Observation on the attachment of muscles onto the hyoid bone in human adults

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1 attachment Okajimas Folia of muscles Anat. onto Jpn., the 85(3): hyoid 79 90, bone November, in human Observation on the attachment of muscles onto the hyoid bone in human adults By Naohiro SONODA and Yuichi TAMATSU Department of Neurology, Gross Anatomy Section, Kagoshima University Graduate School of Medical and Dental Sciences Sakuragaoka, Kagoshima Received for Publication, June 23, 2008 Key Words: gross anatomy, hyoid bone, suprahyoid muscles, infrahyoid muscles Summary: The attachments of muscles onto the hyoid bone were observed macroscopically, and the lengths and widths of each muscles onto the hyoid bone were measured. The tongue-pharyngeal block as a whole obtained from 50 cadavers were used. Each muscle was colored by acrylic pigments for identification. The results showed that the mylohyoid muscles were attached onto the lower anterior surface of the hyoid bone body. The geniohyoid muscles had many types of attachment forms and significant individual differences. The hyoglossal muscles showed various attachments at the posterior end of the greater cornu. The middle pharyngeal constrictor muscles attached with two bundles in some cases. The sternohyoid muscles and omohyoid muscles were classified by their positional relationship with each other. The thyrohyoid muscles were classified by the conditions of their overlaps with the omohyoid muscles and the sternohyoid muscles. From the aforementioned results, the following muscles were found attached to the hyoid bone in a further developed state: mylohyoid muscles, geniohyoid muscles, hyoglossal muscles, thyrohyoid muscles and hyoglossal muscles. Introduction The actions of chewing and swallowing are performed by a delicate coordination of various muscles around the oral cavity. In particular, the hyoid bone is one of the important elements for mandibular movements for mastication. Particularly in the head and neck regions, the hyoid bone is a distinct bone that has no synovial articulation with circumjacent bones but connected to its adjacent structures with ligaments and muscles. About a ligamentous connection, the hyoid bone is connecting to the styloid process of temporal bone with stylohyoid ligament at the top and connecting to the superior border of the thyroid cartilage with thyrohyoid membrane at the bottom. About a muscular connection, the suprahyoid muscles, the infrahyoid muscles and the middle pharyngeal constrictor muscles are situated at the top, bottom and posterior regions. Because of vacuity of joints, the movements of hyoid bone mainly depend on the attached muscles. Though previous anatomical textbooks include morphographic descriptions of the hyoid muscles attached onto the hyoid bone, there are slight differences in each textbook about the attachment area. Regarding the morphology of the attachment of suprahyoid/infrahyoid muscles to the hyoid bone, various description is reported in cases of Japanese previously studies 1 7). Furthermore, there are a number of reports on abnormal cases of muscle attachment to the hyoid bone 8). However, there are few previous reports describing the results of measurements for each muscle attachment area to the hyoid bone. From the abovementioned aspects, it is important to clarify the detailed forms of morphological attachment onto the hyoid bone. Materials and methods In this study, 50 blocks of tongue-pharynx specimens were obtained from 50 cadavers (25 males, 25 females) for dissection course at Kagoshima University Dental School. Firstly, the connective tissues of the submandibular part and the anterior neck were removed. Next, each attached muscle were marked to identify clearly, the muscles attached to the hyoid bone were carefully removed under the stereomicroscope (SZX-12, Olympus). In addition, a mark was placed using the tip of a sharp scalpel. For each muscle, the attachment area on the hyoid bone was colored using acrylic pigments. The specimens were then immediately placed in a hydrator to prevent deformation of the hyoid body, and then dried gradually (Fig. 1, 2). Next, the forms of attachment of each muscle were classified as appropriate and the width and thickness for

2 80 N. Sonoda and Y. Tamatsu each muscle were measured using the slide caliper (Digimatic Caliper CD-S, Mitsutoyo) with 1/20-mm scale. The width refers to the length in the horizontal direction, and the thickness was measured at the widest part of the muscle attachment area (Fig. 3A, B, C, D). However the digastric muscles are indirectly attached to the hyoid bone in a state of aponeurosis9). In addition, the stylohyoid muscles are only attached to the hyoid bone indirectly by forming a ring-shaped9) aponeurosis inside to fix the intermediate tendon of the digastric muscles, and no direct attachment of the muscle fibers onto the Fig. 1. (A) The hyoid bone before extraction and a peripheral muscle group in front. (B) The hyoid bone before extraction and a peripheral muscle group of lateral side. (C) The extracted hyoid bone and muscles. C, lesser cornu; Da, anterior venter of digastric muscle; Dp, posterior venter of digastric muscle; H, hyoglossal muscle; M, mylohyoid muscle; MP, middle pharyngeal constrictor muscle; O, omohyoid muscle; S, sternohyoid muscle; TH, thyrohyoid muscle. Fig. 2. (A) The anterior surface of the hyoid bone body, each attachment site was colored with an acrylic color. (B) lateral side of the greater cornu of the hyoid bone, each attachment site was colored with acrylic color. (C) the medial side of the hyoid bone, each attachment site was colored with acrylic color. C, lesser cornu; G, geniohyoid muscle; H, hyoglossal muscle; M, mylohyoid muscle; MP, middle pharyngeal constrictor muscle; O, omohyoid muscle; S, sternohyoid muscle; TH, thyrohyoid muscle.

