I. CRITERIA FOR DEATH

Before the middle of the twentieth century there was no major dispute about the criteria for death. In the nineteenth century several isolated cases of premature burial from around the world raised some alarm, and safeguards (e.g., coffins equipped with alarms) were established to minimize the possibility of that practice. However, concern about the accuracy of diagnosing death largely abated by the turn of the twentieth century.

Beginning with the advent of more effective artificial respirators in the 1940s, major technological breakthroughs in modern medicine raised serious questions about the traditional ways of diagnosing death. Before the widespread use of respirators, defibrillators, intensive-care units, and cardiopulmonary resuscitation failures of cardiac, respiratory, and neurological functions were closely linked. When one system failed, the other two inevitably failed as well. However, respirators and other advanced life-support systems can sustain cardiac, respiratory, and other autonomic functions for prolonged periods even after neurological functions have ceased.

Terminology

With the advent of those new technologies neurological specialists became aware of certain new neurological syndromes, to which an array of confusing and inconsistent terms were applied.

Several landmark medical events stand out in the early days of the new neurologic syndromes. In 1959 the French first described the syndrome of brain death (coma dépassé) (Mollaret and Coulon), in 1968 a special committee of the Harvard Medical School formulated specific neurological criteria to diagnose brain death ("Definition of Irreversible Coma"), and in 1972 Bryan Jennett of Scotland and Fred Plum of the United States first used the term persistent vegetative state, or PVS (Jennett and Plum).

A variety of terms have been used to describe the medical syndrome of brain death: cerebral death, coma dépassé, and irreversible coma. Terms used as imprecise equivalents for the persistent vegetative state have included apallic state, neocortical death, irreversible coma, and permanent unconsciousness It also became necessary to distinguish the new neurological syndromes from common and well-accepted neurological conditions such as coma and dementia. Many newer terms, for example, persistent vegetative state, were used solely to describe the clinical condition. Others, such as the apallic state and neocortical death, were used in an attempt to correlate the loss of neurological functions with the underlying pathological changes in the brain.

As of 1994 there were two different legal/philosophical positions about what it means to be dead in terms of brain functions. Proponents of the whole-brain-oriented position consider a person dead if there is an irreversible loss of all the functions of the entire brain (brain death). Under the other position, which is not law in any jurisdiction in 2003, a person will be pronounced dead when there is an irreversible loss of higher brain functions (permanent unconsciousness).

Dilemmas surrounding these new syndromes, such as when it is appropriate to stop treatment and when death has occurred, have raised fundamental questions about the meaning of medical concepts such as consciousness, awareness, self-awareness, voluntary interactions with the environment, purposeful movement, pain, and psychological and physical suffering.

Neurological specialists are achieving a much greater understanding of these syndromes and their similarities and differences and are reaching a degree of consensus on terminology. However, they have not reached universal agreement on several major issues related primarily to the persistent vegetative state. A historical example illustrates how difficult it can be to reach consensus on terminology. The Harvard Committee ("Definition of Irreversible Coma,") equated irreversible coma with brain death, as did many neurological specialists in the 1970s. Others, equally knowledgeable and experienced, equated irreversible coma with the persistent vegetative state. Still others used the term in a much broader fashion to denote any form of permanent unconsciousness. Because this term has gathered so many different and contradictory meanings, the only reasonable alternative for neurological specialists was to drop it entirely.

Traditional Criteria

With all the controversy surrounding neurological criteria for death, the traditional criteria related to heartbeat and breathing have remained largely unchanged and undisputed except in the University of Pittsburgh Medical Center's program in which organs are taken from certain patients as soon as possible after expected cardiopulmonary death (Lynn). No major legal or ethical concerns have been raised about the traditional criteria for death. Medical organizations around the world have not felt it necessary to establish specific clinical criteria for the diagnosis of death that are based on the irreversible loss of cardiac and respiratory functions. The medical consultants to the President's Commission for the Study of Ethical Problems in Medicine and Biomedical and Behavioral Research recommended that the clinical examination disclose at least the absence of consciousness, heartbeat, and respiratory effort and that irreversibility be established by persistent loss of these functions for an appropriate period of observation and trial of therapy ("Guidelines for the Determination of Death"). However, these consultants recommended no specific length of time for this period of observation.

