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362
Supraventricular Tachycardia in Patients
With Right Hemisphere Strokes
Richard D. Lane, MD; Jan D. Wallace, MD; Patricia P. Petrosky, MD;
Gary E. Schwartz, PhD; and Alan H. Gradman, MD
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Background and Purpose: The physiological basis for the arrhythmias commonly observed after a stroke
is not well understood. Based on evidence that the right and left cerebral hemispheres influence cardiac
function in different ways, we sought to determine whether the nature and severity of cardiac arrhythmias
in the context of an acute stroke vary in relation to whether the stroke is located in the left or the right
hemisphere.
Methods: Data were obtained from the medical records of nineteen patients with left hemisphere strokes
and nineteen patients with right hemisphere strokes who had also had 24-hour electrocardiographic
(Hotter) recordings within 2 weeks of admission to a stroke unit. Written Hotter monitor reports already
on file were used for the data analysis.
Results: All four patients with supraventricular tachycardia had right hemisphere strokes (p=0.05).
There was a nonsignificant trend for left hemisphere stroke patients to have more severe ventricular
arrhythmias.
Conclusions: These data provide partial support for the hypothesis that the two cerebral hemispheres
have a differential influence on the nature and severity of arrhythmias following an acute stroke. We
speculate that parasympathetic tone was diminished ipsilateral to the affected hemisphere associated with
a reciprocal rise in sympathetic tone on that side and recommend that a prospective study be undertaken
to test this hypothesis more definitively. (Stroke 1992;23:362-366)
KEY WORDS • cardiovascular diseases • cerebrovascular disorders • tachycardia
C
hanges in the electrocardiogram have been observed in association with pathological changes
in the central nervous system for over forty
years.1"3 Most studies in this area of research1-8 have
examined changes in the 12-lead electrocardiogram. A
smaller number of reports using continuous cardiac
monitoring have shown a high incidence of arrhythmias
among stroke patients9-10 which exceeds that among
control subjects.11 To date, the mechanisms that could
account for these changes have not been well understood, but a primary focus has been on increased
sympathetic tone,12"16 perhaps through disinhibition of
hypothalamic or other autonomic regulatory centers.16
The purpose of this study was to determine whether
lesions located in the right or left hemisphere influence
the nature and severity of cardiac arrhythmias in a
differential manner.
Several studies in animals17 and patients18 show that the
sinoatrial node is under right autonomic control, and that
From the Department of Psychiatry (R.D.L.), School of Medicine, and the Department of Psychology (G.E.S.), University of
Arizona, Tucson, Ariz.; Warner Lambert Pharmaceutical Co.
(J.D.W.), Ann Arbor, Mich.; the Department of Pediatrics
(P.P.P.), Baystate Medical Center, Springfield, Mass.; and the
Department of Cardiology, Western Pennsylvania Hospital, Pittsburgh, Pa.
Supported by the Department of Veterans Affairs.
Address for correspondence: Richard D. Lane, MD, Department of Psychiatry, University of Arizona, Health Sciences Center, Tucson, AZ 85724.
Received July 2, 1991; accepted October 17, 1991.
stimulation or inhibition of the right medulla,19 hypothalamus,20 and cerebral hemisphere21-24 have a greater influence on heart rate than do comparable changes on the
left. These studies suggest that asymmetries in brain
function influence the heart through ipsilateral pathways.
Other studies demonstrate that an imbalance in sympathetic tone favoring the left side lowers ventricular fibrillation threshold more than an imbalance favoring the
right.25-26 Consistent with the greater ventricular distribution of left-sided sympathetics and the greater supraventricular distribution of right-sided sympathetics,17 stimulation of the right-sided sympathetics is associated with
supraventricular arrhythmias.27
Based on the evidence suggesting that the brain may
influence the heart through ipsilateral pathways and
that arrhythmias after stroke are primarily due to
increased sympathetic tone, we predicted that strokes
on a given side would be associated with cardiac arrhythmias characteristic of ipsilateral sympathetic stimulation. We therefore predicted an association between
1) right-hemisphere strokes and tachyarrhythmias of
supraventricular origin and 2) left-hemisphere strokes
and arrhythmias of ventricular origin.
