Top

Published in:

01-09-2013 | Original Communication

Low-frequency subthalamic nucleus deep brain stimulation for axial symptoms in advanced Parkinson’s disease

Authors: Christos Sidiropoulos, Richard Walsh, Christopher Meaney, Y. Y. Poon, Melanie Fallis, Elena Moro

Published in: Journal of Neurology | Issue 9/2013

Abstract

Axial symptoms such as freezing of gait and falls are common manifestations of advanced Parkinson’s disease (PD) and are partially responsive to medical treatment. High-frequency (≥130 Hz) deep brain stimulation (DBS) of the subthalamic nucleus (STN) is highly efficacious in ameliorating appendicular symptoms in PD. However, it is typically less effective in improving axial symptomatology, especially in the long term. We have studied the effects of low-frequency stimulation (LFS) (≤80 Hz) for improving speech, gait and balance dysfunction in the largest patient population to date. PD patients with bilateral STN-DBS and resistant axial symptoms were switched from chronic 130 Hz stimulation to LFS and followed up to 4 years. Primary outcome measures were total motor UPDRS scores, and axial and gait subscores before and after LFS. Bivariate analyses and correlation coefficients were calculated for the different conditions. Potential predictors of therapeutic response were also investigated. Forty-five advanced PD patients who had high frequency stimulation (HFS) for 39.5 ± 27.8 consecutive months were switched to LFS. LFS was kept on for a median period of 111.5 days before the assessment. There was no significant improvement in any of the primary outcomes between HFS and LFS, although a minority of patients preferred to be maintained on LFS for longer periods of time. No predictive factors of response could be identified. There was overall no improvement from LFS in axial symptoms. This could be partly due to some study limitations. Larger prospective trials are warranted to better clarify the impact of stimulation frequency on axial signs.

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 Off J Mov Disord Soc 19:1092–1099CrossRef

Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958PubMedCrossRef

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 Off J Mov Disord Soc 19:871–884CrossRef

Brozova H, Barnaure I, Alterman RL, Tagliati M (2009) STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 72:770 (author reply 770–771)PubMedCrossRef

Carpenter MB, Carleton SC, Keller JT, Conte P (1981) Connections of the subthalamic nucleus in the monkey. Brain Res 224:1–29PubMedCrossRef

Castrioto A, Lozano AM, Poon YY, Lang AE, Fallis M, Moro E (2011) Ten-year outcome of subthalamic stimulation in Parkinson disease: a blinded evaluation. Arch Neurol 68:1550–1556PubMedCrossRef

Fasano A, Romito LM, Daniele A, Piano C, Zinno M, Bentivoglio AR, Albanese A (2010) Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain J Neurol 133:2664–2676CrossRef

Fogelson N, Kuhn AA, Silberstein P, Limousin PD, Hariz M, Trottenberg T, Kupsch A, Brown P (2005) Frequency dependent effects of subthalamic nucleus stimulation in Parkinson’s disease. Neurosci Lett 382:5–9PubMedCrossRef

Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P, Marks WJ Jr, Rothlind J, Sagher O, Moy C, Pahwa R, Burchiel K, Hogarth P, Lai EC, Duda JE, Holloway K, Samii A, Horn S, Bronstein JM, Stoner G, Starr PA, Simpson R, Baltuch G, De Salles A, Huang GD, Reda DJ (2010) Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med 362:2077–2091PubMedCrossRef

10.

Giladi N, McMahon D, Przedborski S, Flaster E, Guillory S, Kostic V, Fahn S (1992) Motor blocks in Parkinson’s disease. Neurology 42:333–339PubMedCrossRef

11.

Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B, Paleacu D, Korczyn AD (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm (Vienna, Austria, 1996) 108:53–61CrossRef

12.

Hamani C, Moro E, Lozano AM (2011) The pedunculopontine nucleus as a target for deep brain stimulation. J Neural Transm (Vienna, Austria, 1996) 118:1461–1468CrossRef

13.

Jenkinson N, Nandi D, Muthusamy K, Ray NJ, Gregory R, Stein JF, Aziz TZ (2009) Anatomy, physiology, and pathophysiology of the pedunculopontine nucleus. Mov Disord Off J Mov Disord Soc 24:319–328CrossRef

14.

Kezunovic N, Urbano FJ, Simon C, Hyde J, Smith K, Garcia-Rill E (2011) Mechanism behind gamma band activity in the pedunculopontine nucleus. Eur J Neurosci 34:404–415PubMedCrossRef

15.

Koss AM, Alterman RL, Tagliati M, Shils JL (2005) Calculating total electrical energy delivered by deep brain stimulation systems. Ann Neurol 58:168 (author reply 168–169)PubMedCrossRef

16.

Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid AL, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934PubMedCrossRef

17.

Martinez-Gonzalez C, Bolam JP, Mena-Segovia J (2011) Topographical organization of the pedunculopontine nucleus. Frontiers Neuroanat 5:22

18.

Moreau C, Defebvre L, Destee A, Bleuse S, Clement F, Blatt JL, Krystkowiak P, Devos D (2008) STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 71:80–84PubMedCrossRef

19.

Moreau C, Defebvre L, Devos D, Marchetti F, Destee A, Stefani A, Peppe A (2009) STN versus PPN-DBS for alleviating freezing of gait: toward a frequency modulation approach? Mov Disord Off J Mov Disord Soc 24:2164–2166CrossRef

20.

Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 20:128–154PubMedCrossRef

21.

Piboolnurak P, Lang AE, Lozano AM, Miyasaki JM, Saint-Cyr JA, Poon YY, Hutchison WD, Dostrovsky JO, Moro E (2007) Levodopa response in long-term bilateral subthalamic stimulation for Parkinson’s disease. Mov Disord Off J Mov Disord Soc 22:990–997CrossRef

22.

Ricchi V, Zibetti M, Angrisano S, Merola A, Arduino N, Artusi CA, Rizzone M, Lopiano L, Lanotte M (2011) Transient effects of 80 Hz stimulation on gait in STN DBS treated PD patients: a 15 months follow-up study. Brain Stimul

23.

Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto JL, Pollak P, Rehncrona S, Kulisevsky J, Albanese A, Volkmann J, Hariz MI, Quinn NP, Speelman JD, Guridi J, Zamarbide I, Gironell A, Molet J, Pascual-Sedano B, Pidoux B, Bonnet AM, Agid Y, Xie J, Benabid AL, Lozano AM, Saint-Cyr J, Romito L, Contarino MF, Scerrati M, Fraix V, Van Blercom N (2005) Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain J Neurol 128:2240–2249CrossRef

24.

Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Foltynie T, Limousin P, Bogdanovic M, Zrinzo L, Green AL, Aziz TZ, Brown P (2012) Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in Parkinsonism. Brain J Neurol 135:148–160CrossRef

25.

Tsang EW, Hamani C, Moro E, Mazzella F, Saha U, Lozano AM, Hodaie M, Chuang R, Steeves T, Lim SY, Neagu B, Chen R (2012) Subthalamic deep brain stimulation at individualized frequencies for Parkinson disease. Neurology 78:1930–1938PubMedCrossRef

26.

Wagle Shukla A, Okun MS (2012) Personalized medicine in deep brain stimulation through utilization of neural oscillations. Neurology 78:1900–1901PubMedCrossRef

27.

Weaver FM, Follett KA, Stern M, Luo P, Harris CL, Hur K, Marks WJ Jr, Rothlind J, Sagher O, Moy C, Pahwa R, Burchiel K, Hogarth P, Lai EC, Duda JE, Holloway K, Samii A, Horn S, Bronstein JM, Stoner G, Starr PA, Simpson R, Baltuch G, De Salles A, Huang GD, Reda DJ (2012) Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology 79:55–65PubMedCrossRef

28.

Weinberger M, Hamani C, Hutchison WD, Moro E, Lozano AM, Dostrovsky JO (2008) Pedunculopontine nucleus microelectrode recordings in movement disorder patients. Exp Brain Res (Experimentelle Hirnforschung Experimentation cerebrale) 188:165–174CrossRef

29.

Welter ML, Houeto JL, Tezenas du Montcel S, Mesnage V, Bonnet AM, Pillon B, Arnulf I, Pidoux B, Dormont D, Cornu P, Agid Y (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain J Neurol 125:575–583CrossRef

30.

Wojtecki L, Timmermann L, Jorgens S, Sudmeyer M, Maarouf M, Treuer H, Gross J, Lehrke R, Koulousakis A, Voges J, Sturm V, Schnitzler A (2006) Frequency-dependent reciprocal modulation of verbal fluency and motor functions in subthalamic deep brain stimulation. Arch Neurol 63:1273–1276PubMedCrossRef

Title: Low-frequency subthalamic nucleus deep brain stimulation for axial symptoms in advanced Parkinson’s disease
Authors: Christos Sidiropoulos
Richard Walsh
Christopher Meaney
Y. Y. Poon
Melanie Fallis
Elena Moro
Publication date: 01-09-2013
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 9/2013
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-013-6983-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Low-frequency subthalamic nucleus deep brain stimulation for axial symptoms in advanced Parkinson’s disease

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 9/2013

Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis

Neurogenic orthostatic hypotension: pathophysiology, evaluation, and management

Widespread neuronal damage and cognitive dysfunction in spinocerebellar ataxia type 3

Effect of iron overload on the pituitary gland and associated imaging findings

Communications of the European neurological society

Patients with Parkinson’s disease and scans with (predominant) ipsilateral dopaminergic deficit