Neurosurg. Rev.
15 (1992) 249-254
Brain death: practicability o f evoked potentials Raimund Firsching, Reinhold A. Frowein, Stefan Wilhelms, and Friedrich Buchholz Neurosurgical Clinic, University o f Cologne, Fed. Rep. o f G e r m a n y
Abstract
2 Patients and methods
Multimodally evoked potentials were registered in 85 patients who fulfilled the criteria for brain death. While somatosensory and visual evoked potentials have been found to be of limited value for the diagnosis of brain death, the stepwise abolition of brain stem auditory evoked potentials (BAEP) confirmed brain death in 26 out of 85 patients, i.e. 31%. Registration of the abolition of BAEP is concluded to be a safe and acceptable confirmatory test. It is, however, more feasible for institutions, in which BAEP are analysed routinely. In spite of all efforts sequential BAEP could not be used for the diagnosis of brain death in the majority of cases either because of absence of reproducible responses at the initial registration or because the patient was already apnoic at the time of the initial BAER Assuming that bilateral preservation of wave I has the same significance as the stepwise abolition of BAEP, since it also proves the integrity of the peripheral receptor, BAEP are relevant for the declaration of brain death in approximately 30% of patients.
In a prospective study somatosensory (SEP), visual (VEP), and brain stem a u d i t o r y (BAEP) evoked potentials were recorded in 265 comatose patients in a neurosurgical intensive care unit within 48 hours of admittance or onset o f coma. O f these, 85 patients reached the level o f apnoic brain stem areflexia and met the criteria o f brain death as r e c o m m e n d e d by the "Wissenschaftlicher Beirat, Bundes/irztekammer" (1986). N o patient was hypothermic or had received barbiturates. Causes o f c o m a are listed in table I. Eight patients h a d a p r i m a r y infratentorial lesion.
Keywords: Brain death, evoked potentials. 1 Introduction The recording o f evoked potentials in brain death is getting increasing attention [1, 3, 1 2 - 1 6 , 1 9 22]. The stepwise abolition o f brain stem a u d i t o r y evoked potentials (BAEP) in p r i m a r y supratentorial brain lesions has been suggested as one of four equally relevant alternative tests to confirm the irreversibility o f the loss of brain function after a p r i m a r y supratentorial lesion. The other three tests are a 12 hour waiting period with repeated confirmation of apnoic cranial nerve areflexia, an isoelectric E E G , and cerebral circulatory arrest as d e m o n s t r a t e d by a n g i o g r a p h y [24]. This report is an account o f our practical experience with evoked potentials from patients a p p r o a c h i n g brain death. 9
1992 by Walter de Gruyter & Co. Berlin - New York
Table I. Causes of coma Number of patients Head injury Subarachnoid hemorrhage Intracerebral haematoma Tumor Others
41 18 15 6 5
Total
85
The apnea test was performed in each o f the 85 patients and was carried out when c o m a and complete loss o f cranial nerve reflexes were noted:, W i t h intratracheal administration o f oxygen, ap2 nea was assumed when no breathing was noted inspite o f significantly increased paCO2 b l o o d gas levels after an interval of 10 to 20 min. As d o c u m e n t a t i o n o f the stepwise abolition of B A E P requires a m i n i m u m o f two recordings, it was tried to obtain recordings o f SEP, VEP and
250
Firsching et al., Brain death: practicability of evoked potentials
B A E P prior to and after the apnea test. This was not possible in all 85 patients, mostly because o f intermittent cardiovascular failure or apnea at the time of, or shortly after, admittance. The timing o f the recordings o f evoked potentials is listed in table II. Technical details of the recording o f evoked potentials as used in this study are listed in table III ]9, 10]. Table II. Timing of recording of evoked potentials
Number of patients BAEP
SEP and VEP
22 62 48
18 57 46
m a r y absence o f the N20 c o m p o n e n t p r i o r to the apnea test was noted in 41 patients o f 75 patients (55%) investigated. The cervical response was preserved in 11 out o f 18 patients, i.e. 61% p r i o r to the apnea test but after the onset o f c o m a a n d cranial nerve areflexia. After the apnea test the cervical response was reproducible in 28 of 57 patients, i.e. 49%. In patients with infratentorial lesions after the apnea test the cervical responses was preserved in 50%. The response at the cervical plexus, (Erb's point) was preserved in all patients at all times.
