Abstract
Stroke is a leading cause of death and disability. It is a complex and largely heterogeneous condition. Prognosis for variations in impairment and recovery following stroke continues to be challenging and inaccurate, highlighting the need to examine the influence of other currently unknown variables to better predict and understand interindividual differences in stroke impairment and recovery. The concept of “cognitive reserve,” a feature of brain function said to moderate the relationship between brain pathology and clinical outcomes, might provide a partial explanation. This review discusses the potential significance of cognitive reserve in the context of stroke, with reference to reduced burden of disability poststroke, health promotion, intervention and secondary prevention of cognitive impairment, ease and challenges of translation into clinical practice, prognosis and prediction of recovery, and clinical decisions and trial stratification. Discussions from the review aim to encourage stroke clinicians and researchers to better consider the role of premorbid, lifestyle-related variables, such as cognitive reserve, in facilitating successful neurological outcomes and recovery following stroke.
References
| 1. | Murphy, TH, Corbett, D. Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci. 2009;10:861–872. Google Scholar | Crossref | Medline | ISI |
| 2. | Donkor, ES. Stroke in the 21st century: a snapshot of the burden, epidemiology, and quality of life. Stroke Res Treat. 2018;2018:3238165. Google Scholar | Crossref | Medline |
| 3. | Boyd, LA, Hayward, KS, Ward, NS, et al. Biomarkers of stroke recovery: consensus-based core recommendations from the Stroke Recovery and Rehabilitation Roundtable. Int J Stroke. 2017;12:480–493. Google Scholar | SAGE Journals | ISI |
| 4. | Jang, SH. The role of the corticospinal tract in motor recovery in patients with a stroke: a review. NeuroRehabilitation. 2009;24:285–290. Google Scholar | Crossref | Medline | ISI |
| 5. | Stinear, CM, Byblow, WD, Ackerley, SJ, Smith, MC, Borges, VM, Barber, PA. PREP2: a biomarker-based algorithm for predicting upper limb function after stroke. Ann Clin Transl Neurol. 2017;4:811–820. Google Scholar | Crossref | Medline |
| 6. | Chamorro, A, Vila, N, Ascaso, C, et al. Early prediction of stroke severity. Role of the erythrocyte sedimentation rate. Stroke. 1995;26:573–576. Google Scholar | Crossref | Medline | ISI |
| 7. | Cheng, B, Forkert, ND, Zavaglia, M, et al. Influence of stroke infarct location on functional outcome measured by the modified Rankin scale. Stroke. 2014;45:1695–1702. Google Scholar | Crossref | Medline | ISI |
| 8. | Fridriksson, J, Guo, D, Fillmore, P, Holland, A, Rorden, C. Damage to the anterior arcuate fasciculus predicts non-fluent speech production in aphasia. Brain. 2013;136(pt 11):3451–3460. Google Scholar | Crossref | Medline |
| 9. | Grube, MM, Koennecke, HC, Walter, G, et al; Berlin Stroke Register . Association between socioeconomic status and functional impairment 3 months after ischemic stroke: the Berlin Stroke Register. Stroke. 2012;43:3325–3330. Google Scholar | Crossref | Medline |
| 10. | Lansberg, MG, Lee, J, Christensen, S, et al. RAPID automated patient selection for reperfusion therapy: a pooled analysis of the Echoplanar Imaging Thrombolytic Evaluation Trial (EPITHET) and the Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution (DEFUSE) study. Stroke. 2011;42:1608–1614. Google Scholar | Crossref | Medline | ISI |
