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Cervical vertebral bone mineral density changes inadolescents 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 vari-

ables 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)

E

valuation of patients' facial growth status is impor-tant in developing optimal orthodontic treatment

plans.1,2 Skeletal maturity status should beconsidered to determine effective timing for the use of

growth-modication appliances such as Class II func-tional appliances and headgears. It has been demon-

strated that the cervical vertebrae (C2 to C6) are a validanatomic reference for estimating skeletal maturation,

providing comparable results with those obtained by hand-wrist radiographic assessment.3 The cervical verte-

bral maturation (CVM) method has been widely used toestimate the skeletal maturity for orthodontists.3-6

However, many clinical studies observed that the CVMmethod has poor reliability and repeatability for

evaluation of bone maturity.7-9

A major limitation of the CVM method is that it clas-sies the stages of maturation based on qualitative de-scriptions 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) im-ages of clinical cone-beam computed tomography

(CBCT) for diagnosis and treatment planning.10

Since theCBCTimageeldof view caninclude thecervicalvertebrae,

recent studies have examined the applica bility of CBCT tothe assessment of skeletal maturity.11-13 However, thosestudies investigated only the general morphology of thecervical vertebrae, whereas CBCT can provide additionalinformation including bone mineral density (BMD).

It was observed that the BMD changes reect the phys-iology of bone development during childhood and adoles-

cence.14 A clinical computed tomography image has beenused as a standardized method to assess orthopedic

BMD.15 Many clinical studies have indicated that CBCT

a Resident, Division of Orthodontics, College of Dentistry, Ohio State University,

Columbus, Ohio. bAssociate 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.eAssociate 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, [email protected].

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

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ORIGINAL ARTICLE

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images can be used for volumetric assessment of

BMD.16-20 Combining the observations from theseprevious studies, we hypothesized that the clinicalCBCT-based 3D morphologic and volumetric BMD ana-

lyses for the cervical vertebrae can provide quantitative in-formation 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) whetherthose changes are associated with changes of the CVMstages and mandibular length. We used a longitudinalcomparison of those parameters measured in teenagedpatients before and after orthodontic treatment.

MATERIAL AND METHODS

The institutional review board of Ohio State Univer-sity approved this retrospective study. The CBCT images

were originally taken as diagnostic pretreatment andposttreatment records on routine orthodontic patientsat a collaborating university's graduate orthodonticclinic. This is their standard record procedure. Patientsreceived comprehensive orthodontic treatment withfull xed appliances and were excluded if they had

craniofacial anomalies, facial asymmetries, orthognathicsurgery, rapid palatal expansion, headgear, or extrac-tions (except third molars). Each image was taken at2 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 either292 or 377 mm. Eighty-two paired images from 41 pa-

tients (15 boys, 26 girls) randomly selected before (T1)and after (T2) orthodontic treatment were included forthis study. The average patient ages were 14.47 61.42 years at T1, and 16.15 6 1.38 years at T2. Individ-

ual patient treatment duration ranged from 9 to26 months, with an average duration of 20.17 months.

The 3D CBCTimages were imported to image-analysissoftware (ImageJ, National Institutes of Health,

Bethesda, Md). Two cervical vertebrae (C2 and C3) inthe same CBCT image were digitally cropped, separated,

and saved as individual image les ( Fig 1). Segmentationof bone voxelsfrom nonbone voxelsoutside thevertebrae

was performed automatically using a heuristic algorithmas in previous studies.21,22 Posterior processes weredigitally removed at 10 voxels from each side of the

vertebral end plate, leaving only the vertebral body inthe nal image ( Fig 1). Vertebral body volume was esti-

mated by multiplying the total bone voxel counts aftersegmentation by the volume per voxel. The gray level of each bone voxel, which is equivalent to BMD, was main-tained inside the vertebral body during the segmentationprocess. Gray-level histograms were obtained for the C2

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

was computed by dividing the sum of gray levels by thetotal count of voxels, and a standard deviation of gray-level 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 precisesegmentation between those voxels. Thus, our gray-level

values are comparable with conventional BMD values, but they would not be identical to those of bone tissuemineral density-equivalent gray levels that were obtainedfrom only bone voxels in a previous study.19

