Para os parâmetros de avaliação da deglutição foi utilizado o questionário de risco de disfagia, Eating Assessment Tool-10 (EAT-10) (63), versão traduzida e validada para o português brasileiro (64), a avaliação instrumental da deglutição por meio do protocolo Measurement Tool of Swallowing Impairment - MBSImp (60) e classificação da deglutição de acordo com o Dysphagia Outcome and Severity Scale (DOSS) (68) e Penetration-Aspiration Scale (PAS) (69).
a) Eating Assessment Tool-10 (EAT-10)
O questionário EAT-10 apresenta um escore que pode variar de 0 á 40 pontos, de modo que é considerado risco para disfagia pontuações iguais ou superiores a três. A pontuação do EAT-10 não foi considerada como critério de exclusão (64).
b) Avaliação instrumental da deglutição
O exame foi realizado em uma sala de raio-x, foi utilizado o equipamento radiológico Shimadzu Lexa Vision ( Figura 10).
Para avaliação foi utilizado o protocolo de avaliação videofluoroscópica,
Measurement Tool of Swallowing Impairment - MBSImp (60). A avaliação
videofluoroscópica é considerada padrão ouro para a avaliação da deglutição (44), ela é relevante pois permite a visualização de toda a passagem do bolo alimentar em relação aos movimentos das estruturas do trato aerodigestivo. Permite a detecção da aspiração e auxilia na identificação e no tratamento e compensações das alterações fisiológicas que levam ao processo de aspiração (Figura 11) (21, 70).
Prévio ao início da avaliação, foi realizado o preparo das consistências, com contraste de sulfato de bário, da marca Bariogel 100% 1g/ml, adicionado a água, nas seguintes porcentagens: Líquido fino, nível 1 – 70% de sulfato de bário e 30% água; Néctar (levemente engrossado, nível 2) – 50% sulfato de bário e 50% água; Mel (moderadamente engrossado, nível 3) – 100% sulfato de bário; Pudim(extremamente engrossado, nível 4) – 20ml de bário e uma medida de espessante alimentar a base de amido da marca Thick & Easy; Sólido – bolacha de leite maltado com sulfato de bário. As nomenclaturas descritas foram utilizadas apenas nomear as consistências preparadas e se basearam na American Dietetic Association (2002)(71) e no International
Dysphagia Diet Standardisation Initiative (IDDSI)(72).
O exame foi realizado em duas partes, a primeira parte era realizada em vista lateral, em que são ofertadas as seguintes consistências e volumes: Líquido fino, nível 1 (5ml, duas ofertas de livre volume, 1 gole controlado e 3 goles contínuos), líquido espessado néctar, nível 2 (5ml, goles controlados e goles contínuos), líquido espessado mel, nível 3 (5ml), consistência pudim, nível 4 (5ml), sólido (bolacha). A segunda parte, realizada na vista ântero-posterior, na qual eram ofertadas apenas as consistências: líquido espessado néctar (5ml) e consistência pudim (5ml) (Figura 12). Ao evidenciar risco para alguma consistência, não era ofertada a consistência em maior volume. Conforme recomendado pelo protocolo, o tempo máximo do exame foi de 5 minutos, o que diminuiu o tempo de exposição do participante à radiação.
Figura 11. Figura ilustrativa sobre a avaliação videofluoroscópica (Foto: Martin- Harris et. al. 2008 (60)
O protocolo de avaliação videofluoroscópica é constituído por 17 componentes: vedamento labial (1), controle de língua/bolo alimentar (2), preparação do bolo/mastigação (3), transporte do bolo/mobilidade de língua (4), resíduo oral (5), início da deglutição faríngea (6), elevação do palato mole (7), elevação laríngea (8), excursão anterior do hióide (9), movimento de epiglote (10), fechamento laríngeo e vestibular (11), movimento faríngeo de remoção (12), contração faríngea (13), abertura do esfíncter esofágico superior (14), retração da base da língua (15), resíduo faríngeo (16) e limpeza esofágica (17). Cada componente é avaliado em uma escala que varia de 0-4, 0- 3 ou 0-2, de modo que zero, indica a ausência de alterações e as escalas mais altas, 4, 3 e 2, indicam maior alteração da deglutição. Ao final, não existe um escore total, pois os componentes são separados em grupos, sendo eles, componentes orais (1-6), faríngeos (7-16) e esofágicos (17)(60). Para o presente estudo foram considerados para análise os componentes 8, 9, 14, 15 e os escores referentes aos componentes orais (escore oral) e faríngeos (escore faríngeo).
Para a gravação audiovisual dos exames de videofluoroscopia o computador foi acoplado ao monitor do raio-X (equipamento Shimadzu 120Kv e 800mA), e a captura digital foi realizada por meio do software Pinnacle Studio Video Editing e foi utilizado como protocolo padrão para gravação das imagens, 30 frames por segundo (Figura 13).
Figura 12. Exame de videofluoroscopia em vista lateral e antero-posterior. (Foto: Martin-Harris et. al. 2008)(60)
Os exames digitalizados foram arquivados em sistema online privado para análise, com identificação do participante pelas iniciais e número de registro no Hospital das Clínicas da UNICAMP. Ao final da avaliação, o participante e seu acompanhante recebiam uma devolutiva e orientações em relação à alimentação, necessidade de uso de manobras compensatórias ou outras estratégias para minimizar riscos e, caso haja necessidade, era realizado encaminhamento para outros serviços. A análise do protocolo de videofluoroscopia foi realizada por uma fonoaudióloga com certificação MBSImP Clinician1, que não tinha acesso aos dados da avaliação clínica dos participantes ou informações a respeito de seus antecedentes clínicos. Para a análise foi realizada a visualização frame a frame e atribuição dos códigos numéricos (magnitude das alterações) ocorreu conforme o protocolo padronizado, sendo considerados sempre os piores escores de avaliação (60).
c) Classificação da deglutição
Para classificação da deglutição foram utilizadas as escalas: Penetration-
Aspiration Scale (PAS)(69) e a Dysphagia Outcome and Severity Scale (DOSS)(68). A
1 Ou seja, “fonoaudiólogas que concluíram os requisitos do MBSImP Online Training and Confiability Testing. Esses clínicos são treinados para avaliar os resultados do estudo Modified Bary Swallow Study usando o protocolo MBSImP baseado em evidências e padronizado. O MBSImP fornece um protocolo para identificar e quantificar especificamente e quantificar deficiências de deglutição, que permite a introdução de tratamentos específicos e baseados em evidências de deglutição”. Disponível em: https://www.mbsimp.com/clinicians.cfm
Figura 13. Software e computador para gravação dos exames de videofluroscopia. (Foto: arquivo pessoal)
PAS é uma escala formada por 8 níveis para descrever os eventos associados a penetração e aspiração durante a avaliação instrumental da deglutição. O escore é determinado pelo nível em que o conteúdo entra em região de vias aéreas e se o conteúdo é eliminado ou não. Para efeito de esclarecimento, penetração é definido como a entrada de alimentos ou líquido em região de vias aéreas, acima do nível das pregas vocais, já a aspiração é definida como a entrada deste conteúdo na região de vias aéreas, abaixo do nível de pregas vocais(21).
A DOSS(68) é uma escala de severidade de disfagia, formada por 7 níveis, que classifica o grau de disfagia em deglutição normal, deglutição dentro dos limites funcionais, disfagia discreta, discreta/moderada, moderada, moderada/grave e grave.
Análise estatística dos dados
Os dados foram tabulados no Microsoft Excel (Microsoft Windows 10), em seguida eles foram encaminhados para análise, na qual foi utilizado o software estatístico The SAS System for Windows (Statistical Analysis System, versão 9.4. SAS Institute Inc, 2002-2008, Cary, NC, USA e o software IBM SPSS Statistics 24. A análise estatística descritiva foi apresentada através da média, mínimo e máximo.
De acordo com os resultados da avaliação instrumental da deglutição, as escalas utilizadas e o tamanho amostral, para análise das variáveis categóricas, foi optado por classificar os participantes com nível 5 (68) como o grupo de deglutição alterada e o os participantes com níveis 6 e 7 (68) agrupados, como o grupo de deglutição normal.
Para a escala PAS (69) a maioria dos participantes apresentaram nível 1, sem penetração ou nível 2 com penetração sem resíduo e apenas um participante apresentou nível 3, no qual há penetração com resíduo, por se tratar de um outlier, para efeito de análise, esse participante foi excluído da amostra para que pudesse ser estabelecida uma comparação entre as variáveis referentes aos participantes com nível 1 e 2 da escala PAS (69).
Para as variáveis contínuas, idade, parâmetros de sarcopenia (SARC-F, FPP e CP), parâmetros de pressão de língua (Pmáx anterior e posterior) e parâmetros de deglutição (EAT-10, escore oral e faríngeo) foi utilizado o teste Mann-Whitney e foi estabelecido o nível de significância P-valor ≤ 0,05.
