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Morphological Changes in the Mandible of Male Mice Associated With Aging and Biomechanical Stimulus.

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THE ANATOMICAL RECORD 292:431–438 (2009)
Morphological Changes in the Mandible
of Male Mice Associated With Aging and
Biomechanical Stimulus
MARIA LUISA TAGLIARO,1* RAQUEL MATTOS DE OLIVEIRA,1
DALVA MARIA PEREIRA PADILHA,2 SIDIA MARIA CALLEGARI-JACQUES,3
1
AND EMÍLIO ANTÔNIO JECKEL-NETO
1
Morphophysiological Sciences Department, Biosciences Faculty, Pontifical Catholic
University of Rio Grande do Sul (PUCRS), Prédio 12, Av. Ipiranga, 6681,
Porto Alegre, RS, Brazil
2
Hospital São Lucas, Instituto de Geriatria e Gerontologia, Pontifical Catholic University
of Rio Grande do Sul (PUCRS), Av. Ipiranga, 6690, Porto Alegre, RS, Brazil
3
Statistics Department, Federal University of Rio Grande do Sul (UFRGS),
Av. Bento Gonçalves, 9500, Porto Alegre, RS, Brazil
ABSTRACT
Degenerative changes in the temporomandibular joint (TMJ) associated with aging can affect mandibular shape and reduce growth potential
when stimulated by functional appliance therapy. This study was
designed to evaluate the morphological changes in the mandibles of male
mice associated with aging and biomechanical stimulus. Every 3 days
over the course of 1 month, the lower incisors were trimmed by 1 mm to
induce mandibular advancement (MA) when the animal was feeding. The
left mandibles of the 23 experimental and 27 control animals were subsequently dissected, and digital images were obtained to analyze nine linear/angular measurements. Because mandibular morphology depends on
the maintenance of condylar cartilage, the surfaces of the condylar cartilage and the ascending ramus of the mandible were also analyzed by
scanning electron microscopy (SEM). The linear measurements of the
mandible showed changes according to age in the control group and a
growth response in the mandibular condyle in 7- and 15-month-old mice
after MA. Moreover, SEM analysis revealed depressions in the anterior
region of the condylar cartilage and inclined vascular grooves in the
ascending ramus in the 7- and 15-month-old experimental mice. Although
the growth potential is reduced in mice after 6 months of age, the results
showed that continuous growth of the mandible occurs after maturation,
except in the condyle, and that biomechanical stimulus of the TMJ of
male mice leads to condylar growth. These results suggest that mature
and old individuals can favorably respond to maxillary functional orthopedic therapy. Anat Rec, 292:431–438, 2009. Ó 2009 Wiley-Liss, Inc.
Key words: temporomandibular joint; mandible; functional
maxillary orthopedics; condylar cartilage; condyle
During the aging process, the mandible undergoes
several morphological changes because it is a dynamic,
cellular unit (Nomura et al., 2003). For example, the orientation of the osteons in the mandible adapts to the
changes in the masticatory stimuli from the adjoining
masticatory musculature (Nomura et al., 2003). Furthermore, the condylar cartilage, a growth center of the
Ó 2009 WILEY-LISS, INC.
*Correspondence to: Maria Luisa Tagliaro, PhD, Rua Garibaldi, 891/1002, Porto Alegre, RS, Brazil 90035-051. Fax: 15551-3286-1466. E-mail: mltagliaro@terra.com.br
Received 20 November 2008; Accepted 14 October 2008
DOI 10.1002/ar.20861
Published online in Wiley InterScience (www.interscience.wiley.
com).
432
TAGLIARO ET AL.
mandible, becomes thin (Paulsen et al., 1999) with
reduced growth potential due to biochemical changes
(Blumenfeld et al., 1997; Blumenfeld and Livne, 1999)
and diminished cellular activity (Paulsen et al., 1999).
The mandibular condyle of young animals (6–8 weeks) is
characterized by appositional growth, followed by endochondral ossification. In male mice, till 6 months of age,
both appositional and interstitial patterns of cellular
growth occur, and after 6 or 7 months of age, degeneration of the condylar cartilage can be observed, accompanied by unremarkable insterstitial growth that might be
associated with the repair process (Livne et al., 1990).
