Timing and sequence of permanent tooth emergence in Hungarian children

doi:10.21203/rs.3.rs-3215333/v1

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Research Article

Timing and sequence of permanent tooth emergence in Hungarian children

https://doi.org/10.21203/rs.3.rs-3215333/v1

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Objectives

The aim of this study was to provide new population-specific standards for permanent tooth emergence in a large sample of Hungarian children.

Materials and methods

In this cross-sectional survey records of students from 8 randomly selected elementary schools and 2 kindergartens were examined. Data obtained from 2948 children (1487 boys and 1461 girls), aged between 4 and 15 years, were analyzed statistically. Probit regression analysis was used to calculate medians and percentiles of emergence ages for each tooth except 3rd molars for boys, girls and for the total sample.

Results

Permanent teeth were found to emerge earlier in girls than in boys. The difference was statistically significant for all teeth, except the mandibular central incisor. The greatest difference was observed in the case of mandibular canines. The emergence of mandibular teeth preceded maxillary ones, except premolars. No statistically significant differences were found between the right and left sides. The emergence sequence of permanent teeth was different for the two sexes.

Conclusions

This is the first time we report data on the eruption of permanent teeth from Hungary. The findings of this survey seem to correspond to earlier studies performed in Caucasian child populations. We experienced deviations compared to international standards.

Clinical relevance:

The population-specific data reported in this paper can serve as standards in paediatric dentistry, orthodontics and forensic age estimation when assessing permanent tooth emergence in Hungarian children.

permanent teeth

dental eruption

eruption time

eruption sequence

Hungary

Permanent tooth eruption is a complex and highly regulated process that occurs in humans during childhood and adolescence. While eruption means the whole process of how a tooth moves from its developmental place in the bone to its functional place with a largely axial movement, emergence only a part of this process which begins when the tooth breaks through the gingiva, appears in the oral cavity and ends when it comes into occlusion with its antagonist [1].

Knowing the timing and sequence of eruption is crucial for dentists for several reasons. With the help of this knowledge it is possible to monitor development, detect abnormalities, determine the optimal timing of preventive programs and treatments, identify impacted teeth, and educate patients. The evaluation of dental development and eruption can be useful not only in the field of pediatric dentistry but also in the disciplines of orthodontics, forensic medicine, anthropology and archaeology.

Although permanent tooth eruption is under significant genetic control [2, 3], environmental factors can also play a role in the timing and process of eruption. Among the genetically determined factors sex, race, ethnicity, and craniofacial morphology [4, 5] may influence permanent tooth eruption. The environmental factors that can have a significant impact on eruption are nutrition and BMI [6, 7], socioeconomic status [8, 9], caries in the primary predecessors [10, 11] and secular trends [12]. Additionally, certain systemic diseases and syndromes can also cause significant disturbances in tooth emergence [13, 14].

Studies examining eruption times of permanent teeth have reported some variations among different races and ethnic groups [15, 16]. While there might be general similarities in the eruption times and sequences across countries, having country-specific data allows for better clinical decision-making, cultural considerations, public health planning, and standardized dental education. It promotes accurate diagnosis, culturally sensitive care, and improved oral health outcomes for the population within a particular country.

In Hungary, the last survey regarding the eruption time of permanent teeth was conducted in the 1950s [17]. The social and economic changes that have taken place since then have also caused lifestyle changes, which have had an impact on children's general physical development and oral health. These positive changes, as a result of which children's growth accelerated, may have also caused changes in the eruption of permanent teeth. In the absence of up-to-date country-specific standards, we use international standards in patient care and education, which are based on studies conducted on Anglo-Saxon populations several decades ago [18–20]. According to our clinical experience, there is a discrepancy between the textbook data and the emergence times and sequences we have observed.

The objective of the present study was to determine the timing and sequence of permanent tooth emergence in Debrecen on the basis of a large, representative sample, to provide new standards specific to the Hungarian community.

