Dysphagia

, Volume 28, Issue 3, pp 435–445 | Cite as

Analysis of Hyoid Bone Using 3D Geometric Morphometrics: An Anatomical Study and Discussion of Potential Clinical Implications

  • Nicolas Fakhry
  • Laurent Puymerail
  • Justin Michel
  • Laure Santini
  • Catherine Lebreton-Chakour
  • Danielle Robert
  • Antoine Giovanni
  • Pascal Adalian
  • Patrick Dessi
Original Article

Abstract

The aim of this study was to obtain a quantitative anatomical description of the hyoid bone using modern 3D reconstruction tools and to discuss potential applications of the knowledge in clinical practice. The study was conducted on 88 intact hyoid bones taken from cadavers during forensic autopsies (group 1) and on 92 bones from CT scan images of living adult subjects (group 2). Three-dimensional reconstructions were created from CT scan images using Amira 5.3.3® software. An anatomical and anthropological study of hyoid bones was carried out using metric and morphological analyses. Groups 1 and 2 were compared to evaluate the influence of muscle traction on hyoid bone shape. Characteristics of the hyoid bone were highly heterogeneous and were closely linked with the sex, height, and weight of the individuals. Length and width were significantly greater in men than in women (39.08 vs. 32.50 mm, p = 0.033 and 42.29 vs. 38.61 mm, p = 0.003), whereas the angle between the greater horns was larger in females (44.09 vs. 38.78, p = 0.007). There was a significant positive correlation between the height (Pearson coefficient correlation r = 0.533, p = 0.01) and weight (r = 0.497, p = 0.01) of subjects and the length of the hyoid bone. Significant metric differences were shown between group 1 and group 2. This very reproducible methodology is important because it may lead to clinical studies in, e.g., head and neck cancer or sleep apnea. Such studies are ongoing in our research program.

Keywords

Deglutition Deglutition disorders Dimorphism Sleep apnea Head and neck Cancer 

Introduction

The hyoid bone is the only bone in the body that is not articulated with other skeletal bones. It consists of five parts: a body and two greater and two lesser horns (Fig. 1). The ends of the greater horns are attached by ligaments to the thyroid cartilage of the larynx, while the lesser horns are attached to the temporal styloid process. The hyoid is “free-floating” in primates, but not in other mammals, particularly some (e.g., rodents) that are commonly used as animal models [1, 2, 3]. Almost the entire surface a large number of muscles attached to it that move and support the tongue, larynx, and pharynx. This relationship with the major skeletal system appears to be an essential element that determines the morphology of the bone and probably its hardness, depending on specific functional demands. Many studies have reported descriptions of the hyoid bone as a “U,” “V,” “horseshoe,” or an asymmetrical shape based on visual observation [4, 5, 6].
Fig. 1

Parts of the hyoid bone in superior (a), anterior (b) and lateral (c) views: greater horn (1), lesser horn (2), body (3)

However, visual analysis does not appear to be reproducible and therefore cannot be used in practice [7].

In recent years, three-dimensional (3D) imaging systems have become widely available, leading to their use in research. A metric approach, with rigorous, repeatable, and reproducible methodology using 3D reconstruction obtained from computed tomography (CT) images, has been shown to be more objective than a morphological description of the bone by visual analysis. The metric approach also reduces variability in different models [7]. CT also provides digital 3D data, a source of information for morphometric analysis.

Geometric morphometrics is the statistical analysis of form based on Cartesian landmark coordinates. After separating shape from overall size, position, and orientation of the landmark configurations, the resulting Procrustes shape coordinates can be used for statistical analysis. Results of statistical techniques that preserve these convenient properties (such as principal component analysis (PCA), multivariate regression, or partial least-squares analysis) can be visualized as actual shapes or shape deformations. The powerful visualization tools of geometric morphometrics and the typically large amount of shape variables give rise to a specific exploratory style of analysis, allowing the identification and quantification of previously unknown shape features [8, 9].

