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. 2016 Apr 18;41(3):279–299. doi: 10.1093/jmp/jhw006

Deconstructing the Brain Disconnection–Brain Death Analogy and Clarifying the Rationale for the Neurological Criterion of Death

Melissa Moschella 1,*
PMCID: PMC4889817  PMID: 27095749

Abstract

This article explains the problems with Alan Shewmon’s critique of brain death as a valid sign of human death, beginning with a critical examination of his analogy between brain death and severe spinal cord injury. The article then goes on to assess his broader argument against the necessity of the brain for adult human organismal integration, arguing that he fails to translate correctly from biological to metaphysical claims. Finally, on the basis of a deeper metaphysical analysis, I offer a revised rationale for the validity of the neurological criterion of human death.

Keywords: Alan Shewmon, brain death, determination of death, neurological criterion of death

I. INTRODUCTION

“The brain destruction versus brain disconnection comparison was the epiphany that directly occasioned in 1992 my radical change of opinion about the nature of brain death,” writes Alan Shewmon (2012, 448–449; see also Shewmon, 2011, 30–31). Shewmon, who had previously argued for the validity of the neurological criterion for death, and even for moving beyond a whole-brain definition of death to a higher-brain definition of death (Shewmon, 1985), has since become one of the most influential critics of the neurological criterion for death. His criticism is based fundamentally on his belief that, as long as circulation and respiration continue (with the assistance of a ventilator), a patient with total and irreversible brain failure is still a living human organism as a whole. As indicated in the statement quoted above, Shewmon’s skepticism about the validity of the neurological criterion for death was sparked by his observation of the striking similarities between patients whose brains are alive but functionally disconnected from the rest of their bodies (due, for instance, to high cervical spinal cord transection), and patients whose brains have irreversibly ceased to function (i.e., “brain dead patients”). Most notably, in both cases circulation and respiration would cease without ventilator support. In the following syllogism, Shewmon (2010, 259) summarizes the argument against the validity of the neurological criterion 1 (NC) for human death that is based on this comparison:

  • 1.

    A functionally brain-disconnected patient on a ventilator in an intensive care unit (ICU) (e.g., from high spinal cord transection or extreme Guillain–Barré syndrome) is a severely disabled organism as a whole, not just a conscious head connected to an unintegrated collection of organs and tissues enclosed in a bag of skin.

  • 2.

    The somatic effects of brain nonfunction are necessarily identical to those of brain disconnection.

  • 3.

    Therefore, a patient without brain function is also a severely disabled organism as a whole (merely an unconscious one).

This argument, based on the purported somatic equivalence between brain destruction and brain disconnection, is an important one in the debate over the validity of NC. Shewmon refers to this argument frequently as “definitive” and “decisive,” or as “a trump card” that defeats all other objections (Shewmon, 1998, 258; see also Shewmon, 2010, 259; Shewmon, 2012, 449), and many experts on brain death agree (McMahan, 2002, 433–434; see also the references in Shewmon, 2012, 449). He sees it as a “trump card” in the sense that he believes it allows one to bypass the need to examine in detail the somatic functions and dysfunctions of the brain dead body (BDB) in order to determine the validity of the neurological criterion for human death. Shewmon sees the need to play this “trump card” because, from a metaphysical and biological perspective, many scholars have argued that the “litany of integrative functions” (Shewmon, 1998) exhibited by BDB’s 2 in exceptional cases is not actually evidence of self-regulated integration beyond the tissue level (Condic, 2016; Eberl, 2011, 53–61). Thus a serious engagement with this “trump card” argument, which I will refer to as the Brain Disconnection–Brain Destruction Analogy, is crucial.

Shewmon claims that “the standard rationale for brain death would have us say that the spinal cord victim is a conscious nonorganism, which doesn’t make a whole lot of sense” (2011, 31). I agree with Shewmon that there are serious biological and metaphysical problems with calling a high cervical spinal cord injury (SCI) patient a nonorganism, but I disagree that the standard rationale for brain death—that the brain is necessary to maintain organismal integration (Bernat, Culver, and Gert, 1981)—entails that conclusion.

In what follows (Section II), I will first offer a critique of the Brain Disconnection–Brain Destruction Analogy that ultimately brings us back to the need to engage in a direct metaphysical analysis of the status of the BDB. Then, in subsequent sections of the article, I will outline the key metaphysical principles 3 required for determining the status of the BDB and, on the basis of those principles, I will (1) suggest that Shewmon’s argument that BDB’s are organisms because they exhibit integrative functioning rests on a failure to translate correctly from biological facts to metaphysical claims (Section III); (2) offer a revised criterion for what distinguishes an organism from a nonorganism (Section IV); and (3) propose a revised rationale for the soundness of the total brain death criterion for human death—namely, that total brain death is death because it marks the irreversible loss of the material basis of both the capacity for spontaneous breathing and the capacity for sentience (Section V). 4

II. EVALUATING THE BRAIN DISCONNECTION–BRAIN DESTRUCTION ANALOGY

Problems with the Logical Structure of the Argument

I begin my analysis of the Brain Disconnection–Brain Destruction Analogy by evaluating the logical validity of the argument as a whole. On close examination, it becomes clear that the argument is not logically valid—that is, that the conclusion is not logically entailed by the premises, because a true middle term is lacking. To make this transparent, allow me to restate Shewmon’s argument in simplified (and more precise) form:

P1: A brain disconnected patient is an organism.

P2: The somatic effects (on the body below site of the transection) of brain disconnection are identical to the somatic effects of brain nonfunction.

Conclusion: A brain dead patient is an organism.

Putting the argument this way (which simply removes superfluous words and clarifies Premise 2 to make it plausible and nonquestion-begging in a way that seems to be faithful to the intended meaning), the lack of a middle term that connects “brain disconnected patient” and “brain dead patient” is transparent. For the argument to be valid, Premise 2 would have to be revised as follows:

P2revised: A brain disconnected patient is biologically equivalent to a brain dead patient.

P2revised, however, is obviously false, because a brain disconnected (i.e., SCI) patient has a living brain, and a brain dead patient does not.

