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Table of Contents
ORIGINAL ARTICLES
Year : 2021  |  Volume : 4  |  Issue : 2  |  Page : 73-79

Dysphagia in Parkinson’s disease: Analysis of screening questionnaire and videofluoroscopy findings


1 Department of Deglutology and Swallowing Disorders, Amrita Institute of Medical Sciences, Kerala, India
2 Department of Neurology, Amrita Institute of Medical Sciences, Kerala, India
3 Department of Head and Neck Surgery and Oncology, Amrita Institute of Medical Sciences, Kerala, India
4 Department of ENT, Amrita Institute of Medical Sciences, Kerala, India

Date of Submission09-Sep-2020
Date of Decision12-Mar-2021
Date of Acceptance28-Jul-2021
Date of Web Publication30-Aug-2021

Correspondence Address:
Dr. Unnikrishnan K Menon
Department of ENT, Amrita Institute of Medical Sciences, Kochi, Kerala.
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AOMD.AOMD_43_20

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  Abstract 

Background: Dysphagia is a common symptom of Parkinson’s disease (PD), which is often overlooked. Reliable screening methods for definitive radiological investigation need to be developed. Objectives: To analyze the objective videofluoroscopic study of swallowing (VFSS) findings in PD patients screened using a validated 11-item swallowing disturbance questionnaire (SDQ) and to check for a correlation between the questionnaire and VFSS scale scores, as well as the sensitivity of SDQ to detect abnormal VFSS findings. Material and Methods: PD patients attending a movement disorder clinic were screened using SDQ and underwent VFSS. The findings were recorded and objectively rated by experienced speech and language pathologists using standardized scales. Statistical analysis was performed to check for correlation. Results: Twelve patients were enrolled in the study. Their SDQ scores ranged from 2 to 16. Of the 11 questions, six were checked for correlation with VFSS findings. Bolus stuck in the mouth was reported by four patients; all displayed corresponding VFSS findings. Oral residue was reported by nine, of which seven showed VFSS findings. Multiple swallows were reported by eight, and VFSS findings were observed in seven of them. Overall, even at very low scores, abnormalities were observed in corresponding VFSS parameters. However, no statistical significance (P > 0.05) was found between the SDQ scores and VFSS parameters. Conclusion: VFSS analysis revealed abnormal oropharyngeal swallowing parameters, which corresponded with the SDQ scores, but without statistical significance. Therefore, our questionnaire is a useful tool to predict VFSS findings in PD patients.

Keywords: Correlation study, oropharyngeal dysphagia, Parkinson’s disease, screening questionnaire, videofluoroscopy


How to cite this article:
Aarthi RS, Radhakrishnan SK, Vidhyadharan S, Menon UK, Arya CJ, Thankappan K. Dysphagia in Parkinson’s disease: Analysis of screening questionnaire and videofluoroscopy findings. Ann Mov Disord 2021;4:73-9

How to cite this URL:
Aarthi RS, Radhakrishnan SK, Vidhyadharan S, Menon UK, Arya CJ, Thankappan K. Dysphagia in Parkinson’s disease: Analysis of screening questionnaire and videofluoroscopy findings. Ann Mov Disord [serial online] 2021 [cited 2021 Dec 1];4:73-9. Available from: https://www.aomd.in/text.asp?2021/4/2/73/324803




  Introduction Top


Dysphagia is a common symptom in patients with Parkinson’s disease (PD).[1] Although pathological changes are seen early in the brainstem structures in PD, clinical features of dysphagia in PD patients usually occur in advanced stages. This affects the quality of life, impairs medication intake, and leads to malnutrition and aspiration pneumonia, which is the major cause of death in PD patients.[2]

However, some studies have shown that swallowing problems may not be a phenomenon in only advanced-stage PD. Even if present in the early stages, patients may not complain because they may be unaware of alterations in swallowing.[3] The main issues hampering the early detection of swallowing problems are under-reporting of dysphagia by PD patients during usual out-patient interviews and the lack of short, sensitive questionnaire tools which can be used in an out-patient setting. To bridge this gap, two of the authors of the present study had devised a tool which was validated and used in a series of PD cases, an 11-item questionnaire to assess swallowing difficulty (SDQ).[4],[5] This has been named as the Amrita Institute of Medical Sciences Swallowing Difficulty Questionnaire (AIMS-SDQ), specifically to be used for PD cases, or those conditions causing predominantly oral and oropharyngeal phase dysphagia [Appendix 1].



