Age-Related Changes of Hyoid Bone Position in Healthy Older Adults With Aspiration
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1 The Laryngoscope VC 2013 The American Laryngological, Rhinological and Otological Society, Inc. Age-Related Changes of Hyoid Bone Position in Healthy Older Adults With Aspiration Xin Feng, MD, PhD; Tee Todd, MD; Yunping Hu, MD, PhD; Catherine R. Lintzenich, MD; J. Jeffrey Carr, MD; James D. Browne, MD; Stephen B. Kritchevsky, PhD; Susan G. Butler, PhD Objectives/Hypothesis: Aspiration, the passage of a bolus below the vocal folds, increases morbidity and mortality in the elderly by increasing the risk of aspiration pneumonia and other conditions. We hypothesized that altered position of the hyoid bone associated with aging may negatively affect airway protection during swallowing (i.e., aspiration) in older adults. Study Design: Retrospective study. Methods: We re-reviewed computed tomography (CT) scans of the head from 40 older adults (65 80 years old), comprised of 20 aspirators and 20 nonaspirators, obtained from a previous cohort study. In addition, CT scans of the head from 40 young adults (20 40 years old) were retrieved from a medical records database. Three-dimensional reconstruction and 2- dimensional sagittal views were used to measure the distance between the mandible and hyoid bone. Comparisons between age groups, genders, and aspiration status were made. Results: Older adults had a larger distance between the hyoid and mandible in both latitude and longitudinal positions compared to the young adults. Among older males, there was evidence that the hyoid bone in the aspirators tended to be positioned more posterior compared to the nonaspirators. Conclusions: The distance between the hyoid and mandible is increased with aging, and a more posterior position of the hyoid bone is correlated with aspiration in older males. These findings suggest that age-related changes in hyoid bone position may be a component of decreased swallowing safety and aspiration in older adults and warrant further investigation. Key Words: Mandible, hyoid, aging, aspiration, swallowing, computed tomography. Level of Evidence: N/A. Laryngoscope, 124:E231 E236, 2014 INTRODUCTION Prandial aspiration is the passage of food or liquid below the level of the vocal folds. The incidence of aspiration increases with age. 1 Silent aspiration, defined as aspiration in the absence of cough, 2 often occurs in healthy older adults with no sequelae. 3 5 However, studies have shown that aspiration increases risk of aspiration pneumonia, dehydration, malnutrition, and other disorders. 6 8 The etiology of aspiration is multifactorial, and may be secondary to gastroesophageal reflux disease, dysphagia (neurogenic and nonneurogenic), or other conditions. 3,4,7,8 From the Department of Otolaryngology (X.F., T.T., C.R.L., J.D.B., S.G.B.); and the Department of Neurosurgery (Y.H.); and Department of Radiology (J.J.C.); and Department of Internal Medicine, Section on Gerontology and Geriatric Medicine and Sticht Center on Aging (S.B.K.), Wake Forest School of Medicine, Winston-Salem, North Carolina, U.S.A. Editor s Note: This Manuscript was accepted for publication September 25, This work was supported by NIDCD grant R03 DC009875, Wake Forest School of Medicine, Claude D. Pepper Older Americans Independence Center (P30 AG21332), and the General Clinical Research Center of Wake Forest University (M01 RR07122). The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Xin Feng, MD, PhD, Assistant Professor, Department of Otolaryngology, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC xfeng@ wakehealth.edu DOI: /lary Normal swallowing and airway protection result from complex interactions among oropharyngeal muscles and bones. Closure of the larynx is the result of glottal closure, laryngeal vestibule closure, and descent of the epiglottis Superior and anterior displacement of the hyoid bone by contraction of the tongue base and suprahyoid muscles results in closure of the epiglottis and opening of the upper esophageal sphincter. 11,12 Reduced excursion of the hyoid and laryngeal movement contributes to aspiration risk and pharyngeal residues in dysphagia. 13,14 Precise timing of hyoid elevation is important for laryngeal closure relative to bolus flow through the hypopharynx 14 ; pharyngeal clearing is very important for safe and efficient swallowing. It has been previously reported that anterior and vertical hyoid excursions were reduced in older males versus younger males, 15 but no differences were found between younger and older females. 16 This implies that females may better compensate for age-related changes in order to preserve airway protection. However, no epidemiological studies have investigated gender differences in swallowing disorders in older adults. The hyoid bone is distantly connected to the mandible by suprahyoid muscles that play an important role in hyoid bone elevation during swallowing. Among these muscles, geniohyoid has the most potential to displace the hyoid in the anterior direction; and the mylohyoid has the most potential to displace the hyoid in the E231
