Intensive Care Med DOI 10.1007/s00134-014-3301-0

Robert D. Truog Franklin G. Miller

WHAT’S NEW IN INTENSIVE CA RE

Defining death: the importance of scientific candor and transparency

Received: 6 February 2014 Accepted: 10 April 2014 Ó Springer-Verlag Berlin Heidelberg and ESICM 2014 The opinions expressed are the views of the authors and do not necessarily reflect the policy of the National Institutes of Health, the Public Health Service, or the US Department of Health and Human Services. R. D. Truog ()) Division of Critical Care Medicine, Boston Children’s Hospital, Boston, MA 02115, USA e-mail: [email protected] Tel.: 617-355-7327 R. D. Truog Center for Bioethics, Harvard Medical School, Boston, MA 02115, USA F. G. Miller Department of Bioethics, National Institute of Health, Bethesda, MD 20892-1156, USA

For most of human history, determining when a person had died was straightforward and uncomplicated—the differences between a living person and a cold, gray, stiff corpse were obvious to anyone. Two medical developments fundamentally changed all this. Intensive care medicine made it possible to maintain somatic functioning in patients with irreversible massive brain injury and inability to breathe spontaneously. The advent of organ transplantation made the situation of these hopeless individuals ideal for procuring vital organs. In order to make it possible to obtain living organs from a dead body, medicine endorsed creation of a diagnostic category called brain death, defined in terms of irreversible apneic coma. Individuals who fulfill the diagnostic criteria for this category are considered to be

dead, and hence their vital organs may be legally removed to save the lives of others, consistent with ‘‘the dead donor rule’’ [1]. From a societal perspective, this approach has worked well for decades, and now there is a movement to adopt this definition of death as an international standard [2]. Despite the impressive ability to save lives by means of organ transplantation, the claim that the diagnostic criteria for brain death equate with the biological death of the patient cannot withstand critical scrutiny. We contend that it is time for the medical profession to pause and reflect on its role in resolving difficult questions in medical ethics and health policy. While the meaning of death has many cultural, religious, and philosophical implications, medical science has unique authority for defining death as a biological phenomenon—the irreversible cessation of the functioning of the organism as a whole. In this regard, the profession needs to ask whether the claim that brain death represents biological death conforms with the highest standards of scientific knowledge and candor. The scientific approach to defining life can be traced back at least to the 1850s and Claude Bernard’s concept of the milieu inte´rieur, the internal state of equilibrium maintained by living organisms. Walter Cannon furthered this scholarship by developing the theory of homeostasis in the 1920s [3, 4]. These concepts have continued to evolve, such that today we understand life to be defined in terms of the capacity of organisms to use energy in maintaining a stable homeostatic internal environment and integrated functioning. When this capacity is lost, the organism has died. This definition applies across the biological spectrum, from single-celled organisms to complex plants and animals. In the 1980s, multiple scholars, including a US Presidential Commission, defended the concept of brain death as consistent with this biological definition of life and death, arguing that individuals who met the diagnostic criteria for brain death had lost ‘‘the integrated

Table 1 Patients diagnosed as brain dead often maintain integrated functioning of the organism as a whole—they are distinguished from healthy patients only by the lack of the capacity for consciousness and their dependence upon mechanical ventilation and tube feedings to maintain respiratory and nutritional function

Human characteristic

Healthy patients

‘‘Brain dead’’ patients

‘‘Biologically dead’’ patients

Integrated functioning of the organism as a whole Heart-beating, warm, well perfused Respiring, functional gas exchange Capacity for digestion, nutrition Functioning vital organs (kidneys, liver, etc.) Capable of somatic growth and development Capable of reproducing Intact wound healing Intact immune function Capacity for consciousness

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Yes Yes Yes Yes Yes Yes Yes Yes Yes No

No No No No No No No No No No

functioning of the organism as a whole’’ [5, 6]. Over the past several decades, however, we have learned that this is not scientifically correct. Incontrovertible evidence has been developed that many individuals who meet diagnostic criteria for ‘‘brain death’’ can continue to live and maintain integrated functions for varying periods of time, sometimes for months or even years [7]. The fact that the wide array of biological functions displayed by brain dead individuals are supported by mechanical ventilation is no reason to consider them dead, as this is similar to patients with high cervical quadriplegia, who also can live for years with ventilator support despite the near total physiological separation of the brain from the body [8]. The notion that the body requires the brain to maintain integrated function has been disproven, a point recently acknowledged by another US President’s Council on bioethics [9]. We now know that integrated functioning is an emergent property of organisms, and is not dependent upon an integrating organ like the brain (Table 1). Even if brain death does not cohere with a biological or scientific understanding of death, supporters have pointed to the intuitive plausibility of considering individuals who are irreversibly comatose and apneic as dead [10]. On closer examination, however, this intuitive plausibility quickly breaks down. Patients who are correctly diagnosed as being in a permanent vegetative state are irreversibly unconscious, yet they are not considered dead because they are not apneic. And patients with high cervical quadriplegia are apneic, yet they are not considered dead because they retain consciousness. Neither criterion by itself is sufficient to consider the patient to be dead, and there is no compelling rationale for why the

combination of these two equates to a definition of biological death. What should we conclude about the fact that brain death is not the biological death of the individual? We agree with the widespread consensus that obtaining organs from individuals who meet the diagnostic criteria for brain death is ethical, but not because they are dead. Instead, we argue that a solid ethical justification can be built around the principle of respect for patient autonomy (as manifest by the consent to donation from either the patient or an authorized surrogate) and the principles of nonmaleficence and beneficence. The brain dead are not harmed or wronged by properly authorized donation of their vital organs—a beneficent act that can save the lives of others [11]. Some will undoubtedly object that such an approach would open a Pandora’s box of concerns, and that we should keep the lid on the box by simply affirming that the diagnosis of brain death is a valid basis for determining biological death and that procurement of organs from brain-dead patients conforms with the so-called dead donor rule. But in so doing the medical profession falls short in fulfilling its obligation to certify death on a sound scientific basis. As difficult as it may be to engage in this more honest discussion about the ethics of organ transplantation, we submit that the longer term interests of society and the trust of the public in the medical profession will be better served by an approach more firmly rooted in scientific candor and transparency. Conflicts of interest On behalf of all authors, the corresponding author states that there is no conflict of interest.

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