Long-term outcomes following deep brain stimulation for Parkinson’s disease

Frederick L. Hitti Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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Ashwin G. Ramayya Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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Brendan J. McShane Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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Andrew I. Yang Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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Kerry A. Vaughan Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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Gordon H. Baltuch Department of Neurosurgery, Pennsylvania Hospital, University of Pennsylvania, Philadelphia, Pennsylvania

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OBJECTIVE

Deep brain stimulation (DBS) is an effective treatment for several movement disorders, including Parkinson’s disease (PD). While this treatment has been available for decades, studies on long-term patient outcomes have been limited. Here, the authors examined survival and long-term outcomes of PD patients treated with DBS.

METHODS

The authors conducted a retrospective analysis using medical records of their patients to identify the first 400 consecutive patients who underwent DBS implantation at their institution from 1999 to 2007. The medical record was used to obtain baseline demographics and neurological status. The authors performed survival analyses using Kaplan-Meier estimation and multivariate regression using Cox proportional hazards modeling. Telephone surveys were used to determine long-term outcomes.

RESULTS

Demographics for the cohort of patients with PD (n = 320) were as follows: mean age of 61 years, 70% male, 27% of patients had at least 1 medical comorbidity (coronary artery disease, congestive heart failure, diabetes mellitus, atrial fibrillation, or deep vein thrombosis). Kaplan-Meier survival analysis on a subset of patients with at least 10 years of follow-up (n = 200) revealed a survival probability of 51% (mean age at death 73 years). Using multivariate regression, the authors found that age at implantation (HR 1.02, p = 0.01) and male sex (HR 1.42, p = 0.02) were predictive of reduced survival. Number of medical comorbidities was not significantly associated with survival (p > 0.5). Telephone surveys were completed by 40 surviving patients (mean age 55.1 ± 6.4 years, 72.5% male, 95% subthalamic nucleus DBS, mean follow-up 13.0 ± 1.7 years). Tremor responded best to DBS (72.5% of patients improved), while other motor symptoms remained stable. Ability to conduct activities of daily living (ADLs) remained stable (dressing, 78% of patients; running errands, 52.5% of patients) or worsened (preparing meals, 50% of patients). Patient satisfaction, however, remained high (92.5% happy with DBS, 95% would recommend DBS, and 75% felt it provided symptom control).

CONCLUSIONS

DBS for PD is associated with a 10-year survival rate of 51%. Survey data suggest that while DBS does not halt disease progression in PD, it provides durable symptomatic relief and allows many individuals to maintain ADLs over long-term follow-up greater than 10 years. Furthermore, patient satisfaction with DBS remains high at long-term follow-up.

ABBREVIATIONS

ADLs = activities of daily living; DBS = deep brain stimulation; DVT = deep vein thrombosis; GPi = globus pallidus internus; IPG = implantable pulse generator; PD = Parkinson’s disease; PE = pulmonary embolism; STN = subthalamic nucleus; UPDRS = Unified Parkinson’s Disease Rating Scale.

OBJECTIVE

Deep brain stimulation (DBS) is an effective treatment for several movement disorders, including Parkinson’s disease (PD). While this treatment has been available for decades, studies on long-term patient outcomes have been limited. Here, the authors examined survival and long-term outcomes of PD patients treated with DBS.

METHODS

The authors conducted a retrospective analysis using medical records of their patients to identify the first 400 consecutive patients who underwent DBS implantation at their institution from 1999 to 2007. The medical record was used to obtain baseline demographics and neurological status. The authors performed survival analyses using Kaplan-Meier estimation and multivariate regression using Cox proportional hazards modeling. Telephone surveys were used to determine long-term outcomes.

RESULTS

Demographics for the cohort of patients with PD (n = 320) were as follows: mean age of 61 years, 70% male, 27% of patients had at least 1 medical comorbidity (coronary artery disease, congestive heart failure, diabetes mellitus, atrial fibrillation, or deep vein thrombosis). Kaplan-Meier survival analysis on a subset of patients with at least 10 years of follow-up (n = 200) revealed a survival probability of 51% (mean age at death 73 years). Using multivariate regression, the authors found that age at implantation (HR 1.02, p = 0.01) and male sex (HR 1.42, p = 0.02) were predictive of reduced survival. Number of medical comorbidities was not significantly associated with survival (p > 0.5). Telephone surveys were completed by 40 surviving patients (mean age 55.1 ± 6.4 years, 72.5% male, 95% subthalamic nucleus DBS, mean follow-up 13.0 ± 1.7 years). Tremor responded best to DBS (72.5% of patients improved), while other motor symptoms remained stable. Ability to conduct activities of daily living (ADLs) remained stable (dressing, 78% of patients; running errands, 52.5% of patients) or worsened (preparing meals, 50% of patients). Patient satisfaction, however, remained high (92.5% happy with DBS, 95% would recommend DBS, and 75% felt it provided symptom control).

