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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.

Keywords:
Deglutition; Deglutition Disorders; Ultrasonography; Hyoid Bone; Movement

RESUMO

Objetivo

Sintetizar o estado do conhecimento científico sobre quais medidas do movimento do osso hioide durante a deglutição são obtidas pela ultrassonografia e como extraí-las.

Estratégia de pesquisa

A pergunta PECO e as combinações de descritores e palavras-chave foram formuladas nas bases de dados eletrônicas Medline/PubMed, EMBASE, Web of Science, Scopus and Lilacs.

Critérios de seleção

Foram incluídos os artigos que utilizaram a ultrassonografia para analisar as medidas de movimento do osso hioide durante a deglutição, independentemente do idioma, ano de publicação ou presença de alteração na deglutição.

Análise dos dados

Os artigos incluídos foram analisados quanto: ano, local do estudo, desenho do estudo, população, tamanho da amostra, equipamento utilizado, posicionamento do transdutor, medidas obtidas, método de extração e confiabilidade das medidas.

Resultados

Vinte e seis artigos cumpriram os critérios de elegibilidade. A medida mais frequente foi a de amplitude máxima do movimento, seguida de tempo e velocidade. Houve grande variabilidade quanto à população de estudo, equipamentos utilizados, posicionamento do transdutor e método de extração das medidas, não sendo possível estabelecer padronização. O nível de confiabilidade foi investigado em apenas oito artigos.

Conclusão

Amplitude, tempo e velocidade são as medidas do movimento do osso hioide durante a deglutição que podem ser obtidas por ultrassonografia. Não há padronização dos métodos de extração dessas medidas.

Descritores:
Deglutição; Transtornos de Deglutição; Ultrassonografia; Osso Hioide; Movimento

INTRODUCTION

In oropharyngeal dysphagia there are changes in deglutition performance that can compromise the efficiency and safety of food intake(11 Real CS, Balbinot J, Signorini AV, Hübner LS, de Castro Machado G, Dornelles S. Characterization of posterior leakage in swallowing. CoDAS. 2020;32(4):e20190072. PMid:32049105.,22 Crary MA, Groher ME. Reinstituting oral feeding in tube-fed adult patients with dysphagia. Nutr Clin Pract. 2006;21(6):576-86. http://dx.doi.org/10.1177/0115426506021006576. PMid:17119164.
http://dx.doi.org/10.1177/01154265060210...
), with the possibility of affecting nutritional status, causing pulmonary complications, dehydration, malnutrition and, in more severe cases, pneumonia and death(22 Crary MA, Groher ME. Reinstituting oral feeding in tube-fed adult patients with dysphagia. Nutr Clin Pract. 2006;21(6):576-86. http://dx.doi.org/10.1177/0115426506021006576. PMid:17119164.
http://dx.doi.org/10.1177/01154265060210...
). 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(33 Pearson WG Jr, Langmore SE, Zumwalt AC. Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid. Dysphagia. 2011;26(4):345-51. http://dx.doi.org/10.1007/s00455-010-9315-z. PMid:21069388.
http://dx.doi.org/10.1007/s00455-010-931...
,44 Steele CM, Bailey GL, Chau T, Molfenter SM, Oshalla M, Waito AA, et al. The relationship between hyoid and laryngeal displacement and swallowing impairment. Clin Otolaryngol. 2011;36(1):30-6. http://dx.doi.org/10.1111/j.1749-4486.2010.02219.x. PMid:21414151.
http://dx.doi.org/10.1111/j.1749-4486.20...
).

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(44 Steele CM, Bailey GL, Chau T, Molfenter SM, Oshalla M, Waito AA, et al. The relationship between hyoid and laryngeal displacement and swallowing impairment. Clin Otolaryngol. 2011;36(1):30-6. http://dx.doi.org/10.1111/j.1749-4486.2010.02219.x. PMid:21414151.
http://dx.doi.org/10.1111/j.1749-4486.20...

5 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....

6 Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90-5. http://dx.doi.org/10.1007/BF00714593. PMid:8005013.
http://dx.doi.org/10.1007/BF00714593...