3 attachment of muscles onto the hyoid bone in human 81 hyoid bone is observed. Therefore, the digastric muscles and the stylohyoid muscles were not included on the list of items for measurement in this study, and were instead only observed regarding their forms. Findings and consideration The morphology of the each muscle which is attached to the hyoid bone is shown. We classified the form of the attached area to the anterior surface, dorsal surface, and no relationship was seen regarding the direct attachment onto the hyoid bone. 1. The muscles attached to the anterior surface of the body of hyoid bone 1) Mylohyoid muscle (Fig. 2A) In all cases, the mylohyoid muscles were attached onto throughout the entire length of the lower anterior portion on the body of hyoid bone. On the superior border of this muscle attachment area, geniohyoid muscles and hyoglossal muscles were attached. The measurements of the attachment area showed larger values in male than in female for the width at both sides, while the thickness of the attached area resulted in approximately similar in both sexes. When measuring the ratio between the width/thickness and the length of the body of the hyoid bone, there were no significant differences between the sexes in terms of width and thickness (Table 1). 2) Geniohyoid muscle (Fig. 2A) As a whole, the geniohyoid muscles were attached onto the anterior surface of the body of the hyoid bone. The superior border of the attachment reached the upper part of the body, and the inferior border of the attachment came into contact with the attachment area of the mylohyoid muscle. Particularly strong attachments were seen in the superior part of the attachment. In most cases (right side: 47 cases 94%; left side: 45 cases 90%), geniohyoid muscle was attached so as to enfold the hyoglossal muscle with representing a U-shape tilted 90 that opens to lateral side. In addition by observing whether the muscle extended and reached the lesser cornu, the same morphology cases where the muscle did not reach the lesser cornu were classified as Type 1, while those where the muscle reached the lesser cornu were classified as Type 2 (Fig. 4 A, B). Type 1 was observed on the right side in 45 cases (90%) and on the left side in 41 cases (82%). Type 2 was Table 1. of mylohyoid muscle attachment area and a ratio (%) for the hyoid bone body Side Sex Mean (mm) S.D. Ratio (%) Width Right Thickness Right Fig. 3. The measuring range of (A) the mylohyoid and geniohyoid muscle. (B) the hyoglossus muscle. (C) the middle pharyngeal constrictor muscle. (D) the sternohyoid, omohyoid and thyrohyoid muscle

4 82 N. Sonoda and Y. Tamatsu observed on the right side in 5 cases (10%) and on the left side in 9 cases (18%). Furthermore, regarding to the connection state of the geniohyoid muscle on both sides around the midline area of the hyoid bone body, states in which the muscle did not connect with both sides were classified as Type 1, while states where the muscle connected with both sides were classified as Type 2 (Fig. 4 C, D). Type 1 was observed in 26 cases (52%), and Type 2 was observed in 24 cases (48%). The measurements of attachment area indicated larger values in males than in females for the width and thickness at both sides. In the measurements of the ratio between width/thickness and the length of the hyoid bone body, differences in width were slightly larger in males at both sides. The ratio of thickness was approximately the same between the sexes (Table 2). Table 2. of geniohyoid muscle attachment area and a ratio (%) for the hyoid bone body Side Sex Mean (mm) S.D. Ratio (%) Width Right Thickness Right ) Hyoglossal muscle (Fig. 2A, 2B) The hyoglossal muscle was attached to the part between the geniohyoid muscles or across the entire length of the inferior border of the hyoid bone from both sides of the geniohyoid muscles over the body/greater cornu joint in some cases. In other cases, the muscle bundles of hyoglossal muscles were not attached continuously throughout the entire body of the hyoid bone, and the muscle bundles of the thyrohyoid muscles, omohyoid muscles and middle pharyngeal constrictor muscles were attached to the greater cornu of the hyoid bone. Consequently, these morphology were classified between the continuing pattern (Type 1) and the discontinuing pattern (Type 2) (Fig. 5 A, B). Type 1 was observed on the right side in 31 cases (62%) and on the left side in 22 cases (44%). Type 2 was observed on the right side in 19 cases (38%) and on the left side in 28 cases (56%). The forms of attachment were classified into two types according to whether the muscle was attached so as to enfold the posterior end of the greater cornu. The enclosure-type muscle attachment was classified as Type 