Subcortical Atrophy Is Associated with Cognitive Impairment in Mild Parkinson Disease: A Combined Investigation of Volumetric Changes, Cortical Thickness, and Vertex-Based Shape Analysis

E. Mak; N. Bergsland; M.G. Dwyer; R. Zivadinov; N. Kandiah

doi:10.3174/ajnr.A4055

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Fig 1.
Representative FIRST segmentation of subcortical structures in patients with PD-MCI (left) and PD-NCI (right).
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Fig 2.
Scatterplot showing the associations between the nucleus accumbens and attention and working memory (A) and language domains (B).

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Table 1:

Demographic, clinical, and white matter hyperintensity characteristics between patients with Parkinson disease with and without mild cognitive impairment

Demographic and Clinical Variables	PD-NCI (n = 65)	PD-MCI (n = 25)	P Value
Age (yr) (mean) (SD)	63.4 (7.6)	69.4 (6.4)	.001^{^a,^b}
Sex (male) (No.) (%)	46 (72.3)	18 (76.0)	.723^{^c}
Education (yr) (mean) (SD)	11.0 (3.1)	9.3 (3.5)	.032^{^a,^d}
Hoehn and Yahr (mean) (SD)	1.9 (0.4)	1.8 (0.4)	.357^{^d}
Disease duration (yr) (mean) (SD)	5.4 (4.3)	5.0 (2.7)	.910^{^d}
UPDRS (mean) (SD)	17.5 (7.0)	20.0 (8.4)	.167^{^b}
Levodopa equivalent dose (mg) (mean) (SD)	557.4 (375.7)	510.2 (299.0)	.767^{^d}
Cardiovascular risk factors (No.) (%)
Diabetes	5 (7.8)	8 (32.0)	.004^{^a,^c}
Hypertension	20 (31.3)	13 (52.0)	.069^{^c}
Hyperlipidemia	20 (31.3)	14 (56.0)	.031^{^a,^c}
Smoking	15 (23.4)	6 (24.0)	.955^{^c}
White matter hyperintensities
Total WMH volume (mm) (mean) (SD)	4.2 (5.8)	12.3 (10.3)	<.001^{^a,^e}

Note:—UPDRS indicates Unified Parkinson's Disease Rating Scale, subscore III; WMH, white matter hyperintensities.
↵a Significant differences at P < .05 level.
↵b Student t test.
↵c χ² test.
↵d Mann-Whitney U test.
↵e Analysis of covariance test, corrected for age, sex, and education.

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Table 2:

Comparison of neuropsychological measures between patients with Parkinson disease with and without mild cognitive impairment

Neuropsychological Measures	PD-NCI (Mean) (SD)	PD-MCI (Mean) (SD)	Adjusted P Value
Global cognition (mean) (SD)
MMSE	28.4 (1.6)	26.7 (2.6)	.016^{^a,^b}
MOCA	27.0 (2.9)	24.5 (2.4)	.018^{^a,^b}
ADAS11	6.8 (4.2)	9.8 (3.5)	.071^{^a,^b}
Global Index	0.1 (0.5)	−0.3 (0.3)	.008^{^a,^b}
Cognitive tests (mean) (SD)
Clock drawing	9.31 (1.25)	8.48 (1.47)	.126
Frontal Assessment Battery	16.69 (1.38)	15.28 (2.09)	.027
Digit Span	17.42 (3.50)	15.04 (2.24)	.015
Digit Cancellation	19.86 (6.54)	15.08 (6.45)	.063
Color Trail 1	80.48 (37.59)	137.24 (82.08)	.008
Color Trail 2	138.94 (60.75)	229.58 (103.31)	.002
Maze	18.63 (10.59)	30.80 (17.83)	.005
Maze errors	0.06 (0.30)	0.04 (0.20)	.942
ADAS: Immediate and Delayed Recall	5.08 (2.69)	7.04 (3.28)	.090
ADAS: Recognition	1.55 (2.22)	2.00 (2.50)	.644
ADAS: Language	1.15 (1.37)	2.00 (1.71)	.168
Fruit Fluency	14.11 (3.29)	11.24 (2.80)	.029
Cognitive domains (mean) (SD)
Executive function	0.4 (1.5)	−1.0 (2.0)	.023^{^a,^b}
Attention/working memory	0.8 (1.7)	−2.0 (2.4)	<.000^{^a,^b}
Visuospatial	0.0 (1.8)	−0.1 (1.4)	.919^d
Episodic memory	0.3 (1.6)	−0.6 (1.5)	.193^{^b}
Language	0.4 (1.4)	−1.0 (1.5)	.018^{^a,^b}

Note:—MMSE indicates Mini-Mental State Examination; MOCA, Montreal Cognitive Assessment; ADAS11, Alzheimer Disease Assessment Scale-Cognitive.
↵a Significant differences at P < .05 level.
↵b Analysis of covariance test, corrected for age, sex, and education.

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Table 3:

Volumetric comparisons between patients with Parkinson disease with and without mild cognitive impairment

SDGM Structures^{^a}	PD-NCI (Mean) (SD)	PD-MCI (Mean) (SD)	Adjusted P Value
Amygdala	2.13 (0.51)	2.23 (0.36)	.220^{^b}
Hippocampus	7.65 (0.97)	7.18 (0.79)	.198^{^b}
Nucleus accumbens	0.83 (0.22)	0.64 (0.19)	.044^{^b}
Caudate nucleus	6.37 (0.76)	5.96 (0.76)	.327^{^b}
Putamen	9.51 (1.41)	8.62 (1.17)	.058^{^b}
Pallidum	3.72 (0.66)	3.60 (0.84)	.876^{^b}
Thalamus	13.94 (1.65)	12.71 (1.09)	.025^{^b}
Normalized gray matter	688.76 (34.86)	661.92 (28.24)	.035^{^b}
Normalized white matter	654.43 (41.49)	633.10 (46.04)	.618^{^b}

↵a All volumes are reported in milliliters. Significant difference is at the P < .05 level.
↵b Analysis of variance adjusting for age, sex, education, and head size.

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Table 4:

Mean global and hemispheric cortical thickness between patients with Parkinson disease with and without mild cognitive impairment

Cortical Thickness^{^a}	PD-NCI (Mean) (SD)	PD-MCI (Mean) (SD)	Adjusted P Value
Left hemisphere	2.20 (0.10)	2.13 (0.11)	.095^{^b}
Right hemisphere	2.19 (0.10)	2.13 (0.10)	.264^{^b}
Global mean cortical thickness	4.40 (0.19)	4.26 (0.21)	.151^{^b}

↵a Cortical thickness is expressed in millimeters. Significant difference is at the P < .05 level.
↵b Analysis of variance adjusting for age, sex, education.