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Hyoid Movement During Swallowing in Older Patients With Dysphagia
Katherine A. Kendall, MD;
Rebecca J. Leonard, PhD
Arch Otolaryngol Head Neck Surg. 2001;127:1224-1229.
ABSTRACT
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Objectives To describe the timing, coordination, and extent of hyoid movement in
a population of older adults with dysphagia and to evaluate the effect of
hyoid movement on upper esophageal sphincter opening.
Design A retrospective review of dynamic swallow studies performed between
January 1996 and December 1999 was done.
Subjects Patients included in the study were 65 years or older, without an obvious
medical or surgical cause for their dysphagia. Timing and distance measures
of hyoid movement from the patient population were compared with those from
60 younger (range, 18-62 years) and 23 older (range 67-83 years) control subjects
without dysphagia using 1-way analysis of variance. Analysis of the effect
of hyoid movement on upper esophageal sphincter opening was performed using
contingency tables.
Results In an older population with dysphagia, the coordination of swallowing
gestures and bolus timing was intact, hyoid elevation was slow, and the duration
of maximal hyoid elevation was reduced, but appropriate for the age of the
patients. The hyoid bone elevated farther than normal for small bolus sizes,
but the patients were unable to maintain this strategy in larger bolus swallows.
Conclusion An increased extent of hyoid displacement in older patients with dysphagia
may represent a necessary compensation designed to minimize the effect of
the short duration of hyoid elevation on the upper esophageal sphincter opening.
INTRODUCTION
ALTHOUGH swallowing impairment occurs in all age groups, older persons
represent the largest affected group. Isolated swallowing difficulties are
present in a substantial percentage of older adults, and a common sequela
of dysphagia in this age group is aspiration, with subsequent pneumonia. The
prevalence of dysphagia is 50% in nursing homes.1
Furthermore, the incidence of identifiable swallowing abnormalities is greater
in older patients with dysphagia compared with younger patients who have swallowing
difficulties.2 The clinical effects of dysphagia
in older persons warrant an in-depth analysis of the specific types of abnormalities
occurring in this patient population.
Although multiple swallowing abnormalities are likely to be present
in patients with dysphagia, this study focuses on hyoid function in a population
of older patients with dysphagia. The hyoid bone moves during swallowing as
a result of suprahyoid muscle contraction.3-6
Hyoid movement is required for adequate opening of the upper esophageal sphincter
(UES) and is readily measured from a videofluoroscopic dynamic swallow study.7-8 The timing and extent of hyoid elevation
were included in the analysis. In addition, the coordination of hyoid motion
with movement of the bolus through the pharynx and the effect of hyoid movement
characteristics on UES opening were assessed. The evaluation of the coordination
of swallowing gestures relative to bolus transit enables us to identify cases
in which gesture timing is altered secondary to pathologic conditions or is
used as a strategy to overcome functional abnormalities.
MATERIALS AND METHODS
Dynamic swallow studies performed between January 1996 and December
1999 were reviewed. Those studies from patients 65 years or older with a primary
diagnosis of dysphagia of unknown etiology were included in the study. A primary
diagnosis of dysphagia of unknown etiology was designated if the patient had
no other obvious diagnosis that could cause dysphagia, such as neuromuscular
disease or recent stroke.
The radiographic studies were conducted in the Voice-Speech-Swallowing
Center at University of California, Davis, Medical Center, Sacramento, in
accordance with the routine radiographic protocols approved by the institution.
Equipment used included a properly collimated radiographic and fluoroscopic
unit (Phillips Medical Systems North America Co, Shelton, Conn) that provides
a 63-kV, 1.2-mA output for the full field-of-view mode (22.9-cm input phosphor
diameter). Fluoroscopy studies were recorded on high-quality videotape for
playback and analysis using a videocassette VHS recorder and player (model
1380; Sony Corporation of America, New York, NY). A graphic time display provided
by a character generator (RCA Corp, Indianapolis, Ind) and an alternating
current adapter (model C412; JVC, Wayne, NJ) were included on the videotape,
so that timing information at 0.01-second intervals was recorded. The swallowing
studies were recorded at 30 frames per second. Measurements were made during
the swallowing of 1-mL and 20-mL liquid boluses (Liquid Barosperse barium
sulfate suspension; Lafayette Pharmaceuticals, Inc, Anaheim, Calif). Material
to be swallowed was presented to the subject by cup.
