ORIGINAL ARTICLE

How does the amount of surgical insult affect

bone around moving teeth?
Matthew D. McBride,a Phillip M. Campbell,b Lynne A. Opperman,c Paul C. Dechow,d and Peter H. Buschange
Dallas, Tex

Introduction: The purpose of this study was to determine how the amount of surgical insult affects the quantity
and maturity of dentoalveolar bone around teeth that have been orthodontically moved. Methods: A split-mouth
design with 8 foxhound dogs was used to evaluate bone surrounding maxillary second premolars that were
protracted for 15 days and retained for 7 weeks. The maxillary rst premolars were extracted, and the
interseptal bone was removed to within 1 mm of the second premolars; on the insult (lesser surgical insult)
side, buccal and lingual vertical grooves were made in the extraction socket to undermine the mesial root of
the second premolar; the insult1 (greater surgical insult) side was apped and had modied corticotomies
extending to, but not through, the lingual cortex 1 mm distal to the distal root, and 3 to 5 mm apical to both
roots. Microcomputed tomography analyses were used to evaluate the material density, bone volume
fraction, and trabecular characteristics of surrounding bone. Hematoxylin and eosin sections were used to
determine osteoclast numbers, bone surface areas, and bone volumes. Results: After 7 weeks of consolidation,
there was signicantly (P \0.05) less bone on the insult1 side; it was less dense and less mature than the bone
on the insult side. Relative to the control bone, bone on the insult1 side was signicantly less dense but showed
no differences in bone volume. Preliminary histologic evaluations indicated increased numbers of osteoclasts
and greater bone surface areas on the insult1 side than the insult side, but no differences in bone volume.
Conclusions: Increased surgical insults produce less dense and less mature bone but have no effect on
bone volume at 9 weeks after surgery. (Am J Orthod Dentofacial Orthop 2014;145:S92-9)

tudies evaluating orthodontic treatment duration

indicate that the average patient requires 23.5
to 28.6 months to complete treatment.1,2
Altering the biology of bone to enhance tooth
movement is appealing because it could dramatically
improve treatment efciency. In addition to fewer
appointments, more efcient treatment might prevent
the patient from experiencing negative sequelae
secondary to orthodontic treatment, such as external
apical root resorption3 and enamel decalcication.4
a

Private practice, Dallas, Tex.

Chairman, Department of Orthodontics, Texas A&M University Baylor College of
Dentistry, Dallas, Tex.
c
Professor, Department of Biomedical Sciences, Texas A&M University Baylor
College of Dentistry, Dallas, Tex.
d
Professor and chair, Department of Biomedical Sciences, Texas A&M University
Baylor College of Dentistry, Dallas, Tex.
e
Professor and director of Orthodontic Research, Department of Orthodontics,
Texas A&M University Baylor College of Dentistry, Dallas, Tex.
All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conicts of Interest, and none were reported.
Partially funded by the Robert E. Gaylord Endowed Chair in Orthodontics.
Address correspondence to: Peter H. Buschang, Orthodontic Department, Texas
A&M University Baylor College of Dentistry, 3302 Gaston Ave, Dallas, TX 75246;
e-mail, phbuschang@bcd.tamhsc.edu.
Submitted, March 2013; revised and accepted, October 2013.
0889-5406/$36.00
Copyright 2014 by the American Association of Orthodontists.
http://dx.doi.org/10.1016/j.ajodo.2013.10.020
b

S92

Conventional tooth movement is a biologic

rate-limiting process that depends on the ability of the
periodontal ligament to respond to the strains induced
by orthodontic forces and mediate the repair of bone.5
Under normal conditions, cells of the periodontal
ligament secrete osteoprotegerin to inhibit osteoclast
formation and maintain the integrity of the periodontal
ligament.6 Upon force application, the bone becomes
strained, cell membranes disrupt, and a biochemical
cascade of events occurs, stimulating osteoclastogenesis
and bone formation. As the bone adapts to the strain by
simultaneous resorption and formation, tooth movement occurs. Based on the clinical research, force levels
of 60 to 300 g produce average tooth movement rates of
approximately 1 mm per month in humans.7-13
Tooth movements can be accelerated by altering
bone biology. After a noxious stimulus (ie, bone injury
or operation), acceleration of most ongoing normal
hard-tissue and soft-tissue processes occurs, including
increased bone metabolism, turnover, and modeling.
This complex reaction, known as the regional acceleratory phenomenon, initiates the healing process of the
injured tissue, resulting in a temporary decrease in
regional bone density and an increase in remodeling.14
The use of corticotomies to produce the regional

