Abstract
The association between blood pressure and intracranial artery stenosis (ICAS) in different age groups has not been elucidated. Using data from the “China Hypertension Survey,” we conducted a cross‐sectional analysis of the association between blood pressure parameters and ICAS. In this study, participants older than 35 years were selected by stratified, multistage random sampling. Blood pressure was measured repeatedly at rest, and ICAS was assessed by transcranial doppler ultrasound. Binary logistic regression analysis was used to demonstrate the association between different blood pressure indicators and ICAS. Of the 3640 participants included (mean age 63 ± 13 years old, 57.8% female), systolic blood pressure (SBP) and pulse pressure (PP) were associated with ICAS in the general population; the multivariable adjusted odds ratio (OR) and corresponding 95% confidence interval (95% CI) of ICAS and multivessel stenosis were 1.32 (1.21, 1.45) and 1.29 (1.14, 1.46) per standard deviation (SD) increase in SBP and 1.44 (1.30, 1.59) and 1.52 (1.33, 1.74) for PP, respectively. Further analysis of this association in different age groups revealed inconsistent results between SBP and ICAS. Prehypertension (120 ≤ SBP < 140) could predict ICAS in the older group but not in the younger group, and the positive association between SBP and multivessel stenosis disappeared in the younger age group (P > .05 in all SBP subgroups). In conclusion, SBP and PP could not only identify ICAS in the middle‐aged and elderly population but could also provide some information about ICAS burden; however, these associations need to be interpreted differentially based on age subgroup.
Keywords: blood pressure, intracranial artery stenosis, the middle‐aged and elderly population
1. INTRODUCTION
Intracranial artery stenosis (ICAS) has been established as a major cause of ischemic stroke worldwide1and could account for 50% of ischemic stroke in China.2 Patients with ICAS usually have a higher recurrence risk and poor outcome.3, 4, 5 One study suggested that patients with advanced atherosclerosis (ICAS of ≥2 different intracranial arteries or increased numbers of stenosis/occlusive arteries) have a much higher recurrent stroke risk and composite vascular outcome than participants without ICAS or single ICAS.6, 7, 8
Hypertension as a risk factor of stroke and ICAS has been known for a long while9; however, epidemiological studies regarding the association between different blood pressure parameters and cardiovascular disease (CVD) have revealed confusing results. Some studies have suggested that pulse pressure (PP) is the strongest predictor of cardiovascular risk,10, 11 while others have indicated that systolic blood pressure (SBP) is much better than PP for predicting CVD. PP as an indicator of arterial stiffness is valuable for predicting CVD only in older participants, and this association is SBP‐dependent.12, 13 Regarding the association between blood pressure indicators and ICAS, one study compared four commonly used blood pressure indexes (SBP, diastolic blood pressure [DBP], PP, and mean artery pressure [MAP]) for identifying ICAS in a community‐based cohort, and the results demonstrated that PP was the most sensitive predictor of ICAS.14 However, the researchers did not take into consideration the heterogeneous blood pressure characteristics in different age groups. A previous study on age and hypertension subtypes suggested that the prevalence of hypertension, especially isolated systolic hypertension and systolic‐diastolic hypertension, is increasing with the aging of the population.15 Moreover, no data about the association between blood pressure indexes and ICAS burden were shown in their study.
The purpose of this study was to investigate the association between different blood pressure indexes and ICAS in the middle‐aged and elderly population comprehensively. A better understanding of the relationship between different blood pressure indicators and ICAS will provide some insight into the pathophysiology of intracranial atherosclerosis, as well as some guidance for stroke risk assessment.
2. METHODS
2.1. Study design and participants
The current study was conducted within the framework of the China Hypertension Survey (CHS), a national multicenter cohort study. The rationale, study design, sampling method, and main results have been described elsewhere.16, 17 Briefly, the CHS was a cohort study investigating the prevalence of hypertension in China and following up its effects on cardiovascular events. In this study, a stratified, multistage random sampling method was used to obtain a nationally representative sample of the general population in different age groups. All participants were investigated comprehensively by a group of trained investigators within a framework of a predefined protocol, including obtaining information on demographic characteristics, medical history, and medications. participants older than 35 years were also required to undergo blood tests and vascular examination by carotid and transcranial doppler (TCD) ultrasound to assess atherosclerosis. In this analysis, participants older than 35 years from 3 districts in the urban area (Xicheng, Fangshan, and Tongzhou) and 1 county in the rural area (Yanqing) were included. participants were excluded if they had no complete blood pressure records or TCD results.
The study protocol conformed to the ethical guidelines of the 1975 Declaration of Helsinki and was also approved by the Ethics Committees of Fuwai Hospital and Xuanwu Hospital. Written informed consent was obtained from all participants in this study.
2.2. Data collection and covariate assessment
Each participant underwent a comprehensive assessment of cardiovascular risk factors. The risk factors defined in this study were as follows: diabetes mellitus was diagnosed in those who had a previous history of diabetes or who were on insulin or oral hypoglycemic medication, and participants with fasting glucose over 7 mmol/L were also considered to have diabetes mellitus. Hyperlipidemia was diagnosed according to the adult treatment panel III guidelines18, 19(total cholesterol ≥240 mg/dL, low‐density lipoprotein cholesterol [LDL‐C] ≥160 mg/dL or high‐density lipoprotein cholesterol [HDL‐C] <40 mg/dL) or according to lipid‐lowering medication use. Coronary artery disease and chronic kidney disease (CKD) were also diagnosed based on medical history, and CKD was further confirmed by eGFR (<60 mL/1.73 m2/min). Smoking and alcohol consumption were self‐reported: smoking was defined as having smoked in the past or currently smoking, and alcohol consumption was based on moderate or heavy alcohol consumption (≥2 standardized alcoholic drinks per day). Body mass index (BMI) was calculated as weight in kilograms divided by the square of the height in meters. Blood tests were completed at the national center for cardiovascular disease in Fuwai Hospital, and all procedures were conducted as the protocol demanded.
2.3. Blood pressure measurement
Blood pressure was measured on the right arm after at least 5 minutes of rest by a unified corrected electronic blood pressure monitor (Omron professional portable blood pressure monitor; Omron Corporation) with the participant in a seated position. A total of three measurements were performed at an interval of 30 seconds. The average of the three measurements was used for the analysis. PP was calculated from SBP and DBP.
In this study, hypertension was diagnosed referring to the Eighth Joint National Committee (JNC8) as well as Chinese hypertension guidelines.20, 21 participants with an average SBP ≥140 mm Hg or DBP ≥90 mm Hg or self‐reported use of any antihypertensive drugs during the past 2 weeks met the criteria for hypertension.
2.4. ICAS assessment
ICAS was diagnosed based on the TCD results. All TCD examinations were performed by two experienced vascular neurologists using portable machines (TC 8080, EME). All participating TCD performers were trained by a senior vascular sonographer before the conduction of the study. In cases of uncertainties, the third senior vascular neurologist would confirm the diagnosis. All examiners were blinded to the clinical information.
In this study, ICAS was diagnosed based on systolic peak velocity.22 To be brief, the cutoff velocity for stenosis is 140 cm/s for the middle cerebral artery, 120 cm/s for the anterior cerebral artery and siphon internal carotid artery, and 100 cm/s for the posterior cerebral artery and vertebral‐basilar artery. For participants with poor temporal windows, the blood flow was detected by orbital windows. Any cerebral artery that could not be detected by both temporal windows and orbital windows was defined as nonstenotic. participants who had more than one vessel stenosis were categorized as having multivessel stenosis.
2.5. Data analysis
Student's t test or chi‐square test was used to compare basic characteristics between groups depending on variable types; SBP and DBP were analyzed as continuous and categorical variables. As categorical variables, blood pressure indicators (SBP, DBP, and PP) were grouped per 10 mm Hg, and as continuous variable, we assessed the corresponding odds ratios (ORs) of ICAS or multivessel stenosis per standard deviation (SD) increase in blood pressure indicators. Binary logistic regression analysis was used to demonstrate the association between different blood pressure indicators and ICAS. Two‐tailed P values <.05 were considered statistically significant. All statistical analyses were performed using SPSS19.0.
