Skip to main content

Advertisement

SpringerLink
Log in

Step length predicts executive dysfunction in Parkinson’s disease: a 3-year prospective study

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Cognition and gait appear to be closely related. The chronological interplay between cognitive decline and gait dysfunction is not fully understood. The aim of the present prospective study is investigating whether the dysfunction of specific gait parameters, during specific task and medication conditions, may predict subsequent cognitive impairment in Parkinson’s disease (PD). We evaluated cognition and gait in 39 Parkinsonian patients at an initial assessment and after 3 years. Cognitive performance was evaluated with a neuropsychological battery designed to assess memory, executive/attention, and visuospatial domains. Gait was investigated using a gait analysis system during both the off and on states in the following conditions: (1) normal gait; (2) motor dual task; and (3) cognitive dual task. We used regression models to determine whether gait predicts subsequent cognitive dysfunction. Overall, the cognitive test scores were stable over time with the exception of the executive/attention scores, whereas all gait parameters declined. The step length during the cognitive dual task during the on state at the initial evaluation was the only significant predictor of executive/attention domain dysfunction at follow up. The results were confirmed when executive/attention dysfunction at the initial assessment evaluation was included in the regression model as a covariate. Our longitudinal study offers additional insight into the progression of gait dysfunction, and its chronological relationship with cognitive dysfunction in PD patients. In particular, the present study indicates that step length during a cognitive task when on medication is an independent predictor of future executive/attention decline.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Barone P, Aarsland D, Burn D, Emre M, Kulisevsky J, Weintraub D (2011) Cognitive impairment in nondemented Parkinson’s disease. Mov Disord 26:2483–2495

    Article  Google Scholar 

  2. Muslimović D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245

    Article  Google Scholar 

  3. Delgado-Alvarado M, Gago B, Navalpotro-Gomez I, Jiménez-Urbieta H, Rodriguez-Oroz MC (2016) Biomarkers for dementia and mild cognitive impairment in Parkinson’s disease. Mov Disord 31:861–881

    Article  Google Scholar 

  4. Aarsland D, Larsen JP, Tandberg E, Laake K (2000) Predictors of nursing home placement in Parkinson’s disease: a population-based, prospective study. J Am Geriatr Soc 48:938–942

    Article  CAS  Google Scholar 

  5. Levy BR, Slade MD, Kunkel SR, Kasl SV (2002) Longevity increased by positive self-perceptions of aging. J Pers Soc Psychol 83:261

    Article  Google Scholar 

  6. Mollenhauer B, Rochester L, Chen-Plotkin A, Brooks D (2014) What can biomarkers tell us about cognition in Parkinson’s disease? Mov Disord 29:622–633

    Article  CAS  Google Scholar 

  7. Amboni M, Barone P, Hausdorff JM (2013) Cognitive contributions to gait and falls: evidence and implications. Mov Disord 28:1520–1533

    Article  Google Scholar 

  8. Burn DJ, Rowan EN, Minett T, Sanders J, Myint P, Richardson J et al (2003) Extrapyramidal features in Parkinson’s disease with and without dementia and dementia with Lewy bodies: a cross-sectional comparative study. Mov Disord 18:884–889

    Article  Google Scholar 

  9. Alves G, Larsen JP, Emre M, Wentzel-Larsen T, Aarsland D (2006) Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Mov Disord 21:1123–1130

    Article  Google Scholar 

  10. Uc E, Rizzo M, Anderson S, Qian S, Rodnitzky R, Dawson J (2005) Visual dysfunction in Parkinson disease without dementia. Neurology 65:1907–1913

    Article  CAS  Google Scholar 

  11. Domellöf ME, Elgh E, Forsgren L (2011) The relation between cognition and motor dysfunction in drug-naive newly diagnosed patients with Parkinson’s disease. Mov Disord 26:2183–2189

    Article  Google Scholar 

  12. Amboni M, Barone P, Iuppariello L, Lista I, Tranfaglia R, Fasano A et al (2012) Gait patterns in Parkinsonian patients with or without mild cognitive impairment. Mov Disord 27:1536–1543

    Article  Google Scholar 

  13. Nonnekes J, Timmer MH, de Vries NM, Rascol O, Helmich RC, Bloem BR (2016) Unmasking levodopa resistance in Parkinson’s disease. Mov Disord 31(11):1602–1609

    Article  CAS  Google Scholar 

  14. Verghese J, Wang C, Lipton RB, Holtzer R, Xue X (2007) Quantitative gait dysfunction and risk of cognitive decline and dementia. J Neurol Neurosurg Psychiatry 78:929–935

    Article  Google Scholar 

  15. Mielke MM, Roberts RO, Savica R, Cha R, Drubach DI, Christianson T et al (2013) Assessing the temporal relationship between cognition and gait: slow gait predicts cognitive decline in the Mayo Clinic Study of Aging. J Gerontol A Biol Sci Med Sci 68:929–937

