ORIGINAL ARTICLE
Cervical vertebral bone age in girls Toshinori Mito, DDS,a Koshi Sato, DDS, PhD,b and Hideo Mitani, DDS, MS, PhDc Sendai, Japan The purpose of this study was to establish cervical vertebral bone age as a new index for objectively evaluating skeletal maturation on cephalometric radiographs. Using cephalometric radiographs of 176 girls (ages 7.0-14.9 years), we measured cervical vertebral bodies and determined a regression formula to obtain cervical vertebral bone age. Next, using cephalometric and hand-wrist radiographs of another 66 girls (ages 8.0-13.9 years), we determined the correlation between cervical vertebral bone age and bone age using the Tanner-Whitehouse 2 method. The following results were obtained: (1) a regression formula was determined to obtain cervical vertebral bone age based on ratios of measurements in the third and fourth cervical vertebral bodies; (2) the correlation coefficient for the relationship between cervical vertebral bone age and bone age (0.869) was significantly (P ⬍ .05) higher than that for the relationship between cervical vertebral bone age and chronological age (0.705); and (3) the difference (absolute value) between the cervical vertebral bone age and bone age (0.75 years) was significantly (P ⬍ .001) smaller than that between cervical vertebral bone age and chronological age (1.17 years). These results suggest that cervical vertebral bone age reflects skeletal maturity because it approximates bone age, which is considered to be the most reliable method for evaluating skeletal maturation. Using cervical vertebral bone age, it might be possible to evaluate maturity in a detailed and objective manner on cephalometric radiographs. (Am J Orthod Dentofacial Orthop 2002;122: 380-5)
I
t is important to evaluate skeletal maturation in orthodontic treatment. Skeletal maturation can be assessed by various indicators: body height,1 handwrist measurements, menarche, voice change, and dental development. Bone age determined with hand-wrist radiographs, as in the Tanner-Whitehouse 2 (TW2) method, is the most popular and reliable parameter for evaluating skeletal maturation.1-5 However, this method requires hand-wrist radiographs. Cervical vertebrae appear on cephalometric radiographs that orthodontists usually use in planning treatment, and Sato6 reported that the appearance of the epiphyseal plate of the odontoid process could be used as an indicator of the maximum growth peak. It is well known that the lateral view of cervical vertebral bodies changes with growth (Fig 1).7-9 Lamparski10 published an atlas that simulated the morphological changes in cervical vertebral bodies in puberty and used these changes to evaluate skeletal maturation. From the Division of Orthodontics, Department of Lifelong Oral Health Science, Graduate School of Dentistry, Tohoku University, Sendai, Japan. a Graduate student. b Assistant professor. c Professor and chairman. Reprint requests to: Toshinori Mito, Division of Orthodontics, Department of Lifelong Oral Health Science, Graduate School of Dentistry, Tohoku University, 4-1, Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan; e-mail: mito@mail.cc.tohoku.ac.jp. Submitted, January 2002; revised and accepted, March 2002. Copyright © 2002 by the American Association of Orthodontists. 0889-5406/2002/$35.00 ⫹ 0 8/1/126896 doi:10.1067/mod.2002.126896
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Hassel and Farman11 and Garcia-Fernandez et al12 reported a high correlation between cervical vertebral maturation using the atlas and skeletal maturation of the hand-wrist. Their techniques did not require hand-wrist radiographs and could be used to roughly evaluate pubertal growth based on cephalometric radiographs. However, these techniques could not be used to evaluate growth in a detailed and objective manner, because they used an atlas. The purpose of this study was to establish a new method for objectively evaluating skeletal maturation in cephalometric radiographs. MATERIAL AND METHODS
We examined lateral cephalometric and hand-wrist radiographs from the files of the Department of Orthodontics, Tohoku University Dental Hospital, Sendai, Japan. The images in cephalometric radiographs are 1.0625 times the actual size. Group 1 consisted of 22 Japanese girls in each of 8 age groups (ages 7.0-14.9 years), for a total of 176 girls; this group was used to derive a formula for obtaining cervical vertebral bone age (Table I). Group 2 consisted of another 66 girls (ages 8.0-13.9 years, average age 11.0 ⫾ 1.57 years) and was used to determine the reliability of cervical vertebral bone age in comparison with bone age by the TW2 method with hand-wrist radiographs. On lateral cephalometric radiographs in group 1, the following cervical vertebrae were traced by pencil and measured with micrometer calipers: anterior verte-
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Fig 1. Examples of natural maturational changes in cervical vertebrae. Table I.
