| Abstract|| |
Despite advancements in pharmacotherapeutic and behavioral interventions, a substantial proportion of patients with obsessive-compulsive disorder (OCD) continue to have disabling and treatment-refractory illness. Neurosurgical interventions, including ablative procedures and deep brain stimulation (DBS), have emerged as potential treatment options in this population. We review the recent literature on contemporary surgical options for OCD, focusing on clinical aspects such as patient selection, presurgical assessment, and safety and effectiveness of these procedures. Given the invasiveness and limited evidence, these procedures have been performed in carefully selected patients with severe, chronic, and treatment-refractory illness. Along with informed consent, an independent review by a multidisciplinary team is mandated in many centers. Both ablative procedures and DBS have been found to be helpful in around half the patients, with improvement observed months after the procedure. Various targets have been proposed for either procedure, based on the dominant corticostriatal model of OCD. There is no strong evidence to recommend one procedure over the other. Hence, the choice of procedure is often based on the factors such as affordability, expertise, and reversibility of adverse effects. Surgery is not recommended as a standalone treatment but should be provided as part of a comprehensive package including medications and psychotherapeutic interventions. Available evidence suggest that the benefits of the procedure outweigh the risks in a treatment-refractory population. Advances in neurosurgical techniques and increasing knowledge of neurobiology are likely to bring about further progress in the efficacy, safety, and acceptability of the procedures.
Keywords: Deep brain stimulation, neurosurgery, obsessive-compulsive disorder, psychosurgery, treatment resistance
|How to cite this article:|
Balachander S, Arumugham SS, Srinivas D. Ablative neurosurgery and deep brain stimulation for obsessive-compulsive disorder. Indian J Psychiatry 2019;61, Suppl S1:77-84
| Introduction|| |
Evidence-based guidelines recommend selective serotonin reuptake inhibitors and/or behavior therapy as first-line treatments for obsessive-compulsive disorder (OCD).,, However, around 40%–60% do not respond adequately to either treatment., Around 30% of such patients respond to augmentation with antipsychotics., It has been estimated that around 10%–20% of OCD patients are refractory to all available pharmacological and psychological treatments.,,, Many of these patients have chronic, severe, and disabling symptoms causing significant social and economic burden. Neurosurgical treatments have a role in this population, that is, patients with chronic and severe OCD, who are refractory to available noninvasive treatment strategies.
The advent of stereotactic surgical techniques and advances in neuroimaging in the last few decades have greatly enhanced the specificity and accuracy of targeting in brain surgeries. This is in stark contrast to the earlier procedures such as prefrontal leukotomy and lobotomy, for which the term “psychosurgery” has unfortunately become synonymous with. Contemporary neurosurgical procedures involve either creation of small lesions in the order of millimeters (ablative surgery) or implantation of electrodes in very specific subcortical regions for neuromodulation (deep brain stimulation [DBS]). Refinements of targets based on the experience and understanding of neurobiology have improved the safety and efficacy of these procedures.,,
Careful evaluation and selection of patients for psychosurgery is another area which has improved since the era of lobotomies. As the efficacy and safety of surgical interventions have not been firmly established, they are still considered experimental treatments and generally recommended only in patients with chronic, severe, highly disabling, and treatment-refractory OCD., The suitability of an individual patient for surgery is evaluated by institutional and extramural review boards in most centers. Mental health legislation in most countries (including the Mental Health Care Bill 2017 in India) also stipulate norms for informed consent and the drawing up of review boards and monitoring committees.
In this article, we review the current status of neurosurgical treatment for OCD, providing an overview on clinical aspects including patient selection, consent/review process, a brief description of contemporary surgical procedures, and postoperative follow-up. Neurobiology and neurocircuitry underlying the surgical procedures are beyond the scope of this review and readers are referred to other excellent reviews on these aspects.,
| Treatment Refractoriness in Obsessive-Compulsive Disorder and Candidate Selection|| |
The minimum basic criterion is treatment refractoriness, that is, to establish that the patient has not responded to evidence-based noninvasive treatments including pharmacological and psychological treatments. Most centers operationalize these criteria, by requiring the subject to be nonresponsive to at least three adequate trials of serotonin reuptake inhibitors (including clomipramine) and an adequate trial/intolerance to cognitive-behavioral therapy (CBT). The illness should be of sufficient severity to cause significant socio-occupational dysfunction. Most centers exclude individuals with comorbid psychosis, bipolar disorder, and severe personality disorders. Those with medical comorbidities which may impact surgical fitness, especially for DBS, are excluded from the study. DBS requires regular postoperative follow-up for programming and monitoring of effects/adverse effects; hence, the access to postoperative follow-up is an important consideration. The criteria have been laid out in the most recent Indian Psychiatric Society Clinical Practice Guidelines (IPS-CPG) for OCD, as shown in [Table 1].
