Han-Joon Kim; Beom S. Jeon; Sun Ha Paek

doi:10.14802/jmd.15010

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Review Article Nonmotor Symptoms and Subthalamic Deep Brain Stimulation in Parkinson’s Disease: Han-Joon Kim¹, Beom S. Jeon¹, Sun Ha Paek²; Journal of Movement Disorders 2015;8(2):83-91.
DOI: https://doi.org/10.14802/jmd.15010
Published online: May 31, 2015

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¹Department of Neurology, Movement Disorder Center, Neuroscience Research Institute, College of Medicine, Seoul National University, Seoul, Korea

²Department of Neurosurgery, Movement Disorder Center, Neuroscience Research Institute, College of Medicine, Seoul National University, Seoul, Korea

Corresponding author: Beom S. Jeon, MD, PhD, Department of Neurology, College of Medicine, Seoul National University, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea Tel: +82-2-2072-2876 Fax: +82-2-3672-7553 E-mail: brain@snu.ac.kr

Corresponding author: Sun Ha Paek, MD, PhD, Department of Neurosurgery, College of Medicine, Seoul National University, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea Tel: +82-2-2072-3993 Fax: +82-2-744-8459 E-mail: paeksh@snu.ac.kr

• Received: March 27, 2015 • Revised: April 18, 2015 • Accepted: April 20, 2015

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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ABSTRACT
INTRODUCTION
MECHANISM OF THE EFFECT OF STN DBS IN PD
MOOD AND BEHAVIOR
COGNITION
SLEEP
AUTONOMIC SYMPTOMS
PAIN AND SENSORY SYMPTOMS
NONMOTOR FLUCTUATIONS
CONCLUSION
Notes
REFERENCES

ABSTRACT

Subthalamic deep brain stimulation (STN DBS) is an established treatment for the motor symptoms in patients with advanced Parkinson’s disease (PD). In addition to improvements in motor symptoms, many studies have reported changes in various nonmotor symptoms (NMSs) after STN DBS in patients with PD. Psychiatric symptoms, including depression, apathy, anxiety, and impulsivity, can worsen or improve depending on the electrical stimulation parameters, the locations of the stimulating contacts within the STN, and changes in medications after surgery. Global cognitive function is not affected by STN DBS, and there is no increase in the incidence of dementia after STN DBS compared to that after medical treatment, although clinically insignificant declines in verbal fluency have been consistently reported. Pain, especially PD-related pain, improves with STN DBS. Evidence regarding the effects of STN DBS on autonomic symptoms and sleep-related problems is limited and remains conflicting. Many symptoms of nonmotor fluctuations, which are occasionally more troublesome than motor fluctuations, improve with STN DBS. Although it is clear that NMSs are not target symptoms for STN DBS, NMSs have a strong influence on the quality of life of patients with PD, and clinicians should thus be aware of these NMSs when deciding whether to perform surgery and should pay attention to changes in these symptoms after STN DBS to ensure the optimal care for patients.
Keywords: Parkinson disease; Subthalamic deep brain stimulation; Nonmotor symptoms; Basal ganglia

INTRODUCTION

Subthalamic deep brain stimulation (STN DBS) is an established treatment for the motor symptoms of patients with advanced Parkinson’s disease (PD). Because the prevalence and severity of nonmotor symptoms (NMSs) increase with the progression of motor symptoms in PD [1-3], patients for whom STN DBS is considered also have many NMSs, which are sometimes more troublesome and exert a greater influence on health related quality of life (QoL) than the motor symptoms [4,5].

Although it is clear that NMSs cannot be target symptoms for STN DBS, many studies have shown that STN DBS has beneficial effects on various NMSs in addition to eliciting improvements in motor symptoms and further improving the QoL and satisfaction with surgery [4,6-8]. In contrast, there are studies that have reported worsening of some NMSs following STN DBS [9-11]. Furthermore, in some patients, NMSs, including cognitive dysfunction and mood disorder, should be considered with motor symptoms when deciding whether to perform surgery because changes in these NMSs after surgery may have significant effects on the overall results of STN DBS.

In this regard, the authors will review the effect of STN DBS on NMSs in patients with PD and discuss its possible mechanisms.

MECHANISM OF THE EFFECT OF STN DBS IN PD

The current model of the basal ganglia (BG) indicates that the hypodopaminergic state in PD causes increased activity in the STN, which leads to increased inhibitory output from internal segment of the globus pallidus and substantia nigra pars reticulata [12]. This process results in increased inhibitory activity of the BG on the thalamic and cortical motor system, which manifests clinically as bradykinesia and rigidity. In addition to the motor system, the BG also serve as a conduit for the limbic and associative systems [12]. As in the motor system, the hypodopaminergic state of PD leads to increased inhibition from the BG onto these systems through the hyperactive STN. Dopaminergic medications and STN DBS reduce this increased activity of the STN in patients with PD, and this effect normalizes the increased inhibitory activity of the BG on the motor, limbic, and associative systems. However, when the STN becomes hypoactive due to excessive dopaminergic medications, the inhibitory activity of the BG falls below normal and patients in this state clinically present with hyperactive movement, such as that observed in levodopa-induced dyskinesias, and disinhibited behavior. Similarly, decreased activity in the STN due to STN DBS can also lead to the decreased inhibitory activity of the BG. Furthermore, because the STN is divided into sensorimotor, associative, and limbic territories that constitute the sensorimotor, associative, and limbic BG loops, respectively [13], the effects of STN DBS on motor and NMSs are determined not only by the intensity of the electrical stimulation but also by the location of the stimulating electrode within the STN. For example, if the stimulating contact is located in the ventromedial STN, the patient will experience more prominent changes in symptoms related to limbic-associative circuits, whereas contacts located in dorsolateral STN will primarily affect motor symptoms.

