Predictors of intracranial hemorrhage after mechanical thrombectomy using a stent-retriever for anterior circulation ischemic stroke: A retrospective study : Medicine

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Research Article: Observational Study

Predictors of intracranial hemorrhage after mechanical thrombectomy using a stent-retriever for anterior circulation ischemic stroke: A retrospective study

Lee, In-Hyoung MDa; Ha, Sung-Kon MD, PhDa; Lim, Dong-Jun MD, PhDa; Choi, Jong-Il MD, PhDa,*

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Medicine 102(2):p e32666, January 13, 2023. | DOI: 10.1097/MD.0000000000032666
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1. Introduction

Currently, mechanical thrombectomy (MT) is the gold standard reperfusion treatment for acute ischemic stroke (AIS) derived from large-vessel occlusion (LVO) of anterior circulation. This is based on its proven efficacy and safety in several randomized trials.[1–3] Moreover, the current treatment guidelines recommend MT using a stent-retriever (SR) as the first line of treatment for LVO of the anterior circulation.[4]

Despite advancements in thrombectomy techniques and devices resulting in a reperfusion rate of > 80% in patients with LVO following MT,[5,6] it remains problematic that intracranial hemorrhage (ICH) is a commonly encountered post-procedural complication occurring in approximately 40% of patients with LVO after MT.[7,8] In particular, symptomatic intracranial hemorrhage (SICH) is such a potentially life-threatening complication as to cause unfavorable outcomes and raises mortality, thus eventually decreasing the risk-benefit ratio of endovascular treatment.[8,9] Therefore, it is mandatory to identify potential predictors of the above-mentioned feared complications, which will be essential for maximizing the efficacy of MT through a stringent risk assessment and reasonable strategies for peri-procedural management.

According to previous studies, there are several clinical or procedural predictors of hemorrhagic complications following MT for LVO-induced AIS patients; these include the national institutes of health stroke scale (NIHSS) score on admission, serum glucose level, systolic blood pressure, Alberta stroke program early computed tomography (CT) score (ASPECTS) on admission, delayed MT, duration of the procedure, and multiple passes of SR.[8–14] Still, there is heterogeneity and paucity of consensus concerning various predictors of hemorrhagic complications in patients undergoing MT. Therefore, we conducted this retrospective study to identify independent predictors of hemorrhagic complications (ICH and specifically SICH) in anterior circulation LVO-induced AIS patients undergoing MT using the SR.

2. Methods

2.1. Study population and clinical data

The ethical committee of our institution gave its approval to the current study (IRB No. 2022AS0146). Given that it was designed retrospectively, the written informed consent was waived. We analyzed the clinical and procedural data of 162 patients with anterior circulation LVO-induced AIS who were treated by MT at our institution from March 2014 to December 2021 according to the national treatment guidelines that were current at the time of treatment.[4,15]

The following were the requirements for eligibility in the current study: AIS caused by intracranial LVO of anterior circulation confirmed on digital subtraction angiography; MT initiated within 6 hours of symptom onset; pre-stroke modified Rankin Scale (mRS) score < 2, admission NIHSS score ≥ 6, and ASPECTS on admission ≥ 6; and MT performed with at least 1 pass of the SR device.

Patients diagnosed with intracranial-extracranial tandem occlusion, treated with direct aspiration alone, and those without subsequent imaging data were excluded. Figure 1 demonstrates the flowchart for including the study population.

Figure 1.:
Flowchart of patient inclusion. LVO, large vessel occlusion; MT, mechanical thrombectomy; mRS, modified Rankin Scale; NIHSS, National Institutes of Health Stroke Scale; ASPECTS, Alberta Stroke Program Early CT Score; ICH, intracranial hemorrhage. ASPECTS = Alberta stroke program early CT score.

