Long-term effect of subthalamic nucleus deep brain stimulation on freezing of gait in Parkinson’s disease

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  • 1 Departments of Neurology and
  • 4 Neurosurgery, Seoul National University Hospital, College of Medicine;
  • 3 Department of Neurology, Kyung Hee University Hospital, Seoul; and
  • 2 Department of Neurology, Aerospace Medical Center, Republic of Korea Air Force, Cheongju, Chungcheongbuk-do, Korea
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OBJECTIVE

Subthalamic nucleus deep brain stimulation (STN DBS) is effective against freezing of gait (FOG) in Parkinson’s disease (PD); however, whether this effect persists over the long term is debated. The aim of the current study was to investigate the long-term effect of STN DBS on FOG in patients with PD.

METHODS

Data on 52 cases in which PD patients received bilateral STN DBS were obtained from a prospective registry. The authors blindly analyzed FOG incidence and its severity from the videotapes of a 5-m walking task at the baseline and at the 1-, 2-, and 5- or 7-year follow-up visits. They also compared the axial score from the Unified Parkinson’s Disease Rating Scale (UPDRS) part III, UPDRS part II (UPDRS-II) item 14, and the FOG questionnaire (FOG-Q). Postoperatively, video-based FOG analysis and the axial score were evaluated under 4 conditions (off-medication/off-stimulation, off-medication/on-stimulation, on-medication/off-stimulation, and on-medication/on-stimulation), and UPDRS-II item 14 and the FOG-Q score were evaluated under 2 conditions (off-medication/on-stimulation and on-medication/on-stimulation).

RESULTS

During the off-medication state, the on-stimulation condition improved FOG outcomes, except for video-based FOG severity, up to the last follow-up compared with the baseline. Video-based FOG outcomes and the axial score during the off-medication state were improved with the on-stimulation condition up to the last follow-up compared with the off-stimulation condition. During the on-medication state, the on-stimulation condition did not improve any FOG outcome compared with the baseline; however, it improved video-based FOG outcomes up to the 2-year follow-up and the axial score up to the last follow-up compared with the off-stimulation condition.

CONCLUSIONS

Our findings suggest that STN DBS has a long-term effect on FOG in the off-medication state. However, STN DBS did not show a long-term effect on FOG in the on-medication state, although it had a short-term effect until the 2-year follow-up.

ABBREVIATIONS DBS = deep brain stimulation; FOG = freezing of gait; FOG-Q = FOG questionnaire; GEE = generalized estimating equation; ICC = intraclass correlation coefficient; PD = Parkinson’s disease; SNUH = Seoul National University Hospital; STN = subthalamic nucleus; UPDRS = Unified Parkinson’s Disease Rating Scale; UPDRS-II = UPDRS part II; UPDRS-III = UPDRS part III.

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Contributor Notes

Correspondence Beomseok Jeon: College of Medicine, Seoul National University Hospital, Seoul, Korea. brain@snu.ac.kr.

INCLUDE WHEN CITING Published online January 11, 2019; DOI: 10.3171/2018.8.JNS18350.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Baizabal-Carvallo JF, Jankovic J: Movement disorders induced by deep brain stimulation. Parkinsonism Relat Disord 25:19, 2016

  • 2

    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 68:15501556, 2011

    • Search Google Scholar
    • Export Citation
  • 3

    Davis JT, Lyons KE, Pahwa R: Freezing of gait after bilateral subthalamic nucleus stimulation for Parkinson’s disease. Clin Neurol Neurosurg 108:461464, 2006

    • Search Google Scholar
    • Export Citation
  • 4

    Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, : A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355:896908, 2006

    • Search Google Scholar
    • Export Citation
  • 5

    Fasano A, Romito LM, Daniele A, Piano C, Zinno M, Bentivoglio AR, : Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain 133:26642676, 2010

    • Search Google Scholar
    • Export Citation
  • 6

    Ferraye MU, Debû B, Fraix V, Xie-Brustolin J, Chabardès S, Krack P, : Effects of subthalamic nucleus stimulation and levodopa on freezing of gait in Parkinson disease. Neurology 70:14311437, 2008

    • Search Google Scholar
    • Export Citation
  • 7

    Fleiss JL: The Design and Analysis of Clinical Experiments. New York: Wiley, 1999

  • 8

    Gervais-Bernard H, Xie-Brustolin J, Mertens P, Polo G, Klinger H, Adamec D, : Bilateral subthalamic nucleus stimulation in advanced Parkinson’s disease: five year follow-up. J Neurol 256:225233, 2009

    • Search Google Scholar
    • Export Citation
  • 9

    Kim HJ, Jeon BS, Paek SH, Lee JY, Kim HJ, Kim CK, : Bilateral subthalamic deep brain stimulation in Parkinson disease patients with severe tremor. Neurosurgery 67:626632, 2010

    • Search Google Scholar
    • Export Citation
  • 10

    Kim HJ, Paek SH, Kim JY, Lee JY, Lim YH, Kim DG, : Two-year follow-up on the effect of unilateral subthalamic deep brain stimulation in highly asymmetric Parkinson’s disease. Mov Disord 24:329335, 2009

    • Search Google Scholar
    • Export Citation
  • 11

    Kim R, Kim HJ, Kim A, Kim Y, Kim AR, Shin CW, : Depression may negatively affect the change in freezing of gait following subthalamic nucleus stimulation in Parkinson’s disease. Parkinsonism Relat Disord 44:133136, 2017

    • Search Google Scholar
    • Export Citation
  • 12

    Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, : Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:19251934, 2003

    • Search Google Scholar
    • Export Citation
  • 13

    Landis JR, Koch GG: The measurement of observer agreement for categorical data. Biometrics 33:159174, 1977

  • 14

    Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, : Core assessment program for intracerebral transplantations (CAPIT). Mov Disord 7:213, 1992

    • Search Google Scholar
    • Export Citation
  • 15

    Lee JY, Han JH, Kim HJ, Jeon BS, Kim DG, Paek SH: STN DBS of advanced Parkinson’s disease experienced in a specialized monitoring unit with a prospective protocol. J Korean Neurosurg Soc 44:2635, 2008

    • Search Google Scholar
    • Export Citation
  • 16

    Li J, Zhang Y, Li Y: Long-term follow-up of bilateral subthalamic nucleus stimulation in Chinese Parkinson’s disease patients. Br J Neurosurg 29:329333, 2015

    • Search Google Scholar
    • Export Citation
  • 17

    Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, : Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 339:11051111, 1998

    • Search Google Scholar
    • Export Citation
  • 18

    Moreau C, Defebvre L, Destée A, Bleuse S, Clement F, Blatt JL, : STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 71:8084, 2008

    • Search Google Scholar
    • Export Citation
  • 19

    Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, : Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30:459463, 2009

    • Search Google Scholar
    • Export Citation
  • 20

    Niu L, Ji LY, Li JM, Zhao DS, Huang G, Liu WP, : Effect of bilateral deep brain stimulation of the subthalamic nucleus on freezing of gait in Parkinson’s disease. J Int Med Res 40:11081113, 2012

    • Search Google Scholar
    • Export Citation
  • 21

    Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR: Freezing of gait: a practical approach to management. Lancet Neurol 14:768778, 2015

    • Search Google Scholar
    • Export Citation
  • 22

    Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A: Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734744, 2011

    • Search Google Scholar
    • Export Citation
  • 23

    Rizzone MG, Fasano A, Daniele A, Zibetti M, Merola A, Rizzi L, : Long-term outcome of subthalamic nucleus DBS in Parkinson’s disease: from the advanced phase towards the late stage of the disease? Parkinsonism Relat Disord 20:376381, 2014

    • Search Google Scholar
    • Export Citation
  • 24

    Rochester L, Chastin SF, Lord S, Baker K, Burn DJ: Understanding the impact of deep brain stimulation on ambulatory activity in advanced Parkinson’s disease. J Neurol 259:10811086, 2012

    • Search Google Scholar
    • Export Citation
  • 25

    Romito LM, Contarino MF, Vanacore N, Bentivoglio AR, Scerrati M, Albanese A: Replacement of dopaminergic medication with subthalamic nucleus stimulation in Parkinson’s disease: long-term observation. Mov Disord 24:557563, 2009

    • Search Google Scholar
    • Export Citation
  • 26

    Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N: Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391398, 2003

    • Search Google Scholar
    • Export Citation
  • 27

    Schlenstedt C, Shalash A, Muthuraman M, Falk D, Witt K, Deuschl G: Effect of high-frequency subthalamic neurostimulation on gait and freezing of gait in Parkinson’s disease: a systematic review and meta-analysis. Eur J Neurol 24:1826, 2017

    • Search Google Scholar
    • Export Citation
  • 28

    Shah RS, Chang SY, Min HK, Cho ZH, Blaha CD, Lee KH: Deep brain stimulation: technology at the cutting edge. J Clin Neurol 6:167182, 2010

    • Search Google Scholar
    • Export Citation
  • 29

    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 75:12921299, 2010

    • Search Google Scholar
    • Export Citation
  • 30

    Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Bogdanovic M, Coyne TJ, : A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation. Brain 134:20852095, 2011

    • Search Google Scholar
    • Export Citation
  • 31

    Vercruysse S, Vandenberghe W, Münks L, Nuttin B, Devos H, Nieuwboer A: Effects of deep brain stimulation of the subthalamic nucleus on freezing of gait in Parkinson’s disease: a prospective controlled study. J Neurol Neurosurg Psychiatry 85:871877, 2014

    • Search Google Scholar
    • Export Citation
  • 32

    Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ Jr, : Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 301:6373, 2009

    • Search Google Scholar
    • Export Citation
  • 33

    Williams A, Gill S, Varma T, Jenkinson C, Quinn N, Mitchell R, : Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson’s disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol 9:581591, 2010

    • Search Google Scholar
    • Export Citation
  • 34

    Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, : Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord 26:23272334, 2011

    • Search Google Scholar
    • Export Citation

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