The effect of deep brain stimulation on the non-motor symptoms of Parkinson's disease: a critical review of the current evidence

Mónica M Kurtis, Thadshani Rajah, Luisa F Delgado, Haidar S Dafsari, Mónica M Kurtis, Thadshani Rajah, Luisa F Delgado, Haidar S Dafsari

Abstract

The benefit of deep brain stimulation (DBS) in controlling the motor symptoms of Parkinson's disease is well established, however, the impact on the non-motor symptoms (NMS) remains to be elucidated, although the growing investigative efforts are promising. This article reviews the reported data and considers the level of evidence available with regard to the effect of DBS on NMS total burden and on the cognitive, neuropsychiatric, sleep, pain, dysautonomic, and weight domains. Multiple case series suggest that DBS improves the burden of NMS by reducing prevalence, intensity, and non-motor fluctuations. There is level I evidence on the effect of DBS on cognition and mood. Slight cognitive decline has been reported in most class I studies, although the functional effect is probably minimal. Two randomized prospective studies reported no change in depression while improvement of anxiety has been reported by a class I trial. Prospective cohort studies point to improvement of hyperdopaminergic behaviors, such as impulse control disorders, while others report that hypodopaminergic states, like apathy, can appear after DBS. There is only class III evidence supporting the benefit of DBS on other NMS such as nocturnal sleep, pain, dysautonomia (urinary, gastrointestinal, cardiovascular, and sweating), and weight loss. Although preliminary results are promising, randomized prospectively controlled trials with NMS as primary end points are necessary to further explore the effect of DBS on these often invalidating symptoms and offer conclusions about efficacy.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Deuschl, G. et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N. Engl. J. Med. 355, 896–908 (2006).
    1. Weaver, F. M. et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 301, 63–73 (2009).
    1. Follett, K. A. et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N. Engl. J. Med. 362, 2077–2091 (2010).
    1. Chaudhuri, K. R. & Schapira, A. H. V. Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 8, 464–474 (2009).
    1. Martinez-Martin P., Rodriguez-Blazquez C., Kurtis M. M., Chaudhuri K. R., NMSS Validation Group. The impact of non-motor symptoms on health-related quality of life of patients with Parkinson’s disease. Mov. Disord. 26: 399–406 (2011).
    1. Klingelhoefer, L., Samuel, M., Chaudhuri, K. R. & Ashkan, K. An update of the impact of deep brain stimulation on non motor symptoms in Parkinson’s disease. J. Parkinsons Dis. 4, 289–300 (2014).
    1. Wang, X.-H. et al. Target selection recommendations based on impact of deep brain stimulation surgeries on nonmotor symptoms of Parkinson’s disease. Chin. Med. J. (Engl) 128, 3371–3380 (2015).
    1. Kim, H., Jeon, B. S. & Paek, S. H. Nonmotor symptoms and subthalamic deep brain stimulation in Parkinson’s disease. Mov. Disord. 8, 83–91 (2015).
    1. Lang, A. E. & Lees, A. Management of Parkinson’s disease: an evidence-based review. Mov. Disord. 17, S1–S6 (2002).
    1. Adler, C. H. & Beach, T. G. Neuropathological basis of nonmotor manifestations of Parkinson’s disease. Mov. Disord. 31, 1114–1119 (2016).
    1. Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381 (1986).
    1. Tremblay, L., Worbe, Y., Thobois, S., Sgambato-Faure, V. & Féger, J. Selective dysfunction of basal ganglia subterritories: from movement to behavioral disorders. Mov. Disord. 30, 1155–1170 (2015).
    1. Obeso, J. A. et al. Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov. Disord. 23, 548–559 (2008).
    1. Volkmann, J., Daniels, C. & Witt, K. Neuropsychiatric effects of subthalamic neurostimulation in Parkinson disease. Nat. Rev. Neurol. 6, 487–498 (2010).
    1. Castrioto, A., Lhommée, E., Moro, E. & Krack, P. Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol. 13, 287–305 (2014).
    1. Alessandro, S. et al. Non-motor functions in parkinsonian patients implanted in the pedunculopontine nucleus: focus on sleep and cognitive domains. J. Neurol. Sci. 289, 44–48 (2010).
    1. Trachani, E. et al. Effects of subthalamic nucleus deep brain stimulation on sweating function in Parkinson’s disease. Clin. Neurol. Neurosurg. 112, 213–217 (2010).
    1. Herzog, J. et al. Improved sensory gating of urinary bladder afferents in Parkinson’s Disease following subthalamic stimulation. Brain 131, 132–145 (2008).
    1. Chaudhuri, K. R. et al. International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson’s disease: the NMSQuest study. Mov. Disord. 21, 916–923 (2006).
