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1 These authors contributed equally to the manuscript.
Nicole Pizzorni
Correspondence
Corresponding author at: Phoniatric Unit, Department of Biomedical and Clinical Sciences “Luigi Sacco”, University of Milano, Via GB Grassi 74, 20157 Milan, Italy.
Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health, University of Genoa-IRCCS Ospedale Policlinico San Martino, Genova, Italy
Gastrointestinal Physiology Laboratory, Hospital de Mataró, Universitat Autónoma de Barcelona, Mataró, SpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (Ciberehd), Instituto de Salud Carlos III, Barcelona, Spain
Department of Public Health, Experimental and Forensic Medicine, Unit of Human and Clinical Nutrition, University of Pavia, Pavia, ItalyIRCCS Mondino Foundation, Pavia, Italy
Parkinson disease and Movement Disorders Unit, Neurology Service, Hospital Clínic de Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII) Barcelona, Spain
PD treatments should be optimized to minimize the impact on swallowing function
•
Treatment of dysphagia should be guided by an instrumental assessment of swallowing
•
There is insufficient evidence to support the use of neuromodulation techniques
•
Botulinum toxin is an option for isolated upper esophageal sphincter impairment
•
PEG feeding must be considered on an individual basis, but not in case of dementia
Abstract
Background
Dysphagia is common in Parkinson's disease (PD). The effects of antiparkinsonian drugs on dysphagia are controversial. Several treatments for dysphagia are available but there is no consensus on their efficacy in PD.
Objective
To conduct a systematic review of the literature and to define consensus statements on the treatment of dysphagia in PD and related nutritional management.
Methods
A multinational group of experts in the field of neurogenic dysphagia and/or Parkinson's disease conducted a systematic evaluation of the literature and reported the results according to PRISMA guidelines. The evidence from the retrieved studies was analyzed and discussed in a consensus conference organized in Pavia, Italy, and the consensus statements were drafted. The final version of statements was subsequently achieved by e-mail consensus.
Results
The literature review retrieved 64 papers on treatment and nutrition of patients with PD and dysphagia, mainly of Class IV quality. Based on the literature and expert opinion in cases where the evidence was limited or lacking, 26 statements were developed.
Conclusions
The statements developed by the Consensus panel provide a guidance for a multi-disciplinary treatment of dysphagia in patients with PD, involving neurologists, otorhinolaryngologists, gastroenterologists, phoniatricians, speech-language pathologists, dieticians, and clinical nutritionists.
Parkinson's disease (PD) is the second most common neurodegenerative disorder with an estimated prevalence of 6.1 million individuals all over the world [
]. Dysphagia is common in PD, with a prevalence varying between 11% and 87% depending on the disease stage, the disease duration, and the assessing method [
]. Conversely, the impact, either positive or detrimental, of PD treatments for swallowing impairments is still debated.
Several treatments options for dysphagia are currently available specifically targeting swallowing function. The main goals are to reduce morbidity and mortality associated with pulmonary infections and malnutrition and to maintain a satisfactory quality-of-life (QOL) [
]. Swallowing therapy, generally delivered by speech-language pathologists, aims to improve the safety and efficiency of swallowing by means of compensatory and rehabilitative strategies [
]. Alternative feeding methods are used in patients with severe dysphagia.
Unfortunately, limited and variable information exists as regards the efficacy, the timing, and the best approach for treatments of dysphagia in PD. Despite this, there is consensus on the importance of dysphagia care and referral to a dysphagia specialist as part of the routine clinical workup from the earliest stages of the disease [
Consensus-based processes are recognized through formal methodology to provide a guidance to clinicians in complex health issues in the absence of high-quality evidence. The methodology relies on definition of statements by the consensus of a panel of experts based on the best available evidence and the group's expertise [
]. These guidelines provide evidence-based and detailed recommendations for swallowing therapy in patients with PD, but they reflected the specific context of the Netherlands and the literature search only covered publications until 2008. For this reason, we organized a Multinational Consensus Conference among experts aiming to provide clinical recommendations for physicians and allied health professionals to improve the management of patients with PD and dysphagia and support clinicians in clinical decision making. This manuscript reports the Consensus statements on treatments (PD treatments and dysphagia-specific treatments) and the role of nutritional management in patients with PD and dysphagia.
2. Materials and methods
The project was initiated by the Organizing Committee during the 2018 edition of the ‘Dysphagia Update’ Meeting, an international scientific event focused on neurogenic dysphagia that has been held biannually since 2008 under the patronage of the Italian Society of Neurology, the Italian Society of Neurorehabilitation, and the European Society for Swallowing Disorders. The Multinational Consensus Conference method was designed according to the US National Institutes of Health Consensus Development Program (http://consensus.nih.gov) [
The project covered a period of 36 months following five steps: (1) assignment phase, (2) scoping phase, (3) assessment phase, (4) face-to-face Consensus Conference, held on 27-28th September 2019, at the IRCCS Mondino Foundation, Pavia, Italy, and (5) update of the evidence (up to February 2021) and refinement of statements by e-mail.
The core of the consensus panel was formed by Italian neurologists who met regularly at the ‘Dysphagia Update’ meetings. Additional specialists, also from different medical disciplines and from other Countries were invited in order to achieve a broad geographic and multidisciplinary representation. Participants were selected based on their recognized involvement in the care of large cohorts of PD patients and/or their involvement in research projects on PD and/or neurogenic dysphagia, and/or because of their publication record on neurogenic dysphagia in peer-reviewed journals. Participants were invited by e-mail. A single reminder was sent to those who did not reply to the first invitation. The final group was made up of 21 neurologists, 4 otorhinolaryngologists (ear, nose and throat specialists - ENT), 3 phoniatricians, 2 gastroenterologists, 4 speech-language pathologists, 2 clinical nutritionists, 1 radiologist and a statistician.
