Abstract
Forensic pathology is not simply autopsy pathology. Rather, the determination of why someone died is dependent upon the findings of a competent autopsy interpreted within the context of an excellent investigation of the circumstances of death. It is important that medical examiners remember the critical distinction between “dying with” and “dying of” something. Furthermore, our determination of “the” cause of death may not explain “why” someone died; identifying the underlying cause of death may not explain the mechanism through which the person died.
Sudden deaths occur under any circumstance, may be natural or violent, may be readily apparent as to cause and manner or subtle as to cause or manner or both. Circumstances may be sedentary or extremely active. Sudden ventricular fibrillation deaths without autopsy demonstrable lesions indicate that we lack techniques of pathology necessary to demonstrate the triggering mechanism in the victim at the time of death. Part of this deficiency of knowledge exists because the majority of fatal heart attacks occur outside the hospital setting and without opportunity to study these patients in the manner afforded patients inside coronary care units. Another problem occurs when pathologists depend upon autopsy data to the exclusion of circumstantial data. After four and one half decades of medico-legal death investigation, commencing with two Native American fire fatalities in the Bear Paw Mountains of the state of Montana in 1952, I have developed some
Sudden death investigative options are dependent upon circumstances as well as autopsy
Circumstantial data is usually more important than autopsy data
What we call the “cause” of death does not answer the question, “Why did the victim die?”
Autopsy findings of disease or injury may or may not be relevant to the cause of death
Autopsy findings are useful to provide a means to classify or code according to the ICD (International Classifications of Diseases) of the World Health Organization but listed items are not the precipitating causes of death even though we say they are.
Sudden Death Investigative Opinions are Dependent upon Circumstances as Well as Autopsy
Almost all death investigations require correlation of circumstantial data with autopsy and laboratory data. Some trauma induced autopsy findings are self evident at autopsy. Relatively few natural death causes are self evident
Circumstantial Data is Usually More Important than Autopsy Data
Only a clear detailed reconstruction of the terminal event may clarify the true case and manner of death. This is especially so when death is associated with diseases which do not have clear autopsy findings, diabetes, epilepsy, spontaneous lethal dysrhythmias, etc. In fact, a case occurred in Florida where the bodies of the murder victims were never recovered, yet the murderers were convicted based upon the totality of the circumstantial evidence.
Prior to the autopsy the forensic pathologist should posses sufficient data to have an accurate concept of the anticipated autopsy findings, data to determine the specific procedures and tests that should be performed and data sufficient to know what cause of death will probably be correct. How is this possible? First, know the circumstances based upon witness statements and the physical evidence at the scene of death. Second, know the past medical history and social status of the victim. Third, know the environment in which the terminal events took place. Given this information, the autopsy serves only to add more data to an already existing diagnostic data base. Environments may be lethal. If the victim were utilizing an electric device at time of collapse or was exposed to fumes from a defective gas heater, the environmental hazard takes precedence over autopsy demonstrated disease which, if one thinks about it, was present before death while life processes were adequate. Some lifestyle subsets carry a high risk of poison, injury or disease which should be early indicators of potential causes of non-cardiac death.
The “very sudden cardiac death syndrome” occurs (1). The victim is up and about and suddenly collapses. A rescue paramedic team notes ventricular fibrillation (VF). A superficial scalp wound occurring during the collapse fails to bleed actively. All this points toward a very sudden onset of a lethal cardiac rhythm. Some scenarios come to mind. One is an elderly lady who collapses to the sidewalk while carrying groceries. No vital signs are present but the initial ECG noted by the paramedic team is ventricular fibrillation. Inquiry reveals that she has had several days of chest discomfort. One should anticipate ischemic heart disease evidence at autopsy with an acute myocardial infarct as a reasonable possibility. The same circumstances but with persistent sinus rhythm on initial ECG is likely to be the result of cardiac tamponade from rupture of an infarct. Why? This person has an electrically stable heart. Even after rupture, the rhythmic electrical pulsations continue for a time. Consider another scenario, that of a 39 year old man standing talking to friends. Suddenly he complains of excruciating chest pain, collapses, is without vital signs and has sinus rhythm on arrival of the rescue team. There is a reasonable likelihood of an acute dissecting aneurysm of the aorta with cardiac tamponade. What do these scenarios teach us? We must seek all available data during our investigation. If rescue paramedics arrive at the scene we should know everything they observed in detail, not generic but specific.
