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Are Parkinson’s Patients More Vulnerable to the Effects of Cardiovascular Risk: A Neuroimaging and Neuropsychological Study

  • Jacob D. Jones (a1) (a2), Jared J. Tanner (a1), Michael Okun (a2) (a3), Catherine C. Price (a1) and Dawn Bowers (a1) (a3)...


Objectives: This study examined whether individuals with Parkinson’s disease (PD) are at increased vulnerability for vascular-related cognitive impairment relative to controls. The underlying assumption behind this hypothesis relates to brain reserve and that both PD and vascular risk factors impair similar fronto-executive cognitive systems. Methods: The sample included 67 PD patients and 61 older controls (total N=128). Participants completed neuropsychological measures of executive functioning, processing speed, verbal delayed recall/memory, language, and auditory attention. Cardiovascular risk was assessed with the Framingham Cardiovascular Risk index. Participants underwent brain imaging (T1 and T2 FLAIR). Trained raters measured total and regional leukoaraiosis (periventricular, deep subcortical, and infracortical). Results: Hierarchical regressions revealed that more severe cardiovascular risk was related to worse executive functioning, processing speed, and delayed verbal recall in both Parkinson patients and controls. More severe cardiovascular risk was related to worse language functioning in the PD group, but not controls. In contrast, leukoaraiosis related to both cardiovascular risk and executive functioning for controls, but not the PD group. Conclusions: Overall, results revealed that PD and cardiovascular risk factors are independent risk factors for cognitive impairment. Generally, the influence of cardiovascular risk factors on cognition is similar in PD patients and controls. (JINS, 2017, 23, 322–331)


Corresponding author

Correspondence and reprint requests to: Dawn Bowers, Clinical & Health Psychology, College of Public Health & Health Professions, 101 S. Newell Drive, PO Box 100165, University of Florida, Gainesville, FL 32601. E-mail:


