ORIGINAL ARTICLE

BoneCeramic graft regenerates alveolar defects

but slows orthodontic tooth movement with less
root resorption
Nan Ru,a Sean Shih-Yao Liu,b Yuxing Bai,c Song Li,c Yunfeng Liu,d and Xiaoxia Weie
Beijing, Hangzhou, and Zhengzhou, China, and Indianapolis, Ind

Introduction: BoneCeramic (Straumann, Basel, Switzerland) can regenerate bone in alveolar defects after
tooth extraction, but it is unknown whether it is feasible to move a tooth through BoneCeramic grafting sites.
The objective of this study was to investigate 3-dimensional real-time root resorption and bone responses in
grafted sites during orthodontic tooth movement. Methods: Sixty 5-week-old rats were randomly assigned to
3 groups to receive BoneCeramic, natural bovine cancellous bone particles (Bio-Oss; Geistlich Pharma,
Wolhusen, Switzerland), or no graft, after the extraction of the maxillary left rst molar. After 4 weeks, the
maxillary left second molar was moved into the extraction site for 28 days. Dynamic bone microstructures
and root resorption were evaluated using in-vivo microcomputed tomography. Stress distribution and
corresponding tissue responses were examined by the nite element method and histology. Mixed model
analysis of variance was performed to compare the differences among time points with Bonferroni post-hoc
tests at the signicance level of P \0.05. Results: The BoneCeramic group had the least amount of tooth movement and root resorption volumes and craters, and the highest bone volume fraction, trabecular number, and
mean trabecular thickness, followed by the Bio-Oss and the control groups. The highest stress accumulated
in the cervical region of the mesial roots. Conclusions: BoneCeramic has better osteoconductive potential
and induces less root resorption compared with Bio-Oss grafting and naturally recovered extraction sites.
(Am J Orthod Dentofacial Orthop 2016;149:523-32)

oving a tooth orthodontically into the region

of an alveolar defect with insufcient buccolingual width can be problematic.1 It often
causes root resorption,2 gingival recessions,3 periodontal

a
Lecturer, Department of Orthodontics, School of Stomatology, Capital Medical
University, Beijing, China.
b
Associate professor; director, Mineralized Tissues and Histology Research Laboratory; and director, Orthodontic Fellowship Program, Department of Orthodontics and Oral Facial Genetics, Indiana University School of Dentistry,
Indianapolis, Ind.
c
Professor, Department of Orthodontics, School of Stomatology, Capital Medical
University, Beijing, China.
d
Associate professor, Key Laboratory of Equipment & Manufacturing, Zhejiang
University of Technology, Hangzhou, China.
e
Associate professor, Department of Orthodontics, School of Stomatology,
Zhengzhou University, Zhengzhou, China.
Nan Ru and Sean Shih-Yao Liu are joint rst authors and contributed equally to
this work.
All authors have completed and submitted the ICMJE Form for Disclosure of
Potential Conicts of Interest, and none were reported.
Supported by a grant from the Natural Science Foundation of China (81400537).
Address correspondence to: Yuxing Bai, Department of Orthodontics, School of
Stomatology, Capital Medical University, Tiantan Xili 4, Chongwen District, Beijing, China 100050; e-mail, byuxing@263.net.
Submitted, December 2014; revised and accepted, September 2015.
0889-5406/$36.00
Copyright 2016 by the American Association of Orthodontists.
http://dx.doi.org/10.1016/j.ajodo.2015.09.027

pockets,4 and traumatic injuries to pulp vitality.5 Alveolar defects may appear in patients with cleft lip and palate. If the cleft involves the alveolus, the alveolar ridge
defects in these sites impede tooth eruption6 and delay
orthodontic tooth movement with prolonged treatment
times.7 Alveolar defects may also be secondary to a large
piece of buccal plate with the extraction of an impacted
tooth, jaw inammation, or cyst and trauma surgery.1
Similar scenarios can be seen during extensive remodeling of the edentulous alveolus after the extraction of
damaged or periodontal-involved rst molars. For
some adolescent and young adults, once periodontal
disease is under control, an effective way to replace a
missing molar is to move the adjacent molar into the rst
molar area.1 However, alveolar bone in extraction
sites quickly resorbs, with reduced height and width,
primarily changing to dense cortical bone, which
impedes the movement of teeth through the bone.
Orthodontic tooth movement is not feasible without
reestablishment of the alveolar width with bone grafts
before movement.8
To alleviate alveolar ridge resorption and regenerate
alveolar bone in the defects, bone grafts, such as autogenous bone, allograft,9 or alloplast,10 can be placed in
523

