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Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 1 av 7 Deep Brain Stimulation in Adult and Pediatric Movement Disorders
Laura CIF1, Simone HEMM1, Nathalie VAYSSIERE1, Philippe COUBES1 1Research Group on Movement Disorders, Department of Neurosurgery (Professor Philippe Coubes, Montpellier University Hospital, 34295 MONTPELLIER, CEDEX 5, FRANCE) Correspondence should be addressed to Philippe COUBES Background and purpose
In a wide range of medical conditions, a movement disorder can be the only symptom or it can be associated with other
neurological deficits. Most of them are of unknown origin. Dystonia, dyskinesia, myoclonus, tremor, atethosis are
abnormal movements susceptible to the influence of high frequency modulation of the basal ganglia. Nevertheless, the
control of these symptoms is highly dependent on the etiology. Movement disorders (primary dystonia, myoclonus
dystonia, tardive dyskinesia), which are not associated with other neurological deficits are more likely to be controlled by
high frequency stimulation.
The first validated medical condition successfully treated by Deep Brain Stimulation (DBS) was Parkinson’s disease (1).
Gradually, the indications of this therapy were enlarged to include other diseases associating movement disorders as
dystonia and dyskinesia of various etiologies. Based on the experience of our group (2) with brain lesioning surgery
(pallidotomy) in a young patient with idiopathic generalized dystonia (3) and deep brain stimulation in Parkinson’s
disease dyskinesias (1; 4), we reported, in 1996 the efficacy of DBS in a young lady presenting with severe life
threatening primary generalized dystonia after chronic bilateral stimulation of the GPi (5). Since then, 105 dystonic
patients have been treated for bilateral stimulation of the Internal Globus Pallidus (GPi) in the department of
Neurosurgery in Montpellier.
The originality of our method consists of the use of stereotactic MR imaging for the target determination, without
microelectrode recordings. This considerably reduces the procedure’s duration, which is important especially in children,
as well as for the risk of haemorrhage (0 cases). Furthermore, the surgery is performed under general anesthesia which is
better for patients with permanent involuntary movements.
We will present the population, the surgical procedure, the clinical management of the patients and the results obtained
by DBS. In order to discuss the criteria for selecting the patients with dystonia - dyskinesia, we will briefly consider this
medical condition. Whatever, other movement disorders being influenced by the DBS are sometimes associated with
dystonia in patients to be operated.
Dystonia has been defined as a neurological syndrome characterized by involuntary, sustained muscle contractions,
causing twisting and repetitive movements or abnormal postures. (6)
Its classification is a difficult task and can be done in several ways: according to the spread of the symptoms to different
body parts, to the age of onset or to aetiology.
According to distribution, dystonia is classified into one of the following categories: focal, segmental, multifocal,
hemidystonia and generalized dystonia.
The age of onset is another important criterion for characterizing a patient. In case of early onset, the disease is more
likely to generalize and severely worsen than for adult-onset dystonias.
Dystonia can also be classified by aetiology. In primary dystonia, dystonia is the only symptom and can be sporadic or
inherited (DYT1 dystonia (7)). Dystonia-plus is a group of syndromes where dystonia is usually associated with another
neurological condition such as Parkinsonism or myoclonus (Dopa responsive dystonia, myoclonus-dystonia syndrome).
The group of heredodegenerative dystonias includes numerous diseases and in this group, dystonia is typically not pure.
Amino acid disorders, lipid disorders, Lesch-Nyhan disease, pantothenate kinase-associated neurodegeneration (PKAN),
mitochondrial diseases, Wilson’s disease, Huntington’s disease, Juvenile Parkinsonism-dystonia (8; 9) and many others
are heredodegenerative dystonias. Secondary dystonias are generated by insults such as drugs, strokes, tumours,
infections (6) and this subgroup includes also dystonia-dyskinesia secondary to cerebral palsy (CP).
