Controversy in the Determination of Death: The Definition and Moment of Death

Abstract

This essay reviews recent controversy in the determination of death, with particular attention to the definition and moment of death. Definitions of death have evolved from the intuitive to the pathophysiologic and the medicolegal. Many United States jurisdictions have codified the definition of death relying on guidance from the Uniform Determination of Death Act (UDDA). Flaws in the structure of the UDDA have led to misunderstanding of the physiologic nature of death and methods for the determination of death, resulting in a bifurcated concept of death as either circulatory/respiratory or neurologic. The practice of organ donation after circulatory determination of death (DCDD) raises a number of ethical questions, most prominently revolving around the moment of death and manifested as an expedited time to determination of death, a departure from the unitary concept of death, a violation of the dead donor rule, and a challenge to the standard of irreversibility. Attempts to redefine the determination of death from an irreversibility standard to a permanence standard have significant impact on the social contract upon which deceased donor organ transplantation rests, and must entail broad societal examination. The determination of death is best reached by a clear, strict, and uniform irreversibility standard. In deceased donor organ transplantation, the interests of the donor as a person are paramount, and no interest of organ recipients or of the greater society can justify negation of the rights and bodily integrity of the person who is a donor, nor conversion of the altruism of giving into the calculus of taking.

Modern reexamination of the nature of death includes discussion of the definition, pathophysiology, ethics, and legal structure of the determination of death. This reexamination has been generated in part due to controversies raised by the practice of organ donation after circulatory determination of death (DCDD), particularly as to the definition and moment of death. DCDD questions traditional concepts of the time to determination of death, the unitary nature of death, the dead donor rule, and the irreversibility standard in determination of death. In this essay, I review historical context provided by the development of definitions of death and the conceptual development of the Uniform Determination of Death Act (UDDA). I analyze contemporary ethical controversies raised by the current practice of DCDD regarding an expedited time to determination of death, a departure from the unitary concept of death, a violation of the dead donor rule, and a challenge to the standard of irreversibility. I argue that the determination of death is best reached by a clear, strict, and uniform irreversibility standard, that the interests of the donor as a person are paramount, and that no interest of organ recipients or of the greater society can justify negation of the rights and bodily integrity of the person who is a donor, nor conversion of the altruism of giving into the calculus of taking.

The Definition of Death

Since the dawn of human understanding, we have conceptualized death in binary terms as the absence of life. We also classically understand death as a singular event in time. Samuel Johnson captured both concepts in ¹⁷⁵⁵, defining death as “the extinction of life; the departure of the soul from the body” (p. 542). This intuitive understanding of death persisted well into the modern period. In American law, the first edition of Black’s Law Dictionary in 1891 defined the legal conception of natural death by adopting Johnson’s definition (pp. 334–35). For some time, the medical definition of death also relied on this intuitive construction. In ¹⁹⁰⁰, the first edition of Dorland’s American Illustrated Medical Dictionary defined death as “cessation or extinction of life” (p. 192).

Pathophysiology and the Definition of Death

As medicine progressed, the simplicity of intuitive traditions began to accommodate pathophysiologic understandings of death. As early as 1873, Alfred Swaine Taylor wrote in his Manual of Medical Jurisprudence that “the proof of death is the proof of cessation of the heart’s action for a certain period. The more visible indication of death is the cessation of breathing…” (p. 60). Interestingly, the first edition of Black’s (1891) Law Dictionary followed the legal definition of death with a secondary medical and pathophysiologic definition of death:

DEATH. The extinction of life; the departure of the soul from the body; defined by physicians as a total stoppage of the circulation of the blood, and a cessation of the animal and vital functions consequent thereon, such as respiration, pulsation, etc. (pp. 334–35; emphasis added)

In the preresuscitation era, death was always recognized as a unitary condition of loss of spontaneous circulatory and respiratory functions accompanied by loss of total central nervous system function. With no opportunity for resuscitation, cessation of the function of the brain inevitably followed and was implicitly incorporated into the circulatory/respiratory criterion for death. As Thomas Hawkes Tanner wrote in ¹⁸⁵⁵, “death…approaches through one of the three vital organs—the brain, the heart, or the lungs.…[A] cessation of the functions of either of the three speedily arrests the remaining two.…And so it results that failure in any one of the three links in the chain is fatal” (p. 75). Likewise, the presence of circulation and respiration was evidence that death had not yet occurred.

The advent of mechanical ventilation and cardiopulmonary resuscitative techniques challenged pathophysiologically based medical definitions of death by providing exceptions, while confusing intuitively based legal definitions by providing contradictions. With the availability of mechanical ventilation and artificial cardiac pacing, cardiac and respiratory functions could be either spontaneous or artificially maintained even in cases of devastating neurologic injury. In ¹⁹⁵⁹, Pierre Mollaret and Maurice Goulon described a series of patients who maintained circulation while mechanically ventilated but who lacked brain stem reflexes, had apnea without mechanical support, and had a flat electroencephalogram. The nascent field of organ transplantation called acute attention to these patients on the question of whether they could be considered in essence heartbeating cadavers.

In discussions held at the 1965 Ciba Foundation Symposium Ethics in Medical Progress, G. P. J. Alexandre described a set of criteria to define death in patients “with head injuries whose hearts had not stopped” with the resultant conversion of those patients to heartbeating organ donors (Wolstenholme and O’Connor 1966, 68–69; hereinafter cited as the Ciba Symposium). Roy Calne responded that “although Dr. Alexandre’s criteria are medically persuasive, according to traditional definitions of death he is in fact removing kidneys from live donors” (Wolstenholme and O’Connor 1966, 73). Calne stated that “the traditional diagnosis of death is made if the heart has stopped beating for five minutes in a patient at normal body temperature, or if the heart is quite incapable of resumed action in a patient who is hypothermic—for example, a heart irrevocably damaged during cardiac surgery” (Wolstenholme and O’Connor 1966, 73).¹

Such confusion, and a growing divergence between the legal and medical understandings of death, resulted in efforts to modernize the definition of death. The search for a modern definition of death involved efforts to produce a uniform statutory approach to the determination of death. These processes produced a great deal of controversy and uncertainty as to the precise definition of death, particularly as to whether death is an event of unitary or bifurcated construction.

