Deep brain stimulation versus pallidotomy for status dystonicus: a single-center case series

View More View Less
  • 1 Neurosurgery Department, Functional Neurosurgery Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta;
  • 2 Department of Electronics, Information and Bioengineering, Polytechnic University of Milan;
  • 3 Pediatric Neuroscience Department, Child Neuropsychiatry Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta;
  • 4 Neurology Department, Movement Disorders Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta; and
  • 5 Department of Research and Clinical Development, Scientific Directorate, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy
Free access

OBJECTIVE

First-line pharmacological therapies have shown limited efficacy in status dystonicus (SD), while surgery is increasingly reported as remediable in refractory cases. In this context, there is no evidence regarding which neurosurgical approach is the safest and most effective. The aim of this study was to assess the clinical outcomes and surgery-related complications of globus pallidus internus deep brain stimulation (GPi DBS) and pallidotomy for the treatment of drug-resistant SD.

METHODS

The authors reviewed the records of patients with drug-resistant SD who had undergone GPi DBS or pallidotomy at their institution between 2003 and 2017. The severity of the dystonia was evaluated using the Barry-Albright Dystonia (BAD) Scale. Surgical procedures were performed bilaterally in all cases.

RESULTS

Fourteen patients were eligible for inclusion in the study. After surgery, the mean follow-up was 40.6 ± 30 months. DBS ended the dystonic storm in 87.5% of cases (7/8), while pallidotomy had a success rate of 83.3% (5/6). No significant differences were observed between the two techniques in terms of failure rates (risk difference DBS vs pallidotomy −0.03, 95% CI −0.36 to 0.30), SD mean resolution time (DBS 34.8 ± 19 days, pallidotomy 21.8 ± 20.2 days, p > 0.05), or BAD scores at each postoperative follow-up (p > 0.05). The long-term hardware complication rate after DBS was 37.5%, whereas no surgery-related complications were noted following pallidotomy.

CONCLUSIONS

The study data suggest that DBS and pallidotomy are equally safe and effective therapies for drug-resistant SD. The choice between the two techniques should be tailored on a case-by-case basis, depending on factors such as the etiology and evolution pattern of the underlying dystonia and the clinical conditions at the moment of SD onset. Given the limitation of the low statistical power of this study, further multicentric investigations are needed to confirm its findings.

ABBREVIATIONS AC-PC = anterior commissure–posterior commissure; BAD = Barry-Albright Dystonia; DBS = deep brain stimulation; GPi = globus pallidus internus; ITB = intrathecal baclofen; MNI = Montreal Neurological Institute; SD = status dystonicus; SP = staged pallidotomy.

OBJECTIVE

First-line pharmacological therapies have shown limited efficacy in status dystonicus (SD), while surgery is increasingly reported as remediable in refractory cases. In this context, there is no evidence regarding which neurosurgical approach is the safest and most effective. The aim of this study was to assess the clinical outcomes and surgery-related complications of globus pallidus internus deep brain stimulation (GPi DBS) and pallidotomy for the treatment of drug-resistant SD.

METHODS

The authors reviewed the records of patients with drug-resistant SD who had undergone GPi DBS or pallidotomy at their institution between 2003 and 2017. The severity of the dystonia was evaluated using the Barry-Albright Dystonia (BAD) Scale. Surgical procedures were performed bilaterally in all cases.

RESULTS

Fourteen patients were eligible for inclusion in the study. After surgery, the mean follow-up was 40.6 ± 30 months. DBS ended the dystonic storm in 87.5% of cases (7/8), while pallidotomy had a success rate of 83.3% (5/6). No significant differences were observed between the two techniques in terms of failure rates (risk difference DBS vs pallidotomy −0.03, 95% CI −0.36 to 0.30), SD mean resolution time (DBS 34.8 ± 19 days, pallidotomy 21.8 ± 20.2 days, p > 0.05), or BAD scores at each postoperative follow-up (p > 0.05). The long-term hardware complication rate after DBS was 37.5%, whereas no surgery-related complications were noted following pallidotomy.

CONCLUSIONS

The study data suggest that DBS and pallidotomy are equally safe and effective therapies for drug-resistant SD. The choice between the two techniques should be tailored on a case-by-case basis, depending on factors such as the etiology and evolution pattern of the underlying dystonia and the clinical conditions at the moment of SD onset. Given the limitation of the low statistical power of this study, further multicentric investigations are needed to confirm its findings.

ABBREVIATIONS AC-PC = anterior commissure–posterior commissure; BAD = Barry-Albright Dystonia; DBS = deep brain stimulation; GPi = globus pallidus internus; ITB = intrathecal baclofen; MNI = Montreal Neurological Institute; SD = status dystonicus; SP = staged pallidotomy.

In Brief

This is the first paper comparing the results of deep brain stimulation and pallidotomy for the treatment of status dystonicus in a single-center case series. The two treatments seem to be equally effective and not mutually exclusive. Other important factors should be considered in the treatment algorithms for status dystonicus, such as etiology and evolution of the underlying dystonia and clinical conditions at the moment of onset.

Status dystonicus (SD) is a rare but life-threatening movement disorder emergency characterized by severe episodes of generalized or focal dystonia potentially accompanied by other hyperkinetic movements that have necessitated urgent hospitalization, regardless of the patient’s neurological condition at baseline.24,26,29 Also known as “dystonic storm,” SD is frequently reported in children and can be triggered by several precipitating factors, such as infections, drug withdrawal, and surgical procedures.1,25 Early recognition and intervention are paramount in cases of SD, as its persistence often leads to serious sequelae, such as rhabdomyolysis and respiratory failure, with consequent high mortality rates (10%–15%).1,27

There is still no consensus on the optimal strategy for treating SD. Antidystonic drugs and profound sedation usually represent the first therapeutic options. Unfortunately, their efficacy is limited and surgical alternatives are needed in the majority of cases.15 An increasing number of clinical studies have shown the effectiveness of deep brain stimulation (DBS) of the globus pallidus internus (GPi) in cases of drug-resistant SD.5,6,23,32,37,42,44,45 However, one shortcoming of DBS is the nonnegligible risk of hardware-related complications in the pediatric dystonia population.28 In addition, several reports have described the onset of severe or fatal SD as a consequence of a DBS depleted battery or lead dislocation.34–36 Also, DBS may not be effective in resolving SD. In a recent study by Nerrant et al., 2 patients died as a direct consequence of refractory SD, despite attempts at subsequent rescue DBS therapy.32 In this context, ablative procedures such as pallidotomy, which does not require any hardware implantation, are likely to be of benefit. However, their effectiveness for SD has been reported in only sporadic case reports and small case series.8,9,14,17,28,33

The primary aim of the present study was to compare the clinical outcomes and surgery-related complication rates of pallidotomy and GPi DBS for the treatment of SD in a single-center cohort. Potential correlations among SD characteristics, type of neurosurgical treatment, and outcomes were then analyzed and discussed.

Methods

Study Design and Data Collection

The records of patients with drug-resistant SD who had undergone GPi DBS or pallidotomy at our institution between 2003 and 2017 were reviewed. All the surgical procedures were performed in accordance with the 1964 Declaration of Helsinki and its later amendments. Patients or their relatives provided written informed consent in all cases.

