The Role of Microelectrode Recording and Stereotactic Computed Tomography in Verifying Lead Placement During Awake MRI-Guided Subthalamic Nucleus Deep Brain Stimulation for Parkinson's Disease

R Saman Vinke, Ashok K Selvaraj, Martin Geerlings, Dejan Georgiev, Aleksander Sadikov, Pieter L Kubben, Jonne Doorduin, Peter Praamstra, Bastiaan R Bloem, Ronald H M A Bartels, Rianne A J Esselink, R Saman Vinke, Ashok K Selvaraj, Martin Geerlings, Dejan Georgiev, Aleksander Sadikov, Pieter L Kubben, Jonne Doorduin, Peter Praamstra, Bastiaan R Bloem, Ronald H M A Bartels, Rianne A J Esselink

Abstract

Background: Bilateral deep brain stimulation of the subthalamic nucleus (STN-DBS) has become a cornerstone in the advanced treatment of Parkinson's disease (PD). Despite its well-established clinical benefit, there is a significant variation in the way surgery is performed. Most centers operate with the patient awake to allow for microelectrode recording (MER) and intraoperative clinical testing. However, technical advances in MR imaging and MRI-guided surgery raise the question whether MER and intraoperative clinical testing still have added value in DBS-surgery.

Objective: To evaluate the added value of MER and intraoperative clinical testing to determine final lead position in awake MRI-guided and stereotactic CT-verified STN-DBS surgery for PD.

Methods: 29 consecutive patients were analyzed retrospectively. Patients underwent awake bilateral STN-DBS with MER and intraoperative clinical testing. The role of MER and clinical testing in determining final lead position was evaluated. Furthermore, interobserver variability in determining the MRI-defined STN along the planned trajectory was investigated. Clinical improvement was evaluated at 12 months follow-up and adverse events were recorded.

Results: 98% of final leads were placed in the central MER-track with an accuracy of 0.88±0.45 mm. Interobserver variability of the MRI-defined STN was 0.84±0.09. Compared to baseline, mean improvement in MDS-UPDRS-III, PDQ-39 and LEDD were 26.7±16.0 points (54%) (p < 0.001), 9.0±20.0 points (19%) (p = 0.025), and 794±434 mg/day (59%) (p < 0.001) respectively. There were 19 adverse events in 11 patients, one of which (lead malposition requiring immediate postoperative revision) was a serious adverse event.

Conclusion: MER and intraoperative clinical testing had no additional value in determining final lead position. These results changed our daily clinical practice to an asleep MRI-guided and stereotactic CT-verified approach.

Keywords: Deep brain stimulation; MRI-guided; Parkinson’s disease; microelectrode recording; subthalamic nucleus.

Conflict of interest statement

RSV acts as an independent consultant for Boston Scientific. The other authors have nothing to disclose.

Figures

Fig. 1
Fig. 1
Visualization of the STN, MRI-guided targeting and immediate postoperative verification of final electrode position. Axial stereotactic 3D T2-weighted SPACE MRI at 3.0 T through the inferior portion of the STN. This sequence is used for both targeting the STN and localization of the Leksell Vantage frame. Blue and red bullets are indicating the patient-specific intended target at the left and right side respectively, with the corresponding lines indicating the planned trajectories. The orange metal artefacts indicate the position of the final electrodes of the same patient, verified by co-registering an immediate postoperative stereotactic CT to the 3D T2-weighted SPACE MRI.
Fig. 2
Fig. 2
Evaluation of MER signals and inter-observer variability of the MRI-defined STN along the planned trajectory. Visualization of a one-sided standard evaluation in a particular patient. Depth of the recordings ranges from 7 mm above target (T) to 3 mm below in steps of 0.5 mm starting from 5 mm above target. MER signals of the central track were visualized at each depth and were interpreted by a dedicated neurophysiologist. Characterization of the signals as being STN-specific was indicated in the ‘MER’ column. Two independent observers assessed whether the planned trajectory was located within the MRI-defined STN at every depth. Subsequently, a Jaccard’s Index of Similarity was calculated for MRI Observer 1 and Observer 2. The Jaccard’s Index of Similarity was defined as the number in both sets divided by the number in either set (intersection over union; see formula). The ‘Lead’ column indicates the depth of the contacts of the final lead with the active contact at 12 months follow-up marked in green.

