Hostname: page-component-cb9f654ff-hn9fh Total loading time: 0 Render date: 2025-08-08T14:59:00.290Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex Differences in Cognitive Changes in De Novo Parkinson’s Disease

Published online by Cambridge University Press:  11 December 2019

Ece Bayram Open the ORCID record for Ece Bayram [Opens in a new window] ,
Sarah J. Banks ,
Guogen Shan ,
Nikki Kaplan  and
Jessica Z.K. Caldwell
Ece Bayram*
Affiliation:
Department of Neurosciences, University of California San Diego, La Jolla, CA, USA
Sarah J. Banks
Affiliation:
Department of Neurosciences, University of California San Diego, La Jolla, CA, USA
Guogen Shan
Affiliation:
Department of Environmental and Occupational Health, University of Nevada Las Vegas, Las Vegas, NV, USA
Nikki Kaplan
Affiliation:
Lou Ruvo Center for Brain Health, Cleveland Clinic, Las Vegas, NV, USA
Jessica Z.K. Caldwell
Affiliation:
Lou Ruvo Center for Brain Health, Cleveland Clinic, Las Vegas, NV, USA
*
*Correspondence and reprint requests to: Ece Bayram, University of California San Diego, 9500 Gilman Dr, La Jolla, CA 92093-0886, USA. E-mail: drecebayram@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

To evaluate the sex differences in cognitive course over 4 years in Parkinson’s disease (PD) patients with and without mild cognitive impairment (MCI) compared to controls.

Methods:

Four-year longitudinal cognitive scores of 257 cognitively intact PD, 167 PD-MCI, and 140 controls from the Parkinson’s Progression Markers Initiative were included. Longitudinal scores of men and women, and PD with and without MCI were compared.

Results:

Women had better verbal memory, men had better visuospatial function. There was no interaction between sex, diagnostic group, and/or time (4-year follow-up period).

Conclusions:

Sex differences in cognitive course in de novo PD are similar to healthy aging. Cognitive decline rates in PD with and without MCI are similar for the first 4 years of PD.

Keywords

Parkinson’s diseaseCognitionSexLongitudinal studiesMemoryDecline

Information

Type
Brief Communication
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 2 , February 2020 , pp. 241 - 249
Copyright
Copyright © INS. Published by Cambridge University Press, 2019 