Subjects and Methods
The records of all patients who were admitted to the
Stroke Unit of the West Haven, Conn., Veterans Affairs
Medical Center over a 4V2-year period were reviewed
for the purposes of this study. There were 723 admissions. Patients diagnosed with strokes (ischemic or
Lane et al
hemorrhagic infarcts of the brain resulting in persistent
neurological deficits) localized to either the right or left
hemisphere were identified. Localization was accomplished primarily on the basis of neurological examination, although data such as findings on computed tomography were used as well when available. The final
diagnosis used was that noted in the data base maintained by the director of the stroke unit. Only patients
whose lesions could be localized to the right or left
hemisphere with certainty were included. Patients with
acute onset of bilateral neurological deficits, lesions in
the brain stem, transient ischemic attacks, ischemic
neurological deficits that resolved before 24-hour electrocardiographic (Holter) monitoring, or lesions with
uncertain location were excluded.
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This list of patients with lateralized strokes was then
cross-referenced with the records of all West Haven
Veterans Affairs Medical Center patients who had ever
undergone 24-hour electrocardiographic (Holter) monitoring. Approximately 20% of the patients admitted to
the stroke unit had undergone Holter monitoring during
their hospitalization. Patients who had undergone
Holter monitoring within 2 weeks after their admission
to the stroke unit and who met the other exclusion
criteria listed above were identified. Nineteen patients
with right-hemisphere strokes and 19 patients with
left-hemisphere strokes met these criteria. The percentage of patients with right- and left-hemisphere strokes
who had had Holter monitor recordings was virtually
identical. The written Holter monitor reports already on
file were used for the data analysis.
Charts that could be located were reviewed to determine age, race, and handedness, as well as the presence
of diabetes mellitus, hypertension, previous myocardial
infarction or coronary artery disease, chronic obstructive pulmonary disease, prior structural central nervous
system lesions, carotid artery disease, indication for
obtaining the Holter recording, and antiarrhythmic
medications on admission. In addition, the accuracy of
the localization of the stroke was verified.
Results
The charts of 18 of 19 right-hemisphere stroke patients
and 17 of 19 left-hemisphere stroke patients were located
and reviewed. All patients were male except for one
female left-hemisphere stroke patient. The mean age of
right-hemisphere stroke patients was 68.2 (SD=13.1)
years compared with a mean age of 63.8 (SD=11.1) years
for left-hemisphere stroke patients (t 33=1.06, NS). Except for two right-hemisphere stroke patients who were
black, all patients were white. The number of patients in
each of the two groups who were left-handed as well as
the number of patients in each group who had diabetes
mellitus, hypertension, coronary artery disease including prior MI, COPD, and prior lateralized strokes is
indicated in Table 1.
These charts were also reviewed to determine
whether patients were receiving medication(s) at the
time of admission that might alter the propensity for
cardiac arrhythmias. Among the 18 patients with righthemisphere strokes, five were receiving /3-blockers
alone (for hypertension or angina), three were receiving
digoxin alone, one was receiving quinidine alone, and
one was receiving digoxin and quinidine. Among the 17
Stroke Laterality and Arrhythmias
363
TABLE 1. Number of Patients With Right- and Left-Hemisphere
Strokes With Various Clinical Characteristics
Hemisphere
Right
Left
Clinical characteristic
Left-handed
Diabetes mellitus
Definite
Possible
Hypertension
Essential
Labile or borderline
Coronary artery disease
(including myocardial infarction)
Definite
Possible
Chronic obstructive pulmonary diseases
Prior lateralized strokes
Left
Right
Antiarrhythmic medications
3
2
6
6
0
1
12
7
0
4
8
0
1
6
1
4
0
1
1
10
5
3
patients with left-hemisphere strokes, two were receiving digoxin alone, two were receiving digoxin plus
propranolol, and one was receiving digoxin plus quinidine. The remainder of the patients were receiving
medications that did not have antiarrhythmic effects.
Charts were also reviewed to determine the indication
for obtaining the Holter monitor recording. In over one
third of cases the recording was obtained without specific
indication as part of a broad search for a possible
etiology of the stroke ("rule-out arrhythmia"). The indications and their frequency are listed in Table 2.