References

    1. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schafer H, Botzel K, Daniels C, Deutschlander A, Dillmann U, Eisner W, Gruber D, Hamel W, Herzog J, Hilker R, Klebe S, Kloss M, Koy J, Krause M, Kupsch A, Lorenz D, Lorenzl S, Mehdorn HM, Moringlane JR, Oertel W, Pinsker MO, Reichmann H, Reuss A, Schneider GH, Schnitzler A, Steude U, Sturm V, Timmermann L, Tronnier V, Trottenberg T, Wojtecki L, Wolf E, Poewe W, Voges J, German Parkinson Study Group, Neurostimulation Section (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355, 896–908.
    1. Schuepbach WM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, Halbig TD, Hesekamp H, Navarro SM, Meier N, Falk D, Mehdorn M, Paschen S, Maarouf M, Barbe MT, Fink GR, Kupsch A, Gruber D, Schneider GH, Seigneuret E, Kistner A, Chaynes P, Ory-Magne F, Brefel Courbon C, Vesper J, Schnitzler A, Wojtecki L, Houeto JL, Bataille B, Maltete D, Damier P, Raoul S, Sixel-Doering F, Hellwig D, Gharabaghi A, Kruger R, Pinsker MO, Amtage F, Regis JM, Witjas T, Thobois S, Mertens P, Kloss M, Hartmann A, Oertel WH, Post B, Speelman H, Agid Y, Schade-Brittinger C, Deuschl G, EARLYSTIM Study Group (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368, 610–622.
    1. Abosch A, Timmermann L, Bartley S, Rietkerk HG, Whiting D, Connolly PJ, Lanctin D, Hariz MI (2013) An international survey of deep brain stimulation procedural steps. Stereotact Funct Neurosurg 91, 1–11.
    1. Benabid AL, Krack PP, Benazzouz A, Limousin P, Koudsie A, Pollak P (2000) Deep brain stimulation of the subthalamic nucleus for Parkinson’s disease: Methodologic aspects and clinical criteria. Neurology 55, S40–44.
    1. Ashkan K, Blomstedt P, Zrinzo L, Tisch S, Yousry T, Limousin-Dowsey P, Hariz MI (2007) Variability of the subthalamic nucleus: The case for direct MRI guided targeting. Br J Neurosurg 21, 197–200.
    1. Counelis GJ, Simuni T, Forman MS, Jaggi JL, Trojanowski JQ, Baltuch GH (2003) Bilateral subthalamic nucleus deep brain stimulation for advanced PD: Correlation of intraoperative MER and postoperative MRI with neuropathological findings. Mov Disord 18, 1062–1065.
    1. Hariz M, Blomstedt P, Limousin P (2004) The myth of microelectrode recording in ensuring a precise location of the DBS electrode within the sensorimotor part of the subthalamic nucleus. Mov Disord 19, 863–864.
    1. McClelland S, 3rd, Vonsattel JP, Garcia RE, Amaya MD, Winfield LM, Pullman SL, Yu Q, Fahn S, Ford B, Goodman RR (2007) Relationship of clinical efficacy to postmortem-determined anatomic subthalamic stimulation in Parkinson syndrome. Clin Neuropathol 26, 267–275.
    1. Gorgulho A, De Salles AA, Frighetto L, Behnke E (2005) Incidence of hemorrhage associated with electrophysiological studies performed using macroelectrodes and microelectrodes in functional neurosurgery. J Neurosurg 102, 888–896.
    1. Zrinzo L, Foltynie T, Limousin P, Hariz MI (2012) Reducing hemorrhagic complications in functional neurosurgery: A large case series and systematic literature review. J Neurosurg 116, 84–94.
    1. McClelland S, 3rd (2011) A cost analysis of intraoperative microelectrode recording during subthalamic stimulation for Parkinson’s disease. Mov Disord 26, 1422–1427.
    1. Nakajima T, Zrinzo L, Foltynie T, Olmos IA, Taylor C, Hariz MI, Limousin P (2011) MRI-guided subthalamic nucleus deep brain stimulation without microelectrode recording: Can we dispense with surgery under local anaesthesia? Stereotact Funct Neurosurg 89, 318–325.
    1. Chen T, Mirzadeh Z, Chapple KM, Lambert M, Shill HA, Moguel-Cobos G, Troster AI, Dhall R, Ponce FA (2018) Clinical outcomes following awake and asleep deep brain stimulation for Parkinson disease. J Neurosurg 130, 109–120.
    1. Wodarg F, Herzog J, Reese R, Falk D, Pinsker MO, Steigerwald F, Jansen O, Deuschl G, Mehdorn HM, Volkmann J (2012) Stimulation site within the MRI-defined STN predicts postoperative motor outcome. Mov Disord 27, 874–879.
    1. Patel NK, Khan S, Gill SS (2008) Comparison of atlas- and magnetic-resonance-imaging-based stereotactic targeting of the subthalamic nucleus in the surgical treatment of Parkinson’s disease. Stereotact Funct Neurosurg 86, 153–161.
    1. Bejjani BP, Dormont D, Pidoux B, Yelnik J, Damier P, Arnulf I, Bonnet AM, Marsault C, Agid Y, Philippon J, Cornu P (2000) Bilateral subthalamic stimulation for Parkinson’s disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 92, 615–625.
    1. Holl EM, Petersen EA, Foltynie T, Martinez-Torres I, Limousin P, Hariz MI, Zrinzo L (2010) Improving targeting in image-guided frame-based deep brain stimulation. Neurosurgery 67, 437–447.
    1. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25, 2649–2653.
    1. Real R, Vargas JM (1996) The probabilistic basis of Jaccard’s Index of Similarity. Syst Biol 45, 380–385.
    1. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44, 223–270.
    1. Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ Jr., Rothlind J, Sagher O, Reda D, Moy CS, Pahwa R, Burchiel K, Hogarth P, Lai EC, Duda JE, Holloway K, Samii A, Horn S, Bronstein J, Stoner G, Heemskerk J, Huang GD, CSP 468 Study Group (2009) Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: A randomized controlled trial. JAMA 301, 63–73.
    1. Odekerken VJ, van Laar T, Staal MJ, Mosch A, Hoffmann CF, Nijssen PC, Beute GN, van Vugt JP, Lenders MW, Contarino MF, Mink MS, Bour LJ, van den Munckhof P, Schmand BA, de Haan RJ, Schuurman PR, de Bie RM (2013) Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): A randomised controlled trial. Lancet Neurol 12, 37–44.
    1. Bour LJ, Contarino MF, Foncke EM, de Bie RM, van den Munckhof P, Speelman JD, Schuurman PR (2010) Long-term experience with intraoperative microrecording during DBS neurosurgery in STN and GPi. Acta Neurochir (Wien) 152, 2069–2077.
    1. Temel Y, Wilbrink P, Duits A, Boon P, Tromp S, Ackermans L, van Kranen-Mastenbroek V, Weber W, Visser-Vandewalle V (2007) Single electrode and multiple electrode guided electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. Neurosurgery 61, 346–355; discussion; 355-347.
    1. Hamel W, Fietzek U, Morsnowski A, Schrader B, Herzog J, Weinert D, Pfister G, Muller D, Volkmann J, Deuschl G, Mehdorn HM (2003) Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: Evaluation of active electrode contacts. J Neurol Neurosurg Psychiatry 74, 1036–1046.
    1. Amirnovin R, Williams ZM, Cosgrove GR, Eskandar EN (2006) Experience with microelectrode guided subthalamic nucleus deep brain stimulation. Neurosurgery 58, ONS96–102; discussion ONS196-102.
    1. Rola R, Tutaj M, Koziara H, Koziorowski D, Brodacki B, Karliński M, Tykocki T, Krolicki B, Mandat T (2016) Optimizing final electrode placement Based on intraoperative neurophysiological evaluation during subthalamic deep brain stimulation for Parkinson’s disease. J Neurol Neurophysiol 7, 4.
    1. Frequin HL, Bot M, Dilai J, Scholten MN, Postma M, Bour LJ, Contarino MF, de Bie RMA, Schuurman PR, van den Munckhof P (2020) Relative contribution of magnetic resonance imaging, microelectrode recordings, and awake test stimulation in final lead placement during deep brain stimulation surgery of the subthalamic nucleus in Parkinson’s disease. Stereotact Funct Neurosurg 98, 118–128.
    1. Azmi H, Machado A, Deogaonkar M, Rezai A (2011) Intracranial air correlates with preoperative cerebral atrophy and stereotactic error during bilateral STN DBS surgery for Parkinson’s disease. Stereotact Funct Neurosurg 89, 246–252.
    1. Geevarghese R, O’Gorman Tuura R, Lumsden DE, Samuel M, Ashkan K (2016) Registration accuracy of CT/MRI fusion for localisation of deep brain stimulation electrode position: An imaging study and systematic review. Stereotact Funct Neurosurg 94, 159–163.
    1. Rolston JD, Englot DJ, Starr PA, Larson PS (2016) An unexpectedly high rate of revisions and removals in deep brain stimulation surgery: Analysis of multiple databases. Parkinsonism Relat Disord 33, 72–77.
    1. Okun MS, Tagliati M, Pourfar M, Fernandez HH, Rodriguez RL, Alterman RL, Foote KD (2005) Management of referred deep brain stimulation failures: A retrospective analysis from 2 movement disorders centers. Arch Neurol 62, 1250–1255.
    1. Maiti TK, Konar S, Bir S, Kalakoti P, Nanda A (2016) Intra-operative micro-electrode recording in functional neurosurgery: Past, present, future. J Clin Neurosci 32, 166–172.
    1. LaHue SC, Ostrem JL, Galifianakis NB, San Luciano M, Ziman N, Wang S, Racine CA, Starr PA, Larson PS, Katz M (2017) Parkinson’s disease patient preference and experience with various methods of DBS lead placement. Parkinsonism Relat Disord 41, 25–30.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren