Skip to main content
Log in

Voice features of Parkinson’s disease patients with subthalamic nucleus deep brain stimulation

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Voice and speech disorders are one of the most important issues after subthalamic nucleus deep brain stimulation (STN-DBS) in Parkinson’s disease patients; however, their characteristics remain unclear. We performed a comprehensive voice evaluation including the multi-dimensional voice program for acoustic analysis, the GRBAS scale for perceptual analysis, and the evaluation of the voice handicap index (VHI) for psychosocial analysis. In total, 68 patients who had undergone STN-DBS (37 assessed in the on- and off-stimulation conditions) and 40 who had been treated with medical therapy alone were evaluated. Further, we performed laryngoscopic examinations in 13 STN-DBS and 19 medical-therapy-alone patients. The STN-DBS group, especially females, showed widespread impairment of voice parameters and significantly poorer VHI scores than the medical-therapy-alone group. The degree of voiceless (DUV) and strained voice were the most impaired factors in the STN-DBS group; and DUV significantly improved after stopping stimulation. Furthermore strained voice, breathiness, and asthenia improved after stopping stimulation. Laryngoscopic examination showed that abnormal laryngeal muscle contraction and incomplete glottal closure were more prominent in the STN-DBS group than in the medical-therapy-alone group. We demonstrated that (1) more widespread voice impairment in females, (2) poorer voice-related QOL, (3) worse DUV and strained voice, and (4) abnormal laryngeal muscle contraction were the characteristic voice and laryngeal findings in the STN-DBS group compared with those in the medical-therapy-alone group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

F 0 :

Average fundamental frequency

Jitt:

Jitter percent

Shim:

Shimmer percent

NHR:

Noise-to-harmonic Ratio

FTRI:

F 0-tremor intensity index

ATRI:

Amplitude tremor intensity index

DSH:

Degree of subharmonic segments

DUV:

Degree of voiceless

References

  1. Appleby BS, Duggan PS, Regenberg A, Rabins PV (2007) Psychiatric and neuropsychiatric adverse events associated with deep brain stimulation: a meta-analysis of ten years’ experience. Mov Disord 22:1722–1728

    Article  PubMed  Google Scholar 

  2. Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, Lang AE et al (2006) Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord 21:290–304

    Article  Google Scholar 

  3. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE et al (1995) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345:91–95

    Article  CAS  PubMed  Google Scholar 

  4. Schuepbach WM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, Hälbig TD et al (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368:610–622

    Article  CAS  PubMed  Google Scholar 

  5. Espay AJ, Vaughan JE, Marras C, Fowler R, Eckman MH (2010) Early versus delayed bilateral subthalamic deep brain stimulation for parkinson’s disease: a decision analysis. Mov Disord 25:1456–1463

    Article  PubMed  Google Scholar 

  6. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A et al (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934

    Article  CAS  PubMed  Google Scholar 

  7. Gervais-Bernard H, Xie-Brustolin J, Mertens P, Polo G, Klinger H, Adamec D, Broussolle E et al (2009) Bilateral subthalamic nucleus stimulation in advanced Parkinson’s disease: five year follow-up. J Neurol 256:225–233

    Article  PubMed  Google Scholar 

  8. Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto JL, Pollak P, Rehncrona S, Kulisevsky J et al (2005) Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 128:2240–2249

    Article  CAS  PubMed  Google Scholar 

  9. Gan J, Xie-Brustolin J, Mertens P, Polo G, Klinger H, Mollion H, Benatru I et al (2007) Bilateral subthalamic nucleus stimulation in advanced Parkinson’s disease: three years follow-up. J Neurol 254:99–106

    Article  PubMed  Google Scholar 

  10. Van Lancker Sidtis D, Rogers T, Godier V, Tagliati M, Sidtis JJ (2010) Voice and fluency changes as a function of speech task and deep brain stimulation. J Speech Lang Hear Res 53:1167–1177

