Download PDF
J Neurol Surg A Cent Eur Neurosurg 2012; 73(06): 377-386
DOI: 10.1055/s-0032-1326957
Original Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Clinical Outcome of Subthalamic Stimulation in Parkinson's Disease is Improved by Intraoperative Multiple Trajectories Microelectrode Recording

Christiane Reck
1   Department of Neurology, University Hospital Cologne, Cologne, Germany
,
Mohammad Maarouf
2   Department of Stereotaxy and Functional Neurosurgery, University Hospital Cologne, Cologne, Germany
,
Lars Wojtecki
3   Department of Neurology, Heinrich-Heine-University, Düsseldorf, Germany
4   Institute of Clinical Neuroscience and Medical Psychology, Heinrich-Heine-University, Düsseldorf, Germany
,
Stefan Jun Groiss
3   Department of Neurology, Heinrich-Heine-University, Düsseldorf, Germany
4   Institute of Clinical Neuroscience and Medical Psychology, Heinrich-Heine-University, Düsseldorf, Germany
,
Esther Florin
1   Department of Neurology, University Hospital Cologne, Cologne, Germany
6   McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, Canada
,
Volker Sturm
2   Department of Stereotaxy and Functional Neurosurgery, University Hospital Cologne, Cologne, Germany
,
Gereon R. Fink
1   Department of Neurology, University Hospital Cologne, Cologne, Germany
5   Cognitive Neurology Section, Institute of Neuroscience and Medicine, Research Center Jülich, Jülich, Germany
,
Alfons Schnitzler
3   Department of Neurology, Heinrich-Heine-University, Düsseldorf, Germany
4   Institute of Clinical Neuroscience and Medical Psychology, Heinrich-Heine-University, Düsseldorf, Germany
,
Lars Timmermann
1   Department of Neurology, University Hospital Cologne, Cologne, Germany
› Author Affiliations
Further Information

Publication History

06 June 2011

02 December 2011

Publication Date:
05 October 2012 (online)

Also available at
    Permissions and Reprints

Abstract

Background and Study Aims The use of multiple trajectories microelectrode recording (MER) during implantation of deep brain stimulation (DBS) electrodes into the subthalamic nucleus (STN) in patients with Parkinson's disease (PD) is discussed controversially because of possible risks and unclear benefits. The aim of the study is to investigate whether MER combined with intraoperative evaluation of stimulation effects improve clinical outcome in PD patients undergoing STN DBS surgery.

Material and Methods Prior to final DBS electrode implantation, we performed multiple trajectories MER and intraoperative test stimulations after magnetic resonance imaging (MRI)-guided planning in 32 PD patients. In further 10 patients no MER (only intraoperative test stimulation) was used.

Results We found a significantly better clinical outcome (Unified Parkinson's Disease Rating Scale [UPDRS] III) in patients undergoing MER compared with non-MER patients. In MER patients, DBS electrode placement was performed using the central trajectory in 73%. Another than the central trajectory was taken in 27% of the patients. No difference in clinical outcome between DBS electrodes implanted on the central or a decentral trajectory was observed.

Conclusions DBS surgery based on intraoperative multiple trajectories MER and test stimulation improves clinical outcome if compared with intraoperative test stimulation alone. The data suggest that DBS surgery solely based on MRI and intraoperative test stimulation without MER may lead to nonoptimal placement of DBS electrodes and consequently poorer clinical outcome.

Keywords

deep brain stimulation - microelectrode recording - Parkinson's disease - subthalamic nucleus

Supplementary Material

 

  • References

  • 1 Lang AE, Lozano AM. Parkinson's disease. First of two parts. N Engl J Med 1998; 339 (15) 1044-1053
    CrossrefPubMedGoogle Scholar
  • 2 Deuschl G, Schade-Brittinger C, Krack P , et al; German Parkinson Study Group, Neurostimulation Section. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006; 355 (9) 896-908
    CrossrefPubMedGoogle Scholar
  • 3 Timmermann L, Florin E, Reck C. Pathological cerebral oscillatory activity in Parkinson's disease: a critical review on methods, data and hypotheses. Expert Rev Med Devices 2007; 4 (5) 651-661
    CrossrefPubMedGoogle Scholar
  • 4 Herzog J, Fietzek U, Hamel W , et al. Most effective stimulation site in subthalamic deep brain stimulation for Parkinson's disease. Mov Disord 2004; 19 (9) 1050-1054
    CrossrefPubMedGoogle Scholar
  • 5 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
    CrossrefPubMedGoogle Scholar
  • 6 Sturman MM, Vaillancourt DE, Metman LV, Bakay RA, Corcos DM. Effects of subthalamic nucleus stimulation and medication on resting and postural tremor in Parkinson's disease. Brain 2004; 127 (Pt 9) 2131-2143
    CrossrefPubMedGoogle Scholar
  • 7 Timmermann L, Braun M, Groiss S , et al. Differential effects of levodopa and subthalamic nucleus deep brain stimulation on bradykinesia in Parkinson's disease. Mov Disord 2008; 23 (2) 218-227
    CrossrefPubMedGoogle Scholar
  • 8 Timmermann L, Wojtecki L, Gross J , et al. Ten-Hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson's disease. Mov Disord 2004; 19 (11) 1328-1333
    CrossrefPubMedGoogle Scholar
  • 9 Voges J, Volkmann J, Allert N , et al. Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg 2002; 96 (2) 269-279
    CrossrefPubMedGoogle Scholar
  • 10 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
    CrossrefPubMedGoogle Scholar
  • 11 Schaltenbrand G, Wahren W. Atlas for Stereotaxy of the Human Brain. Stuttgart: Thieme; 1977
    Google Scholar
  • 12 Benazzouz A, Breit S, Koudsie A , et al. Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease. Mov Disord 2002; 17 (Suppl. 03) 145-149
    CrossrefPubMedGoogle Scholar
  • 13 Hutchison WD, Allan RJ, Opitz H , et al. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann Neurol 1998; 44 (4) 622-628
    CrossrefPubMedGoogle Scholar
  • 14 Pollak P, Krack P, Fraix V , et al. Intraoperative micro- and macrostimulation of the subthalamic nucleus in Parkinson's disease. Mov Disord 2002; 17 (Suppl. 03) S155-S161
    CrossrefPubMedGoogle Scholar
  • 15 Sterio D, Zonenshayn M, Mogilner AY , et al. Neurophysiological refinement of subthalamic nucleus targeting. Neurosurgery 2002; 50 (1) 58-67 , discussion 67–69
    PubMedGoogle Scholar
  • 16 Benabid AL, Krack PP, Benazzouz A, Limousin P, Koudsie A, Pollak P. Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology 2000; 55 (1) (2) (Suppl. 06) S40-S44
    PubMedGoogle Scholar
  • 17 Ford B, Winfield L, Pullman SL , et al. Subthalamic nucleus stimulation in advanced Parkinson's disease: blinded assessments at one year follow up. J Neurol Neurosurg Psychiatry 2004; 75 (9) 1255-1259
    CrossrefPubMedGoogle Scholar
  • 18 Senatus PB, Teeple D, McClelland III S , et al. A technique for minimally altering anatomically based subthalamic electrode targeting by microelectrode recording. Neurosurg Focus 2006; 20 (5) E8
    PubMedGoogle Scholar
  • 19 Fahn S, Elton R. Unified Parkinson's Disease Rating Scale. Florham Park, NJ: Macmillan Health Care Information; 1987: 153-163 , 293–304
    Google Scholar
  • 20 Wenzelburger R, Zhang BR, Poepping M , et al. Dyskinesias and grip control in Parkinson's disease are normalized by chronic stimulation of the subthalamic nucleus. Ann Neurol 2002; 52 (2) 240-243
    CrossrefPubMedGoogle Scholar
  • 21 Hilker R, Benecke R, Deuschl G , et al; German Deep Brain Stimulation Association. [Deep brain stimulation for Parkinson's disease. Consensus recommendations of the German Deep Brain Stimulation Association]. Nervenarzt 2009; 80 (6) 646-655
    CrossrefPubMedGoogle Scholar
  • 22 Ende G, Treuer H, Boesecke R. Optimization and evaluation of landmark-based image correlation. Phys Med Biol 1992; 37 (1) 261-271
    CrossrefPubMedGoogle Scholar
  • 23 Rodriguez MC, Guridi OJ, Alvarez L , et al. The subthalamic nucleus and tremor in Parkinson's disease. Mov Disord 1998; 13 (Suppl. 03) 111-118
    PubMedGoogle Scholar
  • 24 Alkhani A, Lozano AM. Pallidotomy for Parkinson disease: a review of contemporary literature. J Neurosurg 2001; 94 (1) 43-49
    CrossrefPubMedGoogle Scholar
  • 25 de Bie RM, de Haan RJ, Schuurman PR, Esselink RA, Bosch DA, Speelman JD. Morbidity and mortality following pallidotomy in Parkinson's disease: a systematic review. Neurology 2002; 58 (7) 1008-1012
    CrossrefPubMedGoogle Scholar
  • 26 Palur RS, Berk C, Schulzer M, Honey CR. A metaanalysis comparing the results of pallidotomy performed using microelectrode recording or macroelectrode stimulation. J Neurosurg 2002; 96 (6) 1058-1062
    CrossrefPubMedGoogle Scholar
  • 27 Gorgulho A, De Salles AA, Frighetto L, Behnke E. Incidence of hemorrhage associated with electrophysiological studies performed using macroelectrodes and microelectrodes in functional neurosurgery. J Neurosurg 2005; 102 (5) 888-896
    CrossrefPubMedGoogle Scholar
  • 28 Sansur CA, Frysinger RC, Pouratian N , et al. Incidence of symptomatic hemorrhage after stereotactic electrode placement. J Neurosurg 2007; 107 (5) 998-1003
    CrossrefPubMedGoogle Scholar
  • 29 Binder DK, Rau G, Starr PA. Hemorrhagic complications of microelectrode-guided deep brain stimulation. Stereotact Funct Neurosurg 2003; 80 (1-4) 28-31
    CrossrefPubMedGoogle Scholar
  • 30 Halpern CH, Danish SF, Baltuch GH, Jaggi JL. Brain shift during deep brain stimulation surgery for Parkinson's disease. Stereotact Funct Neurosurg 2008; 86 (1) 37-43
    CrossrefPubMedGoogle Scholar
  • 31 Hunsche S, Sauner D, Maarouf M , et al. Intraoperative X-ray detection and MRI-based quantification of brain shift effects subsequent to implantation of the first electrode in bilateral implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 2009; 87 (5) 322-329
    CrossrefPubMedGoogle Scholar
  • 32 Khan MF, Mewes K, Gross RE, Skrinjar O. Assessment of brain shift related to deep brain stimulation surgery. Stereotact Funct Neurosurg 2008; 86 (1) 44-53
    CrossrefPubMedGoogle Scholar
  • 33 Miyagi Y, Shima F, Sasaki T. Brain shift: an error factor during implantation of deep brain stimulation electrodes. J Neurosurg 2007; 107 (5) 989-997
    CrossrefPubMedGoogle Scholar
  • 34 McClelland III S, Kim B, Winfield LM , et al. Microelectrode recording-determined subthalamic nucleus length not predictive of stimulation-induced side effects. Neurosurg Focus 2005; 19 (5) E13
    PubMedGoogle Scholar
  • 35 Chen SY, Lee CC, Lin SH , et al. Microelectrode recording can be a good adjunct in magnetic resonance image-directed subthalamic nucleus deep brain stimulation for parkinsonism. Surg Neurol 2006; 65 (3) 253-260 , discussion 260–261
    CrossrefPubMedGoogle Scholar
  • 36 Temel Y, Wilbrink P, Duits A , et al. Single electrode and multiple electrode guided electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. Neurosurgery 2007; 61 (5) (Suppl. 02) 346-355 , discussion 355–357
    CrossrefPubMedGoogle Scholar
  • 37 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 effects of stimulation. J Neurol Neurosurg Psychiatry 2002; 72 (1) 53-58
    CrossrefPubMedGoogle Scholar
  • 38 Amirnovin R, Williams ZM, Cosgrove GR, Eskandar EN. Experience with microelectrode guided subthalamic nucleus deep brain stimulation. Neurosurgery 2006; 58 (1, Suppl) ONS96-ONS102 , discussion ONS96–ONS102
    PubMedGoogle Scholar
  • 39 Maltête D, Navarro S, Welter ML , et al. Subthalamic stimulation in Parkinson disease: with or without anesthesia?. Arch Neurol 2004; 61 (3) 390-392
    CrossrefPubMedGoogle Scholar