ORIGINAL ARTICLE

Cervical vertebral bone mineral density changes in

adolescents during orthodontic treatment
Bethany Crawford,a Do-Gyoon Kim,b Eun-Sang Moon,c Elizabeth Johnson,a Henry W. Fields,d J. Martin Palomo,e
and William M. Johnstonf
Columbus and Cleveland, Ohio

Introduction: The cervical vertebral maturation (CVM) stages have been used to estimate facial growth status.
In this study, we examined whether cone-beam computed tomography images can be used to detect changes of
CVM-related parameters and bone mineral density distribution in adolescents during orthodontic treatment.
Methods: Eighty-two cone-beam computed tomography images were obtained from 41 patients before
(14.47 6 1.42 years) and after (16.15 6 1.38 years) orthodontic treatment. Two cervical vertebral bodies
(C2 and C3) were digitally isolated from each image, and their volumes, means, and standard deviations of
gray-level histograms were measured. The CVM stages and mandibular lengths were also estimated after
converting the cone-beam computed tomography images. Results: Signicant changes for the examined variables were detected during the observation period (P #0.018) except for C3 vertebral body volume (P 5 0.210).
The changes of CVM stage had signicant positive correlations with those of vertebral body volume (P #0.021).
The change of the standard deviation of bone mineral density (variability) showed signicant correlations with
those of vertebral body volume and mandibular length for C2 (P #0.029). Conclusions: The means and
variability of the gray levels account for bone mineral density and active remodeling, respectively. Our results
indicate that bone mineral density distribution and the volume of the cervical vertebral body changed because
of active bone remodeling during maturation. (Am J Orthod Dentofacial Orthop 2014;146:183-9)

valuation of patients' facial growth status is important in developing optimal orthodontic treatment
plans.1,2 Skeletal maturity status should be
considered to determine effective timing for the use of
growth-modication appliances such as Class II functional appliances and headgears. It has been demonstrated that the cervical vertebrae (C2 to C6) are a valid
anatomic reference for estimating skeletal maturation,

a
Resident, Division of Orthodontics, College of Dentistry, Ohio State University,
Columbus, Ohio.
b
Associate professor, Division of Orthodontics, College of Dentistry, Ohio State
University, Columbus, Ohio.
c
Predoctoral student, College of Dentistry, Ohio State University, Columbus, Ohio.
d
Professor, Division of Orthodontics, College of Dentistry, Ohio State University,
Columbus, Ohio.
e
Associate professor, Department of Orthodontics, School of Dental Medicine, Case
Western Reserve University, Cleveland, Ohio.
f
Professor, Division of Restorative, Prosthetic and Primary Care Dentistry, College
of Dentistry, Ohio State University, Columbus, Ohio.
All authors have completed and submitted the ICMJE Form for Disclosure of
Potential Conicts of Interest, and none were reported.
Financial support from the Delta Dental Foundation through the Dental Master's
Thesis Award Program.
Address correspondence to: Do-Gyoon Kim, Division of Orthodontics, College of
Dentistry, Ohio State University, 4088 Postle Hall, 305 W 12th Ave, Columbus,
OH 43210; e-mail, kim.2508@osu.edu.
Submitted, June 2013; revised and accepted, April 2014.
0889-5406/$36.00
Copyright 2014 by the American Association of Orthodontists.
http://dx.doi.org/10.1016/j.ajodo.2014.04.019

providing comparable results with those obtained by

hand-wrist radiographic assessment.3 The cervical vertebral maturation (CVM) method has been widely used to
estimate the skeletal maturity for orthodontists.3-6
However, many clinical studies observed that the CVM
method has poor reliability and repeatability for
evaluation of bone maturity.7-9
A major limitation of the CVM method is that it classies the stages of maturation based on qualitative descriptions of cervical vertebral shape on a 2-dimensional
(2D) cephalogram. Thus, the estimated CVM stages vary
because of possible observer bias. On the other hand,
more dental providers are using 3-dimensional (3D) images of clinical cone-beam computed tomography
(CBCT) for diagnosis and treatment planning.10 Since the
CBCT image eld of view can include the cervical vertebrae,
recent studies have examined the applicability of CBCT to
the assessment of skeletal maturity.11-13 However, those
studies investigated only the general morphology of the
cervical vertebrae, whereas CBCT can provide additional
information including bone mineral density (BMD).
It was observed that the BMD changes reect the physiology of bone development during childhood and adolescence.14 A clinical computed tomography image has been
used as a standardized method to assess orthopedic
BMD.15 Many clinical studies have indicated that CBCT
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184

