Inconsistencies in the ethical declaration of death

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Brain death: resolving inconsistencies in the ethical declaration of death

[La mort
cérébrale : résoudre les contradictions de la
déclaration éthique de la mort]

Christopher James
Doig MD MSc,* Ellen Burgess MD†

The
first criteria for the determination of brain death were developed in
1968 in part to address concerns that had arisen with the retrieval
of organs for transplantation. Despite over 30 years of application,
some professional and public doubt persists over the validity of the
theoretical construct underlying this method of determining death.
Our review will address historical perspectives on the development of
brain death criteria, and inconsistencies in current clinical
criteria.

Narrative
review from selected MEDLINE references and other published sources.

The
primary construct of the determination of death is that either
cardiopulmonary or neurological function irreversibly ceases.
However, there is inconsistency in the neurological criteria for
death between jurisdictions, between patient populations, and in the
use of confirmatory tests. These inconsistencies may cause concern in
the public or profession about the validity of the determination of
death by neurological criteria.

Organ
transplantation is premised on professional and public acceptance
that the donor is dead. Given that the criteria for brain death or
their application remain variable, we suggest that it is reasonable
to consider a national consensus to address these inconsistencies.
Alternatively, the standard use of confirmatory radiographic testing
prior to the retrieval of organs from donors who meet clinical brain
death criteria should be considered to provide conclusive evidence of
permanent and irreversible loss of brain function.

Objectif : Les
premiers critères de mort cérébrale ont été
formulés en 1968 pour répondre, en partie, aux
inquiétudes soulevées par la recherche d’organes pour
les greffes. Malgré 30 ans d’application, un certain doute
subsiste chez les professionnels et le public sur la validité
de la notion théorique à l’origine de cette façon
de déterminer la mort. Notre revue aborde les perspectives
historiques de la formulation des critères de mort cérébrale
et des contradictions des critères cliniques actuels.

Méthode : La
revue descriptive provient de la consultation de

références
dans MEDLINE et d’autres sources publiées. Constatations
principales : Le principal concept de la détermination
de la mort est l’arrêt irréversible de la fonction
cardio-pulmonaire ou neurologique. Cependant, il y a des
contradictions dans les critères neurologiques de la mort
entre les pays, entre les populations de patients et dans l’usage
des tests de confirmation. Ces contradictions peuvent inquiéter
le public et la profession médicale sur la validité de
la détermination de la mort par des critères
neurologiques.

Conclusion: La
greffe d’organes est fondée sur l’acceptation publique et
professionnelle du fait que le donneur soit décédé.
Étant donné que les critères de mort cérébrale,
ou de leur application, demeurent variables, nous croyons qu’il est
raisonnable d’envisager la formation d’un consensus visant à
traiter de ces contradictions. Autrement, l’utilisation standard
des tests radiographiques confirmatifs, qui précèdent
le prélèvement d’organes de donneurs répondant
aux critères cliniques de mort cérébrale,
devrait être considérée pour fournir la preuve
concluante de la perte permanente et irréversible de la
fonction cérébrale.

From the
Department of Critical Care Medicine and the Office of Medical
Bioethics;* and the Division of Nephrology, Department of Medicine,†
Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada.

Address
correspondence to: Dr. Christopher James Doig, Rm EG23G,
Foothills Medical Centre, 1403, 29th Street NW, Calgary Alberta T2N
2T9, Canada. E-mail: cdoig@ucalgary.ca

Accepted for
publication March 17, 2003.

Revision
accepted April 30, 2003.

CAN J ANESTH 2003 / 50: 7 / pp
725–731

726

If one subject
in health law and bioethics can be said to be at once well settled
and persistently unresolved, it is how to determine that death has

1

occurred.

THE
retrieval of organs for transplantation obtained from anonymous
‘cadaveric’ (brain dead, or non-heart beating) donors is based on
the moral acceptance of the ‘dead donor rule’: that these
patients are dead.^2,3 The
retrieval of organs from individuals who are brain dead is based on
the premise that permanent cessation of (whole) brain function
equates with death and can be identified by simple bedside clinical
criteria.^4,5 In
the Uniform Determination of Death Act (UDDA), there are two distinct
definitions for death: "an individual who has sustained either
1) irreversible cessation of circulatory and respiratory function,
and 2) irreversible cessation of all functions of the entire brain,
including the brainstem is dead. A determination of death must be
made in accordance with accepted medical standards."⁶
Below, we address inconsistencies in the
clinical criteria for brain death, and present an opinion that a
reconsideration of a national medical standard is necessary.

In
1959, Mollaret and Goullon used the term coma dépassé,
"a state beyond coma", to describe a condition from which
they believed recovery was not possi-ble.⁷
In 1965, ‘brain dead’ was used to
describe a patient with a heart beat from whom a kidney was procured
for transplant into a non-related recipient.⁸
In 1968, the Harvard criteria for brain
death were developed as the conclusions of the Ad Hoc Committee of
the Harvard Medical School.⁹ All
subsequent criteria for brain death have been founded on this seminal
work. To quote from their original communiqué, "Our
primary purpose is to define irreversible coma as a new criterion for
death. There are two reasons why there is need for a definition: 1)
improvements in resuscitative and supportive measures have led to
increased efforts to save those who are desperately injured.
Sometimes these efforts have only partial success so that the result
is an individual whose heart continues to beat but whose brain is
irreversibly damaged. The burden is great on patients who suffer
permanent loss of intellect, on their families, on the hospitals, and
those in need of hospital beds already occupied by those comatose
patients. 2) Obsolete criteria for the definition of death can lead
to

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controversy in
obtaining organs for transplantation." The ad hoc committee’s
criteria were not based on a physiologic or philosophical
understanding that the brain, and therefore the person, was dead.
Rather, the committee’s recommendations were premised on the
understanding that the coma was irreversible and care was futile "we
are concerned here only with those comatose individuals who have no
discernible central nervous system activity… [and where it is
possible to determine] the characteristics of a permanently
non-functioning brain." The committee identified that function
in the cerebrum including subcortical function (specific examples
presented were thalamic and basal ganglionic mechanisms), and
brainstem must be lost to be consistent with brain death.

The medical
consultants to the President’s Commission for the Study of Ethical
Problems in Medicine and Biomedical and Behavioral Research
subsequently detailed a comprehensive set of clinical circumstances
and a battery of tests to identify brain death:⁶ “1)
Cessation [of brain function] is recognized when evaluation discloses
findings of (a) and (b): (a) cerebral functions are absent, (b) brain
stem functions are absent. 2) Irreversibility is recognized when
evaluation discloses findings of (a), (b), and (c): (a) the cause of
coma is established and is sufficient to account for the loss of
brain functions, (b) the possibility of any recovery of any brain
function is excluded, (c) cessation of all brain functions persists
for an appropriate period of observation and/or trial of therapy.”
The Uniform Determination of Death Act (UDDA - the United States
Federal Legislation adopted by most State Legislatures which legally
defines death) used the recommendation of the President’s
Commission as the basis for the statute. Though the Commission’s
report does provide detailed criteria on how to diagnose brain death,
the authors did not attempt to provide a conceptual understanding of
why these clinical findings equate with death, or provide evidence
that these tests in fact assess the integrity of whole brain
function.

Bernat provided a
structural framework for the conceptual understanding of the
diagnosis of brain death.¹⁰ He argues that the formal
acceptance of ‘brain death’ is dependent on three conditions: 1)
the "permanent cessation and functioning of the whole brain";
2) that future changes in clinical understanding of brain function
and assessment including the use of technology will only slightly
alter the criterion of death, and 3) that the "explicit
formulation" must be consistent with "society’s
traditional" understanding of death. As will be discussed vide
infra, the UDDA criteria (similar to Canadian criteria) for brain
death

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and the accepted
standards of whole brain death enumerated in the policy do not meet
these reasonable criteria of Bernat.

Assessing
permanent cessation of function

The UDDA criteria
for brain death, and guidelines from other jurisdictions such as
current Canadian standards¹¹ do not test function of the
"entire brain", and there is sound evidence that many
individuals who meet the clinical criteria of brain death continue to
have some cortical, subcortical, or brain stem function. The current
clinical tests for brain death do not assess subcortical function of
structures such as the hypothalamus-pituitary axis. Many patients
diagnosed as brain dead have intact neurohumoral control of
hypothalamic-pituitary function, demonstrate normal hypothalamic
mediated thermoregulatory control, and have intact autonomic
function: they do not have hemodynamic collapse, they have physical
findings such as bowel sounds, and are reported to have autonomic
reflexes (tachycardia and hypertension) at the time of organ
retrieval.¹² Thermoregulatory control, maintenance of
normal hypothalamus and pituitary gland function, and intact
autonomic function represent normal subcortical functions
inconsistent with the understanding of ‘permanent cessation of
functioning of the entire brain’. Given that current clinical
testing does not assess subcortical brain function, ‘whole brain
death’ cannot be conclusively identified at the bedside by using
clinical criteria.

