International Orthodontics 2020; 18: 258–265

Websites:
www.em-consulte.com
www.sciencedirect.com
Original article

Reliability of cephalograms derived of cone

beam computed tomography versus lateral
cephalograms to estimate cervical vertebrae
maturity in a Peruvian population:
A retrospective study

Gustavo Echevarría-Sánchez 1, Luis Ernesto Arriola-Guillén 2, Violeta Malpartida-Carrillo 1,

Pedro Luis Tinedo-López 1, Ricardo Palti-Menendez 3, Maria Eugenia Guerrero 1,4

Available online: 31 January 2020
1. Universidad Científica del Sur, Division of Oral Implantology, School of Dentistry,
Lima, Peru
2. Universidad Científica del Sur, School of Dentistry, Division of Orthodontics and
Division of Oral and Maxillofacial Radiology, Lima, Peru
3. IDM Center, Private Practice, Lima, Peru
4. Universidad Nacional Mayor de San Marcos, Faculty of Dentistry, Medico Surgical
Department, Lima, Peru

Correspondence:
Luis Ernesto Arriola-Guillén, Universidad Científica del Sur, Faculty of Dentistry,
Division of Orthodontics, Calle Los Girasoles 194, Surco, Lima, Peru.
luchoarriola@gmail.com

Keywords Summary
Reliability
Cervical vertebrae Objective > Cone beam computed tomography (CBCT) images can be useful for estimating cervical
maturation vertebrae maturity (CVM). The aim of this study was to evaluate the reliability of cephalograms
Cephalometry derived from CBCT versus lateral cephalograms (LC) to estimate the CVM in a Peruvian population.
Cone-beam CT Material and methods > The sample evaluated consisted of 40 cephalograms derived from CBCT
and 40 LC images from individuals aged 10–19 years. One trained and calibrated observer (Kappa
scores  0.90) interpreted the CBCT and LC images twice. Intra-observer reliability of each
maturation stage on CBCT sagittal slices and LC images were analysed using the weighted kappa
statistics (a = 0.05). Comparison of CVM stages between CBCT slices and LC images were analysed
by the Spearman rank correlation coefficient, p < 0.05.
Results > The weighted kappa test showed almost perfect intra-observer agreement for the CVM
stages using the CBCT sagittal slices (0.873). Considering the LC images, the weighted kappa test
showed almost perfect intra-observer agreement too (0.937). In both intra-observer agreement, the
difference was limited to one maturation stage of the CVM method. The first and second intra-observer
agreement for the CVM stages between the CBCT sagittal slices and LC images were almost perfect
(0.937 and 0.874). High correlation values at the first (0.975) and second (0.976) intra-observer
agreement for the CVM stages between CBCT sagittal slices and LC images were also found.
Conclusion > CBCT is a reliable method for CVM assessment and can be used as an alternative
method for this purpose. The orthodontists might use the CBCT scans as a valuable tool for CVM
method estimation.
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https://doi.org/10.1016/j.ortho.2020.01.001
© 2020 CEO. Published by Elsevier Masson SAS. All rights reserved.
Reliability of cephalograms derived of cone beam computed tomography versus lateral cephalograms to
estimate cervical vertebrae maturity in a Peruvian population: A retrospective study