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Aarsland, D., Bronnick, K., Williams-Gray, C., Weintraub, D., Marder, K., Kulisevsky, J., Burn, D., Barone, P., Pagonabarraga, J., Allcock, L., Santangelo, G., Foltynie, T., Janvin, C., Larsen, J.P., Barker, R.A., & Emre, M. (2010). Mild cognitive impairment in Parkinson disease: A multicenter pooled analysis. Neurology, 75(12), 1062–1069. doi: 10.1212/WNL.0b013e3181f39d0e CrossRefGoogle ScholarPubMed
Andreano, J.M. & Cahill, L. (2009). Sex influences on the neurobiology of learning and memory. Learning and Memory, 16, 248–266. doi: 10.1101/lm.918309 CrossRefGoogle ScholarPubMed
Bartels, C., Wegrzyn, M., Wiedl, A., Ackermann, V., & Ehrenreich, H. (2010). Practice effects in healthy adults: A longitudinal study on frequent repetitive cognitive testing. Retrieved from http://www.biomedcentral.com/1471-2202/11/118 CrossRefGoogle Scholar
Benedict, R.H.B., Schretlen, D., Groninger, L., & Brandt, J. (1998). Hopkins verbal learning test – Revised: Normative data and analysis of inter-form and test-retest reliability. The Clinical Neuropsychologist, 12(1), 43–55. doi: 10.1076/clin.12.1.43.1726 CrossRefGoogle Scholar
Benton, A.L., Varney, N.R., & Hamsher, K.D. (1978). Visuospatial judgment. A clinical test. Archives of Neurology, 35(6), 364–367. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/655909 CrossRefGoogle ScholarPubMed
Broeders, M., de Bie, R.M.A., Velseboer, D.C., Speelman, J.D., Muslimovic, D., & Schmand, B. (2013). Evolution of mild cognitive impairment in Parkinson disease. Neurology, 81(4), 346–352. doi: 10.1212/WNL.0b013e31829c5c86 CrossRefGoogle ScholarPubMed
Brunet, H.E., Caldwell, J.Z.K., & Miller, J.B. (2018). Sex differences in learning and memory within a clinical sample of older adults. Alzheimer’s & Dementia, 14(7), P1307. doi: 10.1016/j.jalz.2018.06.1848 CrossRefGoogle Scholar
Burke, S.L., Hu, T., Fava, N.M., Li, T., Rodriguez, M.J., Schuldiner, K.L., Burgess, A., & Laird, A. (2018). Sex differences in the development of mild cognitive impairment and probable Alzheimer’s disease as predicted by the hippocampal volume or white matter hyperintensities. Journal of Women and Aging, 31(2), 140–164. doi: 10.1080/08952841.2018.1419476 CrossRefGoogle ScholarPubMed
Cholerton, B., Johnson, C.O., Fish, B., Quinn, J.F., Chung, K.A., Peterson-Hiller, A.L., Rosenthal, L.S., Dawson, T.M., Albert, M.S., Hu, S.C., Mata, I.F., Leverenz, J.B., Poston, K.L., Montine, T.J., Zabetian, C.P., & Edwards, K.L. (2018). Sex differences in progression to mild cognitive impairment and dementia in Parkinson’s disease. Parkinsonism & Related Disorders, 50, 29–36. doi: 10.1016/J.PARKRELDIS.2018.02.007 CrossRefGoogle ScholarPubMed
de la Riva, P., Smith, K., Xie, S.X., & Weintraub, D. (2014). Course of psychiatric symptoms and global cognition in early Parkinson disease. Neurology, 83(12), 1096–1103. doi: 10.1212/WNL.0000000000000801 CrossRefGoogle ScholarPubMed
Doiron, M., Langlois, M., Dupré, N., & Simard, M. (2018). The influence of vascular risk factors on cognitive function in early Parkinson’s disease. International Journal of Geriatric Psychiatry, 33(2), 288–297. doi: 10.1002/gps.4735 CrossRefGoogle ScholarPubMed
Dotson, V.M., Szymkowicz, S.M., Kirton, J.W., McLaren, M.E., Green, M.L., & Rohani, J.Y. (2014). Unique and interactive effect of anxiety and depressive symptoms on cognitive and brain function in young and older adults. Journal of Depression & Anxiety, Jan(Suppl 1), 22565. doi: 10.4172/2167-1044.S1-003 CrossRefGoogle Scholar
Goetz, C.G., Tilley, B.C., Shaftman, S.R., Stebbins, G.T., Fahn, S., Martinez-Martin, P., Poewe, W., Sampaio, C., Stern, M.B., Dodel, R., Dubois, B., Holloway, R., Jankovic, J., Kulisevsky, J., Lang, A.E., Lees, A., Leurgans, S., LeWitt, P.A., Nyenhuis, D., Olanow, C.W., Rascol, O., Schrag, A., Teresi, J.A., van Hilten, J.J., LaPelle, N., & Movement Disorder Society UPDRS Revision Task Force. (2008). Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Movement Disorders, 23(15), 2129–2170. doi: 10.1002/mds.22340 CrossRefGoogle ScholarPubMed
Harada, C.N., Natelson Love, M.C., & Triebel, K.L. (2013). Normal cognitive aging. Clinics in Geriatric Medicine, 29(4), 737–752. doi: 10.1016/j.cger.2013.07.002 CrossRefGoogle ScholarPubMed
Jaussent, I., Bouyer, J., Ancelin, M.-L., Berr, C., Foubert-Samier, A., Ritchie, K., Ohayon, M.M., Besset, A., & Dauvilliers, Y. (2012). Excessive sleepiness is predictive of cognitive decline in the elderly. Sleep, 35(9), 1201–1207. doi: 10.5665/sleep.2070 CrossRefGoogle ScholarPubMed
Johns, M.W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14(6), 540–545. doi: 10.1093/sleep/14.6.540 CrossRefGoogle ScholarPubMed
