itself. Also, the reduced brake index/absence of transient bradycardia
in the stroke patients may be a result of slow stabilization of blood
pressure due to vascular factors rather than to primary autonomic
dysfunction. This may lead to an absence of the disinhibition of
parasympathetic tone usually seen after vasoconstriction 10 to 20
seconds after upright posture.35 Thus, a possible
interpretation is that these tests did not reveal a disturbed
sympathetic function but rather an orthostatic response to
passive tilting that may be an expression of general
arteriosclerosis.
Conclusion
Compared with lesions on the left side,
localization of strokes on
the right side of the brain correlates with a reduced parasympathetic
influence on heart rate variability. A corresponding asymmetry with
respect to the sympathetic cardiovascular reflexes was
not found.
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Acknowledgments |
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This study was supported by the foundation "1987 års stiftelse för Strokeforskning" and by Swedish Medical Research Council grant 3546.
Received August 14, 1995; revision received October 16, 1995; accepted October 23, 1995.
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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