Skip to main content
SpringerLink
Log in

Cognitive reserve impacts on disability and cognitive deficits in acute stroke

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Objective

Although post-stroke cognitive deficit can significantly limit patient independence and social re-integration, clinical routine predictors for this condition are lacking. ‘Cognitive reserve’ limits the detrimental effects of slowly developing neurodegeneration. We aimed to determine whether comparable effects also exist in acute stroke. Using 'years of education' as a proxy, we investigated whether cognitive reserve beneficially influences cognitive performance and disability after stroke, whilst controlling for age and lesion size as measure of stroke pathology.

Methods

Within the first week of ischemic right hemisphere stroke, 36 patients were assessed for alertness, working memory, executive functions, spatial neglect, global cognition and motor deficit at 4.9 ± 2.1 days post-stroke, in addition to routine clinical tests (NIH Stroke Scale, modified Rankin Scale on admission < 24 h post-stroke and at discharge 9.5 ± 4.7 days post-stroke). The impact of education was assessed using partial correlation analysis adjusted for lesion size, age, and the time interval between stroke and assessment. To validate our results, we compared groups with similar age and lesion load, but different education levels.

Results

In the acute stroke phase, years of education predicted both severity of education independent (alertness) and education dependent (working memory, executive functions, global cognition) cognitive deficits and disability (modified Rankin Scale). Spatial neglect seemed to be independent.

Interpretation

Proxies of cognitive reserve should be considered in stroke research as early as in the acute stroke phase. Cognitive reserve contributes to inter-individual variability in the initial severity of cognitive deficits and disability in acute stroke, and may suggest individualised rehabilitation strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Amunts K, Schleicher A, Burgel U et al (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412:319–341

    Article  CAS  PubMed  Google Scholar 

  2. Ward NS, Brown MM, Thompson AJ, Frackowiak RS (2003) Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 126:2476–2496. https://doi.org/10.1093/brain/awg245

    Article  CAS  PubMed  Google Scholar 

  3. Barulli D, Stern Y (2013) Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci 17:502–509. https://doi.org/10.1016/j.tics.2013.08.012

    Article  PubMed  Google Scholar 

  4. Umarova RM (2017) Adapting the concepts of brain and cognitive reserve to post-stroke cognitive deficits: Implications for understanding neglect. Cortex 97:327–338. https://doi.org/10.1016/j.cortex.2016.12.006

    Article  PubMed  Google Scholar 

  5. Franke K, Ziegler G, Klöppel S et al (2010) Estimating the age of healthy subjects from T1-weighted MRI scans using kernel methods: exploring the influence of various parameters. NeuroImage 50:883–892. https://doi.org/10.1016/j.neuroimage.2010.01.005

    Article  PubMed  Google Scholar 

  6. Knoflach M, Matosevic B, Rücker M et al (2012) Functional recovery after ischemic stroke—a matter of age: data from the Austrian Stroke Unit Registry. Neurology 78:279–285. https://doi.org/10.1212/WNL.0b013e31824367ab

    Article  CAS  PubMed  Google Scholar 

  7. Beumer D, Rozeman AD, Lycklama À, Nijeholt GJ et al (2016) The effect of age on outcome after intra-arterial treatment in acute ischemic stroke: a MR CLEAN pretrial study. BMC Neurol 16:68. https://doi.org/10.1186/s12883-016-0592-5

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jaillard A, Grand S, Le Bas JF, Hommel M (2010) Predicting cognitive dysfunctioning in nondemented patients early after stroke. Cerebrovasc Dis Basel Switz 29:415–423. https://doi.org/10.1159/000289344

    Article  Google Scholar 

  9. Nys GM, Van Zandvoort MJ, De Kort PL et al (2005) Domain-specific cognitive recovery after first-ever stroke: a follow-up study of 111 cases. J Int Neuropsychol Soc 11:795–806

    Article  CAS  PubMed  Google Scholar 

  10. IST-3 collaborative group (2015) Association between brain imaging signs, early and late outcomes, and response to intravenous alteplase after acute ischaemic stroke in the third International Stroke Trial (IST-3): secondary analysis of a randomised controlled trial. Lancet Neurol 14:485–496. https://doi.org/10.1016/S1474-4422(15)00012-5