| 11. | Stern, Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc. 2002;8:448–460. Google Scholar | Crossref | Medline | ISI |
| 12. | Umarova, RM. Adapting the concepts of brain and cognitive reserve to post-stroke cognitive deficits: implications for understanding neglect. Cortex. 2017;97:327–338. Google Scholar | Crossref | Medline |
| 13. | Pinter, D, Enzinger, C, Fazekas, F. Cerebral small vessel disease, cognitive reserve and cognitive dysfunction. J Neurol. 2015;262:2411–2419. Google Scholar | Crossref | Medline |
| 14. | Barulli, D, Stern, Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17:502–509. Google Scholar | Crossref | Medline | ISI |
| 15. | Winkleby, MA, Jatulis, DE, Frank, E, Fortmann, SP. Socioeconomic status and health: how education, income, and occupation contribute to risk factors for cardiovascular disease. Am J Public Health. 1992;82:816–820. Google Scholar | Crossref | Medline | ISI |
| 16. | Stern, Y. Cognitive reserve. Neuropsychologia. 2009;47:2015–2028. Google Scholar | Crossref | Medline | ISI |
| 17. | Rosenich, E, Hordacre, B, McDonnell, M, Hillier, SL. Brain and cognitive reserve measurement in healthy and neurological populations: a scoping review. Paper presented at: 47th Annual Meeting of the International Neuropsychological Society; February 2019; New York, NY. Google Scholar |
| 18. | Satz, P. Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology. 1993;7:273–295. Google Scholar | Crossref |
| 19. | Stern, Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord. 2006;20(3 suppl 2):S69–S74. Google Scholar | Crossref | Medline | ISI |
| 20. | Stern, Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11:1006–1012. Google Scholar | Crossref | Medline | ISI |
| 21. | Jones, RN, Manly, J, Glymour, MM, Rentz, DM, Jefferson, AL, Stern, Y. Conceptual and measurement challenges in research on cognitive reserve. J Int Neuropsychol Soc. 2011;17:593–601. Google Scholar | Crossref | Medline | ISI |
| 22. | Lenehan, ME, Summers, MJ, Saunders, NL, et al. Sending your grandparents to university increases cognitive reserve: the Tasmanian Healthy Brain Project. Neuropsychology. 2016;30:525–531. Google Scholar | Crossref | Medline |
| 23. | Steffener, J, Reuben, A, Rakitin, BC, Stern, Y. Supporting performance in the face of age-related neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging Behav. 2011;5:212–221. Google Scholar | Crossref | Medline |
| 24. | Steffener, J, Stern, Y. Exploring the neural basis of cognitive reserve in aging. Biochim Biophys Acta. 2012;1822:467–473. Google Scholar | Crossref | Medline |
| 25. | Cizginer, S, Marcantonio, E, Vasunilashorn, S, et al. The cognitive reserve model in the development of delirium: the successful aging after elective surgery study. J Geriatr Psychiatry Neurol. 2017;30:337–345. Google Scholar | SAGE Journals | ISI |
| 26. | Albers, GW, Marks, MP, Kemp, S, et al; EFUSE 3 Investigators . Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018;378:708–718. Google Scholar | Crossref | Medline |
| 27. | Vance, DE, Crowe, M. A proposed model of neuroplasticity and cognitive reserve in older adults. Act Adapt Aging. 2006;30:61–79. Google Scholar | Crossref |
| 28. | Booth, AJ, Rodgers, JD, Schwartz, CE, et al. Active cognitive reserve influences the regional atrophy to cognition link in multiple sclerosis. J Int Neuropsychol Soc. 2013;19:1128–1133. Google Scholar | Crossref | Medline |
| 29. | Sachdev, PS, Brodaty, H, Valenzuela, MJ, Lorentz, LM, Koschera, A. Progression of cognitive impairment in stroke patients. Neurology. 2004;63:1618–1623. Google Scholar | Crossref | Medline | ISI |