Original article
Introduction These contradictory results indicate that more investigations
Skeletal maturity or skeletal age informs clinicians of the relative are needed. On the other hand, these studies were performed
maturity of a patient's skeleton at a particular time and is in Canadian [21] and Japanese populations [22]. Hence,
influenced by his or her own biological clock [1]. Research additional studies in different populations are required to
has reported different biological indicators to determinate determine if using a cephalogram derived from CBCT as a
human development including height, weight, chronological diagnostic method can determine the bone maturity stage.
age, voice change, sexual maturation, dental development, With this in mind, when an orthodontist immediately requires
and biomarkers such as insulin-like growth factor I (IGF-I) a CBCT in a specific case, additional cephalometric radiograph
[2–6]. However, skeletal development of the hand and wrist could be avoided for the assessment of skeletal maturity. Hence,
and cervical vertebrae morphology are the most common the objective of this study was to evaluate the reliability of
methods that have been used as indicators of adolescent devel- cephalograms derived from CBCT sagittal slices for assessment
opment. These valuable tools allow clinicians to better select the of CVM method and to compare the CVM method estimation
treatment time for dentofacial orthopaedics, orthodontic, between CBCT sagittal slices and LC images.
orthognathic surgery, and the most appropriate earliest age
Materials and methods
for dental implants placement [7].
The hand-wrist bone analysis is a reliable method for skeletal Materials
maturity assessment [8,9]. Nevertheless, complexity in This retrospective and comparative study was approved by the
landmark identification, time spent, and additional radiation Ethics Committee of Universidad Científica del Sur, Lima, Perú,
exposure are the primary disadvantages [10]. Because of these with the approval N8 000288. This study included LC and CBCTs of
limitations, Lamparski [11] introduced another method for the same patients, obtained in a period of time that did not
assessment of skeletal maturity considering morphological exceed one month between both acquisitions. These auxiliary
changes in the cervical vertebrae called the cervical vertebrae exams were requested by orthodontists or maxillofacial
maturation (CVM) index. Following this guidance, Baccetti et al.
[12] proposed a modified version of the CVM method evaluating
only three cervical vertebrae (C2, C3, and C4) routinely visual-
ized in a lateral cephalometric radiograph. This analysis can be
performed on conventional or digital lateral cephalograms (LC)
and is valid and clinically reliable in predicting the pubertal
growth spurt [13,14]. However, limitations in CVM methods
have been informed using LC, such as difficulties distinguishing
altered ratios of height and width of vertebrae, insufficient
distinctive landmarks, and potential distortion in the sagittal
plane [15]. Several early studies, showed poor reproducibility
and stated the difficulty in classifying the vertebrae bodies on
the CVM method [16,17].
As a result of recent advances in the field of radiology, cone
beam computed tomography (CBCT) has become more popular
as an investigating tool in dental practice allowing the exhibition
of images in all three planes of space (axial, coronal and sagittal
sections). Although, CBCT is available at a lower cost and yields
high-quality data at relatively low radiation doses [18], it cannot
be used as an auxiliary diagnostic protocol for all cases. A few
studies have been conducted on the assessment of the
CVM method based on CBCT [19,20]. Shim et al. [21] reported
weak inter-observer agreement (0.581 Interclass correlation
coefficient) in the evaluation of CVM method between CBCT
and LC. These authors recommended new maturational indica-
tors or landmarks unique to CBCT imaging. Furthermore, more
recently Joshi et al. [22] compared the CVM method between
CBCT and LC and observed a significantly high correlation for the Figure 1
skeletal maturity estimation (0.975 Spearman correlation). Study flow chart to select the CBCT and lateral radiographs
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 G. Echevarría-Sánchez, L.E. Arriola-Guillén, V. Malpartida-Carrillo, P.L. Tinedo-López, R. Palti-Menendez, M.E. Guerrero
Original article

surgeons who required the CBCT to complete their diagnosis. The TABLE I
radiographs and tomographs were obtained at IDM Maxillofacial Definitions of cervical stages using the cervical vertebrae method
Diagnostic Institute, Lima, Peru, from January 2013 to December according to Baccetti et al. [12].
2018. The sample size was determined by a pilot test of 15 sub-
jects using the formula to estimate a proportion with a total Stage Characteristics
population of 50 subjects, a 95% confidence level, a proportion CS1 The lower borders of all the three vertebrae (C2-C4) are flat.
of 84%, and a precision of 5%. According with this analysis, the The bodies of both C3 and C4 are trapezoid in shape (the
number of subjects required was 40 (18 men, 22 women). superior border of the vertebral body is tapered from
Informed consent was obtained from all individuals, their posterior to anterior)

parents or legal tutors. The inclusion criteria were healthy CS2 A concavity is present at the lower border of C2 (in four of
Peruvian individuals between 10 and 19 years old without five cases, with the remaining subjects still showing CS 1).
developmental anomalies, syndromes, and cleft lip and palate. The bodies of both C3 and C4 are still trapezoid in shape