It could be countered that this problem—that is, the lack of a middle term and the subsequent need for revision of P2—only arises because of the minor modification I have made to P2 by specifying that the somatic effects being considered are the effects on the rest of the body (below the brain stem or the site of the transection). This modification, however, really is a genuine clarification rather than the building of a straw man. Indeed, it is a charitable reading of P2, the only reading on which P2 is both plausible and nonquestion-begging. After all, Shewmon obviously does not mean that brain disconnection and brain nonfunction are equivalent in every respect, or that they are equivalent in their effects on the head/brain. Therefore, he must mean that the somatic effects (on the rest of the body) of two different physical impairments (brain disconnection and brain nonfunction) are the same, a claim which at least in some cases is plausible. And if that is in fact what Shewmon meant, then the argument is logically invalid.

A Revised Version of the Brain Disconnection–Brain Destruction Analogy

Yet despite being articulated in logically invalid form, Shewmon’s argument is obviously getting at an important point. In this section, I rearticulate the Brain Disconnection–Brain Destruction Analogy in what I consider to be its strongest form—that is, as a reductio ad absurdum argument, a form of argument which tries to show that one’s own view is true by showing that the opposing view leads to an absurd conclusion. I will then show why the argument nonetheless fails. In reductio form, we could articulate Shewmon’s argument as follows:

Brain disconnection reductio argument

P1: Let us suppose that, as some claim, the BDB is not a living organism because the brain is necessary for organismal integration.

P2: Now, consider the fact that the body of an SCI patient below the site of the transection is disconnected from the brain and therefore functionally equivalent to a BDB.

If Premise 1 is true, it follows that the body of an SCI patient (below the site of the transection) is not a living organism.

But an SCI patient is obviously a living human being (and therefore an organism); the conclusion must be false. Since the argument is logically valid, if the conclusion is false, one of the premises must be false. P2 is true; therefore, P1 must be false.

In other words, it is the indubitable fact that the SCI patient is a human being, combined with the Aristotelian-Thomistic philosophical view that all human beings are organisms, that gives the Brain Disconnection–Brain Destruction Analogy its persuasive force. For it would seem that denying the claim that a BDB on life support is a living organism as a whole 5 would then also require us to deny that the SCI patient is a living organism as a whole: an absurd conclusion.

Yet this is a false dilemma. For it can be true (as I think it is) that an SCI patient “is a severely disabled organism a whole,” even if it is not true that the body below the site of the transection is a proper part of that organism. In other words, in the case of an SCI patient, the “organism as a whole” could be constituted by the head alone, not the head and brain-disconnected body together, because the brain is the material basis of the root capacity for autonomous organismal integration, 6 and the brain continues to have control over the rest of the head, while the body below the transection, since it is disconnected from the brain, lacks the material basis of that root capacity. Of course, I have not yet proven that this interpretation of the metaphysical status of the SCI patient is true; for now I simply propose it as a plausible alternative to show that it is logically possible to hold (1) that BDB is not an organism and (2) that the SCI patient’s body below the site of the transection is functionally equivalent to a BDB (a claim which is in itself doubtful) 7 without being logically committed to the position that the SCI patient is not an organism either.

Since, as I will argue later, the brain-disconnected (or brain dead) body lacks the material basis of the root capacity for autonomous organismal integration, 8 it is therefore strictly speaking neither a separate independent organism nor a proper part of the patient’s overall organism, but rather a collection of organs and tissues that are functionally coordinated with each other and with the brain/head through external agents (mechanical ventilation, pharmacological treatments, etc.). 9 Conversely, as I will also argue later, a living brain, even if largely disconnected from what used to be the rest of the body, does retain the material basis of the root capacity for autonomous organismal integration, and is therefore itself an “organism as a whole,” though a severely disabled one. If I am right that a disconnected head is itself an organism, and if we take seriously Shewmon’s claim that the brain-disconnected body is the equivalent of the BDB, then we would actually end up having to conclude that in an SCI patient there are two severely disabled “organisms as a whole”: the head, and the body below the site of transection. Ironically, then, the reductio ad absurdum could work both ways, depending on one’s view of the metaphysical status of the disconnected head.

Thus, the similarities that exist between a BDB and an SCI patient’s “body” below the site of the transection do not necessarily give us any clear insight at all about the metaphysical status of the BDB. The fact that neither BDB nor SCI patients can breathe on their own due to the death of the brain (in the case of the BDB) or its disconnection from the body (in the case of the SCI patient) may simply mean that neither the BDB nor the “body” of the SCI patient below the point of transection are integrated organisms as a whole (in the case of the BDB) or proper parts of integrated organisms as a whole (in the case of the SCI patient).

In other words, the Brain Disconnection–Brain Destruction Analogy, either in original or revised form, is simply not the trump card that Shewmon takes it to be. Rather, the above consideration of the analogy’s limitations shows that determining the metaphysical status of the BDB requires a direct metaphysical analysis (informed by biological fact) regarding the necessary and sufficient conditions for being a human organism, and an application of that analysis to the difficult case of the BDB. The BDB is sui generis, and therefore no comparison of the BDB to other cases (like that of an SCI patient) can definitively resolve the question about the BDB’s status.

III. LOST IN TRANSLATION: THE FAILURE TO TRANSLATE CORRECTLY FROM BIOLOGICAL FACTS TO METAPHYSICAL CLAIMS

Section II shows that the Brain Disconnection–Brain Destruction Analogy fails. It is therefore not the definitive argument against the validity of the neurological criterion (NC) for human death that Shewmon takes it to be. Yet the failure of this one argument does not show that Shewmon is wrong overall in his criticism of NC. Even without this “trump card,” Shewmon might still have a winning hand, based on the aforementioned “litany of integrative functions” exhibited by BDBs (Shewmon, 1998). I am not persuaded, however, that the functions exhibited by the BDB are actually signs of integration in the requisite sense—that is, in the sense that would indicate that the BDB is itself an organism as a whole rather than an aggregation of organs and tissues inside a bag of skin, maintained in a coordinated relationship with one another through the action of external causes. I will leave it to the scientists to criticize the persuasiveness of Shewmon’s evidence from a biological perspective. Here I will criticize it from a philosophical perspective, and in doing so offer a revised rationale for the validity of NC.

