122

Original Article

AbstractBackground: In several instances, the diagnosis of brain death has been questioned due tothe presence of movements. This case report and review of the literature illustrates thespectrum of movements that have been encountered in brain death.

Methods: A case report and review of the literature on movements seen in brain death wasconducted.

Results: Movements in brain death are common and have a wide range of phenomenology.Several movements wax and wane over time, making movements in brain death difficultto classify. In addition, varying terminology has been used (e.g., Lazarus sign, spinal man,spinal reflexes, spinal automatisms). Although evidence points to a spinal origin for suchmovements, the pathophysiology in many cases remains speculative. Characteristics of move-ments in brain death have been identified that can help differentiate them from brainstemor voluntary origin.

Conclusions: Based on our review, we suggest referring to stimulus-provoked movementsas reflexes and spontaneous movements as automatisms. We propose using the terms braindeath-associated reflexes and brain death-associated automatisms as two main categories for move-ments that occur in brain death. These terms do not imply a specific pathophysiology, butconsistent clinically oriented nomenclature may be useful when reporting such phenomena.

(Neurocrit. Care 2005;3:122–126)

Brain Death-Associated Reflexes and AutomatismsSamay Jain1,* and Michael DeGeorgia2

1Division of Movement Disorders, Neurological Institute, New York, NY and 2Department of Neurology and Neurosurgery,The Cleveland Clinic Foundation, Cleveland, OH

*Correspondence andreprint request to:

Samay JainDivision of MovementDisorders,Neurological Institute,710 W. 168th St., 3rd Floor,New York, NY 10032.E-mail: sjain@neuro.columbia.edu

Neurocritical CareCopyright © 2005 Humana Press Inc. All rights of any nature whatsoever are reserved.ISSN 1541-6933/05/3:122–126DOI: 10.1385/Neurocrit. Care 2005;3:122–126

Humana Press

BackgroundBrain death is defined as the permanent

absence of cortical and brainstem function. Thegrowth of critical care has contributed to theneed for accurate and timely diagnosis of braindeath. Occasionally, certain movements mayraise the possibility of persistent brainstemfunction, such as the spinal cord-generatedendotracheal suction-thoracic contractionreflex that can mimic a cough reflex. We pres-ent an illustrative case report and review theliterature on the spectrum of movementsobserved in the setting of brain death. Toimprove clarity in reporting, we also suggest aconsistent nomenclature for these movements.

MethodsAretrospective review of handwritten and

electronic records of a patient with motor

activity in the presence of brain death wasconducted, followed by a review of the liter-ature. The Institutional Review Board of TheCleveland Clinic Foundation approved thisstudy.

Case ReportA41-year-old man presented with dyspnea

and hypoxia after 1 week of cough, pleuriticchest pain, nausea, and vomiting. Pulmonaryembolism was suspected, and he was antico-agulated with intravenous heparin. Shortlythereafter, he developed asystole and ventric-ular fibrillation. He was resuscitated after 15minutes but again developed asystole.Echocardiography demonstrated a large peri-cardial effusion, and a pericardiocentesis wasimmediately performed. Return of sponta-neous circulation occurred after 23 minutes.

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Brain Death: Associated Reflexes and Automatisms

Neurological examination found him to be intubated andcomatose. He had spontaneous and frequent eye opening thatwas not stimulus sensitive. Pupils were minimally reactivebilaterally. Eyes were straight ahead with no movement withoculo-cephalic maneuvers. Corneal and gag reflexes wereabsent, although he was breathing spontaneously above theset ventilator rate. There were no limb movements to painfulstimulation. He had myoclonic jerks of the face and body, withbilateral lower extremity adductor myoclonic movements.Muscle stretch reflexes were present in the upper extremitiesand absent in the lower extremities. Babinski sign was absent.Abrain computed tomography scan showed effacement of thebasal cisterns consistent with early brain edema.

Later that day, the patient again developed ventricular fib-rillation terminated by countershock. Echocardiographyshowed a small residual pericardial hematoma. The next day,the patient had fixed and dilated pupils and bilateralpapilledema. He had no spontaneous respirations and no brain-stem reflexes, fulfilling brain death criteria. Motor examina-tion demonstrated triple flexion of the lower extremities. Inthe upper extremities, noxious stimulation of the right armresulted in ipsilateral flexion at the elbow and supination ofthe arm, bringing the forearm to rest on the patient’s abdomen.Minute flexion and extension movements occurred sponta-neously in the toes. These movements persisted for 5 days afterthe anoxic event. Electroencephalography revealed electro-cerebral silence.

