Odontology DOI 10.1007/s10266-014-0164-3
ORIGINAL ARTICLE
Formation and development of maxillary first molars with delayed eruption Natsuki Sano • Takashi Kameda • Yukari Terashima Nomintsetseg Batbayar • Kazuto Terada
•
Received: 24 February 2014 / Accepted: 9 June 2014 Ó The Society of The Nippon Dental University 2014
Abstract Cases of congenitally missing and delayed eruption of the maxillary first molar are rare. However, in recent years, we have experienced cases of suspected delayed eruption of or congenitally missing first molars. The purpose of this study was to analyze the formation of delayed erupted maxillary first molars (M1) ([2 standard deviations), which play important roles in occlusion, and normal eruption of the maxillary first molars (U6). The frequency of M1 among patients born between 1974 and 1994 in one institution with a clear total patient number and personal oral histories was 1.55 % [80 % bilateral eruption in 8 of 806 male patients (0.99 %) and 23 of 1195 female patients (1.92 %)]. To evaluate the formation and eruption of M1 according to Moorrees’s tooth formation stages, panoramic X-ray films were obtained every year for 73 patients with M1 from 3 institutions (20 male and 53 female patients, total 131 M1s) without systematic histories or genetic disorders. The development/growth curve of M1 was fitted to both the logistic curve and U6 curve. The M1 development/growth curve was started behind with U6 curve; however, the straight part of the M1 curve exhibited steep inclination compared with the straight part of the U6 curve. The curve of the eruption pathway of M1 also exhibited a sigmoid S shape. These results indicate that the development and migration speed of M1 are faster than that of U6, excluding the delayed start point. These results may help orthodontists in treatment planning for patients with M1.
N. Sano (&) T. Kameda Y. Terashima N. Batbayar K. Terada Department of Orthodontics, The Nippon Dental University School of Life Dentistry at Niigata, 951-8580 Hamaura-chou 1-8, Chuuou-ku, Niigata, Japan e-mail: [email protected]
Keywords Delayed eruption Moorrees’s tooth formation stage Logistic curve Pathway
Introduction Angle’s classification is widely used for diagnostic examination of orthodontic treatment. This classification is based on his assumption that the maxillary first molar with normal eruption (U6), a key tooth in occlusion, is always in the anatomical position and that classification comes from the mesiodistal relation of the jaws [1]. In addition, Andrew [2] stated that the maxillary first molar is an important factor in forming occlusion. Thus, the maxillary first molar is a very important tooth in orthodontic treatment. Congenitally/acquired missing or delayed eruption of the maxillary first molar is said to aggravate jaw disorders by the declination of chewing function and contribute to an unstable bite [3]. Maxillary first molars play important roles as the anchorage teeth in orthodontic treatment with various appliances; e.g., sectional arch wire, lingual arch, head gear and expansion appliance. Delayed or absent eruption of the maxillary first molar causes an unstable occlusion, which may have adverse effects in terms of oral function [4, 5]. Disturbed eruption of the permanent teeth reportedly occurred with an incidence of 4 % [6]. Causes of delayed tooth eruption include cysts, ectopic eruption, maldevelopment of the tooth germ, and delayed odontoma formation. It is thought that the causes of delayed odontoma formation include systemic diseases such as cleidocranial dysplasia. In many clinical cases, the orthodontic treatment plan should be made with reference to the eruption timing of the first molars. Odontogenesis is known to be a reliable index of individual growth and development [7–9]. The crown-root
123
Odontology
ratio [(Crown ? Root)/Crown] is also reported to be a reliable index [10]. Dale [11] studied the quantity of root formation and the odontogenic eruption period. Because delayed eruption of permanent teeth involves embryonic teeth with few individual differences, there is a strong correlation between eruption timing and calendar age [6]. Furthermore, formation of the first molar is known to be anatomically stable, and congenital absence of the first molar is a rare condition [12–14]. Maxillary first molars were present in almost all patients with non-syndromic hypodontia who were missing several other teeth [15, 16]. For its part, it is always studied delayed eruption of tooth and eruption disorder of the maxillary first molar [17–19]. Conversely, reports of patients missing only the maxillary first molar have also been published [5, 20–22]. There have been some recent reports of patterns of congenitally missing teeth, including the first molar [23, 24]. We previously reported 51 Japanese patients (95 teeth) who were suspected to have eruption of the maxillary first molars with delayed eruption of more than two standard deviations (SD), termed ‘‘M1’’ [25]. The general timing of the eruption of the maxillary first molars in Japanese individuals is reportedly 6.67 years of age (SD, 8 months) in males and 6.58 years of age (SD, 8 months) in females [26]. Of 51 patients (18 male and 33 female patients), 7 (14 %) and 44 (86 %) exhibited the delayed eruption unilaterally and bilaterally, respectively. The 95 upper M1s from these 51 patients were assessed to determine the developmental status compared with the mandibular canines as the reference tooth using panoramic radiographs by Moorrees’s tooth formation stages [27]. Interestingly, when we compare the formation of the M1 with that of the first and second molars, the timing of the start of tooth formation occurred between that of the first and second molars, but the speed of tooth formation was faster than that of the maxillary second molar. However, additional details of M1, including its frequency, formation, and eruption, are needed for application to clinical treatment planning. In this study, we examined 73 cases of M1 in terms of frequencies, sex differences, tooth formation stages fitted to the logistic curves, and eruption pathways.
Fig. 1 Delayed development of upper first molars on panoramic radiograph (8y 10 m, female)
eruption of the maxillary first molar due to ectopic eruption or odontoma; and patients without systemic diseases including cleft lip, jaw, or palate. This study evaluated the 131 M1s delayed erupted at the position of U6 with exceeding 2SD (male and female SD: 8 months) above average eruption age of U6 (male: 6.67 years, female: 6.58 years) [26]. These M1s were derived from 73 patients (20 males and 53 females) with observation of the mandibular canine tooth germ on the panoramic X-ray photographs during the subsequent follow-up period. To evaluate the frequency of M1, we examined 2,001 patients from one institution with a clear total patient number and personal oral histories among all patients born between 1974 and 1994. The data were obtained from panoramic X-ray films taken for orthodontic treatment (Fig. 1). The age and sex of each subject were recorded (Table 1). These data were compared with the values reported by Niimura [28] as Japanese Standard age of U6 eruption classified by Moorrees’s tooth formation stage [27]. The data were converted into non-linkable anonymous information prior to evaluation of the results. Frequency of M1 The frequency of M1 was investigated among 2,001 patients with M1 born between 1974 and 1994 in one dental clinic.
