Archives of Oral Biology 113 (2020) 104706

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Archives of Oral Biology

journal homepage: www.elsevier.com/locate/archoralbio

Description of tongue movements on swallowing patterns T

a a,b a,b a,b,c a,d
Giannina Álvarez , Fernando José Dias , Florencia Lezcano , Alain Arias , Pablo Navarro ,
Ramón Fuentesa,b,*
a
Research Centre in Dental Sciences (CICO), Dental School, Universidad de La Frontera, Temuco, Chile
b
Department of Integral Adults Dentistry, Dental School, Universidad de La Frontera, Temuco, Chile
c
Research Group of Health Sciences, Faculty of Health Sciences, Universidad Adventista de Chile, Chillán, Chile
d
Universidad Autónoma de Chile, Chile

A R T I C LE I N FO A B S T R A C T

Keywords: Objective: The purpose of this study was to compare the different swallowing patterns regarding tongue
Deglutition movement during saliva swallowing in healthy participants.
Saliva Design: Seventeen participants (23.0 ± 3.6 years old) were included in this cross-sectional study. The movement
Articulography of the tongue (anterior, middle and posterior portions) on the three axes of space (inferior-superior, anterior-
Swallowing patterns
posterior and medial-lateral) was recorded using a 3D electromagnetic articulograph. The tongue movement
Tongue movements
patterns registered during saliva swallowing were classified according to Bourdiol et al. (2014) into Type I, II or
III.
Results: Three swallowing patterns were identified (Type I, 64.7 %; Type II, 5.9 %; and Type III, 29.4 %). On the
anterior-posterior axis, the displacement of the three portions of the tongue was significantly higher in Type III
pattern compared with the Type I pattern. Furthermore, on the superior-inferior axis, the displacement of the
anterior portion was significantly higher in Type III pattern compared with Type I pattern. In Type I pattern, on
the inferior-superior axis, the smallest range of displacement occurred in the anterior portion of the tongue,
followed by the middle and, finally, the posterior portion.
In the analysis of Type III swallowing pattern, no significant differences were found on the range of dis-
placement of the tongue portions on the three axes.
Conclusion: Statistical differences were found between swallowing patterns Type I and III regarding tongue
movement. The frequency of pattern II found in the participants of this study was not high enough to compare
the three patterns. However, the results obtained indicate that the methodology applied could be used to identify
the patterns based on quantitative data.

1. Introduction
Deglutition is a dynamic process which involves coordinated ac-
tivity of the anatomical structures involved in the transport of food,
water and saliva from the mouth to the stomach, while protecting the
airway (Dodds, Stewart, & Logemann, 1990; Miller, 1982). This process
is commonly divided into four phases: oral preparatory, oral, phar-
yngeal and oesophageal, according to the anatomical location of the
bolus during transport (Dodds et al., 1990). This division into isolated
phases (Martin-Harris, Michel, & Castell, 2005) applies principally to
the biomechanics of the deglutition of liquids, which differs from the
deglutition of solid foods (Dua, Ren, Bardan, Xie, & Shaker, 1997;
Matsuo & Palmer, 2009).
Different patterns have been described for the oral phase, using
different diagnostic methods, to study the deglutition of liquids or
saliva under normal conditions in the absence of motor functions al-
terations (Bourdiol, Mishellany-Dutour, Peyron, & Woda, 2014;
Chuhuaicura et al., 2018; Dodds et al., 1989; Kieser et al., 2014).
Various techniques are available to study deglutition (Álvarez, Dias,
Lezcano, Arias, & Fuentes, 2019; Chuhuaicura et al., 2018; Steele & Van
Lieshout, 2004; Steele, 2015) and their usefulness depends on the as-
pects of deglutition being assessed (Steele, 2015). Videofluoroscopy is
the gold standard, however it requires exposing the participant to io-
nizing radiation (Zammit-Maempel, Chapple, & Leslie, 2007), and the
visualization of tongue movement is restricted (Steele, 2015). With
electromagnetic articulography (EMA) on the other hand, the position