The videotaped images were later captured with a digitizing board (Data
Translation, Inc, Marlboro, Mass) and computer (PPC 9500, Macintosh; Apple
Computers Inc, Cupertino, Calif). A software program in the public domain
(Image; available at: http://rsb.info.nih.gov/nih-image, developed by Wayne Rasband, MS, and colleagues, National Institute
of Mental Health, Bethesda, Md) was used for analysis of fluoroscopic images.
Distance measurements were made after calibration of the digitized image to
the size of the 1.7-cm-diameter wire loop taped to the chin of the study subject.
All measurements were obtained from lateral views. A detailed technical
description of these measures and their acquisition has been previously published7 and is briefly summarized herein. Maximal hyoid elevation
was measured as the distance between the hyoid position at bolus "hold," ie,
when the bolus is held in the oral cavity, and its point of maximal anterior
and superior excursion during the swallow. The first superior-anterior movement
of the hyoid that resulted in a swallow was designated H1. H2 was the point
at which the hyoid achieved maximal displacement during the swallow. The instant
the hyoid began its descent to a resting position was designated H3. The time
required for hyoid elevation (H2-H1) and the duration of maximal hyoid elevation
(H3-H2) can be calculated.
Bolus pharyngeal transit time was defined as the time between the onset
and completion of bolus pharyngeal transit. The onset of pharyngeal transit
was designated B1 and was defined as the first movement of the head of the
bolus from a stable, or "hold," position that passed the posterior nasal spine
and resulted in all or part of the bolus entering the oropharynx. The posterior
nasal spine is located at the end of the hard palate and is a good landmark
for the anterior border of the oropharynx. Pharyngeal transit was complete
when the tail of the bolus was fully within the UES. Pharyngeal transit time
can be divided into an oropharyngeal and a hypopharyngeal phase by the arrival
of the bolus in the vallecula (BV). If the bolus bypassed the vallecula, the
time when the bolus passed the level of the base of the vallecula was designated
BV. Hyoid movement relative to the onset of bolus pharyngeal transit (H1-B1)
and relative to the arrival of the bolus in the vallecula (H1-BV) can be calculated.
Maximal opening of the UES was measured at the narrowest part of the
upper esophagus between C4 and C6 during maximal distension. We believe that
this point best defines the location of the UES. It is also reliably identified
on a dynamic swallow study, as opposed to a measurement made from the often
poorly defined top of the air column in the trachea.9
The data from the measured variables were averaged across subjects according
to bolus size. Patient means were then compared with the means from dynamic
videofluoroscopic swallow studies performed on 60 volunteers without dysphagia
aged 18 to 62 years, and with the means from studies performed on 23 older
volunteers without dysphagia aged 67 to 83, using 1-way analysis of variance.
Posttests were done to evaluate differences between individual pairs of groups.
A Bonferroni correction was applied to take into account that multiple comparisons
were performed. The overall P values, the uncorrected P values determined from comparisons between groups, and
the Bonferroni corrected P values are reported.
The younger control group consisted of 30 men and 30 women. There were
10 men and 13 women in the older control group. None of the control subjects
had symptoms of dysphagia or gastroesophageal reflux disease, a history of
central nervous system or craniofacial abnormalities, or other medical problems.
They took no medications. All of the controls were respondents to advertisements
asking for volunteers to participate in the study. Screening of prospective
participants was carried out to ensure they fit the study criteria. Each volunteer
was examined to rule out potential anatomic abnormalities in the head and
neck region.
The relationship of specific swallowing gestures to one another in individual
patients was analyzed using linear regression. Any abnormality in the opening
size of the UES was noted for each patient and was defined as less than 2
SDs from the mean of the younger controls. Fisher exact test contingency tables
were used to analyze the relationship between UES opening size and duration
of hyoid elevation.
