Advertisement
Research Article| Volume 398, P31-38, March 15, 2019

Cortical thinning across Parkinson's disease stages and clinical correlates

  • Heather Wilson
    Affiliations
    Neurodegeneration Imaging Group, Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
    Search for articles by this author
  • Flavia Niccolini
    Affiliations
    Neurodegeneration Imaging Group, Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
    Search for articles by this author
  • Clelia Pellicano
    Affiliations
    Department of Neuroscience, Mental Health and Secnsory Organs-(NESMOS), Sapienza University, Rome, Italy
    Search for articles by this author
  • Marios Politis
    Correspondence
    Corresponding author at: Neurodegeneration Imaging Group, Maurice Wohl Clinical Neuroscience Institute, 125 Coldharbour Lane, Camberwell, London SE5 9NU, UK.
    Affiliations
    Neurodegeneration Imaging Group, Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
    Search for articles by this author
Published:January 17, 2019DOI:https://doi.org/10.1016/j.jns.2019.01.020

      Highlights

      • Progressive cortical thinning and subcortical volumetric loss with increasing disease severity in PD.
      • Morphometric changes are associated with disease duration and motor symptom severity.
      • Morphometric changes are associated with lower MMSE scores.
      • Subclinical changes could contribute towards future development of cognitive decline.
      • Topographic patterns of cortical thinning could act as marker of disease severity and cognitive dysfunction.

      Abstract

      Background

      Imaging studies have revealed cortical thinning and subcortical atrophy occurring in Parkinson's disease (PD); however, the topographical distribution and clinical associations related to advancing stages of PD remains unclear.

      Objective

      We aimed to investigate the topographical distribution of cortical and subcortical morphometric changes, and their clinical associations, related to increasing disease severity.

      Methods

      In this cross-sectional imaging study, T1-weighted structural magnetic resonance imaging data for 80 non-demented PD patients and 30 age-matched healthy controls were analysed using FreeSurfer software suite to derive morphometric changes using whole-brain vertex-wise analysis, and surface-based (cortical) and volume-based (subcortical) parcellation maps. PD patients were divided into three groups of mild (n = 27), moderate (n = 27), and severe (n = 26) PD based disease duration and Hoehn and Yahr and Unified Parkinson's Disease Rating Scale Part-III motor severity scores.

      Results

      Whole-brain vertex-wise analysis revealed cortical thinning in the orbitofrontal cortex in early PD (P = .011), and in the superior frontal (P = .002), caudal middle frontal gyrus (P = .001) and inferior parietal cortex (P = .006) in moderate PD. Severe PD patients showed additional cortical thinning in temporal and occipital cortices (P < .005). Subcortical volume loss was detected in the thalamus (P = .012) and hippocampus (P = .032) in moderate PD, which extended to the caudate (P = .012), putamen (P = .042) and amygdala (P = .008) in severe PD. Increasing disease duration and motor severity scores, correlated with cortical thinning in frontal, temporal, parietal and occipital cortices, and subcortical volumetric loss in the thalamus, caudate, putamen, amygdala and hippocampus. Lower global cognitive status, measured with MMSE, correlated with cortical thinning in temporal, parietal, frontal and cingulate cortices, and with volumetric loss in the hippocampus (r = 0.31; P = .009); suggesting subclinical pathogenic changes occur prior to the onset of cognitive impairment.

      Conclusion

      In conclusion, in more severe disease stages PD patients exhibit progressive cortical thinning and subcortical volume loss which could have relevance to the development of cognitive impairment.

      Keywords

      Abbreviations:

      H&Y (Hoehn and Yahr), MRI (magnetic resonance imaging), MMSE (Mini Mental State Examination), PD (Parkinson's disease), UPDRS (Unified Parkinson's Disease Rating Scale)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Neurological Sciences
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Hely M.A.
        • et al.
        The Sydney multicenter study of Parkinson's disease: the inevitability of dementia at 20 years.
        Mov. Disord. 2008; 23: 837-844
        • Braak H.
        • et al.
        Staging of brain pathology related to sporadic Parkinson's disease.
        Neurobiol. Aging. 2003; 24: 197-211
        • Burton E.J.
        • et al.
        Cerebral atrophy in Parkinson's disease with and without dementia: a comparison with Alzheimer's disease, dementia with Lewy bodies and controls.
        Brain. 2004; 127: 791-800
        • Ibarretxe-Bilbao N.
        • et al.
        Progression of cortical thinning in early Parkinson's disease.
        Mov. Disord. 2012; 27: 1746-1753
        • Jubault T.
        • et al.
        Patterns of cortical thickness and surface area in early Parkinson's disease.
        NeuroImage. 2011; 55: 462-467
        • Mak E.
        • et al.
        Baseline and longitudinal grey matter changes in newly diagnosed Parkinson's disease: ICICLE-PD study.
        Brain. 2015; 138: 2974-2986
        • Pereira J.B.
        • et al.
        Aberrant cerebral network topology and mild cognitive impairment in early Parkinson's disease.
        Hum. Brain Mapp. 2015; 36: 2980-2995
        • Segura B.
        • et al.
        Cortical thinning associated with mild cognitive impairment in Parkinson's disease.
        Mov. Disord. 2014; 29: 1495-1503
        • Zarei M.
        • et al.
        Cortical thinning is associated with disease stages and dementia in Parkinson's disease.
        J. Neurol. Neurosurg. Psychiatry. 2013; 84: 875-881
        • Pereira J.B.
        • et al.
        Initial cognitive decline is associated with cortical thinning in early Parkinson disease.
        Neurology. 2014; 82: 2017-2025
        • Litvan I.
        • et al.
        Diagnostic criteria for mild cognitive impairment in Parkinson's disease: movement disorder society task force guidelines.
        Mov. Disord. 2012; 27: 349-356
        • Dubois B.
        • et al.
        Diagnostic procedures for Parkinson's disease dementia: recommendations from the movement disorder society task force.
        Mov. Disord. 2007; 22: 2314-2324
        • Beck A.
        • Steer R.
        • Brown G.
        Beck Depression Inventory-II (BDI-II): Manual for Beck Depression Inventory-II.
        Pearson, 1993
        • Cummings J.
        • et al.
        The neuropsychiatric inventory: comprehensive assessment of psychopathology in dementia.
        Neurology. 1994; 44: 2308-2314
        • Fischl B.
        • et al.
        Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain.
        Neuron. 2002; 33: 341-355
        • Malone I.B.
        • et al.
        Accurate automatic estimation of total intracranial volume: a nuisance variable with less nuisance.
        NeuroImage. 2015; 104: 366-372
        • Benjamini Y.
        • Hochberg Y.
        Controlling the false discovery rate: a practical and powerful approach to multiple testing.
        J. R. Stat. Soc. 1995; 57: 289-300
        • Lyoo C.H.
        • Ryu Y.H.
        • Lee M.S.
        Topographical distribution of cerebral cortical thinning in patients with mild Parkinson's disease without dementia.
        Mov. Disord. 2010; 25: 496-499
        • Madhyastha T.M.
        • et al.
        Cerebral perfusion and cortical thickness indicate cortical involvement in mild Parkinson's disease.
        Mov. Disord. 2015; 30: 1893-1900
        • Pagonabarraga J.
        • et al.
        Pattern of regional cortical thinning associated with cognitive deterioration in Parkinson's disease.
        PLoS ONE. 2013; 8: e54980
        • Pereira J.B.
        • et al.
        Assessment of cortical degeneration in patients with Parkinson's disease by voxel-based morphometry, cortical folding, and cortical thickness.
        Hum. Brain Mapp. 2012; 33: 2521-2534
        • Tinaz S.
        • Courtney M.G.
        • Stern C.E.
        Focal cortical and subcortical atrophy in early Parkinson's disease.
        Mov. Disord. 2011; 26: 436-441
        • Melzer T.R.
        • et al.
        Grey matter atrophy in cognitively impaired Parkinson's disease.
        J. Neurol. Neurosurg. Psychiatry. 2012; 83: 188-194
        • Uribe C.
        • et al.
        Patterns of cortical thinning in nondemented Parkinson's disease patients.
        Mov. Disord. 2016; 31: 699-708
        • Seeley W.W.
        • et al.
        Neurodegenerative diseases target large-scale human brain networks.
        Neuron. 2009; 62: 42-52
        • Borghammer P.
        • et al.
        Cortical hypometabolism and hypoperfusion in Parkinson's disease is extensive: probably even at early disease stages.
        Brain Struct. Funct. 2010; 214: 303-317
        • Gonzalez-Redondo R.
        • et al.
        Grey matter hypometabolism and atrophy in Parkinson's disease with cognitive impairment: a two-step process.
        Brain. 2014; 137: 2356-2367
        • Simons J.S.
        • Spiers H.J.
        Prefrontal and medial temporal lobe interactions in long-term memory.
        Nat. Rev. Neurosci. 2003; 4: 637-648
        • Seibert T.M.
        • et al.
        Interregional correlations in Parkinson disease and Parkinson-related dementia with resting functional MR imaging.
        Radiology. 2012; 263: 226-234
        • Yao Z.
        • et al.
        Abnormal cortical networks in mild cognitive impairment and Alzheimer's disease.
        PLoS Comput. Biol. 2010; 6: e1001006
        • Rektorova I.
        • et al.
        Default mode network and extrastriate visual resting state network in patients with Parkinson's disease dementia.
        Neurodegener. Dis. 2012; 10: 232-237
        • Hanganu A.
        • et al.
        Mild cognitive impairment in patients with Parkinson's disease is associated with increased cortical degeneration.
        Mov. Disord. 2013; 28: 1360-1369
        • Summerfield C.
        • et al.
        Structural brain changes in Parkinson disease with dementia: a voxel-based morphometry study.
        Arch. Neurol. 2005; 62: 281-285
        • Chen B.
        • et al.
        Changes in anatomical and functional connectivity of Parkinson's disease patients according to cognitive status.
        Eur. J. Radiol. 2015; 84: 1318-1324
        • Peran P.
        • et al.
        Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature.
        Brain. 2010; 133: 3423-3433
        • Weintraub D.
        • et al.
        Neurodegeneration across stages of cognitive decline in Parkinson disease.
        Arch. Neurol. 2011; 68: 1562-1568
        • Geng D.Y.
        • Li Y.X.
        • Zee C.S.
        Magnetic resonance imaging-based volumetric analysis of basal ganglia nuclei and substantia nigra in patients with Parkinson's disease.
        Neurosurgery. 2006; 58 (discussion 256–62): 256-262
        • Lewis M.M.
        • et al.
        The pattern of gray matter atrophy in Parkinson's disease differs in cortical and subcortical regions.
        J. Neurol. 2016 Jan; 263: 68-75https://doi.org/10.1007/s00415-015-7929-7
        • Harding A.J.
        • et al.
        Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease.
        Brain. 2002; 125: 2431-2445
        • Hoops S.
        • et al.
        Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease.
        Neurology. 2009; 73: 1738-1745