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ORIGINAL ARTICLE
Year : 2019  |  Volume : 67  |  Issue : 1  |  Page : 118-122

Usefulness of a modified questionnaire as a screening tool for swallowing disorders in Parkinson disease: A pilot study


1 Department of Neurology, Amrita Institute of Medical Sciences and Research Centre, Amrita Vishwa Vidyapeetham and Amrita University, Kochi, Kerala, India
2 Department of ENT, Amrita Institute of Medical Sciences and Research Centre, Amrita Vishwa Vidyapeetham and Amrita University, Kochi, Kerala, India
3 Department of Biostatistics, Amrita Institute of Medical Sciences and Research Centre, Amrita Vishwa Vidyapeetham and Amrita University, Kochi, Kerala, India

Date of Web Publication7-Mar-2019

Correspondence Address:
Dr. Sureshkumar Radhakrishnan
Department of Neurology, Amrita Institute of Medical Sciences and Research Centre, Amrita Vishwa Vidyapeetham and Amrita University, Kochi - 682 041, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.253586

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 » Abstract 


Aims: To determine the correlation between our questionnaire scores and two standard Parkinson's disease (PD) disability scores [Unified Parkinsons' Disease Rating Scale (UPDRS) and Hoehn and Yahr (H and Y)], and to study the correlation between the various subgroups of our dysphagia screening questionnaire.
Settings and Design: This study was conducted at a movement disorder clinic in a tertiary care hospital in Kochi, Kerala. This was a cross-sectional observational study.
Materials and Methods: A questionnaire was developed comprising 11 items, keeping in mind the most relevant swallowing issues in PD patients. The questions were subdivided into four groups representing the different stages of swallowing. Reliability and validity studies were conducted for the questionnaire. Corresponding UPDRS and H and Y scores were documented on the same day.
Statistical Analysis Used: Mean and standard deviation (SD) values of the scores in each group and the correlation between scores (Pearson correlation coefficient) were done.
Results: Responses were obtained from 106 PD patients (67 males, 39 females), with a mean age of 66.9 years (SD, 8.62). Our questionnaire score showed a high coefficient of variation (145%) compared to the UPDRS and H and Y scores. There was also moderate correlation between our questionnaire score and the two standard scores with a significant P value. Finally, the highest mean scores were for questions from group A and the least for questions from group D.
Conclusions: The association between worsening motor symptoms and swallowing difficulties has been documented in this study. The oral stage of swallowing remains the most affected in PD, which can be recognized early using our questionnaire.


Keywords: Deglutition disorders, Parkinson's disease, questionnaire, statistical analysis
Key Message: Our study attempts to create a simplified 11-point questionnaire to screen dysphagia in Parkinson's disease. This questionnaire has been validated.


How to cite this article:
Radhakrishnan S, Menon UK, Sundaram K R. Usefulness of a modified questionnaire as a screening tool for swallowing disorders in Parkinson disease: A pilot study. Neurol India 2019;67:118-22

How to cite this URL:
Radhakrishnan S, Menon UK, Sundaram K R. Usefulness of a modified questionnaire as a screening tool for swallowing disorders in Parkinson disease: A pilot study. Neurol India [serial online] 2019 [cited 2019 May 23];67:118-22. Available from: http://www.neurologyindia.com/text.asp?2019/67/1/118/253586




Parkinson's disease (PD) is recognized as the second most common neurodegenerative disorder after Alzheimer's disease. Worldwide, it affects 1% of the population over the age of 65 years.[1] The disease has varied motor as well as nonmotor symptoms. Most physicians give more significance to motor symptoms. Hence, nonmotor symptoms are under-reported [2] and are recognized late.

Swallowing disability in patients with PD is one such symptom. Studies have shown that dysphagia can be an early problem in PD.[3] It becomes more prominent as the disease progresses in severity. Dysphagia can lead to a poor food intake, microaspirations, and malnutrition.[4]

There are predominantly three phases in physiological swallowing – oral, pharyngeal, and esophageal. Of these, oral and oropharyngeal are the most affected in PD.[5],[6] There is a need to detect this problem early, even if it is not primarily reported by the patient. Dysphagia followed by subsequent aspiration is a leading cause of death in most patients with PD in its advanced stage. At present, there is a need for a simple questionnaire which can be used in an outpatient setting so that the clinician can detect dysphagia early in these patients. A validated questionnaire is the most suitable tool. The available questionnaires to detect dysphagia are either too detailed and time consuming or too brief to capture the problem.

Hence, our attempt in this study has been to create a suitable questionnaire which can detect early swallowing problems in PD patients. Brevity and ease of administration in outpatient settings without compromising on screening value were the qualities we wanted to achieve. The present study looks at the utility of this new tool in terms of its correlation with the disability scores from standard tools.

