Journal of Critical Care 29 (2014) 878–880

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Special Section. "Death by Neurologic Criteria 1968 - 2014: Changing Interpretations"

Biophilosophical criticisms of brain death: The need for a new paradigm

There are good reasons why those declared dead on neurologic criteria are dead, but they are not necessarily the reasons that have been traditionally endorsed. In recent years, it has become increasingly clear that “brain-dead” bodies are not dead on biological grounds, which means the definition of death and the operational criteria to satisfy it are not consistent with one another. In other words, it is entirely possible to fulfill the neurologic criterion of death (a dead brain) but not the definition of death (cessation of integrated functioning or fundamental work of the organism) [1]. In addition, although this has remained a point of contention for many academics, the status quo continued and a utilitarian ethic trumped theoretical rigor. After all, to admit there is controversy in defining death does not incite public confidence, and the practical damages of admitting such patients are not yet dead would be enormous for organ donation as well as resource allocation. It remained an interesting but isolated debate. That is, until the Jahi McMath case [2]. When the McMath case captivated the United States in late 2013, it brought the theoretical arguments to the forefront and was the impetus of a renewed discussion on the legitimacy of the determination of death on neurologic criteria. Here was a situation where a mother, Nailah Winkfield, refused to accept that her 13-year-old daughter Jahi McMath, who underwent a tonsillectomy and adenoidectomy, was suddenly dead. At best, Winkfield was considered a grieving mother who could not accept reality, and, at worst, a calculating manipulator looking for a bigger malpractice settlement. The possibility that Winkfield might have been right— that her daughter was alive—was never seriously entertained by the medical community. This article will show that Jahi McMath is alive under the current definition of death despite suffering total brain failure (TBF) and will propose that changing the definition of death itself is warranted. This requires a move from a biological paradigm that focuses on the loss of somatic integration to an ontological one, which considers the irreversible loss of consciousness to be the hallmark of human death. However, given the inherent difficulty in determining the irreversible loss of consciousness, the continued usage of TBF as a criterion of death should be retained [3]. That is, we need not move to a higher brain death or neocortical standard. It is a parsimonious approach where the concept of death and the criteria used to satisfy it are consistent and no major change in clinical practice is required. This change in rationale is required, however, in that it provides both conceptual clarity and clinical confidence that those determined to have TBF are in fact dead and will ensure that cases like McMath are no longer open for debate. http://dx.doi.org/10.1016/j.jcrc.2014.06.016 0883-9441/© 2014 Elsevier Inc. All rights reserved.

The determination of death has always been less precise than we would like to believe. Traditionally, death has been determined by the irreversible loss of circulatory functions. 1 However, in 1968, when it became clear that life support technologies could give the impression of continued survival despite neurologic destruction, a second criterion was introduced. The Ad Hoc Committee of the Harvard Medical School used the term irreversible coma, which became colloquially known as brain death, as an alternative to the circulatory criterion [4]. The language was unfortunate, however, and would have longstanding consequences because it leaves one with the impression that there are 2 kinds of death: heart death and brain death, and with the doubt that perhaps brain death is not really true death. In point of fact there is a difference between the concept, or definition, of death and the criteria used to test for it. In an effort to rectify this confusion, there has been a shift to replace the term brain death with the more accurate TBF because it better represents that it is a criterion of death, not a special kind of death. Bodies suffering from TBF have always posed a particular challenge because they certainly do not look or feel dead. They are pink and warm, circulate blood, and perform tasks that we do not associate with corpses. This raises fundamental questions such as are they really dead, and if so why? The Ad Hoc Committee's argument for the neurologic criterion was based solely on the prognostic claim that death would occur, not on the diagnostic claim that it actually had occurred. To remedy this, over a decade later, The President’s Commission for the Study of Ethical Problems in Medicine and Biomedical and Behavioral Research endorsed the argument that the brain is the "primary integrator" of the organism as a whole, and when the whole brain is dead, the person is dead despite appearances to the contrary [5]. This rationale prevailed until scholars like Shewmon, Younger, Truog, and others systematically proved it wrong [6–8]. The primary integrator theory has 2 components. First is the claim that the brain confers unity to the organism as a whole, and when the brain is dead, the organism rapidly disintegrates. Second is the claim

1 The cessation of heart and lung function had, for centuries, been accepted as a reliable indication of death. However, due to inadequate instruments to measure the loss of such functions (the stethoscope was not discovered until the 19th century), misdiagnosis, in some cases, led to premature burials. Ironically, medical advancements in the 20th century complicated, rather than clarified, the determination of death. Technological interventions can confound the ability to sort the living from the dead. Although the fear of premature burial remains only as a ghastly historical footnote, new post modern horrors are found in the intensive care unit, where “life” can be maintained indefinitely without a subject to experience it.

