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Hovorakova 2007
Hovorakova 2007
Hovorakova 2007
Printed in Singapore. All rights reserved Journal compilation 2007 Eur J Oral Sci
European Journal of
Oral Sciences
The aim of this work was to investigate the early development of the deciduous
dentition and oral vestibule in the human embryonic lower jaw. Histological sections
and three-dimensional reconstructions from prenatal weeks 6–9 were used. A con-
tinuous anlage for the oral vestibule did not exist in the mandible. In contrast to the
upper jaw, where we previously observed that the dental and vestibular epithelia
developed separately, two dento-vestibular bulges differentiated in the incisor region of
the mandible. The lingual parts of each bulge were found to give rise to the respective
central and lateral incisors, whereas the labial parts differentiated into the vestibular R. Peterkova, Department of Teratology,
Institute of Experimental Medicine, Academy of
epithelium. In the canine and molar areas, the dental and vestibular epithelia origin- Sciences CR, Videnska 1083, 142 20 Prague 4,
ated separately. Later, the segments of the vestibular epithelium fused into the labial Czech Republic
vestibular ridge, giving rise to the lower oral vestibule in the lip region. In the cheek
Telefax: +420–241–062604
region, the oral vestibule was found to originate in the mucosal inflection between the
E-mail: repete@biomed.cas.cz
developing jaw and the cheek. A similar heterogenous developmental base for the oral
vestibule was also observed in the upper jaw. There is thus no general scheme for the Key words: deciduous tooth; dental epithelium;
early development of the dental and vestibular epithelia that applies to both the upper development; lower jaw; oral vestibule
and lower jaws, and to both their anterior and posterior regions. Accepted for publication May 2007
Tooth development in humans passes through the clas- However, three-dimensional (3D) imaging has
sical stages of odontogenesis: epithelial thickening; den- documented that the formation of the oral vestibule is
tal lamina; tooth bud; cap; and bell. Different authors much more complex in the human upper embryonic
have reported the first morphological signs of odonto- jaw (14). No continuous horseshoe-shaped vestibular
genesis in human embryos from embryonic day (ED) 28 lamina exists. Instead, the upper vestibular epithelium
(1) to ED 34–40 (2). It is generally accepted that the includes a series of epithelial bulges and ridges
upper and lower deciduous teeth develop from the (Fig. 1B). The dental and vestibular epithelia are
respective horseshoe-shaped dental lamina (3, 4). Text- regionalized in parallel along the mesio-distal axis.
books on human embryology present another horseshoe- They reiteratively fuse together behind the developing
shaped epithelial structure that runs parallel and exter- upper deciduous canine, first molar, and second molar
nally (labial or buccal) to the dental lamina in embryonic (14).
jaws (Fig. 1A). This is a vestibular lamina (also named The aim of this study was to investigate the early
the Ôlip-furrow bandÕ or Ôlabio-gingival ridgeÕ), which morphogenesis and developmental relationships of the
develops between the dental lamina and the future lips dental and vestibular epithelia in the human lower jaw,
and cheeks (5–8). The vestibular lamina is considered to and to compare them with what has previously been
be the developmental base of the oral vestibule, which is observed in the upper jaw (14).
the free space between the alveolar portion of the jaws,
including the teeth, and the lips or cheeks (6). Some
textbooks do not mention the development of the oral
vestibule at all (4, 9). Material and methods
Many authors have discussed the developmental rela- Embryos and fetuses
tionship between the dental and vestibular laminae in
The development of the dental epithelium was examined in a
humans, suggesting their independent development as
collection of serial histological sections held by the
two parallel epithelial anlagen (5, 6, 10), or that they Department of Teratology, IEM AS CR, in Prague. The
arise from a common epithelial thickening (2, 7, 11), collection comprises 53 series of frontal and 7 series of
or that these laminae are subdivisions of a common sagittal histological sections of the heads of normal human
thickened epithelial base in the anterior region and embryos (from artificially aborted embryos of unwanted
develop separately in the posterior region (12, 13). pregnancies) compiled from the 1960s to the 1980s.
