BioMed Central
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Philosophy, Ethics, and Humanities
in Medicine
Open Access
Commentary
The ethics of donation and transplantation: are definitions of death
being distorted for organ transplantation?
Ari R Joffe
Address: Stollery Children's Hospital, 3A3.07 8440 112 Street, Edmonton, Alberta, Canada T6G 2B7
Email: Ari R Joffe - ajoffe@cha.ab.ca
Abstract
A recent commentary defends 1) the concept of 'brain arrest' to explain what brain death is, and
2) the concept that death occurs at 2–5 minutes after absent circulation. I suggest that both these
claims are flawed. Brain arrest is said to threaten life, and lead to death by causing a secondary
respiratory then cardiac arrest. It is further claimed that ventilation only interrupts this way that
brain arrest leads to death. These statements imply that brain arrest is not death itself. Brain death
is a devastating state that leads to death when intensive care, which replaces some of the brain's
vital functions such as breathing, is withdrawn and circulation stops resulting in irreversible loss of
integration of the organism. Circulatory death is said to occur at 2–5 minutes after absent
circulation because, in the context of DCD, the intent is to not attempt reversal of the absent
circulation. No defense of this weak construal of irreversible loss of circulation is given. This means
that paents in identical physiologic states are dead (in the DCD context) or alive (in the
resuscitation context); the current state of death (at 2–5 minutes) is contingent on a future event
(whether there will be resuscitation) suggesting backward causation; and the commonly used
meaning of irreversible as 'not capable of being reversed' is abandoned. The literature supporting
the claim that autoresuscitation does not occur in the context of no cardiopulmonary resuscitation
is shown to be very limited. Several cases of autoresuscitation are summarized, suggesting that the
claim that these cases are not applicable to the current debate may be premature. I suggest that
brain dead and DCD donors are not dead; whether organs can be harvested before death from
these patients whose prognosis is death should be debated urgently.
Introduction
In the commentary "Clarifying the paradigm for the ethics
of donation and transplantation: was 'dead' really so clear
before organ donation," Shemie argues in favor of the
concept of brain death (BD) being death itself, and
defends the rationale for accepting the DCD donor as
dead [1]. On more detailed examination, I suggest that his
arguments are flawed for several reasons. This commen-
tary aims to discuss the limitations of Shemie's argu-
ments, and identifies some of the persistent dilemmas
that have been overlooked. Specifically, I suggest that the
brain arrest argument shows that BD is not death, that
intensive care does replace some critical functions of the
brain, that the DCD patient is not in the irreversible state
called death, that death has always been understood as
'not capable of being reversed', and that minimizing the
information on auto-resuscitation is ill-advised. This has
enormous implications for clinical practice involving
organ donation and the diagnosis of death.
Published: 25 November 2007
Philosophy, Ethics, and Humanities in Medicine 2007, 2:28 doi:10.1186/1747-5341-2-28
Received: 7 September 2007
Accepted: 25 November 2007
This article is available from: http://www.peh-med.com/content/2/1/28
© 2007 Joffe; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Discussion
The brain arrest argument shows that BD is not death (but,
can lead to death)
Shemie suggests that "BD is better understood as 'brain
arrest' [BA], characterized by the complete and irreversible
loss of clinical brain function [1]." For Shemie, and in this
commentary, BD and BA can be used interchangeably.
