Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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)
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
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
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
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
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
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
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
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
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
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
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
Thenganatt MA, Jankovic J (2014) Parkinson disease subtypes. JAMA Neurol 71:499–504. https://doi.org/10.1001/jamaneurol.2013.6233
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
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
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
Acknowledgements
The authors thank the participants for their time and interest in the study. This study was supported by the Ministry of Health of the Czech Republic, Grant No. NV19-04-00120, OP VVV MEYS project “Research Centre for Informatics” (Grant No. CZ.02.1.01/0.0/0.0/16_019/0000765), and by the Czech Ministry of Education (PROGRES-Q27/LF1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors report no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tykalová, T., Rusz, J., Švihlík, J. et al. Speech disorder and vocal tremor in postural instability/gait difficulty and tremor dominant subtypes of Parkinson’s disease. J Neural Transm 127, 1295–1304 (2020). https://doi.org/10.1007/s00702-020-02229-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-020-02229-4