Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T03:47:31.143Z Has data issue: false hasContentIssue false

Psychiatric morbidity in patients with Parkinson’s disease following bilateral subthalamic deep brain stimulation: literature review

Published online by Cambridge University Press:  24 June 2014

Linton J. Meagher*
Affiliation:
Department of Academic Psychiatry, Royal North Shore Hospital, Sydney, Australia
Ralf Ilchef
Affiliation:
Department of Academic Psychiatry, Royal North Shore Hospital, Sydney, Australia
Paul Silberstein
Affiliation:
Department of Neurology, Royal North Shore Hospital, Sydney, Australia
Raymond J. Cook
Affiliation:
Department of Neurosurgery, Royal North Shore Hospital, Sydney, Australia
Daniel Wasson
Affiliation:
North Shore Radiology and Nuclear Medicine, North Shore Private Hospital, Sydney, Australia
Gin S. Malhi
Affiliation:
Department of Academic Psychiatry, Royal North Shore Hospital, Sydney, Australia
*
Dr Linton J. Meagher, Department of Academic Psychiatry, Building 36, Level 5, Royal North Shore Hospital, St Leonards, Sydney, NSW 2065, Australia. Tel: +61 2 99267111; Fax: +61 2 99267730; E-mail: lmeagher@nsccahs.health.nsw.gov.au

Abstract

Objective:

To provide a comprehensive review and evaluation of the literature pertaining to the psychiatric sequelae of deep brain stimulation (DBS) of the subthalamic nucleus (STN) in patients with Parkinson’s disease (PD).

Methods:

A structured search of the EMBASE, PsychINFO and MEDLINE databases was performed on articles published since the first use of STN DBS in 1993 for PD until March 2007. Non-human studies were excluded, along with studies reporting on unilateral DBS and studies reporting on the use of STN DBS for indications other than idiopathic PD. Ninety-seven articles were selected for inclusion in the review.

Results:

Patients with advanced PD have a high rate of psychiatric morbidity. STN DBS has been shown to be an effective treatment for the control of motor symptoms in advanced PD. Neurobehavioural side-effects are, however, relatively common following STN DBS. Side-effects include impaired executive function and verbal fluency, depression, hypomania, apathy, postoperative delirium, anxiety disorders and psychotic symptoms, especially hallucinations. The alteration in dopaminergic medication following surgery as well as the direct effect of STN stimulation both appear to contribute to the short-term and long-term postoperative psychiatric complications. Methodological issues that limit the applicability of the current literature in this field are highlighted.

Conclusions:

STN DBS is an effective treatment for the motor symptoms of advanced PD. However, further research is needed to assess the extent to which STN DBS contributes to or exacerbates psychiatric morbidity over and above that associated with advanced PD. Careful neuropsychiatric evaluation and monitoring are required in this patient group.

