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Observations on the electrocardiographic changes associated with subarachnoid hemorrhage with special reference to their genesis
Observations on the Electrocardiographic
Changes
Associated with Subarachnoid Hemorrhage with Special Reference to Their Genesis
WILLIAM J. HAMMER, M.D.’ ALFRED J. LUESSENHOP, ALAN M. WEINTRAUB.
M.D.
M.D.
Washington, D. C.
From the Department of Medicine (Division of Cardiology) and the Department of Surgery (Division of Neurosurgery), Georgetown University School of Medicine, Georgetown University Hospital, Washtngton, D.C. This work was carried out under the tenure of a U.S. Public Health Service training grant fellowship to Dr. Hammer (Grant No. 2 T12 HE-05433) and was funded by the National Institutes of Health, Bethesda, Maryland. Requests for reprints shoukt be addressed to Dr. Alan M. Weintraub. Georgetown University School of Medicine, Georgetown University Medical Center, 3800 Reservoir Road, N.W., Washington, D.C. 20007. Manuscript accepted October 7. 1974. Present address: Department of Medicine, Division of Cardiology, Temple University Health Science Center, Philadelphii, Pennsylvania. l
A 36 year old man presented with bizarre behavior and had abnormal electrocardiograms on two occasions. Because of ST-T wave changes, he was treated both times for a possibie subendocardial infarction. A more complete evaluation during the second admission revealed a basilar artery aneurysm with subarachnoid hemorrhage as the cause of the central nervous system symptoms. While the aneurysm was successfully clipped, the patient’s electrocardiogram was recorded. Several electrocardiographic changes characteristic of intracranial disease were observed during the procedure. These changes developed with distortion of the circle of Willis and reverted when such distortion stopped. We review the spectrum of the electrocardiographic changes associated with intracranial disease. This list of abnormalities was compiled from observations obtained by the impatient tracings of persons with various central nervous system pathology. The mechanisms used to explain the ahanges are based soieiy on work performed on laboratory animals. The results of our findings in our patient link electrocardiqraphic abnormalities directly with a central nervous system lesion. Over the last two decades a variety of electrocardiographic abnormalities have been associated with intracranial disease, especially subarachnoid hemorrhage [ 1- 131. Various theories, principally involving the autonomic nervous system, have been proposed to account for these abnormalities [3,5,9,12,14-241. The basis for these theories is experiments performed only on laboratory animals. These results have been extrapolated to man to explain the various electrocardiographic changes accompanying intracranial disease. We describe a patient who presented with an abnormal electrocardiogram, and in whom a diagnosis of basilar artery aneurysm with subarachnoid hemorrhage was subsequently made. Surgical intervention afforded the opportunity to make serial observations with a full 12 lead electrocardiogram monitor and to link the experimental work with the actual changes in man. The results support the theory that the local effects of the aneurysm are the initiating mechanism for the characteristic electrocardiographic changes accompanying subarachnoid hemorrhage.
September 1975
The American Journal of Medicine
Volume 59
427
ELECTROCARDIOGRAPHIC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
ET AL
-_
._.
3 Figure 7. These tracings show the sequence of electrocardiographic changes that occurred with two separate hospitalirations involving central nervous system symptoms.
CASE REPORT A 36 year old Caucasian man was admitted to the Georgetown University Medical Center on September 6, 1973. His pertinent medical history began on August 6, 1972, when he entered the emergency room of a local hospital with complaints of vague chest pain. At that time he was confused and was disoriented to time and place. The remainder of the physical examination was within normal limits. An electrocardiogram showed normal sinus rhythm with occasional premature ventricular contractions, right axis deviation, slight S-T segment elevation in leads II, Ill and aVF, and poor R wave progression from leads VI to Vs (Figure 1A). Over the next 46 hours the patient’s confusion cleared, and he became asymptomatic. The electrocardiogram continued to show a normal sinus rhythm and right
Figure 2. Carotid arteriogram demonstrates basilar artery aneurysm.
428
September 1975
The American Journal of Medicine
axis deviation; however, the T waves became deeply inverted in leads I, aVL and V2 to Vs (Figure 1B). The premature ventricular contractions had disappeared, and slight S-T segment elevation was present in leads II and aVF. Over the next 12 days the patient remained asymptomatic and the results of his physical examination continued to be within normal limits. Laboratory results, including creatinine phosphokinase, lactate dehydrogenase and transaminase, were all within normal limits. The electrocardiogram, however, did not change. The patient was discharged after 21 days with the diagnosis of anterolateral subendocardial infarction. He subsequently was lost to follow-up for a year. On August 31, 1973, his landlady found him in a delirious and combative state. He was taken by police to the same emergency room as before. The results of the initial physical examination were negative, except for disorientation. An electrocardiogram showed occasional premature ventricular contractions, right axis deviation and poor R wave progression from leads VI to Vs. The previously mentioned T wave inversions were not present (Figure 1C). The patient was admitted for observation. During the ensuing 12 hours he became more stuporous and had nuchal rigidity. A spinal tap yielded grossly bloody fluid. The electrocardiogram had undergone additional changes by 24 hours. There was now marked T wave inversion in leads I, II, aVL and V2 to Vs. A suggestion of S-T segment elevation was again noted in leads II, Ill and aVF. Right axis deviation of the QRS and normal sinus rhythm persisted (Figure 1D). The creatinine phosphokinase level increased to 463 units, 372 units and 265 units (normal 0 to 60 units) on the 3 subsequent days. Because of the possibility of an acute myocardial infarction, no further diagnostic procedures were performed. Six days later, when no evolution of a myocardial process was seen and there was no improvement in the neurologic picture, the patient was transferred to the Georgetown University Medical Center.
