Abstract
Purpose To identify how the deglutition function has been evaluated using ultrasound (US).
Research strategy This literature review used the PubMed database to survey international scientific publications about US and its use to evaluate deglutition. Studies were located and selected by surveying relevant articles published between January 2002 and August 2013. The survey was limited to studies on humans published in English.
Selection criteria Repeated studies (determined by overlapping keywords), case studies, literature reviews, letters to the editor and studies not directly related to the topic were excluded.
Results A total of 17 studies matching the inclusion criteria were identified. More than half of the studies evaluated the deglutition of healthy adults with no preference for gender. The parameters adopted for image analysis were not unanimous, and there was considerable variation among studies.
Conclusion US proved to be a fast, non-invasive, low-cost method for evaluating objective parameters of deglutition. As a further advantage, US may be performed at bedside because the equipment is typically easy to handle and transport.
Ultrasonography; Ultrasonics; Deglutition; Deglutition disorders; Evaluation
Resumo
Objetivo Identificar como a função da deglutição tem sido avaliada por meio da ultrassonografia (USG).
Estratégia de pesquisa Esta revisão da literatura levantou publicações científicas internacionais sobre a USG e seu uso na avaliação da deglutição, por meio da base de dados PubMed. Foi realizada a localização e seleção dos estudos através de levantamento de textos publicados sobre o assunto, no período de janeiro de 2002 a agosto de 2013, limitando-se a estudos em seres humanos, no idioma inglês.
Critérios de seleção Foram excluídos aqueles repetidos por sobreposição das palavras-chave, estudos de caso, revisões de literatura, cartas ao editor e os não relacionados diretamente à temática.
Resultados Foram identificados 17 estudos que corresponderam aos critérios de inclusão. Observou-se que mais da metade dos estudos avaliou a deglutição de indivíduos adultos saudáveis, sem preferência por nenhum dos gêneros. Os parâmetros adotados para a análise das imagens não foram unânimes, havendo variação considerável entre os estudos.
Conclusão A USG da deglutição demonstrou ser um método rápido, não invasivo, de baixo custo, que fornece parâmetros objetivos sobre a deglutição e que pode ser realizado em beira de leito, uma vez que o equipamento costuma ser de fácil manuseio e transporte.
Ultrassonografia; Ultrassom; Deglutição; Transtornos de deglutição; Avaliação
INTRODUCTION
Ultrasound (US) involves placing a transducer on the body part being examined to transform the echoes reflected by the human body into signals that are electronically decoded to form an image(1). US is a noninvasive examination that provides dynamic images that focus on the soft tissues and body structures(2). The technique is widely applied in clinical practice because of its low cost, safety, speed and lack of radiation(3).
US is a viable option for studying the oral and pharyngeal structures involved in deglutition(2,3). Some advantages related to its use include the possibility of using food under regular conditions without the presence of contrasts and/or dyes and the portability of the device, which allows the test to be performed at bedside(2).
The structures and variables most often analyzed in deglutition studies are the amount and duration of hyoid bone elevation; glottal closure (frequency, latency, response and duration); the amplitude and speed of the vertical movement of the tongue; the total duration of deglutition; the mobility and function of the phonoarticulatory organs during deglutition; the distance between the hyoid bone and the larynx during deglutition; and the laryngeal elevation (beginning, peak and duration)(3,4).
The literature describes the use of US during deglutition in both healthy and sick individuals for organ analysis or for diagnosing dysphagia(2,5). US can also be performed in patients of different age groups and is considered a noninvasive, accurate method for visualizing bolus movement in the pharyngeal phase of deglutition during infant feeding(6).
PURPOSE
The present study aimed to determine how US has been used to assess deglutition based on refereed literature.
RESEARCH STRATEGY
To establish the search method, the precepts of the Cochrane Handbook(7) were followed.
The studies were located and selected by surveying articles on the subject published between August 2002 and August 2013. The articles were selected from the PubMed database and were limited to studies performed on humans and published in English. The following descriptors were used: “Ultrasound and Deglutition”, “Ultrasound and Deglutition Disorders”, “Ultrasound Diagnosis and Deglutition”, “Ultrasound Diagnosis and Deglutition Disorders”, “Ultrasonography and Deglutition”, “Ultrasonography and Deglutition Disorders”, “Ultrasonography Diagnosis and Deglutition”, “Ultrasonography Diagnosis and Deglutition Disorders”.