    Article  CAS  Google Scholar 

  11. Ryu W-S, Woo S-H, Schellingerhout D et al (2017) Stroke outcomes are worse with larger leukoaraiosis volumes. Brain 140:158–170. https://doi.org/10.1093/brain/aww259

    Article  PubMed  Google Scholar 

  12. Pendlebury ST, Rothwell PM (2009) Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis. Lancet Neurol 8:1006–1018. https://doi.org/10.1016/S1474-4422(09)70236-4

    Article  PubMed  Google Scholar 

  13. Cramer SC (2008) Repairing the human brain after stroke: I Mechanisms of spontaneous recovery. Ann Neurol 63:272–287. https://doi.org/10.1002/ana.21393

    Article  PubMed  Google Scholar 

  14. Hillis AE (2014) Tippett DC (2014) Stroke recovery: surprising influences and residual consequences. Adv Med. https://doi.org/10.1155/2014/378263

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hachinski V, Iadecola C, Petersen RC et al (2006) National Institute of Neurological Disorders and Stroke-Canadian Stroke Network Vascular Cognitive Impairment Harmonization Standards. Stroke 37:2220–2241. https://doi.org/10.1161/01.STR.0000237236.88823.47

    Article  PubMed  Google Scholar 

  16. Ojala-Oksala J, Jokinen H, Kopsi V et al (2012) Educational history is an independent predictor of cognitive deficits and long-term survival in postacute patients with mild to moderate ischemic stroke. Stroke J Cereb Circ 43:2931–2935. https://doi.org/10.1161/STROKEAHA.112.667618

    Article  Google Scholar 

  17. Ramsey LE, Siegel JS, Lang CE et al (2017) Behavioural clusters and predictors of performance during recovery from stroke. Nat Hum Behav 1:0038. https://doi.org/10.1038/s41562-016-0038

    Article  PubMed  PubMed Central  Google Scholar 

  18. Beume L-A, Martin M, Kaller CP et al (2017) Visual neglect after left-hemispheric lesions: a voxel-based lesion-symptom mapping study in 121 acute stroke patients. Exp Brain Res 235:83–95. https://doi.org/10.1007/s00221-016-4771-9

    Article  PubMed  Google Scholar 

  19. Nasreddine ZS, Phillips NA, Bédirian V et al (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x

    Article  PubMed  Google Scholar 

  20. Wechsler D (2000) Wechsler-Gedächtnistest—Revidierte Fassung: WMS-R; Testmanual; deutsche Adaptation der revidierten Fassung der Wechsler Memory Scale von David Wechler, 1st edn. Hans Huber, Bern

    Google Scholar 

  21. Aschenbrenner A, Tucha O, Lange K (2000) RWT Regensburger Wortflüssigkeits-Test. Hogrefe Verlag, Göttingen

    Google Scholar 

  22. Rorden C, Karnath HO (2010) A simple measure of neglect severity. Neuropsychologia 48:2758–2763. https://doi.org/10.1016/j.neuropsychologia.2010.04.018

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gauthier L, Dehaut F, Joanette Y (1989) The Bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 11(2):49–54

    Google Scholar 

  24. Ota H, Fujii T, Suzuki K et al (2001) Dissociation of body-centered and stimulus-centered representations in unilateral neglect. Neurology 57:2064–2069

    Article  CAS  PubMed  Google Scholar 

  25. Wilson B, Cockburn J, Haligan PW (1987) Behavioural inattention test. Thames Valley Company, Titchfield

    Google Scholar 

  26. Umarova RM, Reisert M, Beier T-U et al (2014) Attention-network specific alterations of structural connectivity in the undamaged white matter in acute neglect. Hum Brain Mapp 35:4678–4692. https://doi.org/10.1002/hbm.22503