Volume 59
ELECTROCARDIOGRAPHIC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
f --
.
-.
.: ,i
‘- __
^_!
‘:y ;_ -
Figure 3. A tracing performed leads I, a VL and V3 to V,.
1
inverted
I
I I i I
after the induction of anesthesia.
On admission the patient was confused, stuporous and had nuchal rigidity. There were no localizing signs. A carotid arteriogram was performed, and a basilar artery aneurysm was demonstrated (Figure 2). On the 4th hospital day the patient underwent craniotomy; general anesthesia with nitrous oxide was administered. At surgery the temporal lobe was retracted and, with the aid of an operating microscope, dissection along the posterior cerebral artery was performed. The basilar artery aneurysm was identified and was projecting into the interpeduncular cistern. Numerous adhesions were stripped away from the vicinity of the lesion. The neck of the aneurysm was successfully clipped with a small Scoville clamp without provoking any bleeding. At this time, traction was applied to the posterior cerebral artery and to the circle of Willis to allow adequate
previously
i I
I
ET AL.
i
Note T wave inversion
in
visualization. The temporal lobe was then allowed to fall back and the dura mater and bone flaps were closed without complications. The temperature was 94’F throughout the procedure. Blood pressure was 90150 mm Hg at the beginning of the procedure and decreased to 75140 mm Hg at the time of temporal lobe retraction. lt remained at this level until the dura mater was closed. The potassium level was 3.8 meq/liter preoperatively and 3.7 meq/liter postoperatively. The sodium, chloride and carbon dioxide combining powers were unchanged postoperatively from the normal values obtained preoperatively. The patient’s immediate postoperative course was uneventful, and his level of consciousness gradually improved. A persistent third nerve deficit was noted on the right side. On the 6th postoperative day, however, there
T waves in leads V3 to V6 are now upright.
September 1975
The American Journal of Medicine
Volume 59
429
ELECTROCARDOGFIAPHIC
CHANGES IN SUBARACHNOlD HEMORRHAGE-HAMMER
ET AL.
tained 2 minutes after the one in Figure 4. The rhythm has become junctional.
was an abrupt decline in the level of consciousness, and a right hemiparesis developed. A repeat angiogram demonstrated diffuse spasm of the left cerebral vessels, but no specific lesion was seen. After several weeks it became apparent that our patient showed no improvement; a global aphasia and right hemiparesis persisted. MATERIALS
AND METHODS
The patient was monitored during the surgical procedure with a Hewlett-Packard three channel recorder and conventional lead placement [25]. Monitoring was begun at the induction of anesthesia and concluded with the termination of the procedure. A full 12 lead tracing was taken every 5 minutes or when major surgical manipulation was announced by the neurosurgeon. Blood pressure was determined every 5 minutes with a sphygmomanometer placed over the right brachial artery. A constant temperature recording was obtained by a rectal thermocouple. Electrolytes were determined pre- and postoperatively by the routine hospital laboratory. RESULTS On admission
to the Georgetown
University Medical
Center, the patient’s electrocardiogram showed normal sinus rhythm with a rate of 62 beats/min. The P-R interval was 0.14 second. There was right axis deviation of the QRS and T wave inversion in leads I, aVL and VJ to Vg. The first full tracing after induction of anesthesia was similar to the tracing obtained on admission and is shown in Figure 3. Shortly after this recording, the electrode in the lead V2 position became detached. The electrocardiograni remained unchanged from the control tracing while the bone flaps were removed, the dura mater was cut, the temporal lobe retracted and the previously described dissec-
430
September
1975
The American Journal ot Medkine
tion performed.
_
With tension applied to the posterior
cerebral artery and with distortion of the circle of Willis, a series of changes occurred in rapid sequence. First, the T waves in leads V3 to Ve became more upright. Then the T wave in lead I became less negative, and the T waves in leads II, Ill and aVF became pronounced. This is shown in Figure 4. Immediately after these T wave changes, the rhythm became junctional as seen in Figure 5. With release of the traction applied to the aforementioned vessels, the electrocardiogram immediately reverted to a pattern similar to the control tracing with sinus rhythm and T wave inversion in leads I, aVL and Vs to V6 (Figure 6). Except for occasional premature ventricular contractions while the dura mater was closed, there were no further changes in the tracings during the remainder of the procedure. COMMENTS During the last two decades many clinicians have observed abnormalities in the electrocardiograms of patients with intracranial disease, especially subarachnoid hemorrhage. The changes that are generally accepted are listed in Table I [3,1 I]. With regard to arrhythmias, Cropp and Manning [4] have reported an increased incidence of premature ventricular contractions, and wandering atrial pacemaker and junctional rhythms. Poole [6] and Gallon et al. [ 1 l] have noted sinus bradycardia and atrioventricular dissociation. A marked increase in the amplitude of the P wave to greater than 2.5 mm has been reported by Hersch [ 61 and Eisalo et al. [ 91. Both S-T segment elevation and depression great-
volume 59
ELECTROCAROlOGRAPHlC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
ET AL.