3.2 V E P
Before apnea test only After apnea test Before and after apnea
Table III. Technical standards for the registration of evoked potentials
SEP Stimulus: Bandpass: Analysis time: Montage: VEP Stimulus: Bandpass: Analysis time: Montage: BAEP Stimulus:
Bandpass: Analysis time: Montage:
2 x 512 200 Ixs < 20 mA at 5.4 Hz stimulations of median nerve at wrist LF : HF 30 : 3000 Hz 30 ms 1. Erb's point-Fz, 2. Neck at C2-Fz, 3. Contralateral scalp (C3/C4)-Fz
VEP were absent in all cases except one in w h o m c o m a and cranial nerve areflexia were noted, b o t h before and after the apnea test. In five patients VEP were absent before the apnea test, at a time when the E E G did not show electrocerebral silence (ECS). There was one exceptional, but n o t unexpected observation in a case with a posterior fossa haemorrhage: b o t h a nearly n o r m a l E E G , and reproducible VEP were recorded after apnea h a d been d o c u m e n t e d (Figure 1). In six patients the amplitude o f the electroretinogram seemed to increase after the apnea test (Figure 2). 3.3 B A E P
2 • 256 unilateral flashes at 1.7 Hz L F : H F 1 : 100Hz 250 or 300 ms 1. ipsilateral lateral eyelid-Cz, 2. Oz-Cz
2 • 1024 unilateral alternating rarefaction/condensation 200 gs clicks delivered at 11.1 Hz with 95 dB and 65 dB contralateral white noise masking LF : HF 150 : 3000 Hz 10 ms ipsilateral ear lobe-Cz
3 Results 3.1 S E P
The cortical N20 c o m p o n e n t was absent in all 46 patients investigated after the apnea test. The stepwise abolition o f the N20 component, which required an intact N20 at the initial recording before the apnea test, was observed in 23 patients. Pri-
The first registration of B A E P in 85 patients, who h a d exhibited apnoic brain stem areflexia, demonstrated the complete bilateral loss o f waves I I I to V in 49 patients. 36 patients h a d a bilateral wave III or later c o m p o n e n t s o f the B A E P (Figure 3). A bilateral wave I was found in three cases at the initial registration, one before and two after the apnea test. The stepwise bilateral abolition o f waves I I I to V after the apnea test was observed in 34 patients. Since 8 o f these patients h a d an infratentorial lesion, abolition o f B A E P was relevant to the declaration o f brain death in 26 patients. B A E P findings after the apnea test (Figure 4) d e m o n s t r a t e d a complete loss o f all c o m p o n e n t s in 82% of cases. A unilateral wave I was seen in 11%, and three patients d e m o n s t r a t e d a bilateral wave I, and one o f these h a d an additional unilateral wave II. In cases with infratentorial lesions seven out of eight patients exhibited no wave after the apnea test, one patient h a d a bilaterally preserved wave I. Neurosurg. Rev. 15 (1992)
Firsching et al., Brain death: practicability of evoked potentials
251
VEP
M.E. 1652/90 59 y. female Posterior fossa haemorrhage
after brainstem areflexia and apnea .
.,~.~
left eye
,
~.~ right eye
300 ms
/
300 ms
Figure 1. Preserved VEP after apnoic brain stem areflexia in a patient with an infratentorial lesion.
S.B. 185/89 56 y. male Subaraehnoid haemorrhage Clouding o! consciousness
VEP
left eye
right eye
Cz-Oz 5
f
~
~
Eiectroretinogram ~
, i . . . . . .
[2.4pV
Electroretinogram
I i i t,,
250 ms
J,,,
t[2.4pV
250 ms
Apnoic brainstem areflexia left eye ~~-..
~ .............
-
right eye
-~'~-.-...... C~-O= /\, /,'.,:\
U' \l
......J~"~ f~ "t, Electroretmogram L ',
)
,,,
~,,,,,
/ ~f
,[3.05pV 250 ms
x~.~.k.&_r~_ 7 Electroretinogram r
250 ms
Figure 2. While the cortical response is abolished after onset of apnoic brain stem areflexia, the amplitude of the electroretinogram appears to have increased.
