T HE most adequate method of diagnosing subdural collection of blood
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1 THE ELECTROENCEPHALOGRAM SUBDURAL HEMATOMA IN LEWIS L. LEVY, M.D., LUDWIG H. SEGERBERG, M.D., RICHARD P. SCHMIDT, M.D., RICHARD C. TURRELL, M.D., AND EPHRAIM ROSEMAN, M.D. Sections of Neurology, Neurosurgery and Electroencephalography, University of Louisville School of Medicine, and the Louisville General Hospital, Louisville, Kentucky (Received for publication May 28, 1952) T HE most adequate method of diagnosing subdural collection of blood is by complete surgical exploration. Although much aid has been obtained from the electroencephalogram (EEG) in the study of head injuries, the literature tends to be confusing in the interpretation of its value in indicating the presence of subdural hematoma. 1-3,~-14 The reader is referred to the excellent reviews of Smith, Mosberg, Pfeil and Oster 13 and of Marsh, Hjartarson and Courville 9 for a comprehensive discussion of the literature on the subject. The generally accepted EEG findings in unilateral subdural hematoma are ipsilateral reduction in amplitude of the alpha activity and/or a delta focus. PRESENT STUDY In the present study the electroencephalographic findings in 60 cases of severe head injuries were reviewed. Attempts were made to establish the diagnosis of subdural hematoma on the basis of the initial records. Serial records were examined for additional diagnostic clues. In all 60 cases the question arose some time during the hospital course of: (1) the possibility of the presence of a subdural hematoma and (r the need for exploratory surgery. This problem of the necessity for operation was a particularly pressing one in the cases of acute head injuries. In all instances there was an initial period of coma following the injury, bloody cerebrospinal fluid (CSF), a subsequent period of mental depression and/or increasing abnormal focal neurologic signs. Any of these 60 patients by such clinical criteria could have been suspected of having either unilateral or bilateral subdural hematomas. For the most part a Grass 8-channel ink-writing oscillograph was used. A minimum of 13 needle (~7 gauge) electrodes were inserted into the scalp and ear lobes, using the standard ground and bipolar runs (with reference to each other, to the ears and the vertex). RESULTS Thirty of the 60 patients had unilateral subdural hematomas (Table 1). The remaining 80 had neither subdural nor epidural hematomas. All patients having bilateral hematomas and children under 10 years of age are 588
2 THE EEG IN SUBDURAL HEMATOMA 589 TABLE 1 Total number of cases of subdm:al hematom't 1. Cases proven at operation 2. Cases found at autopsy Total number of cases of head injury without subdural hematoma 1. Bilateral burr hole exploration negative No subdural or intracerebral hematoma at autopsy 3 8. Negative X-ray pneumograms 5 4. Clinical improvement after 3 or more months 6 30 Table 1 demonstrates that there were 30 proven cases of unilateral subdural hematoma either at operation or autopsy. In the additional 30 cases of head injury without subdural hematoma, the clinical picture was the same, namely, initial period of coma, hemiparesis, and bloody cerebrospinal fluid. excluded from this study, since the EEG patterns in these groups are heterogeneous and need further study. Table ~ divides these cases, for purposes of convenience only, into the acute (0-5 days), subacute (6-15 days) and chronic head injuries (16 days TABLE Interval of time between injury and first EEG 0-5 Days 6-15 Days 16+ Days Total Subdural Head injury Total ll 60 Subd. H.I. Subd. H.I. Subd. H.I. Subd. H.I Ipsi. Dee Amp. SWF Ipsi. Dec Amp. Alone Ipsi. SWF Alone Ipsi. SWF Contra Dec. Amp. Ipsi. Dec Amp. Contra SWF Contra SWF Contra Amp No Focal ~ Abnormality Totals The head injuries (H.I.) and subdural hematomas (Subd.) are divided arbitrarily into acute (0-5 days), subacute (6-15 days) and chronic (16 days). This period indicates the time in days that the EEG was taken following the head injury. It can be seen that the EEG abnormalities in the two groups, taking into account the factor of time, have an almost identical distribution. Ipsi.=ipsilateral. Dcc.=decrease. Amp. = amplitude. SWF=slow-wave focus. Contra=contralateral.
3 590 LEVY, SEGERBERG, SCHMIDT, TURRELL AND ROSEMAN TABLE 3 Clinical signs of subdural hematoma Contralateral signs Ipsilateral signs No focal signs ~ cases 5 cases S cases In the 5 cases of subdural hematoma with ipsilateral hemiparesis there was homolateral amplitude reduction and/or slow-wave focus in the initial EEG. and over). All possible EEG patterns involving the two parameters of presence or absence of delta activity and amplitude asymmetry are listed. It will be noted that although an ipsilateral decrease in amplitude and/or slowwave focus was present in 43 of the 60 cases, the distribution in those with and without subdural hematomas was about equal. Further perusal of Table shows that all possible EEG combinations occur in relatively equal numbers in both types of eases. Table 3 indicates that 5 of the 30 patients with subdural hematoma had a hemiparesis on the side of the hematoma. This group of 5 had an ipsilateral decrease in amplitude and/or slow-wave focus. As noted in Table 4, seven members of the Neurology Department, whose electroencephalographic experience varied from 1 to 14 years, were shown the initial EEGs of all 60 cases with the names and histories deleted. Those tested were asked to indicate: (1) which records indicated the presence of subdural hematoma, (~) the side of the hematoma, (3) which were not subdural hematomas and (4) those EEGs that they thought were inconclusive. No one person correctly picked more than ~ out of 3 of the hematomas. TABLE 4 Experi- Subd. H.I. H.I. Subd. % Subd. % H. I. Examiner ence Correctly Correctly Called Called No Total Called Called Decision (years) Picked Picked Subd. H.I. Correctly Correctly E.R. lg 1~ 17 1~ L.S T.D ~ W.S R.T. ~ ~ S.A ~0 9 1~ L.L. ~ 5 ~3 7 ~ ~ 54 Total ~ ~0 Av. 5.7 ll ~ 55 Nine members of the Neurology Department with EEG experience varying from 1 to 14 years took the test. In this test they were shown the initial EEGs of all 60 patients, with deletion of case histories. They were asked to select: (1) those records that they thought indicated a subdural hematoma, (~) the side of the hematoma, (3) those records that did not indicate a hematoma, and (4) those EEGs that were inconclusive. It is to be noted that the percentage of error was high. The range of those who correctly picked the subdural hematomas was from 40 to 67 per cent, with an average of 5~ per cent. Subd.=subdural. H.I.=head injury.
4 THE EEG IN SUBDURAL HEMATOMA 591 E.R., with the most concentrated clinical and EEG experience in this field, made a 50 per cent error. The entire group correctly picked 52 per cent of the subdurals and 55 per cent of the nonsubdurals on the basis of the initial EEG findings. The percentage of correct EEG diagnoses was not altered appreciably by taking into account the various types of recordings, e.g., scalp to ear, scalp to vertex, ground and triangulation. Serial records in both groups followed similar patterns. DISCUSSION Review of the literature would give the impression, for the most part, that given an individual who has had a head injury, a presumptive diagnosis of subdural hematoma can be made on the basis of the electroencephalographic changes. The electrical abnormalities most commonly cited are ipsilateral decrease in amplitude with or without associated slow-wave focus. In the series of 60 cases of severe head injury reported here an initial period of coma and bloody CSF followed by a period of clinical worsening, usually with the appearance of focal neurologic abnormalities, were common to all. The EEG abnormalities were the same in all regardless of whether a subdural hematoma was present or not. The number of proven subdural hematomas was 30 of the total 60 cases. In 5 cases of proven subdural hematoma with homolateral focal signs, e.g., hemiparesis, there was an associated ipsilateral reduction in amplitude and slow-wave focus. This combination was not seen in any of the remaining 55 cases. (In a subsequent case which did demonstrate these findings, however, operation failed to reveal a subdural hematoma.) Thus, with the possible exception of this small group it is felt that the initial EEG is of no aid in differentiating the operative from the nonoperative cases. The presence of blood in the subdural or the epidural spaces probably plays no factor in the reduction of amplitude on the side of the lesion. This is seen to persist following operative removal of the clot and in subcortical lesions of a nontraumatic nature. Figs. 1-5 demonstrate some illustrative cases and some of the pitfalls that may be encountered in the EEG study of head injuries with particular reference to the recognition of subdural hematomas. Fig. 1 A shows an EEG taken 15 days after injury. Although it is a relatively normal one, with the exception of slight amplitude reduction on the right side, the patient became worse clinically. Subsequently, negative bilateral exploration was made and the patient returned to normal health. The EEG shown in Fig. 1 B, taken 1 day after head injury, looks very similar, but this patient's clinical course and EEG worsened. Four days after trauma a large subdural hematoma was evacuated from the left side, Thus, in both cases, there were only mildly abnormal initial EEGs; in both there was subsequent increase in clinical symptoms. Fig. ~ shows ~ more cases of head injury, one with (Fig. ~ A) and the
5 59~ LEVY, SEGERBERG, SCHMIDT, TURRELL AND ROSEMAN FIG. 1 A. R.J.T. Head injury with initial coma on July ~8, Persistent left hemiparesis, choked discs and elevated CSF pressure. Because of suspicion of subdural hematoma, bilateral trephination was made on Aug. 1O, 1944, and showed only contused cortex on the right. Subsequent complete clinical improvement. FIQ. 1 B. H.R. Head injury with initial coma ~4 hours prior to EEG. Because of worsening of clinical picture, bilateral burr-hole exploration was made 4 days after injury and a large subdural hematoma was evacuated from the left side. Note that the initial EEGs of these ~ patients are similar. The only abnormalities are a slight decrease in amplitude and delta focus (on the right side in Fig. 1 A and on the left side in Fig. 1 B).
6 THE EEG IN SUBDURAL HEMATOMA 593 Fro. 2 A. F. B.Sept. 2~, 1949,,:evere head injury with initial period of coma lasting 2 hours. Negative bilateral burr-hole exploration Sept. 22, Subsequent complete clinical improvement FIG. 2 B. E. L. Head injury with 3-hour period of coma 24 hours prior to EEG. Bilateral exploration showed large left subdural hcmatoma. Note that although the clinical histories and EEGs are similar, only one (E.L.) bad a subdural hematoma. The common EEG finding in both cases, however, was a decrease in amplitude, seen best in the left temporal region.
7 594 LEVY, SEGERBERG, SCHMIDT, TURRELL AND ROSEMAN FIG. 3 A. G. F. C. Severe head injury, 16 days prior to EEG, with left hemiparesis and confusion. Because of persistent abnormal clinical signs, bilateral burr-bole exploration was made Mar. 5, 194~ and was negative. Subsequent return to clinical normalcy. FIG. 8 B. D. M. Head injury 11 days prior to EEG. Initial coma, followed by improvement, then clinical worsening. Large left subdural hematoma evacuated 1 day later. Note that the common EEG finding in both cases i~ a reduction in amplitude (on the right side in Fig. 8 A and on the left side in Fig. 3 Ba
8 THE EEG IN SUBDURAL HEMATOMA 595 other without (Fig. ~ B) subdural hematoma. In both instances the EEGs taken within ~4 hours after the injury demonstrate very abnormal and yet very similar initial records. They are moderately slow and show an ipsilateral amplitude reduction and homolateral slow-wave focus. Again, the difficulty in differentiation of the two on basis of the EEG findings would seem impossible. Fig. 3 shows a similar difficulty in the recognition and differentiation of FIc. 4. D. S. Head injury 6 years prior to EEG. Asymptomatic in interim, but progressive development of headache, dysphasia and coma 1 day prior to EEG. Subsequent removal of large chronic subdural hematoma and membrane on left side. Note reduction in the amplitude and marked circumscribed delta focus in left temporal region. traumatic cases of a subacute or chronic nature. Fig. 3 A demonstrates an EEG taken 16 days after injury, followed by negative bilateral exploration and return to normalcy. In the case represented in Fig. 3 B a left subdural hematoma had been removed 11 days after injury and 1 day after the EEG. Both EEGs look similar in that they are mildly dysrhythmic, show mild amplitude reduction and a delta focus. In Fig. 3 A these abnormalities are seen on the right side and in Fig. 3 B they are on the left side. Fig. 4 illustrates the EEG picture in a case of chronic subdural hematoma which was asymptomatic for 6 years and then dysphasia and coma rapidly developed. At operation subsequently a large thick membrane covering almost the entire left hemisphere was removed. The right side was normal. The EEG picture presented is not unlike that seen in many types of gross hemispheric lesions. Fig. 5 demonstrates the EEG picture seen in 5 cases of subdural hematoma with ipsilateral hemiparesis. The patient illustrated had been injured 19 days prior to the first EEG (Fig. 5 A). In spite of the left hemiplegia, but
9 596 LEVY, SEGERBERG, SCHMIDT, TURRELL AND ROSEMAN Fro. 5 B because of the reduction of amplitude and slow-wave focus on the left side, a left carotid arteriogram was done and showed a picture compatible with that seen in subdural hematoma. Subsequent operation revealed a large hematoma on the left side; the right side was normal. Fig. 5 B shows initial depression of the EEG 45 minutes following the injection of a total of 40 cc. of 35 per cent diodrast. Subsequent EEGs taken 4 (Fig. 5 C) and ~4 ]~ours (Fig. 5 D) after arteriography demonstrate a worsening of the EEG picture associated with increased clinical symptoms? This occurred in spite of the fact that for the first 19 days the patient was under observation, there had been progressive clinical and EEG improvement. CONCLUSIONS The electroencephalographc analysis of 60 cases of head injury is presented with the view in mind of differentiation of those patients who have
10 THE EEG IN SUBDURAL HEMATOMA 597 Fio. 5 D FIG. 5. D.F. Found comatose on May 12, Left 3rd nerve paralysis, left hemiplegia and bloody CSF. Initial clinieal improvement. EEG taken 19 days later (Fig. 5 A) showed reduction in amplitude and delta focus in left temporal region. Because of this, and in spite of the left hemiplegia, a left earotid arteriogram was done and demonstrated a picture compatible with a subdural hematoma on this side. The patient remained eomatose subsequent to arteriography and a subdural hematoma was evaeuated on the left side. Note the persistent amplitude reduction and delta foeus on the side of the hematoma (Fig. 5 A, B, C and D). In Fig. 5 B, taken 45 minutes after left carotid arteriography, there is a generalized suppression. Subsequently, there is marked slowing of the EEG (Fig. 5 C and D), concomitant with aggravation of the clinical findings. subdural hematoma from those who do not. Thirty had proven subdural hematomas and of the other 30, 16 had negative bilateral explorations, 3 showed no evidence of hematoma at autopsy, and 11, of which 5 had normal pneumograms, returned to clinical normalcy. No data are presented on bilateral subdural hematomas or the EEG picture in infants.
11 598 LEVY, SEGERBERG, SCHMIDT, TURRELL AND ROSEMAN The findings indicate that the initial EEG is identical in these ~ groups of head injuries with and without subdural hematoma and hence make their differentiation impossible. The parameters of ipsilateral reduction in amplitude and slow-wave focus are similarly present in both regardless of whether the initial EEG is taken in the acute, subacute or chronic stage. Hence, with one possible exception, noted below, it would seem that the initial EEG is of no value in the differentiation of the "operative" from the "nonoperative" types of head injuries, particularly insofar as unilateral subdural hematomas in adults are concerned. Five cases of subdural hematoma with ipsilateral paralysis are presented. In all of these instances the hematoma was present on the side of the amplitude reduction with the slow-wave focus. REFERENCES 1. CoHx, R. Subdural hematoma. An experimental study. Arch. Neurol. Psychiat., Chicago, 1948, 59: ~. COUN, R. Clinical electroencephalography. New York: McGraw-tlill Book Co., Inc., 1949, viii, 689 pp. (see p. 174). 3. COliN, R., RAINES, G. N., MVLDER, D. W., and NEVMXNN, M.A. Cerebral vascular lesions. Electroencephalographic and ncuropathologic correlations. Arch. Neurol. Psychiat., Chicago, 1948, 60: FOLTZ, E. L., TtIOMAS, L. B., and WARD, A. A., JR. The effects of intracarotid diodrast. J. Neurosurg., 1952, 9: GURDJIXN, E. S., and WEBSTER, J.E. Traumatic intracranial hemorrhage. Amer. J. Surg., 1948, n.s. 75: 8~ HEERSEMA, P. H., and FREEMAN, J.G. The importance of diagnosing chronic subdural hematoma. Med. Clin. N. Amer., July 1945, 29: JASPER, H. H., KERSHMAN, J., and ELVIDGE, A. Electroencephalographic studies of injury to the head. Arch. Neurol. Psychiat., Chicago, 1940, 44: JASPER, H., KERSHMAN, J., and ELVIDGE, A. Electroencephalography in head injury. Res. Publ. Ass. nerv. ment Dis., 1945, 24: 388-4~0. 9. MARSH, C., HJARTARSON, G. D., and COURVIT.LE, C.B. The electroencephalographic findings in subdural hemorrhage and hematoma. Review of the literature and report of thirteen cases. Bull. Los Angeles neurol. Soc., 1949, 14: ROGERS, L. Electro-encephalography in traumatic intracranial haemorrhage. Brit. reed. J., 1941, 1 : SHORT, A. R., and DUNSTEI~, M. Traumatic extradural haemorrhage. Brit. reed. J., 1940, 1 : SJAARDEMA, H., and GL'~SE1L M.A. The electro-encephalographic diagnosis of subdural hemorrhage. Ann. Surg., 194~, 116: SMITU, G. W., MOSBERG, W. ti., PFEIL, E. T., and OSTER, R.H. The electroencephalogram in subdural hematoma. With a review of the literature and the presentation of seven cases. J. Neurosurg., 1950, 7: ~07-~ ULETT, G. Electroencephalogram of dogs with experimental space-occupying intracranial lesions. Arch. Neurol. Psychiat., Chicago, 1945, 54:
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