Not all of the NMSs in PD are related to a dopaminergic deficit in the BG. Some NMSs, including cognitive dysfunction, mood disorders, and impulse control disorders, are thought to be related to dopaminergic deficits outside the BG [14,15] or abnormalities in other neurotransmitter systems including the serotonin and norepinephrine systems [16,17] Autonomic dysfunction, including orthostatic hypotension and genitourinary dysfunction, have been related to the pathologies outside the brain, including the spinal cord and peripheral autonomic nerves [18]. STN DBS affects some of these NMSs but the mechanism has yet to be elucidated. Another mechanism by which STN DBS affects NMSs is through the reduction of dopaminergic medication after surgery. The adverse effects of dopaminergic medications, including nausea, vomiting, and dizziness, can improve after STN DBS with reductions in medication [19]. In contrast, because the beneficial extrastriatal nonmotor effects of dopaminergic medications cannot be replaced by STN DBS, some NMSs can emerge after STN DBS due to reductions in medications [20].

Depression: Depression is common in PD patients, and clinically significant depressive symptoms occur in 40–50% of patients with PD [21] and constitute one of the most important factors associated with QoL in PD. Evidence indicates that the pathophysiology of depression in PD involves dysfunction of dopaminergic and noradrenergic pathways in brain regions that include the limbic areas, whereas the role of serotoninergic dysfunction is relatively limited [22,23]. Reports about changes in depressive symptoms after STN DBS have provided conflicting results that include improvements, a lack of changes, and worsening [11,24-26]. As mentioned earlier, the direct effect of properly located STN DBS should be a mild elevation of mood [27]. However, the actual change in depressive symptoms is more likely to depend on other factors including changes in medications and the severity of preoperative depressive symptoms than on the electrical stimulation. As demonstrated in a recent systemic review, depressive symptoms typically improve in the initial months after STN DBS [28]. However, in our experience, worsening of depressive symptoms can occur in the initial months and these changes are primarily related to the reduction in dopaminergic medications and can be reversed with dopaminergic medications. Reports of longterm follow-ups after STN DBS show that depressive symptoms improve or remain unchanged compared with baseline [25,26,29].
Suicide: Much concern was been raised about mortality by suicide after STN DBS, particularly in the first postoperative year, by one retrospective case series [30]. However, a subsequent randomized controlled study found no increase in the risks of suicidal ideation or behavior after STN DBS compared with that after medical treatment, although it has been argued that this study was underpowered due to the rarity of suicide events [31]. In the literature, the rates of suicide or suicidal ideation after STN DBS have been reported to be 0.5 to 1.5% [24,30-33]. Postoperative depression, being single, and a previous history of impulse control-related behaviors (ICRB) were independent risk factors in the aforementioned case series [30], and it was recently suggested that unmet unrealistic expectations about surgical outcome may have some role [20]. Therefore, a multidisciplinary team approach that includes a psychiatrist is recommended from the stage of patient selection.
Apathy: Apathy refers to a state of diminished goal-directed speech, motor activity and emotions. The prevalence of apathy in PD varies from 17 to 70% depending on the sample population, diagnostic criteria, and evaluation tools [34]. Although apathy usually occurs in association with cognitive dysfunction and depression, some patients develop apathy in the absence of depression and dementia. Several studies have reported increases in apathy after STN DBS [10,25,35]. Evidence shows that apathy is associated with mesolimbic dopaminergic denervation, and reductions in dopaminergic medications seem to be an important cause of apathy after STN DBS [36]. Indeed, in one study, half of the patients developed apathy associated with anxiety and depression on average 4 months after STN DBS when dopaminergic medications were markedly and abruptly decreased soon after surgery [10]. Preoperative nonmotor fluctuations (NMFs) were predictors of postoperative apathy. The introduction of piribedil, a relatively selective D2/D3 dopaminergic agonist, reversed apathy in these patients [37]. Thus, in our opinion, when a patient develops apathy in the early postoperative period, which is more likely in cases that exhibit good motor improvement with STN DBS that allows for greater reductions in medication, the adjustments in medication should be considered. However, in the long term, apathy may develop as a natural progression of PD NMSs in parallel with dementia.
Mania and impulsivity: In the immediate postoperative period, a patient may develop euphoria, hyperactivity, and disinhibition. When mild and tolerable, these changes might be regarded as normal responses to improvements in motor symptoms and relief from the fear of undergoing surgery and perioperative complications. The patient and caregiver may enjoy these symptoms. The proposed mechanisms of these symptoms reduced activity about limbic STN electrical stimulation, a transient effect of microlesioning of the STN, and a persistent long-term effect of dopaminergic medications [20,38,39]. The latter two effects diminish over time, which explains the gradual spontaneous improvements in these symptoms. However, a small proportion of patients develop hypomania, mania, and pathologically impulsive behaviors in the immediate postoperative period [40-42] that necessitate interventions including the adjustment of the electrical stimulation parameters. It currently remains unknown which patients are at risk of developing these symptoms. The location of the electrode within the STN appears to have an important role. Previous reports have found that stimulation in the more ventromedial STN, which is a limbic-associative subterritory of the STN, produces hypomanic symptoms and associated changes in cortical activations [13,39].; ICRBs in PD consist of dopamine dysregulation syndrome, punding, and impulse control disorders (i.e., hypersexuality, binge eating, pathologic gambling, and pathologic shopping). The prevalences of dopamine dysregulation syndrome and impulse control disorders are approximately 3–4% and 6–14%, respectively [43]. ICRBs in PD are related to the use of dopaminergic medications and improve with reductions in these medications. Thus, it is expected that the symptoms of ICRBs will improve or disappear after STN DBS, which usually allows for significant reductions of dopaminergic medications. However, the results of studies are inconsistent; some have reported improvement, whereas others have reported no significant change or even the development of new ICRBs after STN DBS [44-47]. Notably, a history of ICRBs is a risk factor for suicide after STN DBS [30], which further supports the notion that the vulnerability of the limb-associative system and the sensitivity to changes in dopaminergic medications in a subset of patients with PD are associated with a multitude of mood and behavior symptoms.
Anxiety: Anxiety in PD consists of generalized anxiety, panic attacks, and social phobia. Anxiety usually coexists with depression and can coexist with motor fluctuations as a symptom of NMFs that responds to dopaminergic medications. Studies have shown improvements in anxiety after STN DBS [11,28]. As in depression, postoperative changes in dopaminergic medications appears to have an important role. In the long-term, anxiety appears to remain unchanged compared with baseline [28,29].

