Death is defined biologically as the irreversible loss of the functioning of the organism as a whole, which typically occurs after the loss of cardiorespiratory function. In 1968, a Harvard committee proposed that death could also be defined neurologically as the irreversible loss of brain function. Brain death has been considered to be equivalent to cardiorespiratory arrest on the basis of the belief that the brain is required to maintain functioning of the organism as a whole and that without the brain, cardiorespiratory arrest and biological death are both rapid and certain. Over the past 20 years, however, this equivalence has been shown to be false on the basis of numerous cases of patients correctly diagnosed as brain-dead who nevertheless continued to survive for many years. The issue reached national attention with the case of Jahi McMath, a young woman diagnosed as brain-dead after a surgical accident, who survived for almost 5 years, mostly at home, supported with a ventilator and tube feedings. The fact that brain death is not biological death has many implications, notably including the concern that procurement of organs from brain-dead donors may not comply with the so-called dead donor rule, which requires that vital organs be procured from patients only after they are dead. In this article, I conclude with an analysis of options for moving forward and among them advocate for reframing brain death as a “social construct,” with implicit societal acceptance that patients diagnosed as brain-dead may be treated legally and ethically the same as if they were biologically dead.

Most of us have intuitive understanding of death. When we see photographs or films about violence in the newspapers or on video, we are generally quickly able to distinguish the living from the dead. Dead human bodies share many characteristic features. They are not moving, their skin has a bluish-gray hue, and their bodies are stiff with rigor mortis. And our intuitive sense extends across the biological spectrum. We are equally adept at identifying dead animals, insects, trees, and flowers.

Yet some cases are not so clear. Imagine a young man in a hospital bed in the ICU. An endotracheal tube passes through his mouth into his lungs and is connected to a ventilator, which is breathing for him. His eyes are closed, and he does not respond to his name or any commands. Although his skin is pink and warm, he makes no spontaneous movements. Is he dead?

The answer to this question is complex.1  To answer it, a highly trained physician would need to have a detailed understanding of the mechanism of his illness or injury. A careful neurologic examination would need to be done. Laboratory tests would need to be performed to rule out the presence of metabolic abnormalities or sedative medications. He would most likely need advanced neuroimaging with computed tomography and/or MRI scanning. Finally, in most cases, parts of this examination would need to be repeated several hours later. Only then could the question of whether he is dead be definitively answered. In short, death has become a complicated concept, a concept that is no longer captured by our intuitive understanding.

In 1959, shortly after the development of mechanical ventilation, French neurophysiologists defined a condition they called “le Coma dépassé,” or “beyond coma.”2  In the article, the authors described a number of patients with devastating brain injuries that would have been uniformly fatal before the invention of ventilators. Yet these patients, who were thought to have no hope of any neurologic recovery, were nevertheless being kept alive with mechanical ventilation for an indefinite period of time. Historians often cite this publication as the beginning of our shifting views about the definition of death. How should we think about these patients who were beyond coma? In terms of our intuitive understanding of death, they would appear to be alive. But if being alive means being conscious of one’s surroundings and interacting with the world, then perhaps they should be viewed as being dead, or at least “as good as dead.”

Over the next several decades, this conversation continued. In 1968, a committee at Harvard Medical School proposed that patients who are both unconscious and incapable of spontaneous respiration be defined as dead.3,4  This committee also laid out criteria for making this diagnosis, which are criteria that are similar to those we use today in determining brain death. These criteria were instantiated into law in the United States in 1981, with adoption of the Uniform Determination of Death Act (UDDA).5  It states the following:

An individual who has sustained either (1) irreversible cessation of circulatory and respiratory functions, or (2) irreversible cessation of all functions of the entire brain, including the brain stem, is dead. A determination of death must be made in accordance with accepted medical standards.5 

The first clause is commonly called the cardiorespiratory criterion, whereas the second is referred to as the neurologic criterion. This law has stood the test of time; it has been the legal definition of death in the United States for almost 40 years. Yet it presents an ambiguity that has never been resolved. Do each of the clauses in the law represent different ways of being dead or are they just 2 different ways of determining biological death, that is, the intuitive understanding of what it means to be dead?