7 Ishida R, Palmer J, Hiiemae K. Hyoid motion during swallowing: factors affecting forward and upward displacement. Dysphagia. 2002;17(4):262-7. http://dx.doi.org/10.1007/s00455-002-0064-5. PMid:12355141.
http://dx.doi.org/10.1007/s00455-002-006...
-88 Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274-9. http://dx.doi.org/10.1007/s00455-007-9135-y. PMid:17962998.
http://dx.doi.org/10.1007/s00455-007-913...
). Changes in the spatiotemporal synchrony of hyoid bone movement during deglutition may contribute to the incidence of pharyngeal residue (change in efficiency)(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,66 Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90-5. http://dx.doi.org/10.1007/BF00714593. PMid:8005013.
http://dx.doi.org/10.1007/BF00714593...
) and increased probability of inhalation (change in safety)(77 Ishida R, Palmer J, Hiiemae K. Hyoid motion during swallowing: factors affecting forward and upward displacement. Dysphagia. 2002;17(4):262-7. http://dx.doi.org/10.1007/s00455-002-0064-5. PMid:12355141.
http://dx.doi.org/10.1007/s00455-002-006...
).

Therefore, in order to measure these clinical findings, studies present the importance of developing reliable quantitative methods to analyze the biomechanical events of deglutition(77 Ishida R, Palmer J, Hiiemae K. Hyoid motion during swallowing: factors affecting forward and upward displacement. Dysphagia. 2002;17(4):262-7. http://dx.doi.org/10.1007/s00455-002-0064-5. PMid:12355141.
http://dx.doi.org/10.1007/s00455-002-006...
,88 Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274-9. http://dx.doi.org/10.1007/s00455-007-9135-y. PMid:17962998.
http://dx.doi.org/10.1007/s00455-007-913...
). These quantitative measures of hyoid bone movement during deglutition have already been widely used in diagnostic examinations such as Videofluoroscopic Swallowing Study (VFSS)(99 Zhang Z, Coyle JL, Sejdić E. Automatic hyoid bone detection in fluoroscopic images using deep learning. Sci Rep. 2018;8(1):12310. http://dx.doi.org/10.1038/s41598-018-30182-6. PMid:30120314.
http://dx.doi.org/10.1038/s41598-018-301...

10 Nagy A, Molfenter SM, Péladeau-Pigeon M, Stokely S, Steele CM. The effect of bolus consistency on hyoid velocity in healthy swallowing. Dysphagia. 2015;30(4):445-51. http://dx.doi.org/10.1007/s00455-015-9621-6. PMid:26048615.
http://dx.doi.org/10.1007/s00455-015-962...

11 Garmendia Merino G, Bascuñana Ambrós H. The importance of the quantification of hyoid displacement in the evaluation of the score and evolution of oropharyngeal dysphagia. Acta Otorrinolaringol Esp (Engl Ed). 2019;70(6):327-35. http://dx.doi.org/10.1016/j.otoeng.2018.08.002. PMid:30686483.
http://dx.doi.org/10.1016/j.otoeng.2018....

12 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
-1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
) and Ultrasonography (USG)(66 Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90-5. http://dx.doi.org/10.1007/BF00714593. PMid:8005013.
http://dx.doi.org/10.1007/BF00714593...
,88 Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274-9. http://dx.doi.org/10.1007/s00455-007-9135-y. PMid:17962998.
http://dx.doi.org/10.1007/s00455-007-913...
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,1515 Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids. Dysphagia. 2014;29(2):269-76. http://dx.doi.org/10.1007/s00455-013-9506-5. PMid:24445381.
http://dx.doi.org/10.1007/s00455-013-950...
) 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(1616 Ahn SY, Cho KH, Beom J, Park DJ, Jee S, Nam JH. Reliability of ultrasound evaluation of hyoid-larynx approximation with positional change. Ultrasound Med Biol. 2015;41(5):1221-5. http://dx.doi.org/10.1016/j.ultrasmedbio.2014.12.010. PMid:25616584.
http://dx.doi.org/10.1016/j.ultrasmedbio...
).

