Quantitative approach to analyze hyoid bone movement during swallowing by ultrasound: an integrative review

ABSTRACT Purpose To synthesize the scientific knowledge on which measurements of hyoid bone movement during swallowing are obtained by ultrasonography and how to extract these measures. Research strategies The PECO question and combinations of descriptors and keywords were formulated in the electronic databases Medline/PubMed, EMBASE, Web of Science, Scopus and Lilacs. Selection criteria Articles that used ultrasonography to analyze measurements of hyoid bone movement during swallowing were included, regardless of language, year of publication, or presence of deglutition disorders. Data analysis The included articles were analyzed for: year, study site, study design, population, sample size, equipment used, transducer positioning, measurements obtained, method of extraction, and reliability of measurements. Results Twenty-six articles met the eligibility criteria. The most frequent measurement was hyoid movement maximum amplitude, followed by time and velocity. There was great variability in the study population, equipment used, positioning of the transducer and method of extraction of the measurements. Thus, it was not possible to find a standard model to extract the measures. The level of reliability was investigated in only eight articles. Conclusion Amplitude, time and velocity are the measures of hyoid bone movement during swallowing that can be obtained by ultrasonography. There is no standardization on how to extract these measurements.


INTRODUCTION
In oropharyngeal dysphagia there are changes in deglutition performance that can compromise the efficiency and safety of food intake (1,2) , with the possibility of affecting nutritional status, causing pulmonary complications, dehydration, malnutrition and, in more severe cases, pneumonia and death (2) . One of the precursor factors for the mechanism of this function to occur properly is the elliptical movement of the hyoid bone from the contraction of the suprahyoid muscles that promotes both lifting and hyolaryngeal anteriorization (3,4) .
The movement of the hyoid bone has an important role in the pharyngeal phase of deglutition, as it supports the protection of the lower airways by collaborating for glottis adduction and lowering of the epiglottis cartilage during lifting, as well as assists in the relaxation of the pharyngoesophageal segment during anteriorization (4)(5)(6)(7)(8) . Changes in the spatiotemporal synchrony of hyoid bone movement during deglutition may contribute to the incidence of pharyngeal residue (change in efficiency) (5,6) and increased probability of inhalation (change in safety) (7) .
Therefore, in order to measure these clinical findings, studies present the importance of developing reliable quantitative methods to analyze the biomechanical events of deglutition (7,8) . These quantitative measures of hyoid bone movement during deglutition have already been widely used in diagnostic examinations such as Videofluoroscopic Swallowing Study (VFSS) (9)(10)(11)(12)(13) and Ultrasonography (USG) (6,8,14,15) Although VFSS is the instrumental method considered the reference standard because it allows the analysis of all deglutition phases, USG has been increasingly used as a complementary instrumental examination that allows the extraction of kinematic, temporal and interval measures related to the movement of the hyoid bone during deglutition (16) .
USG is a non-invasive procedure, without emission of ionizing radiation, which can be performed with patients in bed using real food without contrast (17,18) . This type of assessment can be used to estimate the efficiency of rehabilitation in individuals with dysphagia (19) and allows a quantitative frame-by-frame analysis of the movement of the hyoid bone during deglutition (20) . The acoustic shadow generated by the hyoid bone in the USG examination makes it possible to obtain measures related to the course of the hyoid bone during deglutition (21,22) , such as, for example, temporal (8,14) and amplitude measures (12,13,22,23) . In order for this quantitative approach to occur in a valid, reliable and reproducible way in the scientific and clinical environment, it is recommended to standardize the measures and the extraction method from the examination (24) .

OBJECTIVE
This study aims to summarize the situation of the scientific knowledge about which measures of hyoid bone movement during deglutition are obtained by ultrasonography and how to extract them.

RESEARCH STRATEGIES
This is an integrative literature review, so it was not necessary to submit it to the evaluation of the Ethics and Human Research Committee of the institution. The methodological procedures for this type of review were followed according to the steps recommended in the literature.
The research question was formulated following the acronym PECO, which represents the elements Population, Exposure, Comparison and Outcome, respectively. The element (P) corresponds to "adults with or without deglutition disorders"; the second element (E) corresponds to "ultrasonography examination"; the third element (C) was not applied in this review; and the fourth element (O) was the "measures of hyoid bone movement during deglutition obtained by ultrasonography and its extraction method". Thus, the research question was defined as: "What measures of hyoid bone movement during deglutition are obtained by ultrasonography and how are they extracted in adults with or without deglutition disorders?" The database search took place in April 2021 and included the electronic databases Medline/PubMed, EMBASE, Web of Science, Scopus and Lilacs, all widely recognized in the health area. Furthermore, an additional search was carried out in the bibliographic references of the selected articles. The search strategies were made through the combinations between keywords and descriptors from Medical Subjects Headings (MeSH) and Health Sciences Descriptors (DeCS) (Appendix 1).
References were managed and duplicate articles were removed with the help of the EndNote Web® software (Clarivate, Thompson Reuters, New York, NY, USA). All searches were conducted on May 12, 2021. The application Rayyan (Qatar Computing Research Institute) was used as a tool for archiving, organizing and selecting articles among reviewers.

