Basilar artery and posterior circulation collaterals score on digital subtraction angiography predicts prognosis for acute basilar artery occlusion treated with endovascular thrombectomy

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Basilar artery and posterior circulation collaterals score on digital subtraction angiography predicts prognosis for acute basilar artery occlusion treated with endovascular thrombectomy

https://doi.org/10.21203/rs.3.rs-4887314/v1

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Background and purpose

The prognosis of acute basilar artery occlusion (BAO) is poor, carrying a high risk of disability and mortality if left untreated. Several radiological scores may predict the clinical outcome of acute BAO treated with endovascular thrombectomy (EVT). This study aims to assess the prognostic value of a novel radiological score, the Basilar Artery and Posterior Circulation Collaterals (BAPCOR) score.

Methods

A retrospective analysis was performed on consecutive acute BAO patients treated with EVT. The BAPCOR score, a 15-point digital subtraction angiography (DSA)-based grading system, was used to assess thrombus burden and posterior circulation collateral status. Successful recanalization was defined as a modified thrombolysis in cerebral infarction (mTICI) score 2b-3, and a good outcome was defined by a modified Rankin Scale (mRS) score of ≤ 2 at 3 months. Receiver operating characteristic (ROC) curve determined the area under the curve (AUC) and the optimum cutoff value. Multivariate regression analysis was used to identify predictors of clinical outcome.

Results

Among the enrolled patients, 85.1% (40/47) achieved successful recanalization (mTICI, 2b-3) and 34.0% (16/47) had a good outcome (mRS score 0–2). The ROC analysis indicated that the AUC of the BAPCOR score was 0.868 (95%CI: 0.753–0.983). A cut-off value of predicting poor outcome was set at 8.5, with sensitivity of 0.688 and specificity of 0.935. Correlation analysis showed a moderate negative correlation between BAPCOR and mRS.

Conclusion

The BAPCOR scoring system is associated with outcomes in acute BAO patients treated with EVT with superiority in reflecting thrombus burden and collateral status.

Biological sciences/Neuroscience/Diseases of the nervous system/Stroke

Health sciences/Neurology/Neurological disorders/Cerebrovascular disorders

Acute basilar artery occlusion

endovascular thrombectomy

digital subtraction angiography

collateral circulation

prognosis

Acute basilar artery occlusion (BAO) comprises approximately 1% of all strokes and is one of the most devastating neurological conditions, carrying a high risk of disability and mortality without recanalization. [1–3] Based on the findings from the BAOCHE (Basilar Artery Occlusion Chinese Endovascular Trial) and ATTENTION (Trial of Endovascular Treatment for Acute Basilar-Artery Occlusion) trials, combining endovascular thrombectomy (EVT) with optimal drug treatment has shown significantly efficacy in treating acute BAO within 24 hours of onset [4, 5]. Previous studies have identified various clinical predictors of clinical outcome after acute BAO, such as the National Institutes of Health Stroke Scale (NIHSS) score at admission, patient age, time to treatment, thrombolysis, and recanalization [6–9]. In addition, several potential imaging-derived predictors of clinical outcome have been proposed, with pre-EVT radiological scores on computed tomographic angiography (CTA) or digital subtraction angiography (DSA) being particularly noteworthy [10–15]. While these scoring systems effectively evaluate the correlation between thrombus burden and the posterior communicating artery (PcoA) as the primary collateral with outcome, posterior circulation collaterals not only comprise of primary collateral but also secondary collaterals of cerebellar arteries, including superior cerebellar artery (SCA), anterior inferior cerebellar artery (AICA), and posterior inferior cerebellar artery (PICA). These secondary collaterals can be clearly identified on DSA, which has higher spatial and temporal resolution and can dynamically display the direction and velocity of blood flow, thus serving as the gold standard for diagnosing cerebrovascular disease, whereas magnetic resonance angiography (MRA) and CTA have certain limitations. This study aims to assess the prognostic value of a new radiological score to improve prognostic accuracy: Basilar Artery and Posterior Circulation Collaterals (BAPCOR) score on DSA.