Brain Death

The neurological syndrome of brain death has been accepted by the medical profession as a distinct clinical entity that experienced clinicians can diagnose with an extremely high degree of certainty and usually can distinguish easily from other neurological syndromes. Brain death is defined as the irreversible cessation of all the functions of the entire brain, including the brainstem. If the brain can be viewed simplistically as consisting of two parts—the cerebral hemispheres (higher centers) and the brainstem (lower centers)—brain death is defined as the destruction of the entire brain, both the cerebral hemispheres and the brainstem. In contrast, in the permanent vegetative state the cerebral hemispheres are damaged extensively and permanently but the brainstem is relatively intact (Cranford, 1988).

An understanding of the pathological sequence of events that leads to brain death is essential if one is to appreciate fully why brain death is a unique syndrome and why it can be differentiated readily from other neurological syndromes with a high degree of certainty. Although a variety of insults can cause the brain to die, head trauma, cardiorespiratory failure, and intracerebral hemorrhage are the most common causes. Regardless of the underlying cause, the pathological sequence is essentially the same in almost all cases. The acute massive insult to the brain causes brain swelling (cerebral edema). Because the brain is contained in an enclosed cavity, brain swelling gives rise to a massive increase in intracranial pressure. In brain death the increased intracranial pressure becomes so great that it exceeds the systolic blood pressure, thus causing a loss of blood flow to both the cerebral hemispheres and the brainstem. Whatever the primary cause of brain death, this end result of loss of blood flow results in the destruction of the entire brain. This sequence of events usually occurs within a matter of hours after the primary event, and so brain death can be diagnosed within a short period of time with an extraordinarily high degree of certainty.

The loss of both cerebral hemisphere and brainstem functions is usually clearly evident to an experienced clinician from the clinical bedside examination. The patient is in a coma, the deepest possible coma, a sleeplike state associated with a loss of all brainstem functions, such as pupillary reaction to light; gag, swallowing, and cough reflexes; eye movements in response to passive head turning (the oculocephalic response) and in response to cold caloric stimulation (oculovestibular response); and spontaneous respiratory efforts.

However, whereas respirations are completely dependent on the functioning of the brainstem, cardiac function can continue independent of brain destruction because the heart has an independent mechanism for spontaneously firing (semiautonomous functioning). With modern life-support systems continued cardiac and blood pressure functions can persist for hours, days, or even longer. Extremely rare cases of continued cardiovascular functions for over a year in the presence of the loss of all brain functions have been reported. The first cases of prolonged somatic survival in brain death usually occurred in the context of brain-dead pregnant women who were maintained on life-support systems for several months so that a viable fetus could be delivered (Wijdicks). However, the most extraordinary case of prolonged somatic survival of a patient with well-documented brain death involved a young adult age twenty-two who for eighteen years has been without any brain functions (Shewmon, 1998; Cranford, 1998; Shewmon, 2000).

In the 1970s and 1980s numerous medical organizations in the United States and around the world developed specific medical criteria for the diagnosis of brain death (Bernat). In the United States major criteria were published by Harvard University, the University of Minnesota, the National Institutes of Health, Cornell University, and the President's Commission. Major international criteria emerged from Sweden, Japan, the United Kingdom, and Canada. All those standards essentially agreed on three clinical findings: coma, apnea (loss of spontaneous respirations), and absence of brainstem reflexes.

The critical issue distinguishing these international criteria was not the clinical findings but how best to establish irreversibility. The United Kingdom, deemphasizing the use of laboratory studies such as electroencephalography, focused on the basic diagnosis as clinical and asserted that the best way to establish irreversibility was to preclude any reversible processes before making a final determination of brain death (Conference of Royal Colleges). Reversible processes that could mimic brain death include a variety of sedative medications and hypothermia (low body temperature, below 32.2° Centigrade). The British also recommended a period of observation of at least twelve hours. In contrast, the Swedish criteria focused less on the period of observation and more on the need for definitive laboratory studies to document a loss of blood flow to the brain, such as intracranial angiography.

In the United States the earlier standards emphasized the use of electroencephalography to establish electrocerebral silence (a loss of all electrical activity of the brain); more recent standards focused on establishing a loss of intracranial circulation by means of radioisotope angiography. The 1981 report of the medical consultants to the President's Commission, which became the definitive medical standard in the United States, recommended a period of observation of at least six hours combined with a confirmatory study, such as tests measuring intracranial circulation ("Guidelines for the Determination of Death"). If no confirmatory laboratory studies were performed, an observation period of at least twelve hours was suggested, assuming that all reversible causes of loss of brain functions had been excluded. In cases of damage to the brain caused by the lack of blood or oxygen (hypoxic-ischemic encephalopathy) the consultants recommended an observation period of at least twenty-four hours if confirmatory studies were not performed.

The diagnosis of brain death in newborns, infants, and children is often more difficult than is the diagnosis in adults. A major reason for this difficulty is that the usual pathological sequence of events in adults that leads to increased intracranial pressure and loss of all blood flow to the brain does not apply to newborns and infants because the cranial cavity in those patients has not yet closed completely. Thus, the mechanism for brain death in newborns and infants may be different from what it is in older children and adults.

To address this question a task force for the determination of brain death in children representing several neurological and pediatric specialty organizations in the United States developed specific diagnostic criteria for the younger age groups (Task Force for the Determination of Brain Death in Children). That task force stated that it would be extremely difficult to establish brain death in newborns less than seven days old. It recommended that in infants seven days to two months of age there should be two separate clinical examinations and two electroencephalograms separated by at least forty-eight hours; for infants two months to one year of age, two clinical examinations and two electroencephalograms separated by at least twenty-four hours; and for children over one year of age, criteria similar to those established for adults.

Beginning in the early 1990s, the University of Pittsburgh and a few other large transplants centers developed protocols for removing organs from patients whose hearts had stopped beating but who were not brain-dead (nonheartbeating organ donors, or NHBOD) (DeVita et al.). In cases of brain death and organ donation the patient is first pronounced dead after the medical diagnosis of brain death has been established, including a period of time to establish irreversibility. The patient then is transferred to the operating room for organ removal while life-support systems are continued. After the transplantable organs are removed, life-support systems are discontinued, but the cessation of heartbeat at this time has no clinical or legal significance. In cases of non-heartbeating organ donors, patients who are terminally ill or have sustained severe irreversible brain damage and are ventilator-dependent are transferred to the operating room, where the respirator is removed, with the resultant loss of heartbeat, usually within minutes. After two minutes of pulselessness, apnea, and unresponsiveness the patient is pronounced dead on the basis of cardiorespiratory criteria. Organ removal then occurs as expeditiously as possible before the organs incur ischemic damage from lack of perfusion. The entire process is carried out in the most humane and caring way possible, including full disclosure to the appropriate surrogate decision makers and the obtaining of their consent (Ethics Committee, American College of Critical Care Medicine). The success and limitations of this controversial procedure have been reported by some of the pioneering transplant centers.

Permanent Unconsciousness

The syndromes of permanent unconsciousness include two major types. The first is a permanent coma: an eyes-closed, sleeplike form of unarousable unconsciousness. The second is the permanent vegetative state: an eyes-open, wakeful form of unconsciousness (U.S. President's Commission for the Study of Ethical Problems). This entry takes no position on the ethical and legal issues involved in choosing between the whole-brain and higher-brain formulations of death but describes the neurological syndromes of permanent unconsciousness that would be considered the medical basis for the higher-brain formulation of death.

A permanent coma is an uncommon neurological syndrome because most patients with damage sufficient to cause brainstem impairment resulting in permanent coma die soon either naturally or because a decision is made to discontinue treatment as a result of the poor prognosis. Cases of prolonged (more than a few weeks) permanent coma do occur but are extremely uncommon.

The vegetative state has three major classes, depending on the temporal profile of the onset and the progression of the brain damage. The first form is the acute vegetative state. This occurs when the onset of brain damage is sudden and severe, such as with head trauma (traumatic vegetative state) or loss of blood flow to the brain caused by sudden cardiorespiratory insufficiencies (hypoxic-ischemic vegetative state). The second form is the degenerative, or metabolic, vegetative state, in which the brain damage begins gradually and progresses slowly over a period of months to years. In adults the most common form of the degenerative vegetative state is the final stage of Alzheimer's disease, whereas in children it is the final stage of a variety of degenerative and metabolic diseases of childhood. The third form is the congenital vegetative state secondary to a variety of severe congenital malformations of the brain that are present at birth, such as anencephaly.

