Optimising verbal fluency analysis in neurological patients with dysarthria: examples from Parkinson’s disease and hereditary ataxia

Figures & data

Table 1. Demographic and clinical characteristics of participants.

Characteristics	Disease		p-value	Effect size
	Ataxia (N = 61)	Parkinson’s Disease (N = 69)
Gender (N, %) Female Male	37 (60.66%) 24 (39.34%)	34 (49.28%) 35 (50.72%)	0.193	0.013
Age (mean ± SD, range, years)	50.62 ± 13.18 (20–74)	67.62 ± 8.54 (48–83)	<0.001***	1.509
Years of education (N, %)			0.073	0.048
Year 11 or below	_9 (14.75%) 24 (39.34%) 19 (31.15%) 9 (14.75%)	24 (34.78%) 18 (26.09%) 27 (18.84%) 14 (20.29%)
Year 12/diploma/certificate Undergraduate degree Postgraduate degree
Diagnosis (N, %)	35 (57.38%) FA 3 (4.92%) SCA 1 3 (4.92%) SCA 2 1 (1.64%) SCA 3 9 (14.75%) SCA 6 1 (1.64%) SCA 7 2 (3.28%) SCA 14 2 (3.28%) CANVAS 4 (6.56%) Other cerebellar ataxias 1 (1.64%) MSC-A	Idiopathic PD 1 (1.45%) H&Y stage 0 37 (53.62%) H&Y stage 1 28 (40.58%) H&Y stage 2 3 (4.35%) H&Y stage 3	-	-
VFT Total Correct Items (mean, SD) Semantic fluency Phonemic fluency Alternating fluency	17.820 (6.781) 8.738 (4.262) 9.541 (3.650)	18.681 (5.561) 13.058 (4.262) 12.420 (2.977)	0.437--	0.137--
Overall dysarthria (mean, SD, range)	2.05 (1.01; 0–4)	1.55 (0.676; 0–3)	0.001**	0.581
Disease Severity Measure‡ (mean, SD)	22.7 (9.64)	18.4 (11.08)	-	-

Notes: CANVAS = cerebellar ataxia, neuropathy, and vestibular areflexia syndrome; FA = Friedreich ataxia; H&Y Stage = Hoehn and Yahr stage; MSA-C = Multiple system atrophy, cerebellar; SCA = spinocerebellar ataxia; SD = standard deviation; VFT = verbal fluency test.

*p < 0.05; **p < 0.01; ***p < 0.001.

‡ Disease severity measured by the Scale for Assessment and Rating of Ataxia (SARA, 0 = unremarkable, 40 = severe) and the Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) Part III (motor examination) Score. PD patients’ chronological age is significantly greater than ataxia patients’ age (p < 0.001).

Figure 1. Spearman’s correlation between VFT dysarthria ratings and monologue dysarthria ratings (intelligibility, naturalness, N = 58) of the ataxia patients.

Table 2. Hierarchical linear regression analysis: the effect of dysarthria on total correct items.

Group	Task	Step	†Beta	†Standardized Beta	Δ R^2	Δ F	P-value	Partial correlation
PD	Semantic fluency	1 MDS-UPDRS III	−0.124	−0.247	0.124	9.509	0.037	−0.255
		2 Education	0.271	0.168	0.026	2.022	0.139	0.183
		3 dysarthria rating	−2.204	−0.268	0.067	5.555	0.021	−0.281
	Phonemic fluency	1 MDS-UPDRS III	−0.067	−0.154	0.081	5.902	0.185	−0.164
		2 Education	0.460	0.329	0.102	8.195	0.004*	0.345
		3 dysarthria rating	−1.677	−0.235	0.052	4.371	0.040	−0.251
	Alternating fluency	1 MDS-UPDRS III	−0.067	−0.251	0.110	8.303	0.040	−0.251
		2 Education	0.161	0.186	0.033	2.507	0.112	0.196
		3 dysarthria rating	−0.704	−0.160	0.024	1.857	0.178	−0.167
Ataxia	Semantic fluency	1 SARA	−0.153	−0.217	0.180	12.947	0.080	−0.230
		2 Education	−0.079	−0.024	0.000	0.004	0.822	−0.030
		3 dysarthria rating	−2.998	−0.445	0.155	13.266	0.001**	−0.435
	Phonemic fluency	1 SARA	−0.075	−0.170	0.140	9.593	0.177	−0.178
		2 Education	0.352	0.173	0.036	2.498	0.122	0.204
		3 dysarthria rating	−1.777	−0.420	0.138	11.428	0.001**	−0.409
	Alternating fluency	1 SARA	−0.110	−0.290	0.249	19.543	0.014	−0.316
		2 Education	−0.027	−0.015	0.000	0.000	0.882	−0.020
		3 dysarthria rating	−1.626	−0.449	0.157	15.239	0.000***	−0.458

Notes: PD = Parkinson’s Disease; Beta = Linear Regression Coefficient; SARA = Scale for Assessment and Rating of Ataxia; MDS-UPDRS III = Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Part III Score; Education = Years of Education; Δ R² = R square change; Δ F = F change; Bonferroni adjusted α = 0.0166; *p < 0.0166; **p < 0.0033; ***p < 0.00033.

†All Betas and Standardized Betas reported in Table 2 were from the final regression model after all independent variables were entered.

Figure 2. Post-hoc comparisons of dysarthria’s main effect on ambiguous verbalizations, intrusions, interjections and perseverations (mean ± standard error) in semantic, phonemic, and alternating fluency in the ataxia group (N = 61, N = 3, 13, 30, 8, 7 respectively for dysarthria severity 0, 1, 2, 3, 4) and PD group (N = 69, N = 3, 29, 33, 4 respectively for dysarthria severity 0, 1, 2, 3) *p < 0.05; **p < 0.01; ***p < 0.001.

Table 3. Interrater reliability analysis: Intra-class correlation (ICC) in the ataxia and PD groups across speech parameters.

Parameters Group	Articulation	Voice quality	Resonance	Intelligibility	Naturalness
Ataxia (N = 61)	0.905***	0.763***	0.692***	0.920***	0.910***
PD (N = 69)	0.737***	0.796***	NA†	0.938***	0.838***

Notes: PD = Parkinson’s Disease; ***p < 0.001; NA = not available.

† %agreement between raters = 94.2%; ICC could not be calculated because of lack of variability of the ratings, that is, most subjects were rated zero in terms of resonance.

Table A1. Work on the impact of dysarthria on VFT performance in individuals with PD or ataxia.

Study	Population	Main Finding
Barbosa et al., 2017	PD	VFT scores were correlated with both cognition and motor functions exhibited by the Trail Making Test (TMT).
Obeso et al., 2012	PD	Participant performance on semantic and phonemic fluency was impacted by the onset patterns and severity of motor impairment.
Cooper et al., 1991	PD
Hoche et al., 2018	Ataxia	Dysarthria was associated with lower VFT performance, justified by the significant negative correlation between VFT scores and dysarthria ratings.
Lopes et al., 2013	Ataxia
Feng et al., 2014	Ataxia	Authors estimated time required to think of an item to eliminate the impact of dysarthria on VFT.
Bürk et al., 2003	Ataxia	There is no significant correlation between oral-motor impairments and VFT performance.
Leggio, 2000	Ataxia
Tamura et al., 2018	Ataxia	No correlation was found between phonemic fluency and speech disturbance score.

Notes: PD = Parkinson’s disease; VFT = verbal fluency test.

Dysarthria features, severity, and qualitative parameters.

