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ORIGINAL ARTICLE

Hounsfield unit change in root and alveolar bone


during canine retraction
Feifei Jiang,a Sean S.-Y. Liu,b Zeyang Xia,c Shuning Li,d Jie Chen,e Katherine S. Kula,f and George Eckertg
Indianapolis, Ind, and Hong Kong, China

Introduction: The objective of this study was to determine the Hounsfield unit (HU) changes in the alveolar bone
and root surfaces during controlled canine retractions. Methods: Eighteen maxillary canine retraction patients
were selected for this split-mouth design clinical trial. The canines in each patient were randomly assigned to
receive either translation or controlled tipping treatment. Pretreatment and posttreatment cone-beam
computed tomography scans of each patient were used to determine tooth movement direction and HU
changes. The alveolar bone and root surface were divided into 108 divisions, respectively. The HUs in each
division were measured. Mixed-model analysis of variance was applied to test the HU change distribution at
the P \0.05 significance level. Results: The HU changes varied with the directions relative to the canine move-
ment. The HU reductions occurred at the root surfaces. Larger reductions occurred in the divisions that were
perpendicular to the moving direction. However, HUs decreased in the alveolar bone in the moving direction.
The highest HU reduction was at the coronal level. Conclusions: HU reduction occurs on the root surface in
the direction perpendicular to tooth movement and in the alveolar bone in the direction of tooth movement
when a canine is retracted. (Am J Orthod Dentofacial Orthop 2015;147:445-53)

B
one modeling and remodeling are essential to orthodontic tooth movement in patients is still lack-
orthodontic tooth movement.1 When using ing.2-5
mechanical forces to move the teeth with ortho- During tooth movement, the change of mechanical
dontic appliances, coupled bone formation and resorp- environment in terms of stress and strain in the PDL
tion occur on the tension and compression sides of the and bone triggers the biologic reaction. On the compres-
periodontal ligament (PDL). Although biologic responses sion side, osteoclasts are recruited and absorb the bone.
have been widely investigated in animal experiments, On the tension side, osteoblasts are recruited, and new
direct evidence of bone modeling and remodeling during bone is deposited.6,7 Different treatment strategies
introduce different stress distribution patterns in the
a
Postgraduate student, Department of Mechanical Engineering, Indiana Univer- PDL. A clinical study about the effect of treatment
sity-Purdue University, Indianapolis, Ind. strategy to biologic response will help to understand
b
Assistant professor, Department of Orthodontics and Oral Facial Genetics, Indi- the tooth movement mechanism.
ana University, Indianapolis, Ind.
c
Associate professor, Shenzhen Institutes of Advanced Technology, Chinese Cone-beam computed tomography (CBCT) technol-
Academy of Sciences and Chinese University of Hong Kong, Hong Kong, China. ogy can be used for acquiring 3-dimensional (3D) skel-
etal radiographs for dental uses.8 CBCT, which generates
d
Visiting assistant professor, Department of Mechanical Engineering, Indiana
University-Purdue University, Indianapolis, Ind.
e
Professor and chair, Department of Mechanical Engineering, Indiana Universi- lower doses of radiation than medical computed tomog-
ty-Purdue University, Indianapolis, Ind; professor, Department of Orthodontics raphy, allows us to assess bone densities during ortho-
and Oral Facial Genetics, Indiana University, Indianapolis, Ind.
f
dontic treatment.8 To evaluate bone remodeling on
Professor and chair, Department of Orthodontics and Oral Facial Genetics,
Indiana University, Indianapolis, Ind. CBCT images, Hounsfield units (HUs) have been used
g
Biostatistician supervisor, Department of Biostatistics, Indiana University, to represent bone mineral density (BMD) and to quan-
Indianapolis, Ind. tify relative changes in alveolar bone.9 The Hounsfield
All authors have completed and submitted the ICMJE Form for Disclosure of
Potential Conflicts of Interest, and none were reported. scale is used to measure radiodensity in medical
Supported by the NIH/NIDCR under grant #1R01DE018668. computed tomography scans; this provides accurate ab-
Address correspondence to: Jie Chen, Department of Mechanical Engineering solute density for bone or other tissues. Unlike medical
and Department of Orthodontics and Oral Facial Genetics, Indiana University-
Purdue University, 723 W Michigan St, SL260, Indianapolis, IN 46202; e-mail, computed tomography, assigned HUs to voxels in CBCT
jchen3@iupui.edu. images are relative HUs, which are affected by the sur-
Submitted, May 2014; revised and accepted, November 2014. rounding tissues10,11 and cannot be directly used to
0889-5406/$36.00
Copyright Ó 2015 by the American Association of Orthodontists. calculate BMD values.9,12 In addition, the Hounsfield
http://dx.doi.org/10.1016/j.ajodo.2014.11.027 scale varies between CBCT machines; this makes HU
445
446 Jiang et al