2 superior direction. 17 Our previous study found that geniohyoid muscle atrophy associated with aging may increase risk of aspiration in the older adults. 18 Agerelated loss of muscle mass and strength could contribute to the change of relative position of the hyoid bone from the mandible. Conversely, the position of the hyoid bone changes may further impair muscle function and exacerbate the extent of hyoid excursion as it is supposed to be. We hypothesize that the age-related changes in the relative position of the hyoid bone from the mandible may contribute to or exacerbate swallowing problems in older adults. The face undergoes many morphologic changes with age, including changes in bone structure and muscles. 19,20 In addition, facial skeleton remodeling affects the position of overlying soft tissues. 21 Thepositionofmandibleboneis another key component of swallowing safety during oral preparation of the bolus and swallowing. 22 In addition, there is evidence that mandibular length and height decrease and mandibular angle increase with age in males and females. 19,20 These changes in mandibular bone may affect the attached soft tissues, such as the suprahyoid muscles and the ligaments that connect to the hyoid, altering their positions. Given the changes in facial skeletal structure with age and their potential effects on swallowing and airway protection, we sought to compare changes in positions between the mandibleandthehyoidinolder and younger adults. We also examined the relationships between structural changes and aspiration status, as determined by flexible endoscopic evaluation of swallowing (FEES). We utilized CT scans and results of FEES to test the hypotheses that 1) facial skeletal changes associated with aging affect the relative position of the hyoid bone; and 2) among older adults, aspirators have more noteworthy changes in hyoid bone position than do nonaspirators. MATERIALS AND METHODS We retrospectively reviewed head and neck computed tomography (CT) scans of 80 adults, comprised of 40 older (65 80 years old) and 40 young adults (20 40 years old), performed at Wake Forest Baptist Medical Center between 2006 and The 40 healthy older adults (mean age 5 78 yrs) consisted of 20 aspirators and 20 nonaspirators identified from a previous study of 73 older adults. 23,24 Aspiration status was determined by FEES. In brief, the participants were instructed to swallow liquid boluses of four different volumes (5, 10, 15, and 20 ml). Prior to bolus administration, participants were given instructions. Once handed a cup, they were to drink all of the liquid in one swallow when ready; however, they could take more than one swallow if needed. The endoscope was moved throughout the study between two different positions (swallowing position and postswallow position) for review of swallows in real time, slow motion, and frame by frame. If a participant aspirated (liquid material passed below the vocal folds into the trachea with or without a cough reflex) on a minimum of one swallow, then the participant was categorized as an aspirator. FEES is a wellaccepted tool to assess swallowing function both clinically and in research. Compared to videofluoroscopic swallowing evaluation (VFSE), FEES is better able to identify functional bolus flow parameters and delays in pharyngeal response, penetration, aspiration, and residue For the 40 younger adults (mean age 5 32 yrs), we searched electronic medical records at our institution. All younger participants had: 1) no history of head and neck cancer (or other cancer); 2) no known neurological or muscular diseases; 3) no known swallowing, speech, or respiratory diseases; 4) no prior orofacial implant surgery or other head/neck surgery; and 5) no prior facial skeletal fracture. The protocol was approved by the Wake Forest University Health Sciences Institutional Review Board. Demographics Age, gender, race, and aspiration status (older adults) were collected. Results are shown in Table I. Image Analysis For the healthy older adults, noncontrast head and neck CT scan parameters were set at 120 KV, 280 ma, 0.8 sec helical rotation time, 1.25-mm slice thickness, 6.25 speed, pitch, small focal spot, and 18-cm display field view (GE Lightspeed Pro 16, General