Original Article
Fisher Grading Scale Associated with Language Disorders in Patients with Anterior Circulation Aneurysmal Subarachnoid Hemorrhage Moyse´s Loiola Ponte de Souza1-3, Ana Cla´udia C. Vieira4, Gustavo Andrade2, Saul Quinino1,3, Maria de Fa´tima Leal Griz1, Hildo R. C. Azevedo-Filho1,3
OBJECTIVE: To associate the presence of language deficits with varying scores of the Fisher grading scale in patients with subarachnoid hemorrhage in the period preceding the treatment of aneurysm in the anterior circulation, as well as to compare the scores of this scale, identifying the grades more associated with the decline of language.
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METHODS: Database analysis of 185 preoperative evaluations of language, through the Montreal Toulouse Protocol Alpha version and verbal fluency through CERAD battery, of patients from “Hospital da Restauração” with aneurysmal subarachnoid hemorrhage, divided according to the Fisher grading scale (Fisher I, II, III, or IV) and compared with a control group of individuals considered normal.
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RESULTS: The various scores of the Fisher grading scale have different levels of language deficits, more pronounced as the amount of blood increases. Fisher III and IV scores are most associated with the decline of language.
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CONCLUSIONS: Our study made it possible to obtain information not yet available in the literature, by correlating the various scores of the Fisher grading scale with language yet in the period preceding treatment.
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Because it affects a younger population, the proportion of the potential of years of life lost in patients with aSAH is equivalent to that of the patients with ischemic stroke and intracerebral hematomas (13). Despite advances in the treatment of cerebral aneurysm and the prevention of secondary complications of aSAH, about one third of survivors remain dependent (9). Even patients considered with favorable neurologic recovery (i.e., with Glasgow Outcome Scale 4, “moderate disability” or 5, “good recovery,” 6 and 24 months after the aSAH), about 76% of them showed worsening in verbal and semantic fluency (19), and the presence of blood in the subarachnoid space possibly provides alterations in higher cerebral functions (24). Our group (2012) demonstrated cognitive worsening when comparing the assessments in the pretreatment and post-treatment period through paired analysis, proving the deleterious effect of open surgery in the functions of language and memory (26). After establishing the treatment of cerebral aneurysm, the Fisher grading scale (FGS) has been listed as the most important factor of language alterations (5, 11). The objective of this research is to associate the presence of language deficits with the FGS (Table 1), by comparing and identifying the scores more associated with the decline of language in patients with anterior circulation aSAH in the period preceding the treatment of the aneurysm. MATERIAL AND METHODS
INTRODUCTION
A
neurysmal subarachnoid hemorrhage (aSAH) has a high mortality: Approximately 12% of patients die at the exact moment of rupture of cerebral aneurysm (10), and around 30%e40% at 30 days after bleeding (17).
Key words Computed tomography - Fisher scale - Intracranial aneurysm - Neuropsychological assessment - Subarachnoid hemorrhage -
Abbreviations and Acronyms aSAH: Aneurysmal subarachnoid hemorrhage CERAD: Consortium to Establish a Registry for Alzheimer’s Disease FGS: Fisher grading scale HR: Hospital da Restauração
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This study had cross-sectional retrospective analytical design, which used a database with cognitive assessments of 193 patients with anterior circulation aSAH confirmed by digital angiography in the period from March 2007 to November 2009 who were admitted to the emergency department of Hospital da Restauração (HR). Patients with Hunt Hess Scale scores of higher than III,
From the Departments of 1Neurosurgery and 2Interventional Neuroradiology, Hospital da Restauração, Recife, Brazil; and Departments of 3Neuropsychiatry and Behavioral Sciences and 4Phonoaudiology, Federal University of Pernambuco, Pernambuco, Brazil To whom correspondence should be addressed: Moysés Loiola Ponte de Souza, M.D., M.Sc. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 2:308-313. http://dx.doi.org/10.1016/j.wneu.2015.03.017 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.03.017
ORIGINAL ARTICLE MOYSÉS LOIOLA PONTE DE SOUZA ET AL.
