Risks of common complications in deep brain stimulation surgery: management and avoidance

Clinical article

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Object

Deep brain stimulation (DBS) surgery is increasingly prominent in the treatment of various disorders refractory to medication. Despite the procedure's efficacy, the community at large continues to be hesitant about presumed associated risks. The main object of this study was to assess the incidence of various surgical complications occurring both during and after DBS device implantation in a large population of patients with movement disorders in an effort to better quantify patient risk, define management plans, and develop methods for risk avoidance. A second aim was to corroborate the low procedural complication risk of DBS reported by others, which in light of the procedure's efficacy is needed to promote its widespread acceptance.

Methods

All patients who had undergone new DBS device implantation surgery between 2002 and 2010 by a single surgeon were entered into a database after being verified by cross-referencing manufacturer implantation records. All surgical records and charts were reviewed to identify intraoperative, perioperative, and long-term surgical complications, including any characteristics predictive of an adverse event.

Results

Seven hundred twenty-eight patients received 1333 new DBS electrodes and 1218 new internal pulse generators (IPGs) in a total of 1356 stereotactic procedures for the treatment of movement disorders. Seventy-eight percent of the patients had staged lead and IPG implantations. Of the 728 patients, 452 suffered from medically refractory Parkinson disease; in the other patients, essential tremor (144), dystonia (64), mixed disease (30), and other hyperkinetic movement disorders (38) were diagnosed. Severe intraoperative adverse events included vasovagal response in 6 patients (0.8%), hypotension in 2 (0.3%), and seizure in 2 (0.3%). Postoperative imaging confirmed asymptomatic intracerebral hemorrhage (ICH) in 4 patients (0.5%), asymptomatic intraventricular hemorrhage in 25 (3.4%), symptomatic ICH in 8 (1.1%), and ischemic infarction in 3 (0.4%), associated with hemiparesis and/or decreased consciousness in 13 (1.7%). Long-term complications of DBS device implantation not requiring additional surgery included hardware discomfort in 8 patients (1.1%) and loss of desired effect in 10 (1.4%). Hardware-related complications requiring surgical revision included wound infections in 13 patients (1.7%), lead malposition and/or migration in 13 (1.7%), component fracture in 10 (1.4%), component malfunction in 4 (0.5%), and loss of effect in 19 (2.6%).

Conclusions

The authors confirmed that the overall risk of both procedure- and hardware-related adverse events is acceptably low. They offer advice on how to avoid the most common complications.

Abbreviations used in this paper:DBS = deep brain stimulation; ET = essential tremor; GPi = globus pallidus internus; ICH = intracerebral hemorrhage; IPG = internal pulse generator; IVH = intraventricular hemorrhage; IVP = intraventricular pneumocephalus; MER = microelectrode recording; PD = Parkinson disease; STN = subthalamic nucleus; Vim = ventral intermediate nucleus of the thalamus.

Abstract

Object

Deep brain stimulation (DBS) surgery is increasingly prominent in the treatment of various disorders refractory to medication. Despite the procedure's efficacy, the community at large continues to be hesitant about presumed associated risks. The main object of this study was to assess the incidence of various surgical complications occurring both during and after DBS device implantation in a large population of patients with movement disorders in an effort to better quantify patient risk, define management plans, and develop methods for risk avoidance. A second aim was to corroborate the low procedural complication risk of DBS reported by others, which in light of the procedure's efficacy is needed to promote its widespread acceptance.

Methods

All patients who had undergone new DBS device implantation surgery between 2002 and 2010 by a single surgeon were entered into a database after being verified by cross-referencing manufacturer implantation records. All surgical records and charts were reviewed to identify intraoperative, perioperative, and long-term surgical complications, including any characteristics predictive of an adverse event.

Results

Seven hundred twenty-eight patients received 1333 new DBS electrodes and 1218 new internal pulse generators (IPGs) in a total of 1356 stereotactic procedures for the treatment of movement disorders. Seventy-eight percent of the patients had staged lead and IPG implantations. Of the 728 patients, 452 suffered from medically refractory Parkinson disease; in the other patients, essential tremor (144), dystonia (64), mixed disease (30), and other hyperkinetic movement disorders (38) were diagnosed. Severe intraoperative adverse events included vasovagal response in 6 patients (0.8%), hypotension in 2 (0.3%), and seizure in 2 (0.3%). Postoperative imaging confirmed asymptomatic intracerebral hemorrhage (ICH) in 4 patients (0.5%), asymptomatic intraventricular hemorrhage in 25 (3.4%), symptomatic ICH in 8 (1.1%), and ischemic infarction in 3 (0.4%), associated with hemiparesis and/or decreased consciousness in 13 (1.7%). Long-term complications of DBS device implantation not requiring additional surgery included hardware discomfort in 8 patients (1.1%) and loss of desired effect in 10 (1.4%). Hardware-related complications requiring surgical revision included wound infections in 13 patients (1.7%), lead malposition and/or migration in 13 (1.7%), component fracture in 10 (1.4%), component malfunction in 4 (0.5%), and loss of effect in 19 (2.6%).

Conclusions

The authors confirmed that the overall risk of both procedure- and hardware-related adverse events is acceptably low. They offer advice on how to avoid the most common complications.

Since its introduction in 1987 by Benabid et al.,7 deep brain stimulation (DBS) has become a widely recognized technique for reversible modulation of brain function that is adjunctive to the medical management of movement disorders. Its proven efficacy in Parkinson disease (PD)7,15,33,38,56 has led to its worldwide application for a spectrum of hyperkinetic diseases, including essential tremor (ET),6,28,31,49 dystonia,13,34,65,67 cerebellar outflow tremor,9,10,26,57 Gilles de la Tourette syndrome,17,27,63 as well as a growing number of other medically intractable disorders, such as obsessive-compulsive disorder,16,23,24,43,46 major depressive disorder,40,44,45 and cluster headache.60 As this procedure becomes more commonplace, questions of intra- and postprocedural safety, including hardware complications, infection, and suboptimal results,48 will continue to arise during preoperative consultations and must be correctly addressed to prospective patients. In an effort to promote the relative safety of this procedure, we present a retrospective analysis of all adverse effects in 728 consecutive patients treated with DBS by 1 neurosurgeon (R.K.S.) between 2002 and 2010 along with a comparative analysis of the medical literature. Advice on complication avoidance is discussed as well.

Methods

All patients who had undergone new DBS implantation surgery between January 2002 and December 2010 were entered into a database. These patients were identified based on consecutive surgical reports from 1 primary surgeon (R.K.S.) operating at multiple campuses. Procedures were performed at Houston Methodist Hospital, St. Luke's Episcopal Hospital, and Memorial Hermann Hospital. The database was cross-checked with the manufacturers' records of hardware implantations performed at the participating institutions for data verification. The DBS devices were primarily Medtronic implants, with a few investigational device implants (Libra DBS system, St. Jude Medical Neuromodulation). Individual referring neurologists made all diagnoses, and R.K.S. corroborated DBS treatment candidacy, often in a multidisciplinary meeting.

