Predicting final infarct size and clinical outcomes in patients with acute ischemic stroke after endovascular thrombectomy using the Alberta Stroke Program early CT score on venous-phase CT

Abstract

Background

The Alberta Stroke Program Early Computed Tomography Score (ASPECTS) is a semi-quantitative tool for evaluating the extent and distribution of early ischemic changes.

Purpose

To assess the value of ASPECTS on non-contrast CT (NCCT), arterial-phase CT (APCT), or venous-phase CT (VPCT) in predicting the final infarct core (IC) on follow-up diffusion-weighted imaging (DWI) and the clinical outcomes of patients with acute ischemic stroke (AIS) after endovascular thrombectomy (EVT).

Material and Methods

In total, 120 patients with AIS who underwent EVT in our center were retrospectively enrolled. Correlations between CT-ASPECTS and follow-up DWI-ASPECTS were analyzed using Spearman's rank correlation coefficient. Mean differences and limit of agreement (LoA) between CT-ASPECTS and follow-up DWI-ASPECTS were assessed using the Bland–Altman plots. Multivariate logistic regression and receiver operating characteristic curve analyses were used to identify independent factors and evaluate their performances in predicting the clinical outcomes.

Results

VPCT-ASPECTS exhibited the highest correlation with follow-up DWI-ASPECTS (r = 0.846, P < 0.001), followed by APCT-ASPECTS (r = 0.613, P < 0.001) and NCCT-ASPECTS (r = 0.557, P < 0.001). The mean difference between VPCT-ASPECTS and follow-up DWI-ASPECTS was 0.0 (limit of agreement = −2.1 to 2.1). National Institute of Health Stroke Scale (NIHSS) scores at admission (NIHSS_pre) (odds ratio [OR]=1.162, 95% confidence interval [CI]=1.063–1.270; P = 0.001) and VPCT-ASPECTS (OR=0.728, 95% CI=0.535–0.991; P = 0.044) were the independent factors associated with clinical outcomes. The combined model integrating NIHSS_pre and VPCT-ASPECTS exhibited an excellent performance in predicting good clinical outcomes (area under curve [AUC]=0.807; sensitivity=75.0%; specificity=72.3%).

Conclusion

VPCT-ASPECTS may be a promising imaging biomarker to predict the final IC and the clinical outcome of the patients with AIS after EVT.

Keywords

Acute ischemic stroke endovascular thrombectomy computed tomography Alberta Stroke Program early CT score

Introduction

Acute ischemic stroke (AIS) deserves attention because of its high rates of morbidity, disability rate, and mortality worldwide. Endovascular thrombectomy (EVT) has been identified as an important treatment strategy for the patients with AIS due to anterior large vessel occlusion (LVO) (1 –5). However, even if successful recanalization is achieved, more than 50% of patients cannot achieve a good outcome at 3 months after treatment (1,2). The volume of baseline infarct core (IC) has been fully proven to be a useful imaging marker that can help to predict the prognosis of patients with AIS. Diffusion-weighted imaging (DWI) has been viewed as the gold standard for accessing the IC (6); however, it is not always available, especially in the emergency setting (7). Computed tomography perfusion (CTP) is another choice of imaging modality for quantifying the IC (8). However, it is limited by the relatively higher failure rate of imaging scans, the need for sophisticated postprocessing software, and the potential overestimation of IC (9,10). Therefore, finding a simple, reproducible, and effective method to quantify the IC, and to predict the clinical outcomes of the patients with AIS is urgently required in clinical practice.

The Alberta Stroke Program Early CT Score (ASPECTS) is a semi-quantitative tool for evaluating the extent and distribution of early ischemic changes in the middle cerebral artery (MCA) territory (11). The MCA territory is divided into 10 regions (caudate, lentiform, the nucleus, internal capsule, insula, and M1–M6), and each region represents 1 point (11). One point is subtracted for a defined region if focal parenchymal hypo-attenuation on CT or hyperintensity on follow-up DWI occurs compared with the mirror region in the contralateral hemisphere. Previous studies have demonstrated that ASPECTS was associated with the IC and the subsequent clinical outcomes (12,13). Initially, ASPECTS is assessed based on the non-contrast CT (NCCT) (11); however, the lower interrater agreement is the main disadvantage of the ASPECTS based on NCCT (14,15). A previous study has reported that, after endovascular treatment, ASPECTS on arterial-phase CT (APCT) could better predict the IC than ASPECTS on NCCT (16). A contrast agent is required during an APCT scan, which can detect the alterations in cerebral blood volume and enlarge the difference in tissue density between ischemic and normal brain tissues (17). Therefore, APCT-ASPECTS exhibits a higher correlation with the final IC than NCCT-ASPECTS. Subsequently, some further studies have reported that APCT can overestimate the IC because of the slow collateral flow. By contrast, after the blood flow arrives at the ischemic tissue via slow collateral flow, computed tomography angiography (CTA) in the venous phase is more likely to reflect the hemodynamic state, and ASPECTS on venous-phase CT (VPCT) can better represent the final IC (18). However, its prognostic value is not analyzed together with the other demographic and clinical variables.

