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Aging and disease    2016, Vol. 7 Issue (3) : 220-229     DOI: 10.14336/AD.2015.1110
Original Article |
Linear and Curvilinear Trajectories of Cortical Loss with Advancing Age and Disease Duration in Parkinson’s Disease
Claassen Daniel O.1,*, Dobolyi David G.2, Isaacs David A.1, Roman Olivia C.1, Herb Joshua3, Wylie Scott A.1, Neimat Joseph S.4, Donahue Manus J.1,5, Hedera Peter1, Zald David H.6, Landman Bennett A.5,7, Bowman Aaron B.1, Dawant Benoit M.7, Rane Swati5
1Department of Neurology, Vanderbilt University, Nashville, TN 37235, USA
2McIntire School of Commerce, University of Virginia, Charlottesville, VA 22904, USA
3Department of Medicine, University of Virginia, Charlottesville, VA 22904, USA
4Department of Neurosurgery, Vanderbilt University, Nashville, TN 37235, USA
5Department of Radiology, Vanderbilt University, Nashville, TN 37235, USA
6Department of Psychology, Vanderbilt University, Nashville, TN 37235, USA
7Department of Biomedical Engineering, Vanderbilt University, Nashville, TN 37235, USA
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Abstract  

Advancing age and disease duration both contribute to cortical thinning in Parkinson’s disease (PD), but the pathological interactions between them are poorly described. This study aims to distinguish patterns of cortical decline determined by advancing age and disease duration in PD. A convenience cohort of 177 consecutive PD patients, identified at the Vanderbilt University Movement Disorders Clinic as part of a clinical evaluation for Deep Brain Stimulation (age: M= 62.0, SD 9.3), completed a standardized clinical assessment, along with structural brain Magnetic Resonance Imaging scan. Age and gender matched controls (n=53) were obtained from the Alzheimer Disease Neuroimaging Initiative and Progressive Parkinson’s Marker Initiative (age: M= 63.4, SD 12.2). Estimated changes in cortical thickness were modeled with advancing age, disease duration, and their interaction. The best-fitting model, linear or curvilinear (2nd, or 3rd order natural spline), was defined using the minimum Akaike Information Criterion, and illustrated on a 3-dimensional brain. Three curvilinear patterns of cortical thinning were identified: early decline, late decline, and early-stable-late. In contrast to healthy controls, the best-fit model for age related changes in PD is curvilinear (early decline), particularly in frontal and precuneus regions. With advancing disease duration, a curvilinear model depicts accelerating decline in the occipital cortex. A significant interaction between advancing age and disease duration is evident in frontal, motor, and posterior parietal areas. Study results support the hypothesis that advancing age and disease duration differentially affect regional cortical thickness and display regional dependent linear and curvilinear patterns of thinning.

Keywords Parkinson’s disease      Cortex      MRI      Aging      Disease duration      Neurodegeneration     
Corresponding Authors: Claassen Daniel O.   
About author:

These authors equally contribute this work

Issue Date: 09 January 2016
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Articles by authors
Claassen Daniel O.
Dobolyi David G.
Isaacs David A.
Roman Olivia C.
Herb Joshua
Wylie Scott A.
Neimat Joseph S.
Donahue Manus J.
Hedera Peter
Zald David H.
Landman Bennett A.
Bowman Aaron B.
Dawant Benoit M.
Rane Swati
Cite this article:   
Claassen Daniel O.,Dobolyi David G.,Isaacs David A., et al. Linear and Curvilinear Trajectories of Cortical Loss with Advancing Age and Disease Duration in Parkinson’s Disease[J]. Aging and disease, 2016, 7(3): 220-229.
URL:  
http://www.aginganddisease.org/EN/10.14336/AD.2015.1110     OR     http://www.aginganddisease.org/EN/Y2016/V7/I3/220
Parkinson’s Disease (n=177)Healthy Controls (n=53)
Gender (M:F)(121:56)(39:14)
Assessment Age (years)62.0 (9.3)63.68 (12.23)
Disease Duration10.3 (4.8)
UPDRS III Off40.8 (12.9)
UPDRS III On18.7 (10.0)
Table 1  Participant Demographics
Cognitive AssessmentNumber testedMean (S.D)
Scaled Score
Dementia Rating Scale[33]15312.0 (2.5)
Trails A[34,35]1777.6 (3.0)
Trails B[34,35]1778.1 (3.0)
Judgment of Line Orientation[36]17710.7 (2.9)
Letter Fluency[37]1779.4 (2.5)
Word List 1[38]1778.8 (3.4)
Word List 2[38]17711.3 (2.5)
Table 2  Cognitive Profile of PD patients
Figure 1.  Models of age and disease duration effects on cortical thickness

A) Age effects in the pars opercularis are different in PD (blue) compared to healthy controls (red). PD patients show a non-linear trajectory (blue) of ‘early decline’, which stabilizes. Rate of cortical thinning with age in PD is different in this frontal region, likely due to disease processes. However, cortical atrophy rate with respect to increasing disease durations was not significant. B) Age effects in the lateral occipital cortex conform to preservation of the cortex in the early years and an accelerated late decline in healthy controls (late decline), while in PD gray matter atrophies continuously with age (left panel). PD patients also showed a significant effect of disease duration alone, independent of age (right panel). C) Unlike Figure 1a, the parietal cortex shows a linear rate of cortical thinning with age in both controls and PD. However, cortical thinning in PD appears to be faster than in controls (left panel). Cortical thickness is also linearly dependent on duration of PD. Furthermore, increasing disease duration significantly increases the rate of cortical thinning (right panel). D) The interactions between age and disease duration in PD. Older patients with longer disease duration have a greater linear rate of cortical loss in the inferior parietal cortex.

Figure 2.  The effect of age on cortical thickness in healthy Ccontrols and Parkinson’s disease

Green highlighted regions represent those regions that follow a linear rate of atrophy. Red highlighted regions depict rates of early decline (decreasing quickly at first, then stabilizing), while regions in yellow depict regions that atrophy faster over time (stable at first, then decreasing quickly). Regions in orange depict early decline, stabilization, followed by late decline, which is notable in later decades of life (early-stable-late). PD patients show characteristic frontal cortical thinning with age.

Figure 3.  The effects of disease duration, and its interaction with age, on cortical thickness in Parkinson’s disease

Regions in yellow depict regions that atrophy faster over time (concave down, decreasing curve or late decline). Regions in blue shown in the right column are regions showing an interaction between age and disease.

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