Risk factors for poor outcomes of mechanical thrombectomy after anterior circulation large vessel occlusion-related acute ischemic strokes

Abstract

METHODS

Patients (N = 313) undergoing MT within a specified time window after onset of ACLVO-related AIS provided clinical and radiologic data for analysis. Clinical endpoints were symptomatic intracranial hemorrhage (sICH) and 90-day functional outcome (scored by modified Rankin Scale [mRS]). Logistic regression was invoked to identify links between clinical/radiologic parameters and clinical outcomes.

RESULTS

Mean age of patients was 64.0 ± 12.2 years, and women accounted for 29.4%. The median National Institute of Health Stroke Scale [NIHSS] score was 15.2 (interquartile range [IQR]: 12–18). In multivariable analysis, initial Alberta Stroke Program Early CT Score (ASPECTS) determination (odds ratio [OR] = 0.748, 95% confidence interval [CI]: 0.604–0.926; p = 0.008), hyperdense middle cerebral artery sign (HMCAS) (OR = 0.463, 95% CI: 0.238–0.899; p = 0.023), early imaging signs of infarct (OR = 2.837, 95% CI: 1.285–6.263; p = 0.01), baseline NIHSS score (OR = 1.195,95% CI: 1.091–1.309; p < 0.001), age (OR = 1.082,95% CI:1.047–1.118; p < 0.001), and glycosylated hemoglobin (HbA1c) concentration (OR = 1.293, 95% CI: 1.084–1.543; p = 0.004) proved independently predictive of poor clinical outcomes (mRS scores > 2).

CONCLUSIONS

A number of factors, including initially determined ASPECTS, HMCAS, early imaging signs of infarct, baseline NIHSS score, age, and HbA1c concentration, appear to predict poor outcomes of MT after ACLVO-related AIS.

Introduction

After several randomized endovascular therapy trials aimed at patients with acute ischemic strokes (AIS) consistently showed the clinical benefit of mechanical thrombectomy (MT), this has become the standard of care for patients with anterior circulation large vessel occlusion (ACLVO)-related AIS [1–4]. For various reasons, however, many such patients (40–60%) may not experience functional improvement after MT [5–7]. MT prognosticators and efficacy are thus in need of clarification at present. Defining the relations between clinical and radiologic variables and patient prognosis may help physicians improve treatment in this setting.

Duo to non-contrast computed tomography (NCCT) scanning with the advantages of wide acceptability, economy, convenience, rapidity and easing operation, NCCT now still was the presently main examination method to assess stroke. Early imaging signs of infarct are useful to identify cerebral infarction and reflect ischemic edema. If hypoperfusion is profound, with values below 10–15 ml/ (100g*min), ischemic edema will occur early and early imaging signs of infarct will appear. A normal CT scan in a patient with stroke indicates a lesser degree of hypoperfusion and implies potential reversibility of the functional disturbance. According to these, previous studies have shown that early imaging signs of infarct on expeditiously obtained (ie, within 6 hours of stroke symptom onset) on NCCT may predict poorer functional outcomes and hemorrhagic transformation after thrombolysis [8]. Assessment of early imaging signs of infarct has thus been incorporated into established guidelines and consent forms for thrombolysis. However, the relationship between early imaging signs of infarct on NCCT and prognosis of MT in patients with ACLVO remained unclear. Because MT and thrombolysis for ACLVO-related AIS shared similar mechanism [3, 9], we hypothesized that early imaging signs of infarct may be related to the clinical outcomes of MT-treated AIS.

Moreover, other investigations have also demonstrated that initial Alberta Stroke Program Early CT Score (ASPECTS) status, hyperdense middle cerebral artery sign (HMCAS), baseline National Institutes of Health Stroke Scale (NIHSS) scoring, age and glycosylated hemoglobin (HbA1c) concentration are associated with poor outcomes in patients with AIS of ACLVO origins who undergo MT [10–13]. However, each study has different focus and content, and the results of each study are also different. They all put forward some predictive factors and indicators of certain clinical value. Based on their research foundation, we add new content to our research, like early imaging signs of infarct, in order to early predict the possible situation of patients after MT and benefit for patients’ long-term outcomes. Therefore, in this study, we have subsequently analyzed such patient scenarios using a full complement of clinical and radiologic factors, the goal being further improvement in AIS treatment efficacy.

Methods

Patient Selection

In this observational study, we evaluated 313 patients admitted for emergent ACLVO conditions between January 2016 and January 2022. The hospital’s institutional review board approved our study protocol.

