https://orcid.org/0009-0008-1249-5190
Abstract
Background
Progressive arterial stiffening may increase the risk of recurrent cardiovascular events in ischemic stroke survivors. Information about factors associated with progressive arterial stiffening during the follow-up of young patients with ischemic stroke is lacking.
Methods
Arterial stiffness by carotid-femoral pulse wave velocity (cf-PWV) and ambulatory 24-hour blood pressure (24hBP) were assessed in 81 women and 190 men ≤60 years of age included in the Norwegian Stroke in the Young (NOR-SYS) study 3 months and 5.5 years after the incident ischemic stroke, representing baseline and follow-up. Covariables of change in cf-PWV were identified using linear regression analysis.
Results
At baseline, women had less prevalent hypertension (53% vs. 69%, p < 0.05), and lower clinic and 24hBP than men, whereas age, obesity, and prevalence of smoking and antihypertensive drug treatment did not differ. During follow-up, systolic 24hBP remained unchanged, while diastolic 24hBP fell significantly (p < 0.01). Cf-PWV was lower in women both at baseline (7.3 m/s vs. 8.1 m/s) and at follow-up (7.3 m/s vs. 8.0 m/s, both p < 0.001), but the average change during follow-up did not differ between genders. In linear regression analysis, an increase in cf-PWV at the 5-year follow-up was associated with the presence of hypertension and lower cf-PWV at baseline, and higher systolic 24hBP and lack of use of antihypertensive treatment at follow-up (all p < 0.05).
Conclusion
In ischemic stroke survivors participating in the NOR-SYS study, the 5-year increase in cf-PWV did not differ between genders and was associated with higher systolic 24hBP and lack of antihypertensive treatment.
PLAIN LANGUAGE SUMMARY
Progressive arterial stiffening increases the risk of recurrent stroke. More information about factors associated with progression of arterial stiffness in young ischemic stroke survivors is needed. This study followed 81 women and 190 men for 5 years and examined changes in arterial stiffness in relation to blood pressure levels and other factors.
Arterial stiffness was measured using the carotid-femoral pulse wave velocity. We also measured blood pressure at study visits and over a 24-hour period while the study participants led their daily life. Measurements were performed 3 months after the index ischemic stroke (baseline) and repeated after an average of 5.5 years of follow-up.
Our main finding was that hypertension is very common and is important for arterial health in young ischemic stroke survivors. An increase in arterial stiffness during follow-up was associated with hypertension, higher 24-hour blood pressure, and lack of use of blood pressure-lowering drugs in participants with hypertension. There were no differences between women and men.
This study shows the importance of proper blood pressure management in young ischemic stroke survivors to avoid progressive stiffening of the arteries. The results also demonstrated the value of using 24-hour measurements rather than office measurements in the evaluation of blood pressure control during treatment.
Introduction
Hypertension remains the most prevalent modifiable risk factor for ischemic stroke in both women and men [Citation1]. The incidence of ischemic stroke in young adults has increased over the past decades, in parallel with the increasing prevalence of cardiovascular risk factors [Citation2]. In the 15 cities young stroke study among European ischemic stroke survivors younger than 50 years of age, current smoking, dyslipidaemia, and hypertension were the most common cardiovascular risk factors [Citation3]. Recurrent stroke affects up to 15% of young ischemic stroke survivors over 10 years follow-up [Citation4], and is associated with an up to seven-fold higher mortality rate compared to an age- and sex-matched general population [Citation5], pointing to the importance of appropriate secondary prevention management.
In the prospective Norwegian Stroke in the Young (NOR-SYS) study which included patients ≤60 years with a documented ischemic stroke, recurrent cardiovascular events were particularly common in patients with atherosclerosis in pre-cerebral arteries [Citation6]. In a general population, the presence of atherosclerosis in both the aorta and carotid arteries was associated with increased arterial stiffness [Citation7]. Arterial stiffness increases in parallel with age and systolic blood pressure (BP) in both women and men and may be assessed by carotid-femoral pulse wave velocity (cf-PWV) [Citation8–10]. However, factors associated with progressive arterial stiffness in younger patients with ischemic stroke have not been well characterized. Thus, the aim of the present study was to identify covariables of progression of arterial stiffness, measured by cf-PWV, over five years in patients participating in the NOR-SYS research programme.
Methods
Study population
The prospective NOR-SYS research programme has been conducted at Haukeland University Hospital since 2010 [Citation11]. A total of 385 patients with acute ischemic stroke aged 15-60 years were included between 2010 and 2015 [Citation12]. Of these, 352 patients underwent their initial cf-PWV examination 3 months after the incident ischemic stroke, and 271 returned for the scheduled 5-year follow-up visit at the Department of Heart Disease. Of the non-returning participants, 15 died, 8 were too debilitated to participate in follow-up examinations, 15 moved out of our health region and 43 failed to show up at their appointments.