However, mechanical stimuli in the mandible lead to
muscle responses, neural activation, the enhancement of
growth factors (Petrovic and Stutzmann, 1999), and vascular flow (Rabie et al., 2002). Condylar cartilage and
mandibular bone growth (Petrovic and Stutzmann, 1999;
Rabie et al., 2002), and repair (Tagliaro et al., 2006) are
the results of this stimulation. Furthermore, the growth
response is regulated by the orchestrated influences of
many growth and regulatory factors expressed by cellular components in the mandibular condyle (Rabie and
Hagg, 2002).
Functional Maxillary Orthopaedics is based on the
principle of delivering neural and mechanical stimuli to
the craniofacial complex through bimaxillary appliances
(Simões, 1985), leading to growth responses of condylar
cartilage (Fanghanel and Miehe, 1994; Fuentes et al.,
2003; Rabie et al., 2003a,c; Tang et al., 2004), and the
mandible of young and adult animals (Xiong et al., 2004,
2005). The pterygoid muscle forms a stabilizing system
with the mandibular condyle and the articular capsule
in the temporomandibular joint (TMJ) during mastication. The stimulus of mandibular advancement (MA)
provokes a contraction of the lateral pterygoid muscle,
which changes the functional and biomechanical environment of the TMJ (Takahashi et al., 1995). In 16month-old female mice, application of the MA stimulus
for 30 days results in the enhancement of the length of
the mandible, condylar process, and the mandibular condyle as compared to both a control group of females of
the same age and to 2- and 7-month-old MA-stimulated
female mice (Tagliaro et al., 2006).
In male mice, however, the natural tendencies of mandible growth in the aging process are unclear, and the
analysis of probable growth response and condylar cartilage regeneration after mechanical stimuli at all ages is
important. Thus, the present study compared the morphological changes of the mandible of male mice of different ages during natural growth and after the application of MA stimuli.
Fig. 1. The lower incisors were bilaterally trimmed by 1 mm in the
incisal third to induce mandibular advancement during feeding.
chow ad libitum. The mice were randomly assigned to
either the experimental (N 5 23) or the control (N 5 27)
group. The 2-month-old group was divided into nine experimental individuals and seven controls, the 7-monthold mice into eight experimentals and nine controls and
the 15-month group into 10 experimentals and seven controls. In the experimental group, the lower incisors were
trimmed bilaterally by 1 mm at the incisal third every 3
days, eight times in total, to induce an increase in MA
when the animals were feeding (Fig. 1). The experimental
animals were subsequently examined to confirm that the
contact of the posterior upper teeth and lower teeth was
preserved, weighed to verify whether they ate less during
the experimental period, and examined for any signs of
illness. The animals were euthanized 4 days after the
last trim, the left mandibles were dissected, and the tissues were fixed in 10% paraformaldehyde solution for
24 hr. Trimming procedures and cervical dislocation were
carried out in anesthetized animals (10% ketamine and
2% xylazine, 2:1, 0.1 ml/100 g).
MATERIALS AND METHODS
Animals and Experimental Protocol
This experiment was approved by the Research Ethics
Committee of the Pontifı́cal Catholic University of Rio
Grande do Sul (PUCRS), Brazil.
Fifty male Mus domesticus domesticus CF1 mice
(FEPPS, Fundação Estadual de Produção e Pesquisa em
Saúde do Rio Grande do Sul, Brazil) that were 2, 7, and
15 months of age, were studied. The animals were housed
under standard conditions with a 12-hr light:12-hr dark
cycle and supplied with tap water and standard rodent
Scanning Electron Microscopy
The left mandibular condyles were separated from the
mandible, dehydrated, gold-coated in a Balzers Bal-Tec
SCD-005 sputter coater, and examined using a Philips
XL-30 scanning electron microscope. The descriptive
analysis looked at images of the surface of the mandibular condyle and the ascending ramus. The characteristics observed were signs of condylar cartilage degeneration, the orientation of the vascular grooves in the
433
MORPHOLOGICAL CHANGES IN MANDIBLE
Fig. 2. The mandibular measurements and growth tendencies
related to aging and mandibular advancement. Although the condyle
length (C–D) and width (R–Q) decreased in older control animals, the
length of the condylar process (B–F), and mandible (A–F) and the distance from the point of intersection between the lingual surface of the
lower incisors and its lingual alveolar bone to middle point of the mandibular foramen (A–B) were enhanced. After mandibular advancement,
the C–D length was increased (white arrow) in the oldest group.
ascending ramus, and morphological changes induced by
MA in both structures.
Mandibular Measurements
All measurements were made according to the procedure described by Xiong et al. (2004). The width and
length of the condylar head were directly measured
using a Vernier caliper. The linear measurements were
made by digital imaging of the mandible medial side
(Fig. 2) and consisted of: the length of the condylar process (B–F), mandibular length (A–F), the distance from
the point of intersection between the lingual surface of
the lower incisors and its lingual alveolar bone to the
middle point of the mandibular foramen (A–B), condylar
length (C–D), condylar width (Q–R), the distance from
the most anterior point of the condyle to the mandibular
plane (C–GH), the distance from the intersection point
of the (B–E) extension line and the outer contour of the
condyle to the mandibular plane (F–GH), and the distance from the most inferior and posterior points of the
condyle to the mandibular plane (D–GH). The angle of
the condylar process axis to the mandibular plane (BF/
GH) was also measured. The images were obtained at a
90-degree angle using a Sony DSC-W1 digital camera at
a fixed distance and a 90-drgree angle and analyzed by
Image Pro-plus1 4.1 software.
Fig. 3. A: Weight of individuals in the experimental group (2, 7, and
15 months) at each treatment (events 1–8) and on the day the animals
were euthanized (event e). B: Final weights in the experimental (EG)
and control (CG) groups.
Student’s t-test. SPSSÓ v. 8 software was used for the
statistical analyses.
RESULTS
Body Weight
Statistical Analysis
The changes in linear/angular measurements produced by experimental MA in mice of different ages
were evaluated by multivariate analysis of variance
(MANOVA) using a 2-way model with fixed effects and
interaction. The means of treated and untreated individuals in each age group were compared using the least
significant difference (LSD) criterion and confirmed
by Student-Newman-Keuls (SNK) or Tamhane’s test,
according to the acceptance of homogeneity or heterogeneity of the group variances. The values of the weight
differences among the groups were evaluated using the
Weight loss was observed from the first to the second
trim in 7- (5.9%) and 15- (2.5%) month-old MA mice. In
the 2-month-old experimental group, the weight loss
occurred after trim 3 (2.0%). Over the course of the
experiment, the weight of 7-month-old MA mice was
reduced by 6%, 1.0% (15 months), and the weight of
2-month-old mice increased by 2.5% (Fig. 3A).
The final weights of the 2- and 7-month-old experimental mice were 0.8% and 2.0%, respectively, less than
that of the control mice, whereas 15-month-old MA mice
weighed 3.7% more than control mice of the same age
(Fig. 3B).
434
TAGLIARO ET AL.
The weight differences among the groups were not
statistically significant and no sign of illness was
detected.
Scanning Electron Microscopy
The mandibular ascending ramus in the experimental
group was characterized by inclined vascular grooves,
most likely a result of the MA stimulus, whereas the
grooves were less inclined in control groups of the same
age (Fig. 4A–F). In the posterior region of the mandibular condyles, an elongation of the condylar surface in 7and 15-month-old experimental animals was observed
compared with controls (Fig. 5A–F). Depressions in the
anterior region of the condylar cartilage were accentuated in 7- and 15-month-old experimental mice (Fig.
6A,B).
