Hyoid Bone Position in Patients with and without Temporomandibular Joint Osteoarthrosis: A Cone-Beam Computed Tomography and Cephalometric Analysis

Objective To assess the differences in hyoid bone position in patients with and without temporomandibular joint osteoarthrosis (TMJOA). Methods The present cross-sectional study was conducted in 427 participants whose osseous status was evaluated using cone-beam computed tomography and classified into normal, indeterminate osteoarthrosis (OA), and OA. The hyoid bone position and craniofacial characteristics were evaluated using cephalograms. Patients were divided into the normal group (N = 89), indeterminate OA group (N = 182), and OA group (N = 156). Descriptive statistics, one-way analysis of variance, and age- and sex-based stratified analyses were performed. P < 0.05 was considered statistically significant. Results The differences in Hy to MP, Hy-RGn, Hy to C3-RGn, C3-RGn, and Go-Hy-Me among the three groups were statistically significant. The differences in the Frankfort-mandibular plane angle, saddle angle, articular angle, gonial angle, ramus height, and posterior facial height were statistically significant. After adjusting age and sex, the Hy-RGn and C3-RGn in the normal group were significantly greater than the OA group. No statistical differences were observed in the hyoid measurements in the stratified analyses in males or subjects less than 18 years old. The differences in Hy to MP, Hy to C3-RGn, and Go-Hy-Me in female patients among the three groups were statistically significant. The differences in Hy to SN, Hy to FH, Hy to PP, Hy to MP, Hy-RGn, Hy-C3, Hy to C3-RGn, Go-Hy-Me, Hy-S, and C3-Hy-S in adults were statistically significant. Conclusion The differences in the hyoid bone position, mainly relative to the mandible, were statistically significant in patients with or without TMJOA. The difference pattern varied among different age and sex groups. Clinical evaluation of the hyoid position must consider the age and sex of patients. Longitudinal studies are required to clarify the causal relationship between TMJOA and hyoid bone position.


Introduction
Temporomandibular joint osteoarthrosis (TMJOA), a vital subtype of temporomandibular disorders (TMDs), is a degenerative joint disease characterized by cartilage degradation and subchondral remodeling [1,2]. Around 27-38% of the general population had TMD [3]. And 11% of the TMD patients have symptoms of osteoarthritis [4]. As a primary chief complaint of TMJOA patients, pain and TMJ dysfunction could compromise the quality of life of patients, causing a considerable social and economic burden [5,6].
Several studies reported the relation between TMJOA and craniofacial morphology [10,11]. Patients with TMJOA exhibited the retrusion and clockwise rotation of the mandible [12]. Although no study reported the relationship between hyoid bone position and TMJOA, a few studies investigated the relationship between hyoid bone position and TMD [13][14][15]. However, the results of these studies were inconsistent. erefore, the present cross-sectional study attempted to analyze the differences in hyoid bone position in patients with or without TMJOA, which might help understand the etiology of TMJOA and the management of TMJOA pain.

Study Population.
e present cross-sectional study was conducted on 427 patients visiting the orthodontic department of our hospital between 1 January 2020 and 31 July 2021 after institutional ethics clearance. Written informed consent was obtained from all patients or legal guardians. e personal information of all participants was anonymized. Patients with permanent dentition with clear cephalogram and cone-beam computed tomography (CBCT) images at the first visit to our hospital and with the similar osseous status of the left and right joints were included in the study. Patients with tumor or maxillofacial deformity that could cause joint deformity; those with breathing or swallowing disorders; patients with a history of orthodontic treatment, plastic surgery, or other craniofacial surgeries; those with systematic diseases affecting the orofacial regions; and those with a history of TMJ treatment were excluded from the study.

CBCT Evaluation.
CBCT was used to evaluate condylar osseous conditions. CBCT scans were performed with a 256slice CT scanner (J Morita Mfg. Corp., Kyoto, Japan) using the following parameters: tube voltage, 90 kVp; tube current, 5 mA; exposure time, 17.5 s; voxel size, 0.25 m; slice thickness, 0.25 mm; and field of view, 140 × 100 mm 2 . e condylar images were categorized into the following three groups based on the classification of the osseous diagnosis for TMJ [10,16]: e normal size of the condyle, no deformation, subcortical sclerosis, or articular surface flattening.

Indeterminate for Osteoarthrosis (OA).
e normal size of the condyle with subcortical sclerosis or articular surface flattening; no condylar deformation; and condylar hypoplasia with normal condylar morphology but decreased size in all dimensions.

OA.
Deformation caused by erosion, osteophyte, subcortical cyst, or generalized sclerosis and short condyles with decreased condylar height but continual cortical bone. e osseous diagnosis was made by two independent assessors. Any disagreement about the classification was evaluated decisively by a third specialist.