Subjects and methods Laterality and sex differences of M1 Ethical approval from the Local Research Ethics Committee was obtained (ECNG-H-19), and informed consent was obtained prior to commencement of the study. Subjects Selection of subjects among patients visiting orthodontic clinics was performed according to the following criteria: patients [6 years of age; patients without abnormal
123
We estimated sex differences and laterality in 73 patients from three institutions including above one institution. Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age We evaluated the tooth formation stages of M1 until eruption. In this study, eruption was defined as the point
Odontology Table 1 Classification of subjects Tooth formation stages (Moorrees et al. [27])
Male
Female
This study N
Average
SD
Min
Max
Japanese values Niimura
This study
Average
N
1
Initial cusp formation (Ci)
2
Coalescence of cusps (Cco)
3
Cusp outline complete (Coc)
4
Crown 1/2 complete (Cr 1/2)
5
Crown 3/4 complete (Cr 3/4)
1
6.21
6
Croen complete (Crc)
2
7.04
7.00
7
Initial root formation (Ri)
2
7.35
7.00
8
Initial cleft formation (Cli)
4
8.43
0.57
9
Root length 1/4 (R 1/4)
5
8.84
10
Root length 1/2 (R 1/2)
4
9.84
11
Root length 3/4 (R 3/4)
4
10.92
0.69
9.98
11.52
12
Root length complete (Rc)
4
11.79
1.20
10.54
12.86
13 14
Apex 1/2 closed (A 1/2) Apical closure complete (Ac)
3 5
12.72 13.86
1.04 0.86
11.21 12.56
13.56 14.93
9.88 10.86
SD
Average
Japanese values Niimura SD
1.90
Min
Max
Average
SD
3.42
0.48
3
6.04
4.18
7.98
3.36
0.38
7.08
3.83
1.18
2
6.82
7.70
4.19
0.91
5
7.10
0.36
6.78
6.93
3.78
0.56
6.48
7.37
3.89
8.10
9.28
4.58
0.79
16
7.85
0.73
0.90
6.97
9.04
4.61
0.81
8.01
10.01
5.66
1.31
15
1.20
8.46
0.93
7.07
10.03
5.40
1.18
0.52
9.10
10.03
6.13
0.87
13
9.52
0.89
8.04
10.99
6.37
1.12
7.53
1.08
14
9.85
1.04
8.03
11.98
7.39
0.93
8.97
1.15
8
10.96
0.93
9.98
12.23
8.74
1.19
1.07 0.71
9 12
12.30 13.55
0.85 0.53
10.87 12.76
13.01 14.22
9.73 10.14
0.91 1.14
Fig. 2 Tooth formation stages according to Moorrees et al
passing through the alveolar bone during migration of the tooth toward the oral cavity. The developmental status of M1 was classified by a 14-stage scale in accordance with the criteria for assessment of the developmental stages proposed by Moorrees et al. [27] (Fig. 2). We measured it using computerized measurement software. Mandibular
canines on the same side as M1 were classified according to a 13-tooth formation stage by Moorrees. These teeth were used as control teeth because lower canines are little delayed eruption and congenital missing, high persistence compared with the other teeth. Moreover, the frequency of mandibular canine impaction is reportedly lower than that
123
Odontology
Fig. 3 Logistic curve fitting. a. Changes in coefficient A corresponding to a shift in time. b The inclination of liner part (around X = 0) in curve changes when coefficient B changes
of maxillary canine impaction [29]. Evaluations of M1 and canine tooth formation were performed twice at a [1month interval by the same examiner. M1s were evaluated in terms of crosswise differences and gender-associated differences at the tooth formation stage, and any differences observed were tested for statistical significance by the Mann–Whitney test. We calculated sex differences and frequencies of the patients with M1 compared with agematched patients visiting the same hospital with normal eruption of the maxillary first molar (U6). Logistic curve fitting of the M1 tooth formation stage at each age The logistic curve used in this study was as follows: Y ¼ K = ð1 þ AeBX Þ where K represents the maximum value and A and B are coefficients. X indicates age (years), and Y indicates the tooth formation stage, or (C ? R)/C, calculated from the panoramic X-ray photographs (C, crown height, namely length from cusp of tooth crown to anatomical tooth cervix region; R, root length, namely length from anatomical tooth cervix region to apex of root). A characteristic of this curve is that with increments in coefficient A, the shape of the curve does not change, but shifts in parallel with the X axis. Therefore, a change in coefficient A corresponds to a shift in time (Fig. 3a). If, however, coefficient B increases, the inclination in the spurt area of this curve becomes steeper (Fig. 3b). Therefore, if coefficient B is small, the length increases only slowly. If B is large, the length increases remarkably during a short interval. During odontogenic formation of normally erupted teeth, the growth rate was slow in the early stage (e.g., appearance of the tooth germ on X-ray photographs) and then accelerated drastically, which was exhibited as an
123
Fig. 4 Relationship between Moorrees’ tooth formation stage and eruption of M1. a When we assumed that the tooth cervix of the upper second deciduous molar = 100, we obtained the above schematic representation of the axis of coordinates and the coordinate values of L1 (the dotted line indicates alveolar bone). b Location of M1 at each tooth formation stage and age
S-shaped curve. The logistic curve is thought to be a good tool for examination of skeletal development and growth, including tooth growth [30]. We attempted to fit the plot of the tooth formation stage or (C ? R)/C (Y axis) against the calendar age of the subjects (X axis) to a logistic curve defined by Y ¼ K=ð1 þ A eBX Þ, and the degree of fitness was rated at a significance level of 5 % [25, 30]. The coefficients A and B for the significantly fitting logistic curve were analyzed and weighed against the results that we reported. Logistic curves of M1 were compared with
Odontology Table 2 Frequency, laterality and sex differences of M1 Bilateral
Unilateral
Total no.
Right
Left
No. of case with M1 Male
14
3
3
20
Female
44
5
4
53
116
8
7
131
Tooth no. M1
those of U6 created from the data of Niimura [28] and Daito [31] classified by Moorrees’s tooth formation stage [27] as control. The software package used was STAT FREX 6. Eruption pathway of M1 at each tooth formation stage The primary second molars (E) and M1s were traced from panoramic X-ray photographs. We set the origin of the coordinate axes at the point of the distal cementoenamel junction of E. The X axis was the line containing both the mesial and distal cementoenamel junctions of E. We assumed that the tooth cervix of the upper first deciduous molar = 100 and created a schematic representation of the axis of the coordinates and the coordinate values of L1 (the dotted line indicates the mean alveolar bone). The Y axis was the line that crossed at right angles to the X axis and contained the origin point. We obtained coordinate data of M1 classified by tooth formation stage for evaluation of the eruption pathway, which was the center point between the apex of the mesial and distal cusps (L1) (Fig. 4a). The coordinate data of all patients who have M1 at each tooth formation stage were averaged, plotted, and superimposed. The location of M1 at each tooth formation stage and age were evaluated by longitudinal chase of point L1 (Fig. 4b).
differences in the frequency of M1 (Table 2). Among the 73 subjects (20 male and 53 female), M1 was unilateral in 15 (20.5 %) (right 8, left 7) and bilateral in 58 (79.5 %) (Table 2). Among male M1s, 70 % were bilaterally erupted, whereas the remaining 30 % were unilaterally erupted (right:left = 1:1). Among female M1s, 83 % were bilaterally erupted. The frequency of unilaterally female M1s was lower than that of male M1s (total 17 %, right 9.4 %, left 7.6 %). Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age The timing of tooth formation of M1 was examined and compared with that of U6 (Table 1). The speed of tooth formation before the R 1/4 stage was slow; however, it increased in the subsequent stages. Lower canines with normal eruption were used as the control teeth. Logistic curve fitting is a good tool for the examination of skeletal development and growth, including tooth growth. The tooth formation stage of M1 (Y) corresponding to the calendar age (X) was adapted to the logistic curve ðY ¼ K=½1 þ Ae BX Þ. For male subjects, coefficient A = 54.845 and B = 0.541; for female subjects, coefficient A = 51.131 and B = 0.529 (Fig. 5). Daito’s male subjects, coefficient A = 5.679 and B = 0.468; for female subjects, coefficient A = 5.820 and B = 0.481. Niimura’s male subjects, coefficient A = 7.018 and B = 0.421; for female subjects, coefficient A = 7.296 and B = 0.438. Figure 5 shows the logistic curves of M1 labeled by Moorrees’ tooth formation stage. Coefficient A was 54.845 and 51.131 and coefficient B was 0.541 and 0.529 in male and female subjects, respectively. Figure 6 shows the logistic curve of M1 classified by the ratio of crown height with root length to crown height. The development/growth curves of both male and female M1s were in conformity with the logistic curves at a significance level of \5 %.
