Morphology of theOkajimas macaque Folia posterior Anat. superiorJpn., 93 (1):alveolar 5–13, canal May, 20165

A morphological study of the multi-posterior superior alveolar canals of in the Japanese macaque by cone-beam computed tomography

By

Yoko MIWA1, Masataka SUNOHARA1, Hiroshi ARAI1, 3, Tomonori ZAIZEN1, Kazuharu MINE2, Iwao SATO1

1Department of Anatomy, School of Life Dentistry at Tokyo, the Nippon Dental University, 1-9-20 Fujimi, Chiyoda-ku, Tokyo 102 -8159, Japan 2Department of Neurology, Gross Anatomy Section, Kagoshima University Graduate School of Medical and Dental Sciences, 8-35-1 Sakuragaoka, Kagoshima 890-8544 Kagoshima, Japan 3Department of Health Science, Faculty of Physical Education, International Pacific University, 721 Kannonji, Seto-chou, Higashi-ku 709-0863 Okayama, Japan

–Received for Publication, March 15, 2016–

Key Words: ; macaque; posterior superior alveolar canal, alveolar canals of maxilla, CBCT

Summary: The posterior superior alveolar canal (PSAC) composed of several canals which contains vessels and nerve in molar region of the maxilla of Japanese macaque. The PSAC of maxilla run to the . However, the PSAC and accessory canal (AC) of the maxilla in the Japanese macaque (JM) is unknown in morphological features in the maxilla. The purpose of this study was to describe the PSAC of the primates and to determine whether this structure could be used as a model for the human clinical condition. In this study, we showed the course of PSAC structure of the 23 JMs (male: n = 15; female: n = 8) using a cone-beam computed tomography apparatus. In the results, we classified a type to have one AC toward, a type to have two ACs toward, and three ACs in a type to have in PSAC. The main canal have some bony branch canals (BBCs) composed of 3 types (no BBC, one BBC, two BBCs). These canals and they run downward and supply to MS, these roots of maxillary molar region of the craniofacial skeleton in contrast to numerous small accessory canals with no nerve and vessels observed in the posterior regions in maxilla. These morphology features may give useful information about MS in dental treatment human model.

Introduction et al., 1999) of which is an important region for surgical treatments (Rosano et al., 2009). Moreover morpholog- Identifying appropriate structure for clinical treatment ical complex anastomoses information about PSAC and models of human craniofacial morphology is challenging. AC with a location of the PSAA gave an information for Suitable clinical animal model in morphological levels risk in clinically treatments in comparatively. Solar et al. need to match on phylogenetic in some cases which may (1999) have indicated the AC structure surrounding the determine when a more related animal is appropriate in PSAA in human. These AC structures near the MS have functional levels. However, comparatively little has been been large percentages appearances in previous studies published on primates other than humans in this field (Murakami et al., 1994; Elian et al., 2005; Mardinger except for the variation in the course of et al., 2007; Ella et al., 2008). The presence of the bony (IOC) (Zaizen and Sato, 2015). canals of the PSAA with AC may pose a risk during In human, the accessory cannls (ACs) was found surgical treatments with drilling the alveolar on (Kazkayashi et al., 2001, 2003). The infraorbital artery the MS. The IOA and PSAA have supplied to the MS in (IOA) and posterior superior alveolar artery (PSAA) monkey (Matsukawa, 1969). Therefore we need to gain formed complex anastomosis in the lateral and poste- information about PSAC for avoid clinical risks using rior regions in human maxilla (Traxler et al., 1999, Solar animal model. Previous reports indicated that the skull

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: [email protected] 6 Y. Miwa et al.

Fig. 1. The measurement points in the frontal view of a CBCT image of Japanese macaque. A, Height from the palatine plane to the superior mar- gin of the (HPP-SMO); width from the midline of the skull to the lateral margin of the orbit (WMS-LMO); width from the midline of the skull to the entrance of the PSAC (WMS-PSAC). B, The height from the palatine plane to the entrance of the PSAC (HPP-PSAC). Bar = 20 mm (A and B are the same size).

Fig. 2. The posterior superior alveolar foramen (PSAF) structures in the Japanese macaque maxilla using CBCT images. In left and right lateral views of maxilla, PSAF (black arrows) and some small accessory foramens (AFs) (white arrowheads) were found at (A–C). A, one PSAF; B, two PSAFs (PSAF1 and PSAF2), C, three PSAFs (PSAF1, PSAF2 and PSAF3). PSAC is located at upper region of the maxillary tuberosity. Bars = 2cm

form of primates paranasal sinuses (Koppe et al., 1999; course and supply of the PSSA in the molar region of the Rae and Koppe, 2003), development skull (Zumpano, maxilla. 2002; Zumpano and Richtsmeier, 2003) infraorbital canal We examined the morphology of the PSAC and AC in with ACs (Song et al., 2012). Therefore we need to gain the macaque to estimate clarify the course of PSAC information about PSAC for avoid clinical risks using relative to the MS using a cone-beam computed tomog- animal model. The bony region of PSAC in the maxilla raphy apparatus. is unknown in detail. Primate models were used in the study of the PSAC as morphology data to explain the Morphology of the macaque posterior superior alveolar canal 7