An independent set of records was also reviewed to
determine whether ultrasound studies of the internal
carotid arteries had been done within 6 months after
patient admission to the stroke unit. Six of 19 patients
with right-hemisphere strokes and eight of 19 patients
with left-hemisphere strokes had had such studies done.
Among the patients with right-hemisphere strokes, three
had equivalent degrees of disease on the two sides, two
had more severe disease on the left that was not hemodynamically significant, and one had more severe disease
on the right that was hemodynamically significant.
Among the patients with left-hemisphere strokes, four
TABLE 2. Indications for Holter Monitor Recording
Hemisphere
Indication
Rule-out arrhythmia
Bradycardia
History of atrial arrhythmia
History of ventricular arrhythmia
Frequent premature ventricular contractions
Rule-out demand pacemaker malfunction
Syncope
Angina, recent myocardial infarction
Right
Left
(n = 18) (n = 15*)
7
1
6
1
3
2
1
4
0
1
3
2
1
1
0
0
"Two charts reviewed originally could not be located for reanalysis.
364
Stroke
Vol 23, No 3 March 1992
TABLE 3. Number of Patients With Right- and Left-Hemisphere
Strokes With Supraventricular Arrhythmias of Varying Severity
Categories
Right (« = 18) Left (n = 18)
No PACs
Rare PACs
Occasional PACs
Frequent PACs
Supraventricular tachycardia
4
4
8
10
0
2
3
1
4
0
P*
0.65
0.37
0.11
0.50
0.05
PAC, premature atrial contraction.
*For each category, a 2x2 table (right-left, present-absent) was
created and the probability of that result calculated. Probabilities
shown reflect one-tailed tests. A probability value of <0.05 was
considered statistically significant.
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had equivalent degrees of disease on the two sides, three
had greater disease on the left that was not hemodynamically significant, and one had greater disease on the right
that was hemodynamically significant.
One right-hemisphere and one left-hemisphere
stroke patient were in atrial fibrillation. The remaining
patients were classified according to the severity of
supraventricular arrhythmias manifested. Premature
atrial contractions were categorized as follows: no
(none), rare (1-2/min), occasional (3-4/min), or frequent (5-6/min). Supraventricular tachycardia (SVT)
was defined as three or more consecutive supraventricular beats at an average rate of > 100 beats per minute.28
Each patient was classified in the category of greatest
severity.
The results are shown in Table 3. In general, patients
with right-hemisphere strokes had more severe supraventricular arrhythmias. The difference between the
two groups in number of patients with SVT was statistically significant.
Ventricular arrhythmias were classified according to
a modification of the Lown grading system.29 The categories included no premature ventricular contractions
(PVCs), uniform PVCs, multiform PVCs, couplets, and
ventricular tachycardia. No distinction was made between <30 or >30 PVCs per hour, nor was the presence
or absence of R on T included because these distinctions were not always addressed by the original reader.
Ventricular tachycardia was defined as three or more
consecutive beats of ventricular origin at an average rate
>100 beats per minute. Each patient was classified in
the category of greatest severity.
The results are shown in Table 4. There were no
statistically significant differences in any of the categoTABLE 4. Number of Patients With Right Hemisphere and Left
Hemisphere Strokes With Ventricular Arrhythmias of
Varying Severity
Categories
No PVCs
Rare PVCs
Multiform PVCs
Couplets
Ventricular tachycardia
Right (« = 19)
Left (n = 19)
P*
3
1
6
4
4
4
5
3
0.30
0.36
0.36
0.50
0.50
2
6
PVC, premature ventricular contraction.
*For each category, a 2x2 table (right-left, present-absent) was
created and the probability of that result calculated. Probabilities
shown reflect one-tailed tests. A probability value of <0.05 was
considered statistically significant.
ries. However, there was a nonsignificant trend (p=0.16
by Fisher's exact test) for patients with left-hemisphere
strokes to have more severe ventricular arrhythmias,
illustrated by collapsing the first two categories (no
premature atrial contractions and rare premature atrial
contractions) into a "less severe" group and the last
three categories into a "more severe" group.
