Effect of cerebral small vessel disease on cognitive impairment in Parkinson's disease

Ascherio A, Schwarzschild MA (2016) The epidemiology of Parkinson’s disease: risk factors and prevention. Lancet Neurol 15(12):1257–1272. https://doi.org/10.1016/s1474-4422(16)30230-7 Toodayan N (2018) James Parkinson’s Essay on the shaking palsy, 1817–2017. Med J Aust 208(9):384–386. https://doi.org/10.5694/mja17.01085 Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet (London, England) 386(9996):896–912. https://doi.org/10.1016/s0140-6736(14)61393-3 Svenningsson P, Westman E, Ballard C, Aarsland D (2012) Cognitive impairment in patients with Parkinson’s disease: diagnosis, biomarkers, and treatment. Lancet Neurol 11(8):697–707. https://doi.org/10.1016/s1474-4422(12)70152-7 Shibata K, Sugiura M, Nishimura Y, Sakura H (2019) The effect of small vessel disease on motor and cognitive function in Parkinson’s disease. Clin Neurol Neurosurg 182:58–62. https://doi.org/10.1016/j.clineuro.2019.04.029 Foo H, Mak E, Yong TT, Wen MC, Chander RJ, Au WL, Tan L, Kandiah N (2016) Progression of small vessel disease correlates with cortical thinning in Parkinson’s disease. Parkinsonism Relat Disord 31:34–40. https://doi.org/10.1016/j.parkreldis.2016.06.019 Chen H, Wan H, Zhang M, Liu G, Wang X, Wang Z, Ma H, Pan Y, Feng T, Wang Y (2021) Cerebral small vessel disease may worsen motor function, cognition, and mood in Parkinson’s disease. Parkinsonism Relat Disord 83:86–92. https://doi.org/10.1016/j.parkreldis.2020.12.025 Dey AK, Stamenova V, Bacopulos A, Jeyakumar N, Turner GR, Black SE, Levine B (2019) Cognitive heterogeneity among community-dwelling older adults with cerebral small vessel disease. Neurobiol Aging 77:183–193. https://doi.org/10.1016/j.neurobiolaging.2018.12.011 Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12(8):822–838. https://doi.org/10.1016/s1474-4422(13)70124-8 Jokinen H, Koikkalainen J, Laakso HM, Melkas S, Nieminen T, Brander A, Korvenoja A, Rueckert D, Barkhof F, Scheltens P, Schmidt R, Fazekas F, Madureira S, Verdelho A, Wallin A, Wahlund LO, Waldemar G, Chabriat H, Hennerici M, O’Brien J, Inzitari D, Lötjönen J, Pantoni L, Erkinjuntti T (2020) Global burden of small vessel disease-related brain changes on MRI predicts cognitive and functional decline. Stroke 51(1):170–178. https://doi.org/10.1161/strokeaha.119.026170 Shen Y, Dong ZF, Pan PL, Xu G, Huang JY, Liu CF (2019) Association of homocysteine, folate, and white matter hyperintensities in Parkinson’s patients with different motor phenotypes. Neurol Sci 40(9):1855–1863. https://doi.org/10.1007/s10072-019-03906-3 Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–1601. https://doi.org/10.1002/mds.26424 Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184. https://doi.org/10.1136/jnnp.55.3.181 Zijlmans JC, Daniel SE, Hughes AJ, Révész T, Lees AJ (2004) Clinicopathological investigation of vascular parkinsonism, including clinical criteria for diagnosis. Mov Disord 19(6):630–640. https://doi.org/10.1002/mds.20083 Weidauer S, Nichtweiss M, Hattingen E (2014) Differential diagnosis of white matter lesions: nonvascular causes-Part II. Clin Neuroradiol 24(2):93–110. https://doi.org/10.1007/s00062-013-0267-1 Glei DA, Weinstein M (2019) Drug and alcohol abuse: the role of economic insecurity. Am J Health Behav 