Movements in Brain Death: a Systematic Review Gustavo Saposnik, Vincenzo S
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REVIEW ARTICLE Movements in Brain Death: A Systematic Review Gustavo Saposnik, Vincenzo S. Basile, G. Bryan Young ABSTRACT: Brain death is the irreversible lost of function of the brain including the brainstem. The presence of spontaneous or reflex movements constitutes a challenge for the neurological determination of death. We reviewed historical aspects and practical implications of the presence of spontaneous or reflex movements in individuals with brain death and postulated pathophysiological mechanisms. We identified and reviewed 131 articles on movements in individuals with confirmed diagnosis of brain death using Medline from January 1960 until December 2007, using ‘brain death’ or ‘cerebral death’ and ‘movements’ or ‘spinal reflex’ as search terms. There was no previous systematic review of the literature on this topic. Plantar withdrawal responses, muscle stretch reflexes, abdominal contractions, Lazarus’s sign, respiratory-like movements, among others were described. For the most part, these movements have been considered to be spinal reflexes. These movements are present in as many as 40-50% of heart-beating cadavers. Although limited information is available on the determinants and pathophysiological mechanisms of spinal reflexes, clinicians and health care providers should be aware of them and that they do not preclude the diagnosis of brain death or organ transplantation. RÉSUMÉ: Mouvements et mort cérébrale : revue systématique. La mort cérébrale est une perte de fonction irréversible du cerveau et du tronc cérébral. La présence de mouvements spontanés ou réflexes constitue un défi lors de la détermination neurologique de la mort. Nous avons révisé les aspects historiques et les implications pratiques de la présence de mouvements spontanés ou réflexes chez les individus en état de mort cérébrale et nous postulons des mécanismes physiopathologiques pour les expliquer. Nous avons révisé 131 articles identifiés dans Medline, qui avaient été publiés entre janvier 1960 et décembre 2007 et qui portaient sur la présence de mouvements chez des individus dont le diagnostic de mort cérébrale était confirmé. Les mots clés utilisés étaient les suivants : mort cérébrale, mouvements, réflexe spinal. Nous n’avons trouvé aucune revue systématique de la littérature sur ce sujet. Des réflexes de retrait à la stimulation plantaire douloureuse, des réflexes ostéo-tendineux, des contractions abdominales, le signe de Lazare, des mouvements ressemblant à des mouvements respiratoires ont été décrits. En général, ces mouvements ont été considérés comme des réflexes spinaux. Ces mouvements sont présents chez près de 40 à 50% des cadavres dont le cœur bat toujours. Bien que l’information disponible sur les déterminants et les mécanismes physiopathologiques des réflexes spinaux soit limitée, les cliniciens et les soignants devraient connaître leur existence et savoir qu’ils ne sont pas incompatibles avec un diagnostic de mort cérébrale et ne constituent pas un obstacle à la transplantation d’organes. Can. J. Neurol. Sci. 2009; 36: 154-160 Historical Aspects had slashed through the fourth cervical vertebra; the heart kept For centuries physicians, philosophers and various writers beating for an hour after decapitation. According to Alister have written about death and its many peculiarities, including Kershaw in A History of the Guillotine, a French physiologist movements of the dead. One of the very first was René named Pierre Jean Cabanis was given the task in 1795 to Descartes, who mentioned, that the heads, as well as the bodies determine if the victims of the guillotine were conscious after of dead animals continued moving post-decapitation (Discourse beheading. There were also tales of beheaded bodies standing up on the Method, 1637). There have been reports of body movements in beheaded people during the French Revolution. Renaissance paintings illustrate decapitations of the time with the decapitated bodies standing upright. “Fra Giovanni da Fiesole” (Beato Angélico, 1395-1455) painting entitled “The From the Division of Neurology, Department of Medicine, St. Michael’s Hospital decapitation of Saint Cosmas and Saint Damian” (Louvre (GS), Department of Health Policy, Management and Evaluation (GS), Department of Museum, Paris) is an example of the decapitation scenes. Medicine, Division of Neurology (VSB), Neurogenetics Section, Centre for Addiction and Mental Health (VSB), University of Toronto, Toronto; Department of Clinical Regnard and Loye (1887), physicians during the French Neurological Sciences and Critical Care Medicine (GBY), University of Western Revolution, wrote about jaw contraction and eyelid movements Ontario, London, Ontario, Canada. in a decapitated head, although no reflex movements in the body RECEIVED JULY 30, 2008. F INAL REVISIONS SUBMITTED OCTOBER 31, 2008. 