Inclusion criteria for drug-resistant SD included patients of any age with abrupt exacerbation of the baseline dystonic phenomenology, unresponsiveness to at least 2 antidystonic medications, urgent intensive care unit (ICU) admission with profound sedation, and at least one of the Manji diagnostic criteria (Table 1).26 Discharge from the ICU was chosen as the event indicative of the end of the dystonic storm. The following data were collected: patient demographics, baseline dystonia characteristics (age, sex, dystonia etiology, age at onset of dystonia, disease duration before SD, trigger factors), and hospital course (medications, time between SD onset and surgery, type of surgery, SD resolution or persistence, complications). Dystonia severity was evaluated according to the Barry-Albright Dystonia (BAD) Scale at the last available visit before onset of the dystonic storm (baseline BAD), during the storm (SD BAD), 1 month after surgery (postoperative BAD), and at the last available follow-up (last BAD).39 Clinical outcomes at 1 month after surgery were categorized according to a modified Ben-Haim scale (Table 1).6 During telephone interviews conducted in June 2018, all caregivers rated their experience with long-term caregiving and patient comfort levels after surgery by using a subjective rating scale (Table 1).

TABLE 1.

Various scales used in the study

Manji diagnostic criteria
 Bulbar weakness compromising upper airway patency
 Physical exhaustion & pain
 Metabolic imbalances such as myoglobinuria
 Renal or respiratory failure
Modified Ben-Haim scale
 1, death
 2, SD resolution w/ deterioration from baseline dystonia (BAD increase >25%)
 3, SD resolution but w/ unchanged baseline dystonia (BAD variation btwn ±25%)
 4, SD resolution w/ slight improvement of baseline dystonia (BAD reduction >25% but <50%)
 5, SD resolution w/ great improvement of baseline dystonia (BAD reduction ≥50%)
Subjective caregiver benefit scale
 −1, worse than expected
 0, no benefit
 1, minimal benefit
 2, good benefit, as expected
 3, excellent benefit, more than expected

Surgical Procedures

GPi DBS

GPi DBS was usually considered the first surgical option in patients with a good nutritional state and progressive baseline dystonia course. Surgery was always performed under general anesthesia, bilaterally, and under stereotactic conditions with the Leksell (Elekta Inc.) or Maranello (Eidos22) frame. Our routine surgical procedure has been extensively discussed elsewhere.16 GPi coordinates related to the anterior commissure–posterior commissure (AC-PC) midpoint were set at X (±19), Y (+2), and Z (−6) in all cases.

Conventional and Staged Pallidotomy

Conventional pallidotomy was routinely performed under general anesthesia and in stereotactic conditions for the following indications: 1) previous DBS failure, 2) patients with a high risk for DBS hardware-related complications (e.g., those having a low body weight, severe malnutrition, or poor skin condition), and 3) patients who were not usually considered good DBS candidates at our institution because of poor expected responsiveness to stimulation (severe acquired dystonia characterized by a long, static disease course and by the absence of a period of normal development). Based on previous studies of pallidotomies, ablation was performed in the midportion of the GPi, which is still part of the posteroventral GPi.10,28 This targeting technique, in which the target was always defined using direct visualization on preoperative images given the frequent anatomy distortion in these patients, allows for immediate benefit for dystonic symptoms, without preventing patients from receiving further gain from subsequent DBS of the most posterior part of the GPi.28

The radiofrequency monopolar lesions were always created bilaterally at the target, 2 mm above it, and 2 mm below it, through a CSK-TC20 electrode (Cosman Medical; 4-mm exposed uninsulated tip, 1 mm in diameter) with a 60-second train of 40 V through the radiofrequency generator, reaching a temperature of 70°C. The heat generated during the lesioning process was usually monitored, with a thermistor recording the temperature at the probe tip. Microrecording and macrostimulation were performed under electromyography monitoring to exclude involvement of pyramidal fibers of the internal capsule by the lesioning.

More recently, bilateral staged pallidotomy (SP) has been gradually introduced at our institution. Quadripolar DBS leads (3389, Medtronic) are used to generate the ablation by connecting their extracranial termination to a radiofrequency generator (RFG-1A, Cosman Medical).4,18 SP can be used de novo, as a salvage treatment after previous DBS failure, or prior to lead removal because of DBS hardware infection. Its main advantages include the possibility of checking the definitive electrode location prior to lesioning and monitoring ablation evolution over time.18 The lesion is usually created in a bipolar fashion between lead central contacts 2 days after surgery with a 40-second train of 40 V. If needed, the ablation can be easily repeated in the following days. Once the pallidotomy effect is achieved, leads can be left in place (should the patient need DBS in the future) or removed.

Postoperative Lead and Lesion Localization

In the case of DBS or SP, the postoperative CT scan was merged with the preoperative MR image (Framelink, Medtronic) to assess the definitive lead location in the AC-PC space. Final coordinates were identified as the center of the beam-hardening artifact representing the deepest contact (contact 0). The position in the Montreal Neurological Institute (MNI) space of all DBS leads was also detected and reconstructed three-dimensionally by using the Lead-DBS MATLAB toolbox.20

In cases of conventional pallidotomy, lesion location was evaluated in the AC-PC space by merging the postoperative MR image (usually obtained within 1 week after surgery) with the preoperative volumetric CT scan. The center of the lesion was identified in the axial slice in which the lesion had the largest diameter.

Statistical Analysis

Descriptive statistics were provided as percentages for dichotomous data and the mean ± standard deviation for continuous data. Preoperative differences between patients who had undergone DBS and those who had been treated with pallidotomy were evaluated using unpaired t-tests. Differences between SD BAD and postoperative BAD scores were assessed using paired t-tests. Repeated measures ANOVA was used to compare postoperative BAD scores between DBS and pallidotomy groups. Pearson correlation coefficients were used to assess significant associations between the effect of surgery (in terms of the difference between SD BAD score and postoperative BAD score) and baseline dystonia duration or time spent in SD before the final surgery. Statistical analyses were performed using Stata statistical software (release 15, 2017, StataCorp LLC). Statistical significance was set at p ≤ 0.05.

Results

Patient Demographics and Baseline Characteristics

Demographic data and baseline dystonia characteristics are shown in Table 2. Fourteen patients fulfilled the inclusion criteria for the study. The cohort included 12 pediatric and 2 adult patients. Three patients (21.4%) experienced a prior SD episode, which had been successfully managed with antidystonic drugs. Dystonia etiology was identified in all but 1 case.

TABLE 2.

Patient demographics, baseline dystonia characteristics, and initial drug treatment for SD

Case No.SexAge at Diagnosis (yrs)Dystonia EtiologyDystonia CourseBaseline BAD ScoreAge at SD Onset (yrs)Trigger FactorsSD PhenomenologyInitial Pharmacological Treatment
1F2PKAN classicProgressive2810ITB pump infectionTonicMidazolam, propofol, tetrabenazine, trihexyphenidyl
2F4Post-infectiveStatic247Bacterial infectionTonicMidazolam, propofol, tetrabenazine, oral baclofen
3*M1UnknownSlow progressive229Pyrexia of unknown etiologyPhasicPhenobarbital, oral baclofen, trihexyphenidyl, quetiapine, midazolam
4*F1GNAO1Progressive196Dental infectionPhasicMidazolam, tetrabenazine, oral baclofen
5M2PKAN atypicalStatic228ITB pump malfunctionTonicMidazolam, propofol, tetrabenazine
6F3CPStatic2010Viral infectionPhasicMidazolam, propofol, tetrabenazine, oral baclofen
7M6CPStatic2214NoneTonicMidazolam, propofol, trihexyphenidyl
8M11PKAN classicProgressive1213NoneTonicMidazolam, propofol, trihexyphenidyl
9M4PKAN classicProgressive229NoneTonicMidazolam, propofol, tetrabenazine, oral baclofen
10F2PKAN classicProgressive2110NoneTonicMidazolam, propofol, tetrabenazine
11F16PKAN classicProgressive2224BacterialTonicMidazolam, propofol, tetrabenazine
12F1CPStatic2519NonePhasicMidazolam, propofol, tetrabenazine
13*F1GNAO1Progressive2410NonePhasicMidazolam, propofol, trihexyphenidyl
14M2CPStatic2216NoneTonicMidazolam, propofol, thiopentone, tetrabenazine, trihexyphenidyl

CP = cerebral palsy; GNAO1 = guanine nucleotide-binding protein, alpha-activating activity polypeptide O; PKAN = pantothenate kinase-associated neurodegeneration.