Type
Review article
Copyright
Copyright © 2008 Blackwell Munksgaard

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Pollak, P, Benabid, AL, Gross, Cet al. Effects of the stimulation of the subthalamic nucleus in Parkinson’s disease. Rev Neurol 1993;149:175176. Google Scholar
Krack, P, Batir, A, Van Blercom, Net al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 2003;349:19251934. CrossRefGoogle ScholarPubMed
Rodriguez-Oroz, MC, Obeso, JA, Lang, AEet al. Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 2005;128:22402249. CrossRefGoogle ScholarPubMed
Kleiner-Fisman, G, Herzog, J, Fisman, DNet al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord 2006;21(Suppl. 14):S290S304. CrossRefGoogle ScholarPubMed
Hilker, R, Portman, AT, Voges, Jet al. Disease progression continues in patients with advanced Parkinson’s disease and effective subthalamic nucleus stimulation. J Neurol Neurosurg Psychiatry 2005;76:1217. CrossRefGoogle ScholarPubMed
Pahwa, R, Factor, SA, Lyons, KEet al. Practice parameter: treatment of Parkinson disease with motor fluctuations and dyskinesia (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2006;66:983995. CrossRefGoogle Scholar
Yelnik, J. Functional anatomy of the basal ganglia. Mov Disord 2002;17(Suppl. 3):S15S21. CrossRefGoogle ScholarPubMed
Parent, A, Hazrati, LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 1995;20:128154. CrossRefGoogle ScholarPubMed
DeLong, MR, Crutcher, MD, Georgopoulos, AP. Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol 1985;53:530543. Google ScholarPubMed
Wichmann, T, Bergman, H, DeLong, MR. The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 1994;72:494506. Google ScholarPubMed
Hartmann-von, Monakow, Akert, K, Künzle, H. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp Brain Res 1978;33:395403. Google Scholar
Woolf, NJ, Butcher, LL. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 1986;16:603637. CrossRefGoogle ScholarPubMed
Sadikot, AF, Parent, A, Smith, Y, Bolam, JP. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J Comp Neurol 1992;320:228242. CrossRefGoogle ScholarPubMed
Mori, S, Takino, T, Yamada, H, Sano, Y. Immunohistochemical demonstration of serotonin nerve fibers in the subthalamic nucleus of the rat, cat and monkey. Neurosci Lett 1985;62:305309. CrossRefGoogle ScholarPubMed
Temel, Y, Blokland, A, Steinbusch, HW, Visser-Vandewalle, V. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 2005;76:393413. CrossRefGoogle ScholarPubMed
Perlmutter, JS, Mink, JW. Deep brain stimulation. Ann Rev Neurosci 2006;29:229257. CrossRefGoogle ScholarPubMed
McIntyre, CC, Grill, WM, Sherman, DL, Thakor, NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol 2004;91:14571469. CrossRefGoogle Scholar
Hashimoto, T, Elder, CM, Okun, MS, Patrick, SK, Vitek, JL. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 2003;23:19161923. Google ScholarPubMed
Vitek, JL. Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 2002;17(Suppl. 3):S69S72. CrossRefGoogle ScholarPubMed
Giovannoni, G, O’Sullivan, JD, Turner, K, Manson, AJ, Lees, AJL. Hedonistic homeostatic dysregulation in patients with Parkinson’s disease on dopamine replacement therapies. J Neurol Neurosurg Psychiatry 2000;68:423428. CrossRefGoogle ScholarPubMed
Brooks, DJ, Piccini, P. Imaging in Parkinson’s disease: the role of monoamines in behaviour. Biol Psychiatry 2006;59:908918. CrossRefGoogle Scholar
Dujardin, K, Blairy, S, Defebvre, Let al. Subthalamic nucleus stimulation induces deficits in decoding emotional facial expressions in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2004;75:202208. Google ScholarPubMed
Kopell, BH, Greenberg, B, Rezai, AR. Deep brain stimulation for psychiatric disorders. J Clin Neurophysiol 2004;21:5167. CrossRefGoogle ScholarPubMed
Anderson, KE, Mullins, J. Behavioral changes associated with deep brain stimulation surgery for Parkinson’s disease. Curr Neurol Neurosci Rep 2003;3:306313. CrossRefGoogle ScholarPubMed
Mallet, L, Mesnage, V, Houeto, JLet al. Compulsions, Parkinson’s disease, and stimulation. Lancet 2002;360:13021304. CrossRefGoogle ScholarPubMed
Malhi, GS, Berk, M. Does dopamine dysfunction drive depression? Acta Psychiatr Scand 2007;433:116124. CrossRefGoogle Scholar
Menza, MA, Sage, J, Marshall, Eet al. Mood changes and ‘on-off’ phenomena in Parkinson’s disease. Mov Disord 1990;5:148151. CrossRefGoogle ScholarPubMed
Maricle, RA, Nutt, JG, Valentine, RJ, Carter, JH. Dose-response relationship of levodopa with mood and anxiety in fluctuating Parkinson’s disease: a double blind, placebo-controlled study. Neurology 1995;45:17571760. CrossRefGoogle ScholarPubMed
Ferreri, F, Agbokou, C, Gauthier, S. Recognition and management of neuropsychiatric complications in Parkinson’s disease. CMAJ 2006;175:15451552. CrossRefGoogle ScholarPubMed
Lagopoulos, J, Malhi, GS, Ivanovski, B, Cahill, CM, Morris, JGL. A matter of motion or an emotional matter? Management of depression in Parkinson’s disease. Expert Rev Neurother 2005;6:803810. CrossRefGoogle Scholar
Aarsland, D, Larsen, JP, Lim, NGet al. Range of neuropsychiatric disturbances in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1999;67:492496. CrossRefGoogle ScholarPubMed
Woods, SP, Fields, JA, Troster, AI. Neuropsychological sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a critical review. Neuropsychol Rev 2002;12:111126. CrossRefGoogle ScholarPubMed
Saint-Cyr, JA, Albanese, A. STN DBS in PD: selection criteria for surgery should include cognitive and psychiatric factors. Neurology 2006;66:17991800. CrossRefGoogle ScholarPubMed
Temel, Y, Kessels, A, Tan, S, Topdag, A, Boon, P, Visser-Vandewalle, V. Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat Disord 2006;12:265272. CrossRefGoogle ScholarPubMed
Benabid, AL, Chabardes, S, Seigneuret, E. Deep-brain stimulation in Parkinson’s disease: long-term efficacy and safety – what happened this year? Curr Opin Neurol 2005;18:623630. CrossRefGoogle ScholarPubMed
Smeding, HMM, Speelman, JD, Koning-Haanstra, Met al. Neuropsychological effects of bilateral STN stimulation in Parkinson disease: a controlled study. Neurology 2006;66:18301836. CrossRefGoogle ScholarPubMed
Morrison, CE, Borod, JC, Perrine, Ket al. Neuropsychological functioning following bilateral subthalamic nucleus stimulation in Parkinson’s disease. Arch Clin Neuropsychol 2004;19:165181. CrossRefGoogle ScholarPubMed
Castelli, L, Perozzo, P, Zibetti, Met al. Chronic deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: effects on cognition, mood, anxiety and personality traits. Eur Neurol 2006;55:136144. CrossRefGoogle ScholarPubMed
Funkiewiez, A, Ardouin, C, Caputo, Eet al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2004;75:834839. CrossRefGoogle ScholarPubMed
De Gaspari, D, Siri, C, Landi, Aet al. Clinical and neuropsychological follow up at 12 months in patients with complicated Parkinson’s disease treated with subcutaneous apomorphine infusion or deep brain stimulation of the subthalamic nucleus. J Neurol Neurosurg Psychiatry 2006;77:450453. CrossRefGoogle ScholarPubMed
Kleiner-Fisman, G, Fisman, DN, Sime, E, Saint-Cyr, JA, Lozano, AM, Lang, AE. Long-term follow up of bilateral deep brain stimulation of the subthalamic nucleus in patients with advanced Parkinson disease. J Neurosurg 2003;99:489495. CrossRefGoogle ScholarPubMed
Saint-Cyr, JA, Trepanier, LL, Kumar, Ret al. Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain 2000;123:20912108. CrossRefGoogle ScholarPubMed
Witt, K, Pulkowski, U, Herzog, Jet al. Deep brain stimulation of the subthalamic nucleus improves cognitive flexibility but impairs response inhibition in Parkinson disease. Arch Neurol 2004;61:697700. CrossRefGoogle ScholarPubMed
Funkiewiez, A, Ardouin, C, Cools, Ret al. Effects of levodopa and subthalamic nucleus stimulation on cognitive and affective functioning in Parkinson’s disease. Mov Disord 2006;21:16561662. CrossRefGoogle ScholarPubMed
Schroeder, U, Kuehler, A, Haslinger, Bet al. Subthalamic nucleus stimulation affects striato-anterior cingulate cortex circuit in a response conflict task: a PET study. Brain 2002;125:19952004. CrossRefGoogle Scholar
Gaudreau, JD, Gagnon, P. Psychotogenic drugs and delirium pathogenesis: the central role of the thalamus. Med Hypotheses 2005;64:471475. CrossRefGoogle ScholarPubMed
Young, J, Inouye, SK. Delirium in older people. BMJ 2007;334:842846. CrossRefGoogle ScholarPubMed
Pandharipande, P, Ely, EW. Sedative and analgesic medications: risk factors for delirium and sleep disturbances in the critically ill. Crit Care Clin 2006;22:313327. CrossRefGoogle ScholarPubMed
White, S, Calver, BL, Newsway, Vet al. Enzymes of drug metabolism during delirium. Age Ageing 2005;34:603608. CrossRefGoogle ScholarPubMed
Caeiro, L, Ferro, JM, Claro, MI, Coelho, J, Albuquerque, R, Figuera, ML. Delirium in acute stroke: a preliminary study of the role of anticholinergic medications. Eur J Neurol 2004;11:699704. CrossRefGoogle ScholarPubMed
Krack, P, Pollak, P, Limousin, P, Hoffmann, D, Benazzouz, A, Benabid, AL. Inhibition of levodopa effects by internal pallidal stimulation. Mov Disord 1998;13:648652. CrossRefGoogle ScholarPubMed
Witt, K, Daniels, C, Herzog, Jet al. Differential effects of L-dopa and subthalamic stimulation on depressive symptoms and hedonic tone in Parkinson’s disease. J Neuropsychiatry Clin Neurosci 2006;18:397401. CrossRefGoogle Scholar
Voon, V, Saint-Cyr, J, Lozano, AM, Moro, E, Poon, YY, Lang, AE. Psychiatric symptoms in patients with Parkinson disease presenting for deep brain stimulation surgery. J Neurosurg 2005;103:246251. CrossRefGoogle Scholar
Berney, A, Vingerhoets, F, Perrin, Aet al. Effect on mood of subthalamic DBS for Parkinson’s disease: a consecutive series of 24 patients. Neurology 2002;59:14271429. CrossRefGoogle Scholar
Okun, MS, Green, J, Saben, R, Gross, R, Foote, KD, Vitek, JL. Mood changes with deep brain stimulation of STN and GPi: results of a pilot study. J Neurol Neurosurg Psychiatry 2003;74:15841586. CrossRefGoogle ScholarPubMed
Deuschl, G, Schade-Brittinger, C, Krack, Pet al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 2006;355:896908. CrossRefGoogle ScholarPubMed
Voon, V, Kubu, C, Krack, P, Houeto, JL, Troster, AI. Deep brain stimulation: neuropsychological and neuropsychiatric issues. Mov Disord 2006;21(Suppl. 14):S305S327. CrossRefGoogle ScholarPubMed
Chou, KL, Hurtig, HI, Jaggi, JL, Baltuch, GH, Pelchat, RJ, Weintraub, D. Electroconvulsive therapy for depression in a Parkinson’s disease patient with bilateral subthalamic nucleus deep brain stimulators. Parkinsonism Relat Disord 2005;11:4036. CrossRefGoogle Scholar
Mayberg, HS, Lozano, AM. Penfield revisited? Understanding and modifying behavior by deep brain stimulation for PD. Neurology 2002;59:12981299. CrossRefGoogle ScholarPubMed
Jimenez, F, Velasco, F, Salin-Pascual, Ret al. A patient with a resistant major depression disorder treated with deep brain stimulation in the inferior thalamic peduncle. Neurosurgery 2005;57:585593. CrossRefGoogle ScholarPubMed
Mayberg, HS, Lozano, AM, Voon, Vet al. Deep brain stimulation for treatment-resistant depression. Neuron 2005;45:651660. CrossRefGoogle ScholarPubMed
Voon, V, Krack, P, Lang, Aet al. Frequency and risk factors for suicidal outcomes following subthalamic deep brain stimulation for Parkinson’s disease: a multicenter retrospective survey. Neurology 2006;66(Suppl. 2):195. Google Scholar
Burkhard, PR, Vingerhoets, FJ, Berney, Aet al. Suicide after successful deep brain stimulation for movement disorders. Neurology 2004;63:2170. Google Scholar