FGS IN PATIENTS WITH ANTERIOR CIRCULATION ASAH
Table 1. Description of Fisher Grading Scale, Fisher et al., 1980 (5) Grade
Descriptions
Fisher I
No blood detected
Fisher II
Diffuse deposition or thin layer with all vertical layers of blood (interhemispheric fissure, insular cistern, ambient cistern) < 1 mm thick
Fisher III
Localized clots and/or vertical layers of blood 1 mm in thickness
Fisher IV
Diffuse or no subarachnoid blood, but with intracerebral or intraventricular clots
aphasics, and those older than 75 years (25) were excluded and, once removed from the study, not evaluated again. Data relating to the FGS, location of the aneurysm, age, and gender of patients were obtained through a review of medical records after being released by the Board of Ethics (CAAE no. 03890412.8.0000.5198), with the exception that the language assessments would not interfere with the establishment of the definitive treatment of the cerebral aneurysm (surgery or embolization). By convention, when necessary, analysis of the Fisher I was held together with the Fisher II and the Fisher III with the Fisher IV, being those new subgroups designated as Fisher I þ II and Fisher III þ IV, respectively. The analyses were compared with a control group of individuals considered normal. This group of volunteers was formed from the collaboration of accompanying people of patients admitted to the hospital. The individuals underwent the following tests: MontrealToulouse Protocol: Aphasia Examination, Initial Standard Module Alpha Version (16); tests of verbal, semantic, and phonological
fluency used in the CERAD (Consortium to Establish a Registry for Alzheimer disease) battery (1); and semantic fluency for fruits and Edinburgh handedness inventory have been added (20), being the evaluations carried out at least 8 days after the onset of the first symptoms. The results were expressed in percentage and statistical measures: mean, median, and standard deviation. The Shapiro Wilk normality test for quantitative variables with verification of the hypothesis of equality of variances was performed using Levene’s Test F. For the comparison between groups regarding categorical variables, Pearson’s chi-square test was used. Student t test (normal distribution) and Mann-Whitney (non-normal distribution) were used for numeric variables when analyzing two groups. In the case of comparing more than two groups or categories, the F test (Anova) (normal distribution) was applied, followed by comparisons of Tukey or Tamhane, or Kruskal-Wallis test (nonnormal distribution). The margin of error used in decisions of the statistical tests was 5%. The program used for data entry and obtention of statistical calculations was SPSS (Statistical Package for Social Sciences) version 17. RESULTS Three patients were excluded from the initial sample due to the lack of registration in the score range of FGS, and five patients for having more than one register, leaving 185 patients for the further analyses. Regarding the location of the aneurysm, the highest frequency corresponded: anterior communicating artery (34%), middle cerebral artery (23.8%), and posterior communicating artery (22.7%). As for handedness, the majority (90.8%) had right-handedness. The percentage of the subgroups found in the FGS was 21.6% in the Fisher I, 17.8% in the Fisher II, 38.4% in the Fisher III, and 22.2% in the Fisher IV. In Table 2, the following characteristics were analyzed: age, gender, and number of years of education. From this table, it
Table 2. Evaluation of Characteristics (Age, Gender, and Educational Level) According to Fisher Grading Scale and Control Group Types Variables
Control (n [ 63)
Fisher I (n [ 40)
Fisher II (n [ 33)
Fisher III (n [ 71)
Fisher IV (n [ 41)
P Value
Age (years)
44.03 16.65
46.63 12.28
48.21 12.78
50.49 12.37
49.49 9.08
0.059* 0.273y
50 years
43 (68.3%)
28 (70%)
20 (60.6%)
37 (52.1%)
26 (63.4%)
>50 years
20 (31.7%)
12 (30%)
13 (39.4%)
34 (47.9%)
15 (36.6%)
Male
11 (17.5%)
13 (32.5%)
11 (33.3%)
23 (32.4%)
14 (34.1%)
Female
52 (82.5%)
27 (67.5%)
22 (66.7%)
48 (67.6%)
27 (65.9%)
4.60 5.13
5.78 4.19
5.09 4.82
5.27 4.71
3.58 3.56
Gender
Educational level (years)
0.237y 0.169z
*Anova test. yPearson’s chi-square test. zKruskal-Wallis test.
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Table 3. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Patients with Aneurysmal Subarachnoid Hemorrhage and Control Group Types Variables Oral comprehension (maximum score ¼ 11)
Control (n [ 63)
aSAH (n [ 185)
9.66 1.26
8.82 2.13
0.001*
P Value
Repetition (maximum score ¼ 11)
10.10 0.81
9.92 1.59
0.437*
Naming (maximum score ¼ 12)
11.46 0.61
10.87 2.23
0.002*
Written comprehension (maximum score ¼ 11)
10.53 0.77
8.49 2.60
< 0.001*
Oral reading (maximum score ¼ 11)
10.89 0.46
9.53 2.72
< 0.001*
Semantic fluency (animals)
17.00 4.97
10.50 4.76
< 0.001*
Semantic fluency (fruits)
15.62 2.14
9.77 4.26
< 0.001*
Phonologic fluency
14.57 4.67
8.49 4.97
< 0.001*
*Student t test. Values in bold are significant.
can be seen that for the fixed margin of error (5.0%), there are no statistically significant differences between the control group and Fisher I, II, III, and IV groups, with a higher percentage of female gender and patients aged younger than 50 years. In the language tests of Montreal-Toulouse Protocol and verbal fluency of CERAD, the mean of patients with aSAH was correspondingly lower than that of the control group and, except by the performance on the task of repetition, significant differences are proved for all other criteria (Table 3). When separately comparing all different scores of the FGS (Table 4), it can be seen that patients with Fisher III and IV scores had lower scores than the control group at all assessments and were not statistically significant only in the study of repetition (Fisher III and IV) and naming (Fisher III). Only in the criteria of naming and semantic fluency of animals and fruits patients with Fisher IV escores were statistically different of Fisher III.
