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Dysphagia (2018) 33:602–609

https://doi.org/10.1007/s00455-018-9878-7 (0123456789().,-volV)(0123456789().,-volV)

ORIGINAL ARTICLE

Superior and Anterior Hyoid Displacement During Swallowing in Non-


Dysphagic Individuals
James Curtis1 • Jonelyn Langenstein2 • Sarah Schneider3

Received: 14 September 2017 / Accepted: 30 January 2018 / Published online: 14 February 2018
 Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
The Dynamic Swallow Study (DSS) is a methodology used to objectively and quantitatively assess swallowing kinematics
during Videofluoroscopic Swallow Studies (VFSS). No DSS normative data exist delineating superior and anterior hyoid
displacement (Hsup and Hant, respectively), nor the ratio between Hsup and Hant (SAratio). The aims of this study were to (1)
establish normative data for Hsup, Hant, and SAratio and (2) assess the effects of age, sex, and bolus size on these measures in
non-dysphagic patients, within the context of DSS. VFSSs were reviewed for consecutive elderly (C 65 years) and non-
elderly (\ 65 years) male and female non-dysphagic patients. Measurements of Hsup, Hant, and SAratio were made using a
novel measurement methodology within the context of the Dynamic Swallow Study (DSS) protocol. Statistical analysis
was performed to establish interaction effects and main effects of age, sex, and bolus size on Hsup, Hant, and SAratio.
Descriptive statistics (mean ± standard deviations) are outlined for Hsup, Hant, and SAratio. Hsup was significantly effected
by bolus size and age. Additionally, a significant three-way interaction of age, sex, and bolus size was observed. Hant was
significantly effected by bolus size and sex, but no two- or three-way interactions were present. Neither bolus size, age, nor
sex significantly effected SAratio. Age, sex, and bolus size normative data were established for Hsup, Hant, and SAratio for
VFSS kinematic analysis. By outlining these measures, one can more thoroughly evaluate the areas of specific swallowing
impairment, better determine the therapy targets, and track changes over time.

Keywords Hyoid  Displacement  Videofluoroscopic swallow study (VFSS)  Modified barium swallow studies (MBS) 
Swallowing  Dysphagia

Introduction prevention of penetration and aspiration of boluses. Swal-


lowing kinematics can be quantified spatially (how far
Swallowing involves oral, pharyngeal, laryngeal, and eso- structures move) and temporally (when structures move,
phageal structures working in tandem to efficiently propel and how fast they move, relative to each other and relative
food and liquid completely from the mouth into the to bolus flow). Hyoid bone displacement can be measured
stomach, whilst maintaining airway protection for the by its overall displacement, or separated into its superior
and anterior vectors [1, 2]. It is thought that superior hyoid
displacement is an important contributing factor to
& James Curtis epiglottic inversion and laryngeal vestibule closure for the
jarthurcurtis@gmail.com prevention of penetration and aspiration of boluses before
1 and during the swallow, while anterior hyoid displacement
Department of Biobevioral Sciences, Teachers College,
Columbia University, 525 West 120th Street, New York, assists in mechanical opening of the pharyngoesophageal
NY 10027, USA segment to allow for bolus clearance into the esophagus
2
Center for Audiology, Speech, Language, and Learning, [3–9]. Research demonstrates that impairments in superior
Northwestern University, 2315 Campus Drive, Evanston, and anterior displacement of the hyoid bone place indi-
IL 60208, USA viduals at increased risk of penetration, aspiration, and
3
Department of Otolaryngology-Head and Neck Surgery, post-swallow residue; however, it is important to note that
University of California, San Francisco, 2330 Post Street, 5th some studies demonstrate impaired hyoid displacement
Floor, San Francisco, CA 94115, USA