Therefore, the aims of the present study were to assess the relationship between the ASPECTS on NCCT, APCT, or VPCT and that on follow-up DWI, and to investigate the prognostic value of the ASPECTS on CT of the optimal phase in predicting the clinical outcomes of the patients with AIS after EVT.

Material and Methods

Study populations

The study was approved by the First Hospital of Nanjing Medical University's ethical committee for studies in humans (2023-SRFA-216). The requirement for informed consent was waived because of the retrospective nature of this study.

We enrolled 592 patients who underwent EVT in our center between October 2019 and June 2022. We included the following patients: (i) those who had the occlusion of the MCA segment 1 or 2 (M1 or M2) and/or the internal carotid artery (ICA); (ii) those who achieved a successful recanalization that was defined as a grade 2b or 3 of the modified Treatment In Cerebral Infarction (mTICI) scale (19); (iii) those who underwent NCCT and CTP for pre-treatment evaluation; (iv) those who underwent DWI within 1 week after EVT; and (v) those who had a clinical assessment of modified Rankin Scale (mRS) score at 90 days after EVT. We excluded patients for the following reasons: (i) incomplete clinical or demographic information; and (ii) image quality was not adequate for subsequent analysis. Finally, we enrolled 120 patients in our study.

Clinical variables

The following clinical variables were collected from our database: sex; age; history of hypertension; diabetes mellitus; hyperlipidemia; atrial fibrillation; and smoking. Further, National Institute of Health Stroke Scale (NIHSS) scores at admission (NIHSS_pre) and those at 24 h after EVT (NIHSS_24h), onset-to-door time (ODT), door-to-puncture time (DPT), and the functional outcome at 90 days after EVT were also collected. A good functional outcome was defined as a mRS score of 0–2 at 90 days after EVT (3).

Image acquisition

In our center, baseline CT protocol for the patients with AIS included NCCT and CTP scans. CT scans were performed by using a 128-slice multidetector CT scanner (Optima CT 660; GE Healthcare, Boston, America). NCCT was acquired in axial sections using the following parameters: 120 kVp; 100–350 mAs; and a thickness of 5 mm. The mean volume CT dose index (CTDIvol) and dose-length product (DLP) were 41.41 mGy and 687.69 mGy*cm, respectively. The scanning parameters for CTP were as follows: 100 kVp; 200 mAs; rotation time = 0.4 s; 0.984 maximum pitch; four-dimensional adaptive spiral mode; periodic spiral approach; 80 mm in the z-axis; delay of 2 s; 1.7 s temporal resolution; and 30 consecutive spiral scans. The total examination time of one CTP scan was 53 s. The mean CTDIvol and DLP of the CTP scan were 315.67 mGy and 2998.84 mGy*cm, respectively. During the CTP examination, a 50-mL bolus of iodine contrast agent (iopromide, Ultravist 370; Bayer Schering Pharma, XX, XX) was administered at a rate of 5 mL/s, followed by 30 mL of saline at the same rate.

MRI was performed using a 3.0-T unit (Magnetom Skyra; Siemens Healthcare, XX, XX) within 1 week after EVT. Axial DWI was included in the MRI protocol and scanned using the following parameters: b value = 0 and 1000 mm²/s; repetition time (TR) = 6400 ms; echo time (TE) = 98 ms; field of view (FOV) = 220 × 220 mm; matrix = 192 × 192; slice thickness = 4 mm; and number of slices = 20.