|Table 1: Selection criteria for psychosurgery in obsessive-compulsive disorder as per the Indian Psychiatric Society Guidelines (Reddy et al., 2017)|
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Informed consent has to be undertaken after ensuring that the patient and caregivers understand clearly the expected outcomes of the procedure (including the latency, probability, and extent of treatment response), alternative treatments available, and need for continuation of standard treatments including medications/behavior therapy following surgery and risk of adverse events.
| Presurgical Workup|| |
The diagnosis of OCD and the presence of other comorbidities should be carefully evaluated by the primary treating team, preferably supplemented using standardized instruments such as the Mini International Neuropsychiatric Interview or Structured Clinical Interview for DSM-5 (SCID-5). Symptom severity, as measured by standard scales such as the Yale-Brown Obsessive Compulsive Scale (Y-BOCS), would be helpful in assessing baseline severity and monitoring for treatment response. It is important to review prior pharmacological treatment history, including the dose, duration, and adherence to treatment to establish treatment resistance. Adequacy of CBT can be assessed by reviewing the number, frequency and regularity of sessions, number of attempts at CBT, and whether the CBT involved OCD-specific interventions such as exposure and response prevention (ERP).
Comprehensive physical and neurological examinations have to be performed and documented. The surgical procedures are commonly performed under local anesthesia. Hence, basic blood investigations should suffice. A structural magnetic resonance imaging (MRI) brain (T1, T2) is done to rule out any other brain pathology. The subject would also have to undergo another MRI of the brain with the stereotactic frame fixed (generally performed on the day of surgery) for stereotactic guidance. An electroencephalogram is not routinely mandated but may be carried out if the patient has had any history of seizures, as there is a slight risk of postoperative seizures.
Neuropsychological testing would include tests for intelligence, attention, memory, and the frontal lobe functioning, for example, Frontal Assessment Battery. A personality assessment using dimensional measures (such as the Minnesota Multiphasic Personality Inventory-2 or NEO-Personality Inventory) or a structured interview (IPDE or SCID-II PD), though not recommended by any guideline, may also be carried out.
| Independent Multidisciplinary Review|| |
Most centers seek review by independent experts to confirm eligibility for surgery. The IPS-CPG for OCD recommends evaluation by an independent review committee, consisting of a psychiatrist, a neurologist, and a neurosurgeon, who are not directly involved in the patient's treatment before each patient is considered for surgery. The Mental Health Care Act, 2017 mandates the consent of the Mental Health Review Board for surgery.
| Neurosurgical Approaches and Current Evidence|| |
The neurosurgical techniques commonly employed for the treatment of OCD include ablative neurosurgery and DBS. Ablative surgery was previously performed using thermocoagulation (using cautery or radiofrequency ablation) which required burr hole craniotomy. This has been replaced to a large extent by gamma-knife surgery, especially for anterior capsulotomy. The lesions in gamma-knife surgery are made by focusing radiation from a Cobalt-60 source to specific sites in the brain, stereotactically guided using MRI and computed tomography (CT) images. The key advantage of this procedure is that it is less invasive and does not entail significant damage to surrounding brain tissue and thus has a lesser risk of immediate postoperative adverse events. The common targets for ablative surgery in OCD including:
- Anterior cingulate gyrus and the cingulum bundle (Anterior cingulotomy)
- Anterior limb of internal capsule (Anterior capsulotomy)
- Corticostriatal tracts ventral to the head of the caudate nucleus (Subcaudate tractotomy).
Among these, anterior capsulotomy is the most widely used procedure and has the largest evidence base.