In the assignment phase, four working groups were identified:
1.
the Scientific Committee, comprising 7 members, planned and organized the whole project, selected the members of the other groups, and developed the questions following the Classification of Evidence Schemes of the Clinical Practice Guideline Process Manual of the American Academy of Neurology (AAN) [
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
]. Clinically relevant questions were proposed by the Scientific Committee and discussed during several meeting according to the PICO format (Appendix 1);
2.
the Technical Committee, comprising 6 members, systematically reviewed the evidence, organized the results into tables, and assisted the other working groups in all steps;
3.
a Workgroup, comprising 9 members, provided the first draft of answers to the proposed questions prior to the Consensus Conference, based on personal expertise and the literature retrieved from the systematic review. The expert Workgroups, assisted by the Technical Committee and the Scientific Committee, summarized and critically integrated information from multiple sources, and presented findings of this activity during the Consensus Conference also pointing out research gaps and proposing topics for future research;
4.
the Consensus Development Panel, comprising 6 members, was responsible for defining the presentation procedures and for the assessment of the final statements.
In the scoping phase, the procedure for the literature review and the protocol for the conference were defined. The Scientific Committee identified the topics and together with the Technical Committee formulated the questions to be addressed.
In the assessment phase, the Technical Committees carried out a systematic review to analyze the state-of-the-art on dysphagia in PD. The systematic review was reported according to PRISMA guidelines [
]. Studies eligible for inclusion were those dealing with screening, diagnosis, prognosis, treatment, and nutrition published since 1990, any kind of design and reporting original data on PD patients with dysphagia. Exclusion criteria were studies published in abstract form, case-reports, reviews, editorials, letters, studies on animals, studies including patients with dysphagia of mixed etiology. Results of the literature search on treatment and nutrition are presented in this manuscript, whereas those related to screening, diagnosis, and prognosis are reported in another paper [
Cosentino G, Avenal M, Schindler A et al. A multinational consensus on dysphagia in Parkinson's disease - screening, diagnosis and prognostic value. J. Neurol. (In press).
]. Studies were identified from the National Library of Medicine's MEDLINE database, by means of specific search strategies, using a combination of exploded MeSH terms and free text (search strategy is reported in Appendix 2). Reference lists of identified articles were reviewed to find additional references. Records and full papers without electronic abstracts were reviewed independently by two reviewers to identify relevant studies. Disagreements were resolved by discussion between the two reviewers until consensus was reached. Studies were classified according to various descriptors, including topic, sample size, design, and level of evidence according to the AAN Classification of Evidence [
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
]. Each study was graded according to its risk of bias from Class I (highest quality) to Class IV (lowest quality). Risk of bias was judged by assessing specific quality elements (i.e., study design, patient spectrum, data collection, masking). The classification was performed by two reviewers, with disagreement resolved by discussion.
In consideration of the multidisciplinary expert groups and the generally low-level quality of evidence emerged from the systematic analysis of the literature, we adopted a modified Delphi method [
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
] to achieve consensus and develop the final statements. The method consisted in four subsequent rounds. The first one was performed electronically: a first set of statements were generated and sent by e-mail to the experts of the Workgroups. Answers were collected and analyzed to inform necessary changes. The second and the third rounds were carried out face-to-face, during the first and the second day of the Multinational Consensus Conference, respectively, with the participation of the entire panel. The fourth round was performed electronically: the final version of the statements, adapted, when required, according to the additional analysis of paper published since the consensus conference, was circulated by e-mail to the experts. On every round, a minimum of 80% agreement for each statement was required for inclusion in the final consensus statement (25/31).
Ultimately, the systematic literature analysis covered the period from January 1990 to February 2021.
3. Results
3.1 Questions of the consensus conference
The Scientific Committee formulated and submitted two questions on dysphagia treatments and two question on the nutritional management of patients with PD and dysphagia.
Questions on treatment:
a)
What clinical and/or instrumental abnormalities require appropriate treatment?
b)
What are the treatment options for dysphagia in PD (optimization of PD treatments, swallowing therapy, neuromodulation, medical treatments)?
Questions on nutrition.
a)
What are the nutritional interventions for patients with PD and dysphagia?
b)
When should percutaneous endoscopic gastrostomy be indicated for the nutrition of patients with PD and dysphagia?
3.2 Systematic review
The electronic search retrieved 747 citations and 8 additional papers were identified by manual search from the references of included reports (Fig. 1). A total of 174 papers met the inclusion criteria. Sixty-four papers dealt with dysphagia or nutrition in PD, but only 45 contained useful findings for elaborating the statements. The majority of studies were of Class IV. Most studies included <20 patients and had a pre-post design.
Table 1 summarizes the main characteristics of the studies retrieved during literature search (see Supplementary material for complete list of references); Table 2 depicts main information on the studies used as basis for the statements. Where there was no study was available to answer to the question, statements were entirely based on expert opinion and general literature on dysphagia and nutrition.
Table 1Descriptive features of eligible studies on the treatment and nutritional management of patients with PD and dysphagia.
Studies were classified according to various descriptors, including topic domain, sample size, design, presence of diagnostic criteria of the syndrome and level of evidence according to the Classification of Evidence Schemes of the Clinical Practice Guideline Process Manual of the American Academy of Neurology [
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
Table 2Studies used as basis for the development of statements.
