Skip to main content
SpringerLink
Log in

Gait performance and non-motor symptoms burden during dual-task condition in Parkinson’s disease

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

Abstract

Introduction

Impaired gait is observed in patients with Parkinson’s disease (PD) in both single-task (ST) and dual-task (DT) conditions. Non-motor symptoms (NMSs), another vital symptom future experienced along the PD disease trajectory, contribute to gait performance in PD. However, whether DT gait performance is indicative of NMS burden (NMSB) remains unknown. This study investigated correlation between NMS and DT gait performance and whether NMSB is reflected in the DT effects (DTEs) of gait parameters in PD.

Methods

Thirty-three idiopathic PD participants were enrolled in this study; the median H-Y staging was 2.5. NMSB was assessed by Non-motor Symptoms Scale (NMSS). Spatiotemporal gait parameters under ST and DT conditions were evaluated by wearable sensors. Gait parameters under ST and DT conditions and DTEs of gait parameters were compared across NMSB groups. The associations between NMS and DTEs of gait parameters were analyzed by correlation analysis and linear regression models.

Results

Compared to PD patients with mild-moderate NMSB, the severe-very severe NMSB group showed slower gait speed and shorter stride length under both ST and DT conditions (p < 0.05). DT had significantly negative effect on gait parameters in PD patients, including gait speed, stride length, and gait cycle duration (p < 0.05). PD patients with mild-moderate NMSB showed larger DTEs of cadence and bilateral gait cycle duration (p < 0.05). DTEs of bilateral gait cycle duration and swing phase on the more affected (MA) side were significantly correlated with NMSS scores (∣rSp∣ ≥ 0.3, p < 0.05). Gait cycle duration on the less affected (LA) side explained 43% of the variance in NMSS scores, when accounting for demographic and clinical confounders (β =  − 1.095 95% CI − 4.061 ~  − 0.058, p = 0.044; adjusted R2 = 0.434).

Conclusion

DT gait performance could reflect NMSB in PD patients at early stage, and gait cycle duration is a valuable gait parameter to further investigate and to provide more evidence for PD management.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet 386:896–912. https://doi.org/10.1016/s0140-6736(14)61393-3

    Article  CAS  Google Scholar 

  2. Nardello F, Bombieri F, Tinazzi M, Schena F, Pellegrini B (2017) Metabolic and kinematic parameters during walking with poles in Parkinson’s disease. J Neurol 264:1785–1790. https://doi.org/10.1007/s00415-017-8568-y

    Article  Google Scholar 

  3. Glover A, Pillai L, Doerhoff S, Virmani T (2020) Differential gait decline in Parkinson’s disease enhances discrimination of gait freezers from non-freezers. J Parkinsons Dis 10:1657–1673. https://doi.org/10.3233/jpd-201961

    Article  CAS  Google Scholar 

  4. Pistacchi M, Gioulis M, Sanson F, De Giovannini E, Filippi G, Rossetto F, ZambitoMarsala S (2017) Gait analysis and clinical correlations in early Parkinson’s disease. Funct Neurol 32:28–34. https://doi.org/10.11138/fneur/2017.32.1.028

    Article  CAS  Google Scholar 

  5. Zanardi A, da Silva E, Costa R, Passos-Monteiro E, Dos Santos I, Kruel L, Peyré-Tartaruga L (2021) Gait parameters of Parkinson’s disease compared with healthy controls: a systematic review and meta-analysis. Sci Rep 11:752. https://doi.org/10.1038/s41598-020-80768-2

    Article  CAS  Google Scholar 

  6. Iansek R, Danoudis M, Bradfield N (2013) Gait and cognition in Parkinson’s disease: implications for rehabilitation. Rev Neurosci 24:293–300. https://doi.org/10.1515/revneuro-2013-0006

    Article  Google Scholar 

  7. Baiano C, Barone P, Trojano L, Santangelo G (2020) Prevalence and clinical aspects of mild cognitive impairment in Parkinson’s disease: a meta-analysis. Mov Disord : Off J Mov Disord Soc 35:45–54. https://doi.org/10.1002/mds.27902

    Article  Google Scholar 

  8. Penko AL, Streicher MC, Koop MM, Dey T, Rosenfeldt AB, Bazyk AS, Alberts JL (2018) Dual-task interference disrupts Parkinson’s gait across multiple cognitive domains. Neuroscience 379:375–382. https://doi.org/10.1016/j.neuroscience.2018.03.021

    Article  CAS  Google Scholar 

  9. Raffegeau T, Krehbiel L, Kang N, Thijs F, Altmann L, Cauraugh J, Hass C (2019) A meta-analysis: Parkinson’s disease and dual-task walking. Parkinsonism Relat Disord 62:28–35. https://doi.org/10.1016/j.parkreldis.2018.12.012