Geometric morphometric methods have been widely applied in primatology, human variation, and paleoanthropology [10, 11, 12, 13]. In traditional multivariate morphometrics, the form of a biological object is typically recorded as a set of measurements of distances and angles. However, geometric morphometrics links the set of measurements with the shape of the object. The form of the object is recorded as the coordinates of defining features (landmarks), and its geometry is thus preserved. Geometric morphometrics also distinguishes the form of an object (shape plus size) from the shape (form with scale removed) by scaling to unit size, so that it would be possible to model morphological variations without taking into consideration the size factor [14, 15, 16]. In addition, studying the morphology of different forms by superimposition removes the need for a common reference plane. Multivariate analysis, such as principal component analysis (PCA), can then be carried out to investigate the main shape variations.

By analyzing a large sample of hyoid bones, this study aimed (1) to obtain a quantitative anatomical description with metric and morphological analysis using modern 3D reconstruction tools (metric analysis and geometric morphometrics) on a sample of hyoid bones harvested from cadavers, (2) to evaluate the effect of muscle insertions on hyoid bone shape by comparing the sample of hyoid bones harvested from cadavers with a sample of hyoid bone CT images obtained from living subjects (i.e., in vivo conditions), and (3) to discuss the potential applications of the knowledge obtained in forensic science and clinical practice (e.g., head and neck cancer treatment or sleep apnea).

Materials and Methods

Materials

The study was conducted on 180 intact hyoid bones. Eighty-eight were taken from cadavers during forensic autopsies (group 1) and there were 92 anonymized computerized CT scan images of hyoid bones of living adult subjects (group 2). The main characteristics of the study population are summarized in Table 1.
Table 1

Descriptive statistics of the study population

Variables

n

Mean

SD

Min

Median

Max

Age

180

51.37

20.41

18

53

97

Weight (kg)

88

70.57

19.12

30

70

121

Height (cm)

88

169.48

11.28

149

172

190

BMI

88

24.24

5.20

12.98

23.58

41.86

Length B (mm)

180

36.38

4.88

22.31

36.18

51.22

Width A (mm)

180

40.78

7.08

23

39.90

58.12

Width C (mm)

180

20.91

3.04

13.52

20.92

30.22

Angle α

180

40.97

13.02

11.6

40.84

66.77

Group 1 (Hyoid Bones from Cadavers)

Eighty-eight hyoid bones were taken from cadavers during forensic autopsies. Most autopsies were performed 24–48 h after death, while some were performed up to 8 days after death. We excluded juveniles from this study because their bones were still growing, corpses that were charred or in a state of putrefaction, and hyoid bones that had been damaged as a result of trauma. After autopsy, soft tissue was removed from the bones to facilitate identification of bony structures and the bones were fixed in 4 % formaldehyde solution. A CT scan was then carried out on each bone.

Group 2 (Hyoid Bones from Alive Subjects)

Ninety-two anonymized CT scan images of the neck performed in adult subjects were collected from the medical database of La Timone University Hospital (Marseille, France) between June 2010 and January 2011. Exclusion criteria were any pathology, trauma, or surgery that affected the anatomy or the neck area, and any presence of metal artifacts that could degrade the visual quality of CT images.

Methods

Imaging Procedures and Data Acquisition

Multislice spiral CT scans were obtained with a Siemens Somatom Definition (Siemens Healthcare) or a General Electric Light Speed LS 16 Pro (GE) using the following parameters: 120 kV, 130 mAs, slice = 0.3 mm every 0.6 mm. A 3D reconstruction was then created from scanned images using Amira 5.3.3® software (Visage Imaging Inc., San Diego, CA) on a Mac OS X computer (Mac OS X 10.6.6, processor 2 GHz Intel Core i7). The procedure was as follows: (1) Importation of CT scan images (DICOM formats) into Amira 5.3.3®, (2) segmentation process using the half maximum height protocol (ImageJ software version 1.44o) to determine the exact position of the boundaries of the structures, and (3) 3D hyoid bone surface creation.

