Innervation of the human upper primary dentition: Implications for understanding tooth initiation and rethinking growth and eruption patterns

Recent comparisons of humans with apes and early fossil hominids have prompted renewed interest in the study of sequences of dental growth and development. Such comparisons, however, rely on certain assumptions about tooth development and dental homology and the biological reality of distinguishing “deciduous” from “permanent” teeth. In light of earlier suggestions by Schwartz that there might be a correlation between nerves and the stem progenitors of tooth classes, and thus between nerve branch number and number of tooth classes, we studied a large sample of ～ 3 month fetuses to elucidate the nature of nerve branching patterns and the development of the primary dentition (i.e., the “deciduous” incisors, canine, and molars, and the first “permanent” molar). Contrary to expectation, variation in nerve branch patterning was the rule. If nerve fibers do have a role in tooth development, it can only be at the time of initiation, with definitive innervation occurring late in tooth development. In taking into consideration the entire span of tooth development—from initiation to innervation to eruption—and the process by which successional teeth arise (each from the external dental epithelium of a predecessor tooth), we suggest that dividing tooth growth and eruption into patterns of the “deciduous” teeth vs. those of the “permanent” is artificial and that a more meaningful approach would be the study of the entire dentition.     

Dental development and life history in Anapithecus hernyaki

The sample of Anapithecus from Rudabánya, Hungary, is remarkable in preserving a large number of immature individuals. We used perikymata counts, measurements of root length and cuspal enamel thickness, and observations of the sequence of tooth germs that cross match specific developmental stages in Anapithecus to construct the first composite picture and time scale for dental development in a pliopithecoid (Catarrhini, Primates). We conclude that the age of eruption of M1 in Anapithecus was similar to various macaque species (approximately 1.45 months), but that M2 and M3 emergence were close to 2.2 and 3.2 years, respectively (both earlier than expected for similarly sized cercopithecoids). There may have been little difference in individual tooth formation times between cercopithecoids and Anapithecus, but the degree of molar overlap during M1, M2, and M3 crown development, which is extreme in Anapithecus, is fundamentally different. Overall dental development in Anapithecus was very rapid. Old World monkeys appear derived in lacking significant molar overlap, and hominoids may be derived in having longer tooth formation times, both resulting in longer overall dental development times. This is consistent with the general conclusion that the Pliopithecoidea is an outgroup to the Cercopithecoidea and the Hominoidea. On the other hand, rapid dental formation in Anapithecus may be an apomorphy indicative of an unusually rapid life history or unique pressures related to diet and maturation. Folivory and/or predation pressure may be responsible for generating selection to more rapidly erupt permanent teeth and possibly attain adult body masses in Anapithecus. Whatever the case, Anapithecus, with an M3 emergence of approximately 3.2 years, is dramatically faster than any extant catarrhine of similar body mass. This represents yet another unusual attribute of this poorly known fossil catarrhine.     

Schultz's unruly rule: dental developmental sequences and schedules in small-bodied, folivorous lemurs

Schultz's rule (as reconstructed by Smith) states that there is a relationship between the pattern (or relative order) of eruption of molar versus secondary (replacement) teeth and the overall pace (or absolute timing) of growth and maturation. Species with 'fast' life histories (rapid dental development, rapid growth, early sexual maturation, short life spans) are said to exhibit relatively early eruption of the molars and late eruption of the secondary replacement teeth (premolars, canines, incisors), whereas species with 'slow' life histories are said to exhibit relatively late eruption of the molars and early eruption of the secondary dentition. In a recent review, B.H. Smith noted that primates with tooth combs might violate this rule because tooth combs tend to erupt early, regardless of the pace of life history. We show that exceptions to Schultz's rule among lemurs are not limited to the relative timing of eruption of the tooth comb. Rather, among lemurs, some species with extremely accelerated dental development exhibit a pattern of eruption of molars and of secondary teeth in direct opposition to the expectations of Schultz's rule. We focus particularly on the pattern (order) and pace (absolute timing) of dental development and eruption in Avahi and Lepilemur - two relatively small, nocturnal folivores with rapid dental development. These taxa differ markedly in their eruption sequences (the premolars erupt after M2 and M3 in Lepilemur but not Avahi ). We offer an explanation for the failure of Schultz's rule to predict these differences. Schultz's rule presumes that eruption timing is dependent on the size of the jaw and that, therefore, molar crown formation and eruption will be delayed in species with slow-growing jaws. We show that a variety of processes (including developmental imbrication) allows the crowns of permanent teeth to form and to erupt into jaws that might appear to be too small to accommodate them.     