Para as variáveis categóricas, escalas DOSS e PAS foi utilizado o teste exato de Fisher e estabelecido o nível de significância P-valor ≤ 0,05.
RESULTADOS
Artigo 1
Este artigo de revisão sistemática, foi submetido para a revista Archives of Gerontology and Geriatrics em Dezembro de 2019, ele já foi corrigido pela revista e agora está em fase de ajustes para nova submissão e provável publicação.
Relationship between sarcopenia and risk for dysphagia in older adults: Systematic review of observational studies
Aline Lustosa Pinto de Oliveira, Natália Conessa Ortega, Déborah Cristina de Oliveira, Lucia Figueiredo Mourão
Abstract
Background: The ageing process may lead to loss of muscle mass, strength and function which may affect individual’s capacity to swallow. The relationship between sarcopenia and risk of oropharyngeal dysphagia (OD) has been investigated in older adults with neurological conditions and cancer, however little is known about the link between sarcopenia and dysphagia in older adults without such conditions. Aim: This study aimed to explore the relationship between sarcopenia and risk for dysphagia in older adults without neuromotor-related diseases and cancer. Method: A systematic review was conducted using online databases (PubMed, EMBASE, Scopus, Web of Science and Cochrane). Observational studies and in peer-reviewed journals were included. Eligible papers were reviewed by two researchers, a quality assessment was conducted. Results: Six cross-sectional studies were included. In two studies, higher risk for sarcopenia predicted higher risk for dysphagia (OR=10.386, CI:1.115-96.718; OR=2.738, CI: 1.116-6.466) and three found significant positive correlation between sarcopenia and risk for dysphagia (p=0.04; p=0.001; p=0.001). One study found that low tongue strength predicted higher risk for sarcopenia and dysphagia (OR=0.92, CI=0.87-0.98). Conclusion: All the included studies identified significant relationships between sarcopenia and higher risk for OD in older adults. Further research should be conducted to confirm this relationship, as well as to check whether tongue strength could be used as a clinical parameter to establish the relationship between sarcopenia and OD. Health professionals should consider early intervention for older adults with
sarcopenia as these individuals might be at a higher risk for OD dysphagia and its complications.
Keywords
Oropharyngeal Dysphagia; Sarcopenia; Older adults; Aging; Systematic review; Observational studies
Introduction
Physiological changes arising from the natural ageing process may lead to a substantial loss of muscle mass, strength and function as well as to a delay and weakening of the muscle sensorial responses in whole body.[1] Swallowing depends on the strength and mobility of the tong, velopharyngeal sealing, laryngeal elevation, laryngeal vestibule closure, pharyngeal contraction and opening of the upper oesophageal sphincter.[2] Each of these functions depends on muscles like tongue, geniohyoid and thyrohyoid as well as others involved with the contraction and relaxation of the diaphragm muscle (e.g. suprahyoid, infrahyoid, pharyngeal and laryngeal muscles). The loss of muscle mass, strength and functioning associated with ageing can therefore affect the skeletal musculature involved with swallowing leading to oropharyngeal dysphagia (OD).[3] Older adults with oropharyngeal dysphagia are more likely to have negative health outcomes, such as pneumonia and undernutrition.[4] Some studies have been conducted investigating the link between changes in muscle health and risk for oropharyngeal dysphagia in older adults with chronic conditions which are likely to lead to oropharyngeal dysphagia, such as neuromotor-related diseases and some types of cancer.[5,6] However, the relationship between sarcopenia and oropharyngeal
link have been widely discussed without clear definitions about the link between both.[3]
Sarcopenia is a progressive and generalised skeletal muscle impairment characterised by adverse muscle changes such as low levels of muscle strength, low muscle quality/quantity, and reduction of physical performance.[7] According to the most up to date recommended criteria for sarcopenia, there is a probable sarcopenia when low muscle strength is detected.[7] The sarcopenia diagnostic is confirmed by the presence of low muscle quantity or quality.[7]
Studies have shown that sarcopenia is common in ‘healthy’ older adults and increases with age and up to approximately 33% of those aged 65 and over meet the sarcopenia criteria.[7,8] In addition, studies have found sarcopenia to be a risk factor for oropharyngeal dysphagia in individuals with various chronic conditions.[5,6] Given the likely occurrence of dysphagia in individuals with sarcopenia, some researchers have used the term ‘sarcopenic dysphagia’ to characterise cases of dysphagia which are probably caused by a generalised loss of strength in the muscles involved in swallowing.[9,10]
The majority of studies investigating sarcopenia and risk for oropharyngeal dysphagia have been conducted with people with neuromotor-related conditions (e.g. dementia, Parkinson’s disease, stroke) and some types of cancer[5,6,11] which are known to be direct risk factors for sarcopenia[12] and/or dysphagia.[13] Indeed, a previous systematic review about the link between sarcopenia and oropharyngeal dysphagia in individuals with various chronic conditions (e.g. Parkinson’s disease, stroke, dementia) has established a positive correlation between sarcopenia and oropharyngeal dysphagia.[11] However, the current paucity of research in older adults without such conditions may hinder the establishment of the independent relationship between
sarcopenia and oropharyngeal dysphagia. Therefore, this systematic review aimed to investigate the relationship between sarcopenia and risk for oropharyngeal dysphagia in individuals without neuromotor-related diseases and cancer.
Method
This systematic review was conducted in February 2019 and was reported in line with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA).[14]
Eligibility criteria
Inclusion criteria: Quantitative observational studies (e.g. cross-sectional, cohort
studies) investigating the link between sarcopenia and risk of oropharyngeal dysphagia in people aged 60 and over were eligible. These had to be in peer-reviewed journals, from inception up to when the search was conducted (February 2019). The studies needed to have used validated measures to establish sarcopenia and risk for oropharyngeal dysphagia. [7,15]
Exclusion criteria: We excluded studies that involved people with conditions that are
likely to directly affect the muscle health and swallowing, such as dementia, Parkinson’s disease, stroke, cancer, obstructive pulmonary disease and heart failure. Studies that measured nutrition and body mass index only, without specifying the sarcopenia criteria adopted, were excluded.
Search strategy
Searches were conducted in health-related electronic databases (Pubmed, EMBASE, Scopus, Web of Science and Cochrane). The search strategy was adapted according to the requirements of each database and included the following keywords/combinations: ("Deglutition Disorders" OR "Deglutition Disorder" OR "Disorders, Deglutition" OR "Swallowing Disorders" OR "Swallowing Disorder" OR Dysphagia OR "Oropharyngeal Dysphagia" OR "Dysphagia, Oropharyngeal") AND (Sarcopenia OR Sarcopenias) AND ("Muscular Atrophy" OR "Atrophies, Muscular" OR "Atrophy, Muscular" OR "Muscular Atrophies" OR "Atrophy, Muscle" OR "Atrophies, Muscle" OR "Muscle Atrophies" OR "Muscle Atrophy") OR “Loss of muscle mass” AND (Aging OR Senescence OR "Biological Aging" OR "Aging, Biological").
Study selection
The study selection process is detailed in Figure 1. First, all the identified studies (n=252) were exported to Endnote® so that duplicates (n=49) could be removed. Then, two authors (initials removed for blinded review) independently screened all the titles and abstracts, in line with the eligibility criteria, using the Rayyan® software. A total of 161 papers was excluded in this process. The remaining papers (n=42) were read in full by the two authors independently in order to check for eligibility. In case of disagreement regarding the inclusion of any study, a third reviewer was contacted (initials removed for blinded review) for discussion.
Thirty seven papers were excluded because they had samples of people with neurological conditions (n=7) or cancer (n=6); did not use validated measures to assess the risk for dysphagia (n=5), sarcopenia (n=4) or both (n=1); non-relevant study design, such as literature reviews (n=10); included people aged <60 years old (n=1); did not measure the relationship between sarcopenia and risk of dysphagia (n=1); or the full text was not written in English (n=1). Another relevant study was found through handsearching in PubMed and was included in the review, totalling six included studies.
Quality appraisal
The quality appraisal was conducted by two researchers independently (initials removed
for blinded review), in line with the eight criteria proposed by Loney et al[16]. Each of
the items set by the criteria is classified as; Y(yes), if the item was reported; N (no, if the item was not reported); or NC (not clear), if the information was not clearly reported. Any disagreement regarding the quality rating was resolved upon discussion with the help of a third assessor (initials removed for blinded review). Each item classified as ‘Y’ corresponds to one point, and ‘N’ or NC’ correspond to zero. The total scores can range from zero to eight, with eight indicating better methodological quality.
Data synthesis
The included studies (n=6) were read in full and relevant data were extracted. These included authorship, publication year, objectives, sample characteristics, methods and key findings. A narrative approach was used to describe and discuss the main findings.
