Skip to main content
Log in

Association of freezing of gait and clinical features in patients with Parkinson’s disease

  • Original article
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

Freezing of gait (FOG) is a disabling symptom that affects the quality of life of patients with Parkinson’s disease (PD) and its pathophysiology is not fully understood yet. The aim of the present study is to evaluate the relationship between FOG and other clinical characteristics in patients with PD. The clinical characteristics, modified Hoehn and Yahr (mHY) stages, Unified Parkinson’s Disease Rating Scale (UPDRS) scores, and total Freezing of Gait Questionnaire (FOG-Q) scores of the patients with PD were recorded. FOG-Q item 1.3 was used to evaluate patients with or without FOG. A total of 65 patients with PD (32 with FOG and 33 without FOG) were included to the study. Disease duration was longer, mHY stages were higher, bradykinesia and dyskinesia were more common in patients with FOG compared to patients without (p = 0.001, p = 0.036, p = 0.019 and p = 0.021; respectively). Patients with FOG had lower UPDRS part III tremor subscores (p = 0.020), although gait, postural balance subscores and part IV motor fluctuations scores were higher (p = 0.003, p = 0.023 and p < 0.001; respectively). A positive correlation was found between FOG-Q scores and mHY stages (p < 0.001), UPDRS part II and III total scores (p = 0.020 and p = 0.001) and part III bradykinesia, and gait and postural balance subscores (p = 0.003, p = 0.036 and p = 0.003, respectively), and part IV motor fluctuation scores (p = 0.006). The results of the present study point to an association between FOG and bradykinesia rather than tremor, prolonged disease duration and advanced disease stage reflecting its association with more severe and extensive neurodegenerative processes.

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.

Similar content being viewed by others

References

  1. Shine JM, Naismith SL, Lewis SJ (2011) The pathophysiological mechanisms underlying freezing of gait in Parkinson’s disease. J Clin Neurosci 18:1154–1157. https://doi.org/10.1016/j.jocn.2011.021.007

    Article  CAS  PubMed  Google Scholar 

  2. Okuma Y, Yanagisawa N (2008) The clinical spectrum of freezing of gait in Parkinson’s disease. Mov Disord 23(Suppl 2):S426–430. https://doi.org/10.1002/mds.21934(Erratum. In: (2008) Mov Disord 23:1639-1640)

    Article  PubMed  Google Scholar 

  3. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744. https://doi.org/10.1016/S1474-4422(11)70143-0

    Article  PubMed  PubMed Central  Google Scholar 

  4. Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154. https://doi.org/10.1016/j.parkreldis.2011.09.006

    Article  PubMed  Google Scholar 

  5. Giladi N, Nieuwboer A (2008) Understanding and treating freezing of gait in parkinsonism, proposed working definition, and setting the stage. Mov Disord 23(Suppl 2):S423–425. https://doi.org/10.1002/mds.21927.23(S2)

    Article  PubMed  Google Scholar 

  6. Okuma Y (2014) Practical approach to freezing of gait in Parkinson’s disease. Pract Neurol 14:222–230. https://doi.org/10.1136/practneurol-2013-000743

    Article  PubMed  Google Scholar 

  7. Fasano A, Herman T, Tessitore A, Strafella AP, Bohnen NI (2015) Neuroimaging of freezing of gait. J Parkinsons Dis 5:241–254. https://doi.org/10.3233/JPD-150536

    Article  PubMed  PubMed Central  Google Scholar 

  8. Heremans E, Nieuwboer A, Vercruysse S (2013) Freezing of gait in Parkinson’s disease: where are we now? Curr Neurol Neurosci Rep 13:350. https://doi.org/10.1007/s11910-013-0350-7

    Article  PubMed  Google Scholar 

  9. Bharti K, Suppa A, Pietracupa S, Upadhyay N, Giannì C, Leodori G, Di Biasio F, Modugno N, Petsas N, Grillea G, Zampogna A, Berardelli A, Pantano P (2018) Abnormal cerebellar connectivity patterns in patients with parkinson’s disease and freezing of gait. Cerebellum. https://doi.org/10.1007/s12311-018-0988-4(Epub ahead of print)

    Article  Google Scholar 

  10. Contreras A, Grandas F (2012) Risk factors for freezing of gait in Parkinson’s disease. J Neurol Sci 320:66–71. https://doi.org/10.1016/j.jns.2012.06.018

    Article  PubMed  Google Scholar 

  11. Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B, Paleacu D, Korczyn AD (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm (Vienna) 108:53–61

    Article  CAS  Google Scholar 

  12. Lamberti P, Armenise S, Castaldo V, de Mari M, Iliceto G, Tronci P, Serlenga L (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38:297–301

    Article  CAS  Google Scholar 

  13. Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M, Tanner C, Parkinson Study Group (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56:1712–1721

    Article  CAS  Google Scholar 

  14. Perez-Lloret S, Negre-Pages L, Damier P, Delval A, Derkinderen P, Destée A, Meissner WG, Schelosky L, Tison F, Rascol O (2014) Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease. JAMA Neurol 71:884–890. https://doi.org/10.1001/jamaneurol.2014.753

    Article  PubMed  Google Scholar 

  15. Forsaa EB, Larsen JP, Wentzel-Larsen T, Alves G (2015) A 12-year population-based study of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 21:254–258. https://doi.org/10.1016/j.parkreldis.2014.12.020

    Article  CAS  PubMed  Google Scholar 

  16. Macht M, Kaussner Y, Möller JC, Stiasny-Kolster K, Eggert KM, Krüger HP, Ellgring H (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22:953–956

