Advertisement

Journal of Neurology

, Volume 253, Supplement 7, pp vii27–vii32 | Cite as

Freezing of gait in Parkinson’s disease

  • Yasuyuki Okuma
Article

Abstract

Freezing of Gait (FOG) is one of the most disabling and least understood symptoms in Parkinson’s disease (PD), and is usually observed in the advanced stage of the disease. FOG can be experienced on turning, in narrow spaces, whilst reaching a destination, and in stressful situations. FOG is commonly observed in the “off” state, but it can also be observed in the “on” state. Dual tasking (cognitive load) aggravates FOG. Visual or auditory cues often resolve FOG. Analysis of gait revealed that the rhythm of stepping suddenly jumps into high frequency (4–5 Hz) in FOG (hastening), and that floor reaction forces are disregulated. Stride-to-stride variability is increased in FOG. Hastening phenomenon was reported not only in PD patients but also in patients with striatal lesions. The basal ganglia and its frontal projections may be one of the essential lesion sites for FOG.A recent study using single-photon emission tomography (SPECT) revealed enhanced lateral premotor cortex (PMC) activity during paradoxical gait in PD, suggesting that PMC can compensate for the impaired function of the medial frontal cortex when cued by visual input. Treatment of FOG includes behavioural, medical, and surgical approaches. Tricks of all kinds (including external cues) are effective therapeutic approaches. If FOG occurs predominantly in the “off” state, dopaminergic therapy can be increased. For “on” freezing or if “on” response is otherwise optimised, the dose of the dopaminergic agent may be manipulated, but it could lead to the deterioration of parkinsonism. Deep brain stimulation of the STN often alleviates FOG in the “off” state.

Key words

Freezing of gait Parkinson’s disease 

References

  1. 1.
    Ambani L,Van Woert M (1973) Start hesitation—a side effect of long-term levodopa therapy. N Eng J Med 288:1113–1115CrossRefGoogle Scholar
  2. 2.
    Achiron AI Ziv, Goren M et al. (1993) Primary progressive freezing gait. Mov Disord 8:293–297PubMedCrossRefGoogle Scholar
  3. 3.
    Atchison PR, Thompson PD, Frackowiak RSJ, Marsden CD (1993) The syndrome of gait ignition failure: A report of six cases. Mov Disord 8:285–292PubMedCrossRefGoogle Scholar
  4. 4.
    Bakker M, Esselink RA, Munneke M, Limousin-Dowsey P, Speelman HD, Bloem BR (2004) Effects of stereotactic neurosurgery on postural instability and gait in Parkinson’s disease. Mov Disord 19:1092–1099PubMedCrossRefGoogle Scholar
  5. 5.
    Barbeau A (1976) Six years of high level levodopa therapy in severely akinetic parkinsonian patients. Arch Neurol 33:333–338PubMedGoogle Scholar
  6. 6.
    Bartels, AL, Balash Y, Gurevich T et al. (2003) Relationships between freezing of gait (FOG) and other features of Parkinson’s disease. FOG is not correlated with bradykinesia. J Clin Neurosci 10:584–588PubMedCrossRefGoogle Scholar
  7. 7.
    Bejjani B, Gervais D, Arnulf I et al. (2000) Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation. J Neurol Neurosurg psychiatry 68:595–600PubMedCrossRefGoogle Scholar
  8. 8.
    Bloem BR, Hausdorff JM, Visser JE, Giladi N (2004) Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord 19:871–884PubMedCrossRefGoogle Scholar
  9. 9.
    Brichetto B, Pelosin A, Marchese A, Abbruzzese G (2006) Evaluation of physical therapy in parkinsonian patients with freezing of gait: a pilot study. Clin Rehabil 20:31–35PubMedCrossRefGoogle Scholar
  10. 10.
    Camicioli R, Oken BS, Sexton G et al. (1998) Verbal fruency task affects gait in Parkinson’s disease with motor freezing. J Geriatr Psychiatry Neurol 11:181–185PubMedGoogle Scholar
  11. 11.
    Cubo E, Moore CG, Leurgans S, Goetz CG (2003) Wheeled and standard walkers in Parkinson’s disease patients with gait freezing. Parkinsonism Rel Disord 10:9–14CrossRefGoogle Scholar
  12. 12.
    Cubo E, Leurgans S, Goetz CG (2004) Short-term and practice effects of metronome pacing in Parkinson’s disease patients with gait freezing while in the “on” state: randomized single blind evaluation. Parkinsonism Rel Disord 10:507–510CrossRefGoogle Scholar
  13. 13.
    Davis JT, Lyons KE, Pahwa R (2006) Freezing of gait after bilateral subthalamic nucleus stimulation for Parkinson’s disease. Clin Neurol Neurosurg 108:461–464PubMedCrossRefGoogle Scholar
  14. 14.
    Dietz MA, Goetz CG, Stebbins GT (1990) Evaluation of a modified inverted walking stick as a treatment for parkinsonian freezing episodes. Mov Disord 5:243–247PubMedCrossRefGoogle Scholar
  15. 15.
    Fabre N, Brefel C, Sabatini U et al. (1998) Normal frontal perfusion in patients with frozen gait. Mov Disord 13:677–683PubMedCrossRefGoogle Scholar
  16. 16.
    Factor S, Jennings DL, Molho ES, Marek KL (2002) The natural history of the syndrome of primary progressive freezing gait. Arch Neurol 59:1778–1783PubMedCrossRefGoogle Scholar
  17. 17.
    Fahn S (1995) The freezing phenomenon in parkinsonism. Adv Neurol 67:53–63PubMedGoogle Scholar
  18. 18.
    Fernandez HH, Lannon MC, Trieschenann ME, Friedman JH (2004) Botulinum toxin type B for the gait freezing in Parkinson’s disease. Med Sci Monit 10:282–284Google Scholar
  19. 19.
    Ferrarin M, Brambilla M, Garavello L et al. (2004) Microprocessor-controlled optical stimulating device to improve the gait of patients with Parkinson’s disease. Med Biol Eng Comput 42:328–332PubMedCrossRefGoogle Scholar
  20. 20.
    Fukuyama H, Ouchi Y, Matsuzaki S et al. (1997) Brain functional activity during gait in normal subjects: a SPECT study. Neurosci Lett 228:183–186PubMedCrossRefGoogle Scholar
  21. 21.
