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Table of Contents    
ORIGINAL ARTICLE
Year : 2018  |  Volume : 66  |  Issue : 6  |  Page : 1713-1717

Neurological, neuropsychological, and functional outcome after good grade aneurysmal subarachnoid hemorrhage


1 Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bengaluru, Karnataka, India
2 Department of Clinical Psychology, National Institute of Mental Health and Neurosciences, Bengaluru, Karnataka, India

Date of Web Publication28-Nov-2018

Correspondence Address:
Dr. Dhaval Shukla
Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bengaluru - 560 029, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.246243

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 » Abstract 


Background: There is a paucity of information about which impairments, cognitive or neurological, determine the functional outcome after aneurysmal subarachnoid hemorrhage (SAH). The present study aims to determine the relative contributions of each of the above impairments for determining the functional outcome after SAH.
Materials and Methods: This is a prospective observational study including patients with aneurysmal SAH. Patients underwent assessment at 6 months after discharge for neurological deficits, cognitive impairment, and functional outcome using the National Institute of Health and Social Sciences (NIHSS) score, National Institute of Mental Health and Neurosciences (NIMHANS) Neuropsychology Test Battery, and Glasgow Outcome Scale – Extended (GOSE), respectively. The correlation of GOSE with NIHSS scores and neuropsychological test scores was done using Spearman's rho correlation coefficient.
Result: Fifty-six patients underwent assessment using all the three tools, i.e., NIHSS, neuropsychological tests, and GOSE. Fifty-one healthy volunteers participated in the study for neurological examination and neuropsychological assessment. At 6 months, patients with SAH had significant cognitive impairment as compared to controls. The mean NIHSS score was 10.01 ± 9.04, indicating moderately severe impairment. The median GOSE at 6 months was 6 (range: 3–8) indicating the upper level of moderate disability. There was a significant correlation of NIHSS scores with GOSE, Spearman's rho −0.653 (<0.001). There was a significant correlation of neuropsychological test scores with GOSE and NIHSS. The Spearman's rho for NIHSS vs GOSE was within range for neuropsychological scores vs GOSE.
Conclusion: Both the neurological deficits and cognitive impairment determine functional outcome after SAH at 6 months.


Keywords: Cognitive impairment, disability, neuropsychological outcome, subarachnoid haemorrhage
Key Message: Although cognitive deficits after aneurysmal subarachnoid haemorrhage (SAH) are well-known, the neuropsychological outcome of these patients is underreported. Impairments in attention, mental flexibility, visual working memory, verbal fluency, response inhibition, visual constructive ability, and visual memory, are the main determinants of the functional outcome in patients who have had an aneurysmal SAH and appear to in a good neurological grade. Both neurological and cognitive impairments equally determine the functional outcome after SAH, and therefore, both should be sufficiently addressed for attaining a better long-term outcome for the patients.


How to cite this article:
Dey S, Kumar J K, Shukla D, Bhat D. Neurological, neuropsychological, and functional outcome after good grade aneurysmal subarachnoid hemorrhage. Neurol India 2018;66:1713-7

How to cite this URL:
Dey S, Kumar J K, Shukla D, Bhat D. Neurological, neuropsychological, and functional outcome after good grade aneurysmal subarachnoid hemorrhage. Neurol India [serial online] 2018 [cited 2018 Dec 14];66:1713-7. Available from: http://www.neurologyindia.com/text.asp?2018/66/6/1713/246243




Aneurysmal subarachnoid hemorrhage (SAH) represents a relatively small percentage of all stroke cases (5 ~ 7%), however, its mortality and morbidity rates are among the highest.[1] Studies have shown that 15–20% of the patients die before reaching the hospital, and another 20–25% die within the first 48 hours.[2],[3] The 30-day mortality is as high as 50%.[3] There have been improvements in surgery, pharmacological treatment, and intensive care, due to which the overall mortality is decreasing at 0.9% per year over the past 2 decades.[4] In spite of this, the long-term outcome is still poor, with 30% of the survivors remaining dependent on others.[5] The end-result of the pathophysiological mechanisms after SAH is focal, and scattered brain injury may also manifest due to ischemia occurring either during the initial hemorrhage, as a consequence of macro- and microvascular dysfunction, as well as due to delayed cerebral ischemia (DCI).[5] The combination of focal and scattered brain injury results in cognitive impairment and/or focal neurological deficits.

The most frequently impaired cognitive functions after SAH are memory, executive function, and language. This strongly implicates temporal (hippocampal) and frontal lobe dysfunction.[6] Cognitive difficulties including attention, planning, and reasoning impairment after SAH affect the patient's ability to return to work.[7] The neurological deficits, such as hemiparesis or monoparesis, affect activities of daily living. An outcome assessment tool for SAH should measure the outcome caused by both neurological and cognitive impairments. In 1988, the World Federation of Neurosurgical Societies (WFNS) proposed the use of Glasgow outcome scale (GOS) for assessing patient outcomes after SAH.[8] An extended version of GOS (GOSE) has been developed and is used extensively for assessing outcome after traumatic brain injury (TBI). This eight-point scale employs additional categories to further stratify the middle and upper end of the GOS. The GOSE correlates well with other outcome assessment tools, including neuropsychological performance in patients with TBI.[9],[10],[11],[12],[13]

Studies that determine the correlation of cognitive and neurological impairment with functional outcome are lacking. We do not have information regarding which impairments, cognitive or neurological, determine the functional outcome after SAH. Hence, we conducted this study to find the determinants of functional outcome after SAH.


 » Materials and Methods Top


An approval from institute's ethics committee (NIMHANS IEC Sl. No. 5, Clinical Neurosciences) was taken, and informed consent obtained from all participants. This is a prospective observational study of patients with aneurysmal SAH, who were treated at our institute during January 2013 to June 2014. The following patients were enrolled for the study: admitted and treated for ruptured cerebral aneurysm, either with surgical clipping or coiling; and age from 20 to 70 years. Patients with pre-existing neurological or psychological disease were excluded. Clinical and radiological data of all patients who fulfilled the above-mentioned criteria were collected at the time of treatment. All patients who were alive and conscious at the time of discharge were followed up at 3 and 6 months. A total of 156 patients were enrolled at the time of admission. Twenty-six patients died within 2–3 weeks of treatment during hospitalization. From the remaining 130 survivors, 56 patients were available at follow-up for a comprehensive assessment of outcome, i.e., neurological, neuropsychological, and functional. Quantification of neurological deficits was done using the National Institute of Health Stroke Scale (NIHSS) score, which has a total score ranging from 0–42, with higher values representing more severe deficits.[14] Neuropsychological assessment was done using tailored NIMHANS Neuropsychology Test Battery to quantify neurocognitive deficits.[15] The neuropsychological tests used are listed in [Table 1]. Due to their disability and low educational level, all the tests could not be administered in a few patients. The GOSE was used for assessing the functional outcome. The assessment was done using a structured questionnaire.[16],[17] The GOSE has a total of eight categories (1–8), with the lowest value of 1 indicating death and the highest value of 8 indicating an upper level of good recovery. The NIHSS scores were determined by a detailed neurological examination by a neurosurgery resident (SD); the neuropsychological assessment was done under the supervision of neuropsychologist (KK), and GOSE was assessed independently. The evaluation of neurological deficits, the neuropsychological assessment, and the functional outcome assessment were performed 6 months after the patient's discharge from the hospital. Fifty-one healthy volunteers participated in the study for neurological examination and neuropsychological assessment. These volunteers were matched for age, gender, and educational status with that of the study patients.
Table 1: Neuropsychological tests used

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Statistical analysis

The sample size was determined based on the studies on neuropsychological impairment in SAH published in the last decade. The data was entered and analyzed using the Statistical Package for the Social Sciences version 22 (IBM Inc, USA). Independent t-test was used for continuous variables, and Pearsons’ chi-square test was used for categorical variables. The correlation of GOSE with NIHSS scores and neuropsychological assessment scores was done using Spearman's rho correlation coefficient. A multivariable analysis of factors, clinical and radiological, responsible for the outcome was not done because the primary aim of the study was to compare the two outcome tools.


 » Results Top


Fifty-six patients were available at follow-up after 6 months for a comprehensive assessment of outcome. The general demographic and clinical details of patients are listed in [Table 2]. There was no difference between patients and controls regarding their age, gender proportion, and years of education. Most of the patients had WFNS grade 1 SAH.
Table 2: General demographic and clinical profile of patients and controls

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Forty-four (80%) patients had mild-to-moderate neurological impairment (NIHSS score: <15). The mean NIHSS score at 6 months was 10.01 ± 9.04, indicating a moderate impairment. Forty-seven (85.6%) patients had a favorable outcome (GOSE: good recovery or moderate disability). The median GOSE at 6 months was 6 (range: 3–8), indicating an upper level of moderate disability. There was a significant correlation of NIHSS scores with GOSE, [Spearman's rho −0.653 (<0.001)].

All of the neuropsychological tests could not be done on all the patients due to following reasons. Six patients were illiterate and could not complete the Stroop test and the Controlled Oral Words Association (COWA) tests. Two patients were not able to perform the digit span and spatial span test, and 3 patients were not able to perform the trail making test and Rey's Auditory Verbal Learning Test. Six patients were not able to perform the complex figure test. Among the control group, 6 were illiterate and 2 could not perform the Stroop test and the COWA test. There was significant cognitive impairment in patients with SAH as compared to controls [Table 3]. There was a significant correlation of neuropsychological test scores with GOSE and NIHSS [Table 4]. The correlation was the best for the spatial span and Stroop tests, and the least for COWA and complex figure test (CFT)–copy tests. This indicates that impairments in attention and working memory and response inhibition are the main determinants of functional outcome after SAH. The Spearman's rho for NIHSS vs GOSE was within the range for neuropsychological scores vs GOSE. This indicates that both neurological and cognitive impairments equally determine the functional outcome after SAH.
Table 3: Comparison of means of neuropsychological scores between patients and controls at six months after subarachnoid hemorrhage

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Table 4: Correlation between neurological and neurocognitive tests at six months after subarachnoid hemorrhage

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 » Discussion Top


Neurological deficits are not uncommon after SAH. Although the neurological impairment after SAH improves over time, it is still the major determinant of outcome.[18],[19],[20],[21] In our study, we found that patients with SAH had a significant neurological impairment at follow-up, even though the impairment was only mild-to-moderate. There was a significant correlation of neurological impairment, as scored by NIHSS, with the functional outcome, as assessed by GOSE. This indicates that neurological impairment is a significant determinant of functional outcome.

Although cognitive deficit after SAH is well-known, the neuropsychological outcome is underreported.[22],[23] The time course of cognitive recovery after SAH is heterogeneous.[24] It is recommended that the neuropsychological evaluation should be performed 3 months after SAH because patients are likely to improve with time.[25],[26] We conducted the neuropsychological assessment 6 months after SAH. We used a tailored test battery from our institute's comprehensive neuropsychological battery.[15] The tests used by us covered major domains of cognitive impairments seen in patients with SAH. We used a control group that was matched according to age, gender, and level of education. Instead of using a cut-off score for defining cognitive impairment, we used the absolute neuropsychological scores to correlate with functional outcome. We found that patients with SAH had a significant impairment of cognitive function as compared to controls. There was a significant correlation of neuropsychological test scores with GOSE and NIHSS. On reviewing the scores of various neuropsychological tests, we found that the impairments in attention and working memory are the main determinant of functional outcome after SAH.

The functional outcome after SAH has been reported using various outcome assessment tools.[22],[23],[27] The WFNS proposed the use of GOS for assessing patient outcomes after SAH.[8] We preferred the extended version of GOS, i.e. GOSE to determine the functional outcome in our patients. We also used a structured questionnaire to reduce misclassification of GOSE. Although the patients had significant neurological and cognitive impairment, most of the patients had a favourable outcome. Though there are many studies reporting neurological and cognitive impairment after SAH, we found only one study that took into consideration confounding factors, neurological impairment and depression, to assess cognitive functions.[28] In this study, the authors concluded that the functional outcome after SAH is affected by both neurological and cognitive deficits, and cognitive deficits irrespective of neurological deficits also affect the outcome. We found that both cognitive impairment and neurological deficits correlated equally well with functional outcome.

Limitations

The major limitation of this study is that a significant proportion of patients were lost to follow-up. As the primary aim of our study was to compare two forms of impairments, the lack of follow-up may not be a significant factor interfering with the results. The second limitation was that we did not take into consideration other factors such as mood, anxiety, sleep, fatigue, and the method of securing the aneurysm (e.g., clipping or coiling) that can influence the outcome.[23] These factors may not affect neurological examination but can definitely affect neuropsychological assessment. Few of our patients could not complete all the tests because of various reasons. We do not know whether or not, after adjustment of the above factors, there would be a difference in neuropsychological test results. Third, our study comprised patients with a good clinical grade (WFNS I and II). Patients with poor grade SAH are more likely to have severe neurological deficits, and in such circumstances, many patients cannot complete the neuropsychological assessment.


 » Conclusion Top


In the present study, we prospectively studied patients with SAH to determine their neurological, cognitive, and functional outcome using the NIHSS, neuropsychological, and GOSE scores. The patients had significant neurological and cognitive impairment as compared to the control group. The cognitive domains affected were attention, mental flexibility, visual working memory, verbal fluency, response inhibition, visual constructive ability, and visual memory. The profile of deficits indicates the involvement of diffuse areas of brain, particularly the premotor, prefrontal, and medial inferior frontal lobes. At 6 months, both neurological and cognitive impairment equally contributed to the functional outcome, as assessed by GOSE.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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