Review of the Literature

HistoryMovements occurring in the setting of death have been

noted for centuries. During the French Revolution, body move-ments among the beheaded, such as eyelid and jaw contraction,were frequently observed. The guillotine usually cut throughthe lower part of the fourth cervical vertebra (1). Brain deathwas formally defined in 1968 as the irreversible loss of cere-bral and brainstem function (2). At that time, the presence ofany spontaneous or reflex movements invalidated the diag-nosis. Since then, several other criteria have been publishedthat account for brain death-associated motor activity (3).

Most of the literature on this subject includes case reports orsmall series. A summary of the literature is provided in Table 1.Major difficulty in discussing such movements is the lack ofconsistent terminology or categorization. Discussion could beorganized in terms of phenomenology, time of appearance afterbrain death, pathophysiology, or phylogentically. We chose toorganize our review by phenomenology, because this categoryis the least speculative and would likely be of most clinical use.We then briefly discuss time of onset and pathophysiology.

When describing movements in the presence of breath death,there can be linguistic challenges (1). Once a patient is declaredbrain dead, some have argued it is inappropriate to continueto use the term “patient.” In the literature, terms include “heart-beating cadavers” (1), “spinal man” (4), and “brain dead body”(5). In this review, we prefer the simple term of brain dead body.

EpidemiologyIvan retrospectively reviewed 52 brain dead bodies and

found muscle stretch reflexes in 35%, plantar flexor responsesin 60%, plantar withdrawal in 35%, and abdominal reflexes in

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Neurocritical Care ♦ Volume 3, 2005

75% (6). In the same year, Jorgensen introduced the term “spinalman” in reference to such phenomena (4). In his series of 63brain dead bodies, he found a withdrawal response in the lowerlimbs in 79%, and muscle stretch reflexes in 49% of upperextremities and 33% of lower extremities. Jorgensen firstdescribed extension and pronation of the arm in response tocutaneous stimulation, seen in one-third of brain dead bodies.

Saposnik and coworkers prospectively evaluated sponta-neous and reflex movements in 38 brain dead bodies (1) throughnoxious stimuli to the sternum, four limbs, and supraorbitalarea; neck flexion; tactile simulation to the palms of hands andsoles of feet; and elevation of four limbs. Thirty-nine percentof brain dead bodies had either spontaneous or reflex move-ments. These movements were observed mainly within thefirst 24 hours after declaration of brain death and consisted ofspontaneous jerks of the fingers, undulating toe flexion, tripleflexion, unilateral facial myokymia, “Lazarus sign,” upper limbpronation/extension reflex, and flexor plantar response. Inanother study, Dösemeci and coworkers found similar spinalreflexes in 18 of 134 brain dead bodies (13.4%) (7). Saposnikand coworkers reported movements in 47 out of 107 brain deadbodies (44%) (8).

Conci and coworkers looked at 25 brain dead bodies dur-ing kidney removal with a mean time on the ventilator beforenephrectomy of 31 ± 6 hours (9). Abdominal muscle contrac-tion was noted in 60% of brain dead bodies when the parietalperitoneum was cut. Twenty-four percent had sudden changesin blood pressure and heart rate during the incision. Noresponse was seen to bowel manipulation.

Patterns of Motor ActivityMovements that have been studied in brain dead bodies are

numerous. What follows is not intended to be a comprehensivelisting of all movements documented in brain death. Rather, pat-terns of well-documented motor activity in the presence of braindeath are summarized. This summary includes polysegmentalspinal reflexes and automatisms, “Lazarus sign,” undulating toesign (undulating toe flexion movements), eyelid opening, res-piratory-like movements, head turning, pseudodecerebrateposturing, facial myokymia, eyelid opening, abdominal move-ments, upper and lower facial movements, eyelid and tonguemyoclonus, and spinal myoclonus.

Spittler and coworkers focused on systematically describ-ing polysegmental spinal reflex patterns and polysegmentalspinal automatism patterns in brain death (5). They catego-rized spinal movements as monosegmental muscle stretchreflexes, oligosemental cutaneo-muscular reflexes, poly-segmental spinal reflex patterns (PSRPs), polysegmental spinalautomatism patterns (PSAPs), and “Lazarus sign.”

