Multitarget, dual-electrode deep brain stimulation of the thalamus and subthalamic area for treatment of Holmes' tremor

Clinical article

Kazutaka KobayashiDivision of Neurosurgery and

Search for other papers by Kazutaka Kobayashi in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Yoichi KatayamaDivision of Neurosurgery and

Search for other papers by Yoichi Katayama in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Hideki OshimaDivision of Neurosurgery and

Search for other papers by Hideki Oshima in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Mitsuru WatanabeDivision of Neurosurgery and

Search for other papers by Mitsuru Watanabe in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Koichiro SumiDivision of Neurosurgery and

Search for other papers by Koichiro Sumi in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Toshiki ObuchiDivision of Neurosurgery and

Search for other papers by Toshiki Obuchi in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Chikashi FukayaDivision of Applied System Neuroscience, Department of Neurological Surgery, Nihon University School of Medicine, Tokyo, Japan

Search for other papers by Chikashi Fukaya in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
, and
Takamitsu YamamotoDivision of Applied System Neuroscience, Department of Neurological Surgery, Nihon University School of Medicine, Tokyo, Japan

Search for other papers by Takamitsu Yamamoto in
Current site
Google Scholar
PubMed
Close
 M.D., Ph.D.
View More View Less
Restricted access

Purchase Now

USD  $45.00

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

USD  $525.00

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

USD  $624.00
USD  $45.00
USD  $525.00
USD  $624.00
Print or Print + Online Sign in

Object

Holmes' tremor (HT) is generally considered to be a symptomatic tremor associated with lesions of the cerebellum, midbrain, or thalamus. Deep brain stimulation (DBS) therapy for essential tremor and parkinsonian tremor has proved quite successful. In contrast, surgical treatment outcomes for HT have often been disappointing. The use of 2 ipsilateral DBS electrodes implanted in parallel within the thalamus for severe essential tremor has been reported. Since dual-lead stimulation within a single target can cover a wider area than single-lead stimulation, it produces greater effects. On the other hand, DBS of the subthalamic area (SA) was recently reported to be effective for refractory tremor.

Methods

The authors implanted 2 DBS electrodes (one at the nucleus ventralis oralis/nucleus ventralis intermedius and the other at the SA) in 4 patients with HT. For more than 2 years after implantation, each patient's tremor was evaluated using a tremor rating scale under the following 4 conditions of stimulation: “on” for both thalamus and SA DBS; “off” for both thalamus and SA DBS; “on” for thalamus and “off” for SA DBS; and “on” for SA and “off” for thalamus DBS.

Results

The tremor in all patients was improved for more than 2 years (mean 25.8 ± 3.5 months). Stimulation with 2 electrodes exerted greater effect on the tremor than did 1-electrode stimulation. Interestingly, in all patients progressive effects were observed, and in one patient treated with DBS for 1 year, tremor did not appear even while stimulation was temporarily switched off, suggesting irreversible improvement effects.

The presence of both resting and intentional/action tremor implies combined destruction of the pallidothalamic and cerebellothalamic pathways in HT. A larger stimulation area may thus be required for HT patients. Multitarget, dual-lead stimulation permits coverage of the wide area needed to suppress the tremor without adverse effects of stimulation. Some reorganization of the neural network may be involved in the development of HT because the tremor appears several months after the primary insult. The mechanism underlying the absence of tremor while stimulation was temporarily off remains unclear, but the DBS may have normalized the abnormal neural network.

Conclusions

The authors successfully treated patients with severe HT by using dual-electrode DBS over a long period. Such DBS may offer an effective and safe treatment modality for intractable HT.

Abbreviations used in this paper:

AC = anterior commissure; DBS = deep brain stimulation; GPi = globus pallidus internus; HT = Holmes' tremor; PC = posterior commissure; SA = subthalamic area; STN = subthalamic nucleus; TRS = tremor rating scale; VIM = ventralis intermedius; VO = ventralis oralis.
  • Collapse
  • Expand
  • 1

    Akkus DE, & Diramali AB: Postischemic delayed Holmes' tremor responding to low-dose cabergoline. Mov Disord 21:733734, 2006

  • 2

    Andy OJ, , Jurko MF, & Sias FR Jr: Subthalamotomy in treatment of parkinsonian tremor. J Neurosurg 20:860870, 1963

  • 3

    Barthó P, , Freund TF, & Acsády L: Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci 16:9991014, 2002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Benabid AL, , Pollak P, , Gao D, , Hoffmann D, , Limousin P, & Gay E, et al.: Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84:203214, 1996

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Bertrand C, , Hardy J, , Molina Negro P, & Martinez SN, Optimum physiological target for the arrest of tremor. Gillingham FJ, & Donaldson IML: Third Symposium on Parkinson's Disease Edinburgh, Livingstone, 1969. 251259

    • Search Google Scholar
    • Export Citation
  • 6

    Deuschl G, , Bain P, & Brin M: Consensus statement of the Movement Disorder Society on tremor. Mov Disord 13:Suppl 3 223, 1998

  • 7

    Deuschl G, , Raethjen J, , Lindemann M, & Krack P: The pathophysiology of tremor. Muscle Nerve 24:716735, 2001

  • 8

    Diederich NJ, , Verhagen Metman L, , Bakay RA, & Alesch F: Ventral intermediate thalamic stimulation in complex tremor syndromes. Stereotact Funct Neurosurg 86:167172, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Fahn S, , Tolosa E, & Marin C, Clinical rating scale for tremor. Jankovic JJ, & Tolosa E: Parkinson's Disease and Movement Disorders ed 3 Baltimore, Williams & Wilkins, 1988. 225234

    • Search Google Scholar
    • Export Citation
  • 10

    Foote KD, & Okun MS: Ventralis intermedius plus ventralis oralis anterior and posterior deep brain stimulation for posttraumatic Holmes tremor: two leads may be better than one: technical note. Neurosurgery 56:2 Suppl E445, 2005

    • Search Google Scholar
    • Export Citation
  • 11

    Foote KD, , Seignourel P, , Fernandez HH, , Romrell J, , Whidden E, & Jacobson C, et al.: Dual electrode thalamic deep brain stimulation for the treatment of posttraumatic and multiple sclerosis tremor. Neurosurgery 58:4 Suppl 2 ONS-280ONS-286, 2006

    • Search Google Scholar
    • Export Citation
  • 12

    Goto S, & Yamada K: Combination of thalamic Vim stimulation and GPi pallidotomy synergistically abolishes Holmes' tremor. J Neurol Neurosurg Psychiatry 75:12031204, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Hamel W, , Herzog J, , Kopper F, , Pinsker M, , Weinert D, & Müller D, et al.: Deep brain stimulation in the subthalamic area is more effective than nucleus ventralis intermedius stimulation for bilateral intention tremor. Acta Neurochir (Wien) 149:749758, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Heise CE, & Mitrofanis J: Evidence for a glutamatergic projection from the zona incerta to the basal ganglia of rats. J Comp Neurol 468:482495, 2004

  • 15

    Holmes G: On certain tremors in organic cerebral lesions. Brain 27:327375, 1904

  • 16

    Hua SE, , Garonzik IM, , Lee JI, & Lenz FA: Microelectrode studies of normal organization and plasticity of human somatosensory thalamus. J Clin Neurophysiol 17:559574, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Jiménez F, , Velasco F, , Velasco M, , Brito F, , Morel C, & Márquez I, et al.: Subthalamic prelemniscal radiation stimulation for the treatment of Parkinson's disease: electrophysiological characterization of the area. Arch Med Res 31:270281, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Kelly PJ, , Derome P, & Guiot G: Thalamic spatial variability and the surgical results of lesions placed with neurophysiologic control. Surg Neurol 9:307315, 1978

    • Search Google Scholar
    • Export Citation
  • 19

    Kitagawa M, , Murata J, , Kikuchi S, , Sawamura Y, , Saito H, & Sasaki H, et al.: Deep brain stimulation of subthalamic area for severe proximal tremor. Neurology 55:114116, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Kitagawa M, , Murata J, , Uesugi H, , Kikuchi S, , Saito H, & Tashiro K, et al.: Two-year follow-up of chronic stimulation of the posterior subthalamic white matter for tremor-dominant Parkinson's disease. Neurosurgery 56:281289, 2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Kobayashi K, , Katayama Y, , Sumi K, , Otaka T, , Obuchi T, & Kano T, et al.: Effects of electrode implantation angle on thalamic stimulation for treatment of tremor. Neuromodulation 13:3136, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Larochelle L, , Bedard P, , Boucher R, & Poirier LJ: The rubro-olivo-cerebello-rubral loop and postural tremor in the monkey. J Neurol Sci 11:5364, 1970

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Lim DA, , Khandhar SM, , Heath S, , Ostrem JL, , Ringel N, & Starr P: Multiple target deep brain stimulation for multiple sclerosis related and poststroke Holmes' tremor. Stereotact Funct Neurosurg 85:144149, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Liou LM, & Shih PY: Successful treatment of rubral tremor by high-dose trihexyphenidyl: a case report. Kaohsiung J Med Sci 22:149153, 2006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Merello M, , Tenca E, & Cerquetti D: Neuronal activity of the zona incerta in Parkinson's disease patients. Mov Disord 21:937943, 2006

  • 26

    Mundinger F: Stereotaxic interventions on the zona incerta area for treatment of extrapyramidal motor disturbances and their results. Confin Neurol 26:222230, 1965

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Murata J, , Kitagawa M, , Uesugi H, , Saito H, , Iwasaki Y, & Kikuchi S, et al.: Electrical stimulation of the posterior subthalamic area for the treatment of intractable proximal tremor. J Neurosurg 99:708715, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Nikkhah G, , Prokop T, , Hellwig B, , Lücking CH, & Ostertag CB: Deep brain stimulation of the nucleus ventralis intermedius for Holmes (rubral) tremor and associated dystonia caused by upper brainstem lesions. Report of two cases. J Neurosurg 100:10791083, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Péchadre JC, , Larochelle L, & Poirier LJ: Parkinsonian akinesia, rigidity and tremor in the monkey. Histopathological and neuropharmacological study. J Neurol Sci 28:147157, 1976

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Peker S, , Isik U, , Akgun Y, & Ozek M: Deep brain stimulation for Holmes' tremor related to a thalamic abscess. Childs Nerv Syst 24:10571062, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Pezzini A, , Zavarise P, , Palvarini L, , Viale P, , Oladeji O, & Padovani A: Holmes' tremor following midbrain Toxoplasma abscess: clinical features and treatment of a case. Parkinsonism Relat Disord 8:177180, 2002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Plaha P, , Khan S, & Gill SS: Bilateral stimulation of the caudal zona incerta nucleus for tremor control. J Neurol Neurosurg Psychiatry 79:504513, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Plaha P, , Patel NK, & Gill SS: Stimulation of the subthalamic region for essential tremor. J Neurosurg 101:4854, 2004

  • 34

    Remy P, , de Recondo A, , Defer G, , Loc'h C, , Amarenco P, & Planté-Bordeneuve V, et al.: Peduncular ‘rubral’ tremor and dopaminergic denervation: a PET study. Neurology 45:472477, 1995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35

    Roger M, & Cadusseau J: Afferents to the zona incerta in the rat: a combined retrograde and anterograde study. J Comp Neurol 241:480492, 1985

  • 36

    Romanelli P, , Brontë-Stewart H, , Courtney T, & Heit G: Possible necessity for deep brain stimulation of both the ventralis intermedius and subthalamic nuclei to resolve Holmes tremor. Case report. J Neurosurg 99:566571, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Shammah-Lagnado SJ, , Negrão N, & Ricardo JA: Afferent connections of the zona incerta: a horseradish peroxidase study in the rat. Neuroscience 15:109134, 1985

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Velasco F, , Jiménez F, , Pérez ML, , Carrillo-Ruiz JD, , Velasco AL, & Ceballos J, et al.: Electrical stimulation of the prelemniscal radiation in the treatment of Parkinson's disease: an old target revised with new techniques. Neurosurgery 49:293308, 2001

    • Search Google Scholar
    • Export Citation
  • 39

    Yamamoto T, , Katayama Y, , Fukaya C, , Oshima H, , Kasai M, & Kobayashi K: New method of deep brain stimulation therapy with two electrodes implanted in parallel and side by side. Technical note. J Neurosurg 95:10751078, 2001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40

    Yamamoto T, , Katayama Y, , Kano T, , Kobayashi K, , Oshima H, & Fukaya C: Deep brain stimulation for the treatment of parkinsonian, essential, and poststroke tremor: a suitable stimulation method and changes in effective stimulation intensity. J Neurosurg 101:201209, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1187 630 7
Full Text Views 476 31 0
PDF Downloads 446 40 1
EPUB Downloads 0 0 0