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Alexander, G.E., DeLong, M.R., & Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9(1), 357381.
Aronow, W.S., Fleg, J.L., Pepine, C.J., Artinian, N.T., Bakris, G., Brown, A.S., & Kostis, J.B. (2011). ACCF/AHA 2011 expert consensus document on hypertension in the elderly: A report of the American College of Cardiology Foundation Task Force on clinical expert consensus documents developed in collaboration with the American Academy of Neurology, American Geriatrics Society, American Society for Preventive Cardiology, American Society of Hypertension, American Society of Nephrology, Association of Black Cardiologists, and European Society of Hypertension. Journal of the American College of Cardiology, 57(20), 20372114.
Barton, B.R., Bernard, B., Czernecki, V., Goldman, J.G., Stebbins, G., Dubois, B. &Goetz, C.G. (2014). Comparison of the Movement Disorder Society Parkinson’s disease dementia criteria with neuropsychological testing. Movement Disorders, 29(10), 12521257.
Beyer, M.K., Aarsland, D., Greve, O.J., & Larsen, J.P. (2006). Visual rating of white matter hyperintensities in Parkinson’s disease. Movement Disorders, 21(2), 223229.
Bohnen, N.I., & Albin, R.L. (2011). White matter lesions in Parkinson disease. Nature Reviews Neurology, 7(4), 229236.
D’Agostino, R.B., Vasan, R.S., Pencina, M.J., Wolf, P.A., Cobain, M., Massaro, J.M., && Kannel, W.B. (2008). General cardiovascular risk profile for use in primary care the Framingham Heart Study. Circulation, 117(6), 743753.
Dalaker, T.O., Larsen, J.P., Dwyer, M.G., Aarsland, D., Beyer, M.K., Alves, G., & Zivadinov, R. (2009). White matter hyperintensities do not impact cognitive function in patients with newly diagnosed Parkinson’s disease. Neuroimage, 47(4), 20832089.
Debette, S., Seshadri, S., Beiser, A., Au, R., Himali, J.J., Palumbo, C., & DeCarli, C. (2011). Midlife vascular risk factor exposure accelerates structural brain aging and cognitive decline. Neurology, 77(5), 461468.
Dubois, B., & Pillon, B. (1996). Cognitive deficits in Parkinson’s disease. Journal of Neurology, 244(1), 28.
Emre, M., Aarsland, D., Brown, R., Burn, D.J., Duyckaerts, C., Mizuno, Y., & Goldman, J. (2007). Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Movement Disorders, 22(12), 16891707.
Fahn, S., & Elton, R., members of the UPDRS Development Committee. (1987). In S. Fahn, C.D. Mardsen, P. Jenner & P. Teychenne (Eds.), Recent developments in Parkinson’s disease (pp. 153163). New York: Raven Press.
Fischl, B. (2012). FreeSurfer. Neuroimage, 62(2), 774781.
Freitas, S., Simões, M.R., Alves, L., & Santana, I. (2013). Montreal cognitive assessment: Validation study for mild cognitive impairment and Alzheimer disease. Alzheimer Disease & Associated Disorders, 27(1), 3743.
Go, A.S., Mozaffarian, D., Roger, V.L., Benjamin, E.J., Berry, J.D., Borden, W.B., & Turner, M.B. (2013). American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics—2013 update: A report from the American Heart Association. Circulation, 127, e6e245.
Ham, J.H., Lee, J.J., Sunwoo, M.K., Hong, J.Y., Sohn, Y.H., & Lee, P.H. (2016). Effect of olfactory impairment and white matter hyperintensities on cognition in Parkinson’s disease. Parkinsonism & Related Disorders, 24, 9599.
Haugarvoll, K., Aarsland, D., Wentzel‐Larsen, T., & Larsen, J.P. (2005). The influence of cerebrovascular risk factors on incident dementia in patients with Parkinson’s disease. Acta Neurologica Scandinavica, 112(6), 386390.
Heaton, R.K., Miller, S.W., Taylor, M.J., & Grant, I. (2004). Revised comprehensive norms for an expanded Halstead-Reitan Battery: Demographically adjusted neuropsychological norms for African American and Caucasian adults. Lutz, FL: Psychological Assessment Resources.
Hilker, R., Thomas, A.V., Klein, J.C., Weisenbach, S., Kalbe, E., Burghaus, L., & Heiss, W.D. (2005). Dementia in Parkinson disease functional imaging of cholinergic and dopaminergic pathways. Neurology, 65(11), 17161722.
Hughes, A.J., Daniel, S.E., Kilford, L., & Lees, A.J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery, & Psychiatry, 55(3), 181184.
Irwin, D.J., Lee, V.M.Y., & Trojanowski, J.Q. (2013). Parkinson’s disease dementia: Convergence of α-synuclein, tau and amyloid-β pathologies. Nature Reviews Neuroscience, 14(9), 626636.
Jellinger, K. (2012). Heterogenous mechanisms of mild cognitive impairment in Parkinson’s disease. Journal of Neural Transmission, 119(3), 381382.
Jones, J.D., Jacobson, C., Murphy, M., Price, C., Okun, M.S., & Bowers, D. (2014). Influence of hypertension on neurocognitive domains in nondemented Parkinson’s disease patients. Parkinson’s Disease, 2014, 507529.