Fig. 3. The multi-posterior superior alveolar foramen (multi-PSAC) classified one canal (A, B), two canals (C, D), and three canals (E, F) in the maxillary tuberosity of the posterior region of the maxilla. The multi-PSAC classified to three types. A. Lateral view of type I (one BBC) ca- nal, B. Frontal view of type I (one AC) canal, C. Lateral view of type II (two ACs), D. Frontal view of type II (two ACs), E. Lateral view of type III (three ACs), F. Frontal view of type III (three As). The entrances of the PSAC (white arrows) were located in the superior region of the maxilla. Bars = 2cm 8 Y. Miwa et al.

Fig. 4. Type I of the posterior superior alveolar foramen (PSAC) at the frontal and sagittal section of the Japanese macaque skull. A, The entrance of the PSAC with no BBC (white arrows) at the top of the pterygomandibular space in the frontal section of type I. B, The entrance of the PSAC (arrows) at the top of the pterygomandibular space in the sagittal section of type I. C, The PSAC was almost connected to the maxil- lary sinus (MS) in the frontal section of the skull. D, The sagittal section of the alveolar bone of the skull. Bar = 2cm

Material and Methods in this study. Images of the IOC and surrounding struc- tures were acquired for the samples. The CBCT was oper- Animal preparation ated at a tube potential of 80 kV and a tube current of 4 This study was performed with 23 adult skulls of mA, and the scans acquired cylindrical areas of 41×40 the Japanese macaque (JM) (male 15, female 8), whose mm with high resolution (voxel size=0.1 mm). From the ages were estimated from their tooth eruption sequence three-dimensional CBCT images, the diameter of the (Iwamoto et al., 1987). These young adult macaques in IOC was measured using ASAHI vision software (Asahi collections were supplied for this study from the Depart- Roentgen Industry) and Micro AVS version 11 software ment of Neurology, Gross Anatomy Section, Kagoshima (KGT Industry, Tokyo, Japan). After identifying the University Graduate School of Medical and Dental median sagittal plane and the palatal plane, images are Sciences (Kagoshima, Japan) and the Department of defined by the anterior and posterior nasal spines perpen- Anatomy, School of Life Dentistry at Tokyo, the Nippon dicular to the median sagittal planes, as a reference plane, Dental University (Tokyo, Japan) the measurements described below were performed. The diameter of the skull was measured by ASAHI vision CBCT image (Asahi Roentgen Industry, Kyoto, Japan) and MicroAVS Cone beam computed tomography (CBCT) (PSR Version 11 (KGT Industry, Tokyo, Japan) software. The 9000N; Asahi Roentgen Industry, Kyoto, Japan) was used 3D images were produced by INTAGE Realia Profes- Morphology of the macaque posterior superior alveolar canal 9

Fig. 5. Type II of the posterior superior alveolar foramen (PSAC) at the frontal and sagittal section of skull. A, The entrance of the PSAC (arrow) and one BBC (arrow) at top of the pterygomandibular space in frontal section of type II.; B, The entrance of the PSAC (arrow) at top of thepterygomandibular space in sagittal section of type II.; C, PSAC (arrow) and BBC (arrowhead) were located beneath the maxillary sinus in frontal section of the skull; D, PSAC (arrow) was branched one BBC (arrowhead) at the same position of Fig. 5 in the sagittal section of the skull. Bar = 2cm

sional (KGT Industry, Tokyo, Japan) software. Statistical methods The measurement data were analyzed using Student`s Measurements t-test linear regression to correlate AMC, and PSAC. The The points measured in the CBCT images of the JM Pearson’s correlation coefficient was used to determine are shown in Figure 1. Four measurements for each skull the correlations. were made as follows: height from palatine plane to supe- rior margin of orbit (HPP-SMO), width from the midline of the skull to the lateral margin of the orbit (WMS- Results LMO) (see Zaizen and Sato, 2014). The height from pala- tine plane to entrance of PSAC (HPP-PSAC), width from CT images of the PSAC midline of the skull to entrance of PSAC (WMS-PSAC) In lateral view of maxillary tuberosity, numerous are measured (see Figs. 1A, B). Moreover, Index I small accessory foramens (AFs) were found of which (HPP-PSAC / HPP-SMO) / Index II (WMS-PSAC / they formed small bony canals (ACs) to the inside of the WMS-LMO) were measurements performed. body of maxilla (mean numbers 5.5 ± 2.2, Right, 5.6 ± 2.3; Left, 5.3 ± 2.0) by three dimensional structure using 10 Y. Miwa et al.

Fig. 6. Type III of the posterior superior alveolar foramen (PSAC) at the frontal and sagittal section of the skull. A, The entrance of the PSAC (ar- row) and two BBC (arrows) at top of the sagittal and frontal section of the maxilla. Bar = 5mm in white square. B, The PSAC (arrow) at top of the pterygomandibular space in sagittal section of type III; C, PSAC (arrow) and BBCs (arrowheads) were connected with maxillary sinus in frontal section of the skull. Bar = 4cm in C and Bar=1mm in magnified white square. D, PSAC (arrow) was branched one BBC (arrow- head) at the same position of Fig. 6C in the sagittal section of skull. Each square was shown large magnification of each figure.

CBCT images (Figs. 1A, B). This multi-PSAs also found 36.8%, ; 14/38, Right, 6 /14(31.6%); 8/14 Left (42.1%)), on the maxillary tuberosity of the maxilla; one foramen two BBCs (type III 3/38, 7.9%, Right, 1/3,5.3%; Left, 24/ 38 (63.2%), two foramens 13/38 (34.2%), three fora- 2/3, 10.5%) in the mid-facial region of the posterior of mens 1/38 (2.6%). That is, these multi-PSAs is composed the maxilla (see Figs. 3–7.) of main PSAC and no AC (one foramen case), one AC (two foramen case) and two ACs (three foramen case) The measurements data of PSAC JM (Figs. 2–6). Other small foramen are shown no clearly The measurements data of PSAC of JM are shown in developed canal structure in the inside of the maxillary Figs. 3. A significant correlation was detected between tuberosity. Index I and Index II (r = 0.206) in JM. Results indicate In side of the maxillary tuberosity, the canal forming significant gender differences were in Index I and Index bony branch canal (BBC) of the PSAC was mainly found II however no significant both side difference in JM (Fig. in the middle and anterior lateral regions of the MS 8). (Fig. 7). The PSAC mainly located lateral side (37/46: 80.4.0%) and a few inner side location (9/46: 19.6%) at PSAN morphology in the maxilla the MS of the maxilla. The bony canal structure of the The entrance of the PSAC appears at the pterygoman- PSAC was also classified as 3 types of courses by CBCT dibular space, this canal contained PSAA and PSAN, and images; no BBC (type I, 21/38, 55.3%; Right, 12/21 send out thin bony canal contained small blood vessel (63.2%); Left, 9 /21(47.4%)), one BBC (type II, 14/38, and nerve to the posterior or middle and anterior lateral Morphology of the macaque posterior superior alveolar canal 11

Fig. 7. Illustration of three type of bony branch canal of the posterior superior alveolar foramen (PSAC). The bony canal structure of the PSAC was classified as 3 types of courses by CBCT images (see Figs. 3–6). type I (no BBC); type II (one BBC); Type III (two BBCs: BBC1 and BBC2); MS, maxillary sinus,

region of the MS (Fig. 5). The nerves and blood vessels be forming complex communications in the maxilla passed through PSAC supply to the premolar and molar in same manner between human and macaque. There tooth. However these vessels and nerves run through is a need to examine the morphological properties of bony canal, and forming anastomosis to other neighbor AC of macaque if there is a potential corresponding to vessels and nerves from passed through IOC (Fig. 8). the bonny canals of human. That is using the macaque model to define the relationship between PSAC struc- ture and MS is also presented in clinical information. Discussion Especially, the molar region of the maxilla is difficult to plan surgical implantation of grafting bone to gain loca- The arterial supply to the wall of the MS indicated an tion of MS and PSAC. In general, the course of bonny important for surgical information such as MS augmen- canal was identified at the MS in human (55%, 114/208) tation and implantation of grafting bone. There is an (Mardinger et al., 2007). The maxillary vascular network anastomosis between the PSAA and infraorbital artery in of the lateral wall of the MS involves two arteries, the bonny canal of maxilla (Mardinger et al., 2007; Rosano infraorbital artery and the PSAA, which are connected et al., 2009; Song et al., 2012) and complex communica- via anastomoses in human (Solar et al, 1999; Traxler tions (Traxler et al., 1999; Solar et al., 2012) of human. et al., 1999). These anastomoses contribute to the sinus These ACs contained nerves and blood vessels may membrane of the anterolateral wall of the sinus. The AC 12 Y. Miwa et al.

Fig. 9. Scattergram of measurements data of dry skull. Index I (HPP- PSAC/HPP-SMO) and Index II (WMS-PSAC/WMS-LMO) were measured. Fig. 8. Macroscopic observation of the posterior superior alveolar artery (PSAA) and the posterior superior alveolar nerve (PSAN). The nerves and arteries that develop through the posterior supe- rior alveolar canal (PSAC) connected with other nerves and ar- In conclusion, JM maxilla is considered to be useful as teries. PSAA, posterior superior alveolar artery; PSAN, posterior superior alveolar nerve; IOA, infraorbital artery, and ION, in- a clinical risk model by the branches of the PSAC in spite fraorbital nerve, MA; maxillary artery, MSAA; middle superior of a number of ACs. alveolar artery, MSAN; middle superior alveolar nerve, PSAV; posterior superior alveolar vein. References

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