The two main investigative procedures for dysphagia are flexible endoscopic evaluation of swallowing (FEES) and videofluoroscopic study of swallowing (VFSS). The latter is often referred to as the gold standard, although both are used as complementary procedures. However, due to the nature of the pathology of PD, VFSS is considered more suitable. Descriptive findings that can be objectively documented have been described for this radiological investigation. Swallowing problems have been noted in 75–100% patients during VFSS examination.[3]

Our paper aims to study the correlation, if any, between VFSS findings and AIMS–SDQ responses in PD patients. The primary objective was to analyze objective VFSS findings in idiopathic PD (IPD) patients screened using a validated questionnaire (AIMS–SDQ). In addition, we aimed to investigate a correlation between the scores of subjective AIMS–SDQ responses and objective VFSS findings, as well as check if AIMS–SDQ is an adequately sensitive tool to predict abnormal VFSS findings.


  Materials and Methods Top


The study was approved by the Institutional Review Board: IRB-AIMS-2020-051

Sample size

To the best of our knowledge, there are no similar studies available in the literature; therefore, there is no statistically calculated sample size. Our study was conducted as a pilot study.

Patient selection

Patients attending the  Parkinsonism More Details Clinic within the Department of Neurology at Amrita Institute of Medical Sciences, Kochi, during a 10-month period (August 2019 to June 2020) were screened for the study. All patients were examined by a neurologist/movement disorder specialist. Patients with PD were diagnosed according to the United Kingdom Parkinson’s Disease Brain Bank criteria. Their disability was graded based on the Hoehn and Yahr scale. Patients with severe disability and those having significant off periods clinically were excluded from screening.

The inclusion criteria were as follows: patients diagnosed with IPD, ≥40 years of age, male and female, Hoehn and Yahr stages 1–4, and AIMS–SDQ score of ≥1. The exclusion criteria included patients diagnosed with atypical PD and secondary Parkinsonism, bed-ridden patients with an advanced disease stage, and those with nasogastric tubes.

Following these criteria, 12 patients were selected for our study.

Methodology

The selected patients were referred to the dysphagia clinic at the Institute and were reviewed by speech and language pathologists (SLPs) specialized in the management of swallowing disorders. The patients were screened for swallowing dysfunction by completing AIMS–SDQ, either by themselves or with the help of a caregiver.

After clinical assessment, the patients were counselled for VFSS. The procedure was approved by the institution’s ethics committee and was conducted in the radiology suite after obtaining signed informed consent from the patients. A contrast material (barium sulphate) was orally presented in different consistencies (thin and thick) and quantities (3 ml, 5 ml, and 10 ml) with the patients positioned in two planes (anteroposterior and lateral) for evaluation of all the stages of swallowing. The fluoroscopy unit was turned on every 15 to 30 seconds to minimize radiation exposure. It was run continuously only when swallowing function changed, usually signaled by spillover of material into the pyriform sinuses before initiation of the pharyngeal response. Overall, maximum radiation exposure was maintained at a limit of not more than 2 minutes.