Ru et al

524

the extraction sites immediately after tooth extraction.11

Although autogenous bone is recognized as the gold
standard for bone grafts because of the viability of transferable osteogenic cells, it requires a second surgery from
the donor site. Patients tend to decline this treatment
modality because of the additional discomfort.12 Alternatively, deproteinized bovine bone mineral (Bio-Oss;
Geistlich Pharma, Wolhusen, Switzerland) can be used
as a graft material for augmenting an alveolar ridge
defect.13 However, Bio-Oss degrades slowly and induces
uncertain immune responses and brous encapsulation
with healing.14
A new synthetic bone substitute, BoneCeramic (Straumann, Basel, Switzerland), has been used for ridge preservation because it can be rapidly replaced by
regenerative bone.15,16 BoneCeramic consists of 60%
hydroxyapatite and 40% beta tricalcium phosphate.
After grafting, beta tricalcium phosphate is rapidly
resorbed and completely replaced by regenerative
bone.17 Meanwhile, the hydroxyapatite, resorbed slowly,
serves as a good matrix scaffold for ingrowth of new
blood vessels and attachment of bone-forming cells.18
Bone can be greatly regenerated because BoneCeramic
can be totally resorbed and subsequently replaced by
host bone in a shorter time.19 However, whether it will
hamper orthodontic tooth movement in an augmented
area of alveolar ridge is still unknown.
To evaluate whether a tooth can be moved into an
extraction site with bone grafts, one should investigate
the rate or distance of orthodontic tooth movement
with accompanied bone responses or adverse side effects. The aims of this experiment were (1) to evaluate
whether it is feasible to move a tooth in an alveolar ridge
augmented with BoneCeramic, and (2) to evaluate realtime 3-dimensional (3D) changes in root resorption and
bone microarchitectures, and tissue responses when
moving teeth into BoneCeramic and Bio-Oss grafts after
extractions. Understanding the dynamic responses in
bone graft resorption, bone regeneration, and root
resorption will help to establish treatment guidelines
for patients.
MATERIAL AND METHODS

All procedures were approved by the institutional

animal care and use committee of the School of Stomatology, Capital Medical University, Beijing, China. After
they were acclimated, 60 male Sprague Dawley rats
(age, 5 weeks) (specic pathogen free level 3) had the
maxillary left rst molar extracted under anesthesia by
chloral hydrate (2 mL/kg) injected intraperitoneally. A
rectangular (3 3 2 3 2 mm) alveolar ridge defect was
created in the socket by completely resecting the intraradicular septa between the tooth roots at the extraction

April 2016  Vol 149  Issue 4

sites with a low-speed dental handpiece. The animals

were randomly assigned to 3 groups (n 5 20 per group)
to receive BoneCeramic (60% hydroxyapatite, 40% beta
tricalcium phosphate granules), Bio-Oss (natural bovine
spongiosa granules, 0.25-1 mm), or no grafting. The
mucosa was reected and sutured to cover the socket
to prevent the materials from leaking. Signs of infection,
animal weight, and health conditions were monitored.
Four weeks after the extractions, a groove was prepared at the cervical third of the incisors under anesthesia. A nickel-titanium coil spring (0.2 mm in
diameter; IMD, Shanghai, China) was ligated between
the maxillary left second molar and incisors using an
0.08-in ligature wire secured with bonding adhesive
(Transbond; 3M Unitek, Monrovia, Calif). The spring
was activated for approximately 1 mm to produce 10 g
of continuous force to move the molar forward into
the extraction site (Fig 1, A).
After spring installation, each animal was scanned
using an in-vivo microcomputed tomography system
(SkyScan1076; Bruker, Kontich, Belgium) on days 0, 7,
14, 21, and 28. The spring was removed for each invivo microcomputed scan and reattached after scanning.
The palate was secured at the supine position parallel to
the stage in a carbon composite animal holder. The head
was scanned through 180
of rotation at a 0.5
increment with 2 seconds per degree with resolution of
18 mm per pixel. Data were further reconstructed to provide axial cross-section images with SkyScan NRecon
software (version 1.4.4; Bruker) and converted into 16bit bitmapped TIFF images with a resolution of
1024 3 1024 pixels.20
Tooth movement distance (Di) (mm) was measured 3
times and averaged at each time point (i 5 0, 7, 14, 21,
and 28 days). Tooth movement rate (Vi) was then calculated as Vi 5Di  Di1 =7 (Fig 1, B).
The alveolar bone was equally divided into the cervical and apical regions by a selected middle axial slice
from the root apex to the furcation. In the apical region,
6 regions of interest (360 mm3) were selected: 500 mm
mesial to the mesiobuccal and the mesiolingual roots,
500 mm distal to the distobuccal and the distolingual
roots, and the intraradicular septa between the mesiobuccal and distobuccal roots and between the mesiolingual and distolingual roots (Fig 1, C). In the cervical
region, 4 regions of interest (360 mm3) were selected:
500 mm mesial to the mesiobuccal and the mesiolingual
roots, and distal to the distobuccal and the distolingual
roots (Fig 1, D).
Three-dimensional microarchitecture parameters for
trabecular bone were measured as the following: bone
volume fraction (BV/TV), indicating the ratio of bone
volume to total volume; mean trabecular thickness

