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Neurosurgery
Research paper
Sequence of electrode implantation and outcome of deep brain stimulation for Parkinson's disease
  1. Francesco Sammartino1,
  2. Vibhor Krishna1,
  3. Nicolas Kon Kam King1,
  4. Veronica Bruno2,
  5. Suneil Kalia1,
  6. Mojgan Hodaie1,
  7. Connie Marras2,
  8. Andres M Lozano1,
  9. Alfonso Fasano2
  1. 1Division of Neurosurgery, University of Toronto, Toronto Western Hospital, Toronto, Ontario, Canada
  2. 2Morton and Gloria Shulman Movement Disorders Clinic and the Edmond J. Safra Program in Parkinson's Disease, Toronto Western Hospital – UHN, Division of Neurology, University of Toronto, Toronto, Ontario, Canada
  1. Correspondence to Dr Alfonso Fasano, Movement Disorders Centre—Toronto Western Hospital, 399 Bathurst St, 7 Mc412, Toronto, ON Canada M5T 2S8, alfonso.fasano{at}uhn.ca

Abstract

Introduction The effect of the variability of electrode placement on outcomes after bilateral deep brain stimulation of subthalamic nucleus has not been sufficiently studied, especially with respect to the sequence of hemisphere implantation.

Methodology We retrospectively analysed the clinical and radiographic data of all the consecutive patients with Parkinson's disease who underwent surgery at our centre and completed at least 1 year follow-up. The dispersion in electrode location was calculated by the square of deviation from population mean, and the direction of deviation was analysed by comparing the intended and final implantation coordinates. Linear regression analysis was performed to analyse the predictors of postoperative improvement of the motor condition, also controlling for the sequence of implanted hemisphere.

Results 76 patients (mean age 58±7.2 years) were studied. Compared with the first side, the second side electrode tip had significantly higher dispersion as an overall effect (5.6±21.6 vs 2.2±4.9 mm2, p=0.04), or along the X-axis (4.1±15.6 vs 1.4±2.4 mm2, p=0.03) and Z-axis (4.9±11.5 vs 2.9±3.6 mm2, p=0.02); the second side stimulation was also associated with a lower threshold for side effects (contact 0, p<0.001 and contact 3, p=0.004). In the linear regression analysis, the significant predictors of outcome were baseline activities of daily living (p=0.010) and dispersion of electrode on the second side (p=0.005).

Conclusions We observed a higher dispersion for the electrode on the second implanted side, which also resulted to be a significant predictor of motor outcome at 1 year.

https://doi.org/10.1136/jnnp-2015-311426

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    Introduction

    The subthalamic nucleus (STN) is a common deep brain stimulation (DBS) target for the treatment of advanced Parkinson's disease (PD).1 The outcome of DBS is affected by patient-related and surgical-related factors. Among the former, the baseline scores on the Unified Parkinson's Disease Rating Scale (UPDRS) and levodopa responsiveness are well-established predictors of outcomes.2 Likewise, precise targeting and electrode implantation are important for good outcomes after STN DBS.1 ,3 Commonly the surgical technique involves direct STN targeting on MRI with or without confirmatory intraoperative microelectrode recordings (MER).4 ,5

    A variety of factors may introduce targeting error including brain shift,6 ,7 pneumoencephalus,6 ,8 transventricular trajectory9 ,10 and deformation of the electrodes.11 The sequence of electrode placement may also affect the targeting accuracy during bilateral STN DBS implantation.6 Although the side effects associated with electrode deviations may be optimised with programming, the overall effect of electrode dispersion on long-term surgical outcomes is unknown. We hypothesised that the second implanted side is associated with higher dispersion in the electrode locations, and this dispersion is a predictor of STN DBS outcomes.

    Methodology

    This study was approved by the Research Ethics Board, University Health Network and University of Toronto.

    Study population

    We retrospectively included all the consecutive patients with a clinical diagnosis of PD who underwent bilateral STN DBS from October 2007 to December 2013 and fulfilled the following inclusion criteria: appropriate (structural three-dimensional (3D) T1 MRI) pre and immediate (24–72 h) postoperative imaging and clinical evaluation at 1 year postimplantation. Exclusion criteria were: implantation with intracranial leads other than Medtronic model 3387 (Medtronic Inc, Minneapolis, Minnesota, USA), major postoperative complications (eg, bleeding with neurological deficits, infection, etc) and patients who underwent lead revision surgery (due to misplacement or hardware malfunctioning) or were implanted as a part of another trial with electrodes from another manufacturer. In addition, since at our centre we typically implant the DBS electrode first on the right hemisphere and then on the left side, three patients with implantation first on the left side were excluded. Details on the surgical procedures have been described elsewhere.12

