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Acute ischemic stroke (AIS) is a major public health issue, and women have a disproportionate share of stroke-related disability and mortality, which is poorly understood. This study aimed to determine the effect of sex differences on AIS treated by thrombolysis using recombinant tissue plasminogen activator (rTPA). The study included 134 AIS patients eligible for rTPA. Risk factors, clinical presentation, thrombolysis response, complications, and outcomes were recorded. The outcomes were measured using the National Institute of Health Stroke Scale (NIHSS) and the modified Rankin Scale (mRS) 3 months after stroke. The incidence of intracranial haemorrhage was also determined.
Results
Among 134 AIS patients treated with rTPA (59% male, 41% female), females had higher rates of hypertension (67.3% versus 49.4%, p = 0.040) and atrial fibrillation (AF) (12.7% versus 2.5%, p = 0.020), while smoking was more prevalent in males (31.6% versus 0%, p < 0.0001). Cardioembolism was more frequent in females than in males (23.6% versus 6.3%, p = 0.004). Females also had shorter onset-to-door (110.7 ± 63 versus 131.1 ± 50.2 min, p = 0.035) and onset-to-needle times (151.6 ± 66.5 versus 173.7 ± 50.6 min, p = 0.046). Both sexes showed significant improvements in NIHSS (males: 11.58 ± 3.7 to 6.05 ± 5.6; females: 11.64 ± 4.7 to 6.9 ± 5.9; p < 0.0001) and mRS scores (males: 3.34 ± 1.05 to 2.03 ± 2; females: 3.53 ± 1 to 2.02 ± 2; p < 0.0001) over 3 months, with no significant differences between sexes. Predictors of poor outcome (mRS 3–6) differed: diabetes mellitus (DM) (OR 7.79, p = 0.002) and longer door-to-needle time (OR 1.04, p = 0.008) for males, and hemorrhage (OR 9.41, p = 0.048) for females. Hemorrhage predicted mortality in males (OR 27.08, p < 0.0001), while AF was associated with increased mortality in females (OR 8.06, p = 0.024).
Conclusions
This study revealed sex-specific differences in AIS risk factors, aetiology, and rTPA treatment timelines, although post-treatment improvements were comparable between sexes. Notably, outcome predictors and mortality factors differed by sex. These findings emphasize the need for sex-specific considerations in AIS management and risk assessment.
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AIS
Acute Ischemic Stroke
rTPA
Recombinant Tissue Plasminogen Activator
NIHSS
National Institute of Health Stroke Scale
mRS
Modified Rankin Scale
AF
Atrial fibrillation
OR
Odds ratio
TIA
Transient Ischemic Attack
RCT
Randomized clinical trial
WHO
World Health Organization
IRB
Institutional Review Board
BMI
Body Mass Index
ANOVA
Analysis of variance
DM
Diabetes mellitus
ICH
Intracerebral Hemorrhage
NINDS
National Institute of Neurological Disorders and Stroke
Introduction
Acute ischemic stroke (AIS) is a top priority for public health due to its high mortality and morbidity rates. Intravenous thrombolysis using recombinant tissue plasminogen activator (rTPA) is the primary treatment for AIS, and timely treatment is crucial for effective reperfusion [1, 2]. There is strong evidence that patients who receive IV rTPA within 4.5 h of symptom onset have a beneficial response [3].
There are many reasons why sex could influence stroke risk, clinical presentation, treatment response, and outcomes. Females differ from males in neuroprotective factors, endothelium plasminogen activator inhibitor levels, platelet counts, hormonal levels and vascular risk factors [4]. There are also differences in sociocultural roles and lifestyle factors [5]. All of these could influence the risk of stroke, response to rTPA and outcome [6].
