Skip to main content

Advertisement

Log in

The impact of cerebral small vessel disease burden and its imaging markers on gait, postural control, and cognition in Parkinson’s disease

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Objective

This study aimed to investigate how cerebral small vessel disease (CSVD) burden and its imaging markers are related to alterations in different gait parameters in Parkinson’s disease (PD) and whether they affect attention, information processing speed, and executive function when global mental status is relatively intact.

Methods

Sixty-five PD patients were divided into the low CSVD burden group (n = 43) and the high CSVD burden group (n = 22). All patients underwent brain magnetic resonance imaging scans, clinical scale evaluations, and neuropsychological tests, as well as quantitative evaluation of gait and postural control. Multivariable linear regression models were conducted to investigate associations between CSVD burden and PD symptoms.

Results

Between-group analysis showed that the high CSVD group had worse attention, executive dysfunction, information processing speed, gait, balance, and postural control than the low CSVD group. Regression analysis revealed that greater CSVD burden was associated with poor attention, impaired executive function, and slow gait speed; white matter hyperintensity was associated with slow gait speed, decreased cadence, increased stride time, and increased stance phase time; the presence of lacune was associated only with poor attention and impaired executive function; enlarged perivascular space in the basal ganglia was associated with gait speed.

Conclusions

CSVD burden may worsen gait, postural control, attention, and executive function in patients with PD, and different imaging markers play different roles. Early management of vascular risks and treatment of vascular diseases provide an alternate way to mitigate some motor and cognitive dysfunction in PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–1601. https://doi.org/10.1002/mds.26424

    Article  PubMed  Google Scholar 

  2. Song IU, Lee JE, Kwon DY, Park JH, Ma HI (2017) Parkinson’s disease might increase the risk of cerebral ischemic lesions. Int J Med Sci 14(4):319–322. https://doi.org/10.7150/ijms.18025

    Article  PubMed  PubMed Central  Google Scholar 

  3. Lee Y, Ko J, Choi YE, Oh JS, Kim JS, Sunwoo MK, Yoon JH, Kang SY, Hong JY (2020) Areas of white matter hyperintensities and motor symptoms of Parkinson disease. Neurology 95(3):e291–e298. https://doi.org/10.1212/WNL.0000000000009890

    Article  CAS  PubMed  Google Scholar 

  4. de Schipper LJ, Hafkemeijer A, Bouts M, van der Grond J, Marinus J, Henselmans JML, van Hilten JJ (2019) Age- and disease-related cerebral white matter changes in patients with Parkinson’s disease. Neurobiol Aging 80:203–209. https://doi.org/10.1016/j.neurobiolaging.2019.05.004

    Article  PubMed  Google Scholar 

  5. Chung SJ, Lee YH, Yoo HS, Oh JS, Kim JS, Ye BS, Sohn YH, Lee PH (2019) White matter hyperintensities as a predictor of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 66:105–109. https://doi.org/10.1016/j.parkreldis.2019.07.019

    Article  PubMed  Google Scholar 

  6. Ciliz M, Sartor J, Lindig T, Pilotto A, Schaffer E, Weiss M, Scheltens P, Becker S, Hobert MA, Berg D, Liepelt-Scarfone I, Maetzler W (2018) Brain-area specific white matter hyperintensities: associations to falls in Parkinson’s disease. J Parkinsons Dis 8(3):455–462. https://doi.org/10.3233/JPD-181351

    Article  PubMed  Google Scholar 

  7. Liu H, Deng B, Xie F, Yang X, Xie Z, Chen Y, Yang Z, Huang X, Zhu S, Wang Q (2021) The influence of white matter hyperintensity on cognitive impairment in Parkinson’s disease. Ann Clin Transl Neurol 8(9):1917–1934. https://doi.org/10.1002/acn3.51429

    Article  PubMed  PubMed Central  Google Scholar 

  8. Linortner P, McDaniel C, Shahid M, Levine TF, Tian L, Cholerton B, Poston KL (2020) White matter hyperintensities related to Parkinson’s disease executive function. Mov Disord Clin Pract 7(6):629–638. https://doi.org/10.1002/mdc3.12956