Image analysis

After the regions of interest were automatically placed on the distal ICA and sigmoid sinuses, the curves of arterial input function (AIF) and venous input function (VIF) could be generated. According to the method reported by Menon et al. (10), APCT was reconstructed from the peak phase of the AIF curve, and VPCT was reconstructed from the peak phase of the VIF curve. Both APCT and VPCT were reconstructed as a slice thickness of 0.625 mm.

All ASPECTS were independently evaluated by two radiologists (with 3 and 10 years of experience in neuroradiology, respectively) who were blinded to clinical information and study design. We first evaluated the ASPECTS on NCCT, followed by APCT, VPCT, and follow-up DWI. We excluded remote infarcts and chronic lesions from the evaluation. In the event of any disagreement, a consensus score was obtained by a third senior radiologist (with 28 years of experience in neuroradiology).

Statistical analysis

The interrater agreements for evaluating the ASPECTS on NCCT, APCT, VPCT, and follow-up DWI were assessed using the intraclass correlation coefficient (ICC), and the values closer to 1.0 represented better reproducibility. Correlations between NCCT-ASPECTS, APCT-ASPECTS, VPCT-ASPECTS, and follow-up DWI-ASPECTS were assessed using Spearman's correlation analyses. The r values were interpreted as follows: 0–0.2 = poor; 0.2–0.4 = fair; 0.4–0.6 = moderate; 0.6–0.8 = substantial; and 0.8–1.0 = perfect (20). Mean differences and limit of agreement (LoA) between NCCT-ASPECTS, APCT-ASPECTS, or VPCT-ASPECTS and follow-up DWI-ASPECTS were assessed using the Bland–Altman plots and ICC (21). Continuous variables were presented as mean ± standard deviation (SD) if normally distributed, or as median and interquartile range (IQR) if non-normally distributed. Categorical variables were expressed as frequencies (percentages). Comparisons of categorical variables between the good and poor outcome groups were performed using the independent-samples t-test or Mann–Whitney U-test, whereas comparisons of categorical variables between two groups were evaluated using the chi-square test or Fisher's exact test, as appropriate. The variables with P < 0.05 at univariate analysis were enrolled into further multivariate logistic regression analysis to determine the independent variables associated with the clinical outcome. Logistic regression was used to integrate the independent variables to establish the combined model. Receiver operating characteristic (ROC) curve analyses were performed to evaluate the performance of significant variables alone and their combination for predicting the functional outcomes at 90 days after EVT. Statistical analyses were performed using SPSS software version 25.0 (IBM Corp., Armonk, NY, USA) and MedCalc software version 12.3.0. A two-tailed P value < 0.05 was considered statistically significant.

Results

Baseline characteristics

A total of 120 eligible patients (90 men; mean age = 65.0 ± 12.3 years) were enrolled. Among them, 85 (70.8%) patients had a history of hypertension, 24 (20.0%) had a history of diabetes, 21 (17.5%) were smokers, and 30 (25.0%) had a history of atrial fibrillation. In total, 22 patients experienced occlusion of the ICA, 75 of the MCA, or 23 patients of the ICA combined with the MCA. The mean NIHSS_pre score was 11.9 ± 6.5 and the mean NIHSS_24h score was 8.5 ± 7.7. The ODT and DPT were 363.0 ± 272.7 min and 92.8 ± 110.2 min, respectively. In total, 94 (78.3%) patients obtained a good outcome at 90 days after EVT. The baseline characteristics of the enrolled patients are shown in Table 1.

Table 1.

Baseline clinical and imaging characteristics of our study cohort.

Characteristics	Value
Men	90 (75.0)
Age (years)	65.0 ± 12.3 (57.0–74.0)
NIHSS_pre	11.9 ± 6.5 (7.0–16.0)
NIHSS_24h	8.5 ± 7.7 (2.24–12.75)
Vessel occlusion
Intracranial ICA	22 (18.3)
MCA	75 (62.5)
ICA + MCA	23 (19.2)
ODT (min)	363.0 ± 272.7 (159.75–538.50)
DPT (min)	92.8 ± 110.2 (66.25–90.00)
Hypertension	85 (70.8)
Diabetes	24 (20.0)
Hyperlipidemia	1 (0.8)
Smoker	21 (17.5)
Atrial fibrillation	30 (25.0)
Good outcome at 3 months	94 (78.3)
NCCT-ASPECTS	9 (8.0–10.0)
APCT-ASPECTS	7 (6.0–9.0)
VPCT-ASPECTS	7 (6.0–9.0)
DWI-ASPECTS	8 (6.0–9.0)

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

Good outcome at 3 months was defined as a modified Ranking score of 0–2 at 90 days after EVT.

