'Voodoo' Death Revisited: the Modern Lessons of Neurocardiology†

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'Voodoo' Death Revisited: the Modern Lessons of Neurocardiology† KEYNOTE ADDRESS MARTIN A. SAMUELS, MD, DSc (hon), FAAN, MACP* Neurologist-in-Chief and Chairman Department of Neurology Brigham and Women’s Hospital Professor of Neurology Harvard Medical School Boston, MA ‘Voodoo’ death revisited: The modern lessons of neurocardiology† n 1942, Walter Bradford Cannon published a personal danger or threat of injury; (7) after danger is remarkable paper entitled “‘Voodoo’ Death,”1 in over; and (8) reunion, triumph, or happy ending. which he recounted anecdotal experiences, largely Common to all is that they involve events impossible I from the anthropology literature, of death from for the victim to ignore and to which the response is fright. These events, drawn from widely disparate parts overwhelming excitation, giving up, or both. of the world, had several features in common. They were In 1957, Carl Richter reported on a series of experi- all induced by an absolute belief that an external force, ments aimed at elucidating the mechanism of such as a wizard or medicine man, could, at will, cause Cannon’s “voodoo” death.3 Richter studied the length demise and that the victim himself had no power to alter of time domesticated rats could swim at various water this course. This perceived lack of control over a power- temperatures and found that at a water temperature of ful external force is the sine qua non for all the cases 93º these rats could swim for 60 to 80 minutes. recounted by Cannon, who postulated that death was However, if the animal’s whiskers were trimmed, it caused “by a lasting and intense action of the sym- would invariably drown within a few minutes. When pathico-adrenal system.” Cannon believed that this carrying out similar experiments with fierce, wild rats, phenomenon was limited to soct, that they feel them- Richter noted that a number of factors contributed to selves bewildered strangers in a hostile world. Instead of the tendency for sudden death, the most important of knowledge, they have fertile and unrestricted imagina- which were the restraint involved in holding the ani- tions which fill their environment with all manner of evil mals and confinement in the glass swimming jar with spirits capable of affecting their lives disastrously.” no chance of escape. Trimming the rats’ whiskers, Over the years since Cannon’s observations, evi- which destroys possibly their most important proprio- dence has accumulated to support his concept that ceptive mechanism, contributed to the tendency for “voodoo” death is, in fact, a real phenomenon, but far early demise. In the case of the calm domesticated ani- from being limited to ancient peoples, may be a basic mals in which restraint and confinement were appar- biologic principle that provides an important clue to ently not significant stressors, shaving the whiskers understanding the phenomenon of sudden death in rendered these animals as fearful as wild rats with a cor- modern society as well as providing a window into the responding tendency for sudden death. Electro- world of neurovisceral disease. George Engel collect- cardiograms taken during the process showed a brady- ed 160 accounts from the lay press of sudden death cardia developing prior to death, and adrenalectomy that were attributed to disruptive life events.2 He did not protect the animals. Furthermore, atropine pro- found that such events could be divided into eight tected some of the animals and cholinergic drugs led to categories: (1) the impact of the collapse or death of an even more rapid demise. All this was taken as evi- a close person; (2) during acute grief; (3) on threat of dence that overactivity of the sympathetic nervous sys- loss of a close person; (4) during mourning or on an tem was not the cause of the death but rather that anniversary; (5) on loss of status or self-esteem; (6) death was caused by increased vagal tone. We now know that the apparently opposite conclu- sions of Cannon and Richter are not mutually exclu- * Dr. Samuels reported that he has no financial relationships that pose a sive but rather that a generalized autonomic storm, potential conflict of interest with this article. occurring as a result of a life-threatening stressor, will † This article is adapted from “Introduction to Neurocardiology” by Martin A. have both sympathetic and parasympathetic effects. Samuels, chapter 43 in: Mathias CJ, Bannister R, eds. Autonomic Failure: A Textbook of Clinical Disorders of the Autonomic Nervous System, 4th ed; The apparent predominance of one over the other 1999:421–427, by permission of Oxford University Press (www.oup.co.uk). depends on the parameter measured (eg, heart rate, S8 CLEVELAND CLINIC JOURNAL OF MEDICINE VOLUME 74 • SUPPLEMENT 1 FEBRUARY 2007 Downloaded from www.ccjm.org on September 27, 2021. For personal use only. All other uses require permission. SAMUELS blood pressure) and the timing of the observations in be normal, but the details of the pathological examina- relation to the stressor (eg, early