Qualifying patients had undergone MT and met the following inclusion criteria: (1) ACLVO, including intracranial ICA and M1/proximal M2 segments of MCA confirmed by CT or magnetic resonance angiography (MRA); (2) baseline NIHSS score ≥ 8; (3) prior modified Rankin Scale (mRS) stroke score ≤ 1; and (4) NCCT imaging within 6hours of admission; (5) acute ischemic stroke was confirmed by diffusion-weighted imaging (DWI) within 48h (some patients DWI data were obtained from post-treatment following up). Other brain abnormalities (ie, tumors, trauma, or preoperative hemorrhagic infarction) and age ≤ 18 years were grounds for exclusion.

Clinical Data Collection

In addition to age and sex, we retrieved data pertaining to past medical history (hypertension, diabetes mellitus, hyperlipidemia, atrial fibrillation/flutter, coronary artery disease, and prior stroke), current/prior tobacco use, and alcohol consumption. Vital signs on admission (diastolic blood pressure [DBP], systolic blood pressure [SBP]), D-dimer level, HbA1c concentration, and NIHSS scores were recorded as well.

Imaging Acquisition And Analysis

Standard NCCT was obtained on admission, using a Discovery CT750 HD scanner (GE Healthcare, Chicago, IL, USA) at the following settings: tube voltage, 100 kV; tube current, 120 mA; collimator width, 40mm; field of view, 25cm; layer thickness, 5 mm; layer spacing, 5 mm. Patients were placed supine, with upper limbs flat (aside the body) and the head inclined. MRI scan was performed on a 3.0T scanner (Discovery MR750; GE Healthcare, Chicago, IL, USA) using an eight-channel phased-array head coil. DWI parameters: repetition time (TR), 3,000 ms; echo time (TE), 65.3 ms; b-value, 1,000 s/mm2 and MRA parameters: TR, min; TE, 2.3 ms; flip angle, 20◦; slice thickness, 0.6 mm; intersection gap, 0 mm; FOV, 24 × 24 cm 2 ; matrix number, 256 × 256.

Early imaging signs of infarct were specific changes on NCCT images generated within 6 hours after onset of stroke symptoms, namely obscuration of lentiform nucleus (hypoattenuation, indistinct demarcation), cortical sulcal effacement (reduced contrast and muted gray-white boundary at edges of cortical sulci, creating localized mass effect), or loss of insular ribbon with obscuration of sylvian fissure (blurring of gray-white interface at lateral edge of insula) [8]. The HMCAS is a thromboembolic manifestation detectable by NCCT [14].

The ASPECTS is a semiquantitative measure of early ischemic changes, separating the MCA territory into ten regions of interest. A lower score indicates larger infarction volume and more severe ischemia, whereas a higher score suggests smaller infarction volume and less ischemic insult [15]. Baseline imaging information (including ASPECTS, HMCAS, and early imaging signs of infarct), follow-up images (after MT), and angiographic procedural images were evaluated by two neuroradiologists blinded to clinical data. Any inconsistencies were resolved through discussion to reach a consensus.

Study Outcomes

The primary endpoint of functional independence was indicated by mRS scoring of 2 points or less at 90 days. Patients of 90 days mRS were obtained by clinical follow-up at our center. Angiographic outcomes were assessed by modified Thrombolysis in Cerebral Infarction (mTICI) scale, scores ≥ 2b reflecting successful vessel recanalization immediately following MT (at least half of occluded artery perfused) and a score of 3 signaling complete recanalization. Safety outcomes were determined by presence/absence of symptomatic intracranial hemorrhage (sICH), defined as neurologic worsening (≥ 4 point rise in NIHSS score), or post-MT hemorrhage on NCCT within 24 hours. Cerebral edema (CED) was classified into three grades according to the CT appearance after MT. Mild CED (CED 1) was defined as focal edema up to 1/3 of the hemisphere; moderate CED (CED 2) was defined as focal edema greater than 1/3 of the hemisphere; and severe CED (CED 3) was defined as focal edema with midline shift. The signs of focal edema usually are defined as narrowing of the cerebrospinal fluid space, for example, effacement of cortical sulci or ventricular compression [16].

Results

Many of the 569 patients screened for eligibility were rejected due to lack of clinical information and imaging data (n = 94), posterior circulation stroke origins (n = 138), or baseline NIHSS scores < 8 (n = 24). Ultimately, there were 313 qualifying patients who underwent MT after AIS for anterior circulation large artery occlusions. The schematic depicting patient selection is shown in Fig. 1.

