Galvanic vestibular stimulation to improve postural instability, voluntary attention, and quality of life in Parkinson's disease patients

ABSTRACT

Galvanic vestibular stimulation (GVS) influences body balance and has proved to be useful to improve patients’ mood, quality of life, and cognitive skills. This study aimed to present three cases of patients with Parkinson’s disease and postural instability who had been submitted to GVS to improve their balance, by assessing the impact of this intervention on their cognition, mood, and quality of life. Patients were assessed before and after GVS sessions concerning P300 latency and scores on the 15-item Geriatric Depression Scale (GDS-15) and the 39-item quality-of-life Parkinson’s Disease Questionnaire (PDQ-39). The three patients’ P300 latency improved, possibly indicating improved attention. Their PDQ-39 score also improved, possibly indicating a positive impact on their quality of life. Their GDS-15 score did not change before and after the intervention. None of the patients had any intervention side effects. This three-case experimental pilot study has shown that GVS is a safe method, possibly useful to improve attention and, therefore, the quality of life of patients presented with Parkinson’s disease.

Keywords:
Parkinson Disease; Postural Balance; Mental Status and Dementia Tests; Quality of Life; Evoked Potentials

RESUMO

A Estimulação Vestibular Galvânica (EVG) atua no equilíbrio corporal e tem se mostrado útil na melhora do humor, da qualidade de vida e de habilidades cognitivas. O objetivo deste estudo foi apresentar três casos de pacientes com doença de Parkinson e instabilidade postural que foram submetidos à EVG para melhorar o equilíbrio e avaliar o impacto dessa intervenção na cognição, no humor e na qualidade de vida. Os pacientes foram avaliados antes e após as sessões de EVG quanto a latência do potencial evocado P300, pontuação na escala de depressão geriátrica de 15 itens (EDG-15) e pelo questionário de qualidade de vida na doença de Parkinson de 39 itens (PDQ-39). Os três pacientes apresentaram melhora na latência do P300, indicando possível melhora na atenção. Apresentaram melhora na pontuação do PDQ-39, indicando possível impacto positivo na qualidade de vida. A pontuação na EDG-15 não modificou antes e após a intervenção. Nenhum paciente apresentou efeitos colaterais decorrentes da intervenção. Com base neste estudo piloto experimental de três casos, a EVG mostrou-se um método seguro e possivelmente útil para melhorar a atenção e, consequentemente, a qualidade de vida de pacientes com doença de Parkinson.

Descritores:
Doença de Parkinson; Equilíbrio Postural; Testes de Estado Mental e Demência; Qualidade de Vida; Potenciais Evocados

INTRODUCTION

Parkinson’s disease (PD) affects various areas of the brain and brainstem¹. Depression and cognitive dysfunction stand out among its nonmotor manifestations because they greatly interfere with the patients’ quality of life¹. Depression may occur in initial PD phases, even before classic motor manifestations, and it is worse in patients with imbalance². Along with cognitive and mood changes, postural instability is a determinant of worsened quality of life³.

Voluntary attention is the cognitive skill affected in the initial phases of PD-related cognitive changes and depression⁴.

Using P300 is particularly important to test attention changes in the initial PD stages (when these cognitive conditions are subtler)⁵. Hence, this electrophysiological examination, which is a simple and noninvasive procedure, is important to early recognize cognitive dysfunctions in PD patients².

Galvanic vestibular stimulation (GVS) is a type of electric stimulation that produces a complex ocular and perceptual motor response to aid the postural rehabilitation process⁶. Studies demonstrate that the efferent vestibular pathways, which send stimuli to the cerebellar vermis via vestibular nuclei, have an important effect on dopaminergic pathways⁷. GVS can activate these efferent pathways in response to vestibular stimulation, as seen in putamen positron emission tomography³. Thus, GVS, which is a safe and painless method, can be used as an auxiliary rehabilitation tool to address motor instability, with positive effects on cognition and mood⁸.

This study aimed to assess GVS’ effects on the mood, cognition, and quality of life of PD patients with postural instability.

CASE PRESENTATION

This study was approved by the Research Ethics Committee of the Santa Casa de Misericórdia Hospital of Belo Horizonte, Brazil, under evaluation report no. 4.165.733 and CAEE 28850619.9.3001.5138.

This experimental pilot study approached three patients diagnosed with PD and postural instability submitted to GVS. They were assessed between July and December 2021 and previously selected at a movement disorder outpatient center. All of them had been previously diagnosed with PD, were taking medications, had postural instability, and were submitted to GVS to improve their body balance⁹.

