I:le¢ troem ephah)grapl(l al~d, lttm at X,europto,stolog~', 1991, 78: 228- 233 ' 199t Elsevier Scientific Publisher~ Ireland, Ltd. 0013-4649/91/$03.50 A DONI.'~" 001346499100073U
228
EEG 90037
A comparison between electroencephalography and somatosensory evoked potentials for outcome prediction following severe head injury D.O. Hutchinson, R.W. Frith, N.A. Shaw, J.A. Judson and B.R. Cant Departments of Clinical Neurophysiolog}, and Crittcal (_'are Medwine, Auckland Ito~plla[, 4 uckland
(New Zealand)
(Accepted for publication: 6 July 1990)
Summa O' The value of somatosensory evoked potentials (SEPs) for the prediction of outcome following aevere head injury 0tl) is established. The role of the electroencephalogram (EEG) in this setting is uncertain. In this comparative study. SEPs and EEGs were recorded within 3 days of severe HI in 90 patients, and the results related to outcome at 6 inonths. Patients with an isoelectric EEG or an EEG with repeated isoelectric intervals died. Reactivity ol the Et:G to external stimulation tended to be associated with favorable outcome, Grading of the EEGs on the basis of frequency composition otherwise provided no prognostic information. The presence of SEP scalp potentials bilaterally predicted favorable outcome, particularly if the central conduction times were normal. Conversely, the absence of one or both scalp potentials was associated with unfavorable outcome. EEGs thus provided useful prognostic information in only a minority of patients, By comparison. SEPs allowed prediction of both favorable and unfavorable outcomes in a much larger number of patients, and were therefore prognostically superior Key words: Head injury; Prognosis; Outcome prediction; Electroencephalography; Somatosensory evoked potentials
The m a n a g e m e n t of patients with severe head injury (HI) is labor-intensive and expensive. A n accurate method of predicting the outcome in individual patients with severe HI would be valuable. The ideal method would provide reliable prognostic i n f o r m a t i o n as early as possible. Most of the established methods of neurological assessment after HI have limitations with regard to outcome prediction. The Glasgow C o m a Scale ( G C S ; Teasdale and J e n n e t t 1974) has some value ( N a r a y a n et al. 1981; Marshall a n d Bowers 1985), but is affected by variables such as alcohol intoxication and hypoxemia, a n d becomes impossible to o b t a i n in sedated and paralysed patients. C o m p u t e d t o m o g r a p h y (CT) of the head can predict favorable ( N a r a y a n et al. 1981) and unfavorable (Marshall and Bowers 1985) outcomes in a small percentage of cases. C T may, however, be falsely pessimistic in a significant p r o p o r t i o n of patients ( N a r a y a n et al. 1981). l n t r a c r a n i a l pressure m o n i t o r i n g can identify a subset of patients likely to die (Marshall and Bowers 1985), but otherwise provides only limited prognostic information, and is not available in m a n y centers.
Correspondence to: Dr. R.W. Frith, Department of Clinical Neurophysiology, Auckland Hospital, Park Road, Auckland 1 (New Zealand).
Recent studies ha~e shown that evoked potentials can provide prognostic i n f o r m a t i o n following HI ( G r e e n b e r g et al. 198t; G r e e n b e r g a n d Ducker 1982: C h i a p p a t983; S p e h l m a n n 1985). F u r t h e r m o r e , work from this unit ( H u m e et al. 1979; H u m e a n d C a n t 1981: C a n t et al. 1986; Shaw 1986: C h a n c e l l o r el al. 1988: Judson et al. 1990) and from others ( G r e e n b e r g et aL 1977; De la Torre et al. 1978; Lindsay et al. 1981: Lutschg et al. 1983: R u m p l et al. 1983; A n d e r s o n et al. 1984; De Weerd and G r o e n e v e l d 1985) has shown that of the various types routinely recorded, somatosensory evoked potentials (SEPs) following m e d i a n nerve stimulation are the most useful a n d are capable of predicting both favorable and u n f a v o r a b l e outcomes. Electroencephalographic ( E E G ) changes occur following HI (Courjon and Scherzer 1972). In theory, the degree of change might relate to HI severity, a n d hence outcome. The ability of EEG to predict o u t c o m e is, however, uncertain. Bricolo (1976) divided post-H1 EEGs into 5 groups, each associated with a different likelihood of fatal outcome. Using this system, the p r o p o r t i o n of patient> dying ranged from 13~( in those with a diphasic E E G with spindles, to 100~ if the E E G was isoelectric. Bergamasco et al. (1968) reported a correlation between 1-1-.'G sleep patterns, or circadian changes, with s u b s e q u e n t recovery following HI. This study examined a small group of patients a n d involved prohmged polygraphic recordings. G a n e s and L u n d a r
EEG AND SEPs FOLLOWING SEVERE HEAD INJURY (1988) found no relation between non-isoelectric EEG patterns and outcome following HI, although grading of the recordings was not performed. Rodin (1967) was unable to find any features of non-isoelectric EEGs which distinguished early from late death in 42 patients with HI. The relative prognostic values of EEG and SEP recordings in post-traumatic coma have yet to be determined. In this study we compared the predictive values of these recordings following severe HI.
229 TABLE I EEG grading criteria. A. H o c k a d a y system
la Alpha rhythm. 2a Predominanttheta with rare alpha. 3a Delta mixed with theta and rare alpha. 4a Diffusedelta with brief isoelectric intervals. 5a A nearly flat record.
lb Predominantalpha with rare theta. 2b Predominant theta with some delta. 3b Predominant delta and no other activity. 4b Scattered delta in some leads only. 5b No EEG at all.
