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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 1  |  Page : 120-127

Predictors of cerebral vasospasm after aneurysmal subarachnoid hemorrhage


1 Department of Neuropsychiatry, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neurology, Matarya Teaching Hospital, Cairo, Egypt

Date of Submission03-Sep-2021
Date of Decision10-Oct-2021
Date of Acceptance18-Oct-2021
Date of Web Publication18-Apr-2022

Correspondence Address:
Gelan M Salem
Department of Neuropsychiatry, University of Menoufia, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_159_21

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  Abstract 


Objectives
To assess computed tomography (CT) blood clot thickness, aneurysmal site and size as predictors for vasospasm after subarachnoid hemorrhage (SAH).
Background
Cerebral vasospasm and delayed cerebral ischemia are common factors of poor outcome following SAH.
Patients and methods
Forty patients with acute aneurysmal SAH. Outcome was assessed clinically by Glasgow coma scale, Hunt and Hess scale, radiologically by cerebral CT [modified Fisher's scale (MFS)], cerebral CT angiography, and transcranial Doppler (follow-up on the first, third, fifth, seventh, and tenth day from SAH onset) for the appearance of vasospasm.
Results
There is no significant difference between the amount of blood detected by CT (MFS) and cerebral aneurysm sites as U = 0.513, P = 0.972. Early vasospasm was detected in 13 cases in middle cerebral artery, seven cases anterior communicating, four posterior communicating, and the least was internal carotid and posterior cerebral (two cases and one case, respectively). Univariate logistic regression and receiver-operating characteristic curve showed that the predictors for vasospasm were systolic and diastolic blood pressure (DBP) (systolic blood pressure with diagnostic accuracy = area under the curve=[95% confidence interval (CI)=0.82, P = 0.0001, cutoff point >195 and DBP: 95% CI = 0.87, P = 0.0001, cutoff point >95 for DBP], hemoglobin A1C (95% CI = 0.89, P = 0.0001, cutoff point >7), Glasgow coma scale (95% CI = 0.80, P = 0.001, cutoff point <14), Hunt and Hess scale (95% CI = 0.80, P = 0.001, cutoff point >2), MFS (95% CI = 0.70, P = 0.045, cutoff point >1) and aneurysmal size (95% CI = 0.77, P = 0.0003, cutoff point >7) but aneurysmal site and smoking P = 0.995 and 0.99, respectively were not predictors in spite of association.
Conclusion
Clinical severity of SAH, blood clot thickness, aneurysmal size, systolic blood pressure and DBP, and glycated hemoglobin seem to be important predictors for cerebral vasospasm after SAH.

Keywords: cerebral vasospasm, modified Fisher's scale, subarachnoid hemorrhage


How to cite this article:
El Ahmar IE, Okda MA, Essa ES, Salem GM. Predictors of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Menoufia Med J 2022;35:120-7

How to cite this URL:
El Ahmar IE, Okda MA, Essa ES, Salem GM. Predictors of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Menoufia Med J [serial online] 2022 [cited 2024 Mar 29];35:120-7. Available from: http://www.mmj.eg.net/text.asp?2022/35/1/120/343105




  Introduction Top


Aneurysmal subarachnoid hemorrhage (aSAH) incidence approximates 8–11 per 100 000/year [1]. Several complications follow SAH such as rebreeding, vasospasm seizures, and hydrocephalus increasing the death rate to 50% at the first month after the onset of SAH [2]. There are six groups of aneurysmal location: vertebra basilar, internal carotid (IC), middle cerebral artery (MCA), anterior communicated (A.com) pericallosal and intradural [3]. Two-thirds of SAH patients show moderate vasospasm that follows rupture of intracranial aneurysm at least in one cerebral artery. Ischemia and cerebral infarction develops in half of these patients [4]. Cerebral vasospasm (CV) may be radiological or angiographic (early) or symptomatic (delayed ischemic neurological deficit) [2]. SAH is usually evaluated clinically by the Hunt and Hess scale (HHS) and radiologically by transcranial Doppler (TCD) and/or cerebral angiography as they may help early detection or confirmation of vasospasm [3]. TCD is a noninvasive method for assessing blood flow velocity through cerebral blood vessels by measuring the echoes of ultrasound waves moving transcranially through the cranium. So, TCD helps in the detection of critical episodes of decrement of blood and oxygen supply before permanent ischemic deficits occur [5].

