The Palatomaxillary Suture Revisited: a Histological and Immunohistochemical Study Using Human Fetuses
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Okajimas Folia Anat.Fetal Jpn., palatomaxillary 94(2): 65–74, August,suture 201765 The palatomaxillary suture revisited: A histological and immunohistochemical study using human fetuses By Ji Hyun KIM1, Masahito YAMAMOTO2, Hiroshi ABE3, Gen MURAKAMI2, 4, Shunichi SHIBATA5, Jose Francisco RODRÍGUEZ-VÁZQUEZ6, Shin-ichi ABE2 1Department of Anatomy, Seonam University College of Medicine, 439 Chunhyang-ro, Namwon, 55724, Korea 2Department of Anatomy, Tokyo Dental College, 2-9-18, Misaki-cho, Chiyoda-ku, Tokyo 101-0061, Japan 3Department of Anatomy, Akita University School of Medicine, 1-1-1, Hondo, Akita, 010-8543, Japan 4Division of Internal Medicine, Iwamizawa Asuka Hospital, 297-13, Iwamizawa, 068-0833, Japan 5Department of Maxillofacial Anatomy, Graduate School of Tokyo Medical and Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo, 113-8510, Japan 6Department of Anatomy and Human embryology, Institute of Embryology, Faculty of Medicine, Complutense University, Madrid, 28040, Spain –Received for Publication, May 9, 2017– Key Words: Palatomaxillary suture, transverse palatine fissure, palatine aponeurosis, maxilla, human fetuses Summary: In human fetuses, the palatine process of the maxilla is attached to the inferior aspect of the horizontal plate of the palatine bone (HPPB). The fetal palatomaxillary suture is so long that it extends along the anteroposterior axis rather than along the transverse axis. The double layered bony palate disappears in childhood and the transverse suture is formed. To better understand the development of the double layered bone palate, we examined histological sections obtained from 25 fetuses of gestational age 9–11, 16–18 and 30 weeks. The double layered palate was seen in all of the specimens exam- ined. Inferior angulation of the posterior end of the HPPB was evident at 9–11 weeks, but the initial palatine aponeurosis did not attach to the angulation but to a slightly anterior site. Both the maxilla and the HPPB were tightly attached to the vomer at 16–18 weeks. In both bones, bilateral plates met at the midline. The palatomaxillary suture was filled with short, randomly arranged collagen fibers. The nasal end of the suture was covered by a tight periosteum. Immunohistochemical examination of 3 fetuses at 16–18 weeks showed: 1) no expression of versican, tenascin-c or type II collagen in the suture; 2) few mitotic cells positive for proliferating cell nuclear antigen; 3) no or few CD34-positive developing vessels; and 4) no CD68-positive macrophages. These findings suggested that the fetal palatomaxillary suture was inactive for reconstruction and growth and that soft palate muscles likely did not contribute to the development of the double layered configuration. Introduction hood (Melsen and Melsen, 1982). The overlap between the maxilla and the HPPB corresponds to an oral area on In the human fetal hard palate, the palatine process of the medial side of the fifth deciduous tooth or the fourth- the maxilla is attached to the large inferior aspect of the fifth teeth in midterm fetuses (Kim et al., 2016a; Fig. 1). horizontal plate of the palatine bone (HPPB), forming The palatomaxillary suture is likely to contribute consid- a double-layered configuration. Thus, in contrast to the erably to palatal growth. morphology in adults, end-to-end contact between the Many studies have investigated the growth pattern HPPB and maxilla is unlikely in fetuses (Melsen, 1975; of the palate, a major interest among dentists and head Ishimaru, 1984; Fig. 1). A Japanese dentist might first surgeons (Melsen, 1975; Melsen and Melsen, 1982; Njio describe the supero-inferior overlapping of the bony and Kjaer, 1993; Silau et al., 1994; Sejrsen et al., 1996; plates in the human fetal palate (Kamaya, 1957). The fetal Rojvachiranonda et al. 2003). These studies provided a palatomaxillary suture is so long that it extends along the basis for understanding partial anomalies of the palate, anteroposterior axis rather than along the transverse axis. such as segmental odontomaxillary dysplasia (Becktor This double-layered bony palate is maintained until child- et al., 2002; Whitt et al., 2011). Less is known, however, Corresponding author: Masahito Yamamoto, DDS, PhD. Department of Anatomy, Tokyo Dental College, 2-9-18 Misaki-cho, Chiyoda-ku, Tokyo 101-0061, Japan. E-mail: [email protected] 66 J. H. Kim et al. Although soft palate muscles are likely to pull the HPPB posteriorly, they seemed not to push further upward than the palatine process of the maxilla. Another clue to under- standing the development of the double layered bony palate may be provided by the developing vomer, in that it may be tightly connected to the HPPB rather than the maxilla and pull the former upward. Examination of 62 fetuses of gestation age 9–24 weeks found