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Swallowing Disorders in Parkinson's Disease
Acta Otorrinolaringol Esp. 2017;68(1):15---22
www.elsevier.es/otorrino
ORIGINAL ARTICLE
Swallowing Disorders in Parkinson’s Disease夽 Sandra Mamolar Andrés,a María Liliana Santamarina Rabanal,a,b,c Carla María Granda Membiela,a María José Fernández Gutiérrez,a,c Paloma Sirgo Rodríguez,a,c César Álvarez Marcosa,b,d,∗ a
Universidad de Oviedo, Oviedo, Asturias, Spain Unidad de Disfagia, Servicio de Rehabilitación, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain c Unidad de Foniatría y Logopedia, Servicio de Rehabilitación, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain d Servicio de Otorrinolaringología, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain b
Received 30 January 2016; accepted 10 February 2016
KEYWORDS Dysphagia; Parkinson’s disease; Volume-viscosity examination; Pneumonia aspiration; Fibreoptic endoscopic swallowing
Abstract Introduction: Parkinson’s disease is a type of chronic neurodegenerative pathology with a typical movement pattern, as well as different, less studied symptoms such as dysphagia. Disease-related disorders in efficacy or safety in the process of swallowing usually lead to malnutrition, dehydration or pneumonias. The aim of this study was identifying and analyzing swallowing disorders in Parkinson’s disease. Subjects and methods: The initial sample consisted of 52 subjects with Parkinson’s disease to whom the specific test for dysphagia SDQ was applied. Nineteen participants (36.5%) with some degree of dysphagia in the SDQ test were selected to be evaluated by volume-viscosity clinical exploration method and fibreoptic endoscopic evaluation of swallowing. Results: Disorders in swallowing efficiency and safety were detected in 94.7% of the selected sample. With regards to efficiency, disorders were found in food transport (89.5%), insufficient labial closing (68.4%) and oral residues (47.4%), relating to duration of ingestion. Alterations in security were also observed: pharynx residues (52.7%), coughing (47.4%), penetration (31.64%), aspiration and decrease of SaO2 (5.3%), relating to the diagnosis of respiratory pathology in the previous year.
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Please cite this article as: Mamolar Andrés S, Santamarina Rabanal ML, Granda Membiela CM, Fernández Gutiérrez MJ, Sirgo Rodríguez P, Álvarez Marcos C. Trastornos de la deglución en la enfermedad de Parkinson. Acta Otorrinolaringol Esp. 2017;68:15---22. ∗ Corresponding author. E-mail address: [email protected] (C. Álvarez Marcos). 2173-5735/© 2016 Elsevier Espa˜ na, S.L.U. and Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. All rights reserved.
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S. Mamolar Andrés et al. Conclusion: The SDQ test detected swallowing disorders in 36.5% of the subjects with Parkinson’s disease. Disorders in swallowing efficiency and safety were demonstrated in 94.7% of this subset. Disorders of efficiency were more frequent than those of safety, establishing a relationship with greater time in ingestion and the appearance of respiratory pathology and pneumonias. © 2016 Elsevier Espa˜ na, S.L.U. and Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. All rights reserved.
PALABRAS CLAVE Disfagia; Enfermedad de Parkinson; Método volumen-viscosidad; Neumonía aspirativa; Videoendoscopia deglución
Trastornos de la deglución en la enfermedad de Parkinson Resumen Introducción: La enfermedad de Parkinson es una patología neurodegenerativa crónica, con síntomas motores característicos y otros menos estudiados como la disfagia. Suele relacionarse con desnutrición, deshidratación o neumonías por aspiración por trastornos en la eficacia y seguridad en la deglución. El objetivo de este trabajo es identificar y analizar los trastornos deglutorios en la enfermedad de Parkinson. Sujetos y métodos: Muestra inicial de 52 sujetos con enfermedad de Parkinson a los que se aplicó el test SDQ, específico para la disfagia. Se seleccionaron 19 (36,5%) participantes con algún grado de disfagia en dicho test para ser evaluados con el método de exploración clínica volumen-viscosidad y la videoendoscopia de la deglución. Resultados: Se detectaron trastornos de eficacia y seguridad de la deglución en el 94,7%, siendo las alteraciones de la eficacia: dificultad en el transporte de alimento (89,5%), deglución fraccionada (78,9%), mal sello labial (68,4%) y residuos orales (47,4%), relacionándose con el tiempo que dura la ingesta. Se observaron también alteraciones en la seguridad como residuos faríngeos (52,7%), tos (47,4%), penetración (31,64%), aspiración y descenso de SaO2 (5,3%), relacionándose con el diagnóstico de patología respiratoria en el último a˜ no. Conclusiones: El test SDQ detectó trastornos deglutorios en el 36,5% de los pacientes con enfermedad de Parkinson. Las alteraciones en la eficacia y seguridad de la deglución se demostraron en el 94,7% de ellos, siendo más frecuentes los trastornos de eficacia que los de seguridad, estableciendo relación con el mayor tiempo en la ingesta y la aparición de patología respiratoria y neumonías. © 2016 Elsevier Espa˜ na, S.L.U. y Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. Todos los derechos reservados.
Introduction Parkinson’s disease (PD) is a chronic neurodegenerative pathology leading to progressive debilitation. It has been estimated that in Spain there are approximately 70 000 people suffering from the disease, with an incidence of 16/100 000 inhabitants/per year and a prevalence of 1000/100 000 inhabitants, but it is probable that these data have been underestimated.1,2 The aetiology of PD is unknown although it is believed that a number of genetic and environmental factors are involved. The anatomical substrate is the progressive disappearance of dopamine neurones of the locus niger, the midbrain basal ganglia.3 Dopamine controls voluntary movement and postural balance, and its deficiency causes the gradual, inexorable development of the disease.2 The beginning is insidious, with standard motor symptoms: tremor, bradykinesia and rigidity, together with other emotional, cognitive, sensitive, communicative symptoms and changes
in postural reflexes, which determine the Parkinson profile.4 Although PD is chronic and progressive there are replacement, electrophysiological and rehabilitation treatments which impede its evolution.5,6 In Dysphagia Units swallowing disorders (SD) caused by neurodegenerative diseases are increasingly better controlled and the professionals involved are used to dealing with these patients. PD leads to SD in up to 90% of patients in advanced stages of the disease.7,8 However, the number of patients with PD who consult their doctor or speech therapist about dysphagia is limited and does not meet with expectations. SD from PD have been described in all stages of swallowing and are manifold: limitations in transporting food to the mouth, difficulty in chewing, hypersalivation, inability to form a cohesive bolus, reduction in swallowing reflex, delayed and incomplete laryngeal closure, reduced pharyngeal and oesophageal peristalsis, and gastroesophageal reflux.7,9---12 Dysphagia may occur in any evolutive stage but
Swallowing Disorders in Parkinson’s Disease worsens as the disease advances and in the off periods. The most serious complications are aspiration and pneumonia, difficulty in oral drug administration, malnutrition and dehydration. There is a high incidence of silent aspiration with pneumonia being the principal cause of death.13 Treatment with L-DOPA and adaptive feeding methods improve the effectiveness and safety of swallowing and increase the speed of transit.5,6 Occasionally a nasogastric tube or percutaneous endoscopic gastrostomy tube may be used, especially if aspiration and pneumonia present.8,14 SD in PD have an effect on the patient’s quality of life. In advanced stages the desire to eat decreases and the difficulty in selecting food and the duration of meals increases, with repercussions on their nutritional status.15 The aim of this article is to apply a clinical protocol for early detection of SD in PD patients and to assess their frequency, type and severity.
