Cerebral blood volume Alberta Stroke Program Early Computed Tomography Score predicts intracranial hemorrhage after thrombectomy in patients with acute ischemic stroke in an extended time window

Abstract

Background

Higher baseline Alberta Stroke Program Early Computed Tomography Score (ASPECTS) was associated with a lower probability of hemorrhagic transformation in patients with acute ischemic stroke (AIS).

Purpose

To investigate the predictive value of cerebral blood volume (CBV)-ASPECTS of intracranial hemorrhage (ICH) in AIS treated with thrombectomy selected by computed tomographic perfusion (CTP) in an extended time window.

Material and Methods

A total of 91 consecutive patients with AIS with large vessel occlusion in the anterior circulation after thrombectomy in an extended time window were enrolled between January 2018 and September 2019. ICH was diagnosed according to Heidelberg Bleeding Classification. CBV-ASPECTS was assessed by evaluating each ASPECTS region for relatively low CBV value compared with the mirror region in the contralateral hemisphere. Demographic characteristics, clinical data, CBV-ASPECTS, and procedure process and results were compared between patients with ICH and those without.

Results

ICH occurred in 31/91 (34.1%) patients with AIS. Symptomatic ICH (sICH) was observed in 4 (4.4%) patients, while asymptomatic ICH (aICH) was seen in 27 (29.7%). In univariate analysis, both ICH and aICH were associated with high admission NIHSS score (P<0.001 and P<0.001, respectively), more passes of retriever (P = 0.007 and P = 0.019, respectively), low NCCT-ASPECTS (P = 0.013 and P = 0.034, respectively), and low CBV-ASPECTS (P < 0.001 and P < 0.001, respectively). After multivariable analysis, low CBV-ASPECTS remained an independent predictor of ICH (odds ratio [OR] 0.521, 95% confidence interval [CI] 0.371–0.732, P < 0.001) and aICH (OR 0.532, 95% CI 0.376–0.752, P < 0.001), respectively.

Conclusion

Low CBV-ASPECTS independently predicts ICH in patients with AIS treated with thrombectomy selected by CTP in an extended time window.

Keywords

Alberta Stroke Program Early Computed Tomography Score cerebral blood volume CBV-ASPECTS intracranial hemorrhage acute ischemic stroke computed tomographic perfusion

Introduction

While significant advances have been made regarding emergent treatment of acute ischemic stroke (AIS), the different therapeutic revascularization options remain associated with an increased risk of intracranial hemorrhage (ICH) (1,2). ICH, which can be asymptomatic (3 –5) or symptomatic (6,7), may be a serious complication of AIS after intravenous thrombolysis or endovascular treatment (ET). Accordingly, greater understanding about the predictors of ICH after recanalization therapy is essential to improve risk assessment, patient selection, and early prognostication.

The Alberta Stroke Program Early Computed Tomography Score (ASPECTS) is a semi-quantitative and 10-point grading system that assesses the extent and distribution of early ischemic changes in patients with AIS (8). A previous study demonstrated that symptomatic intracerebral hemorrhage (sICH) was increased with lower baseline non-contrast computed tomography (NCCT) ASPECTS in patients with AIS treated with intravenous recombinant tissue plasminogen activator (rtPA) (9). A recent publication demonstrated that higher baseline NCCT-ASPECTS was associated with a lower probability of hemorrhagic transformation (HT) in patients with AIS with anterior circulation large vessel occlusion (10). Furthermore, computed tomography (CT) angiography ASPECTS and diffusion-weighted images ASPECTS were independently associated with ICH (11,12).

Advanced neuroimaging such as computed tomography perfusion (CTP) or magnetic resonance imaging (MRI) is now a regular work-up (13,14) in patients with AIS when ET is performed 6–24 h after the onset of symptoms. However, in most institutions, CTP is still the preferred choice of rapid diagnosis of AIS because MRI is not always available or contraindicated. A previous study concluded that CTP-ASPECTS demonstrated the highest inter-observer agreement compared with NCCT-ASPECTS or ASPECTS on CTA source images (15). To date, limited data exist regarding the value of cerebral blood volume (CBV)-ASPECTS for predicting ICH (16,17), and this relationship has never been investigated in selected patients with AIS presenting within 6–24 h from the last known normal time.

