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Radiological trace of mandibular primary growth center in postnatal human mandibles.

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THE ANATOMICAL RECORD PART A 288A:1234–1242 (2006)
Radiological Trace of Mandibular
Primary Growth Center in Postnatal
Human Mandibles
YOUNG JOON LEE,1 SANG SHIN LEE,1 BYOUNG GEOL PARK,1
SANG DOO WOO,1 EUN CHEOL KIM,2 YEON SOOK KIM,1
SUK KEUN LEE,1* AND JE GEUN CHI3
1
Department of Oral Pathology, College of Dentistry, Kangnung National University,
Gangneung, Korea
2
Department of Oral and Maxillofacial Pathology, College of Dentistry,
Wonkwang University, Iksan, Korea
3
Department of Pathology, College of Medicine, Seoul National University, Seoul, Korea
ABSTRACT
The mandibular primary growth center (MdPGC) of human fetus
was conspicuously defined in the soft X-ray view of fetal mandibles. As
the peripheral adaptive growth of mandible advances during the postnatal period, the MdPGC image became overshadowed by condensed cortical bones in soft X-ray view. In this study, we traced a sclerotic sequela
of MdPGC during the postnatal period. Panoramic radiograms of 200
adults and soft X-ray views of 30 dried adult mandibles were analyzed by
statistical methods. The former clearly showed an MdPGC below the middle portion of apices of canine and first premolar, which was distinguishable from mental foramen, and the latter also showed the MdPGC at the
same area as a radiating and condensed radiopaque image, measuring
0.5–1.0 cm in diameter. This MdPGC position was seldom changed in the
elderly people, even in the edentulous mandibles. Additionally, in the
radiological examination, the benign tumors including odontogenic cysts
hardly involved the MdPGC, while the malignant tumors of both primary and metastatic cancer frequently destroyed the MdPGC. Anat Rec
Part A, 288A:1234–1242, 2006. Ó 2006 Wiley-Liss, Inc.
Key words: mandibular primary growth center; postnatal period; pantomogram; dried adult mandible
The mandible consists of a unique bony structure with
tight attachment of strong masticatory muscles and delicate facial expression muscles and develops a joint with
temporal bone, resulting in temporomandibular joint
(Haskell, 1979; Bresin et al., 1999; Tumer and Gultan,
1999; Bresin, 2001). Although it is well known that the
whole mandibular structure is derived from the first
branchial arch, yet the prenatal development of mandible is one of the debating subjects for the morphogenesis
of orofacial structure (Hall, 1982; Lee et al., 1990, 1996,
2001; Barni et al., 1998). The Meckel’s cartilage may
play an important role in the topographical organization
and in the differentiation of the facial structure during
the embryonal and early fetal period (Plessis et al.,
1991; Orliaguet et al., 1994; MacDonald and Hall, 2001;
Radlanski et al., 2003; Lorentowicz-Zagalak et al., 2005).
Ó 2006 WILEY-LISS, INC.
The initiating role played by the ventral part of Meckel’s
cartilage on the ossification of mandible during the embryonal period leads to the formation of the mandibular primary growth center (MdPGC). The partial fibrous evolu-
Grant sponsor: Korean Science and Engineering Foundation;
Grant numbers: R11-2002-097-07004-0 and R01-2003-000-10891-0.
*Correspondence to: Suk Keun Lee, Department of Oral Pathology, College of Dentistry, Kangnung National University,
Gangneung 210-702, Korea. Fax: 033-642-6410.
E-mail: sklee@kangnung.ac.kr
Received 26 April 2006; Accepted 21 July 2006
DOI 10.1002/ar.a.20392
Published online 19 October 2006 in Wiley InterScience (www.
interscience.wiley.com).
MANDIBULAR PRIMARY GROWTH CENTER
tion and the regression of the major part of the ventral
branch of Meckel’s cartilage start only after 16 weeks of
intrauterine life (Bontemps et al., 2001). Bone growth of
the fetal mandible is a complex process comprising lingual
resorption and buccal apposition, and resting the ossification areas seamed by lining cells (Radlanski et al., 1999;
Radlanski and Klarkowski, 2001).
Later growth of mandible is easily observed in the
condyle head and symphysis suture, but it is still hard
to explain the morphogenetic development of whole
mandible by the condyle and symphysis growth only. In
a previous study, we determined the MdPGC in human
fetuses. The MdPGC has an important morphogenetic
effect 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 (Lee et al.,
2001). From these series of results, one MdPGC was
observed below the middle portion of apices of canine
and first premolar, a little anteriorly located to the mental foramen in soft X-ray view of the removed fetal mandibles. And the MdPGC was the most active site for
mandible body formation during fetal period by the participation of the intramembranous bone ossification along
the radiating trabeculae to form the mandibular body,
including mandibular angle, coronoid process, symphysis,
and alveolar bone, while condyle head was also active for
condyle growth by endochondral ossification (Kjaer, 1978;
Baumrind et al., 1983; Morimoto et al., 1987; Orliaguet
et al., 1993b; Eroz et al., 2000; Lee et al., 2001).
The aim of this study was to define the sequela of the
MdPGC in the postnatal adult mandibles by radiological
method, and we found a focal radiopaque image in the
anterior mandibular body that was clearly distinguishable from the radiological images of mental foramen and
lingual torus. Through the statistical analysis for the
positional measurements of the radiopaque spot during
the postnatal life, we determine this radiopaque spot is
identical to the sequela of MdPGC and discuss its roles
for the postnatal growth of mandible.
MATERIALS AND METHODS
Two hundred cases of pantomograms were obtained
from the patients, ranging from 11 to 79 years old, who
visited for routine check at Kangnung National University Dental Hospital from 2002 to 2005, using X-ray
machine of Cranex 3þ Ceph (Soredex Orion, Finland),
and their images were digitalized by FCR 5000 (Fuji
Medical System, Japan). All materials were legally
approved by Kangnung National University Dental Hospital and Dental College.
The pantomograms were taken in ordinary head position indicated by the X-ray machine protocol and analyzed for the position of MdPGC and mental foramen in
mandibular body by measuring their proportional dimensions of horizontal and vertical positions. The horizontal
ratios of MdPGC and mental foramen were measured by
the ratio of symphysis-MdPGC/symphysis-mandibular
angle, and symphysis-mental foramen/symphysis-mandibular angle, respectively. The symphysis-mandibular
angle is identical to the mandibular body length. And
the vertical ratios of MdPGC and mental foramen were
measured by the ratio of inferior mandibular border-
1235
MdPGC/inferior mandibular border-superior margin of
alveolar bone, and inferior mandibular border-mental
foramen/inferior mandibular border-superior margin of
alveolar bone, respectively. The length between inferior
mandibular border and superior margin of alveolar bone
is identical to the mandibular body height. The positions
of MdPGC and mental foramen, obtained from 11- to 79year-old subjects, were plotted to elucidate the growth
pattern (Fig. 1).
Thirty dried adult mandibles were the materials preserved for anatomical teaching. Their use was approved
by the human tissue committee of Kangnung National
University. They were examined by soft X-ray (film, Fuji,
Tokyo, Japan) using Faxitron machine (Hewlett-Packard,
Corvallis, OR). The radiograms were analyzed to define
the radiopaque image of MdPGC in adult mandibles.
Additionally, in order to evaluate the rigidity of MdPGC
in pathological conditions, 30 cases of benign and malignant tumors involving the anterior mandibular body were
selected and examined for the morphological changes of
radiopaque image of MdPGC on pantomogram.
RESULTS
Pantomograms of Adult Human Mandibles
A focally condensed radiopaque image was observed
bilaterally in the anterior mandibular body on the wellprocessed pantomograms, and it usually appeared as a
round shape with radiating pattern below the middle
portion of apices of canine and first premolar. It measured 0.5–1.0 cm in diameter. This radiopacity was
clearly distinguishable from mental foramen, which also
located more distally, and also from the lingual torus,
which was usually located more mesially and showed
round homogeneous radiopacity (Fig. 4). From 200 pantomograms, the position of the radiological images of
MdPGC and mental foramen were evaluated. The proportional ratios of MdPGC and mental foramen in the
mandibular body were compared. The horizontal ratio of
MdPGC gradually decreased from 0.25 to 0.18 during the
postnatal age, while the horizontal ratio of mental foramen
gradually increased from 0.24 to 0.41 (Fig. 2A and B). The
average horizontal ratio of MdPGC was 0.22 6 0.034,
and the average vertical ratio of MdPGC was 0.37 6
0.061, while the average horizontal ratio of mental foramen was 0.3 6 0.034 and the average vertical ratio of
mental foramen was 0.36 6 0.082 (Table 1). However,
the positions of both MdPGC and mental foramen were
stable, and they were separately observed far apart as
different osseous trabecular pattern on the pantomograms. The distance between MdPGC and mental foramen remained stable during the postnatal period, and
its average was 9.4 6 1.56 mm (Fig. 2C).
Soft X-Ray View of Dried Adult Mandibles
In the soft X-ray view of 30 dried adult mandibles, the
focal condensed radiopaque area could be seen in the
same area seen on the pantomograms of adults. The
radiopacity showed a radiating trabecular pattern, below
the middle portion of apices of canine and first premolar,
and measured between 0.5 and 1.0 cm in diameter. The
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LEE ET AL.
Fig. 1. Schematic presentation of human mandible for the measurements of horizontal and vertical
positions of MdPGC and mental foramen on the pantomogram. MBL, mandibular body length; MBH,
mandibular body height; Xn, mandibular horizontal length from symphysis; Yn, mandibular vertical length
from inferior border of mandibular body.
mental foramen and inferior alveolar canal were separately observed in the anterior mandibular body (Fig. 3).
MdPGCs in Pathological Changes by Benign
and Malignant Tumors
Pantomograms with both benign and malignant lesions
were evaluated. Pantomograms with different benign
lesions, i.e., fibrous dysplasia (n ¼ 3), traumatic bone cyst
(n ¼ 2), odontogenic fibroma (n ¼ 3), and odontogenic
myxoma (n ¼ 2), showed distinctive MdPGCs. There was
no case of destruction or resolution of the MdPGC image.
However, The MdPGCs were slightly displaced in two
cases of odontogenic fibroma. Ten cases of odontogenic
cysts involving the anterior mandibular body area
showed stable MdPGCs, although some MdPGCs were
slightly displaced in three cases of odontogenic keratocyst. On the other hand, malignant lesions, i.e., oral
squamous cell carcinoma (n ¼ 7) and metastatic cancer
(n ¼ 3), showed severe destruction of radiopaque image
of MdPGC by the tumor growth (Fig. 5).
DISCUSSION
The basic growth pattern of the mandibular body and
condyle appears in the 7th week of fertilization. Histologically, the embryonal mandible is originated from pri-
mary intramembranous ossification in the fibrous mesenchymal tissue around the Meckel’s cartilage. From
this initial ossification, the ramifying trabecular bones
develop forward, backward, and upward to form the
symphysis, mandibular angle, and coronoid process of
the mandible, respectively (Lee et al., 2001). Although
the ossification is affected by complicated factors of
endogeneous and exogeneous origins (Morimoto et al.,
1987; Merida-Velasco et al., 1993, 1999; Orliaguet et al.,
1993a, 1993b, 1994; Bach-Petersen et al., 1994; Ishizeki
et al., 1999), the embryonal bones are primarily deposited by intramembranous ossification initiated from the
primary growth center (Pritchett, 1991; Rosati et al.,
1994; Nyska et al., 1995). In the previous studies about
prenatal maxillary and mandibular growth patterns, we
observed the anterior and posterior maxillary primary
growth centers (MxPGCs) and MdPGCs, which have
characteristic radiating trabecular patterns both in the
histological and radiological observations (Lee et al.,
1992, 2001). We also mentioned that the MxPGC and
MdPGC were embryonal initial ossifying sites of jaws,
but they are neither continuously proliferative nor
renewed during the late fetal and postnatal period. They
rather remain as a sclerotic structure with the associated neurovascular tissues.
Even though it was frequently insisted that there is
no direct connection between the Meckel’s cartilage and
embryonal mandible, many authors still believe that the
Meckel’s cartilage, as a core cartilage of first branchial
MANDIBULAR PRIMARY GROWTH CENTER
Fig. 2. Graphs for the measurements of horizontal and vertical
positions of MdPGC and mental foramen during the postnatal period,
ranging from 11 to 79 years. The horizontal ratio of MdPGC (symphysis-MdPGC/mandibular body length) gradually decreased, while the
1237
vertical ratio of MdPGC (inferior border-MdPGC/mandibular body
height) gradually increased. However, the distance between MdPGC
and mental foramen was relatively constant.
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LEE ET AL.
TABLE 1. The average measurements for the position of MdPGC and
mental foramen from 200 pantomograms used in this study
Types
MdPGC (X1, Y1)
Mental foramen (X2, Y2)
Ratio of Xn/mandibular
body length*
0.22 6 0.034
0.3 6 0.034
y
Ratio of Yn/mandibular
body height**
0.37 6 0.061
0.36 6 0.082
*horizontal ratio.
**vertical ratio.
y
unit; ratio (P < 0.005).
The average distance between MdPGC and mental foramen: 9.4 6 1.56 mm (Fig. 2C).
arch, plays some role to induce mandibular growth
(Plessis et al., 1991; Yamasaki et al., 1991; Shum et al.,
1993; Kjaer, 1997; Rodriguez-Vazquez et al., 1997a,
1997b; Trichilis and Wroblewski, 1997; Ishizeki et al.,
1999). It was also reported that the Meckel’s cartilage is
closely associated with the periosteum of the embryonal
mandible, and that the genioglossus muscle is primarily
attached to the Meckel’s cartilage and successively relocated its fusion into the ossifying mandible (Lee et al.,
1990). But the direct histogenetic effect of Meckel’s cartilage for the mandibular development was frequently
debated by many authors (Plessis et al., 1991; Orliaguet
et al., 1994; Rodriguez-Vazquez et al., 1997b; Lee et al.,
2001; Radlanski et al., 2003; Lorentowicz-Zagalak et al.,
2005). In this study, we found that the MdPGC is produced by the intramembranous ossification, and that it
becomes the primary backbone of fetal mandible not
affected by secondary appositional growth of bone by the
tension of functional muscular forces. We also described
that the MdPGC is a relatively rigid structure producing
peripherally radiating trabeculae to form the basic mandibular structures, including symphysis, condyle, coronoid process, and alveolar bone.
These findings lead us to explore the X-ray pantomograms of adults and soft X-ray views of dried adult mandibles preserved for the anatomical teaching. We found
a focal condensed radiopacity, which was easily distinguishable from mental foramen and lingual torus. We
think this condensed radiopacity is identical to the prenatal MdPGC found in the soft X-ray views of fetal mandibles. This radiopaque area could be correlated with
the histological sections of the dried adult mandible,
which diffusely showed sclerosed trabecular bony structure with numerous osteoporotic marrow spaces, but it
was hard to define the spot of MdPGC.
During the mixed dentition, from 7 to 12 years old,
the focal condensed radiopacity was not well defined on
pantomogram due to overlapping with the crowded
mixed dentition. Thereafter, as the mandibular body
rapidly grew from the age of 15 years, the anterior mandibular body increased enough to show the radiopaque
spot. Its trabecular pattern was clearly distinguishable
from the surrounding mandibular bone. In the older-age
group, the radiopaque image was gradually condensed
in the anterior portion of mandible. These facts indicate
that the focal condensed radiopacity of MdPGC may play
a role for the maintenance of mandibular marrow structure during postnatal period.
The gradual decrease of horizontal ratio of MdPGC
during the postnatal period indicates the posterior mandibular body, which grows more backward to produce
prominent mandibular angle. The gradual increase of
vertical ratio of MdPGC indicates that the inferior border of mandible grows more downward than the alveolar
bone, or else the alveolar bony height gradually decreased
as a senile change in the elderly people. These findings
may suggest that the mandibular body grows backward
and downward in contrast to the forward and clockwise
growth of condyle, and conversely when the condensed
radiopaque spot is considered as a landmark of MdPGC
and placed in the center of the mandibular body growth.
It is easily demonstrated that the mandibular body can
grow backward and downward to produce the prominent
mandibular angle and inferior border of mandible, at
which major masticatory and facial expression muscles
are tightly attached. Therefore, we suppose that the condensed radiopaque spot in the anterior mandibular body
is identical to the MdPGC of prenatal mandible and also
plays a central role of mandibular body growth during
the postnatal period.
Particularly the mandible is associated with three different origins of muscle groups, i.e., masseter muscles
originated from the first branchial arch, facial expression muscles originated from the second branchial arch,
and lingual muscles originated from the occipital myotome (Lee et al., 1996; Kuratani et al., 1999). Therefore,
the development of mandible shows heterogeneous morphology, which has been a major debating topic (Maddox
et al., 1998; Ishizeki et al., 1999; Tavakkoli-Jou et al.,
1999; Mina, 2001a, 2001b; Wang et al., 2001). Because
the muscular attachment affects the intramembranous
osteogenesis, and the areas of future muscle attachment
are sites of rapid bone formation throughout the early
formative stages (Gaudino et al., 1995; Lee et al., 2001;
Tan et al., 2002), we also suppose that the sequela of the
MdPGC may persistently play a role for the growth of
mandibular skeletal axis to support the mandibular movement induced by masticatory and facial musculatures.
In the present study using 200 pantomograms and soft
X-ray views of 30 dried adult mandibles, we observed a
condensed radiopaque image, measuring 0.5–1.0 cm in
diameter, below the middle portion of apices of canine
and first premolar. This radiopaque image was clearly
distinguishable from the structures of mental foramen
and lingual torus and showed a conspicuous radiating
pattern. We supposed that it is a remnant of the MdPGC
of prenatal mandible. However, the radiopaque area of
MdPGC was seldom changed in the older person, even
in the edentulous mandible. The odontogenic cysts and
benign tumors hardly destroyed the original structure of
MdPGC, while the primary or metastatic cancer rapidly
destroyed the radiopaque area of MdPGC.
MANDIBULAR PRIMARY GROWTH CENTER
Fig. 3. Soft X-ray views of dried adult mandibles. Oblique lateral view showed the condensed radiopaque image with radiating trabecular pattern (arrows), which was separated from mental foramen (arrowhead). The MdPGC showed conspicuous trabecular pattern (A) or condensed radiopacity (B).
1239
1240
LEE ET AL.
Fig. 4. Pantomograms of normal subjects. Every pantomogram showed the MdPGCs bilaterally in the
anterior mandibular body (arrows). High magnification of the area of MdPGC was also shown in the
square inlet at lower corner.
MANDIBULAR PRIMARY GROWTH CENTER
Fig. 5. Pantomograms of patients involved with different osseous
lesions. A: The MdPGC areas (arrows) were well preserved even though
the extensive swelling of periapical cyst (arrowheads) involved the
whole lower anterior teeth. B: Fibrous dysplasia (arrowheads) involving
the whole right mandibular body was extended near the MdPGC
(arrows), but the radiopaque trabecular pattern was stable compared to
1241
the MdPGC in the left mandibular body (arrows). C: The infiltrative
growth of squamous cell carcinoma (arrowheads) extensively destroyed
not only the mandibular body but also the radiopaque image of MdPGC
(arrows). High magnification of the area of MdPGC was also shown in
the square inlet at lower corner.
1242
LEE ET AL.
ACKNOWLEDGMENTS
The authors thank the donors of human materials.
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