    Data collection—clinical information

    All the patients were evaluated by a multidisciplinary team at the Toronto Western Hospital. The clinical information was collected from the electronic database. Besides the demographic variables (age, gender, handedness), we collected baseline information relevant to PD (duration of disease, worst side affected, levodopa equivalent dose), response to levodopa challenge test as evaluated by the motor section of the UPDRS part III after a supratherapeutic levodopa dose, the activity of daily living score of the UPDRS part II and the complication of therapy, assessed with the part IV of the UPDRS. In addition, postoperative motor condition was also assessed in two medication and stimulation states: ON medication and ON stimulation (ON-ON), OFF medication and ON stimulation (OFF-ON). Similarly, we also retrieved information from the first programming session (threshold and type of side effects at each contact on both sides). For the purpose of this analysis, the best postoperative UPDRS-III score (ON-ON) was considered as the primary outcome measure.

    We reviewed the operative records to include targeting information: frame-based coordinates of the anterior and posterior commissures (AC and PC) and bilateral STN target coordinates. Any changes in trajectory based on the electrophysiology data and the final depth of implantation were reviewed to calculate the final implantation coordinates. The operative technique for DBS and MER has been published previously.5

    Patients are positioned in a ‘beach chair’ position with the head elevation less than 30° from the floor. The burr hole is sealed with gelfoam and fibrin sealant to avoid air entry during MER. We used a single cannula with two microelectrodes driven independently by manual microdrives. The MER typically started 10 mm proximal to the intended target. Besides mapping the proximal and distal borders of STN, the thresholds for side effects on stimulation (100 mA, 100 Hz) were noted. Based on the recording and stimulation results, the trajectory was modified to minimise side effects and maximise efficacy. Typically one MER trajectory provided sufficient information for DBS lead implantation. After confirming acceptable efficacy and side effect profile with the DBS lead stimulation, the MER and implantation procedure was performed on the second side.

    Imaging analysis

    The MRI used for targeting and postoperative imaging was a structural 1.5 T T1 sequence (Signa Excite, GE medical system, Milwaukee, Wisconsin, USA) with 256×256 matrix, accounting for a final voxel size of 1.01×1.01×1.4 mm. All the patients underwent postoperative MRI with the same parameters within the first 24–72 h after implantation. The images were exported to the Medtronic Stealth S7 (Medtronic Inc, Minneapolis, Minnesota, USA) planning station. We aligned the preoperative imaging to the AC-PC plane with Framelink software (V.5, Medtronic, Inc, Minneapolis, Minnesota, USA). The postoperative structural T1 images were then rigidly aligned with the preoperative frame-based T1. We performed ‘point merge’ fusion using six different landmarks (mammillary bodies, right and left trigeminal and facial nerve root entry zone, right and left optic nerve at the level of the optic foramen) and minimised the alignment error to less than 1 mm. Fusion accuracy was also confirmed at the level of optic chiasm, anterior and posterior commissures, and lateral ventricles. We identified the location of the electrode artefact on the axial images and calculated the coordinates of the tip plus all the four contacts bilaterally by selecting a voxel in its centre as previously described.13 ,14 All the coordinates were then expressed in relation to mid-commissural point.

    The deviation in electrode trajectories was analysed using two separate metrics: deviation from population mean (‘electrode dispersion’) and direction of deviation from the intended target. First, we calculated the absolute deviation from the population mean for each individual electrode (mean absolute deviation in mm) separately in X, Y and Z axes. The ‘electrode dispersion’ was then calculated by the square of mean absolute deviation (in mm2) both for the electrode tip and the active electrode (cathode for stimulation at 1 year). The composite of dispersion in all three directions (3D dispersion) was calculated using the formula:Embedded Image

    In order to calculate the direction of deviation from the intended target, we subtracted the actual electrode coordinates from the coordinates of intended trajectory (preoperative coordinates after MER adjustments) separately in X, Y and Z directions. Any deviations greater than 2 mm between the intended and actual tip of electrode location were considered significant. All the measurements were rounded up or down to the nearest whole numbers. The volume of pneumocephalus was also measured on each side using an assisted region-growing algorithm using Osirix V.5.8.

    Statistical analysis

    We performed the statistical analysis using SPSS (V.22, IBM Corp, Armonk, New York, USA). The normality of data was ascertained using the Kolmogorov-Smirnoff test. For normally distributed data, we performed t test to compare continuous variables and χ2 test for categorical variables. For within-patient comparisons, we also performed the paired samples t test. For non-normally distributed continuous data, we used the Mann-Whitney U test.