1, and the type of attachment to the only lower posterior end was classified as Type 2 (Fig. 5 C, D). As a result, Type 1 was observed on the right side in 19 cases (38%) and on the left side in 24 cases (48%). Type 2 was observed on the right side in 31 cases (62%) and on the left side in 26 cases (52%). Those attaching conditions of the attachment area were not hardened and not difficult to dissection. The measurements of the attachment area showed larger values in males than in females for the width at both sides. However, no significant difference was found in thickness between the sexes. In addition, when measuring the ratio between width/thickness and the length of the greater cornu, there was no significant difference in the width between the sexes. The larger thickness values were shown in females on both sides (Table 3). 4) Middle pharyngeal constrictor muscle (Fig. 2B) This is a ring-shaped muscle that constitutes the posterior wall of the pharynx. Upon dissection, the attachment conditions of these muscles were relatively loose, thus allowing for easy dissection to separate each muscle. Numerous anatomical textbooks commonly state that the middle pharyngeal constrictor muscle is attached continuously from the posterior end to the middle part of the greater cornu of the hyoid bone. However, in actual observation of the morphological form, some cases indicated that the muscle bundle attached to the anterior part and posterior part of the greater cornu with separating into two bundles. Therefore, cases of continuous muscle bundles were classified as Type 1, while cases of discontinuous muscle bundles were classified as Type 2 (Fig. 6 A, B). As a result, Type 1 was observed on the right side in 43 cases (86%) and on the left side in 45 cases (90%). Type 2 was observed on the right side in 7 cases (14%) and on the left side in 5 cases (10%). The measurements of attachment area showed larger values in males than in females for the width at both sides. However, no significant difference was observed in Fig. 4. Photographs and illustrations showing the attachment area of the geniohyoid muscle to the hyoid bone. (A) Type1. the geniohyoid muscle without attaching to lesser cornu of the hyoid bone (B) Type 2. The upper border of the attachment area of the geniohyoid muscle reached to the lesser cornu of the hyoid bone which arrow points. (C) Type 1. Both right and left geniohyoid muscles have no contact with each other. (D) Type 2. The right and left geniohyoid muscles have touched mutually. G, geniohyoid muscle; H, hyoglossal muscle; M, mylohyoid muscle;

5 attachment of muscles onto the hyoid bone in human 83

6 84 N. Sonoda and Y. Tamatsu Table 3. of hyoglossal muscle attachment area and a ratio (%) for greater cornu Width Thickness Side Sex Mean (mm) S.D. Ratio (%) Right Left Right Left Muscles attached to the dorsal surface of the hyoid bone 5) Sternohyoid muscle (Fig. 2C) In all cases, the sternohyoid muscle was attached and localized to the outer edge or partial posterior surface of the body on hyoid bone on both sides of the posterior surface. The attachment condition was not firm. In some cases, since the muscle crossed over with the omohyoid muscle, it was necessary to perform dissections while confirming each muscle. The measurements showed larger values in males than in females for the width at both sides. However, few differences in thickness were observed between the sexes. Furthermore, regarding the measurements of the ratio of width/thickness to the length of the hyoid bone body, there was no significant difference in width and thickness between the sexes (Table 5). Fig. 5. Photographs and illustrations showing the attachment area of the hyoglossal muscle to the hyoid bone. (A) Type 1. The attachment area continues from anterior to posterior. (B) Type 2. The attachment area was separated into two regions. (C) Type 1. The muscle was attached so as to enfold the posterior end of the greater cornu. (D) Type 2. The muscle was attached to the only lower posterior end. G, geniohyoid muscle; H, hyoglossal muscle; M, mylohyoid muscle; MP, middle pharyngeal constrictor muscle; O, omohyoid muscle; S, sternohyoid muscle; TH, thyrohyoid muscle. the thickness between the sexes. In addition, when measuring the ratio of width/thickness to the length of the greater cornu, there was no significant difference in width and thickness between the sexes (Table 4). 6) Omohyoid muscle (Fig. 2C) This muscle was attached to the posterior part of the hyoid body near the border between the body and greater cornu. Part of the muscle bundle reached the lower anterior surface. The attachments were not very strong. However, in some cases, the muscle crossed with the sternohyoid muscle. For such cases, some rigidness was felt during the dissection. The forms of attachment were classified into three types according to the relationship between the omohyoid muscle and the stylohyoid muscle. Cases where the omohyoid muscle was adjacent to the sternohyoid muscle were classified as Type 1, cases where the muscle bundle entered the sternohyoid muscle were classified as Type 2, and cases where this muscle was attached so as to cover the sternohyoid muscle were classified as Type 3 (Fig. 7). Type 1 was observed on the right side in 38 cases (76%) and on the left side in 33 cases (66%). Type 2 was ob-

