Show Summary Details
Page of

Critics and Brain Death 

Critics and Brain Death
Chapter:
Critics and Brain Death
Author(s):

Eelco F.M. Wijdicks

DOI:
10.1093/med/9780190662493.003.0005
Page of

PRINTED FROM OXFORD MEDICINE ONLINE (www.oxfordmedicine.com). © Oxford University Press, 2016. All Rights Reserved. Under the terms of the licence agreement, an individual user may print out a PDF of a single chapter of a title in Oxford Medicine Online for personal use (for details see Privacy Policy and Legal Notice).

date: 12 November 2018

Well-meaning physicians and healthcare workers will face criticism and may have to address challenges to their professional opinions. With matters of death, there has to be a binary position: the person is dead or not. For some scholars, the whole notion of brain death does not seem right. Even after nearly half a century of clinical practice in pronouncing brain death in numerous countries, bioethicists and theologians—but also some physicians—have published essays espousing opposing positions and questioning the accuracy of the entire concept.17,21,40,47,48

It may be difficult to understand why such criticism exists and what drives the persistent motivation to emphasize the supposed fallacies of brain death—a neurological condition that, for neurologists and neurosurgeons practicing in intensive care units (ICUs), is an accepted certitude and death. The main philosophy that sustains the critique is often a pro–sanctity-of-life position. Some critics are troubled by the practice of organ retrieval for organ transplantation. Even more blatantly, some have stated that organ donation is a form of physician-assisted death and have insinuated that the involvement of organ procurement coordinators may change (“erode”) the care of the potential donor and even “influence” compliance with practice guidelines and raise “doubt about the accuracy of the diagnosis”.52 These critics believe that physicians have simply convinced themselves and families that brain dead is dead, whereas in fact, patients have only lost consciousness, are alive, and are not even supported with complex means. The prevailing argument for those who object is that all three bodily systems—cardiovascular, respiratory, and nervous system56,59,72—must be destroyed for death to occur.

The responses to these problematic critiques have been appropriately muted and studiously vague, but—although it is tempting—no one has argued that these opinions should not be given a forum or that discussion of the alleged controversy is unworthy of the effort. Some have insisted that definition of death is not a scientific question but a social one and that families should be given a choice.71 However, this book avoids a discussion of whether ethicists should decide public or medical policy. Opinions of philosophers and bioethicists can be found elsewhere.23,31,47,48,70,71,77 Physicians who oppose the concept of brain death15,29,56,61 and participate in the diagnosis of brain death and all its ramifications, including family support, should be taken seriously. This chapter therefore concentrates on their viewpoints and motivations.

The Uncertainty of Death

Even before bioethicists criticized the concept of brain death—in particular, the medical decision of equating it with death—many physicians struggled with the certainty of the clinical signs of death.14 For centuries, books published in Europe questioned the certitude of death (Figure 5.1), and fear of premature burial. Putrefaction after a “death watch” was considered the only infallible sign of death.

Figure 5.1 Cover page of the 1746 London edition of anatomist Jacques-Bénigne Winslow’s thesis suggesting people were at risk of being buried alive.

Figure 5.1 Cover page of the 1746 London edition of anatomist Jacques-Bénigne Winslow’s thesis suggesting people were at risk of being buried alive.

In the twentieth century, signs of death were not initially a topic of controversy, but they became more closely scrutinized with the arrival of organ transplantation. The early transplants that took place in the late 1960s were cadaver transplants, and an arbitrary period (allegedly several minutes) of cardiac arrest was allowed before kidney, heart, and liver recovery proceeded. (For example, in Christian Barnard’s first heart transplant, after withdrawal of ventilation and cardiorespiratory arrest for 5 minutes, a forensic pathologist was called into the operating room to declare the donor dead.5) The required period of cessation of respiration and circulation in order to determine death has remained a topic of debate ever since.

The need to identify correctly the moment of irreversibility of respiratory and circulatory arrest became less urgent when organ donation became linked to brain death determination. With a rekindling of the practice of donation after cardiac or circulatory death (DCD), prompted by a growing and substantial shortage of organs, an accurate definition of the signs of irreversible circulation was warranted.

Modern medicine and the emergence of critical care medicine changed the equation, and hospital patients now could die in three different ways. Respiratory arrest led irrevocably to hypoxemia, hypotension, circulatory arrest, and cardiac asystole. Cardiac arrest led to circulatory arrest and apnea. In both circumstances, the brain injury would be immediately severe with brain function irretrievably compromised. In another clinical scenario, catastrophic brain injury with lost brainstem function would lead to respiratory arrest followed by circulatory and cardiac standstill. The irreversibility of lost brain function was easily accepted; the irreversibility of respiratory and circulatory arrest was not.38

These clinical determinations quickly led to controversy. First, autoresuscitation, or resumption of circulation, seen as long as 30 minutes after the patient was declared dead, was occasionally observed. The explanation for this phenomenon (also known as the Lazarus phenomenon) has remained unclear and has been attributed to the delayed action of intravenous epinephrine or increased venous return after ventilation is discontinued. This event has been noted exclusively after cardiopulmonary resuscitation in adults. It is an exceedingly rare occurrence, transient and largely irrelevant clinically, with no patient surviving long term.24

Second, extracorporeal membrane oxygenation (ECMO) could replace circulation and oxygenation in a patient previously declared dead to preserve organs used for donation.52 Some have even suggested that, in these patients, ECMO may restore brain circulation and consciousness, and they provocatively surmise that the patient may in fact become aware and in severe distress.10 The basic reality is that this scenario is wholly implausible due to irreversible brain injury,46 but such a misdirected representation perfectly captures some of the ongoing discussion.

Third, as in discussions of brain death, new terminology and language in DCD protocols are often unclear and mostly very confusing. Examples include mechanical asystole, permanent versus irreversible cessation, cardiocirculatory death, and circulatory-respiratory determination of death.22

The debate intensified after two hearts from severely injured (but not brain-dead) newborns were successfully transplanted after 85 seconds of circulatory arrest.15 This apparent contradiction—nonfunctioning organs in dead bodies functioning in living bodies—fueled a new discussion of what constitutes death. In Veatch’s words, cardiac donation in DCD was “reversing the irreversible.”67 Bernat correctly suggested rewording the C in DCD as circulatory, in line with the Uniform Determination of Death Act (UDDA) statute that defined death as “irreversible cessation of circulatory and respiratory functions.”10 So, it was distinctly pointed out that cardiac death involved permanent respiratory and circulatory arrest, not the loss of cardiac function.