    Article  PubMed  PubMed Central  Google Scholar 

  27. Lehrl S (1991) Manual zum MWT. Perimed, Balingen

    Google Scholar 

  28. Fugl-Meyer AR, Jääskö L, Leyman I et al (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31

    CAS  PubMed  Google Scholar 

  29. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113. https://doi.org/10.1016/j.neuroimage.2007.07.007

    Article  PubMed  Google Scholar 

  30. Geerligs L, Renken RJ, Saliasi E et al (2015) A brain-wide study of age-related changes in functional connectivity. Cereb Cortex 25:1987–1999. https://doi.org/10.1093/cercor/bhu012

    Article  PubMed  Google Scholar 

  31. Kaller CP, Loosli SV, Rahm B et al (2014) Working memory in schizophrenia: behavioral and neural evidence for reduced susceptibility to item-specific proactive interference. Biol Psychiatry 76:486–494. https://doi.org/10.1016/j.biopsych.2014.03.012

    Article  PubMed  Google Scholar 

  32. Mahalanobis PC (1936) On the generalized distance in statistics. National Institute of Science of India, vol 2, pp 49–55

  33. Rorden C, Karnath H-O, Bonilha L (2007) Improving lesion-symptom mapping. J Cogn Neurosci 19:1081–1088. https://doi.org/10.1162/jocn.2007.19.7.1081

    Article  PubMed  Google Scholar 

  34. Yang Y, Shi Y-Z, Zhang N et al (2016) The disability rate of 5-year post-stroke and its correlation factors: a National Survey in China. PLoS ONE 11:e0165341. https://doi.org/10.1371/journal.pone.0165341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Grimaud O, Roussel P, Schnitzler A et al (2016) Do socioeconomic disparities in stroke and its consequences decrease in older age? Eur J Public Health 26:799–804. https://doi.org/10.1093/eurpub/ckw058

    Article  PubMed  Google Scholar 

  36. Pasi M, Salvadori E, Poggesi A et al (2013) Factors predicting the Montreal cognitive assessment (MoCA) applicability and performances in a stroke unit. J Neurol 260:1518–1526. https://doi.org/10.1007/s00415-012-6819-5

    Article  PubMed  Google Scholar 

  37. Alladi S, Bak TH, Mekala S et al (2016) Impact of bilingualism on cognitive outcome after stroke. Stroke 47:258–261. https://doi.org/10.1161/STROKEAHA.115.010418

    Article  PubMed  Google Scholar 

  38. Bodenburg S, Popp B, Kawski S (2001) Ergänzende Normdaten zu dem Untertest Alertness aus der Testbatterie zur Aufmerksamkeitsprüfung (TAP) in der Altersgruppe 60+. Z Für Neuropsychol 12:125–130. https://doi.org/10.1024//1016-264X.12.2.125

    Article  Google Scholar 

  39. Corbetta M, Ramsey L, Callejas A et al (2015) Common behavioral clusters and subcortical anatomy in stroke. Neuron 85:927–941. https://doi.org/10.1016/j.neuron.2015.02.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  CAS  PubMed  Google Scholar 

  41. Karnath H-O, Rorden C (2012) The anatomy of spatial neglect. Neuropsychologia 50:1010–1017. https://doi.org/10.1016/j.neuropsychologia.2011.06.027

    Article  PubMed  Google Scholar 

  42. Stern Y (2012) Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol 11:1006–1012. https://doi.org/10.1016/S1474-4422(12)70191-6

    Article  PubMed  PubMed Central  Google Scholar 

  43. Tombaugh TN, Kozak J, Rees L (1999) Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol 14:167–177. https://doi.org/10.1016/S0887-6177(97)00095-4

    Article  CAS  PubMed  Google Scholar 

  44. Jacobs B, Schall M, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. II. Gender, hemispheric, and environmental factors. J Comp Neurol 327:97–111. https://doi.org/10.1002/cne.903270108

    Article  CAS  PubMed  Google Scholar 

  45. Brosnan MB, Demaria G, Petersen A et al (2017) Plasticity of the right-lateralized cognitive reserve network in ageing. Cereb Cortex N Y N 1991:1–11. https://doi.org/10.1093/cercor/bhx085