that, in early stages, the vomer attaches inferiorly only to the maxilla, but that it later also attaches to the HPPB (Sandikcioglu et al., 1994). That study, however, did not evaluate the double layered bony palate. This study therefore utilized immunohistochemistry to re-examine the human fetal bony palate, with special reference to its close topograph- ical relationship to soft palate muscles as well as the vomer. Materials and Methods Specimens This study was performed in accordance with the pro- visions of the Declaration of Helsinki 1995 (as revised in Edinburgh 2000). Paraffin-embedded, frontal or sagittal sections of 25 fetuses were examined: 1) 10 of crown- rump length (CRL 45–70 mm) or approximate gestational age (GA) 9–11 weeks; 2) eight of CRL 125–170 mm or approximate GA 16–18 weeks; and 3) seven of CRL 250–270 mm or approximate GA 30 weeks. Frontal sections were prepared from 11 fetuses (three each of GA 9–11 and 16–18 weeks and five of GA 30 weeks), while sagittal sections were prepared from the other 14 fetuses (seven of GA 9–11 weeks; five of GA 16–18 weeks and two of GA 30 weeks). Fig. 1. Diagram showing differences between midterm fetuses and Previously, 15 specimens (seven of GA 9–11 weeks adults in the topographical anatomy of hard palate components. and six of GA 18–20 weeks) had been processed for Midsagittal plane of the hard palate. Panel A displays three bony sagittal or frontal sections. All of these fetuses were part elements in the fetal bony palate. A suture between the maxilla of the large collection kept at the Embryology Institute of (MX) and the horizontal plate (HP) of the palatine bone (i.e., a the Universidad Complutense, Madrid, being the products palatomaxillary suture) is arranged almost along the anteropos- terior axis due to overlapping of these two bony plates. Panel B of urgent abortion, miscarriage or ectopic pregnancy man- shows an adult suture lying almost along the supero-inferior axis. aged at the Department of Obstetrics of the University. Specimens were prepared as described (Kim et al., 2016a, b). Approval for the study was granted by the ethics commit- tee of the University (B08/374). The other midterm fetuses (three of GA 9–11 weeks and two of GA 16–18 weeks) were used for immunohis- about the double layered bony palate, such as whether the tochemical experiments. These fetuses had been donated bony deposition and reconstruction process starts in the by their families to the Department of Anatomy, Yanbian fetal palatomaxillary suture. University Medical College, Yanji, China, and their use A clue to understanding the development of the for research was approved by the university ethics com- double layered bony palate may be provided by the close mittee in Yanji (No. BS-13-35). These fetuses had been relationship of the HPPB with soft palate muscles. Specif- obtained by induced abortion, after which the mother ically, a developing muscle may mechanically stress the was orally informed by an obstetrician at the college HPPB via the palatine aponeurosis. Many studies have as- teaching hospital of the possibility of donating the fetus sessed the contribution of fetal masticatory muscles to the for research; no attempt was made to actively encourage growth of the mandibular condyle (Spyropoulos, 1977; the donation. After the mother agreed, the fetus was as- Öğűtcen-Toller and Juniper, 1993; Carranza et al., 2006). signed a specimen number and stored in 10% w/w neutral Fetal palatomaxillary suture 67 formalin solution for more than 1 month. Because of (HRP), with a dark brown color being positive. As neg- specimen number randomization, there was no possibility ative controls, specimens were incubated with normal of contacting the family at a later date. After dividing rabbit or mouse IgG (10 µg/ml) rather than primary each fetal body into parts, head samples were decalcified antibodies. Sections stained using the DAB method were by incubating them at 4°C in 0.5-mol/L EDTA (pH 7.5) counterstained with hematoxylin and were examined and solution (Decalcifying Solution B; Wako, Tokyo, Japan) photographed under a Nikon Eclipse 80 microscope. for 3–5 days, depending on the size of the sample. The head specimens were sectioned sagittally at 20 micron interval (thickness, 5 µm). Results All seven late stage fetuses (GA around 30 weeks) were part of a collection kept at the Department of Observations of frontal sections Anatomy, Akita University, Akita, Japan. They had been Frontal sections were obtained from 11 fetuses. A donated to the Department by their families during the double layered bony palate was seen in 23 of the 25 speci- period 1975–1985, and preserved in 10% w/w neutral for- mens, with the HPPB consistently attached to the superior malin solution for more than 30 years. The available data aspect of the posterior part of the maxilla and the inferior were limited to the date of donation and GA. There were part of the maxilla protruded medially.