    We compared the variance of ‘electrode dispersion’ between the two cerebral hemispheres using the Levene's test. Finally, we performed a forward step-wise linear regression analysis to identify the significant (p<0.05) predictors of outcome. A univariate analysis was performed to identify significant predictors of primary outcome (postoperative UPDRS-III ON medication and ON stimulation score). The significant variables from univariate analysis were included as covariates in a linear regression model. We constructed several models to individually include variables encoding the ‘electrode dispersion’ (electrode tip, active electrode, Euclidian distance and dispersions separately in X, Y and Z axes). The model with highest R2 value was reported as the final model. The variables with the p values less than 0.05 in final model were considered significant.

    Results

    We included 76 patients who met the inclusion criteria. Population characteristics are outlined in online supplementary table S1. The mean age of this cohort was 58±7.2 years and 20 (26%) were females. The self-reported worst side was left side in 63%, right side in 33% and both sides in 4%.

    Comparison between preoperative and postoperative status

    All the UPDRS subscales showed significant improvement 1 year after implantation (see online supplementary table S1). The preoperative OFF state UPDRS-III scale improved by 36±32.9% and 59±22.6% when compared with the postoperative OFF-ON and ON-ON states, respectively. The levodopa equivalent dose also decreased by 46.8±24.8%, and a commensurate decline in UPDSR-IV subscore was also observed (−34.2±73.2%).

    Dispersion in electrode location and the side effect profile

    The dispersion of the electrode tip on the second side was significantly more than the first side (electrode deviation in Euclidian distance: 2.2±4.9 vs 5.6±21.6 mm2, p=0.04; table 1). This dispersion was significant in the X axis (p=0.03) and Z axis (p=0.02). We observed that the second side electrode were more frequently superficial (15 electrodes vs 8 with deviation of ≥2 mm in Z-axis, p=0.02) (figure 1). This deviation in placement was also reflected in a lower threshold to elicit side effects on the left side on the most proximal and distal electrode contacts (2.1±0.9 vs 2.7±1.2 V, p<0.001 and 3.7±1 vs 4.1±1.2 V, p=0.004, respectively). However, there was no difference in the frequency of the specific side effect (see online supplementary table S3).

    View this table:
    Table 1

    Comparison of electrode (tip and active electrode) dispersion between the first side and second implanted side (Levene's test for comparison of variances unless specified)

    Predictors of outcome

    In the univariate analysis, the significant predictors of postoperative UPDRS-III (ON medication and ON stimulation) were preoperative UPDRS-II (p=0.02), preoperative left-sided UPDRS-III score (p=0.02) and levodopa responsiveness (p=0.03). Other variables (age, p=0.15; gender, p=0.57; preoperative right-sided UPDRS-III, p=0.86; levodopa equivalent, p=0.15; pneumocephalus, p=0.13 and duration of disease, p=0.36) were not significant.

    Figure 1
    Figure 1

    A heat map of active contact coordinates (mid-commissural point based) on the first (right hemisphere, left panel) and the second (left hemisphere, right panel) insertional sites plotted on a coronal MRI to represent the electrode location on the X and Z axes. The ‘dispersion’ of the active electrode on the second insertional site was a significant predictor of postoperative Unified Parkinson's Disease Rating Scale part III (UPDRS-III) at 1 year (‘electrode dispersion’ in Z-axis, p=0.005).

    We constructed the first two multivariate models using the 3D ‘dispersion’ of the electrode tip and active electrode, respectively. In the next two models, we incorporated the ‘dispersion’ of electrode tip and active electrode separately in the X and Z axes. In all the models, the significant predictors of outcome were preoperative UPDRS-II and dispersion of electrode on the second side. In the final model (see online supplementary table S4—model 4 with highest R2 value), the dispersion of the active electrode in the Z-axis was a significant predictor of outcome (coefficient=0.39, p=0.005). The other significant predictor was preoperative UPDRS-II (coefficient=0.23, p=0.005; see online supplementary table S3). Levodopa responsiveness and preoperative UPDRS-III on the left side failed to reach statistical significance (p=0.05 and p=0.2, respectively).

    Discussion

    In this study, we found higher electrode tip dispersion on the second implanted side, significantly in both the X and Z axes. The dispersion of active electrode was not significantly different between the two sides likely reflecting the extensive postoperative programming (see online supplementary table S2). Overall, the higher dispersion on second implanted side was significantly associated with worse UPDRS-III score 1 year postsurgery after adjusting for disease-related covariates (UPDRS-II and disease laterality as measured by left side preoperative UPDRS-III OFF). Although significant, the effect size of this association was small, as for each unit (1 mm2) increase of the electrode dispersion along the Z-axis on the second implanted side, the UPDRS score increases by 0.39 points.