7 attachment of muscles onto the hyoid bone in human 85 Table 4. of middle pharyngeal constrictor muscle attachment area and a ratio (%) for greater cornu Side Sex Mean (mm) S.D. Ratio (%) Width Right Thickness Right Table 5. of sternohyoid muscle attachment area and a ratio (%) for the hyoid bone body Side Sex Mean (mm) S.D. Ratio (%) Width Right Fig. 6. Photographs and illustrations showing the attachment area of the middle pharyngeal constrictor muscle to the hyoid bone. (A) Type 1. The attachment area continues from anterior to posterior. (B) Type2. The attachment area was separated at the middle area of greater cornu. G, geniohyoid muscle; H, hyoglossal muscle; MP, middle pharyngeal constrictor muscle; Thickness Right served on the right side in 7 cases (14%) and on the left side in 10 cases (20%). Type 3 was observed on the right side in 5 cases (10%) and on the left side in 7 cases (14%). The measurements of attachment parts showed larger values in males than in females for the thickness at the left side. However, at other sites, few differences were found between the sexes. Furthermore, in the measurements of the ratio of width/thickness to the length of the hyoid bone body, no significant difference was found in the width and thickness between the sexes (Table 6) ) Thyrohyoid muscle (Fig. 2C) The attachment condition of this muscle was the strongest among the infrahyoid muscles. This muscle was attached to the hyoid bone from the border between the body and greater cornu to approximately 2/3 of the entire length of the lower border of the greater cornu of the hyoid bone in many cases (right side: 45 cases 90%, left side: 44 cases 88%). In addition, when observing the attachment condition of adjacent sternohyoid muscles and omohyoid muscles, in some cases the thyrohyoid muscle spread beyond borders between body and greater cornu and attached so as to overlap with these muscles. Accordingly, cases where the attachment part did not overlap with the sternohyoid muscles and omohyoid muscles were classified as Type 1, and cases where the attachment part overlapped with them were classified as Type 2 (Fig. 8). Type 1 was observed on the right side in 33 cases (66%) and on the left side in 34 cases (68%). Type 2 was observed on the right side in 17 cases (34%) and on the left side in 16 cases (32%). The measurements of the attachment parts indicated larger values in males than in females for the thickness at both sides. However, few differences were observed in width at both sides between the sexes. Furthermore, in the measurements of the ratio of width/thickness to the length of the greater cornu, no difference was observed

8 86 N. Sonoda and Y. Tamatsu Table 6. of omohyoid muscle attachment area and a ratio (%) for the hyoid bone body Width Thickness Fig. 7. Side Sex Mean (mm) S.D. Ratio (%) Right Left Right Left Photographs and illustrations showing the attachment area of the omohyoid muscle to the hyoid bone. (A) Type 1. The omohyoid muscle was adjacent to the sternohyoid muscle. (B) Type 2. The muscle bundle entered the sternohyoid muscle. (C) Type 3. The muscle was attached so as to cover the sternohyoid muscle. O, omohyoid muscle; S, sternohyoid muscle; TH, thyro hyoid muscle;, the attachment area shared by both omo hyoid and sternohyoid muscle. in width and thickness between the sexes (Table 7). 3. Muscles which have no direct attachments to the hyoid bone 8) Digastric muscle Among all specimens recognized in this observation, the digastric muscle was in the state of an intermediate tendon passing through 1 to 2 cm above the hyoid bone without any direct attachments to the hyoid bone. Regarding connections with the hyoid bone, attachment to mylohyoid muscles was found in 10/22 cases (45%), Fig. 8. Photographs and illustrations showing the attachment area of the thyrohyoid muscle to the hyoid bone. (A) Type 1. the attachment part did not overlap with the sternohyoid and omohyoid muscles. (B) Type 2. the attachment part overlapped with the sternohyoid and omohyoid muscles. O, omohyoid muscle; S, sternohyoid muscle; TH, thyrohyoid muscle;, the attachment area shared by both omohyoid and sternohyoid muscle.