Another scenario may occur. A pathologist calls to seek help because the autopsy did not reveal “an anatomical cause of death”. My rejoinder is to ask the name, age, race, address, marital status, occupation, past medical history, terminal event circumstances and location before addressing autopsy and laboratory procedures. Demographic data plus circumstances are essential to the performance of proper autopsy procedures and final diagnosis.
A remarkable case occurred some years ago. A pathologist telephoned me to inquire about toxicology tests because his gross autopsy failed to reveal an obvious major lesion. He wanted to discuss the autopsy and what toxicology tests should be considered. I interrupted to inquire along the procedure mentioned above. “First tell me her name” I asked. “Paricia Van Staveren” he replied. “Oh”, I replied, “she died of primary pulmonary hypertension”. How did I know that? I knew the family history having performed an autopsy upon her young child who died suddenly and unexpectedly a few years earlier (2).
What We Call the “Cause” of Death Does not Answer the Question, “Why Did the Victim Die?”
Disease states do not appear in an instant. What is found at autopsy was present when the victim was alive. Structural abnormalities present at autopsy may be less advanced or severe than what are present in living people. Most of the time we can not determine the exact pathophysiologic or biochemical process which triggered a lethal cardiac rhythm at a particular state of the disease. We may implicate lesions in the conduction system, acute coronary occlusions, ischemic myocardial changes and so forth but these do not explain the sudden change from life to death at that specific instant because these very same lesions exist in living people.
Through convention we designate the disease classification as a “cause” which is alright providing we do not delude ourselves into thinking that no more potential problems exist. In medico-legal death investigation, again through custom or convention, we accept as “cause” that disease or injury which initiates the lethal train of events however brief or prolonged. Mechanisms of death are those physiological or biochemical events which are incompatible with life and which result from the underlying disease or injury process.
A complication exists based upon terminology. The English word “cause” has different meanings to different people depending upon the context in which it is used. To the clinician the cause of death of the burned child is sepsis and electrolyte imbalance. To the medical examiner completing the death certificate the cause is the burn. To the prosecuting attorney the legal cause is the criminal act of setting the victim afire. The pathologist may be satisfied to arrive at a cause of death by drowning. The more important is to seek answers as to why and how the victim entered the water and could not reach safety (3).
Years ago the National Heart and Lung Institute of the National Institutes of Health funded a multi-center study to address the question of what exactly precipitated sudden death from cardiac disease.
At the University of Miami 426 sudden cardiac deaths of patients with lethal dysrhythmias were the subject of intensive study. Within the City of Miami 80 percent of the advanced life support rescue team response times were within four minutes of notification. VF was the initial rhythm recorded in 306 (72%) of the patients. Other rhythms included idioventricular rhythm in 34, asystole in 33, junctional bradycardia in 28, sinus bradycardia in 10, complete AV block in 9 and ventricular tachycardia in 6. The majority of myocardial changes detected in defibrillated patients who survived involved the anterior wall confirming prior impressions that anterior wall lesions may often precipitate VF and sudden cardiac death too rapidly to allow histologic detection. Eighty patients were successfully defibrillated in the field and studied in the hospital. In only 39% of these patients could an acute myocardial infarct be demonstrated (4). This explains the futility in trying through postmortem techniques to demonstrate “early” myocardial infarction when none is ever going to occur.
Did we succeed in determining the exact precipitating pathophysiologic or biochemical disturbance which caused sudden cardiac death or VF to occur in that patient at that particular time? No.
Autopsy Findings are Useful to Provide a Means to Classify or Code According to the ICD (International Classification of Diseases) of the World Health Organization but Listed Items are not the Precipitating Causes of Death Even Though we Say They Are
Through custom we place upon the death certificate “Myocardial infarct due to coronary thrombosis due to coronary atherosclerosis” as the listed cause of death. That is correct on the basis of current custom. As noted previously, the hidden precipitating cause remains occult due to our inability to make such a determination. Accordingly I have developed a philosophical approach to the investigation of sudden cardiac death:
Circumstances indicate the sudden death to be of cardiac origin.
The autopsy findings serve only to permit classification within the scheme of the ICD.