B. Prior system
Methods and materials
The study was carried out over a 3 year period on 100 patients admitted with severe HI to the Auckland Hospital Department of Critical Care Medicine. This department provides a centralized service for severe HI for a population of approximately one million people. The patients were part of another study examining the role of SEPs following HI (Judson et al. 1990). Inclusion criteria included (a) HI the result of blunt trauma, (b) lack of pre-existing brain disease, and (c) initial GCS less than or equal to 8. The GCS was recorded immediately prior to sedation/intubation, or at 6 h if intensive care was delayed. We excluded patients who died for reasons unrelated to their HI. All patients were intubated and hyperventilated (Judson et al. 1990); sedation and neuromuscular blockade were used to produce a state of narcosis and reflex suppression resembling neuroanesthesia. The agents used were papaveretum by infusion (usually 5-10 rag/h), diazepam intermittently i.v. (usually 5-10 mg, 6 hourly) and pancuronium by infusion (usually 4 m g / h ) . Patients with clinical seizures received diphenylhydantoin (20 m g / k g load, then 6 m g / k g / d a y ) . Phenobarbital was not used. CT head scans were performed, and neurosurgery carried out when indicated. EEG and SEPs were performed within 3 days of HI. This was within 24 h of HI in 59 patients, between 24 and 48 h in 26, and between 48 and 72 h in 5. Both tests were performed within 8 h of each other. In patients who had recordings performed more than once, the earliest set was chosen for analysis. We excluded 10 patients from analysis, either because an EEG was not performed, or because the EEG was not available for review. The EEGs were recorded on an 8-channel Mingograf machine (Siemens-Elema), using subdermal platinum alloy electrodes placed according to the international 10-20 system. The gain was 50 or 70 /~V/cm, except with apparently isoelectric traces, where 20/~V/cm was used. Reactivity of the EEG was tested by (a) shouting the patient's name, and (b) applying painful stimuli to each hand in turn. The SEP recordings were made with a TN-3000 evoked response analyzer, using methods we
1 Alpha rhythm dominant. 2 Theta activitydominant; rare alpha waves, or delta activity dominant with plentiful other activity present. 3 Continuousdelta activity dominant with little other activity, or continuous spike activity, or episodic reduction in voltageor complete isoelectric periods of less than 1 sec duration. 4 Isoelectricintervals of 1 sec or more duration separated by any type of activity and not initiated or reversed by stimuli or scattered delta activity in some leads with flat traces in others or an almost isoelectric tracing. Absence of response to stimulation. 5 Isoelectrictracing. No recognizablecerebral activity and absence of response to stimulation.
have previously described (Chancellor et al. 1988). In brief, neck and scalp potentials were recorded simultaneously following unilateral stimulation of the left and right median nerves. Two of the authors graded the EEGs by consensus, blinded to patient outcome. In the absence of an accepted system of EEG grading in post-traumatic coma, the scales of Prior (1973) and Hockaday et al. (1965) were used (Table I). Although neither was designed specifically for use in post-traumatic coma, both have been used in post-anoxic coma. The Hockaday scale has twice as many grades as the Prior system, but they are otherwise similar and involve principally an assessment of the frequency composition of the EEG. Drug-induced beta activity was disregarded for grading purposes. If there was left-right asymmetry, the worse side was graded. Any change in the cerebral activity following external stimulation (reactivity) was noted. The SEPs were graded on a 3-point scale in blind fashion by one of the authors, using (a) the presence or absence of a scalp recorded N20 potential and (b) the central conduction time (CCT), defined as the interpeak latency between cervical and scalp potentials. SEPs were grade 1 if the CCTs were normal bilaterally, grade 2 if one or both CCTs (or the left-right difference) were beyond the upper limits of normal, and grade 3 if one or both scalp potentials were absent. The upper limit of normal for CCT was 3 S.D.s above the age-related mean for this laboratory (i.e., normal is less than 7.0 msec for subjects under 50 years, and less than 7.3 msec for those
230
D.O. H U T C H I N S O N ET AL.
50 or more years) (Hume et al. 1982). We did not consider scalp potential amplitudes in the grading, as it is our experience that these show wide inter-individual variability. One of the authors reviewed the surviving patients at 6 months and categorized their outcomes using a modification of the criteria of Jennett and Bond (1975), into good outcome, moderate disability, severe disability, and death. G o o d outcome and moderate disability were considered favorable outcomes, and severe disability and death were considered unfavorable (Karnaze et al. 1982).
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There were 90 patients (median age 21 years, range 10-70) of whom 65 were male. The majority (73 patients) had HI due to road traffic accidents. Ages, GCSs and number of days ventilated are shown in relation to outcome in Table II. The indications for neurosurgery were extradural hematoma (6 patients), hemorrhagic contusion or intracerebral hematoma (6), subdural hematoma (4), and elevation of skull fracture (2). At 6 months, 27 patients had good outcome, 22 moderate disability, 8 severe disability, and 33 had died. In the last group, death occurred a median of 3 days (range 1-73) after HI. Fig. 1 shows the EEG grades (Hockaday system) in relation to outcome. Ten patients had severely abnormal (grades 4 a - 5 b ) EEGs, and all died. Three patients had EEGs which were grade l b or 2a (no delta activity); all survived but were left with moderate (2) or severe (1) disability. The remaining EEGs, comprising 86% of the total, fell into a limited number of grades (2b, 3a and 3b). Similar results were obtained when the Prior EEG grades were related to outcome (Fig. 2). All of the patients with a severely abnormal EEG (grade 4 or 5) died. All but one of the remaining EEGs (i.e., 88% of the total) were graded as 2 or 3, and similar outcomes were seen in these two patient sets.
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231
with severe disability and the other survived in a vegetative state. Fig. 4 compares the abilities of the EEGs and SEPs to predict favorable outcome. In order to achieve adequate numbers in each set, EEG grades 1 and 2, and grades 4 and 5, were combined. For both the Hockaday and Prior systems, the probability of favorable outcome with a grade 1 or 2 E E G was slightly greater than 0.5, while the probability of favorable outcome with a grade 3 E E G was paradoxically slightly greater. By contrast, the probabilities of favorable outcome were clearly different for each of the SEP grades, with an association between increasing grade and worse outcome.