Patients charts identified in the database were analyzed retrospectively for the occurrence of intraoperative, perioperative, and long-term adverse effects, as described in a similar but less inclusive study by the same surgeon.30 Institutional review board approval for this retrospective chart review was sought and granted at each institution. The perioperative period was defined as the first 2 weeks after implantation; and the long-term, as the period occurring after the first 2 postoperative weeks. Transient programming-related symptoms were excluded since these did not surface at postoperative visits to the neurosurgeon; therefore, only undesired sustained side effects that led to lead replacement were recorded. Internal pulse generator (IPG) replacement due to depletion was not considered a complication.

Surgical Procedure

Our standard surgical procedure for DBS has been described in detail elsewhere.20,30,49 Briefly, a stereotactic frame (Leksell, Elekta AB) is placed, and a patient undergoes volumetric imaging whereby indirect targeting can be completed based on reference to the anterior commissure–posterior commissure line. The trajectory is determined using StealthStation navigation (Medtronic Inc.) to avoid cortical vessels and, if possible, the lateral ventricle, usually choosing bur hole locations 4 cm lateral from the midline at the coronal suture. Occasionally, ventriculomegaly makes ventricular transgression unavoidable. Early in the series, lead implantation was often performed during the same time as placement of the lead extensions and IPG, but by 2004 the procedure largely became staged. Stage 2, which involved placement of the extensions and IPG, would occur 1–2 weeks after Stage 1, which was for lead implantation. Microelectrode recording (MER) was routinely performed for all targets except the ventral intermediate nucleus of the thalamus (Vim), for which the Leksell insertion kit (Elekta AB) was used instead of MER at Houston Methodist Hospital and St. Luke's Episcopal Hospital. At all hospital locations, intraoperative test stimulation was performed to verify target accuracy and the lack of sustained side effects. Postoperative CT was routinely performed to verify the location of leads.

Statistical Analysis

All statistical analyses were performed using standard statistical software (SPSS Statistics, version 17.0, SPSS Inc.). Risk factors for the occurrence of adverse effects, such as patient age, diagnosis, date of surgery, and institution, were analyzed with multivariate logistic regression.

The Student t-test with equal variances was used to compare age at implantation between patients with adverse effects and those without. Evaluation of differences between patients with adverse events depending on implant target and hardware type was performed using the Fisher exact test.

Results

Demographic Data

Seven hundred twenty-eight patients received 1333 new DBS leads and 1218 new IPGs in a total of 1356 stereotactic procedures. In this same population, 32 lead revisions and/or replacements and 637 IPG replacement procedures were performed during the study period. Of the newly implanted leads, 1312 were manufactured by Medtronic (model 3387) and 21 by St. Jude Medical Neuromodulation (Libra). Of the newly implanted pulse generators, 1116 were Soletra, 56 were Kinetra, 14 were Activa PC, and 11 were Activa RC, with 21 Libra from St. Jude Medical. Five hundred ninety-two of the 637 IPG replacements were Soletra, with a few in each of the other categories.

Four hundred fifty-two patients suffered from PD, 144 from ET, and 64 from dystonia. Table 1 shows details regarding patient diagnoses and targets of implantation. Patient ages ranged from 11 to 92 years (average 60.8 ± 14.5 years). Thirteen patients were under the age of 18 years at time of DBS implantation. Only 6% of the patients were left handed, and 65.5% were male. The minimum followup was 6 months in all but 5% of the patients. The mean neurosurgical follow-up was 1.9 ± 2.2 years (range 14–2982 days); this number excludes subsequent programming sessions with the referring neurologist. Note that referrals back to neurosurgery were made up to 12.1 years from the initial implant for IPG exchanges, hardware-related issues, and loss of system efficacy, including patients who required surgical revision in the study period but had undergone initial implantation by R.K.S. prior to 2002. Thus, we estimate that most if not all surgery-related long-term complications were captured in this process.

TABLE 1:

Diagnosis in 728 patients referred for DBS (2002–2010), with stimulation target*

DiseaseNo. of PatientsSTNVimGPiPPNSTN/Vim
UnilatBilatUnilatBilatUnilatBilatUnilatBilat
PD452723181517233313
ET14452931
dystonia6416552
PD/ET303113112
PT or MS tremor24915
GTS55
other92421
total no. patients7287532295140992115
total no. leads§13338464411528091843210

GTS = Gilles de la Tourette syndrome; MS = multiple sclerosis; PPN = pedunculopontine nucleus; PT = posttraumatic.

One side the STN and the other side the Vim in the same patient.

Right pedunculopontine nucleus lead added to 2 patients each with bilateral GPi implants (not included in patient total).

Only original leads.

Adverse Events or Complications

Adverse events were subdivided based on when they occurred relative to implantation: intraoperative, perioperative (≤ 2 weeks after implantation), or long-term postoperative (after 2 weeks from implantation). Table 2 provides a summary of event frequency in these 3 categories.

TABLE 2:

Summary of adverse effects after DBS device implantation in 728 patients*

EventNo. of Patients (%)
intraop
 asymptomatic IVH25 (3.4)
 symptomatic ICH8 (1.1)
 asymptomatic ICH4 (0.5)
 acute perilesional edema2 (0.3)
 cortical/subcortical ischemic infarction3 (0.4)
 vasovagal response6 (0.8)
 hypotension2 (0.3)
 confusion3 (0.4)
 anxiety5 (0.7)
 seizure2 (0.3)
 arrhythmia1 (0.1)
 aborted procedure7 (1.0)
periop (≤2 wks)
 headache31 (4.2)
 hemiparesis w/ or w/o decreased LOC13 (1.7)
 confusion7 (1.0)
 confusion/agitation4 (0.5)
 respiratory distress3 (0.4)
 seizure3 (0.4)
 hallucinations3 (0.4)
 somnolence1 (0.1)
 fall1 (0.1)
long-term postop (>2 wks)
 wound complications
  wound infection–self limited10 (1.4)
  wound infections
   requiring system removal7 (1.0)
   requiring lead removal only1 (0.1)
   requiring IPG/extension removal only3 (0.4)
   requiring debridement only2 (0.3)
  skin erosion–device removal2 (0.3)
  wound dehiscence–debridement only2 (0.3)
 hardware complications
  lead fracture–lead revision7 (1.0)
  lead malposition–lead revision9 (1.2)
  lead migration–lead redirection w/o removal4 (0.5)
  lead malfunction/high impedance–lead revision2 (0.3)
  flipped IPG revision4 (0.5)
  malpositioned/uncomfortable IPG–revision4 (0.5)
  IPG malfunction/high impedance–replace1 (0.1)
  lead extension malfunction/high impedance–replace1 (0.1)
  lead extension fracture–replace3 (0.4)
 satisfaction-related complications
  loss of system efficacy over time lead revision19 (2.6)
  decreased efficacy over time no revision desired10 (1.4)
  results not as desired–no revision desired7 (1.0)
  complete system removal w/o replacement5 (0.7)
  lead extension incision uncomfortable8 (1.1)
  IPG site uncomfortable/hematoma–no revision3 (0.4)

LOC = level of consciousness.