These 3 patients had a previous SD, managed with antidystonic drugs and sedation.

These 2 patients died during the follow-up due to complications unrelated to their baseline dystonia.

All patients had severe generalized dystonia and were on oral antidystonic treatment prior to the onset of SD; 4 of them also had an intrathecal baclofen (ITB) pump. The mean baseline BAD score before the onset of SD was 21.8 ± 3.6 points.

Characteristics of the Dystonic Storms

The mean age at SD onset was 11.8 ± 5 years. The temporal course of SD onset ranged from days to weeks in 85.7% (12/14) of patients, whereas slow worsening of dystonia over a few months was documented in 2 subjects, one affected by a GNAO1 encephalopathy and one suffering from a dyskinetic cerebral palsy (2/14 [14.3%]). Triggering factors were identified in 50% (7/14) of cases (Table 2). Among those patients with an ITB pump, 2 developed SD as a consequence of ITB-related adverse events (1 malfunction and 1 infection), while ITB malfunction was ruled out in the remaining cases.

The mean SD duration was 74.6 ± 55 days. The mean SD BAD score was 31.2 ± 0.8 points. No significant preoperative differences were found between patients who underwent DBS and those who were treated with pallidotomy in terms of age at dystonia onset, age at SD onset, duration of dystonia, time between SD onset and surgery, baseline BAD scores, and SD BAD scores (all p > 0.05).

Clinical Outcomes

The mean dystonia duration before surgery was 7.8 ± 4.1 years, while the mean time from SD onset to surgery was 30.3 ± 20.3 days. After surgery, the total BAD scores were significantly improved both at 1 month (mean postoperative BAD score 24.9 ± 6.7, p < 0.01) and at the last follow-up (mean last BAD score 28 ± 4.8, p < 0.01; mean follow-up 40.6 ± 30 months) as compared to the total SD BAD scores (mean 31.3 ± 0.8; Table 3). The effect of surgery was not correlated with baseline dystonia duration (r = 0.17, p > 0.05) or time spent in SD before the final surgery (r = 0.l9, p > 0.05). Overall clinical outcomes categorized according to the modified Ben-Haim scale at the 1-month follow-up and the subjective benefit reported by caregivers are shown in Fig. 1. No further SD recurrence was noted during follow-up. Mortality as a direct consequence of an SD episode was 7.1% (1/14), while 2 other patients (2/14 [14.3%]) died during follow-up due to complications indirectly related to the underlying dystonia. They both suffered from a severe form of pneumonia evolving into sepsis.

TABLE 3.

Surgery for SD and outcomes

Case No.Type of SurgerySD BAD ScorePostop BAD ScoreLast BAD ScoreTime From SD Onset to Surgery (days)SD Resolution After Surgery (days)Modified Ben-Haim ScaleCaregiver Benefit Assessment ScaleComplicationsFU (mos)
1Pallidotomy3232NA60Death after 35 days1−1NANA
2Pallidotomy32293143122None12
3Staged pallidotomy301415363543None12
4DBS322121152432None12
5Pallidotomy31303031520None12
6DBS322222153332Lead fracture63
7DBS312525403033Lead fracture19
8DBS3292415243None84
9DBS312828151522None36
10DBS30282894022Lead fracture42
11DBS323025636022None28
12*Pallidotomy312428605030None38
13DBS, pallidotomy322828306033None180
14*Pallidotomy30252821830None30

NA = not applicable.

Two patients died during the follow-up due to complications unrelated to their baseline dystonia.

FIG. 1.
FIG. 1.

A: Overall motor outcomes at the 1-month follow-up after surgery, categorized according to the modified Ben-Haim scale. B: A subjective assessment of the surgical procedures was administered to all caregivers during a telephone interview in June 2018 to capture potential easing of caregiving and increased patient comfort levels after surgery in the long term. Among the patients experiencing a good or excellent benefit (red and yellow), 70% underwent DBS surgery. Figure is available in color online only.

Deep Brain Stimulation

Bilateral GPi DBS was performed in 8 patients, ending the storm in 87.5% (7/8) of cases (Table 3). The mean SD resolution time among these patients was 34.8 ± 19 days. Stimulation was usually started 2 days after surgery, set at the following parameters: double monopolar symmetric stimulation (case+, 1−, 2−), 2.5–4 V, 60–90 μsec, and 130–185 Hz.

After 6 months, 1 patient showed a progressive slight dystonia worsening. After a readjustment of stimulation parameters, the patient’s condition immediately improved, and dystonia returned to its baseline characteristics in a few days. In another patient, GPi DBS provided no benefit at all. She then underwent rescue conventional pallidotomy with SD regression.

No immediate postoperative adverse events were observed following DBS surgery, but there were a few hardware-related complications during the long-term follow-up. Three patients (3/8 [37.5%]) had fatigue fracture of the right extracranial lead. They showed acute worsening of the baseline dystonia and consequently underwent urgent lead replacement.

Pallidotomy

Pallidotomy was the first surgical option in 6 patients (Table 3). Of these, 5 underwent conventional bilateral pallidotomy and 1 had bilateral SP. Pallidotomy interrupted SD in 5 patients (5/6 [83.3%]) and was ineffective in 1 patient who eventually died after 1 month. Resolution of the storm among these patients took a mean 21.8 ± 20.2 days. No further neurological deficits or complications were observed after the surgeries. In addition, 1 patient successfully underwent pallidotomy as a last-resort treatment after GPi DBS failure.

DBS Versus Pallidotomy

Repeated measures ANOVA showed no significant difference in BAD scores between the DBS and pallidotomy groups (p for interaction term > 0.05; Fig. 2). Similarly, no significant differences were observed between the two techniques in terms of failure rates (risk difference DBS vs pallidotomy −0.03, 95% CI −0.36 to 0.30) or in terms of SD resolution time after surgery (DBS 34.8 ± 19 days, pallidotomy 21.8 ± 20.2 days, p > 0.05)

FIG. 2.
FIG. 2.

Repeated measures ANOVA of BAD scores (y-axis) showing no significant differences between the surgical procedures (p > 0.05). fu = follow-up; pre = preoperatively; post = postoperatively. Figure is available in color online only.

Postoperative Lead and Lesion Localization

The mean stereotactic atlas coordinates in relation to the midcommissural point confirmed that lesions were usually located slightly anteromedially as compared to the lead location (Fig. 3). All 16 DBS leads were successfully localized in the MNI space, and all cases had at least 1 contact within the border of the posteroventral GPi.

FIG. 3.
FIG. 3.

Upper: Postoperative DBS lead locations in the MNI space. GPi, green; globus pallidus externus, blue; subthalamic nucleus, orange; red nucleus, red. Lower: DBS lead and pallidal lesion localizations in the AC-PC space. Figure is available in color online only.

Discussion

Review of the Literature

As far as we know, this is the first single-center evaluation to report both GPi DBS and pallidotomy outcomes for the treatment of drug-resistant SD. To date, 30 GPi DBS and 8 ablative pallidotomy procedures have been separately described as isolated case reports, with varying success rates (Table 4).2–4,6,7,11,14,19,21–23,28,30,34,40,41,44,45

TABLE 4.