⁎
Corresponding author at: Research Centre in Dental Sciences (CICO), Dental School, Universidad de La Frontera, Av. Francisco Salazar 01145, casilla 54-D, Zip
Code: 4811230, Temuco, Chile.
E-mail address: ramon.fuentes@ufrontera.cl (R. Fuentes).

https://doi.org/10.1016/j.archoralbio.2020.104706
Received 23 September 2019; Received in revised form 25 February 2020; Accepted 6 March 2020
0003-9969/ © 2020 Published by Elsevier Ltd.
G. Álvarez, et al. Archives of Oral Biology 113 (2020) 104706

Fig. 1. 3D EMA AG501 and sensors distribution. a Participant in a recording session with sensors (3 mm diameter) placed on the cutaneous points of the right (1) and
left (2) mastoids, glabella (3) and thyroid cartilage (4) b. Sensors on the tongue in the anterior (5), middle (6) and posterior (7) portions c. Palate contour with sensor
(8) on a wooden stick.

of structures in movement can be easily recorded and a larger amount & Farronato, 2014; Smithpeter & Covell, 2010).
of quantitative data can be obtained without biological risk, quantifying The purpose of this study was to compare the different swallowing
tongue movement with greater temporal and spatial accuracy (Steele & patterns regarding tongue movement during saliva swallowing in
Van Lieshout, 2004). healthy participants.
Dodds et al. (1989) who used videofluoroscopy, reported that two
patterns exist for liquid deglutition. The first is the Tipper pattern, 2. Materials and methods
which begins with the bolus in a supralingual position and the tongue
tip against the palatal surface of the upper incisors or the maxillary 2.1. Participants
alveolar crest. The pattern is classified as High, Intermediate or Low
Tipper, depending on the initial position of the tongue tip. The second This study evaluated 17 volunteers (8 male and 9 female), aged over
pattern, or Dipper type, implies that the bolus, positioned in the ante- 18, without alterations in the functions of speech, respiration or de-
rior sublingual region, is moved to a supralingual position by the glutition, without craniofacial and dento-maxillary alterations, who
downward and upward movement of the apex of the tongue. Then, for agreed to participate in the study and signed an informed consent to
both patterns, the bolus is displaced towards the oropharynx by a that effect. This study was approved by the Scientific Ethics Committee
movement of tongue propulsion (Dodds et al., 1989). of Universidad de La Frontera (Folio no. 001/2017). Prior to inclusion
Kieser et al. (2011) defined three basic swallowing patterns, eval- in the study, the participants completed a basic health questionnaire
uating changes in intraoral pressures during the deglutition of water (anamnesis), a questionnaire to discard dysphagia (EAT-10: Eating
and saliva. They reported that the Type I or Squeezer pattern is char- Assessment Tool (Peláez et al., 2012)) and a screening questionnaire for
acterised by a progressive increase in intraoral pressure, which is signs and symptoms of temporomandibular disorders (Corsini et al.,
generally positive, from the anterior to the posterior sector, with an 2005). They were also subjected to clinical evaluation.
immediate decline. The Type II or Slider pattern is characterised by the
increase, maintenance and gradual decline of intraoral pressure. The
2.2. Recording of saliva swallowing
Type III or Slapper pattern is characterised by large fluctuations be-
tween positive and negative pressures, reaching greater values than in
AG501 3D electromagnetic articulograph was used to record saliva
Types I and II (Kieser et al., 2011).
swallowing. This equipment is capable to record the movements of
Finally, Bourdiol et al. (2014) identified three elemental saliva de-
sensors positioned on structures in the head and neck of participants in
glutition patterns by use of 2D electromagnetic articulography. The
three dimensions (Z axis: inferior-superior, Y axis: medial-lateral and X
Type I pattern is characterised by elevation of the mandible and tongue
axis: posterior-anterior) and in real time.
towards the palate, displacing the saliva towards the pharynx, similar to
Eight articulograph sensors (HQ220-L120-B, Carstens
the Tipper of Dodds et al. (1989) and the Squeezer of Kieser et al.
Medizinelektronik, Germany) were used on the recording sessions ac-
(2011). In the Type II pattern, similar to the Dipper of Dodds et al.
cording to the protocol previously reported by Álvarez, Dias, Lezcano,
(1989), the middle third is further away from the palate when it des-
Arias, & Fuentes, 2019. Seven sensor were glued on different anato-
cends, adopting a spoon shape, while the anterior and posterior thirds
mical points on the head and neck of the participant using a bio-
are in contact with the palate. Then the middle third is raised quickly,
compatible tissue adhesive (Epiglu®, Meyer-Haake, Germany) (Fig. 1A,
impelling the bolus towards the pharynx as the posterior third of the
B). The eighth sensor was attached to the tip of a wooden stick. This last
tongue descends. In the Type III pattern, deglutition starts with the
sensor was used to contour the palate of each participant in the mid-
descent of all three thirds of the tongue, which are then raised si-
sagittal plane (Fig. 1C). The contouring of the palate was carried out at
multaneously towards the palate (Bourdiol et al., 2014).
the beginning of the recording session before deglutition-tasks re-
In swallowing studies, the characterization of tongue movement and
cording. The purpose of the contouring was to have a reference profile
its interaction with the palate in healthy subjects provides a baseline
of the palate to combine with the position of the tongue during de-
necessary for the diagnosis and evaluation of patients with alterations
glutition registered in the next recordings. This individual recording
in their oral functions such as chewing (Iizumi, Yoshino, Kagaya, Hori,
was done with the help of a trained operator in order to register the
& Ono, 2018), swallowing (Kahrilas, Lin, Logemann, Ergun, & Facchini,
sagittal profile of the palate from the basis of the uvula to the incisive
1993; Yagi, Fukuyama, & Soma, 2008), phonetics (Stone, Epstein, &
papilla when the participants were with their mouth open. To eliminate
Iskarous, 2004) and breathing (Wang, Di, Mona, Wang, & Hans, 2018).
the participants' head movements from the all recordings, the Head
Moreover, morphofunctional alterations of structures of the oral cavity
Correction function of the AG501 articulograph was previously used to
can be related with these analyses (Cheng, Peng, Chiou, & Tsai, 2002;
establish a reference system in the craniofacial structure (sensors 1, 2
Garrett, Araujo, & Baker, 2016; Maspero, Prevedello, Giannini, Galbiati,
and 3) (Álvarez, Dias, Lezcano, Arias, & Fuentes, 2019; Fuentes, Arias,