Two SLPs, experienced in VFSS and who were blinded to the patients’ clinical condition, independently evaluated the findings. Eight parameters were assessed in total, as shown in [Table 1]. Among these eight, lingual incoordination, poor bolus propulsion, presence of oral residue, multiple swallows, bolus residue scale (BRS), penetration–aspiration scale (PAS), and dysphagia severity rating scale (DSRS) were considered for the analysis. BRS, PAS, and DSRS were rated by SLPs for standardized scores, as detailed below.
Table 1: VFSS parameters assessed and documented by SLPs

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DSRS: This scale indicates the severity of the impairment/deficit rather than only the status of the functional diet. It is a 7-point scale, ranging from 0 (normal) to 6 (severe).[6]

BRS: This is an observational scale used to determine the absence or presence of contrast residue in the valleculae, pyriform sinuses and/or the posterior pharyngeal wall.[7]

PAS: This is an 8-point scale used to grade the severity of penetration and aspiration of residue by characterizing the depth and response to invasion of contrast into the laryngeal introitus.[8]

The above rating scores, as provided by SLPs, were statistically analyzed to investigate their correlation with SDQ. In particular, six AIMS–SDQ questions were assessed, as detailed in [Table 2].
Table 2: Details of the six parameters checked for correlation between AIMS–SDQ and VFSS

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Statistical analysis

Pearson’s correlation co-efficient between the SDQ score and each VFSS rating score was computed with 95% confidence interval.


  Results Top


A total of 12 patients were included in the study and responses to the questionnaire were obtained from all. There were nine men and three women, with a mean age of 64 years (range, 40–79 years) and mean disease duration of 11.8 years (range, 3–25 years). Grading based on the Hoehn and Yahr scale showed that all patients had mild to moderate PD ([Table 3]). The scoring system for AIMS–SDQ allows for a range of 0–22. In this study, the lowest questionnaire score was 2 and the highest was 16 ([Table 4]). Analysis of the six VFSS parameters and their correlation with the questionnaire scores and VFSS are as follows:
Table 3: Patient demographics and baseline data

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Table 4: AIMS–StDQ score range

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  • A] Bolus stuck in the mouth: 4/12 (25%) patients answered positively to Q. 2 of the questionnaire. In VFSS, all four patients had poor bolus propulsion; however, one patient also had lingual incoordination, with lingual pumping not identified in any of the patients. Among the remaining eight patients who responded negatively, all had poor bolus formation. However, six of them had both lingual incoordination and lingual pumping.


  • B] Oral residue: 9/12 (75%) patients answered positively to Q. 4. However, the VFSS assessment reported only 7/12 (58%) patients having oral residue. Furthermore, those patients who scored a zero in Q. 4 had evidence of oral residue on VFSS ([Table 5]).


  • C] BRS: 3/12 (25%) patients reported that the bolus was stuck in the throat (Q. 7). The VFSS findings of bolus residue were confirmed in two of the three patients. Nine (75%) patients did not report that the bolus was stuck in the throat after swallowing. Among these nine patients, the VFSS findings for residue were confirmed in seven, but no residue was noted in the vallecula or hypo pharynx of two patients ([Table 6]). There was no statistically significant difference between the compared scores (Pearson’s correlation co-efficient, 0; P > 0.05).


  • D] Multiple Swallows: In SDQ, 8/12 (66.6%) patients answered positively to Q. 8. Among them, seven had the abnormal finding of more than two swallows for a single bolus on VFSS. VFSS confirmed the absence of findings in three of the four remaining patients, while one patient had multiple swallows ([Table 7]).


  • E] PAS and BRS scores: 3/12 (25%) patients answered positively to Q. 10, and only one patient had a confirmed abnormal finding on VFSS. Of the nine patients who answered negatively, one had normal PAS and BRS scores and eight had abnormal PAS (3/9) and BRS (7/9) scores on VFSS ([Table 8]). There was no significant correlation between the scores (Pearson’s correlation co-efficient, -0.30861; P = 0.33).