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Despite several studies examining sex-based differences in stroke risk factors, clinical presentation, treatment modalities, and outcomes following rTPA administration in AIS have been conducted globally [7‐23]. However, only one study has been conducted in Egypt, specifically in the northern region [24] with lack of published data from Upper Egypt. This region exhibits several distinct characteristics compared to Northern Egypt, including significant stroke care disparities. These disparities encompass limited diagnostic capabilities and a shortage of specialists, resulting in markedly reduced thrombolysis rates [24]. This treatment gap provides a unique perspective for examining the additional impact of sex difference on the outcome of acute stroke in a region where healthcare disparities are prevalent.
This work aimed to determine the effect of sex disparities, on stroke risk factors, presentation, complications, and 3-month outcomes after administration of rTPA in AIS.
Methods
This study employed an interventional prospective cohort design. Patients presenting with acute stroke were recruited consecutively from the emergency rooms of the Neurology departments at Assiut University Hospitals and Aswan University Hospitals.
The study was approved by the Assiut University, Faculty of Medicine’s ethical committee and registered with the Institutional Review Board (IRB no: 04-2023-300441). The 1964 WHO Declaration of Helsinki and its revisions were followed throughout the study. Each patient and/or caregiver gave written informed consent before the study began.
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The Study participants: 134 out of 2121 patients with AIS eligible for rTPA were recruited and participated in the study during the period from March 1, 2018, to August 31, 2019. See Flowchart in Fig. 1.
Fig. 1
Flowchart shows the selection of eligible stroke patients for inclusion in the current study. It outlines the overall stroke population, with a subset meeting the eligibility criteria and being subsequently analyzed
The inclusion and exclusion criteria were the same as in the National Institute of Neurological Disorders and Stroke (NINDS) study [1].
The participants received an intravenous single alteplase dose of 0.9 mg/kg (not exceeding 90 mg), with 10% as a bolus and the remaining as a continuous infusion over 1 h [1]. The rTPA infusion and monitoring followed the instructions and protocol described in the NINDS study [1]. Participants were evaluated at multiple time points using the National Institutes of Health Stroke Scale (NIHSS) and the modified Rankin scale (mRS). NIHSS and mRS scales were measured at baseline (pre-treatment) and immediately post-treatment. The NIHSS was additionally assessed 1 week after treatment, while both scales were re-evaluated 3-month post-treatment, as indicated in another study [25].
National Institutes of Health Stroke Scale (NIHSS) [26]. NIHSS reduction of ≥ 4 points at 3-month evaluation compared to baseline assessment was considered a favourable outcome [27]. Patients were scored before giving rTPA, 24-h post-infusion, and 1 week and 3 months after infusion.
The modified Rankin scale (mRS) [28]: The primary outcome measure was the 90-day mRS, which was dichotomized as functional independence or good Outcome (mRS ≤ 2) and poor Outcome (mRS > 2) [29]. The score was applied before giving rTPA, 24-h post-infusion and 3 months after infusion.
Evidence of intracranial haemorrhage was classified into four grades by a reading panel who read the CT films blindly: (0) no haemorrhage; (1) hemorrhagic infarction without hematoma; (2) hematoma without midline structures shifting; and (3) hematoma with midline structures shifting [30].
Statistical analysis
IBM-SPSS 26.0 was utilized to analyze the data (IBMSPSS Inc., Chicago, IL, USA). The descriptive data were expressed as means, standard deviations, and percentages. The Chi-square test was utilized to compare the frequency distributions of the two groups (males versus females). The normal distribution of the variables was tested using the Shapiro–Wilk test. One-way repeated measures ANOVA was used to analyze the main effect of time in each group separately. Two-way repeated measure ANOVA (NIHSS and mRS at different time points) with main effects of time and group (male and female). The forward Stepwise technique, a multivariate logistic regression model, was developed to assess the association between independent factors, 3-month outcomes, and mortality following stroke in both sexes. The odds ratios were adjusted for variables that potentially influence treatment results, such as age > 50, smoking, BMI, previous history of stroke or TIA, hypertension, history of ischemic heart disease, atrial fibrillation (AF), stroke aetiology, the affected circulation and onset to needle time. A significant p value was considered to be < 0.05.