CONCLUSIONS

DBS for PD is associated with a 10-year survival rate of 51%. Survey data suggest that while DBS does not halt disease progression in PD, it provides durable symptomatic relief and allows many individuals to maintain ADLs over long-term follow-up greater than 10 years. Furthermore, patient satisfaction with DBS remains high at long-term follow-up.

The natural history of Parkinson’s disease (PD) has been well studied. In addition to the well-known motor symptoms such as rigidity, bradykinesia, and resting tremor, nonmotor symptoms such as dementia, sleep-wake dysregulation, and autonomic failure are major features of the illness. Several studies have found that patients with PD have a higher mortality than the age-matched population, approximately 44% after 9.4 years with the disease11,14 (although see the study by Diem-Zangerl and colleagues6). There is a high prevalence (50%–80%) of dementia, nursing home living, hallucinations, and autonomic dysregulation among 20-year survivors.13 Levodopa therapy improves motor symptoms but has a limited effect on nonmotor features of the disease.12 In this study, we wanted to assess the long-term outcomes associated with deep brain stimulation (DBS) therapy.

DBS is an effective treatment option for several movement disorders including PD, essential tremor (ET), and dystonia.8,15,26,28,29 This remarkable treatment modality has improved quality of life and functional outcomes for many patients.5,9,18 While DBS was FDA approved for ET/PD-associated tremor in 1997 (thalamic stimulation) and PD in 2003 (subthalamic nucleus [STN]/globus pallidus internus [GPi] stimulation), few studies have reported a series with follow-up of greater than 5 years.20 Published long-term DBS studies have included mean/median follow-up times of 2.5 years,17 5 years,24,25 and 6 years.4,19 Bang Henriksen et al. reported the survival and outcomes of PD patients treated with DBS with at least 10 years of follow-up.1 In their study, the measured outcomes included presence of hallucinations, dementia, and nursing home placement. Other outcome domains, however, such as patient satisfaction, motor symptom control, and ability to perform activities of daily living (ADLs) were not reported. Another study did report outcomes of PD patients treated with DBS with a mean follow-up of 11 years; however, the cohort size was relatively small.23 In the present study, we investigated the long-term outcomes of PD patients treated with DBS to determine durability of treatment with regard to patient satisfaction, motor symptom control, and ability to perform ADLs.

Methods

Patient Selection

We obtained approval from our institutional review board (IRB) to retrospectively identify the first 400 consecutive patients at our institution who underwent DBS implantation for any indication. Of these patients, 320 underwent DBS for treatment of PD. The other 80 patients were implanted with DBS systems for treatment of essential tremor, dystonia, epilepsy, or tremor associated with multiple sclerosis. Only the PD patients were enrolled in the present study. The year of implantation ranged from 1999 to 2007.

Clinical Data Collection

Once the target patient population was identified, we collected data from medical records, both paper and electronic (Epic, Epic Systems Corporation). Demographic information, preoperative symptoms, ability to conduct basic ADLs, survival, DBS target, and complications were recorded. If a patient was unable to be contacted by phone, public death records were used to determine if the patient was still alive.

Phone surveys were conducted to determine long-term outcomes and patient satisfaction with DBS. Patients’ phone numbers were obtained from the medical record and a minimum of 3 separate attempts were made to contact each patient. Questions regarding motor symptoms and ADLs were binary yes/no questions. Likert-type response choices were used for the patient satisfaction portion of the survey. For this portion, answer choices were: “completely agree,” “mostly agree,” “unsure,” “mostly disagree,” or “completely disagree.” “Completely agree” and “mostly agree” were scored as affirmative responses.

Statistical Analysis

Statistical analysis was performed using Microsoft Excel and MATLAB (MathWorks, Inc.). We performed survival analyses using Kaplan-Meier estimation and multivariate regression using Cox proportional hazards modeling. Results were considered significant if p < 0.05. Averages are presented as mean ± standard deviation unless otherwise specified.