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Fig. 3. Patient outcome in relation to SEP ~ a d e .
good outcome, 4 moderate disability) and 2 had unfavorable outcome (1 severe disability, 1 death). The EEGs of 5 patients contained epileptiform activity. This consisted of frontal sharp waves or spikes, which were unilateral in 3 patients and bilateral in 2. Four had favorable outcome (1 good outcome, 3 moderate disability), and 1 died. SEP grades in relation to outcome are shown in Fig. 3. Of those with grade 1 (normal) SEPs, 90% had favorable outcome. With grade 2 SEPs, 69% had favorable outcome and with grade 3 SEPs, 6% had favorable outcome. There was a very strong association between SEP grade and outcome (X 2 = 46.77, P < 0.001). Of the patients with grade 3 SEPs, 8 had unilateral, and 23 had bilateral absence of scalp potentials. Of the 5 patients who survived with grade 3 SEPs, 3 had absence of only one scalp potential, and 2 had bilaterally absent scalp potentials. Of the latter, one was left
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Discussion
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Fig. 4. Probability of favorable outcome, with 95% confidence limits, for the EEG and SEP grades. Note the amalgamation of E E G grades 1 and 2 and 4 and 5.
The present study compared the prognostic values of single EEG and SEP recordings in a group of patients with severe HI. There were no clear relationships between most of the Hockaday and Prior EEG grades and outcome. The exception was the isoelectric or very severely abnormal EEG, which was highly predictive of fatal outcome. This association was expected, as the isoelectric EEG is an accepted indicator of brain death (Dawson et al. 1951; Rodin et al. 1965) provided drug effects and hypothermia are excluded. There was a strong tendency, using both grading systems, for the EEGs to fall into a small number of categories. This clustering provided some explanation for the inability of non-isoelectric EEGs to predict outcome. The most likely cause of this is insensitivity of the investigation for assessing HI severity. Another possible explanation is inadequacy of the currently available EEG grading systems, particularly their failure to consider EEG reactivity. There was a significant association between reactivity of the L E G to external stimulation and outcome, with the presence of reactivity tending to predict favorable outcome. We are not aware that this has previously been shown. The observation probably reflects the association between EEG reactivity and relatively light coma (Arfel 1975). Sleep transients, found in a proportion of the EEGs, also predicted favorable outcome, although the numbers were small. Previous authors have associated sleep-like EEG activity with survival following HI, although none have specified residual neurologic disability (Chatrian et al. 1963; Bergamasco et al. 1968; Bricolo 1976). SEPs predicted both favorable and unfavorable outcomes considerably better than the EEG. The presence on both sides of a scalp potential following median nerve stimulation was associated with favorable outcome, regardless of the CCT. The association with favorable outcome was greater, however, for patients in whom the CCTs were both normal. Conversely, the
232
absence of one or both scalp potentials was associated with death or unfavorable outcome, and death resulted in almost all patients in whom both scalp potentials were absent. Thus, normal and severely abnormal SEPs correlated strongly with favorable and unfavorable outcomes respectively. Of note, 69% of those with CCT prolongation as the sole SEP abnormality (grade 2) had favorable outcome, This differs from previous reports (Hume et al. 1979; Lutschg et al. 1983; Rumpl et al. 1983) which have stressed the association between prolonged CCT and unfavorable outcome. The prognostic superiority of SEPs over EEG may be due to a number of reasons: (1) Many factors, not all necessarily affecting outcome, influence the EEG more than the SEP. These, which are common in HI patients, include damage to the skull or scalp, toxic and metabolic disorders, seizures and depth of coma. Medications used in the treatment of HI patients also have a marked effect on the EEG (Bauer 1987) but probably have little influence on SEPs or CCT (Cant and Shaw 1986). (2) The optimal time to record post-HI EEGs has not been established. Some have reported an increased yield of abnormalities early (within 30 min; Dow et al. 1944), while others have shown that significant changes may be delayed beyond 48 h (Dawson et al. 1951). Continuous monitoring has revealed the varying nature of the EEG following HI (Cant and Shaw 1984). SEP recordings, by contrast, show less variability with time and can provide prognostically useful information from an early stage (Judson et al. 1990). (3) EEG interpretation is less objective than SEP interpretation. Judging from the present set of results, it should be possible to construct a modified EEG grading system to incorporate additional factors such as reactivity and the presence of sleep transients. Any increase in predictive power would, however, be gained at the expense of a more complex grading process. A further limitation is that sleep activity appeared in a minority of EEGs, even of those patients who ultimately did well. Similarly, EEG reactivity correlated only weakly with outcome when compared with the SEP findings. For instance, of the patients who died, one-third had reactive EEGs. In contrast, all but one of those patients with a reactive EEG who died had abnormal SEPs. A reactive EEG therefore did not necessarily predict a normal SEP. In summary, we have shown that within the first 3 days following severe HI: (1) An EEG which is isoelectric, or nearly so, is strongly predictive of death (provided other causes of an isoelectric EEG are excluded). (2) Other EEG grades (Hockaday or Prior) have no correlation with outcome. (3) Reactivity of the EEG to external stimulation has a significant association with favorable outcome. (4) With SEPs, the presence of scalp potentials bilaterally correlates strongly with favorable outcome. This association is further strengthened if the CCTs are normal bilaterally. (5) The absence of one or
D.O. H U T C H I N S O N ET At..
both scalp potentials almost always predicts unfavorable outcome. (6) Overall, SEPs provide prognostic information which i.s superior to that obtained by the EEG when the scales of Hockaday or Prior are utilized alone. It is possible that if EEG analysis were to include such information as reactivity and the presence of sleep transients, the prognostic value may be improved.
