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Ning F, Lv S, Liu W, Zhang X, Zhao G, Ning W, Liu Z, Yan H, Qin L, Li H, Xu Y. The Effects of Non-Pharmacological Therapies for Dysphagia in Parkinson's Disease: A Systematic Review. J Integr Neurosci 2024; 23:204. [PMID: 39613473 DOI: 10.31083/j.jin2311204] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/23/2024] [Revised: 08/03/2024] [Accepted: 08/28/2024] [Indexed: 12/01/2024] Open
Abstract
BACKGROUND Parkinson's disease (PD) is currently the second most common degenerative neurological disorder globally, with aspiration pneumonia caused by difficulty swallowing being the deadliest complication. The patient's subjective experience and the safety of swallowing have been the main focus of previous evaluations and treatment plans. The effectiveness of treatment may be attributed to the brain's ability to adapt and compensate. However, there is a need for more accurate assessment methods for dysphagia and further research on how treatment protocols work. OBJECTIVE This systematic review was designed to assess the effectiveness and long-term impact of published treatment options for swallowing disorders in patients with PD. METHODS In adherence to the Preferred Reporting Items for Reviews and Meta-analysis (PRISMA) guidelines, we conducted a systematic review where we thoroughly searched multiple databases (PubMed, Web of Science, Elsevier, and Wiley) for clinical studies published in various languages until December, 2023. Two reviewers evaluated the studies against strict inclusion/exclusion criteria. RESULTS This systematic review included a total of 15 studies, including 523 participants, involving six treatment approaches, including breath training, deep brain stimulation, reduction of upper esophageal sphincter (UES) pressure, transcranial magnetic stimulation, postural compensation, and video-assisted swallowing therapy. Primary outcomes included video fluoroscopic swallowing study (VFSS), fiberoptic endoscopic evaluation of swallowing (FEES), high-resolution pharyngeal impedance manometry (HPRIM), and functional magnetic resonance imaging (fMRI). CONCLUSION Treatments that reduce UES resistance may be an effective way to treat dysphagia in PD patients. HRPIM can quantify pressure changes during the pharyngeal period to identify patients with reduced swallowing function earlier. However, due to the limited number of randomized controlled trials (RCTs) included and the high risk of bias in some studies, large-scale RCTs are needed in the future, and objective indicators such as HRPIM should be used to determine the effectiveness and long-term impact of different therapies on dysphagia in PD patients.
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Affiliation(s)
- Fangli Ning
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Shi Lv
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Wenxin Liu
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Xinlei Zhang
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Guohua Zhao
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Wenjing Ning
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Ziyuan Liu
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Han Yan
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Lei Qin
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Hu Li
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
| | - Yuzhen Xu
- Department of Rehabilitation, The Second Affiliated Hospital of Shandong First Medical University, 271000 Taian, Shandong, China
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Kerschner A, Hassan H, Kern M, Edeani F, Mei L, Sanvanson P, Shaker R, Yu E. Parkinson's disease is associated with low striated esophagus contractility potentially contributing to the development of dysphagia. Neurogastroenterol Motil 2024; 36:e14822. [PMID: 38798058 PMCID: PMC11246227 DOI: 10.1111/nmo.14822] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/18/2023] [Revised: 05/03/2024] [Accepted: 05/09/2024] [Indexed: 05/29/2024]
Abstract
BACKGROUND Parkinson's disease (PD) is the second most common neurodegenerative disorder, and more than 80% of PD patients will develop oropharyngeal dysphagia. Despite its striated histology, proximity to airway, and potential negative impact of its dysfunction on bolus transport and airway safety, the contractile function of the striated esophagus in PD patients has not been systematically studied. METHODS Using our repository of clinical manometry and the Milwaukee ManoBank, we analyzed high-resolution manometry (HRM) studies of 20 PD patients, mean age 69.1 (range 38-87 years); 30 non-PD patients with dysphagia, mean age 64.0 (44-86 years); and 32 healthy volunteers, mean age 65.3 (39-86 years). Patients with abnormal findings based on Chicago Classification 4.0 were identified. Repeat analysis was performed in 20% of the manometric tracings by a different investigator with inter-rater concordance between 0.91 and 0.99. KEY RESULTS The striated esophageal contractile integral in PD patients was significantly lower than that in non-PD dysphagic patients and healthy controls (p = 0.03 and <0.01, respectively). This significant difference persisted after excluding patients with concurrent Chicago Classification motility disorders (p = 0.02 and 0.01, respectively). In both analyses, the distal esophageal contractile integral did not show any significant difference between groups (p = 0.58 and 0.93, respectively). CONCLUSIONS & INFERENCES PD is associated with a significant decrease in striated esophagus contractility compared to non-PD and healthy controls. This finding may play a pathophysiologic role in development of dysphagia in this patient population.
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Affiliation(s)
- Alexander Kerschner
- Department of Internal Medicine, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Hamza Hassan
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Mark Kern
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Francis Edeani
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Ling Mei
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Patrick Sanvanson
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Reza Shaker
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
| | - Elliot Yu
- Division of Gastroenterology and Hepatology, The Hub for Collaborative Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
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Sasegbon A, Cheng I, Labeit B, Lapa S, Rommel N, Hamdy S. New and Evolving Treatments for Neurologic Dysphagia. Drugs 2024; 84:909-932. [PMID: 38954267 DOI: 10.1007/s40265-024-02064-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 06/06/2024] [Indexed: 07/04/2024]
Abstract
Despite swallowing being a frequently performed daily function, it is highly complex. For a safe swallow to occur, muscles within the head, neck, and thorax need to contract in a concerted pattern, controlled by several swallowing centers at multiple levels of the central nervous system, including the midbrain, cerebral cortex, and cerebellum in addition to five cranial nerves. Dysphagia, or difficulty swallowing, is caused by a long list of pathologic processes and diseases, which can interfere with various stages along the swallowing sensorimotor pathway. When present, dysphagia leads to increased mortality, morbidity, hospital length of stay, and reduced quality of life. Current dysphagia management approaches, such as altering the texture and consistency of foods and fluids and teaching patients rehabilitative exercises, have been broadly unchanged for many years and, in the case of texture modification, are of uncertain effectiveness. However, evidence is emerging in support of new medication-based and neuromodulatory treatment approaches. Regarding medication-based therapies, most research has focused on capsaicinoids, which studies have shown are able to improve swallowing in patients with post-stroke dysphagia. Separately, albeit convergently, in the field of neuromodulation, there is a growing and positive evidential base behind three non-invasive brain stimulation techniques: repetitive transcranial magnetic stimulation (rTMS), transcranial direct current stimulation (TDCS), and pharyngeal electrical stimulation (PES). Should some or all of these emerging therapies fulfill their promise, dysphagia-related patient outcomes may be improved. This paper describes the current state of our understanding regarding new medication and neuromodulation-based neurogenic oropharyngeal dysphagia treatments.
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Affiliation(s)
- Ayodele Sasegbon
- Division of Diabetes, Endocrinology and Gastroenterology, Faculty of Biology, Medicine and Health, School of Medical Sciences, Centre for Gastrointestinal Sciences, University of Manchester, Manchester, UK
| | - Ivy Cheng
- Division of Diabetes, Endocrinology and Gastroenterology, Faculty of Biology, Medicine and Health, School of Medical Sciences, Centre for Gastrointestinal Sciences, University of Manchester, Manchester, UK
- Academic Unit of Human Communication, Learning, and Development, Faculty of Education, The University of Hong Kong, Hong Kong, China
- Institute for Biomagnetism and Biosignal Analysis, University of Münster, Münster, Germany
- Universitätsklinikum Münster, Münster, Germany
| | - Bendix Labeit
- Department of Neurology, Medical Faculty, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
| | - Sriramya Lapa
- Department of Neurology, Goethe University and University Hospital, Frankfurt, Germany
| | - Nathalie Rommel
- Deglutology, Experimental Otorhinolaryngology, Department of Neurosciences, University of Leuven, Leuven, Belgium
- Department of Gastroenterology, Neurogastroenterology and Motility, University Hospitals Leuven, Leuven, Belgium
| | - Shaheen Hamdy
- Division of Diabetes, Endocrinology and Gastroenterology, Faculty of Biology, Medicine and Health, School of Medical Sciences, Centre for Gastrointestinal Sciences, University of Manchester, Manchester, UK.
- Centre for Gastrointestinal Sciences, Salford Royal Foundation Trust, University of Manchester, Clinical Sciences Building, Manchester, Eccles Old Road, Salford, M6 8HD, UK.
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Janssen Daalen JM, van den Bergh R, Prins EM, Moghadam MSC, van den Heuvel R, Veen J, Mathur S, Meijerink H, Mirelman A, Darweesh SKL, Evers LJW, Bloem BR. Digital biomarkers for non-motor symptoms in Parkinson's disease: the state of the art. NPJ Digit Med 2024; 7:186. [PMID: 38992186 PMCID: PMC11239921 DOI: 10.1038/s41746-024-01144-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/05/2024] [Accepted: 05/22/2024] [Indexed: 07/13/2024] Open
Abstract
Digital biomarkers that remotely monitor symptoms have the potential to revolutionize outcome assessments in future disease-modifying trials in Parkinson's disease (PD), by allowing objective and recurrent measurement of symptoms and signs collected in the participant's own living environment. This biomarker field is developing rapidly for assessing the motor features of PD, but the non-motor domain lags behind. Here, we systematically review and assess digital biomarkers under development for measuring non-motor symptoms of PD. We also consider relevant developments outside the PD field. We focus on technological readiness level and evaluate whether the identified digital non-motor biomarkers have potential for measuring disease progression, covering the spectrum from prodromal to advanced disease stages. Furthermore, we provide perspectives for future deployment of these biomarkers in trials. We found that various wearables show high promise for measuring autonomic function, constipation and sleep characteristics, including REM sleep behavior disorder. Biomarkers for neuropsychiatric symptoms are less well-developed, but show increasing accuracy in non-PD populations. Most biomarkers have not been validated for specific use in PD, and their sensitivity to capture disease progression remains untested for prodromal PD where the need for digital progression biomarkers is greatest. External validation in real-world environments and large longitudinal cohorts remains necessary for integrating non-motor biomarkers into research, and ultimately also into daily clinical practice.
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Affiliation(s)
- Jules M Janssen Daalen
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands.
| | - Robin van den Bergh
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands
| | - Eva M Prins
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands
| | - Mahshid Sadat Chenarani Moghadam
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands
| | - Rudie van den Heuvel
- HAN University of Applied Sciences, School of Engineering and Automotive, Health Concept Lab, Arnhem, The Netherlands
| | - Jeroen Veen
- HAN University of Applied Sciences, School of Engineering and Automotive, Health Concept Lab, Arnhem, The Netherlands
| | | | - Hannie Meijerink
- ParkinsonNL, Parkinson Patient Association, Bunnik, The Netherlands
| | - Anat Mirelman
- Tel Aviv University, Sagol School of Neuroscience, Department of Neurology, Faculty of Medicine, Laboratory for Early Markers of Neurodegeneration (LEMON), Center for the Study of Movement, Cognition, and Mobility (CMCM), Tel Aviv, Israel
| | - Sirwan K L Darweesh
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands
| | - Luc J W Evers
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands
- Radboud University, Institute for Computing and Information Sciences, Nijmegen, The Netherlands
| | - Bastiaan R Bloem
- Radboud university medical center, Donders Institute for Brain, Cognition and Behaviour, Department of Neurology, Center of Expertise for Parkinson & Movement Disorders, Nijmegen, The Netherlands.
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Flanagan R, Rusch C, Lithander FE, Subramanian I. The missing piece of the puzzle - The key role of the dietitian in the management of Parkinson's disease. Parkinsonism Relat Disord 2024; 121:106021. [PMID: 38326170 DOI: 10.1016/j.parkreldis.2024.106021] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/21/2023] [Revised: 01/29/2024] [Accepted: 01/30/2024] [Indexed: 02/09/2024]
Abstract
The current paradigm for the multidisciplinary management of Parkinson's Disease (PD) does not include regular nutritional assessment despite research showing that 90 % of people living with Parkinson's (PwP) lack access to basic dietetic services. Since many non-motor symptoms such as dysphagia, constipation and orthostatic hypotension and PD complications such as weight loss and sarcopenia can be improved through dietary intervention, dietitians are a critical missing piece of the PD management puzzle. This paper serves to review the role of dietitians and medical nutrition therapy in management of PD as well as a call to action for future studies to investigate improvement of nutritional status and quality of life for all PwP.