Primary objectives of this study were assessment of the relationship between aneurysmal locations and both blood clot thickness and radiological vasospasm in SAH, and secondary objectives were assessed if blood clot thickness, aneurysm characters (site, size), vascular risk factors, and clinical picture could be predictors of radiological vasospasm.


  Patients and methods Top


This study was a prospective randomized study that was approved by the Ethics Committee of Faculty of Medicine, Menoufia University. Forty patients with aSAH were recruited from the neuro-stroke Intensive Care Unit of Neurology Department of Materia Teaching Hospital, Cairo, Egypt, during the period from 2018 to 2020. We exclude patients with decompensated systemic illness (e.g. hepatic, renal), past history of large or disabling stroke interfering with assessment scale, secondary causes of subarachnoid hemorrhage (SAH: e.g. traumatic, blood diseases, etc.) and patients with inaccessible temporal window for TCD assessment [Figure 1]. Written consents were taken from all participants.
Figure 1: A flowchart of included and excluded cases.

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All patients underwent history and general clinical examination with focus on age, sex, and past history of hypertension (HTN), diabetes, smoking, and systolic and diastolic blood pressures (SBP and DBP). Full neurological examination included admission Glasgow coma scale (GCS) score and HHS (which is five grades scale for SAH clinical severity: grade I: asymptomatic or minimal headache and slight nuchal rigidity, grade II: moderate to severe headache, nuchal rigidity, no neurological deficit other than cranial nerve palsy, grade III: drowsiness, confusion or mild focal deficit, grade IV: stupor, moderate to severe hemiparesis, and possibly early decerebrate rigidity and vegetative disturbances, grade V: deep coma, decerebrate rigidity).

Patients were diagnosed using noncontrast brain computed tomography (CT) scan and the extension of blood in the subarachnoid space was classified according to modified Fisher scale (MFS), which is a scale to assess the thickness of blood 0 = none, 1 = minimal SAH without intraventricular hamorrage (IVH), 2 = minimal SAH with intraventricular hamorrage (IVH), 3 = thick SAH without IVH, and 4 = thick SAH with intraventricular hamorrage (IVH).

Cerebral CT angiography was done to confirm aneurismal SAH and demonstrate the location, number, and size of the aneurysm and then compare the site of aneurysm and MFS. Initial laboratory investigations were performed as blood count, hepatic renal tests, lipid profile, bleeding profile, glycated hemoglobin (HbA1C), and serum electrolytes. Daily serial clinical evaluation of patients including GCS and HHS was done to detect early clinical manifestations of delayed cerebral ischemia (DCI) such as the decreased level of consciousness or any focal neurological deficit. TCD of intracranial arteries was done on the first, third, fifth, seventh, and tenth days of the onset of SAH. The mean flow velocity (MFV) of distal internal carotid artery (ICA), M1 segment of MCA, and anterior (ACA) and posterior cerebral arteries (PCA) were measured through transtemporal windows with phased array transducer of 1–3 MHz multifrequency. The ICA divides into the MCA and ACA at about 60 mm away from the probe. This bifurcation is one of the most important reference points for TCD. The C1 segment of ICA is at an insonation depth of between 60 and 64 mm. The M1 segment of MCA is insolated through the transtemporal window with the flow direction toward the probe at an insonation depth of 50–60 mm from the skull surface. The A1 segment of ACA is insonated by TCD between 65 and 80 mm with the probe directed anterosuperiorly. The P1 segment of PCA is insonated by TCD between 60 and 75 mm with the flow direction towards the probe. The criteria of vasospasm include the following: regarding MCA, the MFV less than 120 cm/s is a predictor of the absence of CV, whereas the MFV between 120 and 150 cm/s is indicative of mild-to-moderate CV; the MFV more than 150 cm/s is suggestive of severe CV; and MFV more than 200 cm/s is indicative of critical CV. Regarding the TCD of ACA, vasospasm is considered possible if MFV more than 90 cm/s, probable CV if MFV more than 110 cm/s, and definite CV if MFV more than 120 cm/s. Regarding the TCD of PCA, vasospasm is considered possible if MFV more than 60 cm/s, probable CV if MFV more than 80 cm/s, and definite CV if MFV more than 90 cm/s. Follow-up CT brain was performed with suspected vasospasm to detect vasospasm-associated DCI and exclude other causes of deterioration.