An equally debatable definition of death is to decide on irreversibility as a result of a medical choice not to resuscitate. Thus, a patient with 2 minutes of circulatory and respiratory arrest is dead when not resuscitated and alive if circulation can be restored. It is easy to appreciate that placing the threshold at several minutes may blur the distinction between irreversible and reversible circulatory arrest.63,64

Anyone observing a DCD protocol in the operating room would have no difficulty pronouncing death in a cyanotic and apneic patient who became pulseless in a matter of minutes and was observed for several additional minutes. The time to permanent cessation of respiration and circulation has been set at 2 to 5 minutes; however, this standard may not satisfy critics, and the discussion will likely continue until—at least for them—a better evidentiary basis is available. DCD protocols are currently used in several countries but have remained contentious in many others (see Chapter 6).

Most recently, Truog, a prominent ethicist and anesthesiologist, advocated abandonment of the dead-donor rule in transplantation, which states that the patient must be dead before organs can be recovered. His arguments, along with those of bioethicist Miller, are well outlined in a recently published book.40 Truog has hardened his position that all deaths (diagnosed by physicians in hospitals) are more or less undefinable, and he considers brain death legal fiction (or, more recently, “a useful fiction”) and a utilitarian attempt to facilitate organ donation. This stance has resulted in numerous rebuttals, which run the gamut from mild criticism (“overdoing it”50) to strong denunciation (“a future of moral and legal chaos”1 and problems for the public needing “reassurance of the dead-donor rule”6). Others rose to their defense, stating that, with valid consent, patients cannot be “harmed or wronged.”12 In the end, the question will remain as to whether it is socially, morally, medically, or legally acceptable to recover organs for transplantation in a person not declared dead, and it is very likely that the arguments of the proponents of the dead-donor rule will prevail. Veath, a fervent opponent of the brain death concept, calls it “killing by organ procurement” and concludes that its implementation is nearly impossible.68 Health insurance plans would continue to pay for brain-dead patients, and laws would permit physicians to proceed with organ removal (using additional sedation), which may be seen as a physician-assisted suicide. I cannot imagine a single surgeon who would want to do that. The fact remains that misdiagnoses of irreversible brain injury may occur more often than we think (or hope for), and these errors—taking out organs in patients who may recover—would be inexplicable to the public. A recent survey on public opinion suggests that the American public would support organ donation even if it caused death of the person in irreversible coma, but survey questions based on a single vignette often trivialize complex matters and are inherently confusing for participants.43

Emerging Controversies

The clinical diagnosis of brain death became controversial in the United States in the years after publication of the Harvard criteria (see Chapter 1), and most of the debate has remained in this country. The themes have changed, ranging from objection to the workings of the Harvard Ad Hoc Committee (see Chapter 1) to lack of prospective data.

With publication of the Harvard criteria, most of the objection was directed toward the makeup of the committee. The presence of a transplant surgeon and a transplant nephrologist was considered indicative of a conflict of interest.77 This early objection concerning a potential conflict of interest continued to resurface and (incorrectly) implied that transplant organizations had a hidden agenda. Such was the interpretation; that is, legally declaring a patient brain dead would greatly facilitate transplantation, particularly cardiac transplantation, and remove any legal challenge to the surgeon.

Dissatisfaction with the term brain death was also noted. This term was first suggested by Schwab and colleagues, in a paper on the role of EEG,54 followed by the Harvard Ad Hoc Committee’s use first as brain death syndrome and later as a subtitle of the major document (see Chapter 1). Brain death became a deeply anchored medical term and replaced irreversible coma, largely to allow a distinction from persistent vegetative state. Others used the term cerebral death to indicate cessation of function of the hemispheres73 or dissociated death to emphasize death of the brain and the living heart.36

In like-minded critics, brain death implied death of the brain and all its functioning neurons. Assuming that the brain cannot be entirely dead, other terms would better reflect the pathophysiology. Some have suggested eliminating the word death in brain death. Therefore, total brain failure has been suggested (most recently by the President’s Council on Bioethics) to better describe a lack of brain function.1 Brain arrest was also introduced, presumably to provide a complementary term to cardiac arrest.55 Other terms (e.g., the aperceptivity, areactive, apathic and atonic syndrome32) are lengthy and less distinctive (e.g., status deanimatus,36 total brain infarction,25 irreversible apneic coma,78 mortal brain damage21). Death by neurological criteria is also long, too descriptive for a diagnosis, eliminates the word brain, requires understanding of the lay public of the neurology specialty, and allows consideration of terminology based on endless other biological criteria (e.g., death by mitochondrial criteria). However, apart from the often comical bickering (Figure 5.2) over the right terminology and knowing that brain death terminology is often distinction without a difference, the major issue is whether a person is dead when the brain irreversibly stops functioning.

Figure 5.2 Cartoon depicting terms for the same neurological condition.

Figure 5.2 Cartoon depicting terms for the same neurological condition.

The definition of death as “death of the whole brain” by the President’s Commission (see Chapter 1) may, in retrospect, have been unsatisfactory. To contrast whole brain death with other conditions, two other formulations of brain death were introduced: higher brain death or brainstem death. The controversy began in reference to the word whole.

Whole-brain criteria implied that the hemispheres, brainstem, and cerebellum must be all dead. Absent neuronal function may have to be demonstrated by additional ancillary tests showing encephalographic silence or absence of cerebral blood flow. Failure to find supportive documentation would deny such a conclusion.

Korein interpreted death by neurological criteria as failure of a “critical vital system” that leads to a state of greater disorder and entropy.34,35 Bernat defined death as “the permanent cessation of the critical organism as a whole” and emphasized loss of functional integrity of an organism, similar to Korein in earlier manuscripts.9,11 In a 1981 article authored with a psychiatrist, Charles Culver, and a philosopher, Bernard Gert, neurologist Bernat emphasized “the irreversible cessation of total brain function,” replacing the word whole with the word total.11 Use of the terms critical and whole or total has resulted in numerous papers by bioethicists.