Debrecen is the third largest and second most populous settlement in Hungary, approximately 220 km east of Budapest. In 2016, its population was 202,520. The ethnic composition of the city is relatively homogeneous, and the non-Caucasian permanent population does not even reach 0.1 percent of the total population. There are 43 kindergartens and 38 primary schools in Debrecen and its suburbs.

In Hungary, based on Ministerial Decree 26/1997. (IX.3.) on medical services in school, every child between the ages of 3 and 18 participating in organized education must undergo a mandatory school dental examination in every academic year. The dental screenings are performed with the written consent of the children's legal guardians, by trained specialists in Debrecen. The dental examinations are performed with a dental mirror and a dental probe under appropriate lighting, in a dental chair in school dental offices. During the examinations, the complete dental status is recorded. In addition to decayed, missing and filled teeth, healthy primary and permanent teeth are also documented in the status. Fully erupted teeth are marked with a dot, while partially erupted teeth - teeth whose crown broke through the gingiva in any part and is thus visible in the oral cavity - are marked with a wavy line. Occlusion, the condition of the gingiva and periodontium, and oral hygiene were also examined. The discovered dental, soft tissue and jawbone developmental abnormalities are all documented. X-rays are not taken during group dental screening examinations.

In our study, we reviewed the results of the dental examinations undertaken on 3132 children during the 2015–2016 academic year in 2 randomly selected kindergartens and 8 elementary schools in Debrecen. Access to and use of the data was authorized by the Regional and Institutional Research Ethics Committee of the University of Debrecen (permit number: 5613 − 2020).

Four- to fifteen-year-old children who participated in the school dental examination and had a complete dental record in the given school year were included in the study. Neither systemic diseases, nor physical or mental disorders were exclusionary reasons. There was no selection among the children based on nationality, social status, religion or whether the child was born in Debrecen. We excluded 175 children from the study because of their age (under 4 years or 16 years or older) and 9 because of their non-Caucasian origin. The sample for this cross-sectional study finally consisted of 2948 children (1487 boys and 1461 girls), representing 11.8 percent of Debrecen's 4-15-year-old population in 2016.

The information extracted from the patients’ dental records was transferred to a Microsoft Excel spreadsheet. The data table contained the identifier of each child, which was formed based on the initial letter of the name of the educational institution and the order of the screening, so that anonymity could be ensured in the future. We also recorded the child's sex, date of birth, and the exact time of dental examination. The chronological age of each child was calculated from the child’s date of birth to the date of examination. The records were divided into one-month age groups defined by the number of whole months each individual had lived.

We recorded the eruptive status of each permanent tooth in the data table. If we found a dot or wavy line marking in the child's chart (any part of the tooth emerged to the oral cavity) it was considered ”present” and marked with (1); unerupted teeth were considered ”absent” and marked with (0). Teeth extracted for orthodontic or other known reasons were recorded as “present”. If aplasia or impaction was suspected behind the absence, teeth were excluded and unrecorded. The 3rd molars were excluded from the study, as their eruption time is largely variable and the worldwide rate of agenesis was found to be over 20% [21].

The statistical calculations were made according to earlier studies on permanent tooth eruption [22]. A probit regression analysis was performed using the SPSS statistical program package (Version 17.0). Probit analysis is a statistical technique used to model and analyse categorical dependent variables, particularly when the response variable represents a binary outcome (e.g., present or absent; boy or girl; left or right). In probit analysis, the relationship between the independent variables and the probability of the event is modelled using a cumulative distribution function known as the standard normal (Gaussian) distribution. The dependent variable is assumed to be related to a linear combination of the independent variables through this cumulative distribution function. The estimation of the parameters of the model is performed using the maximum likelihood estimation technique.

We performed a preliminary study to determine whether a significant difference could be measured between the eruption times of teeth on the right and left sides. As no difference between the two sides for any tooth was greater than 0.05 percent and because these differences did not vary systematically, the data from the two sides were pooled.

Median emergence times and 5, 25, 75 and 95 percentiles were calculated for each tooth using 95% confidence intervals. The statistical significance level was set at 0.05. We examined the values characteristic of the entire population and separately by sex. The results obtained in months were finally converted into years.

Eruption sequences of permanent teeth by jawbone and sex were determined based on median emergence ages and 95% confidence intervals. The difference in eruption times was considered statistically significant if there was no overlap between the confidence intervals of the two examined median values. The dynamics of eruption and the probability of emergence of individual teeth were investigated using emergence curves.

Our preliminary tests did not find a significant difference between the emergence times of the teeth on the right and left sides, so pooled data were given for both sides. The median ages for the emergence of maxillary and mandibular teeth for each sex are shown in Table 1.

Table 1. Median ages of permanent tooth emergence in Hungarian boys and girls (in months)

	boys		girls		difference
	median	(95% CI)	median	(95% CI)	months	p-value
Maxilla
I1	85.7	(84.4–87.0)	82.1	(80.6–83.4)	3.6	< 0.001
I2	98.0	(95.5–98.6)	93.5	(91.9–95.1)	4.5	< 0.001
C	135.9	(134.4-137.5)	129.7	(128.1-131.3)	6.2	< 0.001
P1	121.4	(120.1-122.7)	119.4	(118.1-120.8)	2.0	0.009
P2	133.1	(131.6-134.7)	131.2	(129.6-132.7)	1.9	0.017
M1	76.4	(74.4–78.2)	73.7	(71.6–75.6)	2.7	0.004
M2	150.2	(148.5–152.0)	146.2	(144.5-147.9)	4.0	< 0.001
Mandible
I1	74.8	(72.3–76.9)	72.6	(69.8–74.9)	2.2	NS
I2	88.7	(87.0-90.4)	85.2	(83.4–87.0)	3.5	< 0.001
C	124.5	(122.5-126.9)	115.6	(114.2-117.2)	8.9	< 0.001
P1	123.5	(121.4-126.2)	119.4	(117.6-121.7)	4.1	< 0.001
P2	135.4	(133.9-136.9)	131.3	(129.9-132.8)	4.1	< 0.001
M1	75.2	(72.8–77.3)	72.3	(69.8–74.5)	2.9	0.042
M2	144.3	(142.2-146.5)	141.6	(139.5-143.7)	2.7	0.002
I1 - central incisor, I2 - lateral incisor, C - canine, P1–1st premolar, P2–2nd premolar, M1–1st molar, M2–2nd molar;
NS - not significant

Girls are advanced in permanent tooth emergence compared with boys, the difference in median emergence age ranges from 1.9 to 8.9 months. The difference was statistically significant (p < 0.05) for all examined teeth, except the mandibular central incisors (Table 1).

Examining the intermaxillary difference in the eruption of permanent teeth, it can be seen that although the lower teeth usually erupt earlier, in the case of boys the upper premolars precede the lower premolars. In the case of girls, we found no statistically significant difference between the eruption times of the lower and upper premolars. There was no significant difference between the eruption times of the lower and upper first molars in either sex.

The order of emergence of the teeth was different for the two sexes (Fig. 1.). Regarding the median eruption times, the emergence of permanent teeth started with the mandibular first molars in girls, but with the lower central incisors in boys. In the case of girls, the eruption of the canine preceded the eruption of the first premolar in the lower jaw and the second premolar in the upper jaw. In the case of boys, the eruption of canines in the maxilla preceded both premolars, while in the mandible it erupted after the first premolar.

If we examine not only the median values, but also the 95% confidence intervals, no significant difference can be shown between the eruption times of some teeth (Table 1). Since their 95% confidence intervals show a significant overlap, the lower central incisors and the lower and upper first molars erupt almost simultaneously in both sexes. The same is true for the upper canines and the second premolars on both jaws. In boys, the maxillary and mandibular first premolars and the lower canines erupt at the same time. In the case of girls, the lower and upper first premolars erupt with a negligible difference.

