Impact of Sex on Thrombectomy Outcomes in Ischemic Stroke: A Propensity Score‐Matched Study, Systematic Review, and Meta‐Analysis
Stroke: Vascular and Interventional Neurology
Abstract
Background
Women are underrepresented in stroke thrombectomy trials, and the impact of sex differences in outcomes after stroke thrombectomy is unclear. We performed a multicenter propensity matching study to define sex‐related differences in outcome after endovascular thrombectomy and integrated results in a meta‐analysis.
Methods
We included patients with anterior circulation large vessel occlusion consecutively treated with thrombectomy at 2 Comprehensive Stroke Centres (2016–2023). Selection criteria reflected international guidelines. Through systematic review we selected all studies reporting endovascular thrombectomy outcomes in anterior circulation large vessel occlusion stroke, applying propensity score matching. MEDLINE, EMBASE, and Cochrane CENTRAL were searched up to August 15, 2023 according to predefined protocol (OSF.io/je3da). Data were extracted by 2 independent raters, pooled estimates calculated according to random‐effect modeling meta‐analysis and reported as odds ratio (OR) and standard 95% CI. Outcomes were good functional outcome, defined as modified Rankin Scale score 0–2 at 90 days after stroke, and symptomatic intracranial hemorrhage, adjudicated according to European Cooperative Acute Stroke Study II criteria.
Results
After matching, 698 patients (349 women versus 349 men) had similar cardiovascular risk factors, baseline features, and treatment approach. No significant differences were found for good functional outcome (OR = 0.89, 95% CI = 0.66–1.2) and symptomatic intracranial hemorrhage (OR = 1.00, 95% CI = 0.44–2.26) in the cohort study by sex. Systematic review identified 3 studies (n = 3706), all of high quality. No differences emerged in rates of good functional outcome (OR = 1.00, 95% CI = 0.79–1.21) or symptomatic intracranial hemorrhage (OR = 0.85, 95% CI = 0.60–1.19) depending on sex.
Conclusion
Women receiving endovascular thrombectomy for anterior circulation large vessel occlusion related stroke have similar rates of good functional outcome and symptomatic intracranial hemorrhage compared to men.
Graphical Abstract
Nonstandard Abbreviations and Acronyms
- EVT
- endovascular thrombectomy
- LVO
- large vessel occlusion
- mRS
- modified Rankin scale
- sICH
- symptomatic intracranial hemorrhage
Clinical Perspective
What Is Known?
•
Women are underrepresented in thrombectomy trials, and female sex has been associated with lower treatment benefit.
What Is New?
•
In our multicenter study and meta‐analysis, after propensity score matching for demographic data, cardiovascular risk factors, and stroke severity data, women had identical benefit from mechanical thrombectomy compared to men.
What Are the Clinical Implications?
•
Stroke networks and thrombectomy services should be structured to treat all eligible patients, independently from sex.
Endovascular thrombectomy (EVT) currently represents usual care for acute ischemic stroke due to large vessel occlusion (LVO).1 The impact of sex differences in outcomes after stroke thrombectomy is still unclear. Indeed, women were often underrepresented in EVT trials,2, 3 and it is still largely unknown whether the outcomes after EVT differ between women and men. Previous studies reported conflicting results regarding sex‐related differences in the clinical outcome after EVT, with consistent heterogeneity also found in previous meta‐analysis.4 In particular, although age and male sex emerged as determinants of good functional outcome through metaregression analysis, limitations derived from differences in risk factors across groups potentially affected the final estimates.4 What is more, age, prestroke functional status, and cardiovascular disease have all been suggested to influence the effect of sex on EVT outcomes,5 therefore limiting the value of the available evidence from observational studies and registries. To this extent, although regression models depend on sample size and adjustment for limited covariates, propensity‐score matching is an approach for matching relevant baseline factors between groups, limiting potential interactions across covariates.6
We performed a propensity‐score matched study to define the impact of sex on EVT outcomes across 2 Comprehensive Stroke Centers. We also systematically reviewed published studies reporting treatment effects stratified by sex after propensity score matching and pooled our data in a meta‐analysis.
Methods
Data are available from the corresponding author on request.