First author, y
Design
Treatment
N. patients
Level of evidence
Fuh, 1997
Pre-post study
Levodopa
19
IV
Hunter, 1997
Pre-post study
Levodopa
15
IV
Lim, 2008
Pre-post study
Levodopa
10
III
Michou, 2014
Pre-post study
Levodopa
26
III
Warnecke, 2016
Pre-post study
Levodopa
15
IV
Labeit, 2020
Pre-post study
Levodopa-carbidopa intestinal gel
11
IV
Ciucci, 2008
Pre-post study
DBS in STN
14
IV
Robertson, 2011
RCT
DBS in STN e GPi and Levodopa
27
II
Lengerer, 2012
Pre-post study
DBS in STN
18
IV
Sibergleit, 2012
Pre-post study
Bilateral DBS
14
IV
Wolz, 2012
Pre-post study
DBS in STN
34
IV
Troche, 2014
Pre-post study
Unilateral DBS in STN or Gpi
33
IV
Krygowska-Wajs, 2016
Pre-post study
Bilateral DBS in STN
20
IV
Sundstedt, 2017
Pre-post study
Bilateral DBS in cZI
9
IV
Olchik, 2018
Pre-post study
DBS (nfs)
10
IV
Xie, 2018
RCT (cross-over)
DBS in STN
11
II
Kawaguchi, 2020
Pre-post study
Bilateral DBS in STN
26
IV
Pflug, 2020
RCT (cross-over)
Bilateral DBS in STN vs combined STN + Substantia nigra-DBS
15
II
Luchesi, 2013
Pre-post study
Conventional swallowing therapy
24
IV
Manor, 2013
RCT
Conventional swallowing therapy vs video-assisted swallowing therapy
42
II
Luchesi, 2015*
Pre-post study
Conventional swallowing therapy
24
IV
Ayres, 2016
Pre-post study
Conventional swallowing therapy
11
IV
Wei, 2017
Non randomized CT
Out-of-hospital swallowing therapy
217
IV
Logemann, 2008
RCT (cross-over)
Chin-down posture, thickened liquids
360
III
Robbins, 2008
RCT
Chin-down posture, thickened liquids
255
I
Troche, 2008
RCT (cross-over)
Thickened liquids
10
IV
Nascimento, 2020
Pre-post study
Thickened liquids and Levodopa
50
IV
Ortega, 2020
Pre-post study
Thickened liquids
30
IV
Baert, 2021
Cross-sectional
Thickened liquids
83
III
Ayres, 2017
Non randomized CT
Chin-down posture
32
IV
Athukorala, 2014
Pre-post study
Skill-based swallowing training
10
IV
Sharkawi, 2002
Pre-post study
LSVT®
8
IV
Miles, 2017
Pre-post study
LSVT®
20
IV
Pitts, 2009
Pre-post study
EMST
10
IV
Troche, 2010
RCT
EMST
68
I
Byeon, 2013
RCT
EMST
33
IV
Troche, 2014**
Pre-post study
EMST
10
IV
Khedr, 2019
RCT
rTMS
33
I
Baijens, 2012
Pre-post study
TES
10
III
Heijnen, 2012
RCT
TES + standard swallowing therapy
109
IV
Baijens, 2013***
RCT
TES + standard swallowing therapy
109
II
Park, 2018
RCT
TES + standard swallowing therapy
18
IV
Alfonsi, 2010
Pre-post study
BT inoculation
7
IV
Alfonsi, 2017
Pre-post study
BT inoculation
12
IV
Howell, 2019
Pre-post study
Vocal fold augmentation
14
IV
* same study as Luchesi, 2013,**part of the patients from Troche 2010, ***same study as Heijnen, 2012.
Studies were classified according to various descriptors, including topic domain, sample size, design, presence of diagnostic criteria of the syndrome and level of evidence according to the Classification of Evidence Schemes of the Clinical Practice Guideline Process Manual of the American Academy of Neurology [
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
Consensus statements on dysphagia treatment in patients with PD are reported in Box 1. Several swallowing abnormalities are reported in patients with PD [
]. Pharyngeal impairment leads to reduced swallowing safety, i.e., penetration/aspiration, which is associated with an increased risk of aspiration pneumonia [
]. Thus, both pharyngeal and oral impairments deserve prompt and appropriate intervention, regardless of the PD stage. As soon as an impairment of swallowing function is clinically or instrumentally detected across any stages of swallowing, the need of a dysphagia treatment should be considered. Swallowing treatment should be specific and guided by instrumental findings about dysphagia pathophysiology. Videofluoroscopic swallowing study (VFSS) and/or fiberoptic endoscopic evaluation of swallowing (FEES) should be used to identify pathophysiological mechanisms that guide the definition of swallowing treatment and to assess its efficacy [
]. Swallowing electromyography and high-resolution manometry may also be useful for guiding dysphagia treatment. Treatment of dysphagia in PD may rely on a range of interventions. Regardless of the severity of dysphagia and the treatments performed, oral care should be maintained in all patients with PD and dysphagia to reduce the rate of aspiration pneumonia, as suggested by general dysphagia literature [
A) What clinical and/or instrumental abnormalities require appropriate treatment? Statements are based on expert opinion:
Ai.
Treatment should be started when there is clinical or instrumental evidence of impairment of swallowing safety and/or swallowing efficiency and/or reduced QOL, irrespective of the stage of the disease.
Aii.
When patients with PD require treatment for dysphagia, an instrumental assessment of swallowing is indicated to guide the treatment plan.
Aiii.
Treatment may include optimization of antiparkinsonian treatments, dietary modifications and fluid thickening, strategies for nutritional management, postures, swallowing maneuvers, swallowing exercises, neuromodulation, and medical treatments.
B) What are the treatment options for dysphagia in PD? B1) Optimization of PD treatments Statements are based on core literature consisting of Class II-III-IV level studies [
Patients should be tested during both the ON- and OFF-state to assess the impact of dopaminergic treatment on swallowing function.
B1ii.
Dopaminergic treatment should be optimized in patients with PD and dysphagia.
B1iii.
Patients with PD and dysphagia should preferably consume meals during their best ON-state.
B1iv.
In patients with PD undergoing DBS, dysphagia should be carefully assessed in the short and long-term to detect changes and provide intervention when necessary.
B2) Swallowing therapy Statements are based on core literature consisting of Class I-III-IV level studies [
Pathophysiology of swallowing dysfunction in Parkinson disease and lack of dopaminergic impact on the swallow function and on the effect of thickening agents.
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
Therapeutic effect, rheological properties and α-amylase resistance of a new mixed starch and xanthan gum thickener on four different phenotypes of patients with oropharyngeal dysphagia.
Effect of simultaneous application of postural techniques and expiratory muscle strength training on the enhancement of the swallowing function of patients with dysphagia caused by Parkinson’s disease.
Standard swallowing therapy is recommended for some patients with PD and dysphagia with sufficient cognitive level to follow clinicians' indications. When standard swallowing therapy is prescribed, it should address specific biomechanical and/or pathophysiological mechanisms, based on the instrumental findings.
B2ii.
Liquid thickeners may be beneficial in dysphagia associated to PD provided that the viscosity selection is guided instrumentally and the risk of dehydration is monitored.
B2iii.
Postures may have positive effects on dysphagia in some patients with PD. In the absence of precise selection criteria, based on expert opinion, effect of postures may be suggested on a case-by-case basis.
B2iv.