4 Discussion
In most of the increasing number of studies dealing with evoked potentials in brain death either the exact timing of the investigation as related to the apnea test is not specified or only single investigations are performed instead of sequential recordings giving evidence of the stepwise abolition Neurosurg. Rev. 15 (1992)
of evoked potentials. Registration of evoked potentials, however, is only of confirmatory value for the diagnosis of brain death after the apnea test. Sequential recordings giving evidence of the stepwise abolition of evoked potentials have been considered mandatory to make sure, the peripheral receptors had been intact [24].
252
Firsching et al., Brain death: practicability of evoked potentials BAEP findings at initial registration of patients developing brain death.
BAEP findings after the apnea test
Number 50 of patients 4O
100
%
82%
Percentage of patienls
30 50 20 10-
no wave
[--] I--1 unilateral bilateral wave[ waveI
I~ uni- or bilateral wave~
11% ~ bilateral wave Tif toy
Figure 3. Approximately half of all patients developing brain death had bilateral reproducible waves III to V at the initial investigation.
4.1 SEP The stepwise abolition of cervical and cortical SEP during the onset of brain death may indicate the loss of function of the cervical cord and brain stem. As only a cephalic reference was used in this series, the distinction of a cervical and a lower brain stem response within the cervical N13 component [20] was not possible. We found, as did other authors [1, 3, 12, 13] with a cephalic reference only, that 52% of the cases had no cervical responses after the apnea test. Absence of cortical SEP does not have the same significance as an isoelectric EEG, as absence of SEP is frequently observed in patients with nonisoelectric EEGs, and survival without cortical SEP in patients without concurrent spinal injuries has been repeatedly observed [5, 9]. Furthermore, reappearance of lost SEP has been reported [26]. Since 55% of all patients investigated before and after the apnea test had no cortical SEP at the initial registration and 11 patients were not amenable to registration of evoked potentials until after the apnea test, the stepwise abolition could only be documented in 31%, i.e., 23 out of 75 patients. Thus, its value for the determination of brain death remains controversial.
4.2 VEP Preservation of an active electroretinogram (ERG) in brain death has been reported for over 20 years [2, 23]. The increased amplitude of the E R G at brain death in some cases in this series is difficult
no wave
4%
1.5%
1.5%
unilateral bilateral unilateral bilateral waveI waveE wave]s wave][
Figure 4. Bilateral wave I after the onset of apnoic brain stem areflexia was noted in 4% of cases.
to explain, it may possibly be due to variable impedances in spite of efforts to keep them at steady levels of less than 5 kohm. Preservation of VEP in apnoic patients with brain stem areflexia has been described before [7], but remains a rare finding. It confirms the need for a test of supratentorial cerebral functions in apnoic brain stem areflexia after primary infratentorial lesions. VEP and EEG findings do not always coinciCe. In this series the absence of VEP was encountered with non-isoelectric EEGs in several instances. In one exceptional case, concussion of the chiasm was considered the probable cause. We have, however, not yet encountered an isoelectric EEG accompanied by a preserved VEP. The value of VEP for the determination of brain death thus also appears limited.
4.3 BAEP The registration of the stepwise abolition of BAEP has been suggested as a test for the confirmation of the irreversibility of the loss of brain function after supratentorial lesions [24]. At least two sequential recordings are recommended, the first giving evidence of a bilaterally preserved wave III to ensure the function of the peripheral receptor. Stepwise abolition was observed in 26 out of 85 patients, i.e. 31%, who developed brain death. In practice it is not always easy to distinguish individual components in abnormal BAEP, in some cases additional recording of middle latency auditory evoked potentials may be helpful [8]. Neurosurg. Rev. 15 (1992)
Firsching et al., Brain death: practicability of evoked potentials BAEP .......
253
z
,o.e,.r
0.07 uv
0.07 ~JV
10 ms
10 m s
Figure 5. 64 year old patient with a supratentorial haematoma, wide responseless pupils, loss of corneal reflex, and preserved cough reflex. Wave I of the BAEP is preserved bilaterally.