Based only on the median values, we can obtain an incorrect picture of the eruption sequence of permanent teeth. Emergence curves (Fig. 2.) clearly show that in the area of the supporting zone there can be a difference in the order of eruption between the so-called early (first 25 percentile) and late teethers (last 25 percentile). In the case of boys, the eruption curve of the lower canine and the first premolar almost overlap, a significant difference can only be seen in the case of early teethers, in whom the eruption of the first premolar precedes the canine. In the case of girls, there is a significant difference at and above the median values in favour of earlier erupting canines, but this difference does not exist in the case of early teethers. Examining the upper dental arch, in the case of boys, the second premolar erupts earlier than the canine, if we only look at the medians. The difference between the two emergence times is significant in the lower half of the eruption curve, however, after that, the significance disappears and after the 85th percentile, the eruption of the canine precedes the second premolar. In girls, the canine precedes the second premolar at the median value in the maxilla, although the difference is not statistically significant, becoming so only over 75th percentile. Interestingly, in the case of early teething girls, the previously mentioned emergence order is reversed.

Table 2. Percentiles of ages at emergence by sex and for the total sample (in years)

	boys						girls					total sample
	percentile						percentile					percentile						difference
	5th	25th	50th median	75th	95th	5th		25th	50th median	75th	95th	5th	25th	50th median	75th	95th	5–95		25–75
Maxilla
I1	6.03	6.69	7.14	7.60	8.25	5.73		6.38	6.84	7.30	7.95	5.84	6.52	7.99	7.46	8.14	2.30		0.94
I2	6.67	7.51	8.09	8.67	9.51	6.37		7.21	7.79	8.38	9.21	6.49	7.35	7.94	8.54	9.40	2.91		1.19
C	9.37	10.52	11.33	12.13	13.28	8.85		10.01	10.81	11.61	12.76	9.10	10.27	11.07	11.88	13.05	3.95		1.61
P1	8.08	9.28	10.12	10.95	12.16	7.91		9.12	9.95	10.79	11.99	8.00	9.20	10.04	10.88	12.08	4.08		1.68
P2	8.82	10.16	11.10	12.03	13.37	8.65		10.00	10.93	11.86	13.21	8.74	10.08	11.02	11.95	13.29	4.55		1.87
M1	4.92	5.77	6.37	6.96	7.81	4.70		5.55	6.14	6.73	7.58	4.80	5.66	6.25	6.85	7.70	2.90		1.19
M2	10.18	11.56	12.52	13.48	14.86	9.85		11.23	12.18	13.14	14.52	10.01	11.39	12.35	13.30	14.68	4.67		1.91
Mandible
I1	4.90	5.69	6.24	6.78	7.57	4.72		5.51	6.05	6.60	7.39	4.81	5.60	6.15	6.69	7.48	2.67		1.09
I2	6.06	6.85	7.40	7.94	8.73	5.77		6.56	7.10	7.65	8.44	5.88	6.69	7.25	7.81	8.62	2.74		1.12
C	8.86	9.75	10.37	11.00	11.89	8.12		9.01	9.63	10.26	11.15	8.40	9.36	10.03	10.70	11.67	3.27		1.34
P1	8.47	9.55	10.30	11.04	12.12	8.13		9.21	9.95	10.70	11.78	8.29	9.38	10.14	10.90	11.99	3.70		1.52
P2	8.97	10.33	11.28	12.23	13.60	8.63		10.00	10.95	11.90	13.26	8.80	10.17	11.12	12.07	13.43	4.63		1.90
M1	4.87	5.69	6.27	6.84	7.66	4.63		5.45	6.02	6.59	7.41	4.74	5.57	6.14	6.72	7.55	2.81		1.15
M2	9.63	11.05	12.03	13.01	14.42	9.41		10.82	11.80	12.78	14.19	9.53	10.93	11.91	12.89	14.29	4.76		1.96
I1 - central incisor, I2 - lateral incisor, C - canine, P1–1st premolar, P2–2nd premolar, M1–1st molar, M2–2nd molar

Table 2 shows the 5th, 25th, 50th (median), 75th and 95th percentiles of emergence times for the total sample and separately for boys and girls. In 5% of the examined children the first teeth (mandibular first molars and central incisors, maxillary first molars) erupt at the age of 4.7–4.8 years. Even in children who change their teeth at the latest, the eruption of the first permanent teeth begins by the age of 7.5 years. Children in the 95th percentile erupt their last permanent teeth (maxillary second molars) at 14.7 years of age, while children in the first 5th percentile have 28 erupted permanent teeth by the age of 10.

