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Motor improvement with bilateral subthalamic nucleus deep brain stimulation in a patient with levodopa-responsive secondary parkinsonism
Parkinsonism and Related Disorders 18 (2012) 79e81
Contents lists available at SciVerse ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Short communication
Motor improvement with bilateral subthalamic nucleus deep brain stimulation in a patient with levodopa-responsive secondary parkinsonism Vikas Kotagala, *, Parag G. Patilb, Kelvin L. Chouc a
Department of Neurology, University of Michigan Medical School, 1500 East Medical Center Drive, Ann Arbor, MI 48109-5322, USA Departments of Neurosurgery, Anesthesiology and Biomedical Engineering, University of Michigan Medical School, 1500 E. Medical Center Drive, SPC 5338, Ann Arbor, MI 48109-5338, USA c Departments of Neurology and Neurosurgery, University of Michigan Medical School, 1500 E. Medical Center Drive, SPC 5316, Ann Arbor, MI 48109-5316, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 April 2011 Received in revised form 21 July 2011 Accepted 19 August 2011
At many centers, subthalamic nucleus (STN) deep brain stimulation (DBS) is not considered for patients with secondary forms of parkinsonism, due to higher expected rates of treatment failure. We present the case of a woman with secondary parkinsonism that developed following a Measles, Mumps, and Rubella (MMR) vaccination, who experienced sustained improvement in motor function following STN DBS. Despite the diagnosis of a secondary parkinsonism, this patient responded well to dopaminergic therapy, a good predictor of DBS outcome in patients with idiopathic Parkinson’s disease. This case suggests that DBS may be considered in the setting of secondary parkinsonism if such patients have levodoparesponsive symptoms. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Parkinson’s disease Deep brain stimulation Secondary parkinson disease Subthalamic nucleus Levodopa
1. Introduction Deep brain stimulation (DBS) is an effective therapy for patients with idiopathic Parkinson’s disease (PD) complicated by persistent motor fluctuations or dyskinesias [1]. In contrast, there is little evidence that DBS is effective for patients with atypical parkinsonism (AP) [2]. This may be because AP cases have a greater degree of levodopa unresponsive symptoms compared to idiopathic PD. Cases of AP include parkinsonian-like syndromes, such as multiple system atrophy (MSA) or progressive supranuclear palsy (PSP), as well as secondary parkinsonism which can be caused by infection, trauma, ischemia, radiation, or other central nervous system insults. While commonly employed exclusion criteria for DBS include significant cognitive or psychiatric symptoms, the most important screening criteria may in fact be the presence of levodoparesponsive parkinsonian motor symptoms [3]. Many centers use a prespecified target of a 30% improvement with levodopa in Unified Parkinson’s Disease Rating Scale (UPDRS) motor subscores to determine whether a PD patient is a candidate for DBS [4]. We
* Corresponding author. Tel.: þ1 734 936 9020; fax: þ1 734 615 4991. E-mail addresses: [email protected] (V. Kotagal), [email protected] (P.G. Patil), [email protected] (K.L. Chou). 1353-8020/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2011.08.014
present a patient with levodopa-responsive secondary parkinsonism who ultimately benefited from bilateral subthalamic nucleus (STN) DBS.
2. Case history This 62-year-old right-handed woman underwent a general health examination at age 38 in 1987, in preparation for starting a job as a nurse. Because she had negative serum rubella titers, she received an MMR vaccine. Soon after the vaccination, she developed nausea and left-sided slowness, weakness, and upper extremity tremor. Over the following months, she was evaluated by several neurologists who also noted rigidity and bradykinesia involving her left side. Brain MRI at the time and at present reveals scattered periventricular and deep T2/FLAIR hyperintensities in the bilateral thalami, internal capsule, and left cerebellar hemisphere, none of which enhance with gadolinium (Fig. 1). These hyperintensities have neither enhanced nor changed in configuration on serial MRIs over 20 years, and are believed to be consistent with post-vaccination encephalomyelitis. In the year following her vaccination, her left upper extremity rest tremor worsened and she developed a parkinsonian gait. She was initially treated with amantadine, which helped her rest tremor. Soon afterwards, carbidopa/levodopa were added which further improved her tremor.
80
V. Kotagal et al. / Parkinsonism and Related Disorders 18 (2012) 79e81
Fig. 1. Coronal T2 (a) and FLAIR (b) Brain MRI without contrast demonstrating bilateral T2/FLAIR perventricular hyperintensities thought to result from post-vaccination encephalomyelitis.
