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Keywords:

  • deep brain stimulation;
  • freezing of gait;
  • Parkinson's disease;
  • pirouette test

Freezing of gait (FOG) is one of the most challenging motor symptoms of Parkinson's disease (PD) because it limits mobility and causes falls.[1, 2] It is characterized by brief episodes of inability to move forward, despite the intention to walk, which typically occur on initiating gait, when passing obstacles, or on turning.[2] Normally, FOG is overcome after a couple of seconds, sometimes with the help of cueing maneuvers, but episodes can exceed 30 seconds. Medication, DBS, and rehabilitation techniques are helpful in controlling FOG in some patients, but FOG remains one of the most challenging motor symptoms to treat in advanced PD. A particular problem is de novo FOG after otherwise successful STN-DBS. When occurring early after surgery during the adjustment phase of neurostimulation, it cannot be ascribed to disease progression, but is rather provoked by the necessary reduction of dopaminergic medication in combination with inappropriate programming for the control of gait symptoms. Several recent studies have suggested special stimulation parameter settings to control FOG, which address impaired rhythmicity, symmetry, or bilateral coordination associated with FOG episodes, including lower-frequency stimulation with 60 to 80 Hz,[3] reduction of amplitude on the side with longer stride length,[4] and an interleaving stimulation of the distal contact in the SNr.5 Nevertheless, it remains enigmatic as to who responds or may be especially suited for which option.

FOG can be asymmetric, affecting mainly one foot, which then triggers a generalized freezing episode. Assessing gait asymmetry can be challenging for the clinician, because it may not be obvious during normal walking or standard challenge tests. We found forced clockwise or counterclockwise turning most useful in determining the more affected leg, which we termed the “pirouette test.” In the French ballet glossary, “pirouette” refers to “spinning around.” In practice, the patient is asked to perform a full 360-degree circle on the spot by moving one leg around a standing leg. The outer leg walking the circle is more prone to freezing and indicates the dominant symptomatic side, when the pirouette is preformed in both directions (see Video 1; Fig. 1). The pirouette test may be repeatedly performed during DBS parameter adjustments until symmetric clockwise and counterclockwise turning is achieved.

image

Figure 1. A pirouette performed by a professional ballerina with Relevé and la deuxième position (left); the pirouette test of a PD patient to indicate the dominate side of freezing (right).

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Here, we illustrate the usefulness of this approach in a 60-year-old man suffering from PD for the past 6 years. He was considered for STN-DBS at our institution because of severe motor fluctuations, including end-of-dose akinesia, painful off-period dystonia and peak-dose dyskinesia. In the preoperative levodopa challenge test, the patient scored 56 points on the UPDRS-III in the practically defined “off” and 9 points after a suprathreshold dosage of l-dopa. Interestingly, FOG was observed preoperatively only in a minimal degree in the medication (MED) OFF condition (score of 1 point in item III.11).

Because of the excellent l-dopa response and a lack of contraindications, the patient was implanted bilaterally in the STN during June 2013. He opted for a novel rechargeable DBS system (Vercise; Boston Scientific, Valencia, CA). After relief of the microlesioning effect, the initial stimulation settings (right STN: case +, contact 11-, 2.4 mA, 60 μs, 130 Hz; left STN: case +, contact 2- and 3- (50% each), 1.6 mA, 60 μs, 130 Hz) was very satisfactory, resulting in an UPDRS-III score of 12 points in the MED OFF/stimulation (STIM) ON condition. Therefore, an almost complete withdrawal of dopaminergic drugs was possible.

A few weeks later, the patient started to complain about gait freezing, particularly when crossing confined spaces, impairing his professional and social activities and causing two falls. On clinical examination, the patient exhibited mild and brief freezing and festinations during gait initiation, which could not be clearly assigned to one side (total UPDRS III: 20 points; item gait: 5 points). By performing the pirouette test, freezing became obvious for the left leg only (see Video 1). Therefore, we tried to optimize efficacy of right STN stimulation by increasing amplitude (>3.5 mA with 130 Hz) and shifting current to the adjacent contacts (proximal and distal current steering). This could not achieve satisfactory control of FOG, despite an excellent improvement of bradykinesia and rigidity in all extremities. Reducing stimulation frequency to 80 Hz in both hemispheres worsened symptom control on the right body half, but improved freezing of the left leg. Therefore, we finally programmed different frequencies for each lead (right STN: contact 11-, 4.0 mA, 30 μs, 74 Hz; left STN: contact 2- and 3- (50% each), 1.6 mA, 60 μs, 130 Hz), which led to the complete disappearance of FOG (see Video 2; Fig. 2) and good overall mobility.

image

Figure 2. Three-dimensional lead location and estimated volume of tissue activation as visualized by the Guide Software (Boston Scientific, Valencia, CA). The lead and anatomical structures are depicted from an anterior frontal perspective; right STN (coordinates of the active contact: x: −12.89; y: 0.64; z: −1.52 mm) (left) and left STN (coordinates of the active contact: x: 14.77; y: 2.377; z: −1.884 mm) (right), thalamus in yellow, STN in green, and red nucleus in red.

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This case illustrates the need for personalized adaptation of neurostimulation parameters, taking into account the often asymmetric expression of parkinsonian symptoms and the differential response of particular symptoms to the temporal parameters of the stimulation. This asymmetry may also apply to axial features of PD, and simple clinical assessments, such as the pirouette test for FOG, may help to reveal and treat asymmetry in daily practice.

Author Roles

  1. Top of page
  2. Author Roles
  3. Disclosures
  4. References
  5. Supporting Information

(1) Research Project: A. Conception, B. Organization, C. Execution; (2) Manuscript: A. Writing of the First Draft, B. Review and Critique.

M.M.R.: 1A, 1B, 1C, 2A

A.D.S.: 1B, 1C, 2A

F.S.: 1B, 1C, 2B

S.J.: 1C

C.M.: 1C, 2B

J.V.: 1A, 1C, 2B

Disclosures

  1. Top of page
  2. Author Roles
  3. Disclosures
  4. References
  5. Supporting Information

Funding Sources and Conflicts of Interest: The authors report no sources of funding and no conflicts of interest.

Financial Disclosures for previous 12 months: M.M.R. has been awarded a travel grant from Boston Scientific. F.S. has received financial support from Boston Scientific, ECMT, Medtronic, and Archimedes Pharma. J.V. has been a member of the advisory boards of Boston Scientific, Medtronic, and Novartis; has received grant support from Boston Scientific, Medtronic, and AbbVie; and has received honoraria for speaking from Boston Scientific, Medtronic, St. Jude, Novartis, UCB, TEVA, and Allergan.

References

  1. Top of page
  2. Author Roles
  3. Disclosures
  4. References
  5. Supporting Information
  • 1
    Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA. Predictors of future falls in Parkinson disease. Neurology 2010;75:116124.
  • 2
    Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 2011;10:734744.
  • 3
    Moreau C, Defebvre L, Destée A, et al. STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 2008;71:8084.
  • 4
    Fasano A, Herzog J, Seifert E, et al. Modulation of gait coordination by subthalamic stimulation improves freezing of gait. Mov Disord 2011;26:844851.
  • 5
    Weiss D, Walach M, Meisner C, et al. Nigral stimulation for resistant axial motor impairment in Parkinson's disease? A randomized controlled trial. Brain 2013;136(Pt 7):20982108.

Supporting Information

  1. Top of page
  2. Author Roles
  3. Disclosures
  4. References
  5. Supporting Information
FilenameFormatSizeDescription
mdc312018-sup-0001-VideoS1.m4vvideo/x-m4v20447KVideo 1. Clinical examination at first admission to hospital: pirouette test; clinical evaluation of normal gait; and gait while performing provoking maneuver.
mdc312018-sup-0002-VideoS2.m4vvideo/x-m4v3624KVideo 2. Clinical examination with pirouette test after adapting stimulation parameters in an asymmetric manner.

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