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doi:10.1111/jpc.12889
VIEWPOINT
Diagnosing death Stephen Jacobe Paediatric Intensive Care Unit, Children’s Hospital at Westmead, Westmead, New South Wales, Australia
Case History At 7:05 pm, Michael – not his real name – aged 2 was found by his mother unconscious, cyanosed and ‘lifeless’, after choking on a piece of apple. He was in asystole when the paramedics arrived at 7:13 pm. They administered three doses of adrenaline, intubated the trachea after removing some apple fragments and performed cardiopulmonary resuscitation (CPR). In the Emergency Department he received three further doses of adrenaline and ongoing external cardiac massage. There was no response and resuscitation efforts were halted at 7:53 pm by the Emergency Physician. With no signs of life and no palpable pulse, Michael was declared dead. At 8:10 pm a nurse noticed irregular respiratory efforts, and a weak pulse was palpable. Michael was re-intubated, placed on a ventilator and transferred to the Intensive Care Unit for ongoing management. Over the next 12 h Michael developed neurological signs consistent with brain death. At 1:00 pm the next day I performed an initial formal examination of brain stem reflexes, including an apnoea test, and found all reflexes absent. A ceretec cerebral perfusion study demonstrated absent cerebral blood flow at 2:49 pm. The parents declined the offer to consider organ donation and, following negotiation with the family regarding their farewells, Michael was extubated at 8:42 pm. Michael rapidly became pale, remained motionless with no respiratory effort, and was pulseless when examined approximately an hour later (9:45 pm). I met with Michael’s parents after they’d spent time with their son’s body and they asked, ‘When did Michael actually die? Did he die at home when he collapsed, or in the Emergency Department or when he was extubated?’ That relatively straightforward question was actually quite complex to answer. The pronouncement of death is important on many levels. It signals the start of the mourning period; various rights and rituals can proceed; legal affairs may be settled; succession can take place; in certain circumstances a person’s organs may be removed for transplantation; and medical treatment can be terminated.
Correspondence: Dr Stephen Jacobe, Paediatric Intensive Care Unit, Children’s Hospital at Westmead, Locked Bag 4001, Westmead, NSW 2145, Australia. Fax: +61 2 98451993; email: [email protected] Accepted for publication 28 July 2014.
In spite of the obvious importance of diagnosing death, a degree of uncertainty continues to surround the question of exactly when a person is actually dead. As Veatch writes: ‘defining death . . . is not a trivial exercise in coining the meaning of the term. Rather, it is an attempt to reach an understanding of the philosophical nature of man and that which is essentially significant in man which is lost at the time of death’.1 Death has religious, philosophical, metaphysical and scientific aspects, and some of the controversy can be explained by these different perspectives on death. Religious authorities traditionally viewed death as occurring when the soul departs the body. Philosophers might argue death occurs when ‘personhood’ is lost. Biologists might define death as loss of integration of the organism or even loss of integrity of all cells. Although ‘dying’ is clearly a process that precedes death, whether ‘death’ itself is a process or a distinct event marking a change from one binary state to another remains controversial.2,3 Surely a person must be either dead or alive; there can be no in between. There is potentially a time however when, with appropriate intervention, the dying process may be reversed and death prevented. Truog and Fackler suggested that, ‘the moment in this process at which death is said to have occurred is a point that cannot be discovered by any empirical process, but rather must be chosen by societal consent’.4 This article will explore when that exact moment may be, and how death might be reliably diagnosed.
Is ‘Death’ Reversible? Death is inevitable, but most of us wish to prolong our existence on Earth for as long as possible and certainly do not want to be ‘written off for dead’ until there is absolutely no hope left for recovery. Although developments in life-sustaining medical technology in the past 100 years (such as mechanical ventilation and organ transplantation) have added to uncertainties surrounding the timing of death, such uncertainties are by no means confined to the modern era. The phenomenon of apparent ‘resurrection’ is far from new. In addition to Jesus rising from the dead, the Bible describes a number of resurrections performed by Elijah and the resurrection of Lazarus 4 days after his death and entombment.5 Whether such accounts represent true resurrection or cases of premature burial is a matter of conjecture.