3. RESULTS
A total of 6906 participants older than 35 years were recruited, and 3951 of the participants completed the TCD assessment. After excluding 311 participants with missing information, 3640 participants were included in the analysis. The mean age was 63 ± 13 years old, 57.8% were female, 629 (17.3%) participants were found to have ICAS, and 283 (7.8%) presented with multivessel stenosis in this cohort (Figure 1). The demographic characteristics and risk factors of the participants who were included and excluded are shown in Table S1. The participants who were included were much older and more likely to have cardiovascular risk factors.
Figure 1.
Flowchart of participants screening
3.1. Characteristics of participants included in the ICAS and non‐ICAS groups
The demographic characteristics and risk factors of participants with and without ICAS are shown in Table 1. participants with ICAS were much older (66 vs 62 years old, P < .05), less likely to be female (49.3% vs 59.5%, P < .05), and more likely to have hypertension, diabetes, coronary artery disease, chronic kidney disease, and a smoking habit than those without ICAS (all P < .05). No difference in hyperlipidemia, alcohol consumption, or BMI was observed between the two groups. In terms of blood pressure indexes, the mean SBP was much higher, the DBP was lower, and the PP was wider in the ICAS group than in the non‐ICAS group (all P < .05).
Table 1.
Basic characteristics of participants with and without ICAS
|
Variable （M ± SD or n, %） |
Total (n = 3640) |
ICAS （n = 629） |
Non‐ICAS （n = 3011） |
P value |
|---|---|---|---|---|
| Age (y) | 63 ± 13 | 66 ± 11 | 62 ± 13 | <.01 |
| Sex (Female) | 2102 (57.8) | 310 (49.3) | 1793 (59.5) | <.01 |
| Risk factors | ||||
| Hypertension | 2175 (59.8) | 468 (74.4) | 1707 (56.7) | <.01 |
| Antihypertensive drugs | 1433 (39.4) | 324 (51.5) | 1109 (36.8) | <.01 |
| Diabetes | 784 (21.6) | 196 (31.2) | 588 (19.6) | <.01 |
| Hyperlipidemia | 2088 (59.0) | 377 (61.0) | 1711 (58.6) | .27 |
| Smoking | 1115 (30.8) | 230 (36.6) | 885 (29.6) | <.01 |
| Drinking | 992 (27.3) | 182 (28.9) | 810 (26.9) | .31 |
| BMI (kg/m2) | 25.8 ± 3.9 | 25.5 ± 3.6 | 25.8 ± 3.9 | .12 |
| CAD | 338 (9.3) | 82 (13.0) | 256 (8.5) | <.01 |
| CKD | 644 (19.0) | 135 (22.9) | 509 (18.1) | <.01 |
| Blood test (mmol/L) | ||||
| Glucose | 6.20 ± 1.75 | 6.59 ± 2.11 | 6.11 ± 1.65 | <.01 |
| Total cholesterol | 4.90 ± 1.00 | 4.92 ± 1.07 | 4.90 ± 0.99 | .60 |
| HDL‐C | 1.41 ± 0.37 | 1.36 ± 0.37 | 1.42 ± 0.36 | <.01 |
| LDL‐C | 2.87 ± 0.83 | 2.92 ± 0.86 | 2.86 ± 0.83 | .09 |
| BP (mm Hg） | ||||
| SBP | 135 ± 18 | 140 ± 19 | 134 ± 18 | <.01 |
| DBP | 76 ± 11 | 75 ± 11 | 76 ± 11 | <.01 |
| PP | 59 ± 16 | 65 ± 17 | 57 ± 15 | <.01 |
P for ICAS and non‐ICAS group.
Abbreviations: BMI, body mass index; CAD, coronary artery disease; CKD, chronic kidney disease; DBP, diastolic blood pressure; HDL‐C, high‐density lipoprotein cholesterol; ICAS, intracranial artery stenosis; LDL‐C, low‐density lipoprotein cholesterol; PP, pulse pressure; SBP, systolic blood pressure.
3.2. Association between blood pressure indexes and ICAS based on logistic regression analysis
Table 2 shows the multivariate adjusted regression results of blood pressure indexes and ICAS, as well as multivessel stenosis. SBP was associated with ICAS in all categories, with ORs ranging from 1.52 to 2.97 (all P < .05). In general, the risk of ICAS could increase by 32% with per SD increase (18 mm Hg) in SBP. While PP was associated with ICAS in the greater than 60 mm Hg groups, the OR exhibited a trend toward increasing with the increment of PP; the risk of ICAS could increase by 44% per SD increase (16 mm Hg) in PP.