The higher brain criteria of death include a permanently comatose state (e.g., spontaneously breathing patients in a persistent vegetative state). Many scholars argue that absence of hemispheric function is more or less the philosophical equivalent to the absence of hemispheric and brainstem function. The higher brain criterion argues that personal identity is essential for a human organism; when personal identity is absent, the person ceases to exist.37,42,56,66,69,70

The brainstem formulation of death implies that without a functioning brainstem, the person is irreversibly unconscious and apneic. The formulation of brainstem death is largely pragmatic. In Pallis’ words, “Brainstem death is the physiologic kernel of brain death, the anatomical substratum of its cardinal signs (apneic coma with absent brainstem signs).”44,45 The line of thinking here—and the most scientifically convincing one—is that the brainstem in evolutionary biology has been the major structure preceding the development of the neocortex (see Chapter 3). When clinical examination in a comatose patient without confounders shows absence of brainstem reflexes and apnea, the presence of normal brain tissue somewhere in a non-functional, otherwise destroyed brain is not relevant. Brainstem formulation of death stipulates that the brainstem is, in fact, an indispensably necessary system and not just part of a group of important neuronal systems.

As expected, therefore, most of the earlier arguments in the 1970s and 1980s against brain death concentrated on finding ways to show that the whole brain is not dead and, thus, that the person has not died. Over the years, multiple scholarly publications and a number of textbooks representing diverse specialties have appeared. The many other arguments further developed in this chapter are summarized in Table 5.1.17,19,21,26,29,33,56,57,66,78

Table 5.1 MAIN CRITIQUES AGAINST BRAIN DEATH BY PHYSICIANS

Author

Specialty

Critique

Byrne17

Pediatrician

  • No consensus; multiple criteria; brain death by one but not by another

  • The brain may be “stunned,” not dead.

  • There is no valid science.

  • The Harvard Committee had an agenda.

Evans20,21

Cardiologist

  • There are too many protocols, indicating that brain death is not a scientifically based entity.

  • Tests in the United Kingdom (brainstem only) are insufficient.

  • There is no test of cranial nerves I and II (“patient is in a visual nightmare”).

  • A sufficient criterion could only be no blood/oxygen to the entire brain for a considerable amount of time.

Coimbra19

Neurologist

  • The apnea test is unethical (because it is dangerous), and hypercapnia-acidosis may cause cerebral vasoconstriction. Hypoxemia during the test may cause further necrosis.

Shewmon56,57,58

Pediatric neurologist

  • The body may remain alive without brain function, and there is no cardiac arrest in several cases.

Joffe26,27,28,29,30

Pediatric intensivist

  • “Recovery” of brain function has been reported.

Rady (intensivist) and Verheijde (physical therapist and bioethicist) have written over 100 letters to the editor in response to nearly every paper published on the topic requiring authors to rebut their claims. Recently, they perplexingly suggested to “validate a reversibility timeline” in brain death.51,52 As alluded to earlier, Truog and Miller—who seem to embrace death as a intangible medical mystery—suggested “changing the conversation about brain death” but offered no new arguments to supplement the ones summarized in this chapter.62,65 In discussions on the alleged shortcomings of the concept of brain death, the absence of neurointensivists and neurosurgeons is telling.

In the critiques, significant attention has been directed to a possible presence of integrated neuroendocrine function. Some early studies (but not later ones) found no evidence of diabetes insipidus and no evidence of a deficiency of pituitary hormones such as prolactin, human growth hormone, luteinizing hormone, and thyrotropin (thyroid-stimulating hormone), all suggesting an intact hypothalamus and pituitary axis despite absence of flow to the brain on a cerebral angiogram.4

Other critics could not live with the idea that, in a considerable proportion of patients, electroencephalographic activity remained, suggesting in their minds important neuronal function. In other patients, uptake of radioactive material found on cerebral blood flow studies was preserved in several areas of the brain. Cerebral angiograms could document flow in the posterior circulation and slow flow beyond the siphon, providing blood to many areas of the brain that were supposedly dead.

Several physicians maintain a strong opposing voice. Paul Byrne, a neonatologist and past president of the Catholic Medical Association, has lectured extensively against clinical testing for brain death and against organ transplantation.17 Byrne’s main arguments are that (1) spontaneous movements cannot be spinal reflexes and, thus, are not compatible with death; (2) the apnea test causes more brain swelling due to acidosis and hypercarbia; (3) recovery of patients occurs when an apnea test is not performed; (4) the appearance of brain death is different from the appearance of a corpse; (5) the heart rate and blood pressure increase during recovery of organs, implying a response of a living patient; and (6) organ donation is “legal killing of vulnerable patients” or “defenseless, comatose patients,” and therefore, all organ donation in brain-dead patients should be rejected. In a paper coauthored with cardiologist Weaver entitled “ ‘Brain Death’ Is Not Death,” Byrne claims that the observed loss of brain function could in fact be only “stunning” of brain tissue. The authors also suggest that procurement may prevent recovery of the brain.17

Karakatsanis, a nuclear medicine physician, has formulated four more or less similar arguments against brain death.33 The arguments are, again, against the concept of complete and total brain destruction. First, the spinal reflexes could well be generated from the brainstem and not the cervical or thoracic cord. These movements cannot be clinically distinguished from movements seen in brainstem injury and are never seen in patients with an acute cervical spinal cord lesion, suggesting that these movements are generated from intact (or perhaps partly intact) diencephalon and brainstem. Second, physicians are unable to test the neocortex clinically because all reflexes go through the brainstem and the brainstem reflexes are absent. Patients may be “locked in” and cannot express themselves. Third, activity suggesting intact neurons is present on many electrophysiological tests and blood-flow studies. Fourth, often the posterior circulation perfusing the brainstem is intact, and pathological studies have shown no changes in the brainstem.

