Journal of Neurology

, Volume 262, Issue 4, pp 992–1001 | Cite as

Speech disorders reflect differing pathophysiology in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy

  • Jan Rusz
  • Cecilia Bonnet
  • Jiří Klempíř
  • Tereza Tykalová
  • Eva Baborová
  • Michal Novotný
  • Aaron Rulseh
  • Evžen Růžička
Original Communication

Abstract

Although speech disorder is frequently an early and prominent clinical feature of Parkinson’s disease (PD) as well as atypical parkinsonian syndromes (APS) such as progressive supranuclear palsy (PSP) and multiple system atrophy (MSA), there is a lack of objective and quantitative evidence to verify whether any specific speech characteristics allow differentiation between PD, PSP and MSA. Speech samples were acquired from 77 subjects including 15 PD, 12 PSP, 13 MSA and 37 healthy controls. The accurate differential diagnosis of dysarthria subtypes was based on the quantitative acoustic analysis of 16 speech dimensions. Dysarthria was uniformly present in all parkinsonian patients but was more severe in PSP and MSA than in PD. Whilst PD speakers manifested pure hypokinetic dysarthria, ataxic components were more affected in MSA whilst PSP subjects demonstrated severe deficits in hypokinetic and spastic elements of dysarthria. Dysarthria in PSP was dominated by increased dysfluency, decreased slow rate, inappropriate silences, deficits in vowel articulation and harsh voice quality whereas MSA by pitch fluctuations, excess intensity variations, prolonged phonemes, vocal tremor and strained-strangled voice quality. Objective speech measurements were able to discriminate between APS and PD with 95 % accuracy and between PSP and MSA with 75 % accuracy. Dysarthria severity in APS was related to overall disease severity (r = 0.54, p = 0.006). Dysarthria with various combinations of hypokinetic, spastic and ataxic components reflects differing pathophysiology in PD, PSP and MSA. Thus, motor speech examination may provide useful information in the evaluation of these diseases with similar manifestations.

Keywords

Parkinson’s disease Atypical parkinsonism Dysarthria Speech disorder Acoustic analyses 

Supplementary material

415_2015_7671_MOESM1_ESM.pdf (56 kb)
Supplementary material 1 (PDF 55 kb)