Dr Henry Beecher, the chair of the 1968 Harvard committee, clearly thought that the criteria recommended by his committee represented a new understanding of death: “Many today would take the view that when consciousness is permanently lost, … this is the ‘moment’ of death.”6  Yet by 1981, the view had shifted, and the authors of the UDDA took the opposite position: “As a practical matter, alternative standards may be necessary and appropriate. But the use of 2 standards in a statute should not be permitted to obscure the fact that death is a unitary phenomenon.”5 

Since 1981, the mainstream view has been that both the cardiorespiratory criterion and the neurologic criterion are just 2 different ways of diagnosing biological death. The most eloquent defense of this idea was published by Bernat et al7  in the same year that the UDDA was adopted into law. They argued that the brain was essential to maintaining integrated biological functioning of the human organism as a whole. In other words, they claimed that the loss of brain function always led to the disintegration of the body and cardiac arrest within 1 to 2 weeks. According to this logic, brain death does not represent a new understanding of what it means to be dead but is merely a new way of determining biological death in the era of mechanical ventilation and ICU care.

In the decades that have followed, this view has been consistently reiterated and reinforced in neurology literature. In their article, Wijdicks (a leading international authority on brain death) and co-workers8  wrote that “once brainstem function is lostblood pressure is unstable...relentlessly declining…cardiac arrhythmias appear… Support measures are complex, often fail, and the ability to maintain a brain-dead body is virtually impossible.” In another recent essay, Wijdicks9  wrote, “Globally, [physicians] now invariably equate brain death with death and do not distinguish it biologically from cardiac arrest…” This view has recently been adopted as the official position in guidelines from the American Academy of Neurology (AAN).10 

The problem with this understanding of brain death, now deeply ensconced in the neurology literature, is that it is demonstrably false. Overwhelming evidence exists revealing that it is not correct. Much of this evidence comes from the work of Dr Alan Shewmon. Over the years, Shewmon11  has meticulously documented dozens of cases of prolonged biological survival after the diagnosis of brain death.

The most dramatic case involved a young boy who was diagnosed as brain-dead from bacterial meningitis at the age of 4. He was supported with a ventilator and tube feedings for >20 years before succumbing to cardiac arrest and biological death. At autopsy, he had a completely calcified brain. No neural tissue could be identified, grossly or microscopically.12  Although this is only one case, it does dramatically make the point that the body does not need the brain to maintain integrated biological functioning over a long period of time.

Shewmon’s provocative findings were scrutinized by the President’s Council on Bioethics in 2008.13  Their analysis, published as the monograph “Controversies in the Determination of Death,” confirmed Shewmon’s conclusions, stating that, as “Shewmon rightly notes… the brain is not the integrator of the body’s many and varied functions… no single structure in the body plays the role of an indispensable integrator. Integration, rather, is an emergent property of the whole organism…”13 

Cases of prolonged biological survival after the diagnosis of brain death occur on a regular basis, most commonly in women who tragically become brain-dead while pregnant.14  In these cases, families may request that the woman be kept biologically alive long enough to deliver a viable child. Under the logic of the AAN, this means that women who have been biologically dead for weeks or even months are capable of giving birth, a conclusion that would strike many as arguably absurd.

Despite these many cases, however, the controversy about the meaning of brain death did not rise to the level of public awareness until the celebrated case of Jahi McMath.1517  McMath was 13 years old at the time she was admitted to Oakland Children’s Hospital in 2013 for complex pharyngeal surgery. Shortly after surgery, she developed a postoperative hemorrhage, which led to a cardiac arrest. Although she was successfully resuscitated, she suffered severe brain hypoxia and was pronounced brain-dead 3 days later. Her family refused to accept the diagnosis of brain death and initiated legal proceedings.