Skill-based therapy may be prescribed in non-demented PD patients with dysphagia to increase the precision of muscle contraction during swallowing. When prescribed, it should address specific biomechanical and/or pathophysiological mechanisms, based on the instrumental findings.
B2v.
LSVT® is designed to treat voice and should not be considered as a primary treatment for dysphagia in patient with PD.
B2vi.
EMST may be beneficial in some patients with PD and penetration or aspiration and adequate cognition to improve airway protection. When prescribed, it should address specific biomechanical and/or pathophysiological mechanisms, based on the instrumental findings.
B3) Neuromodulation Statements are based on core literature consisting of Class I-II-III-IV level studies [
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
There are no data available on the effects of tDCS in patients with PD and dysphagia.
B3ii.
rTMS may be associated to a beneficial effect on swallowing function in patients with PD, but its use is limited to research settings for the identification of standard protocols of stimulation.
B3iii.
The use of TES is not recommended for the treatment of dysphagia in patients with PD.
B4) Medical treatments Statements are based on core literature consisting of Class IV level studies [
Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders.
BT injection may be an option to treat patients with well-documented UES impairment, in the absence of other significantly impaired swallowing mechanisms or where the UES impairment can be considered as the main pathophysiological mechanism of dysphagia based on instrumental findings.
B4ii.
BT injection should be electromyography-guided and performed by experienced clinicians to avoid adverse effects.
B4iii.
There is insufficient evidence on the efficacy of vocal fold augmentation to reduce aspiration risk in patients with PD and dysphagia.
Treatment of PD rely on dopaminergic medications, infusion therapies and deep brain stimulation. Levodopa and dopamine replacement therapy is the gold-standard treatment for PD [
]. Dopaminergic treatment is known to improve motor function and pulmonary function tests (i.e. peak expiratory flow and upper-airway obstruction metrics) [
]. However, the effects on swallowing function are still debated. Based on the literature search, there is contradictory evidence that dopaminergic medications can improve or delay occurrence of dysphagia in PD. Few studies of Class III and IV with small sample size using different swallowing outcomes and short follow-up period have been conducted [
Effect of intestinal levodopa-carbidopa infusion on pharyngeal dysphagia: results from a retrospective pilot study in patients with Parkinson’s disease.
Pathophysiology of swallowing dysfunction in Parkinson disease and lack of dopaminergic impact on the swallow function and on the effect of thickening agents.
Some studies reported a beneficial effect of the levodopa-ON state on swallowing in about half of the patients with PD, regardless of the disease stage [
]. Other studies reported small improvements in swallowing efficiency after levodopa administration in a certain percentage of patients with PD; however, this improvement did not reduce the rate and the severity of penetration and aspiration [
Effect of intestinal levodopa-carbidopa infusion on pharyngeal dysphagia: results from a retrospective pilot study in patients with Parkinson’s disease.
Pathophysiology of swallowing dysfunction in Parkinson disease and lack of dopaminergic impact on the swallow function and on the effect of thickening agents.
Based on the literature, it is recommended to optimize the dopaminergic therapy in patients with PD and dysphagia, keeping in mind that the effects of this medications on swallowing function may either be beneficial or detrimental. In general, the timing of the administration of dopaminergic treatments should be planned so as to allow the patient to consume meals in the best ON-state. This means that patients should be advised to take levodopa-containing medications at least 30–60 min before meals [
], although more precise adjustments may be necessary on an individual basis. Dysphagia for medications is common in patients with PD, especially but not solely in the advanced stage [
]; therefore, patients' ability to swallow pills should be carefully investigated during instrumental assessment of swallowing, although the impact of dysphagia on dopaminergic response is still unclear [
Deep brain stimulation (DBS) is a widely used and accepted surgical procedure for the treatment of PD with motor fluctuations. Quadripolar electrodes are placed generally in the subthalamic nucleus (STN) or the globus pallidus internal segment (GPi). DBS has been reported to alleviate motor symptoms [
]) were retrieved from literature search. In the majority of the studies, DBS targeted the bilateral STN and was delivered with high frequency stimulation. Two studies compared the stimulation of the STN with the stimulation of the GPi [
]. Xie and colleagues analyzed the effects of a low-frequency stimulation (60 Hz) in patients with PD refractory to the standard high-frequency stimulation (130 Hz) [
]. Some studies provided low-level evidence (Class IV) of positive effects for the STN-DBS on dysphagia. Improvements of pharyngeal kinematic and/or patient-reported symptoms during the STN-DBS stimulation were reported in 6 studies [
]) of long-term potential negative effects on swallowing due to STN-DBS. Six months after surgery, Robertson et al. described detrimental effect of STN DBS on jaw kinematics during the oral preparatory phase, whereas an improvement of jaw kinematics in patients with GPi DBS [
]. Thus, if DBS is recommended for the treatment of other motor symptoms, clinicians should carefully monitor changes in swallowing function both in the short and the long-term.
3.3.2 Swallowing therapy
In patients with PD, due to the progressive nature of the disease, swallowing therapy aims to maintain functional swallowing to provide adequate nutrition and hydration without pulmonary complications as long as possible. Swallowing therapy relies on compensatory and rehabilitative strategies. Compensatory strategies are designed to ease the bolus flow by making eating and drinking safer and easier without actually changing the physiology of the swallow [
Conventional swallowing therapy includes a variety of interventions, such as counseling on swallowing physiology and dysphagia pathophysiology, strategies for meal management, and behavioral therapy (swallowing maneuvers, strengthening exercises, thermal tactile stimulations). Although widely applied in clinical practice, only 4 studies investigated the efficacy of conventional swallowing therapy in patients with PD [
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
]. Luchesi and colleagues followed-up 24 patients with PD who received swallowing therapy including compensatory strategies, swallowing and non-swallowing exercises, and sensory stimulation every 3 months over a 5-year period [
]. Based on the recommended diet type following a fiberoptic endoscopic evaluation of swallowing, they reported improved swallowing function in 10 patients, maintained swallowing function in 5 patients, and a worsening of the swallowing function in 9 patients. Another study analyzed the impact on QOL of a 4-month weekly intervention of conventional swallowing therapy including food modifications and postural adaptations [
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
], but the lack of a control group and instrumental outcomes limits the strength of the results. Manor and colleagues compared the efficacy of conventional swallowing therapy with the efficacy of a video-assisted swallowing therapy [
]. During the video-assisted swallowing therapy, video-recordings from the fiberoptic endoscopic evaluation of swallowing are showed to the patients to improve patient's knowledge on swallowing physiology and pathophysiology and provide off-line biofeedback during the training of compensatory techniques. Both groups significantly reduced the severity of pharyngeal residue, with significantly higher improvements in the video-assisted group. Moreover, swallowing-related QOL was significantly improved in the video-assisted groups after the treatment and at the 6-months follow-up. Finally, Wei and colleagues investigated the efficacy of a community swallowing management regimen targeting patients with PD and dysphagia and their caregivers and including education training sessions on dysphagia knowledge, strategies for meal management, compensatory strategies, and strengthening exercises [
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
]) that standard swallowing therapy can improve dysphagia in PD. When adopted in the early phases of PD, the swallowing therapy seems to be associated with a greater improvement in QOL [
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
]. However, the definition of conventional swallowing therapy is unclear and/or inconsistently applied in the published literature. The lack of control groups of patients with no intervention reduces the quality of the evidence. Some studies [
The impact of dysphagia therapy on quality of life in patients with Parkinson’s disease as measured by the swallowing quality of life questionnaire (SWALQOL).