Composition of group 1
Age group (years) 7.0-7.9 8.0-8.9 9.0-9.9 10.0-10.9 11.0-11.9 12.0-12.9 13.0-13.9 14.0-14.9 Total
Number
Average age (years)
22 22 22 22 22 22 22 22 176
7.53 8.53 9.49 10.51 11.40 12.54 13.46 14.55 -
bral body height (AH), vertebral body height (H), posterior vertebral body height (PH), and anteroposterior vertebral body length (AP) on the third and fourth cervical vertebrae (Fig 2). The ratios of these parameters were calculated (AH/AP, H/AP, PH/AP, AH/H, H/PH, and AH/PH). A formula for obtaining cervical vertebral bone age was determined from the ratios and the chronological age using a stepwise multiple regression analysis. Bone age and cervical vertebral bone age were estimated in group 2 to confirm the validity of this formula. The correlation and difference between cervical vertebral bone age and bone age were determined, as were those between cervical vertebral bone age and chronological age. Bone age was calculated using Japanese standards (RUS: radius, ulna, and short bones)1,2 with the TW2 method.
All cephalometric radiographs were traced and measured by 1 operator (T.M.). Intraoperator error was determined by using 10 cephalometric radiographs selected randomly from group 1; these were traced and measured with micrometer calipers, and the same materials were measured again 10 days later. Statistical analysis
A paired t test was used to determine if there was a significant difference in the average errors and correlation coefficients between cervical vertebral bone age and bone age, and between cervical vertebral bone age and chronological age. All analyses were performed with Statview (SAS Institute, Cary, NY). RESULTS Operator error
The average error between the first and the second measurements for all parameters (absolute value) was 0.30 ⍞ 0.29 mm (r ⍽ 0.998, P � .001). Parameters were measured on the third and fourth cervical vertebrae (Figs 3 and 4). AH3,4, H3,4, and PH3,4 increased in an accelerated manner from 10 to 13 years of age. The ratios of these parameters were calculated. The formula for calculating cervical vertebral bone age was determined by stepwise multiple regression analysis with chronological age as a dependent variable and the ratios of these parameters as independent variables:
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Fig 2. Areas of cervical vertebral bodies measured on cephalometric radiographs. Lower lines are tangent to front and back of lower parts of cervical vertebral bodies. AH3, 4, Distance from top of front part to tangent of lower part; H3, 4, distance from top of middle part to tangent of lower part; PH3, 4, distance from top of back part to tangent of lower part; AP3,4: Anteroposterior distance at middle of cervical vertebral body.
Fig 3. Average changes in each part of third cervical vertebral body (group 1).
Fig 4. Average changes in each part of fourth cervical vertebral body (group 1).
Cervical vertebral bone age ⫽ ⫺0.20 ⫹ 6.20 ⫻ AH3/AP3 ⫹ 5.90 ⫻ AH4/AP4 ⫹ 4.74 ⫻ AH4/PH4. AH3/AP3 and AH4/AP4 increased in an accelerated manner at about 12 years of age, and AH4/PH4 continued to increase until about 14 years of age (Fig 5). Cervical vertebral bone age and bone age in group
2 were calculated to determine the reliability of cervical vertebral bone age for assessing bone age. The difference (absolute value) between cervical vertebral bone age and bone age (0.75 years) was significantly (P ⬍ .001) less than that between cervical vertebral bone age and chronological age (1.17 years) (Table II). The
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Fig 5. Average changes in parameters chosen by stepwise multiple regression analysis (group 1). Fig 6. Scattergram of cervical vertebral bone age (VA) and chronological age (CA) (group 2); ***P ⬍ .001. Table II. Differences between cervical vertebral bone age (VA) and bone age (BA) and chronological age (CA) Average difference (years) (absolute value) VA and BA VA and CA
0.75 ⫾ 0.56 1.17 ⫾ 0.86
Average ⫾ 1SD. Significant (P ⬍ .001) differences were found between VA and BA, and between VA and CA (absolute values).