Linear and Angular Measurements
The mean and standard deviations of the eight linear
and one angular mandibular in individuals of different
ages, in both the control and experimental groups, are
presented in Table 1. Age had a significant effect on all
linear measurements (P < 0.001 for six variables except
C–D and Q–R in which P 5 0.020); no age effect was
observed on angle BF-GH (P 5 0.885). The differences
in all linear measurements of the untreated groups of
all ages were statistically significant although angle BFGH was not. The smallest differences between ages are:
B–F (P < 0.014), A–F (P < 0.003), A–B (P < 0.014), C–D
(P < 0.002), Q–R (P < 0.042), C-GH (P < 0.008), F-GH
(P < 0.023), and D-GH (P < 0.021).
The effects of treatment and of age as well as the
interaction between them were tested using a whole set
of nine variables by MANOVA; all the results were
found to be statistically significant (P 5 0.04; P < 0.001
and P < 0.025, respectively). As for the treatment effect,
MA produced lower averages for D-GH (P 5 0.015), independent of age group (no interaction effect); the C–D
measurement, however, also presented a significant
effect of MA (P 5 0.001) and a significant interaction
among the treatment and age group (P 5 0.003).
For the 7- and 15-month old groups, the average mandibular condyle lengths (C–D) were significantly (P <
0.05) greater than those of controls. The average measurements from treated and control 7-month old mice are
2.26 and 1.91, respectively; for 15-month mice they are
2.04 and 1.79, respectively. There were no statistically
significant differences between the experimental and
control groups for any other variable.
DISCUSSION
The microstructure, morphology, biochemical environment, and the cellular and molecular composition of
bone and cartilage tissues change through the life of an
animal (Weiss et al., 1986; Kloss and Gassner, 2006).
Endogenous and exogenous factors affect the articular
cartilage through mechanical forces (Yamamoto et al.,
2005), and the effects of these factors differ depending
on age for the condylar cartilage of the mandible, the
fibrocartilage of lumbar intervertebral disc, the elastic
cartilage of external ear and the hyaline cartilage of the
xiphoid process. All types of cartilage tend to present
some potential for regeneration in the early stages of
life, followed by a gradual and continuous decline in
metabolic activities (Weiss et al., 1986). Also important
is the distinction between the effects of aging in males
and females. Sex hormones regulate bone metabolism.
For example, in C57BL/6J mice orchiectomized or ovariectomized on the 5th day after birth, both males and
females showed suppressed craniofacial growth, and
these differences suggest an important role for sex hormones in growth control (Fujita et al., 2004). In addition, in humans, biochemical findings (bone loss
markers) and histomorphometric analysis at different
skeletal sites suggests that osteoclast function is preserved during aging in men (Kloss and Gassner, 2006).
This study evaluated the morphological changes of the
mandible and mandibular condyle associated with aging
and the effect of MA, a biomechanical stimulus, in male
mice. In agreement with our previous findings in mice
(Tagliaro et al., 2006), a cephalometric longitudinal
study of humans was performed, and researchers
observed natural and continuous craniofacial bone
growth over a period of 66 years and detected different
patterns of growth for men and women (Behrents, 1993).
These results suggest the potential for growth after mechanical stimulus. In the present study, many linear
measurements of the mandible were enhanced in 7- and
15-month-old male mice compared with controls. However, in the condyle, an important growth center of the
mandible, different effects of age were observed. The
length C–D was diminished in the oldest animals and
the width Q–R was reduced in 7-month-old mice. By
contrast, in 15-month-old mice, the width Q–R was
increased to similar values of the 2-month-old animals
(Table 1). A decrease in the levels of several growth factors and an increase in the levels of pro-inflammatory
cytokines occur in the TMJ. These changes lead to the
reduced growth response and the reduced regenerative
ability of the condylar cartilage of rodents (Livne, 1994;
Livne et al., 1997; Blumenfeld and Livne, 1999; Gepstein
et al., 2002). The enhancement of the linear measurements of the mandibles in control mice observed in this
study can be explained by variations in the calcification
of cranial and facial sutures in young adults and by extrinsic factors such as functional and biomechanical
stimuli (Behrents, 1993).
There were no changes in the direction of condylar
growth in the control group. This observation is confirmed by the measurement averages of angle BF-GH,
which were maintained in the three age groups and by
the significant enhancement from 2 to 15 months of age
in mice in all three linear distances from condylar points
C, F, and D to the mandibular plane (GH). In addition
all measurements were consistent with no modification
of the axial rotation (Table 1). However, in the experimental group, the C–D averages were enhanced in the
7- and 15-month-old mice, and the distance D–GH
diminished independently of age group. These results
confirm the presence of posterior condylar growth, due
to the posterior axial rotation of the mandibular condyle
when the mandible is advanced to incisal contact. Stuzmann and Petrovic (1999) demonstrated that in young
untreated rats, the angle and direction of condylar
growth is in the same direction as the trabecular bone.
However, in mice stimulated by MA (postural hyperpropulsor) or growth hormone (STH), a modification of rotational growth, a different angular direction (BF-GH),
MORPHOLOGICAL CHANGES IN MANDIBLE
435
Fig. 4. Scanning electron microscopy of the mandibular ascending ramus. In 2- (A), 7- (C), and 15- (E)
month-old mandibular advancement mice an elongation characterized by inclined vascular grooves was
observed while the grooves were less inclined in control mice of the same age (B, D, and F).
condylar growth, and new trabecular bone were
observed (Stutzmann and Petrovic, 1999). In the present
study, the condyle of control male mice decreased in
length from 2 to 15 months of age over the course of
natural development. The width was less in 7-month-old
animals compared with 2-month-old animals, and it was
greater in 15-month-old animals compared with 7month-old animals (Table 1). These data are compatible
436
TAGLIARO ET AL.
Fig. 5. Scanning electron microscopy of the condyles. An elongated form was observed in condyles
of the 7- (C) and 15- (E) month-old experimental groups than in 7- (D) and 15- (F) control group. No difference was detected between the 2-month-old treated (A) and control mice (B).
with the fact that condylar cartilage becomes thin in the
oldest mice and that cellular activity is involved in the
repair of cartilage (Livne et al., 1990); however, it does
not explain why the width was increased in 15-month-
old animals. According to Blumenfeld et al. (1997), the
degenerative changes in the condylar cartilage remain
stable in female mice beginning at 12 months of age,
suggesting that 15-month-old mice are metabolically
437
MORPHOLOGICAL CHANGES IN MANDIBLE
(Kobayashi et al., 2002), it could affect the condylar
length but not the width in mice.
The results also showed a significant enhancement in
the length of mandibular condyle in 7- and 15-month-old
mice after MA (Table 1). This protrusive movement
modifies the biophysical and biochemical environment in
the TMJ and increases vascular endothelial growth factor expression (Rabie et al., 2002). As a result, blood-vessels proliferate; mesenchymal cells migrate, chondrogenesis is induced, cartilaginous matrix and type II collagen
synthesis are enhanced, which together promote the formation of new cartilage and bone (Rabie et al., 2003a,b,
2004). By contrast, a morphological study in 7-month-old
female mice showed no condylar growth after 30 days of
MA, although the regeneration of cartilage was observed
by SEM (Tagliaro et al., 2006). In 2-month-old male
mice, MA produced lower, but not significantly different
values, in distance D–GH and in angle BF-GH (Table 1).
This result suggests that the stimulus changed the
activity of the lateral pterygoid muscle modifying the
direction of condylar growth, causing it to become horizontally oriented as justified by the posterior rotation of
the mandible (Stutzmann and Petrovic, 1999). In this
study, the SEM analyses of the ascending ramus showed
a different orientation of vascular grooves in the experimental groups of all ages in comparison with controls.
The grooves are more prominent and follow the direction
of the protrusive movement (Fig. 4). The MA provokes
the contraction of the pterygoid lateral muscle, which
pulls the mandibular condyle to a more forward and
lower position (Petrovic and Stutzmann, 1999) and could
cause a tension remodelling of the vascular grooves in
the ascending ramus. In the 7- and 15-month-old MA
groups, the condyle is elongated in the posterior region,
confirming the significant enhancement of condyle
length in the linear measurements after MA (Fig. 5).
The biomechanical stimulus and the consequent condylar cartilage enhancement mostly occurred in the middle
to posterior region. As a result, the depressions in the
anterior region of the condylar cartilage became pronounced and deep.
It was observed that in 7- and 15-month-old experimental male mice the growth response occurred in the
condyle length and that no significant differences
occurred in the remainder of the mandible (Table 1).
These patterns of growth suggest that the MA stimulus
in 7- and 15-month-old male mice can activate the
growth potential of the condylar cartilage. This step
stable. Therefore, the 15-month-old group could repair
naturally the cartilage and return to the original dimensions of the condyle. Because postero-anterior movements are predominant during the mastication
Fig. 6. Scanning electron microscopy of the anterior region of a
representative condylar cartilage from the 7-month-old group. The
depressions (white arrows) were more accentuated in the experimental
mice (A) than in the control mice (B).
TABLE 1. Mean 6 standard deviation for nine linear (in mm) and angular (in degrees) measurements in the
mandibles of no treated male mice of different ages
Linear (mm)
and angular (8)
variables
B–F
A–F
A–B
C–D
Q–R
C–GH
F–GH
D–GH
BF/GH (8)
2-month-old
control
(N 5 9)
2.91
12.73
10.25
2.07
0.84
6.00
5.88
4.71
40.22
6
6
6
6
6
6
6
6
6
0.22a
0.40a
0.34a
0.18a
0.10a
0.25a
0.24a
0.22a
3.12a
2-month-old
experimental
(N 5 7)
2.94
12.88
10.28
1.99
0.84
5.89
5.65
4.40
36.85
6
6
6
6
6
6
6
6
6
0.18a
0.51a
0.32a
0.13a
0.00a
0.21a
0.19a
0.15a
2.54a
7-month-old
control
(N 5 8)
3.12
13.44
10.80
1.91
0.74
6.12
5.97
4.82
39.06
6
6
6
6
6
6
6
6
6
0.07b
0.19b
0.19b
0.19a,b
0.05b
0.25a
0.31a
0.25a
2.67a
7-month-old
experimental
(N 5 9)
3.03
13.39
10.84
2.26
0.78
6.08
5.85
4.67
38.83
6
6
6
6
6
6
6
6
6
0.20b
0.18b
0.18b
0.20c
0.11b
0.18a
0.21a
1.80a
4.67a
15-month-old
control
(N 5 10)
3.39
13.76
10.81
1.79
0.81
6.50
6.33
5.12
38.10
6
6
6
6
6
6
6
6
6
0.15c
0.60b,c
0.60b
0.15b
0.06a
0.32b
0.38b
0.28b
2.87a
15-month-old
experimental
(N 5 7
3.36
13.84
10.86
2.04
0.83
6.50
6.34
5.04
38.79
6
6
6
6
6
6
6
6
6
Means indicated by the same letter do not differ significantly at 0.05 level in each linear and angular measurement.
0.18c
0.41c
0.26b
0.19a
0.00a
0.31b
0.32b
0.32b
1.20a
438
TAGLIARO ET AL.
precedes bone formation as a morphologic guide for
blood invasion (Rabie and Hagg, 2002), although it may
be necessary to prolong the stimulus to obtain mandibular bone growth.
These data suggest that some mechanisms of growth
exist in the mandibles of male mice during aging. The
linear and angular measurements revealed a continuous
growth of the mandible during the aging process, except
in the condyle, which showed the potential for growth
when induced by a biomechanical stimulus. In addition,
MA induced growth of the mandibular condyle. Thus,
the functional maxillary orthopaedics could be an option
for treating mature and old individuals when mandibular growth and regeneration of the condylar cartilage
are necessary.
ACKNOWLEDGMENTS
We are very grateful to Luisa Maria Gomes de Macedo
Braga, PhD and Patricia Sesterheim MSc for mouse husbandry at FEPPS (Fundação Estadual de Produção e
Pesquisa em Saúde), and to Clı́via Pazin Miwa, Deise Forneck Flores and Marcus Rodrigo Guidoti Soares, undergraduate students of PUCRS, for laboratory assistance.
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