    Giladi N, McMahon D, Przedborski et al. (1992) Motor blocks in Parkinson’s disease. Neurology 42:333–339PubMedGoogle Scholar
  22. 22.
    Giladi N, Kao R, Fahn S (1997) Freezing phenomenon in patients with parkinsonian syndromes. Mov Disord 12:302–305PubMedCrossRefGoogle Scholar
  23. 23.
    Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn AD (2000) Construction of freezing of gait questionnaire for patients with parkinsonism. Parkinsonism Rel Disord 6:165–170CrossRefGoogle Scholar
  24. 24.
    Giladi N, Shabtai H, Rozenberg E, Shabtai E (2001) Gait festination in Parkinson’s disease. Parkinsonism Rel Disord 7:135–138CrossRefGoogle Scholar
  25. 25.
    Giladi N (2001) Freezing of gait. Clinical overview. Adv Neurol 87:191–197PubMedGoogle Scholar
  26. 26.
    Giladi N, Treves TA, Simon ES, Shabtai H et al. (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm 108:53–61PubMedCrossRefGoogle Scholar
  27. 27.
    Giladi N, Guerevich T, Shabtai H, Paleacu D, Simon ES (2001) The effect of botulinum toxin injections to the calf muscles on freezing of gait in parkinsonism: a pilot study. J Neurol 248:572–576PubMedCrossRefGoogle Scholar
  28. 28.
    Giladi N, McDermott MP, Fahn S et al. (2001) Freezing of gait in Parkinson’s disease; prospective assessment in the DATATOP cohort. Neurology 56:1712–1721PubMedGoogle Scholar
  29. 29.
    Gurevich T, Giladi N (2003) Freezing of gait in multiple system atrophy (MSA). Parkinsonism Rel Disord 9:169–174CrossRefGoogle Scholar
  30. 30.
    Hanakawa T, Katsumi Y, Fukuyama H et al. (1999) Mechanism underlying gait disturbance in Parkinson’s disease: a Single photon emission computed tomography study. Brain 112:1271–1282CrossRefGoogle Scholar
  31. 31.
    Hanakawa T, Fukuyama H, Katsumi Y et al. (1999) Enhanced lateral premotor activity during paradoxical gait in Parkinson’s disease. Ann Neurol 45:329–336PubMedCrossRefGoogle Scholar
  32. 32.
    Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMedGoogle Scholar
  33. 33.
    Imai H (1980) Syndrome of pure akinesia or freezing phenomenon without rigidity and tremor and with no effect by L-Dopa therapy. Adv Neurol Res (Tokyo) 24:838–848Google Scholar
  34. 34.
    Imai H, Narabayashi H, Sakata E (1986) “Pure akinesia” and the later added supranuclear ophthalmoplegia. Adv Neurol 45:207–212Google Scholar
  35. 35.
    Imai H (1993) Festination and freezing. Rinsho Shinkeigaku 33:1307–1309PubMedGoogle Scholar
  36. 36.
    Jiang Y, Norman KE (2006) Effects of visual and auditory cues on gait initiation in people with Parkinson’s disease. Clin Rehabil 20:36–45PubMedCrossRefGoogle Scholar
  37. 37.
    Katayama Y, Kasai M, Oshima H, Fukaya C, Yamamoto T (2000) Effects of anterodorsal pallidal stimulation on gait freezing (kinesia paradoxa) in Parkinson’s disease. Stereotact Funct Neurosurg 74:99–105PubMedCrossRefGoogle Scholar
  38. 38.
    Kompoliti K, Goetz CG, Leurgans S, Morrissey M, Siegel IM (2000) “On” freezing in Parkinson’s disease: resistance to visual cue walking devices. Mov Disord 15:309–312PubMedCrossRefGoogle Scholar
  39. 39.
    Lamberti P, Armenise S, Castaldo V et al. (1997) Freezing gait in Parkinson’s disease. Eur Neurol 38:297–301PubMedGoogle Scholar
  40. 40.
    Matsui H, Udaka F, Miyoshi T et al. (2005) Three-demensional stereotactic surface projection study of freezing of gait and brain perfusion image in Parkinson’s disease. Mov Disord 20:1272–1277PubMedCrossRefGoogle Scholar
  41. 41.
    Muller J, Seppi K, Stefanova N, Poewe W, Litvan I, Wenning GK (2002) Freezing of gait in postmortem-confirmed atypical parkinsonism. Mov Disord 17:1041–1045PubMedCrossRefGoogle Scholar
  42. 42.
    Nagasaki H, Kosaka K, Nakamura R (1981) Disturbance of rhythm formation in patients with hemispheric lesion. Tohoku J Exp Med 135:231–236PubMedCrossRefGoogle Scholar
  43. 43.