Results

Patient Population

Of the first 400 consecutive patients at our institution implanted with a DBS system, 320 were implanted for treatment of PD (Table 1). The average age at implantation was 61.1 ± 9.4 years and the majority of patients were male (n = 225, 70%). The STN was the stimulation target for the majority of patients (n = 304, 95%). The GPi was targeted in 16 (5%) patients. The vast majority of patients received bilateral stimulation (n = 295, 92%). Only 25 patients (8%) were implanted with unilateral systems. We also examined the longevity of patients’ implantable pulse generators (IPGs). Excluding patients who transferred their care to another facility or patients for whom date of death could not be definitively determined, we found an average IPG longevity of 3.7 ± 0.1 years (SEM).

TABLE 1.

Patient demographics

Value
Mean age at implantation, yrs61.1 ± 9.4
Sex225 (70%) M, 95 (30%) F
Target304 (95%) STN, 16 (5%) GPi
Laterality295 (92%) bilateral, 25 (8%) unilateral
Mean ± SEM IPG longevity, yrs3.7 ± 0.1

Values are number of patients (%) and means are presented ± SD unless otherwise indicated.

Survival Analysis

In a subset of patients who had at least 10 years of follow-up, we performed a Kaplan-Meier survival analysis (Fig. 1). We found that 51% of patients survived through the follow-up interval. For patients who died during the follow-up interval, the mean age of death was 73 years. We performed multivariate regression analysis to assess for factors that were associated with survival probability. We found that age at implantation (HR 1.02, p = 0.01) and male sex (HR 1.42, p = 0.02) were predictive of reduced survival. The number of medical comorbidities was not significantly associated with survival (p > 0.5).

FIG. 1.
FIG. 1.

Kaplan-Meier survival curves in patients with PD following DBS with at least 10 years of follow-up (n = 200) stratified by age at implantation (A), sex (B), and number of medical comorbidities (C). Dotted lines represent 95% confidence intervals. num comorb = number of comorbidities. See main text for statistical analysis details.

Telephone Survey

The surviving patients were surveyed by telephone to determine patient outcomes and satisfaction. Of the surviving patients, 40 patients had completed both a preoperative questionnaire and the follow-up telephone survey (Table 2). The average age at DBS implantation in this cohort (55.1 ± 6.4 years) was less than the mean age of the entire study cohort. Otherwise, the demographics of this cohort of patients were similar to the demographics of the entire study cohort. The majority were male (n = 29, 72.5%) and were treated with STN stimulation (n = 38, 95%). Only 2 (5%) patients were treated with GPi stimulation. All patients in this group received bilateral stimulation (Table 2). Average length of follow-up was 13.0 ± 1.7 years (range 10.6–18.0 years).

TABLE 2.

Demographics of survey responders

Value
Mean age at implantation, yrs55.1 ± 6.4
Sex29 (72.5%) M, 11 (27.5%) F
Target38 (95%) STN, 2 (5%) GPi
Laterality40 (100%) bilateral
FU, yrs13.0 ± 1.7 (range 10.6–18.0)

FU = follow-up.

Values are number of patients (%) unless otherwise indicated. Means are presented ± SD.

Long-Term Motor Function Outcomes

The presence of several motor manifestations of PD (tremor, freezing, speech difficulty, and swallowing difficulty) was assessed with a preoperative questionnaire and a long-term follow-up telephone survey (Table 3). Tremor was the most common preoperative motor symptom in this patient population (n = 34, 85%). The majority of patients also reported freezing (n = 27, 68%) and difficulty with speech (n = 24, 60%) preoperatively. Only 15 patients (38%) reported difficulty with swallowing preoperatively. At long-term follow-up, tremor was effectively abolished in the majority of patients; 29 patients (72.5%) saw improvement in tremor at long-term follow-up. Only 6 patients (15%) reported presence of tremor at long-term follow-up. Other motor symptoms of PD including freezing, speech difficulty, and swallowing difficulty were stable in the majority of patients (n = 23, 57.5%), (n = 27, 67.5%), and (n = 22, 55%), respectively.

TABLE 3.

