Protocols and assessment procedures in fiberoptic endoscopic evaluation of swallowing: an updated systematic review

Aline Prikladnicki Márcia Grassi Santana Maria Cristina Cardoso About the authors

Abstract

Introduction

Neurological alterations can generate swallowing disorders and fiberoptic endoscopic evaluation of swallowing is one of the tests performed for its diagnosis, as well as assistance in dysphagia management.

Objective

To identify and describe a fiberoptic endoscopic evaluation of swallowing standardized protocol for the neurological adult population and its stages.

Methods

Systematic review registered on the PROSPERO platform (CRD42018069428), carried out on the websites: MEDLINE, Cochrane Library and Scielo; published between 2009 and 2020. Randomized clinical trials, cross-sectional, and longitudinal studies were included. Two independent judges evaluated the study design and extracted the data from the selected studies. Doubts regarding inclusion or not of the studies were evaluated by a third judge. Scientific articles included were those with adult neurological remained patients with outcomes: (1) diagnosis of swallowing disorder (2) change in sensitivity in laryngeal region (3) penetration of food offered (4) aspiration of food offered.

Results

3724 articles were initially selected, after personalized search for patients with neurological alterations 101 studies remained. In the end, 21 qualitative studies from 2009 to 2020 remained in the systematic review and they were described in detail and compared. Seven articles used protocols of the institutions in which the research took place and four mentioned using the same protocol. The reliable reproducibility of the protocols is feasible only in three of the articles, even presenting different protocols.

Conclusion

There is no standard or validated protocol to assess the swallowing function of adults with neurological diseases.

Keywords
Swallowing disorders; Endoscopy; Speech-language and hearing science

Resumo

Introdução

As alterações neurológicas podem gerar distúrbios deglutitórios e a videoendoscopia da deglutição é um dos exames feitos para o seu diagnóstico e auxílio no manejo da disfagia.

Objetivo

Identificar e descrever o protocolo para videoendoscopia da deglutição padronizado para a população adulta com transtornos neurológicos e suas etapas.

Método

Revisão sistemática registrada na plataforma Prospero (CRD42018069428), realizada nos sites: Medline, Cochrane Library e Scielo; publicados entre 2009 e 2020. Foram incluídos ensaios clínicos randomizados, estudos transversais e longitudinais. Dois avaliadores independentes analisaram o delineamento do estudo e extrairam os dados dos estudos selecionados. As dúvidas de inclusão ou não dos estudos foram avaliadas por um terceiro avaliador. Artigos científicos incluídos englobam pacientes adultos neurológicos. Os desfechos avaliados: 1) diagnóstico de distúrbio deglutitório ou disfagia; (2) alteração de sensibilidade em região laríngea; (3) penetração laríngea do bolo alimentar ofertado; (4) aspiração traqueal do bolo alimentar ofertado.

Resultados

Foram selecionados inicialmente 3.724 artigos, após busca personalizada para pacientes com alterações neurológicas permaneceram 101 estudos. Ao final, 21 estudos qualitativos de 2009 a 2020 permaneceram na revisão sistemática e foram descritos detalhadamente e comparados. Sete estudos usaram protocolos das instituições promotoras e quatro citaram usar o mesmo protocolo. A reprodutibilidade fidedigna dos protocolos é viável apenas em três dos artigos, mesmo com protocolos diferentes.

Conclusões

Não há protocolo padronizado ou validado para avaliar a deglutição da população adulta neurológica.

Palavras-chave
Transtornos de deglutição; Endoscopia; Fonoaudiologia

Introduction

The fiberoptic endoscopic evaluation of swallowing (FEES) is one of the tests used to assess the function of swallowing and is currently considered a test already established to identify dysphagia in both children and adults. Described in 1988 by Langmore et al.11 Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2:216-9. in a scientific article, in 2001 FEES had its procedures detailed.22 Langmore S. Endoscopic evaluation and treatment of swallowing disorders. 1st ed. New York: Thieme; 2001. p. 263. A historical study on FEES has recently been published,33 Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32:27-38. describing the evolution of the procedures used to perform the test and its management in dysphagia, as well as some validations in specific populations.

Some published studies on FEES have focused on the validation of protocols for specific populations, such as extubated patients,44 Ajemian MS, Nirmul GB, Anderson MT, Zirlen DM, Kwasnik EM. Routine fiberoptic endoscopic evaluation of swallowing following prolonged intubation: implications for management. Arch Surg. 2001;136:434-7. head and neck cancer patients,55 Deutschmann MW, McDonough A, Dort JC, Dort E, Nakoneshny S, Mathews TW. Fiber-optic endoscopic evaluation of swallowing (FEES): predictor of swallowing-related complications in the head and neck cancer population. Head Neck. 2013;35:974-9. tracheostomized patients,66 Leder SB, Ross DA. Confirmation of no causal relationship between tracheotomy and aspiration status: a direct replication study. Dysphagia. 2010;25:35-9. vocal fold paralysis patients,77 Ollivere B, Duce K, Rowlands G, Harrison P, O’Reilley BJ. Swallowing dysfunction in patients with unilateral vocal fold paralysis: aetiology and outcomes. J Laryngol Otol. 2006;120:38-41. osteopathy,88 Seidler TO, Alvarez JCP, Wonneberger K, Hacki T. Dysphagia caused by ventral osteophytes of the cervical spine: clinical and radiographic findings. Eur Arch Otorhinolaryngol. 2009;266:285-91. and myasthenia gravis.99 Warnecke T, Teismann I, Zimmermann J, Oelenberg S, Ringelstein EB, Dziewas R. Fiberoptic endoscopic evaluation of swallowing with simultaneous Tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008;255:224-30. Other studies validated FEES protocols for specific neurological populations, however, not all studies described the protocol used and validated to be used in clinical practice or even to have its study replicated, in order to confirm the results in similar populations.

