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Skeletal maturation evaluation using

cervical vertebrae
Brent Hassel, BA, DDS, MS," and Allan G. Farman, BDS, PhD(odont), Dip ABOMR, EdS, MBA b
Montere)4, Calif., and Louisville, Ky.
Lateral cephalometric and left hand-wrist radiographs from the Bolton-Brush Growth Center at Case
Western Reserve University were reviewed a posteriori to develop a cervical vertebrae maturation
index (CVMI). By using the lateral profiles of the second, third and fourth cervical vertebrae, it was
possible to develop a reliable ranking of patients according to the potential for future adolescent
growth potential. (AM J ORTHOD DENTOFAC ORTHOP 1995;107:58-66.)
Se xua l maturation characteristics, chron-
ologic age, dental development, height, weight, and
skeletal development are some of the more com-
mon means that have been used to identify stages
of growth. Determination of maturation and sub-
sequent evaluation of growth potential during pre-
adolescence or adolescence is extremely important.
With many orthodontic patients, pubertal growth
needs to be factored into the diagnostic equation.
One important diagnostic tool currently used in
determining whether the pubertal growth has
started, is occurring, or has finished is the hand-
wrist radiographic evaluation. Biologic age, skeletal
age, bone age, and skeletal maturation are nearly
synonymous terms used to describe the stages of
maturation of a person. Because of individual
variations on timing, duration and velocity of
growth, skeletal age assessment is essential in for-
mulating viable orthodontic treatment plans.
The primary objective of this study was to
create a method of evaluating the skeletal matura-
tion of the orthodontic patient with the cephalo-
metric radiograph that is routinely taken with
pretreatment records. Correlations were made be-
tween cervical vertebrae maturation and the skel-
etal maturation of the hand-wrist.
BACKGROUND
Skeletal maturation refers to the degree of
development of ossification in bone. Size and matu-
ration can vary independently of each other. Skel-
etal maturation is more closely related to sexual
maturity than to stature? -5
The views expressed herein by the authors are not necessarily those of the
Department of Defense or the U.S. Government.
aLieutenant Colonel, U.S. Army Dental Corp, Monterey, Calif.
bProfessor of Radiology & Imaging Sciences, University of Louisville
School of Dentistry.
8/1/47789
During growth, every bone goes through a se-
ries of changes that can be seen radiologically. The
sequence of changes is relatively consistent for a
given bone in every person. The timing of the
changes varies because each person has his or her
own biologic clock. There are some exceptions, but
generally speaking, the events are reproducible
enough to provide a basis for comparison between
different persons. 6-9
Many authors have shown that significant cor-
relation exists between facial and statural growth.
Statural growth acceleration generally precedes fa-
cial growth acceleration by 6 to 12 months. 1°2°
Hand-wrist radiographic evaluation
After Roentgen demonstrated his new radio-
graphic discovery in 1895, Roland, in 1896, intro-
duced the idea of using the comparative size and
shape of the radiographic shadows of growing
bones as indicators of rate of growth and ma-
turity. 21
In the early 1900s, Pryor, = Rotch, 23 and Cramp-
ton 24 began tabulating indicators of maturity on
sequential radiographs of the growing hand and
wrist. Hellman published his observations on the
ossification of epiphysial cartilages of the hand in
1928. 25
Todd 26 compiled hand-wrist data that was fur-
ther elaborated on by Greulich and Pyle in atlas
form 6 Flory. in 1936, indicated that the beginning
of calcification of the carpal sesamoid (adductor
sesamoid) was a good guide to determining the
period immediately before puberty. 27 The appear-
ance of the adductor sesamoid has been highly
correlated to peak height velocity and the start of
the adolescent growth s pur t . 11-13'28-34 Most authors
agree that peak height velocity follows adductor
sesamoid appearance by ~pproximately 1 year.
Fishman developed a system of hand-wrist skel-
58
American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Far man 59
Volume 107, No. t
etal mat ur at i on indicators (SMIs) using four stages
of bone mat ur at i on at six anat omi c sites on the
hand and the wrist. 35-a7
Hagg and Tar anger creat ed a met hod using the
hand-wrist radi ograph to correl at e certain mat uri t y
indicators to the pubert al growth spurt. 38-4°
Cervical vertebrae
Maturation. The first seven vert ebrae in the
spinal col umn constitute the cervical spine. The
first two, the atlas and the axis, are quite unique,
the third t hrough the seventh have great similar-
ity. 41 Mat urat i onal changes can be observed from
birth to full maturity. 42-45
Vert ebral growth t akes place from the cartilag-
enous layer on the superi or and inferior surfaces of
each vert ebrae. 46-52 Secondary ossification nuclei on
the tips of the bifid spinous processes and trans-
verse processes appear during puberty. 47'48"52'53 Sec-
ondary ossification nuclei unite with the spinous
processes when vert ebral growth is com-
plete.41,47.48. 53
Measurement. Aft er compl et i on of endochon-
dral ossification, growth of the vert ebral body takes
place by peri ost eal apposition. It appears to take
place only at the front and si des. 51"54 Todd and
Pyle, 55 Lanier, 56 and Ta yl or 57 made measur ement s
from lateral radi ographs of the lower cervical ver-
t ebrae. Lamparski studied changes in size and
shape of cervical ver t ebr ae to creat e mat urat i onal
st andards for the cervical vert ebrae, s8 His met hod
was t aken from Todd and Pyle, 55 El sberg and
Dyke, 59 Lanier, 56 Bick and Copel, 45 and Hinck. 6°
Normal variations in the cervical spine. Cattel
and Filtzer studied 160 children and found the
following variations of normal: (1) variations due to
di spl acement of ver t ebr ae that may resembl e sub-
luxation; (2) variations of curvat ure t hat may re-
sembl e spasm and l i gament ous injury; and (3)
variations rel at ed to skeletal growth centers resem-
bling fractures. 61
Ogden f ound variations of the ant eri or cont our
of the dens were fairly common. ~2 Bailey report ed
the frequent appear ance of forward di spl acement
of the second and third cervical ver t ebr ae resem-
bling subluxations in children under 8 years. 63 Far-
man et al . 64-66 found that the lateral cephal omet ri c
radi ographi c profile of the atlas could be useful in
forensic identification.
Disorders in children and adolescents. The or-
t hodont i st does not have to be an expert in cervical
vert ebrae abnormalities, but he must be aware of
normal anat omy of the cervical spine on the lateral
cephal ogram. Many abnormal i t i es of the cervical
spine do not mani fest t hemsel ves symptomatically
until adol escence or young adulthood, and the
ort hodont i st has the opport uni t y to det ect some of
t hese abnormalities. If the progressively degenera-
tive defects can be discerned early, severity of
consequences can be diminished.
Some anomal i es seen in the cervical spines of
children and adolescents are fractures, infections,
polyarthritis, ankylosis, and ankylosing spondyli-
tis. 46'67 Post eri or arch defects, odont oi d anomalies,
and congenital defects of the cervical spine can be
fairly common. 52
METHODS AND MATERIALS
Sample
The sample of 11 groups of 10 males and 10 females
(220 subjects) aged from 8 to 18 years was taken from the
Bolton-Brush Growth Center at Case Western Reserve
University. The subjects were white and primarily of
Northern European descent. 68 The radiographs used in-
cluded the left hand-wrist and the lateral cephalogram.
Records were selected randomly, the only segregation of
subjects was on the basis of gender.
Methods
The system developed by Fishman was used to de-
termine skeletal maturation by hand-wrist evaluation on
each subject? 6 Once skeletal maturation was assessed
from the hand-wrist radiograph, the lateral cephalogram
taken on the same date was taken from the record. Three
parts of the cervical vertebrae were traced on 0.003-inch
matte acetate with a 0.5 mm diameter mechanical lead
pencil. These entities were the dens (odontoid process),
the body of the third cervical vertebra (C3), and the body
of the fourth cervical vertebra (C4). These areas were
selected because C3 and C4 could be visualized even
when a thyroid protective collar was worn during radia-
tion exposure.