The CVM stage and mandibular length were assessed

in 2D cephalometric views by converting the same 3DCBCT images to their corresponding 2D lateral cephalo-metric views with orthodontic imaging software (Dol-phin3D; Dolphin Imaging & Management Solutions,

Chatsworth, Calif). The CVM stage was assigned accord-ing to the 5-stage method developed previously.6 Thismethod categorizes patients into 1 of 5 stages based onthe shape of the cervical vertebrae (C3 and C4) by assess-ing whether they are trapezoidal or rectangular in thehor-izontal dimension, square, or rectangular in the vertical

dimension, and by evaluating for the presence or absenceof a concavity on the inferior borders of C2, C3, and C4.

When using this method, peak mandibular growth is pre-sumed to occur between stages II and III. The mandibularlength was measured using the same 2D cephalometric

view for each patient at T1 and T2. The mandibular lengthmeasurement was based on the distance from condylion,

which was dened as the most posterior-superior pointon the condyle, to anatomic gnathion, which was denedas the midpoint between the most anterior-inferior pointon 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 repeatedmeasurements by the same examiner for an intrarater reli-ability test. An additional 5 images were randomly selected and evaluated by a second examiner (E.J.) to

determine the interrater reliability. Intrarater and inter-rater agreements were analyzed with the intraclass corre-lation coef cient with the Shrout-Fleiss random setmethod and single score method, respectively (SAS[r]

Proprietary Software 9.2; SAS Institute Inc, Cary, NC).23

Although this statistical test is intended for continuousrather than ranked data, this data set was perfectly

ranked, making this an appropriate evaluation.A paired t test was used to compare the vertebral vari-

ables (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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obtained using an absolute difference by subtractingmeasurements at T1 from those at T2. Then, the pairedt 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 correla-tions were examined for all parameters between T1and T2, and also between changes of the vertebral pa-rameters and the mandibular length. Spearman rank

correlations were tested between changes of the CVMstage and all other parameters. Signicance was set atP #0.05.

RESULTS

Interrater reliability between the 2 raters (B.C. and E.J.) was 0.54 for CVM. Intrarater reliability for the rstrater was 0.90 for the same variable.

Fig 2. Typical histograms of gray level at A, T1, and B, T 2 o f C 2 (black ) and C3 (gray ) vertebral bodies

of the same patient.

Fig 1. A typical CBCT image process to isolate the cervical vertebrae (C2 and C3). From the initial full

eld-of-view 3D image, thevertebrae are cropped and viewed as a single slice. Next, using thecropped

image, the vertebral voxels are separated from nonvertebral voxels, and the vertebral body is cropped

from the entire image.

Crawford et al 185

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The cervical vertebrae were successfully isolated from

the CBCT images ( Fig 1), providing the gray-level histo-grams at T1 and T2 ( Fig 2).

All variables at T1 had signicant positive correla-

tions with those at T2 (P #

0.027). The correlations be-tween T1 and T2 of the CVM stage and mandibularlength are shown in Figure 3.

The BMD means of both C2 and C3, CVM stage, andmandibular length signicantly increased during theobservation period (P \0.001) (Table I). The BMD stan-dard deviation and vertebral body volume of C2 signi-cantly decreased (P #0.018); the BMD standarddeviation of C3 signicantly decreased (P #0.006), butthe 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 forthe C3 vertebral body at T1 (P \0.001), whereas no sig-nicant difference was detectable at T2 (P 5 0.669). Themean of the vertebral body volume for the C2 vertebral

body was signicantly higher than that for the C3 verte-

bral 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 wasthe vertebral body volume (P \0.001) (Table II).

The changes of BMD standard deviation for C2 were

signicantly correlated with those of vertebral body vol-ume 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 volumeand 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 observationperiod. In contrast, the higher variability (standard devi-ation) of gray-level distribution for C2 at T1 decreased tothe same level as C3 at T2. Consistently, we found thatthe mean, standard deviation, and vertebral body vol-ume 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 observa-tion period for growing adolescents, resulting in thealteration of BMD distribution. This seems to indicatethat changes were occurring in the C2 vertebra that

were robust enough to be biologically meaningful dur-

ing this period. This activity cannot be dismissed, eventhough many view this as a nearly nongrowing periodas judged by CVM. It is still an active area of change

and development. We also found that the CVM leveland mandibular length increased during the sameperiod. Taken together, these results indicate that the

3D clinical CBCT-based analysis could provide informa-tion of BMD distribution and changes in both skeletalmaturation and facial growth.

Many studies have evaluated the applicability of CBCT for the assessment of BMD for patients in clinicalpractice.16-20 However, the consistency of CBCT-based

BMD measurements is still open to debate because of

questions regarding the variations of scanning condi-tions and target locations to scan.24-27 The patient-specic variations include the thickness of soft tissuesand the head position during the scan.28,29 On the

other hand, many recent studies have shown that theCBCT-based BMD measurement is reliable.16,19,30-32

Similar to these previous studies, we also found thatthe changes of gray-level variability could explain thedifference 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 resultingfrom bone modeling and remodeling.22,33,34 Activated

bone modeling is an uncoupled process by whichresorption of preexisting bone tissue and formation of

new bone tissue occur independently. The coupled bone remodeling process comprises new boneformation 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 mineraldensity. In this study, the C2 vertebral body hadgreater variability but a lower mean of gray levels,

indicating that more active bone modeling andremodeling occurred in the C2 vertebral body than inthe C3 vertebral body during the observation period.The high degree of bone remodeling of the C2

vertebral body subsided at T2, reaching a similar levelto that of the C3 vertebral body. These ndings wereconsistent with observations from a previous study

that showed a growth rate approximately twice as highfor C2 than for C3 in 14.5-year-old girls and progres-sively declining to the same level between C2 and C3in 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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change in adolescents; this would be related to othermaturational changes and specically at C2.

The lower level of bone remodeling in the C3 vertebral body at T1 most likely resulted from the develop-

ment of greater bone mineralization with lessresorption of the highly mineralized preexisting boneand less formation of the less mineralized new bone, re-sulting in the high mean of BMD values for C3 at T2. Thegreater 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

bone modeling and remodeling during the observationperiod. Again, C2 is a focus of activity.

The skeletal maturity estimated using CVMsignicantly increased along with the changes of other

parameters during the observation period. The signi-cant correlations between the changes of CVM stageand vertebral body volume indicated that the 2Dimage-based morphologic analysis of vertebrae usedfor 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,

Fig 3. Correlations of A, CVM stage (T2 5 0.5317 T1 1 2.0048; r 5 0.692; P \0.001) and B, mandib-

ular 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 T1 T2 P value

BMD mean

C2 1948.312 6 81.873 1997.257 6 50.028 \0.001

C3 1969.746 6 87.370 2054.788 6 2.916 \0.001

BMD SD

C2 141.635 6 27.739 121.063 6 13.299 \0.001

C3 133.530 6 23.642 120.504 6 13.829 \0.001

Vertebral body volume (mm3)

C2 6348.342 6 1109.801 5652.91 6 1933.960 0.018

C3 3411.728 6 671.176 3205.432 6 1115.353 0.210

CVM stage 2.9276

1.010 3.5616

0.776 \0.001 Mandibular length (mm) 115.827 6 5.261 119.022 6 5.813 \0.001

Table II. Comparison of changes (DT5 jT2-T1j) of vertebral parameters between C2 and C3, and DT values for CVMstages and mandibular length

Variable C2 vertebral body C3 vertebral body P value

DT BMD mean 65.022 6 44.566 91.450 6 55.838 \0.001

DT BMD SD 27.773 6 18.285 21.606 6 13.086 \0.001

DT (vertebral body volume) (mm3) 1436.676 6 1270.435 850.389 6 612.565 \0.001

DT (CVM stage) 0.63 6 0.733

DT (mandibular length) (mm) 3.278 6 2.717

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