Online citations, reference lists, and bibliographies.
← Back to Search

Altered Pharyngeal Muscles In Parkinson Disease

L. Mu, S. Sobotka, J. Chen, Hungxi Su, I. Sanders, C. Adler, H. Shill, J. Caviness, J. Samanta, T. Beach
Published 2012 · Medicine

Cite This
Download PDF
Analyze on Scholarcy
Share
Abstract Dysphagia (impaired swallowing) is common in patients with Parkinson disease (PD) and is related to aspiration pneumonia, the primary cause of death in PD. Therapies that ameliorate the limb motor symptoms of PD are ineffective for dysphagia. This suggests that the pathophysiology of PD dysphagia may differ from that affecting limb muscles, but little is known about potential neuromuscular abnormalities in the swallowing muscles in PD. This study examined the fiber histochemistry of pharyngeal constrictor and cricopharyngeal sphincter muscles in postmortem specimens from 8 subjects with PD and 4 age-matched control subjects. Pharyngeal muscles in subjects with PD exhibited many atrophic fibers, fiber type grouping, and fast-to-slow myosin heavy chain transformation. These alterations indicate that the pharyngeal muscles experienced neural degeneration and regeneration over the course of PD. Notably, subjects with PD with dysphagia had a higher percentage of atrophic myofibers versus with those without dysphagia and controls. The fast-to-slow fiber-type transition is consistent with abnormalities in swallowing, slow movement of food, and increased tone in the cricopharyngeal sphincter in subjects with PD. The alterations in the pharyngeal muscles may play a pathogenic role in the development of dysphagia in subjects with PD.
This paper references
10.1002/MUS.880120807
Muscle fatigue, effects of training and disuse
K. Hainaut (1989)
10.1369/jhc.6A7084.2006
Adult Human Upper Esophageal Sphincter Contains Specialized Muscle Fibers Expressing Unusual Myosin Heavy Chain Isoforms
L. Mu (2007)
10.1002/1531-8257(200003)15:2<238::AID-MDS1006>3.0.CO;2-J
Motor unit changes in sporadic idiopathic Parkinson's disease
J. Caviness (2000)
10.1016/J.PARKRELDIS.2007.08.003
Is drooling secondary to a swallowing disorder in patients with Parkinson's disease?
A. Nóbrega (2008)
10.1073/PNAS.82.13.4544
Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles.
J. Covault (1985)
An electrophysiological study of the functional changes in the spinal motoneurones in Parkinson's disease.
R. Sica (1976)
10.1378/CHEST.124.3.1009
Impaired efficacy of cough in patients with Parkinson disease.
S. Ebihara (2003)
10.1001/ARCHNEUR.56.1.33
Diagnostic criteria for Parkinson disease.
D. Gelb (1999)
10.1007/s00455-007-9144-x
Voluntary Cough Production and Swallow Dysfunction in Parkinson’s Disease
T. Pitts (2007)
10.1002/mds.20113
Does parkin play a role in the peripheral nervous system? A family report
G. Abbruzzese (2004)
10.1055/S-1999-8758
Kehlkopfbefunde bei Patienten mit Morbus Parkinson
Y. Stelzig (1999)
10.1055/S-2008-1064219
The Neurology of Swallowing
A. Perlman (1991)
10.1002/mds.21065
Stanley Fahn Lecture 2005: The staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered
H. Braak (2006)
A study of salivary secretion in Parkinson's disease.
H. Bagheri (1999)
10.1111/j.1750-3639.2006.00032.x
Degeneration of Cardiac Sympathetic Nerve Begins in the Early Disease Process of Parkinson’s Disease
S. Orimo (2007)
10.1017/cbo9780511763281.013
[The Unified Parkinson's Disease Rating Scale].
A. Bonnet (2000)
SURGICAL TREATMENT OF PARKINSON'S DISEASE.
N. Wetzel (1963)
Parkinson’s disease: An immunohistochemical study of Lewy bodyYcontaining neurons in the enteric nervous system
K Wakabayashi (1990)
10.1002/AR.A.20065
Adult human mylohyoid muscle fibers express slow-tonic, alpha-cardiac, and developmental myosin heavy-chain isoforms.