Results
Table 1 summarizes the sociodemographic data, risk factors, and clinical characteristics of AIS patients treated with rTPA in relation to sex distribution. Of 134 patients, 59.0% were male and 41.0% female. Females had a significantly higher mean BMI (27.63 ± 4.6 versus 25.86 ± 2.95, p = 0.014). Hypertension (67.3% versus 49.4%, p = 0.040) and AF (12.7% versus 2.5%, p = 0.020) were more frequent in females, while smoking was exclusively observed in males (31.6% versus 0%, p < 0.0001). Cardioembolism as stroke aetiology was more frequent in females (23.6% versus 6.3%, p = 0.004). Females had significantly shorter onset-to-door and onset-to-needle times. There was no significant sex effect on the type of occluded vessels. Regarding the complications, re-infarction was more common in females (14.5% versus 3.8%, p = 0.026).
Table 1
Demographic data and risk factors of AIS treated with rTPA in relation to sex distribution
Tables 2 and 3 show the NIHSS and mRS scores at different assessment points for AIS patients treated with rTPA, comparing outcomes between males and females. Both sexes demonstrated significant improvements in NIHSS and mRS scores over time (p < 0.0001 for both groups). The mean NIHSS scores decreased from 11.58 ± 3.7 to 6.05 ± 5.6 in males and from 11.64 ± 4.7 to 6.9 ± 5.9 in females at 3-month post-treatment. Similarly, mean mRS scores decreased from 3.34 ± 1.05 to 2.03 ± 2 in males and from 3.53 ± 1 to 2.02 ± 2 in females. Notably, there were no significant differences between males and females in NIHSS or mRS scores at any assessment point. In addition, see Fig. 2.
Table 2
NIHSS at each point of assessment of acute ischemic stroke patients treated with rTPA in relation to sex distribution
Pre-NIHSS score
Mean ± SD
Post-NIHSS score
Mean ± SD
One week later-NIHSS score
Mean ± SD
Three months later, the NIHSS score
Mean ± SD
Two Way ANOVA repeated measure analysis with the main effect of time for each group separately (F, dF, p value)
Two Way ANOVA repeated measure analysis (Time X groups) F, dF, p value
Males
11.58 ± 3.7
7.04 ± 6.8***
6.8 ± 7.3NS
6.05 ± 5.6*
59.9, 1.44, < 0.0001
0.15, 1.44, 0.78
Females
11.64 ± 4.7
7.16 ± 6.4***
6.49 ± 6.88*
6.9 ± 5.9*
61.4, 1.44, < 0.0001
Post-hoc t test between sex at each point of assessment (T and p value)
− 0.02, 0.98
− 0.9, 0.92
0.24, 0.80
0.15, 0.87
NIHSS: National Institutes of Health Stroke Scale; rTPA: recombinant Tissue Plasminogen Activator
*** = p < 0.0001 (p value between pre- and post-NIHSS), * = p < 0.01 (p value between 1 week later – Post 3-month NIHSS)
Table 3
mRS at each point of assessment of acute ischemic stroke patients treated with rTPA in relation to sex distribution
Pre-mRS score
Mean ± SD
Post-mRS score
Mean ± SD
Three months later, the mRS score
Mean ± SD
Two Way ANOVA repeated measure analysis with the main effect of time for each group separately (F, dF, p value)
Two Way ANOVA repeated measure analysis (Time X groups) F, dF, p value
Males
3.34 ± 1.05
2.43 ± 1.4***
2.03 ± 2***
39.7, 1.44, < 0.0001
0.46, 1.41, 0.56
Females
3.53 ± 1
2.65 ± 1.5***
2.02 ± 2***
35.9, 1.41, < 0.0001
Post-hoc t test between sex at each point of assessment (T and p value)
*** = p < 0.0001 (p value between pre- and post-mRS), *** = p < 0.0001 (p value between pre- and post-mRS), *** = p < 0.0001 (p value between post rTPA–Post 3-month mRS
Fig. 2
NHSS and mRS at each point of assessment of acute ischemic stroke patients treated with rTPA in relation to sex distribution follow-up. *** = p < 0.0001 (p value between pre- and post-NIHSS), * = p < 0.01 (p value between 1 week later—post 3-month NIHSS). *** = p < 0.0001 (p value between pre- and post-mRS), *** = p < 0.0001 (p value between post-rTPA—post 3-month mRS)
Table 4 illustrates the potential predictors of poor functional outcome (mRS 3–6) at 3 months and mortality (mRS 6) according to sex, using multivariable binary logistic regression analysis. For males, diabetes mellitus (DM) (adjusted OR 7.79, 95% CI 2.10–28.86, p = 0.002) and longer door-to-needle time (adjusted OR 1.04, 95% CI 1.01–1.07, p = 0.008) were associated with poor functional outcome. For females, hemorrhage was a significant independent predictor of poor functional outcome (adjusted OR 9.41, 95% CI 1.05–87.19, p = 0.048). Regarding mortality, hemorrhage was a strong independent predictor in males (adjusted OR 27.08, 95% CI 4.70–156.11, p < 0.0001), while AF was associated with increased mortality in females (adjusted OR 8.06, 95% CI 1.31–49.46, p = 0.024).