] excluded patients with dementia. The ability to follow clinician's instruction is critical for many swallowing and non-swallowing exercises, thus, in case of cognitive impairment, the range of interventions from conventional swallowing therapy would be limited.
Compensatory treatments include bolus modifications, postures, swallowing maneuvers, and sensory stimulation. The effects are immediate. However, the long-term effects on dysphagia-related complications may not reflect immediate benefits.
Aspiration of thin liquids is common in PD. In patients with dysphagia, thickening of liquids improves the situation by slowing down the flow of liquids, which allows more time for airway closure [
Pathophysiology of swallowing dysfunction in Parkinson disease and lack of dopaminergic impact on the swallow function and on the effect of thickening agents.
Therapeutic effect, rheological properties and α-amylase resistance of a new mixed starch and xanthan gum thickener on four different phenotypes of patients with oropharyngeal dysphagia.
]) that thickening liquids reduces the risk of aspiration in patients with PD. However, very thickened liquids are often considered unpleasant and a fatigue effect can be observed [
]. Patient-reported palatability was found to be reduced for all types of thickeners, with gum-based thickeners demonstrating lower taste and aroma intensity compared to startch-based thickeners [
]) when compared to the chin-down posture intervention with thin liquids. In one study, patients with PD randomized to honey-thickened liquids were reported to exhibit a higher rate of aspiration pneumonia, dehydration, fever, and urinary tract infections compared to patients drinking thin liquids with the chin-down posture, although the differences were not significant and both interventions were associated to a lower than the expected rate of pneumonia [
]. New generations of gum thickeners cause a strong viscosity-dependent therapeutic effect on the safety of the swallow. This effect depends on the phenotype and is similar among elderly, PD and post-stroke patients [
Therapeutic effect, rheological properties and α-amylase resistance of a new mixed starch and xanthan gum thickener on four different phenotypes of patients with oropharyngeal dysphagia.
Systematic review and evidence based recommendations on texture modified foods and thickened liquids for adults (above 17 years) with oropharyngeal dysphagia - an updated clinical guideline.
]. Because of cognitive impairment, anatomic postural changes, and tremor, chin-down posture in patients with PD may be challenging. There is still insufficient evidence (Class III-IV [
Therapeutic effect, rheological properties and α-amylase resistance of a new mixed starch and xanthan gum thickener on four different phenotypes of patients with oropharyngeal dysphagia.
Systematic review and evidence based recommendations on texture modified foods and thickened liquids for adults (above 17 years) with oropharyngeal dysphagia - an updated clinical guideline.
]. It should be taken into account that patients with PD often present with abnormal posture, such as camptocormia and antecollis, which results in spontaneously adopting a chin-down posture during swallowing. Hence, when aspiration of liquids and foods is detected in these patients, the possibility to apply a chin-down posture as a compensatory strategy to reduce the aspiration risk is limited.
Thus, the use of compensatory strategies may be suggested in patients with PD on a case-by-case basis. The recommendation should always rely on three aspects: (i) the immediate efficacy to eliminate aspiration verified during the instrumental assessment, (ii) the risk of pulmonary complication and dehydration, and (iii) patients' and caregivers' preferences.
Swallowing exercises from conventional swallowing therapy are designed to improve the strength of the muscles involved during swallowing. Recently, a shift toward including skill-based exercises in the swallowing therapy of PD patients has been observed. Skill training is the process of learning and fine-tuning new sequences of movements [
]. The study included 10 patients with PD and dysphagia. Patients with dementia were excluded. Patients underwent 10 skill training therapy sessions over a 2-week period using a surface EMG biofeedback device and the Biofeedback in Swallowing Skill Training software. The protocol included tasks with increasing difficulty and immediate feedback. The aim was to improve the precision of swallowing muscle contraction by developing conscious control over timing and strength of swallowing. Post-treatment, swallowing rate for liquids, surface EMG durational parameters of premotor time and pre-swallow time improved. Although the short-term results suggest an improvement in swallowing efficiency, there is currently low-level evidence (Class IV) that swallowing skill-based training can improve dysphagia in PD [
]. Therefore, additional research is needed to better quantify the efficacy of this approach.
Lee Silverman Voice Therapy (LSVT®) is a standardized and intensive voice training designed specifically for patients with PD. LSVT® improved loudness up to two years after treatment [
Effects of intensive voice treatment (the Lee Silverman Voice Treatment [LSVT]) on vowel articulation in dysarthric individuals with idiopathic Parkinson’s disease: acoustic and perceptual findings.
The science and practice of LSVT/LOUD: neural plasticity-principled approach to treating individuals with Parkinson’s disease and other neurological disorders.