    Our finding is in keeping with Azmi et al,6 who also reported higher deviation on the second implanted side after bilateral STN DBS procedures. Hunsche et al15 assessed the degree of brain shift following the implantation of first electrode using intraoperative X-ray and MRI. The authors reported that a deviation of >1 mm in the location of anterior commissure was detected in up to 8% of their patients. In a small study, Sadeghi et al16 also assessed the distance between planned and expected target in bilateral STN DBS procedures. Although more adjustments in trajectory were needed on the second implanted side, the deviations in X and Y axes failed to reach statistical significance. The authors did not analyse the deviation in Z-axis. The current study is the first to associate higher electrode dispersion on the second implanted side with long-term clinical outcomes. Although small in magnitude, this association has important implications for surgical planning during STN DBS. We must also emphasise that the regression model only accounted for 18% (R2 value) of variance in the outcome data indicating other unmeasured confounders like factors related to patient's disease process (eg, gait problems, poor general health, medication dosage, etc) and other factors like access to healthcare (eg, the distance of patient's residence from our movement disorder centre).

    The most common reasons for this increased targeting dispersion on the second side may include brain shift or pneumoencephalus.6 ,8 ,17 ,18 Brain shift can increase the number of microelectrode tracks and also decrease the implantation accuracy.6 Winkler et al8 reported a patient who required repositioning of an electrode implanted on the second side due to lack of clinical efficacy. Using deformation field analysis, they identified a significant shift in the location of STN due to intraoperative brain shift. Previous studies have reported a brain shift mainly in the posterior direction along with the enlargement of the ‘body’ of the lateral ventricle.7 Pneumocephalus may also contribute to error in stereotactic accuracy, especially on the second side.5 ,8 ,9 We did not observe a difference in the numbers of MER tracks performed between the two implanted sides (93 tracks on the first implanted side vs 97 tracks on the second implanted side, p=0.91). Also the volume of pneumocephalus in this series was in the order of 3–4 mL. This volume was significantly smaller than the volume of air previously shown to affect electrode accuracy.6 Intraventricular trajectory11 ,12 and the deformation of the electrodes during surgery can also affect the final position of implantation.15 However, among the 76 patients in this series, we observed eight transventricular trajectories on the second implanted side and six transventricular trajectories on the first implanted side (p=0.78). We speculate that the potential reasons for different lead locations on the two implanted sides may include difficulty in intraoperative X-ray visualisation of the tip of the second side DBS lead in the presence of previously implanted DBS lead and a shift in the location of STN on the second side after implantation of DBS lead on the first side. Other non-surgical factors may introduce variability in electrode position, for example, patients may be less cooperative at the time of second electrode implantation due to increasing fatigue after the implantation and testing on the first side.

    This retrospective study has several limitations. In order to minimise selection bias, we studied all the consecutive patients satisfying our inclusion and exclusion criteria. In order to minimise measurement bias, we reviewed the clinical data from our prospectively collected electronic database. Moreover, the imaging analysis was carried out before assessing the clinical outcomes. It is possible that the greater electrode dispersion on the second side of insertion is specific to our centre and our surgical technique of implantation (Leksell frame, bilateral implantations, MER-guided implantation, right hemisphere implantation first). However, our technique of insertion is a standard frame-based technique and is widely used for DBS procedures. Although the use of CT scan for stereotactic surgery has been widely considered the most accurate imaging modality available,15 ,19–28 the use of MR for targeting and postoperative verification of electrode location is desirable for the greater anatomical detail. A number of authors have demonstrated that the greater source of inaccuracy deriving from the use of MR due to b0 inhomogeneity, non-linearities in the gradient fields and magnetic susceptibility variations in imaged objects. The correct calibration of the scanner and the choice of the 3D sequence can partially correct for the spatial distortion. Overall, the inaccuracy associated with MRI is inevitably less than 1 mm in all the axes.29 We did not record accurate surgical times for the first and second side procedures. However, based on clinical experience and the similar number of MER tracks on the two implanted sites, we believe that the two sides had similar operative times. Lastly, analysis of the immediate postimplantation MRI will fail to detect any delayed changes in electrode position. In fact, van den Munckhof et al30 reported an upward displacement of electrodes several weeks following implantation (3.3±2.5 mm along the trajectory), mainly in cases with large postoperative subdural air volumes. These authors did not find a significant effect of the sequence of implantation. The authors however reported that a delayed significant change in electrode location should be accompanied either by the loss of efficacy or new stimulation-related side effects, which were not observed in our cohort.

    In conclusion, this study shows that the order of insertion of the DBS electrode during bilateral DBS has a small impact on clinical outcomes arising from the increased ‘electrode dispersion’ on the second implanted side. Although further studies with a prospective design and larger sample are certainly needed, our findings would suggest a careful assessment of implantation accuracy on the second implanted side to obtain the greatest benefit from DBS.

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    View Abstract

    Supplementary materials

    • Supplementary Data

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    Footnotes

    • Competing interests None declared.

    • Ethics approval UHN REB.

    • Provenance and peer review Not commissioned; externally peer reviewed.