Metaphysical Presuppositions

On an Aristotelian-Thomistic hylomorphic account, it is the form or soul that is the cause of the unity of a living being. The soul is in every part of that being, and it is the source (as formal principle) of all of that being’s actions, operations and capacities (root capacities as well as immediately exercisable capacities) (Aquinas, Questiones Disputatae de Anima (QDA) a.10, Summa Theologiae (ST), I., q.76, Summa Contra Gentiles (SCG) II, 72). Every living being has one, and only one soul, one substantial form that accounts for the unity, essential identity and integrated functioning of the organism. Each human being has one soul, a rational soul, that makes the body be a body (as opposed to an aggregation of molecules) and be a human body (Aquinas, QDA, a. 11; ST I, q. 76, a. 3; SCG, II, 58). The rational soul is the formal principle of the unity and essential identity of the human person as a psychophysical substance, and the source (as formal principle) of all of the human being’s actions, operations, and capacities, ranging from vegetative functions like metabolism and homeostasis to rational activities like engaging in a philosophical dispute. Since, for humans, it is the rational soul that is the formal principle of self-directed integrated functioning, the presence of self-directed integrated functioning (or of the material basis of the root capacity for such functioning) is sufficient evidence 10 for the presence of the rational soul. Conversely, since the soul that is the principle of organismal unity is the same soul that is the principle of sentient/rational activities, evidence of sentient/rational capacities (either in immediately exercisable or root form) is also sufficient evidence for the presence of the whole human soul, including the soul as principle of organismal integration. I take these basic metaphysical ideas to be common ground among both critics and defenders of NC from a hylomorphic metaphysical perspective.

A Metaphysical Critique of Shewmon’s Claim that a BDB is an Organism

Translated into metaphysical terms, Shewmon’s positive argument for the claim that the BDB is an organism as a whole is that the “litany of integrative functions” present in some BDBs are sufficient evidence for the presence of the human soul. As always when moving from one level of discourse to another—in this case, from the biological to the metaphysical—special care is necessary to ensure that nothing is lost in translation. The key concept that we have to be particularly careful not to employ equivocally when translating from biological observations to metaphysical conclusions is the concept of “integrative function,” also referred to by Shewmon as the possession of “emergent, holistic-level properties” (2001, 460; restated in 2012, 469), which he believes is sufficient, together with enclosure within a continuous membrane, to show “integrative unity.” Translated into metaphysical terms, Shewmon thinks that any putative organism really is an organism—that is, really has a single soul animating, organizing, and unifying it—if it is enclosed by a continuous membrane and possesses at least one emergent, holistic-level property. Since the soul that animates the human body is a rational soul, Shewmon thinks that BDBs’ possession of emergent, holistic level properties within a closed membrane is an indication that BDBs possess rational souls and are therefore living human beings.

In his 2012 article, Shewmon employs a different framework that appears to be an attempt to clarify and add more nuance to the previous one. Shewmon distinguishes among five different levels of integration: organism level integration, body system integration, organ level integration, cell-level integration, and cellular organelle level integration (2012, 430–431). Using this terminology, the evidence we would need to show that a BDB is an organism as a whole, rather than just a collection of organs and body systems in a bag of skin, is organism level integration. 11

The question then becomes: what are the criteria by which we can determine whether or not a putative organism actually possesses organism level integration—that is, actually is an organism? In order to answer this question, Shewmon shifts from the discussion of levels of integration to a discussion of types of integration: life-constituting (constitutive) integration, which “makes a body simply to be alive and to be a whole” (Shewmon, 2012, 435), versus life-sustaining integration, which only helps a body stay alive, and which he distinguishes into two types: health maintaining and survival promoting (438). He goes on to claim that, unlike health-maintaining and survival-promoting integration, constitutive integration is nonreplaceable, meaning that, in the absence of constitutive integration, the organism cannot survive even with the help of external agents like mechanical ventilation, antibiotics, insulin, vasopressors, etc. His strategy is then to show that “all brain-mediated somatic integration is either of the health-promoting or of the survival-promoting type” by showing that it is replaceable, thus implying that it is not of the constitutive type (441).

In the midst of this complex theoretical apparatus, however, the key metaphysical questions are unfortunately obscured. Shewmon simply asserts that constitutive integration is nonreplaceable, yet this claim, like the concept of constitutive integration itself, is highly ambiguous. It seems that the concept “constitutive integration” in Shewmon’s argument effectively plays the role of the concept “soul” in Aristotelian-Thomistic metaphysics. This is evident in his definition of constitutive integration as the type of integration that “makes a body to be alive and to be a whole” (Shewmon, 2012, 435), a definition equivalent to the Thomistic-Aristotelian definition of soul. Thus, to possess constitutive integration is to possess a soul, and therefore to be a unified whole. Noting the conceptual equivalence of “constitutive integration” and “soul” also makes sense of Shewmon’s assertion that constitutive integration is nonsubstitutable even in part: “By its very nature, if it [constitutive integration] does not exist at a given hierarchical level, neither does the corresponding organism, organ or cell exist. . . . Constitutive integration is all or none, just as ‘unity’ is all or none” (440). The word “constitutive integration” can be replaced by the word “soul” in each of these sentences—and, indeed, making the replacement actually clarifies what Shewmon is getting at from a metaphysical perspective and helps to explain how he can so confidently assert (without argument) these particular characteristics of constitutive integration. 12

Shewmon then goes on to make the claim—a claim which turns out to be more crucial to his argument than is initially apparent—that “no futuristic intensive-care technology can prevent the increase in entropy (i.e., biological decay) if it is not endogenously opposed from the very life-processes themselves of the living organism” (Shewmon, 2012, 440). What he is saying, in other words, is that unless an organism is alive (unless it possesses a soul/constitutive integration), no amount of technological intervention can prevent the remains of that organism from undergoing biological decay. He treats this claim as if it followed logically from the prior claims about constitutive integration (the soul) as the cause of organic unity. Yet this claim neither follows logically from the prior claims, nor is true biologically or metaphysically.

For instance, a “lung” 13 ex vivo which has already begun the process of biological decay (indicating that it now lacks unity, since it is incapable of endogenously opposing disintegration) can be maintained through external causes (perfusion with nutrients, proteins, and oxygen), reversing the damage caused by the incipient decay and preventing further decay until the “lung” can be transplanted (Okamoto et al., 2010). This shows that increase in entropy can be successfully opposed through exogenous factors even when, as evidenced by the incipient decay, endogenous antientropic mechanisms of the organ as a whole are absent.