Fisher I and II subgroups showed means statistically different from the control group only in the fluency tests (semantic and phonological). Through the tests of multiple pairwise comparisons of the written comprehension criterion, a significant difference between the subgroup Fisher I and the control group (P ¼ 0.003) is proved, but not between the subgroups Fisher I and II (P > 0.05). In Table 5 the subgroups Fisher I þ II and Fisher III þ IV were analyzed, and significant differences were found between Fisher I þ II and the control group in the criteria of written comprehension, reading, and fluency tests (semantic and phonological), as well as between Fisher III þ IV and the control group in all performed tests, except the analysis of repetition. When comparing the data of Fisher I þ II with Fisher III þ IV, it can be seen that the last group has lower scores on all evaluations and that statistical significance was found between the groups in
Table 4. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Fisher Grading Subgroups (I, II, III, or IV) and Control Group Types Control (n [ 63) Fisher I (n [ 40) Fisher II (n [ 33) Fisher III (n [ 71) Fisher IV (n [ 41) P Value*
Variables Oral comprehensiony (maximum score ¼ 11)
9.66 1.26a
9.70 1.22a
8.97 1.96ab
8.75 2.23b
7.95 2.46b
0.001
Repetition (maximum score ¼ 11)
10.10 0.81
10.40 0.81
10.06 1.14
9.83 1.70
9.49 2.10
0.057
Namingy (maximum score ¼ 12)
11.46 0.61a
11.50 0.68a
11.09 1.53ab
11.00 1.96a
9.85 3.51b
0.001
10.53 0.77
8.78 2.30
9.05 2.38
8.75 2.10
7.08 3.60
0.001
Oral reading (maximum score ¼ 11)
10.89 0.46
10.19 2.17
9.67 2.59
9.65 2.44
b
8.32 3.65
0.014
Semantic fluency (animals)z
17.00 4.97a
12.10 3.82b
11.73 5.20b
10.52 4.60b
7.90 4.53c
0.001
Semantic fluency (fruits)
15.62 2.14
11.56 3.88
10.27 3.93
9.94 3.72
c
7.34 3.92
0.001
Phonologic fluencyz
14.57 4.67a
10.28 5.39b
8.25 4.58bc
5.80 3.94c
0.001
y
Written comprehension (maximum score ¼ 11) y
y
a a
a
b ab
b
ab ab
b
9.55 5.18bc
b b
b
b
If all letters in superscript are distinct, it demonstrates a significant difference between the corresponding groups by paired comparisons of yTamhane’s T2 test or zTukey test. *Anova test. Values in bold are significant.
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FGS IN PATIENTS WITH ANTERIOR CIRCULATION ASAH
Table 5. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Fisher Grading Subgroups (I þ II or III þ IV) and Control Group Control (n [ 63)
Variables Oral comprehensiony (maximum score ¼ 11)
Control vs. Fisher I D II (P Value)*
Fisher I D II (n [ 73)
Control vs. Fisher III D IV (P Value)*
Fisher III D IV (n [ 112)
Fisher I D II vs. Fisher III D IV (P Value)*
9.66 1.26
0.607
9.37 1.63
< 0.001
8.46 2.34
0.006
Repetition (maximum score ¼ 11)
10.10 0.81
0.750
10.25 0.98
0.174
9.71 1.85
0.031
Namingy (maximum score ¼ 12)
11.46 0.61
0.748
11.32 1.15
0.004
10.58 2.68
0.033
Written comprehensiony (maximum score ¼ 11)
10.53 0.77
< 0.001
8.89 2.31
< 0.001
8.22 2.77
0.355
Oral readingy (maximum score ¼ 11)
10.89 0.46
0.028
9.98 2.34
< 0.001
9.22 2.93
0.284
17.00 4.97
< 0.001
11.93 4.47
< 0.001
9.56 4.73
0.003
15.62 2.14
< 0.001
10.97 4.41
< 0.001
8.98 3.98
0.007
14.57 4.67
0.001
9.98 5.27
< 0.001
7.46 4.51
0.010
Semantic fluency (animals)z y
Semantic fluency (fruits) z
Phonologic fluency
y
z
*Anova test followed by Tamhane’s T2 test or Tukey test. Values in bold are significant.
the study of oral comprehension, repetition, naming, and fluency tests (semantic and phonological). It is emphasized that the analysis of repetition, which had not demonstrated statistical difference in previous evaluations, showed significant difference between the groups Fisher I þ II and Fisher III þ IV (P ¼ 0.031). DISCUSSION This study aimed to try to correlate the amount of blood identified on brain tomography with the development of language disorders in patients with aSAH secondary to ruptured aneurysms in the anterior circulation. The association between the FGS and the language performance in the period preceding the surgery or embolization had not yet been performed in the literature due to the need for early treatment. We are aware that the sample of this study does not represent the totality of patients with aSAH assisted in HR because some of them have not had clinical conditions or were removed from the study by the exclusion criterion. The study of Cheng, Shi, and Zhou (2006) corroborates our difficulty because 24% of its initial sample did not complete the neuropsychological evaluations due to bad clinical conditions (3). FGS has several limitations: Patients with higher scores do not have a higher risk of developing vasospasm because Fisher III is the most associated with this phenomenon (5); it does not make a distinction between patients with cisternal aSAH and intraventricular hemorrhage, which makes a difference in the development of vasospasm (4, 7, 18), and it also does not consider the density and clot clearance rate (6, 21). By using the method proposed by Hijdra et al. (1990), which ranks the hematic densities in 10 cisterns/fissures and in the four ventricles
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(8), Kreiter et al. (2002) showed, although not demonstrating that higher scores were associated with cognitive changes, the presence of blood in the interhemispheric fissure and sylvian fissures was associated with cognitive decline (15). However, Caeiro et al. (2011) showed that the amount of hematic density was not associated with neuropsychiatric disorders (2). Our results show that both groups of patients with Fisher III and Fisher IV have worse scores on all evaluations performed, being statistically significant in seven of eight tests for the Fisher IV group (excluding repetition) and in six of the eight tests for the Fisher III group (except repetition and naming). The greater impairment of the Fisher IV group was also found by Rincon et al. (2010), who showed as risk factors for developing hydrocephalus requiring shunting: admission tomography with bicaudate index of at least 0.20, fourth ventricle hemorrhage or Fisher IV, initial glucose of at least 126 mg/dL, and nosocomial meningitis (22). The lower scores in the FGS (Fisher I and II) were associated with a decline in language only in the fluency criteria, denoting the greatest influence of this factor even in the presence of minor amount of bleeding. Hutter et al. (2001) compared patients with minimal/mild aSAH (Fisher I and II) with moderate/severe aSAH (Fisher III and IV), showing that those with major bleeding had worse ratings regarding the quality of life (12). Thus we decided to carry out the analysis of the Fisher I together with the Fisher II and the Fisher III with the Fisher IV. The subgroup Fisher III þ IV showed lower scores in all assessments, which was statistically significant compared with the control group in seven of the eight tests (excluding repetition) and, in relation to Fisher I þ II, in six of the eight tests (except written comprehension and reading).
