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Ultrasonography and swallowing: a critical review of the literature

Abstracts

Purpose

To identify how the deglutition function has been evaluated using ultrasound (US).

Research strategy

This literature review used the PubMed database to survey international scientific publications about US and its use to evaluate deglutition. Studies were located and selected by surveying relevant articles published between January 2002 and August 2013. The survey was limited to studies on humans published in English.

Selection criteria

Repeated studies (determined by overlapping keywords), case studies, literature reviews, letters to the editor and studies not directly related to the topic were excluded.

Results

A total of 17 studies matching the inclusion criteria were identified. More than half of the studies evaluated the deglutition of healthy adults with no preference for gender. The parameters adopted for image analysis were not unanimous, and there was considerable variation among studies.

Conclusion

US proved to be a fast, non-invasive, low-cost method for evaluating objective parameters of deglutition. As a further advantage, US may be performed at bedside because the equipment is typically easy to handle and transport.

Ultrasonography; Ultrasonics; Deglutition; Deglutition disorders; Evaluation


Objetivo

Identificar como a função da deglutição tem sido avaliada por meio da ultrassonografia (USG).

Estratégia de pesquisa

Esta revisão da literatura levantou publicações científicas internacionais sobre a USG e seu uso na avaliação da deglutição, por meio da base de dados PubMed. Foi realizada a localização e seleção dos estudos através de levantamento de textos publicados sobre o assunto, no período de janeiro de 2002 a agosto de 2013, limitando-se a estudos em seres humanos, no idioma inglês.

Critérios de seleção

Foram excluídos aqueles repetidos por sobreposição das palavras-chave, estudos de caso, revisões de literatura, cartas ao editor e os não relacionados diretamente à temática.

Resultados

Foram identificados 17 estudos que corresponderam aos critérios de inclusão. Observou-se que mais da metade dos estudos avaliou a deglutição de indivíduos adultos saudáveis, sem preferência por nenhum dos gêneros. Os parâmetros adotados para a análise das imagens não foram unânimes, havendo variação considerável entre os estudos.

Conclusão

A USG da deglutição demonstrou ser um método rápido, não invasivo, de baixo custo, que fornece parâmetros objetivos sobre a deglutição e que pode ser realizado em beira de leito, uma vez que o equipamento costuma ser de fácil manuseio e transporte.

Ultrassonografia; Ultrassom; Deglutição; Transtornos de deglutição; Avaliação


INTRODUCTION

Ultrasound (US) involves placing a transducer on the body part being examined to transform the echoes reflected by the human body into signals that are electronically decoded to form an image(1 Santos HCO, Amaral WN, Tacon KCB. A história da ultrassonografia no Brasil e no mundo. EFDeportes.com Rev Digit. 2012 [acesso em 12 jan 2014];17(167). Disponível em: http://www.efdeportes.com/efd167/a-historia-da-ultrassonografia.htm
http://www.efdeportes.com/efd167/a-histo...
). US is a noninvasive examination that provides dynamic images that focus on the soft tissues and body structures(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
). The technique is widely applied in clinical practice because of its low cost, safety, speed and lack of radiation(3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
).

US is a viable option for studying the oral and pharyngeal structures involved in deglutition(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
). Some advantages related to its use include the possibility of using food under regular conditions without the presence of contrasts and/or dyes and the portability of the device, which allows the test to be performed at bedside(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
).

The structures and variables most often analyzed in deglutition studies are the amount and duration of hyoid bone elevation; glottal closure (frequency, latency, response and duration); the amplitude and speed of the vertical movement of the tongue; the total duration of deglutition; the mobility and function of the phonoarticulatory organs during deglutition; the distance between the hyoid bone and the larynx during deglutition; and the laryngeal elevation (beginning, peak and duration)(3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,4 Ardakani FE. Evaluation of swallowing patterns of the tongue using real-time B-mode sonography. J Contemp Dent Pract. 2006;7(3):67-74.).

The literature describes the use of US during deglutition in both healthy and sick individuals for organ analysis or for diagnosing dysphagia(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
). US can also be performed in patients of different age groups and is considered a noninvasive, accurate method for visualizing bolus movement in the pharyngeal phase of deglutition during infant feeding(6 Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
https://doi.org/10.1007/s00455-009-9241-...
).