Table 2.
Association between blood pressure parameters and ICAS
| Blood pressure index (mm Hg) | ICAS | Multivessel stenosis | ||
|---|---|---|---|---|
| OR (95%CI） | P value | OR (95%CI) | P value | |
| SBP | ||||
| <120 | 1.00 (reference) | 1.00 (reference) | ||
| 120‐129 | 1.69 (1.16, 2.22) | <.01 | 1.19 (0.74, 1.90) | .47 |
| 130‐139 | 1.52 (1.10, 2.11) | .01 | 1.46 (0.93, 2.29) | .11 |
| 140‐149 | 1.78 (1.26, 2.51) | <.01 | 1.41 (0.87, 2.29) | .17 |
| 150‐159 | 2.30 (1.58, 3.35) | <.01 | 1.68 (0.99, 2.85) | .05 |
| ≥160 | 2.97 (2.06, 4.28) | <.01 | 2.55 (1.56, 4.18) | <.01 |
| 1SD (18 mm Hg) increment | 1.32 (1.21, 1.45) | <.01 | 1.29 (1.14, 1.46) | <.01 |
| DBP | ||||
| <60 | 1.00 (reference) | |||
| 60‐69 | 0.72 (0.49, 1.06) | .09 | ||
| 70‐79 | 0.86 (0.60, 1.25) | .43 | ||
| 80‐89 | 0.73 (0.49, 1.09) | .12 | ||
| ≥90 | 0.68 (0.43, 1.09) | .11 | ||
| 1SD (11 mm Hg) increment | 0.96 (0.87, 1.06) | .44 | ||
| PP | ||||
| <50 | 1.00 (reference) | 1.00 (reference) | ||
| 50‐59 | 1.19 (0.90, 1.58) | .22 | 1.58 (1.03, 2.42) | .04 |
| 60‐69 | 1.62 (1.21, 2.18) | <.01 | 1.86 (1.19, 2.92) | <.01 |
| 70‐79 | 2.48 (1.80, 3.41) | <.01 | 2.93 (1.83, 4.71) | <.01 |
| ≥80 | 2.84 (2.03, 3.98) | <.01 | 3.90 (2.41, 6.31) | <.01 |
| 1SD (16 mm Hg) increment | 1.44 (1.30, 1.59) | <.01 | 1.52 (1.33, 1.74) | <.01 |
Adjusted for age, sex, diabetes, hyperlipidemia, antihypertensive medication, BMI, smoking, drinking, coronary artery disease, and chronic kidney disease in multivariate analysis.
Abbreviations: CI, confidence interval; DBP, diastolic blood pressure; ICAS, intracranial artery stenosis; OR, odds ratio; PP, pulse pressure; SBP, systolic blood pressure; SD, standard deviation.
In addition, both SBP and PP as continuous variables were associated with multivessel stenosis, with OR = 1.29, 95% CI (1.14, 1.46) and OR = 1.52, 95% CI (1.33, 1.74), individually. However, as a categorical variable, the positive relationship between SBP and multivessel stenosis could be seen only in the SBP ≥ 160 mm Hg subgroups. No association between DBP and ICAS was found in this cohort (all P > .05).
3.3. Associations between SBP, PP, and ICAS by age subgroups
Based on the abovementioned results, we further compared the associations between SBP, PP, and ICAS and multivessel stenosis in different age subgroups, respectively. Figure 2 shows the prevalence of ICAS and multivessel stenosis distribution trends by age and blood pressure level. The incidence of ICAS and multivessel stenosis exhibited an increasing trend with increasing age and blood pressure levels. However, the cutoff blood pressure values for discriminating ICAS differed between the two groups. Prehypertension status (120 ≤ SBP < 140) could identify ICAS in the elderly group but not in the younger population. Moreover, the positive association between SBP and multivessel stenosis disappeared in the younger age group but was significant in the elderly group (Figure 3A). As for the association between PP and ICAS, although the PP ranges in identifying ICAS differed between the two age groups, a higher PP (≥70 mm Hg) could predict multivessel stenosis in both groups (Figure 3B).