It may be argued that two sequential recordings are not necessary when wave I is preserved bilaterally, since this proves the preservation of intact peripheral receptors. This phenomenon was encountered in three out of 63 patients after the apnea test (5%) which is near the findings reported by others [6, 18, 25]. Thus, the acceptance o f a bilaterally preserved wave I during a single recording as of equal value as the stepwise abolition of wave Ill to V in sequential recordings only increases the number of cases in which BAEP are relevant for the declaration of brain death. Since preserved spontaneous respiration has been reported in a patient with abolition of BAER the value of BAEP as a confirmatory test in brain death has been questioned [4]. A comparable observation was encountered in this series in a 64 year old male with a preserved bilateral wave I concurrent with a preserved cough reflex (Figure 5), thus indicating a strictly confined local and not generalized lesion of the brain stem. Similarly, isoelectric EEG's concurrent with preserved spontaneous respiration [11] underscore the non-reversible sequence of investigations: confirmatory tests are only valid after the apnea test, which should be performed after coma and cranial nerve areflexia have been established. To our knowledge there has been no report of a patients with a
stepwise abolition of waves III to V or preserved bilateral wave I only after apnoic brain stem areflexia due to a primary supratentorial brain lesion in whom the confirmatory value of BAEP appeared doubtful. Recovery of lost BAEP has only been reported in patients with a secondary brain lesion [17].
5 Conclusion While SEP and VEP appear to be of limited value for the diagnosis of brain death, the stepwise abolition of BAEP in sequential recordings seems to be a valuable confirmatory test in patients with supratentorial brain lesions. So far there have been no serious challenges to this concept. BAEP proved to be of practical value in 31% of patients developing brain death. Its particular resistance to drug effects adds to the safety of the diagnosis. Registration of BAEP appears more practicable for those intensive care units, in which evoked potentials are regularly monitored in comatose patients.
Acknowledgements: This study was supported in part by a grant from the "Kuratorium ffir Heimdialyse', and in part by grant Fi 390/2-1-857/88 by the "Deutsche Forschungsgemeinschaft'.
References [1] ANZISKABJ, RQ CRACCO:Short latency somatosensory evoked potentials in brain dead patients. Arch Neurol 37 (1980) 222-225 [2] ARFELG: Stimulations visuelles et silence c6r6bral. Electroenceph clin Neurophysiol 23 (1967) 172175 Neurosurg. Rev. 15 (1992)
[3] BELSHJM, S CHOKROVERTY;Short latency somatosensory evoked potentials in brain-dead patients. Electroenceph clin Neurophysiol 68 (1987) 75-78 [4] BINIEKR, A FERBERT,H BUCHNER,H BRUCKMANN: Loss of brainstem acoustic evoked potentials with spontaneous breathing in a patient with supratentorial lesion. Eur Neurol 30 (1990) 38-41
254
Firsching et al., Brain death: practicability of evoked potentials
[5] BRUNKOE, D ZEGERSDE BEYL:Prognostic value of early cortical somatosensory evoked potentials after resuscitation from cardiac arrest. Electroenceph clin Neurophysiol 66 (1987) 1 5 - 2 4 [6] DESBORDESJM, C KRt~MER,M MESZ, B DEGLAIRE, F MAISSIN, B BATAILLE,A MARILLAUD:Potentials 6voqu6s auditifs du tronc c6r6bral dans la mort c6r6brale. Ann Fr Anesth R6anim 7 (1988) 13--16 [7] FERBERTA, H BUCHNER,E RINGELSTEIN,W HACKE: Isolated brain-stem death. Case report with demonstration of preserved visual evoked potentials (VEPs). Electroenceph clin Neurophysiol 65 (1986) 157-160 [8] F1RSCHINOR: The brain-stem and 40 Hz middle latency auditory evoked potentials in brain death. Acta Nearochir 101 (1989) 52--55 [9] FIRSCmNGR: Evoked potentials in head injury. In: Advances in Neurotraumatology. RP Vigouroux, RA Frowein (eds) Springer Wien New York 1991 [10] FIRSCmNGR, RA FROWEIN:Multimodality evoked potentials and early prognosis in comatose