Intraoperative Events

The most common overt intraoperative complication was a vasovagal response, which occurred in 6 patients (0.8%), precipitating syncope in 4 patients and causing the procedure to be aborted on 4 occasions. One such episode caused only very transient hemiplegia but did not postpone the case; postoperative CT showed putaminal and intraventricular hemorrhage (IVH). One episode leading to an aborted procedure was later found to be correlated with a postoperative CT finding of air in the cavernous sinus. One intracerebral hemorrhage (ICH) and 1 subcortical infarction produced intraoperative symptoms of hemiparesis, occurring immediately after the first lead insertion, requiring postponement of the remainder of the case.

The most severe complication was hemorrhage: symptomatic ICH developed in 8 patients (1.1%) and manifested as postoperative hemiparesis in 7 and early somnolence in 4. Asymptomatic ICH was identified on postoperative CT in 4 patients (0.5%). More common was the incidental reporting of small IVH layering in either the atrium or the occipital horn of the lateral ventricle in 28 patients (3.8%); only 3 of these patients (11% of those with IVH, 0.4% of the series total) had transient postoperative confusion.

Two patients (0.3%) had a tonic-clonic seizure just prior to MER, with negative emergent imaging findings, causing the procedure to be aborted. Isolated intraoperative issues included 1 case of arrhythmia (0.1%), 2 of transient confusion (0.3%), and 5 of anxiety (0.7%), which was remedied with a small propofol infusion that wore off prior to MER.

Perioperative Events

Perioperative events, which occurred ≤ 2 weeks after surgery, were witnessed during either the hospitalization after Stage 1 or a return to the operating room for Stage 2 of the procedure. Most patients complained of headache (31 patients [4.2%]), which was transient. Confusion either with (4 patients [0.5%]) or without (7 patients [1.0%]) agitation was the next most common symptom, and again was transient; 10 such incidences were associated with subthalamic nucleus (STN) trajectories. Transient hallucinations occurred in 3 patients (0.4%).

Several serious adverse events occurred as well, most within a few hours after the procedure. Thirteen patients (1.7%) had postoperative hemiplegia with or without decreased consciousness, 8 of whom had ICH identified on postoperative CT. One patient had evidence of cortical infarction (0.1%), 2 (0.3%) had subcortical infarctions, and still 2 others (0.3%) had “ill-defined hypodensities” around the electrode tip on postoperative CT, believed to be edema, causing only transient hemiparesis.

Further serious adverse events included seizure in 3 patients (0.4%) on postoperative Day 1 or 2 (with negative CT findings) and respiratory distress in 3 patients (0.4%), 2 of whom required reintubation due to pulmonary edema (1 patient) and aspiration pneumonia requiring subsequent tracheostomy (1 patient).

Long-Term Events

Long-term adverse events were defined as those events that occurred more than 2 weeks after surgery (Table 2). Given this study's surgical perspective, only adverse events that were presented back to the neurosurgery clinic are listed; thus, transient programming-induced ill effects are excluded. These events can be categorized into wound, hardware, or satisfaction-related complications.

Wound Complications

Among wound complications, infection was the most common, occurring in a total of 23 cases (3.1%), 10 (1.4%) of which were self-limited and 13 (1.7%) of which required a return to surgery for debridement and/or device removal (Table 2). Erosions and dehiscence occurred in 2 patients (0.3%) each, requiring surgical debridement only.

Hardware Complications

All hardware-related complications required a reoperation. Lead malposition (9 cases [1.2%]) or migration (4 cases [0.5%]), were the most common hardware complications, leading to revision at an average of 1.3 years after initial implantation (range 0.25–6 years).

Lead fractures (7 cases [1.0%]) and lead extension fractures (3 cases [0.4%]) were also common hardware complications, followed by component malfunction (4 cases [0.5%]) as identified by high impedance in the system, resulting in lead revision (2 cases [0.3%]), lead extension or IPG revision (1 case each [0.1%]) occurring at an average of 4.4 years after the initial operation (range 0.5–8.7 years). Four patients (0.5%) had an IPG that flipped or an uncomfortable or malpositioned IPG, all requiring repositioning.

Satisfaction and System Effectiveness

During the follow-up, stimulation-induced side effects that limited effective use of the DBS device to treat the underlying disorder included dysarthria, diplopia, paresthesia, and nausea in 7 patients (1.0%), none of whom wanted a revision. All patients with malpositioned DBS leads requiring revision (9 cases [1.2%]) eventually suffered from such stimulation-induced side effects, limiting utility of the system. Eight patients complained of discomfort around the lead extensions in the cervical area (1.1%). Pocket hematoma developed in 3 patients (0.4%) after pulse generator implantation, although it subsequently resolved in each case.

Nineteen patients (2.6%) ultimately lost efficacy of 1 or both of their leads over the duration of the study and underwent lead revision. Eighteen of them had either ET or PD tremor that worsened such that initial motor control derived from stimulation was lost despite repeat programming, with lead revision at an average of 4.8 years after initial implantation. One patient with secondary parkinsonism and dystonia had bilateral STN leads revised after 5 years because of limited initial effects. Ten other patients (1.4%) with tremor noted loss of system efficacy over time but did not desire lead revision.

Five patients (0.7%) ultimately wished for complete removal of their system because the system was ineffective (2 patients), symptoms had resolved (1 patient with MS tremor), serial brain MRI studies were needed (1 patient with comorbid tremor and Rasmussen's encephalopathy), and severe dementia had developed (1 patient).

If the total number of hardware complications (n = 29), infections (n = 13), and erosions (n = 2) requiring reoperation are combined, then the total number of long-term device-related complications requiring repeat surgery was 44 (6%). Over the 9 years of this study, 1365 leads were placed, amounting to 12,285 electrode-years; thus, the device-related complication rate was calculated as 0.3% per electrode-year.

Patient age and sex, implant type, or implant location showed no statistical predilection for an adverse event. Complications did not occur any more often at a specific time in the 9-year study period. However, 7 of 8 observed symptomatic ICHs and 3 of 4 asymptomatic ICHs were attributable to lead placement targeting the STN, which is interesting. Note that no ICH occurred upon targeting the globus pallidus internus (GPi).

Discussion

Although it is known that DBS is a relatively safe and effective procedure, actual rates of complications in the literature vary because of the differences in their definition, the relative lack of large series, and the difficulty in making comparisons across studies. Through our large series' compilation of adverse effects, we corroborated the overall low complication rate attributed to DBS surgery. Through our volume of cases, we hoped to emphasize the relative safety of the procedure to both the physician and patient communities so that more patients can benefit from its tremendous efficacy.