Levy, G., Schupf, N., Tang, M.-X., Cote, L.J., Louis, E.D., Mejia, H., Stern, Y., & Marder, K. (2002). Combined effect of age and severity on the risk of dementia in Parkinson’s disease. Annals of Neurology, 51(6), 722–729. doi: 10.1002/ana.10219 CrossRefGoogle ScholarPubMed
Litvan, I., Aarsland, D., Adler, C.H., Goldman, J.G., Kulisevsky, J., Mollenhauer, B., Rodriguez-Oroz, M.C., Tröster, A.I., & Weintraub, D. (2011). MDS task force on mild cognitive impairment in Parkinson’s disease: Critical review of PD-MCI. Movement Disorders: Official Journal of the Movement Disorder Society, 26(10), 1814–1824. doi: 10.1002/mds.23823 CrossRefGoogle ScholarPubMed
Litvan, I., Goldman, J.G., Tröster, A.I., Schmand, B.A., Weintraub, D., Petersen, R.C., Mollenhauer, B., Adler, C.H., Marder, K., Williams-Gray, C.H., Aarsland, D., Kulisevsky, J., Rodriguez-Oroz, M.C., Burn, D.J., Barker, R.A., & Emre, M. (2012). Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Movement Disorders, 27(3), 349–356. doi: 10.1002/mds.24893 CrossRefGoogle ScholarPubMed
Liu, G., Locascio, J.J., Corvol, J.-C., Boot, B., Liao, Z., Page, K., Franco, D., Burke, K., Jansen, I.E., Trisini-Lipsanopoulos, A., Winder-Rhodes, S., Tanner, C.M., Lang, A.E., Eberly, S., Elbaz, A., Brice, A., Mangone, G., Ravina, B., Shoulson, I., Cormier-Dequaire, F., Heutink, P., van Hilten, J.J., Barker, R.A., Williams-Gray, C.H., Marinus, J., Scherzer, C.R., HBS, CamPaIGN, PICNICS, PROPARK, PSG, DIGPD, & PDBP (2017). Prediction of cognition in Parkinson’s disease with a clinical–genetic score: A longitudinal analysis of nine cohorts. The Lancet Neurology, 16(8), 620–629. doi: 10.1016/S1474-4422(17)30122-9 CrossRefGoogle ScholarPubMed
Liu, R., Umbach, D.M., Peddada, S.D., Xu, Z., Tröster, A.I., Huang, X., & Chen, H. (2015). Potential sex differences in nonmotor symptoms in early drug-naive Parkinson disease. Neurology, 84(21), 2107–2115. doi: 10.1212/WNL.0000000000001609 CrossRefGoogle ScholarPubMed
Marek, K., Jennings, D., Lasch, S., Siderowf, A., Tanner, C., Simuni, T., Coffey, C., Kieburtz, K., Flagg, E., Chowdhury, S., & Poewe, W. (2011). The Parkinson Progression Marker Initiative (PPMI). Progress in Neurobiology, 95(4), 629–635. doi: 10.1016/j.pneurobio.2011.09.005 CrossRefGoogle Scholar
Meara, J., Mitchelmore, E., & Hobson, P. (1999). Use of the GDS-15 geriatric depression scale as a screening instrument for depressive symptomatology in patients with Parkinson’s disease and their carers in the community. Age and Ageing, 28(1), 35–38. doi: 10.1093/ageing/28.1.35 CrossRefGoogle Scholar
Munro, C.A., Winicki, J.M., Schretlen, D.J., Gower, E.W., Turano, K.A., Muñoz, B., Keay, L., Bandeen-Roche, K., West, S.K. (2012). Sex differences in cognition in healthy elderly individuals. Neuropsychology, Development, and Cognition. Section B, Aging, Neuropsychology and Cognition, 19(6), 759–768. doi: 10.1080/13825585.2012.690366 CrossRefGoogle ScholarPubMed
Nasreddine, Z.S., Phillips, N.A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J.L., & Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699. doi: 10.1111/j.1532-5415.2005.53221.x CrossRefGoogle ScholarPubMed
Pigott, K., Rick, J., Xie, S.X., Hurtig, H., Chen-Plotkin, A., Duda, J.E., Morley, J.F., Chahine, L.M., Dahodwala, N., Akhtar, R.S., & Siderowf, A. (2015). Longitudinal study of normal cognition in Parkinson disease. Neurology, 85(15), 1276–1282. doi: 10.1212/WNL.0000000000002001 CrossRefGoogle ScholarPubMed
Rana, A.Q., Yousuf, M.S., Naz, S., & Qa’aty, N. (2012). Prevalence and relation of dementia to various factors in Parkinson’s disease. Psychiatry and Clinical Neurosciences, 66(1), 64–68. doi: 10.1111/j.1440-1819.2011.02291.x CrossRefGoogle ScholarPubMed
Rosen, W.G. (1980). Verbal fluency in aging and dementia. Journal of Clinical Neuropsychology, 2(2), 135–146. doi: 10.1080/01688638008403788 CrossRefGoogle Scholar
Samat, N.A., Abdul Murad, N.A., Mohamad, K., Abdul Razak, M.R., & Mohamed Ibrahim, N. (2017). Apolipoprotein Eϵ4: A biomarker for executive dysfunction among Parkinson’s disease patients with mild cognitive impairment. Frontiers in Neuroscience, 11, 712. doi: 10.3389/fnins.2017.00712 CrossRefGoogle Scholar
Smith, A. (1968). The symbol-digit modalities test: A neuropsychologic test of learning and other cerebral disorders. In Helmuth, J. (Ed.), Learning disorders (pp. 83–91). Seattle: Special Child Publications.Google Scholar
Spielberger, C.D., Gorsuch, R.L., & Lushene, R.E. (1970). The state-trait anxiety inventory. MANUAL. https://doi.org/10.1037/t06496-000 CrossRefGoogle Scholar
Wechsler, D. (1997). WAIS – III: Wechsler Adult Intelligence Scale (3rd ed.). Administration and scoring manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Supplementary material: File

Bayram et al. supplementary material

Tables S1-S3

Download Bayram et al. supplementary material(File)
File 24.9 KB