patients. Neurosurg Rev 13 (1990) 141--146 [11] FROWEIN RA, H G~NSHIRT, KE RICHARD, E HAraE5, WF HAUPT: Kriterien des Hirntodes: 3. Generation. Anfisth Intensivther Notfallmed 22 (1987) 1 7 - 2 0 [12] GANEST, P NAKSTAD:Subcomponents of the cervical evoked response in patients with intracerebral circulatory arrest. J Neurol Neurosurg Psych 47 (1984) 292-297 [13] GOLDIEWD, KH CHIAPPA,RR YOUNG,E BROOKS: Brainstem auditory and short-latency somatosensory evoked responses in brain death. Neurol 31 (1981) 248-256 [14] GUERIT JM, P MAHIEU: Are evoked potentials a valuable tool for the diagnosis of brain death? Transplantation Proceedings Vol XVIII 3, Grune & Stratton Inc (1986) 386-387 [15] HALLJW, J MACKEY-HARGADINE,E KIM: Auditory brain-stem response in determination of brain death. Arch Otolaryngol 111 (1985) 613 - 620 [16] PFURTSCHELLERG, G SCHWAZ,W LIST:Brain death and bioelectrical brain activity. Intens Care Med 11 (1985) 149-153
[17] ROSSINIP, R KULA, W HOUSE, R CRACCO: Alteration of brainstem auditory evoked responses following cardiorespiratory arrest and resuscitation. Electroenceph din Neurophysiol 54 (1982) 232-234 [18] SHIOGAIT: Evaluation of eleetrophysiological neuromonitoring in the diagnosis of brain death. NoTo-Shinkei 41 (1989) 7 3 - 8 3 [19] STARRA: Auditory brain-stem responses in brain death. Brain 90 (1976) 543-554 [20] STOHRM, B RIFFEL,E TROST,P WENGERT:Bedeutung der somatosensibel evozierten Potentiale (SEP) bei der Feststellung des Hirntodes. Anaesth Intensivther Notfallmed 22 (1987) 2 1 - 2 5 [21] STOHRM, E TROST,A ULLRICH,B RIFFEL,P WENGERT: Bedeutung der ffiihen akustisch evozierten Potentiale bei der Feststellung des Hirntodes. Dtsch reed Wschr 111 (1986) 1515-1519 [22] TROJABORG,W, E JORGENSEN:Evoked cortical potentials in patients with 'isoelectric' EEG. Electroenceph clin Neurophysiol 35 (1973) 3 0 1 - 309 [23] WILKUD R, G CHATRIAN,E LETTICH:The electroretinogram during terminal anoxia in humans. Electroenceph clin Neurophysiol 31 (1971) 537-546 [24] Wissenschaftlicher Beirat der Bundesfirztekammer: Kriterien des Hirntodes. Entscheidungshilfen zur Feststellung des Hirntodes. Dtsch ~rztebl 83 (1986) 2940- 2946 [25] YOKOYAMAT, K UEMURA,H RYU, T MIYAMOTO,K SUGIYAMA,T TOKUYAMA,A SHIRASAKA:The findings of auditory and somatosensory evoked potenrials in brain death confirmed by the apnea test. To-To-Shinkei 40 (1988) 561--567 [26] ZmERS DE BEYL D, E BRUNKO: Prediction of chronic vegetative state with somatosensory evoked potentials. Neurol 36 (1986) 134 Submitted April 17, 1991. Accepted June 18, 1991. Priv.-Doz. Dr. Raimund Firsching Klinik ffir Neurochirurgie Ruhr-Universitiit Am Knappschaftskrankenhaus In der Schornau 2 3 - 2 5 W-4630 Bochum 7 Fed. Rep. of Germany
Neurosurg. Rev. 15 (1992)
15 (1992) 249-254
Brain death: practicability o f evoked potentials Raimund Firsching, Reinhold A. Frowein, Stefan Wilhelms, and Friedrich Buchholz Neurosurgical Clinic, University o f Cologne, Fed. Rep. o f G e r m a n y
Abstract
2 Patients and methods
Multimodally evoked potentials were registered in 85 patients who fulfilled the criteria for brain death. While somatosensory and visual evoked potentials have been found to be of limited value for the diagnosis of brain death, the stepwise abolition of brain stem auditory evoked potentials (BAEP) confirmed brain death in 26 out of 85 patients, i.e. 31%. Registration of the abolition of BAEP is concluded to be a safe and acceptable confirmatory test. It is, however, more feasible for institutions, in which BAEP are analysed routinely. In spite of all efforts sequential BAEP could not be used for the diagnosis of brain death in the majority of cases either because of absence of reproducible responses at the initial registration or because the patient was already apnoic at the time of the initial BAER Assuming that bilateral preservation of wave I has the same significance as the stepwise abolition of BAEP, since it also proves the integrity of the peripheral receptor, BAEP are relevant for the declaration of brain death in approximately 30% of patients.