This series features one of the largest populations with movement disorders that has received DBS hardware from 1 primary surgeon; thus, data concerning actual risks to patient safety can be clearly interpreted. The most common side effects due to implantation in the immediate postoperative period (headache or confusion), fortunately, were transient. The most serious complication resulting from DBS device implantation is a symptomatic vascular accident due to lead insertion, which was uncommon in our series for both ICH (1.1%) and infarction (0.4%).

Our observed rate of DBS-related ICH was considerably lower than that reported in the literature (1.0%–25.0%).1,4,8,15,22,25,31,33,35,36,39,41,42,47,50,55,64 Cortical or subcortical ischemic infarction related to DBS is very rarely reported in the literature, occurring in about 1 patient per series (0.3%–0.9%).61,64 This finding could be due to the fact that ICH is not readily identifiable on routine postoperative CT imaging and that most are asymptomatic. The very low incidence of either hemorrhagic or ischemic stroke, despite a large number of procedures, could be attributed to greater surgical experience.

It is interesting to note that 1 capsular ischemic stroke (50%), both cases of acute perilesional edema (100%), and 10 (83%) of 12 ICHs were attributable to electrode placement targeting the STN. This finding does not seem to be wholly corroborated by the literature. Starr and Sillay61 reported that 4 of 8 symptomatic ICHs on postoperative imaging occurred when targeting the STN; 3 were subcortical (2 capsular, 1 thalamic). In our present series, we found that 7 of 8 symptomatic ICHs occurred when targeting the STN, and 4 of them were subcortical (1 putaminal, 3 thalamic). A possible explanation for our higher incidence is that the STN was targeted most frequently (53% of patients with implants). There are no viable anatomical arguments as to why the subthalamic area is more vulnerable to infarction than other subcortical areas. Although delayed ischemic infarction following pallidotomy has been described,3,37 its occurrence could be the result of stereotactic methodology rather than an inherent feature of DBS.

Of further interest is our finding that only 3 (11%) of the 28 observed IVHs were associated with transient postoperative confusion, and the patients in all 3 of these symptomatic cases had electrodes placed in the STN. Of this series' 28 incidences of IVH, 9 (32%) had occurred because of targeting the Vim and 19 (68%) because of targeting the STN. Twenty-five small IVHs in the occipital horn and/or atrium were incidental findings on postoperative CT and were considered to represent asymptomatic passage of either the microelectrode or the stimulating lead through the ventricle. This is probably an underestimate of the total number of ventricular wall penetrations. Elias et al.18 reported that 113 (46%) of 248 trajectories in their series violated the ventricle, with only 5 (4.4%) resulting in asymptomatic IVH. Gologorsky et al.21 noted 16 ventricular wall transgressions on postoperative MRI of 145 consecutive leads placed in the STN, with only 1 having associated IVH. The patients in 8 of these cases experienced postoperative confusion, and the authors identified a significantly greater risk (p < 0.001) of neurological compromise in such ventricular wall passes. In the present study, 3 (16%) of 19 STN trajectories causing IVH were associated with confusion, whereas 10 of the 11 patients with postoperative confusion and/or agitation had STN trajectories. Given the series total of 397 patients with STN targets, we calculated a 2.4% risk of postoperative confusion. We noted 728 consecutive leads placed in the STN; as we do not have postoperative MRI studies for every patient, it was impossible to determine total transventricular transgressions. However, postoperative CT evaluation could easily demonstrate IVH or intraventricular pneumocephalus (IVP), which would give quick proof of ventricular penetration. In this series, we observed IVP in 141 patients; 98 instances occurred in patients with a targeted STN, 38 in patients with a targeted Vim, and 5 in patients with a targeted GPi. Therefore, we calculated that at least 25% of the patients with STN trajectories in this series had penetration of the lateral ventricle; each of the 10 patients with STN targets and postoperative confusion also had IVP (9.8%). What we can infer from our study and others'18,21 is that evading transventricular passage is desirable when planning trajectories to avoid IVH and/or IVP and possible transient confusion, especially when targeting the STN. Patients and families should be appropriately counseled. However, if a ventricular trajectory is unavoidable, our experience indicates that such passage causing IVP and/or IVH produces only transient confusion if anything.

Most asymptomatic hemorrhages detailed in the literature reflect a subcortical or cortical finding on CT.12,61,64 Starr and Sillay observed that asymptomatic subcortical blood on routine postoperative MRI in 15 patients (4%) was located at the microelectrode terminus and thus was believed to be due to MER.61 We found 4 cases of asymptomatic ICH, but only 1 was near the actual electrode tract; the others were cortical. We noted 2 patients (0.3%) with intraoperative seizures, which was similar to the reported occurrence of 0.3%–2.3% of patients in large DBS series.8,12,41,61,64,66 Postoperative seizures have been reported to range from 0.9% to 9.1%,8,51,64 although we noted 3 cases (0.4%).

Vasovagal responses were the most common, overt intraoperative adverse effects (6 patients) and are well known to us and others.30,61 They are heralded by an episode of coughing soon after bur holes are made and are commonly followed by a “swoon” in blood pressure. These responses are overt manifestations of transvenous air embolism, which are especially frequent in DBS surgery because the patients are in a seated position, with the head above the heart, and are awake, spontaneously breathing and generating negative venous pressures. The surgeon must anticipate the occurrence of air embolism and wax the bone edges well and copiously flood the field with saline to prevent possible venous air embolism. Similarly, the anesthesiologist must recognize it and quickly correct the blood pressure to prevent prolonged hypotension, which would increase the risk for ischemic infarction. Intravenous lidocaine and modest doses of propofol have proven effective, in our experience, to suppress the coughing, which in itself raises intracranial pressure and increases the risk of hemorrhage.61 So long as the coughing subsides, hypotension is averted, and the patient remains neurologically intact, the procedure can continue.

The risk of infectious complications has been reported to range from 0% to 15% in various studies,5,8,11,14,22,29,31,32,36,39,41,52,58,59,62,64,66 a rate unfortunately marred by the lack of standardized definition. We report an overall incidence of 3% (23 cases). It is important to note that of these 23 wound infections among the 728 patients, only 17 occurred within the first 12 months of the original implantation, without antecedent trauma, and only 9 (1.24%) of 728 patients required a return to surgery. (Details of the presentation and management of such wound infections are detailed in Tables 2 and 3 in Fenoy and Simpson20). Thus, 1.24% represents a more reasonable rate for comparison across studies examining postoperative infection requiring reoperation and is indeed lower than, if not the lowest, of those in most studies. Wound complication avoidance seemed best correlated to a consistent surgical team with strict enforcement of sterility, a relatively quick procedure, and use of prophylactic antibiotics.20

There is sufficient discussion in the literature about redirecting malpositioned DBS leads,19,54 and our study seems to corroborate this strategy. There were 9 (1.2%) malpositioned leads with a mean latency of 1.6 years before revision, and the leads were moved a mean distance of 5.6 mm, which is similar to the distances in other series.19 Four leads were placed too deep and were simply elevated 0.5–1 mm without using a new lead or MER, at an average of 0.4 year after insertion. The poor positioning was determined based on lead asymmetry on postoperative CT and the lack of any effect, and thus was detected earlier. Since ending this study, we have adopted the use of multiple trajectories during MER to optimize lead placement, which we have found particularly useful when targeting the STN. Like other groups, we most often choose the center trajectory;53 however, electrophysiological comparison during MER allows the best choice for lead placement. We do not have an increased risk of hemorrhage with this technique, and lead misplacement has been less than 1% with it, which has led to good clinical outcomes.53

As others have observed,2 loss of system efficacy occurs over time in progressive disease, most noticeably in ET and parkinsonian tremor, even when good control is obtained without side effects. We observed this phenomenon in 19 patients in this series. Given the long study period of 9 years, we can reliably estimate that most patients who became dissatisfied with the effectiveness of their DBS system did return to the implant surgeon (R.K.S.) for revision.