Our treatment protocol was nonsurgical. Patients maintained spontaneous breathing or with a face mask to maintain oxygen saturation more than 97%. The use of antihypertensive agents was indicated when the mean systolic pressure exceeds 140 mmHg. The first-line drug was beta-blockers and the second-line drug is angiotensin converting enzymes inhibitors (ACEIs), which is a relatively slower onset than beta-blockers. All patients underwent strict bed rest to minimize stimuli that may lead to elevation of intracranial pressure, provided that the head of the bed is elevated at 30° to ensure optimal venous drainage. Sedatives and analgesics were cautiously used to avoid masking the neurologic examination findings. Oral nimodipine (360 mg/day) were given to all patients at a dose of 60 mg/4 h from the first day of admission until 21th day, according to recommendations of the 2012 guidelines of the American Stroke Association (class I: level of evidence A) [6]; cases of vasospasm were managed medically by nimodipine infusion, positive fluid balance, positive central venous pressure (CVP), and by maintaining blood pressure toward the hypertensive side and in some failed cases, endovascular intervention was used

Statistical analysis

The collected data were organized, tabulated, and statistically analyzed using the Statistical Package for the Social Studies (SPSS), version 19 created by IBM (Illinois, Chicago, USA). According to numerical values the range, mean, and SDs were calculated. Also, for categorical variables the number and percentage were calculated. Differences between subcategories were tested by t test, Mann–Whitney (used to detect significant differences in mean and median quantitative variable between two groups of patients), χ2, Monte Carlo exact test, and pairwise comparison (study the significant association between two categorical variable). Univariate regression test (detect the effect of some parameters on vasospasm occurrence) and receiver-operating characteristic curve were used for diagnostic accuracy of some factors. The level of significance was adopted at P value less than 0.05.


  Results Top


The study was carried out on 40 patients with acute aSAH. Their mean age was 45.4 ± 7.8 years, which ranged from 28 to 57 years. Majority of cases were females (60%), while 40% were males. Risk factors in our patients were: HTN in 19 (47.5%) patients, diabetes in six (15%) patients, and smoking in 11 (27.5%) patients. GCS was less than 12 in three (7.5%) patients, 13 in three (7.5%) patients, 14 in 13 (32.5%) patients, 15 in 21 (52.5%) patients, HHS was one (20%) in eight, two (42.5%) in 17, three (37.5%) in 15, no patients had more than 4. MFS was one (47.5%) in 19, three (42.5%) in 17, and four (10%) in four. Admission blood pressure: SBP (range, 130–180 mmHg; mean ± SD, 153.25 ± 16.7), DBP (80–115) 153.25 ± 16.7, Na (134.75 ± 1.9, 130–139), HbA1C (7.7 ± 1.25, 5.8–9.9), cholesterol (155.4 ± 22.2, 130–215 mg/dl), triglycerides (158.7 ± 29.88, 90–225 mg/dl), Na (134.75 ± 1.9, 130–139). Cerebral aneurysm characteristics were: mean size was 8.2 ± 4.2 mm and ranged from 3 to 22 mm, as regards site: the majority lied in the MCA (13, 32.5%), A.com (12, 30%), then posterior communicating (P.com: 8, 20%), ICA (5, 12.5%), and PC (2, 5%) [Figure 2]. There is no significant difference between the amount of blood detected by CT (MFS) and cerebral aneurysms sites as U = 0.513, P = 0.972 as shown in [Table 1].
Figure 2: Distribution of the studied cases according to cerebral aneurysms.