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Affiliation(s)
| | - Carley Rusch
- Food Science and Human Nutrition Department, Center for Nutritional Sciences, University of Florida, Gainesville, FL, USA; Department of Neurology, Norman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, FL, USA
| | | | - Indu Subramanian
- Parkinson's Disease Research, Education, and Clinical Center, Greater Los Angeles Veterans Affairs Medical Center, Los Angeles, CA, USA; Department of Neurology, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
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Pasricha TS, Guerrero-Lopez IL, Kuo B. Management of Gastrointestinal Symptoms in Parkinson's Disease: A Comprehensive Review of Clinical Presentation, Workup, and Treatment. J Clin Gastroenterol 2024; 58:211-220. [PMID: 38260966 PMCID: PMC10855995 DOI: 10.1097/mcg.0000000000001961] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/07/2023] [Accepted: 12/11/2023] [Indexed: 01/24/2024]
Abstract
Gastrointestinal symptoms in Parkinson's disease (PD) are among the most prevalent and debilitating of complications and present unique diagnostic and management challenges. Patients with PD commonly experience dysphagia, nausea, bloating, and constipation related to pathologic involvement of the enteric nervous system. In turn, gastrointestinal complications may impact motor fluctuations and the efficacy of levodopa therapy. This review will explore the common gastrointestinal manifestations of PD with an emphasis on clinical presentation, workup, and treatment strategies.
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Affiliation(s)
- Trisha S. Pasricha
- Division of Gastroenterology, Massachusetts General Hospital
- Harvard Medical School, Boston, MA
| | | | - Braden Kuo
- Division of Gastroenterology, Massachusetts General Hospital
- Harvard Medical School, Boston, MA
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Gandor F, Berger L, Gruber D, Warnecke T, Vogel A, Claus I. [Dysphagia in Parkinsonian Syndromes]. DER NERVENARZT 2023; 94:685-693. [PMID: 37115255 DOI: 10.1007/s00115-023-01475-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 03/08/2023] [Indexed: 04/29/2023]
Abstract
Dysphagia is a clinically relevant problem in Parkinson's disease as well as in atypical Parkinsonian syndromes, such as multiple system atrophy and diseases from the spectrum of 4‑repeat tauopathies, which affect most patients to a varying degree in the course of their disease. This results in relevant restrictions in daily life due to impaired intake of food, fluids, and medication with a subsequent reduction in quality of life. This article not only gives an overview of the pathophysiological causes of dysphagia in the various Parkinson syndromes, but also presents screening, diagnostic and treatment procedures that have been investigated for the different diseases.
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Affiliation(s)
- F Gandor
- Neurologisches Fachkrankenhaus für Bewegungsstörungen/Parkinson, Str. nach Fichtenwalde 16, 14547, Beelitz-Heilstätten, Deutschland.
- Klinik für Neurologie, Otto-von-Guericke Universität Magdeburg, Magdeburg, Deutschland.
| | - L Berger
- Neurologisches Fachkrankenhaus für Bewegungsstörungen/Parkinson, Str. nach Fichtenwalde 16, 14547, Beelitz-Heilstätten, Deutschland
- Klinik für Neurologie, Otto-von-Guericke Universität Magdeburg, Magdeburg, Deutschland
| | - D Gruber
- Neurologisches Fachkrankenhaus für Bewegungsstörungen/Parkinson, Str. nach Fichtenwalde 16, 14547, Beelitz-Heilstätten, Deutschland
- Klinik für Neurologie, Otto-von-Guericke Universität Magdeburg, Magdeburg, Deutschland
| | - T Warnecke
- Klinik für Neurologie und neurologische Frührehabilitation, Klinikum Osnabrück, Osnabrück, Deutschland
| | - A Vogel
- Neurologisches Fachkrankenhaus für Bewegungsstörungen/Parkinson, Str. nach Fichtenwalde 16, 14547, Beelitz-Heilstätten, Deutschland
| | - I Claus
- Klinik für Neurologie mit Institut für translationale Neurologie, Universitätsklinikum Münster, Münster, Deutschland
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Le KHN, Low EE, Yadlapati R. Evaluation of Esophageal Dysphagia in Elderly Patients. Curr Gastroenterol Rep 2023; 25:146-159. [PMID: 37312002 PMCID: PMC10726678 DOI: 10.1007/s11894-023-00876-7] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 05/10/2023] [Indexed: 06/15/2023]
Abstract
PURPOSE OF REVIEW While guidelines exist for the evaluation and management of esophageal dysphagia in the general population, dysphagia disproportionately affects the elderly. In this article, we reviewed the literature on evaluating esophageal dysphagia in elderly patients and proposed a diagnostic algorithm based on this evidence. RECENT FINDINGS In older patients, dysphagia is often well compensated for by altered eating habits and physiologic changes, underreported by patients, and missed by healthcare providers. Once identified, dysphagia should be differentiated into oropharyngeal and esophageal dysphagia to guide diagnostic workup. For esophageal dysphagia, this review proposes starting with endoscopy with biopsies, given its relative safety even in older patients and potential for interventional therapy. If endoscopy shows a structural or mechanical cause, then further cross-sectional imaging should be considered to assess for extrinsic compression, and same session endoscopic dilation should be considered for strictures. If biopsies and endoscopy are normal, then esophageal dysmotility is more likely, and high-resolution manometry and additional workup should be performed following the updated Chicago Classification. Even after diagnosis of the root cause, complications including malnutrition and aspiration pneumonia should also be assessed and monitored, as they both result from and can further contribute to dysphagia. The successful evaluation of esophageal dysphagia in elderly patients requires a thorough, standardized approach to collecting a history, selection of appropriate diagnostic workup, and assessment of risk of potential complications, including malnutrition and aspiration.
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Affiliation(s)
| | - Eric E Low
- Department of Gastroenterology and Hepatology, University of California, San Diego, CA, USA
| | - Rena Yadlapati
- Department of Gastroenterology and Hepatology, University of California, San Diego, CA, USA.
- , La Jolla, CA, USA.
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Rudisch DM, Krasko MN, Burdick R, Broadfoot CK, Rogus-Pulia N, Ciucci MR. Dysphagia in Parkinson Disease: Part I - Pathophysiology and Diagnostic Practices. CURRENT PHYSICAL MEDICINE AND REHABILITATION REPORTS 2023; 11:176-187. [PMID: 37608845 PMCID: PMC10441627 DOI: 10.1007/s40141-023-00392-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/06/2023] [Indexed: 03/30/2023]
Abstract
Purpose of Review Dysphagia affects the majority of individuals with Parkinson disease (PD) and is not typically diagnosed until later in disease progression. This review will cover the current understanding of PD pathophysiology, and provides an overview of dysphagia in PD including diagnostic practices, gaps in knowledge, and future directions. Recent Findings Many non-motor and other motor signs of PD appear in the prodrome prior to the manifestation of hall- mark signs and diagnosis. While dysphagia often presents already in the prodrome, it is not routinely addressed in standard neurology examinations. Summary Dysphagia in PD can result in compromised efficiency and safety of swallowing, which significantly contributes to malnutrition and dehydration, decrease quality of life, and increase mortality. The heterogeneous clinical presentation of PD complicates diagnostic procedures which often leads to delayed treatment. Research has advanced our knowledge of mechanisms underlying PD, but dysphagia is still largely understudied, especially in the prodromal stage.
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Affiliation(s)
- Denis Michael Rudisch
- Department of Surgery, Division of Otolaryngology-Head & Neck Surgery, University of Wisconsin-Madison, 1300 University Ave, Madison, WI 53706, USA
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, 1975 Willow Drive, Madison, WI 53706, USA
| | - Maryann N Krasko
- Department of Surgery, Division of Otolaryngology-Head & Neck Surgery, University of Wisconsin-Madison, 1300 University Ave, Madison, WI 53706, USA
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, 1975 Willow Drive, Madison, WI 53706, USA
| | - Ryan Burdick
- Department of Medicine, Division of Geriatrics and Gerontology, School of Medicine and Public Health, University of Wisconsin-Madison, 1685 Highland Avenue, Madison, WI 53705, USA
- Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison, WI 53705, USA
| | - Courtney K Broadfoot
- Department of Medicine, Division of Geriatrics and Gerontology, School of Medicine and Public Health, University of Wisconsin-Madison, 1685 Highland Avenue, Madison, WI 53705, USA
- Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison, WI 53705, USA
| | - Nicole Rogus-Pulia
- Department of Medicine, Division of Geriatrics and Gerontology, School of Medicine and Public Health, University of Wisconsin-Madison, 1685 Highland Avenue, Madison, WI 53705, USA
- Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison, WI 53705, USA
| | - Michelle R Ciucci
- Department of Surgery, Division of Otolaryngology-Head & Neck Surgery, University of Wisconsin-Madison, 1300 University Ave, Madison, WI 53706, USA
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, 1975 Willow Drive, Madison, WI 53706, USA
- Neuroscience Training Program, University of Wisconsin-Madison, 1111 Highland Ave, Madison, WI 53705, USA
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Wu J, Wang Y, Wang X, Xie Y, Li W. A systematic review and meta-analysis of acupuncture in Parkinson's disease with dysphagia. Front Neurol 2023; 14:1099012. [PMID: 37305760 PMCID: PMC10251408 DOI: 10.3389/fneur.2023.1099012] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/15/2022] [Accepted: 05/15/2023] [Indexed: 06/13/2023] Open
Abstract
Objective The systematic review and meta-analysis aimed to comprehensively evaluate acupuncture's efficacy and safety in treating dysphagia in Parkinson's disease (PD). Methods We searched PubMed, Cochrane Library, Embase, Web of Science, China Knowledge Infrastructure (CNKI), China Science Journal Database (VIP), Wan-fang Database, and the China Biomedical Literature Service System (CBM) for randomized controlled trials (RCTs) comparing the efficacy of acupuncture alone or in combination with control treatment in improving dysphagia by October 2022. The degree of dysphagia was the primary outcome indicator, with secondary outcomes including serum albumin (ALB) and hemoglobin (Hb) levels, the incidence of pneumonia, and adverse events. Two investigators independently extracted information according to the inclusion and exclusion criteria. Data synthesis was calculated by RevMan (V.5.4.1) software. Results This study included ten randomized controlled trials with 724 patients. Most RCTs have a high or uncertain risk of bias due to the lack of a blinded design. Meta-analysis showed that acupuncture combined with control treatment was superior to control treatment alone in improving Videofluoroscopic Swallowing Study (VFSS) scores (MD: 1.48; 95% CI: 1.16, 1.81; P < 0.00001) and reducing Standardized Swallowing Assessment (SSA) scores (MD: -3.08; 95% CI: -4.01, -2.15; P < 0.00001). Acupuncture combined with control therapy has a more significant benefit in improving the clinical efficiency of dysphagia in PD (RR: 1.40; 95%CI: 1.25, 1.58; P < 0.00001). Compared to the control group without acupuncture, acupuncture improved the nutritional status of patients and increased their serum ALB (MD: 3.38, 95%CI: 1.83, 4.92, P < 0.00001) and Hb levels (MD: 7.66; 95%CI: 5.57, 9.75; P < 0.00001). Three RCTs reported that the rate of pulmonary infections in the acupuncture group was lower than without acupuncture intervention (RR: 0.29, 95% CI: 0.14, 0.63; P = 0.001). Conclusion Acupuncture could be recommended as an adjunctive treatment for dysphagia in PD. However, due to the high risk of bias in the included studies, more high-quality evidence is needed to confirm the efficacy and safety of acupuncture for dysphagia in PD. Systematic review registration https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42022370221.