  • F] PAS: 7/12 (58.3%) patients answered positively to Q. 11. Of these, only two (28.5%) confirmed penetration on VFSS. Among the remaining five patients who answered negatively, one had penetration (PAS score 2) and the remaining four had normal swallows (PAS score 1). Taken together, the answers to Q. 11 of 6/12 (50%) patients correlated with the VFSS parameter, the PAS score. There was no statistically significant association between the compared scores (Pearson’s correlation co-efficient, -0.45175; P = 0.1404).
Table 5: Association between score of AIMS–SDQ question number 4 and VFSS parameter

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Table 6: Association between score of AIMS–SDQ question number 7 and VFSS parameter

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Table 7: Association between score of AIMS–SDQ question number 8 and VFSS parameter

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Table 8: Association between score of AIMS–SDQ question number 10 and VFSS parameter

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Overall comparison of SDQ with DSRS scores revealed that all 12 patients had an AIMS–SDQ score of ≥2 and a DSRS score of ≥1 on objective VFSS imaging ([Graph 1]). However, no correlation was observed between the two scores.
Graph 1: Comparison of overall AIMS–SDQ scores (X axis) with Dysphagia Severity Rating Scale (DSRS) (Y axis). Abbreviations: AIMS, Amrita Institute of Medical Sciences; SDQ, swallowing disturbance questionnaire

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  Discussion Top


Dysphagia, caused by neurological injuries and neuromuscular diseases, is usually the end result of the impairment of sensorimotor components involved in the oral and pharyngeal phases of swallowing. The onset, progression, and severity of the disease, as well as the neuromuscular symptoms, may occur suddenly or progress gradually.

In PD patients, early identification of swallowing problems is crucial, as it can lead to the development of aspiration pneumonia, which can be potentially life threatening if left untreated. However, the severity and duration of PD are not predictors of dysphagia.[9] Most PD patients develop dysphagia in the later stage of the disease, despite early pathological changes in brainstem structures. The prevalence of oropharyngeal dysphagia in PD varies from 18.5% to 100% across studies. A cohort study revealed that dysphagia was reported approximately 10–11 years after the appearance of motor symptoms, and the prevalence was at 68%, even in the on-drug phase of patients with advanced-stage PD.[10]

VFSS or FEES are essential procedures to identify swallowing problems in the pharyngeal stage. In particular, VFSS provides temporal parameters related to both oral and pharyngeal dysphagia, including the etiology of aspiration. Studies using VFSS have revealed that dysphagia begins with reduced tongue retraction and a repetitive rocking-rolling movement of the tongue. In addition, food residues in the valleculae and piriform sinuses from piecemeal deglutition were markedly associated with penetration/aspiration in PD patients.[10] Due to lingual incoordination and pumping during the oral phase, there is reduced oral bolus content with reduced oropharyngeal bolus transport following festination of the tongue onto the soft palate. In contrast, during the pharyngeal phase, there is reduced velopharyngeal closure, reduced pharyngeal contraction, and backward movement of the tongue, leading to residue collection in the pharynx.

In the present study, we attempted to correlate the AIMS–SDQ scores with objective VFSS findings for of six out of the 11 questions. We found that for all six questions, even at very low scores, corresponding objective abnormalities were observed in the VFSS parameters. This confirms that the questionnaire is sensitive to VFSS abnormalities even at low scores. However, no statistical significance was established between the AIMS–SDQ scores and VFSS parameters, which could be due to the small sample size. An inconsistency in the severity of the subjective complaints of patients and the objective findings of swallowing assessments is not an unusual observation; in most cases the former category appears less severe.[9] This discrepancy was observed in our study as well. Even when patients scored low on a particular AIMS–SDQ question, significant abnormality was observed in the corresponding VFSS finding. Therefore, AIMS–SDQ in our study sensitively detected changes in VFSS. In contrast, a corresponding VFSS finding was not always noted when patients gave positive answers to questions. This could be due to a bias on the part of the patient when responding to such subjective questionnaires. Moreover, some patients tended to over or under respond.

Some VFSS studies showed that a substantial number of patients may have experienced silent aspiration even when they had no related complaints.[1] In our study, we found that even when patients had a short duration of the disease and mild disability (Hoehn and Yahr stages 1 and 2), the VFSS findings were abnormal. This shows that dysphagia is clinically under reported in patients, despite detailed history taking and neurological evaluation; even patients in early stages of the disease can experience swallowing disturbances that can be observed on VFSS.