References Anderson, D.C.. Bundlie, S. and Rockswold, G.L. Multimodalit~ evoked potentials in closed head trauma. Arch. Neurol., 1984, 41: 369-374. Arfel, G. Introduction to clinical and EEG studies in coma. In: R. Harner and R. Naquet (Eds.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 12. Elsevier, Amsterdam, 1975: 5--23. Bauer, G. EEG, drug effects, and central nervous system poisoning. In: E. Niedermeyer and F. Lopes da Silva (Eds,), Electroencephalography: Basic Principles, Clinical Applications. and Related Fields, 2nd Edn. Urban and Schwarzenberg, Baltimore, MD, 1987: 567-578. Bergamasco. B.. Bergammi. L.. Doriguzzi, T. and Fabiam. D. EEG sleep patterns as a prognostic criterion m post-traumatic coma. Electroenceph. clin. Neurophysiol.. 1968, 24: 374-377. Bricolo. A Electroencephalography in neurotraumatology. Clin. Electroenceph., 1976. 7: 184-197. ('ant. B.R. and Shaw. N.A. Monitoring by compressed spectral array in prolonged coma. Neurology, 1984. 34: 35-39. Cant. B.R. and Shaw. N.A. Central somatosensory conduction trine: method and clinical applications. In: R.Q. Cracco and I. BodisWollner (Eels.), Evoked Potentials. Alan R. Liss. New York. 1986: 58 -67. Cant, B.R.. Hume. A.L.. Judson, J.A. and Shaw. N.A. The assessment of severe head injury by short-latency somatosensory and brainstem auditory evoked potentials. Electroenceph. clin. Neurophysiol.. 1986. 65: 188-195. Chancellor, A.M.. Frith. R.W. and Shaw. N.A. Somatosensorv evoked potentials following severe head injury: loss of the thalamic potential with brain death. J. Neurol. Set 1988. 87: 255-263. ('hatrian. G.E.. White. LE. and Daly, D. Electroencephalographic patterns resembling those of sleep in certain comatose states after injuries to the head. Electroencepl7 clin. Neurophysiol., 1963. 15: 272-280. ('hiappa. K . H Evoked Potentials an Clinical Medicine. Raven Press. New York, 1983. ('ourjon, J. and Scherzer. t'.. Iraumat]c disorders: early EEG changes. In: J. Courjon (Ed.), Handbook of Electroencephalography and Clinical Neurophysiolog?,, Vol. 14B. Elsevier, Amsterdam, 1972: 8-18. Dawson, R.E., Webster, J ~,. and ~,iurdjian, E.S. Serial electroencephalography in acute head injuries. J. Neurosurg.. 1951, 8: 613-630. De let Torre, ,I.C., Trimble, LL., Beard, R.T., Hanlon, K. and Surgeon. J,W. Somatosensory evoked potentials for the prognosis of coma in humans. Exp. Neurol., 1978.60: 304-317. De Weerd, A.W. and Groeneveld, C. The use of evoked potentials in the management of patients with severe cerebral trauma. Acta Neurol. Scand., 1985, 72: 489-494. Dow, R.S., Ulett, G. and Raaf, J. Electroencephalographic studies immediately following head injury. Am. J. Psychiat., 1944, 101: 174-183.
EEG AND SEPs FOLLOWING SEVERE HEAD INJURY Ganes, T. and Lundar, T. EEG and evoked potentials in comatose patients with severe brain damage. Electroenceph. clin. Neurophysiol., 1988, 69: 6-13. Greenberg, R.P. and Ducker, T.B. Evoked potentials in the clinical neurosciences. J. Neurosurg., 1982, 56: 1-18. Greenberg, R.P., Becker, D.P., Miller, J.D. and Mayer, D.J. Evaluation of brain function in severe human head trauma with multimodality evoked potentials. Part 2. Localization of brain dysfunction and correlation with post-traumatic neurological conditions. J. Neurosurg., 1977, 47: 163-177. Greenberg, R.P., Newlon, P.G., Hyatt, M.S., Narayan, R.K. and Becker, D.P. Prognostic implications of early multimodality evoked potentials in severely head-injured patients. A prospective study. J. Neurosurg., 1981, 55: 227-236. Hockaday, J.M., Potts, F., Epstein, E., Bonazzi, A. and Schwab, R.S. Electroencephalographic changes in acute cerebral anoxia from cardiac or respiratory arrest. Electroenceph. clin. Neurophysiol., 1965, 18: 575-586. Hume, A.L. and Cant, B.R. Central somatosensory conduction after head injury. Ann. Neurol., 1981, 10: 411-419. Hume, A.L., Cant, B.R. and Shaw, N.A. Central somatosensory conduction time in comatose patients. Ann. Neurol., 1979, 5: 379-384. Hume, A.L., Cant, B.R., Shaw, N.A. and Cowan, J.C. Central somatosensory conduction time from 10 to 79 years. Electroenceph. clin. Neurophysiol., 1982, 54: 49-54. Jennett, B. and Bond, M. Assessment of outcome after severe brain damage: a practical scale. Lancet, 1975, i: 480-484. Judson, J.A., Cant, B.R. and Shaw, N.A. The early prediction of outcome from cerebral trauma by somatosensory evoked potentials. Crit. Care Med., 1990, 18: 363-368. Karnaze, D.S., Marshall, L.F., McCarthy, C.S., Klauber, M.R. and Bickford, R.G. Localizing and prognostic value of auditory evoked responses in coma after closed head injury. Neurology, 1982, 32: 299-302.