    Article  Google Scholar 

  17. Choi SM, Jung HJ, Yoon GJ, Kim BC (2018) Factors associated with freezing of gait in patients with Parkinson’s disease. Neurol Sci. https://doi.org/10.1007/s10072-018-3625-6(Epub ahead of print)

    Article  PubMed  Google Scholar 

  18. García-Ruiz PJ, Del Val J, Fernández IM, Herranz A (2012) What factors influence motor complications in Parkinson disease?: a 10-year prospective study. Clin Neuropharmacol 35:1–5. https://doi.org/10.1097/WNF.0b013e31823dec73

    Article  PubMed  Google Scholar 

  19. Amboni M, Stocchi F, Abbruzzese G, Morgante L, Onofrj M, Ruggieri S, Tinazzi M, Zappia M, Attar M, Colombo D, Simoni L, Ori A, Barone P, Antonini A, DEEP Study Group (2015) Prevalence and associated features of self-reported freezing of gait in Parkinson disease: the DEEP FOG study. Parkinsonism Relat Disord 21:644–649. https://doi.org/10.1016/j.parkreldis.2015.03.028

    Article  CAS  PubMed  Google Scholar 

  20. Ou R, Guo X, Song W, Cao B, Yang J, Wei Q, Shao N, Shang H (2014) Freezing of gait in Chinese patients with Parkinson disease. J Neurol Sci 345:56–60

    Article  Google Scholar 

  21. Zhang H, Yin X, Ouyang Z, Chen J, Zhou S, Zhang C, Pan X, Wang S, Yang J, Feng Y, Yu P, Zhang QA (2016) Prospective study of freezing of gait with early Parkinson disease in Chinese patients. Medicine (Baltimore) 95:e4056. https://doi.org/10.1097/MD.0000000000004056

    Article  Google Scholar 

  22. Ehgoetz Martens KA, Lukasik EL, Georgiades MJ, Gilat M, Hall JM, Walton CC, Lewis SJG (2018) Predicting the onset of freezing of gait: a longitudinal study. Mov Disord 33:128–135. https://doi.org/10.1002/mds.27208

    Article  PubMed  Google Scholar 

  23. Hall JM, Shine JM, Walton CC, Gilat M, Kamsma YP, Naismith SL, Lewis SJ (2014) Early phenotypic differences between Parkinson’s disease patients with and without freezing of gait. Parkinsonism Relat Disord 20:604–607. https://doi.org/10.1016/j.parkreldis.2014.02.028(Erratum. In: (2014) Parkinsonism Relat Disord. 20:1040)

    Article  CAS  PubMed  Google Scholar 

  24. Bartels AL, Balash Y, Gurevich T, Schaafsma JD, Hausdorff JM, Giladi N (2003) Relationship between freezing of gait (FOG) and other features of Parkinson’s: FOG is not correlated with bradykinesia. J Clin Neurosci 10:584–588

    Article  CAS  Google Scholar 

  25. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  CAS  Google Scholar 

  26. Factor SA, Steenland NK, Higgins DS, Molho ES, Kay DM, Montimurro J, Rosen AR, Zabetian CP, Payami H (2011) Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry 82(5):564–568. https://doi.org/10.1136/jnnp.2010.222042

    Article  PubMed  Google Scholar 

  27. Riederer P, Jellinger KA, Kolber P, Hipp G, Sian-Hülsmann J, Krüger R (2018) Lateralisation in Parkinson disease. Cell Tissue Res 373:297–312. https://doi.org/10.1007/s00441-018-2832-z

    Article  CAS  PubMed  Google Scholar 

  28. Ehgoetz Martens KA, Pieruccini-Faria F, Silveira CR, Almeida QJ (2013) The contribution of optic flow to freezing of gait in left- and right-PD: different mechanisms for a common phenomenon? Parkinsonism Relat Disord 19:1046–1048. https://doi.org/10.1016/j.parkreldis.2013.06.011

    Article  PubMed  Google Scholar 

  29. Pieruccini-Faria F, Ehgoetz Martens KA, Silveira CR, Jones JA, Almeida QJ (2015) Side of basal ganglia degeneration influences freezing of gait in Parkinson’s disease. Behav Neurosci 129:214–218. https://doi.org/10.1037/bne0000039

    Article  PubMed  Google Scholar 

  30. Plotnik M, Hausdorff JM (2008) The role of gait rhythmicity and bilateral coordination of stepping in the pathophysiology of freezing of gait in Parkinson’s disease. Mov Disord 23(Suppl 2):S444–450. https://doi.org/10.1002/mds.21984(Erratum. In: (2008) Mov Disord 23:1639–1640)

    Article  PubMed  Google Scholar 

  31. Frazzitta G, Pezzoli G, Bertotti G, Maestri R (2013) Asymmetry and freezing of gait in parkinsonian patients. J Neurol 260:71–76. https://doi.org/10.1007/s00415-012-6585-4

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hayat Güven.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was carried out according to the 1964 Helsinki Declaration and its later amendments or comparable ethical standards and with the ethical standards of the institutional and national research committee. The study was approved by the Institutional Ethics Committee.

Informed constent

All patients participating in the study provided a written informed consent.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aktürk, T., Güven, H., Güven, B. et al. Association of freezing of gait and clinical features in patients with Parkinson’s disease. Acta Neurol Belg 121, 153–159 (2021). https://doi.org/10.1007/s13760-019-01217-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-019-01217-0

Keywords

Navigation