ONLINE ONLY

Effect of 8-hour intermittent orthodontic force on

osteoclasts and root resorption
Tomoko Kumasako-Haga,a Tetsuro Konoo,b Kazunori Yamaguchi,c and Hidetetsu Hayashid
Kitakyushu, Japan

Introduction: The duration of force application is an important factor in optimizing orthodontic tooth move-
ment with less root resorption. It has previously been shown that the amount of tooth movement achieved
by 8-hour intermittent force application exceeds what would be the expected by the duration. The purpose
of this study was to compare osteoclast recruitment and the extent of root resorption in response to an 8-
hour intermittent force regimen with those from a continuous force. Methods: Rat molars (n 5 110) were as-
signed to 3 groups: 8-hour intermittent force, continuous force, and control. A coil spring that exerted 40 cN of
force was suspended between the maxillary first molars and the incisors. At 1, 3, 5, 7, and 14 days, osteoclast
numbers, osteoclast surfaces, and root resorption were quantified histomorphometrically in the undecalcified
sections and statistically analyzed. Results: At the mesial sites, osteoclast numbers in the intermittent force
group were 100.5% of the continuous force group, and osteoclast surfaces in the intermittent force group were
68.2% of the continuous force group. At the mesial sites, root resorption of the intermittent group was approx-
imately 30.0% of the continuous group (P \0.01). Conclusions: Our results show that an 8-hour intermittent
force efficiently recruits osteoclasts while causing minimal root resorption. (Am J Orthod Dentofacial Orthop
2009;135:278.e1-278.e8)

of the applied force.3 Continuous force is applied in

O
ne goal of clinical orthodontists is to efficiently
move teeth while limiting root damage. Root
resorption is an undesirable side effect of or-
thodontic treatment. Since Ketcham1,2 first reported
the problem, many studies have clarified various factors
affecting root resorption related to orthodontic tooth
movement.
The relationship between root resorption and bio-
mechanical treatment factors such as magnitude, dura-
tion, direction, and type of force (eg, intermittent and
continuous), and amount of tooth movement is unclear.
It is important to control risk factors to prevent root
resorption. These factors can be controlled by the ortho-
dontist. Orthodontic forces can be classified as continu-
ous, intermittent, and interrupted based on the duration
From Kyushu Dental College, Kitakyushu, Japan.
a
Postgraduate student, Department of Growth and Development of Functions,
Division of Orofacial Functions and Orthodontics.
b
Assistant professor, Department of Clinical Communication and Practice,
Division of Comprehensive Dentistry.
c
Professor and head, Department of Growth and Development of Functions,
Division of Orofacial Functions and Orthodontics.
d
Research fellow, Department of Growth and Development of Functions, Divi-
sion of Orofacial Functions and Orthodontics.
Partly supported by a grant in aid (14571959) from the Japan Society for the Pro-
motion of Science and the Support Committee of Kyushu Dental College.
Reprint requests to: Tetsuro Konoo, Department of Clinical Communication and
Practice, Division of Comprehensive Dentistry, Kyushu Dental College, 2-6-1
Manazuru, Kokurakita-ku, Kitakyushu, 803-8580, Japan; e-mail, tetsuro@
kyu-dent.ac.jp.
Submitted, December 2007; revised and accepted, April 2008.
0889-5406/$36.00
Copyright 2009 by the American Association of Orthodontists.
doi:10.1016/j.ajodo.2008.04.019
orthodontic treatment with multiple bracket systems.
However, functional appliances, headgear, and inter-
maxillary elastics can be used to exert intermittent
forces. Intermittent force systems decline to zero
when a removable appliance is removed.3,4
Oppenheim5 suggested that intermittent force was
suitable for tooth movement, because it provided
a rest period to allow reconstruction of the periodontal
tissues. Reitan4,6 and Brudvik and Rygh7 suggested
that discontinuation or reduction of orthodontic force
stops active root resorption and starts the healing pro-
cess. Recent studies indicated that the rest period in
tooth movement with intermittent forces might allow
the resorbed cementum to heal and prevent further re-
sorption.8-12 Maltha et al13 reported that an intermittent
force (16 hours per day) resulted in significantly less
root resorption than a continuous force in dogs. They
stated that teeth in the intermittent force group moved
over a shorter distance, and this might also explain the
less severe root resorption. On the other hand, a risk fac-
tor of root resorption is the amount of tooth move-
ment.14,15 However, there is little information on the
direct relationship between the amount of tooth move-
ment and root resorption, compared with intermittent
and continuous forces in the same experimental system.
In our previous studies, we generated effective tooth
movement by applying intermittent forces in rats using
a standard force by modifying the method of King
et al.16 Konoo et al17 reported that a 1-hour intermittent
278.e1
278.e2 Kumasako-Haga et al
force could stimulate osteoclasts, but tooth movement
did not occur. Hayashi et al18 reported that the tooth
movement induced by 8 hours of intermittent force
was 65.9% of that induced by a continuous force; this
exceeded the expected amount that was predicted by
the duration (33.3%) of force application. Therefore,
we concluded that 8-hour intermittent force is more ef-
fective for orthodontic tooth movement compared with
continuous force. But the reasons for effective tooth
movement, root resorption, and osteoclast recruitment
caused by continuous and intermittent forces were not
clear. In addition, few studies have been done on the
direct relationship between the amount of tooth
movement and root resorption with intermittent and
continuous forces in the same experimental system.
We recently examined the molecular changes of an
8-hour intermittent force on cultured human periodontal
ligament (PDL) cells and showed that it induced the ex-
pression of receptor activator of nuclear factor-kappaB
ligand (RANKL), which plays an important role in
recruitment of osteoclasts to the PDL.19
The purposes of this study were to investigate the re-
action of continuous and intermittent forces, and to
compare the severity of root resorption and the effec-
tiveness of bone resorption induced by 8-hour intermit-
tent and continuous forces.
MATERIAL AND METHODS
The experimental protocol was reviewed and ap-
proved by the Animal Care Committee at Kyushu Dental
College in Japan. Fifty-five male Sprague-Dawley rats
(35-41 days old) were acclimatized for at least 2 weeks
under the experimental conditions. During the experi-
mental period, the rats were maintained on a 12-hour
light/dark cycle and fed a diet softened with tap water
and powdered feed (Clea Japan, Tokyo, Japan).
The rats were weighed and anesthetized with an in-
tramuscular injection of ketamine (Nomopain, Daiichi
Pharmaceutical, Montvale, NJ; 33 mg/kg) and xylazine
(Celactal, Bayer Yakuhin, Osaka, Japan; 67 mg/kg). Or-
thodontic cleats were bonded bilaterally to the occlusal
surfaces of all acid-etched maxillary first molars with
orthodontic adhesive materials. A band with a soldered
hook was fixed to the maxillary incisors. All mandibular
first and second molars were extracted to prevent occlu-
sal interference. The mandibular incisors were reduced
slightly to prevent band damage. At this point (66 days
old), when the rats were allowed to recover for 2 weeks,
110 molars of 55 rats were randomly divided into con-
trol (30 molars of 15 rats), continuous force (40 molars
of 20 rats), and intermittent force (40 molars of 20 rats)
groups.
American Journal of Orthodontics and Dentofacial Orthopedics
March 2009
In the continuous and intermittent forces groups,
mesial movement of the molars was performed as de-
scribed by King et al.16 A nickel-titanium closed-coil
spring (Ultra Light, 75 mg, 9 mm, Medika, Tokyo,
Japan) was placed between the molar cleats and the in-
cisor hooks. The initial force was 40 cN.
In the intermittent force group, the coil spring was
placed at 8 AM and removed at 4 PM every day for a total
force application time of 8 hours.18 In the continuous
force group, the same amount of force was applied
throughout the experiment. In the control group, no
spring was used. The rats in the continuous force and
control groups were also anesthetized twice per day in
the same way as the intermittent force group. The exper-
imental period was 14 days.
Of the 110 teeth, 96 molars were studied histologi-
cally when the devices did not fall off. The rats were
killed at 1, 3, 5, 7, and 14 days under anesthesia by de-
capitation. Each subgroup consisted of more than 6 mo-
lars. The maxilla was dissected into 2 halves, fixed in
10% formalin for 24 hours, dehydrated in increasing
concentrations of ethanol, and embedded undecalcified
in methyl methacrylate.20 The embedded tissues were
sectioned parasagittally at the mesiodistal aspect of
the first molars in 4- to 5-mm thickness, by using a micro-
tome (Leica Microsystems, Werzlar, Germany), and
mounted on gelatinized slides. Each section included
crown, root, periodontal membrane, and adjacent alve-
olar bone. Alternate sections were stained according
to the Von Kossa method with a tetrachrome counter-
stain.
Paradental and interradicular alveolar bones imme-
diately adjacent to the PDL of the distobuccal and me-
siobuccal maxillary first molar roots were sampled.
We selected parasagittal sections from areas that dem-
onstrated radicular pulp to the apical third of the roots;
multiple nonoverlapping fields at 400 times were then
sampled from the mesial and distal sides of the roots.
All parameters were scanned by using a CoolSNAP
CCD camera (RS Photometrics, Tucson, Ariz) mounted
on a light microscope (Olympus Optical, Tokyo, Japan).
The outlines of the root surfaces, root resorption areas,
and osteoclast surfaces on the alveolar bone were traced
and measured by an image analysis system (Scion
Image, Scion Corporation, Frederick, Md), and the
numbers of osteoclasts on the alveolar bone were
counted.16,17 Osteoclasts were identified based on char-
acteristic morphologic criteria, including residence on
the bone surface and presence of Howships lacunae.
Using the methods of King et al16,21 and Parfitt et al,22
we calculated 3 parametersosteoclast numbers, oste-
oclast surfaces, and root resorption. Osteoclast numbers
(osteoclast numbers per length of bone surface)
American Journal of Orthodontics and Dentofacial Orthopedics Kumasako-Haga et al 278.e3
Volume 135, Number 3

represented the number of osteoclasts on the bone sur-

face from the alveolar crest to the root apex. Length
of bone surface was the distance in millimeters from
the alveolar crest to the root apex. Osteoclast surface
was the length of osteoclast surface per length of bone
surface as a percentage. Root resorption (root surface
with cratering per length of the root surface) was the
surface with cratering, representing the entire root sur-
face adjacent to the alveolar bone including the craters,
as a percentage.

Statistical analysis
The mean and standard error of the mean were calcu-
lated for each time and group. Root resorption data were
compared across groups and times with analysis of
variance (ANOVA). When ANOVA indicated significant
differences, pairwise (Tukey-Kramer) comparisons were
performed between groups and times. Osteoclast number
and osteoclast surface data were compared across groups
and times with Steel-Dwass test.

RESULTS
In the control group, there were no time-related
changes in osteoclast number and osteoclast surfaces
on either the mesial or the distal surface (Figs 1 and 2).
Osteoclast numbers on the mesial surface increased
in the continuous force group and reached a peak at day
5 with significantly (P \0.05) higher numbers than at
day 1 (Fig 1). Furthermore, the osteoclast surfaces on
the mesial surface increased over time, reaching
a peak at day 14 (Fig 2). The osteoclast numbers and
surfaces at days 3, 5, 7, and 14 were significantly
(P \0.05) higher than at day 1 (Figs 1 and 2).
The osteoclast numbers and osteoclast surfaces in-
creased on the mesial side by 1.86% and 9.32% at day
14, respectively. The continuous force group had signif-
icantly (P \0.05) higher osteoclast numbers than did
the control group at days 5, 7, and 14 (Fig 1). On the
distal surfaces, there were no significant time-related
changes in the continuous force group (Figs 1 and 2).
There were no significant differences between the con-
tinuous force and the control groups.
Osteoclast numbers increased on the mesial surface
in the intermittent group over time and reached a peak at
day 7 (Fig 1). The osteoclast surfaces on the mesial sur-
face increased and reached a peak at day 7 (Fig 2). The
osteoclast numbers and surfaces at days 5, 7, and 14
were significantly (P \0.05) higher than at day 1
(Figs 1 and 2). The osteoclast numbers and surfaces in-
creased on the mesial side by 1.88% and 6.36% at day
14, respectively.
Fig 1. Changes in osteoclast numbers per alveolar bone
surface at the mesial (A) and distal (B) surfaces. A, The
control group showed no significant time-related
changes. There were significant time-related changes
in the intermittent force group, with day 1 different
from days 5, 7, and 14 (P \0.05). There were significant
time-related changes in the continuous force group, with
day 1 different from days 3, 5, 7, and 14 (P \0.05). There
were significant group-related changes in the intermit-
tent force group, different from the control group at
days 7 and 14. There were significant group-related
changes in the continuous force group, different from
the control group at days 5, 7 and 14. B, There were
no significant time- or group-related changes in the dis-
tal surfaces.
The osteoclast numbers on the mesial surfaces in the
intermittent group were significantly (P \0.05) higher
than in the control group at days 7 and 14 (Fig 1), and
the osteoclast surfaces on the mesial surface in the inter-
mittent group were significantly larger (P \0.05) than
in the control group at days 5, 7, and 14 (Fig 2). On
the distal surfaces, there were no significant time-re-
lated changes in the continuous force group (Figs 1
and 2). There were no significant differences between
the intermittent force and the control groups.
278.e4 Kumasako-Haga et al
Fig 2. Changes in osteoclasts at the mesial (A) and
distal (B) surfaces. A, The control group showed no
significant time-related changes. There were significant
time-related changes in the intermittent force group,
with day 1 different from days 5, 7, and 14 (P \0.05).
There were significant time-related changes in the
continuous force group, with day 1 different from days
3, 5, 7, and 14 (P \0.05). There were significant group-
related changes in the intermittent force group, different
from the control group at days 5, 7, and 14. There were
significant group-related changes in the continuous
force group, different from the control group at days 5,
7, and 14. B, There were no significant time- or group-
related changes in the distal surfaces.
There was no significant difference in osteoclast
numbers and surfaces on the mesial surfaces at any
time between the intermittent and the continuous forces
groups (Figs 1 and 2). At day 14, osteoclast numbers in
the intermittent force group were 100.5% of the contin-
uous force group, and osteoclast surfaces in the inter-
mittent group were 68.2% of the continuous force
group. On the distal surfaces, no significant differences
were found at any time between the intermittent and
continuous forces groups (Figs 1 and 2).
There was no significant time-related difference in
root resorption in the control group at either the mesial
or the distal root surface (Table). The root resorption
American Journal of Orthodontics and Dentofacial Orthopedics
March 2009
areas in the control group were about 5% and 10% at
the mesial and distal sides, respectively (Fig 3).
In the continuous force group, root resorption
rapidly increased at the mesial (compression) side to
39.49% at day 14. It was significantly (P \0.01 or P
\0.05) higher at day 14 than that at days 1, 3, and 7
(Fig 3 and Table). However, root resorption gradually
decreased at the distal side and was significantly
(P \0.01 or P \0.05) lower at day 14 than at days
1 and 3 (Fig 3 and Table).
The continuous force group had significantly (P
\0.01 or P \0.05) greater root resorption than did the
control group at days 1, 3, 5, 7, and 14 (Fig 3 and Table).
In the intermittent force group, root resorption at the
mesial side increased to 15.31% at day 14, but there was
no significant time-related difference (Fig 3 and Table).
Root resorption decreased over time at the distal side,
but there were no significant differences between days
1 and 14 (Fig 3 and Table).
There was no significant difference in root resorp-
tion on the mesial surface at any time between the inter-
mittent and control groups.
Root resorption at the mesial side was significantly
(P \0.01) less in the intermittent group than in the con-
tinuous force group at days 3, 5, 7, and 14 (Fig 3 and Ta-
ble). Root resorption at the mesial side at day 14 in the
intermittent force group was significantly (P \0.01)
lower than that at all days in the continuous force group
(Fig 3 and Table). It was 29.9% of that in the continuous
force group. There was no significant difference at the
distal side between the continuous and intermittent
forces groups (Table).
DISCUSSION
Among experimental animals, rats are useful and
easy to keep in large numbers. They are comparatively
inexpensive, need little living space, can be housed eas-
ily for long times, and are easy to handle. For these rea-
sons, we could obtain larger samples for fewer
individual differences with demonstrable statistical dif-
ferences.
There are morphologic and physiologic differences
in alveolar bone and PDL between rats and humans.
The alveolar bone is generally denser in rats than in hu-
mans.23 Root formation and histologic changes in the
periodontal tissues after orthodontic treatment appear
to be faster in rats than in humans, although the princi-
pal mechanisms are the same.23 Because of the high
turnover rate, this bone is a good model to study bone
modeling and remodeling activities,24 and we could ex-
amine and discuss periodontal changes over a short
time. In addition, the literature from 1981 to 2002
American Journal of Orthodontics and Dentofacial Orthopedics Kumasako-Haga et al 278.e5
Volume 135, Number 3

Table. Comparison of root resorption at the mesial and distal sides between groups at each time point with the Tukey-
Kramer test
Control Intermittent force Continuous force

Day 1 3 5 7 14 1 3 5 7 14 1 3 5 7 14

Mesial root resorption

Control 1 *
3 *
5 *
7 *
14
Intermittent force 1
3
5
7 * *
14 *
Continuous force 1
3 *
5
7 *
14
Distal root resorption
Control 1
3
5
7
14
Intermittent force 1
3
5
7
14
Continuous force 1
3 *
5
7
14

*P \0.05; P \0.01.

indicated that rats were used in 57% of animal studies
about orthodontic tooth movement.23
Degree of force, duration of force application, direc-
tion of force application, and distribution of force are
believed to be significant factors for effective tooth
movement. King et al16 examined tooth movement us-
ing various forces (20, 40, and 60 g) in rats. They dem-
onstrated that effective tooth movement of rat molars
required a force of 20 to 40 g, and that its velocity did
not increase if the force was greater than 40 g. In previ-
ous studies, Konoo et al17 and Hayashi et al18 used 40 g
of continuous and intermittent forces for mesial move-
ment of the maxillary first molars in rats. In these stud-
ies, the degree and the direction of force were
standardized, and the effect of duration of force applica-
tion on effective tooth movement was tested. They
found that 8-hour intermittent force provided more ef-
fective tooth movement compared with continuous
force. To allow comparison among studies, we also
used a force of 40 g. Osteoclast numbers and osteoclast
surfaces indicate bone resorption activity. In this study,
the effectiveness of tooth movement was estimated by
these parameters, which increase at the compression
surface and histologically demonstrate orthodontic
tooth movement.
For effective tooth movement and to prevent root
resorption, hyalinized tissue of the PDL should be
removed. Most orthodontic root resorption has been
correlated with removal of hyalinized tissue of the
PDL.25-30 Less hyalinized tissue has been considered
a factor that leads to less risk of root resorption. On the
compression side, orthodontic force produces sustained
pressure, occluding the PDL arterioles and causing their
collapse and necrosis of the PDL, a process termed
hyalinization.31 Intermittent force periodically falls
to zero when removable appliances are taken out, so
278.e6 Kumasako-Haga et al
Fig 3. Changes in root resorption rate at the mesial (A)
and distal (B) sides.
the pressure of the PDL arterioles stops. This phenome-
non allows recovery of blood flow and probably cessa-
tion of expansion of the hyalinized area.32 Preventing
hyalinization of the PDL and prompt removal might pre-
vent further resorption.10,11,13,33 Reitan6 reported that
intermittent forces caused hyalinized tissue in less ex-
tensive areas and in less time compared with continuous
forces. In the above reports, intermittent force is be-
lieved to produce less root resorption than continuous
force. In this study, root resorption with 8-hour intermit-
tent forces was significantly less than that with continu-
ous forces at days 3, 5, 7, and 14.
On the other hand, intermittent force might cause jig-
gling. Physiologically, rat molars moves distally.16,18,24
When a tooth stops moving mesially, distal relapse
movement will be subjected to jiggling force. Jiggling
is generally recognized as the primary risk factor for
root resorption.12 However, Alwali et al34 indicated
that the headgear and jiggling do not significantly
shorten the root in humans. Although intermittent force
was recognized as the jiggling force in our study, root
resorption in the intermittent force group did not in-
American Journal of Orthodontics and Dentofacial Orthopedics
March 2009
crease significantly compared with the continuous force
group. Intermittent force controlled by magnitude and
direction can reduce root damage.
The osteoclast numbers and osteoclast surfaces at
the mesial sides in the continuous force group did not in-
crease at day 1; the increase began at day 3, and osteo-
clast numbers peaked at day 5. This finding is consistent
with previous reports with similar methods.21 In this
study, the significant increases of osteoclast numbers
and osteoclast surface in the intermittent force group
were from day 5, and those in the continuous force
group were from day 3. Those findings showed that sig-
nificant increases of osteoclast numbers and surfaces
stimulated by 8-hour intermittent force are delayed
compared with continuous forces.
Osteoclast numbers and osteoclast surfaces indicate
bone resorption activity. In our study, osteoclast num-
bers at day 14 in the intermittent force group were
100.5% of the continuous force group, and osteoclast
surfaces at day 14 in the intermittent group were
68.2% of the continuous force group. These results indi-
cate that intermittent forces stimulated the same osteo-
clast numbers as did continuous forces, although the
size was small. Duration of force application (8 hours)
in the intermittent force group was one third (33.3%)
of the 24 hours in the continuous force group. The oste-
oclasts stimulated by 8-hour intermittent forces ex-
ceeded the expected value predicted by the duration
(33.3%) of the force application.
Hayashi et al18 reported that mesial tooth movement
with an 8-hour intermittent force of 40 g was 65.9% of
that with less than 40 g of continuous force at day 14. In
our study, root resorption at the mesial side of the inter-
mittent force group was 29.9% of the continuous force
group at day 14. It suggested that 8-hour intermittent
force produced more tooth movement but not more
root resorption than the predicted value (33.3%).
In this study, intermittent forces caused less root re-
sorption compared with continuous forces at each time
point. Accordingly, we suggest that intermittent forces
reduce the severity of root resorption. However, one
should also consider that the intermittent force pro-
duced less tooth movement than did the continuous
force at each time. It is generally recognized that in-
creases in tooth movement cause severe root resorption.
Therefore, it is necessary to compare root resorption at
similar levels of tooth movement. According to Hayashi
et al,18 tooth movement with 8-hour intermittent forces
at days 14 and 7 were almost the same as tooth move-
ment with continuous forces at days 7 and 3, respec-
tively. Root resorption amounts on the mesial side
with intermittent forces were 15.3% at day 14 and
11.9% at day 7, whereas those with continuous forces
American Journal of Orthodontics and Dentofacial Orthopedics
Volume 135, Number 3
were 27.2% at day 7 and 25.2% at day 3, and those in the
intermittent force group were significantly less than in
the continuous force group. Therefore, for equivalent
tooth movement, the root resorption rate was higher in
the continuous force group than in the intermittent force
group. Root resorption under intermittent forces was
also significantly less than that with continuous forces
at similar points of tooth movement. Intermittent forces
produced the same amount of tooth movement as did
continuous forces with less root damage. Therefore,
we believe that intermittent forces are effective in re-
ducing root resorption.
CONCLUSIONS
1. There were no significant differences in parameters
of bone resorption (osteoclast numbers and osteo-
clast surfaces with alveolar bone) between the in-
termittent and continuous force groups.
2. Osteoclast numbers and osteoclast surfaces in the
intermittent force group were 100.5% and 68.2%
of the respective values in the continuous force
group at day 14. This means that the osteoclasts
stimulated by 8-hour intermittent forces exceeded
the expected value predicted by the duration
(33.3%) of force application.
3. Root resorption induced by the intermittent force
was significantly less than that by the continuous
force on the mesial side at days 3, 5, 7, and 14.
4. In the intermittent force group, root resorption was
29.9% of that in the continuous force group, al-
though tooth movement was 65.9% of that in the
continuous force group. This means that root re-
sorption with 8-hour intermittent forces was not
more than the expected value predicted by the dura-
tion (33.3%) of force application.
5. With the same amount of tooth movement, root re-
sorption with intermittent forces was significantly
less than that with continuous forces.
Our results suggest that 8-hour intermittent forces
not only are efficient for tooth movement but also cause
less damage to the root and produce more efficient oste-
oclast recruitment.
We thank Dr G. J. King of the University of Wash-
ington in Seattle for suggesting and encouraging publi-
cation of this study.
REFERENCES
1. Ketcham AH. A preliminary report of an investigation of apical
root resorption of vital permanent teeth. Int J Orthod 1927;13:
97-127.
2. Ketcham AH. A progress report of an investigation of apical root
resorption of vital permanent teeth. Int J Orthod 1929;15:310-28.
Kumasako-Haga et al 278.e7
3. Proffit WR. The biologic basis of orthodontic therapy. In:
Warfel DB, editor. Contemporary orthodontics. St Louis: Mosby;
1986. p. 228-45.
4. Reitan K. Biomechanical principles and reactions. In: Graber TM,
Swain BF, editors. Orthodontics: current principles and tech-
niques. St Louis: Mosby; 1985. p. 101-92.
5. Oppenheim A. A possibility for physiologic orthodontic move-
ment. Am J Orthod 1944;30:277-328.
6. Reitan K. Some factors determining the evaluation of forces in or-
thodontics. Am J Orthod 1957;43:32-45.
7. Brudvik P, Rygh P. The repair of orthodontic root resorption: an
ultrastructural study. Eur J Orthod 1995;17:189-98.
8. Faltin RM, Faltin K, Sander FG, Arana-Chavez VE. Ultrastruc-
ture of cementum and periodontal ligament after continuous intru-
sion in humans: a transmission electron microscopy study. Eur J
Orthod 2001;23:35-49.
9. Acar A, Canyurek U, Kocaaga M, Erverdi N. Continuous vs. dis-
continuous force application and root resorption. Angle Orthod
1999;69:159-63.
10. Weiland F. Constant versus dissipating forces in orthodontics: the
effect on initial tooth movement and root resorption. Eur J Orthod
2003;25:335-42.
11. Kameyama T, Matsumoto Y, Warita H, Soma K. Inactivated pe-
riods of constant orthodontic forces related to desirable tooth
movement in rats. J Orthod 2003;30:31-7.
12. Pizzo G, Licata ME, Guiglia R, Giuliana G. Root resorption and
orthodontic treatment. Review of the literature. Minerva Stomatol
2007;56:31-44.
13. Maltha JC, van Leeuwen EJ, Dijkman GE, Kuijpers-Jagtman AM.
Incidence and severity of root resorption in orthodontically moved
premolars in dogs. Orthod Craniofac Res 2004;7:115-21.
14. Sharpe W, Reed B, Subtelny JD, Polson A. Orthodontic relapse,
apical root resorption, and crestal alveolar bone levels. Am J Or-
thod Dentofacial Ortop 1987;91:252-8.
15. Brezniak N, Wasserstein A. Orthodontically induced inflamma-
tory root resorption. Part II: the clinical aspects. Angle Orthod
2002;72:180-4.
16. King GJ, Keeling SD, McCoy EA, Ward TH. Measuring dental
drift and orthodontic tooth movement in response to various initial
forces in adult rats. Am J Orthod Dentofacial Orthop 1991;99:
456-65.
17. Konoo T, Kim YJ, Gu GM, King GJ. Intermittent force in ortho-
dontic tooth movement. J Dent Res 2001;80:457-60.
18. Hayashi H, Konoo T, Yamaguchi K. Intermittent 8-hour activation
in orthodontic molar movement. Am J Orthod Dentofacial Orthop
2004;125:302-9.
19. Nakao K, Goto T, Gunjigake KK, Konoo T, Kobayashi S,
Yamaguchi K. Intermittent force induces high RANKL expres-
sion in human periodontal ligament cells. J Dent Res 2007;86:
623-8.
20. Baron R, Neff L, Tran Van P, Nefussi JR, Vignery A. Kinetic and
cytochemical identification of osteoclast precursors and their dif-
ferentiation into multinucleated osteoclasts. Am J Pathol 1986;
122:363-78.
21. King GJ, Keeling SD, Wronski TJ. Histomorphometric study of
alveolar bone turnover in orthodontic tooth movement. Bone
1991;12:401-9.
22. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H,
Meunier PJ, et al. Bone histomorphometry: standardization of no-
menclature, symbols, and units. Report of the ASBMR Histo-
morphometry Nomenclature Committee. J Bone Miner Res
1987;2:595-610.
278.e8 Kumasako-Haga et al
23. Ren Y, Maltha JC, Kuijpers-Jagtman AM. The rat as a model for
orthodontic tooth movementa critical review and a proposed so-
lution. Eur J Orthod 2004;26:483-90.
24. Vignery A, Baron R. Dynamic histomorphometry of alveolar bone
remodeling in the adult rat. Anat Rec 1980;196:191-200.
25. Reitan K. The initial tissue reaction incident to orthodontic tooth
movement as related to the influence of function: an experimental
histologic study on animal and human material. Acta Odontol
Scand 1951;(Suppl 10):1-240.
26. Kvam E. A study of the cell-free zone following experimental
tooth movement in the rat. Trans Eur Orthod Soc 1970;45:419-34.
27. Rygh P. Orthodontic root resorption studied by electron micros-
copy. Angle Orthod 1977;47:1-16.
28. Brudvik P, Rygh P. Non-clast cells start orthodontic root resorp-
tion in the periphery of hyalinized zones. Eur J Orthod 1993;15:
467-80.
American Journal of Orthodontics and Dentofacial Orthopedics
March 2009
29. Brudvik P, Rygh P. The initial phase of orthodontic root resorption
incident to local compression of the periodontal ligament. Eur J
Orthod 1993;15:249-63.
30. Brudvik P, Rygh P. Transition and determinants of orthodontic
root resorption-repair sequence. Eur J Orthod 1995;17:177-88.
31. King GJ. Orthodontic root resorption. J Tokyo Orthod Soc 2005;
15:170-8.
32. Yamaguchi K, Nanda RS. Blood flow changes in gingival tissue
due to the displacement of teeth. Angle Orthod 1992;62:257-64.
33. Gu G, Lemery SA, King GJ. Effect of appliance reactivation after
decay of initial activation on osteoclasts, tooth movement, and
root resorption. Angle Orthod 1999;69:515-22.
34. Alwali S, Marklund M, Persson M. Apical root resorption of up-
per first molars as related to anchorage system. Swed Dent J 2000;
24:145-53.