43(4):838–853. https://doi.org/10.5993/ajhb.43.4.16 Liu K, Ding Y, Lu X, Wang Z (2021) Trends and socioeconomic factors in smoking and alcohol consumption among Chinese people: evidence from the 2008–2018 National Health Service Surveys in Jiangsu Province. Arch Public Health Archives belges de sante publique 79(1):127. https://doi.org/10.1186/s13690-021-00646-9 Wu X, Liu X, Liao W, Kang N, Dong X, Abdulai T, Zhai Z, Wang C, Wang X, Li Y (2021) Prevalence and characteristics of alcohol consumption and risk of type 2 diabetes mellitus in rural China. BMC Public Health 21(1):1644. https://doi.org/10.1186/s12889-021-11681-0 Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653. https://doi.org/10.1002/mds.23429 Tsai JC, Chen CW, Chu H, Yang HL, Chung MH, Liao YM, Chou KR (2016) Comparing the sensitivity, specificity, and predictive values of the montreal cognitive assessment and mini-mental state examination when screening people for mild cognitive impairment and dementia in Chinese population. Arch Psychiatr Nurs 30(4):486–491. https://doi.org/10.1016/j.apnu.2016.01.015 Troughton JA, Woodside JV, Young IS, Arveiler D, Amouyel P, Ferrières J, Ducimetière P, Patterson CC, Kee F, Yarnell JW, Evans A (2007) Homocysteine and coronary heart disease risk in the PRIME study. Atherosclerosis 191(1):90–97. https://doi.org/10.1016/j.atherosclerosis.2006.05.014 Prins ND, Scheltens P (2015) White matter hyperintensities, cognitive impairment and dementia: an update. Nat Rev Neurol 11(3):157–165. https://doi.org/10.1038/nrneurol.2015.10 Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM (2014) Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology 83(14):1228–1234. https://doi.org/10.1212/wnl.0000000000000837 Licking N, Murchison C, Cholerton B, Zabetian CP, Hu SC, Montine TJ, Peterson-Hiller AL, Chung KA, Edwards K, Leverenz JB, Quinn JF (2017) Homocysteine and cognitive function in Parkinson’s disease. Parkinsonism Relat Disord 44:1–5. https://doi.org/10.1016/j.parkreldis.2017.08.005 Baiano C, Barone P, Trojano L, Santangelo G (2020) Prevalence and clinical aspects of mild cognitive impairment in Parkinson’s disease: a meta-analysis. Mov Disord 35(1):45–54. https://doi.org/10.1002/mds.27902 Nicoletti A, Luca A, Baschi R, Cicero CE, Mostile G, Davì M, La Bianca G, Restivo V, Zappia M, Monastero R (2021) Vascular risk factors, white matter lesions and cognitive impairment in Parkinson’s disease: the PACOS longitudinal study. J Neurol 268(2):549–558. https://doi.org/10.1007/s00415-020-10189-8 Guo Y, Xu W, Liu FT, Li JQ, Cao XP, Tan L, Wang J, Yu JT (2019) Modifiable risk factors for cognitive impairment in Parkinson’s disease: a systematic review and meta-analysis of prospective cohort studies. Mov Disord 34(6):876–883. https://doi.org/10.1002/mds.27665 Malek N, Lawton MA, Swallow DM, Grosset KA, Marrinan SL, Bajaj N, Barker RA, Burn DJ, Hardy J, Morris HR, Williams NM, Wood N, Ben-Shlomo Y, Grosset DG (2016) Vascular disease and vascular risk factors in relation to motor features and cognition in early Parkinson’s disease. Mov Disord 31(10):1518–1526. https://doi.org/10.1002/mds.26698 Park YW, Shin NY, Chung SJ, Kim J, Lim SM, Lee PH, Lee SK, Ahn KJ (2019) Magnetic resonance imaging-visible perivascular spaces in basal ganglia predict cognitive decline in Parkinson’s disease. Mov Disord 34(11):1672–1679. https://doi.org/10.1002/mds.27798 