    Article  Google Scholar 

  46. Mandolesi L, Gelfo F, Serra L et al (2017) Environmental factors promoting neural plasticity: insights from animal and human studies. Neural Plast 2017:7219461. https://doi.org/10.1155/2017/7219461

    Article  PubMed  PubMed Central  Google Scholar 

  47. Steffener J, Reuben A, Rakitin BC, Stern Y (2011) Supporting performance in the face of age-related neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging Behav 5:212–221. https://doi.org/10.1007/s11682-011-9125-4

    Article  PubMed  PubMed Central  Google Scholar 

  48. EClipSE Collaborative Members, Brayne C, Ince PG et al (2010) Education, the brain and dementia: neuroprotection or compensation? Brain J Neurol 133:2210–2216. https://doi.org/10.1093/brain/awq185

    Article  Google Scholar 

  49. Monakow CV (1906) Aphasie und diaschisis. Neurol Cent 25:1026–1038

    Google Scholar 

Download references

Acknowledgements

The authors thank Sebastian Kuebel for his help in the neuropsychological testing. This work was supported by funds of the Department of Neurology, Freiburg, the Brain-Links Brain-Tools Cluster of Excellence (Grant number EXC 1086) as well as by Grant KA1258/23-1 funded by the Deutsche Forschungsgemeinschaft (DFG). Christoph Sperber was supported by the Friedrich Naumann Foundation.

Author information

Author notes

  1. Cornelius Weiller and Hans-Otto Karnath contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, Faculty of Medicine, Medical Center-University of Freiburg, University of Freiburg, Freiburg, Germany

    Roza M. Umarova, Christoph P. Kaller, Charlotte S. M. Schmidt & Cornelius Weiller

  2. Department of Psychiatry and Psychotherapy, Faculty of Medicine, Medical Center-University of Freiburg, University of Freiburg, Freiburg, Germany

    Roza M. Umarova & Stefan Klöppel

  3. BrainLinks-BrainTools Cluster of Excellence, Faculty of Medicine, Medical Center-University of Freiburg, University of Freiburg, Freiburg, Germany

    Roza M. Umarova, Christoph P. Kaller, Stefan Klöppel & Cornelius Weiller

  4. Department of Neurology, Inselspital, University Hospital Bern, University of Bern, Freiburgstrasse 16, 3010, Bern, Switzerland

    Roza M. Umarova

  5. Centre of Neurology, Division of Neuropsychology, Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany

    Christoph Sperber & Hans-Otto Karnath

  6. Department of Neuroradiology, Faculty of Medicine, Medical Center-University of Freiburg, University of Freiburg, Freiburg, Germany

    Horst Urbach

  7. University Hospital of Old Age Psychiatry Bern, University of Bern, Bern, Switzerland

    Stefan Klöppel

  8. Department of Psychology, University of South Carolina, Columbia, USA

    Hans-Otto Karnath

Authors
  1. Roza M. Umarova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christoph Sperber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph P. Kaller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charlotte S. M. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Horst Urbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stefan Klöppel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cornelius Weiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hans-Otto Karnath
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RMU and SK contributed to conception; RMU, CW and CPK contributed to the study design; RMU, HU, CSMS and CW contributed to data acquisition, RMU, CS, CPK, SK and H-OK contributed to data analysis; RMU, CS and H-OK wrote the manuscript.

Corresponding author

Correspondence to Roza M. Umarova.

Ethics declarations

Conflicts of interest

Nothing to report.

Ethical standards

The Ethics Committee of the University Medical Centre Freiburg approved the study (10/2013), which was conducted according to the principles of the Declaration of Helsinki.

Informed consent

Written informed consent was obtained from each subject.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Umarova, R.M., Sperber, C., Kaller, C.P. et al. Cognitive reserve impacts on disability and cognitive deficits in acute stroke. J Neurol 266, 2495–2504 (2019). https://doi.org/10.1007/s00415-019-09442-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-019-09442-6

Keywords

Search

Navigation

-