The vegetative state is considered persistent when it is present longer than one month in the acute form and permanent when the condition becomes irreversible. The exact prevalence is unknown, but it is estimated that in the United States there are approximately 10,000 to 25,000 adults and 4,000 to 10,000 children in a vegetative state (Multi-Society Task Force on PVS). When it becomes permanent, this syndrome is the major neurological condition that is the prototype for the higher-brain formulation of death.

Vegetative State

The vegetative state is characterized by the loss of all higher brain functions, with relative sparing of brainstem functions. Because brainstem functions are still present, the arousal mechanisms contained in the brainstem are relatively intact and the patient therefore is not in a coma. The patient has sleep/wake cycles but at no time manifests any signs of consciousness, awareness, voluntary interaction with the environment, or purposeful movements. Thus, the patient can be awake but is always unaware: a mindless wakefulness.

Unlike brain death, in which the pathology and sequence of changes are relatively uniform regardless of the primary cause of the brain damage, the pathological changes in the vegetative state vary substantially with the cause of the unconsciousness. Although there are a variety of causes, the two most common causes of the acute form are head trauma and hypoxic-ischemic encephalopathy. In head trauma the major damage is due to shearing injuries to the subcortical white matter (the fiber tracts that connect the cell bodies of the cerebral cortex with the rest of the brain) of the cerebral hemispheres. With hypoxic-ischemic encephalopathy the primary damage is to the neurons in the cerebral cortex. These different patterns of brain damage are important for several reasons, among them the fact that the chances for recovery of neurological functions and the time necessary to establish irreversibility vary with the underlying cause.

For patients, both adults and children, in a hypoxicischemic vegetative state that lasts longer than three months the prognosis for recovery is uniformly dismal. The vast majority who recover and do well after a hypoxic-ischemic insult to the brain are those who have regained consciousness in the first three months. Among adults in a traumatic vegetative state the majority who do well usually will have regained consciousness within six months of the injury. The prognosis for the recovery of children in a traumatic vegetative state is slightly more favorable than that for adults (Council on Scientific Affairs and Council on Ethical and Judicial Affairs). However, in both children and adults a period of observation of at least twelve months may be appropriate before permanency is established (Multi-Society Task Force on PVS).

Although specific medical criteria for brain death have been established by numerous organizations around the world, no comparable criteria have been established for the diagnosis of the vegetative state. It is unlikely that any criteria as specific as those for brain death will be formulated in the near future because the diagnosis of the vegetative state is not nearly as precise and definitive. The determination of irreversibility in brain death usually takes hours and does not vary according to etiology, whereas it may take months to establish irreversibility in patients who are in the permanent vegetative state, and the time necessary to establish this irreversibility varies substantially with cause and age (Institute of Medical Ethics Working Party on the Ethics of Prolonging Life and Assisting Death).

Because all vegetative state patients are unconscious, they are unable to experience suffering of any kind, psychological or physical. These patients normally manifest periods of eyes opening and closing with accompanying sleep/wake cycles. They also may demonstrate a variety of facial expressions and eye movements that originate from the lower centers of the brain and do not indicate consciousness. They may appear at times to smile and grimace, but observation over prolonged periods reveals no evidence either of voluntary interaction with the environment or of self-awareness (Executive Board, American Academy of Neurology). Neuroimaging studies such as computerized axial tomography (CAT) and magnetic resonance imaging (MRI) may be helpful in establishing the severity and irreversibility of the brain damage. After several months in a vegetative state the brain begins to show progressive shrinkage (atrophy), primarily of the cerebral hemispheres. The loss of consciousness and the inability to experience suffering, which are established on the basis of clinical observations, have been supported by measuring the metabolism of glucose and oxygen at the level of the cerebral cortex by means of positron emission tomography (PET) scanning. These studies have shown a 50 to 60 percent decrease in cerebral cortical metabolism, a level consistent with unconsciousness and deep anesthesia (Levy et al.).

Long-term survival of vegetative state patients at all ages is reduced drastically compared with the normal population. Life expectancy in adult patients is generally about two to five years; the vast majority do not live longer than ten years. In elderly patients the prognosis for survival is even worse; many do not survive for more than a few months. Infants and children may survive longer than adults do, but probably not significantly longer. Some studies have shown the average life expectancy to be four years for infants up to two months of age and about seven years for children seven to eighteen years old (Ashwal et al.).

