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Prenatal development of the human mandible.

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THE ANATOMICAL RECORD 263:314 –325 (2001)
Prenatal Development
of the Human Mandible
SUK KEUN LEE,1 YEON SOOK KIM,1 HEE SOO OH,2 KYU HO YANG,2
EUN CHEOL KIM,3 AND JE GEUN CHI4*
1
Department of Oral Pathology, Kangnung National University College of Dentistry,
Seoul, Korea
2
Department of Pedodontics, Chonnam National University Dental College,
Seoul, Korea
3
Department of Oral Pathology, Wonkwang University Dental College, Seoul, Korea
4
Department of Pathology, Seoul National University College of Medicine,
Chongno-gu, Seoul, Korea
ABSTRACT
In an effort to better understand the interrelationship of the growth and development
pattern of the mandible and condyle, a sequential growth pattern of human mandibles in 38
embryos and 111 fetuses were examined by serial histological sections and soft X-ray views. The
basic growth pattern of the mandibular body and condyle appeared in week 7 of fertilization.
Histologically, the embryonal mandible originated from primary intramembranous ossification in
the fibrous mesenchymal tissue around the Meckel cartilage. From this initial ossification, the
ramifying trabecular bones developed forward, backward and upward, to form the symphysis,
mandibular body, and coronoid process, respectively. We named this initial ossification site of
embryonal mandible as the mandibular primary growth center (MdPGC). During week 8 of
fertilization, the trabecular bone of the mandibular body grew rapidly to form muscular attachments to the masseter, temporalis, and pterygoid muscles. The mandible was then rapidly
separated from the Meckel cartilage and formed a condyle blastema at the posterior end of linear
mandibular trabeculae. The condyle blastema, attached to the upper part of pterygoid muscle,
grew backward and upward and concurrent endochondral ossification resulted in the formation
of the condyle. From week 14 of fertilization, the growth of conical structure of condyle became
apparent on histological and radiological examinations. The mandibular body showed a conspicuous radiating trabecular growth pattern centered at the MdPGC, located around the apical area
of deciduous first molar. The condyle growth showed characteristic conical structure and abundant hematopoietic tissue in the marrow. The growth of the proximal end of condyle was also
approximated to the MdPGC on radiograms. Taken together, we hypothesized that the MdPGC
has an important morphogenetic affect for the development of the human mandible, providing a
growth center for the trabecular bone of mandibular body and also indicating the initial growth
of endochondral ossification of the condyle. Anat Rec 263:314 –325, 2001.
©
2001 Wiley-Liss, Inc.
Key words: mandible growth; condyle growth; mandibular primary growth
center; human; fetus
The mandible, derived from the first branchial arch
mesenchyme, remains one of the most debated topics in
the morphogenesis of oro-facial structure. The mandible, comparable to long bone, is movable and antagonistic to the maxilla with the control of masticatory, facial
expression, and some suprahyoid muscles (Azeredo et
al., 1996; Bareggi et al., 1995; Lee et al., 1992). Anatomically, the mandible is connected to the temporal
bone through the temporomandibular joint, innervated
by a mandibular branch of the trigeminal nerve and
serves important functions such as mastication, deglutition, and speech. Through the outcome of phylogenetic
©
2001 WILEY-LISS, INC.
evolution it is likely that the mandible has evolved into
more complex regulatory development via different
Grant sponsor: Ministry of Health and Welfare, Republic of
Korea; Grant number: HMP-98-M-4-0048.
*Correspondence to: Je Geun Chi, MD, Department of Pathology, Seoul National University College of Medicine, 28 Yongondong, Chongno-gu, Seoul 110-799, Korea.
E-mail: pathr@plaza.snu.ac.kr
Received 22 August 2000; Accepted 15 February 2001
Published online 00 Month 2001
DEVELOPMENTAL PATTERN OF HUMAN MANDIBLE
315
Fig. 1. Measurements of prenatal mandibular growth. a, b: soft X-ray view of 24-week-old fetus, a; lateral
view, b; vertical view, c, d: scheme of (a) and (b). Co, condyle head; Go, Gonion; Al, alveolar bone; Lb, lower
border of mandible; MdPGC, mandibular primary growth center.
pathways, i.e., muscular, alveolar, neural, and articular
parts (Goret-Nicaise and Dhem, 1984; Jakobsen et al.,
1991; Padwa et al., 1998).