Inskip, H, Harris, C, Barraclough, B. Lifetime risk of suicide for affective disorder, alcoholism and schizophrenia. Br J Psychiatry 1998;172:3537. CrossRefGoogle Scholar
Myslobodsky, M, Lalonde, FM, Hicks, L. Are patients with Parkinson’s disease suicidal? J Geriatr Psychiatry Neurol 2001;14:120124. CrossRefGoogle ScholarPubMed
Balash, Y, Merims, D, Giladi, N. Suicidal thoughts in patients with Parkinson’s disease treated by deep brain stimulation of the subthalamic nuclei: two case reports and review of the literature. Acta Neuropsychiatr 2007;19:208210. CrossRefGoogle ScholarPubMed
Mandat, TS, Hurwitz, T, Honey, CR. Hypomania as an adverse effect of subthalamic nucleus stimulation: report of two cases. Acta Neurochir 2006;148:895897. CrossRefGoogle ScholarPubMed
Funkiewiez, A, Ardouin, C, Krack, Pet al. Acute psychotropic effects of bilateral subthalamic nucleus stimulation and levodopa in Parkinson’s disease. Mov Disord 2003;18:524530. CrossRefGoogle ScholarPubMed
Houeto, JL, Mesnage, V, Mallet, Let al. Behavioural disorders, Parkinson’s disease and subthalamic stimulation. J Neurol Neurosurg Psychiatry 2002;72:701707. CrossRefGoogle ScholarPubMed
Romito, LM, Raja, M, Daniele, Aet al. Transient mania with hypersexuality after surgery for high frequency stimulation of the subthalamic nucleus in Parkinson’s disease. Mov Disord 2002;17:13711374. CrossRefGoogle ScholarPubMed
Herzog, J, Reiff, J, Krack, Pet al. Manic episode with psychotic symptoms induced by subthalamic nucleus stimulation in a patient with Parkinson’s disease. Mov Disord 2003;18:13821384. CrossRefGoogle Scholar
Lawrence, AD, Evans, AH, Lees, AJ. Compulsive use of dopamine replacement therapy in Parkinson’s disease: reward systems gone awry? Lancet Neurol 2003;2:595604. CrossRefGoogle ScholarPubMed
Ulla, M, Thobois, S, Lemaire, JJet al. Manic behaviour induced by deep-brain stimulation in Parkinson’s disease: evidence of substantia nigra implication? J Neurol Neurosurg Psychiatry 2006;77:13631366. CrossRefGoogle ScholarPubMed
Daniele, A, Albanese, A, Contarino, MFet al. Cognitive and behavioural effects of chronic stimulation of the subthalamic nucleus in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 2003;74:175182. CrossRefGoogle ScholarPubMed
Schupbach, WM, Maltete, D, Houeto, JLet al. Neurosurgery at an earlier stage of Parkinson disease: a randomized, controlled trial. Neurology 2007;68:267271. CrossRefGoogle Scholar
Ardouin, C, Voon, V, Worbe, Yet al. Pathological gambling in Parkinson’s disease improves on chronic subthalamic nucleus stimulation. Mov Disord 2006;22:19411946. CrossRefGoogle Scholar
Schupbach, M, Gargiulo, M, Welter, MLet al. Neurosurgery in Parkinson disease: a distressed mind in a repaired body? Neurology 2006;66:18111816. CrossRefGoogle Scholar
ClinicalTrials.gov [database on the internet]. U.S. National Institutes of Health. The Mood/Cognitive Effects of STN vs. GPi Deep Brain Stimulation in Parkinson’s Disease [updated December 2007; cited 21 December 2007]. Available from: http://clinicaltrials.gov/ct2/show/NCT00360009. Google Scholar
Bezerra, ML, Martinez, JV, Nasser, JA. Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med 1999;341:1003. Google ScholarPubMed
Vitek, JL, Bakay, RA, Freeman, Aet al. Randomized trial of pallidotomy versus medical therapy for Parkinson’s disease. Ann Neurol 2003;53:558569. CrossRefGoogle ScholarPubMed
Haldane, M, Frangou, S. Functional neuroimaging studies in mood disorders. Acta Neuropsychiatr 2006;18:8899. CrossRefGoogle ScholarPubMed
Lagopoulos, J, Malhi, GS, Ivanovski, Bet al. Cerebrovascular autoregulation as a neuroimaging tool. Acta Neuropsychiatr 2006;18:100104. CrossRefGoogle ScholarPubMed
Malhi, GS, Lagopoulos, J. Cutting edge neuropsychiatry. Acta Neuropsychiatr 2007;19:380381. CrossRefGoogle Scholar
Williams, LJ, Jacka, FN, Pasco, JA, Dodd, S, Berk, M. Depression and pain: an overview. Acta Neuropsychiatr 2006;18:7987. CrossRefGoogle ScholarPubMed