Abstract
Airway invasion is common in patients with Parkinson’s disease (PD) and can cause serious complications. However, a PD-related dysphagic pattern has not been clearly elucidated. In this study, 53 patients with early to moderate PD were enrolled to undergo a videofluoroscopic study of swallowing evaluation (VFSS) and a battery of neuropsychological assessments. A set of VFSS variables (three visuoperceptual, nine temporal, and six spatial) were measured. The main effects of bolus viscosity and volume on airway invasion were calculated. Statistical analyses were performed to determine key kinematic factors of airway invasion for swallowing each bolus type. Airway invasion frequency was significantly higher for liquid boluses (liquid vs. pudding P < 0.001; liquid vs. honey P = 0.006). Laryngeal vestibule closure reaction time (LVCrt) was the key kinematic factor of airway invasion for 3 ml liquid swallow (P = 0.040), anterior displacement of hyoid bone was the key kinematic factor for both 5 ml and 10 ml liquid swallows (P = 0.010, 0.034, respectively). Male sex and advanced Hoehn and Yahr stage were significantly related to reduced anterior displacement of hyoid bone. These results reveal the dysphagic pattern related to PD, demonstrating that prolonged LVCrt and reduced anterior displacement of hyoid bone are two crucial kinematic factors contributing to airway invasion during the liquid swallow. In addition, hyoid bone dysfunction was correlated with disease severity and male sex. Our findings warrant further investigation of the pathophysiological mechanism of dysphagia in PD and would guide clinical intervention.
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References
Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids[J]. Dysphagia. 2014;29(2):269–76.
Kalf JG, de Swart BJ, Bloem BR, et al. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis[J]. Parkinsonism Relat Disord. 2012;18(4):311–5.
Tomita S, Oeda T, Umemura A, et al. Video-fluoroscopic swallowing study scale for predicting aspiration pneumonia in Parkinson’s disease[J]. PLoS ONE. 2018;13(6):e197608.
Wang G, Li XJ, Hu YS, et al. Mortality from Parkinson’s disease in China: findings from a five-year follow up study in Shanghai[J]. Can J Neurol Sci. 2015;42(4):242–7.
Lee JH, Lee KW, Kim SB, et al. The functional Dysphagia Scale is a useful Tool for Predicting Aspiration Pneumonia in patients with Parkinson Disease[J]. Ann Rehabil Med. 2016;40(3):440–6.
Cosentino G, Avenali M, Schindler A, et al. A multinational consensus on dysphagia in Parkinson’s disease: screening, diagnosis and prognostic value[J]. J Neurol. 2022;269(3):1335–52.
Labeit B, Ahring S, Boehmer M, et al. Comparison of simultaneous swallowing Endoscopy and Videofluoroscopy in Neurogenic Dysphagia[J]. J Am Med Dir Assoc. 2022;23(8):1360–6.
Kuuskoski J, Vanhatalo J, Rekola J et al. The Water Swallow Test and EAT-10 as Screening Tools for Referral to Videofluoroscopy[J]. Laryngoscope, 2023. Online ahead of print.
Argolo N, Sampaio M, Pinho P, et al. Videofluoroscopic predictors of Penetration-Aspiration in Parkinson’s Disease Patients[J]. Dysphagia. 2015;30(6):751–8.
Curtis JA, Molfenter S, Troche MS. Predictors of Residue and Airway Invasion in Parkinson’s Disease[J]. Dysphagia. 2020;35(2):220–30.
Dumican M, Watts C. Swallow Safety and Laryngeal kinematics: a comparison of Dysphagia between Parkinson’s Disease and Cerebrovascular Accident[J]. J Parkinsons Dis. 2022;12(7):2147–59.
Dumican M, Watts C. Predicting Airway Invasion using screening tools and laryngeal kinematics in people with Parkinson’s Disease: a pilot Study[J]. J Parkinsons Dis. 2020;10(3):1153–60.
Gaeckle M, Domahs F, Kartmann A, et al. Predictors of Penetration-Aspiration in Parkinson’s Disease patients with Dysphagia: a retrospective Analysis[J]. Ann Otol Rhinol Laryngol. 2019;128(8):728–35.
Wang P, Wang B, Chen X, et al. Six-year Follow-Up of Dysphagia in patients with Parkinson’s Disease[J]. Dysphagia. 2022;37(5):1271–8.
Nascimento D. Clinical features associated with drooling in Parkinson’s disease[J]. Neurol Sci. 2021;42(3):895–903.
Cereda E, Cilia R, Klersy C, et al. Swallowing disturbances in Parkinson’s disease: a multivariate analysis of contributing factors[J]. Parkinsonism Relat Disord. 2014;20(12):1382–7.
Manor Y, Giladi N, Cohen A, et al. Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease[J]. Mov Disord. 2007;22(13):1917–21.
Hanson B, Jamshidi R, Redfearn A, et al. Experimental and computational investigation of the IDDSI Flow Test of liquids used in Dysphagia Management[J]. Ann Biomed Eng. 2019;47(11):2296–307.
Ding X, Gao J, Xie C, et al. Prevalence and clinical correlation of dysphagia in Parkinson disease: a study on Chinese patients[J]. Eur J Clin Nutr. 2018;72(1):82–6.
Clark HM, Stierwalt J, Tosakulwong N, et al. Dysphagia in Progressive Supranuclear Palsy[J] Dysphagia. 2020;35(4):667–76.
Dumican M, Watts C, Drulia T, et al. Dysphagia Presentation, Airway Invasion, and gender differences in a clinically based sample of people with Parkinson’s Disease[J]. Dysphagia. 2023;38(1):353–66.
Smaoui S, Peladeau-Pigeon M, Steele CM. Determining the relationship between hyoid bone kinematics and Airway Protection in Swallowing[J]. J Speech Lang Hear Res. 2022;65(2):419–30.
Stokely SL, Peladeau-Pigeon M, Leigh C, et al. The relationship between pharyngeal constriction and post-swallow Residue[J]. Dysphagia. 2015;30(3):349–56.
Hutcheson KA, Hammer MJ, Rosen SP, et al. Expiratory muscle strength training evaluated with simultaneous high-resolution manometry and electromyography[J]. Laryngoscope. 2017;127(4):797–804.
Dharmarathna I, Miles A, Allen J. Quantifying Bolus Residue and its risks in children: a videofluoroscopic study.[J]. Am J Speech-Lang Pat. 2021;30(2):687–96.
Molfenter SM, Lenell C, Lazarus CL. Volumetric changes to the pharynx in healthy aging: consequence for pharyngeal swallow mechanics and Function[J]. Dysphagia. 2019;34(1):129–37.
Koo TK, Li MY. A Guideline of selecting and reporting Intraclass correlation coefficients for Reliability Research[J]. J Chiropr Med. 2016;15(2):155–63.
Viera AJ, Garrett JM. Understanding interobserver agreement: the kappa statistic[J]. Fam Med. 2005;37(5):360–3.
Mu L, Sobotka S, Chen J, et al. Parkinson disease affects peripheral sensory nerves in the pharynx[J]. J Neuropathol Exp Neurol. 2013;72(7):614–23.
Wei KC, Hsiao MY, Wang TG. The kinematic features of hyoid bone movement during swallowing in different disease populations: a narrative review[J]. J Formos Med Assoc. 2022;121(10):1892–9.
Lee WH, Lim MH, Nam HS, et al. Differential kinematic features of the hyoid bone during swallowing in patients with Parkinson’s disease[J]. J Electromyogr Kinesiol. 2019;47:57–64.
Okada T, Aoyagi Y, Inamoto Y, et al. Dynamic change in hyoid muscle length associated with trajectory of hyoid bone during swallowing: analysis using 320-row area detector computed tomography[J]. J Appl Physiol (1985). 2013;115(8):1138–45.
Kim YH, Oh BM, Jung IY, et al. Spatiotemporal characteristics of swallowing in Parkinson’s disease[J]. Laryngoscope. 2015;125(2):389–95.
Claus I, Muhle P, Suttrup J, et al. Predictors of pharyngeal dysphagia in patients with Parkinson’s Disease[J]. J Parkinsons Dis. 2020;10(4):1727–35.
Claus I, Muhle P, Czechowski J, et al. Expiratory Muscle Strength Training for Therapy of Pharyngeal Dysphagia in Parkinson’s Disease[J]. Mov Disord. 2021;36(8):1815–24.
Lee JJ, Ham JH, Lee PH, et al. Gender differences in Age-Related Striatal Dopamine Depletion in Parkinson’s Disease[J]. J Mov Disord. 2015;8(3):130–5.
Suttrup I, Warnecke T. Dysphagia in Parkinson’s Disease[J]. Dysphagia. 2016;31(1):24–32.
McCullough GH, Kim Y. Effects of the Mendelsohn maneuver on extent of hyoid movement and UES opening post-stroke[J]. Dysphagia. 2013;28(4):511–9.
Benfield JK, Everton LF, Bath PM, et al. Does Therapy with Biofeedback improve swallowing in adults with Dysphagia? A systematic review and Meta-Analysis[J]. Arch Phys Med Rehabil. 2019;100(3):551–61.
Martin-Harris B, McFarland D, Hill EG, et al. Respiratory-swallow training in patients with head and neck cancer[J]. Arch Phys Med Rehabil. 2015;96(5):885–93.
Watts CR, Dumican MJ. The effect of transcutaneous neuromuscular electrical stimulation on laryngeal vestibule closure timing in swallowing[J]. BMC Ear Nose Throat Disord. 2018;18:5.
Keiichi T, Shuji M, Miho K, et al. Novel neuromuscular electrical stimulation system for treatment of Dysphagia after Brain Injury[J]. Neurol Med-Chir. 2014;54(7):521–8.
Umemoto G, Furuya H. Management of Dysphagia in patients with Parkinson’s Disease and Related Disorders[J]. Intern Med. 2020;59(1):7–14.
Kim JY, Kim H. Effects of behavioural swallowing therapy in patients with Parkinson’s disease: a systematic review.[J]. Int J Speech-Lang Pa. 2023;25(2):269–80.
Acknowledgements
We sincerely thank the patients participated in our study. We also acknowledge the support of the National Natural Science Foundation of China (82201393) and the Foundation of Zhejiang Rehabilitation Medical Center (ZKYJ2316).
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This study was supported by the National Natural Science Foundation of China (82201393) and the Foundation of Zhejiang Rehabilitation Medical Center (ZKYJ2316).
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Ping Wang and Xinhui Chen contributed equally to this work.
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Wang, P., Chen, X., Chen, M. et al. Dysphagia Pattern in Early to Moderate Parkinson’s Disease Caused by Abnormal Pharyngeal Kinematic Function. Dysphagia (2024). https://doi.org/10.1007/s00455-024-10672-8
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DOI: https://doi.org/10.1007/s00455-024-10672-8