PURPOSE

The present study aimed to determine how US has been used to assess deglutition based on refereed literature.

RESEARCH STRATEGY

To establish the search method, the precepts of the Cochrane Handbook(7 Higgins JPT, Green S, editors Cochrane handbook for systematic reviews of interventions Version 5.1.0 [internet]; Baltimore: The Cochrane Collaboration; 2011 [acesso em 11 maio 2011]. Disponível em: http://www.cochrane.org/training/cochrane-handbook
http://www.cochrane.org/training/cochran...
) were followed.

The studies were located and selected by surveying articles on the subject published between August 2002 and August 2013. The articles were selected from the PubMed database and were limited to studies performed on humans and published in English. The following descriptors were used: “Ultrasound and Deglutition”, “Ultrasound and Deglutition Disorders”, “Ultrasound Diagnosis and Deglutition”, “Ultrasound Diagnosis and Deglutition Disorders”, “Ultrasonography and Deglutition”, “Ultrasonography and Deglutition Disorders”, “Ultrasonography Diagnosis and Deglutition”, “Ultrasonography Diagnosis and Deglutition Disorders”.

SELECTION CRITERIA

The database searches were performed independently by the researchers to minimize the possible loss of citations and to analyze the relevance of each retrieved citation for selection and inclusion in the study. Citations in languages other than English were excluded, as were those that contained overlapping keywords. Among the full articles obtained, case studies, literature reviews, letters to the editor and those not directly related to the topic were excluded. Articles that were effectively related to the research proposal were analyzed. The researchers conducted all stages of the study independently; when disagreements occurred, only articles with consensual final agreement were included. By its nature, this study was not single-blind (Figure 1).

Figure 1
Search pathway for article selection

The rationale for the exclusion of 279 citations is provided in Table 1.

Table 1
Articles excluded because of a lack of direct relation to the topic

DATA ANALYSIS

The 17 citations selected were critically evaluated in terms of their objectives; number, gender and ages of the participants; criteria and evaluation methods; results; and conclusions.

Regarding the criteria and evaluation methods, we sought to assess and describe the methods used in the articles to determine whether there was homogeneity among them.

Regarding the results and conclusions, in addition to the general information the articles provided in these sections, we also noted the advantages and disadvantages of the techniques discussed in each study.

RESULTS

The results of the study are briefly described in Chart 1.

DISCUSSION

After analyzing the selected articles, we observed that the studies that used US to assess deglutition could be divided into three groups: studies that investigated the deglutition of healthy individuals (52.9%)(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,6 Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
https://doi.org/10.1007/s00455-009-9241-...
,8 Welge-Lüssen A, Ebnöther M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses. 2009;34(6):499-502. http://dx.doi.org/10.1093/chemse/bjp024
https://doi.org/10.1093/chemse/bjp024...

Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
https://doi.org/10.1007/s00455-002-0070-...

10  Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
https://doi.org/10.1044/1092-4388(2002/0...

11  Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
https://doi.org/10.1038/ajg.2009.411...

12  Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
https://doi.org/10.1159/000163036...
-1313  Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
https://doi.org/10.1007/s00056-007-0547-...
); studies that compared the deglutition of diseased individuals and their healthy controls(1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
,1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...

16  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
https://doi.org/10.1007/s00415-003-1007-...

17  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...

18  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
-1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
) (i.e., those with craniofacial abnormalities(1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
) [16.7%], stroke(1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...
,1818  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
,1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
) [50%] and neurogenic dysphagia(1616  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
https://doi.org/10.1007/s00415-003-1007-...
,1717  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...
) [33.3%]) to that of healthy controls (35.3%)(1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
,1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...

16  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
https://doi.org/10.1007/s00415-003-1007-...

17  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...

18  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
-1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
); and studies that investigated deglutition in two specific diseases(5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
,2020  Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.) (11.8%): nephropathic cystinosis and amyotrophic lateral sclerosis.