Literature review on DBS and pallidotomy for the treatment of SD

Authors & YearProcedureNo. of PatientsType of DystoniaAge at Dystonia OnsetTrigger FactorsAge at SDTime to SurgeryOutcome ReportedComplications From Surgery
Coubes et al., 1999DBS1GD DYT1−3 yrsNone8 yrs2 mosSD resolution after 6 wksNone
Angelini et al., 2000DBS1NS5 mosNone13 yrsNRExtubation w/in 1 wk, pharmacological therapy discontinued after 3 wks, walking independently after 7 mosNone
Teive et al., 2005DBS1Primary craniocervical dystoniaNS“Stress”NRNRImprovement above baselineMild lt hemiparesis
Zorzi et al., 2005DBS3GD DYT1−1.6 yrsNone8.2 yrs4 mosSedation discontinued at 3 mos, improvedIPG turned off inexplicably
GD DYT1−3 yrsNone10.6 yrs6 mosSD resolution in 2 days, improvementIPG turned off inexplicably
Idiopathic encephalopathy6 mosUrinary infection14.2 yrs2 mosSD resolution in 1 wk, no improvementNone
Borggraefe et al., 2008DBS1DYT1+7 yrsNone14 mosNSImprovement above baseline after 4 mosNone
Elkay et al., 2009DBS1Batten’s disease17 yrsNone19 yrsNRImprovement after unsuccessful pallidotomyNone
Jech et al., 2009DBS1GD DYT1−8 yrsNone11 yrs2 wksExtubated after 45 days, sedation for 70 days, marked improvementNone
Martinez-Torres et al., 2009DBS1GD DYT3+33 yrsNone reported34 yrsNR“Immediate improvement after surgery”None
Timmerman et al., 2010DBS2PKAN4 yrsNone reported14 yrs“Emergency DBS”Death after 6 wks from surgeryDeath
PKAN8 yrsDBS surgery17 yrs1 day after DBS surgerySD resolution after “several days of stimulation” w/ improvement above baselineOpen femur fracture from SD
Apetauerova et al., 2010DBS2CP“Early age”MetoclopramideNS4 mosExtubation w/in 1 day, unchanged from baselineNone
CPNSSurgery (omentectomy)NS2 mosExtubation w/in 2 days, unchanged from baselineNone
Grandas et al., 2011DBS1PKAN13 yrsNone reported19 yrs3 daysImprovement above baseline after a few daysNone
Kovacs et al., 2011DBS1Tardive dystonia17 yrsNone reported18 yrs1 moImprovement above baseline after a few days of stimulationNone
Walcott et al., 2012DBS3CPNSSurgical infection14 yrs1 moExtubation after a few days, improved at the 1-yr FULt lower contacts not functioning properly
GDNSNone reported9 yrs4 mosDischarge home 6 wks after surgeryIPG infection w/ system explantation on the rt
CPNSPulmonary illness9 yrs2 mosImprovement at the 3-mo FUNone
Ben-Haim et al., 2016DBS5GD DYT1+6 yrsAbdominal surgery13 yrs14 daysComplete recoveryNone
GD DYT1+8 yrsDBS infection11 yrs2 daysImproved from baselinePostop pneumonia
GD DYT1+7 yrsDBS surgery8 yrs5 daysImproved from baselineNone
GD DYT1+7 yrsDBS lead fracture15 yrs4 daysReturn to baselineNone
GD DYT1+8 yrsAbdominal distress11 yrs131 daysImproved from baselineNone
Oterdoom et al., 2018DBS1GD DYT6+3.5 yrsConstipation11 yrs (previous GPi DBS 15 mos before)4 wks (lead reposition)Improvement after 1 wkNone
Lobato-Polo et al., 2018DBS5Idiopathic41 yrsNone41 yrs17 daysImprovement after 3 daysDelirium
CP1 moRespiratory infection8 yrs8 daysImprovement after 21 daysNone
Idiopathic41 yrsMedication tolerance41 yrs36 daysImprovement after 1 dayBehavioral changes
CP1 yrDisplacement of DBS lead10 yrs3 daysImprovement after 7 daysInfection (no hardware removal)
GCH1 mutation7 yrsMedication change32 ys6 days (STN DBS)Improvement after 1 dayNone
Teive et al., 2005Pallidotomy1CPNRNone8 yrsNRExcellentNone
Balas et al., 2006Pallidotomy1HSD5 yrsNone10 yrsNR“Immediate postoperative improvement” after bilateral pallido-thalamotomyNone
Elkay et al., 2009Pallidotomy2Batten’s disease9 yrsNone21 yrsNRMarked improvement after 10 daysNone
Batten’s disease17 yrsNone19 yrsNRImprovement for only 3 wks, requiring subsequent GPi DBSNone
Marras et al., 2014Pallidotomy4Chromosomopathy3 yrsMononucleosis13 yrs2 mosSD resolution after 40 daysNone
Encephalopathy1 moFever17 yrs14 daysSD resolution w/in 1 moNone
Idiopathic bilateral striatal necrosis4 mosEnteritis5 yrs50 daysSD resolution after 3 wksNone
CP8 mosNone10 yrs60 daysSD resolution after 2 mosNone

GD = generalized dystonia; HSD = Hallervorden-Spatz disease; IPG = internal pulse generator; NR = not reported; NS = not specified; STN = subthalamic nucleus.

Ablative procedures, such as thalamotomy and pallidotomy, were the first surgical treatments used in SD patients.37 In 1998, Manji et al. performed for the first time 2-stage ventrolateral thalamic nuclei lesioning in a 9-year-old boy with severe SD and a unilateral left thalamotomy in a 38-year-old woman affected by a prevalent right-sided severe postencephalitic hemidystonia.26 In subsequent years, pallidotomy was found to be effective in the treatment of L-dopa–induced dyskinesia in patients with advanced Parkinson’s disease; thus, the main target of stereotactic ablative procedures shifted from the thalamus to the GPi in dystonic patients as well.9 Currently, a larger study on SD and pallidotomy has been reported by Marras et al., who described the indications, surgical strategy, and outcome of bilateral pallidotomy in 4 pediatric patients with secondary dystonia who developed sudden refractory SD.28 In their series, pallidotomy was performed in the midportion of the GPi (X: 14–18, Y: 3–5, Z: −2) with progressive improvement of dystonia in all patients without any observed recurrence at a mean follow-up of 18.2 months. No postoperative complications were noted.

As with ablative surgical methods, the number of SD patients treated with GPi DBS is still limited. The first instance of bilateral GPi stimulation for SD was reported in 1996 by Philippe Coubes, who knew of the great efficacy of Laitinen’s posteroventral pallidotomy for parkinsonian dyskinesias and thus proposed GPi stimulation as a compassionate intervention in an 8-year-old girl who had been in a complete refractory dystonic storm for several weeks.11 The striking result obtained by Coubes caused him to apply GPi DBS in 7 patients with DYT1 generalized dystonia, opening the way for the surgical treatment of many other types of dystonia.12 In 2016, a review by Ben-Haim et al. found that of the 28 SD patients described in the literature who had been treated with DBS or ablative surgery, 26 had cessation of their dystonic crisis with a return to baseline function and, in most cases, clinical improvement.6 Since then, a growing number of reports describing the effectiveness of DBS in cases of SD have been published because of the increased availability of the technique worldwide along with its great popularity for the treatment of other movement disorders, such as Parkinson disease and tremor (Table 4). Recently, Nerrant and colleagues retrospectively analyzed a cohort of 328 dystonia patients who had been seen over a period of 20 years.32 Twenty-five of these patients underwent de novo DBS to control an ongoing SD episode, with resolution in 92% of them, whereas 9 patients underwent subsequent lead implantation as rescue therapy while already benefiting from DBS, with a success rate of 91.3%. Mortality as a direct consequence of an SD episode that was refractory to medical treatment and DBS was 10%.

