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Journal of NeuroEngineering and Rehabilitation

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Open Access 01-12-2017 | Research

Does Nordic Walking restore the temporal organization of gait variability in Parkinson’s disease?

Authors: Thibault Warlop, Christine Detrembleur, Maïté Buxes Lopez, Gaëtan Stoquart, Thierry Lejeune, Anne Jeanjean

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2017

Abstract

Background

Gait disorders of Parkinson’s disease (PD) are characterized by the breakdown of the temporal organization of stride duration variability that was tightly associated to dynamic instability in PD. Activating the upper body during walking, Nordic Walking (NW) may be used as an external cueing to improve spatiotemporal parameters of gait, such as stride length or gait variability, in PD. The aim of this study was to evaluate the beneficial effects of NW on temporal organization of gait variability and spatiotemporal gait variables in PD.

Methods

Fourteen mild to moderate PD participants and ten age-matched healthy subjects performed 2 × 12 min overground walking sessions (with and without pole in a randomized order) at a comfortable speed. Gait speed, cadence, step length and temporal organization (i.e. long-range autocorrelations; LRA) of stride duration variability were studied on 512 consecutive gait cycles using a unidimensional accelerometer placed on the malleola of the most affected side in PD patients and of the dominant side in healthy controls. The presence of LRA was determined using the Rescaled Range Analysis (Hurst exponent) and the Power Spectral Density (α exponent). To assess NW and disease influences on gait, paired t-tests, Z-score and a two-way (pathological condition x walking condition) ANOVA repeated measure were used.

Results

Leading to significant improvement of LRA, NW enhances step length and reduces gait cadence without any change in gait speed in PD. Interestingly, LRA and step length collected from the NW session are similar to that of the healthy population.

Conclusion

This cross-sectional controlled study demonstrates that NW may constitute a powerful way to struggle against the randomness of PD gait and the typical gait hypokinesia. Involving a voluntary intersegmental coordination, such improvement could also be due to the upper body rhythmic movements acting as rhythmical external cue to bypass their defective basal ganglia circuitries.

Ethics committee’s reference number

B403201318916

Trial registration

NCT02419768

Morris ME, Iansek R, Matyas TA, Summers JJ. Ability to modulate walking cadence remains intact in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1968;1994:1532–4.

Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson’s disease Normalization strategies and underlying mechanisms. Brain. 1996;119:551–68.CrossRefPubMed

Van Wegen E, De Goede C, Lim I, Rietberg M, Nieuwboer A, Willems A. The effect of rhythmic somatosensory cueing on gait in patients with Parkinson’s disease. J Neurol Sci. 2006;248:210–4. doi:10.1016/j.jns.2006.05.034.CrossRefPubMed

Snijders AH, Delval A, Weerdesteyn V, Duysens J, Overeem S, Bloem BR. Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience. 2011;182:217–24. doi:10.1016/j.neuroscience.2011.02.061.CrossRefPubMed

Hausdorff JM. Gait dynamics, fractals and falls : Finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci. 2007;26:555–89. doi:10.1016/j.humov.2007.05.003.CrossRefPubMedPubMedCentral

Warlop T, Detrembleur C, Bollens B, Stoquart G, Crevecoeur F, Jeanjean A, Lejeune T. Temporal organization of stride duration variability as an index of gait instability in Parkinson’s disease. J Rehabil Med. 2016;48:865–71. doi:10.2340/16501977-2158.CrossRefPubMed

Peng CK, Havlin S, Stanley HE, Goldberger AL. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos. 1995;5(1):82–7.CrossRefPubMed

Stergiou N, Decker LM. Human Movement Science Human movement variability, nonlinear dynamics, and pathology: Is there a connection? Hum Mov Sci. 2011;30(5):869–88. doi:10.1016/j.humov.2011.06.002.CrossRefPubMedPubMedCentral

Diniz A, Wijnants ML, Torre K, Barreiros J, Crato N, Bosman A, Hasselman, Cox R, Van Orden G, Delignières D. Contemporary theories of 1/f noise in motor control. Hum Mov Sci. 2011;30(5):889–905. doi:10.1016/j.humov.2010.07.006.CrossRefPubMed

10.

Cugusi L, Solla P, Serpe R, Carzedda T, Piras L, Oggianu M, Gabba S, Di Blasio A, Bergamin M, Cannas A, Marrosu F, Mercuro G. Effects of a Nordic Walking program on motor and non-motor symptoms, functional performance and body composition in patients with Parkinson’s disease. NeuroRehabilitation. 2015;37(2):245–54. doi:10.3233/NRE-151257.CrossRefPubMed

11.

