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Clinical Article
The correlation between the number and location distribution of cerebral microbleeds and imaging of cerebral small vessel disease
LI Jinze  ZHANG Luojin  FENG Jie  LI Xiaowan  SUN Jingshuang  YANG Benqiang  DUAN Yang 

Cite this article as: LI J Z, ZHANG L J, FENG J, et al. The correlation between the number and location distribution of cerebral microbleeds and imaging of cerebral small vessel disease[J]. Chin J Magn Reson Imaging, 2023, 14(10): 46-52. DOI:10.12015/issn.1674-8034.2023.10.009.


[Abstract] Objective To evaluate the number and location distribution of cerebral microbleeds (CMBs) based on susceptibility weighted imaging (SWI), and analyze the correlation with the severity of cerebral small vessel disease (CSVD).Materials and Methods Three hundred and ninety four patients who diagnosed with CSVD by clinical and imaging features were enrolled in this study. Evaluating the imaging markers of CSVD, including lacunar lacunae (LI), white matter hyperintensities (WMH), CMBs, recent small subcortical infarct (RSSI), perivascular spaces (PVS) and cerebral atrophy. The total CSVD score was calculated to evaluate the severity of CSVD. The Microhemorrhage Anatomical Rating Scale (MARS) were used to evaluate the distribution and severity of CMBs. The correlation between the severity and location distribution of CMBs and the imaging characteristics of CSVD was analyzed.Results There were statistical differences in the severity of CMBs in terms of age, WMH, brain atrophy and the total CSVD score (P=0.005; P<0.001; P=0.005; P<0.001). After adjusting for age, the severity of CMBs was correlated with the total CSVD score and WMH (r=0.441, P<0.001; r=0.380, P<0.001). The location distribution of CMBs was correlated with WMH. The modified Fazekas scores of mixed CMBs group was significantly higher than that of simple lobar type, simple deep type and simple subtentorial type (P=0.011; P=0.034; P=0.023).Conclusions The severity and distribution of CMBs are related to WMH and the severity of CMBs is related to the total CSVD score.
[Keywords] cerebral microbleeds;cerebral small vessel disease;susceptibility-weighted imaging;magnetic resonance imaging;Microbleed Anatomical Rating Scale

LI Jinze1   ZHANG Luojin2   FENG Jie3   LI Xiaowan3   SUN Jingshuang2   YANG Benqiang4   DUAN Yang4*  

1 Jinzhou Medical University General Hospital of Northern Theater Command Postgraduate Training Base, Shenyang 110016, China

2 Dalian Medical University General Hospital of Northern Theater Command Postgraduate Training Base, Shenyang 110016, China

3 China Medical University General Hospital of Northern Theater Command Postgraduate Training Base, Shenyang 110016, China

4 Department of Radiology, General Hospital of Northern Theater Command, Shenyang 110016, China

Corresponding author: DUAN Y, E-mail: duanyang100@126.com

Conflicts of interest   None.

ACKNOWLEDGMENTS 2022 Science and Technology Project of Liaoning Province (No. 2022JH2/101500024); 2020 Science and Technology Project of Shenyang (No. 20-205-4-044).
Received  2023-05-16
Accepted  2023-09-26
DOI: 10.12015/issn.1674-8034.2023.10.009
Cite this article as: LI J Z, ZHANG L J, FENG J, et al. The correlation between the number and location distribution of cerebral microbleeds and imaging of cerebral small vessel disease[J]. Chin J Magn Reson Imaging, 2023, 14(10): 46-52. DOI:10.12015/issn.1674-8034.2023.10.009.

