- Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, United Kingdom
- Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, London, WC1N 3BG, United Kingdom
Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, United Kingdom
Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, London, WC1N 3BG, United Kingdom
DOI:10.4103/2152-7806.91612Copyright: © 2012 Zrinzo L. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
How to cite this article: Zrinzo L. Pitfalls in precision stereotactic surgery. Surg Neurol Int 14-Jan-2012;3:
How to cite this URL: Zrinzo L. Pitfalls in precision stereotactic surgery. Surg Neurol Int 14-Jan-2012;3:. Available from: http://sni.wpengine.com/surgicalint_articles/pitfalls-in-precision-stereotactic-surgery/
Precision is the ultimate aim of stereotactic technique. Demands on stereotactic precision reach a pinnacle in stereotactic functional neurosurgery. Pitfalls are best avoided by possessing in-depth knowledge of the techniques employed and the equipment used. The engineering principles of arc-centered stereotactic frames maximize surgical precision at the target, irrespective of the surgical trajectory, and provide the greatest degree of surgical precision in current clinical practice. Stereotactic magnetic resonance imaging (MRI) provides a method of visualizing intracranial structures and fiducial markers on the same image without introducing significant errors during an image fusion process. Although image distortion may potentially limit the utility of stereotactic MRI, near-complete distortion correction can be reliably achieved with modern machines. Precision is dependent on minimizing errors at every step of the stereotactic procedure. These steps are considered in turn and include frame application, image acquisition, image manipulation, surgical planning of target and trajectory, patient positioning and the surgical procedure itself. Audit is essential to monitor and improve performance in clinical practice. The level of stereotactic precision is best analyzed by routine postoperative stereotactic MRI. This allows the stereotactic and anatomical location of the intervention to be compared with the anatomy and coordinates of the intended target, avoiding significant image fusion errors.
Keywords: Magnetic resonance imaging, precision, stereotactic
In 1906, Clarke and Horsley published a landmark paper describing a topographical method of precise navigation within the brain of an experimental animal.[
Since these early beginnings, numerous technological advancements have been adopted to improve accuracy and precision of stereotactic interventions. Ventriculography[
Technological advances have culminated in the advent of stereotactic magnetic resonance imaging (MRI), a tool that permits in vivo stereotactic localization of visualized pathological and anatomical structures, both before and after the surgical intervention.
Surgical accuracy is a measure of the degree of veracity or proximity of the intervention to the intended target. Surgical precision is the degree of reproducibility or repeatability of the intervention [
Specific indications demand varying levels of accuracy and precision. For instance, the level of accuracy and precision required during functional neurosurgery when targeting the sensorimotor portion of the subthalamic nucleus for Parkinson's disease is greater than that required when performing a biopsy of a large deep-seated lesion. Nevertheless, many of the principles that assist in improving precision and avoiding complications are relevant to any form of stereotactic surgery.
Pitfalls are defined as hidden or unsuspected dangers or difficulties. They are best avoided by considering known factors that may lead to potential problems. A thorough knowledge of clinical presentation, medical history, risk factors, and results of investigations, as well as an in-depth knowledge of the possible benefits and hazards of surgery are essential when considering patient selection.
Despite their relatively low incidence, hemorrhagic complications carry by far the highest risk of devastating neurological outcome in functional neurosurgery. Self-medication with aspirin or non-steroidal anti-inflammatory drugs may not be disclosed unless the physician asks specifically about their use.[
As with other surgical procedures, patient selection and perioperative management play a crucial role in avoiding complications. However, this work focuses on the technical aspects of ensuring precision during a stereotactic procedure. The most reliable way of avoiding potential pitfalls is by having a surgeon who understands the basic principles of the technique and is confident with the equipment being used.
