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(11 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(22 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(33 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(22 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...
,33 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(22 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)(33 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-...
,44 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(22 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...
,55 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(66 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(77 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).
The rationale for the exclusion of 279 citations is provided in Table 1.
DATA ANALYSIS
The 17 citations selected were critically evaluated in terms of their objectives; number, gender and ages of the participants; criteria and evaluation methods; results; and conclusions.
Regarding the criteria and evaluation methods, we sought to assess and describe the methods used in the articles to determine whether there was homogeneity among them.
Regarding the results and conclusions, in addition to the general information the articles provided in these sections, we also noted the advantages and disadvantages of the techniques discussed in each study.
RESULTS
The results of the study are briefly described in Chart 1.
DISCUSSION
After analyzing the selected articles, we observed that the studies that used US to
assess deglutition could be divided into three groups: studies that investigated the
deglutition of healthy individuals (52.9%)(22 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...
,33 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-...
,66 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-...
,88 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-...
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(55 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%)(22 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...
,33 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-...
,55 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-...
,88 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-...
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(55 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(33 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-...
,99 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(88 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(22 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...
,66 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(22 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...
,33 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-...
,99 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(33 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-...
,99 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(88 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(55 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(66 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(33 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(22 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(55 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(66 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.
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» https://doi.org/10.1002/jcu.20733 -
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» https://doi.org/10.1007/s11547-010-0523-2 -
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» https://doi.org/10.1093/chemse/bjp024 -
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» https://doi.org/10.1007/s00455-002-0070-7 -
10Chi-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 -
11Jadcherla 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 -
12Komori 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 -
13Peng 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 -
14Galén 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 -
15Huang 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 -
16Kuhl 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 -
17Söder 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 -
18Kim 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 -
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20Sonies 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.
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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
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Publication in this collection
30 Sept 2014 -
Date of issue
Oct-Dec 2014
History
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Received
12 Feb 2014 -
Accepted
16 July 2014