Subjects and Methods There were 52 participants in the study (26 men and 26 women) with a mean age of 72.4 (age range 34---88 years), who were members of the ‘‘Asturias Parkinson Association (APA) in Oviedo. In this preliminary sample the ‘‘Swallowing Disturbance Questionnaire’’ (SDQ)16 was applied in order to select those who presented with significant SD, and when the final sample was obtained all subsequent procedures were performed. All participants of the final sample had been diagnosed in the Neurology Department of the Hospital Universitario Central de Asturias and regularly attended the APA for two weekly speech therapy sessions. The patients attended the day centre from early morning, completing the SDQ after having taken their recommended medication. None of the participants had previously been evaluated and diagnosed with SC by means of any specific tests. During phase one, from 10th to 14th November 2014, recruitment and selection of the participants was carried out in the APA central office. This phase was approved by the APA management board. The speech therapists of the association personally administered the SDQ, with confidentiality being guaranteed, and the patients’ acceptance of inclusion in the study was key. The 52 participants represented the majority of associates who regularly attended the centre during this period. They had not been diagnosed with any degree of dementia and were capable of reading and understanding the SDQ contents, in addition to participating in the instrumental tests. The SDQ is an easily applied questionnaire, designed to specifically detect SD in PD.16 It assesses the response to a general, subjective question (‘‘do you think you have problems with eating and drinking?’’) to which a yes/no response is requested. Thereafter there are 15 items on dysphagia. In 14 of the questions the response is made on a Likert scale of 0 (never) to 3 (very frequently), 5 of them relating to the oral stage of swallowing and 9 to the pharyngeal. The last of the items (‘‘have you suffered from a respiratory pneumonia or bronchitis type infection in the last year?) is answered with yes/no and assessed with 2.5 points if it is Yes and 0.5 points if it is No. The SDQ was originally designed and validated in English and has not been adapted or validated in Spanish.
17 However, as there is no similar test in our language and given its renowned usefulness, a literal translation was made of it since neither vocal nor phonetic elements of quality were assessed (Appendix). The SDQ selection of participants for the final sample was made with cut-off values ≥11 in the 15 items or if the response to the subjective question was ‘‘yes’’ (16). The second stage of the study consisted in applying the dysphagia clinical assessment protocol to the selected participants. This phase was performed in the Otorhinolaryngology Department of Hospital Universitario Central de Asturias between December 2014 and March 2015, under medical supervision, with patients attending a single session first thing in the morning after taking their mediation. The protocol comprised: 1. Data collection (parentage, background, stage, evolution of PD, dysphagia symptoms, etc.) offered by the patient/family member/carer and computerised medical record. 2. Explanation and signing of informed consent for the tests. The study was approved by the Medical Board and the Ethics Committee, which authorised its completion in the relevant hospitals. 3. Clinical screening, evaluated by the volume-viscosity swallow test (V-VST) and the fibreoptic endoscopic evaluation of swallowing (FEES). 4. Personalised report with recommendations on diet and exercise targeted at swallowing, depending on observed changes. The V-VST is designed to select the safest and most effective volume and viscosity, assessing whether there are any signs of alterations in efficacy and/or safety of swallow.17 Three different viscosities are prepared (liquid, nectar and pudding) mixing water at room temperature with a commercial thickening agent, following manufacturer’s recommendations (nectar: 100 ml water+1 level scoop of 4.5 g; pudding: 100 ml water+2 level scoops of 9 g). The patient remains seated with the head in a vertical position; the secretions in the mouth (alveolar recesses) and oropharynx are cleaned, and the patient is asked to say their name so their voice can be heard. Basal SaO2 in capillary blood is measured through a finger pulse, with normality ranging between 95% and 97% (2% range of variation). The decrease of basal SaO2 ≥3% during intake of any viscosity is a sign of aspiration.18 The viscosities were administered with 3 spoons: 2.5 ml (teaspoon), 5 ml (dessert spoon) and 10 ml (soup spoon) and a 20 ml glass. For safety measures, the original Clavé protocol was altered, on reducing initial volume to 2.5 ml, since this reduced the risk of aspiration. Initial administration was therefore 2.5 ml with nectar and, if there were no changes in safety, the volume was increased to 20 ml and liquid was administered. If there were any alterations in safety with the nectar the pudding was administered, with the liquid being omitted, since the changes would probably have been greater. If the changes were apparent in liquid form the pudding was also then administered. All participants were administered the pudding viscosity. Clinical signs affecting efficacy were assessed (insufficient labial closing, oral residues, pharyngeal residues or fractionated
18 swallowing) and the safety in swallow (moist vocals, cough and reduction of SaO2 ). If during V-VST there is any sign of efficacy changing, the test for that volume/viscosity is positive and means that the patient will not be able to maintain an appropriate nutritional status and hydration. If there are alterations in safety, the test is also positive, with the bolus being unsafe, with a risk of penetration-aspiration, and the viscosity should be increased and/or the volume decreased. FEES is a procedure using instruments and is carried out by an ENT specialist. The nasal passage is selectively anaesthetised where the flexible video endoscope (Olympus ENF-V2) passes. This is connected to a video (OTV-SI digital processor) and to recording equipment. The video endoscope is angled to reach the cavum until its end is located level with the uvula. Exploration is first completed without food to confirm laryngeal closure during sustained vowel phonation (/e/,/i/), the effectiveness of coughing (fold approximation, secretion mobilisation, sound) and the retention of saliva and secretions (epiglottic valleculas, aryepiglottic folds, pyriform sinuses and retrocricoid area), together with their movement during dry swallowing. Active swallowing was subsequently tested, using the same V-VST consistencies, and the same reference values. 0.4 ml of methylene blue was poured over them to improve visualisation. The following was assessed: whether there is fractionated swallowing (>2 per bolus), posterior spillage, oral residues (epiglottic valleculas, pharyngeal wall, pyriform sinuses), laryngeal penetration and aspiration. The variables of the clinical report and the tests performed (V-VST and FEES) were studied. The clinical variables were: years of evolution of the PD (<10 years and >10 years), clinical grade and stage, weight loss, nutrition (normal diet or diet modified with thickening agents, meal duration, consultation for dysphagia) and respiratory problem (pneumonias or bronchitis) during the last year. The variables which assessed swallowing efficacy were: difficulty in transferring food from the plate to the mouth, insufficient labial closing, oral residues and fractionated swallowing. Four levels of involvement were obtained with these variables (with and without thickening agent): non involvement (no affected variable); mild involvement (one affected variable); moderate involvement (2 or 3 affected variables) and serious involvement (all 4 variables affected). The variables which assess swallowing safety are: reduction of ≥3% of basal SaO2 , pharyngeal particles in epiglottic valleculas, pharyngeal wall and pyriform sinuses after a second swallowing, coughing after swallowing, penetration of the bolus to the laryngeal vestibule above the vocal cords, bolus aspiration to subglottis and trachea. Four levels of effectiveness were obtained with these variables (with and without thickening agent): non involvement (no affected variable); mild involvement (1 or 2 affected variables); moderate involvement (3 or 4 affected variables) and serious involvement (5 variables affected or simply ‘‘aspiration’’). The SPSS programme version 22.0 for Windows (SPSS Inc., Chicago, IL) was used for analysis of variables. Descriptive statistical data were obtained (mean, standard deviation, range) and the correlation between the clinical variables
S. Mamolar Andrés et al. and the degree to which efficacy and safety were affected were analysed using the Spearman invariable correlation and the chi-squared coefficient. P<0.05 was considered to be statistically significant.
