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Published in: Journal of Neurology 2/2019

Open Access 01-02-2019 | Original Communication

Gait festination in parkinsonism: introduction of two phenotypes

Authors: Jorik Nonnekes, Nir Giladi, Anasuya Guha, Urban M. Fietzek, Bastiaan R. Bloem, Evžen Růžička

Published in: Journal of Neurology | Issue 2/2019

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Abstract

Gait festination is one of the most characteristic gait disturbances in patients with Parkinson’s disease or atypical parkinsonism. Although festination is common and disabling, it has received little attention in the literature, and different definitions exist. Here, we argue that there are actually two phenotypes of festination. The first phenotype entails a primary locomotion disturbance, due to the so-called sequence effect: a progressive shortening of step length, accompanied by a compensatory increase in cadence. This phenotype strongly relates to freezing of gait with alternating trembling of the leg. The second phenotype results from a postural control problem (forward leaning of the trunk) combined with a balance control deficit (inappropriately small balance-correcting steps). In this viewpoint, we elaborate on the possible pathophysiological substrate of these two phenotypes of festination and discuss their management in daily clinical practice.
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Literature
1.
go back to reference Akiyama H, Nukui S, Akamatu M, Hasegawa Y, Nishikido O, Inoue S (2017) Effectiveness of spinal cord stimulation for painful camptocormia with Pisa syndrome in Parkinson’s disease: a case report. BMC Neurol 17:148CrossRefPubMedPubMedCentral Akiyama H, Nukui S, Akamatu M, Hasegawa Y, Nishikido O, Inoue S (2017) Effectiveness of spinal cord stimulation for painful camptocormia with Pisa syndrome in Parkinson’s disease: a case report. BMC Neurol 17:148CrossRefPubMedPubMedCentral
2.
go back to reference Barthel C, Nonnekes J, van Helvert M, Haan R, Janssen A, Delval A, Weerdesteyn V, Debu B, van Wezel R, Bloem BR, Ferraye MU (2018) The laser shoes: a new ambulatory device to alleviate freezing of gait in Parkinson disease. Neurology 90:e164–e171CrossRefPubMed Barthel C, Nonnekes J, van Helvert M, Haan R, Janssen A, Delval A, Weerdesteyn V, Debu B, van Wezel R, Bloem BR, Ferraye MU (2018) The laser shoes: a new ambulatory device to alleviate freezing of gait in Parkinson disease. Neurology 90:e164–e171CrossRefPubMed
3.
go back to reference Benninger F, Khlebtovsky A, Roditi Y, Keret O, Steiner I, Melamed E, Djaldetti R (2015) Beneficial effect of levodopa therapy on stooped posture in Parkinson’s disease. Gait Posture 42:263–268CrossRefPubMed Benninger F, Khlebtovsky A, Roditi Y, Keret O, Steiner I, Melamed E, Djaldetti R (2015) Beneficial effect of levodopa therapy on stooped posture in Parkinson’s disease. Gait Posture 42:263–268CrossRefPubMed
4.
go back to reference Berardelli A, Rothwell JC, Thompson PD, Hallet M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146CrossRefPubMed Berardelli A, Rothwell JC, Thompson PD, Hallet M (2001) Pathophysiology of bradykinesia in Parkinson’s disease. Brain 124:2131–2146CrossRefPubMed
5.
go back to reference Bloem BR, Beckley DJ, van Dijk JG, Zwinderman AH, Remler MP, Roos RA (1996) Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov Disord 11:509–521CrossRefPubMed Bloem BR, Beckley DJ, van Dijk JG, Zwinderman AH, Remler MP, Roos RA (1996) Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov Disord 11:509–521CrossRefPubMed
6.
go back to reference Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci 6:755–765CrossRefPubMed Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci 6:755–765CrossRefPubMed
7.