USG is a non-invasive procedure, without emission of ionizing radiation, which can be performed with patients in bed using real food without contrast(1717 Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonographic evaluation of hyoid-larynx approximation in dysphagic stroke patients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006. PMid:19427098.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,1818 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...
). This type of assessment can be used to estimate the efficiency of rehabilitation in individuals with dysphagia(1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
) and allows a quantitative frame-by-frame analysis of the movement of the hyoid bone during deglutition(2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
). 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(2121 Kuhl V, Eicke BM, Dieterich M, Urban PP. Sonographic analysis of laryngeal elevation during swallowing. J Neurol. 2003;250(3):333-7. http://dx.doi.org/10.1007/s00415-003-1007-2. PMid:12638025.
http://dx.doi.org/10.1007/s00415-003-100...
,2222 Lynch CS, Chammas MC, Mansur LL, Cerri GG. Biomecânica ultra-sonográfica da deglutição: estudo preliminar. Radiol Bras. 2008;41(4):241-4. http://dx.doi.org/10.1590/S0100-39842008000400008.
http://dx.doi.org/10.1590/S0100-39842008...
), such as, for example, temporal (88 Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274-9. http://dx.doi.org/10.1007/s00455-007-9135-y. PMid:17962998.
http://dx.doi.org/10.1007/s00455-007-913...
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
) and amplitude measures(1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,2222 Lynch CS, Chammas MC, Mansur LL, Cerri GG. Biomecânica ultra-sonográfica da deglutição: estudo preliminar. Radiol Bras. 2008;41(4):241-4. http://dx.doi.org/10.1590/S0100-39842008000400008.
http://dx.doi.org/10.1590/S0100-39842008...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
). 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(2424 Allen JE, Clunie G, Ma JK, Coffey M, Winiker K, Richmond S, et al. Translating ultrasound into clinical practice for the assessment of swallowing and laryngeal function: a speech and language pathology-led consensus study. Dysphagia. 2022;37(6):1586. http://dx.doi.org/10.1007/s00455-022-10413-9. PMid:35201387.
http://dx.doi.org/10.1007/s00455-022-104...
).

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 Appendix 1 Search strategies used in databases Databases Descriptors Results Pubmed/Medline ((“deglutition”[MeSH Terms] OR “deglutition”[All Fields] OR “deglutitions”[All Fields] OR “swallowing”[All Fields] OR “swallowings”[All Fields] OR “swallow”[All Fields] OR “swallows”[All Fields] OR “deglutition disorders”[MeSH Terms] OR “deglutition disorders”[All Fields] OR “deglutition disorder”[All Fields] OR “swallowing disorder”[All Fields] OR “swallowing disorders”[All Fields] OR “dysphagia”[All Fields]) AND (“hyoid bone”[MeSH Terms] OR “hyoid”[All Fields]) AND (“ultrasonography”[MeSH Terms] OR “ultrasonography”[All Fields] OR “diagnostic ultrasound”[All Fields] OR “ultrasound”[All Fields] OR “ultrasounds”[All Fields] OR “ultrasound imaging”[All Fields] OR “ultrasonic imaging”[All Fields] OR “medical sonography”[All Fields] OR “ultrasonographic imaging”[All Fields] OR “echography”[All Fields] OR “ultrasonic diagnoses”[All Fields] OR “ultrasonic diagnosis”[All Fields] OR “ultrasonics”[All Fields] OR “sonographic”[All Fields])) 61 results EMBASE (‘dysphagia’/exp OR ‘swallowing’/exp) AND (‘echography’/exp OR ‘ultrasound’/exp) AND (‘hyoid bone’/exp) 98 results 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 Scopus (TITLE-ABS-KEY (deglutition OR deglutitions OR swallowing OR swallowingsOR swallow OR swallows OR “deglutition AND disorders” OR “deglutition AND disorder” OR “swallowing AND disorder” OR “swallowing AND disorders” OR dysphagia) AND TITLE-ABS-KEY (“hyoid AND bone” OR “hyoid” ) AND TITLE-ABS-KEY (ultrasonography OR “diagnostic AND ultrasound” OR ultrasound OR ultrasounds)) 78 results LILACS (deglutition OR “deglutition disorders” OR deglutição OR deglución OR “transtornos de deglutição” OR “trastornos de deglución” OR “troubles de la deglutition” OR deglutition) AND (“hyoid bone” OR “osso hioide” OR “hueso hioides” OR “os hyoide”) AND (Ultrasonography OR ultrasonografía OR échographie OR ultrassonografia) 8 results Caption: ICC: intraclass correlation coefficient; HB: hyoid bone; USG: ultrasonograph ).