Table 4
Multivariable binary logistic regression analysis of the potential predictors of poor functional Outcome (mRS = 3–6) at 3 months and potential predictors of Mortality (mRS = 6) according to sex
Variable
Males (n = 79)
Females (n = 55)
Unadjusted OR (95% CI)
p value
Adjusted OR (95% CI)
p value
Unadjusted OR (95% CI)
p value
Adjusted OR (95% CI)
p value
3-month mRS score: 3–6
DM
5.31 (1.68–16.80)
0.005
7.79 (2.10–28.86)
0.002
–
–
–
–
Haemorrhage
3,424,392,916.41 (0.000)
0.990
4,810,593,591.6 (0.000)
0.999
9.41 (1.05–87.19)
0.048
9.41 (1.05–87.19)
0.048
Door to needle time (min)
–
–
1.04 (1.01–1.07)
0.008
–
–
–
–
Mortality (mRS: 6)
AF
16.25 (0.85–310.47)
0.064
16.25 (0.85–310.47)
0.064
8.06 (1.31–49.46)
0.024
8.06 (1.31–49.46)
0.024
Haemorrhage
27.08 (4.70–156.11)
< 0.0001
27.08 (4.70–156.11)
< 0.0001
–
–
–
–
Averaged results of all patients with pathogenic variants in the same BBS gene are highlighted in bold
AF atrial fibrillation, DM diabetes mellitus, mRS modified Rankin Scale, OR odds ratio, CI confidence interval
Reference categories are Age ≤ 50 years, No Hypertension, No Diabetes mellitus, No Smoking, No Hyperlipidaemia, No Previous history of stroke or TIA, No Previous history of IHD, No Atrial fibrillation, No Large artery atherosclerosis, No Cardioembolism, No lacunar infarction, No other causes of stroke, No Anterior circulation, No Haemorrhage
Discussion
Controversial results have been reported on the impact of sex differences on stroke risk factors, clinical presentation and functional outcomes of AIS receiving rTPA.
This is the first study from Upper Egypt to assess the influence of sex on stroke risk factors, presentation, and 3-month outcomes of rTPA-treated patients. The main findings were that a smaller proportion of females received rTPA than males. Females had a higher rate of hypertension and AF as risk factors for stroke, with cardioembolic stroke being more prevalent compared to males. In addition, the onset-to-door and onset-to-needle times were significantly faster than in males. Sex distribution did not affect the primary Outcome or death rate. However, re-infarction was a substantially more frequent complication in women than in men.
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Regarding the risk factors, in the present study, females had a significantly elevated BMI compared to males. This finding likely stems from biological and sociocultural forces [31], since other studies have found that BMI is more pronounced in females than males (Spain) [32] or that females have a significantly lower BMI than males (Vietnam) [29]. Wang and colleagues, in 2022, explored the relationship between BMI and the risk of stroke in a systematic review and reported a positive association between the risk of stroke and BMI and that the association was stronger in males with AIS [33].
