Hypokinetic dysarthria is a multidimensional impairment affecting all main speech subsystems with variable patterns and severity across individual Parkinson's disease (PD) patients. We can thus assume that inter-individual abnormal speech patterns are related to the various clinical subtypes of PD with different prominent motor symptoms. The aim of this cross-sectional study was to compare speech disorder between patients with the postural instability/gait difficulty (PIGD) and tremor-dominant (TD) motor phenotypes of PD. Speech samples were acquired from a total of 63 participants, including 21 PIGD patients, 21 TD patients, and 21 healthy controls. Quantitative acoustic vocal assessment of 12 unique speech dimensions related to phonation, vocal tremor, oral diadochokinesis, articulation, prosody and speech timing was performed. Speech impairment was more pronounced in the PIGD group than in the TD group, with an area under the curve of 0.76. Patients in the PIGD group manifested abnormalities in pitch breaks, articulatory decay, decreased rate of follow-up speech segments and inappropriate silences, apart from monopitch and irregular AMR that were affected in TD group as well. An abnormal vocal tremor was present in only 10% of PD patients, with no differences between the PD phenotypes. We found a correlation between non-motor symptom severity and speech timing (r = - 0.40, p = 0.009). The present study demonstrates that speech disorder reflects the underlying motor phenotypes. Vocal tremor appeared to be an isolated phenomenon that does not share similar pathophysiology with limb tremor.

Center for Neurodegenerative Diseases Department of Medicine Surgery and Dentistry Scuola Medica Salernitana University of Salerno Salerno Italy

Department of Circuit Theory Faculty of Electrical Engineering Czech Technical University Prague Prague Czech Republic

Department of Computing and Control Engineering Faculty of Chemical Engineering University of Chemistry and Technology Prague Czech Republic

Department of Neurology and Centre of Clinical Neuroscience 1st Faculty of Medicine Charles University Prague Czech Republic

Zobrazit více v PubMed

Beltrami D, Gagliardi G, Rossini Favretti R, Ghidoni E, Tamburini F, Calza L (2018) Speech analysis by natural language processing techniques: a possible tool for very early detection of cognitive decline? Front Aging Neurosci 10:369. https://doi.org/10.3389/fnagi.2018.00369 PubMed DOI PMC

Burk BR, Watts CR (2019) The effect of Parkinson disease tremor phenotype on cepstral peak prominence and transglottal airflow in vowels and speech. J Voice 33(4):580.e11–580.e19. https://doi.org/10.1016/j.jvoice.2018.01.016 DOI

Cantiniaux S, Vaugoyeau M, Robert D, Horrelou-Pitek C, Mancini J, Witjas T, Azulay JP (2010) Comparative analysis of gait and speech in Parkinson's disease: hypokinetic or dysrhythmic disorders? J Neurol Neurosurg Psychiatry 166:158–167. https://doi.org/10.1136/jnnp.2009.174375 DOI

Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P, Ondo W, Abe K, Macphee G, Macmahon D, Barone P, Rabey M, Forbes A, Breen K, Tluk S, Naidu Y, Olanow W, Williams AJ, Thomas S, Rye D, Tsuboi Y, Hand A, Schapira AH (2007) The metric properties of a novel non-motor symptoms scale for Parkinson's disease: results from an international pilot study. Mov Disord 22:1901–1911. https://doi.org/10.1002/mds.21596 PubMed DOI

Choi SM, Kim BC, Cho BH, Kang KW, Choi KH, Kim JT, Lee SH, Park MS, Kim MK, Cho KH (2018) Comparison of two motor subtype classifications in de novo Parkinson's disease. Parkinsonism Relat Disord 54:74–78. https://doi.org/10.1016/j.parkreldis.2018.04.021 PubMed DOI

Defazio G, Guerrieri M, Liuzzi D, Gigante AF, di Nicola V (2016) Assessment of voice and speech symptoms in early Parkinson's disease by the Robertson dysarthria profile. Neurol Sci 37:443–449. https://doi.org/10.1007/s10072-015-2422-8 PubMed DOI

Duffy JR (2020) Motor speech disorders: substrates, differential diagnosis and management, 4th edn. Mosby, St. Louis

Fereshtehnejad SM, Zeighami Y, Dagher A, Postuma RB (2017) Clinical criteria for subtyping Parkinson's disease: biomarkers and longitudinal progression. Brain 140:1959–1976. https://doi.org/10.1093/brain/awx118 PubMed DOI

Gillivan-Murphy P, Miller N, Carding P (2019) Voice tremor in Parkinson's disease: an acoustic study. J Voice 33:526–535. https://doi.org/10.1016/j.jvoice.2017.12.010 PubMed DOI

Goberman AM (2005) Correlation between acoustic speech characteristics and non-speech motor performance in Parkinson disease. Med Sci Monit 11:109–116

Hariz GM, Forsgren L (2010) Activities of daily living and quality of life in persons with newly diagnosed Parkinson's disease according to subtype of disease, and in comparison to healthy controls. Acta Neurol Scand 123:20–27. https://doi.org/10.1111/j.1600-0404.2010.01344.x DOI

Hlavnicka J (2018) Automated analysis of speech disorders in neurodegenerative diseases. Ph.D. Thesis, Faculty of Electrical Engineering, Czech Technical University, Prague, Czechia

Hlavnicka J, Tykalova T, Ulmanova O, Dusek P, Horakova D, Ruzicka E, Klempir J, Rusz J (2020) Characterizing vocal tremor in progressive neurological diseases via automated acoustic analyses. Clin Neurophysiol 131:1155–1165. https://doi.org/10.1016/j.clinph.2020.02.005 PubMed DOI

Ho AK, Iansek R, Marigliani C, Bradshaw JL, Gates S (1998) Speech impairment in a large sample of patients with Parkinson's disease. Behav Neurol 11:131–137 DOI

Huang X, Ng SY, Chia NS, Setiawan F, Tay KY, Au WL, Tan EK, Tan LC (2019) Non-motor symptoms in early Parkinson's disease with different motor subtypes and their associations with quality of life. Eur J Neurol 26(3):400–406. https://doi.org/10.1111/ene.13803 PubMed DOI

Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosur Psychiatry 55:181–184. https://doi.org/10.1136/jnnp.55.3.181 DOI

Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I et al (1990) Variable expression of Parkinson's disease: a base-line analysis of the DATATOP cohort. Neurology 40:1529–1534. https://doi.org/10.1212/WNL.40.10.1529 PubMed DOI

Midi I, Dogan M, Koseoglu M, Can G, Sehitoglu MA, Gunal DI (2008) Voice abnormalities and their relation with motor dysfunction in Parkinson's disease. Acta Neurol Scand 117:26–34. https://doi.org/10.1111/j.1600-0404.2007.00965.x PubMed DOI

Mohl B, Berman BD, Shelton E, Tanabe J (2017) Levodopa response differs in Parkinson's motor subtypes: a task-based effective connectivity study. J Comp Neurol 525:2192–2201. https://doi.org/10.1002/cne.24197 PubMed DOI PMC

Moreau C, Ozsancak C, Blatt JL, Derambure P, Destee A, Defebvre L (2007) Oral festination in Parkinson's disease: biochemical analysis and correlation within festination and freezing of gait. Mov Disord 22:1503–1506. https://doi.org/10.1002/mds.21549 PubMed DOI

Novotny M, Dusek P, Daly I, Ruzicka E, Rusz J (2020) Glottal source analysis of voice deficits in newly diagnosed drug-naïve patients with Parkinson's disease: correlation between acoustic speech characteristics and non-speech motor performance. Biomed Sig Process Control 57:101818. https://doi.org/10.1016/j.bspc.2019.101818 DOI

Park HK, Yoo JY, Kwon M, Lee JH, Lee SJ, Kim SR, Kim MJ, Lee MC, Lee SM, Chung SJ (2014) Gait freezing and speech disturbance in Parkinson's disease. Neurol Sci 35:357–363. https://doi.org/10.1007/s10072-013-1519-1 PubMed DOI

Polychronis S, Niccolini F, Pagano G, Yousaf T, Politis M (2019) Speech difficulties in early de novo patients with Parkinson's disease. Parkinsonism Relat Disord 64:256–261. https://doi.org/10.1016/j.parkreldis.2019.04.026 PubMed DOI

Rektorova I, Mekyska J, Janousova E, Kostalova M, Eliasova I, Mrackova M, Berankova D, Necasova T, Smekal Z, Marecek R (2016) Speech prosody impairment predicts cognitive decline in Parkinson's disease. Parkinsonism Relat Disord 29:90–95. https://doi.org/10.1016/j.parkreldis.2016.05.018 . (Epub 2016 May 20) PubMed DOI