Motor function

Motor SymptomPreop vs FUStable vs Improved vs Worsened
Tremor34 (85%) vs 6 (15%)10 (25%) vs 29 (72.5%) vs 1 (2.5%)
Freezing27 (68%) vs 24 (60%)23 (57.5%) vs 10 (25%) vs 7 (17.5%)
Speech difficulty24 (60%) vs 31 (78%)27 (67.5%) vs 3 (7.5%) vs 10 (25%)
Swallowing difficulty15 (38%) vs 15 (38%)22 (55%) vs 9 (22.5%) vs 9 (22.5%)

Values are number of patients (%). Boldface type indicates the result with the highest percentage for each symptom.

Long-Term ADL Outcomes

Preoperative questionnaires and long-term follow-up surveys were also used to assess patients’ ability to perform ADLs. Preoperatively, the majority of patients were able to clothe themselves (n = 38, 95%), prepare their own meals (n = 31, 78%), and run errands (n = 30, 75%). While the majority of patients could still clothe themselves at long-term follow-up (n = 29, 73%), many patients lost the ability to prepare meals or run errands. Only 13 patients (33%) could prepare their own meals or run errands at long-term follow-up. Twenty patients (50%) lost the ability to prepare their own meals, and 18 patients (45%) lost the ability to run errands (Table 4).

TABLE 4.

Activities of daily living

ActivityAble Preop vs at FUStable vs Improved vs Worsened
Putting clothing on38 (95%) vs 29 (73%)31 (78%) vs 0 (0%) vs 9 (23%)
Preparing meals31 (78%) vs 13 (33%)18 (45%) vs 2 (5%) vs 20 (50%)
Running errands30 (75%) vs 13 (33%)21 (52.5%) vs 1 (2.5%) vs 18 (45%)

Values are number of patients (%). Boldface type indicates the result with the highest percentage for each activity.

Patient Satisfaction

Phone surveys were conducted to assess patient satisfaction with DBS therapy (Table 5). The vast majority were pleased with their DBS system (n = 37, 92.5%) and would recommend it to their friends/family (n = 38, 95%). A majority of patients felt that the DBS system ameliorated their symptoms (n = 30, 75%). DBS relies on an IPG that could be seen as bothersome; however, only a small minority of patients (n = 5, 12.5%) felt this way. Furthermore, very few patients were fearful of their DBS system (n = 3, 7.5%). A high frequency of IPG changes could negatively impact patient satisfaction and our results could be confounded if survey participants had less frequent battery changes due to survey participation bias. We, however, found no statistically significant difference (p = 0.92, unpaired t-test) between IPG lifespan in survey participants (3.72 ± 0.16 years, mean ± SEM) and nonparticipants (3.68 ± 0.13 years, mean ± SEM).

TABLE 5.

Patient satisfaction

QuestionNo. (%) Replying in Affirmative
Does your DBS control your symptoms?30 (75)
Are you happy with your DBS system?37 (92.5)
Would you recommend DBS to friends/family?38 (95)
Are you fearful of or do you worry about your DBS?3 (7.5)
Does your DBS battery bother you?5 (12.5)

Complications

We reviewed patient charts to determine complications following DBS surgery (Table 6). Infection requiring surgical washout or hardware removal/replacement was the most common complication of DBS surgery (n = 35, 10.94%). Other less common surgical complications included deep vein thrombosis (DVT)/pulmonary embolism (PE) (n = 4, 1.25%), seizure (n = 2, 0.63%), and intracranial hemorrhage (n = 3, 0.94%). Of the 3 patients with intracranial hemorrhage, only one had permanent neurological deficits postoperatively. Four patients (1.25%) required surgical revision of extension wires due to high impedances or fractures and 3 patients (0.94%) required revision of the intracranial leads due to suboptimal placement. A few patients elected to have their devices removed (n = 3, 0.94%) or turned off (n = 1, 0.31%) due to lack of efficacy or stimulation intolerance. A small subset of patients required revision of their IPG due to hematoma (n = 2, 0.63%) or discomfort described as a sensation of electric shocks (n = 1, 0.31%). One patient presented with PD crisis and 1 patient died from perioperative PE. As demonstrated above, we observed a high rate of satisfaction following DBS surgery. One possible confounder is participation or nonresponse bias. Hypothetically, survey responders may have been more willing to participate in the survey if they were less likely to have had surgical complications. To assess this, we compared complication rates in survey participants versus nonparticipants. We found no significant difference (Fisher’s exact test, p = 0.66) between complication rate in survey participants (n = 8, 20%) versus nonparticipants (n = 49, 17.5%).

TABLE 6.