L. Mu (2004)
Muscle biopsy — a practical approach
M. Dalakas (1986)
10.1136/jnnp.63.5.579
Response of parkinsonian swallowing dysfunction to dopaminergic stimulation
P. Hunter (1997)
The Sun Health Research Institute Brain Donation Program: Description and experience
T G Beach (2008)
10.1007/BF00493169
The reliability of histochemical fibre typing of human necropsy muscles
P. Eriksson (2004)
The patient with Parkinson's disease.
Sarah J Dirks (2003)
10.1016/S0197-4580(97)00057-2
Consensus recommendations for the postmortem diagnosis of Alzheimer's disease
M. Ball (1997)
10.1016/0022-510X(73)90135-4
An electrophysiological investigation of skeletal muscle in Parkinson's disease.
R. Sica (1973)
10.1007/BF00125308
Characterization of human skeletal muscle fibres according to the myosin heavy chains they express
S. Ennion (2004)
10.1002/MDS.870110110
Cricopharyngeal dysfunction in Parkinson's disease: Role in dysphagia and response to myotomy
L. J. Born (1996)
10.1212/WNL.0b013e3181cff6d5
α-SYNUCLEIN ACCUMULATION IN SKIN NERVE FIBERS REVEALED BY SKIN BIOPSY IN PURE AUTONOMIC FAILURE
T. Shishido (2010)
10.1212/01.wnl.0000171859.85078.3d
Reduced amplitude of the sural nerve sensory action potential in PARK2 patients
Y. Ohsawa (2005)
10.1016/S0303-8467(97)80006-6
Swallowing difficulty in Parkinson's disease
J. Fuh (1997)
10.1159/000266286
Speech and swallowing symptoms associated with Parkinson's disease and multiple sclerosis: a survey.
L. Hartelius (1994)
10.1016/S0016-5085(99)70144-7
AGA technical review on management of oropharyngeal dysphagia.
I. Cook (1999)
10.1093/AGEING/23.3.251
Asymptomatic swallowing disorders in elderly patients with Parkinson's disease: a description of findings on clinical examination and videofluoroscopy in sixteen patients.
M. R. Bird (1994)
10.1136/jnnp.55.7.572
A component analysis of the generation and release of isometric force in Parkinson's disease.
N. Jordan (1992)
10.1212/WNL.50.2.318
Parkinsonism: onset, progression, and mortality. 1967.
M. Hoehn (2001)
10.1053/GAST.1996.V110.PM8566584
Mechanisms of oral-pharyngeal dysphagia in patients with Parkinson's disease.
G. N. Ali (1996)
10.1093/brain/awn102
Sensory deficit in Parkinson's disease: evidence of a cutaneous denervation.
M. Nolano (2008)
10.1007/s100720200099
Clinical assessment of dysphagia in early phases of Parkinson's disease
M. A. Volontè (2002)
10.1136/jnnp.54.3.210
Abnormal most-rapid isometric contractions in patients with Parkinson's disease.
M. Wierzbicka (1991)
10.1179/016164104225013824
Muscle–nerve–muscle neurotization for the reinnervation of denervated somatic muscle
M. Urbanchek (2004)
An electrophysiological study of the functional changes in the spinal motoneurones in Parkinson's disease.
Sica Re (1976)
10.1159/000083970
Capgras’ Syndrome of Time
V. Aziz (2005)
10.1016/S1072-7515(00)00768-7
Is this a practical approach?
R. Wallace (2001)
10.1212/WNL.23.9.990
Sporadic and familial parkinsonism and motor neuron disease
K. Brait (1973)
Abnormal mostrapid isometric contractions in patients with Parkinson’s disease
MM Wierzbicka (1991)
10.1016/j.neulet.2005.02.030
Skin and platelet α-synuclein as peripheral biomarkers of Parkinson's disease
A. W. Michell (2005)
10.1097/00005072-199710000-00002
Editorial on Consensus Recommendations for the Postmortem Diagnosis of Alzheimer Disease from the National Institute on Aging and the Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer Disease
B. Hyman (1997)
10.1002/ANA.410210512
Neural cell adhesion molecule in normal, denervated, and myopathic human muscle
N. Cashman (1987)
10.1056/NEJM200204113461517
Botulinum toxin for cricopharyngeal dysfunction in Parkinson's disease.
D. Restivo (2002)
Botulin toxin for cricopharyngeal dysfunction in Parkinson’s disease
DA Restivo (2002)
10.1111/J.1365-2702.2005.01454.X
Avoidance of solid food in weight losing older patients with Parkinson's disease.