The ventralmost portion of the anterior limb of the internal capsule (ALIC) has fibers that relay from the prefrontal cortex to the basal ganglia structures, including the striatum. This is the target for anterior capsulotomy. The most commonly used technique, known as “Gamma Ventral Capsulotomy (GVC),” involves creation of the very small lesions in the ventral portion of ALIC using gamma rays.,, [Figure 1] shows MRI images of a patient taken before and 3 months following gamma-knife capsulotomy. Owing to the minimally invasive nature of gamma-knife surgery and the small size of the lesion, the procedure is safe, has very quick postoperative recovery.
|Figure 1: T1 magnetic resoncance images of a patient who underwent gamma knife capsulotomy before (left) and 3 months after the procedure (right)|
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Anterior cingulotomy is a popular procedure in the USA and has been extensively performed at the Massachusetts General Hospital. The anterior cingulate cortex (Brodmann area 24 and 32) along with the underlying white matter tract known as the cingulum bundle are targeted in this procedure. As this requires a larger lesion, it is typically done using thermocoagulation through burr holes under stereotactic guidance and local anesthesia. The anterior cingulate cortex is involved in error monitoring, which is implicated in the pathophysiology of OCD. Further, the cingulum bundle is an important white matter relay in the cortico-striato-thalamo-cortical circuit. Nonresponders to anterior cingulotomy may benefit from a repeat cingulotomy which involves extension of the lesion or by undergoing additional subcaudate tractotomy.,
Deep brain stimulation
DBS is done in three stages. The first stage, involves surgery for stereotactic image-guided insertion of electrodes through bilateral burr holes, performed under local anesthesia and mild sedation. The electrodes have multiple contacts (usually 4 per side). Intraoperative “macrostimulation” is done for monitoring adverse effects. The patient is usually awake during the procedure. Hence, the effect of stimulation on speech and other critical motor functions can be monitored “on table.”
The common targets for DBS electrodes in OCD including:
- ALIC, ventral capsule/ventral striatum (VC/VS), nucleus accumbens (NA), bed nucleus of stria terminalis (BNST): The above targets are close to each other, and there is a substantial overlap in the area of stimulation between the above targets. They can be collectively called “Striatal DBS” and are the most common areas targeted in DBS for OCD
- Subthalamic nucleus (STN): This is the most widely used site for DBS in idiopathic Parkinson's disease; hence, most neurosurgery centers have a greater degree of experience in electrode implantation at this site. Further, a recent evidence-based guideline recommended DBS over STN for OCD with Level-I evidence
- Others: inferior thalamic peduncle, medial dorsal nucleus of thalamus, and medial forebrain bundle. These targets have preliminary evidence and need replication.
The second stage involves subcutaneous implantation of the pulse generator, commonly in the infraclavicular space. Extension wires connecting the electrodes to the pulse generator are tunneled subdermally through the neck to the scalp. [Figure 2] shows image postoperative CT images of a patient who underwent DBS for Tourette's syndrome.
|Figure 2: Sagittal computed tomography image of a patient who underwent deep brain stimulation with leads in situ|
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The third stage involves programming. Various stimulation parameters such as polarity, amplitude, frequency, and pulse duration can be modulated to obtain a balance between effectiveness and adverse effects, which provides a flexibility in treatment. Programming is generally done on an outpatient basis using a handheld programming device which communicates wirelessly to the implanted pulse generator. For patients with Parkinson's disease and other movement disorders, programming is relatively straightforward as clinical improvement can be observed immediately after modulating the stimulation parameters. However, the improvement in OCD and other psychiatric disorders may be noticeable only after a few months of stimulation. Hence, the parameters are adjusted on a trial and error basis, based on adverse effects, immediate subjective effects on “mood,” “anxiety,” “energy,” and improvements in the OCD symptoms over long term.
