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ORIGINAL ARTICLE

Phases of the dentition for the assessment of skeletal maturity: A diagnostic performance study
Lorenzo Franchi,a Tiziano Baccetti,a Laura De Toffol,b Antonella Polimeni,c and Paola Cozzad Florence and Rome, Italy Introduction: The aim of this study was to analyze the relationship between the circumpubertal phases of the dentition (early mixed, intermediate mixed, late mixed, early permanent) and skeletal maturity as assessed by means of the cervical vertebral maturation (CVM) method. Methods: The sample of 1000 subjects included 250 (125 boys, 125 girls) in each of the 4 dentition phases. Individual skeletal maturity was determined by using the CVM method. The relationship between the skeletal maturity (stages in CVM) and the phases of the dentition was evaluated statistically by means of indicators of diagnostic test performance. Results: Prepubertal stage 1 (CS1) was the variable diagnosed in the early mixed and intermediate mixed dentitions; pubertal stage 3 (CS3) was the variable diagnosed in the late mixed and early permanent dentitions. Conclusions: The early mixed dentition phase showed a strong diagnostic value for the identication of prepubertal skeletal maturity (CS1), whereas the intermediate mixed dentition phase had a low diagnostic value for the same prepubertal stage. Neither the late mixed dentition nor the early permanent dentition appeared to be a valid indicator for the onset of the pubertal growth spurt. (Am J Orthod Dentofacial Orthop 2008;133:395-400)

iming is a fundamental part of treatment planning in orthodontics, with special regard to dentofacial orthopedics. Starting treatment in a growing patient at the right time has demonstrated signicant favorable effects in the correction of disharmonies in the sagittal, transverse, and vertical planes.1-3 Optimal timing for treatment is different in the various malocclusions. Recently, it was highlighted that treatment protocols aimed to enhance or restrain maxillary growth take advantage of treatment performed before the adolescent growth spurt, whereas treatment regimens aimed to enhance or restrain mandibular growth produce greater effects when the pubertal growth spurt is included in the treatment interval.3 The appraisal of a patients skeletal maturity is a key factor for the application of the concept of treata

Assistant professor, Department of Orthodontics, University of Florence, Florence, Italy; Thomas M. Graber Visiting Scholar, Department of Orthodontics and Pediatric Dentistry, School of Dentistry, University of Michigan, Ann Arbor. b Fellow, Department of Orthodontics, University of Rome Tor Vergata, Rome, Italy. c Professor and head, Department of Pediatric Dentistry, University of Rome La Sapienza, Rome, Italy. d Professor and head, Department of Orthodontics, University of Rome Tor Vergata, Rome, Italy. Reprint requests to: Lorenzo Franchi, Universit degli Studi di Firenze, Via del Ponte di Mezzo, 46-48, 50127, Firenze, Italy; e-mail, l.franchi@odonto.uni.it. Submitted, December 2005; revised and accepted, February 2006. 0889-5406/$34.00 Copyright 2008 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2006.02.040

ment timing to clinical practice. Several biological indicators of skeletal maturity have been used in many studies in orthodontics: increases in statural height,4-10 hand and wrist maturation,11-17 cervical vertebral maturation (CVM).18-22 In addition to these methods, the relationship between the development of the dentition and skeletal maturation has been investigated. The studies refer mainly to the correlations between the formation of teeth (with special regard to the mandibular permanent canines and second molars) and the onset of the pubertal growth spurt.23-29 The results show much variability in the concordance between stages of calcication and eruption of teeth and skeletal maturation. Correlations of tooth development with the peak in mandibular growth are not reported in the literature, whereas those with the peak in statural height are generally weak (r 0.03-0.42).28,29 On the other hand, the phases of the dentition (deciduous, early and late mixed, permanent) have often been used in investigations of the different outcomes of treatment protocols at earlier vs later stages of development. The effects of Class III treatment have been analyzed in the deciduous vs the mixed dentition30-33 and in the early vs the late mixed dentition.34-36 Class II correction in the early mixed dentition has been confronted with outcomes of treatment of malocclusion in the late mixed dentition.37,38 No study,
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Fig 1. Schematic representation of the 6 stages of the CVM method. Reprinted from Baccetti et al3 with permission from Elsevier.