Baseline Patient Characteristics

Mean age of the study population was 64.0 years, with women accounting for 29.4% (92/313). The initial ASPECTS median was 7.6 (IQR: 6–9), the median baseline NIHSS score was 15.2 (IQR: 12–18), and reperfusion after MT succeeded in 231 patients (73.8%) (Table 1).

Clinical And Imaging Factors Linked To Poor Prognosis (Mrs Score > 2)

All eligible patients underwent 90-day follow-up assessments to determine long-term functional independence. Overall, 175 (55.9%) showed good functional independence at 90 days. Patients were then stratified into good prognosis (mRS scores 0–2) and poor prognosis (mRS scores > 2) groups to compare clinical baseline variables and radiologic parameters (Table 1).

Patients in the poor (vs good) prognosis group were older (68.2 ± 12.7 vs 60.2 ± 10.7 years; p < 0.001), with more serious presentations (mean baseline NIHSS score: 17.1 ± 5.0 vs 13. 8 ± 3.6; p < 0.001; mean initial ASPECTS: 6.7 ± 2.1 vs 8.2 ± 1.7; ; p < 0.001), higher HbA1c concentrations (8.6 ± 4.3% vs 6.6 ± 1.7%; p < 0.001), and steeper D-dimer levels (3.5 ± 5.0 mcg/mL vs 2.0 ± 2.6 mcg/mL; p < 0.001). Likewise, there were more patients with diabetes mellitus (34.1% [47/138] vs 22.9% [40/175]; p = 0.028), atrial fibrillation/flutter (44.9% [62/138] vs 32.0% [56/175]; p = 0.019), and current/prior drinking histories (41.3% [57/138] vs 53.7% [94/175]; p = 0.029). Patients of the poor (vs good) prognosis group more often presented with early imaging signs of infarct (78.3% [108/138] vs 46.9% [82/175]; p = 0.001), whereas HMCAS was less likely (49.3% [68/138 vs 69.7% [122/175]; p = 0.001). By comparison, ICA occlusions were more frequent (39.0% [41/138] vs 17.3% [36/175]; p < 0.001), with less inclination for ICA + MCA occlusions (20.0% [21/138] vs 26.9% [56/175]; p = 0.009). Finally, the mean number of device passes was greater (1.9 ± 1.0 vs 1.5 ± 0.8; p < 0.001), there were more unsuccessful (mTICI score of 0) reperfusions (15.2% [21/138] vs 2.3% [4/175]; p = 0.001) and fewer complete (mTICI score of 3) reperfusions (33.3% [46/138] vs 45.7% [80/175]; p = 0.027) of occluded vessels after MT. Thus, the rate of successful reperfusion was lower (65.9% [91/138] vs 80.0% [140/175]; p = 0.005), and the probability of developing sICH was less (32.6% [45/138] vs 39.2% [29/175]; p = 0.001). And patients were more likely to have CED3 (15.2% [21/138] vs 5.1% [9/175]; p = 0.003). Figure 2 summarizes the 90-day functional outcome analysis stratified by ASPECTS.

Multivariate Analysis

Once adjusted for confounding factors (variables of significance [p < 0.05] in univariate analysis), initial ASPECTS status (OR = 0.761, 95%CI: 0.616–0.940; p = 0.011), HMCAS (OR = 0.454, 95%CI: 0.237–0.870; p = 0.017), early imaging signs of infarct (OR = 2.803, 95%CI: 1.289–6.096; p = 0.009), baseline NIHSS score (OR = 1.169, 95%CI: 1.072–1.275; p < 0.001), age (OR = 1.081, 95%CI: 1.047–1.115; p < 0.001), and HbA1c concentration (OR = 1.275, 95%CI: 1.073–1.515; p = 0.006) proved to be independently predictive of a poor prognosis (mRS score > 2) by logistic regression (Table 2,Fig. 3).

Discussion

Herein, we have shown that 44% of patients with ACLVO-related AIS failed to achieve long-term functional independence after MT. Similar to other studies [17–20], this study concluded that predictors of poor clinical outcomes in multivariable analysis were related to stroke severity (low-level ASPECTS, high NIHSS score) and baseline characteristics (older age, higher HbA1c concentration, ICA + MCA non-occlusion). Furtherly, we found that absent HMCAS and early imaging signs of infarct were also independent predictors of clinical outcomes after MT.