Cohort
We included patients with anterior circulation LVO consecutively admitted and treated with EVT at 2 Comprehensive Stroke Centers (Bufalini Hospital Stroke Hub, Cesena, Italy; Charing Cross Hospital, Imperial College Healthcare Trust, London, UK) serving a population of 1.2 million and 6.4 million people, respectively, with local stroke registries available.7, 8 Briefly, both registries included demographic, imaging, clinical, and processing data, prospectively collected since foundation (2021 and 2016, respectively). Each registry was approved by the local committee (CSN221010, HRA275260). The study was conducted in accordance with the Declaration of Helsinki 1964 recommendations. For the purpose of this study, all patients undergoing EVT for anterior circulation LVO (internal carotid artery, M1, proximal M2) were included, therefore excluding those being treated with thrombolysis only or not undergoing EVT. Selection criteria in both centers reflected international and national guidelines and included EVT in patients with modified Rankin scale (mRS) scores ranging from 0 to 2 beforetheir stroke, independent from their age, sex, or ethnic group.9 Baseline characteristics, admission and discharge National Institutes of Health Stroke Scale scores, location of occlusion, Alberta Stroke Program Early CT [Computed Tomography] score, reperfusion treatment details, and timing were routinely collected.
The primary outcome was good functional outcome, defined as mRS score 0–2 at 90 days after the stroke.10 Secondary outcomes were symptomatic intracranial hemorrhage (sICH), adjudicated according to European Cooperative Acute Stroke Study II criteria (for both registries and for all studies included in meta‐analysis). Additional outcomes were the combination of sICH or parenchymal hematoma, successful reperfusion (thrombolysis in cerebral infarction score 2b‐3), excellent functional outcome (mRS score 0–1), and 90‐day mortality (mRS score = 6).
Systematic Review
Search Strategy
A systematic review of the literature was registered with OSF (OSF.io/je3da), and followed MOOSE (Meta‐Analysis of Observational Studies in Epidemiology)11 and PRISMA (Preferred Reporting Items for Systematic Reviews and Meta‐Analyses)12 guidelines. We considered observational studies (either prospective or retrospective) reporting sex association with EVT outcomes in anterior circulation stroke and that applied propensity score matching to limit differences in distribution of cardiovascular risk factors, stroke severity, and treatment across sex groups (Supplementary material—Figure S1). Propensity score matching‐based studies were selected, as differences in the distribution of risk factors and procedural details emerged in both registries and trials. MEDLINE, EMBASE, and Cochrane CENTRAL were searched from inception up to August 15, 2023 independently by 2 authors (M.R., L.D.A.). The search strategy included terms for stroke, LVO, anterior circulation stroke, EVT, sex, and propensity score matching. For all potentially eligible studies, reference lists were cross‐checked to identify additional records. Search restrictions were (1) inclusion of studies involving only human participants, and (2) exclusion of studies in languages other than English, German, or Italian. No restrictions were set for sample size and age. Randomized controlled trials were excluded due to the heterogeneity in inclusion of sex in randomization procedures and the balance of baseline factors across sex groups.
Data Abstraction, Quality Control, and Outcomes
Titles, abstracts, and full text were rated by 2 authors (M.R., L.D.A.), with disagreements resolved by consensus. Data extraction was performed independently by 2 authors (M.R., L.D.A.), with inconsistencies resolved by consensus. Eligible studies were assessed for bias using the Newcastle–Ottawa scale, as previously reported,13 by 2 authors (M.R., L.D.A.), with final rating reached by consensus. Data extraction was performed on structured forms for string and numerical variables.
Statistical Analysis
Categorical variables are presented as count and percentage, continuous variables as mean and SD or median and interquartile range according to normal distribution. A propensity‐score matching algorithm was implemented to mitigate potential differences in risk factor distribution across sex groups. Propensity score of the treatment variable (women versus men) was calculated for each patient and a 1:1 nearest neighbor matching no‐replacing algorithm was used to match women to men within 0.1×SD of the logit of the propensity score according to their status. To determine whether the propensity score approach achieved balance in potential confounders, we compared baseline characteristics between the 2 groups before and after matching, reporting standardized mean difference (SMD) and accepting SMD<0.1 for the matched cohort. All available demographic, neuroradiological, treatment, and time metrics data were included in matching (age, hypertension, diabetes, dyslipidemia, atrial fibrillation, coronary artery disease, heart failure, previous stroke, prestroke mRS score, use of intravenous thrombolysis, systolic and diastolic blood pressure, National Institutes of Health Stroke Scale score, onset to groin, Alberta Stroke Program Early CT score, and study center). Statistical comparisons were performed between sex groups with χ2 test, Fisher exact test, Student's t‐test, and Mann–Whitney U test as indicated for dichotomous or continuous variables.
Binary logistic regression was implemented to weight the predictive value of sex on primary outcome, importing variables reaching P value <0.1 on univariate analysis together with sex a priori. After systematic review and data extraction, pooled prevalence of primary outcome in each group was calculated according to meta‐analysis with random effect modeling, and reported as odds ratio (ORs) and standard CI. When missing data limited the reconstruction of OR, original estimates were extracted from each study and pooled according to meta‐analysis of OR. Statistical analysis was carried out with R v 3.3.4 (r‐project).
Results
During the study period, 962 patients with acute ischemic stroke and LVO of the anterior circulation underwent EVT in our 2 centers. After propensity score matching, 698 patients were matched according to baseline characteristics (349 women versus 349 men; Table 1). Reperfusion strategies, systolic and diastolic blood pressure levels, neuroimaging characteristics, and stroke severity were similar across sex groups (Table 1).
| Before matching | After matching | |||||
|---|---|---|---|---|---|---|
| Women n=474 | Men n=488 | SMD | Women n=349 | Men n=349 | SMD | |
| Age, y | 75 ± 12.6 | 71 ± 12.7 | 0.34 | 73 ± 11.8 | 73 ± 13 | 0.01 |
| Hypertension | 313 (66%) | 258 (52.9%) | 0.26 | 205 (58.7%) | 201 (57.6%) | 0.02 |
| Diabetes | 77 (16.2%) | 97 (19.9%) | 0.11 | 61 (17.5%) | 59 (16.9%) | 0.02 |
| Dyslipidemia | 167 (35.2%) | 181 (37.1%) | 0.01 | 121 (34.7%) | 120 (34.4%) | 0.01 |
| Atrial fibrillation | 156 (32.9%) | 106 (21.7%) | 0.25 | 89 (25.5%) | 99 (28.4%) | 0.06 |
| Coronary artery disease | 37 (7.8%) | 72 (14.8%) | 0.29 | 39 (11.2%) | 34 (9.7%) | 0.05 |
| Heart failure | 46 (9.7%) | 54 (11.1%) | 0.11 | 43 (12.3%) | 35 (10%) | 0.05 |
| Previous stroke | 27 (5.7%) | 33 (6.8%) | 0.09 | 22 (6.3%) | 20 (5.7%) | 0.02 |
| Modified Rankin Scale score 0–2 at baseline | 467 (98.9%) | 485 (99.8%) | 0.08 | 348 (99.7%) | 349 (100%) | 0.02 |
| Thrombolysis | 308 (65%) | 328 (67.2%) | 0.05 | 225 (64.5%) | 228 (65.3%) | 0.01 |
| Systolic blood pressure (mm Hg) | 153 ± 28.4 | 150 ± 27.5 | 0.02 | 151 ± 29.7 | 151 ± 27.2 | 0.01 |
| Diastolic blood pressure (mm Hg) | 81 ± 15.1 | 83 ± 15.2 | 0.02 | 84 ± 15.1 | 80 ± 14.5 | 0.07 |
| National Institutes of Health Stroke Scale score | 17 (9–26) | 19 (10–27) | 0.03 | 17 (9–26) | 17 (9–26) | 0.09 |
| Onset to groin (minutes) | 287 ± 111.6 | 276 ± 103.9 | 0.09 | 277 ± 102.6 | 289 ± 119.1 | 0.09 |
| Alberta Stroke Program Early CT score | 8 (6–10) | 8 (6–10) | 0.06 | 8 (6–10) | 8 (6–10) | 0.02 |
| Occlusion site internal carotid artery | 95 (20%) | 152 (31.1%) | 0.18 | 91 (26.1%) | 79 (22.6%) | 0.01 |
| M1 | 318 (67.1%) | 279 (57.2%) | 208 (59.6%) | 233 (66.8%) | ||
| M1‐M2 | 61 (12.9%) | 57 (11.7%) | 50 (14.3%) | 37 (10.6%) | ||
John Wiley & Sons, Ltd.