SELECTION CRITERIA
For this review, the following inclusion criteria were applied: articles that used ultrasonography to analyze quantitative measures of hyoid bone movement during deglutition in adults aged 18 years or older, regardless of language, year of publication or presence of deglutition disorders. The following exclusion criteria were applied (1) : review articles, editorials, letters to the editor, conference annals, theses, and dissertations (2) ; articles that evaluated hyoid bone movement through strictly descriptive analyses (3) ; articles that included the adult and child population without separating the results by age group.

DATA ANALYSIS
The articles were selected by two researchers independently, who compared their analyses and when disagreements occurred, these were resolved by a third evaluator. After extracting the articles from the databases and filtering out the duplicates, it was followed to the screening by reading the titles and abstracts, excluding those that did not meet the inclusion criteria.
The remaining articles that met the eligibility criteria or that generated some doubts were submitted to the reading of the full text. The reference lists of the selected articles were consulted in search of studies that had not been previously collected.
The articles that met the eligibility criteria were submitted to the extraction of the following data: author, year and place of the study, study design, population, sample size, objective, device used, positioning of the ultrasonography transducer, measures related to the movement of the hyoid bone during deglutition, method of extraction of the measures and reliability/accuracy of the measures.

RESULTS
Using the aforementioned research strategies, 296 articles were located. After sorting by titles and abstracts, followed by reading the full text, the final sample consisted of 26 articles. This process is outlined in Figure 1.
The included studies were analyzed according to the data presented in the analysis matrix (Chart 1).

Submandibular area Time
The duration measures of each deglutition were made from a frameby-frame analysis of the videos, using a 10-second Sony video card. The time was measured from the moment the HB first moved anteriorly and superiorly from rest until its return to the stable rest position. The HB's movement was classified into four distinct phases and each phase was measured: from rest to anterior amplitude; time that the HB remained stable in the anterior amplitude; return to rest and total time.

Submandibular area Amplitude
The amplitude peak position was defined as the frame with the shortest distance between the acoustic shadow of the HB and the acoustic shadow of the mental spine of the mandible. The extent of movement of the HB was expressed as a percentage of the distance in amplitude since rest (rest distance between the mental spine of the mandible and the HB -maximum distance between the two structures) / rest distance between the two structures) × 100.

