Effects of different side motor impairments at early onset on voice acoustic performance in patients with Parkinson’s disease

Highlights

• •Movement impairments of the left or right limbs at an early onset influence voice disorders differently in patients with Parkinson's disease.
• •Patients with Parkinson's disease who have left-sided motor impairments at an early onset showed a rapid deterioration of voice difficulties.
• •Evaluations of voice disorders in patients with Parkinson's disease should consider the laterality of motor impairments at the early onset as a predictive factor for the development of voice disorders.

Abstract

Purpose

This study aimed to explore the effects of motor impairments on different sides of the body at early onset in relation to voice acoustic performance in patients with Parkinson’s disease.

Materials and methods

Participants were classified based on which side (left or right) experienced motor impairments first, as well as the stage (early or late) of the disease. Hoehn-Yahr stages one and two were categorized as early-stage, while stages three and four were categorized as late-stage. Participants were divided into four groups: Group A, left-side early-stage conditions; Group B, left-side late-stage conditions; Group C, right-side early-stage conditions; Group D, right-side late-stage conditions. Participants performed three recording tasks that involved sustained phonation of the vowels/a/,/i/, and/u/. The study analyzed four acoustic parameters: Maximum Phonation Time (MPT), jitter, shimmer, and vF0.

Results

An Analysis of Variance revealed that for the acoustic parameters of /a/vF0 and /a/jitter, Group B performed significantly worse than Group A (p < 0.05). No significant differences were found in the other acoustic parameters or in MPT voice performance across the four groups.

Conclusions

The side of motor impairments at early onset is correlated with the severity of voice disorders. Notably, when impairments occur on the left side, the resulting voice disorders become more pronounced as the disease progresses.

1. Introduction

Progressive neurological diseases often significantly impact speech. One of the examples, Parkinson’s disease (PD), is a chronic degenerative disease of the central nervous system that is primarily characterized by motor function impairment and a wide range of non-motor symptoms. Hypokinetic dysarthria causes are unknown; they may be neural, physiological changes, or abnormal coordination across systems. Dysarthria is a speech-motor control disorder caused by damage to the central or peripheral nervous system, which leads to disrupted muscle control during speech production. This results in unclear articulation, hoarse voice quality, monotone speech, and other abnormalities. Motor speech disorders affect articulation, phonation, respiration, and resonance due to motor dysfunction [1]. The study has shown that the control of force in complex motor sequences involving speech and limb movement is affected by a common deficit in the frontostriatal circuit [2]. Speech movements are complex behaviors. Although the organizational mechanisms of speech and limb movements differ, speech and gait rhythm disorders have similar underlying pathomechanisms in patients with PD [3]. Both motor difficulties and speech disorders are considered axial symptoms of PD and share some common pathophysiological mechanisms [4]. A correlation was observed between gait impairment and oral diadochokinesis in patients with PD [5]. Similarly, the speech rate and walking speed of patients with PD were correlated [6].

In patients with PD, motor impairments typically begin on one side of the body and eventually affect both sides as the disease progresses. Studies indicate that the laterality of initial onset is linked to the trajectory of symptom development and is essential for prognosis because the progression rate and incidence of secondary symptoms vary depending on the side of motor impairment [7]. The study demonstrated that the initial laterality of motor impairment in patients with PD is related to the evolution of motor dysfunction severity and non-motor symptoms [8]. Furthermore, asymmetrical motor impairments in patients with PD are associated with lateralized brain activity. Specifically, patients with left-side motor impairments exhibit greater motor dysfunction variability than those with right-side impairments [9]. Patients with PD who exhibit lower availability of the left dopamine transporter (DAT) experience more severe dysarthria compared to those with lower right DAT availability [10]. Some research indicates that while levodopa improves general motor function, it doesn't necessarily translate to significant improvements in speech [[11], [12], [13]]. For each dose of levodopa, the “ON” benefit typically lasts about 2–3 h on average [14]. To ensure consistency in the research, it was essential for participants to complete their voice sample recordings within 2 h after taking the medication.

Various parameters of acoustic analysis have emerged as an increasingly utilized objective assessment method for studying speech disorders in patients with PD. Maximum phonation time (MPT) reflects the longest duration of phonation possible in a single breath, serving as an indicator of the function of respiration and phonation. The longer the MPT, the better the function of respiration and phonation. Jitter percent (%) measures the irregularity of the fundamental frequency period during phonation, indicating the degree of frequency perturbation, with higher values suggesting less stable voice quality. Shimmer percent (%) assesses the variation in the amplitude of vocal fold vibrations, with higher values indicating more significant fluctuations in voice volume. Lastly, fundamental frequency variation (vF0, %) represents the relative standard deviation of the fundamental frequency (F0), reflecting long-term variations in F0 across all analyzed speech samples. This study used acoustic analysis software to gather data on four acoustic parameters: jitter, shimmer, vF0, and MPT—during the production of the vowels /a/,/i/, and /u/.