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Fig 1. A, Schematic of orthodontic tooth movement into the bone graft area. Dotted shadow, the alveolar ridge defect was embedded with bone grafts after the maxillary left rst molar extraction; the nickeltitanium spring was ligated to move the molar forward into the extraction site. M2, maxillary left second
molar. B, Sagittal view of the tooth roots. Tooth movement distance (Di) was calculated as the shortest
width between the second and third molar crowns on the sagittal plane along the distal root of the third
molar. White squares, regions of interest. C, Horizontal view of the apical region of tooth roots: 1-6
squares represent the selected regions of interest in the alveolar bone adjacent to the apical region
of the 4 roots of the maxillary left second molar. D, Horizontal view of the cervical region of the tooth
roots: 7-10 squares represent the selected regions of interest in the alveolar bone adjacent to the cervical region of the 4 roots of the maxillary left second molar. E, Tooth movement distances at different
time points in the 3 groups. *Signicance between the experimental groups and the control (P \0.05).
F, Tooth movement rates at different time points in the 3 groups. *Signicance between the experimental groups and the control (P \0.05).

(Tb.Th), indicating the local thickness at each voxel representing bone; trabecular number (Tb.N), indicating the
average number of trabeculae per unit of length; and
trabecular separation (Tb.Sp), indicating the mean distance between trabeculae.
After segmenting the roots from the images using
Mimics software (version 17.0; Materialise, Leuven,
Belgium), the cervical, apical, and total root volumes of
each root were measured for each time point.21 The volumes of root resorption in each region on days 7, 14, 21,
and 28 were calculated by subtracting the root volume at
each time point from the root volume on day 0.
After 28 days, the animals were killed, and the
maxillae were dissected, xed, decalcied, and
embedded in parafn and serially sectioned (5 mm) along
the mesiodistal axis of the second molar. The sections
were stained with hematoxylin and eosin.

A 3D nite element method model of the maxillary

second molar (day 0) was constructed with the Mimics
software and imported into Ansys software (Ansys, Canonsburg, Pa). The geometry of the model consisted of
50019 isoparametric tetrahedral-node solid elements
and 69731 nodes. The width of the periodontal ligament
was set at 0.2 mm, and Young's modulus of the tooth,
periodontal ligament, and bone were set as 19,600,
0.7, and 13,700 MPa, respectively. The Poisson ratios
of the tooth, periodontal ligament, and bone were
0.15, 0.49, and 0.15, respectively.22 A 10-g force was
applied in the nite element method model in the
same direction as the spring attached intraorally. Movement was suppressed in 6 degrees of freedom for the nodes on the bottom edge of the alveolar bone. Tooth
displacement and stress distribution analyses were performed with the Ansys software.

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526

Fig 2. Microarchitecture parameter schematic of region of interest 1 adjacent to the second molar:
bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular separation (Tb.Sp), mean trabecular thickness (Tb.Th), and at different time points in the BoneCeramic, Bio-Oss, and control groups.
*Signicance between the experimental groups and the control (P \0.05).

Statistical analysis

For each parameter, mixed-model measures analysis

of variance was performed to compare the differences
among time points and between groups with Bonferroni
post hoc tests using the Statistical Package for the Social
Sciences (version 11.5; SPSS, Chicago, Ill). The signicance level was set at P \0.05.
RESULTS

The greatest amount of tooth movement was

observed in the control group, followed by the Bio-Oss
group and then the BoneCeramic group (Fig 1, E). In
all groups, tooth movement rates accelerated from
days 0 to 7 and slightly decelerated from days 7 to 14.
This similar tooth movement pattern repeated with acceleration from days 14 to 21, followed by deceleration
from days 21 to 28 (Fig 1, F).
In all regions of interest, the BV/TV, Tb.N, and Tb.Th
signicantly decreased from days 0 to 7 but increased
from days 14 to 28, except for regions of interest 2
and 8 in all groups. Tb.Sp signicantly decreased from
days 0 to 7 but uctuated from days 14 to 28 in all
groups (Fig 2). The typical changes of BV/TV, Tb.N,
Tb.Th, and Tb.Sp in all regions of interest during tooth

April 2016  Vol 149  Issue 4

movement were found in regions of interest 1, 2, 7, 8,

and 10 (Tables I-III; Fig 2). Regions of interest 3 to 6
and 9 are omitted because of their similar changes to regions of interest 1, 2, 7, 8, and 10.
In the BoneCeramic group, BV/TV, Tb.N, and Tb.Th
in regions of interest 1, 2, and 7 were signicantly higher
than in the Bio-Oss and control groups at each time
point (Tables I and II; Fig 2). In the Bio-Oss group, BV/
TV and Tb.Th in regions of interest 2, 7, and 8 on days
0, 21, and 28 were signicantly higher than in the control group (Tables I and II). Tb.Sp values in the
BoneCeramic group from days 7 to 28 were
signicantly lower than in the other 2 groups in
regions of interest 1, 2, and 10 (Tables I and III; Fig 2).
However, in regions of interest 1, 2, and 7, there was
no difference in Tb.Sp between the Bio-Oss and control
groups (Tables I and II; Fig 2).
Root volumes reduced in all groups over time. All
roots had a smooth surface on day 0. Starting at day 7
through day 28, small isolated lacunae were mainly scattered on the mesial surfaces of the roots, and wide
shallow resorption craters were observed mostly on the
distal surfaces of the roots (Fig 3).
The greatest root resorption volumes were observed
in the apical region of the mesiobuccal root in all groups,

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527

Table I. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm

1

), Tb.Sp (mm), and Tb.Th

(mm) in regions of interest (ROI) 1 and 2

ROI 1
Day
0

14

21

28

Group
A
B
C
A
B
C
A
B
C
A
B
C
A
B
C

BV/TV
82.98 (7.21)*
58.48 (8.22)
57.38 (8.24)
78.99 (5.21)*
45.24 (4.22)
35.08 (3.09)
45.22 (3.56)*
21.25 (4.63)
22.03 (5.21)
68.90 (4.11)*
58.33 (3.56)
34.58 (3.09)
69.06 (3.41)*
66.70 (3.56)
43.73 (4.11)

Tb.N
5.31 (0.12)*
4.78 (0.22)
5.86 (0.13)
4.96 (0.21)*y
3.12 (0.14)*
2.17 (0.11)
4.76 (0.08)*
3.01 (0.09)
3.12 (0.10)
4.27 (0.11)
4.28 (0.12)
3.21 (0.14)*
4.87 (0.09)
4.90 (0.12)
3.57 (0.15)

ROI 2

Tb.Sp
0.06 (0.01)*
0.10 (0.01)
0.08 (0.01)
0.09 (0.02)*
0.12 (0.01)
0.16 (0.02)
0.09 (0.01)*
0.19 (0.02)
0.11 (0.02)
0.07 (0.01)*
0.10 (0.01)
0.10 (0.01)
0.05 (0.01)*
0.13 (0.02)
0.13 (0.02)

Tb.Th
0.18 (0.02)*
0.10 (0.01)
0.11 (0.01)
0.12 (0.02)*
0.09 (0.01)
0.09 (0.01)
0.09 (0.01)
0.06 (0.01)
0.09 (0.01)
0.16 (0.02)*y
0.11 (0.01)*
0.06 (0.01)
0.17 (0.02)*
0.13 (0.02)
0.08 (0.01)

BV/TV
80.82 (5.12)*y
48.41 (4.12)*
23.78 (5.67)
57.57 (4.23)*y
42.47 (4.67)*
39.43 (5.78)
32.33 (6.79)
29.25 (2.54)
28.33 (2.57)
43.37 (4.12)
42.24 (4.67)
21.37 (3.29)*
42.46 (5.67)
43.33 (4.43)
23.40 (2.47)*