values incomparable between different CBCT systems.13 2.1 6 1.5 mm. Canine displacement and its direction
However, studies suggest that reliable HUs can be ob- at the end of canine retraction were determined from
tained from serial CBCT images during orthodontic the CBCT images.18
treatment using the same machine with identical scan- For each patient, segmental T-loops were randomly
ning settings.14,15 In this kind of longitudinal study with assigned to the right and left canines to implement
subjects as their own controls, HUs acquired from CBCT either translation or controlled tipping. The T-loop
are reportedly highly reliable compared with medical delivered approximately 125 cN of closing force with a
computed tomography and actual BMD, particularly predesigned moment-to-force ratio to provide a transla-
when evaluation of their percent changes is of tion or a controlled tipping load.19
interest.9,10,13,16,17 The maxillary CBCT scans were performed on the
Reduction in BMD with a decreased alveolar bone same i-CAT Next Generation Imaging System (Imaging
fraction was noted in both animal2-5 and human Sciences International, Hatfield, Pa).17-19 The field of
studies after tooth movement.14,15 Chang et al14 sug- view was 16 3 13.3 cm, voxel size was 0.25 mm, and
gested that maximum BMD reduction occurs along the scan time was 26.9 seconds. The scans of each patient
direction of the tooth movement, and Hsu et al15 showed were taken immediately before and after canine
BMD changes along the tooth's long axis as the tooth retraction. The same subject's posture with a head
moves. In these studies, tooth displacement in terms of strap and the same setting were used for all the scans.
magnitude and direction was not well defined, and the Both CBCT images were imported by 1 investigator
BMD was checked only in scattered areas. Furthermore, (F.J.) into Mimics (version 13.0; Materialise, Leuven,
HU change on the dental root surface indicating root Belgium) to reconstruct the 3D root and alveolar bone.
resorption during orthodontic treatment has not been The occlusal plane was aligned with the horizontal
reported previously. plane. The canine displacements were computed by
The aim of this prospective radiographic study was to overlapping the reconstructed 3D digital maxilla before
investigate HU changes in the root and surrounding and after canine retraction using the interactive closest
alveolar bone during canine retraction. The objectives point method. The calculated tooth displacement
were to determine (1) how the HUs change due to the included both tooth displacement and direction.18 The
canine retraction, and (2) whether the changes depend tooth movement direction was used to align the divi-
on the treatment strategies (translation vs controlled sions characterizing the locations of HU changes. To
tipping). study the HU changes, the root was segmented first.
The PDL was recognized as 1 voxel (0.25 mm) of radio-
lucency surrounding the root. The surrounding alveolar
MATERIAL AND METHODS bone within 2 radiopaque voxels (0.5 mm) to the PDL
After institutional review board approval from Indi- was formed into a bone shell. A root surface shell was
ana University and signed consents from patients, 18 pa- then defined by eroding the PDL with 2 voxels (Fig 1).
tients (7 male, 11 female) were recruited for this The root surface and alveolar bone shells were
prospective study. The inclusion criterion was necessity divided into 3 vertical levels, each with 36 circumferen-
for extraction of both maxillary first premolars and tial divisions. In the vertical direction, the serial axial
maxillary canine retraction for orthodontic treatment. slices from the root apex to the cervical enamel junc-
The average age of the patients was 19 6 9 years old tion were equally divided into 3 levels: apical, middle,
(range, 12-47 years). Before the study, the right and and coronal. In the occlusal plane, the shells were
left first premolars were extracted, and the maxillary divided into 36 divisions circumferentially around the
dental arch was leveled and aligned with tooth (D1 to D36). For the occlusal view, the divisions
0.019 3 0.025-in stainless steel archwire engaged in were labeled counterclockwise for the left canine and
0.022 3 0.028-in slot brackets. The maxillary clockwise for the right canine with the division in the
second molars were included in the archwire, and the direction of movement (compression side) labeled as
maxillary second premolar, first molar, and D1 (Fig 2). The divisions D19 on both canines were
second molar were coligated with a 0.010-in stainless opposite to the direction of movement and subjected
steel wire on each side. The bilateral first molars to tension. The divisions D2 to D18 were located on
were connected with a transpalatal arch to strengthen the buccal side, whereas D20 to D36 were on the
the anchorage. The canine retraction period varied lingual side. The average value of the HU of each divi-
depending on the size of initial space, appointment, sion in each level was computed from both pretreat-
and interpatient variations. The average was 4.9 months. ment and posttreatment CBCT scans. The changes in
The canines were displaced by an average of HU defined by subtraction of the pretreatment HU

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Jiang et al 447

Fig 1. Segmentation of the root, PDL, and surrounding alveolar bone: A, root identification; B, forma-
tion of PDL (yellow) and alveolar bone (red) as well as the root surface (blue); and C, alveolar bone shell
(red) and root surface shell (blue).

