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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 37  |  Issue : 4  |  Page : 208-214

Management of hardware infections in deep-brain stimulation: A 4-year, single-center experience


1 Department of Neurosurgery, Faculty of Medicine, Mersin University, Mersin, Turkey
2 Department of Neurology, Faculty of Medicine, Mersin University, Mersin, Turkey
3 Department of Neurosurgery, Neuro Spinal Hospital, Dubai, United Arab Emirates

Date of Submission07-Apr-2020
Date of Decision31-May-2020
Date of Acceptance06-Jun-2020
Date of Web Publication29-Dec-2020

Correspondence Address:
Vural Hamzaoglu
Department of Neurosurgery, Faculty of Medicine, Mersin University, Ciftlikkoy Campus, 33343, Yenisehir Mersin
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/NSN.NSN_43_20

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  Abstract 


Objectives: The introduction of deep-brain stimulation (DBS) was a milestone in the treatment of movement disorders, intractable epilepsy, and severe psychiatric disorders. We aimed to identify risk factors for hardware infection in patients with these conditions who underwent DBS at our center over a 4-year period. Materials and Methods: Bilateral DBS was performed in seventy patients by the Department of Neurosurgery at the Mersin University School of Medicine between April 2016 and January 2020. The surgical indication was Parkinson's disease in 48 patients, dystonia in 11 patients (10 primary generalized and 1 secondary), and tremor in 11 patients (10 essential tremor and 1 other). Results: Infection was detected in eight patients (11.4%). There were no hardware complications other than infection or postoperative intracerebral hematomas. The entire device was explanted in four (50%) patients with infection; device explantation occurred at 3, 13, 19, and 42 months after surgery. The other 4 (50%) patients who developed infection were successfully treated with antibiotics without complication. A patient with primary dystonia who underwent bilateral globus pallidus interna DBS sustained a severe acute subdural hematoma due to trauma 45 days after electrode implantation but prior to stimulation. We elected not to explant the device after hematoma evacuation; delayed stimulation programming was successful. Conclusion: DBS surgeries are susceptible to complications related to the anatomic target, hardware, and the procedure itself. Infection is the most common complication; however, there is no established protocol for its treatment. Antibiotics and partial removal of the device may be a rational approach.

Keywords: Deep-brain stimulation, infection, Parkinson's disease, subthalamic nucleus


How to cite this article:
Hamzaoglu V, Özalp H, Doğu O, Öksüz N, Aydın S, Akbıyık T, Dağtekin A, Avcı E, Bağdatoğlu C. Management of hardware infections in deep-brain stimulation: A 4-year, single-center experience. Neurol Sci Neurophysiol 2020;37:208-14

How to cite this URL:
Hamzaoglu V, Özalp H, Doğu O, Öksüz N, Aydın S, Akbıyık T, Dağtekin A, Avcı E, Bağdatoğlu C. Management of hardware infections in deep-brain stimulation: A 4-year, single-center experience. Neurol Sci Neurophysiol [serial online] 2020 [cited 2021 Jan 20];37:208-14. Available from: http://www.nsnjournal.org/text.asp?2020/37/4/208/305387




  Introduction Top


Deep-brain stimulation (DBS) is a well-known surgical treatment modality performed between the anterior and posterior commissure (AC/PC) [Figure 1] for patients with movement disorders resistant to medical therapy. Parkinson's disease (PD), essential tremor (ET), and dystonia are the main indications for surgery. However, DBS procedures may be complicated by infection, hardware malfunction, and intracerebral hematoma (ICH).[1],[2],[3],[4] The most frequent complication of DBS is infection. Surgical infection after DBS is typically associated with normal skin bacteria, such as Staphylococcus aureus and epidermidis , which contaminate the implant during surgery.[5],[6],[7],[8] The reported infection rate ranges from 1% to 16.2% in the English literature.[6],[9],[10],[11] Associated risk factors include male sex, number of previous internal pulse generator (IPG) replacements, type of prophylactic antibiotic, anatomic location of IPG, patient age, and medical comorbidities.[12] Hardware malfunction is seen in 4.9%–13.3% of patients undergoing DBS.[13],[14] Perhaps, the most feared complication is ICH resulting from electrode implantation into the brain parenchyma; ICH occurs in 0.2%–5.6% of patients.[15],[16] Previous studies have reported and discussed the potential complications and associated risks of DBS surgery. Here, we present our experience with seventy patients (141 implants) who underwent DBS surgery for movement disorders and discuss the relevant literature.
Figure 1: The panoramic postero-inferior view of a dissected cadaver showing the commissural line in vertical dots. Red arrow: Anterior commissure, Yellow arrow: Posterior commissure, T: Thalamus, SC: Superior colliculus, IC: Inferior colliculus, C: Cerebellum

