High Cervical Spinal Cord Stimulation: A One Year Follow-Up Study on Motor and Non-Motor Functions in Parkinson's Disease

Paolo Mazzone, Fabio Viselli, Stefano Ferraina, Margherita Giamundo, Massimo Marano, Marco Paoloni, Francesco Masedu, Annamaria Capozzo, Eugenio Scarnati, Paolo Mazzone, Fabio Viselli, Stefano Ferraina, Margherita Giamundo, Massimo Marano, Marco Paoloni, Francesco Masedu, Annamaria Capozzo, Eugenio Scarnati

Abstract

Background: The present study investigated the effectiveness of stimulation applied at cervical levels on pain and Parkinson's disease (PD) symptoms using either tonic or burst stimulation mode.

Methods: Tonic high cervical spinal cord stimulation (T-HCSCS) was applied on six PD patients suffering from low back pain and failed back surgery syndrome, while burst HCSCS (B-HCSCS) was applied in twelve PD patients to treat primarily motor deficits. Stimulation was applied percutaneously with quadripolar or octapolar electrodes. Clinical evaluation was assessed by the Unified Parkinson's Disease Rating Scale (UPDRS) and the Hoehn and Yahr (H&Y) scale. Pain was evaluated by a visual analog scale. Evaluations of gait and of performance in a cognitive motor task were performed in some patients subjected to B-HCSCS. One patient who also suffered from severe autonomic cardiovascular dysfunction was investigated to evaluate the effectiveness of B-HCSCS on autonomic functions.

Results: B-HCSCS was more effective and had more consistent effects than T-HCSCS in reducing pain. In addition, B-HCSCS improved UPDRS scores, including motor sub-items and tremor and H&Y score. Motor benefits appeared quickly after the beginning of B-HCSCS, in contrast to long latency improvements induced by T-HCSCS. A slight decrease of effectiveness was observed 12 months after implantation. B-HCSCS also improved gait and ability of patients to correctly perform a cognitive-motor task requiring inhibition of a prepared movement. Finally, B-HCSCS ameliorated autonomic control in the investigated patient.

Conclusions: The results support a better usefulness of B-HCSCS compared to T-HCSCS in controlling pain and specific aspects of PD motor and non-motor deficits for at least one year.

Keywords: Parkinson’s disease; Valsava maneuver; burst stimulation; cervical spinal cord stimulation; gait; reaction time; tonic stimulation.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(A,C) Position of active contacts and type of electrode in Group I and Group II patients. (B,D) Representative examples of a quadripolar and octapolar electrode inserted at cervical level.
Figure 2
Figure 2
Schematic representation of the cognitive–motor task. (A) In Go trials, the subjects had to respond by moving a joystick at the presentation of a green arrow to generate the reaction time (RT). (B) In stop trials, they had to suppress the ongoing movement if a red square was presented in the interval within the reaction time window of the Go trial. The interval between presentation of the stop signal and suppression of movement represented the stop signal reaction time (SSRT).
Figure 3
Figure 3
(A) Tonic stimulation (red) UPDRS scores at 3, 6, and 12 months differed significantly compared to presurgery, stimulation OFF, and acute stimulation values (# p < 0.001). Burst stimulation (blue) improved UPDRS scores significantly after acute stimulation as well as at 3, 6, and 12 months (° p < 0.001) compared to presurgery and stimulation OFF values. Burst stimulation was more effective than tonic stimulation at all the timepoints considered (* p < 0.001). (B) 27–31 motor sub-items evaluations at 3, 6, and 12 months differed significantly during tonic stimulation compared to presurgery, stimulation OFF, and acute stimulation values (# p < 0.05). Burst stimulation significantly improved motor sub-items comparing acute, stimulation OFF and 3, 6, and 12 months to presurgery value (° p < 0.001). Burst stimulation was significantly more effective than tonic stimulation in the acute condition (* p < 0.05). (C) Hoehn and Yahr evaluations at 3, 6, and 12 months differed significantly during tonic stimulation compared to presurgery, stimulation OFF, and acute stimulation values (# p < 0.001). Burst stimulation significantly improved Hoehn and Yahr score comparing acute, 3, 6, and 12 months to presurgery and stimulation OFF values (° p < 0.001). Burst stimulation was significantly more effective than tonic stimulation in the acute condition (* p < 0.05). Statistics were assessed by Friedman tests.
Figure 4
Figure 4
(A) Tremor was significantly reduced during burst stimulation at all time points compared to presurgery and stimulation OFF values (° p < 0.05). (B) Pain at 3, 6, and 12 months poststimulation was significantly reduced by both types of stimulation compared to the presurgery condition (#° p < 0.05). Statistics were assessed by Friedman tests.
Figure 5
Figure 5
Improvement of spatiotemporal gait parameters (gait speed, cadence, step length, stride length, step width, swing speed, stance duration, double support) in the two groups of patients investigated at six months under T-HCSCS (red) or B-HCSCS (blue). * p < 0.05: Control vs. T-OFF and B-OFF; # T-OFF vs. T-ON; ° B-OFF vs. B-ON (except cadence: p < 0.001) and stance duration (not significant). Statistics were assessed by Mann–Whitney tests.
Figure 6
Figure 6
In patients, burst stimulation reduced the duration of the SSRT, while the RT duration was unaffected. Go signal: * p < 0.05 controls vs. OFF and vs. ON; Stop signal: * p < 0.05 controls vs. OFF and vs. ON, ° p < 0.05 OFF vs. ON. Statistics were assessed by Mann–Whitney tests.

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