Clinical materials

We conducted a retrospective analysis involving 47 consecutive stroke patients with acute BAO who was treated with EVT between October 2016 and January 2019. Prior to EVT, all eligible patients received intravenous thrombolysis with recombinant tissue plasminogen activator (rt-PA) in accordance with current guidelines. Otherwise, patients proceeded directly to EVT if the treatment window was ≤ 24 hours. Exclusion criteria for EVT encompassed a modified Rankin scale score (mRS) of>2 prior to onset, intracranial hemorrhage, brain tumor, severe craniocerebral trauma, active bleeding, serious underlying conditions such as vital organ failure or short life expectancy due to malignant tumors. Informed consent was obtained from the legally authorized representatives of all patients before underdoing EVT, and the study protocol was approved by China-Japan Union Hospital of Jilin University institutional review board.

The time of symptoms onset was recorded based on the patient’s or witness’s account; if unknown, it was considered to be the last time the patient was observed to be well. In patients presenting with mild symptoms followed by sudden onset of aggravated symptoms or decrease in conscious state, the time of deterioration in clinical state was taken as estimated time of occlusion.

Clinical baseline characteristics, including age, sex, risk factors, stroke type, NIHSS, blood glucose level, and blood pressure and pc-ASPECT score upon admission, were recorded (Table 1). The severity of stroke at admission, as measured by the NIHSS score, was documented by trained fellows at the stroke center. Brain computed tomography (CT) scans were performed using a 16-slice, 64-slice scanner or discovery CT 750 HD with 0.5 mm thickness in axial acquisitions. DSA images were acquired using SIEMENS Artis zee floor III or zee biplane device. EVT procedures were performed under either local anesthesia or general anesthesia (Table 2). Stent retrievers with different types of Solitaire or a direct aspiration first pass thrombectomy (ADAPT) were used for mechanical thrombectomy as first-line EVT, while balloon dilation or stent placement served as remedy strategies. Intracerebral stent placement utilized devices such as Wingspan, Solitaire, or Apollo stent. Successful recanalization was defined as achieving a Thrombolysis in Cerebral Infarction (TICI) score of 2b-3. Door-to-puncture time (DPT), onset-to-puncture time (OPT), puncture-to-recanalization time (PRT), onset-to-recanalization time (ORT) were recorded as key pre-EVT and intra-EVT time metrics. Diagnostic radiologic imaging was independently interpreted by two neurointerventionalists. The mRS score was assessed via telephone call or clinical visit at 3 months, with an mRS score of 0–2 indicating a good outcome at 3 months.