The aim of the present study was to determine whether CBV-ASPECTS was able to predict ICH in patients with AIS treated with thrombectomy in an extended time window.

Material and Methods

Study population

We conducted a retrospective analysis of a prospectively collected thrombectomy database at a single stroke center for all consecutive patients with AIS who received ET with the Solitaire AB device between January 2018 and September 2019.

Demographic features and clinical information were extracted from the registered data and included age, gender, smoking, etc. Stroke severity on admission was assessed using National Institute of Health Stroke Scale (NIHSS) scores by certified raters (18).

Inclusion criteria were as follows: age was ≥18 years; baseline NIHSS scores were ≥6; occlusions in the M1/M2 segment of the middle cerebral artery (MCA) and/or intracranial internal carotid artery (ICA) were confirmed; ET could be initiated within 6–24 h from onset of symptoms or last known normal time; CTP imaging was performed well without significant motion artifacts and the imaging criteria fulfilled DAWN or DEFUSE 3 criteria (13,14); the Solitaire AB device was used; and baseline modified Rankin scale (mRS) score was < 2. Exclusion criteria were as follows: detection of ICH at admission NCCT; posterior circulation infarction and anterior cerebral artery infarction; contraindications to iodinated contrast agent; pregnancy; and loss of follow-up CT.

Preoperative imaging evaluation

NCCT, CTA, and CTP scan were performed on a 128-slice multidetector CT scanner (optima CT 660, GE Healthcare, Milwaukee, WI, USA) according to our institutional stroke imaging protocol for patients with AIS. In our stroke center, CTP was performed in patients with AIS with stroke onset time >5 h or with unclear time. CTP data were reconstructed for CT angiography analysis.

Non-contrast whole-brain helical CT was performed with 5-mm axial section thickness using the imaging parameters of 120 kVp and 100–350 auto-mAs. CTP was acquired using a periodic spiral approach (four-dimensional adaptive spiral mode, maximum pitch 0.984) consisting of 30 consecutive spiral scans (80 mm in z-axis, 2-s delay, 1.7-s temporal resolution). CTP scan parameters were 100 kVp, 200 mAs, and rotation of 0.4 s. Total examination time of CTP was 53 s. During the CTP scan, 50 mL of contrast medium (iopromide, Ultravist 370, Bayer Schering Pharma, Berlin, Germany) was administered intravenously at a flow rate of 5 mL/s using a power indicator, followed by a 30-mL saline chaser at the same rate.

CTP was postprocessed using commercially available software (Advantage Workstation 4.7; GE Healthcare) and standard singular value deconvolution algorithms. The CBV parameter was calculated as the integral of the tissue time attenuation curve divided by the integral of the normalized arterial and venous input function. The arterial and venous inputs were obtained from the anterior cerebral artery and superior sagittal sinus, respectively. Parametric CBV maps were automatically generated and overlaid on the source CTP images. The CBV parameter was expressed in units of milliliters per 100 mg, and the scale was set at 0–8 mL/100 mg for CBV maps.

During the assessment of CBV-ASPECTS, MCA territory was divided into 10 regions (caudate, lentiform nucleus, internal capsule, insula, and M1–M6) at two levels of basal ganglia/internal capsules and the upper portion of the lateral ventricles, respectively. The readers visually evaluated each ASPECTS region for relatively low CBV value compared with the mirror region in the contralateral hemisphere. Two neuroradiologists (both with six years of experience in neuroradiology), who were blinded to the clinical information and study design, independently viewed the CBV maps, and assessed the CBV-ASPECTS. If discrepancy existed between two readers, another neuroradiologist (with 15 years of experience in neuroradiology) would re-evaluate the CBV maps and help to reach a consensus agreement.

