LETTERS:
PUBLISHED
Validation of CT-MRI Fusion for Intraoperative Assessment of Stereotactic Accuracy in DBS Surgery The article by Mirzadeh et al.1 contains errors conveying the inappropriate impression that intraoperative CT fused with preoperative MRI alone provides “accurate” placement of the DBS lead. First, the researchers did not study accuracy (percent reaching the clinically effective target), but rather precision (percentage reaching a single point). One can reproducibly (high precision) put the DBS lead in the wrong location (poor accuracy). Second, the researchers reference Ostrem et al.2 describing excellent outcomes with CT only comparable to use of microelectrode recordings (MERs). At best, Ostrem et al.,2 and similar studies, only showed no obvious differences. However, failure to demonstrate a difference is not evidence of no difference, and the results could merely be a type II statistical error, which is likely given the small sample sizes typically used. There are more appropriate statistical approaches to demonstrate noninferiority.3 Third, the researchers err by describing their methods as “direct” targeting, which presupposes that the actual target can be directly visualized. Whereas the STN may be visualized, the actual target is the sensorimotor region of the STN, which does not differ in its MRI or CT signals from adjacent STN regions, which should be avoided, such as the cognitive and limbic regions. Consequently, the sensorimotor region cannot be directly targeted. These researchers, as have other researchers, create a “straw man” false argument by suggesting that the use of MERs results in multiple penetrations of the brain and increased risk. However, in the retrospective study by Montgomery,4 the average number of MER penetrations for DBS in the vicinity of STN in 144 surgeries was 1.40, compared to 1.18 penetrations without MER in the study by Ostrem et al.2 The researchers use another straw man false argument to suggest
------------------------------------------------------------
ARTICLE
that their methods allow the patient to be asleep with the implication that MER use does not. This is not true given that MERs can be done using dexmedetomidine anesthesia. The researchers quoted Montgomery4 out of context, ascribing to Montgomery that the use of MERs relies on the “admitted assumption that the physiologically defined optimal target is sufficiently predictive of subsequent clinical response.” That was the assumption for the research study, but it is not the assumption made when deciding to use MER clinically. Rather, the decision to use MER is based on reasoned clinical judgment grounded on numerous factors, particularly the impossibility to date of alternative methods to directly target the sensorimotor regions, and in the case of the ventral intermediate nucleus of the thalamus and the globus pallidus interna, the appropriate sensorimotor homunculus of the DBS targets. Finally, the researchers use argumentum ignorantiam (arguing from ignorance), stating that there is no level 1 evidence supporting the use of MERs. This logic is analogous to “because I don’t know you are an honest person, you must not be an honest person.” There are many therapies lacking level 1 evidence, and failure to use those therapies risks malpractice. Erwin B. Montgomery, Jr., MD* Greenville Neuromodulation Center Greenville, Pennsylvania, USA
References 1.
Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. Validation of CT-MRI fusion for intraoperative assessment of stereotactic accuracy in DBS surgery. Mov Disord 2014;29:1788-1795.
2.
Ostrem JL, Galifianakis NB, Markun LC, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg 2013;115:708-712.
3.
Wellek S. Testing Statistical Hypotheses of Equivalence and Noninferiority, 2nd ed. Boca Raton, FL: CRC; 2010.
4.
Montgomery EB, Jr. Microelectrode targeting of the subthalamic nucleus for deep brain stimulation surgery. Mov Disord 2012;27: 1387-1391.
