Hostname: page-component-77c89778f8-vsgnj Total loading time: 0 Render date: 2024-07-16T23:18:04.692Z Has data issue: false hasContentIssue false
  • English
  • Français

A Positive Relationship between Cognitive Reserve and Cognitive Function after Stroke: Dynamic Proxies Correlate Better than Static Proxies

Published online by Cambridge University Press:  18 July 2019

Macarena Gil-Pagés Open the ORCID record for Macarena Gil-Pagés [Opens in a new window] ,
Rocío Sánchez-Carrión ,
Jose M. Tormos ,
Antonia Enseñat-Cantallops  and
Alberto García-Molina
Macarena Gil-Pagés*
Affiliation:
Institut Guttmann, Institut Universitari de Neurorehabilitació, adscrit a la Universitat Autònoma de Barcelona, Badalona, Barcelona, Spain Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Fundació Institut d´Investigació en Ciències de la Salut Germans Trias i Pujol, Badalona, Barcelona, Spain Departament de Psicologia Clínica i de la Salut, Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain
Rocío Sánchez-Carrión
Affiliation:
Institut Guttmann, Institut Universitari de Neurorehabilitació, adscrit a la Universitat Autònoma de Barcelona, Badalona, Barcelona, Spain Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Fundació Institut d´Investigació en Ciències de la Salut Germans Trias i Pujol, Badalona, Barcelona, Spain
Jose M. Tormos
Affiliation:
Institut Guttmann, Institut Universitari de Neurorehabilitació, adscrit a la Universitat Autònoma de Barcelona, Badalona, Barcelona, Spain Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Fundació Institut d´Investigació en Ciències de la Salut Germans Trias i Pujol, Badalona, Barcelona, Spain
Antonia Enseñat-Cantallops
Affiliation:
Institut Guttmann, Institut Universitari de Neurorehabilitació, adscrit a la Universitat Autònoma de Barcelona, Badalona, Barcelona, Spain Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Fundació Institut d´Investigació en Ciències de la Salut Germans Trias i Pujol, Badalona, Barcelona, Spain
Alberto García-Molina
Affiliation:
Institut Guttmann, Institut Universitari de Neurorehabilitació, adscrit a la Universitat Autònoma de Barcelona, Badalona, Barcelona, Spain Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Fundació Institut d´Investigació en Ciències de la Salut Germans Trias i Pujol, Badalona, Barcelona, Spain
*
*Correspondence and reprint requests to: Mailing address: Cami de Can Ruti s/n, 08916 Badalona, Barcelona, Spain. E-mail: macarenagil@guttmann.com. Telephone number: (+34) 934977700 ext.2141
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: How brain damage after stroke is related to specific clinical manifestation and recovery is incompletely understood. We studied cognitive reserve (CR) in stroke patients by two types of measurements: (i) objectively verifiable static proxies (i.e., education, occupational attainment), and (ii) subjective, dynamic proxies based on patient testimony in response to a questionnaire. We hypothesized that one or both of these types of CR measurements might correlate positively with patient cognitive performance during the post-acute and chronic phases of recovery. Method: Thirty-four stroke patients underwent neuropsychological assessment at 2, 6 and 24 months after stroke onset. In chronic stage at 24+ months, self-rating assessments of cognitive performance in daily life and social integration were obtained. CR before and after stroke was estimated using static proxies and dynamic proxies were obtained using the Cognitive Reserve Scale (CRS-Pre-stroke, CRS-Post-stroke). Results: CRS-Pre-stroke and CRS-Post-stroke showed significant mean differences. Dynamic proxies showed positive correlation with self-assessment of attention, metacognition, and functional ability in chronic stage. In contrast, significant correlations between static proxies and cognitive recovery were not found. Conclusions: Dynamic proxies of CR were positively correlated with patients’ perception of their functional abilities in daily life. To best guide cognitive prognosis and treatment, we propose that dynamic proxies of CR should be included in neuropsychological assessments of patients with brain damage.

Keywords

Brain injuryDaily livingSelf-assessmentPrognosisCognitionNeuropsychological tests
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 9 , October 2019 , pp. 910 - 921
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.)