Regarding the participants’ gender, most of the studies included individuals of both genders (82.3%)(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
,8 Welge-Lüssen A, Ebnöther M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses. 2009;34(6):499-502. http://dx.doi.org/10.1093/chemse/bjp024
https://doi.org/10.1093/chemse/bjp024...

Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
https://doi.org/10.1007/s00455-002-0070-...

10  Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
https://doi.org/10.1044/1092-4388(2002/0...
-1111  Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
https://doi.org/10.1038/ajg.2009.411...
,1313  Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
https://doi.org/10.1007/s00056-007-0547-...
,1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...

16  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
https://doi.org/10.1007/s00415-003-1007-...

17  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...

18  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...

19  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
-2020  Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.). Only one study included only male subjects(1212  Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
https://doi.org/10.1159/000163036...
) (5.9%).

The age of the participants varied considerably among the studies. Most of the studies(5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
,1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...

16  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
https://doi.org/10.1007/s00415-003-1007-...

17  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...

18  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
-1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
) included adult and elderly subjects (35.2%). Some of the studies(3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,9 Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
https://doi.org/10.1007/s00455-002-0070-...
,1010  Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
https://doi.org/10.1044/1092-4388(2002/0...
) divided the adults into different age groups (17.6%), and others(8 Welge-Lüssen A, Ebnöther M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses. 2009;34(6):499-502. http://dx.doi.org/10.1093/chemse/bjp024
https://doi.org/10.1093/chemse/bjp024...
,1212  Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
https://doi.org/10.1159/000163036...
) examined adults of a particular age group (11.8%). Studies involving children and infants were the minority(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,6 Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
https://doi.org/10.1007/s00455-009-9241-...
,1111  Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
https://doi.org/10.1038/ajg.2009.411...
,1313  Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
https://doi.org/10.1007/s00056-007-0547-...
,2020  Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.) (29.41%).

The parameters evaluated during the US examination were not unanimous. In seven studies(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
,3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,9 Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
https://doi.org/10.1007/s00455-002-0070-...
,1010  Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
https://doi.org/10.1044/1092-4388(2002/0...
,1212  Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
https://doi.org/10.1159/000163036...
,1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...
,1616  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
https://doi.org/10.1007/s00415-003-1007-...
) (41.1%), the lifting motion of the hyoid bone during deglutition was assessed, and in four of those studies(3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
,9 Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
https://doi.org/10.1007/s00455-002-0070-...
,1010  Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
https://doi.org/10.1044/1092-4388(2002/0...
,1212  Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
https://doi.org/10.1159/000163036...
), the duration of hyoid movement was also considered. Four studies(8 Welge-Lüssen A, Ebnöther M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses. 2009;34(6):499-502. http://dx.doi.org/10.1093/chemse/bjp024
https://doi.org/10.1093/chemse/bjp024...
,1313  Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
https://doi.org/10.1007/s00056-007-0547-...
,1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
,1717  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...
) evaluated tongue movements during deglutition (23.5%), and the others assessed different parameters: mobility and functionality of the phonoarticulatory organs during deglutition(5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
) (5.9%); duration of deglutition and apnea(6 Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
https://doi.org/10.1007/s00455-009-9241-...
) (5.9%); glottal closure and its characteristics (frequency, response latency and duration)(1111  Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
https://doi.org/10.1038/ajg.2009.411...
) (5.9%); movement of the lateral wall of the pharynx(1818  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
) (5.9%); movement of the hyoid bone and tongue thickness(1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
) (5.9%); and tongue and hyoid bone movements during deglutition(2020  Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.) (5.9%).

For a better discussion of the studies’ methods, results and conclusions, the articles were grouped according to the parameters considered for the assessment, as described above.

In studies that assessed the movement of the hyoid bone - elevation and/or duration - the overall objective was to correlate the movement of the hyoid bone with the participant’s age, gender and clinical status. A longer mean duration of hyoid bone elevation was observed with increasing age, as was decreased peak elevation of the hyoid bone(3 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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
https://doi.org/10.1007/s12194-010-0107-...
). A study conducted with children found that gender may affect hyoid bone elevation - the mean movement was significantly greater in females(2 Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
https://doi.org/10.1002/jcu.20733...
). Regarding the participant’s clinical condition, the hyoid bone movement was significantly greater in healthy subjects compared with individuals with neurogenic dysphagia(1515  Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
https://doi.org/10.1016/j.ultrasmedbio.2...
,1616  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
https://doi.org/10.1007/s00415-003-1007-...
).

