ORIGINAL ARTICLE

Histomorphometric evaluation of alveolar bone

turnover between the maxilla and the mandible
during experimental tooth movement in dogs
Toru Deguchi,a Teruko Takano-Yamamoto,b Toshinori Yabuuchi,c Ryoko Ando,c W. Eugene Roberts,d and
Lawrence P. Garettoe
Okayama and Sendai, Japan, and Indianapolis, Ind

Introduction: The purpose of this study was to quantify the histomorphometric properties of alveolar bone
to identify the characteristics of the changes of quantity and quality of alveolar bone between the maxilla and
the mandible during orthodontic tooth movement in dogs. Methods: A force of 200 to 250 g was applied
from miniature implants to the premolars for either 4 or 12 weeks. Maxillary and mandibular tooth specimens
were embedded and sectioned at 100 ␮m in the sagittal plane for microscopic examination. Results:
Significantly more orthodontic tooth movement was observed for maxillary than for mandibular teeth. The
primary histomorphometric analysis indicated that, after 4 weeks of tooth movement, a marginal increase in
resorptive parameters was associated with a decrease of bone volume at both the tension and compression
sites. On the other hand, after 12 weeks of tooth movement, secondary histomorphometric analysis indicated
an increase in the bone formation rate, resulting in increased woven bone formation, especially at the tension
sites. Conclusions: Clinically, maxillary and mandibular bone responds differently to orthodontic force,
resulting in a significant difference in the amounts of tooth movement. Significant differences in the primary
and secondary histomorphometric indexes between the jaws and at the different time points during
orthodontic tooth movement might affect the amount and rate of tooth movement in orthodontic patients.
Moreover, orthodontic tooth movement is characterized by a regional acceleratory phenomenon, manifested
as increased bone turnover in the alveolar process. (Am J Orthod Dentofacial Orthop 2008;133:889-97)

C
linically, when orthodontic force is applied, the
maxillary teeth tend to move faster than those
in the mandible.1 The relative resistance of
mandibular molars to mesial movement is a well-
known principle of differential mechanics. However, to
the best of our knowledge, no study has quantitatively
compared the amount and the rate of tooth movement
a
Assistant professor, Department of Orthodontics, Okayama University Grad-
uate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama,
Japan.
b
Professor and chair, Division of Orthodontics, Tohoku University Graduate
School of Dentistry, Sendai, Japan.
c
Graduate student, Department of Orthodontics, Okayama University Graduate
School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama, Japan.
d
Professor, Department of Orthodontics and Orofacial Genetics, School of
Dentistry, Indiana University, Indianapolis.
e
Professor, Department of Orthodontics and Orofacial Genetics, School of
Dentistry; Department of Cellular/Integrative Physiology, School of Medicine,
Indiana University, Indianapolis.
Supported by the Special Research Fund for Bone Research Laboratory at
Indiana University School of Dentistry and in part by a Grant-in Aid for
Scientific Research from the Ministry of Education, Science and Culture of
Japan.
Reprint requests to: Lawrence P. Garetto, 1121 W Michigan St, Indianapolis,
IN 46202; e-mail, lgaretto@iupui.edu.
Submitted, August 2006; revised and accepted, December 2006.
0889-5406/$34.00
Copyright © 2008 by the American Association of Orthodontists.
doi:10.1016/j.ajodo.2006.12.013
between the jaws. Structurally, the maxilla has rela-
tively thin cortices interconnected by a network of
trabeculae similar to a vertebral body or an epiphysis.1
The mandible is composed of thick cortices and more
radially oriented trabeculae similar to the diaphysis of a
long bone.1,2 The thin cortices and trabecular bone of the
maxilla might offer less resistance to resorption than the
thick cortices and coarser trabeculae of the mandible.
Generally, the maxilla is loaded predominantly in com-
pression and transfers much of its load to the rest of the
cranium. The mandible, on the other hand, is subjected to
substantial torsional and bending strain. Thus, structural
differences such as geometry and mass of the different
types of bone between the jaws might be a reason for the
different responses to orthodontic force.
If there is a physiologically balanced relationship
between bone formation and resorption of the osseous
tissue, the amount of the alveolar bone surrounding the
teeth does not change during orthodontic tooth move-
ment.3,4 Although the absolute amount of bone mass is
stable during orthodontically induced tooth movement,
the metabolic activity is highly dynamic. Orthodontic
force application is known to increase bone modeling
and remodeling activity in both formation and resorp-
889
890 Deguchi et al
tion areas in rats.3-5 As defined originally by Frost,6,7
bone modeling is an uncoupled process that results in a
net change in size or form of osseous tissue. On the
other hand, bone remodeling is a normally coupled
process of bone turnover of the existing osseous tissue.
In human adults, typical remodeling rates are about 3%
per year for cortical and 24% per year for trabecular
bone.8 The lower rate in mandible occurs because only
the inner portion of the cortex undergoes the intense
turnover of the metabolic fraction, whereas the outer
cortex is protected by mechanical function. The latter is
the support role of cortical bone such as in the case of
the mandible. In the dog mandible, the remodeling rate
is much higher than in the appendicular skeleton.9 Bone
formation rates surrounding teeth are as high as 37%
per year in the coronal region.9 However, no study has
compared actual bone formation rates between the
maxilla and the mandible during orthodontic tooth
movement.
Beyond providing a qualitative view of bone tissue
by light microscope, histomorphometric techniques
enable us to understand the kinetics of bone turnover
and quantify the changes in bone structure at the
cellular level.8-11 Thus, histomorphometric analysis
enables us to quantitatively assess the alveolar bone
response to orthodontic force. There are primary histo-
morphometric indexes and secondary derived histo-
morphometric indexes.10,11 Primary histomorphometric
indexes are measured directly on the histologic section.
Secondary derived histomorphometric indexes can pro-
vide biologically more meaningful information and are
calculated from the primary indexes. In this study, bone
volume/total volume (BV/TV), woven bone volume/
total volume (WV/TV), and erosion surface/bone sur-
face (ES/BS) rate were analyzed as the primary histo-
morphometric indexes, and mineral appositional rate
(MAR), mineralized surface/bone surface (MS/BS)
rate, and bone formation rate (BFR) were analyzed as
secondary histomorphometric indexes.
We hypothesized that significant differences in
bone histomorphometric indexes occur between the
maxilla and the mandible during orthodontic tooth
movement. In addition, for the method of orthodontic
tooth movement, miniature implants were used as
anchorage units to precisely assess the movement of the
teeth.
MATERIAL AND METHODS
In 12 male beagle dogs (age, 8 months), the first
premolars were subjected to orthodontic force for 4
(n ⫽ 4) or 12 weeks (n ⫽ 8). The contralateral side
served as the nonloaded control (n ⫽ 24; 12 for the
maxilla, 12 for the mandible). Forty-eight titanium
American Journal of Orthodontics and Dentofacial Orthopedics
June 2008
Fig 1. Schematic drawing indicates the method of
orthodontic tooth movement. First premolars were dis-
tally moved by implant placed between the roots of third
premolars.
screws (5.0 ⫻ 1.0 mm, Stryker Leibinger, Kalamazoo,
Mich) were placed between the roots of the third
premolars. A force of 200 g was applied with an
elastomeric chain attached from the implant (Fig 1).
Every 2 weeks, the force was calibrated with a force
gauge. Digital radiographs were obtained with the
Schick computer dental radiography program (Schick
Technologies, Long Island, NY) before, every 2 weeks,
and at the end of the study. These digital radiographs
were used to assess the amount of tooth movement. At
3 and 10 days before tissue sampling, a sequence of
fluorochrome labels with tetracycline (Lederle Labora-
tories, American Cyanamid, Pearl River, NY; 10 mg
per kilogram) and calcein green (Sigma Chemical, St
Louis, Mo; 5 mg per kilogram) were administered by
intravenous injection. The study protocol was reviewed
and approved by the Indiana University Review Com-
mittee for Animal Care and Use.
Maxillary and mandibular block specimens were
harvested and dehydrated in an ascending series of
ethyl alcohols and cleared in xylene. The specimens
were infiltrated with methylmethacrylate, containing
3% dibutyl phthalate, in an automatic tissue processor
(Hypercenter XP, Shandon, Pittsburgh, Pa). The em-
bedded specimens were serially sectioned in the sagittal
plane with a saw microtome (Leica 1600, Deerfield,
Mass) and a cutting/grinding system (Exakt Medical
Instruments, Oklahoma City, Okla) to approximately
100 ␮m. Furthermore, microradiographic images were
produced by using a Faxitron (Hewlett-Packard, Bea-
verton, Ore) on high-resolution radiographic plates
(type 649-0, Kodak, Rochester, NY). Microradiographs
were used to measure periodontal ligament (PDL)
width, BV/TV, WV/TV, and ES/BS.
Radiographs taken every 2 weeks were used to
measure the distance of the cusp tip of the first premolar
between the preforce and postforce application by
superimposing at the miniscrew. Replication errors in
duplicate measurements for radiographs were calcu-
lated from the equation:
American Journal of Orthodontics and Dentofacial Orthopedics Deguchi et al 891
Volume 133, Number 6

Table I. Average tooth movement in maxilla and mandible (mm)

2 wk 4 wk 6 wk 8 wk 10 wk 12 wk

Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD

Maxilla (mesiodistal) 0.8 0.4 1.8* 0.6 2.8* 0.6 3.2 0.6 4.5 0.7 5.1 0.6
Mandible (mesiodistal) 0.4 0.3 0.6 0.2 1.9 0.4 2.9 0.4 4.1 0.6 4.7 0.5
Maxilla (intrusion) 0.3 0.1 0.6 0.1 1.5 0.4 2.4* 0.3 2.7* 0.2 3.1* 0.4
Mandible (intrusion) 0.2 0.1 0.5 0.1 1.3 0.5 1.5 0.3 1.7 0.3 1.9 0.3

*Statistically significant compared with the mandible.

Sx ⫽ 冑 兺D2
2N
surface/bone surface (MS/BS%: [(double label int. ⫹
1/2 single label int.) ⫻ 100]/bone surface).

where Sx is the error of the measurement, D is the
difference between duplicated measurements, and N is
the number of double measurements.12 Error of mea-
surement was 0.12 mm in this analysis.
Histomorphometric analysis was performed on an
epifluorescent microscope (FXA, Nikon, Melville, NY)
by using stereologic point-hit and linear-intercept
methods at magnification of 100 times with a 10 ⫻ 10
point ocular square grid.13 Thus, the static variables
(BV/TV, WV/TV, ES/BS) were calculated under 100-
times magnification. Dynamic variables were calcu-
lated by using the fluorescent labels administered at
specific times to allow calculation of rates of change.
Interlabel distance was measured at 250-times magni-
fication. Histomorphometric measurements and calcu-
lations followed standard nomenclature and formu-
lae.8,10,11 A line bisecting the roots longitudinally and 3
lines perpendicular to this line at the cervical, midpoint,
and apical levels were drawn. Then, the alveolar
surface within 1.5 mm that directly faced the PDL was
equally divided into 2 regions (Fig 1). The results
indicated significantly reduced PDL width at the cervi-
cal area (maxilla, 130.0 ⫾ 21.3 ␮m; mandible, 121.1 ⫾
14.1 ␮m) and increased PDL width at the apical area
(maxilla, 279.4 ⫾ 18.2 ␮m; mandible, 235.8 ⫾ 11.1
␮m) compared with the control (maxilla, 188.1 ⫾ 19.0
␮m; mandible, 176.3 ⫾ 18.8 ␮m) after 4 weeks of
orthodontic tooth movement. Thus, the cervical area
was considered the compression area and apical area
the tension area.
Formulas for the derived histomorphometric in-
dexes are as follows: bone volume (BV/TV%: bone
hits/total hits ⫻ 100), woven bone volume (WV/TV%:
woven bone hits/total hits ⫻ 100), erosion surface
(ES/BS%: erosion surface hits/total hits ⫻ 100), bone
formation rate (BFR% per year: MAR ⫻ MS/BV ⫻
100 ⫻ 365), mineral appositional rate (MAR ␮m per
day; interlabel width per 7 days), and mineralizing
Statistical analysis
Analysis of variance (ANOVA) models were used
to examine the effects of area and application of force
on the histomorphometric indexes of the maxilla and
the mandible. The model comparison, corrected for a
random dog effect, was used to correlate all measure-
ments from the same dog as well as fixed effects for
controls and force application, duration, location (max-
illa or mandible). Comparisons were made by using the
Fisher protected least significant differences method to
control the overall significance level at 5%. All histo-
morphometric data are presented as average ⫾ the
standard deviation.
RESULTS
For orthodontic tooth movement, implants were
used as an anchor unit (the results describing the
physiological response of the bone to these implants
was previously reported14). In addition, by comparing
the radiographs and the cast models taken before and
after experimental tooth movement, there was no sig-
nificant change in the control teeth.
The amount of tooth movement was compared
between the maxilla and the mandible from 2 to 12
weeks after the start of orthodontic tooth movement. A
significantly higher rate in the mesiodistal direction was
found at 4 and 6 weeks in the maxilla (P ⬍0.001; Table I)
compared with that in the mandible in distal direction.
On the other hand, significantly higher amounts of
intrusion were found in the maxilla compared with the
mandible at 8, 10, and 12 weeks (P ⬍0.001; Table I).
Significant differences in the bone-labeling pattern
were observed between the control, the 4-week, and the
12-week (Fig 2) groups from the low magnification
photographs. In the control teeth, only a few bone
labels were observed in the cervical (Fig 3, a) and the
apical (Fig 3, b) areas. After 4 weeks of orthodontic
tooth movement, a significant increase in bone labeling
892 Deguchi et al American Journal of Orthodontics and Dentofacial Orthopedics
June 2008

Table II. Histomorphometric parameter

Control 4 wk

Maxilla Mandible Maxilla Mandible

Compression Tension Compression Tension Compression Tension Compression Tension

Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD

BV/TV (%) 55.1 10.5 59.5 9.2 63.9 7.1 63.3 8.2 43.2 17.9 47.5 10.2 55 14.8 58.8 6.9
ES/BS (%) 17.9 8.3 14.4 7.2 16.3 8.7 10.6 7.1 68.6 15.1 61.3 15.9 46 26.7 38.1 16.5
WV/TV (%) 11.7 6.3 10.1 4.9 9.1 3.3 8.4 3.4 26.6 8.2 24.9 7.7 22.2 10.5 21.5 9.7
MAR (␮m) 2 0.7 2.4 0.8 2.3 0.6 2.2 0.7 2.5 0.5 2.5 0.7 2.3 0.4 2.2 0.4
MS/BS (%) 22.2 9.8 12.6 6.7 19.8 6.9 10.1 3.8 40 20.3 31.8 10.9 24.5 11.4 32.4 23.1
BFR (%) 37.2 12.5 32.6 16.4 25.6 10.1 20.6 7.6 128 55.6 143 48.3 106 37.7 116 36.1

*Significant difference vs control.

†
Significant difference within area (compression vs tension).

on the fluorescent micrographs (Fig 3, h). These resorp-

Fig 2. Fluorescent low-magnification photographs of
distal root of the first premolar after 12 weeks of
orthodontic tooth movement. Bone modeling (arrows) at
the tension areas and remodeling (arrow heads) in the
alveolar bone are clearly shown at 12 weeks after
experimental tooth movement.
was observed at both compression (Fig 3, c) and
tension (Fig 3, d) areas. There was also a significant
increase in bone labeling at 12 weeks after orthodontic
tooth movement in the compression (Figs 2 and 3, e)
and especially in the tension (Figs 2 and 3, f ) areas. In
the 4-week group, resorptive lacunae were observed in
the alveolar bone at the compression area (Fig 3, g), and
osteoclasts were observed in these resorptive lacunae
tive lacunae were significantly reduced with increased
woven bone formation after 12 weeks of force appli-
cation (Fig 3, i and j).
There were no significant differences in the BV/TV
throughout the experimental periods between the 4- and
12-week groups and the control in all areas (Table II).
No significant difference was observed between the
compression and tension areas in all groups (Table II).
ES/BS at 4 weeks tended to be higher in all groups
compared with the control. ES/BS tended to be higher
at 4 weeks compared with 12 weeks in both areas in the
maxilla. At 12 weeks, only the compression area
showed a significantly higher ES/BS than the controls
(P ⬍0.05; Table II).
At 12 weeks in the mandible, a significantly higher
ES/BS was observed at the compression area compared
with the tension area (P ⬍0.01; Table II).
ES/BS tended to be higher in the maxilla than in the
mandible in both areas at 4 weeks (Table II).
At 4 weeks, WV/TV tended to be higher compared
with the control in both areas. At 12 weeks, it showed
a significantly higher WV/TV compared with the con-
trols in all areas (P ⬍0.001; Table II). At 12 weeks,
WV/TV tended to be higher than at 4 weeks in the
tension areas in both jaws.
Significantly more WV/TV was observed at the
tension area than in the compression area at 12 weeks
(P ⬍0.001; Table II).
Significantly higher MAR was observed at 12
weeks in the tension areas compared with the control; it
tended to be higher than the 4-week tension areas in
both the maxilla (P ⬍0.05) and the mandible (P ⬍0.01;
Table II).
At 12 weeks in the mandible, a significantly higher
MAR was observed at the tension area than in the
compression areas (P ⬍0.05; Table II).
American Journal of Orthodontics and Dentofacial Orthopedics Deguchi et al 893
Volume 133, Number 6

Table II. Continued

12 wk

Maxilla Mandible

Compression Tension Compression Tension

Mean SD Mean SD Mean SD Mean SD

48.2 8.1 52.5 11 59.2 9.5 64.5 5.4

38.6* 21.4 24.3 6.7 49.3*† 20.3 26.1 20.8
34.9*† 6.5 51.2* 11 30.9*† 10.7 49.7* 10
2.7 0.9 3.2* 0.5 2.5 0.3 3.4*† 0.5
38.1* 20.5 63.3*† 12.6 29.6 13.3 45.8*† 11.5
147.2* 29.7 208.7*† 57.6 132* 40.1 191.5*† 78

At 4 weeks, MS/BS tended to be higher in the
maxillary and mandibular tension areas compared with
the control (Table II). At 12 weeks, significantly higher
MS/BS was observed in the maxillary compression
(P ⬍0.05) and tension areas (P ⬍0.001), and in the
mandibular tension areas (P ⬍0.001) compared with
the controls (Table II).
At 12 weeks, in both the maxilla and the mandible,
significantly higher MS/BS was observed in the tension
areas than in the compression areas (P ⬍0.05).
BFR was significantly higher in all areas of the
12-week groups compared with the controls (P ⬍0.001;
Table II). BFR also tended to be higher in all areas in
the 4-week group than the control. BFR in the tension
areas at 12 weeks tended to be higher than at 4 weeks
in both jaws.
Higher BFR was observed in the tension areas than
in the compression areas at 12 weeks (P ⬍0.01; Table II).
DISCUSSION
In this study, the BFRs averaged 34.9% per year in
the maxilla and 23.1% per year in the mandible in the
control. When evaluated independently, MAR and
MS/BS showed similar patterns as the BFR. The
alveolar BFR is approximately 20% per year in the dog
mandible.9 However, no study has shown the actual
BFR in the dog maxilla. In our study, the maxilla had
a higher BFR than did the mandible. The actual
percentage of bone formation was substantially higher
in alveolar bone than in cortical bone at other sites in
the body. We speculate that the reason for this high
BFR in alveolar bone in the physiologic circumstance
might be elevated peak strains due to functional load-
ing. Alternatively, the increased surface area of trabec-
ular bone in the maxilla might be more susceptible to
hormonal or marrow-induced remodeling.1,15,16 From a
histologic perspective, some bone labeling was in the
alveolar bone (data not shown), and only a few labels
were observed along the PDL surface of the alveolar
bone in the control dogs. The former bone labeling is
consistent with remodeling and later with modeling.1,9
Several studies analyzed the proportion or the rates of
modeling and remodeling sites in rat vertebra and
tibia.17,18 In our study, most bone labels were observed
in the alveolar bone that was considered to be remod-
eling in the control dogs. However, to distinguish
whether the bone labels are modeling or remodeling, a
surface- staining technique was necessary to visualize
the cement (arrest) lines. Furthermore, even with ce-
ment-line stain, there is no reliable way to determine
how old a cement line is. Thus, a future investigation is
necessary to precisely differentiate whether bone labels
in the alveolar process during orthodontic tooth move-
ment are modeling or remodeling.
In this study, progressive tooth movement occurred
approximately 2 weeks faster in the maxilla than in the
mandible in the distal direction. Furthermore, the maxil-
lary teeth were intruded twice as much as the mandibular
teeth during 12 weeks of orthodontic loading. One reason
for faster tooth movement in the maxilla might be because
the maxilla is composed of relatively thin cortices com-
pared with the mandible. However, from the histomor-
phometric analysis, significantly greater ES/BS was ob-
served in the 4-week maxilla compared with the mandible
at the same time, when the most significant difference
between the maxillary and mandibular teeth in the amount
of tooth movement was observed. Thus, the faster tooth
movement was in the maxilla because of the higher rate of
bone resorption, initiating more rapid bone turnover com-
pared with the mandible. Therefore, our findings suggest
that not only the anatomic difference but also the physi-
ologic response can differ between the jaws from mechan-
ical force.
In this study, significant changes in the histomor-
phometric indexes at the compression and tension areas
were observed during orthodontic tooth movement.
894 Deguchi et al American Journal of Orthodontics and Dentofacial Orthopedics
June 2008

R R
R
AB AB AB
AB R
PDL

PDL PDL
PDL

a b c d

R R
g h

PDL
AB PDL AB
i
e f j
Fig 3. Fluorescent micrographs show bone labels in first premolars of control (a, b) compared with
4 (c, d, g, h) and 12 (e, f, i, j) weeks after orthodontic force application. With higher magnification
by microradiographs, resorptive lacunae (arrows in g) along with osteoclasts by fluorescent
micrographs (arrows in h) were observed in compression areas. Resorptive lacunae were signifi-
cantly reduced (arrows in i), and increase of woven bone (arrows in j) was observed by
microradiographs. AB, alveolar bone; R, root; PDL, periodontal ligament. Bars indicate 50 ␮m.