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(11 Real CS, Balbinot J, Signorini AV, Hübner LS, de Castro Machado G, Dornelles S. Characterization of posterior leakage in swallowing. CoDAS. 2020;32(4):e20190072. PMid:32049105.): review articles, editorials, letters to the editor, conference annals, theses, and dissertations(22 Crary MA, Groher ME. Reinstituting oral feeding in tube-fed adult patients with dysphagia. Nutr Clin Pract. 2006;21(6):576-86. http://dx.doi.org/10.1177/0115426506021006576. PMid:17119164.
http://dx.doi.org/10.1177/01154265060210...
); articles that evaluated hyoid bone movement through strictly descriptive analyses(33 Pearson WG Jr, Langmore SE, Zumwalt AC. Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid. Dysphagia. 2011;26(4):345-51. http://dx.doi.org/10.1007/s00455-010-9315-z. PMid:21069388.
http://dx.doi.org/10.1007/s00455-010-931...
); 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.

Figure 1
Flowchart of article selection

The included studies were analyzed according to the data presented in the analysis matrix (Chart 1).

Chart 1
Analysis matrix of studies that used ultrasonography to evaluate measures of hyoid bone movement during deglutition

Among the publications included, two(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...
) were classified as a case-control, one(2626 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...
) as cohort and 23(1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....

13 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
-1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.

28 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...

29 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...

30 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...

31 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of submental ultrasonographic evaluation for dysphagia patients. Ann Rehabil Med. 2016;40(2):197-205. http://dx.doi.org/10.5535/arm.2016.40.2.197. PMid:27152268.
http://dx.doi.org/10.5535/arm.2016.40.2....

32 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...

33 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...

34 Rocha SG, Silva RG, Berti LC. Qualitative and quantitative ultrasound analysis of oropharyngeal swallowing. CoDAS. 2015;27(5):437-45. http://dx.doi.org/10.1590/2317-1782/20152015015. PMid:26648214.
http://dx.doi.org/10.1590/2317-1782/2015...

35 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...

36 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...

37 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...

38 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...

39 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...

40 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...

41 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...

42 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
-4343 Li CM, Wang TG, Lee HY, Wang HP, Hsieh SH, Chou M, et al. Swallowing training combined with game-based biofeedback in poststroke dysphagia. PM R. 2016;8(8):773-9. http://dx.doi.org/10.1016/j.pmrj.2016.01.003.
http://dx.doi.org/10.1016/j.pmrj.2016.01...
) as cross-sectional. Most of the articles were from North America (1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2828 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...

29 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
-3030 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...
,3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...

36 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...
-3737 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...
,3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
) and Asia(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2626 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.,3131 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of submental ultrasonographic evaluation for dysphagia patients. Ann Rehabil Med. 2016;40(2):197-205. http://dx.doi.org/10.5535/arm.2016.40.2.197. PMid:27152268.
http://dx.doi.org/10.5535/arm.2016.40.2....
,3232 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...
,4141 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...

42 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
-4343 Li CM, Wang TG, Lee HY, Wang HP, Hsieh SH, Chou M, et al. Swallowing training combined with game-based biofeedback in poststroke dysphagia. PM R. 2016;8(8):773-9. http://dx.doi.org/10.1016/j.pmrj.2016.01.003.
http://dx.doi.org/10.1016/j.pmrj.2016.01...
).

There was a higher concentration of studies published between 2011 and 2021(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2626 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.,3030 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...

31 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of submental ultrasonographic evaluation for dysphagia patients. Ann Rehabil Med. 2016;40(2):197-205. http://dx.doi.org/10.5535/arm.2016.40.2.197. PMid:27152268.
http://dx.doi.org/10.5535/arm.2016.40.2....

32 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...

33 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...
-3434 Rocha SG, Silva RG, Berti LC. Qualitative and quantitative ultrasound analysis of oropharyngeal swallowing. CoDAS. 2015;27(5):437-45. http://dx.doi.org/10.1590/2317-1782/20152015015. PMid:26648214.
http://dx.doi.org/10.1590/2317-1782/2015...
,3838 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...
,4040 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...
,4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
,4343 Li CM, Wang TG, Lee HY, Wang HP, Hsieh SH, Chou M, et al. Swallowing training combined with game-based biofeedback in poststroke dysphagia. PM R. 2016;8(8):773-9. http://dx.doi.org/10.1016/j.pmrj.2016.01.003.
http://dx.doi.org/10.1016/j.pmrj.2016.01...
), followed by the period between 2000 and 2010(2828 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...
,2929 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
,4141 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...
), 1990 to 1999(1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...
,3737 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...
) and 1980 to 1989(3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...
,3636 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...
,3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
). The sample size varied from one(1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
) and 120(2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...
) participants and most studies were conducted only with individuals without dysphagia or associated disease(1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...

