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.
A retrospective review of dynamic swallow studies performed between January 1996 and December 1999 was done.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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: email@example.com).
B Aging and neurological disease.
In: Normal and Abnormal Swallowing Imaging in Diagnosis and Therapy.
New York, NY: Springer-Verlag NY Inc; 1991:189-202.
MY Functional abnormalities of the pharynx: a prospective analysis of radiographic abnormalities relative to age and symptoms. AJR Am J Roentgenol.
et al Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol.
1990;258(suppl 5, pt 1):G675-G681.Google Scholar
MK The effect of bolus volume and consistency on swallow-induced submental and infrahyoid electromyographic activity. Braz J Med Biol Res.
RJ Quantitative relationship between liquid bolus flow and laryngeal closure during deglutition. Am J Physiol.
1993;265(suppl 4, pt 1):G704-G711.Google Scholar
et al Timing of videofluoroscopic, manometric events, and bolus transit during the oral and pharyngeal phases of swallowing. Dysphagia.
R Dynamic swallow study: objective measures and normative data and dynamic swallow study: instrumentation and measurement techniques.
In: Dysphagia Assessment and Treatment Planning: A Team Approach.
San Diego, Calif: Singular; 1997:101-160.
A Structural displacements mobility in normal swallowing: a videofluoroscopic study. Dysphagia.
et al Influence of normal aging on oral-pharyngeal and UES function during swallowing. Am J Physiol.
A Timing of events in normal swallowing: a videofluoroscopic study. Dysphagia.
BC Oropharyngeal dysphagia in the elderly. Clin Geriatr Med.
GB Oropharyngeal swallowing in normal adults of different ages. Gastroenterology.
JA Age and volume effects on liquid swallowing function in normal women. J Speech Lang Hear Res.
FMS Timing of major events of pharyngeal swallowing. Arch Otolaryngol Head Neck Surg.
BJ Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia.
FMS Analysis of pressure generation and bolus transit during pharyngeal swallowing. Laryngoscope.
JA Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR Am J Roentgenol.