Although the exact mechanism of DBS is not clearly known, it is postulated that the high-frequency stimulation of the regions results in a functional lesioning of the surrounding tissue, which may disrupt dysfunctional circuits. This inhibition has been explained through various mechanisms including depolarization blockade, exhaustion of neurotransmitter pool, and release of inhibitory neurotransmitters.
| Postsurgical Care and Follow-Up Management|| |
The immediate postoperative recovery from gamma-knife surgery is generally uneventful. Short-term prophylaxis with steroids is usually prescribed, as perilesional edema can occur due to the high dose of radiation administered. Radiological lesions following gamma-knife surgery can usually be identified 3 months following surgery. However, there is a latency for the onset of the therapeutic response, which generally occurs 6–12 months following the procedure. Pharmacotherapy should continue as usual during this period. CBT may be reattempted after this period. There are reports demonstrating improved tolerability for CBT with ERP after surgery (or DBS). Most patients require continuous pharmacotherapy and intermittent psychotherapeutic interventions over long term.
As the neuromodulatory effects of DBS appear earlier, it has been recommended that CBT may be reattempted even earlier, that is, within 1–2 months, as and when the patient recovers postsurgically and gets acclimatized to the device after adequate stimulus programming. However, the efficacy of DBS may be discernable only after months of continuous stimulation.
| Outcomes|| |
Evidence for the efficacy of anterior capsulotomy for OCD comes from several case series and one sham-controlled randomized trial. These reports have come from various centers worldwide, with minor variations in the procedure (dose of radiation used, “single-shot GVC” vs. “double-shot GVC”) and follow-up care. In the only randomized controlled trial (RCT) conducted till date, 16 patients were randomized to receive either “real” capsulotomy (n = 8) or “sham” surgery (n = 8) and were followed up for a period of 12 months. None of the patients in the “sham” arm improved, whereas two patients in the “true” showed response. Although there was no significant difference between the groups in the primary outcome measure (percentage of responders), the study was possibly under-powered to demonstrate such differences. Further, three additional patients in the active group and 2/4 patients in the sham group who underwent capsulotomy became responders during open long-term follow-up. Two meta-analyses of all published reports on anterior capsulotomy for OCD found mean response rates of 54% (range: 37%–50%, n = 5 studies, 50 patients) and 62% (n = 108, 10 studies). Recent large case series have found response rates between 56% (n = 55; 3-year follow-up) and 73% (n = 37; 5-year follow-up).
Predictors of outcome
There is very little data on predictors of response for surgery. The presence of hoarding and symmetry/ordering have been shown to predict poor response to ablative surgeries.
Gamma-knife capsulotomy is generally considered a safe procedure with few reports of serious adverse events. Immediate side effects of capsulotomy include headache, seizures, delirium, urinary incontinence, and cerebral edema. There is also a risk (5%) of radiation-induced delayed cyst formation, which can occur up to 5 years postoperatively. These cysts are commonly asymptomatic. Symptomatic cysts may require medical as well as surgical interventions. Thus, postoperative follow-up MRIs are recommended for screening for cyst formation. Weight gain (>10% of body weight) is a common (29%) long-term side effect of capsulotomy.,
Most outcome studies have also simultaneously reported pre- and postsurgical neuropsychological functioning. None of them have reported significant worsening in neuropsychological functioning following surgery. In the RCT, true GVC was found to improve visuospatial memory compared to sham GVC. Two other studies have compared neuropsychological functioning patients with severe treatment-refractory OCD who undergo capsulotomy versus those treated nonsurgically.,, Along with decrease in obsessive-compulsive symptoms, patients receiving GVC had improved neuropsychological functioning (verbal and visual memory, visuospatial skills, and executive functions). Earlier reports describe personality changes following thermocapsulotomy. However, recent reports on GVC have not found any deleterious effects on personality.,,,,
Deep brain stimulation
A meta-analysis of all DBS studies (n = 116) found a global Y-BOCS severity score reduction of around 45.1%, along with a response rate of 60%. No statistically significant differences between ventral striatum targets (n = 83) and the STN target (n = 27). Few studies have also monitored outcomes over long term, showing that the initial improvements are usually sustained during long-term follow-up. A recent study suggested that DBS targeting the BNST may yield better outcomes compared to other striatal areas, with response rates of 83% after ≥4-year follow-up. Despite the huge cost and the treatment-refractoriness of the study population, DBS has been found to be cost-effective over long term.,
Predictors of outcome
Meta-analyses show that older age of onset and the presence of sexual/religious obsession predict better outcomes to DBS. Induction of smile/laughter/mirth during intraoperative stimulation was found to strongly predict response to OC symptoms in striatal DBS.