go back to reference Capecci M, Serpicelli C, Fiorentini L, Censi G, Ferretti M, Orni C, Renzi R, Provinciali L, Ceravolo MG (2014) Postural rehabilitation and kinesio taping for axial postural disorders in Parkinson’s disease. Arch Phys Med Rehabil 95:1067–1075CrossRefPubMed Capecci M, Serpicelli C, Fiorentini L, Censi G, Ferretti M, Orni C, Renzi R, Provinciali L, Ceravolo MG (2014) Postural rehabilitation and kinesio taping for axial postural disorders in Parkinson’s disease. Arch Phys Med Rehabil 95:1067–1075CrossRefPubMed
8.
go back to reference Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR (2004) Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:1245–1254CrossRefPubMedPubMedCentral Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR (2004) Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:1245–1254CrossRefPubMedPubMedCentral
9.
go back to reference Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed
10.
go back to reference de Kam D, Nonnekes J, Oude Nijhuis LB, Geurts AC, Bloem BR, Weerdesteyn V (2014) Dopaminergic medication does not improve stepping responses following backward and forward balance perturbations in patients with Parkinson’s disease. J Neurol 261:2330–2337CrossRef de Kam D, Nonnekes J, Oude Nijhuis LB, Geurts AC, Bloem BR, Weerdesteyn V (2014) Dopaminergic medication does not improve stepping responses following backward and forward balance perturbations in patients with Parkinson’s disease. J Neurol 261:2330–2337CrossRef
11.
go back to reference Delval A, Rambour M, Tard C, Dujardin K, Devos D, Bleuse S, Defebvre L, Moreau C (2016) Freezing/festination during motor tasks in early-stage Parkinson’s disease: a prospective study. Mov Disord 31:1837–1845CrossRefPubMed Delval A, Rambour M, Tard C, Dujardin K, Devos D, Bleuse S, Defebvre L, Moreau C (2016) Freezing/festination during motor tasks in early-stage Parkinson’s disease: a prospective study. Mov Disord 31:1837–1845CrossRefPubMed
12.
go back to reference Djaldetti R, Mosberg-Galili R, Sroka H, Merims D, Melamed E (1999) Camptocormia (bent spine) in patients with Parkinson’s disease—characterization and possible pathogenesis of an unusual phenomenon. Mov Disord 14:443–447CrossRefPubMed Djaldetti R, Mosberg-Galili R, Sroka H, Merims D, Melamed E (1999) Camptocormia (bent spine) in patients with Parkinson’s disease—characterization and possible pathogenesis of an unusual phenomenon. Mov Disord 14:443–447CrossRefPubMed
13.
go back to reference Doherty KM, van de Warrenburg BP, Peralta MC, Silveira-Moriyama L, Azulay JP, Gershanik OS, Bloem BR (2011) Postural deformities in Parkinson’s disease. Lancet Neurol 10:538–549CrossRefPubMed Doherty KM, van de Warrenburg BP, Peralta MC, Silveira-Moriyama L, Azulay JP, Gershanik OS, Bloem BR (2011) Postural deformities in Parkinson’s disease. Lancet Neurol 10:538–549CrossRefPubMed
14.
go back to reference Fasano A, Aquino CC, Krauss JK, Honey CR, Bloem BR (2015) Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol 11:98–110CrossRefPubMed Fasano A, Aquino CC, Krauss JK, Honey CR, Bloem BR (2015) Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol 11:98–110CrossRefPubMed
15.
go back to reference Fasano A, Geroin C, Berardelli A, Bloem BR, Espay AJ, Hallett M, Lang AE, Tinazzi M (2018) Diagnostic criteria for camptocormia in Parkinson’s disease: a consensus-based proposal. Parkinsonism Relat Disord 53:53–57CrossRefPubMed Fasano A, Geroin C, Berardelli A, Bloem BR, Espay AJ, Hallett M, Lang AE, Tinazzi M (2018) Diagnostic criteria for camptocormia in Parkinson’s disease: a consensus-based proposal. Parkinsonism Relat Disord 53:53–57CrossRefPubMed
16.
17.
go back to reference Fietzek UM, Schroeteler FE, Ziegler K, Zwosta J, Ceballos-Baumann AO (2014) Randomized cross-over trial to investigate the efficacy of a 2-week physiotherapy programme with repetitive exercises of cueing to reduce the severity of freezing of gait in patients with Parkinson’s disease. Clin Rehabil 28:902–911CrossRefPubMed Fietzek UM, Schroeteler FE, Ziegler K, Zwosta J, Ceballos-Baumann AO (2014) Randomized cross-over trial to investigate the efficacy of a 2-week physiotherapy programme with repetitive exercises of cueing to reduce the severity of freezing of gait in patients with Parkinson’s disease. Clin Rehabil 28:902–911CrossRefPubMed