images can be used for volumetric assessment of

BMD.16-20 Combining the observations from these
previous studies, we hypothesized that the clinical
CBCT-based 3D morphologic and volumetric BMD analyses for the cervical vertebrae can provide quantitative information to estimate a patient's skeletal maturity. Thus,
the objectives of this study were to examine (1) whether
CBCT images can be used to detect changes of cervical
vertebral volume and BMD distribution and (2) whether
those changes are associated with changes of the CVM
stages and mandibular length. We used a longitudinal
comparison of those parameters measured in teenaged
patients before and after orthodontic treatment.
MATERIAL AND METHODS

The institutional review board of Ohio State University approved this retrospective study. The CBCT images
were originally taken as diagnostic pretreatment and
posttreatment records on routine orthodontic patients
at a collaborating university's graduate orthodontic
clinic. This is their standard record procedure. Patients
received comprehensive orthodontic treatment with
full xed appliances and were excluded if they had
craniofacial anomalies, facial asymmetries, orthognathic
surgery, rapid palatal expansion, headgear, or extractions (except third molars). Each image was taken at
2 mA and 120 kV with a Hitachi CB MercuRay scanner
(Hitachi Medical Systems America, Twinsburg, Ohio)
(Fig 1). The voxel size of the 3D CBCT image was either
292 or 377 mm. Eighty-two paired images from 41 patients (15 boys, 26 girls) randomly selected before (T1)
and after (T2) orthodontic treatment were included for
this study. The average patient ages were 14.47 6
1.42 years at T1, and 16.15 6 1.38 years at T2. Individual patient treatment duration ranged from 9 to
26 months, with an average duration of 20.17 months.
The 3D CBCT images were imported to image-analysis
software (ImageJ, National Institutes of Health,
Bethesda, Md). Two cervical vertebrae (C2 and C3) in
the same CBCT image were digitally cropped, separated,
and saved as individual image les (Fig 1). Segmentation
of bone voxels from nonbone voxels outside the vertebrae
was performed automatically using a heuristic algorithm
as in previous studies.21,22 Posterior processes were
digitally removed at 10 voxels from each side of the
vertebral end plate, leaving only the vertebral body in
the nal image (Fig 1). Vertebral body volume was estimated by multiplying the total bone voxel counts after
segmentation by the volume per voxel. The gray level of
each bone voxel, which is equivalent to BMD, was maintained inside the vertebral body during the segmentation
process. Gray-level histograms were obtained for the C2

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and C3 vertebral bodies at T1 and T2 (Fig 2). A mean value

was computed by dividing the sum of gray levels by the
total count of voxels, and a standard deviation of graylevel distribution was also computed using the histogram
for each vertebral body. We used BMD-equivalent gray
levels that were obtained from both bone and nonbone
(bone marrow) voxels inside the vertebral body because
the rough resolution of the clinical images limited precise
segmentation between those voxels. Thus, our gray-level
values are comparable with conventional BMD values,
but they would not be identical to those of bone tissue
mineral density-equivalent gray levels that were obtained
from only bone voxels in a previous study.19
The CVM stage and mandibular length were assessed
in 2D cephalometric views by converting the same 3D
CBCT images to their corresponding 2D lateral cephalometric views with orthodontic imaging software (Dolphin3D; Dolphin Imaging & Management Solutions,
Chatsworth, Calif). The CVM stage was assigned according to the 5-stage method developed previously.6 This
method categorizes patients into 1 of 5 stages based on
the shape of the cervical vertebrae (C3 and C4) by assessing whether they are trapezoidal or rectangular in the horizontal dimension, square, or rectangular in the vertical
dimension, and by evaluating for the presence or absence
of a concavity on the inferior borders of C2, C3, and C4.
When using this method, peak mandibular growth is presumed to occur between stages II and III. The mandibular
length was measured using the same 2D cephalometric
view for each patient at T1 and T2. The mandibular length
measurement was based on the distance from condylion,
which was dened as the most posterior-superior point
on the condyle, to anatomic gnathion, which was dened
as the midpoint between the most anterior-inferior point
on the bony chin.
All CVM stage evaluations were performed by a
blinded examiner (B.C.) using the randomly coded CBCT
images. Five images were randomly selected for repeated
measurements by the same examiner for an intrarater reliability test. An additional 5 images were randomly
selected and evaluated by a second examiner (E.J.) to
determine the interrater reliability. Intrarater and interrater agreements were analyzed with the intraclass correlation coefcient with the Shrout-Fleiss random set
method and single score method, respectively (SAS[r]
Proprietary Software 9.2; SAS Institute Inc, Cary, NC).23
Although this statistical test is intended for continuous
rather than ranked data, this data set was perfectly
ranked, making this an appropriate evaluation.
A paired t test was used to compare the vertebral variables (mean, standard deviation, and vertebral volume),
CVM stage, and mandibular length between T1 and T2.
The changes in all parameters between T1 and T2 were