Adverse effects may occur secondary to different aspects of the procedure including the following:
- Complications of the surgical intervention include intracerebral hemorrhage during lead implantation (0.2% to 5%), possibly higher with STN DBS. The risk postoperative infection is around 0%–15%, which can present as meningitis or more commonly as infection in the chest pocket, at the site of pulse generator implantation. The risk for immediate postoperative seizures is around 4%
- Device related: Breakage of lead or extension wire (around 2%) or device-related discomfort may occur. Depletion of battery can result in a rebound acute increase in anxiety and depression
- Adverse effects of the stimulation itself: Dyskinesia, dysarthria, eyelid apraxia, gait disturbances, depression/suicidal ideation, mania, increased libido, and micturition problems. These are generally reversible on modifying the parameters of stimulation.
Studies have not found any significant deterioration in neurocognitive functioning post-DBS., The available literature suggests that there are no deleterious personality changes following DBS.,,
| Deep Brain Stimulation Versus Ablative Surgeries – Which Procedure to Choose?|| |
There are no head-to-head trials comparing DBS and ablative surgeries. The available evidence in the form of independent reports are plagued with biases, with few blinded reports. A systematic review compared the outcomes of anterior capsulotomy with DBS in the striatal areas (ALIC, VC/VS, and NAc) using pooled data from independent reports. Although the difference in percentage of responders was not statistically significant between the two groups, capsulotomy was associated with greater decrease in Y-BOCS scores and more likelihood of remission. The main advantage of ablative surgery over DBS is its lesser cost and absence of “maintenance” hassles such as programming and battery changes. However, as the lesions are irreversible, it may result in long-term adverse effects.
In contrast, the effects of DBS are potentially reversible in that the stimulation can be modulated if there are intolerable adverse effects or no beneficial effects. DBS also has greater appeal due to its flexibility in terms of its programming and is becoming a useful investigative tool in the field of neuroscience. However, the cost of DBS is much higher and is known to have a longer learning curve. Hence, it is currently practiced only at highly specialized centers. In addition, the procedures for removal or repositioning of the implanted electrodes in case of nonresponse carries a risk of intracerebral hemorrhage. [Table 2] summarizes the main differences in the procedure of gamma-knife capsulotomy and their outcomes.
|Table 2: Key differences between gamma knife surgery and deep brain stimulation|
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| Conclusion|| |
Stereotactic ablative surgeries and DBS may be attempted in carefully selected patients with severe, disabling, and chronic treatment-refractory OCD. The commonly performed ablative surgeries include GVC and anterior cingulotomy. The most common targets for DBS in OCD include the VC/VS and subthalamic nucleus. Both procedures have similar outcomes, around 40%–60% of patients showing improvement 6–12 months following the procedure. The patient should be aware of the fact that surgery is not a standalone treatment and is a component of a comprehensive package of interventions for refractory OCD.
As OCD is a heterogeneous illness, it is rather unlikely that “one site may fit all” in terms of either lesioning or electrode positioning for DBS. There is a need to identify reliable predictors for treatment response, which would aid in patient selection.
Several advancements are already underway to increase the safety and specificity of the lesion in ablative surgery, such as MR-focused ultrasound. There are a few reports of anterior capsulotomy for OCD performed with magnetic resonance-guided focused ultrasound, which is a thermoablative procedure allowing intraoperative monitoring of the lesions in real time., “Closed-loop DBS” involves automated feedback loops for DBS, wherein the stimulation parameters are determined by electrophysiological parameters from the stimulation site. This would greatly help reduce the amount of charge used and prolong battery life of the DBS stimulators, thus reducing adverse effects and cost over long term. Another potential way of reducing the cost of DBS is through use of refurbished and resterilized pulse generators, an approach that has been attempted by cardiologists in India for pacemakers and implantable cardiac defibrillators., The safety and efficacy of these techniques have to be studied rigorously before wider clinical application.
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Conflicts of interest
There are no conflicts of interest.
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Dr. Shyam Sundar Arumugham
Department of Psychiatry, National Institute of Mental Health and Neurosciences, Bengaluru - 560 029, Karnataka
Source of Support: None, Conflict of Interest: None
[Figure 1], [Figure 2]
[Table 1], [Table 2]