Longitudinal quantitative electroencephalographic study in mono-hemispheric stroke patients
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摘要
The identification of individual factors modulating clinical recovery after a stroke is fundamental to personalize the therapeutic intervention to enhance the final clinical outcome.In this framework,electrophysiological factors are promising since are more directly related to neuroplasticity,which supports recovery in stroke patients,than neurovascular factors.In this retrospective observational study,we investigated brain neuronal activity assessed via spectral features and Higuchi's fractal dimension(HFD) of electroencephalographic signals in acute phase(2–10 days from symptom onset,T0) and sub-acute phase(2.5 months,T1) in 24 patients affected by unilateral middle cerebral artery stroke.Longitudinal assessment of the clinical deficits was performed using the National Institutes of Health Stroke Scale(NIHSS),together with the effective recovery calculated as the ratio between difference of NIHSS at T0 and T1 over the NIHSS value at T0.We observed that delta and alpha band electroencephalographic signal power changed between the two phases in both the hemispheres ipsilateral(ILH) and contralateral(CHL) to the lesion.Moreover,at T0,bilateral higher delta band power correlated with worse clinical conditions(Spearman's rs = 0.460,P = 0.027 for ILH and rs = 0.508,P = 0.013 for CLH),whereas at T1 this occurred only for delta power in ILH(rs = 0.411,P = 0.046) and not for CHL.Inter-hemispheric difference(ILH vs.CLH) of alpha power in patients was lower at T0 than at T1(P = 0.020).HFD at T0 was lower than at T1(P = 0.005),and at both phases,ILH HFD was lower than CLH HFD(P = 0.020).These data suggest that inter-hemispheric low band asymmetry and fractal dimension changes from the acute to the sub-acute phase are sensitive to neuroplasticity processes which subtend clinical recovery.The study protocol was approved by the Bioethical Committee of Ospedale San Giovanni Calibita Fatebenefretelli(No.40/2011) on July 14,2011.
The identification of individual factors modulating clinical recovery after a stroke is fundamental to personalize the therapeutic intervention to enhance the final clinical outcome.In this framework,electrophysiological factors are promising since are more directly related to neuroplasticity,which supports recovery in stroke patients,than neurovascular factors.In this retrospective observational study,we investigated brain neuronal activity assessed via spectral features and Higuchi's fractal dimension(HFD) of electroencephalographic signals in acute phase(2–10 days from symptom onset,T0) and sub-acute phase(2.5 months,T1) in 24 patients affected by unilateral middle cerebral artery stroke.Longitudinal assessment of the clinical deficits was performed using the National Institutes of Health Stroke Scale(NIHSS),together with the effective recovery calculated as the ratio between difference of NIHSS at T0 and T1 over the NIHSS value at T0.We observed that delta and alpha band electroencephalographic signal power changed between the two phases in both the hemispheres ipsilateral(ILH) and contralateral(CHL) to the lesion.Moreover,at T0,bilateral higher delta band power correlated with worse clinical conditions(Spearman's rs = 0.460,P = 0.027 for ILH and rs = 0.508,P = 0.013 for CLH),whereas at T1 this occurred only for delta power in ILH(rs = 0.411,P = 0.046) and not for CHL.Inter-hemispheric difference(ILH vs.CLH) of alpha power in patients was lower at T0 than at T1(P = 0.020).HFD at T0 was lower than at T1(P = 0.005),and at both phases,ILH HFD was lower than CLH HFD(P = 0.020).These data suggest that inter-hemispheric low band asymmetry and fractal dimension changes from the acute to the sub-acute phase are sensitive to neuroplasticity processes which subtend clinical recovery.The study protocol was approved by the Bioethical Committee of Ospedale San Giovanni Calibita Fatebenefretelli(No.40/2011) on July 14,2011.