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Affiliation(s)
- Jing Wu
- Basic Medical School of Chengdu University of Traditional Chinese Medicine, Chengdu, China
| | - Yi Wang
- Basic Medical School of Chengdu University of Traditional Chinese Medicine, Chengdu, China
| | - Xueyan Wang
- Clinical Medical School of Chengdu University of Traditional Chinese Medicine, Chengdu, China
| | - Yujia Xie
- Basic Medical School of Chengdu University of Traditional Chinese Medicine, Chengdu, China
| | - Weihong Li
- Basic Medical School of Chengdu University of Traditional Chinese Medicine, Chengdu, China
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Winiker K, Kertscher B. Behavioural interventions for swallowing in subjects with Parkinson's disease: A mixed methods systematic review. INTERNATIONAL JOURNAL OF LANGUAGE & COMMUNICATION DISORDERS 2023. [PMID: 36951546 DOI: 10.1111/1460-6984.12865] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/11/2022] [Accepted: 02/14/2023] [Indexed: 06/18/2023]
Abstract
BACKGROUND Dysphagia is prevalent in subjects with Parkinson's disease (PD). Swallowing intervention to improve or maintain swallowing function is of major importance as dysphagia may considerably impact physical and psycho-social health. AIMS A mixed methods systematic review was conducted to summarize and appraise literature reporting (1) effects of behavioural interventions for swallowing in individuals with PD; and (2) participants' perspectives of swallowing interventions. METHODS & PROCEDURES Electronic databases were searched systematically in July 2020 for articles published between 2014 and 2020. In addition, studies published between 2000 and 2014 were identified non-systematically through previous reviews. Peer-reviewed quantitative and qualitative research in English or German documenting behavioural interventions for swallowing in individuals with a diagnosis of PD was eligible for inclusion. Participants at all disease stages were included. Behavioural interventions included rehabilitative and compensatory strategies. Studies reporting swallowing outcomes with and without a comparative group were included. For each study, the National Health and Medical Research Council level of evidence was defined. Included studies were critically appraised using the Standard Quality Assessment Criteria for Evaluating Primary Research Papers from a Variety of Fields. An integrated synthesis was performed after separate analysis of effect data and data reflecting participants' experiences. This review was conducted based on published JBI methodology and the guideline from the Preferred Reporting Items for Systematic Reviews and Meta-Analysis system was followed. MAIN CONTRIBUTION A total of 33 studies published in English met the inclusion criteria. Thirty-one studies reported quantitative data, one was qualitative and one was mixed methods. Intervention effects on swallowing function, swallowing safety and swallowing-related quality of life were reported for various treatment approaches. Three studies explored how participants perceived the intervention. Overriding themes including subjects' views regarding treatment schedules and levels of effort or comfort associated with the intervention were identified across these studies. Combining evidence of intervention effects and subjects' experiences was possible for one rehabilitative and one compensatory intervention. CONCLUSIONS & IMPLICATIONS Beneficial effects of swallowing interventions have been reported; however, most experiments were case studies of variable methodological quality. Randomized-controlled trials with robust methodology to explore treatment effects in larger samples is needed to guide clinical practice. Research reporting subjects' views is scarce. More studies exploring how individuals perceive behavioural interventions for swallowing are necessary to inform clinical decision-making. WHAT THIS PAPER ADDS What is already known on the subject Dysphagia is common in individuals with PD. Swallowing intervention is of major importance as dysphagia may negatively affect physical and psycho-social health of subjects with PD. What this study adds Beneficial effects of behavioural interventions for swallowing, including rehabilitative and compensatory strategies, have been reported; however, available data are mostly based on case studies of variable quality. Data on how participants perceive specific behavioural interventions are lacking. Based on the available data, integration of efficacy data and individuals' experiences is limited. What are the clinical implications of this work? Given the current evidence of intervention effects and individuals' views on behavioural treatment strategies, interventions implemented into clinical practice require careful evaluation on a case-by-case basis. More high-quality research is needed to examine interventions' short- and long-term effects in larger samples to guide clinical practice. In addition to studies evaluating intervention effects, research exploring participants' experiences with interventions is required as a foundation for clinical decision-making.
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Affiliation(s)
- Katharina Winiker
- Department of Research and Development, Swiss University of Speech and Language Sciences SHLR, Rorschach, Switzerland
| | - Berit Kertscher
- Institute for Therapy & Rehabilitation, Cantonal Hospital Winterthur, Winterthur, Switzerland
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Shaibdat NS, Ahmad N, Azmin S, Ibrahim NM. Causes, factors, and complications associated with hospital admissions among patients with Parkinson's disease. Front Neurol 2023; 14:1136858. [PMID: 36959822 PMCID: PMC10027758 DOI: 10.3389/fneur.2023.1136858] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/03/2023] [Accepted: 02/06/2023] [Indexed: 03/09/2023] Open
Abstract
Introduction Patients with Parkinson's disease (PD) are at a higher risk of hospital admissions compared to the general population. We studied the causes and factors associated with admissions among patients with PD over 6 years. Methods We included all PD admissions between 1 January 2016 and 31 December 2021. Other causes of parkinsonism were excluded. Causes of admissions were divided into PD-related (direct or indirect) or non-PD-related. The type of admission was categorized into emergency or elective. Results We identified 605 hospital admissions (259 patients with PD); 345 (57.0%) were PD-related and 260 (43%) were non-PD-related. Emergency PD admissions contributed to 50.4% of all admissions, most commonly from respiratory infection (23%). PD admissions in comparison to non-PD admissions were associated with worse disease severity (HY ≥ 3; p < 0.001), longer disease duration [8.71 (SD 6.23) vs. 6.60 (SD 5.39) years; p < 0.001], and longer hospital stay [7.70 (SD 5.89) vs. 6.42 (SD 7.63) days; p = 0.020]. Non-PD admissions were associated with more comorbidities (97.3%; p = 0.013). There were 124 (20.5%) complications and 31 deaths (5.1%). A total of 29 deaths were due to respiratory infection and 3 deaths were due to COVID-19 pneumonia. Emergency admission (PD- and non-PD-related; p = 0.001) and respiratory-related causes (p < 0.001) were predictors of unfavorable hospital admission outcomes (death and complications). Conclusion Respiratory infection was the leading cause of hospital admission and a significant independent predictor of unfavorable hospital admission outcomes (death and complications). PD-related admissions were associated with disease severity and led to more complications and longer hospital stays. Non-PD-related admissions were associated with comorbidities.
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Affiliation(s)
- Navena Sharma Shaibdat
- Department of Medicine, Hospital Canselor Tuanku Muhriz, Faculty of Medicine, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia
| | - Norfazilah Ahmad
- Department of Community Health, Faculty of Medicine, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia
| | - Shahrul Azmin
- Department of Medicine, Hospital Canselor Tuanku Muhriz, Faculty of Medicine, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia
| | - Norlinah Mohamed Ibrahim
- Department of Medicine, Hospital Canselor Tuanku Muhriz, Faculty of Medicine, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia
- *Correspondence: Norlinah Mohamed Ibrahim ;
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13
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Youn J, Umemoto G, Oh E, Park J, Jang W, Oh YS, Kim HT, Cho JW, Fujioka S, Tsuboi Y. Cardiac sympathetic denervation could be associated with dysphagia in Parkinson's disease. Front Neurol 2022; 13:1010006. [PMID: 36303556 PMCID: PMC9592804 DOI: 10.3389/fneur.2022.1010006] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2022] [Accepted: 09/20/2022] [Indexed: 11/13/2022] Open
Abstract
BackgroundDysphagia is an important non-motor symptom that is closely associated with quality of living and mortality in Parkinson's disease (PD). However, the pathophysiology of dysphagia in PD remains inconclusive. We tried to confirm whether the occurrence of dysphagia could be related to sympathetic degeneration using cardiac 123I-metaiodobenzylguanidine (MIBG) scintigraphy.MethodsWe prospectively recruited 27 PD patients and classified them into two groups (PD with dysphagia vs. PD without dysphagia) by Swallowing Disturbance Questionnaire (SDQ) score and compared the clinical characteristics, videofluoroscopic swallowing study (VFSS) findings and parameters from cardiac MIBG scintigraphy.ResultsThe mean early and late H/M ratios were significantly lower in the PD with dysphagia group than those in the PD without dysphagia group (1.39 ± 0.21 vs. 1.86 ± 0.21, p < 0.01; 1.26 ± 0.18 vs. 1.82 ± 0.29, p < 0.01). In the correlation analysis, both the early and late H/M ratios were negatively correlated with the SDQ score and total VDS score (r = −0.65, p < 0.01; r = −0.53, p < 0.01; r = −0.65, p < 0.01, r = −0.58, p < 0.01).ConclusionWe confirmed that cardiac sympathetic denervation might be associated with the presence and severity of dysphagia. This finding indicates that dysphagia in PD could be associated with a nondopaminergic mechanism.
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Affiliation(s)
- Jinyoung Youn
- Department of Neurology, Samsung Medical Center, School of Medicine, Sungkyunkwan University, Seoul, South Korea
| | - George Umemoto
- Swallowing Disorders Center, Fukuoka University Hospital, Fukuoka, Japan
| | - Eungseok Oh
- Department of Neurology, Chungnam National University College of Medicine, Chungnam National University Hospital, Daejeon, South Korea
| | - Jinse Park
- Department of Neurology, Inje University, Haeundae Paik Hospital, Busan, South Korea
| | - Wooyoung Jang
- Department of Neurology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, South Korea
- *Correspondence: Wooyoung Jang
| | - Yoon-Sang Oh
- Department of Neurology, College of Medicine, The Catholic University of Korea, Seoul, South Korea
| | - Hee-Tae Kim
- Department of Neurology, Hanyang University College of Medicine, Seoul, South Korea
| | - Jin Whan Cho
- Department of Neurology, Samsung Medical Center, School of Medicine, Sungkyunkwan University, Seoul, South Korea
| | - Shinsuke Fujioka
- Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
- Shinsuke Fujioka
| | - Yoshio Tsuboi
- Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
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Bhidayasiri R, Phuenpathom W, Tan AH, Leta V, Phumphid S, Chaudhuri KR, Pal PK. Management of dysphagia and gastroparesis in Parkinson's disease in real-world clinical practice - Balancing pharmacological and non-pharmacological approaches. Front Aging Neurosci 2022; 14:979826. [PMID: 36034128 PMCID: PMC9403060 DOI: 10.3389/fnagi.2022.979826] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/28/2022] [Accepted: 07/18/2022] [Indexed: 12/23/2022] Open
Abstract
Gastrointestinal (GI) issues are commonly experienced by patients with Parkinson's disease (PD). Those that affect the lower GI tract, such as constipation, are the most frequently reported GI problems among patients with PD. Upper GI issues, such as swallowing dysfunction (dysphagia) and delayed gastric emptying (gastroparesis), are also common in PD but are less well recognized by both patients and clinicians and, therefore, often overlooked. These GI issues may also be perceived by the healthcare team as less of a priority than management of PD motor symptoms. However, if left untreated, both dysphagia and gastroparesis can have a significant impact on the quality of life of patients with PD and on the effectiveness on oral PD medications, with negative consequences for motor control. Holistic management of PD should therefore include timely and effective management of upper GI issues by utilizing both non-pharmacological and pharmacological approaches. This dual approach is key as many pharmacological strategies have limited efficacy in this setting, so non-pharmacological approaches are often the best option. Although a multidisciplinary approach to the management of GI issues in PD is ideal, resource constraints may mean this is not always feasible. In 'real-world' practice, neurologists and PD care teams often need to make initial assessments and treatment or referral recommendations for their patients with PD who are experiencing these problems. To provide guidance in these cases, this article reviews the published evidence for diagnostic and therapeutic management of dysphagia and gastroparesis, including recommendations for timely and appropriate referral to GI specialists when needed and guidance on the development of an effective management plan.
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Affiliation(s)
- Roongroj Bhidayasiri
- Chulalongkorn Centre of Excellence for Parkinson’s Disease and Related Disorders, Department of Medicine, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand
- Academy of Science, Royal Society of Thailand, Bangkok, Thailand
| | - Warongporn Phuenpathom
- Chulalongkorn Centre of Excellence for Parkinson’s Disease and Related Disorders, Department of Medicine, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand
| | - Ai Huey Tan
- Division of Neurology, Department of Medicine, Faculty of Medicine, Universiti Malaya, Kuala Lumpur, Malaysia
| | - Valentina Leta
- Department of Basic and Clinical Neurosciences, The Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology & Neuroscience, Parkinson’s Foundation Centre of Excellence, King’s College London, London, United Kingdom
| | - Saisamorn Phumphid
- Chulalongkorn Centre of Excellence for Parkinson’s Disease and Related Disorders, Department of Medicine, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand
| | - K. Ray Chaudhuri
- Department of Basic and Clinical Neurosciences, The Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology & Neuroscience, Parkinson’s Foundation Centre of Excellence, King’s College London, London, United Kingdom
| | - Pramod Kumar Pal
- National Institute of Mental Health and Neurosciences, Bengaluru, India
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Dilmaghani S, Atieh J, Khanna L, Hosfield EA, Camilleri M, Katzka DA. Severity of dysphagia is associated with hospitalizations and mortality in patients with Parkinson's disease. Neurogastroenterol Motil 2022; 34:e14280. [PMID: 34628711 DOI: 10.1111/nmo.14280] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/26/2021] [Revised: 09/11/2021] [Accepted: 09/27/2021] [Indexed: 02/05/2023]
Abstract
BACKGROUND Aspiration pneumonia is the commonest cause of hospitalizations and death in patients with Parkinson's disease (PD). Among these patients, the relationships between severity of dysphagia, hospitalizations for related complications, and death are not robustly defined. Our aim was to characterize the relationship between PD-related oropharyngeal dysfunction and clinically relevant outcomes. METHODS Retrospective cohort study of 312 patients with PD at a tertiary center who underwent videofluoroscopic swallow studies conducted by expert therapists between 2010 and 2015. Level of swallowing function was represented using the 7-point Functional Oral Intake Scale (FOIS) (7 = normal function). Significance and relative risk calculations utilized Poisson regression. Time to composite outcome of first hospitalization or death was summarized using Kaplan-Meier curve with log-rank test. KEY RESULTS One hundred thirty eight patients had a recorded FOIS score. The prevalence of oropharyngeal dysfunction was 76.1%. The median duration of follow-up was 26.8 months. In multivariate analyses, patients with FOIS 5 (RR = 2.01 [95% CI: 1.22, 3.32]), FOIS 3 (RR = 2.78 [95% CI: 1.75, 4.40]), and FOIS 1 (RR = 2.50 [95% CI: 1.49, 4.20]) were significantly associated with increased risk of hospitalization or death compared to FOIS 7 after co-variate adjustments. GERD was also associated with a significant increased risk of hospitalization or death (RR = 1.28 [95% CI: 1.01, 1.64]). Time to first hospitalization or death was shorter in patients with lower FOIS scores (p < 0.00005). CONCLUSIONS AND INFERENCES Severity of oropharyngeal dysphagia, as measured by the FOIS, is associated with poorer survival and shorter time to hospitalization for dysphagia-related complications, pneumonia, or death in PD.
