Neurosurg Rev DOI 10.1007/s10143-014-0588-9

REVIEW

Unusual complications of deep brain stimulation Fumin Tong & Adolfo Ramirez-Zamora & Lucy Gee & Julie Pilitsis

Received: 24 February 2014 / Revised: 1 May 2014 / Accepted: 22 June 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Deep brain stimulation (DBS) has emerged as a successful therapy for the treatment of several neurological disorders with potential implications in management of psychiatric disease. A variety of well-characterized hardware and surgical complications have been reported after the procedure, including postoperative hardware infection, system failure, and intracranial hemorrhage. Fortunately, serious surgical complications are rare, but they can lead to immediate or long-term disability. As the number of patients undergoing DBS continues to increase, newer and less common complications continue to emerge. It is imperative that clinicians become familiar with these complications in order to promptly recognize them and institute adequate early treatment. In this report, we examine the occurrence of unusual complications after DBS with emphasis on surgical, hardware, and stimulation-related complications. Keywords DBS . Complications . Intracranial hemorrhage . Infection

Introduction Deep brain stimulation (DBS) is an effective treatment for a variety of medically refractory movement disorders including advanced Parkinson disease (PD), generalized and segmental dystonia, and essential tremor (ET) [2, 19, 29, 37, 87]. Evolving techniques and newer targets continue to expand F. Tong : A. Ramirez-Zamora (*) Department of Neurology, Albany Medical College, 47 New Scotland Ave, Albany, NY 12208, USA e-mail: [email protected] L. Gee : J. Pilitsis Department of Neurosurgery, Albany Medical College, 47 New Scotland Ave, Albany, NY 12208, USA

the spectrum of diseases treated with DBS. Multiple reports have addressed the occurrence of serious surgical and hardware complications after DBS. However, reporting of other less well-recognized, infrequent complications following surgery has been scarce. It is important to emphasize that assessing the actual occurrence of infrequent DBS complications is difficult because such complications tend to be underreported. Complications typically are published only if they are truly unusual, and reporting of more common adverse effects requires large samples. The management of these complications remains unclear due to the paucity of cases. Nevertheless, it is critical that physicians become familiar with these adverse effects not only to provide accurate diagnosis but also to implement early, disease-specific treatment. In this article, we have reviewed uncommon complications reported after DBS. We conducted a PubMed-based literature search for papers published between 1990 and June 2013. Keywords used were “deep brain stimulation,” “DBS,” “subthalamic stimulation,” “adverse event,” “pallidal stimulation,” “surgery,” and “complications.” Relevant references were chosen and an additional cross-reference search was also carried out in the retrieved manuscripts. Unusual adverse events observed during perioperative and long-term follow-up periods were selected and individually analyzed.

Surgical complications Serious surgical complications of DBS are infrequent. Multicenter studies have reported similar rates of postoperative complications, with a 30-day perioperative mortality of 0.4 % and permanent neurologic morbidity around 1 % [35, 84]. Permanent neurological sequelae are generally thought to result from intracranial hemorrhage (ICH), but less reported are the effects of ischemia or venous infarction. Some groups

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have suggested that the number of microelectrodes used for intraoperative microelectrode recordings (MER) can be a risk factor for ICH, while others found no or minimal bleeding with MER [62, 76, 89]. In cases where added force is needed to pass the cannula through the cortex, hemorrhage along the tract has been reported [41]. Use of microelectrodes with stepoffs may also result in increased risk of ICH [59]. In most cases of ICH, acute evacuation or hardware revision is not necessary as most patients improve with supportive treatment [5, 8, 22, 26, 33, 36, 71, 79]. Subcortical ischemic strokes in the internal capsule and thalamus have been observed after subthalamic (STN) DBS [31, 53, 72]. Retrospectively, difficulties with neurophysiological mapping, silence during MER, and delayed clinical effects with stimulation have been noted. The etiology of DBS-associated ischemia remains unclear, as does the incidence, which may be more frequent than presently recognized due to delayed clinical symptoms and inconsistent MRI follow-up (Fig. 1). Possible mechanisms include preexisting vascular disease, uncontrolled blood pressure, small vessel vasospasm induced by electrical stimulation, edema, or mechanical irritation. There are publications suggesting that age, gender, perioperative hypertension, and use of anticoagulants, including aspirin, are predisposing factors for ICH, and whether this holds true for ischemia needs to be defined [8, 69]. Furthermore, pediatric patients treated for dystonia seem to have the highest risk of ICH [27]. Whether this is due to age, the vascularity of the globus pallidus internus (GPi) in this cohort or the disease itself remains unclear, and thus, the incidence of ischemia in this group should be carefully monitored. Additionally, transient neurological deficits may also result from cerebral edema [57]. When focal deficits occur in the initial 24–48 h postoperatively, peri-electrode edema, which occurs in 0–6.3 % of cases, should be considered [17]. Perielectrode T2 hyperintensities can occur and typically are not recognized unless postoperative neuroimaging is obtained. The occurrence of symptomatic peri-electrode edema is less predictable. Deogaonkar et al. [14] published a retrospective case series of eight patients who underwent DBS for PD or dystonia and developed symptomatic edema. Thirty MER passes were performed in this cohort, with an average of 3.75 tracts per lead. Clinical and radiological onset of edema located near the electrode tip, subcortical region, and/or around the entire electrode were observed on average 27 days after surgery (range 4–120 days). Symptoms included headaches, focal neurological deficits, seizures, or worsening of preexisting symptoms. Workups showed patients had no systemic infection or allergic reaction. Symptoms resolved completely over 33 days on average after treatment with low-dose steroids for 2–3 weeks. Although no correlation was found between the number of MER tracts and the size and timing of edema, there was positive correlation with the duration of edema resolution.