The mandibular second molar takes the longest to erupt (4.8 years), while the maxillary central incisor erupts within the shortest time interval (2.3 years). The most intense period of tooth eruption, accounts for approximately 40% of the total eruption period, seen between the 25th and 75th percentiles (Table 2). This takes approximately 1 year for central and lateral incisors and first molars, and 2 years for other teeth. The total time interval (between the 5th and 95th percentiles) of the emergence can be calculated as the time between the 25th and 75th percentiles plus/minus 1 year. The only exceptions to this are the longest erupting second premolars and second molars, where plus/minus 1.5 years applies.

In this cross-sectional study of 4- to 15-year-old children living in Debrecen, Hungary, we determined the timing and sequence of emergence of permanent teeth and first compared the results with a previous representative Hungarian survey. Few publications have dealt with the time and sequence of eruption of the permanent teeth of Hungarian children. Adler and co-workers [17] investigated the eruption in the 1950s on a large, representative sample in rural settlements. Since they examined elementary school children who started school after their 6th birthday and thus already had a few permanent teeth, they could not determine the eruption time of the first teeth to erupt (first molars and lower central incisors).

Comparing the results of our present study with those of more than 60 years ago [17], it is difficult to draw firm conclusions, since the methodology of the two studies, primarily the statistical analysis, is not exactly the same, but the emergence ages of the present study are apparently earlier. The most evident differences are seen in the case of teeth of the second transitional phase. In boys, the change is greater for all teeth, and the eruption of the teeth in the upper supporting zone is 0.4–0.5 years earlier, while the emergence of the lower canine and premolars is accelerated by 0.6–0.8 years. This acceleration can be explained by the acceleration of physical development and the increased body mass index observed in Hungarian children during the past 60 years [23]. It is interesting that the eruption of the second molars was delayed. The delay in boys is only 0.1–0.2 years, which may be due to methodological differences or measurement errors, but the lower second molar in girls erupted 0.53 years later than 60 years ago. Eskeli et al. [12] also experienced the extension of the mixed dentition period. We must take this phenomenon into account when scheduling preventive interventions and planning orthodontic treatments.

Regarding the emergence order of the teeth, in the upper jaw, the sequence in boys was the same as that observed 60 years ago [17]. In the case of girls, previously the median eruption time of the upper canine and the second premolar was the same, while currently, the second premolar precedes the canine. In the mandible, in the previous study of Adler [17], the median eruption times of the second premolar and the second molar in girls were identical, while in boys the emergence of the second molar preceded the second premolar. The minor changes that have occurred in the sequence of eruption since the mid-1950s can be clearly explained by the improvement of the caries situation in Hungary, the decrease in the caries intensity and the fewer early primary molar extractions [24].

Comparing our results with the findings of international publications, it can be said that we found agreement at several points and differences at others. For the comparison we used international studies with similar methodologies. There may be differences between individual studies in the use of statistical measures. Several authors assume that the distribution of emergence times of teeth corresponds to a Gaussian (normal) distribution [17, 25]. If we assume a normal distribution, then both the arithmetic mean and the median reliably describe the time of eruption. A significant part of scientific publications examining eruption times give the mean (average) eruption time of the teeth [26–29], while the others determine the median values [30–39], when the given tooth erupted in 50% of the studied individuals. If the data are not heavily skewed or do not have extreme values, the mean may be a suitable measure of central tendency. However, if the data are skewed or contain outliers, the median may provide a more representative value that is not influenced by those extreme observations. However, the median results in lower age values than the mean [40]. This is confirmed by Leroy at al. [34], who calculated both values and found that the medians were 0.03–0.1 years lower than the mean values. Since in our work we determined the median of emergence times, we selected those examining medians from international studies for comparison (Tables 3 and 4).