9 attachment of muscles onto the hyoid bone in human 87 Table 7. attachment via tendinous or fibrous connective tissues was found in 7/22 cases (32%), attachment to stylohyoid muscles was observed in 4/22 cases (18%), and attachment to omohyoid muscles was found in 1/22 case (5%). Attachments to the mylohyoid muscles include those attached to the part of the fine muscle fibers of the digastric muscles or aponeurosis. Some of them were not clearly differentiated from those attached via tendinous or fibrous connective tissues. 9) Stylohyoid muscle Similar to the digastric muscle, the stylohyoid muscle was bundled into an aponeurotic state 1 to 1.5 cm above the hyoid bone and attached to the surrounding muscles or connective tissues in most cases. In 3/22 cases (14%), the stylohyoid muscle extended to enfold the venter posterior of the digastric muscles. Although it was extremely tenuous, direct muscle attachment was seen in only one case. Regarding connections with the hyoid bone, attachment to the peripheral connective tissues that included the hyoid bone in the tendinous or aponeurotic state was seen in 10/22 cases (45%), attachment to mylohyoid muscles was seen in 7/22 cases (32%), joints with the attachment part of the omohyoid muscles were seen in 4/22 cases (18%), and joints with the attachment part of the sternohyoid muscles and thyrohyoid muscles were seen in 1/22 cases (5%). Discussion of thyrohyoid muscle attachment area and a ratio (%) for greater cornu Side Sex Mean (mm) S.D. Ratio (%) Width Right Thickness Right Using a gross anatomic method, the forms of attachment of hyoid muscles were observed. In contrast to past reports, each muscle will herein be discussed individually. 1. Mylohyoid muscle There are a few reports on the mylohyoid muscles of Japanese subjects. According to Suzuki (1918) 10), when no mylohyoid muscle exists and when the muscle becomes extremely thin, the muscle may be separated into the anterior and posterior parts, and the submandibular glands enter the gap. On the other hand, in a report on the form relationship between the mylohyoid muscle and the hyoid bone, Tanaka (1958) 11) classified the forms of mylohyoid muscle-attachment to the hyoid bone into the following seven types: both ends reached the greater cornu (Type 1); the left end reached the greater cornu and the right end reached the border of the body and the greater cornu (Type 2); the reverse of Type 2 (Type 3); the same as Type 3 except that the left end did not reach the border of the body and the greater cornu (Type 4); both ends reached the border of the body and the greater cornu (Type 5); the right end did not reach the border of the body and the greater cornu and the left end did not reach the border (Type 6); both ends did not reach the border of the body and the greater cornu (Type 7). It was reported that among these types, Type 5 was observed most frequently. In addition, according to a report by Saka et al. (1958) 12), they classified the attachments into two types: one type in which both ends terminated at the border of the body and the greater cornu, as well as another type in which the attachment part was situated on the geniohyoid muscles and thyrohyoid muscles, extending outward by 4 mm or so. It was reported that the former type was the most frequently observed. In most cases of this study, both ends reached the border of the body and the greater cornu. In Tanaka s report, Type 5 (the form in which both ends reached the body and the greater cornu) was observed in more than half of all cases. In the report from Saka et al., the type in which both ends reached the body and the greater cornu was found in most cases as well. Consequently, our findings were fairly close to the reports by both Tanaka and Saka et al. 2. Geniohyoid muscle Anomalies in the geniohyoid muscle were rarely reported. According to Suzuki (1918) 10), when both sides of a muscle are fused or separated into bundles, a further separated outer muscle bundle may reach the greater cornu of the hyoid bone. In addition, according to Ogata (2002) 13), despite the variety of forms of the attachment parts, they were approximately symmetric at both sides. According to Tanaka (1985) 11), there are three types for the superior border of the geniohyoid muscle termination part: one in which the muscle bundle on the upper part of the geniohyoid muscle extended outward and reached the lesser cornu (Type A), one in which the muscle bundle came into contact with the lesser cornu (Type B), and one in which the muscle bundle did not come into contact with the root part of the lesser cornu (Type C). On the other hand, Saka et al. (1958) 12) also reported classifica-