Metaphysically speaking, Shewmon’s claim that technology cannot prevent entropy unless the soul is still present is problematic because it rests on a misunderstanding of the difference between internal and external principles of unity. The soul is an internal principle of unity, and therefore, in the absence of the soul, the root capacity for internally-directed integration or self-integration is lacking. To put this positively, from a metaphysical perspective the soul is present if and only if a root capacity for self-integration is present. Shewmon would agree with all of the above statements. What his understanding of self-integration seems to lack, however, is the specification that to be self-integrated, an organism must control and direct its essential vital functions.

Why is this specification necessary, and what precisely does it mean? Consider the claim that an embryo is a whole (though immature) human organism. This claim is based on the biological observation that, beginning at sperm–egg fusion, the new organism directs itself toward maturity and controls its own vital functions. The support that an embryo receives from the mother’s body—nutrition, oxygen, protection from external threats—is essentially no different from the external support that any organism needs in order to live. No external agent controls or directs the vital functioning of the embryo. This is the crucial point in the argument that the embryo is an individual organism as a whole, not merely a part of the mother. Thus, returning to the basic metaphysical presuppositions asserted in Section III, the fact that the embryo controls and directs its own vital functioning provides sufficient evidence for the presence of the human soul.

Shewmon’s argument implicitly denies the claim that self-integration requires control over one’s essential vital functions. This is what enables him to claim that a BDB, maintained with the help of a ventilator, is self-integrated. I grant that the biological evidence provided by Shewmon shows that the cells, organs, and tissues of a BDB, like the cells in a “lung” ex vivo, have an internal capacity to respire (i.e., to make use of the oxygen that comes to them, thanks to mechanically induced breathing). But control over the essential vital functions of respiration and circulation requires not only the ability to make use of the oxygen, nutrients, etc., carried to the various parts of the body through circulation, but also the ability to regulate and direct that vital function oneself—i.e., the ability to breathe spontaneously.

Shewmon therefore makes a fundamental metaphysical error by stating that, in the absence of the soul, it would be impossible to prevent decay even with the help of external causes, from which he infers the positive principle that if, with the help of external causes, an entity successfully opposes decay, that entity must possess a soul. Shewmon’s 2001 criterion for distinguishing organisms (living beings vivified and unified by a single soul) from nonorganisms—the presence of at least one emergent, holistic property within an enclosed membrane—suffers from exactly the same problem: he presumes that if internal causes of emergent, holistic properties are lacking, those properties cannot result from external causes, forgetting (or denying) that self-integration requires control over essential vital functions. 14

Shewmon might respond to this criticism by claiming that a BDB does have control over essential vital functions, returning to his claim that if an entity can oppose entropy, even with the help of medical technology, this means that the entropy is being opposed from internal causes, and thus that internal control of vital functions is present. He would claim, in other words, that unless the soul is present, even the most advanced medical interventions will not succeed in functionally integrating that entity. As mentioned before, however, I see no reason why we should believe that this claim is true. Of course, in the case of a BDB the degree of functional integration that can be maintained in some cases with the help of mechanical ventilation and pharmacological interventions would not be possible if the organs, tissues, and cells that make up the BDB did not retain any of their own internal capacities and “programming,” developed when they were proper parts of the organism as a whole, in the service of the organism as a whole. But the fact that an external cause can, by replacing the capacity for spontaneous breathing, trigger 15 the internal capacities of a multitude of living entities that used to be parts of a whole in such a way that those entities can continue to exhibit some degree of functional coordination, thus maintaining functional integration and successfully opposing entropy, does not imply that genuine self-integration is present.

Thus, even granting that Shewmon is right when he claims that “the empirical evidence suggests that all brain mediated somatic integration is either of the health-maintaining or of the survival-promoting type” (Shewmon, 2012, 441; see also 457), by which he means that external causes can substitute for them, there is still insufficient evidence to show that a BDB is an organism as a whole informed by a single rational soul. Metaphysically, the soul is the principle of self-integration, which requires control of one’s vital functions. The fact that the integration of which the soul is the formal principle can be maintained (to some degree) by external causes (with the help of the internal capacities of the cells, organs, and tissues that make up the BDB) does not show that the soul (the internal cause of integration) is still present. And thus the fact that the integrative functions of the brain—understood as the primary organ through which the soul acts to integrate the body in humans beyond a certain stage of development—can in some cases be replaced with the help of external causes, likewise does not show that the soul can continue to be present when all brain function has irreversibly ceased.

IV. A REVISED CRITERION TO DISTINGUISH ORGANISMS FROM NONORGANISMS

On the basis of the foregoing discussion, I propose the following as a necessary and sufficient condition for being a living organism:

A putative organism really is an organism if it possesses the root capacity for self-integration. Possession of the root capacity for self-integration (of which the soul is the principle) is evidenced by (1) possession of the material basis of the capacity for self-integration—i.e., the capacity for control of respiration and circulation—or (2) possession of the material basis of the capacity for sentience. 16

This criterion specifies three crucial things that Shewmon’s original criterion omits, and thus enables us to avoid the metaphysical confusions to which the applications of Shewmon’s criterion has led. The revised criterion specifies, first, that to be an organism an entity must have the root capacity for self-integration. This helps us to make the crucial distinction between those who temporarily rely on life-support systems until the body has sufficiently recovered from a trauma (the effects of which amount to a kind of external blockage of the ability to exercise the capacity for self-integration, the material basis of which is nonetheless still present) to be able to direct its own integration once again, and a BDB which will never again be able to direct its own integration—most essentially, never again be able to breathe spontaneously—because it has irreversibly lost the material basis of the capacity to breathe on its own. It also helps us to explain why the head of the high cervical SCI patient can itself be understood to be an organism as a whole (though a severely mutilated one), not only because the SCI patient maintains the capacity for sentience, but also because in the SCI patient the brain’s inability to integrate the rest of the body is due to external causes (the severing of neuronal pathways), not to an inner impairment, and thus there is evidence that the material basis of the active dynamism or potency toward integration of the rest of the body remains (and therefore that the soul, as formal basis of that active dynamism as well as of the capacity for sentience, remains as well).