Table 1

Baseline patients and stroke characteristics
	All patients (n = 47)	Good outcomes (mRS ≤ 2, n=16)	Bad outcomes(mRS > 2, n=31)	P value
Age, mean (SD)	58.5 ± 9.8	55.9 ± 9.7	59.8 ± 9.8	0.203
Gender, male (%)	37 (78.7)	12 (75.0)	25 (80.6)	0.654
Baseline NIHSS, median (IQR)	19 (15–26)	15 (12.75–18.25)	23 (17-27.5)	0.014
Intravenous thrombolysis	20 (42.6)	10 (62.5)	10 (32.3)	0.047
pc-ASPECT, mean (SD)	9.5 ± 0.9	9.9 ± 0.3	9.4 ± 1.0	0.054
Risk factors
Hypertension, n (%)	32(68.1)	10 (62.5)	22 (71.0)	0.555
Hyperlipidemia, n (%)	7 (14.9)	1 (6.2)	6 (19.4)	0.232
Diabetes mellitus, n (%)	6 12.8)	0 (0.0)	6 (19.4)	0.060
Atrial fibrillations, n (%)	4 (8.5)	1 (6.2)	3 (9.7)	0.690
Hyperhomocysteinemias, n (%)	8 (17.0)	5 (36.2)	3 (9.7)	0.062
Smoking, n(%)	27 (57.4)	8 (50)	19 (61.3)	0.458
BAO site				0.828
Proximal-BA, n (%)	15 (31.9)	9 (29)	6 (37.5)
Mid-BA, n (%)	25 (53.2)	17 (54.8)	8 (50)
Distal-BA, n (%)	7 (14.9)	5 (16.1)	2 (12.5)
Stroke etiology				0.585
LA	41 (87.2)	26 (83.9)	15 (93.8)
CE	5 (10.6)	4 (12.9)	1 (6.2)
SUE	1 (2.1)	1 (3.2)	0
Time metrics
OPT (min), median (IQR)	310 (225-436.5)	249 (150.25-373.75)	368 (260–449)	0.347
DPT (min), median (IQR)	117 (62.5–150)	99 (62.5-148.5)	122 (68.5-152.5)	0.591
ORT (min), median (IQR)	418(290-504.5)	310 (226.75–426)	458 (351-536.5)	0.242
PRT (min), median (IQR)	62 (51-82.5)	58 (38.75–66.25)	63 (53.5–94.5)	0.148
Prognostic score for BAO on DSA
PcoA, median (IQR)	1 (0–2)	1.5 (0–2)	0 (0–1)	0.019
BATMAN score, median (IQR)	4 (2–6)	4.5 (3.75-6)	3 (2–5)	0.001
BAPCOR score, median (IQR)	7 (5–9)	9 (7.75–10.25)	6 (5–8)	0.000
BAO: basilar artery occlusion; BA: basilar artery; LA: large-artery atherosclerosis; CE: cardioembolism; SUE: undetermined etiology; OPT: Onset-to-puncture time; DPT: Door-to-puncture time; ORT: Onset to recanalization time; PRT: Puncture-to-recanalization time; DSA: digital subtraction angiography; PcoA: posterior communicating artery.

Table 2

Angiographic characteristics and endovascular procedure
Basilar occlusion site
Proximal BA& VBJ	15(12&3)
Mid-BA	25
Distal BA	7
Thrombectomy
SR	24
SR with balloon angioplasty only	9
SR with Stent angioplasty	10
SR with aspiration	1
ADAPT with stent angioplasty	1
Spontaneous recanalization	2
No. of SR (mean ± SD, range)	1.52 ± 0.93, 1–5
mTICI
0–2a (n, %)	7, 14.9%
2b–3 (n, %)	40, 85.1%
Anesthesia, general n (%)	6, 12.8%
Complications, n (%)	14, 29.8%
Symptomatic ICH (n, %)	5, 10.6%
SAH	3
fatal hemorrhage	2
Vessel reocclusion (fatal)	1
Tirofiban (n, %)	31, 76.0%
BA: basilar artery; VBJ: vertebrobasilar junction; SR: stent retriever; ICH: intracerebral hemorrhage; SAH: subarachnoid hemorrhage

Basilar artery segmentation

Basilar artery can be subdivided into three segments: the proximal segment (extending from the confluence of the vertebral arteries to the origin of the anterior inferior cerebellar arteries); the middle segment (extending from the origin of the anterior inferior cerebellar arteries to the origin of the superior cerebellar arteries); and the distal segment (extending from the origin of the superior cerebellar arteries to the top of the basilar artery) (Table 2).

BAPCOR score

In our study, the BAPCOR score is a 15-point semiquantitative scoring system based on DSA, designed to assess thrombus burden and collateral status (Fig. 1). The scoring system includes the following components: (1) Assessment of occlusion in the posterior circulation, with a maximum of 6 points allocated as follows: 1 point for the dominant vertebral artery for surgical approach, 1 point each for the distal, middle, and proximal basilar artery, and 1 point each for the P1 segment; (2) Evaluation of potential collateral pathways in the posterior circulation, with a maximum of 9 points assigned as follows: 1 point for the PICA from the dominant vertebral artery for surgical approach, 1 point each for the AICA, and 1 point each for the superior SCA, and 2 points for each patent posterior communicating artery (PCoA), and 1 point for a hypoplastic PCoA (caliber smaller than 1 mm) if retrograde blood flow can reach the distal basilar artery via the P1 segment, or 3 points for each fetal PCoA. Examples using the application of the BAPCOR scoring system are presented in Fig. 2.