Fig 2. Formation of the root surface and alveolar bone shell and division of the 3 levels into 36 circum-
ferential regions for the left canine.

from the posttreatment HU at each division were Norfolk, Virginia) was scanned 5 times using the iden-
computed and plotted. tical CBCT settings, and 1 investigator (F.J.) determined
all HU measures. The phantom included 16 standard-
Statistical analysis ized BMD rods distributed on the dental arches, with
Mixed-model analysis of variance (ANOVA) was BMD ranging between 100 and 700 mg per cubic
used to evaluate the effects of treatment strategy, di- centimeter. The intraclass correlation coefficient
rection of tooth movement, and divisions by different (ICC) was calculated to assess the variation and the
thirds on HU changes. Random effects were included reliability.
for subject, subject-by-treatment, subject-by-direc- The errors due to the segmentation process were also
tion, and subject-by-division. Means, standard errors, assessed. The process for segmenting the root surface
and 95% confidence intervals for the means were esti- and surrounding alveolar bone from 1 CBCT scan was
mated using ANOVA. repeated 5 times. The averages and standard deviations
To assess the repeatability of the HU measurement of the HUs of all directions were computed at the root
obtained from the CBCT images, a custom-designed surface and the surrounding alveolar bone to estimate
phantom (Computerized Imaging Reference Systems, the segmentation errors and variations.

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448 Jiang et al

Fig 3. Average HU percent change distributions at the root surfaces. The red frames cover the divi-
sions in the direction of tooth movement, and the blue frames cover the divisions that were perpendic-
ular to the movement direction. The greatest HU reductions occurred in the directions in the blue
frames.

RESULTS Within the specific canine displacement directions,


The CBCT scans of a phantom with the same set- the reductions varied among the levels. Comparing the
tings have negligible variations, since the ICC was average HU values among the 3 levels, no significant dif-
determined to be 0.94 between the HU values of the ferences (P 5 0.3) were observed. However, the reduc-
standardized BMD rods and the HU values obtained tions among the 3 levels in the directions of D11 to
from the CBCT images, indicating high correlation D13 and D19 to D28 were significantly different
among the scans. The segmentation error test resulted (P \0.05).
in an average error of 3.1 HU for root surface and 3.3 We compared HU changes in root surface between
HU for surrounding alveolar bone; these are less than the 2 strategies. Both strategies resulted in reductions
1% of the maximum HU value. The method is adequate of HUs in root surfaces. The 2 treatment strategies re-
for this study. sulted in similar HU change patterns. No division showed
We studied HU changes at the root surface using the a statistically significant difference between the transla-
combined data from the 2 strategies. The average HU tion and controlled tipping strategies (Fig 4). There was
changes on the entire root surface due to canine retrac- no significant difference between the overall HU
tion are shown in Figure 3. In general, the HU values on changes as well (P 5 0.32).
the root surfaces decreased because of the treatment. At each level, the HU reductions also had no signifi-
Apparently, the HU reduction varied among the 3 levels. cant differences between the 2 strategies (P 5 0.61 for
The division average HU values were reduced by 1.7% the apical level, P 5 0.29 for the middle level, and
(611.2%), 2.0% (610.1%), and 2.9% (611.3%) at the P 5 0.29 for the coronal level). Considering the effects
apical, middle, and coronal levels, respectively. For the of levels on the HUs in each strategy, there were no sig-
HU reductions in different directions, the maximum nificant differences among the levels for controlled
average reductions occurred in D11 and D27, which tipping (P 5 0.47) or translation (P 5 0.24).
were approximately perpendicular to the direction of We used the combined data from the 2 strategies
movement. The maximum reductions were 4.3% to determine HU changes in surrounding alveolar
(611.6%) in D12 and 4.3% (611.2%) in D27. The bone. The average HU changes in the 3 levels in the
most severe reduction was at the coronal level. surrounding alveolar bone from the canine retractions
Without considering the level effect, the average di- are shown in Figure 5. The HUs on the surrounding
vision HU values in different color frames (blue and alveolar bone decreased in most directions. The
red) were significantly different (P \0.05), as seen in average division HUs were reduced by 4.2%
Figure 3. The HU was reduced more in D10 to D13 (626.3%), 3.0% (627.7%), and 11.0% (628.5%) at
and D25 to D28, than in D31 to D4 and D18 to D21. the apical, middle, and coronal levels, respectively.