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Fig 1. A typical CBCT image process to isolate the cervical vertebrae (C2 and C3). From the initial full
eld-of-view 3D image, the vertebrae are cropped and viewed as a single slice. Next, using the cropped
image, the vertebral voxels are separated from nonvertebral voxels, and the vertebral body is cropped
from the entire image.

Fig 2. Typical histograms of gray level at A, T1, and B, T2 of C2 (black) and C3 (gray) vertebral bodies
of the same patient.

obtained using an absolute difference by subtracting

measurements at T1 from those at T2. Then, the paired
t test was used to compare the values and the changes of
the vertebral parameters (mean, standard deviation, and
vertebral volume) between C2 and C3. Pearson correlations were examined for all parameters between T1
and T2, and also between changes of the vertebral parameters and the mandibular length. Spearman rank

correlations were tested between changes of the CVM

stage and all other parameters. Signicance was set at
P #0.05.
RESULTS

Interrater reliability between the 2 raters (B.C. and

E.J.) was 0.54 for CVM. Intrarater reliability for the rst
rater was 0.90 for the same variable.

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186

The cervical vertebrae were successfully isolated from

the CBCT images (Fig 1), providing the gray-level histograms at T1 and T2 (Fig 2).
All variables at T1 had signicant positive correlations with those at T2 (P #0.027). The correlations between T1 and T2 of the CVM stage and mandibular
length are shown in Figure 3.
The BMD means of both C2 and C3, CVM stage, and
mandibular length signicantly increased during the
observation period (P \0.001) (Table I). The BMD standard deviation and vertebral body volume of C2 signicantly decreased (P #0.018); the BMD standard
deviation of C3 signicantly decreased (P #0.006), but
the vertebral body volume of C3 was not signicantly
different (P 5 0.210) during the observation period.
The mean of the gray levels for the C2 vertebral body
was signicantly lower than that for the C3 vertebral
body at both T1 and T2 (P \0.001) (Table I). In contrast,
the mean of the standard deviation values for the C2
vertebral body was signicantly higher than that for
the C3 vertebral body at T1 (P \0.001), whereas no signicant difference was detectable at T2 (P 5 0.669). The
mean of the vertebral body volume for the C2 vertebral
body was signicantly higher than that for the C3 vertebral body at both T1 and T2 (P \0.001).
The changes of BMD mean and standard deviation
were signicantly different between C2 and C3, as was
the vertebral body volume (P \0.001) (Table II).
The changes of BMD standard deviation for C2 were
signicantly correlated with those of vertebral body volume and mandibular length (P #0.029) (Table III). The
changes of BMD standard deviation for C3 and that of
mandibular length were signicantly correlated
(P 5 0.018). The changes of vertebral body volume
and CVM were positively correlated for both C2 and C3
(P #0.021).
DISCUSSION

The means of the gray levels, which are equivalent to

BMD, were signicantly different between the C2 and C3
cervical vertebrae and increased during the observation
period. In contrast, the higher variability (standard deviation) of gray-level distribution for C2 at T1 decreased to
the same level as C3 at T2. Consistently, we found that
the mean, standard deviation, and vertebral body volume of C2 changed signicantly more than those of
C3 during the observation period. These results imply
that more bone remodeling occurred in the C2 vertebral
body than in the C3 vertebral body during the observation period for growing adolescents, resulting in the
alteration of BMD distribution. This seems to indicate
that changes were occurring in the C2 vertebra that