Tb.N
5.22 (0.14)*
4.11 (0.10)
4.08 (0.09)
4.25 (0.14)
4.10 (0.09)
2.47 (0.13)*
4.69 (0.10)*y
3.52 (0.12)*
2.50 (0.13)
5.10 (0.09)
4.29 (0.08)
2.85 (0.13)
5.51 (0.12)*y
4.46 (0.08)*
3.29 (0.13)

Tb.Sp
0.13 (0.01)*
0.14 (0.02)
0.08 (0.01)
0.18 (0.02)*
0.14 (0.01)
0.12 (0.01)
0.11 (0.01)*
0.13 (0.02)
0.12 (0.01)
0.10 (0.01)*
0.11 (0.01)
0.12 (0.01)
0.08 (0.01)*
0.09 (0.01)
0.12 (0.02)

Tb.Th
0.18 (0.01)*
0.11 (0.09)
0.09 (0.01)
0.12 (0.02)
0.11 (0.02)
0.06 (0.01)*
0.12 (0.02)
0.06 (0.02)*
0.11 (0.01)
0.12 (0.02)*y
0.10 (0.02)*
0.0 (0.01)
0.11 (0.02)
0.10 (0.01)
0.07 (0.01)*

Regions of interest 3 and 4 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 1 and 2.
A, BoneCeramic; B, Bio-Oss; C, control.
*Signicance between the experimental groups and the control; ysignicance between the 2 experimental groups (P \0.05).

1

), Tb.Sp (mm), and Tb.Th

Table II. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm

(mm) in regions of interest (ROI) 7 and 8

ROI 7
Day
0

14

21

28

Group
A
B
C
A
B
C
A
B
C
A
B
C
A
B
C

BV/TV
82.72 (5.78)*y
62.25 (4.18)*
53.91 (3.36)
60.25 (5.56)*y
50.21 (2.59)*
36.16 (5.78)
24.15 (3.56)
22.37 (2.54)
17.37 (4.12)*
36.29 (4.16)*y
27.18 (1.38)*
22.74 (2.54)
38.13 (3.56)*y
27.19 (1.19)*
25.21 (2.54)

Tb.N
4.95 (0.14)*
4.54 (0.13)
4.20 (0.12)
4.52 (0.11)*y
3.92 (0.14)*
3.20 (0.08)
4.01 (0.11)
2.48 (0.08)
1.53 (0.12)*
3.75 (0.14)*
2.62 (0.08)
2.62 (0.12)
3.77 (0.12)
3.36 (0.14)
2.96 (0.15)

ROI 8
Tb.Sp
0.17 (0.02)
0.13 (0.01)
0.14 (0.02)
0.15 (0.01)
0.15 (0.02)
0.14 (0.01)
0.23 (0.02)
0.23 (0.02)
0.22 (0.01)
0.17 (0.02)
0.16 (0.02)
0.17 (0.01)
0.15 (0.02)
0.17 (0.02)
0.16 (0.01)

Tb.Th
0.12 (0.02)
0.11 (0.01)
0.10 (0.02)
0.09 (0.02)*
0.07 (0.01)
0.07 (0.02)
0.05 (0.01)
0.05 (0.01)
0.08 (0.01)*
0.06 (0.02)*y
0.08 (0.02)*
0.10 (0.01)
0.08 (0.01)
0.06 (0.01)
0.07 (0.02)

BV/TV
34.60 (3.35)
30.00 (3.11)*
30.45 (3.56)
20.97 (4.12)
18.73 (2.54)
12.28 (1.38)*
21.25 (4.12)
19.27 (1.19)
12.39 (1.38)*
20.15 (2.54)
20.47 (2.01)
17.40 (2.94)*
17.58 (4.12)
17.50 (1.38)
15.57 (2.54)*

Tb.N
3.58 (0.11)*y
3.68 (0.12)*
2.37 (0.11)
2.35 (0.12)*
2.05 (0.08)
2.06 (0.11)
2.42 (0.14)
2.04 (0.08)
1.70 (0.11)*
3.13 (0.14)
2.85 (0.08)
2.69 (0.11)*
3.21 (0.12)
3.07 (0.14)
3.03 (0.12)

Tb.Sp
0.17 (0.01)
0.15 (0.02)
0.13 (0.01)*
0.15 (0.01)
0.14 (0.01)
0.15 (0.02)
0.15 (0.01)
0.14 (0.02)
0.14 (0.01)*
0.15 (0.02)*y
0.18 (0.01)*
0.15 (0.01)
0.15 (0.02)
0.13 (0.01)
0.14 (0.01)

