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Current Neurovascular Research

Editor-in-Chief

ISSN (Print): 1567-2026
ISSN (Online): 1875-5739

Research Article

Diffusion-weighted Imaging Detection of Acute Ischemia Brain Lesions in Spontaneous Intracerebral Hemorrhage Associated with White Matter Hyperintensities, Enlarged Perivascular Spaces and Diabetes Mellitus

Author(s): Yutong Hou, Wei Qin, Shuna Yang, Yue Li, Lei Yang and Wenli Hu*

Volume 20, Issue 5, 2023

Published on: 26 January, 2024

Page: [544 - 552] Pages: 9

DOI: 10.2174/0115672026283323240108052711

Price: $65

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Abstract

Objective: Diffusion-weighted imaging (DWI) is commonly detected after spontaneous intracerebral hemorrhage (sICH) and is associated with poor functional outcomes. However, the etiology and significance of DWI lesions remain unclear. Thus, our study aimed to explore the prevalence and risk factors of acute ischemic lesions in sICH and discussed the possible mechanisms.

Methods: We conducted a retrospective review of a consecutive cohort of 408 patients from June 2013 to October 2019 with sICH, who had brain computed tomography (CT) and magnetic resonance imaging (MRI) within 14 days of symptoms onset. Acute ischemic lesions were assessed on MRI using DWI lesions. We compared the clinical and imaging characteristics of patients with and without DWI lesions. The data were analyzed by univariate and multivariate logistic regression.

Results: Among the enrolled 408 patients, the mean age was 56.8 ± 14.5 years, 68 (16.7%) of them had been diagnosed with diabetes mellitus (DM). DWI lesions were observed in 89 (21.8%) patients, and most of them had a history of lacunar infarctions, which were located in cortical or subcortical. In multivariate logistic regression analysis, DM (odds ratio (OR) 3.962, p <0.001), severe deep white matter hypertensities (DWMH) (OR 2.463, p =0.001) and severe centrum semiovale enlarged perivascular spaces (CSO-EPVS) (OR 2.679, p =0.001) were independently associated with the presence of DWI lesions.

Conclusion: In our cohort, we found DM, severe DWMH and severe CSO-EPVS were the independent risk factors in sICH patients with DWI lesions.

Keywords: Spontaneous intracerebral hemorrhage, diffusion-weighted imaging lesion, white matter hyperintensities, enlarged perivascular spaces, diabetes mellitus, non-traumatic bleeding.