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Vilkki et al. (2004) correlated the severity of aSAH with some cognitive deficits, which confirmed that patients with a thick (>1 mm) layer of subarachnoid blood in vertical cisterns are associated with the presence of cerebral infarction and decline in test of executive functioning, although no differences have been found in some questionnaires (27). Wong et al. (2012) demonstrated that, after 3 months of aSAH, 73% of the patients had cognitive decline when using the Montreal Cognitive Assessment (28). When analyzing data of this study, it is shown that 100% of the patients had scores III or IV in the FGS, making impossible the association between this scale and cognitive deficits. On the other hand, in the study of Krajewski et al. (2014) it is evident that 78% of patients with aSAH had scores I or II in the FGS (14) and there were no differences in ratings among any groups of the scale. Sheldon et al. (2013) showed significant difference in working memory between patients with aSAH and individuals considered normal (23). However, it was not possible to differentiate among the subgroups of the FGS, probably due to the small sample of patients with aSAH (21 patients).
REFERENCES
Our sample of 185 patients made it possible for us to obtain information not yet available in the literature, by correlating the various scores of the FGS with language disorders in individuals with aSAH secondary to ruptured aneurysms of the anterior circulation in the period preceding treatment. This was because several studies in the literature have not carried out language tests or have shown no differences between the scores of the FGS by inadequacy in the size or in the uniform distribution of the subgroups of the sample. CONCLUSIONS The FGS, originally created to foresee vasospasm development, did not have a direct association, being grade III worse than grade IV (5). Nevertheless, for language disorders after anterior circulation aSAH, the FGS had a direct correlation, with Fisher III and IV the most associated with language decline in the period preceding the treatment, thus making it possible to inform the patient and family of the chance for greater cognitive impairment and encourage the early initiation of rehabilitation.
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2. Caeiro L, Santos CO, Ferro JM, Figueira ML: Neuropsychiatric disturbances in acute subarachnoid haemorrhage. Eur J Neurol 18:857-864, 2011.
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3. Cheng H, Shi J, Zhou M: Cognitive assessment in Chinese patients with aneurysmal subarachnoid hemorrhage. Behav Neurol 17:117-120, 2006. 4. Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA: Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher Scale revisited. Stroke 32: 2012-2020, 2001. 5. Fisher CM, Kistler JP, Davis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1-9, 1980. 6. Fujita S: Computed tomographic grading with Hounsfield number related to delayed vasospasm in cases of ruptured cerebral aneurysm. Neurosurgery 17:609-612, 1985. 7. Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, van Crevel H: Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke 19: 1250-1256, 1988. 8. Hijdra A, Brouwers PJ, Vermeulen M, van Gijn J: Grading the amount of blood on computed tomograms after subarachnoid haemorrhage. Stroke 21:1156-1161, 1990. 9. Hop JW, Rinkel GJ, Algra A, van Gijn J: Casefatality rates and functional outcome after
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12. Hütter BO, Kreitschmann-Andermahr I, Gilsbach JM: Health-related quality of life after aneurysmal subarachnoid hemorrhage: impacts of bleeding severity, computerized tomography findings, surgery, vasospasm, and neurological grade. J Neurosurg 94:241-251, 2001. 13. Johnston SC, Selvin S, Gress DR: The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology 50:1413-1418, 1998. 14. Krajewski K, Dombek S, Martens T, Köppen J, Westphal M, Regelsberger J: Neuropsychological assessments in patients with aneurysmal subarachnoid hemorrhage, perimesencephalic SAH, and incidental aneurysms. Neurosurg Rev 37: 55-62, 2014. 15. Kreiter KT, Copeland D, Bernardini GL, Bates JE, Peery S, Claassen J, Du YE, Stern Y, Connolly ES, Mayer SA: Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 33:200-208, 2002. 16. Lecours AR, Mehler J, Parente MA, Caldeira A, Cary L, Castro MJ, Dehaut F, Delgado R, Gurd J, Karmann DF, Jakubovitz R, Osorio Z, Cabral LS, Junqueira AMS: Illiteracy and brain damage—1. Aphasia testing in culturally contrasted populations (control subjects). Neuropsychologia 25: 231-245, 1987.