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Table 1: Relation between site of cerebral aneurysms and blood clot thickness in brain computed tomography (modified Fisher's scale)

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Vasospasm was detected using TCD in 27 (67.5%) cases, while 13 (32.5%) cases had negative vasospasm. Days of vasospasm were: one (3.7%) case at day 3, eight (29.6) cases at day 5, 15 (55.6) cases at 7 days, and three (11.1%) cases at day 10 [Figure 3]. The vasospasm was symptomatic in nine (33.3%) patients. There is significant association between early vasospasm and symptomatic vasospasm (χ2 = 5.6, P = 0.018) as 33.3% of positive cases had symptoms versus 0% in the other negative group having no symptoms as illustrated in [Figure 4].
Figure 3: Days of early vasospasm using transcranial Doppler.

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Figure 4: Relation between early vasospasm with symptomatic vasospasm.

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There is no significant difference between cases with positive vasospasm versus negative vasospasm as regards age and sex. There is significant association between early vasospasm and HTN as 66.7% of positive cases had HTN versus 7.7% in the other negative group having no HTN (χ2 = 12.2, P = 0.001) as well as with smoking, diabetes (HbA1C), GCC, HHS, and MFS [Table 2].
Table 2: Early vasospasm with clinical and laboratory vascular risk factors, Glasgow coma scale, Hunt and Hess scale, and modified Fisher's scale

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There is significant association between early vasospasm and cerebral aneurysms site as early vasospasm was detected in 13 cases in MCA, seven cases in A.com, 4 P.com and the least was ICA and PCA (two cases and one case, respectively). Pairwise comparison was detected using χ2 test between site as significant was detected between ICA versus MCA, MCA versus P.com as the P value was 0.02 and 0.18, respectively. Also, there is significant association between early vasospasm and cerebral aneurysm size as the mean size in positive cases were higher than negative cases (9.4 ± 4.49 vs. 5.7 ± 2.2 mm), (t = 2.7, P = 0.009) [Table 3].
Table 3: Relation between early vasospasm and characteristics of cerebral aneurysms (site and size)

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SBP more than 195, DBP more than 95, HbA1C more than 7, GCS less than 14, HHS more than 2, MFS more than 1, and aneurysmal size more than 7 mm were risk factors for early vasospasm; however aneurysmal site and smoking were not in spite of association [Table 4] and [Table 5] and [Figure 5].
Figure 5: Female patient 44 years, represented by SAH with GCS: 13, HHS: 3, MFS: 4; CT angiography showed left internal carotid aneurysm, on transcranial Doppler: vasospasm occurs on the fifth day in both ACA and MCA. ACA, anterior cerebral artery; CT, computed tomography; GCS, Glasgow coma scale; HHS, Hunt and Hess scale; MCA, middle cerebral artery; MFS, modified Fisher's scale; SAH, subarachnoid hemorrhage.

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Table 4: Univariate logistic regression to detect the effect of some parameters (separately) on occurrence of vasospasm

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Table 5: Diagnostic ability of some factors to predict early vasospasm

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  Discussion Top


CV is one of the leading causes of poor outcome and higher global disease burden following aSAH. CV is narrowing of a cerebral blood vessel enough to cause reduction in distal blood flow [7]. Of the aSAH patients, 70% develop angiographic vasospasm but only 30% progress to develop evident neurological deficits [8]. The clinical syndrome occurring because of CV is called DCI, which is defined as the development of new focal neurological signs and/or a deterioration in the level of consciousness, lasting for more than 1 h in patients with aSAH [9]. Early detection of DCI is an important step in the improvement of the outcome and the survival of aSAH patients. Transcranial duplex (TCD) can assess the cerebral blood vessel diameters and flow velocities that can be a useful maneuver in the early detection of vasospasm after aSAH [10].