10 88 N. Sonoda and Y. Tamatsu tions for the superior border of the geniohyoid muscle termination part, including one in which the outer end came into contact with the root part of the lesser cornu of the hyoid bone, and another in which there was a gap between the outer end and the root part of the lesser cornu. In these reports, Tanaka stated that Type B (in which the muscle reached the root part of the lesser cornu) was observed most frequently among the types of the superior border of the geniohyoid muscle termination part, while Saka et al. reported that the type in which the outer end came into contact with the root part of the hyoid bone of the lesser cornu was observed most frequently among those of the superior border of the geniohyoid muscle termination part. In this observation, for the classification of the forms of joints at both termination parts, only two types were used: jointed or unjointed. This is because the forms of attachment parts varied between broad groups, and individual differences were also significant. The wide variety of attachment conditions of geniohyoid muscles is believed to be due to considerable changes depending on the attachment conditions of hyoglossal muscles entering from the outside. 3. Hyoglossal muscle In Tanaka s report (1985) 11), there are two types, including one in which the hyoglossal muscle originates from the lower posterior end of the greater cornu, and one originating from the upper posterior end. Saka et al. (1985) 12) classified two types, including one in which the hyoglossal muscle reached the posterior end ampullar part and another in which the hyoglossal muscle originated from an area slightly ahead of the ampullar part. In this observation, we found cases where the attachment terminated at the lower posterior border of the greater cornu, as well as cases where the hyoglossal muscle was attached so as to enfold the posterior end of the greater cornu. However, according to Tanaka (1985) 11), there were no observed cases where the attachment part of the hyoglossal muscle split off in the middle. Saka et al. (1985) 12) classified cases into ones in which the attachment part to the outer inferior border of the greater cornu was clearly separated and others in which the attachment part continued. On the other hand, Ogata et al. (2002) 13) reported that the muscle bundle separated into an anterior part and a posterior part. In the results from our observations, cases where each muscle bundle separated into two parts were seen on the right side in 19 out of 50 cases (38%) and on the left side in 28 cases (56%). 4. Middle pharyngeal constrictor muscle Although there are few reports on the middle pharyngeal constrictor muscle, the individual differences are believed to be significant (Suzuki, 1918) 10). Tanaka (1985) 11) classified the attachment conditions of the muscle on the greater cornu of the hyoid bone into the following types: one in which the attachment part extends along almost the entire length of greater cornu and the anterior end reaches the root part of the lesser cornu (Type 1); one in which the attachment part spreads forward, exceeding half of the greater cornu (Type 2); one in which the attachment part does not extend to half of the greater cornu (Type 3); and one in which the attachment part is situated only around the posterior end of the greater cornu (Type 4). Subgroups were created for each type for cases in which the muscle was torn, thus resulting in a total of 8 types. In addition, Saka et al. (1985) 12) classified cases into three types: one in which muscles were attached only to the apical part of the greater cornu (Type I); one in which muscles were attached on the greater cornu to 1/3 ahead of the apical part, around the outer end of thyrohyoid muscle (Type II); and one in which muscles reached close to the lesser cornu at a position further ahead (Type III). In these reports, Tanaka observed Type I (cases where the attachment part extended along almost the entire length of the greater cornu and the anterior end reached the root part of the lesser cornu) most frequently, while Saka et al. observed Type II (cases where the attachment part extended to 1/3 ahead of the apical part of greater cornu, around the outer end of thyrohyoid muscles) most frequently. In this study, we observed the muscle in terms of continuity and discontinuity. Similar to Tanaka s report, many of the muscle attachments had continuity. The report by Saka et al. did not observe any cases of discontinued muscles. In our observation, based on the attachment conditions of pharyngeal muscles, it seemed that this muscle should be supported by attachments on the greater cornu of the hyoid bone. 5. Sternohyoid muscle/omohyoid muscle There are a number of reports on abnormal cases of omohyoid muscles by Yamada (1934) 14), Fukuyama & Li (1941) 15), Sekido & Takahasi (1953) 16), Yamada & Nishijima (1954) 17), Yonekura (1854) 18), Takano & Adachi (1954) 19), Yamada et al. (1960) 20), Sato et al (1969) 21). Examples include cases where the muscle is either entirely or partially missing, where the intermediate tendon is absent, where the muscle bundle originates from the clavicle, where the superior belly and the sternal muscles are fused, and where muscle fibers diffuse into the cervical fascia. As mentioned above, there are a number of reports on muscle shape. With attention paid to the attachment condition of these muscles and the tongue, Tanaka (1985) 11) reported the following four classifications: a type in which, depending on the overlapping status of omohyoid muscles and sternohyoid muscles, the anterior part of omohyoid muscle is situated above the sternohyoid muscle (Type 1); a type in which more than half of the omohyoid muscles are situated on the sternohyoid muscle (Type 2); a type in which less than half of the omohyoid muscles are situated on the sternohyoid muscle (Type 3); and a type in which the attachment parts

