Cortical thinning is associated with disease stages and dementia in Parkinson's disease

Objective To investigate the pattern of cortical thinning in Parkinson's disease (PD) across different disease stages and to elucidate to what extent cortical thinning is related to cognitive impairment. Design Ninety-six subjects including 39 controls and 57 PD patients participated in this study. PD subjects were divided into three groups (early, n=24; moderate, n=18; with dementia, n=15). High field structural brain MRI images were acquired in a 3T scanner and analyses of cortical thickness and surface were carried out. Vertex-wise group comparisons were performed and cortical thickness was correlated with motor and cognitive measures. Results We found a positive correlation between Mini-Mental State Examination scores and cortical thickness in the anterior temporal, dorsolateral prefrontal, posterior cingulate, temporal fusiform and occipitotemporal cortex. Unified Parkinson's Disease Rating Scale-III (motor subsection) scores showed a robust negative correlation with caudate volumes. We found that disease stage in PD was associated with thinning of the medial frontal (premotor and supplementary motor cortex), posterior cingulate, precuneus, lateral occipital, temporal and dorsolateral prefrontal cortex. Discriminant analysis and a receiver operating characteristics approach showed that mean cortical thickness and hippocampus volume have 80% accuracy in identifying PD patients with dementia. PD stage and PD dementia can be characterised by a specific pattern of cortical thinning. Conclusions We conclude that measuring cortical thickness can be useful in assessing disease stage and cognitive impairment in patients with PD. In addition, cortical thickness may be useful in identifying dementia in PD.

[1]  Bruce Fischl,et al.  Cerebral cortex and the clinical expression of Huntington's disease: complexity and heterogeneity. , 2008, Brain : a journal of neurology.

[2]  W. Poewe,et al.  Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: Status and recommendations The Movement Disorder Society Task Force on rating scales for Parkinson's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[3]  E. Perry,et al.  Differences in neuropathologic characteristics across the Lewy body dementia spectrum , 2006, Neurology.

[4]  Nuria Bargallo,et al.  Assessment of cortical degeneration in patients with Parkinson's disease by voxel‐based morphometry, cortical folding, and cortical thickness , 2012, Human brain mapping.

[5]  I. McKeith,et al.  SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders , 2003, Movement disorders : official journal of the Movement Disorder Society.

[6]  H. Braak,et al.  Staging of brain pathology related to sporadic Parkinson’s disease , 2003, Neurobiology of Aging.

[7]  André J. W. van der Kouwe,et al.  Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast , 2009, NeuroImage.

[8]  A. Siderowf,et al.  Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease , 2009, Neurology.

[9]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[10]  J. Morris,et al.  Differential effects of aging and Alzheimer's disease on medial temporal lobe cortical thickness and surface area , 2009, Neurobiology of Aging.

[11]  F. Piras,et al.  Regional cortical thickness and cognitive functions in non‐demented Parkinson’s disease patients: a pilot study , 2012, European journal of neurology.

[12]  Dag Aarsland,et al.  Parkinson Disease With Dementia: Comparing Patients With and Without Alzheimer Pathology , 2009, Alzheimer disease and associated disorders.

[13]  P. Moberg,et al.  Neurodegeneration across stages of cognitive decline in Parkinson disease. , 2011, Archives of neurology.

[14]  Chul Hyoung Lyoo,et al.  Topographical distribution of cerebral cortical thinning in patients with mild Parkinson's disease without dementia , 2010, Movement disorders : official journal of the Movement Disorder Society.

[15]  Constantinos Kallis,et al.  Lewy- and Alzheimer-type pathologies in Parkinson's disease dementia: which is more important? , 2011, Brain : a journal of neurology.

[16]  A. Lees,et al.  Parkinson's Disease Society Brain Bank, London: overview and research. , 1993, Journal of neural transmission. Supplementum.

[17]  Udo Rüb,et al.  Where Does Parkinson Disease Pathology Begin in the Brain? , 2002, Journal of neuropathology and experimental neurology.

[18]  E. Tolosa,et al.  Brain structural MRI correlates of cognitive dysfunctions in Parkinson's disease , 2011, Journal of the Neurological Sciences.

[19]  E. Tolosa,et al.  Neuroanatomical correlates of impaired decision‐making and facial emotion recognition in early Parkinson’s disease , 2009, The European journal of neuroscience.

[20]  Alan C. Evans,et al.  Patterns of cortical thickness and surface area in early Parkinson's disease , 2011, NeuroImage.

[21]  C. Davatzikos,et al.  Alzheimer's disease pattern of brain atrophy predicts cognitive decline in Parkinson's disease. , 2012, Brain : a journal of neurology.

[22]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[23]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  T. Robbins,et al.  Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. , 2007, Brain : a journal of neurology.

[25]  G. Halliday,et al.  The Sydney multicenter study of Parkinson's disease: The inevitability of dementia at 20 years , 2008, Movement disorders : official journal of the Movement Disorder Society.

[26]  H. Braak,et al.  Pathology associated with sporadic Parkinson's disease--where does it end? , 2006, Journal of neural transmission. Supplementum.

[27]  G. Halliday,et al.  The progression of pathology in longitudinally followed patients with Parkinson’s disease , 2008, Acta Neuropathologica.

[28]  E. Tolosa,et al.  Cerebrospinal tau, phospho‐tau, and beta‐amyloid and neuropsychological functions in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[29]  H. Braak,et al.  Staging of Sporadic Parkinson Disease-Related α-Synuclein Pathology: Inter- and Intra-Rater Reliability , 2005, Journal of neuropathology and experimental neurology.

[30]  E. Tolosa,et al.  Grey matter volume correlates of cerebrospinal markers of Alzheimer-pathology in Parkinson's disease and related dementia. , 2012, Parkinsonism & related disorders.

[31]  Hans J. Johnson,et al.  Cerebral cortex structure in prodromal Huntington disease , 2010, Neurobiology of Disease.

[32]  D. Aarsland,et al.  Prevalence and characteristics of dementia in Parkinson disease: an 8-year prospective study. , 2003, Archives of neurology.

[33]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[34]  E. Tolosa,et al.  MRI and cognitive impairment in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[35]  Jaime Kulisevsky,et al.  Parkinson's disease‐cognitive rating scale: A new cognitive scale specific for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[36]  H. Braak,et al.  Cognitive status correlates with neuropathologic stage in Parkinson disease , 2005, Neurology.