    Article  Google Scholar 

  16. Morris R, Lord S, Bunce J, Burn D, Rochester L (2016) Gait and cognition: mapping the global and discrete relationships in ageing and neurodegenerative disease. Neurosci Biobehav Rev 64:326–345

    Article  Google Scholar 

  17. Rochester L, Galna B, Lord S, Yarnall AJ, Morris R, Duncan G et al (2017) Decrease in Aβ42 predicts dopa-resistant gait progression in early Parkinson disease. Neurology 88(16):1501–1511

    Article  CAS  Google Scholar 

  18. Morris R, Lord S, Lawson RA, Coleman S, Galna B, Duncan GW et al (2017) Gait rather than cognition predicts decline in specific cognitive domains in early Parkinson’s disease. J Gerontol A Biol Sci Med Sci 72(12):1656–1662

    Article  Google Scholar 

  19. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39

    Article  CAS  Google Scholar 

  20. Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22(12):1689–1707

    Article  Google Scholar 

  21. Caltagirone C, Gainotti G, Masullo C, Miceli G (1979) Validity of some neuropsychological tests in the assessment of mental deterioration. Acta Psychiatr Scand 60:50–56

    Article  CAS  Google Scholar 

  22. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626

    Article  CAS  Google Scholar 

  23. Barbarotto R, Laiacona M, Frosio R, Vecchio M, Farinato A, Capitani E (1998) A normative study on visual reaction times and two Stroop colour–word tests. Ital J Neurol Sci 19:161–170

    Article  CAS  Google Scholar 

  24. Manos PJ, Wu R (1994) The ten point clock test: a quick screen and grading method for cognitive impairment in medical and surgical patients. Int J Psychiatry Med 24:229–244

    Article  CAS  Google Scholar 

  25. Spinnler H, Tognoni G (1987) Italian Group on the Neuropsychological Study of Ageing: Italian standardization and classification of neuropsychological tests. Ital J Neurol Sci 6:1–120

    Google Scholar 

  26. Litvan I, Goldman JG, Tröster AI, Schmand BA, Weintraub D, Petersen RC et al (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord 27(3):349–356

    Article  Google Scholar 

  27. Aarsland D, Bronnick K, Williams-Gray C, Weintraub D, Marder K, Kulisevsky J et al (2010) Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis. Neurology 75:1062–1069

    Article  CAS  Google Scholar 

  28. Field A (2013) Discovering statistics using IBM SPSS statistics. Sage, London

    Google Scholar 

  29. Reinoso G, Allen JC Jr, Au WL, Seah SH, Tay KY, Tan LC (2015) Clinical evolution of Parkinson’s disease and prognostic factors affecting motor progression: 9-year follow-up study. Eur J Neurol 22:457–463

    Article  CAS  Google Scholar 

  30. Galna B, Lord S, Burn DJ, Rochester L (2015) Progression of gait dysfunction in incident Parkinson’s disease: impact of medication and phenotype. Mov Disord 30:359–367

    Article  CAS  Google Scholar 

  31. Brown R, Marsden C (1990) Cognitive function in Parkinson’s disease: from description to theory. Trends Neurosci 13:21–29

    Article  CAS  Google Scholar 

  32. Azuma T, Cruz RF, Bayles KA, Tomoeda CK, Montgomery EB (2003) A longitudinal study of neuropsychological change in individuals with Parkinson’s disease. Int J Geriatr Psychiatry 18:1115–1120

    Article  Google Scholar 

  33. Muslimović D, Post B, Speelman JD, De Haan RJ, Schmand B (2009) Cognitive decline in Parkinson’s disease: a prospective longitudinal study. J Int Neuropsychol Soc 15:426–437

    Article  Google Scholar 

  34. Pigott K, Rick J, Xie SX, Hurtig H, Chen-Plotkin A, Duda JE et al (2015) Longitudinal study of normal cognition in Parkinson disease. Neurology 85:1276–1282

    Article  CAS  Google Scholar 

  35. Pedersen KF, Larsen JP, Tysnes O-B, Alves G (2013) Prognosis of mild cognitive impairment in early Parkinson disease: the Norwegian ParkWest study. JAMA Neurol 70:580–586

    Article  Google Scholar 

  36. Santangelo G, Vitale C, Picillo M, Moccia M, Cuoco S, Longo K et al (2015) Mild cognitive impairment in newly diagnosed Parkinson’s disease: a longitudinal prospective study. Parkinsonism Relat Disord 21:1219–1226

    Article  Google Scholar 

  37. Lawson RA, Yarnall AJ, Duncan GW, Breen DP, Khoo TK, Williams-Gray CH et al (2017) Stability of mild cognitive impairment in newly diagnosed Parkinson’s disease. J Neurol Neurosurg Psychiatry 88(8):648–652