SELECTION CRITERIA
The database searches were performed independently by the researchers to minimize the possible loss of citations and to analyze the relevance of each retrieved citation for selection and inclusion in the study. Citations in languages other than English were excluded, as were those that contained overlapping keywords. Among the full articles obtained, case studies, literature reviews, letters to the editor and those not directly related to the topic were excluded. Articles that were effectively related to the research proposal were analyzed. The researchers conducted all stages of the study independently; when disagreements occurred, only articles with consensual final agreement were included. By its nature, this study was not single-blind (Figure 1).
The rationale for the exclusion of 279 citations is provided in Table 1.
DATA ANALYSIS
The 17 citations selected were critically evaluated in terms of their objectives; number, gender and ages of the participants; criteria and evaluation methods; results; and conclusions.
Regarding the criteria and evaluation methods, we sought to assess and describe the methods used in the articles to determine whether there was homogeneity among them.
Regarding the results and conclusions, in addition to the general information the articles provided in these sections, we also noted the advantages and disadvantages of the techniques discussed in each study.
RESULTS
The results of the study are briefly described in Chart 1.
DISCUSSION
After analyzing the selected articles, we observed that the studies that used US to assess deglutition could be divided into three groups: studies that investigated the deglutition of healthy individuals (52.9%)(2,3,6,8-13); studies that compared the deglutition of diseased individuals and their healthy controls(14,15-19) (i.e., those with craniofacial abnormalities(14) [16.7%], stroke(15,18,19) [50%] and neurogenic dysphagia(16,17) [33.3%]) to that of healthy controls (35.3%)(14,15-19); and studies that investigated deglutition in two specific diseases(5,20) (11.8%): nephropathic cystinosis and amyotrophic lateral sclerosis.
Regarding the participants’ gender, most of the studies included individuals of both genders (82.3%)(2,3,5,8-11,13,15-20). Only one study included only male subjects(12) (5.9%).
The age of the participants varied considerably among the studies. Most of the studies(5,15-19) included adult and elderly subjects (35.2%). Some of the studies(3,9,10) divided the adults into different age groups (17.6%), and others(8,12) examined adults of a particular age group (11.8%). Studies involving children and infants were the minority(2,6,11,13,20) (29.41%).
The parameters evaluated during the US examination were not unanimous. In seven studies(2,3,9,10,12,15,16) (41.1%), the lifting motion of the hyoid bone during deglutition was assessed, and in four of those studies(3,9,10,12), the duration of hyoid movement was also considered. Four studies(8,13,14,17) evaluated tongue movements during deglutition (23.5%), and the others assessed different parameters: mobility and functionality of the phonoarticulatory organs during deglutition(5) (5.9%); duration of deglutition and apnea(6) (5.9%); glottal closure and its characteristics (frequency, response latency and duration)(11) (5.9%); movement of the lateral wall of the pharynx(18) (5.9%); movement of the hyoid bone and tongue thickness(19) (5.9%); and tongue and hyoid bone movements during deglutition(20) (5.9%).
For a better discussion of the studies’ methods, results and conclusions, the articles were grouped according to the parameters considered for the assessment, as described above.
In studies that assessed the movement of the hyoid bone - elevation and/or duration - the overall objective was to correlate the movement of the hyoid bone with the participant’s age, gender and clinical status. A longer mean duration of hyoid bone elevation was observed with increasing age, as was decreased peak elevation of the hyoid bone(3). A study conducted with children found that gender may affect hyoid bone elevation - the mean movement was significantly greater in females(2). Regarding the participant’s clinical condition, the hyoid bone movement was significantly greater in healthy subjects compared with individuals with neurogenic dysphagia(15,16).
All of the studies that assessed the hyoid bone movement found that US could quantitatively and reliably evaluate this parameter.
Among the studies that assessed tongue movement during deglutition, two subgroups could be defined. The first subgroup aimed to determine the extent of intrapersonal variability in the duration of tongue movements during deglutition. The results indicated high intrapersonal variability in both healthy individuals and individuals with neurogenic dysphagia; however, greater variability in the duration of the transport phase was observed in the dysphagic group(17). The second subgroup(13,14) investigated US modes using tongue movement as the parameter of interest. High intra- and/or interpersonal variability was also found in this parameter, and it was observed that M-mode US provided better information about tongue movement during deglutition.
For all of the studies in this group, US provided information about tongue movements during deglutition without any side effects, and it was considered a useful tool. It should be noted that most of the studies concluded that this parameter exhibits high intra- and interpersonal variability, which can often complicate data analysis, as described by Galen and Jost-Brinkmann (2010)(14).