2
G. Álvarez, et al.
Saravia, Lezcano, & Dias, 2017).
After the registration of the sagittal profile of the palate, each par-
ticipant was asked to concentrate on his/her breathing and listen to
music for 5 min. During this period, three recordings were made with
the EMA, of one minute each, in order to record tongue movement
during non-induced, spontaneous saliva deglutition. The participant
was not warned exactly when the recordings were being made.
2.3. Data processing and determination of swallowing patterns
The movement recordings made with the articulograph were ex-
ported as binary files (.pos) and then processed with the MATLAB®
software (MathWorks Inc., USA) by elaboration of specific scripts. This
allowed us to obtain graphics of position vs. time for each sensor on the
tongue and on the three spatial axes (inferior-superior, medial-lateral,
and anterior-posterior). These graphics show the displacement of the
tongue on each axis, and in the case of the inferior-superior axis, the
distance from the palate. Finally, the displacement ranges (mm) of each
sensor on the tongue were calculated for the different axes and the
mean of the three recordings was used for the analysis.
To determine the swallowing patterns in each of the EMA record-
ings, the position vs. time graphics of the inferior-superior axis of each
tongue sensor were analysed. The graphics represented the behaviour
of the tongue during one minute, when generally one or more sponta-
neous deglutition of saliva might occur. The tongue movement re-
cording was only included in this analysis if at least one deglutition
occurred. In the recordings in which more than one deglutition oc-
curred, the most clearly defined deglutition was included in the ana-
lysis. The identification of the swallowing event in the graphs is similar
to that observed in real time on the monitor, the initial position of the
tongue, the displacement while swallowing and the return to the initial
position are observed. The movement of the thyroid was also included
as a reference, sometimes very marked and sometimes very subtle,
because it depends on how much the sensor on the skin moves.
Therefore the identification is mainly due to the change in the initial
position of the tongue. The swallowing pattern was determined using
the classification of Bourdiol et al. (2014), according to the sequence of
movements of the different portions of the tongue during swallowing.
2.4. Statistical analysis
The data collected were organized in an Excel spreadsheet
(Microsoft Office Excel 2013) and saved. A descriptive analysis of the
data was prepared by determining the means and standard deviations.
The Shapiro-Wilk test was used to determine the normality of the data,
the t-test for independent samples, one-way ANOVA, Bonferroni's post
hoc test for multiple comparisons and Kruskal-Wallis test were applied.
The data analysis was carried out using the software IBM SPSS Statistics
(version 23.0). A value of p < 0.05 was chosen as the threshold for
significance.
3. Results
The mean age of the participants was 23.0 ± 3.6 years (23 ± 3.5
years for men and 23 ± 3.9 years for women). The 64.7 % (n = 11) of
the participants presented the Type I swallowing pattern (Fig. 2A), 5.9
% (n = 1) presented Type II (Fig. 2B), and 29.4 % (n = 5) presented
Type III (Fig. 2C). Only type I and type III swallowing patterns were
compared, the type II swallowing pattern is less frequent and in this
study there is only one case.
Regarding the mean displacement range of the tongue portions and
the three axes, no significant difference was found between men and
women.
Table 1 shows the mean displacement ranges of the three portions of
the tongue for the spatial axes by type of swallowing pattern.
On the inferior-superior axis, the mean range of displacement of the
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Archives of Oral Biology 113 (2020) 104706
anterior portion was smallest in Type I, and larger still in Type III (p =
0.022, t-test). No significant difference was found between swallowing
patterns type I and type III regarding the range of displacement of the
middle and posterior portions (p = 0.059, p = 0.151 respectively, t-
test).
On the anterior-posterior axis, the range of displacement of the
anterior, middle and posterior portions were significantly greater in the
Type III pattern than the Type I (p = 0.020, p = 0.002 and p = 0.009
respectively, t-test).
Finally, on the medial-lateral axis, no significant difference was
found between swallowing patterns type I and type III for the range of
displacement of the anterior, middle and posterior portions (p = 0.081,
p = 0.057 and p = 0.214 respectively, t-test).
Statistical differences were found among the ranges of displacement
of each portion within type I swallowing pattern (inferior-superior, p =
0.001; medial-lateral, p = 0.001; anterior-posterior, p = 0.002;
ANOVA). On the inferior-superior axis, the smallest range of displace-
ment occurred in the anterior portion of the tongue, followed by the
middle and finally the posterior portion; there were significant differ-
ences between all three portions (anterior vs middle, p = 0.007;
anterior vs posterior, p < 0.001; middle vs posterior, p = 0.017;
Bonferroni test). The anterior-posterior axis the displacement range was
significantly smaller in the anterior portion than in the middle (p =
0.014; Bonferroni test) and posterior portions (p = 0.003, Bonferroni
test). Finally, for the medial-lateral axis the displacement range was
significantly greater in the posterior portion than in the anterior
(p < 0.001, Bonferroni test) and middle portions (p = 0.012,
Bonferroni test).
In the analysis of Type III swallowing pattern, no significant dif-
ferences were found on the range of displacement of the tongue por-
tions in the superior – inferior axis (p = 0.075, Kruskal-Wallis test),
anterior - posterior axis (p = 0.105, Kruskal-Wallis test) and medial –
lateral axis (p = 0.878, Kruskal-Wallis test).
4. Discussion
The tongue and its interaction with the palate play a key role in
swallowing. The tongue is one of the most complex and least under-
stood musculoskeletal organs of the body (Palmer, Hiiemae, & Liu,
1997); its biomechanics can be compared to a muscular hydrostat based
on hydraulic principles (Kier & Smith, 1985; Sanders & Mu, 2013).
Studying the tongue under physiological or non-physiological condi-
tions is even more complex because it is contained within the oral
cavity.
We used 3D EMA, which is an innocuous and replicable technique,
to obtain more precise data and with a greater temporal and spatial
resolution (Fuentes et al., 2017) of lingual kinematics in three planes.
The lingual movement has been studied mainly in the sagittal plane
(Bourdiol et al., 2014; Dodds et al., 1989); and also in the frontal plane
(Mikushi, Seki, Brodsky, Matsuo, & Palmer, 2014). However, medial-
lateral plane quantitative analysis as well its relationship with other
two movement planes were not found. Our previous study was the only
one that characterized quantitatively the tongue movements during
water and saliva swallowing in medial-lateral plane (Álvarez, Dias,
Lezcano, Arias, & Fuentes, 2019).
The present study provides innovative data on the displacement
ranges of the tongue in three anatomical planes, the delimitation of the
palate, and the identification of lingual movement patterns in saliva
swallowing on the inferior-superior axis. Confirming the independence
of movement found in different parts of the tongue (Tasko, Kent, &
Westbury, 2002), its action was analysed in the anterior, middle and
posterior portions (Bourdiol et al., 2014; Kennedy et al., 2010; Steele &
Van Lieshout, 2004; Steele & Van Lieshout, 2009).
The movements of the different portions of the tongue and the se-
quence of how these interact to transport the bolus of saliva were
translated into the swallowing patterns proposed by Bourdiol et al.
G. Álvarez, et al. Archives of Oral Biology 113 (2020) 104706

Fig. 2. Tongue movements on the inferior-superior axis in the different swallowing patterns. Graphs of displacement (mm) vs time (s) in the inferior-superior axis of
the anterior, middle and posterior tongue portions, during spontaneous saliva swallowing (1 min) used to determine the saliva swallowing pattern according to
Bourdiol et al. (2014) The black lines dotted on each graph represent the palate and its relation to the tongue. In the red box the selected swallowing event is shown to
determine the type of pattern. 2A. Pattern type I, greater displacement of middle and posterior portions. 2B. Pattern type II greater downward displacement of the
middle portion of the tongue. 2C. Pattern type III, simultaneous displacement of the three tongue portions. (For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article).

(2014). Our data agree with Dodds et al. (1989) that the “Tipper pat-
tern” (Type I) is the most frequent; however our results differ with
Bourdiol et al. (2014), who found a Type II pattern frequency (43.4 %)
similar to Type I frequency (41.5 %), while Type III (15.1 %) presented
the lowest frequency. In a previous study conducted by our research
group, we found a lower frequency of the type II pattern (14.3 %) and
higher frequencies of the type I (35.7 %) and III (50 %) patterns
(Álvarez et al., 2019Álvarez, Dias, Lezcano, Arias, & Fuentes, 2019).
These differences could be explained by the characteristics of our
population differences and also due to use of the AG501 3D EMA
technique. In addition, the delimitation of the palate may be another
critical difference, allowing the precise shape of the hard and soft palate

4
G. Álvarez, et al.
Table 1
Mean and standard deviation of the displacement range (mm) of the tongue
portions in different axes according to the type of swallowing pattern.
Type I Type III
Inferior – Superior axis
Anterior portion 2.98 ± 1.39 I,a,b 7.60 ± 2.97 I
Middle portion 7.54 ± 3.93 a,c 11.88 ± 3.88
Posterior portion 11.62 ± 3.97 b,c 15.10 ± 5.43
Anterior – posterior axis
Anterior portion 3.30 ± 2.45II,d,e 7.78 ± 4.49II
Middle portion 6.54 ± 2.78III,d 13.02 ± 4.05III
Posterior portion 7.16 ± 2.19IV,e 11.26 ± 3.11IV
Medial – lateral axis
Anterior portion 1.95 ± 0.87f 4.29 ± 2.27
Middle portion 2.54 ± 0.49g 4.67 ± 1.81
Posterior portion 3.79 ± 1.27f,g 4.78 ± 1.70
The statistical differences are presented with the letters a–g in the columns and
with numerals I - IV in the rows.
of each participant to be determined. This produced an accurate re-
presentation of the tongue-palate relationship during deglutition, de-
fining the relationship of the different portions of the tongue with the
palate and allowing the type of pattern to be defined. It should also be
considered that the determination of swallowing patterns in these stu-
dies (Álvarez et al., 2019Álvarez, Dias, Lezcano, Arias, & Fuentes, 2019;
Bourdiol et al., 2014; Dodds et al., 1989) was performed based on the
visual analysis of generated graphics and recorded videos.
The relationship with the types of swallowing pattern was estab-
lished according to a quantitative analysis of the displacement ranges of
the portions of the tongue. In Type I, greater contact with the palate
was observed on the inferior-superior axis; the anterior portion of the
tongue maintained a more superior position when swallowing, pre-
senting the lowest range of displacement as it does not need to descend
to collect saliva. A soft, undulating movement of the middle portion of
the tongue, which presents its smallest displacement in this pattern,
allows the posterior portion of the tongue to make its greatest dis-
placement, propelling the bolus towards the pharynx. The smaller dis-
placement of the anterior portion of the tongue on the anterior-pos-
terior axis was corroborated in our study; while on the medial-lateral
axis the posterior portion presented the greatest displacement, although
this is smaller than found in the other patterns.
In Type III, the three portions of the tongue descend and ascend
simultaneously. Nevertheless, the greatest range of displacement of the
anterior portion was recorded in Type III, which corroborates greater
displacements in this pattern. For the anterior-posterior axis, Type III
presents greater displacements of all portions of the tongue than Type I.
The study is subject to limitations, mainly that the methodology
applied is restricted to the oral phase of deglutition. Diagnostic tech-
niques can be combined to evaluate the other phases and the whole
process, however, our purpose was focused on this phase and on tongue
movement. Furthermore, the presence of cables attached to the sensors
limits the study of deglutition to liquid and semi-liquid consistencies,
which do not involve chewing and possible damage to the cables.
Moreover, EMA sensors, however miniaturized, have a volume that
could potentially change the tongue-palate perception.
In conclusion, the classification of the saliva swallowing records
into different patterns was corroborated with quantitative data on the
articulation of the tongue's movement and its relation with the palate.
Unlike other studies that only consider the tongue's interaction with the
hard palate, we included both, the hard and the soft palate, in order to
observe the complete tongue-palate interaction. These findings will
allow us to explore the variability of deglutition in different age groups,
with different consistencies, textures and volumes of bolus. The meth-
odology used could be also applied in diagnosis and treatment of people
with swallowing disorders.
Looking forward, we project to further improve our methods and
5
Archives of Oral Biology 113 (2020) 104706
analysis developing new protocols and data processing tools to exploit
the potential of this technology in the study of swallowing. Our future
efforts will be focus on develop a more comprehensive three-dimen-
sional analysis of the tongue movements placing sensors not only in the
sagittal line but also in lateral areas that are also contacting with the
palate and teeth. This develop will allow us to obtain more detailed
kinematic parameters such as spatial trajectory-length and velocity.
CRediT authorship contribution statement
Giannina Álvarez: Conceptualization, Methodology, Investigation,
Resources, Writing - original draft, Writing - review & editing, Project
administration, Funding acquisition. Fernando José Dias:
Visualization, Writing - original draft. Florencia Lezcano:
Methodology, Visualization, Software, Writing - review & editing. Alain
Arias: Visualization, Writing - original draft. Pablo Navarro: Formal
analysis. Ramón Fuentes: Conceptualization, Supervision, Writing -
review & editing.
Declaration of Competing Interest
The authors declare that there is no conflict of interest.
Acknowledgements
The authors have received support from Red Estatal de Odontología
de Chile. This work is part of project DIE18-0001.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.archoralbio.2020.
104706.
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