In a prospective study somatosensory (SEP), visual (VEP), and brain stem a u d i t o r y (BAEP) evoked potentials were recorded in 265 comatose patients in a neurosurgical intensive care unit within 48 hours of admittance or onset o f coma. O f these, 85 patients reached the level o f apnoic brain stem areflexia and met the criteria o f brain death as r e c o m m e n d e d by the "Wissenschaftlicher Beirat, Bundes/irztekammer" (1986). N o patient was hypothermic or had received barbiturates. Causes o f c o m a are listed in table I. Eight patients h a d a p r i m a r y infratentorial lesion.
Keywords: Brain death, evoked potentials. 1 Introduction The recording o f evoked potentials in brain death is getting increasing attention [1, 3, 1 2 - 1 6 , 1 9 22]. The stepwise abolition o f brain stem a u d i t o r y evoked potentials (BAEP) in p r i m a r y supratentorial brain lesions has been suggested as one of four equally relevant alternative tests to confirm the irreversibility o f the loss of brain function after a p r i m a r y supratentorial lesion. The other three tests are a 12 hour waiting period with repeated confirmation of apnoic cranial nerve areflexia, an isoelectric E E G , and cerebral circulatory arrest as d e m o n s t r a t e d by a n g i o g r a p h y [24]. This report is an account o f our practical experience with evoked potentials from patients a p p r o a c h i n g brain death. 9
1992 by Walter de Gruyter & Co. Berlin - New York
Table I. Causes of coma Number of patients Head injury Subarachnoid hemorrhage Intracerebral haematoma Tumor Others
41 18 15 6 5
Total
85
The apnea test was performed in each o f the 85 patients and was carried out when c o m a and complete loss o f cranial nerve reflexes were noted:, W i t h intratracheal administration o f oxygen, ap2 nea was assumed when no breathing was noted inspite o f significantly increased paCO2 b l o o d gas levels after an interval of 10 to 20 min. As d o c u m e n t a t i o n o f the stepwise abolition of B A E P requires a m i n i m u m o f two recordings, it was tried to obtain recordings o f SEP, VEP and
250
Firsching et al., Brain death: practicability of evoked potentials
B A E P prior to and after the apnea test. This was not possible in all 85 patients, mostly because o f intermittent cardiovascular failure or apnea at the time of, or shortly after, admittance. The timing o f the recordings o f evoked potentials is listed in table II. Technical details of the recording o f evoked potentials as used in this study are listed in table III ]9, 10]. Table II. Timing of recording of evoked potentials
Number of patients BAEP
SEP and VEP
22 62 48
18 57 46
m a r y absence o f the N20 c o m p o n e n t p r i o r to the apnea test was noted in 41 patients o f 75 patients (55%) investigated. The cervical response was preserved in 11 out o f 18 patients, i.e. 61% p r i o r to the apnea test but after the onset o f c o m a a n d cranial nerve areflexia. After the apnea test the cervical response was reproducible in 28 of 57 patients, i.e. 49%. In patients with infratentorial lesions after the apnea test the cervical responses was preserved in 50%. The response at the cervical plexus, (Erb's point) was preserved in all patients at all times.
3.2 V E P
Before apnea test only After apnea test Before and after apnea
Table III. Technical standards for the registration of evoked potentials
SEP Stimulus: Bandpass: Analysis time: Montage: VEP Stimulus: Bandpass: Analysis time: Montage: BAEP Stimulus:
Bandpass: Analysis time: Montage:
2 x 512 200 Ixs < 20 mA at 5.4 Hz stimulations of median nerve at wrist LF : HF 30 : 3000 Hz 30 ms 1. Erb's point-Fz, 2. Neck at C2-Fz, 3. Contralateral scalp (C3/C4)-Fz
VEP were absent in all cases except one in w h o m c o m a and cranial nerve areflexia were noted, b o t h before and after the apnea test. In five patients VEP were absent before the apnea test, at a time when the E E G did not show electrocerebral silence (ECS). There was one exceptional, but n o t unexpected observation in a case with a posterior fossa haemorrhage: b o t h a nearly n o r m a l E E G , and reproducible VEP were recorded after apnea h a d been d o c u m e n t e d (Figure 1). In six patients the amplitude o f the electroretinogram seemed to increase after the apnea test (Figure 2). 3.3 B A E P
2 • 256 unilateral flashes at 1.7 Hz L F : H F 1 : 100Hz 250 or 300 ms 1. ipsilateral lateral eyelid-Cz, 2. Oz-Cz
2 • 1024 unilateral alternating rarefaction/condensation 200 gs clicks delivered at 11.1 Hz with 95 dB and 65 dB contralateral white noise masking LF : HF 150 : 3000 Hz 10 ms ipsilateral ear lobe-Cz