Limitations of this study include the fact that we focused only on complications of the DBS surgery itself to better characterize various procedural risks and their avoidance and that we did not concentrate on the efficacy of the DBS system for individual patient motor function, for example, by using motor disease scales, but instead looked at the series of patients as a whole. However, as evidenced by patients returning for revision more than 10 years from the initial implant (before 2002), we did have long-term follow-up data on patients who became dissatisfied with the loss of system effectiveness over time.

It is possible that we underestimated the number of complications sustained over the 9-year study period. We only included in the study those patients who had returned to the neurosurgery clinic for reevaluation and did not analyze quantification of the efficacy of stimulation or the effects or side effects of programming. Nonetheless, we believe that all complications that may have been presented back to the neurologist—that is, those that may have been significant, sustained, and/or surgery related—would have been referred back to the implanting surgeon for evaluation. Some patients were indeed lost to follow-up (approximately 15% of the 728), and we could not control for this aspect; therefore, some long-term complications may be incompletely identified. Note that because this study represents a large series treated by 1 primary implanting neurosurgeon, interoperator error is avoided, and the true procedural risk can be better quantified.

Conclusions

In this large series of consecutive DBS implantation procedures for patients with a variety of movement disorders, we concluded that the risk of intraoperative adverse events is low and that complications related to the implanted hardware are also acceptably low. In fact, long-term complications are low relative to the high rate of procedural efficacy. Intraventricular trajectories should be avoided if possible, given the increased risk of subsequent transient confusion, but are not associated with a significant risk of long-term sequelae.

Disclosure

Dr. Fenoy is a consultant for, and has received clinical or research support for the described study from, Medtronic.

Author contributions to the study and manuscript preparation include the following. Conception and design: Fenoy. Acquisition of data: both authors. Analysis and interpretation of data: Fenoy. Drafting the article: Fenoy. Critically revising the article: both authors. Reviewed submitted version of manuscript: both authors. Approved the final version of the manuscript on behalf of both authors: Fenoy.

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    Benabid ALKoudsie ABenazzouz APiallat Bvan Blerkom NFraix V: Subthalamic nucleus deep brain stimulation. Lozano AMLunsford LD: Movement Disorder Surgery. Progress in Neurological Surgery 15:BaselKarger2000. 196226

  • 5

    Benabid ALKrack PPBenazzouz ALimousin PKoudsie APollak P: Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology 55:12 Suppl 6S40S442000

  • 6

    Benabid ALPollak PGervason CHoffmann DGao DMHommel M: Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337:4034061991

  • 7

    Benabid ALPollak PLouveau AHenry Sde Rougemont J: Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 50:3443461987

  • 8

    Beric AKelly PJRezai ASterio DMogilner AZonenshayn M: Complications of deep brain stimulation surgery. Stereotact Funct Neurosurg 77:73782001

  • 9

    Berk CCarr JSinden MMartzke JHoney CR: Thalamic deep brain stimulation for the treatment of tremor due to multiple sclerosis: a prospective study of tremor and quality of life. J Neurosurg 97:8158202002

  • 10

    Bittar RGHyam JNandi DWang SLiu XJoint C: Thalamotomy versus thalamic stimulation for multiple sclerosis tremor. J Clin Neurosci 12:6386422005

  • 11

    Blomstedt PHariz MI: Hardware-related complications of deep brain stimulation: a ten year experience. Acta Neurochir (Wien) 147:106110642005

  • 12

    Boviatsis EJStavrinou LCThemistocleous MKouyialis ATSakas DE: Surgical and hardware complications of deep brain stimulation. A seven-year experience and review of the literature. Acta Neurochir (Wien) 152:205320622010

  • 13

    Cif LEl Fertit HVayssiere NHemm SHardouin EGannau A: Treatment of dystonic syndromes by chronic electrical stimulation of the internal globus pallidus. J Neurosurg Sci 47:52552003

  • 14

    Constantoyannis CBerk CHoney CRMendez IBrownstone RM: Reducing hardware-related complications of deep brain stimulation. Can J Neurol Sci 32:1942002005

  • 15

    Deep-Brain Stimulation for Parkinson's Disease Study Group: Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345:9569632001

  • 16

    Denys DMantione MFigee Mvan den Munckhof PKoerselman FWestenberg H: Deep brain stimulation of the nucleus accumbens for treatment-refractory obsessive-compulsive disorder. Arch Gen Psychiatry 67:106110682010

  • 17

    Diederich NJKalteis KStamenkovic MPieri VAlesch F: Efficient internal pallidal stimulation in Gilles de la Tourette syndrome: a case report. Mov Disord 20:149614992005

  • 18

    Elias WJSansur CAFrysinger RC: Sulcal and ventricular trajectories in stereotactic surgery. Clinical article. J Neurosurg 110:2012072009

  • 19

    Ellis TMFoote KDFernandez HHSudhyadhom ARodriguez RLZeilman P: Reoperation for suboptimal outcomes after deep brain stimulation surgery. Neurosurgery 63:7547612008

  • 20

    Fenoy AJSimpson RK Jr: Management of device-related wound complications in deep brain stimulation surgery. Clinical article. J Neurosurg 116:132413322012

  • 21

    Gologorsky YBen-Haim SMoshier ELGodbold JTagliati MWeisz D: Transgressing the ventricular wall during subthalamic deep brain stimulation surgery for Parkinson's disease increases the risk of adverse neurological sequelae. Neurosurgery 69:2943002011

  • 22

    Goodman RRKim BMcClelland S IIISenatus PBWinfield LMPullman SL: Operative techniques and morbidity with subthalamic nucleus deep brain stimulation in 100 consecutive patients with advanced Parkinson's disease. J Neurol Neurosurg Psychiatry 77:12172006

  • 23

    Greenberg BDGabriëls LAMalone DA JrRezai ARFriehs GMOkun MS: Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: worldwide experience. Mol Psychiatry 15:64792010