References

REFERENCES

Adam, S., Bonsang, E., Grotz, C., & Perelman, S. (2013). Occupational activity and cognitive reserve: Implications in terms of prevention of cognitive aging and Alzheimer’s disease. Clinical Interventions in Aging, 8, 377–390.CrossRefGoogle ScholarPubMed
Alosco, M.L., Mez, J., Kowall, N.W., Stein, T.D., Goldstein, L.E., Cantu, R.C., … McKee, A.C. (2017). Cognitive reserve as a modifier of clinical expression in CTE. The Journal of Neuropsychiatry and Clinical Neuroscience, 29(1), 6–12.CrossRefGoogle Scholar
Baldivia, B., Andrade, V., & Bueno, O. (2008). Contribution of education, occupation and cognitively stimulating activities to the formation of cognitive reserve. Dementia & Neuropsychologia, 2(3), 173–182.CrossRefGoogle ScholarPubMed
Barker-Collo, S., Feigin, V.L., Parag, V., Lawes, C.M., & Senior, H. (2010). Auckland stroke outcomes study. Part 2: Cognition and functional outcomes 5 years poststroke. Neurology, 75(18), 1608–1616.CrossRefGoogle ScholarPubMed
Barulli, D., & Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: Emerging concepts in cognitive reserve. Trends in Cognitive Sciences, 17(10), 502–509.CrossRefGoogle ScholarPubMed
Bennett, D., Schneider, J.A., Tang, Y., Arnold, S.E., & Wilson, R.S. (2006). The effect of social networks on the relationship between Alzheimer’s disease pathology and level of cognitive function in old people: A longitudinal cohort study. Lancet Neurology, 5(5) 406–412.CrossRefGoogle Scholar
Berggren, R., Nilsson, J., & Lövdén, M. (2018). Education does not affect cognitive decline in aging: A Bayesian assessment of the association between education and change in cognitive performance. Frontiers in Psychology, 9, 1138.CrossRefGoogle Scholar
Bouffioulx, E., Thonnard, J., Arnould, C., & Vandervelde, L. (2010). Changes in satisfaction with activities and participation between acute, post-acute and chronic stroke phases: A responsiveness study of the SATIS-Stroke questionnaire. Journal of Rehabilitation Medicine, 42(10), 944–948.CrossRefGoogle ScholarPubMed
Crawford, J.R., Smith, G., Maylor, E.A., Della Sala, S., & Logie, R.H. (2003). The Prospective and Retrospective Memory Questionnaire (PRMQ): Normative data and latent structure in a large non-clinical sample. Memory, 11(3), 261–75.CrossRefGoogle Scholar
Cott, C., Wiles, R., & Devitt, R. (2007). Continuity, transition and participation: Preparing clients for life in the community post-stroke. Disability and Rehabilitation, 29(20–21), 1566–1574.CrossRefGoogle ScholarPubMed
Dalemans, R.J., De Witte, L.P., Beurskens, A.J., Van Den Heuvel, W.J., & Wade, D.T. (2010). An investigation into the social participation of stroke survivors with aphasia. Disability and Rehabilitation, 32(20), 1678–1685.CrossRefGoogle ScholarPubMed
Dijkers, M. (2000). The community integration questionnaire. The Center for Outcome Measurement in Brain Injury. Retrieved from http://www.tbims.org/combi/ciq (Accessed October 31, 2018).Google Scholar
Donaghy, M. (2009). Brain’s Diseases of the Nervous System. Oxford: Oxford University Press.Google Scholar
Eacea.ec.europa.eu (2013). Organisation of the Education System and of its Structure. Retrieved from: https://eacea.ec.europa.eu/national-policies/eurydice/content/organisation-education-system-and-its-structure-79_enGoogle Scholar
Effect sizes (2018). Retrieved from http://staff.bath.ac.uk/pssiw/stats2/page2/page14/page14.htmlGoogle Scholar
Elkins, J.S., Longstreth, W.T., Manolio, T.A., Newman, A. B., Bhadelia, R.A., & Johnston, S.C. (2006). Education and the cognitive decline associated with MRI-defined brain infarct. Neurology, 67(3), 435–440.CrossRefGoogle ScholarPubMed
Elsner, B., Kugler, J., Pohl, M., & Mehrholz, J. (2013). Transcranial direct current stimulation for improving function and activities of daily living in patients after stroke. First results of a systematic Cochrane-Review. Clinical Neurophysiology, 124(10), e113.Google Scholar
Ferguson, C.J. (2009). An effect size primer: A guide for clinicians and researchers. American Psychological Association, 40(5), 532–538.Google Scholar