18.
go back to reference Freeman JS, Cody FWJ, Schady W (1993) The influence of external timing cues upon the rhythm of voluntary movements in Parkinsons-disease. J Neurol Neurosur Ps 56:1078–1084CrossRef Freeman JS, Cody FWJ, Schady W (1993) The influence of external timing cues upon the rhythm of voluntary movements in Parkinsons-disease. J Neurol Neurosur Ps 56:1078–1084CrossRef
19.
go back to reference Giladi N, Shabtai H, Rozenberg E, Shabtai E (2001) Gait festination in Parkinson’s disease. Parkinsonism Relat Disord 7:135–138CrossRefPubMed Giladi N, Shabtai H, Rozenberg E, Shabtai E (2001) Gait festination in Parkinson’s disease. Parkinsonism Relat Disord 7:135–138CrossRefPubMed
20.
go back to reference Iansek R, Huxham F, McGinley J (2006) The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Mov Disord 21:1419–1424CrossRefPubMed Iansek R, Huxham F, McGinley J (2006) The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Mov Disord 21:1419–1424CrossRefPubMed
21.
go back to reference Jacobs JV, Horak FB (2006) Abnormal proprioceptive-motor integration contributes to hypometric postural responses of subjects with Parkinson’s disease. Neuroscience 141:999–1009CrossRefPubMed Jacobs JV, Horak FB (2006) Abnormal proprioceptive-motor integration contributes to hypometric postural responses of subjects with Parkinson’s disease. Neuroscience 141:999–1009CrossRefPubMed
22.
go back to reference Janssen AM, Munneke MAM, Nonnekes J, van der Kraan T, Nieuwboer A, Toni I, Snijders AH, Bloem BR, Stegeman DF (2017) Cerebellar theta burst stimulation does not improve freezing of gait in patients with Parkinson’s disease. J Neurol 264:963–972CrossRefPubMedPubMedCentral Janssen AM, Munneke MAM, Nonnekes J, van der Kraan T, Nieuwboer A, Toni I, Snijders AH, Bloem BR, Stegeman DF (2017) Cerebellar theta burst stimulation does not improve freezing of gait in patients with Parkinson’s disease. J Neurol 264:963–972CrossRefPubMedPubMedCentral
23.
go back to reference Janssen S, Bolte B, Nonnekes J, Bittner M, Bloem BR, Heida T, Zhao Y, van Wezel RJA (2017) Usability of three-dimensional augmented visual cues delivered by smart glasses on (freezing of) gait in Parkinson’s disease. Front Neurol 8:279CrossRefPubMedPubMedCentral Janssen S, Bolte B, Nonnekes J, Bittner M, Bloem BR, Heida T, Zhao Y, van Wezel RJA (2017) Usability of three-dimensional augmented visual cues delivered by smart glasses on (freezing of) gait in Parkinson’s disease. Front Neurol 8:279CrossRefPubMedPubMedCentral
24.
go back to reference Konczak J, Ackermann H, Hertrich I, Spieker S, Dichgans J (1997) Control of repetitive lip and finger movements in Parkinson’s disease: influence of external timing signals and simultaneous execution on motor performance. Mov Disord 12:665–676CrossRefPubMed Konczak J, Ackermann H, Hertrich I, Spieker S, Dichgans J (1997) Control of repetitive lip and finger movements in Parkinson’s disease: influence of external timing signals and simultaneous execution on motor performance. Mov Disord 12:665–676CrossRefPubMed
25.
go back to reference Logigian E, Hefter H, Reiners K, Freund HJ (1991) Does tremor pace repetitive voluntary motor behavior in Parkinsons-disease. Ann Neurol 30:172–179CrossRefPubMed Logigian E, Hefter H, Reiners K, Freund HJ (1991) Does tremor pace repetitive voluntary motor behavior in Parkinsons-disease. Ann Neurol 30:172–179CrossRefPubMed
26.
go back to reference Morris ME, Lansek R, Galna B (2008) Gait festination and freezing in Parkinson’s disease: Pathogenesis and rehabilitation. Mov Disord 23:S451–S460CrossRefPubMed Morris ME, Lansek R, Galna B (2008) Gait festination and freezing in Parkinson’s disease: Pathogenesis and rehabilitation. Mov Disord 23:S451–S460CrossRefPubMed