COGNITION

Cognitive dysfunction is intrinsic to PD. Dementia affects up to 80% of patients in the late stage of the disease, and detailed evaluations have revealed frontal dysfunction even in the early stage of the disease. There have been concerns about the possibility of cognitive worsening after bilateral STN DBS because the placements of the permanent stimulating electrodes itself and the insertions of the recording electrodes during surgery cause bilateral cortical and subcortical damage. Furthermore, the effects of electrical stimulation on cognitive function are still not well understood. However, although there are some reports about cognitive deterioration after STN DBS [48,49], it is generally accepted that bilateral STN DBS is safe from a cognitive perspective [20,50]. Although it is true that declines in frontal executive function, especially verbal fluency, have consistently been reported after bilateral STN DBS compared with after medical treatment, these differences are not clinically significant in most cases [11,50-52]. Many studies have shown no significant changes in global cognitive function and no increase in the incidence of dementia after bilateral STN DBS compared with those after medical treatment, and the observed cognitive worsening after bilateral STN DBS has been attributed to the natural course of the disease rather than the adverse effects of STN DBS [20,50]. In support of this conjecture, the risk factors for cognitive decline or the development of dementia after STN DBS are not different from those for the medical treatment of PD; i.e., old age, severe axial symptoms, the presence of hallucination, impaired frontal function and attention, and the presence of mild cognitive impairment at baseline [48,49,53].

The presence of dementia is regarded as a contraindication for STN DBS without supportive data [54] likely due to the following reasons: 1) the patient him/herself cannot give informed consent and cannot participate in the decision-making process; 2) the surgical procedure or chronic electrical stimulation may accelerate cognitive decline; 3) PD patients with dementia are in a more advanced stage of the disease than those without dementia and thus are more likely to develop end-stage problems that are resistant to medical therapy and STN DBS and may exhibit shorter survival times [55-57]; 4) these patients are at greater risk due to living with implanted electrical hardware [58]; and 5) these patients may not be able to enjoy the benefits of STN DBS subjectively, and it is impossible to measure the extent to which the patients are satisfied with DBS.

SLEEP

Sleep-related problems in PD include insomnia, excessive daytime sleepiness, REM-sleep behavior disorder (RBD), and restless legs syndrome (RLS). In studies investigating the effect of STN DBS on sleep in PD, improvements in sleep quality, increases in total sleep time and uninterrupted sleep time, increases in stage 3–4 non-REM sleep, and decreases in wakefulness after sleep onset have been reported [59-61]. These beneficial effects have been attributed to improvements in the nighttime motor disability. Another study revealed reductions in daytime sleepiness, increases in normal REM sleep, decreases in REM sleep without atonia, improvements in total sleep scale scores, and decreases in wakefulness after sleep onset [62]. The authors suggested the role of reduced dopaminergic medications, a direct effect of STN DBS on sleep, and improvements in motor symptoms as possible mechanisms.

Despite the reported effects of STN DBS on REM sleep in PD, previous reports have shown that RBD is not affected by STN DBS [59,60,63,64], although there is one case report that involved the development of RBD in the immediate postoperative period [65]. A recent study of the clinically diagnosed RBD revealed that the prevalence of clinical RBD increased after STN DBS because preoperative RBD persisted and de novo RBD developed after STN DBS [66].

Reports on the effects of STN DBS on RLS are scarce and inconclusive. Some have reported improvements [67,68]; however, worsening or a lack of significant change have also been reported [59,69].

AUTONOMIC SYMPTOMS

The BG exert an inhibitory effect on micturition probably via the D1-GABAergic direct pathway [70]. It has been reported that 64–87% of early untreated PD patients suffer from lower urinary tract symptoms (LUTS) and that 27–39% of PD patients have severe LUTS [71-75]. Studies have shown that STN DBS improves LUTS, especially detrusor hyperreflexia [76,77]. The mechanism seems to involve afferent bladder information processing in the cortex in addition to the BG [78,79].

Gastrointestinal motility is decreased in PD. One study reported that STN DBS improves gastric emptying, whereas dopaminergic medication had no effect [80]. Improvements in constipation and swallowing have also been described [61,81]. However, the clinical significance of these findings is not yet clear.