Finkel, D., Andel, R., Gatz, M., & Pedersen, N.L. (2009). The role of occupational complexity in trajectories of cognitive aging before and after retirement. Psychology and Aging, 24, 563–573.CrossRefGoogle ScholarPubMed
Fortuny, L. (1999). Manual de normas y procedimientos para la batería neuropsicológica en español. Hove: Psychology Press.Google Scholar
Garibotto, V., Borroni, B., Kalbe, E., Herholz, K., Salmon, E., Holtoff, V., … Perani, D. (2008). Education and occupation as proxies for reserve in aMCI converters and AD: FDG-PET evidence. Neurology, 71(17), 1342–1349.CrossRefGoogle Scholar
Helmer, C., Letenneur, L., Rouch, I., Richard-Harston, S., Barberger-Gateau, P., Fabrigoule, C., … Dartigues, J.F. (2001). Occupation during life and risk of dementia in French elderly community residents. Journal of Neurology, Neurosurgery & Psychiatry, 71(3), 303–309.CrossRefGoogle ScholarPubMed
Hindle, J.V., Martyr, A., & Clare, L. (2013) Cognitive reserve en Parkinson’s Disease: A Systematic review and meta-analysis. Parkinsonism & Related Disorders, 20(1), 1–7.CrossRefGoogle Scholar
Iacobucci, D. (2010). Structural equations modeling: Fit Indices, sample size, and advanced topics. Journal of Consumer Psychology, 20(1), 90–98.CrossRefGoogle Scholar
Incual.mecd.es. (2018). Incual. Retrieved from: http://incual.mecd.es/Google Scholar
Jellema, S., van Hees, S., Zajec, J., van der Sande, R., Nijhuis-van der Sanden, M., & Steultjens, E. (2017). What environmental factors influence resumption of valued activities post stroke: A systematic review of qualitative and quantitative findings. Clinical Rehabilitation, 31(7), 936–947.CrossRefGoogle ScholarPubMed
Jones, R.N., Manly, J., Glymour, M.M., Rentz, D.M., Jefferson, A.L., & Stern, Y. (2011) Conceptual and measurement challenges in research on cognitive reserve. Journal of the International Neuropsychological Society, 17(4), 593–601.CrossRefGoogle ScholarPubMed
Kesler, S. R., Adams, H. F., Blasey, C. M., & Bigler, E. D. (2003). Premorbid intellectual functioning, education, and brain size in traumatic brain injury: An investigation of the cognitive reserve hypothesis. Applied Neuropsychology, 10(3), 153–162.CrossRefGoogle ScholarPubMed
Kessels, R., Eikelboom, W., Schaapsmeerders, P., Maaijwee, N., Arntz, R., van Dijk, E., & de Leeuw, F. (2017). Effect of formal education on vascular cognitive impairment after stroke: A meta-analysis and study in young-stroke patients. Journal of the International Neuropsychological Society, 23(03), 223–238.CrossRefGoogle ScholarPubMed
Lee, H., Lee, Y., Choi, H., & Pyun, S.B. (2015) Community integration and quality of life in aphasia after stroke. Yonsei Medical Journal, 56(6), 1694–1702.CrossRefGoogle ScholarPubMed
Lenehan, M., Summers, M., Saunders, N., Summers, J., & Vickers, J. (2014). Relationship between education and age-related cognitive decline: A review of recent research. Psychogeriatrics, 15(2), 154–162.CrossRefGoogle ScholarPubMed
León, I., García-García, J. & Roldán-Tapia, L. (2011). Development of the scale of cognitive reserve in Spanish population: A pilot study. Revista de Neurología, 52, 653–660.Google ScholarPubMed
León, I., García-García, J. & Roldán-Tapia, L. (2014). Estimating cognitive reserve in healthy adults using the cognitive reserve scale. PLoS ONE, 9(7), 102632.CrossRefGoogle ScholarPubMed
Lezak, M. (2012). Neuropsychological Assessment (5th ed.). Oxford: Oxford University Press.Google Scholar
Ma, V., Chan, L., & Carruthers, K. (2014). Incidence, prevalence, costs, and impact on disability of common conditions requiring rehabilitation in the United States: Stroke, spinal cord injury, traumatic brain injury, multiple sclerosis, osteoarthritis, rheumatoid arthritis, limb loss, and back pain. Archives of Physical Medicine and Rehabilitation, 95(5), 986–995.e1.CrossRefGoogle ScholarPubMed
