153Morphology of the multiple foramina of the macaque mandible

Introduction

Identifying the appropriate structure of clinical treat-ment models of human craniofacial morphology is chal-lenging. A suitable clinical animal model at the morpho-logical level should phylogenetically match, which may determine when a more related animal is appropriate on the functional level (Bradley and Kincaid, 1974). In humans, numerous accessory foramina are found in various regions of the mandible (Sutton, 1974). Consid-ering the morphological properties, many previous reports have indicated a clinical risk for the existence of foramina (Fanibunda and Matthews, 1999, 2000; Katakami et al., 2009; Kaufman et al., 2000; Kawai et al., 2007; Liang et al., 2004, 2006, 2007; Rosano et al., 2009; Yoshida et al., 2005). These foramina are present in the internal, inner surfaces of the posterior and ante-rior regions of the mandible (Chapnick, 1980; Fani-bunda and Matthews, 1999, 2000; Haveman and Tebo, 1976; McDonnell et al., 1994; Ossenberg, 1987; Casey, 1978; Barker and Locket, 1972). During aging, the

A morphological study of the foramina of the mandible inthe Japanese macaque by cone-beam computed tomography

By

Masataka SUNOHARA, Yoko MIWA, Iwao SATO

1Department of Anatomy, School of Life Dentistry at Tokyo, The Nippon Dental University,1-9-20 Fujimi, Chiyoda-ku, Tokyo 102 -8159, Japan

–Received for Publication, January 20, 2016–

Key Words: CBCT, skull, macaque, mental foramen, lingual foramen

Summary: The mandibular canal (MC) contains vessels and nerves in the mandible of the Japanese macaque (JM). The inferior alveolar nerves and vessels of the mandible insert from the mandibular foramen and then run through the MC, the mental foramen and spinal foramen to the outside of the mandible. However, the detailed morphological properties of multiple canals, such as the accessory canal (AC) of the mandible, are unknown in JMs. The purpose of this study was to describe the multiple canals of JMs and to determine the location and analyse the measurements of the JM mandible. In this study, we also showed the course of the lingual foramen in 17 JMs (male: n = 8; female: n = 9) using cone-beam computed tomography (CBCT). In our results, we classified multiple mental foramina and multiple lingual foramina found on the mandibular body at the premolar or molar region. However, there was no significance between the formation of mandibular properties and the lingual foramen. These multiple foramina contain nerves and blood vessels have a few branched canals; these branches run downward and connect with the inferior mandibular nerve and artery. These morphological features may provide useful information about surgical treatment of the alveolus in a human model.

number of ACs differ among adults, infants, and foetuses (Przystańska and Bruska, 2012). Specifically, lingual ACs are related to dental crypts (Shiozaki et al., 2014). These numerous canals are called ‘gubernacular canals’ in the crab-eating monkey (Minegishi, 1981). These struc-tures were also related to tooth eruption from deciduous teeth to permanent teeth during development. Moreover, the arrangement of vessels is complex and composed of four courses in the rhesus monkey mandible (Castelli and Huelke, 1965). However, comparatively little has been published on primates other than humans in this field except for the variation in the course of ACs and foramina. Therefore, we require further information about ACs to avoid clinical risks using animal models such as primates, which resemble humans. Therefore, we sought to gain detailed information about the bony region of ACs in the macaque mandible.

Okajimas Folia Anat. Jpn., 93(4): 153–158, February, 2017

Corresponding author: Iwao Sato, PhD., Department of Anatomy, School of Life Dentistry at Tokyo, The Nippon Dental University 1-9-20 Fujimi, Chiyoda-ku, Tokyo 102-8159, Japan. E-mail: iwaoa1@tokyo.ndu.ac.jp

154 M. Sunohara et al.

Materials and Methods

Animal preparationThis study was performed with 17 adult skulls of

the Japanese macaque (JM) (male 8, female 9), whose ages were estimated from their tooth eruption sequence (Iwamoto et al., 1987). These young adult macaques in collections were supplied for this study from the Depart-ment of Neurology, Gross Anatomy Section, Kagoshima University Graduate School of Medical and Dental Sciences (Kagoshima, Japan) and the Department of Anatomy, School of Life Dentistry at Tokyo, The Nippon Dental University (Tokyo, Japan).

CBCT imagingCone beam computed tomography (CBCT) (PSR

9000N; Asahi Roentgen Industry, Kyoto, Japan) was used in this study. Images of the mandible were acquired for the samples. The CBCT was operated at a tube poten-tial of 80 kV and a tube current of 4 mA, and the scans acquired cylindrical areas of 41 × 40 mm with high resolution (voxel size = 0.1 mm). From the three-di-mensional CBCT images, the diameter of the mandible was measured using ASAHI vision software (Asahi Roentgen Industry) and Micro AVS version 11 software (KGT Industry, Tokyo, Japan). Images were defined by the mandibular plane as a reference plane, and the measurements described below were performed. The diameter of the skull was measured by ASAHI vision (Asahi Roentgen Industry, Kyoto, Japan) and Micro-AVS Version 11 (KGT Industry, Tokyo, Japan) software. The 3D images were produced by INTAGE Realia Profes-sional (KGT Industry, Tokyo, Japan) software.

MeasurementsThe points measured in the CBCT images of the

mandible are shown in Fig. 1. We identified the multiple foramina with canals connected to the MC in the inner and outer surface of mandible. Ten measurements for each mandible were made as follows: the distance from the gonion to the condyle (LG-Co), the width of the mandibular branch (WMB-Co) (both condyle distance), the distance from the mandibular foramen to the condyle (LMAF-Co), the distance from the mental foramen to the condyle (LMEF-Co), and the distance from the lingual foramen to the condyle (LIF-Co). The height from the mandibular plane to the condyle (HMAP-Co), HMP-MAF, the height from the mandibular plane to the entrance of the mandibular foramen, the height from the mandibular plane to the entrance of the mental foramen (HMAP-MF), and the height from the mandib-ular plane to the entrance of the lingual foramen (HMAP-LF) were also measured (see Figs. 1A–C). Moreover, Index 1 (LMAF-Co/LG-Co×100), Index 2 (LMEF-Co/LG-Co × 100), Index 3 (LIF-Co/LG-Co × 100), Index 4 (HMAP-MF/HMAP-Co × 100), and Index 5 (HMAP-LF/

HMAP-Co × 100) were measured (Fig. 1).

Statistical methodsThe measurement data were analysed using Student’s

t-test and linear regression to correlate the right and left sides. Pearson’s correlation coefficient was used to deter-mine the correlations. Index data were converted to the arcsine-transformed proportion, before calculating Pear-son’s correlation coefficient.

Results

CT images of the mental and lingual foramina In the lateral view of the mandible, some small mental

foramina were found. They formed small bony canals (ACs) on the inside of the MC according to three-di-mensional CBCT images (Figs. 1A, B). These multiple mental foramina were found on the mandibular body at the premolar portion; one foramen 1/34 (63.2%), two foramina 2/34 (34.2%), and three foramina 3/34 (2.6%) (Figs. 2A–C). That is, these multiple foramina were composed of the main MC (one foramen), two foramina and three foramina. Other small foramina were not shown with clearly developed canal structures connected with the MC (Fig. 2).

The bony canal of the mental foramen was mainly found in the premolar region of the mandible (Fig. 2). In contrast, the lingual foramen was mainly located at the first molar location (10/34: 29.4%), second molar location (12/34: 35.3%), second premolar location (4/34: 11.8%) and third molar location (3/34: 8.8%) in the mandible. The number of lingual foramina (LF) was classified into six types: single foramen (17/34, 50.0%), two multi-ca-nals (6/34, 17.6%), three multi-canals (7/34, 20.6%), four multi-canals (2/34, 5.9%), five multi-canals (1/34, 2.9%), and six multi-canals (1/34, 2.9%). The running struc-ture of the LF was classified into three patterns: canals running at right angles to the MC (8/34, 23.5%), a canal running towards the anterior (7/34, 20.6%), and a canal running posterior (19/34, 55.9%).