Complications

ComplicationNo. of Pts (%)
Infection requiring surgery35 (10.94)
DVT/PE4 (1.25)
Extension wire revision4 (1.25)
Lead placement revision3 (0.94)
Intracranial hemorrhage3 (0.94)
Device removal3 (0.94)
IPG site hematoma2 (0.63)
Seizure2 (0.63)
PD crisis1 (0.31)
IPG discomfort1 (0.31)
Device turned off1 (0.31)
Death1 (0.31)

Pts = patients.

Discussion

In this study, we aimed to investigate long-term outcomes associated with DBS for PD at a single academic center (n = 320). We report the following results. First, we found a 10-year survival probability of 51% in a subgroup of 200 patients with confirmed 10-year follow-up. Second, based on telephone surveys completed in a subset of surviving patients (n = 40), the improvement in tremor after DBS therapy was sustained at 10 years. Third, non–tremor symptoms such as speech difficulty, freezing, and a decline in ability to perform activities of daily living were prevalent at long-term follow-up.

We found that the 10-year survival following DBS for PD was 51%. Multivariate regression analyses showed that survival probability was higher in younger patients and women. We did not observe an association between survival and number of medical comorbidities as we have previously reported when studying 30-day readmission rates.22 The 10-year survival probability reported in our study is similar to those in previous studies of PD that report a mortality rate of approximately 44% after 9.5 years with the disease.6,11,14 However, our 10-year survival probability (51% in 200 patients) is lower than that reported by Bang Henriksen and colleagues (70% in 79 patients).1 This discrepancy is likely a result of regression to the mean and differences in the patient samples, although we did not identify any obvious differences in age at implantation, sex distribution, or medical comorbidities between the two studies.

We found that tremor associated with PD responded best to DBS, and that symptomatic improvement was durable even at long-term follow-up of more than 10 years. However, non–tremor motor symptoms such as freezing and dysarthria persisted at long-term follow-up. While these patients may have had transient improvement of these symptoms postoperatively, relief was not sustained at long-term follow-up.

These results are in agreement with and expand upon previous data. Lezcano and colleagues reported that tremor improved at 5-year follow-up relative to baseline while speech and communication worsened.16 A meta-analysis demonstrated that STN and GPi DBS results in durable tremor suppression up to 5 years postoperatively.25 Another study revealed that tremor had improved at the 11-year mean follow-up and speech had worsened.23 Our results confirm these findings in a larger patient cohort.

Importantly, the DBS-treated PD patients in this cohort maintained their ability to perform basic tasks at long-term follow-up, such as dressing themselves. On the other hand, the majority of patients could not accomplish more complex tasks at long-term follow-up, such as preparing meals or running errands independently.

One study demonstrated that patients’ self-reported improvement with ADLs was sustained up to 5 years after surgery.16 Another study with a mean follow-up time of 11 years, however, reported worsening of ability to perform ADLs.23 The former study grouped several ADLs together when doing the analysis. This difference in the data analysis method could explain the difference in our findings. Another study compared PD patients treated with STN-DBS with those treated with medication alone at 6 year follow-up and found that ability to perform ADLs (as measured by mean UPDRS-II [Unified Parkinson’s Disease Rating Scale II] score remained stable in the DBS group but worsened in the medication-alone group.19 Furthermore, another group demonstrated that even older patients (≥ 65 years old) treated with STN-DBS exhibited improvement in ability to perform ADLs at follow-up of 3–5 years. Our results extend these findings by examining patient outcomes for a mean follow-up time of over 10 years.

Our survey data demonstrate that satisfaction with DBS remains high even at long-term follow-up. The majority of patients felt that their DBS helps control their symptoms. The vast majority of patients were happy with their DBS system and would recommend DBS to family/friends. Having an implanted device could result in patient anxiety; however, very few patients endorsed fears regarding their DBS system and few found it bothersome. One study examined patient satisfaction with STN-DBS at the 6-month follow-up and found that the majority of patients felt that they made the right decision to get DBS (89%) and would recommend it to other patients (72%).10 Our data demonstrate that patient satisfaction remains high even at long-term (> 10 years) follow-up.