26 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...

27 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.

28 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...

29 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
-3030 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...
,3333 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...

34 Rocha SG, Silva RG, Berti LC. Qualitative and quantitative ultrasound analysis of oropharyngeal swallowing. CoDAS. 2015;27(5):437-45. http://dx.doi.org/10.1590/2317-1782/20152015015. PMid:26648214.
http://dx.doi.org/10.1590/2317-1782/2015...

35 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...

36 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...

37 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...

38 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...

39 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...

40 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...

41 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...
-4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
). Half of the articles included did not specify the absolute frequency of the sample according to sex and, in those that included the information(1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2828 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...

29 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
-3030 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...
,3232 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...
,3333 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...
,3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...
,3737 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...

38 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...
-3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
,4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
), the groups were mostly mixed.

There was high variability regarding the equipment and the types and frequencies of the transducers used to perform the ultrasonography examination, with similarity only when the articles were from the same research group, which made it impossible to establish any standardization regarding these parameters. The positioning of the transducer was more frequent in the submandibular area(5,12,19,20,23,26-31,33-40,43, followed by the laryngeal area(1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,3232 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...
,4141 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...
,4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
). One study did not specify the positioning(2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...
).

The most investigated measures, in ascending order of frequency, were amplitude(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1313 Matsuo T, Matsuyama M, Nakatani K, Mori N. Evaluation of swallowing movement using ultrasonography. Radiological Phys Technol. 2020;13(1):62-8. http://dx.doi.org/10.1007/s12194-019-00547-1. PMid:31786806.
http://dx.doi.org/10.1007/s12194-019-005...
,1919 Cordaro MA, Sonies BC. An image processing scheme to quantitatively extract and validate hyoid bone motion based on real-time ultrasound recordings of swallowing. IEEE Trans Biomed Eng. 1993;40(8):841-4. http://dx.doi.org/10.1109/10.238473. PMid:8258453.
http://dx.doi.org/10.1109/10.238473...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.

28 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...

29 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...

30 Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG. Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope. 2015;125(8):1886-91. http://dx.doi.org/10.1002/lary.25224. PMid:25739655.
http://dx.doi.org/10.1002/lary.25224...

31 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of submental ultrasonographic evaluation for dysphagia patients. Ann Rehabil Med. 2016;40(2):197-205. http://dx.doi.org/10.5535/arm.2016.40.2.197. PMid:27152268.
http://dx.doi.org/10.5535/arm.2016.40.2....

32 Matsuo T, Matsuyama M. Detection of poststroke oropharyngeal dysphagia with swallowing screening by ultrasonography. PLoS One. 2021;16(3):e0248770. http://dx.doi.org/10.1371/journal.pone.0248770. PMid:33730038.
http://dx.doi.org/10.1371/journal.pone.0...

33 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...
-3434 Rocha SG, Silva RG, Berti LC. Qualitative and quantitative ultrasound analysis of oropharyngeal swallowing. CoDAS. 2015;27(5):437-45. http://dx.doi.org/10.1590/2317-1782/20152015015. PMid:26648214.
http://dx.doi.org/10.1590/2317-1782/2015...
,3737 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...
,4040 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...

41 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...

42 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
-4343 Li CM, Wang TG, Lee HY, Wang HP, Hsieh SH, Chou M, et al. Swallowing training combined with game-based biofeedback in poststroke dysphagia. PM R. 2016;8(8):773-9. http://dx.doi.org/10.1016/j.pmrj.2016.01.003.
http://dx.doi.org/10.1016/j.pmrj.2016.01...
), time (55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...

26 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...

27 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.

28 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...
-2929 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
,3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...

36 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...

37 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...