The UDDA

As states began to struggle with statutory constructions that would incorporate seemingly divergent definitions of death and that would clarify determination of the time of death, many saw the need for a more uniform statutory approach (Compton 1974). In 1981, the President’s Commission for the Study of Ethical Problems in Medicine and Biomedical and Behavioral Research reached conclusions as to both the moment of death and the pathophysiology of death. The President’s Commission accepted the idea that death occurs as a singular event at a defined moment in time, though it declined to offer further specific guidance on that point (President’s Commission for the Study of Ethical Problems in Medicine and Biomedical and Behavioral Research 1981, 57–58; hereinafter cited as the President’s Commission Report).² Regarding pathophysiology, the President’s Commission concluded that “death is a singular phenomenon,” which could be diagnosed by distinct criteria:

When the presence of a mechanical ventilator precludes the use of traditional vital signs (i.e., respiration and heartbeat) to ascertain whether a person is alive, the use of brain-based criteria provides another means of making such a determination. Thus, brain-based criteria do not introduce a new “kind of death,” but rather reinforce the concept of death as a single phenomenon—the collapse of psycho-physical integrity. (The President’s Commission Report 1981)

In defining death at the “level of general physiological standards,” the President’s Commission proposed two “alternative standards,” detailing the background of this construction by stating that,

[I]n the vast majority of cases irreversible circulatory and respiratory cessation will be the obvious and sufficient basis for diagnosing death. When a patient is not supported on a respirator, the need to evaluate brain functions does not arise. (The President’s Commission Report 1981, 73–74)

The President’s Commission then endorsed the UDDA as a work product:

Uniform Determination of Death Act. 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. (The President’s Commission Report 1981)

Unfortunately, the text of the Act was flawed on several key points. It did not clearly specify that its circulatory/respiratory criterion applied to spontaneous nonsupported functions.³ It did not clarify that death as a singular unitary phenomenon must encompass irreversible loss of both spontaneous circulatory/respiratory function and whole brain function. And it left unclear that its either/or construction established two criteria to diagnose a singular unitary state of death, as opposed to two kinds of death.

The summary effect of these flaws is that many now erroneously read the UDDA to establish a “bifurcated” definition of death, codifying two distinct types of death, each of which may be diagnosed to the exclusion of the other.⁴ This error provokes confusion regarding when a person is dead and is particularly apparent in the field of DCDD.

The Moment of Death

The search for transplant donors, having previously catalyzed questions regarding the definition of death, is again provoking fundamental reexamination of the nature of death, now questioning the moment of death in the context of DCDD. DCDD, previously known as nonheartbeating organ donation (NHBD) or donation after cardiac death (DCD), is distinct from organ donation from brain-dead heartbeating donors in that it involves removal of organs from a patient who is not yet dead at the time that the patient is transported to the operating room. The patient is prepped and draped for organ recovery while still alive and then undergoes a planned withdrawal of life supportive measures, followed by an expedited declaration of death by circulatory/respiratory criteria. Once death is declared, organ recovery urgently proceeds (The President’s Council on Bioethics 2008, 79–87).⁵ DCDD raises a number of ethical questions, most prominently revolving around the moment of death and manifested in an expedited time to determination of death, the departure from a unitary concept of death, a violation of the dead donor rule, and a challenge to the standard of irreversibility.

An Expedited Time to Determination of Death

One of the principle rationales for DCDD is to minimize the warm ischemic time—the time from cessation of circulation to the cold perfusion of the organ—that is incurred in recovery of organs from nonheartbeating donors. Prior to the development of DCDD protocols, this time for kidneys procured by NHBD was often as much as sixty to ninety minutes due to the need to pronounce death, obtain consent, assemble the operating team, transport the cadaver to the surgery suite, and remove the kidney for cold perfusion (White 2016). In 1989, Gauke Kootstra began to regularly employ withdrawal of ventilator support from donors who were brain injured but not brain dead, establishing modern DCDD practice (Kootstra, Kievit, and Heineman 1997). Kootstra had initial ethical concerns with this practice, centering on the irreversibility of loss of circulatory/respiratory functions. He noted that in DCDD practice, “the question arises as to whether somebody is really dead at the moment of cardiac arrest and whether the dead donor rule is respected” (Kootstra, Kievit, and Heineman 1997, 846). His procedures thus included a waiting period after circulatory declaration of death in order to be sure that cardiac arrest was irreversible, thereafter followed by cannulation and cold perfusion of the aorta (Kootstra and Daeman 1996).