Results The mean age of the 52 participants in the study (26 men and 26 women) was 72.4 (age range 33---88 years). They regularly attended the APA day-care centre throughout the duration of the study. The final sample selected with the SDQ comprised 19 participants (36.5%), 13 men and 6 women, with a mean age of 69.9 (range 53---88 years). The 19 participants were PD classified as follows: moderate: 16 (84.2%), mild: 1 (5.3%) and advanced: 2 (10.5%). Clinical status (Hoehn and Yahr) was mostly given a score of 2 and 3 (16 patients; 84.2%) with a total mean value of 2.57±1.15. Data from the Unified Parkinson Disease Rating Scale was obtained for 12 participants (63.1%), with a mean score for motor activity (part III) of 28±9.2 compared with a reference score of between 0 and 68. On the Unified Parkinson Disease Rating Scale of daily activities (part II) the scores for the 3 sections relating to dysphagia (salivation, swallowing, cutting foods and managing cutlery) were collected, with a mean score of 1.6±0.3 compared to a reference score of between 0 and 12. With the exception of gender, where the SDQ detected over double males, the mean age and range of both samples (preliminary and final) had approximate values. The participants of the final sample demonstrated a 10.8 year mean of having been diagnosed with PD (range from 0 to 25 years). 10 participants had been diagnosed for over 10 years and the other 9 had been diagnosed for less than 10 years. One patient presented with mild cognitive disorders, but decided to participate and was able to do so correctly. In the final sample, 15 participants (78.9%) stated they were aware of their dysphagia problems in the subjective questions, and 11 of them also obtained scores of ≥11 in the numerical SDQ responses, compared with 4 who had lower values. Another 4 got scores >11 for the numerical responses to the test, but were not aware of dysphagia in the subjective question. Only one participant (5.3%) had consulted for SD. With regard to type of diet 4 participants (21.1%) used thickening agents compared with the other 15 (78.9%) who had not modified their diet. The time dedicated to meals was long (>30 min) for 10 participants (52.6%); normal (15---30 min) for 8 (42.1%) and there was only one recorded case of meal time lasting under 15 min. 6 participants (31.6%) stated they had suffered from respiratory problems during the last year (bronchitis or pneumonia). In the swallowing efficacy variables, 18 (94.7%) participants had been affected by some of them. The detected variables are listed in order in Table 1. On grouping the efficacy variables into degrees of affection we observed a predominance of ‘‘serious involvement’’ and ‘‘moderate involvement’’ as shown in Fig. 1. In the safety of swallow variables tested by V-VST and FEES, 11 (57.9%) participants were affected by some of them. The alterations detected are listed in order in Table 2. On
Swallowing Disorders in Parkinson’s Disease Table 1
19
Variables Which Change the Efficacy of Swallowing the Final Sample (n=19). Participants
Total
Liquids and Thickening Agents Fractionated swallowing Plate-to-mouth difficulty Insufficient labial closing Oral residues
Table 2
Only Thickening Agents
9 --6 2
8 --7 7
17 15 13 9
Variables Which Change the Safety of Swallowing in the Final Sample (n=19). Participants
Total
Liquids and Thickening Agents Pharyngeal residues Cough Penetration Aspiration SaO2 (reduction of <3%)
Just Thickening Agents
--5 4 -----
10 4 2 1 1
6
6
4
7 36.84%
2
8 42.11%
4
8 42.11%
4 21.05%
2
1 5.26%
1 5.26%
0 Mild
Moderate
Severe
No change
Degree
Figure 1
(52.7%) (47.4%) (31.6%) (5.3%) (5.3%)
6 31.58%
3 15.79%
No change
10 9 6 1 1
Changes in efficacy of swallowing 8
Cases
Cases
Changes in efficacy of swallowing 8
0
(89.5%) (78.9%) (68.4%) (47.4%)
Changes in efficacy of swallowing.
grouping the safety variables into levels of influence, we observed a predominance of the ‘‘not affected’’ or ‘‘mildly affected’’ as shown in Fig. 2. In the final sample selected with the SDQ the SD in only one participant (5.3%) did not show up when tested with V-VST and FEES. We attempted to establish a relationship between the changes in efficacy and safety, individually, with different clinical variables. The results obtained in the SDQ were significantly correlated with a degree of alteration of efficacy (P=0.037), i.e. the higher the score in the SDQ the higher the degree of alteration. However, there was no correlation between the SDQ scores and the degree of change in safety. The clinical variable ‘‘time used for meals’’ was significantly associated with a degree of change in efficacy (P=0.001). A significant association was also demonstrated between the presence of respiratory problems in the last year and alterations in safety (P=0.032), where the penetration score was the most significant (P=0.004).
Mild
Moderate
Severe
Degree
Figure 2
Changes in swallowing safety.
There were no significant associations between the variables ‘‘time of PD evolution’’, ‘‘Degree and clinical status’’, ‘‘modified diet’’ and ‘‘weight loss’’ and levels of efficacy and safety of swallow.
Discussion SD are common in PD, as shown by the SDQ in 36.5% of the preliminary samples. In the final sample studied with the V-VST or the FEES SD were found in 18 (94.7%), which affected efficacy and/or safety individually or jointly. The tests resulted normal in only one participant (5.3%) with the SDQ serving as a screener. This case detected by the SDQ, but not confirmed by the tests, could be explained by the anxiety the disease generates in patients or the adjustment to medical treatment which may improve this situation.5,16 Another possible explanation would be the fluctuation of the swallow function during on-off periods. This issue was
20 also reflected and dealt with by Manor when the SDQ was designed.16 Although the detected SD are frequent, only four participants had diets adapted with thickening agents and only one had consulted a physician about this problem. The reason why PD patients are not inclined to discuss their SD may be explained by the progressively slow evolution of the disease and the development of dietary adaptations. Other authors have reported that patients do not consult their SD until they are serious and lead to serious complications, possibly relating to the associated cognitive change to PD (dysexecutive syndrome, bradypsychia, apathy, dementia, etc.).1,7,16 Logeman considered that the level of awareness of swallowing problems is low due to a failure to recognise its symptoms.13 Notwithstanding, in our study 15 participants (78.9%) showed they had SD if they were asked directly about it. The particular sensitivity of the participants to symptoms related to swallowing could be explained by their regular attendance at speech therapy sessions in the APA, where they were informed and updated about their disease and the symptoms it could entail. A relationship has been found between the SDQ scores and efficacy variables obtained, but none was observed with the safety variables. This situation could be due to the fact that the participants are more familiar with efficacy symptoms and also that those relating to safety are less frequent. Alterations in efficacy were observed in many participants, since 37% and 42% presented with moderate or serious changes respectively, with three or four variables having changed. There was a significant relationship between serious problems in efficacy and a longer time used in ingestion. Other authors have observed that efficacy in swallow is related to the ability to feed oneself, to maintain an appropriate state of nutrition and hydration and in the difficulty in taking oral medicine, with malnutrition being detected in one out of every three patients.18 Increase in the duration of meal times observed in our study (52.6%) would be interpreted as relating to mobility and swallowing limitations, together with a reduced desire to eat, with repercussions in the patient’s nutritional status.14 We were unable to use the Unified Parkinson Disease Rating Scale on all clinical records. Those that were observed showed an intermediate total score in the mobility section and a low score in sections relating to swallowing, in the section on daily life activities. Although we did not obtain data relating to malnutrition or its causes, many participants or their families mentioned major weight loss. 79% of participants experienced difficulty in conveying the food on the plate to their mouth. Similarly to Miller, this situation was included in the changes in efficacy section, on consideration that the standard triad of PD symptoms (tremors, bradikinesia, stiffness) had an effect on transporting food to the mouth.9 The main difficulty resided in obtaining appropriate mastication, cohesion and control of the bolus in the mouth, leading to the food coming out of the mouth due to insufficient labial closing, which was found in 68.4% of the sample. Food residues in the oral cavity (47.4%) and over two swallows per bolus (89.5%) completed our data with regards to changes in efficacy. Repeated anteroposterior tongue movements have been reported in