Figure 6. With release of the tension on the circle of Willis, two changes occurred immediately. The rhythm became sinus in origin, and the T waves in leads V, to V6 were once again inverted. There was also more prominent T wave inversion in leads I and a VL.
er than 1.0 mm have been seen [8,11]. T wave inversion is also apparently a common phenomenon [ l-31. Elevated T waves have been observed in the early phase after a cerebrovascular accident [2325]. Prominent U waves have also been observed [2,3,6]. The Q-T interval is prolonged according to several investigators [4,6,9,24]. Burch et al. [2] questioned this finding and suggested that the prominent U wave may merge with the T waves thereby giving a prolonged Q-U interval mimicking an increased Q-T interval. Abnormalities of the QRS complex per se have not been documented. A patient with an intracranial process may have one or more of these changes, and their incidence tends to increase as the person’s neurologic status deteriorates [ 81. Although there is general agreement that the aforementioned electrocardiographic changes are associated with intracranial disease, there is less consensus as to the cause of the phenomena. Welt et al. [ 191 observed the occurrence of hyponatremia and hypothermia in patients with brain injury. Some investigators have attempted to link these and other metabolic abnormalities, especially hypokalemia, with the electrocardiographic changes but they were unsuccessful [20]. Poole [5] demonstrated, at the time of stimulation of the circle of Willis, a sinus bradycardia in persons undergoing neurosurgical procedures. This change could be induced only if the patient was hypothermic and was under light anesthesia. The investigator postulated that this change in heart rate was secondary to a vagocardiac reflex initiated by local stimulation of the autonomically rich circle of Willis. After this re-
port, other investigators produced some of the characteristic electrocardiographic changes by stimulating various parts of the central nervous system in experimental animals. Kontweig et al. [21] produced nonspecific ST-T wave changes with stimulation of the subcortical areas in dogs. Manning and Cotten [ 171 stimulated the hypothalamus of cats and were able to show ST-T wave abnormalities. Interest then shifted from an emphasis on the local stimulating effects of the intracranial lesion to the work emphasizing the importance of the autonomic nervous system in the genesis of the characteristic electrocardiographic abnormalities. Jacobson and Danufsky [ 161 produced experimental head trauma in dogs and were able to produce some of the charTABLE
September 1975
I
Generally Accepted Electrocardiographic Changes Associated with Intracranial Disease (3, 11,
131
1. Conduction
2.
3. 4. 5. 6. 7. 8. 9.
disturbances a. Shortened P-R interval b. Junctional rhythms c. Atrioventricular dissociation Arrhythmias a. Sinus bradycardia b. Ventricular premature beats c. Atrial premature beats d. Wandering atrial pacemaker Prominent P waves S-T segment elevation S-T segment depression T wave inversion Prominent upright T waves Prominent U waves Prolonged Q-T interval
The American Journal of Medicine
Volume 5g
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ELECl-RDCARDlDGRAPHlCCHANGES IN SUBARACHNOlD HEMORRHAGE-HAMMER ET AL.
acteristic changes in the tracing which could be blocked by the administration of atropine. Barger et al. [ 141 noted that the tall peaked P waves which occurred with the intracranial processes could also be produced by the administration of epinephrine to a normal subject. Shuster [3] was able to reverse the S-T segment depression seen in subarachnoid hemorrhage with the administration of atropine. The S-T segment elevation and T wave changes produced by stimulation of the diencephalon of cats was prevented by high section of the cervical sympathetic chain [22]. Offerhaus and Van Gool [ 151 experimentally induced subarachnoid hemorrhages in rabbits. Premature ventricular contractions and S-T segment elevations were observed, and both were blocked by the administration of propranolol. The aforementioned data certainly seemed to implicate the autonomic nervous system in the development of the electrocardiographic changes. lt was interpreted by some investigators that the primary site of the central nervous system pathology was relatively unimportant, and that almost any intracranial stimulation would result in activation of the autonomic nervous system with the subsequent electrocardiographic changes caused by autonomic discharge
[121.
Several investigators have suggested more elaborate explanations. They believe that the electrocardiographic changes are representative of actual myocardial lesions such as subendocardial hemorrhage and necrosis [26,27]. Such a pathologic process could be caused by an excess of circulating catecholamines produced by a mechanism independent of the primary site of intracerebral disease [lO,ll]. The myriad of information does not clearly lead to one mechanism which could explain the production of the electrocardiographic changes seen in intracranial disease. Burch and Philips’ [23] analysis of the
data concludes that the essential ingredient to cause these changes seems to be a specific intracranial injury which results in an autonomic discharge that is reflected in the electrocardiogram. The observations related to the study of our patient are unique. The characteristic electrocardiographic changes associated with intracranial disease, especially subarachnoid hemorrhage, have been derived from empiric observation [l-l 21. The mechanisms used to explain these changes are derived from experiments with laboratory animals. Our patient provided an opportunity to link an observed change directly to one of these proposed mechanisms. He initially presented with electrocardiographic abnormalities which are commonly associated with subarachnoid hemorrhage. A basilar artery aneurysm and subarachnoid hemorrhage were subsequently demonstrated. With manipulation of the aneurysm and the adjacent vessels resulting in distortion of the circle of Willis, electrocardiographic changes were produced during surgery. These changes occurred almost immediately with the manipulation, and they disappeared in the same manner when the manipulation was discontinued. The electrolytes and the body temperature clearly did not play a role in the genesis of these changes. The amount of anesthesia was not a deciding factor. None of the other intracranial manipulations performed during surgery produced any changes in the electrocardiogram. It is also quite unlikely that actual myocardial damage could have caused changes which would appear and then disappear in the manner described. These observations, therefore, are the first to be noted in man, which clearly support the hypothesis that the local effects of the aneurysm, operating possibly through the autonomic nervous system, are a necessary inciting stimuli for the well known electrocardiographic changes associated with subarachnoid hemorrhage.