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Affiliation(s)
- Saam Dilmaghani
- Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Gastroenterology and Hepatology, Rochester, Minnesota, USA
| | - Jessica Atieh
- Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Gastroenterology and Hepatology, Rochester, Minnesota, USA
| | - Lehar Khanna
- Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Gastroenterology and Hepatology, Rochester, Minnesota, USA
| | - Emily A Hosfield
- Division of Speech Pathology, Department of Neurology, Mayo Clinic, Rochester, Minnesota, USA
| | - Michael Camilleri
- Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Gastroenterology and Hepatology, Rochester, Minnesota, USA
| | - David A Katzka
- Clinical Enteric Neuroscience Translational and Epidemiological Research (CENTER), Division of Gastroenterology and Hepatology, Rochester, Minnesota, USA
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16
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Szczesniak MM, Omari TI, Lam TY, Wong M, Mok VCT, Wu JCY, Chiu PWY, Yuen MTY, Tsang RK, Cock C, Sung JJ, Wu P. Evaluation of oropharyngeal deglutitive pressure dynamics in patients with Parkinson's disease. Am J Physiol Gastrointest Liver Physiol 2022; 322:G421-G430. [PMID: 35138164 DOI: 10.1152/ajpgi.00314.2021] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/31/2023]
Abstract
In Parkinson's disease (PD), oropharyngeal dysphagia is common and clinically relevant. The neurophysiology of dysphagia in PD is complex and incompletely understood. The aim of the study was to determine the changes in oropharyngeal deglutitive pressure dynamics in PD and to correlate these with clinical characteristics including dysphagia and PD severity. In prospective consecutive series of 64 patients with PD [mean age: 66.9 ± 8.3 (SD)], we evaluated dysphagia severity clinically as well as with Sydney Swallow Questionnaire (SSQ) and Swallow Quality-of-Life Questionnaire (SWAL-QOL). PD severity was assessed with Movement Disorder Society-Unified Parkinson's Disease Rating Scale (MDS-UPDRS). We used high-resolution pharyngeal impedance manometry (HRPIM) to objectively evaluate swallow function and compared data from 23 age-matched healthy controls [mean age 62.3 ± 9.1 (SD)]. Metrics assessed were upper esophageal sphincter (UES), integrated relaxation pressure (IRP), relaxation time (RT), maximum opening (MaxAdm), and pharyngeal intrabolus pressure (IBP) and pharyngeal contractility (PhCI). Mean MDS-UPDRS score was positively associated with dysphagia severity on SSQ and SWAL-QOL. HRPIM in PD compared with controls showed impaired UES relaxation parameters, with shorter RT, and elevated IRP and IBP. MaxAdm was not affected. The overall pharyngeal contractility was significantly higher in PD. Only the IBP and IRP were associated with PD severity and only IBP was significantly associated with dysphagia severity. UES dysfunction leading to increased flow resistance is common in patients with PD and correlates with dysphagia severity. Increased flow resistance may suggest impaired UES relaxation and/or impaired neuromodulation to bolus volume.NEW & NOTEWORTHY In Parkinson's disease, objective assessment of swallow function with high-resolution impedance manometry identifies upper esophageal sphincter dysfunction leading to increased flow resistance.
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Affiliation(s)
- Michal M Szczesniak
- St George and Sutherland Clinical School, University of NSW, Sydney, Australia.,Department of Gastroenterology and Hepatology, St. George Hospital, Sydney, Australia
| | - Taher I Omari
- College of Medicine and Public Health, Flinders University, Adelaide, Australia
| | - Thomas Y Lam
- Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Marc Wong
- Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Vincent C T Mok
- Margaret K. L. Cheung Research Centre for Management of Parkinsonism, Division of Neurology, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Justin C Y Wu
- Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Philip W Y Chiu
- Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Margaret T Y Yuen
- Division of Esophageal and Upper Gastrointestinal Surgery, Department of Surgery, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, People's Republic of China.,Division of Otorhinolaryngology, Department of Surgery, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, People's Republic of China
| | - Raymond K Tsang
- Division of Otorhinolaryngology, Department of Surgery, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, People's Republic of China
| | - Charles Cock
- College of Medicine and Public Health, Flinders University, Adelaide, Australia
| | - Joseph J Sung
- Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
| | - Peter Wu
- St George and Sutherland Clinical School, University of NSW, Sydney, Australia.,Department of Gastroenterology and Hepatology, St. George Hospital, Sydney, Australia.,Institute of Digestive Disease, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, People's Republic of China
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Warnecke T, Schäfer KH, Claus I, Del Tredici K, Jost WH. Gastrointestinal involvement in Parkinson's disease: pathophysiology, diagnosis, and management. NPJ Parkinsons Dis 2022; 8:31. [PMID: 35332158 PMCID: PMC8948218 DOI: 10.1038/s41531-022-00295-x] [Citation(s) in RCA: 93] [Impact Index Per Article: 31.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2021] [Accepted: 02/23/2022] [Indexed: 12/12/2022] Open
Abstract
Growing evidence suggests an increasing significance for the extent of gastrointestinal tract (GIT) dysfunction in Parkinson's disease (PD). Most patients suffer from GIT symptoms, including dysphagia, sialorrhea, bloating, nausea, vomiting, gastroparesis, and constipation during the disease course. The underlying pathomechanisms of this α-synucleinopathy play an important role in disease development and progression, i.e., early accumulation of Lewy pathology in the enteric and central nervous systems is implicated in pharyngeal discoordination, esophageal and gastric motility/peristalsis impairment, chronic pain, altered intestinal permeability and autonomic dysfunction of the colon, with subsequent constipation. Severe complications, including malnutrition, dehydration, insufficient drug effects, aspiration pneumonia, intestinal obstruction, and megacolon, frequently result in hospitalization. Sophisticated diagnostic tools are now available that permit more detailed examination of specific GIT impairment patterns. Furthermore, novel treatment approaches have been evaluated, although high-level evidence trials are often missing. Finally, the burgeoning literature devoted to the GIT microbiome reveals its importance for neurologists. We review current knowledge about GIT pathoanatomy, pathophysiology, diagnosis, and treatment in PD and provide recommendations for management in daily practice.
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Affiliation(s)
- T Warnecke
- Department of Neurology with Institute of Translational Neurology, University Hospital of Münster, 48149, Münster, Germany
| | - K-H Schäfer
- Research and Transfer Working Group Enteric Nervous System (AGENS), University of Applied Sciences Kaiserslautern, Campus Zweibrücken, 66482, Zweibrücken, Germany
| | - I Claus
- Department of Neurology with Institute of Translational Neurology, University Hospital of Münster, 48149, Münster, Germany
| | - K Del Tredici
- Clinical Neuroanatomy, Department of Neurology, Center for Biomedical Research, University of Ulm, 89081, Ulm, Germany
| | - W H Jost
- Parkinson-Klinik Ortenau, 77709, Wolfach, Germany.
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Pathophysiology and Symptomatology of Drooling in Parkinson’s Disease. Healthcare (Basel) 2022; 10:healthcare10030516. [PMID: 35326994 PMCID: PMC8951596 DOI: 10.3390/healthcare10030516] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/31/2021] [Revised: 03/02/2022] [Accepted: 03/08/2022] [Indexed: 12/29/2022] Open
Abstract
Drooling can present in patients with Parkinson’s disease (PD), and it is manifested as an excessive pooling of saliva inside the oral cavity. Currently, the exact pathophysiological mechanism of drooling in PD is not yet fully explicated. Thus, it becomes crucial to understand if some clinical characteristics may emphasize drooling or if they are just concomitant. In PD, excessive drooling has been associated with a higher burden of non-motor symptoms, such as cognitive impairment, sleep problems, autonomic dysfunction, constipation and orthostatic hypotension, and of worse severity of motor fluctuations and bradykinesia. PD patients with excessive drooling also showed a reduction of striatal DAT availability at DaTSCAN imaging. Excessive drooling in patients with Parkinson’s cannot be attributed to a single factor but to a mixture of factors, including but not limited to impaired nigrostriatal pathways.
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Kuo WY, Huang KH, Kuan YH, Chang YC, Tsai TH, Lee CY. Antidepressants Usage and Risk of Pneumonia Among Elderly Patients With the Parkinson's Disease: A Population-Based Case-Control Study. Front Med (Lausanne) 2022; 9:740182. [PMID: 35252227 PMCID: PMC8896435 DOI: 10.3389/fmed.2022.740182] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2021] [Accepted: 01/05/2022] [Indexed: 11/27/2022] Open
Abstract
The patients with Parkinson's disease (PD) are associated with a higher risk of pneumonia. Antidepressants exert an anticholinergic effect in varying degrees and various classes of antidepressants also can produce a different effect on immune function. The relationship between the risk of pneumonia and the use of antidepressants among elderly patients with PD is unknown. The study investigated the risk of pneumonia associated with the use of antidepressants in elderly patients with PD. This case-control study was based on data from the longitudinal health insurance database in Taiwan. We analyzed the data of 551,975 elderly patients with PD between 2002 and 2018. To reduce the potential confounding caused by unbalanced covariates in non-experimental settings, we used propensity score matching to include older patients without pneumonia to serve as the comparison. The antidepressants in the study included tricyclic antidepressants (TCAs), monoamine oxidase inhibitors (MAOIs), selective serotonin reuptake inhibitors (SSRIs), serotonin, and norepinephrine reuptake inhibitors (SNRIs). The conditional logistic regression was used to investigate the association between antidepressants and pneumonia. Control variables in the study included sex, age, income level, urbanization, Charlson comorbidity index score, and comorbidities related to pneumonia. In terms of TCAs users, compared with patients not receiving TCAs, current users had a lower risk of incident pneumonia (adjusted odds ratio [aOR] = 0.86, 95% CI = 0.82–0.90) and recent users (aOR = 0.83, 95% CI = 0.80–0.87). In terms of MAOIs users, current users had a lower risk of incident pneumonia (aOR = 0.88, 95% CI = 0.83–0.93), recent users (aOR = 0.89, 95% CI = 0.85–0.93). In terms of SSRIs users, current users had a higher risk of incident pneumonia (a OR = 1.13, 95% CI = 1.01–1.17), recent users (aOR = 1.01, 95% CI = 1.06–1.13), and past users (aOR = 1.19, 95% CI = 1.17–1.21). In terms of SNRIs users, past users had a higher risk of incident pneumonia (aOR = 1.07, 95% CI = 1.03–1.10). The incident pneumonia is associated with the use of individuals of different classes of antidepressants. The use of TCAs (such as, amitriptyline and imipramine) had a lower odds of incident pneumonia. The use of MAOIs (such as, selegiline and rasagiline) had a lower odds of pneumonia during recent use. The use of SSRIs (such as, fluoxetine, sertraline, escitalopram, paroxetine, and citalopram) and SNRIs (such as, milnacipran, and venlafaxine) had a higher odds of incident pneumonia.