    1. Chaudhuri, K. R. et al. The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov. Disord. 22, 1901–1911 (2007).
    1. Reich, M. M. et al. Changes in the non-motor symptom scale in Parkinson’s disease after deep brain stimulation. Basal Ganglia 1, 131–133 (2011).
    1. Nazzaro, J. M., Pahwa, R. & Lyons, K. E. The impact of bilateral subthalamic stimulation on non-motor symptoms of Parkinson’s disease. Parkinsonism Relat. Disord. 17, 606–609 (2011).
    1. Dafsari, H. S. et al. Beneficial effects of bilateral subthalamic stimulation on non-motor symptoms in Parkinson’s disease. Brain Stimul. 9, 78–85 (2016).
    1. Wolz, M. et al. Immediate effects of deep brain stimulation of the subthalamic nucleus on nonmotor symptoms in Parkinson’s disease. Park. Relat. Disord. 18, 994–997 (2012).
    1. Storch, A. et al. Nonmotor fluctuations in Parkinson disease: severity and correlation with motor complications. Neurology 80, 800–809 (2013).
    1. Witjas, T. et al. Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson’s disease. Mov. Disord. 22, 1729–1734 (2007).
    1. Ortega-Cubero, S. et al. Effect of deep brain stimulation of the subthalamic nucleus on non-motor fluctuations in Parkinson’s disease: two-years' follow-up. Parkinsonism Relat. Disord. 19, 543–547 (2013).
    1. Hely, M. A., Reid, W. G. J., Adena, M. A., Halliday, G. M. & Morris, J. G. L. The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov. Disord. 23, 837–844 (2008).
    1. Parsons, T. D., Rogers, S. A., Braaten, A. J., Woods, S. P. & Tröster, A. I. Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol. 5, 578–588 (2006).
    1. Witt, K. et al. Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol. 7, 605–614 (2008).
    1. Appleby, B. S., Duggan, P. S., Regenberg, A. & Rabins, P. V. Psychiatric and neuropsychiatric adverse events associated with deep brain stimulation: a meta-analysis of ten years’ experience. Mov. Disord. 22, 1722–1728 (2007).
    1. Williams, A. et al. 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, 581–591 (2010).
    1. Pillon, B. et al. Neuropsychological changes between ‘off’ and ‘on’ STN or GPi stimulation in Parkinson’s disease. Neurology 55, 411–418 (2000).
    1. Krack, P. et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N. Engl. J. Med. 349, 1925–1934 (2003).
    1. Daniele, A. et al. Cognitive and behavioural effects of chronic stimulation of the subthalamic nucleus in patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 74, 175–182 (2003).
    1. Funkiewiez, A. et al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 75, 834–839 (2004).
    1. Castelli, L. et al. Chronic deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: effects on cognition, mood, anxiety and personality traits. Eur. Neurol. 55, 136–144 (2006).
    1. Rizzone, M. G. et al. 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, 376–381 (2014).
    1. Odekerken, V. J. et al. Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. Lancet Neurol. 12, 37–44 (2013).
    1. Witt, K. et al. Relation of lead trajectory and electrode position to neuropsychological outcomes of subthalamic neurostimulation in Parkinson’s disease: results from a randomized trial. Brain 136, 2109–2119 (2013).
    1. McDonald, L. M., Page, D., Wilkinson, L. & Jahanshahi, M. Deep brain stimulation of the subthalamic nucleus improves sense of well-being in Parkinson’s disease. Mov. Disord. 27, 372–378 (2012).
    1. Kaiser, I., Kryspin-Exner, I., Brücke, T., Volc, D. & Alesch, F. Long-term effects of STN DBS on mood: psychosocial profiles remain stable in a 3-year follow-up. BMC Neurol. 8, 43 (2008).
    1. Lhommée, E. et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain 135, 1463–1477 (2012).
    1. Rossi, P. J., Gunduz, A. & Okun, M. S. The subthalamic nucleus, limbic function, and impulse control. Neuropsychol. Rev. 25, 398–410 (2015).
    1. Ardouin, C. et al. Pathological gambling in Parkinson’s disease improves on chronic subthalamic nucleus stimulation. Mov. Disord. 21, 1941–1946 (2006).
    1. Shotbolt, P. et al. Relationships between deep brain stimulation and impulse control disorders in Parkinson’s disease, with a literature review. Parkinsonism Relat. Disord. 18, 10–16 (2012).
    1. Demetriades, P., Rickards, H. & Cavanna, A. E. Impulse control disorders following deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: clinical aspects. Parkinsons Dis. 2011, 658415 (2011).
    1. Moum, S. J. et al. Effects of STN and GPi deep brain stimulation on impulse control disorders and dopamine dysregulation syndrome. PLoS One 7, e29768 (2012).