Second, the revised criterion specifies that to be an organism an entity must not only be integrated, but self-integrated—that is, the causes of the organism’s emergent and holistic properties must be internal, not external, and it further specifies that self-integration requires control of one’s essential vital capacities, especially (at least in the case of mammals) the capacity to breathe. This revision captures the crucial metaphysical truth that to be an organism is to have an internal principle of unity, rather than a mere passive potentiality to be unified by external causes. As Aquinas writes: “By vital operations are meant those whose principles are within the operator, and in virtue of which the operator produces such operations of itself” (ST, I, q. 18, a.2, ad 2; Eberl, 2011, 58–59).

Finally, the revised criterion indicates that to be an organism what is needed is the root capacity for self-integration, not the immediately exercisable capacity for self-integration or even the material basis of the root capacity for self-integration. All that is needed is the formal basis of the root capacity for self-integration—that is, the soul. As long as the soul continues to inform the body, the root capacity for self-integration remains, and we know that the soul continues to inform the body as long as the body retains the material basis for any of the capacities of which the soul is the principle—not only organismal self-integration, but also sentience (rationality, strictly speaking, has no material basis). I will elaborate on this point in the next section.

These revisions remedy the mis-translation between the metaphysical concept of “soul” and Shewmon’s concepts of “constitutive integration” (2012) and “integrative unity” (2001; 2012), a mis-translation which seems to me to be at the heart of the larger confusion involved in the rejection of total brain death as a sound criterion for human death.

V. A REVISED RATIONALE FOR THE NEUROLOGICAL CRITERION FOR HUMAN DEATH

How, then, can we really know with sufficient certainty that a human being has lost the material basis of the capacity for self-integration, as well as the material basis of the capacity for sentience, and that death has occurred—that is, that soul and body have separated because the body is no longer proportionate matter for the soul? I would propose that in fact the only way we can know with certainty that the material basis of the root capacities for self-integration and sentience have been lost is if the person has suffered total brain death. The essential vital capacity over which the organism must have control in order to be actually self-integrated is the capacity to breathe, which is controlled by the brainstem at least in post-natal stages of human life. And in mammals, the material basis of the root capacity for sentience resides in the brain (or in the genetic and structural primordial of the brain during the early stages of human development). In other words, not only is the neurological criterion for death a valid one, it is the only valid one (for humans that have developed to the point at which the brain has taken over the regulation of breathing).

In order to explain more fully the reasons behind this claim, it is necessary to go back to the key metaphysical presuppositions laid out in Section III. It is in the soul, not in any particular body part or even in all of the body parts together, that the root capacity for organismal self-integration, as well as the root capacities for sentience and rationality, reside. Indeed, it is arguably the case that even when separated from the body after death the soul retains not only the capacity for rationality (which it retains as its proper subject), but also, as their principle, the root capacities for organismal self-integration and sentience, 17 despite the fact that those capacities cannot be exercised due to defects in the matter, because the body that the soul once informed is no longer adequate to rational ensoulment. Indeed, what causes death is precisely that the matter ceases to be proportionate to the soul that unified it and made it what it is, and comes to be informed instead by a multitude of lower-level forms.

The question that concerns us here is how we can know that this substantial change has taken place—that is, how we can know that the matter is no longer proportionate to rational ensoulment, and therefore that it no longer materially constitutes a human body, despite retaining the external appearance of a human body for quite some time. As mentioned earlier, the soul is the principle of a human being’s capacities at all levels—vegetative (organismal self-integration), sentient, and rational. Therefore, we have sufficient evidence for the presence of the soul if we have evidence of the existence of the material basis of the capacity for organismal self-integration or the capacity for sentience. 18 Conversely, we have sufficient evidence for the absence of the soul if we have evidence that the material bases for both organismal self-integration and sentience are entirely and irreversibly lacking, for if the material prerequisites for all levels of human functioning are lacking, that means that the matter is no longer adequate to rational ensoulment, and therefore that the soul has left the matter that it used to inform and unify.

Thus we come to my revised rationale for NC.

Rationale for the Neurological Criterion of Death

The reason why NC is the only valid criterion for death is that only after total brain death can we be certain that a human being has irreversibly lost both (1) the material basis of the capacity to breathe—that is, the capacity to control the essential vital capacities of circulation and respiration and (2) the material basis of the capacity for sentience. (Note that the capacity for rationality is excluded because the principle of conceptual thought is immaterial. 19 ) Only after we are certain that the material basis for both vegetative and sentient functioning have been irreversibly lost can we be certain that there is no longer proportionate matter for rational ensoulment, and thus that soul and body have separated—that is, that death has occurred.

I will examine the two aspects of this rationale one at a time. First, how do we know that the material basis for self-integration is lost when the whole brain is dead, and, specifically, why is loss of the material basis of the capacity for control of circulation and respiration sufficient evidence that the material basis for self-integration is lost? Eberl explains that

a human body’s having control over its vital functions of circulation and respiration is a necessary criterion for it to have integrative unity; these specific activities are the vital functions necessary for somatic integrative unity insofar as all other organs of the body depend upon oxygenated blood circulating through them in order to survive and function. (Eberl, 2011, 61)

It is the brain stem, specifically, that controls these vital functions. Therefore, as long as the brain stem remains alive, the material basis of the capacity for regulation of circulation and respiration remains, even if external causes (like high cervical spinal cord transection) render the person unable to exercise that capacity. Conversely, if the brain stem is dead, the material capacity for self-regulation of circulation and respiration has been irreversibly lost.

In a sense, my claim about circulation and respiration as the essential vital capacities could be seen as a rapprochement between defenders of NC and defenders of the circulatory-respiratory criterion (CRC) of death. Defenders of CRC claim that, from a biological perspective, circulation and respiration are the sine qua non of organismal integration. As Shewmon notes after discussing the “litany of integrative functions” found in a BDB:

Both circulation and respiration (in the technical, biochemical sense linked with energy generation) are presupposed as means to many, if not all, of the above functions. In the sudden absence of either, the thermodynamic “point of no return’“ for the organism is reached within a matter of tens of minutes (excluding anomalous contexts such as ischemia-protective drugs, deep hypothermia, suspended animation, etc.). And once past that moment, the progressive increase in entropy characteristic of inanimate matter would not be therapeutically circumventable even in theory (e.g., even by artificial perfusion of the body with oxygenated blood). (Shewmon, 2001, 469)

My explanation of the brain’s critical importance for the maintenance of human life also has the advantage of clearly highlighting that a human being is a rational animal, a unified psychophysical substance, and not just a mind or a functional brain inhabiting a body. For on this account, the brain is properly understood (for human beings beyond a certain level of development) to be the “primary organ,” not only because it is necessary for the exercise of our rational capacities, but also because it is through the brain that the soul operates to regulate and coordinate the other parts, enabling them to function integrally. 20 And the brain does so most essentially by controlling respiration and circulation, which makes possible the transmission of nutrients, oxygen, and information throughout the whole body.