In the current study, females had a significantly higher rate of AF than males, which agrees with previous studies that reported that females had a significantly higher risk for AF-related AIS [16, 29, 34‐37]. AF is associated with double the risk of stroke in females [38], who experienced more severe strokes [39], and increased all-cause mortality in females compared to males [40].
In this study, females had a significantly higher frequency of hypertension compared to males, which agrees with findings reported in previous studies [16, 36, 37, 41]. In addition, other studies from the US and international cohorts demonstrated a stronger association between hypertension and risk of AIS in females compared with males, adjusted for the use of antihypertensives [15, 42, 43]. This finding could be explained by the fact that females are vulnerable to an increased risk of hypertension compared to males stemming from the hypertensive disorders of pregnancy.
Smoking was significantly predominant in males, which is in line with the findings reported by previous studies [29, 41] and is similar to that reported by the ANGEL–ACT prospective large vessel occlusion registry in China [44]. This result could be explained by sociocultural issues related to gender.
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Regarding the stroke subtypes and stroke severity at presentation, in the current study, females had a significantly higher frequency of cardioembolic stroke compared to males, which was in accordance with the results from several previous studies [36, 44, 45]. However, Ton and colleagues, in 2023, found no difference between the sexes [29]. The higher frequency of cardioembolic stroke in females can be explained partially by their higher frequency of AF. Moreover, the lower rate of large artery atherosclerosis in females may be related to the absence of tobacco use in females.
Concerning stroke severity at onset, there were no significant sex differences in the stroke severity by the NIHSS scale and mRS on admission. This result agrees with the findings of Ton and colleagues in 2923 [29], who reported no sex differences in stroke severity at admission using the NIHSS scale. This finding could be related to patients receiving r-TPA exclusion criteria, as patients with NIHSS below ≤ 5 and above ≥ 25 were excluded.
Regarding the access to thrombolytic therapy (rTPA), pre-and in-hospital delays, response to thrombolysis, and complications, the current study shows the percentage of females received rTPA was lower than in males; however, we cannot say that females are less likely to receive thrombolysis. This finding could be attributed to the fact that we did not have information on the sex distribution of the initial cohort of patients admitted to each hospital with stroke.
In this study, the onset to needle time was significantly shorter in females than males (p = 0.035), and the door to the needle was significantly shorter in females than males. Our results were in accordance with the findings reported by Ton and colleagues in 2023. They found that females had significantly shorter door-to-needle and door-to-recanalization times [29]. However, the present findings contrast with the results reported by Cai and colleagues in 2020 [46], who stated that the onset-to-door time was not different between sexes, whereas the door-to-needle time was significantly longer in females than males. The current finding demonstrates that in-hospital treatment delays were not different between sexes, but pre-hospital delays were substantially shorter in females, which could be attributed to the fact that our cases are from Upper Egypt, the region in which the male is the predominant figure in the family; therefore, when a female suffers a stroke, there is a rapid response in seeking medical advice, resulting in a shorter time to arrive at the hospital and to receive treatment.
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Concerning the complications of rTPA, we found no significant difference between males and females in the intracerebral haemorrhage (ICH) rate after thrombolysis. This result contrasts with the findings by Cai and colleagues in 2020 [46], who reported that ICH was higher in females. However, sex was no longer associated with ICH after adjusting for age, disease severity, and relative pathogenic mechanisms.
Regarding the functional outcomes and mortality and their predictors, there was a significant improvement in the NIHSS in both sexes at 3 months, with no significant difference between them. Our results are consistent with those reported in several previous studies [7, 29, 36, 37], although Cai and colleagues, in 2020, reported that improvement in NIHSS scores was more significant in females than in males [46]. In contrast, Spaander and colleagues 2017 found that females had poorer functional outcomes than males [47]. The variations could be attributed to differences in the study sample sizes.