Fig. 1 MRI image of lacunar infarct following DBS implantation. Follow-up MRI T2-weighted axial image revealed lacunar infarct in a patient 6 months after right GPi DBS for dystonia. She remained neurologically well

Cerebral venous infarction should also be considered as part of the differential diagnosis of ischemia. A recent retrospective review reported four cases (0.8 % per lead, 1.3 % per patient) of symptomatic cerebral venous infarction out of 500 DBS lead implantation procedures performed over 7 years [50]. All four patients developed neurological symptoms on postoperative day 1. In all cases, symptoms resolved after supportive care including head elevation, blood pressure control, fluid resuscitation, and rehabilitation therapy. Air embolus may be another uncommon cause of ischemia, with a reported incidence of 1.3–4.5 % per procedure [12, 28], likely because these cases are performed in awake patients in a recumbent position. Intraoperative venous air embolism (VAE) presents with coughing, tachypnea, and hypoxemia and can be life-threatening if unrecognized. Response should include flooding the field with irrigation and placing the patient in Trendelenburg or left lateral decubitus position along with close monitoring. Rare surgical complications have been reported in stage II procedures secondary to the tunneling process for extension placement. Tambasco et al. reported the development of progressive intense pain over the left parietal-occipital region in a 68-year-old woman following DBS, with a pulsatile mass in synchrony with the heartbeat found on examination [73]. A giant pseudoaneurysm of the distal occipital artery near the extension lead was identified on angiography and repaired by occlusion of the terminal branch of the occipital artery. Other tunneling injuries also occur similar to those which have been reported in tunneling of a ventriculoperitoneal shunt. In shunt placements, skin violation, pneumothorax, hydrothorax, and

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atlantoaxial rotatory fixation following tunneling have been described [15, 25]. Although known as common adverse events in ventriculoperitoneal shunt, these complications are rarely described as DBS complications, likely secondary to development of the surgical technique and underreporting of the cases in the literature.

Hardware complications Postoperative hardware complications have been observed in a reported range of 1.5–36 % of DBS patients [60, 76, 83]. Commonly, these include lead fracture, lead extension fractures, hardware infections (battery, connector, or both), skin erosion, internal pulse generator (IPG) failure, component malfunction, electrode misplacement, and migration [24]. IPG infections occur in approximately 5–8 % of DBS cases, requiring antibiotic treatment and frequent removal of the hardware. Nevertheless, only seven cases of intracerebral infections have been reported [9, 46, 82]; thus, this could be the most underreported complication of all. Aseptic cysts have been reported to occur months after DBS placement [64]. Patients in these cases presented with new-onset neurological deficits (Fig. 2) and were treated with removal of hardware. Cultures were taken and were negative. Over time, another set of complications may result secondarily to the body’s reaction to the device or device malfunction. Miller et al. described six patients with moderate to severe “wire tethering” leading to restriction of movement [47]. Janson and colleagues published a retrospective case series describing similar phenomena as “bowstringing” [30]. Six of 228 DBS cases were reported to have abnormal tethering of leads between the pulse generator and stimulating electrode that may have resulted in discomfort and equipment malfunction. Anecdotally, these cases are more common in patients with dystonia or repetitive head and neck motion movements due to tremor (Fig. 3) [10, 23]. Lead migration is uncommon and reports are limited to case reports [60]. Morishita et al. also reported a case of neurological deterioration in a 7-year-old child who underwent bilateral GPi DBS and was found to suffer from dorsal lead migration likely secondary to skull growth in a year [49]. Piacentini and colleagues observed a case of remarkable behavioral complications after bilateral GPi stimulation, which were attributed to ventral lead migration to the left amygdala [61]. Hardware-related complications may result from individual patient factors. Geissinger et al. [21] reported a case of compulsive manipulation of the IPG device through the skin termed “Twiddler’s syndrome,” which resulted in the twisting and fracture of the leads and IPG movement. Women with considerable breast tissue may experience difficulty with IPG sagging. We have also seen erosion of the battery through the