[1]
BEAMAN C, KOZII K, HILAL S, et al. Cerebral microbleeds, cerebral amyloid angiopathy, and their relationships to quantitative markers of neurodegeneration[J/OL]. Neurology, 2022, 98(16): e1605-e1616 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/35228332/. DOI: 10.1212/wnl.0000000000200142.
[2]
WADI L C, GRIGORYAN M M, KIM R C, et al. Mechanisms of cerebral microbleeds[J]. J Neuropathol Exp Neurol, 2020, 42(2): 1093-1099. DOI: 10.1093/jnen/nlaa082.
[3]
GAO Y, LI D, LIN J, et al. Cerebral small vessel disease: Pathological mechanisms and potential therapeutic targets[J/OL]. Front Aging Neurosci, 2022, 14: 961661 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/36034144/. DOI: 10.3389/fnagi.2022.961661.
[4]
NANNONI S, OHLMEIER L, BROWN R B, et al. Cognitive impact of cerebral microbleeds in patients with symptomatic small vessel disease[J]. Int J Stroke, 2022, 17(4): 415-424. DOI: 10.1177/17474930211012837.
[5]
SOUSANIDOU A, TSIPTSIOS D, CHRISTIDI F, et al. Exploring the impact of cerebral microbleeds on stroke management[J]. Neurol Int, 2023, 15(1): 188-224. DOI: 10.3390/neurolint15010014.
[6]
KHALADKAR S M, CHANABASANAVAR V, DHIRAWANI S, et al. Susceptibility weighted imaging: An effective auxiliary sequence that enhances insight into the imaging of stroke[J/OL]. Cureus, 2022, 14(5): e24918 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/35706758/. DOI: 10.7759/cureus.24918.
[7]
GREGOIRE S M, CHAUDHARY U J, BROWN M M, et al. The Microbleed Anatomical Rating Scale (MARS): reliability of a tool to map brain microbleeds[J]. Neurology, 2009, 73(21): 1759-1766. DOI: 10.1212/WNL.0b013e3181c34a7d.
[8]
CHEN X, WANG J, SHAN Y, et al. Cerebral small vessel disease: neuroimaging markers and clinical implication[J]. J Neurol, 2019, 266(10): 2347-2362. DOI: 10.1007/s00415-018-9077-3.
[9]
ZANON ZOTIN M C, SVEIKATA L, Viswanathan A, et al. Cerebral small vessel disease and vascular cognitive impairment: from diagnosis to management[J]. Curr Opin Neurol, 2021, 34(2): 246-257. DOI: 10.1097/wco.0000000000000913.
[10]
PASI M, CHARIDIMOU A, BOULOUIS G, et al. Mixed-location cerebral hemorrhage/microbleeds: Underlying microangiopathy and recurrence risk[J/OL]. Neurology, 2018, 90(2): e119-e126 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/29247070/. DOI: 10.1212/wnl.0000000000004797.
[11]
POELS M M, VERNOOIJ M W, IKRAM M A, et al. Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam scan study[J]. Stroke, 2010, 41(10Suppl): S103-S106. DOI: 10.1161/strokeaha.110.595181.
[12]
GIACOMOZZI S, CASO V, AGNELLI G, et al. Lacunar stroke syndromes as predictors of lacunar and non-lacunar infarcts on neuroimaging: a hospital-based study[J]. Intern Emerg Med, 2020, 15(3): 429-436. DOI: 10.1007/s11739-019-02193-2.
[13]
ZEESTRATEN E, BENJAMIN P, LAMBERT C, et al. Application of diffusion tensor imaging parameters to detect change in longitudinal studies in cerebral small vessel disease[J/OL]. PLoS One, 2016, 11(1): e0147836 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/26808982/. DOI: 101371/journalpone0147836.
[14]
GREENBERG S M, VERNOOIJ M W, CORDONNIER C, et al. Cerebral microbleeds: a guide to detection and interpretation[J]. Lancet Neurol, 2009, 8(2): 165-174. DOI: 10.1016/S1474-4422(09)70013-4.
[15]
WARDLAW J M, SMITH E E, BIESSELS G J, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration[J]. Lancet Neurol, 2013, 12(8): 822-838. DOI: 10.1016/s1474-4422(13)70124-8.
[16]
DOUBAL F N, MACLULLICH A M, FERGUSON K J, et al. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease[J]. Stroke, 2010, 41(3): 450-454. DOI: 10.1161/STROKEAHA.109.564914.
[17]
STAALS J, MAKIN S D, DOUBAL F N, et al. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden[J]. Neurology, 2014, 83(14): 1228-1234. DOI: 10.1212/wnl.0000000000000837.
[18]
GYANWALI B, LUI B, TAN C S, et al. Cerebral microbleeds and white matter hyperintensities are associated with cognitive decline in an asian memory clinic study[J]. Curr Alzheimer Res, 2021, 18(5): 399-413. DOI: 10.2174/1567205018666210820125543.
[19]
NAKA H, NOMURA E, WAKABAYASHI S, et al. Frequency of asymptomatic microbleeds on T2*-weighted MR images of patients with recurrent stroke: association with combination of stroke subtypes and leukoaraiosis[J]. AJNR Am J Neuroradiol, 2004, 25(5): 714-719.