The period of time postcirculatory arrest before organ recovery may legitimately proceed in DCDD has subsequently been a topic of extensive interest on points of both irreversibility of circulatory cessation and compliance with neurologic death criteria. In 1992, the University of Pittsburgh published a protocol allowing the immediate recovery of organs from nonheartbeating donors after a period of two minutes of ventricular fibrillation, asystole, or electromechanical dissociation in an unresponsive apneic patient (University of Pittsburgh Medical Center 1993; hereinafter cited as the Pittsburgh Protocol). This time was chosen on grounds of circulatory irreversibility, described as a lack of cardiac “autoresuscitation” (De Vita and Snyder 1993). Kootstra noted this short interval, and, in addition to his prior concerns of circulatory irreversibility, he was also concerned about the neurologic status of these donors. In 1995, he extended the postarrest period in his protocol to ten minutes, believing that a ten-minute absence of circulation would be sufficient to cause brain death (Kootstra 1996). In 1997, the Institute of Medicine (IOM) noting that the two-minute interval was too short to support a determination of brain death, recommended a five-minute interval of loss of circulatory function before pronouncement of death and recovery of organs (Potts, Herdman, and the Division of Health Care Services, Institute of Medicine 1997, 59).⁶ In 2006, the National Conference on DCD supported the position of the Society of Critical Care Medicine that after asystole, a period of no less than two and no more than five minutes should elapse before organ recovery begins (Bernat et al. 2006). As part of a multi-organizational joint statement on ethical and policy concerns in DCDD, principally authored under the auspices of the American Thoracic Society (ATS), the United Network for Organ Sharing (UNOS) in 2012 endorsed a two-minute period of absent circulation as sufficient to pronounce death and begin organ recovery (Gries et al. 2013; hereinafter cited as the ATS/UNOS statement).

There are clearly concerns as to whether the neurologic criteria for a unitary death are met under these circumstances. In its 1981 report, the President’s Commission Report cited a much longer interval to reach the neurologic criteria, stating that “if deprived of blood flow for at least 10-15 minutes the brain, including the brain stem, will completely cease functioning” (pp. 16–17). In an animal study carefully designed to reproduce the procedures of DCDD, Stiegler and colleagues performed continuous electroencephalographic (EEG) monitoring and assessment of brain stem reflexes to assess the neurologic state at various time intervals after the loss of circulation. Their study induced ventricular fibrillation for variable periods of time, then employed cardiopulmonary resuscitation, and assessed subsequent evidence of neurologic recovery of functions (Stiegler et al. 2012). The authors concluded that two-minute intervals as specified in the Pittsburgh Protocol “do not fulfill clinical and electrophysiological criteria of brain death at the time of donation” (Stiegler et al. 2012, 489). Based on their experimental data, they felt that the ideal time period to meet brain death criteria, including irreversibility of cessation of functions, was between five and ten minutes and that a ten-minute period would reliably do so.

There is no significant doubt that the warm ischemic time is directly related to function of the donor organ in the recipient (Asher and Navarro 2009). However, expediting the time for organ recovery to two minutes (or less) raises substantive doubt as to whether the donors are dead by neurologic criteria. In DCDD, tension between these concerns is often resolved by departing from the unitary concept of death and conceiving death as a bifurcated phenomenon, by accepting the possibility of violations of the dead donor rule, and by challenging long-agreed standards of irreversibility in the determination of death.

A Departure from the Unitary Concept of Death

Unlike colleagues of a past generation who faced the conceptual challenges of brain death prior to statutory definitions, physicians caring for patients under DCDD protocols have largely abandoned the unitary construct of death and have instead promulgated a bifurcated death construction. As noted above, this is in large part due to confusion generated by the structure of the UDDA with its alternative physiologic criteria for determining death. However, the President’s Commission explicitly stated that it chose this structure only because circulatory and respiratory cessation were “the obvious and sufficient basis for diagnosing death” (The President’s Commission Report 1981, 73–74). The Commission held that “temporary loss of blood flow (ischemia) becomes a permanent cessation only because of the damage it inflicts on the brain” (The President’s Commission Report 1981, 74). Regarding the idea that both circulatory/respiratory and neurologic criteria should be formally documented, the President’s Commission stated,

Most of the time people do not, and need not, go through this two-step process because—setting aside any mythical connotations of the heart—a person without blood flow simply cannot live. (The President’s Commission Report 1981)

What the President’s Commission did not foresee was a time in which transplant surgeons might wish to incise the body of a person within seconds or minutes of circulatory/respiratory cessation in order to perform procedures that would be considered harmful or fatal to a person who was not certainly dead by neurologic criteria.⁷ The circulatory/respiratory death at the foundation of the President’s Commission Report was a traditional unitary death—patients found dead or observed to die were pronounced dead after a process of loss of circulation temporally “obvious and sufficient” to insure the permanent and irreversible loss of functions of the central nervous system.

With the promulgation of the Pittsburgh Protocol, the criterion for death in the DCDD donor was explicitly set as an irreversible cessation of circulatory/respiratory function, defined conceptually as “when it is determined that auto-resuscitation will not occur” (De Vita and Snyder 1993, 139). As David Cole (1993) has noted, the developers of the Pittsburgh Protocol “explicitly seek to ignore any measure of CNS function or capacity that might permit resuscitation. That is, the UPMC protocol countenances pronouncing as dead persons who may well have sufficient CNS function to permit resuscitation.…” (p. 148). That is to say—some patients under the Pittsburgh Protocol may be undergoing retrieval incisions at a time when they are not dead, and their surgeons know or should know that they are not dead.

Similar concerns have been raised about procedures approved for DCDD by the IOM. In its 1997 report, the IOM explicitly committed to a bifurcated death construction in which neurologic determination of death was irrelevant:

The NHBD is a donor whose death is defined by “irreversible cessation of circulatory and respiratory functions” as opposed to “irreversible cessation of all functions of the entire brain, including the brainstem.”

In addition, although this is not relevant to a determination of death, the interval of absent circulation recommended here will, in a donor with normal body temperature, produce irreversible brain damage (Potts, Herdman, and IOM 1997, 23, 59; emphasis added).