In 40% of the patients with early-onset dystonia a specific cause can be found. The aetiological diagnosis is established
by clinical evaluation, neuroimaging and molecular analysis in primary dystonias. When the history of the disease, the
clinical examination and the brain MRI suggest a heredodegenerative dystonia, further investigations are performed such
as blood work-up, urine sample analysis, CSF testing, electrophysiological studies, muscle, skin, liver biopsies, PET, eye
slit-lamp examination.
The identification of the aetiology is very important for the prognosis of the disease and because of the existence of very
few medical conditions having a specific treatment such as Dopa-Responsive dystonia, creatine deficiency or Wilson’s
disease.
Several drugs are available to treat dystonic symptoms but their efficacy is often limited, transient and difficult to assess
(often because of the fluctuation of the symptoms). The most important drugs to be used are Levodopa (also as a
diagnosis trial in Dopa responsive dystonia), anticholinergics, benzodiazepines, baclofen (10) and Botulinum toxin
http://www.dystonia-europe.org/europe/articles/Coubes%20L.%20Article.htm Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 2 av 7 injections especially for the treatment of focal dystonias (11)
Because of the poor efficacy of the pharmaceutical treatment in cases of very severe forms of movement disorders
(especially generalized dystonias with onset in childhood) we were led to propose deep brain stimulation as another
therapeutic strategy in order to control the symptoms generating life-threatening complications.
Patients (Population)
In the following report, we will present the results of 82 patients presenting with segmentary or generalized dystonia
treated by bilateral chronic electrical stimulation of the GPi. The population was divided in subgroups separating, for
each of them, children from adults. Group 1 included patients with primary generalized DYT1 dystonia, group 2 primary
generalized dystonia without DYT1 mutation, group 3 primary segmentary dystonia (cervical-axial dystonia), group 4
generalized dystonia-dyskinesia due to postanoxic cerebral palsy, group 5 generalized dystonia secondary to PKAN and
group 6 one generalized dystonia secondary to mitochondrial disease. For the reported patients, the follow-up was at
least of 6 months.
Clinical evaluation
Dystonic movements and abnormal postures were evaluated using the Burke-Fahn-Marsden-Dystonia-Rating scale
(BFMDRS, motor and disability part) (12) before the surgical procedure, several times during the post-operative hospital
stay, every month during the first year and every three months afterwards.
Surgical procedure
Bilateral electrode implantation was performed in a single surgical session under general anesthesia (13-15). The MR-
compatible Leksell stereotactic frame was applied and a 3D-SPGR (spoiled gradient recall) acquisition was performed.
The postero-ventral part of the GPi was located through axial, sagittal and coronal MRI studies (Figure 1A). The target
coordinates (x, y, z) and the trajectory angles (α,β) were calculated using a dedicated software.
Two four contact electrodes (DBS 3389, Medtronic, Minneapolis) were implanted under strict profile radioscopic
control. Immediate postoperative control MRI (Figure 1B) was obtained with the stereotactic frame on. Electrodes were
connected to a pulse generator five days later (Itrel II or III, Kinetra and Soletra Medtronic, Minneapolis, USA), which
was subcutaneously introduced in the abdominal area. In each patient final placement of the implanted devices and their
connections were checked by a radiographic control during the postoperative hospital stay (Figure 2).
Electric parameter settings
After implantation, stimulators were switched on. Electrical variables were set at high frequency (130Hz), 450 µsec for
the pulse width with one contact negatively activated. Intensity was progressively increased according to the needs of
each patient (16) and the clinical evolution. Usually the first levels for the voltage were between 0.5V-0.8V. Over the
time, we modified the electric parameters in several patients, by increasing the voltage or activating a second contact
when requested. The mean steady state value of the voltage was 1.6 ± 0.3V. (17)
Clinical results
Motor and disability scores’ evolution (BMFDRS) for primary and secondary dystonia is presented in table I and II.
Within each group, the improvement was progressive over time. With more than 3 years of follow-up, the clinical
improvement was comparable for the two groups of primary dystonia (82% of improvement on the motor scale). The
results obtained in the group of secondary dystonia and heredodegenerative diseases are less important but yet around
40% with 3 years of follow-up. After three years, the disability score improvement was superior in the group of primary
DYT1 dystonia (80%) compared to non-DYT1 primary dystonia (56%) and to secondary dystonia (19%). The group of
secondary dystonia and heredodegenerative diseases is a very heterogeneous group. This is why results for all etiologies
should be presented separately.
Discussion
We report here our experience with bilateral chronic electrical stimulation of the GPi in the treatment of primary DYT1positive and DYT1 negative generalized dystonia (5; 18-21), generalized dystonia – dyskinesia secondary to post-anoxic cerebral palsy, generalized dystonia secondary to PKAN syndrome and to mitochondrial diseases. We also report theresults obtained by DBS in primary segmentary dystonia. Since the first child has been operated, 126 other patientsunderwent surgery for DBS in our department (Dystonia + Parkinson). While at the beginning DBS was proposed in children with primary generalized dystonia (with or without DYT1mutation), selection criteria were revisited and enlarged for including now other types of dystonia in children and adults.
Several patients with generalized dystonia associating myoclonus underwent surgery for chronic electrical stimulation ofthe GPi and we could see an early and complete control of myoclonus. These findings led us to propose this treatment ina child with genetically proven myoclonus-dystonia syndrome (20)(MDS, DYT11, mutation in the epsilon-amino sarcoglycan gene (22; 23)) and we obtained a very satisfactory improvement of his symptoms. We confirmed in a secondpatient with MDS the efficiency of GPi stimulation. Being confronted with very severe clinical conditions in patients with secondary dystonia and heredodegenerativediseases, in which the efficacy of the medical treatment was poor and in which dystonic movements and postures werecomparable with those met in primary dystonia, we proposed DBS in several selected patients of these groups.
http://www.dystonia-europe.org/europe/articles/Coubes%20L.%20Article.htm Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 3 av 7 The criteria for patient selection in this group were clinical, electrophysiological and based on brain imaging as well ason etiology. We performed surgery for DBS in patients in whom dystonia and dyskinesia were prominent compared to otherneurological deficits (especially motor deficit and spasticity), the motor pattern was preserved and in patients presentingwith severe or life threatening symptoms due to dystonia - dyskinesia (swallowing difficulties, permanent opisthotonos, painful muscle spasms). Electroencephalogram, electroretinogram, visual and brainstem, somatosensory evoked responses were obtained. Motorevoked potentials were performed in elder children to identify pyramidal tract impairment. In order to exclude brainabnormalities contraindicating surgery (major cortical atrophy, severe periventicular leucomalacia especially met incerebral palsy, basal ganglia and thalamic lesions), brain MR under general anesthesia was performed in all patients. As shown in tables I and II, best results were obtained within the group of patients with DYT1 mutation (5; 18; 21; 24). The surgery of abnormal movements should intervene before the occurrence of skeletal deformities, which alwaysdiminish the outcome. Within the population of non-DYT1 dystonia and especially in secondary and heredodegenerativedystonias, results are not so predictable. The improvement of dysarthria is variable and often very few influenced byDBS. Stimulation’s switch-off systematically causes the recurrence of symptoms within some hours or days. Whatever, in several patients we could see a long lasting preservation of the clinical improvement for several weeks withoutstimulation. In the secondary dystonia group, the efficacy of stimulation is far more limited. We were led to propose it for veryhandicapped patients for whom other therapeutic strategies failed to improve dystonia, as already mentioned. The clinicaland etiological heterogeneity among this group almost prevents any global interpretation of these results. In this group, afrequently associated hypertonia of pyramidal origin influences the dystonic component. An important negative prognostic factor under stimulation is the