3 Results 3.1 S E P
The cortical N20 c o m p o n e n t was absent in all 46 patients investigated after the apnea test. The stepwise abolition o f the N20 component, which required an intact N20 at the initial recording before the apnea test, was observed in 23 patients. Pri-
The first registration of B A E P in 85 patients, who h a d exhibited apnoic brain stem areflexia, demonstrated the complete bilateral loss o f waves I I I to V in 49 patients. 36 patients h a d a bilateral wave III or later c o m p o n e n t s o f the B A E P (Figure 3). A bilateral wave I was found in three cases at the initial registration, one before and two after the apnea test. The stepwise bilateral abolition o f waves I I I to V after the apnea test was observed in 34 patients. Since 8 o f these patients h a d an infratentorial lesion, abolition o f B A E P was relevant to the declaration o f brain death in 26 patients. B A E P findings after the apnea test (Figure 4) d e m o n s t r a t e d a complete loss o f all c o m p o n e n t s in 82% of cases. A unilateral wave I was seen in 11%, and three patients d e m o n s t r a t e d a bilateral wave I, and one o f these h a d an additional unilateral wave II. In cases with infratentorial lesions seven out of eight patients exhibited no wave after the apnea test, one patient h a d a bilaterally preserved wave I. Neurosurg. Rev. 15 (1992)
Firsching et al., Brain death: practicability of evoked potentials
251
VEP
M.E. 1652/90 59 y. female Posterior fossa haemorrhage
after brainstem areflexia and apnea .
.,~.~
left eye
,
~.~ right eye
300 ms
/
300 ms
Figure 1. Preserved VEP after apnoic brain stem areflexia in a patient with an infratentorial lesion.
S.B. 185/89 56 y. male Subaraehnoid haemorrhage Clouding o! consciousness
VEP
left eye
right eye
Cz-Oz 5
f
~
~
Eiectroretinogram ~
, i . . . . . .
[2.4pV
Electroretinogram
I i i t,,
250 ms
J,,,
t[2.4pV
250 ms
Apnoic brainstem areflexia left eye ~~-..
~ .............
-
right eye
-~'~-.-...... C~-O= /\, /,'.,:\
U' \l
......J~"~ f~ "t, Electroretmogram L ',
)
,,,
~,,,,,
/ ~f
,[3.05pV 250 ms
x~.~.k.&_r~_ 7 Electroretinogram r
250 ms
Figure 2. While the cortical response is abolished after onset of apnoic brain stem areflexia, the amplitude of the electroretinogram appears to have increased.
4 Discussion
In most of the increasing number of studies dealing with evoked potentials in brain death either the exact timing of the investigation as related to the apnea test is not specified or only single investigations are performed instead of sequential recordings giving evidence of the stepwise abolition Neurosurg. Rev. 15 (1992)
of evoked potentials. Registration of evoked potentials, however, is only of confirmatory value for the diagnosis of brain death after the apnea test. Sequential recordings giving evidence of the stepwise abolition of evoked potentials have been considered mandatory to make sure, the peripheral receptors had been intact [24].
252
Firsching et al., Brain death: practicability of evoked potentials BAEP findings at initial registration of patients developing brain death.
BAEP findings after the apnea test
Number 50 of patients 4O
100
%
82%
Percentage of patienls
30 50 20 10-
no wave
[--] I--1 unilateral bilateral wave[ waveI
I~ uni- or bilateral wave~
11% ~ bilateral wave Tif toy
Figure 3. Approximately half of all patients developing brain death had bilateral reproducible waves III to V at the initial investigation.
4.1 SEP The stepwise abolition of cervical and cortical SEP during the onset of brain death may indicate the loss of function of the cervical cord and brain stem. As only a cephalic reference was used in this series, the distinction of a cervical and a lower brain stem response within the cervical N13 component [20] was not possible. We found, as did other authors [1, 3, 12, 13] with a cephalic reference only, that 52% of the cases had no cervical responses after the apnea test. Absence of cortical SEP does not have the same significance as an isoelectric EEG, as absence of SEP is frequently observed in patients with nonisoelectric EEGs, and survival without cortical SEP in patients without concurrent spinal injuries has been repeatedly observed [5, 9]. Furthermore, reappearance of lost SEP has been reported [26]. Since 55% of all patients investigated before and after the apnea test had no cortical SEP at the initial registration and 11 patients were not amenable to registration of evoked potentials until after the apnea test, the stepwise abolition could only be documented in 31%, i.e., 23 out of 75 patients. Thus, its value for the determination of brain death remains controversial.