Fig. 2 MRI image of a cyst following DBS implantation. Four months postoperatively, MRI T1 axial image depicted a cyst when patient developed new-onset paresthesias and weakness. Removal of the DBS system led to immediate improvement in the patient’s symptoms and long-term resolution of the cyst

chest wall site due to patient manipulation of the incision. Romito et al. reported a rare case of a 65-year-old male patient who developed herpes zoster along the right anterior T4 dermatome at the IPG site [65]. Other rare device-related adverse events include unexplained switching off and cable dehiscence [66]. Migration and fracture may also occur. When concerned, we obtain Xrays of the system and check electrode impedances. Many extensions lose their radiopacity over time, and thus, X-rays alone may not determine a break. If batteries or connectors have moved, our index of suspicion is higher. On initial placement, connectors should be placed above the level of

Fig. 3 A chest X-ray revealed a twisted left DBS extension lead in a patient with severe dyskinesias during the postoperative period

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the pinna and sutured. To avoid erosion (Fig. 4), the cranium can be drilled down at the connector site. This technique can also be used at burr hole sites. In cases where patients have thinner scalps, we suggest drilling out a portion of the calvarian inner table to make the extension more flush with the skin. We do advise all patients to avoid shaving their heads “to the skin” after undergoing this surgery to avoid potential hardware and scalp compromise.

Unusual stimulation-related complications Both motor and non-motor complications may occur postoperatively despite significant motor benefit from DBS. These complications are related to the specific target being stimulated and potentially the disease being treated. They occur when stimulation spreads to neighboring regions and are generally reversible. The most common adverse events include cognition and behavioral decline, depression, dysarthria, dysphagia, dysequilibrium, gait disturbances, dyskinesias, dystonia, weakness, eyelid-opening apraxia, drooling, orthostatic hypotension, double vision, pain, and muscle spasms [24, 80]. Postsurgical suicide is the most worrisome behavioral effect. The estimated suicidal rate is 0.45–4.3 % irrespective of excellent motor outcome following DBS [11]. Subthalamic nucleus Several randomized clinical trials revealed a higher incidence of cognitive adverse events after STN DBS, including hypomania and acute depression, when compared to GPi DBS for PD [1, 3, 4, 7, 19, 24, 39, 40, 52, 54, 63, 68, 78, 85]. Additionally, Romito et al. documented two cases of hypersexuality in high-frequency stimulation of the STN in PD [67]. Motor complications such as unilateral blepharospasm, buccinator spasm [66], and restless leg syndrome [80] are uncommon but have been reported. Kataoka et al. also described a patient with PD who had sudden respiratory difficulty due to a fixed epiglottis after STN DBS, which was aggravated by increasing the voltage of the STN stimulator [32]. In cases where stimulation-related side effects are suspected, the use of different settings and/or less stimulation can be attempted. Low et al. also presented a case of reversible pathological crying in a 48-year-old woman following bilateral STN DBS implantation with stimulation of a contact near the left internal capsule region [43]. In one of our patients, we were able to evoke uncontrollable laughter with contact 0 despite appropriate lead location within ventral STN, possibly due to spreading to the substantia nigra reticulata or stimulation of the limbic STN territory. Pseudobulbar laughter and crying has also been reported with neurostimulation [38, 55, 88].