In contrast to MRA or CTA, DSA stands out as the gold standard for cerebrovascular examination due to its exceptional resolution and precise dynamic visualization of blood flow, which aids in assessing collateral circulation of the cerebellar artery. Two trained neurologists at our stroke center independently reviewed the radiological images, blinded to the patient’s clinical features and prognosis. In case of discrepancy, the final BAPCOR score was determined through consensus with a third experienced senior neurointerventionalist.

Moreover, the BAPCOR score was compared with existing assessment of PcoA patency and the basilar artery on computed tomography angiography (BATMAN) score on DSA to determine whether it was superior in predicting favorable prognosis following EVT in patients with acute BAO (Fig. 3).

Statistical Analysis

Statistical analyses were performed using IBM SPSS version 20 software (IBM SPSS Statistics, Armonk, NY). For univariate analysis, the Mann–Whitney U test was performed for continuous variables, while the χ2 test or 2-sided Fisher exact test was used for categorical variables. Receiver operating characteristic (ROC) test was performed to evaluate the area under the curve (AUC) of the prediction and to identify the optimal cutoff value for distinguishing between good and poor clinical outcomes. To identify independent predictors of outcome, multivariate backward stepwise logistic regression was performed, with variables included if P < .05 in univariate analysis, in addition to age.

Between October 2016 to January 2019, 60 consecutive patients with acute BAO were treated with EVT at our hospital. Among them, 13 patients were excluded because of incomplete baseline data, missing imaging data, and loss of follow-up, resulting in the enrollment of 47 eligible patients for the analysis in this study. The baseline characteristics of these patients are presented in Table 1. The median NIHSS scores for the included patients was 19. The median age of the patients was 61 years, with female patients comprising 21.3% of the cohort. The median time from symptom onset to recanalization was 310 mins. Approximately 44.7% of the patients received intravenous thrombolysis with recombinant tissue plasminogen activator prior to undergoing EVT. The vast majority (87.2%) of strokes were attributed to large-artery atherosclerosis, while cardioembolism accounted for 10.6% of cases.

In the initial EVT approach, 43 patients (91.5%) received stent-retriever thrombectomy, with only 1 patient additionally receiving aspiration, and 2 experiencing spontaneous recanalization. Successful recanalization (modified thrombolysis in cerebral infarction [mTICI] 2b-3) was achieved in 40 patients (85.1%), with 34.0% (16/47) showing good outcomes (mRS score 0–2). Symptomatic intracranial hemorrhage, as per ECASS III criteria, occurred in 5 patients (10.6%), and fatal reocclusion post-recanalization was observed in 1 patient. Median BATMAN and BAPCOR scores on DSA were 4 and 7, respectively. Notably, pre-EVT BAPCOR scores were significantly higher in patients with mrs ≤ 2 compared to those with mrs > 2 after 90 days (9 vs 6, p = 0.000). Univariable analysis revealed that lower NIHSS score, intravenous thrombolysis before EVT, BATMAN score, and BAPCOR score were independently associated with 90-day clinical outcomes. The mRS distribution based on the categorized BAPCOR scores is presented in Fig. 4.