S. Mamolar Andrés et al. PD which impede the propulsion of the bolus into the pharynx, leading to muscular fatigue, increasing meal time and malnutrition.13 Another event we observed is that there are many changes in efficacy if the bolus consistency is increased or if the volume is greater, although these also appear with the liquid consistency when there is insufficient labial closing (31.6%), oral remains (10.5%) and fractionated swallowing (47.3%). Clavé concluded that patients with neurogen dysphagia tolerated nectar viscosity better, because greater viscosity led to a slower oropharyngeal transit, less force of propulsion of the bolus and a greater accumulation in the oropharynx.19 Alterations in safety are related to a very high incidence of silent aspiration, with pneumonia being the main cause of death. In our study the presence of respiratory diseases during the last year cited aspiration as the cause. We observed a correlation between respiratory conditions during the last year and the severity of alterations in safety, although in the FEES, aspiration with a lowering of SaO2 was only present in one participant. Miller refers to possible silent aspirations in PD with no presentation of subjective complaints of dysphagia.9 The limitations observed in the portable finger pulses regarding a reliable SaO2 20 mean should also be taken into account. Particles of food in the epiglottic vallecula and pyriform sinuses were frequent (52.7%), and could be explained by muscular weakness at the base of the tongue and in the pharyngeal constrictors, limiting laryngeal elevation and increasing the risk of penetration. As a result, 6 participants (31.6%) presented with penetrations, generally after swallowing, as a result of particles of food which had accumulated in the pharynx brimming up and penetrating the laryngeal vestibule. There was a significant relationship between participants with penetrations and those who presented with respiratory disease. Velasco recorded that 2 out of every 3 patients with SD were at serious risk of contracting pneumonia from aspiration, and respiratory infections.21 During the tests 9 (47.4%) participants presented with coughing. The cough reflex is considered to be a defence mechanism against aspiration but we did, however, not observe any relationship between both variables. A cough may be a confusing sign to assess, since several participants presented with it due to distaste and repugnance at the flavour and consistency of the thickening agent. Other authors refer to possible silent aspirations without the presentation of a cough or subjective complaints about dysphagia.9,14 There was no observation of any relationship between the time of evolution of the disease and the degree of how safety was affected and several participants saw changes to efficacy and safety during the first year following diagnosis of PD. There are several discrepancies in the references and some authors state that many patients with PD, even in advanced stages, have no serious problems in swallowing,9 whilst others suffer from this in 90% of advanced stages.8 One explanation for the disparity of opinions would be that pharmacological treatment improves the symptoms if the dose and drugs are appropriate, together with the actual evolution of the PD with its on-off periods.1,16,18
Swallowing Disorders in Parkinson’s Disease We did not experience any significant relationship between the stages and clinical conditions of PD and the degree of SD, possibly due to the fact that the majority of participants were contained at the moderate level and in stages 2 and 3. Furthermore, current suggested changes to PD patients regarding the consistency of foods, exercise and postural changes whilst eating improve their symptoms and condition irregular presentation of dysphagia.4 One possible limitation to the study was using the SDQ as a screener, since up until now it has only been validated in English. However, given that no alternative was available in Spanish, a literal translation was produced. The test questions are clear and direct and there was no linguistic confusion. They were completed with additional explanations when necessary, which was almost never. The final sample was similar to that presented by Manor who designed and validated the SDQ with 57 patients whose mean age was 69, with a (Hoehn and Yahr) clinical status of 2.6±1.1 and disease evolution of 6.7±5.3 years of age.16 We believe that the SDQ, as designed, was appropriate for its screening purpose and its literal translation did not lead to any interpretation weighting from participants. However, its validation into Spanish is recommended. We did not consider it ethical to do a V-VST and FEES screening of all PD patients if they did not present with SD or complications at that time, especially in the knowledge that the situation could change. This took us to an unlimited number of tests, which took up a considerable amount of time in the clinic and entailed upset for the patients. We therefore emphasise the importance of having the SDQ available in Spanish as a screening prior to V-VST and FEES. The number of participants in our study is still low and they are not representative of the whole group with PD, although they do define those who attend a specific centre. It would be of great interest to extend the study to other centres in the community to obtain a wider and more representative sample, with more reliable data which could then be extrapolated to all patients. These tests could be protocolised in a routine manner during clinical visits, to detect possible complications, plan corrective measures and improve quality of life.
Conclusions The SD detected by the SDQ affected 36.5% of the PD patients in our study. Of the participants selected by the SDQ, 94.7% presented changes in efficacy and safety in the V-VST and/or FEES. There was a high level of effect from changes in efficacy, with fractionated swallowing (89.5%) and plate-to-mouth transport (78.9%) as the most common. Alterations in safety were less frequent (57.9%), and the level of effects was lower, with food particles in the pharynx (52.7%) and laryngeal penetrations (31.6%) as the most common. Alterations in safety are linked to the risk of pneumonia due to aspiration and respiratory infections, whilst changes in efficacy are due to meal time duration. A final reflection may be that the professionals who work in Dysphagia Units must make a competent diagnosis and administer relevant treatment for SD in PD, in addition to
21 participating in training all other personnel who are treating these patients. An action plan protocol would need to be established to prevent any further serious complications such as malnutrition and pneumonia from aspiration.
Conflict of Interests The authors have no conflict of interests to declare.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.otoeng.2017.01.003.
References 1. Enfermedad de Parkinson. Guía terapéutica de la Sociedad Catalana de Neurología. Kulisevsky Bojarski J (Coord). Fundación Sociedad Catalana de Neurología. Available at: http://www.scn.es/sp/form/guias/park/Parkinson.htm 2. La situación de los enfermos afectados por la enfermedad de Parkinson, sus necesidades y sus demandas. Dávila P, Rubí E y Mateo A (Coords). Colección Estudios. Ministerio de Educación, Política Social y Deporte Secretaría de Estado de Política Social, Familias y Atención a la Dependencia y la Discapacidad. Madrid: Instituto de Mayores y Servicios Sociales (IMSERSO); 2008. pp. 17---36. 3. Webb W, Adle R. Sindromes clínicos del habla secundarios a la alteración de los sistemas motores. In: Webb W, Adle R, editors. Neurología para el logopeda. Barcelona: Elservier Masson; 2010. p. 169---89. 4. Goetz CG. The history of Parkinson’s disease: early clinical descriptions and neurological therapies. Cold Spring Harb Perspect Med. 2011:1. Available at: http:// perspectivesinmedicine.cshlp.org/content/1/1/a008862.full. pdf+html 5. Baijens LWJ, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24:91---102. 6. Luchesi KF, Kitamura S, Mourão LF. Management of dysphagia in Parkinson’s disease and amyotrophic lateral sclerosis. CoDAS. 2013;25:358---64. 7. Clemente-Benaiges I, Avi˜ nó-Farret C. Papel de la logopedia en el tratamiento de la disartria y la disfagia en la enfermedad de Parkinson. Neurol Supl. 2007;3:30---3. 8. González-Fernández J, Prieto-Tedejo R, Velasco-Palacios L, Jorge-Roldán S, Cubo-Delgado E. Trastornos digestivos en la enfermedad de Parkinson: disfagia y sialorrea. Rev Neurol. 2010;50:51---4. 9. Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing. 2006;35:614---8. 10. Zaras K. Dysphagia in Parkinson’s disease. In: Logopedia. Lublin: Editorial Board; 2007. p. 221---8. 11. Bayés-Rusi˜ nol A, Forjaz MJ, Ayala A, Crespo MC, Prats A, Valles E, et al. Conciencia de la disfagia en la enfermedad de Parkinson. Rev Neurol. 2011;53:664---72. 12. Santos García D, de Deus T, Tejera Pérez C, Expósito Ruiz I, Suárez Castro E, Carpintero P, et al. Rev Neurol. 2015;61:261---70. 13. Logemann J. Evaluation and treatment of swallowing disorders. Austin, TX: Pro-Ed; 1998. 14. Almirall J, Cabré M, Clavé P. Neumonía aspirativa. Med Clin (Barc). 2007;129:424---32.