Studies of the effects of STN DBS on sweating have produced conflicting results [27,61,82,83]. However, all of these studies are limited by small numbers of included subjects. Orthostatic hypotension improvements after STN DBS have been reported in one study [84].

PAIN AND SENSORY SYMPTOMS

Pain is a common but under-recognized and under-treated problem in PD. Studies have found that 40–85% of patients with PD suffer from pain [85-89]. Pain in PD is negatively associated with QoL. Patients with PD experience many types of pain, and these pains can be classified in several manners. Generally, pain in PD is classified into two types: PDrelated pain, which is caused or aggravated by PD; and PD-unrelated pain [87]. Both types of pain are known to respond to treatment targeting the motor symptoms of PD. Pain in PD can also be classified according to the presumed etiologies as follows: dystonic, musculoskeletal, central, and radicular/neuropathic [90].

A beneficial effect of STN DBS on pain in PD has consistently been reported in many studies [6,91,92]. The mechanisms by which pain improves with STN DBS in PD are not fully understood. Presumably, several mutually nonexclusive mechanisms underlie the improvement in pain after STN DBS including the following: improvements in pain associated with increased muscle tone, alleviation of altered pain processing in the central nervous system, effects on mood, and increased mobility due to improved motor function after STN DBS [93]. Among these putative mechanism, the central pain-modulating effect of STN DBS is notable. One study reported that dystonic pain and central pain improve substantially with STN DBS, whereas radicular/neuropathic pain and musculoskeletal pain were less responsive to STN DBS [91,94], suggesting that the reductions in pain with STN DBS involve a central mechanism. This notion is supported by reports of the lack of correlation between improvements in pain and improvements in motor symptoms [6,95,96]. In line with this, it has long been recognized that the BG are involved in central pain processing [97]. This pain processing mechanism is altered in patients with PD; these patients exhibit decreases in pain thresholds with corresponding changes in functional neuroimaging, and these effects are reversed by STN DBS [98-100].

Notably, although pain improves after STN DBS, new pains develop with the progression of the disease [94,101]. These pains are primarily of musculoskeletal origin and do not readily respond to the treatment of the motor symptoms of PD. Proper evaluation and management of musculoskeletal problems is needed for patients with STN DBS, given that musculoskeletal problems were the leading cause of functional impairments at 3 years after surgery in one report [102].

NONMOTOR FLUCTUATIONS

In addition to motor fluctuations, many patients with advanced PD experience NMFs. The prevalence of NMFs in PD ranges from 15% to 100% across studies, and in some patients, these NMFs are more troublesome than the motor fluctuations [103-105]. The most commonly experienced NMFs are the following: psychiatric and cognitive symptoms including anxiety, panic attacks, euphoria, and slowness of thinking; autonomic symptoms including sweating, facial flushing, dyspnea, and urinary frequency; and sensory symptoms including akathisia and pain [106]. NMFs tend to fluctuate with motor symptoms, and their temporal relation with the medication schedule indicate that the fluctuations between hyperdopaminergic states and hypodopaminergic states are the core mechanism underlying NMFs. Accordingly, it is expected that STN DBS would improve NMFs, and it has been reported that many, if not all, of the symptoms of NMFs improve with STN DBS [25,107].

CONCLUSION

Many NMSs in PD improve after STN DBS, although some NMSs remain unchanged or even worsen. The exact mechanisms of these responses are yet unknown; however, evidence indicates multiple mechanisms that include the direct effect of the stimulation of the STN, reductions in dopaminergic medications and the progression of PD itself. Because NMSs strongly influence the QoL of patients with PD, clinicians should be aware of these NMSs when deciding whether to perform surgery and should pay attention to changes in these symptoms after STN DBS to ensure the optimal adjustments of the electrical stimulation parameters and medications.

Notes

Conflicts of Interest

The authors have no financial conflicts of interest.

