A survey of American neurologists about brain death: understanding the conceptual basis and diagnostic tests for brain death

This study was a prospective survey of a random sampling of board-certified neurologists in the United States regarding their opinions about BD. The mailing list was obtained from Healthcare Lists Division SDI (Yardley, PA) in August 2009. Each neurologist was mailed the survey in January 2010, along with a $5 gift certificate to encourage them to have a coffee while filling out the questionnaire. A cover letter asked participants to complete the survey and mail it back in the addressed, stamped envelope. A second mailing was done in May 2010 to nonresponders. All responses were received by July 2010. The cover letter stated, "We are sending you a short questionnaire asking your opinions around some of the concepts surrounding BD. We want to sample the opinions regarding the concept of BD. Your responses are voluntary and confidential." The study was approved by our university health ethics research board.

The development and initial testing of the instrument are described in more detail elsewhere [12, 13]. The current instrument (Additional File 1) is identical to that used in a survey of Canadian pediatric intensivists and Canadian neurosurgeons, with the following changes: (a) in the first question about acceptable conceptual reasons to explain BD, we added the choice "cessation of the vital work of a living organism--the work of self preservation, achieved through the organism's need driven commerce with the surrounding world" as stated by the President's Council; and (b) we modified the scenario regarding family refusal to stop "life support" in a brain-dead patient to describe continued support for 8 months until ventilator withdrawal, and asked "was this patient dead for the last 8 months?" and if the patient, during the last 8 months, was doing any of the three vital activities stated by the President's Council to indicate life (Additional File 1) [14].

To generate the items for inclusion in the questionnaire, we searched MEDLINE from 1996 to 2004 for articles on BD, followed by review of the relevant article reference lists. The new questions described above were based on the President's Council White Paper [14]. To ensure clarity, realism, validity, and ease of completion, initial pilot testing was done by having five local pediatric intensivists, one local pediatrician, and one local organ donation coordinator complete the questionnaire, followed by a semistructured interview for feedback.

Certain definitions were made a priori for two of the survey questions. The first question asked the respondent to choose from a list of "stand-alone" reason(s) that "is/are an acceptable conceptual reason to explain why 'brain death' is equivalent to 'death'." The seventh question asked, "This patient fulfills all brain death criteria unequivocally, including the suitable interval. Conceptually, why are they dead (i.e., in your own words, what is it about loss of brain function, including the brainstem, that makes this patient dead)?" For analysis, we classified responses into categories that have been discussed in the literature, including loss of integration concept of BD, higher brain concept of BD, prognosis concept of BD, and statement of the criterion only.

Anonymous data were entered into REDCap Survey (Version 1.3.9-^©2010 Vanderbilt University) and uploaded to the Statistical Package for the Social Sciences (SPSS, Inc., Chicago, IL) version 15.0 for Windows. We analyzed responses using standard descriptive tabulations and give adjusted Wald 95% confidence intervals (95% CI).

BD is said to be death by most professional bodies because it satisfies the concept/definition of death (Table 4): loss of integrative unity of the organism as a whole, marking when an organism is no longer an organism because it no longer can resist the forces of entropy and no longer can maintain internal homeostasis [1‐4]. Many have argued that integrative unity of the organism as a whole often continues during BD (hence, integration is not dependent on functions of the brain), and a central integrator is not required for life; therefore, many no longer consider this a concept of death that BD satisfies [3, 6, 14]. Loss of personhood, based on irreversible loss of consciousness (sentience, or agency) is necessary, but not sufficient, for death (Table 4) [3, 4]. Although nonconscious patients may be allowed to die due to their profound neurological disability, no society has accepted that they are already dead. It may be true that BD patients have poor quality of life or certainty of cardiac arrest in a short period; however, this denotes a prognosis and not a diagnosis of death. The President's Council suggested a novel concept of death: that vital external work of an organism is required to be alive, and once an organism no longer interacts with the environment to obtain what it needs to survive, it is dead [14]. Importantly, simply restating the criterion of BD does not give any concept of death that BD satisfies to justify BD being death.