APCT, arterial-phase CT; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; DPT, door-to-puncture time; DWI, diffusion-weighted imaging; ICA, internal carotid artery; IQR, interquartile range; MCA, middle cerebral artery; NCCT, non-contrast CT; NIHSS_pre, National Institutes of Health Stroke Scale at admission; NIHSS_24h, National Institutes of Health Stroke Scale 24 h after treatment; ODT, onset-to-door time; SD, standard deviation; VPCT, venous-phase CT.

Correlations between ct-ASPECTS and follow-up DWI ASPECTS

Good interrater agreement was obtained in the evaluation of NCCT-ASPECTS (ICC = 0.695), and excellent inter-rater agreements were achieved in the assessment of APCT-ASPECTS (ICC = 0.873), VPCT-ASPECTS (ICC = 0.875), and follow-up DWI-ASPECTS (ICC = 0.897).

The baseline median NCCT-ASPECTS was 9 (IQR = 8–10), APCT-ASPECTS was 7 (IQR = 6–9), VPCT-ASPECTS was 7 (IQR = 6–9), and follow-up DWI-ASPECTS was 8 (IQR = 6–9). VPCT-ASPECTS exhibited an almost perfect correlation with follow-up DWI-ASPECTS (r = 0.846; P < 0.001) and the ICC was 0.837. APCT-ASPECTS exhibited a substantial correlation with follow-up DWI-ASPECTS (r = 0.613; P < 0.001) and the ICC was 0.607. NCCT-ASPECTS exhibited a moderate correction with follow-up DWI-ASPECTS (r = 0.557; P < 0.001) and the ICC was 0.455 (Fig. 1). The mean difference between NCCT-ASPECTS, APCT-ASPECTS, or VPCT-ASPECTS and follow-up DWI-ASPECTS was −1.1 (LoA = −4.3 to 2.0), 0.1 (LoA = −3.1 to 3.3), and 0.0 (LoA = −2.1 to 2.1), respectively (Fig. 2). A representative case is shown in Fig. 3.

Fig. 1.

Correlations between (a) NCCT-ASPECTS, (b) APCT-ASPECTS, or (c) VPCT-ASPECTS and follow-up DWI-ASPECTS. VPCT-ASPECTS showed the highest correlation with follow-up DWI-ASPECTS (r = 0.846, P < 0.001), followed by APCT-ASPECTS (r = 0.613, P < 0.001) and NCCT-ASPECTS (r = 0.557, P < 0.001). APCT, arterial-phase CT; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; DWI, diffusion-weighted imaging; NCCT, non-contrast CT; VPCT, venous-phase CT.

Fig. 2.

Bland–Altman plots of (a) NCCT-ASPECTS, (b) APCT-ASPECTS, or (c) VPCT-ASPECTS vs. follow-up DWI-ASPECTS. APCT, arterial-phase CT; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; DWI, diffusion-weighted imaging; NCCT, non-contrast CT; VPCT, venous-phase CT.

Fig. 3.

A 42-year-old male patient with acute ischemic stroke due to occlusion of the left MCA. (a) NCCT revealed a hypoattenuation in the insula, yielding an ASPECTS of 9. (b) APCT revealed hypoattenuations in the insula, M2 territory, M5 territory, and M6 territory yielding an ASPECTS of 6. (c) VPCT revealed hypoattenuations in the insula and M2 territory, yielding an ASPECTS of 8. The occluded vessel was completely recanalized (TICI 2c) after EVT. (d) Follow-up DWI revealed hyperintensities in the insula and M2 territory, yielding an ASPECTS of 8, and the mRS score was 0 at 90 days. APCT, arterial-phase CT; ASPECTS, Alberta Stroke Program Early Computed Tomography Score; DWI, diffusion-weighted imaging; MCA, middle cerebral artery; mRS, modified Rankin score; NCCT, non-contrast CT; VPCT, venous-phase CT.