17. Longstreth WT Jr, Nelson LM, Koepsell TD, van Belle G: Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington. Neurology 43: 712-718, 1993. 18. Macdonald RL, Rosengart A, Huo D, Karrison T: Factors associated with the development of vasospasm after planned surgical treatment of aneurysmal subarachnoid hemorrhage. J Neurosurg 99: 644-652, 2003. 19. Mavaddat N, Sahakian BJ, Hutchinson PJ, Kirkpatrick PJ: Cognition following subarachnoid hemorrhage from anterior communicating artery aneurysm: relation to timing of surgery. J Neurosurg 91:402-407, 1999. 20. Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113, 1971. 21. Reilly C, Amidei C, Tolentino J, Jahromi BS, Macdonald RL: Clot volume and clearance rate as independent predictors of vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 101:255-261, 2004. 22. Rincon F, Gordon E, Starke RM, Buitrago MM, Fernandez A, Schmidt JM, Claassen J, Wartenberg KE, Frontera J, Seder DB, Palestrant D, Connolly ES, Lee K, Mayer SA, Badjatia N: Predictors of long-term shuntdependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 113:774-780, 2010. 23. Sheldon S, Macdonald RL, Cusimano M, Spears J, Schweizer TA: Long-term consequences of subarachnoid hemorrhage: examining working memory. J Neurol Sci 332:145-147, 2013. 24. Sonesson B, Säveland H, Ljunggren B, Brandt L: Cognitive functioning after subarachnoid haemorrhage of unknown origin. Acta Neurol Scand 80:400-410, 1989.
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Received 21 August 2014; accepted 11 March 2015 Citation: World Neurosurg. (2015) 84, 2:308-313. http://dx.doi.org/10.1016/j.wneu.2015.03.017 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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Fisher Grading Scale Associated with Language Disorders in Patients with Anterior Circulation Aneurysmal Subarachnoid Hemorrhage Moyse´s Loiola Ponte de Souza1-3, Ana Cla´udia C. Vieira4, Gustavo Andrade2, Saul Quinino1,3, Maria de Fa´tima Leal Griz1, Hildo R. C. Azevedo-Filho1,3
OBJECTIVE: To associate the presence of language deficits with varying scores of the Fisher grading scale in patients with subarachnoid hemorrhage in the period preceding the treatment of aneurysm in the anterior circulation, as well as to compare the scores of this scale, identifying the grades more associated with the decline of language.
-
METHODS: Database analysis of 185 preoperative evaluations of language, through the Montreal Toulouse Protocol Alpha version and verbal fluency through CERAD battery, of patients from “Hospital da Restauração” with aneurysmal subarachnoid hemorrhage, divided according to the Fisher grading scale (Fisher I, II, III, or IV) and compared with a control group of individuals considered normal.
-
RESULTS: The various scores of the Fisher grading scale have different levels of language deficits, more pronounced as the amount of blood increases. Fisher III and IV scores are most associated with the decline of language.
-
CONCLUSIONS: Our study made it possible to obtain information not yet available in the literature, by correlating the various scores of the Fisher grading scale with language yet in the period preceding treatment.
-
Because it affects a younger population, the proportion of the potential of years of life lost in patients with aSAH is equivalent to that of the patients with ischemic stroke and intracerebral hematomas (13). Despite advances in the treatment of cerebral aneurysm and the prevention of secondary complications of aSAH, about one third of survivors remain dependent (9). Even patients considered with favorable neurologic recovery (i.e., with Glasgow Outcome Scale 4, “moderate disability” or 5, “good recovery,” 6 and 24 months after the aSAH), about 76% of them showed worsening in verbal and semantic fluency (19), and the presence of blood in the subarachnoid space possibly provides alterations in higher cerebral functions (24). Our group (2012) demonstrated cognitive worsening when comparing the assessments in the pretreatment and post-treatment period through paired analysis, proving the deleterious effect of open surgery in the functions of language and memory (26). After establishing the treatment of cerebral aneurysm, the Fisher grading scale (FGS) has been listed as the most important factor of language alterations (5, 11). The objective of this research is to associate the presence of language deficits with the FGS (Table 1), by comparing and identifying the scores more associated with the decline of language in patients with anterior circulation aSAH in the period preceding the treatment of the aneurysm. MATERIAL AND METHODS
INTRODUCTION
A
neurysmal subarachnoid hemorrhage (aSAH) has a high mortality: Approximately 12% of patients die at the exact moment of rupture of cerebral aneurysm (10), and around 30%e40% at 30 days after bleeding (17).