The crucial difference between my view and that of Shewmon and other defenders of CRC is my claim that the self-integration required of an “organism as a whole” demands control over the capacity for respiration and circulation—that is, the ability to breathe spontaneously. 21 Thus, it is precisely because circulation and respiration are the sine qua non of organismal integration that the brain, as controller of circulation and respiration, is (beyond a certain point in human development) the sine qua non of self-integration (see also Eberl, 2011, 60–61). 22

Now I will briefly elaborate on the second aspect of my Rationale for NC, that total brain death marks the irreversible loss of the material basis of the capacity for sentience. 23 Why is this part of the rationale actually necessary? It is necessary because absence of the material basis for organismal self-integration is not sufficient evidence for the absence of the soul, given that the soul, as form of the body, is the principle not only of organismal self-integration but also of sentience. 24 Thus, if the material basis of either of those capacities remains, there is sufficient evidence to show that the soul remains. Only absence of the material basis of both the capacity for organismal self-integration and the capacity for sentience is sufficient to show that the soul is absent because proportionate matter is lacking. 25 A person who suffers serious damage to the brain stem due to a stroke or some other cause, rendering the brain stem irreversibly incapable of controlling respiration and circulation, but whose higher brain (perhaps along with other parts of the brain stem) remains functional, is not dead despite lacking the material basis of the capacity for organismal self-integration, because that person still retains the material basis of the capacity for sentience. Even if this brain-stem-damaged person is in an “irreversible” 26 coma, and thus lacks the immediately exercisable capacity for sentience, the fact that the higher brain is still alive means that the material basis of the capacity for sentience remains, and thus that the soul remains because there is proportionate matter for the soul to inform (or at least that we lack sufficient evidence to be sure that proportionate matter is lacking). Note that such a person would not lack the root capacity for organismal self-integration (which remains virtually present in the soul as principle of that capacity), but only the material basis of the organismal capacity for self-integration. Thus, a patient in such an unfortunate condition can still be truly called a rational animal, though a severely disabled one.

VI. CONCLUSION

In conclusion, total brain death is death because total brain death marks the loss of the material basis of the capacity for self-integration—understood most essentially as the capacity to breathe spontaneously—as well as the material basis of the capacity for sentience—and thus renders the body inadequate for rational ensoulment. A living disconnected head has both the material basis of the capacity for self-integration (although it is not exercisable due to the disconnection of the brain stem from the rest of the body) and the material basis of the capacity for sentience, which, together with the capacity for rationality, are both immediately exercisable. Thus, an SCI patient more than satisfies the minimal criteria for being a living human organism, a rational animal. However, a BDB has neither the material basis of the capacity for organismal self-integration nor the material basis of the capacity for sentience, and therefore the BDB is dead because it is not proportionate matter for a human soul. Thus, we come full circle to an explanation of why a high cervical SCI patient is a human organism, while a BDB or a body disconnected from a brain is not an organism at all.

NOTES

1.

I use the term “neurological criterion for human death” (hereafter NC) as synonymous with the total brain death criterion for human death, and, in line with the recommendation of the 2008 President’s Council on Bioethics, I understand total brain death to mean total and irreversible brain failure. Note that I make no claims regarding the adequacy of current diagnostic criteria for determining that total and irreversible brain failure has in fact occurred.

2.

I refer to “brain dead bodies” (BDBs) for the sake of convenience, but in doing so I use the term “body” in the loose sense to include an aggregate of separate substances, because I do not in fact think that the brain dead “body” is a body in the strict metaphysical sense of a unified whole or single substance.

3.

In this article, I presume the truth of a broadly Aristotelian hylomorphic account of the nature and unity of material substances, including, paradigmatically, living organisms. Defending these admittedly controversial metaphysical presuppositions is beyond the scope of this paper. It is worth noting, however, that Aristotelian hylomorphism has undergone a resurgence both in the philosophy of personal identity and in ontology more generally. (See, for instance, Hoffman and Rosenkranz, 1997; Johnston, 1992, 2006; Lee and George, 2008; Lowe, 2011; Marmodoro, 2013). Further, prominent and influential arguments on both sides of the brain death debate presume (often implicitly) a hylomorphic understanding of the human being as a body–soul unity, with “soul” understood philosophically as the principle of functional integration of the organism as a whole, making the organism a genuine whole rather than a mere aggregation of cells, tissues, and organs (see, for instance, Bernat, Culver, and Gert, 1981; President’s Commission, 1981; Shewmon, 2012). Finally, only a defense of the neurological criterion for death that is in line with an Aristotelian-Thomistic anthropology will be acceptable to the Roman Catholic Church, which is the largest nongovernmental provider of health care in the world, and which has significantly influenced the brain death debate from the very beginning.

4.

If this revised rationale is correct, then Miller, Truog, and Halpern are wrong in their judgment that the neurological criterion for human death is no longer defensible. Thus, they are also wrong to claim that the only way to justify the practice of organ donation after total brain failure is to abandon the dead donor rule (Truog, 1997; Truog, Miller, and Halpern, 2013; Miller and Truog, 2009).

5.

I use the phrase “organism as a whole” to indicate a single, unified organism (not just an aggregation of separate organisms). To be an “organism as a whole”, it is not necessary to be a “whole organism.” As Shewmon explains, “structural or functional incompleteness, to lesser or greater degrees, does not per se vitiate the integral wholeness of an organism” (Shewmon, 2012, 431).

6.