Recent studies have shown that patients with PD exhibit higher values for specific vowel acoustic parameters, specifically jitter percentage and vocal fundamental frequency (vF0), compared to healthy controls [15]. These impairments were shown to worsen as the disease progressed. There has been extensive research on motor impairments and speech communication challenges in individuals with PD. However, to date, there have been no studies exploring how different-sided motor impairments at early onset impact voice acoustic performance in patients with PD. We believe this is a critical issue in preventing communication disorders for patients with PD.

2. Methods

2.1. Design

2.1.1. Participants

This study included 62 patients with primary PD, comprising 32 females and 30 males with a mean age of 69 years (SD = 9.21). Patients with PD were referred by a physician and diagnosed and confirmed as having primary PD in the department of neurology at a medical center. Informed consent was obtained from all of them. The patients with hearing impairment or cognitive factors were excluded. Hearing impairment was determined by failure in response to 512 Hz and 1024 Hz tuning fork tests. The cognitive factor was determined when a Clinical Dementia Rating (CDR) [16] score was equal to or greater than 1.

2.2. Measurement tools

2.2.1. Hoehn and Yahr scale (H & Y Scale)

The H & Y Scale is a commonly used system for clinically recording the level of symptoms of PD patients [17].

2.2.2. CDR

A CDR score of 0 indicates no dementia; 0.5 indicates undetermined or under observation; 1 indicates mild dementia; 2 indicates moderate dementia; 3 indicates severe dementia; 4 indicates profound dementia; and 5 indicates terminal dementia [16].

2.2.3. Multidimensional voice program (MDVP)

This study conducted an acoustic analysis using the MDVP (Model 5101). There are several software programs used in analyzing the voice, of which MDVP is currently used in routine clinical practice. It is commented that MDVP is the most widely used software for the acoustic analysis of voice globally [18].

2.3. Research procedure

The study procedure involved participants reporting the side (left or right) where movement impairments first experienced at early onset, which was confirmed and recorded by neurologists. Then, neurologists assessed the stage of motor impairments using the H&Y scale, and cognitive function was evaluated using the CDR scale.

This study classified participants based on which side (left or right) experienced motor impairments first, as well as the stage of the disease (early or late). H&Y stages one and two were categorized as early-stage disease, while stages three and four were classified as late-stage disease. Participants were divided into four groups: Group A, left-side early-stage conditions; Group B, left-side late-stage conditions; Group C, right-side early-stage conditions; and Group D, right-side late-stage conditions, as detailed in Table 1.

Table 1.

Demographic characteristics of the participants (N = 62).

Variable	Age(years): Mean (SD)	n
Total	69.0 (9.2)	62
Male	67.9 (9.9)	30
Female	70.0 (8.5)	32
Group A	68.2 (7.4)	23
Male	65.8 (7.2)	10
Female	70.0 (6.6)	13
Group B	66.9 (13.8)	13
Male	64.7 (13.3)	7
Female	69.3 (12.9)	6
Group C	68.9 (7.2)	13
Male	67.8 (5.5)	6
Female	69.9 (7.8)	7
Group D	72.7 (8.2)	13
Male	74.3 (8.5)	7
Female	70.8 (6.6)	6

The researchers collected speech samples in a quiet, private space. The speech samples included three recording tasks that involved the sustained phonation of the vowels /a/, /i/, and /u/. This study analyzed four acoustic parameters: MPT, jitter, shimmer, and vF0. All recordings of participants were conducted one hour after medication and completed within two hours of drug administration. The background noise in the recording space was kept below 30 dB. Speech samples were captured with a portable high-resolution digital recorder (Tascam, DR-07), placed at a distance of 15 cm from the participants to ensure the stability of speech sample volume and voice quality. Each recording session lasted approximately 5 minutes.

2.4. Statistical analysis

Data analyses were performed using SPSS Version 20. The significance level p was set at 0.05. This study analyzed the data using a one-way ANOVA followed by post-hoc tests (Tukey’s HSD) to control for multiple comparisons.

3. Results

An Analysis of Variance revealed that for the acoustic parameters of /a/vF0 and /a/jitter, Group B performed significantly worse than Group A (p < 0.05). No significant differences were found in the other acoustic parameters or in MPT voice performance across the four groups. Detailed statistical data are presented in Table 2, Table 3, Table 4.

Table 2.

SUMMARY.

		Groups	Count	Average	SD
/a/vF0		A	23	1.999	0.973
		B	13	8.860	12.521
		C	13	4.485	7.970
		D	13	3.998	2.129
/a/jitter		A	23	1.281	0.932
		B	13	2.963	2.890
		C	13	1.797	1.760
		D	13	1.877	1.025

Table 3.

ANOVA.

	Source of variation	SS	df	MS	F	p-value
/a/vF0	Between Groups	393.271	3	131.090	2.797	0.048
	Within Groups	2718.675	58	46.874
	Total	3111.946	61
/a/jitter	Between Groups	23.576	3	7.859	2.695	0.054
	Within Groups	169.097	58	2.915
	Total	192.673	61

Table 4.