Key words Computed tomography - Fisher scale - Intracranial aneurysm - Neuropsychological assessment - Subarachnoid hemorrhage -
Abbreviations and Acronyms aSAH: Aneurysmal subarachnoid hemorrhage CERAD: Consortium to Establish a Registry for Alzheimer’s Disease FGS: Fisher grading scale HR: Hospital da Restauração
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This study had cross-sectional retrospective analytical design, which used a database with cognitive assessments of 193 patients with anterior circulation aSAH confirmed by digital angiography in the period from March 2007 to November 2009 who were admitted to the emergency department of Hospital da Restauração (HR). Patients with Hunt Hess Scale scores of higher than III,
From the Departments of 1Neurosurgery and 2Interventional Neuroradiology, Hospital da Restauração, Recife, Brazil; and Departments of 3Neuropsychiatry and Behavioral Sciences and 4Phonoaudiology, Federal University of Pernambuco, Pernambuco, Brazil To whom correspondence should be addressed: Moysés Loiola Ponte de Souza, M.D., M.Sc. [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 2:308-313. http://dx.doi.org/10.1016/j.wneu.2015.03.017 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE MOYSÉS LOIOLA PONTE DE SOUZA ET AL.
FGS IN PATIENTS WITH ANTERIOR CIRCULATION ASAH
Table 1. Description of Fisher Grading Scale, Fisher et al., 1980 (5) Grade
Descriptions
Fisher I
No blood detected
Fisher II
Diffuse deposition or thin layer with all vertical layers of blood (interhemispheric fissure, insular cistern, ambient cistern) < 1 mm thick
Fisher III
Localized clots and/or vertical layers of blood 1 mm in thickness
Fisher IV
Diffuse or no subarachnoid blood, but with intracerebral or intraventricular clots
aphasics, and those older than 75 years (25) were excluded and, once removed from the study, not evaluated again. Data relating to the FGS, location of the aneurysm, age, and gender of patients were obtained through a review of medical records after being released by the Board of Ethics (CAAE no. 03890412.8.0000.5198), with the exception that the language assessments would not interfere with the establishment of the definitive treatment of the cerebral aneurysm (surgery or embolization). By convention, when necessary, analysis of the Fisher I was held together with the Fisher II and the Fisher III with the Fisher IV, being those new subgroups designated as Fisher I þ II and Fisher III þ IV, respectively. The analyses were compared with a control group of individuals considered normal. This group of volunteers was formed from the collaboration of accompanying people of patients admitted to the hospital. The individuals underwent the following tests: MontrealToulouse Protocol: Aphasia Examination, Initial Standard Module Alpha Version (16); tests of verbal, semantic, and phonological
fluency used in the CERAD (Consortium to Establish a Registry for Alzheimer disease) battery (1); and semantic fluency for fruits and Edinburgh handedness inventory have been added (20), being the evaluations carried out at least 8 days after the onset of the first symptoms. The results were expressed in percentage and statistical measures: mean, median, and standard deviation. The Shapiro Wilk normality test for quantitative variables with verification of the hypothesis of equality of variances was performed using Levene’s Test F. For the comparison between groups regarding categorical variables, Pearson’s chi-square test was used. Student t test (normal distribution) and Mann-Whitney (non-normal distribution) were used for numeric variables when analyzing two groups. In the case of comparing more than two groups or categories, the F test (Anova) (normal distribution) was applied, followed by comparisons of Tukey or Tamhane, or Kruskal-Wallis test (nonnormal distribution). The margin of error used in decisions of the statistical tests was 5%. The program used for data entry and obtention of statistical calculations was SPSS (Statistical Package for Social Sciences) version 17. RESULTS Three patients were excluded from the initial sample due to the lack of registration in the score range of FGS, and five patients for having more than one register, leaving 185 patients for the further analyses. Regarding the location of the aneurysm, the highest frequency corresponded: anterior communicating artery (34%), middle cerebral artery (23.8%), and posterior communicating artery (22.7%). As for handedness, the majority (90.8%) had right-handedness. The percentage of the subgroups found in the FGS was 21.6% in the Fisher I, 17.8% in the Fisher II, 38.4% in the Fisher III, and 22.2% in the Fisher IV. In Table 2, the following characteristics were analyzed: age, gender, and number of years of education. From this table, it
Table 2. Evaluation of Characteristics (Age, Gender, and Educational Level) According to Fisher Grading Scale and Control Group Types Variables
Control (n [ 63)
Fisher I (n [ 40)
Fisher II (n [ 33)
Fisher III (n [ 71)
Fisher IV (n [ 41)
P Value
Age (years)
44.03 16.65
46.63 12.28
48.21 12.78
50.49 12.37
49.49 9.08
0.059* 0.273y
50 years
43 (68.3%)
28 (70%)
20 (60.6%)
37 (52.1%)
26 (63.4%)
>50 years
20 (31.7%)
12 (30%)
13 (39.4%)
34 (47.9%)
15 (36.6%)
Male
11 (17.5%)
13 (32.5%)
11 (33.3%)
23 (32.4%)
14 (34.1%)
Female
52 (82.5%)
27 (67.5%)
22 (66.7%)
48 (67.6%)
27 (65.9%)
4.60 5.13
5.78 4.19
5.09 4.82
5.27 4.71
3.58 3.56
Gender
Educational level (years)
0.237y 0.169z
*Anova test. yPearson’s chi-square test. zKruskal-Wallis test.
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Table 3. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Patients with Aneurysmal Subarachnoid Hemorrhage and Control Group Types Variables Oral comprehension (maximum score ¼ 11)
Control (n [ 63)
aSAH (n [ 185)
9.66 1.26
8.82 2.13
0.001*
P Value
Repetition (maximum score ¼ 11)
10.10 0.81
9.92 1.59
0.437*
Naming (maximum score ¼ 12)
11.46 0.61
10.87 2.23
0.002*
Written comprehension (maximum score ¼ 11)
10.53 0.77
8.49 2.60
< 0.001*
Oral reading (maximum score ¼ 11)
10.89 0.46
9.53 2.72
< 0.001*
Semantic fluency (animals)
17.00 4.97
10.50 4.76
< 0.001*
Semantic fluency (fruits)
15.62 2.14
9.77 4.26
< 0.001*
Phonologic fluency
14.57 4.67
8.49 4.97
< 0.001*
*Student t test. Values in bold are significant.
can be seen that for the fixed margin of error (5.0%), there are no statistically significant differences between the control group and Fisher I, II, III, and IV groups, with a higher percentage of female gender and patients aged younger than 50 years. In the language tests of Montreal-Toulouse Protocol and verbal fluency of CERAD, the mean of patients with aSAH was correspondingly lower than that of the control group and, except by the performance on the task of repetition, significant differences are proved for all other criteria (Table 3). When separately comparing all different scores of the FGS (Table 4), it can be seen that patients with Fisher III and IV scores had lower scores than the control group at all assessments and were not statistically significant only in the study of repetition (Fisher III and IV) and naming (Fisher III). Only in the criteria of naming and semantic fluency of animals and fruits patients with Fisher IV escores were statistically different of Fisher III.
Fisher I and II subgroups showed means statistically different from the control group only in the fluency tests (semantic and phonological). Through the tests of multiple pairwise comparisons of the written comprehension criterion, a significant difference between the subgroup Fisher I and the control group (P ¼ 0.003) is proved, but not between the subgroups Fisher I and II (P > 0.05). In Table 5 the subgroups Fisher I þ II and Fisher III þ IV were analyzed, and significant differences were found between Fisher I þ II and the control group in the criteria of written comprehension, reading, and fluency tests (semantic and phonological), as well as between Fisher III þ IV and the control group in all performed tests, except the analysis of repetition. When comparing the data of Fisher I þ II with Fisher III þ IV, it can be seen that the last group has lower scores on all evaluations and that statistical significance was found between the groups in
Table 4. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Fisher Grading Subgroups (I, II, III, or IV) and Control Group Types Control (n [ 63) Fisher I (n [ 40) Fisher II (n [ 33) Fisher III (n [ 71) Fisher IV (n [ 41) P Value*
Variables Oral comprehensiony (maximum score ¼ 11)
9.66 1.26a
9.70 1.22a
8.97 1.96ab
8.75 2.23b
7.95 2.46b
0.001
Repetition (maximum score ¼ 11)
10.10 0.81
10.40 0.81
10.06 1.14
9.83 1.70
9.49 2.10
0.057
Namingy (maximum score ¼ 12)
11.46 0.61a
11.50 0.68a
11.09 1.53ab
11.00 1.96a
9.85 3.51b
0.001
10.53 0.77
8.78 2.30
9.05 2.38
8.75 2.10
7.08 3.60
0.001
Oral reading (maximum score ¼ 11)
10.89 0.46
10.19 2.17
9.67 2.59
9.65 2.44
b
8.32 3.65
0.014
Semantic fluency (animals)z
17.00 4.97a
12.10 3.82b
11.73 5.20b
10.52 4.60b
7.90 4.53c
0.001
Semantic fluency (fruits)
15.62 2.14
11.56 3.88
10.27 3.93
9.94 3.72
c
7.34 3.92
0.001
Phonologic fluencyz
14.57 4.67a
10.28 5.39b
8.25 4.58bc
5.80 3.94c
0.001
y
Written comprehension (maximum score ¼ 11) y
y
a a
a
b ab
b
ab ab
b
9.55 5.18bc
b b
b
b
If all letters in superscript are distinct, it demonstrates a significant difference between the corresponding groups by paired comparisons of yTamhane’s T2 test or zTukey test. *Anova test. Values in bold are significant.
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Table 5. Performance of Montreal-Toulouse Protocol Language Tests and Consortium to Establish a Registry for Alzheimer’s Disease Verbal Tests of Fisher Grading Subgroups (I þ II or III þ IV) and Control Group Control (n [ 63)
Variables Oral comprehensiony (maximum score ¼ 11)
Control vs. Fisher I D II (P Value)*
Fisher I D II (n [ 73)
Control vs. Fisher III D IV (P Value)*
Fisher III D IV (n [ 112)
Fisher I D II vs. Fisher III D IV (P Value)*
9.66 1.26
0.607
9.37 1.63
< 0.001
8.46 2.34
0.006
Repetition (maximum score ¼ 11)
10.10 0.81
0.750
10.25 0.98
0.174
9.71 1.85
0.031
Namingy (maximum score ¼ 12)
11.46 0.61
0.748
11.32 1.15
0.004
10.58 2.68
0.033
Written comprehensiony (maximum score ¼ 11)
10.53 0.77
< 0.001
8.89 2.31
< 0.001
8.22 2.77
0.355
Oral readingy (maximum score ¼ 11)
10.89 0.46
0.028
9.98 2.34
< 0.001
9.22 2.93
0.284
17.00 4.97
< 0.001
11.93 4.47
< 0.001
9.56 4.73
0.003
15.62 2.14
< 0.001
10.97 4.41
< 0.001
8.98 3.98
0.007
14.57 4.67
0.001
9.98 5.27
< 0.001
7.46 4.51
0.010
Semantic fluency (animals)z y
Semantic fluency (fruits) z
Phonologic fluency
y
z
*Anova test followed by Tamhane’s T2 test or Tukey test. Values in bold are significant.
