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: Significant 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 significant positive correlations with those of vertebral body volume (P #0.021). The change of the standard deviation of bone mineral density (variability) showed significant 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)

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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-modification 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 Conflicts 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 Ó 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 classifies 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 field 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 reflect 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 183

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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 fixed 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 files (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 final 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 defined as the most posterior-superior point on the condyle, to anatomic gnathion, which was defined 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 coefficient 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 field-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. Significance 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 first rater was 0.90 for the same variable.

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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 significant 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 significantly increased during the observation period (P \0.001) (Table I). The BMD standard deviation and vertebral body volume of C2 significantly decreased (P #0.018); the BMD standard deviation of C3 significantly decreased (P #0.006), but the vertebral body volume of C3 was not significantly different (P 5 0.210) during the observation period. The mean of the gray levels for the C2 vertebral body was significantly 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 significantly higher than that for the C3 vertebral body at T1 (P \0.001), whereas no significant difference was detectable at T2 (P 5 0.669). The mean of the vertebral body volume for the C2 vertebral body was significantly 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 significantly 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 significantly 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 significantly 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 significantly 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 significantly 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 patientspecific 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 findings 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 specifically 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 significantly increased along with the changes of other parameters during the observation period. The significant 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 significant 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 significant.

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 ½) 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 significantly 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 significant 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 significant 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 definitive clinically significant relationships at this time, they do provide a window to potentially meaningful relationships. CONCLUSIONS

To our best knowledge, this study is the first 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. REFERENCES 1. Baccetti T, Franchi L, Cameron CG, McNamara JA Jr. Treatment timing for rapid maxillary expansion. Angle Orthod 2001;71: 343-50. 2. Kopecky GR, Fishman LS. Timing of cervical headgear treatment based on skeletal maturation. Am J Orthod Dentofacial Orthop 1993;104:162-9.

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Cervical vertebral bone mineral density changes in adolescents during orthodontic treatment.

The cervical vertebral maturation (CVM) stages have been used to estimate facial growth status. In this study, we examined whether cone-beam computed ...
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