The oropharyngeal phase of swallowing is the most affected process in PD patients. Several studies have investigated abnormalities in the oropharyngeal phase of swallowing in PD patients.[11] In addition, several authors have concluded that rigidity, hypokinesia, and bradykinesia, which are the cardinal manifestations of PD, lead to swallowing disruption in the oral and pharyngeal stages.[1] Our study demonstrated this conclusion using the AIMS–SDQ tool.[5] Therefore, in our study, we examined six VFSS parameters that would best represent abnormalities in the oropharyngeal phase. These were bolus stuck in the mouth, oral residue, BRS, multiple swallows, PAS, and DSRS. There were significant abnormalities in all the parameters examined, signifying that objective VFSS abnormalities are common in PD patients, even with low questionnaire response scores. This is an indication that PD patients evidently under report swallowing issues in the clinic because they may focus more on reporting motor symptoms like tremors, rigidity, bradykinesia, and postural disabilities. Monteiro et al. studied 35 PD patients and observed that 22% of dysphagia patients with laryngeal penetration had no swallowing complaints.[12]

In addition, silent dysphagia symptoms (silent laryngeal penetration/aspiration without any sensibility and reaction to clear the throat/airways by hawking or coughing) are observed in PD patients, even in early stages. Patients may not recognize symptoms at the beginning because of the lack of oral/pharyngeal/laryngeal tactile/kinesthetic sensibility or lack of awareness of changes in voice quality after swallowing; this indicates bolus penetration at the level of the vocal folds as well as the fact that the presenting symptoms may fluctuate in the early stages of dysphagia (partially associated with good responsiveness of levodopa-equivalent therapy in the initial phase).[13]

The other possible reason for under reporting is the lack of an adequate tool to detect symptoms during outpatient examinations. Developing questionnaires that are sensitive to detect the symptoms not yet presented in the patient’s history but are simple to answer and easy to conduct are vital. Some examples of short questionnaires used to screen for dysphagia are the 17-item Sydney Swallow Questionnaire, 15-item Tel-Aviv swallow disturbance questionnaire, and 15-item Ohkuma Dysphagia Screening. However, except for the Tel-Aviv questionnaire, the others have not been validated for PD patients, like how we have done using the questionnaire in our study, nor are they available in the vernacular. Moreover, we wanted to include only a minimum number of questions that could represent all likely aspects of oropharyngeal dysphagia. Hence, we developed our 11-item tool and validated it in the vernacular. Our questionnaire could elicit abnormal findings in VFSS at low scores but without a statistical association between the questionnaire scores and VFSS parameter scores. This discrepancy could be due to several reasons such as the long duration of the disease and its varied speed of progression in individual patients. In addition, it could be due to the multiple neurological axes involved in the complex process of swallowing.

The VFSS examination of IPD patients revealed that objective findings such as poor bolus propulsion, oral residue, vallecular and hypopharyngeal residue, multiple swallows, and laryngeal penetration were noted to correspond with their positive responses to related questions in our AIMS–SDQ tool.

To the best of our knowledge, ours is the first study to demonstrate a correlation between the scores of most questions in AIMS–SDQ and the VFSS parameter scores, to a varying extent. However, we could not obtain a statistically significant correlation, which may be due to the small sample size. Overall, AIMS–SDQ is a sensitive tool to predict objective changes in VFSS, which is a strong indicator of the dysphagia spectrum in IPD patients.

Despite the promising nature of our findings, our study has some limitations. Our study included one patient <50 years of age and few patients with a Hoehn and Yahr score of 3. Similarly, we did not consider the age of >75 years as a factor for dysphagia. Therefore, future studies should include a larger cohort of IPD patients and multiple institutions.

Declaration of patient consent

The authors declare that they have obtained all appropriate signed patient consent forms. The patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity but anonymity cannot be guaranteed.

Acknowledgments

The authors thank Dr. Subramania Iyer, Professor and Head, Centre for Head and Neck Surgery and Oncology, Amrita Institute of Medical Sciences and Research Centre, for his support and guidance.