At autopsy there is almost always no pathological lesion boundary between a lethal and nonlethal cardiac lesion. Whether large or small the anatomic lesion in the heart serves best to permit classification. Why? We observe sudden cardiac death with only one stenosis of a coronary artery and without an accompanying myocardial lesion. We see similar deaths where the myocardium has functioned well years after the onset of severe myocardial fibrosis. There exists a spectrum of observable pathological change from minimal or none at all to advanced severity, all which may result in sudden cardiac death in some victims but not others.
Just because cardiac lesions may be “small” they are not insignificant. We have on indisputable fact, the patient died suddenly under circumstances which indicate probably cardiac death. The autopsy discloses no alternative cause. Whatever abnormality is found within the heart now becomes useful for classification and is listed upon the death certificate. This may be upsetting to the pathologist who thinks in terms of “an anatomical cause of death” or lesions which are “pathognomonic” while working in an academic setting without responsibility to determine the cause and manner of death.
A forensic pathologist medical examiner in the United States is faced with a dead body. The pathologist has the legal responsibility to determine the cause and manner of death. The fact of death is valuable diagnostic information. Something killed the victim! When circumstances indicate a sudden cardiac death, any lesions within the heart become significant, at the very least to classify the cause on the death certificate. If no cardiac lesions may be demonstrated, the death remains cardiac on the basis of circumstances. A death certificate which states as cause “probably ventricular fibrillation” is just as valid as one which list “acute coronary thrombosis”. Either way, the circumstances indicate the cause of death as cardiac. In the Miami study mentioned above, we had two sets of sudden cardiac death patient populations. One group died inside the City of Miami which already had in place a fully equipped and functioning advanced life support paramedic system. Outside the city, the paramedics were available but without the advantage of portable ECG equipment. Careful epidemiologic and autopsy comparisons of the two groups disclosed no discernable differences. What may we infer from this data? With or without the ECG data, the terminal fatal rhythms are the same. There is no legitimate reason for a pathologist to ignore sudden cardiac death circumstantial data and list the cause as “unknown” or “undetermined”.
Case Examples and Discussion
Approximately 60 percent of the medical examiner death cases in Dade County, Florida are natural. Of the natural deaths, about 60 percent are cardiac. Of the cardiac cases, about 90 percent are due to coronary atherosclerosis. The remaining 10 percent constitute a rich source of unusual, little understood or poorly studied variations of cardiac disease. Let us review only a few of our cardiac death investigations to exemplify the principles being discussed.
Sudden Cardiac Death - “Negative Autopsy”
A 15 year old girl participated in a fashion modeling competition when she suddenly collapsed. During ineffectual resuscitation attempts ventricular fibrillation was noted. She had been previously hospitalized for evaluation of epilepsy because of infrequent episode of sudden loss of consciousness related to emotional stress. Neurological study including electroencephalograms had been non-revealing. No one thought to perform an ECG. Hopefully today such a patient would have a thorough cardiac study as a search for cause of unexplained syncope (5).
At autopsy she appeared anatomically normal. Her heart weighed 240 grams and was grossly and microscopically (Hematoxylin and eosin stains) normal. This case was chosen for discussion because it occurred in September, 1961 and was amongst the first such similar cases noted since the creation of the Dade County Medical Examiner Department in 1956. Cases as these clearly indicate the need for careful evaluation of circumstances and the need to acquire all past medical records as well as detailed accounts from all witnesses. Additionally, lack of pulmonary edema helps one to infer sudden cessation of cardiac function otherwise pumping of blood into oxygen deficient lungs following respiratory cessation would result in escape of fluid and protein into alveolar spaces. With respiratory failure mechanisms of death, the heart my continue to pump and cause pulmonary edema.
One problem with autopsy indicators of sequential shut down of life systems is cardiopulmonary resuscitation artifact. It is essential in all autopsy work to differentiate therapeutic artifacts from underlying disease or injury.
A favorite explanation found in older forensic tests is death by inhibition, cardiac standstill due to vagal inhibition. This notion arose in the days before rescue paramedic systems documented agonal rhythms. Today, ventricular fibrillation rather than cardiac standstill is more likely. Unfortunately the authors of textbooks of forensic pathology tend not to pay attention to current medical advances.
A number of clinical conditions are known to be associated with VF in the absence of anatomical lesions, prolonged QT syndrome and so forth. I choose not to put these upon a death certificate unless I can acquire prior clinical records to substantiate such a diagnosis. Today, with a better cardiac study protocol and improved staining techniques, I may have listed the cause of death of the fifteen year old girl in the fashion show as “myxoid heart disease”.