    Article  Google Scholar 

  10. Chaudhuri K, Martinez-Martin P, Brown R, Sethi K, Stocchi F, Odin P, Ondo W, Abe K, Macphee G, Macmahon D, Barone P, Rabey M, Forbes A, Breen K, Tluk S, Naidu Y, Olanow W, Williams A, Thomas S, Rye D, Tsuboi Y, Hand A, Schapira A (2007) The metric properties of a novel Non-Motor Symptoms Scale for Parkinson’s disease: results from an international pilot study. Mov Disord : Off J Mov Disord Soc 22:1901–1911. https://doi.org/10.1002/mds.21596

    Article  Google Scholar 

  11. Ray Chaudhuri K, Rojo J, Schapira A, Brooks D, Stocchi F, Odin P, Antonini A, Brown R, Brown R, Martinez-Martin P (2013) A proposal for a comprehensive grading of Parkinson’s disease severity combining motor and non-motor assessments: meeting an unmet need. PLoS ONE 8:e57221. https://doi.org/10.1371/journal.pone.0057221

    Article  CAS  Google Scholar 

  12. Gassner H, Marxreiter F, Steib S, Kohl Z, Schlachetzki JCM, Adler W, Eskofier BM, Pfeifer K, Winkler J, Klucken J (2017) Gait and cognition in Parkinson’s disease: cognitive impairment is inadequately reflected by gait performance during dual task. Front Neurol 8:550. https://doi.org/10.3389/fneur.2017.00550

    Article  Google Scholar 

  13. Salazar RD, Ren X, Ellis TD, Toraif N, Barthelemy OJ, Neargarder S, Cronin-Golomb A (2017) Dual tasking in Parkinson’s disease: cognitive consequences while walking. Neuropsychology 31:613–623. https://doi.org/10.1037/neu0000331

    Article  Google Scholar 

  14. Johansson H, Ekman U, Rennie L, Peterson DS, Leavy B, Franzen E (2021) Dual-task effects during a motor-cognitive task in Parkinson’s disease: patterns of prioritization and the influence of cognitive status. Neurorehabil Neural Repair 35:356–366. https://doi.org/10.1177/1545968321999053

    Article  Google Scholar 

  15. Dragasevic-Miskovic NT, Bobic V, Kostic M, Stankovic I, Radovanovic S, Dimitrijevic K, Svetel M, Petrovic I, Duric-Jovicic M (2021) Impact of depression on gait variability in Parkinson’s disease. Clin Neurol Neurosurg 200:106324. https://doi.org/10.1016/j.clineuro.2020.106324

    Article  Google Scholar 

  16. Ehgoetz Martens K, Silveira C, Intzandt B, Almeida Q (2018) Overload from anxiety: a non-motor cause for gait impairments in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 30:77–80. https://doi.org/10.1176/appi.neuropsych.16110298

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  19. Vítečková S, Horáková H, Poláková K, Krupička R, Růžička E, Brožová H (2020) Agreement between the GAITRite system and the wearable sensor BTS G-Walk for measurement of gait parameters in healthy adults and Parkinson’s disease patients. PeerJ 8:e8835. https://doi.org/10.7717/peerj.8835

    Article  Google Scholar 

  20. Jagos H, Pils K, Haller M, Wassermann C, Chhatwal C, Rafolt D, Rattay F (2017) Mobile gait analysis via eSHOEs instrumented shoe insoles: a pilot study for validation against the gold standard GAITRite. J Med Eng Technol 41:375–386. https://doi.org/10.1080/03091902.2017.1320434

    Article  Google Scholar 

  21. Kelly V, Janke A, Shumway-Cook A (2010) Effects of instructed focus and task difficulty on concurrent walking and cognitive task performance in healthy young adults. Exp Brain Res 207:65–73. https://doi.org/10.1007/s00221-010-2429-6

    Article  Google Scholar 

  22. Vitorio R, Hasegawa N, Carlson-Kuhta P, Nutt JG, Horak FB, Mancini M, Shah VV (2021) Dual-task costs of quantitative gait parameters while walking and turning in people with Parkinson’s disease: beyond gait speed. J Parkinsons Dis 11:653–664. https://doi.org/10.3233/JPD-202289

    Article  Google Scholar 

  23. Vitorio R, Stuart S, Mancini M (2020) Executive control of walking in people with Parkinson’s disease with freezing of gait. Neurorehabil Neural Repair 34:1138–1149. https://doi.org/10.1177/1545968320969940

    Article  Google Scholar 

  24. Huang C, Chen Y, Hwang I, Wu R (2018) Improving dual-task control with a posture-second strategy in early-stage parkinson disease. Arch Phys Med Rehabil 99:1540-1546.e1542. https://doi.org/10.1016/j.apmr.2018.02.013