22 15. Leow L, Huckabee M, Anderson T, Beckert L. The impact of dysphagia on quality of life in ageing and Parkinson’s disease as measured by the Swallowing Quality of Life (SWAL-QOL) Questionnaire. Dysphagia. 2010;25:216---20. 16. Manor Y, Giladi N, Cohen A, Fliss DM, Cohen JT. Validation of swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease. Mov Disord. 2007;22:1917---21. 17. Clavé P, García P. Guía de diagnóstico y tratamiento nutricional y rehabilitador de la disfagia orofaríngea. Barcelona: Editorial Glosa; 2011. 18. Correa-Flores M, Arch-Tiradi E, Villeda-Miranda A, RochaCacho K, Verduzco-Mendoza A, Hernández-López X. Análisis de
S. Mamolar Andrés et al. la disfagia orofaríngea por medio de la evaluación fibroendoscópica de la deglución en pacientes con enfermedad de Parkinson. Cirugía y Cirujanos. 2012;80:31---7. 19. Clavé P, Kraa M, de Arreola V, Girvent M, Farré R, Palomera E, et al. The effect of bolus viscosity on swallowing function in neurogenicdysphagia. Aliment Pharmacol Therap. 2006;24:1385---94. 20. Martínez González A, Irizar Aranburu MI. La pulsioximetría en atención primaria. Revista AMF. 2006;2:46---50. 21. Velasco MM, Arreola V, Clavé P, Puiggrós C. Abordaje clínico de la disfagia orofaríngea: diagnóstico y tratamiento. Nutr Clín Med. 2007;1:174---202.
www.elsevier.es/otorrino
ORIGINAL ARTICLE
Swallowing Disorders in Parkinson’s Disease夽 Sandra Mamolar Andrés,a María Liliana Santamarina Rabanal,a,b,c Carla María Granda Membiela,a María José Fernández Gutiérrez,a,c Paloma Sirgo Rodríguez,a,c César Álvarez Marcosa,b,d,∗ a
Universidad de Oviedo, Oviedo, Asturias, Spain Unidad de Disfagia, Servicio de Rehabilitación, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain c Unidad de Foniatría y Logopedia, Servicio de Rehabilitación, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain d Servicio de Otorrinolaringología, Hospital Universitario Central de Asturias (HUCA), Oviedo, Asturias, Spain b
Received 30 January 2016; accepted 10 February 2016
KEYWORDS Dysphagia; Parkinson’s disease; Volume-viscosity examination; Pneumonia aspiration; Fibreoptic endoscopic swallowing
Abstract Introduction: Parkinson’s disease is a type of chronic neurodegenerative pathology with a typical movement pattern, as well as different, less studied symptoms such as dysphagia. Disease-related disorders in efficacy or safety in the process of swallowing usually lead to malnutrition, dehydration or pneumonias. The aim of this study was identifying and analyzing swallowing disorders in Parkinson’s disease. Subjects and methods: The initial sample consisted of 52 subjects with Parkinson’s disease to whom the specific test for dysphagia SDQ was applied. Nineteen participants (36.5%) with some degree of dysphagia in the SDQ test were selected to be evaluated by volume-viscosity clinical exploration method and fibreoptic endoscopic evaluation of swallowing. Results: Disorders in swallowing efficiency and safety were detected in 94.7% of the selected sample. With regards to efficiency, disorders were found in food transport (89.5%), insufficient labial closing (68.4%) and oral residues (47.4%), relating to duration of ingestion. Alterations in security were also observed: pharynx residues (52.7%), coughing (47.4%), penetration (31.64%), aspiration and decrease of SaO2 (5.3%), relating to the diagnosis of respiratory pathology in the previous year.
夽
Please cite this article as: Mamolar Andrés S, Santamarina Rabanal ML, Granda Membiela CM, Fernández Gutiérrez MJ, Sirgo Rodríguez P, Álvarez Marcos C. Trastornos de la deglución en la enfermedad de Parkinson. Acta Otorrinolaringol Esp. 2017;68:15---22. ∗ Corresponding author. E-mail address: [email protected] (C. Álvarez Marcos). 2173-5735/© 2016 Elsevier Espa˜ na, S.L.U. and Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. All rights reserved.
16
S. Mamolar Andrés et al. Conclusion: The SDQ test detected swallowing disorders in 36.5% of the subjects with Parkinson’s disease. Disorders in swallowing efficiency and safety were demonstrated in 94.7% of this subset. Disorders of efficiency were more frequent than those of safety, establishing a relationship with greater time in ingestion and the appearance of respiratory pathology and pneumonias. © 2016 Elsevier Espa˜ na, S.L.U. and Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. All rights reserved.
PALABRAS CLAVE Disfagia; Enfermedad de Parkinson; Método volumen-viscosidad; Neumonía aspirativa; Videoendoscopia deglución
Trastornos de la deglución en la enfermedad de Parkinson Resumen Introducción: La enfermedad de Parkinson es una patología neurodegenerativa crónica, con síntomas motores característicos y otros menos estudiados como la disfagia. Suele relacionarse con desnutrición, deshidratación o neumonías por aspiración por trastornos en la eficacia y seguridad en la deglución. El objetivo de este trabajo es identificar y analizar los trastornos deglutorios en la enfermedad de Parkinson. Sujetos y métodos: Muestra inicial de 52 sujetos con enfermedad de Parkinson a los que se aplicó el test SDQ, específico para la disfagia. Se seleccionaron 19 (36,5%) participantes con algún grado de disfagia en dicho test para ser evaluados con el método de exploración clínica volumen-viscosidad y la videoendoscopia de la deglución. Resultados: Se detectaron trastornos de eficacia y seguridad de la deglución en el 94,7%, siendo las alteraciones de la eficacia: dificultad en el transporte de alimento (89,5%), deglución fraccionada (78,9%), mal sello labial (68,4%) y residuos orales (47,4%), relacionándose con el tiempo que dura la ingesta. Se observaron también alteraciones en la seguridad como residuos faríngeos (52,7%), tos (47,4%), penetración (31,64%), aspiración y descenso de SaO2 (5,3%), relacionándose con el diagnóstico de patología respiratoria en el último a˜ no. Conclusiones: El test SDQ detectó trastornos deglutorios en el 36,5% de los pacientes con enfermedad de Parkinson. Las alteraciones en la eficacia y seguridad de la deglución se demostraron en el 94,7% de ellos, siendo más frecuentes los trastornos de eficacia que los de seguridad, estableciendo relación con el mayor tiempo en la ingesta y la aparición de patología respiratoria y neumonías. © 2016 Elsevier Espa˜ na, S.L.U. y Sociedad Espa˜ nola de Otorrinolaringolog´ıa y Cirug´ıa de Cabeza y Cuello. Todos los derechos reservados.