however, has described the relationship between the phases of the dentition and skeletal maturation, despite the role of skeletal maturity in treatment timing. This information is needed both as an aid in clinical practice and for the interpretation of the results of investigations on timing of orthodontic treatment that use the dentition stages as a categorization factor. Our aim in this investigation was to analyze the diagnostic performance of the circumpubertal phases of the dentition (early mixed, intermediate mixed, late mixed, early permanent39,40) with respect to individual skeletal maturity as assessed with the CVM method.3
MATERIAL AND METHODS

deciduous teeth in the buccal region (deciduous canine, rst molar, and second molar). 3. Late mixed dentition: shedding of the deciduous canines and molars, eruption of the permanent canines and premolars. 4. Early permanent dentition: presence of all permanent teeth (possible presence of second molars; absence of third molars). Mean ages were 7.6 1.1 years for the early mixed dentition group, 8.9 1.2 years for the intermediate mixed dentition group, 10.1 1.1 years for the late mixed dentition, and 12.8 1.2 years for the early mixed dentition group.
Appraisal of skeletal maturity

This large cross-sectional investigation included 1000 subjects (500 boys, 500 girls) from a parent sample of 1600 subjects from the departments of orthodontics of the universities of Florence and Rome Tor Vergata. The exclusion criteria consisted of full deciduous dentition, adult permanent dentition, craniofacial anomalies, cleft lip and palate, extensive caries, early loss of deciduous teeth due to trauma or caries, supernumerary teeth, tooth agenesis, and other tooth anomalies. Dental casts, panoramic radiographs, and lateral cephalograms of good quality were available for all selected subjects. The sample of 1000 subjects comprised 250 subjects (125 boys, 125 girls) in each of the 4 dentition phases, which were appraised by analyzing the dental casts and the panoramic radiographs, and categorized according to the following denitions.39,40 1. Early mixed dentition: shedding of the deciduous incisors, eruption of the rst permanent molars and permanent incisors. 2. Intermediate mixed dentition: permanent incisors and rst molars fully erupted, presence of the

All subjects were analyzed with a reliable method for the assessment of skeletal maturity. The recently improved version of the CVM method was used on lateral cephalograms.3 The 6 stages of CVM are illustrated in the Figure 1 and dened as follows. Cervical stage 1 (CS1). The lower borders of the 3 vertebrae are at. The bodies of both the third and fourth cervical vertebrae (C3 and C4) are trapezoidshaped (the superior border of the vertebral body is tapered from posterior to anterior). The peak in mandibular growth will occur not earlier than 2 years after this stage. Cervical stage 2 (CS2). The lower border of the second cervical vertebra (C2) is concave. The bodies of both C3 and C4 are still trapezoid-shaped. The peak in mandibular growth will occur not earlier than 1 year after this stage. Cervical stage 3 (CS3). Concavities at the lower borders of both C2 and C3 are present. The bodies of C3 and C4 can be either trapezoid or rectangular

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Table I.

Prevalence of the CVM stages in the various dentition phases


CS1 CS2 9 (3.6%) 71 (28.4%) 61 (24.4%) 47 (18.8%) CS3 0 (0%) 10 (4%) 90 (36%) 76 (30.4%) CS4 0 (0%) 0 (0%) 21 (8.4%) 74 (29.6%) CS5 0 (0%) 0 (0%) 0 (0%) 27 (10.8%) CS6 0 (0%) 0 (0%) 0 (0%) 8 (3.2%)

Early mixed (n 250) Intermediate mixed (n 250) Late mixed (n 250) Early permanent (n 250)

241 (96.4%) 169 (67.6%) 78 (31.2%) 18 (7.2%)

horizontal. The peak in mandibular growth will occur within 1 year after this stage. Cervical stage 4 (CS4). Concavities at the lower borders of C2, C3, and C4 now are present. The bodies of both C3 and C4 are rectangular horizontal. The peak in mandibular growth occurred 1 or 2 years before this stage. Cervical stage 5 (CS5). The concavities at the lower borders of C2, C3, and C4 still are present. At least 1 of the bodies of C3 and C4 is square. If not square, the body of the other cervical vertebra still is rectangular horizontal. The peak in mandibular growth occurred not later than 1 year before this stage. Cervical stage 6 (CS6). The concavities at the lower borders of C2, C3, and C4 still are evident. At least 1 of the bodies of C3 and C4 is rectangular vertical. If not rectangular vertical, the body of the other cervical vertebra is square. The peak in mandibular growth occurred not later than 2 years before this stage.
Statistical analysis