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Affiliation(s)
- Wei-Yin Kuo
- Department of Health Services Administration, China Medical University, Taichung, Taiwan
| | - Kuang-Hua Huang
- Department of Health Services Administration, China Medical University, Taichung, Taiwan
| | - Yu-Hsiang Kuan
- Department of Pharmacology, Chung Shan Medical University, Taichung, Taiwan
- Department of Pharmacy, Chung Shan Medical University Hospital, Taichung, Taiwan
| | - Yu-Chia Chang
- Department of Long Term Care, National Quemoy University, Kinmen, Taiwan
- Department of Healthcare Administration, Asia University, Taichung, Taiwan
- Department of Medical Research, China Medical University Hospital, Taichung, Taiwan
| | - Tung-Han Tsai
- Department of Health Services Administration, China Medical University, Taichung, Taiwan
| | - Chien-Ying Lee
- Department of Pharmacology, Chung Shan Medical University, Taichung, Taiwan
- Department of Pharmacy, Chung Shan Medical University Hospital, Taichung, Taiwan
- *Correspondence: Chien-Ying Lee
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Zeng W, Fan W, Kong X, Liu X, Liu L, Cao Z, Zhang X, Yang X, Cheng C, Wu Y, Xu Y, Cao X, Xu Y. Altered Intra- and Inter-Network Connectivity in Drug-Naïve Patients With Early Parkinson’s Disease. Front Aging Neurosci 2022; 14:783634. [PMID: 35237144 PMCID: PMC8884479 DOI: 10.3389/fnagi.2022.783634] [Citation(s) in RCA: 13] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2021] [Accepted: 01/17/2022] [Indexed: 12/22/2022] Open
Abstract
The aim of our study was to investigate differences in whole brain connectivity at different levels between drug-naïve individuals with early Parkinson’s disease (PD) and healthy controls (HCs). Resting-state functional magnetic resonance imaging data were collected from 47 patients with early-stage, drug-naïve PD and 50 HCs. Functional brain connectivity was analyzed at the integrity, network, and edge levels; UPDRS-III, MMSE, MOCA, HAMA, and HAMD scores, reflecting the symptoms of PD, were collected for further regression analysis. Compared with age-matched HCs, reduced functional connectivity were mainly observed in the visual (VSN), somatomotor (SMN), limbic (LBN), and deep gray matter networks (DGN) at integrity level [p < 0.05, false discovery rate (FDR) corrected]. Intra-network analysis indicated decreased functional connectivity in DGN, SMN, LBN, and ventral attention networks (VAN). Inter-network analysis indicated reduced functional connectivity in nine pairs of resting-state networks. At the edge level, the LBN was the center of abnormal functional connectivity (p < 0.05, FDR corrected). MOCA score was associated with the intra-network functional connectivity strength (FC) of the DGN, and inter-network FC of the DGN-VAN. HAMA and HAMD scores were associated with the FC of the SMN and DGN, and either the LBN or VAN, respectively. We demonstrated variations in whole brain connections of drug-naïve patients with early PD. Major changes involved the SMN, DGN, LBN, and VSN, which may be relevant to symptoms of early PD. Additionally, our results support PD as a disconnection syndrome.
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Affiliation(s)
- Weiqi Zeng
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Wenliang Fan
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- Hubei Province Key Laboratory of Molecular Imaging, Wuhan, China
| | - Xiangchuang Kong
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- Hubei Province Key Laboratory of Molecular Imaging, Wuhan, China
| | - Xiaoming Liu
- Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- Hubei Province Key Laboratory of Molecular Imaging, Wuhan, China
| | - Ling Liu
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Ziqin Cao
- Department of Chemistry, Emory University, Atlanta, GA, United States
| | - Xiaoqian Zhang
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Xiaoman Yang
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Chi Cheng
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Yi Wu
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Yu Xu
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
| | - Xuebing Cao
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- *Correspondence: Xuebing Cao,
| | - Yan Xu
- Department of Neurology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
- Yan Xu,
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21
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Scott GD, Lim MM, Drake MG, Woltjer R, Quinn JF. Onset of Skin, Gut, and Genitourinary Prodromal Parkinson's Disease: A Study of 1.5 Million Veterans. Mov Disord 2021; 36:2094-2103. [PMID: 33942370 PMCID: PMC8734457 DOI: 10.1002/mds.28636] [Citation(s) in RCA: 24] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2021] [Revised: 04/02/2021] [Accepted: 04/14/2021] [Indexed: 12/20/2022] Open
Abstract
BACKGROUND Prodromal Parkinson's disease of skin, genitourinary, and gastrointestinal systems offers a unique window for understanding early disease pathogenesis and developing disease modifying treatments. However, prior studies are limited by incomplete timing information, small sample size, and lack of adjustment for known confounders. Verifying prodromal timing and identifying new disorders in these accessible organs is critically important given their broad use. OBJECTIVE We aimed to measure onset timing for gastrointestinal, genitourinary, and skin disorders in a large, nationwide clinically characterized cohort of 1.5 million participants. METHODS Patients with Parkinson's disease (n = 303,693) were identified using diagnostic codes in the medical records database of the United States Veterans Affairs healthcare system and were compared 4:1 with matched controls. Disorder prevalence and estimated onset times were assessed for 20 years preceding diagnosis. RESULTS The earliest significantly increased prodromal disorders were gastroesophageal reflux, sexual dysfunction, and esophageal dyskinesia at 17, 16, and 15 years before diagnosis. Estimated onset times for each disorder occurred 5.5 ± 3.4 years before the first measured increase. The earliest estimated onset times were smell/taste, upper gastrointestinal tract, and sexual dysfunction at 20.9, 20.6, and 20.1 years before diagnosis. Onset times for constipation and urinary dysfunction were notably longer by 7 and 9 years compared to prior studies in sleep disorder patients. Dermatophytosis and prostatic hypertrophy were identified as new high prevalence prodromal disorders. CONCLUSIONS Gastrointestinal, genitourinary, and skin disorders manifest decades before diagnosis of Parkinson's disease, reiterating their potential as sites for developing early diagnostic testing and understanding pathogenesis.
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Affiliation(s)
- Gregory D. Scott
- Department of Pathology, Oregon Health and Science University, Portland, Oregon, USA
- Department of Pathology and Laboratory Services, VA Portland Medical Center, Portland, Oregon, USA
| | - Miranda M. Lim
- Department of Neurology, Oregon Health and Science University, Portland, Oregon, USA
- Department of Neurology, VA Portland Medical Center, Portland, Oregon, USA
- Department of Pulmonary and Critical Care Medicine, Oregon Health and Science University, Portland, Oregon, USA
| | - Matthew G. Drake
- Department of Pulmonary and Critical Care Medicine, Oregon Health and Science University, Portland, Oregon, USA
| | - Randy Woltjer
- Department of Pathology, Oregon Health and Science University, Portland, Oregon, USA
| | - Joseph F. Quinn
- Department of Neurology, Oregon Health and Science University, Portland, Oregon, USA
- Department of Neurology, VA Portland Medical Center, Portland, Oregon, USA
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22
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The upper esophageal sphincter in the high-resolution manometry era. Langenbecks Arch Surg 2021; 406:2611-2619. [PMID: 34462811 DOI: 10.1007/s00423-021-02319-1] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2021] [Accepted: 08/26/2021] [Indexed: 12/13/2022]
Abstract
BACKGROUND The evaluation of the upper esophageal sphincter (UES) has been neglected during routine manometric tests for decades, mostly due to the limitations of the conventional manometry which were eventually overcome by high-resolution manometry (HRM). METHODS This study reviewed the current knowledge of the manometric evaluation of the UES in health and disease in the HRM era. RESULTS We found that HRM allowed more precise measurements, in addition to the parameters as compared to conventional manometry, but most of them still need confirmation of the clinical significance. The parameters used to evaluate the UES were extension, basal pressure, residual pressure, relaxation duration, relaxation time to nadir, recovery time, intrabolus pressure, and deglutitive sphincter resistance. UES may be affected by different diseases: achalasia (UES is hypertonic with impaired relaxation), gastroesophageal reflux disease (UES is short and hypotonic), globus (UES ranges from normal to impaired relaxation to hypertonic), neurologic diseases (stroke and Parkinson - UES is hypotonic in early-stage to impaired relaxation in end-stage disease), and Zenker's diverticulum (UES has impaired relaxation). CONCLUSION This review shows that UES dysfunction is part of several disease processes and that the study of the UES is possible and valuable with the aid of HRM.
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23
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Cheval M, Villain C, Gay P, Toméo C, Barrou Z, Verny M. A case of type 1 achalasia associated with Parkinson's disease. Rev Neurol (Paris) 2021; 177:1198-1199. [PMID: 34154828 DOI: 10.1016/j.neurol.2020.12.011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/11/2020] [Revised: 12/18/2020] [Accepted: 12/21/2020] [Indexed: 10/21/2022]
Affiliation(s)
- M Cheval
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France.
| | - C Villain
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France
| | - P Gay
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France
| | - C Toméo
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France
| | - Z Barrou
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France
| | - M Verny
- Médecine Sorbonne Université, Centre de Gériatrie, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Assistance Publique Hôpitaux de Paris, 47-83, boulevard de l'hôpital, 75013 Paris, France
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24
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Risk and mortality of aspiration pneumonia in Parkinson's disease: a nationwide database study. Sci Rep 2021; 11:6597. [PMID: 33758213 PMCID: PMC7988066 DOI: 10.1038/s41598-021-86011-w] [Citation(s) in RCA: 36] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/10/2020] [Accepted: 03/09/2021] [Indexed: 11/08/2022] Open
Abstract
This retrospective cohort study investigated the risk and mortality rate due to aspiration pneumonia in patients with Parkinson's disease (PD) using a nationwide database. We identified 10,159 newly diagnosed PD patients between 2004 and 2006, and four age- and sex-matched controls for each PD patient from the National Health Insurance Service database in Korea. We analyzed the relative risk of aspiration pneumonia and mortality after the first occurrence of aspiration pneumonia until 2017. Throughout the study period, PD patients showed a higher incidence of aspiration pneumonia than their matched controls (3.01 vs. 0.59 events per 1,000 person-years), and they were at an increased risk of aspiration pneumonia (hazard ratio = 4.21; 95% confidence interval, 3.87-4.58). After the first occurrence of aspiration pneumonia, the mortality rate of PD patients was 23.9% after one month, 65.2% after 1 year, and 91.8% after 5 years, while that of controls was 30.9%, 67.4%, and 88.9%, respectively. Patients with PD are at an increased risk of aspiration pneumonia, and approximately two-thirds of the patients die within a year after experiencing aspiration pneumonia. Further studies are warranted to prevent aspiration pneumonia and implement proper treatments to prevent death after aspiration pneumonia in patients with PD.
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25
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Patel B, Legacy J, Okun MS, Wheeler-Hegland K, Herndon NE. Response to: The need of reliable warning signs for dysphagia in Parkinson's disease: an often-overlooked issue. Expert Rev Gastroenterol Hepatol 2021; 15:343-344. [PMID: 33131348 DOI: 10.1080/17474124.2021.1842195] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 10/23/2022]
Affiliation(s)
- Bhavana Patel
- Department of Neurology, University of Florida College of Medicine , Gainesville, FL, USA.,Norman Fixel Institute for Neurological Diseases , Gainesville, FL, USA
| | - Joseph Legacy
- Department of Neurology, University of Florida College of Medicine , Gainesville, FL, USA.,Norman Fixel Institute for Neurological Diseases , Gainesville, FL, USA
| | - Michael S Okun
- Department of Neurology, University of Florida College of Medicine , Gainesville, FL, USA.,Norman Fixel Institute for Neurological Diseases , Gainesville, FL, USA
| | - Karen Wheeler-Hegland
- UF Health Rehab Center at Norman Fixel Institute for Neurological Diseases , Gainesville, FL, USA.,Department of Speech, Language and Hearing Sciences, University of Florida , Gainesville, FL, USA
| | - Nicole E Herndon
- UF Health Rehab Center at Norman Fixel Institute for Neurological Diseases , Gainesville, FL, USA.,Department of Speech, Language and Hearing Sciences, University of Florida , Gainesville, FL, USA
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26
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Dibble LE, Ellis TD. The sobering and puzzling reality of rehabilitation referrals for Parkinson disease. Parkinsonism Relat Disord 2021; 83:113-114. [PMID: 33551313 DOI: 10.1016/j.parkreldis.2021.01.016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/20/2020] [Revised: 01/18/2021] [Accepted: 01/21/2021] [Indexed: 11/17/2022]
Affiliation(s)
- Leland E Dibble
- Department of Physical Therapy and Athletic Training, University of Utah, 520 Wakara Way, Salt Lake City, UT, 84108, USA.
| | - Theresa D Ellis
- Department of Physical Therapy and Athletic Training, Boston University College of Health and Rehabilitation Sciences: Sargent College, 635 Commonwealth Avenue, Boston, MA, 02215, USA.