Discussion
These data provide partial support for the hypothesis
that right- and left-hemispheric lesions are associated with
different types of cardiac arrhythmias. The finding that
SVT was found only in patients with right-sided strokes is
consistent with the literature showing that hemispheric
modulation of cardiac function is predominantly ipsilateral. This finding is also consistent with a case report30
describing a patient with a tumor in the right frontal lobe
who experienced repeated bouts of SVT until the tumor
was excised, after which time SVT did not recur.
The two groups of stroke patients were comparable in
terms of handedness, diabetes, chronic obstructive pulmonary disease, prior arrhythmia history, and coronary
artery disease, including past myocardial infarction.
Although more right-sided stroke patients were hypertensive, taking )3-blockers, and had prior structural
lesions of the central nervous system on the contralateral side, these differences (none were statistically significant) cannot explain the association between SVT
and right-sided strokes: none of the four patients with
SVT had a history of SVT before the index admission,
and only one of the four patients with SVT had had a
prior lateralized stroke. Because /3-blockers are an
effective treatment for most cases of SVT,31 the greater
use of /3-blockers in patients with right-sided strokes
may have masked an even larger association with SVT.
Supraventricular tachycardia is a heterogeneous phenomenon, the subtype of which can be elucidated in most
cases by special leads and bedside maneuvers. Unfortunately, such special techniques were not used in this study.
However, it is known that SVT is initiated by one of three
general mechanisms: reentry, enhanced automaticity, and
triggered automaticity.32 All three mechanisms can be
activated by an increase in sympathetic tone.32 Reentry is
the cause in over two thirds of cases,31 and triggered
automaticity is least common. Asymmetry in sympathetic
tone is well accepted as a source of reentry.33
The findings of Yokoyama and colleagues,34 who
demonstrated that patients with right-hemisphere
strokes manifested impairment in a parasympathetically
mediated heart-rate response, make it possible to hypothesize how right-sided strokes can induce SVT. The
parasympathetic innervation of the heart follows a
course parallel to that of the sympathetics.35 Although a
decrease in parasympathetic tone would be associated
with an increase in atrial refractoriness,36 the probable
reciprocal rise in sympathetic tone37 could enhance
automaticity, increase the dispersion of refractory periods (and the propensity for reentry), or increase the
likelihood of triggered automaticity.
The finding of a nonsignificant trend linking leftsided strokes with ventricular arrhythmias can be understood in several different ways. 1) Only the right
hemisphere has a direct influence on cardiac function.
Although only patients with right-hemisphere impair-
Lane et al
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merit have been shown to manifest attenuated autonomic arousal,22-23-38"40 no previous study, to our knowledge, has been specifically designed to look at the
relation between left-hemisphere function and leftsided autonomic influences on the heart. 2) A weaker
relation with unilateral stroke would be expected with
ventricular compared to supraventricular arrhythmias,
to the extent that the effects of unilateral stroke are
primarily mediated through parasympathetic mechanisms: the latter are dominant in the atria, whereas
sympathetic mechanisms are dominant in the ventricles.
3) The greater proportion of old contralateral central
nervous system lesions in the right-sided stroke patients
weakened a larger true difference between the groups.
The opposing view that a greater use of /3-blockers in
the right-sided stroke group should have increased this
difference is not likely, in that three of these five
patients were classified in the more severe ventricular
arrhythmia group.
Lane and Schwartz41 hypothesized that emotion may
trigger ventricular arrhythmias and sudden death
through lateralized hemispheric activation, which may
get channeled downstream to induce a lateralized imbalance in sympathetic input to the heart. Our findings
are consistent with this hypothesis in that right-hemispheric lesions appeared to influence cardiac rhythm
through ipsilateral autonomic mechanisms. It may be
necessary to induce hemispheric asymmetry through
activation rather than inhibition (as in this study) to
adequately test the applicability of this model to ventricular arrhythmias.