The identification of individual factors modulating clinical recovery after a stroke is fundamental to personalize the therapeutic intervention to enhance the final clinical outcome.In this framework,electrophysiological factors are promising since are more directly related to neuroplasticity,which supports recovery in stroke patients,than neurovascular factors.In this retrospective observational study,we investigated brain neuronal activity assessed via spectral features and Higuchi's fractal dimension(HFD) of electroencephalographic signals in acute phase(2–10 days from symptom onset,T0) and sub-acute phase(2.5 months,T1) in 24 patients affected by unilateral middle cerebral artery stroke.Longitudinal assessment of the clinical deficits was performed using the National Institutes of Health Stroke Scale(NIHSS),together with the effective recovery calculated as the ratio between difference of NIHSS at T0 and T1 over the NIHSS value at T0.We observed that delta and alpha band electroencephalographic signal power changed between the two phases in both the hemispheres ipsilateral(ILH) and contralateral(CHL) to the lesion.Moreover,at T0,bilateral higher delta band power correlated with worse clinical conditions(Spearman's rs = 0.460,P = 0.027 for ILH and rs = 0.508,P = 0.013 for CLH),whereas at T1 this occurred only for delta power in ILH(rs = 0.411,P = 0.046) and not for CHL.Inter-hemispheric difference(ILH vs.CLH) of alpha power in patients was lower at T0 than at T1(P = 0.020).HFD at T0 was lower than at T1(P = 0.005),and at both phases,ILH HFD was lower than CLH HFD(P = 0.020).These data suggest that inter-hemispheric low band asymmetry and fractal dimension changes from the acute to the sub-acute phase are sensitive to neuroplasticity processes which subtend clinical recovery.The study protocol was approved by the Bioethical Committee of Ospedale San Giovanni Calibita Fatebenefretelli(No.40/2011) on July 14,2011.
引文
Ahmed I(1988)Predictive value of the electroencephalogram in acute hemispheric lesions.Clin Electroencephalogr 19:205-209.
Aminov A,Rogers JM,Johnstone SJ,Middleton S,Wilson PH(2017)Acute single channel EEG predictors of cognitive function after stroke.PLoS One 12:e0185841.
Amzica F,Steriade M(1995)Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation.J Neurosi15:4658-4677.
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Assenza G,Zappasodi F,Pasqualetti P,Vernieri F,Tecchio F(2013)Acontralesional EEG power increase mediated by interhemispheric disconnection provides negative prognosis in acute stroke.Restor Neurol Neurosci 31:177-188.
Assenza G,Di Lazzaro V(2015)A useful electroencephalography(EEG)marker of brain plasticity:delta waves.Neural Regen Res 10:1216-1217.
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Barbati G,Porcaro C,Zappasodi F,Rossini PM,Tecchio F(2004)Optimization of ICA approach for artifact identification and removal in MEG signals.Clin Neurophys 115:1220-1232.
Bernhardt J,Dewey H,Collier J,Thrift A,Lindley R,Moodie M,Donnan G(2006)A very early rehabilitation trial(AVERT).Int J Stroke1:169-171.
Blatow M,Rozov A,Katona I,Hormuzdi SG,Meyer AH,Whittington MA,Caputi A,Monyer H(2003)A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex.Neuron 38:805-817.
Butz M,Gross J,Timmermann L,Moll M,Freund HJ,Witte OW,Schnitzler A(2004)Perilesional pathological oscillatory activity in the magnetoencephalogram of patients with cortical brain lesions.Neurosci Lett 355:93-96.
Buzsaki G,Mizuseki K(2014)The log-dynamic brain:how skewed distributions affect network operations.Nat Rev Neurosci 15:264-278.
Calautti C,Leroy F,Guincestre JY,MariéRM,Baron JC(2001)Sequential activation brain mapping after subcortical stroke:changes in hemispheric balance and recovery.Neuroreport 12:3883-3886.
Carrera E,Tononi G(2014)Diaschisis:past,present,future.Brain137:2408-2422.
Carter AR,Astafiev SV,Lang CE,Connor LT,Rengachary J,Strube MJ,Pope DL,Shulman GL,Corbetta M(2010)Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke.Ann Neurol 67:365-375.
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Di Pino G,Pellegrino G,Assenza G,Capone F,Ferreri F,Formica D,Ranieri F,Tombini M,Ziemann U,Rothwell JC,Di Lazzaro V(2014)Modulation of brain plasticity in stroke:a novel model for neurorehabilitation.Nat Rev Neurol 10:597-608.
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Finnigan S,Wong A,Read S(2016)Defining abnormal slow EEGactivity in acute ischaemic stroke:Delta/alpha ratio as an optimal QEEG index.Clin Neurophysiol 127:1452-1459.
Finnigan SP,Rose SE,Chalk JB(2008)Contralateral hemisphere delta EEG in acute stroke precedes worsening of symptoms and death.Clin Neurophysiol 119:1690-1694.
Garrett DD,Samanez-Larkin GR,MacDonald SW,Lindenberger U,McIntosh AR,Grady CL(2013)Moment-to-moment brain signal variability:A next frontier in human brain mapping?Neurosci Biobehav Rev 37:610-624.
Giovanni A,Capone F,di Biase L,Ferreri F,Florio L,Guerra A,Marano M,Paolucci M,Ranieri F,Salomone G,Tombini M,Thut G,Di Lazzaro V(2018)Oscillatory activities in neurological disorders of elderly:biomarkers to target for neuromodulation.Front Aging Neurosci 9:189.
Graziadio S,Tomasevic L,Assenza G,Tecchio F,Eyre JA(2013)The myth of the‘unaffected’side after unilateral stroke:Is reorganisation of the non-infarcted corticospinal system to re-establish balance the price for recovery?Exp Neurol 238:168-175.
Harmony T,Fernández-Bouzas A,Marosi E,Fernández T,Valdés P,Bosch J,Riera J,Jackel RA,Harner RN(1989)Computed EEG topography in acute stroke.Neurophysiol Clin 19:185-197.
He BJ(2011)Scale-free properties of the functional magnetic resonance imaging signal during rest and task.J Neurosci 31:13786-13795.
Higuchi T(1988)Approach to an irregular time series on the basis of the fractal theory.Physica D 31:277-283.
Jackel RA,Harner RN(1989)Computed EEG topography in caute stroke.Neurophysiol Clin 19:185-197.
Juhász C,Kamondi A,Szirmai I(1997)Spectral EEG analysis following hemispheric stroke:evidences of transhemispheric diaschisis.Acta Neurol Scand 96:397-400.
Lagreze HL,Levine RL,Pedula KL,Nickles RJ,Sunderland JS,Rowe BR(1987)Contralateral flow reduction in unilateral stroke:evidence for transhemispheric diaschisis.Stroke 18:882-886.
Leon-Carrion J,Martin-Rodriguez JF,Damas-Lopez J,Barroso y Martin JM,Dominguez-Morales MR(2009)Delta-alpha ratio correlates with level of recovery after neurorehabilitation in patients with acquired brain injury.Clin Neurophysiol 120:1039-1045.
Machado C,Cuspineda E,Valdés P,Virues T,Llopis F,Bosch J,Aubert E,Hernández E,Pando A,Alvarez MA,Barroso E,Galán L,Avila Y(2004)Assessing acute middle cerebral artery ischemic stroke by quantitative electric tomography.Clin EEG Neurosci 35:116-124.
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Marzetti L,Nolte G,Perrucci MG,Romani GL,Del Gratta C(2007)The use of standardized infinity reference in EEG coherency studies.Neuroimage 15:48-63.
Melamed E,Lavy S,Portnoy Z,Sadan S,Carmon A(1975)Correlation between regional cerebral blood flow and EEG frequency in the contralateral hemisphere in acute cerebral infarction.J Neurol Sci 26:21-27.
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National Institute of Health,National Institute of Neurological Disorders and Stroke.Stroke Scale.https://www.ninds.nih.gov/sites/default/files/NIH_Stroke_Scale_Booklet.pdf.Accessed December 2,2018.
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Assenza G,Zappasodi F,Squitti R,Altamura C,Ventriglia M,Ercolani M,Quattrocchi CC,Lupoi D,Passarelli F,Vernieri F,Rossini PM,Tecchio F(2009)Neuronal functionality assessed by magnetoencephalography is related to oxidative stress system in acute ischemic stroke.NeuroImage 44:1267-1273.
Assenza G,Zappasodi F,Pasqualetti P,Vernieri F,Tecchio F(2013)Acontralesional EEG power increase mediated by interhemispheric disconnection provides negative prognosis in acute stroke.Restor Neurol Neurosci 31:177-188.
Assenza G,Di Lazzaro V(2015)A useful electroencephalography(EEG)marker of brain plasticity:delta waves.Neural Regen Res 10:1216-1217.
Baldassarre A,Ramsey LE,Siegel JS,Shulman GL,Corbetta M(2016)Brain connectivity and neurological disorders after stroke.Curr Opin Neurol 29:706-713.
Barbati G,Porcaro C,Zappasodi F,Rossini PM,Tecchio F(2004)Optimization of ICA approach for artifact identification and removal in MEG signals.Clin Neurophys 115:1220-1232.
Bernhardt J,Dewey H,Collier J,Thrift A,Lindley R,Moodie M,Donnan G(2006)A very early rehabilitation trial(AVERT).Int J Stroke1:169-171.
Blatow M,Rozov A,Katona I,Hormuzdi SG,Meyer AH,Whittington MA,Caputi A,Monyer H(2003)A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex.Neuron 38:805-817.
Butz M,Gross J,Timmermann L,Moll M,Freund HJ,Witte OW,Schnitzler A(2004)Perilesional pathological oscillatory activity in the magnetoencephalogram of patients with cortical brain lesions.Neurosci Lett 355:93-96.
Buzsaki G,Mizuseki K(2014)The log-dynamic brain:how skewed distributions affect network operations.Nat Rev Neurosci 15:264-278.
Calautti C,Leroy F,Guincestre JY,MariéRM,Baron JC(2001)Sequential activation brain mapping after subcortical stroke:changes in hemispheric balance and recovery.Neuroreport 12:3883-3886.
Carrera E,Tononi G(2014)Diaschisis:past,present,future.Brain137:2408-2422.
Carter AR,Astafiev SV,Lang CE,Connor LT,Rengachary J,Strube MJ,Pope DL,Shulman GL,Corbetta M(2010)Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke.Ann Neurol 67:365-375.
Cramer SC(2010)Stratifying patients with stroke in trials that target brain repair.Stroke 41(10 Suppl):S114-116.
Crichton SL,Bray BD,McKevitt C,Rudd AG,Wolfe CDA(2016)Patient outcomes up to 15 years after stroke:survival,disability,quality of life,cognition and mental health.J Neurol Neurosurg Psychiatry 87:1091-1098.
Di Ieva A,Grizzi F,Jelinek H,Pellionisz AJ,Losa GA(2014)Fractals in the Neurosciences,Part I:General Principles and Basic Neurosciences.Neuroscientist 20:403-417.
Di Lazzaro V,Profice P,Pilato F,Capone F,Ranieri F,Pasqualetti P,Colosimo C,PravatàE,Cianfoni A,Dileone M(2010)Motor cortex plasticity predicts recovery in acute stroke.Cereb Cortex 20:1523-1528.
Di Pino G,Pellegrino G,Assenza G,Capone F,Ferreri F,Formica D,Ranieri F,Tombini M,Ziemann U,Rothwell JC,Di Lazzaro V(2014)Modulation of brain plasticity in stroke:a novel model for neurorehabilitation.Nat Rev Neurol 10:597-608.
Dromerick AW,Reding MJ(1995)Functional outcome for patients with hemiparesis,hemihyposthesia and hemianopsia.Stroke11:2023-2026.
Fanciullacci C,Bertolucci F,Lamola G,Panarese A,Artoni F,Micera S,Rossi B,Chisari C(2017)Delta power is higher and more symmetrical in ischemic stroke patients with cortical involvement.Front Hum Neurosci 11:385.
Fernandez-Bouzas A,Harmony T,Fernandez T,Silva-Pereyra J,Valdes P,Bosch J,Aubert E,Casián G,Otero Ojeda G,Ricardo J,Hernández-Ballesteros A,Santiago E(2000)Sources of abnormal EEG activity in brain infarctions.Clin Electroencephalogr 31:165-169.
Finnigan S,Wong A,Read S(2016)Defining abnormal slow EEGactivity in acute ischaemic stroke:Delta/alpha ratio as an optimal QEEG index.Clin Neurophysiol 127:1452-1459.
Finnigan SP,Rose SE,Chalk JB(2008)Contralateral hemisphere delta EEG in acute stroke precedes worsening of symptoms and death.Clin Neurophysiol 119:1690-1694.
Garrett DD,Samanez-Larkin GR,MacDonald SW,Lindenberger U,McIntosh AR,Grady CL(2013)Moment-to-moment brain signal variability:A next frontier in human brain mapping?Neurosci Biobehav Rev 37:610-624.
Giovanni A,Capone F,di Biase L,Ferreri F,Florio L,Guerra A,Marano M,Paolucci M,Ranieri F,Salomone G,Tombini M,Thut G,Di Lazzaro V(2018)Oscillatory activities in neurological disorders of elderly:biomarkers to target for neuromodulation.Front Aging Neurosci 9:189.
Graziadio S,Tomasevic L,Assenza G,Tecchio F,Eyre JA(2013)The myth of the‘unaffected’side after unilateral stroke:Is reorganisation of the non-infarcted corticospinal system to re-establish balance the price for recovery?Exp Neurol 238:168-175.
Harmony T,Fernández-Bouzas A,Marosi E,Fernández T,Valdés P,Bosch J,Riera J,Jackel RA,Harner RN(1989)Computed EEG topography in acute stroke.Neurophysiol Clin 19:185-197.
He BJ(2011)Scale-free properties of the functional magnetic resonance imaging signal during rest and task.J Neurosci 31:13786-13795.
Higuchi T(1988)Approach to an irregular time series on the basis of the fractal theory.Physica D 31:277-283.
Jackel RA,Harner RN(1989)Computed EEG topography in caute stroke.Neurophysiol Clin 19:185-197.
Juhász C,Kamondi A,Szirmai I(1997)Spectral EEG analysis following hemispheric stroke:evidences of transhemispheric diaschisis.Acta Neurol Scand 96:397-400.
Lagreze HL,Levine RL,Pedula KL,Nickles RJ,Sunderland JS,Rowe BR(1987)Contralateral flow reduction in unilateral stroke:evidence for transhemispheric diaschisis.Stroke 18:882-886.
Leon-Carrion J,Martin-Rodriguez JF,Damas-Lopez J,Barroso y Martin JM,Dominguez-Morales MR(2009)Delta-alpha ratio correlates with level of recovery after neurorehabilitation in patients with acquired brain injury.Clin Neurophysiol 120:1039-1045.
Machado C,Cuspineda E,Valdés P,Virues T,Llopis F,Bosch J,Aubert E,Hernández E,Pando A,Alvarez MA,Barroso E,Galán L,Avila Y(2004)Assessing acute middle cerebral artery ischemic stroke by quantitative electric tomography.Clin EEG Neurosci 35:116-124.
Makela JP,Salmelin R,Kotila M,Salonen O,Laaksonen R,Hokkanen L,Hari R(1998)Modification of neuromagnetic cortical signals by thalamic infarctions.Electroencephalogr Clin Neurophysiol 106:433-443.
Marzetti L,Nolte G,Perrucci MG,Romani GL,Del Gratta C(2007)The use of standardized infinity reference in EEG coherency studies.Neuroimage 15:48-63.
Melamed E,Lavy S,Portnoy Z,Sadan S,Carmon A(1975)Correlation between regional cerebral blood flow and EEG frequency in the contralateral hemisphere in acute cerebral infarction.J Neurol Sci 26:21-27.
Murri L,Gori S,Massetani R,Bonanni E,Marcella F,Milani S(1998)Evaluation of acute ischemic stroke using quantitative EEG:a comparison with conventional EEG and CT scan.Neurophysiol Clin28:249-257.
Nagata K,Mizukami M,Araki G,Kawase T,Hirano M(1982)Topographic electroencephalographic study of cerebral infarction using computed mapping of the EEG.J Cereb Blood Flow Metab 2:79-88.
National Institute of Health,National Institute of Neurological Disorders and Stroke.Stroke Scale.https://www.ninds.nih.gov/sites/default/files/NIH_Stroke_Scale_Booklet.pdf.Accessed December 2,2018.
Niedermeyer E(1997)Cerebrovascular disorders and EEG.In:Electroencephalography:Basic Principles,Clinical Applications and Related Fields,4th ed(Niedermeyer E,Lopes Da Silva F,eds),pp320-321.Oxford,UK:Oxford University Press.
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