Advertisement

Reduced lateral occipital gray matter volume is associated with physical frailty and cognitive impairment in Parkinson’s disease

  • Yueh-Sheng Chen
  • Hsiu-Ling Chen
  • Cheng-Hsien Lu
  • Meng-Hsiang Chen
  • Kun-Hsien Chou
  • Nai-Wen Tsai
  • Chiun-Chieh Yu
  • Pi-Ling Chiang
  • Wei-Che Lin
Neuro
  • 6 Downloads

Abstract

Introduction

To investigate the structural changes of the brain that correlate with physical frailty and cognitive impairments in Parkinson’s disease (PD) patients.

Methods

Sixty-one PD patients and 59 age- and sex-matched healthy controls were enrolled. For each participant, a frailty assessment using Fried’s criteria and comprehensive neuropsychological testing using the Wechsler Adult Intelligence Scale-III and Cognitive Ability Screening Instrument were conducted, and structural brain MR images were acquired for voxel-based morphometric analysis. The neuropsychological testing includes various tests in these five domains: attention, executive, memory, speech and language, and visuospatial functions. Exploratory group-wise comparisons of gray matter volume (GMV) in the PD patients and controls were conducted. Voxel-wise multiple linear regression analyses were conducted for physical frailty–related and cognitive impairment–related GMV changes in the PD patients. Voxel-wise multiple linear regressions were also performed with the five cognitive domains separated using the same model.

Results

The PD patients exhibited diffuse GMV reductions in comparison to the controls. In the PD patients, physical frailty–related decreases in GMV were observed in the bilateral frontal and occipital cortices, while cognitive impairment–related decreases in GMV were observed in the bilateral frontal, occipital, and temporal cortices. These regions overlap in the lateral occipital cortex. After the five domains of cognitive functions were analyzed separately, physical frailty–related decreases in GMV still overlap in lateral occipital cortices with every domain of cognitive impairment–related decreases in GMV.

Conclusion

Reduced GMV in the lateral occipital cortex is associated with cognitive impairment and physical frailty in PD patients.

Key Points

• Physical frailty in PD was associated with decreased GMV in the frontal and occipital cortices, while cognitive impairment was associated with decreased GMV in the frontal, temporal, and occipital cortices.

• Physical frailty and cognitive impairment were both associated with decreased GMV in the lateral occipital cortex, which is part of the ventral object-based visual pathway.

• Decreased GMV in the lateral occipital cortex may serve as a potential imaging biomarker for physical frailty and cognitive impairment in PD.

Keywords

Frailty Cognitive impairment Gray matter volume Voxel-based morphometry Parkinson’s disease 

Abbreviations

GMV

Gray matter volume

MMSE

Mini-Mental State Examination

PD

Parkinson’s disease

TIV

Total intracranial volume

UPDRS

Unified Parkinson’s Disease Rating Scale

Notes

Funding

This study has received funding by National Science Council (MOST 106-2314-B-182A-031-MY2 to W-C Lin).

Compliance with ethical standards

Guarantor

The scientific guarantor of this publication is Wei-Che Lin.

Conflict of interest

The authors declare that they have no conflict of interest.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• Prospective

• Cross-sectional study

• Performed at one institution

Supplementary material

330_2018_5855_MOESM1_ESM.docx (208 kb)
ESM 1 (DOCX 208 kb)