Five landmarks were then chosen for their reproducibility and repeatability, as previously published by Pollard et al. [7], in order to measure anthropometric variables (Fig. 2). Two were positioned on the distal parts of the greater horns of the hyoid bone (one on each side of the hyoid bone, landmarks 1 and 5), two were positioned in the medial part of the junction of the greater and lesser horn (one on each side of the hyoid bone, landmarks 2 and 4), and one was positioned on the middle of the anterior part of the body (landmark 3). Each landmark had three Cartesian coordinates (x, y, and z).
Fig. 2

Position of landmarks on hyoid bone

Data Analysis

Metric and morphological analyses were done for the entire sample of hyoid bones. A complete anatomical and anthropological study was carried out on the group 1 hyoid bones (from cadavers), analyzing the relationship between sex, age, size, weight, body mass index (BMI), and hyoid bone anthropometric measurements. Groups 1 and 2 were then compared in order to validate the results with in vivo hyoid bones, i.e., to evaluate the influence of muscle traction on hyoid bone shape.

Metric Analysis

Twelve anthropometric variables were measured using the software (Fig. 3): Distance A (or width) is the distance between the distal parts of the greater horns of the hyoid bone. Distance B (or length) is the distance from the middle of the anterior part of the body to a hypothetical line connecting the distal parts of the greater horns. Distance C (width of the body) is the distance between the lesser horns. The other distances measured (D, E, F, G, H, I, J, K) are shown in Fig. 3. Finally, the angle α is the angle between the two greater horns.
Fig. 3

Anthropometric variables used for metric analysis

Statistical analysis was performed using IBM® SPSS® Statistics 18 software with a 5 % threshold of significance. Measurements of males and females (in the whole sample) and of group 1 and group 2 were compared using student’s t test. Levene’s test was used to assess the equality of variance.

Pearson’s correlation coefficient (r) was calculated to analyze the relationship between the anthropometric variables of the hyoid bone and the characteristics of the individuals (height, weight, and BMI).

A canonical discriminant analysis was used to establish prediction about determination of gender according to hyoid bone size using Wilks’ lambda distribution.

Morphological Analysis

MorphoJ software version 1.04a was used to analyze the 3D landmark coordinates [17]. The shape analysis was done by performing a generalized Procrustes analysis [18]. This procedure allowed visual and statistical assessment of shape after scaling to common centroid size. PCA of shape coordinates was used to examine overall shape variations in the sample and the distribution of each group in shape space [19]. Wireframe and polygon-rendered models were used to visualize variations in hyoid bone shape.

Statistical analysis was done using R2.14.1 software with a 5 % threshold of significance. Centroid size was compared between males and females and between group 1 and group 2 using student’s t test. We used MANOVA in order to test the dimorphism and difference between the two groups about the PCA scores on shape space. We also tested the allometry, i.e., the relationship between size and shape using ANOVA.

Results

Metric Analysis

Descriptive statistics of the study population are given in Table 1.

Relationship Between Sex and Hyoid Bone Dimensions

Student’s t test revealed a p value <0.05 for length, width between the greater horns, and width of the body, and angle of the hyoid bone, indicating a significant difference between men and women for these four variables (Tables 2, 3). The Pearson correlation coefficients shown in Table 4 confirm these results.
Table 2

Descriptive statistics of anthropometric measurements by sex

Sex

n

Variables

Mean

SD

Min

Median

Max

Men

106

Age

50.83

18.84

18

54

86

  

Length B

39.08

3.96

30.33

39.23

51.22

  

Width A

42.29

7.56

23.00

41.75

58.12

  

Width C

22.27

2.76

16.54

22.53

30.22

  

Angle α

38.78

13.93

11.6

38.52

64.09

Women

74

Age

52.11

22.54

18

51

97

  

Length B

32.50

3.15

22.31

32.59

41.24

  

Width A

38.61

5.69

24.57

38.55

51.99

  

Width C

18.95

2.25

13.52

18.82

24.47

  

Angle α

44.09

10.97

15.68

42.92

66.77

Table 3

Comparison of anthropometric measurements by sex

Variables

Men

Women

p

Age

50.83

52.11

0.079

Length B

39.08

32.50

0.001

Width A

42.29

38.61

0.001

Width C

22.27

18.95

0.001

Angle α

38.78

44.09

0.007

Student test; p < 0.05

Table 4

Correlation between anthropometric measurements and individual variables

Variables

n

 

