outcome evaluation following subarachnoid hemorrhage

J Neurosurg 64:191-196,1986

Outcome evaluation following subarachnoid hemorrhage

HANS S.~VELAND, M.D., BENGT SONESSON, PH.D., BENGT LJUNGGREN, M.D., LENNART BRANDT, M.D., TOnE USKI, M.D., STEFAN ZYGMUNT, M.D., AND BENGT HINDFELT, M.D.

Departments of Neurosurgery, Psychiatry, and Neurology, University Hospital, Lund, Sweden

u- Seventy-eight individuals among a population of 1.46 million suffered aneurysmal subarachnoid hemorrhage (SAH) during ~ 1983. Within 24 hours after the bleed, 32 of the 78 patients were in Hunt and Hess neurological Grades I to II, 13 were in Grade III, 21 were in Grades IV to V, and 12 were dead on admission to a hospital or forensic department. When the amount of blood visualized on computerized tomography (CT) scanning was integrated with the Hunt and Hess neurological classification in order to improve prediction of prognosis, only 16 patients were considered to have a good prognosis (CT-modified Grades I to II), 21 had a less favorable prognosis (CT-modified Grade III), and 29 had a poor prognosis (CT-modified Grades IV to V).

Assessment at 1 year revealed that only 32 patients (41%) had a good physical recovery. The physical morbidity rate was 22%, and the overall mortality rate was 37%. Twenty-six individuals with a good neurological outcome and five with a fair outcome also underwent reexamination 1 year or more post-SAH, which included a comprehensive evaluation of the quality of life, assessment of cognitive dysfunction, and determination of general adjustment. Five of the patients with a good neurological outcome and all five with a fair outcome (four of whom had had a poor prognosis in the acute stage) showed severe psychosocial and cognitive incapacitation. When functional morbidity, based upon persistent severe cognitive and psychosocial impairment, was included in the outcome assessment, only 33% of the total series was considered to have a favorable outcome. Approximately 60% of the initially good-risk patients (Grades I and II) showed a good physical outcome without concomitant indications of severe cognitive dysfunction and/or psychosocial impairment. Among the good-risk patients with a CT-modified grade, the figure was 70%. It is suggested that in any outcome grading system, persistent cognitive and psychosocial disturbances be taken into account.

KEY WORDS ~ intracranial aneurysm �9 subarachnoid hemorrhage �9 psychosocial function �9 cognition outcome

T HE prognosis of aneurysmal subarachnoid hem-

orrhage (SAH) depends on an array of factors such as neurological condition, patient s age,

associated disease, and aneurysm configuration and location. These factors have been taken into account to varying extents in the existing grading systems used to assess surgical risk and potential outcome. 5"13'14'21'22'27"32' 38,39,43 In the acute stage after the bleed, clinical features may offer valuable guidance in determining risk and outcome, but they do not allow selection of those patients who are likely to develop delayed ischemic cerebral com- plications. Over the last decade, computerized tomography (CT) has come into routine use in the acute evaluation of patients with SAH ,2,7-I 1,15,19,20,25,26,28,30,31,33,34,37,41,42 and evidence is emerging that the amount of extravasated blood within the intracranial compartment correlates positively with the subsequent development of vasospasm and ischemic deterioration) 1.12,28 The CT

findings in the acute stage could therefore reasonably be integrated into any prognostic grading system in order to identify the patients likely to develop delayed ischemic cerebral dysfunction.

In most previous reports, the final outcome after SAH has been classified as either good, fair, or poor; "good" usually means no neurological deficits, "fair" denotes slight or moderate neurological disability, and "poor" indicates severe permanent deficits. Other grading systems have also been used. Thus, Auer t classified those patients who could lead a full and independent life without neurological deficit as having made an excellent recovery, while minimally disabled patients were classified as good, moderately disabled as fair, and severely disabled as having a poor outcome. Suzuki, et al.,35 defined the surgical results at the time of discharge from the hospital as excellent (completely intact patients), good (mild neurological deficits allowing normal

J. Neurosurg. / Volume 64/February, 1986 191

TABLE 1 Assessment of psychosocial and cognitive recovery

Assessment of Function Score* subjective disturbances in energy resources, emotional

state, self-assertion, and cognition slight restriction, although close to normal living + 1 moderate disturbances imposing noticeable limita- +2

tions in daily life severe psychological restriction and considerable ham- +3

pering of quality of life, marked reduction in working capacity

objective neuropsychological assessment of cognitive functioning

slight impairment of single intellectual modalities, + 1 predominantly memory dysfunction

moderate impairment of several modalities; memory +2 deficits and disturbances of spatial perception and perceptual speed

considerable impairment involving memory, percep- +3 tion, and concept formation

* Scores are totaled for determination of psychological and cognitive status: see Table 2.

social life), fair (normal social life not possible), and poor (unassisted domestic life impossible).

Despite a satisfactory neurological recovery, many SAH patients may show personality changes and cognitive dysfunction that interfere with rehabilitation and social reintegration. 24'4~ Furthermore, it has been rec- ognized that cognitive and emotional sequelae often provide a greater handicap in the post-hemorrhage recovery process than does the physical disability. 3,4,6'16,36 Such disturbances could reasonably be included when assessing the grade of recovery after aneurysmal SAH.

Consequently, there is a need for a revision of the outcome grading system which takes into account not only neurological sequelae but also persistent cognitive dysfunction and other manifestations of SAH-induced encephalopathy. The present retrospective study of patients with aneurysmal SAH will address the additional impact of CT findings of blood accumulation in the subarachnoid space with respect to clinical prognosis, considering not only neurological sequelae but also cognitive and psychosocial disturbances.

Clinical Material and Methods

Seventy-eight individuals among a population of 1.46 million suffered aneurysmal SAH during 1983. 23 Sixty-three of these patients received neurosurgical care at our institution, and three remained at local hospitals. Twelve individuals were dead on admission to the hospital or forensic department.

Retrospective grading of CT-visualized subarachnoid blood into four groups according to the method of Fisher, et al., 11 was performed in the 45 patients who were in Hunt and Hess 14 neurological Grades 1 to III in the acute stage following SAH. Patients with thick vertical layers of blood (Fisher Group 3) with or without intracerebral or intraventricular hemorrhage were as-

H. Sfiveland, et al.

TABLE 2 Psychosocial and cognitive status

Status Score* completely unaffected 0 mild incapacitation 1-2 moderate incapacitation 3-4 severe incapacitation 5-6

* Scores determined by totaling the subjective and objective scores in Table 1.

signed to the next less favorable Hunt and Hess grade. The 21 patients in poor condition (Hunt and Hess Grade IV or V) were not reclassified.

At reexamination of all 49 surviving patients 1 year or more post-SAH (mean 19 months), the physical outcome was assessed as good (no neurological deficit), fair (independent with minor to moderate deficits, and/ or hydrocephalus demanding a secondary shunt operation), and poor (not independent, or institutionalized with major deficit). Outcome results obtained at assess- merit 2 months post-SAH have been reported previ- ously. 23 Twenty-seven of the 32 patients who were classified at 1 year as having a good physical recovery and five of the seven patients with a fair outcome fulfilled our criteria for neuropsychological assessment; that is, they were younger than 70 years of age. This age limit was established in order to minimize the effect of senile degenerative brain disease in evaluating cognition. One patient with a good physical outcome could not be assessed due to language difficulties.

The neuropsychological assessment of the 31 avail- able patients with a good and fair outcome included a comprehensive psychological examination and a clinical interview to determine the quality and functioning of the patients' cognitive abilities and their psychosocial reintegration. Standardized instruments were used to evaluate verbal intellectual capacity, learning and memory function, visuo-spatial organization, perceptual speed and accuracy, and concept formation. The general procedures and psychometric instruments used are described in a recent paperfl 4 The outcome for this group of patients was scored according to the protocol shown in Tables 1 and 2.

Results

At the 1-year assessment of outcome, two individuals were reclassifed from a fair to a good physical outcome, and one patient was reclassified from a poor to a fair outcome. Table 3 gives the clinical grade in the acute stage according to Hunt and Hess 14 in relation to the physical outcome at 1 year. Of the original 78 patients, 32 (41%) had a good physical recovery at 1 year, 17 (22%) were in fair or poor condition, and 29 (37%) were dead.

The CT-modified grades in relation to physical outcome at 1 year are presented in Table 4. A comparison

192 J. Neurosurg. / Volume 64/February, 1986

Outcome evaluation after SAH

TABLE 3 Neurological grade in the acute stage after SAH versus

outcome at 1 year*

Physical Outcome Total Grade

Good Fair Poor Deadt Cases

I 5 1 1 2 9 1I 19 0 3 1 23 III 6 1 4 2 13 IV 2 2 2 2 8 V 0 3 0 10 13 total 32 7 10 17 66

* Neurological grading was according to the system of Hunt and HessJ 4 SAH = subarachnoid hemorrhage.

t The 12 individuals who were dead on admission are not included in this table.

of Tables 3 and 4 shows that the patients in H u n t and Hess Grades I to III and who were in Fisher Group 3 according to the CT examinat ion were reclassified to the next lower grade, as described above.

Of the 26 individuals with a good neurological recovery who were examined with regard to psychosocial and cognitive status, none was completely unaffected. In- capacitation was mild in five, moderate in 16, and severe in five. All five examined patients with a fair neurological outcome demonstrated severe psychological incapacitation. Table 5 shows the psychosocial and cognitive status in the 31 patients younger than 70 years of age with a good or fair neurological outcome compared to the H u n t and Hess grade in the acute stage after SAH. The psychosocial and cognitive outcome in these 31 patients related to CT-modif ied grade is given in Table 6.

This study reveals that approximately one of five patients (five of 26) with a good physical recovery is so incapacitated by persistent psychosocial and cognitive disturbances that the final outcome has to be considered

TABLE 4 CT-modified neurological grade in the acute stage after SAH

versus outcome at I year*

Physical Outcome Total Grade

Good Fair Poor Deadt Cases

I 5 0 0 0 5 II 7 1 1 2 11 IIl 12 2 4 3 21 IV 8 1 5 2 16 V 0 3 0 10 13 total 32 7 10 17 66

* Neurological grading was according to the system of Hunt and Hess] 4 For a description of the method of modified grading using computerized tomography (CT) see text. SAH = subarachnoid hemorrhage.

t The 12 individuals who were dead on admission are not included in this table.

TABLE 5 Neurological grade in the acute stage after SAH versus

psychosocial and cognitive status at 1 year*

Psychosocial and Cognitive Statust

Mild Moderate Severe Total Grade Completely Incapaci- Incapaci- Incapaci- Cases

Unaffected ration ration ration

I 0 2 2 0 4 II 0 2 8 5 (1) 15 III 0 1 5 1 (1) 7 IV 0 0 1 2 (1) 3 V 0 0 0 2 (2) 2 total 0 5 16 10 (5) 31

* Neurological grading was according to the system of Hunt and Hess. '4 SAH = subarachnoid hemorrhage.

t Psychosocial and cognitive status was assessed in patients with a good or fair physical outcome. Numbers in parentheses indicate patients with a fair outcome.

as unfavorable despite the absence of gross neurological deficits. When severe psychosocial and cognitive im- pa i rment was integrated in the outcome assessment at 1 year, only 21 of 66 individuals were considered to have a favorable physical and psychological outcome. Of the 32 patients who initially were in H u n t and Hess Grades I to II, 19 (59%) showed a good physical outcome without concomi tan t indications of any severe psychosocial or cognitive impairment . Such favorable outcome was shown by 11 (69%) of the 16 individuals in CT-modif ied Grade I or II in the acute stage (Table 6). Table 7 summarizes the outcome based on good physical recovery and on combined good physical and psychological recovery in all individuals in the series, in good-risk patients (Grades I to II), and in good-risk patients with a CT-modif ied grade.

TABLE 6

CT-mod~[~ed neurological grade in the acute stage after SAH versus psychosocial and cognitive status at 1 year*

Grade

Psychosocial and Cognitive Statust

Mild Moderate Severe Total Completely Incapaci- Incapaci- Incapaci- Cases Unaffected ration tation tation

1 0 2 2 0 4 II 0 2 3 2 (1) 7 III 0 0 7 3 10 IV 0 1 4 3 (2) 8 V 0 0 0 2 (2) 2 total 0 5 16 10 (5) 31

* Neurological grading was according to the system of Hunt and HessJ 4 For a description of the method of modified grading using computerized tomography (CT) see text. SAH = subarachnoid hemorrhage.

t Psychosocial and cognitive status was assessed in patients with a good or fair physical outcome. Numbers in parentheses indicate patients with a fair outcome.


Discussion

The severity of an aneurysmal bleed is indicated by the patient's clinical status in the early recovery phase after the SAH and by the amount of extravasated blood. Previous grading systems relate the severity ofan- eurysm rupture only to the clinical status of the patient. 5'1s~14'21'22'27 With the advent of CT, a new diagnos- tic tool was added that allows evaluation of the amount of blood in the subarachnoid space, the ventricles, and the brain parenchyma. 2'7-12'15'19'20'25'26'28'3~

Subsequently, it has been shown that the development of vasospasm or delayed ischemic cerebral deterioration correlates with increasing amounts of blood in the subarachnoid cisterns and cerebral fissures as visualized by CT. 11'12'19"25'26'28'30'31 In a 1984 update of the Inter- national Cooperative Study on timing of aneurysm surgery, Kassell and Torner ~s reported that vasospasm was the leading cause of mortality and morbidity (34%) in 1272 patients with an unfavorable outcome.

Therefore, a modification of the Hunt and Hess grading system that takes into account the amount of extravasated blood ought to improve predictability of final outcome. As shown in Table 7, such a modification increased predictability only with regard to cognitive and psychosocial recovery. The fact that predictability in terms of neurological recovery was not altered is probably explained by the fact that the good-risk patients were subjected to early aneurysm operation with intraoperative evacuation of blood-contaminated cerebrospinal fluid and clots around the exposed cerebral arteries, and that these patients received additional anti-ischemic treatment with nimodipine. 23 Of 18 good- risk patients with a good physical recovery who were subjected to an additional neuropsychological assessment, four showed severe incapacitation from a diffuse post-SAH encephalopathy, while only one of 10 good- risk patients with a CT-modified grade and a good physical outcome showed severe psychosocial and cognitive incapacitation. Thus, there seems to exist a relationship between persistent disturbances of cognition

TABLE 7 Percentage of patients with a good outcome based on

neurological grade in the acute stage after SAH*

Good Good Physical & Patient Group Physical Psychological

Outcome Outcome all patients with aneurysmal SAH 41% 33 % patients in Hunt & Hess Grade l-II 75% 59% patients in CT-modified Grade I-II 75% 69%

* Neurological grading based on the system of Hunt and HessJ 4 For a description of the modified grading system involving computerized tomography (CT) quantitation of extravasated blood see text. Patients with a good physical outcome had no neurological deficit and those with a good psychological outcome had no severe psychosocial or cognitive incapacitation. SAH = subarachnoid hemorrhage.

H. S~iveland, et al.

and psychological function after aneurysmal SAH and the severity of the aneurysmal bleed.

A careful neuropsychological assessment following SAH will frequently reveal subtle yet important cognitive defects that should be considered in any outcome evaluation. It does not seem appropriate to grade the results of surgical treatment into rough categories based only on gross neurological examination and superficial estimation of psychosocial and cognitive recovery. Many patients will consider themselves more or less fully recovered, whereas information from relatives or family members may disclose difficulties frequently disregarded or suppressed by the patient. Sometimes, even a total denial of any incapacitation may be en- countered, while circumstantial information may present a totally different picture. Such incorrect information may also be the result of psychological defensive measures or even an expression of cerebral pathology with concomitant lack of awareness. Thus, a careful investigation into the post-SAH reintegration process will yield information quite often at variance with firsthand impressions and statements of recovery. With our present knowledge about the impact of cognitive dysfunction and psychosocial disturbances on prognosis and the quality of life after a major aneurysmal SAH, 24"4~ it seems inappropriate not to include evidence of such dysfunction when considering the final outcome.

It is our experience that very few patients, if any, will have a full recovery with no signs or symptoms of a psychosocial or cognitive disturbance after a major aneurysmal SAH (see Tables 5 and 6). When working capacity is markedly reduced or the quality of life otherwise impaired, it appears reasonable to designate the outcome as unfavorable despite lack of gross neurological deficits. When the neuropsychological evaluation was integrated in the final outcome assessment 1 year or more post-SAH, not more than 33% of all patients were regarded as having achieved a favorable outcome. This result may be compared to the estimation by Kassell and Drake 17 that only 36% of individuals who suffer an aneurysmal SAH may be expected to become functional survivors.

Ropper and Zervas 29 intensively followed for at least 1 year 1 12 consecutive individuals who initially had normal neurological function following aneurysmal SAH. They found a 64% management success rate based on the number of patients who returned to work. When patients taking less demanding jobs than before SAH were excluded, the success rate was lowered to 44%. In the present series, management success based upon physical and psychological recovery was approximately 60% for the initially good-risk patients. In the majority of patients in the study by Ropper and Zer- vas, z9 loss of the capacity to work was not caused by physical deficits. The authors stressed the importance of considering functional outcome and morbidity when comparing different management protocols, and em- phasized the large proportion of patients unable to


Outcome evaluation after SAH

resume their previous level of performance due to reported psychological or emotional disturbances. Their results, obtained in patients subjected to late (delayed) operation, are corroborated in the present study, which in fact shows that no patient among those with a good neurological recovery was completely unaffected by the SAH in terms of cognitive or psychosocial effects. The widespread presence of vaguely defined psychological problems not associated with neurological deficit strongly indicates that it is improper to use the term "excellent" when describing a favorable physical outcome in patients who have suffered a major aneurys- real SAH.

It may certainly be concluded that aneurysmal SAH is a catastrophic event from which few patients recover with only minor sequelae. Seventy-four percent of the patients with SAH in the present series who had a good or fair neurological recovery were operated on in the acute stage after hemorrhage (within 3 days). 23 The important question - - whether early aneurysm operation results in an unacceptable morbidity rate when neuropsychological and cognitive status is considered as well - - so far remains unresolved, even though the results reported by Ropper and Zervas z9 indicate that psychological or emotional disturbances also occur frequently after late surgery. We conclude that persistent cognitive disturbances and psychosocial impairment should be taken into account in any outcome assessment, and, if such incapacitation is severe, the outcome should be considered unfavorable even in individuals without gross neurological deficits.

Acknowledgment

This study was conducted in honor of Dr. Einar Bj6rkelund of Lund, Sweden.

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Manuscript received March 25, 1985. Accepted in final form July 24, 1985. This study was supported by grants from the Swedish

Society of Medicine, the Thorsten and Elsa Segerfalk Foun- dation for Medical Research, and the Elsa Schmitz Founda- tion.

Address reprint requests to: Bengt Ljunggren, M.D., De- partment of Neurosurgery, University Hospital, S-221 85 Lund, Sweden.


outcome evaluation following subarachnoid hemorrhage

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