Skip to main content
Log in

The spectrum of preclinical gait disorders in early Parkinson’s disease: subclinical gait abnormalities and compensatory mechanisms revealed with dual tasking

  • Neurology and Preclinical Neurological Studies - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

Patients with early Parkinson’s disease (PD) may not complain of gait difficulties but subtle gait abnormalities may be revealed as part of a “preclinical gait syndrome” when they are challenged by dual tasks. 21 early PD patients (n = 21, mean age 63.5 years, H&Y 1.62, disease duration <5 years, mean UPDRS-III 7.7) who did not have gait complaints were as compared to age- and gender-matched healthy controls (n = 21). Memory function was not different between the two groups. Under normal walking conditions, there were no significant differences in gait parameters between the patients and the control group. In both groups, normalized gait velocity decreased in response to dual tasking in a parallel fashion (p < 0.001). Similarly, gait variability increased in both groups with dual tasking although not statistically significant. In PD patients, the performance of an additional task resulted in an increased number of cadences (p = 0.04), a reduction in swing time (p = 0.02) and cycle time (p = 0.04) compared with the control group but there was no significant reduction in normalized velocity. Stride width also increased in the PD patients. The addition of a cognitive task may affect certain aspects of gait and is able to elicit subclinical deficits in early PD patients. In an attempt to maintain velocity, early PD patients develop compensatory mechanisms by increasing cadence and decreasing swing time and cycle time. Increased step width helps support balance, and prevents going beyond the base-of-support which may predispose to unsteadiness and falls. We propose that these findings occur as part of a spectrum of a “preclinical gait syndrome” and longitudinal studies are needed to assess the predictive values of these early markers of gait deficits.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baltadjieva R, Giladi N, Gruendlinger L, Peretz C, Hausdorff JM (2006) Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson’s disease. Eur J Neurosci 24(6):1815–1820

    Article  PubMed  Google Scholar 

  • Bhidayasiri R, Truong DD (2012) Therapeutic strategies for nonmotor symptoms in early Parkinson’s disease: the case for a higher priority and stronger evidence. Parkinsonism Relat Disord 18(Suppl 1):S110–S113

    Article  PubMed  Google Scholar 

  • Bloem BR, Grimbergen YA, van Dijk JG, Munneke M (2006) The “posture second” strategy: a review of wrong priorities in Parkinson’s disease. J Neurol Sci 248(1–2):196–204

    Article  PubMed  Google Scholar 

  • Carpinella I, Crenna P, Calabrese E, Rabuffetti M, Mazzoleni P, Nemni R et al (2007) Locomotor function in the early stage of Parkinson’s disease. IEEE Trans Neural Syst Rehabil Eng 15(4):543–551

    Article  PubMed  Google Scholar 

  • Chastan N, Debono B, Maltete D, Weber J (2008) Discordance between measured postural instability and absence of clinical symptoms in Parkinson’s disease patients in the early stages of the disease. Mov Disord 23(3):366–372

    Article  PubMed  Google Scholar 

  • 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(Pt 8):2151–2160

    Article  PubMed  Google Scholar 

  • Donner A, Eliasziw M (1987) Sample size requirements for reliability studies. Stat Med 6(4):441–448

    Article  PubMed  CAS  Google Scholar 

  • Evans JR, Mason SL, Williams-Gray CH, Foltynie T, Brayne C, Robbins TW et al (2011) The natural history of treated Parkinson’s disease in an incident, community based cohort. J Neurol Neurosurg Psychiatry 82(10):1112–1118

    Article  PubMed  Google Scholar 

  • Fearnley JM, Lees AJ (1991) Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114(Pt 5):2283–2301

    Article  PubMed  Google Scholar 

  • Ferrarin M, Carpinella I, Rabuffetti M, Calabrese E, Mazzoleni P, Nemni R (2006) Locomotor disorders in patients at early stages of Parkinson’s disease: a quantitative analysis. Conf Proc IEEE Eng Med Biol Soc 1:1224–1227

    PubMed  CAS  Google Scholar 

  • Fioretti S, Guidi M, Ladislao L, Ghetti G (2004) Analysis and reliability of posturographic parameters in Parkinson patients at an early stage. Conf Proc IEEE Eng Med Biol Soc 1:651–654

    PubMed  CAS  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    Article  PubMed  CAS  Google Scholar 

  • Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger L, Hausdorff JM (2005) Effect of gait speed on gait rhythmicity in Parkinson’s disease: variability of stride time and swing time respond differently. J Neuroeng Rehabil 2:23

    Article  PubMed  Google Scholar 

  • Ganguli M, Ratcliff G, Huff FJ, Belle S, Kancel MJ, Fischer L et al (1990) Serial sevens versus world backwards: a comparison of the two measures of attention from the MMSE. J Geriatr Psychiatry Neurol 3(4):203–207

    Article  PubMed  CAS  Google Scholar 

  • Geurts AC, Boonstra TA, Voermans NC, Diender MG, Weerdesteyn V, Bloem BR (2011) Assessment of postural asymmetry in mild to moderate Parkinson’s disease. Gait Posture 33(1):143–145

    Article  PubMed  CAS  Google Scholar 

  • Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51(6):745–752

    Article  PubMed  CAS  Google Scholar 

  • Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676

    Article  PubMed  CAS  Google Scholar 

  • Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C et al (2004) Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19(9):1020–1028

    Article  PubMed  Google Scholar 

  • Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J Neuroeng Rehabil 2:19

    Article  PubMed  Google Scholar 

  • Hausdorff JM (2007) Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci 26(4):555–589

    Article  PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17(5):427–442

    Article  PubMed  CAS  Google Scholar 

  • Karzmark P (2000) Validity of the serial seven procedure. Int J Geriatr Psychiatry 15(8):677–679

    Article  PubMed  CAS  Google Scholar 

  • Kressig RW, Beauchet O (2006) Guidelines for clinical applications of spatio-temporal gait analysis in older adults. Aging Clin Exp Res 18(2):174–176

    Article  PubMed  Google Scholar 

  • Lang AE (2011) A critical appraisal of the premotor symptoms of Parkinson’s disease: potential usefulness in early diagnosis and design of neuroprotective trials. Mov Disord 26(5):775–783

    Article  PubMed  Google Scholar 

  • Lee CS, Samii A, Sossi V, Ruth TJ, Schulzer M, Holden JE et al (2000) In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson’s disease. Ann Neurol 47(4):493–503

    Article  PubMed  CAS  Google Scholar 

  • Lewek MD, Poole R, Johnson J, Halawa O, Huang X (2010) Arm swing magnitude and asymmetry during gait in the early stages of Parkinson’s disease. Gait Posture 31(2):256–260

    Article  PubMed  Google Scholar 

  • Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC et al (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47(1):1–9

    Article  PubMed  CAS  Google Scholar 

  • Morris ME, Iansek R, Matyas TA, Summers JJ (1994) Ability to modulate walking cadence remains intact in Parkinson’s disease. J Neurol Neurosurg Psychiatry 57(12):1532–1534

    Article  PubMed  CAS  Google Scholar 

  • Nandhagopal R, Kuramoto L, Schulzer M, Mak E, Cragg J, McKenzie J et al (2011) Longitudinal evolution of compensatory changes in striatal dopamine processing in Parkinson’s disease. Brain 134(Pt 11):3290–3298

    Article  PubMed  Google Scholar 

  • Nelson AJ (1974) Functional ambulation profile. Phys Ther 54(10):1059–1065

    PubMed  CAS  Google Scholar 

  • Nelson AJ, Zwick D, Brody S, Doran C, Pulver L, Rooz G et al (2002) The validity of the GaitRite and the Functional Ambulation Performance scoring system in the analysis of Parkinson gait. NeuroRehabilitation 17(3):255–262

    PubMed  Google Scholar 

  • Pickering RM, Grimbergen YA, Rigney U, Ashburn A, Mazibrada G, Wood B et al (2007) A meta-analysis of six prospective studies of falling in Parkinson’s disease. Mov Disord 22(13):1892–1900

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Hausdorff JM (2009) Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking. J Neurol Neurosurg Psychiatry 80(3):347–350

    Article  PubMed  CAS  Google Scholar 

  • Rocchi L, Chiari L, Mancini M, Carlson-Kuhta P, Gross A, Horak FB (2006) Step initiation in Parkinson’s disease: influence of initial stance conditions. Neurosci Lett 406(1–2):128–132

    Article  PubMed  CAS  Google Scholar 

  • Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G et al (2004) Attending to the task: interference effects of functional tasks on walking in Parkinson’s disease and the roles of cognition, depression, fatigue, and balance. Arch Phys Med Rehabil 85(10):1578–1585

    Article  PubMed  Google Scholar 

  • van Nuenen BF, Helmich RC, Ferraye M, Thaler A, Hendler T, Orr-Urtreger A et al (2012) Cerebral pathological and compensatory mechanisms in the premotor phase of leucine-rich repeat kinase 2 parkinsonism. Brain 135(Pt 12):3687–3698

    Article  PubMed  Google Scholar 

  • Yang YR, Lee YY, Cheng SJ, Lin PY, Wang RY (2008) Relationships between gait and dynamic balance in early Parkinson’s disease. Gait Posture 27(4):611–615

    Article  PubMed  CAS  Google Scholar 

  • Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM (2005) Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 22(5):1248–1256

    Article  PubMed  Google Scholar 

  • Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23(3):329–342 (quiz 472)

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by the Rachadaphiseksomphot Endowment Fund Part of the “Strengthen CU’s Researcher’s Project” and research unit (RU) grant number GRU 52-026-30-005 of Chulalongkorn University, Bangkok, Thailand. We would like to thank Wannipat Buated for her assistance in patients recruitment and the data assortment.

Conflict of interest

The authors have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roongroj Bhidayasiri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Panyakaew, P., Bhidayasiri, R. The spectrum of preclinical gait disorders in early Parkinson’s disease: subclinical gait abnormalities and compensatory mechanisms revealed with dual tasking. J Neural Transm 120, 1665–1672 (2013). https://doi.org/10.1007/s00702-013-1051-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-013-1051-8

Keywords

Navigation