Mitral Valve Prolapse - An Anatomical Signpost of Fatal Dysrhythmia
A 47 year old tourist suddenly collapsed while sitting on his hotel bed. VF was noted by the rescue team upon arrival. No prior medical records could be located. The heart weighed 430 grams (body weight 97 kilograms). The only abnormality was mitral valve prolapse with thickened chorda tendinae, a redundant hooded posterior cusp and myxoid degeneration of the valve.
The relatively few people with mitral valve prolapse who die, do so suddenly and are apt to come to the attention of the forensic pathologist. The valve is usually competent and not anatomically different than it was before sudden death ensued associated with VF. Over recent years these cases have been studied intensively in our department. We note the following. The circumstances are those of the very sudden cardiac death syndrome. One or more valves, mitral and tricuspid most common, are involved with occasional friction fibrosis of the contiguous endocardium present depending upon the degree of redundancy of the mitral valve. Microscopically the valve has increased myxoid tissue readily apparent by the H & E stain. With better study, more detailed and with proper colloidal iron staining, increased myxoid tissue is seen in the nerves and conduction system of the heart. In some of these hearts when preserved in formaldehyde, the acid mucopolysaccharides (AMP) are in such amount as to commence dissolution. The formaldehyde preserved organ may feel slimy when picked up in the rubber gloved hand.
Correlation of the degree of nerve and conduction involvement with sudden cardiac death as compared with mitral valve prolapse incidental to death from injury, reveals more nerve and conduction system involvement in the sudden cardiac death cases (6). Fatal mitral valve prolapse cases are not valvular but are functional with autonomic nervous system involvement. In one case, in which I had occasion to examine the patient when he was alive at age 14 years, the vagus nerves were similarly involved with AMP as were the cardiac nerves when the lad dropped dead at age seventeen while playing basketball. The vagus nerve deposits were sufficient to be seen on the colloidal iron stained glass microscopic slides with the unaided eye. Try to find this constellation in the published cardiology literature! He was not a Marfan syndrome but did have increased AMP involvement of the root of the aorta as well as some minimal involvement of the mitral valve. These types of cases we certify as “myxoid heart disease” as a reflection of the extra-valvular distribution of AMP. Biochemical studies in our university likewise indicates increased amounts of AMP in myocardium connective tissue in such sudden death cases.
Functional studies of symptomatic mitral valve prolapse patients compared with asymptomatic patients clearly indicates autonomic nervous system imbalance, increased vasoconstrictor activity, decreased vagal tone and higher heart rates in the symptomatic patients (7–8). To my knowledge, no one has yet published AMP autopsy data upon patients who have been studied utilizing the techniques of Gaffney and associates. Cardiac nerve involvement by AMP might have played a role in the clinical observations of Gaffney. His patients were alive. Whether any deaths occurred subsequently in his study group is unknown. But it is fair to say that, if autopsied, no one thought to study the cardiac nerves and conduction system utilizing the colloidal iron staining technique.
Minimal aberrant coronary distribution - a lesson in dominance
A 27 year old black basketball player suddenly collapsed. He was in ventricular fibrillation when the rescue paramedics arrived. One month previous his recorded blood pressure was 142/80. Body weight was 73 kilograms and the heart weight was 465 grams. The right coronary artery was small in diameter and too short to reach the acute margin of the heart. The left circumflex did not form a posterior descending branch. The anterior descending artery consisted of small branches which passed over the apex to the inferior wall, mainly the right ventricle. In the posterior central apex region, at the junction of the interventricular septum and the posterior (inferior) wall was a 1.5 centimeter zone of fibrosis of the subendocardial and midwall region. Note that this area of the heart may posses variations of myocardial bundles as normal but not with the degree of confluent fibrosis noted in this case.