*Correspondence to: Erwin B. Montgomery, Dept. of Neurology, University of Alabama at Birmingham, Birmingham, AL United States, E-mail: [email protected]
Relevant conflicts of interest/financial disclosures: E.R.B. holds intellectual property rights on patents on automated microelectrode recording analyses; consults for FHC, Inc.; serves on the advisory boards for ST/Dystonia Inc. and the American Parkinson Disease Association; is employed by the Greenville Neuromodulation Center; and has received royalties from Oxford University Press. Full financial disclosures and author roles may be found in the online version of this article. Received: 6 December 2014; Accepted: 18 January 2015 Published online 0 Month 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.26178
Reply: DBS With Versus Without MER: Clinical Equipoise or Malpractice? We appreciate the commentary provided by Dr. Montgomery, as it focuses attention on several important aspects of the current practice of deep brain stimulation (DBS), some of which were addressed in our recent paper.1
Movement Disorders, Vol. 30, No. 3, 2015
439
L E T T E R S :
P U B L I S H E D
A R T I C L E
First, our study assessed the accuracy of stereotactic techniques for placement of a DBS lead at a surgeon-selected intracranial target in a series of patients. For the purposes of the data we reported, we studied our ability to surgically place the lead at that target, regardless of the clinical efficacy of stimulating the target. To confuse this definition of accuracy with that provided by Dr. Montgomery, regarding a clinically effective target, invokes many assumptions (discussed later) and thereby degrades the scientific merit of our study. Dr. Montgomery’s assertion that we were studying precision is incorrect. Precision is better reflected in the error bars around our accuracy measurement; that is, from one patient to the next, is our accuracy measurement consistent (we are precise) or highly variable (we are imprecise)? Second, Dr. Montgomery questions the validity of clinical outcomes data2,3 in DBS performed with image guidance alone without microelectrode recording (MER) because of the small sample sizes published to date (increasing the likelihood of type II error). This topic is not specifically addressed with primary data in our current paper, but we agree that larger studies are needed. We anticipate larger clinical outcomes studies for image-guided DBS in the near future as more practitioners use this method. As referenced in our manuscript, we are currently enrolling patients undergoing DBS with and without MER in a prospective study to compare outcomes more rigorously in larger samples. Third, Dr. Montgomery questions our use of the word “direct” to describe our targeting method because the sensorimotor region of the subthalamic nucleus (STN) is not visible on magnetic resonance imaging (MRI). This argument is largely semantic because 1) most authors and readers use and understand the terms “direct” and “indirect” targeting as we have used them; 2) our method is certainly more direct than the conventional indirect method based on stereotactic atlases; and 3) although the sensorimotor region of STN cannot be seen, studies evaluating clinically effective lead locations using postoperative imaging after MER-based DBS have revealed that the optimal target is the dorsolateral portion of the STN volume.4-9 Finally, and this is clearly the root of his issues with our paper, Dr. Montgomery defends MER as integral to the success of the DBS procedure and disparages any attempt to perform DBS without MER, as he has done in similar letters to the editor in the past 2 years in response to other primary research reports describing DBS without MER.10,11 As Dr. Montgomery asserts, it is not always necessary to have level I evidence, especially when without an alternative method of treatment.12 However, “asleep” DBS is an alternative approach with accumulating data to support its safety and efficacy, and it deserves to be fairly assessed. We apologize for citing Dr. Montgomery’s quote13 out of context, but,
-----------------------------------------------------------*Correspondence to: Francisco A. Ponce, MD, c/o Neuroscience Publications; Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W. Thomas Road; Phoenix, AZ 85013, USA, E-mail: [email protected] Relevant conflicts of interest/financial disclosures: Nothing to report. Author roles may be found in the online version of this article. Received: 12 January 2015; Accepted: 18 January 2015 Published online 17 February 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.26168
440
Movement Disorders, Vol. 30, No. 3, 2015