We collected the following clinical variables from the finally enrolled 135 patients: age, sex, relevant comorbidities, history of antiplatelet and/or anticoagulant agent use, baseline laboratory findings, initial blood pressure in the emergency department, initial stroke severity assessed with the NIHSS score on admission, ASPECTS based on pre-procedural brain CT scan,[16] and stroke subtypes based on the Trial of Org 10172 in Acute Stroke Treatment (TOAST) criteria.[17]

Procedural variables included the site of arterial occlusion, intravenous tissue plasminogen activator pretreatment, time from stroke onset to groin puncture (OTP), procedure time (PT) defined as the time from groin puncture to the first successful recanalization or abortion of the procedure without successful recanalization,[18] procedure details (use of direct aspiration technique, number of SR attempts per procedure), and rescue therapies (implantation of an intracranial stent, intra-arterial glycoprotein IIb/IIIa inhibitor infusion, and/or intra-arterial thrombolysis).

2.2. Endovascular treatment

Intravenous tissue plasminogen activator was given to eligible patients (within 4.5 hours of stroke onset) prior to the procedure in accordance with the national guidelines.[4,15] Then they were transferred to an angiographic suite for emergent thrombectomy. All endovascular procedures were conducted using a biplane neuro-angiography system (Allura Clarity FD20/15; Philips Healthcare, Best, The Netherlands) under conscious sedation by experienced neuro-interventionists.

All enrolled patients underwent MT using second-generation stent-like thrombectomy devices, such as Solitaire (Medtronic Neurovascular, Irvine, CA) or Trevo (Stryker Neurovascular, Fremont, CA), concurrently with 8F balloon-guiding catheter to modulate the carotid antegrade flow by temporary inflation, which reduces embolic burden in a new territory. Some patients underwent thrombectomy using both SR and large-bore aspiration catheter (SOFIA 6F; Micro Vention-Terumo, Tustin, CA). The aspiration catheter was used to perform the previously reported direct contact aspiration.[19] With the aspiration catheter placed in the region adjacent to the occlusion site, direct aspiration was carried out with a 50 mL syringe. If the initial direct aspiration was unsuccessful, the thrombectomy strategy was switched to using SR devices. If MT was unsuccessful to the last, adjunctive rescue therapy was administered. The attending neuro-interventionist made the decision on thrombectomy devices and adjunctive rescue therapies.

Angiographic result of MT was assessed based on the grade of recanalization according to the modified Thrombolysis in Cerebral Infarction (mTICI) scoring system, for which successful recanalization was defined as mTICI score of 2b or 3 on the final cerebral angiography, as previously described.[20]

2.3. Intracerebral hemorrhage assessment

Post-procedural follow-up conventional brain CT scan was taken 24 hours following MT or earlier in the occurrence of sudden neurological deterioration, which suggests hemorrhagic complications.[11,14] Subsequent CT scans were obtained at various time points 3 to 7 days after MT considering the patient’s clinical status. Post-procedural ICH was defined according to the European cooperative acute stroke study (ECASS) criteria,[21] and dichotomized into SICH and asymptomatic intracranial hemorrhage (AICH). SICH was determined by assessing the correlation between clinical worsening and radiologic findings (any ICH on CT scan associated with the neurological deterioration that increased NIHSS score by more than 4 points within 24 hours or caused death).[22] AICH was defined as any newly reported ICH without additional neurological deterioration. Representative images of AICH and SICH are shown in Figure 2. Two neuro-interventionists and 1 neuro-radiologist blinded to the clinical details independently assessed all radiologic data. The final judgments were made by consensus.

Figure 2.:
Representative images of (A) asymptomatic intracranial hemorrhage (ICH) and (B) symptomatic ICH on axial computed tomography (CT) scans. (A) CT scan demonstrating ICH of left putamen without additional neurological deterioration, classified hemorrhagic infarction type 2 according to ECASS criteria. (B) CT scan showing ICH of left basal ganglia with intraventricular hemorrhage and mass effect causing a midline shift to the right (ECASS criteria parenchymal hematoma type 2), leading to clinical deterioration. ECASS, European Cooperative Acute Stroke Study.