38 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...
-3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
,4141 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...
,4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
), and velocity (26,-29,37). However, the methods for extraction were heterogeneous, with the use of different softwares to support the analysis of images decomposed into frames, and different methods of marking anatomical points of reference (Chart 1). The level of reliability was investigated in only six articles(1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.,4040 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...
), mostly through the intraclass correlation coefficient (ICC) with results ranging from moderate to excellent (Chart 1).

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(3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...
,3636 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...
,3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
), 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(2424 Allen JE, Clunie G, Ma JK, Coffey M, Winiker K, Richmond S, et al. Translating ultrasound into clinical practice for the assessment of swallowing and laryngeal function: a speech and language pathology-led consensus study. Dysphagia. 2022;37(6):1586. http://dx.doi.org/10.1007/s00455-022-10413-9. PMid:35201387.
http://dx.doi.org/10.1007/s00455-022-104...
).

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(1212 Chen YC, Hsiao MY, Wang YC, Fu CP, Wang TG. Reliability of ultrasonography in evaluating hyoid bone movement. J Med Ultrasound. 2017;25(2):90-5. http://dx.doi.org/10.1016/j.jmu.2017.01.002. PMid:30065466.
http://dx.doi.org/10.1016/j.jmu.2017.01....
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.,4040 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...
), 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 (2020 Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of Ultrasonography in Assessing Oropharyngeal Dysphagia in Stroke Patients. Ultrasound Med Biol. 2012;38(9):1522-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.04.017. PMid:22698507.
http://dx.doi.org/10.1016/j.ultrasmedbio...
,2727 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.,3131 Lee YS, Lee KE, Kang Y, Yi TI, Kim JS. Usefulness of submental ultrasonographic evaluation for dysphagia patients. Ann Rehabil Med. 2016;40(2):197-205. http://dx.doi.org/10.5535/arm.2016.40.2.197. PMid:27152268.
http://dx.doi.org/10.5535/arm.2016.40.2....
,4040 Winiker K, Burnip E, Gozdzikowska K, Guiu Hernandez E, Hammond R, Macrae P, et al. Ultrasound: validity of a pocket-sized system in the assessment of swallowing. Dysphagia. 2021;36(6):1010-8. http://dx.doi.org/10.1007/s00455-020-10232-w. PMid:33389177.
http://dx.doi.org/10.1007/s00455-020-102...
), the cervical vertebral body(4444 Logemann JA. Evaluation and treatment of swallowing disorders. Nerang: Pro-Ed Australia; 1983.) and adjacent musculature were used(2323 Macrae PR, Doeltgen SH, Jones RD, Huckabee ML. Intra- and inter-rater reliability for analysis of hyoid displacement measured with sonography. J Clin Ultrasound. 2012;40(2):74-8. http://dx.doi.org/10.1002/jcu.20874. PMid:21953135.
http://dx.doi.org/10.1002/jcu.20874...
,2929 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
,3333 Perry SE, Winkelman CJ, Huckabee ML. Variability in ultrasound measurement of hyoid bone displacement and submental muscle size using 2 methods of data acquisition. Folia Phoniatr Logop. 2016;68(5):205-10. http://dx.doi.org/10.1159/000473876. PMid:28456801.
http://dx.doi.org/10.1159/000473876...
,3434 Rocha SG, Silva RG, Berti LC. Qualitative and quantitative ultrasound analysis of oropharyngeal swallowing. CoDAS. 2015;27(5):437-45. http://dx.doi.org/10.1590/2317-1782/20152015015. PMid:26648214.
http://dx.doi.org/10.1590/2317-1782/2015...
). 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(33 Pearson WG Jr, Langmore SE, Zumwalt AC. Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid. Dysphagia. 2011;26(4):345-51. http://dx.doi.org/10.1007/s00455-010-9315-z. PMid:21069388.
http://dx.doi.org/10.1007/s00455-010-931...

4 Steele CM, Bailey GL, Chau T, Molfenter SM, Oshalla M, Waito AA, et al. The relationship between hyoid and laryngeal displacement and swallowing impairment. Clin Otolaryngol. 2011;36(1):30-6. http://dx.doi.org/10.1111/j.1749-4486.2010.02219.x. PMid:21414151.
http://dx.doi.org/10.1111/j.1749-4486.20...

5 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....

6 Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90-5. http://dx.doi.org/10.1007/BF00714593. PMid:8005013.
http://dx.doi.org/10.1007/BF00714593...