B. Lorefält (2006)
Neurophysiological basis of swallowing dysphagia
AJ Miller (1986)
Neural organization of deglutition
RW Doty (1968)
Oral-pharyngeal dysfunction in patients with Parkinson’s disease and dysphagia
GN Ali (1994)
10.1007/PL00009512
Pharyngo-Esophageal Dysphagia in Parkinson's Disease
N. Leopold (1997)
10.1002/mds.22137
Neuropathy as a potential complication of levodopa use in Parkinson's disease
C. Toth (2008)
10.1002/mds.10240
Electrophysiological evaluation of pharyngeal phase of swallowing in patients with Parkinson's disease
C. Ertekin (2002)
10.1007/s00401-010-0664-3
Multi-organ distribution of phosphorylated α-synuclein histopathology in subjects with Lewy body disorders
T. Beach (2010)
10.1007/s00455-005-0015-z
Intrinsic Properties of the Adult Human Mylohyoid Muscle: Neural Organization, Fiber-Type Distribution, and Myosin Heavy Chain Expression
M. Bs (2005)
Swallowing and esophageal function in Parkinson's disease.
B. Johnston (1995)
10.1016/j.neulet.2009.12.027
Clinical availability of skin biopsy in the diagnosis of Parkinson's disease
Y. Miki (2010)
10.1016/0022-510X(70)90104-8
Selective changes in the sizes of red and white muscle fibres in upper motor lesions and Parkinsonism.
L. Edström (1970)
10.1007/BF00417905
Quantitative assessment of oral and pharyngeal function in Parkinson's disease
H. Nilsson (2004)
10.1111/J.1432-1033.1990.TB19379.X
Myosin heavy chain isoform composition in striated muscle after denervation and self-reinnervation.
A. Jakubiec-Puka (1990)
10.1093/BRAIN/AWM302
Axonal α-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease
S. Orimo (2008)
10.1007/s00401-008-0355-5
A not entirely benign procedure: progression of Parkinson’s disease
K. Del Tredici (2008)
10.1016/0003-9969(83)90034-1
Histochemical and morphological muscle-fibre characteristics of the human masseter, the medial pterygoid and the temporal muscles.
P. Eriksson (1983)
10.1016/S1353-8020(02)00114-1
Sensory neuropathy in autosomal recessive juvenile parkinsonism (PARK2).
Y. Okuma (2003)
Myosin heavy chain isoform composition in striated muscle after denervation and selfreinnervation
A Jakubiec-Puka (1990)
10.1002/ana.22021
Levodopa, methylmalonic acid, and neuropathy in idiopathic Parkinson disease
C. Toth (2010)
10.1002/mds.21989
Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson's disease
H. Fujishiro (2008)
10.1007/BF00294234
Parkinson's disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system
K. Wakabayashi (2004)
10.1097/MOO.0b013e3282febd3a
Speech and swallowing disorders in Parkinson disease
S. Sapir (2008)
10.1212/WNL.42.4.726
Gastrointestinal dysfunction in Parkinson's disease
L. Edwards (1992)
10.1007/s00702-005-0431-0
Skin biopsy for assessment of autonomic denervation in Parkinson’s disease
R. Dabby (2005)
10.1007/BF03159935
Pathology of Parkinson's disease. Changes other than the nigrostriatal pathway.
K. Jellinger (1991)
10.1002/ANA.410190310
Swallowing and speech production in Parkinson's disease
J. Robbins (1986)
10.1212/WNL.17.5.427
Parkinsonism: onset, progression, and mortality
M. Hoehn (1967)
10.1007/BF01608336
Fibre type specific expression of Leu19-antigen and N-CAM in skeletal muscle in various stages after experimental denervation
W. Müller-Felber (2005)
10.1093/ageing/afgi30
[Parkinson's disease].
Houeto Jean-Luc (2005)
10.1097/NRL.0b013e3181b1cde5
The Larynx for Neurologists
T. Meyer (2009)
10.1007/s00401-010-0665-2
Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson’s disease
K. Del Tredici (2010)
10.1097/00005537-199611000-00009
Laryngeal Activity During Swallow, Phonation, and the Valsalva Maneuver: An Electromyographic Analysis
T. McCulloch (1996)
10.1093/BRAIN/110.2.361
Disturbance of sequential movements in patients with Parkinson's disease.
R. Benecke (1987)
10.1083/JCB.102.2.420
Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle
J. Sanes (1986)
10.1259/0007-1285-64-766-890
Radiological assessment of dysphagia in Parkinson's disease.
J. Stroudley (1991)
10.1212/WNL.39.10.1309
Swallowing abnormalities and their response to treatment in Parkinson's disease
M. Bushmann (1989)
10.1016/j.neulet.2005.11.012
Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology
H. Braak (2006)
10.1136/jnnp.2007.131045
Parkinson’s disease: clinical features and diagnosis
J. Jankovic (2008)
10.1007/s00455-001-0087-3
Prevention of Pneumonia in Elderly Stroke Patients by Systematic Diagnosis and Treatment of Dysphagia: An Evidence-Based Comprehensive Analysis of the Literature
David L. Doggett (2001)
10.1002/mds.10459
SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders
I. Litvan (2003)
10.1016/0924-980X(96)94672-X
Muscle modifications in Parkinson's disease: myoelectric manifestations.
B. Rossi (1996)
10.1111/j.1365-2990.2006.00727.x
α‐Synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects
A. Bloch (2006)
10.1016/S1353-8020(01)00007-4
Motor unit number estimates in idiopathic Parkinson's disease.
J. Caviness (2002)
10.1097/NEN.0b013e318186de48
Lewy Body Pathology Involves Cutaneous Nerves
M. Ikemura (2008)
10.1007/s10561-008-9067-2
The Sun Health Research Institute Brain Donation Program: Description and Eexperience, 1987–2007
T. Beach (2008)
10.1097/PHM.0b013e3181a9ed9b
Is There Muscular Weakness in Parkinson's Disease?
R. Cano-de-la-Cuerda (2010)
10.1007/BF00385794
Prepharyngeal dysphagia in Parkinson's disease
N. Do (2004)
10.1002/ar.1155
Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle
A. B. Borisov (2001)
10.1002/mds.20609
Burden of illness in Parkinson's disease
D. Huse (2005)
10.1007/BF02407121
Neurophysiological basis of swallowing
A. Miller (2006)
10.1007/s004050100401
Abnormal elevation of resting pressure at the upper esophageal sphincter of Parkinson’s disease patients
R. Higo (2001)
10.1097/00006205-199707000-00005
Pathophysiology, assessment, and treatment of Parkinson's disease.
V. Tapper (1997)
10.1177/000348940711600809
Neuromuscular Specializations within Human Pharyngeal Constrictor Muscles
L. Mu (2007)
10.1002/mus.20741
Myosin heavy chain–based fiber types in the adult human cricopharyngeus muscle
L. Mu (2007)
10.5507/BP.2009.010
Peripheral nerve involvement and severity of motor disorder in Parkinson's disease: a correlational study.
Z. Chovancová (2009)
10.1212/WNL.18.7.681
Correlative histochemical study of skeletal muscle after suprasegmental denervation, peripheral nerve section, and skeletal fixation
G. Karpati (1968)
10.1152/AJPCELL.1994.267.6.C1723
Type IIx myosin heavy chain transcripts are expressed in type IIb fibers of human skeletal muscle.
V. Smerdu (1994)
10.1007/s00401-009-0538-8
Unified staging system for Lewy body disorders: correlation with nigrostriatal degeneration, cognitive impairment and motor dysfunction
T. Beach (2009)



This paper is referenced by
10.1371/journal.pone.0186611
Arytenoid cartilage movements are hypokinetic in Parkinson’s disease: A quantitative dynamic computerised tomographic study
L. Perju-Dumbrava (2017)
10.1016/j.parkreldis.2019.12.001
Obstructive sleep apnea, CPAP therapy and Parkinson's disease motor function: A longitudinal study.
Lingrui Meng (2019)
10.1007/s00455-015-9612-7
Alpha-Synuclein Pathology in Sensory Nerve Terminals of the Upper Aerodigestive Tract of Parkinson’s Disease Patients
L. Mu (2015)
10.1152/japplphysiol.00702.2019
Skeletal Muscle Transcriptional Networks Linked to Type I Myofiber Grouping in Parkinson's Disease.
