Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-23T15:55:52.950Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  06 February 2017

Jacob D. Jones ,
Jared J. Tanner ,
Michael Okun ,
Catherine C. Price  and
Dawn Bowers
Jacob D. Jones
Affiliation:
Department of Clinical and Health Psychology, McKnight Brain Institute, University of Florida, Gainesville, Florida Center for Movement Disorders and Neurorestoration, McKnight Brain Institute, University of Florida, Gainesville, Florida
Jared J. Tanner
Affiliation:
Department of Clinical and Health Psychology, McKnight Brain Institute, University of Florida, Gainesville, Florida
Michael Okun
Affiliation:
Center for Movement Disorders and Neurorestoration, McKnight Brain Institute, University of Florida, Gainesville, Florida Department of Neurology, McKnight Brain Institute, University of Florida, Gainesville, Florida
Catherine C. Price
Affiliation:
Department of Clinical and Health Psychology, McKnight Brain Institute, University of Florida, Gainesville, Florida
Dawn Bowers*
Affiliation:
Department of Clinical and Health Psychology, McKnight Brain Institute, University of Florida, Gainesville, Florida Department of Neurology, McKnight Brain Institute, University of Florida, Gainesville, Florida
*
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: dawnbowers@phhp.ufl.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

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)

Keywords

Parkinson’s diseaseCognitionMemoryExecutive functionCerebrovascular diseasesMagnetic resonance imaging
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 4 , April 2017 , pp. 322 - 331
Copyright
Copyright © The International Neuropsychological Society 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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), 357–381.Google Scholar
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), 2037–2114.Google Scholar
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), 1252–1257.Google Scholar
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), 223–229.Google Scholar
Bohnen, N.I., & Albin, R.L. (2011). White matter lesions in Parkinson disease. Nature Reviews Neurology, 7(4), 229–236.Google Scholar
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), 743–753.Google Scholar
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), 2083–2089.Google Scholar
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), 461–468.Google Scholar
Dubois, B., & Pillon, B. (1996). Cognitive deficits in Parkinson’s disease. Journal of Neurology, 244(1), 2–8.Google Scholar
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), 1689–1707.Google Scholar
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. 153–163). New York: Raven Press.Google Scholar
Fischl, B. (2012). FreeSurfer. Neuroimage, 62(2), 774–781.Google Scholar
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), 37–43.Google Scholar
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, e6–e245.Google Scholar
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, 95–99.Google Scholar
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), 386–390.Google Scholar
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.Google Scholar
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), 1716–1722.Google Scholar
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), 181–184.Google Scholar
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), 626–636.Google Scholar
Jellinger, K. (2012). Heterogenous mechanisms of mild cognitive impairment in Parkinson’s disease. Journal of Neural Transmission, 119(3), 381–382.Google Scholar
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.Google Scholar
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), 1073–1078.Google Scholar
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), 211–216.Google Scholar
Jurica, P.J., Mattis, S., & Leitten, C.L. (2001). Dementia Rating Scale-2: DRS-2. Lutz, FL: Psychological Assessment Resources.Google Scholar
Kehagia, A.A., Barker, R.A., & Robbins, T.W. (2012). Cognitive impairment in Parkinson’s disease: The dual syndrome hypothesis. Neurodegenerative Diseases, 11(2), 79–92.Google Scholar
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), 227–233.Google Scholar
Levin, B.E., & Katzen, H.L. (1994). Early cognitive changes and nondementing behavioral abnormalities in Parkinson’s disease. Advances in Neurology, 65, 85–95.Google Scholar
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), 83–100.Google Scholar
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), 349–356.Google Scholar
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), 754–760.Google Scholar
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.Google Scholar
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), 1841–1849.Google Scholar
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), 533–541.Google Scholar
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), 563–570.Google Scholar
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), 734–740.Google Scholar
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), 833–847.Google Scholar
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.Google Scholar
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), 138–143.Google Scholar
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), 2649–2653.Google Scholar
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.Google Scholar
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), 160–167.Google Scholar
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), 29–34.Google Scholar
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), 193–210.Google Scholar
Supplementary material: File

Jones supplementary material S1

Supplementary Table

Download Jones supplementary material S1(File)
File 41.3 KB
Supplementary material: File

Jones supplementary material S2

Supplementary Table

Download Jones supplementary material S2(File)
File 44.4 KB
Supplementary material: File

Jones supplementary material S3

Supplementary Table

Download Jones supplementary material S3(File)
File 89.1 KB