regardless, that the electrophysiologically defined optimal target is predictive of clinical response remains unproven. In fact, other studies challenge this assumption: 1) Bour et al.14 found that the site of best MER activity did not necessarily correlate with the site that showed the best clinical response on intraoperative macrostimulation testing; 2) Wodarg et al.15 found that MER was unable to distinguish differences in long-term clinical outcomes among patients but that lead location within the MRI-defined STN was predictive of motor response. We have no vested interest in performing DBS either with or without MER, because each approach may have its place in the physician’s armamentarium. Dr. Roy Bakay remarked in 1998 that “good stereotactic surgery for movement disorders can be performed with or without the microelectrode, and poor surgical results can occur both with and without the microelectrode.”16 More recently, Drs. Ron Alterman and Donald Weisz, who also routinely use MER in their DBS practices, stated in 2012 that “sufficient data exist to suggest that experienced surgeons can perform these procedures successfully without MER, and so it is left for those of us who continue to employ this technique to define precisely why we do so, not vice versa.”17 The data obtained with MER may provide the surgeon with information needed to “correct for anatomic variation as well as mechanical translational errors.”16 With the increasing availability of intraoperative imaging, coupled with advances in high-field MRI, we have new tools with which to reassess the “decades-old question”17 of whether or how MER improves targeting. In the existing literature, stereotactic analysis of postoperative imaging after DBS surgery has not been performed consistently. If one were to target the left STN at (212, 23, 24), and MER were to guide a 2-mm anterior offset, we might be led to believe that the target for that particular patient was actually (212, 21, 24). However, through routine stereotactic analysis of the final lead position, we find that in most of our cases, offsets guided by MER or test stimulation have the effect of moving the lead toward our initial plan, not away from the plan, such that, in the above example, the offset would have the effect of bringing the lead closer to, not farther from, (212, 23, 24) (manuscript in process). This implies that the initial plan was appropriate, and that our use of test stimulation and MER helped us to correct for stereotactic error or deflection, rather than for an incorrect anatomic target. Because these data are absent from the literature, this area deserves reappraisal for us to understand what is happening and why. Whether Dr. Montgomery means to suggest in his final point that “failure to use” MER “risks malpractice” is unclear, but if he does, we strongly disagree. We do not believe that this particular comment invites open scientific discourse and inquiry. “Asleep” DBS is not being performed on the fringes; rather, it is being subjected to rigorous scrutiny at the major DBS centers where it is offered; indeed, we believe a randomized trial comparing the two techniques is feasible. Zaman Mirzadeh, MD, PhD, and Francisco A. Ponce, MD Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona, USA
L E T T E R S :
Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. Validation of CT-MRI fusion for intraoperative assessment of stereotactic accuracy in DBS surgery. Mov Disord 2014;29:1788-1795.
2.
3.
A R T I C L E
effects of stimulation. J Neurol Neurosurg Psychiatry 2002;72:5358.
References 1.
P U B L I S H E D
9.
Foltynie T, Zrinzo L, Martinez-Torres I, et al. MRI-guided STN DBS in Parkinson’s disease without microelectrode recording: efficacy and safety. J Neurol Neurosurg Psychiatry 2011;82:358-363.
Maks CB, Butson CR, Walter BL, Vitek JL, McIntyre CC. Deep brain stimulation activation volumes and their association with neurophysiological mapping and therapeutic outcomes. J Neurol Neurosurg Psychiatry 2009;80:659-666.
10.
Ostrem JL, Galifianakis NB, Markun LC, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg 2013;115:708-712.
Montgomery EB, Jr. Letter to the editor: deep brain stimulation without microelectrode recording. J Neurosurg 2014;120:14971498.
11.
Montgomery EB, Jr. Microelectrode recordings in DBS: still in need of reasoned discussion. Mov Disord 2013;28:255.
12.
Smith G, Pell J. Parachute use to prevent death and major trauma related to gravitational challenge: systematic review of randomised controlled trials. Br Med J 2003;327:1459-1461.
4.
Starr PA, Christine CW, Theodosopoulos PV, et al. Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 2002;97:370-387.
13.
5.
Saint-Cyr JA, Hoque T, Pereira LC, et al. Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 2002;97:1152-1166.
Montgomery EB, Jr. Microelectrode targeting of the subthalamic nucleus for deep brain stimulation surgery. Mov Disord 2012;27: 1387-1391.
14.
6.
McClelland S, 3rd, Ford B, Senatus PB, et al. Subthalamic stimulation for Parkinson disease: determination of electrode location necessary for clinical efficacy. Neurosurg Focus 2005;19:E12.
Bour LJ, Contarino MF, Foncke EM, et al. Long-term experience with intraoperative microrecording during DBS neurosurgery in STN and GPi. Acta Neurochir 2010;152:2069-2077.
15.
7.
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: 216-225; discussion 225-216.
Wodarg F, Herzog J, Reese R, et al. Stimulation site within the MRI-defined STN predicts postoperative motor outcome. Mov Disord 2012;27:874-879.
16.
Bakay RA. Ablative surgery and deep brain stimulation for Parkinson’s disease: comments. Neurosurgery 1998;43:513.
17.
Alterman RL, Weisz D. Microelectrode recording during deep brain stimulation and ablative procedures. Mov Disord 2012;27: 1347-1349.
8.
