Risk Factors for Asymptomatic and Symptomatic Intracranial Atherosclerosis Determined by Magnetic Resonance Vessel Wall Imaging in Chinese Population: A Case-Control Study

Yongjun Han, Runhua Zhang, Dandan Yang, Dongye Li, Hualu Han, Huiyu Qiao, Shuo Chen, Yu Wang, Miaoxin Yu, Yin Hong, Zhiqun Wang, Xihai Zhao, Gaifen Liu, Yongjun Han, Runhua Zhang, Dandan Yang, Dongye Li, Hualu Han, Huiyu Qiao, Shuo Chen, Yu Wang, Miaoxin Yu, Yin Hong, Zhiqun Wang, Xihai Zhao, Gaifen Liu

Abstract

Background and purpose: The association between risk factors and intracranial atherosclerosis disease (ICAD) determined by magnetic resonance (MR) vessel wall imaging in Chinese population has not been investigated. The aim of this study was to investigate the associations of conventional vascular risk factors with asymptomatic and symptomatic ICAD using MR vessel wall imaging in Chinese population.

Methods: The study population was recruited from two cohort studies of ICASMAP and CAMERA comprised 104 symptomatic ICAD subjects (57.1 ± 11.1 years; 35.6% females), 51 asymptomatic ICAD subjects (70.1 ± 8.4 years; 50.0% females) and 418 controls (58.0 ± 13.3 years; 61.0% females) defined as asymptomatic subjects without ICAD on MR vessel wall imaging. We compared the vascular risk factors between the three groups using a multivariate logistic regression analysis.

Results: Compared with controls, there was a significant positive association between age (OR: 1.07, 95% CI: 1.03-1.10, p < 0.001) and hypertension (OR: 3.03, 95% CI: 1.45-6.36, p = 0.003) and asymptomatic ICAD. There was a positive association of smoking (OR: 3.41, 95% CI: 1.57-7.42, p = 0.001), hypertension (OR: 7.43, 95% CI: 3.81-14.49, p < 0.001) and diabetes (OR: 3.54, 95% CI: 1.93-6.49, p < 0.001) and an inverse association of high-density lipoprotein (HDL) (p < 0.017) with symptomatic ICAD. Compared to asymptomatic ICAD, there was a significant inverse association of age (OR: 0.86, 95% CI: 0.81-0.92, p < 0.001) and HDL (p < 0.001) with symptomatic ICAD.

Conclusion: Old age and hypertension are associated with asymptomatic ICAD and smoking, hypertension, diabetes and lower HDL are associated with an increased risk of symptomatic ICAD in Chinese population.

Clinical trial registration: URL: http://www.clinicaltrials.gov. Unique identifier: NCT03417063.

Keywords: atherosclerosis; intracranial artery; magnetic resonance; risk factors; vessel wall imaging.

Conflict of interest statement

The authors declare that they have no competing interests.

© 2022 Han et al.

Figures

Figure 1
Figure 1
The derivation of the study groups.

References

    1. Mortality GBD; Causes of Death C. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the global burden of disease study 2013. Lancet. 2015;385:117–171.
    1. Liu L, Wang D, Wong KS, Wang Y. Stroke and stroke care in China: huge burden, significant workload, and a national priority. Stroke. 2011;42(12):3651–3654. doi:10.1161/STROKEAHA.111.635755
    1. Wang W, Jiang B, Sun H, et al. Prevalence, incidence, and mortality of stroke in China: results from a nationwide population-based survey of 480687 adults. Circulation. 2017;135(8):759–771. doi:10.1161/CIRCULATIONAHA.116.025250
    1. Qureshi AI, Caplan LR. Intracranial atherosclerosis. Lancet. 2014;383(9921):984–998. doi:10.1016/S0140-6736(13)61088-0
    1. López-Cancio E, Galán A, Dorado L, et al. Biological signatures of asymptomatic extra- and intracranial atherosclerosis: the Barcelona-Asia (asymptomatic intracranial atherosclerosis) study. Stroke. 2012;43(10):2712–2719. doi:10.1161/STROKEAHA.112.661702
    1. Leng X, Wong KS, Liebeskind DS. Evaluating intracranial atherosclerosis rather than intracranial stenosis. Stroke. 2014;45(2):645–651. doi:10.1161/STROKEAHA.113.002491
    1. Banerjee C, Chimowitz MI. Stroke caused by atherosclerosis of the major intracranial arteries. Circ Res. 2017;120(3):502–513. doi:10.1161/CIRCRESAHA.116.308441
    1. Qiao Y, Anwar Z, Intrapiromkul J, et al. Patterns and implications of intracranial arterial remodeling in stroke patients. Stroke. 2016;47(2):434–440. doi:10.1161/STROKEAHA.115.009955
    1. Qiao Y, Guallar E, Suri FK, et al. MR imaging measures of intracranial atherosclerosis in a population-based study. Radiology. 2016;280(3):860–868. doi:10.1148/radiol.2016151124
    1. Zhang N, Zhang F, Deng Z, et al. 3D whole-brain vessel wall cardiovascular magnetic resonance imaging: a study on the reliability in the quantification of intracranial vessel dimensions. J Cardiovasc Magn Reson. 2018;20(1):39. doi:10.1186/s12968-018-0453-z
    1. Han Y, Qiao H, Chen S, et al. Intracranial artery stenosis magnetic resonance imaging aetiology and progression study: rationale and design. Brain Behav. 2018;8(12):e01154. doi:10.1002/brb3.1154
    1. Putaala J, Metso AJ, Metso TM, et al. Analysis of 1008 consecutive patients aged 15 to 49 with first-ever ischemic stroke: the Helsinki young stroke registry. Stroke. 2009;40(4):1195–1203. doi:10.1161/STROKEAHA.108.529883
    1. Griswold MG, Fullman N, Hawley C; GBD 2016 Alcohol Collaborators. Alcohol use and burden for 195 countries and territories, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2018;392(10152):1015–1035. doi:10.1016/S0140-6736(18)31310-2
    1. Yuan C, Mitsumori LM, Ferguson MS, et al. In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation. 2001;104(17):2051–2056. doi:10.1161/hc4201.097839
    1. Xu WH, Li ML, Gao S, et al. In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis. Atherosclerosis. 2010;212(2):507–511. doi:10.1016/j.atherosclerosis.2010.06.035
    1. Choi YJ, Jung SC, Lee DH. Vessel wall imaging of the intracranial and cervical carotid arteries. J Stroke. 2015;17(3):238–255. doi:10.5853/jos.2015.17.3.238
    1. Bae HJ, Lee J, Park JM, et al. Risk factors of intracranial cerebral atherosclerosis among asymptomatics. Cerebrovasc Dis. 2007;24(4):355–360. doi:10.1159/000106982
    1. Huang HW, Guo MH, Lin RJ, et al. Prevalence and risk factors of middle cerebral artery stenosis in asymptomatic residents in Rongqi county, Guangdong. Cerebrovasc Dis. 2007;24(1):111–115. doi:10.1159/000103125
    1. Uehara T, Tabuchi M, Mori E. Risk factors for occlusive lesions of intracranial arteries in stroke-free Japanese. Eur J Neurol. 2005;12(3):218–222. doi:10.1111/j.1468-1331.2004.00959.x
    1. Wang JC, Bennett M. Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ Res. 2012;111(2):245–259. doi:10.1161/CIRCRESAHA.111.261388
    1. López-Cancio E, Dorado L, Millán M, et al. The Barcelona-asymptomatic intracranial atherosclerosis (Asia) study: prevalence and risk factors. Atherosclerosis. 2012;221(1):221–225. doi:10.1016/j.atherosclerosis.2011.12.020
    1. Zhang S, Zhou Y, Zhang Y, et al. Prevalence and risk factors of asymptomatic intracranial arterial stenosis in a community-based population of Chinese adults. Eur J Neurol. 2013;20(11):1479–1485. doi:10.1111/ene.12210
    1. Park KY, Chung CS, Lee KH, Kim GM, Kim YB, Oh K. Prevalence and risk factors of intracranial atherosclerosis in an asymptomatic Korean population. J Clin Neurol. 2006;2(1):29–33. doi:10.3988/jcn.2006.2.1.29
    1. Kamal AK, Majeed F, Pasha O, et al. Clinical, lifestyle, socioeconomic determinants and rate of asymptomatic intracranial atherosclerosis in stroke free Pakistanis. BMC Neurol. 2014;14(1):155. doi:10.1186/s12883-014-0155-6
    1. Sasamura H, Itoh H. Hypertension and arteriosclerosis. Nihon Rinsho. 2011;69(1):125–130.
    1. Alexander RW; Theodore cooper memorial lecture. Hypertension and the pathogenesis of atherosclerosis. Oxidative stress and the mediation of arterial inflammatory response: a new perspective. Hypertension. 1995;25(2):155–161. doi:10.1161/01.HYP.25.2.155
    1. Zhou M, Offer A, Yang G, et al. Body mass index, blood pressure, and mortality from stroke: a nationally representative prospective study of 212,000 Chinese men. Stroke. 2008;39(3):753–759. doi:10.1161/STROKEAHA.107.495374
    1. Kurth T, Gaziano JM, Berger K, et al. Body mass index and the risk of stroke in men. Arch Intern Med. 2002;162(22):2557–2562. doi:10.1001/archinte.162.22.2557
    1. Bos D, van der Rijk MJ, Geeraedts TE, et al. Intracranial carotid artery atherosclerosis: prevalence and risk factors in the general population. Stroke. 2012;43(7):1878–1884. doi:10.1161/STROKEAHA.111.648667
    1. Hsu SP, Lee WS. Effects of female sex hormones on the development of atherosclerosis. Chin J Physiol. 2020;63(6):256–262. doi:10.4103/CJP.CJP_69_20
    1. Clarkson TB, Appt SE. Controversies about HRT–lessons from monkey models. Maturitas. 2005;51(1):64–74. doi:10.1016/j.maturitas.2005.02.016
    1. Parhami F, Tintut Y, Ballard A, Fogelman AM, Demer LL. Leptin enhances the calcification of vascular cells: artery wall as a target of leptin. Circ Res. 2001;88(9):954–960. doi:10.1161/hh0901.090975
    1. Yamagishi SI, Edelstein D, Du XL, Kaneda Y, Guzmán M, Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase A. J Biol Chem. 2001;276(27):25096–25100. doi:10.1074/jbc.M007383200
    1. Kim JS, Nah HW, Park SM, et al. Risk factors and stroke mechanisms in atherosclerotic stroke: intracranial compared with extracranial and anterior compared with posterior circulation disease. Stroke. 2012;43(12):3313–3318. doi:10.1161/STROKEAHA.112.658500
    1. Li Y, Cai Y, Zhao M, Sun J. Risk factors between intracranial-extracranial atherosclerosis and anterior-posterior circulation stroke in ischaemic stroke. Neurol Res. 2017;39(1):30–35. doi:10.1080/01616412.2016.1250856
    1. Chaturvedi S, Turan TN, Lynn MJ, et al. Risk factor status and vascular events in patients with symptomatic intracranial stenosis. Neurology. 2007;69(22):2063–2068. doi:10.1212/01.wnl.0000279338.18776.26
    1. Tsivgoulis G, Vadikolias K, Heliopoulos I, et al. Prevalence of symptomatic intracranial atherosclerosis in caucasians: a prospective, multicenter, transcranial Doppler study. J Neuroimaging. 2014;24(1):11–17. doi:10.1111/j.1552-6569.2012.00707.x
    1. Csordas A, Bernhard D. The biology behind the atherothrombotic effects of cigarette smoke. Nat Rev Cardiol. 2013;10(4):219–230. doi:10.1038/nrcardio.2013.8
    1. Sun J, Canton G, Balu N, et al. Blood pressure is a major modifiable risk factor implicated in pathogenesis of intraplaque hemorrhage: an in vivo magnetic resonance imaging study. Arterioscler Thromb Vasc Biol. 2016;36(4):743–749. doi:10.1161/ATVBAHA.115.307043
    1. Selwaness M, van den Bouwhuijsen QJ, Verwoert GC, et al. Blood pressure parameters and carotid intraplaque hemorrhage as measured by magnetic resonance imaging: the Rotterdam study. Hypertension. 2013;61(1):76–81. doi:10.1161/HYPERTENSIONAHA.112.198267
    1. Fassaert LMM, Timmerman N, van Koeverden ID, Pasterkamp G, de Kleijn DPV, de Borst GJ. Preoperative hypertension is associated with atherosclerotic intraplaque hemorrhage in patients undergoing carotid endarterectomy. Atherosclerosis. 2019;290:214–221. doi:10.1016/j.atherosclerosis.2019.09.008
    1. van den Bouwhuijsen QJ, Vernooij MW, Hofman A, Krestin GP, van der Lugt A, Witteman JC. Determinants of magnetic resonance imaging detected carotid plaque components: the Rotterdam study. Eur Heart J. 2012;33(2):221–229. doi:10.1093/eurheartj/ehr227
    1. Moreno PR, Murcia AM, Palacios IF, et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation. 2000;102(18):2180–2184. doi:10.1161/01.CIR.102.18.2180
    1. Paneni F, Beckman JA, Creager MA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J. 2013;34(31):2436–2443. doi:10.1093/eurheartj/eht149
    1. Kim BJ, Hong KS, Cho YJ, et al. Predictors of symptomatic and asymptomatic intracranial atherosclerosis: what is different and why? J Atheroscler Thromb. 2014;21(6):605–617.
    1. Johnsen SH, Mathiesen EB, Fosse E, et al. Elevated high-density lipoprotein cholesterol levels are protective against plaque progression: a follow-up study of 1952 persons with carotid atherosclerosis the tromsø study. Circulation. 2005;112(4):498–504. doi:10.1161/CIRCULATIONAHA.104.522706
    1. Taylor AJ, Burke AP, Farb A, et al. Arterial remodeling in the left coronary system: the role of high-density lipoprotein cholesterol. J Am Coll Cardiol. 1999;34(3):760–767. doi:10.1016/S0735-1097(99)00275-2
    1. Sviridov D, Mukhamedova N, Remaley AT, Chin-Dusting J, Nestel P. Antiatherogenic functionality of high density lipoprotein: how much versus how good. J Atheroscler Thromb. 2008;15(2):52–62. doi:10.5551/jat.E571

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する