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Characteristic laryngoscopic findings in Parkinson’s disease patients after subthalamic nucleus deep brain stimulation and its correlation with voice disorder

  • Neurology and Preclinical Neurological Studies - Original Article
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Abstract

Speech and voice disorders are one of the most common adverse effects in Parkinson’s disease (PD) patients treated with subthalamic nucleus deep brain stimulation (STN-DBS). However, the pathophysiology of voice and laryngeal dysfunction after STN-DBS remains unclear. We assessed 47 PD patients (22 treated with bilateral STN-DBS (PD-DBS) and 25 treated medically (PD-Med); all patients in both groups matched by age, sex, disease duration, and motor and cognitive function) using the objective and subjective voice assessment batteries (GRBAS scale and Voice Handicap Index), and laryngoscopy. Laryngoscopic examinations revealed that PD-DBS patients showed a significantly higher incidence of incomplete glottal closure (77 vs 48 %; p = 0.039), hyperadduction of the false vocal folds (73 vs 44 %; p = 0.047), anteroposterior hypercompression (50 vs 20 %; p = 0.030) and asymmetrical glottal movement (50 vs 16 %; p = 0.002) than PD-Med patients. On- and off-stimulation assessment revealed that STN-DBS could induce or aggravate incomplete glottal closure, hyperadduction of the false vocal folds, anteroposterior hypercompression, and asymmetrical glottal movement. Incomplete glottal closure and hyperadduction of the false vocal folds significantly correlated with breathiness and strained voice, respectively (r = 0.590 and 0.539). We should adjust patients’ DBS settings in consideration of voice and laryngeal functions as well as motor function.

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References

  • Burghaus L, Hilker R, Thiel A, Galldiks N, Lehnhardt FG, Zaro-Weber O et al (2006) Deep brain stimulation of the subthalamic nucleus reversibly deteriorates stuttering in advanced Parkinson’s disease. J Neural Transm 113:625–631

    Article  CAS  PubMed  Google Scholar 

  • Darley FL, Aronson AE, Brown JR (1969) Differential diagnostic patterns of dysarthria. J Speech Hear Res 12:246–269

    Article  CAS  PubMed  Google Scholar 

  • Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K et al (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355:896–908

    Article  CAS  PubMed  Google Scholar 

  • Dromey C, Bjarnason S (2011) A preliminary report on disordered speech with deep brain stimulation in individuals with Parkinson’s disease. Parkinsons Dis 2011:796205

    PubMed Central  PubMed  Google Scholar 

  • Dromey C, Kumar R, Lang AE, Lozano AM (2000) An investigation of the effects of subthalamic nucleus stimulation on acoustic measures of voice. Mov Disord 15:1132–1138

    Article  CAS  PubMed  Google Scholar 

  • Fytagoridis A, Åström M, Wårdell K, Blomstedt P (2013) Stimulation-induced side effects in the posterior subthalamic area: distribution, characteristics and visualization. Clin Neurol Neurosurg 115:65–71

    Article  CAS  PubMed  Google Scholar 

  • Gallena S, Smith PJ, Zeffiro T, Ludlow CL (2001) Effects of levodopa on laryngeal and offset in Parkinson disease. J Speech Lang Hear Res 44:1284–1299

    Article  CAS  PubMed  Google Scholar 

  • Gamboa J, Jimnez-jimnez J, Nieto A, Montojo J, Molina A, Cobeta I (1997) Acoustic voice analysis in patients with Parkinson’s disease treated with dopaminergic drugs. J Voice 11:314–320

    Article  CAS  PubMed  Google Scholar 

  • Goberman AM, Blomgren M (2008) Fundamental Frequency change during offset and onset of voicing in individuals with Parkinson disease. J Voice 22:178–191

    Article  PubMed  Google Scholar 

  • Hanson DG, Gerratt BR, Ward PH (1984) Cinegraphic observations of laryngeal function in Parkinson’s disease. Laryngoscope 94:348–353

    Article  CAS  PubMed  Google Scholar 

  • Hirano M (1981) Clinical examination of voice. Springer-Verlag, New York

    Google Scholar 

  • 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 55:181–184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jacobson BH, Johnson A, Grywalski C, Silbergleit A, Jacobson G, Benninger MS (1997) The voice handicap index (VHI): development and validation. Am J Speech Lang Pathol 6:66–70

    Article  Google Scholar 

  • Karlsson F, Blomstedt P, Olofsson K, Linder J, Nordh E, van Doorn J (2012) Control of phonatory onset and offset in Parkinson patients following deep brain stimulation of the subthalamic nucleus and caudal zona incerta. Park Relat Disord 18:824–827

    Article  Google Scholar 

  • Klostermann F, Ehlen F, Vesper J, Nubel K, Gross M, Marzinzik F 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 

  • Lowell SY, Kelley RT, Awan SN, Colton RH, Chan NH (2012) Spectral- and cepstral-based acoustic features of dysphonic, strained voice quality. Ann Otol Rhinol Laryngol 121:539–548

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Moreau C, Pennel-Ployart O, Pinto S, Plachez A, Annic A, Viallet F et al (2011) Modulation of dysarthropneumophonia by low-frequency STN DBS in advanced Parkinson’s disease. Mov Disord 26:659–663

    Article  PubMed  Google Scholar 

  • Pinto S, Ozsancak C, Tripoliti E, Thobois S, Limousin-Dowsey P, Auzou P (2004) Treatments for dysarthria in Parkinson’s disease. Lancet Neurol 3:547–556

    Article  PubMed  Google Scholar 

  • Pinto S, Gentil M, Krack P, Sauleau P, Fraix V, Benabid AL et al (2005) Changes induced by levodopa and subthalamic nucleus stimulation on parkinsonian speech. Mov Disord 20:1507–1515

    Article  PubMed  Google Scholar 

  • Plaha P, Ben-Shlomo Y, Patel NK, Gill SS (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129:1732–1747

    Article  PubMed  Google Scholar 

  • Rehncrona S, Johnels B, Widner H, Törnqvist AL, Hariz M, Sydow O (2003) Long-term efficacy of thalamic deep brain stimulation for tremor: double-blind assessments. Mov Disord 18:163–170

    Article  PubMed  Google Scholar 

  • Reich MM, Steigerwald F, Sawalhe AD, Reese R, Gunalan K, Johannes S (2015) Short pulse width widens the therapeutic window of subthalamic neurostimulation. Ann Clin Transl Neurol 2:427–432

    Article  PubMed Central  PubMed  Google Scholar 

  • Schaltenbrand G, Wahren W (1977) Atlas for stereotaxy of the human brain, 2nd edn. Thieme, Stuttgart

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Skodda S, Grönheit W, Schlegel U, Südmeyer M, Schnitzler A, Wojtecki L (2014) Effect of subthalamic stimulation on voice and speech in Parkinson’s disease: for the better or worse? Front Neurol 4:218

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 

  • Steep C (2014) Relative fundamental frequency during vocal onset and offset in older speakers with and without Parkinson’s disease. J Acoust Soc Am 133:1637–1643

    Article  Google Scholar 

  • Tanaka Y, Tsuboi T, Watanabe H, Kajita Y, Fujimoto Y, Ohdake R et al (2015) Voice features of Parkinson’s disease patients with subthalamic nucleus deep brain stimulation. J Neurol 262:1173–1181

    Article  PubMed  Google Scholar 

  • Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653

    Article  PubMed  Google Scholar 

  • Tommasi G, Krack P, Fraix V, Le Bas JF, Chabardes S, Benabid AL et al (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 

  • Tripoliti E, Zrinzo L, Martinez-Torres I, Frost E, Pinto S, Foltynie T et al (2011a) Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology 76:80–86