sensitivity and the specicity of the test and provides a direct estimate of how much a test result will change the odds of having a condition. The likelihood ratio for a positive result indicates how much the probability of the condition (specic stage in skeletal maturation) increases when a test is positive (specic phase of the dentition).41 A likelihood ratio greater than 1 indicates that the test result is associated with the disease, whereas a result of 1 means absence of any diagnostic performance. The further the likelihood ratios are from 1, the stronger the evidence for the presence or absence of the condition (eg, a likelihood ratio of 2 means minimal strength in the diagnostic performance of the testing variable or method); likelihood ratios above 10 are considered to provide strong evidence to rule in diagnosis in most circumstances.42 Variables to be diagnosed (conditions) were dened on the basis of the most prevalent CVM stage in the different phases of the dentition.
RESULTS

The clinical records of the 1000 subjects were analyzed as follows. An expert examiner (T.B.) appraised the phases of the dentition on the dental casts and the panoramic x-rays, and another examiner (L.F.) appraised the CVM stages on the lateral cephalograms. The examiner who evaluated the phases of the dentition was blind as to CVM stages and vice versa. Percent agreement and kappa statistics were calculated for the evaluation of intraexaminer agreement. For the appraisal of the CVM stages, agreement was 94.8% with a kappa of 0.90; for the appraisal of the phases of the dentition, agreement was 98.8% with a kappa of 0.98. The prevalence of the CVM stages in the various phases of the dentition was calculated. The relationship between the skeletal maturity stages in the CVM method and the phases of the dentition was evaluated with measures of diagnostic performance41: sensitivity, specicity, positive predictive value, and positive likelihood ratio. The positive predictive value of a test is the probability that the patient has the condition (specic stage in skeletal maturation) when restricted to patients who test positive (specic phase of the dentition).41 The likelihood ratio incorporates both the

The prevalence of the CVM stages in the various phases of the dentition is given in Table I. The diagnostic tests with the corresponding 95% condence intervals are shown in Table II. The early mixed dentition phase showed high values in the diagnostic tests for the prepubertal CS1 in skeletal maturation (positive predictive value and positive likelihood ratio), whereas the intermediate mixed dentition phase had low diagnostic scores for that stage. This outcome indicates that a subject who tests positive (ie, a subject in the early mixed dentition) has a high probability to exhibit the condition that needs to be diagnosed (CS1) (positive likelihood ratio 26.14), whereas the probability of CS1 stage is low if the subject is in the intermediate mixed dentition (positive likelihood ratio 2.04). The low scores for the positive predictive value and the positive likelihood ratio for both the late mixed and early permanent dentitions indicate that these phases perform poorly in the diagnosis of the onset of the pubertal growth spurt (CS3). In other words, a subject who tests positive (ie, a subject in the late mixed or early permanent dentition) has a low probability to have

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Table II.

Diagnostic performance of the dentition phases in determining skeletal maturity


Phase of the dentition Early mixed Variable diagnosed: CS1 Intermediate mixed Variable diagnosed: CS1 Value 33.4% 83.6% 67.6% 2.04 (95% CI) (30.835.8) (81.086.1) (62.472.5) (1.622.58) Late mixed Variable diagnosed: CS3 Value 51.1% 80.6% 36% 2.63 (95% CI) (44.757.4) (79.281.9) (31.540.4) (2.153.18) Early permanent Variable diagnosed: CS3 Value 43.2% 78.9% 30.4% 2.04 (95% CI) (36.949.6) (77.580.2) (2634.9) (1.642.51)

Diagnostic tests Sensitivity Specicity Positive predictive value Positive likelihood ratio

Value 47.6% 98.2% 96.4% 26.14

(95% CI) (46.248.5) (96.799.0) (93.598.1) (13.9649.83)

the condition that needs to be diagnosed (CS3) (positive likelihood ratios 2.63 and 2.04 for the late mixed and early permanent dentitions, respectively).
DISCUSSION