2.4. Statistical Analysis

The Student’s t test was used to evaluate continuous variables that were presented as either mean with standard deviation or median with interquartile range. Categorical variables, expressed as the numbers of patients with percentages, were analyzed using Pearson’s chi-squared test. According to the presence of ICH, patients were categorized into 2 groups, and univariate analyses were conducted to compare the 2 groups (ICH vs no ICH). In addition, patient characteristics in the SICH and AICH groups were compared. Consequently, multivariate logistic regression analysis was conducted for variables with a P value of < .10 in univariate analysis to identify predictors of ICH and SICH, respectively. Adjusted odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. The optimal cutoff value for predicting SICH was determined using receiver operating characteristic (ROC) analysis. The cutoff value was established using the highest sum of the Youden index measures of sensitivity and specificity. All statistical analyses were conducted using SPSS 23.0 software (IBM Corp., Armonk, NY), and statistics were determined significant at P < .05.

3. Results

In the current study, 135 eligible patients were enrolled (Fig. 1). Among the entire cohort, any form of ICH was detected in 52 (38.5%) patients, and 17 (12.6%) patients were classified as having SICH according to the ECASS criteria. Table 1 demonstrates all patient’s demographic, clinical, and procedural variables.

Table 1 - Demographic, clinical and procedural variables of all patients.
All patients (n = 135)
Male 66 (48.9)
Age (yr) 69.6 ± 12.0
Hypertension 75 (55.6)
Diabetes mellitus 32 (23.7)
Atrial fibrillation 55 (40.7)
Dyslipidemia 42 (31.1)
Coronary heart disease 32 (23.7)
Previous stroke 20 (14.8)
Antiplatelet medication 45 (33.3)
Anticoagulant medication 26 (19.3)
Initial SBP (mm Hg) 151.9 ± 22.1
Initial DBP (mm Hg) 89.5 ± 15.2
Platelet count (109/L) 244.0 ± 86.9
INR 1.12 ± 0.20
Serum glucose (mg/dL) 136.0 ± 32.9
Admission NIHSS score 17 (14–20)
Baseline ASPECTS 8 (7-9)
Cause of stroke
 Large-artery atherosclerosis 36 (26.7)
 Cardioembolic 88 (65.2)
 Other or unknown 11 (8.1)
Occlusion site
 Intracranial ICA 40 (29.6)
 MCA - M1 78 (57.8)
 MCA - M2 17 (12.6)
Pretreatment of IV tPA 90 (66.7)
Onset to groin puncture (min) 275 (235–300)
Procedure time (min) 65 (45–87.5)
Direct aspiration 38 (28.1)
Number of stent-retriever passes 2.59 ± 1.16
 1 22 (16.3)
 2 51 (37.8)
 3 33 (24.4)
 4 21 (15.6)
 >5 8 (5.9)
Rescue therapies
 Intracranial stenting 32 (23.7)
 IA glycoprotein IIb/IIIa inhibitor 8 (5.9)
 IA thrombolysis 14 (10.4)
Successful recanalization 107 (79.3)
Data are presented as mean ± standard deviations or numbers (%), or median (interquartile range).
ASPECTS = alberta stroke program early CT score, DBP = diastolic blood pressure, ICH = intracranial hemorrhage, IA = intra-arterial, ICA = internal carotid artery, INR = international normalized ratio, SBP = systolic blood pressure, MCA = middle cerebral artery, NIHSS = national institutes of health stroke scale, IV tPA = intravenous tissue plasminogen activator.

3.1. Predictors of ICH

In the univariate analysis, serum glucose, admission NIHSS score, baseline ASPECTS, PT, and the number of SR passes correlated with ICH occurrence (P < .1). Serum glucose level (OR 1.016, 95% CI 1.004–1.029, P = .011) and number of SR passes (OR 2.607, 95% CI 1.742–3.902, P < .001) were found to be independent predictive variables of ICH in multivariate logistic regression (Table 2).