In conclusion, these data provide partial support for
the hypothesis that the right and left hemispheres
influence the nature and severity of cardiac arrhythmias
in a differential manner. A prospective study is now
needed in which Holter monitor recordings are obtained on consecutively admitted stroke patients. Such a
study could also include greater control of variables
such as type of lesion (e.g., ischemic versus hemorrhagic
infarct), exact location of the lesion, time interval from
onset of symptoms to Holter recording, handedness,
and prior structural central nervous system lesions, as
well as more precise quantification of other relevant
conditions such as diabetes, hypertension, chronic obstructive pulmonary disease, coronary artery disease,
prior arrhythmias, medications that decrease or increase the propensity for certain types of arrhythmias,
and electrolyte abnormalities. In addition, once arrhythmias are detected, new cardiological techniques31 could
be used to further elucidate the likely proximal electrophysiological mechanisms involved.
Acknowledgments
This work was supported by the Department of Veterans
Affairs, and was conducted in the Stroke Unit, West Haven
Veterans Affairs Medical Center, West Haven, Conn.
References
1. Byer E, Ashman R, Toth L: Electrocardiogram with large, upright
T waves and long Q-T intervals. Am Heart J 1947;33:796-806
2. Burch G, Myers R, Abildskov J: A new electrocardiographic
pattern observed in cerebrovascular accidents. Circulation 1954;9:
719-723
3. Wasserman F, Choquette G, Cassinelli R, Bellet S: The electrocardiographic observations in patients with cerebrovascular accident. Am J Med Sci 1956;231:502-510
Stroke Laterality and Arrhythmias
365
4. Kreus K, Kemila S, Takala J: Electrocardiographic changes in
cerebrovascular accidents. Ada Med Scand 1969;185:327-334
5. Eisalo A, Perasalo J, Halonen P: Electrocardiographic abnormalities and some laboratory findings in patients with subarachnoid
hemorrhage. Br Heart J 1972;34:217-226
6. Hansson L, Larsson O: The incidence of ECG abnormalities in
acute cerebrovascular accidents. Ada Med Scand 1974;195:45-47
7. Goldstein D: The electrocardiogram in stroke: Relationship to
pathophysiological type and comparison with prior tracings. Stroke
1979;10:253-259
8. Melin J, Fogelholm R: Electrocardiographic findings in subarachnoid hemorrhage. Ada Med Scand 1983;213:5-8
9. Lavy S, Yaar I, Melamed E, Stern S: The effect of acute stroke on
cardiac functions as observed in an intensive stroke care unit.
Stroke 1974;5:775-780
10. Britton M, de Faire U, Helmers C, Miah K, Ryding C, Wester P:
Arrhythmias in patients with acute cerebrovascular disease. Ada
Med Scand 1979;205:425-428
11. Mikolich J, Jacobs C, Fletcher G: Cardiac arrhythmias in patients
with acute cerebrovascular accidents. JAMA 1981;246:1314—1317
12. Norris J, Froggatt G, Hachinski V: Cardiac arrhythmias in acute
stroke. Stroke 1978;9:392-396
13. Abildskov J, Millar K, Burgess M, Vincent W: The electrocardiogram and the central nervous system. Prog Cardiovasc Dis 1970;
13:210-216
14. Talman W: Cardiovascular regulation and lesions of the central
nervous system. Ann Neurol 1985;18:1—12
15. Natelson BH: Neurocardiology: An interdisciplinary area for the
80s. Arch Neurol 1985;42:178-184
16. Oppenheimer S, Cechetto D, Hachinski V: Cerebrogenic cardiac
arrhythmias. Arch Neurol 1990;47:513-519
17. Randall W, Armour J, Geis W, Lippincott D: Regional cardiac
distribution of the sympathetic nerves. Fed Proc 1972;31:1199—1208
18. Rogers M, Battit G, McPeek B, Todd D: Lateralization of sympathetic control of the human sinus node: ECG changes of stellate
ganglion block. Anesthesiology 1978;48:139-141