[1]
de Oliveira Manoel AL, Goffi A, Zampieri FG, Turkel-Parrella D, Duggal A, Marotta TR. The critical care management of spontaneous intracranial hemorrhage: A contemporary review. Crit Care 2016; 20: 272.
[http://dx.doi.org/10.1186/s13054-016-1432-0]
[2]
van Asch CJJ, Luitse MJA, Rinkel GJE, van der Tweel I, Algra A, Klijn CJM. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: A systematic review and meta-analysis. Lancet Neurol 2010; 9(2): 167-76.
[http://dx.doi.org/10.1016/S1474-4422(09)70340-0] [PMID: 20056489]
[3]
Tsai CF, Thomas B, Sudlow CLM. Epidemiology of stroke and its subtypes in Chinese vs white populations. Neurology 2013; 81(3): 264-72.
[http://dx.doi.org/10.1212/WNL.0b013e31829bfde3] [PMID: 23858408]
[4]
Garg RK, Liebling SM, Maas MB, Nemeth AJ, Russell EJ, Naidech AM. Blood pressure reduction, decreased diffusion on MRI, and outcomes after intracerebral hemorrhage. Stroke 2012; 43(1): 67-71.
[http://dx.doi.org/10.1161/STROKEAHA.111.629493] [PMID: 21980211]
[5]
Kang DW, Han MK, Kim HJ, et al. New ischemic lesions coexisting with acute intracerebral hemorrhage. Neurology 2012; 79(9): 848-55.
[http://dx.doi.org/10.1212/WNL.0b013e3182648a79] [PMID: 22843271]
[6]
Gioia LC, Kate M, Choi V, et al. Ischemia in intracerebral hemorrhage is associated with leukoaraiosis and hematoma volume, not blood pressure reduction. Stroke 2015; 46(6): 1541-7.
[http://dx.doi.org/10.1161/STROKEAHA.114.008304] [PMID: 25922504]
[7]
Wu B, Yao X, Lei C, Liu M, Selim MH. Enlarged perivascular spaces and small diffusion-weighted lesions in intracerebral hemorrhage. Neurology 2015; 85(23): 2045-52.
[http://dx.doi.org/10.1212/WNL.0000000000002169] [PMID: 26546632]
[8]
Kidwell CS, Rosand J, Norato G, et al. Ischemic lesions, blood pressure dysregulation, and poor outcomes in intracerebral hemorrhage. Neurology 2017; 88(8): 782-8.
[http://dx.doi.org/10.1212/WNL.0000000000003630] [PMID: 28122903]
[9]
Xu XH, Gao T, Zhang WJ, Tong LS, Gao F. Remote diffusion-weighted imaging lesions in intracerebral hemorrhage: Characteristics, mechanisms, outcomes, and therapeutic implications. Front Neurol 2017; 8: 678.
[http://dx.doi.org/10.3389/fneur.2017.00678]
[10]
Boulanger M, Schneckenburger R, Join-Lambert C, Werring D, Wilson D, Hodel J. Diffusion-weighted imaging hyperintensities in subtypes of acute intracerebral hemorrhage. Stroke 2018; 50(1): 135-42.
[http://dx.doi.org/10.1161/STROKEAHA.118.021407] [PMID: 30580720]
[11]
Xu XH, Ye XH, Cai JS, Gao T, Zhao GH, Zhang WJ. Association of renal dysfunction with remote diffusion-weighted imaging lesions and total burden of cerebral small vessel disease in patients with primary intracerebral hemorrhage. Front Aging Neurosci 2018; 10: 171.
[http://dx.doi.org/10.3389/fnagi.2018.00171]
[12]
Ye XH, Gao T, Xu XH, Cai JS, Li JW, Liu KM. Factors associated with remote diffusion-weighted imaging lesions in spontaneous intracerebral hemorrhage. Front Neurol 2018; 9: 209.
[http://dx.doi.org/10.3389/fneur.2018.00209]
[13]
Revel-Mouroz P, Viguier A, Cazzola V, et al. Acute ischaemic lesions are associated with cortical superficial siderosis in spontaneous intracerebral hemorrhage. Eur J Neurol 2019; 26(4): 660-6.
[http://dx.doi.org/10.1111/ene.13874] [PMID: 30561110]
[14]
Wang YW, Zhang GM. New silent cerebral infarction in patients with acute non-cerebral amyloid angiopathy intracerebral hemorrhage as a predictor of recurrent cerebrovascular events. Med Sci Monit 2019; 25: 418-26.
[http://dx.doi.org/10.12659/MSM.914423] [PMID: 30640895]
[15]
Garg RK, Khan J, Dawe RJ, et al. The influence of diffusion weighted imaging lesions on outcomes in patients with acute spontaneous intracerebral hemorrhage. Neurocrit Care 2020; 33(2): 552-64.
[http://dx.doi.org/10.1007/s12028-020-00933-3] [PMID: 32072457]
[16]
Murthy SB, Cho SM, Gupta A, Shoamanesh A, Navi BB, Avadhani R. A pooled analysis of diffusion-weighted imaging lesions in patients with acute intracerebral hemorrhage. JAMA Neurol 2020; 77(11): 1390-7.