Reuter I, Mehnert S, Leone P, Kaps M, Oechsner M, Engelhardt M. Effects of a flexibility and relaxation programme, walking, and nordic walking on Parkinson’s disease. J Aging Res. 2011;2011:232473. doi:10.4061/2011/232473.CrossRefPubMedPubMedCentral

12.

Van Eijkeren FJM, Reijmers RSJ, Kleinveld MJ, Minten A, Pieter J, Bloem BR. Nordic walking improves mobility in Parkinson’s Disease. Mov Disord. 2008;23(15):2239–43. doi:10.1002/mds.22293.CrossRefPubMed

13.

Baatile J, Langbein WE, Weaver F, Maloney C, Jost MB. Effect of exercise on perceived quality of life of individuals with Parkinson’s disease. J Rehabil Res Dev. 2000;37(5):529–34.PubMed

14.

Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease : a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992;55(3):181–4.CrossRefPubMedPubMedCentral

15.

Crevecoeur F, Bollens B, Detrembleur C, Lejeune TM. Towards a “gold-standard” approach to address the presence of long-range auto-correlation in physiological time series. J Neurosci Methods. 2010;192(1):163–72. doi:10.1016/j.jneumeth.2010.07.017.CrossRefPubMed

16.

Zijlstra W, Hof AL. Assessment of spatio-temporal gait parameters from trunk accelerations during human walking. Gait Posture. 2003;18:1–10.CrossRefPubMed

17.

Terrier P, Dériaz O. Kinematic variability, fractal dynamics and local dynamic stability of treadmill walking. J Neuroeng Rehabil. 2011;8(1):12. doi:10.1186/1743-0003-8-12.CrossRefPubMedPubMedCentral

18.

Fortune E, Morrow MMB, Kaufman KR. Assessment of gait kinetics using Tri-Axial accelerometers. J Appl Biomech. 2014;30(5):668–74. doi:10.1123/jab.2014-0037.Assessment.CrossRefPubMedPubMedCentral

19.

Fortune E, Lugade V, Morrow M, Kaufman K. Validity of using Tri-Axial accelerometers to measure human movement – Part II: step counts at a wide range of gait velocities. Med Eng Phys. 2014;36(6):659–69. doi:10.1016/j.medengphy.2014.02.006.Validity.CrossRefPubMedPubMedCentral

20.

Sinclair J, Hobbs SJ, Protheroe L, Edmundson CJ. Determination of gait events using an externally mounted shank accelerometer. J Appl Biomech. 2013;29:118–22.CrossRefPubMed

21.

Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM. Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J Neurol Sci. 2003;212(1-2):47–53. doi:10.1016/S0022-510X(03)00104-7.CrossRefPubMed

22.

Lord S, Baker K, Nieuwboer A, Burn D, Rochester L. Gait variability in Parkinson’ s disease : an indicator of non-dopaminergic contributors to gait dysfunction ? J Neurol. 2011:566-572. doi:10.1007/s00415-010-5789-8.

23.

Bollens B, Crevecoeur F, Detrembleur C, Guillery E, Lejeune T. Effects of age and walking speed on long-range autocorrelations and fluctuation magnitude of stride duration. Neuroscience. 2012;210:234–42. doi:10.1016/j.neuroscience.2012.02.039.CrossRefPubMed

24.

Moon Y, Sung J, An R, Hernandez M, Sosnoff J. Gait variability in people with neurological disorders: a systematic review and meta-analysis. Hum Mov Sci. 2016;47:197–208.CrossRefPubMed

25.

Ayoubi F, Launay CP, Kabeshova A, Fantino B, Annweiler C, Beauchet O. The influence of fear of falling on gait variability: results from a large elderly population-based cross-sectional study. J Neuroeng Rehabil. 2014;11(1):128. doi:10.1186/1743-0003-11-128.CrossRefPubMedPubMedCentral

26.

Winter DA. The Biomechanics and Motor Control of Human Gait: Normal, Elderly and Pathological. Waterloo: University of Waterloo Press; 1991.

27.

Andriacchi T, Ogle J, Galante J. Walking Speed as a basis for normal and abnormal gait measurements. J Biomechanics. 1977;10:261–8. doi:10.1016/0021-9290(77)90049-5.CrossRef

28.

Baker K, Rochester L, Nieuwboer A. The immediate effect of attentional, auditory, and a combined cue strategy on gait during single and dual tasks in Parkinson’s Disease. Arch Phys Med Rehabil. 2007;88:1593–600. doi:10.1016/j.apmr.2007.07.026.CrossRefPubMed

29.