This study addressed the effects of GVS on cognition, mood, and quality of life. P300 (auditory cognition), the 15-item Geriatric Depression Scale (GDS-15), and the 39-item quality-of-life PD questionnaire (PDQ-39) were assessed before and after the GVS intervention. The participating patients’ hearing was enough to obtain the P300 evoked potential, and they were cognitively intact, as verified with the Mini-Mental State Examination (MMSE), considering the cutoff score equal to or below 24 points to define cognitive decline¹⁰. Before performing P300, patients were submitted to pure-tone threshold audiometry - having hearing loss above 40 dB in a four-frequency mean (500 Hz, 1000 Hz, 2000 Hz, and 4000 Hz) was an exclusion criterion.

Auditory cognition was electrophysiologically assessed with P300 in a single-channel MASBE/system Act Plus equipment (CONTRONIC, Pelotas, Brazil). Electrodes were positioned according to the international 10-20 system, using electrolytic paste between the skin and electrode to improve electric conductivity. The active electrode was fixed on the forehead midline (Fz); the negative electrodes were fixed on the right (A2) and left (A1) earlobes; and the ground electrode (Fp1) was fixed on the forehead to the left of Fz. The electrodes were connected to the preamplifier, and the maximum impedance was set at 2 kΩ. Auditory stimuli were presented through TDH-39 earphones at 90 dBHL, and participants were instructed to identify and count the rare ones. Altogether, 300 stimuli were presented in each examination, divided into 80% frequent ones at 1000 Hz and 20% rare ones at 2000 Hz. The procedure was repeated at least once to ensure record replicability. The initial screening amplitude was 5 uV, with a 20-Hz low-pass filter, 1-Hz high-pass filter, and 60-Hz filter. It was considered that normal hearing older adults without dementia have P300 values compatible with their age range - i.e., 300 to 340 ms in those 48 to 65 years old and 320 to 360 ms in those 66 to 81 years old¹¹.

The GDS-15 cutoff score to screen depression was equal to or above 5 points¹².

PDQ-39 assesses the quality of life in PD, with scores ranging from 0 to 100% - the higher the value, the worse the self-perceived quality of life¹³.

Tests before and after the intervention

Before being submitted to the GVS protocol, the patients answered MMSE. They were also classified on the Hoehn & Yahr scale regarding their degree of disability, based on the neurological examination¹⁴. Hearing loss was characterized based on air-conduction and bone-conduction pure-tone threshold audiometry and the Speech Recognition Index.

Patients were submitted to P300, GDS-15, and PDQ-39 before and after the intervention. The researchers had previously trained the examiners who administered the scales and applied the tests, and the results were blindly analyzed as to whether they were from before or after the intervention.

Galvanic vestibular stimulation (GVS)

The GVS protocol (intervention) had eight weekly sessions, with gradually increasing duration and current intensity, according to the rehabilitation protocol described in Chart 1.

Chart 1
Galvanic vestibular stimulation protocol used for 8 weeks

Number of sessions	1st (1 wk)	2nd (2 wk)	3rd (3 wk)	4th (1 mo)	5th (5 wk)	6th (6 wk)	7th (7 wk)	8th (2 mo)
Stimulation 1	1.0/1.0/3.0	2.0/2.0/3.0	2.0/2.0/5.0	2.0/3.0/5.0	2.5/2.0/5.0	2.5/2.0/5.0	2.5/2.0/5.0	2.5/2.0/5.0
Stimulation 2	1.5/1.0/3.0	2.5/2.0/3.0	2.5/2.0/5.0	2.5/2.0/5.0	3.0/2.0/5.0	3.0/2.0/5.0	3.0/2.0/5.0	3.0/2.0/5.0
Stimulation 3	2.0/1.0/5.0	2.5/2.0/3.0	2.5/2.0/5.0	2.5/3.0/5.0	3.5/2.0/5.0	3.5/2.0/5.0	3.5/2.0/5.0	3.5/2.0/5.0

• Captions: wk = weeks; mo = months; (voltage in milliampere/ stimulus duration in minutes/number of stimulus repetition)

GVS was applied with an EVKGVS Galvanic Stimulator (CONTRONIC, Pelotas, Brazil). The stimulation was presented through disposable, adhesive, 3-cm-wide surface electrodes (manufactured by Valutrode, model CF3200), fixed on both mastoid processes, providing binaural and bipolar stimulation. The stimuli were generated by a rectangular current stimulator with pulsed alternating polarity, at an intensity ranging from 1 to 3.5 mA, lasting from 1 to 3 minutes.

RESULTS

The patients’ characteristics, time with PD, educational attainment, and pre-intervention examination results are described in Chart 1. The three patients had no history of previous vestibular disease, myelitis, or stroke; they did not have a pacemaker, and their PD medication had not been changed within 30 days before the assessment. Their best-ear hearing thresholds were all compatible with mild sensorineural hearing loss, and none of the patients had abnormal MMSE.

Cases 1 and 2 were on Hoehn & Yahr¹⁴ PD disability stage 3 (bilateral symptoms and moderate postural instability - i.e., the patient is independent but has some functional loss). Case 3 was on stage 4 (important functional disability; stands and walks with help)¹⁵. Scale and examination results before and after the intervention are shown in Charts 2, 3, and 4.

Chart 2
Information on sex, age, time with the disease, educational attainment, best-ear hearing threshold, and Mini-Mental State Examination

Case	Sex	Age (years)	Time with the disease (years)	Educational attainment (years)	Best-ear mean* hearing threshold (Hz)	MMSE
1	male	77	9	8	30	25
2	male	70	8	4	30	28
3	female	65	11	4	25	27

• Caption: MMSE = Mini-Mental State Examination; *considering the three-frequency mean between 500, 1000, and 2000 Hz

Chart 3
Scores of the quality-of-life questionnaire and Geriatric Depression Scale before and after 8 galvanic vestibular stimulation sessions

Tests	GVS	Case 1	Case 2	Case 3
PDQ-39 µ	Before	61	45	62
	After	21	38	40
GDS ρ	Before	8	5	4
	After	7	8	2

• Captions: PDQ-39^µ = quality-of-life questionnaire; GDS-15^ρ = Geriatric Depression Scale; GVS = galvanic vestibular stimulation; ^µ = higher scores indicate a worse perception of the quality of life; ^ρ = cutoff score ≥ 5 to determine the presence of depressive symptoms in older adults.

Chart 4 shows that the three cases’ P300 latency decreased after the intervention, which indicates improved voluntary attention.

Chart 4
Latency and amplitude of the long-latency auditory evoked potential before and after 8 galvanic vestibular stimulation sessions

Examination	GVS	Parameters	Case 1	Case 2	Case 3
P300	Before	Latency (ms)	376.74	379.27	351.51
		Amplitude (µV)	3.15	4.83	5.77
	After	Latency (ms)	328.81	336.38	321.24
		Amplitude (µV)	1.9	11.83	15.8

• Captions: ms = milliseconds; µV = microvolts; P300 = long-latency auditory evoked potential; GVS = galvanic vestibular stimulation

DISCUSSION

The three patients in this study had their cognitive parameters improved after GVS.

PD patients have cognitive changes more often¹. Since dementia can interfere with P300 response, this study only included cognitively intact patients, as screened with MMSE. Hence, it was possible to assess whether any change had taken place in the auditory cognition of patients without dementia, based on the P300 evoked response, after they had been submitted to GVS sessions. P300 latency reflects the auditory processing speed regarding external stimuli, attention, and working memory¹⁶. The three patients’ latency values decreased after the intervention, which possibly indicates an improvement.

This study showed improved GDS-15 scores after the intervention in two patients. A previous study demonstrated that GVS positively impacts mood and anxiety¹⁷. It has also been observed that GVS quickened the bradykinetic rest-to-active transition in PD¹⁸. This gain helped improve these patients’ quality of life and, consequently, their mood^19,20. PDQ-39 scores in this study improved after GVS - thus, agreeing with findings in the literature on GVS’ positive impact on cognition and mood.

Previous articles have demonstrated that GVS generally influences brain connectivity, possibly improving neural interactions in PD^9,21.

The cerebellar visual network and other pontine/cortical projections derived from the prefrontal, posterior parietal, and temporal lobe cortex and the limbic system are impaired in PD²². GVS is believed to promote cognition improvement mechanisms by increasing cerebellar connectivity^9,22.

This study has some limitations concerning GVS effectiveness and efficiency to improve attention and quality of life in PD. It did not analyze a control group receiving placebo stimuli, and its sample size was insufficient for statistical analyses. On the other hand, in a clinical trial design, three cases assessed before and after the intervention make it possible to evaluate safety and tolerability. Paresthesia, itchy skin where electrodes had been fixed, and dysgeusia have been reported as possible GVS side effects²². None of the patients in this study complained of possible intervention side effects.

CONCLUSION

The analysis of three cases before and after applying GVS showed that this method is safe, well-tolerated, easy to perform, and possibly useful to improve PD patients’ executive function, attention, and, therefore, quality of life and body imbalance.

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• Study conducted at Universidade Federal de Minas Gerias, Belo Horizonte, Minas Gerais, Brazil.
• Financial support: Nothing to declare.

Publication Dates

• Publication in this collection
  14 Aug 2023
• Date of issue
  2023

History

• Received
  28 Jan 2023
• Accepted
  12 June 2023