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  Materials and Methods Top


Seventy patients with movement disorder underwent bilateral DBS surgery (141 implants) by the Department of Neurosurgery at the Mersin University School of Medicine in Turkey between April 2016 and January 2020. The anatomic stimulation targets were as follows: 96 subthalamic nucleus (STN), 23 globus pallidus interna (Gpi), and 22 ventral intermediate nucleus (VIM). The distribution of the contact depths of the STN, Gpi, and VIM targets for microelectrode recording (MER) (Leadpoint® System, Medtronic Japan Co., Ltd., Tokyo, Japan) and demographic patient data is shown in [Table 1]. All patients' follow-up was conducted by a single neurologist in the Department of Neurology at Mersin University. Preoperative anatomic targeting was performed using 1.5 Tesla magnetic resonance imaging (MRI) (Optima MR360 1.5T, General Electric Co., Boston, MA, USA). A Leksell stereotactic frame (Elekta, Stockholm, Sweden) affixed to the patient's skull was used for computed tomography (CT) localization of the selected surgical coordinates. Contrast-enhanced axial and coronal T1-weighted and axial T2-weighted images with 3-mm slice thickness were obtained the day before surgery with a 64-slice scanner. CT images (Aquillion 64, Toshiba Medical Systems, Tokyo, Japan) with 1-mm thickness were merged with the MRI images with the Leksell frame in place. These images were transferred to a Stealth surgical planning station, and target/trajectory planning was performed by reformatting the merged images with FrameLink 5.0 software (Medtronic, Inc., Minneapolis, MN, USA). In the first stage of the operation, the quadripolar electrodes (Model KN 1063, Medtronic, Inc.) were implanted while the patient was awake. The second stage of surgery consisted of pulse generator (Activa PC, Medtronic, Inc. Minneapolis, MN, USA) implantation under general anesthesia.
Table 1: The distribution of the contact depths of the subthalamic nucleus, globus pallidus interna, and ventral intermediate nucleus targets in the control of microelectrode recording with the demographic data of patients

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The Infectious Disease Department was consulted in all patients for appropriate prophylactic preoperative antibiotics: intravenous teicoplanin 800 mg and ceftriaxone 2 g were administered 3 h before incision to allow adequate time for diffusion of the drugs into the brain tissue.[17] In patients receiving anticoagulants, the drug was discontinued at least 10 days prior to the DBS procedure. All patients received a postoperative brain CT scan on the day after surgery in order to merge the preoperative MRI to check electrode placement.


  Results Top


The mean functional coordinates (x, y, and z) for the STN target were 11.48, 1.98, and 4.97 mm, respectively, on the left side on the mean anterior–posterior commissure line as 25.92 mm, whereas the mean x, y, and z coordinates were 11.26, 2.04, and 4.77 mm, respectively, on the right side. For the Gpi target, the mean functional coordinates (x, y, and z) were 18.89, 5.52, and 3.96 mm, respectively, on the left side on a mean AC–PC line as 24.17 mm, whereas the mean x, y, and z were 19.03, 5.61, and 3.81 mm on the right side, respectively. The mean functional coordinates (x, y, and z) were 14.11, 5.81, and 0 mm, respectively, for the VIM target on the left and right sides on a mean AC–PC line as 24.92 mm [Table 2].
Table 2: The mean values of the functional coordinates of subthalamic nucleus, globus pallidus interna, and ventral intermediate nucleus targets with the average of anterior commissure-posterior commissure line