Age

Weight

Height

BMI

Sex

Group

Length B

180

r

0.004

0.497

0.533

0.358

−0.665

−0.198

  

p

0.95

0.01

0.01

0.01

0.01

0.008

Width A

180

r

0.066

0.1

0.302

−0.21

−256

−0.119

  

p

0.38

0.36

0.006

0.85

0.01

0.11

Width C

180

r

0.197

0.13

0.351

0.014

−0.539

−0.26

  

p

0.009

0.24

0.001

0.9

0.01

0.01

Angle α

180

r

−0.004

−0.107

−0.21

−0.119

0.201

0.047

  

p

0.95

0.33

0.84

0.28

0.007

0.53

r = Pearson’s correlation coefficient; p < 0.05

Relationship Between Group and Hyoid Bone Dimensions

Student’s t test revealed a p value <0.05 for length and width of the body of the hyoid bone, indicating a significant difference between groups 1 and 2. In contrast, no significant difference (p > 0.05) was observed for width between the greater horns and for angle of the hyoid bone (Tables 5, 6). The Pearson correlation coefficients shown in Table 4 confirm these results.
Table 5

Descriptive statistics of anthropometric measures by group

Group

n

Variables

Mean

SD

Min

Median

Max

1 (cadavers)

88

Age

49.22

19.44

18

47.5

91

  

Length B

37.36

4.99

26.56

37.89

51.22

  

Width A

41.64

8.10

23.00

40.84

58.12

  

Width C

21.72

3.10

16.42

21.86

30.22

  

Angle α

40.34

14.88

11.6

39.91

64.07

2 (alive subjects)

92

Age

53.30

21.16

18

57

97

  

Length B

35.43

4.59

22.31

35.12

47.69

  

Width A

39.96

5.86

24.57

39.04

54.96

  

Width C

20.14

2.78

13.52

19.92

26.28

  

Angle α

41.57

11.03

15.68

41.35

66.77

Table 6

Comparison of anthropometric measurements by group

Variables

Group 1

Group 2

p

Age

49.22

53.30

0.187

Length B

37.36

35.43

0.08

Width A

41.64

39.96

0.113

Width C

21.72

20.14

0.001

Angle α

40.34

41.57

0.53

Student test; p < 0.05

Relationship Between Hyoid Bone Dimensions

There was a significant correlation between the angle and the length and between the angle and the width (A and C) of the hyoid bone (p < 0.05). The positivity of Pearson’s correlation coefficient (r) indicated that the angle of the hyoid bone increased with increasing width between the greater horns (r = 0.719, p < 0.01). The negativity of r indicated that the angle of the hyoid bone decreased with increasing length (r = −0.485, p < 0.01) and width of the body of the hyoid bone (r = −0.169, p = 0.023). A significant correlation between width A and width C (r = 0.412, p < 0.01) and between length B and width C (r = 0.54, p < 0.01) was also noted. Finally, the length B was not correlated with the width A (r = 0.125, p = 0.093) (Table 7).
Table 7

Relationship between hyoid bone dimensions

Variables

n

 

Length B

Width A

Width C

Angle α

Length B

180

r

0.125

0.540

−0.485

  

p

0.093

0.01

0.01

Width A

180

r

0.125

0.412

0.719

  

p

0.093

0.01

0.01

Width C

180

r

0.540

0.412

−0.169

  

p

0.01

0.01

0.023

Angle α

180

r

−0.485

0.719

−0.169

  

p

0.01

0.01

0.023

r = Pearson’s correlation coefficient; p < 0.05

Relationship Between Weight and Height of an Individual and Hyoid Bone Dimensions

The relationships between weight and height and hyoid bone dimensions are given in Table 4. There was a significant correlation between the weight and height of subjects and the length of the hyoid bone (p < 0.05). The positivity of r indicated that the length of the hyoid bone increased with increasing weight and height. The significant association between BMI and length of the hyoid bone confirmed this correlation.

A significant correlation between height and width (distances A and C) of the hyoid bone (p < 0.05) was noted. The positivity of r showed that the width of the hyoid bone increased as the height of the subjects increased. Weight and BMI were not correlated with the width of the hyoid bone (p > 0.05).

Finally, the angle of the hyoid bone was not correlated with the morphology of individuals, and age was correlated only with the width of the body of the hyoid bone, with a positive Pearson correlation coefficient (Table 4).

