halpern 2008

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Clinical Study

Stereotact Funct Neurosurg 2008;86:3743 DOI: 10.1159/000108587

Brain Shift during Deep Brain Stimulation Surgery for Parkinsons Disease

Casey H. Halpern Shabbar F. Danish Gordon H. Baltuch Jurg L. Jaggi

Department of Neurosurgery, University of Pennsylvania, Philadelphia, Pa. , USA

compromise target localization, requiring multiple micro-electrode adjustments. This may provide indirect justifica-tion for the necessity of microelectrode recordings during DBS surgery. Copyright 2007 S. Karger AG, Basel

Introduction

Deep brain stimulation (DBS) of the subthalamic nu-cleus (STN) is the surgical treatment of choice for care-fully screened and selected patients with medically in-tractable Parkinsons disease (PD) who were previously levodopa responsive. Although STN localization using magnetic resonance imaging (MRI) and a stereotactic head frame can have an accuracy of less than 1 mm [1] , a small amount of error can dramatically impact proper target localization. Despite our ability to make direct and indirect measurements of STN using MRI [2] , intraop-erative neurophysiologic and clinical monitoring tech-niques such as macrostimulation have been shown to dramatically impact the location of the final active con-tact. Lanotte et al. [3] reported that despite stereotactic localization, multiple tracks directed posteromedially were required in numerous patients given atypical micro-electrode recordings and side effects, indicative of subop-timal STN targeting. Similar decrements in accuracy of preoperative measurements using neuronavigational sys-tems have been reported in cases of tumor resection in which significant brain shift was noted [4] . Nimsky et al.

Key Words Brain shift Brain deformation Deep brain stimulation Subthalamic nucleus Red nucleus Parkinsons disease

Abstract Background: Brain shift may occur during deep brain stimu-lation (DBS) surgery, which may affect the position of sub-cortical structures, compromising target localization. Meth-ods: We retrospectively evaluated pre- and postoperative magnetic resonance imaging in 50 Parkinsons disease pa-tients who underwent bilateral subthalamic nucleus (STN) DBS. Patients were separated into two groups: group A those with ! 2 mm cortical displacement (66 leads) and group B those with 6 2 mm cortical displacement (34 leads). Pre and post-op coordinates of anterior (AC) and pos-terior commissures (PC), as well as the boundaries of red nu-cleus (RN) were compared. Results: AC-PC shortening due to posterior displacement of AC correlated with cortical dis-placement (p ! 0.02) and was significantly greater in group B (0.41 8 0.68 mm) than A (0.04 8 0.76 mm; p ! 0.005). Pos-terior shift of AC and RNs center positively correlated (p ! 0.0001). Shift appeared to impact the number of microelec-trode tracks made to optimize STN targeting. AC-PC shorten-ing also correlated with age (p ! 0.003) and duration of sur-gery (p ! 0.04). Conclusions: Subcortical structures shift during DBS surgery. This shift appears to be gravity-depen-dent since structures only shifted posteriorly, and patients were primarily in the supine position. Posterior shift of RN may indicate STN displacement. Such positional change may

Published online: September 18, 2007

Jurg L. Jaggi, PhD Department of Neurosurgery Center for Functional and Restorative Neurosurgery University of Pennsylvania, Philadelphia, PA 19107 (USA) Tel. +1 215 829 7144, Fax +1 215 829 6645, E-Mail [email protected]

200 S. Karger AG, Basel10116125/08/08610037$24.50/0

Accessible online at:www.karger.com/sfn

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Halpern/Danish/Baltuch/Jaggi

Stereotact Funct Neurosurg 2008;86:374338

[4] have attributed this limitation in preoperative target-ing to loss of cerebrospinal fluid (CSF). A recent study of DBS using real-time intraoperative MRI reported obser-vations in which appreciable ipsilateral brain shift was evident during burr hole access [5] . We hypothesize that CSF loss may account at least in part for this targeting er-ror in STN DBS by causing a shift of subcortical struc-tures during surgery, although other factors must be con-sidered. This structural shift can be visualized by exam-ining cortical displacement from the inner table of the calvarium which in turn can be easily quantified radio-graphically.

Methods

Patient Population Fifty patients who underwent bilateral STN DBS surgery for

advanced PD were retrospectively examined, including 36 male and 14 females with a mean (range) age of 59.7 years (3674 years). Table 1 summarizes the basic demographic and clinical features for this patient population. We performed preoperative MRI (1.5-tesla Signa magnet, GE Medical Systems Inc., Milwaukee, Wisc., USA) after placement of a Leksell G stereotactic frame (Elekta, Inc.). All patients included in this study underwent bilateral STN DBS placement and received postoperative MRI approximately4 h after their operation as part of our routine clinical care proto-col. These images were retrospectively reviewed.

Surgical Targeting and Procedure STN location was determined from preoperative T 1 and T 2

imaging using both direct and indirect targeting techniques [6, 7] . Details of the surgical procedure have been previously report-ed [8] . Briefly, based on the Schaltenbrand-Wahren atlas [9] , in-direct target coordinates of STN were calculated 12 mm lateral to the midline, 2 mm posterior to the midcommissural line, and5 mm inferior to the line leading from the anterior commissure

(AC) to the posterior commissure (PC). Direct targeting was based on direct visualization of STN on the coronal FSE sequence. The final preoperative target was determined by the surgical team based on frame coordinates derived from direct and indirect methods.

All patients were placed in the supine position for this proce-dure with the neck flexed at 2030 in order to minimize CSF loss. A 14-mm burr hole was placed on the coronal suture, The surgical trajectory usually started at the coronal suture approximately3 cm lateral to the midline, and attempted to avoid deep cortical sulci. Standard packing techniques with gel foam were applied to the burr hole to prevent CSF loss. Microelectrode electrophysio-logical recordings were performed bilaterally to define ventral and dorsal borders of STN. Target refinement was considered ad-equate when recordings were obtained from at least 4.5 mm of STN. The permanent quadripolar DBS leads (model 3387; Med-tronic, Minneapolis, Minn., USA) and internal pulse generators (model 7424, Itrel II; Medtronic) were then implanted.

MRI Measurements Axial and sagittal images were transferred and the image vol-

ume was transformed into stereotactic coordinate space using Medronics StimPilot Neuronavigation system (Medtronic SNT, Minneapolis, Minn., USA). Preoperative axial and sagittal slices of T 1 -weighted images were used to identify AC and PC frame coordinates (TR 317 ms, TE 14 ms, slice thickness 2 mm, echo train 2, FOV 27, matrix 256 ! 256, bandwidth 15 kHz). Coronal and sagittal reconstructions were derived from axial slices to as-sist in preoperative targeting of STN.

During postoperative image evaluation, preoperative axial slices of T 1 -weighted images were merged with preoperative T 2 -weighted images, as well as postoperative T 1 and T 2 images using the StimPilot system. The Leksell G stereotactic frame was regis-tered to the MR images. A point merge was performed using at least four clearly defined landmarks such as the external auditory canal and nasal septum, as well as the lens of the eye for the ma-jority of image fusions ( fig. 1 and 2 ). The automerge function us-ing the StimPilot software was suboptimal in the majority of cas-es, which is attributed either to postoperative scalp swelling or extracranial lead artifacts. Often head position was altered on postoperative scans once the head frame was removed, further complicating the automerge. The distance from the anterior-most edge of the medial frontal gyrus to the inner table of the calvarium was measured at the superior edge of frontal sinus on both pre- and postoperative T 1 -weighted images ( fig. 3 ). Cortical displace-ment was determined by calculating the change in this distance after surgery. Patients were separated into two groups: those with-out cortical displacement (A; ! 2 mm; 58 leads) and those with cortical displacement from the inner table to the calvarium (B; 6 2 mm; 42 leads). In order to evaluate the effect of ventricular penetration and consequential CSF loss on cortical displacement, we also separated patients into groups with and without ventricu-lar lead penetration on the postoperative MRI.

For all of our analyses of deep brain structures, the distances in the x-, y- and z-axes were defined as the difference in the me-diolateral, anteroposterior, and dorsoventral directions, respec-tively. We defined AC and PC as the centers of the AC and PC, respectively, the locations of which were determined based on the position of their ventricular edges in the midline on both pre- and postoperative axial T 1 -weighted images. The AC-PC distance was

Table 1. Clinical features of patients with advanced PD who un-derwent bilateral STN DBS

Group A Group B

Age1 59.80811.45 60.7688.83Gender, M/F 26/7 10/7Surgery duration1 140.26828.64 147.24835.00Trajectories2 1.1980.47 1.3380.54Average change from initial

target2, 3, mm 0.2680.68 0.4880.87

1 Groups A and B did not differ in age or surgery duration ac-cording to t tests (no p values less than p < 0.05).

2 Groups A and B did not differ according to a 2 analysis. 3 All adjustments in trajectory were made 2 mm posteriorly.

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Brain Shift during Deep Brain Stimulation Surgery for PD

Stereotact Funct Neurosurg 2008;86:3743 39

then measured on both pre- and postoperative scans. The ante-rior, posterior, medial, and lateral borders of red nucleus (RN) were taken primarily from T 2 -weighted axial slices demonstrat-ing the largest dimensions ( fig. 4 ). The dorsal and ventral borders were measured using both coronal and sagittal T 2 images to ob-tain the most accurate frame coordinates possible. The assigned

dorsal and ventral coordinates were the result of an average be-tween the sagittal and coronal locations. DBS implants precluded postoperative border determination of STN. Given superior reso-lution, we used axial slices as a source of reference to guide our analyses of sagittal and coronal reconstructions. In addition, the Schaltenbrand-Wahren atlas provided a general sense of location of each nucleus [9] . However, the atlas was turned off prior to structure identification in order to avoid bias from an unwarped (generic) atlas of the borders.

Statistical Analysis We used parametric statistical analyses. A univariate analysis

of variance (ANOVA) was used to test the mean difference in shift of deep brain structures between groups A and B. Richter et al. [10] demonstrated that the type of data analyzed in this study is normally distributed. 2 analyses were used to test the difference in the number of trajectories required to obtain an optimal target location. Statistical significance was assumed for tests yielding p values of less than 0.05. SPSS software (CMC International, Dal-las, Tex., USA) was used for the statistical processing of our data.

Results

A univariate analysis of variance (ANOVA), using a between-subject factor of group (2-A, B) and a within-subject factor of change in AC-PC distance to evaluate shift of deep brain structures, revealed significantly greater shortening of the AC-PC distance in group B ver-

a b

c d

e f

Fig. 1. Point merge of postoperative axial slices of T 2 -weighted images ( a , c , e ) and preoperative T 1 -weighted images ( b , d , f ) us-ing bony landmarks such as the external auditory canal ( a , b ), nasal septum ( c , d ), and lens of the eye ( e , f ). White-filled ( a , b , c , d , f ) and black-filled ( e ) circles indicate the designated bony land-mark used for each point merge.

Fig. 2. Fused postoperative T 2 -weighted (left) and preoperative T 1 -weighted (right) axial slice using the point merge function of the StimPilot system.

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sus group A [F(1, 99) = 8.09; p ! 0.005] ( table 2 ). Within-group comparisons, using paired sample t tests, showed that the AC-PC distance in group B was indeed signifi-cantly shorter postoperatively compared to the preopera-tive AC-PC distance [t(41) = 2.95; p ! 0.005], while there was no significant difference in group A. AC-PC shorten-ing appeared to be a result of relatively more posterior displacement of AC relative to PC [t(41) = 4.61; p ! 0.0001] in group B, according to paired sample t tests.

For group B, two-tailed Pearsons correlations revealed that AC-PC shortening positively correlated with cortical displacement from the inner table of the calvarium [r = 0.37; p ! 0.02], posterior shift of AC [r = 0.30; p ! 0.058], and marginally with the posterior shift of RNs geometric center [r = 0.29; p ! 0.07], as well as patient age [r = 0.45;

Table 2. Mean 8SD shift of cortical and subcortical structures in the anteroposterior plane yaxis in patients with PD undergo-ing bilateral STN DBS

Tissue Group A Group B

Frontal cortex, mm 0.5681.15 4.8081.521, 2Preoperative AC-PC distance, mm 27.0981.36 26.5681.46Postoperative AC-PC distance, mm 27.1381.52 26.1481.71AC-PC shortening, mm 0.0480.76 0.4180.681AC, mm 1.4582.67 1.5481.742PC, mm 1.1882.39 0.9981.61RN, mm 0.9281.66 1.4281.652

1 Significant difference between groups A and B (p < 0.05).2 Correlation with AC-PC shortening (marginal for RN).

a b

a b

Fig. 3. Axial slice of a T 1 -weighted preop-erative ( a ) and postoperative ( b ) MRI from a patient with large cortical displacement. The distance between white arrows repre-sents the measured distance from the an-terior-most portion of frontal cortex to the inner table of the calvarium at the superior edge of frontal sinus. The difference in these distances represents cortical dis-placement due at least in part to CSF loss.

Fig. 4. Representative axial slice ( a ) with sagittal ( b ) reconstructions of a T 2 -weight-ed MRI that show reliable borders of the RN.

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p ! 0.003] and the time elapsed between incision and skin closure [r = 0.43; p ! 0.04]. Posterior shift of AC [r = 0.71; p ! 0.0001] correlated with the posterior shift of RNs geometric center ( fig. 5 ). There was marginal correlation between cortical displacement and the posterior shift of RNs center [r = 25; p ! 0.12]. There was no significant correlation between AC-PC shortening and the posterior shift of PC [r = 0.015; ns]. None of these correlations were found in group A.

The number of trajectories required to obtain optimal microelectrode recording patterns and improved test stimulation responses revealed a trend for an association between the number of attempts made and the degree of cortical displacement ( table 1 ). Eleven of the 42 (26%) im-planted leads in group B required more than one attempt, while 9 of the 54 (17%) implanted leads in group A re-quired more than one attempt. All of the adjustments made to our trajectory were directed 2 mm posterior to the initial. A similar trend was found when comparing the mean adjustment in the posterior direction between groups A and B ( table 1 ). However, neither of these rela-tionships reached statistical significance. In order to ana-lyze the impact of a ventricular trajectory found on post-operative MRI scans on brain shift, we performed an uni-variate ANOVA, using a between-subject factor of group (2-A, B) and a within-subject factor of the presence of

ventricular penetration. This did not demonstrate a sig-nificant difference in cortical displacement or shift of deep brain structures from those scans without ventricu-lar penetration.

Discussion

There is little knowledge about dynamic structural changes that may occur during an intracranial proce-dure. This is, in fact, the first reported analysis of sur-gery-associated brain shift of a large series of patients un-dergoing bilateral DBS. Winkler et al. [11] recently re-ported a case of brain shift during bilateral STN DBS. They were unable to obtain typical microelectrode re-cordings after successful lead implantation in STN. Test macrostimulation induced unwanted side effects without improved clinical effect. A permanent electrode was im-planted, though postoperative MRI revealed 2 mm of dis-placement from the planned target, which they surmised accounted for the absence of expected microelectrode re-cordings and test stimulation responses. Deformation field analysis revealed 13 mm of cortical displacement and 2 mm of STN shift. This case report is consistent with our findings that some patients are at risk for significant brain shift during DBS.

We grouped our patients into those with no cortical displacement from the inner table of the calvarium and those with cortical displacement. We considered up to2 mm of displacement as negligible given the accepted error of 2 mm of the point merge StimPilot system. The findings of our study indicate that shift of subcortical tar-get structures is possible during bilateral STN DBS sur-gery for PD. Indeed, cortical displacement from the inner table correlated with posterior shift of deep brain struc-tures. This positional change may be gravity-dependent given patients supine position and appears to affect the number of attempts made to obtain an optimal trajectory in targeting STN. All of our trajectory adjustments were directed posteriorly, despite a recent report of posterome-dial correction [3] . This is consistent with the finding that there was no significant shift of AC, PC or RN in either the mediolateral or dorsoventral directions. Neck flexion at 2030 did not appear to cause any caudal displace-ment. It is interesting that an intraventricular trajectory did not appear to be associated with more significant brain shift. We hypothesize that either a considerable amount of CSF must be lost from the subarachnoid space or other factors must be implicated in brain shift. Further implications of our study suggest that in cases where large

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Fig. 5. Trend plot showing positive correlation between posterior shift of the AC and the center of the RN. Correlation was signifi-cant at p ! 0.0001.

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cortical shift is observed, immediate postoperative imag-ing may be inaccurate in determining the location of the stimulating lead. In these cases, it may be advisable to obtain delayed postoperative imaging to more accurately assess the location of the active contact. However, given limitations in the image-fusion software addressed previ-ously and the need to point merge the majority of preop-erative and postoperative MR scans in this study, it may be most beneficial to perform the postoperative MR with the head frame in place to improve merging capabilities and better assess lead location.

Some authors attribute error in preoperative targeting to the low resolution of STN on imaging using a 1.5-tesla MR scanner [12] . Indeed, this study has shown that the definition of STNs borders cannot be fully appreciated in about 10% of cases using 1.5-tesla MRI. Although 3-tesla MRI has improved contrast resolution, which may enhance target visualization, microelectrode recordings are still currently the most accepted and commonly used technique to evaluate targets intraoperatively. Intraoper-ative MRI is a promising adjunct to our targeting strate-gies [5] . Further, a recent report has proposed the use of a three-dimensional patient-specific brain model that may improve presurgical planning by accurately predict-ing brain shift [13] . Further studies are necessary to de-termine the utility of these modalities in clinical prac-tice.

CSF loss during DBS may be secondary to inherent qualities of the brain, failure to adequately seal the burr hole, and the time required to perform the procedure. We found a positive correlation between brain shift and the duration of surgery which is consistent with previous re-ports [4] . However, the majority of shift may occur dur-ing burr hole placement, according to a recent study us-ing intraoperative MRI [5] . Although groups A and B did not differ in age, older age appeared to be associated with brain shift. Elderly patients have been shown to have higher resistance to CSF outflow resulting in ventricular enlargement, which is commonly seen in older patients [14] . Another possible explanation for a positive correla-tion with age is the hypothesis that older age is associated with negative intracranial pressure [1517] . This may at least in part underlie increased cortical displacement in some patients due to the introduction of air into the cra-nial cavity. Hakim et al. [15] postulated that a dilated ven-tricular system commonly seen in elderly patients leads to dissipation of the transmantle pressure gradient across a larger surface area and negative intracranial pressure. Others argue that a new equilibrium is established due to a larger ventricular volume with very low or negative

pressures [16] . Further investigation is necessary at this point to determine the precise association between sur-gery duration and patient age with brain shift.

The RN is often a reliable visual landmark for indirect STN localization [2, 7, 18] . Ideally, we would have mea-sured the borders of STN in the postoperative images; however, visualization of its borders was difficult given the artifact surrounding the implanted lead. Thus, we were unable to directly measure shift of STN and used RN as a surrogate marker of positional change. This issue may be resolved by an investigation of patients undergo-ing unilateral DBS surgery, in which the postoperative location of the contralateral STN could be measured. Un-til then, RN is a promising alternative to measuring sub-cortical shift given its proximity to STN and the remark-able clarity of its borders on postoperative T 2 -weighted images ( fig. 4 ). If one assumes that the RN-STN spatial relationship is unaffected by cortical shift, then RN may be a more suitable marker for STN shift than AC. Our data revealed shift of RN in the posterior direction, and given the assumption that the RN-STN relationship re-mains constant despite cortical shift, this may explain why multiple tracks with only posterior correction were required to target STN optimally. Many of the cases in-cluded in this study were associated with significant post-operative shift of RN. It appears that these cases required multiple trajectories aimed posteriorly to the predeter-mined target to obtain the expected microelectrode re-cording patterns of STN and the appropriate responses to test stimulation. This finding is indirect evidence for pos-terior shift of STN and that RN is a reliable marker of STN position.

The clinical importance of this study is highlighted by the increased number of recording tracks required in cas-es where brain shift was observed. Although these differ-ences did not reach statistical significance, this was only due to sample size. Increasing our sample size by a factor of four would have demonstrated a statistically signifi-cant difference. The risk of brain shift may justify the necessity of microelectrode recordings during DBS sur-gery. Furthermore, this study emphasizes the importance of realizing that in cases where there may be increased risk of brain shift, there may be a need to take a posterior trajectory if the patient is primarily in the supine posi-tion. Our data support that elderly patients may be at in-creased risk for significant brain shift during DBS sur-gery. The duration of time elapsed between incision and skin closure also appears to be associated with significant deformation. In addition, when there is significant corti-cal brain shift, immediate postoperative imaging may be

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inaccurate in determining the location of the electrodes in relation to the underlying subcortical target struc-tures.

Conclusions

Subcortical structures appear to shift posteriorly dur-ing DBS surgery when performed primarily in the supine position. This may compromise accuracy of preoperative targeting measurements and must be considered when intraoperative microelectrode recording patterns and

test stimulations are suboptimal. Intraoperative shift may be due at least in part to CSF loss and correlates with patient age and the duration of time elapsed between in-cision and skin closure. In cases of significant brain shift, multiple trajectories may be necessary to target STN ac-curately despite preoperative direct and indirect mea-surements. This puts patients at greater risk for develop-ing complications. Although postoperative imaging is necessary to confirm accuracy of lead placement, delayed postoperative imaging may be preferable to more accu-rately evaluate the location of the final active contact in cases with large cortical displacement.

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