Jerry Menikoff (2002) criticized this bifurcated construction as operationally insufficient, noting that “at the time the individual is declared dead, it is quite possible that substantial portions of that person’s brain (including the higher brain, responsible for thoughts and emotions) have not yet permanently ceased to function” (p. 14). In 2000, the IOM clarified its position, referring to “death established by neurological criteria” and “death established by cardiopulmonary criteria” as two ways of determining that death had occurred (Institute of Medicine, Division of Health Care Services 2000, 17–18). However, the IOM did not retreat from its abandonment of the neurologic criteria and its endorsement of a bifurcated construction in the determination of death in DCDD, holding that “the UDDA specifies the irreversible loss of all brain function or the irreversible cessation of cardiopulmonary function, not both” (Institute of Medicine, Division of Health Care Services 2000, 24; emphasis in the original). By 2006, the IOM position had moved further toward a unitary concept of death in DCDD with its statement that “the starting point for organ donation is death—death that is determined by using one of two sets of criteria” (Childress, Liverman, and the Institute of Medicine 2006, 129). However, while acknowledging controversy over the neurologic issue, the IOM maintained that the neurologic criteria were subsumed by the circulatory criteria:

Once circulation is permanently lost, so, too, is neurologic function permanently lost. Consciousness is lost and brain function ceases approximately 15 seconds after circulation to the brain ceases. If the circulation does not resume, neither will neurologic functions resume. (Childress, Liverman, and the Institute of Medicine 2006, 146)

In 2013, the ATS/UNOS statement again returned to a bifurcated death construction, stating that “in the United States, death is defined as the irreversible cessation of either neurological or circulatory function” and made no mention of any need to evaluate neurologic functions in DCDD (Gries et al. 2013, 106).

The Organ Procurement and Transplantation Network (OPTN) maintains an implicitly bifurcated construction for the definition of death in its “Deceased Donor Organ Procurement Policy.” In this document, the OPTN (2019) states that “Donation after Circulatory Death (DCD) describes the organ recovery process that may occur following death by irreversible cessation of circulatory and respiratory functions,” with no mention made of any need to confirm neurologic signs of death (p. 3).

The notion that clinical evidence of the neurologic criteria for death should be explicitly sought in DCDD as part of a unitary determination of death is neither novel nor burdensome. In 2008, the Academy of Medical Royal Colleges in its Code of Practice for the Diagnosis and Determination of Death stated that the conditions identifying the death of a living human being after cardiorespiratory arrest should include “the simultaneous and irreversible onset of apnoea and unconsciousness in the absence of the circulation” with the confirmation of “the absence of the pupillary responses to light, of the corneal reflexes, and of any motor response to supra-orbital pressure” after five minutes of continued cardiopulmonary arrest (Academy of Royal Medical Colleges 2008, 12).

The ²⁰¹⁰ consensus report Donation after Circulatory Death supported by the British Department of Health and endorsed by the Intensive Care Society and the British Transplantation Society relied on the Academy of Royal Medical Colleges’ Code of Practice stating that,

Within the context of DCD, death is diagnosed using cardiorespiratory criteria, and with the “confirmation that there has been irreversible damage to the vital centres in the brain-stem, due to the length of time in which the circulation to the brain has been absent.” (p. 36)⁸

The British Transplantation Society (2013) stressed the importance of the neurologic state of the DCDD donor in its 2013 guidelines, stating that “death is in essence a neurological event and occurs when there is a permanent loss of the capacity for consciousness [and] all brain stem function” (p. 26).

Thus, although the transplant community in the United States has broadly applied a bifurcated construction to the determination of death and has largely abandoned the required determination of a unitary death, the British transplant community has not done so. Perhaps this is because the British experience has not been subject to the misinterpretation of the UDDA. There is no statutory definition of death in Britain; rather, the courts have adopted medical guidelines for the determination of death in case law (Academy of Royal Medical Colleges 2008, 11).

A Violation of the Dead Donor Rule

Some suggest that concerns regarding a departure from the unitary concept of death in DCDD are theoretic, or at most immaterial, as to the determination of death and the violation of the dead donor rule. James Bernat took such a position in 2013:

If one were to conclude that DCDD violated the DDR [dead donor rule], I have argued that it would constitute a justified violation because, by preventing the donation from killing the donor, it satisfies the spirit of the DDR. Once circulation has ceased permanently, the brain is gradually destroyed by lack of circulation causing hypoxic-ischemic neuronal destruction. The subsequent recovery of organs for transplantation has no impact whatsoever on this inevitable process so it neither causes nor accelerates the death of the donor. Therefore, DCDD does not constitute a violation of the DDR and, in any event, respects the spirit of the DDR. (p. 427)

To hold DCDD as a justified violation of the DDR is to mount an explicitly teleological or exceptively deontological defense. Here, we may disregard the neurologic criteria of a unitary death and expedite the time for the moment of death under the circulatory/respiratory criteria simply because the patient, although perhaps not dead, is going to die, and we are not causally impacting that process by taking their organs. So if we remove a kidney (or more vitally a liver, a lung, or a heart) before the brain has irreversibly ceased to function—where is the harm?

Such an “as good as dead” approach is fundamentally inconsistent with the foundations of the dead donor rule on the one hand and with our general prohibitions of surrogate consent for living organ donation from incompetents on the other. Examination of the latter inconsistency is beyond the scope of this essay, but as to the former, we should note that the dead donor rule is normative in nature and founds the social contract that governs organ donation. We have seen that from the time of the foundation of deceased donor transplantation, the guiding principle has been that the donor must be certainly dead. The position that a person with absent circulation but not certainly dead by neurologic criteria may permissibly have vital organs removed rests on one of two premises—firstly that the unitary construction of death does not apply or secondly that the normative dead donor rule is either explicitly teleological or exceptively deontological.⁹

As we have seen, the construct of death as bifurcated and nonunitary is widely held throughout the transplant community in the United States. But Bernat (2013) holds that “the best definition of death is the cessation of the critical functions of the organism as a whole” and that “the criterion that best satisfies the definition of death is the irreversible cessation of all clinical brain functions” (p. 424). There is no doubt that in the DCDD donor with absent circulation, the brain is “gradually destroyed.” But as Bernat points out, “A higher organism can reside in only one of two states, alive or dead: no organism can be in both states simultaneously or in neither state” (p. 423). The person who is a DCDD donor just becoming asystolic on an operating table is either alive or dead but is not in a state of as good as dead.

Thus, the position justifying removal of organs from such a person must either rest on the idea that the dead donor rule is normatively teleological or that it is deontological but allows exceptions. Teleological construction of the dead donor rule applies a utilitarian consequentialist ethic—that the good to come from harvesting of the organ even though the person is not certainly dead outweighs the good of protecting the rights and bodily integrity of the dying person on the operating table. An actualizable good—improving the health of the organ recipient—is weighed against the nonphysical good of preservation of the rights and the bodily integrity of the person who is to become a deceased donor. This approach is more than inherently dangerous. Allowing a pure utilitarian calculus to apply relative weight to the essential right of a person not to be killed or nonbeneficially harmed is to potentially allow the problems raised by DCDD to expand far beyond the DCDD surgical suite and its debate over several additional minutes of circulatory cessation to reach an irreversible unitary death. Here, we may justify all sorts of takings, particularly those by empowered political elites, so long as the consequences merit. Here, we may harvest organs from Falun Gong political prisoners on an as needed basis. Here, we may perform partial-birth abortion (or infanticide) without so much as a wince. Here, we may clone human beings and create human–animal hybrids to further medical research with no reservations. Teleological normative ethos weighs the weak and vulnerable in the balances and finds them wanting.

An exceptive deontological construction of the dead donor rule applies a duty based on recognition of the rights of the person not to be killed or nonbeneficially harmed but allows a conditional exception to that duty based on the situational circumstances. Here, the imminent death of a person allows abrogation of the requirement for certainty that their essential rights are not being violated. This is what has been described as “threshold deontology” wherein the consequences may mitigate the deontological rule if they are of a certain weight (Alexander and Moore 2016). In this case, we are considering that the imminent death of the person mitigates the duties imposed by the rights of that person. This argument rests on several possible foundations. One is that the person as good as dead is no longer a person at all and thus has no essential rights. Another holds that such a person is less of a person, and their rights, though present, are diluted and subject to negation. Third is that the aggregation of rights of the many may remove, dilute, or negate the rights of the one. These foundations are an acceptance of a fluid concept of personhood and a collapse of deontology into teleology, subject to all its perverse consequences.

Either construction arguably transforms the DCDD process from a postmortem giving authorized by the donor (or surrogate) to a premortem taking by organ recipients and their agents. This conception has been unacceptable since the beginning of transplantation, when authorizing legislation took a strict deontological approach to organ donation and recovery. The 1968 Uniform Anatomical Gift Act (1968) provided in Section 2 that “any individual of sound mind and 18 years of age or more may give all or any part of his body for any purpose specified in section 3, the gift to take effect upon death” (§ 2; emphasis added). This construction persists in the Revised Uniform Anatomical Gift Act of 2006, which provides that “‘Anatomical gift’ means a donation of all or part of a human body to take effect after the donor’s death for the purpose of transplantation, therapy, research, or education” (emphasis added).

Persons who agree to provide an anatomical gift do so with the understanding that the processes authorized by the statute require certainty in the determination of death. Furthermore, consent (or authorization) is not relevant to the concept of a premortem recovery. Within the realm of deceased donor transplantation, its practice and its legal structure recognize the right of a person to consent to the postmortem taking of their organs but do not recognize the right of a person to consent to the taking of their lives or the premortem removal of their vital organs.

There is no allowance for an uncertain premortem taking here. There is no weighing of goods. There is no mention of the interests of the organ recipient. There is only the strict deontologically normative rule that the donor must be dead. Surgeons who consequentially stray beyond this statutory authorization are working in the territory of battery or something worse.¹⁰

It is clear that this statutory construction does not allow for exceptions. It does not recognize the state of “imminent neurological death” outlined in the OPTN policies.¹¹ The statutory construction is binary—a person is dead or nondead, and an anatomical gift is only effectuated upon the death of the person who is the giver. We must, without exception, be certain that the person is dead.

Examination of whether the dead donor rule prohibits the taking of vital organs from a donor not yet dead is also proscriptively important. Dalle Ave, Sulmasy, and Bernat (2019) have recently held that the DDR prohibition on procurement of vital organs before death was a later addition to the concepts embodied in the DDR and is not violated by the practice of DCDD. Citing the 1999 construction of John Robertson, they hold that expedited recovery of organs from a donor dead by circulatory criteria does not violate the DDR and is only called into question by later authorities.¹²

However, a 1999 formulation of the DDR is clearly retrospective to more than thirty years of transplant practice. The earliest formulations of the DDR date to the dawn of the transplant era. In 1963, the British Medical Journal, in commenting on the Potter case at the Newcastle General Hospital, advised readers that “to hasten the death of a person whose death (through sickness or previous injury) is already inevitable is homicide in law” (“Moment of Death” 1963, 394).¹³ The Journal further held that “anyone removing organs from an apparently inanimate body (for instance, one retrieved from a serious traffic accident) must first ask himself whether he can positively pronounce the body dead” (“Moment of Death” 1963, 394).