The Enlightenment – Resuscitation, Reanimation and Galvinism Scientific and social advances during the period of the Enlightenment (1740–1850) blurred the boundary between life and
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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death and resulted in a widespread fear of being falsely diagnosed as being dead and potentially buried alive. The notion that the human body was a mysterious creation of God was being challenged by science. With access to human corpses for dissection and an increasing knowledge of physiology, physicians were beginning to discover the body’s more ‘mechanistic’ workings. By the late 18th century a number of Humane societies were developed ‘for the recovery of persons apparently drowned’.6,7 Techniques employed by resuscitators to ‘restore vitality’ included smelling salts (1721), artificial respiration (1744),8 rectal insufflation of tobacco smoke and the administration of electric shocks.7 Up to 2/3 of reported resuscitation attempts were said to be successful. A number of conditions including apoplexy, trances, syncope, fits, convulsions, and intoxication with opium or spirits were said to mimic death.7 Mesmerism (hypnosis) was demonstrated in the 1770s and, 50 years later, general anaesthesia could produce an almost death-like state; these were felt to represent states of ‘suspended animation’. Luigi Galvani demonstrated that electric shocks could produce muscle movements in isolated frog muscle.9 His nephew Giovanni Aldini toured Europe demonstrating the power of electricity. In 1803, at the Royal College of Surgeons in London, Aldini was provided with the fresh corpse of the hanged murderer George Foster. Aldini placed electrodes connected to a bank of batteries on various parts of Foster’s face and body, causing movements and grotesque contortions. Application of the electrodes to the ear and rectum were said to cause the corpse ‘such violent muscular contractions . . . as to almost give the appearance of reanimation’.10 Aldini concluded that galvanism ‘is stronger than any mechanical action . . . [and] affords very powerful means of resuscitation in cases of suspended animation . . .’10 It is widely believed that accounts of Aldini’s demonstration inspired Mary Shelley when writing her novel ‘Frankenstein’. These 19th century ‘scientific’ developments, as well as reports in medical journals of premature burial,11 led many to fear that death might be misdiagnosed, resulting in premature withdrawal of medical care and internment. Such fears fuelled and were fuelled by publications in the popular press and literature, for example, ‘The Premature Burial’ by Edgar Allan Poe, 1844. A range of tests of death were developed. Confirmatory signs included: absent inflammatory response to subcutaneously injected ammonia (Monteverde’s sign); no movement of flags attached to needles inserted into the heart (Balfour’s test); direct palpation of the heart via an intercostal incision (Foubert’s test); failure of a fingertip with a proximal ligature to become congested (Magnus’ sign); and persistent eyeball indentation following external pressure (Ripault’s sign). Tests of ‘sensibility’ included smelling salts, mustard up the nose, objects inserted under the fingernails, loud noise such as blowing a trumpet in the ear, scalding, and instilling tobacco smoke per rectum.12 In 1889, Sir Benjamin Ward Richardson published 11 ‘absolute signs and proofs of death’ in his book, Asclepiad:13 apnoea, absent cardiac activity (pulse, apex beat and heart sounds); absent turgescence (filling) of the veins; hypothermia; rigor mortis; coagulation of the blood; absent rust oxidation of a 574
bright steel blade plunged deep into the tissues; absent red colour when semi-transparent parts were transilluminated; absent muscle contraction under the stimulus of galvanism, heat or puncture; absent red blush of the skin after subcutaneous injection of ammonia; and putrefactive decomposition. The businessman and social campaigner William Tebb, previously active in anti-vaccination campaigns in America and Britain, co-founded the London Association for the Prevention of Premature Burial in 1896 and published ‘Premature burial, and how it may be prevented’.14 Tebb lobbied the government unsuccessfully to legislate for safeguards around diagnosing death to prevent premature burial. Some individuals, including Tebb, stipulated in their wills that they were not to be interred before signs of putrefaction. Patented safety coffins and waiting mortuaries (mainly in Germany) were developed in response to ‘moral panic’15 arising from a fear of premature burial (Fig. 1).
The 20th Century Many religions believe the moment of death coincides with the departure of the soul. Dr McDougal believed the soul contained ‘substance’. In 1907, to test this hypothesis, he conducted an experiment to weigh the soul.16 He observed closely six terminally ill patients placed on a bed mounted on a platform with sensitive beam scales. Sudden weight loss at the time of death would indicate the soul had departed. A weight loss of 3/4 ounce was observed in the first subject and 3/8 ounce in another. In two patients the balance beam dropped not once but twice. Two other patients were excluded due to ‘technical difficulties’. Despite this limited evidence, McDougal reported that the human soul weighed 3/4 ounce (21 grams).16 Prior to the early 20th century, apnoea resulted in hypoxia and inexorably progressed to cardiac standstill and death but mechanical ventilation, developed largely in response to the polio epidemic, broke this nexus. Patients who became apnoeic for whatever reason could now be kept alive. In the 1950s, a group of French neurologists observed a number of patients who were totally unresponsive and died despite ventilation, and all had cortical necrosis at subsequent autopsy. They coined the term coma depassé (beyond coma) for this condition.17 Developments in organ transplantation culminated in the first heart transplant in 1967 by Dr Christiaan Barnard in Cape Town. The donor heart came from a patient who died after ‘cardiac death’ (following cessation of life-sustaining treatment in the operating room). Some felt it was time to redefine death.