The exclusion criteria were the presence of pathological CS3 Concavities at the lower borders of both C2 and C3 are
changes, problems in growth and development, foreign bodies present. The bodies of C3 and C4 may be either trapezoid or
in the images, and CBCT sagittal slices and LC images with rectangular and horizontal in shape

impairment of full visualization of the vertebrae bodies of C2, CS4 Concavities at the lower borders of C2, C3, and C4 now are
C3, and C4 and CBCTs or LC of individuals with orthodontic or present. The bodies of both C3 and C4 are rectangular
horizontal in shape
surgical treatment (figure 1).
CS5 The concavities at the lower borders of C2, C3, and C4 are
Methods still present. At least one of the bodies of C3 and C4 is
squared in shape. If not squared, the body of the other
Image acquisition cervical vertebra still is rectangular horizontal
LC images were obtained using a Planmeca Proline XC (Roselle,
CS6 The concavities at the lower borders of C2, C3, and C4 are
Illinois, USA) with exposure settings of 68 kV, 12 mA, and 0.6–0.8 s
still evident. At least one of the bodies of C3 and C4 is
exposure time. Good quality cephalograms with a ruler on the rectangular and vertical in shape. If not rectangular and
cephalostat for exact measurement of the magnification factor vertical, the body of the other cervical vertebra is squared
were required. They showed C2–C4 vertebrae bodies in full view
taken on the same date as the CBCT sagittal slices. The LC
were scanned at 600 dpi for presentation as high-resolution
images in TIFF format to maintain the original radiographic quality.
Radiographs were scanned (Epson Perfection V700, Japan) and
digitally examined prior to scoring. The brightness and contrast of
images were edited to improve clarity.
Additionally, all CBCT images were acquired using a Pointnix
Point 3D Combi 500 C (Imaging Sciences, Hatfield, Philadelphia,
PA) examined on sagittal slices. The imaging parameters
were set at 120 kV, 8 mA, scan time of 26.9 seconds, resolution
of 0.4 mm, isotropic voxel with resolution of 0.160 mm, and
10  9 cm to 19  16 cm field of view. Subjects were placed in a
stated position in maximum intercuspation. The head position
was maintained by devices such that the midsagittal plane was
Figure 2
perpendicular to the floor and the Frankfort plane was parallel to
Cervical stages using the cervical vertebrae method according to
the floor. After, the DICOM files of each CBCT slice were exported
Baccetti et al. [12]
and transferred to a desktop computer equipped with the
RealScan 2.0 viewer software.

Assessment of individual skeletal maturity (RPM) using 20 CBCTs slices and 20 cephalograms of subjects of
The maturation stages of the cervical vertebrae were deter- both genders aged 10–19 years randomly selected. The observer
mined according to the method described by Baccetti et al. [12] was trained in the CVM method as follow:
based on the morphology of C2, C3, and C4 cervical vertebrae.  he was showed the CVM method using exact figures and

The developmental stages are described in table I and figure 2. legends described by Baccetti et al. [12];
To discard any evaluating error, the training and calibration were  he received a hard-copy handout with a written description of

