|Year : 2011 | Volume
| Issue : 2 | Page : 309-316
|Evaluation of skeletal maturation by comparing the hand wrist radiograph and cervical vertebrae as seen in lateral cephalogram
Department of Orthodontics and Dentofacial Orthopaedics, Uttar Pradesh Dental College and Research Centre, Lucknow, Uttar Pradesh, India
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|Date of Submission||24-Feb-2010|
|Date of Decision||24-Jul-2010|
|Date of Acceptance||18-Apr-2011|
|Date of Web Publication||27-Aug-2011|
| Abstract|| |
Background and Objectives: Aim of this study was to determine the validity of cervical vertebrae radiographic assessment to predict skeletal maturation.
Materials and Methods: Left-hand wrist and lateral cephalometric radiographs of 100 Bangalore children aged 8-18 years, divided into 10 groups of 10 subjects each with equal distribution of males and females, were measured. On left-hand wrist radiograph, the classification of Fishman was used to assess skeletal maturation. Cervical vertebrae maturation was evaluated with lateral cephalometric radiograph, using the stages developed by Hassel and Farman. The changes in hand wrist and cervical vertebrae were correlated.
Results: Significant association was observed between skeletal maturation indicator stages and cervical vertebrae maturation indicator stages. Correlation coefficient was found to be significant (P<0.0001).
Conclusion: The results of the study indicated that the cervical vertebrae maturation and hand wrist skeletal maturation was significantly related.
Keywords: Cervical vertebrae, cervical vertebrae maturation indicator, hand wrist radiograph, skeletal maturation indicator
|How to cite this article:|
Mahajan S. Evaluation of skeletal maturation by comparing the hand wrist radiograph and cervical vertebrae as seen in lateral cephalogram. Indian J Dent Res 2011;22:309-16
Growth biologically and histologically is a composite of morphogenetic and histogenetic changes occurring continuously over a period of time in response to genetic coding and environmental influences. Human growth is characterized by considerable variation in the rate of progress of different persons toward physiologic maturity. It is one of the most myriad variations in nature and plays an important role in the etiology of malocclusion and also in evaluation of diagnosis, treatment planning, retention and stability of any case.
|How to cite this URL:|
Mahajan S. Evaluation of skeletal maturation by comparing the hand wrist radiograph and cervical vertebrae as seen in lateral cephalogram. Indian J Dent Res [serial online] 2011 [cited 2019 Oct 22];22:309-16. Available from: http://www.ijdr.in/text.asp?2011/22/2/309/84310
The developmental status of a child is usually assessed in relation to events that take place during the progress of growth. Thus, chronological age, dental development, height and weight measurements, sexual maturation characteristics and skeletal age are some biological indicators that have been used to identify stages of growth.
Many researchers have agreed that skeletal maturity is also closely related to the craniofacial growth, and bones of hand wrist and cervical vertebrae are very reliable parameters in assessing it.
The complete hand wrist radiograph involves 30 bones and assessment of these stages is one elaborate task which needs time and experience and also involves increased radiation exposure, therefore putting a question mark on ALARA (as low as reasonably achievable) principle.
Fishman developed a system of skeletal maturity indicators using four stages of bone maturation found at six anatomical sites on hand and wrist radiographs.  The use of cervical vertebrae to determine the skeletal maturity was first suggested by Lamparski.  He concluded that the cervical vertebrae, seen in normal routine lateral cephalograms, were as statistically and clinically reliable in assessing skeletal age as hand wrist technique. This was confirmed by Farman and Hassel,  Fernandz,  and Nazanet al. 
The primary aim and objective of the study were to assess the skeletal age of an individual by interpretation of the cervical vertebrae as seen in lateral cephalogram which is obtained as a standard pre-treatment diagnostic record and to correlate and evaluate the changes in the shape and size of the cervical vertebrae with the skeletal maturity index on a hand wrist radiograph.
| Materials and Methods|| |
The study was conducted in the Department of Orthodontics at Bangalore Institute of Dental Sciences and Postgraduate Research Centre and Hospital, Bangalore.
The sample consisted of 100 subjects aged between 8 and 18 years, divided into 10 groups of 10 subjects each with an equal distribution of males and females in each group. The subjects were randomly selected from the patients visiting Department of Oral Medicine, Diagnosis and Radiology, Department of Orthodontics and Department of Pediatric Dentistry, Bangalore Institute of Dental Sciences and Postgraduate Research Centre and Hospital, Bangalore, and also from the schools of local suburban area of Bangalore city.