1 Correspondence to: Gustavo Saposnik, Departments of Medicine and Health Policy, were appreciated . On further examination of the head severed Management and Evaluation, University of Toronto, 55 Queen St East, Toronto, from the body, it was noticed that although the guillotine blade Ontario, M5C 1R6, Canada. 154 LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES after the fall of the guillotine blade and walking around before finally collapsing 2. The mechanism behind these phenomena was not described and as such, the mysteries surrounding movements in the dead had continued to bewilder people across borders and civilizations. Concept of Brain Death Although by definition the diagnosis of brain death (BD) requires the irreversible loss of cerebral function, including the brainstem (AAN practice parameters, 1995) 3, it appears that all functions are not immediately lost. Several functions including temperature regulation, hypothalamic-pituitary-adrenal axis function, as well as spinal reflexes can be maintained for up to several hours/days. With the advent of donor organ trans- plantation, the need for a well-established and reproducible BD diagnostic criteria emerged. The first of these criteria were developed in 1968 by the Harvard Medical School Committee. However, these criteria did not allow for any spontaneous or Figure: Illustration of the decapitation of Saint Cosmas and Saint reflex movements (SRMs) (Ad Hoc Committee of the Harvard Damian. Saint Cosmas and Saint Damian were twin brothers born in 4 Arabia, who became skilled doctors. Known as the "moneyless", they Medical School 1968) . The criteria included deep, unresponsive never accepted money for their services, but offered them in the spirit of coma, with absent brainstem reflexes and apnea. The Canadian charity. When the persecution under Diocletian broke out, their very guidelines for brain death declaration were first published in prominence rendered them marked objects of persecution. Being 1981; these allowed for the presence of spinal reflexes 5. Further apprehended by order of Lysias, governor of Cilicia, they were arrested, refinements followed, again allowing for spinal reflexes in the tortured, and beheaded in the year 283. Fra Giovanni da Fiesole (Beato 4-7 Angélico, 1395-1455) illustrated decapitated bodies maintaining the USA, the UK and Canada . Most guidelines also preclude the postural tone as represented by the bodies standing upright. The picture presence of hypothermia, central nervous system (CNS) is currently exhibited at Louvre Museum, Paris. depressant toxins/drugs, metabolic derangements and neuro- muscular blocking agents. The concept of BD and its correct diagnosis have gained importance with organ transplantations 8. However, data from a survey published in 1989 revealed that only 35% of health professionals (76 physicians and 80 nurses) involved in organ procurement for transplantation was able to correctly diagnose 9 AAN guidelines. Specifically, there has to be a clear document- BD . This also reflects the lack of a systematic approach or well- ation of i) unresponsiveness, ii) absent brainstem reflexes, and defined diagnostic criteria of BD. iii) apnea and/or complementary studies revealing the absence of The word ‘patient’, after coming to the diagnosis of BD, does cerebral blood flow. We included case reports if the diagnosis of not seem appropriate as ‘patient’ implies a person who is alive. BD was adequately described in the methods section or specified Further, in countries where BD is equivalent to death of the diagnostic criteria. We also evaluated the references of the individual, the patient has lost his legal personhood. Since brain retrieved articles. Titles and abstracts of identified published dead victims are "legally dead" in Canada, we prefer to use articles were reviewed independently (by GS and VB) to ‘heart-beating cadaver’ (HBC) instead of ‘patient’. In a recent 10 determine the relevance of the articles. Each citation was review and case report , the authors also acknowledged classified as 'inclusion' or 'exclusion'. For feasibility reasons, no problems with terms for “movements” in BD nomenclature, attempts were made to directly contact authors of published suggesting that stimulus-provoked movements be referred to as papers. BD-associated reflexes, while spontaneous movements as BD- In case of disagreement between the two reviewers, associated automatisms. consensus was reached to solve the disagreement. After this, Awareness of the clinical criteria for BD diagnosis and its excluded citations were no longer considered. legal and practical implications are of utmost importance. We have, therefore examined the nature, frequency, and patho-