Shemie writes (all italics added): "Breathing replacement
machines merely interrupt the way brain failure leads to
cardiac arrest [1]." Shemie further writes that "Advances in
organ support and replacement technologies teach us
about the mechanics of death. Survival of...the human
organism is related to adequacy of oxygenated blood
flow...There are 3 basic mechanisms [leading to death]: a)
primary cardiac arrest leading to arrest of the circulation b)
primary respiratory arrest, which via loss of oxygen causes
a secondary cardiac arrest, or c) primary BA, which via
interruption of respiratory control causes a secondary respi-
ratory then cardiac arrest. Regardless of initial disease
state, all critical illnesses threaten life in this way [1]." He
further states that life sustaining technologies are
deployed to interrupt this sequence and therefore "to
reverse the underlying life threatening state...the removal
of those applied life sustaining technologies must occur for
'natural' death and cardiac arrest to ensue [1]." Thus, by
these descriptions in defense of BD, we can conclude that
'BA' leads to death when it is allowed to result in irreversi-
ble loss of circulation. If 'BA' threatens life, and leads to
death, it follows that BA cannot be death itself. What BA
must be is a mechanism leading to death. This is compatible
with what Shemie writes in another paper: the "basic
physiological mechanism of death [in BA occurs]...via
interruption of airway control and respiratory drive cause
a secondary respiratory arrest and then cardiac arrest...
[BA] threatens life in this manner [2]." Shemie also
implies this when he writes, when referring to cardiac
arrest, that "the event may be cardiac arrest, but death only
occurs if it leads to an accompanying [permanent] loss of
circulation [1]."
To see that this is true, we should consider that the reason-
ing behind BA being a "better way" to understand BD can
be applied to other situations. For example, if we label
kidney failure as "kidney arrest", we could write that "dial-
ysis to perform the function of the kidneys merely inter-
rupts the way kidney arrest leads to death;" but, this does
not mean we are misled to consider 'kidney arrest' death.
Whether the state is named 'BD', or 'BA' (or 'kidney
arrest') does not provide a rationale for why this state is
death. Shemie's statements clearly show that BA is not
death; it will only lead to death if we stop the ventilator
and allow a secondary respiratory and then a cardiac arrest
to be followed by irreversible loss of circulation.
Misunderstanding of brain death (intensive care replaces
some critical brain functions)
Shemie writes: "ICU care does not replace any functions of
the brain...any degree of brain failure, including BD, can
be sustained indefinitely with mechanical ventilation and
vigilant care [1]." This is a problematic statement requir-
ing some background information. The standard and
accepted philosophical concept (or definition) of death is
the irreversible loss of the integration of the organism as a
whole [3,4]. In other words, when the organism is no
longer integrated as a whole, there is an irreversible pro-
gression to increasing entropy, and this state of dis-inte-
gration is death. There are said to be two medical/
biological criteria for this state of death: brain death, and
circulatory death [3]. When the brain is 'dead', some have
argued, there is irreversible loss of the integration of the
organism as a whole, and therefore this inevitably results
in irreversible circulatory arrest in a very short time, and
this is why BD is death. The bedside tests (often called 'the
criteria' for brain death) are used to determine that the
brain is dead; that is, that there is irreversible loss of the
function of the entire brain, including the brainstem.
If death is the loss of integrative unity of the organism,
then the 'BA' patient "sustained indefinitely" by intensive
care must not be dead. If the 'BA' patient (organism) can
be "sustained indefinitely" by intensive care, as has been
reported many times in the literature, then he/she must
have integrative unity, and he/she must have had brain-
stem functions (such as breathing) taken over by intensive
care [5,6]. If breathing is a function of the brain, account-
ing for the need for an apnea test in confirming BD, then
the ventilator must have taken over this function of the
brain. If temperature regulation and electrolyte balance is
a function of the brain, then the BD patient having exter-
nal warming for temperature control, and electrolyte bal-
ance maintained by desmopressin must have had these
functions of the brain replaced. This is similar to an anuric
renal failure patient having dialysis to replace the function
of the kidneys, or a diabetic patient having insulin injec-
tions to replace the function of the pancreas, both of
which "merely interrupt" the way these diseases lead to
cardiac arrest.
It is tempting to consider the brain dead patient to have
'integrative unity' that is different from the patient with
kidney failure or diabetes receiving artificial support.