Cephalometrics.
All cephalograms were performed as per the standardized technique with natural head position and teeth in centric occlusion. e patients were instructed not to swallow when taking the cephalograms. e digital cephalograms obtained were traced using Uceph software (version 961, Chengdu, China). An experienced orthodontist, blinded to the diagnoses of the patients, performed the cephalogram tracing. e Frankfort horizontal plane was considered the reference plane, and 13 hyoid-related and 18 craniofacial measurements were performed ( Figure 1; Table 1) [15,17]. e intra-and inter-rater reliability of cephalometric tracing was tested, and the intra-class correlation coefficients were >0.8 [17,18].

Statistical Analysis.
Descriptive statistics were presented as mean ± standard deviation. All statistical analyses were performed with the R package (http://www.R-project.org, e R Foundation) and Empowerstats (http:// www.empowerstats.com, X&Y Solutions, Inc., Boston, MA). An α level of 0.05 was considered statistically significant. e differences in the cephalometric measurements among the groups were evaluated through a one-way analysis of variance (ANOVA) when equal variances were assumed. P > 0.05 was considered statistically significant. After the ANOVA test, multiple comparisons between the groups were confirmed by using the S-N-K method. Separate stratified analyses were performed based on sex and age (<18 years vs. ≥18 years).

Overall Analysis.
Of the 427 subjects included in this study, 89 were classified into the normal group, 182 in the indeterminate group, and 156 in the OA group. Subjects in the indeterminate groups were statistically older than the other two groups (P < 0.001). e normal group exhibited a higher proportion of males than the other two groups (P � 0.016; Table 2). e differences in five hyoid measurements, namely, Hy to MP, Hy-RGn, Hy to C3-RGn, C3-RGn, and Go-Hy-Me, were statistically significant. e differences in craniofacial measurements, namely, Frankfort-mandibular plane angle (FMA), saddle angle, articular angle, gonial angle, ramus height, and posterior facial height among the three groups, were statistically significant (Table 3).
After adjusting age and sex using the generalized additive model, the Hy-RGn and C3-RGn in the normal group were significantly greater than those in the OA group. e differences in ANB, FMA, saddle angle, articular angle, gonial angle, ramus height, posterior facial height, and overbite among the three groups were statistically significant ( Table 4).

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Pain Research and Management

Stratified Analysis Based on Sex.
e female patients in the indeterminate OA group were older than those in the other two groups. e differences in Hy to MP, Hy to C3-RGn, and Go-Hy-Me among the three groups were statistically significant. e differences in FMA, FH-OP, gonial angle, ramus height, posterior cranial base length, and anterior and posterior facial height among the three groups were statistically significant (Table 5). e male patients in the indeterminate OA group were older than those in the other two groups. No statistical differences were observed in hyoid measurements among the three groups. e differences in FMA, saddle, articular, and interincisal angles among the three groups were statistically significant ( Table 6).

Stratified Analysis Based on Age.
Patients <18 years of age in the normal group exhibited a greater proportion of males than the other two groups (P � 0.016). No statistical differences were observed in hyoid measurements. e differences in saddle angle, articular angle, ramus height, posterior cranial base length, posterior facial height, and SNB angle among the three groups were statistically significant (Table 7).
Adults in the indeterminate OA group were significantly older than those in the normal group (P < 0.05). e differences in Hy to SN, Hy to FH, Hy to PP, Hy to MP, Hy-RGn, Hy-C3, Hy to C3-RGn, Go-Hy-Me, Hy-S, and C3-Hy-S were statistically significant. e Hy-C3 in the indeterminate group was smaller than that in the normal group. e Go-Hy-Me angle in the indeterminate OA group was greater than that in the other two groups. e differences in the saddle angle, articular angle, ramus height, posterior cranial base length, posterior facial height, and SNB angle were statistically significant. Additionally, the differences among the three groups were statistically significant in ANB, FMA, FH-OP, articular angle, gonial angle, ramus height, and posterior facial height (Table 8).