Redefining ‘Death’ An ad hoc Committee of the Harvard Medical School convened to examine the issue published guidelines in 1968 suggested ‘irreversible coma as a new criterion for death’.18 The criteria for irreversible coma were unreceptivity and unresponsivity; no movements or breathing; no reflexes; and a flat electroencephalogram (with no coexistent hypothermia or central nervous system depressant drugs) on two occasions 24 h apart. Many jurisdictions have legislation defining death. In Australia, all states and territories except Western Australia have a statutory definition of death as either irreversible cessation of all
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
S Jacobe
Diagnosing death
still be considered technically ‘dead’ by the same ‘circulatory’ criteria?19 Debate of these issues continues.20–22
The Lazarus Phenomenon Autoresuscitation is the spontaneous return of circulation after someone is pronounced dead, and this apparent ‘resurrection’ has been referred to as the Lazarus phenomenon. There is no consensus on how long circulation must cease after cardiac arrest before pronouncing death. Two recent systematic reviews summarise the literature on autoresuscitation.23,24 The more comprehensive found 27 articles describing 32 cases of autoresuscitation (aged 27–94 years), all very low quality case reports or letters to the editor.23 All cases occurred following failed cardiopulmonary resuscitation (CPR) from a few seconds to 33 min. The continuity of observation and methods of monitoring were highly variable, but in eight cases where continuous electrocardiogram (ECG) monitoring and exact times were reported, no cases of autoresuscitation occurred beyond 7 min after ceasing CPR. Only one article reported autoresuscitation in a child.25 Notably, there are no reported cases of autoresuscitation in the absence of CPR. There are no reports of autoresuscitation following planned withdrawal of lifesustaining treatment, a situation where donation after cardiac death (DCD) may be considered.23,26 This is important because the time to diagnosis of death when donating organs has a direct and measurable influence on organ recipient outcomes. Mechanisms proposed to explain the Lazarus phenomenon in failed resuscitation include impaired venous return due to airtrapping and positive intrathoracic pressure, delayed onset of drug actions, hyperkalaemia, myocardial stunning and transient asystole.24 A false-positive diagnosis of death may also be responsible.
False Positive Diagnosis of Death Fig. 1 Safety coffin designed by Franz Vester, 1868. Should a person be interred ere life is extinct, he can, on recovery to consciousness, ascend from the grave and the coffin by the ladder; or, if not able to ascend by said ladder, ring the bell, thereby giving an alarm, and thus save himself from premature burial and death.’ (See http:// australianmuseum.net.au/safety-coffins) [Accessed April 2015]
brain function or irreversible cessation of circulation of blood. Although the law may define death, a medical practitioner, following appropriate standards of the profession, has to diagnose and pronounce death. Controversies in diagnosing death persist. After the heart stops beating, how long before circulation has ceased ‘irreversibly’? How long must we wait before being certain that autoresuscitation (where the heart starts beating again spontaneously) will not, or more importantly cannot, occur? Is palpation of the pulse accurate enough to diagnose ‘cessation of circulation’, or is cardiac ultrasound necessary to demonstrate mechanical asystole? What about mechanical circulatory assist devices?: a patient declared dead on circulatory criteria may be placed on extra-corporeal life support, essentially heart-lung bypass, to maintain organ function prior to donation. Can they
Few patients undergoing emergency resuscitation have intraarterial pressure monitoring lines, so the assessment of ‘lack of circulation’ must rely on clinical signs such as no palpable pulse and absent heart sounds. A study assessing the reliability of the pulse check in infants and children found clinicians misdiagnosed pulselessness on 36% of occasions.27 Palpation of the brachial pulse was slightly more reliable than femoral palpation, and palpation for greater than 30 s also improved accuracy.28
How Should Death Be Diagnosed? Death may be diagnosed on circulatory or neurological criteria. Recent guidelines describe well the criteria for determining death on neurological grounds.29 Anyone practising in an area where they may be called upon to confirm death on neurological criteria must be familiar with these guidelines. Clinicians are more often asked to pronounce death on circulatory criteria. Pragmatically, the patient should be observed for at least 2 min for immobility/lifelessness, apnoea, absent skin perfusion, absent heart sounds and absent pulse.30 If a continuous ECG monitor is attached, 2 min of electrical asystole (assuming no technical difficulty) would confirm lack of circulation. In the presence of cardiac electrical activity (but
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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absent palpable pulse), a cardiac ultrasound should ideally be performed to confirm the presence of mechanical asystole (pulseless electrical activity or PEA). In television medical dramas such as ‘ER’, the doctors are often portrayed declaring death simultaneously with termination of resuscitation (‘I’m going to call it – time of death, 10:43’) without performing any formal examination for ‘signs of life’. Although autoresuscitation is rare, it can occur following failed CPR, can traumatise family and staff members alike and lead to a mistrust of doctors. The declaration of death must be thorough and unhurried and ‘decoupled’ from cessation of CPR. It is therefore recommended that once CPR ceases, the patient should be observed for signs of life for at least 10 min before the formal examination and declaration of death.