DISCUSSION
This review summarized which measures of hyoid bone movement during deglutition are obtained by USG in adults with or without dysphagia, as well as their extraction methods. It was possible to identify more studies measuring movement amplitude, followed by time and velocity. In addition, the lack of standardization of the methods for obtaining and analyzing these measures was evidenced.
The results showed that the use of USG to analyze measures of hyoid bone movement during deglutition has been increasingly recurrent over the decades, mainly in studies in the United States, although other countries also stand out. This finding indicates increased interest of researchers and clinicians in finding instruments that are still not widespread and that can add benefits to the management of patients with dysphagia. In addition, it is necessary to consider that this scenario is also influenced by the momentum of accelerated technological advances in the health area in recent years, which allows techniques, procedures, and instruments to be developed or improved to be incorporated into clinical and research practice.
Although these aspects are positive, this study showed that the use of USG to measure the movement of the hyoid bone during deglutition does not yet have standardized procedures. Although the use of USG with quantitative approach to evaluate deglutition-related aspects has been described since the 80s (35,36,39) , its transposition into clinical practice remains challenging, considering that it is not a procedure usually explored for this purpose in the training of professionals who work with dysphagia (24) .
As for the quantitative parameters investigated in the studies included in this review, the measures of time, velocity and amplitude of movement, especially the latter, stand out as the main outcomes of the ultrasonography examination. However, the equipment used and the methods for obtaining and analyzing the measures are still quite heterogeneous or described in an incipient way, which compromises reproducibility and makes it difficult to transpose the examination to the clinical context.
The heterogeneity of the equipment used, including transducers, is a characteristic that limits comparisons between studies, given that each device has a different visualization rate, matrix and frequency, which can impact the marking of structures of interest. Regarding the positioning of the transducer, it can be concluded that the laryngeal and submandibular areas were the most used, the latter being the most frequent. Although in the same area, the anatomical markers may be different and interfere with the result of the image that will be analyzed. It is noteworthy that among the few studies that estimated the reliability (12,14,20,23,27,40) , the highest levels were among those that positioned the transducer in the submandibular area. However, it is not possible to prove whether there is a direct relationship between transducer positioning and reliability only from the data in this review.
The measure of maximum amplitude achieved by the hyoid bone during deglutition was the most investigated, although the reference points for obtaining this measure have been different. In addition to markers in the structure of the hyoid bone itself or in the acoustic shadow generated by it in the ultrasonography image, the mandible (20,27,31,40) , the cervical vertebral body (44) and adjacent musculature were used (23,29,33,34) . Something that may explain the maximum amplitude being the most investigated measure is that it directly reflects how far the hyoid bone is able to move away from its resting point while the individual swallows. This data is traditionally considered relevant in the diagnosis of oropharyngeal dysphagia, as it is related to the integrity of the lower airways protection and clearance pharyngeal (3)(4)(5)(6)(7)(8) . In addition, among the measures found, amplitude is the simplest to be analyzed in operational terms, which may have favored its more frequent use.
With regard to temporal measures, it can be observed that the most investigated measure by the studies was the time interval between the beginning of the movement of the hyoid bone for deglutition until its maximum amplitude in the course (5,14,(25)(26)(27)(28)(29)(35)(36)(37)(38)(39)41,42) . It is worth highlighting this measure, because it is one of the indicators for the risk of penetration or inhalation (6) , since the decrease in amplitude time can compromise the movement of the epiglottis impairing the protection of the airway and, therefore, also hindering the opening of the pharyngoesophageal segment for passage of the food bolus (44) .
Most of the studies included were conducted with healthy individuals and investigated the measures regarding age, volume and consistency of the food bolus, since deglutition undergoes changes with advancing age (44) and it is relevant to analyze the interrelationships between kinematic parameters to understand how motor control strategies occur by adjusting the volume and consistency (29) .
The levels of reliability found, although acceptable, are not comparable between studies, since the methods are different. It is noteworthy that the analysis of ultrasonography images is perceptual-visual, requires training and most studies performed the markings and analyses with non-automated processes. All these aspects constitute biases for the inter-and intraevaluator reliability levels. In this review, we did not evaluate the outcomes of the measures, but we emphasize that they should be analyzed and interpreted considering the characteristics of the population studied.

CONCLUSION
The most investigated measure of hyoid bone movement during deglutition using ultrasonography is amplitude, followed by time and velocity. The method for extracting the measures is not standardized with regard to the equipment used, transducer positioning and image analysis procedures. 15 Web of Science (TS=(("deglutition" OR "deglutitions" OR "swallowing" OR "swallowings" OR "swallow" OR "swallows" OR "deglutition disorders" OR "deglutition disorder" OR "swallowing disorder" OR "swallowing disorders" OR "dysphagia") AND ("hyoid bone" OR "hyoid") AND ("ultrasonography" OR "diagnostic ultrasound" OR "ultrasound" OR "ultrasound imaging" OR "ultrasonic imaging" OR "medical sonography" OR "ultrasonographic imaging" OR "echography" OR "ultrasonic diagnoses" OR "ultrasonic diagnosis" OR "ultrasonics" OR "sonographic"))) 51 results

results
This is an Open Access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.   Articles that used ultrasonography to analyze measurements of hyoid bone movement during swallowing were included, regardless of language, year of publication, or presence of deglutition disorders. Data analysis: The included articles were analyzed for: year, study site, study design, population, sample size, equipment used, transducer positioning, measurements obtained, method of extraction, and reliability of measurements. Results: Twenty-six articles met the eligibility criteria. The most frequent measurement was hyoid movement maximum amplitude, followed by time and velocity. There was great variability in the study population, equipment used, positioning of the transducer and method of extraction of the measurements. Thus, it was not possible to find a standard model to extract the measures. The level of reliability was investigated in only eight articles. Conclusion: Amplitude, time and velocity are the measures of hyoid bone movement during swallowing that can be obtained by ultrasonography. There is no standardization on how to extract these measurements.