Dysarthria Parameters	Explanation
Articulation	Precision and accuracy of consonant and vowel production
Voice quality	Deviation of voice parameters relating to roughness, strain, breathiness, pitch, and loudness.
Resonance	Hyper-, hypo-nasality or mixed nasality
Intelligibility	The extent to which listeners can understand a speaker.
Naturalness	The extent of speech output being perceived as normal or natural by listeners.
Dysarthria severity	Explanation
0 (normal)	Unremarkable speech.
1 (subclinical)	Very mild changes of participant’s speech, typically not identified by untrained listeners.
2 (mild)	Speech mildly dysarthric, with deficits across a single or multiple subdomains and some words difficult to understand.
3 (moderate)	Clear dysarthric profile with deficits across several speech subsystems and multiple words of phrases difficult to understand.
4 (severe)	Significant difficulty understanding the speaker. Deficits across most subdomains.
VFT parameters	Explanation	Example
Total Correct Items	Words belong to the specified category.	“apple” when asked to recall fruit
Intrusions	Words that do not exist or do not follow instructions.	“apple” when asked to recall vegetables
Ambiguous verbalizations	Verbalizations that cannot be recognized.
Perseverations	Repeated correct items or repeated incorrect items.	Mention “dog” or “apple” twice in animal semantic fluency.
Interjections	Fillers.	“uh”; “um”

Dysarthria rating training procedure.

Dysarthria rating training
Trainer	An experienced examiner with speech pathology background from the SpeechATAX study who had developed expertise in working discriminating dysarthric speech.
Trainee	Three Master of Speech Pathology students working on the current study.
Training session design	60 minutes video meeting each session. 2 sessions were delivered.
Procedures:	The trainer introduced the definition of parameters: articulation, voice quality, resonance, intelligibility, naturalness. Specific examples were provided for the normal and abnormal presentation for each parameter. The Trainer played audio recordings of a de-identified participant from the ataxia group with unknown dysarthria severity. The trainees provided rating across 5 parameters and discuss a consensus rating for each parameter. Trainees discussed the reasons for giving certain ratings. The trainer provided the agreed dysarthria from the SpeechATAX study. The trainer and the trainee repeated 2–4 for five patients. The trainees and the trainer discussed any unresolved questions. Trainer kept providing ongoing support during the scoring process.

Supplemental regression analysis: The effect of dysarthria on total correct items (with speech items omitted from disease severity measures).

Group	Task	Step	Beta	Standardized Beta	Δ R^2	Δ F	P-value	Partial correlation
PD	Semantic fluency	1 MDS-UPDRS III without speech items	−0.126	−0.243	0.121	9.215	0.041	−0.251
		2 Education	0.272	0.169	0.026	2.027	0.139	0.183
		3 dysarthria rating	−2.224	−0.270	0.068	5.653	0.020	−0.283
	Phonemic fluency	1 MDS-UPDRS III without speech items	−0.067	−0.148	0.078	5.660	0.202	−0.158
		2 Education	0.461	0.329	0.102	8.210	0.004*	0.345
		3 dysarthria rating	−1.692	−0.237	0.053	4.454	0.039	−0.253
	Alternating fluency	1 MDS-UPDRS III without speech items	−0.071	−0.256	0.113	8.543	0.036	−0.257
		2 Education	0.160	0.185	0.032	2.473	0.115	0.194
		3 dysarthria rating	−0.704	−0.160	0.024	1.867	0.177	−0.167
Ataxia	Semantic fluency	1 SARA without speech items	−0.146	−0.195	0.148	10.267	0.108	−0.212
		2 Education	−0.083	−0.026	0.000	0.004	0.815	−0.031
		3 dysarthria rating	−3.144	−0.467	0.181	15.382	0.000***	−0.461
	Phonemic fluency	1 SARA without speech items	−0.073	−0.155	0.117	7.851	0.205	−0.168
		2 Education	0.350	0.172	0.035	2.430	0.124	0.202
		3 dysarthria rating	−1.844	−0.436	0.158	13.024	0.001**	−0.431
	Alternating fluency	1 SARA without speech items	−0.110	−0.272	0.217	16.309	0.019*	−0.306
		2 Education	−0.030	−0.017	0.000	0.000	0.868	−0.022
		3 dysarthria rating	−1.712	−0.473	0.185	17.932	0.000***	−0.486

Notes: PD = Parkinson’s Disease; Beta = Linear Regression Coefficient; SARA = Scale for Assessment and Rating of Ataxia; MDS-UPDRS III = Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Part III Score; Education = Years of Education; Δ R² = R square change; Δ F = F change; Bonferroni adjusted α = 0.0166; *p < 0.0166; **p < 0.0033; ***p < 0.00033.

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