7 Ishida R, Palmer J, Hiiemae K. Hyoid motion during swallowing: factors affecting forward and upward displacement. Dysphagia. 2002;17(4):262-7. http://dx.doi.org/10.1007/s00455-002-0064-5. PMid:12355141.
http://dx.doi.org/10.1007/s00455-002-006...
-88 Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274-9. http://dx.doi.org/10.1007/s00455-007-9135-y. PMid:17962998.
http://dx.doi.org/10.1007/s00455-007-913...
). 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(55 Kwak HJ, Kim L, Ryu BJ, Kim YH, Park SW, Cho DG, et al. Influence of nasogastric tubes on swallowing in stroke patients: measuring hyoid bone movement with ultrasonography. Ann Rehabil Med. 2018;42(4):551-9. http://dx.doi.org/10.5535/arm.2018.42.4.551. PMid:30180524.
http://dx.doi.org/10.5535/arm.2018.42.4....
,1414 Costa BOI, Rodrigues DSB, de Magalhães DDD, Santos AS, Santos RV, Azevedo EHM, et al. Quantitative ultrasound assessment of hyoid bone displacement during swallowing following thyroidectomy. Dysphagia. 2020;36:659-69. http://dx.doi.org/10.1007/s00455-020-10180-5. PMid:32889628.
http://dx.doi.org/10.1007/s00455-020-101...
,2525 Dejaeger E, Pelemans W. Swallowing and the duration of the hyoid movement in normal adults of different ages. Aging (Milano). 1996;8(2):130-4. http://dx.doi.org/10.1007/BF03339567. PMid:8737612.
http://dx.doi.org/10.1007/BF03339567...

26 Chen YC, Chen PY, Wang YC, Wang TG, Han DS. Decreased swallowing function in the sarcopenic elderly without clinical dysphagia: a cross-sectional study. BMC Geriatr. 2020;20(1):419. http://dx.doi.org/10.1186/s12877-020-01832-0. PMid:33087067.
http://dx.doi.org/10.1186/s12877-020-018...

27 Chen YC, Hsiao MY, Chen PY, Wang TG. Effects of age on the speed of hyoid bone movement during swallowing. Int J Gerontol. 2019;13:344-8.

28 Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on Hyoid Movement Kinematics Gloria. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7. PMid:12355143.
http://dx.doi.org/10.1007/s00455-002-007...
-2929 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
,3535 Shawker TH, Sonies B, Hall TE, Baum BF. Ultrasound analysis of tongue hyoid and larynx activity during swallowing. Invest Radiol. 1984;19(2):82-6. http://dx.doi.org/10.1097/00004424-198403000-00003. PMid:6398320.
http://dx.doi.org/10.1097/00004424-19840...

36 Sonies BC, Ph D, Parent LJ, Morrish K, Ph D, Baum BJ, et al. Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia. 1988;3(1):1-10. http://dx.doi.org/10.1007/BF02406274. PMid:3073915.
http://dx.doi.org/10.1007/BF02406274...

37 Sonies BC, Wang C, Sapper DJ. Evaluation of normal and abnormal hyoid bone movement during swallowing by use of ultrasound duplex-Doppler imaging. Ultrasound Med Biol. 1996;22(9):1169-75. http://dx.doi.org/10.1016/S0301-5629(96)00158-5. PMid:9123641.
http://dx.doi.org/10.1016/S0301-5629(96)...

38 Steele C, Sasse C, Bressmann T. Tongue-pressure and hyoid movement timing in healthy liquid swallowing. Int J Lang Commun Disord. 2012;47(1):77-83. http://dx.doi.org/10.1111/j.1460-6984.2011.00082.x. PMid:22268903.
http://dx.doi.org/10.1111/j.1460-6984.20...
-3939 Stone M, Shawker TH. An ultrasound examination of tongue movement during swallowing. Dysphagia. 1986;1(2):78-83. http://dx.doi.org/10.1007/BF02407118. PMid:3527582.
http://dx.doi.org/10.1007/BF02407118...
,4141 Yabunaka K, Ohue M, Hashimoto T, Katsuda T, Yamamoto K, Sanada S. Sonographic analysis of hyoid bone movement during swallowing. IFMBE Proc. 2009;22:840-2. http://dx.doi.org/10.1007/978-3-540-89208-3_201.
http://dx.doi.org/10.1007/978-3-540-8920...
,4242 Yabunaka K, Sanada H, Sanada S, Konishi H, Hashimoto T, Yatake H, et al. Sonographic assessment of hyoid bone movement during swallowing: A study of normal adults with advancing age. Radiological Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9. PMid:20945118.
http://dx.doi.org/10.1007/s12194-010-010...
). It is worth highlighting this measure, because it is one of the indicators for the risk of penetration or inhalation(66 Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90-5. http://dx.doi.org/10.1007/BF00714593. PMid:8005013.
http://dx.doi.org/10.1007/BF00714593...
), 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(4444 Logemann JA. Evaluation and treatment of swallowing disorders. Nerang: Pro-Ed Australia; 1983.).

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(4444 Logemann JA. Evaluation and treatment of swallowing disorders. Nerang: Pro-Ed Australia; 1983.) and it is relevant to analyze the interrelationships between kinematic parameters to understand how motor control strategies occur by adjusting the volume and consistency(2929 Chi-fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002 Jun;45(3):457-68. http://dx.doi.org/10.1044/1092-4388(2002/036). PMID: 12068999.
http://dx.doi.org/10.1044/1092-4388(2002...
).

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 intra-evaluator 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.

Appendix 1 Search strategies used in databases

Databases Descriptors Results
Pubmed/Medline ((“deglutition”[MeSH Terms] OR “deglutition”[All Fields] OR “deglutitions”[All Fields] OR “swallowing”[All Fields] OR “swallowings”[All Fields] OR “swallow”[All Fields] OR “swallows”[All Fields] OR “deglutition disorders”[MeSH Terms] OR “deglutition disorders”[All Fields] OR “deglutition disorder”[All Fields] OR “swallowing disorder”[All Fields] OR “swallowing disorders”[All Fields] OR “dysphagia”[All Fields]) AND (“hyoid bone”[MeSH Terms] OR “hyoid”[All Fields]) AND (“ultrasonography”[MeSH Terms] OR “ultrasonography”[All Fields] OR “diagnostic ultrasound”[All Fields] OR “ultrasound”[All Fields] OR “ultrasounds”[All Fields] OR “ultrasound imaging”[All Fields] OR “ultrasonic imaging”[All Fields] OR “medical sonography”[All Fields] OR “ultrasonographic imaging”[All Fields] OR “echography”[All Fields] OR “ultrasonic diagnoses”[All Fields] OR “ultrasonic diagnosis”[All Fields] OR “ultrasonics”[All Fields] OR “sonographic”[All Fields])) 61 results
EMBASE (‘dysphagia’/exp OR ‘swallowing’/exp) AND (‘echography’/exp OR ‘ultrasound’/exp) AND (‘hyoid bone’/exp) 98 results
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
Scopus (TITLE-ABS-KEY (deglutition OR deglutitions OR swallowing OR swallowingsOR swallow OR swallows OR “deglutition AND disorders” OR “deglutition AND disorder” OR “swallowing AND disorder” OR “swallowing AND disorders” OR dysphagia) AND TITLE-ABS-KEY (“hyoid AND bone” OR “hyoid” ) AND TITLE-ABS-KEY (ultrasonography OR “diagnostic AND ultrasound” OR ultrasound OR ultrasounds)) 78 results
LILACS (deglutition OR “deglutition disorders” OR deglutição OR deglución OR “transtornos de deglutição” OR “trastornos de deglución” OR “troubles de la deglutition” OR deglutition) AND (“hyoid bone” OR “osso hioide” OR “hueso hioides” OR “os hyoide”) AND (Ultrasonography OR ultrasonografía OR échographie OR ultrassonografia) 8 results

Caption: ICC: intraclass correlation coefficient; HB: hyoid bone; USG: ultrasonograph

  • Study conducted at Programa Associado de Pós-graduação em Fonoaudiologia, Universidade Federal da Paraíba - UFPB, João Pessoa (PB), Brasil.
  • Financial support: This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Financial Code 001.

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    » http://dx.doi.org/10.1044/1092-4388(2002/036)
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Publication Dates

  • Publication in this collection
    17 July 2023
  • Date of issue
    2023

History

  • Received
    17 Jan 2022
  • Accepted
    01 July 2022
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