In the current study, there was no significant difference in the amount of blood detected by CT regarding cerebral aneurysm sites as P = 0.972. These results did not agree with the work of Yin et al. [11], who stated that anterior aneurysms are more liable to rupture with significant amounts of bleeding than the posterior ones and they attributed this to genetic factors, which result in different anterior aneurysm wall structures compared with posterior ones.

In the current study, using TCD vasospasm was detected in 27 (67.5%) cases, and 13 (32.5%) cases had negative vasospasm. Similarly, the incidence ranged from 34.5 to 80.0% in previous studies [12]. In the current study, the day of vasospasm was at day 7 in 55.6% of cases and at day 5 in 29.6% of cases. This previous result was in accordance with Kale et al. [13], who revealed that vasospasm usually does not begin before day 3 and its occurrence peaks during days 7–8, and resolves spontaneously after 21 days. Also, in harmony with our results, Kiser [14] found that CV typically occurs between 3 and 14 days after SAH, with a peak incidence ~1 week after the original event. But in Kistka et al. [15], in a small series, detected symptomatic vasospasm on average 3 days. In this study, there was significant difference between cases with positive vasospasm versus negative vasospasm as regards SBP and DBP and HbA1C without significant difference in Na, cholesterol, and triglycerides. This result was in agreement with Nakae et al. [16], who stated that there is a significant relation between high DBP and incidence of vasospasm. The previous result was in agreement with de Rooij et al. [17], who showed that initial hyperglycemia has a predictor role of moderate evidence for vasospasm and a limited association between cholesterol or triglyceride level and incidence of vasospasm. In contrast, Hirashima et al. [18] found no significant differences in SBP and DBP on admission between the two groups. Patients with longstanding diabetes mellitus developed chronic insulin resistance, which is associated with higher vascular resistance and play a role in the development of vascular disease secondary to diabetes mellitus. Microscopic changes including endothelial hypertrophy and increased wall thickness are considered as a mirror for the changes noted in patients with CV seen after aSAH. So, diabetic patients are at a higher risk for the development of microvascular disease following SAH [19]. In chronic hypertensive patients, arterial vasoconstriction, enlargement of vascular endothelium, and subendothelial fibrosis that result from different mechanisms such as inflammatory, immunologic, free radical production, and abnormalities in ion channels have been proposed to cause this alteration in vessel constriction and relaxation. Also, release of serotonin and certain prostaglandins from the platelets is also considered as a potential cause of early vasospasm [18]. In this study, there was significant difference between cases with positive vasospasm versus negative vasospasm as regards GCS, HHS, and MFS. This previous result was in agreement with Chhor et al. [20], who said that lower GCS is a risk factor for CV and DCI. The grade of HHS showed a significant prognostic role on vasospasm with a cutoff point of more than 2. This finding was in accordance with Inagawa et al. [19], who demonstrated that Hunt–Hess grades III–IV SAH are associated with CV and DCI. Also, Nassar et al. [21] showed that in accordance with our results, on admission, patients who developed vasospasm (group I) had significantly higher HHS than group II and did not develop vasospasm (41.2 ± 6.2 years, 2.2 ± 0.4 versus 56± 6.9 years, 1.8 ± 0.4 with P = 0.0031, respectively) and had higher MFS Similarly, Jabbarli et al. [22] found the poor HHS grade correlated significantly with the earlier development of vasospasm on TCD ultrasound. In contrast to this study, Hirashima et al. [18] found no significant differences in HH grade between cases who developed CV from those who did not develop vasospasm, while the Fisher scale was higher in the vasospasm group.