    Article  PubMed  PubMed Central  Google Scholar 

  9. Huang X, Wen MC, Ng SY, Hartono S, Chia NS, Choi X, Tay KY, Au WL, Chan LL, Tan EK, Tan LC (2020) Periventricular white matter hyperintensity burden and cognitive impairment in early Parkinson’s disease. Eur J Neurol 27(6):959–966. https://doi.org/10.1111/ene.14192

    Article  CAS  PubMed  Google Scholar 

  10. Shibata K, Sugiura M, Nishimura Y, Sakura H (2019) The effect of small vessel disease on motor and cognitive function in Parkinson’s disease. Clin Neurol Neurosurg 182:58–62. https://doi.org/10.1016/j.clineuro.2019.04.029

    Article  PubMed  Google Scholar 

  11. Chen H, Zhang M, Liu G, Wang X, Wang Z, Ma H, Pan Y, Wang D, Wang Y, Feng T (2020) Effect of small vessel disease burden and lacunes on gait/posture impairment in Parkinson’s disease. Neurol Sci 41(12):3617–3624. https://doi.org/10.1007/s10072-020-04452-z

    Article  PubMed  Google Scholar 

  12. Chen HM, Wan HJ, Zhang MM, Liu GL, Wang XM, Wang Z, Ma HZ, Pan YS, Feng T, Wang YL (2021) Cerebral small vessel disease may worsen motor function, cognition, and mood in Parkinson’s disease. Parkinsonism Relat D 83:86–92. https://doi.org/10.1016/j.parkreldis.2020.12.025

    Article  Google Scholar 

  13. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17(5):427–442. https://doi.org/10.1212/wnl.17.5.427

    Article  CAS  PubMed  Google Scholar 

  14. Katzman R, Zhang MY, Ouang Ya Q, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the Mini-Mental State Examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41(10):971–978. https://doi.org/10.1016/0895-4356(88)90034-0

    Article  CAS  PubMed  Google Scholar 

  15. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653. https://doi.org/10.1002/mds.23429

    Article  PubMed  Google Scholar 

  16. Smith A (1982) Symbol Digit Modalities Test (SDMT): manual (revised). Los Angeles: Western Psychological Services.

  17. Reitan RM (1955) The relation of the trail making test to organic brain damage. J Consult Psychol 19(5):393–394. https://doi.org/10.1037/h0044509

    Article  CAS  PubMed  Google Scholar 

  18. Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32(1):50–55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.x

    Article  CAS  PubMed  Google Scholar 

  19. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62. https://doi.org/10.1136/jnnp.23.1.56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39(2):142–148. https://doi.org/10.1111/j.1532-5415.1991.tb01616.x

    Article  CAS  PubMed  Google Scholar 

  21. Laboratories ATSCoPSfCPF, (2002) ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 166(1):111–117. https://doi.org/10.1164/ajrccm.166.1.at1102

    Article  Google Scholar 

  22. Lang JT, Kassan TO, Devaney LL, Colon-Semenza C, Joseph MF (2016) Test-retest reliability and minimal detectable change for the 10-Meter Walk Test in older adults with Parkinson’s disease. J Geriatr Phys Ther 39(4):165–170. https://doi.org/10.1519/JPT.0000000000000068

    Article  PubMed  Google Scholar 

  23. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, nEuroimaging STfRVco, (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12(8):822–838. https://doi.org/10.1016/S1474-4422(13)70124-8

    Article  PubMed  PubMed Central  Google Scholar 

  24. Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43(9):1683–1689. https://doi.org/10.1212/wnl.43.9.1683

    Article  CAS  PubMed  Google Scholar 

  25. Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM (2010) Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke 41(3):450–454. https://doi.org/10.1161/STROKEAHA.109.564914

    Article  PubMed  Google Scholar 

  26. Toda K, Iijima M, Kitagawa K (2019) Periventricular white matter lesions influence gait functions in Parkinson’s disease. Eur Neurol 81(3–4):120–127. https://doi.org/10.1159/000499908

    Article  PubMed  Google Scholar 

  27. Bohnen NI, Albin RL (2011) White matter lesions in Parkinson disease. Nat Rev Neurol 7(4):229–236. https://doi.org/10.1038/nrneurol.2011.21

    Article  PubMed  PubMed Central  Google Scholar 

  28. Piccini P, Pavese N, Canapicchi R, Paoli C, Del Dotto P, Puglioli M, Rossi G, Bonuccelli U (1995) White matter hyperintensities in Parkinson’s disease. Clinical correlations Arch Neurol 52(2):191–194. https://doi.org/10.1001/archneur.1995.00540260097023