Table 3 Comparison of the median emergence ages of permanent teeth in boys

	Caucasian									Asian		African
	HUN	CRO	LTU	CZE	FIN	BEL^a	GBR	JOR	AUS^c	MAS	KOR^a	UGA^b
	present	[30]	[31]	[32]	[33]	[34]	[35]	[36]	[37]	[38]	[39]	[28]
Maxilla
I1	7.1	7.5	6.9	7.0	6.8	7.1	7.4	7.3	7.4	7.2	7.4	6.3
I2	8.2	8.5	8.0	8.0	8.1	8.3	8.7	8.5	8.6	8.6	8.5	8.5
C	11.3	11.6	11.1	11.3	11.3	11.5	12.0	11.6	11.8	11.0	10.9	10.8
P1	10.1	10.3	9.9	9.5	10.9	10.7	11.2	10.5	11.3	9.5	9.7	9.6
P2	11.1	10.8	10.8	11.0	11.7	11.6	12.3	11.4	12.1	10.4	10.5	9.5
M1	6.4	6.8	6.4	6.9	6.3	6.3	6.8	6.4	6.7	6.4	6.6	6.4
M2	12.5	12.6	12.3	12.7	12.4	12.3	12.8	12.6	12.7	12.2	12.8	11.0
Mandible
I1	6.2	6.6	6.1	6.4	6.0	6.3	6.6	6.5	6.6	6.4	6.5	6.5
I2	7.4	7.7	7.2	7.3	7.1	7.4	7.8	7.5	7.8	7.5	7.5	5.8
C	10.4	10.9	10.4	9.4	10.5	10.6	11.0	10.6	11.0	10.2	10.2	10.1
P1	10.3	10.6	10.1	10.0	10.7	10.7	11.2	10.5	11.2	9.9	10.0	10.0
P2	11.3	10.9	11.1	10.9	11.6	11.7	12.2	11.7	12.1	10.9	10.9	10.8
M1	6.3	6.6	6.2	6.5	6.2	6.3	6.8	6.2	6.6	6.0	6.1	6.0
M2	12.0	11.9	11.7	12.4	12.0	11.8	12.3	12.2	12.2	11.4	11.7	11.5
^alongitudinal study, ^bmean values, ^cmixed population with Caucasian predominance
HUN – Hungary, CRO – Croatia, LTU – Lithuania, CZE – Czech Republic, FIN – Finland, BEL – Belgium, GBR – Great Britain, JOR – Jordan, AUS – Australia, MAS – Malaysia, KOR – Korea, UGA - Uganda

Table 4. Comparison of the median emergence ages of permanent teeth in girls

	Caucasian									Asian		African
	HUN	CRO	LTU	CZE	FIN	BEL^a	GBR	JOR	AUS^c	MAS	KOR^a	UGA^b
	present	[30]	[31]	[32]	[33]	[34]	[35]	[36]	[37]	[38]	[39]	[28]
Maxilla
I1	6.8	7.2	6.8	6.9	6.8	6.9	7.2	7.1	7.2	7.1	7.2	6.2
I2	7.8	8.3	7.6	7.6	7.6	7.9	8.2	8.1	8.2	8.5	8.0	7.2
C	10.8	11.1	10.5	10.4	10.8	11.0	11.4	11.1	11.2	10.5	10.0	9.3
P1	10.0	10.1	9.5	9.4	10.3	10.4	10.9	10.0	10.8	9.2	9.2	9.3
P2	10.9	10.7	10.6	10.9	11.6	11.4	11.8	11.0	11.7	10.2	10.1	10.1
M1	6.1	6.9	6.3	6.6	6.1	6.2	6.5	6.2	6.5	6.2	6.4	5.3
M2	12.2	12.4	12.1	12.5	11.9	12.0	12.4	12.3	12.3	12.0	12.1	10.7
Mandible
I1	6.1	7.2	5.9	6.2	5.9	6.2	6.4	6.3	6.3	6.3	6.1	5.6
I2	7.1	7.2	6.9	7.2	6.8	7.1	7.4	7.3	7.4	7.3	7.2	6.8
C	9.6	10.0	9.6	9.1	9.7	9.7	10.3	9.8	10.1	9.5	9.4	9.7
P1	10.0	10.4	9.7	9.7	10.3	10.3	10.7	10.1	10.6	9.7	9.6	9.2
P2	10.9	10.9	10.6	10.6	11.3	11.4	11.9	11.2	11.7	10.6	10.5	10.2
M1	6.0	7.0	6.0	6.2	6.1	6.2	6.5	6.1	6.3	6.0	6.1	5.2
M2	11.8	11.8	11.3	11.8	11.6	11.6	12.0	11.7	11.8	11.0	11.3	10.3
^alongitudinal study, ^bmean values, ^cmixed population with Caucasian predominance
HUN – Hungary, CRO – Croatia, LTU – Lithuania, CZE – Czech Republic, FIN – Finland, BEL – Belgium, GBR – Great Britain, JOR – Jordan, AUS – Australia, MAS – Malaysia, KOR – Korea, UGA – Uganda