McBride et al

acceleratory phenomenon and facilitate orthodontic

treatment dates back to the late 1950s,15 but corticotomies were not used clinically to enhance treatment
outcomes until the late 1980s and early 1990s.16-18
Wilcko et al19 popularized this approach to accelerate
orthodontic tooth movement rates. Since then, corticotomies have been used to facilitate the intrusion,20-22
distalization,23 and extrusion24 of teeth.
Experimental studies have demonstrated positive
effects of corticotomies on tooth movements. Cho
et al25 reported 2 to 4 times greater experimental than
control tooth movements in beagle dogs. Others have
shown greater experimental tooth movements as early
as the rst week but not after the fourth week.26,27
Longitudinal models have demonstrated that
experimental tooth movements in the mandibles of
dogs peak after the third week, when they were
moving 85% faster than the control teeth.28 These
studies indicate that there is a relatively small window
of opportunity to take advantage of the regional
acceleratory phenomenon.
Importantly, the effects of the regional acceleratory
phenomenon on tooth movements are not all or
nothing. Sanjideh et al28 demonstrated that an additional corticotomy procedure, initiated 4 weeks after
the rst surgical insult, produced signicantly greater
tooth movements than 1 initial corticotomy. Increased
amounts of injury around multirooted teeth also cause
increased tooth movements, with the maxillary second
premolars protracted 1.8 and 2.9 mm on the limited
and extensive surgical insult sides, respectively.29
Although increased surgical insults are related to
increased tooth movements, it remains unknown how
different amounts of surgical insult affect the bone
around treated teeth. The purpose of this study was to
evaluate the dentoalveolar bone subjected to heavy
orthodontic forces and differing amounts of surgical
insult. The null hypothesis was that there are no
differences in the quantity and maturity of dentoalveolar
bone between 2 treatments producing differing
amounts of surgical insult.
MATERIAL AND METHODS

Eight skeletally mature (1-2 years of age) male

foxhound dogs, weighing 25 to 30 kg, were used for
this study. The surgical and orthodontic procedures
were fully described by Cohen et al,29 who evaluated
their tooth movements. Before the surgeries, the maxillary right and left rst premolars were extracted. The
extraction sites were extended distally to within 1 mm
of the second premolars (to simulate the width of human
interseptal bone). The maxillary quadrants were
randomly assigned to 1 of 2 groups, insult or

S93

insult1, signifying the level of insult to the alveolar

bone surrounding the second premolar.
On the insult side, the investigators undermined the
interseptal bone mesial to the second premolars by making vertical grooves in the extraction socket along the
buccal and lingual sides, extending the cuts obliquely
toward the base of the interseptal bone to weaken its
resistance and stimulate the regional acceleratory phenomenon (Fig 1). On the insult1 side, a full-thickness
gingival ap was raised, and the buccal plate between
the second premolar and the canine was removed, along
with any possible interference to translation of the tooth
and bony segment. A vertical osteotomy extending to,
but not through, the lingual cortex was performed 1
mm distal to the second premolar. The vertical osteotomy and extraction sites were then connected by a
horizontal corticotomy 1 to 2 mm deep and 3 to 5 mm
apical to the second premolar (Fig 1).
Immediately after surgery, custom orthodontic appliances, consisting of bands soldered to a hyrax screw
(opened to allow protraction of the maxillary second premolar upon activation), were cemented in place.
Protraction of the maxillary second premolars was initiated at a rate of .5 mm per day (2 closing turns of the
hyrax screw) for 15 days. After protraction, the second
premolars were retained by the appliance over a 7-week
consolidation period, after which the experimental animals were sacriced. The maxillas were then sectioned
and removed from the skulls and stored in 70% ethanol.
Insult, insult1, and control bone specimens were
harvested from each dog. Seven regions of interest
were evaluated on the insult and insult1 sides, including
the (1) mesial trabecular, (2) interradicular trabecular, (3)
distal trabecular, (4) buccal cortical, and (5) lingual
cortical bones, as well as the cortical (bundle) bone along
the (6) mesial and (7) distal root surfaces of the mesial
root (Fig 2). An eighth region of interest, located in the
interradicular trabecular bone of the maxillary third premolar, served as the untreated control bone.
Bone quantity was based on the material density (the
amount of bone mass per unit of volume, minus any
voids) and the percent of bone volume (ratio of the
number of bone voxels to the total number of voxels
in a specic region of interest). Bone maturity was
measured based on trabecular number, trabecular
thickness, and trabecular separation.
The heights of the specimens from the most occlusal
aspect of the experimental crown to within 5 mm of
bone apical to the root apices were approximately 30
mm. The specimens were trimmed to t in 30-mmdiameter tubes, using foam to stabilize their positions;
70% ethanol was poured over the specimens, and the
tubes were covered with Paralm (Pechiney Plastic