    Article  CAS  PubMed  Google Scholar 

  29. Arena JE, Cerquetti D, Rossi M, Chaves H, Rollan C, Dossi DE, Merello M (2016) Influence of white matter MRI hyper-intensities on acute l-dopa response in patients with Parkinson’s disease. Parkinsonism Relat Disord 24:126–128. https://doi.org/10.1016/j.parkreldis.2016.01.017

    Article  CAS  PubMed  Google Scholar 

  30. Chung SJ, Yoo HS, Lee YH, Jung JH, Baik K, Ye BS, Sohn YH, Lee PH (2020) White matter hyperintensities and risk of levodopa-induced dyskinesia in Parkinson’s disease. Ann Clin Transl Neurol 7(2):229–238. https://doi.org/10.1002/acn3.50991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dadar M, Miyasaki J, Duchesne S, Camicioli R (2021) White matter hyperintensities mediate the impact of amyloid β on future freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 85:95–101. https://doi.org/10.1016/j.parkreldis.2021.02.031

    Article  CAS  PubMed  Google Scholar 

  32. Cavallieri F, Fraix V, Bove F, Mulas D, Tondelli M, Castrioto A, Krack P, Meoni S, Schmitt E, Lhommee E, Bichon A, Pelissier P, Chevrier E, Kistner A, Seigneuret E, Chabardes S, Moro E (2021) Predictors of long-term outcome of subthalamic stimulation in Parkinson disease. Ann Neurol 89(3):587–597. https://doi.org/10.1002/ana.25994

    Article  CAS  PubMed  Google Scholar 

  33. Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17(11):1016–1024. https://doi.org/10.1016/S1474-4422(18)30318-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sundaram S, Hughes RL, Peterson E, Muller-Oehring EM, Bronte-Stewart HM, Poston KL, Faerman A, Bhowmick C, Schulte T (2019) Establishing a framework for neuropathological correlates and glymphatic system functioning in Parkinson’s disease. Neurosci Biobehav Rev 103:305–315. https://doi.org/10.1016/j.neubiorev.2019.05.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lv W, Yue Y, Shen T, Hu X, Chen L, Xie F, Zhang W, Zhang B, Gui Y, Lai HY, Ba F (2021) Normal-sized basal ganglia perivascular space related to motor phenotype in Parkinson freezers. Aging (Albany NY) 13 (14): 18912–18923. https://doi.org/10.18632/aging.203343

  36. Chung SJ, Yoo HS, Shin NY, Park YW, Lee HS, Hong JM, Kim YJ, Lee SK, Lee PH, Sohn YH (2021) Perivascular spaces in the basal ganglia and long-term motor prognosis in newly diagnosed Parkinson disease. Neurology 96(16):e2121–e2131. https://doi.org/10.1212/WNL.0000000000011797

    Article  CAS  PubMed  Google Scholar 

  37. Shen T, Yue Y, Zhao S, Xie J, Chen Y, Tian J, Lv W, Lo CZ, Hsu YC, Kober T, Zhang B, Lai HY (2021) The role of brain perivascular space burden in early-stage Parkinson’s disease. NPJ Parkinsons Dis 7(1):12. https://doi.org/10.1038/s41531-021-00155-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Si XL, Gu LY, Song Z, Zhou C, Fang Y, Jin CY, Wu JJ, Gao T, Guo T, Guan XJ, Xu XJ, Yin XZ, Yan YP, Zhang MM, Pu JL (2020) Different perivascular space burdens in idiopathic rapid eye movement sleep behavior disorder and Parkinson’s disease. Front Aging Neurosci 12:580853. https://doi.org/10.3389/fnagi.2020.580853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fang Y, Gu LY, Tian J, Dai SB, Chen Y, Zheng R, Si XL, Jin CY, Song Z, Yan YP, Yin XZ, Pu JL, Zhang BR (2020) MRI-visible perivascular spaces are associated with cerebrospinal fluid biomarkers in Parkinson’s disease. Aging (Albany NY) 12 (24): 25805–25818. https://doi.org/10.18632/aging.104200

  40. Wan Y, Hu W, Gan J, Song L, Wu N, Chen Y, Liu Z (2019) Exploring the association between cerebral small-vessel diseases and motor symptoms in Parkinson’s disease. Brain Behav 9(4):e01219. https://doi.org/10.1002/brb3.1219