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Of the seventy study patients, 31 (44.3%) were female and 39 (55.7%) were male. The mean patient age at the time of surgery was 49.8 (range, 18–74) years. The indication for DBS was PD in 48 patients, dystonia in 11 (10 primary and 1 secondary), ET in 10 patients, and Holmes tremor in one patient. Surgery at another center was previously performed in four of the 48 patients with PD: one who had a previous right thalamotomy underwent bilateral STN DBS because of an inadequate response to the previous surgery, and the other three had undergone previous STN DBS surgery, but the leads were not in the anatomic target when checked with CT scans, and no symptom relief was detected. Accordingly, these three patients underwent reimplantation for the same target. In the patient with Holmes tremor, bilateral stimulation of the VIM alone was inadequate; therefore, unilateral Gpi as an additional third stimulation target was added intraoperatively with a successful result [Figure 2]. One patient with primary dystonia (bilateral Gpi targets) sustained a severe acute subdural hematoma due to trauma 45 days after electrode implantation but prior to stimulation. We elected not to explant the device after hematoma evacuation; delayed stimulation programming was later successful [Figure 3] and [Figure 4].
Figure 2: The unilateral functional and frame coordinates of the two nuclei (ventral intermediate nucleus and globus pallidus interna) of the left side were demonstrated on the sagittal dissected cadaveric specimen with the commissural line as 22.47 mm. The axial section of computed tomography on the top right side shows also the distal contacts in the two different targets. ViM: Ventral intermediate nucleus, Gpi: Globus pallidus interna, DBS: Deep-brain stimulation, L: Left, C: Center, XL: X coordinate of the left side, YL: Y coordinate of the left side, ZL: Z coordinate of the left side, AC: Anterior commissure, PC: Posterior commissure

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Figure 3: (a) The coronal section of computed tomography showing the shift of the trajectory of the lead on the right side because of an acute subdural hematoma, (b) the sagittal section of computed tomography showing the trajectory of the lead, (c) the axial section of computed tomography showing the midline shift and also shift of the trajectory of lead on the right side because of an acute subdural hematoma, (d) the axial section of computed tomography showing the shift of the trajectory of the lead and the thickness of the hematoma on vertex level. GCS: Glasgow Coma Scale

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Figure 4: (a) The axial section of computed tomography showing the distal contacts of the lead on 1/18, (b) the axial section of computed tomography showing the distal contacts of the lead on 5/18, (c) the axial section of computed tomography showing the distal contacts of the lead on 9/18, (d) the axial section of computed tomography showing the distal contacts of the lead on 2/19

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Infection was observed in eight patients (11.4%). The entire device was explanted in four (50%) of the eight patients. One explantation was due to early infection (3 months); the other three patients experienced late infection and had the devices removed at 13, 19, and 42 months after surgery. Two of the three patients who had late explantations had a superficial infection early after surgery, both of which were initially treated with antibiotics alone and there were no signs of infection until the time of device removal. A common feature of the patients who underwent late explantation was obsessive behavior, such as scratching the cranial and subclavicular incision regions. The etiologic organisms, antibiotic therapy, and explantation times of the patients with DBS infections are presented in [Table 3]. No hardware complications or any misplacement of leads due to brain shift, and involvement of extension cables or IPG, were observed. No procedure-related ICH occurred.
Table 3: The distribution of etiologic agents and related antibiotic therapy of infected deep-brain stimulation patients including the explant of leads, extension cables, and internal pulse generator

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  Discussion Top


In recent years, DBS has been increasingly used in the treatment of PD and other movement disorders. Numerous large series have reported that centers that are experienced in performing DBS have both low complication rates and successful clinical results.[18],[19] However, infection, procedure-related ICH, and hardware complications are still encountered. In this report, we present our experience and complications. Previous studies have reported DBS infection rates ranging from 1% to 16.2%.[2],[6],[9],[10],[11] The risk of infection has been associated with previous surgery, patient diagnosis, target nucleus, and patient characteristics, including age, sex, comorbidities such as diabetes mellitus (DM), and smoking status.[6] Some studies reported that sex, smoking, and DM did not significantly increase the risk of postoperative infection.[16],[20] However, others found that infection was more likely in males and patients undergoing IPG replacement.[21],[22] We found an 11.42% infection rate in this study. Seventy-five percent of the patients with infections were male. Infection was detected in two (6.45%) of 31 female patients and six (15.3%) of 39 male patients. None of the patients who developed infections had previous surgery. In addition, although ten of the seventy patients in this study had co-existing DM, none of them developed infections. The infection rate was found to be three times higher in men, but DM was not an infection risk factor.

S. aureus and coagulase-negative Staphylococci are the most frequently isolated microorganisms from IPG infections in both DBS and cardiac procedures.[5],[6],[23],[24],[25] In our study, methicillin-sensitive coagulase-negative Staphylococcus was the most commonly isolated microorganism (n = 3, 37.5%). One patient had methicillin-resistant S. aureus , one had methicillin-sensitive S. aureus , one had Burkholderia gladioli , and two had two different microorganisms isolated at 2-month intervals. The isolated etiologic organisms are shown in [Table 3]. Time to infection was ≤6 months in three patients and ≥12 months in five patients. Our earliest infection was in the 1st month, which was caused by B. gladioli , a Gram-negative anaerobic rod that frequently causes infections in patients undergoing lung transplant surgery. Early explant was performed, and this patient's postoperative wound care was performed with the same routine; there was also no difference in the surgical prophylactic treatment for this case. The duration of the DBS lasted 3 h for this patient, which was the approximate time of implanting the leads bilaterally for the other patients also.

Complete removal of hardware should be avoided in DBS surgeries complicated by infection.[6] Bjerknes et al . detected 33 infections in a DBS series of 588 patients. Only seven (21%) of these patients recovered successfully after antibiotic treatment alone. Twenty-two (67%) patients underwent partial removal and four (12%) underwent complete removal of the device in their series.[6] However, in another series by Gorgulho et al ., complete removal was performed in 12 (60%) of 20 patients with infection; infections were primarily treated with antibiotic therapy and clinically followed before total device removal was deemed necessary.[25] In the present study, we performed total removal in 4 (50%) of eight patients who developed infection. Early removal was performed in only one patient; this was because a Gram-negative anaerobic rod, B. gladioli , was isolated and there was no literature to guide us. Other than this early explant, the other three removals were performed at months 13, 19, and 42. These three patients had a satisfactory response to antibiotic treatment in the early period but underwent explant surgery at months 4, 7, and 9 prior to the initial infection time, mainly because of psychosis and hallucinations [Table 3]. Although preoperative evaluation of patients undergoing DBS (Montreal Cognitive Assessment, Beck Depression Inventory) is conducted by a psychiatrist, we also recommend postoperative routine psychiatric follow-up. In our series, the other four (50%) patients who developed infection in the extension wire and IPG side were successfully treated with antibiotics. There were no cases of explant with an infected DBS lead side in the current series. Based on our experience, medical treatment should be the first option in DBS infection. We tried a partial removal of the system (IPG) in one patient, but this resulted with failure because of unresponsiveness to medical treatment. Partial or total removal should be reserved for cases of antibiotic therapy failure. However, if unresolved psychiatric problems are present, total removal should be considered primarily. The determination of infection of the system is considered according to the microorganism, infection side, and also the psychiatric conditions of the patients in the follow-up of DBS.

Another complication encountered after DBS surgery for movement disorders is ICH. MER has been shown to increase the risk of ICH.[26],[27] Meta-analyses reported that the ICH risk ranges between 3.0% and 3.9%.[28],[29] In our study, ICH did not occur despite using MER. Visualization of the vessels using contrast-enhanced CT for trajectory planning, electrode depth, mean arterial pressure (≤90 mmHg) of the patient during implantation, and cessation of anticoagulant drugs at least 10 days before surgery are factors that may explain this. We experienced a favorable complication rate without any neurologic deficits. It is also valuable to witness the synchronization of the anatomic and physiological targeting by MER and macro stimulation correlated with the depth of the electrode at the target side during surgery [Table 1]. The greater the depth of the contacts, the greater the risk of ICH because of the long course of the electrode. In our series, the number of contacts beyond the target was not negligible because there is continuous neuron activity in MER.

In one of the patients with dystonia who developed an acute subdural hematoma due to trauma 45 days after implantation, even though severe midline shift was present, we elected not to explant the device after hematoma evacuation because the electrode was still in its proper place. In this rare situation, we recommend evacuation of the life-threatening hematoma without removing the device.


  Conclusion Top


A multidisciplinary approach, proper stimulation technique (including the number of channels), precise electrode targeting, and the use of MER are fundamental for successful DBS surgery with favorable outcomes and low complication rates. Although there is still no definitive treatment protocol for postoperative infections after DBS, successful treatment affects surgical outcomes and cost-effectiveness. Based on our experience, medical treatment together with partial removal of the device may be the first choice in treatment. Total removal of these devices should be preferred in patients with unresolved postoperative psychiatric problems.

Acknowledgment

The authors thank Professor Gülden Ersöz for her contribution in planning the prophylactic antibiotic treatment of DBS patients before and after surgery in the present study. We also thank senior neurosurgeon, Kim J Burchiel, M.D., F.A.C.S., for his strong recommendation to the manuscript.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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