All of the studies that assessed the hyoid bone movement found that US could quantitatively and reliably evaluate this parameter.

Among the studies that assessed tongue movement during deglutition, two subgroups could be defined. The first subgroup aimed to determine the extent of intrapersonal variability in the duration of tongue movements during deglutition. The results indicated high intrapersonal variability in both healthy individuals and individuals with neurogenic dysphagia; however, greater variability in the duration of the transport phase was observed in the dysphagic group(1717  Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
https://doi.org/10.1007/s00455-002-0071-...
). The second subgroup(1313  Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
https://doi.org/10.1007/s00056-007-0547-...
,1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
) investigated US modes using tongue movement as the parameter of interest. High intra- and/or interpersonal variability was also found in this parameter, and it was observed that M-mode US provided better information about tongue movement during deglutition.

For all of the studies in this group, US provided information about tongue movements during deglutition without any side effects, and it was considered a useful tool. It should be noted that most of the studies concluded that this parameter exhibits high intra- and interpersonal variability, which can often complicate data analysis, as described by Galen and Jost-Brinkmann (2010)(1414  Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
https://doi.org/10.1007/s00056-010-9928-...
).

The other parameters were only investigated in single studies. Thus, the conclusions regarding the use of US and its results apply to only one study per parameter.

One of the studies investigated the mobility and function of the phonoarticulatory organs during deglutition. The authors sought to determine the role of US in the diagnostic evaluation of dysphagia in patients with amyotrophic lateral sclerosis (ALS). The exam was conducted concurrently with deglutition videofluoroscopy (VDF), and the study found that US provided static and dynamic functionality data for the oropharyngeal phase of deglutition more efficiently than VDF. Thus, the authors concluded that US should be used as a complement to VDF because it provides a precise description of the oral deglutition phase(5 Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
https://doi.org/10.1007/s11547-010-0523-...
).

Using deglutition apnea as parameter, one study evaluated the ability of US to identify deglutition apnea in infants(6 Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
https://doi.org/10.1007/s00455-009-9241-...
). The study involved the concomitant use of US and respiratory plethysmography and showed that the passage of the bolus during pharyngeal deglutition in a nursing child can be recorded using US, regardless of the respiration phase. Deglutition US was correlated with deglutition apnea detected with respiratory inductive plethysmography. Both techniques, when combined, have the potential to provide useful information about children who have nursing difficulties.

A study conducted in healthy newborns used the parameter glottal closure to investigate the concomitant use of esophageal manometry and glottis US. It found that glottal adduction during basal or adaptive deglutition occurs in any respiratory phase, thus ensuring protection of the airways against aspiration before or during deglutition. The methods used in this assessment allowed the study of glottis movement during deglutition, and it was concluded that investigation of the pharyngeal-glottal relationship using non-invasive methods, such as US, may be acceptable for and applicable to all ages(1111  Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
https://doi.org/10.1038/ajg.2009.411...
).

One study examined the duration of the pharyngeal phase of deglutition based on the tongue and hyoid bone movements needed to start and finish deglutition. For this purpose, US was used to assess the deglutition of 101 patients with nephropathic cystinosis. The authors found that oral motor dysfunction of deglutition in patients with cystinosis increases progressively with age and is correlated with generalized muscular dysfunction but not with disease severity. Based on cross-sectional data, the dysfunction increased with increasing age and the number of years without cysteamine treatment(2020  Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.).

A study conducted with healthy subjects and stroke patients used the displacement and duration of pharyngeal movement during deglutition as a parameter. The patients were subdivided into two groups: the first (Group A) consisted of patients who presented with penetration and/or aspiration of food, indicated through VDF, and the second (Group B) consisted of patients with no VDF findings. The mean pharyngeal displacement of Groups A and B was significantly lower compared with that of healthy individuals, while the mean duration of pharyngeal movement of Groups A and B was longer than that of healthy individuals. In conclusion, the study indicated that the use of US to analyze pharyngeal movement may help to quantify pharyngeal function and can serve as a complementary method for the anatomical evaluation of the pharyngeal phase in patients with stroke and dysphagia(1818  Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
https://doi.org/10.1016/j.ultrasmedbio.2...
).