The focus on the use of FEES in populations of neurological etiology has some particularities, since the examination in the adult neurogenic population may be difficult due to factors such as: the cognitive aspect,1010 Castagna A, Ferrara L, Asnaghi E, Rega V, Fiorini G. Functional limitations, and cognitive impairment predict the outcome of dysphagia in older patients after an acute neurologic event. Neuro Rehabil. 2019;44:413-8.,1111 Tangalos EG, Petersen RC. Mild cognitive impairment in geriatrics. Clin Geriatr Med. 2018;34:563-89. trunk and head posture during the exam and the occurrence of fatigue,1212 Penner IK, Paul F. Fatigue as a symptom or comorbidity of neurological diseases. Nat Rev Neurol. 2017;13:662-75.

13 Siciliano M, Trojano L, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson’s disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23.
-1414 Farrugia ME, Di Marco M, Kersel D, Carmichael C. A physical and psychological approach to managing fatigue in myasthenia gravis: a pilot study. J Neuromuscul Dis. 2018;5:373-85. which requires the test interruption and makes the diagnosis and treatment plan difficult.

In general, the FEES assessment protocol is divided into three stages: the first is through careful observation of the anatomy, secretions, and visualization of the movements of the nasal structures when a patient is asked to speak and breathe. Some protocols include assessment of sensitivity in the oropharyngeal region by touching the endoscope in specific regions.1515 Aviv JE, Kim T, Sacco RL, Kaplan S, Goodhart K, Diamond B, et al. FEESST: a new bedside endoscopic test of the motor and sensory components of swallowing. Ann Otol Rhinol Laryngol. 1998;107:378-87.,1616 Kamarunas EE, McCullough GH, Guidry TJ, Mennemeier M, Schluterman K. Effects of topical nasal anesthetic on fiberoptic endoscopic examination of swallowing with sensory testing (FEESST). Dysphagia. 2014;29:33-43. The second stage consists of the direct evaluation of swallowing, offering food and liquids in different consistencies. The third stage consists of verifying postural maneuvers, variations in consistencies and observing eating behaviors, directly identifying postures and food consistencies that favor oral intake in a safer way.

Instrumental assessments to evaluate swallowing function have a gold standard in the FEES and in the videofluoroscopic swallowing study (VFSS).1717 Costa MM. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47:327-8.

VFSS is a test in which the swallowing process is observed from the time the bolus is captured, passing through all the swallowing phases (oral preparatory phase, oral phase, pharyngeal phase, and esophageal phase).1818 The Speech Pathology Association of Australia Limited. Clinical guideline videofluoroscopic swallow study; 2013. Therefore, this is an exam that determines the degree (mild, moderate, severe) of swallowing changes. In contrast, the FEES observes the pharyngeal phase of swallowing, however it has the advantage of identifying the exact location of the waste in that phase of swallowing, its quantity, and identifying which best maneuvers performs the partial or total cleaning of this residue. In addition, FEES, due to the fact that it does not use radiation, demonstrates greater ease of reproducibility and replicability, both in inpatients and outpatients. Focusing on the adult neurological population, in its evaluation and therapeutic follow-up, FEES is often indicated.1919 Madden C, Fenton J, Hughes J, Timon C. Comparison between videofluoroscopy and milk-swallow endoscopy in the assessment of swallowing function. Clin Otolaryngol Allied Sci. 2000;25:504-6.

Therefore, the use of a specific protocol by speech therapists and physicians during FEES performance facilitates the examination and the clinical diagnosis, offering evidence-based recommendations and reducing the rate of variation. The aim of this study is to identify and describe, based on a systematic review of the scientific literature, the FEES protocol to be used in the adult neurological population with details and the possibility of worldwide standardization.

Methods

A systematic review of the literature was carried out guided by the question: “Is there a protocol for performing FEES and, if so, is it validated to be used universally in patients with neurogenic diseases?”

This study was registered on PROSPERO (CRD42018069428). The databases searched were PubMed/Medline, Cochrane Library, Web of Science and SciELO. The main descriptors related to the investigated theme, crossed, were: FEES evaluation; adults; neurogenic disease; swallowing assessment, as shown in the strategies presented in Table 1. The outcome of each study was considered, that is: presence of a diagnosis of swallowing disorder; impaired laryngeal sensation (at the level of vocal folds); presence of laryngeal penetration of bolus; and/or occurrence of tracheal aspiration.

Table 1
Search strategies for the selected databases.

The review included cross-sectional studies, randomized clinical trials, and longitudinal cohort studies, which used FEES as a standard assessment instrument with neurogenic disease patients. Other types of studies or formats were excluded, as well as cross-sectional studies that included children and/or adolescents. The selection of articles covered the period between 2009 and 2019. The survey of bibliographic data took place between March 2018 and March 2020, based on the aforementioned inclusion criteria (Table 1).

The first phase of article selection was the exclusion of duplicate studies, followed by the reading and analysis of titles and abstracts of all identified works. Afterwards there was a complete reading of the selected studies, which led to the exclusion of works that did not meet the review criteria. The selected articles were submitted to methodological evaluation, according to the checklist provided by the report Strengthening the Reporting of Observational Studies in Epidemiology (STROBE)2020 Cuschieri S. The STROBE guidelines. Saudi J Anaesth. 2019;13:S31-4. for cross-sectional studies, which received a score of 1 when the item was considered, of 0 when not contemplated, and of 0.5 when partially contemplated. Afterwards, the averages between the scores assigned by the two evaluators were established. All phases were carried out by two of the authors/researchers, independently. Faced with doubts about whether or not to include the study, the third author/evaluator was called. This study included only articles with at least 70% of the score determined by the STROBE checklist. The arithmetic mean of study scores was 17.86, making up a proportion of 81% of the STROBE score. The included articles were analyzed regarding the possibility of bias, study limitations, number of participants, gender, age, and statistical method (Table 2). All review procedures presented here were conducted in accordance with Checklist Preferred Reporting Items for Systematic Reviews and Meta-Analyzes (Prisma).