  • 24

    Greenberg BDMalone DAFriehs GMRezai ARKubu CSMalloy PF: Three-year outcomes in deep brain stimulation for highly resistant obsessive-compulsive disorder. Neuropsychopharmacology 31:238423932006

  • 25

    Herzog JVolkmann JKrack PKopper FPötter MLorenz D: Two-year follow-up of subthalamic deep brain stimulation in Parkinson's disease. Mov Disord 18:133213372003

  • 26

    Hooper JTaylor RPentland BWhittle IR: A prospective study of thalamic deep brain stimulation for the treatment of movement disorders in multiple sclerosis. Br J Neurosurg 16:1021092002

  • 27

    Houeto JLKarachi CMallet LPillon BYelnik JMesnage V: Tourette's syndrome and deep brain stimulation. J Neurol Neurosurg Psychiatry 76:9929952005

  • 28

    Hubble JPBusenbark KLWilkinson SPenn RDLyons KKoller WC: Deep brain stimulation for essential tremor. Neurology 46:115011531996

  • 29

    Joint CNandi DParkin SGregory RAziz T: Hardware-related problems of deep brain stimulation. Mov Disord 17:Suppl 3S175S1802002

  • 30

    Kenney CSimpson RHunter COndo WAlmaguer MDavidson A: Short-term and long-term safety of deep brain stimulation in the treatment of movement disorders. J Neurosurg 106:6216252007

  • 31

    Koller WCLyons KEWilkinson SBTroster AIPahwa R: Long-term safety and efficacy of unilateral deep brain stimulation of the thalamus in essential tremor. Mov Disord 16:4644682001

  • 32

    Kondziolka DWhiting DGermanwala AOh M: Hardware-related complications after placement of thalamic deep brain stimulator systems. Stereotact Funct Neurosurg 79:2282332002

  • 33

    Krack PBatir AVan Blercom NChabardes SFraix VArdouin C: Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349:192519342003

  • 34

    Krauss JKYianni JLoher TJAziz TZ: Deep brain stimulation for dystonia. J Clin Neurophysiol 21:18302004

  • 35

    Lagrange EKrack PMoro EArdouin CVan Blercom NChabardes S: Bilateral subthalamic nucleus stimulation improves health-related quality of life in PD. Neurology 59:197619782002

  • 36

    Levy RMLamb SAdams JE: Treatment of chronic pain by deep brain stimulation: long term follow-up and review of the literature. Neurosurgery 21:8858931987

  • 37

    Lim JYDeSalles AAFBronstein JMasterman DLSaver JL: Delayed internalcapsule infarctions following radiofrequency pallidotomy. J Neurosurg 87:9559601997

  • 38

    Limousin PKrack PPollak PBenazzouz AArdouin CHoffmann D: Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 339:110511111998

  • 39

    Limousin PSpeelman JDGielen FJanssens M: Multicentre European study of thalamic stimulation in parkinsonian and essential tremor. J Neurol Neurosurg Psychiatry 66:2892961999

  • 40

    Lozano AMMayberg HSGiacobbe PHamani CCraddock RCKennedy SH: Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry 64:4614672008

  • 41

    Lyons KEKoller WCWilkinson SBPahwa R: Long term safety and efficacy of unilateral deep brain stimulation of the thalamus for parkinsonian tremor. J Neurol Neurosurg Psychiatry 71:6826842001

  • 42

    Lyons KEWilkinson SBOverman JPahwa R: Surgical and hardware complications of subthalamic stimulation: a series of 160 procedures. Neurology 63:6126162004

  • 43

    Mallet LPolosan MJaafari NBaup NWelter MLFontaine D: Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359:212121342008

  • 44

    Malone DA JrDougherty DDRezai ARCarpenter LLFriehs GMEskandar EN: Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry 65:2672752009

  • 45

    Mayberg HSLozano AMVoon VMcNeely HESeminowicz DHamani C: Deep brain stimulation for treatment-resistant depression. Neuron 45:6516602005

  • 46

    Nuttin BJGabriëls LACosyns PRMeyerson BAAndréewitch SSunaert SG: Long-term electrical capsular stimulation in patients with obsessive-compulsive disorder. Neurosurgery 52:126312742003

  • 47

    Oh MYAbosch AKim SHLang AELozano AM: Long-term hardware-related complications of deep brain stimulation. Neurosurgery 50:126812762002

  • 48

    Okun MSTagliati MPourfar MFernandez HHRodriguez RLAlterman RL: Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. Arch Neurol 62:125012552005

  • 49

    Ondo WJankovic JSchwartz KAlmaguer MSimpson RK: Unilateral thalamic deep brain stimulation for refractory essential tremor and Parkinson's disease tremor. Neurology 51:106310691998

  • 50

    Pahwa RWilkinson SSmith DLyons KMiyawaki EKoller WC: High-frequency stimulation of the globus pallidus for the treatment of Parkinson's disease. Neurology 49:2492531997

  • 51

    Pahwa RWilkinson SBOverman JLyons KE: Bilateral subthalamic stimulation in patients with Parkinson disease: long-term follow up. J Neurosurg 99:71772003

  • 52

    Pollak PFraix VKrack PMoro EMendes AChabardes S: Treatment results: Parkinson's disease. Mov Disord 17:Suppl 3S75S832002

  • 53

    Reck CMaarouf MWojtecki LGroiss SJFlorin ESturm V: Clinical outcome of subthalamic stimulation in Parkinson's disease is improved by intraoperative multiple trajectories in microlectrode recording. J Neurol Surg A Cent Eur Neurosurg 73:3773862012

  • 54

    Richardson RMOstrem JLStarr PA: Surgical repositioning of misplaced subthalamic electrodes in Parkinson's disease: location of effective and ineffective leads. Stereotact Funct Neurosurg 87:2973032009

  • 55

    Rodriguez-Oroz MCGorospe AGuridi JRamos ELinazasoro GRodriguez-Palmero M: Bilateral deep brain stimulation of the subthalamic nucleus in Parkinson's disease. Neurology 55:12 Suppl 6S45S512000

  • 56

    Rodriguez-Oroz MCObeso JALang AEHoueto JLPollak PRehncrona S: Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 128:224022492005

  • 57

    Schulder MSernas TMahalick DAdler RCook S: Thalamic stimulation in patients with multiple sclerosis. Stereotact Funct Neurosurg 72:1962011999

  • 58

    Schuurman PRBosch DABossuyt PMBonsel GJvan Someren EJde Bie RM: A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med 342:4614682000

  • 59

    Sillay KALarson PSStarr PA: Deep brain stimulator hardware-related infections: incidence and management in a large series. Neurosurgery 62:3603672008

  • 60

    Sillay KASani SStarr PA: Deep brain stimulation for medically intractable cluster headache. Neurobiol Dis 38:3613682010

  • 61

    Starr PASillay KComplication avoidance and management in deep brain stimulation surgery. Tarsy DVitek JLStarr PA: Current Clinical Neurology: Deep Brain Stimulation in Neurological and Psychiatric Disorders Totowa, NJHumana Press2008. 135150