    Article  Google Scholar 

  11. Frost E, Tripoliti E, Hariz MI, Pring T, Limousin P (2010) Self-perception of speech changes in patients with Parkinson’s disease following deep brain stimulation of the subthalamic nucleus. Int J Speech Lang Pathol 12:399–404

    Article  PubMed  Google Scholar 

  12. Tsuboi T, Watanabe H, Tanaka Y, Ohdake R, Yoneyama N, Hara K, Nakamura R, Watanabe H, Senda J, Atsuta N, Ito M, Hirayama M, Yamamoto M, Fujimoto Y, Kajita Y, Wakabayashi T, Sobue G (2015) Distinct phenotypes of speech and voice disorders in Parkinson’s disease after subthalamic nucleus deep brain stimulation. J Neurol Neurosurg Psychiatry (in press)

  13. Valálik I, Smehák G, Bognár L, Csókay A (2011) Voice acoustic changes during bilateral subthalamic stimulation in patients with Parkinson’s disease. Clin Neurol Neurosurg 113:188–195

    Article  PubMed  Google Scholar 

  14. Hughes AJ, Ben-Shlomo Y, Daniel SE, Lees AJ (1992) What features improve the accuracy of clinical diagnosis in Parkinson’s disease: a clinicopathologic study. Neurology 42:1142–1146

    Article  CAS  PubMed  Google Scholar 

  15. Klostermann F, Ehlen F, Vesper J, Nubel K, Gross M, Marzinzik F, Curio G et al (2008) Effects of subthalamic deep brain stimulation on dysarthrophonia in Parkinson’s disease. J Neurol Neurosurg Psychiatry 79:522–529

    Article  CAS  PubMed  Google Scholar 

  16. Hoffman-Ruddy B, Schulz G, Vitek J, Evatt M (2001) A preliminary study of the effects of sub thalamic nucleus (STN) deep brain stimulation (DBS) on voice and speech characteristics in Parkinson’s Disease (PD). Clin Linguist Phon 15:97–101

    Article  CAS  PubMed  Google Scholar 

  17. D’Alatri L, Paludetti G, Contarino MF, Galla S, Marchese MR, Bentivoglio AR (2008) Effects of bilateral subthalamic nucleus stimulation and medication on parkinsonian speech impairment. J Voice 22:365–372

    Article  PubMed  Google Scholar 

  18. Mate MA, Cobeta I, Jiménez-Jiménez FJ, Figueiras R (2012) Digital voice analysis in patients with advanced Parkinson’s disease undergoing deep brain stimulation therapy. J Voice 26:496–501

    Article  PubMed  Google Scholar 

  19. Xie Y, Zhang Y, Zheng Z, Liu A, Wang X, Zhuang P, Lo Y et al (2011) Changes in speech characters of patients with Parkinson’s disease after bilateral subthalamic nucleus stimulation. J Voice 25:751–758

    Article  PubMed  Google Scholar 

  20. Dromey C, Bjarnason S (2011) A preliminary report on disordered speech with deep brain stimulation in individuals with Parkinson’s disease. Parkinsons Dis 2011:1–11

    Article  Google Scholar 

  21. Tanaka Y, Nishio M, Niimi S (2011) Vocal acoustic characteristics of patients with Parkinson’s disease. Folia Phoniatr Logop 63:223–230

    Article  PubMed  Google Scholar 

  22. Kent RD, Kent JF (2000) Task-based profiles of the dysarthrias. Folia Phoniatr Logop 52:48–53

    Article  CAS  PubMed  Google Scholar 

  23. Kent RD, Vorperian HK, Kent JF, Duffy JR (2003) Voice dysfunction in dysarthria: application of the multi-dimensional voice program. J Commun Disord 36:281–306

    Article  CAS  PubMed  Google Scholar 

  24. Midi I, Dogan M, Koseoglu M (2008) Voice abnormalities and their relation with motor dysfunction in Parkinson’s disease. Acta Neurol Scand 117:26–34

    CAS  PubMed  Google Scholar 

  25. Nishio M, Niimi S (2002) Multi-parametic analysis for normal voices using a multi-dimensional voice program. Sogo Rihabiriteshon 30:927–933

    Google Scholar 

  26. Kent RD, Weismer G, Kent JF, Vorperian HK, Duffy JR (1999) Acoustic studies of dysarthric speech: methods, progress, and potential. J Commun Disord 32:141–189

    Article  CAS  PubMed  Google Scholar 

  27. González J, Cervera T, Miralles JL (2002) Acoustic voice analysis: reliability of a set of multi-dimensional parameters. Acta Otorrinolaringol Esp 53:256–268

    Article  PubMed  Google Scholar 

  28. Carding PN, Steen IN, Webb A, Mackenzie K, Deary IJ, Wilson JA (2004) The reliability and sensitivity to change of acoustic measures of voice quality. Clin Otolaryngol Allied Sci 29:538–544

    Article  CAS  PubMed  Google Scholar 

  29. Deliyski D (1993) Acoustic model and evaluation of pathological voice production. In 3-rd Conference on Speech Commununication and Technology EUROSPEECH’93, pp 1969–1972

  30. Deliyski D, Gress C (1998) Inter-system reliability of MDVP for Windows95/98 and DOS. In ASHA’98, pp 1–5

  31. Natour Y, Cimino-Knight AM, Wingate J, Sapienza CM (2002) The consistency of the Kay Elemetrics Multidimensional Voice Program (MDVP) for the acoustic analysis of the dysphonic voice. Florida J Commun Disord 20:23–27

    Google Scholar 

  32. Lee VS, Zhou XP, Rahn D, Wang EQ, Jiang JJ (2008) Perturbation and nonlinear dynamic analysis of acoustic phonatory signal in Parkinsonian patients receiving deep brain stimulation. J Commun Disord 41:485–500

    Article  PubMed Central  PubMed  Google Scholar 

  33. Hirano M (1981) Clinical examination of voice. Springer, Berlin Heidelberg

    Google Scholar 

  34. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  35. Shiromoto O, Ikenaga E (2011) Reliability and validity of VHI (voice handicap index) and V-RQOL (Voice-related quality of life): Japanese versions. Japan J Logop Phoniatr 52:254–262

    Article  Google Scholar 

  36. Jacobson BH, Johnson A, Grywalski C, Silbergleit A, Jacobson G, Benninger MS, Newman CW (1997) The voice handicap index (VHI) development and validation. AM J Speech Lang Pat 6:66–70

    Article  Google Scholar 

  37. Smith ME, Ramig LO, Dromey C, Perez KS, Samandari R (1995) Intensive voice treatment in Parkinson disease: Laryngostroboscopic findings. J Voice 9:453–459

    Article  CAS  PubMed  Google Scholar 

  38. Kay Pentax (2008) Software instruction manual: multi-dimensional voice program (MDVP), p 139

  39. Deliyski D, Zielinski T (1989) Objective diagnosis of laryngeal pathology using the Wigner–Ville distribution. In: 12° Colloque sur le traitement du signal et des images, FRA. GRETSI, Groupe d’Etudes du Trait. du Signal des Image, pp 973–976

  40. Amir O, Wolf M, Amir N (2009) A clinical comparison between two acoustic analysis softwares: MDVP and Praat. Biomed Signal Process Control 4:202–205

    Article  Google Scholar 

  41. Manfredi C, Cantarella G, Migali N, Berlusconi A, Maraschi B (1996) Assessing the effectiveness of botulinus treatment in spasmodic dysphonia. Measurements 117:219–224

    Google Scholar 

  42. Velasco García MJ, Cobeta I, Martín G, Alonso-Navarro H, Jimenez-Jimenez FJ (2011) Acoustic analysis of voice in Huntington’s disease patients. J Voice 25:208–217