Table 2
Average among blind evaluators of the published observational studies according to the Strobe tool.

Results

The selection of studies carried out by 2 independent evaluators in three databases, as described in the methodology, found a total of 3724 published studies based on the crossed descriptors “fiberoptic endoscopic evaluation of swallowing AND protocols of assessments” and “endoscopic swallowing assessment AND assessment procedures” .

Based on the personalized search and the inclusion of the descriptor “neurology”, aiming at studies performed with adult neurological population, 77 articles were selected on the PubMed platform, 14 in the Cochrane Library, 10 in Scielo, making a total of 101 articles. In search of article eligibility and from reading abstracts, articles that did not meet the inclusion criteria of the study were excluded, 28 articles remaining for full reading, which were analyzed by two blinded evaluators.

Finally, 21 studies published between 2009 and 2020, considered as updated publications, were selected because they were the only ones with complete FEES protocols described in the publications. The description of the search for the articles is shown in Fig. 1 based on PRISMA guidelines (Fig. 1).

Figure 1
Study search diagram according to Preferred Reporting Items for Systematic Reviews and Meta-Analyzes statement (PRISMA).

Of these, 18 studies are cross-sectional, 02 cross-sectional longitudinal and 01 application of a protocol developed through a cohort. The neurological diseases assessed in the selected studies were: progressive supranuclear palsy (PSP), amyotrophic lateral sclerosis (ALS), elderly patients hospitalized with some health condition, Parkinson’s disease (PD), stroke, myotonic dystrophy type 1 (DM1), myasthenia gravis (MG), elderly >60 years, traumatic brain injury (TBI), and vascular dementia. The description of the articles and the methodological characteristics of the articles are shown in Table 3.

Table 3
Analysis of selected studies.

The methodological evaluation of the studies using the STROBE report, by individual evaluation of two blinded and independent evaluators, and the hypothesis for this review found 21 studies which were selected for this systematic review, 5 of them with high score,2121 Mandysova P, Skvrňáková J, Ehler E, Cerný M. Development of the brief bedside dysphagia screening test in the Czech Republic. Nurs Health Sci. 2011;13:388-95.

22 Leder SB, Suiter DM, Agogo GO, Cooney LM Jr. An epidemiologic study on ageing and dysphagia in the acute care geriatrichospitalized population: a replication and continuation study. Dysphagia. 2016;31:619-25.

23 de Lima Alvarenga EH, Dall’Oglio GP, Murano EZ, Abrahão M. Continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443-9.

24 Braun T, Juenemann M, Viard M, Meyer M, Reuter I, Prosiegel M, et al. Adjustment of oral diet based on flexible endoscopic evaluation of swallowing (FEES) in acute stroke patients: a cross-sectional hospital-based registry study. BMC Neurol. 2019;19:282.
-2525 Suntrup-Krueger S, Schmidt S, Warnecke T, Steidl C, Muhle P, Schroeder JB, et al. Extubation readiness in critically ill stroke patients. Stroke. 2019;50:1981-8. and one highlighted due to its results and statistical analysis performed.2525 Suntrup-Krueger S, Schmidt S, Warnecke T, Steidl C, Muhle P, Schroeder JB, et al. Extubation readiness in critically ill stroke patients. Stroke. 2019;50:1981-8.