This resulted in McMath being transported to New Jersey, the only state that allows patients and families to categorically opt out of the determination of death by neurologic criteria.18  There, she remained biologically alive for almost 5 years, mostly at home, with occasional hospitalizations. During that time, she had a ventilator to breathe for her, she was fed through a gastrostomy tube, and she received supplemental hormones. Over those years, her body continued to grow and develop, and she began having menses. In 2018, she developed liver failure. Her family declined further interventions, and she died biologically from a cardiac arrest. She currently has 2 legally valid death certificates; in California, she died on December 12, 2013, and in New Jersey, she died on June 22, 2018.

There are many lessons that can be drawn from the case of Jahi McMath, not least of which are the ways that race and class impact medical care and may threaten the trust that should exist between patients, families, and their care providers.19  In terms of how we define death, however, the McMath case is significant because it clearly brought public attention to the fact that the diagnosis of brain death is not synonymous with biological death.

Given the significance of the case, one might wonder why there are not more cases like Jahi McMath. Several reasons can be offered. First, the diagnosis of brain death is almost always a self-fulfilling prophecy because it is quickly followed by either organ donation or ventilator withdrawal. Second, few families insist on continuing life support in the face of such a severe brain injury and a poor prognosis. Third, even those who do object to the diagnosis are typically overridden because brain death is recognized as legal death in every state. Nevertheless, in the rare cases in which life support is continued after the diagnosis, prolonged biological survival is not only possible but is not unusual.

One can only speculate on the answer to this question, but it is probably related to our observance of the dead donor rule (DDR).20  The DDR is not an actual law or regulation but rather an ethical assumption that has been seen as foundational to the ethics of organ procurement and transplant. In essence, the DDR prohibits the procurement of organs for transplant from patients before they are determined to be dead. The problem could then be stated as follows: if brain-dead patients are not biologically dead, then the common practice of procuring their organs would be in violation of the DDR.

This problem could be addressed in several possible ways. First, we could conclude that our current practices are unethical and stop procuring organs from brain-dead donors. This draconian response would put a halt to practices that save thousands of lives each year, in ways that most people find not only highly ethical but laudable.

Another alternative would be to critically examine the DDR itself. Is it really necessary that organ donors be determined to be dead before it is permissible for them to donate their organs? Would it be sufficient for us to know that they were beyond any hope of neurologic recovery and that they had given their permission for their organs to be used to save the lives of others? This is a possible solution that philosopher Frank Miller and I carefully examined in our book Death, Dying, and Organ Transplantation: Reconstructing Medical Ethics at the End of Life.21  We argue that this position is both conceptually sound and could provide a solid basis for a change in public policy.

A third possibility would be to explore the fact that “death” can be defined in more than just biological terms. Human death is a social, cultural, religious, and legal phenomenon. The determination of death signifies when we should begin religious and cultural rituals that allow us to mourn the loss of the person. It signifies when we should execute wills and pay out life insurance policies. In medicine, it defines the point at which clinicians are no longer obligated to continue with life-sustaining therapies, even when families insist. And, of course, it determines when organs may be procured for donation in accord with the DDR.

Using this perspective, we see that there is no binding reason for societies to define death in purely biological terms. Instead, societies could choose definitions of death that best serve their communal social and cultural needs. Rather than seeing death is a purely biological phenomenon, we could explicitly recognize that death is a social construct.

The philosopher Robert Veatch has developed this notion by proposing that “Death is the irreversible loss of that which is essentially significant to the nature of man.”22  This idea challenges us to consider what characteristics should be considered “essentially significant.” Many people, particularly in the Western world, identify strongly with their cognitive capabilities. If those cognitive capabilities are irreversibly lost, as, for example, when a person is determined to be irreversibly unconscious, then many people would believe they had lost something that was essentially significant.