Jellinger KA (2006) The morphological basis of mental dysfunction in Parkinson’s disease. J Neurol Sci 248(1–2):167–172. https://doi.org/10.1016/j.jns.2006.05.002 Aarsland D, Perry R, Brown A, Larsen JP, Ballard C (2005) Neuropathology of dementia in Parkinson’s disease: a prospective, community-based study. Ann Neurol 58(5):773–776. https://doi.org/10.1002/ana.20635 Mak E, Dwyer MG, Ramasamy DP, Au WL, Tan LC, Zivadinov R, Kandiah N (2015) White matter hyperintensities and mild cognitive impairment in Parkinson’s disease. J Neuroimaging 25(5):754–760. https://doi.org/10.1111/jon.12230 Shin J, Choi S, Lee JE, Lee HS, Sohn YH, Lee PH (2012) Subcortical white matter hyperintensities within the cholinergic pathways of Parkinson’s disease patients according to cognitive status. J Neurol Neurosurg Psychiatry 83(3):315–321. https://doi.org/10.1136/jnnp-2011-300872 van den Berg E, Geerlings MI, Biessels GJ, Nederkoorn PJ, Kloppenborg RP (2018) White matter hyperintensities and cognition in mild cognitive impairment and Alzheimer’s disease: a domain-specific meta-analysis. J Alzheimer’s Dis JAD 63(2):515–527. https://doi.org/10.3233/jad-170573 Kynast J, Lampe L, Luck T, Frisch S, Arelin K, Hoffmann KT, Loeffler M, Riedel-Heller SG, Villringer A, Schroeter ML (2018) White matter hyperintensities associated with small vessel disease impair social cognition beside attention and memory. J Cereb Blood Flow Metab 38(6):996–1009. https://doi.org/10.1177/0271678x17719380 Lampe L, Kharabian-Masouleh S, Kynast J, Arelin K, Steele CJ, Löffler M, Witte AV, Schroeter ML, Villringer A, Bazin PL (2019) Lesion location matters: the relationships between white matter hyperintensities on cognition in the healthy elderly. J Cereb Blood Flow Metab 39(1):36–43. https://doi.org/10.1177/0271678x17740501 Brown R, Benveniste H, Black SE, Charpak S, Dichgans M, Joutel A, Nedergaard M, Smith KJ, Zlokovic BV, Wardlaw JM (2018) Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res 114(11):1462–1473. https://doi.org/10.1093/cvr/cvy113 Wardlaw JM, Sandercock PA, Dennis MS, Starr J (2003) Is breakdown of the blood–brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke 34(3):806–812. https://doi.org/10.1161/01.str.0000058480.77236.b3 Wardlaw JM, Smith C, Dichgans M (2013) Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol 12(5):483–497. https://doi.org/10.1016/s1474-4422(13)70060-7 Huijts M, Duits A, Staals J, Kroon AA, de Leeuw PW, van Oostenbrugge RJ (2014) Basal ganglia enlarged perivascular spaces are linked to cognitive function in patients with cerebral small vessel disease. Curr Neurovasc Res 11(2):136–141. https://doi.org/10.2174/1567202611666140310102248 Paradise M, Crawford JD, Lam BCP, Wen W, Kochan NA, Makkar S, Dawes L, Trollor J, Draper B, Brodaty H, Sachdev PS (2021) Association of dilated perivascular spaces with cognitive decline and incident dementia. Neurology 96(11):e1501–e1511. https://doi.org/10.1212/wnl.0000000000011537 Ding J, Sigurðsson S, Jónsson PV, Eiriksdottir G, Charidimou A, Lopez OL, van Buchem MA, Guðnason V, Launer LJ (2017) Large perivascular spaces visible on magnetic resonance imaging, cerebral small vessel disease progression, and risk of dementia: the age gene/environment susceptibility-reykjavik study. JAMA Neurol 74(9):1105–1112. https://doi.org/10.1001/jamaneurol.2017.1397 