When verifying the risk of bias within studies, some studies have exposed their limitations and were found in Warnecke et al.2626 Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45. that to avoid the expectation bias, the FEES performed in the study were evaluated randomly by two independent judges; that is, out of the order in which the exams were performed. Alvarenga et al.2323 de Lima Alvarenga EH, Dall’Oglio GP, Murano EZ, Abrahão M. Continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443-9. reported as one of the limitations of the study a probable sample bias, since the patients who accepted it probably did so due to presenting swallowing symptoms. Braun et al.2424 Braun T, Juenemann M, Viard M, Meyer M, Reuter I, Prosiegel M, et al. Adjustment of oral diet based on flexible endoscopic evaluation of swallowing (FEES) in acute stroke patients: a cross-sectional hospital-based registry study. BMC Neurol. 2019;19:282. reported a possible selection bias when researching patients in the intensive care unit, demonstrating that the study sample was more severely affected. Suntrup-Krueger et al.2525 Suntrup-Krueger S, Schmidt S, Warnecke T, Steidl C, Muhle P, Schroeder JB, et al. Extubation readiness in critically ill stroke patients. Stroke. 2019;50:1981-8. pointed out limitations on possible biased results of the study due to the fact that in the intensive care unit there is a high knowledge of post-extubation dysphagia. Nienstedt et al.2727 Nienstedt JC, Buhmann C, Bihler M, Niessen A, Plaetke R, Gerloff C, et al. Drooling is no early sign of dysphagia in Parkinson’s disease. Neurogastroenterol Motil. 2018;30:e13259. and Pflug et al.2828 Pflug C, Bihler M, Emich K, Niessen A, Nienstedt JC, Flügel T, et al. Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. 2018;33:41-50. stated that they minimized selection bias and Warnecke et al.2929 Warnecke T, Ritter MA, Kroger B, Oelenberg S, Teismann I, Heuschmann PU, et al. Fiberoptic endoscopic Dysphagia severity scale predicts outcome after acute stroke. Cerebrovasc Dis. 2009;28:283-9. commented on a possible selection bias based on the inclusion and exclusion criteria of the study. Shapira-Galitz et al.3030 Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81. suggested a possibility of assessment bias at the time when the researchers needed to read the questionnaire for patients over the phone. D’Ottaviano et al.,3131 D’Ottaviano FG, Linhares Filho TA, Andrade HM, Alves PC, Rocha MS. Fiberoptic endoscopy evaluation of swallowing in patients with amyotrophic lateral sclerosis. Braz J Otorhinolaryngol. 2013;79:349-53. Leder et al.,2222 Leder SB, Suiter DM, Agogo GO, Cooney LM Jr. An epidemiologic study on ageing and dysphagia in the acute care geriatrichospitalized population: a replication and continuation study. Dysphagia. 2016;31:619-25. Mandysova et al.,2121 Mandysova P, Skvrňáková J, Ehler E, Cerný M. Development of the brief bedside dysphagia screening test in the Czech Republic. Nurs Health Sci. 2011;13:388-95. Marian et al.,3232 Marian T, Schröder J, Muhle P, Claus I, Oelenberg S, Hamacher C, et al. Measurement of oxygen desaturation is not useful for the detection of aspiration in dysphagic stroke patients. Cerebrovasc Dis Extra. 2017;7:44-50. Gozzer et al.,3333 Gozzer MM, Cola PC, Onofri SMM, Merola BN, Silva RGD. Fiberoptic endoscopic findings of oropharyngeal swallowing of different food consistencies in Amyotrophic Lateral Sclerosis. Achados videoendoscópicos da deglutição em diferentes consistências de alimento na Esclerose Lateral Amiotrófica. CoDAS. 2019;32:e20180216. Imaizumi et al.,3434 Imaizumi M, Suzuki T, Matsuzuka T, Murono S, Omori K. Low-risk assessment of swallowing impairment using flexible endoscopy without food or liquid. Laryngoscope. 2019;129:2249-52. Schröder et al.,3535 Schröder JB, Marian T, Claus I, Muhle P, Pawlowski M, Wiendl H, et al. Substance P saliva reduction predicts pharyngeal dysphagia in parkinson’s disease. Front Neurol. 2019;10:386. Pilz et al.,3636 Pilz W, Baijens LW, Passos VL, Verdonschot R, Wesseling F, Roodenburg N, et al. Swallowing assessment in myotonic dystrophy type 1 using fiberoptic endoscopic evaluation of swallowing (FEES). Neuromuscul Disord. 2014;24:1054-62. Somasundaram et al.,3737 Somasundaram S, Henke C, Neumann-Haefelin T, Isenmann S, Hattigen E, Lorenz MW, et al. Dysphagia risk assessment in acute left-hemispheric middle cerebral artery stroke. Cerebrovasc Dis. 2014;37:217-22. Souza et al.,3838 Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114. Souza et al.,3939 Souza GAD de, Silva RG da, Cola PC, Onofri Suely MM. Resíduos faríngeos nas disfagias orofaríngeas neurogênicas. CoDAS. 2019;31:e20180160. Umay et al.,4040 Umay EK, Karaahmet F, Gurcay E, Balli F, Ozturk E, Karaahmet O, et al. Dysphagia in myasthenia gravis: the tip of the Iceberg. Acta Neurol Belg. 2018;118:259-66. and Farneti et al.4141 Farneti D, Fattori B, Bastiani L. Time as a factor during endoscopic assessment of swallowing: relevance in defining the score and severity of swallowing disorders. Acta Otorhinolaryngol Ital. 2019;39:244-9. did not describe the bias assessment.

The number of patients evaluated in the selected studies ranged from 1 to 961, all of them being adults and or elderly, both men and women, and 6 of the studies carried out an evaluation in a control group compared to age matching.2525 Suntrup-Krueger S, Schmidt S, Warnecke T, Steidl C, Muhle P, Schroeder JB, et al. Extubation readiness in critically ill stroke patients. Stroke. 2019;50:1981-8.,2727 Nienstedt JC, Buhmann C, Bihler M, Niessen A, Plaetke R, Gerloff C, et al. Drooling is no early sign of dysphagia in Parkinson’s disease. Neurogastroenterol Motil. 2018;30:e13259.,2828 Pflug C, Bihler M, Emich K, Niessen A, Nienstedt JC, Flügel T, et al. Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. 2018;33:41-50.,3030 Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81.,3636 Pilz W, Baijens LW, Passos VL, Verdonschot R, Wesseling F, Roodenburg N, et al. Swallowing assessment in myotonic dystrophy type 1 using fiberoptic endoscopic evaluation of swallowing (FEES). Neuromuscul Disord. 2014;24:1054-62.,4040 Umay EK, Karaahmet F, Gurcay E, Balli F, Ozturk E, Karaahmet O, et al. Dysphagia in myasthenia gravis: the tip of the Iceberg. Acta Neurol Belg. 2018;118:259-66.

Among the protocols presented in the 21 studies, 7 of the articles used protocols from the institutions where the research was carried out or even protocols only detailed in the articles; 2 used the protocol by Dzeiwas et al.4242 Dziewas R, Warnecke T, Olenberg S, Teismann I, Zimmermann J, Kramer C, et al. Towards a basic endoscopic assessment of swallowing in acute stroke development and evaluation of a simple dysphagia score. Cerebrovasc Dis. 2008;26:41 7.; 2 studies used the Langmore protocol11 Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2:216-9.; 2 used the Langmore protocol4343 Langmore SE, Terpenning MS, Schork A, Chen Y, Murray JT, Lopatin D, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998:69-81.; 4 used the Langmore protocol22 Langmore S. Endoscopic evaluation and treatment of swallowing disorders. 1st ed. New York: Thieme; 2001. p. 263.; 1 article performed FEES evaluations with protocol by Warnecke et al.99 Warnecke T, Teismann I, Zimmermann J, Oelenberg S, Ringelstein EB, Dziewas R. Fiberoptic endoscopic evaluation of swallowing with simultaneous Tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008;255:224-30.; 1 study evaluated using the brief bedside dysphagia screening test2121 Mandysova P, Skvrňáková J, Ehler E, Cerný M. Development of the brief bedside dysphagia screening test in the Czech Republic. Nurs Health Sci. 2011;13:388-95.; 1 used the FEES levedopa-test2626 Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45.; and 1 performed evaluations without the use of food using the protocol by Hyodo et al.4444 Hyodo M, Nishikubo K, Hirose K. New scoring proposed for endoscopic swallowing evaluation and clinical significance [in Japanese]. Nihon Jibiinkoka Gakkai Kaiho. 2010;113:670-8. However, even though studies have mentioned the use of the same protocol to perform the FEES, in the description of the protocols, we observed differences in the chosen consistencies, foods and volumes, not characterizing the same protocol. The way in which FEES images were captured was not discussed in the articles, which is why it was not discussed in this systematic review.