Introduction Parkinson’s disease (PD) is a chronic neurodegenerative pathology leading to progressive debilitation. It has been estimated that in Spain there are approximately 70 000 people suffering from the disease, with an incidence of 16/100 000 inhabitants/per year and a prevalence of 1000/100 000 inhabitants, but it is probable that these data have been underestimated.1,2 The aetiology of PD is unknown although it is believed that a number of genetic and environmental factors are involved. The anatomical substrate is the progressive disappearance of dopamine neurones of the locus niger, the midbrain basal ganglia.3 Dopamine controls voluntary movement and postural balance, and its deficiency causes the gradual, inexorable development of the disease.2 The beginning is insidious, with standard motor symptoms: tremor, bradykinesia and rigidity, together with other emotional, cognitive, sensitive, communicative symptoms and changes
in postural reflexes, which determine the Parkinson profile.4 Although PD is chronic and progressive there are replacement, electrophysiological and rehabilitation treatments which impede its evolution.5,6 In Dysphagia Units swallowing disorders (SD) caused by neurodegenerative diseases are increasingly better controlled and the professionals involved are used to dealing with these patients. PD leads to SD in up to 90% of patients in advanced stages of the disease.7,8 However, the number of patients with PD who consult their doctor or speech therapist about dysphagia is limited and does not meet with expectations. SD from PD have been described in all stages of swallowing and are manifold: limitations in transporting food to the mouth, difficulty in chewing, hypersalivation, inability to form a cohesive bolus, reduction in swallowing reflex, delayed and incomplete laryngeal closure, reduced pharyngeal and oesophageal peristalsis, and gastroesophageal reflux.7,9---12 Dysphagia may occur in any evolutive stage but
Swallowing Disorders in Parkinson’s Disease worsens as the disease advances and in the off periods. The most serious complications are aspiration and pneumonia, difficulty in oral drug administration, malnutrition and dehydration. There is a high incidence of silent aspiration with pneumonia being the principal cause of death.13 Treatment with L-DOPA and adaptive feeding methods improve the effectiveness and safety of swallowing and increase the speed of transit.5,6 Occasionally a nasogastric tube or percutaneous endoscopic gastrostomy tube may be used, especially if aspiration and pneumonia present.8,14 SD in PD have an effect on the patient’s quality of life. In advanced stages the desire to eat decreases and the difficulty in selecting food and the duration of meals increases, with repercussions on their nutritional status.15 The aim of this article is to apply a clinical protocol for early detection of SD in PD patients and to assess their frequency, type and severity.
Subjects and Methods There were 52 participants in the study (26 men and 26 women) with a mean age of 72.4 (age range 34---88 years), who were members of the ‘‘Asturias Parkinson Association (APA) in Oviedo. In this preliminary sample the ‘‘Swallowing Disturbance Questionnaire’’ (SDQ)16 was applied in order to select those who presented with significant SD, and when the final sample was obtained all subsequent procedures were performed. All participants of the final sample had been diagnosed in the Neurology Department of the Hospital Universitario Central de Asturias and regularly attended the APA for two weekly speech therapy sessions. The patients attended the day centre from early morning, completing the SDQ after having taken their recommended medication. None of the participants had previously been evaluated and diagnosed with SC by means of any specific tests. During phase one, from 10th to 14th November 2014, recruitment and selection of the participants was carried out in the APA central office. This phase was approved by the APA management board. The speech therapists of the association personally administered the SDQ, with confidentiality being guaranteed, and the patients’ acceptance of inclusion in the study was key. The 52 participants represented the majority of associates who regularly attended the centre during this period. They had not been diagnosed with any degree of dementia and were capable of reading and understanding the SDQ contents, in addition to participating in the instrumental tests. The SDQ is an easily applied questionnaire, designed to specifically detect SD in PD.16 It assesses the response to a general, subjective question (‘‘do you think you have problems with eating and drinking?’’) to which a yes/no response is requested. Thereafter there are 15 items on dysphagia. In 14 of the questions the response is made on a Likert scale of 0 (never) to 3 (very frequently), 5 of them relating to the oral stage of swallowing and 9 to the pharyngeal. The last of the items (‘‘have you suffered from a respiratory pneumonia or bronchitis type infection in the last year?) is answered with yes/no and assessed with 2.5 points if it is Yes and 0.5 points if it is No. The SDQ was originally designed and validated in English and has not been adapted or validated in Spanish.
17 However, as there is no similar test in our language and given its renowned usefulness, a literal translation was made of it since neither vocal nor phonetic elements of quality were assessed (Appendix). The SDQ selection of participants for the final sample was made with cut-off values ≥11 in the 15 items or if the response to the subjective question was ‘‘yes’’ (16). The second stage of the study consisted in applying the dysphagia clinical assessment protocol to the selected participants. This phase was performed in the Otorhinolaryngology Department of Hospital Universitario Central de Asturias between December 2014 and March 2015, under medical supervision, with patients attending a single session first thing in the morning after taking their mediation. The protocol comprised: 1. Data collection (parentage, background, stage, evolution of PD, dysphagia symptoms, etc.) offered by the patient/family member/carer and computerised medical record. 2. Explanation and signing of informed consent for the tests. The study was approved by the Medical Board and the Ethics Committee, which authorised its completion in the relevant hospitals. 3. Clinical screening, evaluated by the volume-viscosity swallow test (V-VST) and the fibreoptic endoscopic evaluation of swallowing (FEES). 4. Personalised report with recommendations on diet and exercise targeted at swallowing, depending on observed changes. The V-VST is designed to select the safest and most effective volume and viscosity, assessing whether there are any signs of alterations in efficacy and/or safety of swallow.17 Three different viscosities are prepared (liquid, nectar and pudding) mixing water at room temperature with a commercial thickening agent, following manufacturer’s recommendations (nectar: 100 ml water+1 level scoop of 4.5 g; pudding: 100 ml water+2 level scoops of 9 g). The patient remains seated with the head in a vertical position; the secretions in the mouth (alveolar recesses) and oropharynx are cleaned, and the patient is asked to say their name so their voice can be heard. Basal SaO2 in capillary blood is measured through a finger pulse, with normality ranging between 95% and 97% (2% range of variation). The decrease of basal SaO2 ≥3% during intake of any viscosity is a sign of aspiration.18 The viscosities were administered with 3 spoons: 2.5 ml (teaspoon), 5 ml (dessert spoon) and 10 ml (soup spoon) and a 20 ml glass. For safety measures, the original Clavé protocol was altered, on reducing initial volume to 2.5 ml, since this reduced the risk of aspiration. Initial administration was therefore 2.5 ml with nectar and, if there were no changes in safety, the volume was increased to 20 ml and liquid was administered. If there were any alterations in safety with the nectar the pudding was administered, with the liquid being omitted, since the changes would probably have been greater. If the changes were apparent in liquid form the pudding was also then administered. All participants were administered the pudding viscosity. Clinical signs affecting efficacy were assessed (insufficient labial closing, oral residues, pharyngeal residues or fractionated
18 swallowing) and the safety in swallow (moist vocals, cough and reduction of SaO2 ). If during V-VST there is any sign of efficacy changing, the test for that volume/viscosity is positive and means that the patient will not be able to maintain an appropriate nutritional status and hydration. If there are alterations in safety, the test is also positive, with the bolus being unsafe, with a risk of penetration-aspiration, and the viscosity should be increased and/or the volume decreased. FEES is a procedure using instruments and is carried out by an ENT specialist. The nasal passage is selectively anaesthetised where the flexible video endoscope (Olympus ENF-V2) passes. This is connected to a video (OTV-SI digital processor) and to recording equipment. The video endoscope is angled to reach the cavum until its end is located level with the uvula. Exploration is first completed without food to confirm laryngeal closure during sustained vowel phonation (/e/,/i/), the effectiveness of coughing (fold approximation, secretion mobilisation, sound) and the retention of saliva and secretions (epiglottic valleculas, aryepiglottic folds, pyriform sinuses and retrocricoid area), together with their movement during dry swallowing. Active swallowing was subsequently tested, using the same V-VST consistencies, and the same reference values. 0.4 ml of methylene blue was poured over them to improve visualisation. The following was assessed: whether there is fractionated swallowing (>2 per bolus), posterior spillage, oral residues (epiglottic valleculas, pharyngeal wall, pyriform sinuses), laryngeal penetration and aspiration. The variables of the clinical report and the tests performed (V-VST and FEES) were studied. The clinical variables were: years of evolution of the PD (<10 years and >10 years), clinical grade and stage, weight loss, nutrition (normal diet or diet modified with thickening agents, meal duration, consultation for dysphagia) and respiratory problem (pneumonias or bronchitis) during the last year. The variables which assessed swallowing efficacy were: difficulty in transferring food from the plate to the mouth, insufficient labial closing, oral residues and fractionated swallowing. Four levels of involvement were obtained with these variables (with and without thickening agent): non involvement (no affected variable); mild involvement (one affected variable); moderate involvement (2 or 3 affected variables) and serious involvement (all 4 variables affected). The variables which assess swallowing safety are: reduction of ≥3% of basal SaO2 , pharyngeal particles in epiglottic valleculas, pharyngeal wall and pyriform sinuses after a second swallowing, coughing after swallowing, penetration of the bolus to the laryngeal vestibule above the vocal cords, bolus aspiration to subglottis and trachea. Four levels of effectiveness were obtained with these variables (with and without thickening agent): non involvement (no affected variable); mild involvement (1 or 2 affected variables); moderate involvement (3 or 4 affected variables) and serious involvement (5 variables affected or simply ‘‘aspiration’’). The SPSS programme version 22.0 for Windows (SPSS Inc., Chicago, IL) was used for analysis of variables. Descriptive statistical data were obtained (mean, standard deviation, range) and the correlation between the clinical variables
S. Mamolar Andrés et al. and the degree to which efficacy and safety were affected were analysed using the Spearman invariable correlation and the chi-squared coefficient. P<0.05 was considered to be statistically significant.