233 Lindsay, K.W, Carlin, J., Kennedy, I., Fry, J., Mclnnes, A. and Teasdale, G.M. Evoked potentials in severe head injury - analysis and relation to outcome. J. Neurol. Neurosurg. Psychiat., 1981, 44: 796-802. Lutschg, J., Pfenninger, J., Ludin, H.E and Vassella, F. Brain-stem auditory evoked potentials and early somatosensory evoked potentials in neurointensively treated comatose children. Am. J. Dis. Child., 1983, 137: 421-426. Marshall, L.F. and Bowers, S.A. Outcome prediction in severe head injury. In: R.H. Wilkins and S.S. Rengachary (Eds.), Neurosurgery, Vol. 2. McGraw-Hill, New York, 1985: 1605-1608. Narayan, R.K., Greenberg, R.P., Miller, J.D., Enas, G.G., Choi, S.C., Kishore, P.R.S., Selhorst, J.B., Lutz, H.A. and Becker, D.P. Improved confidence of outcome prediction in severe head injury. A comparative analysis of the clinical examination, multimodality evoked potentials, CT scanning and intracranial pressure. J. Neurosurg., 1981, 54: 751-762. Prior, P.F. The EEG in Acute Cerebral Anoxia. Excerpta Medica, Amsterdam, 1973: 43-46. Rodin, E.A. Contribution of the EEG to prognosis after head injury. Dis. Nerv. Syst., 1967, 28: 595-601. Rodin, E., Whelan, J., Taylor, R., Tomita, T., Grisell, J., Thomas, L.M. and Gurdjian, E.S. The electroencephalogram in acute fatal head injuries. J. Neurosurg., 1965, 23: 329-337. Rumpl, E., Prugger, M., Gerstenbrand, F., Hackl, J.M. and Pallua, A. Central somatosensory conduction time and short latency somatosensory evoked potentials in post-traumatic coma. Electroenceph, clin. Neurophysiol., 1983, 56: 583-596. Shaw, N.A. Somatosensory evoked potentials after head injury: the significance of the double peak. J. Neurol. Sci., 1986, 73: 145-153. Spehlmann, R. Evoked Potential Primer. Butterworth, Boston, MA, 1985. Teasdale, G. and Jennett, B. Assessment of coma and impaired consciousness: a practical scale. Lancet, 1974, ii: 81-84.
228
EEG 90037
A comparison between electroencephalography and somatosensory evoked potentials for outcome prediction following severe head injury D.O. Hutchinson, R.W. Frith, N.A. Shaw, J.A. Judson and B.R. Cant Departments of Clinical Neurophysiolog}, and Crittcal (_'are Medwine, Auckland Ito~plla[, 4 uckland
(New Zealand)
(Accepted for publication: 6 July 1990)
Summa O' The value of somatosensory evoked potentials (SEPs) for the prediction of outcome following aevere head injury 0tl) is established. The role of the electroencephalogram (EEG) in this setting is uncertain. In this comparative study. SEPs and EEGs were recorded within 3 days of severe HI in 90 patients, and the results related to outcome at 6 inonths. Patients with an isoelectric EEG or an EEG with repeated isoelectric intervals died. Reactivity ol the Et:G to external stimulation tended to be associated with favorable outcome, Grading of the EEGs on the basis of frequency composition otherwise provided no prognostic information. The presence of SEP scalp potentials bilaterally predicted favorable outcome, particularly if the central conduction times were normal. Conversely, the absence of one or both scalp potentials was associated with unfavorable outcome. EEGs thus provided useful prognostic information in only a minority of patients, By comparison. SEPs allowed prediction of both favorable and unfavorable outcomes in a much larger number of patients, and were therefore prognostically superior Key words: Head injury; Prognosis; Outcome prediction; Electroencephalography; Somatosensory evoked potentials
The m a n a g e m e n t of patients with severe head injury (HI) is labor-intensive and expensive. A n accurate method of predicting the outcome in individual patients with severe HI would be valuable. The ideal method would provide reliable prognostic i n f o r m a t i o n as early as possible. Most of the established methods of neurological assessment after HI have limitations with regard to outcome prediction. The Glasgow C o m a Scale ( G C S ; Teasdale and J e n n e t t 1974) has some value ( N a r a y a n et al. 1981; Marshall a n d Bowers 1985), but is affected by variables such as alcohol intoxication and hypoxemia, a n d becomes impossible to o b t a i n in sedated and paralysed patients. C o m p u t e d t o m o g r a p h y (CT) of the head can predict favorable ( N a r a y a n et al. 1981) and unfavorable (Marshall and Bowers 1985) outcomes in a small percentage of cases. C T may, however, be falsely pessimistic in a significant p r o p o r t i o n of patients ( N a r a y a n et al. 1981). l n t r a c r a n i a l pressure m o n i t o r i n g can identify a subset of patients likely to die (Marshall and Bowers 1985), but otherwise provides only limited prognostic information, and is not available in m a n y centers.
Correspondence to: Dr. R.W. Frith, Department of Clinical Neurophysiology, Auckland Hospital, Park Road, Auckland 1 (New Zealand).
Recent studies ha~e shown that evoked potentials can provide prognostic i n f o r m a t i o n following HI ( G r e e n b e r g et al. 198t; G r e e n b e r g a n d Ducker 1982: C h i a p p a t983; S p e h l m a n n 1985). F u r t h e r m o r e , work from this unit ( H u m e et al. 1979; H u m e a n d C a n t 1981: C a n t et al. 1986; Shaw 1986: C h a n c e l l o r el al. 1988: Judson et al. 1990) and from others ( G r e e n b e r g et aL 1977; De la Torre et al. 1978; Lindsay et al. 1981: Lutschg et al. 1983: R u m p l et al. 1983; A n d e r s o n et al. 1984; De Weerd and G r o e n e v e l d 1985) has shown that of the various types routinely recorded, somatosensory evoked potentials (SEPs) following m e d i a n nerve stimulation are the most useful a n d are capable of predicting both favorable and u n f a v o r a b l e outcomes. Electroencephalographic ( E E G ) changes occur following HI (Courjon and Scherzer 1972). In theory, the degree of change might relate to HI severity, a n d hence outcome. The ability of EEG to predict o u t c o m e is, however, uncertain. Bricolo (1976) divided post-H1 EEGs into 5 groups, each associated with a different likelihood of fatal outcome. Using this system, the p r o p o r t i o n of patient> dying ranged from 13~( in those with a diphasic E E G with spindles, to 100~ if the E E G was isoelectric. Bergamasco et al. (1968) reported a correlation between 1-1-.'G sleep patterns, or circadian changes, with s u b s e q u e n t recovery following HI. This study examined a small group of patients a n d involved prohmged polygraphic recordings. G a n e s and L u n d a r
EEG AND SEPs FOLLOWING SEVERE HEAD INJURY (1988) found no relation between non-isoelectric EEG patterns and outcome following HI, although grading of the recordings was not performed. Rodin (1967) was unable to find any features of non-isoelectric EEGs which distinguished early from late death in 42 patients with HI. The relative prognostic values of EEG and SEP recordings in post-traumatic coma have yet to be determined. In this study we compared the predictive values of these recordings following severe HI.
229 TABLE I EEG grading criteria. A. H o c k a d a y system
la Alpha rhythm. 2a Predominanttheta with rare alpha. 3a Delta mixed with theta and rare alpha. 4a Diffusedelta with brief isoelectric intervals. 5a A nearly flat record.
lb Predominantalpha with rare theta. 2b Predominant theta with some delta. 3b Predominant delta and no other activity. 4b Scattered delta in some leads only. 5b No EEG at all.
B. Prior system
Methods and materials
The study was carried out over a 3 year period on 100 patients admitted with severe HI to the Auckland Hospital Department of Critical Care Medicine. This department provides a centralized service for severe HI for a population of approximately one million people. The patients were part of another study examining the role of SEPs following HI (Judson et al. 1990). Inclusion criteria included (a) HI the result of blunt trauma, (b) lack of pre-existing brain disease, and (c) initial GCS less than or equal to 8. The GCS was recorded immediately prior to sedation/intubation, or at 6 h if intensive care was delayed. We excluded patients who died for reasons unrelated to their HI. All patients were intubated and hyperventilated (Judson et al. 1990); sedation and neuromuscular blockade were used to produce a state of narcosis and reflex suppression resembling neuroanesthesia. The agents used were papaveretum by infusion (usually 5-10 rag/h), diazepam intermittently i.v. (usually 5-10 mg, 6 hourly) and pancuronium by infusion (usually 4 m g / h ) . Patients with clinical seizures received diphenylhydantoin (20 m g / k g load, then 6 m g / k g / d a y ) . Phenobarbital was not used. CT head scans were performed, and neurosurgery carried out when indicated. EEG and SEPs were performed within 3 days of HI. This was within 24 h of HI in 59 patients, between 24 and 48 h in 26, and between 48 and 72 h in 5. Both tests were performed within 8 h of each other. In patients who had recordings performed more than once, the earliest set was chosen for analysis. We excluded 10 patients from analysis, either because an EEG was not performed, or because the EEG was not available for review. The EEGs were recorded on an 8-channel Mingograf machine (Siemens-Elema), using subdermal platinum alloy electrodes placed according to the international 10-20 system. The gain was 50 or 70 /~V/cm, except with apparently isoelectric traces, where 20/~V/cm was used. Reactivity of the EEG was tested by (a) shouting the patient's name, and (b) applying painful stimuli to each hand in turn. The SEP recordings were made with a TN-3000 evoked response analyzer, using methods we
1 Alpha rhythm dominant. 2 Theta activitydominant; rare alpha waves, or delta activity dominant with plentiful other activity present. 3 Continuousdelta activity dominant with little other activity, or continuous spike activity, or episodic reduction in voltageor complete isoelectric periods of less than 1 sec duration. 4 Isoelectricintervals of 1 sec or more duration separated by any type of activity and not initiated or reversed by stimuli or scattered delta activity in some leads with flat traces in others or an almost isoelectric tracing. Absence of response to stimulation. 5 Isoelectrictracing. No recognizablecerebral activity and absence of response to stimulation.
have previously described (Chancellor et al. 1988). In brief, neck and scalp potentials were recorded simultaneously following unilateral stimulation of the left and right median nerves. Two of the authors graded the EEGs by consensus, blinded to patient outcome. In the absence of an accepted system of EEG grading in post-traumatic coma, the scales of Prior (1973) and Hockaday et al. (1965) were used (Table I). Although neither was designed specifically for use in post-traumatic coma, both have been used in post-anoxic coma. The Hockaday scale has twice as many grades as the Prior system, but they are otherwise similar and involve principally an assessment of the frequency composition of the EEG. Drug-induced beta activity was disregarded for grading purposes. If there was left-right asymmetry, the worse side was graded. Any change in the cerebral activity following external stimulation (reactivity) was noted. The SEPs were graded on a 3-point scale in blind fashion by one of the authors, using (a) the presence or absence of a scalp recorded N20 potential and (b) the central conduction time (CCT), defined as the interpeak latency between cervical and scalp potentials. SEPs were grade 1 if the CCTs were normal bilaterally, grade 2 if one or both CCTs (or the left-right difference) were beyond the upper limits of normal, and grade 3 if one or both scalp potentials were absent. The upper limit of normal for CCT was 3 S.D.s above the age-related mean for this laboratory (i.e., normal is less than 7.0 msec for subjects under 50 years, and less than 7.3 msec for those
230
D.O. H U T C H I N S O N ET AL.
50 or more years) (Hume et al. 1982). We did not consider scalp potential amplitudes in the grading, as it is our experience that these show wide inter-individual variability. One of the authors reviewed the surviving patients at 6 months and categorized their outcomes using a modification of the criteria of Jennett and Bond (1975), into good outcome, moderate disability, severe disability, and death. G o o d outcome and moderate disability were considered favorable outcomes, and severe disability and death were considered unfavorable (Karnaze et al. 1982).