Lanotte MM, Rizzone M, Bergamasco B, Faccani G, Melcarne A, Lopiano L. Deep brain stimulation of the subthalamic nucleus: anatomical, neurophysiological, and outcome correlations with the
Movement Disorders, Vol. 30, No. 3, 2015
441
PUBLISHED
Validation of CT-MRI Fusion for Intraoperative Assessment of Stereotactic Accuracy in DBS Surgery The article by Mirzadeh et al.1 contains errors conveying the inappropriate impression that intraoperative CT fused with preoperative MRI alone provides “accurate” placement of the DBS lead. First, the researchers did not study accuracy (percent reaching the clinically effective target), but rather precision (percentage reaching a single point). One can reproducibly (high precision) put the DBS lead in the wrong location (poor accuracy). Second, the researchers reference Ostrem et al.2 describing excellent outcomes with CT only comparable to use of microelectrode recordings (MERs). At best, Ostrem et al.,2 and similar studies, only showed no obvious differences. However, failure to demonstrate a difference is not evidence of no difference, and the results could merely be a type II statistical error, which is likely given the small sample sizes typically used. There are more appropriate statistical approaches to demonstrate noninferiority.3 Third, the researchers err by describing their methods as “direct” targeting, which presupposes that the actual target can be directly visualized. Whereas the STN may be visualized, the actual target is the sensorimotor region of the STN, which does not differ in its MRI or CT signals from adjacent STN regions, which should be avoided, such as the cognitive and limbic regions. Consequently, the sensorimotor region cannot be directly targeted. These researchers, as have other researchers, create a “straw man” false argument by suggesting that the use of MERs results in multiple penetrations of the brain and increased risk. However, in the retrospective study by Montgomery,4 the average number of MER penetrations for DBS in the vicinity of STN in 144 surgeries was 1.40, compared to 1.18 penetrations without MER in the study by Ostrem et al.2 The researchers use another straw man false argument to suggest
------------------------------------------------------------
ARTICLE
that their methods allow the patient to be asleep with the implication that MER use does not. This is not true given that MERs can be done using dexmedetomidine anesthesia. The researchers quoted Montgomery4 out of context, ascribing to Montgomery that the use of MERs relies on the “admitted assumption that the physiologically defined optimal target is sufficiently predictive of subsequent clinical response.” That was the assumption for the research study, but it is not the assumption made when deciding to use MER clinically. Rather, the decision to use MER is based on reasoned clinical judgment grounded on numerous factors, particularly the impossibility to date of alternative methods to directly target the sensorimotor regions, and in the case of the ventral intermediate nucleus of the thalamus and the globus pallidus interna, the appropriate sensorimotor homunculus of the DBS targets. Finally, the researchers use argumentum ignorantiam (arguing from ignorance), stating that there is no level 1 evidence supporting the use of MERs. This logic is analogous to “because I don’t know you are an honest person, you must not be an honest person.” There are many therapies lacking level 1 evidence, and failure to use those therapies risks malpractice. Erwin B. Montgomery, Jr., MD* Greenville Neuromodulation Center Greenville, Pennsylvania, USA
References 1.
Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. Validation of CT-MRI fusion for intraoperative assessment of stereotactic accuracy in DBS surgery. Mov Disord 2014;29:1788-1795.
2.
Ostrem JL, Galifianakis NB, Markun LC, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg 2013;115:708-712.
3.
Wellek S. Testing Statistical Hypotheses of Equivalence and Noninferiority, 2nd ed. Boca Raton, FL: CRC; 2010.
4.
Montgomery EB, Jr. Microelectrode targeting of the subthalamic nucleus for deep brain stimulation surgery. Mov Disord 2012;27: 1387-1391.
*Correspondence to: Erwin B. Montgomery, Dept. of Neurology, University of Alabama at Birmingham, Birmingham, AL United States, E-mail: [email protected]
Relevant conflicts of interest/financial disclosures: E.R.B. holds intellectual property rights on patents on automated microelectrode recording analyses; consults for FHC, Inc.; serves on the advisory boards for ST/Dystonia Inc. and the American Parkinson Disease Association; is employed by the Greenville Neuromodulation Center; and has received royalties from Oxford University Press. Full financial disclosures and author roles may be found in the online version of this article. Received: 6 December 2014; Accepted: 18 January 2015 Published online 0 Month 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.26178
Reply: DBS With Versus Without MER: Clinical Equipoise or Malpractice? We appreciate the commentary provided by Dr. Montgomery, as it focuses attention on several important aspects of the current practice of deep brain stimulation (DBS), some of which were addressed in our recent paper.1
Movement Disorders, Vol. 30, No. 3, 2015
439
L E T T E R S :
P U B L I S H E D
A R T I C L E
First, our study assessed the accuracy of stereotactic techniques for placement of a DBS lead at a surgeon-selected intracranial target in a series of patients. For the purposes of the data we reported, we studied our ability to surgically place the lead at that target, regardless of the clinical efficacy of stimulating the target. To confuse this definition of accuracy with that provided by Dr. Montgomery, regarding a clinically effective target, invokes many assumptions (discussed later) and thereby degrades the scientific merit of our study. Dr. Montgomery’s assertion that we were studying precision is incorrect. Precision is better reflected in the error bars around our accuracy measurement; that is, from one patient to the next, is our accuracy measurement consistent (we are precise) or highly variable (we are imprecise)? Second, Dr. Montgomery questions the validity of clinical outcomes data2,3 in DBS performed with image guidance alone without microelectrode recording (MER) because of the small sample sizes published to date (increasing the likelihood of type II error). This topic is not specifically addressed with primary data in our current paper, but we agree that larger studies are needed. We anticipate larger clinical outcomes studies for image-guided DBS in the near future as more practitioners use this method. As referenced in our manuscript, we are currently enrolling patients undergoing DBS with and without MER in a prospective study to compare outcomes more rigorously in larger samples. Third, Dr. Montgomery questions our use of the word “direct” to describe our targeting method because the sensorimotor region of the subthalamic nucleus (STN) is not visible on magnetic resonance imaging (MRI). This argument is largely semantic because 1) most authors and readers use and understand the terms “direct” and “indirect” targeting as we have used them; 2) our method is certainly more direct than the conventional indirect method based on stereotactic atlases; and 3) although the sensorimotor region of STN cannot be seen, studies evaluating clinically effective lead locations using postoperative imaging after MER-based DBS have revealed that the optimal target is the dorsolateral portion of the STN volume.4-9 Finally, and this is clearly the root of his issues with our paper, Dr. Montgomery defends MER as integral to the success of the DBS procedure and disparages any attempt to perform DBS without MER, as he has done in similar letters to the editor in the past 2 years in response to other primary research reports describing DBS without MER.10,11 As Dr. Montgomery asserts, it is not always necessary to have level I evidence, especially when without an alternative method of treatment.12 However, “asleep” DBS is an alternative approach with accumulating data to support its safety and efficacy, and it deserves to be fairly assessed. We apologize for citing Dr. Montgomery’s quote13 out of context, but,
-----------------------------------------------------------*Correspondence to: Francisco A. Ponce, MD, c/o Neuroscience Publications; Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W. Thomas Road; Phoenix, AZ 85013, USA, E-mail: [email protected] Relevant conflicts of interest/financial disclosures: Nothing to report. Author roles may be found in the online version of this article. Received: 12 January 2015; Accepted: 18 January 2015 Published online 17 February 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.26168
440
Movement Disorders, Vol. 30, No. 3, 2015