There was no statistically significant difference in
BV/TV; however, BV/TV from the 4-week group
showed a marginal decrease as a result of a resorptive
phase at the early stage of orthodontic tooth movement.
This is consistent with the results that a significant
increase in ES/BS was observed compared with the
control in this study. These data confirm the conven-
tional understanding that, during the early phase of
orthodontic tooth movement, alveolar bone resorption
is prominent and results in a decreased bone volume at
American Journal of Orthodontics and Dentofacial Orthopedics
Volume 133, Number 6
later stages of the tooth movement.19 After 12 weeks of
orthodontic tooth movement, BV/TV tended to return
to the control level, and ES/BS significantly decreased
compared with the 4-week. Instead of osseous resorp-
tion, the formation process predominantly occurred in
alveolar bone at the later stage of the orthodontic
movement, resulting in an increase of BV/TV to the
control level.
A significant increase in the percentage of WV/TV
was observed in both the 4-and 12-week periods
compared with the controls for both areas. WV/TV
indicates bone formation that results in change in the
quality of bone. In normal circumstances, there was
approximately 5% of woven bone in the dog alveolar
bone. This WV/TV seems to be more than for adult
humans (approximately 2%).20 The reason for this high
rate of WV/TV might be related to the age of the dogs
we used. When the force is applied to the teeth, WV/TV
increased up to about twice as much after 4 weeks, and,
at 12 weeks, it increased to 3 to 4 times that of the
control. Furthermore, the 12-week groups had signifi-
cantly more woven bone compared with the 4-week
groups, especially at the tension areas, indicating in-
tense bone formation. In addition, from a dynamic
perspective, after 4 and 12 weeks of tooth movement,
significant increases in BFR of approximately 100% to
150% per year in the compression areas and up to 200%
per year in the tension areas were observed—ie, 3 to 4
times as much as the control. In contrast with our
findings in dogs, previous reports in rats found a
significant increase in BFR at 1 day and a significant
decrease at 3 days in the compression areas, and a
significant increase in the tension areas 7 days after
experimental tooth movement.3
Furthermore, MAR in that study resulted in in-
creases at 7 and 14 days but not at 10 days at the tension
site, and increases in MS/BS at 3 days in the compres-
sion site, and at 7 and 10 days at the tension site after
experimental tooth movement.3 MAR is considered a
measure of osteoblast activity, and a mineralizing
surface is the proportion of a surface that is active in
mineralization at a given time. Thus, the increases in
MAR and MS/BS indicate active bone formation at
given sites. In this study, MAR increased only at the
tension sites in both jaws compared with the control
after 12 weeks of orthodontic tooth movement. MS/BS
also significantly increased at 12 weeks after orthodon-
tic tooth movement in the tension site compared with
the control and in the compression sites in both jaws.
Therefore, from these results, the increase of osteo-
blasts might have resulted in the change of mineraliza-
tion of the alveolar bone at the tension sites at a later
stage of orthodontic tooth movement. The inconsistent
Deguchi et al 895
results of the previous rat study could be related to the
difficulty in producing a consistent force in such small
teeth or a difference in the physiologic state of the
bone, such as the lack of Haversian remodeling.17,21,22
“Modeling” and “remodeling” have been defined
previously.1,8,9,17,18 The remodeling events are defined
as turnover or internal restructuring of previously
existing bone. It is a coupled process: activation ¡
resorption ¡ formation, with resorption preceding
formation. Because of this, a remodeling site must be
defined as having a scalloped arrest line or an inter-
rupted collagen structure indicating previous bone re-
sorption. In this study, the bone label was predomi-
nately observed in the intracortical bone of the control
and the 4-week groups. Moreover, under polarized light
microscopy, a different orientation of collagen fibers
compared with the adjacent bone was mainly observed
in the bone labels at the intracortical bone areas. On the
other hand, modeling is a change in shape or size of
previously existing bone. Anabolic modeling is an
uncoupled process, meaning that bone formation starts
without a need for bone resorption as a prior and
required step.23 But modeling can be either anabolic or
catabolic. Bone resorption and formation can occur
independently or in a closely coordinated pattern. From
a histologic perspective, after 12 weeks, the bone labels
were mainly observed along the PDL surface of the
alveolar bone at the tension area in contrast to the
control. Thus, the alveolar process at the tension area,
after 12 weeks of continuous force application, was
characterized by a significant increase in bone model-
ing rather than remodeling, as evidenced by increased
woven bone formation. This hypothesis is consistent
with Frost’s mechanostat theory—that force exceeding
the minimal effective strain results in a hypertrophic
increase in modeling and a concomitant decrease in
remodeling.24 In addition, a decrease in bone volume at
the initial stage followed by an increase at a later stage
of orthodontic tooth movement might be the result of
the regional acceleratory phenomenon described by
Frost.25 A regional acceleratory phenomenon is an
elevation in remodeling observed during wound heal-
ing after surgical procedures such as implant place-
ment.1 The intensity of the response progressively
decreases as the distance from the surgical site in-
creases. Thus, we suggest that orthodontic tooth move-
ment is a variation of skeletal wound healing and
adaptation, characterized by an elevated bone remod-
eling response in addition to the increase of woven
bone formation associated with a widened PDL.
From our results, we confirmed that there is a
significant difference in the histomorphometric in-
dexes, such as the BFR between the tension and
896 Deguchi et al
compression sites and among different time points after
orthodontic tooth movement. In the past, many studies
indicated that bone metabolism has a significant influ-
ence in bone modeling or remodeling that affects the
rate of tooth movement.15,16,26 The rate of tooth move-
ment is influenced by several factors, including sys-
temic hormone balance. Thus, a patient’s bone metab-
olism (BFR) may be key to effective tooth movement.
Moreover, from our results of different amount of tooth
movement, a significant difference was noted between
the jaws. Our findings— eg, the difference in the bone
turnover rate between the jaws—indicate that the max-
illa and the mandible respond differently to orthodontic
force. Therefore, in patients with postmenopausal os-
teoporosis, especially in the maxilla with its higher
tendency of BFR, different types and methods of tooth
movement might be required. Further investigation is
necessary to elucidate the clinical significance in pa-
tients with different bone turnover rates.
CONCLUSIONS
1. A significantly greater amount of tooth movement
was observed in the maxillary teeth compared with
the mandibular teeth during 12 weeks of orthodon-
tic tooth movement.
2. Results from the primary histomorphometric indexes
(BV/TV, WV/TV, and ES/BS) indicated a temporal
decrease of bone volume at the early phase of orth-
odontic tooth movement and an increase in resorption
activity. However, the increased woven bone forma-
tion (30% to 50%) enabled the maintenance (50% to
60%) of bone volume throughout active orthodontic
tooth movement.
3. From the results from the secondary histomorphomet-
ric indexes (MS/BS, MAR, and BFR), an approxi-
mately 10% higher bone turnover rate was observed
in the maxilla compared with the mandible in the
control. After the start of orthodontic tooth movement,
a significant increase of BFR was observed at the
tension sites (up to 200%) compared with the com-
pression sites (100% to 150%). Localized bone for-
mation at the tension areas and resorption at the
compression areas were observed at later stages (12
weeks) of orthodontic tooth movement.
4. From both primary and secondary histomorphomet-
ric indexes, orthodontic tooth movement is charac-
terized by a regional acceleratory phenomenon that
appears to be a variation of the skeletal wound
healing and adaptation response.
We thank Patsy Dunn-Jena and Irina Leyvand for
technical assistance and George Eckert for statistical
American Journal of Orthodontics and Dentofacial Orthopedics
June 2008
assistance. We dedicate this article to Dr Harold Frost,
scholar, mentor, and friend.
REFERENCES
1. Roberts WE. Bone physiology, metabolism, and biomechanics in
orthodontic practice. In: Graber TM, Vanarsdall RL Jr, editors.
Orthodontics, current principles and techniques. St Louis:
Mosby-Year Book; 2000. p. 193-257.
2. Roberts WE, Arbuckle RA, Analoui M. Rate of mesial transla-
tion of mandibular molars using implant-anchored mechanics.
Angle Orthod 1996;66:331-8.
3. King GJ, Keeling SD, Wronski TJ. Histomorphometric study of
alveolar bone turnover in orthodontic tooth movement. Bone
1991;12:401-9.
4. Vignery A, Baron R. Dynamic histomorphometry of alveolar
bone remodeling in the adult rat. Anat Rec 1980;196:191-200.
5. Verna C, Melsen B. Tissue reaction to orthodontic tooth move-
ment in different bone turnover conditions. Orthod Craniofac Res
2003;6:155-63.
6. Frost HM. Skeletal structural adaptations to mechanical usage
(SATMU): 1. Redefining Wolff’s law: the bone modeling prob-
lem. Anat Rec 1990;226:403-13.
7. Frost HM. Skeletal structural adaptations to mechanical usage
(SATMU): 2. Redefining Wolff’s law: the remodeling problem.
Anat Rec 1990;226:414-22.
8. Parfitt AM. Stereologic basis of bone histomorphometry: theory
of quantitative microscopy and reconstruction in the third dimen-
sion. In: Recker RR, editor. Bone histomorphometry. Techniques
and interpretations. Boca Raton, Fla: CRC Press; 1983. p. 53-88.
9. Garetto LP, Tricker ND. Bone remodeling surrounding implants.
In: Garetto LP, Turner CH, Duncan RL, Burr DB, editors.
Bridging the gap between dental and orthopaedic implants.
Indianapolis: Indiana University School of Dentistry; 2002.
p. 89-99.
10. Takahashi H. Definition and abbreviation of histomorphometric
parameters of trabecular and cortical bones. In: Takahashi H,
editor. Handbook of bone morphometry. Niigata, Japan: Nish-
imura; 1984. p. 71-9.
11. Eriksen EF, Axelrod DW, Melsen F. Bone histology and
histomorphometry. In: Eriksen EF, Axelrod DW, Melsen F,
editors. Bone histomorphometry. New York: Raven Press;
1994. p. 33-48.
12. Dahlberg G. Statistical methods for medical and biological
students. London, United Kingdom: George Allen & Unwin;
1940. p. 122-32.
13. Kimmel DB, Jee WS. Measurements of area, perimeter, and
distance: details of data collection in bone histomorphometry. In:
Recker RR, editor. Bone histomorphometry. Techniques and
interpretation. Boca Raton, Fla: CRC Press; 1983. p. 89-108.
14. Deguchi T, Takano-Yamamoto T, Kanomi R, Hartsfield JK Jr,
Roberts WE, Garetto LP. The use of small titanium screws for
orthodontic anchorage. J Dent Res 2003;82:377-81.
15. Tanaka M, Ejiri S, Toyooka E, Kohno S, Ozawa H. Effects of
ovariectomy on trabecular structures of rat alveolar bone. J
Periodontal Res 2002;37:161-5.
16. Jerome CP. Hormonal therapies and osteoporosis. ILAR J
2004;45:170-8.
17. Chow JW, Badve S, Chambers TJ. Bone formation is not coupled
to bone resorption in a site-specific manner in adult rats. Anat
Rec 1993;236:366-72.
18. Erben RG. Trabecular and endocortical bone surface in the rat:
modeling or remodeling? Anat Rec 1996;246:39-46.
American Journal of Orthodontics and Dentofacial Orthopedics
Volume 133, Number 6
19. Verna C, Zaffe D, Siciliani G. Histomorphometric study of bone
reactions during orthodontic tooth movement in rats. Bone
1999;24:371-9.
20. Garetto LP, Chen J, Parr JA, Roberts WE. Remodeling dynamics
of bone supporting rigidly fixed titanium implants: a histomor-
phometric comparison in four species including humans. Implant
Dent 1995;4:235-43.
21. Frost HM. Some concepts crucial to the effective study of bone
turnover and bone balance in human skeletal disease and in
experimental models of skeletal physiology and pathophysiology.
In: Jaworski ZF, editor. Proceedings of the First Workshop on Bone
Morphometry. Ottawa: University of Ottawa Press; 1976. p. 219-23.
Deguchi et al 897
22. Baron R, Tross R, Vignery A. Evidence of sequential remodeling in
rat trabecular bone: morphology, dynamic histomorphometry, and
changes during skeletal maturation. Anat Rec 1984;208:137-45.
23. Frost HM. Bone modeling and skeletal modeling errors. Spring-
field, Ill: Charles C. Thomas Publishers; 1973.
24. Frost HM. Intermediary organization of the skeleton. Vols I and
II. Boca Raton, Fla: CRC Press; 1986.
25. Frost HM. The regional acceleratory phenomenon: a review.
Henry Ford Hosp Med J 1983;31:3-9.
26. Yamashiro T, Takano-Yamamoto T. Influences of ovariectomy
on experimental tooth movement in the rat. J Dent Res 2001;80:
1858-61.