Preliminary investigation of dental microstructure in the Yuanmou hominoid (Lufengpithecus hudienensis), Yunnan Province,China

Fieldwork in the Yuanmou Basin of southern China has uncovered a large assemblage of late Miocene hominoid fossils assigned to Lufengpithecus hudienensis. Two mandibular first molars from this species were made available for histological analysis as part of a larger ongoing study on the ontogeny of dental development in Miocene to Recent hominoids. Results are compared with published and unpublished data on tooth growth in a wide range of extant and extinct hominoids. The Yuanmou molars are smaller than those of Lufengpithecus lufengensis and have markedly shorter crown formation times, overlapping slightly with Pan, but most similar to Proconsul and Dryopithecus. In other aspects of molar development (including enamel extension rates and enamel thickness), L. hudienensis shows similarities with all extant hominoids, in particular, Pongo. Ultimately, charting the ontogeny of molar crown formation may help shed light on the relationship of Lufengpithecus hudienensis to orangutans, and other Miocene to Recent hominoids.     

Formation of a successional dental lamina in the zebrafish (Danio rerio): support for a local control of replacement tooth initiation

In order to test whether the formation of a replacement tooth bud in a continuously replacing dentition is linked to the functional state of the tooth predecessor, I examined the timing of development of replacement teeth with respect to their functional predecessors in the pharyngeal dentition of the zebrafish. Observations based on serial semithin sections of ten specimens, ranging in age from four week old juveniles to adults, indicate that (i) a replacement tooth germ develops at the distal end of an epithelial structure, called the successional dental lamina, budding off from the crypt epithelium surrounding the erupted part of a functional tooth; (ii) there appears to be a developmental link between the eruption of a tooth and the formation of a successional dental lamina and (iii) there can be a time difference between successional lamina formation and initiation of the new tooth germ, i.e., the successional dental lamina can remain quiescent for some time. The data suggest that the formation of a successional lamina and the differentiation of a replacement tooth germ from this lamina, are two distinct phases of a process and possibly under a different control. The strong spatio-temporal coincidence of eruption of a tooth and development of a successional dental lamina is seen as evidence for a local control over tooth replacement.     

The cytology of the dental follicle and adjacent alveolar bone during tooth eruption in the dog

Previous studies from our laboratories have shown that premolar eruption in dogs depends upon the presence of the dental follicle and is independent of root or crown growth or attachment to the oral epithelium. The present study is an analysis of the cellular composition of the dental follicle and the cellular investment of the adjacent walls of the bony crypt before and during eruption of the third and fourth mandibular permanent premolars in young beagle dogs. Four premolar follicles and their adjacent bony crypts were examined at 2-week intervals over 12 weeks before and during eruption of these teeth. Tissues were removed, fixed, processed, and oriented so that each follicle and the adjacent crypt wall could be reproducibly examined in vertical and horizontal planes. Mononuclear cells with abundant cytoplasm, euchromatic nuclei, and prominent nucleoli were present in juxtavascular location in the coronal part of the dental follicle; and these cells increased in number immediately preceding and during tooth eruption in parallel with an increase in osteoclasts on the adjacent crypt wall. These data are interpreted to mean that the coronal part of the dental follicle may coordinate the alveolar bone resorption required for tooth eruption by attracting and directing to the crypt wall a population of mononuclear cells, which either become osteoclasts and/or direct osteoclastic activity during tooth eruption.     