The sample was a mixed one consisting of patients with normal occlusion, malocclusion, those undergoing orthodontic treatment with no congenital disorders and falling into the norms of Indian society.
The radiographs taken included the lateral cephalogram and the left hand wrist radiograph.
The materials used for the study were as follows.
Lateral cephalogram for recording cervical vertebrae maturation factors [Figure 1].
|Figure 1: Patient positioning for recording cervical vertebrae maturation indicator using lateral cephalogram|
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Planmecaproline XC with digital cephalostat X-ray machine, recently introduced in India, was used to take the lateral cephalograms.
The technical specifications of Planmeca XC machine are tabulated below:
*IEC - International electrical code; **SID- Source to image distance
Patient positioning for exposure of lateral cephalogram
Digital cephalograms were taken with functional head positioners. The patients were made to stand in orthoposition and a triple laser beam system accurately indicated the correct anatomical positioning points as follows:
- The midsaggital plane positioning beam indicated the correct sideways alignment of patient's head. The image will be symmetric and undistorted in right left direction.
- The Frankfort horizontal plane positioning beam indicated the correct forward tilt of patient's head.
- Focal layer positioning beam indicated the focal layer's position in incisor region which helps in positioning the patient fully inside the focal layer for sharp and clear images.
With this triple laser beam system, the operator can monitor the patient freely from the front and side, making patient positioning quick, precise, easy and minimizes the errors caused by incorrect positioning which is one of the most frequent reasons for failed radiographs.
Hand wrist machine for recording maturational status
Meditronics 300 MA, X-ray machine (Toshiba, RotanodeTM) 44 kVp and 45 mA was used with exposure time of 0.4 sec.
Patient positioning for hand wrist radiographs
Patients were made to sit straight and were instructed to place their left hand with "PALM DOWN" flat on the cassette, with fingers slightly separated and the axis of hand wrist and forearm in a straight line. The center of tube was halfway between the tips of fingers and distal end of radius. The radiographs included complete fingers and the radius.
Cassette used for taking both hand wrist radiograph and lateral cephalogram
ADC CR cassettes (AGFA) of size 8″×10″ (18×24 cm) were used to take both the lateral cephalogram and left-hand wrist radiograph.
ADC cassette contains the photostimulable phosphor imaging plate and has a permanently mounted memory chip to store data entered at the ID terminal. The identification data and the image are thus joined from the beginning and are permanently linked as they pass through the electronic processing system.
The cassettes are lead backed to ensure optimal backscatter protection and to avoid adverse effects of backscatter on image quality.
The ADC cassettes are loaded with the corresponding imaging plates and pre-initialized in the factory. The embedded initialization software will drive readout process to select a pixel matrix corresponding to a partial resolution of 9 pixels/mm.
Digitizer used for computed radiography
CR 25.0 digitizer (AGFA) was used for computed radiography. It is compatible with all the existing X-ray systems, allowing X-ray departments to go digital without significant additional investments and workflow adaptations. It reads imaging plates at a standard resolution of 6 pixels/mm.
Assessment of skeletal maturation using skeletal maturation indicators (SMIs) from hand wrist radiograph as an indicator [Figure 2] and [Figure 3].
The system developed by Fishman was used to determine skeletal maturation by hand wrist evaluation on each subject.
Once skeletal maturation was assessed from the hand wrist radiograph, the lateral cephalogram taken on the same date was taken from the record. The hand wrist X-ray and lateral cephalogram were traced on 0.003-inch matte acetate with a 0.5-mm-diameter lead pencil, using a radiographic illuminator.
The entities traced were body of third cervical vertebrae (C 3 ) and body of fourth cervical vertebrae (C 4 ).
To evaluate the maturational patterns of the indicators in the hand wrist, 11-grade system of Fishman was used. 
Assessment of skeletal maturation using cervical vertebrae as an indicator (Hassel and Farman) [Figure 4]
Cervical vertebral development of the sample was evaluated by Hassel and Farman, by a modification of Lamparski's criteria, which assess maturational changes of the second, third and fourth cervical vertebrae. 
Six distinct stages of growth can be related to the skeletal maturity indicator developed by Fishman. 