events tend to be tion are not revealed. The point is made that ECG dominated by sympathetic effects, whereas late events changes seen in the context of neurologic disease do not tend to be dominated by parasympathetic effects). represent ischemic heart disease but are merely a mani- In human beings, one of the easily accessible win- festation of autonomic dysregulation, possibly emanat- dows into autonomic activity is the electrocardiogram ing from a lesion affecting the cortical representation of (ECG). Edwin Byer and colleagues reported six the autonomic nervous system. The authors argued that patients whose ECGs showed large upright T waves Brodmann area 13 on the orbital surface of the frontal and long QT intervals.4 Two of these patients had lobe and area 24 on the anterior cingulate gyrus were hypertensive encephalopathy, one had a brainstem the cortical centers for cardiovascular control. stroke with neurogenic pulmonary edema, one had an In contrast to this rather inconclusive clinical data, intracerebral hemorrhage, one had a postpartum there is clear evidence that cardiac lesions can be pro- ischemic stroke possibly related to toxemia, and one duced as the result of nervous system disease. The had no history except a blood pressure of 210/110 mm concept of visceral organ dysfunction occurring as a Hg. Based on experimental results of cooling or result of neurologic stimuli can be traced to Pavlov, warming the endocardial surface of the dog’s left ven- who may have introduced the concept of a neurogenic tricle, Byer et al concluded that these ECG changes dystrophy. Selye, a student of Pavlov, described an were due to subendocardial ischemia. electrolyte–steroid cardiopathy with necroses, referred Levine reported on several disorders other than to as ESCN.8 His view was that this cardiac lesion was ischemic heart disease that could produce ECG common and often described using different names in changes reminiscent of coronary disease.5 Among the the world’s literature. He argued that this lesion was reported cases was that of a 69-year-old woman who distinct from the coagulation necrosis that occurred as was admitted and remained in coma. Her admission a result of ischemic disease, but could exist in the same ECG showed deeply inverted T waves in the anterior heart. Selye felt that certain steroids and other hor- and lateral precordial leads. An ECG 2 days later mones created a predisposition for the development of showed ST-segment elevation with less deeply inverted ESCN, but that other factors were required for ESCN T waves, a pattern suggestive of myocardial infarction. to develop. The most effective conditioning steroid However, at autopsy a ruptured berry aneurysm was was 2-alpha-methyl-9-alpha-chlorocortisol. Among found and no evidence of myocardial infarction or the factors that led to ESCN in steroid-sensitized ani- pericarditis was noted. Levine did not propose a spe- mals were certain electrolytes (eg, NaH2PO4), various cific mechanism but referred to experimental work on hormones (eg, vasopressin, adrenaline, insulin, thy- the production of cardiac arrhythmias by basal ganglia roxine), certain vitamins (eg, dihydrotachysterol), stimulation and ST and T-wave changes induced by cardiac glycosides, surgical interventions (eg, cardiac injecting caffeine into the cerebral ventricle. reperfusion after ischemia), and psychic or nervous Burch et al reported on 17 patients who were said stimuli (eg, restraint, fright). The cardiac lesions could to have “cerebrovascular accidents” (ie, strokes).6 In not be prevented with adrenalectomy, suggesting that 14 of the 17, hemorrhage was demonstrated by lum- the process, if related to autonomic hyperactivity, bar puncture. It is not possible to determine which of must exert its influence by direct neural connection to these patients had hemorrhagic infarction, intracere- the heart rather than by a blood-borne route. bral hemorrhage, and subarachnoid hemorrhage, and Cardiac lesions may be produced in rats by pre- no data about the territory of the strokes are available. treating with either 2-alpha-methyl-9-alpha-fluorohy- The essential features of the ECG abnormalities were: drocortisone (fluorocortisol), dihydrotachysterol (cal- (1) Long QT intervals in all patients ciferol), or thyroxine and then restraining the animals (2) Large, usually inverted, T waves in all patients on a board for 15 hours or by using cold stress.9 Agents (3) U waves in 11 of the 17 patients. that act by inhibition of the catecholamine-mobilizing Cropp and Manning reported on the details of the reflex arc at the hypothalamic level (eg, chlorpro- ECG abnormalities in 29 patients with subarachnoid mazine) or by blockade of only the circulating, but not hemorrhage.7 Twenty-two of these patients survived. the neurogenic, intramyocardial catecholamines (eg, Two of those who died had no postmortem examina- dibenamine) were the least effective in protecting car- tion, leaving five in whom autopsies confirmed the diac muscle, whereas those drugs that act by ganglionic presence of a ruptured cerebral aneurysm.
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