Another candidate for a characteristic we might consider to be essentially significant could be the capacity for spontaneous respiration. Although it may be difficult to construct a philosophical argument for why spontaneous respiration should have this status, we all share an intuitive reluctance to consider any breathing organism, whether human or otherwise, as being “dead.” The absence of spontaneous respiration could never be considered sufficient for the determination of death (patients with high-cervical quadriplegia are incapable of spontaneous respiration, yet in many cases, are fully conscious and clearly alive), but this characteristic could nevertheless be considered a necessary condition for the determination of death.

These “death-making” characteristics are worth considering because they precisely capture the essential elements of the diagnosis of brain death. Conceptually, brain death can be defined as “irreversible apneic coma.” That is, the essential characteristics of brain death are that we have determined the patient to be both irreversibly unconscious and irreversibly incapable of spontaneous respiration. As such, the state of brain death is one plausible way of defining what Veatch22  refers to as “the irreversible loss of that which is essentially significant to the nature of man.”

One obvious objection to this argument is that society has never deliberated about, nor agreed on, either the idea that death is the irreversible loss of what is essentially significant to the nature of humans or that the state of brain death fulfills this condition. But one way of reading the history of organ transplant over the past 50 years is that most of society has, de facto, expressed acceptance of this premise by its actions. For the most part, members of Western societies seem to be comfortable with the notion that brain-dead patients are in fact dead, even if they are not dead in the biological sense of the term. This is not the case in many Eastern civilizations, in which people do not identify as strongly with their cognitive capacities and the concept of brain death is much less accepted.23 

In the earlier sections, I mentioned 3 possible ways of addressing the conflict between recognizing that brain death is not biological death and our observance of the DDR. There is a fourth option, and indeed probably the most likely, which is to ignore the problem. In accord with the guidelines from the AAN, we could continue to insist, against all of the evidence, that brain death is biological death.

This may be, in fact, the most expedient solution. Many technological developments suggest that in the future, we may no longer need to procure organs from human beings at all. For example, research is actively underway to develop gene-editing techniques for overcoming the immunologic and infectious hurdles that currently preclude using pigs as a virtually unlimited source of transplantable organs.24  Those who are developing this strategy argue that it could be in clinical trials within just a few years. If this technology, or others like it, come to fruition, then the need for making the diagnosis of brain death will virtually disappear. This will solve the problem, not by resolving conceptual difficulties inherent in the concept of brain death but rather by making the diagnosis irrelevant.

But in the meantime, I think the medical profession should be cautious in continuing to insist that brain death means something that it clearly does not. We are increasingly living in an era when “fake news” is being developed as an art form. Politicians and the corporate world literally create the facts they need to support their agendas rather than shaping their agendas to fit the facts. This is rapidly leading to a tremendous loss of the public’s trust in many of the basic institutions of society. Yet nothing is as essential to the integrity of the medical profession as the trust that patients have in their doctors and other care providers. Although the failure of the medical profession to tell the truth about the meaning of brain death may seem relatively small and insignificant in the big picture, it could also represent the crack in the dike where the profession’s commitment to truth begins to break down. Given the perilous times in which we live, this could be precisely the moment when the profession needs to stand up and show its commitment to honesty, integrity, and truth telling.

Dr Truog is entirely and solely responsible for the content of this manuscript, is accountable for all aspects of the work, and approved the final manuscript as submitted.

FUNDING: No external funding.

     
  • AAN

    American Academy of Neurology

  •  
  • DDR

    dead donor rule

  •  
  • UDDA

    Uniform Determination of Death Act

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Competing Interests

POTENTIAL CONFLICT OF INTEREST: The author has indicated he has no potential conflicts of interest to disclose.

FINANCIAL DISCLOSURE: Dr Truog is a member of data safety monitoring boards for Sanofi and Covance.