Cases of prolonged survival—longer than twenty years—have been reported but are rare. One patient, Elaine Esposito from Tarpon Springs, Florida, lived for 37 years and 111 days without regaining consciousness, from age six to age forty-three. Another patient, Rita Greene, a surgical nurse from Wheeling, West Virginia, who survived for 47 years, 100 days from age twenty-four to age seventy-one, is probably the longest survivor in a permanent vegetative state ("Woman Lived Since '51 in Comalike State"). Considering the total estimated number of patients in a persistent vegetative state and the small number of well-documented cases of survival beyond fifteen years, the probability of an individual patient having such a prolonged survival is extremely low, probably less than 1 in 15,000 to 1 in 75,000 (Multi-Society Task Force on PVS).

It is more difficult to make the diagnosis of the vegetative state in newborns and infants. Generally, the diagnosis cannot be made below the age of three months except in the case of the condition of anencephaly. Anencephaly is the congenital malformation form of the permanent vegetative state (Stumpf et al.). This extensive and severe congenital malformation of the brain can be diagnosed with an extraordinarily high degree of certainty. At birth it is readily apparent by visual observation alone that the child has only rudimentary cerebral hemispheres and no skull except in the rear of the head. These children have variable degrees of brainstem functions but usually not enough functions to sustain life for any length of time. The vast majority are dead within two months, and most die within a few weeks.

The Locked-In Syndrome and the Minimally Conscious State

Brain death and the vegetative state should be contrasted with two other contemporary neurological syndromes of severe brain damage: the locked-in syndrome and the minimally conscious state. The locked-in syndrome, first named by Fred Plum and Jerome Posner in 1966, is characterized by a severe paralysis of the entire body, including the extremities and facial muscles, but with normal or nearly normal consciousness. This often results from a severe stroke to the brainstem that spares the cerebral hemispheres (in one sense the reverse of the vegetative state), and these patients often appear to be unconscious; however, a careful history and neurological examination uncover a high degree of cognitive functioning. Some physicians use this term to denote patients with any degree (e.g., mild to moderate) of disparity between paralysis and cognitive functioning. However, this term, when used properly, means a profound disparity between paralysis (severe) and consciousness (normal or nearly normal).

Unlike brain death, the vegetative state, and the lockedin syndrome, all of which are fairly well characterized and accepted by the medical profession, the term minimally conscious state is of relatively recent vintage, and its acceptance and potential usefulness as a distinct neurological syndrome are far from settled. Formally called the minimally responsive state, the minimally conscious state is defined as a condition of "severely altered consciousness in which minimal but definite behavioral evidence of self or environmental awareness is demonstrated," in other words, a condition of severely to profoundly impaired cognitive functioning (Giacino et al.). This diagnosis is made by the demonstration on a reproducible or sustained basis of one or more of the following behaviors: following simple commands, gestural or verbal yes/no responses, intelligible verbalization, and purposeful behavior such as appropriate smiling or crying, pursuit eye movement, and sustained visual fixation. Even though the difference between being vegetative and thus completely unconscious and being "minimally" conscious may seem to be a subtle distinction and even though some have argued that being minimally conscious is a medical fate worse than being vegetative, the courts in recent landmark decisions and many healthcare professionals have treated these syndromes radically differently from a medical, ethical, and legal standpoint (Rich).

Conclusion

The criteria for diagnosing cardiorespiratory death and brain death have been well established and accepted by the medical profession. Even though there are differences in how physicians may apply these criteria in individual cases and even though the standards may vary somewhat in different countries, there are no major disputes about the medical diagnosis itself.

The syndromes of permanent unconsciousness, in contrast, are much more variable than are those of brain death. The three major forms of the vegetative state—acute, degenerative, and congenital—are substantially different in terms of causes, type of brain damage, and length of time necessary to establish irreversibility. Thus, the criteria for a higher-brain formulation of death are far more complex and uncertain than are those for the whole-brain formulation of death.

ronald e. cranford (1995)

revised by author

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Death, Definition and Determination of: I. Criteria for Death

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