However, as noted by several authors, this suggestion is
surprisingly hard to defend when one looks at the details
[6-12]. Kamm writes that "some argument would be
needed for why artificiality in cause matters when 'lower'
integrated functioning of the organism results but not
when 'higher' integrated functioning results...It is not clear
why completely replacing the component at the apex
should be different from replacing a component some-
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where else in the loop [13]." For example, a brain dead
patient can be compared to a patient with an "intact"
brain, and also to a patient with a brain only capable of
initiating infrequent ineffective breaths when the PaC02
reaches 61 mmHg. These patients are both considered
alive, because they have integrative unity. However, the
latter patient has no more integrative unity than a brain
dead patient. The breathing is just an attempt to respire,
not even enough to sustain the organism; it is not integra-
tion, just an attempt at it [13]. The integration of the
organism is present in this case independent of brain
activity, just as it is in brain death.
If 'BA' is death, there must be some concept of death other
than integrative unity that it satisfies; however, what this
concept is has never been clarified. One candidate concept
of death may be the irreversible loss of the capacity for
consciousness. Shemie suggests as much when arguing
that "it takes less than 20 seconds for cortical brain func-
tion to stop after cardiac arrest...any permanent absence of
brain blood flow beyond 20 seconds will lead to perma-
nent absence of brain function [1]." If it is true that death
is the irreversible loss of the capacity for consciousness,
then we should be willing to consider the patient in an
irreversible vegetative state at "the point in time after
which consequences occur." This means we should bury
or cremate or autopsy or harvest organs from patients in
an irreversible vegetative state, while breathing and mov-
ing but without consciousness [7]. Clearly, and in all
countries, this concept of death fails, and we are left with
the persistent problem of somehow finding a concept of
death that can allow BD to be a criterion for death.
Avoiding the issue of the irreversibility of death of the
organism (focusing on the cell)
Shemie makes some statements about cellular death that
at first seem relevant to the discussion about death, but on
reflection are not. He discusses that "the complete and
irreversible cessation of all cell life has become increas-
ingly indefinable," and "that at the cellular level, 'irrevers-
ible cessation of the entire brain' is elusive [1]." He later
writes "The so-called time of death has always been an
arbitrary moment within an overlapping segment of
decreasing vital functions and increasing quantity of cell
death. No matter how convenient it is to assume that
death and life are opposite and that a patient is either
dead or alive, the process of death is a gradual event where
organs and cells die at different rates, depending on their
resistance to the lack of oxygen. As a result, the biology of
death cannot be a moment... [1]." These statements about
cellular death are generally interesting, but are devoid of
information relevant to determining the death of the
organism. The problem is that these variable times of
death of each cell are not directly related to the concept of
death of the organism. The time of death is that moment
when the organism is dead and hence no longer alive;
conceptually, it is the moment when there is irreversible
loss of integrative unity of the organism. The variable
times of death of each cell do not mean that death of the
organism is "an arbitrary moment."
We are being misled to believe that when defining a
moment of death of the organism the requirement is that
all the cells of that organism have undergone necrosis.
Shemie implies that this is what critiques of DCD and BD
require as the "line of 'unequivocal death'." I do not
believe that this has been required by the literature
describing concerns about DCD or BD. What has been
required is that the organism that is dead is in an irrevers-
ible state of no circulation such that the organism has lost
integrative unity. Pointing out that at the cellular level not
all cells have undergone necrosis when death has occurred
is not contributing to the discussion about death at the
organism level. This interesting information detracts from
the real issue: when has irreversible loss of integration of
the organism occurred? At present, we know that this has
occurred when there is an irreversible loss of circulation.
There may be other criteria for death; however, what these
are, and how to justify them is unknown. If BD or DCD
patients are dead, they must satisfy some concept of death
other than the "irreversible loss of the integration of the
organism as a whole;" however, this new concept of death
has not been described to date.