Conclusions There is arguably a narrow yet profound difference between ‘dying’ and ‘dead’. Doctors must ensure that they do not confuse the two and are clear about how to diagnose death. Death should not be diagnosed until at least 2 min of electrical asystole has been observed or, in the presence of cardiac pulseless electrical activity, 2 min of ‘acirculation’ (i.e. mechanical asystole), confirmed either by echocardiography/cardiac ultrasound or intra-arterial pressure monitoring. If neither is available, careful palpation of a central pulse for at least 60 s is recommended prior to declaring death. Apart from declaring death for DCD, there is generally no need for haste. Theodore Dalrymple wrote31 that, as an exhausted houseman, he was phoned by a nurse on the ward in the middle of the night to be told, ‘Doctor, I think Mr Jones is dead’. He replied, ‘Well, if you’re right, he’ll still be dead in the morning’, and went back to sleep. As for Michael, I declared that he died at 8:42 pm – the exact same time he came into the world, and a time of lasting significance for his parents.
References 1 Veatch RM. Case studies in bioethics: brain death: welcome definition . . . or dangerous judgment? Hastings Cent. Rep. 1972; 2: 10–13. 2 Morison RS. Death: process or event. Science 1971; 173: 694–8. 3 Kass LR. Death as an event: a commentary on Robert Morison. Science 1971; 173: 698–702. 4 Truog RD, Fackler JC. Rethinking brain death. Crit. Care Med. 1992; 20: 1705–13. 5 Clarke A. The Holy Bible, Containing the Old and New Testaments . . . : With a Commentary and Critical Notes, Vol. 1. London: Applegate & Co., 1856. 6 Johnson A. An Account of Some Societies at Amsterdam and Hamburgh for the Recovery of Drowned Persons: And of Similar Institutions at Venice, Milan, Padua, Vienna, and Paris; with a Collection of Authentic Cases 1773. London: Woodbridge, 1986. 7 Hawes W. Reports of the humane society for the recovery of persons apparently drowned 1783–1784. Available from: https://books .google.com.au/books?id=WbwpAAAAYAAJ&printsec=frontcover& dq=Reports+of+the+Society:+Instituted+in+1774,+for+the+Recovery+ of+Persons+...&hl=en&sa=X&ei=j5ocVYjALoTRmAXCoIDABA&ved= 0CB0Q6AEwAA [accessed April 2015].
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8 Fothergill J. Observations on a case published in the last volume of the medical essays, etc. of recovering a man dead in appearance, by distending the lungs with air. Phil. Trans. 1744; 43: 275–81. 9 Parent A. Giovanni Aldini: from animal electricity to human brain stimulation. Can. J. Neurol. Sci. 2004; 31: 576–84. 10 Aldini G. General Views on the Application of Galvanism to Medical Purposes. Whitefish, MT: Kessinger, 1819. 11 Anon. Death or coma. Br. Med. J. 1885; 2: 841. 12 Powner DJ, Ackerman BM, Grenvik A. Medical diagnosis of death in adults: historical contributions to current controversies. Lancet 1996; 348: 1219–23. 13 Richardson BW. The Asclepiad, A Book of Original Research and Observation in the Science, Art, and Literature of Medicine, Preventive and Curative. London: Longmans, 1889. 14 Tebb W, Vollum E. Premature Burial and How It May Be Prevented: With Special Reference to Trance, Catalepsy, and other Forms of Suspended Animation. London: Sonnenschein, 1905. 15 Behlmer GK. Grave doubts: Victorian medicine, moral panic, and the signs of death. J. Br. Stud. 2003; 42: 206–35. 16 MacDougall D. Hypothesis concerning soul substance, together with experimental evidence of the existence of such substance. J. Am. Soc. Phys. Res. 1907; 1: 237–44. 17 Mollaret P, Bertrand I, Mollaret H. Coma dépassé et nécroses nerveuses centrales massives. Rev. Neurol. 1959; 101: 116–39. 18 Ad Hoc Committee of the Harvard Medical School. A definition of irreversible coma. JAMA 1968; 205: 337–40. 19 Ko W-J, Chen Y-S, Tsai P-R, Lee P-H. Extracorporeal membrane oxygenation support of donor abdominal organs in non-heart-beating donors. Clin. Transplant. 2000; 14: 152–6. 20 Bernat JL, Capron AM, Bleck TP et al. The circulatory-respiratory determination of death in organ donation. Crit. Care Med. 2010; 38: 963–70. 