Spittler et al. examined 235 patients on 278 examinationsfor brain death. Interindividual and intraindividual phe-nomenological variability was noted. Thus, the authors set outto distinguish characteristics by which PSRPs and PSAPs canbe differentiated from voluntary or brainstem-generated invol-untary movements. They assigned the loss of pupillary lightreflex as the start of the brain death process and loss of thecough reflex the completion of the brain death process.

Spinal movements were observed on 42 occasions in 27 ofthe brain dead bodies. Up to five distinct spinal reflexes wereobserved in a single body. Thirty-one different spinal reflexes

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Brain Death: Associated Reflexes and Automatisms

and four different spinal automatisms were documented. Whendiscussing their findings, Spittler et al. stated, “The variableelicitation mechanisms and the different patterns of reflexesand automatisms make a systematical classification difficult:A uniform registration even of latency and duration for allforms of reflexes is not feasible and in cases of automatisms isimpossible” (5). Dösemeci and coworkers described spinalreflexes which included the Lazarus sign, flexion of the armswith abduction of the shoulders, extension at the arms andshoulders, and flexion of the arms and feet. The most commonmovement they reported was finger and toe jerk (7). Saposnikand coworkers found undulating toe flexion movements to bethe most common, seen in 23% of brain dead bodies (8).

Spittler et al. noted wide interindividual variation, and mostpatterns were observed in only one body. However, salient char-acteristics of polysynaptic spinal reflexes and automatisms werefound, which can be useful when attempting to rule out brain-stem activity. Spinal movements were found to have stereo-typical elicitation upon a trigger of limited variation, constantpattern of latency and duration, habituation with frequent trig-gers (refractory period), no habituation with slow sequence oftriggers, similarity of reflexes and automatisms, and a mono-tone stereotyped course of the motor pattern. Well- documentedbrain death movement patterns are summarized in Table 1.

Timing of Movements in the Course of Brain Death

Although most movements are observed within the first 24hours after the declaration of brain death, the timing can behighly variable (hours to days). The timing of brain death isdefined by the time a clinical brain death exam fits acceptedcriteria, which may be seconds, minutes, hours, or days afterphysiological brain function has ceased. Jorgensen made theobservation that those who lost spinal reflexes and regainedthem did so within 6 hours (4). This timing occurred with theflexion-withdrawal response first, followed by the cremastericand abdominal reflexes, and then muscle stretch reflexes. Thedelayed appearance of spinal reflexes was invariably associ-ated with severe arterial hypotension. Dösemeci noted that allspinal reflexes were seen during the first 24 hours after braindeath was confirmed and remitted by 72 hours (7). Undulatingtoe flexion movements are more likely to be seen in the first12 hours after the diagnosis of brain death (8).

PathophysiologyThe spinal cord is the putative source for movement of the

brain dead body. Various mechanisms have been proposed forthese movements. Conci and coworkers proposed that spinalreflexes are present in brain death if the ischemic lesion is aboveC1–C4 (9). Within the spinal cord, neuronal networks exist thatserve as central generators for specific motor patterns (1).Corticospinal and rubrospinal tracts located in the lateral funicu-lus control distal portions of the limbs. Vestibulospinal andreticulospinal tracts modulate tone and posture, contributingto synergistic movement of an entire limb. Supraspinal dis-connection of these tracts may increase their excitability at thespinal level, resulting in spinal movements emerging duringbrain death. However, this possibility has not been thoroughlystudied, and the precise physiology is unknown.

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Neurocritical Care ♦ Volume 3, 2005

Spittler and coworkers proposed that some spinal reflexescan be considered phylogenetically “old motor patterns,”which may be set free when the cord is uncoupled from the“younger” input of the brainstem and neocortex. This per-spective allows an orderly categorization of some observedphenomena. In this schema, spinal reflexes or automatismsthat do not have an apparent evolutionary purpose can beunderstood as disintegration or irradiation of spinal circuitry.The temporal variability of the emergence of spinal reflexeshas been explained by spinal shock that can be observed afterbrain death (6).