SMD, standardized mean difference.
Good functional outcome at 3 months (mRS score 0–2) was similar between the 2 groups (OR for women versus men = 0.89, 95% CI = 0.66–1.2, Table 2). The two groups also did not differ in secondary (sICH) and additional study outcomes (Table 2).
| Women n=349 | Men n=349 | OR (95% CI) | P value | |
|---|---|---|---|---|
| mRS 0–2 | 152 (43.6%) | 162 (46.4%) | 0.89 (0.66–1.2) | 0.45 |
| mRS 0–1 | 117 (33.5%) | 122 (35%) | 0.94 (0.69–1.28) | 0.69 |
| Death | 67 (19.2%) | 82 (23.5%) | 0.77 (0.54–1.11) | 0.17 |
| Successful recanalization (thrombolysis in cerebral infarction 2b‐3) | 270 (77.4%) | 278 (79.7%) | 0.87 (0.61–1.25) | 0.46 |
| sICH | 12 (3.4%) | 12 (3.4%) | 1 (0.44–2.26) | 1 |
| sICH or parenchymal hematoma | 27 (7.7%) | 27 (7.8%) | 1 (0.57–1.74) | 0.99 |
John Wiley & Sons, Ltd.
mRS indicates modified Rankin scale; OR, odds ratio; and sICH, symptomatic intracranial hemorrhage.
Logistic regression analysis for the primary outcome showed that age, National Institutes of Health Stroke Scale score, and Alberta Stroke Program Early CT score were independent predictors of good functional outcome, whereas sex was not associated with good functional outcome (OR for women versus men = 0.97, 95% CI = 0.57–1.66; Supplementary material—Table S1).
Systematic review identified 3 studies (n = 3706) reporting outcomes of EVT in anterior circulation LVO stroke that used propensity matching between sex groups (Supplementary material—Figure S1). All studies had low risk of bias, particularly regarding comparability as their matching included reperfusion strategies and baseline factors (Supplementary material—Table S2). All studies represented secondary analyses of large registries, including the ANGEL‐ACT (Endovascular Treatment Key Technique and Emergency Work Flow Improvement of Acute Ischemic Stroke),14, 15 SELECT (Optimizing Patient's Selection for Endovascular Treatment in Acute Ischemic Stroke),16, 17 and IRETAS (Italian Registry of Endovascular Thrombectomy in Acute Stroke)18, 19 studies.
There was no difference in good functional outcome (OR 1.00, 95% CI 0.79–1.21), or sICH rates between sex groups (OR 0.85, 95% CI 0.60–1.19; Figure).