The issue of the irreversibility of death (irreversible usually
means 'not capable of being reversed')
Shemie suggests that death as a biological event "is rela-
tive to the context [in which it occurs]." For example, "the
ability to restore the circulation depends on the location
of the [cardiac] arrest, a predetermined ethical decision
regarding level of medical intervention, the types of inter-
ventions available..., and the types of interventions actu-
ally used [1]." By this, he means "the issue is not whether
the body or brain circulation and function can be resumed
(because it can), but rather, whether it will be [1]" (i.e. the
present state of death is contingent on a predicted future
event, suggesting backward causation [14]). What Shemie
does not do is defend this point of view. He has simply
implied that he accepts this weak construal of irreversible
loss of circulation. This means that purported permanent
cessation of circulation is equivalent to the irreversible
state of death. Why we should accept this weak construal
of irreversible is nowhere discussed or defended, other
than stating that "DCD in particular, has by necessity
enhanced the rigour of the determination of death [1];"
this, by clarifying that we mean permanent loss of circula-
tion which occurs at 2 minutes in Pittsburgh, 5 minutes in
Canada, 10 minutes in some places in the United States
and United Kingdom, and 20 minutes in Sweden [15-18].
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One can argue that this clarification was developed solely
for organ donation (utilitarian) purposes.
The ethical concern of when to declare a person dead, with
irreversible cessation of circulation, is central to the debate
regarding DCD. Many authors have argued for a weak
construal of irreversibility, whereby the state will not be
reversed (i.e. there is a "do not resuscitate" order and car-
diac auto-resuscitation is not possible) [15,16]. This con-
strual is weaker than generally stated because it is actually
based on the premise that loss of circulation ought not be
reversed, rather than will not be reversed. Others argue for
a stronger construal, whereby the state cannot be reversed
even if resuscitation is attempted [14,19,20]. With resus-
citation attempted, absent circulation for over 10 minutes
can be reversed and not result in death or BD. By the weak
construal of irreversibility, patients in the identical physi-
ological state are dead or alive based on their location and
prediction of a future event (attempted resuscitation).
What needs to be decided is if it is sensible that one
patient whose heart has stopped for 2 minutes (in Pitts-
burgh) or 5 minutes (in Canada) is pronounced dead for
organ donation, while another identical patient whose
heart has stopped for 5 minutes and then has CPR is not
pronounced dead and survives. The commonly held
meaning of irreversible is 'not capable of being reversed;'
this means that after 10 or 15 minutes of absent circula-
tion, without the intention to intervene, the patient's prog-
nosis is death, and their physiological state is dying [14]. It
seems that the prognosis of death has been confused (or
conflated) with the diagnosis of death. Admitting that one
can reverse the process of death is an admission that the
individual is not dead. Is a drowning man dead because
no one will swim out to save him? Or is he merely going
to die?
Was dead really so clear before organ donation? (the
irreversibility of death was)
Shemie writes that "the so-called time of death...is and
always has been a line within an overlapping segment of
decreasing cell functions and increasing cell death... [1]."
The title of Shemie's commentary asks "Was 'dead' really
so clear before organ donation [1]?" I suggest that the
notion of death was clear before organ donation.
Shemie writes that in diagnosing death in the past "Obser-
vation and confirmation was not required and the irre-
versibility of death was not a practical concern, although
diagnostic errors were made [1]." Acknowledging that "diag-
nostic errors were made" shows that what death is has
been clear in the past. Outside the context of organ dona-
tion, when one was claimed to be dead based on the irre-
versible loss of circulation, if the patient was subsequently
revived (by auto-resuscitation or by intervention) and
clearly alive, one simply had to admit that the pronounce-
ment of death was incorrect. I do not believe that in this sit-
uation one would continue to insist that the diagnosis of
death was correct, and that somehow the patient was
revived from the irreversible state known as death. This
shows that death in the past was understood as an irre-
versible state of dis-integration of the organism. However,
in the context of DCD, we are now forced to "enhance the
rigour of the determination of death," and would in this
situation of revival have to explain somehow that the
patient in the irreversible (or "permanent") state 'death'
has now somehow become alive. I do not know how pro-
ponents of DCD would explain this.