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McBride et al

S94

Fig 1. Surgical procedure diagrams with corresponding photos: A, insult group diagram (buccal view);
B, sample insult group photo (occlusal view); C, insult1 group diagram (buccal view); D, sample insult1 group photo (buccal view).

Fig 2. Diagrams showing regions of interest: A, regions 1 (mesial), 2 (interradicular), 3 (distal), 6

(mesial radicular), and 7 (distal radicular) of the insult and insult1 groups, and 8 (interradicular) of
the control group (buccal view); B, regions 1 (mesial), 2 (interradicular), 3 (distal), 4 (buccal), and 5
(lingual) of the insult and insult1 groups (occlusal view).

Packaging, Chicago, Ill) to prevent dehydration. The

specimens were then scanned using a Micro-CT 35
(Scanco Medical, Br
uttisellen, Switzerland) at a medium
resolution of 30 mm. Three-dimensional reconstructions, 50 slices thick occlusoapically, were obtained
from the 8 areas of interest of each specimen. Vertically,
the bone analyzed was located approximately midway
between the crests of the alveolar bone and the apices
of the mesial and distal roots. At this level, segments
of bone from the buccal and lingual cortices, bone

April 2014  Vol 145  Issue 4  Supplement 1

mesial to the mesial root and distal to the distal root,

and mesial and distal bundle bone were outlined.
Fifty-slice-thick segments of interradicular control
bone were also outlined at the same level. The threshold
boundaries for the scans were set between 250 and 1000
Hounseld units for all specimens.
The histologic specimens were obtained by removing
with a trephine bur (Ace Surgical, Brockton, Mass) 3mm-diameter samples of interradicular bone, taken
midway between the crests of the alveolar bone and

American Journal of Orthodontics and Dentofacial Orthopedics

McBride et al

the mesial and distal root apices, from 6 specimens on

the insult1 side, along with their respective controls (total of 12 samples). The tissues were xed in 10%
buffered formalin and washed thoroughly with tap
water. They were then decalcied in .5 mol per liter of
EDTA (ethylenediamine tetraacetic acid, tetrasodium
salt) using the PELCO BioWave (Ted Pella, Inc, Redding,
Calif). Radiographs were used to monitor the decalcication process. After decalcication, the specimens were
dehydrated, cleared, inltrated with parafn with an
automatic tissue processor (VIP model 2000; MilesCo
Scientic, Fergus Falls, Minn), and embedded in parafn
blocks. The blocks were hardened on a cold plate and
sectioned at 6 mm with a microtome. Five sections
were chosen per block and mounted on 1 3 3-in coated
glass slides, dried on a warming tray at 42 for 2 hours,
and then dried overnight in an oven at 54 .
One slide per block was randomly selected to be
stained using standard hematoxylin and eosin procedures. The number of osteoclasts on each slide was
manually counted 3 times under 20-times magnication
with a microscope (Zeiss, Thornwood, NY) and then
averaged. Osteo software (version 11.2.6; Bioquant,
Nashville, Tenn) was used to segment matrix bone tissue
by adjusting threshold values; the bone was traced, and
the bone surface area was calculated. When analyzing
surface areas, the cut margins resulting from retrieval
of the specimens with the trephine bur were segmented
and excluded from the evaluation.
Statistical analysis

SPSS statistical software (version 18; IBM SPSS,

Chicago, Ill) was used to describe the results and
compare the groups. The nonparametric Wilcoxon
signed rank test was used for all comparisons. Statistical
signicance was based on a P value of #0.05.
RESULTS

The 3-dimensional reconstructions obtained from the

scans were all 1.5 mm thick occlusoapically and ranged in
width from 1 to 3 mm, depending on the distances
between the tooth roots and/or the surgical cuts. The
amount of surgical insult had a direct effect on the quantity and maturity of bone. Bone volume fraction and bone
density were consistently less on the insult1 than on the
insult sides. The insult1 side had signicantly less material density in the distal, buccal, and lingual regions than
did the insult side (Table I). The insult side also showed
a signicantly greater bone volume fraction than did the
insult1 side in the buccal and mesial radicular regions.
The insult side also showed signicantly (P 5 0.036)
denser bone than did the insult1 side in the interradicular region. The interradicular bone of the insult and

S95

Table I. Material densities and bone volume fractions

around the maxillary second premolars

Insult1
Bone index
Material density (mg HA/cm3)
Mesial
Distal
Buccal
Lingual
Mesial radicular
Distal radicular
Bone volume fraction (%)
Mesial
Distal
Buccal
Lingual
Mesial radicular
Distal radicular

Insult

Mean SD Mean SD Probability

847.2
795.7
857.3
881.5
835.8
816.4
50.3
48.8
70.2
86.2
65.2
57.1

30.7
32.6
23.3
19.6
35.6
46.4
19
17
8
9
18
23

866.4
867.6
898.4
905
866.1
859

20.9
27.8
31.3
14.6
28
34.7

56.3 8
52.5 11
90.1 5
88.3 8
82.6 6
73.9 12

0.208
0.012
0.017
0.050
0.123
0.068
0.401
0.889
0.012
0.575
0.036
0.208

mg HA/cm3, Milligrams of hydroxylapatite per cubic centimeter.

insult1 sides showed signicantly (P 5 0.012) less

material density than did the control bone (Table II).
There were no statistically signicant group differences
in bone volume fraction of interradicular bone between
the treatment groups and the controls.
The distal bone of the insult1 side showed significantly more trabeculae, signicantly thinner trabeculae, and signicantly less trabeculae separation
than did the insult side (Table III). Compared with
the controls (Fig 3, Table II), the interradicular bone
of the insult1 group showed signicantly greater
numbers of trabeculae (P 5 0.017), signicantly
thinner trabeculae (P 5 0.042), and signicantly less
trabecular separation (P 5 0.012).
The experimental sections (Fig 4, A-D) showed
mature lamellar bone with concentric lamellae radiating
from central osteons. Osteocytes were found in the calcied tissues, and osteoblasts lined the endosteal surfaces.
There also were mature multinucleated osteoclasts with
rufed borders lining the periosteal surfaces and in the
Howship's lacunae. The trabecular spaces contained
multiple spindle-shaped broblasts. The control bone
(Fig 4, E-H) showed mature lamellar bone containing
osteocytes. Although osteoblasts and osteoclasts were
found lining the periosteal surfaces, there were fewer
compared with the experimental group.
Quantitative analyses showed no difference in the
size of interradicular bone areas between the insult1
and control groups. The insult1 group showed significantly more osteoclasts (P 5 0.028) than did the
control group (Table IV). The differences in osteoclasts per unit of surface (P 5 0.028) in the interradicular bone of the insult1 and control groups were
also statistically signicant.

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McBride et al

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Table II. Material densities, bone volume fractions, trabecular numbers, trabecular thickness, and trabecular separa-

tion in the interradicular region of the maxillary second premolars

Insult1
Bone index
Material density (mg HA/cm3)
Bone volume fraction (%)
Trabecular number (n/mm)
Trabecular thickness (mm)
Trabecular separation (mm)

Mean
837.5
36.1
2.1
0.2
0.5

SD
19.9
7
0.3
0
0.1

Insult
Mean
856.1
35
1.8
0.3
0.6

Control

SD
16.3
11
0.3
0.1
0.1

Mean
929.1
34.7
1.6
0.3
0.7

SD
30.8
13
0.2
0.1
0.1

Probability
Insult1 vs insult
0.036
0.779
0.093
0.111
0.123

Insult1 vs control
0.012
0.779
0.017
0.042
0.012

Insult vs control
0.012
0.779
0.263
0.203
0.176

mg HA/cm3, Milligrams of hydroxylapatite per cubic centimeter.

Table III. Trabecular number, trabecular thickness,

and trabecular separation mesial and distal to the

maxillary second premolars
Insult1
Bone index
Mean
SD
Trabecular number (n/mm)
Mesial
2.5
0.5
Distal
3.7
0.8
Trabecular thickness (mm)
Mesial
0.3
0.1
Distal
0.2
0
Trabecular separation (mm)
Mesial
0.4
0.1
Distal
0.3
0.1

Insult
Mean

SD

Probability

2.6
2.4

0.6
0.4

0.779
0.017

0.3
0.3

0.1
0

0.401
0.012

0.4
0.5

0.1
0.1

0.799
0.012

DISCUSSION

Greater surgical insults resulted in less dense bone. The

insult1 side showed less material density than did the
insult side in all regions. Cattermole et al,30 who used
dual-energy x-ray absorptiometry to measure bone density, found less dense bone in the fractured than in the
contralateral unfractured areas. Whereas others have
shown decreased density associated with the regional acceleratory phenomenon, this is the rst time that
decreased material density with increased surgical insults
has been demonstrated.31-34 The differences identied in
the interradicular and distal regions were probably due to
the extension of the surgical insult apical to the roots, and
distal to the distal root on the insult1 side. The buccal
bone on the insult1 side might be expected to be less
dense because of the removal of the buccal plate and
disruption of the blood supply from the ap surgery.
Additionally, the lingual bone on the insult1 side might
have been less dense because of increased strain
secondary to increased tooth movement.
Greater surgical insults also produced greater decreases in the bone volume fraction, which measures
the relative amount of bone. Although the amount of
bone has not been previously related to the extent of

April 2014  Vol 145  Issue 4  Supplement 1

the insult, insults have been shown to reduce the amounts

of bone.35-37 The fact that bone density was affected to a
greater extent than the bone volume fraction can be
explained by the normal healing process. After 7 weeks
of consolidation, it can be assumed that the blood
supply had been reestablished, new bone had formed,
and bone was becoming more mature. The density of
the bone remains low until the newly formed bone has
remodeled into mature lamellar bone.
The amount of mesial radicular bone on the insult1
side was less than on the insult side. Since this is a type of
cortical bone, with less blood supply than trabecular
bone, the increased strain in cortical bone secondary
to increased tooth movement could have delayed the
angiogenic response necessary for bone formation.38
The other regions displayed similar differences in bone
volume fractions, but the differences were smaller.
The magnitude of the surgical insult also affected
bone maturity. The bone on the insult1 side showed
greater trabecular numbers, less trabecular thickness,
and less trabecular separation than did the bone on
the insult side. This pattern indicates newly formed
woven bone composed of greater amounts of thin and
densely packed collagen brils. The differences were
greatest in the distal region, probably because it was
the site of the greatest difference in the surgical insult.
Previous microcomputed tomography comparisons of
regenerate bone after distraction osteogenesis found
signicant increases in trabecular numbers and signicant decreases in trabecular thickness compared with
the controls after 6 weeks of consolidation.39,40
Although a decrease in bone maturity is expected after
injury, this study is the rst to show that greater injury
to bone results in decreased bone maturity.
After 7 weeks of consolidation, bone that had been
surgically insulted showed less material density than
did the control bone. The interradicular bones on the
insult1 and insult sides were 9.9% and 7.9% less dense,
respectively, than the control bone, but only the insult1
side showed statistically signicant differences. Zapata

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McBride et al

S97

Fig 3. Comparisons of the measures of bone maturity of the insult1, insult, and control groups for the
interradicular regions: A, trabecular numbers; B, trabecular thickness; C, trabecular separation.