], which yielded low-level evidence that LSVT® influences swallowing as a by-product of voice treatment. Sharkawi and colleagues investigated swallowing changes on VFSS in 8 patients with PD who underwent the LSVT® [
]. After treatment, they observed a reduction of half of the swallowing motility disorders observed at the baselined and an improvement in some swallowing temporal measures and in oral residue. Miller et al. analyzed the swallowing effects of LSVT® in 20 patients with PD with vocal deterioration and adequate cognition to perform the treatment [
]. PD severity was mild and 40% of the patient sample reported mild symptoms of swallowing impairment. Self-reported swallowing assessment was found to be improved both 1 week and 6 months after the end of the treatment compared to the baseline. Significant changes in pharyngeal constriction, upper esophageal sphincter opening, and residue were detected during VFSS, although VFSS measures were generally normal at baseline. However, LSVT® does not specifically target swallowing function and it should not be considered as a primary treatment of dysphagia in PD.
Expiratory muscle strength training (EMST) is a behavioral treatment aiming to increase expiratory and submental muscle force production. EMST is known to be effective in improving maximum expiratory pressure and cough effectiveness [
Expiratory muscle strength training in persons with multiple sclerosis having mild to moderate disability: effect on maximal expiratory pressure, pulmonary function, and maximal voluntary cough.
]. The efficacy of EMST on swallowing function in patients with PD has been investigated by several studies. In 2009, Pitts and colleagues studied 10 mid-stage patients with PD exhibiting penetration or aspiration during videofluoroscopy and adequate cognition who underwent a 4 -week training using the EMST [
]. After training, several parameters of volitional cough were improved and the PAS score was significantly reduced. However, 6 out of 10 patients continued to exhibit penetration after the training. In 2010, Troche et al. conducted a randomized controlled trial on 68 patients with PD reporting symptoms of dysphagia [
]. Patients were randomized to the active EMST and the sham-EMST. After the 4-week training, only the patients in the active EMST showed a significant although small reduction in the PAS score (mean change 0.61 ± 1.43). Afterwards, 10 patients in the active EMST training underwent a detraining period and were reassessed with VFSS after 3 months [
]. After the detraining period, PAS scores were on average unchanged compared to the post-training assessment. However, no data from the control group were available at this time-point. Finally, Byeon studied the efficacy of EMST in 33 patients with PD and dysphagia and reported significant improvement on swallowing function as detected by VFSS after 4 weeks of training [
Effect of simultaneous application of postural techniques and expiratory muscle strength training on the enhancement of the swallowing function of patients with dysphagia caused by Parkinson’s disease.
Effect of simultaneous application of postural techniques and expiratory muscle strength training on the enhancement of the swallowing function of patients with dysphagia caused by Parkinson’s disease.
]) that EMST can improve dysphagia in PD, although the effect size is small.
3.3.3 Neurostimulation
Neurostimulation techniques include non-invasive brain stimulation (NIBS) and transcutaneous electrical stimulation (TES).
Researchers have investigated the possibility to use NIBS techniques for dysphagia rehabilitation. NIBS is based on the principle of neuroplasticity, defined as changes in neuronal pathways to increase neural functioning via synaptogenesis, reorganization, and network strengthening and suppression [
]. The most commonly used techniques are transcranial direct current stimulation (tDCS) and repetitive transcranial magnetic stimulation (rTMS). The literature search failed to retrieved studies assessing the effects of tDCS on swallowing in PD. Thus, future studies are needed to provide evidence for its application in dysphagia management in this population. There is preliminary evidence from 1 study (Class I [
The effect of high-frequency repetitive transcranial magnetic stimulation on advancing Parkinson’s disease with dysphagia: double blind randomized clinical trial.
]) that suggests a positive effect of rTMS on dysphagia in PD. Khedr and colleguaes randomized 33 patients with PD and dysphagia to a sham rTMS group and a real rTMS group (2000 pulses; 20 Hz; 90% resting motor threshold; 10 trains of 10 s with 25 s between each train) over the hand area of each motor cortex (5 min between hemispheres) for 10 days (5 days per week) followed by 5 booster sessions every month for 3 months [
The effect of high-frequency repetitive transcranial magnetic stimulation on advancing Parkinson’s disease with dysphagia: double blind randomized clinical trial.
]. The authors found an improvement in self-reported dysphagia, hyoid elevation, and pharyngeal transit time only in the real rTMS group, suggesting that rTMS may be effective in improving swallowing function in patients with PD, although no changes were recorded for penetration and aspiration or residue. Since data are available from a single study on a relatively small sample size and standard treatment protocols are lacking, rTMS for the treatment of dysphagia in patients with PD is currently not recommended in clinical practice.
Transcutaneous electrical stimulation (TES) has been introduced in dysphagia treatment as a therapeutic adjunct to standard swallowing therapy [
]. TES delivers stimulation to the muscles through surface electrodes. By stimulating the nerve and the motor end plate of the nerve in the muscle fibers, TES promotes a re-training of the functional muscle contraction patterns [
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
]. Baijens et al. tested the effects of TES (VitalStim® electrical stimulator) in different electrode positions (above the hyoid bone, below the hyoid bone, and both) on swallowing function in 10 patients with PD and dysphagia [
]. The majority of temporal, spatial, and visuoperceptual VFSS variables were unchanged during TES regardless of the electrode position. The few significant changes to VFSS parameters suggested a potential detrimental effect of TES on dysphagia in patients with PD, especially when the electrodes were placed only below the hyoid bone. Three studies compared the efficacy of the adjunct of TES to standard swallowing therapy to efficacy of the standard swallowing therapy alone [
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
]. Dysphagia significantly improved in both groups compared to the baseline assessment, but no significant difference was found between the two interventions. A group of authors from the Netherlands randomized 109 patients with PD to 3 groups of intervention: (i) standard swallowing therapy, (ii) standard swallowing therapy plus motor-level TES, (iii) standard swallowing therapy plus sensory-level TES. After the intervention no statistical differences in FEES and VFS parameters [
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
] were found among the 3 groups. Similar findings were reported by Park and colleagues comparing the standard swallowing therapy to the standard swallowing therapy with the adjunct of TES in 18 patients with PD and dysphagia [
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
]. Overall, both groups showed an improvement of swallowing function as measured by VFSS. No significant changes were found between the groups, except for a higher improvement in the hyoid displacement in the TES group. Thus, the adjunct of TES does not seem to result in a significant improvement of dysphagia outcomes in PD beyond those attributable to standard swallowing therapy [
Neuromuscular electrical stimulation versus traditional therapy in patients with Parkinson’s disease and oropharyngeal dysphagia: effects on quality of life.
Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial.
Medical approaches for dysphagia may be indicated for selected pathophysiological impairments, specifically inadequate lower airway protection and upper esophageal sphincter (UES) dysfunction, by means of pharmacological treatments and surgery.
Among pharmacological options, botulinum toxin (BT) may be considered for the treatment of dysphagia due to spasm and/or reduced relaxation of the UES. BT injection is delivered into the cricopharyngeal muscle (main component of the UES), improving UES relaxation during swallowing. Two studies analyzed the efficacy of unilateral BT injection in the cricopharyngeal muscle in PD patients with dysphagia [
Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders.
Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders.
Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders.
]) that BT injection improves dysphagia in PD. Nevertheless, some aspects should be considered. Firstly, when inadequate UES opening is observed during VFSS or FEES, a careful electromyographic evaluation of the activity of the cricopharyngeal muscle is recommended to ascertain whether inadequate UES relaxation is due to an altered control of the muscle tone or to other causes which require a different intervention. Pharyngeal high-resolution impedance manometry may also guide the identification and selection of candidates for this treatment. Secondly, before BT injection, it is essential to verify that other swallowing mechanisms, such as laryngeal closure, elevation and anterior misplacement, are preserved. This is essential to maintain airways safety, considering that the BT treatment results in both a greater UES relaxation during swallowing and a lower cricopharyngeal muscle resting tone, which may increase the risk of aspiration of gastric contents from the esophagus. Additionally, BT injection into the cricopharyngeal muscle exposes to the risk of diffusion of the toxin to nearby muscles involved in laryngeal and vocal fold motility with potential risk of respiratory and phonation disturbances [
Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders.
]. Taken together, it is recommended that BT injection should be electromyography-guided and performed by experienced clinicians that should also optimize the injected dose to obtain the desired effect on the UES, while minimizing the risk of adverse effects.
Glottic insufficiency has been reported in around 60% of patients with PD [
]. Injection laryngoplasty is a surgical technique aimed at augmenting and medializing the vocal fold to decrease the glottic insufficiency caused by a variety of medical conditions. One retrospective Class IV study investigated the efficacy of vocal fold augmentation through injection laryngoplasty in adjunct to speech and language therapy on a small sample of patients with PD (n = 14) with glottal insufficiency and vocal bowing [
]. The procedure was found to be safe in all patients. The authors reported that injection laryngoplasty seems to improve glottic closure and reduce the severity of patient-reported symptoms of dysphagia. However, no control group was available, the outcomes data were missing for some of the patients, no statistical analysis was performed due to the small sample size, and instrumental assessment before and after treatment was lacking to confirm the efficacy and safety of the procedure on swallowing. Thus, future studies are needed to test the feasibility of injection laryngoplasty as a therapeutic option for dysphagia in PD.
3.4 Nutritional management
3.4.1 Nutritional interventions
Consensus statements on nutritional management of patients with PD and dysphagia are reported in Box 2. Despite limited evidence from intervention studies on the management of dysphagia by oral nutritional interventions is available, there is strong consensus on the importance of nutritional care in PD [
] and it is substantially agreed that referral to a nutrition specialist should be part of the routine clinical workup since the earliest stages of PD [
Statements on the nutritional management of patients with PD and dysphagia.
Tabled
1
C) What are the nutritional interventions for patients with PD and dysphagia? Statements are based on expert opinion:
Ci.
Nutritional intervention should be prescribed based on a multidisciplinary evaluation (including neurologist, ENT, phoniatrician, gastroenterologists, speech-language pathologists, dietitians, and clinical nutritionists) and may include dietary counseling (including oral nutritional supplements), texture modified diet, as well as artificial nutrition.
Cii.
Intervention should focus not only on safety and efficiency of swallowing, swallowing-related QOL, but also on both general (nutritional status, hydration status, energy balance) and disease-specific (levodopa containing medications and protein intake interactions, vitamin status, fiber intake) issues.
D) When should percutaneous endoscopic gastrostomy indicated for the nutrition of patients with PD and dysphagia? Statements are based on expert opinion:
Di.
PEG should be placed in case of inadequate oral intake expected to be longer than 4 weeks resulting in involuntary body weight loss (≥5% in 1 month or ≥10% in 3 months) and/or significant risk of prandial aspiration exceeding the risk of aspiration of reflux.
Dii.
In case of potentially reversible swallowing impairment (short-term exacerbation or expectations of positive treatment response), nasogastric tube feeding should be considered.
Diii.
PEG feeding should be carefully considered on an individual basis taking into account patient and family choice, caregiving context, health ethics, prognosis and QOL.
Div.
In case of dementia, PEG insertion is not indicated.
Dv.
In case of continuous intra-jejunal levodopa infusion, oral nutrition may be continued in patients with sufficiently safe and efficient swallowing.
Dvi.
Oral hygiene interventions and oral intake (if safe based on clinical/instrumental assessment) should be continued even after PEG placement.
Nutritional interventions for dysphagia in PD should be prescribed on the basis of a multi-disciplinary evaluation by specialized personnel (neurologists, ENT, phoniatricians, gastroenterologists, speech-language pathologists, dieticians, and clinical nutritionists).
Nutritional interventions should address not only the safety and efficacy of swallowing, to reduce the risk of dehydration, malnutrition, and aspiration, but should also take into account general and disease-specific issues. Furthermore, interventions should be balanced on an individual basis with pertinent risk-benefit analysis and monitoring of the impact on QOL.