There is no huge difference between the major anthropological races in terms of the time and sequence of eruption of permanent teeth, however, some differences are observed when examining the beginning and duration of eruption of permanent teeth. In Ghana Houpt et al. [41] and in Uganda Krumholt et al. [42] found that the eruption of permanent teeth of Negroid (African) children begins 1-1.5 years earlier than that of Caucasians, and a significantly shorter time elapses between the first and second phases of tooth transition. Forty years after the first surveys [28], the time advantage decreased, but the difference was still significant, primarily in the area of the supporting zone (Tables 3 and 4). According to Dhamo at al. [15], the reason for this is probably the earlier onset of puberty in Africans. Mongoloids (Asian) also show differences compared to Caucasians. The period of dentition of the Asian children is between the relatively long period of the Caucasian group and the very short total period of the Negroid group. According to the measurements of Hassanali and Odhiambo [16] permanent teeth erupted earlier by 0.2–0.7 years in African children than in Asians. Nizam and co-worker’s [38] studies in Malaysia produced similar results to ours from several points of view, but in the area of premolars the eruption times were significantly earlier and the lag period between the two phases of tooth transition was less than half of that experienced in our study. Kim et al. [39] in Korea also report a very short resting period and a relatively early eruption of the premolars. Surveys in Australia [37, 40] mostly examined a mixed population, where the majority of subjects had European ancestry, and it is not surprising that the Australian data are similar to the UK data (Tables 3 and 4). Studies conducted on indigenous (Australoid) people are rarer and have a smaller sample size. Brown [43] reported, that compared to those of European descendants, in the case of Aboriginal children teeth of the second transitional period erupted earlier and had a shorter resting time between the two phases, which is similar to that found in other non-European populations. Thus, a genetic and geographic approach of ancestry may help to explain the variations in dental development and eruption [15].

Due to minor differences that could be measured between children of different geographic ancestry, for the sake of the homogeneity of the study group, we excluded non-Caucasian subjects from the study. Our results show that the eruption time of the Hungarian subjects corresponded to the results of several studies conducted on Caucasian children [30–37]. Examining the eruption time of the permanent teeth of children with Caucasian ancestry (Tables 3 and 4), we found that there was a difference of 0.4–1.8 years between the lowest and highest eruption median values of individual teeth. The largest deviation of the values (more than 1 year) was observed for the premolars and lower canines. Our values are most similar to Lithuanian [31] and Jordanian [36] data. Among Caucasians, permanent teeth erupt at the latest in the United Kingdom [35]. The Hungarian data are very similar to the continental data, but differ the most from those from the British Isles. This can mostly be explained by genetic differences, since lifestyle and environmental differences within urbanized Europe are constantly decreasing.

Examining the emergence times separately by sex, it can be seen that there is a significant difference between boys and girls. In our survey, we found a statistically significant difference between the sexes for all teeth; the only exception was the mandibular central incisor. The vast majority of international studies confirm a female advantage, although in the case of some teeth (usually first molars and lower central incisors) the difference was not found to be significant [30, 36]. However, the Pakistani studies of Khan [44] found no significant difference between the sexes, except for the upper second premolars and the lower right canine. Kim's [39] longitudinal study in Korea did not find a significant difference between the eruption time of boys and girls for any tooth. There is no certain explanation for the sex difference in the eruption time of individual teeth, but it can be assumed that the exfoliation of the primary teeth and the eruption of permanent teeth of girls, which usually starts earlier, is a symptom of the general developmental difference between the sexes [13].