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J. Curtis et al.: Superior and Anterior Hyoid Displacement… 603

that does not necessarily predict compromised laryngeal complete horizontal and vertical epiglottic inversion for all
closure or bolus clearance [9–15]. swallows during the VFSS; and normal (i.e., \ 2 SD below
Videofluoroscopic swallow studies (VFSS) are used to mean) pharyngeal constriction ratio (PCR), hyolaryngeal
analyze spatial and temporal swallowing kinematics in approximation (HL), pharyngoesophageal segment opening
addition to observing adverse airway protective events (PESmax), and maximal hyoid displacement (Hmax) DSS
such as penetration and aspiration of foods and liquids. displacement measures for 1, 3, and 20 cc nectar-thick
While many swallowing kinematic measurement method- liquid swallows [16, 33, 34]. Patients having the following
ologies exist, one standardized and frequently used criteria were excluded: a history of oral cavity, laryngeal,
approach to kinematic assessment is the Dynamic Swallow or pharyngeal surgical intervention (with the exception of
Study (DSS) protocol, originally developed by Rebecca routine dental work); a history of radiation therapy to the
Leonard and Katherine Kendall [11, 16–21]. The DSS head and/or neck; diagnosis of a neurologic and/or neuro-
protocol involves having an examinee establish a ‘‘pseudo- muscular disease; and/or a formal diagnosis of a structural-
rest’’ position by way of holding a 1 cc liquid bolus in their or motility-based esophageal abnormalities.
mouth. After establishing the pseudo-rest position, the
examinee performs a single cued swallow of 1, 3, and/or Videofluoroscopic Swallow Studies
20 cc nectar-thick liquids. Upon completion of the exam,
the examiner can perform a frame-by-frame fluorographic Videofluoroscopic examinations were performed at the
analysis of a variety of spatial and temporal swallowing University of California San Francisco (UCSF) Medical
kinematics [11, 16, 22–32]. Center in accordance with established and routine
The ‘‘Hmax’’ is a DSS hyoid displacement measure VFSS?DSS protocols. Two different fluoroscopic machi-
describing the total distance traveled by the hyoid bone nes were used: the Axiom Luminos TF (Siemens Health-
from the pseudo-rest position to the point of maximal care, USA) and the Luminos Agile Max (Siemens
anterior–superior hyoid displacement at or near the height Healthcare, USA). Patients were presented with 1, 3, and
of 1, 3, or 20 cc nectar-thick liquid swallows. While 20 cc nectar-thick liquid barium boluses (40% w/v Varibar
healthy volunteer DSS Hmax norms have been previously Nectar Barium Sulfate Suspension) and were instructed to
established, normative DSS data separately describing (1) hold the liquid bolus in their mouth (i.e., the ‘‘pseudo-
superior and anterior hyoid displacement, and their rela- rest’’ position) and then (2) attempt to swallow the entire
tionships to one another, have not been previously inves- bolus in a single swallow when cued by the clinician. All
tigated [16]. Given the unique physiologic contributions of video segments were recorded in a lateral viewing plane
superior hyoid movement and anterior hyoid movement, with an image-capturing rate of 25–30 images per second
establishing separate normative data within the context of a (depending on the capabilities of the fluoroscopy machine)
DSS protocol, and describing their kinematic relationship and a magnification level of 1–2 9. All VFSS videos were
to one another, would provide meaningful information for saved directly into a picture archiving and communication
clinical and research purposes. system (PACS) for later review and analysis.
The aims of this study were to (1) establish normative
data for maximal superior hyoid displacement (Hsup), Hyoid Displacement Measurement Methodology
maximal anterior hyoid displacement (Hant), and the ratio
of superior to anterior hyoid displacement (SAratio) in non- Both superior hyoid displacement (Hsup) and anterior hyoid
dysphagic patients within the context of the DSS maximal displacement (Hant) were measured at the same points in
hyoid displacement (Hmax) measure and (2) assess the time within the same video frames—during the pseudo-rest
effects of age, sex, and bolus size on these measures. position (i.e., 1 cc bolus hold) and during maximal overall
hyoid displacement (i.e., Hmax) at or near height of swallow
for 1, 3, and 20 cc liquid swallows. The Hsup was defined
Methods as the change in vertical hyoid position from the pseudo-
rest position (‘‘Hsup-rest’’) to the Hmax position (‘‘Hsup-max’’).
Record Review The Hant was defined as the change in horizontal hyoid
position from the pseudo-rest position (‘‘Hant-rest’’) to the
Records were reviewed for consecutive non-elderly (\ 65) Hmax position (‘‘Hant-max’’). The relationship between
and elderly (C 65 years) male and female non-dysphagic superior and anterior hyoid displacement was calculated by
patients who presented for VFSS at an outpatient, tertiary dividing Hsup by Hant, in order to get the superior-to-an-
swallowing center. Non-dysphagic patients were included terior hyoid displacement ratio (SAratio). See Figs. 1a–d for
if VFSSs revealed a Functional Oral Intake Scale (FOIS) more detailed instructions on measurement methodology.
score of 1; a Penetration Aspiration Scale score B 2;

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604 J. Curtis et al.: Superior and Anterior Hyoid Displacement…

A B

P1

P2

C D

Hant-max Hsup-max
P1 P1
Hant-rest Hsup-rest
P2
P2

Fig. 1 a Measurement methodology: Establish horizontal and vertical to the P1–P2 line drawn in Fig. 1b until a 908 intersection is made.
planes relative to the larynx during a pseudo-rest position (1 cc bolus Extend the P1–P2 line superiorly as needed. Measure the distance
hold) by connecting the anterior-inferior hyoid to anterior–superior from P2 to the 908 intersection (‘‘Hsup-rest’’) and the distance from the
tracheal air column. b Move the line established in Fig. 1a from the hyoid to the 908 intersection (‘‘Hant-rest’’). d Advance to the point of
larynx to the spine with rotation or distortion. Ensure that the line maximal overall hyoid displacement (Hmax). Repeat the instructions
crosses over the anterior-inferior point of cervical spine 2 (P1). Make outlined in Fig. 1c by retracing a line using the original P1 and
note of a second identifiable point (P2) that is inferior to both P1 point P2 points. Trace a line from the anterior-inferior hyoid until
and the hyoid bone but that also lays along the same line—extend the a 908 intersection is made. Measure from P2 to the 908 intersection
line inferiorly as necessary. In this example, P2 is along the superior (‘‘Hsup-max’’), and from the hyoid to the 908 intersection (‘‘Hant-max’’)
border of C4. c Next, trace a line from the anterior-inferior hyoid bone

Data Abstraction and Reliability Testing Statistical Analysis

All measures were performed by one primary rater (JC). Descriptive statistics were performed for demographic
Ten percent of the video clips were selected at random and information, Hmax, Hsup, Hant, and SAratio. A mixed-design
were repeated for analysis 1 week later by the primary rater repeated-measures analysis of variance (ANOVA) with
to facilitate intra-rater reliability estimation. A second rater post hoc analysis and Bonferroni corrections, using bolus
(JL) analyzed the same randomly selected video segments size (1, 3, 20 cc) as a within-subject factor, and age
in order to assess inter-rater reliability. Both raters (elderly and non-elderly) and gender (male and female) as
had C 2 years of experience performing DSS kinematic between subject-factors, was used to assess differences
analysis and were blinded to patient’s history and identity. with Hsup, Hant, and SAratio as a function of age, sex, and
bolus size. A p \ 0.05 was set as the significance level for
all statistical tests. Two-way random effects, absolute

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J. Curtis et al.: Superior and Anterior Hyoid Displacement… 605

agreement, intraclass correlation coefficients (ICC) were Table 1 Maximal superior hyoid displacement (Hsup) in millimeters
used to calculate intra- and inter-rater reliabilities. Inter- (mm)
pretation of ICC was judged to be ‘excellent’ if C 0.90, Bolus size
‘good’ if between 0.75 and 0.90, ‘moderate’ if between
1 cc 3 cc 20 cc
0.50 and 0.75, and ‘poor’ if \ 0.50 [35]. Statistical anal-
yses were performed using SPSS statistical package ver- Men \ 65 16.4 ± 6.4 17.4 ± 6.6 21.8 ± 7.2
sion 24 (SPSS Inc., Chicago IL). (3.8–29.3) (7.6–33.1) (5.3–39.1)
Women \ 65 12.1 ± 4.1 13.5 ± 4.1 16.2 ± 5.3
(2.8–20.8) (2.2–20.7) (2.2–28.4)
Results Men C 65 14.9 ± 4.4 16.3 ± 5.4 18.1 ± 5.4
(4.2–26.2) (5.5–29.4) (6.6–31.1)
Patient Demographics Women C 65 12.8 ± 5.3 13.8 ± 4.8 17.3 ± 5.6
(3.7–23.6) (5.6–25.0) (5.7–27.8)
One hundred sixty-five patients met the above inclusion–
Mean ± standard deviation (range) of superior hyoid displacement
exclusion criteria and were included for initial study (Hsup) for elderly and non-elderly males and females for 1, 3, and
analysis. Four of the exams were extreme outliers ([ 3 SD 20 cc boluses
away from the Hmax mean) and were therefore excluded. A
total of 161 exams were included in the final analysis. Non-
elderly men (n = 39) had an average age of 50.3 years 312) = 3.712, p = 0.026, partial g2 = 0.023 (Fig. 2).
(± 12.1), with an age range from 18 to 64 years. Elderly Statistical significance of a simple two-way interaction was
men (n = 42) had an average age of 76.7 years (± 7.7), accepted at a Bonferroni-adjusted alpha level of 0.025.
with an age range from 65 to 94 years. Non-elderly women There was a statistically significant simple two-way inter-
(n = 46) had an average age of 46.5 years (± 13.8), with action of sex and age for 20 cc bolus size, F (1,
an age range from 18 to 64 years. Elderly women (n = 34) 156) = 6.254, p = 0.013, but not for 1 cc or 3 cc bolus
had an average age of 77.3 years (± 8.9), with an age sizes (p [ 0.05). Statistical significance of a simple simple
range from 65 to 96 years. main effect was accepted at a Bonferroni-adjusted alpha
level of 0.025. There was a statistically significant simple
Intra- and Inter-rater Reliabilities simple main effect of age for males for 20 cc bolus size,
F (1, 156) = 7.758, p = 0.006, but not for females
Sixteen exams were selected at random and yielded a total (p [ 0.05).
of 102 repeated anterior and superior hyoid displacement
measures. Intraclass correlation coefficient estimates Anterior Hyoid Displacement (Hant)
demonstrated excellent inter-and intra-rater reliabilities for
superior hyoid displacement and good intra-and inter-rater Age, sex, and bolus size norms [mean ± standard devia-
reliabilities for anterior hyoid displacement. For Hsup, tion (range)] are outlined for Hant (Table 2). Hant was sta-
inter-rater ICC was 0.929 (95% CI 0.866–0.962) and intra- tistically effected by bolus size, F (2, 312) = 6.845,
rater ICC was 0.973 (95% CI 0.951–0.986). For Hant, inter- p = 0.001, and age, F (1, 156) = 10.449, p = 0.001, but
rater ICC was 0.821 (95% CI 0.639–0.908) and intra-rater not sex (p [ 0.05). Pairwise comparisons were performed
ICC was 0.887 (95% CI 0.801–0.938). for statistically significant differences between bolus size
with Bonferroni corrections being made, revealing signif-
Superior Hyoid Displacement (Hsup) icant differences (p \ 0.01) between 1 and 3 cc and 1 and
20 cc, but not between 3 and 20 cc (p = 0.497). Three-
Age, sex, and bolus size norms [mean ± standard devia- way mixed ANOVA was run to understand the effects of
tion (range)] are outlined for Hsup (Table 1). Hsup was age, sex, and bolus size on Hant. There were no statistically
significantly effected by bolus size, F (2, 312) = 94.158, significant three- or two-way interactions between age, sex,
p \ 0.005, and sex, F (1, 156) = 16.869, p \ 0.0005, but and bolus size (p [ 0.05). Statistical significance of a
not age (p [ 0.05). Pairwise comparisons were performed simple simple main effect was accepted at a Bonferroni-
for statistically significant differences between bolus size adjusted alpha level of 0.025.
with Bonferroni corrections being made, revealing signif-
icant differences (p \ 0.0005) between all three bolus sizes
(i.e., 1 and 3 cc, 1 and 20 cc, and 3 and 20 cc). Three-way
mixed ANOVA revealed a statistically significant three-
way interaction between age, sex, and bolus size, F (2,

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Fig. 2 Three-way interaction between age, sex, and 20 cc bolus size for superior hyoid displacement, with simple simple main effects between
young and elderly males

Table 2 Maximal anterior hyoid displacement (Hant) in millimeters


(mm)
Discussion
Bolus size This study establishes normative data for superior and
1 cc 3 cc 20 cc anterior hyoid displacement, and the ratio between these
two measures, for elderly and non-elderly males and
Men \ 65 8.0 ± 3.7 8.5 ± 3.5 8.5 ± 4.0
females for 1, 3, and 20 cc liquid boluses within the con-
(- 1.2 to 16.5) (0.4–16.9) (0.6–18.1)
text of the Hmax DSS measurement. Superior and anterior
Women \ 65 7.0 ± 3.7 7.8 ± 3.6 7.9 ± 4.7
hyoid displacement varied significantly by bolus size. Sex
(- 3.3 to 13.9) (- 3.0 to 15.6) (- 3.3 to 17.0)
was noted to significantly impact superior hyoid displace-
Men C 65 5.9 ± 3.2 6.2 ± 3.4 6.8 ± 3.5
ment but not anterior hyoid displacement. Age was seen to
(- 0.3 to 11.2) (- 2.4 to 14.9) (- 2.4 to 14.9)
significantly impact anterior hyoid displacement, but not
Women C 65 5.8 ± 3.1 6.0 ± 3.6 6.6 ± 3.4 superior hyoid displacement. Neither bolus size, age, nor
(- 0.9 to 12.3) (- 1.0 to 14.7) (- 0.9 to 12.4) sex significantly impacted the ratio of superior to anterior
Mean ± standard deviation (range) of anterior hyoid displacement hyoid displacement. Generally speaking, superior and
(Hant) for elderly and non-elderly males and females for 1, 3, and anterior displacements became larger with increasing bolus
20 cc boluses
sizes, and was larger in males compared to females, and
non-elderly when compared to elderly. These findings are
similar with previous studies, which demonstrate that hyoid
Superior-to-Anterior Ratio of Hyoid displacement increases with increasing bolus sizes, and
Displacement (SAratio) may be impacted by age and sex [11, 16–18, 29].
The hyoid bone was found to frequently move an
Age, sex, and bolus size norms [mean ± standard devia- average of two to three times more superiorly than as it
tion (range)] are outlined for SAratio (Table 3). SAratio was does anteriorly. In some instances, anterior displacement
not significantly effected by bolus size, age, or sex was noted to be negative, in other words, moving slightly
(p [ 0.05). A three-way mixed ANOVA was run to posterior at time of maximal overall hyoid displacement. It
understand the effects of age, sex, and bolus size on SAratio. is unclear if these patterns for increasingly larger superior-
There were no statistically significant three- or two-way to-anterior hyoid displacement ratios and large variability
interactions between bolus size, age, and sex for SAratio of anterior hyoid displacement reflect outcomes inherent to
(p [ 0.05). this measurement methodology (both superior and anterior

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Table 3 Ratio of superior to


Bolus size
anterior hyoid displacement
(SAratio) 1 cc 3 cc 20 cc

Men \ 65 2.3 ± 3.3 3.2 ± 5.6 4.0 ± 5.4


(- 9.9 to 16.8) (0.4–36.0) (0.3–34.3)
Women \ 65 2.8 ± 5.0 2.2 ± 2.4 2.6 ± 10.6
(- 2.5 to 33.5) (- 2.8 to 14.4) (- 33.8 to 61.3)
Men C 65 3.7 ± 9.8 3.4 ± 3.8 3.5 ± 4.5
(- 36.1 to 45.2) (- 7.5 to 17.8) (- 7.7 to 26.1)
Women C 65 2.6 ± 5.2 1.5 ± 15.9 3.0 ± 5.3
(- 18.7 to 18.2) (- 70.0 to 42.8) (- 19.8 to 16.8)
Means ± standard deviation (range) for the ratio of superior to anterior hyoid displacement (SAratio) for
elderly and non-elderly males and females for 1, 3, and 20 cc boluses

measures taken at the same point in time), or if they truly point of analysis for the two measures in this study in an
demonstrate a highly variable nature in anterior hyoid effort to minimize clinical burden by collapsing three
movement in normal swallow function. This result is sig- separate hyoid displacement time frames into one, there-
nificant, as findings of marginal-to-nil (or even negative) fore reducing the time required to collect and calculate the
anterior hyoid displacements relative to large superior measures. All that is needed to obtain Hmax is a
hyoid displacements may not reflect a disrupted swallow Pythagoreans theorem calculation, rather than an additional
pattern, but rather be a variant of normal healthy swallow, measurement, where Hmax = (H2sup ? H2ant)0.5.
as was observed with multiple exams in the present study. The main limitation of this study is that analyses were
This finding would also call into question the extent to performed on ‘‘non-dysphagic’’ individuals previously seen
which anterior hyoid displacement plays in functional air- in an outpatient otolaryngology clinic rather than on
way protection and pharyngoesophageal segment opening healthy volunteers. Strict inclusion–exclusion criteria were
in non-dysphagic and dysphagic patients. established to rule out abnormal physiology and people
Two key points should be noted when extrapolating the with compromised bolus clearance and airway protection;
data for swallow function interpretation. Firstly, Hsup and however abnormal physiology not representative of healthy
Hant displacement measures are made by establishing ver- volunteers cannot be ruled out. However, one could argue
tical and horizontal planes relative to the orientation of the that even if the findings of the present study were not
larynx. This methodology varies from many studies eval- representative of ‘‘normal healthy’’ physiology, the present
uating superior and anterior hyoid displacement norms, information is still valuable in understanding the deviant
which use vertical and horizontal planes relative to the non-dysphagic physiology that still results in complete
lateral fluoroscopic viewing plane or anterior aspects of the bolus clearance and airway protection.
spine, and as a result, superior movement appears generally
longer and anterior movement appears generally shorter
than previously reported [6, 18, 21, 36–38]. Secondly, it Conclusion
should be recognized that while maximal anterior and
superior hyoid displacements tend to occur within close This study presents age, sex, and bolus size norms for Hsup,
temporal proximity to each other, these displacement Hant, and SAratio, taken at time at maximal hyoid dis-
measures often occur at different time points during the placement (Hmax), within the context of a Dynamic Swal-
swallow. Hsup and Hant may therefore not reflect true low Study protocol for videofluoroscopic swallow studies.
maximal superior and anterior hyoid displacements outside Establishing normative data for anterior and superior hyoid
of the context of DSS’s Hmax. However, Hmax was chosen displacement should allow clinicians using DSS to more
as the single point of analysis for Hsup and Hant measure- thoroughly identify areas of swallowing impairment,
ments in hopes of capitalizing on the excellent reliability determine targets for therapeutic intervention, and track
that was previously reported for Hmax. This method proved individual physiologic changes over time.
successful, as the reliability of the present two measures
also appear to have good-to-excellent intra- and inter-rater Acknowledgements The authors thank Michelle Troche, PhD, CCC-
SLP for contributions to manuscript review and statistical guidance.
reliabilities. Further, the Hmax was chosen as the single

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