Discussion
e present study investigated the hyoid position in patients with or without TMJOA using cephalograms and CBCT. e patients with condylar flattening or subcortical sclerosis were diagnosed with indeterminate OA as these radiological signs were a physiological phenomenon. e patients with indeterminate OA were attempted to be distinguished from those with OA or completely normal condyles. Additionally, patients with inconsistent bilateral osseous status were excluded to prevent cephalometric errors. e differences in hyoid position and Hy to MP and Hy-RGn after adjusting age and sex between the three groups were statistically significant.
Although no study reported the relationship between hyoid bone position and TMJOA, a few studies investigated the relationship between hyoid bone position and TMD. A magnetic resonance imaging study observed that disc displacement was not related to hyoid bone position [14].  Ar-Go, the distance between articulare and gonion. Mandibular body length (mm) Go-Me, the distance between gonion and menton.
Anterior cranial base length (mm) S-N, the distance between sella and nasion.
Posterior cranial base length (mm) S-Ar, the distance between sella and articulare.
Anterior facial height (mm) N-Me, the distance between nasion and menton. Posterior facial height (mm) S-Go, the distance between sella and gonion. Overjet (mm) e horizontal distance between the upper and lower incisal edge with reference to the occlusal plane. Overbite (mm) e vertical overlap between the upper and lower incisal edge. Câmara-Souza et al. observed no relationship between TMD and hyoid bone position in 80 dental students [19]. Ekici and Camci reported that the hyoid bone in patients with TMD was located closer to the cranium [15]. e inconsistencies in the findings of these studies may be probably due to inconsistent diagnostic criteria, heterogeneity in sample selection, and methodological differences. Although the relationship between hyoid bone position and TMD is debated, the abnormality of the hyoid bone is often related to cervical painful symptomatology that could be claimed by TMD patients [20,21]. Nathan et al. detected a release of the hyoid bone away from the floor of the mouth in patients resolved of myofascial pain [22]. ese not only support that these structures are anatomically and functionally related  Pain Research and Management but also imply that the position of hyoid bone might be an indicator or a contributing factor of painful TMJOA. A larger proportion of patients in the OA and indeterminate OA group were female. is finding is concurrent with that of other studies [18,23]. e patients in the indeterminate OA group were older than the other two groups, with a higher percentage of adults, indicating an age-related change in the condyles [24]. is change could be a normal physiological change [25], resulting from condylar remodeling after mild inflammation or a transition stage to OA [26]. In the OA group, 37.82% were aged less than 18 years, indicating that TMJOA can occur early. Studies have reported the mean age of TMJOA patients as 34 years. is finding is in contrast with that of the present study, where patients with OA were younger. is may be because the patients included in the present study were those undergoing preorthodontic examinations, which consists of most adolescents and young adults.
us, another population in which TMJOA occurs, namely, the climacteric women aged 40-55 years, was not included. e present study observed that patients with OA exhibited the largest ANB angle, gonial angle, smaller ramus height, and posterior facial height. e differences in the cephalometric persisted even after adjusting for sex and age, suggesting that patients with OA exhibit clockwise-rotated mandibles with low posterior facial height. is finding is concurrent with that of other studies [10,27,28]. Stratified analysis exhibited that ramus height and posterior facial height deficiency were more significant in females, whereas no significant differences were observed in males among the three groups.
is may be related to the fluctuations in estrogen. Estrogen has multiple effects on TMJ, such as stimulating bone formation and inhibiting bone resorption [29]. Estrogen levels in women may fluctuate during puberty and near menopause, affecting the stability of the intraarticular environment [30]. On the other hand, androgens are a protective factor in TMD, inhibiting the inflammatory response and reducing pain. Overall, the craniofacial characteristics of the present study population were generally consistent with those of other studies, allowing the generalization of our results.
Ekici and Camci investigated 113 adults, with 55 patients with TMD and 58 healthy volunteers. ey observed that adult patients with TMD exhibited hyoid bones closer to the cranium and larger Go-Hy-Me angle [31]. In the present study, adult patients with TMJOA      [31]. e hyoid bone was closer to the third cervical vertebrae in the indeterminate OA group than normal. However, no difference was observed between the OA and the normal group. e distance between the hyoid bone and third cervical vertebrae was related to the upper airway space [9]. Our results revealed that the relative position of the hyoid bone to the third cervical vertebra in patients with indeterminate OA might be more unique. Further studies are required to clarify the characteristics of the hyoid bone position in patients with indeterminate OA.
In the present study, the differences in more parameters among adults and females were statistically significant than between adolescents and males. Adolescents still have growth potential. erefore, adolescents have more variability in their cephalometric parameters, which may account for the inability to derive statistical differences. For males, indicators such as Hy-RGn did not yield statistical differences due to the relatively small sample size. Further studies with a larger sample size for males may better evaluate the differences in some hyoid indicators. Different patterns of differences in hyoid bone position in different sexes and age groups may be observed. us, future studies subdividing the populations are required. In clinical practice, when evaluating the hyoid position, the age and sex of the patient should be considered to obtain an accurate diagnosis.
e main limitation of this study is its cross-sectional design. erefore, no causal relationship can be built between the hyoid position and OA. Future longitudinal studies are necessary to clarify the causal relationship. Additionally, the hyoid bone and cranium measurements were two-dimensional, and three-dimensional measurements could be used to explore the relationship between the bilateral TMJ and the position and size of the hyoid bone [32].

Conclusion
Hyoid bone position, mainly relative to the mandible, differs in patients with or without TMJOA. e pattern of differences varies in different age and sex groups. Clinicians should be aware that the patients might have with abnormal position. Clinical evaluation of the hyoid position might be required to consider the age and sex of the patients.
Longitudinal studies are required to clarify the causal relationship between TMJOA and hyoid bone position.

Data Availability
e data used to support the findings of this study are available from the corresponding author upon reasonable request.

Conflicts of Interest
e authors declare that they have no conflicts of interest.

Authors' Contributions
Xueman Zhou and Xin Xiong contributed equally to this work. Xueman Zhou and Xin Xiong are co-first authors.