21 Halpern SD, Truog RD. Organ donors after circulatory determination of death: not necessarily dead, and it does not necessarily matter. Crit. Care Med. 2010; 38: 1011–12. 22 Youngner SJ, Arnold RM, DeVita MA. When is ‘dead’? Hastings Cent. Rep. 1999; 29: 14–21. 23 Hornby K, Hornby L, Shemie SD. A systematic review of autoresuscitation after cardiac arrest. Crit. Care Med. 2010; 38: 1246–53. 24 Adhiyaman V, Adhiyaman S, Sundaram R. The Lazarus phenomenon. J. R. Soc. Med. 2007; 100: 552–7. 25 Cummings BM, Noviski N. Autoresuscitation in a child: the young Lazarus. Resuscitation 2011; 82: 134. 26 Sheth KN, Nutter T, Stein DM, Scalea TM, Bernat JL. Autoresuscitation after asystole in patients being considered for organ donation. Crit. Care Med. 2012; 40: 158–61. 27 Tibballs J, Russell P. Reliability of pulse palpation by healthcare personnel to diagnose paediatric cardiac arrest. Resuscitation 2009; 80: 61–4. 28 Tibballs J, Weeranatna C. The influence of time on the accuracy of healthcare personnel to diagnose paediatric cardiac arrest by pulse palpation. Resuscitation 2010; 81: 671–5. 29 Australia and New Zealand Intensive Care Society Death and Organ Donation Committee. The ANZICS Statement on Death and Organ Donation. 2013; 3.2. Available from: http://www.anzics.com.au/ death-and-organ-donation [accessed June 2014]. 30 Australia and New Zealand Intensive Care Society Death and Organ Donation Committee. Determination of Death. 2010. Available from: http://www.anzics.com.au/death-and-organ-donation [accessed June 2014]. 31 Dalrymple T. Between the lines: Premature burial. Br. Med. J. 2007; 334: 99.
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
doi:10.1111/jpc.12889
VIEWPOINT
Diagnosing death Stephen Jacobe Paediatric Intensive Care Unit, Children’s Hospital at Westmead, Westmead, New South Wales, Australia
Case History At 7:05 pm, Michael – not his real name – aged 2 was found by his mother unconscious, cyanosed and ‘lifeless’, after choking on a piece of apple. He was in asystole when the paramedics arrived at 7:13 pm. They administered three doses of adrenaline, intubated the trachea after removing some apple fragments and performed cardiopulmonary resuscitation (CPR). In the Emergency Department he received three further doses of adrenaline and ongoing external cardiac massage. There was no response and resuscitation efforts were halted at 7:53 pm by the Emergency Physician. With no signs of life and no palpable pulse, Michael was declared dead. At 8:10 pm a nurse noticed irregular respiratory efforts, and a weak pulse was palpable. Michael was re-intubated, placed on a ventilator and transferred to the Intensive Care Unit for ongoing management. Over the next 12 h Michael developed neurological signs consistent with brain death. At 1:00 pm the next day I performed an initial formal examination of brain stem reflexes, including an apnoea test, and found all reflexes absent. A ceretec cerebral perfusion study demonstrated absent cerebral blood flow at 2:49 pm. The parents declined the offer to consider organ donation and, following negotiation with the family regarding their farewells, Michael was extubated at 8:42 pm. Michael rapidly became pale, remained motionless with no respiratory effort, and was pulseless when examined approximately an hour later (9:45 pm). I met with Michael’s parents after they’d spent time with their son’s body and they asked, ‘When did Michael actually die? Did he die at home when he collapsed, or in the Emergency Department or when he was extubated?’ That relatively straightforward question was actually quite complex to answer. The pronouncement of death is important on many levels. It signals the start of the mourning period; various rights and rituals can proceed; legal affairs may be settled; succession can take place; in certain circumstances a person’s organs may be removed for transplantation; and medical treatment can be terminated.
Correspondence: Dr Stephen Jacobe, Paediatric Intensive Care Unit, Children’s Hospital at Westmead, Locked Bag 4001, Westmead, NSW 2145, Australia. Fax: +61 2 98451993; email: [email protected] Accepted for publication 28 July 2014.