Myocardium needs an adequate flow of oxygenated blood in order to remain functional and intact. The initial examination of the epicardial arteries in terms of size and distribution enables one to estimate which area of myocardium is most apt to be deficient in blood flow. In this case that technique permitted me to anticipate the point of least blood flow and to quickly find the area of fibrosis. Postmortem angiography may be better but is not feasible when five or ten other autopsies need to be performed on the same day by the busy forensic pathologist. The lesson is that no “routine” dissection method is applicable to the heart. One must be thinking of the circumstances of death and commence with a general inspection of the heart which includes the estimate of epicardial blood flow past points of narrowing. It is essential to describe the epicardial distribution and not use the term “dominant”. Giorgio Baroldi and Guiseppe Scomazzoni pointed this out in their book on the coronary circulation three decades ago (9). The reason is because some researchers used angiography and others use gross dissection to determine “dominance”. Another good reason is that an autopsy description should be objective in order to paint a word picture of what was seen through the eyes of the pathologist.
Ventricular Fibrillation - Blow to Chest.
A previously healthy 19 year old baseball player ran to catch a fly ball and collided with another player. He collapsed and was taken to a nearby hospital by the rescue paramedic team but could not be successfully resuscitated. This was the police history furnished to me. He was 170 centimeters in height, weighed 66 kilograms and had a heart weight of 310 grams. No evidence existed of blunt injury to skin, ribs, pleura, pericardium or heart. Brown macrophages within pulmonary alveoli plus a carbon monoxide of 5.9% hemoglobin saturation was consistent with cigarette smoking. An incidental finding was sickle cell trait.
As with almost all sudden deaths, the initial police derived information was useful but not adequate. Accordingly I contacted the other player and determined that the point of contact was his elbow to the precordium of the victim. After impact the victim walked about five meters and collapsed. The witness thought the victim was play acting but became quickly convinced that something was wrong. The rescue paramedics were called while the players commenced mouth to mouth resuscitation. I telephoned the rescue lieutenant and learned that the initial rhythm was VF. Within ten minutes of the initial collapse he was admitted to a hospital where 30 more minutes of resuscitation efforts were of no use.
A blow to the precordium can result in very sudden cardiac death. The Consumer Products Safety Commission of the United States Government has recently published an account of over a dozen youths who died from being struck in the front of the chest by a thrown baseball. That is why the catcher should wear a padded vest. The method of induction of VF is unclear but it is not coronary spasm. The collapse is too fast for an induced ischemia from coronary spasm to explain the event. We know that physical stimulation of reactive muscle, including myocardium, will induce contraction. The physical force transmitted to the heart from the blow to the chest is similar.
The real lesson in this case is that the forensic pathologist must personally contact the key witnesses and determine exactly what happened rather than remain a passive recipient of information from other investigators.
Discussion
The forensic pathologist has a unique opportunity to study very sudden cardiac deaths which result from all types of cardiac disease. Sarcoid, myocarditis, numerous types of myocardiopathies including fibrofatty dysplasia, and congenial aberrations may be found. Some very sudden cardiac deaths may lead to controversy. A cardiac cripple may die suddenly when confronted with an armed robber. In this circumstance the assailant may be charged with murder (10). The victim may be “high profile” such as Elvis Presley whose last moments were reading a book while sitting on the commode. An enlarged heart and narrowed coronary arteries associated with well documented hypertension, coupled with the terminal circumstances, indicate without doubt that the drugs also present were only incidental and did not contribute significantly to the terminal event. A drowning may be the result of cardiac syncope proven only by a careful study of circumstances (3). The same applies to automobile fatal injury when loss of control was sudden incapacitation of the driver from natural disease. We studied 1,171 driver fatalities over a twelve year period. About six percent of fatal automobile crashes where the driver who lost control died with massive injuries were the result of sudden incapacitation by natural disease, two thirds cardiovascular and one third epilepsy (11). Conversely the demonstration of heart disease in a dead driver may not be relevant to the death. A careful study of the circumstances is the only way to determine relevancy of autopsy demonstrated disease when death is associated with physical injury.
Summation
The circumstances of death will indicate whether or not a case of the very sudden cardiac death syndrome occurred. Once it is apparent that the death is cardiac in origin, usually VF, the anatomical abnormality disclosed at autopsy becomes useful for classification for death certification purposes. The forensic pathologist must play the part of a clinician and actively seek diagnostic information rather than to sit passive and rely only upon fragmentary information plus the autopsy findings. Autopsy findings of cardiac disease may or may not be relevant to the cause of death. And finally, the autopsy does not indicate why the heart chose to change from a viable rhythm to a lethal rhythm. Circumstances may better assist but often the precise reason is elusive in the light of our present knowledge of sudden cardiac death.