REFERENCES 1.
2.
3. 4.
5. 6.
432
Levine l-ID: Non-specificity of the electrocardiogram associated with coronary artery disease. Am J Med 15: 344, 1953. Burch GE, Myers R, Abildskov JA: A new electrocardiographic pattern observed in cerebra-vascular accidents. Circulation 9: 719, 1954. Shuster S: The electrocardiiram in subarachnoid hemorrhage. Br Heart J 22: 316, 1960. Cropp 61, Manning GW: Electrocardiographic changes sim ulating myocardiil ischemia and infarction associated with spontaneous subarachnold hemorrhage. Circulation 22: 25, 1960. Poole JL: Vasocardiac effects of the circle of Willis. Arch Neurol Psychiatry 78: 355, 1957. Hersch C: Electrocardiographic changes in head injury. Circulation 23: 853, 1961.
September
1975
The Amerkan
Journal of Medlclne
7. 8. 9.
10.
11.
12.
Schubart AF, Marriott HJL, Gorten RJ: lsorhythmic dissociation. Am J Med 24: 209. 1958. Hersch C: The electrocardiogram in cerebral disease. Br Heart J 26: 785, 1964. Eisalo A, Perasalo J. Halonen PI: Electrocardiographic abnormalitiis and some laboratory findings in patients with subarachnoid hemorrhage. Br Heart J 34: 217, 1972. Umall F, Gould L, Gomprecht RF: The electrocardiographic changes in intracerebral lesions. Angiology 22: 616, 1971. Gallon S, Rees GAD, Briscoe CE. Davies S, Kilpatrick GS: Prospective study of electrocardiographic changes associated with subarachnokl hemorrhages. Br J Anaesth 44: 511.1972. McIntyre JWR, Dobson D, Weir BKA, West R, Overton TR: Monitoring under anesthesia with reference to subarach-
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ELECTROCARDIOGRAPHICCHANGES IN SURARACHNOIO HEMORRHAGE-HAMMER ET AL.
13. 14.
15.
16.
17.
18.
19.
20.
noid hemorrhage and the T wave as an electrocardiographic manifestation. Can Anaesth Sot J 18: 293, 1971. Surawicz B: Electrocardiographic pattern of cerebrovascular accident. JAMA 197: 913, 1966. Barger AC, Liebowitz MR. Herd JA: Chronic catheterization of the coronary artery. Infusion of autonomic drugs in the unanesthetized dog. Fed Proc 20: 101. 1961. Offerhaus L, Van Go01 J: Electrocardiographic changes and tissue catecholamines in experimental subarachnoid hemorrhage. Cardiovasc Res 3: 433, 1969. Jacobson SA, Danufsky P: Marked electrocardiographic changes produced by experimental head trauma. J Neuropathol Exp Neurol 13: 462. 1954. Manning JW, Cotten M: Mechanism of cardiac arrhythmia induced in diencephalic stimulation. Am J Physiol 203: 1120. 1962. Melville KI, Blum B, Shuster HF, Silver M: Card&c ischemic changes and arrhythmia induced by hypothalmic stimulation. Am J Cardiol 12: 787. 1963. Welt LG. Seldin DW, Nelson WP. German WJ. Peters JP: The role of the central nervous system in metabolism of electrolytes and water. Arch Intern Med 90: 355, 1952. Wasserman F, Bellet S: The electrocardiographic observa-
21.
22.
23.
24.
25. 26.
27.
28.
September 1975
tions in patients with cerebrovascular accident. Am J Med Sci 231: 502, 1956. Kontweig B, Bolts CT, Ten Cote J: Influence of stimulation of some subcortical areas on the electrocardiogram. J Neurophysiol20: 100, 1957. Ponta R: Persistent electrocardiographic abnormalities experimentally induced by stimulation of the brain. Am Heart J 69: 815, 1964. Burch GE, Philips JH: The upright T wave as an electrocardiographic manifestation of intracranial disease. South Med J 61: 331, 1988. Tobin JL: Complications of meningococcus infection in a series of sixty-three sporadic cases. Am J Med Sci 231: 241, 1956. Marriott H: Practical Electrocardiography. 5th ed, Baltimore, Williams & Wilkins, 1972. Kreus K, Kremilin SJ. Takala JK: Electrocardiographic changes in cerebrovascular accidents. Acta Med Stand 185: 327, 1969. Koskelo P. Pensan S. Sipila W: Subendocardial hemorrhage and electrocardiographic changes in intracranial bleeding. Br Med J 1: 1479, 1964. Greenhort JH, Runchenback DD: Cardiac injury and subarachnoid hemorrhage. A clinical, pathologic and physiological correlation. J Neurosurg 30: 521. 1969.