Special Section. "Death by Neurologic Criteria 1968 - 2014: Changing Interpretations" / Journal of Critical Care 29 (2014) 878–880

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time—for example, to fight infection, heal wounds, and maintain temperature. If these kinds of integration were sufficient to identify the presence of a living “organism as a whole,” total brain failure could not serve as a criterion for organismic death, and the neurological standard enshrined in law would not be philosophically well grounded [14].

that if continued functions are maintained by life support, and not by the brain, they are artifact and may be disregarded [9]. However, is this rationale sound? Does a dead brain prove the loss of somatic integration and are the functions that do persist irrelevant if driven by machines? The short answer to both questions is a resounding no. A patient diagnosed with TBF can exhibit some or all of the following functions: respiration and circulation of blood, regain hemodynamic stability, metabolize and excrete waste, exhibit some brain function including measureable EEG output, retain an intact neurohormonal pathway, raise his or her temperature with the help of blankets, gestate a fetus to term, and fight infection [10]. Clearly, a patient who performs these functions does not fulfill the definition of death on biological grounds. These are, by definition, integrated functions in that they are examples of physiologic homeostasis. But what of the claim that these integrated functions are irrelevant because they are controlled by an intervention and not the brainstem? If such interventions were removed, the body would rapidly cease, so perhaps life support is simply masking death. Although it may sound satisfying at the outset, when examined further, it becomes clear that it is premised on faulty logic. Life support is not masking death in the case of TBF; it is preventing death by maintaining biological integration. Put in another way, a person is not alive or dead based on whether she can perform biological functions spontaneously or with the help of life support systems [11]. Strictly speaking, the point of life support is to support life. One may claim that as soon as you remove support for a TBF body the organism quickly fails. But the same could be said of any critically ill patient dependent on life support in the intensive care unit. Whether one can perform functions spontaneously or not is irrelevant in determining life from death. This perspective confuses a function as identical with the mechanism that performs it [12]. However, there is a difference between the thing that sponsors the function (brain) and the function itself (respiration, circulation, etc). If the function is what is significant, then it does not matter what causes it so long as it occurs. The central question is whether such functions persist, not the source. If those integrated functions are what is important, as the biological definition of death indicates, and since they persist in the presence of a dead brain, then it is clear either the definition of death needs to change, or we ought to abandon the neurologic criterion altogether. The last nail in the coffin of the biological definition of death is the fact that TBF bodies can continue to integrate for much longer periods than originally thought. Pregnant women with TBF have continued to gestate pregnancies for as many as 110 days to deliver viable fetuses [13]. To continue to claim such women are dead requires a new rationale since they are biologically very much alive. Finally, while some are satisfied that since there have been no documented cases of recovery from TBF that it is enough of a reason to determine death. But this is a prognostic self-fulfilling prophecy since such patients usually become organ donors or go to the morgue. A valid argument for why a dead brain is equivalent with a dead patient is still required. In the wake of these objections, The President’s Council on Bioethics delivered a white paper in 2008 to evaluate whether the neurologic criterion was still valid [14]. In their report, they provide a comprehensive overview of the philosophical and clinical controversies in the determination of death. In referring to the traditional defenders of the neurologic criterion they write,

To this end the Council defends TBF on a new account of “wholeness.” Their assessment of whether an organism is a whole depends on whether the fundamental vital work of an organism continues. They define such work as “the work of self-preservation, achieved through the organism’s need- driven commerce with the surrounding world.” [14]. According to this rationale, TBF is still an acceptable criterion for declaring death, not because it proves the body lacks integration, but because the organism can no longer engage in the essential work that defines living things. In their final analysis, if both consciousness and spontaneous breathing are irreversibly lost, the body cannot perform its vital work and the patient is dead. The scope of this article does not allow for a full examination of the Council’s report, but while an improvement over the integration argument, the new rationale does not rescue the neurologic criterion from many of the same inconsistencies that plagued earlier arguments. For a comprehensive treatment of the Council's arguments, see Shewmon's article [15]. 2 Total brain failure bodies are dead but not on the merits of biological arguments that focus on integrated function or the fundamental work of an organism. Total brain failure bodies are dead because they have lost that which is essential to the human person, which is capacity for consciousness. If we want to keep the neurologic standard, we cannot avoid what it is that we consider most important about the brain. This is not a radical idea. We already shifted concepts in 1968 when, for the first time in history, death was declared in the presence of breathing and spontaneous heartbeat. Further, the neurologic criterion has always rested on the permanent loss of consciousness as essentially significant since it is only when consciousness is permanently lost that integrated functions are ever considered superfluous [16]. However, assessing consciousness is perilous because it is an entirely subjective phenomenon and incredibly difficult to quantify, especially in cases of seriously incapacitated individuals. For example, it was traditionally thought that awareness or consciousness was sponsored solely by the cerebral cortex, but the brainstem also serves as an interface in the process. This demonstrates that complex interactions occur within the brain diffusely rather than in isolated parts, which is a primary reason we should not move to a higher brain or neocortical standard. Patients with TBF are dead because they have irreversibly lost the capacity for consciousness. A change in definition is required, but this does not require changing our current criteria since TBF ensures there is no capacity for consciousness. Those patients in persistent vegetative state or anencephalics would not be declared dead because they would not pass a TBF protocol. Only those who meet criteria for TBF will necessarily have irreversibly lost the capacity for consciousness. In so doing, we acknowledge the complexity of the brain and our limitations in assessment. To conclude, the claim that a dead brain fulfills the biological definition of death is not clinically or philosophically coherent and will lead to additional confusion as more people challenge the crumbling

