Skeletal maturation evaluation using cervical vertebrae

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1 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.) Sexual maturation characteristics, chronologic age, dental development, height, weight, and skeletal development are some of the more common means that have been used to identify stages of growth. Determination of maturation and subsequent evaluation of growth potential during preadolescence 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 handwrist 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 formulating viable orthodontic treatment plans. The primary objective of this study was to create a method of evaluating the skeletal maturation of the orthodontic patient with the cephalometric radiograph that is routinely taken with pretreatment records. Correlations were made between cervical vertebrae maturation and the skeletal maturation of the hand-wrist. BACKGROUND Skeletal maturation refers to the degree of development of ossification in bone. Size and maturation can vary independently of each other. Skeletal 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 series 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 correlation exists between facial and statural growth. Statural growth acceleration generally precedes facial growth acceleration by 6 to 12 months. 1 2 Hand-wrist radiographic evaluation After Roentgen demonstrated his new radiographic discovery in 1895, Roland, in 1896, introduced the idea of using the comparative size and shape of the radiographic shadows of growing bones as indicators of rate of growth and maturity. 21 In the early 1900s, Pryor, = Rotch, 23 and Crampton 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 Todd 26 compiled hand-wrist data that was further 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 appearance of the adductor sesamoid has been highly correlated to peak height velocity and the start of the adolescent growth spurt '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

2 American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Farman 59 Volume 107, No. t etal maturation indicators (SMIs) using four stages of bone maturation at six anatomic sites on the hand and the wrist. 35-a7 Hagg and Taranger created a method using the hand-wrist radiograph to correlate certain maturity indicators to the pubertal growth spurt Cervical vertebrae Maturation. The first seven vertebrae in the spinal column constitute the cervical spine. The first two, the atlas and the axis, are quite unique, the third through the seventh have great similarity. 41 Maturational changes can be observed from birth to full maturity Vertebral growth takes place from the cartilagenous layer on the superior and inferior surfaces of each vertebrae Secondary ossification nuclei on the tips of the bifid spinous processes and transverse processes appear during puberty. 47'48"52'53 Secondary ossification nuclei unite with the spinous processes when vertebral growth is complete.41, Measurement. After completion of endochondral ossification, growth of the vertebral body takes place by periosteal apposition. It appears to take place only at the front and sides. 51"54 Todd and Pyle, 55 Lanier, 56 and Taylor 57 made measurements from lateral radiographs of the lower cervical vertebrae. Lamparski studied changes in size and shape of cervical vertebrae to create maturational standards for the cervical vertebrae, s8 His method was taken from Todd and Pyle, 55 Elsberg 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 displacement of vertebrae that may resemble subluxation; (2) variations of curvature that may resemble spasm and ligamentous injury; and (3) variations related to skeletal growth centers resembling fractures. 61 Ogden found variations of the anterior contour of the dens were fairly common. ~2 Bailey reported the frequent appearance of forward displacement of the second and third cervical vertebrae resembling subluxations in children under 8 years. 63 Farman et al found that the lateral cephalometric radiographic profile of the atlas could be useful in forensic identification. Disorders in children and adolescents. The orthodontist does not have to be an expert in cervical vertebrae abnormalities, but he must be aware of normal anatomy of the cervical spine on the lateral cephalogram. Many abnormalities of the cervical spine do not manifest themselves symptomatically until adolescence or young adulthood, and the orthodontist has the opportunity to detect some of these abnormalities. If the progressively degenerative defects can be discerned early, severity of consequences can be diminished. Some anomalies seen in the cervical spines of children and adolescents are fractures, infections, polyarthritis, ankylosis, and ankylosing spondylitis. 46'67 Posterior arch defects, odontoid 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 included 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 determine 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 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 radiation 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 vertebrae tracings were paired with their respective handwrist radiographs that had been grouped by SMI categories. These tracings were photocopied. The photocopies of the vertebral tracings were evaluated to see whether changes in shape and dimension of the vertebrae could

3 60 Hassel and Farman American Journal of Orthodontics and Dentofacial Orthopedics January INITIATION ACCELERATION TRANSITION,,,,,,,,, DECELERATION MATURATION COMPLETION 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 evaluated by the same two independent evaluators and B.H. to determine interoperator and intraoperator error. Cervical 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 evaluated by B.H. who evaluated the same radiographs 3 weeks later. RESULTS Photocopies of the cervical vertebrae tracings introduced in the methods section of this article were sequentially segregated by SMI grouping. Six categories of cervical vertebrae skeletal maturation 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 cephalometric radiographs for each CVMI category. Category 1 was called INITIATION. This corresponded 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 vertebrae were wedge shaped, and the superior vertebral borders were tapered from posterior to anterior (Fig. 2). Category 2 was called ACCELERATION. This corresponded to a combination of SMI 3 and 4. Growth 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 corresponded to a combination of SMI 5 and 6. Adolescent growth was still accelerating at this stage toward peak height velocity, with 25% to 65% of adolescent growth expected26 Distinct concavities were seen in the inferior borders of C2 and C3. A concavity was beginning to develop in the inferior 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 decelerate dramatically at this stage, with 10% to 25% of adolescent growth expected26 Distinct concavities were seen in

4 American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Farman 61 Volume 107, No. 1 Fig. 2. CVMI 1: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using Fig. 3. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using the inferior borders of C2, C3, and C4. The vertebral 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 maturation of the vertebrae took place during this stage, with 5% to 10% of adolescent growth expected. 36 More accentuated 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. Growth 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 greater in vertical dimension than in horizontal dimension (Fig. 7). Interoperator error Evaluator A agreed with the SMI determinations of B.H. in 18 of the 20 cases. Both discrepancies were within one SMI category of that found by the author (r 2 = 0.99, p < 0.001). Evaluator B agreed 16 out of 20 times. All four

5 62 Hassel and Farman American Journal of Orthodontics and Dentofacial Orthopedics January 1995 Table I. Cervical vertebrae maturation indicators 1. Initiation Very significant amount of adolescent growth expected C2, C3, and C4 inferior vertebral body borders are flat Superior vertebral borders are tapered posterior to anterior 2. Acceleration Significant amount of adolescent growth expected Concavities developing in lower borders of C2 and C3 Lower border of C4 vertebral body is flat C3 and C4 are more rectangular in shape 3. Transition Moderate amount of adolescent growth expected Distinct concavities in lower borders of C2 and C3 C4 developing concavity in lower border of body C3 and C4 are rectangular in shape 4. Deceleration Small amount of adolescent 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 adolescent growth expected Accentuated concavities of inferior vertebral body borders of C2, C3, and C4 C3 and C4 are square in shape 6. Completion Adolescent growth is completed Deep concavities are present for inferior vertebral body borders of C2, C3, and C4 C3 and C4 heights are greater than widths differences in opinion were within one SMI category. Borderline cases were interpreted one category higher by evaluator B than by B.H. (r 2 = 0.99, p < 0.001). The same 20 cephalometric radiographs evaluated by B.H. to determine CVMI categories were evaluated by the same two independent evaluators. Evaluators A and B were each given 10 minutes instruction by B.H. on CVMI determination criteria. Fig. 1 was given to each evaluator for guidance Significant agreement was seen between evaluators A and B (r 2 = 0.85, p < 0.001; /,2 = 0.90, p > 0.001). When SMI categories and CVMI categories determined 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 determined from 20 hand-wrist radiographs These same radiographs were reevaluated 3 weeks later by the same person and the SMI categories were again assigned Nineteen of 20 SMI determinations were the same in the second evaluation as they were in the first (r 2 = 1.00, p < 0 001) Lateral cephalometric 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 Nineteen of 20 CVMI category determinations coincided with those determined 3 weeks previously (r 2 = 1.00, p < 0.001). DISCUSSION The purpose of this investigation was to provide the orthodontist with an additional tool to help determine growth potential in the adolescent patient. This was to be accomplished by using anatomic changes of the cervical vertebrae observed on the lateral cephalometric radiograph to determine skeletal maturity. By using a routinely taken diagnostic radiograph, the orthodontist would have a reliable diagnostic tool to aid in formulating treatment options. This study combined the observations of the changes in the hand-wrist and the changes in the cervical vertebrae during skeletal maturation The observations of Lamparski s8'67 were confirmed, excepting the lack of a narrowing of intervertebral space with increased age. The shapes of the cervical vertebrae were seen to differ at each level of skeletal development. This provided a means with

6 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 Fig. 5. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using which to determine the skeletal maturity of a person 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 rectangular, 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 became 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 maturation index) groupings were condensed into six CVMI (cervical vertebrae maturation index) categories. 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).

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 Fig. 7. CVMI 2: A. Typical hand-wrist radiograph. B. Typical cervical vertebrae appearance using The evaluation of intraoperator error in SMI determination suggested that B.H. varied insignificantly in his interpretation from one time to the next. The criteria used for SMI determination appeared 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. significantly in choosing CVMI classification. The instances 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

8 American Journal of Orthodontics and Dentofacial Orthopedics Hassel and Farman 65 Volume I07, No. 1 variability seen in interpretation of borderline cases. It must be remembered that skeletal maturation is a continuous process. Skeletal maturity indicators 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 observations by the orthodontist. One diagnostic test should not be relied on too heavily. The growth factor is a critical variable in orthodontic treatment. A treatment plan can vary from orthognathic surgery to extraction of teeth to nonextraction of teeth, depending 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 factored into anticipated treatment. A special word of thanks is due to Dr. John Yancey for guidance on the statistical analyses employed for this study. REFERENCES 1. Tanner JM. Growth at adolescence an introduction. In: Carlson D, Ribbens K, eds. Monograph 20, Craniofacial Growth Series. Ann Arbor: Center for Human Growth and Development, University of Michigan, Scammon R. The first seriatim study of human growth. Am J Phys Anthropol 1927;10: Tanner JM. A history of the study of human growth. Cambridge: Cambridge University Press, Falkner F, Tanner JM. Human growth. Vols 1-3. New York: Plenum Press, Poznanski A. The hand in radiologic diagnosis. Vol. 1.2nd ed. Philadelphia: WB Saunders, Greulich WW, Pyle SI. 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9 66 Hassel and Farrnan American Journal of Orthodontics and Dentofacial Orthopedics January 1995 tion; a clinically oriented method based on hand wrist films. Angle Orthod 1982;52: Fishman LS. Maturation patterns and prediction during adolescence. Angle Orthod 1987;57: Hagg U, Taranger J. Skeletal stages of the hand and wrist as indicators of the pubertal growth spurt. Acta Odont Scand 1980;38: Hagg U, Taranger J. Maturation indicators and the pubertal growth spurt. AM J ORTHOD 1982;82: Taranger J, Hagg U. The timing and duration of the adolescent growth spurt. Acta Odontol Scand 1980;38: Rothman RH, Simeone FA. The spine. Vol. 1. Philadelphia: WB Saunders, Gray H, Clemente CD, ed. Anatomy of the human body, 30th ed. Philadelphia: Lea & Febiger, 1985: Epstein B. A radiological text and atlas. Philadelphia: Lea & Febiger, Gooding CA, Neuhauser EB. Growth and development of the vertebral body in the presence of and absence of normal stress. Am J Roentgenol 1965;93: Bick E, Copel J. Longitudinal growth of the human vertebrae J. Bone Joint Surg (Am) 1950;32A: Bland JH. Disorders of the cervical spine. Philadelphia: WB Saunders, Bradford DS. The pediatric spine. New York: Theime, Bradford DS. Moe's text of scoliosis and other spinal deformities. 2nd ed. Philadelphia: WB Saunders, Ghosh P. The biology of the intervertebral disc. Orlando: CRC Press, Hadley LA. The spine-radiographic studies-development and the cervical spine. Springfield: Charles C. Thomas, Knutsson F. Growth and differentiation of the postnatal vertebrae. Acta Radiol 1961;55: Riamondi AJ. The pediatric spine, vol 1. New York: Springer and Verlag, Sherk H, Parke W. The cervical spine. Cervical Spine Research Society. Philadelphia: JB Lippincott, Wholey M, Bruwer M, Hiller L. The lateral roentgenogram of the neck. Radiology 1958;71: Todd T, Pyle SI. Quantitative study of the vertebral column. Am J Phys Anthropol 1928;12: Lanier R. Presacral vertebrae of white and negro males. Am J Phys Anthropol 1939;25: Taylor JR. Growth of human intervertebral discs and vertebral bodies. J Anat 1975;120: Lamparski D. Skeletal age assessment utilizing cervical vertebrae. [Thesis.] Pittsburgh: University of Pittsburgh, Elsberg CA, Duke CG. The diagnosis and localization of tumors of the spinal cord by means of measurement made of the x-ray films of the vertebrae and the correlation of clinical and x-ray findings. Bull Neuro Inst 1934;3: Hinck V, Hopkins C, Savara B. Sagittal diameter of the cervical spine in children. Radiology 1962;70: Cattell H, Filtzer D. Pseudoluxation and other normal variations in the cervical spine in children. J Bone Joint Surg 1965;47A: Ogden JA, Murphy MJ, Southwick WO, Ogden A. Radiology of post natal skeletal development-c1-c2 interrelationships. Skeletal Radiol 1986;15: Bailey DK. The normal cervical spine in infants and children. Radiology 1952;59: Farman A, Haskell B, Hunter N. The first cervical vertebrae, a plausible parameter for use in forensic identification. J Forensic Odonto-Stom 1984;2: Farman A, Escobar V. Radiographic appearance of the cervical vertebrae in normal and abnormal development. Br J Oral Surg 1982;20: Farman AG, Nortj6 CJ, Joubert J de V. Radiographic profile of the first cervical vertebrae. J Anat 1979;128: Kein HA. The adolescent spine. New York: Springer-Verlag, Broadbent BR Sr, Broadbent BH Jr. Bolton standards of dentofacial developmental growth. St. Louis: CV Mosby, Reprint requests to: Dr. Allan G. Farman School of Dentistry University of Louisville Louisville, KY 40292

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