Results Eruption pathway of M1 at each tooth formation stage Frequency of M1 Thirty-one of 2,001 patients from one institution among all patients born between 1974 and 1994 had M1 (1.55 %); i.e., 8 of 806 male patients (0.99 %) and 23 of 1,195 female patients (1.92 %). Approximately, 80 % of patients with M1 showed bilateral eruption. Of 31 patients with delayed eruption, 20 % (right 3, left 3) showed unilateral eruption (normal eruption on the opposite side). Laterality and sex differences of M1 Seventy-three patients with M1 from three institutions were examined to investigate laterality and gender
The eruption pathway of M1 was examined (Fig. 4a). When we observed a mesiodistal plane of the crown, the M1 in the early stages (e.g., it was grow up in R 1/4 from Ci) was distally inclined, and then gradually became mesially inclined during eruption through the alveolar bone, which was similar to the finding of Saijo [32], though it was cephalometrics. The migration speed of M1 exhibited an S-shaped curve (Fig. 4b). M1 erupted through the alveolar bone into the oral cavity at the Moorrees’ stage between R 1/4 and R 1/2; this stage exhibited the fastest eruption (Fig. 4b). A strong correlation was found between the M1 position and the ratio of crown height to observed root length on X-ray photographs or between the M1
123
Odontology Fig. 5 Logistic curves of delayed development of the upper first molars
Fig. 6 Logistic curve of M1 classified by ratio of crown height with root length to crown height
position and calendar age. Spearman’s rank correlation coefficient between the M1 position and the ratio of crown height to root length showed a correlation [bilateral coefficient of correlation, rs = 0.81 (Z value = 8.93)]. Spearman’s rank correlation coefficient also showed a
123
correlation between the M1 position and calendar age [bilateral coefficient of correlation, rs = 0.62 (Z value = 6.80)]. When we performed simple regression analysis between the root length/crown height and alveolar bone distances
Odontology
from M1 (point L1 to alveolar crest), a regression equation of L = 75.41 9 R/C - 87.25 was obtained (P \ 0.01). A regression equation of L = 21.21 9 Age - 196.28 was also obtained from the results of single regression analysis between calendar age and alveolar bone distances from M1 (point L1 to alveolar crest) (P \ 0.01). U6 was already fully erupted at this age; thus, we did not photograph it from an ethical standpoint. However, if we are presented with the opportunity, we investigate this issue in the future.
Discussion Frequency of M1 The frequency of delayed eruption of the maxillary M1 in 2,001 patients born from 1974 to 1994 in one institution with a clear total patient number and personal oral histories was 1.55 % (31 patients) in this study. This value was higher than those previously reported by Grover and Lorton in 1985 (0.01 %) and by Kramer and Williams in 1970 (0.25 %) [12, 13]. Laterality and sex differences of M1 Of the 73 patients with M1 from three institutions in this study, 15 (20.55 %) showed unilaterally delayed eruption and 58 (79.45 %) showed bilaterally delayed eruption. These frequencies are similar, but slightly higher than those reported by Rasmussen [33], who indicated that 9 of 10 cases of M1 were bilateral. Among the 73 subjects (20 male and 53 female subjects) from three institutions including the above-mentioned single institution in this study, the numbers of male and female subjects with M1s were 20 and 53, respectively, resulting in a sex ratio of 1:2.65 (Table 2). These sex ratios were almost identical to those in previous reports, indicating that the number of female M1s was two- to threefold higher than the number of male M1s [14, 33]. Among male M1s, 70 % were bilaterally erupted, whereas the remaining 30 % were unilaterally erupted (right:left = 1:1). Among female M1s, 83 % were bilaterally erupted, whereas the remaining 17 % were unilaterally erupted (right:left = 5:4). From these results, the female subjects had a higher incidence of bilateral M1s than did male subjects. Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age The timing of tooth formation of M1 was examined and compared with that of U6 (Table 1). The timing of root
formation of M1 was, in all cases, between that of the permanent maxillary M1s and maxillary second molars [33]. Lower canines with normal eruption were used as control teeth. According to the report of Yamada [34], M1 might be early erupted second molars which exhibited degenerative characteristic, when the first molar was congenitally missing tooth. According to the report by Rasmussen, the tooth formation in the early stages was rapid, and that in the later stages of development became slower according to the odontogenic formation stages of Moorrees (Fig. 2). In contrast, the early stage of development, before Moorrees’ R 1/4 stage of tooth formation, was late; however, the tooth formation speed in the stages following R 1/4 increased in this study (Table 1). To evaluate the tooth formation stage as classified by Moorrees’ method, we applied the stage to the logistic curve calculated by Y ¼ K=ð1 þ A eBX Þ. If coefficient A in the logistic curve increases, the curve moves to the right and the formation will be late. If coefficient B decreases, the start of the curve becomes sudden and the formation speed increases. Because of the formation stage of M1, coefficient A was large and coefficient B was small, which shifted the start of the graph to the right and caused a sudden steep inclination. In other words, this graph lagged behind the tooth development, but the actual tooth formation was early. We evaluated conformity to the logistic curve in the same way as that shown by Niimura [28] and Daito [31] who evaluated the average Japanese tooth formation stage using Moorrees’ method. The results obtained in this study indicated that the hazard ratio for male and female subjects was \5 % and showed conformity to the logistic curve. These results are similar to those seen in other articles showing that the odontogenic formation speed was fitted to the logistic curve [35]. Calendar age at each tooth formation stage of M1 was delayed compared with that of U6. We checked the calendar ages of Moorrees’ stage Cli (initial cleft formation, Fig. 2) and Rc (root length complete) of M1 and U6 from Niimura’s data. We found that the age of Cli of M1 was 8.08 years (males) and 7.17 years (females), whereas the age of Cli of U6 was 5.08 years (males) and 4.92 years (females). In addition, Rc of M1 was 10.50 years (males) and 10.17 years (females), whereas Rc of U6 was 8.17 years (males) and 7.92 years (females). Using these findings, which indicated that development of M1 was 2–3 years later than that of U6, we fitted the data of tooth formation of maxillary M1s by Niimura and Daito for comparison with our logistic curves of the M1 tooth formation stage and ratio of crown height to root length (Table 1; Figs. 5, 6). From these results, the coefficients of the M1 and U6 logistic curves were the same after the fourth decimal point.
