Introduction
The aims of this study were to compare the radiographic development of permanent teeth in a group of children affected by dental agenesis with an unaffected control group and to determine the effects of confounding factors including the severity of the dental agenesis, age, sex, ethnicity, and the number of stages used to estimate dental age.
Methods
A single-center retrospective cross-sectional study of dental panoramic tomographs was undertaken between July 2007 and April 2008 in a postgraduate teaching school. A total of 139 patients (aged 9-18 years) were recruited from the orthodontic clinic on the basis of predetermined inclusion and exclusion criteria to either a dental agenesis group or a control group. Dental panoramic tomograms were assessed, and the stages of development of the permanent teeth in the left maxillary and left mandibular regions were scored by using the 12 stages of Haavikko and the 8 stages of Demirjian and Goldstein. For each tooth scored, the mean dental age and standard error were determined by using the dental age assessment method, and an estimated dental age for each subject was derived by using the weighted average method.
Results
A statistically significant delay in dental age was found in the patients with dental agenesis compared with the control group. The dental age assessment method of Haavikko showed a delay of 1.20 years (SD, 1.74), and the method of Demirjian and Goldstein showed a delay of 1.64 years (SD, 1.75). It was also observed that older patients with dental agenesis had greater delays in tooth formation ( P <0.001). With the Haavikko method, for every year of chronologic age, the delay in dental age increased by 0.53 year; with the Demirjian and Goldstein method, the delay increased by 0.48 year. A significant association was seen between the severity of dental agenesis and the delay in dental age ( P <0.01). With both methods, for each additional developmentally absent tooth, the dental age was delayed by 0.13 year (lower confidence interval, −0.22; upper confidence interval, 0.35). There was no evidence that sex or ethnicity has an effect on the delay in dental age in patients with dental agenesis.
Conclusions
The development of permanent teeth in children with dental agenesis is delayed when compared with a matched control group. The severity of dental agenesis affected the magnitude of the delay ( P <0.01). This delay has implications in orthodontic treatment planning and in the estimation of age for legal, immigration, archaeological, and forensic purposes.
Dental agenesis describes the developmental absence of at least 1 deciduous or permanent tooth, excluding the third molars. Alternative terms used in the literature include hypodontia and oligodontia. Recent advances in the understanding of the genetics of tooth development and dental agenesis have suggested that specific genes including PAX9 and MSX1 are associated with characteristic patterns of dental agenesis, and these genetic factors can also cause delayed dental development of the remaining teeth. Dentofacial anomalies associated with agenesis include microdontia, impaction or transposition, taurodontism, reduced alveolar bone volume, and skeletal jaw malrelationships. A few studies have investigated the link between dental agenesis and delayed dental development, although the literature contains no consensus concerning the latter phenomenon.
Bailit et al found no significant difference in the eruption of the teeth in 177 patients with dental agenesis compared with a control group of 4000 Japanese children. On the other hand, Garn et al described a delay in tooth formation of premolars and molars in 22 subjects with dental agenesis compared with a control group of 126 patients, although the delay was not quantified. Rune and Sarnäs evaluated tooth formation using the method of Haavikko in 42 boys and 43 girls with severe dental agenesis and reported mean delays of 1.8 and 2.0 years for boys and girls, respectively.
Odagami et al assessed the dental age of 177 Japanese children (aged 5-10 years) with dental agenesis and reported an insignificant delay of a few months that was not statistically significantly different between the dental and chronologic ages. They also found that, as the number of developmentally missing permanent teeth increased, the differences between the dental and chronologic ages of the dental agenesis group also increased.
Using the method of Demirjian and Goldstein, Lozada and Infante assessed the dental maturity of 56 children with dental agenesis, finding delays of 0.7 year for boys and 1 year for girls. They also reported that, although there was a delay of a few months in tooth formation in patients with dental agenesis, this delay was not statistically significant.