These arguments lingered for years, but the controversy over brain death became definitively more interesting after Shewmon, a pediatric neurologist, published a provocative paper titled “Chronic ‘Brain Death’.”57 In the paper, he gathered 56 previously published documented cases of survival lasting 1 week or more. Cardiac arrest in other cases was presumed to be due to associated systemic injury to major vital organs (i.e., severe, traumatic brain injury leading to sympathetic storm or disseminated intravascular coagulation) rather than a direct consequence of brain death. These examples of prolonged support in persons after brain death occurred because of certain religious practices, because of pregnancy, and because physicians were capitulating to the demands of family members who refused to accept the death of a loved one.

Shewmon’s charge has been fundamental. Patients who have fulfilled the clinical criteria of brain death do not necessarily progress to what he called “somatic disintegration.” The full panoply of modern life-prolonging machinery may not be needed for stabilization of the rest of the body. These integrative functions—observed in two personal cases—included wound healing, fighting off infection, development of a febrile response to infection, maturation in children, and improvement in clinical condition (withdrawal of vasopressors).

Shewmon concludes,

The phenomenon of chronic brain death implies that the body’s integrative unity derives from mutual interaction among its parts, not from a top-down imposition of one ‘critical’ organ upon an otherwise mere bag of organs and tissues. If brain death is to be equated with human death, therefore, it must be on some basis more plausible than that the body is dead.57

Shewmon credited his recent conversion to theism as being responsible for his change in position and his moral obligation to speak out, but his long-standing rejection of brain death seems to predate this. His earlier writings, for example, include an article on a mathematical calculation on the impossibility of validating criteria for brain death.56

His definition of brain death is deep coma in a dying patient but not death. He has made the following statement:

[A]‌ probable valid criterion close to the mode of death might be something like cessation of circulation of blood for a sufficient time, depending on blood temperature, depending on body temperature, to produce irreversible damage to a critical number of organs and tissue throughout the body so that irrevocable process of disintegration has begun. At normothermia, the minimum sufficient time is probably somewhere around 20 minutes, although there is insufficient data to support the precise duration with certainty. I do not believe that the critical number of organs and tissues can be universally specified as it will no doubt vary from case to case. Surely the brain is included but not only the brain.56

Thus, the view expressed is that the ICU can be seen as “the surrogate brain stem.”61 If we are able to maintain integrated somatic function for many months, critics claim, the ICU treatment (ventilator, vasopressors, vasopressin, and nutrition) maintains life.

The controversy has continued, with the critics challenging the defenders. Among the defenders of brain death are a few spokespersons who have tried to debunk the critics,8 only to leave open the discussion of why the defense is not good enough. None of the critics feel that any of the arguments presented are sufficient to change their minds. Subsequently, Shewmon stated that the defenders have an “apologetic task” and should explain why they still feel that brain death is death.6

Joffe, a pediatric intensivist, recently emerged as another critic of the clinical state of brain death by publishing a series of provocative articles.26,27,28,29 In one commentary, he summarized the inadequate defenses of the brain death concept.28 This was buttressed by a recent survey of neurosurgeons and pediatric intensivists in Canada.29 Approximately one-third of the physicians surveyed would continue life support if the family insisted on it for a patient who met the clinical criteria of brain death. In addition, the survey exposed lack of understanding among physicians concerning the concept of brain death. When asked whether brain death and cardiac death were the same, 45% of Canadian neurosurgeons answered no, meaning that they did not consider both to signify the death of a patient. Joffe also criticized prior statements, particularly by Bernat, saying that brain death might be a “compromise or approximation” in order to maintain public confidence in organ procurement. Joffe also pointed out that if brain death is the loss of brain function in the entire brain, including the brainstem, he has great difficulty accepting that 20% of patients have EEG activity, 50% have evidence of hypothalamic function, and none have evidence of excessive brain destruction in many areas of the brain. Finally—and most provocatively—Joffe and colleagues published the case of a newborn diagnosed as brain dead who developed “hiccups” that were interpreted as return of a respiratory drive. (The examination was markedly confounded by the prior use of sedatives.) In addition, Joffe claimed to have identified cases of “recoveries,” but he acknowledged that the examinations in the published articles were incomplete.30

In 2008, a white paper by the President’s Council on Bioethics was published (Figure 5.3).1 This Council was chaired by Edmond Pellegrino, emeritus professor of medicine and medical ethics. It consisted mostly of professors of medical ethics law, social and political ethics, metaphysics, political economy, government, and international studies, among other fields. One pediatric neurosurgeon and one neurologist participated. The Council invited Shewmon to present his case. He introduced his presentation with multiple examples alleging that even experts in this area write confusing texts, claiming that some use the word comatose when referring to brain death (implying a living organism) and others use the term mode of death when writing about brain death, also suggesting that another event is needed to die. Shewmon also compared the clinical manifestations of acute spinal cord transection and bilateral vagotomy with the clinical manifestations of brain death, showing that the only difference is the presence of consciousness and thus arguing that the systemic manifestations in brain death are not sufficiently discriminatory.58 Moreover, his prior examples of prolonged support suggested that the body is integrated with the ability to survive with support and recover from intermittent illnesses such as infections. In his opinion, one could only conclude that these are living organisms.

Figure 5.3 White paper by the President’s Council on Bioethics (2008).

Figure 5.3 White paper by the President’s Council on Bioethics (2008).

The Council used his arguments to formulate a divided conclusion: “The Council has concluded that the neurological standard remains valid. A few Council members argue that there is sufficient uncertainty about the neurologic standard to warrant an alternative approach to the ‘brain dead’ human being and the question of organ procurement.” The Council further concluded that “if there are no signs of consciousness and if spontaneous breathing is absent and if the clinical judgment is that these neurophysiological facts cannot be reversed … a once living patient has now died.”1 The white paper also included three personal statements (including that of the chairman of the Council) that disagreed with the final letter. In a critique of the Council’s manuscript, Shewmon bluntly stated that the time had come to add a footnote to signing a donor card and he suggested the following language: “Warning: It remains controversial whether you will actually be dead at the time of removal of your organs… . You should study the President’s Council on Bioethics white paper carefully and decide for yourself before signing an organ donor card.”56

The Council was abruptly dissolved by the Obama administration. The Council accepted the dismissal, but speculation abounds that its bias may have played a role. (The Council had just prepared a document on “the ethics of transplantation” but the document was not finalized before dismissal.)

In sum, the selection and interpretation of single cases by several critics and focusing on a few inconsistencies may succeed in creating doubt. Certain organizational bodies may be persuaded, and the issue can become a matter of debate. Then, if the defenders are unconvincing, or worse, ambiguous, in their answers, critics will argue that both positions (supporting vs. opposing) must be taken into account and allowed to participate in the discussion on this topic. And so a “controversy” emerges.

Critique

There is no disagreement that brain death is a separate clinical neurological state. The clinical findings in brain death are different from those in any other comatose patients. Brain death has been understood medically as loss of all brain function, and its unique clinical presentation—an apneic comatose, poikilothermic, polyuric, and hypotensive patient with no brainstem reflexes—is what physicians diagnose. It is impossible to have a better medical standard. (For those who seek technology, functional magnetic resonance imaging—perhaps the closest test showing activation of the brain—shows the absence of functional connectivity.13) Brain death is unsustainable. Patients who meet the criteria of brain death would, without any further intensive care support, de facto progress to hemodynamic collapse, and cardiac standstill.

Brain death can be reliably diagnosed, and when it is present, the findings are irreversible in adults. All “recovered” cases reported in the literature—recently compiled by Joffe—are suspect (due to the presence of confounders) or incomplete (with no detailed description of testing and no mention of the apnea test). To claim that the brain is “stunned” is a grave misreading of the neurobiology of a catastrophic injury.17 Brain death has a sound physiological basis and is mostly the end stage of destruction of the thalamus, mesencephalon, pons, and medulla oblongata, in that order. To claim that the apnea test causes further brain injury (hypercarbia causes a rise in intracranial pressure [ICP]) ignores the absence of cerebral autoregulation with this degree of injury and also ignores the significantly elevated ICP that led to brain death in the first place.19 Hypoxemia resulting in additional brain injury could theoretically occur with a poorly performed apnea test, but our findings argue otherwise. In a correctly performed apnea test, the opposite is true, and hyperoxemia is a common finding at the completion of the test.76 Others are concerned that the apnea test causes CO2 narcosis, but such a statement minimizes the true extent of the brain injury when apnea testing is performed (usually after all brainstem reflexes are absent in an apneic patient).60

The repeated claim that patients “squirm” (Byrne’s term17) during organ recovery and develop tachycardia and hypertension at the time of recovery is false and is not seen by experienced transplant surgeons. Anesthesia is never used, but neuromuscular-blocking agents are used in some instances to relax the abdominal musculature in order to assess the organs for procurement.

Long-term hemodynamic support of brain-dead patients for weeks is not feasible; the overwhelming majority of cases show a hemodynamic instability or relentless progressive decline in blood pressures despite increase in vasopressors. If brain death diagnosis takes too long, patients are lost for organ procurement as a result of circulatory arrest (Chapter 7).

How can this possibly agree with Shewmon’s case of prolonged support? It is therefore important to summarize the breakdown of the cases cited.56 The 56 cases of prolonged support consisted of 28 cases from four series of patients with brain death (from a total of 143 cases) and 28 isolated cases from letters to the editor, case reports, and newspaper articles. Of the latter 28 isolated cases, 15 involved a “brain-dead” pregnant mother. Imprecision in the study sample is introduced by excluding all reportedly brain-dead patients in whom cardiac arrest developed within 1 week.

These cases almost certainly represent incomplete brain death determinations. First, in only 2 of the 56 cases were apnea tests done, with documentation of absent respiratory effort at a PaCO2 of 60 mm Hg. Most cases included brief (minutes) disconnection of the ventilator alone. Second, many cases did not have sufficiently documented details of the neurological examination, coughing to tracheal suctioning was not mentioned, and examination of the patients by at least one neurologist was inconsistent. Most disturbingly, the cited material provided with the paper included a neurosurgeon’s telling note: “We knew she was brain dead but we did not do any tests to formally establish this because a death certificate would have to be completed. We were conscious of the stigma attached to a child born to a dead mother.” The questionable literature associated with prolonged support of maternal death is further discussed in Chapter 7, and I have not come across a single convincing case of successful prolonged support.49 To illustrate this further, a case of a “brain-dead” adult patient with 5½ months of successful support has recently been published.39 The accuracy in reporting of the case is questionable because of failure to perform the apnea test. (The case demonstrates the challenges that physicians in Japan face with continuous threat of criminal charges when the ventilator is removed.39) The apnea test remains an important test, not because it assesses lack of a breathing drive, but because it is an indicator of significant medulla-pontine injury; conversely, patients who have a persistent breathing drive almost always have hemodynamic stability.

Most of this new argument (i.e., lack of top-down function of the brain and largely autonomic, coordinated multisystem organ function) is based on the extraordinary Repertinger case. Repertinger and associates, from the Department of Pathology at Creighton University Medical Center, published a pathology report of a 4½-year-old boy with a fulminant Hemophilus influenzae type B meningitis.53 Few details are provided about his medulla oblongata function and breathing drive. The boy was able to survive without vasopressors, resulting in maturation to adulthood. At autopsy, a calcified and mummified brain was found with no recognizable neurons. Unfortunately, the cervical cord was not examined, leaving open the possibility that the cervical medullary junction and medulla oblongata were not subjected to microscopy. One is inclined not to accept this case as meeting the criteria of brain death. (In my experience I have seen patients finally declare themselves with a sudden need for multiple vasopressors and new apnea—even after a considerable time interval.)

The more recent case of 13-year-old Jahi McMath bolsters even more the argument that brain-dead patients can be supported for a prolonged time.16 (The legal issues are described in Chapter 7.) The clinical diagnosis of brain death and the procedure used were not in question and seemed appropriately documented with additional “confirmation” by isoelectric EEG and a nuclear scan. She was moved to a long-term care facility, where she showed movements of hands and feet to commands.

At the request of the plaintiff attorney Dolan, both Alan Shewman and Calixto Machado declared she was not brain dead (“a very much alive teenage girl”).2,3 Shewman interpreted the findings (video interpretation) as proof of a recovering brain-dead patient. Dr. Machado expressed concern that the brain was not “liquefied” and the heart rate variability showed a response to the voice of her mother. (A state appellate court ruled in July 2016 that the child’s mother may try to prove she is alive. If the court rules Jahi is alive, the family could sue the hospital for millions of dollars, but they would be limited to a wrongful-death lawsuit capped at $250,000 if she was ruled dead.)

These two cases may suggest (1) that errors were made and (2) that in exceptional circumstances, blood pressures are supported by a sympathetic overdrive from the spinal cord. (It has been know for decades that visceral stimulation in a decapitated animal can produce significant rises in a blood pressure.) A few remaining dorsal-caudal medulla pressure neurons may cause perfusing pressures, which would not be impossible in a scenario where anoxic-ischemic injury played a role. However, without full access to medical records and with contradictory statements by physicians, it is difficult to judge any of this, and it evokes memories of the Schiavo case, in which physicians made assessments on the basis of family-provided videotapes. So it begs the question as to why these cases are unforeseen and whether we can supposedly “minimally” support patients who are physically brain dead. Without prevarication, my answer to these highly unusual pediatric situations with prolonged support is that I do not know enough about each of these cases. I doubt many of these stories having seen many pediatric neurologists struggle to keep a brain-dead donor stable.

Whether patients are biologically dead when the brain irrevocably stops functioning is purely a philosophical and, perhaps, spiritual issue. A patient with no functioning brainstem and thus brain may have the rest of his or her body “alive” if adequately supported, and we may even find a way to get better at that. I have called it a “magnificent cell culture,”73 and in the rare cases of maternal brain death others called it a “human incubator.” I believe that to be the case. In Shewmon’s words, most of us are brain (mind) reductionists, in contrast to traditional philosophical anthropologists, who may see a human organism—without a brain—as biologically unified and alive. His basic premise is thus quite simple. The determination of death is not based on brain function, and he—seemingly paradoxically, as a neurologist—rejects any brain criteria of death.

It may come down to a neurological-versus-vitalist argument. In the practice of medicine, certain signs suffice for a diagnosis; in the practice of philosophy, none are definitive. Not one recent essay written by a philosopher has declared solidarity with the determination of brain death, and all have noncritically accepted alternative explanations.

Discussions about how much of the brain must die go nowhere.9 Pallis considers them “terminologic quagmires.”44 Speculation on how patients might be living (in heaven or hell) with no functioning brainstem alone is useless and simplifies the catastrophic injury and the clinical context. It is precisely these issues that cause misconceptions about the irreversible loss of brain function.

Conclusions

Critics come and go, and over the years the commentaries against the clinical diagnosis of brain death or the concept of brain death have shifted their focus. These range from criticisms of the Harvard Committee (alleging conflict of interest, as shown by the presence of transplant physicians), to clinical examination (alleging injury with the apnea test), to critiques of the total brain necrosis criteria (alleging intact pituitary and hypothalamic function), to critiques on the difficulty of support (alleging long-term support in pregnant “brain-dead” women and children) and, most recently, to critiques on irreversibility (alleging possible recoveries). Critics can demand an alternative explanation, but as yet they have no supportive original data on large series of patients. All have been using previously published data and interpret them wholly otherwise.72 Many of the more recent exceptional cases are presented to conjure up a controversy (and to write opinion papers).

Is there nothing disconcerting? Going back to the Harvard criteria, a committee without transplantation representatives would have been ideal, but a carefully detailed evaluation of the deliberation has not revealed bias among the writers of the document.7,74,75 Brain death determination and organ procurement are two totally different procedures but are linked closely, with 70% of brain death declarations converting into organ donors. Intermingling of transplant surgeons in brain death determination is avoided carefully in most practices, and in fact, most transplant surgeons want nothing to do with it.

There is no questioning the early arguments have been weak, namely that (1) the brain is totally necrotic; (2) cardiac arrest always occurs within hours after clinical diagnosis; and (3) invariably, supporting electrophysiology or blood flow studies confirming the clinical condition. We now know that neuropathological examination of brains coming to autopsy soon after the diagnosis of brain death may show normal areas of the brain in patients with and without complete circulatory arrest on blood flow testing. This suggests that no study can reliably exclude cerebral perfusion. Arguments that brain death is similar to physiological decapitation thus are incorrect,41 but this does not mean that even in the presence of seemingly intact regions of the brain, the brain did not irreversibly stop functioning.75 Hemodynamic instability is common in most patients, but hypertension (likely due to unopposed sympathetic spinal cord activity or by lingering effects of caudal medulla oblongata pressor areas) requiring antihypertensives may occur. Nothing here should invalidate the diagnosis.

Since the original description of brain death more than 50 years ago (as well as enormous clinical experience), the certitude of a brain death diagnosis has not been questioned by expert physicians in the field. These criticisms are also indirectly a comment on our practice of judging irreversible neurological injury and the use of organ donation and perhaps even an insinuation that those involved in these decisions may have less respect for the patient’s life. There may be a serious attempt to delegitimize the practice of organ donation. Physicians in the neurosciences who are closely and frequently involved in brain death determination will be vexed and less intrigued by the disputations outlined in this chapter, and some may be greatly struck by the fact that such vast literature even exists. It will be hard to find one who would concede that these potential organ donors are not dead. Most of us practicing neurologists and neurosurgeons agree that death of the brain is a sufficient condition for the death of the individual. It is not an irreversibly comatose patient with a poor prognosis because the dead have no prognosis. But that may not bridge the positions outlined in this chapter or reconcile their position that the definition of death by brain criteria is also a social and value construct. Sad to say, critics, confusionists, and deniers will remain. In Capron’s legal commentary, “There are good and sufficient reasons why the existing consensus about the determination of death has endured for more than 30 years even in the face of persistent criticism.”18

References

1. Controversies in the determination of brain death: a white paper by the President’s Council on Bioethics. Washington, DC; 2008.Find this resource:

2. Declaration of Calixto Machado, MD, PhD, RP13-707598 Latasha Winkfield v. Children’s Hospital Oakland, Superior Court of the State of California in and for the County of Alameda.Find this resource:

3. Declaration of Death. Alan Shewmon, M.D., RP13-707598 Latasha Winkfield v. Children’s Hospital Oakland, Superior Court of the State of California in and for the County of Alameda.Find this resource:

4. Arita K, Uozumi T, Oki S, Kurisu K, Ohtani M, Mikami T. The function of the hypothalamo-pituitary axis in brain dead patients. Acta Neurochir (Wien) 1993;123:64–75.Find this resource:

5. Barnard CN. The operation. A human cardiac transplant: an interim report of a successful operation performed at Groote Schuur Hospital, Cape Town. S Afr Med J 1967;41:1271–1274.Find this resource:

6. Battro A, Bernat JL, Bousser N, et al. Why the concept of brain death is valid as a definition of death. Proceedings of the Working Group of 11-12 September 2006; 2007; Vatican City.Find this resource:

7. Belkin G. Death before Dying: History, Medicine, and Brain Death. New York: Oxford University Press; 2014.Find this resource:

8. Bernat JL. A defense of the whole-brain concept of death. Hastings Cent Rep 1998;28:14–23.Find this resource:

9. Bernat JL. How much of the brain must die in brain death? J Clin Ethics 1992;3:21–26; discussion 27–28.Find this resource:

10. Bernat JL, Capron AM, Bleck TP, et al. The circulatory-respiratory determination of death in organ donation. Crit Care Med 2010;38:963–970.Find this resource:

11. Bernat JL, Culver CM, Gert B. On the definition and criterion of death. Ann Intern Med 1981;94:389–394.Find this resource:

12. Birch SC. The dead donor rule: a defense. J Med Philos 2013;38:426–440.Find this resource:

13. Boly M, Tshibanda L, Vanhaudenhuyse A, et al. Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 2009;30:2393–2400.Find this resource:

14. Bondeson J. Buried Alive: The Terrifying History of Our Most Primal Fear. New York: W. W. Norton; 2001.Find this resource:

15. Boucek MM, Mashburn C, Dunn SM, Frizell R, Edwards L, Pietra B, Campbell D, Denver Children’s Pediatric Heart Transplant Team. Pediatric heart transplantation after declaration of cardiocirculatory death. N Engl J Med 2008;359:709–714.Find this resource:

16. Burkle CM, Sharp RR, Wijdicks EF. Why brain death is considered death and why there should be no confusion. Neurology 2014;83:1464–1469.Find this resource:

17. Byrne PA, Weaver WF. “Brain death” is not death. In: Machado C, Shewman DA, eds. Brain Death and Disorders of Consciousness. New York: Kluwer Academic Press/Plenum; 2004:43–60.Find this resource:

18. Capron AM. Brain death—well settled yet still unresolved. N Engl J Med 2001;344:1244–1246.Find this resource:

19. Coimbra CG. Implications of ischemic penumbra for the diagnosis of brain death. Braz J Med Biol Res 1999;32:1479–1487.Find this resource:

20. Evans DW. Brainstem tests not adequate to diagnose death in organ donors. Nature 2009;461:1198.Find this resource:

21. Evans DW. The demise of “brain” in Britain. In: Potts M, Nilges RG, eds. Beyond Brain Death. London: Kluwer Academic; 2000:139–158.Find this resource:

22. Fugate JE, Stadtler M, Rabinstein AA, Wijdicks EF. Variability in donation after cardiac death protocols: a national survey. Transplantation 2011;91:386–389.Find this resource:

23. Green MB, Wikler D. Brain death and personal identity. Philos Public Aff 1980;9:105–133.Find this resource:

24. Hornby K, Hornby L, Shemie SD. A systematic review of autoresuscitation after cardiac arrest. Crit Care Med 2010;38:1246–1253.Find this resource:

25. Ingvar DH. Brain death—total brain infarction. Acta Anaesthesiol Scand Suppl 1971;45:129–140.Find this resource:

26. Joffe AR. Are recent defences of the brain death concept adequate? Bioethics 2010;24:47–53.Find this resource:

27. Joffe AR. Brain death is not death: a critique of the concept, criterion, and tests of brain death. Rev Neurosci 2009;20:187–198.Find this resource:

28. Joffe AR, Anton N. Brain death: understanding of the conceptual basis by pediatric intensivists in Canada. Arch Pediatr Adolesc Med 2006;160:747–752.Find this resource:

29. Joffe AR, Anton N, Mehta V. A survey to determine the understanding of the conceptual basis and diagnostic tests used for brain death by neurosurgeons in Canada. Neurosurgery 2007;61:1039–1045; discussion 1046–1037.Find this resource:

30. Joffe AR, Kolski H, Duff J, deCaen AR. A 10-month-old infant with reversible findings of brain death. Pediatr Neurol 2009;41:378–382.Find this resource:

31. Jonas H. Against the stream. In Philosophical Essays: From Ancient Creed to Technological Man. Englewood Cliffs, NJ: Prentice-Hall; 1974.Find this resource:

32. Jouvet M. Coma and other disorders of consciousness. In: Vinken PJ, Bruyn GW, eds. Handbook of Clinical Neurology. Vol 3. Disorders of Higher Nervous Activity. Amsterdam: North-Holland; 1969:62–79.Find this resource:

33. Karakatsanis KG. ‘Brain death’: should it be reconsidered? Spinal Cord 2008;46:396–401.Find this resource:

34. Korein J. Ontogenesis of the brain in the human organism: definition of life and death of the human being and person. In: Edwards RB, ed. New Essays on Abortion and Bioethics. Greenwich, CT: Jai Press; 1997:1–74.Find this resource:

35. Korein J. The problem of brain death: development and history. Ann N Y Acad Sci 1978;315:19–38.Find this resource:

36. Kramer W. From reanimation to deanimation (intravital death of the brain during artificial respiration). Acta Neurol Scand 1963;39:139–153.Find this resource:

37. Lizza JP. The conceptual basis for brain death revisited: loss of organic integration or loss of consciousness? Adv Exp Med Biol 2004;550:51–59.Find this resource:

38. Marquis D. Are DCD donors dead? Hastings Cent Rep 2010;40:24–31.Find this resource:

39. Maruya J, Nishimaki K, Nakahata J, Suzuki H, Fujita Y, Minakawa T. Prolonged somatic survival of clinically brain-dead adult patient. Neurol Med Chir (Tokyo) 2008;48:114–117.Find this resource:

40. Miller FG, Truog RD. Death, Dying, and Organ Transplantation. New York: Oxford University Press; 2012.Find this resource:

41. Miller FG, Truog RD. Decapitation and the definition of death. J Med Ethics 2010;36:632–634.Find this resource:

42. Miller FG, Truog RD. Rethinking the ethics of vital organ donations. Hastings Cent Rep 2008;38:38–46.Find this resource:

43. Nair-Collins M, Green SR, Sutin AR. Abandoning the dead donor rule? A national survey of public views on death and organ donation. J Med Ethics 2015;41:297–302.Find this resource:

44. Pallis C. Brain stem death—the evolution of a concept. Med Leg J 1987;55(Pt 2):84–107.Find this resource:

45. Pallis C. Whole-brain death reconsidered—physiological facts and philosophy. J Med Ethics 1983;9:32–37.Find this resource:

46. Pana R, Hornby L, Shemie SD, Dhanani S, Teitelbaum J. Time to loss of brain function and activity during circulatory arrest. J Crit Care 2016;34:77–83.Find this resource:

47. Pernick MS. Back from the grave: recurring controversies over defining and diagnosing death in history. In: Zaner RM, ed. Death: Beyond Whole-Brain Criteria. Dordrecht, The Netherlands: Kluwer Academic; 1988:17–24.Find this resource:

48. Potts M, Byrne PA, Nilges RG. Beyond Brain Death: The Case against Brain-Based Criteria for Human Death. Dordrecht, The Netherlands: Kluwer Academic; 2000.Find this resource:

49. Powner DJ, Bernstein IM. Extended somatic support for pregnant women after brain death. Crit Care Med 2003;31:1241–1249.Find this resource:

50. Racine E. Defining death without science? A pragmatic rebuttal. Am J Bioeth 2014;14:41–43.Find this resource:

51. Rady MY, Verheijde JL. Letter to the editor. JAMA Neurol 2016;73:760.Find this resource:

52. Rady MY, Verheijde JL, McGregor JL. Scientific, legal, and ethical challenges of end-of-life organ procurement in emergency medicine. Resuscitation 2010;81:1069–1078.Find this resource:

53. Repertinger S, Fitzgibbons WP, Omojola MF, Brumback RA. Long survival following bacterial meningitis-associated brain destruction. J Child Neurol 2006;21:591–595.Find this resource:

54. Schwab RS, Potts F, Mathis P. EEG as an aid in determining death in the presence of cardiac activity. Electroencephalogr Clin Neurophysiol 1963;15:147.Find this resource:

55. Shemie SD, Doig C, Dickens B, et al. Severe brain injury to neurological determination of death: Canadian forum recommendations. CMAJ 2006;174:S1–13.Find this resource:

56. Shewmon DA. Brain death: can it be resuscitated? Issues Law Med 2009;25:3–14.Find this resource:

57. Shewmon DA. Chronic “brain death”: meta-analysis and conceptual consequences. Neurology 1998;51:1538–1545.Find this resource:

58. Shewmon DA. Spinal shock and brain death: somatic pathophysiological equivalence and implications for the integrative-unity rationale. Spinal Cord 1999;37:313–324.Find this resource:

59. Shewmon DA. The probability of inevitability: the inherent impossibility of validating criteria for brain death or ‘irreversibility’ through clinical studies. Stat Med 1987;6:535–553.Find this resource:

60. Tibballs J. A critique of the apneic oxygenation test for the diagnosis of “brain death”. Pediatr Crit Care Med 2010;11:475–478.Find this resource:

61. Truog RD. Brain death—too flawed to endure, too ingrained to abandon. J Law Med Ethics 2007;35:273–281.Find this resource:

62. Truog RD, Miller FG. Changing the conversation about brain death. Am J Bioeth 2014;14:9–14.Find this resource:

63. Truog RD, Miller FG. Counterpoint: are donors after circulatory death really dead, and does it matter? No and not really. Chest 2010;138:16–18; discussion 18–19.Find this resource:

64. Truog RD, Miller FG. The dead donor rule and organ transplantation. N Engl J Med 2008;359:674–675.Find this resource:

65. Truog RD, Miller FG, Halpern SD. The dead-donor rule and the future of organ donation. N Engl J Med 2013;369:1287–1289.Find this resource:

66. Veatch RM. Brain death and slippery slopes. J Clin Ethics 1992;3:181–187.Find this resource:

67. Veatch RM. Donating hearts after cardiac death—reversing the irreversible. N Engl J Med 2008;359:672–673.Find this resource:

68. Veatch RM. Killing by organ procurement: brain-based death and legal fictions. J Med Philos 2015;40:289–311.Find this resource:

69. Veatch RM. The death of whole-brain death: the plague of the disaggregators, somaticists, and mentalists. J Med Philos 2005;30:353–378.Find this resource:

70. Veatch RM. The impending collapse of the whole-brain definition of death. Hastings Cent Rep 1993;23:18–24.Find this resource:

71. Veatch RM, Ross LF. Defining Death: The Case for Choice. Washington, DC: Georgetown University Press; 2016.Find this resource:

72. Verheijde JL, Rady MY, McGregor JL. Brain death, states of impaired consciousness, and physician-assisted death for end-of-life organ donation and transplantation. Med Health Care Philos 2009;12:409–421.Find this resource:

73. Walker EA. Cerebral Death. Baltimore & Munich: Urban & Schwarzenberg; 1985.Find this resource:

74. Wijdicks EF. The neurologist and Harvard criteria for brain death. Neurology 2003;61:970–976.Find this resource:

75. Wijdicks EF. The neurology of death and what it does not mean. Brain 2014;137:2105–2108.Find this resource:

76. Wijdicks EF, Rabinstein AA, Manno EM, Atkinson JD. Pronouncing brain death: contemporary practice and safety of the apnea test. Neurology 2008;71:1240–1244.Find this resource:

77. Youngner SJ, Arnold RM, Schapiro R, eds. The Definition of Death: Contemporary Controversies. Baltimore: Johns Hopkins University Press; 1999.Find this resource:

78. Zamperetti N, Bellomo R, Defanti CA, Latronico N. Irreversible apnoeic coma 35 years later. Towards a more rigorous definition of brain death? Intensive Care Med 2004;30:1715–1722.Find this resource: