Computers in Biology and Medicine 145 (2022) 105446

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Computers in Biology and Medicine

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

Two dimensional computational model coupling myoarchitecture-based

lingual tissue mechanics with liquid bolus flow during
oropharyngeal swallowing
Dana M. Leichter a, b, Nicole E. Stark c, Owen P. Leary b, d, Martin B. Brodsky e,
Richard J. Gilbert b, d, 1, Mark A. Nicosia c, 1, *
a
Center for Biomedical Engineering, Brown University, Providence, RI, 02912, USA
b
Research Service, Providence VA Medical Center, Providence, RI, 02908, USA
c
Department of Mechanical Engineering, Widener University, Chester, PA, 19013, USA
d
Department of Pathology and Laboratory Medicine, Warren Alpert Medical School of Brown University, Providence, RI, 02903, USA
e
Department of Physical Medicine and Rehabilitation, Johns Hopkins University, USA

A R T I C L E I N F O A B S T R A C T

Keywords: Biomechanical relationships involving lingual myoanatomy, contractility, and bolus movement are fundamental
Swallowing properties of human swallowing. To portray the relationship between lingual deformation and bolus flow during
Lingual myoarchitecture swallowing, a weakly one-way solid-fluid finite element model (FEM) was derived employing an elemental mesh
Computational modeling
aligned to magnetic resonance diffusional tractography (Q-space MRI, QSI) of the human tongue, an arbitrary
Lagrangian-Eulerian (ALE) formulation with remeshing to account for the effects of lingual surface (boundary)
deformation, an implementation of patterned fiber shortening, and a computational visualization of liquid bolus
flow. Representing lingual tissue deformation in terms of its 2D principal Lagrangian strain in the mid-sagittal
plane, we demonstrated that the swallow sequence was characterized by initial superior-anterior expansion
directed towards the hard palate, followed by sequential, radially directed, contractions of the genioglossus and
verticalis to promote lingual rotation (lateral perspective) and propulsive displacement. We specifically assessed
local bolus velocity as a function of viscosity (perfect slip conditions) and observed that a low viscosity bolus (5
cP) exhibited maximal displacement, surface spreading and local velocity compared to medium (110 cP, 300 cP)
and high (525 cP) viscosity boluses. Analysis of local nodal velocity revealed that all bolus viscosities exhibited a
bi-phasic progression, with the low viscosity bolus being the most heterogeneous and fragmented and the high
viscosity bolus being the most homogenous and cohesive. Intraoral bolus cohesion was depicted in terms of the
distributed velocity gradient, with higher gradients being associated with increased shear rate and bolus frag­
mentation. Lastly, we made a sensitivity analysis on tongue stiffness and contractility by varying the degree of
extracellular matrix (ECM) stiffness through effects on the Mooney-Rivlin derived passive matrix and by varying
maximum tetanized isometric stress, and observed that a graded increase of ECM stiffness was associated with
reduced bolus spreading, posterior displacement, and surface velocity gradients, whereas a reduction of global
contractility resulted in a graded reduction of obtainable accommodation volume, absent bolus spreading, and
loss of posterior displacement. We portray a unidirectionally coupled solid-liquid FEM which associates
myoarchitecture-based lingual deformation with intra-oral bolus flow, and deduce that local elevation of the
velocity gradient correlates with bolus fragmentation, a precondition believed to be associated with aspiration
vulnerability during oropharyngeal swallowing.

* Corresponding author. Department of Mechanical Engineering, School of Engineering, Widener University, One University Place, Chester, PA, 19013, USA.
E-mail address: manicosia@widener.edu (M.A. Nicosia).
1
Shared senior author.

https://doi.org/10.1016/j.compbiomed.2022.105446
Received 22 December 2021; Received in revised form 13 March 2022; Accepted 21 March 2022
Available online 25 March 2022
0010-4825/© 2022 Elsevier Ltd. All rights reserved.
D.M. Leichter et al.
1. Introduction
The human swallow is an instinctive and precisely orchestrated
event, whose principal goal is to transport ingested fluids and food from
the mouth to the esophagus [1,2]. Central to this process is the
force-generating deformation exhibited by the tongue, a structurally
intricate and functionally versatile muscular organ. The study of lingual
structure and function has long been impeded by the complexity of its
fiber organization and associated mechanics. To address this limitation,
we developed multiscale diffusional magnetic resonance imaging and
computational methods that depict the tongue’s anatomy as an array of
oriented fiber-like structures (Q-space MRI, QSI) [3] which, in the
aggregate, form an anatomical template for purposeful modifications of
tissue configuration [4–8]. Through this approach, we demonstrated
that the human tongue modifies its shape through a series of local de­
formations [9,10] that together impart pressure to the contained bolus,
and under normal conditions, promote cohesive flow [11–15]. Owing to
the high level of structural redundancy exhibited by the tissue’s orga­
nization [16,17], we have modeled the tongue as a continuous material
with anisotropic properties templated to its myoarchitecture [18,19]
and then modified this formulation to include its microscopic material
characteristics [20]. However, these and other models have not explic­
itly related the properties of the deforming tongue to the consequential
flow of the fluid bolus.
Prior studies have modeled oropharyngeal fluid mechanics using
finite element, finite volume, or particle methods [14,15,21–27] inten­
ded to specify the forces applied to the bolus by the oropharyngeal
musculature [28] or by mechanical systems designed to emulate the
deforming lingual surface (see below). One such approach simulated the
rolling deformation of the tongue surface against the hard palate
through the rotation of a mechanical device extending from a pivoting
arm to derive time-variant bolus velocity as a function of bolus rheology
[12,29]. An alternative approach depicted the oropharynx as a pres­
surized container [30] and demonstrated bolus flow dynamics based on
flow imaging and manometry-derived bolus pressure [31]. Considerable
research has, moreover, examined the interactions between bolus
rheology and tongue-related bolus displacement [32,33]. Extending
previous research relating bolus rheology, intra-oral containment and
flow [22,34], and finite element models (FEMs) of lingual mechanical
function based on architectural anatomy [19,20], we now seek to
demonstrate the effect of dynamic lingual surface deformation resulting
from patterned contractility of the tongue on the fluid mechanics of
intra-oral bolus flow in the mid-sagittal plane. Our goal is to demon­
strate a 2D partially coupled solid-fluid model of oropharyngeal swal­
lowing that relates myoarchitecture-derived lingual deformation to
liquid bolus flow. The output of such a model would not be limited to the
relationship of surface motion and fluid mechanics, but, moreover,
would define the relationship between underlying patterns of muscular
anatomy with bolus flow through architecture-dependent lingual me­
chanical properties. We expect that this distinction will be important in
the setting of lingual myopathology, where structure-function relation­
ships reflecting the interface of anatomy and bolus flow may be
exceedingly complex. Our supposition is that abnormal contraction
patterns exhibited by pathological lingual tissue, derived in part on its
underlying myoarchitecture and material properties, will predict aber­
rant patterns of bolus flow.
2. Methods
2.1. Overall computational strategy
The goal of the current model was to predict patterns of bolus flow in
response to simulated lingual contraction and surface deformation
during the accommodative and propulsive phases of human swallowing.
This model provides unidirectional coupling of a solid mechanics model
of lingual contractility with intraoral bolus flow. The elements of the
2
Computers in Biology and Medicine 145 (2022) 105446
lingual model are aligned with fiber architecture derived from diffusion
tensor magnetic resonance imaging (DTI) and tractography, a Q-space
MRI based model. In a previous study, we employed diffusion weighted
MRI methods, developed in the Gilbert laboratory [35–39], to depict the
underlying myoarchitecture of the human tongue for use as a geometric
template to support finite element (FE) mesh generation, and then use
the myofiber tractography depiction from that study to define fiber
orientation within each element of the FE mesh in the current model.
The development of a partially coupled solid-fluid model (Fig. 1) was
accomplished by the adaptation of DTI-derived fiber tractography to an
aligned mesh, the implementation of lingual mechanical activity using a
model of tissue mechanics, the extraction of the deforming lingual sur­
face, and the simulation of bolus motion.
2.2. Assumptions of partially coupled solid-fluid model
The physiological and biomechanical assumptions employed in the
current model include: 1) The model depicts the accommodative and
propulsive phase of the swallow, marked by the initial association of the
tongue tip with the hard palate through expansion anteriorly and su­
periorly, followed by anterior-posterior lingual surface of deformation
and secondary clockwise rotation of the tongue (from the lateral
perspective), with the resulting effect being transit of the fluid bolus
within the oral cavity across the tongue surface and from the oral cavity
to the pharynx. 2) The anterior-inferior tongue is rigidly associated with
the genioid process through the attachment of the genioglossus, while
the anterior tip of the tongue is opposed to the hard palate through the
initial stages of the swallow. 3) The tongue is elastically constrained
(without imposition of contractile force) from the posterior (via the
styloglossus) and the inferior (via the hyoglossus) directions. 4) The
bolus is comprised of liquid material whose shape is formed by the air-
fluid interface (superior) and a deformable solid-liquid interface
constituted by the lingual surface (inferior). 5) The bolus is considered
to have no mechanical effects on lingual surface deformation. 6) The
model is developed, for the purposes of simplification, in two di­
mensions only, that is, the myoarchitecture and derived mechanical
functions occurring in the mid-sagittal plane are included in the model,
and events occurring in planes lateral to the midline, for example,
contractions of the transversus, hyoglossus, and styloglossus muscles
that would be expected to affect the shape of the bolus, the depth of its
concavity, and the net force applied to the bolus during retrograde
displacement are excluded.
2.3. Myoarchitecture-templated solid model of deglutitive lingual
deformation
To model lingual deformation during deglutitive accommodation
and propulsion, a planar, 2D finite element model (FEM) of the tongue
was developed, based, in part, on a model previously published by the
Gilbert laboratory [19] (Fig. 2). The Abaqus pre-processor was used to
generate a finite element mesh from the geometric model (3960 nodes
and 1871 elements) and DTI tractography data were used to define the
local muscle fiber orientation within each element based on multivoxel
aligned fiber arrays. Material properties and activation properties were
applied to each element based on previously published assumptions
[19]. Once configured, the mesh was exported from Abaqus into FEBio
[40], where swallow-specific mechanical simulations were performed
(as defined below). FEBio solves the weak form of the momentum bal­
ance equation using a nonlinear finite element method. The material
properties of muscle were modeled as an anisotropic, incompressible
hyperelastic continuum, with nonlinear material properties. The total
stress within the tissue was decomposed into an isotropic matrix and a
fiber-aligned active contractile stress according to Ref. [41]:
σ = σ p + Ta a ⊗ a
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 1. Model development coupling lingual contractility, surface deformation and intra-oral bolus flow. The following sequence was used to generate a
model associating myoarchitecture-derived lingual tissue deformation with intra-oral bolus flow. A) DTI tractography obtained from normal volunteers was used to
depict the underlying myoarchitecture of the human tongue. (Figure 1A adapted from reference [39].) B) DTI-based myoarchitecture served as a geometric template
aligning elements within a mesh in order to simulate soft tissue mechanics based on the time-varied activation functions of the imaged muscle groups. (Figure 1B
adapted from reference [19].) C) The lingual surface deformation resulting from patterned lingual fiber contractions served as the basis for intra-oral bolus flow that
was represented by a distributed velocity profile specific to its rheology.

Fig. 2. Solid phase finite element (FE) model generation spatially templated from DTI tractography. A) A human swallow is portrayed as a sequence of mid-
sagittal images of lingual deformation acquired at 10-Hz using magnetic resonance imaging, and displaying the phases early accommodation, late accommodation
and propulsion (Figure 2A adapted from reference [9].) B) DTI tractography with FE mesh overlaid, demonstrating the points of insertion of the hyoglossus (hg),
geniohyoid (gh), styloglossus (sg), and genioglossus (gg). Yellow lines indicate individual muscle fiber groups for which activation functions and mechanical
properties are assigned. (Figure 2B adapted from reference [19].) C) FE mesh with each colored section representing different muscle fiber groups. Fiber alignment
was assigned for each muscle group based on the principal diffusion direction of the underlying DTI tractography image. Muscle activation functions used to simulate
the human swallow were specified for each muscle group at discrete time points as a fraction of the isometric force relative to the maximum active force that can be
generated for a given fiber length.

where σ p is due to the passive elastic stress Ta denotes the active fiber
where c10 and c01 are empirically determined material constants, I1 and
stress, and a is a unit vector along the deformed fiber direction. The
I2 are invariants of the deviatoric portion of the right Cauchy-Green
passive stress was modeling using a two-parameter Mooney-Rivlin
deformation tensor, K is the bulk modulus, and J is the Jacobian of
model [41–43], whose strain-energy density, W, is given by
the deformation gradient. The active fiber stress was modeled using a
1 Hill-type formulation [44–46], which includes only the contractile
W = c10 (I 1 − 3) + c01 (I 2 − 3) + K(ln J)2
2 element, with passive elastic behavior from the Mooney-Rivlin model.
Muscle activation functions were specified at discrete time points in the

3
D.M. Leichter et al.
accommodative and propulsive sequence, denoting the fraction of iso­
metric force relative to maximum active force that could be generated
for a given set of fibers. Since the architectural complexity of the lingual
tissue precludes an exact knowledge of fiber activation history, an in­
verse approach was employed to approximate activation functions
distributed throughout the tissue from a known set of global de­
formations associated with FE groups of similar myofiber alignment
[19].
We depict the following sequence of biomechanical events: 1) su­
perior bending and elevation of the tongue tip and its apposition to the
hard palate through longitudinal expansion directed to the hard palate,
derived from prior demonstration of tongue bending [7–9], so con­
structing a midline concavity to accommodate the fluid bolus, and 2)
sequential posterior-directed hydrostatic deformation of the tongue
accomplished by serial activation (antero-superior to postero-inferior)
of the elements comprising the mid-sagittal genioglossus muscle
(lateral perspective) in order to achieve maximal contraction and net
clockwise rotation of the tongue [9,47]. In this manner, retrograde
propulsion was achieved by posterior-directed deformation of the
longitudinally-expanded and superiorly-opposed lingual tissue, with the
expectation that the absence of 3D considerations affect maximal
midline deformation during accommodation. In particular, the lack of
modeled transversus contractions (due to the inability to portray myo­
fiber distribution in the transverse plane) reduced the obtainable force
applied by the tongue tip to the hard palate during early accommoda­
tion, since bidirectional verticalis-transversus contraction, and the
associated force generating expansion in the anterior direction, could
not be fully achieved. Furthermore, the absence of augmentatory con­
tractions by the hyoglossus and styloglossus, attached inferiorly and
superiorly, respectively, to the lateral complex, and the loss of the
compressive effects of the superior and inferior longitudinalis muscles
on the genioglossus would be expected to minimize the achievable depth
of the accommodating concavity, and thus limit the maximal size of the
modeled bolus. We simulated lingual mechanical pathology in two
ways: 1) We depicted the effect of graded decreases of global lingual
deformability by increasing the stiffness of the isotropic, passive matrix
modeled by the Mooney-Rivlin formulation. The c10 constant of the
Mooney-Rivlin model was specifically increased for each FE group by
factors of 25%, 50%, and 75%. 2) We depicted the effect of graded
reduction of global contractility by decreasing the maximum tetanized
isometric stress for each FE group by factors of 25%, 50%, and 75%. All
modeled pathologies were implemented in the current 2D mechanical
model and outcomes depicted in terms of their effects on local
Lagrangian strain.
2.4. Fluid finite element mesh generation in relation to a deforming
boundary (lingual surface)
To model the geometry of the oropharyngeal space that the bolus
traverses during the swallow, the lingual surface was extracted at each
time point of the simulation. The initial state was imported into the LS-
Dyna finite element software (Ansys, Inc., Canonsburg, PA) and used to
generate the initial mesh. Successive states were input as boundary
motion, which in turn drove fluid displacement. The location and shape
of the initial free surface corresponded to an approximately 3 mL bolus
(assuming a 3 cm width of the tongue).
To account for mesh motion associated with a deforming lingual
boundary, an arbitrary Lagrangian-Eulerian (ALE) formulation was
utilized. An ALE formulation allows the computational mesh to move
independently of the underlying material. This allows the mesh inside
the fluid domains to move arbitrarily in order to optimize the shapes of
elements as the mesh deform (due principally to surface motions).
Remeshing to account for mesh distortion is accomplished using
Delauney triangulation. The ALE formulation is distinguished from pure
Lagrangian methods, in which the computational grid is attached to
material particles of the fluid are unable to track large distortions of the
4
Computers in Biology and Medicine 145 (2022) 105446
computational domain without frequent remeshing, or pure Eulerian
algorithms with stationary grids, which account for large distortions of
continuum motion at the expense of the resolution of the solid interface
and flow details. The computational principles which define this model
and its application for fluid simulations at the interface with the
deformable solid surface, in this instance the lingual surface, have been
previously described [48]. To illustrate the process of remeshing, we
depict in Fig. 3, the changing fluid mesh as a function of lingual surface
deformation during the swallow at 4 discrete time points following
tongue tip opposition to the hard palate. Because the boundary condi­
tion at the tongue-bolus interface was mobile [22,34], both “perfect-­
slip” (absence of surface adhesion of the fluid to the tongue surface) and
“no-slip” (presence of surface adhesion of the fluid to the tongue surface)
conditions were implemented.
2.5. Computational depiction of intra-oral bolus flow
The flow of an incompressible liquid is governed by the conservation
of mass and momentum. In an ALE framework, they are given by:
∂ui
=0 (1)
∂xi
[ ]
∂ui ( ) ∂ui ∂σij
ρ + uj − vj = ρfi + (2)
∂t ∂xj ∂xj
where ui , vi , fi , and σij represent the fluid velocity, mesh velocity, body
force per unit mass and the Cauchy stress tensor, and where repeated
indices imply summation. A constitutive model describing the fluid
behavior, either Newtonian or non-Newtonian, was included to com­
plete the system. Stress in a Newtonian fluid is given by:
( )
∂ui ∂uj
σ ij = − Pδij + μ + (3)
∂xj ∂xi
where P is the pressure, and μ is the constant viscosity. Values of 5, 110,
300, and 525 cP were studied in this work. In addition to this Newtonian
constitutive model, a non-Newtonian shear-thinning model was also
utilized, in which the apparent viscosity is given as a function of the
strain rate, γ̇, by:
μ = kγ̇n− 1
(4)
where k is the consistency index, n is the power law index, and the strain
rate, γ̇, is the norm of the velocity gradient tensor. A fractional-step
method was employed to step forward in time and account for the
incompressibility constraint [48].
To track the free surface (bolus-air interface), a scalar parameter, φ,
was introduced, such that the φ = 0 isocontour represents the free sur­
face. Regions in which φ > 0 represent fluid and φ < 0 represent vac­
uum. A convection equation was solved to define φ(t):
∂φ ∂φ
+ uj = 0 (5)
∂t ∂xj
A particular challenge in the use of level-set methods relates to the
accuracy of Eulerian methods to track small portions of fluid that are
split from the main fluid body. However, the current software imple­
ments adaptive meshing that adds elements in regions when necessary
to maintain accuracy. The remeshing algorithm discussed previously
also provides increased resolution around the free surface (see Fig. 3). In
addition, a variable time-step based on the CFL number was employed.
The intra-oral bolus flow resulting from the coupled FEM was
analyzed in Paraveiw (Version 5.8.0). The liquid bolus was first identi­
fied from the surrounding air in the oral cavity using a threshold filter of
the level-set. The velocity magnitude was displayed as a contour map at
100 ms intervals and further studied by extracting the velocities of the
head and tail of the bolus at each time point, with the shear rate
D.M. Leichter et al.
computed as the magnitude of the velocity gradient tensor.
3. Results
3.1. Lagrangian stain maps (2D) of the tongue in association with
deglutitive deformation during liquid bolus accommodation and propulsion
(normal)
A contour map was overlaid on the deforming tongue geometry at
various time points originating with the tongue tip opposed to the hard
palate and depicted the minimum principal Lagrange strain in the mid-
sagittal plane that was associated with the sequence of lingual de­
formations characteristic of the accommodative and propulsive phases
of swallowing (Fig. 4). Extension in the region of the inferior longi­
tudinalis in association with tongue prepositioning to the hard palate
(shown as a bar) along with compressive strain in the region of the su­
perior longitudinalis is shown. This occurs in place of graded bidirec­
tional contraction of the verticalis and tranversus, which leads to
hydrostatic expansion in the superior-anterior direction in vivo during
5
Computers in Biology and Medicine 145 (2022) 105446
Fig. 3. Derivation of finite element (FE)
mesh depicting the changing dynamics
involving the fluid and air domains. A FE
mesh was constructed using the mesh
generator function of LS-Dyna based on
Delaunay triangulation, a method for
generating triangular meshes without over­
lap through the connection of scattered
sample points. We employed adaptive
meshing to improve computational resolu­
tion in the region adjacent to the fluid phase.
We demonstrate the mesh applied to the air-
fluid domain within the oral cavity adjacent
to the deformed lingual surface at the outset
of the propulsive phase of swallowing (left)
and demonstrate the differential mesh reso­
lution between the air and the fluid domains
(right inset) for tongue with bolus accom­
modated prior to swallow initiation, and at
200, 300, and 400 ms after initiation of the
propulsive sequence.
lingual protrusion and bending towards the hard palate. This was fol­
lowed by maximum compressive (negative) strain which was experi­
enced by the tongue in the region immediately adjacent to the
deforming lingual surface between 185 and 365 ms, likely reflecting the
combined effects of sequential genioglossus and verticalis contractions.
The net effect of these midline mechanical events was extension of the
anterior tip so that it apposed the hard palate, thus comprising the
accommodated cavity (from the lateral perspective) to promote bolus
displacement within the oral cavity and from the oral cavity to the
pharyngeal cavity (not shown). We further demonstrated the extraction
of the spatial coordinates for each point on the surface of the
architecturally-derived deforming tongue, which were then displayed as
a series of deforming shapes that comprised the inferior (soft) boundary
of the liquid bolus for the purpose of carrying out the fluid simulations.
3.2. Myoarchitecture-driven lingual deformation and liquid bolus flow
To depict the shape of the oropharyngeal space, we incorporated the
lingual surface derived from the solid phase FEM into the LS-Dyna pre-
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 4. Deglutitive lingual mechanical function during accommodation and propulsion. A) The deforming tongue is represented in terms of its local Lagrangian
strain, a dimensionless rendering of the change of linear strain, referenced to its initial length depicted at 45 ms intervals. Strain is depicted on a continuous scale of
0 (minimal strain) to 0.45 (maximal strain). Results demonstrate initial net strain that was manually induced by expansion in the inferior longitudinalis combined
with compression in the superior longitudinalis to comprise the midline bolus accommodating concavity, followed by maximum strain adjacent to the deforming
lingual surface reflecting superior-inferior progressive contractions of the segments of the genioglossus and verticalis contractions. Points of lingual attachment are
shown for the styloglossus (SG), hyoglossus (HG) and genioid process (GP). B) The spatial coordinates associated with the deforming lingual surface generated by the
implementation of soft tissue activation through a finite element representation were extracted at 140 ms intervals and displayed as a series of time-sensitive
deforming shapes. This surface rendering of the tongue formed the mobile inferior boundary of the bolus and was employed to drive intra-oral bolus flow in the
simulations.

processor. The pattern of deformation was consistent with a model 3 mL
bolus contained in the midline concavity on the surface of the tongue
between the tongue, palate, and air-liquid interface. The flow of the low-
viscosity bolus in response to perfect slip (top) and no-slip (bottom)
conditions is shown in Fig. 5A. The outline of the bolus was defined by
the φ = 0 isocontour, and the bolus shape was colored by the magnitude
of the local velocity vector. The velocity magnitude was generally higher
for the perfect-slip case due to the lack of wall friction. The velocity
gradient is a 2nd order tensor whose components in a Cartesian coor­
dinate system are given by ∂∂xvij . The magnitude of the velocity gradient
tensor is referred to as the shear rate, a quantity of interest when non-
Newtonian boluses are considered. This velocity difference from the
wall to the free surface approximates the shear rate and in the no slip
case leads to a “cresting” of the bolus starting at about 275 ms, as the
inertia of the bolus starts to pull away from the lingual surface as the
surface begins to curve downward. This eventually led to bolus splitting
into subcomponents, or fragmentation, a reaction that was not observed
for the perfect-slip case. We observed that the variation in velocity from
the wall to the free surface is greater in the no-slip case than the perfect-
slip case throughout the entire swallow. Overall, the perfect slip con­
dition promoted higher bolus velocities, enhanced bolus cohesion, and
more efficient bolus transit compared to the no-slip condition.
3.3. Effect of bolus viscosity on intra-oral flow
To study how variations in fluid viscosity influence bolus flow pat­
terns, boluses with viscosities of 5 cP (low), 110 cP and 300 cP (medium)
and 525 cP (high) were simulated under perfect-slip conditions

6
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 5. Effect of bolus viscosity on distributed local velocity. A finite element model depiction of the velocity profile in the flowing bolus liquid bolus was compared
under perfect slip (without adhesion) and no slip (with adhesion) conditions. In this setting, we provide a computational description of intra-oral liquid bolus flow in
terms of its local velocity vector distribution, as affected principally by the deforming lingual surface. Demonstrations of the velocity profile of a low viscosity (5 cP)
bolus under perfect-slip and no-slip boundary conditions are demonstrated. The perfect slip condition promoted higher overall bolus velocity, greater bolus cohesion,
and more efficient bolus delivery to the oropharynx relative to the no slip condition, which led to bolus fragmentation in the oropharynx (B). A finite element
depiction of the velocity profile for the liquid bolus was demonstrated under a perfect slip condition for three viscosities, namely medium viscosities (110 cP and 300
cP) and high viscosity (525 cP), during the propulsive phase of swallowing. Local velocity was generally highest at the bolus head for all conditions, but velocity was
distributed throughout the bolus based on its viscosity. The low viscosity bolus (5 cP) exhibited maximal overall displacement, bolus thinning, and overall velocity,
whereas the medium (110 cP) and high (525 cP) bolus viscosities demonstrated significantly lower overall velocities, less bolus and thinning and reduced bolus
displacement (C).

(Fig. 5B). For all conditions, local velocity was generally highest at the
bolus head, although velocity varied within the body of the bolus. The
low viscosity bolus (5 cP) exhibited maximal overall displacement, bolus
thinning and overall velocity relative to the medium (110 cP) and high
(525 cP) bolus viscosities. For the highest viscosity case, we observed
that the bolus had not exited the oral cavity by the end of the simulated
propulsive phase, indicating that the modeled surface displacement was
insufficient to achieve complete intra-oral transit. We extracted from
these simulations the spatial and temporal patterns of local bolus speed
for each of the four Newtonian viscosity conditions (Fig. 6). All bolus
conditions demonstrated a tri-phasic pattern of nodal velocity, which
manifested as an initial increase during the initiation of lingual defor­
mation followed by a decrease during transit of the bolus across the
lingual surface and was completed with a second increase during the
return of the tongue to its undeformed position. The range of bolus ve­
locities (bolus head and tail) was approximately 0.1–0.5 m/s, which was
similar to values of intra-oral bolus velocity previously reported in the
literature (0.1–1.0 m/s) [29,49,50]. In all cases, the bolus head

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D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 6. Patterns of local nodal velocity for bolus head and tail. Local nodal velocity was extracted at two regions (head, tail) of the bolus and plotted as a function
of time during each of four Newtonian viscosity conditions during the propulsive phase of the swallow. All bolus conditions demonstrated a bi-phasic pattern of
velocity progressions (direction of velocity not specified), manifesting as an early increase of nodal velocity coincident with the initiation of lingual deformation and
followed by a decrease of nodal velocity that varies with viscosity and is coincident with transit of the bolus across the lingual surface. The low viscosity (5 cP)
condition had the most heterogeneous velocity profile and resulted in bolus fragmentation. The high viscosity (525 cP) condition was the most homogenous and was
least affected by fragmentation. In all four Newtonian cases, the bolus head demonstrated greater velocity and heterogeneity than the bolus tail.

demonstrated greater velocity and heterogeneity than the tail. The high
viscosity (525 cP) condition was the most spatially homogenous in terms
of nodal velocity and least affected by fragmentation, whereas the
lowest viscosity was the least spatially homogenous and most affected
by fragmentation. The flow of a non-Newtonian, shear-thinning bolus
was simulated under perfect-slip conditions (Fig. 7). At a shear rate of 1
s− 1, the apparent viscosity is 660 cP, which is comparable to the high
viscosity Newtonian bolus. At 50 s− 1, the apparent viscosity drops to
138 cP, similar to the medium viscosity (110 cP) bolus and never falls
below approximately 40 cP for shear rates that are expected during
physiological swallowing. The velocity contours for the non-Newtonian
case appeared quite similar to the medium viscosity Newtonian case as

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D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 7. Comparison of local velocity flow profiles in the cases of Newtonian and non-Newtonian fluids. A) The velocity profile through finite element
modeling for a non-Newtonian bolus following the Power-Law model and under perfect slip boundary conditions was demonstrated, and the non-Newtonian bolus
demonstrated significantly lower bolus velocities as compared to a similar viscosity bolus with Newtonian properties and less overall bolus displacement. B) Nodal
velocity is depicted for the non-Newtonian bolus at both the head and tail as a function of time in comparison with that of a Newtonian bolus of medium viscosity
(110 cP). A least square linear regression method was used to portray the similarity of the derived slope of the relationship between nodal velocity as a function of
time for the Newtonian and non-Newtonian conditions.

the apparent viscosity is mostly in this range for physiologically relevant
shear rates, whereas the extracted nodal velocity pattern depicted as a
function of time during the propulsive swallow was nearly superim­
posable. Lastly, in order to better predict bolus cohesion, and its
converse, i.e. fragmentation, we estimated the shear rate of the bolus as
the distribution of velocity across its thickness, which was portrayed
graphically as the velocity gradient for each node in the simulated bolus
at each swallow time point, and then related to the degree of fragmen­
tation. As demonstrated in Fig. 8, the low viscosity, free slip condition
demonstrates the highest velocity gradient on the air-liquid surface,
which predicts the highest rate of bolus fragmentation. With increasing
viscosity (110, 300, 525 cP), under free slip conditions, the velocity
gradient on the air-liquid surface is gradually diminished along with the
propensity for bolus fragmentation.
3.4. Effect of modeled tissue stiffness and reduced muscle cell activation
on lingual mechanics and bolus flow
Two cases of simplified mechano-pathology were modeled and dis­
played in terms of Lagrangian strain maps and coupled bolus flow. In the
first instance, reduction of deformability resulting from increased tissue
stiffness was modeled through an increase in the isotropic, passive
matrix of the Mooney-Rivlin model (Fig. 9). This resulted in decreases in
the minimum principal Lagrange strain of the inferior longitudinalis and
verticalis of the anterior tongue, limiting the initial elevation of the
tongue tip at the 100 ms time point. Between 200 and 300 ms, the
rotation of the entire tongue body to displace the bolus was somewhat
limited, likely caused by the reduced strains in the superior genioglossus
regions of the posterior tongue as well as the geniohyoid. As shown in
Fig. 10, the effect of a graded increase of stiffness on bolus flow prop­
erties for an equivalent bolus (5 cP, free slip) included a loss of bolus
thinning, reduced overall posterior displacement, and limitation of
surface velocity gradient elevation to the latter time points. In the sec­
ond instance, the reduction in global contractility of the entire tongue
was modeled by decreasing the maximum tetanized isometric stress for
each FE muscle group, resulting in significant reductions in strain
throughout the entire tissue. This resulted in a reduction of the overall
speed and maximum displacement of the tongue, preventing the tongue
from fully elevating to oppose the hard palate at 100 ms and the tongue
body from rotating to displace the bolus into the pharyngeal cavity
between 200 and 300 ms (Fig. 11). As shown in Fig. 12, the effects of this
modification included a graded reduction of achievable bolus volume
due to the near complete loss of obtainable concavity, absence of bolus
spreading across the lingual surface, and loss of posterior displacement.
4. Discussion
The distribution and spatial orientation of lingual muscle fibers at
the mesoscale contribute substantially to the mechanics of lingual
deformation and bolus flow during oropharyngeal swallowing. We
previously portrayed a computational model of lingual deformation
aligned with its underlying myoarchitecture [19], which was subse­
quently adapted to account for its microscopic material characteristics
[20] and mechanical function [47]. While computational models have
independently portrayed lingual mechanics and bolus flow, the explicit
coupling of contraction-induced lingual surface deformation and bolus

9
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 8. Effects bolus viscosity on the distribution of velocity gradients within the liquid bolus. The overall magnitude of the velocity gradient was depicted as a
function of perfect slip (A) and non-slip (B) boundary conditions and as a function of varied bolus viscosities (C–E). The velocity gradient is equivalent to the shear
rate of the fluid bolus and serves as an indication of the shear forces experienced by the bolus during the swallow sequence. The non-slip bolus experienced greater
velocity gradients along the tongue’s surface as compared to the perfect slip boundary conditions, which promoted greater velocity gradients at the air-liquid
interface. The lowest bolus viscosities experienced the greatest velocity gradients during the propulsive phase of swallowing, with greater velocity gradients at
the head of the bolus. This corresponds with higher shear forces and greater bolus fragmentation in these regions. Conversely, the higher viscosity boluses expe­
rienced lower velocity gradients, promoting greater bolus homogeneity and less fragmentation.

flow, a relationship central to the clinical assessment of aspiration
vulnerability, has not been demonstrated. We present herein a
solid-fluid model of deglutitive lingual bolus flow during human swal­
lowing that depicts bolus motion as a function of architecture-driven
intramural contractility and patterned lingual deformation. This
model is presented for the purpose of relating architectural differences
possessing voxel scaled changes of material or activation properties with
intrabolus velocity and velocity gradients. We postulate that such vari­
ations are the harbingers of bolus fragmentation, a condition which may
increase vulnerability to deglutitive aspiration.
Flow of a liquid bolus through the oropharynx is inherently complex
and includes the 3D displacement of an air-fluid mixture through an
irregularly shaped cavity with moving boundaries. We chose an ALE FE
approach to account for the moving boundaries while using a level-set
method to track the free surface. Bolus flow is a function of both pro­
pulsive lingual motion and rheological properties and is subject to the
laws of mass and momentum conservation. Although various simplified
analytical frameworks have been applied to model bolus flow within the
oropharynx [23,34,51], computational modeling is necessary for a
complete fluid mechanical representation of swallowing. In previous
models, which used numerical techniques, including finite volume,
finite element, or particle methods [11,21,22,26–28] specified motion
of the lingual and oropharyngeal surfaces were used to infer bolus mo­
tion. The current work differs from these previous models in that the
representation of wall motion that drives bolus flow was derived from
imaged tissue myoarchitecture and modeled tissue contractility and
elasticity. This approach thereby computationally links lingual myoa­
natomy and material properties with deglutitive bolus flow. The current

10
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 9. Effect of increased ECM stiffness on modeled lingual mechanics during swallowing. Graded decreases of lingual tissue deformation were modeled by
increasing the stiffness of the isotropic, passive matrix modeled by the Mooney-Rivlin formulation. The C10 constant of the Mooney-Rivlin formulation was increased
for each FE group by factors of 25%, 50%, and 75%, and the resulting biomechanical outcome was represented in terms of its Minimum Principal Lagrangian strain at
100 ms intervals. The decrease in global lingual deformability demonstrated moderate reductions in the elevation of the tongue tip at 100 ms and rotation of the
tongue body at the 200 and 300 ms intervals. Most notably, there were reductions in strain in coincident with the inferior longitudinalis and verticalis of the anterior
tongue, the superior genioglossus regions of the posterior tongue, and the geniohyoid regions of the inferior tongue.

work uses partially coupled solid-fluid modeling to assess lingual control
of bolus cohesion during the course of the swallow. The explicit rela­
tionship between myoarchitecture, local patterns of tissue contraction,
net deformation, and surface modifications that contain and propel the
bolus is pivotal for describing how an anatomically complex tissue such
as the tongue promotes purposeful bolus flow. The goal of the current
paper is to relate myoarchitecture-driven surface changes with patterns
of bolus flow. In so doing, we are able to infer the specific contributions
of localized muscles and muscle groups on net changes of lingual surface
deformation, and thereby deduce the impact on distributed (local) bolus
velocity throughout the swallow.
Simulations of lubricated (perfect slip) or non-lubricated (no slip)
boundary conditions have been considered in regard to intra-oral bolus
flow [22]. No-slip boundary conditions assume that the velocity of the
fluid layer in contact with the lingual surface is the same as the velocity
of the boundary. Alternatively, the perfect slip condition assumes that
there is no friction between the fluid and the adjacent surface, allowing
relative motion to occur unimpeded. Extending prior work, we observed
in the setting of physiological lingual deformation that perfect slip
conditions are associated with higher velocity, greater cohesion and
more effective bolus transit, whereas no-slip conditions are associated
with reduced velocity, bolus thinning and less effective bolus transit.
It is generally thought that increased bolus consistency promotes
greater bolus cohesion (and reduced fragmentation) and thereby
reduces airway vulnerability to aspiration in the dysphagic patient [52].
However, the relationship between local velocity within the flowing
bolus and physiological or pathophysiological lingual surface deforma­
tion has not to date been derived. The current work fills that gap by
providing a model that couples architecture-driven surface deformation
with fluid dynamics for boluses with varied rheological properties.
Hayoun et al. established that basic principles of viscosity-dependent
flow in an artificial environment emulate in part the forces applied by
the deforming tongue to the hard palate [13]. In so doing, they deter­
mined that bolus flow related to model swallowing occurred as an initial
viscosity-insensitive phase exhibiting transient acceleration phase fol­
lowed by a viscosity-sensitive phase exhibiting constant velocity. Our
work extends this model by depicting velocity as a function of human
myoarchitecture-based surface deformation and demonstrates the
presence of a biphasic model, which relates bolus acceleration or
deceleration with lingual mechanics and surface deformation. Hetero­
geneity of the nodal velocity and bolus fragmentation was principally
observed in the setting of the lowest viscosity condition, whereas ho­
mogeneity of nodal velocity and minimal fragmentation was principally
observed for the high viscosity condition. Distributed nodal velocity can
be derived across the thickness of the bolus (lingual surface to air-liquid
interface) and represented graphically as the velocity gradient, which in
turn represents shear properties. Within the boundaries of the current
model, we demonstrate that elevations of the velocity gradient, located

11
D.M. Leichter et al.
principally at the air-fluid surface, are most predictive of bolus frag­
mentation, and may provide a physical basis to understand the clinical
observation relating increased bolus “thickness” with reduced aspiration
risk. These observations have particular significance in the setting of
non-Newtonian fluids, commonly used in swallow therapy, where the
shear rate impacts the apparent viscosity. By demonstrating how shear
12
Computers in Biology and Medicine 145 (2022) 105446
Fig. 10. Effects of reduced tissue
deformability (ECM stiffness) on distrib­
uted velocity gradients during swallow­
ing. We assessed the effect of decreased
lingual tissue deformability (shown in Fig. 9)
on distributed bolus velocity gradients under
control conditions at 5 and 300 cP viscosities
(free slip), and at 25%, 50%, and 75%
induced ECM stiffness (reduced deforma­
tion) for each viscosity condition. The
graded decrease of tissue deformability
resulted in graded reductions of intra-oral
bolus movement during the propulsive
phase of swallowing in both the low (5 cP)
viscosity case (A) and the higher (300 cP)
(B) viscosity case. All cases promoted higher
velocity gradients at the bolus head at the
280 ms interval, indicating a higher shear
rate and greater shear forces in this region.
This consequently leads to bolus thinning
and fragmentation in the low viscosity, 25%
ECM stiffness case.
rate varies within the bolus, one can predict how the thickness of a
non-Newtonian bolus changes during the swallow. This information,
combined with prediction of bolus fragmentation or residue for
abnormal swallowing, suggests a strategy for choosing texture modifi­
cations targeted towards the particular mechanical deficiency. The
current 2D model was, however, unable to depict complete transit of the
D.M. Leichter et al. Computers in Biology and Medicine 145 (2022) 105446

Fig. 11. Effect of reduced tissue contractility on modeled lingual deformation during swallowing. Graded reduction of global contractility was modeled by
decreasing the maximum tetanized isometric stress for each FE group by factors of 25%, 50%, and 75%. The resulting biomechanical outcome was represented in
terms of its Minimum Principal Lagrangian strain at 100 ms intervals. The reduction in global contractility resulted in significant reductions in net tissue
displacement, limiting the elevation of the tongue tip at the 100 ms interval and the rotation of the overall tongue body at the 200 and 300 ms intervals, as well as
commensurate reductions of Lagrangian strain throughout the tissue.

oral bolus for high viscosity materials due to the absence of force applied
to the hard palate [53–55] and the subsequent lack of stiffening from
intrinsic bidirectional contraction [7]. Future models will be intended to
derive changing velocity gradients in all spatial dimensions, thereby
more comprehensive tracking of bolus properties throughout the swal­
low in myo-pathological settings.
We further implemented this analysis to determine the impact of two
model pathologies on deglutitive lingual deformation and associated
bolus flow. In the first instance we modeled changes of overall tissue
stiffness through modifications of the isotropic Mooney-Rivlin constant
[56] as a means to infer the effects of collagen deposition related to
pathological conditions, such as lingual irradiation for carcinoma [57]
or inclusion body myositis [58]. We recognize that our approach likely
underestimates actual tissue fibrosis since we are studying only the
presence of a “stiffening factor” incorporated in the ECM component,
which is aligned with myocytes comprising normal lingual myoarchi­
tecture. In contrast, actual fibrosis would likely be associated with
myocyte death and replacement with an inflammatory infiltrate con­
sisting of isotropic T-cells, myofibroblasts, and secreted collagen. As
such, the mechanical effect of inflammo-fibrosis in the setting of clilnical
pathology would be considerably more complex than that imparted by
the relatively variations of the isotropic Mooney-Rivlin constants shown
and reflect distributed effects of both isotropic and anisotropic elements
in a structurally complex milieu. By our model, we demonstrated a
graded effect on bolus thinning and the obtainable velocity gradients. In
the second instance, we derived the effects of global muscle weakness
through graded effects on activation functions aligned with diffusion
tractography as a means to infer impairments expected during
myopathic conditions, and observed a loss of achievable concavity,
absence of bolus thinning, and loss of posterior bolus displacement.
This analysis provides a method for clinical translation that explicitly
relates impaired myoarchitecture with local contractility, global tissue
deformation, and bolus cohesion. We posit that pathological myoarch­
itecture, as may typify various myo-pathologies, forms in part the un­
derpinnings of impaired surface deformation that may impact the degree
of bolus cohesion exhibited under varied rheological conditions. From
the above, we postulate that a critical component of aspiration vulner­
ability is likely to be bolus incohesion, promoted, in part, by abnormal
patterns of myoarchitecture-driven lingual surface deformation and
associate mechanics [59]. The components of this model include alter­
ations of lingual architecture and contractility that contribute to
abnormal swallow-associated lingual surface deformation, and the
rheological properties of the bolus (viscosity, adhesion, shear stress
modification), with the outcome being either a homogeneous pattern of
distributed nodal velocity (i.e. cohesion) or varying degrees of in­
homogeneity of distributed nodal velocity (i.e. incohesion or
fragmentation).
Several limitations of the current study should be acknowledged.
First, the fact that the current simulation depicts only events in the mid-
sagittal plane constrains our ability to depict laterally situated muscular
events significant for bolus handling, for example, the compressive and
displacing effects of hyoglossal or styloglossal contractions on the depth
of the accommodating concavity or the speed of lingual rotation, or the
effects of side-specific lesions. Second, we acknowledge that the

13
D.M. Leichter et al.
structure-fluid interaction as portrayed in this model is largely unidi­
rectional, that is, solid deformation of the tongue affecting bolus flow
but not the effect of bolus presence/flow affecting solid deformation of
the tongue. Lastly, our model does not incorporate posterior pharyngeal
contractile dynamics in promoting bolus flow, and therefore lingual
propulsion is the only force-generating muscular action that is perceived
by the bolus.
In summary, we demonstrate a finite element model which partially
couples myoarchitecture-based lingual contractility, surface deforma­
tion, and bolus flow during swallowing. This current model specifically
infers fluid motions from the 2D displacement of the deforming lingual
surface during the propulsive phase of swallowing. Future models will
14
Computers in Biology and Medicine 145 (2022) 105446
Fig. 12. Effects of reduced overall tissue
contractility on the magnitude of the
distributed velocity gradients during
swallowing. Global decrease of lingual
contractility was simulated in the manner
described in Fig. 11 for each FE muscle
group under control conditions at 5 and 300
cP viscosities (free slip), and at 25%, 50%,
and 75% diminished contractility for each
viscosity condition. Graded reduction of
contractility resulted in graded reductions in
tongue concavity, accommodated bolus vol­
ume, and bolus displacement for the low (5
cP) viscosity case (A) and the higher (300
cP) (B) viscosity case. Notably, decreased
tissue contractility by factors of 25% and
50% demonstrated higher velocity gradients
at the bolus head, indicating greater shear
rate and shear forces and contributing to
greater bolus thinning.
be designed to incorporate more complex multi-dimensional renditions
involving the lateral and transverse domains of the tissue, the volitional
aspects of bolus accommodation, and pathological myoarchitectures, in
order to provide a more precise depiction of oral bolus control.
Declaration of competing interest
None of the authors have any conflicts of interest to declare.
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