Figure 2.
Prevalence of ICAS, multivessel stenosis according to SBP, PP categories, and age subgroups. (The x‐axis denotes SBP subgroups in A, B, and PP subgroups in C, D [mm Hg]. y‐axis denotes the prevalence of ICAS in A, C, and multivessel stenosis in B, D [%]. z‐axis represents age subgroups [y])
Figure 3.
Association between blood pressure indicators and ICAS by age subgroups. (A: SBP and ICAS by age subgroups; B: PP and ICAS by age subgroups; Adjusted age, sex, diabetes, hyperlipidemia, antihypertensive medication, BMI, smoking, drinking, coronary artery disease, and chronic kidney disease in multivariate analysis.)
4. DISCUSSION
Our study revealed some novel knowledge about blood pressure parameters and ICAS by analyzing a representative population: (a) SBP and PP can not only be used to identify ICAS in the general middle‐aged and elderly population but can also inform ICAS burden. (b) The cutoff value of SBP for identifying ICAS differs among different age groups. (c) The association between SBP and multivessel stenosis is much stronger in the elderly population than in the younger group. (d) No association between DBP and ICAS was found in this cohort.
4.1. Blood pressure indexes and ICAS
Our results validated the positive relationship between SBP, PP, and ICAS in a population with asymptomatic polyvascular abnormalities in a community‐based study investigating different blood pressure indexes for predicting ICAS,14 and further demonstrated their association in different age subgroups, which has not been shown before. A Korean study indicated that stage 1 hypertension (SBP 130‐139 mm Hg or DBP 80‐89 mm Hg based on the 2017 ACC/AHA hypertension guidelines23) can be used as a predictor of ICAS by retrospectively analyzing the association between different blood pressure levels and ICAS in health checkup participants.24 However, our study demonstrated the different roles of blood pressure levels and ICAS in different age subgroups, and the cutoff value of SBP in identifying ICAS is much higher in the younger age group. Some distinctions and hypotheses are proposed here. First, our study focuses on the middle‐aged and elderly population, while a significantly younger age (mean age 56 years old) could be seen in the Korean study. Second, the absolute difference in age can bring about differences in hypertension subtype distribution between the two cohorts. The proportion of participants with isolated systolic and systolic‐diastolic hypertension is much higher in the older population,15 which may also have an effect on the results to some extent. Third, the significantly lower prevalence of ICAS in their study (3% in their routine health checkup population vs 17.3% in our randomized sampling population) could possibly result in disproportionate estimation of the relationship between SBP and ICAS. Thus, the association between SBP level and ICAS in different age groups needs to be considered with caution.
4.2. Association between blood pressure indexes and ICAS burden
Our data about the association between blood pressure indexes and ICAS burden are a novel finding and will provide some additional evidence in the understanding of the relationship between blood pressure and ICAS. We used the number of stenotic arteries to assess ICAS burden in this study to facilitate comparison with a previous study about ICAS burden and stroke risk.6 Regarding the results, SBP and PP were associated with multivessel stenosis when considered as a continuous variable; however, as a categorical variable, the positive relationship could be seen only in participants in the SBP ≥ 160 mm Hg group, and this positive relationship was limited in the elderly group. Therefore, we should interpret the relationship between SBP and multivessel stenosis tentatively. We speculated that the accumulative blood pressure load contributes to multivessel stenosis. participants in the elderly group usually have a longer hypertension history and a higher blood pressure level; thus, the comparatively short hypertension history in the younger group needs to be compensated by an increased blood pressure level. Another fact is that elderly participants have a higher prevalence of other cardiovascular risk factors, which will also contribute to ICAS burden.
Another interesting finding in our study is the positive and significant relationship between higher PP and multivessel stenosis, even in different age groups. In other words, higher PP can be used as a predictor of ICAS burden, independent of age subgroup. However, an important point that needs to be mentioned here is that the general PP in the younger group is significantly lower than that in the elderly group, and few participants had a PP over 80 mm Hg, which can affect the result in some way. Otherwise, PP, as a substitute indicator of arterial stiffness, may share common risk factors with ICAS, both of which are the result of atherosclerosis. The association between increased arterial stiffness and ICAS has already been reported in a previous population‐based study.25 PP may be used as a potential indicator of ICAS burden in the middle‐aged and elderly populations.