Canonical Discriminant Analysis

All anthropometric variables (length B, width A, width C, angle α, and distances D, E, F, G, H, I, J, K) were used to establish a predictive classification of gender. Wilks’ lambda (value of 0.441) was significant (p < 0.001), with a canonical correlation of 0.748. With this model, 89.5 % of males and 86.5 % of females were correctly assigned to their gender group, and 89.5 % of males and 85.1 % of females after cross-validation.

Morphological Analysis

There was a statistically significant difference between the centroid size of males and females, showing a sexual dimorphism (p < 0.001), whereas no difference was found between groups 1 and 2 (Fig. 4). Analysis of the shape of the hyoid bones in shape space showed a statistically significant difference between males and females but there was no difference between groups 1 and 2 (Fig. 5). Moreover, a relationship between shape and size was found with ANOVA (p < 0.01).
Fig. 4

Boxplots of centroid size depending on sex and group

Fig. 5

Placement of the individuals on PC1 and PC2 in the shape space (principal components analysis of the Procrustes shape coordinates) showing a wide interindividual heterogeneity in terms of hyoid bone shape

Averaged specimens for males and females were extracted from the shape space, and 3D reconstruction using thin-plate splines are shown in Fig. 6. We observed that gender differences are localized in long horns, which are longer and narrower in males, and in the hyoid bone body, which is longer in males than in females. Moreover, a wide interindividual variation in terms of hyoid bone shape within the study population is shown in Figs. 5 and 7.
Fig. 6

3D reconstruction of the average female (red) and male (blue) shape in superior (a) and inferior (b) views. Differences are localized in long horns, which are longer and more constricted in males, and in hyoid bone bodies, which are longer in males than in females

Fig. 7

Superimposed warped hyoid bones according to PC1 (left) and PC2 (right). Superior views (top) and inferior views (bottom) of hyoid bone surface. a, b The blue warped hyoid bone corresponds to −0.2PC1 and the green warped hyoid bone corresponds to +0.2PC1. c, d The yellow warped hyoid bone corresponds to −0.1PC2 and the orange warped hyoid bone corresponds to +0.1PC2

Discussion

Anatomical and Anthropological Study of the Hyoid Bone

In this study we have shown that the characteristics of the hyoid bone, as defined by metric analysis and geometric morphometrics, including size and the relationship of the different parts of the bone, are highly heterogeneous and are closely linked with the sex, height, and weight of individuals. The metric approach, with its rigorous, repeatable, and reproducible methodology using 3D reconstruction, is more objective than morphological descriptions of the bone by visual analogy [4, 5]. This new methodology replaces a system in which the hyoid bone was simply described as a “U,” “V,” “horseshoe,” or asymmetrical shape based on visual observation, leading to observations that were not reproducible [6] and which, therefore, could not be used in practice. Moreover, geometric morphometrics, used for the first time in this kind of study, distinguishes the form of an object (shape plus size) from its shape (form with scale removed) by scaling to unit size, so that it is possible to model morphological variations without taking into consideration the size factor [14, 15, 16]. These observations highlight the need to use these hyoid bone models to study their impact in clinical practice.

Hyoid Bone and Sexual Dimorphism

The sexual dimorphism we observed was not an unexpected finding and constitutes a major feature for the purpose of modeling. In our study, the length and width of the hyoid were statistically greater in men than in women. These results are consistent with some previous reports where female hyoid bones tended to be smaller [6, 7, 20, 21, 22, 23, 24]. Furthermore, in our study, the angle formed by the two greater horns differed significantly between the sexes, being larger in women than in men. This significant difference may reflect gender differences in the pull of muscle on bone. In men, the muscles around the larynx and the two sternocleidomastoid muscles are more developed than in women so that the two greater horns come closer together, resulting in a smaller angle, as suggested by Pollard [7]. In our study, these results are confirmed, for the first time, by geometric morphometric analysis. Analysis of the shape of hyoid bones in shape space revealed a statistically significant difference between males and females. Our results show that conformation of the hyoid bone is a factor in sexual dimorphism. We observed that gender differences are localized in long horns, which are longer and more constricted in males, and in the body of hyoid bones, which is longer in males than in females. Moreover, we found a statistically significant difference between the centroid size of males and females. We also observed a relationship between shape and size. Indeed, this dimorphism is explained by an allometric relationship.