During the study, 1315 dynamic swallow studies were performed. Of those,
361 (27.5%) were performed in individuals 65 years or older. The diagnostic
categories in the patient population are listed in Table 1. Only patients in the first category, nonspecific dysphagia,
were included in the study. When subsequent studies in the same individuals
were excluded, the final number of patients included in the study was 65 (age
range, 65-89 years). Only 8 of the 65 patients (12%) did not have at least
one other medical problem, such as hypertension, diabetes, or arthritis.
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Table 1. Diagnostic Categories in 361 Patients
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Not all patients had complete data available for analysis. Hyoid displacement
data were often available for only one bolus size per patient. Reported results
include the number of patients with data available for each measured variable.
A swallow study variable was defined as normal if it was within 2 SDs of the
normal mean. For ease of comparison, results from control subjects are reported
in the tables alongside those from the patients. A list of abbreviations used
in the text is provided in Table 2 for reference.
RESULTS
Differences in the timing and extent of hyoid bone elevation between
the patient population and younger controls were identified in this study.
However, when the data from the patient population were compared with those
from the older controls, more subtle differences were identified.
The onset of hyoid elevation (H1) relative to the onset of bolus pharyngeal
transit (B1) was delayed in the patient population compared with the younger
controls for both bolus categories. H1 was also delayed in the older control
group, but not to the extent found in the patient group (Table 3). The point at which the hyoid reached maximal elevation
(H2) and the point at which the hyoid began its descent back to a resting
position (H3) were similarly delayed in the patient population compared with
the younger controls. Again, the timing of these events relative to the onset
of bolus pharyngeal transit was delayed in the older controls compared with
the younger controls, but not to the extent found in the patient group (Table 4 and Table 5). Some delay in the timing of hyoid movements is expected
in older persons. Although the difference in data between the patient group
and the older controls did not reach statistical significance, a trend toward
greater delays in the patient population was identified.
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Table 3. Onset of Hyoid Elevation (H1-B1)
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Table 4. Hyoid Reaches Maximal Elevation (H2-B1)
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Table 5. Onset of Hyoid Descent (H3-B1)
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To evaluate the coordination of hyoid movement with the position of
the bolus in the pharynx, H1 was compared with BV. In younger persons without
swallowing abnormalities, the hyoid begins to elevate just after the arrival
of the bolus in the vallecula.10 In the patient
population and in the older controls in our study, this relationship was maintained
for the 1-mL bolus. For the 20-mL bolus in the patient group, the hyoid bone
began to elevate early relative to the arrival of the bolus in the vallecula
(Table 6). To summarize, coordination
of hyoid elevation with the position of the bolus in the pharynx was normal
or slightly early in the patient population.
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Table 6. Onset of Hyoid Elevation Relative to Arrival of the Bolus
in the Vallecula (H1-BV)
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Once hyoid elevation began, the time required for the hyoid to reach
maximal elevation (H2-H1) was prolonged in the patient population relative
to the younger controls for both bolus categories. When the patient population
was compared with the older controls, no difference in H2-H1 was identified
(Table 7). The hyoid was held
maximally elevated (H3-H2) for a shorter duration in the patient population
and in the older control group for the 1-mL bolus, and tended toward shorter
duration of elevation for the 20-mL bolus (Table 8). The duration that the hyoid was elevated (H3-H1), however,
was not significantly different among the 3 groups (Table 9). Because the patients and the older control subjects took
longer to elevate the hyoid bone maximally and held it elevated for a shorter
duration, compared with the younger controls, it is possible that this difference
is due to aging rather than pathophysiologic conditions.
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Table 7. Time Required for Hyoid to Reach Maximal Elevation (H2-H1)
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Table 8. Duration of Maximal Hyoid Elevation (H3-H2)
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Table 9. Hyoid Elevation Duration (H3-H1)
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To determine if the shorter duration of maximal hyoid elevation (H3-H2)
corresponded directly to longer times required to achieve the maximal position
(H2-H1), bolus-specific regression analysis comparing the 2 variables in individual
patients was performed. No direct relationship was identified.