References

  1. 1.
    Schrag A, Ben-Shlomo Y, Quinn NP (1999) Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study. Lancet 354:1771–1775CrossRefPubMedGoogle Scholar
  2. 2.
    Wenning GK, Litvan I, Tolosa E (2011) Milestones in atypical and secondary Parkinsonisms. Mov Disord 26:1083–1095CrossRefPubMedGoogle Scholar
  3. 3.
    Berti V, Pupi A, Monsconi L (2011) PET/CT in diagnosis of movement disorders. Ann N Y Acad Sci 1228:93–108PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Tang CC, Poston KL, Eckert T, Feigin A, Frucht S et al (2010) Differential diagnosis of parkinsonism: a metabolic imaging study using pattern analysis. Lancet Neurol 9:149–158CrossRefPubMedGoogle Scholar
  5. 5.
    Rusz J, Cmejla R, Ruzickova H, Klempir J, Majerova V et al (2011) Acoustic assessment of voice and speech disorders in Parkinson’s disease through quick vocal test. Mov Disord 26:1951–1952CrossRefPubMedGoogle Scholar
  6. 6.
    Ho AK, Iansek R, Marigliani C, Bradshaw J, Gates S (1998) Speech impairment in large sample of patients with Parkinson’s disease. Behav Neurol 11:131–137CrossRefPubMedGoogle Scholar
  7. 7.
    Kluin KJ, Foster NL, Berent S, Gilman S (1993) Perceptual analysis of speech disorders in progressive supranuclear palsy. Neurology 43:563–566CrossRefPubMedGoogle Scholar
  8. 8.
    Kluin KJ, Gilman S, Lohman M, Junck L (1996) Characteristics of the dysarthria in multiple system atrophy. Arch Neurol 53:545–548CrossRefPubMedGoogle Scholar
  9. 9.
    Kim Y, Kent RD, Kent J, Duffy JR (2010) Perceptual and acoustic features of dysarthria associated with multiple system atrophy. J Med Speech Lang Pathol 18:66–70Google Scholar
  10. 10.
    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 129:350–369CrossRefPubMedGoogle Scholar
  11. 11.
    Rusz J, Cmejla R, Tykalova T, Ruzickova H, Klempir J et al (2013) Imprecise vowel articulation as a potential early marker of Parkinson’s disease: effect of speaking task. J Acoust Soc Am 134:2171–2181CrossRefPubMedGoogle Scholar
  12. 12.
    Rusz J, Megrelishvili M, Bonnet C, Okujava M, Brozova H et al (2014) A distinct variant of mixed dysarthria reflects parkinsonism and dystonia due to ephedrone abuse. J Neural Transm 121:655–664CrossRefPubMedGoogle Scholar
  13. 13.
    Sachin S, Shukla G, Goyal V, Singh S, Aggarwal V et al (2008) Clinical speech impairment in Parkinson’s disease, progressive supranuclear palsy, and multiple system atrophy. Neurol India 56:122–126CrossRefPubMedGoogle Scholar
  14. 14.
    Skodda S, Visser W, Schlegel U (2011) Acoustical analysis of speech in progressive supranuclear palsy. J Voice 25:725–731CrossRefPubMedGoogle Scholar
  15. 15.
    Saxena M, Behari M, Kumaran SS, Goyal V, Narang V (2014) Assessing speech dysfunction using BOLD and acoustic analysis in parkinsonism. Parkinsonism Relat D 20:855–861CrossRefGoogle Scholar
  16. 16.
    Litvan I, Agid Y, Calne D, Campbell G, Dubois B et al (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSS international workshop. Neurology 47:1–9CrossRefPubMedGoogle Scholar
  17. 17.
    Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ et al (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    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 Neurosurg Psychiatry 55:181–184PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Payan CA, Viallet F, Landwerhrmeyer BG, Bonnet AM, Borg M et al (2011) Disease severity and progression in progressive supranuclear palsy and multiple system atrophy: validation of the NNIPPS-Parkinson plus scale. PLoS One 6:e22293PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Duffy JR (2013) Motor Speech Disorders: Substrates, Differential Diagnosis and Management, 3rd edn. Mosby, St. LouisGoogle Scholar
  21. 21.
    Darley FL, Aronson AE, Brown JR (1969) Differential diagnostic patterns of dysarthria. J Speech Hear Res 12:246–269CrossRefPubMedGoogle Scholar
  22. 22.
    Novotny M, Rusz J, Cmejla R, Ruzicka E (2014) Automatic evaluation of articulatory disorders in Parkinson’s disease. IEEE/ACM T Audio Speech Lang Process 22:1366–1378CrossRefGoogle Scholar
  23. 23.