This survey shows that neurologists do not understand if, or disagree whether, the criterion BD fulfils a concept of death. Few consider irreversible loss of integration of the organism as a whole or irreversible loss of the ability to perform external vital work as a reason to accept BD as death (some even consider that external work continues during BD). Many confused a restatement of the criterion of BD as justification that it is death, and a few conflated the prognosis of death with the diagnosis of death. Most consider a higher brain concept of death justified. This is concerning because neurologists often are the specialist declaring BD and explaining it to families in the intensive care unit.

The tests for BD are performed to confirm that irreversible loss of all functions of the brain, including the brainstem, has occurred. It has been shown that some brain functions continue after accurately clinically diagnosed BD, including EEG activity in 20%, evoked potential activity in 5%, and hypothalamic neuroendocrine function in > 50% [15]. These activities may be explained by the finding that continued brain blood flow occurs in 5-40% of BD patients, and pathologic destruction of brain does not occur in more than 40% of BD patients (even after over 24-48 hr of maintained circulation) [15, 16]. The ongoing brain functions have been explained with several controversial claims (Table 4) [3, 4, 15, 17‐19]. First, these are mere activities and not functions; however, the brain seems too complex an organ to simply make this claim [3, 17]. Second, these are insignificant functions; however, this is an ad hoc claim [3, 4, 15, 17]. Third, these are not critical clinical functions, and BD is a clinical diagnosis; however, this claim is both ad hoc and circular (critical clinical functions are necessary for maintenance of life, and death is the loss of critical clinical functions, is a trivial tautologous statement) [3, 17]. Fourth, these are not critical functions, because they are replaceable mechanically; however, this would only lead to a higher brain consciousness based concept of death [3, 4, 15, 17‐19].

This survey shows that most neurologists do not understand, or disagree, that certain brain functions can remain in patients diagnosed dead using accepted clinical tests confirming the BD criterion. This may suggest that the accepted medical standard of clinical tests for BD can produce false-positive diagnoses of death. At the very least, the neurologists often are unaware of (or worse, disagree with) the debates regarding the meaning of significant, critical, clinical, brain functions.

First, we assumed that there is a "standard concept of death." However, we included in the survey all the concepts offered in the literature and also provided an opportunity to provide a new concept in the open-ended question. Although we found that most neurologists did not agree with the concept of loss of integrative unity, the main alternative was a higher brain concept. This would imply that patients with permanent vegetative state are dead in their state of wakefulness and breathing. Second, perhaps the finding that 97% of neurologists are comfortable diagnosing death based on BD only shows that neurologists are not able to justify explicitly why the equivalency truly holds. After all, this is a philosophical question and may not involve terminology used in clinical training. Perhaps the main finding of the survey is uncovering an unmet neurologists' educational need. Although a potential interpretation, this may not be reassuring to families who are told that their loved one is dead based on the criterion BD. In addition, the American Board of Psychiatry and Neurology lists an understanding of BD on the objectives of training [20]. Third, although the survey did not determine this, perhaps neurologists accept BD as "dead enough" for organ donation and withdrawal of life-support purposes. Accordingly, patients with BD should be allowed to die or should be treated as if they no longer are part of the human moral community; but, this is different than being biologically dead. We agree with other authors who have suggested that if BD is not death, whether BD can be considered a state where vital organ donation complies with nonmaleficence (death is an unavoidable and minimal harm) and autonomy (with informed consent) requires further discussion and debate [21].

The relatively small sample size, only modest response rate to this survey, and lack of information regarding respondents' exposure to BD patients are significant limitations. In addition, the closed-ended questions may not have allowed respondents to elaborate and clarify their responses. The strengths of the survey include the development methodology, and unambiguous nature of most of the questions. In addition, the striking similarity of our results to those of other surveys done in the past, including using this same survey in different populations of North American nonneurologist medical specialists, enhances the generalizability of the results [12, 13, 22‐24]. The preponderance of evidence from this survey, and other surveys, support the conclusions we have drawn.