Ultrasonography and swallowing: a critical review of the
          literature

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

Excluded articles	n
Esophagus-related study	179
US for diagnostic purposes (not specific to deglutition)	44
Used other complementary tests (non-US)	11
US for treatment control	16
Review articles	6
Studies of fetuses	5
US for analysis of other body parts	7
Animal studies	4
US used for surgery control	3
Nonspecific articles	3
US for mastication analysis	1

Reference	Objective	Method	Results and Conclusions
Yabunaka et al., 2011⁽³⁾	To evaluate the movement of the hyoid bone and the changes arising from aging during deglutition in healthy patients using ultrasound.	- 30 adults with no complaints or history of deglutition difficulties divided into three groups: 20-39 years old (5 men and 5 women); 40-59 years old (5 men and 5 women); 60-79 years old (5 men and 5 women). - Variable: trajectory of the hyoid bone (slowly ascending phase, rapidly ascending phase, temporary pause phase and resting position phase) during deglutition of 5 ml of water.	- Mean duration of deglutition increased and peak elevation of the hyoid bone decreased with advancing age. - US can be a quantitative method for clinically evaluating hyoid bone movement during deglutition.
Scarborough et al., 2010⁽²⁾	To explore the parameters of maximum displacement of the hyoid bone during spontaneous deglutition in healthy preschool children using US. To observe whether gender is associated with greater displacement of the hyoid bone.	- 29 subjects (16 boys and 13 girls) with a mean age of 4 years and 2 months, ranging from 3 years to 4 years and 10 months. - Variable: amount of hyoid bone elevation when swallowing two food consistencies (puree and liquid) at three different volumes (0.5, 1.5 and 2.5 ml).	- A significant gender effect was observed for all consistencies and volumes: the mean hyoid bone movement was significantly greater in females. - The study concluded that gender can influence the amount of hyoid bone elevation in children.
Galén & Jost-Brinkmann, 2010⁽¹⁴⁾	To investigate the possibility of using B-mode and M-mode US to differentiate visceral and somatic deglutition.	- 11 patients referred for orofacial myofunctional therapy (for anterior open bite or excessive overjet and visceral deglutition pattern). - B-mode and M-mode US was applied before and after myofunctional therapy. - Variable: the amplitude and speed of the vertical movement of the tongue and total duration of deglutition of saliva (at least 6 deglutition episodes from each participant). - 13 subjects with visceral deglutition pattern and normal occlusion comprised the control group.	- There was wide intraindividual variability in the variables studied, making interindividual comparisons difficult. - The M-mode images determined the amplitude and speed of the vertical movement of the tongue and the total duration of deglutition. - The B-mode images did not identify characteristics that could be designated as only visceral or physiological deglutition movements.
Tamburrini et al., 2010⁽⁵⁾	To determine the role of US in diagnosing dysphagia in patients with amyotrophic lateral sclerosis (ALS).	- 9 patients underwent simultaneous static and dynamic deglutition examinations with US and videofluoroscopy (VDF), respectively: 5 presented with classic ALS and 4 with bulbar ALS; 8 subjects were clinically dysphagic. - Variable: mobility/function of the orofacial myofunctional organs during deglutition, especially during the oropharyngeal phase. - 3 volumes of water (5, 10 and 15 ml) were offered.	- Static phase: 5 patients had tongue atrophy. Abnormal bolus position was observed in 6 patients with US and in 3 patients with VDF. Both techniques identified the inability to maintain the bolus in the oral cavity in 4 patients. - Dynamic phase: decreased tongue movement was observed in 5 patients with US and in 2 patients with VDF. Disorganized movement of the tongue was observed in 3 patients with US and in 2 patients with VDF. - Multiple deglutitions were only visualized with US. The presence of stasis was not observed with US, whereas it was observed in 2 patients with VFS. - US of the tongue is complementary to VDF, as it provides a precise description of the oral phase of deglutition.
Geddes et al., 2009⁽⁶⁾	To develop a rough visualization of infants during breastfeeding using US and to determine the accuracy of the US image of deglutition compared with respiratory plethysmography in a cohort of infants.	- 16 lactating women and their healthy infants participated in the study. The infants were between 24 and 156 days of age (mean of 57 days) and were within the normal parameters of growth for their age (mean of 4871 g). - US was used to examine deglutition, and plethysmography was used to verify breathing. - Variables: duration of deglutition and of deglutition apnea. To measure breathing during deglutition, breast-feeding was recorded.	- US is a noninvasive, accurate method for visualizing the movement of the milk bolus during the pharyngeal phase of deglutition. - Deglutition apnea was identified using US, and the results correlated well with the results of respiratory inductive plethysmography. - The combined use of these techniques has the potential to provide useful information in cases of breastfeeding difficulties.