    Article  PubMed  Google Scholar 

  43. Ramig LA (1985) Acoustic analyses of phonation in patients with Huntington’s disease. Preliminary report. Ann Otol Rhinol Laryngol 95:288–293

    Article  Google Scholar 

  44. Tanaka S, Banno H, Katsuno M, Suzuki K, Suga N, Hashizume A, Mano T et al (2014) Distinct acoustic features in spinal and bulbar muscular atrophy patients with laryngospasm. J Neurol Sci 337:193–200

    Article  PubMed  Google Scholar 

  45. Linville SE (1996) The sound of senescence. J Voice 10:190–200

    Article  CAS  PubMed  Google Scholar 

  46. Böhme G, Hecker G (1970) Gerontological studies on vocal range and vocal register. Folia Phoniatr (Basel) 22:176–184

    Article  Google Scholar 

  47. Mysak ED (1959) Pitch and duration characteristics of older males. J Speech Hear Res 2:46–54

    Article  CAS  PubMed  Google Scholar 

  48. Nishio M, Tanaka Y, Niimi S (2011) Analysis of age-related changes in the acoustic characteristics of voice. J Commun Res 2:1

    Google Scholar 

  49. Honjo I, Isshiki N (1980) Laryngoscopic and voice characteristics of aged persons. Arch Otolaryngol 106:149–150

    Article  CAS  PubMed  Google Scholar 

  50. Mueller PB, Sweeney RJ, Baribeau LJ (1984) Acoustic and morphologic study of the senescent voice. Ear Nose Throat J 63:292–295

    CAS  PubMed  Google Scholar 

  51. Hollien H (1987) “Old voices”: What do we really know about them? J Voice 1:2–17

    Article  Google Scholar 

  52. Tommasi G, Krack P, Fraix V, Le Bas JF, Chabardes S, Benabid AL, Pollak P (2008) Pyramidal tract side effects induced by deep brain stimulation of the subthalamic nucleus. J Neurol Neurosurg Psychiatry 79:813–819

    Article  CAS  PubMed  Google Scholar 

  53. Weiss D, Wächter T, Breit S, Jacob SN, Pomper JK, Asmus F, Valls-Solé J et al (2010) Involuntary eyelid closure after STN-DBS: evidence for different pathophysiological entities. J Neurol Neurosurg Psychiatry 81:1002–1007

    Article  PubMed  Google Scholar 

  54. Pollo C, Kaelin-Lang A, Oertel MF, Stieglitz L, Taub E, Fuhr P, Lozano AM et al (2014) Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain 137:2015–2026

    Article  PubMed  Google Scholar 

  55. Yim SH, Kim JH, Han ZA, Jeon S, Cho JH, Kim GS, Choi SA et al (2013) Distribution of the corticobulbar tract in the internal capsule. J Neurol Sci 334:63–68

    Article  PubMed  Google Scholar 

  56. Tommasi G, Krack P, Fraix V, Le Bas JF, Chabardes S, Benabid AL, Pollak P (2008) Pyramidal tract side effects induced by deep brain stimulation of thesubthalamic nucleus. J Neurol Neurosurg Psychiatry 79:813–819

    Article  CAS  PubMed  Google Scholar 

  57. Åström M, Tripoliti E, Hariz MI, Zrinzo LU, Martinez-Torres I, Limousin P, Wårdell K (2010) Patient-Specific Model-Based Investigation of Speech Intelligibility and Movement during Deep Brain Stimulation. Stereotact Funct Neurosurg 88:224–233

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Conflicts of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gen Sobue.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tanaka, Y., Tsuboi, T., Watanabe, H. et al. Voice features of Parkinson’s disease patients with subthalamic nucleus deep brain stimulation. J Neurol 262, 1173–1181 (2015). https://doi.org/10.1007/s00415-015-7681-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-015-7681-z

Keywords

Navigation