There were no gender differences in the stroke death rate, consistent with Abdu and Seyoum in 2022 [41]. In contrast to our results, Cai and colleagues in 2020 [46] found that the mortality rate was higher in females than in males after thrombolysis.
Despite longer onset-to-door times in males, the lack of outcome differences suggests a role for sex-based ischemic tolerance factors potentially related to hormone-mediated cytoprotection. However, interpretations are limited, given unaccounted confounders and sample size constraints in subset analysis.
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The potential predictors of poor Outcome 3 months after AIS included DM, door-to-needle time, and haemorrhage (DM and door-to-needle time for males; haemorrhage for females). The main potential predictors for mortality were haemorrhage and AF (AF for females; haemorrhage for males). These findings indicate the need for close follow-up of patients with these risk factors, proper rTPA patient selection to avoid haemorrhage risk, and aggressive management for good outcomes. We cannot definitively explain the sex-specific predictors of mortality and poor outcomes identified here. Sample size limitations restrict multivariate adjustment for possible confounders.
This study has several limitations. First, a relatively small sample size may have affected the statistical power and generalizability of the findings. Second, the lack of data on socioeconomic status, education, length of stay, and long-term follow-up precluded a more comprehensive analysis of potential confounding variables. To address these limitations, future studies should employ larger cohorts and collect more comprehensive demographic and longitudinal data to examine long-term sex-specific outcomes and associated factors better.
Conclusion
Our study has shown that sex differences exist in risk factors, stroke aetiology, and treatment timelines for AIS patients treated with rTPA. However, both sexes show similar improvements in neurological and functional outcomes. Predictors of poor outcome and mortality differ between sexes: DM and longer door-to-needle time for males, hemorrhage for females. Hemorrhage predicted mortality in males, while AF was associated with increased mortality in females. These findings have particular relevance for underserved Upper Egypt and emphasize the importance of considering sex-specific factors in managing AIS patients receiving rTPA, potentially informing tailored approaches to stroke care and risk assessment. Further research is needed to characterize sex effects in larger cohorts across diverse settings.
Acknowledgements
The authors would like to thank Professor John C Rothwell, Professor of Human Neurophysiology, UCL Institute of Neurology, for his valuable comments and revision of this manuscript.
Declarations
Ethics approval and consent to participate
This study was approved by the Assiut University, Faculty of Medicine’s ethical committee and registered with the Institutional Review Board (IRB no: 04-2023-300441). The 1964 WHO Declaration of Helsinki and its revisions were followed throughout the study. Each patient and/or caregiver gave written informed consent before the study began.
Consent for publication
Not applicable.
Competing interests
The authors declared no potential conflicts of interest concerning this article’s research, authorship, and/or publication of this article.
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Wer insgesamt zuversichtlicher aufs Leben blickt, trägt ein geringeres Risiko, später einmal an Demenz zu erkranken als pessimistischere Zeitgenossen. Dafür sprechen zumindest Ergebnisse einer Längsschnittdatenanalyse aus den USA. Ob mehr Optimismus allerdings tatsächlich einer Demenz vorbeugt, bleibt unklar.
Eine hochdosierte Influenza-Vakzine geht mit einer verzögerten Demenzdiagnose einher. Darauf deutet eine Auswertung von US-Gesundheitsdaten hin. Besonders auffällig sind die Effekte in den ersten Monaten nach der Impfung.
Intensive Senkung eines erhöhten Blutdrucks kann nach einer intrazerebralen Blutung die funktionelle Erholung verbessern – mutmaßlich über eine Reduktion der Hämatomausdehnung. Offenbar hängt das aber vom Ausgangsvolumen ab, wie eine Analyse ergeben hat.
Da schmeckt das Rinderfilet gleich doppelt so gut: Fleisch beugt einer aktuellen Studie zufolge einer Demenz vor. Allerdings gilt das nur für ApoE4-Träger. Diese haben sich im Laufe der Evolution offenbar an einen hohen Fleischkonsum angepasst – und brauchen ihre Steak-Rationen.