Relationship Between Weight and Height of an Individual and Hyoid Bone Dimensions

In contrast, few authors have attempted to study the hyoid bone in relation to other variables except sex, such as weight and height or BMI. In our study, there was a significant positive correlation between the height, weight, and BMI of subjects and hyoid bone length. On the other hand, the width was correlated only with the height of subjects and no correlation was found with the angle of the hyoid bone. This is consistent with our previous observation in which men had a longer hyoid bone than women. Generally, men are more corpulent (in terms of height and weight) than women [25]. These results are consistent with those of Pollard, except for the angle of the hyoid bone for which no correlation was found with either height or weight [7].

Influence of Muscles on Hyoid Bone Shape (Group 1 vs. Group 2)

Almost the entire surface of the hyoid bone has a large number of muscles attached, which move and support the tongue, larynx, and pharynx [26].

In our study, the length and width of the body of the hyoid bone were statistically greater in group 1 than in group 2. However, no statistical difference was observed in width between the greater horns and the angle of the hyoid bone between the two groups. This result highlights the influence of muscles on hyoid bone shape. In bones harvested from cadavers, all muscle insertions were removed from the bone before scanning, whereas in living subjects, the hyoid bone was under the influence of all the attached muscles. These results, previously unpublished to our knowledge, show that the muscles have an influence on hyoid bone morphology. The question is whether a narrower hyoid bone may induce a decrease in pharyngeal volume that may influence, in association with other risk factors, the development of pathologies such as sleep apnea. On the other hand, treatments such as radiotherapy or surgery for head and neck cancer induce muscle fibrosis that may increase the narrowness of the hyoid bone and thus of the pharyngeal volume, with potential consequences in terms of swallowing. These suggestions highlight the need for further anatomical studies to correlate the anatomy of the pharynx with morphology of the hyoid bone.

The increase in size of hyoid bones taken from cadavers could be explained by the fusion or not between the body and the greater horns which may make the hyoid bone more elastic. Variability in the time of fusion has been observed in many studies [6, 21, 27, 28, 29, 30, 31]. According to these studies, the fusion of these parts increases with age, with some authors reporting that fusion rarely occurs before 40 years [32], while others indicate fusion occurs before 30 years [21]. Gupta et al. [32] also state that fusion occurs earlier in women than in men. Forces exerted by muscles on the hyoid bone at rest and in movement (including speech articulation and mastication) have never been studied using a biomechanical approach. Some elements of response have been published by Pearson et al. [33] who showed that, based on structural properties, the geniohyoid had the most potential to displace the hyoid in the anterior direction, and the mylohyoid had the most potential to displace the hyoid in the superior direction. However, in their study only hyoid movement was analyzed and not the mechanical forces exerted on the entire surface of the hyoid bone. Our results suggest compression forces between the greater horns and the body rather than traction which could explain the fact that hyoid bones from group 1 (i.e., liberated from all muscle insertions) were longer than those from group 2. However, biomechanical studies are required to confirm this hypothesis.

Other data such as age, sex, and the morphology of individuals should be taken into account. Height of subjects may also influence hyoid bone morphology, as shown in our results. However, weight, and thus BMI, must be carefully analyzed as they can fluctuate during life. Moreover, age, sex, and muscular strength may influence bone mineralization, and thus bone hardness, with morphological consequences [34]. With respect to bones harvested from cadavers, even though muscles and soft tissues can be remodeled within 24–48 h after death, hyoid bone, due to its hardness, is not likely to be modified, particularly after soft tissue removal during autopsies.

Potential Applications in Clinical Practice

Forensic Science and Bioarchaeology

Determination of sex from skeletons remains an important feature of bioarchaeology and forensic science. Hip bones are considered the most efficient pointer to sex determination [35]. However, the craniocervical bones may be well preserved in archaeological or disaster-related contexts [36, 37]. Previous reports have shown that sex could be determined by analyzing hyoid bones on digital photographs [38], or from direct measurements on specimens [39, 40]. Our study showed that by using a highly reproducible technique, we could correctly assign 89.5 % of males and 86.5 % of females to their gender group by analyzing hyoid bone morphology. An interesting point is that age, in our study, did not influence the hyoid bone characteristics.

