Deep brain stimulation for camptocormia in dystonia and Parkinson s disease
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1 J Neurol (2011) 258: DOI /s ORIGINAL COMMUNICATION Deep brain stimulation for camptocormia in dystonia and Parkinson s disease Hans-Holger Capelle Christoph Schrader Christian Blahak Wolfgang Fogel Thomas M. Kinfe Hansjoerg Baezner Joachim K. Krauss Received: 18 December 2009 / Revised: 20 July 2010 / Accepted: 28 July 2010 / Published online: 28 August 2010 Ó Springer-Verlag 2010 Abstract Camptocormia, or bent spine syndrome, may occur in various movement disorders such as primary dystonia or idiopathic Parkinson s disease (PD). Although deep brain stimulation (DBS) is an established treatment in refractory primary dystonia and advanced PD, few data are available on the effect of DBS on camptocormia comparing these two conditions. Seven patients (4 with dystonia, 3 with PD; mean age 60.3 years at surgery, range years) with camptocormia were included in the study. Five patients underwent bilateral GPi DBS and two patients underwent bilateral STN DBS guided by CT-stereotactic surgery and microelectrode recording. Pre- and postoperative motor assessment included the BFM in the dystonia patients and the UPDRS in the PD patients. Severity of camptocormia was assessed by the BFM subscore for the trunk at the last available follow-up at a mean of 17.3 months (range 9 36 months). There were no surgical complications. In the four patients with dystonia there was a mean improvement of 53% in the BFM motor score (range 41 79%) and of 63% (range 50 67%) in the BFM H.-H. Capelle T. M. Kinfe J. K. Krauss (&) Department of Neurosurgery, Medical School Hannover, MHH, Carl-Neuberg-Straße 1, Hannover, Germany krauss.joachim@mh-hannover.de C. Schrader Department of Neurology, Medical School Hannover, MHH, Hannover, Germany C. Blahak H. Baezner Department of Neurology, University Hospital Mannheim, Mannheim, Germany W. Fogel Department of Neurology, Deutsche Klinik für Diagnostik, Wiesbaden, Germany subscore for the trunk at the last available follow-up (mean 14.3 months, range 9 18 months). In the three patients with camptocormia in PD who underwent bilateral STN DBS (2 patients) or pallidal DBS (1 patient), the PD symptoms improved markedly (mean improvement in the UPDRS motor subscore stimulation on/medication off 55%, range 49 61%), but there was no or only mild improvement of camptocormia in the two patients who underwent STN DBS, and only moderate improvement in the patient with GPi DBS at the last available follow-up (mean 21 months, range months). GPi DBS is an effective treatment for camptocormia in dystonia. The response of camptocormia to chronic STN or GPi DBS in PD is more heterogenous. The latter may be due to a variety of causes and needs further clarification. Keywords Camptocormia Deep brain stimulation Dystonia Parkinson s disease Introduction Camptocormia, or bent spine syndrome, is defined as a forced posture with a forward-bent trunk which increases during standing or walking and vanishes in the recumbent position [1]. Azher and Jankovic [1] recently proposed classifying camptocormia according to etiology. Camptocormia may occur in movement disorders, most frequently in Parkinson s disease (PD) and in primary dystonia [2, 3]; it may be a sequel of stroke, spine deformities, spine surgery, or of psychogenic origin [4, 5]; and, finally, it can develop due to myopathic changes, including inflammatory or metabolic mitochondrial myopathies of the erector spinae muscle [6]. This etiologic classification is important, since treatment options for camptocormia depend crucially
2 J Neurol (2011) 258: on the etiology. For camptocormia in PD and primary dystonia, drugs including levodopa, anticholinergics, muscle relaxants and tetrabenazine are frequently tried, however, in most cases only minimal or no effect at all is achieved. Chronic deep brain stimulation (DBS) of the posteroventral lateral globus pallidus internus (GPi) and the subthalamic nucleus (STN) has been established as a powerful tool in the treatment of refractory primary dystonia and of advanced PD [7 13]. There are few data available, however, on the effect of DBS on camptocormia in dystonia or in PD [1, 14 17]. Here, we report a series of seven patients with camptocormia in dystonia or in PD to evaluate the effect of chronic DBS and to determine whether the therapeutic response depends on etiology. s and methods Seven patients with disabling camptocormia were included in this prospective study. Mean age at surgery was 60.3 years (range years). s were included only when camptocormia constituted a component of significant disability and a primary indication for surgery. All patients were assessed according to a standard protocol and video tape recording which included the Burke Fahn Marsden (BFM) scale in dystonia and the unified Parkinson s disease rating scale (UPDRS) in PD preoperatively and at scheduled follow-up investigations. To assess the severity of camptocormia and to evaluate the effect of DBS, the BFM motor subscore for the trunk was used (range 0 16 points). In addition, pre- and postoperative low back pain scores (visual analogue scale, range 0 10; with 0 = no pain, 10 = worst pain) and postoperative patient s self rating scores (0 100%; with 0% = no effect, 100% = excellent improvement) for the effect of DBS on their camptocormia were ascertained. Three patients had camptocormia embedded in a clinical picture of segmental or generalized dystonia (2 m/l f, mean age 50 years at surgery, years). Oral medication including trihexiphenidyl, levodopa and benzodiazepines, as well as repeated botulinum toxin (BTX) injections did not yield therapeutic benefit for their camptocormia. 4 (f, 69 years old) presented with disabling camptocormia without other dystonic features or PD symptoms. In this patient, histological examination of a biopsy of the erector trunci muscle which was performed 2 years earlier had shown findings consistent with a myopathy. Since she suffered markedly but her camptocormia was refractory to medication with biperiden and levodopa, as well as to extensive physiotherapy, DBS was offered to her as an optional treatment. s 1 4 were scheduled for bilateral GPi DBS. Demographic and clinical data are summarized in Table 1. Three patients suffered from advanced idiopathic PD according to UK brain bank criteria (3 men, mean age 67.3 years at surgery, years; see Table 1). None of Table 1 Diagnostic and clinical data of seven patients with camptocormia in dystonia or in PD Age/sex Disorder Duration of movement disorder Medication preoperative (LEDD) Medication postoperative at last available follow-up 1 72/F Segmental dystonia 25 years Levodopa Clonazepam Trihexiphenidyl Tetrabenazine Clonazepam Bromazepam Botulinum toxine A injections 2 39/M Segmental dystonia 13 years Trihexiphenidyl None Botulinum toxine A injections 3 40/M Generalized dystonia 15 years Trihexiphenidyl Trihexiphenidyl Levodopa 4 69/F Isolated dystonic camptocormia 5 years Biperiden None (associated with myopathy) Levodopa 5 73/M Parkinson s disease 12 years LEDD 1100 mg LEDD 900 mg 6 65/M Parkinson s disease 15 years LEDD 570 mg LEDD 570 mg Amantadin Baclofen Baclofen 7 64/M Parkinson s disease 10 years LEDD 800 mg LEDD 800 mg LEDD levodopa equivalent daily dose
3 98 J Neurol (2011) 258: them showed signs of psychosis or had cognitive deficits according to the preoperative assessments. Dopaminergic medication improved the cardinal symptoms of their PD, yet it was ineffective for camptocormia. All three patients had marked degenerative spinal disorders including multilevel osteochondrosis and spondylarthrosis. s 5 and 6 suffered also from motor fluctuations and were therefore scheduled for bilateral STN DBS. 7 was scheduled for DBS of the posteroventral lateral GPi. The target for implantation of the DBS electrodes was defined by MR imaging and CT-stereotactic imaging as described in detail elsewhere [18]. The preliminary target for the GPi was 20 mm lateral to and 4 mm below the intercommissural line, and 2 3 mm anterior to the intercommissural midpoint. The preliminary target for the STN was 12 mm lateral to and 4 mm below the intercommissural line, and 4 mm posterior to the intercommissural midpoint. All patients, except for patient 4, were operated under local anaesthesia. The detailed surgical procedure has been reported elsewhere [18]. Microelectrode recordings (MER) were performed to delineate the target in the GPi or STN further. MER for the pallidum started at 15 mm above the target. To place the electrodes into the sensorimotor part of the GPi, passive movements of the contralateral joints were conducted intraoperatively and were linked to the response in the MER. Based on the mapping of neurons and the response to passive movements, the DBS electrode was implanted so that contact 1 and 2 (electrode 3387, Medtronic) were placed within the sensorimotor part of the GPi. Macrostimulation was used to assess the thresholds for visual phosphenes or capsular responses. For localization of the STN, MER started at 10 mm above target. Again, passive movements of the contralateral joints were performed intraoperatively along the trajectory to locate the dorsolateral part of the STN. The DBS electrode (model 3389, Medtronic, Minneapolis, MN, USA) was placed so that contact 2 was in the dorsolateral portion of the nucleus and contact 3 at the border to or in the zona incerta. Macrostimulation was used to assess thresholds for paraesthesias and capsular responses. Electrode localizations were controlled by postoperative stereotactic CT scans. Additionally, the stereotactic CT scans were matched with the preoperative MR scans to determine the morphological position of the electrodes inside the GPi or STN. Postoperative programming of the stimulator settings were performed as described elsewhere in detail [18]. For the GPi we routinely used a bipolar configuration with contact 1 as the cathode and contact 2 as the anode. In the beginning of stimulation the frequency was set at 130 Hz, and pulse width at 210 ls, but could subsequently be adjusted to other settings to achieve optimal efficacy. In the following 6 8 weeks the amplitude was increased stepwise up to V in case there were no stimulation-induced side effects, such as hypokinetic dysarthria. If satisfactory clinical improvement occurred, the amplitude was not further increased. Otherwise, the amplitude was increased up to 6 V. At this stage, monopolar stimulation via single contacts was also evaluated. For the STN we routinely started stimulation in a unipolar setting with contact 2 as the cathode. The frequency was set at 130 Hz, and pulse width at 60 ls. The amplitude was adapted according to the effect on the PD symptoms and occurrence of stimulationinduced side effects. Impedances of all electrode contacts were checked routinely at follow-up visits. Localization of the electrodes and their contacts within the target region was confirmed in all patients. Two single channel pacemakers were used in five patients (Soletra, Medtronic) and a dual channel pacemaker in two (Kinetra, Medtronic). The percentage of improvement for the pre- and postoperative BFM motor scores, the BFM motor subscores for the trunk, and for the low back pain scores was calculated as follows: [(score preoperative-score postoperative)/score preoperative] The statistical analysis was performed using a paired t-test. In case of failed normality test of data, the Wilcoxon signed-rank test was used for analysis. For statistical analysis of two independent groups an unpaired t-test was used; in case of failed normality test of data the Wilcoxon rank sum test was used (SigmaStat Software; SPSS Inc., Chicago, IL, USA). For patients self rating the percentage of improvement was used for the statistical analysis. Results There were no surgery-related complications in any instance. All patients experienced sustained benefit of dystonia or of the cardinal PD symptoms, respectively (Table 2; Fig. 1). In the four patients with dystonia, there was a mean improvement by 53% (range, 41 79%; p = 0.135) according to the BFM motor score after a mean follow-up period of 14.3 months (range, 9 18 months). The three patients with PD who underwent bilateral STN DBS (2 patients) or GPi DBS (1 patient) showed a mean of 55% improvement (range, 49 61%; p \ 0.001) in the UPDRS motor subscore medication off/stimulation on, compared to the preoperative medication off state at the last available follow-up at a mean of 21 months (range, months). The pre- and postoperative BFM and UPDRS motor scores are summarized in Table 2. Camptocormia was improved in six of the seven patients. The mean change in all seven patients was 44% (range, 0 67%, p = 0.007) according to the BFM motor
4 J Neurol (2011) 258: Table 2 Pre- and postoperative BFM motor (patients with dystonia) and UPDRS motor scores (patients with Parkinson s disease) and BFM motor subscores for the trunk BFM motor subscore trunk at last available FU (provoking 9 severity factor) BFM motor last available FU Last available follow-up in months BFM motor subscore trunk preoperative (provoking 9 severity factor) BFM motor preoperative Target of DBS 1 GPi (4 9 3) (2 9 2) 2 GPi (4 9 3) (2 9 2) 3 GPi (4 9 3) (2 9 2) 4 GPi (4 9 3) (3 9 2) BFM motor subscore trunk at last available FU (provoking 9 severity factor) UPDRS III (med off/stim on) last available FU Last available follow-up in months BFM motor subscore trunk preoperative (provoking 9 severity factor) UPDRS III preoperative (med off/on) Target of DBS 5 STN 43/21 8 (4 9 2) (3 9 2) 6 STN 36/15 12 (4 9 3) (4 9 3) 7 GPi 47/25 9 (3 9 3) (2 9 3) Summarized pre- and postoperative BFM motor (patients with dystonia) and UPDRS motor scores (patients with Parkinson s disease) of the seven patients at the last available follow-up at a mean of 17.3 months (range, 9 36 months). The second score for all patients shows the BFM motor subscore for the trunk to assess camptocormia UPDRS unified Parkinson s disease rating scale; BFM Burke Fahn Marsden dystonia rating scale Relative improvement of BFM or UPDRS motor score (%) Relative improvement of BFM motor subscore for the trunk (%) Fig. 1 Relative improvement of the BFM motor scores and the BFM motor subscores for the trunk in dystonia patients (patients 1 4) and PD patients (patients 5 7) at the last available follow-up. The left columns show the improvement (in % as compared to baseline) of the BFM or UPDRS motor scores, the right columns show the improvement (in % as compared to baseline) of the BFM motor subscore for the trunk as a measurement for camptocormia subscore for the trunk at the last available follow-up at a mean of 17.3 months (range, 9 36 months). In the patients with dystonia, pallidal DBS yielded marked and sustained improvement of their camptocormia. Compared to the preoperative BFM motor subscore for the trunk, patients with camptocormia in dystonia showed a mean improvement of 63% (range, 50 67%; p = 0.125) at the last available follow-up at a mean of 14.3 months (range, 9 18 months). 4 initially experienced a more unstable benefit with no improvement of her camptocormia after initiation of stimulation but reported more marked improvement at 18 months after changing stimulation frequency, which was reflected by 50% improvement in the BFM subscore for the trunk. Figure 2 shows pre- and postoperative video stills at the last follow-up (Fig. 2). In the four dystonia patients, scores for low back pain improved by a mean of 42% (range, 33 50%; p = 0.03) (Fig. 3). The effect of DBS as estimated by the patients self rating score indicated a 58% mean improvement as compared to baseline (range, 50 70%; p = 0.001) at the last available follow-up. The three PD patients experienced improvement of camptocormia by a mean of 19% (range, 0 33%; p = 0.199) according to the BFM subscore for the trunk at the last available follow-up at a mean of 21 months (range,
5 100 J Neurol (2011) 258: Fig. 2 Video stills of patient 4 preoperatively and at 18-month follow-up with stimulation frequency set to 60 Hz A Visual Analogue Scale B Effect on camptocormia % Low back pain score preoperative Low back pain score postoperative s self rating scores: Effect of DBS on camptocormia % Fig. 3 a Pre- and postoperative low back pain scores. b s self rating scores on the effect of DBS on camptocormia. VAS, visual analogue scale; patients self rating: range 0 100%; 0%, no effect, 100%, excellent improvement months). 7, who underwent GPi DBS, showed the most pronounced improvement of his camptocormia among the PD patients by 33% at 36 months followup. The UPDRS motor subscore was improved by 49%. Dopaminergic medication was nearly equivalent to preoperative levels in all three patients at the last follow-up. Scores for low back pain changed according to the preoperative VAS by a mean of 13% (range, 0 25%; p = 0.225) (Fig. 3). s self rating score showed a mean change of 20% (range, 0 40%; p = 0.225) at the last follow-up. In the patients with dystonia, the camptocormia improvement was more pronounced than in the patients with PD (p = 0.057), comparing the BFM motor subscore for the trunk at baseline and at the last available follow-up (Fig. 1). The patients self rating scores in the dystonia patients were higher at the last available follow-up than were those of the PD patients (mean improvement of 58 vs. 20%; p = 0.057) (see Fig. 3). Stimulation settings at the last follow-up were as follows. s 1 3 were on bipolar stimulation (cathode contact 1, anode contact 2): mean amplitude 4.2 V, pulse width 210 ls, frequency 130 Hz. 4 had no benefit of camptocormia at 12 months postoperatively but developed shuffling gait with difficulty walking while on bipolar stimulation at 7 V and 130 Hz. After setting the frequency to 60 Hz, the gait disorder disappeared and there was consistent improvement of camptocormia at 3 V. At the last follow-up, the PD patient with GPi DBS was on bipolar stimulation with contact 1 set negative and 2 positive, the patients with STN DBS were on unipolar stimulation with contact 2 negative and the impulse generator positive. In STN DBS mean amplitude was 3.1 V, pulse width 60 ls, and frequency 130 Hz. In the patient with GPi DBS the amplitude was 3.5 V, pulse width 210 ls, and frequency 130 Hz. 7 presented with deterioration of his camptocormia due to battery depletion at 24 months postoperatively. After changing the pacemakers, camptocormia improved within days to the same extent as before. Discussion Our prospective study on the effect of DBS on camptocormia in seven patients presents the largest systematic
6 J Neurol (2011) 258: long-term follow-up study thus far. It demonstrates clearly that chronic DBS of the posteroventral lateral GPi yields sustained improvement in patients with camptocormia due to dystonia. The effect on camptocormia with pallidal DBS is comparable with the range of improvement for dystonia in general [7, 8, 11, 19, 20]. Changes of objective measurements for camptocormia were paralleled by patients self rating indices postoperatively. Furthermore, subjective improvement of back pain was in a similar range. The experience with pallidal DBS for camptocormia in dystonia is limited. Only a few patients had been reported earlier [14, 15, 21]. The results are summarized in Table 3. The beneficial effect of DBS was demonstrated first by Nandi and colleagues in a patient with tardive dystonia with sustained improvement at 6 months postoperatively. Fukaya et al. [15] mentioned three patients with camptocormia in a series of 36 patients with primary dystonia undergoing bilateral GPi DBS. They observed substantial improvement in camptocormia which was more pronounced than improvement of other dystonic symptoms. Camptocormia, however, was not assessed with a specific score. The postoperative course of patient 4 who was diagnosed as having a myopathy is puzzling. While myopathy has been thought by some to be the actual cause of camptocormia, it should also be considered that the focal myopathic changes in the truncal muscles might rather be a secondary phenomenon [22]. While chronic stimulation at 130 Hz yields good improvement of dystonia in the majority of patients with primary dystonia, recent observations indicate that mild parkinsonian symptoms might occur in a subset of patients [23, 24]. This is also reflected in the appearance of micrographia in patients with segmental dystonia upon chronic pallidal DBS [25]. It is somehow unusual that a parkinsonian gait disorder became manifest in our patient at 130 Hz stimulation without any Table 3 DBS for camptocormia: literature review Author/year, age Etiology of camptocormia Improvement of camptocormia Procedure Follow-up (months) Nandi et al. (2002) 1 patient, 39 Camptocormia in dystonia (tardive) Marked improvement 6 months Micheli et al. (2005) 1 patient, 62 Camptocormia in Parkinson s disease 90% 14 months Azher and Jankovic 1 patient, n.a. Camptocormia in Parkinson s disease No improvement of camptocormia (2005) Bilateral STN DBS PD symptoms improved Hellman et al. 1 patient, 53 Camptocormia in Parkinson s disease Marked improvement (2006) Bilateral STN DBS 10 months Fukaya et al. (2006) 3 patients out of 36 patients with Idiopathic camptocormia, camptocormia in 92.2% (±5.3%) primary dystonia dystonia 14 months Yamada et al. (2006) 1 patient, 71 Camptocormia in Parkinson s disease 75% Bilateral STN DBS 20 months Sako et al. (2009) O Riordan et al. (2009) 6 patients, mean age 60, range patients, mean age 64, range Capelle et al. (2010) 7 patients, mean age 60, range Camptocormia in Parkinson s disease Bilateral STN DBS Camptocormia in dystonia [1] Camptocormia in Parkinson s disease [2] 78% (±9.1%), Improvement of thoracolumbar angle 17 months Marked improvement of camptocormia in dystonia 60 months No improvement/modest improvement in PD 6 months Camptocormia in dystonia [4] 63% (range, 50 67%) 14.3 months Camptocormia in Parkinson s disease [3] 19% (range, 0 33%) 21 months Bilateral STN DBS [2] [1]
7 102 J Neurol (2011) 258: improvement of camptocormia. The concept that stimulation with 60 Hz or lower might be more valuable in some dystonia patients than high-frequency stimulation has been introduced only recently [26]. It may be that an altered balance between neuronal inhibition and orthodromic and antidromic fibre stimulation of pallidal pathways underlies the differential effects, both on improvement of dystonia and the manifestation of bradykinetic symptoms. The effects of chronic DBS on camptocormia in PD were less gratifying. GPi DBS appeared to be more effective then STN DBS. Similar to the occurrence of foot dystonia in PD patients not treated with levodopa, camptocormia may be a unique form of a secondary segmental dystonia in PD [27]. Others have thought that camptocormia in PD is an extreme form of stooped posture which may be linked to dysfunction of the caudate nucleus or the external pallidum [22, 28]. These considerations may explain why our patient 7, who underwent GPi DBS, experienced the most benefit. In another series, pallidal DBS has been described as resulting in moderate improvement in one PD patient, and as ineffective in another [21]. Micheli et al. [29] also reported a PD patient in whom bilateral GPi DBS showed beneficial and sustained improvement of PD symptoms and of camptocormia by 90%. Although bilateral STN DBS resulted in satisfactory improvement in motor symptoms,as shown by changes in the UPDRS III scores, this was not paralleled by improvement of camptocormia. Data on the effect of DBS on camptocormia in PD published thus far have yielded quite variable results (see Table 3). While STN DBS resulted in limited benefit or had no effect on camptocormia in some patients, marked improvement was noted in others [1, 16, 30]. The only multipatient series was published by Sako et al. [17] recently. In this series of six patients, improvement of camptocormia was described in all patients after STN DBS. Improvement was defined as a change in the thoracolumbar angle which was sustained at a mean follow-up period of 17 months. A limitation of our study is that we did not systematically test contacts other than the contact located at the dorsal STN for chronic stimulation in the two patients with STN DBS to achieve a better effect on camptocormia. Since camptocormia usually does not respond to levodopa treatment [31] and STN DBS is thought to be effective mainly for the dopa-responsive symptoms of PD, the mechanisms by which STN DBS improves camptocormia in some patients while not in others remain unclear. Note that camptocormia has also been considered a form of off-period dystonia in some instances [16]. Apart from methodological differences such as study design, the use of various rating scales and duration of disease, other patient-specific variables that did not receive attention might be relevant. While all three patients included in our study had marked degenerative spinal disorders at the thoracolumbar level, there is very limited information available on that in previous reports. The absence of improvement of camptocormia in patient 6 may also be due to severe degenerative changes of his lumbar spine. This is also reflected by the minimal change in the low-back pain level postoperatively. Further study on the effect of chronic DBS on camptocormia in PD is needed to clarify if the responsiveness of camptocormia to dopaminergic medication might be a predictive positive factor. Regarding such differences in responsiveness to levodopa, pallidal DBS might be reconsidered in some PD patients with camptocormia. Conclusions Pallidal DBS provides beneficial improvement for camptocormia as a symptom of segmental or generalized dystonia. The response to DBS of camptocormia in PD patients is more heterogeneous. More studies are needed in the latter in order to define those patients who will benefit from DBS surgery. References 1. Azher SN, Jankovic J (2005) Camptocormia: pathogenesis, classification, and response to therapy. Neurology 65: Lepoutre AC, Devos D, Blanchard-Dauphin A, Pardessus V, Maurage CA, Ferriby D, Hurtevent JF, Cotten A, Destée A, Defebvre L (2006) A specific clinical pattern of camptocormia in Parkinson s disease. J Neurol Neurosurg Psychiatry 77: Tolosa E, Compta Y (2006) Dystonia in Parkinson s disease. J Neurol 253(Suppl 7):VII7 VII13 4. Duman I, Baklaci K, Tan AK, Kalyon TA (2008) Unusual case of camptocormia triggered by lumbar disc herniation. Clin Rheumatol 27: Skidmore F, Anderson K, Fram D, Weiner W (2007) Psychogenic camptocormia. 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