Nigral stimulation for resistant axial motor impairment in Parkinson's disease? A randomized controlled trial

Brain

Volumn 136, Issue 7, 2013, Pages 2098-2108

  Weiss, Daniel ^a,b,c   Walach, Margarete ^a,b,c   Meisner, Christoph ^b   Fritz, Melanie ^a,b,c   Scholten, Marlieke ^a,b,c   Breit, Sorin ^a,b,c   Plewnia, Christian ^b   Bender, Benjamin ^b   Gharabaghi, Alireza ^b   Wächter, Tobias ^a,b,c   Krüger, Rejko ^a,b,c  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

DBS; freezing; gait; Parkinson's disease; subthalamic nucleus

Indexed keywords

LEVODOPA;

ADULT; AGED; ARTICLE; BODY EQUILIBRIUM; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; FEMALE; FOLLOW UP; GAIT; HUMAN; MALE; MOTOR DYSFUNCTION; PARKINSON DISEASE; PATIENT SAFETY; PRIORITY JOURNAL; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; UNIFIED PARKINSON DISEASE RATING SCALE;

EID: 84879948179     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt122     Document Type: Article

References (55)

1. Bejjani BP, Damier P, Arnulf I, Thivard L, Bonnet AM, Dormont D, et al. Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med 1999; 340: 1476-80
2. Bender R, Lange S. Adjusting for multiple testing-when and how? J Clin Epidemiol 2001; 54: 343-9
3. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: Validation of an instrument. Can J Public Health 1992; 83: S7-11
4. Blomstedt P, Hariz MI, Lees A, Silberstein P, Limousin P, Yelnik J, et al. Acute severe depression induced by intraoperative stimulation of the substantia nigra: A case report. Parkinsonism Relat Disord 2008; 14: 253-6
5. Breit S, Lessmann L, Unterbrink D, Popa RC, Gasser T, Schulz JB. Lesion of the pedunculopontine nucleus reverses hyperactivity of the subthalamic nucleus and substantia nigra pars reticulata in a 6-hydroxydopamine rat model. Eur J Neurosci 2006; 24: 2275-82
6. Carpenter M, Carleton SC, Keller JT, Conte P. Connection of the subthalamic nucleus in the monkey. Brain Res 1981; 224: 1-29
7. Castrioto A, Lozano AM, Poon YY, Lang AE, Fallis M, Moro E. Ten-year outcome of subthalamic stimulation in Parkinson disease: A blinded evaluation. Arch Neurol 2011; 68: 1550-6
8. Chastan N, Westby GW, Yelnik J, Bardinet E, Do MC, Agid Y, et al. Effects of nigral stimulation on locomotion and postural stability in patients with Parkinson's disease. Brain 2009; 132: 172-84
9. Childs JA, Gale K. Neurochemical evidence for nigrotegmental GABAergic projection. Brain Res 1983; 258: 109-114
10. Cooper SE, McIntyre CC, Fernandez HH, Vitek JL. Association of deep brain stimulation washout effects with Parkinson disease duration. JAMA Neurol 2013; 70: 95-9
11. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schafer H, Botzel K, et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006; 355: 896-908
12. Dybdal D, Forcelli PA, Dubach M, Oppedisano M, Holmes A, Malkova L, et al. Topography of dyskinesias and torticollis evoked by inhibition of substantia nigra pars reticulata. Mov Disord 2013; 28: 460-8
13. Fasano A, Herzog J, Seifert E, Stolze H, Falk D, Reese R, et al. Modulation of gait coordination by subthalamic stimulation improves freezing of gait. Mov Disord 2011; 26: 844-51
14. Ferraye MU, Debu B, Fraix V, Goetz L, Ardouin C, Yelnik J, et al. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain 2010; 133: 205-14
15. Giladi N, Tal J, Azulay T, Rascol O, Brooks DJ, Melamed E, et al. Validation of the freezing of gait questionnaire in patients with Parkinson's disease. Mov Disord 2009; 24: 655-61
16. Grofova I, Zhou M. Nigral innervation of cholinergic and glutamatergic cells in the rat mesopontine tegmentum: Light and electron microscopic anterograde tracing and immunohistochemical studies. J Comp Neurol 1998; 395: 359-79
17. Hamani C, Moro E, Lozano AM. The pedunculopontine nucleus as a target for deep brain stimulation. J Neural Transm 2011; 118: 1461-8
18. Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, et al. Subthalamic nucleus deep brain stimulation: Summary and meta-Analysis of outcomes. Mov Disord 2006; 21 (Suppl 14): S290-304
19. Kovacs N, Janszky J, Nagy F, Balas I. Changing to interleaving stimulation might improve dystonia in cases not responding to pallidal stimulation. Mov Disord 2012; 27: 163-5
20. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 2003; 349: 1925-34
21. Kuriakose R, Saha U, Castillo G, Udupa K, Ni Z, Gunraj C, et al. The nature and time course of cortical activation following subthalamic stimulation in Parkinson's disease. Cereb Cortex 2010; 20: 1926-36
22. Lafreniere-Roula M, Kim E, Hutchison WD, Lozano AM, Hodaie M, Dostrovsky JO. High-frequency microstimulation in human globus pallidus and substantia nigra. Exp Brain Res 2010; 205: 251-61
23. McNeely ME, Hershey T, Campbell MC, Tabbal SD, Karimi M, Hartlein JM, et al. Effects of deep brain stimulation of dorsal versus ventral subthalamic nucleus regions on gait and balance in Parkinson's disease. J Neurol Neurosurg Psychiatry 2011; 82: 1250-5
24. Moreau C, Defebvre L, Destee A, Bleuse S, Clement F, Blatt JL, et al. STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 2008; 71: 80-4
25. Moreau C, Delval A, Defebvre L, Dujardin K, Duhamel A, Petyt G, et al. Methylphenidate for gait hypokinesia and freezing in patients with Parkinson's disease undergoing subthalamic stimulation: A multicentre, parallel, randomised, placebo-controlled trial. Lancet Neurol 2012; 11: 589-96
26. Moro E, Hamani C, Poon YY, Al-Khairallah T, Dostrovsky JO, Hutchison WD, et al. Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. Brain 2010; 133: 215-24
27. Nakamura Y, Tokuno H, Moriizumi T, Kitao Y, Kudo M. Monosynaptic nigral inputs to the pedunculopontine tegmental nucleus neurons which send their axons to the medial reticular formation in the medulla oblongata. An electron microscopic study in the cat. Neurosci Lett 1989; 103: 145-50
28. Nandi D, Jenkinson N, Stein J, Aziz T. The pedunculopontine nucleus in Parkinson's disease: Primate studies. Br J Neurosurg 2008; 22 (Suppl 1): S4-8
29. Noda T, Oka H. Distribution and morphology of tegmental neurons receiving nigral inhibitory inputs in the cat: An intracellular HRP study. J Comp Neurol 1986; 244: 254-66
30. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: Moving forward on a mysterious clinical phenomenon. Lancet Neurol 2011; 10: 734-44
31. Okun MS, Fernandez HH, Wu SS, Kirsch-Darrow L, Bowers D, Bova F, et al. Cognition and mood in Parkinson's disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: The COMPARE trial. Ann Neurol 2009; 65: 586-95
32. Peto V, Jenkinson C, Fitzpatrick R. Determining minimally important differences for the PDQ-39 Parkinson's disease questionnaire. Age Ageing 2001; 30: 299-302
33. Potter M, Herzog J, Siebner HR, Kopper F, Steigerwald F, Deuschl G, et al. Subthalamic nucleus stimulation modulates audiospinal reactions in Parkinson disease. Neurology 2008; 70: 1445-51
34. Potter-Nerger M, Ilic TV, Siebner HR, Deuschl G, Volkmann J. Subthalamic nucleus stimulation restores corticospinal facilitation in Parkinson's disease. Mov Disord 2008; 23: 2210-5
35. Ricchi V, Zibetti M, Angrisano S, Merola A, Arduino N, Artusi CA, et al. Transient effects of 80 Hz stimulation on gait in STN DBS treated PD patients: A 15 months follow-up study. Brain Stimul 2012; 5: 388-92
36. Salenius S, Avikainen S, Kaakkola S, Hari R, Brown P. Defective cortical drive to muscle in Parkinson's disease and its improvement with levodopa. Brain 2002; 125: 491-500
37. Schiesling C, Kieper N, Seidel K, Kruger R. Review: Familial Parkinson's disease -genetics, clinical phenotype and neuropathology in relation to the common sporadic form of the disease. Neuropathol Appl Neurobiol 2008; 34: 255-71
38. Schuepbach WM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, et al. Neurostimulation for Parkinson's disease with early motor complications. N Engl J Med 2013; 368: 610-22
39. St George RJ, Nutt JG, Burchiel KJ, Horak FB. A meta-regression of the long-Term effects of deep brain stimulation on balance and gait in PD. Neurology 2010; 75: 1292-9
40. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, et al. Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. Brain 2007; 130: 1596-607
41. Storch A, Odin P, Trender-Gerhard I, Fuchs G, Reifschneider G, Ray Chaudhuri K, et al. Non-motor Symptoms Questionnaire and Scale for Parkinson's disease. Cross-cultural adaptation into the German language [in German]. Nervenarzt 2010; 81: 980-5
42. Sutton AC, Yu W, Calos ME, Smith AB, Ramirez-Zamora A, Molho ES, et al. Deep brain stimulation of the substantia nigra pars reticulata improves forelimb akinesia in the hemiparkinsonian rat. J Neurophysiol 2013; 109: 363-74
43. Thevathasan W, Coyne TJ, Hyam JA, Kerr G, Jenkinson N, Aziz TZ, et al. Pedunculopontine nucleus stimulation improves gait freezing in Parkinson disease. Neurosurgery 2011a; 69: 1248-53; discussion 1254
44. Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Bogdanovic M, Coyne TJ, et al. A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation. Brain 2011b; 134: 2085-95
45. Tsang EW, Hamani C, Moro E, Mazzella F, Poon YY, Lozano AM, et al. Involvement of the human pedunculopontine nucleus region in voluntary movements. Neurology 2010; 75: 950-9
46. Ulla M, Thobois S, Llorca PM, Derost P, Lemaire JJ, Chereau-Boudet I, et al. Contact dependent reproducible hypomania induced by deep brain stimulation in Parkinson's disease: Clinical, anatomical and functional imaging study. J Neurol Neurosurg Psychiatry 2011; 82: 607-14
47. Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ Jr, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: A randomized controlled trial. JAMA 2009; 301: 63-73
48. Weiss D, Breit S, Hoppe J, Hauser AK, Freudenstein D, Kruger R, et al. Subthalamic nucleus stimulation restores the efferent cortical drive to muscle in parallel to functional motor improvement. Eur J Neurosci 2012a; 35: 896-908
49. Weiss D, Breit S, Wachter T, Plewnia C, Gharabaghi A, Kruger R. Combined stimulation of the substantia nigra pars reticulata and the subthalamic nucleus is effective in hypokinetic gait disturbance in Parkinson's disease. J Neurol 2011a; 258: 1183-5
50. Weiss D, Brockmann K, Srulijes K, Meisner C, Klotz R, Reinbold S, et al. Long-Term follow-up of subthalamic nucleus stimulation in glucocerebrosidase- Associated Parkinson's disease. J Neurol 2012b; 259: 1970-2
51. Weiss D, Wachter T, Meisner C, Fritz M, Gharabaghi A, Plewnia C, et al. Combined STN/SNr-DBS for the treatment of refractory gait disturbances in Parkinson's disease: Study protocol for a randomized controlled trial. Trials 2011b; 12: 222
52. Wellek S, Blettner M. On the proper use of the crossover design in clinical trials: Part 18 of a series on evaluation of scientific publications. Dtsch Arztebl Int 2012; 109: 276-81
53. Winder-Rhodes SE, Evans JR, Ban M, Mason SL, Williams-Gray CH, Foltynie T, et al. Glucocerebrosidase mutations influence the natural history of Parkinson's disease in a community-based incident cohort. Brain 2013; 136: 392-9
54. Wojtecki L, Vesper J, Schnitzler A. Interleaving programming of subthalamic deep brain stimulation to reduce side effects with good motor outcome in a patient with Parkinson's disease. Parkinsonism Relat Disord 2011; 17: 293-4
55. Ziegler K, Schroeteler F, Ceballos-Baumann AO, Fietzek UM. A new rating instrument to assess festination and freezing gait in Parkinsonian patients. Mov Disord 2010; 25: 1012-8