ROC analysis indicated that the AUC of the BATMAN-DSA score was 0.796 (95%CI: 0.658–0.935), with a cut-off value 4.5 for predicting poor outcomes, demonstrating a sensitivity of 0.688 and specificity of 0.871. Similarly, the BAPCOR score exhibited an AUC of 0.868 (95%CI: 0.753–0.983), with a cut-off value of 8.5 for predicting poor outcomes, showing a sensitivity of 0.688 and specificity of 0.935. Correlation analysis showed a moderate negative correlation between BAPCOR and mRS. Compared to the BATMAN score on DSA, the BAPCOR score for predicting poor outcomes demonstrated a larger AUC, higher Youden index, and correlation index.

In multivariate backward stepwise logistic regression analysis, which included BAPCOR scores higher than 8.5, baseline NIHSS score, and intravenous thrombolysis, BPC scores higher than 8.5 (odds ratio [OR], 12.603; 95% confidence interval [CI], 1.922–82.638; P = .008) emerged as independent predictors of favorable outcomes. Inter-rater agreement was substantial for the BAPCOR score (intraclass coefficient correlation, .902; 95% CI, 0.830–0.944).

This study evaluates the prognostic value of the BAPCOR scoring system on DSA for predicting clinical outcomes in patients treated with EVT for acute BAO. The results show that the BAPCOR score is a reliable predictor of clinical outcomes in acute BAO cases. Patients with higher BAPCOR scores are more likely to achieve favorable outcomes post-endovascular treatment at 3 months.

Numerous studies highlight the significance of collateral circulation in acute BAO cases [16], and assessing thrombus burden and collaterals in acute BAO plays an important role for determining prognosis and treatment efficacy. Collateral flow in BAO could originate from the anterior circulation through PCoAs, the posterior aspect of the C7 segment of the internal carotid artery (ICA), and anastomoses of cerebellar arteries. CTA and DSA are two commonly employed imaging modalities for identifying the culprit occlusive vessel and evaluating collateral flow in acute BAO patients. Favorable pretreatment collateral status has been associated to higher chances of positive outcomes following EVT for acute BAO. Ongoing efforts seek to standardize collateral assessment to facilitate more reliable and generalizable investigations into its clinical implications. Therefore, collaterals assessment represents a valuable aspect of acute BAO management, offering insights into predicting patient outcomes and informing treatment decisions.

CTA has become increasingly prevalent for collateral assessment in acute BAO due to its noninvasive nature, rapid imaging capabilities, and ability to visualize collateral flow from all vessels simultaneously. Several CTA-based grading systems have been used to assess thrombus burden and collateral flow, demonstrating predictive value for outcomes of acute BAO (Table 3). It is well documented that the presence of bilateral PcoA has been associated with a favorable prognosis following intravascular therapy [10]. van der Hoeven et al. [11] proposed the Posterior Circulation Collateration Score (PC-CS), mainly evaluating primary and secondary posterior circulation. Da Ros et al [12] assessed the extent of vertebrobasilar artery occlusion using the Vascular Computed Tomography Based Grading System in Posterior Circulation (PC-CTA). Additionally, Alemseged et al proposed the BATMAN score, which considers thrombus length and primary collateral circulation in acute BAO cases [13]. Their study showed that patients with a BATMAN score ≥ 7 are more likely to benefit from EVT and have favorable prognoses. However, the PC-CS, PC-CTA, and BATMAN scales predominantly rely on single-phase CTA images, which may be less sensitive to delayed collateral perfusion, thus inadequately reflecting collateral blood flow that fills slowly downstream of BAO.

Table 3

Comparison of prognostic score studies for acute basilar artery occlusion treated with endovascular thrombectomy.
	Year	Nomenclature	No. of cases	Total Scores	BAO length: P1/BA/V4	Primary collateral: PcoA	Secondary collaterals: SCA/AICA/PICA	Favorable outcome score
CTA
Goyal	2016	CS	21	2	/	+/+	-	2
van der Hoeven	2016	PC-CS	149	10	/	++/++	++/++/++	≥ 6
Da Ros	2016	PC-CTA	15	6	--/---/-	/	/	≤ 2
Alemseged	2017	BATMAN-CTA	73	10	++/+++/+	++/++	/	≥ 7
DSA
Yang	2018	BATMAN-DSA	63	10	++/+++/+	++/++	/	≥ 3
Shen	2024	BAPCOR	47	15	++/+++/+	++/++	++/++/+	≥ 8.5
+: 1 point for presence of artery; -: 1 point for absence of artery.