MT has been found beneficial in most patients with ischemic stroke triggered by ACLVO, gaining wide acceptance and use in clinical practice [4]. However, the clinical merit of this approach is time dependent, so it is important to quickly and efficiently identify qualifying patients. NCCT imaging is generally undertaken to determine prognosis and select therapeutic candidates, achieving early detection of intracranial thrombi and gauging infarct extent [21]. Consequently, NCCT is still the most commonly used diagnostic method during admissions for stroke. Analyzing the relations between imaging indicators on NCCT and clinical prognosis may help delineate patient status and improve treatment effects.

ASPECTS is a 10-point semi-quantitative system devised to assess early ischemic changes on NCCT after anterior circulation AIS. As such, it may be utilized clinically to discern the most appropriate patients for stroke therapy [22]. Our findings indicate that patients are less likely to benefit from MT as the ASPECTS ranking declines. This observation is consistent with results of a subgroup analysis in the randomized, phase 3 MR CLEAN trials, showing a relation between baseline ASPECTS value and intra-arterial treatment effect. Past studies have also demonstrated that ASPECTS status correlates with infarct size, lower values denoting more extensive damage [23]. Higher (vs lower) ASPECTS values seem to reflect significantly better outcomes after endovascular thrombectomy as well [17].

The NIHSS score is another incremental measurement scale for stroke severity, serving as an independent predictor of functional outcomes. Higher NIHSS scores are known to correspond with more severe neurologic disability [22]. In multiple regression analysis of the NASA registry, NIHSS scoring was strongly linked with outcomes of MT, increasing the risk of a poor outcome approximately 4-fold [24]. We have similarly found the NIHSS score is an independent predictor of MT prognosis (OR = 1.169, 95%CI: 1.072–1.275; p < 0.001).

An important finding of the present study is that more patients of the poor (vs good) prognosis group (> 2 vs 0–2 mRS scores) showed early imaging signs of infarct (78.3% vs 46.9%; p = 0.001). In logistic regression, the latter also emerged as strongly predictive of MT outcomes (OR = 2.803, 95%CI: 1.289–6.096; p = 0.009). NCCT changes of cerebral infarction may be subtle during the first few hours after AIS, yet these vague irregularities are likely highly predictive of clinical outcomes [15]. Slightly density of lentiform nucleus and insular or convex cortex may be noted within hours after ischemic stroke onset, at times accompanied by nominal mass effects (such as narrowed sulci). The European Cooperative Acute Stroke Study (ECASS) has confirmed the importance of early CT ischemic changes in predicting intravenous thrombolytic benefit, demonstrating that patients with AIS and early imaging signs of infarct are at a higher risk of hemorrhagic transformation, cerebral edema, and thus poor prognosis [25]. Furthermore, the highly effective reperfusion efforts recorded in multiple endovascular stroke trials (HERMES) suggest that in patients with low ASPECTS values and hypodensity, sICH is four times more frequent, with more than one-third of ischemic MCA are as involved [26].

The HMCAS signals an embolus of MCA segment, seen as increased attenuation/density on NCCT. In the pre-thrombectomy era (or in absence of treatment), its presence was a hall mark of severe cerebral ischemia and poor functional outcomes in patients with strokes [27]. Our multivariate regression model has shown that HMCAS negatively correlates with clinical outcomes in patients with AIS undergoing MT (OR = 0.454, 95%CI: 0.237–0.870; p = 0.017). This particular finding is nonetheless supported by Kiddy et al., having claimed greater odds of disability and death in patients lacking HMCAS on admission NCCT studies [13]. The pathophysiologic underpinnings of our data may be rooted in components of the embolus itself. Upon systematic review, it seems that the HMCAS likely depicts an erythrocyte-predominant clot; whereas in its absence, afibrin/platelet-predominant clot prevails [28]. Kim et al. have suggested that despite the low prognostic implications of HMCAS in clinical outcomes after MT, its absence may imply in situ thrombotic occlusion due to atherosclerotic stenosis [29]. The less calcific components of atherosclerotic plaque ostensibly are devoid of density on NCCT [28]. We suspect that erythrocyte-rich emboli due to atherosclerosis are less calcific than fibrin/platelet-rich emboli and may be removed by MT more efficiently to achieve vascular recanalization.