Jadcherla et al., 2009⁽¹¹⁾	To investigate the pharyngoglottal relationship during basal and adaptive deglutition.	- 12 healthy neonates who were orally fed without structural, chromosomal, or neurological disturbances. - Simultaneous pharyngoesophageal manometry, plethysmography, electromyography (submental) and glottal US were used. - Variables: temporal changes in the kinetics of glottal closure (frequency, response latency and duration) during spontaneous and adaptive pharyngeal deglutition.	- Glottal adduction during basal or adaptive deglutition occurs in any respiratory phase, thus ensuring airway protection before and during deglutition. - The duration of adduction of the pharyngeal-glottal closure reflex suggests a state of glottal hypervigilance in preventing aspiration during deglutition or during events of high gastroesophageal reflux. - Investigation of the pharyngoglottal relationship using noninvasive methods may be more acceptable for patients and is applicable to all ages.
Huang et al., 2009⁽¹⁵⁾	To evaluate the reliability of US in stroke patients with or without dysphagia.	- 55 adults divided into 3 groups: 15 normal (control group); 20 with stroke and without dysphagia (G1); 20 with stroke and with dysphagia (G2). - Variable: distance between the hyoid bone and larynx during deglutition. - Participants had to swallow 3 times with an interval of 1-2 minutes between each deglutition.	- The distance between the hyoid bone and the thyroid cartilage was significantly greater in normal subjects compared with stroke patients and even greater compared with patients with stroke and dysphagia. - The distance between the hyoid bone and the thyroid cartilage during deglutition was significantly smaller in normal subjects than in the stroke group. - The hyoid-larynx approximation was smaller in dysphagic patients with stroke than in stroke patients without dysphagia. - The hyoid-larynx approximation can be quantitatively and reliably evaluated by US using a simple clinical setting.
Welge-Lüssen et al., 2009⁽⁸⁾	To examine whether retronasal olfaction combined with simultaneous gustatory stimuli affects deglutition differently than orthonasal olfaction.	- 47 healthy, non-smoking adults. - US (transducer placed on the floor of the mouth) of deglutition. - Variable: tongue movements (speed and frequency) during deglutition and after the presentation of an olfactory stimulus and latency of deglutition. A sweet taste was presented simultaneously with an essence of an edible food (randomly presented either ortho- or retronasally) using a computer-controlled olfactometer.	- After retronasal stimulation, deglutition occurred significantly more rapidly and more frequently compared with deglutition after orthonasal stimulation. - These results show that an essence of edible food presented as retronasal stimulation in combination with a congruent taste stimulus may influence deglutition.
Komori et al., 2008⁽¹²⁾	To evaluate a new method of bedside deglutition assessment that combined US and videoendoscopy (VED) compared with videofluoroscopy (VDF) alone.	- 8 healthy male volunteers aged 25-31 years with no deglutition disorders. - Simultaneous combined videoendoscopy (VED), US of deglutition and videofluoroscopy of deglutition (VDF). - Variable: laryngeal elevation (beginning, peak and duration).	- The beginning of laryngeal elevation was identified with VDF and US. - After the beginning, the pharynx became invisible with VED. - The peak elevation of the larynx was identified with VDF and US, and this moment was almost identical in both examinations. - The distance and duration of peak laryngeal elevation, measured with US and with VDF, were almost equal and were positively correlated. - This study suggests that the combined technique (US + VED) can demonstrate the deglutition function as efficiently as VDF.
Peng et al., 2007⁽¹³⁾	To evaluate the movement of the tongue during deglutition using a system assisted by M-mode US.	- 55 individuals (30 females and 25 males) with a mean age of 22.7 years (8 to 50 years). - Variable: movement pattern and duration of the activity of the dorsum of the tongue. Three deglutitions of saliva from each subject were evaluated using M-mode US. The images obtained with US were video recorded and evaluated.	- The duration, amplitude and pattern of tongue movements during deglutition varied considerably among individuals. - M-mode US provides valid information about tongue movements without any side effects and is therefore a useful tool in the diagnosis and research of tongue functions in orthodontics and dentistry.
Sonies et al., 2005⁽²⁰⁾	To evaluate the deglutition function of patients with cystinosis, with special attention to the effects of cysteamine treatment.	- 101 patients with nephropathic cystinosis diagnosis. - Oropharyngeal US was used. - Variables: movement of the tongue and of the hyoid bone during deglutition, duration of the oropharyngeal phase of deglutition and movements of the tongue and the hyoid bone needed to initiate and complete deglutition.	- Oral motor dysfunction of deglutition in patients with cystinosis progressively increases with age and is correlated with generalized muscular dysfunction but not with the severity of disease in general. - Long-term therapy of oral cysteamine seems to reduce the severity of oral motor dysfunction and deglutition. - Deglutition dysfunction in patients with cystinosis presents a risk of fatal aspiration and correlates with the presence of muscle atrophy.