Endovascular therapy

All procedures were carried out under local anesthesia/conscious sedation. An 8-F or 6-F guiding catheter was placed in the common carotid or internal carotid artery through a femoral sheath. Thrombectomy was performed with the use of the Solitaire AB device (Solitaire, Covidien, Irvine, CA, USA) in all patients. For the patients with tandem lesions, the intracranial occluded artery was treated with thrombectomy, while combined ipsilateral cervical carotid occlusion was treated with stent placement when necessary. For the residual stenosis in cases with in situ thrombosis, balloon angioplasty and stent placement were performed at the discretion of the operator. Aspiration through an 8-F guiding catheter or Navien intermediate catheter was conducted if necessary. Intra-arterial thrombolysis or administration of intra-catheter tirofiban might also be performed as rescue therapies. During the study period, we often used Solitaire AB only as first-line therapy in the patients without curved supra-aortic vessels or with possible intracranial atherosclerosis-related occlusions. Otherwise, a combined approach called SWIM (Solitaire AB Stent With Intracranial Support Catheter for Mechanical Thrombectomy) technique was used. In the “Solitaire AB only as first-line therapy” group, only two patients were given SWIM technique as rescue therapy, the others were given Solitaire AB only to try a second time or more, if the first attempt failed. In the “SWIM technique as first-line therapy” group, after the first attempt of SWIM technique failed, we always used this technique to try a second time or more.

Postoperative evaluation and diagnosis of ICH

A CT scan was usually performed 24–48 h after treatment or whenever an ICH was indicated by clinical symptoms. ICH, including sICH or asymptomatic ICH (aICH), was diagnosed according to the Heidelberg Bleeding Classification (HBC) (19).

Hyperdense lesions that disappeared or prominently cleared were deemed as contrast extravasation on follow-up NCCT scans obtained in the next 24 h (20).

Recanalization results were assessed using the modified Treatment in Cerebral Ischemia (mTICI) classification (21). Good reperfusion was defined as mTICI 2b or 3. Door to puncture (DTP) time was defined as time from hospital arrival to groin puncture. Total time of operation was defined as time from groin puncture to mTICI 2b or 3 or completion of the procedure in cases for which reperfusion was not achieved.

Statistical analysis

Data are presented as mean ± SD or median (interquartile range [IQR]) for continuous variables and number (%) for categorical variables. Univariate analysis was performed using the Fisher’s exact or chi-square tests for categorical data, and the two-sample t-test or Mann–Whitney U test for continuous data. Multivariable logistic regression was performed including all variables with P < 0.1 from the univariate analysis to identify the factors independently associated with ICH. Odds ratios (OR) and their 95% confidence intervals (CI) were calculated. Intraclass correlation coefficient (ICC) was used as a measure of concordance of CBV-ASPECTS. Statistical testing was done at the two-tailed a level of 0.05 using SPSS 20.0 (IBM Corp., Chicago, IL, USA).

Results

Overall, 91 consecutive patients (40.7% women; mean age = 66.8 years) with AIS who received ET with the Solitaire AB between January 2018 and September 2019 in our stroke center fulfilled the inclusion criteria. Of the 91 patients, 12 received intravenous rtPA before transfer to our hospital and their onset time to our hospital was > 5 h. Thus, these patients were included in our study as the ones in an extended time window. Of the 91 patients included in our study, 59 were treated with SWIM technique as first-line therapy, while the remaining 32 were treated with Solitaire AB only as first-line therapy. Fifty-three patients were treated with the secondary thrombectomy or more after failed stent-retriever thrombectomy, of which 18 were in the “Solitaire AB only as first line therapy” group. In the “Solitaire AB only as first line therapy” group, two were treated with SWIM technique as rescue therapy, five were deemed as intracranial atherosclerosis-related occlusions but treated with stent thrombectomy twice, and the other 11 were treated with Solitaire AB only to try second times or more. In the “SWIM technique as first-line therapy” group, we always used SWIM technique to try two or more times if this technique failed in embolism-related occlusions. For the five patients deemed as intracranial atherosclerosis-related occlusions in this group, two were treated with stent thrombectomy twice and later with balloon angioplasty and/or stent placement.

Hypertension was seen in 60.4%, diabetes mellitus in 20.9%, atrial fibrillation in 24.2%, coronary artery disease in 20.9%, stroke/TIA in 23.1%, and smoking in 27.5% of patients. Median baseline NIHSS score was 14 (IQR = 10–17). Good reperfusion occurred in 80.2%. Median CBV-ASPECTS was 9 (IQR = 7–10; range = 3–10), while median NCCT-ASPECTS was 8 (IQR = 7–9; range = 3–10). ICC for NCCT-ASPECTS and CBV-ASPECTS was 0.782 and 0.892, respectively. According to the HBC, ICH occurred in 31 of 91 (34.1%) patients with AIS. sICH was observed in 4 (4.4%) patients, while aICH was seen in 27 (29.7%). At 90 days, 38 of 91 patients (41.8%) had a good functional outcome (mRS = 0–2) and 13 (14.3%) patients died.