CTA still faces limitations in assessment of collateral circulation in posterior circulation stroke due to an incomplete understanding of its hemodynamics [17]. As the gold standard for diagnosing cerebrovascular disease, DSA offers superior spatial and temporal resolution, dynamically displaying blood flow direction and velocity, thus providing richer information. Although DSA-based ASITN/SIR scale [18] has been initially applied for posterior circulation strokes, it lacks specificity for acute BAO, and the PCoA scale overlooks the leptomeningeal anastomoses from the anterior circulation and cerebellar arteries.

Through investigation of the BATMAN score on different imaging modalities, Yang et al. [14] found that a BATMAN-DSA score ≥ 3 may be associated with good prognosis, which is much lower than the threshold of BATMAN-CTA ≥ 7. In our study, we further verified that a BATMAN-DSA score ≥ 4.5 is an independent predictor of a good prognosis. Moreover, the BAPCOR grading system for acute BAO offers a more comprehensive interpretation of the correlation between collateral circulation and good prognoses, encompassing thrombus burden, primary, and secondary collateral circulation. Similarly, the DSA-based angiographic collateral grading system for BAO (ACGS-BAO) emphasized the significance of the top of the BA in predicting EVT outcomes [15]. Both BAPCOR and ACG-BAO provide richer collateral circulation information, enhancing the comprehensiveness and reliability of assessing clinical outcomes in acute BAO treated with EVT.

Following the greenway mode of stroke in our stroke center, we adopted a comprehensive imaging approach combining “CT + DWI + MRA + DSA” to assess patients suspected of acute posterior circulation infarction due to large vessel occlusion. Specifically, DWI accurately detected the site of posterior circulation infarction, while MRA identified the presence of large vessel occlusion. Rapid pre-treatment DSA was utilized to pinpoint the culprit occlusive vessel and evaluate collateral circulation, providing valuable information for the surgical team. In addition, whenever feasible, local anesthesia was preferred to expedite DPT or DRT.

The BATMAN scoring system assesses the length of thrombus and primary collateral, whereas the BAPCOR scoring system offers better prediction for acute BAO by evaluating the length of thrombus, primary, and secondary collaterals. A higher BAPCOR score indicates a shorter thrombus or better collateral circulation, potentially correlating with a good clinical outcome in patients with acute BAO.

The main limitations of this study include its retrospective design at a single center, the relatively small sample size, and potential selection bias. In addition, the use of aspiration as the first-line EVT technique was relatively uncommon.

In our study, the BAPCOR score appears to be associated with outcomes in acute BAO treated with EVT, similar to the presence of bilateral PcoA and BATMAN score on DSA. However, it demonstrated superiority in reflecting collateral status and thrombus burden compared to the latter.

Conflicts of interest

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

Funding statement

This study received no external funding support.

Author Contribution

Conceptualization: GS, JZ, GN. Data collection: YM, ZP. Writing-original draft: GS, JZ. Writing-review & editing: YM, LZ, LC, KL, GN. Approval of final manuscript: all authors.

Data Availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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No competing interests reported.

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You are reading this latest preprint version

Basilar artery and posterior circulation collaterals score on digital subtraction angiography predicts prognosis for acute basilar artery occlusion treated with endovascular thrombectomy

Status:

Version 1

Abstract

Background and purpose

Methods

Results

Conclusion

Figures

Introduction

Methods

Clinical materials

Basilar artery segmentation

BAPCOR score

Statistical Analysis

Results

Discussion

Conclusion

Declarations

Conflicts of interest

Funding statement

Author Contribution

Data Availability

References

Additional Declarations

Supplementary Files

Status:

Version 1