Kuhl et al., 2003⁽¹⁶⁾	To noninvasively analyze the vertical movement of the larynx during deglutition using US techniques in patients with dysphagia and in healthy subjects.	- 18 patients (mean age: 63 ± 8 years) with dysphagia caused by neurological diseases. - Control group was composed of 42 healthy subjects (mean age 57 ± 19 years). - Deglutition US was used. - Variables: distance between the hyoid bone and the upper edge of the thyroid cartilage during laryngeal elevation in deglutition.	- Healthy subjects: mean distance of 220 mm (± 30) at rest; the shortest distance during deglutition of 5 or 10 ml of water was 85 mm (± 11), representing a reduction of 61% (± 3) under physiological conditions. - Neurogenic dysphagia patients: the mean relative elevation of the larynx was reduced to only 42% (± 10). - US is a viable, noninvasive method for investigating the elevation of the larynx during deglutition. - US allows direct visualization of the larynx in patients with neurogenic dysphagia.
Söder & Miller, 2002⁽¹⁷⁾	To determine the extent of intrapersonal variability in the duration of tongue movement during deglutition.	- 10 individuals diagnosed with neurogenic dysphagia. - 10 subjects without disturbances and with no diagnosis of dysphagia (control group). - Deglutition US was used. - Variable: total duration of movement of the tongue and the duration of the oral transport phase during deglutition. The subjects were instructed to swallow water and, after 10 seconds, to swallow saliva. The investigation continued in this manner until at least 15 dry deglutitions were recorded.	- The results indicate considerable intrapersonal variability in both groups. - There were no significant differences between groups. - US was a highly suitable technique for the purpose of the study.
Chi-Fishman & Sonies, 2002⁽⁹⁾	To investigate the movement of the hyoid bone during the deglutition of different consistencies.	- 31 healthy individuals (16 male, 15 female) divided into three age groups: 20-39 years, 40-59 years and 60-79 years. - Deglutition US was used. - Variables: hyoid bone movement - duration of the movement, actions, maximum amplitudes, total distances, and peak velocities - analyzed in relation to the variance of viscosity, volume, age and gender. - 612 deglutitions were studied.	- The results showed that older individuals were slower to start deglutition and also presented with higher maximum vertical amplitude, higher total vertical distance and higher peak velocity compared with younger individuals. - Males had higher values for most of the motion parameters. - The results illustrate the importance of examining the relationships among the movement variables to better understand the tasks and strategies of motor control. - The evidence also illustrates the functional adaptation of the infrahyoid muscles and their compensation in healthy elderly adults.
Chi-Fishman & Sonies, 2002⁽¹⁰⁾	To examine the details of the relationships among the kinematic variables to distinguish strategies of hyoid bone movement in discrete deglutition and in fast sequential deglutition.	- 30 healthy subjects divided into three age groups: 20-39 years, 40-59 years and 60-79 years. - Variables: movement, movement duration and maximum amplitude of the hyoid bone. - Changes in the position of the hyoid bone were recorded for a total of 236 discrete deglutitions and 318 rapid sequential deglutitions.	- Rapid sequential deglutitions differ significantly from discrete deglutitions in relation to the movement of the hyoid bone. - When instructed to swallow as quickly as possible, the subjects achieved the smallest movement without increasing the peak speed. This finding suggests greater flexibility in the functional range of movement of the hyoid bone.
Kim & Kim, 2012⁽¹⁸⁾	To analyze the movement of the lateral wall of the pharynx using US.	- 26 individuals with stroke and dysphagia and 15 healthy individuals. - Individuals with stroke and dysphagia were divided into two groups (A and B) based on videofluoroscopy swallow studies (VFSS). In Group A (n = 12), the subjects presented with penetration or aspiration on the VFSS, while in Group B (n = 14), there was no evidence of penetration or aspiration. - Variables: movement of the lateral pharyngeal wall. The movement was assessed by B/M-mode US. - Comparative analysis between the groups and the relationship between movement parameters in the pharyngeal phase was performed.	- The mean pharyngeal displacement in Groups A and B was significantly smaller compared with that of healthy individuals. - The mean duration of pharyngeal movement of Groups A and B was longer than that of healthy individuals. - The mean displacement in Group A was significantly correlated with residue in the vallecula, duration of the delay of pharynx movement and larynx elevation.
Hsiao et al., Jan 2012⁽¹⁵⁾	To measure changes in tongue thickness of and hyoid bone displacement in patients with stroke using US examination in the submental region.	- 60 stroke patients (30 with exclusive alternative feeding and 30 with regular oral intake). - 30 healthy subjects. Another 10 healthy subjects were included to assess the reliability of the examination. - The subjects were instructed to swallow 5 ml of water. During deglutition, videofluoroscopy and US were performed in the mentonian region. The videofluoroscopy exam was complementary to the US for evaluating the displacement of the hyoid bone.	- The changes in tongue thickness and hyoid bone displacement were significantly smaller in stroke patients with exclusive alternative feeding compared with stroke patients with oral intake. - No significant changes were observed between the control group and stroke patients with oral intake in either the tongue thickness or the displacement of the hyoid bone. - US of the submental region showed good reliability and correlated well with videofluoroscopy.

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

Acompanhe os números deste periódico no seu leitor de RSS

[1] Correspondence address: Claudia Regina Furquim de Andrade. R. Cipotânea, 51, Cidade Universitária, São Paulo (SP), Brazil, CEP: 05360-160. E-mail: clauan@usp.br