    Article  Google Scholar 

  38. Marras C, Armstrong MJ, Meaney CA, Fox S, Rothberg B, Reginold W et al (2013) Measuring mild cognitive impairment in patients with Parkinson’s disease. Mov Disord 28:626–633

    Article  Google Scholar 

  39. Rochester L, Baker K, Nieuwboer A, Burn D (2011) Targeting dopa-sensitive and dopa-resistant gait dysfunction in Parkinson’s disease: Selective responses to internal and external cues. Mov Disord 26:430–435

    Article  Google Scholar 

  40. Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB (2015) Levodopa is a double-edged sword for balance and gait in people with Parkinson’s disease. Mov Disord 30:1361–1370

    Article  CAS  Google Scholar 

  41. Rochester L, Yarnall AJ, Baker MR, David RV, Lord S, Galna B et al (2012) Cholinergic dysfunction contributes to gait disturbance in early Parkinson’s disease. Brain 135:2779–2788

    Article  Google Scholar 

  42. Bohnen NI, Frey KA, Studenski S, Kotagal V, Koeppe RA, Scott PJ et al (2013) Gait speed in Parkinson disease correlates with cholinergic degeneration. Neurology 81:1611–1616

    Article  CAS  Google Scholar 

  43. Blin O, Ferrandez A, Pailhous J, Serratrice G. Sci (1991) Dopa-sensitive and dopa-resistant gait parameters in Parkinson’s disease. J Neurol 103:51–54

    CAS  Google Scholar 

  44. Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM (2003) Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J Neurol Sci 212:47–53

    Article  Google Scholar 

  45. Lord S, Howe T, Greenland J, Simpson L, Rochester L (2011) Gait variability in older adults: a structured review of testing protocol and clinimetric properties. Gait Posture 34:443–450

    Article  Google Scholar 

  46. Lord S, Galna B, Rochester L (2013) Moving forward on gait measurement: toward a more refined approach. Mov Disord 28(11):1534–1543

    Article  Google Scholar 

  47. Lord S, Galna B, Coleman S, Yarnall A, Burn D, Rochester L (2014) Cognition and gait show a selective pattern of association dominated by phenotype in incident Parkinson’s disease. Front Aging Neurosci 6:249

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine and Surgery “Scuola Medica Salernitana”, Center for Neurodegenerative Diseases, University of Salerno, Via S. Allende, 1, 84081, Baronissi, SA, Italy

    Marianna Amboni, Marina Picillo & Paolo Barone

  2. Istituto di Diagnosi e Cura Hermitage-Capodimonte, Via Cupa delle Tozzole, 2, 80131, Naples, Italy

    Marianna Amboni, Rosaria Rucco, Pasquale Varriale, Carmine Vitale & Giuseppe Sorrentino

  3. DIETI, University of Naples, “Federico II”, Naples, Italy

    Luigi Iuppariello & Mario Cesarelli

  4. Department of Pediatric Rehabilitation, Santobono-Pausilipon Children’s Hospital, Naples, Italy

    Luigi Iuppariello

  5. Neurological and Stroke Unit, Centro Traumatologico Ortopedico Hospital AORN “Ospedali dei Colli”, Naples, Italy

    Alessandro Iavarone

  6. Morton and Gloria Shulman Movement Disorders Clinic and the Edmond J. Safra Program in Parkinson’s Disease, Division of Neurology, Toronto Western Hospital, UHN, University of Toronto, Toronto, ON, Canada

    Alfonso Fasano

  7. Krembil Research Institute, Toronto, ON, Canada

    Alfonso Fasano

  8. Department of Primary Care and Public Health, Imperial College, London, UK

    Raffaele Palladino

  9. Department of Public Health, University of Naples, “Federico II”, Naples, Italy

    Raffaele Palladino

  10. Department of Motor Sciences and Wellness, University of Naples Parthenope, Naples, Italy

    Rosaria Rucco, Ilaria Lista, Pasquale Varriale, Carmine Vitale & Giuseppe Sorrentino

Authors
  1. Marianna Amboni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luigi Iuppariello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandro Iavarone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alfonso Fasano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raffaele Palladino
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosaria Rucco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marina Picillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ilaria Lista
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pasquale Varriale
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Carmine Vitale
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mario Cesarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Giuseppe Sorrentino
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Paolo Barone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marianna Amboni.

Ethics declarations

Conflicts of interest

MA, LI, AI, AF, RP, RR, MP, IL, PV, CV, MC, and GS have no financial disclosures to report; PB reports personal fees from Acorda, Union Chimique Belge, Zambon, Grants from Abbvie, Biotie, and Zambon. On behalf of all authors, the corresponding author states that there is no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amboni, M., Iuppariello, L., Iavarone, A. et al. Step length predicts executive dysfunction in Parkinson’s disease: a 3-year prospective study. J Neurol 265, 2211–2220 (2018). https://doi.org/10.1007/s00415-018-8973-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-018-8973-x

Keywords

Search

Navigation