Auto-resuscitation (it cannot be dismissed so easily)
Two claims are made regarding resuscitation. First, She-
mie claims that "the limits of brain resuscitation are com-
monly quoted as 4–10 minutes [1]." While this may be
common teaching, it is inaccurate. The literature shows
that in animals and humans, absent circulation for over
10–15 minutes can be followed by resuscitation without
BD. This is not just survival of individual cells, it is sur-
vival of the organism as a whole without the state of BD
occurring. For example, Hossmann et al report a cat who
survived with integrative neurological function after one
hour of global cerebro-circulatory arrest at normothermia
[21], and Kolata reported that 80% of 10 rabbits with
brain ischemia for 20 minutes and 75% of 4 rabbits with
brain ischemia for 30 minutes survived [22]. It is interest-
ing that these animals were given heparin after the
ischemia, something done for DCD donors that may pre-
vent injury to the brain. A study in Spain of combined in
and out of hospital arrests showed the following mortality
at hospital discharge with <4 min, 4–10 min, 10–20 min,
and >20 min delay to start of CPR: 56.5%, 61.1%, 81%,
and 100% [23].
The second claim is that "no autoresuscitation after with-
drawal of life sustaining treatment has been described
beyond 2 minutes in the absence of CPR suggesting that
the provision of CPR is a confounding condition [1]."
This claim merits careful scrutiny. There are many cases of
autoresuscitation described in the literature, and some
have indeed been hampered by inadequate monitoring
[24]. Some cases have had constant EKG monitoring with
constant observation; 6 of these had autoresuscitation at
5–8 minutes after absent circulation and asystole (imply-
ing also absent brain blood flow) (Table 1) [25-30]. Some
cases have had arterial line monitoring in addition to con-
tinuous EKG and observation, with 3 of these having
autoresuscitation at 3–5 minutes after absent circulation
and asystole (Table 1) [31-33]. Some cases with inade-
quate monitoring but with constant observation were
found to have autoresuscitated 8–10 minutes after absent
circulation with asystole (Table 1) [34-36]. It has been
hypothesized that these cases may be due to reversal of
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auto-PEEP once ventilation is stopped, or delayed delivery
of resuscitation drugs to the heart. These hypotheses seem
inadequate to account for the time delay of several min-
utes before autoresuscitation has occurred [37]. Auto-
PEEP resolves within seconds of stopping ventilation, as
shown by studies documenting lung derecruitment within
seconds of disconnection from a ventilator [38]. Drug
delivery to the heart during asystole is difficult to explain.
Attributing all the autoresuscitation cases to CPR may be
ill-advised considering that there have been no prospec-
tive studies.
Shemie claims that autoresuscitation after withdrawal of
life sustaining treatment in the absence of CPR has never
been described [1]. This is based on data from studies that
will be scrutinized here [see Additional file 1] [39-43].
This data is limited by: poorly described patient selection
criteria, no description of whether there was continuous
clinical monitoring other than EKG, no arterial line mon-
itoring, many patients who did have resuscitation
attempts, and only 5 cases where EKG monitoring was stated
to have continued more than 2 minutes after loss of cardiac
activity [39-43]. A more recent report of 12 patients who
had withdrawal of ventilation after catastrophic brain
injury showed that 2 "showed a salvo of 5 to 20 heartbeats
1.23 and 6 minutes after asystole, followed by EKG
silence. An arterial catheter in two of these patients did
not record measurable tracings during the cardiac activity.
Four recordings showed broad undefined complexes after
5, 7, 9, and 10 minutes after initial cardiac arrest... [44]" A
report from Pittsburgh on 15 DCD patients stated that
"after 2 mins monitor activity was not recorded, so contin-
uously recorded data after this time are not available
[45]." This information suggests that the data is not ade-
quate to state that autoresuscitation is "extremely rare and
is likely negligible [1]."
Laying my cards on the table
I have argued that brain death is not death itself. It is a
devastating neurological state with a dismal prognosis,
but not death. I agree with Shemie that it leads to death
when (and only when) ventilation is stopped, and there-
fore breathing stops, followed by cardiac arrest, followed
by irreversible loss of circulation. This results in an irre-
versible state of loss of integration of the organism, and
this is death.
Further, I believe that at 2 to 10 minutes after loss of cir-
culation the DCD donor is not dead. This is because there
is not necessarily irreversible loss of circulation (i.e. loss of
circulation could still be reversed) and hence irreversible
loss of integration of the organism. When exactly this state
of irreversibility occurs is an important question. At
present this is not known; however, it is known that it is
not at even 10 minutes after cardiac arrest.
Whether I am challenging the practice of organ donation
is another question. The question is not whether organ
donors are dead (because they are not). The question is
whether organs can be harvested before death from
patients whose prognosis is death, and hence be a contrib-
uting cause of death. My argument is that this is the cur-
rent practice, and this is also precisely what needs to be
debated urgently. Is organ harvesting before death violat-
ing respect for persons and using them as a means?
Conclusion
This commentary suggests that many of the arguments in
support of BD and DCD may be questioned. If BD threat-
ens life, and leads to death, it must not be death itself. If
intensive care only interrupts the way BD leads to death,
then intensive care must take over some of the brain func-
tions, allowing the organism to be sustained indefinitely
Table 1: Selected reported cases of autoresuscitation.
Author Age (yr) Diagnosis Rhythm Min* Outcome EKG AL Obs**
Letellier [25] 80 Pulmonary edema asystole 5 normal + - +
Voekkel [26] 55 Sudden death asystole 7 death at 3 d + - +
MacGillivray [27] 76 COPD asystole 5 death 24 hr later + - +
Rosengarten [28] 36 asthma EMD 5 normal + - +
Abdullah [29] 93 sepsis asystole 5 not stated + ? +
Al-Ansari [30] 63 COPD asystole 3 normal + - +
Frolich [31] 67 MI asystole 5 normal d3; death d7 + + +
Casielles-Garcia [32] 94 hemorrhage EMD 3 death at 18 d + + +
Maleck [33] 80 sepsis asystole <5 death at d2 + + +
Quick [34] 70 hyperkalemia asystole 8 normal - - +
Ben-David [35] 66 sudden VF asystole 10 normal - - +
Monticelli et al [36] 78 MI asystole >10 death at 19 hr - - +
AL: arterial line; COPD: chronic obstructive pulmonary disease; EKG: electrocardiogram; EMD: electromechanical dissociation; MI: myocardial
infarction; VF: ventricular fibrillation. *Min: time in minutes from stopping resuscitation in the stated rhythm to return of circulation. **Obs: refers
to continuous clinical bedside observation.
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in a state of integrative unity. If the DCD donor is dead
after 2–5 minutes of cardiac arrest, then patients in iden-
tical physiologic states actually are dead or alive depend-
ing on the context, the state of death is contingent on a
future event (whether resuscitation is attempted), and the
commonly used meaning of irreversible as 'not capable of
being reversed' is abandoned. The literature supporting
the claim that autoresuscitation does not occur in the con-
text of no resuscitation attempts is more limited than usu-
ally acknowledged. Several cases of autoresuscitation in
the literature were well monitored and described, suggest-
ing that ignoring these cases may not be warranted. These
problems have major implications for the practice of
medicine today. I suggest that brain death is not death
itself, and that the DCD donor is not dead even at 10 min-
utes after absent circulation. Whether organs can be har-
vested before death from patients whose prognosis is death
should be debated urgently.
Competing interests
The author(s) declare that they have no competing inter-
ests.
Additional material
Acknowledgements
I have no funding source to declare.
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Additional file 1
Case series documenting lack of auto-resuscitation. The table provides
details of the studies quoted by several groups to justify the claim that auto-
resuscitation does not occur after more than 2 minutes after withdrawal
of life support. The limitations of these studies are described in the table.
Click here for file
[http://www.biomedcentral.com/content/supplementary/1747-
5341-2-28-S1.doc]
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