Another study analyzed the hyoid bone movement and tongue thickness. These parameters were compared between healthy individuals and stroke patients with and without the use of an alternative feeding route. The study found significantly less hyoid bone displacement and tongue thickness in patients fed exclusively by an alternate route compared with stroke patients with oral ingestion. No significant differences in either variable were observed between the control group and the stroke patients with oral ingestion(1919  Hsiao MY, Chang YC, Chen HC, 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
https://doi.org/10.1016/j.ultrasmedbio.2...
).

Generally, all of the articles assessed found that deglutition US was a fast, noninvasive, low-cost method that provides objective information about parameters of deglutition and can be performed at bedside because the equipment is usually easy to handle and transport. Equally important, the authors of the examined studies all concluded that deglutition assessment with US has some inherent disadvantages, including the following: the pressure exerted by the transducer on the examined structure, transducer positioning and the lack of precise anatomical markers for some of the structures being investigated. Because of these limitations, although US was effective for the initial diagnosis of impaired deglutition, it should be used in conjunction with other exams that complement the assessment of phonoarticulatory organ function during deglutition to accurately diagnose dysphagia.

CONCLUSION

The heterogeneity of the studies showed that different groups and pathologies can be assessed with US; however, the methodological variability of the included studies hinders the definition and generalization of the patterns found.

The present review found that US examination is effective for assessing the components involved in the dynamics of deglutition, especially the oral and early pharyngeal phases, such as phonoarticulatory organ function, deglutition apnea duration, glottal closure and its aspects, and hyoid bone movement. However, US should not replace other examinations that assist in the assessment of the pharyngeal and esophageal phase and in dysphagia diagnosis because US cannot identify some dynamic components of function, such as food stasis in the pharynx. Thus, US has been used as a complement to VDF, plethysmography, surface electromyography (EMG), deglutition videoendoscopy and manometry to provide more reliable parameters of the oral phase and the beginning of the pharyngeal phase of deglutition.


Chart 1. Summary of the articles included in the study

REFERÊNCIAS

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  • 2
    Scarborough DR, Waizenhofer S, Siekemeyer L, Hughes M. Sonographically measured hyoid bone displacement during swallow in preschool children: a preliminary study. J Clin Ultrasound. 2010;38(8):430-4. http://dx.doi.org/10.1002/jcu.20733
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  • 3
    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. Radiol Phys Technol. 2011;4(1):73-7. http://dx.doi.org/10.1007/s12194-010-0107-9
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    Ardakani FE. Evaluation of swallowing patterns of the tongue using real-time B-mode sonography. J Contemp Dent Pract. 2006;7(3):67-74.
  • 5
    Tamburrini S, Solazzo A, Sagnelli A, Del Vecchio L, Reginelli A, Monsorrò M, et al. Amyotrophic lateral sclerosis: sonographic evaluation of dysphagia. Radiol Med. 2010;115(5):784-93. http://dx.doi.org/10.1007/s11547-010-0523-2
    » https://doi.org/10.1007/s11547-010-0523-2
  • 6
    Geddes DT, Chadwick LM, Kent JC, Garbin CP, Hartmann PE. Ultrasound imaging of infant swallowing during breast-feeding. Dysphagia. 2010;25(3):183-91. http://dx.doi.org/10.1007/s00455-009-9241-0
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  • 8
    Welge-Lüssen A, Ebnöther M, Wolfensberger M, Hummel T. Swallowing is differentially influenced by retronasal compared with orthonasal stimulation in combination with gustatory stimuli. Chem Senses. 2009;34(6):499-502. http://dx.doi.org/10.1093/chemse/bjp024
    » https://doi.org/10.1093/chemse/bjp024
  • 9
    Chi-Fishman G, Sonies BC. Effects of systematic bolus vviscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17(4):278-87. http://dx.doi.org/10.1007/s00455-002-0070-7
    » https://doi.org/10.1007/s00455-002-0070-7
  • 10
    Chi-Fishman G, Sonies BC. Kinematic strategies for hyoid movement in rapid sequential swallowing. J Speech Lang Hear Res. 2002;45(3);457-68. http://dx.doi.org/10.1044/1092-4388(2002/036
    » https://doi.org/10.1044/1092-4388(2002/036
  • 11
    Jadcherla SR, Gupta A, Wang M, Coley BD, Fernandez S, Shaker R. Definition and implications of novel pharyngo-glottal reflex in human infants using concurrent manometry ultrasonography. J Gastroenterol. 2009;104(10):2572-82. http://dx.doi.org/10.1038/ajg.2009.411
    » https://doi.org/10.1038/ajg.2009.411
  • 12
    Komori M, Hyodo M, Gyo K. A swallowing evaluation with simultaneous videoendoscopy, ultrasonography and videofluorography in healthy controls. ORL J Otorhinolaryngol Relat Spec. 2008;70(6):393-8. http://dx.doi.org/10.1159/000163036
    » https://doi.org/10.1159/000163036
  • 13
    Peng CL, Miethke RR, Pong SJ, Lin CT. Investigation of tongue movements during swallowing with M-mode ultrasonography. J Orofac Orthop. 2007;68(1):17-25. http://dx.doi.org/10.1007/s00056-007-0547-y
    » https://doi.org/10.1007/s00056-007-0547-y
  • 14
    Galén S, Jost-Brinkmann PG. B-mode and M-mode ultrasonography of tongue movements during swallowing. J Orofac Orthop. 2010;71(2):125-35. http://dx.doi.org/10.1007/s00056-010-9928-8
    » https://doi.org/10.1007/s00056-010-9928-8
  • 15
    Huang YL, Hsieh SF, Chang YC, Chen HC, Wang TG. Ultrasonagraphic evaluation of hyoid-larinx approximation in dysphagic stroke pacients. Ultrasound Med Biol. 2009;35(7):1103-8. http://dx.doi.org/10.1016/j.ultrasmedbio.2009.02.006
    » https://doi.org/10.1016/j.ultrasmedbio.2009.02.006
  • 16
    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
    » https://doi.org/10.1007/s00415-003-1007-2
  • 17
    Söder N, Miller N. Using ultrasound to investigate intrapersonal variability in durational aspects of tongue movement during swallowing. Dysphagia. 2002;17(4):288-97. http://dx.doi.org/10.1007/s00455-002-0071-6.
    » https://doi.org/10.1007/s00455-002-0071-6
  • 18
    Kim JH, Kim MS. Lateral pharyngeal wall motion analysis using ultrasonography in stroke patients with dysphagia. Ultrasound Med Biol. 2012;38(12):2058-64. http://dx.doi.org/10.1016/j.ultrasmedbio.2012.07.028
    » https://doi.org/10.1016/j.ultrasmedbio.2012.07.028
  • 19
    Hsiao MY, Chang YC, Chen HC, 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
    » https://doi.org/10.1016/j.ultrasmedbio.2012.04.017
  • 20
    Sonies BC, Almajid P, Kleta R, Bernardini I, Gahl WA. Swallowing dysfunction in 101 patients with nephropathic cystinosis: benefit of long-term cysteamine therapy. Medicine (Baltimore). 2005;84(3):137-46.
  • Study conducted at the Department of Physical, Speech and Occupational Therapy, School of Medicine, Universidade de São Paulo and Clinics Hospital, School of Medicine, Universidade de São Paulo – USP – São Paulo, (SP), Brazil.

Publication Dates

  • Publication in this collection
    30 Sept 2014
  • Date of issue
    Oct-Dec 2014

History

  • Received
    12 Feb 2014
  • Accepted
    16 July 2014
Academia Brasileira de Audiologia Rua Itapeva, 202, conjunto 61, CEP 01332-000, Tel.: (11) 3253-8711, Fax: (11) 3253-8473 - São Paulo - SP - Brazil
E-mail: revista@audiologiabrasil.org.br