REFERENCES

1. Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P, et al. The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 2007;22:1901–1911.Article PubMed
2. Koh SB, Kim JW, Ma HI, Ahn TB, Cho JW, Lee PH, et al. Validation of the Korean-version of the nonmotor symptoms scale for Parkinson’s disease. J Clin Neurol 2012;8:276–283.Article PubMed PMC
3. Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, MacPhee G, et al. Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 2007;22:1623–1629.Article PubMed
4. Floden D, Cooper SE, Griffith SD, Machado AG. Predicting quality of life outcomes after subthalamic nucleus deep brain stimulation. Neurology 2014;83:1627–1633.Article PubMed PMC
5. Martinez-Martin P, Rodriguez-Blazquez C, Kurtis MM, Chaudhuri KR; NMSS Validation Group. The impact of non-motor symptoms on health-related quality of life of patients with Parkinson’s disease. Mov Disord 2011;26:399–406.Article PubMed
6. Cury RG, Galhardoni R, Fonoff ET, Dos Santos Ghilardi MG, Fonoff F, Arnaut D, et al. Effects of deep brain stimulation on pain and other nonmotor symptoms in Parkinson disease. Neurology 2014;83:1403–1409.Article PubMed
7. Nazzaro JM, Pahwa R, Lyons KE. The impact of bilateral subthalamic stimulation on non-motor symptoms of Parkinson’s disease. Parkinsonism Relat Disord 2011;17:606–609.Article PubMed
8. Siderowf A, Jaggi JL, Xie SX, Loveland-Jones C, Leng L, Hurtig H, et al. Long-term effects of bilateral subthalamic nucleus stimulation on health-related quality of life in advanced Parkinson’s disease. Mov Disord 2006;21:746–753.Article PubMed
9. Le Jeune F, Drapier D, Bourguignon A, Péron J, Mesbah H, Drapier S, et al. Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology 2009;73:1746–1751.Article PubMed
10. Thobois S, Ardouin C, Lhommée E, Klinger H, Lagrange C, Xie J, et al. Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain 2010;133(Pt 4):1111–1127.Article PubMed PDF
11. Witt K, Daniels C, Reiff J, Krack P, Volkmann J, Pinsker MO, et al. Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol 2008;7:605–614.Article PubMed
12. Obeso JA, Marin C, Rodriguez-Oroz C, Blesa J, Benitez-Temiño B, Mena-Segovia J, et al. The basal ganglia in Parkinson’s disease: current concepts and unexplained observations. Ann Neurol 2008;64 Suppl 2:S30–S46.
13. Mallet L, Schüpbach M, N’Diaye K, Remy P, Bardinet E, Czernecki V, et al. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc Natl Acad Sci U S A 2007;104:10661–10666.Article PubMed PMC
14. Ko JH, Antonelli F, Monchi O, Ray N, Rusjan P, Houle S, et al. Prefrontal dopaminergic receptor abnormalities and executive functions in Parkinson’s disease. Hum Brain Mapp 2013;34:1591–1604.Article PubMed PMC
15. Lee JY, Seo SH, Kim YK, Yoo HB, Kim YE, Song IC, et al. Extrastriatal dopaminergic changes in Parkinson’s disease patients with impulse control disorders. J Neurol Neurosurg Psychiatry 2014;85:23–30.Article PubMed
16. Ballanger B, Klinger H, Eche J, Lerond J, Vallet AE, Le Bars D, et al. Role of serotonergic 1A receptor dysfunction in depression associated with Parkinson’s disease. Mov Disord 2012;27:84–89.Article PubMed
17. Del Tredici K, Braak H. Dysfunction of the locus coeruleusnorepinephrine system and related circuitry in Parkinson’s disease-related dementia. J Neurol Neurosurg Psychiatry 2013;84:774–783.Article PubMed
18. Lim SY, Fox SH, Lang AE. Overview of the extranigral aspects of Parkinson disease. Arch Neurol 2009;66:167–172.Article PubMed
19. Lim SY, Lang AE. The nonmotor symptoms of Parkinson’s disease--an overview. Mov Disord 2010;25 Suppl 1:S123–S130.Article
20. Castrioto A, Lhommée E, Moro E, Krack P. Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol 2014;13:287–305.Article PubMed
21. Reijnders JS, Ehrt U, Weber WE, Aarsland D, Leentjens AF. A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 2008;23:183–189.quiz 313. Article PubMed
22. Huot P, Fox SH. The serotonergic system in motor and non-motor manifestations of Parkinson’s disease. Exp Brain Res 2013;230:463–476.Article PubMed
23. Vriend C, Raijmakers P, Veltman DJ, van Dijk KD, van der Werf YD, Foncke EM, et al. Depressive symptoms in Parkinson’s disease are related to reduced [123I]FP-CIT binding in the caudate nucleus. J Neurol Neurosurg Psychiatry 2014;85:159–164.Article PubMed
24. Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P, et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med 2010;362:2077–2091.Article PubMed
25. Funkiewiez A, Ardouin C, Caputo E, Krack P, Fraix V, Klinger H, et al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2004;75:834–839.Article PubMed PMC
26. 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;349:1925–1934.Article PubMed
27. Wolz M, Hauschild J, Koy J, Fauser M, Klingelhöfer L, Schackert G, et al. Immediate effects of deep brain stimulation of the subthalamic nucleus on nonmotor symptoms in Parkinson’s disease. Parkinsonism Relat Disord 2012;18:994–997.Article PubMed
28. Couto MI, Monteiro A, Oliveira A, Lunet N, Massano J. Depression and anxiety following deep brain stimulation in Parkinson’s disease: systematic review and meta-analysis. Acta Med Port 2014;27:372–382.Article PubMed