Table 1 shows the results from the univariate statistical tests performed on the baseline variables and endovascular procedural variables between patients with or without ICH. There were no statistically significant differences in age, sex, vascular risk factors, occlusion site, use of IV rtPA, good reperfusion, DTP time, and total time of operation between ICH and without ICH groups (Table 1). In univariate analysis, ICH was associated with high admission NIHSS score (P < 0.001), more passes of retriever (P = 0.007), low NCCT-ASPECTS (P = 0.013), and CBV-ASPECTS (P < 0.001). Further multivariable logistic regression analysis indicated that high admission NIHSS score (OR = 1.10, 95% CI = 1.004–1.203, P = 0.042) and high CBV-ASPECTS (OR = 0.529, 95% CI = 0.369–0.758, P < 0.001) were independently associated with ICH (Table 2, Fig. 1).

Table 1.

Baseline characteristics (unadjusted) of the studied patient population as stratified by ICH.

Characteristics	All patients (n = 91)	ICH (n = 31)	No ICH (n = 60)	P value
Age (years)	66.8 ± 12.7	68.1 ± 16	66.1 ± 10.7	0.474
Female sex	37 (40.7)	13 (41.9)	24 (40)	1.0
Stroke/TIA	21 (23.1)	9 (29)	12 (20)	0.432
Atrial fibrillation	22 (24.2)	9 (29)	13 (21.7)	0.450
Hypertension	55 (60.4)	19 (61.3)	36 (60)	1
Coronary artery disease	19 (20.9)	9 (29)	10 (16.7)	0.184
Diabetes mellitus	19 (20.9)	5 (16.1)	14 (23.3)	0.588
Smoking	25 (27.5)	7 (22.6)	18 (30)	0.621
Baseline measurements
Admission NIHSS score	14 (10–17)	17 (14–19)	12 (9–15)	<0.001
Admission blood glucose	6.16 ± 2.37	6.74 ± 2.53	5.86 ± 2.25	0.094
INR	1.07 (1.01–1.13)	1.09 (1.01–1.18)	1.04 (1–1.13)	0.146
Platelet (10⁹/L)	189.8 ± 64.8	188.6 ± 64.4	190.4 ± 65.5	0.906
Occlusion site				0.808
MCA	65 (71.4)	23 (74.2)	42 (70%)
ICA	26 (28.6)	8 (25.8)	18 (30%)
Use of IV rtPA	12 (13.2)	2 (6.5)	10 (16.7%)	0.209
Procedure process and results
Good reperfusion	73 (80.2)	24 (77.4)	49 (81.7%)	0.782
IA tirofiban	22 (24.2)	4 (12.9)	18 (30%)	0.120
IA thrombolysis	3 (3.3)	1 (3.2)	2 (3.3%)	1
Angioplasty and stenting	26 (28.6)	6 (19.4)	20 (33.3%)	0.222
Passes of retriever	2 (1–3)	2 (2–3)	1 (1–3)	0.007
DTP time (min)	94 (79–112)	94 (71–109)	95 (79–115)	0.586
Total time of operation (min)	90 (59–120)	92 (59–123)	87 (59–120)	0.828
Outcome
90-day mRS 0-2	38 (41.8)	6 (19.4)	32 (53.3)	0.002
90-day mortality	13 (14.3)	6 (19.4)	7 (11.7)	0.354
NCCT-ASPECTS	8 (7–9)	7 (6–8)	8 (7–9)	0.013
CBV-ASPECTS	9 (7–10)	7 (5–9)	10 (8–10)	<0.001

Values are given as n (%), mean ± SD, or median (IQR).

ASPECTS, Alberta Stroke Program Early Computed Tomography Score; CBV, cerebral blood volume; DTP, door to puncture; IA, intra-arterial; ICA, internal carotid artery; ICH, intracranial hemorrhage; INR, international normalized ratio; IQR, interquartile range; IV, intravenous; MCA, middle cerebral artery; mRS, modified Ranking scale; NCCT, non-contrast computed tomography; NIHSS, National Institute of Health Stroke Scale; rtPA, recombinant tissue plasminogen activator; SD, standard deviation; TIA, transient ischemic attack.

Table 2.

Multivariate logistic regression analysis of the independent predictors of ICH.

	OR (95% CI)	P value
Model 1: ICH
High NIHSS score at admission	1.10 (1.004–1.203)	0.042
High CBV-ASPECTS	0.529 (0.369–0.758)	<0.001
Model 2: aICH
High NIHSS score at admission	1.09 (0.99–1.20)	0.068
High CBV-ASPECTS	0.539 (0.374–0.778)	<0.001

Model 1 and Model 2: variables entered: high NIHSS score at admission, high CBV-ASPECTS, passes of retriever, high NCCT-ASPECTS, high admission blood glucose.

aICH, asymptomatic intracranial hemorrhage; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; CBV, cerebral blood volume; CI, confidence interval; ICH, intracranial hemorrhage; NIHSS, National Institute of Health Stroke Scale; OR, odds ratio.

Fig. 1.

Images from a 73-year-old patient with sudden onset of left hemiplegia and aphasia. (a) CTA showed occlusion of the proximal M1 segment of MCA. (b, c) Colored CBV map showed relative hypoperfusion in the insular ribbon, anterior MCA cortex (M1), MCA cortex lateral to insular ribbon (M2) and lateral MCA territories superior to M2 (M5), yielding an ASPECT of 6. (d, e) Despite successful recanalization being achieved through endovascular therapy, follow-up CT indicated hemorrhage transformation occurred in the infarct lesion (f). ASPECT, Alberta Stroke Program Early Computed Tomography Score; CTA, computed tomography angiography; CBV, cerebral blood volume; MCA, middle cerebral artery.

Baseline characteristics of patients with or without aICH are summarized in Supplementary Table 1. There was also no significant difference between the aICH and without aICH groups with respect to age, sex, vascular risk factors, occlusion site, use of IV rtPA, good reperfusion, DTP time, and total time of operation. Subsequently, a multivariate logistic regression was performed using the statistically significant variables in univariate analysis as predictor variables and the incidence of aICH as the dependent variable (Supplementary Table 1). High CBV-ASPECTS (OR = 0.539, 95% CI = 0.374–0.778, P < 0.001) also independently inversely predicted aICH (Table 2).

Discussion

In the present study, we observed an incidence of about 35% for ICH in the patients with AIS with large vessel occlusion in the anterior circulation treated with thrombectomy in an extended time window. Meanwhile, a low CBV-ASPECTS was found to be an independent prognostic factor for ICH after thrombectomy. Furthermore, the positive results can also be applied to aICH.

A previous study indicated that a high baseline NCCT-ASPECTS was associated with a lower probability of HT in patients with AIS after neurothrombectomy (10). ASPECTS has also been applied to CTP with better inter-observer variability (15), and CTP-ASPECTS is more accurate at predicting the irreversibly damaged tissue and clinical outcome than NCCT-ASPECTS (22,23). Recently, randomized trials provided level 1 evidence for the utilization of advanced neuroimaging (13,14), such as CTP or MRI, in patient selection for ET beyond a 6-h time window. In most institutions, however, CTP is still the preferred choice of rapid diagnosis of hyperacute ischemic stroke by generating maps of CBV, cerebral blood flow, and mean transit time. Several studies demonstrated that low CBV was a more powerful predictor of HT than other CTP-derived parameters in AIS (24,25). Although automated software analysis can be used to process the CTP imaging, it is not obtainable in many stroke centers mainly due to the high price. Thus, a technique such as ASPECTS with rapid and inexpensive assessment may be widely accepted.