| 30. | Vemuri, P, Lesnick, TG, Przybelski, SA, et al. Vascular and amyloid pathologies are independent predictors of cognitive decline in normal elderly. Brain. 2015;138(3 pt):761–771. doi:10.1093/brain/awu393 Google Scholar | Crossref | Medline |
| 31. | Langhorne, P, Bernhardt, J, Kwakkel, G. Stroke rehabilitation. Lancet. 2011;377:1693–1702. Google Scholar | Crossref | Medline | ISI |
| 32. | Levin, MF, Kleim, JA, Wolf, SL. What do motor “recovery” and “compensation” mean in patients following stroke? Neurorehabil Neural Repair. 2009;23:313–319. Google Scholar | SAGE Journals | ISI |
| 33. | Stern, Y, Gazes, Y, Razlighi, Q, Steffener, J, Habeck, C. A task-invariant cognitive reserve network. Neuroimage. 2018;178:36–45. Google Scholar | Crossref | Medline |
| 34. | Buchman, AS, Yu, L, Boyle, PA, Schneider, JA, De Jager, PL, Bennett, DA. Higher brain BDNF gene expression is associated with slower cognitive decline in older adults. Neurology. 2016;86:735–741. Google Scholar | Crossref | Medline |
| 35. | Nithianantharajah, J, Hannan, AJ. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog Neurobiol. 2009;89:369–382. Google Scholar | Crossref | Medline | ISI |
| 36. | Babulal, GM, Huskey, TN, Roe, CM, Goette, SA, Connor, LT. Cognitive impairments and mood disruptions negatively impact instrumental activities of daily living performance in the first three months after a first stroke. Top Stroke Rehabil. 2015;22:144–151. Google Scholar | Crossref | Medline |
| 37. | Brainin, M, Tuomilehto, J, Heiss, WD, et al. Post-stroke cognitive decline: an update and perspectives for clinical research. Eur J Neurol. 2015;22:229–238,e13-e16. Google Scholar | Crossref | Medline | ISI |
| 38. | Cumming, TB, Marshall, RS, Lazar, RM. Stroke, cognitive deficits, and rehabilitation: still an incomplete picture. Int J Stroke. 2013;8:38–45. Google Scholar | SAGE Journals | ISI |
| 39. | Pendlebury, ST, Rothwell, PM; Oxford Vascular Study . Incidence and prevalence of dementia associated with transient ischaemic attack and stroke: analysis of the population-based Oxford Vascular Study. Lancet Neurol. 2019;18:248–258. Google Scholar | Crossref | Medline |
| 40. | Makin, SDJ, Turpin, S, Dennis, MS, Wardlaw, JM. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry. 2013;84:893–900. Google Scholar | Crossref | Medline | ISI |
| 41. | Ojala-Oksala, J, Jokinen, H, Kopsi, V, et al. Educational history is an independent predictor of cognitive deficits and long-term survival in postacute patients with mild to moderate ischemic stroke. Stroke. 2012;43:2931–2935. Google Scholar | Crossref | Medline | ISI |
| 42. | Umarova, RM, Sperber, C, Kaller, CP, et al. Cognitive reserve impacts on disability and cognitive deficits in acute stroke. J Neurol. 2019;266:2495–2504. Google Scholar | Crossref | Medline |
| 43. | Farfel, JM, Nitrini, R, Suemoto, CK, et al; Brazilian Aging Brain Study Group . Very low levels of education and cognitive reserve: a clinicopathologic study. Neurology. 2013;81:650–657. Google Scholar | Crossref | Medline |
| 44. | Makin, SD, Doubal, FN, Shuler, K, et al. The impact of early-life intelligence quotient on post stroke cognitive impairment. Eur Stroke J. 2018;3:145–156. Google Scholar | SAGE Journals | ISI |
| 45. | Alladi, S, Bak, TH, Mekala, S, et al. Impact of bilingualism on cognitive outcome after stroke. Stroke. 2016;47:258–261. Google Scholar | Crossref | Medline |