existence of a permanent hypertonia at rest, whatevermay be its origin. Although we are not yet able to predict the long-term prognosis, we observed an interesting improvement with dyskinesia- dystonia secondary to a perinatal anoxia (dyskinetic forms of cerebral palsy accountingfor less than 10% of all forms CP) (25), PKAN and mitochondrial diseases treated by GPi stimulation. A constant controlof pain associated with muscle spasms was obtained in patients suffering from secondary dystonia. The progression of the causal disease is of critical importance for patient’s prognosis. Using this surgical method based on MRI alone (13-15), the associated morbidity is low. We didn’t observe hemorrhage due to the intracerebral tracts as reported before in other series (our experience reaches 236 electrodes) (26). Secondary infection of the stimulation system remains the major complication of this technique and was observed in 4 patients. Wesummarize the complications observed in our population in table III. The remarkable tolerance of the internal pulse generator must be also emphasized in children. We never observed anycomplication due to displacement with growth (loss of efficacy linked to the displacement of the electrode). As shown infigure 2 and 3, a residual length was enrolled around the battery and the electrode in order to compensate for growth inchildren and to provide some flexibility with movements in the system (Figure 2). Furthermore, it appears that growthdoes not interfere with stimulation, and the implantation of a single 90 cm extension compensates adequately for thegrowth of the child. We observed in two patients (1 child, 1 adult) an extension fracture due to adherences fixing theextension and limiting its mobility and flexibility. The children’s physical development (height, body weight) was followed as well as hormonal levels (Insulin-like Growth
Factor-IGF1, Insulin–like Growth Factor Binding Protein 3-IGF-BP3, Estradiol, Testosterone, Folliculine Stimulating
Hormone-FSH and Luteinizing Hormone-LH) in order to check puberty development.
Conclusion
Despite cost and complexity of the follow-up, bilateral chronic electrical stimulation can be proposed as first line
treatment for early onset primary generalized dystonia when pharmacologically intractable and also early considered in
segmentary dystonia in adults and in well-selected cases of secondary dystonia. It is conservative, adaptable, reversible
and well tolerated by the whole population. It must be applied soon, especially in primary dystonia before neuro-
orthopaedic sequels occur. The complication rate remains low.
For secondary dystonia, pallidal stimulation can partially improve dystonic syndromes with important control of pain and
swallowing difficulties.
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FIGURE LEGENDS
Figure 1: Stereotactic MRI. A. Pre-operative planning. B. Post-operative MRI to control the final electrode position
(black points = electrode artefacts).
Figure 2: Radiographic control of the implanted devices. A. Electrodes connected to the extensions. B. Neurostimulators
with extension length reserve. Arrow indicates a extension fracture during sports.
http://www.dystonia-europe.org/europe/articles/Coubes%20L.%20Article.htm Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 5 av 7 http://www.dystonia-europe.org/europe/articles/Coubes%20L.%20Article.htm Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 6 av 7 Table II. Motor scores (BMFDRS) of dystonic children treated by DBS.
Mean values ±SD. The values in brackets represent the mean improvement in percent. A reduction in the score indicates
an improvement in function. BMFDRS denotes Burke-Marsden Fahn's Dystonia Rating Scale.
1The improvement in percent is calculated based on the maximal possible gain (Score
2Primary generalized dystonia 3DYT1 mutation 4Pantothenate kinase-associated neurodegeneration 5Number of patients http://www.dystonia-europe.org/europe/articles/Coubes%20L.%20Article.htm Treatment of dystonic syndromes by chronic electrical stimulation of the internal glob. Sida 7 av 7 Table III. Disability scores (BMFDRS) of dystonic children treated by DBS.
Mean values ±SD. The values in brackets represent the mean improvement in percent. A reduction in the score indicates
an improvement in function. BMFDRS denotes Burke-Marsden Fahn's Dystonia Rating Scale.
1The improvement in percent is calculated based on the maximal possible gain (Score
2Primary generalized dystonia 3DYT1 mutation 4Pantothenate kinase-associated neurodegeneration 5Number of patients Complications
Table IV.
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