    Article  PubMed  PubMed Central  Google Scholar 

  41. Song IU, Kim YD, Cho HJ, Chung SW (2013) The effects of silent cerebral ischemic lesions on the prognosis of idiopathic Parkinson’s disease. Parkinsonism Relat Disord 19(8):761–763. https://doi.org/10.1016/j.parkreldis.2013.04.006

    Article  PubMed  Google Scholar 

  42. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67(1):53–83. https://doi.org/10.1016/s0301-0082(02)00011-4

    Article  CAS  PubMed  Google Scholar 

  43. Bezdicek O, Ballarini T, Ruzicka F, Roth J, Mueller K, Jech R, Schroeter ML (2018) Mild cognitive impairment disrupts attention network connectivity in Parkinson’s disease: a combined multimodal MRI and meta-analytical study. Neuropsychologia 112:105–115. https://doi.org/10.1016/j.neuropsychologia.2018.03.011

    Article  PubMed  Google Scholar 

  44. Bocquillon P, Bourriez JL, Palmero-Soler E, Destee A, Defebvre L, Derambure P, Dujardin K (2012) Role of basal ganglia circuits in resisting interference by distracters: a swLORETA study. PLoS ONE 7(3):e34239. https://doi.org/10.1371/journal.pone.0034239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zgaljardic DJ, Borod JC, Foldi NS, Mattis P (2003) A review of the cognitive and behavioral sequelae of Parkinson’s disease: relationship to frontostriatal circuitry. Cogn Behav Neurol 16(4):193–210. https://doi.org/10.1097/00146965-200312000-00001

    Article  PubMed  Google Scholar 

  46. Dey AK, Stamenova V, Turner G, Black SE, Levine B (2016) Pathoconnectomics of cognitive impairment in small vessel disease: a systematic review. Alzheimers Dement 12(7):831–845. https://doi.org/10.1016/j.jalz.2016.01.007

    Article  PubMed  Google Scholar 

  47. Ter Telgte A, van Leijsen EMC, Wiegertjes K, Klijn CJM, Tuladhar AM, de Leeuw FE (2018) Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol 14(7):387–398. https://doi.org/10.1038/s41582-018-0014-y

    Article  PubMed  Google Scholar 

  48. Hamilton OKL, Cox SR, Okely JA, Conte F, Ballerini L, Bastin ME, Corley J, Taylor AM, Page D, Gow AJ, Munoz Maniega S, Redmond P, Valdes-Hernandez MDC, Wardlaw JM, Deary IJ (2021) Cerebral small vessel disease burden and longitudinal cognitive decline from age 73 to 82: the Lothian Birth Cohort 1936. Transl Psychiatry 11(1):376. https://doi.org/10.1038/s41398-021-01495-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Benjamin P, Lawrence AJ, Lambert C, Patel B, Chung AW, MacKinnon AD, Morris RG, Barrick TR, Markus HS (2014) Strategic lacunes and their relationship to cognitive impairment in cerebral small vessel disease. Neuroimage Clin 4:828–837. https://doi.org/10.1016/j.nicl.2014.05.009

    Article  PubMed  PubMed Central  Google Scholar 

  50. Benjamin P, Trippier S, Lawrence AJ, Lambert C, Zeestraten E, Williams OA, Patel B, Morris RG, Barrick TR, MacKinnon AD, Markus HS (2018) Lacunar infarcts, but not perivascular spaces, are predictors of cognitive decline in cerebral small-vessel disease. Stroke 49(3):586–593. https://doi.org/10.1161/STROKEAHA.117.017526

    Article  PubMed  PubMed Central  Google Scholar 

  51. Dalaker TO, Larsen JP, Dwyer MG, Aarsland D, Beyer MK, Alves G, Bronnick K, Tysnes OB, Zivadinov R (2009) White matter hyperintensities do not impact cognitive function in patients with newly diagnosed Parkinson’s disease. Neuroimage 47(4):2083–2089. https://doi.org/10.1016/j.neuroimage.2009.06.020

    Article  PubMed  Google Scholar 

  52. Terra MB, Da Silva RA, Bueno MEB, Ferraz HB, Smaili SM (2020) Center of pressure-based balance evaluation in individuals with Parkinson’s disease: a reliability study. Physiother Theory Pract 36(7):826–833. https://doi.org/10.1080/09593985.2018.1508261