11 attachment of muscles onto the hyoid bone in human 89 of the omohyoid muscles and the sternohyoid muscles comes into contact with each other (Type 4). Saka et al. (1985) 12) reported three classifications: a type in which the omohyoid muscle covered the sternohyoid muscle, passing the inferior border to reach the outer surface (Type I), a type in which the omohyoid muscle covered the sternohyoid muscles, terminating at the inferior border (Type II), and a type in which both muscles came into contact with each other (Type III). Tanaka reported that Type 4 (the type in which the attachment parts of the omohyoid muscles and the sternohyoid muscles came to contact) was observed most frequently. Saka et al reported that Type I (the type in which the omohyoid muscle covered the sternohyoid muscles, passing the inferior border to reach the outer surface) was observed most frequently. In our observation, cases where the omohyoid muscle was adjacent to the sternohyoid muscle were observed on the right side in 38 cases (76%) and on the left side in 33 cases (66%), cases where the muscle bundle entered into the sternohyoid muscle were observed on the right side in 7 cases (14%) and on the left side in 10 cases (20%), and cases where the omohyoid muscle was attached so as to cover the sternohyoid muscles were observed on the right side in 5 cases (10%) and on the left side in 7 cases (14%). Tanaka observed cases where the omohyoid muscle was adjacent to the sternohyoid muscle most frequently. However, in our observations, cases where the muscle bundle of the omohyoid muscles entered into the sternohyoid muscle were observed on the right side for 10% and on the left side for 14% of observed cases. Such observed cases were not described in the reports by Tanaka and Saka et al. This is believed to be due to the various forms of omohyoid muscles, as it is said that the omohyoid muscle terminates at the outer border of the lower anterior surface of the hyoid bone body, and that the intermediate tendon is covered by the cervical fascia and fixed 8), and it is well known that there are many abnormal cases involving these muscles. 6. Thyrohyoid muscle Regarding the attachment parts of thyrohyoid muscles, based on the overlapping condition of omohyoid muscles and sternohyoid muscles, Tanaka (1985) 11) classified cases into three types, including one in which the thyrohyoid muscle was covered by sternohyoid muscles and omohyoid muscles (Type 1), one in which the thyrohyoid muscle was covered by omohyoid muscles only (Type 2), and one in which the thyrohyoid muscle was not covered by either of the two muscles (Type 3). It was reported that Type 2, in which the thyrohyoid muscle was covered by omohyoid muscles only, was frequently observed. However, in our observations, we classified cases where the thyrohyoid muscle did not overlap with sternohyoid muscles and omohyoid muscles as Type 1 and cases where the thyrohyoid muscle overlapped as Type 2. In relation to Tanaka s report, Type 1 is equivalent to Type 3 and Type 2 is equivalent to Types 1 and 2. In our observations, Type 1 was seen on the right side in 33 cases (66%) and on the left side in 34 cases (68%). Type 2 was observed on the right side in 17 cases (34%) and on the left side in 16 cases (32%), thus contradicting Tanaka s report. Consequently, it was found that the following four muscles were firmly attached to the hyoid bone: mylohyoid muscles, geniohyoid muscles, hyoglossal muscle, and thyrohyoid muscles. This is also true in terms of the width and thickness of the muscle attachment parts measured in this study. The abovementioned four muscles indicated high values in the measurements reported by Tanaka (1985) 11) and Saka et al (1985) 12). However, because Tanaka measured both sides of the hyoglossal muscles as a block, we could not compare it with our measurements. Regarding geniohyoid muscles, similar results were reported. As to the hyoglossal muscles, higher values for the muscle venter part were reported by Tanaka. In our observations, there were cases where the attachment forms of the hyoglossal muscles were divided in two. On the other hand, such cases were not confirmed in the report by Tanaka. Therefore, the measurements by Tanaka seemed to be larger. Regarding the thyrohyoid muscle, in comparison to the measurements by Tanaka, our measurements indicated larger values (Table 8). For our study, we measured the ratio between the size of the attachment area for each muscle and the size of the hyoid bone. No significant difference was observed between the sexes. This is believed to be because the size of the hyoid bone affects the attachment area of each muscle, and the size is larger for males. On the other hand, according to the report by Sato et al 22) on the constitution of the muscle fiber of hyoid muscles, the most developed muscles (in terms of the total number of muscle fibers, thickness, and density) are the anterior belly of digastrics muscles and the geniohyoid muscles. Moderately developed muscles include the mylohyoid muscles, the thyrohyoid muscles and the sternohyoid muscles. In our observations of the forms of attachments to the hyoid bone, the attachment conditions, and the constitution of each muscle fiber, the geniohyoid muscles are considered to perform the most significant action among the muscles that are attached to the hyoid bone, functioning to pull the hyoid bone upward together with the mylohyoid muscles and the digastrics muscles. This seems rational, since when the geniohyoid muscle is attached onto the hyoid bone, the attachment extends from the upper anterior to the anterior surface of the hyoid bone body broadly in terms of both width and thickness, and the attachment strength is high. Mylohyoid muscles serve as jaw-opening muscles that pull the mandible downward. In addition, during the lateral movements of the tongue, these muscles are believed