The other parameters were only investigated in single studies. Thus, the conclusions regarding the use of US and its results apply to only one study per parameter.
One of the studies investigated the mobility and function of the phonoarticulatory organs during deglutition. The authors sought to determine the role of US in the diagnostic evaluation of dysphagia in patients with amyotrophic lateral sclerosis (ALS). The exam was conducted concurrently with deglutition videofluoroscopy (VDF), and the study found that US provided static and dynamic functionality data for the oropharyngeal phase of deglutition more efficiently than VDF. Thus, the authors concluded that US should be used as a complement to VDF because it provides a precise description of the oral deglutition phase(5).
Using deglutition apnea as parameter, one study evaluated the ability of US to identify deglutition apnea in infants(6). The study involved the concomitant use of US and respiratory plethysmography and showed that the passage of the bolus during pharyngeal deglutition in a nursing child can be recorded using US, regardless of the respiration phase. Deglutition US was correlated with deglutition apnea detected with respiratory inductive plethysmography. Both techniques, when combined, have the potential to provide useful information about children who have nursing difficulties.
A study conducted in healthy newborns used the parameter glottal closure to investigate the concomitant use of esophageal manometry and glottis US. It found that glottal adduction during basal or adaptive deglutition occurs in any respiratory phase, thus ensuring protection of the airways against aspiration before or during deglutition. The methods used in this assessment allowed the study of glottis movement during deglutition, and it was concluded that investigation of the pharyngeal-glottal relationship using non-invasive methods, such as US, may be acceptable for and applicable to all ages(11).
One study examined the duration of the pharyngeal phase of deglutition based on the tongue and hyoid bone movements needed to start and finish deglutition. For this purpose, US was used to assess the deglutition of 101 patients with nephropathic cystinosis. The authors found that oral motor dysfunction of deglutition in patients with cystinosis increases progressively with age and is correlated with generalized muscular dysfunction but not with disease severity. Based on cross-sectional data, the dysfunction increased with increasing age and the number of years without cysteamine treatment(20).
A study conducted with healthy subjects and stroke patients used the displacement and duration of pharyngeal movement during deglutition as a parameter. The patients were subdivided into two groups: the first (Group A) consisted of patients who presented with penetration and/or aspiration of food, indicated through VDF, and the second (Group B) consisted of patients with no VDF findings. The mean pharyngeal displacement of Groups A and B was significantly lower compared with that of healthy individuals, while the mean duration of pharyngeal movement of Groups A and B was longer than that of healthy individuals. In conclusion, the study indicated that the use of US to analyze pharyngeal movement may help to quantify pharyngeal function and can serve as a complementary method for the anatomical evaluation of the pharyngeal phase in patients with stroke and dysphagia(18).
Another study analyzed the hyoid bone movement and tongue thickness. These parameters were compared between healthy individuals and stroke patients with and without the use of an alternative feeding route. The study found significantly less hyoid bone displacement and tongue thickness in patients fed exclusively by an alternate route compared with stroke patients with oral ingestion. No significant differences in either variable were observed between the control group and the stroke patients with oral ingestion(19).
Generally, all of the articles assessed found that deglutition US was a fast, noninvasive, low-cost method that provides objective information about parameters of deglutition and can be performed at bedside because the equipment is usually easy to handle and transport. Equally important, the authors of the examined studies all concluded that deglutition assessment with US has some inherent disadvantages, including the following: the pressure exerted by the transducer on the examined structure, transducer positioning and the lack of precise anatomical markers for some of the structures being investigated. Because of these limitations, although US was effective for the initial diagnosis of impaired deglutition, it should be used in conjunction with other exams that complement the assessment of phonoarticulatory organ function during deglutition to accurately diagnose dysphagia.
CONCLUSION
The heterogeneity of the studies showed that different groups and pathologies can be assessed with US; however, the methodological variability of the included studies hinders the definition and generalization of the patterns found.
The present review found that US examination is effective for assessing the components involved in the dynamics of deglutition, especially the oral and early pharyngeal phases, such as phonoarticulatory organ function, deglutition apnea duration, glottal closure and its aspects, and hyoid bone movement. However, US should not replace other examinations that assist in the assessment of the pharyngeal and esophageal phase and in dysphagia diagnosis because US cannot identify some dynamic components of function, such as food stasis in the pharynx. Thus, US has been used as a complement to VDF, plethysmography, surface electromyography (EMG), deglutition videoendoscopy and manometry to provide more reliable parameters of the oral phase and the beginning of the pharyngeal phase of deglutition.
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