- Initiation stage of cervical vertebrae [cervical vertebrae maturation indicator (CVMI)-1] (skeletal maturity indicator 1 and 2)
- C 2 , C 3 and C 4 inferior vertebral body borders are flat
- Superior vertebral borders of C 3 and C 4 are tapered from posterior to anterior (wedge shape)
- 100% of pubertal growth remains
- Acceleration stage of cervical vertebrae (CVMI-2) (skeletal maturity indicator 3 and 4)
- Concavities begin to develop on the inferior borders of C 2 and C 3
- Inferior border of fourth vertebrae remains flat
- Vertebral bodies of C 3 and C 4 are nearly rectangular in shape
- 65-85% of pubertal growth remains
- Transition stage of cervical vertebrae (CVMI-3) (skeletal maturity indicator 5 and 6)
- Distinct concavities seen in lower borders of C 2 and C 3
- Developing concavity seen in lower border of body of C 4
- 25-65% of pubertal growth remains
- Deceleration stage of cervical vertebrae (CVMI-4) (skeletal maturity indicator 7 and 8)
- Distinct concavities in lower borders of C 2C 3 and C 4 are observed
- C 3 and C 4 are nearly square in shape
- 10-25% of pubertal growth remains
- Maturation stage of cervical vertebrae (CVMI-5) (skeletal maturity indicator 9 and10)
- Accentuated concavities of inferior vertebral body borders of C 2 , C 3 and C 4 are observed
- C 3 and C 4 are square in shape
- 5-10% of pubertal growth remains
- Completion stage of cervical vertebrae (CVMI-6) (skeletal maturity indicator 11)
- Deep concavities are present for inferior vertebral body borders of C 2 , C 3 and C 4
- C 3 and C 4 heights are greater than widths
- Pubertal growth has been completed
All radiographs were evaluated by the same operator and later verified by an independent evaluator to determine any interoperator and intraoperator errors.
The cervical vertebrae C 3 and C 4 were observed and each patient was placed in CVMI category. The CVMI readings were then evaluated against the previously determined SMI readings to see what correlations existed.
| Results and Observations|| |
The SMI scores and CVMI scores were obtained and analyzed with reference to chronological age and sex.
The SMI and CVMI were compared with each other and their correlation was established statistically.
The obtained data were fed into the computer and statistical analysis was done for the same using the software "Statistical Package for Social Sciences" (SPSS) for windows (version 10.0) and analyzed accordingly (SPSS Inc., 1999 New York, USA). Statistical significance was tested at P<0.05 level.
The following statistical methods were employed in the present investigation:
The following results were drawn from the statistical analysis.
- Mean and standard deviation
- Correlation coefficient
- Student's " t" test
- Analysis of variance (ANOVA) test
[Table 1] shows the sample size selected for the study, which consisted of 100 subjects with equal distribution of males and females in the age group 8-18 years.
In [Table 2]a-c, a significant difference in the chronological age was observed in the descriptive statistics of age of both sexes for SMI score.F values of 61.780 for males and 47.113 for females were found to be significant at P <0.0001. The difference in mean age between males and females at SMI grade 3 and 10 was found to be statistically significant at P <0.05 and P <0.02, respectively. A striking feature observed was that the maturation development for females was earlier than their male counterparts. The mean age for initiation of skeletal maturation was 8.43±0.535 years for males and 8.00±0.00 years for females (SMI 1). Females completed skeletal maturation at mean age of 16.18±0.874 years and males completed the skeletal maturation at mean age of 16.56±0.527 years (SMI 11), indicating that the growth spurts existed for a longer duration in males as compared to their female counterparts.
In [Table 3]a-c showing the descriptive statistics of age for both sexes of CVMI, it is seen that the mean age of both the sexes for CVMI is steadily increasing in relation to an increase in CVMI grade. F values of 103.559 for males and 78.661 for females were observed at P <0.0001.Difference in mean age between males and females when the CVMI grade was 2 and 5 was found to be statistically significant at P <0.04 and P <0.001, respectively, thus indicating that the maturation development of females was earlier than their male counterparts.
Mean age for the initiation of skeletal maturation was 8.83±0.937 years for males and 8.73 0.405 years for females. The mean age for maximum puberty growth spurt was 13.40±0.548 years for males and 13.00±1.414 years for females. Females completed skeletal maturation at mean age of 16.67±0.577 years, thus confirming the above statement.
A high degree of correlation coefficient of SMI and CVMI grades (0.976 at P <0.0001) [Table 4] at different age groups of both males and females was observed, especially between the age groups of 10-11 and 12-16 years. Also, a high degree of positive correlation was observed to exist between the SMI and CVMI scores [Table 5] of both the sexes. This indicates that the 11 discrete stages of SMI can be confidently correlated to the corresponding 6 stages of CVMI in both male and female subjects.
|Table 4: Correlation coefficient of skeletal maturation indicator and cervical vertebrae maturation indicator grades at different age groups of both males and females|
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|Table 5: Correlation coefficient of skeletal maturation indicator and cervical vertebrae maturation indicator grades between both males and females|
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| Discussion|| |
Adolescence is a period during which the rate of growth accelerates, reaches a peak velocity and then decelerates until adulthood is achieved. This pattern can be found in all individuals, but there may be a marked individual variation in the initiation, duration rates and amounts of growth during this period of life. In certain individuals, physiologic development proceeds rapidly and the entire pubertal growth period is short, in other words it is sluggish and takes much longer time. 
Knowledge of maturation status of a child plays an important role in the diagnosis, treatment planning and eventual outcome of the treatment. The developmental status of a child may be best assessed not by chronologic age but by physiologic parameters such as peak growth velocity in standing height, voice change in boys, menarche in girls, dental development and skeletal ossification. ,,
The present study was conducted with an aim to assess the skeletal age of an individual by interpretation of the cervical vertebrae as seen in lateral cephalogram and to correlate and evaluate changes in the size and shape of the cervical vertebrae with the skeletal maturity index on a hand wrist radiograph in local Bangalore population. The study was designed with a purpose to equip the orthodontist with new evaluation criteria which would enable him to accurately evaluate the amount of growth remaining, using the existing growth assessment methods in a single clinical visit and using a single diagnostic tool.
This study shows the subjects (males and females) in different stages of skeletal development, when SMI scores were taken as skeletal maturity indicator, especially in SMI 3, where males are in age group of 10-14 years and SMI 10 where females are in age group 12-17 years. Similar results were obtained when subjects were assessed using developmental stages in cervical vertebrae as a biological indicator where subjects in the age group of 8-12 years (males) and 12-17 years (females) demonstrated wide variation in their maturational development. Hence, the present study shows that chronological age was not a reliable indicator of maturation and did not correlate with skeletal maturation indicators (SMI and CVMI). These results are in confirmation with the studies conducted by Bjork and Helm (1967),  Brown,  Fishman,  and Hagg and Taranger (1982). 
There are some physiological events which take place during normal growth of bones, as stated in the literature. Many investigators, namely Tanner (1975),  Grave and Brown,  Hagg, Taranger (1980),  Fishman,  Abder Kader (1998, 1999), , have delineated several specific ossification stages that occur before, at or after peak height velocity. The identification of these skeletal maturation levels provides a useful means of identification of specific points along the progressive path of adolescent growth.
The information from the hand wrist radiographs has been used in number of ways to evaluate the skeletal age or bone age of the child. Bone age can be obtained by either comparing the radiograph in question with a series of standard films representative of normal children at different ages and assigning to the film in question the age of standard that matches it most closely, or by assigning a weighted score to the development stage of each of the 30 bones in the hand and wrist, the bone age then being the total score for the radiograph. 
During a detailed examination of 100 hand wrist radiographs which recorded SMI stages as described by Fishman,  a distinct change in stages was observed.
Though skeletal maturation assessed on hand wrist radiograph has been considered the best indicator of assessment of somatic maturity stage, however, the routine use of hand radiographs has lately been questioned from radiation hygiene safety point of view. ,,
To overcome the issue of additional exposure to the patient, the researchers thought of considering the lateral cephalogram to determine the skeletal maturation as it forms an important armamentarium of the clinical records that were routinely taken for orthodontic diagnosis and treatment planning and also eliminates the need for an additional radiographic exposure.
The first seven cervical vertebrae in the spinal column constitute the cervical spine. The first two, namely Atlas More Details and axis vertebrae, are unique, and the third through seventh vertebrae have great similarity. The maturational changes can be observed in these vertebrae from birth to full maturity. Lamparski first suggested the use of cervical vertebrae to determine the skeletal maturity. He analysed the changes in size and shape of the bodies of five cervical vertebrae (from second to sixth cervical vertebrae) and then created separate standards of cervical vertebral maturation for males and female subjects. Hassel and Farman  later modified Lamparski's method and developed six stages of CVMI by using lateral profiles of 2 nd , 3 rd and 4 th cervical vertebrae which significantly corresponded to 11 SMI values of Fishman. 
In the present study, a significant difference was observed to exist between SMI scores and their corresponding chronological age. F value of 84.069 was found to be highly significant at P <0.0001 level. A general trend observed is that as the SMI scores increased, the corresponding chronological age also increased linearly. A striking feature is that in the male subjects, skeletal maturity was much slower as compared to female subjects of the same age group.
A significant association was observed between SMI stages and CVMI stages. Correlation coefficient of 0.976 was found to be highly significant (P <0.0001). Further, it is evident that the lesser the SMI stages, lesser are the CVMI stages, and also, as SMI stages increased, CVMI stages also increased almost linearly.
As in the case of previous instances, a significant association was observed between SMI stages and CVMI stages when the data were subjected to correlation coefficient analysis for females and males alone. The correlation coefficients of 0.975 and 0.981, respectively, were found to be highly significant (P <0.0001).
Subjects with different SMI stages did not differ significantly in their chronological age (F=84.069; P <0.0001). Even though we find somewhat linear increase in the chronological age with SMI stage, statistically this increase is nonsignificant, i.e. there is no equality of mean age in all SMI grades. Even the subjects with different CVMI stages did not differ significantly in their chronological age (F=132.511; P <0.0001), but there is no equality of mean age observed in all CVMI grades.
So, for clinicians wishing to start orthopedic treatment, continuous monitoring of the skeletal maturity using hand wrist films may not be necessary. Instead, they can monitor the changes in the shape and inferior border curvature of the cervical vertebrae as seen on the routinely taken lateral cephalogram which could be more easily interpreted and is readily available and acceptable.
Orthopedic treatment can be accomplished when the patient is in the stages of initiation and acceleration as there is a good amount of adolescent growth potential still left. The same is difficult to accomplish during the stage of transition wherein probably fixed functional orthopedic treatment can be accomplished. Once the stage of transition is completed, not much of growth is expected. Once the patient attains the stage of deceleration, orthopedic appliances can bring about only minimal skeletal changes and more of dental changes. The same becomes unrealistic in the stage of maturation wherein the bone is completely matured and hence cannot undergo any orthopedic change. Carrying out dentofacial orthopedic treatment in the stage of completion is futile as the growth phase is completed and orthopedic remodeling cannot be attained. Hence, during the stages of deceleration, maturation, completion, it is advisable to let the growth be completed and then advise the patient to undergo orthodontic treatment alone or surgical orthodontic intervention depending on the magnitude of discrepancy.
The advantages of using the cervical vertebrae as a skeletal maturation indicator over hand wrist are the following:
- It is simple and reliable.
- We can avoid taking additional hand wrist film to study the skeletal maturation as it can be accomplished by using the anatomic changes of cervical vertebrae as observed on a routine lateral cephalogram.
- We can avoid an additional exposure of X-rays to the patient, thus following as low as reasonably achievable (ALARA) principle.
- It is economical.
There is definitely a need for further study with a larger sample as it can show much higher correlation than the reading we have obtained in this study, and hence can affirm and confirm to say that this is a much better method than the study of hand wrist radiograph.
However, the need for a longitudinal study is overdue, and if done, will be useful and appreciated. This is because it is more reliable than a cross-sectional study and it is also more individualized. In a cross-sectional study, the amount of variation is too much since socioeconomic status, nutritional status, etc. can vary the maturational status of individuals, whereas in a longitudinal study, the samples being the same, the degree of variation is much less.
| Conclusion|| |
To conclude, we can say that cervical vertebrae radiograph does not score over the hand wrist radiograph in revealing the maturity status of an individual. However, it is as good as a hand wrist radiograph for its diagnostic value in those patients where we do not need to know the exact skeletal age of a patient. This can be helpful to know whether the patient will grow during the 1 or 2 years treatment period and whether percentage of growth can reasonably be expected during the time when orthopedic treatment is initiated.
All this at a significantly reduced radiation exposure to the patient and less elaborate armamentarium itself places cervical vertebrae in the same platform as a hand wrist radiograph.
| References|| |
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|13.||Hussam. M. Abdel Kader. The reliability of dental x-ray film in assessment of MP3 stages of the pubertal growthspurt. Am J Orthod Dentofac Orthop 1998;114:427-9. |
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Department of Orthodontics and Dentofacial Orthopaedics, Uttar Pradesh Dental College and Research Centre, Lucknow, Uttar Pradesh
Source of Support: None, Conflict of Interest: None
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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