Increasing human tooth length between birth and 5.4 years

Most previous studies of tooth development have used fractional stages of tooth formation to construct growth standards suitable for aging juvenile skeletal material. A simple alternative for determining dental age is to measure tooth length throughout development. In this study, data on tooth length development are presented from 63 individuals of known age at death, between birth and 5.4 years, from an archeological population recovered from the crypt of Christ Church, Spitalfields, London. Isolated developing teeth (304 deciduous, 269 permanent) were measured in millimeters and plotted against individual age. Regression equations to estimate age from a given tooth length, are presented for each deciduous maxillary and mandibular tooth type and for permanent maxillary and mandibular incisors, canines, and first permanent molars. Data on the earliest age of root completion of deciduous teeth and initial mineralization and crown completion of some permanent teeth in this sample are given, as well as the average crown height and total tooth length from a small number of unworn teeth. This method provides an easy, quantitative and objective measure of dental formation appropriate for use by archeologists and anthropologists. © 1993 Wiley-Liss, Inc.     

The developing dentition and tooth structure in hominoids

This review of hominoid dental development is presented in two parts. The first section reviews (1) the general relationship between dental development and life history in hominoids; (2) the methods used to document dental development, and (3) the nature of incremental growth markings in hominoid teeth. The second section builds on this and reviews the contributions to hominoid dental development that have been made by (1) studies of tooth emergence; (2) studies of tooth calcification stages, and (3) histological studies of incremental growth markings made either from sections of teeth or replicas of early hominid teeth prepared for scanning electron microscopy.     

The eruption times of permanent teeth in boys and girls in the Stormarn District, Schleswig-Holstein (Germany)

In a longitudinal study in two small towns in southern Schleswig-Holstein (Ammersbek and Ahrensburg, District Stormarn; 9155 inhabitants) we investigated 2832 oral findings of 1396 patients (711 males, 685 females). The minimum age was 1.51 years, and the maximum age was 25.50 years. The dental findings were collected over a period of about 20 years (1982-2002). The oral findings per child were assessed between one and eight times. The eruption times of teeth in females are earlier than those for the same teeth in males. Further, the permanent dentition in females is completed earlier than in males. In both sexes the tooth eruption occurs symmetrically in both jaws. The comparison of both jaws revealed a slightly advanced eruption of the lower jaw teeth in both sexes. There is a noteworthy change in the eruption sequence of the teeth. In contrast to other reports we observed that the eruption of the canine proceeds the eruption of the second molar. We found no acceleration of the dentition when compared with other reports and could confirm the rules of tooth eruption in man. Conclusion: Oral examination of teeth is a simple tool to calculate tooth eruption intervals. This first investigation on a population of Schleswig-Holstein revealed a change in the eruption sequence of permanent teeth. These findings are relevant for dental treatment planning and should be reconfirmed at certain intervals.     

Masculinization of the eruption pattern of permanent mandibular canines in opposite sex twin girls

The aim of this study is to explore the effect of prenatal androgenization on the clinical eruption of permanent teeth expressing dimorphism and bimaturism. The eruption curves of permanent teeth (except third molars), including those that make up the canine complex (permanent canines, lower first premolars), are compared among opposite sex twins (OS twins) relative to single‐born boys and girls. The comparisons are made with regard to three phases of eruption (pierced mucosa, half‐ erupted, and completely erupted) from a cross‐sectional sample of dental casts, using Kaplan–Meier survival and Cox regression analyzes. The casts were collected from 2159 school children from the US Collaborative Perinatal Project, including 39 pairs of OS‐twins, of which 12 pairs (30.8%) were Euro‐Americans and 27 pairs (69.2%) were of African‐American ancestry. The eruption patterns of the incisors, upper first molars, and lower canines were found to be significantly masculinized (delayed) among OS twin girls. The differences in most other teeth were either not significant, or the number of observations of active eruption phases were too few, such as in the upper first molars and incisors, to yield strong evidence and meaningful results. The masculinization of the tooth eruption pattern in OS twin girls is intriguing because of the lower canine responses during puberty, as well as canine primordial formation during early fetal androgenization of their co‐twin during the 8th to 14th gestational weeks. The present results offer a challenge for future research exploring tooth eruption mechanisms, and may also highlight some cases of delayed or ectopic canines, which are biased toward females. Am J Phys Anthropol 151:566–572, 2013. © 2013 Wiley Periodicals, Inc.     

