Poststroke QEEG informs early prognostication of cognitive impairment
Emma Schleiger
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia
School of Medicine, The University of Queensland, Brisbane, Australia
Search for more papers by this authorAndrew Wong
School of Medicine, The University of Queensland, Brisbane, Australia
Acute Stroke Unit, Neurology Department, Royal Brisbane and Women's Hospital, Herston, Australia
Search for more papers by this authorStephen Read
School of Medicine, The University of Queensland, Brisbane, Australia
Search for more papers by this authorTennille Rowland
Acute Stroke Unit, Neurology Department, Royal Brisbane and Women's Hospital, Herston, Australia
Occupational Therapy Department, Royal Brisbane and Women's Hospital, Herston, Australia
Search for more papers by this authorCorresponding Author
Simon Finnigan
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia
Internal Medicine Research Unit, Royal Brisbane and Women's Hospital, Herston, Australia
Address correspondence to: Simon Finnigan, UQ Centre for Clinical Research, Royal Brisbane and Women's Hospital, Herston, Queensland 4029, Australia. E-mail: [email protected]Search for more papers by this authorEmma Schleiger
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia
School of Medicine, The University of Queensland, Brisbane, Australia
Search for more papers by this authorAndrew Wong
School of Medicine, The University of Queensland, Brisbane, Australia
Acute Stroke Unit, Neurology Department, Royal Brisbane and Women's Hospital, Herston, Australia
Search for more papers by this authorStephen Read
School of Medicine, The University of Queensland, Brisbane, Australia
Search for more papers by this authorTennille Rowland
Acute Stroke Unit, Neurology Department, Royal Brisbane and Women's Hospital, Herston, Australia
Occupational Therapy Department, Royal Brisbane and Women's Hospital, Herston, Australia
Search for more papers by this authorCorresponding Author
Simon Finnigan
The University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia
Internal Medicine Research Unit, Royal Brisbane and Women's Hospital, Herston, Australia
Address correspondence to: Simon Finnigan, UQ Centre for Clinical Research, Royal Brisbane and Women's Hospital, Herston, Queensland 4029, Australia. E-mail: [email protected]Search for more papers by this authorThis study was funded in part by the University of Queensland, the Royal Brisbane and Women's Hospital Foundation, and the National Stroke Foundation (Australia). SF was supported in part by a Career Development Award from the National Health and Medical Research Council (Australia). ES was supported by a Royal Brisbane and Women's Hospital Postgraduate Scholarship.
Abstract
Cognitive impairment is a common consequence of stroke, but remains difficult to predict. We investigate the ability of early QEEG assessment to inform such prediction, using binary logistic regression. Thirty-five patients (12 female, ages 18–87) suffering middle cerebral artery, ischemic stroke were studied. Resting-state EEG was recorded 48–239 h after symptom onset. Relative power for delta, theta, alpha, and beta bands, delta:alpha ratio, and peak alpha frequency were analyzed. Montreal Cognitive Assessment (MoCA) was administered, where possible, on day of EEG and at median 99 days (range 69–138) poststroke. Eight patients could not complete the baseline MoCA, and four the follow-up MoCA, for varying reasons (most commonly, stroke symptoms). Fifteen patients (48%) had cognitive impairment (MoCA score ≤25) at follow-up. One QEEG index was able to correctly predict presence/absence of cognitive impairment in 24/31 patients (77.4%), whereas predischarge MoCA did so in 23 patients. This index, relative theta frequency (4–7.5 Hz) power, was computed from only three posterior electrodes over the stroke-affected hemisphere. Its predictive accuracy (three electrodes) was higher than that of any “global” QEEG measure (averaged over 19 electrodes). These results may signify association between poststroke alpha slowing and cognitive impairment, which may be mediated by attentional (dys)function, which warrants further investigation. Pending further studies, QEEG measure(s)—from a few electrodes—could inform early prognostication of poststroke cognitive outcomes (and clinical decisions), particularly when cognitive function cannot be adequately assessed (due to symptoms, language, or other issues) or when assessment is equivocal.