29. Aviles-Olmos I, Kefalopoulou Z, Tripoliti E, Candelario J, Akram H, Martinez-Torres I, et al. Long-term outcome of subthalamic nucleus deep brain stimulation for Parkinson’s disease using an MRI-guided and MRI-verified approach. J Neurol Neurosurg Psychiatry 2014;85:1419–1425.Article PubMed PMC
30. Voon V, Krack P, Lang AE, Lozano AM, Dujardin K, Schüpbach M, et al. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain 2008;131(Pt 10):2720–2728.Article PubMed PMC PDF
31. Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, 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 2013;84:1113–1118.Article PubMed PMC
32. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 2006;355:896–908.Article PubMed
33. 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;368:610–622.Article PubMed
34. Starkstein SE, Merello M, Jorge R, Brockman S, Bruce D, Power B. The syndromal validity and nosological position of apathy in Parkinson’s disease. Mov Disord 2009;24:1211–1216.Article PubMed
35. Drapier D, Drapier S, Sauleau P, Haegelen C, Raoul S, Biseul I, et al. Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? J Neurol 2006;253:1083–1091.Article PubMed
36. Tremblay L, Worbe Y, Thobois S, Sgambato-Faure V, Féger J. Selective dysfunction of basal ganglia subterritories: from movement to behavioral disorders. Mov Disord 2015;Mar. 15. [Epub]. http://dx.doi.org/10.1002/mds.26199. Article
37. Thobois S, Lhommée E, Klinger H, Ardouin C, Schmitt E, Bichon A, et al. Parkinsonian apathy responds to dopaminergic stimulation of D2/D3 receptors with piribedil. Brain 2013;136(Pt 5):1568–1577.Article PubMed PDF
38. Mosley PE, Marsh R. The psychiatric and neuropsychiatric symptoms after subthalamic stimulation for Parkinson’s disease. J Neuropsychiatry Clin Neurosci 2015;27:19–26.Article PubMed
39. 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;82:607–614.Article PubMed
40. Herzog J, Reiff J, Krack P, Witt K, Schrader B, Müller D, et al. Manic episode with psychotic symptoms induced by subthalamic nucleus stimulation in a patient with Parkinson’s disease. Mov Disord 2003;18:1382–1384.Article PubMed
41. Kulisevsky J, Berthier ML, Gironell A, Pascual-Sedano B, Molet J, Parés P. Mania following deep brain stimulation for Parkinson’s disease. Neurology 2002;59:1421–1424.Article PubMed
42. Romito LM, Raja M, Daniele A, Contarino MF, Bentivoglio AR, Barbier A, et al. Transient mania with hypersexuality after surgery for high frequency stimulation of the subthalamic nucleus in Parkinson’s disease. Mov Disord 2002;17:1371–1374.Article PubMed
43. Zhang G, Zhang Z, Liu L, Yang J, Huang J, Xiong N, et al. Impulsive and compulsive behaviors in Parkinson’s disease. Front Aging Neurosci 2014;6:318.PubMed PMC
44. Amami P, Dekker I, Piacentini S, Ferré F, Romito LM, Franzini A, et al. Impulse control behaviours in patients with Parkinson’s disease after subthalamic deep brain stimulation: de novo cases and 3-year follow-up. J Neurol Neurosurg Psychiatry 2015;86:562–564.Article PubMed
45. Castrioto A, Funkiewiez A, Debû B, Cools R, Lhommée E, Ardouin C, et al. Iowa gambling task impairment in Parkinson’s disease can be normalised by reduction of dopaminergic medication after subthalamic stimulation. J Neurol Neurosurg Psychiatry 2015;86:186–190.Article PubMed
46. Kim YE, Kim HJ, Kim HJ, Lee JY, Yun JY, Kim JY, et al. Impulse control and related behaviors after bilateral subthalamic stimulation in patients with Parkinson’s disease. J Clin Neurosci 2013;20:964–969.Article PubMed
47. Lhommée E, Klinger H, Thobois S, Schmitt E, Ardouin C, Bichon A, et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain 2012;135(Pt 5):1463–1477.Article PubMed PDF
48. Aybek S, Gronchi-Perrin A, Berney A, Chiuvé SC, Villemure JG, Burkhard PR, et al. Long-term cognitive profile and incidence of dementia after STN-DBS in Parkinson’s disease. Mov Disord 2007;22:974–981.Article PubMed
49. Kim HJ, Jeon BS, Paek SH, Lee KM, Kim JY, Lee JY, et al. Long-term cognitive outcome of bilateral subthalamic deep brain stimulation in Parkinson’s disease. J Neurol 2014;261:1090–1096.Article PubMed
50. Massano J, Garrett C. Deep brain stimulation and cognitive decline in Parkinson’s disease: a clinical review. Front Neurol 2012;3:66.PubMed PMC
51. Fasano A, Romito LM, Daniele A, Piano C, Zinno M, Bentivoglio AR, et al. Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain 2010;133:2664–2676.Article PubMed PDF
52. Zangaglia R, Pasotti C, Mancini F, Servello D, Sinforiani E, Pacchetti C. Deep brain stimulation and cognition in Parkinson’s disease: an eight-year follow-up study. Mov Disord 2012;27:1192–1194.Article PubMed
53. Smeding HM, Speelman JD, Huizenga HM, Schuurman PR, Schmand B. Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson’s Disease. J Neurol Neurosurg Psychiatry 2011;82:754–760.Article PubMed
54. Lang AE, Houeto JL, Krack P, Kubu C, Lyons KE, Moro E, et al. Deep brain stimulation: preoperative issues. Mov Disord 2006;21 Suppl 14:S171–S196.Article
55. Buter TC, van den Hout A, Matthews FE, Larsen JP, Brayne C, Aarsland D. Dementia and survival in Parkinson disease: a 12-year population study. Neurology 2008;70:1017–1022.Article PubMed