We tracked surgical complications in our patients and found that the majority of complications were a result of infections requiring surgical treatment. This finding is in agreement with those of prior studies of DBS complications.2,3,7,27,30 We have implemented measures to reduce our infection rate, including irrigation with povidone-iodine and placement of vancomycin powder in the cranial and chest wounds. Relative to other intracranial procedures, DBS is considered relatively safe. We did unfortunately observe one death due to PE in the perioperative period. We have since implemented treatment with subcutaneous heparin preoperatively for DVT/PE prophylaxis during DBS implantation. Prophylaxis is continued in the postoperative period as well.

Study Limitations

Our study has several limitations. First, we had a number of patients drop out of the study due to death, inability to contact the patient, or patient refusal to take the surveys. Second, our outcome metrics were not based on widely used scales such as the UPDRS21 so our findings may not be comparable to those of other studies. Our study also included a retrospective component to identify the patient cohort. The above limitations may limit the generalizability of our results.

Conclusions

The current study demonstrates that while DBS does not stop disease progression in all domains, it does provide durable symptomatic relief of tremor and allows many individuals to maintain ADLs over a long-term follow-up of more than 10 years. Furthermore, patient satisfaction with DBS remains high even at a mean follow-up of more than 10 years.

Acknowledgments

We thank the members of the Neurosurgery Clinical Research Division (NCRD) for their assistance with IRB approval and data collection.

Disclosures

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

Author Contributions

Conception and design: Baltuch. Acquisition of data: Ramayya, McShane. Analysis and interpretation of data: Hitti, Ramayya. Drafting the article: Hitti. Critically revising the article: Baltuch, Hitti, Ramayya, Yang, Vaughan. Reviewed submitted version of manuscript: all authors. Statistical analysis: Hitti, Ramayya. Administrative/technical/material support: Baltuch. Study supervision: Baltuch.

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    Rizzone MG, Fasano A, Daniele A, Zibetti M, Merola A, Rizzi L, 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 20:376381, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Shalash A, Alexoudi A, Knudsen K, Volkmann J, Mehdorn M, Deuschl G: The impact of age and disease duration on the long term outcome of neurostimulation of the subthalamic nucleus. Parkinsonism Relat Disord 20:4752, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    St George RJ, Nutt JG, Burchiel KJ, Horak FB: A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology 75:12921299, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Tröster AI, Fields JA, Pahwa R, Wilkinson SB, Strait-Tröster KA, Lyons K, et al.: Neuropsychological and quality of life outcome after thalamic stimulation for essential tremor. Neurology 53:17741780, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Voges J, Waerzeggers Y, Maarouf M, Lehrke R, Koulousakis A, Lenartz D, et al.: Deep-brain stimulation: long-term analysis of complications caused by hardware and surgery—experiences from a single centre. J Neurol Neurosurg Psychiatry 77:868872, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

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

    • Crossref
    • PubMed
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    • Export Citation
  • 29

    Weaver FM, Follett KA, Stern M, Luo P, Harris CL, Hur K, et al.: Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology 79:5565, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zhang J, Wang T, Zhang CC, Zeljic K, Zhan S, Sun BM, et al.: The safety issues and hardware-related complications of deep brain stimulation therapy: a single-center retrospective analysis of 478 patients with Parkinson’s disease. Clin Interv Aging 12:923928, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Figure from Minchev et al. (pp 150–158).

  • FIG. 1.

    Kaplan-Meier survival curves in patients with PD following DBS with at least 10 years of follow-up (n = 200) stratified by age at implantation (A), sex (B), and number of medical comorbidities (C). Dotted lines represent 95% confidence intervals. num comorb = number of comorbidities. See main text for statistical analysis details.

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    Bang Henriksen M, Johnsen EL, Sunde N, Vase A, Gjelstrup MC, Østergaard K: Surviving 10 years with deep brain stimulation for Parkinson’s disease—a follow-up of 79 patients. Eur J Neurol 23:5361, 2016

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    Bhatia S, Zhang K, Oh M, Angle C, Whiting D: Infections and hardware salvage after deep brain stimulation surgery: a single-center study and review of the literature. Stereotact Funct Neurosurg 88:147155, 2010

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    Bjerknes S, Skogseid IM, Sæhle T, Dietrichs E, Toft M: Surgical site infections after deep brain stimulation surgery: frequency, characteristics and management in a 10-year period. PLoS One 9:e105288, 2014

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    Børretzen MN, Bjerknes S, Sæhle T, Skjelland M, Skogseid IM, Toft M, et al.: Long-term follow-up of thalamic deep brain stimulation for essential tremor—patient satisfaction and mortality. BMC Neurol 14:120, 2014