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There were 90 patients (median age 21 years, range 10-70) of whom 65 were male. The majority (73 patients) had HI due to road traffic accidents. Ages, GCSs and number of days ventilated are shown in relation to outcome in Table II. The indications for neurosurgery were extradural hematoma (6 patients), hemorrhagic contusion or intracerebral hematoma (6), subdural hematoma (4), and elevation of skull fracture (2). At 6 months, 27 patients had good outcome, 22 moderate disability, 8 severe disability, and 33 had died. In the last group, death occurred a median of 3 days (range 1-73) after HI. Fig. 1 shows the EEG grades (Hockaday system) in relation to outcome. Ten patients had severely abnormal (grades 4 a - 5 b ) EEGs, and all died. Three patients had EEGs which were grade l b or 2a (no delta activity); all survived but were left with moderate (2) or severe (1) disability. The remaining EEGs, comprising 86% of the total, fell into a limited number of grades (2b, 3a and 3b). Similar results were obtained when the Prior EEG grades were related to outcome (Fig. 2). All of the patients with a severely abnormal EEG (grade 4 or 5) died. All but one of the remaining EEGs (i.e., 88% of the total) were graded as 2 or 3, and similar outcomes were seen in these two patient sets.
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231
with severe disability and the other survived in a vegetative state. Fig. 4 compares the abilities of the EEGs and SEPs to predict favorable outcome. In order to achieve adequate numbers in each set, EEG grades 1 and 2, and grades 4 and 5, were combined. For both the Hockaday and Prior systems, the probability of favorable outcome with a grade 1 or 2 E E G was slightly greater than 0.5, while the probability of favorable outcome with a grade 3 E E G was paradoxically slightly greater. By contrast, the probabilities of favorable outcome were clearly different for each of the SEP grades, with an association between increasing grade and worse outcome.
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good outcome, 4 moderate disability) and 2 had unfavorable outcome (1 severe disability, 1 death). The EEGs of 5 patients contained epileptiform activity. This consisted of frontal sharp waves or spikes, which were unilateral in 3 patients and bilateral in 2. Four had favorable outcome (1 good outcome, 3 moderate disability), and 1 died. SEP grades in relation to outcome are shown in Fig. 3. Of those with grade 1 (normal) SEPs, 90% had favorable outcome. With grade 2 SEPs, 69% had favorable outcome and with grade 3 SEPs, 6% had favorable outcome. There was a very strong association between SEP grade and outcome (X 2 = 46.77, P < 0.001). Of the patients with grade 3 SEPs, 8 had unilateral, and 23 had bilateral absence of scalp potentials. Of the 5 patients who survived with grade 3 SEPs, 3 had absence of only one scalp potential, and 2 had bilaterally absent scalp potentials. Of the latter, one was left
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Fig. 4. Probability of favorable outcome, with 95% confidence limits, for the EEG and SEP grades. Note the amalgamation of E E G grades 1 and 2 and 4 and 5.
The present study compared the prognostic values of single EEG and SEP recordings in a group of patients with severe HI. There were no clear relationships between most of the Hockaday and Prior EEG grades and outcome. The exception was the isoelectric or very severely abnormal EEG, which was highly predictive of fatal outcome. This association was expected, as the isoelectric EEG is an accepted indicator of brain death (Dawson et al. 1951; Rodin et al. 1965) provided drug effects and hypothermia are excluded. There was a strong tendency, using both grading systems, for the EEGs to fall into a small number of categories. This clustering provided some explanation for the inability of non-isoelectric EEGs to predict outcome. The most likely cause of this is insensitivity of the investigation for assessing HI severity. Another possible explanation is inadequacy of the currently available EEG grading systems, particularly their failure to consider EEG reactivity. There was a significant association between reactivity of the L E G to external stimulation and outcome, with the presence of reactivity tending to predict favorable outcome. We are not aware that this has previously been shown. The observation probably reflects the association between EEG reactivity and relatively light coma (Arfel 1975). Sleep transients, found in a proportion of the EEGs, also predicted favorable outcome, although the numbers were small. Previous authors have associated sleep-like EEG activity with survival following HI, although none have specified residual neurologic disability (Chatrian et al. 1963; Bergamasco et al. 1968; Bricolo 1976). SEPs predicted both favorable and unfavorable outcomes considerably better than the EEG. The presence on both sides of a scalp potential following median nerve stimulation was associated with favorable outcome, regardless of the CCT. The association with favorable outcome was greater, however, for patients in whom the CCTs were both normal. Conversely, the
232
absence of one or both scalp potentials was associated with death or unfavorable outcome, and death resulted in almost all patients in whom both scalp potentials were absent. Thus, normal and severely abnormal SEPs correlated strongly with favorable and unfavorable outcomes respectively. Of note, 69% of those with CCT prolongation as the sole SEP abnormality (grade 2) had favorable outcome, This differs from previous reports (Hume et al. 1979; Lutschg et al. 1983; Rumpl et al. 1983) which have stressed the association between prolonged CCT and unfavorable outcome. The prognostic superiority of SEPs over EEG may be due to a number of reasons: (1) Many factors, not all necessarily affecting outcome, influence the EEG more than the SEP. These, which are common in HI patients, include damage to the skull or scalp, toxic and metabolic disorders, seizures and depth of coma. Medications used in the treatment of HI patients also have a marked effect on the EEG (Bauer 1987) but probably have little influence on SEPs or CCT (Cant and Shaw 1986). (2) The optimal time to record post-HI EEGs has not been established. Some have reported an increased yield of abnormalities early (within 30 min; Dow et al. 1944), while others have shown that significant changes may be delayed beyond 48 h (Dawson et al. 1951). Continuous monitoring has revealed the varying nature of the EEG following HI (Cant and Shaw 1984). SEP recordings, by contrast, show less variability with time and can provide prognostically useful information from an early stage (Judson et al. 1990). (3) EEG interpretation is less objective than SEP interpretation. Judging from the present set of results, it should be possible to construct a modified EEG grading system to incorporate additional factors such as reactivity and the presence of sleep transients. Any increase in predictive power would, however, be gained at the expense of a more complex grading process. A further limitation is that sleep activity appeared in a minority of EEGs, even of those patients who ultimately did well. Similarly, EEG reactivity correlated only weakly with outcome when compared with the SEP findings. For instance, of the patients who died, one-third had reactive EEGs. In contrast, all but one of those patients with a reactive EEG who died had abnormal SEPs. A reactive EEG therefore did not necessarily predict a normal SEP. In summary, we have shown that within the first 3 days following severe HI: (1) An EEG which is isoelectric, or nearly so, is strongly predictive of death (provided other causes of an isoelectric EEG are excluded). (2) Other EEG grades (Hockaday or Prior) have no correlation with outcome. (3) Reactivity of the EEG to external stimulation has a significant association with favorable outcome. (4) With SEPs, the presence of scalp potentials bilaterally correlates strongly with favorable outcome. This association is further strengthened if the CCTs are normal bilaterally. (5) The absence of one or
D.O. H U T C H I N S O N ET At..
both scalp potentials almost always predicts unfavorable outcome. (6) Overall, SEPs provide prognostic information which i.s superior to that obtained by the EEG when the scales of Hockaday or Prior are utilized alone. It is possible that if EEG analysis were to include such information as reactivity and the presence of sleep transients, the prognostic value may be improved.
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EEG AND SEPs FOLLOWING SEVERE HEAD INJURY Ganes, T. and Lundar, T. EEG and evoked potentials in comatose patients with severe brain damage. Electroenceph. clin. Neurophysiol., 1988, 69: 6-13. Greenberg, R.P. and Ducker, T.B. Evoked potentials in the clinical neurosciences. J. Neurosurg., 1982, 56: 1-18. Greenberg, R.P., Becker, D.P., Miller, J.D. and Mayer, D.J. Evaluation of brain function in severe human head trauma with multimodality evoked potentials. Part 2. Localization of brain dysfunction and correlation with post-traumatic neurological conditions. J. Neurosurg., 1977, 47: 163-177. Greenberg, R.P., Newlon, P.G., Hyatt, M.S., Narayan, R.K. and Becker, D.P. Prognostic implications of early multimodality evoked potentials in severely head-injured patients. A prospective study. J. Neurosurg., 1981, 55: 227-236. Hockaday, J.M., Potts, F., Epstein, E., Bonazzi, A. and Schwab, R.S. Electroencephalographic changes in acute cerebral anoxia from cardiac or respiratory arrest. Electroenceph. clin. Neurophysiol., 1965, 18: 575-586. Hume, A.L. and Cant, B.R. Central somatosensory conduction after head injury. Ann. Neurol., 1981, 10: 411-419. Hume, A.L., Cant, B.R. and Shaw, N.A. Central somatosensory conduction time in comatose patients. Ann. Neurol., 1979, 5: 379-384. Hume, A.L., Cant, B.R., Shaw, N.A. and Cowan, J.C. Central somatosensory conduction time from 10 to 79 years. Electroenceph. clin. Neurophysiol., 1982, 54: 49-54. Jennett, B. and Bond, M. Assessment of outcome after severe brain damage: a practical scale. Lancet, 1975, i: 480-484. Judson, J.A., Cant, B.R. and Shaw, N.A. The early prediction of outcome from cerebral trauma by somatosensory evoked potentials. Crit. Care Med., 1990, 18: 363-368. Karnaze, D.S., Marshall, L.F., McCarthy, C.S., Klauber, M.R. and Bickford, R.G. Localizing and prognostic value of auditory evoked responses in coma after closed head injury. Neurology, 1982, 32: 299-302.
233 Lindsay, K.W, Carlin, J., Kennedy, I., Fry, J., Mclnnes, A. and Teasdale, G.M. Evoked potentials in severe head injury - analysis and relation to outcome. J. Neurol. Neurosurg. Psychiat., 1981, 44: 796-802. Lutschg, J., Pfenninger, J., Ludin, H.E and Vassella, F. Brain-stem auditory evoked potentials and early somatosensory evoked potentials in neurointensively treated comatose children. Am. J. Dis. Child., 1983, 137: 421-426. Marshall, L.F. and Bowers, S.A. Outcome prediction in severe head injury. In: R.H. Wilkins and S.S. Rengachary (Eds.), Neurosurgery, Vol. 2. McGraw-Hill, New York, 1985: 1605-1608. Narayan, R.K., Greenberg, R.P., Miller, J.D., Enas, G.G., Choi, S.C., Kishore, P.R.S., Selhorst, J.B., Lutz, H.A. and Becker, D.P. Improved confidence of outcome prediction in severe head injury. A comparative analysis of the clinical examination, multimodality evoked potentials, CT scanning and intracranial pressure. J. Neurosurg., 1981, 54: 751-762. Prior, P.F. The EEG in Acute Cerebral Anoxia. Excerpta Medica, Amsterdam, 1973: 43-46. Rodin, E.A. Contribution of the EEG to prognosis after head injury. Dis. Nerv. Syst., 1967, 28: 595-601. Rodin, E., Whelan, J., Taylor, R., Tomita, T., Grisell, J., Thomas, L.M. and Gurdjian, E.S. The electroencephalogram in acute fatal head injuries. J. Neurosurg., 1965, 23: 329-337. Rumpl, E., Prugger, M., Gerstenbrand, F., Hackl, J.M. and Pallua, A. Central somatosensory conduction time and short latency somatosensory evoked potentials in post-traumatic coma. Electroenceph, clin. Neurophysiol., 1983, 56: 583-596. Shaw, N.A. Somatosensory evoked potentials after head injury: the significance of the double peak. J. Neurol. Sci., 1986, 73: 145-153. Spehlmann, R. Evoked Potential Primer. Butterworth, Boston, MA, 1985. Teasdale, G. and Jennett, B. Assessment of coma and impaired consciousness: a practical scale. Lancet, 1974, ii: 81-84.