References

  1. 1.
    Fried LP, Tangen CM, Walston J et al (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56:M146–M156CrossRefGoogle Scholar
  2. 2.
    Rothman MD, Leo-Summers L, Gill TM (2008) Prognostic significance of potential frailty criteria. J Am Geriatr Soc 56:2211–2216CrossRefGoogle Scholar
  3. 3.
    Chen WT, Chou KH, Liu LK et al (2015) Reduced cerebellar gray matter is a neural signature of physical frailty. Hum Brain Mapp 36:3666–3676CrossRefGoogle Scholar
  4. 4.
    Nadkarni NK, Nunley KA, Aizenstein H et al (2014) Association between cerebellar gray matter volumes, gait speed, and information-processing ability in older adults enrolled in the Health ABC study. J Gerontol A Biol Sci Med Sci 69:996–1003CrossRefGoogle Scholar
  5. 5.
    Rosano C, Studenski SA, Aizenstein HJ, Boudreau RM, Longstreth WT Jr, Newman AB (2012) Slower gait, slower information processing and smaller prefrontal area in older adults. Age Ageing 41:58–64CrossRefGoogle Scholar
  6. 6.
    Robertson DA, Savva GM, Kenny RA (2013) Frailty and cognitive impairment--a review of the evidence and causal mechanisms. Ageing Res Rev 12:840–851CrossRefGoogle Scholar
  7. 7.
    Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K (2013) Frailty in elderly people. Lancet 381:752–762CrossRefGoogle Scholar
  8. 8.
    Kelaiditi E, Cesari M, Canevelli M et al (2013) Cognitive frailty: rational and definition from an (I.A.N.A./I.A.G.G.) international consensus group. J Nutr Health Aging 17:726–734CrossRefGoogle Scholar
  9. 9.
    Weintraub D, Doshi J, Koka D et al (2011) Neurodegeneration across stages of cognitive decline in Parkinson disease. Arch Neurol 68:1562–1568CrossRefGoogle Scholar
  10. 10.
    Panza F, Seripa D, Solfrizzi V et al (2015) Targeting cognitive frailty: clinical and neurobiological roadmap for a single complex phenotype. J Alzheimers Dis 47:793–813CrossRefGoogle Scholar
  11. 11.
    Ahmed NN, Sherman SJ, Vanwyck D (2008) Frailty in Parkinson’s disease and its clinical implications. Parkinsonism Relat Disord 14:334–337CrossRefGoogle Scholar
  12. 12.
    Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752CrossRefGoogle Scholar
  13. 13.
    Zhao YJ, Wee HL, Chan YH et al (2010) Progression of Parkinson’s disease as evaluated by Hoehn and Yahr stage transition times. Mov Disord 25:710–716CrossRefGoogle Scholar
  14. 14.
    Ramaker C, Marinus J, Stiggelbout AM, Van Hilten BJ (2002) Systematic evaluation of rating scales for impairment and disability in Parkinson’s disease. Mov Disord 17:867–876CrossRefGoogle Scholar
  15. 15.
    Qu NN, Li KJ (2004) Study on the reliability and validity of international physical activity questionnaire (Chinese vision, IPAQ). Zhonghua Liu Xing Bing Xue Za Zhi 25:265–268Google Scholar
  16. 16.
    Wechsler D, Chen Y, Chen X (2002) WAIS-III Chinese version technical manual. Psychological Corporation, San AntonioGoogle Scholar
  17. 17.
    Lin KN, Wang PN, Liu HC, Teng EL (2012) Cognitive abilities screening instrument, Chinese version 2.0 (CASI C-2.0): administration and clinical application. Acta Neurol Taiwan 21:180–189Google Scholar
  18. 18.
    Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211CrossRefGoogle Scholar
  19. 19.
    Litvan I, Goldman JG, Tröster AI et al (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord 27:349–356CrossRefGoogle Scholar
  20. 20.
    Emre M, Aarsland D, Brown R et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707 quiz 1837CrossRefGoogle Scholar
  21. 21.
    Burton EJ, McKeith IG, Burn DJ, Williams ED, O'Brien JT (2004) Cerebral atrophy in Parkinson’s disease with and without dementia: a comparison with Alzheimer’s disease, dementia with Lewy bodies and controls. Brain 127:791–800CrossRefGoogle Scholar
  22. 22.
    Fairhall N, Langron C, Sherrington C et al (2011) Treating frailty--a practical guide. BMC Med 9:83CrossRefGoogle Scholar
  23. 23.
    Gill TM, Gahbauer EA, Allore HG, Han L (2006) Transitions between frailty states among community-living older persons. Arch Intern Med 166:418–423CrossRefGoogle Scholar
  24. 24.
    Luft AR, Skalej M, Schulz JB et al (1999) Patterns of age-related shrinkage in cerebellum and brainstem observed in vivo using three-dimensional MRI volumetry. Cereb Cortex 9:712–721CrossRefGoogle Scholar
  25. 25.
    Wu T, Hallett M (2013) The cerebellum in Parkinson’s disease. Brain 136:696–709CrossRefGoogle Scholar
  26. 26.
    Mirdamadi JL (2016) Cerebellar role in Parkinson’s disease. J Neurophysiol 116:917–919CrossRefGoogle Scholar
  27. 27.
    Mishkin M, Ungerleider LG, Macko KA (1983) Object vision and spatial vision: two cortical pathways. Trends Neurosci 6:414–417CrossRefGoogle Scholar
  28. 28.
    Kamitani Y, Tong F (2005) Decoding the visual and subjective contents of the human brain. Nat Neurosci 8:679–685CrossRefGoogle Scholar
  29. 29.
    du Boisgueheneuc F, Levy R, Volle E et al (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328CrossRefGoogle Scholar
  30. 30.
    Kravitz DJ, Saleem KS, Baker CI, Ungerleider LG, Mishkin M (2013) The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn Sci 17:26–49CrossRefGoogle Scholar
  31. 31.
    James TW, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. Brain 126:2463–2475CrossRefGoogle Scholar
  32. 32.
    Whitson HE, Cousins SW, Burchett BM, Hybels CF, Pieper CF, Cohen HJ (2007) The combined effect of visual impairment and cognitive impairment on disability in older people. J Am Geriatr Soc 55:885–891CrossRefGoogle Scholar
  33. 33.
    Lin MY, Gutierrez PR, Stone KL et al (2004) Vision impairment and combined vision and hearing impairment predict cognitive and functional decline in older women. J Am Geriatr Soc 52:1996–2002CrossRefGoogle Scholar
  34. 34.
    Pereira JB, Svenningsson P, Weintraub D et al (2014) Initial cognitive decline is associated with cortical thinning in early Parkinson disease. Neurology 82:2017–2025CrossRefGoogle Scholar
  35. 35.
    Lin WC, Chou KH, Lee PL et al (2015) Brain mediators of systemic oxidative stress on perceptual impairments in Parkinson’s disease. J Transl Med 13:386CrossRefGoogle Scholar
  36. 36.
    Hwang O (2013) Role of oxidative stress in Parkinson’s disease. Exp Neurobiol 22:11–17CrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  1. 1.Department of Diagnostic Radiology, Kaohsiung Chang Gung Memorial HospitalChang Gung University College of MedicineKaohsiungTaiwan
  2. 2.Department of Neurology, Kaohsiung Chang Gung Memorial HospitalChang Gung University College of MedicineKaohsiungTaiwan
  3. 3.Department of Biological ScienceNational Sun Yat-Sen UniversityKaohsiungTaiwan
  4. 4.Institute of NeuroscienceNational Yang-Ming UniversityTaipeiTaiwan

Personalised recommendations