Progress on the Relationship between Albuminuria and Ischemic Stroke

doi:10.3969/j.issn.1673-5765.2021.06.019

Abstract

Abstract: Ischemic stroke is one of the most leading diseases with high morbidity and disability worldwide. Extra-and-intracranial large artery atherosclerosis is the primary cause of ischemic stroke. Previous studies have suggested that microalbuminuria is not only an important marker of generalized endothelial dysfunction, but also an early marker of atherosclerosis. More recently, many studies have found that albuminuria is closely linked to the pathogenesis, progression and prognosis of ischemic stroke. This article aimed to review the research advances in the relationship between albuminuria and ischemic stroke.

Key words: Albuminuria; Ischemic stroke; Pathogenesis; Prognosis

摘要： 缺血性卒中是世界范围内病残率最高的疾病之一。颈部或颅底大动脉粥样硬化是缺血性卒中的首要病因。既往研究提示，微量白蛋白尿不仅是全身血管内皮功能紊乱的重要标志，还可能是动脉粥样硬化发生的早期标志。近年来研究发现，白蛋白尿与缺血性卒中的发生、发展及预后均存在密切联系。本文旨在对白蛋白尿与缺血性卒中关系的研究进展进行综述。

关键词: 白蛋白尿; 缺血性卒中; 发病机制; 预后

CHEN Shuang-Shuang, ZHOU Yi-Lun. Progress on the Relationship between Albuminuria and Ischemic Stroke[J]. Chinese Journal of Stroke, 2021, 16(06): 625-630.

陈霜霜, 周亦伦. 白蛋白尿与缺血性卒中关系的研究进展[J]. 中国卒中杂志, 2021, 16(06): 625-630.

References

[1] WANG W Z，JIANG B，SUN H X，et al. Prevalence，
incidence，and mortality of stroke in China：results
from a nationwide population-based survey of
480 687 adults[J]. Circulation，2017，135（8）：759-
771.
[2] MYKKÄNEN L，ZACCARO D J，O'LEARY D H，
et al. Microalbuminuria and carotid artery intimamedia
thickness in nondiabetic and NIDDM subjects.
The Insulin Resistance Atherosclerosis Study（IRAS）
[J]. Stroke，1997，28（9）：1710-1716.
[3] VIBERTI G C，HILL R D，JARRETT R J，et
al. Microalbuminuria as a predictor of clinical
nephropathy in insulin-dependent diabetes
mellitus[J]. Lancet，1982，1（8287）：1430-1432.
[4] ZHANG Y H，GAO Y，MAO X，et al. Assessment
of carotid atherosclerosis in type 2 diabetes
mellitus patients with microalbuminuria by
high-frequency ultrasonography[J/OL]. Int J
Endocrinol，2013：819584[2020-11-12]. https：//doi.
org/10.1155/2013/819584.
[5] KONG X L，JIA X Y，WEI Y，et al. Association
between microalbuminuria and subclinical
atherosclerosis evaluated by carotid artery intimamedia
in elderly patients with normal renal
function[J/OL]. BMC Nephrol，2012，13：37[2020-
11-12]. https：//doi.org/10.1186/1471-2369-13-37.
[6] KIM J J，HWANG B H，CHOI I J，et al. A
prospective two-center study on the associations
between microalbuminuria，coronary atherosclerosis
and long-term clinical outcome in asymptomatic
patients with type 2 diabetes mellitus：evaluation
by coronary CT angiography[J]. Int J Cardiovasc
Imaging，2015，31（1）：193-203.
[7] MA H，LIN H，HOFMAN A，et al. Low-grade
albuminuria is associated with carotid atherosclerosis
in normotensive and euglycemic Chinese middleaged
and elderly adults：the Shanghai Changfeng
Study[J]. Atherosclerosis，2013，228（1）：237-242.
[8] YUYUN M F，KHAW K T，LUBEN R，et al.
Microalbuminuria and stroke in a British population：
the European Prospective Investigation into Cancer