Detailing the protocols, only 3 of the studies cited the international dysphagia diet standardization initiative (IDDSI)4545 ADA: American Dietetic Association. National dysphagia diet: standardization for optimal care. Chicago: ADA; 2002. as a basis for standardizing the food consistencies offered during the FEES of the studies, with thick and liquid consistencies being offered in these studies. One of the studies included the evaluation of liquid in addition to the other consistencies mentioned. Three of the articles presented better and more accurate details of the protocols used to perform FEES, Warnecke et al.,2626 Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45. Shapira-Galitz et al.3030 Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81. and Souza et al.3838 Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114., specifying the tested consistencies, declaring the foods that were used for each consistency, the quantity offered at each moment, and how many times each consistency was offered. Of the 21 studies, 11 mentioned having used food coloring to contrast the color of the food in relation to the structures, blue or green and possible secretions present during the exam.

Among the outcomes assessed by de Lima Alvarenga et al.,2323 de Lima Alvarenga EH, Dall’Oglio GP, Murano EZ, Abrahão M. Continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443-9. Gozzer et al.,3333 Gozzer MM, Cola PC, Onofri SMM, Merola BN, Silva RGD. Fiberoptic endoscopic findings of oropharyngeal swallowing of different food consistencies in Amyotrophic Lateral Sclerosis. Achados videoendoscópicos da deglutição em diferentes consistências de alimento na Esclerose Lateral Amiotrófica. CoDAS. 2019;32:e20180216. Souza et al.3838 Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114., and Souza et al.,3939 Souza GAD de, Silva RG da, Cola PC, Onofri Suely MM. Resíduos faríngeos nas disfagias orofaríngeas neurogênicas. CoDAS. 2019;31:e20180160. there were: posterior oral leakage, pharyngeal residues, laryngeal penetration, laryngotracheal aspiration, and laryngeal sensitivity. The study by Souza et al.3939 Souza GAD de, Silva RG da, Cola PC, Onofri Suely MM. Resíduos faríngeos nas disfagias orofaríngeas neurogênicas. CoDAS. 2019;31:e20180160. evaluated mainly residues, all of them according to each tested consistency. The studies by Warnecke et al.,99 Warnecke T, Teismann I, Zimmermann J, Oelenberg S, Ringelstein EB, Dziewas R. Fiberoptic endoscopic evaluation of swallowing with simultaneous Tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008;255:224-30. Warnecke et al.,2626 Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45. Marian et al.,3232 Marian T, Schröder J, Muhle P, Claus I, Oelenberg S, Hamacher C, et al. Measurement of oxygen desaturation is not useful for the detection of aspiration in dysphagic stroke patients. Cerebrovasc Dis Extra. 2017;7:44-50. and Braun et al.2424 Braun T, Juenemann M, Viard M, Meyer M, Reuter I, Prosiegel M, et al. Adjustment of oral diet based on flexible endoscopic evaluation of swallowing (FEES) in acute stroke patients: a cross-sectional hospital-based registry study. BMC Neurol. 2019;19:282. used the severity scale for dysphagia in their outcomes, the fiberoptic endoscopic dysphagia severity score (FEDSS).99 Warnecke T, Teismann I, Zimmermann J, Oelenberg S, Ringelstein EB, Dziewas R. Fiberoptic endoscopic evaluation of swallowing with simultaneous Tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008;255:224-30. As for the autonomy and capacity for oral intake based on the Functional Oral Intake Scale (FOIS), they were assessed as outcomes by Leder et al.,2222 Leder SB, Suiter DM, Agogo GO, Cooney LM Jr. An epidemiologic study on ageing and dysphagia in the acute care geriatrichospitalized population: a replication and continuation study. Dysphagia. 2016;31:619-25. Farneti et al.,4141 Farneti D, Fattori B, Bastiani L. Time as a factor during endoscopic assessment of swallowing: relevance in defining the score and severity of swallowing disorders. Acta Otorhinolaryngol Ital. 2019;39:244-9. Imaizumi et al.,3434 Imaizumi M, Suzuki T, Matsuzuka T, Murono S, Omori K. Low-risk assessment of swallowing impairment using flexible endoscopy without food or liquid. Laryngoscope. 2019;129:2249-52. and Shapira-Galitz et al.3030 Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81. In the study by Imaizumi et al.,3434 Imaizumi M, Suzuki T, Matsuzuka T, Murono S, Omori K. Low-risk assessment of swallowing impairment using flexible endoscopy without food or liquid. Laryngoscope. 2019;129:2249-52. the International Classification of Functionality was also used for the assessment. The detailed outcomes in each study separately are shown in Table 4.

Table 4
Prevalence and swallowing outcomes assessed and demonstrated by the selected studies.