[20]
BALESTRIERI A, LUCATELLI P, SURI H S, et al. Volume of white matter hyperintensities, and cerebral micro-bleeds[J/OL]. J Stroke Cerebrovasc Dis, 2021, 30(8): 105905 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/34107418/. DOI: 10.1016/j.jstrokecerebrovasdis.2021.105905.
[21]
HAN J, GAO P, LIN Y, et al. Three-tesla magnetic resonance imaging study of cerebral microbleeds in patients with ischemic stroke[J]. Neurol Res, 2009, 31(9): 900-903. DOI: 10.1179/174313209x382485.
[22]
YAMADA S, SAIKI M, SATOW T, et al. Periventricular and deep white matter leukoaraiosis have a closer association with cerebral microbleeds than age[J]. Eur J Neurol, 2012, 19(1): 98-104. DOI: 10.1111/j.1468-1331.2011.03451.x.
[23]
KIM D E, BAE H J, LEE S H, et al. Gradient echo magnetic resonance imaging in the prediction of hemorrhagic vs ischemic stroke: a need for the consideration of the extent of leukoariosis[J]. Arch Neurol, 2002, 59(3): 425-429. DOI: 10.1001/archneur.59.3.425.
[24]
YATES P A, VILLEMAGNE V L, ELLIS K A, et al. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations[J/OL]. Front Neurol, 2014, 4: 205 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/24432010/. DOI: 10.3389/fneur.2013.00205.
[25]
AN S J, KIM T J, YOON B W. Epidemiology, risk factors, and clinical features of intracerebral hemorrhage: An update[J]. J Stroke, 2017, 19(1): 3-10. DOI: 10.5853/jos.2016.00864.
[26]
ARIMA H, TZOURIO C, ANDERSON C, et al. Effects of perindopril-based lowering of blood pressure on intracerebral hemorrhage related to amyloid angiopathy: the PROGRESS trial[J]. Stroke, 2010, 41(2): 394-396. DOI: 10.1161/STROKEAHA.109.563932.
[27]
ZHU R, LI Y, CHEN L, et al. Total burden of cerebral small vessel disease on MRI may predict cognitive impairment in Parkinson's disease[J/OL]. J Clin Med, 2022, 11(18): 5381 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/36143028/. DOI: 10.3390/jcm11185381.
[28]
WANG M, LI Y, SONG Y, et al. Association of total cerebral small vessel disease burden with the cavitation of recent small subcortical infarcts[J]. Acta Radiol, 2023, 64(1): 295-300. DOI: 10.1177/02841851211066583.
[29]
WEI C, LIU J, LI J, et al. A non-linear association between total small vessel disease score and hemorrhagic transformation after ischemic stroke with atrial fibrillation and/or rheumatic heart disease[J/OL]. Front Neurol, 2019, 10: 769 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/31396145/. DOI: 10.3389/fneur.2019.00769.
[30]
SCHWARZ G, BANERJEE G, HOSTETTLER I C, et al. Magnetic resonance imaging-based scores of small vessel diseases: Associations with intracerebral haemorrhage location[J/OL]. J Neurol Sci, 2022, 434: 120165 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/35121207/. DOI: 10.1016/j.jns.2022.120165.
[31]
WILSON D, AMBLER G, LEE K J, et al. Cerebral microbleeds and stroke risk after ischaemic stroke or transient ischaemic attack: a pooled analysis of individual patient data from cohort studies[J]. Lancet Neurol, 2019, 18(7): 653-665. DOI: 10.1016/s1474-4422(19)30197-8.
[32]
XIA Y, WANG Y, YANG L, et al. Incident cerebral microbleeds and hypertension defined by the 2017 ACC/AHA Guidelines[J/OL]. Ann Transl Med, 2021, 9(4): 314 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/33708941/. DOI: 10.21037/atm-20-5142.
[33]
WANG Z J, ZHAO R, HU X, et al. Higher cerebral small vessel disease burden in patients with small intracerebral hemorrhage[J/OL]. Front Neurosci, 2022, 16: 888198 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/35645707/. DOI: 10.3389/fnins.2022.888198.
[34]
PARK K I, JUNG K H, LEE E J, et al. Classification of white matter lesions and characteristics of small vessel disease markers[J]. Eur Radiol, 2023, 33(2): 1143-1151. DOI: 10.1007/s00330-022-09070-1.
[35]
XU M, CHENG Y, ZHANG S, et al. Higher cerebral small vessel disease burden is associated with smaller hematoma volume in mixed-location intracerebral hemorrhage[J/OL]. Microcirculation (New York, NY: 1994), 2021, 28(6): e12705 [2023-05-15]. https://pubmed.ncbi.nlm.nih.gov/33977609/. DOI: 10.1111/micc.12705.
[36]
WARDLAW J M. What causes lacunar stroke?[J]. J Neurol Neurosurg Psychiatry, 2005, 76(5): 617-619. DOI: 10.1136/jnnp.2004.039982.

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