  • 62

    Temel YAckermans LCelik HSpincemaille GHvan der Linden CWalenkamp GH: Management of hardware infections following deep brain stimulation. Acta Neurochir (Wien) 146:3553612004

  • 63

    Temel YVisser-Vandewalle V: Surgery in Tourette syndrome. Mov Disord 19:3142004

  • 64

    Umemura AJaggi JLHurtig HISiderowf ADColcher AStern MB: Deep brain stimulation for movement disorders: morbidity and mortality in 109 patients. J Neurosurg 98:7797842003

  • 65

    Vidailhet MVercueil LHoueto JLKrystkowiak PBenabid ALCornu P: Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med 352:4594672005

  • 66

    Voges JWaerzeggers YMaarouf MLehrke RKoulousakis ALenartz D: Deep-brain stimulation: long-term analysis of complications caused by hardware and surgery—experiences from a single centre. J Neurol Neurosurg Psychiatry 77:8688722006

  • 67

    Yianni JBain PGiladi NAuca MGregory RJoint C: Globus pallidus internus deep brain stimulation for dystonic conditions: a prospective audit. Mov Disord 18:4364422003

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Article Information

Address correspondence to: Albert J. Fenoy, M.D., Mischer Neuroscience Institute, Department of Neurosurgery, University of Texas Health Science Center at Houston, 6400 Fannin St., Ste. 2800, Houston, TX 77030. email: albert.j.fenoy@uth.tmc.edu.

Please include this information when citing this paper: published online November 15, 2013; DOI: 10.3171/2013.10.JNS131225.

© AANS, except where prohibited by US copyright law.

Headings

References

1

Albanese ANordera GPCaraceni TMoro E: Long-term ventralis intermedius thalamic stimulation for parkinsonian tremor. Italian Registry for Neuromodulation in Movement Disorders. Adv Neurol 80:6316341999

2

Bahgat DMagill STBerk CMcCartney SBurchiel KJ: Thalamotomy as a treatment option for tremor after ineffective deep brain stimulation. Stereotact Funct Neurosurg 91:18232013

3

Baron MSVitek JLBakay RAEGreen JKaneoke YHashimoto T: Treatment of advanced Parkinson's disease by posterior GPi pallidotomy: 1-year results of a pilot study. Ann Neurol 40:3553661996

4

Benabid ALKoudsie ABenazzouz APiallat Bvan Blerkom NFraix V: Subthalamic nucleus deep brain stimulation. Lozano AMLunsford LD: Movement Disorder Surgery. Progress in Neurological Surgery 15:BaselKarger2000. 196226

5

Benabid ALKrack PPBenazzouz ALimousin PKoudsie APollak P: Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology 55:12 Suppl 6S40S442000

6

Benabid ALPollak PGervason CHoffmann DGao DMHommel M: Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337:4034061991

7

Benabid ALPollak PLouveau AHenry Sde Rougemont J: Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol 50:3443461987

8

Beric AKelly PJRezai ASterio DMogilner AZonenshayn M: Complications of deep brain stimulation surgery. Stereotact Funct Neurosurg 77:73782001

9

Berk CCarr JSinden MMartzke JHoney CR: Thalamic deep brain stimulation for the treatment of tremor due to multiple sclerosis: a prospective study of tremor and quality of life. J Neurosurg 97:8158202002

10

Bittar RGHyam JNandi DWang SLiu XJoint C: Thalamotomy versus thalamic stimulation for multiple sclerosis tremor. J Clin Neurosci 12:6386422005

11

Blomstedt PHariz MI: Hardware-related complications of deep brain stimulation: a ten year experience. Acta Neurochir (Wien) 147:106110642005

12

Boviatsis EJStavrinou LCThemistocleous MKouyialis ATSakas DE: Surgical and hardware complications of deep brain stimulation. A seven-year experience and review of the literature. Acta Neurochir (Wien) 152:205320622010

13

Cif LEl Fertit HVayssiere NHemm SHardouin EGannau A: Treatment of dystonic syndromes by chronic electrical stimulation of the internal globus pallidus. J Neurosurg Sci 47:52552003

14

Constantoyannis CBerk CHoney CRMendez IBrownstone RM: Reducing hardware-related complications of deep brain stimulation. Can J Neurol Sci 32:1942002005

15

Deep-Brain Stimulation for Parkinson's Disease Study Group: Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345:9569632001

16

Denys DMantione MFigee Mvan den Munckhof PKoerselman FWestenberg H: Deep brain stimulation of the nucleus accumbens for treatment-refractory obsessive-compulsive disorder. Arch Gen Psychiatry 67:106110682010

17

Diederich NJKalteis KStamenkovic MPieri VAlesch F: Efficient internal pallidal stimulation in Gilles de la Tourette syndrome: a case report. Mov Disord 20:149614992005

18

Elias WJSansur CAFrysinger RC: Sulcal and ventricular trajectories in stereotactic surgery. Clinical article. J Neurosurg 110:2012072009

19

Ellis TMFoote KDFernandez HHSudhyadhom ARodriguez RLZeilman P: Reoperation for suboptimal outcomes after deep brain stimulation surgery. Neurosurgery 63:7547612008

20

Fenoy AJSimpson RK Jr: Management of device-related wound complications in deep brain stimulation surgery. Clinical article. J Neurosurg 116:132413322012

21

Gologorsky YBen-Haim SMoshier ELGodbold JTagliati MWeisz D: Transgressing the ventricular wall during subthalamic deep brain stimulation surgery for Parkinson's disease increases the risk of adverse neurological sequelae. Neurosurgery 69:2943002011

22

Goodman RRKim BMcClelland S IIISenatus PBWinfield LMPullman SL: Operative techniques and morbidity with subthalamic nucleus deep brain stimulation in 100 consecutive patients with advanced Parkinson's disease. J Neurol Neurosurg Psychiatry 77:12172006

23

Greenberg BDGabriëls LAMalone DA JrRezai ARFriehs GMOkun MS: Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: worldwide experience. Mol Psychiatry 15:64792010

24

Greenberg BDMalone DAFriehs GMRezai ARKubu CSMalloy PF: Three-year outcomes in deep brain stimulation for highly resistant obsessive-compulsive disorder. Neuropsychopharmacology 31:238423932006

25

Herzog JVolkmann JKrack PKopper FPötter MLorenz D: Two-year follow-up of subthalamic deep brain stimulation in Parkinson's disease. Mov Disord 18:133213372003

26

Hooper JTaylor RPentland BWhittle IR: A prospective study of thalamic deep brain stimulation for the treatment of movement disorders in multiple sclerosis. Br J Neurosurg 16:1021092002

27

Houeto JLKarachi CMallet LPillon BYelnik JMesnage V: Tourette's syndrome and deep brain stimulation. J Neurol Neurosurg Psychiatry 76:9929952005