4.2 VEP Preservation of an active electroretinogram (ERG) in brain death has been reported for over 20 years [2, 23]. The increased amplitude of the E R G at brain death in some cases in this series is difficult
no wave
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1.5%
1.5%
unilateral bilateral unilateral bilateral waveI waveE wave]s wave][
Figure 4. Bilateral wave I after the onset of apnoic brain stem areflexia was noted in 4% of cases.
to explain, it may possibly be due to variable impedances in spite of efforts to keep them at steady levels of less than 5 kohm. Preservation of VEP in apnoic patients with brain stem areflexia has been described before [7], but remains a rare finding. It confirms the need for a test of supratentorial cerebral functions in apnoic brain stem areflexia after primary infratentorial lesions. VEP and EEG findings do not always coinciCe. In this series the absence of VEP was encountered with non-isoelectric EEGs in several instances. In one exceptional case, concussion of the chiasm was considered the probable cause. We have, however, not yet encountered an isoelectric EEG accompanied by a preserved VEP. The value of VEP for the determination of brain death thus also appears limited.
4.3 BAEP The registration of the stepwise abolition of BAEP has been suggested as a test for the confirmation of the irreversibility of the loss of brain function after supratentorial lesions [24]. At least two sequential recordings are recommended, the first giving evidence of a bilaterally preserved wave III to ensure the function of the peripheral receptor. Stepwise abolition was observed in 26 out of 85 patients, i.e. 31%, who developed brain death. In practice it is not always easy to distinguish individual components in abnormal BAEP, in some cases additional recording of middle latency auditory evoked potentials may be helpful [8]. Neurosurg. Rev. 15 (1992)
Firsching et al., Brain death: practicability of evoked potentials BAEP .......
253
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0.07 ~JV
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10 m s
Figure 5. 64 year old patient with a supratentorial haematoma, wide responseless pupils, loss of corneal reflex, and preserved cough reflex. Wave I of the BAEP is preserved bilaterally.
It may be argued that two sequential recordings are not necessary when wave I is preserved bilaterally, since this proves the preservation of intact peripheral receptors. This phenomenon was encountered in three out of 63 patients after the apnea test (5%) which is near the findings reported by others [6, 18, 25]. Thus, the acceptance o f a bilaterally preserved wave I during a single recording as of equal value as the stepwise abolition of wave Ill to V in sequential recordings only increases the number of cases in which BAEP are relevant for the declaration of brain death. Since preserved spontaneous respiration has been reported in a patient with abolition of BAER the value of BAEP as a confirmatory test in brain death has been questioned [4]. A comparable observation was encountered in this series in a 64 year old male with a preserved bilateral wave I concurrent with a preserved cough reflex (Figure 5), thus indicating a strictly confined local and not generalized lesion of the brain stem. Similarly, isoelectric EEG's concurrent with preserved spontaneous respiration [11] underscore the non-reversible sequence of investigations: confirmatory tests are only valid after the apnea test, which should be performed after coma and cranial nerve areflexia have been established. To our knowledge there has been no report of a patients with a
stepwise abolition of waves III to V or preserved bilateral wave I only after apnoic brain stem areflexia due to a primary supratentorial brain lesion in whom the confirmatory value of BAEP appeared doubtful. Recovery of lost BAEP has only been reported in patients with a secondary brain lesion [17].
5 Conclusion While SEP and VEP appear to be of limited value for the diagnosis of brain death, the stepwise abolition of BAEP in sequential recordings seems to be a valuable confirmatory test in patients with supratentorial brain lesions. So far there have been no serious challenges to this concept. BAEP proved to be of practical value in 31% of patients developing brain death. Its particular resistance to drug effects adds to the safety of the diagnosis. Registration of BAEP appears more practicable for those intensive care units, in which evoked potentials are regularly monitored in comatose patients.
Acknowledgements: This study was supported in part by a grant from the "Kuratorium ffir Heimdialyse', and in part by grant Fi 390/2-1-857/88 by the "Deutsche Forschungsgemeinschaft'.
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Neurosurg. Rev. 15 (1992)