56. Posada IJ, Benito-León J, Louis ED, Trincado R, Villarejo A, Medrano MJ, et al. Mortality from Parkinson’s disease: a population-based prospective study (NEDICES). Mov Disord 2011;26:2522–2529.Article PubMed
57. Willis AW, Schootman M, Kung N, Evanoff BA, Perlmutter JS, Racette BA. Predictors of survival in patients with Parkinson disease. Arch Neurol 2012;69:601–607.Article PubMed PMC
58. Farris S, Ford P, DeMarco J, Giroux ML. Deep brain stimulation and the ethics of protection and caring for the patient with Parkinson’s dementia. Mov Disord 2008;23:1973–1976.Article PubMed
59. Arnulf I, Bejjani BP, Garma L, Bonnet AM, Houeto JL, Damier P, et al. Improvement of sleep architecture in PD with subthalamic nucleus stimulation. Neurology 2000;55:1732–1734.Article PubMed
60. Cicolin A, Lopiano L, Zibetti M, Torre E, Tavella A, Guastamacchia G, et al. Effects of deep brain stimulation of the subthalamic nucleus on sleep architecture in parkinsonian patients. Sleep Med 2004;5:207–210.Article PubMed
61. Zibetti M, Torre E, Cinquepalmi A, Rosso M, Ducati A, Bergamasco B, et al. Motor and nonmotor symptom follow-up in parkinsonian patients after deep brain stimulation of the subthalamic nucleus. Eur Neurol 2007;58:218–223.Article PubMed
62. Nishida N, Murakami T, Kadoh K, Tohge R, Yamanegi M, Saiki H, et al. Subthalamic nucleus deep brain stimulation restores normal rapid eye movement sleep in Parkinson’s disease. Mov Disord 2011;26:2418–2422.Article PubMed
63. Amara AW, Watts RL, Walker HC. The effects of deep brain stimulation on sleep in Parkinson’s disease. Ther Adv Neurol Disord 2011;4:15–24.Article PubMed PMC
64. 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 2002;72:661–664.Article PubMed PMC
65. Piette T, Mescola P, Uytdenhoef P, Henriet M, Vanderkelen B, Jacquy J, et al. A unique episode of REM sleep behavior disorder triggered during surgery for Parkinson’s disease. J Neurol Sci 2007;253:73–76.Article PubMed
66. Kim YE, Jeon BS, Paek SH, Yun JY, Yang HJ, Kim HJ, et al. Rapid eye movement sleep behavior disorder after bilateral subthalamic stimulation in Parkinson’s disease. J Clin Neurosci 2015;22:315–319.Article PubMed
67. Chahine LM, Ahmed A, Sun Z. Effects of STN DBS for Parkinson’s disease on restless legs syndrome and other sleep-related measures. Parkinsonism Relat Disord 2011;17:208–211.Article PubMed
68. Driver-Dunckley E, Evidente VG, Adler CH, Hillman R, Hernandez J, Fletcher G, et al. Restless legs syndrome in Parkinson’s disease patients may improve with subthalamic stimulation. Mov Disord 2006;21:1287–1289.Article PubMed
69. Kedia S, Moro E, Tagliati M, Lang AE, Kumar R. Emergence of restless legs syndrome during subthalamic stimulation for Parkinson disease. Neurology 2004;63:2410–2412.Article PubMed
70. Sakakibara R, Tateno F, Kishi M, Tsuyuzaki Y, Uchiyama T, Yamamoto T. Pathophysiology of bladder dysfunction in Parkinson’s disease. Neurobiol Dis 2012;46:565–571.Article PubMed
71. Araki I, Kuno S. Assessment of voiding dysfunction in Parkinson’s disease by the international prostate symptom score. J Neurol Neurosurg Psychiatry 2000;68:429–433.Article PubMed PMC
72. Herzog J, Volkmann J, Krack P, Kopper F, Pötter M, Lorenz D, et al. Two-year follow-up of subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord 2003;18:1332–1337.Article PubMed
73. Kim HJ, Park SY, Cho YJ, Hong KS, Cho JY, Seo SY, et al. Nonmotor symptoms in de novo Parkinson disease before and after dopaminergic treatment. J Neurol Sci 2009;287:200–204.Article PubMed
74. Østergaard K, Aa Sunde N. Evolution of Parkinson’s disease during 4 years of bilateral deep brain stimulation of the subthalamic nucleus. Mov Disord 2006;21:624–631.Article PubMed
75. Winge K, Skau AM, Stimpel H, Nielsen KK, Werdelin L. Prevalence of bladder dysfunction in Parkinsons disease. Neurourol Urodyn 2006;25:116–122.Article PubMed
76. Finazzi-Agrò E, Peppe A, D’Amico A, Petta F, Mazzone P, Stanzione P, et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson’s disease. J Urol 2003;169:1388–1391.Article PubMed
77. Winge K, Nielsen KK, Stimpel H, Lokkegaard A, Jensen SR, Werdelin L. Lower urinary tract symptoms and bladder control in advanced Parkinson’s disease: effects of deep brain stimulation in the subthalamic nucleus. Mov Disord 2007;22:220–225.Article PubMed
78. Herzog J, Weiss PH, Assmus A, Wefer B, Seif C, Braun PM, et al. Subthalamic stimulation modulates cortical control of urinary bladder in Parkinson’s disease. Brain 2006;129(Pt 12):3366–3375.Article PubMed PDF
79. Herzog J, Weiss PH, Assmus A, Wefer B, Seif C, Braun PM, et al. Improved sensory gating of urinary bladder afferents in Parkinson’s disease following subthalamic stimulation. Brain 2008;131(Pt 1):132–145.Article PubMed PDF
80. Arai E, Arai M, Uchiyama T, Higuchi Y, Aoyagi K, Yamanaka Y, et al. Subthalamic deep brain stimulation can improve gastric emptying in Parkinson’s disease. Brain 2012;135(Pt 5):1478–1485.Article PubMed PDF
81. Chou KL, Taylor JL, Patil PG. The MDS-UPDRS tracks motor and non-motor improvement due to subthalamic nucleus deep brain stimulation in Parkinson disease. Parkinsonism Relat Disord 2013;19:966–969.Article PubMed PMC