What I mean by “the material basis of the root capacity for integration” will be become clear in the following sections of the article. Here, let me just clarify that I speak of “root” capacities to refer to what others sometimes call “radical” capacities, “basic natural capacities,” “active potencies,” “second order capacities,” or capacities at the level of “first act.” A root capacity (or radical capacity, basic natural capacity, etc.) is the basis of an active dynamism toward the development and maintenance of an immediately exercisable capacity. I prefer the term “root capacity” both because it seems to capture the concept in language accessible to nonspecialists, and because it is shorter (and thus less cumbersome) than the alternatives. I speak of the brain as the material basis of the root capacity for integration because, as I will explain in Section III, the formal principle of self-integration is the soul, not any particular organ.

7.

As a matter of medical fact, there do actually seem to be important differences between the body of an SCI patient below the site of the transection and a BDB: in SCI patients, the ninth and tenth cranial nerves are still connected, and brain-mediated hormonal regulation continues to occur through non-neuronal pathways. Shewmon recognizes these differences, dismissing them as insignificant, but other doctors whom he cites clearly disagree with his judgment on this point (Shewmon, 2012, 450–451). Although I am not fully convinced of Shewmon’s claim, for the sake of argument I grant his premise that a BDB and the body of an SCI patient below the site of the transection are functionally equivalent, in order to show that even if Shewmon is right on this factual point, his argument still fails.

8.

As I will argue later, in the case of the BDB it lacks this capacity because the brain is dead; in the case of the brain-disconnected body, it lacks this capacity insofar as communication between the relevant parts of the brain and the rest of the “body” has been cut off such that the brain no longer controls and coordinates essential vital functions below the point of the transection.

9.

The rest of the body could be seen as analogous to a kidney taken from a live donor that is artificially maintained ex vivo through the perfusion of oxygenated blood until it can be transplanted into the intended recipient. On a Thomistic understanding, the kidney is only truly a kidney when it is united with the rest of the body; once separated, it has lost its inner principle of unity (which was the principle of unity of the body as a whole) and thus can only be called a “kidney” in an equivocal sense. The “kidney” ex vivo is thus not really a unity, which is why external agents are required to maintain it until it is successfully integrated into a new body of which it then becomes a proper part (Aquinas, Questiones Disputatae de Anima, q. 10, ad. 15; Summa Contra Gentiles II, 72; Eberl, 2011, 52).

10.

Here and throughout the remainder of the discussion, I am assuming that we are dealing with organisms that are noncontroversially human in a biological sense—that is, organisms that came from human parents and that have a human genome.

11.

Shewmon also discusses three vital–operational levels of integration—vegetative, sensorimotor, and intellectual–volitional, and argues that a human being persists if the highest level of structural–functional or vital–operational integration persists (Shewmon, 2012, 431–432). Thus he claims that a “brain in a vat” is a living human organism because, ex hypothesi, it “supports the rational consciousness characteristic of a human organism” (433). I largely agree with these points, although I would argue that the “brain in a vat” is a human organism as a whole both because it retains the material basis for organismal integration and because it retains the material basis for sentience, thus indicating that the soul as formal principle of those capacities is still present. I say more about this in Sections IV–V.

12.

Perhaps it could be argued that constitutive integration is not the conceptual equivalent of soul, but rather the biological result of having a soul. Yet if that is what Shewmon means by constitutive integration, then it is not clear why constitutive integration has to be “all or none,” since this is not true of the actions and operations of which the soul is the formal principle. Likewise, if Shewmon thinks that constitutive integration is the result of having a soul, rather than the equivalent of soul, then his statement that constitutive integration is what “makes a body to be alive and to be a whole” is also false, since that statement is true only of the soul itself, not of any specific effect of which the soul is the formal principle.

13.

I use the term “lung” only for convenience, in the same way that the term “body” is often used to refer to a corpse. For the incipient decay indicates that organ-level integration is absent, and thus there really is no unified substance which we could, strictly speaking, call a lung. This is true of any organ removed from the body of which it was a part (see Aquinas, QDA, q. 10, ad. 15, SCG II, 72; Eberl, 2011).

14.

The second criterion proposed by Shewmon in 2001 (and reiterated in 2012) to distinguish an organism from a nonorganism is: “Any body requiring less technological assistance to maintain its vital functions than some other similar body that is nevertheless a living whole must possess at least as much integration and hence also be a living whole” (Shewmon, 2001, 462). Yet this criterion seems to be completely beside the point from the perspective of the crucial metaphysical question regarding the presence or absence of the soul as evidenced by the presence or absence of the material basis of the root capacity for self-integration. Maintaining the life of a human being suffering from a traumatic injury may require aggressive and complex technological and pharmacological intervention (much more intervention than is required to oppose entropy in a BDB) for a period of time until the body recovers sufficiently to be able to breathe spontaneously—that is, exercise its self-integrating capacities on its own once again. But the trauma patient retains the material basis of the root capacity for self-integration (and sentience), and thus the trauma patient is alive and has a soul, even during the period when he cannot exercise that capacity. The fact that he retains the material basis of this root capacity is evidenced by his later recovery of immediately exercisable self-integrating capacities. (Or, in other cases, the failure to recover immediately exercisable self-integrating capacities after an extended period of time may show that the material basis of those capacities has indeed been irreversibly lost. Aside from the case of total brain death, however, I do not think that we can have certainty that the material basis of self-integrating capacities and sentience have both been irreversibly lost (which, as I later argue, is what we would need to know in order to know that the soul has ceased to inform the body and that the human being is therefore dead). Although nonbrain dead patients have been known to recover their immediately exercisable self-integrating capacities after extended amounts of time on life support, there has not been even one case of a BDB ever recovering to the point of being able to survive (i.e., to actively oppose entropy) without mechanical ventilation. Of course, spinal cord injury (SCI) patients also never recover their ability to survive without mechanical ventilation, but, as I argued above, it is plausible to claim that only the head of the SCI patient that is a rationally ensouled organism as a whole, relying on what used to be the rest of its body as an artificially maintained, external life support system.

15.

I am not sure if “trigger” is exactly the right word here, but the idea I am trying to express is that breathing sets everything else in motion, kind of like knocking down the first in a long row of dominoes, except that what breathing provides is not merely a single impulse but a constant, repeated impulse.

16.

These criteria are similar to the ones that Condic (2016) proposes. The difference in our approaches, flowing from the fact that mine is primarily metaphysical while hers is primarily biological, is that I emphasize that the possession of a root capacity for self-integration is a necessary and not only sufficient criterion for being a living human, and then indicate that possession of that root capacity is evidenced either by the material basis of the capacity to breathe or the material basis of the capacity for sentience. Thus while Condic (2016), from a biological perspective, argues that an SCI patient is a living human being but not an organism, on my view an SCI patient (or even someone with permanent brain stem damage due to a stroke but with a functioning higher brain) is an organism metaphysically because he or she continues to possess the root capacity for self-integration—the SCI patient still possesses the material basis of that root capacity because the brain stem itself is not damaged, while the person with brain stem damage possesses only the root capacity (without its material basis) which resides formally in the soul. Despite the differences in our views, however, it is striking that Condic and I, reasoning relatively independently and from two different perspectives, have both arrived at what in practice amount to the same criteria for the determination of death. This convergence bodes well for the possibility of articulating criteria for the determination of death that can be acceptable to scholars and practitioners from a variety of fields, even if each accepts those criteria on the basis of slightly different reasoning.

17.

Aquinas claims that, since “all the powers of the soul belong to the soul alone as their principle,” even though the proper subject of the vegetative and sensitive powers is the body-soul composite, the vegetative and sensitive powers “remain virtually in the soul, as in their principle or root” (ST I, q.77, a.8). Likewise, Eberl notes that “if one takes account of Aquinas’s metaphysical view of a human person’s post-mortem existence, it is conceivable for a human animal—defined in terms of the persistent existence of a rational soul with unactualized vegetative and sensitive capacities—to exist without being composed of a material, organic body” (Eberl, 2011, 67).

18.

Here, I exclude the capacity for rationality because the intellect (the principle of conceptual thought) is relatively independent of materiality, even though as humans our natural mode of knowing involves sense perception (which does have a material basis) as its prerequisite. As Aquinas explains, “The body is necessary for the action of the intellect, not as its origin of action, but on the part of the object; for the phantasm is to the intellect what color is to the sight. Neither does such a dependence on the body prove the intellect to be nonsubsistent; otherwise it would follow that an animal is nonsubsistent, since it requires external objects of the senses in order to perform its act of perception” (I-II, q. 75, a.2, ad 3). In other words, the intellect understood as the principle of conceptual thought has a relative independence from the body (and therefore, according to Aquinas, can subsist apart from the body), because the operation of which it is the principle surpasses the spatio-temporal limitations inherent in material things. Nonetheless, for its normal mode of operation the human intellect relies on the brain for the provision of an adequate object, just as the human auditory system relies on the presence of sound waves within a particular frequency range for its normal operation. (For an extended discussion of this issue, see Lee and George, 2008, ch.2.)

19.

See note 18.

20.

QDA, a. 10, ad. 4.

21.

Austriaco’s systems biology perspective also fails to recognize that self-integration requires control of the capacity for respiration and circulation (Austriaco, Cole, and May, 2001; Austriaco, 2003). Austriaco is right to reject a reductionistic, mechanistic view of the organism and to emphasize, by contrast, that the body is organized “all the way down;” he is also right to say that this organization is a manifestation of the immaterial soul. As mentioned above, the soul informs, unifies, and organizes the whole body; the soul is in every part of the organism. Yet the fact that organization exists all the way down to the molecular level is insufficient to show that these organized molecules, cells, organs, etc., make up a larger unified whole informed by a single soul. To know that you are in the presence of an organism as a whole, animated by a single soul, rather than an aggregate of molecules, cells, organs, and tissues, you need evidence of self-directed holistic functioning, which includes control over one’s essential vital functions. As argued above, the fact that a BDB can function holistically with the help of external causes does not show that it is a single, unified organism as a whole, animated by a single soul, precisely because the holistic functioning of the BDB is not self-directed insofar as the BDB does not control its own breathing. To claim that in more complex organisms—like human beings beyond the embryonic stage of development (brain-stem control over breathing begins at 11–13 weeks in utero [Kandel et al., 2013, 632])—the soul operates through a primary organ to coordinate the other parts is in no way to deny that the soul is in every part of the body (see Aquinas, Summa Theologiae I, q.76, a.8). As Eberl explains, “While a human person’s soul informs her body as a whole, it actualizes the body’s various parts through the brain’s operation—among other things—of coordinating the vital functions responsible for the circulation of oxygenated blood throughout the body, as well as voluntary muscle control” (2011, 47). It seems plausible more generally to claim that, just as unity (coordination toward the common good) among a group of individual persons requires authority unless the group is extremely small; likewise, the unity of an organism requires a primary organ unless the organism is relatively simple. It is noteworthy that all of Austriaco’s examples of organisms that are unified without having a primary organ that is materially responsible for that unity are relatively simple organisms like flatworms and embryos (Austriaco, 2003, 301).

22.

This also helps to explain Aristotle and Aquinas’s belief that the primary organ—by which the soul operates to coordinate the other parts—was the heart. However, now that we know that it is not actually the heart that controls circulation and respiration, but rather that the heart (and lungs) are controlled by the brain, the same reasoning leads us to conclude that the primary organ is the brain (e.g., Ashley, 2001; Eberl, 2011; Tonti-Filippini, 2012).

23.

Austriaco (2016) questions the biological claim that the absence of the brain indicates the absence of the material basis of the capacity for sentience. Although not a biologist, I find that the evidence he provides for questioning this claim to be unconvincing. He cites a number of experiments showing that “the animal spinal cord... is capable of acquiring the ability to perform complex motor tasks, such as stepping and standing, following the elimination of descending input from the brain... In the absence of the brain, it can assume a primitive brain-like function that involves coordinated behaviors in response to external stimuli” (2016, 320). As impressive and fascinating as these experiments are, it is insufficient evidence for sentience in the robust sense in which I am using the term—that is, in the sense that involves consciousness/perceptual awareness, not just the unconscious ability to react appropriately to external stimuli.

24.

The soul is also, of course, the principle of human rational capacities, but the soul is the principle of those capacities not as form of the body, but as the subject of those capacities.

25.

My view is therefore incompatible with “higher brain” definitions of death advocated by authors like Veatch (2005) and Green and Wikler (1980).

26.

I put this term in quotation marks because it does not refer to irreversibility at the metaphysical level, but rather to a diagnostic label indicating that beyond a certain point it is extremely unlikely (though not in fact impossible) that the patient will recover consciousness.

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