28

Hubble JPBusenbark KLWilkinson SPenn RDLyons KKoller WC: Deep brain stimulation for essential tremor. Neurology 46:115011531996

29

Joint CNandi DParkin SGregory RAziz T: Hardware-related problems of deep brain stimulation. Mov Disord 17:Suppl 3S175S1802002

30

Kenney CSimpson RHunter COndo WAlmaguer MDavidson A: Short-term and long-term safety of deep brain stimulation in the treatment of movement disorders. J Neurosurg 106:6216252007

31

Koller WCLyons KEWilkinson SBTroster AIPahwa R: Long-term safety and efficacy of unilateral deep brain stimulation of the thalamus in essential tremor. Mov Disord 16:4644682001

32

Kondziolka DWhiting DGermanwala AOh M: Hardware-related complications after placement of thalamic deep brain stimulator systems. Stereotact Funct Neurosurg 79:2282332002

33

Krack PBatir AVan Blercom NChabardes SFraix VArdouin C: Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349:192519342003

34

Krauss JKYianni JLoher TJAziz TZ: Deep brain stimulation for dystonia. J Clin Neurophysiol 21:18302004

35

Lagrange EKrack PMoro EArdouin CVan Blercom NChabardes S: Bilateral subthalamic nucleus stimulation improves health-related quality of life in PD. Neurology 59:197619782002

36

Levy RMLamb SAdams JE: Treatment of chronic pain by deep brain stimulation: long term follow-up and review of the literature. Neurosurgery 21:8858931987

37

Lim JYDeSalles AAFBronstein JMasterman DLSaver JL: Delayed internalcapsule infarctions following radiofrequency pallidotomy. J Neurosurg 87:9559601997

38

Limousin PKrack PPollak PBenazzouz AArdouin CHoffmann D: Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 339:110511111998

39

Limousin PSpeelman JDGielen FJanssens M: Multicentre European study of thalamic stimulation in parkinsonian and essential tremor. J Neurol Neurosurg Psychiatry 66:2892961999

40

Lozano AMMayberg HSGiacobbe PHamani CCraddock RCKennedy SH: Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biol Psychiatry 64:4614672008

41

Lyons KEKoller WCWilkinson SBPahwa R: Long term safety and efficacy of unilateral deep brain stimulation of the thalamus for parkinsonian tremor. J Neurol Neurosurg Psychiatry 71:6826842001

42

Lyons KEWilkinson SBOverman JPahwa R: Surgical and hardware complications of subthalamic stimulation: a series of 160 procedures. Neurology 63:6126162004

43

Mallet LPolosan MJaafari NBaup NWelter MLFontaine D: Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359:212121342008

44

Malone DA JrDougherty DDRezai ARCarpenter LLFriehs GMEskandar EN: Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry 65:2672752009

45

Mayberg HSLozano AMVoon VMcNeely HESeminowicz DHamani C: Deep brain stimulation for treatment-resistant depression. Neuron 45:6516602005

46

Nuttin BJGabriëls LACosyns PRMeyerson BAAndréewitch SSunaert SG: Long-term electrical capsular stimulation in patients with obsessive-compulsive disorder. Neurosurgery 52:126312742003

47

Oh MYAbosch AKim SHLang AELozano AM: Long-term hardware-related complications of deep brain stimulation. Neurosurgery 50:126812762002

48

Okun MSTagliati MPourfar MFernandez HHRodriguez RLAlterman RL: Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. Arch Neurol 62:125012552005

49

Ondo WJankovic JSchwartz KAlmaguer MSimpson RK: Unilateral thalamic deep brain stimulation for refractory essential tremor and Parkinson's disease tremor. Neurology 51:106310691998

50

Pahwa RWilkinson SSmith DLyons KMiyawaki EKoller WC: High-frequency stimulation of the globus pallidus for the treatment of Parkinson's disease. Neurology 49:2492531997

51

Pahwa RWilkinson SBOverman JLyons KE: Bilateral subthalamic stimulation in patients with Parkinson disease: long-term follow up. J Neurosurg 99:71772003

52

Pollak PFraix VKrack PMoro EMendes AChabardes S: Treatment results: Parkinson's disease. Mov Disord 17:Suppl 3S75S832002

53

Reck CMaarouf MWojtecki LGroiss SJFlorin ESturm V: Clinical outcome of subthalamic stimulation in Parkinson's disease is improved by intraoperative multiple trajectories in microlectrode recording. J Neurol Surg A Cent Eur Neurosurg 73:3773862012

54

Richardson RMOstrem JLStarr PA: Surgical repositioning of misplaced subthalamic electrodes in Parkinson's disease: location of effective and ineffective leads. Stereotact Funct Neurosurg 87:2973032009

55

Rodriguez-Oroz MCGorospe AGuridi JRamos ELinazasoro GRodriguez-Palmero M: Bilateral deep brain stimulation of the subthalamic nucleus in Parkinson's disease. Neurology 55:12 Suppl 6S45S512000

56

Rodriguez-Oroz MCObeso JALang AEHoueto JLPollak PRehncrona S: Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 128:224022492005

57

Schulder MSernas TMahalick DAdler RCook S: Thalamic stimulation in patients with multiple sclerosis. Stereotact Funct Neurosurg 72:1962011999

58

Schuurman PRBosch DABossuyt PMBonsel GJvan Someren EJde Bie RM: A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med 342:4614682000

59

Sillay KALarson PSStarr PA: Deep brain stimulator hardware-related infections: incidence and management in a large series. Neurosurgery 62:3603672008

60

Sillay KASani SStarr PA: Deep brain stimulation for medically intractable cluster headache. Neurobiol Dis 38:3613682010

61

Starr PASillay KComplication avoidance and management in deep brain stimulation surgery. Tarsy DVitek JLStarr PA: Current Clinical Neurology: Deep Brain Stimulation in Neurological and Psychiatric Disorders Totowa, NJHumana Press2008. 135150

62

Temel YAckermans LCelik HSpincemaille GHvan der Linden CWalenkamp GH: Management of hardware infections following deep brain stimulation. Acta Neurochir (Wien) 146:3553612004

63

Temel YVisser-Vandewalle V: Surgery in Tourette syndrome. Mov Disord 19:3142004

64

Umemura AJaggi JLHurtig HISiderowf ADColcher AStern MB: Deep brain stimulation for movement disorders: morbidity and mortality in 109 patients. J Neurosurg 98:7797842003

65

Vidailhet MVercueil LHoueto JLKrystkowiak PBenabid ALCornu P: Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med 352:4594672005

66

Voges JWaerzeggers YMaarouf MLehrke RKoulousakis ALenartz D: Deep-brain stimulation: long-term analysis of complications caused by hardware and surgery—experiences from a single centre. J Neurol Neurosurg Psychiatry 77:8688722006

67

Yianni JBain PGiladi NAuca MGregory RJoint C: Globus pallidus internus deep brain stimulation for dystonic conditions: a prospective audit. Mov Disord 18:4364422003

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