| 46. | Glymour, MM, Weuve, J, Fay, ME, Glass, T, Berkman, LF. Social ties and cognitive recovery after stroke: does social integration promote cognitive resilience? Neuroepidemiology. 2008;31:10–20. Google Scholar | Crossref | Medline | ISI |
| 47. | Abutalebi, J, Guidi, L, Borsa, V, et al. Bilingualism provides a neural reserve for aging populations. Neuropsychologia. 2015;69:201–210. Google Scholar | Crossref | Medline |
| 48. | Antoniou, M, Wright, SM. Uncovering the mechanisms responsible for why language learning may promote healthy cognitive aging. Front Psychol. 2017;8:2217. Google Scholar | Crossref | Medline |
| 49. | Luk, G, Bialystok, E, Craik, FI, Grady, CL. Lifelong bilingualism maintains white matter integrity in older adults. J Neurosci. 2011;31:16808–16813. Google Scholar | Crossref | Medline | ISI |
| 50. | Langhorne, P, Coupar, F, Pollock, A. Motor recovery after stroke: a systematic review. Lancet Neurol. 2009;8:741–754. Google Scholar | Crossref | Medline | ISI |
| 51. | Stinear, CM. Prediction of motor recovery after stroke: advances in biomarkers. Lancet Neurol. 2017;16:826–836. Google Scholar | Crossref | Medline |
| 52. | Bigourdan, A, Munsch, F, Coupé, P, et al. Early fiber number ratio is a surrogate of corticospinal tract integrity and predicts motor recovery after stroke. Stroke. 2016;47:1053–1059. Google Scholar | Crossref | Medline | ISI |
| 53. | Grefkes, C, Fink, GR. Connectivity-based approaches in stroke and recovery of function. Lancet Neurol. 2014;13:206–216. Google Scholar | Crossref | Medline | ISI |
| 54. | Cramer, SC . Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Ann Neurol. 2008;63:272–287. Google Scholar | Crossref | Medline | ISI |
| 55. | Marshall, IJ, Wang, Y, Crichton, S, McKevitt, C, Rudd, AG, Wolfe, CD. The effects of socioeconomic status on stroke risk and outcomes. Lancet Neurol. 2015;14:1206–1218. Google Scholar | Crossref | Medline | ISI |
| 56. | Bettger, JP, Zhao, X, Bushnell, C, et al. The association between socioeconomic status and disability after stroke: findings from the Adherence eValuation After Ischemic stroke Longitudinal (AVAIL) registry. BMC Public Health. 2014;14:281. Google Scholar | Crossref | Medline | ISI |
| 57. | Marsh, EB, Lawrence, E, Hillis, AE, Chen, K, Gottesman, RF, Llinas, RH. Pre-stroke employment results in better patient-reported outcomes after minor stroke. Clin Neurol Neurosurg. 2018;165:38–42. Google Scholar | Crossref | Medline |
| 58. | El Hachioui, H, Lingsma, HF, van de Sandt-Koenderman, MW, Dippel, DW, Koudstaal, PJ, Visch-Brink, EG. Long-term prognosis of aphasia after stroke. J Neurol Neurosurg Psychiatry. 2013;84:310–315. Google Scholar | Crossref | Medline |
| 59. | Watila, MM, Balarabe, SA. Factors predicting post-stroke aphasia recovery. J Neurol Sci. 2015;352:12–18. Google Scholar | Crossref | Medline |
| 60. | González-Fernández, M, Davis, C, Molitoris, JJ, Newhart, M, Leigh, R, Hillis, AE. Formal education, socioeconomic status, and the severity of aphasia after stroke. Arch Phys Med Rehabil. 2011;92:1809–1813. Google Scholar | Crossref | Medline |
| 61. | Marchina, S, Zhu, LL, Norton, A, Zipse, L, Wan, CY, Schlaug, G. Impairment of speech production predicted by lesion load of the left arcuate fasciculus. Stroke. 2011;42:2251–2256. Google Scholar | Crossref | Medline | ISI |
| 62. | Hackett, ML, Pickles, K. Part I: frequency of depression after stroke: an updated systematic review and meta-analysis of observational studies. Int J Stroke. 2014;9:1017–1025. Google Scholar | SAGE Journals | ISI |
| 63. | Backhouse, EV, McHutchison, CA, Cvoro, V, Shenkin, SD, Wardlaw, JM. Cognitive ability, education and socioeconomic status in childhood and risk of post-stroke depression in later life: a systematic review and meta-analysis. PLoS One. 2018;13:e0200525. Google Scholar | Crossref | Medline |
| 64. | Feigin, VL, Forouzanfar, MH, Krishnamurthi, R, et al. Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet. 2014;383:245–255. Google Scholar | Crossref | Medline | ISI |
| 65. | Feigin, VL, Roth, GA, Naghavi, M, et al. Global burden of stroke and risk factors in 188 countries, during 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet Neurol. 2016;15:913–924. Google Scholar | Crossref | Medline | ISI |
| 66. | Nunnari, D, Bramanti, P, Marino, S. Cognitive reserve in stroke and traumatic brain injury patients. Neurol Sci. 2014;35:1513–1518. Google Scholar | Crossref | Medline |
| 67. | Richards, M, Sacker, A. Lifetime antecedents of cognitive reserve. J Clin Exp Neuropsychol. 2003;25:614–624. Google Scholar | Crossref | Medline | ISI |
| 68. | Fratiglioni, L, Paillard-Borg, S, Winblad, B. An active and socially integrated lifestyle in late life might protect against dementia. Lancet Neurol. 2004;3:343–353. Google Scholar | Crossref | Medline | ISI |
| 69. | Chan, D, Shafto, M, Kievit, R, et al. Lifestyle activities in mid-life contribute to cognitive reserve in late-life, independent of education, occupation, and late-life activities. Neurobiol Aging. 2018;70:180–183. Google Scholar | Crossref | Medline |
| 70. | Moretti, L, Cristofori, I, Weaver, SM, Chau, A, Portelli, JN, Grafman, J. Cognitive decline in older adults with a history of traumatic brain injury. Lancet Neurol. 2012;11:1103–1112. Google Scholar | Crossref | Medline | ISI |
| 71. | Mirza, SS, Portegies, ML, Wolters, FJ, et al. Higher education is associated with a lower risk of dementia after a stroke or TIA. The Rotterdam study. Neuroepidemiology. 2016;46:120–127. Google Scholar | Crossref | Medline |
| 72. | Malsch, C, Liman, T, Wiedmann, S, et al. Outcome after stroke attributable to baseline factors—the PROSpective Cohort with Incident Stroke (PROSCIS). PLoS One. 2018;13:e0204285. Google Scholar | Crossref | Medline |
| 73. | Colcombe, SJ, Erickson, KI, Scalf, PE, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci. 2006;61:1166–1170. Google Scholar | Crossref | Medline | ISI |
| 74. | Marzolini, S, Oh, P, McIlroy, W, Brooks, D. The effects of an aerobic and resistance exercise training program on cognition following stroke. Neurorehabil Neural Repair. 2013;27:392–402. Google Scholar | SAGE Journals | ISI |
| 75. | Bo, W, Lei, M, Tao, S, et al. Effects of combined intervention of physical exercise and cognitive training on cognitive function in stroke survivors with vascular cognitive impairment: a randomized controlled trial. Clin Rehabil. 2019;33:54–63. Google Scholar | SAGE Journals | ISI |
| 76. | Ploughman, M, Eskes, GA, Kelly, LP, et al. Synergistic benefits of combined aerobic and cognitive training on fluid intelligence and the role of IGF-1 in chronic stroke. Neurorehabil Neural Repair. 2019;33:199–212. Google Scholar | SAGE Journals | ISI |
| 77. | Wang, HX, MacDonald, SW, Dekhtyar, S, Fratiglioni, L. Association of lifelong exposure to cognitive reserve-enhancing factors with dementia risk: a community-based cohort study. PLoS Med. 2017;14:e1002251. Google Scholar | Crossref | Medline |
| 78. | Chapko, D, McCormack, R, Black, C, Staff, R, Murray, A. Life-course determinants of cognitive reserve (CR) in cognitive aging and dementia—a systematic literature review. Aging Ment Health. 2018;22:915–926. Google Scholar | Crossref | Medline |
| 79. | Feigin, VL, Krishnamurthi, R, Bhattacharjee, R, et al. New strategy to reduce the global burden of stroke. Stroke. 2015;46:1740–1747. Google Scholar | Crossref | Medline | ISI |
| 80. | Willis, K, Hakim, AM. Stroke prevention and cognitive reserve: emerging approaches to modifying risk and delaying onset of dementia. Front Neurol. 2013;4:13. Google Scholar | Crossref | Medline |
| 81. | Nucci, M, Mapelli, D, Mondini, S. Cognitive Reserve Index questionnaire (CRIq): a new instrument for measuring cognitive reserve. Aging Clin Exp Res. 2012;24:218–226. Google Scholar | Medline |
| 82. | Stinear, C. Prediction of recovery of motor function after stroke. Lancet Neurol. 2010;9:1228–1232. Google Scholar | Crossref | Medline | ISI |
| 83. | Leary, JB, Kim, GY, Bradley, CL, et al. The association of cognitive reserve in chronic-phase functional and neuropsychological outcomes following traumatic brain injury. J Head Trauma Rehabil. 2018;33:E28–E35. Google Scholar | Crossref | Medline |
| 84. | Cramer, SC, Wolf, SL, Adams, HP, et al. Stroke recovery and rehabilitation research: issues, opportunities, and the National Institutes of Health StrokeNet. Stroke. 2017;48:813–819. Google Scholar | Crossref | Medline |
| 85. | Fortune, DG, Walsh, RS, Richards, HL. Cognitive reserve and preinjury educational attainment: effects on outcome of community-based rehabilitation for longer-term individuals with acquired brain injury. Int J Rehabil Res. 2016;39:234–239. Google Scholar | Crossref | Medline |
| 86. | Munsch, F, Sagnier, S, Asselineau, J, et al. Stroke location is an independent predictor of cognitive outcome. Stroke. 2016;47:66–73. Google Scholar | Crossref | Medline |
| 87. | Matthews, KA, Gallo, LC. Psychological perspectives on pathways linking socioeconomic status and physical health. Annu Rev Psychol. 2011;62:501–530. Google Scholar | Crossref | Medline | ISI |
| 88. | Glader, EL, Edlund, H, Sukhova, M, Asplund, K, Norrving, B, Eriksson, M. Reduced inequality in access to stroke unit care over time: a 15-year follow-up of socioeconomic disparities in Sweden. Cerebrovasc Dis. 2013;36:407–411. Google Scholar | Crossref | Medline |
| 89. | Stecksén, A, Glader, EL, Asplund, K, Norrving, B, Eriksson, M. Education level and inequalities in stroke reperfusion therapy: observations in the Swedish stroke register. Stroke. 2014;45:2762–2768. Google Scholar | Crossref | Medline |
| 90. | Ikanga, J, Hill, EM, MacDonald, DA. The conceptualization and measurement of cognitive reserve using common proxy indicators: testing some tenable reflective and formative models. J Clin Exp Neuropsychol. 2017;39:72–83. Google Scholar | Crossref | Medline |
| 91. | Reed, BR, Mungas, D, Farias, ST, et al. Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain. 2010;133(pt 8):2196–2209. Google Scholar | Crossref | Medline |
| 92. | Sandry, J, DeLuca, J, Chiaravalloti, N. Working memory capacity links cognitive reserve with long-term memory in moderate to severe TBI: a translational approach. J Neurol. 2015;262:59–64. Google Scholar | Crossref | Medline |
| 93. | Schwartz, CE, Michael, W, Zhang, J, Rapkin, BD, Sprangers, MAG. Assessing reserve-building pursuits and person characteristics: psychometric validation of the Reserve-Building Measure. Qual Life Res. 2018;27:423–436. Google Scholar | Crossref | Medline |
TBI Rehabilitation 