Using the method of Haavikko, Uslenghi et al conducted a retrospective cross-sectional study of dental panoramic tomographs of 135 children (mean age, 10.38 years; range, 3.08-15.02 years) with agenesis of at least 1 permanent tooth and an equal number of controls, finding that there was a statistically significant difference between the 2 groups, with the dental agenesis group demonstrating a mean delay in dental development of 1.51 years (SD, 1.37 years). The delay was greater for teeth adjacent to the site of agenesis and in subjects with increased severity of dental agenesis. The authors did not compare the sexes separately.
It is difficult to draw conclusions from comparisons with previous studies because different methods of assessing dental developmental age were used. Methodologic differences might also account for disparate results. Racial variations of the populations studied can also affect the results. Variations in the age of the population studied also need to be considered. The methods of Haavikko and Demirjian and Goldstein were based on European subjects, and they did not test the accuracy and precision of their methods on separate samples.
A greater understanding of dental development in patients with dental agenesis is important for orthodontic treatment planning and for providing a reference for age assessment specific to patients with dental agenesis when birth data are lacking or disputed for forensic purposes.
There have been several approaches relating tooth development to the prediction of chronologic age. They can be based on dental emergence or on the stages of tooth formation observed on radiographs. The disadvantages of the tooth-emergence methods are that local factors such as crowding or early loss of deciduous teeth influence the timing of tooth eruption and the difficulty in recording the exact time of tooth eruption. As a consequence, radiographic assessment of the stages of tooth development has gained popularity for determining age. Two distinct methods based on the stages of tooth development are in widespread use, having been developed by Haavikko and Demirjian and Goldstein. The first method divides dental development into 12 stages, and the second classifies tooth development into 8 stages. Recently, a dental age assessment method was devised; it uses the staging systems of the Haavikko and Demirjian and Goldstein and shows promising results for age determination from the dentition.
In this study, teeth were assessed by using both the 12 stages described by Haavikko and the 8 stages of Demirjian and Goldstein because it was hypothesized that using different numbers of stages might influence the accuracy of dental age estimation. The dental age assessment method has been tested on separate study samples and described in the literature.
The aims of this study were to (1) investigate the radiographic development of permanent teeth in a group of children affected by dental agenesis, (2) determine whether the severity (mild, moderate, or severe) of the dental agenesis has an effect on dental development, (3) determine whether using 12 or 8 stages improves the accuracy of dental age estimation, and (4) determine the effects of these confounding factors: age, sex, and ethnicity.
The null hypotheses for this study were that (1) there is no significant difference in the development of permanent teeth in children with dental agenesis compared with a control group, and (2) there is no difference in dental age with 12 or 8 stages.
Material and methods
This study had the approval of the research and ethics committee (reference 03/E023) of University College Hospitals National Health Service Trust. The design was a retrospective cross-sectional study of dental panoramic tomograms. These were good-quality diagnostic radiographs taken in the orthodontic department of University College London Hospitals Eastman Dental Hospital during routine care and provided material for assessment of the developmental stages of all permanent teeth.
The criteria for selection of the dental agenesis group were (1) patients aged 9 to 18 years with confirmed dental agenesis, who required panoramic radiographs for treatment planning; (2) patients and parents who gave informed consent to participate in the study; and (3) patients in good health with no medical problems or syndromes.
A decision was made to limit the study to include only patients aged 9 to 18 years (age at the day of the x-ray) for the following reasons.
- 1.
A patient cannot be fully diagnosed with dental agenesis and the true extent confirmed until the age of at least 9 years. By this time, all tooth buds, including second premolars, should have appeared on the radiograph.
- 2.
It was not necessary to await the formation of the third molars because these teeth were not included in the study.
There was a similar age distribution in the control group and the dental agenesis groups.
The dental agenesis patients were divided into 3 categories by using previously accepted severity indicators (mild agenesis, 1-2 absent teeth; moderate agenesis, 3-5 absent teeth; severe agenesis, 6 or more absent teeth).
The criteria for selection of the control group were the same as those for the agenesis groups, except for radiographic confirmation of complete dentition, excluding the third molars.
The sample size was calculated by using data from the first 33 dental agenesis patients and 10 control patients recruited. A sample size calculation was performed by using nQuery Advisor software (version 5.0; Statistical Solutions, Saugus, Me). For a t test (α = 0.05) to have 80% power to detect a difference in means of 1 year, a minimum sample size of 30 patients in each of the 4 groups (control and mild, moderate, and severe dental agenesis) was required.
One hundred thirty-nine panoramic radiographs were assessed for this study. The radiographs were taken by experienced radiographers using a Proline 2002 CC machine (Planmeca Oy, Helsinki, Finland), with a variable anode voltage of 64 to 66 kV, an anodic current of 0.4 to 0.8 mA, and an exposure time of 15 to 18 seconds. Agfa film (Agfa, Mortsel, Belgium), size 15 × 30 cm, was used with a regular intensifying screen (Kodak, Rochester, NY); the films were developed in a Curix 260 automated developing machine (Agfa). These radiographs had a magnification factor of 1.45 times.
The criteria for acceptance of the radiographs for use in the study were that: (1) all the teeth in the maxillary and mandibular left buccal segments of the mouth were visible, and (2) the images of the teeth were sufficiently clear to permit accurate assessment of the stage of crown and root development. Radiographs with distorted or poor-quality images were excluded from the study.
The selected radiographs were converted into digital images for analysis and storage. This was achieved by placing the radiograph on a viewing box in a vertical orientation and taking a photographic image with a digital camera (EOS 400; Canon, Tokyo, Japan) mounted on a tripod. The camera was programmed at ISO 100 to 200 in automatic mode, whereby the camera automatically adjusted the shutter speed and the aperture according to the amount of light available. The digital images were downloaded and stored as jpeg files by using Office Picture Manage software (version 2007; Microsoft, Redmond, Wash). The software permitted magnification of the images for better visualization of the stages of development of the permanent teeth according to the 2 methods described by Haavikko and Demirjian and Goldstein.
The principal investigator (E.R.M.) underwent extensive training in the use of the tooth development assessment scales and was calibrated to a coinvestigator (S.P.), an experienced operator in the field. Twenty panoramic radiographs were randomly chosen, examined, and rated by both the principal investigator and the calibrator after a 3-week interval to test for intraexaminer and interexaminer reproducibility and repeatability. Cohen’s kappa statistic was used between the 2 assessors to test the reproducibility of the stages described by Haavikko and Demirjian and Goldstein. The main assessments of all radiographs were carried out by the principal investigator.
For the 139 panoramic radiographs, all permanent maxillary and mandibular teeth on the left side of the radiograph (except for the third molars) were assessed, and the stages of development of these teeth in these regions were recorded according to the 12 stages of Haavikko and the 8 stages of Demirjian and Goldstein. (Only the staging systems were used, not the methodology to determine dental age).
For all stages of all discernible teeth, except Apex Closed or H, a mean age of attainment was derived from the dental age assessment database. For each subject, the mean and standard error of the age of attainment of each tooth were calculated by using the weighted average method to estimate the dental age. Teeth that had completed their development—ie, stage Apex Closed or H—were excluded, since it was not possible to ascertain when this stage had been reached.
The dental age assessment method was developed by Roberts et al based on a multi-ethnic population of 1547 healthy subjects in London with chronologic ages from 1.8 to 26.1 years. It involved assessing the maxillary and mandibular teeth on the left side with the stages of Haavikko and Demirjian and Goldstein to obtain a mean age of attainment and standard error for each tooth development stage.
Statistical analysis
The statistical method of weighted averages was used to derive an estimated dental age for each subject. Teeth were assessed by using the methods of both Haavikko and Demirjian and Goldstein to determine whether the number of stages influenced the accuracy and precision of the dental age estimation. The dental age assessment method was tested on a separate sample of 50 subjects, and it was found that on average the dental age overestimated chronologic age by 0.29 year, providing a more accurate estimate of age from tooth development than was previously possible.
The data were analyzed by using SPSS software (version 14; SPSS, Chicago, Ill). Descriptive statistics were used to describe both sample groups (control and dental agenesis) in terms of age, sex, ethnicity, and number of missing teeth. The estimated dental age was calculated by meta-analysis with software (Intercooled version 9; StataCorp, College Station, Tex). The differences between dental and chronologic ages of the dental agenesis group with the 12 stages of Haavikko and the 8 stages of Demirjian and Goldstein of tooth formation were compared with the difference between dental and chronologic ages of the control group with an independent samples t test.
Paired t tests were used to test for differences between dental and chronologic ages for both sexes in the control and dental agenesis groups by using the 12 stages of Haavikko and the 8 stages of Demirjian and Goldstein. A multiple regression analysis was performed to test for the association among sex, severity of dental agenesis, ethnicity, and delay in dental age by using the same stages of tooth formation. To compare the agreement in prediction of dental age between the methods of Haavikko and Demirjian and Goldstein, a Bland-Altman assessment was performed.
Results
All patients approached agreed to participate, and there were no withdrawals. The recruited sample comprised 139 patients (67 boys, 72 girls) distributed among the different groups as outlined in Table I .
| Dental agenesis groups | Control group | Total | |||
|---|---|---|---|---|---|
| Mild | Moderate | Severe | |||
| Boys | 19 | 12 | 18 | 12 | 67 |
| Girls | 24 | 19 | 17 | 19 | 72 |
| Total | 43 | 31 | 35 | 31 | 139 |
Each patient’s ethnic group was recorded. The patient could select 1 of 16 ethnic groups on a list. Because most (71%) of the subjects were white, the sample was then divided in 2 main groups: white and nonwhite, which included Asian, Asian British, Chinese, black, black British, mixed, or other ethnic group. In the control group, the number of white patients was slightly higher (55%) than nonwhite patients (45%). In the 3 dental agenesis groups, most subjects were white (76%), as shown in Table II .
| Ethnic group | Control group n (%) |
Dental agenesis groups | ||
|---|---|---|---|---|
| Mild n (%) |
Moderate n (%) |
Severe n (%) |
||
| White | 17 (55%) | 34 (79%) | 21 (70%) | 27 (77%) |
| Nonwhite | 14 (45%) | 9 (21%) | 9 (30%) | 8 (23%) |
| Total | 31 (100%) | 43 (100%) | 30 (100%) | 35 (100%) |
The study group subjects were between 9.01 and 17.65 years, with a mean age of 12.66 years. Table III shows the mean ages, standard deviations, and age ranges for the control and the dental agenesis groups.
| Control | Dental agenesis groups | |||
|---|---|---|---|---|
| Mild | Moderate | Severe | ||
| Mean (y) | 12.28 | 12.69 | 12.77 | 12.90 |
| SD (y) | 1.84 | 2.13 | 2.15 | 2.40 |
| Minimum (y) | 9.27 | 9.01 | 9.77 | 9.02 |
| Maximum (y) | 16.29 | 17.31 | 17.65 | 17.52 |
Cohen’s kappa statistic demonstrated intraexaminer agreement of 0.97 for the 12-stage method of Haavikko and 0.98 for the 8-stage method of Demirjian and Goldstein, indicating almost perfect agreement. Interexaminer agreement between the 2 observers was 0.80 for Haavikko and 0.83 for Demirjian and Goldstein; this corresponds to almost perfect agreement.
For the difference between chronologic and dental ages, with the 12 stages of Haavikko of tooth formation to assess the patient’s dental age, the control group showed mean delays of 0.51 year (SD, 1.50) in boys and 0.38 year (SD, 1.23) in girls ( Table IV ). The dental agenesis group showed mean delays of 1.40 years (SD, 1.67) for boys and 0.98 year (SD, 1.81) for girls ( Table V ).
| Sex | Haavikko | Demirjian and Goldstein | ||
|---|---|---|---|---|
| Male | Female | Male | Female | |
| Mean (y) | −0.51 | −0.38 | −1.00 | −0.56 |
| SD (y) | 1.50 | 1.23 | 1.75 | 1.50 |
| Minimum (y) | −3.39 | −2.67 | −4.80 | −3.31 |
| Maximum (y) | 1.11 | 1.43 | 0.90 | 2.87 |
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