Discussion
The results of our observational study coupled with the findings of the current meta‐analysis including propensity score matched studies investigating the impact of sex on EVT outcome show that women and men had similar rates of good functional outcome and sICH. Our findings are at odds with previous literature reporting a lower treatment effect in women. In a MR CLEAN ((Multicenter Randomized Clinical Trial of Endovascular Treatment of Acute Ischemic Stroke in the Netherlands) post hoc analysis, women had lower rates of good functional outcome after EVT compared to men, although the ordinal assumption of benefit was not met among women, and a potential effect due to casualty was suggested for final estimates.20 In a large study based on the “Get With The Guidelines–Stroke” project, enrolling more than 40 000 participants, women were found to receive EVT less frequently and to have a reduced rate of good functional recovery compared to men.21 However, baseline mRS score was not available, and no matching was performed across sex groups, leaving space for marginal imbalances to influence outcomes. Similar issues limit the interpretation of evidence in favor of a similar treatment effect across sexes. In the pooled analysis of SWIFT (Solitaire With the Intention for Thrombectomy), STAR (Solitaire Flow Restoration Thrombectomy for Acute Revascularization), and SWIFT PRIME (Solitaire With the Intention for Thrombectomy as Primary Endovascular Treatment) cohorts,22 women had similar benefit from EVT compared to men but consistently older age and higher rates of atrial fibrillation at baseline.22 Similar findings emerged in the HERMES (Highly Effective Reperfusion Evaluated in Multiple Endovascular Stroke Trials) collaboration,1 intrinsically limited by the entry criteria of randomized controlled clinical trials, and in the SOLSTICE consortium (Selection of Late‐Window Stroke for Thrombectomy by Imaging Collateral Extent), with limitations in interpretation derived from lack of baseline mRS score, antithrombotic use, and significant differences in age and LVO site.23 The results of our cohort study, together with those emerging from systematic review and meta‐analysis, do not support any relevant difference in the outcome of EVT in acute ischemic stroke depending on sex. Functional recovery and the risk of sICH were similar in women and men, with no critical trend identified. These findings emerge from studies that applied propensity score matching, therefore limiting the potential influence that measurable factors, including cardiovascular disease and treatment timing,5 could have had on the relationship between sex and treatment effect. Despite efforts in limiting sex bias, women are still underrepresented in stroke trials.2, 3 Moreover, in the real world, women also seem less likely to receive EVT, to be admitted to a stroke unit, and to be older at stroke onset,21, 24 all factors negatively affecting recovery. As approximately 40% of patients reach functional independence after EVT, guaranteeing the access to such an effective treatment for women and men is paramount.24 Importantly, there has been an increasing rate of inclusion of women in global registries and trials in more recent years.24, 25
Our study has limitations. First, all included studies were nonrandomized and used a priori cohort selection based on completeness of data. However, propensity‐matched analysis was implemented in all studies included in the meta‐analysis to reduce imbalance in baseline characteristics. Despite this, it is still an imperfect balance as would be expected in randomized controlled trials. We did not include randomized trials as their subgroup analyses may not build on balance between men and women groups.26 Second, the studies included were carried out in different continents, potentially exposing to selection bias. Nevertheless, the limited heterogeneity and the consistency in outcome estimates across studies support the robustness of our findings. Finally, despite the power of propensity score matching, it should be noticed that potential unmeasured confounders may still have a role in driving treatment equipoise across sex groups. However, as the studies included reflect real‐world practice, the general estimate of similar outcomes of EVT independently from sex seems to be directly applicable.
Conclusions
In this meta‐analysis of propensity‐matched studies, also including original data from 2 large registries, women and men with anterior circulation LVO stroke had similar odds of good functional outcome and likelihood of sICH. Actions should be taken, and policies implemented, to guarantee the access to EVT and stroke care for all people, independent of sex.
Sources of Funding
The current study received no funding. Dr Romoli is supported by young investigator awards from the Italian Stroke Association (ISA‐AII). Dr Katsanos is supported by a New Investigator Award from the Heart and Stroke Foundation Canada.
Disclosures
Thanh N. Nguyen serves on the Editorial Board of S:VIN. Editorial Board members are not involved in the handling or final disposition of submissions.
Acknowledgments
None.
Footnote
Registration Systematic review protocol available at OSF.io/je3da.
Supplemental Material
Supplemental Tables S1 and S2.Supplemental figure S1.Supporting Information.
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© 2024 The Authors. Stroke: Vascular and Interventional Neurology published by Wiley Periodicals LLC on behalf of American Heart Association; The Society for Vascular and Interventional Neurology. This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
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Received: 7 October 2023
Accepted: 7 December 2023
Published online: 26 February 2024
Published in print: May 2024
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- Sex‐Specific Effects of Endovascular Treatment in Large‐Vessel Occlusion Stroke, Stroke: Vascular and Interventional Neurology, 4, 4, (2024).https://doi.org/10.1161/SVIN.124.001398
- Exploring the Impact of Age and Pre-Stroke Modified Rankin Scale in Elderly Thrombectomy: A 15-Year Single-Center Experience, Cerebrovascular Diseases Extra, 14, 1, (125-133), (2024).https://doi.org/10.1159/000540992
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