    Article  PubMed  Google Scholar 

  53. Perez-Sanchez JR, Grandas F (2019) Early postural instability in Parkinson’s disease: a biomechanical analysis of the pull test. Parkinsons Dis 2019:6304842. https://doi.org/10.1155/2019/6304842

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kamieniarz A, Michalska J, Marszalek W, Stania M, Slomka KJ, Gorzkowska A, Juras G, Okun MS, Christou EA (2021) Detection of postural control in early Parkinson’s disease: clinical testing vs. modulation of center of pressure. PLoS One 16 (1): e0245353. https://doi.org/10.1371/journal.pone.0245353

  55. Chen T, Fan Y, Zhuang X, Feng D, Chen Y, Chan P, Du Y (2018) Postural sway in patients with early Parkinson’s disease performing cognitive tasks while standing. Neurol Res 40(6):491–498. https://doi.org/10.1080/01616412.2018.1451017

    Article  CAS  PubMed  Google Scholar 

  56. Sciadas R, Dalton C, Nantel J (2016) Effort to reduce postural sway affects both cognitive and motor performances in individuals with Parkinson’s disease. Hum Mov Sci 47:135–140. https://doi.org/10.1016/j.humov.2016.03.003

    Article  PubMed  Google Scholar 

  57. Marchese R, Bove M, Abbruzzese G (2003) Effect of cognitive and motor tasks on postural stability in Parkinson’s disease: a posturographic study. Mov Disord 18(6):652–658. https://doi.org/10.1002/mds.10418

    Article  PubMed  Google Scholar 

  58. Ndayisaba A, Kaindlstorfer C, Wenning GK (2019) Iron in neurodegeneration — cause or consequence? Front Neurosci 13:180. https://doi.org/10.3389/fnins.2019.00180

    Article  PubMed  PubMed Central  Google Scholar 

  59. Pilotto A, Romagnolo A, Tuazon JA, Vizcarra JA, Marsili L, Zibetti M, Rosso M, Rodriguez-Porcel F, Borroni B, Rizzetti MC, Rossi C, Vizcarra-Escobar D, Molano JR, Lopiano L, Ceravolo R, Masellis M, Espay AJ, Padovani A, Merola A (2019) Orthostatic hypotension and REM sleep behaviour disorder: impact on clinical outcomes in alpha-synucleinopathies. J Neurol Neurosurg Psychiatry 90(11):1257–1263. https://doi.org/10.1136/jnnp-2019-320846

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to all the patients and the medical staff of the Neurological Rehabilitation Center of Beijing Rehabilitation Hospital who contributed to this project.

Funding

This study was supported by the National Key R&D Program of China (No. 2018YFC0115405) for BF and the Science and Technology Development Fund of Beijing Rehabilitation Hospital, Capital Medical University (2019R-006 for ZJ; 2020–069 for BF; 2020–051 for HY).

Author information

Authors and Affiliations

Authors

Contributions

Author contributions included conception and study design (BF, JX, AL, ZJ, QW, and KC), data collection or acquisition (ZJ, JF, LQ, CL, RW, YS, HY, QW, and KC), statistical analysis (BF and KC), interpretation of results (BF and JX), drafting the manuscript work (KC and QW), revising the manuscript critically for important intellectual content (BF, JX, AL, and QW), and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (KC, ZJ, JF, LQ, CL, RW, YS, HY, AL, JX, QW, and BF).

Corresponding authors

Correspondence to Qiping Wen or Boyan Fang.

Ethics declarations

Disclaimer

The funding body had no role in protocol design, statistical analysis, and manuscript preparation.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki and was approved by the Institutional Ethics Committee of Beijing Rehabilitation Hospital, Capital Medical University (approval No. 2021bkky-001).

Consent to participate

Informed consents were obtained from all participants and/or their legal guardian(s) prior to inclusion.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Qiping Wen and Boyan Fang share last authorship.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 128 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, K., Jin, Z., Fang, J. et al. The impact of cerebral small vessel disease burden and its imaging markers on gait, postural control, and cognition in Parkinson’s disease. Neurol Sci 44, 1223–1233 (2023). https://doi.org/10.1007/s10072-022-06563-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-022-06563-1

Keywords

Navigation