Discussion

The objective of this systematic review of identifying a standardized and validated protocol for endoscopic evaluation of swallowing in patients with underlying neurogenic disease has not been achieved. All studies evaluated and selected for this study used described and detailed protocols, but none were validated. Mandysova et al.2121 Mandysova P, Skvrňáková J, Ehler E, Cerný M. Development of the brief bedside dysphagia screening test in the Czech Republic. Nurs Health Sci. 2011;13:388-95. developed a dysphagia screening test for bedside application and validated it based on FEES, but it is not a validated FEES protocol. Dziewas et al.4242 Dziewas R, Warnecke T, Olenberg S, Teismann I, Zimmermann J, Kramer C, et al. Towards a basic endoscopic assessment of swallowing in acute stroke development and evaluation of a simple dysphagia score. Cerebrovasc Dis. 2008;26:41 7. have been mentioned in some of the articles as a validated FEES protocol, however it is the development and validation of a new score for the assessment of dysphagia severity, which does not correspond to a validated FEES protocol for the neurological population. The Hyodo score4444 Hyodo M, Nishikubo K, Hirose K. New scoring proposed for endoscopic swallowing evaluation and clinical significance [in Japanese]. Nihon Jibiinkoka Gakkai Kaiho. 2010;113:670-8. was developed and validated to identify the presence and degree of dysphagia, indirectly, that is, without the use of liquids and food, only based on secretion management and intraoral sensitivity in neurological patients, consequently not characterizing a FEES protocol, but an evaluation score. As for all studies that cited the Langmore protocol, in different years of publication (1988, 1998, 2001) and updates, these are considered guidelines, as the author says in a recent 2017 article,33 Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32:27-38. requiring validation for different populations.

Regarding the protocols presented by the selected studies, 7 out of 21 studies used the consistency of pureed, liquid, and soft & bite sized, 6 of the studies used pureed, liquid and solid. The other studies used different consistencies, as an example of liquid and slightly thick only. Considering the existence of consistency standardization based on IDDSI, an international diet standardization initiative4545 ADA: American Dietetic Association. National dysphagia diet: standardization for optimal care. Chicago: ADA; 2002. since 2015 and updated in 2019, only Souza et al.,3838 Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114. Souza et al.,3939 Souza GAD de, Silva RG da, Cola PC, Onofri Suely MM. Resíduos faríngeos nas disfagias orofaríngeas neurogênicas. CoDAS. 2019;31:e20180160. and Gozzer et al.3333 Gozzer MM, Cola PC, Onofri SMM, Merola BN, Silva RGD. Fiberoptic endoscopic findings of oropharyngeal swallowing of different food consistencies in Amyotrophic Lateral Sclerosis. Achados videoendoscópicos da deglutição em diferentes consistências de alimento na Esclerose Lateral Amiotrófica. CoDAS. 2019;32:e20180216. used international validation. IDDSI favors the use of the same nomenclature worldwide, facilitating the standardization and validation of assessment protocols such as FEES for neurological populations, for example. However, 13 of the 21 studies were published after 2015, the year in which IDDSI was created and published, and did not use international standardization, making it difficult to validate a protocol.

The volumes presented in the study protocols were widely different, varying from studies testing all consistencies in 3, 5 and 10 mL, others testing only 10 mL three times and others identifying volumes as the size of the spoon offered, with the teaspoon being specified, to studies that did not specify volumes or number of offers or even the utensils used.

Some of the utensils used in some studies were straw, glass, but without specifying the size or even diameter of each utensil, making it difficult to understand the quantity offered to the study participant. Therefore, the use of spoons, straws or cups without specifying size and quantity cannot be characterized as a description of volumes, as there are different diameters and sizes for each of these utensils. Additionally, studies citing the same protocol in the description of the article used different consistencies and volumes, consequently not being the same protocol.

Finally, the presence of a speech therapist to provide food and guide the swallowing of patients during FEES alongside the doctor who performs endoscopy was mentioned in 11 of the 21 selected studies. It is clear that the evaluation of swallowing and its possible changes during FEES is of exclusive medical responsibility in Brazil, while the role of the speech therapist is to monitor the evaluation and verify the patient’s responses to body maneuvers for food. Teamwork is the gold standard for an accurate diagnosis and determination of the appropriate therapeutic plan for that patient.

Regarding the quality of the studies, even considering a high cut-off point, most studies were evaluated as good or satisfactory, making it difficult to consider any of these protocols for standardization and/or validation for FEES in the neurological population. However, three of these studies were the ones that best detailed their procedures and protocol for FEES evaluation.2626 Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45.,3030 Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81.,3838 Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114. Three studies brought all the items meticulously detailed since the tested consistencies, one of them using the IDDSI, the volumes offered in units of “mL” or “cc”, mentioned the use of food coloring to favor contrast in relation to the structures and secretions of the organism, food and liquids offered according to each consistency, how many times each one was offered, and which utensils were used to offer each consistency. The way in which FEES images were captured was not discussed in the articles, which is why they are not highlighted in this systematic review.

However, none of these protocols have been validated for the neurological population. The lack of a validated protocol makes it difficult to widely standardize the assessment and changes the therapeutic approach, since the entire rehabilitation is based on a detailed, accurate and reliable assessment. Adequate and correct diagnosis is the basis for any rehabilitation and management of dysphagia in adult patients with neurological disease.

The importance of having a standardized and validated protocol for neurological populations, including specific populations, is crucial because each neurological disease has its own particularities and pathophysiology, as well as the presentation of dysphagia. Dysphagia characteristics vary widely according to the neurological diagnosis. The literature details these differences regarding dysphagia in Parkinson’s disease,4646 Prosiegel M, Heintze M, Wagner-Sonntag E, Hannig C, Wuttge-Hannig A, Yassouridis A. Deglutition disorders in neurological patients. A prospective study of diagnosis, pattern of impairment, therapy and outcome. Der Nervenarzt. 2002;73:364-70. dysphagia in supranuclear progressive paralysis (PSP),4747 Clark HM, Stierwalt JAG, Tosakulwong N, Botha H, Ali F, Whitwell JL, et al. Dysphagia in progressive supranuclear palsy. Dysphagia. 2020;35:667-76. dysphagia in amyotrophic lateral sclerosis (ALS),4848 Jani MP, Gore GB. Swallowing characteristics in Amyotrophic Lateral Sclerosis. Neuro Rehabilitation. 2016;39:273-6. as well as dysphagia in traumatic brain injury (TBI),4949 Lee WK, Yeom J, Lee WH, Seo HG, Oh BM, Han TR. Characteristics of dysphagia in severe traumatic brain injury patients: a comparison with stroke patients. Ann Rehabil Med. 2016;40:432-9. among others.

Some of the limitations faced in this systematic review were the possible bias in evaluating the quality of the studies, due to the fact that one of the blinded evaluators was the same to account for the averages of the items and the final score and the non-use of the third evaluator in this phase of the study. In addition to the possible bias in the selection of studies, as we have delimited more recent research (from the last eleven years), we may have left out historically important research for this topic, although mentioned in the introduction and discussion.

The lack of a standardized and validated protocol for the adult population with neurogenic diseases significantly limits a detailed, accurate, and focused assessment of the possible swallowing difficulties faced by these patients. The clinical diagnosis of dysphagia may be underestimated or overestimated according to the protocol used and outcomes assessed. This systematic review, the first in the field, highlights the need to validate protocols with a focus on adults with underlying neurogenic diseases considering the characteristics of dysphagia and its pathophysiology. Adequate, reliable and accurate diagnosis is the basis for the management of swallowing in these populations.

Conclusion

The reliable reproducibility of the protocols is only feasible in three of the articles, even with different protocols, but none were standardized or validated for the adult neurological population.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - finance code 001.

  • Peer Review under the responsibility of Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico-Facial.

References

  • 1
    Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2:216-9.
  • 2
    Langmore S. Endoscopic evaluation and treatment of swallowing disorders. 1st ed. New York: Thieme; 2001. p. 263.
  • 3
    Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32:27-38.
  • 4
    Ajemian MS, Nirmul GB, Anderson MT, Zirlen DM, Kwasnik EM. Routine fiberoptic endoscopic evaluation of swallowing following prolonged intubation: implications for management. Arch Surg. 2001;136:434-7.
  • 5
    Deutschmann MW, McDonough A, Dort JC, Dort E, Nakoneshny S, Mathews TW. Fiber-optic endoscopic evaluation of swallowing (FEES): predictor of swallowing-related complications in the head and neck cancer population. Head Neck. 2013;35:974-9.
  • 6
    Leder SB, Ross DA. Confirmation of no causal relationship between tracheotomy and aspiration status: a direct replication study. Dysphagia. 2010;25:35-9.
  • 7
    Ollivere B, Duce K, Rowlands G, Harrison P, O’Reilley BJ. Swallowing dysfunction in patients with unilateral vocal fold paralysis: aetiology and outcomes. J Laryngol Otol. 2006;120:38-41.
  • 8
    Seidler TO, Alvarez JCP, Wonneberger K, Hacki T. Dysphagia caused by ventral osteophytes of the cervical spine: clinical and radiographic findings. Eur Arch Otorhinolaryngol. 2009;266:285-91.
  • 9
    Warnecke T, Teismann I, Zimmermann J, Oelenberg S, Ringelstein EB, Dziewas R. Fiberoptic endoscopic evaluation of swallowing with simultaneous Tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008;255:224-30.
  • 10
    Castagna A, Ferrara L, Asnaghi E, Rega V, Fiorini G. Functional limitations, and cognitive impairment predict the outcome of dysphagia in older patients after an acute neurologic event. Neuro Rehabil. 2019;44:413-8.
  • 11
    Tangalos EG, Petersen RC. Mild cognitive impairment in geriatrics. Clin Geriatr Med. 2018;34:563-89.
  • 12
    Penner IK, Paul F. Fatigue as a symptom or comorbidity of neurological diseases. Nat Rev Neurol. 2017;13:662-75.
  • 13
    Siciliano M, Trojano L, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson’s disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23.
  • 14
    Farrugia ME, Di Marco M, Kersel D, Carmichael C. A physical and psychological approach to managing fatigue in myasthenia gravis: a pilot study. J Neuromuscul Dis. 2018;5:373-85.
  • 15
    Aviv JE, Kim T, Sacco RL, Kaplan S, Goodhart K, Diamond B, et al. FEESST: a new bedside endoscopic test of the motor and sensory components of swallowing. Ann Otol Rhinol Laryngol. 1998;107:378-87.
  • 16
    Kamarunas EE, McCullough GH, Guidry TJ, Mennemeier M, Schluterman K. Effects of topical nasal anesthetic on fiberoptic endoscopic examination of swallowing with sensory testing (FEESST). Dysphagia. 2014;29:33-43.
  • 17
    Costa MM. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47:327-8.
  • 18
    The Speech Pathology Association of Australia Limited. Clinical guideline videofluoroscopic swallow study; 2013.
  • 19
    Madden C, Fenton J, Hughes J, Timon C. Comparison between videofluoroscopy and milk-swallow endoscopy in the assessment of swallowing function. Clin Otolaryngol Allied Sci. 2000;25:504-6.
  • 20
    Cuschieri S. The STROBE guidelines. Saudi J Anaesth. 2019;13:S31-4.
  • 21
    Mandysova P, Skvrňáková J, Ehler E, Cerný M. Development of the brief bedside dysphagia screening test in the Czech Republic. Nurs Health Sci. 2011;13:388-95.
  • 22
    Leder SB, Suiter DM, Agogo GO, Cooney LM Jr. An epidemiologic study on ageing and dysphagia in the acute care geriatrichospitalized population: a replication and continuation study. Dysphagia. 2016;31:619-25.
  • 23
    de Lima Alvarenga EH, Dall’Oglio GP, Murano EZ, Abrahão M. Continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443-9.
  • 24
    Braun T, Juenemann M, Viard M, Meyer M, Reuter I, Prosiegel M, et al. Adjustment of oral diet based on flexible endoscopic evaluation of swallowing (FEES) in acute stroke patients: a cross-sectional hospital-based registry study. BMC Neurol. 2019;19:282.
  • 25
    Suntrup-Krueger S, Schmidt S, Warnecke T, Steidl C, Muhle P, Schroeder JB, et al. Extubation readiness in critically ill stroke patients. Stroke. 2019;50:1981-8.
  • 26
    Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein EB, et al. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25:1239-45.
  • 27
    Nienstedt JC, Buhmann C, Bihler M, Niessen A, Plaetke R, Gerloff C, et al. Drooling is no early sign of dysphagia in Parkinson’s disease. Neurogastroenterol Motil. 2018;30:e13259.
  • 28
    Pflug C, Bihler M, Emich K, Niessen A, Nienstedt JC, Flügel T, et al. Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. 2018;33:41-50.
  • 29
    Warnecke T, Ritter MA, Kroger B, Oelenberg S, Teismann I, Heuschmann PU, et al. Fiberoptic endoscopic Dysphagia severity scale predicts outcome after acute stroke. Cerebrovasc Dis. 2009;28:283-9.
  • 30
    Shapira-Galitz Y, Yousovich R, Halperin D, Wolf M, Lahav Y, Drendel M. Does the Hebrew Eating Assessment Tool-10 correlate with pharyngeal residue, penetration and aspiration on fiberoptic endoscopic examination of swallowing? Dysphagia. 2019;34:372-81.
  • 31
    D’Ottaviano FG, Linhares Filho TA, Andrade HM, Alves PC, Rocha MS. Fiberoptic endoscopy evaluation of swallowing in patients with amyotrophic lateral sclerosis. Braz J Otorhinolaryngol. 2013;79:349-53.
  • 32
    Marian T, Schröder J, Muhle P, Claus I, Oelenberg S, Hamacher C, et al. Measurement of oxygen desaturation is not useful for the detection of aspiration in dysphagic stroke patients. Cerebrovasc Dis Extra. 2017;7:44-50.
  • 33
    Gozzer MM, Cola PC, Onofri SMM, Merola BN, Silva RGD. Fiberoptic endoscopic findings of oropharyngeal swallowing of different food consistencies in Amyotrophic Lateral Sclerosis. Achados videoendoscópicos da deglutição em diferentes consistências de alimento na Esclerose Lateral Amiotrófica. CoDAS. 2019;32:e20180216.
  • 34
    Imaizumi M, Suzuki T, Matsuzuka T, Murono S, Omori K. Low-risk assessment of swallowing impairment using flexible endoscopy without food or liquid. Laryngoscope. 2019;129:2249-52.
  • 35
    Schröder JB, Marian T, Claus I, Muhle P, Pawlowski M, Wiendl H, et al. Substance P saliva reduction predicts pharyngeal dysphagia in parkinson’s disease. Front Neurol. 2019;10:386.
  • 36
    Pilz W, Baijens LW, Passos VL, Verdonschot R, Wesseling F, Roodenburg N, et al. Swallowing assessment in myotonic dystrophy type 1 using fiberoptic endoscopic evaluation of swallowing (FEES). Neuromuscul Disord. 2014;24:1054-62.
  • 37
    Somasundaram S, Henke C, Neumann-Haefelin T, Isenmann S, Hattigen E, Lorenz MW, et al. Dysphagia risk assessment in acute left-hemispheric middle cerebral artery stroke. Cerebrovasc Dis. 2014;37:217-22.
  • 38
    Souza GAD de, Gozzer MM, Cola PC, Onofri SMM, Gonçalves da Silva R. Desempenho longitudinal da deglutição orofaríngea na distrofia miotônica tipo 1. Audiol Commun Res. 2019;24:e2114.
  • 39
    Souza GAD de, Silva RG da, Cola PC, Onofri Suely MM. Resíduos faríngeos nas disfagias orofaríngeas neurogênicas. CoDAS. 2019;31:e20180160.
  • 40
    Umay EK, Karaahmet F, Gurcay E, Balli F, Ozturk E, Karaahmet O, et al. Dysphagia in myasthenia gravis: the tip of the Iceberg. Acta Neurol Belg. 2018;118:259-66.
  • 41
    Farneti D, Fattori B, Bastiani L. Time as a factor during endoscopic assessment of swallowing: relevance in defining the score and severity of swallowing disorders. Acta Otorhinolaryngol Ital. 2019;39:244-9.
  • 42
    Dziewas R, Warnecke T, Olenberg S, Teismann I, Zimmermann J, Kramer C, et al. Towards a basic endoscopic assessment of swallowing in acute stroke development and evaluation of a simple dysphagia score. Cerebrovasc Dis. 2008;26:41 7.
  • 43
    Langmore SE, Terpenning MS, Schork A, Chen Y, Murray JT, Lopatin D, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998:69-81.
  • 44
    Hyodo M, Nishikubo K, Hirose K. New scoring proposed for endoscopic swallowing evaluation and clinical significance [in Japanese]. Nihon Jibiinkoka Gakkai Kaiho. 2010;113:670-8.
  • 45
    ADA: American Dietetic Association. National dysphagia diet: standardization for optimal care. Chicago: ADA; 2002.
  • 46
    Prosiegel M, Heintze M, Wagner-Sonntag E, Hannig C, Wuttge-Hannig A, Yassouridis A. Deglutition disorders in neurological patients. A prospective study of diagnosis, pattern of impairment, therapy and outcome. Der Nervenarzt. 2002;73:364-70.
  • 47
    Clark HM, Stierwalt JAG, Tosakulwong N, Botha H, Ali F, Whitwell JL, et al. Dysphagia in progressive supranuclear palsy. Dysphagia. 2020;35:667-76.
  • 48
    Jani MP, Gore GB. Swallowing characteristics in Amyotrophic Lateral Sclerosis. Neuro Rehabilitation. 2016;39:273-6.
  • 49
    Lee WK, Yeom J, Lee WH, Seo HG, Oh BM, Han TR. Characteristics of dysphagia in severe traumatic brain injury patients: a comparison with stroke patients. Ann Rehabil Med. 2016;40:432-9.

Publication Dates

  • Publication in this collection
    27 June 2022
  • Date of issue
    May-Jun 2022

History

  • Received
    30 Sept 2020
  • Accepted
    05 Mar 2021
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