82. Halim A, Baumgartner L, Binder DK. Effect of deep brain stimulation on autonomic dysfunction in patients with Parkinson’s disease. J Clin Neurosci 2011;18:804–806.Article PubMed
83. Trachani E, Constantoyannis C, Sirrou V, Kefalopoulou Z, Markaki E, Chroni E. Effects of subthalamic nucleus deep brain stimulation on sweating function in Parkinson’s disease. Clin Neurol Neurosurg 2010;112:213–217.Article PubMed
84. Stemper B, Beric A, Welsch G, Haendl T, Sterio D, Hilz MJ. Deep brain stimulation improves orthostatic regulation of patients with Parkinson disease. Neurology 2006;67:1781–1785.Article PubMed
85. Beiske AG, Loge JH, Rønningen A, Svensson E. Pain in Parkinson’s disease: prevalence and characteristics. Pain 2009;141:173–177.Article PubMed
86. Defazio G, Berardelli A, Fabbrini G, Martino D, Fincati E, Fiaschi A, et al. Pain as a nonmotor symptom of Parkinson disease: evidence from a case-control study. Arch Neurol 2008;65:1191–1194.Article PubMed
87. Lee MA, Walker RW, Hildreth TJ, Prentice WM. A survey of pain in idiopathic Parkinson’s disease. J Pain Symptom Manage 2006;32:462–469.Article PubMed
88. Nègre-Pagès L, Regragui W, Bouhassira D, Grandjean H, Rascol O; DoPaMiP Study Group. Chronic pain in Parkinson’s disease: the cross-sectional French DoPaMiP survey. Mov Disord 2008;23:1361–1369.Article PubMed
89. Tinazzi M, Del Vesco C, Fincati E, Ottaviani S, Smania N, Moretto G, et al. Pain and motor complications in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2006;77:822–825.Article PubMed PMC
90. Ford B. Pain in Parkinson’s disease. Clin Neurosci 1998;5:63–72.Article PubMed
91. Kim HJ, Paek SH, Kim JY, Lee JY, Lim YH, Kim MR, et al. Chronic subthalamic deep brain stimulation improves pain in Parkinson disease. J Neurol 2008;255:1889–1894.Article PubMed
92. Sürücü O, Baumann-Vogel H, Uhl M, Imbach LL, Baumann CR. Subthalamic deep brain stimulation versus best medical therapy for L-dopa responsive pain in Parkinson’s disease. Pain 2013;154:1477–1479.Article PubMed
93. Kim HJ, Jeon BS, Paek SH. Effect of deep brain stimulation on pain in Parkinson disease. J Neurol Sci 2011;310:251–255.Article PubMed
94. Jung YJ, Kim HJ, Jeon BS, Park H, Lee WW, Paek SH. An 8-Year Follow-up on the Effect of Subthalamic Nucleus Deep Brain Stimulation on Pain in Parkinson Disease. JAMA Neurol 2015;Mar. 23. [Epub]. http://dx.doi.org/10.1001/jamaneurol.2015.8. Article
95. Marques A, Chassin O, Morand D, Pereira B, Debilly B, Derost P, et al. Central pain modulation after subthalamic nucleus stimulation: a crossover randomized trial. Neurology 2013;81:633–640.Article PubMed
96. Pellaprat J, Ory-Magne F, Canivet C, Simonetta-Moreau M, Lotterie JA, Radji F, et al. Deep brain stimulation of the subthalamic nucleus improves pain in Parkinson’s disease. Parkinsonism Relat Disord 2014;20:662–664.Article PubMed
97. Chudler EH, Dong WK. The role of the basal ganglia in nociception and pain. Pain 1995;60:3–38.Article PubMed
98. Ciampi de Andrade D, Lefaucheur JP, Galhardoni R, Ferreira KS, Brandão Paiva AR, Bor-Seng-Shu E, et al. Subthalamic deep brain stimulation modulates small fiber-dependent sensory thresholds in Parkinson’s disease. Pain 2012;153:1107–1113.Article PubMed
99. Dellapina E, Ory-Magne F, Regragui W, Thalamas C, Lazorthes Y, Rascol O, et al. Effect of subthalamic deep brain stimulation on pain in Parkinson’s disease. Pain 2012;153:2267–2273.Article PubMed
100. Schestatsky P, Kumru H, Valls-Solé J, Valldeoriola F, Marti MJ, Tolosa E, et al. Neurophysiologic study of central pain in patients with Parkinson disease. Neurology 2007;69:2162–2169.Article PubMed
101. Kim HJ, Jeon BS, Lee JY, Paek SH, Kim DG. The benefit of subthalamic deep brain stimulation for pain in Parkinson disease: a 2-year follow-up study. Neurosurgery 2012;70:18–23.discussion 23-24. Article PubMed PDF
102. Yun JY, Jeon BS, Kim HJ, Kim YE, Lee JY, Paek SH. Musculoskeletal problems need more attention in deep brain stimulation for Parkinson’s disease. Neurol Asia 2013;18:53–58.
103. Gunal DI, Nurichalichi K, Tuncer N, Bekiroglu N, Aktan S. The clinical profile of nonmotor fluctuations in Parkinson’s disease patients. Can J Neurol Sci 2002;29:61–64.Article PubMed
104. Hillen ME, Sage JI. Nonmotor fluctuations in patients with Parkinson’s disease. Neurology 1996;47:1180–1183.Article PubMed
105. Witjas T, Kaphan E, Azulay JP, Blin O, Ceccaldi M, Pouget J, et al. Nonmotor fluctuations in Parkinson’s disease: frequent and disabling. Neurology 2002;59:408–413.Article PubMed
106. Bayulkem K, Lopez G. Nonmotor fluctuations in Parkinson’s disease: clinical spectrum and classification. J Neurol Sci 2010;289:89–92.Article PubMed
107. Witjas T, Kaphan E, Régis J, Jouve E, Chérif AA, Péragut JC, et al. Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson’s disease. Mov Disord 2007;22:1729–1734.Article PubMed

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Journal of Clinical Neurology.2016; 12(4): 393. CrossRef
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Neuropsychology Review.2015; 25(4): 398. CrossRef