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Jiang et al 449

Fig 4. Comparison of average HU percent changes in root boundary with treatment strategy.

Fig 5. Average HU percent change distributions in alveolar bone. The blue frames cover the divisions
in the direction of tooth movement, and the red frames cover the divisions that were perpendicular to the
movement direction. The greatest HU reductions occurred in the directions in the blue frames.

At each level, the maximum reductions occurred in D6 Without considering the level effect, the average
and D20, which were closely aligned to the tooth's division HU values in different color frames were
movement direction. The maximum reductions were significantly different (P \0.05). The HUs reduced
12.7% (628.6%) in D6 and 12.0% (633.7%) in the most in D17 to D22 and D35 to D8, and
D20. The maximum average increases occurred in increased in D10 to D14 and D26 to D28. Without
D12 and D27, which were approximately perpendic- considering the division effect, there were significant
ular to the direction of movement. The increases differences among the levels. The coronal level ob-
were about 8.1% (627.4%) in D12 and 3.1% tained more reduction than did the apical level
(625.4%) in D27. (P 5 0.04) and the middle level (P 5 0.01).

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450 Jiang et al

Fig 6. Comparison of average HU percent changes in alveolar bone with treatment strategy.

Considering the effect of the levels on the specific di- DISCUSSION


visions, the HU reductions in the directions of D27 to This study was focused on HU changes in the alveolar
D3 (distal and distolingual regions) were significantly bone and root surface as the canines move by 2 treat-
different (P \0.05). ment strategies, translation and controlled tipping. The
We compared HU changes in alveolar bone be- HU changes were expressed relative to the clinical tooth
tween the 2 strategies. The 2 treatment strategies re- movement direction for the purpose of this study. The
sulted in similar HU change patterns. No division orthodontic load systems on the canines were well
showed a statistically significant difference between controlled, with a higher moment-to-force ratios on
the translation and controlled tipping strategies. the translation side than on the controlled tipping
(Fig 6). There was no significant difference between side.19 However, the resulting canine displacements var-
the overall HU changes as well (P 5 0.62). At each ied and did not fully agree with the intended displace-
level, the HU changes had no significant differences ment pattern. Therefore, the controlled tipping and
between the 2 strategies (P 5 0.91 for the apical level, translation sides used in this study referred to the
P 5 0.83 for the middle level, and P 5 0.32 for the T-loop design rather than to the resulting clinical
coronal level). displacement patterns.
However, the 2 strategies showed some differ- The primary purpose of this study was to investigate
ences in the comparisons of the level differences HU changes; thus, only relative HUs were of interest.
individually. Considering each treatment strategy, Although using HUs from CBCT images has not been
there were no significant differences among the considered a reliable way to quantify absolute BMD, it
levels for translation in general (P 5 0.38), whereas is still the best method available to monitor changes of
there were significant differences among the levels BMD in terms of HUs through longitudinal studies as
for controlled tipping in general (P \0.05). For long as the same CBCT machine and the same scan set-
controlled tipping, HU reduction at the coronal level tings are used; this was validated in our repeatability
was greater than at the apical (P 5 0.03) and middle test. Our study showed that the multiple scans of the
(P 5 0.01) levels. The general significant level differ- same phantom with different standardized BMD rods
ence for controlled tipping was primarily introduced embedded at different locations produced consistent re-
at D27 to D3 (P \0.05, distal and distolingual re- sults (ICC, 0.94), proving that the HUs obtained from
gions), with the highest reduction at the coronal CBCT correlated well with the HUs obtained from stan-
level. dardized BMD rods. The results are also reliable because