123
Odontology
Eruption pathway of M1 at each tooth formation stage
References
The eruption pathway of M1 was examined by the movement of point L1, the center point between the apex of the mesial and distal cusps of M1, on panoramic X-ray photographs. The X axis was the cementoenamel junction of the mesiodistal aspect of the second primary molar, and the Y axis was a tangent line of the second primary molar efferent to that traveling directly to the X axis. M1 was first located near the apex of the root of the second primary molar (Cr 3/4), but as it continued to erupt, it moved to the region of the cervix of the second primary molar (R 1/4); eruption rapidly continued into the oral cavity (between R 1/4 and R 1/2). When we examined this process in detail, R 3/4 showed rapid growth from R 1/4, and the gradient of the graph increased when we made it the average coordinate, creating an S-shaped curve. Spearman’s rank correlation coefficient and single regression analysis suggest that the M1 position during eruption and the calendar age or ratio of crown height to root length have relatively high correlations. These results suggest that the eruption timing of M1 can be predicted by the tooth formation stage and ratio of root length to crown height of M1 on panoramic X-ray photographs. To know the periods of deciduous teeth replacement and permanent teeth eruption is one of the most important information for better orthodontic treatment planning based on the evidence-based medicine. The prediction of these information can be obtained from the patients, e.g., individual growth state, cast models, and X-ray photographs. However, the prediction of eruption periods of delayed erupting teeth including M1 is difficult and needed lots of X-ray photographs compared with those of normal erupting teeth. Recently, the patients become sensitive to radiation exposure especially in Japan since the Grate Est Japan earthquake on March 11, 2011. In this paper, tooth development of M1 with eruption pathway at each stage is represented. These results should be helpful for the prediction of eruption timing of M1, and the decrease of the radiation exposure to the patients by the increase of the intervals of X-ray photographing. These data in this paper will hopefully plan the orthodontic treatment for both patient and clinician. Further studies are needed to realize more exact prediction of M1 eruption for construction of better orthodontic treatment planning.
1. Hahn GW. Edward Hartley Angle (1855–1930). Am J Orthod. 1965;51:529–35. 2. Andrew LF. The six keys to normal occlusion. Am J Orthod. 1972;62:296–309. 3. Barnett EM, Mehta JD. Olar growth stages—the keys to guiding occlusal development. J Am Dent Assoc. 1970;81(6):1360–8. 4. Proff P, Bayerlein T, Fangha¨nel J, Allegrini S Jr, Gedrange T. Morphological and clinical considerations of first and second permanent molar eruption disorders. Ann Anat. 2006;188:353–61. 5. Barberia-Leache E, Suarez-Clu´a C, Saavedra-Ontiveros D. Ectopic eruption of the maxillary first permanent molar: characteristics and occurrence in growing children. Angle Orthod. 2005;75:610–5. 6. Johnsen DC. Prevalence of delayed emergence of permanent teeth as a result of local factors. J Am Dental Assoc. 1977;94:100–6. 7. Demirjian A, Goldstein H, Tanner JM. A new system of dental age assessment. Hum Biol. 1973;45:211–27. 8. Demirjian A, Goldstein H. New system for dental maturity based on seven and four teeth. Ann Hum Biol. 1976;3:411–21. 9. Leurs IH, Wattel E, Aartman IH, Etty E, Prahl-Andersen B. Dental age in Dutch children. Eur J Orthod. 2005;27(3):309–14. 10. Gleiser I, Hunt EE Jr. The permanent mandibular first molar: its calcification, eruption and decay. Am J Phys Anthropol. 1955;13(2):253–83. 11. Dale JG. Interceptive guidance of occlusion with emphasis on diagnosis. Alpha Omegan. 1999;92(4):36–43. 12. Kramer RM, Williams AC. The incidence of impacted teeth. Oral Surg Oral Med Oral Pathol. 1970;29:237–41. 13. Grover PS, Lorton L. The incidence of unerupted permanent teeth and related clinical cases. Oral Surg Oral Med Oral Pathol. 1985;59:420–5. 14. Noda T, Takagi M, Hayashi-Sakai S, Taguchi Y. Eruption disturbances in Japanese children and adolescents. Pediatric Dental J. 2006;16:50–6. 15. Valmaseda-Castello´n E, De-la-Rosa-Gay C, Gay-Escoda C. Eruption disturbances of the first and second permanent molars: results of treatment in 43 cases. Am J Orthod Dentofac Orthop. 1999;116:651–8. 16. Ga´bris K, Tarja´n I, Csiki P, Konra´d F, Sza´deczky B, Ro´zsa N. Prevalence of congenital hypodontia in the permanent dentition and its treatment. Fogorv Sz. 2001;94(4):137–40. 17. Baccetti T. Tooth anomalies associated with failure of eruption of first and second permanent molars. Am J Orthod Dentofac Orthop. 2000;118:608–10. 18. Philipsen HP, Thosaporn W, Reichart PA, Grundt G. Odontogenic lesions in opercula of permanent molars delayed in eruption. J Oral Pathol. 1982;21:38–41. 19. Chintakanon K. Ectopic eruption of the first permanent molars: prevalence and etiologic factors. Angle Orthod. 1998;68: 153–60. 20. Bjerklin K, Gleerup A, Kurol J. Long-term treatment effects in children with ectopic eruption of the maxillary first permanent molars. Eur J Orthod. 1995;17:293–304. 21. Tomizawa M, Yonemochi H, Kohno M, Noda T. Unilateral delayed eruption of maxillary permanent first molars: four case reports. Int J Jpn Soc Pediatric Dent. 1998;20:53–6. 22. Nakano K, Matsuoka T, Takahashi A, Matsumura M, Sobue S, Ooshima T. Delayed development or congenital absence of a single first permanent molar in Japanese child patients. Int J Pediatr Dent. 1999;9:271–6.
Acknowledgments We are indebted to Dr. Iijima (Orthodontist in Mito, Ibaraki Prefecture), Dr. Ohtake (Orthodontist in Nagaoka, Niigata Prefecture), and Dr. Sugiyama (Orthodontist in Niigata) for their data and advice on this study. Conflict of interest of interest.
123
The authors declare that they have no conflict
Odontology 23. van Wijk AJ, Tan SP. Patterns of tooth agenesis. A numerical code for describing dental agenesis. Ned Tijdschr Tandheelkd. 2009;116:63–7. 24. Cre´ton MA, Cune MS, Verhoeven JW, Meijer GJ. Patterns of missing teeth in a population of oligodontia patients. Int J Prosthodont. 2007;20(4):409–13. 25. Sano N, Hasegawa Y, Iijima S, Terada K. Study of delayed development of the upper first molars. Okajimas Folia Anat Jpn. 2010;87(1):25–31. 26. The Japanese Society of Pedodontics. The chronology of deciduous and permanent dentition in Japanese children. Int J Jpn Soc Pediatric Dent. 1988;26:1–18 Japanese. 27. Moorrees CFA, Fanning EA, Hunt EE. Age variation of formation stages for ten permanent teeth. J Dent Res. 1963;42:1490–502. 28. Niimura K. Development of permanent tooth formation in children (in Japan). J Fukuoka Dental Coll. 1995;22:485–509 Japanese.
29. Jacoby H. The etiology of maxillary canine impactions. Am J Orthod. 1983;84:125–32. 30. Terada K, Saito I, Liu H, Hanada K. Longitudinal study on the length change of digital bones and mandible with a logistic curve. J Jpn Orthod Soc. 1995;54:413–24. 31. Daito M, Kawahara S, Tanaka M, Imai G, Nishihara G, Hieda T. Calcification of the permanent first molars observed in panoramic radiographs. J Osaka Dental Univ. 1989;23:45–55 Japanese. 32. Saijo K, Ogino C, Sasaki N, Saito F, Chiba H, Kamiyama K. Clinical study of ectopic eruption of the permanent first molars. Shoni Shikagaku Zasshi. 1990;28:1093–103 Japanese. 33. Rasmussen P. ‘‘9-year-molars’’ aberrantly developing and erupting: report of cases. J Clin Pediatr Dent. 1998;22:151–3. 34. Yamada H. Tooth size morphology of affected molars in individuals with congenitally missing first molar. Anthropol Sci Jpn Ser. 2010;118(2):83–96. 35. Goya HA, Satake T, Maeda T. Dental age in Japanese children using a modified Demirjian method. Pediatric Dental J. 2009;19(1):82–8.