    Nakamura R, Nagasaki H, Narabayashi H (1976) Arrhythmokinesia in parkinsonism. In: Birkmayer W, Hornykievicz O (eds) Advances in Parkinsonism. Roche, Basel, pp 258–268Google Scholar
  44. 44.
    Narabayashi H, Kondo T, Hayashi A et al. (1981) L-threo-3,4,dihydroxyphenylserine treatment for akinesia and freezing of parkinsonism Proc Jap Acad 57:351–354Google Scholar
  45. 45.
    Narabayashi H, Kondo T (1987) Results of a double-blind study of L-threo-DOPS in parkinsonism. In: Fahn S, Marsden CD, Gold stein M (eds) Recent developments in Parkinson’s disease. New York. MacMillan, pp 279–291Google Scholar
  46. 46.
    Narabayashi H (1993) Three types of akinesia in the progressive course of Parkinson’s disease. Adv Neurol 60:18–24PubMedGoogle Scholar
  47. 47.
    Nieuwboer A, Feys P, DeWeerdt W, Dom R (1997) Is using a cue to the treatment of freezing in Parkinson’s disease? Physiotherapy Res International 2:125–134CrossRefGoogle Scholar
  48. 48.
    Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fiuws S, Broens-Kaucsik E (2001) Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov disord 16:1066–1075PubMedCrossRefGoogle Scholar
  49. 49.
    Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Janssens L, Stijn V (2004) Electromyographic profiles of gait prior to onset of freezing episodes in patients with Parkinson’s disease. Brain 127:1650–1660PubMedCrossRefGoogle Scholar
  50. 50.
    Ogawa N, Kuroda H, Yamamoto M et al. (1984) Improvement in freezing phenomenon of Parkinson’s disease after DL-threo-3,4-dihydroxyphenylserine Acta Med Okayama 38:301–304PubMedGoogle Scholar
  51. 51.
    Parkinson J (1817) An essay on the shaking palsy. London: Sherwood, Neerby and JonesGoogle Scholar
  52. 52.
    Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2006) Is freezing of gait in Parkinson’s disease related to asymmetric motor functions? Ann Neurol 57:656–663CrossRefGoogle Scholar
  53. 53.
    Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391–398PubMedCrossRefGoogle Scholar
  54. 54.
    Shoulson I, Oakes D, Fahn S et al. (2002) Impact of sustained deprenyl (selegiline) in levodopa-treated Parkinson’s disease: a randomized controlled extension of the deprenyl and tocopherol antioxidative therapy of parkinsonism trial. Ann Neurol 51:604–612PubMedCrossRefGoogle Scholar
  55. 55.
    Stern G, Lander C, Lees A (1980) Akinetic freezing and trick movements in Parkinson’s disease. J Neural Transm 16(Suppl):137–141Google Scholar
  56. 56.
    Stolze H, Klebe S, Poepping M et al. (2001) Effects of bilateral subthalamic nucleus stimulation on parkinsonian gait. Neurology 57:144–146PubMedGoogle Scholar
  57. 57.
    Ueno E, Yanagisawa N, Takami M (1993) Gait disorders in parkinsonism. A study with floor reaction forces and EMG. In: Narabayashi H, Nagatsu T, Yanagisawa N et al. (eds) Parkinson’s disease. From basic research to treatment. New York: Raven Press, pp 414–418Google Scholar
  58. 58.
    Wieler M, Camicioli R, Jones CA, Martin WR (2005) Botulinum toxian injections do not improveve freezing of gait on Parkinson disease. Neurology 65:626–628PubMedCrossRefGoogle Scholar
  59. 59.
    Yanagisawa N, Ueno E, Takami M (1991) Frozen gait of Parkinson’s disease and parkinsonism. A study with floor reaction forces and EMG. In: Shimamura M, Grillner S, Edgerton VR (eds) Neurophysiological basis of human locomotion. Tokyo: Japan Scientific Societies Press, pp 291–304Google Scholar
  60. 60.
    Yokochi F (2006) Effect of deep brain stimulation on FOG. Parkinsonism Rel Disord (in press)Google Scholar
  61. 61.
    Yokoyama T, Sugiyama K, Nishizawa S, Yokota N, Ohta S, Uemura K (1999) Subthalamic nucleus stimulation for gait disturbance in Parkinson’s disease. Neurosurgery 45:41–47PubMedCrossRefGoogle Scholar

Copyright information

© Steinkopff-Verlag 2006

Authors and Affiliations

  1. 1.Department of NeurologyJuntendo University Shizuoka HospitalShizuoka 410-2295Japan

Personalised recommendations