In spite of the obvious importance of diagnosing death, a degree of uncertainty continues to surround the question of exactly when a person is actually dead. As Veatch writes: ‘defining death . . . is not a trivial exercise in coining the meaning of the term. Rather, it is an attempt to reach an understanding of the philosophical nature of man and that which is essentially significant in man which is lost at the time of death’.1 Death has religious, philosophical, metaphysical and scientific aspects, and some of the controversy can be explained by these different perspectives on death. Religious authorities traditionally viewed death as occurring when the soul departs the body. Philosophers might argue death occurs when ‘personhood’ is lost. Biologists might define death as loss of integration of the organism or even loss of integrity of all cells. Although ‘dying’ is clearly a process that precedes death, whether ‘death’ itself is a process or a distinct event marking a change from one binary state to another remains controversial.2,3 Surely a person must be either dead or alive; there can be no in between. There is potentially a time however when, with appropriate intervention, the dying process may be reversed and death prevented. Truog and Fackler suggested that, ‘the moment in this process at which death is said to have occurred is a point that cannot be discovered by any empirical process, but rather must be chosen by societal consent’.4 This article will explore when that exact moment may be, and how death might be reliably diagnosed.
Is ‘Death’ Reversible? Death is inevitable, but most of us wish to prolong our existence on Earth for as long as possible and certainly do not want to be ‘written off for dead’ until there is absolutely no hope left for recovery. Although developments in life-sustaining medical technology in the past 100 years (such as mechanical ventilation and organ transplantation) have added to uncertainties surrounding the timing of death, such uncertainties are by no means confined to the modern era. The phenomenon of apparent ‘resurrection’ is far from new. In addition to Jesus rising from the dead, the Bible describes a number of resurrections performed by Elijah and the resurrection of Lazarus 4 days after his death and entombment.5 Whether such accounts represent true resurrection or cases of premature burial is a matter of conjecture.
The Enlightenment – Resuscitation, Reanimation and Galvinism Scientific and social advances during the period of the Enlightenment (1740–1850) blurred the boundary between life and
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
573
Diagnosing death
S Jacobe
death and resulted in a widespread fear of being falsely diagnosed as being dead and potentially buried alive. The notion that the human body was a mysterious creation of God was being challenged by science. With access to human corpses for dissection and an increasing knowledge of physiology, physicians were beginning to discover the body’s more ‘mechanistic’ workings. By the late 18th century a number of Humane societies were developed ‘for the recovery of persons apparently drowned’.6,7 Techniques employed by resuscitators to ‘restore vitality’ included smelling salts (1721), artificial respiration (1744),8 rectal insufflation of tobacco smoke and the administration of electric shocks.7 Up to 2/3 of reported resuscitation attempts were said to be successful. A number of conditions including apoplexy, trances, syncope, fits, convulsions, and intoxication with opium or spirits were said to mimic death.7 Mesmerism (hypnosis) was demonstrated in the 1770s and, 50 years later, general anaesthesia could produce an almost death-like state; these were felt to represent states of ‘suspended animation’. Luigi Galvani demonstrated that electric shocks could produce muscle movements in isolated frog muscle.9 His nephew Giovanni Aldini toured Europe demonstrating the power of electricity. In 1803, at the Royal College of Surgeons in London, Aldini was provided with the fresh corpse of the hanged murderer George Foster. Aldini placed electrodes connected to a bank of batteries on various parts of Foster’s face and body, causing movements and grotesque contortions. Application of the electrodes to the ear and rectum were said to cause the corpse ‘such violent muscular contractions . . . as to almost give the appearance of reanimation’.10 Aldini concluded that galvanism ‘is stronger than any mechanical action . . . [and] affords very powerful means of resuscitation in cases of suspended animation . . .’10 It is widely believed that accounts of Aldini’s demonstration inspired Mary Shelley when writing her novel ‘Frankenstein’. These 19th century ‘scientific’ developments, as well as reports in medical journals of premature burial,11 led many to fear that death might be misdiagnosed, resulting in premature withdrawal of medical care and internment. Such fears fuelled and were fuelled by publications in the popular press and literature, for example, ‘The Premature Burial’ by Edgar Allan Poe, 1844. A range of tests of death were developed. Confirmatory signs included: absent inflammatory response to subcutaneously injected ammonia (Monteverde’s sign); no movement of flags attached to needles inserted into the heart (Balfour’s test); direct palpation of the heart via an intercostal incision (Foubert’s test); failure of a fingertip with a proximal ligature to become congested (Magnus’ sign); and persistent eyeball indentation following external pressure (Ripault’s sign). Tests of ‘sensibility’ included smelling salts, mustard up the nose, objects inserted under the fingernails, loud noise such as blowing a trumpet in the ear, scalding, and instilling tobacco smoke per rectum.12 In 1889, Sir Benjamin Ward Richardson published 11 ‘absolute signs and proofs of death’ in his book, Asclepiad:13 apnoea, absent cardiac activity (pulse, apex beat and heart sounds); absent turgescence (filling) of the veins; hypothermia; rigor mortis; coagulation of the blood; absent rust oxidation of a 574
bright steel blade plunged deep into the tissues; absent red colour when semi-transparent parts were transilluminated; absent muscle contraction under the stimulus of galvanism, heat or puncture; absent red blush of the skin after subcutaneous injection of ammonia; and putrefactive decomposition. The businessman and social campaigner William Tebb, previously active in anti-vaccination campaigns in America and Britain, co-founded the London Association for the Prevention of Premature Burial in 1896 and published ‘Premature burial, and how it may be prevented’.14 Tebb lobbied the government unsuccessfully to legislate for safeguards around diagnosing death to prevent premature burial. Some individuals, including Tebb, stipulated in their wills that they were not to be interred before signs of putrefaction. Patented safety coffins and waiting mortuaries (mainly in Germany) were developed in response to ‘moral panic’15 arising from a fear of premature burial (Fig. 1).
