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|Year : 2018 | Volume
| Issue : 6 | Page : 1713-1717
Neurological, neuropsychological, and functional outcome after good grade aneurysmal subarachnoid hemorrhage
Subir Dey1, J Keshav Kumar2, Dhaval Shukla1, Dhananjaya Bhat1
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 Publication||28-Nov-2018|
Dr. Dhaval Shukla
Department of Neurosurgery, National Institute of Mental Health and Neurosciences, Bengaluru - 560 029, Karnataka
Source of Support: None, Conflict of Interest: None
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 2021 Jun 24];66:1713-7. Available from: https://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. Studies have shown that 15–20% of the patients die before reaching the hospital, and another 20–25% die within the first 48 hours., The 30-day mortality is as high as 50%. 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. In spite of this, the long-term outcome is still poor, with 30% of the survivors remaining dependent on others. 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). 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. Cognitive difficulties including attention, planning, and reasoning impairment after SAH affect the patient's ability to return to work. 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. 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.,,,,
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|| |
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. Neuropsychological assessment was done using tailored NIMHANS Neuropsychology Test Battery to quantify neurocognitive deficits. 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., 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.
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|| |
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|| |
Neurological deficits are not uncommon after SAH. Although the neurological impairment after SAH improves over time, it is still the major determinant of outcome.,,, 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., The time course of cognitive recovery after SAH is heterogeneous. It is recommended that the neuropsychological evaluation should be performed 3 months after SAH because patients are likely to improve with time., We conducted the neuropsychological assessment 6 months after SAH. We used a tailored test battery from our institute's comprehensive neuropsychological battery. 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.,, The WFNS proposed the use of GOS for assessing patient outcomes after SAH. 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. 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.
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. 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|| |
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.
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Conflicts of interest
There are no conflicts of interest.
| » References|| |
Le Roux PD, Winn HR. Management of the ruptured aneurysm. Neurosurg Clin N Am 1998;9:525-40.
Schievink WI, Wijdicks EF, Piepgras DG, Chu CP, O'Fallon WM, Whisnant JP. The poor prognosis of ruptured intracranial aneurysms of the posterior circulation. J Neurosurg 1995;82:791-5.
Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 1994;25:1342-7.
Lovelock CE, Rinkel GJ, Rothwell PM. Time trends in outcome of subarachnoid hemorrhage: Population-based study and systematic review. Neurology 2010;11;74:1494-501.
van GJ, Rinkel GJ. Subarachnoid hemorrhage: Diagnosis, causes and management. Brain 2001;124:249-78.
Michael C, Tranel D. Neuroscience in Medicine 2nd
Ed. Totowa, NJ, USA: Humana Press; 2003. p. 621-35.
Wermer MJ, Kool H, Albrecht KW, Rinkel GJ; Aneurysm Screening after Treatment for Ruptured Aneurysms Study Group. Subarachnoid hemorrhage treated with clipping: Long-term effects on employment, relationships, personality, and mood. Neurosurgery 2007;60:91-7.
Drake CG, Hunt WE, Sano K, Kessel N, Pertuiset B, de Villers JC. Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg 1988;68:985-6.
Shukla D, Devi BI, Agrawal A. Outcome measures for traumatic brain injury. Clin Neurol Neurosurg 2011;113:435-41.
Wilson JT, Pettigrew LE, Teasdale GM. Emotional and cognitive consequences of head injury in relation to the Glasgow Outcome Scale. J Neurol Neurosurg Psychiatry 2001;70:267-8.
Levin HS, Boake C, Song J, Mccauley S, Contant C, Diaz-Marchan P, et al
. Validity and sensitivity to change of the extended Glasgow Outcome Scale in mild to moderate traumatic brain injury. J Neurotrauma 2001;18:575-84.
Clifton GL, Kreutzer JS, Choi SC, Devany CW, Eisenberg HM, Foulkes MA, et al
. Relationship between Glasgow Outcome Scale and neuropsychological measures after brain injury. Neurosurgery 1993;33:34-9.
Satz P, Zaucha K, Forney DL, McCleary C, Asarnow RF, Light R, et al
. Neuropsychological, psychosocial and vocational correlates of the Glasgow Outcome Scale at 6 months post-injury: A study of moderate to severe traumatic brain injury patients. Brain Inj 1998;12:555-67.
Rao SL, Subbukrishna DK, Gopal Kumar K. NIMHANS neuropsychology battery manual. Bangalore: NIMHANS publication; 2004.
Pettigrew EL, Wilson JT, Teasdale G. Assessing disability after head injury: Improved use of the Glasgow Outcome Scale. J Neurosurg 1998;89:939-43.
Lu J, Marmarou A, Lapane K, Turf E, Wilson L; IMPACT Group; American Brain Injury Consortium Study Participation Centers. A method for reducing misclassification in the extended Glasgow outcome score. J Neurotrauma 2010;27:843-52.
Bulters DO, Santarius T, Chia HL, Parker RA, Trivedi R, Kirkpatrick PJ, et al
. Causes of neurological deficits following clipping of 200 consecutive ruptured aneurysms in patients with good-grade aneurysmal subarachnoid hemorrhage. Acta Neurochir 2011;153:295-303.
Ogden JA, Mee EW, Henning M. A prospective study of impairment of cognition, memory, and recovery after subarachnoid hemorrhage. Neurosurgery 1993;33:572-87.
Cedzich C, Roth A. Neurological and psychosocial outcome after subarachnoid hemorrhage, and the Hunt and Hess scale as a predictor of clinical outcome. Zentralbl Neurochir 2005;66:112-8.
Mahaney KB, Todd MM, Bayman EO, Torner JC; IHAST Investigators. Acute postoperative neurological deterioration associated with surgery for ruptured intracranial aneurysm: Incidence, predictors, and outcomes. J Neurosurg 2012;116:1267-78.
Stienen MN, Weisshaupt R, Fandino J, Fung C, Keller E, Hildebrandt G, et al
. Current practice in neuropsychological outcome reporting after aneurysmal subarachnoid hemorrhage. Acta Neurochir 2013;155:2045-51.
Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010;41:e519-36.
Haug T, Sorteberg A, Sorteberg W, Lindegaard KF, Lundar T, Finset A. Cognitive outcome after aneurysmal subarachnoid hemorrhage: Time course of recovery and relationship to clinical, radiological, and management parameters. Neurosurgery 2007;60:649-57.
Suarez JI. Timing of neuropsychological outcome measures in patients with subarachnoid hemorrhage. Stroke 2007;38:1724-5.
Hutter BO, Kreitschmann-Andermahr I, Gilsbach JM. Cognitive deficits in the acute stage after subarachnoid hemorrhage. Neurosurgery 1998;43:1054-65.
Huetter BO, Gilsbach JM, Kreitschmann I. Quality of life and cognitive deficits after subarachnoid hemorrhage. Br J Neurosurg 1995;9:465-75.
Wong GKC, Lam SW, Ngai K, Wong A, Siu D, Poon WS, et al
. Cognitive Dysfunction after Aneurysmal Subarachnoid Hemorrhage Investigators. Cognitive domain deficits in patients with aneurysmal subarachnoid hemorrhage at 1 year. J Neurol Neurosurg Psychiatry 2013;84:1054-8.
[Table 1], [Table 2], [Table 3], [Table 4]