Previous studies on mandibular development were focused mainly on the growth of condyle and symphysis
(Bareggi et al., 1995; Ben-Ami et al., 1992; Berraquero et
al., 1995; Bjork and Skieller, 1983; Kjaer, 1978b; Morimoto et al., 1987; Orliaguet et al., 1993b). A study on
mandibular growth in an early human fetal development
(weeks 8 –14) revealed the mandibular ramus grew faster
than the body, both in length and height; the greatest
growth rate was found in the height of ramus; and the
mandibular growth patterns differed significantly from
those of successive developmental periods (Bareggi et al.,
1995). Many authors had emphasized the importance of
growth of the Meckel cartilage (Bhaskar et al., 1953),
condylar head in mandibular growth (Kjaer 1978a; Morimoto et al., 1987; Shibata et al., 1996; Xu et al., 1983). A
precise description of the prenatal human mandibular
growth and developmental pattern, however, has not been
reported.
The purpose of this study is to investigate a sequential
growth pattern of the prenatal human mandible using
radiological and histological methods. This study is intended to show how morphogenetic evidence of the prenatal mandible relates to the developmental mechanism and
functional structure of the human mandible.
MATERIALS AND METHODS
Thirty-eight normally developed embryos and 111 fetuses were obtained from the Department of Pathology,
Seoul National University Hospital after thorough gross
and microscopic examinations. Gestational age of each
embryo and fetus was deduced from the crown-rump
length or maternal records. The 38 embryos aged from
5– 8 weeks of fertilization (six at 5 weeks old; 19 at 6 weeks
old; eight at 7 weeks old; and five at 8 weeks old, respectively). Embryos were fixed in 10% buffered formalin,
embedded in paraffin, serially sectioned in 4 ␮m thickness
on sagittal, transverse, or horizontal planes, and stained
with hematoxylin and eosin. Twenty-three fetal heads
developed early, ranging from week 9 to week 15 of fertilization (six at 9 weeks old; five at 10 weeks old; one at 12
weeks old; four at 13 weeks old; four at 14 weeks old; and
three at 15 weeks old, respectively). Fetal heads were
fixed in 10% buffered formalin, decalcified in 10% EDTA,
pH 7.0, embedded in paraffin, and serially sectioned on
frontal and horizontal planes in 4 ␮m thickness and
stained with hematoxylin and eosin. The later-developed
fetal mandibles (from 17 to 40 weeks of gestation) were
removed and fixed in 10% buffered formalin. Removed
mandibles were radiographed on lateral and vertical
views using Faxitron (Hewlett Packard, Corvallis, OR)
and soft X-ray film (Fuji, Tokyo, Japan). The specimens
were decalcified in 5% nitric acid, embedded in paraffin, and
longitudinal and cross sections of the mandibles were made
in 4 ␮m thickness and stained with hematoxylin and eosin.
A point of concentric radiopacity at the apical area of
deciduous first molar, from which linear trabecular bones
radiate to all directions of the mandible, was named as the
mandibular primary growth center (MdPGC). For the statistical analysis, five measurements of the fetal mandible
were made on the lateral and vertical view: 1) the length
of condyle growth was measured from MdPGC to condyle
head (Co); 2) the length of anterior mandibular growth
was measured from MdPGC to symphysis; 3) the length of
posterior mandibular body growth was measured from
MdPGC to mandibular angle (Go); 4) the length of anterior
mandibular height growth was measured from upper border
of alveolar (Al) bone to lower border (Lb) of mandible
through the MdPGC; and 5) the length of posterior mandibular height growth was measured from Go to Co. The gonial
angles formed by lower and posterior borderlines of the mandible at the mandibular angle were also measured (Fig. 1).
RESULTS
Growth of Mandibular Body
In the middle of week 5 of fertilization (Streeter stage
16), a pair of Meckel cartilage appeared in the center of
mandibular arch along with the growth of mandibular
316
LEE ET AL.
TABLE 1. Incremental growth of mandibular measurements of human fetus on radiogram
Fertilization
age (week)
Cases
(n ⫽ 111)
Co-MdPGC
(mm)
Co-Go
(mm)
MdPGC-Go
(mm)
MdPGC-Sym
(mm)
Al-Lb
(mm)
Gonial
angle
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
2
1
4
5
7
4
3
2
3
6
3
4
4
6
10
5
5
4
3
6
4
4
10
3
14.1
15.10.5
16.90.1
17.2
18.32.0
17.90.9
20.90.6
23.01.7
23.32.3
24.91.2
25.74.5
24.81.7
26.01.8
27.81.7
27.02.6
28.61.9
29.62.6
30.80.6
31.22.0
32.32.0
32.91.4
35.53.3
35.12.9
35.92.2
35.12.9
39.32.6
4.5
6.50.0
6.90.1
7.0
7.50.6
8.40.4
9.90.5
11.10.4
11.00.5
11.60.0
11.80.7
12.00.3
11.90.2
12.30.2
13.10.6
13.10.8
14.30.6
14.20.3
14.80.8
15.80.6
17.00.5
17.30.6
17.00.8
17.80.6
18.21.2
19.80.3
8.0
9.50.7
9.50.7
10.0
10.50.4
11.00.3
12.41.3
12.91.0
12.80.3
14.50.7
15.20.8
14.60.5
16.20.8
17.81.0
16.60.8
17.70.8
18.21.0
18.30.3
17.40.5
18.10.3
18.71.2
20.01.1
20.31.3
19.91.2
21.21.4
22.30.6
—
5.90.4
5.30.5
6.4
7.0.1.1
8.01.1
8.21.0
8.50.4
9.10.0
9.50.9
9.31.6
9.21.6
10.40.3
12.11.6
12.72.0
11.51.3
13.22.4
13.01.2
11.92.1
10.51.5
15.52.2
14.22.5
13.30.9
15.40.5
13.90.9
15.51.6
4.0
4.30.4
4.80.4
5.0
5.00.7
5.8
7.40.6
7.50.4
7.30.6
8.0
9.01.0
7.90.4
8.80.3
9.30.3
9.90.6
9.60.5
10.70.8
11.10.2
10.70.4
11.60.4
11.30.6
12.00.7
12.50.6
12.40.5
13.40.8
12.80.8
150
1484
1484
—
1483
1423
1474
1448
1400
1450
1445
1465
1464
1467
1466
1416
1403
1414
1397
1447
1423
1438
1418
1404
1367
1395
nerves and vessels to form the hyaline cartilaginous
tissue and thick perichondral fibrous mesenchyme.
From the middle of week 6 of fertilization (Streeter
stage 19), the mandibular ossification appeared as intramembranous bony apposition in close approximation
to the Meckel cartilage. The initial intramembranous
ossification of the mandible began at the facial fibrous
mesenchyme around the Meckel cartilage, with a direct
contact (Fig. 5a), or an encirclement with the Meckel
cartilage in contrast to the other long bones. In week 7
of fertilization (Streeter stage 21), the linear trabeculae
of mandible developed anteroposteriorly from the initial
ossification of the mandible. Serial sections revealed
that these linear trabeculae branched toward the future
mandibular symphysis, alveolar bone, mandibular
body, and coronoid process. At this time, the genioglossus muscle (Fig. 5b,c) was tightly attached to the lower
side of the anterior portion of Meckel cartilage, whereas
the primordium of masticatory muscle was located
around the middle portion of Meckel cartilage, i.e., masseter as well as temporalis muscles on the facial side
and pterygoid muscle on the lingual side of Meckel
cartilage respectively. As the ossification of mandible
progressed into the week 7– 8 of fertilization (Streeter
stage 22–23), the muscular attachment of the genioglossus muscle gradually changed from Meckel cartilage
into the anterior portion of linear trabeculae of mandibular symphysis (Fig. 5b). The primordia of masticatory
muscles (Fig. 6a), i.e., masseter, temporalis, and pterygoid muscles, departed from the Meckel cartilage and
repositioned around the linear trabeculae of mandible.
Late in week 9 of fertilization, the serial sections of
masseter and temporalis muscles showed muscular attachment to the buccal side of mandibular body and
coronoid process, respectively. The pterygoid muscle
(Fig. 6c), which had been primarily located on the lingual side of Meckel cartilage, was far from the lingual
side of mandibular body, because the mandibular body
was gradually shifted toward the facial direction. Simultaneously, the pterygoid muscle gradually moved
toward the posterior portion of mandibular body and
was divided mesially and laterally respectively; the
former attached to the lingual side of posterior mandibular body and the latter attached to the posterior end of
linear trabeculae of mandible, but not to Meckel cartilage. Serial sections of the embryonic jaw also revealed
that the thinned fibrous mesenchyme around Meckel
cartilage was traced to the thickened periosteal mesenchyme of mandible. Subsequently, the condyle blastema
appeared with the condensation of cellular mesenchyme
at the posterior end of linear trabeculae of the mandible
with an attachment to the lateral pterygoid muscle. In
week 10 of fertilization, the mandibular ossification advanced to form an anatomical structure of the lower jaw
including the mandibular angle (Fig. 7a), coronoid process (Fig. 7a), and symphysis (Fig. 5e). By this time, the
lower part of genioglossus muscle was attached to the
lower portion of mandibular symphysis, while the upper
part of genioglossus muscle was still attached to the
anterior portion of Meckel cartilage. In week 11 of fertilization, as the anteroposterior growth of the mandible
increased with multilayered bony trabeculae, then the
upper part of genioglossus muscle was almost detached
from Meckel cartilage. The site of initial intramembranous ossification of the mandible (Fig. 5d), however,
remained approximate to the Meckel cartilage (Fig.
5d,f,g). In week 12 of fertilization, most of the genioglossus muscle was attached to the lower portion of anterior
DEVELOPMENTAL PATTERN OF HUMAN MANDIBLE
Fig. 2. Growth pattern of prenatal mandible by soft X-ray view, lateral view of mandible. a: 16-week-old
fetus; b: 17-week-old fetus; c: 18-week-old fetus; d: 20-week-old fetus; e: 25-week-old fetus; f: 30-week-old
fetus; g: 34-week-old fetus; h: 38-week-old fetus.
317
318
LEE ET AL.
Fig. 3. Incremental growth of representative measurements of prenatal human mandible. Co-MdPGC, length from condyle head to
mandibular primary growth center; MdPGCGo, length from mandibular primary growth
center to Gonion; Co-Go, length from condyle
head to Gonion; MdPGC-Sym, length from
mandibular primary growth center to mandibular symphysis; Al-Lb, length from alveolar
bone to lower mandibular border.
Fig. 4.
Changes of gonial angle during fetal period.
Fig. 5. Relationship between Meckel cartilage and mandible during morphogenetic stage of human embryos. a: Six weeks old, mandible (Md)
appears at facial side of Meckel cartilage (Mc) (HE, ⫻40). Tg, tongue; DL, dental lamina. b: Eight weeks old, lingual side of Meckel cartilage is not
covered with intramembranous ossification of mandible, note the genioglossus muscle (Gg) attached tightly both on the lower side of anterior portion
of Meckel cartilage and on the portion of mandibular symphysis (HE, ⫻20). Mx, maxilla; UL, upper lip; LL, lower lip. c: High magnification of (b),
intramembranous ossification of mandible is closely associated with the fibrous mesenchyme of Meckel cartilage (HE, ⫻70). d: Eleven weeks old,
mandibular ossification continuously grows outwardly from Meckel cartilage with a direct contact (HE, ⫻70), square; site of initial intramembranous
ossification. e: Ten weeks old, frontal section, newly formed mandibular arch is larger than Meckel cartilage arch (HE, ⫻60). Sym, symphysis. f:
Eleven weeks old, horizontal section of mandible shows the initial ossification site of mandible that was named as mandibular primary growth center
(MdPGC) (HE, ⫻10). SM, submandibular gland; Hy, hyoid cartilage. g: High magnification of (f), the MdPGC showed ramifying trabecular structure,
the portion of Meckel cartilage approximated by MdPGC was rapidly resolved (arrows) (HE, ⫻60). h: Twelve weeks old, sagittal section showing
longitudinal alignment of Meckel cartilage and linear trabecular bone of mandible (⫻5). TG, trigeminal ganglion; SM, submandibular gland; IE, inner
ear organ; Ey, Eye. i: High magnification of (h), the linear trabeculae of mandible was approximated to the anterior portion of Meckel cartilage (⫻70).
To, tooth germ. j: Ten weeks old, hyalin cartilage with intact cellular morphology (inlet, ⫻1,000) (HE, ⫻200). k: Twelve weeks old, the chondrocytes
were swollen and some of them disappeared (arrows) (HE, ⫻400). l: Twenty weeks old, the Meckel cartilage was shrunken and separated from
mandible (HE, ⫻200). m: high magnification of (l), peripheral chondrocytes were gradually resolved (arrows) (HE, ⫻1,000).
DEVELOPMENTAL PATTERN OF HUMAN MANDIBLE
Figure 5.
319
320
LEE ET AL.
mandible to form the median symphyseal structure. As
a result, Meckel cartilage became completely detached
from the linguo-mandibular architecture (Fig. 5f,g) and
rapidly decreased in size (Fig. 5h,i). At this stage, the
Meckel cartilage became atrophic and its perichondral
fibrous mesenchyme remained thin, and its hyaline cartilage tissue also showed degenerative changes of chondrocytes, i.e., enlarged empty lacunae without nuclei or
pyknotic/karyorrhectic nuclei (Fig. 5j,k). The cartilage
matrix and chondrocytes of the Meckel cartilage were
gradually shrunken and finally resolved with infiltration of tissue macrophages into the perichondral fibrous
tissue. The Meckel cartilage, however, showed no endochondral ossification until later in fetal life (Fig. 5l,m).
From week 12 of fertilization, the intramembranous
bony ossification was active at the periphery of ramifying
trabeculae of the mandibular body, coronoid process and
symphysis. The central trabecular bone became thick and
sclerotic (Fig. 5h,i). During weeks 13–15 of fertilization,
the mandible grew as multilayered trabeculae radiating
from the primary ossification site of the embryonic mandible, namely the mandibular primary growth center (MdPGC). From week 16 of fertilization, the radiating trabeculae of mandible could easily be demonstrated by a soft
X-ray view. Thereafter, the radiating trabecular bones
from the MdPGC corroborate the mandibular body growth
during later in fetal life (Fig. 2). The radiological dimensions of MdPGC-Sym and MdPGC-Go, which represent
the growth of anterior and posterior body of mandible
respectively, showed similar incremental growth rates
during the fetal period. The incremental growth rate of
Go-Co, representing the posterior mandibular height, was
higher than that of Al-Lb, representing the anterior mandibular height. The incremental growth rate of Al-Lb was
similar to those of MdPGC-Sym and MdPGC-Go during
the fetal period (Fig. 3). The gonial angle was measured
about 146 –148° in an early fetal period, and decreased to
141–143° until late in fetal period (Fig. 4).
Growth of Condyle
In the early week 7 of fertilization (Streeter stage 21), a
group of cellular mesenchymal tissue was formed around
the posterior end of linear trabeculae of the mandible (Fig.
6a,b). In serial sections, this cellular mesenchymal tissue
was traced to the fibrous mesenchyme around the Meckel
cartilage (Fig. 6c). A branch of pterygoid muscle was
clearly associated with the condensed mesenchyme late in
week 7 of fertilization. Early in week 8 of fertilization
(Streeter stage 23), the posterior end of linear trabeculae
of the mandible showed an increased osteoblastic hyperplasia and was well surrounded by the condensed mesenchyme that produced a condyle blastema, to which the
lateral pterygoid muscle was attached. From early in week
9 of fertilization, however, the blastema of the condyle
produced a cartilaginous tissue forming a condylar head
at the posterior end of linear trabeculae of the mandible.
The condyle grew rapidly with the bony deposition of
endochondral ossification. As the condyle was elongated
upward and laterally, a part of pterygoid muscle moved
along with the condyle head. Simultaneously, the pterygoid muscle was divided into mesial (internal) and lateral
(external) groups (Fig. 6d,e). The mesial pterygoid muscle
remained at the mesial side (lingual or internal side) of
the mandibular body, while the lateral pterygoid muscle
moved continuously upward and laterally (externally) in
concert with the rapid condyle head growth. Expansive
growth of the cartilaginous condyle head produced a conical bony structure, which was in contrast to the adjacent
mandibular body growth on radiograms and histological
sections. In week 12 of fertilization, the conical shaped
condyle was elongated toward the temporal squama to
form the temporomandibular joint. Thereafter, the condyle grew in a characteristic conical shape. The condyle,
composed of a distally thickened cartilaginous cap and
proximally thinned apex, converged toward the MdPGC
(Fig. 7a–f), where bundles of vessels and nerves were
located (Fig. 7g). The conical condyle contained abundant
hematopoietic cells in its marrow space, and formed a
curve along the angulation from the ramus to the mandibular body as it’s growth advanced (Fig. 7h,i). The
amount of incremental growth of the conical condyle (CoMdPGC), however, was highest in the representative anatomical dimensions of the human mandible during the
fetal period (Fig. 3).
DISCUSSION
We observed that mandibular ossification started from
the mandibular primary growth center (MdPGC), and
that the mandibular growth pattern was characterized by
intramembranous ossification of the mandibular body and
endochondral ossification of the condyle. In our previous
study, we explored the growth pattern of human prenatal
maxillae and confirmed a pair of maxillary primary
growth centers (MxPGC). The MxPGC showed the characteristic radiating, trabecular patterns by both the histological and radiological observations (Lee et al., 1992). It
was suggested that the MxPGC is an initial ossification
site of the maxilla. The MxPGC was an important anatomical landmark to analyze the stress-bearing maxillary
structure, and remained as a sclerotic trabecular bone
containing channels of nerve bundles and vessels later in
fetal life, while major growth sites of the maxilla were at
the distal ends of trabecular bones that radiated from the
MxPGC. In this study we found a similar growth pattern
in the mandibular development of human fetuses. During
the developmental stages of the mandible, its primary
growth center (MdPGC) was detected as a primary site of
intramembranous ossification around the middle portion
of the embryonal jaw. The MdPGC became the central
part of the mandibular body, which appeared as a sclerotic
focus of radiating trabeculae of the mandibular body
Fig. 6. a– d: Condyle growth. e– g: Cross section of mandibular body. a:
Seven weeks old, condyle blastema (CB) developed from the posterior
end of linear trabeculae of mandible (HE, ⫻40). Tp, temporalis muscle;
MN, mandibular nerve; LPt, lateral pterygoid muscle; MPt, mesial pterygoid muscle; Ms, masseter muscle. b: High magnification of (a), the
condyle blastema consists of active osteoblastic deposition (arrow) and
abundant mesenchymal condensation (HE, ⫻400). c: Eleven weeks old.
d: Twelve weeks old. e: High magnification of (d), condyle blastema (CB)
attached by lateral pterygoid muscle (LPt) grew toward temporal bone
(Te), note upper lateral pterygoid muscle (ULPt) and lower lateral pterygoid muscle (LLPt) (HE, ⫻40). f: Sixteen weeks old, cross section of
mandible at first deciduous molar area (To), retrogressive Meckel cartilage (Mc) is remained at the lingual side of mandible (Md) (HE, ⫻40). g:
High magnification of (f), the Meckel cartilage (Mc) has no direct connection to mandibular ossification (HE, ⫻200). h: Twenty weeks old,
cross section of mandible, the Meckel cartilage (Mc) is rudimentary and
almost isolated from the mandible (Md) (HE, ⫻40).
DEVELOPMENTAL PATTERN OF HUMAN MANDIBLE
Figure 6.
321
322
LEE ET AL.
shown on radiograms taken later in fetal life, whereas
major growth sites of the mandible were at the distal ends
of trabecular bones radiated from MdPGC.
The sequential development of the human mandible
started from the middle of week 5 of fertilization, with the
formation of core cartilage in mandibular swelling i.e.,
Meckel cartilage, and the mandible grew actively to
form a mandibular arch protuberance. Three stages of
Streeter’s development appeared particularly important
during the mandibular development: stage 16 (appearance of Meckel cartilage), stage 20 (beginning of membranous ossification), and stage 23 (end of the human embryonic period, week 8) (Orliaguet et al., 1993a). Many
authors presumed that the Meckel cartilage, the first
branchial arch cartilage, had no relationship to the processes of mandibular ossification (Merida-Velasco et al.,
1993; Orliaguet et al., 1993b, 1994; Rodriguez-Vazquez et
al., 1997a,b; Tomo et al., 1997). Unlike the long bones,
Meckel cartilage entirely regressed during the later fetal
period (Ellis and Carlson, 1986). In this study, however,
we observed the primary intramembranous ossification of
embryonal mandible developed in Streeter stage 19, earlier than the ossification of long bones usually found at
Streeter stage 20 (Orliaguet et al., 1993a). We found that
the intramembranous ossification as well as the condensed cellular mesenchyme of the condylar blastema was
closely associated with a portion of perichondral fibrous
tissue of the Meckel cartilage. Because the primary intramembranous ossification of the mandible greatly affects the following histomorphogenetic processes of the
whole mandible (Bareggi et al., 1995; Berraquero et al.,
1995; Orliaguet et al., 1993b, 1994; Rodriguez-Vazquez et
al., 1997b; Tomo et al., 1997), we accentuate the primary
intramembranous ossification and named it as the mandibular primary growth center (MdPGC). The MdPGC
was approximated to the middle portion but lateral in
position of the Meckel cartilage in the early embryonal
period. Then, the trabecular bones originating from the
MdPGC grew out rapidly toward the facial side, losing the
relationship to the Meckel cartilage. These findings imply
an important role of Meckel cartilage for the initial ossification of the mandible. We have also observed that the
primary intramembranous ossification of the embryonic
mandible did not encircle the Meckel cartilage the same as
long bones but rather dislocated gradually to the facial
side apart from the Meckel cartilage. It was also noted
that the human Meckel cartilage did not undergo endochondral ossification unlike the core cartilages of long
bones, although some animals showed calcification of the
Meckel cartilage during the fetal period (Ishizeki et al.,
1999; Tomo et al., 1997; Yamazaki et al., 1997). In the
serial sections of human embryonic mandibles, however,
we observed that the ossifying mandible and its attached
muscles were detached from Meckel cartilage and dislocated outwardly as the lingual growth was advanced to fill
the stomodeal cavity and to influence the mandibular
movement. Thus, we hypothesize that early mandibular
movement by the masseter and suprahyoid muscles may
influence the premature dislocation of the primary mandible from Meckel cartilage in the early embryonic period.
From the serial sections of human embryos we also
observed that the genioglossus muscle was attached to the
perichondral fibrous tissue of Meckel cartilage in the early
week 6 of fertilization. The genioglossus muscle was successively reattached to the inferior portion of mandibular
symphysis at 12 week of fertilization. Other muscles, such
as masticatory, mylohyoid, etc., were not attached but
were positioned around the perichondral fibrous tissue of
Meckel cartilage during weeks 6 –7 of fertilization. When
the intramembranous ossification of the mandible advanced to form multilayered linear trabeculae, the masticatory and mylohyoid muscles were attached tightly to the
outgrowing mandible rather than Meckel cartilage during
weeks 8 –9 of fertilization. Although the direct histogenetic effect of Meckel cartilage on the embryonal induction
of mandible remains unclear, we presume that the Meckel
cartilage plays an important role to integrate the formation of human mandible, which was evolutionarily
adapted to provide increased arch size and mobility. The
question of “What influences the transition of the mandibular core skeleton from Meckel cartilage into mandible?”
remained unanswered. It was suggested that it may depend on the early mouth opening movement, primarily
induced by tongue musculature which matured quite
early in orofacial structures (Bresin et al., 1999; Kang et
al., 1992; Kiliaridis and Katsaros, 1998; Lee et al., 1990;
Lightfoot and German 1998; Ogutcen-Toller and Juniper,
1993; Radlanski et al., 1999; Robertson and Bankier 1999;
Sato et al., 1994). It was also reported that it may be
influenced by mandibular movement in the human embryo beginning around week 8 of fertilization, when the
temporomandibular joint is yet to be formed (Hall
1982a,b; Kjaer, 1997; Ouchi et al., 1998). Although the
mechanism of an early mouth movement is unclear, it is
apparent that the masticatory muscles do not induce the
early embryonic mandibular movement at this stage because of their immaturity. We presume that the tongue
movements directly induce the early mandibular movement, because Meckel cartilage, a primary skeleton of the
mandible during weeks 5–7 of fertilization, was tightly
attached to the genioglossus muscle. We also observed,
however, that the primordia of the masseter, temporalis,
and pterygoid muscles became attached to the newly
formed mandible in the late week 8 of fertilization. This
finding may imply that the early mouth opening movement causes the primordia of the masseter, temporalis,
and pterygoid muscles relocate from the Meckel cartilage
to the newly formed mandible moving along with tongue
movement. Thus, we believe that the mandible supported
by masticatory and tongue muscles would be able to control the development of the lower jaw as a new articulation
without the influence of Meckel cartilage from approximately week 8 of fertilization.
The present study also indicates that the characteristic
structure of the mandibular body exhibits a radiating
trabecular pattern from the MdPGC that is closely related
to the attachment of surrounding muscles. The pulling
force of associated muscles may induce continuous appositional growth of intramembranous ossification on the
periosteal side, rather than in the MdPGC, which is no
longer proliferative later in fetal life. We suggest that the
MdPGC is a primary ossification site of the fetal mandible,
forming a rigid center of the mandibular structure. Serial
sections of fetal mandibles showed that the linear trabeculae of the mandibular body were focused at the center of
the MdPGC. In week 12 of fertilization, however, the
architecture of the mandibular body was almost complete
with the characteristic shapes of the mandibular body,
coronoid process, mandibular angle, and symphysis. From
week 15 to 16 of fertilization, the growth of mandibular
Fig. 7. Growth pattern of mandibular body and conical condyle. a:
Twenty weeks old, longitudinal section of mandible, conical condyle
growth (C) is characteristic (HE, ⫻5). CP, coronoid process; MA, mandibular angle; Sy, symphysis; ToD, deciduous first molar tooth germ;
ToE, deciduous second molar tooth germ. b: Twenty-five weeks old,
tube like condyle growth is conspicuously demarcated (arrows) (HE, ⫻7).
EA, external auditory meatus. c: Twenty-seven weeks old, rapid growth
of conical condyle (arrows) (HE, ⫻10). d: Twenty-eight weeks old, conical condyle growth is clearly distinguished by its trabecular pattern
(arrows) (HE, ⫻10). e: Thirty-five weeks old, conical condyle remained as
sclerotic bone (*) (HE, ⫻10), ToC, deciduous canine tooth germ; To6,
permanent first molar tooth germ. f: High magnification of asterisk (*)
area of (e), still the trabecular structure of conical condyle growth (arrows) is different from that of mandibular body growth (HE, ⫻40). g: High
magnification of arrow area of (e), dilated vessel (V) and thick sclerotic
trabecular bone around the MdPGC (HE, ⫻200). h: Thirty weeks old,
cross section of mandible at deciduous second molar (ToE) area, the
conical condyle growth is demarcated by arrows, and it contains hematopoietic tissue in the center (HE, ⫻10). i: Thirty weeks old, longitudinal
section of mandible, hematopoietic tissue (*) is abundant in the marrow
space in the conical condyle growth (arrows) (HE, ⫻100).
body and condyle was clearly distinguished by radiography. The MdPGC clearly showed a radiating trabecular
pattern originating from the apical area of the deciduous
first molar tooth germ. This growth pattern of the mandibular body became most conspicuous during weeks
20 –25 of gestation. The MdPGC was conspicuously detected near the apical area of the first deciduous molar
tooth germ. Numerous linear bony trabeculae originating
from the MdPGC grew peripherally, extending to the coronoid process, mandibular angle, symphyseal area, and
even to the alveolar ridge (Fig. 8). Later in the fetal period,
from week 30 of fertilization, the image of the radiating
trabecular pattern was gradually overlapped with the image of tooth germs and peripheral cortical bone consolidated by muscular attachments.
A morphological study on the developing lateral pterygoid muscle and its relationships to the temporomandibular joint and Meckel cartilage indicated that all of temporomandibular joint structures and lateral pterygoid
muscle assumed their adult shapes by week 14 of fetal life.
At this stage, the lateral pterygoid muscle formed a complex structure with several aponeuroses dividing the muscle into three main parts: superior, inferomedial, and inferoanterior (Ogutcen-Toller and Juniper, 1993). This
means that the muscular forces arising from mandibular
movement directly influence the growth of the condyle and
temporomandibular joint simultaneously. Thus, in this
study we observed that the lateral pterygoid muscle was
primarily attached to the condyle blastema tissue and
became elongated through rapid condylar growth during
weeks 8 –10 of fertilization. This may imply that the lateral pterygoid muscle guides the conical condyle to form
the temporomandibular joint. These data, however, suggest that the mandibular movement primarily controlled
by the genioglossus muscle in the early embryonic period
could affect the growth of the mandibular body and the
condyle. Premature mandibular movement occurred at
least 2 weeks earlier than the temporomandibular joint
movement and stimulated the adaptational growth of the
mandibular body and condyle. Thereafter, condyle growth
was highly accelerated to form its conical structure and
became independent of mandibular body growth.
The incremental growth of the mandibular dimension
on the radiogram showed well-harmonized growth curves
between the growth rate of mandibular body and condyle
during the fetal period. The incremental growths of MdPGC-Sym, MdPGC-Go, and Al-Lb represent the pattern of
mandibular body growth and the incremental growths of
MdPGC-Co and Co-Go represent the pattern of condyle
growth. The former group, however, showed a slightly
reduced growth curve compared with that of the latter
group. This may imply that condylar growth is much accelerated compared with those of the mandibular body.
The slight reduction in gonial angle during the fetal period
may also indicate increased growth of the condyle more in
a vertical than a horizontal direction. These findings are
concurrent with previous concepts of the mandibular development and growth (Baccetti et al., 1997; Bareggi et al.,
1995; Buschang et al., 1999; Keith, 1982; Kjaer 1978a,b;
Radlanski et al., 1999; Ronning, 1995).
In summary, we studied the sequential growth of the
human fetal mandible and found that radiating trabeculae of the mandibular body focused into a primary growth
center, MdPGC. From the MdPGC, the mandibular development was divided into two distinctive growth patterns
Fig. 8. Representative scheme for mandibular body growth (upper)
and condyle growth (lower).
of the mandibular body and condyle, as shown in Figure 8.
We suggest that the MdPGC is an important anatomical
landmark from which we can measure the growth directions or amounts of the mandible and that the MdPGC has
an important morphogenetic implication for the development of human mandible, providing a growth center for
the trabecular bone of the mandibular body and also indicating an initial growth of endochondral ossification of
the condyle.
ACKNOWLEDGMENTS
We would like to express our sincere appreciation to the
devoted donors of human materials, who made it possible
to perform this study through the legally approved procedure from the center of Congenital Malformation, Seoul,
Korea. We are very thankful to Dr. Soo Il Chung and Dr.
Yoo Mie Chung for their kind and critical review of the
manuscript.
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