123
ORIGINAL ARTICLE
Formation and development of maxillary first molars with delayed eruption Natsuki Sano • Takashi Kameda • Yukari Terashima Nomintsetseg Batbayar • Kazuto Terada
•
Received: 24 February 2014 / Accepted: 9 June 2014 Ó The Society of The Nippon Dental University 2014
Abstract Cases of congenitally missing and delayed eruption of the maxillary first molar are rare. However, in recent years, we have experienced cases of suspected delayed eruption of or congenitally missing first molars. The purpose of this study was to analyze the formation of delayed erupted maxillary first molars (M1) ([2 standard deviations), which play important roles in occlusion, and normal eruption of the maxillary first molars (U6). The frequency of M1 among patients born between 1974 and 1994 in one institution with a clear total patient number and personal oral histories was 1.55 % [80 % bilateral eruption in 8 of 806 male patients (0.99 %) and 23 of 1195 female patients (1.92 %)]. To evaluate the formation and eruption of M1 according to Moorrees’s tooth formation stages, panoramic X-ray films were obtained every year for 73 patients with M1 from 3 institutions (20 male and 53 female patients, total 131 M1s) without systematic histories or genetic disorders. The development/growth curve of M1 was fitted to both the logistic curve and U6 curve. The M1 development/growth curve was started behind with U6 curve; however, the straight part of the M1 curve exhibited steep inclination compared with the straight part of the U6 curve. The curve of the eruption pathway of M1 also exhibited a sigmoid S shape. These results indicate that the development and migration speed of M1 are faster than that of U6, excluding the delayed start point. These results may help orthodontists in treatment planning for patients with M1.
N. Sano (&) T. Kameda Y. Terashima N. Batbayar K. Terada Department of Orthodontics, The Nippon Dental University School of Life Dentistry at Niigata, 951-8580 Hamaura-chou 1-8, Chuuou-ku, Niigata, Japan e-mail: [email protected]
Keywords Delayed eruption Moorrees’s tooth formation stage Logistic curve Pathway
Introduction Angle’s classification is widely used for diagnostic examination of orthodontic treatment. This classification is based on his assumption that the maxillary first molar with normal eruption (U6), a key tooth in occlusion, is always in the anatomical position and that classification comes from the mesiodistal relation of the jaws [1]. In addition, Andrew [2] stated that the maxillary first molar is an important factor in forming occlusion. Thus, the maxillary first molar is a very important tooth in orthodontic treatment. Congenitally/acquired missing or delayed eruption of the maxillary first molar is said to aggravate jaw disorders by the declination of chewing function and contribute to an unstable bite [3]. Maxillary first molars play important roles as the anchorage teeth in orthodontic treatment with various appliances; e.g., sectional arch wire, lingual arch, head gear and expansion appliance. Delayed or absent eruption of the maxillary first molar causes an unstable occlusion, which may have adverse effects in terms of oral function [4, 5]. Disturbed eruption of the permanent teeth reportedly occurred with an incidence of 4 % [6]. Causes of delayed tooth eruption include cysts, ectopic eruption, maldevelopment of the tooth germ, and delayed odontoma formation. It is thought that the causes of delayed odontoma formation include systemic diseases such as cleidocranial dysplasia. In many clinical cases, the orthodontic treatment plan should be made with reference to the eruption timing of the first molars. Odontogenesis is known to be a reliable index of individual growth and development [7–9]. The crown-root
123
Odontology
ratio [(Crown ? Root)/Crown] is also reported to be a reliable index [10]. Dale [11] studied the quantity of root formation and the odontogenic eruption period. Because delayed eruption of permanent teeth involves embryonic teeth with few individual differences, there is a strong correlation between eruption timing and calendar age [6]. Furthermore, formation of the first molar is known to be anatomically stable, and congenital absence of the first molar is a rare condition [12–14]. Maxillary first molars were present in almost all patients with non-syndromic hypodontia who were missing several other teeth [15, 16]. For its part, it is always studied delayed eruption of tooth and eruption disorder of the maxillary first molar [17–19]. Conversely, reports of patients missing only the maxillary first molar have also been published [5, 20–22]. There have been some recent reports of patterns of congenitally missing teeth, including the first molar [23, 24]. We previously reported 51 Japanese patients (95 teeth) who were suspected to have eruption of the maxillary first molars with delayed eruption of more than two standard deviations (SD), termed ‘‘M1’’ [25]. The general timing of the eruption of the maxillary first molars in Japanese individuals is reportedly 6.67 years of age (SD, 8 months) in males and 6.58 years of age (SD, 8 months) in females [26]. Of 51 patients (18 male and 33 female patients), 7 (14 %) and 44 (86 %) exhibited the delayed eruption unilaterally and bilaterally, respectively. The 95 upper M1s from these 51 patients were assessed to determine the developmental status compared with the mandibular canines as the reference tooth using panoramic radiographs by Moorrees’s tooth formation stages [27]. Interestingly, when we compare the formation of the M1 with that of the first and second molars, the timing of the start of tooth formation occurred between that of the first and second molars, but the speed of tooth formation was faster than that of the maxillary second molar. However, additional details of M1, including its frequency, formation, and eruption, are needed for application to clinical treatment planning. In this study, we examined 73 cases of M1 in terms of frequencies, sex differences, tooth formation stages fitted to the logistic curves, and eruption pathways.
Fig. 1 Delayed development of upper first molars on panoramic radiograph (8y 10 m, female)
eruption of the maxillary first molar due to ectopic eruption or odontoma; and patients without systemic diseases including cleft lip, jaw, or palate. This study evaluated the 131 M1s delayed erupted at the position of U6 with exceeding 2SD (male and female SD: 8 months) above average eruption age of U6 (male: 6.67 years, female: 6.58 years) [26]. These M1s were derived from 73 patients (20 males and 53 females) with observation of the mandibular canine tooth germ on the panoramic X-ray photographs during the subsequent follow-up period. To evaluate the frequency of M1, we examined 2,001 patients from one institution with a clear total patient number and personal oral histories among all patients born between 1974 and 1994. The data were obtained from panoramic X-ray films taken for orthodontic treatment (Fig. 1). The age and sex of each subject were recorded (Table 1). These data were compared with the values reported by Niimura [28] as Japanese Standard age of U6 eruption classified by Moorrees’s tooth formation stage [27]. The data were converted into non-linkable anonymous information prior to evaluation of the results. Frequency of M1 The frequency of M1 was investigated among 2,001 patients with M1 born between 1974 and 1994 in one dental clinic.
Subjects and methods Laterality and sex differences of M1 Ethical approval from the Local Research Ethics Committee was obtained (ECNG-H-19), and informed consent was obtained prior to commencement of the study. Subjects Selection of subjects among patients visiting orthodontic clinics was performed according to the following criteria: patients [6 years of age; patients without abnormal
123
We estimated sex differences and laterality in 73 patients from three institutions including above one institution. Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age We evaluated the tooth formation stages of M1 until eruption. In this study, eruption was defined as the point
Odontology Table 1 Classification of subjects Tooth formation stages (Moorrees et al. [27])
Male
Female
This study N
Average
SD
Min
Max
Japanese values Niimura
This study
Average
N
1
Initial cusp formation (Ci)
2
Coalescence of cusps (Cco)
3
Cusp outline complete (Coc)
4
Crown 1/2 complete (Cr 1/2)
5
Crown 3/4 complete (Cr 3/4)
1
6.21
6
Croen complete (Crc)
2
7.04
7.00
7
Initial root formation (Ri)
2
7.35
7.00
8
Initial cleft formation (Cli)
4
8.43
0.57
9
Root length 1/4 (R 1/4)
5
8.84
10
Root length 1/2 (R 1/2)
4
9.84
11
Root length 3/4 (R 3/4)
4
10.92
0.69
9.98
11.52
12
Root length complete (Rc)
4
11.79
1.20
10.54
12.86
13 14
Apex 1/2 closed (A 1/2) Apical closure complete (Ac)
3 5
12.72 13.86
1.04 0.86
11.21 12.56
13.56 14.93
9.88 10.86
SD
Average
Japanese values Niimura SD
1.90
Min
Max
Average
SD
3.42
0.48
3
6.04
4.18
7.98
3.36
0.38
7.08
3.83
1.18
2
6.82
7.70
4.19
0.91
5
7.10
0.36
6.78
6.93
3.78
0.56
6.48
7.37
3.89
8.10
9.28
4.58
0.79
16
7.85
0.73
0.90
6.97
9.04
4.61
0.81
8.01
10.01
5.66
1.31
15
1.20
8.46
0.93
7.07
10.03
5.40
1.18
0.52
9.10
10.03
6.13
0.87
13
9.52
0.89
8.04
10.99
6.37
1.12
7.53
1.08
14
9.85
1.04
8.03
11.98
7.39
0.93
8.97
1.15
8
10.96
0.93
9.98
12.23
8.74
1.19
1.07 0.71
9 12
12.30 13.55
0.85 0.53
10.87 12.76
13.01 14.22
9.73 10.14
0.91 1.14
Fig. 2 Tooth formation stages according to Moorrees et al
passing through the alveolar bone during migration of the tooth toward the oral cavity. The developmental status of M1 was classified by a 14-stage scale in accordance with the criteria for assessment of the developmental stages proposed by Moorrees et al. [27] (Fig. 2). We measured it using computerized measurement software. Mandibular
canines on the same side as M1 were classified according to a 13-tooth formation stage by Moorrees. These teeth were used as control teeth because lower canines are little delayed eruption and congenital missing, high persistence compared with the other teeth. Moreover, the frequency of mandibular canine impaction is reportedly lower than that
123
Odontology
Fig. 3 Logistic curve fitting. a. Changes in coefficient A corresponding to a shift in time. b The inclination of liner part (around X = 0) in curve changes when coefficient B changes
of maxillary canine impaction [29]. Evaluations of M1 and canine tooth formation were performed twice at a [1month interval by the same examiner. M1s were evaluated in terms of crosswise differences and gender-associated differences at the tooth formation stage, and any differences observed were tested for statistical significance by the Mann–Whitney test. We calculated sex differences and frequencies of the patients with M1 compared with agematched patients visiting the same hospital with normal eruption of the maxillary first molar (U6). Logistic curve fitting of the M1 tooth formation stage at each age The logistic curve used in this study was as follows: Y ¼ K = ð1 þ AeBX Þ where K represents the maximum value and A and B are coefficients. X indicates age (years), and Y indicates the tooth formation stage, or (C ? R)/C, calculated from the panoramic X-ray photographs (C, crown height, namely length from cusp of tooth crown to anatomical tooth cervix region; R, root length, namely length from anatomical tooth cervix region to apex of root). A characteristic of this curve is that with increments in coefficient A, the shape of the curve does not change, but shifts in parallel with the X axis. Therefore, a change in coefficient A corresponds to a shift in time (Fig. 3a). If, however, coefficient B increases, the inclination in the spurt area of this curve becomes steeper (Fig. 3b). Therefore, if coefficient B is small, the length increases only slowly. If B is large, the length increases remarkably during a short interval. During odontogenic formation of normally erupted teeth, the growth rate was slow in the early stage (e.g., appearance of the tooth germ on X-ray photographs) and then accelerated drastically, which was exhibited as an
123
Fig. 4 Relationship between Moorrees’ tooth formation stage and eruption of M1. a When we assumed that the tooth cervix of the upper second deciduous molar = 100, we obtained the above schematic representation of the axis of coordinates and the coordinate values of L1 (the dotted line indicates alveolar bone). b Location of M1 at each tooth formation stage and age
S-shaped curve. The logistic curve is thought to be a good tool for examination of skeletal development and growth, including tooth growth [30]. We attempted to fit the plot of the tooth formation stage or (C ? R)/C (Y axis) against the calendar age of the subjects (X axis) to a logistic curve defined by Y ¼ K=ð1 þ A eBX Þ, and the degree of fitness was rated at a significance level of 5 % [25, 30]. The coefficients A and B for the significantly fitting logistic curve were analyzed and weighed against the results that we reported. Logistic curves of M1 were compared with
Odontology Table 2 Frequency, laterality and sex differences of M1 Bilateral
Unilateral
Total no.
Right
Left
No. of case with M1 Male
14
3
3
20
Female
44
5
4
53
116
8
7
131
Tooth no. M1
those of U6 created from the data of Niimura [28] and Daito [31] classified by Moorrees’s tooth formation stage [27] as control. The software package used was STAT FREX 6. Eruption pathway of M1 at each tooth formation stage The primary second molars (E) and M1s were traced from panoramic X-ray photographs. We set the origin of the coordinate axes at the point of the distal cementoenamel junction of E. The X axis was the line containing both the mesial and distal cementoenamel junctions of E. We assumed that the tooth cervix of the upper first deciduous molar = 100 and created a schematic representation of the axis of the coordinates and the coordinate values of L1 (the dotted line indicates the mean alveolar bone). The Y axis was the line that crossed at right angles to the X axis and contained the origin point. We obtained coordinate data of M1 classified by tooth formation stage for evaluation of the eruption pathway, which was the center point between the apex of the mesial and distal cusps (L1) (Fig. 4a). The coordinate data of all patients who have M1 at each tooth formation stage were averaged, plotted, and superimposed. The location of M1 at each tooth formation stage and age were evaluated by longitudinal chase of point L1 (Fig. 4b).
differences in the frequency of M1 (Table 2). Among the 73 subjects (20 male and 53 female), M1 was unilateral in 15 (20.5 %) (right 8, left 7) and bilateral in 58 (79.5 %) (Table 2). Among male M1s, 70 % were bilaterally erupted, whereas the remaining 30 % were unilaterally erupted (right:left = 1:1). Among female M1s, 83 % were bilaterally erupted. The frequency of unilaterally female M1s was lower than that of male M1s (total 17 %, right 9.4 %, left 7.6 %). Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age The timing of tooth formation of M1 was examined and compared with that of U6 (Table 1). The speed of tooth formation before the R 1/4 stage was slow; however, it increased in the subsequent stages. Lower canines with normal eruption were used as the control teeth. Logistic curve fitting is a good tool for the examination of skeletal development and growth, including tooth growth. The tooth formation stage of M1 (Y) corresponding to the calendar age (X) was adapted to the logistic curve ðY ¼ K=½1 þ Ae BX Þ. For male subjects, coefficient A = 54.845 and B = 0.541; for female subjects, coefficient A = 51.131 and B = 0.529 (Fig. 5). Daito’s male subjects, coefficient A = 5.679 and B = 0.468; for female subjects, coefficient A = 5.820 and B = 0.481. Niimura’s male subjects, coefficient A = 7.018 and B = 0.421; for female subjects, coefficient A = 7.296 and B = 0.438. Figure 5 shows the logistic curves of M1 labeled by Moorrees’ tooth formation stage. Coefficient A was 54.845 and 51.131 and coefficient B was 0.541 and 0.529 in male and female subjects, respectively. Figure 6 shows the logistic curve of M1 classified by the ratio of crown height with root length to crown height. The development/growth curves of both male and female M1s were in conformity with the logistic curves at a significance level of \5 %.