Contemporary stereotactic frames are based on the arc-centered principle that tends to maximize surgical precision at the target, irrespective of the surgical trajectory. Mini-frame or frameless navigation enjoys maximum precision at the entry point and then endeavors to replicate the planned virtual trajectory during surgery. However, small errors in trajectory can translate into significant errors at the target level [
(a) The engineering principles of the arc-centred frame tend to maximise accuracy and precision at the target, irrespective of the surgical trajectory. (b) The engineering principles of mini-frame or frameless navigation maximise precision and accuracy at the entry point. Errors between planned and actual trajectory during surgery can result in significant errors at the target level
An early study comparing the accuracy of frame-based with frameless techniques did not find any significant difference between frame-based and mini-frame techniques. However, error calculations were based on “fused” images, introducing errors that render the methodology inappropriate in making such a comparison (see section on image fusion below).[
In a subsequent well-designed study from Lund, the stereotactic targeting error during thalamic deep brain stimulation (DBS) was significantly greater with mini-frame than with frame-based technique (2.5 ± 1.4 mm vs. 1.2 ± 0.6, P < 0.05–0.001).[
Given the greater accuracy and precision of frame-based techniques, this work focuses on frame-based surgery. However, many aspects are also applicable to other forms of stereotactic surgery.
Surgical robots allow precise, deliberate, and spatially encoded movement; in essence, they are stereotactic instruments with the potential of achieving high levels of accuracy.[
Stereotactic surgery demands meticulous attention to detail during every step of the procedure.
The surgeon should be familiar with the stereotactic system being used and knowledgeable about its strengths and weaknesses. Equipment should be checked prior to commencing a stereotactic procedure – a loose screw may result in geometrical inaccuracy that may compromise both the procedure and patient. As with any precision instrument, the stereotactic system requires regular maintenance and quality checks.
The stereotactic frame should be firmly secured to the skull to avoid any movement between image acquisition and surgery. Any such movement would result in targeting errors. A more perilous scenario would be if the head were to “slip” out of the fixation pins in the presence of an intracranial probe. On the other hand, overzealous tightening of pins should be avoided as this may result in penetration of the inner table of the skull and damage to intracranial structures.[
Due consideration should be give to the surgical trajectory and the frame placed such that the securing pins will not obstruct the surgical field. Particular consideration should be given when working with high-field MR machines and insulated posts should be used to prevent overheating of pin sites during imaging.
The surgeon should supervise acquisition of stereotactic images. Thin-slice contiguous images through the target are required using a modality that allows optimal localization of the planned target. The use of contrast media will highlight vessels that can then be avoided during surgical planning. Rare instances of iatrogenic pseudoaneurysm have been reported following stereotactic procedures.[
An effort should be made to ensure that the axes of the frame are in line with those of the scanner. A small spirit level will assist alignment of the frame axes with the scanning plane and will ensure that frame geometry is reproduced accurately on cross-sectional imaging. This is particularly important if the surgeon is relying upon manual calculation of target coordinates.
When obtaining a stereotactic MRI, the target region should be centered within the bore of the magnet since this is the region where MR distortion is the least. The field of view should include all the required fiducial markers and imaging should cover the intended entry point and target. Thin-slice contiguous imaging from entry point to target is also desirable.
MRI sequences designed for visualization of specific targets allow direct localization of anatomical structures. T2-weighted images may be used to visualize the subthalamic nucleus[
Geometric distortion and MRI-guided surgery
Unlike diagnostic radiology, imaging for stereotactic surgery requires more than just visualization of structures. Although computed tomography (CT) imaging does not suffer from image distortion, anatomical detail is lacking in comparison with MRI. Inhomogeneities of the magnetic field within MR scanners can lead to geometric distortion of the acquired images.[
A number of methods for correction of field inhomogeneities have been described.[
With adequate care and quality control, high fidelity stereotactic MR images offer a true geometric representation of spatial arrangement with distortion errors in the subvoxel range.[
Image fusion – An under-recognized and significant source of targeting error
Initial attempts to circumvent problems of MR distortion relied on fusing or morphing non-stereotactic MR data onto stereotactic CT images. This idea suggested that contrast-rich MR data at the center of the field could be supplemented with accurate fiducial localization with CT at the field periphery.[
Image manipulation and registration
Some stereotactic systems allow manual calculation of the target coordinates from a selected target slice [
Manual calculation of target coordinates from axial T2 weighted image with the Leksell frame. The outer fiducials of the lateral plates form a rectangle; the diagonals of this rectangle intersect at the centre of the frame. The geometry of the frame dictates that the Z (vertical) coordinate can be determined by adding 40 mm to the distance between the posterior and middle fiducial markers on the lateral fiducial plates. X (mediolateral) and Y (anteroposterior) axes are defined by lines drawn through the frame centre and parallel to the sides of the rectangle. The geometry of the frame dictates that centre of the frame corresponds to X = 100 mm and Y = 100 mm. The X and Y coordinate of any point within the image can therefore be calculated by measuring its displacement from the centre of the frame. Lateral displacements to the left are added and displacements to the right subtracted from 100 to give the X coordinate. Anterior displacements are added to 100 and posterior displacements subtracted from 100 to give the Y coordinate. In this example, a target was selected in the right STN: Z coordinate = 40 + (Z1 + Z2)/2 mm; X coordinate = (100 − X1) mm, since the target lies to the right of the frame centre. Y coordinate = (100 + Y1) mm since the target lies anterior to the frame centre
The default on some software platforms is to minimize registration error across the volume of the acquired images. However, the aim of stereotactic surgery is to maximize accuracy at the target level. Therefore, accuracy of registration at the target slice / level is more desirable.
Surgical planning of the target and trajectory
A surgical trajectory that avoids sulci and ventricles has been shown to reduce the incidence of hemorrhagic complications, presumably by avoiding the enclosed vessels.[
In this example, the left subthalamic nucleus was targeted on T2 weighted stereotactic MRI (inset left). Stereotactic T1 volumetric images allowed selection of the entry point in the ipsilateral, pericoronal region right): Coronal and sagittal images are not sufficient to confirm avoidance of sulci and ventricles (left panel); this is best achieved by reformatting of the images in line with the planned trajectory (middle panel). The final target coordinates, together with the arc and ring angles then define the surgical trajectory (right). It should be noted that, prior to surgical planning, the fiducials were registered on the T2-weighted stereotactic MRI to avoid fusion errors during target selection. The entry point was selected on the basis of the volumetric T1 images fused to the T2 images and is therefore susceptible to errors of image fusion. However, inaccuracies are of less clinical relevance at the entry point than at the target point
Incursion into sulcus or ventricle can often be avoided by reconsideration of the planned entry point and, when performing DBS, can maximize the number of lead contacts within the target structure.
When considering stereotactic approaches to the brainstem, transgression of pial, ependymal, or tentorial surfaces can be avoided by considering ipsilateral transfrontal[
When performing biopsy of a partially solid, partially cystic lesion, the solid portion should be targeted first to prevent targeting errors that would occur with significant brain shift after cyst aspiration.
The author uses a simple proforma to record the target coordinates and the “arc” and “angle” of the trajectory. The target coordinates obtained from manual calculations may be compared to those obtained from the planning station. This process offers a measure of redundancy and reduces errors in the transcription of coordinates. Some groups use a checklist in an attempt to standardize the procedure.[
As with other forms of surgery, patient positioning is a vital part of the surgical procedure. Performing surgery in a similar position to that adopted during image acquisition may limit shift by minimizing postural movement of intracranial structures.[
Rather than being fixed to the operating table with a Mayfield clamp, head and frame may be supported by a sand-filled vacuum pillow. In the event of an intraoperative seizure, this precludes the head being forced from the retaining pins and the resulting brain trauma by an indwelling intracerebral probe.
Setting up the stereotactic equipment
Care must be taken when transferring coordinates to the frame. Some stereotactic systems provide a phantom that “double checks” the planned trajectory and coordinates (e.g. Cosman–Roberts–Wells or CRW).
Equipment essential to the procedure should be prepared and checked. Probes are assessed for any curvature that would undermine accuracy and precision. Implant and probe lengths are “marked out” according to the radius of the stereotactic system being used (e.g. 190 mm when using the Leksell frame, 160 mm when using the CRW) to ensure that the target is reached without being overshot. Equipment used for physiological monitoring (impedance, microelectrode recording) is tested.
After the coordinates are transferred to the frame, it is prudent to double check coordinates, ring, arc, and platform depth, and to perform a “reality check” on the patient to ensure that the planned trajectory and target are appropriate. When the entry point and trajectory have not been defined by the stereotactic plan, it is important to clearly mark the intended entry point on the scalp before draping to ensure that the entry point avoids eloquent cortex and venous sinuses.
Extradural surgical procedure
When a precise entry point has been planned, the surgical trajectory is re-established at each anatomical layer. A twist drill directed by the frame is sometimes employed when trephining the skull. However, a standard 14-mm burr hole provides access for hemostasis on the dura and the underlying pia and avoids transmission of excessive force to the frame. When not using the frame to direct the drill, it should be noted that when held perpendicular to the skull, the drill axis is often different from that of the planned trajectory. This should be taken into account to ensure that the final probe trajectory avoids the bony margins of the burr hole [
On the left of the figure the intended trajectory has been marked on the outer table of the skull (small black dot) and the “burrhole” centred on this point. This method does not take into account that the burrhole trajectory is orthogonal to the outer table and differs to the planned trajectory. As a result, the edge of the inner table obstructs the intended trajectory. On the right of the figure, the burrhole was placed slightly lateral to the intended trajectory (small black dot). This adjustment allows the planned trajectory to traverse the burrhole unimpeded by both outer and inner bone margins
Minimizing brain shift
Accurate stereotactic targeting does not necessarily result in accurate anatomical targeting. Brain shift or “brain sinking” has often been considered an obstacle to reliable neuronavigation based on preoperative images.[
Up to 5.7 mm of subcortical shift has been reported during DBS procedures, predominantly in the direction of gravity.[
A number of surgical practices may be expected to reduce or avoid brain shift. Reducing CSF loss and pneumocephalus can be accomplished by the following: minimizing the time from dural opening to final DBS electrode implantation, flooding the burr hole with saline irrigation after dural opening,[
Intradural surgical procedure
The dural opening should ensure that the trajectory avoids the margins of the burr hole and should be large enough to admit the stereotactic probe whilst being small enough to prevent excessive CSF loss. The underlying pia is opened sharply and hemostasis secured before the probe is advanced into the brain parenchyma.
A sharp tip probe would theoretically result in less brain deformation; however, the authors favor a blunt tip probe in view of potential penetration, rather than displacement, of intraparenchymal vessels and the resulting hemorrhage [
Blunt probes tend to displace rather than rupture blood vessels crossing the surgical trajectory. These still shots are from an endoscopic video recorded during extraction of a small, 3 mm diameter blunt- tip endoscope from the brain. The left panel demonstrates the parenchyma and vessels in the distal brain track without evidence of haemorrhage. On the middle panel, a larger calibre vessel (arteriole) appears out of focus on the left side of the picture as the endoscope is withdrawn. The right panel confirms that the aforementioned vessel was in the path of the probe. The vessel had clearly been pushed aside by the advancing probe without damage or penetration causing haemorrhage (video courtesy of Prof Marwan Hariz)
After the dura has been opened, high-flow saline irrigation and sealing of the defect with fibrin glue (Tisseel VH Fibrin Sealant, Baxter AG) will prevent excessive CSF egress – an important consideration when performing bilateral surgery.
Brain mapping in functional neurosurgery
Microelectrode recording (MER) is currently the most commonly used technique for physiological brain mapping. Despite the lack of available evidence that this approach improves clinical outcome, many groups believe that the target should be identified physiologically with MER. Some authors have suggested that the presence of brain shift demands the use of surrogate markers during precision stereotactic surgery in order to adjust for stereotactic and anatomical targeting errors.[
Some authors avoid brain mapping in favor of an MRI-guided and MRI-verified approach that minimizes brain shift;[
Postoperative stereotactic imaging best documents the accuracy and precision of an intervention – this allows a comparison of the intended target coordinates with the actual target coordinates of the surgical intervention [
Calculation of the stereotactic targeting error in a DBS procedure: the planned target point is shown in relation to the actual quadripolar lead location. The centres of the deepest and most superficial DBS contact and the intended target point form a triangle in space (depicted in blue with sides a, b and c). The perpendicular distance between planned target point and electrode trajectory (h) is defined as the stereotactic targeting error
Safety is a concern when performing MRI in the presence of implanted DBS hardware and neurosurgeons should liaise closely with radiology and MR physicist colleagues to establish local practices and monitoring of MRI events. They should also be aware of the reality that the number of reported adverse neurological events in such situations is extremely low when sensible precautions are taken and many thousands of MRI scans have been obtained with implanted MRI hardware without adverse consequences.[
Imprecision of stereotactic targeting can be rectified immediately since the frame can be used to guide an additional brain pass. The previous stereotactic coordinates are modified according to the observed targeting error. Extension of the initial dural opening will allow a new corticotomy a few millimeters away from the first in the direction of the targeting error. This approach avoids the trajectory of the new track crossing that of the old and results in correction of suboptimal targeting.
Numerous stereotactic systems are currently used in clinical practice and a variety of intra-procedural techniques are employed with the aim of improving safety and precision of the surgical procedure. Comprehensive clinical assessment, appropriate patient selection, purposeful stereotactic visualization of the brain target, meticulous calculation of coordinates and trajectory, and a surgical team that is familiar with the basic principles of the techniques being employed are essential in avoiding pitfalls. Routine acquisition of postoperative stereotactic imaging documents the actual location of the surgical procedure and allows comparison with the intended target. Meticulous audit of the results will allow incremental improvement in the accuracy and precision of stereotactic surgery.
Publication of this manuscript has been made possible by an educational grant from
1. Abernathey CD, Camacho A, Kelly PJ. Stereotaxic suboccipital transcerebellar biopsy of pontine mass lesions. J Neurosurg. 1989. 70: 195-200
2. Alexander E, Kooy HM, van Herk M, Schwartz M, Barnes PD, Tarbell N. Magnetic resonance image-directed stereotactic neurosurgery: Use of image fusion with computerized tomography to enhance spatial accuracy. J Neurosurg. 1995. 83: 271-6
3. Amundson EW, McGirt MJ, Olivi A. A contralateral, transfrontal, extraventricular approach to stereotactic brainstem biopsy procedures. Technical note. J Neurosurg. 2005. 102: 565-70
4. Aziz TZ, Nandi D, Parkin S, Liu X, Giladi N, Bain P. Targeting the subthalamic nucleus. Stereotact Funct Neurosurg. 2001. 77: 87-90
5. Bakay R, Smith A. Deep brain stimulation: Complications and attempts at avoiding them. Open Neurosurg J. 2011. 4: 42-52
6. Bjartmarz H, Rehncrona S. Comparison of accuracy and precision between frame-based and frameless stereotactic navigation for deep brain stimulation electrode implantation. Stereotact Funct Neurosurg. 2007. 85: 235-42
7. Chang EF, Cheng JS, Richardson RM, Lee C, Starr PA, Larson PS. Incidence and management of venous air embolisms during awake deep brain stimulation surgery in a large clinical series. Stereotact Funct Neurosurg. 2011. 89: 76-82
8. Chang H, Fitzpatrick JM. A technique for accurate magnetic resonance imaging in the presence of field inhomogeneities. IEEE Trans Med Imaging. 1992. 11: 319-29
9. Cif L, Vasques X, Gonzalez V, Ravel P, Biolsi B, Collod-Beroud G. Long-term follow-up of DYT1 dystonia patients treated by deep brain stimulation: An open-label study. Mov Disord. 2010. 25: 289-99
10. Clarke RH, Horsley V. On a method of investigating the deep ganglia and tracts of the central nervous system (cerebellum). BMJ. 1906. 2: 1799-800
11. Coffey RJ, Lunsford LD. Stereotactic surgery for mass lesions of the midbrain and pons. Neurosurgery. 1985. 17: 12-8
12. Connolly PJ, Kilpatrick M, Jaggi JL, Church E, Baltuch GH. Feasibility of an operational standardized checklist for movement disorder surgery.A pilot study. Stereotact Funct Neurosurg. 2009. 87: 94-100
13. Cuny E, Guehl D, Burbaud P, Gross C, Dousset V, Rougier A. Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: The role of electrophysiological guidance. J Neurosurg. 2002. 97: 591-7
14. Dandy WE. Ventriculography following the injection of air into the cerebral ventricles. Ann Surg. 1918. 68: 5-11
15. Doran SJ, Charles-Edwards L, Reinsberg SA, Leach MO. A complete distortion correction for MR images: I.Gradient warp correction. Phys Med Biol. 2005. 50: 1343-61
16. Duffner F, Schiffbauer H, Breit S, Friese S, Freudenstein D. Relevance of image fusion for target point determination in functional neurosurgery. Acta Neurochir (Wien). 2002. 144: 445-51
17. Elias WJ, Fu KM, Frysinger RC. Cortical and subcortical brain shift during stereotactic procedures. J Neurosurg. 2007. 107: 983-8
18. Elias WJ, Sansur CA, Frysinger RC. Sulcal and ventricular trajectories in stereotactic surgery. J Neurosurg. 2009. 110: 201-7
19. Eljamel MS. Robotic neurological surgery applications: Accuracy and consistency or pure fantasy?. Stereotact Funct Neurosurg. 2009. 87: 88-93
20. Foltynie T, Zrinzo L, Martinez-Torres I, Tripoliti E, Petersen E, Holl E. MRI-guided STN DBS in Parkinson's disease without microelectrode recording: Efficacy and safety. J Neurol Neurosurg Psychiatry. 2011. 82: 358-63
21. Guiot G, Hardy J, Albe-Fessard D. [Precise delimitation of the subcortical structures and identification of thalamic nuclei in man by stereotactic electrophysiology.]. Neurochirurgia (Stuttg). 1962. 5: 1-18
22. Guthrie BL, Steinberg GK, Adler JR. Posterior fossa stereotaxic biopsy using the Brown-Roberts-Wells stereotaxic system.Technical note. J Neurosurg. 1989. 70: 649-52
23. Halpern CH, Danish SF, Baltuch GH, Jaggi JL. Brain shift during deep brain stimulation surgery for Parkinson's disease. Stereotact Funct Neurosurg. 2008. 86: 37-43
24. Hariz MI, Krack P, Melvill R, Jorgensen JV, Hamel W, Hirabayashi H. A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg. 2003. 80: 96-101
25. Hirabayashi H, Tengvar M, Hariz MI. Stereotactic imaging of the pallidal target. Mov Disord. 2002. 17: S130-4
26. Holl EM, Petersen EA, Foltynie T, Martinez-Torres I, Limousin P, Hariz MI. Improving targeting in image-guided frame-based deep brain stimulation. Neurosurgery. 2010. 67: 437-47
27. Holloway KL, Gaede SE, Starr PA, Rosenow JM, Ramakrishnan V, Henderson JM. Frameless stereotaxy using bone fiducial markers for deep brain stimulation. J Neurosurg. 2005. 103: 404-13
28. Hooper AK, Okun MS, Foote KD, Haq IU, Fernandez HH, Hegland D. Venous air embolism in deep brain stimulation. Stereotact Funct Neurosurg. 2009. 87: 25-30
29. Kamiryo T, Jackson T, Laws E. A methodology designed to increase accuracy and safety in stereotactic brain surgery. Minim Invasive Neurosurg. 2000. 43: 1-3
30. Khan MF, Mewes K, Gross RE, Skrinjar O. Assessment of brain shift related to deep brain stimulation surgery. Stereotact Funct Neurosurg. 2008. 86: 44-53
31. Kondziolka D, Dempsey PK, Lunsford LD, Kestle JR, Dolan EJ, Kanal E. A comparison between magnetic resonance imaging and computed tomography for stereotactic coordinate determination. Neurosurgery. 1992. 30: 402-6
32. Krack P. Subthalamic stimulation for Parkinson's disease: A new benchmark. J Neurol Neurosurg Psychiatry. 2011. 82: 356-7
33. Kratimenos GP, Nouby RM, Bradford R, Pell MF, Thomas DG. Image directed stereotactic surgery for brain stem lesions. Acta Neurochir (Wien). 1992. 116: 164-70
34. Kumar R, Goyal V, Chauhan RS. Venous air embolism during microelectrode recording in deep brain stimulation surgery in an awake supine patient. Br J Neurosurg. 2009. 23: 446-8
35. Langlois S, Desvignes M, Constans JM, Revenu M. MRI geometric distortion: A simple approach to correcting the effects of non-linear gradient fields. J Magn Reson Imaging. 1999. 9: 821-31
36. Leksell L, Leksell D, Schwebel J. Stereotaxis and nuclear magnetic resonance. J Neurol Neurosurg Psychiatry. 1985. 48: 14-8
37. Martin AJ, Larson PS, Ostrem JL, Keith Sootsman W, Talke P, Weber OM. Placement of deep brain stimulator electrodes using real-time high-field interventional magnetic resonance imaging. Magn Reson Med. 2005. 54: 1107-14
38. Mathisen JR, Giunta F, Marini G, Backlund EO. Transcerebellar biopsy in the posterior fossa: 12 years experience. Surg Neurol. 1987. 28: 100-4
39. Miyagi Y, Shima F, Sasaki T. Brain shift: An error factor during implantation of deep brain stimulation electrodes. J Neurosurg. 2007. 107: 989-97
40. Nathoo N, Cavusoglu MC, Vogelbaum MA, Barnett GH. In touch with robotics: Neurosurgery for the future. Neurosurgery. 2005. 56: 421-33
41. Nazzaro JM, Lyons KE, Honea RA, Mayo MS, Cook-Wiens G, Harsha A. Head positioning and risk of pneumocephalus, air embolism, and hemorrhage during subthalamic deep brain stimulation surgery. Acta Neurochirurgica. 2010. 152: 2047-52
42. Neal JH, Van Norman AS. Transcerebellar biopsy of posterior fossa lesions using the Leksell gamma model stereotactic frame. Neurosurgery. 1993. 32: 473-4
43. O’Gorman RL, Jarosz JM, Samuel M, Clough C, Selway RP, Ashkan K. CT/MR image fusion in the postoperative assessment of electrodes implanted for deep brain stimulation. Stereotact Funct Neurosurg. 2009. 87: 205-10
44. Pallavaram S, Dawant BM, Remple M, Neimat JS, Kao C, Konrad PE. Effect of brain shift on the creation of functional atlases for deep brain stimulation surgery. Int J Comput Assist Radiol Surg. 2010. 5: 221-8
45. Patel NK, Plaha P, Gill SS. Magnetic resonance imaging-directed method for functional neurosurgery using implantable guide tubes. Neurosurgery. 2007. 61: 358-65
46. Patel NK, Plaha P, O’Sullivan K, McCarter R, Heywood P, Gill SS. MRI directed bilateral stimulation of the subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry. 2003. 74: 1631-7
47. Petersen EA, Holl EM, Martinez-Torres I, Foltynie T, Limousin P, Hariz MI. Minimizing brain shift in stereotactic functional neurosurgery. Neurosurgery. 2010. 67: 213-21
48. Rayes M, Bahgat DA, Kupsky WJ, Mittal S. Middle cerebral artery pseudoaneurysm formation following stereotactic biopsy. Can J Neurol Sci. 2008. 35: 664-8
49. Reinsberg SA, Doran SJ, Charles-Edwards EM, Leach MO. A complete distortion correction for MR images: II.Rectification of static-field inhomogeneities by similarity-based profile mapping. Phys Med Biol. 2005. 50: 2651-61
50. Robinson BW, Bryan JS, Rosvold HE. Locating brain structures.Extensions to the impedance method. Arch Neurol. 1965. 13: 477-86
51. Rodriguez-Oroz MC, Rodriguez M, Leiva C, Rodriguez-Palmero M, Nieto J, Garcia-Garcia D. Neuronal activity of the red nucleus in Parkinson's disease. Mov Disord. 2008. 23: 908-11
52. Rohlfing T, Maurer CR, Dean D, Maciunas RJ. Effect of changing patient position from supine to prone on the accuracy of a Brown-Roberts-Wells stereotactic head frame system. Neurosurgery. 2003. 52: 610-8
53. Roujeau T, Machado G, Garnett MR, Miquel C, Puget S, Geoerger B. Stereotactic biopsy of diffuse pontine lesions in children. J Neurosurg. 2007. 107: 1-4
54. Sankar T, Lozano AM. Magnetic resonance imaging distortion in functional neurosurgery. World Neurosurg. 2011. 75: 29-31
55. Schiff SJ, Dunagan BK, Worth RM. Failure of single-unit neuronal activity to differentiate globus pallidus internus and externus in Parkinson disease. J Neurosurg. 2002. 97: 119-28
56. Smeding HM, Speelman JD, Koning-Haanstra M, Schuurman PR, Nijssen P, van Laar T. Neuropsychological effects of bilateral STN stimulation in Parkinson disease: A controlled study. Neurology. 2006. 66: 1830-6
57. Spiegel EA, Wycis HT, Marks M, Lee AJ. Stereotaxic Apparatus for Operations on the Human Brain. Science. 1947. 106: 349-50
58. Spiegelmann R, Friedman WA. Stereotactic suboccipital transcerebellar biopsy under local anesthesia using the Cosman-Roberts-Wells frame. Technical note. J Neurosurg. 1991. 75: 486-8
59. Starr PA, Martin AJ, Ostrem JL, Talke P, Levesque N, Larson PS. Subthalamic nucleus deep brain stimulator placement using high-field interventional magnetic resonance imaging and a skull-mounted aiming device: Technique and application accuracy. J Neurosurg. 2010. 112: 479-90
60. Sumanaweera TS, Adler JR, Glover GH, Hemler PF, van den Elsen PA, Martin D. Method for correcting magnetic resonance image distortion for frame-based stereotactic surgery, with preliminary results. J Image Guid Surg. 1995. 1: 151-7
61. Sumanaweera TS, Adler JR, Napel S, Glover GH. Characterization of spatial distortion in magnetic resonance imaging and its implications for stereotactic surgery. Neurosurgery. 1994. 35: 696-703
62. Sumanaweera TS, Glover GH, Binford TO, Adler JR. MR susceptibility misregistration correction. IEEE Trans Med Imaging. 1993. 12: 251-9
63. Van Horn G, Hassenbusch SJ, Zouridakis G, Mullani NA, Wilde MC, Papanicolaou AC. Pallidotomy: A comparison of responders and nonresponders. Neurosurgery. 2001. 48: 263-71
64. Vitek JL, Bakay RA, Hashimoto T, Kaneoke Y, Mewes K, Zhang JY. Microelectrode-guided pallidotomy: Technical approach and its application in medically intractable Parkinson's disease. Journal of Neurosurgery. 1998. 88: 1027-43
65. Winkler D, Tittgemeyer M, Schwarz J, Preul C, Strecker K, Meixensberger J. The first evaluation of brain shift during functional neurosurgery by deformation field analysis. J Neurol Neurosurg Psychiatry. 2005. 76: 1161-3
66. Yu C, Apuzzo ML, Zee CS, Petrovich Z. A phantom study of the geometric accuracy of computed tomographic and magnetic resonance imaging stereotactic localization with the Leksell stereotactic system. Neurosurgery. 2001. 48: 1092-8
67. Yu C, Petrovich Z, Apuzzo ML, Luxton G. An image fusion study of the geometric accuracy of magnetic resonance imaging with the Leksell stereotactic localization system. J Appl Clin Med Phys. 2001. 2: 42-50
68. Zonenshayn M, Sterio D, Kelly PJ, Rezai AR, Beric A. Location of the active contact within the subthalamic nucleus (STN) in the treatment of idiopathic Parkinson's disease. Surg Neurol. 2004. 62: 216-25
69. Zrinzo L, Foltynie T, Limousin P, Hariz MI. Reducing hemorrhagic complications in functional neurosurgery: A large case series and systematic literature review. J Neurosurg. 2011. p.
70. Zrinzo L, van Hulzen AL, Gorgulho AA, Limousin P, Staal MJ, De Salles AA. Avoiding the ventricle: A simple step to improve accuracy of anatomical targeting during deep brain stimulation. J Neurosurg. 2009. 110: 1283-90
71. Zrinzo L, Yoshida F, Hariz MI, Thornton J, Foltynie T, Yousry TA. Clinical safety of brain magnetic resonance imaging with implanted deep brain stimulation hardware: Large case series and review of the literature. World Neurosurg. 2011. 76: 164-72
72. Zrinzo LU, Hariz MI, Lozano AM, Gildenberg PL, Tasker RR.editors. Recording in Functional Neurosurgery. Textbook of stereotactic and functional neurosurgery. Berlin: Springer; 2009. p. 1325-30