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    Diamond A, Jankovic J: The effect of deep brain stimulation on quality of life in movement disorders. J Neurol Neurosurg Psychiatry 76:11881193, 2005

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    Fernández-Pajarín G, Sesar A, Ares B, Relova JL, Arán E, Gelabert-González M, et al.: Delayed complications of deep brain stimulation: 16-year experience in 249 patients. Acta Neurochir (Wien) 159:17131719, 2017

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    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 362:20772091, 2010

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    Hälbig TD, Gruber D, Kopp UA, Schneider GH, Trottenberg T, Kupsch A: Pallidal stimulation in dystonia: effects on cognition, mood, and quality of life. J Neurol Neurosurg Psychiatry 76:17131716, 2005

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    Hasegawa H, Samuel M, Douiri A, Ashkan K: Patients’ expectations in subthalamic nucleus deep brain stimulation surgery for Parkinson disease. World Neurosurg 82:12951299, 2014

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    Hely MA, Reid WGJ, Adena MA, Halliday GM, Morris JGL: The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord 23:837844, 2008

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    Kleiner-Fisman G, Liang GSL, Moberg PJ, Ruocco AC, Hurtig HI, Baltuch GH, et al.: Subthalamic nucleus deep brain stimulation for severe idiopathic dystonia: impact on severity, neuropsychological status, and quality of life. J Neurosurg 107:2936, 2007

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    Lezcano E, Gómez-Esteban JC, Tijero B, Bilbao G, Lambarri I, Rodriguez O, et al.: Long-term impact on quality of life of subthalamic nucleus stimulation in Parkinson’s disease. J Neurol 263:895905, 2016

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    Liang GS, Chou KL, Baltuch GH, Jaggi JL, Loveland-Jones C, Leng L, et al.: Long-term outcomes of bilateral subthalamic nucleus stimulation in patients with advanced Parkinson’s disease. Stereotact Funct Neurosurg 84:221227, 2006

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  • 18

    Martínez-Martín P, Valldeoriola F, Tolosa E, Pilleri M, Molinuevo JL, Rumià J, et al.: Bilateral subthalamic nucleus stimulation and quality of life in advanced Parkinson’s disease. Mov Disord 17:372377, 2002

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  • 19

    Merola A, Rizzi L, Zibetti M, Artusi CA, Montanaro E, Angrisano S, et al.: Medical therapy and subthalamic deep brain stimulation in advanced Parkinson’s disease: a different long-term outcome? J Neurol Neurosurg Psychiatry 85:552559, 2014

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  • 20

    Miocinovic S, Somayajula S, Chitnis S, Vitek JL: History, applications, and mechanisms of deep brain stimulation. JAMA Neurol 70:163171, 2013

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    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 18:738750, 2003

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  • 22

    Ramayya AG, Abdullah KG, Mallela AN, Pierce JT, Thawani J, Petrov D, et al.: Thirty-day readmission rates following deep brain stimulation surgery. Neurosurgery 81:259267, 2017

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  • 23

    Rizzone MG, Fasano A, Daniele A, Zibetti M, Merola A, Rizzi L, 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 20:376381, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Shalash A, Alexoudi A, Knudsen K, Volkmann J, Mehdorn M, Deuschl G: The impact of age and disease duration on the long term outcome of neurostimulation of the subthalamic nucleus. Parkinsonism Relat Disord 20:4752, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    St George RJ, Nutt JG, Burchiel KJ, Horak FB: A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology 75:12921299, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Tröster AI, Fields JA, Pahwa R, Wilkinson SB, Strait-Tröster KA, Lyons K, et al.: Neuropsychological and quality of life outcome after thalamic stimulation for essential tremor. Neurology 53:17741780, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Voges J, Waerzeggers Y, Maarouf M, Lehrke R, Koulousakis A, Lenartz D, et al.: Deep-brain stimulation: long-term analysis of complications caused by hardware and surgery—experiences from a single centre. J Neurol Neurosurg Psychiatry 77:868872, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

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

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Weaver FM, Follett KA, Stern M, Luo P, Harris CL, Hur K, et al.: Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology 79:5565, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zhang J, Wang T, Zhang CC, Zeljic K, Zhan S, Sun BM, et al.: The safety issues and hardware-related complications of deep brain stimulation therapy: a single-center retrospective analysis of 478 patients with Parkinson’s disease. Clin Interv Aging 12:923928, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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