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Mechanisms of Swallowing, Speech and Voice Disorders in Parkinson’s Disease: Literature Review with Our First Evidence for the Periperal Nervous System Involvement

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Abstract

The majority of patients with Parkinson’s disease (PD) develop swallowing, speech, and voice (SSV) disorders. Importantly, swallowing difficulty or dysphagia and related aspiration are life-threatening conditions for PD patients. Although PD treatments have significant therapeutic effects on limb motor function, their effects on SSV disorders are less impressive. A large gap in our knowledge is that the mechanisms of SSV disorders in PD are poorly understood. PD was long considered to be a central nervous system disorder caused by the death of dopaminergic neurons in the basal ganglia. Aggregates of phosphorylated α-synuclein (PAS) underlie PD pathology. SSV disorders were thought to be caused by the same dopaminergic problem as those causing impaired limb movement; however, there is little evidence to support this. The pharynx, larynx, and tongue play a critical role in performing upper airway (UA) motor tasks and their dysfunction results in disordered SSV. This review aims to provide an overview on the neuromuscular organization patterns, functions of the UA structures, clinical features of SSV disorders, and gaps in knowledge regarding the pathophysiology underlying SSV disorders in PD, and evidence supporting the hypothesis that SSV disorders in PD could be associated, at least in part, with PAS damage to the peripheral nervous system controlling the UA structures. Determining the presence and distribution of PAS lesions in the pharynx, larynx, and tongue will facilitate the identification of peripheral therapeutic targets and set a foundation for the development of new therapies to treat SSV disorders in PD.

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Data Availability

The data sources used in this review are publicly available and referenced accordingly in the article. Any additional information or data used in this review can be obtained by contacting the corresponding author.

Abbreviations

AChE:

Acetylcholinesterase

ASMA:

Anti-synuclein monoclonal antibody

CNS:

Central nervous system

CP:

Cricopharyngeus

CT:

Cricothyroid muscle

ESLN:

External superior laryngeal nerve

GG:

Genioglossus

HG:

Hyoglossus

HN:

Hypoglossal nucleus

IA:

Interarytenoid muscle

IL:

Inferior longitudinalis

IPC:

Inferior pharyngeal constrictor

ISLN:

Internal superior laryngeal nerve

IX:

Glossopharyngeal nerve

IX-L:

Lingual branch of the IX nerve

LCA:

Lateral cricoarytenoid muscle

LN:

Lingual nerve

MPC:

Middle pharyngeal constrictor

NA:

Nucleus ambiguous

PAS:

Phosphorylated α-synuclein

PC:

Pharyngeal constrictor

PCA:

Posterior cricoarytenoid muscle

PD:

Parkinson’s disease

Ph-IX:

Pharyngeal branch of the IX nerve

Ph-X:

Pharyngeal branch of the X nerve

PNS:

Peripheral nervous system

RLN:

Recurrent laryngeal nerve

SG:

Styloglossus

SL:

Superior longitudinalis

SLN:

Superior laryngeal nerve

SPC:

Superior pharyngeal constrictor

SSV:

Swallowing,speech and voice

T:

Transversus

TA:

Thyroarytenoid muscle

UA:

Upper airway

UE:

Upper esophagus

USSLBD:

Unified Staging System for Lewy Body Disorders

V:

Verticalis

VFB:

Vocal fold bowing

X:

Vagus nerve

XII:

Hypoglossal nerve

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Acknowledgements

This work was supported by the Department of Defense, Defense Health Program, Congressionally Directed Medical Research Programs (CDMRP), Parkinson’s Research Program under Award No. HT9425-23-1-0481 (to Dr. Liancai Mu). Opinions, interpretations, conclusions and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. We are grateful to the Banner Sun Health Research Institute Brain and Body Donation Program of Sun City, Arizona for the provision of human biological materials. The Brain and Body Donation Program has been supported by the National Institute of Neurological Disorders and Stroke (U24 NS072026 National Brain and Tissue Resource for Parkinson’s Disease and Related Disorders), the National Institute on Aging (P30AG019610 and P30AG072980, Arizona Alzheimer’s Disease Center), the Arizona Department of Health Services (contract 211002, Arizona Alzheimer’s Research Center), the Arizona Biomedical Research Commission (contracts 4001, 0011, 05-901 and 1001 to the Arizona Parkinson’s Disease Consortium) and the Michael J. Fox Foundation for Parkinson’s Research. The authors thank the anonymous reviewers for their constructive comments on this manuscript.

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  1. Upper Airway Reserch Laboratory, Center for Discovery and Innovation, Hackensack Meridian Health, 111 Ideation Way, Nutley, NJ, 07110, USA

    Liancai Mu, Jingming Chen, Jing Li & Themba Nyirenda

  2. Upper Airway Dysfunction Laboratory, M.A. Program in Communication Sciences & Disorders, Department of Speech, Language and Hearing Sciences, College of Public Health and Health Professions, University of Florida, 1225 Center Dr., Gainesville, FL, 32611, USA

    Karen Wheeler Hegland

  3. Director of Neuroscience, Director of Brain and Body Donation Program, Banner Sun Health Research Institute, 10515 West Santa Fe Dr, Sun City, AZ, 85351, USA

    Thomas G. Beach

  4. Center for Discovery and Innovation, Hackensack Meridian Health, 111 Ideation Way, Nutley, NJ, 07110, USA

    Liancai Mu

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Mu, L., Chen, J., Li, J. et al. Mechanisms of Swallowing, Speech and Voice Disorders in Parkinson’s Disease: Literature Review with Our First Evidence for the Periperal Nervous System Involvement. Dysphagia (2024). https://doi.org/10.1007/s00455-024-10693-3

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