One of the
enduring arguments in support of the consistency of the clinical
confirmation of brain death equating with death is that loss of
integrative functions of the cortex and brainstem will rapidly result
in failure of other systems and death of the person - the so called
somatic disintegration hypothesis.¹³ "That structural
disintegration follows brain death is not a contingent matter; it is
a necessary consequence of the death of the critical system. The
death of the brain is the point beyond which other systems cannot
survive with, or without, mechanical support."¹⁴ Shewmon
reviewed 12,200 sources to identify 175 cases of individuals with
brain death reported to have cardiac function persist for a minimum
of one week; 56 cases are reported in detail.¹⁵ In
approximately 60% of the 56 cases, cardiac function persisted to one
month. Of the individuals whose cardiac function ceased in this one
month interval, half had cardiac arrest as a result of withdrawal of
ventilatory support. Shewmon’s publication has questioned the
construct of the somatic integration hypothesis. His work was subject
to much criticism in subsequent correspondence,^16–19 but
the importance of his work cannot be overlooked given that many
lawmakers and judges have viewed the somatic integration hypothesis
as a cornerstone to the legal basis for brain death equating with
death.¹³

Consistent
standards

It would be
reasonable to assume that the criteria for the clinical diagnosis of
brain death have remained relatively static over the past three
decades since no new relevant physical examination maneuvers have
been described during this time. This assumption is incorrect. In
1977, Walker published on behalf of a collaborative group from the
National Institute of Neurological Diseases and Strokes, a study
reviewing the then current criteria for cerebral death.²⁰ The
criteria included coma, apnea, dilated pupils, absent motor
responses, and electrocerebral silence on electroencephalogram (EEG).
Four years later, the President’s Commission criteria expanded the
required number of brain stem reflexes that needed to be absent, and
removed the criterion of electrocerebral silence. However, the
Commission still recommended EEG as desirable when objective
documentation was required to confirm clinical findings…
"electrocerebral silence verifies irreversible loss of cortical
functions, except in patients with drug intoxication or hypothermia…
when joined with the clinical findings of absent brainstem functions,
electrocerebral silence confirms the diagnosis." The
Commission’s decision to remove electrocerebral silence as a
necessary confirmatory test remains puzzling given its subsequent
recommendation for its use. Subsequent to the President’s
Commission report there are studies that document the presence of
electrocerebral activity following the declaration of brain
death.^21,22 Grigg and colleagues from Loyola University
Medical Centre reported on EEG activity in a consecutive case series
of 56 patients with confirmed clinical ‘brain death’.²¹
These authors reported that in 11 patients, electrocerebral
silence was not present following the diagnosis of brain death. These
authors used appropriate measures to avoid external interference
(room noises, internal machine noise, muscle activity, or movement
artifact), as a source of observed EEG activity. As well, EEG
interpretations were conservative assuming any observed activity as
artifact unless the observer was without doubt. EEG activity observed
was categorized into low voltage theta or beta activity, alpha like
activity, or sleep-like activity. In one of two patients EEG activity
resembling physiologic sleep persisted at repeat EEG testing 168 hr
following ‘declaration’ of ‘brain death’. The finding of
coordinated EEG activity, such as sleep, is inconsistent with the
presumption of loss of coordinated and integrating whole brain
function and raises doubt about the accuracy of the clinical
diagnosis of brain death.