performed by a specialist in Oral and Maxillofacial Radiology the radiographic features of each cervical stage;
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Reliability of cephalograms derived of cone beam computed tomography versus lateral cephalograms to
estimate cervical vertebrae maturity in a Peruvian population: A retrospective study
 he received a detailed explanation of the morphologic
features of each cervical stage in a PowerPoint (Microsoft,
Redmond, WA, USA) high-resolution image presentation
containing 15 CBCT sagittal slices and 15 LC images.
The calibration with the specialist was done two times with a
washout period of four weeks. Data recorded were submitted
for analysis of agreement to check the calibration and the kappa
coefficients were  0.90 indicating optimal agreement
accepted to proceed with the research.
The observer did not have prior knowledge of the identification
of individuals (age and gender) on LC images and CBCT slices.
Later, the lateral radiographs were randomly mixed and
observed in a dimly lit room with constant light intensity.
Furthermore, to obtain the cephalograms derived of the CBCT,
the sagittal plane was adjusted to pass through both anterior
and posterior nasal spines and in the axial plane regarding to the
mid palatine suture [22]. These images were exhibited on the
screen of a Samsung Intel Core i7 and observed in a dimly lit
room with constant light intensity too. Four weeks after the first
observation, the examiner was retrained in the CVM method
receiving the images in a different random order, and he was
asked to re-observe the slices and images to rule out any
evaluating error.
Statistical analyses
Statistical analysis was performed using the STATA version 16
(Stata Corp., College Station, TX, USA) software for windows.
Intra-observer reliability of each maturation stage on CBCT
sagittal slices and LC images was analysed by the weighted
kappa statistics (a = 0.05). For the interpretation of weighted
kappa in intra-observer agreement studies, the guidelines
developed in Landis and Koch [23] for strength of agreement
were used, with the following kappa values: 0, poor; 0.01–0.20,
slight; 0.21–0.40, fair; 0.41–0.60, moderate; 0.61–0.80,
TABLE II
Intra-observer agreement for the cervical vertebrae maturation stages using CBCT sagittal slices.
CBCT slices CS1 CS2
First assessment CS1 2 1
CS2 1 9
CS3 1 11
CS4
CS5
CS6
Total 3 11
The kappa coefficient: 0.873 (p < 0.001). CBCT: Cone Beam Computed Tomography.
tome 18 > n82 > June 2020
Original article
substantial, and 0.81–1, almost perfect. The correlation between
the CBCT sagittal slices and LC images in two times was
evaluated by the Spearman rank correlation coefficient test.
Statistical significance was set at p ˂ 0.05 for all tests. As a
complement, a Bland-Altman plot was used for comparing the
first and second intra-observer agreement for the CVM stages
between the CBCT sagittal slices and LCR images.
Results
Intra-observer reliability
The weighted kappa test showed almost perfect intra-observer
agreement for the CVM stages using the CBCT sagittal slices
(0.873; p < 0.001), and this result is showed in table II. Consid-
ering the LC images, the weighted kappa test showed almost
perfect intra-observer agreement too (0.937; p < 0.001), and
these results are shown in table III. In both intra-observer
agreement, the difference was limited to one maturation stage
of the CVM method, as it is observed in the central diagonal line
in tables II, III.
The first and second intra-observer agreement for the CVM
stages between the CBCT sagittal slices and LC images were
almost perfect (0.937 and 0.874; p < 0.001). Disagree in the first
intra-observer agreement was observed in only two subjects,
and disagree in the second intra-observer agreement was
observed in four subjects. The difference between both
agreements was limited to one maturation stage of the CVM
method. The greatest disagreements were observed between
stage 1 and 2. Figure 3 shows the Bland-Altman plots where the
differences (vertical axis) were distributed consistently along
the averages (horizontal axis) when the concordance of the first
and second intra-examiner agreement between CBCT sagittal
slices and LCR images were evaluated.
Second assessment
CS3 CS4 CS5 CS6 Total
3
10
1 13
6 6
5 5
3 3
11 7 5 3 40
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 G. Echevarría-Sánchez, L.E. Arriola-Guillén, V. Malpartida-Carrillo, P.L. Tinedo-López, R. Palti-Menendez, M.E. Guerrero
Original article

TABLE III
Intra-observer agreement for the cervical vertebrae maturation stages using LC images.

Second assessment
LC images CS1 CS2 CS3 CS4 CS5 CS6 Total

First assessment CS1 3 1 4

CS2 1 8 9

CS3 12 12

CS4 7 7

CS5 5 5

CS6 3 3

Total 4 9 12 7 5 3 40

Kappa coefficient: 0.937 (p < 0.001). LC: lateral cephalograms.

Figure 3
The Bland-Altman graphs shows the concordance in the first (left) and in the second (right) intra-observer agreement for the CVM
stages between CBCT sagittal slices and LC images

Figure 4
Three-dimensional reconstruction of CS3 Cervical vertebrae maturation stage on CBCT sagittal slice (left), cephalogram derived of CBCT
(middle) and lateral cephalometric (right) of the most representative stage
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Reliability of cephalograms derived of cone beam computed tomography versus lateral cephalograms to
estimate cervical vertebrae maturity in a Peruvian population: A retrospective study
Comparison of CVM stages between CBCT slices and
LC images
The correlation between the two methods for evaluating CVM
method at the first and second time was high (0.988 and 0.976;
p < 0.001). The correlation was strongly positive despite the
disagreement on stages 1 and 2. Finally, as a complement,
stage 3 was the more representative stage in the evaluated
patients (30%). The images of stage 3 in CBCT and LC
radiographs are showed in figure 4.
Discussion
One of the mayor concerns in skeletal evaluation is whether the
adolescent pubertal growth spurt has arrived. This element is
important as it will provide valuable information for better
diagnosis and optimization of the treatment results and
duration. CVM method has been proposed as a diagnostic tool
for assessing skeletal maturation and it has demonstrated
clinical applicability [11–14,24]. The objective of this study
was to test the reliability of CBCT sagittal slices for CVM method
assessment and to compare the CVM method estimation
between CBCT sagittal slices and LC images.
The CVM method is based on the change of C2–C4 vertebrae
body shape, mainly on the inferior concavity depth and the
height-width ratio. Zhao et al. [25] stated that some factors can
affect the accuracy and reproducibility of the CVM method: First,
the observations are purely subjective, the difference between
horizontally rectangular, square, and vertically rectangular ver-
tebrae shapes depend on the researcher's arbitrary decision.
Second, the cervical vertebrae shapes show marked variation
from subject to subject, sometimes the shape and inferior
borders of C2–C4 cannot fulfil the definition of a cervical stage
at the same time. In addition, when using cephalograms, mat-
urational changes may be subject to distortion if the sagittal
plane of the cervical vertebrae is not precisely perpendicular to
the x-ray beam. Also, certain lateral cephalograms could have a
greater level of radiographic "noise'', making staging difficult
because of decreased image clarity [17]. All these criticisms and
questions on the CVM method may promote further research.
With this in mind, it is logical to understand why alternative
methods have been proposed to evaluate skeletal maturation
such as: insulin-like growth factor I (IGF-I) [6], hyoid bone
morphology [26], middle phalanx of the third finger [27],
midpalatal suture maturation [28], spheno-occipital synchond-
rosis [29], and frontal sinus morphology [30].
According with Hassel and Farman [31], skeletal maturation is a
continuous process and each maturation stage blends into the
next which makes it difficult to differentiate between borderline
subjects. Actually, CBCT is becoming a valuable tool in dental
practice showing tridimensional images with high quality at
relatively low radiation doses. However, the difficulty in making
a detailed comparison of different units is recognized in
published studies [32]. CBCT radiation doses range widely, some
tome 18 > n82 > June 2020
Original article
of them are capable of delivering low doses and this technology
continues to evolve quickly turning it into a technique that could
become very promising in the near future instead of using
cephalograms. Although it cannot be used as an auxiliary
diagnostic protocol for all cases.
In this study, the reliability of the CVM method was tested by
intraobserver agreement. The kappa scores indicated almost a
perfect intraobserver agreement of 0.937 for the CVM stages
using LC images and a similar result was found in the study of
Perinetti et al. [33] who reported 0.88 for intraobserver agree-
ment when 10 operators performed the evaluations. Also, other
authors reported substantial agreement of 0.67 [25], 0.70 [14],
and 0.74 [34] respectively. However, Gabriel et al. [16] reported
poor reproducibility of the CVM method for skeletal maturity
assessment although 0.60 and 0.65 kappa values were obtained
at the first and second evaluation done by 10 orthodontists. They
also stated that the orthodontists agreed with their previous
staging only 62% of the observations. Subsequently, this
percentage was confirmed by Nestman et al. [17]. This
difference could have occurred because those specialists were
trained on the CVM method using only exact figures and legends
of the article of Baccetti et al. [12] presented as simplified
versions of the full range of possibilities [33]. In this study,
the observer received more intensive training and practice
not only with figures and legends but also using a hard-copy
handout, written description and detailed explanation of the
radiographic features of each cervical stage using a PowerPoint
presentation. This reinforces the concept that regular training is
necessary to obtain high diagnostic accuracy and intraobserver
repeatability in the visual assessment of the CVM method
[14,25,33].
These results are according with Tekin and Aydin [35] who recently
used CBCT for determination of skeletal maturity using CVM
method. These authors reported an intra-observer agreement
of 0.756 when one investigator evaluated the images. These
results suggest that CBCT may be a highly reliable method for
CVM assessment. On the other hand, Shim et al. [21] evaluated
the application of CBCT for CVM method and reported an interclass
correlation coefficient (ICC) of 0.58 when two examiners
evaluated the slices. Another method to determine the skeletal
maturation status in CBCT is using a regression formula to obtain
CVM age. This method uses ratios of C2–C4 vertebral bodies, lower
concavity angles and measurements of the C2 vertebral body and
the odontoid process, and suggest that quantitative analysis might
be used as an alternative tool [36]. Recently, Bonfim et al. [37]
used CBCT to compared the CVM index between tridimensional
reconstructions and tridimensional sagittal sections and they
obtained 0.99 kappa score, showing almost perfect intra-observer
agreement as the one obtained in this study. The difference
between the first and second intra-observer agreement for
the CVM stages between the CBCT sagittal slices and LC images
were almost perfect (0.937 and 0.874) and was limited to one
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 G. Echevarría-Sánchez, L.E. Arriola-Guillén, V. Malpartida-Carrillo, P.L. Tinedo-López, R. Palti-Menendez, M.E. Guerrero
Original article

maturation stage of the CVM method. These results indicate that
CBCT sagittal slices and LC images can be validly used. Therefore, if
CBCT is selected in a specific case, additional LC could be avoided
for the assessment of skeletal maturity preventing increased
radiation doses in patients.
Almost perfect agreement was found at the first and second
intra-observer agreement for the CVM stages between CBCT
sagittal slices and LC images. This was confirmed with the high
correlation values at the first and second evaluation (0.988 and
0.976) and these results are according with Joshi et al. [22].
Previous evidence showed that intra-observer repeatability was
much lower in assessing the shape of C3–C4 and C4–C5 bodies
[17,33]. In our study disagreements were registered in assess-
ing C1–C2 and C3–C4 stages. These results are in concordance
with Gabriel et al. [16] who reported the major disagreement in
C1–C2 stages. Likewise, Sohrabi et al. [38] stated that difficulty
in determining the morphology of C3 and C4 leads to poor
reproducibility of the CVM method.
One limitation of this study was the number of subjects required
since the limited source of both CBCT slices and LC images
registration was the same day requested by their orthodontists
or surgeons for specific procedures. However, a sample size
was obtained using a formula to estimate a proportion and
40 individuals were calculated. Also, in order to avoid observa-
tion bias, the observer received more intensive training,
retraining and practice in the CVM method assessment.
Although the results of this study are promising, additional
longitudinal research comparisons of the CVM method based
on CBCT slices with larger sample sizes are needed to address
the exact relationship between CVM stages and skeletal
maturity.
Conclusions
The cephalograms derived from CBCT for assessment of the CVM
method has reliability and may replace the use of lateral radiographs
for CVM method estimation. The orthodontists might use the CBCT
scans as a diagnostic tool for CVM method estimation.
Disclosure of interest: the authors declare that they have no competing
interest.

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