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Dopaminergic medication does not improve stepping responses following backward and forward balance perturbations in patients with Parkinson’s disease

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Abstract

In this study, we investigated the effect of dopaminergic medication on reactive stepping responses to forward and backward balance perturbations in patients with moderately severe Parkinson’s disease (PD). Twelve PD patients, Hoehn and Yahr stage ranging from 2 to 3, and 15 healthy controls were exposed to multidirectional translational stance perturbations on a moveable platform. Perturbations were unpredictable in terms of amplitude, timing and direction. Patients were tested in the medication ON and OFF (at least 12 h of dopaminergic medication withdrawal) state on two separate days. Forward and backward stepping responses were quantified in terms of (1) presence, onset and amplitude of anticipatory postural adjustments (APAs); (2) spatiotemporal step variables (step onset, length and velocity); and (3) leg inclination angle at first stepping-foot contact. When perturbed forward, patients performed worse than controls in terms of step length (0.32 ± 0.07 vs. 0.38 ± 0.05 m, p = 0.01) and step velocity (1.21 ± 0.16 vs. 1.37 ± 0.13 m/s, p = 0.01), while step onset was not different. The number of steps with an APA was larger in patients in the OFF state than in controls which was, however, only significant after forward perturbations (43 vs. 20 %, p = 0.01). Following backward perturbations, leg angles at foot contact were smaller in patients compared to controls (−2.71° ± 4.29° vs. 0.26° ± 2.80°, p = 0.04) reflecting a poorer mechanical efficiency of the step. Dopaminergic medication had no significant effect on any of these outcomes. In conclusion, dopaminergic medication does not improve underscaling of stepping responses in PD. Therefore, other interventions are needed to improve these important defense postural reactions.

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References

  1. Dibble LE, Christensen J, Ballard DJ, Foreman KB (2008) Diagnosis of fall risk in Parkinson disease: an analysis of individual and collective clinical balance test interpretation. Phys Ther 88:323–332

    Article  PubMed  Google Scholar 

  2. Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG (2008) The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837–844

    Article  PubMed  Google Scholar 

  3. Cooper C (1997) The crippling consequences of fractures and their impact on quality of life. Am J Med 103:12S–17S (discussion 17S–19S)

    Article  CAS  PubMed  Google Scholar 

  4. Matinolli M, Korpelainen JT, Sotaniemi KA, Myllyla VV, Korpelainen R (2011) Recurrent falls and mortality in Parkinson’s disease: a prospective two-year follow-up study. Acta Neurol Scand 123:193–200

    Article  CAS  PubMed  Google Scholar 

  5. Wenning GK, Ebersbach G, Verny M et al (1999) Progression of falls in postmortem-confirmed parkinsonian disorders. Mov Disord 14:947–950

    Article  CAS  PubMed  Google Scholar 

  6. Stowe RL, Ives NJ, Clarke C et al (2008) Dopamine agonist therapy in early Parkinson’s disease. Cochrane Database Syst Rev 16(2):CD006564

  7. Espay AJ, Fasano A, van Nuenen BF, Payne MM, Snijders AH, Bloem BR (2012) “On” state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology 78:454–457

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Beuter A, Hernandez R, Rigal R, Modolo J, Blanchet PJ (2008) Postural sway and effect of levodopa in early Parkinson’s disease. Can J Neurol Sci 35:65–68

    Article  PubMed  Google Scholar 

  9. 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 Parkinso’s disease. Mov Disord 11:509–521

    Article  CAS  PubMed  Google Scholar 

  10. Horak FB, Frank J, Nutt J (1996) Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J Neurophysiol 75:2380–2396

    CAS  PubMed  Google Scholar 

  11. King LA, Horak FB (2008) Lateral stepping for postural correction in Parkinson’s disease. ArchPhysMedRehabil 89:492–499

    Google Scholar 

  12. King LA, St George RJ, Carlson-Kuhta P, Nutt JG, Horak FB (2010) Preparation for compensatory forward stepping in Parkinson’s disease. Arch Phys Med Rehabil 91:1332–1338

    Article  PubMed Central  PubMed  Google Scholar 

  13. Mancini M, Rocchi L, Horak FB, Chiari L (2008) Effects of Parkinson’s disease and levodopa on functional limits of stability. Clin Biomech (Bristol, Avon) 23:450–458

    Article  Google Scholar 

  14. McNeely ME, Duncan RP, Earhart GM (2012) Medication improves balance and complex gait performance in Parkinson disease. Gait Posture 36(1):144–148

  15. Nova IC, Perracini MR, Ferraz HB (2004) Levodopa effect upon functional balance of Parkinson’s disease patients. ParkinsonismRelat Disord 10:411–415

    Article  Google Scholar 

  16. 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(12):1303–1308

  17. McVey MA, Stylianou AP, Luchies CW et al (2009) Early biomechanical markers of postural instability in Parkinson’s disease. Gait Posture 30:538–542

    Article  PubMed  Google Scholar 

  18. 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 75:1245–1254

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Horak FB, Dimitrova D (2005) Direction-specific postural instability in subjects with Parkinson’s disease. ExpNeurol 193:504–521

    Google Scholar 

  20. Smulders K, Esselink RA, De Swart BJ, Geurts AC, Bloem BR, Weerdesteyn V (2014) Postural inflexibility in PD: does it affect compensatory stepping? Gait Posture 39:700–706

    Article  PubMed  Google Scholar 

  21. Nonnekes J, Scotti A, Oude Nijhuis LB et al (2013) Are postural responses to backward and forward perturbations processed by different neural circuits? Neuroscience 245:109–120

    Article  CAS  PubMed  Google Scholar 

  22. Weerdesteyn V, Laing AC, Robinovitch SN (2012) The body configuration at step contact critically determines the successfulness of balance recovery in response to large backward perturbations. Gait Posture 35:462–466

    Article  PubMed  Google Scholar 

  23. Goetz CG, Tilley BC, Shaftman SR et al (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170

    Article  PubMed  Google Scholar 

  24. Nieuwboer A, Rochester L, Herman T et al (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. GaitPosture 30:459–463

    Google Scholar 

  25. Carpenter MG, Thorstensson A, Cresswell AG (2005) Deceleration affects anticipatory and reactive components of triggered postural responses. Exp Brain Res 167:433–445

    Article  PubMed  Google Scholar 

  26. Tokuno CD, Cresswell AG, Thorstensson A, Carpenter MG (2010) Age-related changes in postural responses revealed by support-surface translations with a long acceleration-deceleration interval. Clin Neurophysiol 121:109–117

    Article  PubMed  Google Scholar 

  27. Davis RB, Ounpuu S, Tyburski D, Gage JR (1991) A gait analysis data-collection and reduction technique. Hum Mov Sci 10:575–587

    Article  Google Scholar 

  28. Visser JE, Allum JH, Carpenter MG et al (2008) Subthalamic nucleus stimulation and levodopa-resistant postural instability in Parkinson’s disease. J Neurol 255:205–210

    Article  PubMed  Google Scholar 

  29. Vrancken AM, Allum JH, Peller M et al (2005) Effect of bilateral subthalamic nucleus stimulation on balance and finger control in Parkinson’s disease. J Neurol 252:1487–1494

    Article  CAS  PubMed  Google Scholar 

  30. Grimbergen YA, Langston JW, Roos RA, Bloem BR (2009) Postural instability in Parkinson’s disease: the adrenergic hypothesis and the locus coeruleus. Expert Rev Neurother 9:279–290

    Article  CAS  PubMed  Google Scholar 

  31. Bohnen NI, Albin RL (2010) The cholinergic system and Parkinson disease. BehavBrain Res 221(2):564–573

  32. Thevathasan W, Silburn PA, Brooker H et al (2010) The impact of low-frequency stimulation of the pedunculopontine nucleus region on reaction time in parkinsonism. J Neurol Neurosurg Psychiatry 81:1099–1104

    Article  PubMed  Google Scholar 

  33. Moro E, Hamani C, Poon YY et al (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson’s disease. Brain 133:215–224

    Article  PubMed  Google Scholar 

  34. Chung KA, Lobb BM, Nutt JG, Horak FB (2010) Effects of a central cholinesterase inhibitor on reducing falls in Parkinson disease. Neurology 75:1263–1269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Jacobs JV, Horak FB (2006) Abnormal proprioceptive-motor integration contributes to hypometric postural responses of subjects with Parkinson’s disease. Neuroscience 141:999–1009

    Article  CAS  PubMed  Google Scholar 

  36. Sethi K (2008) Levodopa unresponsive symptoms in Parkinson disease. Mov Disord 23(Suppl 3):S521–S533

    Article  PubMed  Google Scholar 

  37. Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA (1997) Step initiation in Parkinson’s disease: influence of levodopa and external sensory triggers. Mov Disord 12:206–215

    Article  CAS  PubMed  Google Scholar 

  38. Jacobs JV, Nutt JG, Carlson-Kuhta P, Stephens M, Horak FB (2009) Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp Neurol 215:334–341

    Article  PubMed Central  PubMed  Google Scholar 

  39. Nanhoe-Mahabier W, Allum JH, Overeem S, Borm GF, Oude Nijhuis LB, Bloem BR (2012) First trial reactions and habituation rates over successive balance perturbations in Parkinson’s disease. Neuroscience 217:123–129

    Article  CAS  PubMed  Google Scholar 

  40. Oude Nijhuis LB, Allum JH, Borm GF, Honegger F, Overeem S, Bloem BR (2009) Directional sensitivity of “first trial” reactions in human balance control. J Neurophysiol 101:2802–2814

    Article  PubMed  Google Scholar 

  41. Bohnen NI, Frey KA, Studenski S et al (2013) Gait speed in Parkinson disease correlates with cholinergic degeneration. Neurology 81:1611–1616

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Karachi C, Grabli D, Bernard FA et al (2010) Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 120:2745–2754

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Rochester L, Yarnall AJ, Baker MR et al (2012) Cholinergic dysfunction contributes to gait disturbance in early Parkinson’s disease. Brain 135:2779–2788

    Article  PubMed Central  PubMed  Google Scholar 

  44. Protas EJ, Mitchell K, Williams A, Qureshy H, Caroline K, Lai EC (2005) Gait and step training to reduce falls in Parkinso’s disease. NeuroRehabilitation 20:183–190

    PubMed  Google Scholar 

  45. van Nimwegen M, Speelman AD, Overeem S et al (2013) Promotion of physical activity and fitness in sedentary patients with Parkinson’s disease: randomised controlled trial. BMJ 346:f576

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This research was funded by a Radboud University Medical Centre Research Grant to J. H. Nonnekes and Netherlands Organization for Scientific Research Veni Research Grant 916.10.106 to V. Weerdesteyn. We thank Roland Loeffen for technical assistance.

Conflicts of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Rehabilitation, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Po Box 9101, 6500 HB, Nijmegen, The Netherlands

    Digna de Kam, Jorik Nonnekes, Alexander C. H. Geurts & Vivian Weerdesteyn

  2. Department of Neurology, Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, Nijmegen, The Netherlands

    Lars B. Oude Nijhuis & Bastiaan R. Bloem

  3. Sint Maartenskliniek Research, Nijmegen, The Netherlands

    Alexander C. H. Geurts & Vivian Weerdesteyn

Authors
  1. Digna de Kam
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  2. Jorik Nonnekes
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  3. Lars B. Oude Nijhuis
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  4. Alexander C. H. Geurts
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  5. Bastiaan R. Bloem
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  6. Vivian Weerdesteyn
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Correspondence to Digna de Kam.

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de Kam, D., Nonnekes, J., Oude Nijhuis, L.B. et al. Dopaminergic medication does not improve stepping responses following backward and forward balance perturbations in patients with Parkinson’s disease. J Neurol 261, 2330–2337 (2014). https://doi.org/10.1007/s00415-014-7496-3

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  • DOI: https://doi.org/10.1007/s00415-014-7496-3

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