    Article  Google Scholar 

  25. Huang X, Ng SY, Chia NS, Setiawan F, Tay KY, Au WL, Tan EK, Tan LC (2019) Non-motor symptoms in early Parkinson’s disease with different motor subtypes and their associations with quality of life. Eur J Neurol 26:400–406. https://doi.org/10.1111/ene.13803

    Article  CAS  Google Scholar 

  26. Ren J, Hua P, Pan C, Li Y, Zhang L, Zhang W, Xu P, Zhang M, Liu W (2020) Non-motor symptoms of the postural instability and gait difficulty subtype in de novo Parkinson’s disease patients: a cross-sectional study in a single center. Neuropsychiatr Dis Treat 16:2605–2612. https://doi.org/10.2147/ndt.S280960

    Article  Google Scholar 

  27. Onder H, Ozyurek O (2021) The impact of distinct cognitive dual-tasks on gait in Parkinson’s disease and the associations with the clinical features of Parkinson’s disease. Neurol Sci 42:2775–2783. https://doi.org/10.1007/s10072-020-04874-9

    Article  Google Scholar 

  28. Amundsen-Huffmaster SL, Petrucci MN, Linn-Evans ME, Chung JW, Howell MJ, Videnovic A, Tuite PJ, Cooper SE, MacKinnon CD (2021) REM sleep without atonia and gait impairment in people with mild-to-moderate Parkinson’s disease. J Parkinsons Dis 11:767–778. https://doi.org/10.3233/JPD-202098

    Article  CAS  Google Scholar 

  29. Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K, Cockburn J (2011) Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 35:715–728. https://doi.org/10.1016/j.neubiorev.2010.08.008

    Article  Google Scholar 

  30. Cho C, Kunin M, Kudo K, Osaki Y, Olanow C, Cohen B, Raphan T (2010) Frequency-velocity mismatch: a fundamental abnormality in parkinsonian gait. J Neurophysiol 103:1478–1489. https://doi.org/10.1152/jn.00664.2009

    Article  Google Scholar 

  31. Rietdijk CD, Perez-Pardo P, Garssen J, van Wezel RJ, Kraneveld AD (2017) Exploring Braak’s hypothesis of Parkinson’s disease. Front Neurol 8:37. https://doi.org/10.3389/fneur.2017.00037

    Article  Google Scholar 

  32. Kim S, Kwon S, Kam T, Panicker N, Karuppagounder S, Lee S, Lee J, Kim W, Kook M, Foss C, Shen C, Lee H, Kulkarni S, Pasricha P, Lee G, Pomper M, Dawson V, Dawson T, Ko H (2019) Transneuronal propagation of pathologic α-synuclein from the gut to the brain models Parkinson’s disease. Neuron 103:627-641.e627. https://doi.org/10.1016/j.neuron.2019.05.035

    Article  CAS  Google Scholar 

  33. Donoghue O, O’Hare C, King-Kallimanis B, Kenny R (2015) Antidepressants are independently associated with gait deficits in single and dual task conditions. Am J Geriatr Psychiatry : Off J Am Assoc Geriatr Psychiatry 23:189–199. https://doi.org/10.1016/j.jagp.2014.04.005

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank all the participants who were enrolled in this study.

Funding

The study was supported by grants from the National Key Technology Research and Development Program of China (2018YFC2002300, 2018YFC2002302, 2020YFC2004102), and the National Nature Science Foundation of China (NSFC:81972144, 31872785, 81972148).

Author information

Authors and Affiliations

  1. Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Meimei Zhang, Yawen Gan, Xuemei Wang, Zhan Wang & Tao Feng

  2. China National Clinical Research Center for Neurological Diseases (NCRC-ND), Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, No. 119 South 4th Ring West Road, Fengtai District, Beijing, 100070, China

    Tao Feng & Yumei Zhang

  3. China National Clinical Research Center for Neurological Diseases, Department of Rehabilitation, Beijing Tiantan Hospital, Capital Medical University, No. 119 South 4th Ring West Road, Fengtai District, Beijing, 100070, China

    Yumei Zhang

Authors
  1. Meimei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yawen Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuemei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tao Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yumei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors listed have made a substantial, direct, and intellectual contribution to the work, and approved it for publication.

Corresponding authors

Correspondence to Tao Feng or Yumei Zhang.

Ethics declarations

Ethical approval

The studies involving human participants were reviewed and approved by the Ethics Committee of the Beijing Tiantan Hospital. The participants provided their written informed consent to participate in this study.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher's note

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

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 KB)

Rights and permissions

Springer Nature or its licensor 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

Zhang, M., Gan, Y., Wang, X. et al. Gait performance and non-motor symptoms burden during dual-task condition in Parkinson’s disease. Neurol Sci 44, 181–190 (2023). https://doi.org/10.1007/s10072-022-06411-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-022-06411-2

Keywords

Search

Navigation