[http://dx.doi.org/10.1001/jamaneurol.2020.2349]
[17]
Kimberly WT, Gilson A, Rost NS, Rosand J, Viswanathan A, Smith EE. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology 2009; 72(14): 1230-5.
[http://dx.doi.org/10.1212/01.wnl.0000345666.83318.03]
[18]
Prabhakaran S, Gupta R, Ouyang B, et al. Acute brain infarcts after spontaneous intracerebral hemorrhage: A diffusion-weighted imaging study. Stroke 2010; 41(1): 89-94.
[http://dx.doi.org/10.1161/STROKEAHA.109.566257] [PMID: 19892994]
[19]
Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: A critical review. Stroke 2012; 43(8): 2258-63.
[http://dx.doi.org/10.1161/STROKEAHA.112.655910] [PMID: 22821611]
[20]
Beitzke M, Enzinger C, Pichler A, Wunsch G, Fazekas F. Acute diffusion-weighted imaging lesions in cerebral amyloid angiopathy-related convexal subarachnoid hemorrhage. J Cereb Blood Flow Metab 2018; 38(2): 225-9.
[http://dx.doi.org/10.1177/0271678X17744736]
[21]
Gregoire SM, Charidimou A, Gadapa N, et al. Acute ischaemic brain lesions in intracerebral haemorrhage: Multicentre cross-sectional magnetic resonance imaging study. Brain 2011; 134(8): 2376-86.
[http://dx.doi.org/10.1093/brain/awr172] [PMID: 21841203]
[22]
Menon RS, Burgess RE, Wing JJ, Gibbons MC, Shara NM, Fernandez S. Predictors of highly prevalent brain ischemia in intracerebral hemorrhage. Ann Neurol 2012; 71(2): 199-205.
[http://dx.doi.org/10.1002/ana.22668]
[23]
Li X, Zhang B, Lou M. The relation between acute intracerebral hemorrhage and diffusion-weighted imaging lesions: A meta-analysis. J Thromb Thrombolysis 2021; 52(3): 962-70.
[http://dx.doi.org/10.1007/s11239-021-02430-6] [PMID: 33783661]
[24]
Won SY, Zagorcic A, Dubinski D, et al. Excellent accuracy of ABC/2 volume formula compared to computer-assisted volumetric analysis of subdural hematomas. PLoS One 2018; 13(6)e0199809
[http://dx.doi.org/10.1371/journal.pone.0199809] [PMID: 29944717]
[25]
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 1987; 149(2): 351-6.
[http://dx.doi.org/10.2214/ajr.149.2.351] [PMID: 3496763]
[26]
Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12(8): 822-38.
[http://dx.doi.org/10.1016/S1474-4422(13)70124-8] [PMID: 23867200]
[27]
Boulanger M, Poon MT, Wild SH, Al-Shahi SR. Association between diabetes mellitus and the occurrence and outcome of intracerebral hemorrhage. Neurology 2016; 87(9): 870-8.
[http://dx.doi.org/10.1212/WNL.0000000000003031]
[28]
Liebkind R, Gordin D, Strbian D, et al. Diabetes and intracerebral hemorrhage: Baseline characteristics and mortality. Eur J Neurol 2018; 25(6): 825-32.
[http://dx.doi.org/10.1111/ene.13603] [PMID: 29443444]
[29]
Ye X, Cai X, Nie D, et al. Stress-induced hyperglycemia and remote diffusion-weighted imaging lesions in primary intracerebral hemorrhage. Neurocrit Care 2020; 32(2): 427-36.
[http://dx.doi.org/10.1007/s12028-019-00747-y] [PMID: 31313140]
[30]
Garg R, Ouyang B, Khan J, Panos N, Da Silva I, Hall D. Association of longitudinal glycemia with diffusion weighted imaging lesions in spontaneous intracerebral hemorrhage. J Stroke Cerebrovasc Dis 2021; 30(3)105554
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.105554]
[31]
Won SJ, Tang XN, Suh SW, Yenari MA, Swanson RA. Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by Increasing superoxide production. Ann Neurol 2011; 70(4): 583-90.
[http://dx.doi.org/10.1002/ana.22538] [PMID: 22002675]
[32]
Chiu CD, Chen CCV, Shen CC, et al. Hyperglycemia exacerbates intracerebral hemorrhage via the downregulation of aquaporin-4: Temporal assessment with magnetic resonance imaging. Stroke 2013; 44(6): 1682-9.
[http://dx.doi.org/10.1161/STROKEAHA.113.675983] [PMID: 23592763]
[33]
Parsons MW, Barber PA, Desmond PM, et al. Acute hyperglycemia adversely affects stroke outcome: A magnetic resonance imaging and spectroscopy study. Ann Neurol 2002; 52(1): 20-8.
[http://dx.doi.org/10.1002/ana.10241] [PMID: 12112043]
[34]
Arboix A, Rivas A, García-Eroles L, de Marcos L, Massons J, Oliveres M. Cerebral infarction in diabetes: Clinical pattern, stroke subtypes, and predictors of in-hospital mortality. BMC Neurol 2005; 5(1): 9.
[http://dx.doi.org/10.1186/1471-2377-5-9] [PMID: 15833108]
[35]
King GL, Park K, Li Q. Selective insulin resistance and the development of cardiovascular diseases in diabetes: The 2015 edwin bierman award lecture. Diabetes 2016; 65(6): 1462-71.
[http://dx.doi.org/10.2337/db16-0152] [PMID: 27222390]
[36]
Meissner A. Hypertension and the brain: A risk factor for more than heart disease. Cerebrovasc Dis 2016; 42(3-4): 255-62.
[http://dx.doi.org/10.1159/000446082] [PMID: 27173592]
[37]
Umemura T, Kawamura T, Hotta N. Pathogenesis and neuroimaging of cerebral large and small vessel disease in type 2 diabetes: A possible link between cerebral and retinal microvascular abnormalities. J Diabetes Investig 2017; 8(2): 134-48.
[http://dx.doi.org/10.1111/jdi.12545] [PMID: 27239779]
[38]
Smith EE. Leukoaraiosis and stroke. Stroke 2010; 41(S10): S139-43.
[http://dx.doi.org/10.1161/STROKEAHA.110.596056]
[39]
Promjunyakul N, Lahna D, Kaye JA, Dodge HH, Erten-Lyons D, Rooney WD. Characterizing the white matter hyperintensity penumbra with cerebral blood flow measures. Neuroimage Clin 2015; 8: 224-9.
[http://dx.doi.org/10.1016/j.nicl.2015.04.012]
[40]
Bahrani AA, Powell DK, Yu G, Johnson ES, Jicha GA, Smith CD. White matter hyperintensity associations with cerebral blood flow in elderly subjects stratified by cerebrovascular risk. J Stroke Cerebrovasc Dis 2017; 26(4): 779-86.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.10.017]
[41]
Georgakis MK, Duering M, Wardlaw JM, Dichgans M. WMH and long-term outcomes in ischemic stroke. Neurology 2019; 92(12): e1298-308.
[http://dx.doi.org/10.1212/WNL.0000000000007142] [PMID: 30770431]
[42]
Manschot SM, Brands AMA, van der Grond J, et al. Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 2006; 55(4): 1106-13.
[http://dx.doi.org/10.2337/diabetes.55.04.06.db05-1323] [PMID: 16567535]
[43]
Braffman BH, Zimmerman RA, Trojanowski JQ, et al. Pathologic correlation with gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces. AJR Am J Roentgenol 1988; 151(3): 551-8.
[http://dx.doi.org/10.2214/ajr.151.3.551] [PMID: 3261517]
[44]
Zhu YC, Tzourio C, Soumaré A, Mazoyer B, Dufouil C, Chabriat H. Severity of dilated Virchow-Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: A population-based study. Stroke 2010; 41(11): 2483-90.
[http://dx.doi.org/10.1161/STROKEAHA.110.591586] [PMID: 20864661]
[45]
Charidimou A, Meegahage R, Fox Z, Peeters A, Vandermeeren Y, Laloux P. Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: A multicentre MRI cohort study. J Neurol Neurosurg Psychiatry 2013; 84(6): 624-9.
[http://dx.doi.org/10.1136/jnnp-2012-304434]
[46]
Roher AE, Kuo YM, Esh C, Knebel C, Weiss N, Kalback W. Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer’s disease. Mol Med 2003; 9(3-4): 112-22.
[http://dx.doi.org/10.1007/BF03402043]
[47]
Mikami T, Tamada T, Suzuki H, Ukai R, Wanibuchi M, Mikuni N. Influence of hemodynamics on enlarged perivascular spaces in atherosclerotic large vessel disease. Neurol Res 2018; 40(12): 1021-7.
[http://dx.doi.org/10.1080/01616412.2018.1509827] [PMID: 30156508]
[48]
Charidimou A, Boulouis G, Haley K, Auriel E, van Etten ES, Fotiadis P. White matter hyperintensity patterns in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology 2016; 86(6): 505-11.
[http://dx.doi.org/10.1212/WNL.0000000000002362]
[49]
Riba-Llena I, Jiménez-Balado J, Castañé X, et al. Arterial stiffness is associated with basal ganglia enlarged perivascular spaces and cerebral small vessel disease load. Stroke 2018; 49(5): 1279-81.
[http://dx.doi.org/10.1161/STROKEAHA.118.020163] [PMID: 29669870]
[50]
Arboix A, Font A, Garro C, Garcia-Eroles L, Comes E, Massons J. Recurrent lacunar infarction following a previous lacunar stroke: A clinical study of 122 patients. J Neurol Neurosurg Psychiatry 2007; 78(12): 1392-4.
[http://dx.doi.org/10.1136/jnnp.2007.119776]

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