Tb.Th
0.08 (0.01)
0.08 (0.01)
0.08 (0.01)
0.09 (0.02)
0.09 (0.02)
0.08 (0.01)
0.08 (0.02)
0.08 (0.01)
0.06 (0.01)*
0.11 (0.02)
0.08 (0.02)
0.07 (0.01)
0.09 (0.01)
0.09 (0.02)
0.08 (0.01)

Regions of interest 5 and 6 are omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to regions 7 and 8.
A, BoneCeramic; B, Bio-Oss; C, control.
*Signicance between the experimental groups and the control; ysignicance between the 2 experimental groups (P \0.05).

especially in the control group (0.078 6 0.002 mm3;

Fig 4). The smallest root resorption volumes occurred
in the cervical region of the distobuccal root in all
groups, especially in the BoneCeramic group (0.039 6
0.003 mm3; Fig 4). Root resorption crater volumes
signicantly increased from days 0 to 7 (BoneCeramic,
0.067 6 0.002 mm3; Bio-Oss, 0.069 6 0.002 mm3;
control, 0.074 6 0.001 mm3) and plateaued until day

28 in the apical regions in all groups (BoneCeramic,

0.068 6 0.002 mm3; Bio-Oss, 0.070 6 0.002 mm3; control, 0.075 6 0.002 mm3). However, in the cervical regions, root resorption crater volumes signicantly
increased from days 0 to 14 (BoneCeramic,
0.044 6 0.001 mm3; Bio-Oss, 0.054 6 0.002 mm3; control: 0.062 6 0.002 mm3) and plateaued from days 14 to
28 (BoneCeramic, 0.045 6 0.001 mm3; Bone-Oss,

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Table III. Descriptive statistics (means and standard deviations) of BV/TV (%), Tb.N (mm

1

), Tb.Sp (mm), and Tb.Th

(mm) in region of interest (ROI) 10

ROI 10
Day
0

14

21

28

Group
A
B
C
A
B
C
A
B
C
A
B
C
A
B
C

BV/TV
20.02 (3.56)
20.94 (2.06)
21.52 (1.18)*
14.26 (1.26)
15.24 (1.64)
14.48 (2.16)
17.44 (1.19)
16.37 (2.96)
15.36 (1.38)
25.21 (2.51)
23.47 (2.04)
20.24 (2.54)
27.92 (2.21)
26.91 (2.01)
27.28 (2.54)

Tb.N
2.74 (0.09)
3.32 (0.12)
2.65 (0.07)
1.97 (0.08)
2.07 (0.05)
1.75 (0.04)
2.01 (0.06)
2.32 (0.09)
2.06 (0.07)
3.09 (0.08)
2.65 (0.06)
2.59 (0.05)
4.23 (0.12)*y
3.87 (0.08)*
2.13 (0.07)

Tb.Sp
0.16 (0.02)
0.15 (0.01)
0.12 (0.01)
0.20 (0.02)
0.18 (0.02)
0.17 (0.01)
0.12 (0.01)*
0.17 (0.01)
0.15 (0.02)
0.15 (0.02)
0.16 (0.01)
0.15 (0.02)
0.14 (0.02)
0.13 (0.01)
0.14 (0.01)

Tb.Th
0.10 (0.02)
0.09 (0.02)
0.08 (0.01)
0.05 (0.01)
0.08 (0.02)
0.07 (0.02)
0.08 (0.01)
0.08 (0.01)
0.07 (0.02)
0.07 (0.02)
0.06 (0.01)
0.06 (0.01)
0.09 (0.02)
0.08 (0.02)
0.07 (0.01)

Region of interest 9 is omitted because of the similar changes in BV/TV, Tb.N, Tb.Th, and Tb.Sp to region 10.
A, BoneCeramic; B, Bio-Oss; C, control.
*Signicance between the experimental groups and the control; ysignicance between the 2 experimental groups (P \0.05).

Fig 3. Reconstructed 3D images of the mesiobuccal (MB), distobuccal (DB), mesiolingual (ML), and
distolingual (DL) roots at different time points in groups A (BoneCeramic), B (Bio-Oss), and C (control).
White arrows indicate root lacunae.

