Three-dimensional SPACE fluid-attenuated inversion recovery at 3 T to improve subthalamic nucleus lead placement for deep brain stimulation in Parkinson's disease: from preclinical to clinical studies

View More View Less
  • 1 Service de Neurochirurgie,
  • 2 Service de Neuroradiologie, and
  • 3 Service des Explorations Fonctionnelles, Assistance Publique des Hopitaux de Paris, Hôpital H. Mondor, DHU PePsy;
  • 4 Inserm U955 Team 14;
  • 5 Faculté de Médecine, Université Paris Est, Créteil;
  • 6 DSV/I2BM/MIRCen/Laboratory of Neurodegenerative Diseases, CNRS, Commissariat à l'Energie Atomique, Fontenay-aux-Roses; and
  • 7 DSV/I2BM/Neurospin/UNIACT, Commissariat à l'Energie Atomique, Saclay, France
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is a well-established therapy for motor symptoms in patients with pharmacoresistant Parkinson's disease (PD). However, the procedure, which requires multimodal perioperative exploration such as imaging, electrophysiology, or clinical examination during macrostimulation to secure lead positioning, remains challenging because the STN cannot be reliably visualized using the gold standard, T2-weighted imaging (T2WI) at 1.5 T. Thus, there is a need to improve imaging tools to better visualize the STN, optimize DBS lead implantation, and enlarge DBS diffusion.

METHODS

Gradient-echo sequences such as those used in T2WI suffer from higher distortions at higher magnetic fields than spin-echo sequences. First, a spin-echo 3D SPACE (sampling perfection with application-optimized contrasts using different flip angle evolutions) FLAIR sequence at 3 T was designed, validated histologically in 2 nonhuman primates, and applied to 10 patients with PD; their data were clinically compared in a double-blind manner with those of a control group of 10 other patients with PD in whom STN targeting was performed using T2WI.

RESULTS

Overlap between the nonhuman primate STNs segmented on 3D-histological and on 3D-SPACE-FLAIR volumes was high for the 3 most anterior quarters (mean [± SD] Dice scores 0.73 ± 0.11, 0.74 ± 0.06, and 0.60 ± 0.09). STN limits determined by the 3D-SPACE-FLAIR sequence were more consistent with electrophysiological edges than those determined by T2WI (0.9 vs 1.4 mm, respectively). The imaging contrast of the STN on the 3D-SPACE-FLAIR sequence was 4 times higher (p < 0.05). Improvement in the Unified Parkinson's Disease Rating Scale Part III score (off medication, on stimulation) 12 months after the operation was higher for patients who underwent 3D-SPACE-FLAIR–guided implantation than for those in whom T2WI was used (62.2% vs 43.6%, respectively; p < 0.05). The total electrical energy delivered decreased by 36.3% with the 3D-SPACE-FLAIR sequence (p < 0.05).

CONCLUSIONS

3D-SPACE-FLAIR sequences at 3 T improved STN lead placement under stereotactic conditions, improved the clinical outcome of patients with PD, and increased the benefit/risk ratio of STN-DBS surgery.

ABBREVIATIONSDBS = deep brain stimulation; eSTN = electrophysiologically identified subthalamic nucleus; H&Y = Hoehn and Yahr; LEDD = levodopa equivalent daily dose; M12 = month 12 after implantation; NHP = nonhuman primate; PD = Parkinson's disease; SPACE = sampling perfection with application-optimized contrasts using different flip angle evolutions; STN = subthalamic nucleus; TEED = total electrical energy delivered; T1WI = T1-weighted imaging; T2WI = T2-weighted imaging; UPDRS = Unified Parkinson's Disease Rating Scale.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

INCLUDE WHEN CITING Published online January 8, 2016; DOI: 10.3171/2015.7.JNS15379.

Drs. Senova and Hosomi contributed equally to this work.

Correspondence Stéphane Palfi, Service de Neurochirurgie, CHU Henri Mondor, 51 Avenue du Marechal de Lattre de Tassigny, Créteil 94110, France. email: stephane.palfi@hmn.aphp.fr.
  • 1

    Andrade-Souza YM, , Schwalb JM, , Hamani C, , Eltahawy H, , Hoque T, & Saint-Cyr J, : Comparison of three methods of targeting the subthalamic nucleus for chronic stimulation in Parkinson's disease. Neurosurgery 56:2 Suppl 360368, 2005

    • Search Google Scholar
    • Export Citation
  • 2

    Benabid AL, , Chabardes S, , Mitrofanis J, & Pollak P: Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol 8:6781, 2009

    • Search Google Scholar
    • Export Citation
  • 3

    Dammann P, , Kraff O, , Wrede KH, , Özkan N, , Orzada S, & Mueller OM, : Evaluation of hardware-related geometrical distortion in structural MRI at 7 Tesla for image-guided applications in neurosurgery. Acad Radiol 18:910916, 2011

    • Search Google Scholar
    • Export Citation
  • 4

    Daniluk S, , Davies KG, , Ellias SA, , Novak P, & Nazzaro JM: Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson's disease using magnetic resonance imaging. Acta Neurochir (Wien) 152:201210, 2010

    • Search Google Scholar
    • Export Citation
  • 5

    Dauguet J, , Delzescaux T, , Condé F, , Mangin JF, , Ayache N, & Hantraye P, : Three-dimensional reconstruction of stained histological slices and 3D non-linear registration with in-vivo MRI for whole baboon brain. J Neurosci Methods 164:191204, 2007

    • Search Google Scholar
    • Export Citation
  • 6

    Dauguet J, , Peled S, , Berezovskii V, , Delzescaux T, , Warfield SK, & Born R, : Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37:530538, 2007

    • Search Google Scholar
    • Export Citation
  • 7

    Deuschl G, , Schade-Brittinger C, , Krack P, , Volkmann J, , Schäfer H, & Bötzel K, : A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 355:896908, 2006

    • Search Google Scholar
    • Export Citation
  • 8

    Dice LR: Measures of the amount of ecologic association between species. Ecology 26:297302, 1945

  • 9

    Dohan A, , Gavini JP, , Placé V, , Sebbag D, , Vignaud A, & Herbin C, : T2-weighted MR imaging of the liver: qualitative and quantitative comparison of SPACE MR imaging with turbo spinecho MR imaging. Eur J Radiol 82:e655e661, 2013

    • Search Google Scholar
    • Export Citation
  • 10

    Dormont D, , Ricciardi KG, , Tandé D, , Parain K, , Menuel C, & Galanaud D, : Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am J Neuroradiol 25:15161523, 2004

    • Search Google Scholar
    • Export Citation
  • 11

    Elolf E, , Bockermann V, , Gringel T, , Knauth M, , Dechent P, & Helms G: Improved visibility of the subthalamic nucleus on high-resolution stereotactic MR imaging by added susceptibility (T2*) contrast using multiple gradient echoes. AJNR Am J Neuroradiol 28:10931094, 2007

    • Search Google Scholar
    • Export Citation
  • 12

    Fleiss JL, , Levin B, & Paik MC: Statistical Methods for Rates and Proportions ed 3 Hoboken, NJ, Wiley, 2003

  • 13

    Follett KA, , Weaver FM, , Stern M, , Hur K, , Harris CL, & Luo P, : Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N Engl J Med 362:20772091, 2010

    • Search Google Scholar
    • Export Citation
  • 14

    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 82:358363, 2011

    • Search Google Scholar
    • Export Citation
  • 15

    Frangi AF, , Rueckert D, , Schnabel JA, & Niessen WJ: Automatic construction of multiple-object three-dimensional statistical shape models: application to cardiac modeling. IEEE Trans Med Imaging 21:11511166, 2002

    • Search Google Scholar
    • Export Citation
  • 16

    Hoehn MM, & Yahr MD: Parkinsonism: onset, progression, and mortality. Neurology 17:427442, 1967

  • 17

    Kim DY, , Lee JH, , Goh MJ, , Sung YS, , Choi YJ, & Yoon RG, : Clinical significance of an increased cochlear 3D fluid-attenuated inversion recovery signal intensity on an MR imaging examination in patients with acoustic neuroma. AJNR Am J Neuroradiol 35:18251829, 2014

    • Search Google Scholar
    • Export Citation
  • 18

    Kleiner-Fisman G, , Herzog J, , Fisman DN, , Tamma F, , Lyons KE, & Pahwa R, : Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord 21:Suppl 14 S290S304, 2006

    • Search Google Scholar
    • Export Citation
  • 19

    Koss AM, , Alterman RL, , Tagliati M, & Shils JL: Calculating total electrical energy delivered by deep brain stimulation systems. Ann Neurol 58:168169, 2005

    • Search Google Scholar
    • Export Citation
  • 20

    Mallet L, , Polosan M, , Jaafari N, , Baup N, , Welter ML, & Fontaine D, : Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359:21212134, 2008

    • Search Google Scholar
    • Export Citation
  • 21

    Nakajima T, , Zrinzo L, , Foltynie T, , Olmos IA, , Taylor C, & Hariz MI, : MRI-guided subthalamic nucleus deep brain stimulation without microelectrode recording: can we dispense with surgery under local anaesthesia?. Stereotact Funct Neurosurg 89:318325, 2011

    • Search Google Scholar
    • Export Citation
  • 22

    Odekerken VJ, , van Laar T, , Staal MJ, , Mosch A, , Hoffmann CF, & Nijssen PC, : Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson's disease (NSTAPS study): a randomised controlled trial. Lancet Neurol 12:3744, 2013

    • Search Google Scholar
    • Export Citation
  • 23

    Okun MS, , Gallo BV, , Mandybur G, , Jagid J, , Foote KD, & Revilla FJ, : Subthalamic deep brain stimulation with a constant-current device in Parkinson's disease: an open-label randomised controlled trial. Lancet Neurol 11:140149, 2012

    • Search Google Scholar
    • Export Citation
  • 24

    Pui MH, & Fok EC: MR imaging of the brain: comparison of gradient-echo and spin-echo pulse sequences. AJR Am J Roentgenol 165:959962, 1995

    • Search Google Scholar
    • Export Citation
  • 25

    Richter EO, , Hoque T, , Halliday W, , Lozano AM, & Saint-Cyr JA: Determining the position and size of the subthalamic nucleus based on magnetic resonance imaging results in patients with advanced Parkinson disease. J Neurosurg 100:541546, 2004

    • Search Google Scholar
    • Export Citation
  • 26

    Satzer D, , Maurer EW, , Lanctin D, , Guan W, & Abosch A: Anatomic correlates of deep brain stimulation electrode impedance. J Neurol Neurosurg Psychiatry 86:398403, 2015

    • Search Google Scholar
    • Export Citation
  • 27

    Schuepbach WM, , Rau J, , Knudsen K, , Volkmann J, , Krack P, & Timmermann L, : Neurostimulation for Parkinson's disease with early motor complications. N Engl J Med 368:610622, 2013

    • Search Google Scholar
    • Export Citation
  • 28

    Sedrak M, , Gorgulho A, , Bari A, , Behnke E, , Frew A, & Gevorkyan I, : Diffusion tensor imaging (DTI) and colored fractional anisotropy (FA) mapping of the subthalamic nucleus (STN) and the globus pallidus interna (GPi). Acta Neurochir (Wien) 152:20792084, 2010

    • Search Google Scholar
    • Export Citation
  • 29

    Shin M, , Lefaucheur JP, , Penholate MF, , Brugières P, , Gurruchaga JM, & Nguyen JP: Subthalamic nucleus stimulation in Parkinson's disease: postoperative CT-MRI fusion images confirm accuracy of electrode placement using intraoperative multi-unit recording. Neurophysiol Clin 37:457466, 2007

    • Search Google Scholar
    • Export Citation
  • 30

    Shin M, , Penholate MF, , Lefaucheur JP, , Gurruchaga JM, , Brugieres P, & Nguyen JP: Assessing accuracy of the magnetic resonance imaging-computed tomography fusion images to evaluate the electrode positions in subthalamic nucleus after deep-brain stimulation. Neurosurgery 66:11931202, 2010

    • Search Google Scholar
    • Export Citation
  • 31

    Slavin KV, , Thulborn KR, , Wess C, & Nersesyan H: Direct visualization of the human subthalamic nucleus with 3T MR imaging. AJNR Am J Neuroradiol 27:8084, 2006

    • Search Google Scholar
    • Export Citation
  • 32

    Stebbins GGoetz CG: Factor structure of the Unified Parkinson's Disease rating scale: motor examination section. Mov Disord 13:633636, 1998

    • Search Google Scholar
    • Export Citation
  • 33

    Tani N, , Joly O, , Iwamuro H, , Uhrig L, , Wiggins CJ, & Poupon C, : Direct visualization of non-human primate subcortical nuclei with contrast-enhanced high field MRI. Neuroimage 58:6068, 2011

    • Search Google Scholar
    • Export Citation
  • 34

    Tomlinson CL, , Stowe R, , Patel S, , Rick C, , Gray R, & Clarke CE: Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Mov Disord 25:26492653, 2010

    • Search Google Scholar
    • Export Citation
  • 35

    Urbach H, , Mast H, , Egger K, & Mader I: Presurgical MR imaging in epilepsy. Clin Neuroradiol 25:Suppl 2 151155, 2015

  • 36

    Weaver F, , Follett K, , Hur K, , Ippolito D, & Stern M: Deep brain stimulation in Parkinson disease: a metaanalysis of patient outcomes. J Neurosurg 103:956967, 2005

    • Search Google Scholar
    • Export Citation
  • 37

    Welter ML, , Schüpbach M, , Czernecki V, , Karachi C, , Fernandez-Vidal S, & Golmard JL, : Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology 82:13521361, 2014

    • Search Google Scholar
    • Export Citation
  • 38

    Wichmann T, , Bergman H, & DeLong MR: The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72:521530, 1994

    • Search Google Scholar
    • Export Citation
  • 39

    Williams A, , Gill S, , Varma T, , Jenkinson C, , Quinn N, & Mitchell R, : Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson's disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol 9:581591, 2010

    • Search Google Scholar
    • Export Citation
  • 40

    Zonenshayn M, , Rezai AR, , Mogilner AY, , Beric A, , Sterio D, & Kelly PJ: Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 47:282294, 2000

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 683 251 11
PDF Downloads 664 346 27
EPUB Downloads 0 0 0