Fig 4. Sample photomicrographs showing differences in osteoclastic activity between the insult1 (top
row) and their respective controls (bottom row): A-D, photomicrographs of the insult1 group showing
selected osteoclasts (*), osteoblasts (1), and osteocytes (o); E-H, photomicrographs of the respective
controls showing absence of osteoclasts.

et al,41 who evaluated regenerate bone density after

distraction osteogenesis and 6 weeks of consolidation
in foxhound mandibles, found that the bone was
11.6% less dense compared with the controls. Similar
studies evaluating regenerate bone densities have
reported 22.3%42 less dense bone after 4 weeks of
consolidation, and no differences after 12 weeks.43
Surgically insulted bone was also less mature than
control bone. Bone generated by distraction osteogenesis in dogs has been shown to be fully mineralized after 8
weeks of consolidation, but the regenerate remained
distinguishable from host bone because of incomplete
remodeling.44 After distraction osteogenesis in dogs,
approximately 24 weeks of consolidation is needed

before new bone resembles control bone.45 The insult

group showed the same pattern of maturity as the
insult1 group, but the changes relative to the controls
were not signicant. This study is unique in showing
that increased surgical insults result in decreased overall
bone maturity, and that the decrease in maturity
matches the level of the insult.
Surgical insults increased the rates of remodeling at 9
weeks postsurgery. Compared with the controls, both
bone surface area and osteoclastic activity increased in
the insult1 group. Since the insult group was not evaluated and only 1 slice per block was counted, these ndings remain preliminary. Increases in bone surface area
are related to increased metabolic activity46 and

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Table IV. Total number of osteoclasts, bone volume,

bone surface, osteoclasts per unit of volume, and osteoclasts per unit of surface area
Insult1

Control

Bone index
Mean SD Mean SD Probability
Total osteoclasts (n)
24.3 13.5
3.9 1.4
0.028
Bone volume (mm2)
7.2
1.5
7.1 1.2
0.462
Bone surface (mm)
59.9 14.2 37.1 7.4
0.046
Osteoclasts/volume (mm2)
3.4
1.6
0.6 0.2
0.028
Osteoclasts/surface (mm)
0.4
0.2
0.1 0
0.028

decreased density.47 Decreased bone density has been

associated with increased osteoclastic activity.25,48 The
analyses conrmed that increased surgical trauma
decreases bone density because of the increased
osteoclastic activity. Decreased bone density associated
with insults has been linked to increased osteoclastic
activity in beagle dogs and rats.48
This study explains why Cohen et al29 observed significantly greater tooth movements after greater surgical
insults. The greater surgical insults produced a larger
regional acceleratory phenomenon response, characterized by less dense and less mature bone. These changes
were made possible by increased osteoclastic activity.
The osteoclasts create a demineralized bony matrix
through which the teeth can more easily move, whereas
the osteoblasts maintain bone volume. The new bone
remains immature until full remodeling of the bone has
taken place. It is the combination of demineralized bone
matrix and immature, uncalcied bone secondary to the
increased strain that allows for faster tooth movement.
This study was limited by the sample size and the
assessments that were made. The small sample in this
split-mouth design was sufcient to produce signicant
results (ie, it had sufcient power). However, the sample
was too small to capture the variability among animals,
making it possible that different results could be
obtained if the study were repeated. Although the histology
conrms the presence of osteoclasts, tartrate-resistant acid
phosphatase staining would have made it possible to determine whether they were active. With these limitations, the
results must be considered to be preliminary.
CONCLUSIONS

Based on a split-mouth design comparing bone surrounding maxillary second premolars that had and had
not been surgically insulted, the following preliminary
conclusions can be drawn.
1.

With greater surgical insults, there is less bone, less

dense bone, and less mature bone around teeth than
with a lesser surgical insult.

April 2014  Vol 145  Issue 4  Supplement 1

2.
3.

Surgical insults produced bone that was less dense

than the control bone.
Surgical insults produced bone with increased
numbers of osteoclasts and greater bone surface
areas.

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April 2014  Vol 145  Issue 4  Supplement 1