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were robust enough to be biologically meaningful during this period. This activity cannot be dismissed, even
though many view this as a nearly nongrowing period
as judged by CVM. It is still an active area of change
and development. We also found that the CVM level
and mandibular length increased during the same
period. Taken together, these results indicate that the
3D clinical CBCT-based analysis could provide information of BMD distribution and changes in both skeletal
maturation and facial growth.
Many studies have evaluated the applicability of
CBCT for the assessment of BMD for patients in clinical
practice.16-20 However, the consistency of CBCT-based
BMD measurements is still open to debate because of
questions regarding the variations of scanning conditions and target locations to scan.24-27 The patientspecic variations include the thickness of soft tissues
and the head position during the scan.28,29 On the
other hand, many recent studies have shown that the
CBCT-based BMD measurement is reliable.16,19,30-32
Similar to these previous studies, we also found that
the changes of gray-level variability could explain the
difference of the morphologic parameter (volume) of
C2 that showed more alteration during the observation
period.
The mean of gray levels is equivalent to the averaged
BMD of each vertebral body. The standard deviation of
gray levels accounts for variability of BMD resulting
from bone modeling and remodeling.22,33,34 Activated
bone modeling is an uncoupled process by which
resorption of preexisting bone tissue and formation of
new bone tissue occur independently. The coupled
bone remodeling process comprises new bone
formation after resorption.35-39 Because the newly
forming bone tissue has less tissue mineral density
than does preexisting bone tissue, the variability of
tissue mineral density inherently increases. Prolonged
progressive mineralization of bone tissue after new
bone formation alters the variability of tissue mineral
density. In this study, the C2 vertebral body had
greater variability but a lower mean of gray levels,
indicating that more active bone modeling and
remodeling occurred in the C2 vertebral body than in
the C3 vertebral body during the observation period.
The high degree of bone remodeling of the C2
vertebral body subsided at T2, reaching a similar level
to that of the C3 vertebral body. These ndings were
consistent with observations from a previous study
that showed a growth rate approximately twice as high
for C2 than for C3 in 14.5-year-old girls and progressively declining to the same level between C2 and C3
in the same patients at the age of 16.5 years.40 Hence,
these cervical vertebrae are an active region of bony

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Fig 3. Correlations of A, CVM stage (T2 5 0.5317 T1 1 2.0048; r 5 0.692; P \0.001) and B, mandibular length (T2 5 1.028 T1; r 5 0.999; P \0.001) between T1 and T2.

Table I. Comparison between T1 and T2 for all parameters

Parameter
BMD mean
C2
C3
BMD SD
C2
C3
Vertebral body volume (mm3)
C2
C3
CVM stage
Mandibular length (mm)

T1

T2

P value

1948.312 6 81.873
1969.746 6 87.370

1997.257 6 50.028
2054.788 6 2.916

\0.001
\0.001

141.635 6 27.739
133.530 6 23.642

121.063 6 13.299
120.504 6 13.829

\0.001
\0.001

6348.342 6 1109.801
3411.728 6 671.176
2.927 6 1.010
115.827 6 5.261

5652.91 6 1933.960
3205.432 6 1115.353
3.561 6 0.776
119.022 6 5.813

0.018
0.210
\0.001
\0.001

Table II. Comparison of changes (DT 5 jT2-T1j) of vertebral parameters between C2 and C3, and DT values for CVM

stages and mandibular length

Variable
DT BMD mean
DT BMD SD
DT (vertebral body volume) (mm3)
DT (CVM stage)
DT (mandibular length) (mm)

C2 vertebral body
65.022 6 44.566
27.773 6 18.285
1436.676 6 1270.435
0.63 6 0.733
3.278 6 2.717

change in adolescents; this would be related to other

maturational changes and specically at C2.
The lower level of bone remodeling in the C3 vertebral body at T1 most likely resulted from the development of greater bone mineralization with less
resorption of the highly mineralized preexisting bone
and less formation of the less mineralized new bone, resulting in the high mean of BMD values for C3 at T2. The
greater change in vertebral body volume for C2 than C3
vertebral bodies at T2 supported these observations
because this volume change could result from the active