Table 2 - Results of univariate analysis and multivariate logistic regression for predictors of ICH.
ICH (+) (n = 52) ICH (-) (n = 83) P value (univariate) Odds ratio (95% CI) P value (multivariate)
Male 24 (46.2) 42 (50.6) .618
Age (yr) 71.0 ± 10.4 68.7 ± 12.9 .282
Hypertension 29 (55.8) 46 (55.4) .969
Diabetes mellitus 16 (30.8) 16 (19.3) .144
Atrial fibrillation 25 (48.1) 30 (36.1) .177
Dyslipidemia 19 (36.5) 23 (27.7) .294
Coronary heart disease 13 (25.0) 19 (22.9) .781
Previous stroke 10 (19.2) 10 (12.0) .278
Antiplatelet medication 14 (26.9) 31 (37.3) .206
Anticoagulant medication 11 (21.2) 15 (18.1) .661
Initial SBP (mm Hg) 154.8 ± 21.1 150.2 ± 22.6 .243
Initial DBP (mm Hg) 90.1 ± 14.9 89.1 ± 15.5 .703
Platelet count (109/L) 239.1 ± 90.7 247.1 ± 84.8 .601
INR 1.10 ± 0.30 1.05 ± 0.22 .316
Serum glucose (mg/dL) 146.3 ± 26.1 129.6 ± 35.1 .002 1.016 (1.004–1.029) .011*
Admission NIHSS score 18 (15–21) 16 (13–19) .071 1.003 (0.912–1.103) .949
Baseline ASPECTS 7.75 ± 1.25 8.37 ± 1.13 .003 0.808 (0.548–1.192) .283
Cause of stroke
 Large-artery atherosclerosis 14 (26.9) 22 (26.5) .958
 Cardioembolic 33 (63.5) 55 (66.3) .742
 Other or unknown 5 (9.6) 6 (7.2) .625
Occlusion site
 Intracranial ICA 15 (28.8) 25 (30.1) .623
 MCA - M1 31 (59.6) 47 (56.6) .735
 MCA - M2 6 (11.5) 11 (13.3) .772
Pretreatment of IV tPA 35 (67.3) 55 (66.3) .901
Onset to groin puncture (min) 275 (235–291) 280 (225–300) .885
Procedure time (min) 80 (70–100) 55 (40–75) <.001 1.015 (0.993–1.038) .179
Direct aspiration 15 (28.8) 23 (27.7) .888
Number of stent-retriever passes 3.25 ± 1.19 2.17 ± 0.92 <.001 2.607 (1.742–3.902) <.001*
Rescue therapies
 Intracranial stenting 11 (21.2) 21 (25.3) .585
 IA glycoprotein IIb/IIIa inhibitor 3 (5.8) 5 (6.0) .952
 IA thrombolysis 5 (9.6) 9 (10.8) .821
Successful recanalization 39 (75.0) 68 (81.9) .338
Data are presented as mean ± standard deviations or numbers (%), or median (interquartile range).
ASPECTS = alberta stroke program early CT score, DBP = diastolic blood pressure, IA = intra-arterial, ICA = internal carotid artery, ICH = intracranial hemorrhage, INR = international normalized ratio, IV tPA = intravenous tissue plasminogen activator, MCA = middle cerebral artery, NIHSS = national institutes of health stroke scale, SBP = systolic blood pressure.
*Statistical significance.

3.2. Predictors of SICH

Univariate and multivariate analyses were conducted to compare SICH and AICH groups (Table 3). The SICH group showed lower ASPECTS, prolonged OTP, longer PT, and a higher number of passes of SR than the AICH group. In the multivariate analysis, baseline ASPECTS (OR 0.485, 95% CI 0.242–0.973, P = .042), OTP (OR 1.033, 95% CI 1.006–1.061, P = .016), and number of SR passes (OR 2.342, 95% CI 1.049–5.229, P = .038) were found to be independent predictors of SICH.