许家窑人幼年个体的釉质发育缺陷

上世纪70年代在许家窑-侯家窑地点发现的人类化石对了解东亚中晚更新世过渡时期古人类的形态演化起到了重要作用。除形态特征外,针对许家窑人病理表现也开展过相关研究,其中许家窑人幼年个体前部牙齿上出现的黄色小坑被认为是患有氟斑牙病的证据,且可能代表世界范围内该牙病的最早实例。然而,经电子显微镜和显微断层扫描显示,这些黄色小坑或凹陷是釉质发育不良表现,而不是代表个体患有氟斑牙病后牙齿受咀嚼压力而产生的物理破损。同步辐射扫描显示,许家窑幼年个体前部牙齿釉质密度均匀,没有出现浅层釉质矿化减小的现象,不支持该个体因釉质矿化过程受影响而患有典型氟斑牙的结论。尽管如此,后部牙齿上大量坑状的釉质缺陷和坑状缺陷底部的加重生长线特征不排除是个体氟摄入过量而影响釉质形成的分泌期而导致的。除表面坑状釉质缺陷外,许家窑幼年个体恒齿不同部位的釉质内部出现缺失（空间结构一般为圆球状）。缺失主要集中在浅层区域,沿齿尖-齿颈方向的密集程度变化与釉质发育不良位置具有一定相关性。釉质内部缺失有时互连并与釉质表面垂直。以上特征显示釉质内部缺失是釉质形成过程受影响所致,且影响因素和发生机理可能与釉质发育不良的类似。许家窑幼年个体不同牙齿在外部釉质缺陷和内部釉质缺失密集程度上的差别可能反映的是个体在发育过程中所需应对的外界扰动因素程度不同。未来研究可对包含许家窑人化石的堆积物中以及许家窑人牙齿中的氟含量进行测定,以进一步研究许家窑人个体的生活环境中是否有过量的氟以及许家窑人是否摄入了过量氟元素,从而对许家窑人的牙齿发育缺陷机理有一个进一步的了解。     

MT1-MMP expression in the odontogenic region of rat incisors undergoing interrupted eruption

MT1-MMP (membrane type matrix metalloproteinase-1) has been considered an important membrane-type matrix metalloproteinase involved in the remodeling process in tissue and organ development, including the processes of the tooth and root growth and dental eruption. Therefore, the aims of this study were to evaluate MT1-MMP expression in the odontogenic region, as well as the eruption rate and morphology of the lower-left rat incisor, where the eruption process was interrupted for 14 days by a steel wire attached from the center of the incisor labial face and braced to the first molar. In the interrupted eruption group, the eruption rate was significantly reduced, producing drastic morphological alterations in the tooth germ and socket area. The MT1-MMP expression was widespread in the dental follicle, in both groups studied (normal and interrupted eruption groups); however a significant decrease in immunostaining was observed in the interrupted eruption group. Results indicate that MT1-MMP may have an important role in the process of dental eruption.     

Ultrastructure of alveolar bone during tooth eruption in the dog

Previous work from our laboratories has established that eruption of the permanent mandibular premolars in dogs is dependent upon the presence of the dental follicle and that it involves resorption of alveolar bone and the roots of the deciduous predecessor above and formation of alveolar bone below the developing crown. This study illustrates the topography of the bone surfaces of the crypt by scanning electron microscopy and the ultrastructure of the cells on alveolar bone surfaces during tooth eruption. Above the developing crown where the eruption pathway forms, the bone surface is a pitted sheet, the characteristic topographic feature of bone resorption; between the crown and the mandibular canal, the bone surface has numerous interconnecting trabeculae. Transmission electron microscopy of bone cells lining the eruption pathway area of the crypt showed numerous osteoclasts with adjacent mononuclear cells. Both cell types contained specific, membrane-bound cytoplasmic vesicles shown by the work of others to be characteristic features of osteoclasts and their precursors. Basal trabeculated bone in the crypt was covered by plump osteoblasts. These data show that the metabolic events in alveolar bone associated with tooth eruption have the appropriate cellular and bony surface correlates and that the suspected control of alveolar bone resorption by the dental follicle may be mediated by its recruiting and directing to adjacent bone surfaces the mononuclear precursors of osteoclasts.     

From Embryo to Adult: The Complete Development and Unusual Replacement of the Dentition of the Tammar Wallaby (Macropus eugenii)

Unlike their reptile-like ancestors with continuous tooth replacement, mammals have evolved to replace each tooth either only once, or not at all. In previous large-scale comparative studies, it has been suggested that this tooth replacement only occurs from a successional dental lamina produced lingually to the primary tooth. This study aims to document the complete tooth development and replacement pattern of the tammar wallaby (Macropus eugenii). The tammar wallaby is a diprotodont marsupial, a group defined by their two procumbent lower incisors. To provide a comprehensive documentation of the spatio-temporal pattern of tooth development, we used Lugol’s Iodine staining and microCT scanning (diceCT) of embryos and pouch young into adulthood, resulting in high resolution 3D models for both soft and mineralised stages of development for all tooth positions. Our results reveal that the eponymous lower incisors are the successional generation at the third incisor locus, where the primary dentition initiates but never erupts. Furthermore, we track the development of the only replacement tooth, the permanent third premolar (P3), from initiation to eruption, and found it develops from the primary dental lamina, mesial to the dP3. This is contrary to the conventional view of lingual replacement from successional lamina in mammals. Our findings indicate that no functional tooth replacement occurs in the tammar wallaby, and expands the diversity of tooth replacement patterns found in mammals. We also conclude that since almost all marsupial and placental mammals produce replacement teeth from the distalmost deciduous premolar, this tooth should be considered homologous in these two groups.

     

A reconsideration of the Archi 1 Neandertal mandible

A reassessment of the early last glacial immature Neandertal mandibular corpus from Archi indicates a series of features in which it closely resembles other pre-adolescent Neandertal mandibles and contrasts with those of similarly aged recent humans. These are in the context of a re-aging of the specimen to ca. 3 years on the basis of deciduous dental eruption and attrition and permanent dental calcification. The Archi 1 mandible resembles other immature Neandertals in having a “retreating” symphyseal profile in the context of moderate development of mental trigone features. It is relatively robust in the development of lateral and basilar corpus features and some increased symphyseal and lateral corpus thickness. And it exhibits, along with other Middle Paleolithic immature mandibles, anteriorly wide dental arcades, probably due to large developing anterior permanent tooth crowns.     

Critical revision of the alleged delayed dental eruption in South American “ungulates”

The endemic South American “ungulates” (SANU) were traditionally assumed to be a monophyletic offshoot of the Granorder Ungulata, but the current reorganization of the extant ungulates in Laurasiatheria and Afrotheria (based on molecular data) leaved them in an undetermined systematic position. The delayed dental eruption versus cranial growth was proposed as a hard-tissue synapomorphy of Afrotheria. In a recent paper, at least some endemic SANU (Notoungulata, Astrapotheria, and possibly Pyrotheria) were interpreted as allied to Afrotheres by having a late replacement of deciduous cheek teeth. This statement was based on: (1) the usual occurrence within these groups of individuals with deciduous and permanent teeth; (2) the individual size (estimated comparing the length/width ratio of cheek teeth) of specimens with permanent premolars erupted is indistinguishable from that of specimens with deciduous premolars (putative juveniles), and (3) the retention of at least dP1–dP3 in adult specimens of Parastrapotherium (Astrapotheria). Herein we critically examine the presumed existence of delayed dental eruption in astrapotheres, pyrotheres and xenungulates and the assumptions on which it was based. The alleged evidences supporting the occurrence of delayed dental eruption in SANU arise from misinterpreted information from the literature and conceptual mistakes (i.e. delayed dental eruption versus cranial growth was confused with delayed replacement of premolars versus molar eruption). Based on examination of at-hand specimens, we found that there is no evidence for a delayed premolar replacement relative to the eruption of the molars in astrapotheres, pyrotheres, and xenungulates. A delayed dental eruption in relation to jaw growth does not occur at least in Astrapotherium magnum. Although a very recent study proposed close relationships among afrotheres and at least notoungulates and xenungulates, a more complete analysis is still needed to elucidate the evolutionary relationships of astrapotheres and pyrotheres.     

Evolutionary Implications of Dental Eruption in Dasypus (Xenarthra)

Late eruption of the permanent dentition was recently proposed as a shared anatomical feature of endemic African mammals (Afrotheria), with anecdotal reports indicating that it is also present in dasypodids (armadillos). In order to clarify this question, and address the possiblity that late eruption is shared by afrotherians and dasypodids, we quantified the eruption of permanent teeth in Dasypus, focusing on growth series of D. hybridus and D. novemcinctus. This genus is the only known xenarthran that retains two functional generations of teeth. Its adult dentition typically consists of eight upper and eight lower ever-growing (or euhypsodont) molariforms, with no premaxillary teeth. All but the posterior-most tooth are replaced, consistent with the identification of a single molar locus in each series. Comparison of dental replacement and skull metrics reveals that most specimens reach adult size with none or few erupted permanent teeth. This pattern of growth occurring prior to the full eruption of the dentition is similar to that observed in most afrotherians. The condition observed in Dasypus and many afrotherians differs from that of most other mammals, in which the permanent dentition erupts during (not after) growth, and is complete at or near the attainment of sexual maturity and adult body size. The suture closure sequence of basicranial and postcranial epiphyses does not correlate well with dental eruption. The basal phylogenetic position of the taxon within dasypodids suggests that diphyodonty and late dental replacement represent the condition of early xenarthrans. Additionally, the inferred reduction in the number of molars to a single locus and the multiplication of premolars represent rare features for any living mammal, but may represent apomorphic characters for Dasypus.     

Expression of CSF-1 receptor on TRAP-positive multinuclear cells around the erupting molars in rats

Bone resorption overlying a developing tooth is a necessary event in the creation of an eruption pathway. The formation and function of osteoclasts, which play a major role in bone resorption, are controlled by several factors. Although CSF-1 and its mRNA are expressed in dental follicle cells required for eruption, little is known about the contribution of CSF-1 to osteoclast formation on the bony crypt around the tooth germ. The receptor protein of the CSF-1 encoded proto-oncogene c-fms was identified on multinucleated cells adjacent to the dental follicle, in conjunction with TRAP staining as a marker enzyme for osteoclasts in rat. c-Fms was highly expressed in TRAP-positive multinuclear cells at 3 days postnatal and the number of c-Fms-expressing cells was reduced thereafter. Administration of IL-1alpha, which enhances formation and function of osteoclasts, caused an increase in the number of c-Fms and TRAP-positive cells in rat. On the contrary, injection of calcitonin, which depresses osteoclast formation, caused a decrease in the number. It is obvious that the receptor of CSF-1 is expressed on the surface of osteoclasts around the tooth germ, on the dental follicle. These findings suggested that CSF-1 directly enhances the influx of osteoclasts adjacent to the erupting tooth, resulting in the formation of an eruption pathway.