Bouvy WH, van Veluw SJ, Kuijf HJ, Zwanenburg JJ, Kappelle JL, Luijten PR, Koek HL, Geerlings MI, Biessels GJ (2020) Microbleeds colocalize with enlarged juxtacortical perivascular spaces in amnestic mild cognitive impairment and early Alzheimer’s disease: a 7 Tesla MRI study. J Cereb Blood Flow Metab 40(4):739–746. https://doi.org/10.1177/0271678x19838087 Wang ML, Yu MM, Wei XE, Li WB, Li YH (2021) Association of enlarged perivascular spaces with Aβ and tau deposition in cognitively normal older population. Neurobiol Aging 100:32–38. https://doi.org/10.1016/j.neurobiolaging.2020.12.014 Dubost F, Yilmaz P, Adams H, Bortsova G, Ikram MA, Niessen W, Vernooij M, de Bruijne M (2019) Enlarged perivascular spaces in brain MRI: automated quantification in four regions. Neuroimage 185:534–544. https://doi.org/10.1016/j.neuroimage.2018.10.026 Charidimou A, Hong YT, Jäger HR, Fox Z, Aigbirhio FI, Fryer TD, Menon DK, Warburton EA, Werring DJ, Baron JC (2015) White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke 46(6):1707–1709. https://doi.org/10.1161/strokeaha.115.009090 Banerjee G, Kim HJ, Fox Z, Jäger HR, Wilson D, Charidimou A, Na HK, Na DL, Seo SW, Werring DJ (2017) MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain J Neurol 140(4):1107–1116. https://doi.org/10.1093/brain/awx003 Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Investig 123(3):1299–1309. https://doi.org/10.1172/jci67677 Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4(147):147111. https://doi.org/10.1126/scitranslmed.3003748 Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212(7):991–999. https://doi.org/10.1084/jem.20142290 Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560):337–341. https://doi.org/10.1038/nature14432 Duperron MG, Tzourio C, Sargurupremraj M, Mazoyer B, Soumaré A, Schilling S, Amouyel P, Chauhan G, Zhu YC, Debette S (2018) Burden of dilated perivascular spaces, an emerging marker of cerebral small vessel disease, is highly heritable. Stroke 49(2):282–287. https://doi.org/10.1161/strokeaha.117.019309 Ballerini L, Booth T, Valdés Hernández MDC, Wiseman S, Lovreglio R, Muñoz Maniega S, Morris Z, Pattie A, Corley J, Gow A, Bastin ME, Deary IJ, Wardlaw J (2020) Computational quantification of brain perivascular space morphologies: associations with vascular risk factors and white matter hyperintensities. A study in the Lothian Birth Cohort 1936. NeuroImage Clin 25:102120. https://doi.org/10.1016/j.nicl.2019.102120 Laveskog A, Wang R, Bronge L, Wahlund LO, Qiu C (2018) Perivascular spaces in old age: assessment, distribution, and correlation with white matter hyperintensities. AJNR Am J Neuroradiol 39(1):70–76. https://doi.org/10.3174/ajnr.A5455 Wang X, Valdés Hernández Mdel C, Doubal F, Chappell FM, Piper RJ, Deary IJ, Wardlaw JM (2016) Development and initial evaluation of a semi-automatic approach to assess perivascular spaces on conventional magnetic resonance images. J Neurosci Methods 257:34–44. https://doi.org/10.1016/j.jneumeth.2015.09.010 Banerjee G, Jang H, Kim HJ, Kim ST, Kim JS, Lee JH, Im K, Kwon H, Lee JM, Na DL, Seo SW, Werring DJ (2018) Total MRI small vessel disease burden correlates with cognitive performance, cortical atrophy, and network measures in a memory clinic population. J Alzheimer’s Dis JAD 63(4):1485–1497. https://doi.org/10.3233/jad-170943