Human lower dentition and oral vestibule 281
B C
Fig. 1. Schemes of the spatial relationship between the dental and vestibular epithelium in human embryos. Yellow, dental epithe-
lium; orange, base of the oral vestibule. The remaining vestibular epithelium is green. (A) According to the generally accepted
concept, the oral vestibule arises from a vestibular lamina (VL), which is a continuous structure running externally and parallel to the
dental lamina (DL). (B) Data on the upper jaw (14) have shown epithelial bulges that initially emerge externally to the dental
epithelium in the lip region. They fuse, being transformed into the canine vestibular ridge (CVR) in the posterior direction. The CVR
fuses with the dental mound behind the deciduous canine primordium (c). In the cheek region, the vestibular epithelium forms the
molar vestibular ridge (MVR) and the cheek-furrow ridge (the CFR is the epithelium lining the mucosal inflection between the
alveolus with teeth and cheeks). The MVR splits posteriorly into the medial (MMVR) and lateral (LMVR) branches. The fornix of
the oral vestibule originates from the bulges and the CVR in the lip region and from the CFR in the cheek area (14). AC, accessory
epithelial cap; m1 and m2, the upper first and second deciduous molars, respectively. (C) Present data on the lower jaw. The level of
the mouth corner (MC) is labeled. Different vestibular structures are shown: the area of irregularly thickened vestibular epithelium
(ITVE), the labial vestibular ridge (LVR), and the mandibular cheek furrow ridge (dCFR). The deciduous lower tooth primordia are
labeled: m1, first molar; m2, second molar.
Table 1
The specimens used for three-dimensional reconstructions ranked according to the stage of tooth development.
eosin, alcian blue–hematoxylin & eosin, or by a Periodic sional images were generated using a volume-rendering
Acid Schiff method. The early stages of tooth development program (Sun Voxel Sun Microsystems, Santa Clara, CA,
(epithelial thickening, dental lamina, tooth bud) were USA).
identified according to criteria reported by Peterkova et al. In addition to different views on the 3D reconstructions,
(18). we also performed sagittal sections through the 3D recon-
structions for complementary visualization of the relation-
ships between the dental and vestibular epithelia.
Computer-aided 3D reconstructions
Three-dimensional reconstructions of the dental and adja-
cent oral epithelium of the lower jaw quadrant were per-
formed in a representative sample of nine human embryos
Results
(Table 1). This sample showed a longitudinal adjustment of Morphology of the dental epithelium
the successive steps of tooth development. In each of the
embryos, the right or left jaw quadrant was randomly In a jaw quadrant at ED 40–42, two fields of thickened
selected for 3D reconstruction. epithelium were present along the mesio-distal axis
Contours of the dental and adjacent oral epithelium (Fig. 2A). These thickenings were situated in an end-to-
were drawn (magnification ·120–260, depending on the end orientation and separated by a deep notch
size of the specimen) at 10-lm intervals from each of the (Fig. 2A). The adjacent ends showed a bulge shape
serial histological sections using a Leica DMLB (Leica corresponding to the regions of the deciduous lower
Microsystems, Wetzlar, Germany) or a Jenaval (Carl Zeiss, lateral incisor (i2) and canine (c), respectively. Another
Jena, Germany) microscope equipped with a drawing
bulge was observed in the region of the deciduous lower
chamber. The superimposition of the drawings was per-
formed by the Ôbest fitÕ method (19) with respect to the central incisor (i1) (Fig. 2A). The two bulges in the
middle line and horizontal level for correct spatial posi- incisor region comprised the prospective dental and
tioning of the reconstructed structures. The digitalization vestibular epithelia (dento-vestibular bulges). The lin-
of the serial drawings and the correlation of successive gual parts of these bulges protruded (prospective buds
images have previously been described (20). Three-dimen- of deciduous i1 and i2), whereas the labial parts
Fig. 2. Computer-aided three-dimensional reconstructions of the epithelium on the oral surface of the lower jaw in HU1 at embryonic
days (ED) 40–42 (A), in HU3 at ED 42–44 (B), and in HU10 at ED 44–46 (C) at different stages of development (see Table 1) and
their schematic interpretation. The deciduous lower tooth primordia are labeled: c, canine; i1, central incisor; i2, lateral incisor; and
m1, first molar. Different vestibular structures are shown: the labial vestibular ridge (LVR), the irregularly thickened vestibular
epithelium (ITVE), and the epithelium lining the inflection of the forming lower vestibule adjacent to the cheek region of the
mandible (dCFR). The position of the mouth corner (MC) and ductus parotideus (DP) is indicated. The midline is shaded. The levels
labeled h–j indicate the positions of frontal histological sections shown in Fig. 4H–J, respectively.
Human lower dentition and oral vestibule 283
remained low (prospective vestibular epithelium). The fetus (HU8), i1, i2, c, and m1 reached the bell stage of
bulge in the canine region corresponded to the prim- tooth development, and the cap of the deciduous second
ordium of c. From the canine region, a thickening of molar (m2) became distinct (Fig. 3B).
the dental epithelium extended in the distal direction At all stages, the dental epithelium divided into two
(Fig. 2A), where the deciduous lower first molar (m1) parts behind the most distal developing tooth. The
showed the bud stage. medial band disappeared after a short distance, whereas
At ED 42–44, the buds of i1 and i2 differentiated from the lateral band continued in a disto-lateral direction
the lingual parts of the corresponding bulge. During (e.g. Figs 2B and 3B).
further development, the labial parts of the two dento-
vestibular bulges in the incisor region gave rise to the
Morphology of the vestibular epithelium
vestibular epithelium. Further posteriorly along the
course of the mandible, the dental epithelium formed a The vestibular epithelium did not arise as a continuous
mound with swellings at the places of c and m1 (Fig. 2B). vestibular lamina. While the bulges in the incisor area
As tooth swellings, as well as the mound, showed a bud were formed by the dento-vestibular epithelium (ED
shape on frontal sections, it was not yet possible to 40–44), the dental and vestibular epithelia developed
delimitate tooth primordia at a bud stage. However, separately in the canine–molar area. In the incisor area,
tooth primordia started to be distinct in developmentally the labial parts of the epithelial bulges progressively
more advanced embryos at ED 44–46 (HU10 and older separated from i1 and i2 as the vestibular epithelium.
embryos; see Table 1, Fig. 2C), after the teeth reached a In the canine and molar regions, the band of thickened
cap stage, whereas the mound epithelium in interdental vestibular epithelium was present externally to the dental
spaces retained a bud-shape on frontal sections epithelium at ED 40–42 (Fig. 2A). In the cheek region,
(Fig. 2C). During prenatal wk 8 the situation was similar the area of the irregularly thickened vestibular epithe-
to that at ED 44–46. However, the tooth caps were more lium (ITVE) differentiated from ED 42–44 (Figs 2, 3
differentiated (Figs 3A and 4). In the oldest examined and 4E–G).
Fig. 3. Computer-aided three-dimensional reconstructions of the epithelium on the oral surface of the lower jaw in HU7 at prenatal
wk 8 (A) and HU8 at prenatal wk 9 (B) at different stages of development (see Table 1) and their schematic interpretation. In (B) only
the distal part of the long dental arch could be reconstructed because of the technical limits of the camera. The deciduous tooth
primordia are labeled: c, canine; i1, central incisor; i2, lateral incisor; m1, first molar; and m2, second molar. Different vestibular
structures are shown: the labial vestibular ridge (LVR), the irregularly thickened vestibular epithelium (ITVE) and the epithelium
lining the inflection of the forming lower vestibule (dCFR). The position of the mouth corner (MC) and ductus parotideus (DP) is
indicated. The midline is shaded. The levels labeled a–g indicate the positions of frontal histological sections shown in Fig. 4A–G,
respectively.
284 Hovorakova et al.
fourth premolars from the basic mammalian dentition region, the segments of the dental and vestibular epi-
(29). The missing first and second premolars might thelia arise separately (14), whereas in the lower incisor
explain the presence of a significant interdental space region, there were two segments (bulges), each compri-
between the canine and the first deciduous molar (¼ sing precursors of the prospective incisor and its adjacent
third deciduous premolar) in the human embryonic vestibule (Figs 1 and 5). In the canine and cheek region
dental arch. of both the upper (14) and lower jaws, the dental and
vestibular epithelia arose independently (Figs 1, 2 and 5).
The lower oral vestibule had different developmental
The vestibular epithelium and the prospective
origins in the lip and cheek regions (Fig. 1C). In the lip
vestibule of the mouth
region, it developed from the labial vestibular ridge,
There was always a protrusion of the vestibular epithe- which presumably corresponds to the Ôlip-furrow-bandÕ
lium externally to the dental epithelium on histological of, for example Schour (5), or with the Ôlabio-gingival
sections (Fig. 4). Without correlation with the corres- sheetÕ of Bolk (11). However, in the cheek region of the
ponding 3D views, this protrusion could be considered as mandible (located behind the level of the mouth corner),
a component of a continuous horseshoe-shaped vestib- the oral vestibule originated from the epithelial ridge
ular lamina, giving rise to the prospective oral vestibule that lines the inflection between the cheeks and the
(Fig. 1A). The concept of the development of the oral prospective alveolus (Fig. 1C). The distinct origins of the
vestibule from a continuous vestibular lamina has been fornix of the oral vestibule in the lip and cheek regions
presented by many authors (1,5) and is still maintained in have also been reported in the human upper jaw (14)
embryological textbooks (6–8). However, the present 3D (Fig. 1B), in mice (30), and in sheep (31).
reconstructions did not show any continuous vestibular The developmental relationship between the dentition
lamina in the lower jaw (Figs 2 and 3). In its place, there (dental lamina) and the oral vestibule (vestibular lamina)
were several discontinuous epithelial structures (Fig. 1C) has not been completely explained in the literature. It has
as already observed in the upper jaw (14) (Fig. 1B). been stated that these structures: (i) evolve separately
The vestibular epithelium adjacent to the incisor (5, 6, 10); (ii) have a common origin (2, 7, 11); or (iii) are
primordia was segmented in parallel to individual teeth subdivisions of a common thickened epithelial base an-
in both the upper (14) and lower jaws (Fig. 1). However, teriorly, whereas they develop as two separate epithelial
there was an apparent difference: in the upper incisor structures in the posterior regions of the jaw (12, 13).
A B
C D
Fig. 5. Comparison of the upper and lower dental (DE) and vestibular (VE) epithelia on three-dimensional (3D) reconstructions. The
DE and VE of the upper (A, B) and lower (C, D) jaws of the embryo HU2 [embryonic days (ED) 42–44] are presented as an aerial
view on the 3D reconstruction (A, C) and on a sagittal section through the 3D reconstruction (B, D). In the upper incisor region, DE
and VE differentiate apart from each other, being separated by a groove indicated by a blue arrow (A, B). However, in the lower jaw,
one bulge formed by the dento-vestibular epithelium (DVE) is present in each of the central and lateral incisor regions (C, D). At later
stages, the lingual parts of the two bulges give rise to i1 and i2, respectively. The labial parts differentiate into the vestibular
epithelium. The midline is shaded.
286 Hovorakova et al.
26. Ooë T. On the development of position of the tooth germs in 30. Peterkova R. The common developmental origin and phylo-
the human deciduous molar teeth. Okajimas Folia Anat Jap genetic aspects of teeth, rugae palatinae and fornix vestibuli oris
1959; 32: 97–108. in the mouse. J Cran Genet Dev Biol 1985; 5: 89–104.
27. Ooë T. On the development of position of the human deciduous 31. Pavlikova H, Witter K, Misek I. The primordium of the
molar germs in the latter half of the fetal life. Okajimas Folia upper vestibulum oris in the domestic sheep. Acta Vet Brno
Anat Jap 1962; 38: 51–71. 1999; 68: 175–178.
28. Peyer B. Tooth formulae. In: Zangler R, ed. Comparative 32. Ooë T. On the early development of human dental lamina.
odontology. Chicago: University of Chicago Press, 1968; 197– Okajimas Folia Anat Jap 1957; 30: 197–210.
200. 33. Peterkova R, Lesot H, Peterka M. Phylogenetic memory of
29. Klein RG. The human career. Chicago: Chicago University developing mammalian dentition. J Exp Zool B Mol Dev Evol
Press, 1989. 2006; 306: 234–250.