J Neurol Surg A Cent Eur Neurosurg 2015; 76(03): 181-189
DOI: 10.1055/s-0033-1354749
Original Article
Georg Thieme Verlag KG Stuttgart · New York

The Role of 3T Magnetic Resonance Imaging for Targeting the Human Subthalamic Nucleus in Deep Brain Stimulation for Parkinson Disease

Michele Longhi
1   Department of Neurosurgery, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Giuseppe Ricciardi
2   Department of Neuroradiology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Giorgio Tommasi
3   Department of Neurology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Antonio Nicolato
1   Department of Neurosurgery, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Roberto Foroni
1   Department of Neurosurgery, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Laura Bertolasi
3   Department of Neurology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Alberto Beltramello
2   Department of Neuroradiology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Giuseppe Moretto
3   Department of Neurology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Michele Tinazzi
3   Department of Neurology, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
Massimo Gerosa
1   Department of Neurosurgery, Azienda Ospedaliera Universitaria Integrata di Verona, Verona, Italy
› Author Affiliations
Further Information

Publication History

07 September 2012

07 June 2013

Publication Date:
12 March 2015 (online)


Background Chronic stimulation of the human subthalamic nucleus (STN) is gradually becoming accepted as a long-term therapeutic option for patients with advanced Parkinson disease (PD).

3Tesla (T) magnetic resonance imaging (MRI) improves contrast resolution in basal ganglia nuclei containing high levels of iron, because of magnetic susceptibility effects that increase significantly as the magnetic field gets higher. This phenomenon can be used for better visualization of the STN and may reduce the time necessary for detailed microrecording (MER) mapping, increasing surgery efficacy and lowering morbidity.

Objective The objective of this retrospective study is to analyze a population of 20 deep brain stimulation (DBS) electrode implanted patients with PD divided into two groups in which different targeting methods were used.

Methods Mean age was 56 years (range 37 to 69 years). Mean disease duration was 11.6 years. Mean follow-up was 12 months (range 6 to 36 months). Patients were divided into two groups: Group A contained 6 patients who underwent STN targeting using 1T stereotactic (T1w + T2w) MRI plus STN indirect atlas derived targeting. Group B consisted of 14 patients who underwent STN targeting using 3T nonstereotactic (T2w) MRI fused with 1T T1w stereotactic MRI and STN direct targeting. For statistical analysis, we compared (five different parameters in both (matched) groups: Unified Parkinson's disease rating scale (UPDRS) score reduction (medication off before surgery against stimulation on/medication off after surgery), postoperative drug reduction, duration of surgery, the “central preoperative track” chosen as final implantation track during surgery, and correspondence between the targeted STN and the intraoperative neurophysiologic data.

Results Mean UPDRS III score reduction (medication off/stimulation on versus preoperative medication off) was 69% in Group A and 74% in Group B (p = 0.015, log-rank test) respectively. Postoperatively, antiparkinsonian treatment was reduced by 66% in Group A and 75% in Group B (p = 0.006, log-rank test). The preoperative “central” track (which corresponds to ideal STN targeting) proved to be the most clinically effective in 2/12 leads for Group A versus 21/28 for Group B (p < 0.001).

Neurophysiologic data confirmed these results; the hypothetical target was confirmed by MER data in 76% of tracks in Group A, and in 75% of tracks in Group B (p < 0.001, univariate and multivariate analysis).

Conclusion 3T MRI appears to be a useful tool in STN-DBS preoperative targeting. Neurophysiologic testing remains fundamental to determine lead deepness (and prevent clinical side effects.