Roark B, Mitchell M, Hosom JP, Hollingshead K, Kaye JA (2011) Spoken language derived measures for detecting Mild Cognitive Impairment. IEEE Trans Audio Speech Lang Processing 19:2081–2090. https://doi.org/10.1109/TASL.2011.2112351 DOI PMC

Rusz J, Cmejla R, Ruzickova H, Ruzicka E (2011) Quantitative acoustic measurements for characterization of speech and voice disorders in early untreated Parkinson's disease. J Acoust Soc Am 129:350–367. https://doi.org/10.1121/1.3514381 PubMed DOI

Rusz J, Tykalova T, Cmejla R, Klempir J, Ruzicka E (2016) Effects of dopaminergic replacement therapy on motor speech disorders in Parkinson's disease: a longitudinal follow-up study on previously untreated patients. J Neural Transm 123:379–387. https://doi.org/10.1007/s00702-016-1515-8 PubMed DOI

Rusz J, Tykalova T, Krupicka R, Zarubova K, Novotny M, Jech R, Szabo Z, Ruzicka E (2017) Comparative analysis of speech impairment and upper limb motor dysfunction in Parkinson's disease. J Neural Transm 124:463–470. https://doi.org/10.1007/s00702-016-1662-y PubMed DOI

Rusz J, Tykalova T, Salerno G, Bancone S, Scarpelli J, Pellecchia MT (2019) Distinctive speech signature in cerebellar and parkinsonian subtypes of multiple system atrophy. J Neurol 266:1394–1404. https://doi.org/10.1007/s00415-019-09271-7 PubMed DOI

Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson's disease. Brain 132:2947–2957. https://doi.org/10.1093/brain/awp234 PubMed DOI

Simuni T, Caspell-Garcia C, Coffey C, Lasch S, Tanner C, Marek K (2016) How stable are Parkinson's disease subtypes in de novo patients: analysis of the PPMI cohort? Parkinsonism Relat Disord 28:62–67. https://doi.org/10.1016/j.parkreldis.2016.04.027 PubMed DOI

Skodda S, Visser W, Schlegel U (2011) Gender related patterns of dysprosody in Parkinson's disease and correlation between speech variables and motor symptoms. J Voice 25:76–82. https://doi.org/10.1016/j.jvoice.2009.07.005 PubMed DOI

Skodda S, Gronheit W, Schlegel U (2012) Impairment of vowel articulation as a possible marker of disease progression in Parkinson's disease. PLoS ONE 7:e32132. https://doi.org/10.1371/journal.pone.0032132 PubMed DOI PMC

Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson's disease rating scale: comparison with the unified Parkinson's disease rating scale. Mov Disord 28:668–670. https://doi.org/10.1002/mds.25383 PubMed DOI

Stewart C, Winfield L, Hunt A, Bressman SB, Fahn S, Blitzer A, Brin MF (1995) Speech dysfunction in early Parkinson's disease. Mov Disord 10:562–565. https://doi.org/10.1002/mds.870100506 PubMed DOI

Thenganatt MA, Jankovic J (2014) Parkinson disease subtypes. JAMA Neurol 71:499–504. https://doi.org/10.1001/jamaneurol.2013.6233 PubMed DOI

Wu Y, Guo XY, Wei QQ, Ou RW, Song W, Cao B, Zhao B, Shang HF (2015) Non-motor symptoms and quality of life in tremor dominant vs postural instability gait disorder Parkinson′s disease patients. Acta Neurol Scand 133:330–337. https://doi.org/10.1111/ane.12461 PubMed DOI

Yair E, Gath I (1988) On the use of pitch power spectrum in the evaluation of vocal tremor. Proc IEEE 76:1166–1175. https://doi.org/10.1109/5.9662 DOI

Zarzur A, Duarte I, Holanda GD, Martins MAUR (2010) Laryngeal electromyography and acoustic voice analysis in Parkinson's disease: a comparative status. Braz J Otorhinol 76:40–43. https://doi.org/10.1590/S1808-86942010000100008 DOI

Speech and gait abnormalities in motor subtypes of de-novo Parkinson's disease

Distinct patterns of speech disorder in early-onset and late-onset de-novo Parkinson's disease