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27
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Groher ME. Dysphagia Unplugged. Dysphagia 2021. [DOI: 10.1016/b978-0-323-63648-3.00001-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/24/2022]
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28
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Mönkemüller K, Fry LC. Gastrointestinal Endoscopy: Considerations. GERIATRIC GASTROENTEROLOGY 2021:879-908. [DOI: 10.1007/978-3-030-30192-7_31] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/04/2025]
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29
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Legacy J, Herndon NE, Wheeler-Hegland K, Okun MS, Patel B. A comprehensive review of the diagnosis and treatment of Parkinson's disease dysphagia and aspiration. Expert Rev Gastroenterol Hepatol 2020; 14:411-424. [PMID: 32657208 PMCID: PMC10405619 DOI: 10.1080/17474124.2020.1769475] [Citation(s) in RCA: 27] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/24/2020] [Accepted: 05/12/2020] [Indexed: 01/29/2023]
Abstract
INTRODUCTION Bulbar dysfunction is common in Parkinson's disease (PD) with more than 80% of affected individuals developing dysphagia during the course of the disease. Symptoms can begin in the preclinical stage and individuals may remain clinically asymptomatic for years. Furthermore, patients may be unaware of swallowing changes, which contributes to the difference between the prevalence of self-reported dysphagia and deficits identified during instrumental evaluations. Dysphagia is underrecognized and contributes to the development of aspiration pneumonia which is the leading cause of death in PD. Dysphagia in PD is complex and not completely understood. Both dopaminergic and nondopaminergic pathways likely underpin dysphagia. AREAS COVERED This comprehensive review will cover the epidemiology, pathophysiology, clinical evaluation, and expert management of dysphagia and aspiration in patients with PD. EXPERT OPINION A multidisciplinary team approach is important to properly identify and manage PD dysphagia. Regular clinical screenings with objective instrumental assessments are necessary for early detection of dysphagia. Studies are needed to better understand the mechanism(s) involved in PD dysphagia, establish markers for early detection and progression, and develop evidence-based treatment options.
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Affiliation(s)
- Joseph Legacy
- Department of Neurology, University of Florida College of Medicine, Gainesville, FL
- Norman Fixel Institute for Neurological Diseases, Gainesville, FL
| | - Nicole E. Herndon
- Norman Fixel Institute for Neurological Diseases, Gainesville, FL
- Department of Speech, Language, and Hearing Sciences, University of Florida, Gainesville, FL
| | - Karen Wheeler-Hegland
- Norman Fixel Institute for Neurological Diseases, Gainesville, FL
- Department of Speech, Language, and Hearing Sciences, University of Florida, Gainesville, FL
| | - Michael S. Okun
- Department of Neurology, University of Florida College of Medicine, Gainesville, FL
- Norman Fixel Institute for Neurological Diseases, Gainesville, FL
| | - Bhavana Patel
- Department of Neurology, University of Florida College of Medicine, Gainesville, FL
- Norman Fixel Institute for Neurological Diseases, Gainesville, FL
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30
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Marano M, Gupta D, Motolese F, Rossi M, Luccarelli V, Altamura C, Di Lazzaro V. Excessive daytime sleepiness is associated to the development of swallowing impairment in a cohort of early stage drug naïve Parkinson's disease patients. J Neurol Sci 2019; 410:116626. [PMID: 31874415 DOI: 10.1016/j.jns.2019.116626] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2019] [Revised: 11/14/2019] [Accepted: 12/10/2019] [Indexed: 11/17/2022]
Abstract
OBJECTIVE The aim of the present study was to investigate the potential predictors of subjectively reported swallowing impairment in a cohort of early-stage and drug naïve Parkinson's disease patients. METHODS A retrospective analysis of the Parkinson Progression Markers Initiative (PPMI) data was conducted. PD patients with score ≥ 1 on MDS-UPDRS "item 2.3" and on SCOPA-AUT "question 1" were classified as "dysphagic" and were compared with "non-dysphagic" patients at baseline. After excluding baseline dysphagic subjects, we assessed the predictors of the development of dysphagia in the third year of follow-up. RESULTS The baseline prevalence of dysphagia in PD was 10.4%, growing as high as 19.1% within year 3. Compared to PD subjects not complaining swallowing difficulties, dysphagic patients had significantly higher scores on REM sleep behavior questionnaire, Epworth sleepiness scale (ESS), geriatric depression scale and MDS-UPDRS I (p < .01), significantly lower caudate [123I]FP-CIT uptake parameters and BMI, and mild cognitive changes at symbol digit modalities (p < .01). In the longitudinal analysis of non-dysphagic patients, 14.6% developed dysphagic symptoms at year 3. Excessive daytime sleepiness estimated through ESS was strongly related to the development of swallowing impairment at year 3 in the univariate (odds ratio 3.2, p < .001) and multivariate regression model (odds ratio 2.5, p = .01). CONCLUSIONS Early-stage PD patients often report swallowing difficulties. We found a close relationship between excessive daytime sleepiness and the development of swallowing impairment over three years of follow-up of de novo patients.
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Affiliation(s)
- Massimo Marano
- Neurology, Neurophysiology and Neurobiology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy.
| | - Deepak Gupta
- Binter Center for Parkinson's Disease and Movement Disorders, University of Vermont Medical Center, Burlington, VT, USA
| | - Francesco Motolese
- Neurology, Neurophysiology and Neurobiology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy
| | - Mariagrazia Rossi
- Neurology, Neurophysiology and Neurobiology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy
| | - Vitaliana Luccarelli
- Otolaryngology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy
| | - Claudia Altamura
- Headache and Neurosonology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy
| | - Vincenzo Di Lazzaro
- Neurology, Neurophysiology and Neurobiology unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy
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31
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Broadfoot CK, Abur D, Hoffmeister JD, Stepp CE, Ciucci MR. Research-based Updates in Swallowing and Communication Dysfunction in Parkinson Disease: Implications for Evaluation and Management. PERSPECTIVES OF THE ASHA SPECIAL INTEREST GROUPS 2019; 4:825-841. [PMID: 32104723 PMCID: PMC7043100 DOI: 10.1044/2019_pers-sig3-2019-0001] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
PURPOSE Individuals with Parkinson disease (PD) present with complex and variable symptoms, with recent findings suggesting that the etiology of PD extends beyond the involvement of just the basal ganglia. These symptoms include significant impairments in the speech and swallowing domains, which can greatly affect quality of life and therefore require therapeutic attention. This research-based update reviews the neurophysiological basis for swallowing and speech changes in PD, the effectiveness of various types of treatments, and implications for symptom evaluation and management. CONCLUSION The mechanisms responsible for swallowing and speech symptoms in PD remain largely unknown. Dopaminergic medication and deep-brain-stimulation do not provide consistent benefits for these symptoms suggesting a non-dopaminergic network is involved. Importantly, evidence suggests that symptoms of dysphagia and hypokinetic dysarthria may be early indications of PD, so it is critical to investigate the cause of these changes.
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Affiliation(s)
- C K Broadfoot
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI
| | - D Abur
- Department of Speech, Language, and Hearing Sciences, Boston University, Boston, MA
| | - J D Hoffmeister
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI
| | - C E Stepp
- Department of Speech, Language, and Hearing Sciences, Boston University, Boston, MA
- Department of Biomedical Engineering, Boston University, Boston, MA
- Department of Otolaryngology, Boston University, Boston, MA
| | - M R Ciucci
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI
- Department of Surgery-Division of Otolaryngology Head & Neck Surgery, University of Wisconsin-Madison, Madison, WI
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32
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Kwon M, Lee JH. Oro-Pharyngeal Dysphagia in Parkinson's Disease and Related Movement Disorders. J Mov Disord 2019; 12:152-160. [PMID: 31556260 PMCID: PMC6763715 DOI: 10.14802/jmd.19048] [Citation(s) in RCA: 44] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2019] [Accepted: 08/15/2019] [Indexed: 12/11/2022] Open
Abstract
Oro-pharyngeal dysphagia is a common symptom in patients with Parkinson’s disease (PD) and related disorders, even in their early stage of diseases. Dysphagia in these patients has been underdiagnosed, probably due to poor the self-awareness of the conditions and the underuse of validated tools and objective instruments for assessment. The early detection and intervention of dysphagia are closely related to improving the quality of life and decreasing the mortality rate in these patients. The purpose of this paper is to give an overview of the characteristics of dysphagia, including the epidemiology, pathophysiology, and clinical symptomatology, in patients with PD compared with other parkinsonian disorders and movement disorders. The management of dysphagia and future research directions related to these disorders are also discussed.
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Affiliation(s)
- Miseon Kwon
- Department of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jae-Hong Lee
- Department of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
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33
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34
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Ciucci M, Hoffmeister J, Wheeler-Hegland K. Management of Dysphagia in Acquired and Progressive Neurologic Conditions. Semin Speech Lang 2019; 40:203-212. [PMID: 31158904 DOI: 10.1055/s-0039-1688981] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/26/2022]
Abstract
As the act of deglutition involves much of the central and peripheral nervous systems, neurologic disease can affect swallowing behaviors ranging from mild to profound in severity. The key in working with neurogenic dysphagia is to have a solid foundation in normal swallowing processes, including neural control. Within this framework, then, understanding how the neurologic condition affects neural control will guide hypothesis-based assessment and evidence-based treatment. The purpose of this article is to provide an overview of evaluation and treatment of neurogenic dysphagia in adult populations as well to propose assessment of co-occurring speech, language, and airway compromise. Furthermore, it is vital to be familiar with ethical decision making and end-of-life issues. Continuing education in the form of research articles, conferences, and professional discussion boards is useful in maintaining a high level of service delivery. Whenever possible, an inter- or transdisciplinary approach is recommended.
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Affiliation(s)
- Michelle Ciucci
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, Wisconsin.,Division of Otolaryngology-Head and Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, Wisconsin.,Neuroscience Training Program, University of Wisconsin-Madison, Madison, Wisconsin
| | - Jesse Hoffmeister
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, Wisconsin.,Division of Otolaryngology-Head and Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, Wisconsin
| | - Karen Wheeler-Hegland
- Department of Speech, Language and Hearing Sciences, University of Florida, Gainesville, Florida
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35
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Polychronis S, Niccolini F, Pagano G, Yousaf T, Politis M. Speech difficulties in early de novo patients with Parkinson's disease. Parkinsonism Relat Disord 2019; 64:256-261. [PMID: 31078401 DOI: 10.1016/j.parkreldis.2019.04.026] [Citation(s) in RCA: 21] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/01/2018] [Revised: 09/20/2018] [Accepted: 04/30/2019] [Indexed: 11/25/2022]
Abstract
INTRODUCTION Speech difficulties are a common debilitating feature of Parkinson's disease and we aimed to investigate whether speech difficulties are associated with striatal dopaminergic deficits and faster disease progression. METHODS Using the Parkinson's Progression Markers Initiative database, 143 early de novo Parkinson's disease patients with speech difficulties were identified and matched 1:1 with 143 Parkinson's disease patients without speech difficulties for age, disease duration and motor symptom severity. We investigated differences in clinical features and striatal [123I]FP-CIT single photon emission computed tomography (SPECT) uptake in Parkinson's disease patients with and without speech difficulties. Cox proportional hazards analysis was carried out to investigate whether speech difficulties were predictive of a faster motor progression and cognitive decline. RESULTS Speech difficulties were more common in patients with an akinetic-rigid motor phenotype compared to those with a tremor-dominant phenotype. Parkinson's disease patients with speech difficulties had lower resting tremor (P = 0.027), higher autonomic dysfunction (P = 0.034), increased daytime sleepiness (ESS; P = 0.048), and a higher prevalence of REM sleep behaviour disorder (RBD) symptoms (P = 0.007) compared to those without speech difficulties. Parkinson's disease patients with speech difficulties had significantly lower [123I]FP-CIT uptake in the striatum (P < 0.001), caudate (P = 0.003) and putamen (P = 0.003) compared to those without speech difficulties. The presence of speech difficulties was a predictor of cognitive decline [Hazard Ratio (HR): 0.341, 95% Confidence Interval (CI): 0.153-0.759; Wald: 6.945; P = 0.008), whereas it had no influence on motor progression (HR: 0.885, 95% CI: 0.662-1.183; Wald: 0.680; P > 0.10). CONCLUSION Speech difficulties are associated with greater autonomic dysfunction, sleep disturbances and striatal dopaminergic deficit, and can serve as a predictor of faster cognitive decline in early Parkinson's disease.