0.056 6 0.002 mm3; control, 0.065 6 0.002 mm3;

Fig 4).
In the histology testing, root resorption was found on
the mesial and distal sides of all roots after tooth movement, especially on the mesiobuccal and distobuccal

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roots in all groups. In the BoneCeramic group, root

resorption mostly occurred on the distal surfaces of the
cervical region of the distobuccal root, with mostly small
and shallow craters with clear margins (Fig 5, A). In the
Bio-Oss group, root resorption occurred on the mesial

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529

Fig 4. Schematics of root resorption crater volumes of the mesiolingual (ML), distolingual (DL), mesiobuccal (MB), and distobuccal (DB) root; root resorption crater volumes in the cervical (CML, CDL, CMB,
and CDB) and apical (AML, ADL, AMB, and ADB) regions of the roots at different time points in the 3
groups. *Signicance between the experimental groups and the control (P \0.05).

Fig 5. Histologic slices depicting damaged root surfaces with hematoxylin and eosin staining in the 3
groups: A, BoneCeramic; B, Bio-Oss; C, control. Black arrows indicate root resorption craters; M and D
indicate the mesial and distal surfaces, respectively. D-F, In the visualized nite element models of the
tooth roots, different amounts of stress were distributed on the root surfaces. White arrows indicate the
loading forces.

surface of the apical regions of the mesiobuccal and distobuccal roots, with wide shallow or deep resorption craters. Multinucleated osteoclasts appeared in the root
resorption lacunae with some evident deposition of
cellular cementum on resorbed root cavities (Fig 5, B).

In the control group, the largest root resorption crater

was found on the distal surface of the mesiobuccal
root. It extended from the cervical region to the apical
region with massive dentin destruction. Small or wide
resorption craters were also observed on the mesial

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530

and distal surfaces of the mesiobuccal and distobuccal

roots (Fig 5, C).
When tested with the nite element method, more
stress accumulated in the cervical region than in the apical region of the root surface. The highest level of stress
accumulated on the mesial side in the cervical region of
the mesiolingual root, followed by the mesial side of the
cervical region of the mesiobuccal root, and the distal
side of the cervical region of the distobuccal and distolingual roots (Fig 5, D-F).
DISCUSSION

This study demonstrated that it is feasible to move a

tooth into a BoneCeramic grafting extraction site that
intends to preserve bone and reduce the potential for
alveolar bone loss. Our data showed that the rats'
second molars experienced the least tooth movement
rate when they traveled through the BoneCeramic
grafts, followed by the Bio-Oss grafts and the control
extraction sites with no grafts. This result is opposite
to that found by Sei and Ghoraishian,23 who observed
an increased tooth movement rate in the group with the
alveolar defect lled with demineralized freeze-dried
bone allograft. Others reported that a similar tooth
movement distance was observed between the group
lled with Bio-Oss and the control group.10 However,
with the same amount of orthodontic traction force, it
is obvious that bone substitutes decrease the tooth
movement rate.
The rats' extraction site healing process consisted of
3 phases: (1) organization of the blood clot and covering
of the extraction socket by epithelium (1-5 days), (2) new
bone formation (5-20 days), and (3) new bone maturation and alveolar ridge remodeling (20-60 days).24,25
The alveolar ridge resorbs with signicant reductions
in height and width; this is more pronounced during
the initial phase of wound healing than during later
phases. Schropp et al26 stated that in humans approximately two thirds of this reduction occurs within the rst
3 months after tooth extraction. The healing process of a
rat's extraction site is similar to a human's but 3 times
faster, indicating that the alveolar ridge resorbs within
1 month in rats after tooth removal.27 In our study,
grafting of bone substitutes immediately after extraction
slowed ridge resorption. When the second molars were
moved into the alveolar ridge defects 1 month after
bone grafting, bone substitutes were not absorbed
completely, with new bone forming in the extraction
sockets. Measuring the distance of tooth movement,
the bone density, and the root resorption provided the
means of evaluating the feasibility of moving teeth
into the augmented alveolar ridges with or without
adverse effects.