The measurement data of the mandibleThe measurement data of the mandible of JM are

shown in Table 1 (see Figs. 1A, B). A significant correla-tion was detected between the WMB-Co and LG-Co (r = 0.655, p < 0.01), the WMB-Co and HMAP-MF (r = 0.531, p < 0.01), the LGCo and LMAF-Co (r = 0.544, p < 0.01), the LG-Co and LMEF-Co (r = 0.519, p < 0.01), LMAF-Co and WMB-Co (r = 0.532, p < 0.01), and LMEF-Co and LMAF-Co (r = 0.432, p < 0.05) in the mandible of JM.

A significant correlation was detected between Index 2 and Index 4 (r = 0.891, p < 0.01), Index 3 and Index 5 (r = 0.917, p < 0.01), and Index 1 and Index 2 (r = 0.397, p < 0.01) in the mandible of JM. Measurement data were

155Morphology of the multiple foramina of the macaque mandible

not significantly different between genders in JM.

The morphology in the mandibular, mental and lingual canals

The entrance of the lingual foramen appears at the superior part of the sublingual fossa. This canal contained the submental artery and mylohyoid nerve and sent out MC contained with the inferior alveolar nerve and artery (Fig. 2). However, these vessels and nerves run through the bony canal and form an anastomosis to other neigh-boring vessels and nerves (Fig. 3).

Discussion

Lingual foramenThe lingual foramen is related to dental crypts

connected to deciduous tooth crypts or MC in the human fetal mandible (Shiozaki et al., 2014). Our macaque results indicated that all of our LFs connected with MC and no submandibular canal existed compared to that of three MCs. Although the morphological features of the LF seen in the human embryonic period could not be compared with adult monkeys, the presence of at least the lingual foramen in the macaque occurs in the infe-rior alveolar artery and the inferior alveolar nerve before ossification of the mandible occurs in the macaque. These branches of the inferior alveolar nerve and artery should

Fig. 1. The measurement points in a CBCT image of a JM. A, Outer view of the cranial base: LG-Co, length from the gonion to the condyle; WMB-Co, width of the mandible (WM-Co) (both condyle distances); LMEF-Co, distance between the mental foramen and condyle; LIF-Co, distance between the lingual foramen and condyle (see Fig. 1A). B, Lateral view of the cranial base: HMAP-Co, height from the man-dibular plane to the condyle; width of the mandibular branch (WMB-Co); HMAP-MF; C, height from the mandibular plane to the entrance of the mandibular foramen; HMAF-Co, height from the mandibular plane to the entrance of mental foramen; HMAP-LF, height from man-dibular plane to the entrance of the lingual foramen (see Fig. 1B). bar = 50 mm (A, B and C are the same size).

156 M. Sunohara et al.

have made many connections with the submental artery and the mylohyoid nerve amongst each other. That is, these blood vessels and nerves are confined in the bone during the process of bone formation, and the surround-ings are thought to be a bony canal. Because our macaque

results indicated that multiple mental foramina connected with an MC containing an artery and nerve and no-multi MCs were present in the macaque mandible, even though the human fetal mandible has multiple mandibular canals. The process of formation of multi-canals was supported by Chavez-Lomeli et al.’s report (Chávez-Lomeli et al., 1996). Moreover, our multiple lingual canals differed from numerous lingual small foramina mainly found in the lingual alveolar bone around teeth in beagles (Cahill, 1974) and macaque mandibles (Minegishi, 1981). In our results, there were no subernacular canals at the supe-rior part of the sublingual fossa as found in crab-eating monkeys (Minegishi, 1981). Therefore, it is possible that this characteristic is transient; that is, these structures are related to tooth eruption from the deciduous tooth to the permanent tooth during development, but they then disap-pear at the adult stage.

Table 1. The measurements data of mandible of JM.

Measurement points mean ± SD

HMAP-CoWMB-Co

LG-CoLMAF-CoLMEF-CoHMAP-MF

LIF-CoHMAP-LF

21.55 ± 2.6020.32 ± 1.7258.45 ± 4.709.70 ± 0.8840.82 ± 4.514.54 ± 4.8427.85 ± 7.495.76 ± 2.24

(mm)

Fig. 2. The foramen and canal structures of the MJ mandible using CBCT images A, In the right lateral view of the mandible, three mental foram-ina (arrows) were found on the surface of the premolar region. B, In the right inner lateral view of mandible, four lingual foramina (LFs) (ar-rows) were found at the sublingual fossa from the premolar to molar regions. Moreover, the mandibular foramen (MAF) (arrow) was located at the middle region of the inner surface of the mandibular branch. C, In a series of the frontal section of the TM head, the root of the lingual canal was found as small holes (arrows) in each section. A, B, bar = 2 cm, C, bar = 5 cm.

157Morphology of the multiple foramina of the macaque mandible

The correlation between the lingual foramen and other measurement data from the JM mandible

In our measurement data from CBCT, the length of the mandible correlated with the mental foramen and mandibular foramen and the width of the mandibular condyle, which indicated that the mandible elongated in a posterior direction during mandible development in JM. During the formation of the mandible, a complex pattern of resorption and formation in each region of the human mandible is evident (Enlow, 1996). Specifically, the human mandible undergoes lengthening of the posterior region of the corpus, and then the ramus and the molar region elongate with lateral growth to the ramus, condyle and coronoid region (Enlow, 1996; Martinez-Maza et al., 2013). Therefore, the location of the mandibular foramen and mental foramen were also reflected by the elongated mandible length during development in JM, as in the human mandible (Enlow, 1996). However, the location of the LF was not significant from other measurement data. Therefore, the LF was already in the molar tooth region before bone formation, and its position may not be influ-enced by mandible bone formation and development in JM.

Comparison with humans and JM lingual foramina in different locations

In the human mandible, many previous reports indi-cated the LF (Fanibunda and Matthews, 1999, 2000; Katakami et al., 2009; Kaufman et al., 2000; Kawai et al.,

2007; Liang et al., 2004, 2006, 2007; Rosano et al., 2009; Yoshida et al., 2005). These foramina were also present at various locations in the internal, inner surfaces of the posterior and anterior regions of the mandible (Chapnick, 1980; Fanibunda and Matthews, 1999, 2000; Haveman and Tebo, 1976; McDonnell et al., 1994; Ossenberg, 1987; Casey, 1978; Barker and Locket, 1972). Specifi-cally, these ACs are mainly found on the internal surface of human mandible (Chapnick, 1980; Fanibunda and Matthews, 1999, 2000; Haveman and Tebo, 1976; Sutton, 1974; Przystańska and Bruska, 2012; McDonnell et al., 1994; Ossenberg, 1987; Zivanović, 1970; Carter and Keen, 1971; Casey, 1978; Barker and Locket, 1972). In our results, the lingual foramina were found on the outer and inner surfaces of the mandible. The LF and multiple lingual canals were present on the outside and inside of the mandible. In rhesus monkeys, the external carotid system is very complex, and there are four pathways of supplied vessels to the mandible: the temporal muscle, temporomandibular joint, inferior alveolar artery, and alveolar dental artery (Castelli and Huelke, 1965). These vessels insert into the mandible with four origin direc-tions, which may be related to the existence of numerous accessory foramina in the JM mandible. However, the locations of lingual foramina were similar to those of the human mandible in our results. Previous reports indicated that modifications in the technique for alveolar surgery need to model animal research (Bradley and Kincaid, 1974). In conclusion, the JM mandible is considered to be

Fig. 3. Macroscopic observation of mylohyoid nerve and submental artery. The mylohyoid nerve branch (N) (black arrow) run through the man-dibular branch and are inserted into the premolar region of the inner mandibular body. The fine blood vessel of submental artery (BV) (white arrows) inserted into the mandibular body. Man; mandible, MM; mylohyoid muscle, bar = 2 cm

158 M. Sunohara et al.

useful as a clinical risk model by the branches of the LF using CBCT analysis with a non-destructive model.

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