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Changes
Associated with Subarachnoid Hemorrhage with Special Reference to Their Genesis
WILLIAM J. HAMMER, M.D.’ ALFRED J. LUESSENHOP, ALAN M. WEINTRAUB.
M.D.
M.D.
Washington, D. C.
From the Department of Medicine (Division of Cardiology) and the Department of Surgery (Division of Neurosurgery), Georgetown University School of Medicine, Georgetown University Hospital, Washtngton, D.C. This work was carried out under the tenure of a U.S. Public Health Service training grant fellowship to Dr. Hammer (Grant No. 2 T12 HE-05433) and was funded by the National Institutes of Health, Bethesda, Maryland. Requests for reprints shoukt be addressed to Dr. Alan M. Weintraub. Georgetown University School of Medicine, Georgetown University Medical Center, 3800 Reservoir Road, N.W., Washington, D.C. 20007. Manuscript accepted October 7. 1974. Present address: Department of Medicine, Division of Cardiology, Temple University Health Science Center, Philadelphii, Pennsylvania. l
A 36 year old man presented with bizarre behavior and had abnormal electrocardiograms on two occasions. Because of ST-T wave changes, he was treated both times for a possibie subendocardial infarction. A more complete evaluation during the second admission revealed a basilar artery aneurysm with subarachnoid hemorrhage as the cause of the central nervous system symptoms. While the aneurysm was successfully clipped, the patient’s electrocardiogram was recorded. Several electrocardiographic changes characteristic of intracranial disease were observed during the procedure. These changes developed with distortion of the circle of Willis and reverted when such distortion stopped. We review the spectrum of the electrocardiographic changes associated with intracranial disease. This list of abnormalities was compiled from observations obtained by the impatient tracings of persons with various central nervous system pathology. The mechanisms used to explain the ahanges are based soieiy on work performed on laboratory animals. The results of our findings in our patient link electrocardiqraphic abnormalities directly with a central nervous system lesion. Over the last two decades a variety of electrocardiographic abnormalities have been associated with intracranial disease, especially subarachnoid hemorrhage [ 1- 131. Various theories, principally involving the autonomic nervous system, have been proposed to account for these abnormalities [3,5,9,12,14-241. The basis for these theories is experiments performed only on laboratory animals. These results have been extrapolated to man to explain the various electrocardiographic changes accompanying intracranial disease. We describe a patient who presented with an abnormal electrocardiogram, and in whom a diagnosis of basilar artery aneurysm with subarachnoid hemorrhage was subsequently made. Surgical intervention afforded the opportunity to make serial observations with a full 12 lead electrocardiogram monitor and to link the experimental work with the actual changes in man. The results support the theory that the local effects of the aneurysm are the initiating mechanism for the characteristic electrocardiographic changes accompanying subarachnoid hemorrhage.
September 1975
The American Journal of Medicine
Volume 59
427
ELECTROCARDIOGRAPHIC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
ET AL
-_
._.
3 Figure 7. These tracings show the sequence of electrocardiographic changes that occurred with two separate hospitalirations involving central nervous system symptoms.
CASE REPORT A 36 year old Caucasian man was admitted to the Georgetown University Medical Center on September 6, 1973. His pertinent medical history began on August 6, 1972, when he entered the emergency room of a local hospital with complaints of vague chest pain. At that time he was confused and was disoriented to time and place. The remainder of the physical examination was within normal limits. An electrocardiogram showed normal sinus rhythm with occasional premature ventricular contractions, right axis deviation, slight S-T segment elevation in leads II, Ill and aVF, and poor R wave progression from leads VI to Vs (Figure 1A). Over the next 46 hours the patient’s confusion cleared, and he became asymptomatic. The electrocardiogram continued to show a normal sinus rhythm and right
Figure 2. Carotid arteriogram demonstrates basilar artery aneurysm.
428
September 1975
The American Journal of Medicine
axis deviation; however, the T waves became deeply inverted in leads I, aVL and V2 to Vs (Figure 1B). The premature ventricular contractions had disappeared, and slight S-T segment elevation was present in leads II and aVF. Over the next 12 days the patient remained asymptomatic and the results of his physical examination continued to be within normal limits. Laboratory results, including creatinine phosphokinase, lactate dehydrogenase and transaminase, were all within normal limits. The electrocardiogram, however, did not change. The patient was discharged after 21 days with the diagnosis of anterolateral subendocardial infarction. He subsequently was lost to follow-up for a year. On August 31, 1973, his landlady found him in a delirious and combative state. He was taken by police to the same emergency room as before. The results of the initial physical examination were negative, except for disorientation. An electrocardiogram showed occasional premature ventricular contractions, right axis deviation and poor R wave progression from leads VI to Vs. The previously mentioned T wave inversions were not present (Figure 1C). The patient was admitted for observation. During the ensuing 12 hours he became more stuporous and had nuchal rigidity. A spinal tap yielded grossly bloody fluid. The electrocardiogram had undergone additional changes by 24 hours. There was now marked T wave inversion in leads I, II, aVL and V2 to Vs. A suggestion of S-T segment elevation was again noted in leads II, Ill and aVF. Right axis deviation of the QRS and normal sinus rhythm persisted (Figure 1D). The creatinine phosphokinase level increased to 463 units, 372 units and 265 units (normal 0 to 60 units) on the 3 subsequent days. Because of the possibility of an acute myocardial infarction, no further diagnostic procedures were performed. Six days later, when no evolution of a myocardial process was seen and there was no improvement in the neurologic picture, the patient was transferred to the Georgetown University Medical Center.