Results The mean age of the 52 participants in the study (26 men and 26 women) was 72.4 (age range 33---88 years). They regularly attended the APA day-care centre throughout the duration of the study. The final sample selected with the SDQ comprised 19 participants (36.5%), 13 men and 6 women, with a mean age of 69.9 (range 53---88 years). The 19 participants were PD classified as follows: moderate: 16 (84.2%), mild: 1 (5.3%) and advanced: 2 (10.5%). Clinical status (Hoehn and Yahr) was mostly given a score of 2 and 3 (16 patients; 84.2%) with a total mean value of 2.57±1.15. Data from the Unified Parkinson Disease Rating Scale was obtained for 12 participants (63.1%), with a mean score for motor activity (part III) of 28±9.2 compared with a reference score of between 0 and 68. On the Unified Parkinson Disease Rating Scale of daily activities (part II) the scores for the 3 sections relating to dysphagia (salivation, swallowing, cutting foods and managing cutlery) were collected, with a mean score of 1.6±0.3 compared to a reference score of between 0 and 12. With the exception of gender, where the SDQ detected over double males, the mean age and range of both samples (preliminary and final) had approximate values. The participants of the final sample demonstrated a 10.8 year mean of having been diagnosed with PD (range from 0 to 25 years). 10 participants had been diagnosed for over 10 years and the other 9 had been diagnosed for less than 10 years. One patient presented with mild cognitive disorders, but decided to participate and was able to do so correctly. In the final sample, 15 participants (78.9%) stated they were aware of their dysphagia problems in the subjective questions, and 11 of them also obtained scores of ≥11 in the numerical SDQ responses, compared with 4 who had lower values. Another 4 got scores >11 for the numerical responses to the test, but were not aware of dysphagia in the subjective question. Only one participant (5.3%) had consulted for SD. With regard to type of diet 4 participants (21.1%) used thickening agents compared with the other 15 (78.9%) who had not modified their diet. The time dedicated to meals was long (>30 min) for 10 participants (52.6%); normal (15---30 min) for 8 (42.1%) and there was only one recorded case of meal time lasting under 15 min. 6 participants (31.6%) stated they had suffered from respiratory problems during the last year (bronchitis or pneumonia). In the swallowing efficacy variables, 18 (94.7%) participants had been affected by some of them. The detected variables are listed in order in Table 1. On grouping the efficacy variables into degrees of affection we observed a predominance of ‘‘serious involvement’’ and ‘‘moderate involvement’’ as shown in Fig. 1. In the safety of swallow variables tested by V-VST and FEES, 11 (57.9%) participants were affected by some of them. The alterations detected are listed in order in Table 2. On
Swallowing Disorders in Parkinson’s Disease Table 1
19
Variables Which Change the Efficacy of Swallowing the Final Sample (n=19). Participants
Total
Liquids and Thickening Agents Fractionated swallowing Plate-to-mouth difficulty Insufficient labial closing Oral residues
Table 2
Only Thickening Agents
9 --6 2
8 --7 7
17 15 13 9
Variables Which Change the Safety of Swallowing in the Final Sample (n=19). Participants
Total
Liquids and Thickening Agents Pharyngeal residues Cough Penetration Aspiration SaO2 (reduction of <3%)
Just Thickening Agents
--5 4 -----
10 4 2 1 1
6
6
4
7 36.84%
2
8 42.11%
4
8 42.11%
4 21.05%
2
1 5.26%
1 5.26%
0 Mild
Moderate
Severe
No change
Degree
Figure 1
(52.7%) (47.4%) (31.6%) (5.3%) (5.3%)
6 31.58%
3 15.79%
No change
10 9 6 1 1
Changes in efficacy of swallowing 8
Cases
Cases
Changes in efficacy of swallowing 8
0
(89.5%) (78.9%) (68.4%) (47.4%)
Changes in efficacy of swallowing.
grouping the safety variables into levels of influence, we observed a predominance of the ‘‘not affected’’ or ‘‘mildly affected’’ as shown in Fig. 2. In the final sample selected with the SDQ the SD in only one participant (5.3%) did not show up when tested with V-VST and FEES. We attempted to establish a relationship between the changes in efficacy and safety, individually, with different clinical variables. The results obtained in the SDQ were significantly correlated with a degree of alteration of efficacy (P=0.037), i.e. the higher the score in the SDQ the higher the degree of alteration. However, there was no correlation between the SDQ scores and the degree of change in safety. The clinical variable ‘‘time used for meals’’ was significantly associated with a degree of change in efficacy (P=0.001). A significant association was also demonstrated between the presence of respiratory problems in the last year and alterations in safety (P=0.032), where the penetration score was the most significant (P=0.004).
Mild
Moderate
Severe
Degree
Figure 2
Changes in swallowing safety.
There were no significant associations between the variables ‘‘time of PD evolution’’, ‘‘Degree and clinical status’’, ‘‘modified diet’’ and ‘‘weight loss’’ and levels of efficacy and safety of swallow.