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Affiliation(s)
- Sotirios Polychronis
- Neurodegeneration Imaging Group, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
| | - Flavia Niccolini
- Neurodegeneration Imaging Group, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
| | - Gennaro Pagano
- Neurodegeneration Imaging Group, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
| | - Tayyabah Yousaf
- Neurodegeneration Imaging Group, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
| | - Marios Politis
- Neurodegeneration Imaging Group, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
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Cullen KP, Grant LM, Kelm-Nelson CA, Brauer AFL, Bickelhaupt LB, Russell JA, Ciucci MR. Pink1 -/- Rats Show Early-Onset Swallowing Deficits and Correlative Brainstem Pathology. Dysphagia 2018; 33:749-758. [PMID: 29713896 PMCID: PMC6207473 DOI: 10.1007/s00455-018-9896-5] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2018] [Accepted: 04/16/2018] [Indexed: 02/06/2023]
Abstract
Parkinson disease (PD) compromises oropharyngeal swallowing, which negatively affects quality of life and contributes to aspiration pneumonia. Dysphagia often begins early in the disease process, and does not improve with standard therapies. As a result, swallowing deficits are undertreated in the PD population. The Pink1 -/- rat is used to model PD, and demonstrates widespread brainstem neuropathology in combination with early-onset sensorimotor dysfunction; however, to date, swallowing behaviors have not been evaluated. To test the hypothesis that Pink1 -/- rats demonstrate early-onset differences in swallowing, we analyzed within-subject oropharyngeal swallowing using videofluoroscopy. Pink1 -/- and wildtype (WT) controls at 4 (Pink1 -/- n = 16, WT = 16) and 8 (Pink1 -/- n = 12, WT = 12) months of age were tested. The average and maximum bolus size was significantly increased in Pink1 -/- rats at both 4 and 8 months. Bolus average velocity was increased at 8 months for all animals; yet, Pink1 -/- animals had significantly increased velocities compared to WT at 8 months. The data show a significant reduction in mastication rate for Pink1 -/- rats at 8 months suggesting the onset of oromotor dysfunction begins at this time point. Relationships among swallowing variables and neuropathological findings, such as increased alpha-synuclein protein in the nucleus ambiguus and reductions in noradrenergic cells in the locus coeruleus in the Pink1 -/- rats, were determined. The presence of early oropharyngeal swallowing deficits and relationships to brainstem pathology in Pink1-/- rat models of PD indicate that this may be a useful model of early swallowing deficits and their mechanisms. These findings suggest clinical implications for early detection and management of dysphagia in PD.
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Affiliation(s)
- Kaylee P Cullen
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, 53706, USA
- Division of Otolaryngology, Department of Surgery, University of Wisconsin-Madison, 1300 University Avenue, 483 Medical Sciences Center, Madison, WI, 53706, USA
| | - Laura M Grant
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, 53706, USA
- Division of Otolaryngology, Department of Surgery, University of Wisconsin-Madison, 1300 University Avenue, 483 Medical Sciences Center, Madison, WI, 53706, USA
| | - Cynthia A Kelm-Nelson
- Division of Otolaryngology, Department of Surgery, University of Wisconsin-Madison, 1300 University Avenue, 483 Medical Sciences Center, Madison, WI, 53706, USA.
| | - Alexander F L Brauer
- Division of Otolaryngology, Department of Surgery, University of Wisconsin-Madison, 1300 University Avenue, 483 Medical Sciences Center, Madison, WI, 53706, USA
| | - Luke B Bickelhaupt
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, 53706, USA
| | - John A Russell
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, 53706, USA
| | - Michelle R Ciucci
- Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, 53706, USA
- Division of Otolaryngology, Department of Surgery, University of Wisconsin-Madison, 1300 University Avenue, 483 Medical Sciences Center, Madison, WI, 53706, USA
- Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, 53706, USA
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Abstract
PURPOSE OF REVIEW Patients with Parkinson's disease (PD) often display gastrointestinal and genitourinary autonomic symptoms years or even decades prior to diagnosis. These symptoms are thought to be caused in part by pathological α-synuclein inclusions in the peripheral autonomic and enteric nervous systems. It has been proposed that the initial α-synuclein aggregation may in some PD patients originate in peripheral nerve terminals and then spread centripetally to the spinal cord and brainstem. In vivo imaging methods can directly quantify the degeneration of the autonomic nervous system as well as the functional consequences such as perturbed motility. Here, we review the methodological principles of these imaging techniques and the major findings in patients with PD and atypical parkinsonism. RECENT FINDINGS Loss of sympathetic and parasympathetic nerve terminals in PD can be visualized using radiotracer imaging, including 123I-MIBG scintigraphy, and 18F-dopamine and 11C-donepezil PET. Recently, ultrasonographical studies disclosed reduced diameter of the vagal nerves in PD patients. Radiological and radioisotope techniques have demonstrated dysmotility and prolonged transit time throughout all subdivisions of the gastrointestinal tract in PD. The prevalence of objective dysfunction as measured with these imaging methods is often considerably higher compared to the prevalence of subjective symptoms experienced by the patients. Degeneration of the autonomic nervous system may play a key role in the pathogenesis of PD. In vivo imaging techniques provide powerful and noninvasive tools to quantify the degree and extent of this degeneration and its functional consequences.
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Affiliation(s)
- Karoline Knudsen
- Department of Nuclear Medicine and PET Centre Aarhus University Hospital, Institute of Clinical Medicine Aarhus University, Norrebrogade 44, Building 10, 8000, Aarhus C, Denmark
| | - Per Borghammer
- Department of Nuclear Medicine and PET Centre Aarhus University Hospital, Institute of Clinical Medicine Aarhus University, Norrebrogade 44, Building 10, 8000, Aarhus C, Denmark.
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Tomita S, Oeda T, Umemura A, Kohsaka M, Park K, Yamamoto K, Sugiyama H, Sawada H. Video-fluoroscopic swallowing study scale for predicting aspiration pneumonia in Parkinson's disease. PLoS One 2018; 13:e0197608. [PMID: 29874285 PMCID: PMC5991364 DOI: 10.1371/journal.pone.0197608] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2017] [Accepted: 05/04/2018] [Indexed: 11/30/2022] Open
Abstract
Introduction A number of video-fluoroscopic swallowing study (VFSS) abnormalities have been reported in patients with Parkinson’s disease (PD). However, the most crucial finding of subsequent aspiration pneumonia has not been validated fully. We conducted a retrospective and case-control study to determine the clinically significant VFSS findings in this population, and to propose a practical scale for predicting aspiration pneumonia in patients with PD. Methods We enrolled 184 PD patients who underwent VFSS because of suspected dysphagia. The patients who developed aspiration pneumonia within six months of the VFSS were assigned as cases and the patients without aspiration pneumonia at six months were designated as controls. Logistic regression analysis was performed to determine the prognostic VFSS features based on the data of swallowing 3 mL of jelly, which were used to make a PD VFSS scale (PDVFS). The validity of the new PDVFS was evaluated by ROC analysis. Additionally, we used the survival time analysis to compare time to death between groups, stratified by the PDVFS score. Results Twenty-five patients developed aspiration pneumonia. Among the previously-proposed VFSS features, mastication, lingual motility prior to transfer, aspiration, and total swallow time were identified as significant prognostic factors. We combined these factors to form the PDVFS. The PDVFS score ranges from 0 to 12, with 12 being the worst. ROC analysis revealed 92% sensitivity and 82% specificity at a cutoff point of 3. The higher PDVFS group showed shorter time-to-death than the lower PDVFS group (log rank P = 0.001). Conclusion Our newly developed VFSS severity scale (based on jelly swallowing) for patients with PD was easy to rate and could predict subsequent aspiration pneumonia and poor prognosis in patients with PD.
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Affiliation(s)
- Satoshi Tomita
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Tomoko Oeda
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Atsushi Umemura
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Masayuki Kohsaka
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Kwiyoung Park
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Kenji Yamamoto
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Hiroshi Sugiyama
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
| | - Hideyuki Sawada
- Clinical Research Center and Department of Neurology, Utano National Hospital, Kyoto, Japan
- * E-mail:
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Vecchia DD, Kanazawa LKS, Wendler E, de Almeida Soares Hocayen P, Bruginski E, Campos FR, Stern CAJ, Vital MABF, Miyoshi E, Wöhr M, Schwarting RK, Andreatini R. Effects of ketamine on vocal impairment, gait changes, and anhedonia induced by bilateral 6-OHDA infusion into the substantia nigra pars compacta in rats: Therapeutic implications for Parkinson’s disease. Behav Brain Res 2018; 342:1-10. [DOI: 10.1016/j.bbr.2017.12.041] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/04/2017] [Accepted: 12/31/2017] [Indexed: 12/22/2022]
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Kelm-Nelson CA, Trevino MA, Ciucci MR. Quantitative Analysis of Catecholamines in the Pink1 -/- Rat Model of Early-onset Parkinson's Disease. Neuroscience 2018; 379:126-141. [PMID: 29496635 DOI: 10.1016/j.neuroscience.2018.02.027] [Citation(s) in RCA: 31] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2017] [Revised: 02/14/2018] [Accepted: 02/17/2018] [Indexed: 10/17/2022]
Abstract
Parkinson's disease (PD) related to homozygous mutations in the Pink1 gene is associated with nigrostriatal dopamine depletion and a wide range of sensorimotor deficits. In humans and animal models of PD, not all sensorimotor deficits are levodopa-responsive. We hypothesized that the underlying mechanisms of locomotion, limb control, and vocal communication behavior include other pathologies. Here, Pink1 -/- rats were treated with an oral dose of levodopa and limb motor and vocal communication behaviors were measured. Levodopa significantly improved some aspects of locomotion but did not improve ultrasonic vocalization intensity or frequency. Catecholamine concentrations in the striatum (SR), substantia nigra (SN), and locus coeruleus (LC) were analyzed to test the hypothesis that behavioral deficits would correlate to altered protein levels. There were no differences in dopamine concentrations in the SR and SN of Pink1 -/- animals compared to wild-type controls. There was a significant increase in norepinephrine concentration in the SN of Pink1 -/- animals. Moreover, an observed decrease in norepinephrine concentrations in the LC is consistent with the hypothesis that early-stage PD includes noradrenergic loss in the brainstem, and is congruent with a significant increase in catechol-O-methyltransferase expression in the LC of Pink1 -/- animals. Pearson's correlations showed that increases in time to traverse a tapered balance beam are significantly associated with reductions in striatal dopamine. Ultrasonic vocalization complexity was positively correlated with LC norepinephrine concentrations. These data support the evolving hypothesis that differences in neural substrates and early-onset noradrenergic mechanisms in the brainstem may contribute to pathogenesis in the Pink1 -/- rat.
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Affiliation(s)
- Cynthia A Kelm-Nelson
- Department of Surgery, Division of Otolaryngology, University of Wisconsin-Madison, Madison, WI, USA.
| | - Michael A Trevino
- Department of Psychology, University of Illinois-Urbana Champaign, Urbana-Champaign, IL, USA.
| | - Michelle R Ciucci
- Department of Surgery, Division of Otolaryngology, University of Wisconsin-Madison, Madison, WI, USA; Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA; Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, USA.
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41
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Wollmer E, Klein S. A review of patient-specific gastrointestinal parameters as a platform for developing in vitro models for predicting the in vivo performance of oral dosage forms in patients with Parkinson’s disease. Int J Pharm 2017; 533:298-314. [DOI: 10.1016/j.ijpharm.2017.08.126] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/26/2017] [Revised: 08/25/2017] [Accepted: 08/31/2017] [Indexed: 02/06/2023]
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Triadafilopoulos G, Gandhy R, Barlow C. Pilot cohort study of endoscopic botulinum neurotoxin injection in Parkinson's disease. Parkinsonism Relat Disord 2017; 44:33-37. [PMID: 28847681 DOI: 10.1016/j.parkreldis.2017.08.020] [Citation(s) in RCA: 18] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/01/2017] [Revised: 08/12/2017] [Accepted: 08/20/2017] [Indexed: 02/08/2023]
Abstract
BACKGROUND Gastrointestinal symptoms, such as dysphagia, postprandial bloating, and defecatory straining are common in Parkinson's Disease (PD) and they impact quality of life. Endoscopic botulinum neurotoxin (BoNT) injection has been used in the treatment of dysphagia, gastroparesis and chronic anismus. AIMS To examine the feasibility, safety and efficacy of endoscopically delivered BoNT injection to distal esophagus, pylorus or anal canal aiming at relieving regional gastrointestinal symptoms in patients with PD. METHODS This is a retrospective open cohort pilot study to assess the clinical response to endoscopic BoNT injection on selected PD patients with symptoms and identifiable abnormalities on high-resolution manometry and wireless motility capsule, to generate early uncontrolled data on feasibility, tolerability, safety and efficacy. Baseline symptoms and response to therapy were assessed by questionnaires. RESULTS Fourteen PD patients (10 M:4 F), mean age 73 (range: 62-93) were treated. Three patients had esophageal Botox for ineffective esophageal motility (IEM) (n = 1), esophago-gastric junction outlet obstruction (EGJOO) & IEM (n = 1), and diffuse esophageal spasm (DES) (n = 1). Nine patients were treated with pyloric BoNT injection for gastroparesis with mean gastric transit time of 21.2 h; range 5.2-44.2 h. Two patients received anal Botox for defecatory dyssynergia ((Type I) (n = 1) and overlap (slow-transit and dyssynergic) constipation (n = 1). Endoscopic BoNT injection (100-200 units) was well tolerated and there were no significant adverse events. CONCLUSIONS Endoscopic BoNT injection to esophagus, pylorus or anal canal is safe, well-tolerated and leads to symptomatic improvement that lasts up to several months. The procedure can be repeated as needed and combined with other therapies.