    Hartelius L, Gustavsson H, Astrand M, Holmberg B (2006) Perceptual analysis of speech in multiple system atrophy and progressive supranuclear palsy. J Med Speech Lang Pathol 14:241–247Google Scholar
  24. 24.
    Liss JM, Spitzer SM, Caviness JN, Adler C (2002) The effect of familiarization on intelligibility and lexical segmentation in hypokinetic and ataxic dysarthria. J Acoust Soc Am 112:3022–3030PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Benke T, Hohenstein C, Poewe W, Butterworth B (2000) Repetitive speech phenomena in Parkinson’s disease. J Neurol Neurosurg Psychiatry 69:319–325PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
    Nath U, Ben-Shlomo Y, Thomson RG, Lees AJ, Burn DJ (2003) Clinical features and natural history of progressive supranuclear palsy: a clinical cohort study. Neurology 69:910–916CrossRefGoogle Scholar
  27. 27.
    Nebel A, Reese R, Deuschl G, Mehdorn HM, Volkmann J (2009) Acquired stuttering after pallidal deep brain stimulation for dystonia. J Neural Transm 116:167–169CrossRefPubMedGoogle Scholar
  28. 28.
    Neef NE, Hoang TNL, Neef A, Paulus W, Sommer M (2015) Speech dynamics are coded in the left motor cortex in fluent speakers but not in adults who stutter. Brain. doi:10.1093/brain/awu390 (in press)
  29. 29.
    Tykalova T, Rusz J, Cmejla R, Klempir J, Ruzickova H, et al (2015) Effect of dopaminergic medication on speech dysfluency in Parkinson’s disease: a longitudinal study. J Neural Transm: in press. doi:10.1007/s00702-015-1363-y
  30. 30.
    Louis ED, Winfield L, Fahn S, Ford B (2001) Speech dysfluency exacerbated by levodopa in Parkinson’s disease. Mov Disord 16:562–565CrossRefPubMedGoogle Scholar
  31. 31.
    Ostock CY, Dupre KB, Jaunarajs KL, Walters H, George J et al (2011) Role of the primary motor cortex in L-Dopa-induced dyskinesia and its modulation by 5-HT1A receptor stimulation. Neuropharmacology 61:753–760PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Rusz J, Klempir J, Tykalova T, Baborova E, Cmejla R et al (2014) Characteristics and occurrence of speech impairment in Huntington’s disease: possible influence of antipsychotic medication. J Neural Transm 121:655–664CrossRefPubMedGoogle Scholar
  33. 33.
    Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ et al (2001) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71:670–676CrossRefGoogle Scholar
  34. 34.
    Kluin KJ, Gilman S, Foster NL, Sima AAF, D’Amato CJ et al (2001) Neuropathological correlates of dysarthria in progressive supranuclear palsy. Arch Neurol 58:265–269CrossRefPubMedGoogle Scholar
  35. 35.
    Prodoehl J, Li H, Planetta JP, Goetz CG, Shannon KM, Tangonan R et al (2013) Diffusion Tensor Imaging of Parkinson’s disease, atypical parkinsonism, and essential tremor. Mov Disord 28:1816–1822CrossRefPubMedGoogle Scholar
  36. 36.
    Nakleh MK, Badarny S, Winer R, Jeries R, Finberg J, Haick H. (2015) Distinguishing idiopathic Parkinson’s disease from other parkinsonian syndromes by breath test. Parkinsonism Relat D. doi:10.1016/j.parkreldis.2014.11.023 (in press)
  37. 37.
    Ho AK, Bradshaw R, Iansek R (2008) For better or worse: the effect of levodopa on speech in Parkinson’s disease. Mov Disord 23:575–580CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jan Rusz
    • 1
    • 2
  • Cecilia Bonnet
    • 2
    • 3
  • Jiří Klempíř
    • 2
    • 4
  • Tereza Tykalová
    • 1
  • Eva Baborová
    • 2
  • Michal Novotný
    • 1
  • Aaron Rulseh
    • 5
    • 6
  • Evžen Růžička
    • 2
  1. 1.Department of Circuit Theory, Faculty of Electrical EngineeringCzech Technical University in PraguePrague 6Czech Republic
  2. 2.Department of Neurology and Centre of Clinical Neuroscience, First Faculty of MedicineCharles University in PraguePrague 2Czech Republic
  3. 3.AP HP, Neurology DepartmentPitié Salpêtrière HospitalParisFrance
  4. 4.Institute of Anatomy, 1st Faculty of MedicineCharles UniversityPrague 2Czech Republic
  5. 5.Department of RadiologyNa Homolce HospitalPragueCzech Republic
  6. 6.Department of Radiology, 1st Faculty of Medicine and General University HospitalCharles UniversityPragueCzech Republic

Personalised recommendations