Lindholm B, Hagell P, Hansson O, Nilsson MH. Prediction of falls and/or near falls in people with mild Parkinson’s Disease. PLoS One. 2015;10(1):1–11. doi:10.1371/journal.pone.0117018.CrossRef

30.

Combs SA, Diehl MD, Filip J, Long E. Short-distance walking speed tests in people with Parkinson disease: Reliability, responsiveness, and validity. Gait Posture. 2014;39(2):784–8. doi:10.1016/j.gaitpost.2013.10.019.CrossRefPubMed

31.

Hove MJ, Suzuki K, Uchitomi H, Orimo S, Miyake Y. Interactive Rhythmic Auditory Stimulation Reinstates Natural 1/f Timing in Gait of Parkinson’s Patients. 2012;7(3):1-8. doi:10.1371/journal.pone.0032600.

32.

Delignières D, Torre K. Fractal dynamics of human gait: a reassessment of the 1996 data of Hausdorff et al. J Appl Physiol. 2009;106:1272–9. doi:10.1152/japplphysiol.90757.2008.CrossRefPubMed

33.

Hausdorff JM, Mitchell S, Firtion E, et al. Altered fractal dynamics of gait : reduced stride-interval correlations with aging and Huntington’s disease. J Appl Physiol. 1997;82(1):262–9.PubMed

34.

Bollens B, Crevecoeur FF, Detrembleur C, Warlop T, Lejeune TM. Variability of human gait: effect of backward walking and dual-tasking on the presence of long-range autocorrelations. Ann Biomed Eng. 2014;42(4):742–50. doi:10.1007/s10439-013-0961-9.CrossRefPubMed

35.

Lohnes CA, Earhart GM. Gait & Posture The impact of attentional, auditory, and combined cues on walking during single and cognitive dual tasks in Parkinson disease. Gait Posture. 2011;33(3):478–83. doi:10.1016/j.gaitpost.2010.12.029.CrossRefPubMed

36.

Wu T, Hallett M, Chan P. Motor automaticity in Parkinson’s disease. Neurobiol Dis. 2015;82:226–34. doi:10.1016/j.nbd.2015.06.014.CrossRefPubMed

37.

Nourrit-Lucas D, Tossa A, Zélic G, Delignières D. Learning, Motor Skill, and Long-range correlations. J Motor Behav. 2015:37-41. doi:10.1080/00222895.2014.967655.

38.

Meyns P, Bruijn SM, Duysens J. The how and why of arm swing during human walking. Gait Posture. 2013;38(4):555–62. doi:10.1016/j.gaitpost.2013.02.006.CrossRefPubMed

39.

Punt M, Bruijn SM, Wittink H, van Dieën JH. Effect of arm swing strategy on local dynamic stability of human gait. Gait Posture. 2015;41(2):504–9. doi:10.1016/j.gaitpost.2014.12.002.CrossRefPubMed

40.

Paul SS, Thackeray A, Duncan RP, Cavanaugh JT, Ellis TD, Earhart GM, Ford MP, Foreman KB, Dibble LE. Two-year trajectory of fall risk in people with Parkinson’s disease: a latent class analysis. Arch Phys Med Rehabil. 2016;97(3):372–9. doi:10.1016/j.apmr.2015.10.105.CrossRefPubMed

41.

Dietz V. Quadrupedal coordination of bipedal gait : implications for movement disorders. J Neurol. 2011;258:1406–12. doi:10.1007/s00415-011-6063-4.CrossRefPubMed

42.

Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci. 2001;14:1906–14.CrossRefPubMed

43.

Dietz V. Spinal cord pattern generators for locomotion. Clin Neurophysiol. 2003;114:1379–89. doi:10.1016/S1388-2457(03)00120-2.CrossRefPubMed

44.

Zehr EP, Duysens J. Regulation of arm and leg movement during human locomotion. Neuroscientist. 2004;10(4):347–61. doi:10.1177/1073858404264680.CrossRefPubMed

45.

Zehr EP, Carroll TJ, Chua R, et al. Possible contributions of CPG activity to the control of rhythmic human arm movement. Can J Physiol Pharmacol. 2004;82:556–68. doi:10.1139/y04-056.CrossRefPubMed

46.

Haridas C, Zehr EP, Zehr EP. Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol. 2003;90:2850–61.CrossRefPubMed

47.

Lim I, van Wegen E, de Goede C, et al. Effects of external rhythmical cueing on gait in patients with Parkinson’s disease: a systematic review. Clin Rehabil. 2005;19(7):695–713.CrossRefPubMed

48.

Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME. Cueing and gait improvement among people with Parkinson’s Disease: a meta-analysis. Arch Phys Med Rehabil. 2013;94(3):562–70. doi:10.1016/j.apmr.2012.10.026.CrossRefPubMed

49.

Pellegrini B, Peyré-tartaruga LA, Zoppirolli C, Bortolan L, Savoldelli A, Minetti AE, Schena F. Gait & Posture Mechanical energy patterns in nordic walking : comparisons with conventional walking. Gait Posture. 2017;51:234–8. doi:10.1016/j.gaitpost.2016.10.010.CrossRefPubMed

50.

Thorwesten L, Overhaus N, Völker K. Ground reaction forces in nordic walking and walking. XXIV ISBS Symposium, 2006. https://ojs.ub.uni-konstanz.de/cpa/article/view/289/246https://ojs.ub.uni-konstanz.de/cpa/article/view/289/246

51.

Stief F, Kleindienst FI, Wiemeyer J, Wedel F, Campe S, Krabbe B. Inverse dynamic analysis of the lower extremities during nordic walking, walking, and running. J Appl Biomech. 2008;24:351–9.CrossRefPubMed

52.

Boonsinsukh R, Saengsirisuwan V, Carlson-kuhta P, Horak FB. A cane improves postural recovery from an unpracticed slip during walking in people with Parkinson Disease. Phys Ther. 2012;92:1117–29.CrossRefPubMedPubMedCentral

53.

Kegelmeyer DA, Parthasarathy S, Kostyk SK, White SE, Kloos AD. Assistive devices alter gait patterns in Parkinson disease : Advantages of the four-wheeled walker. Gait Posture. 2013;38(1):20–4. doi:10.1016/j.gaitpost.2012.10.027.CrossRefPubMed

54.

Bryant MS, Pourmoghaddam A, Thrasher MSA. Gait changes with walking devices in persons with Parkinson's disease. Disabil Rehabil Assist Technol. 2012;7(2):149–52. doi:10.3109/17483107.2011.602461.CrossRefPubMed

55.

Herfurth M, Godau J, Kattner B, Rombach S, Grau S, Maetzler W, Berg D. Parkinsonism and Related Disorders Gait velocity and step length at baseline predict outcome of Nordic walking training in patients with Parkinson’s disease. Park Relat Disord. 2015;21(4):413–6. doi:10.1016/j.parkreldis.2015.01.016.CrossRef

56.

Winogrodzka A, Wagenaar RC, Booij J, Wolters EC. Rigidity and Bradykinesia Reduce Interlimb Coordination in Parkinsonian Gait. Arch Phys Med Rehabil. 2005;86:183–9. doi:10.1016/j.apmr.2004.09.010.CrossRefPubMed

57.

Peterson D, Smulders K. Cues and Attention in Parkinsonian Gait : Potential Mechanisms and Future Directions. Front Neurol. 2015;6:1–5. doi:10.3389/fneur.2015.00255.CrossRef

58.

Menz HB, Lord SR, Fitzpatrick RC. Acceleration patterns of the head and pelvis when walking on level and irregular surfaces. Gait Posture. 2003;18:35–46.CrossRefPubMed

59.

Hamacher D, Hamacher D, Herold F, Schega L. Effect of dual tasks on gait variability in walking to auditory cues in older and young individuals. Exp Brain Res. 2016;234(12):3555–63. doi:10.1007/s00221-016-4754-x.CrossRefPubMed

60.

Terrier P. Fractal fluctuations in human walking : comparison between auditory and visually guided stepping. Ann Biomed Eng. 2016;44(9):2785–93. doi:10.1007/s10439-016-1573-y.CrossRefPubMed

61.

Moraiti CO, Stergiou N, Vasiliadis HS, Motsis E, Georgoulis A. Gait & Posture Anterior cruciate ligament reconstruction results in alterations in gait variability. Gait Posture. 2010;32(2):169–75. doi:10.1016/j.gaitpost.2010.04.008.CrossRefPubMed

Title: Does Nordic Walking restore the temporal organization of gait variability in Parkinson’s disease?
Authors: Thibault Warlop
Christine Detrembleur
Maïté Buxes Lopez
Gaëtan Stoquart
Thierry Lejeune
Anne Jeanjean
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Journal of NeuroEngineering and Rehabilitation / Issue 1/2017
Electronic ISSN: 1743-0003
DOI: https://doi.org/10.1186/s12984-017-0226-1

At a glance: The STEP trials

Springer Medicine

Does Nordic Walking restore the temporal organization of gait variability in Parkinson’s disease?

Abstract

Background

Methods

Results

Conclusion

Ethics committee’s reference number

Trial registration

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Ethics committee’s reference number

Trial registration

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