They may have been mistaken, however, in focusing on the loss of somatic integration as the critical sign that the organism is no longer a whole. They interpreted—plausibly but perhaps incorrectly— “an organism as a whole” to mean “an organism whose parts are working together in an integrated way.” But, as we have seen, even in a patient with total brain failure, some of the body’s parts continue to work together in an integrated way for some

2 Shewmon explains that life-sustaining treatments can also continue the essential work of an organism regardless of brain status and the fact that such functions are not spontaneous is, as we have seen, irrelevant. Further, the absence of spontaneous breathing is not sufficient to declare death (eg, high spinal cord injury or Ondine’s curse) and the absence of consciousness is not sufficient to declare death (eg, those in persistent vegetative state), so Shewmon rightly questions why the loss of both conditions combined would be sufficient for death.

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Special Section. "Death by Neurologic Criteria 1968 - 2014: Changing Interpretations" / Journal of Critical Care 29 (2014) 878–880

dogma. We cannot sit idle hoping that problem cases like McMath will simply go away. This is a misguided approach that relies on the old paternalistic trope that “you’re dead when your doctor says you’re dead.” The McMath family, in fact, did not go away but pursued legal recourse and were successful in securing the right to maintain their daughter’s dead body precisely because there are medical and philosophical inconsistencies in these arguments. These must be rectified to preserve the integrity of the medical establishment and the public's trust. Leslie M. Whetstine, PhD Walsh University, North Canton, OH 44720 Email address: [email protected]

References [1] Tomlinson Tom. The conservative use of the brain-death criterion—a critique. J Med Philos 1984;9:377–94. [2] http://www.mercurynews.com/ci_24993245/jahi-mcmath-could-her-casechange-how-california. [3] Whetstine LM. An examination of the bio-philosophical literature on the definition and criteria of death; when is dead ‘dead’ and why some donation after cardiac death donors are not. PhD thesis Duquesne University; 2006.

[4] Ad Hoc Committee of the Harvard Medical School to examine the definition of death. “A definition of irreversible coma”. J Am Med Assoc 1968;205(6):85–8. [5] President’s Commission for the Study of Ethical Problems in Medicine and Biomedical and Behavioral Research. Defining death: a report on the medical, legal, and ethical issues in the determination of death. Government Printing Office; 1981. [6] Allen Shewmon D. The brain and somatic integration: insights into the standard biological rationale for equating "brain death" with death. J Med Philos 2001;26:457–78. [7] Youngner Stuart J, Arnold Robert M. Philosophical debates about the definition of death: who cares? J Med Philos 2001;26:527–37. [8] Truog Robert D. Brain death: at once “well settled” and “persistently unresolved”. AMA Policy Forum 2004;6. [9] Berna James L. How much of the brain must die in brain death? J Clin Ethics 1992;3(1):21–6. [10] Halevy Amir, Brody Baruch. Brain death: reconciling definitions, criteria, and tests. Ann Intern Med 1993;119(6):519–25. [11] Wikler Daniel. Brain death: a durable consensus? Bioethics 1993;7(2-3):239–46. [12] Tomlinson, "The Conservative use of the Brain-Death Criterion-A Critique", 1984. [13] Said A, Amer AJ, Masood UR, Dirar A, Faris C. A brain-dead pregnant woman with prolonged somatic support and successful neonatal outcome: a grand rounds case with a detailed review of literature and ethical considerations. Int J Crit Illn Inj Sci 2013;3(3):220–4. [14] CONTROVERSIES IN THE DETERMINATION OF DEATH A White Paper of the President’s Council on Bioethics Washington, DC December 2008; 2008 [www.bioethics.gov]. [15] Shewmon Alan. Brain death: can it be resuscitated? Hast Cent Rep 2009;39 (2):18–24. [16] Grandstrand Gervais Karen. Redefining death. New Haven: Yale University Press; 1986.

Biophilosophical criticisms of brain death: the need for a new paradigm.

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