Table 3 - Results of univariate analysis and multivariate logistic regression for predictors of SICH.
SICH (n = 17) AICH (n = 35) P value (univariate) Odds ratio (95% CI) P value (multivariate)
Male 7 (41.2) 17 (48.6) .624
Age (yr) 71.7 ± 8.0 70.6 ± 11.5 .731
Hypertension 9 (52.9) 20 (57.1) .780
Diabetes mellitus 5 (29.4) 11 (31.4) .885
Atrial fibrillation 6 (35.3) 19 (54.3) .206
Dyslipidemia 6 (35.3) 13 (37.1) .899
Coronary heart disease 3 (17.6) 10 (28.6) .403
Previous stroke 3 (17.6) 7 (20.0) .844
Antiplatelet medication 5 (29.4) 9 (25.7) .783
Anticoagulant medication 5 (29.4) 6 (17.1) .319
Initial SBP (mm Hg) 155.8 ± 22.2 154.3 ± 20.8 .812
Initial DBP (mm Hg) 89.5 ± 14.3 90.4 ± 15.3 .845
Platelet count (109/L) 250.2 ± 96.1 233.7 ± 88.9 .542
INR 1.12 ± 0.33 1.09 ± 0.28 .721
Serum glucose (mg/dL) 154.1 ± 19.7 142.5 ± 28.3 .138
Admission NIHSS score 18 (17–21) 18 (15–20.5) .450
Baseline ASPECTS 7.00 ± 1.06 8.11 ± 1.18 .002 0.485 (0.242–0.973) .042*
Cause of stroke .638
 Large-artery atherosclerosis 5 (29.4) 9 (25.7) .783
 Cardioembolic 9 (52.9) 24 (68.6) .281
 Other or unknown 3 (17.6) 2 (5.7) .260
Occlusion site .425
 Intracranial ICA 4 (23.5) 11 (31.4) .403
 MCA - M1 11 (64.7) 20 (57.1) .610
 MCA - M2 2 (11.8) 4 (11.4) .972
Pretreatment of IV tPA 12 (70.6) 23 (65.7) .732
Onset to groin puncture 290 (285–300) 260 (220–285) <.001 1.033 (1.006–1.061) .016*
Procedure time 100 (75–105) 75 (57.5–92.5) .034 1.022 (0.992–1.054) .156
Direct aspiration 6 (35.3) 9 (25.7) .484
Number of stent-retriever passes 4 ± 1.23 2.89 ± 0.99 .001 2.342 (1.049–5.229) .038*
Rescue therapies .885
 Intracranial stenting 4 (23.5) 7 (20.0) .775
 IA glycoprotein IIb/IIIa inhibitor 1 (5.9) 2 (5.7) .981
 IA thrombolysis 1 (5.9) 4 (11.4) .534
Successful recanalization 12 (70.6) 27 (77.1) .617
Data are presented as mean ± standard deviations or numbers (%), or median (interquartile range).
AICH = asymptomatic intracranial hemorrhage, ASPECTS = alberta stroke program early CT score, DBP = diastolic blood pressure, IA = intra-arterial, ICA = internal carotid artery, INR = international normalized ratio, IV tPA = intravenous tissue plasminogen activator, MCA = middle cerebral artery, NIHSS = national institutes of health stroke scale, SBP = systolic blood pressure, SICH = symptomatic intracranial hemorrhage.
*Statistical significance.

The ROC analysis revealed that the optimal cutoff values for SICH prediction were baseline ASPECTS ≤ 7, OTP > 280 minutes, and number of SR passes > 3. The results of subsequent multivariate analysis of the above 3 independent SICH predictors’ cutoff points are shown in Table 4.

Table 4 - Results of multivariate analysis for cutoff values of independent predictors of SICH.
Odds ratio (95% CI) P value
Baseline ASPECTS ≤ 7 5.380 (1.236–23.416) 0.025*
Onset to groin puncture > 280 min 9.380 (2.046–42.999) 0.004*
Number of stent-retriever passes > 3 5.697 (1.104–29.398) 0.038*
ASPECTS = alberta stroke program early CT score, SICH = symptomatic intracranial hemorrhage.
*Statistical significance.

4. Discussion

ICH following reperfusion treatment for AIS was not an uncommon post-procedural complication. We found that this occurred at a rate of 38.5% in our series. This is consistent with previously published studies showing that it was estimated at approximately 40%.[7,8,13] Moreover, SICH is a severe complication of MT, occurring at a rate of 12.6% (17/135) in our study. This is also in agreement with previously published literatures.[8,13] This retrospective study identified several potential predictors of ICH and SICH following MT using the SR in anterior circulation LVO-induced AIS patients. Hyperglycemia and multiple passes of SR were independent predictors of any form of ICH. Moreover, patients with lower ASPECTS on admission, prolonged OTP, and multiple passes of SR were more vulnerable to SICH.

Our results showed that the higher serum glucose level on admission was a predictor of SICH following MT in patients with LVO-induced AIS. This concurs with previously published studies.[9,10,12] Hyperglycemia may cause blood-brain barrier disruption, cytotoxic edema, and exacerbation of the thrombo-inflammatory response. Therefore, hyperglycemic patients in AIS undergoing MT may be susceptible to hemorrhagic complications.[23–25] However, a recent study showed that glycosylated hemoglobin (HbA1c) is a more reliable predictive factor of hemorrhagic complications than serum glucose value on admission.[26] This suggests that long-term vascular injury derived from chronically uncontrolled blood glucose was more precisely reflected in HbA1c rather than hyperglycemia on admission, which possibly arose from acute stress response after AIS.[27] However, it is limited for global use because HbA1c is not measured as a routine laboratory parameter in all patients with stroke. This warrants further large-scale prospective trials because it is unclear which parameters are more accurate predictors of the possibility of hemorrhagic complications in AIS patients.

Contrary to the results of the current study, according to a previous retrospective study conducted on 329 patients, the number of SR passes was found to be insignificant for hemorrhagic transformation.[28] However, this should be regarded with caution; the number of passes per procedure in the above study was almost 3 or less (96.7%), and more than 3 passes were too sparse (3.3%). The number of SR passes and an increased risk of SICH are positively correlated, according to several previous studies.[10,13,14] In more detail, a recent multi-center study revealed that more than 3 attempts of SR was an independent predictor of SICH.[8] Several mechanisms support the correlation between hemorrhagic transformation and multiple attempts of SR. First, multiple passes of SR may cause an endothelial injury to the arterial wall after each trial through an additional mechanical stretch during thrombus retrieval, which could lead to hemorrhagic transformation.[29] In particular, the use of SR may injure the endothelium by generating a sustained radial force to the vessel wall to trap the thrombus clot.[30] Second, multiple attempts to remove the clot cause blood-brain barrier disruption, and its severity is associated with aggravation of hemorrhagic transformation.[31]

As we know the importance of time on clinical outcomes in AIS, recent studies on the association between various time metrics and hemorrhagic complications have been conducted. The association of PT with post-procedural hemorrhagic complications has been described previously, with prolonged PT increasing the risk of SICH.[11,18] However, we failed to reproduce these results in the multivariate analysis, whereas OTP remained a significant predictor for SICH. This may be because, in addition to the SR passes, multifactorial variables were involved in the composition of overall PT, such as proficiency in attending neuro-interventionists, complicated vessel anatomy, and procedure details (direct aspiration, and rescue therapies). In summary, multiple thrombectomy maneuvers may increase PT, but the number of passes does not necessarily equal the PT; therefore, we speculate that it cannot be used as a surrogate marker for SICH.