Aims of the study

  1. To see if there is a correlation between our questionnaire scores and the two standard PD disability scores (UPDRS and Hoehn and Yahr)
  2. To study the correlation between the various subgroups of our dysphagia screening questionnaire.



 » Materials and Methods Top


This study was conducted in a tertiary medical care centre providing healthcare services to a population of approximately 30 million in the state of Kerala in south India.

The study was planned by a neurologist dealing with movement disorders, along with an otolaryngologist interested in swallowing disorders.

Questionnaire development

Based on a detailed study of various available standard questionnaires, we developed an 11-question form. Our focus was on brevity. Only those questions which pertained to the swallowing disorders likely to present in PD were included, with the exclusion of associated symptoms and quality of life-related questions. The form was then translated into Malayalam, the vernacular of the patients of the study area.

The eleven questions were subdivided into four groups A, B, C, and D. Group A had four questions predominantly related to the oral phase of swallowing, B had four that involved the pharyngeal phase, C had two questions related to aspiration, and D had one question related to the upper esophageal phase. These groups were not shown on the form itself but were marked on our data analysis chart.

To check the reliability, the same questionnaire was administered to age-matched controls, consisting of patients visiting the neurology, ENT, and geriatric outpatient departments (OPDs). We ensured that none of these patients had swallowing difficulty as a presenting symptom. For validity, it would have been ideal to administer another standard questionnaire. However, logistical and patient compliance issues precluded this. As a prerequisite for this study, statistical validation of our questionnaire was also done and we published these results recently.[7]

All the questions were in the form of simple, concise statements. There was no necessity for a medical translator. The vernacular questionnaire was first administered as a trial to a few patients attending the neurology OPD. The responses were satisfactory. Hence, we proceeded to administer it to the study population.

Study method

Inclusion criteria

Patients with a confirmed diagnosis of PD, based on the UK Brain Bank criteria, and under regular review in the Movement Disorders Clinic were included in the study.

Exclusion criteria

All  Parkinsonism More Details syndromes other than idiopathic PD; patients who had Hoehn and Yahr disability scoring score greater than 3; patients who were unable to read, were excluded from the study.

All patients underwent UPDRS and Hoehn and Yahr Disability Scoring during the study initiation visit.

The questionnaire was administered by an assigned staff in the movement disorder clinic, with instructions to the patient and the accompanying caregiver about the method (ticking one of the three options for each question). The patients were encouraged to complete the given questionnaire themselves. In case of inability to fill the form due to lack of fine motor control, the caregiver was allowed to do the physical act of ticking after the patient had read the question and conveyed the answer.

The questionnaire consisted of 11 questions, as explained above, with each question having three responses with individual score given in the bracket – never (0), sometimes, (1) and always (2). The patient had to tick the most appropriate response from the three options. The questionnaire was administered as a one-time process, so that an individual patient responded only once during the PD clinic visits. The study was conducted over a period of 15 months. The responses were tabulated and statistical analysis applied.

Statistical analysis

  1. Mean and standard deviation (SD) values of the scores in each group were computed
  2. Correlation between scores from the three methods (H and Y, UPDRS, questionnaire) was assessed by computing Pearson's correlation coefficient
  3. Correlation of scores between scores of various groups in our questionnaire was assessed by computing Pearson's correlation coefficient
  4. The amount of variation (standardized) in each method of scoring was assessed by computing the coefficient of variation
  5. Statistical significance of the differences in average scores among various groups was tested by applying analysis of variance. In case of significant differences among the groups, Bonferroni's multiple comparison test was done to identify statistically significant pairs of groups.



 » Results Top


Responses were obtained from 106 PD patients (67 males, 39 females), with a mean age of 66.9 years (standard deviation [SD] = 8.62). The scoring pattern for the questionnaire implied that there could be a minimum score of zero, indicating no subjective swallowing difficulty whatsoever, to a maximum of 22.

Coefficient of variation among the known disability scales and our questionnaire

We initially looked at the coefficient of variation among the UPDRS and H and Y scales and our validated questionnaire. Mean and SD of scores obtained by the three methods showed the coefficient of variation to be very high (145.3%) in the questionnaire score. Lowest percentage of variation was observed for the H and Y score (36.8%) [Table 1].
Table 1: Mean and SD of different types of scores

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Correlation between our questionnaire and the existing disability scores

The main research question was to look for correlation between our questionnaire scores and the two neurological evaluation scores. The coefficient values among the different scoring systems showed the highest correlation to be between H and Y score and UPDRS score (0.734). Correlation coefficient values (r) of the questionnaire score with the H and Y and UPDRS scores were more or less the same (0.339 and 0.384, respectively). These represent moderate correlation with significant P values [Table 2].
Table 2: Correlation among different types of scores