Fig. 4 This picture was sent by a patient via email showing what he thought was “a staple” remaining in his head. In fact, it was a portion of the exposed lead approaching the connector

Globus pallidus interna A number of motor complications have been described following GPi stimulation for dystonia, including hypokinetic gait disorder with freezing of gait [70] as well as new difficulties with coordination, bradykinesia, rigidity, balance, and walking involving previously nondystonic body regions [6, 56, 90]. Compared to STN DBS, GPi stimulation has fewer cognitive or behavioral concerns. Miyawaki et al. reported a rare case of recurrent mania episodes associated with chronic GPi DBS for a PD patient [48]. Additionally, Foncke et al. also reported that 2 of 16 patients with dystonia undergoing bilateral GPi stimulation committed suicide after follow-up periods of 3 weeks and 14 months [20]. It is essential for all patients to be preoperatively assessed for depression. At-risk patients should be identified and a multidisciplinary treatment plan implemented before and after the surgery. Ventral intermediate nucleus of the thalamus Stimulation of the ventral intermediate (VIM) nucleus of the thalamus is most commonly used for medication-resistant, disabling essential tremors (ET) [44, 51, 58, 86]. The most common adverse events in ET patients with bilateral implants include dysarthria, ataxia, pain, paresthesia, asthenia, insomnia, hypophonia, somnolence, and dysphagia [58]. Abnormal eye movements have also been reported as a rare stimulationinduced complication of DBS. Taylor et al. presented a case of a 34-year-old woman who developed transient stimulationassociated central nystagmus after chronic electrical stimulation of the centromedian nucleus of the thalamus to treat refractory seizures [74]. The localization of the nystagmogenic area represents a region likely involved in optokinetic nystagmus generation.

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Other rare complications

References

Clinicians must also take into account medication- and disease-related factors in patients undergoing surgery. In PD patients, four cases of Parkinsonism-hyperpyrexia syndrome (PHS), a rare but life-threatening neurological complication observed after discontinuation or abrupt reduction of levodopa, have been reported [18, 34, 42, 77]. Patients are required to be off PD medications for CAPSIT testing and for surgery. Symptoms of PHS include altered mental status, fever, muscle rigidity, and autonomic instability including tachycardia and labile blood pressure. Longer medication withdrawal seems to contribute to a higher incidence of PHS as illustrated by a case reported by Kim et al. [34] resulting from presurgery discontinuation of levodopa two times longer than the usual 12-h overnight withdrawal. A quick diagnosis and proper management of this syndrome is critical, including reinitiation of dopaminergic drugs, maintenance of fluid and electrolytes, and supportive therapy of systemic complications. In dystonia patients, dystonic storm or status dystonicus is a rare but life-threatening condition in which patients present with severe generalized hyperkinetic dystonic spasms [16, 45, 75, 81]. Multiple medical issues such as trauma and infection can trigger dystonic storm. No standard treatment is established, although successful treatment has been reported by using dopamine blockade with nonselective agents such as pimozide, risperidone, olanzapine, or haloperidol and sedation with propofol and midazolam. Intrathecal baclofen or emergent DBS also have been reported to treat dystonic storm successfully [13]. ICU care with supportive therapy is warranted in most cases.

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Conclusions Overall, DBS has been shown to be a safe and effective treatment for several neurological disorders. Serious complications with permanent sequelae are rare, and most of the adverse events are abridged with increasing surgical experience, development of new surgical equipment, and implementation of new surgical techniques. Appropriate patient selection and preoperative planning are essential components to optimize outcomes and minimize adverse events. Recognition and familiarity with rare DBS complications can facilitate the correct diagnosis and treatment and will improve outcomes as clinicians more frequently encounter patients with DBS and its complications. The creation of a national registry of DBS cases should be entertained, as it would provide unique insight into the prevalence and management of less reported events.

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Comments Selçuk Peker, Istanbul, Turkey DBS surgery has been carried out with various indications for the last few years. Using this method, it has been possible to offer thousands of patients a better quality of life. However, as with any surgical technique, experience is paramount in DBS surgery. The rate of complications is much lower in experienced clinics. The duration of surgeries in clinics that treat multiple cases is much shorter, making this a factor in decreasing complication development in older patients. According to some authors, microelectrode recording is a reason for this increase in intracranial complications. However, our experience indicates that this is not quite the case. The selection of cases is an important factor. It is necessary to work with experienced movement-disorder specialist neurologists as a team; otherwise, systemic problems become an invitation to complications. In my opinion, another crucial thing is to report such cases when they arise without hesitation. This way, other colleagues would be informed by these experiences. A lot of very interesting complications come up in various meetings among colleagues but remain unreported. It is foreseen that the frequency of DBS surgery will increase in the upcoming years, as well as the variety in its complications.