Head and Neck Cancer

Swallowing is a complex, dynamic motor behavior with both voluntary and involuntary components, and hyoid displacement is a critical component of swallowing. During swallowing, the hyoid bone is displaced vertically and anteriorly. This displacement is dependent on a sequenced and balanced contraction of the suprahyoid and infrahyoid muscles [41, 42]. It has been shown that reduction of this movement could lead to a swallowing impairment [43]. Some consequences of this could be impaired bolus transport, aspiration, and abnormal opening of the upper esophageal sphincter [44]. Several studies have reported the repercussions of cancer treatments such as radiation therapy or surgery on hyoid bone displacement and their impact in terms of swallowing impairment [45, 46, 47]. Pearson et al. [33] previously evaluated the structural properties of suprahyoid muscles using a cadaver model in order to understand how their morphology influences function. They showed that, based on structural properties, the geniohyoid had the most potential to displace the hyoid in the anterior direction and the mylohyoid had the most potential to displace the hyoid in the superior direction. German et al. [48] recently emphasized interest in such studies and discussed the relevance of further anatomical studies to better understand function. To our knowledge, no study has yet evaluated anatomical predisposition in post-treatment impairment. Indeed, due to the wide variations in hyoid bone morphology shown in our study and their potential impact on neck anatomy, anatomical predisposition should be studied as a predictor of post-treatment outcomes.

Sleep Apnea

The etiology of obstructive sleep apnea syndrome (OSAS) includes abnormalities in both the physiology and the anatomy of the airway and associated facial structures that lead to airway collapse. It has been suggested that patients with OSAS have a narrower pharyngeal airway than normal persons because of fat infiltration, the weight of the soft tissue of the neck, or reduced pharyngeal muscle tone. In recent years, upper airway size and shape have been measured by a number of techniques, including CT, fluoroscopy, MRI, nasoendoscopy and acoustic reflection [49]. Although these studies have demonstrated there to be considerable differences in pharyngeal shape and size between individuals with and without OSAS in terms of baseline anatomy and dynamic behavior, many studies have suggested that for a similar degree of obesity, differences in craniofacial and upper airway morphology contribute to the severity of OSAS [49, 50, 51, 52, 53, 54, 55]. An inferiorly positioned hyoid bone in OSAS has been well documented [56, 57]. However, the shape of the bone could influence the size or patency of the pharynx by modifying pharyngeal muscle insertions. To date, no study has assessed the role of hyoid bone morphology as a risk factor for sleep apnea.

Conclusion

In this study, we showed that the characteristics of the hyoid bone, including size and the relationship of the different parts of the bone as determined by metric analysis and geometric morphometrics, are highly heterogeneous and are closely linked with the sex, height, and weight of individuals. This very reproducible methodology is important because it can be applied to other bones or cartilages such as the thyroid and cricoid cartilages and the mandible and may lead to clinical studies, in head and neck cancer or sleep apnea, for example. Such studies are ongoing in our research program.

Notes

Conflict of interest

The authors have no conflicts of interest to disclose.

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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Nicolas Fakhry
    • 1
    • 2
  • Laurent Puymerail
    • 2
  • Justin Michel
    • 1
    • 2
  • Laure Santini
    • 1
    • 2
  • Catherine Lebreton-Chakour
    • 2
    • 3
    • 4
  • Danielle Robert
    • 1
  • Antoine Giovanni
    • 1
  • Pascal Adalian
    • 2
  • Patrick Dessi
    • 1
    • 2
  1. 1.Service d’ORL et Chirurgie Cervico-Faciale, Centre Hospitalier Universitaire (CHU) La TimoneAssistance Publique-Hôpitaux de Marseille (AP-HM)/Aix-Marseille UniversitéMarseille Cedex 05France
  2. 2.Unité d’Anthropologie Bioculturelle, CNRS-EFS, Faculté de Médecine NordUMR 6578, Aix-Marseille UniversitéMarseilleFrance
  3. 3.Laboratoire de Médecine Légale et de droit Médical, Faculté de MédecineAix-Marseille UniversitéMarseilleFrance
  4. 4.AP-HM, Hôpital Timone, Institut de Médecine LégaleMarseilleFrance

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