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The determination of the best moment to intervene is a constant pursuit in orthodontic treatments. The evaluation of the skeletal age can provide additional information that can contribute for this decision. Hand-wrist radiography is recognized as a reliable parameter to evaluate the skeletal age of a patient. In 1972, Lamparski proposed the use of lateral cephalometric radiography and the observation of cervical vertebrae as a new parameter to evaluate the patient’s skeletal age. Several studies were and are being carried out to confirm the efficiency of this evaluation. A review of the literature, and whether the reliability of this type of interpretation is safe, are the objectives of this work.
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1
Skeletal and vertebral age – a literature review
Sergio Polizio Terçarolli Jaw Functional Orthopedics Specialist
ABSTRACT
The determination of the best moment to intervene is a constant pursuit in
orthodontic treatments. The evaluation of the skeletal age can provide additional
information that can contribute for this decision. Hand-wrist radiography is
recognized as a reliable parameter to evaluate the skeletal age of a patient. In
1972, Lamparski proposed the use of lateral cephalometric radiography and the
observation of cervical vertebrae as a new parameter to evaluate the patient’s
skeletal age. Several studies were and are being carried out to confirm the
efficiency of this evaluation. A review of the literature, and whether the reliability
of this type of interpretation is safe, are the objectives of this work.
Key words: jaw functional orthopedics, cervical vertebrae, vertebral age,
cephalometry, maturity.
=======================================================
Understanding the development pattern of growing patients is one of the
greatest responsibilities of Jaw Functional Orthopedists and/or Orthodontists.
It is of fundamental importance for the functional orthopedic or orthodontic
treatment to know if the growth surge will happen, is happening or has
happened1. Based on this information, it is possible to intervene at the most
appropriate moment, obtaining faster and more efficient results.
Manifestations of secondary sexual characteristics2,3, height and weight
variations4, chronological age5, dental age6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24
2
and skeletal age7,25,26,27,28,29,30,31,32,33 are part of the enormous arsenal referenced
in literature, and serve as criteria for the evaluation of the physiological age of
an individual. These criteria are based on the degree of maturity of different
tissues of the system and can be applied together or separately21.
Several body locations were studied to determine skeletal maturity or skeletal
age.: ulnar sesamoid of the thumb34,35,36, wrist and hand27,28,31,
teeth9,10,11,12,14,15,16,17,18,20,21,22,23, calcification of the hook of the hamate bone37,
development of the epiphysis of the middle phalanx of the 3rd finger28,36,37.
Based on Lamparski’s works38, another source of inquiry and reference in the
study of skeletal maturity of individuals can be evaluated: the vertebral skeletal
age.
“The process of skeletal maturation consists of differentiation, growth and
change of shape. These alterations start at the ossification centers and end with
the complete development of the bone. The entire process can be accompanied
or investigated by radiographic exams”39.
As the concern with the quality of life of patients is ever more present, one of the
alternatives to reduce the amount of ionizing radiation40 (elimination of hand-
wrist radiograph), is the use of lateral cephalometric radiography, which is
present in any routine orthodontic exam, to evaluate the skeletal maturity of an
individual.
Thus, structures not observed before, such as the frontal sinus41 and cervical
vertebrae1,25,38,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57 became the objective of
investigations. Other alternatives, such as the inclusion of the first three fingers
of the right hand in a cephalometric radiograph58,59 and the periapical x-ray of
the middle finger to evaluate the middle phalanx, were also investigated58.
A review of the literature about the reliability of evaluating the maturation of
cervical vertebrae (vertebral skeletal age) is the subject of this article.
3
LITERATURE REVIEW
The vertebral column is formed by cervical, thoracic and lumbar vertebrae and
by the sacrum60. The first seven vertebrae form the cervical column, with great
similarity between the four last ones61. Maturational alterations can be seen from
birth till maturity60,62.
Lamparski38 proposed in his study to examine growth (increase in size with age)
and development (maturation) of cervical vertebrae to determine if alterations
found in this area could be used to evaluate skeletal age in lieu of hand-wrist
radiographs. His method was based on the works by Bick and Copel62, Todd
and Pyle63, Eslberg and Duke64, Lanier65 e Hinck, Hopkins, Savara66.
Lamparski38 then established a maturational pattern for cervical vertebrae using
vertebrae C2, C3, C4, C5 and C6. This standardization consisted of 6 stages.
The following conclusions were taken from his work: the maturational changes
that occur between the second and sixth cervical vertebrae can be used to
evaluate the skeletal age of an individual; the evaluation of vertebral age is
statistically valid and reliable, and has the same clinical value of hand-wrist
evaluations, thus, an additional radiograph is not needed to evaluate growth
potential; the cervical vertebrae maturation indicators (CVMI’s) are: initiation and
development of concavities on the lower borders of the vertebral bodies, and
increase of the anterior portion and of the total height of these vertical bodies,
causing changes in their shape, changing from a wedge shape to a rectangular
shape and later, to a square, and at the end of development presenting a
predominance of height over width; the vertebral maturity indicators are the
same for males and females. The difference lies in the fact that each stage of
vertebral development occurred earlier in females than in males.
Biological, osseous or skeletal age and skeletal maturation are synonyms used
to describe maturation stages in humans, i.e., the degree of development of
ossification on the bone. All changes in bones during growth can be observed
4
by radiographs. These changes are relatively constant for a given bone in a
person. Size and maturity can vary independently of each other. Modifying the
method proposed by Lamparski38, Hassel and Farman1 observed the vertebral
bodies of C2 (odontoid process), C3 and C4 vertebrae in a lateral cephalometric
radiograph, and evaluated their skeletal maturity through a correlation with the
Fishman method26 which, in turn, evaluates skeletal hand-wrist maturation with
a Skeletal Maturity Indicator (SMI) system developed by him. The main objective
of the study was to create an evaluation method of skeletal maturity using a
routine radiograph in orthodontic treatments. For this purpose were used 220
male and female individuals aged 8 to 18 years, from whom were taken, on the
same day, left hand-wrist radiographs and lateral cephalometric radiographs.
They then determined 6 separate phases for the maturation stages of cervical
vertebrae: initiation, acceleration, maturation, transition, deceleration and
finalization. Each has specific characteristics related to vertebra shape, which
determines skeletal maturity and whether there is a potential for growth.
1- INITIATION
Corresponds to the combination of Fishman’s stages 1 and 226;
Great amount of pubertal growth expected (80 a 100%);
Upper C3 and C4 edges are funneled from the posterior to the anterior region;
Lower borders of C2, C3 and C4 are plane or flat;
The vertebrae are wedge-shaped, with upper border inclined from posterior to
anterior region (figure 1).
2- ACCELERATION
Corresponds to the combination of Fishman’s stages 3 and 426;
Significant pubertal growth expected (65 a 85%);
5
Start of development of concavities on the lower borders of C2 and C3 (figure
1);
Lower border of C4 plane or flat;
The vertebral bodies of C3 and C4 tend towards a rectangular shape.
3- TRANSITION
Corresponds to the combination of Fishman’s stages 5 and 626;
Moderate pubertal growth expected (25 a 65%);
Presence of noticeable concavities on the lower borders of C2 and C3;
Start of development of a concavity on the lower border of C4 (figure 1);
C3 and C4 have a rectangular shape.
4- DECELERATION
Corresponds to the combination of Fishman’s stages 7 and 826;
Reduced expectation of pubertal growth (10 a 25%);
Presence of noticeable concavities on the lower borders of C2, C3 and C4
(figure1);
Shape of C3 and C4 nearing that of a square.
5- MATURATION
Corresponds to the combination of Fishman’s stages 9 and 1026;
Insignificant puberal growth expected (5 a 10%);
Presence of prominent concavities on the lower borders of C2, C3 and C4;
Square shape of vertebrae C3 and C4 (figure 1).
6- FINALIZATION
Corresponds to Fishman’s stage 1126;
Pubertal growth completed at this stage (little or no growth expected);
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Presence of deep concavities on the lower borders of C2, C3 and C4;
In the vertebral bodies of C3 and C4, there is a predominance of height over
width (figure 1).
Fig. 1 – The 6 stages of vertebral maturity described by Lamparski38 and modified by Hassel and Farman1. In their conclusions, the authors admit the reliability of lateral cephalometric
radiography to evaluate growth potential through skeletal maturity of cervical
vertebrae, thus making it easier to plan for the orthodontic or functional
orthopedic treatment.
In their work, Rajagopal and Kansal58 compared the six stages of skeletal
maturity observed on the middle phalanx of the middle finger (MP3) and
reported by Hagg and Taranger67, with the six maturation indicators of cervical
vertebrae (MICV) proposed by Hassel and Farman1. However, the technique
CC22
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CC44
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CC33
CC44
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CC33
CC44
CC22
CC33
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INITIATION ACCELERATION TRANSITION
MATURATION FINALIZATION DECELERATION
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was modified by the use of a radiographic film appropriate for periapical to
radiograph the middle finger, instead of a hand-wrist radiograph. Of the 150
individuals analyzed, 75 were male and 75 females, with ages varying from 9 to
17. In their conclusion, the authors affirm that the modification of technique is
accurate, simple, practical and economical, in addition to showing an intimate
correlation with the MICV’s.
Garcia-Fernandez, Torres, Flores, Rea43 investigated the correlation between
cervical vertebrae and hand-wrist maturational indicators in a group of 113
Mexicans (50 men and 63 women) with ages ranging from 9 to 18 years. The
lateral cephalometric and hand-wrist radiographies were taken on the same day,
similarly to the work by Hassel and Farman1.
In the authors’ opinion, the orthodontist and/or jaw functional orthopedist do not
need to know accurately the skeletal age; how much will the bones grow during
treatment, or exactly when growth will take place. They need to know whether
the patient will grow during treatment and what percentage of growth can be
expected during that period.
The results of this investigation showed that there is no significant difference
between the two techniques of skeletal maturity evaluation in the Mexican
populational group. For this reason, cervical vertebrae could be used for this
type of evaluation.
O’Reilly and Yanniello45 report that a series of studies about mandibular growth
during adolescence have direct relationship with the ossification events
observed in hand-wrist radiographs68,69,70. The authors investigated the
maturation stages of cervical vertebrae determined by Lamparski38 and the
changes in the measurements of corpus length and height of ramus of the
mandible. Annual lateral cephalometric radiographies were taken of 13 girls
varying between 9 and 15 years of age. The analysis of the results showed a
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significant increase in corpus length and height of the mandibular ramus during
the stages of vertebral maturation.
It was clear from the study that the stages of cervical vertebrae maturation have
a relationship with mandibular growth, and serve as an tool to evaluate when
mandibular changes take place during adolescence.
Research by Santos and Almeida71) compared changes in cervical vertebrae
with the ossification events in the hand-wrist region, with the objective of
showing the reliability of cervical vertebrae evaluation. Lateral cephalometric
radiographs and hand-wrist radiographs of individuals between 8-years-and-5-
months and 16-years-and-5-months of age, male and female, were used. In
their conclusion, the authors reported that both methods were of easy to apply
and that the correlation between them was statistically significant. Additionally,
the morphological changes of cervical vertebrae observed in lateral
cephalometric radiographs were a useful additional method to determine
skeletal age. Should there be a need for a more precise diagnosis, this type of
exam should not be used alone.
Nanda72, carried out a longitudinal study with 19 female patients,
leukodermatous, healthy, of medium-high social-economical level, in the city of
Denver, Colorado. Annual lateral cephalometric radiographies of these patients
were taken between the ages of 3 and 19 years, with a minimum of 10 and a
maximum of 15 radiographies evaluated for each patient. The Sella-Gnathion
linear distance was used to determine the maximum moment of facial growth
during adolescence, expressed by the increase of vertical and horizontal face
dimensions. Other aspects observed were the variations of stature in
centimeters, skeletal age by carpal radiography, according to Greulich and
Pyle27,28, dental age by the observation of Nolla’s stages8 of the first, second and
third molars, in addition to the vertebral age based in Lamparski’s work38. After
the evaluation of results, the author concluded that skeletal age, evaluation of
9
stature and vertebral age can be used to determine facial development pattern
determined by the measurement Sella-Gnathion. However, dental age showed
ample variations, especially above the age of 13.
Hellsing44, using lateral cephalometric radiographs of 107 patients of both
sexes, and correlating the changes in cervical vertebrae height and width with
pubertal stature growth (record of the patient’s height) concluded that the height
and width of the vertebrae can be used as indicators of skeletal growth.
Additionally, according to the author, the main advantage of using vertebral
development as an alternative for the evaluation of skeletal maturity, is the fact
that it does not require more than one radiographic technique, as the lateral
teleradiography commonly used for diagnosis can be used.
Mito, Sato, Hideo48 proposed in their work the establishment of vertebral skeletal
age as an objective index to evaluate skeletal maturation. Through the
observation of cephalometric radiographs enlarged 1.0625 times (and
evaluation of C3 and C4 vertebrae) in a group of 176 girls between 7 and 14.9
years of age, a formula was determined to obtain the vertebral skeletal age. In a
second group of 66 girls (between 8 and 13.9 years of age, thus with an
average age of 11 +/- 1.57 years) an evaluation was made of the reliability of
vertebral skeletal age in comparison to skeletal age obtained through the
Tanner-Whitehouse method (TW2)73 of hand-wrist radiographs . The authors 73
consider the TW2 method the most reliable one to evaluate skeletal age, and
the exams showed a high significance index between vertebral age and skeletal
age, even more than between vertebral age and chronological age. The results
suggested that vertebral age, evaluated in lateral cephalometric radiographs, is
as reliable as skeletal age obtained through hand-wrist radiographs by the TW2
method73. This method evolved to method TW3, more efficient and easier to
handle74.
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Román, Palma, Oteo, Nevado57 developed a complex and rigorous investigation
with the objective of determining if morphological changes observed in cervical
vertebrae were as advantageous to determine growth stages as they were to
determine maturation stages, through the use of hand-wrist exams. The
research involved 958 individuals between 5 and 18 years of age (428 boys with
average age of 11.6 years and 530 girls with average age of 11.5 years). Lateral
cephalometric radiographs and hand-wrist radiographs were done during a
period of less than one month. To evaluate skeletal age, the Grave and Brown
method75 and the Björk and Helm growth curve4 were used. The method
developed by Lamparski38, and later by Hassel and Farman1, was used to
evaluate vertebral maturation. Using a system developed by the authors, they
analyzed: concavity of the lower borders of C2 to C6, height of vertebral bodies
of C3 and C4, and the shape of vertebral bodies of C3 and C4. Correlations
between skeletal age and different classifications of vertebral maturation
between skeletal age and anatomical parameters of the cervical vertebrae and
between skeletal age estimated by the concavity, height and shape of cervical
vertebrae were done. The results suggest that this method to evaluate skeletal
maturation, although very reliable, requires the development of a simpler
manner of investigation. According to the authors, the observation of the lower
border of the cervical vertebrae is the best parameter to evaluate vertebral
maturation.
Kucukkeles, Acar, Biren, Arun56 compared the cervical vertebrae and hand-wrist
skeletal maturity evaluation methods in a study with 180 individuals, male and
female, with ages varying between 8 and 18. The lateral cephalometric
radiographs and the hand-wrist radiographs of each individual were observed
according to the evaluation indices professed by Hassel/Farman1 and Fishman26
respectively.
11
The CVMI (cervical vertebrae maturation index) and the SMI (skeletal
maturation index) were divided into 3 pubertal growth periods: pre-peak, peak e
post-peak. The authors showed that the CVMI’s could be used to evaluate the
stages of pubertal growth periods.
DISCUSSION
The first maturational development pattern created in 1959 by Greulich and
Pyle28 Fishman26 demonstrated that the accelerations and decelerations of
craniofacial growth were associated with the concurrent changes of maturational
development revealed in hand-wrist radiographs. Like Fishman’s26, a series of
methods to evaluate skeletal maturity indicators can be found in literature, such
as Greulich and Pyle28, Tanner and Whitehouse76, Todd77 and Grave and
Brown78. Some of these methods are based on observations of a number of
maturational indicators that represent stages of skeletal development for each
age28. Others are based on skeletal stage and events at each age76,26. The
observation of the ossification of epiphysial cartilages in the hand79 can also
serve as an evaluation method.
All of them have a sole objective, to evaluate a patient’s skeletal age and
establish if growth has happened, is happening or will happen. Although hand-
wrist radiographs are used by jaw functional orthopedists and orthodontists to
this end, the need of an additional radiographic technique has been
questioned40. Alternatives have been tried29,41,58,59.
Firstly Lamparski38, and later several other authors42,43,44,46,47,48,51,52,53,56,57
determined a new way to evaluate skeletal maturity using cervical vertebrae as
a reference. According to the majority of them, this method is simpler, more
economical, and avoids one additional exposure to ionizing radiation, since a
carpal radiograph is not needed. This method has shown to be more and more
reliable in view of the enormous amount of research on the subject. Based on
12
the work by Lamparski38, four other vertebral maturation evaluation criteria were
found in the literature: Hassel and Farman1, Baccetti, Franchi and McNamara
JR51, Mito, Sato and Hideo48 and Román, Palma and Oteo57. Variables like race
and sex1,38,42,43,45,46,47,48,52,57,80 were amply explored in these researches, and
none of the authors reported significance of these parameters. Townsend and
Grave52 suggest that the evaluation of vertebral maturation can be applied in a
general manner to orthodontic practice.
Mandibular growth can be forecast by observation of cervical
vertebrae45,50,51,55,81. According to Baccetti, Franchi and McNamara JR51 (using
their own evaluation criteria), the peak of mandibular growth happens between
CVMI 2 and 3.
The exactness and reliability of the use of cervical vertebrae to evaluate growth
potential were also researched54. There was little concern with chassis
position46,47 and with positioning of the individual38,46,57 in the literature reviewed.
CONCLUSION
Based on the literature reviewed, it was determined that the relationship
between skeletal age and vertebral age is very close and, for this reason, the
reliability of this type of interpretation is sufficiently safe.
It is suggested that the best vertebrae to be evaluated are C3 and C4.
The fact that only one radiograph is needed to evaluate skeletal discrepancies,
positional changes and growth potential of patients, solidly demonstrates the
validity, in clinical practice, of this type of evaluation for jaw functional
orthopedists and/or orthodontists.
======================================================
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