Vol 53, No 5 (2019)
Research Paper
Published online: 2019-10-17
Evaluating reflexive saccades and UDPRS as markers of Deep Brain Stimulation and Best Medical Treatment improvements in Parkinson’s disease patients: a prospective controlled study
1
, 2, 1, 3, 2, 1
, 2, 1, 3, 2, 1
Abstract
Introduction. To date, there has been no clear evidence regarding the evaluation of saccades as a monitoring tool of motor impairment in Parkinson’s disease (PD) Subthalamic Nucleus Deep Brain Stimulation (STN-DBS) patients. The aim of this study was to evaluate the long-term impact of STN-DBS and pharmacological treatment on reflexive saccades’ (RS) parameters and UPDRS alterations.
Material and methods. The DBS group consisted of 20 PD patients who underwent bilateral STN-DBS. The Postoperative (POP) group consisted of 14 post-DBS patients. The Best Medical Therapy (BMT) group consisted of 20 patients on pharmacotherapy only. RS parameters and the UPDRS scale were measured during three visits in four phases of treatment (i.e. BMT-ON/OFF, DBS-ON/OFF).
Results. The significant UPDRS III and UPDRS. Total improvements were observed in all three study groups (p < 0.05), but RS latency improvement was stated only in the DBS group in the DBS-ON phase (p < 0.05). A significant correlation between RS latency increase and UPDRS III score worsening was found in all study groups, with the most evident effect in the UPDRS III ON phase (p < 0.05).
Conclusion. RS parameters correlated with UPDRS III outcomes during the postoperative period in DBS-STN patients. Therefore, saccadic evaluation may be a good biomarker of the patient’s response to surgical and/or pharmacological treatment.
Keywords: Parkinson’s diseaseBMTDBSreflexive saccadesmarker
References
- Krack P, Pollak P, Limousin P, et al. Stimulation of subthalamic nucleus alleviates tremor in Parkinson's disease. Lancet. 1997; 350(9092): 1675.
- Krack P, Batir A, Van Blercom N, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med. 1998; 339(16): 1105–1111.
- Limousin P, Pollak P, Benazzouz A, et al. Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord. 1995; 10(5): 672–674.
- Krack P, Limousin P, Benabid AL, et al. Chronic stimulation of subthalamic nucleus improves levodopa-induced dyskinesias in Parkinson's disease. Lancet. 1997; 350(9092): 1676.
- Fawcett AP, Dostrovsky JO, Lozano AM, et al. Eye movement-related responses of neurons in human subthalamic nucleus. Exp Brain Res. 2005; 162(3): 357–365.
- Fawcett AP, Cunic D, Hamani C, et al. Saccade-related potentials recorded from human subthalamic nucleus. Clin Neurophysiol. 2007; 118(1): 155–163.
- Sieger T, Bonnet C, Serranová T, et al. Basal ganglia neuronal activity during scanning eye movements in Parkinson's disease. PLoS One. 2013; 8(11): e78581.
- Chan F, Armstrong IT, Pari G, et al. Deficits in saccadic eye-movement control in Parkinson's disease. Neuropsychologia. 2005; 43(5): 784–796.
- Choi SM, Lee SH, Choi KH, et al. Directional asymmetries of saccadic hypometria in patients with early Parkinson's disease and unilateral symptoms. Eur Neurol. 2011; 66(3): 170–174.
- Pinkhardt EH, Jürgens R, Lulé D, et al. Eye movement impairments in Parkinson's disease: possible role of extradopaminergic mechanisms. BMC Neurol. 2012; 12: 5.
- Rivaud-Péchoux S, Vermersch AI, Gaymard B, et al. Improvement of memory guided saccades in parkinsonian patients by high frequency subthalamic nucleus stimulation. J Neurol Neurosurg Psychiatry. 2000; 68(3): 381–384.
- Yugeta A, Terao Y, Fukuda H, et al. Effects of STN stimulation on the initiation and inhibition of saccade in Parkinson disease. Neurology. 2010; 74(9): 743–748.
- Antoniades CA, Buttery P, FitzGerald JJ, et al. Deep brain stimulation: eye movements reveal anomalous effects of electrode placement and stimulation. PLoS One. 2012; 7(3): e32830.