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psyp12785-sup-0001-suppinfo1.docx16.4 KB | Table S1: Coefficients of the supplementary QEEG regression models predicting poststroke cognitive impairment. |
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References
- Angelakis, E., Lubar, J. F., Stathopoulou, S., & Kounios, J. (2004). Peak alpha frequency: An electroencephalographic measure of cognitive preparedness. Clinical Neurophysiology; 115, 887–897. doi: 10.1016/j.clinph.2003.11.034
-
Caviness, J. N.,
Hentz, J. G.,
Belden, C. M.,
Shill, H. A.,
Driver-Dunckley, E. D.,
Sabbagh, M. N.,
… Adler, C. H. (2008). Longitudinal EEG changes correlate with cognitive measure deterioration in Parkinson's disease. Journal of Parkinsons Disease, 5, 117–124. doi: 10.3233/jpd-140480
10.3233/jpd-140480 Google Scholar
- Cummins, T. D. R, Broughton, M., & Finnigan, S. (2008). Theta oscillations are affected by amnestic mild cognitive impairment and cognitive load. International Journal of Psychophysiology, 70, 75–81. doi: 10.1016/j.ijpsycho.2008.06.002
- Dong, Y., Sharma, V. K., Chan, B. P.-L, Venketasubramanian, N., Teoh, H. L., Seet, R. C. S., … Chen, C. (2010). The Montreal Cognitive Assessment (MoCA) is superior to the Mini-Mental State Examination (MMSE) for the detection of vascular cognitive impairment after acute stroke. Journal of Neurological Sciences, 299, 15–18. doi: 10.1016/j.jns.2010.08.051
- Dong, Y., Slavin, M. J., Chan, B. P., Venketasubramanian, N., Sharma, V. K, Collinson, S. L., … Chen, C. L. H. (2014). Improving screening for vascular cognitive impairment at three to six months after mild ischemic stroke and transient ischemic attack. International Psychogeriatrics, 26, 787–793.doi: 10.1017/s1041610213002457
- Dong, Y. H., Venketasubramanian, N., Chan, B. P. L., Sharma, V. K., Slavin, M. J., Collinson, S. L., … Chen, C. L. H. (2012). Brief screening tests during acute admission in patients with mild stroke are predictive of vascular cognitive impairment 3–6 months after stroke. Journal of Neurology Neurosurgery and Psychiatry, 83,: 580–585.doi: 10.1136/jnnp-2011-302070
- Finnigan, S., & Robertson, I. H. (2011). Resting EEG theta power correlates with cognitive performance in healthy older adults. Psychophysiology, 48, 1083–1087. doi: 10.1111/j.1469-8986.2010.01173.x
- Finnigan, S., & van Putten, M. J. A. M. (2013). EEG in ischaemic stroke: Quantitative EEG can uniquely inform (sub-)acute prognoses and clinical management. Clinical Neurophysiology, 124, 10–19. doi: 10.1016/j.clinph.2012.07.003
- Finnigan, S., Wong, A., & Read, S. (2016). Defining abnormal slow EEG activity in acute ischaemic stroke: Delta/alpha ratio as an optimal QEEG index. Clinical Neurophysiology, 127, 1452–1459. doi: 10.1016/j.clinph.2015.07.014
- Freitas, S., Simoes, M. R., Alves, L., Vicente, M., & Santana, I. (1994). Montreal Cognitive Assessment (MoCA): Validation study for vascular dementia. Journal of the International Neuropsychological Society, 18, 1031–1040. doi: 10.1017/s135561771200077x
- Gur, A. Y., Neufeld, M. Y., Treves, T. A., Aronovich, B. D., Bornstein, N. M., & Korczyn, A. D. (1994). EEG as predictor of dementia following first ischemic stroke. Acta Neurologica Scandinavica, 90, 263–265. doi: 10.1111/j.1600-0404.1994.tb02718.x
- Hebb, M. O, McArthur, D. L., Alger, J., Etchepare, M., Glenn, T. C., Bergsneider, M., … Vespa, P. M. (2007). Impaired percent alpha variability on continuous electroencephalography is associated with thalamic injury and predicts poor long-term outcome after human traumatic brain injury. Journal of Neurotrauma, 24, 579–590. doi: 10.1089/neu.2006.0146
- Hurford, R., Charidimou, A., Fox, Z., Cipolotti, L., & Werring, D. J. (2013). Domain-specific trends in cognitive impairment after acute ischaemic stroke. Journal of Neurology, 260, 237–241. doi: 10.1007/s00415-012-6625-0
- Juhász, C., Kamondi, A., & Szirmai, I. (1997). Spectral EEG analysis following hemispheric stroke: Evidences of transhemispheric diaschisis. Acta Neurologica Scandinavica, 96, 397–400. doi: 10.1111/j.1600-0404.1997.tb00305.x
-
Kelly-Hayes, M.,
Beiser, A.,
Kase, C. S.,
Scaramucci, A.,
D'Agostino, R. B., &
Wolf, P. A. (2003). The influence of gender and age on disability following ischemic stroke: The Framingham study. Journal of Stroke and Cerebrovascular Diseases, 12, 119–126. doi: 10.1016/s1052-3057(03)00042-9
10.1016/s1052-3057(03)00042-9 Google Scholar
- Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Research Reviews, 29, 169–195. doi: 10.1016/s0165-0173(98)00056-3
- Klimesch, W. (2012). Alpha-band oscillations, attention, and controlled access to stored information. Trends in Cognitive Sciences, 16, 606–617. doi: 10.1016/j.tics.2012.10.007
- Mathewson, K. J., Hashemi, A., Sheng, B., Sekuler, A. B., Bennett, P. J., & Schmidt, L. A. (2015). Regional electroencephalogram (EEG) alpha power and asymmetry in older adults: A study of short-term test-retest reliability. Frontiers in Aging Neuroscience, 7. doi: 10.3389/fnagi.2015.00177
- Meerwijk, E. L., Ford, J. M., & Weiss, S. J. (2015). Resting-state EEG delta power is associated with psychological pain in adults with a history of depression. Biological Psychology, 105, 106–114. doi: 10.1016/j.biopsycho.2015.01.003
- Mitchell, D. J., McNaughton, N., Flanagan, D., & Kirk, I. J. (2008). Frontal-midline theta from the perspective of hippocampal “theta.” Progress in Neurobiology, 86, 156–185. doi: 10.1016/j.pneurobio.2008.09.005
- Moretti, D. V., Babiloni, C., Binetti, G., Cassetta, E., Dal Forno, G., Ferreric, F., … Rossini, P. M. (2004) Individual analysis of EEG frequency and band power in mild Alzheimer's disease. Clinical Neurophysiology, 115, 299–308. doi: 10.1016/s1388-2457(03)00345-6
- Muresanu, D. F., Alvarez, X. A., Moessler, H., Buia, M., Stan, A., Pintea, D., … Popescu, B. O. (2008). A pilot study to evaluate the effects of cerebrolysin on cognition and qEEG in vascular dementia: Cognitive improvement correlates with qEEG acceleration. Journal of Neurological Sciences, 267, 112–119. doi: 10.1016/j.jns.2007.10.016
- Narasimhalu, K., Ang, S., De Silva, D. A., Wong, M. C., Chang, H. M., Chia, K. S., … Chen, C. (2009). Severity of CIND and MCI predict incidence of dementia in an ischemic stroke cohort. Neurology, 73, 1866–1872. doi: 10.1212/WNL.0b013e3181c3fcb7
- Nasreddine, Z. S., Phillips, N. A., Bedirian, V., Charbonneau, S., Whitehead, V., Collin, I., … Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53, 695–699. doi: 10.1111/j.1532-5415.2005.53221.x
- Niedermeyer, E., & Da Silva, F. L. (2005). Electroencephalography: Basic principles, clinical applications, and related fields ( 5th ed.). Philadelphia, PA: Lippincott, Williams & Wilkins.
- Novak, P., Lepicovska, V., & Dostalek, C. (1992). Periodic amplitude modulation of EEG. Neuroscience Letters, 136, 213–215. doi: 10.1016/0304-3940(92)90051-8
- Nuwer, M. R., Hovda, D. A., Schrader, L. M., & Vespa, P. M. (2005). Routine and quantitative EEG in mild traumatic brain injury. Clinical Neurophysiology, 116, 2001–2025. doi: 10.1016/j.clinph.2005.05.008
- Pendlebury, S. T., Cuthbertson, F. C., Welch, S. J. V., Mehta, Z., & Rothwell, P. M. (2010). Underestimation of cognitive impairment by Mini-Mental State Examination versus the Montreal Cognitive Assessment in patients with transient ischemic attack and stroke: A population-based study. Stroke, 41, 1290–1293. doi: 10.1161/strokeaha.110.579888
- Pendlebury, S. T., Mariz, J., Bull, L., Mehta, Z., & Rothwell, P. M. (2012). MoCA, ACE-R, and MMSE versus the National Institute of Neurological Disorders and Stroke–Canadian Stroke Network Vascular Cognitive Impairment Harmonization Standards: Neuropsychological Battery after TIA and stroke. Stroke, 43, 464–469. doi: 10.1161/strokeaha.111.633586
- Robertson, I. H., Ridgeway, V., Greenfield, E., & Parr, A. (1997). Motor recovery after stroke depends on intact sustained attention: A 2-year follow-up study. Neuropsychology, 11, 290–295. doi: 10.1037/0894-4105.11.2.290
- Schleiger, E., Sheikh, N., Rowland, T., Wong, A., Read, S., & Finnigan, S. (2014). Frontal EEG delta/alpha ratio and screening for post-stroke cognitive deficits: The power of four electrodes. International Journal of Psychophysiology, 94, 19–24. doi: 10.1016/j.ijpsycho.2014.06.012
- Song, Y., Zang, D. W., Jin, Y. Y., Wang, Z. J., Ni, H. Y., Yin, J. Z., & Ji, D. X. (2014). Background rhythm frequency and theta power of quantitative EEG analysis: Predictive biomarkers for cognitive impairment post-cerebral infarcts. Clinical EEG and Neuroscience, 46(2), 142–147, doi: 10.1177/1550059413517492
- Srikanth, V. K., Thrift, A. G., Saling, M. M., Anderson, J. F. I., Dewey, H. M., Macdonell, R. A. L., & Donnan, G. A. (2003). Increased risk of cognitive impairment 3 months after mild to moderate first-ever stroke: A community-based prospective study of nonaphasic English-speaking survivors. Stroke, 34, 1136–1143. doi: 10.1161/01.str.0000069161.35736.39
- van der Kooi, A. W., Zaal, I. J., Klijn, F. A., Koek, H. L., Meijer, R. C., Leijten, F. S., & Slooter, A. J. (2015). Delirium detection using EEG: What and how to measure. Chest, 147, 94–101. doi: 10.1378/chest.13-3050
- Vespa, P. M., Boscardin, W. J., Hovda, D. A., McArthur, D. L., Nuwer, M. R., Martin, N. A., … Becker, D. P. (2002). Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. Journal of Neurosurgery, 97, 84–92. doi: 10.3171/jns.2002.97.1.0084
- Yuasa, T., Maeda, A., Higuchi, S., & Motohashi Y. (2001). Quantitative EEG data and comprehensive ADL (activities of daily living) evaluation of stroke survivors residing in the community. Journal of Physiological Anthropology and Applied Human Science, 20, 37–41. doi: 10.2114/jpa.20.37