Variables associated with clinical outcome

Because of the superior correlation and smaller difference between VPCT-ASPECTS and follow-up DWI-ASPECTS, we only adopted VPCT-ASPECTS into further grouped comparison and multivariate logistic regression analysis. In the grouped comparison, patients with good outcomes showed significantly younger age (63.79 ± 12.69 vs. 69.42 ± 9.97 years; P = 0.039), lower NIHSS_pre (10.52 ± 6.07 vs. 17.04 ± 5.61; P < 0.001), lower NIHSS_24h (6.91 ± 6.76 vs. 14.23 ± 8.07; P < 0.001), and higher VPCT-ASPECTS (8 [6–9] vs. 7 [5–8]; P = 0.004) than those with poor outcomes. For the remaining variables, no significant difference was found between the good and poor outcome groups (all P > 0.05) (Table 2).

Table 2.

Independent clinical and imaging variables associated with the outcome.

	Univariate analysis			Multivariate analysis
Variables	Good outcome(n = 94)	Poor outcome(n = 26)	P	OR (95% CI)	P
Men	72 (76.6)	18 (69.2)	0.443
Age (years)	63.79 ± 12.69	69.42 ± 9.97	0.039
ODT (min)	353.26 ± 264.67	398.12 ± 302.91	0.460
DPT (min)	94.57 ± 120.11	86.54 ± 63.80	0.744
NIHSS_pre	10.52 ± 6.07	17.04 ± 5.61	<0.001	1.162(1.063–1.270)	0.001
NIHSS_24h	6.91 ± 6.76	14.23 ± 8.07	<0.001
Hypertension	63 (67.0)	22 (84.6)	0.081
Hyperlipidemia	1 (1.1)	0 (0.0)	1.000
Diabetes	18 (19.1)	6 (23.1)	0.658
Smoker	17 (18.1)	4 (15.4)	1.000
Atrial fibrillation	23 (24.5)	7 (26.9)	0.798
VPCT-ASPECTS	8 (6–9)	7 (5–8)	0.004	0.728(0.535–0.991)	0.044

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

ASPECTS, Alberta Stroke Program Early Computed Tomography Score; CI, confidence interval; DPT, door-to-puncture time; IQR, interquartile range; NIHSS_pre, National Institutes of Health Stroke Scale at admission; NIHSS_24h, National Institutes of Health Stroke Scale 24 h after treatment; ODT, onset-to-door time; OR, odds ratio; SD, standard deviation; VPCT, venous-phase CT.

Multivariate logistic regression analysis indicated that NIHSS_pre (odds ratio [OR] = 1.162, 95% confidence interval [CI] = 1.063–1.270; P = 0.001) and VPCT-ASPECTS (OR = 0.728, 95% CI = 0.535–0.991; P = 0.044) were independently associated with the clinical outcome and were used to establish a combined model. The combined model (NIHSS_pre+ VPCT-ASPECTS) exhibited an optimal performance in predicting a good outcome (AUC = 0.807; sensitivity = 75.0%; specificity = 72.3%), followed by NIHSS_pre alone (AUC = 0.799; sensitivity = 76.9%; specificity = 74.5%) and VPCT-ASPECTS alone (AUC = 0.682; sensitivity = 38.5%; specificity = 90.4%) (Fig. 4).

Fig. 4.

Diagnostic performances of NIHSS_pre, VPCT-ASPECTS, and their combined model in predicting the clinical outcome. ASPECTS, Alberta Stroke Program Early Computed Tomography Score; NCCT, non-contrast CT; VPCT, venous-phase CT.

Discussion

The present study has several main findings. First, compared with NCCT-ASPECTS and APCT-ASPECTS, VPCT-ASPECTS correlated well with follow-up DWI-ASPECTS. The mean difference between VPCT-ASPECTS and follow-up DWI-ASPECTS was smaller. Second, together with NIHSS_pre, VPCT-ASPECTS was found to be the independent factor associated with the patients’ outcomes. Third, after integrating NIHSS_pre and VPCT-ASPECTS, an excellent performance was obtained in predicting the good clinical outcomes of the patients with AIS after EVT. Our study indicates that VPCT-ASPECTS can serve as a simple, reproductive, and effective method to quantify the IC and to predict the clinical outcomes of the patient with AIS. Based on our study, we suggest that VPCT-ASPECTS should be referred before an emergency treatment decision is made for patients with AIS, and further artificial intelligence-based software could be established based on VPCT for quantifying the ASPECTS.

