Hypokinetic dysarthria (HD) and freezing of gait (FOG) are both axial symptoms that occur in patients with Parkinson's disease (PD). It is assumed they have some common pathophysiological mechanisms and therefore that speech disorders in PD can predict FOG deficits within the horizon of some years. The aim of this study is to employ a complex quantitative analysis of the phonation, articulation and prosody in PD patients in order to identify the relationship between HD and FOG, and establish a mathematical model that would predict FOG deficits using acoustic analysis at baseline. We enrolled 75 PD patients who were assessed by 6 clinical scales including the Freezing of Gait Questionnaire (FOG-Q). We subsequently extracted 19 acoustic measures quantifying speech disorders in the fields of phonation, articulation and prosody. To identify the relationship between HD and FOG, we performed a partial correlation analysis. Finally, based on the selected acoustic measures, we trained regression models to predict the change in FOG during a 2-year follow-up. We identified significant correlations between FOG-Q scores and the acoustic measures based on formant frequencies (quantifying the movement of the tongue and jaw) and speech rate. Using the regression models, we were able to predict a change in particular FOG-Q scores with an error of between 7.4 and 17.0 %. This study is suggesting that FOG in patients with PD is mainly linked to improper articulation, a disturbed speech rate and to intelligibility. We have also proved that the acoustic analysis of HD at the baseline can be used as a predictor of the FOG deficit during 2 years of follow-up. This knowledge enables researchers to introduce new cognitive systems that predict gait difficulties in PD patients.

1st Department of Neurology St Anne's University Hospital Pekarska 53 656 91 Brno Czech Republic

Applied Neuroscience Research Group Central European Institute of Technology Masaryk University Kamenice 5 62500 Brno Czech Republic

Data and Signal Processing Research Group University of Vic Central University of Catalonia Perot Rocaguinarda 17 08500 Vic Catalonia Spain

Department of Neurology Faculty Hospital and Masaryk University Jihlavska 20 63900 Brno Czech Republic

Department of Telecommunications Brno University of Technology Technicka 10 61600 Brno Czech Republic

Escola Superior Politecnica Tecnocampus Avda Ernest Lluch 32 08302 Mataro Barcelona Spain

Neuromorphic Processing Laboratory Center for Biomedical Technology Universidad Politécnica de Madrid Campus de Montegancedo s n 28223 Pozuelo de Alarcón Madrid Spain

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Ackermann H, Konczak J, Hertrich I. The temporal control of repetitive articulatory movements in parkinson’s disease. Brain Lang. 1997;56(2):312–9. PubMed

Alonso-Martinez C, Faundez-Zanuy M, Mekyska J. A comparative study of in-air trajectories at short and long distances in online handwriting. Cogn Comput. 2017;9(5):712–20. PubMed PMC

Arias-Vergara T, Vásquez-Correa JC, Orozco-Arroyave JR. Parkinson’s disease and aging: analysis of their effect in phonation and articulation of speech. Cogn Comput. 2017;9(6):731–48.

Azulay JP, Brand CVD, Mestre D, Blin O, Sangla I, Pouget J, Serratrice G. Automatic motion analysis of gait in patients with Parkinson disease: effects of levodopa and visual stimulations. Ren Neurol. 1996;152(2):128–34. PubMed

Bartels A, Balash Y, Gurevich T, Schaafsma J, Hausdorff J, Giladi N. Relationship between freezing of gait (FOG) and other features of Parkinson’s: FOG is not correlated with bradykinesia. J Clin Neurosci. 2003;10(5):584–8. PubMed

Becker C, Rigamonti R, Lepetit V, Fua P. 2013. Supervised feature learning for curvilinear structure segmentation. In: International conference on medical image computing and computer-assisted intervention, pp 526–533. PubMed

Berankova D, Janousova E, Mrackova M, Eliasova I, Kostalova M, Skutilova S, Rektorova I. 2015. Addenbrooke’s cognitive examination and individual domain cut-off scores for discriminating between different cognitive subtypes of Parkinson’s disease. Parkinsons Dis 2015. PubMed PMC

Boersma P, Weenink D. 2017. Praat: doing phonetics by computer. http://www.fon.hum.uva.nl/praat/.

Brabenec L, Mekyska J, Galaz Z, Rektorova I. Speech disorders in Parkinson’s disease: early diagnostics and effects of medication and brain stimulation. J Neural Transm. 2017;124(3):303–34. PubMed

Brodal P. The central nervous system: structure and function. 3rd ed. Oxford: Oxford University Press; 2003.

Caligiuri MP. The influence of speaking rate on articulatory hypokinesia in parkinsonian dysarthria. Hum Mov Sci. 2006;36:493–502. PubMed

Canter GJ. Speech characteristics of patients with Parkinson’s disease: III. Articulation, diadochokinesis, and over-all speech adequacy. J Speech Hear Disord. 1965;30(3):217–24. PubMed

Cantiniaux S, Vaugoyeau M, Robert D, Horrelou-Pitek C, Mancini J, Witjas T, Azulay JP. Comparative analysis of gait and speech in Parkinson’s disease: hypokinetic or dysrhythmic disorders? J Neurol Neurosurg Psychiatry. 2010;81(2):177–84. PubMed

Chai T, Draxler RR. Root mean square error (RMSE) or mean absolute error (MAE)? – Arguments against avoiding RMSE in the literature. Geosci Model Dev. 2014;7(3):1247–50.

Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P. Parkinson’s disease: the non-motor issues. Park Relat Disord. 2011;17(10):717–23. PubMed

Darley FL, Aronson AE, Brown JR. Clusters of deviant speech dimensions in the dysarthrias. J Speech Lang Hear Res. 1969;12(3):462–96. PubMed

Dauer W, Przedborski S. Parkinson’s disease: mechanisms and models. Neuron. 2003;39(6):889–909. PubMed

Espay A, Fasano A, Van Nuenen B, Payne M, Snijders A, Bloem B. On state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology. 2012;78(7):454–7. PubMed PMC

Fahn S, Elton RL. UPDRS development committee (1987) unified parkinson’s disease rating scale recent developments in parkinson’s disease. Florham Park: Macmillan; 1987.

Faundez-Zanuy M, Hussain A, Mekyska J, Sesa-Nogueras E, Monte-Moreno E, Esposito A, Chetouani M, Garre-Olmo J, Abel A, Smekal Z, et al. Biometric applications related to human beings: there is life beyond security. Cogn Comput. 2013;5(1):136–51.

Folstein M, Folstein SE, McHugh PR. Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189–98. PubMed

Galaz Z, Mekyska J, Mzourek Z, Smekal Z, Rektorova I, Eliasova I, Kostalova M, Mrackova M, Berankova D. Prosodic analysis of neutral, stress-modified and rhymed speech in patients with Parkinson’s disease. Comput Methods Programs Biomed. 2016;127:301–17. PubMed

Giladi N, Kao R, Fahn S. Freezing phenomenon in patients with parkinsonian syndromes. Mov Disord. 1997;12(3):302–5. PubMed

Giladi N, Shabtai H, Simon ES, Biran S, Tal J, Korczyn SD. Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord. 2000;6(3):165–70. PubMed

Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M, Tanner C. Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology. 2001;56(12):1712–21. PubMed

Giladi N, Shabtai H, Rozenberg E, Shabtai E. Gait festination in Parkinson’s disease. Parkinsonism Relat Disord. 2001;7(2):135–8. PubMed

Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B, Paleacu D, Korczyn AD. Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm. 2001;108(1):53–61. PubMed

Goberman A, Coelho C, Robb M. Phonatory characteristics of parkinsonian speech before and after morning medication: the ON and OFF states. J Commun Disord. 2002;35(3):217–39. PubMed

Goberman AM. Correlation between acoustic speech characteristics and non-speech motor performance in Parkinson’s disease. Med Sci Monit. 2005;11(3):CR109–116. PubMed

Gómez-Vilda P, Rodellar-Biarge V, Nieto-Lluis V, Muñoz-Mulas C, Mazaira-Fernández LM, Martínez-Olalla R, Álvarez-Marquina A, Ramírez-Calvo C, Fernández-Fernández M. Characterizing neurological disease from voice quality biomechanical analysis. Cogn Comput. 2013;5(4):399–425.

Gómez-Vilda P, Ferrández-Vicente JM, Palacios-Alonso D, Gómez-Rodellar A, Rodellar-Biarge V, Mekyska J, Smekal Z, Rektorova I, Eliasova I, Kostalova M. Vowel articulation distortion in parkinson’s disease. Cham: Springer International Publishing; 2017. pp. 21–31.

Gomez-Vilda P, Mekyska J, Ferrandez JM, Palacios-Alonso D, Gmez-rodellar A, Rodellar-Biarge V, Galaz Z, Smekal Z, Rektorova I, Eliasova I, Kostalova M. Parkinson disease detection from speech articulation neuromechanics. Front Neuroinform. 2017;11:1–17. PubMed PMC

Gray P, Hildebrand K. Fall risk factors in Parkinson’s disease. J Neurosci Nurs. 2000;32(4):222–8. PubMed

Hall D, Ouyang B, Lonnquist E, Newcombe J. Pragmatic communication is impaired in Parkinson disease. Int J Neurosci. 2011;121(5):254–6. PubMed

Herzog J, Volkmann J, Krack P, Kopper F, Pötter M, Lorenz D, Steinbach M, Klebe S, Hamel W, Schrader B, et al. Two-year follow-up of subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord. 2003;18(11):1332–7. PubMed

Hillenbrand J, Houde RA. Acoustic correlates of breathy vocal quality: dysphonic voices and continuous speech. J Speech Hear Res. 1996;39(2):311–21. PubMed

Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17:427–42. PubMed

Hornykiewicz O. Biochemical aspects of Parkinson’s disease. Neurology. 1998;51(2 Suppl 2):S2–S9. PubMed

Lopez-de Ipiña K, Alonso JB, Solé-Casals J, Barroso N, Henriquez P, Faundez-Zanuy M, Travieso CM, Ecay-Torres M, Martinez-Lage P, Eguiraun H. On automatic diagnosis of Alzheimer’s disease based on spontaneous speech analysis and emotional temperature. Cogn Comput. 2015;7(1):44–55.

Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry. 2008;79(4):368–76. PubMed

Kostalova M, Mrackova M, Marecek R, Berankova D, Eliasova I, Janousova E, Roubickova J, Bednarik J, Rektorova I. The 3F Test dysarthric profile—normative speach values in Czech. Cesk Slov Neurol Neurochir. 2013;76(5):614–18.

Lee JY, Kim JW, Lee WY, Kim JM, Ahn TB, Kim HJ, Cho J, Jeon BS. Daily dose of dopaminergic medications in Parkinson’s disease: clinical correlates and a posteriori equation. Neurol Asia. 2010;15(2):137–43.

Leentjens AF, Verhey FR, Luijckx GJ, Troost J. The validity of the Beck Depression Inventory as a screening and diagnostic instrument for depression in patients with Parkinson’s disease. Mov Disord. 2000;15(6):1221–4. PubMed

Macht M, Kaussner Y, Möller JC, Stiasny-Kolster K, Eggert KM, Krüger HP, Ellgring H. Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord. 2007;22(7):953–6. PubMed

McCaig CM, Adams SG, Dykstra AD, Jog M. Effect of concurrent walking and interlocutor distance on conversational speech intensity and rate in Parkinson’s disease. Gait Posture. 2016;43:132–6. PubMed

Mekyska J, Smekal Z, Kostalova M, Mrackova M, Skutilova S, Rektorova I. Motor aspects of speech impairment in Parkinson’s disease and their assessment. Cesk Slov Neurol N. 2011;74(6):662–8.

Mekyska J, Janousova E, Gomez-Vilda P, Smekal Z, Rektorova I, Eliasova I, Kostalova M, Mrackova M, Alonso-Hernandez JB, Faundez-Zanuy M, de Ipiña KL. Robust and complex approach of pathological speech signal analysis. Neurocomputing. 2015;167:94–111.

Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR. The Addenbrooke’s cognitive examination revised (ACE-r): a brief cognitive test battery for dementia screening. Int J Ger Psychiatry. 2006;21(11):1078–85. PubMed

Moreau C, Ozsancak C, Blatt JL, Destee A, Defebvre L. Oral festination in Parkinson’s disease: biomechanical analysis and correlation with festination and freezing of gait. Mov Disord. 2007;22(10):1503–6. PubMed

Morris ME, Huxham F, McGinley J, Dodd K, Iansek R. The biomechanics and motor control of gait in Parkinson disease. Clin Biomech. 2001;16(6):459–70. PubMed

Nilsson MH, Hagell P. Freezing of gait questionnaire: validity and reliability of the Swedish version. Acta Neurol Scand. 2009;120(5):331–4. PubMed

Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011;10(8):734–44. PubMed PMC

Okuma Y. Freezing of gait and falls in Parkinson’s disease. J Parkinsons Dis. 2014;4(2):255–60. PubMed

Park HK, Yoo JY, Kwon M, Lee JH, Lee SJ, Kim SR, Kim MJ, Lee MC, Lee SM, Chung SJ. Gait freezing and speech disturbance in Parkinson’s disease. Neurol Sci. 2014;35(3):357–63. PubMed

Pederson SW, Eriksson T, Öberg B. Effects of withdrawal of antiparkinson medication on gait and clinical score in the Parkinson patient. Acta Neurol Scand. 1991;84(1):7–13. PubMed

Pell MD, Cheang HS, Leonard CL. The impact of Parkinson’s disease on vocal-prosodic communication from the perspective of listeners. Brain Lang. 2006;97(2):123–34. PubMed

Ramig LO, Fox C, Sapir S. Speech treatment for Parkinson’s disease. Expert Rev Neurother. 2008;8(2):297–309. PubMed

Rektorova I, Mekyska J, Janousova E, Kostalova M, Eliasova I, Mrackova M, Berankova D, Necasova T, Smekal Z, Marecek R. Speech prosody impairment predicts cognitive decline in Parkinson’s disease. Parkinsonism Relat Disord. 2016;29:90–5. PubMed

Ricciardi L, Ebreo M, Graziosi A, Barbuto M, Sorbera C, Morgante L, Morgante F. Speech and gait in Parkinson’s disease: when rhythm matters. Parkinsonism Relat Disord. 2016;32:42–7. PubMed

de Rijk MC, Launer LJ, Berger K, Breteler MM, Dartigues JF, Baldereschi M, Fratiglioni L, Martinez-Lage LoboJA, Trenkwalder C, Hofman A. Prevalence of Parkinson’s disease in Europe: a collaborative study of population-based cohorts. Neurology. 2000;54:21–3. PubMed

Rosenblum S, Luria G. Applying a handwriting measurement model for capturing cognitive load implications through complex figure drawing. Cogn Comput. 2016;8(1):69–77.

Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM. Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J Neurol Sci. 2003;212(1-2):47–53. PubMed

Shao J, MacCallum JK, Zhang Y, Jiang JJ. Acoustic analysis of the tremulous voice: assessing the utility of the correlation dimension and perturbation parameters. J Commun Disord. 2010;43(1):35–44. PubMed PMC

Shine J, Naismith S, Lewis S. The pathophysiological mechanisms underlying freezing of gait in Parkinson’s disease. J Clin Neurosci. 2011;18(9):1154–7. PubMed

Shine J, Naismith S, Lewis S. The differential yet concurrent contributions of motor, cognitive and affective disturbance to freezing of gait in Parkinson’s disease. Clin Neurol Neurosurg. 2013;115(5):542–45. PubMed

Skodda S, Flasskamp A, Schlegel U. Instability of syllable repetition as a marker of disease progression in Parkinson’s disease: a longitudinal study. Mov Disord. 2011;26(1):59–64. PubMed

Skodda S, Visser W, Schlegel U. Vowel articulation in Parkinson’s disease. J Voice. 2011;25(4):467–72. PubMed

Stiasny-Kolster K, Mayer G, Schafer S, Muller JC, Heinzel-Gutenbrunner M, Oertel WH. The REM sleep behavior disorder screening questionnaire—a new diagnostic instrument. Mov Disord. 2007;22(16):2386–93. PubMed

Sznitman R, Becker C, Fleuret F, Fua P. 2013. Fast object detection with entropy-driven evaluation. In: IEEE conference on computer vision and pattern recognition (CVPR), pp 3270–3277.

Teager H. Some observations on oral air flow during phonation. IEEE Trans Acoust Speech Signal Process. 1980;28(5):599–601.

Varanese S, Birnbaum Z, Rossi R, Di Rocco A. Treatment of advanced Parkinson’s disease. Parkinsons Dis. 2010;2010:480,260. PubMed PMC

Vercruysse S, Gilat M, Shine JM, Heremans E, Lewis S, Nieuwboer A. Freezing beyond gait in Parkinson’s disease: a review of current neurobehavioral evidence. Neurosci Biobehav Rev. 2014;43:213–27. PubMed

Vesely B, Antonini A, Rektor I. The contribution of white matter lesions to Parkinsons disease motor and gait symptoms: a critical review of the literature. J Neural Transm. 2016;123(3):241–50. PubMed

Videnovic A, Marlin C, Alibiglou L, Planetta P, Vaillancourt D, Mackinnon C. Increased REM sleep without atonia in Parkinson disease with freezing of gait. Neurology. 2013;81(12):1030–5. PubMed PMC

Virmani T, Moskowitz CB, Vonsattel JP, Fahn S. Clinicopathological characteristics of freezing of gait in autopsy-confirmed Parkinson’s disease. Mov Disord. 2015;30(14):1874–84. PubMed

Walton CC, Shine JM, Hall JM, O’callaghan C, Mowszowski L, Gilat M, Jennifer Y, Szeto Y, Naismith SL, Simon J, et al. The major impact of freezing of gait on quality of life in Parkinson’s disease. J Neurol. 2015;262(1):108–15. PubMed

Xiao H, Li M, Cai J, Li N, Zhou M, Wen P, Xie Z, Wang Q, Chang J, Zhang W. Selective cholinergic depletion of pedunculopontine tegmental nucleus aggravates freezing of gait in parkinsonian rats. Neurosci Lett. 2017;659:92–98. PubMed

Yao Z, Shao Y, Han X. Freezing of gait is associated with cognitive impairment in patients with Parkinson disease. Neurosci Lett. 2017;656:126–30. PubMed

Zhang H, Yin X, Ouyang Z, Chen J, Zhou S, Zhang C, Pan X, Wang S, Yang J, Feng Y, et al. A prospective study of freezing of gait with early Parkinson disease in Chinese patients. Medicine. 2016;95(26):e4056. PubMed PMC

Zwirner P, Barnes GJ. Vocal tract steadiness: a measure of phonatory and upper airway motor control during phonation in dysarthria. J Speech Hear Res. 1992;35(4):761–8. PubMed

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