Dietary counseling including the use of oral nutritional supplements and texture-modified oral diets represents the first-line nutritional strategy for treating dysphagia. To prevent or treat malnutrition and muscle loss, the diet should be of adequate protein-calorie content and density, resulting in higher energy intake with reduced meal interruption and feeding assistance. Nevertheless, monitoring of compliance is mandatory as these diets could be unpleasant and may lead to reduced energy and protein intake [
]. As neutral aminoacids and levodopa compete for transportation through a specific active-transport system in the small intestine and at the blood-brain barrier, protein-redistribution diet (low-protein breakfast and lunch and consumption of a second-course only at dinner) with normal protein content (1.0–1.2 g/kg/day) should be considered to maximize levodopa absorption and efficacy, particularly in patients experiencing motor fluctuations. There is no evidence supporting the use of low-protein, gluten-free or plant-food based diets. Dietary modifications should also address the need to guarantee or improve the status of relevant vitamins (vitamin D, folic acid, vitamin B12) [
]. The maintenance of adequate fiber intake with texture-modified diets may be difficult and should be also taken into account considering the frequency of constipation in patients with PD [
There are no PD-specific recommended criteria to guide percutaneous endoscopic gastrostomy (PEG) placement in daily practice and there are no data indicating that tube feeding prolongs survival in PD or improves QOL. Accordingly, we suggest referring to available international guidelines dealing with this issue [
Where oral feeding is no longer possible, safe or adequate in covering energy and fluids requirements, thus resulting in significant weight loss (e.g. about 5% in 1 month or 10% in 3 months) and/or dehydration, tube feeding should be considered on an individual basis taking into account patient willingness, caregiving context, ethical reasons, respiratory function and the patient's general condition, prognosis and expected outcomes [
]. In case of potentially reversible swallowing impairment, nasogastric tube feeding should be considered, but when impairment is expected to be longer than 4 weeks PEG insertion should be considered as it has been associated with better QOL [
]. However, PEG placement does not eliminate the risk of aspiration. Accordingly, high-risk patients, as well as those presenting gastroduodenal motility problems, should be candidates for a jejunal extension tube (PEG-J) or jejunostomy and post-pyloric feeding [
]. In the advanced stages of the disease, patients with PD may require continuous intrajejunal delivery of levodopa-carbidopa intestinal gel via a PEG-J. In presence of concomitant dysphagia, anticipated enteral nutrition through the gastric port could be considered in these patients. Patient's monitoring is mandatory as the infusion of nutrition could negatively affect levodopa absorption and efficacy [
] and both interventions may need implementation by adjusting medication dosages and/or changing the nutritional treatment regimen. Nonetheless, gastroparesis might be a limiting factor for gastric feeding and the use of prokinetic agents should be considered [
Enteral nutrition could be either exclusive or integrative as oral intake should be continued even after PEG placement, if safe based on instrumental assessment. In both cases, oral hygiene interventions should be implemented to reduce the risk of aspiration pneumonia.
3.5 Limitations of the study
Some shortcomings of the present work should be mentioned. Firstly, the recruitment of participants lacked a strictly codified methodology for selection and was mainly based on practical considerations and on their voluntary acceptance of our invitation. Thus, the expert group had a prevalent representation of neurologists compared to other specialists and of Italian specialists compared to specialists from other countries. Consequently, it is possible that the statements elaborated by this panel group do not reflect entirely the point of view of the wider international medical and scientific communities. Nevertheless, it should be mentioned that we put in place several measures to involve as many experts in the field as possible and that, once the panel was created based on voluntary adhesion, the ruling process was supported by a thorough revision of the data available from the literature. Another limitation of the consensus process is that PD patients, their caregivers, or representatives were not involved.
3.6 Directions for future research
This consensus process identified several research gaps emerged on the treatment and the nutritional management of PD patients with dysphagia that could not be properly addressed by the panel of experts due to the lack of reliable evidence. In particular, the experts agreed on the need for large, well-designed studies to:
1.
investigate the optimal time in the disease to initiate intervention for swallowing and to explore the impact of the natural evolution of dysphagia in patients with PD
2.
evaluate the efficacy and adverse effects of compensatory treatment on clinical endpoints such are nutrition, hydration, respiratory complication, hospital readmission, QOL and mortality in patients with PD and dysphagia
3.
compare the efficacy and complications of different swallowing treatments and to evaluate their effect on the progression of dysphagia in PD
4.
evaluate the impact of nutritional intervention for dysphagia in patients with PD, including the impact of PEG placement on nutrition, respiratory complication, QOL and mortality.
Funding
This work was supported by grants of the Italian Ministry of Health to Ricerca Corrente 2020-2021. The Consensus Conference was founded by the IRCCS Mondino Foundation, Pavia, Italy.
Questions on screening and diagnosis: presence and absence of oropharyngeal dysphagia, and any diagnostic test or screening test.
Questions on prognosis: oropharyngeal dysphagia as exposures.
Question on treatment: any treatment of oropharyngeal dysphagia.
Comparator(s)/control
Not applicable.
Main outcome(s)
The primary outcome of the systematic review is to provide the evidence to an International Consensus Conference on oropharyngeal in Parkinson's disease (PD), that has the aim to (1) establish the screening pathway of oropharyngeal dysphagia in PD, (2) define the diagnostic criteria of oropharyngeal dysphagia in PD, (3) define the prognostic value of oropharyngeal dysphagia on MSA survival and QOL, (4) suggest the therapeutic options for oropharyngeal dysphagia.
Appendix 2. Search strategy on MEDLINE
(“deglutition disorders”[MeSH] OR (“deglutition disorder”[All Fields] OR “deglutition disorders”[All Fields] OR “swallowing disorders”[All Fields] OR “swallowing disorder”[All Fields] OR (“deglutition disorders”[MeSH Terms] OR (“deglutition”[All Fields] AND “disorders”[All Fields]) OR “deglutition disorders”[All Fields] OR “dysphagia”[All Fields])))
AND
(“Parkinson's disease”[Mesh] OR (“Parkinson's disease”[All Fields] OR “Parkinson's disease”[All Fields] OR Parkinson[All Fields]))
AAN (American Academy of Neurology). Clinical Practice Guideline Process Manual, 2011 Ed. St. Paul, MN: The American Academy of Neurology [online]. Available at: http://tools.aan.com/globals/axon/assets/9023.pdf. Accessed September 29, 2018.
Cosentino G, Avenal M, Schindler A et al. A multinational consensus on dysphagia in Parkinson's disease - screening, diagnosis and prognostic value. J. Neurol. (In press).
Effect of intestinal levodopa-carbidopa infusion on pharyngeal dysphagia: results from a retrospective pilot study in patients with Parkinson’s disease.
Pathophysiology of swallowing dysfunction in Parkinson disease and lack of dopaminergic impact on the swallow function and on the effect of thickening agents.
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