4.3. Association between DBP and ICAS
Contradictory to a previous study on DBP and ICAS or cardiovascular disease,14, 26 we did not find any association between DBP and ICAS in this study. The negative findings in our study can be explained as follows. First, we focused on a middle‐aged and elderly population, and data from the Framingham heart study indicated that the predictive value of DBP decreases with the age increasing.27 The Systolic Blood Pressure Intervention Trial (SPRINT) subgroup analysis also suggested that lower DBP is not related to the first episode of stroke risk in the high‐risk population.28 Second, the DBP in this population was relatively lower than that in the previous study,14 both in the ICAS group and in the non‐ICAS group, and the absolute difference between groups was not as significant (only 1 mm Hg absolute difference between the ICAS and non‐ICAS groups), which could also underestimate the relationship between DBP and ICAS to some degree.
4.4. Strengths and limitations
The key strengths of this study are (a) the use of a large representative middle‐aged and elderly population sampled by demographics, and minimization of some bias by multistage sampling; (b) a thorough investigation between different blood pressure indexes and ICAS, as well as ICAS burden; and (c) most importantly, we found that the relationship between SBP and ICAS can be affected by age. The results of our study will add some knowledge about blood pressure indexes and ICAS burden, fill in the knowledge gap regarding the relationship between blood pressure parameters and stroke risk and provide some insight into stroke risk stratification.
However, there are some limitations to this study. First, this study focused on the middle‐aged and elderly population. Considering the blood pressure patterns in different populations, the conclusion could not be extrapolated to the general population. Second, the blood pressure indexes in this study were measured on one occasion, and the results may have been influenced by some undetermined factors; multiple measurements would be much better to evaluate blood pressure load. Third, TCD was used to access ICAS in our study; compared with other more reliable vascular imaging, TCD may underestimate the prevalence of ICAS to a certain extent, and failure to identify the causes of ICAS is another weak point. Finally, the cross‐sectional design of this study needs to be stated here, and many more prospective studies, including studies exploring accumulative blood pressure load and cardiovascular events, should be conducted in the future.
5. CONCLUSIONS
In conclusion, although SBP and PP were associated with ICAS and multivessel stenosis in the general middle‐aged and elderly population, their association in different age groups needs to be discerned.
CONFLICT OF INTEREST
No conflict of interest to declare for this study.
AUTHOR CONTRIBUTIONS
Xiaowei Song and Jian Wu proposed the analysis plan; Xiaowei Song and Qiannan Zhao contributed equally to the data interpretation and manuscript preparation. Qiannan Zhao, Chunxiu Wang, and Shaochen Guan performed statistical analyses. Yang Hua, Jun Li, and Beibei Liu interpreted the TCD data; Zhongying Zhang contributed to the acquisition of the data. Xianghua Fang contributed to the design and helped perform analysis with constructive discussion. Jian Wu and Xianghua Fang received the financial support and designed the whole study; Jian Wu reviewed and edited the manuscript.
Supporting information
ACKNOWLEDGMENTS
We thank all the participants and associated investigators in China Hypertension Survey.
Song X, Zhao Q, Hua Y, et al. Association between blood pressure and intracranial artery stenosis in a Chinese population. J Clin Hypertens. 2020;22:77–85. 10.1111/jch.13770
Fang and Wu contributed equally to this work; they are co‐corresponding authors.
Jian Wu is designated as the contact who in charge of the submission, peer review, and publication process.
Funding information
This study was supported by National Key Program in the Twelfth Five‐year Plan (Professor Xianghua Fang, Grant No. 2011BAI11B01) from the Chinese Ministry of Science and Technology, Commission of Science and Technology of Beijing (Professor Xianghua Fang, Grant No. D121100004912002), Beijing Municipal Administration of Hospitals’ Ascent Plan (Professor Jian Wu, Grant No. DFL20152201); Beijing Municipal Health Bureau project (Professor Jian Wu, Grant No.2013‐2‐034).
Contributor Information
Xianghua Fang, Email: xhfang163@163.com.
Jian Wu, Email: wujianxuanwu@126.com.
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