regardless, that the electrophysiologically defined optimal target is predictive of clinical response remains unproven. In fact, other studies challenge this assumption: 1) Bour et al.14 found that the site of best MER activity did not necessarily correlate with the site that showed the best clinical response on intraoperative macrostimulation testing; 2) Wodarg et al.15 found that MER was unable to distinguish differences in long-term clinical outcomes among patients but that lead location within the MRI-defined STN was predictive of motor response. We have no vested interest in performing DBS either with or without MER, because each approach may have its place in the physician’s armamentarium. Dr. Roy Bakay remarked in 1998 that “good stereotactic surgery for movement disorders can be performed with or without the microelectrode, and poor surgical results can occur both with and without the microelectrode.”16 More recently, Drs. Ron Alterman and Donald Weisz, who also routinely use MER in their DBS practices, stated in 2012 that “sufficient data exist to suggest that experienced surgeons can perform these procedures successfully without MER, and so it is left for those of us who continue to employ this technique to define precisely why we do so, not vice versa.”17 The data obtained with MER may provide the surgeon with information needed to “correct for anatomic variation as well as mechanical translational errors.”16 With the increasing availability of intraoperative imaging, coupled with advances in high-field MRI, we have new tools with which to reassess the “decades-old question”17 of whether or how MER improves targeting. In the existing literature, stereotactic analysis of postoperative imaging after DBS surgery has not been performed consistently. If one were to target the left STN at (212, 23, 24), and MER were to guide a 2-mm anterior offset, we might be led to believe that the target for that particular patient was actually (212, 21, 24). However, through routine stereotactic analysis of the final lead position, we find that in most of our cases, offsets guided by MER or test stimulation have the effect of moving the lead toward our initial plan, not away from the plan, such that, in the above example, the offset would have the effect of bringing the lead closer to, not farther from, (212, 23, 24) (manuscript in process). This implies that the initial plan was appropriate, and that our use of test stimulation and MER helped us to correct for stereotactic error or deflection, rather than for an incorrect anatomic target. Because these data are absent from the literature, this area deserves reappraisal for us to understand what is happening and why. Whether Dr. Montgomery means to suggest in his final point that “failure to use” MER “risks malpractice” is unclear, but if he does, we strongly disagree. We do not believe that this particular comment invites open scientific discourse and inquiry. “Asleep” DBS is not being performed on the fringes; rather, it is being subjected to rigorous scrutiny at the major DBS centers where it is offered; indeed, we believe a randomized trial comparing the two techniques is feasible. Zaman Mirzadeh, MD, PhD, and Francisco A. Ponce, MD Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona, USA
L E T T E R S :
Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. Validation of CT-MRI fusion for intraoperative assessment of stereotactic accuracy in DBS surgery. Mov Disord 2014;29:1788-1795.
2.
3.
A R T I C L E
effects of stimulation. J Neurol Neurosurg Psychiatry 2002;72:5358.
References 1.
P U B L I S H E D
9.
Foltynie T, Zrinzo L, Martinez-Torres I, et al. MRI-guided STN DBS in Parkinson’s disease without microelectrode recording: efficacy and safety. J Neurol Neurosurg Psychiatry 2011;82:358-363.
Maks CB, Butson CR, Walter BL, Vitek JL, McIntyre CC. Deep brain stimulation activation volumes and their association with neurophysiological mapping and therapeutic outcomes. J Neurol Neurosurg Psychiatry 2009;80:659-666.
10.
Ostrem JL, Galifianakis NB, Markun LC, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg 2013;115:708-712.
Montgomery EB, Jr. Letter to the editor: deep brain stimulation without microelectrode recording. J Neurosurg 2014;120:14971498.
11.
Montgomery EB, Jr. Microelectrode recordings in DBS: still in need of reasoned discussion. Mov Disord 2013;28:255.
12.
Smith G, Pell J. Parachute use to prevent death and major trauma related to gravitational challenge: systematic review of randomised controlled trials. Br Med J 2003;327:1459-1461.
4.
Starr PA, Christine CW, Theodosopoulos PV, et al. Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 2002;97:370-387.
13.
5.
Saint-Cyr JA, Hoque T, Pereira LC, et al. Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 2002;97:1152-1166.
Montgomery EB, Jr. Microelectrode targeting of the subthalamic nucleus for deep brain stimulation surgery. Mov Disord 2012;27: 1387-1391.
14.
6.
McClelland S, 3rd, Ford B, Senatus PB, et al. Subthalamic stimulation for Parkinson disease: determination of electrode location necessary for clinical efficacy. Neurosurg Focus 2005;19:E12.
Bour LJ, Contarino MF, Foncke EM, et al. Long-term experience with intraoperative microrecording during DBS neurosurgery in STN and GPi. Acta Neurochir 2010;152:2069-2077.
15.
7.
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: 216-225; discussion 225-216.
Wodarg F, Herzog J, Reese R, et al. Stimulation site within the MRI-defined STN predicts postoperative motor outcome. Mov Disord 2012;27:874-879.
16.
Bakay RA. Ablative surgery and deep brain stimulation for Parkinson’s disease: comments. Neurosurgery 1998;43:513.
17.
Alterman RL, Weisz D. Microelectrode recording during deep brain stimulation and ablative procedures. Mov Disord 2012;27: 1347-1349.
8.
Lanotte MM, Rizzone M, Bergamasco B, Faccani G, Melcarne A, Lopiano L. Deep brain stimulation of the subthalamic nucleus: anatomical, neurophysiological, and outcome correlations with the
Movement Disorders, Vol. 30, No. 3, 2015
441