12 90 N. Sonoda and Y. Tamatsu to support an appropriate position of the hyoid bone. Furthermore, upon swallowing, the mylohyoid muscles carry out the function of tensing the bottom of the oral cavity to lift the tongue. The attachment conditions to the hyoid bone range broadly between the upper anterior, upper lateral and the inferior surfaces of the hyoid bone body, and the degree of attachment is strong. Therefore, it is assumed that the mylohyoid muscles perform significant actions. Thyrohyoid muscles act to pull the hyoid bone downward and fix the bone in cooperation with the sternohyoid muscles upon opening the mouth. When the hyoid bone is fixed, the thyrohyoid muscles lift the thyroid cartilage to pull up the pharynx. It has been shown that the main actions of thyrohyoid muscles include ensuring the closure of the laryngeal inlet together with the epiglottis to prevent accidental ingestions and asphyxiation. Although it was not described in the report by Sato et al. 22) on hyoglossal muscles, which are extrinsic muscles, the attachments to the hyoid bone were firm compared to the attachments to the greater cornu. These muscles originate in the hyoid bone body and the greater cornu. When hyoglossal muscles constrict when the hyoid bone is fixed, it acts to pull the tongue toward the lower posterior. Other middle pharyngeal constrictor muscles, sternohyoid muscles and omohyoid muscles have small attachment areas and weak attachment conditions. Even though it is necessary to take the shape of the hyoid bone, differences between the sexes 23, 24), individual differences, etc., into consideration, based on the gross anatomical observations of this study. References 1) Leonhardt H, Tillmann B, Töndury G and Zilles K. Rauber/ Kopsch Anatomie des Menschen Band1. Georg Thieme Verlag Stuttgart New York, 1987; ) Anderson JE. Grant s Atlas of Anatomy; Williams & Wilkins Baltimore, 1983; figure 7 86, 87. 3) Romanes GJ. Cunningham s Textbook of Anatomy; Oxford University Press Oxford, 1981; ) Petra Köpf-Maier. Wolf-Heidegger s Atlas of Human Anatomy Volume 2; Karger Basel, 2000; ) Williams PL, Warwick R, Dyson M and Bannister LH. Grey s Anatomy; Churchill Livingstone London, 1989; ) Dubrul EL. Sicher s oral anatomy; The C. V. Mosby Company St. Louis, 1980; 55. 7) Mitsui T, Shimai K, Yasuda K, Kato S, Kubota K and Inoue Y. Okajima s Anatomy New Edition; Kyorin Shoin Japan, 1986; (in Japanese). 8) Sato T and Akita K. Anatomic variations in Japanese; University of Tokyo Press Tokyo, 2000; (in Japanese). 9) Shigemasa K and Moriyama H. Morphology of the human digastric muscle emphasizing the intermediate tendon. Showa Univ J Med Sci 1999; 59: (in Japanese with English abstract). 10) Suzuki B. Jintai Keito Kaibogaku; Maruzen Tokyo, 1918; (in Japanese). 11) Tanaka M. Anatomical study of a Japanese hyoid bone (Part1) About muscle adhesion department of a hyoid bone. Tokyo Dental College Kaibogakugyosekisyu 1958; 9:1 20 (in Japanese). 12) Saka M and Tanaka M. About muscle adhesion department in a hyoid bone. Tokyo Dental College Kaibogakugyosekisyu 1958; 7:1 7 (in Japanese). 13) Ogata S, Mine K and Simada K. Attachments of the geniohyoid and hyoglossus muscles on the hyoid bone with special reference to oral rehabilitation. Bull Sch Health Sci Kagoshima Univ 2002; 13:5 8 (in Japanese with English abstract). 14) Yamada S. Üder Einige Variationen der Mm. Infrahyoidei und Anomalien des Clavicularen Ansatzes des M. Trapezius an den Japanischen Foeten und Neugeborenen. Acta Anatomica Nipponica 1934; 7: (in Japanese). 15) Fukuyama U and Me-Lin Li. Üder Gehäuft Aufgetretene Varietäten der Halsmuskulatur an Einem Individuum. Acta Anatomica Nipponica 1941; 18: (in Japanese with German abstract). 16) Sekido K and Takahasi M. Unprecedented several examples of neck muscle other. Nihon Univ J med 1953; 12: (in Japanese). 17) Yamada H and Nishijima T. A rare case of abnormity in the M. omohyoideus. Kyushu-Shika-Gakkai-zasshi 1957; 11:1 2 (in Japanese with English abstract). 18) Yonekura S. A study of the muscles of the neck chest, abdomen and back in Japanese fetuses. Igakukenkyu 1954; 24: (in Japanese). 19) Takano T and Adati H. On the anomalies in the infra-hyoid muscles especially in the omohyoid muscle. Acta Anatomica Nipponica 1954; 29:5 6 (in Japanese). 20) Yamada H, kuga H and Ozumi K. Case report of abnormities in M. omohyoideus and M. sternothyreoideus. Kyushu-Shika-Gakkai -zasshi 1960; 14:390 (in Japanese with English abstract). 21) Sato Y, Oota Y and Yokota A. La anomalio de M. omohyoideus ĉe japanoj. Nihon Univ J med 1969; 28: (in Japanese with Esperant abstract). 22) Sato I, Kozu M, Onda S and Inokuchi S. Myofibrous organization of the anterior neck muscles (Mm. hyoidei). Showa Univ J Med Sci 1983; 43: (in Japanese with English abstract). 23) Murata H. Studies on the hyoid bone of Japanese people from viewpoint of individual identification. Jpn J Legal Med 1963; 17: (in Japanese with English abstract). 24) Houga T. Anthropological study measurement of a Japanese hyoid bone; Tokyo Dental College Kaibogakugyosekisyu 1957; 3:1 9 (in Japanese).

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