Jones, J.D., Malaty, I., Price, C.C., Okun, M.S., & Bowers, D. (2012). Health comorbidities and cognition in 1948 patients with idiopathic Parkinson’s disease. Parkinsonism & Related Disorders, 18(10), 10731078.
Jones, J.D., Mangal, P., Lafo, J., Okun, M.S., & Bowers, D. (2016). Mood Differences Among Parkinson’s Disease Patients With Mild Cognitive Impairment. The Journal of Neuropsychiatry and Clinical Neurosciences, 28(3), 211216.
Jurica, P.J., Mattis, S., & Leitten, C.L. (2001). Dementia Rating Scale-2: DRS-2. Lutz, FL: Psychological Assessment Resources.
Kehagia, A.A., Barker, R.A., & Robbins, T.W. (2012). Cognitive impairment in Parkinson’s disease: The dual syndrome hypothesis. Neurodegenerative Diseases, 11(2), 7992.
Lee, S.J., Kim, J.S., Yoo, J.Y., Song, I.U., Kim, B.S., Jung, S.L., & Lee, K.S. (2010). Influence of white matter hyperintensities on the cognition of patients with Parkinson disease. Alzheimer Disease & Associated Disorders, 24(3), 227233.
Levin, B.E., & Katzen, H.L. (1994). Early cognitive changes and nondementing behavioral abnormalities in Parkinson’s disease. Advances in Neurology, 65, 8595.
Libon, D.J., Price, C.C., Davis Garrett, K., & Giovannetti, T. (2004). From Binswanger’s disease to leuokoaraiosis: What we have learned about subcortical vascular dementia. The Clinical Neuropsychologist, 18(1), 83100.
Litvan, I., Goldman, J.G., Tröster, A.I., Schmand, B.A., Weintraub, D., Petersen, R.C., & Aarsland, D. (2012). Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Movement Disorders, 27(3), 349356.
Mak, E., Dwyer, M.G., Ramasamy, D.P., Au, W.L., Tan, L., Zivadinov, R., && Kandiah, N. (2015). White matter hyperintensities and mild cognitive impairment in Parkinson’s disease. Journal of Neuroimaging, 25(5), 754760.
McDowd, J., Hoffman, L., Rozek, E., Lyons, K.E., Pahwa, R., Burns, J., && Kemper, S. (2011). Understanding verbal fluency in healthy aging, Alzheimer’s disease, and Parkinson’s disease. Neuropsychology, 25(2), 210.
Melzer, T.R., Watts, R., MacAskill, M.R., Pitcher, T.L., Livingston, L., Keenan, R.J., & Anderson, T.J. (2013). White matter microstructure deteriorates across cognitive stages in Parkinson disease. Neurology, 80(20), 18411849.
Nanhoe-Mahabier, W., De Laat, K.F., Visser, J.E., Zijlmans, J., de Leeuw, F.E., & Bloem, B.R. (2009). Parkinson disease and comorbid cerebrovascular disease. Nature Reviews Neurology, 5(10), 533541.
Pilotto, A., Turrone, R., Liepelt-Scarfone, I., Bianchi, M., Poli, L., Borroni, B., & Cosseddu, M. (2016). Vascular risk factors and cognition in Parkinson’s disease. Journal of Alzheimer’s Disease, 51(2), 563570.
Price, C.C., Mitchell, S.M., Brumback, B., Tanner, J.J., Schmalfuss, I., Lamar, M., & Libon, D.J. (2012). MRI-leukoaraiosis thresholds and the phenotypic expression of dementia. Neurology, 79(8), 734740.
Price, C.C., Tanner, J.J., Schmalfuss, I.M., Brumback, B., Heilman, K.M., & Libon, D.J. (2015). Dissociating statistically-determined Alzheimer’s disease/vascular dementia neuropsychological syndromes using white and gray neuroradiological parameters. Journal of Alzheimer’s Disease, 48(3), 833847.
Satz, P. (1993). Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. Neuropsychology, 7(3), 273.
Scigliano, G., Ronchetti, G., Girotti, F., & Musicco, M. (2009). Sympathetic modulation by levodopa reduces vascular risk factors in Parkinson disease. Parkinsonism & Related Disorders, 15(2), 138143.
Tomlinson, C.L., Stowe, R., Patel, S., Rick, C., Gray, R., & Clarke, C.E. (2010). Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Movement Disorders, 25(15), 26492653.
Troyer, A.K., Moscovitch, M., & Winocur, G. (1997). Clustering and switching as two components of verbal fluency: Evidence from younger and older healthy adults. neuropsychology, 11(1), 138.
Verdelho, A., Madureira, S., Moleiro, C., Ferro, J.M., Santos, C.O., Erkinjuntti, T., & Wallin, A. (2010). White matter changes and diabetes predict cognitive decline in the elderly The LADIS Study. Neurology, 75(2), 160167.
Whiteside, D.M., Kealey, T., Semla, M., Luu, H., Rice, L., Basso, M.R., && Roper, B. (2016). Verbal Fluency: Language or Executive Function Measure? Applied Neuropsychology: Adult, 23(1), 2934.
Zgaljardic, D.J., Borod, J.C., Foldi, N.S., & Mattis, P. (2003). A review of the cognitive and behavioral sequelae of Parkinson’s disease: Relationship to frontostriatal circuitry. Cognitive and Behavioral Neurology, 16(4), 193210.


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Are Parkinson’s Patients More Vulnerable to the Effects of Cardiovascular Risk: A Neuroimaging and Neuropsychological Study

  • Jacob D. Jones (a1) (a2), Jared J. Tanner (a1), Michael Okun (a2) (a3), Catherine C. Price (a1) and Dawn Bowers (a1) (a3)...


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