In the current study, there was significant association between early vasospasm and symptomatic to vasospasm (P = 0.018) as 33.3% of positive cases had symptoms versus 0% in the other negative group who had no symptoms. At the same time, according to Nassar et al. [21], patients who progressed to DCI had earlier onset of vasospasm manifestations than those who passed a regressive course. This result is in accordance with Aldakkan et al. [23] as well as Phan et al. [24], who stated that earlier ultrasonographic signs of vasospasm are associated with higher incidence of clinically evident symptoms, and they recommend early intervention and aggressive therapy in this sector of patients. Conversely, according to the Jabbarli et al. [22] results, the early onset of vasospasm was significantly associated with the severity of vasospasm (P = 5.0469).

In the current study, there was significant association (P = 0.034) between early vasospasm and cerebral aneurysm site as early vasospasm was detected in 13 cases in the MCA, seven cases A.com, four P.com, and the least was ICA and ICA and PCA (two cases and one case, respectively). Using the χ2 test, significant difference was detected between ICA versus MCA, MCA versus P.com (P = 0.02 and 0.018, respectively). However, Abla et al. [25] stated a greater risk of vasospasm in pericallosal aneurysms. In contrary to our results, Nassar et al. [21] angiography showed that the ruptured aneurysmal sites were the A.com, MCA, P.com, terminal ICA, and ACA aneurysms at a rate of 23.7, 36.8, 21.1, 10.5, and 7.9%, respectively. There were no significant differences between groups I (patients developed CV) and II (did not develop vasospasm) regarding the sites of ruptured aneurysms.

In this study, there was significant association between early vasospasm and cerebral aneurysm size as the mean size in positive cases higher than negative cases (9.4 ± 4.49 vs. 5.7 ± 2.2 mm, P = 0.009). Regarding the aneurysmal size, Nassar et al. [21], found that, 26 (68.4%) patients had aneurysms less than or equal to 12 mm, 11 (29%) had 13–25 mm, and the last one (2.6%) had giant aneurysm more than 25 mm. Six patients had aneurysms less than or equal to 12 mm, seven had aneurysms 13–25 mm, and the included case with giant aneurysm developed vasospasms.

In the current study, using univariate logistic regression for risk factors of early vasospasm, there was significant risk and significant prognostic value of each parameter (HbA1C >7, SBP >145, DBP >95, GCS with cutoff point of <14, HHS >2, MFS >1, and aneurysmal size >7 mm) on the occurrence of vasospasm. According to Mijiti et al. [26], in univariate analysis age more than or equal to 53 years, poor MFS (3–4), and poor HHS (4–5) were risk factors of CV. In addition, aneurysm size more than or equal to 10 mm was a risk factor for vasospasm and symptomatic vasospasm.

In this study, aneurysmal size can significantly predict early vasospasm such as diagnostic accuracy [area under the curve (95% confidence interval (CI)=0.77 (0.611–0.88), P = 0.0003], at a cutoff point of 7 mm, which has highest sensitivity (55.6%) and specificity (84.6%). This was supported by the Nassar et al. [21] results which showed that 23% of aneurysms of size less than or equal to 12 mm, 64% of aneurysms of size 13–25 mm, and 100% of aneurysms more than 25 mm developed vasospasm. Six patients had aneurysms less than or equal to 12 mm, seven had aneurysms of 13–25 mm, and the included case with giant aneurysm developed vasospasms.

The limitation of this study is the small number of patients; however, our sample was comparable to that in majority of previous studies. We only included patients with repeated neuroimaging studies, which may introduce selection bias. Some other factors that are potentially associated with CV such as hydrocephalus, electrocardiogram changes, and cardiac abnormalities were not evaluated in our study. Also, treatment lines for each case of vasospasm separately and follow up after treatments are not documented in our study.


  Conclusion Top


Clinical severity of SAH (GCS, HHS), blood clot thickness (MFS), cerebral aneurysmal size, SBP and DBP, and HbA1C seem to be important predictors for CV after SAH while smoking, lipid profile, and site of aneurysm did not reveal prediction of vasospasm.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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