Spontaneous and reflex movements in brain death

Methods.

Among patients admitted to our hospital from July 1997 to January 1999, we prospectively studied all subjects with a diagnosis of BD. All cases met the criteria for BD, as established by the American Academy of Neurology Practice Parameters,1 including the following: unresponsiveness or coma, absence of brainstem reflexes, and apnea. These clinical features had to be present for at least 24 hours. Hypothermia and drug intoxication were excluded. An EEG was performed in all patients with motor movements. All patients had an appropriate workup to determine the cause of BD, including a CT scan of the head. Laboratory tests were performed in all subjects to exclude metabolic causes of coma.

We looked for a relationship between the presence of movements and the cause and duration of BD. All patients were evaluated by at least two neurologists, one of them specializing in movement disorders. In all cases, we followed a standardized protocol, especially designed to bring out motor movements, before and during an 8- to 10-minute apnea test, including 1) painful stimuli to the sternum, four limbs, and supraorbital area; 2) neck flexion; 3) tactile stimuli to the palmar and plantar areas; and 4) elevation of the four limbs. All patients with movements were recorded on video after the appropriate consent of the next of kin.

Results.

During the study period, 38 patients met criteria for BD. Their mean age was 45 years (range 1 to 77). Eleven individuals had intracerebral hemorrhage; 8, subarachnoid hemorrhage; 5, traumatic brain injury; 3, anoxic encephalopathy; 3, cerebellar hemorrhage; 3, pontine hemorrhage; 2, brain tumors; 1, meningitis; 1, subdural hematoma; and 1, primary intraventricular hemorrhage.

Fifteen (39%) subjects had motor movements. In all cases, motor movements were observed in the first 24 hours of BD diagnosis, and in no case were they present for longer than 72 hours. They were slightly more common in men (44%) than in women (30%). Six patients had spontaneous jerks of the fingers, three undulating toe flexion sign, two triple flexion reflex, one unilateral facial myokymia, one “Lazarus sign,” one upper limb pronation–extension reflex, and one had a flexor plantar response (table). We found spontaneous or reflex movements in patients with all of the above-mentioned causes of BD except in those with subarachnoid hemorrhage or meningitis. Movements were seen both before and during the apnea test. They were triggered by tactile stimuli, except for limb jerks and facial myokymia, which were spontaneous. Movements were present whether patients were normotensive or hypotensive. The EEG did not show discharges in any patient with movements.

Discussion.

In the past, death was a synonym of immobility. However, BD patients may have movements. BD is a state that includes absence of cortical functions and brainstem reflexes. It ends with the cardiac arrest, usually occurring within 24 to 48 hours.

We designed a standardized protocol to determine the frequency and characteristics of motor movements in patients who fulfilled diagnostic criteria for BD. We found 15 (39%) subjects with such movements, the most common being jerks of the fingers (myoclonus-like).

In 1973, Ivan5 examined 52 patients with BD and found deep tendon reflexes in 35%, plantar flexor responses in 35%, and abdominal reflexes in 40%. Another series of 63 patients with BD showed the presence of deep tendon reflexes of the upper extremities in 31 subjects and of the lower limbs in 24. In 50 patients, there was a withdrawal response of the lower limbs and in 21, an extension and pronation of the arm and forearm in response to cutaneous stimulation.6 In one report, a 28-year-old woman injured by a bullet had spontaneous jerking movements of the left leg followed by flexion–extension movements of the upper and lower extremities that remained for 5 days.7 Another study reports the classic “Lazarus sign” in 5 patients with BD, with the typical sequence of bilateral arm flexion to the chest, shoulder adduction, and hand crossing.8 Later on, there was another report of a case of Lazarus sign in a BD patient during nonhypoxic apnea testing.9 Furthermore, one report describes 3 subjects with BD with complex patterned sequential movements of the toes, which were called the “undulating toe flexion sign.”10 In the literature, there is no report of abnormal facial movements in BD subjects. The presence of this kind of movements could be interpreted as a brainstem reflex, which can invalidate the diagnosis of BD according to all proposed criteria.

All the above-mentioned studies were retrospective and did not follow a standardized protocol to evaluate motor movements. Moreover, BD diagnostic criteria differed among them. Although our series is small, our findings confirm that motor movements may be a common phenomenon in BD, with jerks of the fingers being the most frequent. Other motor movements include undulating toe flexion, triple flexion response, upper limb pronation–extension reflex, Lazarus sign, plantar flexor response, and facial myokymia. We believe that these motor movements represent spinal reflexes. However, caution should be used when considering facial myokymia as an accepted movement in BD patients because it may represent brainstem activity. Electrophysiologic, functional imaging, or flow studies can help to elucidate the nature of all of these motor movements in the setting of a standardized protocol.

We conclude that motor movements in BD patients may be more common than reported and usually are seen in the first 24 hours of the BD diagnosis. Because of the practical and legal implications, neurologists need to identify these movements. Their presence may not preclude the BD diagnosis.