  • References

  • 1 Benabid AL, Pollak P, Gross C , et al. Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. Stereotact Funct Neurosurg 1994; 62 (1-4) 76-84
  • 2 Limousin P, Krack P, Pollak P , et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 1998; 339 (16) 1105-1111
  • 3 Obeso JA, Rodriguez-Oroz MC, Rodriguez M , et al. Pathophysiologic basis of surgery for Parkinson's disease. Neurology 2000; 55 (12) (Suppl. 06) S7-S12
  • 4 Rodriguez-Oroz MC, Obeso JA, Lang AE , et al. Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 2005; 128 (Pt 10) 2240-2249
  • 5 Zonenshayn M, Rezai AR, Mogilner AY, Beric A, Sterio D, Kelly PJ. Comparison of anatomic and neurophysiological methods for subthalamic nucleus targeting. Neurosurgery 2000; 47 (2) 282-292, discussion 292–294
  • 6 Morel A, Magnin M, Jeanmonod D. Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 1997; 387 (4) 588-630
  • 7 Reck C, Maarouf M, Wojtecki L , et al. Clinical outcome of subthalamic stimulation in Parkinsońs disease is improved by intraoperative multiple trajectories microelectrode recording. J Neurol Surg A 2012; 73: 377-386
  • 8 Dormont D, Ricciardi KG, Tandé D , et al. Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. AJNR Am J Neuroradiol 2004; 25 (9) 1516-1523
  • 9 Sterio D, Zonenshayn M, Mogilner AY , et al. Neurophysiological refinement of subthalamic nucleus targeting. Neurosurgery 2002; 50 (1) 58-67, discussion 67–69
  • 10 Vesper J, Klostermann F, Stockhammer F, Funk T, Brock M. Results of chronic subthalamic nucleus stimulation for Parkinson's disease: a 1-year follow-up study. Surg Neurol 2002; 57 (5) 306-311, discussion 311–313
  • 11 Volkmann J, Sturm V, Weiss P , et al. Bilateral high-frequency stimulation of the internal globus pallidus in advanced Parkinson's disease. Ann Neurol 1998; 44 (6) 953-961
  • 12 Slavin KV, Thulborn KR, Wess C, Nersesyan H. Direct visualization of the human subthalamic nucleus with 3T MR imaging. AJNR Am J Neuroradiol 2006; 27 (1) 80-84
  • 13 Zhu XL, Hamel W, Schrader B , et al. Magnetic resonance imaging-based morphometry and landmark correlation of basal ganglia nuclei. Acta Neurochir (Wien) 2002; 144 (10) 959-969, discussion 968–969
  • 14 Bejjani BP, Dormont D, Pidoux B , et al. Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 2000; 92 (4) 615-625
  • 15 Schaltenbrand G, Wahren W. Atlas for Stereotaxy of the Human Brain. Stuttgart, Georg Thieme Verlag, 1977.
  • 16 Volz S, Hattingen E, Preibisch C, Gasser T, Deichmann R. Reduction of susceptibility-induced signal losses in multi-gradient-echo images: application to improved visualization of the subthalamic nucleus. Neuroimage 2009; 45 (4) 1135-1143
  • 17 Hamani C, Richter EO, Andrade-Souza Y, Hutchison W, Saint-Cyr JA, Lozano AM. Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg Neurol 2005; 63 (3) 249-253 , discussion 253
  • 18 Terao T, Okiyama R, Takahashi H , et al. [Comparison and examination of stereotactic surgical complications in movement disorders]. No Shinkei Geka 2003; 31 (6) 629-636
  • 19 Terao T, Takahashi H, Yokochi F, Taniguchi M, Okiyama R, Hamada I. Hemorrhagic complication of stereotactic surgery in patients with movement disorders. J Neurosurg 2003; 98 (6) 1241-1246
  • 20 Toda H, Sawamoto N, Hanakawa T , et al. A novel composite targeting method using high-field magnetic resonance imaging for subthalamic nucleus deep brain stimulation. J Neurosurg 2009; 111 (4) 737-745
  • 21 Benabid AL, Koudsie A, Benazzouz A, Le Bas JF, Pollak P. Imaging of subthalamic nucleus and ventralis intermedius of the thalamus. Mov Disord 2002; 17 (Suppl. 03) S123-S129
  • 22 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 (2) 370-387
  • 23 Gringel T, Schulz-Schaeffer W, Elolf E, Frölich A, Dechent P, Helms G. Optimized high-resolution mapping of magnetization transfer (MT) at 3 Tesla for direct visualization of substructures of the human thalamus in clinically feasible measurement time. J Magn Reson Imaging 2009; 29 (6) 1285-1292
  • 24 Vertinsky AT, Coenen VA, Lang DJ , et al. Localization of the subthalamic nucleus: optimization with susceptibility-weighted phase MR imaging. AJNR Am J Neuroradiol 2009; 30 (9) 1717-1724
  • 25 Duchin Y, Abosch A, Yacoub E, Sapiro G, Harel N. Feasibility of using ultra-high field (7 T) MRI for clinical surgical targeting. PLoS ONE 2012; 7 (5) e37328
  • 26 Abosch A, Yacoub E, Ugurbil K, Harel N. An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 2010; 67 (6) 1745-1756, discussion 1756
  • 27 Cho ZH, Oh SH, Kim JM , et al. Direct visualization of Parkinson's disease by in vivo human brain imaging using 7.0T magnetic resonance imaging. Mov Disord 2011; 26 (4) 713-718
  • 28 Brunenberg EJ, Platel B, Hofman PA, Ter Haar Romeny BM, Visser-Vandewalle V. Magnetic resonance imaging techniques for visualization of the subthalamic nucleus. J Neurosurg 2011; 115 (5) 971-984
  • 29 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 2007; 28 (6) 1093-1094
  • 30 Kerl HU, Gerigk L, Pechlivanis I, Al-Zghloul M, Groden C, Nölte I. The subthalamic nucleus at 3.0 Tesla: choice of optimal sequence and orientation for deep brain stimulation using a standard installation protocol: clinical article. J Neurosurg 2012; 117 (6) 1155-1165
  • 31 Mack A, Wolff R, Scheib S , et al. Analyzing 3-tesla magnetic resonance imaging units for implementation in radiosurgery. J Neurosurg 2005; 102 (Suppl): 158-164
  • 32 Watanabe Y, Lee CK, Gerbi BJ. Geometrical accuracy of a 3-tesla magnetic resonance imaging unit in Gamma Knife surgery. J Neurosurg 2006; 105 (Suppl): 190-193
  • 33 Liu X, Rowe J, Nandi D , et al. Localisation of the subthalamic nucleus using Radionics Image Fusion and Stereoplan combined with field potential recording. A technical note. Stereotact Funct Neurosurg 2001; 76 (2) 63-73
  • 34 Beric A, Kelly PJ, Rezai A , et al. Complications of deep brain stimulation surgery. Stereotact Funct Neurosurg 2001; 77 (1-4) 73-78
  • 35 Østergaard K, Sunde N, Dupont E. Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson's disease and motor fluctuations. Mov Disord 2002; 17 (4) 693-700
  • 36 Takeshita S, Kurisu K, Trop L, Arita K, Akimitsu T, Verhoeff NP. Effect of subthalamic stimulation on mood state in Parkinson's disease: evaluation of previous facts and problems. Neurosurg Rev 2005; 28 (3) 179-186 , discussion 187