Volume 59
ELECTROCARDIOGRAPHIC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
f --
.
-.
.: ,i
‘- __
^_!
‘:y ;_ -
Figure 3. A tracing performed leads I, a VL and V3 to V,.
1
inverted
I
I I i I
after the induction of anesthesia.
On admission the patient was confused, stuporous and had nuchal rigidity. There were no localizing signs. A carotid arteriogram was performed, and a basilar artery aneurysm was demonstrated (Figure 2). On the 4th hospital day the patient underwent craniotomy; general anesthesia with nitrous oxide was administered. At surgery the temporal lobe was retracted and, with the aid of an operating microscope, dissection along the posterior cerebral artery was performed. The basilar artery aneurysm was identified and was projecting into the interpeduncular cistern. Numerous adhesions were stripped away from the vicinity of the lesion. The neck of the aneurysm was successfully clipped with a small Scoville clamp without provoking any bleeding. At this time, traction was applied to the posterior cerebral artery and to the circle of Willis to allow adequate
previously
i I
I
ET AL.
i
Note T wave inversion
in
visualization. The temporal lobe was then allowed to fall back and the dura mater and bone flaps were closed without complications. The temperature was 94’F throughout the procedure. Blood pressure was 90150 mm Hg at the beginning of the procedure and decreased to 75140 mm Hg at the time of temporal lobe retraction. lt remained at this level until the dura mater was closed. The potassium level was 3.8 meq/liter preoperatively and 3.7 meq/liter postoperatively. The sodium, chloride and carbon dioxide combining powers were unchanged postoperatively from the normal values obtained preoperatively. The patient’s immediate postoperative course was uneventful, and his level of consciousness gradually improved. A persistent third nerve deficit was noted on the right side. On the 6th postoperative day, however, there
T waves in leads V3 to V6 are now upright.
September 1975
The American Journal of Medicine
Volume 59
429
ELECTROCARDOGFIAPHIC
CHANGES IN SUBARACHNOlD HEMORRHAGE-HAMMER
ET AL.
tained 2 minutes after the one in Figure 4. The rhythm has become junctional.
was an abrupt decline in the level of consciousness, and a right hemiparesis developed. A repeat angiogram demonstrated diffuse spasm of the left cerebral vessels, but no specific lesion was seen. After several weeks it became apparent that our patient showed no improvement; a global aphasia and right hemiparesis persisted. MATERIALS
AND METHODS
The patient was monitored during the surgical procedure with a Hewlett-Packard three channel recorder and conventional lead placement [25]. Monitoring was begun at the induction of anesthesia and concluded with the termination of the procedure. A full 12 lead tracing was taken every 5 minutes or when major surgical manipulation was announced by the neurosurgeon. Blood pressure was determined every 5 minutes with a sphygmomanometer placed over the right brachial artery. A constant temperature recording was obtained by a rectal thermocouple. Electrolytes were determined pre- and postoperatively by the routine hospital laboratory. RESULTS On admission
to the Georgetown
University Medical
Center, the patient’s electrocardiogram showed normal sinus rhythm with a rate of 62 beats/min. The P-R interval was 0.14 second. There was right axis deviation of the QRS and T wave inversion in leads I, aVL and VJ to Vg. The first full tracing after induction of anesthesia was similar to the tracing obtained on admission and is shown in Figure 3. Shortly after this recording, the electrode in the lead V2 position became detached. The electrocardiograni remained unchanged from the control tracing while the bone flaps were removed, the dura mater was cut, the temporal lobe retracted and the previously described dissec-
430
September
1975
The American Journal ot Medkine
tion performed.
_
With tension applied to the posterior
cerebral artery and with distortion of the circle of Willis, a series of changes occurred in rapid sequence. First, the T waves in leads V3 to Ve became more upright. Then the T wave in lead I became less negative, and the T waves in leads II, Ill and aVF became pronounced. This is shown in Figure 4. Immediately after these T wave changes, the rhythm became junctional as seen in Figure 5. With release of the traction applied to the aforementioned vessels, the electrocardiogram immediately reverted to a pattern similar to the control tracing with sinus rhythm and T wave inversion in leads I, aVL and Vs to V6 (Figure 6). Except for occasional premature ventricular contractions while the dura mater was closed, there were no further changes in the tracings during the remainder of the procedure. COMMENTS During the last two decades many clinicians have observed abnormalities in the electrocardiograms of patients with intracranial disease, especially subarachnoid hemorrhage. The changes that are generally accepted are listed in Table I [3,1 I]. With regard to arrhythmias, Cropp and Manning [4] have reported an increased incidence of premature ventricular contractions, and wandering atrial pacemaker and junctional rhythms. Poole [6] and Gallon et al. [ 1 l] have noted sinus bradycardia and atrioventricular dissociation. A marked increase in the amplitude of the P wave to greater than 2.5 mm has been reported by Hersch [ 61 and Eisalo et al. [ 91. Both S-T segment elevation and depression great-
volume 59
ELECTROCAROlOGRAPHlC CHANGES IN SUBARACHNOID HEMORRHAGE-HAMMER
ET AL.
Figure 6. With release of the tension on the circle of Willis, two changes occurred immediately. The rhythm became sinus in origin, and the T waves in leads V, to V6 were once again inverted. There was also more prominent T wave inversion in leads I and a VL.
er than 1.0 mm have been seen [8,11]. T wave inversion is also apparently a common phenomenon [ l-31. Elevated T waves have been observed in the early phase after a cerebrovascular accident [2325]. Prominent U waves have also been observed [2,3,6]. The Q-T interval is prolonged according to several investigators [4,6,9,24]. Burch et al. [2] questioned this finding and suggested that the prominent U wave may merge with the T waves thereby giving a prolonged Q-U interval mimicking an increased Q-T interval. Abnormalities of the QRS complex per se have not been documented. A patient with an intracranial process may have one or more of these changes, and their incidence tends to increase as the person’s neurologic status deteriorates [ 81. Although there is general agreement that the aforementioned electrocardiographic changes are associated with intracranial disease, there is less consensus as to the cause of the phenomena. Welt et al. [ 191 observed the occurrence of hyponatremia and hypothermia in patients with brain injury. Some investigators have attempted to link these and other metabolic abnormalities, especially hypokalemia, with the electrocardiographic changes but they were unsuccessful [20]. Poole [5] demonstrated, at the time of stimulation of the circle of Willis, a sinus bradycardia in persons undergoing neurosurgical procedures. This change could be induced only if the patient was hypothermic and was under light anesthesia. The investigator postulated that this change in heart rate was secondary to a vagocardiac reflex initiated by local stimulation of the autonomically rich circle of Willis. After this re-
port, other investigators produced some of the characteristic electrocardiographic changes by stimulating various parts of the central nervous system in experimental animals. Kontweig et al. [21] produced nonspecific ST-T wave changes with stimulation of the subcortical areas in dogs. Manning and Cotten [ 171 stimulated the hypothalamus of cats and were able to show ST-T wave abnormalities. Interest then shifted from an emphasis on the local stimulating effects of the intracranial lesion to the work emphasizing the importance of the autonomic nervous system in the genesis of the characteristic electrocardiographic abnormalities. Jacobson and Danufsky [ 161 produced experimental head trauma in dogs and were able to produce some of the charTABLE
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Generally Accepted Electrocardiographic Changes Associated with Intracranial Disease (3, 11,
131
1. Conduction
2.
3. 4. 5. 6. 7. 8. 9.
disturbances a. Shortened P-R interval b. Junctional rhythms c. Atrioventricular dissociation Arrhythmias a. Sinus bradycardia b. Ventricular premature beats c. Atrial premature beats d. Wandering atrial pacemaker Prominent P waves S-T segment elevation S-T segment depression T wave inversion Prominent upright T waves Prominent U waves Prolonged Q-T interval
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acteristic changes in the tracing which could be blocked by the administration of atropine. Barger et al. [ 141 noted that the tall peaked P waves which occurred with the intracranial processes could also be produced by the administration of epinephrine to a normal subject. Shuster [3] was able to reverse the S-T segment depression seen in subarachnoid hemorrhage with the administration of atropine. The S-T segment elevation and T wave changes produced by stimulation of the diencephalon of cats was prevented by high section of the cervical sympathetic chain [22]. Offerhaus and Van Gool [ 151 experimentally induced subarachnoid hemorrhages in rabbits. Premature ventricular contractions and S-T segment elevations were observed, and both were blocked by the administration of propranolol. The aforementioned data certainly seemed to implicate the autonomic nervous system in the development of the electrocardiographic changes. lt was interpreted by some investigators that the primary site of the central nervous system pathology was relatively unimportant, and that almost any intracranial stimulation would result in activation of the autonomic nervous system with the subsequent electrocardiographic changes caused by autonomic discharge
[121.
Several investigators have suggested more elaborate explanations. They believe that the electrocardiographic changes are representative of actual myocardial lesions such as subendocardial hemorrhage and necrosis [26,27]. Such a pathologic process could be caused by an excess of circulating catecholamines produced by a mechanism independent of the primary site of intracerebral disease [lO,ll]. The myriad of information does not clearly lead to one mechanism which could explain the production of the electrocardiographic changes seen in intracranial disease. Burch and Philips’ [23] analysis of the
data concludes that the essential ingredient to cause these changes seems to be a specific intracranial injury which results in an autonomic discharge that is reflected in the electrocardiogram. The observations related to the study of our patient are unique. The characteristic electrocardiographic changes associated with intracranial disease, especially subarachnoid hemorrhage, have been derived from empiric observation [l-l 21. The mechanisms used to explain these changes are derived from experiments with laboratory animals. Our patient provided an opportunity to link an observed change directly to one of these proposed mechanisms. He initially presented with electrocardiographic abnormalities which are commonly associated with subarachnoid hemorrhage. A basilar artery aneurysm and subarachnoid hemorrhage were subsequently demonstrated. With manipulation of the aneurysm and the adjacent vessels resulting in distortion of the circle of Willis, electrocardiographic changes were produced during surgery. These changes occurred almost immediately with the manipulation, and they disappeared in the same manner when the manipulation was discontinued. The electrolytes and the body temperature clearly did not play a role in the genesis of these changes. The amount of anesthesia was not a deciding factor. None of the other intracranial manipulations performed during surgery produced any changes in the electrocardiogram. It is also quite unlikely that actual myocardial damage could have caused changes which would appear and then disappear in the manner described. These observations, therefore, are the first to be noted in man, which clearly support the hypothesis that the local effects of the aneurysm, operating possibly through the autonomic nervous system, are a necessary inciting stimuli for the well known electrocardiographic changes associated with subarachnoid hemorrhage.
REFERENCES 1.
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Levine l-ID: Non-specificity of the electrocardiogram associated with coronary artery disease. Am J Med 15: 344, 1953. Burch GE, Myers R, Abildskov JA: A new electrocardiographic pattern observed in cerebra-vascular accidents. Circulation 9: 719, 1954. Shuster S: The electrocardiiram in subarachnoid hemorrhage. Br Heart J 22: 316, 1960. Cropp 61, Manning GW: Electrocardiographic changes sim ulating myocardiil ischemia and infarction associated with spontaneous subarachnold hemorrhage. Circulation 22: 25, 1960. Poole JL: Vasocardiac effects of the circle of Willis. Arch Neurol Psychiatry 78: 355, 1957. Hersch C: Electrocardiographic changes in head injury. Circulation 23: 853, 1961.
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Schubart AF, Marriott HJL, Gorten RJ: lsorhythmic dissociation. Am J Med 24: 209. 1958. Hersch C: The electrocardiogram in cerebral disease. Br Heart J 26: 785, 1964. Eisalo A, Perasalo J. Halonen PI: Electrocardiographic abnormalitiis and some laboratory findings in patients with subarachnoid hemorrhage. Br Heart J 34: 217, 1972. Umall F, Gould L, Gomprecht RF: The electrocardiographic changes in intracerebral lesions. Angiology 22: 616, 1971. Gallon S, Rees GAD, Briscoe CE. Davies S, Kilpatrick GS: Prospective study of electrocardiographic changes associated with subarachnokl hemorrhages. Br J Anaesth 44: 511.1972. McIntyre JWR, Dobson D, Weir BKA, West R, Overton TR: Monitoring under anesthesia with reference to subarach-
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noid hemorrhage and the T wave as an electrocardiographic manifestation. Can Anaesth Sot J 18: 293, 1971. Surawicz B: Electrocardiographic pattern of cerebrovascular accident. JAMA 197: 913, 1966. Barger AC, Liebowitz MR. Herd JA: Chronic catheterization of the coronary artery. Infusion of autonomic drugs in the unanesthetized dog. Fed Proc 20: 101. 1961. Offerhaus L, Van Go01 J: Electrocardiographic changes and tissue catecholamines in experimental subarachnoid hemorrhage. Cardiovasc Res 3: 433, 1969. Jacobson SA, Danufsky P: Marked electrocardiographic changes produced by experimental head trauma. J Neuropathol Exp Neurol 13: 462. 1954. Manning JW, Cotten M: Mechanism of cardiac arrhythmia induced in diencephalic stimulation. Am J Physiol 203: 1120. 1962. Melville KI, Blum B, Shuster HF, Silver M: Card&c ischemic changes and arrhythmia induced by hypothalmic stimulation. Am J Cardiol 12: 787. 1963. Welt LG. Seldin DW, Nelson WP. German WJ. Peters JP: The role of the central nervous system in metabolism of electrolytes and water. Arch Intern Med 90: 355, 1952. Wasserman F, Bellet S: The electrocardiographic observa-
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tions in patients with cerebrovascular accident. Am J Med Sci 231: 502, 1956. Kontweig B, Bolts CT, Ten Cote J: Influence of stimulation of some subcortical areas on the electrocardiogram. J Neurophysiol20: 100, 1957. Ponta R: Persistent electrocardiographic abnormalities experimentally induced by stimulation of the brain. Am Heart J 69: 815, 1964. Burch GE, Philips JH: The upright T wave as an electrocardiographic manifestation of intracranial disease. South Med J 61: 331, 1988. Tobin JL: Complications of meningococcus infection in a series of sixty-three sporadic cases. Am J Med Sci 231: 241, 1956. Marriott H: Practical Electrocardiography. 5th ed, Baltimore, Williams & Wilkins, 1972. Kreus K, Kremilin SJ. Takala JK: Electrocardiographic changes in cerebrovascular accidents. Acta Med Stand 185: 327, 1969. Koskelo P. Pensan S. Sipila W: Subendocardial hemorrhage and electrocardiographic changes in intracranial bleeding. Br Med J 1: 1479, 1964. Greenhort JH, Runchenback DD: Cardiac injury and subarachnoid hemorrhage. A clinical, pathologic and physiological correlation. J Neurosurg 30: 521. 1969.
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