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Jiang et al 451

the variations of the segmentation proved to be small divided the surrounding alveolar bone into 3 layers
(\1% of the maximum value). and only 4 directions, and the region studied did not
HUs at the surface layer of the canine roots cover all the surrounding alveolar bone. Generally, our
decreased in all divisions, indicating remodeling activ- results agree with the common belief that the alveolar
ities occurring on the root surface. Relatively larger re- bone remodels as the canine moves into the area in
ductions occurred at the divisions located closely front of it and models behind it. Both modeling and
perpendicular to the moving direction, indicating that remodeling result in formation of less mineralized bone.
high stress in the PDL might not be the only factor trig- The HU reductions because of bone modeling or re-
gering the remodeling. When the canine moves, the root modeling occurred with different intensities at the
experiences a high compressive stress in the moving di- different levels. In the moving direction (D33 to D6),
rection and tensile stress on the back. The stresses in the HU reduction at the coronal level was more severe
perpendicular directions are less affected. The observa- than at the apical and middle levels, indicating more po-
tion contradicts the theory that remodeling occurs at tential tipping. Because the larger bony areas are in front
high stress areas in bone. However, the root may of the root at the coronal level, relatively less dense bone
respond differently from bone; this needs to be further may be needed for the intended tooth movement. Con-
investigated. trary to the root surface, the high modeling and remod-
Higher HU reductions at the coronal level in the eling areas in the cortical plate of the alveolar bone
direction perpendicular to the movement direction indi- experience higher stresses and strains from orthodontic
cated higher remodeling activities resulting in relatively movement.
less dense root surfaces. The mechanical environment Considering the effects of treatment strategy on the
in the area is less affected by the orthodontic load HU reductions, only the controlled tipping side showed
than by the direction of tooth movement. Thus, the significant HU reductions among the 3 levels in certain
area experiences less resistance to tooth movement. directions. The load on the controlled tipping side had
The HUs at the apical level were reduced significantly a relatively lower moment-to-force ratio, which resulted
in certain divisions (D10 to D13 and D25 to D28). The in a relatively higher compressive force at the coronal
apex has a small surface area. When its density decreases, level. As shown in Figure 6, the coronal level showed a
it becomes vulnerable to surface loss, which may result statistically significant higher HU reduction than at the
in root shortening. Consistent surface density loss for a apical level, especially in the moving direction (D33 to
longer time may be the beginning of root resorption, D3), which may be due to the higher compressive stress.
which has been observed clinically.20 Treatment strategy differences did not lead to overall
HUs in the surrounding alveolar bone had mixed significant differences in the HU change distribution in
changes. The HUs of the bone decreased along the di- the root surface or surrounding alveolar bone. Signifi-
rection of tooth movement and slightly increased cant differences were determined only in a few divisions.
perpendicular to the moving direction. Contrary to The results may explain the conclusion from a previous
the root, the maximum HU reduction occurred in the study, which showed that apical root resorption was
direction of tooth movement (D33 to D6). The bone not related to translation or tipping of the root.21
on the tension side also experienced a significant HU Clinicians must understand the biologic changes
reduction. The results confirmed the general finding that occur as a tooth moves. The rate of orthodontic
of Chang et al14 that the BMD reduces in the direction tooth movement largely depends how fast the alveolar
of tooth movement, but our results showed less reduc- bone resorbs in the direction of tooth movement,
tion. The average HU reduction (4.2%-11.0% among which can be observed as a change in HUs with cur-
the levels) in alveolar bone in this study was less than rent CBCT technologies. In our study, relative HUs
the 24% reported by Chang et al and Hsu et al.15 On in the alveolar bone and on the root surface were
the other hand, HUs increased in D10 to D14 and D26 quantified, providing meaningful information for pre-
to D28, which were approximately perpendicular to dicting tooth movement and potential root resorption.
the moving direction. Only 2 of 144 teeth showed Furthermore, the HU changes can be used as an indi-
increased BMD around the teeth in previous cator to evaluate responses of root and surrounding
reports.14,15 The inconsistency could be due to bone with different clinical loading and treatment
differences in treatment and analysis. In those studies, strategies.
the treatment period (7 months) was longer than ours One limitation of this study was resolution. When this
(4.9 months); the tooth displacement was shorter clinical study was started, the highest resolution of
(nonextraction orthodontic treatments) than ours 0.125-mm voxel size for this CBCT system was not cho-
(space closure treatment). Furthermore, their studies sen because it requires a longer scan time. Motion blur

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452 Jiang et al

occurred even with strapping the head of each patient. 3. HUs changed in the surrounding alveolar bone. The
Therefore, the 0.25-mm voxel size was used to obtain maximum reduction was in the direction of the
consistently satisfactory images. This problem can be tooth movement and at the coronal level.
solved by future CBCT technology with higher resolu- 4. Translation and controlled tipping have similar ef-
tions over a shorter scanning time. fects on HU changes.
Next, although the trend of bone resorption was
observed with reliable HU values between CBCT scans
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