Table III. Correlation between cervical vertebral bone age (VA) and bone age (BA) and chronological age (CA) Correlation coefficient VA and BA VA and CA
0.869*** 0.705***
Average ⫾ 1SD; ***P ⬍ .001. Correlation coefficients between VA and BA, and between VA and CA were also significant (P ⬍ .05).
correlation coefficient between cervical vertebral bone age and bone age (0.87) was significantly (P ⬍ .05) higher than that between cervical vertebral bone age and chronological age (0.71) (Table III, Figs 6 and 7). DISCUSSION Material selection
An abnormal cervical vertebral body due to injury, deformation, degeneration, inflammation, tumor, or
Fig 7. Scattergram of cervical vertebral bone age (VA) and bone age (BA) (group 2); ***P ⬍ .001.
other causes13 is rare, and these conditions were not seen in the materials used in this study. We examined only girls because of sex-dependent differences in growth patterns. Lamparski10 reported that boys and girls differed with regard to the timing of morphological changes in cervical vertebral bodies. In group 1, each year during puberty was represented by the same number of girls to ensure that the reliability of the formula would not vary with age. The subjects in group 2 were in the same age range as those in group 1.
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Therefore, it should be reasonable to apply the formula determined from group 1 to obtain cervical vertebral bone age in group 2. Method
Almost all previous evaluations in puberty with cervical vertebrae on cephalometric radiographs either used or referred to the atlas reported by Lamparski.10 The use of an atlas is convenient because changes in cervical vertebral bodies can be evaluated with regard to growth in the atlas. However, an atlas cannot be used to evaluate growth in an objective and detailed manner because the results can differ from operator to operator, and an atlas also cannot be used to calculate age as the TW2 method can. Thus, the method used in this study is more objective than those used in most previous studies. Cervical vertebral bone age can be easily calculated based on an analysis of cephalometric radiographs. A program to automatically calculate cervical vertebral bone age is needed to increase objectivity. We measured vertebral bodies in cervical vertebrae because various investigators11,12,14-16 have suggested a relationship between changes in cervical vertebral bodies and growth, and vertebral bodies are easy to measure. We selected the third and fourth vertebral bodies and omitted other cervical vertebrae for various reasons: the first cervical vertebra (atlas) does not show the body, the second cervical vertebra (axis) shows very little morphological change and is difficult to measure, and the fifth cervical vertebra might not appear clearly on cephalometric radiographs. We used ratios to calculate cervical vertebral bone age because this considers only the shape of cervical vertebrae and discounts their size. When deriving the formula for cervical vertebral bone age, we used chronological age instead of bone age determined from hand-wrist radiographs. There were 2 reasons for this: (1) generally, average chronological age corresponded with average bone age when there was no great deviation within groups, and (2) chronological age had little operator error compared with bone age. The measurement error averaged only 0.30 ⫾ 0.29 mm on the cephalometric radiographs, and there was a strong correlation between the first measurement and that taken 10 days later (r ⫽ 0.998, P ⬍ .001). The average difference between these measurements was as small as 0.35 mm for the fourth posterior vertebral body height (PH4), which showed the greatest measurement error. Therefore, this method was sufficiently accurate to assess skeletal development.