The extent of hyoid displacement was analyzed separately for men and
women, because of previously identified sex differences in this variable.8 Women in the patient population elevated the hyoid
much farther than did younger female controls for the 1-mL bolus, and to a
normal extent for the 20-mL bolus. The older female controls also elevated
the hyoid bone to a greater extent for a 1-mL bolus than did younger female
controls, but not to the extent found in the female patients (Table 10). A review of individual data revealed that none of the
women with dysphagia had decreased hyoid elevation during a 1-mL swallow.
Four of the women had decreased hyoid elevation on a 20-mL bolus, but the
overall means from the 3 groups were not significantly different.
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Table 10. Hyoid Displacement
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Men with dysphagia also demonstrated greater than normal hyoid elevation
during a 1-mL bolus swallow compared with younger male controls, but the difference
did not reach statistical significance. The older male controls also elevated
the hyoid bone farther than the younger male controls, but not to the extent
found in the men with dysphagia. Data on hyoid elevation during a 20-mL bolus
swallow were available for only 5 male patients. Three of these patients had
decreased hyoid elevation during the swallow of the larger bolus, and the
overall mean was significantly less than those from the younger and older
control groups (Table 11).
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Table 11. Hyoid Displacement
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The distance of hyoid bone elevation is usually greater for the larger
bolus categories. Patients elevated the hyoid bone significantly farther than
normal during a small bolus swallow. Perhaps, this finding represents a strategy
that compensates for other abnormalities. It was also seen, but to a lesser
extent, in the older control group. However, on the larger bolus swallows,
the patient population could not maintain this strategy, and the distance
of hyoid elevation diminished to normal or below normal levels. Although the
difference identified in the older control group did not reach statistical
significance, a trend toward farther elevation of the hyoid during a larger
bolus swallow was found.
To determine if the prolonged time required for the hyoid to reach maximal
elevation was directly related to an increased distance of hyoid elevation,
regression analysis comparing bolus-specific H2-H1 in each patient to the
distance of hyoid elevation in that patient was performed. The analysis failed
to reveal a consistent relationship, however. Similar analyses did not identify
any relationship between the duration the hyoid was held at maximal elevation
(H3-H2), the duration of hyoid movement (H3-H1), and the extent of hyoid displacement
in individual patients.
A Fisher exact test revealed that decreased extent of hyoid elevation
was statistically related to a decreased maximal opening of the UES (P = .004). The converse was not true. That is, greater
hyoid elevation was not correlated with a larger UES opening size. No correlation
was found between the distance or duration of hyoid elevation and the duration
of UES opening.
In summary, although the timing of hyoid elevation in the patient population
was delayed relative to the onset of bolus pharyngeal transit, this was also
found in the older control group. Only a trend toward greater delays in the
patient population compared with the older controls was identified. Likewise,
the increased time in the patient population required to achieve maximal hyoid
elevation once elevation was initiated, and the decreased duration the hyoid
was held at maximal elevation, was also found in the older controls. No inverse
relationship between the time required to reach maximal elevation and the
duration of maximal elevation was found, although the overall duration of
hyoid movement (H3-H1) did not differ between any of the groups. The coordination
of hyoid elevation with the arrival of the bolus in the vallecula was maintained
in the older groups for 1-mL boluses, and was early relative to the arrival
of the bolus in the vallecula in the patient population for 20-mL boluses.
The distance of hyoid elevation was greater in both older groups for the 1-mL
bolus compared with the younger controls. The patients were unable to maintain
this strategy during deglutition of larger boluses, while the older controls
did. A linear relationship between the distance of hyoid elevation and the
time required for hyoid elevation was not demonstrated, but a relationship
between diminished hyoid elevation and smaller UES opening size was found.
COMMENT
The evaluation of older patients with dysphagia is complicated by the
need to distinguish deglutitive changes due to pathophysiologic conditions
from those expected with normal aging. Aging of elastic fibers in connective
tissues of the neck, sensory end-organ deterioration, and muscular weakness
affecting oropharyngolaryngeal structures have been presumed to interfere
with swallowing function. These assumptions are based on studies documenting
the results of aging on the mammalian neuromuscular system. However, changes
in muscles with age appear to be associated with disuse atrophy, which supports
the hypothesis that only minor changes in the muscles of the oropharynx, used
constantly for swallowing, can be attributed to aging alone.1, 11-12
Systemic factors, rather than normal aging, may be important in explaining
muscular weakness and fatigue seen in older persons. On the other hand, the
older control group in this study, in whom clear differences from the younger
controls were identified, took no medication and denied other medical problems.