Electric, Chalfont St.Giles, UK). CT scans were taken while the subjects were in the supine position, with the head fixed in a padded head cradle and chin slightly toward the ceiling. Participants were instructed not to swallow or to have any other oral movement during the CT scans. There was no standardization of scan protocol for the younger adults because they were scanned as part of a medical workup. However, these patients heads would have been similarly positioned as part of the usual protocol for head and neck CT scans at our imaging center. The scans were imported into a GE workstation and 2- dimensional images were reformatted and constructed in the sagittal plane. Scans were also imported into a TeraRecon workstation where 3-dimensional reformatting was performed. TABLE I. Demographic Data of the Participants. Young Adults Old Adults (n 5 40) (n 5 40) Male Female Male Female Number of participants Age (years) Number of aspirators N/A N/A 15 5 Race Caucasian African American Hispanic N/A 3 N/A N/A E232
3 The hyoid bone to mandibular plane distance (H-MP) was obtained from 3-dimensional reconstruction (Fig. 1A). Hyoid bone to retrognathion distance (H-RGN) was obtained from the sagittal plane of the 2-dimensional reconstructions (Fig. 1B). All measurements were made using the measurement tool in the respective software programs, and measurements were recorded in millimeters to 2 decimal places. When analyzing the relationships between the craniofacial parameters and the body height, all bone measurements were adjusted by height to control for a potential confounding factor. 29 The images were reviewed by two raters: a radiologist and an otolaryngologist. The two raters were blinded to age group and aspiration status for all of the measurements. Each rater performed all the measurements twice separately by 7 days. Inter- and intrarater reliabilities were analyzed using the interclass correlation coefficient (ICC). ICC of all the measures for interrater were 0.86 to 0.90 (P < 0.001) and for intrarater were 0.95 to 0.97 (P < 0.001) suggesting high inter- and intrarater reliabilities. Values for each measurement from two investigators were averaged and calculated for statistical analysis. Statistical Analysis Statistical analysis was performed using SPSS 10.0 statistical software (IBM, Armonk, NY). Data are reported as the mean 6 standard deviation. Multivariate general linear models were used to assess the differences in bone measurements as a function of age, gender, and aspiration status. Linear regression was used to analyze the relationships between H-MP and H-RGN. A one-way analysis of variance (ANOVA) was conducted to compare H-MP and H-RGN between categories of age (Young/Old), gender (Female/Male), and aspiration (No/Yes). All significance tests were two-tailed and P < 0.05 was considered significant. Fig. 1. Representative constructions of CT scans used for bone measurements. (A) Three-dimensional bone reconstructions of CT scans. H-MP indicates the shortest distance between the hyoid bone (H) and the mandible plane. (B) Sagittal plane of 2- dimensional CT scans. H-Rgn indicates the distance between the hyoid bone and Rgn. CT 5computed tomography; MP 5 inferior border of the mandible bone; Rgn 5 retrognathion. RESULTS Bone measurements adjusted by height as a function of age, gender, and aspiration status are summarized in Table II. There were significant differences in the H-MP and H-Rgn as a function of gender (P < 0.05). H- MP was positively correlated with H-Rgn (r , P < 0.001, Fig. 2). Table III provides bone measurements in young and old adults. TABLE II. Adjusted Means of Bone Measurements as a Function of Age, Gender, and Aspiration Status.* H-MP (mm) H-Rgn (mm) Age Young Old One-way ANOVA tests F(1,74) , P F(1,76) , P Gender Female Male One-way ANOVA tests F(1,74) , P F(1,76) , P Aspiration status in older adults No Yes One-way ANOVA tests F(1,37) , P F(1,38) , P *Adjusted by height. H-MP 5 distance between the hyoid bone (H) and the mandibular plane (MP); H-Rgn 5 distance between the hyoid bone (H) and retrognathion (Rgn). E233
4 age-related position changes between mandible and hyoid relative to aspiration status in older adults. Our main findings were: 1) the distance between hyoid and mandible bone was larger in the older males compared to the younger males; 2) Among the older males, aspirators had shorter distance for the H-MP and similar H-Rgn measurements compared to nonaspirators, suggesting a larger posterior distance of hyoid relative to the mandible bone; and 3) Males showed significant changes in hyoid bone position during normal aging compared to females. Fig. 2. Correlations between H-MP and H-Rgn. Black dots indicate individual data points. Dashed lines represent best fit by linear regression analysis with 95% confidence intervals over all subjects. R represents the Pearson correlation coefficient with the corresponding P value. H-MP 5 distance between the hyoid bone (H) and the mandibular plane (MP); Rgn 5 retrognathion. Effects of Age on the Relative Position Between the Hyoid and Mandible A significant increase in H-MP and H-Rgn associated with aging was found in males (P < 0.05). Older males had significantly greater H-MP and H-Rgn than the older females (P < 0.05). Table IV provides bone measurements in the older adult aspirators versus nonaspirators. Effects of Aspiration Status on the Relative Position Between the Hyoid and Mandible Male nonaspirators had longer H-MP and H-Rgn than female nonaspirators (P < 0.05). Male aspirators had shorter H-MP compared to the male nonaspirators (P < 0.05). DISCUSSION The current pilot study investigated: 1) changes in hyoid-mandible bone position in normal aging, and 2) Position Changes in Hyoid Bone and Aspiration Status Contrary to our hypothesis, we observed shorter distances between the hyoid bone and the mandibular plane in older male aspirators, while distances between the hyoid and retrognathion were maintained between aspirators and nonaspirators. To maintain H-RGN distance, the hyoid has to be positioned more posteriorly in the aspirators if the hyoid bone stays closer to the mandibular plane. This will increase the vertical distance between the hyoid and the chin, which may interrupt the normal hyoid bone motion anteriorly during swallowing in aspirators. Hyoid bone excursion during swallowing is a complex interaction of musculoskeletal structure. It may depend not only on the hyoid bone position but also the output of related musculature contraction. Based on the structural properties of the suprahyoid muscles, the geniohyoid and mylohyoid muscles have the most potential to displace the hyoid in the anterior and superior directions, respectively. 17 In this study, we did not evaluate the excursion distance in the anterior, and superior directions was reduced in aspirators compared to nonaspirators, although a decrease in the range of hyoid motion and in velocity of hyoid movement occurs in older adults compared to younger adults. 15,30 Atrophy of the geniohyoid muscle was correlated with aspiration status in older adults. 31 Our previous studies found that decreased pharyngeal strength and TABLE III. Adjusted Bone Measurements in Younger and Older Adults.* Age Young Old n Mean 6 SD n Mean 6 SD One-Way ANOVA Tests H-MP (mm) Female F(1,30) , p Male F(1,42) , P One-way ANOVA tests F(1,35) , P F(1,37) , P H-Rgn (mm) Female F (1,33) , P Male F(1,41) , P One-way ANOVA tests F(1,36) , P F(1,38) , P p p *Adjusted by height. H-MP 5 distance between the hyoid bone (H) and the mandibular plane (MP); H-Rgn 5 distance between the hyoid bone (H) and retrognathion (Rgn). E234
5 TABLE IV. Adjusted Bone Measurements in Older Adults.* Aspiration No n Mean6 SD n Mean 6 SD Yes One-Way ANOVA Tests H-MP (mm) Female F(1,13) , P Male F(1,22) , P One-way ANOVA tests F(1,17) , P F(1,18) , P H-Rgn (mm) Female F(1,14) , P Male F(1,22) , P One-way ANOVA tests F(1,18) , P F(1,18) , P *Adjusted by height. H-MP 5 distance between the hyoid bone (H) and the mandibular plane (MP); H-Rgn 5 distance between the hyoid bone (H) and retrognathion (Rgn). decreased posterior tongue strength are associated with aspiration status in healthy older adults, 24,32 which suggests that age-related sarcopenia of swallowing muscles plays an important role in swallowing disorders. 33 In addition, incomplete pharyngeal constriction increases pharyngeal residue, and thus the chance for unsafe swallowing. Pharyngeal constriction in the elderly could be reduced by enlarged pharyngeal space, foreshortening by laryngeal elevation, and lower position of larynx associated with aging. 34,35 The etiology of the swallowing deficits in aging is multifactorial. Thus, age-related loss in suprahyoid muscle mass, strength, ligament plasticity, and relative positional changes of hyoid bone could interrupt hyoid bone movement during swallowing, which may be associated with (or contribute to) aspiration in older adults. A series of studies from Kendall and Leonard 34,35 using videofluoroscopic measures have shown that poor pharyngeal constriction, suggestive of pharyngeal weakness, contributed to 75% of the cases of aspiration in the elderly. In addition, the pharyngeal constriction ratio was associated with the presence of aspiration on fluoroscopy. 