Several studies have postulated the impact of OTP as a predictor of SICH, which is consistent with our results. According to a retrospective study conducted on 632 patients, OTP of more than 270 min was a significant predictor for SICH.[8] Similar results have been demonstrated in a previous study: prolonged OTP significantly increases the risk of parenchymal hematoma.[32] These results may be attributed to the enhanced susceptibility of ischemic brain tissue to reperfusion injury. Consequently, after arriving at the emergency department, a fast transfer to the angiography suite for eligible patients is the key to reducing hemorrhagic events after MT. A more recent multi-center analysis discovered that a longer interval between onset and admission was significantly correlated with hemorrhagic complications classified as parenchymal hematoma type 2 according to the ECASS criteria. Moreover, it was the time metric with the most significant impact.[33] Therefore, further studies based on subdivided time metrics are warranted to clarify novel time-related variables to help predict hemorrhagic complications.

This study did not identify a higher baseline NIHSS score as a predictor of hemorrhagic complications, unlike previous reports.[9,10] This might imply that in addition to reflecting the ischemic core, the NIHSS score also represents the reversible penumbra, in contrast to ASPECTS. In previous studies, lower ASPECTS had a significant correlation with a risk of SICH, in line with our results.[12,14,34] Notably, 2 validated predictive models for SICH (TAG score and The ASIAN Score) contained ASPECTS as a significant variable.[14,34] Patients with large-sized infarct core may be vulnerable to SICH, which indirectly suggests an enormous stroke burden and vulnerability to reperfusion injury after endovascular procedures. Our results indicate that MT should be performed in a timely manner to prevent the occurrence of SICH, which decreases the risk-benefit ratio of MT.

Our results cannot be generalized; several limitations of this study are as follows: First, we included a relatively small series of retrospectively enrolled patients with SICH. This may have confounded the results of multivariate analyses, underestimating the impact of other variables. Second, we failed to evaluate potentially relevant parameters such as biological markers, collateral status, and time-related variability in blood pressure during and after the procedure, which may contribute to the development of hemorrhagic complications. Nevertheless, our findings can be useful in predicting ICH and SICH in AIS patients undergoing MT in a real-world clinical setting.

5. Conclusions

This study identified several significant predictors of ICH and SICH in LVO-induced AIS patients treated with MT using the SR. Serum glucose level and the number of SR passes were predictors of any form of ICH. Specifically, patients with lower ASPECTS on admission (≤7), prolonged OTP (>280 minutes), and multiple passes of SR (>3) are more vulnerable to SICH. Our study suggests that timely MT is important in preventing SICH. In addition, when more than 3 passes of SR is necessary for recanalization, neuro-interventionists should be aware of the possibility of post-procedural hemorrhagic complications.

Author contributions

Conceptualization: In-Hyoung Lee, Sung-Kon Ha, Dong-Jun Lim, Jong-Il Choi.

Data curation: In-Hyoung Lee, Jong-Il Choi.

Formal analysis: In-Hyoung Lee.

Funding acquisition: In-Hyoung Lee, Jong-Il Choi.

Investigation: In-Hyoung Lee.

Methodology: In-Hyoung Lee, Dong-Jun Lim, Jong-Il Choi.

Project administration: Jong-Il Choi.

Resources: In-Hyoung Lee, Sung-Kon Ha, Jong-Il Choi.

Software: In-Hyoung Lee.

Supervision: Sung-Kon Ha, Dong-Jun Lim, Jong-Il Choi.

Validation: Sung-Kon Ha, Dong-Jun Lim, Jong-Il Choi.

Visualization: In-Hyoung Lee.

Writing – original draft: In-Hyoung Lee.

Writing – review & editing: Sung-Kon Ha, Jong-Il Choi.


asymptomatic intracranial hemorrhage
acute ischemic stroke
Alberta stroke program early CT score
CT =
computed tomography
European cooperative acute stroke study
intracranial hemorrhage
large vessel occlusion
MT =
mechanical thrombectomy
national institutes of health stroke scale
onset to groin puncture
PT =
procedure time
symptomatic intracranial hemorrhage
SR =


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acute ischemic stroke; intracranial hemorrhages; risk factors; stents; thrombectomy

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