The finding of our study that low CBV-ASPECTS independently predicted ICH is consistent with that of prior studies (16,17). In a previous study, Padroni et al. (16) included 62 patients with AIS within 8 h of onset of symptoms. Among these patients, 28 were treated with intravenous thrombolysis, three with intra-arterial thrombolysis, and six with mechanical thrombectomy, whereas the other 25 patients did not accept any therapy. They concluded that CBV-ASPECTS were higher in patients with no HT than those with HT. Another study also demonstrated that CBV-ASPECTS 0–7 remained independent prognostic factors for HT in the 52 anterior circulation cardioembolic stroke patients within 12 h of onset of symptoms (17). In their study, however, only seven patients received intravenous rtPA and mechanical thrombectomy, and two patients were given intravenous and intra-arterial rtPA, while the remainder received intravenous rtPA only or did not receive any therapy. To date, studies exploring the relationship between CBV-ASPECTS and ICH in acute ET are scarce and include only small numbers of patients. The present study focused on this association particularly in the setting of AIS and reperfusion therapy where only thrombectomy was used. Our results indicated the previous observation that low CBV-ASPECTS was associated with ICH also existed in patients with AIS treated with thrombectomy in an extended time window.

Although low CBV-ASPECTS has been proven to be useful in predicting subsequent ICH or even aICH, the number of sICH in our study cohort was too small for sub-group analysis. Previous studies focused more attention on sICH because ample existing data demonstrated that sICH has a negative impact on functional outcomes in patients with AIS treated with ET or intravenous tPA (26,27). However, aICH has been reported to have varied effects on functional outcomes in patients treated with intravenous rtPA (28,29). In contrast, many studies have questioned the “benign” nature of aICH in patients with AIS treated with ET, demonstrating that aICH appears to be associated with functional dependence and high mortality (3,4). It seems that aICH after ET and after sole medical treatment may have a distinct prognostic value. Compared with sICH, aICH is a more common complication in patients with AIS undergoing ET. Previous studies showed that approximately 10%–40% of patients with AIS experienced aICH after thrombectomy (3,4,30,31). The proportion of patients with aICH after ET in the present analysis (29.9%) was within the range of those reported in previous studies. Considering the relatively higher incidence and negative impacts on functional outcomes, aICH should be paid more attention as well as sICH or at least should not be ignored in patients treated with thrombectomy.

In our cohort, consistent with previous studies, NIHSS scores at admission were significantly higher in the patients with ICH (32,33). However, previously identified risk factors, such as age, diabetes, atrial fibrillation, and use of intravenous rtPA, were not correlated with ICH in this series, which may be attributable to the relatively small sample size.

The present study has some limitations. First, it was a retrospective single-center study with a small cohort size, which might result in selection bias. Second, the number of patients with sICH was too small (four sICH patients) in our study cohort. The association between CBV-ASPECTS and sICH could not be assessed statistically although we found that CBV-ASPECTS were numerically lower in patients with sICH (range = 3–7) than those without (range = 4–10). This is unfortunate, as sICH can cause death or severe disability. However, ICH or aICH has also been implicated in worse clinical outcome (3 –5). Our results may not be directly transferable to the sICH population in particular, but are nonetheless important for the prediction of ICH as well as aICH. Third, anticoagulation and antiplatelet treatments were not analyzed, both of which may influence the risk of ICH. Further studies including these confounding variables are warranted.

In conclusion, our study indicates that a low CBV-ASPECTS independently predicts ICH in patients with AIS treated with thrombectomy in an extended time window. Further studies with the inclusion of adequate numbers of patients with sICH are warranted to assess the value of CBV ASPECTS in predicting sICH risk in this kind of AIS population.

Supplemental Material

sj-pdf-1-acr-10.1177_0284185121990843 - Supplemental material for Cerebral blood volume Alberta Stroke Program Early Computed Tomography Score predicts intracranial hemorrhage after thrombectomy in patients with acute ischemic stroke in an extended time window

Supplemental material, sj-pdf-1-acr-10.1177_0284185121990843 for Cerebral blood volume Alberta Stroke Program Early Computed Tomography Score predicts intracranial hemorrhage after thrombectomy in patients with acute ischemic stroke in an extended time window by Yue-Zhou Cao, Lin-Bo Zhao, Zhen-Yu Jia, Qiang-Hui Liu, Xiao-Quan Xu, Hai-Bin Shi and Sheng Liu in Acta Radiologica

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Hai-Bin Shi

Sheng Liu

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