At the Ciba Symposium, held in the early transplantation era and prior to the acceptance of brain death, Thomas Starzl addressed such concerns directly, commenting on the reverse paradigm in which organs were to be removed from neurologically devastated donors before the cessation of the heartbeat:

We have been discussing this practice in relation to renal homografts. Here, a mistake in evaluation of the “living cadaver” might not necessarily lead to an avoidable death since one kidney could be left. But what if the liver or heart were removed? Would any physician be willing to remove an unpaired vital organ before circulation had ceased? (Wolstenholme and O’Connor 1966, 70)¹⁴

Here, Starzl is vigorously defending the dead donor rule in the context of a donor who is certainly near death and arguably may be dead. This is the logical equivalent of the asystolic DCDD donor prior to a neurologic determination of death. Starzl argues that to remove organs in this situation is to risk “an avoidable death.” In that same Symposium, G. P. J. Alexandre said that “I would like to make it clear that, in my opinion, there has never been and there never will be any question of taking organs from a dying person who has ‘no reasonable chance of getting better or resuming consciousness.’ The question is of taking organs from a dead person.…” (Wolstenholme and O’Connor 1966, 154). For these physicians, the supposition that death was going to independently ensue was not relevant to the wrongness of taking an action that harmed a nondead person.

These early formulations of the dead donor rule illustrate both its underlying moral standard—killing or nonbeneficially harming an innocent is wrong—and its general moral principle—the good of organ donation does not invalidate the wrongness of killing or nonbeneficially harming the innocent.¹⁵ The prohibition of removal of vital organs, including a single kidney, from a donor not certainly dead is clearly present in the earliest understandings of the dead donor rule as exemplified in the positions articulated by such transplant pioneers as Roy Calne, Thomas Starzl, and G. P. J. Alexandre.

Likewise, Anne Dalle Ave and colleagues (2019) have proposed that the concept of nonbeneficial harm to the DCDD donor is irrelevant to the application of the dead donor rule. They assert that “there is no clear way to distinguish differentially between harming a patient whose circulation has ceased permanently and harming an individual whose circulation has ceased irreversibly.”¹⁶ This presupposes that one is not willing to wait the sufficient period of time to allow irreversibility of cessation of neurologic functions. That such a time following circulatory arrest in the normothermic individual is not precisely known is true, but its range has been broadly discussed. Classic experiments in transient circulatory arrest reportedly put the upper limit for full recovery of neurologic functions at three to four minutes (Hossmann and Kleihues 1973, 375). Calne held that death by irreversibility occurred at five minutes. The President’s Commission postulated it to be ten to fifteen minutes. Kootstra applied ten minutes. The Academy of Medical Royal Colleges requires it to be at least five minutes.¹⁷ Stiegler experimentally determined it to be five to ten minutes.¹⁸

The moral judgments as to the particulars of DCDD follow. We cannot willfully reconstruct the unitary nature of death into a bifurcated structure facilitating DCDD without abrogating the extensive social discussions that established our norms for the modern determination of death and that founded the social contract of organ donation. We cannot willfully expedite the time for determination of death beyond the pale and abandon or ignore the required neurologic criteria for death without deserting the governing deontological ethic of organ donation for an ethic of utilitarian consequentialism. Robertson (1999), examining the DDR and DCDD, directly addressed the removal of vital organs from DCDD donors not certainly dead, observing that “if the dead donor rule is relaxed to facilitate organ procurement in these marginal cases, it will require a concomitant relaxation in prohibitions against physicians killing” (p. 6). And if that is what DCDD requires of us, then we should either reject the practice altogether or place it under significant constraint.

Persons as good as dead are not dead. They are persons, subject to the protections of our laws and guarded by our ethics. Their circumstances may be exceptional, but their moral standing is not. And to harm them for some purported greater good is to do much greater harm to the Good. DCDD protocols and practitioners who do not demonstrate that donors have reached a unitary death should be constrained from taking their vital organs. If we cannot be certain that these donors are dead under our current legal structures, then we should assume that they are not.

A Challenge to the Standard of Irreversibility

The early intuitive definitions of death incorporated finality—most notably as an “extinction.” As the concept was translated to pathophysiologic terms, this became a “cessation,” but adjectival modifiers were needed to insure the meaning of finality. “Permanent,” being understood as durable or lasting, was an early candidate. Taylor in ¹⁸⁷³ advised that the medical observer giving an opinion on death “should satisfy himself of the permanent cessation of the heart’s action” (p. 61; emphasis added). Writing of the effects of increased intracranial pressure, William Sharpe wrote in ¹⁹²⁰, “If it were not for the regulatory mechanism of the circulation in the medulla, such an occurrence would result in the immediate and permanent cessation of the cardiac and pulmonary activity, and, therefore, the death of a patient” (p. 51; emphasis added).

The concept of permanence was well-fitted for the preresuscitation era, when a cessation of circulatory/respiratory function not only would not but could not be reversed. This permanent cessation of circulatory/respiratory function would produce within a short-time total cessation of function of the central nervous system with complete finality. Prior to the resuscitative era, permanence was also without question irreversibility.

The Oxford English dictionary defines permanent as meaning “continuing or designed to continue indefinitely without change” while it defines irreversible as “that cannot be undone, repealed, or annulled” (Simpson and Weiner 1989). The etymology of permanent is Latin and connotes a remaining to the end while that of “irreversible” is Old French connoting an inability to bring back or to turn the other way (Onions 1966). Irreversibility ensures permanence—something that cannot be moved will not be moved, and a physiologic state that cannot be altered will not be altered. But permanence does not ensure irreversibility, and the scope of these concepts is very distinct. Irreversibility is always permanent. But permanence is not always irreversible. Permanence is conditional and in most of its forms is dependent on the intent and capacity of a causal agent or force of reversal that does not or cannot act. The only exception to this conditionality is the case in which irreversibility ensures permanence. By distinction, irreversibility is unconditional and is independent of the intent or capacity of causal agents or forces of reversal. It is dependent only on the universe of all such possible causal actions or forces, being the state which lies just beyond the boundary of that universe.

The modern era of resuscitation and life support in medicine challenged the ability of permanence to define death. It became readily apparent that some pathophysiologic states that previously were permanent could in fact be reversed—and thus, that permanence did not always equate to irreversibility in the determination of death. The universe of possible causal actions had expanded. The initial report of external defibrillation in humans by Paul Zoll and colleagues is an example on point:

Ventricular fibrillation causes an immediate cessation of circulation; it rarely stops spontaneously, and its treatment is unsatisfactory. This paper reports the successful termination of ventricular fibrillation in 4 patients by countershock applied externally across the closed chest and demonstrates that external countershock is an immediately effective, safe and clinically feasible procedure (Zoll, Linenthal, Gibson, et al. 1956, 727).

It also became apparent that resuscitative technology had cleaved the permanent cessation of circulatory/respiratory function from the irreversible cessation of neurologic function. This point was vividly made by Hannibal Hamlin in the Journal of the American Medical Association in 1964:

Heart stimulators, compact respirators, and other resuscitative devices can serve to maintain the look of life in the face of death while agonizing and expensive prolongation of false hope continues for all concerned.…We have become accustomed to gruesome examples of brain-damaged victims who, while maintained alive technically for days unto weeks, were actually heart-lung preparations, because, once in operation, the automatic respirator had to be continued until permanent cessation of dying heart action ensued. (Hamlin 1964, 113)

During this time, cessation of functions in death increasingly became characterized as irreversible. At the Ciba Symposium, Alexandre characterized the physiology of death as indicated by “irreversible damage to the central nervous system” (Wolstenholme and O’Connor 1966, 154–55). In 1968, Martin Halley and William Harvey (1968) described the “ordinary” medical definition of death as insensibility, cessation of respiration and circulation, and irreversibility. Henry Beecher and the Harvard Ad Hoc Committee transitioned from permanence to irreversibility in their report, making it clear that they were utilizing the particular subtype of permanence ensured by irreversibility in promulgating criteria for the “brain death syndrome.” Their report stated that “responsible medical opinion is ready to adopt new criteria for pronouncing death to have occurred in an individual sustaining irreversible coma as a result of permanent brain damage” (Ad Hoc Committee of the Harvard Medical School to Examine the Definition of Brain Death 1968, 339).

The President’s Commission Report in 1981 settled on irreversible rather than permanent as the adjectival modifier to define the finality of cessation of functions in death for statutory purposes. In a position that has been widely adopted, Cole (1993) maintains that, at least operationally, the UDDA really means permanent when it says irreversible. He bases this largely on the fact that the Guidelines for the Determination of Death appended to the President’s Commission Report (1981) by the medical consultants contain this statement: “Irreversibility is recognized by persistent cessation of functions during an appropriate period of observation and/or trial of therapy” (p. 162).

Citing the last clause, Cole concludes that the Guidelines interpret the construction of irreversibility adopted by the President’s Commission as a weaker construal defined by a choice not to employ therapies which might reverse the cessation. Thus, the irreversibility of cessation of functions defining death becomes a matter of our choosing—and the moment of death, now converted to a broad permanence standard, becomes explicitly situational. This construction has been seized by the transplant community in the United States in the practice of DCDD.

Defending the two- to five-minute period of observation to determine cessation of circulatory/respiratory functions in DCDD, the IOM maintains that “although this reliance on ‘permanent’ loss of function may seem like a shift from a strict notion of ‘irreversibility’ it is a reasonable interpretation of the concept of ‘irreversibility’ and is compatible with the probable intentions of the President’s Commission that formulated the UDDA definition.…” (Childress, Liverman, and the Institute of Medicine 2006, 146). Bernat (2010), while maintaining that strict irreversibility is necessary for neurologic determination of death, has proposed that permanent cessation of circulatory and respiratory functions is “a perfect surrogate indicator for irreversibility” in declaration of death by circulatory/respiratory criteria, conforming to the UDDA and derivative state statutes, thereby operationally validating DCDD (p. 247).

Likewise, in 2010, a panel of experts convened and funded by the Health Resources and Services Administration of the US Department of Health and Human Services concluded that,

It is ethically and legally appropriate to procure organs when permanent cessation (will not return) of circulation and respiration has occurred but before irreversible cessation (cannot return) has occurred because permanent cessation: 1) is an established medical practice standard for determining death; 2) is the meaning of “irreversible” in the Uniform Determination of Death Act; and 3) does not violate the “Dead Donor Rule.” (Bernat et al. 2010, 963)

That is probably not the case. I have raised concerns regarding the dead donor rule above. Regarding established medical practice, as previously noted, the President’s Commission used the obvious and sufficient conditional to insure the permanent and irreversible loss of functions of the central nervous system as a necessary standard for the irreversibility of cessation of circulatory and respiratory functions. Thus, the observation period in the Guidelines is temporally that of traditional death and not that of the hurried death of DCDD. Likewise, the established standard in medical practice is obvious and sufficient rather than “a justified violation.”

Several points are pertinent as to the intent of the UDDA. The President’s Commission held that the concept of irreversibility should be uniformly applied in determining cessation of both cardiopulmonary and neurologic functions (The President’s Commission Report 1981, 76). Thus, its detailed discussion of the standards applied to the neurologic issues is applicable to a modern reexamination of circulatory/respiratory issues provoked by DCDD. The President’s Commission noted that “temporary loss of blood flow (ischemia) becomes a permanent cessation because of the damage it inflicts on the brain” (The President’s Commission Report 1981, 74). This is not a brief interlude in function, capable of reversal. It is pathophysiologic damage to the organ resulting in a cessation of function that will persist and that cannot be undone. It is irreversibility, not broader permanence.