    1. Kim, Y. E. et al. Impulse control and related behaviors after bilateral subthalamic stimulation in patients with Parkinson’s disease. J. Clin. Neurosci. 20, 964–969 (2013).
    1. Hack, N. et al. Impulsive and compulsive behaviors in Parkinson Study Group (PSG) centers performing deep brain stimulation surgery. J. Parkinsons Dis. 4, 591–598 (2014).
    1. Thobois, S. et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain 133, 1111–1127 (2010).
    1. Pagonabarraga, J., Kulisevsky, J., Strafella, A. P. & Krack, P. Apathy in Parkinson’s disease: Clinical features, neural substrates, diagnosis, and treatment. Lancet Neurol. 14, 518–531 (2015).
    1. Higuchi, M. et al. Predictors of the emergence of apathy after bilateral stimulation of the subthalamic nucleus in patients with Parkinson’s disease. Neuromodulation 18, 113–117 (2015).
    1. Voon, V. et al. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain 131, 2720–2728 (2008).
    1. Weintraub, D. et al. Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson’s disease: results from a randomised, controlled trial. J. Neurol. Neurosurg. Psychiatry 84, 1113–1118 (2013).
    1. Chaudhuri, K. R. & Martinez-Martin, P. Clinical assessment of nocturnal disability in Parkinson’s disease: the Parkinson's Disease Sleep Scale. Neurology 63, S17–S20 (2004).
    1. Chaudhuri, K. R. & Healy, D. G. Schapira AHV. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 5, 235–245 (2006).
    1. Iranzo, A., Valldeoriola, F., Santamaría, J., Tolosa, E. & Rumià, J. Sleep symptoms and polysomnographic architecture in advanced Parkinson’s disease after chronic bilateral subthalamic stimulation. J. Neurol. Neurosurg. Psychiatry 72, 661–664 (2002).
    1. Hjort, N., Østergaard, K. & Dupont, E. Improvement of sleep quality in patients with advanced Parkinson’s disease treated with deep brain stimulation of the subthalamic nucleus. Mov. Disord. 19, 196–199 (2004).
    1. Amara, A. W. et al. Unilateral subthalamic nucleus deep brain stimulation improves sleep quality in Parkinson’s disease. Parkinsonism Relat. Disord. 18, 63–68 (2012).
    1. Lyons, K. E. & Pahwa, R. Effects of bilateral subthalamic nucleus stimulation on sleep, daytime sleepiness, and early morning dystonia in patients with Parkinson disease. J. Neurosurg. 104, 502–505 (2006).
    1. Loher, T. J., Burgunder, J.-M., Weber, S., Sommerhalder, R. & Krauss, J. K. Effect of chronic pallidal deep brain stimulation on off period dystonia and sensory symptoms in advanced Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 73, 395–399 (2002).
    1. Kim, H.-J., Jeon, B. S., Lee, J.-Y., Paek, S. H. & Kim, D. G. The benefit of subthalamic deep brain stimulation for pain in Parkinson disease: a 2-year follow-up study. Neurosurgery 70, 18–23 (2012).
    1. Cury, R. G. et al. Effects of deep brain stimulation on pain and other nonmotor symptoms in Parkinson disease. Neurology 83, 1403–1409 (2014).
    1. Gierthmühlen, J. et al. Influence of deep brain stimulation and levodopa on sensory signs in Parkinson’s disease. Mov. Disord. 25, 1195–1202 (2010).
    1. Chaudhuri, K. R. et al. King’s Parkinson's disease pain scale, the first scale for pain in PD: an international validation. Mov. Disord. 30, 1623–1631 (2015).
    1. Seif, C. et al. Effect of subthalamic deep brain stimulation on the function of the urinary bladder. Ann. Neurol. 55, 118–120 (2004).
    1. Herzog, J. et al. Subthalamic stimulation modulates cortical control of urinary bladder in Parkinson’s disease. Brain 129, 3366–3375 (2006).
    1. Winge, K. et al. Lower urinary tract symptoms and bladder control in advanced Parkinson’s disease: effects of deep brain stimulation in the subthalamic nucleus. Mov. Disord. 22, 220–225 (2007).
    1. Arai, E. et al. Subthalamic deep brain stimulation can improve gastric emptying in Parkinson’s disease. Brain 135, 1478–1485 (2012).
    1. Zibetti, M. et al. Motor and nonmotor symptom follow-up in parkinsonian patients after deep brain stimulation of the subthalamic nucleus. Eur. Neurol. 58, 218–223 (2007).
    1. Troche, M. S., Brandimore, A. E., Foote, K. D. & Okun, M. S. Swallowing and deep brain stimulation in Parkinson’s disease: a systematic review. Parkinsonism Relat. Disord. 19, 783–788 (2013).
    1. Derrey, S. et al. Impact of deep brain stimulation on pharyngo-esophageal motility: a randomized cross-over study. Neurogastroenterol. Motil. 27, 1214–1222 (2015).