The 5-year follow-up visits started in October 2015, but were interrupted by the Covid-19 pandemics and were therefore not concluded until June 2022. All the participants provided written informed consent. This study was approved by the Regional Committee for Medical Research Ethics of Western Norway (2010/74 and 19422). This research programme was registered at ClinicalTrials.gov (NCT01597453).
Cardiovascular risk factors
Attended clinical BP was measured in a seated position after 5 minutes of initial rest. Three serial measurements were performed at 1-minute intervals using a regularly calibrated automated blood pressure device with an appropriate cuff size (Welch Allyn NIBP 3400 series, Hill-Rom Holdings, Chicago, IL, USA). Hypertension was defined as elevated clinic BP (systolic BP ≥ 140 mmHg or diastolic BP ≥ 90 mmHg) or the use of antihypertensive medication at baseline. A 24-hour ambulatory blood pressure (24hBP) recording was performed using a DiaSYS Integra II device (Novacor, Cedex, France). The device was mounted by a trained study nurse and pre-set to measure BP every 15 minutes during the day and every 30 minutes at night. If <70% of the BP measurements were valid, the 24hBP recording was repeated. Elevated 24hBP was considered present if systolic 24hBP ≥130 mmHg or diastolic 24hBP ≥80 mmHg [Citation13]. Uncontrolled hypertension was defined as elevated 24hBP at follow-up. 247 participants (91%) accepted 24hBP measurement at follow-up.
Self-reported medical history was captured in a standardised questionnaire, including history of cardiovascular disease, diabetes mellitus, smoking status, and medical drug therapy at baseline and follow-up. Information was quality assured against the digital hospital records and the electronic prescription portal by study personnel. Standard venous blood samples were drawn at the index admission or baseline visit for analysis of serum lipids, HbA1c, electrolytes, and renal function. Body mass index (BMI) was calculated using the body weight/body height2 ratio. Obesity was considered present when BMI ≥30 kg/m2. Diabetes mellitus was considered present if fasting blood glucose was ≥7 mmol/L, HbA1c was ≥6.5% [Citation14], or if use of glucose lowering drugs was reported in the individual participant at the incident hospitalization.
Arterial stiffness
Arterial stiffness was assessed using a SphygmoCor apparatus (AtCor Medical, Sydney, West Ryde, Australia). All examinations were performed under standardized laboratory conditions in accordance with the guidelines [Citation15]. Applanation tonometry was used to measure central BP and cf-PWV. To assess cf-PWV, synchronized pulse pressure waveforms were acquired transcutaneously from the carotid and femoral arteries. Cf-PWV was calculated as the distance between the recording sites divided by the transit time [Citation15]. The cf-PWV value was averaged over 10 cardiac cycles in a single measurement. A cf-PWV > 10 m/s was defined as increased in both genders [Citation13].
Statistical analyses
Data management and statistical analyses were performed using SPSS statistical package version 28 (IBM SPSS Statistics, Armonk, New York, USA). Continuous data were reported as mean values and standard deviation (SD). Categorical variables are reported as percentages. Group comparisons were performed using chi-squared tests or two-sample t-tests for categorical and continuous variables, respectively. Correlations were explored using Pearson’s correlations and univariate linear regression analysis. Multivariable associations of changes in cf-PWV with baseline and follow-up covariables, were examined by linear regression analyses using the enter methods and collinearity tools. The final combined model was run using the stepwise forward method. The results are reported as standardised β-coefficients and p-values. A two-tailed p-value of <0.05 was considered statistically significant in all analyses.
Results
Clinical characteristics and change during follow-up in women and men
The study participants were 49.5 ± 9.9 years old at baseline and included 30% women and 70% men (). At baseline, 4% had atrial fibrillation, 7% had diabetes mellitus, and 11% had a history of prior cardiovascular disease. Daily smoking was common at baseline but significantly reduced during follow-up (). Fewer women than men used statins at follow-up (63% vs. 76%, p < 0.05) ().
Table 1. Clinical characteristics of women (n = 81) and men (n = 190) with ischemic stroke at age up to 60 years at baseline and at 5-year follow-up, included in the Norwegian Stroke in the Young Study.
Women had less prevalent hypertension (53% vs. 69%, p < 0.05) and lower clinic, 24hBP, and central BP than men at baseline (, ). During follow-up, the prevalence of treated hypertension increased in both women and men (p < 0.001) ().
Table 2. Blood pressure measurements and antihypertensive medication in women (n = 81) and men (n = 190) with ischemic stroke, at baseline and after 5-year follow-up, included in the Norwegian Stroke in the Young Study.