There remains
considerable international inconsistency in the application of
clinical criteria for the diagnosis of brain death.²³ In
North America, the recently published guidelines prepared by expert
opinion of the Canadian Neurocritical Care group differ from the
‘evidence based approach’ of the American Academy of
Neurology.^11,24 A recent article reviews the American
criteria.²⁵ For example, the Canadian guidelines do not
require the testing of the oculocephalic reflex, permit a core
temperature as low as 32.2°C during the apnea test, and allow an
interval between examinations as short as two hours, or as long as 24
hr if due to anoxic-ischemic insult. The American criteria do not
specify a necessary interval between assessments but recommend as
reasonable an arbitrary six-hour interval, require a core temperature
of 36.5°C during the apnea test, and do require testing of the
oculocephalic reflex. The criteria used for the diagnosis of brain
death in infants less than one year of age are also different than
the criteria for the diagnosis in adults. In England, this definition
of death has been adopted: "irreversible loss of the capacity
for consciousness, combined with irreversible loss of the capacity to
breathe should be regarded as the definition of death." The
nomenclature in the United Kingdom has been changed from ‘brain
death’ to ‘brain stem death’.²⁶ Takeuchi has
published on other inconsistencies.²⁷ There has been no
coherent cogent pathophysiologic or philosophical explanation to
explain these differences in diagnostic criteria. Perhaps, as
discussed by Wijdicks in the only ‘evidence based’ synthesis of
brain death criteria, the diagnosis of brain death has been
established largely on class III data defined as "evidence
provided by expert opinion, nonrandomized historical controls, or one
or more case reports."^24,28 These inconsistencies,
changes in the criteria for ‘brain death’ over time, and lack of
specificity in tests of cortical and subcortical brain function
exemplify the inadequacy and inconsistency of clinical criteria for
confirming "complete cessation of brain function" and
therefore brain death. This raises concern over whether these
criteria are satisfactory.

Society’s
and the medical profession’s understanding of brain death

There is a
misunderstanding of the concept, definition, and clinical criteria
for the diagnosis of brain death among the health care professions.
Youngner and colleagues performed a multicentre survey of staff
caring for organ donors including physicians responsible for
determining brain death, and medical and

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nursing staff
involved in the care of the potential donor/their family.²⁹ Only
64% of physicians and 28% of other staff accurately identified the
clinical criteria for brain death, and/or in case scenarios correctly
categorized patients as dead or alive. Even physicians actively
involved in the identification of brain death were unable to identify
the requisite diagnostic components of brain death, and/or were
unable to apply the criteria correctly.

In a recent
editorial in the Journal Anaesthesia, Young and Matta advocate
for the use of anesthetics during the harvesting of organs from brain
dead organ donors.³⁰ They provided three reasons, of which
two are particularly relevant: 1) the surgical retrieval of organs
from brain dead donors is often associated with hypertension and
tachycardia and this is distressing for operating room personnel to
witness (ostensibly because these findings during operative
procedures are usually an indication of awareness and/or pain); and
2) that the concept of brain death is not well understood and given
the arbitrary nature of the clinical criteria for brain death,
caution is required before assuming anesthesia is not necessary. In
subsequent commentaries,^31,32 these authors were chided in
part because "by urging the use of anaesthetic agents, they have
accepted that there are doubts over the state of consciousness in the
brainstem dead individual. It would have been far more appropriate to
suggest reappraisal of the UK brainstem criteria, public debate, or
even more openness and honesty in our discussions with bereaved
relatives. We cannot hope to maintain public confidence merely by
following their ill thought out suggestions."

Although two
physicians with experience and expertise must be responsible for the
declaration of brain death, and a neurologic condition capable of
causing brain death is a mandatory prerequisite to the diagnosis of
brain death, there are reports in the literature of conditions that
mimic brain death or that provide examples of the mistaken diagnosis
of brain death.^33–40

Van Norman⁴¹
describes three cases (two of which she has apparent immediate
knowledge) involving the determination of brain death. In these three
cases, the patients did not meet the clinical criteria for brain
death, yet were referred for organ retrieval. In two of the cases,
the patient’s had suffered devastating brain injuries, but were
breathing spontaneously. Despite spontaneous respiratory effort,
these patients were certified as brain dead, and proceeded to organ
retrieval. In the second of these two cases, organ retrieval occurred
against the protests of the anesthesiologist who questioned the
diagnosis of brain death, and despite the patient demon

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strating
hypertension and movement during organ retrieval necessitating the
use of muscle relaxants and general anesthesia. In the third case, a
young woman postvaginal delivery with concomitant pregnancy induced
hypertension suffered generalized seizures, and had clinical and
radiographic evidence (computed tomography findings of coning,
diffuse edema, and occipital lobe infarcts) of a "catastrophic
neurological event". The patient was determined to be brain
dead, and prepared for organ retrieval. One physician subsequently
identified intact brainstem reflexes. A review of this case
determined that the clinical diagnosis of brain death had occurred
after the patient had received iv muscle relaxants, and had a
serum magnesium level of

5.2 mEq·L^–1.
In the third case, the mother regained consciousness, and was
discharged home alert and oriented, but with unspecified neurological
deficits.