27.
go back to reference Nonnekes J, de Kam D, Geurts AC, Weerdesteyn V, Bloem BR (2013) Unraveling the mechanisms underlying postural instability in Parkinson’s disease using dynamic posturography. Expert Rev Neurother 13:1303–1308CrossRefPubMed Nonnekes J, de Kam D, Geurts AC, Weerdesteyn V, Bloem BR (2013) Unraveling the mechanisms underlying postural instability in Parkinson’s disease using dynamic posturography. Expert Rev Neurother 13:1303–1308CrossRefPubMed
28.
go back to reference Nonnekes J, Goselink R, Weerdesteyn V, Bloem BR (2015) The retropulsion test: a good evaluation of postural instability in Parkinson’s disease? J Parkinson’s Dis 5:43–47 Nonnekes J, Goselink R, Weerdesteyn V, Bloem BR (2015) The retropulsion test: a good evaluation of postural instability in Parkinson’s disease? J Parkinson’s Dis 5:43–47
29.
go back to reference Nonnekes J, Goselink RJM, Ruzicka E, Fasano A, Nutt JG, Bloem BR (2018) Neurological disorders of gait, balance and posture: a sign-based approach. Nat Rev Neurol 14:183–189CrossRefPubMed Nonnekes J, Goselink RJM, Ruzicka E, Fasano A, Nutt JG, Bloem BR (2018) Neurological disorders of gait, balance and posture: a sign-based approach. Nat Rev Neurol 14:183–189CrossRefPubMed
30.
go back to reference Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR (2015) Freezing of gait: a practical approach to management. Lancet Neurol 14:768–778CrossRefPubMed Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR (2015) Freezing of gait: a practical approach to management. Lancet Neurol 14:768–778CrossRefPubMed
31.
go back to reference Nonnekes J, Timmer MH, de Vries NM, Rascol O, Helmich RC, Bloem BR (2016) Unmasking levodopa resistance in Parkinson’s disease. Mov Disord 31:1602–1609CrossRefPubMed Nonnekes J, Timmer MH, de Vries NM, Rascol O, Helmich RC, Bloem BR (2016) Unmasking levodopa resistance in Parkinson’s disease. Mov Disord 31:1602–1609CrossRefPubMed
32.
go back to reference 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 10:734–744CrossRef 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 10:734–744CrossRef
33.
go back to reference Parkinson J (2002) An essay on the shaking palsy (reprinted). J Neuropsych Clin Neurosurg 14:223–236CrossRef Parkinson J (2002) An essay on the shaking palsy (reprinted). J Neuropsych Clin Neurosurg 14:223–236CrossRef
34.
go back to reference Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME (2013) Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil 94:562–570CrossRefPubMed Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME (2013) Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil 94:562–570CrossRefPubMed
35.
go back to reference von Coelln R, Raible A, Gasser T, Asmus F (2008) Ultrasound-guided injection of the iliopsoas muscle with botulinum toxin in camptocormia. Mov Disord 23:889–892CrossRef von Coelln R, Raible A, Gasser T, Asmus F (2008) Ultrasound-guided injection of the iliopsoas muscle with botulinum toxin in camptocormia. Mov Disord 23:889–892CrossRef
36.
go back to reference Young WR, Rodger MWM, Craig CM (2014) Auditory observation of stepping actions can cue both spatial and temporal components of gait in Parkinson’s disease patients. Neuropsychologia 57:140–153CrossRefPubMed Young WR, Rodger MWM, Craig CM (2014) Auditory observation of stepping actions can cue both spatial and temporal components of gait in Parkinson’s disease patients. Neuropsychologia 57:140–153CrossRefPubMed
Metadata
Title
Gait festination in parkinsonism: introduction of two phenotypes
Authors
Jorik Nonnekes
Nir Giladi
Anasuya Guha
Urban M. Fietzek
Bastiaan R. Bloem
Evžen Růžička
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 2/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-9146-7

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