- Nilsson MH, Patel M, Rehncrona S, et al. Subthalamic deep brain stimulation improves smooth pursuit and saccade performance in patients with Parkinson's disease. J Neuroeng Rehabil. 2013; 10: 33.
- Kumru H, Summerfield C, Valldeoriola F, et al. Effects of subthalamic nucleus stimulation on characteristics of EMG activity underlying reaction time in Parkinson's disease. Mov Disord. 2004; 19(1): 94–100.
- Sauleau P, Pollak P, Krack P, et al. Subthalamic stimulation improves orienting gaze movements in Parkinson's disease. Clin Neurophysiol. 2008; 119(8): 1857–1863.
- Temel Y, Visser-Vandewalle V, Carpenter RHS. Saccadometry: a novel clinical tool for quantification of the motor effects of subthalamic nucleus stimulation in Parkinson's disease. Exp Neurol. 2009; 216(2): 481–489.
- Vermersch AI, Rivaud S, Vidailhet M, et al. Sequences of memory-guided saccades in Parkinson's disease. Ann Neurol. 1994; 35(4): 487–490.
- Rascol O, Clanet M, Montastruc JL, et al. Abnormal ocular movements in Parkinson's disease. Evidence for involvement of dopaminergic systems. Brain. 1989; 112 ( Pt 5): 1193–1214.
- Michell AW, Xu Z, Fritz D, et al. Saccadic latency distributions in Parkinson's disease and the effects of L-dopa. Exp Brain Res. 2006; 174(1): 7–18.
- Hood AJ, Amador SC, Cain AE, et al. Levodopa slows prosaccades and improves antisaccades: an eye movement study in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2007; 78(6): 565–570.
- Yugeta A, Terao Y, Fukuda H, et al. Effects of levodopa on saccade performance in Parkinson’s disease. Mov Disord. 2008; 23(Suppl. 1): S296.
- Dec-Ćwiek M, Tutaj M, Gracies JM, et al. Opposite effects of l-dopa and DBS-STN on saccadic eye movements in advanced Parkinson's disease. Neurol Neurochir Pol. 2017; 51(5): 354–360.
- Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990; 13(7): 266–271.
- Terao Y, Fukuda H, Ugawa Y, et al. New perspectives on the pathophysiology of Parkinson's disease as assessed by saccade performance: a clinical review. Clin Neurophysiol. 2013; 124(8): 1491–1506.
- Deuschl G, Schade-Brittinger C, Krack P, et al. German Parkinson Study Group, Neurostimulation Section. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med. 2006; 355(9): 896–908.
- Weaver FM, Follett K, Stern M, et al. CSP 468 Study Group. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA. 2009; 301(1): 63–73.
- Williams A, Gill S, Varma T, et al. PD SURG Collaborative Group. 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. 2010; 9(6): 581–591.
- Schuepbach WMM, Rau J, Knudsen K, et al. EARLYSTIM Study Group. Neurostimulation for Parkinson's disease with early motor complications. N Engl J Med. 2013; 368(7): 610–622.
- Movement Disorder Society Task Force on Rating Scales for Parkinson's Disease. The Unified Parkinson's Disease Rating Scale (UPDRS): status and recommendations. Mov Disord. 2003; 18(7): 738–750.
- Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry. 1988; 51(6): 745–752.
- Defer GL, Widner H, Marié RM, et al. Core assessment program for surgical interventional therapies in Parkinson's disease (CAPSIT-PD). Mov Disord. 1999; 14(4): 572–584.
- Douglas Bates, Martin Maechler, Ben Bolker, Steve Walker . Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software. 2015; 67(1): 1–48.
- Lenth R. Least-Squares Means: TheRPackagelsmeans. Journal of Statistical Software. 2016; 69(1).
- Hirshler YK, Polat U, Biegon A. Intracranial electrode implantation produces regional neuroinflammation and memory deficits in rats. Exp Neurol. 2010; 222(1): 42–50.
- Orlowski D, Michalis A, Glud AN, et al. Brain Tissue Reaction to Deep Brain Stimulation-A Longitudinal Study of DBS in the Goettingen Minipig. Neuromodulation. 2017; 20(5): 417–423.
- Colangelo AM, Alberghina L, Papa M. Astrogliosis as a therapeutic target for neurodegenerative diseases. Neurosci Lett. 2014; 565: 59–64.