Brain death is a
concept often misunderstood by the general public. Sanner performed a
survey about attitudes toward autopsy and organ donation in a sample
size of 1,950 randomly selected individuals.⁴² Of
respondents, only 62% would donate their organs, and only 39% would
assent to the donation of their rela-tive’s organs. The two
predominant reasons for refusal were the fear of not being dead at
the time of organ retrieval and the uncertainty of the concept of
brain death. Because families misunderstand brain death, many organ
retrieval programs stress the necessity of stating that the patient
is ‘dead’ and not ‘brain dead’, thereby potentially obviating
any family concerns about the status of their loved one.

In summary, the
current clinical criteria for brain death are not consistent with the
stated objective of the outcome "to identify the permanent
cessation of entire brain function". Nor are the clinical
criteria for brain death either universally understood, and/or
correctly applied, and at least in one report, two cases were
presented where the criteria were deliberately misrepresented in an
attempt to retrieve an organ for transplantation. Finally, brain
death is not a concept that is coherent and clearly understood in the
general public.

Reconsidering
the criteria for brain death

Is this simply a
pedantic and pedagogical discourse, or is there relevance in
discussing these inconsistencies? As was identified in the seminal
Harvard report, there are two reasons to determine that brain death
has occurred: 1) to support withdrawal of treatment as further
interventions are futile, or 2) for the purposes of solid organ
donation which is now the most common practical reason.

A premature death
from end-stage organ dysfunction is potentially preventable with an
organ transplant.

Unfortunately, the scarcity of
available organs for transplantation is a barrier to saving more
lives. The ethical approach to organ donation dictates that the need
of those requiring organs should not supercede the ethical management
of potential donors.

Society’s acceptance of organ
transplantation, and the willingness to donate organs is dependent on
absolute trust in the process, a process that starts with the
diagnosis of brain death. Therefore, it would seem a reasonable
proposal for a broad based coalition to reexamine the Canadian
criteria to address issues such as the evidence that justifies the
clinical criteria as proposed, the differences between published
criteria and the current application of criteria in Canadian
hospitals including professional training and standards. Such a forum
is planned, and this approach should help ensure public confidence in
the validity of the medical standard, and also address mechanisms to
avoid conflict of interest when organ donation is considered.⁴³

There is an alternative
approach. A lack of blood flow to an organ causes an organ to die.
The brain is considered the organ most sensitive to necrosis from
cessation of blood flow. Lack of blood flow to the entire brain is an
anatomic equivalent to the cessation of brain function. In the
setting of normal arterial pressures, technetium 99
hexamethylpropyleneamineoxime (Tc99-HMPAO) perfusion scanning, or
four-vessel selective cerebral contrast dye angiography can
accurately assess anterior and posterior cerebral circulation (that
is ‘whole brain’ blood flow).^44,45 Tc99-HMPAO scanning
is usually performed with dynamic and static imaging. The dynamic
imaging can quickly assess the presence or absence of intracranial
perfusion, whereas static imaging detects any uptake of the tracer by
functioning neurons. Both of these tests provide irrefutable proof of
absent blood flow to the brain, and therefore permanent and
irreversible cessation of brain function. If we cannot resolve the
inconsistencies in the use of current clinical criteria, it may be
reasonable to consider them as a mandatory component of determining
‘whole’ brain death.

Increasing
organ donation is an important and laudable objective. To do so at
the expense of exploiting society’s most vulnerable cannot be
supported despite the best of intentions. We share the opinion of
Dossetor who states: "ethics dictates the following: organs
should not be procured from bodies where there is life... no measures
should be carried out on the dying person even with family consent,
that are not directed at serving the best interests of the dying
person… Our faith in the supposedly objective diagnosis of brain
death leads us to remove organs from the dead body where the heart is
still beating. We now need to take seriously the question of whether
the criteria to establish brain death are as reliable as we claim
them to be. If they are not as satisfactory as we once thought, the
whole matter should be brought into debate."⁴⁶

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