Results Eruption pathway of M1 at each tooth formation stage Frequency of M1 Thirty-one of 2,001 patients from one institution among all patients born between 1974 and 1994 had M1 (1.55 %); i.e., 8 of 806 male patients (0.99 %) and 23 of 1,195 female patients (1.92 %). Approximately, 80 % of patients with M1 showed bilateral eruption. Of 31 patients with delayed eruption, 20 % (right 3, left 3) showed unilateral eruption (normal eruption on the opposite side). Laterality and sex differences of M1 Seventy-three patients with M1 from three institutions were examined to investigate laterality and gender
The eruption pathway of M1 was examined (Fig. 4a). When we observed a mesiodistal plane of the crown, the M1 in the early stages (e.g., it was grow up in R 1/4 from Ci) was distally inclined, and then gradually became mesially inclined during eruption through the alveolar bone, which was similar to the finding of Saijo [32], though it was cephalometrics. The migration speed of M1 exhibited an S-shaped curve (Fig. 4b). M1 erupted through the alveolar bone into the oral cavity at the Moorrees’ stage between R 1/4 and R 1/2; this stage exhibited the fastest eruption (Fig. 4b). A strong correlation was found between the M1 position and the ratio of crown height to observed root length on X-ray photographs or between the M1
123
Odontology Fig. 5 Logistic curves of delayed development of the upper first molars
Fig. 6 Logistic curve of M1 classified by ratio of crown height with root length to crown height
position and calendar age. Spearman’s rank correlation coefficient between the M1 position and the ratio of crown height to root length showed a correlation [bilateral coefficient of correlation, rs = 0.81 (Z value = 8.93)]. Spearman’s rank correlation coefficient also showed a
123
correlation between the M1 position and calendar age [bilateral coefficient of correlation, rs = 0.62 (Z value = 6.80)]. When we performed simple regression analysis between the root length/crown height and alveolar bone distances
Odontology
from M1 (point L1 to alveolar crest), a regression equation of L = 75.41 9 R/C - 87.25 was obtained (P \ 0.01). A regression equation of L = 21.21 9 Age - 196.28 was also obtained from the results of single regression analysis between calendar age and alveolar bone distances from M1 (point L1 to alveolar crest) (P \ 0.01). U6 was already fully erupted at this age; thus, we did not photograph it from an ethical standpoint. However, if we are presented with the opportunity, we investigate this issue in the future.
Discussion Frequency of M1 The frequency of delayed eruption of the maxillary M1 in 2,001 patients born from 1974 to 1994 in one institution with a clear total patient number and personal oral histories was 1.55 % (31 patients) in this study. This value was higher than those previously reported by Grover and Lorton in 1985 (0.01 %) and by Kramer and Williams in 1970 (0.25 %) [12, 13]. Laterality and sex differences of M1 Of the 73 patients with M1 from three institutions in this study, 15 (20.55 %) showed unilaterally delayed eruption and 58 (79.45 %) showed bilaterally delayed eruption. These frequencies are similar, but slightly higher than those reported by Rasmussen [33], who indicated that 9 of 10 cases of M1 were bilateral. Among the 73 subjects (20 male and 53 female subjects) from three institutions including the above-mentioned single institution in this study, the numbers of male and female subjects with M1s were 20 and 53, respectively, resulting in a sex ratio of 1:2.65 (Table 2). These sex ratios were almost identical to those in previous reports, indicating that the number of female M1s was two- to threefold higher than the number of male M1s [14, 33]. Among male M1s, 70 % were bilaterally erupted, whereas the remaining 30 % were unilaterally erupted (right:left = 1:1). Among female M1s, 83 % were bilaterally erupted, whereas the remaining 17 % were unilaterally erupted (right:left = 5:4). From these results, the female subjects had a higher incidence of bilateral M1s than did male subjects. Tooth formation of M1 and logistic curve fitting of the M1 tooth formation stage at each age The timing of tooth formation of M1 was examined and compared with that of U6 (Table 1). The timing of root
formation of M1 was, in all cases, between that of the permanent maxillary M1s and maxillary second molars [33]. Lower canines with normal eruption were used as control teeth. According to the report of Yamada [34], M1 might be early erupted second molars which exhibited degenerative characteristic, when the first molar was congenitally missing tooth. According to the report by Rasmussen, the tooth formation in the early stages was rapid, and that in the later stages of development became slower according to the odontogenic formation stages of Moorrees (Fig. 2). In contrast, the early stage of development, before Moorrees’ R 1/4 stage of tooth formation, was late; however, the tooth formation speed in the stages following R 1/4 increased in this study (Table 1). To evaluate the tooth formation stage as classified by Moorrees’ method, we applied the stage to the logistic curve calculated by Y ¼ K=ð1 þ A eBX Þ. If coefficient A in the logistic curve increases, the curve moves to the right and the formation will be late. If coefficient B decreases, the start of the curve becomes sudden and the formation speed increases. Because of the formation stage of M1, coefficient A was large and coefficient B was small, which shifted the start of the graph to the right and caused a sudden steep inclination. In other words, this graph lagged behind the tooth development, but the actual tooth formation was early. We evaluated conformity to the logistic curve in the same way as that shown by Niimura [28] and Daito [31] who evaluated the average Japanese tooth formation stage using Moorrees’ method. The results obtained in this study indicated that the hazard ratio for male and female subjects was \5 % and showed conformity to the logistic curve. These results are similar to those seen in other articles showing that the odontogenic formation speed was fitted to the logistic curve [35]. Calendar age at each tooth formation stage of M1 was delayed compared with that of U6. We checked the calendar ages of Moorrees’ stage Cli (initial cleft formation, Fig. 2) and Rc (root length complete) of M1 and U6 from Niimura’s data. We found that the age of Cli of M1 was 8.08 years (males) and 7.17 years (females), whereas the age of Cli of U6 was 5.08 years (males) and 4.92 years (females). In addition, Rc of M1 was 10.50 years (males) and 10.17 years (females), whereas Rc of U6 was 8.17 years (males) and 7.92 years (females). Using these findings, which indicated that development of M1 was 2–3 years later than that of U6, we fitted the data of tooth formation of maxillary M1s by Niimura and Daito for comparison with our logistic curves of the M1 tooth formation stage and ratio of crown height to root length (Table 1; Figs. 5, 6). From these results, the coefficients of the M1 and U6 logistic curves were the same after the fourth decimal point.
123
Odontology
Eruption pathway of M1 at each tooth formation stage
References
The eruption pathway of M1 was examined by the movement of point L1, the center point between the apex of the mesial and distal cusps of M1, on panoramic X-ray photographs. The X axis was the cementoenamel junction of the mesiodistal aspect of the second primary molar, and the Y axis was a tangent line of the second primary molar efferent to that traveling directly to the X axis. M1 was first located near the apex of the root of the second primary molar (Cr 3/4), but as it continued to erupt, it moved to the region of the cervix of the second primary molar (R 1/4); eruption rapidly continued into the oral cavity (between R 1/4 and R 1/2). When we examined this process in detail, R 3/4 showed rapid growth from R 1/4, and the gradient of the graph increased when we made it the average coordinate, creating an S-shaped curve. Spearman’s rank correlation coefficient and single regression analysis suggest that the M1 position during eruption and the calendar age or ratio of crown height to root length have relatively high correlations. These results suggest that the eruption timing of M1 can be predicted by the tooth formation stage and ratio of root length to crown height of M1 on panoramic X-ray photographs. To know the periods of deciduous teeth replacement and permanent teeth eruption is one of the most important information for better orthodontic treatment planning based on the evidence-based medicine. The prediction of these information can be obtained from the patients, e.g., individual growth state, cast models, and X-ray photographs. However, the prediction of eruption periods of delayed erupting teeth including M1 is difficult and needed lots of X-ray photographs compared with those of normal erupting teeth. Recently, the patients become sensitive to radiation exposure especially in Japan since the Grate Est Japan earthquake on March 11, 2011. In this paper, tooth development of M1 with eruption pathway at each stage is represented. These results should be helpful for the prediction of eruption timing of M1, and the decrease of the radiation exposure to the patients by the increase of the intervals of X-ray photographing. These data in this paper will hopefully plan the orthodontic treatment for both patient and clinician. Further studies are needed to realize more exact prediction of M1 eruption for construction of better orthodontic treatment planning.
1. Hahn GW. Edward Hartley Angle (1855–1930). Am J Orthod. 1965;51:529–35. 2. Andrew LF. The six keys to normal occlusion. Am J Orthod. 1972;62:296–309. 3. Barnett EM, Mehta JD. Olar growth stages—the keys to guiding occlusal development. J Am Dent Assoc. 1970;81(6):1360–8. 4. Proff P, Bayerlein T, Fangha¨nel J, Allegrini S Jr, Gedrange T. Morphological and clinical considerations of first and second permanent molar eruption disorders. Ann Anat. 2006;188:353–61. 5. Barberia-Leache E, Suarez-Clu´a C, Saavedra-Ontiveros D. Ectopic eruption of the maxillary first permanent molar: characteristics and occurrence in growing children. Angle Orthod. 2005;75:610–5. 6. Johnsen DC. Prevalence of delayed emergence of permanent teeth as a result of local factors. J Am Dental Assoc. 1977;94:100–6. 7. Demirjian A, Goldstein H, Tanner JM. A new system of dental age assessment. Hum Biol. 1973;45:211–27. 8. Demirjian A, Goldstein H. New system for dental maturity based on seven and four teeth. Ann Hum Biol. 1976;3:411–21. 9. Leurs IH, Wattel E, Aartman IH, Etty E, Prahl-Andersen B. Dental age in Dutch children. Eur J Orthod. 2005;27(3):309–14. 10. Gleiser I, Hunt EE Jr. The permanent mandibular first molar: its calcification, eruption and decay. Am J Phys Anthropol. 1955;13(2):253–83. 11. Dale JG. Interceptive guidance of occlusion with emphasis on diagnosis. Alpha Omegan. 1999;92(4):36–43. 12. Kramer RM, Williams AC. The incidence of impacted teeth. Oral Surg Oral Med Oral Pathol. 1970;29:237–41. 13. Grover PS, Lorton L. The incidence of unerupted permanent teeth and related clinical cases. Oral Surg Oral Med Oral Pathol. 1985;59:420–5. 14. Noda T, Takagi M, Hayashi-Sakai S, Taguchi Y. Eruption disturbances in Japanese children and adolescents. Pediatric Dental J. 2006;16:50–6. 15. Valmaseda-Castello´n E, De-la-Rosa-Gay C, Gay-Escoda C. Eruption disturbances of the first and second permanent molars: results of treatment in 43 cases. Am J Orthod Dentofac Orthop. 1999;116:651–8. 16. Ga´bris K, Tarja´n I, Csiki P, Konra´d F, Sza´deczky B, Ro´zsa N. Prevalence of congenital hypodontia in the permanent dentition and its treatment. Fogorv Sz. 2001;94(4):137–40. 17. Baccetti T. Tooth anomalies associated with failure of eruption of first and second permanent molars. Am J Orthod Dentofac Orthop. 2000;118:608–10. 18. Philipsen HP, Thosaporn W, Reichart PA, Grundt G. Odontogenic lesions in opercula of permanent molars delayed in eruption. J Oral Pathol. 1982;21:38–41. 19. Chintakanon K. Ectopic eruption of the first permanent molars: prevalence and etiologic factors. Angle Orthod. 1998;68: 153–60. 20. Bjerklin K, Gleerup A, Kurol J. Long-term treatment effects in children with ectopic eruption of the maxillary first permanent molars. Eur J Orthod. 1995;17:293–304. 21. Tomizawa M, Yonemochi H, Kohno M, Noda T. Unilateral delayed eruption of maxillary permanent first molars: four case reports. Int J Jpn Soc Pediatric Dent. 1998;20:53–6. 22. Nakano K, Matsuoka T, Takahashi A, Matsumura M, Sobue S, Ooshima T. Delayed development or congenital absence of a single first permanent molar in Japanese child patients. Int J Pediatr Dent. 1999;9:271–6.
Acknowledgments We are indebted to Dr. Iijima (Orthodontist in Mito, Ibaraki Prefecture), Dr. Ohtake (Orthodontist in Nagaoka, Niigata Prefecture), and Dr. Sugiyama (Orthodontist in Niigata) for their data and advice on this study. Conflict of interest of interest.
123
The authors declare that they have no conflict
Odontology 23. van Wijk AJ, Tan SP. Patterns of tooth agenesis. A numerical code for describing dental agenesis. Ned Tijdschr Tandheelkd. 2009;116:63–7. 24. Cre´ton MA, Cune MS, Verhoeven JW, Meijer GJ. Patterns of missing teeth in a population of oligodontia patients. Int J Prosthodont. 2007;20(4):409–13. 25. Sano N, Hasegawa Y, Iijima S, Terada K. Study of delayed development of the upper first molars. Okajimas Folia Anat Jpn. 2010;87(1):25–31. 26. The Japanese Society of Pedodontics. The chronology of deciduous and permanent dentition in Japanese children. Int J Jpn Soc Pediatric Dent. 1988;26:1–18 Japanese. 27. Moorrees CFA, Fanning EA, Hunt EE. Age variation of formation stages for ten permanent teeth. J Dent Res. 1963;42:1490–502. 28. Niimura K. Development of permanent tooth formation in children (in Japan). J Fukuoka Dental Coll. 1995;22:485–509 Japanese.
29. Jacoby H. The etiology of maxillary canine impactions. Am J Orthod. 1983;84:125–32. 30. Terada K, Saito I, Liu H, Hanada K. Longitudinal study on the length change of digital bones and mandible with a logistic curve. J Jpn Orthod Soc. 1995;54:413–24. 31. Daito M, Kawahara S, Tanaka M, Imai G, Nishihara G, Hieda T. Calcification of the permanent first molars observed in panoramic radiographs. J Osaka Dental Univ. 1989;23:45–55 Japanese. 32. Saijo K, Ogino C, Sasaki N, Saito F, Chiba H, Kamiyama K. Clinical study of ectopic eruption of the permanent first molars. Shoni Shikagaku Zasshi. 1990;28:1093–103 Japanese. 33. Rasmussen P. ‘‘9-year-molars’’ aberrantly developing and erupting: report of cases. J Clin Pediatr Dent. 1998;22:151–3. 34. Yamada H. Tooth size morphology of affected molars in individuals with congenitally missing first molar. Anthropol Sci Jpn Ser. 2010;118(2):83–96. 35. Goya HA, Satake T, Maeda T. Dental age in Japanese children using a modified Demirjian method. Pediatric Dental J. 2009;19(1):82–8.
123