K. M. Lavin (2019)
10.1016/j.clineuro.2020.106249
Effectiveness of expiratory flow acceleration in patients with Parkinson's disease and swallowing deficiency: A preliminary study
G. Riboldazzi (2020)
10.1371/journal.pone.0240366
Functional characterization of extrinsic tongue muscles in the Pink1-/- rat model of Parkinson disease
Tiffany J Glass (2020)
10.11138/FNeur/2017.32.3.137
Obstructive sleep apnea syndrome in Parkinson's disease and other parkinsonisms.
F. Crosta (2017)
10.1007/s00455-019-10052-7
Pharyngeal Area Changes in Parkinson’s Disease and Its Effect on Swallowing Safety, Efficiency, and Kinematics
James A. Curtis (2019)
10.1007/978-3-319-92615-5_8
Drugs and Dysphagia
J. Alonso (2019)
10.1111/apha.13195
The sympathetic nervous system regulates skeletal muscle motor innervation and acetylcholine receptor stability
A. Z. Rodrigues (2019)
10.1016/j.cgh.2014.08.031
Emergence of deglutology: a transdisciplinary field.
A. Babaei (2014)
10.1097/NEN.0b013e3182801cde
Alpha-synuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson disease.
L. Mu (2013)
10.1055/s-0038-1627463
Immunohistochemical Detection of Motor Endplates in the Long‐Term Denervated Muscle
L. Mu (2018)
10.1016/j.amjmed.2013.11.014
Perioperative management of patients with Parkinson's disease.
L. Katus (2014)
10.1007/174_2017_118
Dysphagia in Parkinson’s Disease
Emilia Michou (2017)
10.1007/s11910-018-0889-4
Imaging the Autonomic Nervous System in Parkinson’s Disease
K. Knudsen (2018)
10.1186/s12883-015-0362-9
Rate of aspiration pneumonia in hospitalized Parkinson’s disease patients: a cross-sectional study
D. Martinez-Ramirez (2015)
10.5535/arm.2016.40.2.190
Assessment of Oropharyngeal Dysphagia in Patients With Parkinson Disease: Use of Ultrasonography
E. H. Oh (2016)
10.2217/nmt-2017-0006
Swallowing in Parkinson's disease: clinical issues and management.
Nick Miller (2017)
Improving the management of Parkinson's disease : the experience of hospitalisation and a novel MRI-based diagnostic tool
S. Muzerengi (2017)
10.14802/jmd.14008
Electrophysiological Evaluation of Oropharyngeal Dysphagia in Parkinson’s Disease
C. Ertekin (2014)
10.11152/mu-2317
The association between jaw-opening strength, geniohyoid muscle thickness and echo intensity measured by ultrasound.
Y. Miura (2020)
10.1093/jnen/nlw103
The Search for a Peripheral Biopsy Indicator of &agr;-Synuclein Pathology for Parkinson Disease
J. Lee (2017)
10.1007/s00455-020-10201-3
Swallowing Assessment in Parkinson’s Disease: Patient and Investigator Reported Outcome Measures are not Aligned
M. R. A. van Hooren (2020)
Success of cricopharyngeal myotomy for specific and non-specific cervical dysphagia.
N. deZoysa (2013)
10.1007/s00455-017-9831-1
Critical Dysphagia is Common in Parkinson Disease and Occurs Even in Early Stages: A Prospective Cohort Study
C. Pflug (2017)
Manejo de la disfunción autonómica en la enfermedad de Parkinson
José Antonio Crespo-Burillo (2015)
10.1111/joor.12824
Effects of Parkinson's disease on molar bite force, electromyographic activity and muscle thickness of the masseter, temporal and sternocleidomastoid muscles: A case-control study.
Edson Donizete Verri (2019)
10.1044/PERSP2.SIG13.93
Mechanisms for Successful Rehabilitation of Cough in Parkinson's Disease Using Expiratory Muscle Strength Training
Alyssa Huff (2017)
10.1038/s41531-017-0017-1
Imaging Parkinson’s disease below the neck
P. Borghammer (2017)
10.5056/jnm16104
Effects of Age on Esophageal Motility: Use of High-resolution Esophageal Impedance Manometry
Young Kwang Shim (2017)
10.1016/j.ijmedinf.2012.10.006
Accurate telemonitoring of Parkinson's disease diagnosis using robust inference system
Indrajit Mandal (2013)
See more
Semantic Scholar Logo Some data provided by SemanticScholar