the study of oral comprehension, repetition, naming, and fluency tests (semantic and phonological). It is emphasized that the analysis of repetition, which had not demonstrated statistical difference in previous evaluations, showed significant difference between the groups Fisher I þ II and Fisher III þ IV (P ¼ 0.031). DISCUSSION This study aimed to try to correlate the amount of blood identified on brain tomography with the development of language disorders in patients with aSAH secondary to ruptured aneurysms in the anterior circulation. The association between the FGS and the language performance in the period preceding the surgery or embolization had not yet been performed in the literature due to the need for early treatment. We are aware that the sample of this study does not represent the totality of patients with aSAH assisted in HR because some of them have not had clinical conditions or were removed from the study by the exclusion criterion. The study of Cheng, Shi, and Zhou (2006) corroborates our difficulty because 24% of its initial sample did not complete the neuropsychological evaluations due to bad clinical conditions (3). FGS has several limitations: Patients with higher scores do not have a higher risk of developing vasospasm because Fisher III is the most associated with this phenomenon (5); it does not make a distinction between patients with cisternal aSAH and intraventricular hemorrhage, which makes a difference in the development of vasospasm (4, 7, 18), and it also does not consider the density and clot clearance rate (6, 21). By using the method proposed by Hijdra et al. (1990), which ranks the hematic densities in 10 cisterns/fissures and in the four ventricles
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(8), Kreiter et al. (2002) showed, although not demonstrating that higher scores were associated with cognitive changes, the presence of blood in the interhemispheric fissure and sylvian fissures was associated with cognitive decline (15). However, Caeiro et al. (2011) showed that the amount of hematic density was not associated with neuropsychiatric disorders (2). Our results show that both groups of patients with Fisher III and Fisher IV have worse scores on all evaluations performed, being statistically significant in seven of eight tests for the Fisher IV group (excluding repetition) and in six of the eight tests for the Fisher III group (except repetition and naming). The greater impairment of the Fisher IV group was also found by Rincon et al. (2010), who showed as risk factors for developing hydrocephalus requiring shunting: admission tomography with bicaudate index of at least 0.20, fourth ventricle hemorrhage or Fisher IV, initial glucose of at least 126 mg/dL, and nosocomial meningitis (22). The lower scores in the FGS (Fisher I and II) were associated with a decline in language only in the fluency criteria, denoting the greatest influence of this factor even in the presence of minor amount of bleeding. Hutter et al. (2001) compared patients with minimal/mild aSAH (Fisher I and II) with moderate/severe aSAH (Fisher III and IV), showing that those with major bleeding had worse ratings regarding the quality of life (12). Thus we decided to carry out the analysis of the Fisher I together with the Fisher II and the Fisher III with the Fisher IV. The subgroup Fisher III þ IV showed lower scores in all assessments, which was statistically significant compared with the control group in seven of the eight tests (excluding repetition) and, in relation to Fisher I þ II, in six of the eight tests (except written comprehension and reading).
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Vilkki et al. (2004) correlated the severity of aSAH with some cognitive deficits, which confirmed that patients with a thick (>1 mm) layer of subarachnoid blood in vertical cisterns are associated with the presence of cerebral infarction and decline in test of executive functioning, although no differences have been found in some questionnaires (27). Wong et al. (2012) demonstrated that, after 3 months of aSAH, 73% of the patients had cognitive decline when using the Montreal Cognitive Assessment (28). When analyzing data of this study, it is shown that 100% of the patients had scores III or IV in the FGS, making impossible the association between this scale and cognitive deficits. On the other hand, in the study of Krajewski et al. (2014) it is evident that 78% of patients with aSAH had scores I or II in the FGS (14) and there were no differences in ratings among any groups of the scale. Sheldon et al. (2013) showed significant difference in working memory between patients with aSAH and individuals considered normal (23). However, it was not possible to differentiate among the subgroups of the FGS, probably due to the small sample of patients with aSAH (21 patients).
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Our sample of 185 patients made it possible for us to obtain information not yet available in the literature, by correlating the various scores of the FGS with language disorders in individuals with aSAH secondary to ruptured aneurysms of the anterior circulation in the period preceding treatment. This was because several studies in the literature have not carried out language tests or have shown no differences between the scores of the FGS by inadequacy in the size or in the uniform distribution of the subgroups of the sample. CONCLUSIONS The FGS, originally created to foresee vasospasm development, did not have a direct association, being grade III worse than grade IV (5). Nevertheless, for language disorders after anterior circulation aSAH, the FGS had a direct correlation, with Fisher III and IV the most associated with language decline in the period preceding the treatment, thus making it possible to inform the patient and family of the chance for greater cognitive impairment and encourage the early initiation of rehabilitation.
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Received 21 August 2014; accepted 11 March 2015 Citation: World Neurosurg. (2015) 84, 2:308-313. http://dx.doi.org/10.1016/j.wneu.2015.03.017 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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