Little is known about the relationship between the onset of puberty and dental maturation. Some studies showed that correlations between tooth mineralization and other parameters of physical development are generally low, whereas there is little more than slight covariation between tooth eruption and the adolescent growth spurt.23-29 Since no previous data are available with regard to the correspondence between dentition phases and skeletal maturation, we analyzed the relationship between the circumpubertal phases of the dentition and skeletal maturity determined with a reliable indicator (the CVM method).3 The dentition phases include 4 developmental stages identied on the basis of classical denitions by Bjrk et al39 and van der Linden and Duterloo.40 The early mixed dentition corresponds with shedding of the deciduous incisors and eruption of the rst permanent molars and permanent incisors (rst transitional period of the dentition, according to van der Linden and Duterloo40). In the intermediate mixed dentition, the permanent incisors and rst molars are fully erupted, and deciduous teeth (canine, rst molar, and second molar) are present in the buccal region (intertransitional period of the dentition, according to van der Linden and Duterloo40). The late mixed dentition is characterized by shedding of the deciduous canines and molars and eruption of the permanent canines and premolars (second transitional period of the dentition, according to van der Linden and Duterloo40). In the early permanent dentition, all teeth in the dental arches are permanent (possible presence of second molars, absence of third molars). Although phases of the dentition have often been used in investigations of treatment timing in dentofacial orthopedics,30-38 the literature lacks information about the correspondence between dentition phases and skeletal maturity in individual patients.

Our ndings demonstrate the usefulness of the early mixed dentition phases for the identication of CS1, as shown by the high scores of diagnostic performance measures. In other terms, the developmental interval characterized by shedding of the deciduous incisors and eruption of the permanent incisors and the rst molars is a powerful indicator of the prepubertal stage of skeletal maturity. Previous data suggest that this phase might be the optimal time to start treatment protocols aimed at altering orthopedically the maxilla (rapid maxillary expansion, facemask treatment).3,21,34-36 Although showing a low diagnostic value for the specic CS1, the intermediate mixed dentition still showed that 96% of the subjects were at a prepubertal stage of skeletal maturity (67.6% at CS1, 28.4% at CS2). On the other hand, the phases of the dentition do not appear to be useful for determining the onset of the pubertal growth spurt (CS3). When permanent canines or premolars are erupting (late mixed dentition), one third of the subjects are at the onset of their pubertal growth spurt, and about half still exhibit prepubertal stage of skeletal maturity. Some 8.4%show postpubertal stage of skeletal maturity (CS4). Therefore, the diagnostic performance of the late mixed dentition in the identication of the onset of the pubertal growth spurt is low. The early permanent dentition phase is not a valid indicator of peak skeletal maturity, either. About 30% of growing subjects with early display of full permanent dentition (except the third molars) can show either the onset of the pubertal growth spurt (CS3) or a postpeak stage of skeletal maturity (CS4). The relationship between early permanent dentition and skeletal maturity is so weak that 26% of the subjects are still at the prepubertal stage of skeletal maturity, whereas 14% of the subjects are already in CS5 or CS6. Our results indicate that, when confronted with a reliable indicator of skeletal maturity (such as the CVM method), the dentition phases perform poorly in the detection of the onset of the pubertal peak in skeletal growth, which is a fundamental part of treatment planning for protocols aimed at enhancing mandibular

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growth.3-6,8-10,19 This study also provided interesting data about the variability of chronologic age with respect to the onset of the pubertal peak in skeletal maturation. The age range at CS3 was from 8 years to 14 years 6 months. This wide variability emphasizes once again that chronologic age has little value for the appraisal of skeletal maturation, especially for the identication of the pubertal growth spurt and, consequently, for the evaluation of treatment timing in dentofacial orthopedics.43
CONCLUSIONS

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This study on the diagnostic performance of the phases of the dentition as indicators of individual skeletal maturity showed that the early mixed dentition phase shows strong diagnostic value for the identication of prepubertal skeletal maturity (CS1), whereas the intermediate mixed dentition phase has poor diagnostic value for that stage. Neither the late mixed dentition nor the early permanent dentition is a valid indicator for the onset of the pubertal growth spurt (CS3).
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