36 Elderly subjects did not elevate the larynx to the same extent, or clear the pharynx, as well as the younger control subjects, suggesting a lower position of the larynx; and pharyngeal expansion increased the risk of swallowing dysfunction in the older adults. We hypothesize that the anatomical findings in the hyoid bone position associated with aging in the current study could be correlated with the functional changes in pharyngeal constriction and hyolaryngeal excursion in older adults. Thus, a functional test of hyoid bone displacement and pharyngeal function in these participants using a dynamic imaging technique will be done in further studies to support or refute this hypothesis. Gender and Age Differences Older adults had a bigger distance between the hyoid and mandible compared to younger adults, but only in males. Gender differences in hyoid and mandible distance were only found in older adults, that is, older males had larger distance than older females. This finding suggests that (a) males had bigger differences in hyoid bone position relative to mandible between younger and older adults, and (b) hyoid bone position was lower in older males compared to older females. Movement of the hyoid bone is known as one of the leading processes at the onset of the swallow. Its upward displacement is related to the bolus position in the oral cavity; its forward displacement is related to pharyngeal processes that induce a thickening and rotation of the epiglottis to close the laryngeal vestibule and opening of the upper esophageal sphincter. 37,38 Craniofacial morphology affects anterior hyoid excursion. 39 Previous studies have noted changes in hyoid bone excursion in males associated with aging. 15,16 In the current study, we found that the distance between the hyoid bone and the mandibular plane and retrognathion increased only in older males; in other words, the hyoid bone moved farther away from the mandible in the older males compared to younger males or older women. This finding suggests that a compensatory effort may be required in older males to achieve enough hyoid bone movement upward and forward to completely protect the airway during swallowing. However, previous studies found that during aging, normal males lose more range of motion in oropharyngeal muscles than do females, 15,16 implying that males may have a defective compensatory mechanism associated with aging. Together with more severe changes of the skeletal anatomy in the males, such as the changes in hyoid bone position, these aging-related skeletal changes may predispose older males to aspiration and swallowing disorders. The 20 aspirators in this study (15 males and 5 females) were identified from a previously studied cohort of 73 adults, 23,24 which suggested that males were more likely to be aspirators than females. In addition, the CT E235
6 scans were taken in the supine position during testing in the current study, which introduced gravity as a confounder. Further studies with larger cohorts are needed to compare gender differences and body positions/head and neck postures in the prevalence of aspiration/swallowing deficits in older adults and also to control the possible confounds from age and gender. A limitation of this study is the lack of information on aspiration status from the younger participants. An earlier study assessing age effects on aspiration in healthy adults found that older adults were more likely to demonstrate aspiration on liquids whereas the younger adults were not. 40 Nevertheless, future studies in larger cohorts that include aspiration status in both age groups may elucidate the relationships among age-associated morphologic changes in the facial skeleton, positional changes in the hyoid bone, and aspiration status. CONCLUSION The facial skeleton undergoes many changes with age that may alter the hyoid bone position. In the current study, among older male aspirators, the hyoid bone was in a more posterior and lower position relative to the mandible compared to nonaspirators. These findings suggest that facial skeletal changes may be a component of decreased swallowing safety and aspiration in older adults and warrant further investigation. Acknowledgement The authors thank Caresse Hightower and Chris O Rourke (Department of Radiology) for their assistance with CT acquisition and imaging analysis; Greg Russell (Department of Biostatistics) for his help with the data analysis; and Karen Potvin Klein, MA, ELS (Translational Science Institute, Wake Forest School of Medicine), for her editorial contributions to this article. BIBLIOGRAPHY 1. Rofes L, Arreola V, Romea M, et al. Pathophysiology of oropharyngeal dysphagia in the frail elderly. Neurogastroent Motil 2010;22:851 E Hammond CAS, Goldstein LB. 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