19. Henry J, Calaresu F: Excitatory and inhibitory inputs from medullary nuclei projecting to spinal cardioacceleratory neurons in the
cat. Exp Brain Res 1974;20:485-504
20. Fang H, Wang S: Cardioaccelerator and cardioaugmentor points in
hypothalamus of the dog. Am J Physiol 1962;203:147-150
21. Zamrini E, Meador K, Loring D, Nichols F, Lee G, Figueroa R,
Thompson W: Unilateral cerebral inactivation produces differential left/right heart rate responses. Neurology 1990;40:1408-1411
22. Rosen A, Gur RC, Sussman N, Gur RE, Hurtig H: Hemispheric
asymmetry in the control of heart rate (abstract). Neurosci Abstr
1982;8:917
23. Lane R, Novelty R, Cornell C, Zeitlin S, Schwartz G: Asymmetric
hemispheric control of heart rate. Psychophysiology 1988;25:464
24. Lane R, Abrams R, Swartz C, DuBois M, Van A: Differential
effects of right and left unilateral ECT on heart rate. Psychophysiology 1991;28(3A):S36
25. Lown B, Verrier R, Rabinowitz S: Neural and psychologic mechanisms and the problem of sudden cardiac death. Am J Cardiol
1977;39:890-902
26. Schwartz P: Sympathetic imbalance and cardiac arrhythmias, in
Randall W (ed): Nervous Control of Cardiovascular Function. New
York, Oxford University Press, Publishers, 1984, pp 225-252
27. Randall W, Thomas J, Euler D, Rozanski G: Cardiac dysrhythmias
associated with autonomic nervous system imbalance in the conscious dog, in Schwartz P, Brown A, Malliani A, Zanchetti A (eds):
Neural Mechanisms in Cardiac Arrhythmias. New York, Raven
Press, Publishers, 1978, pp 123-138
28. Wellens H, Bragado P: Mechanisms of supraventricular tachycardia. Am J Cardiol 1988;62:10D-15D
29. Lown B, Wolf M: Approaches to sudden death from coronary
disease. Circulation 1971;44:130-142
30. Rush J, Everett B, Adams A, Kusske J: Paroxysmal atrial tachycardia and frontal lobe tumor. Arch Neurol 1977;34:578-580
31. Manoli A, Estes M: Supraventricular tachycardia: Mechanisms and
therapy. Arch Intern Med 1987;147:1706-1716
32. Braunwald E (ed): Heart Disease: A Textbook of Cardiovascular
Medicine, ed 3. Philadelphia, Pa, WB Saunders Co, 1988
33. Han J, Moe G: Nonuniform recovery of excitability in ventricular
muscle. Circ Res 1964;14:44-60
34. Yokoyama K, Jennings R, Ackles P, Hood P, Boiler F: Lack of
heart rate changes during an attention-demanding task after right
hemisphere lesions. Neurology 1987;37:624-630
35. Higgins C, Vatner S, Braunwald E: Parasympathetic control of the
heart. Pharmacol Rev 1973;25:119-155
366
Stroke
Vol 23, No 3 March 1992
36. Zipes D, Mihalick M, Robbins G: Effects of selective vagal and
stellate ganglion stimulation on atrial refractoriness. Cardiovasc
Res 1974;8:647-655
37. Berne R, Levy M: The autonomic nervous system and its central
control, in Berne R, Levy M (eds): Physiology, ed 2. St Louis, Mo,
CV Mosby Co, 1988
38. Heilman K, Schwartz H, Watson R: Hypoarousal in patients with
the neglect syndrome and emotional indifference. Neurology 1978;
28:229-232
39. Morrow L, Vrtunski P, Kim Y, Boiler F: Arousal responses to emotional stimuli and laterality of lesion. Neuropsychologia 1981; 19:65-71
40. Zoccolotti P, Caltagirone C, Benedetti N, Gainotti G: Perturbation
des responses vegetatives aux stimuli emotionnels au cours de
lesions hemispheriques unilaterales. L'Encephale 1986;12:263-268
41. Lane R, Schwartz G: Induction of lateralized sympathetic input to
the heart by the CNS during emotional arousal: A possible
neurophysiologic trigger of sudden cardiac death. Psychosom Med
1987;49:274-284
Downloaded from http://stroke.ahajournals.org/ by guest on June 11, 2017
Supraventricular tachycardia in patients with right hemisphere strokes.
R D Lane, J D Wallace, P P Petrosky, G E Schwartz and A H Gradman
Stroke. 1992;23:362-366
doi: 10.1161/01.STR.23.3.362
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