The 20th Century Many religions believe the moment of death coincides with the departure of the soul. Dr McDougal believed the soul contained ‘substance’. In 1907, to test this hypothesis, he conducted an experiment to weigh the soul.16 He observed closely six terminally ill patients placed on a bed mounted on a platform with sensitive beam scales. Sudden weight loss at the time of death would indicate the soul had departed. A weight loss of 3/4 ounce was observed in the first subject and 3/8 ounce in another. In two patients the balance beam dropped not once but twice. Two other patients were excluded due to ‘technical difficulties’. Despite this limited evidence, McDougal reported that the human soul weighed 3/4 ounce (21 grams).16 Prior to the early 20th century, apnoea resulted in hypoxia and inexorably progressed to cardiac standstill and death but mechanical ventilation, developed largely in response to the polio epidemic, broke this nexus. Patients who became apnoeic for whatever reason could now be kept alive. In the 1950s, a group of French neurologists observed a number of patients who were totally unresponsive and died despite ventilation, and all had cortical necrosis at subsequent autopsy. They coined the term coma depassé (beyond coma) for this condition.17 Developments in organ transplantation culminated in the first heart transplant in 1967 by Dr Christiaan Barnard in Cape Town. The donor heart came from a patient who died after ‘cardiac death’ (following cessation of life-sustaining treatment in the operating room). Some felt it was time to redefine death.
Redefining ‘Death’ An ad hoc Committee of the Harvard Medical School convened to examine the issue published guidelines in 1968 suggested ‘irreversible coma as a new criterion for death’.18 The criteria for irreversible coma were unreceptivity and unresponsivity; no movements or breathing; no reflexes; and a flat electroencephalogram (with no coexistent hypothermia or central nervous system depressant drugs) on two occasions 24 h apart. Many jurisdictions have legislation defining death. In Australia, all states and territories except Western Australia have a statutory definition of death as either irreversible cessation of all
Journal of Paediatrics and Child Health 51 (2015) 573–576 © 2015 The Author Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
S Jacobe
Diagnosing death
still be considered technically ‘dead’ by the same ‘circulatory’ criteria?19 Debate of these issues continues.20–22
The Lazarus Phenomenon Autoresuscitation is the spontaneous return of circulation after someone is pronounced dead, and this apparent ‘resurrection’ has been referred to as the Lazarus phenomenon. There is no consensus on how long circulation must cease after cardiac arrest before pronouncing death. Two recent systematic reviews summarise the literature on autoresuscitation.23,24 The more comprehensive found 27 articles describing 32 cases of autoresuscitation (aged 27–94 years), all very low quality case reports or letters to the editor.23 All cases occurred following failed cardiopulmonary resuscitation (CPR) from a few seconds to 33 min. The continuity of observation and methods of monitoring were highly variable, but in eight cases where continuous electrocardiogram (ECG) monitoring and exact times were reported, no cases of autoresuscitation occurred beyond 7 min after ceasing CPR. Only one article reported autoresuscitation in a child.25 Notably, there are no reported cases of autoresuscitation in the absence of CPR. There are no reports of autoresuscitation following planned withdrawal of lifesustaining treatment, a situation where donation after cardiac death (DCD) may be considered.23,26 This is important because the time to diagnosis of death when donating organs has a direct and measurable influence on organ recipient outcomes. Mechanisms proposed to explain the Lazarus phenomenon in failed resuscitation include impaired venous return due to airtrapping and positive intrathoracic pressure, delayed onset of drug actions, hyperkalaemia, myocardial stunning and transient asystole.24 A false-positive diagnosis of death may also be responsible.