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tripoliti E, Strong L, Hickey F, Foltynie T, Zrinzo L, Candelario J et al (2011b) Treatment of dysarthria following subthalamic nucleus deep brain stimulation for Parkinson’s disease. Mov Disord 26:2434–2436

    Article  PubMed Central  PubMed  Google Scholar 

  • Tripoliti E, Limousin P, Foltynie T, Candelario J, Aviles-Olmos I, Hariz MI et al (2014) Predictive factors of speech intelligibility following subthalamic nucleus stimulation in consecutive patients with Parkinson’s disease. Mov Disord 29:532–538

    Article  CAS  PubMed  Google Scholar 

  • Tsuboi T, Watanabe H, Tanaka Y, Ohdake R, Yoneyama N, Hara K, et al. (2015) Distinct phenotypes of speech and voice disorders in Parkinson’s disease after subthalamic nucleus deep brain stimulation. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp-2014-308043

    PubMed  Google Scholar 

  • Wertheimer J, Gottuso AY, Nuno M, Walton C, Duboille A, Tuchman M et al (2014) The impact of STN deep brain stimulation on speech in individuals with Parkinson’s disease: the patient’s perspective. Parkinsonism Relat Disord 20:1065–1070

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by Health and Labor Sciences Research grants for research on measures for intractable diseases and comprehensive research on aging and health from the Ministry of Health, Labor and Welfare, Japan. The authors would like to thank Enago (www.enago.jp) for the English language review.

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Authors and Affiliations

  1. Department of Neurology, Nagoya University Graduate School of Medicine, Showa-ku, Nagoya, 466-8550, Japan

    Takashi Tsuboi, Hirohisa Watanabe, Yasuhiro Tanaka, Reiko Ohdake, Noritaka Yoneyama, Kazuhiro Hara, Mizuki Ito, Masaaki Hirayama & Gen Sobue

  2. Faculty of Psychological and Physical Science, Aichi-Gakuin University, Aichi, 470-0195, Japan

    Masahiko Yamamoto

  3. Department of Otorhinolaryngology, Nagoya University Graduate School of Medicine, Nagoya, 466-8550, Japan

    Yasushi Fujimoto

  4. Department of Neurosurgery, Nagoya University Graduate School of Medicine, Nagoya, 466-8550, Japan

    Yasukazu Kajita & Toshihiko Wakabayashi

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  1. Takashi Tsuboi
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  2. Hirohisa Watanabe
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  3. Yasuhiro Tanaka
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  13. Gen Sobue
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Correspondence to Gen Sobue.

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Electronic supplementary material

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Segment 1. Patient 1 had moderate incomplete glottal closure, mild hyperadduction of the false vocal folds, and asymmetrical glottal movement in the on-stimulation condition. Thirty minutes after stopping stimulation, incomplete glottal closure was marginally ameliorated and asymmetrical glottal movement disappeared. (MP4 16520 kb)

Segment 2. Patient 2 had moderate incomplete glottal closure, severe hyperadduction of the false vocal folds, anteroposterior hypercompression, and asymmetrical glottal movement in the on-stimulation condition. Thirty minutes after stopping stimulation, incomplete glottal closure and anteroposterior hypercompression disappeared and hyperadduction of the false vocal folds slightly improved. (MP4 18507 kb)

Segment 3. Patient 6 had severe incomplete glottal closure, severe hyperadduction of the false vocal folds, anteroposterior hypercompression, and asymmetrical glottal movement in the on-stimulation condition. Incomplete glottal closure, hyperadduction of the false vocal folds, and anteroposterior hypercompression disappeared with off-stimulation of the left-side DBS. (MP4 18005 kb)

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Tsuboi, T., Watanabe, H., Tanaka, Y. et al. Characteristic laryngoscopic findings in Parkinson’s disease patients after subthalamic nucleus deep brain stimulation and its correlation with voice disorder. J Neural Transm 122, 1663–1672 (2015). https://doi.org/10.1007/s00702-015-1436-y

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  • DOI: https://doi.org/10.1007/s00702-015-1436-y

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