Overall Efficacy of Surgery for the Treatment of Drug-Resistant SD

In our series, the per-procedure success rate of surgery (86.7% [13/15] success rate; 1 patient required salvage pallidotomy after DBS failure) was in line with rates previously reported in the literature on the subject.6,15 In addition, the positive effect of surgery was independent of the baseline dystonia duration and the time spent in SD before surgical intervention. In contrast with previously published experiences, only 2 patients in our study showed mild improvement in their baseline dystonic conditions, with dystonic conditions remaining unchanged or even worsening in the other patients (Fig. 1).6,23 This difference in results may be due, in part, to the great heterogeneity of baseline dystonia traits or SD characteristics among studies. Follow-ups are also highly variable among studies, and only a few papers have reported long-term motor outcomes. Recently, Elkaim et al. showed that the grade of motor improvement is not very predictable after surgery for SD.13 Patients who had undergone surgical intervention, in fact, showed improvement compared to pre-SD baseline in 65.5% of cases, with the other cases (34.5%) remaining unchanged or even worsening. These data are not negligible, especially if they are compared to the outstanding long-term surgical motor outcomes reported for the general dystonic population.31

In our opinion, SD should be considered more than a transient event overlapping the baseline dystonia. It may be indicative of an evolution of the disease causing high instability of the basal ganglia–cortical network, which is hard to revert.

Given our data, DBS or pallidotomy seems to be effective in down-regulating this instability in the acute phase of SD but with poor results in the long term. Why this happens is difficult to explain. In our opinion, this question may find an exhaustive answer only after collecting a large amount of electrophysiological data on SD, allowing those in the field to better understand the complex and still unknown pathophysiology of the disease. In order to do this, however, considering the rarity of the disease, international cooperation among multiple centers is of paramount importance.

DBS Versus Pallidotomy

Bilateral GPi DBS and pallidotomy were successful in 87.5% and 83.3% of SD cases, respectively. In terms of postoperative BAD values, no significant differences were found between the two techniques. Pallidotomy resulted in a shorter time to SD resolution than that following DBS (21.8 ± 20.2 and 34.8 ± 19 days, respectively); however, the difference between the two techniques in this regard was not significant, although it nevertheless seems reasonable. DBS is, in fact, a pure neuromodulation technique that reestablishes neuronal networks’ electrical stability over time. It is well known, for instance, that the effect of DBS in uncomplicated dystonia usually takes weeks to months to appear. Conversely, pallidotomy may work by anatomically interrupting an unregulated and disruptive circuit, allowing the remaining structures and circuits to function more properly in a shorter time.38,43

Although both procedures were extremely safe in terms of intraoperative complications and postoperative neurological deficits, DBS was associated with an increased number of long-term hardware failures (37.5%). This finding is not surprising given that pallidotomy does not require implantation of permanent devices.

With regard to the postoperative location of pallidal lesions, our data suggest that lesioning a slightly more anteromedial portion of the GPi is equally safe, feasible, and effective as the ablation of the classic posteroventral DBS target. In our opinion, these data may be of some utility in the future considering that new, minimally invasive lesioning techniques, such as focused ultrasound, could soon be applied to dystonia and SD as well.

DBS showed greater subjective benefit among caregivers than pallidotomy (good and excellent benefit with DBS 70%, vs 30% with pallidotomy). However, these data should be considered with caution given that 3 deaths occurred in the pallidotomy group (1 directly related to SD and the other 2 from a severe form of pneumonia evolving into sepsis). In particular, the 2 deaths occurring during the follow-up period may have introduced an important bias influencing the final caregivers’ evaluations. In addition, pallidotomy, as a permanent lesional procedure, may have raised unrealistic caregiver expectations. Finally, it is not possible to exclude the fact that the anteromedial location of the lesions generated adverse events that the motor scale score and clinical evaluations were unable to detect. All of these points are purely speculative, however, and the low numbers of our sample do not allow for any definitive conclusions in this respect.

Study Limitations

This study has several limitations because of the unusual features of the pathological condition considered. First, the retrospective and nonrandomized design of the study may have introduced several forms of bias. More severe forms of SD may have been treated only with pallidotomy rather than DBS, thus hampering pallidotomy outcomes. In addition, the two populations are not strictly comparable because the target chosen for DBS is different from the one used for pallidotomy. Pharmacological therapies attempted before surgery were quite heterogeneous, and this could have strongly influenced the outcome after DBS and pallidotomy. Another important limitation of the study is the small sample size, which did not allow us to reach adequate statistical power. This could have definitely biased our statistical analysis.

Conclusions

SD is a rare, life-threatening emergency that can complicate a wide range of pediatric and adult dystonias. In this context, both GPi DBS and pallidotomy are effective, safe, and life-saving therapies and should be proposed early in the treatment of SD. The choice between the two procedures, in our opinion, should be tailored on a case-by-case basis, depending on factors such as etiology and evolution pattern of the underlying dystonia and clinical conditions at the moment of SD onset.

Acknowledgments

We thank all the patients and their families who participated in this study.

Disclosures

Dr. Levi is a medical advisor at Newronika S.R.L. (neurostimulator manufacturer), but this activity is not relevant to the paper.

Author Contributions

Conception and design: Levi. Acquisition of data: Levi, Zorzi. Analysis and interpretation of data: Levi, Zorzi. Drafting the article: Levi. Critically revising the article: Zorzi, Messina, Romito, Tramacere, Dones, Nardocci, Franzini. Approved the final version of the manuscript on behalf of all authors: Levi. Statistical analysis: Tramacere.

References

  • 1

    Allen NM, Lin JP, Lynch T, King MD: Status dystonicus: a practice guide. Dev Med Child Neurol 56:105112, 2014

  • 2

    Angelini L, Nardocci N, Estienne M, Conti C, Dones I, Broggi G: Life-threatening dystonia-dyskinesias in a child: successful treatment with bilateral pallidal stimulation. Mov Disord 15:10101012, 2000

    • Search Google Scholar
    • Export Citation
  • 3

    Apetauerova D, Schirmer CM, Shils JL, Zani J, Arle JE: Successful bilateral deep brain stimulation of the globus pallidus internus for persistent status dystonicus and generalized chorea. J Neurosurg 113:634638, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    Balas I, Kovacs N, Hollody K: Staged bilateral stereotactic pallidothalamotomy for life-threatening dystonia in a child with Hallervorden-Spatz disease. Mov Disord 21:8285, 2006

    • Search Google Scholar
    • Export Citation
  • 5

    Barbosa BJAP, Carra RB, Duarte KP, Godinho F, de Andrade DC, Teixeira MJ, : Bilateral subthalamic nucleus stimulation in refractory status dystonicus. J Neurol Sci 388:159161, 2018

    • Search Google Scholar
    • Export Citation
  • 6

    Ben-Haim S, Flatow V, Cheung T, Cho C, Tagliati M, Alterman RL: Deep brain stimulation for status dystonicus: a case series and review of the literature. Stereotact Funct Neurosurg 94:207215, 2016

    • Search Google Scholar
    • Export Citation
  • 7

    Borggraefe I, Boetzel K, Boehmer J, Berweck S, Mueller-Felber W, Mueller K, : Return to participation – significant improvement after bilateral pallidal stimulation in rapidly progressive DYT-1 dystonia. Neuropediatrics 39:239242, 2008

    • Search Google Scholar
    • Export Citation
  • 8

    Cif L, Coubes P: Historical developments in children’s deep brain stimulation. Eur J Paediatr Neurol 21:109117, 2017

  • 9

    Cif L, Hariz M: Seventy years of pallidotomy for movement disorders. Mov Disord 32:972982, 2017 (Erratum in Mov Disord 32:1498, 2017)

    • Search Google Scholar
    • Export Citation
  • 10

    Cohn MC, Hudgins PA, Sheppard SK, Starr PA, Bakay RA: Pre- and postoperative MR evaluation of stereotactic pallidotomy. AJNR Am J Neuroradiol 19:10751080, 1998

    • Search Google Scholar
    • Export Citation
  • 11

    Coubes P, Echenne B, Roubertie A, Vayssière N, Tuffery S, Humbertclaude V, : [Treatment of early-onset generalized dystonia by chronic bilateral stimulation of the internal globus pallidus. Apropos of a case.] Neurochirurgie 45:139144, 1999 (French)

    • Search Google Scholar
    • Export Citation
  • 12

    Coubes P, Roubertie A, Vayssiere N, Hemm S, Echenne B: Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus. Lancet 355:22202221, 2000

    • Search Google Scholar
    • Export Citation
  • 13

    Elkaim LM, De Vloo P, Kalia SK, Lozano AM, Ibrahim GM: Deep brain stimulation for childhood dystonia: current evidence and emerging practice. Expert Rev Neurother 18:773784, 2018

    • Search Google Scholar
    • Export Citation
  • 14

    Elkay M, Silver K, Penn RD, Dalvi A: Dystonic storm due to Batten’s disease treated with pallidotomy and deep brain stimulation. Mov Disord 24:10481053, 2009

    • Search Google Scholar
    • Export Citation
  • 15

    Fasano A, Ricciardi L, Bentivoglio AR, Canavese C, Zorzi G, Petrovic I, : Status dystonicus: predictors of outcome and progression patterns of underlying disease. Mov Disord 27:783788, 2012

    • Search Google Scholar
    • Export Citation
  • 16

    Franzini A, Cordella R, Messina G, Marras CE, Romito LM, Albanese A, : Targeting the brain: considerations in 332 consecutive patients treated by deep brain stimulation (DBS) for severe neurological diseases. Neurol Sci 33:12851303, 2012

    • Search Google Scholar
    • Export Citation
  • 17

    Franzini A, Franzini A, Levi V, Cordella R, Messina G: An unusual surgical indication for cerebral tuberculosis: status dystonicus. Case report. Acta Neurochir (Wien) 160:13551358, 2018

    • Search Google Scholar
    • Export Citation
  • 18

    Franzini A, Levi V, Franzini A, Dones I, Messina G: Staged pallidotomy: MRI and clinical follow-up in status dystonicus. Br J Neurosurg 33:184187, 2019

    • Search Google Scholar
    • Export Citation
  • 19

    Grandas F, Fernandez-Carballal C, Guzman-de-Villoria J, Ampuero I: Treatment of a dystonic storm with pallidal stimulation in a patient with PANK2 mutation. Mov Disord 26:921922, 2011

    • Search Google Scholar
    • Export Citation
  • 20

    Horn A, Kühn AA: Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage 107:127135, 2015

    • Search Google Scholar
    • Export Citation
  • 21

    Jech R, Bares M, Urgosík D, Cerná O, Klement P, Adamovicová M, : Deep brain stimulation in acute management of status dystonicus. Mov Disord 24:22912292, 2009

    • Search Google Scholar
    • Export Citation
  • 22

    Kovacs N, Balas I, Janszky J, Simon M, Fekete S, Komoly S: Status dystonicus in tardive dystonia successfully treated by bilateral deep brain stimulation. Clin Neurol Neurosurg 113:808809, 2011

    • Search Google Scholar
    • Export Citation
  • 23

    Lobato-Polo J, Ospina-Delgado D, Orrego-González E, Gómez-Castro JF, Orozco JL, Enriquez-Marulanda A: Deep brain stimulation surgery for status dystonicus: a single-center experience and literature review. World Neurosurg 114:e992e1001, 2018

    • Search Google Scholar
    • Export Citation
  • 24

    Lumsden DE, Allen NM: Rethinking status dystonicus: a welcome start to a challenging problem. Mov Disord 33:344, 2018

  • 25

    Lumsden DE, King MD, Allen NM: Status dystonicus in childhood. Curr Opin Pediatr 29:674682, 2017

  • 26

    Manji H, Howard RS, Miller DH, Hirsch NP, Carr L, Bhatia K, : Status dystonicus: the syndrome and its management. Brain 121:243252, 1998 (Erratum in Brain 123[Pt 2]:419, 2000)

    • Search Google Scholar
    • Export Citation
  • 27

    Mariotti P, Fasano A, Contarino MF, Della Marca G, Piastra M, Genovese O, : Management of status dystonicus: our experience and review of the literature. Mov Disord 22:963968, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Marras CE, Rizzi M, Cantonetti L, Rebessi E, De Benedictis A, Portaluri F, : Pallidotomy for medically refractory status dystonicus in childhood. Dev Med Child Neurol 56:649656, 2014

    • Search Google Scholar
    • Export Citation
  • 29

    Marsden CD, Marion MH, Quinn N: The treatment of severe dystonia in children and adults. J Neurol Neurosurg Psychiatry 47:11661173, 1984

    • Search Google Scholar
    • Export Citation
  • 30

    Martinez-Torres I, Limousin P, Tisch S, Page R, Pinto A, Foltynie T, : Early and marked benefit with GPi DBS for Lubag syndrome presenting with rapidly progressive life-threatening dystonia. Mov Disord 24:17101712, 2009

    • Search Google Scholar
    • Export Citation
  • 31

    Meoni S, Fraix V, Castrioto A, Benabid AL, Seigneuret E, Vercueil L, : Pallidal deep brain stimulation for dystonia: a long term study. J Neurol Neurosurg Psychiatry 88:960967, 2017

    • Search Google Scholar
    • Export Citation
  • 32

    Nerrant E, Gonzalez V, Milesi C, Vasques X, Ruge D, Roujeau T, : Deep brain stimulation treated dystonia-trajectory via status dystonicus. Mov Disord 33:11681173, 2018

    • Search Google Scholar
    • Export Citation
  • 33

    Ondo WG, Desaloms JM, Jankovic J, Grossman RG: Pallidotomy for generalized dystonia. Mov Disord 13:693698, 1998

  • 34

    Oterdoom DLM, van Egmond ME, Ascencao LC, van Dijk JMC, Saryyeva A, Beudel M, : Reversal of status dystonicus after relocation of pallidal electrodes in DYT6 generalized dystonia. Tremor Other Hyperkinet Mov (N Y) 8:530, 2018

    • Search Google Scholar
    • Export Citation
  • 35

    Rohani M, Munhoz RP, Shahidi G, Parvaresh M, Miri S: Fatal status dystonicus in tardive dystonia due to depletion of deep brain stimulation’s pulse generator. Brain Stimul 10:160161, 2017

    • Search Google Scholar
    • Export Citation
  • 36

    Sobstyl M, Ząbek M, Kmieć T, Sławek J, Budohoski KP: Status dystonicus due to internal pulse generator depletion in a patient with primary generalized dystonia. Mov Disord 29:188189, 2014

    • Search Google Scholar
    • Export Citation
  • 37

    Sobstyl MR, Sławek JW, Ząbek M: The neurosurgical treatment of patients in dystonic state - overview of the literature. Neurol Neurochir Pol 48:6370, 2014

    • Search Google Scholar
    • Export Citation
  • 38

    Starr PA, Rau GM, Davis V, Marks WJJ Jr, Ostrem JL, Simmons D, : Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson’s disease and normal macaque. J Neurophysiol 93:31653176, 2005

    • Search Google Scholar
    • Export Citation
  • 39

    Stewart K, Harvey A, Johnston LM: A systematic review of scales to measure dystonia and choreoathetosis in children with dyskinetic cerebral palsy. Dev Med Child Neurol 59:786795, 2017

    • Search Google Scholar
    • Export Citation
  • 40

    Teive HAG, Munhoz RP, Souza MM, Antoniuk SA, Santos MLSF, Teixeira MJ, : Status dystonicus: study of five cases. Arq Neuropsiquiatr 63:2629, 2005

    • Search Google Scholar
    • Export Citation
  • 41

    Timmermann L, Pauls KAM, Wieland K, Jech R, Kurlemann G, Sharma N, : Dystonia in neurodegeneration with brain iron accumulation: outcome of bilateral pallidal stimulation. Brain 133:701712, 2010

    • Search Google Scholar
    • Export Citation
  • 42

    Trezza A, Antonini A, Sganzerla EP, Landi A: Globus pallidus internus deep brain stimulation for the treatment of status dystonicus in tardive dystonia. Acta Neurochir (Wien) 158:17891791, 2016

    • Search Google Scholar
    • Export Citation
  • 43

    Vitek JL, Chockkan V, Zhang JY, Kaneoke Y, Evatt M, DeLong MR, : Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann Neurol 46:2235, 1999

    • Search Google Scholar
    • Export Citation
  • 44

    Walcott BP, Nahed BV, Kahle KT, Duhaime AC, Sharma N, Eskandar EN: Deep brain stimulation for medically refractory life-threatening status dystonicus in children. J Neurosurg Pediatr 9:99102, 2012

    • Search Google Scholar
    • Export Citation
  • 45

    Zorzi G, Marras C, Nardocci N, Franzini A, Chiapparini L, Maccagnano E, : Stimulation of the globus pallidus internus for childhood-onset dystonia. Mov Disord 20:11941200, 2005

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

Correspondence Vincenzo Levi: Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy. vincenzo.levi@istituto-besta.it.

INCLUDE WHEN CITING Published online December 20, 2019; DOI: 10.3171/2019.10.JNS191691.

V.L. and G.Z. share first authorship, and N.N. and A.F. share senior authorship.

Disclosures Dr. Levi is a medical advisor at Newronika S.R.L. (neurostimulator manufacturer), but this activity is not relevant to the paper.

  • View in gallery

    A: Overall motor outcomes at the 1-month follow-up after surgery, categorized according to the modified Ben-Haim scale. B: A subjective assessment of the surgical procedures was administered to all caregivers during a telephone interview in June 2018 to capture potential easing of caregiving and increased patient comfort levels after surgery in the long term. Among the patients experiencing a good or excellent benefit (red and yellow), 70% underwent DBS surgery. Figure is available in color online only.

  • View in gallery

    Repeated measures ANOVA of BAD scores (y-axis) showing no significant differences between the surgical procedures (p > 0.05). fu = follow-up; pre = preoperatively; post = postoperatively. Figure is available in color online only.

  • View in gallery

    Upper: Postoperative DBS lead locations in the MNI space. GPi, green; globus pallidus externus, blue; subthalamic nucleus, orange; red nucleus, red. Lower: DBS lead and pallidal lesion localizations in the AC-PC space. Figure is available in color online only.

  • 1

    Allen NM, Lin JP, Lynch T, King MD: Status dystonicus: a practice guide. Dev Med Child Neurol 56:105112, 2014

  • 2

    Angelini L, Nardocci N, Estienne M, Conti C, Dones I, Broggi G: Life-threatening dystonia-dyskinesias in a child: successful treatment with bilateral pallidal stimulation. Mov Disord 15:10101012, 2000

    • Search Google Scholar
    • Export Citation
  • 3

    Apetauerova D, Schirmer CM, Shils JL, Zani J, Arle JE: Successful bilateral deep brain stimulation of the globus pallidus internus for persistent status dystonicus and generalized chorea. J Neurosurg 113:634638, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    Balas I, Kovacs N, Hollody K: Staged bilateral stereotactic pallidothalamotomy for life-threatening dystonia in a child with Hallervorden-Spatz disease. Mov Disord 21:8285, 2006

    • Search Google Scholar
    • Export Citation
  • 5

    Barbosa BJAP, Carra RB, Duarte KP, Godinho F, de Andrade DC, Teixeira MJ, : Bilateral subthalamic nucleus stimulation in refractory status dystonicus. J Neurol Sci 388:159161, 2018

    • Search Google Scholar
    • Export Citation
  • 6

    Ben-Haim S, Flatow V, Cheung T, Cho C, Tagliati M, Alterman RL: Deep brain stimulation for status dystonicus: a case series and review of the literature. Stereotact Funct Neurosurg 94:207215, 2016

    • Search Google Scholar
    • Export Citation
  • 7

    Borggraefe I, Boetzel K, Boehmer J, Berweck S, Mueller-Felber W, Mueller K, : Return to participation – significant improvement after bilateral pallidal stimulation in rapidly progressive DYT-1 dystonia. Neuropediatrics 39:239242, 2008

    • Search Google Scholar
    • Export Citation
  • 8

    Cif L, Coubes P: Historical developments in children’s deep brain stimulation. Eur J Paediatr Neurol 21:109117, 2017

  • 9

    Cif L, Hariz M: Seventy years of pallidotomy for movement disorders. Mov Disord 32:972982, 2017 (Erratum in Mov Disord 32:1498, 2017)

    • Search Google Scholar
    • Export Citation
  • 10

    Cohn MC, Hudgins PA, Sheppard SK, Starr PA, Bakay RA: Pre- and postoperative MR evaluation of stereotactic pallidotomy. AJNR Am J Neuroradiol 19:10751080, 1998

    • Search Google Scholar
    • Export Citation
  • 11

    Coubes P, Echenne B, Roubertie A, Vayssière N, Tuffery S, Humbertclaude V, : [Treatment of early-onset generalized dystonia by chronic bilateral stimulation of the internal globus pallidus. Apropos of a case.] Neurochirurgie 45:139144, 1999 (French)

    • Search Google Scholar
    • Export Citation
  • 12

    Coubes P, Roubertie A, Vayssiere N, Hemm S, Echenne B: Treatment of DYT1-generalised dystonia by stimulation of the internal globus pallidus. Lancet 355:22202221, 2000

    • Search Google Scholar
    • Export Citation
  • 13

    Elkaim LM, De Vloo P, Kalia SK, Lozano AM, Ibrahim GM: Deep brain stimulation for childhood dystonia: current evidence and emerging practice. Expert Rev Neurother 18:773784, 2018

    • Search Google Scholar
    • Export Citation
  • 14

    Elkay M, Silver K, Penn RD, Dalvi A: Dystonic storm due to Batten’s disease treated with pallidotomy and deep brain stimulation. Mov Disord 24:10481053, 2009

    • Search Google Scholar
    • Export Citation
  • 15

    Fasano A, Ricciardi L, Bentivoglio AR, Canavese C, Zorzi G, Petrovic I, : Status dystonicus: predictors of outcome and progression patterns of underlying disease. Mov Disord 27:783788, 2012

    • Search Google Scholar
    • Export Citation
  • 16

    Franzini A, Cordella R, Messina G, Marras CE, Romito LM, Albanese A, : Targeting the brain: considerations in 332 consecutive patients treated by deep brain stimulation (DBS) for severe neurological diseases. Neurol Sci 33:12851303, 2012