Clinically, HbA1c determinations reflect average blood glucose levels during prior 3-month intervals (roughly), identifying patients with impaired glucose metabolism and chronic hyperglycemia [30]. High HbA1c concentration also emerged as an independent predictor of poor 90-day functional outcomes in our multivariable logistic regression model (OR = 1.275, 95%CI: 1.073–1.515; p = 0.006). This result is aligned with other research on patients undergoing endovascular thrombectomy, in whom every 10 mmol/mol increase in HbA1c heightened the odds of sICH, mortality, and functional independence by 33%, 26%, and 24%, respectively [18]. Precisely why elevated HbA1c adversely impacts clinical outcomes of thrombolysis or endovascular thrombectomy in this setting is perhaps the potential for post-stroke hyperglycemia to worsen reperfusion injury [11, 31]. Hyperglycemia is apt to enhance intracellular acidosis in the ischemic penumbra, with formation of free radicals. This then results in mitochondrial dysfunction and energy failure, which further exacerbate brain injury. Cerebral auto regulation may also be affected, inducing reperfusion damage and potential hemorrhagic change in infarcts. Moreover, hyperglycemia is an activator of matrix metalloproteinase 9, serving to aggravate malignant CED. Hence, high levels of HbA1c on admission should alert physicians treating post-MT malignant complications (intra cerebral hemorrhage and CED) to the likelihood of poor long-term functional independence.

Although we did not exclude elderly patients, studies on MT often set an upper age limit for participation. The mean age of our subjects overall was 64.0 years, rising significantly in the poor prognosis group (68.2 vs 60.2; p < 0.001). In multivariate logistic regression analysis, age was a strong predictor of clinical outcome in patients with ACLVO-related AIS undergoing MT (OR = 1.081, 95%CI: 1.047–1.115; p < 0.001). Many investigations have corroborated that advanced age is a key predictor of poor prognosis in patients with strokes. Unlike younger counterparts, older patients have poorer clinical outcomes due to more frequent adverse comorbidities and less functional reserve [32]. Relevant studies have shown that endovascular thrombectomy may significantly improve clinical outcomes for advanced age patients of this sort, more so than intravenous thrombolysis [19]. However, higher age is still linked to a lower rate of functional independence and higher rates of sICH and mortality, regardless of treatment modality. Also, vascular access may not be achievable in elderly patients due to aging-related stiffness and to rtuosity of the aorta and large vessels [20].

Our study has certain notable limitations. This was a single-center, observational, and retrospective analysis of patients meeting current MT guidelines. The results are therefore not applicable beyond the boundaries specified. Our sampling of patients with ASPECTS of 0–5 was also undersized; and our analysis did not include MRI related indicators (DWI volume, DWI-ASPECTS and DWI–perfusion-weighted imaging mismatch) because lack of whole pre-treatment DWI data. The blood flow reperfusion and the status of vessel reflows were not completely evaluated because of some patients did not perform CTP examination after MT. A multicenter prospective study addressing more imaging factors is warranted to confirm the results we obtained.

Conclusion

Herein, we explored both clinical factors and imaging features in patients with ACLVO-related AIS undergoing MT. In doing so, initial ASPECTS, baseline NIHSS score, HMCAS, early imaging signs of infarct, age, and HbA1c concentration emerged as significant independent predictors of clinical outcomes.

Declarations

Ethics approval and consent to participate

The research was conducted ethically in accordance with the World Medical Association Declaration of Helsinki and relevant guidelines. The Institutional Review Board of the General Hospital of the Northern Theater Command approved the study protocol and provided the reference number (Approval Number Y (2020) 012) and waived the requirement of the informed consent for the study.

Consent for publication

Not Applicable.

Availability of data and materials

The author takes full responsibility for the data, the analyses and interpretation, and the conduct of the research. The research data supporting the conclusions of this article will be made available by the authors, without undue reservation. The datasets generated and/or analyzed during the current study are not publicly available but are available from the corresponding author on reasonable request. 

Competing interests

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

Funding

This work was supported by Project of Natural Science Foundation of Shenyang (grant no. 20-205-4-044), Project of Natural Science Foundation of Liaoning Province (grant no. 201602768) and Key Research and the Development Program of Liaoning Province, China (grant no. 2020JH2/10300119).

Authors' contributions

JL and YD: study design. XL and JD: data acquisition. ZX and LZ: image analysis. JL and ZX: primary manuscript writing. JL, YD and BY: critical revision and final approval of the manuscript.

Acknowledgements

We thank Lin Shi for help in collecting clinical data.

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