Table 3. Vascular characteristics of women (n = 81) and men (n = 190) with ischemic stroke, at baseline and 5-year follow-up, included in the Norwegian Stroke in the Young Study.
Blood pressure control
Among 170 patients treated for hypertension at follow-up, 154 had valid 24hBP recording. Assessment of BP control differed significantly between clinic BP compared to 24hBP (p < 0.05). Based on clinic BP, 55% had uncontrolled hypertension (52% of women vs. 56% of men, p = 0.73). Among patients with uncontrolled clinic BP, this was confirmed in 44% by 24hBP, while white coat effect was found in 56% (). Among patients treated for hypertension with normal clinic BP, an additional 28% (6% of women vs. 41% of men, p < 0.001) had elevated 24hBP, reflecting masked uncontrolled hypertension. Furthermore, elevated nocturnal BP was common at follow-up, found in 45% of the total study cohort (55% of men and 20% of women, p < 0.001) ().
Figure 1. Correspondence between clinic BP and 24hBP, in ischemic stroke patients treated for hypertension (n = 154), at 5-year follow-up in the Norwegian Stroke in the Young Study.
Additionally, the vast majority of patients with treated hypertension (86% of women vs. 82% of men, p = 0.58) remained with a clinic BP above the recommended treatment threshold of <130/80mmHg for ischemic stroke survivors [Citation16].
Cf-PWV in different BP categories
Among patients not using antihypertensive drug therapy at follow-up, cf-PWV did not differ between patients with masked hypertension compared to other BP categories (normotension, white coat hypertension, and hypertension, all p > 0.221). Among patients treated with antihypertensive drug therapy at follow-up, the group with masked uncontrolled hypertension had lower cf-PWV compared to those with white coat hypertension (7.6 vs. 8.8 m/s) or uncontrolled hypertension (7.6 vs. 8.7 m/s, both p < 0.05).
When comparing patients with normal systolic night-time BP to those with elevated systolic night-time BP, cf-PWV at follow-up was higher in the group with elevated systolic night-time BP (8.7 vs. 7.6 m/s, p < 0.001). No difference in cf-PWV at follow-up was found between groups with normal and elevated diastolic night-time BP.
Cf-PWV and change during follow-up
Cf-PWV was lower in women than in men both at baseline and follow-up (both p < 0.001), but the average change during follow-up did not differ between the genders (, ). In univariate analyses, a larger increase in cf-PWV during follow-up was associated with the presence of obesity, hypertension, higher clinic systolic BP, and lower cf-PWV at the baseline examination (all p < 0.05), while no significant associations were found with age, gender, diabetes mellitus, 24h systolic BP, LDL-cholesterol, or smoking (). In the multivariable analyses, only the presence of baseline hypertension and cf-PWV at baseline remained significant covariables ().
Figure 2. Mean cf-PWV values at baseline and 5-year follow-up, in women (n = 81) and men (n = 190) with ischemic stroke, included into the Norwegian Stroke in the Young Study.
Table 4. Covariables of change in cf-PWV in patients with ischemic stroke (n = 271), at baseline and 5-year follow-up, included in the Norwegian Stroke in the Young Study.
When exploring the association of increase in cf-PWV with findings at the follow-up visit, lack of antihypertensive drug treatment in patients with hypertension and higher 24h systolic BP were associated with increase in cf-PWV in univariable analysis (both p < 0.05), while clinic systolic BP, tobacco smoking, statin treatment, and obesity at follow-up were not (). In a combined multivariable analysis, including variables with significant associations at baseline or follow-up, lower baseline cf-PWV and higher 24h systolic BP at follow-up remained significantly associated with increase in cf-PWV (both p < 0.005).
When grouping the cohort according to decrease or increase in cf-PWV during follow-up, those that had an increase in cf-PWV had a higher 24h systolic BP (120 vs. 116 mmHg), daytime systolic BP (123 vs. 120 mmHg) and night-time systolic BP (108 vs. 105 mmHg, all p < 0.05) at follow-up compared to those who experienced a decrease in cf-PWV, while none of these BPs differed between these groups at baseline.
Discussion
This study demonstrated the importance of hypertension management in counteracting progressive arterial stiffening in young and middle-aged ischemic stroke survivors. Both uncontrolled 24h systolic BP and lack of antihypertensive drug therapy were associated with an increase in cf-PWV during follow-up. Furthermore, masked uncontrolled hypertension and uncontrolled BP in subjects with treated hypertension were common, indicating the usefulness of 24hBP recording in this patient group.