C3 vertebral body
91.450 6 55.838
21.606 6 13.086
850.389 6 612.565

P value
\0.001
\0.001
\0.001

bone modeling and remodeling during the observation

period. Again, C2 is a focus of activity.
The skeletal maturity estimated using CVM
signicantly increased along with the changes of other
parameters during the observation period. The signicant correlations between the changes of CVM stage
and vertebral body volume indicated that the 2D
image-based morphologic analysis of vertebrae used
for CVM could partly account for the 3D changes of
vertebral volume. In addition, the values obtained at
T1 had signicant correlations with those at T2,

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Table III. Correlations of changes (DT 5 jT2-T1j) of

vertebral parameters with those of CVM stage and

mandibular length

Parameter
DT BMD mean
C2
C3
DT BMD SD
C2

DT (vertebral
body volume)
(mm3)

DT (CVM
stage)

DT (mandibular
length) (mm)

NS
NS

NS
NS

NS
NS

r 5 0.628
P \0.001
NS

NS

r 5 0.340
P 5 0.029
r 5 0.367
P 5 0.018

C3

NS

DT (vertebral body volume) (mm3)

C2
r51
r 5 0.403
P 5 0.009
C3
r51
r 5 0.360
P 5 0.021

NS
NS

NS, Not signicant.

suggesting that the progress of growth and maturity

can be estimated by having the patient's parameters
measured at T1. Furthermore, the alteration of
mandibular length was associated with the change of
bone mineral variability (standard deviation) resulting
from bone remodeling activity. More studies to
investigate mandibular bone mineral distribution are
needed to clarify how the bone remodeling controls
the morphologic change during maturation of the
mandible.
A limitation of this study was that only 2 longitudinal adolescent age groups at T1 and T2 were examined.
It has been strongly recommended that a series of CBCT
images should not be taken from younger patients.
Thus, CBCT images of younger patients are rare. Baccetti et al6 indicated that the 5-stage method would
not provide substantial changes of C2 and C3 after
CVM stage III, which might result in the less change
of CVM stage between T1 (average, stage III) and T2
(average, stage III ) as assessed in our study. Despite
these concerns, in the current range of patient ages,
all parameters including CVM stages, mandibular
length, bone mineral distribution, and vertebral body
volume signicantly changed during the observation
period. Thus, in this retrospective study, we focused
on examining whether the 3D image-based analyses
could provide a better explanation for the signicant
changes between T1 and T2, and their relationships
were demonstrated. This should prove even more
powerful when more robust data are used. The age
range that we examined could be expanded to include
prepeak, peak, and postpeak changes.40 There were no
sex effects on the results.

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Another limitation was that the bone voxels inside

the vertebral body were not segmented from nonbone
voxels, although the nonbone voxels outside the vertebral body were successfully excluded. The rough clinical
CBCT-image resolution did not allow for accurate separation between bone and nonbone voxels. Thus, the gray
levels of this study represent BMD values that included
bone marrow gray levels in part as the conventional
BMD was measured.15 As such, these results of BMD
distribution are comparable with those that are readily
obtained from the clinical CBCT images.
In spite of these limitations, these data indicate that
C2 is a highly active area that cannot be dismissed, even
in the latter stages of growth. The signicant changes
related to BMD, vertebral volume, and mandibular
length make this a vital and directly explorable area via
CBCT that provides opportunities not available with
2D methods. Although these data do not demonstrate
denitive clinically signicant relationships at this
time, they do provide a window to potentially meaningful relationships.
CONCLUSIONS

To our best knowledge, this study is the rst to

examine the applicability of BMD distribution for the
assessment of bone maturation using the 3D clinical
CBCT images taken from dental patients. Our conclusions can be summarized as follows.
1.

2.
3.

4.

The 3D CBCT image-based analysis can detect significant changes of BMD distribution and morphology
during the observation period.
A patient's initial CBCT information can be used to
estimate the progress of growth and maturity.
Two-dimensional image-based CVM changes can
partly be accounted for by the 3D changes of vertebral volume.
The clinical 3D CBCT image-based analysis of BMD
distribution can provide additional information to
assess a patient's maturity.

ACKNOWLEDGMENTS

We thank the Craniofacial Imaging Center at Case

Western Reserve University for the CBCT images used
in this study.
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American Journal of Orthodontics and Dentofacial Orthopedics

August 2014
Vol 146
Issue 2