False Positive Diagnosis of Death Fig. 1 Safety coffin designed by Franz Vester, 1868. Should a person be interred ere life is extinct, he can, on recovery to consciousness, ascend from the grave and the coffin by the ladder; or, if not able to ascend by said ladder, ring the bell, thereby giving an alarm, and thus save himself from premature burial and death.’ (See http:// australianmuseum.net.au/safety-coffins) [Accessed April 2015]
brain function or irreversible cessation of circulation of blood. Although the law may define death, a medical practitioner, following appropriate standards of the profession, has to diagnose and pronounce death. Controversies in diagnosing death persist. After the heart stops beating, how long before circulation has ceased ‘irreversibly’? How long must we wait before being certain that autoresuscitation (where the heart starts beating again spontaneously) will not, or more importantly cannot, occur? Is palpation of the pulse accurate enough to diagnose ‘cessation of circulation’, or is cardiac ultrasound necessary to demonstrate mechanical asystole? What about mechanical circulatory assist devices?: a patient declared dead on circulatory criteria may be placed on extra-corporeal life support, essentially heart-lung bypass, to maintain organ function prior to donation. Can they
Few patients undergoing emergency resuscitation have intraarterial pressure monitoring lines, so the assessment of ‘lack of circulation’ must rely on clinical signs such as no palpable pulse and absent heart sounds. A study assessing the reliability of the pulse check in infants and children found clinicians misdiagnosed pulselessness on 36% of occasions.27 Palpation of the brachial pulse was slightly more reliable than femoral palpation, and palpation for greater than 30 s also improved accuracy.28
How Should Death Be Diagnosed? Death may be diagnosed on circulatory or neurological criteria. Recent guidelines describe well the criteria for determining death on neurological grounds.29 Anyone practising in an area where they may be called upon to confirm death on neurological criteria must be familiar with these guidelines. Clinicians are more often asked to pronounce death on circulatory criteria. Pragmatically, the patient should be observed for at least 2 min for immobility/lifelessness, apnoea, absent skin perfusion, absent heart sounds and absent pulse.30 If a continuous ECG monitor is attached, 2 min of electrical asystole (assuming no technical difficulty) would confirm lack of circulation. In the presence of cardiac electrical activity (but
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absent palpable pulse), a cardiac ultrasound should ideally be performed to confirm the presence of mechanical asystole (pulseless electrical activity or PEA). In television medical dramas such as ‘ER’, the doctors are often portrayed declaring death simultaneously with termination of resuscitation (‘I’m going to call it – time of death, 10:43’) without performing any formal examination for ‘signs of life’. Although autoresuscitation is rare, it can occur following failed CPR, can traumatise family and staff members alike and lead to a mistrust of doctors. The declaration of death must be thorough and unhurried and ‘decoupled’ from cessation of CPR. It is therefore recommended that once CPR ceases, the patient should be observed for signs of life for at least 10 min before the formal examination and declaration of death.
Conclusions There is arguably a narrow yet profound difference between ‘dying’ and ‘dead’. Doctors must ensure that they do not confuse the two and are clear about how to diagnose death. Death should not be diagnosed until at least 2 min of electrical asystole has been observed or, in the presence of cardiac pulseless electrical activity, 2 min of ‘acirculation’ (i.e. mechanical asystole), confirmed either by echocardiography/cardiac ultrasound or intra-arterial pressure monitoring. If neither is available, careful palpation of a central pulse for at least 60 s is recommended prior to declaring death. Apart from declaring death for DCD, there is generally no need for haste. Theodore Dalrymple wrote31 that, as an exhausted houseman, he was phoned by a nurse on the ward in the middle of the night to be told, ‘Doctor, I think Mr Jones is dead’. He replied, ‘Well, if you’re right, he’ll still be dead in the morning’, and went back to sleep. As for Michael, I declared that he died at 8:42 pm – the exact same time he came into the world, and a time of lasting significance for his parents.
References 1 Veatch RM. Case studies in bioethics: brain death: welcome definition . . . or dangerous judgment? Hastings Cent. Rep. 1972; 2: 10–13. 2 Morison RS. Death: process or event. Science 1971; 173: 694–8. 3 Kass LR. Death as an event: a commentary on Robert Morison. Science 1971; 173: 698–702. 4 Truog RD, Fackler JC. Rethinking brain death. Crit. Care Med. 1992; 20: 1705–13. 5 Clarke A. The Holy Bible, Containing the Old and New Testaments . . . : With a Commentary and Critical Notes, Vol. 1. London: Applegate & Co., 1856. 6 Johnson A. An Account of Some Societies at Amsterdam and Hamburgh for the Recovery of Drowned Persons: And of Similar Institutions at Venice, Milan, Padua, Vienna, and Paris; with a Collection of Authentic Cases 1773. London: Woodbridge, 1986. 7 Hawes W. Reports of the humane society for the recovery of persons apparently drowned 1783–1784. Available from: https://books .google.com.au/books?id=WbwpAAAAYAAJ&printsec=frontcover& dq=Reports+of+the+Society:+Instituted+in+1774,+for+the+Recovery+ of+Persons+...&hl=en&sa=X&ei=j5ocVYjALoTRmAXCoIDABA&ved= 0CB0Q6AEwAA [accessed April 2015].
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