The President’s Commission also definitionally seems to have conceived irreversibility in its strictest sense as falling outside the universe of possible causal actions or forces of reversal. In elaborating on the term “irreversible” as used in the construction of the UDDA statute, the President’s Commission observed that

Any decision to recognize “the end” is inevitably restricted by the limits of available medical knowledge and techniques. Since “irreversibility” adjusts to the times the proposed statute can incorporate new clinical capabilities. Many patients declared dead fifty years ago because of heart failure would have not experienced an “irreversible cessation of circulatory and respiratory functions” in the hands of a modern hospital. (The Presdient’s Commission Report 1981, 76; emphasis in original).

This is a discussion of a narrowly drawn concept of permanence manifesting irreversibility. It is not a discussion of irreversibility manifesting a broad concept of permanence.

In the UDDA and in many jurisdictions throughout the world, irreversibility is a necessary condition for cessation of functions defining death. Irreversibility is not permanence and is a strict standard. Morphing irreversibility into permanence subverts the express language and intent of the law and undermines the established social contract of organ donation.

However, the British Transplantation Society in its 2013 guideline “Transplantation from Deceased Donors after Circulatory Death,” while requiring documentation of loss of neurologic functions for the determination of death, expressly applied a permanence standard to that determination:

Death is in essence a neurological event and occurs when there is a permanent loss of the capacity for consciousness [and] all brain stem function. In this context, “permanent” refers to loss of function that cannot be restored spontaneously and which will not be restored artificially (p. 26).

The rewrite of the policies of the OPTN in 2014 changed the language concerning the declaration of death to implicitly accommodate a weakening of the concept of strict irreversibility to that of broader permanence. OPTN policy language in ²⁰¹³ stated that

Declaration of death must not occur until after both of the following:

• 1. The patient has an irreversible cessation of circulatory and respiratory functions

• 2. A sufficient time has passed, as defined by hospital policy.” (p. 35; emphasis added)

This policy language mirrored the obvious and sufficient standard for irreversibility adopted by the President’s Commission Report. It was replaced by the OPTN in 2014 with the following:

Organ recovery will only proceed after circulatory death is determined, inclusive of a predetermined waiting period of circulatory cessation to ensure no auto-resuscitation occurs.…Circulatory death is death defined as the irreversible cessation of circulatory and respiratory functions. Death is declared in accordance with hospital policy and applicable state and local statutes or regulation. (OPTN 2019, 34)

This language moved the OPTN to the autoresuscitation criteria for irreversibility as in the Pittsburgh Protocol, encompassing a concept of broad permanence and allowing short intervals of time to the pronouncement of circulatory death and the retrieval incision.

A 2014 international forum sponsored by Health Canada and Canadian Blood Services and in collaboration with the World Health Organization has proposed an operational definition of death centered on permanence and based on biologic and clinical factors. This definition provides that

Death is the permanent loss of capacity for consciousness and all brainstem functions. This may result from permanent cessation of circulation or catastrophic brain injury. In the context of death determination, “permanent” refers to loss of function that cannot resume spontaneously and will not be restored through intervention. (Shemie et al. 2014, 795)

These policies and proposals formalize a challenge to irreversibility as the standard for the determination of death. But their evaluation and acceptance is a matter of social, and not just medical or scientific, concern and consideration.

Since inception, deceased donor organ transplantation has rested upon a social contract forged upon the fundamental understanding that the removal of organs would be from a person certainly dead, that the certainty of death rests on a strict irreversibility standard, and that the interests of persons other than the donor would not enter into the conduct of the organ donation process. That social contract was reached and actuated through a political process in which legislative initiatives such as the Uniform Anatomical Gift Act were debated in a representative democratic structure.¹⁹ For permanence to replace irreversibility as the standard for cessation of functions in death, then society should have an honest and forthright political discussion on that point, with benefit of full public disclosure and a transparent public debate. As that discussion unfolds, those who wish a variable utilitarian ethos will be met in the public arena by those who deontologically hold that the determination of death is best reached by a clear, strict, and uniform irreversibility standard, that the interests of the donor as a person are paramount, and that no interest of organ recipients or of the greater society can justify negation of the rights and bodily integrity of the person who is a donor, nor conversion of the altruism of giving into the calculus of taking.

Conclusion

The classic intuitive unitary concept of death faced challenges as modern medicine cleaved the support of cardiorespiratory functions from the irreversible cessation of neurologic function. The UDDA conceptually applied a singular unitary structure of death with both circulatory and neurologic criteria. The practice of DCDD has challenged prior understandings of the nature of death by questioning traditional concepts of the time to determination of death, the unitary nature of death, the dead donor rule, and the irreversibility standard in determination of death.

In the United States, provisions of the UDDA have been widely misunderstood and misapplied, fostering concepts of death in a bifurcated structure. The time to determination of death has been expedited in DCDD practice to a point that raises questions as to whether the donors are certainly dead at the time of the retrieval incision. These practices rest in part on a departure from the unitary concept of death, a violation of the dead donor rule, and a challenge to the standard of irreversibility. Abandoning the irreversibility standard is not a matter for decision by the scientific and medical communities in isolation. Rather, any reconsideration must entail a broad societal examination of these issues through full public disclosure and a transparent public debate within the political process, analogous to the process originally followed in addressing matters pertaining to the definition and determination of death.

Biographical Note

Frederick J. White III, MD, practices cardiology in Shreveport, Louisiana. He is certified by the American Board of Internal Medicine in both internal medicine and cardiovascular diseases. He is a fellow of the American College of Cardiology and the American College of Chest Physicians. He is Past Chair of the Institutional Ethics Committee of the Willis-Knighton Health System, having served in that capacity for twenty years.