Lazarus sign has been reported to occur spontaneously, afterrespirator removal, during apnea testing, in the setting of arte-rial hypotension, noxious stimuli, or passive neck flexion(7,9–14). It has been thought to result from hypoxic stimula-tion of cervical spinal cord neurons functionally isolated fromrostral brain areas. Supportive of this concept was the findingby de Freitas and coworkers of complex spinal reflexes in a sub-set of brain dead bodies with lower systolic blood pressures(10). Mechanical stimulation of spinal roots, cord, or sensoryneurons also may contribute to this complex movement (15).

Hanna and Frank comment that automatic stepping is aspinal automatism that occurs in animals after transaction atthe superior colliculus level and cite evidence that supports aspinal pattern generator for locomotion (16). Stepping motionsoccur in patients before brain death when brain inhibition isreleased and transmission is continued in the ventral spinalcord and brainstem motor tracts.

Short-latency somatosensory evoked potentials have beenrecorded in the presence of upper and lower extremity move-ments during brain death (8,11). During arm movements noresponses were recorded on scalp electrodes except far-fieldcomponents. The spinal N13 component was preserved.Auditory brainstem-evoked potentials were absent for bothears, demonstrating preserved spinal dorsal horn potentialsin the presence of movements. Further evidence for suchmovements being spinal in origin comes from Saposnik andcoworkers. In five brain dead bodies that had undulating toeflexion movements, SSEPs did not elicit cortical responses (8).Urasaki and coworkers postulated that respiratory-likemovements can be spinal in origin (11).

Facial myokymia is a movement that has been studied bythe orbicularis oculi reflex and facial nerve stimulation. Whentested, the early and late components of the orbicularis oculireflex were found to absent bilaterally, whereas peripheralnerve conduction was preserved. This finding suggests facialmyokymia in brain death is due to muscle denervation (2).

DiscussionOur review shows that movements in brain dead bodies

are common and display a wide spectrum of phenomenology.The terms “automatism” and “reflex” have been used incon-sistently, at times referring to the same movement. We suggestreferring to stimulus-provoked movements as reflexes andspontaneous movements as automatisms. In the setting of braindeath, we propose using the terms brain death-associated reflexesand brain death-associated automatisms. This terminology is clin-ically useful because all movements reported in brain deadbodies can be placed in one of these two categories.

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Furthermore, it does not imply a particular mechanism, whichremains speculative in some cases. Although primarily descrip-tive, these terms have important implications. Brain death-asso-ciated reflexes are stimulus provoked movements that do notcontradict the diagnosis of death. Such movements may or maynot be present during life. Thus, subsets of these reflexes includemuscle stretch reflexes, abdominal reflexes, and plantar flexion.Likewise, brain death-associated automatisms are spontaneousmovements that do not contradict the diagnosis of death.

Brain death-associated reflexes and automatisms can betime dependent, emerging or resolving depending on the timeelapsed from the onset of brain death. If possible, it is impor-tant to determine the time elapsed from declaration of braindeath to the onset of movements. Most reported brain stem-associated reflexes are no longer present 72 hours after braindeath declaration. Certain characteristics are typical of move-ments in brain death that can help differentiate them fromvoluntary or brainstem-derived motor activity (5). Evokedpotentials may be helpful when the spinal origin of a particularmovement is questioned (11).

The diagnosis of breath death has evolved to incorporatethe observations of brain death associated reflexes and automa-tisms. In 1995, the American Academy of Neurology estab-lished criteria for the diagnosis of brain death which includedcertain movements as acceptable findings (16). These mani-festations are occasionally seen and should not be misinter-preted as evidence for brainstem function:

1. Spontaneous movements of limbs other than pathologi-cal flexion or extension response.

2. Respiratory-like movements (shoulder elevation andadduction, back arching, intercostal expansion withoutsignificant tidal volumes).

3. Sweating, blushing, tachycardia.4. Normal blood pressure without pharmacological sup-

port or sudden increases in blood pressure.5. Absence of diabetes insipidus.6. Deep tendon reflexes, superficial abdominal reflexes,

triple flexion response.7. Babinski reflex.

However, movements in the setting of brain death stillcast doubt on the diagnosis (7), resulting in considerationof confirmatory testing and prolonged treatment. When clin-ical criteria for brain death are met, the recognition of braindeath-associated movements can reduce uncertainty ofdeath and reliance on confirmatory testing. Greater aware-ness of such motor activity can reduce doubt for cliniciansand provide an explanation for families in the difficult sit-uation of witnessing brain death-associated movements.

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Neurocritical Care ♦ Volume 3, 2005

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