Author contributions

Ms. Ravichandran Sumathi Aarthi: Data acquisition and analysis, statistical analysis, literature search; Dr. Suresh Kumar R.: Concept, design, manuscript editing and review; Dr. Sivakumar Vidhyadharan: Design, manuscript editing and review; Dr. Unnikrishnan K. Menon: Manuscript preparation, editing and review; Ms. Chandrababu Jaya Arya: Literature search, data acquisition; Dr. Krishnakumar Thankappan: Concept, data acquisition.

Ethical compliance statement

The study was cleared by the Institutional Review Board: IRB-AIMS-2020-051.

Conflicts of interest

There are no conflicts of interest to declare.

Financial support and sponsorship

None.



 
  References Top

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Baijens LW, Speyer R, Passos VL, Pilz W, Roodenburg N, Clave P. Swallowing in Parkinson patients versus healthy controls: Reliability of measurements in videofluoroscopy. Gastroenterol Res Pract 2011. doi: 10.1155/2011/380682.  Back to cited text no. 1
    
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Mohamed AAB, Mohamed GF, Elnady HM, Sayed MA, Imam AM, Hassan MM, et al. Evaluation of dysphagia in different phenotypes of early and idiopathic Parkinsonism. Egypt J Neurol Psychiatr Neurosurg 2018;54:28.  Back to cited text no. 2
    
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Bird MR, Woodward MC, Gibsin EM, Phyland DJ, Fonda D. Asymptomatic swallowing disorders in elderly patients with Parkinsons disease: A description of findings on clinical examination and videofluroscopy in sixteen patients. Age Ageing 1994;23:251-4.  Back to cited text no. 3
    
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Menon U, Radhakrishnan SR, Sundaram KR. Reliability and validity of a questionnaire to assess swallowing disorders in Parkinsons disease Cases. Int J Phonosurg Laryngol 2016;1:35-9.  Back to cited text no. 4
    
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Radhakrishnan S, Menon UK, Sundaram KR. Usefulness of a modified questionnaire as a screening tool for swallowing disorders in Parkinson’s disease: A pilot study. Neurol India 2019;67:118-22.  Back to cited text no. 5
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Gramigna GD. How to perform video-fluoroscopic swallowing studies. GI Motility Online 2006. doi: 10.1038/gimo95.  Back to cited text no. 6
    
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Rommel N, Borgers C, Van Beckevoort D, Goeleven A, Dejaeger E, Omari TI. Bolus residue scale: An easy-to-use and reliable videofluoroscopic analysis tool to score bolus residue in patients with dysphagia. Int J Otolaryngol 2015;2015:780197.  Back to cited text no. 7
    
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Borders JC, Brates D. Use of the penetration-aspiration scale in dysphagia research: A systematic review. Dysphagia 2020;35:583-97.  Back to cited text no. 8
    
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Nobrega AC, Rodrigues B, Torres AC, Scarpel R, Neves CA, Melo A. Is drooling secondary to swallowing disorder in Parkinson’s disease patients. Parkinsonism Relat Disord 2008;14:243-5.  Back to cited text no. 9
    
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Kwon M, Lee JH. Oro-pharyngeal dysphagia in Parkinson’s disease and related movement disorders. J Mov Disord 2019;12:152-60.  Back to cited text no. 10
    
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Ali GN, Wallace L, Schwartz R, Dcarle DJ, Zagami AS, Cook IJ. Mechanisms of oro-pharyngeal dysphagia in patients with Parkinson’s disease. Gastroenterology 1996;110:383-92.  Back to cited text no. 11
    
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Monteiro L, Souza-Machado A, Pinho P, Sampaio M, Nóbrega AC, et al. Swallowing impairment and pulmonary dysfunction in Parkinson’s disease: The silent threats. J Neurol Sci 2014:339:149-52.  Back to cited text no. 12
    
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Simons JA. Swallowing dysfunctions in Parkinson’s disease. Int Rev Neurobiol 2017;134:1207-38.  Back to cited text no. 13
    


    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

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