Malek-Ahmadi, M., Lu, S., Chan, Y., Perez, S.E., Chen, K., & Mufson, E.J. (2017) Static and dynamic cognitive reserve proxy measures: Interactions with Alzheimer’s disease neuropathology and cognition. Journal of Alzheimer’s Disease & Parkinsonism, 7(6), 390.Google ScholarPubMed
Moyano, Á. (2010). El accidente cerebrovascular desde la mirada del rehabilitador. Revista Hospital Clínica Universitaria de Chile, 21, 348–355.Google Scholar
Nunnari, D., Bramanti, P., & Marino, S. (2014). Cognitive reserve in stroke and traumatic brain injury patients. Neurological Sciences, 35, 1513–1518.CrossRefGoogle ScholarPubMed
Ojala-Oksala, J., Jokinen, H., Kopsi, V., Lehtonen, K., Luukkonen, L., Paukkunen, A., … Oksala, N. (2012). Educational history is an independent predictor of cognitive deficits and long-term survival in post-acute patients with mild to moderate ischemic stroke. Stroke, 43(11), 2931–2935.CrossRefGoogle Scholar
Ponsford, J., & Kinsella, G. (1991). The use of a rating scale of attentional behavior. Neuropsychological Rehabilitation, 1(4), 241–257. doi: 10.1080/09602019108402257CrossRefGoogle Scholar
Prigatano, G., & Fordyce, D. (1986). Neuropsychological Rehabilitation After Brain Injury. Baltimore: Johns Hopkins University Press.Google Scholar
R Core Team (2018). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org/.Google Scholar
Rosseel, Y. (2018). lavaan: An R Package for Structural Equation Modeling. Retrieved from http://lavaan.ugent.be/tutorial/tutorial.pdfGoogle Scholar
Roth, R.M., Isquith, P.K., & Goia, G.A. (2005). BRIEF-A: Behavior Rating Inventory of Executive Function–Adult version. Lutz, Florida: Psychological Assessment Resources Inc. Version 2.00.026.Google Scholar
Sacco, R., Kasner, S., Broderick, J., Caplan, L., Connors, J., Culebras, A., … Vinters, H.V. (2013). An updated definition of stroke for the 21st century. Stroke, 44(7), 2064–2089. doi: 10.1161/str.0b013e318296aecaCrossRefGoogle ScholarPubMed
Sachdev, P.S., Brodaty, H., Valenzuela, M.J., Lorentz, L.M., & Koschera, A. (2004) Progression of cognitive impairment in stroke patients. Neurology, 63, 1618–1623.CrossRefGoogle ScholarPubMed
Sánchez, J.L., Rodríguez, M., Carro, J. (2002). Neuropsychological variables in sporadic late onset Alzheimer disease in subjects of Spanish nationality: A fast and efficient assessment procedure. Neuropsychiatry, Neuropsychology, and Behavioral Neurology. 15(3), 207–215.Google ScholarPubMed
Satz, P. (1993). Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. Neuropsychology, 7(3), 273–295.CrossRefGoogle Scholar
Scarmeas, N., Levy, G., Tang, M.X., Manly, J., & Stern, Y. (2001). Influence of leisure activity on the incidence of Alzheimer’s disease. Neurology, 57(12), 2236–2242.CrossRefGoogle ScholarPubMed
Scarmeas, N., & Stern, Y. (2003). Cognitive reserve and lifestyle. Journal of Clinical and Experimental Neuropsychology, 25(5), 625–633.CrossRefGoogle Scholar
Schmidt, M. (1996). Rey Auditory Verbal Learning Test. Los Angeles, CA: Western Psychological Services.Google Scholar
Schneider, E. B., Sur, S., Raymont, V., Duckworth, J., Kowalski, R. G., Efron, D. T., … Stevens, R. D. (2014). Functional recovery after moderate/severe traumatic brain injury: A role for cognitive reserve? Neurology, 82(18), 1636–1642.CrossRefGoogle ScholarPubMed
Schooler, C., Mulatu, M.S., & Oates, G. (1999). The continuing effects of substantively complex work on the intellectual functioning of older workers. Psychology and Aging, 147, 483–506.CrossRefGoogle Scholar
Schooler, C., Mulatu, M.S., & Oates, G. (2004). Occupational self-direction, intellectual functioning, and self-directed orientation in older workers: Findings and implication for individuals and societies. American Journal of Sociology, 110, 161–167.CrossRefGoogle Scholar
Singam, A., Ytterberg, C., Tham, K., & von Koch, L. (2015). Participation in complex and social everyday activities six years after stroke: Predictors for return to pre-stroke level. PLOS ONE, 10(12), e0144344.CrossRefGoogle ScholarPubMed
Stern, Y. (1994). Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA: The Journal of the American Medical Association, 271 (13), 1004.CrossRefGoogle ScholarPubMed
