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History, Applications, and Mechanisms of Deep Brain Stimulation

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History, Applications, and Mechanisms of Deep Brain Stimulation NEUROLOGICAL REVIEW SECTION EDITOR: DAVID E. PLEASURE, MD History, Applications, and Mechanisms of Deep Brain Stimulation Svjetlana Miocinovic, MD, PhD; Suvarchala Somayajula, MD; Shilpa Chitnis, MD, PhD; Jerrold L. Vitek, MD, PhD eep brain stimulation (DBS) is an effective surgical treatment for medication-refractory hypokinetic and hyperkinetic movement disorders, and it is being explored for a variety of other neurological and psychiatric diseases. Deep brain stimulation has been Food and Drug Administration–approved for essential tremor and Parkinson disease and has Da humanitarian device exemption for dystonia and obsessive-compulsive disorder. Neurostimulation is the fruit of decades of both technical and scientific advances in the field of basic neuroscience and functional neurosurgery. Despite the clinical success of DBS, the therapeutic mechanism of DBS re- mains under debate. Our objective is to provide a comprehensive review of DBS focusing on move- ment disorders, including the historical evolution of the technique, applications and outcomes with an overview of the most pertinent literature, current views on mechanisms of stimulation, and de- scription of hardware and programming techniques. We conclude with a discussion of future devel- opments in neurostimulation. JAMA Neurol. 2013;70(2):163-171. Published online November 12, 2012. doi:10.1001/2013.jamaneurol.45 Deep brain stimulation (DBS) has evolved recovery.1-4 New applications continue to as an important therapy for the treat- emerge, encouraged by past successes and ment of essential tremor, Parkinson dis- the fact that DBS effects are reversible al- ease (PD), and dystonia, and it is also lowing exploration of new targets and ap- emerging for the treatment of medication- plications not previously possible with le- refractory psychiatric disease. Food and sion surgery. The history of DBS is a Drug Administration approval was granted fascinating example of the interplay be- in 1997 for thalamic DBS for essential tween basic and clinical research. It is the tremor and PD-related tremor, followed in coming together of these 2 arenas that has 2003 by approval for subthalamic nucleus led to the evolution of DBS for the treat- (STN) and globus pallidus internus (GPi) ment of disease as it is used today and will DBS for PD. A humanitarian device ex- be used tomorrow. Table 1 summarizes emption for STN DBS and GPi DBS for milestones in the evolution of surgical primary generalized and segmental dys- therapy for movement disorders. tonia was granted in 2003 and for obses- sive-compulsive disorder, in 2009. Deep CURRENT APPLICATIONS brain stimulation has also been used suc- AND OUTCOMES cessfully in the treatment of Tourette syn- drome, depression, and epilepsy, and there Tremor are case reports of using DBS for the treat- ment of headache, pain, vegetative state, Deep brain stimulation is an attractive al- addiction, obesity, dementia, and stroke ternative to surgery for the management of tremor. Surgical ablation of the ventral Author Affiliations: Department of Neurology and Neurotherapeutics, University intermediate nucleus of the thalamus has of Texas Southwestern Medical Center, Dallas (Drs Miocinovic and Chitnis); and been used as a therapy for tremor since the Department of Neurology, University of Minnesota, Minneapolis (Drs Somayajula 1950s.8 However, bilateral thalamotomy and Vitek). is not well tolerated because of the risk of JAMA NEUROL/ VOL 70 (NO. 2), FEB 2013 WWW.JAMANEURO.COM 163 ©2013 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/27/2021 Parkinson Disease Table 1. Evolution of Surgical Therapy for Movement Disorders One of the primary clinical uses of DBS is for the treat- ment of PD. A robust motor response to levodopa is gen- 1890 Horsley5 performed extirpation of the motor cortex for treatment of athetosis. erally considered a prerequisite for successful DBS out- 1947 Spiegel et al6 described a stereotactic frame. come in PD (except for tremor-predominant PD), and 1950 Spiegel et al7 made lesions in patients with PD to stimulation may be considered once patients develop dis- interrupt pallidofugal fibers causing improvement in abling motor fluctuations and dyskinesias while receiv- bradykinesia, rigidity, and tremor. ing medical therapy. Although thalamic stimulation has 8 9 1950s Hassler and Riechert and Talairach et al treated been effective in controlling parkinsonian tremor, the lack parkinsonism with lesions in the VL thalamic nucleus. Cooper10 attempted to section the cerebral peduncle of a reliable effect on other motor symptoms has limited but inadvertently interrupted the anterior choroidal thalamic DBS for the treatment of PD.45,46 Today, the STN artery and was forced to ligate it, leading to and GPi are the most commonly used targets in PD.20,21 disappearance of rigidity and tremor with preserved Electrode placement in the STN was initially favored be- motor and sensory function. 1963 Albe Fessard et al11 reported that stimulation in the area cause of reports that it yielded greater improvement in of the ventrointermediate nucleus of the thalamus at motor scores and a greater reduction in antiparkinso- frequencies of 100-200 Hz improved tremor in nian mediations compared with placement in the GPi.27,47 patients with parkinsonism. Additional studies have shown that GPi DBS also signifi- 1969 Levodopa was introduced, parkinsonian symptoms were 12 cantly improved the cardinal motor symptoms, drug- improved, and stereotactic surgery fell out of favor. 23,24,32,39 1987 Benabid and colleagues13 heralded the modern era of induced dyskinesia, and motor fluctuations. Al- DBS through their publication of thalamic DBS though STN remains the preferred target, GPi can be contralateral to thalamotomy in patients with tremor. considered in patients who have speech, cognitive, and 1989-1990 Albin et al14 and DeLong15 introduced a model of basal mood disturbances, as STN DBS can sometimes worsen ganglia function based on the hypothesis that there these symptoms.32,39 were segregated circuits within the basal ganglia thalamocortical network, each serving a different Studies of DBS for PD have reported significant im- function. provement in cardinal motor signs, including tremor, bra- 1992 Laitinen and colleagues16 reintroduced the Leksell dykinesia, and rigidity, with variable response in medi- pallidotomy technique for patients with advanced PD cation-refractory gait freezing, postural instability, and along with severe adverse effects from levodopa gait mechanics (Table 2). Marked benefits in improve- therapy. 1998 Documentation of safety and efficacy of bilateral STN ment of levodopa-related complications such as drug- DBS by Limousin et al,17 including its potential for induced dyskinesia, motor fluctuations, and off-period reducing the dose of dopaminergic medications in dystonia have also been demonstrated.29 Adverse effects patients with advanced PD. are typically transient and reversible.17,39 Additional limi- 18 2000 Coubes et al presented data for GPi DBS in treatment tations of DBS therapy that need to be considered prior of dystonia. to surgery include risk of hemorrhage or infection, risk Abbreviations: DBS, deep brain stimulation; GPi, globus pallidus internus; of mechanical failure (now much less common as both PD, Parkinson disease; STN, subthalamic nucleus; VL, ventrolateral. physicians and manufacturers develop more familiarity with the device), frequent follow-up visits, and cost of speech and swallowing deficits. Thalamic DBS has been the device and battery replacements. shown to be efficacious in the treatment of essential and parkinsonian tremor, with excellent long-term out- Dystonia comes and an acceptable adverse effect profile (Table 2). The main adverse effects of the stimulation Deep brain stimulation has also been useful for treat- are paresthesias, headache, dysarthria, paresis, gait dis- ment of primary dystonia. Renewed interest in pal- turbance, and ataxia.40 Adverse effects are usually mild lidotomy for PD in the early 1990s and the observation and effectively managed by stimulation parameter ad- that it improved dystonic symptoms in PD led to the pro- justment. Deep brain stimulation and thalamotomy posal of using pallidotomy for patients with primary gen- have also been used with less success in the treatment of eralized dystonia.48,49 Given concerns about bilateral GPi action tremor. This type of tremor typically occurs in lesions causing speech and cognitive deficits as seen in patients with multiple sclerosis, trauma, or stroke that PD, it was not long before GPi DBS was being explored leads to interruption of cerebellar outflow pathways for the treatment of primary generalized dystonia, some- and has a more complex pathophysiology.41 Clinical times with remarkable outcomes.18,25,50,51 Unlike tremor improvement in these patients is often short lived and, and PD, there is typically a gradually increasing clinical in the case of multiple sclerosis, complicated by disease response to stimulation over weeks to months of therapy. progression.42,43 Although treatment for tremor targets Efficacy of DBS in primary generalized and segmental dys- the ventral intermediate nucleus, several studies have tonia has been well documented35 (Table 2). There has suggested that the posterior subthalamic area is a better been no difference in outcomes based on DYT1 gene sta- location and that patients may be incidentally benefit- tus,31 but shorter disease duration has been
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