Approximately five to seven years after starting levodopa, she experienced wearing-off symptoms with prominent left-sided rigidity, for which pramipexole was effective. Entacapone was added a few years later to further prevent wearing-off effects. She was also treated with 0.5 g/kg of intravenous immunoglobulin every 1e2 months for several years with clinical benefit including ambulation without an assistive device in the month following immunoglobulin infusions. She received this therapy, off and on, for approximately 15 years, but discontinued it in early 2008 secondary to out-of-pocket cost. She expressed interest in DBS in 2005, but was not offered surgery due to her diagnosis of secondary parkinsonism. However, she continued to have prominent wearing-off symptoms about three to 4 h after a levodopa dose and had occasional dose failures, particularly with regard to rigidity. Consequently, she was referred for a multidisciplinary DBS evaluation at our center in 2009. Her best “on” times tended to come in the mornings. During these times she felt loose and could walk with minimal assistance. This allowed her to work in the garden independently, an important aspect of her quality of life. During her “off” times she was completely dependent on her husband for all activities. She never had dyskinesias, hallucinations, depression, or cognitive complaints. She realized that DBS would not allow her to walk independently and her hope was that DBS might provide her with her “morning” functional status throughout the day. Neuropsychological evaluation showed no dementia. Her pre-operative levodopa equivalent dose (LED) was 1805 mg [5]. Her MDS-UPDRS motor score was 79 off medications and 54 on medications, representing a 32% improvement with dopaminergic therapy. Her medications included carbidopa/levodopa 25/100, 2pills given 5 times daily, pramipexole 1.5 mg four times daily, amantadine 100 mg three times daily, entacapone200 mg three times daily, and oxybutynin 5 mg three times daily. Off/on testing was performed using her typical morning dose of levodopa. The patient underwent bilateral STN DBS electrode placement followed a month later by implantation of a Kinetra stimulator (Kinetra system, Medtronic Inc, Minneapolis, Minnesota). Postoperatively, she had a wound infection requiring IV antibiotics but had no tremor or wearing-off symptoms once stimulation parameters were optimized. At six month follow-up, MDS-UPDRS motor scores were 63 off-medication/on-stimulation and 44 onmedication/on-stimulation. At one year follow-up, her MDS-UPDRS scores remained stable at 53 off-medication/on-stimulation and 45 on-medication/on-stimulation. LED was reduced by 57% at one year follow-up (see Video S1).
3. Discussion Despite the diagnosis of secondary parkinsonism, our patient had a motor response to levodopa. Because of her motor response, she underwent bilateral STN DBS and has had a sustained motor response for at least one year. DBS for secondary parkinsonism has been reported previously in the literature, though results have been mixed. Revilla et al. reported the case of a 20 year old man with radiation-induced parkinsonism [6]. Within a nine year period, he developed bilateral rest tremor, left upper extremity dystonia, postural instability, and a parkinsonian gait. His pre-operative UPDRS motor score off-medications was 79 and improved to 47 on dopaminergic medications. He underwent bilateral STN DBS and post-operatively his off-medication/off-stimulation UPDRS motor score was 70.5 compared to an off-medication/on-stimulation score of 57. He was ultimately able to decrease his levodopa dose by 33% at six month follow-up. Krack et al. reported the case of patient who developed a post-anoxic akinetic-parkinsonian syndrome. He did not have any subjective or objective response to levodopa or apomorphine challenge prior to surgery and had a preoperative UPDRS motor score of 65 off-medications. He ultimately underwent bilateral STN DBS 18 months after the development of parkinsonian symptoms. His initial post-stimulation Off/On UPDRS motor scores were 61 and 62 respectively though he did describe a subjective improvement in swallowing and gait [7]. Taken together, these cases illustrate that levodopa response may predict DBS response in secondary parkinsonism.
Video S1. Supplementary Video: Subject’s examination in three different stages: a) pre-operative off-medication testing, b) pre-operative on-medication testing, and c) 12 month post-operative on-medication & on stimulation testing.
V. Kotagal et al. / Parkinsonism and Related Disorders 18 (2012) 79e81
A limited number of cases of post vaccination parkinsonism have been reported, though none have undergone DBS. Alveset al. presented the case of a 5 year old boy who developed a febrile syndrome 15 days after a live measles vaccination and who, months later, developed hemiparkinsonism with an MRI showing bilateral substantia nigra T2 hyperintensities [8]. Similarly, our patient developed parkinsonism from an MMR vaccine with subcortical T2 hyperintensities on MR imaging. Increased activity within the STN is thought to pay a role in the pathogenesis of Parkinson’s disease through its excitatory effects on the Globus Pallidus internal (GPi) leading to inhibition of thalamocortical neurons and the subsequent development of parkinsonian symptoms [9]. Decreased striatal dopamine most likely leads to this STN-specific-excitation in Parkinson’s disease by increasing inhibition to the Globus Pallidus external (GPe). DBS is thought to modulate this circuit in idiopathic PD by altering the tempo and frequency of STN firing rates thereby affecting downstream neuronal thalamocortical targets [10]. Interestingly this classically cited model of idiopathic PD was heavily influenced by an animal model of secondary parkinsonism, namely 1-methyl-4pheynl-1,2,3,6-tetrahydropyride (MPTP)-induced parkinsonism in non-human primates [11]. Contemporary understanding of basal ganglia physiology is consistent with the notion that those patients who experience a significant levodopa-mediated clinical improvement in UPDRS motor scores may stand to benefit from STN DBS regardless of the etiology of their parkinsonism. A robust response to a levodopa challenge is crucial to predict which parkinsonian patients will have a favorable outcome following STN DBS. Many surgical centers have formed DBS selection criteria based on the CAPSIT-PD report which proposes offering surgery to those patients with idiopathic PD for greater than five years who have had a positive response to levodopa therapy [12]. While this standard is both appropriate and widely accepted, it should be noted that such selection criteria will continue to evolve as we gain insight into the underlying mechanisms of DBS and parkinsonism. As our case illustrates, patients suffering from secondary parkinsonism that is responsive to levodopa may, in the appropriate clinical setting, respond well to STN DBS therapy. Competing interests Dr. Chou has received honoraria from Allergan, Teva Neuroscience, and Medtronic for speaking engagements and from Merz and Medtronic for consulting work. He receives royalties from
81
publishing chapters in UpToDate (2007) and receives research support from the NIH, the Parkinson Study Group, and the Huntington Study Group. Dr. Patil receives research support from the National Institutes of Health, the American Parkinson’s Disease Association, the Coulter Foundation, the Foundation for Physical Therapy, the Parkinson’s Disease Foundation, and the University of Michigan Department of Neurosurgery. Funding for this research was provided by the University of Michigan Department of Neurosurgery.
Acknowledgments None.
References [1] Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks Jr WJ, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 2009;301(1):63e73. [2] Shih LC, Tarsy D. Deep brain stimulation for the treatment of atypical parkinsonism. Mov Disord 2007;22(15):2149e55. [3] Charles PD, Van Blercom N, Krack P, Lee SL, Xie J, Besson G, et al. Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 2002; 59(6):932e4. [4] Bronstein JM, Tagliati M, Alterman RL, Lozano AM, Volkmann J, Stefani A, et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol; 2010. doi:10.1001/archneurol.2010.260. Published Online First: 11 October. [5] Herzog J, Volkmann J, Krack P, Kopper F, Potter M, Lorenz D, et al. Two-year follow-up of subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord 2003;18(11):1332e7. [6] Revilla F, Mink J, McGee-Minnich L, Antenor J, Leverich L, Moerlein S, et al. Radiation-induced parkinsonism with good response to levodopa and bilateral subthalamic nuclei stimulation. Mov Disord 2002;17:1113 [abstract]. [7] Krack P, Dowsey PL, Benabid AL. Ineffective subthalamic nucleus stimulation in levodopa-resistant postischemic parkinsonism subthalamic nucleus postischemic parkinsonism. Neurology 2000;54(11):2182e4. [8] Alves RS, Barbosa ER, Scaff M. Postvaccinal parkinsonism. Mov Disord 1992; 7(2):178e80. [9] DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990;13(7):281e5. [10] Chang J-Y, Shi L-H, Luo F, Zhang W-M, Woodward DJ. Studies of the neural mechanisms of deep brain stimulation in rodent models of Parkinson’s disease. Neurosci Biobehav Rev 2007;31(5):643e57. [11] Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990;249(4975):1436e8. [12] Defer G-L, Widner H, Marie R-M. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord 1999;14(4):572e84.
Contents lists available at SciVerse ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Short communication
Motor improvement with bilateral subthalamic nucleus deep brain stimulation in a patient with levodopa-responsive secondary parkinsonism Vikas Kotagala, *, Parag G. Patilb, Kelvin L. Chouc a
Department of Neurology, University of Michigan Medical School, 1500 East Medical Center Drive, Ann Arbor, MI 48109-5322, USA Departments of Neurosurgery, Anesthesiology and Biomedical Engineering, University of Michigan Medical School, 1500 E. Medical Center Drive, SPC 5338, Ann Arbor, MI 48109-5338, USA c Departments of Neurology and Neurosurgery, University of Michigan Medical School, 1500 E. Medical Center Drive, SPC 5316, Ann Arbor, MI 48109-5316, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 April 2011 Received in revised form 21 July 2011 Accepted 19 August 2011
At many centers, subthalamic nucleus (STN) deep brain stimulation (DBS) is not considered for patients with secondary forms of parkinsonism, due to higher expected rates of treatment failure. We present the case of a woman with secondary parkinsonism that developed following a Measles, Mumps, and Rubella (MMR) vaccination, who experienced sustained improvement in motor function following STN DBS. Despite the diagnosis of a secondary parkinsonism, this patient responded well to dopaminergic therapy, a good predictor of DBS outcome in patients with idiopathic Parkinson’s disease. This case suggests that DBS may be considered in the setting of secondary parkinsonism if such patients have levodoparesponsive symptoms. Ó 2011 Elsevier Ltd. All rights reserved.
Keywords: Parkinson’s disease Deep brain stimulation Secondary parkinson disease Subthalamic nucleus Levodopa
1. Introduction Deep brain stimulation (DBS) is an effective therapy for patients with idiopathic Parkinson’s disease (PD) complicated by persistent motor fluctuations or dyskinesias [1]. In contrast, there is little evidence that DBS is effective for patients with atypical parkinsonism (AP) [2]. This may be because AP cases have a greater degree of levodopa unresponsive symptoms compared to idiopathic PD. Cases of AP include parkinsonian-like syndromes, such as multiple system atrophy (MSA) or progressive supranuclear palsy (PSP), as well as secondary parkinsonism which can be caused by infection, trauma, ischemia, radiation, or other central nervous system insults. While commonly employed exclusion criteria for DBS include significant cognitive or psychiatric symptoms, the most important screening criteria may in fact be the presence of levodoparesponsive parkinsonian motor symptoms [3]. Many centers use a prespecified target of a 30% improvement with levodopa in Unified Parkinson’s Disease Rating Scale (UPDRS) motor subscores to determine whether a PD patient is a candidate for DBS [4]. We
* Corresponding author. Tel.: þ1 734 936 9020; fax: þ1 734 615 4991. E-mail addresses: [email protected] (V. Kotagal), [email protected] (P.G. Patil), [email protected] (K.L. Chou). 1353-8020/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.parkreldis.2011.08.014
present a patient with levodopa-responsive secondary parkinsonism who ultimately benefited from bilateral subthalamic nucleus (STN) DBS.
2. Case history This 62-year-old right-handed woman underwent a general health examination at age 38 in 1987, in preparation for starting a job as a nurse. Because she had negative serum rubella titers, she received an MMR vaccine. Soon after the vaccination, she developed nausea and left-sided slowness, weakness, and upper extremity tremor. Over the following months, she was evaluated by several neurologists who also noted rigidity and bradykinesia involving her left side. Brain MRI at the time and at present reveals scattered periventricular and deep T2/FLAIR hyperintensities in the bilateral thalami, internal capsule, and left cerebellar hemisphere, none of which enhance with gadolinium (Fig. 1). These hyperintensities have neither enhanced nor changed in configuration on serial MRIs over 20 years, and are believed to be consistent with post-vaccination encephalomyelitis. In the year following her vaccination, her left upper extremity rest tremor worsened and she developed a parkinsonian gait. She was initially treated with amantadine, which helped her rest tremor. Soon afterwards, carbidopa/levodopa were added which further improved her tremor.
80
V. Kotagal et al. / Parkinsonism and Related Disorders 18 (2012) 79e81
Fig. 1. Coronal T2 (a) and FLAIR (b) Brain MRI without contrast demonstrating bilateral T2/FLAIR perventricular hyperintensities thought to result from post-vaccination encephalomyelitis.
Approximately five to seven years after starting levodopa, she experienced wearing-off symptoms with prominent left-sided rigidity, for which pramipexole was effective. Entacapone was added a few years later to further prevent wearing-off effects. She was also treated with 0.5 g/kg of intravenous immunoglobulin every 1e2 months for several years with clinical benefit including ambulation without an assistive device in the month following immunoglobulin infusions. She received this therapy, off and on, for approximately 15 years, but discontinued it in early 2008 secondary to out-of-pocket cost. She expressed interest in DBS in 2005, but was not offered surgery due to her diagnosis of secondary parkinsonism. However, she continued to have prominent wearing-off symptoms about three to 4 h after a levodopa dose and had occasional dose failures, particularly with regard to rigidity. Consequently, she was referred for a multidisciplinary DBS evaluation at our center in 2009. Her best “on” times tended to come in the mornings. During these times she felt loose and could walk with minimal assistance. This allowed her to work in the garden independently, an important aspect of her quality of life. During her “off” times she was completely dependent on her husband for all activities. She never had dyskinesias, hallucinations, depression, or cognitive complaints. She realized that DBS would not allow her to walk independently and her hope was that DBS might provide her with her “morning” functional status throughout the day. Neuropsychological evaluation showed no dementia. Her pre-operative levodopa equivalent dose (LED) was 1805 mg [5]. Her MDS-UPDRS motor score was 79 off medications and 54 on medications, representing a 32% improvement with dopaminergic therapy. Her medications included carbidopa/levodopa 25/100, 2pills given 5 times daily, pramipexole 1.5 mg four times daily, amantadine 100 mg three times daily, entacapone200 mg three times daily, and oxybutynin 5 mg three times daily. Off/on testing was performed using her typical morning dose of levodopa. The patient underwent bilateral STN DBS electrode placement followed a month later by implantation of a Kinetra stimulator (Kinetra system, Medtronic Inc, Minneapolis, Minnesota). Postoperatively, she had a wound infection requiring IV antibiotics but had no tremor or wearing-off symptoms once stimulation parameters were optimized. At six month follow-up, MDS-UPDRS motor scores were 63 off-medication/on-stimulation and 44 onmedication/on-stimulation. At one year follow-up, her MDS-UPDRS scores remained stable at 53 off-medication/on-stimulation and 45 on-medication/on-stimulation. LED was reduced by 57% at one year follow-up (see Video S1).
3. Discussion Despite the diagnosis of secondary parkinsonism, our patient had a motor response to levodopa. Because of her motor response, she underwent bilateral STN DBS and has had a sustained motor response for at least one year. DBS for secondary parkinsonism has been reported previously in the literature, though results have been mixed. Revilla et al. reported the case of a 20 year old man with radiation-induced parkinsonism [6]. Within a nine year period, he developed bilateral rest tremor, left upper extremity dystonia, postural instability, and a parkinsonian gait. His pre-operative UPDRS motor score off-medications was 79 and improved to 47 on dopaminergic medications. He underwent bilateral STN DBS and post-operatively his off-medication/off-stimulation UPDRS motor score was 70.5 compared to an off-medication/on-stimulation score of 57. He was ultimately able to decrease his levodopa dose by 33% at six month follow-up. Krack et al. reported the case of patient who developed a post-anoxic akinetic-parkinsonian syndrome. He did not have any subjective or objective response to levodopa or apomorphine challenge prior to surgery and had a preoperative UPDRS motor score of 65 off-medications. He ultimately underwent bilateral STN DBS 18 months after the development of parkinsonian symptoms. His initial post-stimulation Off/On UPDRS motor scores were 61 and 62 respectively though he did describe a subjective improvement in swallowing and gait [7]. Taken together, these cases illustrate that levodopa response may predict DBS response in secondary parkinsonism.
Video S1. Supplementary Video: Subject’s examination in three different stages: a) pre-operative off-medication testing, b) pre-operative on-medication testing, and c) 12 month post-operative on-medication & on stimulation testing.