ASPECTS is a simple and effective tool for assessing the location and extent of early ischemic changes in the anterior circulation, which is usually evaluated based on NCCT. Previously published studies reported the association between baseline ASPECTS and the volume of the ischemic core (22,23). Nannoni et al. reported that there was a moderate correlation between ASPECTS and the volume of ischemic core calculated based on CTP (22). The correlations were more obvious in the patients in the late window and in the presence of large vessel occlusion (23). However, the interrater variability was a major limitation of ASPECTS based on NCCT, especially in the region of the internal capsule (24).

In addition to NCCT, CTA is another imaging modality that is typically used in patients with AIS to evaluate the status of intracranial large vessel and collateral circulation. Different from the hypo-attenuation on NCCT, which indicates the shift of water content in brain tissue, the hypo-attenuation on the source images of CTA mainly demonstrates the alternation of cerebral blood flow reflected as a decrease in contrast enhancement. A large number of water shifts are required for visible hypo-attenuation to human eyes on NCCT, whereas CTA may more quickly and clearly show the difference in cerebral flow between ischemic and normal brain tissues. Therefore, these mechanisms may explain our results that there were better inter-rater agreements when assessing APCT-ASPECTS and VPCT-ASPECTS, and that there were stronger correlations and fewer differences between APCT-ASPECTS or VPCT-ASPECTS and follow-up DWI-ASPECTS.

With regard to the comparison between APCT and VPCT, Cheng et al. reported an almost perfect correlation between CTA venous-ASPECTS and follow-up CT-ASPECTS, which was better than that in CTA arterial-ASPECTS and NCCT-ASPECTS (18). This result was also confirmed by our study. Previous studies have demonstrated that collateral status was a very important factor associated with the process of ischemic core, and better collateral was usually related to a slower infarct progression (25). During the APCT, the contrast agent may not traverse the collateral and reach the distal bed, which may lead to an overestimation of the final infarct. By contrast, VPCT contained information on the hemodynamic state, collateral status, and overall tissue perfusion. Therefore, it appeared to reflect the final perfusion status in patients with AIS.

As a measure of the severity of neurological deficits, NIHSS has been proven to be effective in identifying patients with AIS. The prognostic value of both NIHSS_pre and NIHSS_24h had also been fully studied in previous studies (13,26 –28). In line with previous studies, our study also found that both NIHSS_pre and NIHSS_24h were associated with functional independence at 90 days in the univariate analysis. However, only NIHSS_pre was identified as an independent predictor in multivariate analysis, whereas NHISS_24h was not, which was in line with one previous study (29). By contrast, some other studies indicated that NHISS_24h was more valuable than NIHSS_pre in predicting clinical outcomes (30). This discrepancy may be caused by the different sample sizes and composition of the study population.

In the multivariate logistic regression analysis, our study found that NIHSS_pre and VPCT-ASPECTS were independent variables associated with the clinical outcome. NIHSS_pre reflected the clinical status of the patients, whereas VPCT-ASPECTS integrated the volumetric and hemodynamic information of the ischemic lesion itself. Therefore, it was not surprising that combining these two variables could further improve the performance in predicting the clinical outcome. This result indicates that NIHSS_pre and VPCT-ASPECTS should be principally considered when we need to make a treatment decision in the emergency setting for patients with AIS.

The present study has some limitations. First, this was a retrospective study with a limited sample size and was conducted in a single center. Second, the follow-up DWI was used to define the final infarct extent. In clinical practice, only the patients with relatively better outcomes could accept follow-up MRI evaluation. This situation could inevitably lead to selection bias in our study.

In conclusion, our study indicated that VPCT-ASPECTS correlated well with the final infarction extent after EVT. It may be a promising imaging biomarker that could be integrated with other clinical and serological variables, for predicting the final infarction extent and clinical outcomes of patients with AIS after EVT.

Footnotes

Data availability

The raw data of this article is available upon reasonable request from the corresponding author (FYW).

Declaration of conflicting interests

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

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Nanjing Post-doctoral Science Foundation (X-QX); Jiangsu Province Capability Improvement Project through Science, Technology and Education (JSDW202243 to H-BS); Jiangsu Provincial Special Program of Medical Science (BE2021604 to X-QX); and the National Natural Science Foundation of China (82471945 to X-QX).

ORCID iDs

Hai-Bin Shi

Xiao-Quan Xu

Fei-Yun Wu

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