Previous studies13-14 have
identified changes in swallowing function in older subjects who do not complain
of difficulty swallowing, in particular, slower bolus transit through the
pharynx. Because coordination of hyoid movement with bolus position in the
pharynx was preserved in the older subjects evaluated in this study, slower
bolus transit could account for the delay in the onset of hyoid movement relative
to the onset of bolus transit that was identified. Previous studies4, 10, 15 in younger subjects
without swallowing abnormalities demonstrate that the onset of hyoid bone
elevation is linked to the location of the bolus in the pharynx rather than
to changes in the size of the bolus. The findings of this study indicate that
this relationship is preserved in older persons with and without dysphagia.
The early onset of hyoid elevation observed in the patient population with
a larger bolus size may be a strategy designed to compensate for abnormalities,
such as poor UES compliance.
Although the hyoid elevated slowly and remained maximally elevated for
a shorter duration in older subjects compared with the younger controls, it
elevated farther. This phenomenon was more dramatic for the 1-mL boluses than
for the 20-mL boluses. Previous research in younger subjects without swallowing
abnormalities has found greater displacement of the hyoid on swallowing of
a larger bolus volume.8, 10 Perhaps
greater displacement reflects compensation for slower hyoid elevation and
shorter duration at maximal elevation. This compensation may break down with
larger boluses in patients with dysphagia. If so, one implication of the finding
would be the clinical application of restricted bolus volume in patients demonstrating
poor hyoid elevation.
None of the previous studies of hyoid elevation in older persons evaluated
the timing and the extent of hyoid bone elevation. Similar to the findings
of this study, Rademaker and coworkers14 found
that the overall duration of hyoid motion was unchanged in older women without
dysphagia compared with younger female controls. Sonies et al16
found that the time required to reach maximal elevation was longer in an older
population (N = 19) but, contrary to the findings of this study, noted that
the duration at maximal elevation was also longer.
Previous manometric studies of UES function in older persons have demonstrated
lower UES resting tone and higher pressures at maximal distension. However,
using simultaneous videofluoroscopy and manometry, Shaw and coworkers9 found that the sagittal diameter (measured in the
lateral view) of the UES was unchanged in an older population without dysphagia,
while the transverse diameter (measured in the anterior-posterior view) was
diminished. Elevation of the hyoid is essential for UES opening.5, 17-19
In our study, despite the hyoid's slower rate of elevation and shorter duration
once maximally elevated, no link to changes in UES opening in the lateral
view was identified in the patient group, as long as the hyoid displacement
was normal or greater than normal. If, in addition to a slow and reduced duration
of hyoid elevation, the extent of elevation was diminished, however, a correlation
with decreased size of UES opening could be identified.
The coordination of hyoid movement remained intact in this older patient
population with dysphagia. However, the gestures may have been slow and weak
because of aging, and compensatory strategies (greater extent of hyoid elevation)
may have been required to maintain sufficient upper esophageal opening. Failure
of compensatory strategies may have led to symptoms of dysphagia. Although
the patients in this study did not have medical or surgical histories that
could be directly related to their dysphagia, the high incidence of other
medical problems in this patient population must be considered as possible
etiologic factors. Further study is needed to differentiate changes in swallowing
function that result from intercurrent disease. In the meantime, strategies
and therapies designed to improve the distance of hyoid elevation may be helpful.
AUTHOR INFORMATION
Accepted for publication May 16, 2001.
Corresponding author and reprints: Katherine A. Kendall, MD, Department
of Otolaryngology, University of California, Davis, Medical Center, 2521 Stockton
Blvd, Suite 7200, Sacramento, CA 95817 (e-mail: katherine.kendall{at}ucdmc.ucdavis.edu).
From the Department of Otolaryngology, University of California, Davis,
Medical Center, Sacramento.
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