V. Kotagal et al. / Parkinsonism and Related Disorders 18 (2012) 79e81
A limited number of cases of post vaccination parkinsonism have been reported, though none have undergone DBS. Alveset al. presented the case of a 5 year old boy who developed a febrile syndrome 15 days after a live measles vaccination and who, months later, developed hemiparkinsonism with an MRI showing bilateral substantia nigra T2 hyperintensities [8]. Similarly, our patient developed parkinsonism from an MMR vaccine with subcortical T2 hyperintensities on MR imaging. Increased activity within the STN is thought to pay a role in the pathogenesis of Parkinson’s disease through its excitatory effects on the Globus Pallidus internal (GPi) leading to inhibition of thalamocortical neurons and the subsequent development of parkinsonian symptoms [9]. Decreased striatal dopamine most likely leads to this STN-specific-excitation in Parkinson’s disease by increasing inhibition to the Globus Pallidus external (GPe). DBS is thought to modulate this circuit in idiopathic PD by altering the tempo and frequency of STN firing rates thereby affecting downstream neuronal thalamocortical targets [10]. Interestingly this classically cited model of idiopathic PD was heavily influenced by an animal model of secondary parkinsonism, namely 1-methyl-4pheynl-1,2,3,6-tetrahydropyride (MPTP)-induced parkinsonism in non-human primates [11]. Contemporary understanding of basal ganglia physiology is consistent with the notion that those patients who experience a significant levodopa-mediated clinical improvement in UPDRS motor scores may stand to benefit from STN DBS regardless of the etiology of their parkinsonism. A robust response to a levodopa challenge is crucial to predict which parkinsonian patients will have a favorable outcome following STN DBS. Many surgical centers have formed DBS selection criteria based on the CAPSIT-PD report which proposes offering surgery to those patients with idiopathic PD for greater than five years who have had a positive response to levodopa therapy [12]. While this standard is both appropriate and widely accepted, it should be noted that such selection criteria will continue to evolve as we gain insight into the underlying mechanisms of DBS and parkinsonism. As our case illustrates, patients suffering from secondary parkinsonism that is responsive to levodopa may, in the appropriate clinical setting, respond well to STN DBS therapy. Competing interests Dr. Chou has received honoraria from Allergan, Teva Neuroscience, and Medtronic for speaking engagements and from Merz and Medtronic for consulting work. He receives royalties from
81
publishing chapters in UpToDate (2007) and receives research support from the NIH, the Parkinson Study Group, and the Huntington Study Group. Dr. Patil receives research support from the National Institutes of Health, the American Parkinson’s Disease Association, the Coulter Foundation, the Foundation for Physical Therapy, the Parkinson’s Disease Foundation, and the University of Michigan Department of Neurosurgery. Funding for this research was provided by the University of Michigan Department of Neurosurgery.
Acknowledgments None.
References [1] Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks Jr WJ, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 2009;301(1):63e73. [2] Shih LC, Tarsy D. Deep brain stimulation for the treatment of atypical parkinsonism. Mov Disord 2007;22(15):2149e55. [3] Charles PD, Van Blercom N, Krack P, Lee SL, Xie J, Besson G, et al. Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 2002; 59(6):932e4. [4] Bronstein JM, Tagliati M, Alterman RL, Lozano AM, Volkmann J, Stefani A, et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol; 2010. doi:10.1001/archneurol.2010.260. Published Online First: 11 October. [5] Herzog J, Volkmann J, Krack P, Kopper F, Potter M, Lorenz D, et al. Two-year follow-up of subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord 2003;18(11):1332e7. [6] Revilla F, Mink J, McGee-Minnich L, Antenor J, Leverich L, Moerlein S, et al. Radiation-induced parkinsonism with good response to levodopa and bilateral subthalamic nuclei stimulation. Mov Disord 2002;17:1113 [abstract]. [7] Krack P, Dowsey PL, Benabid AL. Ineffective subthalamic nucleus stimulation in levodopa-resistant postischemic parkinsonism subthalamic nucleus postischemic parkinsonism. Neurology 2000;54(11):2182e4. [8] Alves RS, Barbosa ER, Scaff M. Postvaccinal parkinsonism. Mov Disord 1992; 7(2):178e80. [9] DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990;13(7):281e5. [10] Chang J-Y, Shi L-H, Luo F, Zhang W-M, Woodward DJ. Studies of the neural mechanisms of deep brain stimulation in rodent models of Parkinson’s disease. Neurosci Biobehav Rev 2007;31(5):643e57. [11] Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990;249(4975):1436e8. [12] Defer G-L, Widner H, Marie R-M. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord 1999;14(4):572e84.