    1. Suttrup, I. & Warnecke, T. Dysphagia in Parkinson’s disease. Dysphagia 31, 24–32 (2016).
    1. Stemper, B. et al. Deep brain stimulation improves orthostatic regulation of patients with Parkinson disease. Neurology 67, 1781–1785 (2006).
    1. Trachani, E. et al. Heart rate variability in Parkinson’s disease unaffected by deep brain stimulation. Acta Neurol. Scand. 126, 56–61 (2012).
    1. Sumi, K. et al. Effect of subthalamic nucleus deep brain stimulation on the autonomic nervous system in Parkinson’s disease patients assessed by spectral analyses of R-R interval variability and blood pressure variability. Stereotact. Funct. Neurosurg. 90, 248–254 (2012).
    1. Hummel, T., Jahnke, U., Sommer, U., Reichmann, H. & Müller, A. Olfactory function in patients with idiopathic Parkinson’s disease: effects of deep brain stimulation in the subthalamic nucleus. J. Neural Transm. 112, 669–676 (2005).
    1. Fabbri, M. et al. Subthalamic deep brain stimulation effects on odor identification in Parkinson’s disease. Eur. J. Neurol. 22, 207–210 (2015).
    1. Guo, X. et al. Effects of bilateral deep brain stimulation of the subthalamic nucleus on olfactory function in Parkinson’s disease patients. Stereotact. Funct. Neurosurg. 86, 237–244 (2008).
    1. Chen, H., Zhang, S. M., Hernán, M. A., Willett, W. C. & Ascherio, A. Weight loss in Parkinson’s disease. Ann. Neurol. 53, 676–679 (2003).
    1. Rieu, I. et al. Body weight gain and deep brain stimulation. J. Neurol. Sci. 310, 267–270 (2011).
    1. Strowd, R. E. et al. Weight change following deep brain stimulation for movement disorders. J. Neurol. 257, 1293–1297 (2010).
    1. Strowd, R. E. et al. Association between subthalamic nucleus deep brain stimulation and weight gain: results of a case-control study. Clin. Neurol. Neurosurg. 140, 38–42 (2016).
    1. Gironell, A., Pascual-Sedano, B., Otermin, P. & Kulisevsky, J. Weight gain after functional surgery for Parkinsons disease. Neurologia 17, 310–316 (2002).
    1. Foubert-Samier, A. et al. A long-term follow-up of weight changes in subthalamic nucleus stimulated Parkinson’s disease patients. Rev. Neurol. 168, 173–176 (2012).
    1. Montaurier, C. et al. Mechanisms of body weight gain in patients with Parkinson’s disease after subthalamic stimulation. Brain 130, 1808–1818 (2007).
    1. Walker, H. C. et al. Weight changes associated with unilateral STN DBS and advanced PD. Parkinsonism Relat. Disord. 15, 709–711 (2009).
    1. Nirenberg, M. J. & Waters, C. Compulsive eating and weight gain related to dopamine agonist use. Mov. Disord. 21, 524–529 (2006).
    1. Macia, F. et al. Parkinson’s disease patients with bilateral subthalamic deep brain stimulation gain weight. Mov. Disord. 19, 206–212 (2004).
    1. Weintraub, D. et al. Validation of the questionnaire for impulsive-compulsive disorders in Parkinson’s disease. Mov. Disord. 24, 1461–1467 (2009).
    1. Sixel-Döring, F., Schweitzer, M., Mollenhauer, B. & Trenkwalder, C. Intraindividual variability of REM sleep behavior disorder in Parkinson’s disease: a comparative assessment using a new REM sleep behavior disorder severity scale (RBDSS) for clinical routine. J. Clin. Sleep Med. 7, 75–80 (2011).
    1. Okun, M. S. et al. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE trial. Ann. Neurol. 65, 586–595 (2009).
    1. Anderson, V. C., Burchiel, K. J., Hogarth, P., Favre, J. & Hammerstad, J. P. Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. Arch. Neurol. 62, 554–560 (2005).
    1. Reker, P., Dembek, T. A., Becker, J., Visser-Vandewalle, V. & Timmermann, L. Directional deep brain stimulation: a case of avoiding dysarthria with bipolar directional current steering. Parkinsonism Relat. Disord. 31, 156–158 (2016).
    1. Steigerwald, F., Müller, L., Johannes, S., Matthies, C. & Volkmann, J. Directional deep brain stimulation of the subthalamic nucleus: a pilot study using a novel neurostimulation device. Mov. Disord. 31, 1240–1243 (2016).
    1. Marras, C. & Chaudhuri, K. R. Nonmotor features of Parkinson’s disease subtypes. Mov. Disord. 31, 1095–1102 (2016).

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel