Escolar Documentos
Profissional Documentos
Cultura Documentos
The PDF of the article you requested follows this cover page.
Commentary and Perspective, data tables, additional images, video clips and/or
translated abstracts are available for this article. This information can be accessed
at http://www.ejbjs.org/cgi/content/full/83/8/1212/DC1
Subject Collections
Click here to order reprints or request permission to use material from this
article, or locate the article citation on jbjs.org and click on the [Reprints and
Permissions] link.
Publisher Information
COPYRIGHT 2001
BY
THE JOURNAL
OF
BONE
AND JOINT
SURGERY, INCORPORATED
Background: The radiographic anatomy of the cervical spine in children is complex and can be difficult to interpret. The present study was undertaken to document radiographically the growth and development of the cervical
spine in a prospective, longitudinal manner and to establish standard radiographic measurements on the basis of
findings in patients who were followed serially from the age of three months until skeletal maturity.
Methods: The radiographic resources of the Cleveland Study of Normal Growth and Development (Bolton-Brush
Collection, Cleveland, Ohio) were reviewed. From this large database, we identified fifty boys and forty-six girls
who had a sufficient number of radiographs of the cervical spine for inclusion in our study. With use of a computerized image analyzer, the growth and development of the atlantodens interval, the diameter of the spinal canal,
the Torg ratio, the height and width of the second through fifth cervical vertebral bodies, the height of the dens,
and the ossification of the first cervical vertebra were assessed on serial radiographs made from the age of three
months until skeletal maturity.
Results: Serial measurements of the atlantodens interval, the anteroposterior diameter of the cervical canal, the
height and anteroposterior width of the cervical vertebral bodies, and the height of the dens, made in normal,
healthy children from the age of three months to fifteen years, are presented in tabular and graphic forms. The
median Torg ratio was 1.47 for both males and females primarily, and it reached values of 1.06 for males and
1.10 for females by maturity. The anterior arch of the first cervical vertebra had ossified in 33% of the children by
the age of three months and in 81% of the children by the age of one year. Closure of the synchondroses was
completed in all children by the age of three years.
Conclusions: The measurements presented in the current study are important because they are the first, as far
as we know, to document the radiographic parameters of the cervical spine in children who were followed longitudinally from before the age of three years through the course of growth and development until skeletal maturity.
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
The present radiographic standards for children and adolescents have been established from studies of small groups
of patients1,10,12,13. We are not aware of any previous longitudinal study in which the growth and development of the cervical
spine has been followed from birth to maturity. The purpose
of our study was to document radiographically the growth
and development of the cervical spine in a highly controlled,
longitudinal manner and to establish standard radiographic
measurements for the pediatric cervical spine. We assessed the
atlantodens interval, the canal diameter, the Torg ratio, the
height and width of the second through fifth cervical vertebral
bodies, the height of the dens, and the ossification of the anterior arch of the first cervical vertebra in patients from the age
of three months until skeletal maturity16.
Materials and Methods
he radiographic resources of the Cleveland Study of Normal Growth and Development (Bolton-Brush Collection,
Cleveland, Ohio) were reviewed. The collection was compiled
from 1927 to 1942 and includes data only from healthy children with no evidence of congenital, neurological, or developmental disease who were evaluated at regular intervals from
the age of three months until skeletal maturity17,18. Approximately 3000 children participated in the overall study. The
Gruelich and Pyle atlases of skeletal maturation of the hand,
wrist, and knee were developed from this database19.
Approximately 200 children participated in the radiographic evaluation of the cervical spine. Each subject was to
have a plain lateral radiograph of the cranium and the cervical
spine made at the ages of three, six, nine, twelve, eighteen,
twenty-four, thirty, thirty-six, forty-two, forty-eight, fifty-four,
and sixty months and then annually until the age of seventeen
years. A standard tube-to-film distance was used with a filmto-focal spot distance of approximately 72 in (183 cm). The
head was immobilized in a rigid frame during the exposures.
Fifty boys and forty-six girls had a sufficient number of radiographs of the cervical spine for inclusion in the present study.
This group was considered to be eligible for our study on the
basis of the clarity of the radiographs and the availability of
studies that had been made until skeletal maturity. Radiographs were considered to be suboptimal if they were blurred
by motion or if any of the osseous structures were obscured by
the head-holder; suboptimal studies were not included in the
analysis. Additionally, not every child had each scheduled radiograph. However, radiographs were available for a total of
more than seventy-five subjects at each time-point before the
age of twelve years. More than one-half of the subjects had radiographs made until the age of fourteen years, and approximately one-third of the subjects had radiographs made until
the age of seventeen years.
The outline of the cervical spine on each radiograph was
traced onto a transparent sheet. Examples of some of the measured variables are shown in Figure 1. As the radiographs
frequently did not include the sixth and seventh cervical vertebrae, these levels were not included in the measurements.
Vertical lines were placed along the most anterior and poste-
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY
rior points of the vertebral bodies and along the most anterior point of the posterior arches, along the posterior portion
of the anterior aspect of the atlas, and along the anterior portion of the dens. Horizontal lines were placed along the most
superior and inferior portions of the vertebral bodies. Images
were entered into a computer with use of a SummaSketch
Plus digitizing pad (SummaGraphics, GTCO CalComp, Scottsdale, Arizona). The images were analyzed with use of a customdesigned software program written in Turbo Basic.
The atlantodens interval was measured as the distance
between the posterior aspect of the anterior arch of the first
cervical vertebra and the anterior aspect of the dens in the anteroposterior direction. The sagittal diameter of the canal at
the second cervical level was measured from the most anterior
aspect of the posterior arch of that vertebra to the posterior
aspect of the dens at the same level on a horizontal line in the
anteroposterior direction on the lateral radiograph. For the
third, fourth, and fifth cervical vertebrae, the sagittal diameter of the canal was measured from the most anterior portion
of the posterior arch to the center of the posterior aspect of the
corresponding vertebral body along the anteroposterior plane.
The Torg ratio was also calculated, in the fashion originally
described by Torg, by dividing the value for the sagittal diameter of the canal at the fifth cervical level by the anteroposterior
diameter of the vertebral body16. The width of the second,
third, fourth, and fifth cervical vertebral bodies was measured
at the midpoint of the posterior aspect of each vertebral body.
The vertical height was measured at both the anterior and
Fig. 1
Diagram of the method that was used to measure the variables that
were examined. The diagram on the left shows the tracing of the cephalad part of the cervical spine. The diagram on the right demonstrates
some, but not all, of the variables that were measured. A = width of the
dens, B = sagittal diameter of the canal at the first cervical level, C =
width of the second cervical vertebra, D = sagittal diameter of the
canal at the second cervical level, E = sagittal diameter of the third
cervical vertebral body, F = sagittal diameter of the canal at the third
cervical level, and G = height of the fourth cervical vertebra.
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
TABLE I
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY
Data on the Atlantodens Interval and the Canal Diameters According to Gender and Age*
Male
Variable
Female
0-60 mo
61-120 mo
2.02 (0.40)
2.16 (0.57)
2.19 (0.67)
2.16 (0.96)
1.91 (0.51)
1.83 (0.64)
15.63 (1.01)
17.89 (1.19)
18.22 (1.35)
14.73 (1.21)
17.02 (1.39)
17.42 (1.63)
13.92 (0.88)
13.51 (0.84)
15.55 (1.19)
15.06 (1.09)
15.76 (1.34)
15.37 (1.28)
13.30 (0.98)
13.00 (0.92)
14.93 (1.08)
14.64 (0.99)
15.44 (1.20)
14.93 (1.35)
13.79 (0.89)
14.98 (1.03)
15.22 (1.41)
13.41 (1.21)
14.79 (1.00)
14.82 (1.29)
121-180 mo
0-60 mo
61-120 mo
121-180 mo
*The values are given as the median, with the standard deviation in parentheses.
Results
he study began with forty-six female subjects and fifty
male subjects. Some radiographs could not be included in
the study for technical reasons, and some subjects were lost to
follow-up as the study progressed. The sample size for the
male and female subjects who had radiographs that could be
measured remained fairly constant until a gradual attrition of
subjects began at the age of ten years and continued until the
age of seventeen years. Forty-four (96%) of the original fortysix female subjects and forty-seven (94%) of the original fifty
male subjects had radiographs made until the age of ten years.
Only twenty-one female subjects and seventeen male subjects
were followed for more than fifteen years. There was equal
representation of both boys and girls at all time-points. The
results are presented in Tables I and II.
Data on the Width and Height of the Cervical Vertebrae According to Gender and Age*
Male
Variable
Female
0-60 mo
61-120 mo
121-180 mo
0-60 mo
61-120 mo
121-180 mo
10.41 (0.61)
12.88 (0.82)
14.52 (0.98)
9.79 (0.70)
12.49 (0.84)
14.30 (1.02)
10.36 (0.62)
10.37 (0.62)
12.93 (0.84)
12.76 (1.18)
14.53 (0.97)
14.10 (1.18)
9.74 (0.65)
9.68 (0.69)
12.26 (0.91)
12.11 (0.92)
13.86 (0.95)
13.38 (1.08)
10.57 (0.66)
12.57 (0.95)
13.94 (1.60)
10.05 (0.74)
12.03 (1.24)
13.64 (1.17)
Width (mm)
Height (mm)
Second cervical vertebra
18.79 (5.03)
27.54 (3.26)
33.65 (3.71)
18.92 (5.49)
27.48 (3.09)
34.28 (3.75)
5.52 (1.18)
7.82 (1.29)
11.51 (2.45)
5.84 (1.18)
8.09 (1.20)
11.56 (2.69)
5.41 (1.24)
7.77 (1.15)
10.98 (2.12)
5.70 (1.17)
8.01 (1.24)
11.27 (2.43)
5.47 (1.19)
7.53 (0.99)
10.51 (2.10)
5.74 (1.12)
7.69 (1.10)
10.79 (2.16)
*The values are given as the median, with the standard deviation in parentheses.
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY
Fig. 2
Canal Diameter
In male subjects, the median canal diameter at the second cervical level increased from 12.79 mm at six months to 16.00 mm
by 156 months and remained constant thereafter. In female
subjects, the median canal diameter at the second cervical level
increased from 12.27 mm at six months to 15.75 mm by 168
months. A graph of the results is shown in Figure 3. The canal
diameters at the third and fourth cervical levels were nearly
identical in terms of both dimension and rate of change. In
male subjects, the median canal diameter increased from 12.33
mm initially to 15.54 mm by maturity. In female subjects, the
median canal diameter at these levels increased from 11.76 mm
to 15.31 mm. In male subjects, the median canal diameter at the
fifth cervical level increased from 12.74 mm to 15.67 mm, and
in female subjects, it increased from 12.26 mm to 15.22 mm.
Torg Ratio
The median Torg ratio (the ratio of the canal diameter to the
vertebral body diameter) at the fifth cervical level was 1.47
(tenth to ninetieth percentile, 1.26 to 1.64) at three months
and 1.06 (0.81 to 1.33) by maturity for male subjects and 1.47
(1.04 to 1.75) and 1.10 (0.88 to 1.20), respectively, for female
subjects. A graph of the results is shown in Figure 4.
Width of the Cervical Vertebral Bodies
The median width of the second cervical vertebral body increased from 9.13 mm initially to 15.15 mm by maturity for
male subjects and from 8.40 mm to 14.90 mm for female sub-
Fig. 3
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY
Fig. 4
Fig. 5
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
basis. Their patients were at least three years old, whereas our
patients were followed beginning at the age of three months.
Additionally, Locke et al. measured only the atlantodens interval, whereas we evaluated a wide variety of radiographic dimensions of the cervical spine in the growing child. The
atlantodens interval is a radiographic representation of the relationship between the posterior aspect of the anterior arch of
the first cervical vertebra and the anterior aspect of the odontoid process. The normal value suggests that the transverse ligament and the other check ligaments are still functional.
A standard set of normal values for the cervical vertebral
bodies has not been published in the literature. Very few, if
any, investigators have even attempted to examine the growth
and development of the pediatric cervical vertebral body1.
Most investigators have concentrated on depicting standard
values for the cervical canal14,15. Swischuk et al. examined the
lateral radiographs of the cervical spine of 481 pediatric patients to assess the configuration of the vertebral bodies21.
Their findings demonstrated that cervical vertebral bodies are
oval early in infancy and become more rectangular as maturation proceeds. That study was not longitudinal. The authors
also did not attempt to provide numerical values for the vertebrae as they developed.
It is important to note that the current study is an examination of radiographic manifestations and measurements of
development and applies only to the portion of the skeleton
that has transformed into bone.
To our knowledge, the present investigation is the first
prospective, highly controlled study in which the growth and
development of the cervical spine was assessed in a longitudinal manner from the age of three months to skeletal maturity.
We found that the cervical canal grows rapidly during the first
three years of life, by which time it has reached nearly 95% of
its mature diameter. The increase in the height of the third,
fourth, and fifth vertebral bodies was linear from the age of six
months to maturity, but the growth of the second cervical vertebra was most rapid in the first five years of life and became
linear thereafter. This appears to be a function of the increasing height of the dens, and it may be an artifact of the ossification of the superior portion of the dens. Our findings indicate
that the vertebral bodies grow rapidly during the first five
years of life and then continue to grow at a slower rate until
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY
References
1. Bailey DK. The normal cervical spine in infants and children. Radiology.
1952;59:712-9.
2. Fesmire FM, Luten RC. The pediatric cervical spine: developmental anatomy
and clinical aspects. J Emerg Med. 1989;7:133-42.
3. Fielding JW, Cochran GV, Lawsing JF, Hohl M. Tears of the transverse ligament of the atlas. A clinical and biomechanical study. J Bone Joint Surg Am.
1974;56:1683-91.
4. Kaufman RA, Carroll CD, Buncher CR. Atlantooccipital junction: standards for
measurement in normal children. AJNR Am J Neuroradiol. 1987;8:995-9.
5. Shapiro R, Youngberg AS, Rothman SL. The differential diagnosis of traumatic lesions of the occipito-atlanto-axial segment. Radiol Clin North Am.
1973;11:505-26.
6. Swischuk LE. Anterior displacement of C2 in children: physiologic or pathologic? Radiology. 1977;122:759-63.
THE JOUR NAL OF BONE & JOINT SURGER Y JBJS.ORG
VO L U M E 83-A N U M B E R 8 A U G U S T 2001
G ROW T H A N D D E VE L O P M E N T O F T H E P E D I A T R I C
CER V ICAL SPINE DOCUMENTED RADIOGRAPHICALLY