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society, 8(03), 448–460.CrossRefGoogle ScholarPubMed
Stern, Y. (2006) Cognitive reserve and Alzheimer disease. Alzheimer Disease Association Disorders, 20(3 Suppl 2), S69–74.CrossRefGoogle ScholarPubMed
Stern, Y. (2009) Cognitive reserve. Neuropsychologia, 47(10), 2015–2028.CrossRefGoogle ScholarPubMed
Stern, Y. (2016). An approach to studying the neural correlates of reserve. Brain Imaging and Behavior, 11(2), 410–416.CrossRefGoogle Scholar
Stern, Y., Arenaza-Urquijo, E., Bartrés-Faz, D., Belleville, S., Cantilon, M., Chetelat, G., … Vuoksimaa, E. (2018). Whitepaper: Defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimer’s & Dementia. doi: 10.1016/j.jalz.2018.07.219CrossRefGoogle Scholar
Stern, Y., Albert, S., Tang, M., & Tsai, W. (1999). Rate of memory decline in AD is related to education and occupation: Cognitive reserve? Neurology, 53(9), 1942–1942.CrossRefGoogle ScholarPubMed
Steward, K.A., Kennedy, R., Novack, T.A., Crowe, M., Marson, D.C., & Triebel, K.L. (2018). The role of cognitive reserve in recovery from traumatic brain injury. The Journal of Head Trauma Rehabilitation, 33(1), E18–E27. doi: 10.1097/HTR.0000000000000325Google ScholarPubMed
Sumowski, J.F., Chiaravalloti, N., Krch, D. Paxton, J., DeLuca, J. (2013). Education attenuates the negative impact of traumatic brain injury on cognitive status. Archives of Physical Medicine and Rehabilitation, 94(12), 2562–4.CrossRefGoogle ScholarPubMed
Sumowski, J.F., Rocca, M.A., Leavitt, V.M., Riccitelli, G., Comi, G., DeLuca, J., & Filippi, M. (2013). Brain reserve and cognitive reserve in multiple sclerosis: What you’ve got and how you use it. Neurology, 80(24), 2186–2193.CrossRefGoogle Scholar
Teasell, R., & Hussein, N. (2016). Rehabilitation of cognitive impairment post stroke. In Stroke Rehabilitation Clinician Handbook. Retrieved from http://www.ebrsr.com/sites/default/files/Chapter%205_Cognitive.pdfGoogle Scholar
Tombaugh, T. (2004). Trail making Test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203–214.CrossRefGoogle Scholar
Umarova, R. (2017). Adapting the concepts of brain and cognitive reserve to post-stroke cognitive deficits: Implications for understanding neglect. Cortex, 97, 327–338.CrossRefGoogle ScholarPubMed
Valenzuela, M., & Sachdev, P. (2006). Brain reserve and dementia: A systematic review. Psychological Medicine, 36(4),441–454.CrossRefGoogle ScholarPubMed
Verberne, D., Post, M., Köhler, S., Carey, L., Visser-Meily, J., & van Heugten, C. (2018). Course of social participation in the first 2 years after stroke and its associations with demographic and stroke-related factors. Neurorehabilitation and Neural Repair, 32(9), 821–833.CrossRefGoogle ScholarPubMed
Verghese, J., Wang, C., Katz, M. J., Sanders, A., & Lipton, R. B. (2009). Leisure activities and risk of vascular cognitive impairment in older adults. Journal of Geriatric Psychiatry and Neurology, 22(2), 110–118.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). WAIS-III. San Antonio, TX: Psychological Corporation.Google Scholar
Willer, B., Rosenthal, M., Kreutzer, J., Gordon, W., & Rempel, R. (1993). Assessment of community integration following rehabilitation for traumatic brain injury. Journal of Head Trauma Rehabilitation, 8(2), 75–87.CrossRefGoogle Scholar
World Medical Association Declaration of Helsinki (2013). JAMA: The Journal of the American Medical Association, 310(20), 2191.CrossRefGoogle Scholar
Zieren, N., Dueringa, M., Peters, N., Reyes, S., Jouvent, E., Hervéc, D., … Dichgansd, M. (2013). Education modifies the relation of vascular pathology to cognitive function: Cognitive reserve in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurobiology of Aging, 34(2), 400–407.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gil-Pagés et al. supplementary material

Gil-Pagés et al. supplementary material
Download Gil-Pagés et al. supplementary material(File)
File 31.8 KB