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Reliability of cervical vertebral bone age
As shown in Table III, the correlation coefficient between cervical vertebral bone age and bone age by the TW2 method (r ⫽ 0.869) was significantly (P ⬍ .05) higher than that between cervical vertebral bone age and chronological age (r ⫽ 0.705). Furthermore, the difference between cervical vertebral bone age and bone age (0.75 years) was significantly (P ⬍ .001) smaller than that between cervical vertebral bone age and chronological age (1.17 years). Cervical vertebral bone age is thought to more closely approximate bone age by the TW2 method rather than chronological age. Cervical vertebral bone age might reflect skeletal maturity because it can approximate bone age by the TW2 method on hand-wrist radiographs; the TW2 is considered to be the most reliable method for measuring the degree of maturity. CONCLUSIONS
The results suggest that cervical vertebral bone age on cephalometric radiographs is as reliable at estimating bone age as is the TW2 method on hand-wrist radiographs. By determining the cervical vertebral bone age, skeletal maturity can be evaluated in a detailed and objective manner with cephalometric radiographs. REFERENCES 1. Tanner JM, Whitehouse RH, Cameron N, Marshall WA, Healy MJR, Goldstein H. Assessment of skeletal maturity and prediction of adult height (TW2 method). 2nd edition. London: Academic Press; 1983. p. 22-37; 50-85. 2. Murata M, Matsuo N, Tanaka T, Ashizawa K, Otsuki F, Tatara H, et al. Atlas of standard bone maturation for Japanese – based on TW2 method. Tokyo: Kanehara Shuppan; 1993. p.141-53. 3. Sato K, Abe M, Shirato Y, Mitani H. Standard growth curve of maxilla and mandible applied to the growth prediction based on standards of bone age (Tanner-Whitehouse 2 method) for Japanese females. J Jpn Orthod Soc 1996;55:545-8. 4. Sato K, Mitani H. Evaluation of growth potentialities of maxilla and mandible by use of TW2 method and ossification events in skeletal Class III. J Jpn Orthod Soc 1998;57:1-9. 5. Sato K, Mito T, Mitani H. An accurate method of predicting mandibular growth potential based on bone maturity. Am J Orthod Dentfacial Orthop 2001;120:286-93. 6. Sato K. A study on growth timing of mandibular length, body height, hand bones and cervical vertebrae during puberty. J Jpn Orthod Soc 1987;46:517-33. 7. Taylor JR. Growth of human intervertebral discs and vertebral bodies. J Anat 1975;120:49-68. 8. Kasai T, Ikata T, Katoh S, Miyake R, Tsubo M. Growth of the cervical spine with special reference to its lordosis and mobility. Spine 1996;21:2067-73. 9. Remes VM, Heinanen MT, Kinnunen JS, Marttinen EJ. Reference values for radiological evaluation of cervical vertebral body shape and spinal canal. Pediatr Radiol 2000;30:190-5. 10. Lamparski DG. Skeletal age assessment utilizing cervical vertebrae [dissertation]. Pittsburgh: University of Pittsburgh; 1972.
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11. Hassel B, Farman AG. Skeletal maturation evaluation using cervical vertebrae. Am J Orthod Dentfacial Orthop 1995;107:58-66. 12. Garcı`a-Fernandez P, Torre H, Flores L, Rea J. The cervical vertebrae as maturational indicator. J Clin Orthod 1998;32: 221-5. 13. Bland JH. Disorders of the cervical spine. Philadelphia: W. B. Saunders; 1987. 14. O’Reilly MT, Yanniello GJ. Mandibular growth changes and
maturation of cervical vertebrae: a longitudinal cephalometric study. Angle Orthod 1988;58:179-84. 15. Kucukkeles N, Acar A, Biren S, Arun T. Comparison between cervical vertebrae and hand-wrist maturation for the assessment of skeletal maturity. J Clin Pediatr Dent 1999;24:47-52. 16. Franchi L, Baccetti T, McNamara JA Jr. Mandibular growth as related to cervical vertebral maturation and body height. Am J Orthod Dentfacial Orthop 2000;118:335-40.
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