Radiographs of high clarity and good contrast were
used. Any radiographs that showed motion unsharpness
or had poor contrast were discarded from the evaluation.
Radiographic techniques were standardized as much as
possible in the Bolton Study. Object to radiation source
was fixed at 5 feet by the Broadbent cephalometer. Since
relative measurements, not absolute measurements were
used in the present study, magnification was of minimal
concern.
Ten male and 10 female subjects were placed in each
SMI group numbered 1 through 11. The cervical verte-
brae tracings were paired with their respective hand-
wrist radiographs that had been grouped by SMI catego-
ries. These tracings were photocopied. The photocopies
of the vertebral tracings were evaluated to see whether
changes in shape and dimension of the vertebrae could
60 Hassel and Farman American Journal of Orthodontics and Dentofacial Orthopedics
January 1995
1 2 3
INITIATION ACCELERATION TRANSITION
,,,,, , , , ,
DECELERATION MATURATION COMPLETION
4 5 6
Fig. 1. Cervical vertebrae maturation indicators using C3 as guide. (See Table I.)
be observed between SMI groupings. Specific entities
looked at were the presence or absence of curvature in
the inferior borders of the dens, C3, and C4. General
shapes of the bodies of C3 and C4 were evaluated.
Intervertebral spacing was visualized.
Eleven female and 9 male hand-wrist radiographs
were read by two independent evaluators (designated
evaluators A and B) and B.H. to evaluate interoperator
error in determining SMI categories. Intraoperator error
was determined by B.H. evaluating the same records
3 weeks later. The same patient records were used in
determining the cervical vertebrae maturation indices
(CVMIs). Lateral cephalometric radiographs were evalu-
ated by the same two independent evaluators and B.H. to
determine interoperator and intraoperator error. Cervi-
cal vertebrae C2, C3, and C4 were observed and each
patient was placed in a CVMI category by using the
criteria detailed in the results and the discussion section
of this article. The CVMI readings were then evaluated
against the previously determined SMI readings to see
what correlations existed. Intraoperator error was evalu-
ated by B.H. who evaluated the same radiographs
3 weeks later.
RESULTS
Photocopies of the cervical vert ebrae tracings
i nt roduced in the met hods section of this article
were sequentially segregated by SMI grouping. Six
categories of cervical vert ebrae skeletal mat urat i on
could be defined, .and the following observations
were made for each category. Refer to Fig. 1 for a
graphic synopsis of these findings. Figs. 2 through 7
are photographs of representative hand-wrist ra-
diographs and lateral cephal omet ri c radiographs
for each CVMI category.
Category 1 was called INITIATION. This cor-
responded to a combination of SMI 1 and 2. At this
stage, adolescent growth was just beginning and
80% to 100% of adolescent growth was expected. 36
Inferior borders of C2, C3, and C4 were flat at this
stage. The vert ebrae were wedge shaped, and the
superior vertebral borders were t apered from pos-
terior to ant eri or (Fig. 2).
Category 2 was called ACCELERATION. This
corresponded to a combination of SMI 3 and 4.
Growt h acceleration was beginning at this stage,
with 65% to 85% of adolescent growth expected. 36
Concavities were developing in the inferior borders
of C2 and C3. The inferior border of C4 was flat.
The bodies of C3 and C4 were nearly rectangular in
shape (Fig. 3).
Category 3 was called TRANSITION. This cor-
responded to a combination of SMI 5 and 6.
Adol escent growth was still accelerating at this
stage toward peak height velocity, with 25% to 65%
of adolescent growth expected26 Distinct concavi-
ties were seen in the inferior borders of C2 and C3.
A concavity was beginning to develop in the infe-
rior border of C4. The bodies of C3 and C4 were
rectangular in shape (Fig. 4).
Category 4 was called DECELERATION. This
corresponded to a combination of SMI 7 and 8.
Adolescent growth began to decel erat e dramati-
cally at this stage, with 10% to 25% of adolescent
growth expected26 Distinct concavities were seen in
American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Far man 61
Volume 107, No. 1
Fig. 2. CVMI 1: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
Fig. 3. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
the inferior borders of C2, C3, and C4. The verte-
bral bodies of C3 and C4 were becoming more
square in shape (Fig. 5).
Category 5 was called MATURATION. This
corresponded to a combination of SMI 9 and 10.
Final mat urat i on of the vert ebrae t ook place during
this stage, with 5% to 10% of adolescent growth
expected. 36 More accent uat ed concavities were
seen in the inferior borders of C2, C3, and C4. The
bodies of C3 and C4 were nearly square to square
in shape (Fig. 6).
Category 6 was called COMPLETION. This
corresponded to SMI 11. Growt h was considered to
be complete at this stage. Little or no adolescent
growth was expected. 36 Deep concavities were seen
in the inferior borders of C2, C3, and C4. The
bodies of C3 and C4 were square or were great er in
vertical dimension than in horizontal di mensi on
(Fig. 7).
Interoperator error
Eval uat or A agreed with the SMI determina-
tions of B.H. in 18 of the 20 cases. Both discrep-
ancies were within one SMI category of that found
by the aut hor (r 2 = 0.99, p < 0.001).
Eval uat or B agreed 16 out of 20 times. All four
62 Hassel and Far man American Journal of Orthodontics and Dentofacial Orthopedics
January 1995
Table I. Cervical vert ebrae mat urat i on indicators
1. Initiation
• Very significant amount of adol escent growt h expected
• C2, C3, and C4 inferior vert ebral body borders are flat
• Superior vert ebral borders are t apered post eri or to anterior
2. Acceleration
• Significant amount of adol escent growth expected
• Concavities developing in lower borders of C2 and C3
• Lower border of C4 vert ebral body is flat
• C3 and C4 are mor e rect angul ar in shape
3. Transition
• Moder at e amount of adol escent growt h expected
• Distinct concavities in lower borders of C2 and C3
• C4 developing concavity in lower border of body
• C3 and C4 are rect angul ar in shape
4. Deceleration
• Small amount of adol escent growth expected
• Distinct concavities in lower borders of C2, C3, and C4
• C3 and CA are nearly square in shape
5. Maturation
• Insignificant amount of adol escent growt h expected
• Accent uat ed concavities of inferior vert ebral body borders of C2, C3, and C4
• C3 and C4 are square in shape
6. Completion
• Adol escent growt h is compl et ed
• Deep concavities are pr esent for inferior vert ebral body borders of C2, C3, and C4
• C3 and C4 hei ght s are great er t han wi dt hs
differences in opinion were within one SMI cat-
egory. Borderl i ne cases were i nt erpret ed one cat-
egory higher by evaluator B t han by B.H.
(r 2 = 0.99, p < 0.001).
The same 20 cephal omet ri c radiographs evalu-
ated by B.H. to det ermi ne CVMI categories were
evaluated by the same two i ndependent evaluators.
Evaluators A and B were each given 10 minutes
instruction by B.H. on CVMI det ermi nat i on crite-
ria. Fig. 1 was given to each evaluator for guidance•
Significant agreement was seen bet ween evaluators
A and B (r 2 = 0.85, p < 0.001; /,2 = 0.90,
p > 0.001).
When SMI categories and CVMI categories
det ermi ned for each subject were compared with
the criteria specified in the, Discussion section of
this article, high correlation was seen (r 2 = 0.89,
p < 0.001).
Intraoperator error
The SMI categories for 11 males and 9 females
were det ermi ned from 20 hand-wrist radiographs•
These same radiographs were reevaluated 3 weeks
later by the same person and the SMI categories
were again assigned• Ni net een of 20 SMI determi-
nations were the same in the second evaluation as
they were in the first (r 2 = 1.00, p < 0•001)•
Lateral cephal omet ri c radiographs from the
same 20 patients as the hand-wrist films were
evaluated• The same radiographs were reevaluated
3 weeks later by the same person• Ni net een of 20
CVMI category determinations coincided with
those det ermi ned 3 weeks previously (r 2 = 1.00,
p < 0.001).
DI SCUSSI ON
The purpose of this investigation was to provide
the orthodontist with an additional tool to help
det ermi ne growth potential in the adolescent pa-
tient. This was to be accomplished by using ana-
tomic changes of the cervical vert ebrae observed on
the lateral cephal omet ri c radiograph to det ermi ne
skeletal maturity. By using a routinely t aken diag-
nostic radiograph, the orthodontist would have a
reliable diagnostic tool to aid in formulating treat-
ment options.
This study combined the observations of the
changes in the hand-wrist and the changes in the
cervical vert ebrae during skeletal maturation• The
observations of Lamparski s8'67 were confirmed, ex-
cepting the lack of a narrowing of intervertebral
space with increased age. The shapes of the cervi-
cal vert ebrae were seen to differ at each level of
skeletal development. This provided a means with
American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Farman 63
Volume 107, No. 1
Fig, 4. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
Fig. 5. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
which to determine the skeletal maturity of a per-
son and thereby determine whether the possibility
of potential growth existed.
The shapes of the vertebral bodies of C3 and C4
changed from somewhat wedge shaped, to rectan-
gular, to square, to greater in dimension vertically
than horizontally as skeletal maturity progressed.
The inferior vertebral borders were flat when most
immature, and they were concave when mature.
The curvatures of the inferior vertebral borders
were seen to appear sequentially from C2 to C3 to
C4 as the skeleton matured. The concavities be-
came more distinct as the person matured.
When two successive SMI-CVMI groups were
combined, it was observed that distinct cervical
vertebrae anatomic characteristics were unique to
each of these groupings. Eleven SMI (skeletal mat-
uration index) groupings were condensed into six
CVMI (cervical vertebrae maturation index) cate-
gories. The SMI groupings 1 and 2, 3 and 4, 5 and
6, 7 and 8, 9 and 10, and SMI 11 were given CVMI
categories 1 through 6, respectively (Figs. 1-7).
64 Hassel and Farman American Journal of Orthodontics and Dentofacial Orthopedics
January 1995
Fig. 6. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
Fig. 7. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using
lateral cephalograph.
The evaluation of intraoperator error in SMI
determination suggested that B.H. varied insignifi-
cantly in his interpretation from one time to the
next. The criteria used for SMI determination ap-
peared to be valid. Intraoperator error in CVMI
determination was also insignificant.
There was slight variation in SMI determination
from one evaluator to the next. Evaluation of
subjective criteria carried with it some inherent
variability. In this study, SMI determination by
three evaluators showed little discrepancy from
person to person.
Evaluators A and B correlated with B.H. sig-
nificantly in choosing CVMI classification. The in-
stances of disagreement fell within one CVMI
category of B.H.' s interpretation. Clinically, the
differences would be negligible. Statistically, the
CVMI criteria used was consistently applied by two
evaluators. Additional training and clarification of
evaluation criteria would eliminate much of the
American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Far man 65
Volume I07, No. 1
variability seen in interpretation of borderline
c as e s .
It must be remembered that skeletal maturation
is a conti nuous process. Skeletal maturity indica-
tors in the hand-wrist and the cervical vertebrae are
categorized by distinct events in this continuum.
Each stage of maturation blends into the next, and
it is sometimes difficult to differentiate borderline
cases. Clinically, these differences should not be of
great importance. Radiologic skeletal maturation
indicators should be used to augment other obser-
vations by the orthodontist. One diagnostic test
should not be relied on too heavily.
The growth factor is a critical variable in orth-
odonti c treatment. A treatment plan can vary from
orthognathic surgery to extraction of teeth to non-
extraction of teeth, dependi ng on the growth factor.
By looking briefly at the cervical vertebrae on a
lateral cephalometric radiograph the orthodontist
can now evaluate skeletal maturity of the patient at
that one point in time. He or she can then have a
reasonable idea how much growth should be fac-
tored into anticipated treatment.
A special word of thanks is due to Dr. John Yancey
for guidance on the statistical analyses employed for this
study.
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Reprint requests to:
Dr. Allan G. Farman
School of Dentistry
University of Louisville
Louisville, KY 40292