Results
Study characteristics
The main characteristics of the included studies are given in Table 1. Sample sizes ranged from 104[9] to 245,[17] with a mean of 173 people enrolled in each study. All the studies were conducted in Asia; five from Japan and one from South Korea.[18] All the studies were cross-sectional; four investigated the relationship between sarcopenia and risk for oropharyngeal dysphagia,[9,18,19,20] and three evaluated the correlation between tongue strength, sarcopenia and risk for oropharyngeal dysphagia.[9,17,21] One study involved older adults living in care homes,[20] another included those living at home,[18] and four were conducted at hospitals.[9,17,19,21] Reasons for hospitalization included infectious and gastric illnesses, low-risk and emergency surgeries due to orthopaedic, respiratory or cardiological conditions. However, the authors affirmed in their papers that none of the individuals had the conditions listed as part of our exclusion criteria.
<Insert Table 1 here>
Quality assessment
Table 2 shows that all the six studies scored three out of eight in their methodological quality.[9,17,18,19,20,21] All the studies used a cross-sectional design, some of them hypothesized that sarcopenia would lead to a higher risk for oropharyngeal dysphagia. Those assessing tongue strength hypothesised that lower tongue strength would be significantly correlated with a higher risk for both oropharyngeal dysphagia and
sarcopenia. Whilst only two studies[17,18] described their sample size calculations, all of them used validated measures.
<Insert Table 2 here>
Measurement tools
Oropharyngeal dysphagia
Five studies evaluated risk for oropharyngeal dysphagia using screening tools, such as Eating Assessment Tool 10 (EAT-10),[21] Water Swallow Test (WST),[17,21] Standardized Swallowing Assessment (SSA)[18] and Repetitive Saliva Swallow Test (RSST)[18] (Table 1). One study conducted a clinical assessment of swallowing (e.g. observing participants’ eating behaviour, physical tests, cervical auscultation, pulse oximetry and anamneses with patients, family members and multidisciplinary teams).[19] Two studies classified dysphagia severity using the Dysphagia Severity Scale (DSS)[19,20] and three used the Functional Oral Intake Scale (FOIS).[9,17,21] The study from Shiozu et. al.[20] also assessed the position and distance of the thyroid cartilage, geniohyoid in relation to the sternum bone, neck circumference and the maximum phonation time.
Sarcopenia
Most of the studies used the European sarcopenic criteria[9,15,17,19,20] and just one used the Asian sarcopenic criteria.[18,22] In all the studies, sarcopenia was assessed using grip strength and physical performance (Table 1). Four studies used anthropometric measures, such as calf circumference (CC)[17,19,20,21] and tricipital fold, muscle area and arm circumference[9,21]. One study assessed the skeletal muscle
mass using the Dual-energy X-ray absorptiometry (DXA)[18], and one study used the bioelectrical impedance analysis (BIA)[20]. In most studies, physical performance was assessed using the Barthel Index (BI), with only two studies using other measures such as Gait Speed[20], Functional Independence Measure[20], and long-distance walk.[18] In most of the studies, nutritional state was assessed using the Mini-Nutritional Assessment Tool-Short Form,[9,17,19,20,21] Controlling Nutritional Status[9,21], Body Mass Index[9,17,19,20,21] and measure of serum albumin.[9,17]
Tongue strength was measured in three studies[9,17,21] using the same method (JMS, Hiroshima, Japan). Participants were asked to place a bulb, which was connected to the machine through a plastic tube, behind their incisive central teeth and to press it as strong as they could. The participants’ tongue strength was based on the mean score of the three measures,[9] or on the highest pressure detected in the three measurement attempts.[17,21]
Relationship between sarcopenia and risk for oropharyngeal dysphagia
As shown in Table 1, more older adults with sarcopenia had oropharyngeal dysphagia in one study[20] and more older adults with oropharyngeal dysphagia had sarcopenia in two studies.[9,20]A signifcantpositive relationship was found between sarcopenia and oropharyngeal dysphagia in to studies .[9,18]
Relationship between tongue strength, sarcopenia and risk for oropharyngeal dysphagia
As shown in Table 1, three studies investigated the relationship between tongue strength, sarcopenia and oropharyngeal dysphagia,[9,17,21] two of which found a
positive relationship between the three variables.[17,21] Only one study found a negative correlation between tongue strength and sarcopenia.[9]
Relationship tongue strength, sarcopenia, risk for oropharyngeal dysphagia and further nutritional assessments
Except for a single study,[18] all the remaining five studies conducted further nutritional assessments. Two of them found a positive (though weak) association