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It was evident that the placement of a bone substitute interfered with the processes of bone modeling
and remodeling. In regions of interest 1, 2, and 7 of
the BoneCeramic group, the highest levels of BV/TV,
Tb.N, and Tb.Th, and the lowest level of Tb.Sp indicated
the increased new bone formation in the extraction sites.
These demonstrated that BoneCeramic stimulates bone
growth with increases in both Tb.N and Tb.Th, implying
that BoneCeramic has the potential for osteoconduction. These ndings agree with those of Mardas et al19
that BoneCeramic completely preserved the height and
width of the alveolar ridge and the interproximal bone
in the extraction sites. Because of the highest BV/TV in
the BoneCeramic group (BoneCeramic, 69.6%; BioOss, 62.3%; control, 52.8%) (Fig 2), the tooth movement
distance and the rate decreased. This is supported by
others, showing that the tooth movement rate relies
on the density of the alveolar bone.28-30
The tooth movement rate depends on removing hyalinized tissue on the compression side of alveolar bone
caused by direct or undermining bone resorption.31
From days 0 to 7, stress on the tooth root induced alveolar bone resorption, shown by decreases in BV/TV,
Tb.N, and Tb.Th in region of interest 7 (Table II). Meanwhile, the tooth was rapidly moved into the space of the
resorbed bone with a signicantly increased tooth movement rate. Once the tooth is completely moved into the
resorbed space, the roots were again pulled against the
alveolar bone and developed hyalinized tissues.32 It is
believed that hyalinization of the tissues provides high
resistance and slows orthodontic tooth movement as
shown from days 7 to 14 in our study. To continue tooth
movement, hyalinized tissues need to be removed by
undermining bone resorption. Osteoclasts continued to
resorb bone as indicated by decreased BV/TV, Tb.N,
and Tb.Th. Interestingly, in all groups, Tb.Sp signicantly decreased accompanied by increased BV/TV,
Tb.N, and Tb.Th from days 14 to 28 (Fig 2), suggesting
that bone regeneration in the extraction sites was preserved by BoneCeramic in the later period of orthodontic
treatment.
In this study, bone density increased more in the regions of BoneCeramic grafting compared with Bio-Oss
grafting, and both grafting methods slowed tooth
movement. Under clinical conditions, slowing tooth
movement by bone graft materials may be good for preventing neighboring teeth from drifting into the space
that is to be prepared for the implant. Whether to graft
BoneCeramic or Bio-Oss depends on the alveolar ridge
defect width and height, and the tooth movement
design. The orthodontist should anticipate how the
defect will affect tooth movement and consider which
bone substitute will preserve the alveolar ridge better.

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Since two thirds of alveolar ridge resorption occurs in the

rst 3 months after tooth extraction, this resorption
becomes stable in 6 months.26 If the extraction space
can be closed in 6 months, Bio-Oss could be placed in
the extraction site and will not affect tooth movement.
However, if the extraction space would take longer
than 6 months to close, the patient might be left with
a periodontally involved rst molar and lack of alveolar
bone around the molar. The orthodontic mechanics are
to extract the rst molar and to mesialize the
second molar to replace the missing rst molar. It takes
a long time to mesialize the molar and needs enough
bone to sustain the alveolar ridge width and height.
BoneCeramic increases bone density more and preserves
the alveolar ridge for a longer time than does Bio-Oss,
and there is no difference in tooth movement rates between BoneCeramic and Bio-Oss at the end of the orthodontic loading cycle. Therefore, BoneCeramic should be
grafted in the alveolar ridge defect.
Accompanied by tooth movement, root resorption
increased signicantly from days 0 to 7 after grafting
with BoneCeramic. This result agreed with our previous
experiment that most resorption occurred on the apical
third of the root on day 7.20 However, the whole root
resorption volume did not increase from days 7 to 28,
suggesting that the root resorption craters were stabilized. The mesiolingual and distolingual roots showed
great amounts of root resorption and stress on the
root surfaces. These ndings are supported by those of
Chan and Darendeliler33 that more root resorption undergoes a higher level of stress. Interestingly, our reconstructed 3D images and histologic ndings of tooth
roots showed that wide or deep resorption craters did
not concentrate in the regions with the highest accumulated stress, but rather in the distal and apical regions.
This was because the tooth was tipped rather than translated forward in parallel. The distal and apical regions
were subjected to accumulated stress on the relatively
small root surface. The volumetric measurements and
nite element method model also conrmed that the
apical regions had smaller volumes and underwent
higher levels of stress per unit of area. Therefore, more
root resorption appeared in the distal and apical regions.
The root resorption volumes in the extraction sites preserved by BoneCeramic did not increase signicantly
compared with the other groups. We deduced that BoneCeramic is safe and therapeutic for alveolar bone formation and orthodontic tooth movement.
CONCLUSIONS

It is suggested that although BoneCeramic slows orthodontic tooth movement, it has a better osteoconductive potential and induces less root resorption compared

531

with Bio-Oss grafting and naturally recovered extraction

sites.
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