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Comparison between the four subgroups (A, B, C, and D) within our questionnaire

The next statistical parameter that we looked at was the comparison between the four groups within our questionnaire. This was to check both the correlation between the groups and the scoring pattern and significance of each group. [Table 3] presents the mean and SD of scores for the different groups of questions. It also gives the results (P value) of the comparison of mean scores among the different groups of questions, as well as the corresponding correlation coefficient values (r) among the different groups of questions. The results showed that the highest mean score was for the questions in group A and the lowest for those in group D. The differences in mean scores between all pairs of groups, except for the comparison between groups B and C and B and D were statistically significant. Correlation coefficient values between the mean scores of various groups ranged from 0.56 to 0.73, indicating a comparatively high degree of correlation among the different groups of questions.
Table 3: Comparison of mean score among the four groups of questions

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 » Discussion Top


Dysphagia is a common nonmotor symptom in PD, affecting almost 80% of the patients.[8] However, patients may be unaware of their swallowing difficulties, at least in the early stages of the disease.[9] Kalf et al., in a systematic meta-analysis review observed that, though subjective dysphagia occurred in one-third of community dwelling PD patients, the incidence of objectively measured dysphagia was much higher, with 4 out 5 patients being affected.[10] The reason for this under recognition is their preoccupation with overt motor symptoms such as tremor, bradykinesia, balance, and immobility. Affected patients rarely complain of dysphagia unless they are specifically asked about it in a clinical interview. Hence, this often becomes an under-recognized symptom and is mostly managed late in the course of the disease. Second, being a nondopaminergic symptom, there is only a modest response to available medical treatment. Hence, early identification and management of dysphagia becomes a challenging task for the treating neurophysician to prevent aspiration, and subsequently, an early mortality.

In our movement disorders clinic, we regularly administer the well-accepted and popular UPDRS to all our patients. In this scoring system, there is only one question dedicated to swallowing.[11] This is not sensitive enough to identify early or mild swallowing problems. However, it is also difficult to do a detailed study on all patients in an outpatient clinic as it would be time consuming. Hence, a brief questionnaire, that would capture all the phases of swallowing, that is simple to use, and that can be easily attempted by the patient alone or with the help of a caregiver, would be ideal.

The swallowing problems in PD are usually related to the oral and pharyngeal phases. Fuh et al., while studying swallowing disabilities in PD patients with modified barium swallow concluded that vallecular sinus and pyriform sinus residues were the most common abnormalities.[12] Similarly Brega et al., observed that drooling, a common symptom seen in PD, is associated with oropharyngeal dysphagia. In their study, they noted changes in the oral phase of swallowing among all their patients, and in the pharyngeal phase in 94% patients. Drooling also increases with the severity of dysphagia.[13] Hence, in our questionnaire more questions were included to capture these two phases of dysphagia with four questions dedicated to each group (A and B).

The cross-sectional nature of our study meant that our questionnaire was administered to PD patients in varying stages of disease progression. This would explain the high coefficient of variation in the questionnaire scores noted in the statistical analysis.

Correlation between the three scores revealed that the questionnaire scores in our study correlated moderately with the disability (UPDRS and H and Y) scores. This shows that subjective dysphagia in PD increases with functional disability. Our questionnaire could reliably demonstrate this. A study by Clarke et al., revealed that the swallowing speed and bolus volume are significantly lower in patients with PD compared to age-matched controls, and this worsens with increased disease severity as measured by the H and Y score.[14] However, the flip side is that we got only a moderate correlation. This can be accounted for by the well-established fact of PD patients downplaying or under-reporting their swallowing symptoms.

However, as expected, there was a very good correlation between the two established parameters, H and Y and UPDRS. This is understandable as both are measures of motor disabilities in PD.[15],[16]

Another aspect of our study was the comparison between the four groups of questions within our questionnaire. This showed the highest mean score for questions in Group A and the lowest for Group D. The former consisted of issues related to difficulties in the oral stage of swallowing, and the latter the esophageal stage. It is well-known that in PD, the oral stage is affected the most. Our subgroup score documented this. It is worth considering a questionnaire expanded only from this subgroup to be administered to PD patients to see whether a greater correlation can be established. The other statistical finding was the high degree of correlation among the different groups of questions.

Thus, our questionnaire is a reliable screening tool for patients with swallowing problems in PD. As it was validated in Malayalam, a majority of our patients found it easy to understand it and respond to it. The time taken for its completion was in the range of about 5–10 minutes. A few patients with severe tremors involving the hands needed help from their caregivers in completing the questionnaire. The Tel Aviv 15-item questionnaire similarly attempts at capturing early swallowing difficulties in PD patients. However, in India, patients are less educated and need a simple questionnaire which is easier to respond to. Hence, our questionnaire contains fewer questions (11 items) and each question has fewer responses. It was also validated in the local vernacular language for better understanding. We also compared our questionnaire with the two existing and well-accepted standard disability scales, the UPDRS and the H and Y score.


 » Conclusions Top


The association between worsening motor symptoms and swallowing difficulties has been documented in this study. The oral stage of swallowing remains the most affected in PD, and this can be recognized early by using our questionnaire. The brief questionnaire developed by us can be used as a screening tool for early detection of dysphagia in patients with PD in a busy outpatient clinic. We propose this simple 11-item questionnaire as a convenient, yet useful, tool for use in the routine neurology or PD clinic. It can function as an interface between the detailed the H and Y scoring systems.

Future plans

  1. To continue this study to look for a cut-off value in the questionnaire score, which would indicate the need for further investigations for dysphagia such as fiberoptic endoscopic evaluation of swallowing (EFES) and videofluoroscopic evaluation of swallowing (VFES).
  2. To carry out modifications in the questionnaire to make it applicable for other neurological conditions with swallowing disorders


Recommendations

This questionnaire can be utilized by neurologists and institutions. Further studies regarding the utility of this tool are needed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

1.
Tanner CM, Goldman SM. Epidemiology of Parkinson's disease. Neurol Clin 1996;14:317-35.  Back to cited text no. 1
    
2.
Chaudhuri KR, Schapira AH. Non-motor symptoms of Parkinson's disease: Dopaminergic pathophysiology and treatment. Lancet Neurol 2009;8:464-74.  Back to cited text no. 2
    
3.
Nilsson H, Ekberg O, Olsson R, Hindfelt B. Quantitative assessment of oral and pharyngeal function in Parkinson's disease. Dysphagia 1996;11:144-50.  Back to cited text no. 3
    
4.
Tjaden K. Speech and swallowing in Parkinson's disease. Top Geriatr Rehabil 2008;24:115-26.  Back to cited text no. 4
    
5.
Dawes C, Kubieniec K. The effects of prolonged gum chewing on salivary flow rate and composition. Arch Oral Biol 2004;49:665-9.  Back to cited text no. 5
    
6.
Felix VN, Corrêa SM, Soares RJ. A therapeutic maneuver for oropharyngeal dysphagia in patients with Parkinson's disease. Clinics (Sao Paulo) 2008;63:661-6.  Back to cited text no. 6
    
7.
Menon U, Radhakrishnan SR, Sundaram KR. Reliability and validity of a questionnaire to assess swallowing disorders in Parkinson's disease Cases. Int J Phonosurg Laryngol 2016;1:35-9.  Back to cited text no. 7
    
8.
Potulska A, Friedman A, Królicki L, Spychala A. Swallowing disorders in Parkinson's disease. Parkinsonism Relat Disord 2003;9:349-53.  Back to cited text no. 8
    
9.
Robbins JA, Logemann JA, Kirshner HS. Swallowing and speech production in Parkinson's disease. Ann Neurol 1986;19:283-7.  Back to cited text no. 9
    
10.
Kaif JG, de Swart BJ, Bloem BR, Munneke M. Prevalance of oropharyngeal dysphagia in Parkinsons Disease: A meta-analysis review. Parkinsonism Relat Disord 2011;18:311-5.  Back to cited text no. 10
    
11.
Movement Disorder Society Task Force on Rating Scales for Parkinson's disease. The Unified Parkinson's Disease Rating Scale (UPDRS): Status and recommendations. Mov Disord 2003;18:738-50.  Back to cited text no. 11
    
12.
Fuh JL, Lee RC, Wang SJ, Lin CH, Wang PN, Chiang JH, et al. Swallowing difficulties in Parkinsons disease. Clin Neurol Neurosurg 1997;99:106-12.  Back to cited text no. 12
    
13.
Nobrega AC, Rodrigues B, Torres AC, Scarpel RD, Neves CA, Melo A. Is drooling secondary to a swallowing disorder in patients with Parkinsons disease? Parkinsonism Relat Disord 2008;14:243-5.  Back to cited text no. 13
    
14.
Clarke CE, Gullaksen E, Macdonald S, Lowe F. Referral criteria for speech and language therapy assessment of dysphagia caused by idiopathic Parkinson's disease. Acta Neurol Scand 1998;97:27-35.  Back to cited text no. 14
    
15.
Yorkston KM, Miller RM, Strand EA. Management of speech and swallowing disorders in degenerative diseases. Pro ed; 2004.  Back to cited text no. 15
    
16.
Manor Y, Giladi N, Cohen N, Fliss DM, Cohen JT. Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinsons disease. Mov Disord 2007;22:1917-21.  Back to cited text no. 16
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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