    • Search Google Scholar
    • Export Citation
  • 17

    Franzini A, Franzini A, Levi V, Cordella R, Messina G: An unusual surgical indication for cerebral tuberculosis: status dystonicus. Case report. Acta Neurochir (Wien) 160:13551358, 2018

    • Search Google Scholar
    • Export Citation
  • 18

    Franzini A, Levi V, Franzini A, Dones I, Messina G: Staged pallidotomy: MRI and clinical follow-up in status dystonicus. Br J Neurosurg 33:184187, 2019

    • Search Google Scholar
    • Export Citation
  • 19

    Grandas F, Fernandez-Carballal C, Guzman-de-Villoria J, Ampuero I: Treatment of a dystonic storm with pallidal stimulation in a patient with PANK2 mutation. Mov Disord 26:921922, 2011

    • Search Google Scholar
    • Export Citation
  • 20

    Horn A, Kühn AA: Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage 107:127135, 2015

    • Search Google Scholar
    • Export Citation
  • 21

    Jech R, Bares M, Urgosík D, Cerná O, Klement P, Adamovicová M, : Deep brain stimulation in acute management of status dystonicus. Mov Disord 24:22912292, 2009

    • Search Google Scholar
    • Export Citation
  • 22

    Kovacs N, Balas I, Janszky J, Simon M, Fekete S, Komoly S: Status dystonicus in tardive dystonia successfully treated by bilateral deep brain stimulation. Clin Neurol Neurosurg 113:808809, 2011

    • Search Google Scholar
    • Export Citation
  • 23

    Lobato-Polo J, Ospina-Delgado D, Orrego-González E, Gómez-Castro JF, Orozco JL, Enriquez-Marulanda A: Deep brain stimulation surgery for status dystonicus: a single-center experience and literature review. World Neurosurg 114:e992e1001, 2018

    • Search Google Scholar
    • Export Citation
  • 24

    Lumsden DE, Allen NM: Rethinking status dystonicus: a welcome start to a challenging problem. Mov Disord 33:344, 2018

  • 25

    Lumsden DE, King MD, Allen NM: Status dystonicus in childhood. Curr Opin Pediatr 29:674682, 2017

  • 26

    Manji H, Howard RS, Miller DH, Hirsch NP, Carr L, Bhatia K, : Status dystonicus: the syndrome and its management. Brain 121:243252, 1998 (Erratum in Brain 123[Pt 2]:419, 2000)

    • Search Google Scholar
    • Export Citation
  • 27

    Mariotti P, Fasano A, Contarino MF, Della Marca G, Piastra M, Genovese O, : Management of status dystonicus: our experience and review of the literature. Mov Disord 22:963968, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Marras CE, Rizzi M, Cantonetti L, Rebessi E, De Benedictis A, Portaluri F, : Pallidotomy for medically refractory status dystonicus in childhood. Dev Med Child Neurol 56:649656, 2014

    • Search Google Scholar
    • Export Citation
  • 29

    Marsden CD, Marion MH, Quinn N: The treatment of severe dystonia in children and adults. J Neurol Neurosurg Psychiatry 47:11661173, 1984

    • Search Google Scholar
    • Export Citation
  • 30

    Martinez-Torres I, Limousin P, Tisch S, Page R, Pinto A, Foltynie T, : Early and marked benefit with GPi DBS for Lubag syndrome presenting with rapidly progressive life-threatening dystonia. Mov Disord 24:17101712, 2009

    • Search Google Scholar
    • Export Citation
  • 31

    Meoni S, Fraix V, Castrioto A, Benabid AL, Seigneuret E, Vercueil L, : Pallidal deep brain stimulation for dystonia: a long term study. J Neurol Neurosurg Psychiatry 88:960967, 2017

    • Search Google Scholar
    • Export Citation
  • 32

    Nerrant E, Gonzalez V, Milesi C, Vasques X, Ruge D, Roujeau T, : Deep brain stimulation treated dystonia-trajectory via status dystonicus. Mov Disord 33:11681173, 2018

    • Search Google Scholar
    • Export Citation
  • 33

    Ondo WG, Desaloms JM, Jankovic J, Grossman RG: Pallidotomy for generalized dystonia. Mov Disord 13:693698, 1998

  • 34

    Oterdoom DLM, van Egmond ME, Ascencao LC, van Dijk JMC, Saryyeva A, Beudel M, : Reversal of status dystonicus after relocation of pallidal electrodes in DYT6 generalized dystonia. Tremor Other Hyperkinet Mov (N Y) 8:530, 2018

    • Search Google Scholar
    • Export Citation
  • 35

    Rohani M, Munhoz RP, Shahidi G, Parvaresh M, Miri S: Fatal status dystonicus in tardive dystonia due to depletion of deep brain stimulation’s pulse generator. Brain Stimul 10:160161, 2017

    • Search Google Scholar
    • Export Citation
  • 36

    Sobstyl M, Ząbek M, Kmieć T, Sławek J, Budohoski KP: Status dystonicus due to internal pulse generator depletion in a patient with primary generalized dystonia. Mov Disord 29:188189, 2014

    • Search Google Scholar
    • Export Citation
  • 37

    Sobstyl MR, Sławek JW, Ząbek M: The neurosurgical treatment of patients in dystonic state - overview of the literature. Neurol Neurochir Pol 48:6370, 2014

    • Search Google Scholar
    • Export Citation
  • 38

    Starr PA, Rau GM, Davis V, Marks WJJ Jr, Ostrem JL, Simmons D, : Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson’s disease and normal macaque. J Neurophysiol 93:31653176, 2005

    • Search Google Scholar
    • Export Citation
  • 39

    Stewart K, Harvey A, Johnston LM: A systematic review of scales to measure dystonia and choreoathetosis in children with dyskinetic cerebral palsy. Dev Med Child Neurol 59:786795, 2017

    • Search Google Scholar
    • Export Citation
  • 40

    Teive HAG, Munhoz RP, Souza MM, Antoniuk SA, Santos MLSF, Teixeira MJ, : Status dystonicus: study of five cases. Arq Neuropsiquiatr 63:2629, 2005

    • Search Google Scholar
    • Export Citation
  • 41

    Timmermann L, Pauls KAM, Wieland K, Jech R, Kurlemann G, Sharma N, : Dystonia in neurodegeneration with brain iron accumulation: outcome of bilateral pallidal stimulation. Brain 133:701712, 2010

    • Search Google Scholar
    • Export Citation
  • 42

    Trezza A, Antonini A, Sganzerla EP, Landi A: Globus pallidus internus deep brain stimulation for the treatment of status dystonicus in tardive dystonia. Acta Neurochir (Wien) 158:17891791, 2016

    • Search Google Scholar
    • Export Citation
  • 43

    Vitek JL, Chockkan V, Zhang JY, Kaneoke Y, Evatt M, DeLong MR, : Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann Neurol 46:2235, 1999

    • Search Google Scholar
    • Export Citation
  • 44

    Walcott BP, Nahed BV, Kahle KT, Duhaime AC, Sharma N, Eskandar EN: Deep brain stimulation for medically refractory life-threatening status dystonicus in children. J Neurosurg Pediatr 9:99102, 2012

    • Search Google Scholar
    • Export Citation
  • 45

    Zorzi G, Marras C, Nardocci N, Franzini A, Chiapparini L, Maccagnano E, : Stimulation of the globus pallidus internus for childhood-onset dystonia. Mov Disord 20:11941200, 2005

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 53 53 53
PDF Downloads 28 28 28
EPUB Downloads 0 0 0