Post hoc (Tukey HSD).

	(i) Group	(j) Group	Mean Difference (i-j)	Std. Error	Sig.
/a/vF0	A	B	−6.860*	2.376	0.027
		C	−2.485	2.376	0.723
		D	−1.999	2.376	0.835
/a/jitter	A	B	−1.682*	0.593	0.031
		C	−0.515	0.593	0.820
		D	−0.596	0.593	0.747

*p < 0.05.

4. Discussion

The study findings indicated that there were no significant differences in MPT performance among the four groups of patients with PD. This suggests that the control of respiration and phonation may not be significantly affected by the progression of the disease or by laterality. Previous research has shown that many healthy older adults can phonate for at least 20 seconds. In our study, although there was no significant difference in MPT among the four groups of PD subjects, the average duration was found to be less than 20 s. MPT is a vital clinical tool for assessing phonation and respiratory muscle function. A reduction in MPT among patients with PD indicates compromised respiratory function, highlighting the importance of maintaining MPT to prevent deterioration of lung function and related complications. A study noted that reduced MPT often occurs alongside low vocal intensity and limited prosodic range in both neurologic and aging populations, which can restrict audibility and expressive nuance in everyday communication [19].

The vF0 % is a voice stability indicator based on sustained vowels. A high vF0 % may indicate reduced neuromuscular control, developmental immaturity in children, certain pathological conditions, or compensatory behavior [20]. Clinically, differences in vF0 % are often used to assess vocal changes related to age and specific neurological conditions. Jitter % commonly used in clinical acoustic examinations reflects the control of vocal fold vibration [21]. Jitter % specifically measures the micro-instability of the vocal fold vibrations, which are the source of sound in the voice. Elevated jitter % signals unstable vocal fold vibration and is associated with rough/hoarse quality and higher overall dysphonia ratings. High jitter % are often indicative of voice pathologies, such as roughness, hoarseness, or breathiness, due to irregular vocal fold vibration [20]. A systematic literature review indicated that jitter % is significantly elevated in patients with PD [20].

A study reported that healthy elderly individuals, aged 62 to 75, had average values of 2.327 for /a/-vF0 and 1.508 for /a/-jitter [20]. In contrast, Group A showed lower performance for the vowel /a/, with values of 1.999 for vF0 and 1.281 for jitter. Meanwhile, Group B exhibited significantly higher values, with 8.860 for vF0 and 2.963 for jitter, surpassing those of the healthy elderly individuals. Therefore, patients with PD who initially experienced movement impairments on the left side have their voice disorders progress rapidly. On the other hand, the average values of /a/-vF0 in Groups C and D were 4.485 and 3.998, respectively, while the /a/-jitter values were 1.797 and 1.877, respectively. Although these values were higher than those found in healthy elderly adults, the differences were not significant. This indicates that patients with PD who initially experienced movement impairments on the right side tend to have a slow progression of voice disorders. In comparison, /a/-simmer in healthy elderly adults was 6.670, and for the four groups of PD patients were 4.573, 6.117, 6.002, and 4.846, respectively, all of which fall within the normal range of 1.65 to 6.73 [20].

Voice acoustic analysis is a valuable clinical tool for detecting changes in voice disorders in patients with PD. However, previous reports on acoustic analysis have produced inconsistent results, likely due to the failure to account for the lateralization of motor impairments that patients initially experienced. Therefore, future evaluations of voice disorders in patients with PD should consider the laterality of motor impairments at early onset as a predictive factor for the development of voice disorders.

This study included participants from a medical center in the southern region of Taiwan, which may have limitations due to specific Mandarin and cultural factors. Future research will aim to increase the sample size by including participants from a variety of Mandarin dialects and cultures.

5. Conclusions

Speech is essential for maintaining a good quality of life, highlighting the urgent need for early and objective diagnostic markers. This study found no significant differences in the acoustic parameters between the early and late stages of the disease in patients with PD who have right-side motor impairments at the early onset. This suggests that voice difficulties progress relatively slowly in these patients. In contrast, patients with PD who have left-side motor impairments at the early onset showed significant differences in voice disorders between the early and late stages of the disease, indicating a rapid deterioration of voice difficulties in these patients. Therefore, future speech therapy should take into account the influence of motor impairment laterality at the early onset in patients with PD.

Ethical approval

This study received ethical approval from the KAOHSIUNG V.G.H. IRB (No: VGHKS17-CT11-07) on October 6th, 2017, and informed consent was obtained from all participants.

CRediT authorship contribution statement

Chi-Lin Chen: Writing – review & editing, Writing – original draft, Software, Methodology, Data curation, Conceptualization. Ching-Huang Lin: Supervision, Resources. Kai-Li Chen: Validation, Writing – review & editing. Chen-San Su: Supervision, Resources.

Funding

The author(s) received no financial support for this article’s research, authorship, and publication.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.