in Norfolk（EPIC-Norfolk）population stu

[9] LEE M，SAVER J L，CHANG K H，et al. Impact
of microalbuminuria on incident stroke：a metaanalysis[
J]. Stroke，2010，41（11）：2625-2631.
[10] KELLY D M，ROTHWELL P M. Proteinuria as an
independent predictor of stroke：systematic review
and meta-analysis[J]. Int J Stroke，2020，15（1）：29-
38.
[11] HORN J W，ROMUNDSTAD S，ELLEKJAER
H，et al. Low grade albuminuria as a risk factor for
subtypes of stroke-the HUNT Study in Norway[J].
BMC Neurol，2020，20（1）：170.
[12] DECKERT T，FELDT-RASMUSSEN B，BORCHJOHNSEN
K，et al. Albuminuria reflects widespread
vascular damage. The steno hypothesis[J].
Diabetologia，1989，32（4）：219-226.
[13] GIMBRONE M J，GARCÍA-CARDEÑA G.
Endothelial cell dysfunction and the pathobiology of
atherosclerosis[J]. Circ Res，2016，118（4）：620-636.
[14] ITO S，NAGASAWA T，ABE M，et al. Strain vessel
hypothesis：a viewpoint for linkage of albuminuria
and cerebro-cardiovascular risk[J]. Hypertens Res，
2009，32（2）：115-121.
[15] NAGASAWA T，MORI T，OHSAKI Y，et al.
Albuminuria indicates the pressure-associated injury
of juxtamedullary nephrons and cerebral strain
vessels in spontaneously hypertensive stroke-prone
rats[J]. Hypertens Res，2012，35（10）：1024-1031.
[16] LASTILLA M. Lacunar infarct[J]. Clin Exp
Hypertens，2006，28（3/4）：205-215.
[17] SENERS P，TURC G，OPPENHEIM C，et al.
Incidence，causes and predictors of neurological
deterioration occurring within 24 h following
acute ischaemic stroke：a systematic review with
pathophysiological implications[J]. J Neurol
Neurosurg Psychiatry，2015，86（1）：87-94.
[18] KANAMARU T，SUDA S，MURAGA K，et
al. Albuminuria predicts early neurological
deterioration in patients with acute ischemic stroke[J/
OL]. J Neurol Sci，2017，372：417-420[2020-11-12].
https：//doi.org/10.1016/j.jns.2016.11.007.
[19] 程曦，刘康，钱云，等. 尿微量白蛋白/尿肌酐比率与
急性缺血性脑卒中早期神经功能恶化的相关性分析
[J]. 临床神经病学杂志，2017，30（6）：410-414.
[20] RODRÍGUEZ-YÁÑEZ M，CASTELLANOS M，
BLANCO M，et al. Micro- and macroalbuminuria
predict hemorrhagic transformation in acute
ischemic stroke[J]. Neurology，2006，67（7）：1172-
1177.
[21] CHO B H，KIM J T，CHANG J，et al. Prediction
of hemorrhagic transformation in acute ischaemic
stroke by micro- and macroalbuminuria after
intravenous thrombolysis[J]. Eur J Neurol，2013，20
（8）：1145-1152.
[22] NORWOOD M G，SAYERS R D. Urinary albumin：
creatinine ratio（ACR）and the prediction of
postoperative complications after abdominal aortic
aneurysm repair[J]. Eur J Vasc Endovasc Surg，2005，
30（4）：353-358.
[23] SZCZUDLIK A，TURAJ W，SLOWIK A，et al.
Microalbuminuria and hyperthermia independently
predict long-term mortality in acute ischemic stroke
patients[J]. Acta Neurol Scand，2003，107（2）：96-
101.
[24] SLOWIK A，TURAJ W，ISKRA T，et al.
Microalbuminuria in nondiabetic patients with acute
ischemic stroke：prevalence，clinical correlates，and
prognostic significance[J]. Cerebrovasc Dis，2002，
14（1）：15-21.
[25] SANDER D，WEIMAR C，BRAMLAGE P，et
al. Microalbuminuria indicates long-term vascular
risk in patients after acute stroke undergoing inpatient
rehabilitation[J/OL]. BMC Neurol，2012，12：
102[2020-11-12]. https：//doi.org/10.1186/1471-2377-
12-102.
[26] WARNOCK D G，MUNTNER P，MCCULLOUGH
P A，et al. Kidney function，albuminuria，and
all-cause mortality in the REGARDS（Reasons
for Geographic and Racial Differences in Stroke）
study[J]. Am J Kidney Dis，2010，56（5）：861-871.
[27] BROUWERS F P，ASSELBERGS F W，HILLEGE
H L，et al. Long-term effects of fosinopril and
pravastatin on cardiovascular events in subjects
with microalbuminuria：ten years of follow-up of
Prevention of Renal and Vascular End-stage Disease
Intervention Trial（PREVEND IT）[J]. Am Heart J，
2011，161（6）：1171-1178.
[28] WATANABE Y，SUDA S，KANAMARU T，et al.
High urinary albumin/creatinine ratio at admission
predicts poor functional outcome in patients with
acute ischaemic stroke[J]. Nephrology（Carlton），
2017，22（3）：199-204.
[29] LEE S，LEE D. Relationship between kidney
dysfunction and ischemic stroke outcomes：
albuminuria，but not estimated glomerular filtration
rate，is associated with the risk of further vascular
events and mortality after stroke[J/OL]. PLoS One，
2016，11（5）：e01559395[2020-11-12]. https：//doi.
org/10.1371/journal.pone.0155939.
[30] JOOSTEN H，IZAKS G J，SLAETS J P，et al.
Association of cognitive function with albuminuria
and eGFR in the general population[J]. Clin J Am
Soc Nephrol，2011，6（6）：1400-1409.
[31] CHO E B，SHIN H Y，PARK S E，et al. Albuminuria，
cerebrovascular disease and cortical atrophy：among
cognitively normal elderly individuals[J/OL]. Sci Rep，
2016，6：20692[2020-11-12]. https：//doi.org/10.1038/
srep20692.
[32] YOKOTA C，MINEMATSU K，ITO A，et al.
Albuminuria，but not metabolic syndrome，is a
significant predictor of stroke recurrence in ischemic
stroke[J]. J Neurol Sci，2009，277（1/2）：50-53.
[33] ELYAS S，SHORE A C，KINGWELL H，et al.
Microalbuminuria could improve risk stratification
in patients with TIA and minor stroke[J]. Ann Clin
Transl Neurol，2016，3（9）：678-683.