In the current study, the mean cf-PWV values remained virtually unchanged over the 5.5-year follow-up period. In contrast, in the Oxford Vascular (OxVasc) study of patients with transient ischemic attack or minor stroke, cf-PWV increased by 2.4% annually during the 5.8-year follow-up period [Citation17]. However, the OxVasc participants were on average 16 years older than the present NOR-SYS cohort, and the cf-PWV increase was predominantly found in subjects older than 55 years of age [Citation17]. Previous population-based studies have documented a steeper increase in cf-PWV in women than in men, particularly after menopause [Citation8, Citation9, Citation18]. However, in the present study, no difference in cf-PWV increase between the genders was observed. Of note, the present study in ischemic stroke survivors had a limited follow-up period, and many women probably were premenopausal at baseline, given that the average menopausal age is 53 years in Norway.
Uncontrolled hypertension was also common in this cohort. As demonstrated, among patients with treated hypertension, clinic BP overestimated the prevalence of uncontrolled BP in more than half of the cases but missed the diagnosis of masked uncontrolled hypertension in 28% when compared to 24hBP. In a recent publication on cryptogenic ischemic stroke survivors younger than 50 years of age, 50% of patients with hypertension had uncontrolled office BP, and 20% had uncontrolled 24hBP [Citation19]. A more accurate identification of uncontrolled BP with 24hBP measurements in ischemic stroke survivors is in line with the pooled knowledge from hypertension studies in non-stroke subjects [Citation20]. The current study adds to this by demonstrating 24h systolic BP as an important marker of arterial stiffness progression in ischemic stroke survivors, reflecting progressive arterial aging, which has been linked to the risk of recurrent stroke [Citation21].
Another finding in this cohort was the relatively high prevalence of nocturnal hypertension, as unveiled by 24hBP measurements, adding to a previous report based on baseline findings in this cohort [Citation22]. Nocturnal hypertension has been associated with adverse prognosis and organ damage [Citation23]. In a nationwide hospital-based longitudinal cohort study in China, reverse dipping (higher BP at night-time than during daytime) was particularly associated with poor functional outcomes 1 year after ischemic stroke [Citation24]. This further underlines the importance of performing 24hBP measurement in young patients with ischemic stroke to ensure good BP control as part of targeted secondary prevention. Indeed, a recent review summarizing the key findings of data from international databases on ambulatory and home BP measurements in relation to cardiovascular outcomes, found 24h and night-time BP levels to be the best predictors for adverse health outcomes [Citation25].
The current European [Citation16] and American [Citation26] guidelines for stroke prevention recommend an office BP treatment target of <130/80 mmHg for secondary prevention to reduce the risk of recurrent vascular events. In the present cohort, this was achieved in only 23% of patients at follow-up. None of these guidelines currently recommend 24hBP measurements to initiate or evaluate antihypertensive treatment. However, the European Stroke Organization 2022 guideline working group supported out-of-office BP measurements, wherever feasible, to achieve better long-term BP control [Citation16]. This recommendation is supported by the current findings.
Obesity was common among both women and men in the present cohort, and its prevalence increased during the follow-up period. Although obesity at baseline was associated with an increase in cf-PWV in the univariate analysis, the association was lost in the adjusted analysis. In particular abdominal obesity has been associated with higher arterial stiffness in cross-sectional population-based cohorts [Citation27, Citation28]. However, prospective observational studies in ischemic stroke survivors have demonstrated that being underweight rather than obese is associated with higher mortality and recurrent cardiovascular events, probably reflecting the obesity paradox [Citation29, Citation30]. However, these studies did not include an assessment of the arterial stiffness.
Study limitations
The limitations of this study include the small sample size and a relatively short follow-up period of 5.5 years. Furthermore, serum cholesterol levels were not measured at follow-up, precluding a more detailed assessment of the association of lipids and lipid control with progression of arterial stiffness. However, the present study adds to the current knowledge in this field by providing information on the importance of accurate BP measurement and management for progressive arterial aging in young and middle-aged ischemic stroke survivors.
Conclusion
In the prospective NOR-SYS study, an increase in cf-PWV did not differ between genders over a 5.5-year follow-up period, while higher 24h systolic BP and lack of treatment for hypertension were associated with increase in arterial stiffness. Ambulatory 24hBP measurements revealed uncontrolled BP in 44% of patients with treated hypertension and masked uncontrolled hypertension in 28% of those with normal clinic BP at follow-up. These results suggest that 24hBP measurements should be incorporated in the diagnostic work-up and follow-up of young patients with ischemic stroke, to ensure better risk stratification and management of this patient group.
Author contributions
All listed authors have contributed substantially to the manuscript and agreed to the final submitted version.
Acknowledgements
We would like to express our gratitude to the study participants for their time and willingness to contribute to medical research. In addition, this study would not have been possible without the commitment and dedicated work of the study nurse, Liv Himle RN.
Disclosure statement
The authors did not report any potential conflicts of interest.
Data availability statement
The participants in this study did not agree to share data publicly; hence, the supporting data were not made publicly available.
Additional information
Funding
References
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