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Affiliation(s)
- George Triadafilopoulos
- Stanford Multidimensional Program for Innovation and Research in the Esophagus (S-MPIRE), Division of Gastroenterology and Hepatology, Stanford University School of Medicine, Stanford, CA, 94305, USA.
| | - Rita Gandhy
- The Parkinson's Institute and Clinical Center, Sunnyvale, CA, USA
| | - Carrolee Barlow
- The Parkinson's Institute and Clinical Center, Sunnyvale, CA, USA
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Pflug C, Bihler M, Emich K, Niessen A, Nienstedt JC, Flügel T, Koseki JC, Plaetke R, Hidding U, Gerloff C, Buhmann C. Critical Dysphagia is Common in Parkinson Disease and Occurs Even in Early Stages: A Prospective Cohort Study. Dysphagia 2017; 33:41-50. [PMID: 28828545 DOI: 10.1007/s00455-017-9831-1] [Citation(s) in RCA: 93] [Impact Index Per Article: 11.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2017] [Accepted: 07/29/2017] [Indexed: 01/20/2023]
Abstract
To assess the prevalence of dysphagia and its typical findings in unselected "real-world" Parkinson patients using an objective gold-standard method. This was a prospective, controlled, cross-sectional study conducted in 119 consecutive Parkinson patients of all stages independent of subjective dysphagia. Patients and 32 controls were clinically and endoscopically examined by flexible endoscopic evaluation of swallowing (FEES) to evaluate the deglutition with regard to three consistencies (water, biscuit, and bread). Typical findings of dysphagia like penetration and aspiration, residues, and leakage were assessed. Dysphagia was common in Parkinson patients and occurred in all, even early, disease stages. Only 5% (6/119) of patients showed a completely unremarkable deglutition. Aspiration was seen in 25% (30/119) of patients and always related to water. Residues occurred in 93% (111/119), most commonly for bread. Leakage was much less frequent and was found in only 3-18%, depending on consistency. In a significant fraction of patients, objective dysphagia was not subjectively perceived. A total of 16% of asymptomatic patients suffered from critical aspiration. Significant swallowing deficiencies already occurred in early disease. Aspiration was found in 4 of 20 (20%) patients with disease duration of less than 2 years. Seven of 57 patients (12%) with Hoehn and Yahr stage 2 suffered from severe aspiration. Given the high frequency of critical aspiration in Parkinson disease, these patients should be evaluated early for dysphagia to avoid complications and recommend an adequate therapy. FEES is a simple, cost efficient, minimally invasive method that is ideally suited for this purpose.
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Affiliation(s)
- Christina Pflug
- Department of Voice, Speech and Hearing Disorders, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany.
| | - Moritz Bihler
- Department of Neurology, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Katharina Emich
- Department of Neurology, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Almut Niessen
- Department of Voice, Speech and Hearing Disorders, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany
| | - Julie Cläre Nienstedt
- Department of Voice, Speech and Hearing Disorders, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany
| | - Till Flügel
- Department of Voice, Speech and Hearing Disorders, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany
| | - Jana-Christiane Koseki
- Department of Voice, Speech and Hearing Disorders, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany
| | - Rosemarie Plaetke
- Institute of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Ute Hidding
- Department of Neurology, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Christian Gerloff
- Department of Neurology, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Carsten Buhmann
- Department of Neurology, Center for Clinical Neurosciences, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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Jellinger KA. Neuropathology of Nonmotor Symptoms of Parkinson's Disease. INTERNATIONAL REVIEW OF NEUROBIOLOGY 2017; 133:13-62. [PMID: 28802920 DOI: 10.1016/bs.irn.2017.05.005] [Citation(s) in RCA: 34] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/18/2022]
Abstract
Parkinson's disease (PD), a multiorgan neurodegenerative disorder associated with α-synuclein deposits throughout the nervous system and many organs, is clinically characterized by motor and nonmotor features, many of the latter antedating motor dysfunctions by 20 or more years. The causes of the nonmotor manifestations such as olfactory, autonomic, sensory, neuropsychiatric, visuospatial, sleep, and other disorders are unlikely to be related to single lesions. They are mediated by the involvement of both dopaminergic and nondopaminergic systems, and diverse structures outside the nigrostriatal system that is mainly responsible for the motor features of PD. The nonmotor alterations appear in early/prodromal stages of the disease and its further progression, suggesting a topographical and chronological spread of the lesions. This lends further support for the notion that PD is a multiorgan proteinopathy, although the exact relationship between presymptomatic and later developing nonmotor features of PD and neuropathology awaits further elucidation.
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45
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Abstract
Changes to swallowing affect most people with Parkinson's disease (PD). Changes may not initially exercise a decisive impact, but can later pose significant threats to nutritional, hydration and respiratory health and psychosocial quality of life. This review, from a largely clinical viewpoint, outlines the nature of changes in PD and considers the issue of how many people are affected and in what ways. It outlines main approaches to assessment and management, with an emphasis on aspects relevant to PD. Dysphagia contributes to drooling in PD. The review therefore also touches on the nature and management of this condition that has its own set of health and psychosocial quality-of-life issues.
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Affiliation(s)
- Nick Miller
- Newcastle University Institute for Ageing, Speech & Language Sciences, George VI Building, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
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46
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Umemoto G, Tsuboi Y, Furuya H, Mishima T, Fujioka S, Fujii N, Arahata H, Sugahara M, Sakai M. Dysphagia in Perry Syndrome: Pharyngeal Pressure in Two Cases. Case Rep Neurol 2017; 9:161-167. [PMID: 28690533 PMCID: PMC5498940 DOI: 10.1159/000457900] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2017] [Accepted: 01/21/2017] [Indexed: 11/25/2022] Open
Abstract
Background To investigate the impact of dysphagia in Perry syndrome (PS), an autosomal dominant parkinsonism caused by mutation of DCTN1, which is associated with hypoventilation, depression, and weight loss. Case Presentation We used tongue pressure measurements and manofluorography to investigate swallowing function in 2 patients with PS. Case 1, a 60-year-old male showing parkinsonism, and case 2, a 49-year-old male admitted with pneumonia, were diagnosed as having PS based on the DCTN1 gene analysis. Case 1 showed a pharyngeal retention of the bolus on videofluorography (VF) and a few swallows were required for its passage into the esophagus. However, tongue pressure and manometry were within the normal range. This patient could eat a normal diet under supervision. Case 2 required artificial ventilation and tube feeding on admission. The VF image showed a slow transfer of the bolus, delayed swallow reflex, and pharyngeal retention of the bolus that required several swallows for its passage into the esophagus. The tongue pressure was within the normal range, but manometry showed a significant decrease in pressure at the hypopharynx and upper esophageal sphincter. The oral intake of the patients was limited to 2 cups of jelly per day. Conclusions The investigation of swallowing dysfunction of 2 cases of PS showed that maintaining pharyngeal pressure within the normal range was very important for oral feeding success and prognosis.
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Affiliation(s)
- George Umemoto
- Department of Oral and Maxillofacial Surgery, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
| | - Yoshio Tsuboi
- Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
| | - Hirokazu Furuya
- Department of Neurology, Kochi Medical School, Kochi University, Kochi, Japan
| | - Takayasu Mishima
- Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
| | - Shinsuke Fujioka
- Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan
| | - Naoki Fujii
- Department of Neurology, National Hospital Organization Omuta National Hospital, Fukuoka, Japan
| | - Hajime Arahata
- Department of Neurology, National Hospital Organization Omuta National Hospital, Fukuoka, Japan
| | - Miwa Sugahara
- Department of Neurology, National Hospital Organization Omuta National Hospital, Fukuoka, Japan
| | - Mitsuaki Sakai
- Department of Rehabilitation, National Hospital Organization Omuta National Hospital, Fukuoka, Japan
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47
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A practical review of gastrointestinal manifestations in Parkinson's disease. Parkinsonism Relat Disord 2017; 39:17-26. [DOI: 10.1016/j.parkreldis.2017.02.029] [Citation(s) in RCA: 35] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/12/2016] [Revised: 02/06/2017] [Accepted: 02/21/2017] [Indexed: 02/06/2023]
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Stegemöller EL, Hibbing P, Radig H, Wingate J. Therapeutic singing as an early intervention for swallowing in persons with Parkinson's disease. Complement Ther Med 2017; 31:127-133. [PMID: 28434465 DOI: 10.1016/j.ctim.2017.03.002] [Citation(s) in RCA: 33] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/03/2016] [Revised: 03/01/2017] [Accepted: 03/02/2017] [Indexed: 11/20/2022] Open
Abstract
OBJECTIVE For persons with Parkinson's disease (PD), secondary motor symptoms such as swallow impairment impact the quality of life and are major contributors to mortality. There is a present need for therapeutic interventions aimed at improving swallow function during the early stages of PD. The purpose of this pilot study was to examine the effects of a group therapeutic singing intervention on swallowing in persons with PD with no significant dysphagia symptoms. DESIGN Cohort study. SETTING University in the United States. PARTICIPANTS Twenty-four participants with PD. INTERVENTION Eight weeks of group therapeutic singing. MAIN OUTCOME MEASURES Electromyography (EMG) was used to assess muscle activity associated with swallow pre and post the group singing intervention. Swallow quality of life (SWAL-QOL) and the Unified Parkinson's Disease Rating Scale (UPDRS) were also obtained pre- and post-intervention. RESULTS Participants reported minimal difficulty with swallowing, yet results revealed a significant increase in EMG outcome measures, as well as significant improvement in UPDRS total and UPDRS motor scores. No significant differences were revealed for SWAL-QOL. CONCLUSION Increases in EMG timing measures may suggest that group singing results in the prolongation of laryngeal elevation, protecting the airway from foreign material for longer periods of time during swallow. Combined with the improvement in UPDRS clinical measures, therapeutic singing may be an engaging early intervention strategy to address oropharyngeal dysphagia while also benefiting additional clinical symptoms of PD.
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Affiliation(s)
- E L Stegemöller
- Department of Kinesiology, Iowa State University, Ames, IA, United States.
| | - P Hibbing
- Department of Kinesiology, Iowa State University, Ames, IA, United States
| | - H Radig
- Department of Kinesiology, Iowa State University, Ames, IA, United States
| | - J Wingate
- Department of Communication Sciences and Disorders, Jacksonville University, Jacksonville, FL, United States
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49
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Jones CA, Ciucci MR. Multimodal Swallowing Evaluation with High-Resolution Manometry Reveals Subtle Swallowing Changes in Early and Mid-Stage Parkinson Disease. JOURNAL OF PARKINSONS DISEASE 2017; 6:197-208. [PMID: 26891176 DOI: 10.3233/jpd-150687] [Citation(s) in RCA: 50] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
Abstract
BACKGROUND Parkinson disease (PD) has detrimental effects on swallowing function. Treatment options are largely behavioral; thus, patients would benefit from an earlier start to therapy. Early swallowing changes in PD are not well-known, so patients do not typically receive swallowing treatment until later in the progression of PD. OBJECTIVE We used predictive modeling to determine what quantitative swallowing variables best differentiate individuals with early to mid-stage PD from healthy controls. METHODS Participants included twenty-six individuals with early to mid-stage PD and 26 healthy, age- and sex-matched controls. Swallowing was evaluated by simultaneous high-resolution manometry and videofluoroscopy as well as the Sydney Swallow Questionnaire (SSQ). Binomial logistic regression was performed on 4 sets of data: 1) high-resolution manometry only; 2) videofluoroscopy only; 3) SSQ only; and 4) all data combined. RESULTS A model from a combined data set had the highest accuracy in differentiating individuals with PD from controls. The model included maximum pressure in the velopharynx (soft palate), pressure variability in the velopharynx, and the SSQ item concerning difficulty with swallowing saliva. No significant models could be generated using the videofluoroscopy data. CONCLUSIONS Individuals with PD show quantitative changes in pressure generation and are able to self-assess aspects of swallowing function in the early and mid-stages of PD, even in the absence of swallowing changes seen on videofluoroscopy. A multimodal approach for the assessment of swallowing may be more accurate for determining subtle swallowing changes that occur in the early stages of PD.
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Affiliation(s)
- Corinne A Jones
- Department of Surgery, Division of Otolaryngology, University of Wisconsin-Madison, Madison, WI, USA.,Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, USA.,Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
| | - Michelle R Ciucci
- Department of Surgery, Division of Otolaryngology, University of Wisconsin-Madison, Madison, WI, USA.,Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, USA.,Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
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Dysphagia in Parkinson’s Disease. Dysphagia 2017. [DOI: 10.1007/174_2017_118] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/18/2022]
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