Discussion SD are common in PD, as shown by the SDQ in 36.5% of the preliminary samples. In the final sample studied with the V-VST or the FEES SD were found in 18 (94.7%), which affected efficacy and/or safety individually or jointly. The tests resulted normal in only one participant (5.3%) with the SDQ serving as a screener. This case detected by the SDQ, but not confirmed by the tests, could be explained by the anxiety the disease generates in patients or the adjustment to medical treatment which may improve this situation.5,16 Another possible explanation would be the fluctuation of the swallow function during on-off periods. This issue was
20 also reflected and dealt with by Manor when the SDQ was designed.16 Although the detected SD are frequent, only four participants had diets adapted with thickening agents and only one had consulted a physician about this problem. The reason why PD patients are not inclined to discuss their SD may be explained by the progressively slow evolution of the disease and the development of dietary adaptations. Other authors have reported that patients do not consult their SD until they are serious and lead to serious complications, possibly relating to the associated cognitive change to PD (dysexecutive syndrome, bradypsychia, apathy, dementia, etc.).1,7,16 Logeman considered that the level of awareness of swallowing problems is low due to a failure to recognise its symptoms.13 Notwithstanding, in our study 15 participants (78.9%) showed they had SD if they were asked directly about it. The particular sensitivity of the participants to symptoms related to swallowing could be explained by their regular attendance at speech therapy sessions in the APA, where they were informed and updated about their disease and the symptoms it could entail. A relationship has been found between the SDQ scores and efficacy variables obtained, but none was observed with the safety variables. This situation could be due to the fact that the participants are more familiar with efficacy symptoms and also that those relating to safety are less frequent. Alterations in efficacy were observed in many participants, since 37% and 42% presented with moderate or serious changes respectively, with three or four variables having changed. There was a significant relationship between serious problems in efficacy and a longer time used in ingestion. Other authors have observed that efficacy in swallow is related to the ability to feed oneself, to maintain an appropriate state of nutrition and hydration and in the difficulty in taking oral medicine, with malnutrition being detected in one out of every three patients.18 Increase in the duration of meal times observed in our study (52.6%) would be interpreted as relating to mobility and swallowing limitations, together with a reduced desire to eat, with repercussions in the patient’s nutritional status.14 We were unable to use the Unified Parkinson Disease Rating Scale on all clinical records. Those that were observed showed an intermediate total score in the mobility section and a low score in sections relating to swallowing, in the section on daily life activities. Although we did not obtain data relating to malnutrition or its causes, many participants or their families mentioned major weight loss. 79% of participants experienced difficulty in conveying the food on the plate to their mouth. Similarly to Miller, this situation was included in the changes in efficacy section, on consideration that the standard triad of PD symptoms (tremors, bradikinesia, stiffness) had an effect on transporting food to the mouth.9 The main difficulty resided in obtaining appropriate mastication, cohesion and control of the bolus in the mouth, leading to the food coming out of the mouth due to insufficient labial closing, which was found in 68.4% of the sample. Food residues in the oral cavity (47.4%) and over two swallows per bolus (89.5%) completed our data with regards to changes in efficacy. Repeated anteroposterior tongue movements have been reported in
S. Mamolar Andrés et al. PD which impede the propulsion of the bolus into the pharynx, leading to muscular fatigue, increasing meal time and malnutrition.13 Another event we observed is that there are many changes in efficacy if the bolus consistency is increased or if the volume is greater, although these also appear with the liquid consistency when there is insufficient labial closing (31.6%), oral remains (10.5%) and fractionated swallowing (47.3%). Clavé concluded that patients with neurogen dysphagia tolerated nectar viscosity better, because greater viscosity led to a slower oropharyngeal transit, less force of propulsion of the bolus and a greater accumulation in the oropharynx.19 Alterations in safety are related to a very high incidence of silent aspiration, with pneumonia being the main cause of death. In our study the presence of respiratory diseases during the last year cited aspiration as the cause. We observed a correlation between respiratory conditions during the last year and the severity of alterations in safety, although in the FEES, aspiration with a lowering of SaO2 was only present in one participant. Miller refers to possible silent aspirations in PD with no presentation of subjective complaints of dysphagia.9 The limitations observed in the portable finger pulses regarding a reliable SaO2 20 mean should also be taken into account. Particles of food in the epiglottic vallecula and pyriform sinuses were frequent (52.7%), and could be explained by muscular weakness at the base of the tongue and in the pharyngeal constrictors, limiting laryngeal elevation and increasing the risk of penetration. As a result, 6 participants (31.6%) presented with penetrations, generally after swallowing, as a result of particles of food which had accumulated in the pharynx brimming up and penetrating the laryngeal vestibule. There was a significant relationship between participants with penetrations and those who presented with respiratory disease. Velasco recorded that 2 out of every 3 patients with SD were at serious risk of contracting pneumonia from aspiration, and respiratory infections.21 During the tests 9 (47.4%) participants presented with coughing. The cough reflex is considered to be a defence mechanism against aspiration but we did, however, not observe any relationship between both variables. A cough may be a confusing sign to assess, since several participants presented with it due to distaste and repugnance at the flavour and consistency of the thickening agent. Other authors refer to possible silent aspirations without the presentation of a cough or subjective complaints about dysphagia.9,14 There was no observation of any relationship between the time of evolution of the disease and the degree of how safety was affected and several participants saw changes to efficacy and safety during the first year following diagnosis of PD. There are several discrepancies in the references and some authors state that many patients with PD, even in advanced stages, have no serious problems in swallowing,9 whilst others suffer from this in 90% of advanced stages.8 One explanation for the disparity of opinions would be that pharmacological treatment improves the symptoms if the dose and drugs are appropriate, together with the actual evolution of the PD with its on-off periods.1,16,18
Swallowing Disorders in Parkinson’s Disease We did not experience any significant relationship between the stages and clinical conditions of PD and the degree of SD, possibly due to the fact that the majority of participants were contained at the moderate level and in stages 2 and 3. Furthermore, current suggested changes to PD patients regarding the consistency of foods, exercise and postural changes whilst eating improve their symptoms and condition irregular presentation of dysphagia.4 One possible limitation to the study was using the SDQ as a screener, since up until now it has only been validated in English. However, given that no alternative was available in Spanish, a literal translation was produced. The test questions are clear and direct and there was no linguistic confusion. They were completed with additional explanations when necessary, which was almost never. The final sample was similar to that presented by Manor who designed and validated the SDQ with 57 patients whose mean age was 69, with a (Hoehn and Yahr) clinical status of 2.6±1.1 and disease evolution of 6.7±5.3 years of age.16 We believe that the SDQ, as designed, was appropriate for its screening purpose and its literal translation did not lead to any interpretation weighting from participants. However, its validation into Spanish is recommended. We did not consider it ethical to do a V-VST and FEES screening of all PD patients if they did not present with SD or complications at that time, especially in the knowledge that the situation could change. This took us to an unlimited number of tests, which took up a considerable amount of time in the clinic and entailed upset for the patients. We therefore emphasise the importance of having the SDQ available in Spanish as a screening prior to V-VST and FEES. The number of participants in our study is still low and they are not representative of the whole group with PD, although they do define those who attend a specific centre. It would be of great interest to extend the study to other centres in the community to obtain a wider and more representative sample, with more reliable data which could then be extrapolated to all patients. These tests could be protocolised in a routine manner during clinical visits, to detect possible complications, plan corrective measures and improve quality of life.
Conclusions The SD detected by the SDQ affected 36.5% of the PD patients in our study. Of the participants selected by the SDQ, 94.7% presented changes in efficacy and safety in the V-VST and/or FEES. There was a high level of effect from changes in efficacy, with fractionated swallowing (89.5%) and plate-to-mouth transport (78.9%) as the most common. Alterations in safety were less frequent (57.9%), and the level of effects was lower, with food particles in the pharynx (52.7%) and laryngeal penetrations (31.6%) as the most common. Alterations in safety are linked to the risk of pneumonia due to aspiration and respiratory infections, whilst changes in efficacy are due to meal time duration. A final reflection may be that the professionals who work in Dysphagia Units must make a competent diagnosis and administer relevant treatment for SD in PD, in addition to
21 participating in training all other personnel who are treating these patients. An action plan protocol would need to be established to prevent any further serious complications such as malnutrition and pneumonia from aspiration.
Conflict of Interests The authors have no conflict of interests to declare.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.otoeng.2017.01.003.
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