Regarding the eruption sequence of the teeth, which is usually determined based on the median/mean values, there were similarities and differences between the orders we observed and the findings of international studies. The first transitional phase of mixed dentition is usually initiated by the emergence of the first molars and then the central incisors in both sexes. This order prevails in the majority of international studies [26, 27, 30, 37–39, 45]. In a minority of surveys [31, 33–35, 46], the lower central incisor precedes the first permanent molar in both sexes. If only the median values are used to establish the order of emergence, then the lower central incisor of the Hungarian boys erupted earlier than the first molar, similar to the case of the Czech boys [32]. If we examine the emergence curves of the central incisor and the first molar (Fig. 2), it is clearly visible that in the case of the lower teeth the two curves almost completely overlap each other, the two teeth erupt almost completely at the same time for both sexes, as in the Jordanian studies of Shaweesh [36].

In the supporting zone, in our survey, the mandibular canine erupted later than the first premolar but earlier than the second premolar in boys. This order is not common, only Eastern European Lithuania [31] Middle Eastern Jordan [36], Syria [29] and Asian Malaysia [38] have reported similar results. The maxillary order of the boys, although it does not match that found in any Western or Northern European country, is similar to reports from Central and Eastern Europe [30–32] and to those reported from Syria [29], Jordan [36], Lebanon [45], Iran [46] and Malaysia [38]. The eruption sequence of the permanent teeth of girls is much more similar to that experienced in Western Europe [33–35], and in Central and Eastern Europe [31, 32], and it is also the same as the Greek [26], Turkish [27] and Australian [37] sequences.

In the present study, we experienced a temporal difference in the emergence of the teeth of the lower and upper jaws. Usually the mandibular teeth precede the maxillary ones, but in the case of boys, the upper premolars erupted earlier than the lower ones. In the case of girls, we found no statistically significant difference between the eruption times of the lower and upper premolars. Some of the authors of the reviewed publications came to the conclusion that all lower teeth erupt before their upper pair [27, 33, 45, 46], while others have found that this is not true for the area of premolars, the upper 1st and 2nd premolars either erupt earlier than the lower ones [29–32, 38, 44] or almost at the same time [36]. There was no significant difference between the eruption times of the lower and upper first molars in either sex. This is in complete agreement with the findings of Leroy [34], Almonaitiene [31] and Shaweesh [36].

Examining the symmetry of the eruption of the permanent teeth in the right and left halves of the jaw, we did not find any significant differences between the sides. This is in full agreement with the majority of studies [31, 32, 36–38, 45]. According to Leroy et al. [34], the eruption of permanent teeth did not occur symmetrically, and individual teeth could also erupt asymmetrically, but the differences between eruption times were not statistically significant. It is interesting that where asymmetry was noticed, the teeth on the left usually erupted earlier [28, 34]. On the contrary, a study investigating the laterality of motor functions found that, like right-handedness, earlier eruption on the right side is more common [47]. According to Lo and Moyers [48], the laterality of eruption is symmetrical, except for those cases where the deciduous teeth are removed prematurely due to caries, and thus the eruption of the permanent teeth is accelerated. The symmetry of the eruption can be explained by the fact that the endocrine effect is equally strong on the left and right sides, so contralateral teeth, similar to symmetrical organs, form at the same time.

Comparing our results with international standards, we can see obvious differences. The eruption times presented in the AAPD Reference Manual [18] are based on Logan and Kronfeld's studies [49], with only minimal changes since 1933. This table does not provide medians, but a range, which may correspond to the range between the 25th and 75th percentiles. Textbooks provide these data or the same data with minimal modifications [19]. In his textbook of orthodontics, Proffit [20] reports the median values for the eruption of permanent teeth. The Hungarian data are very similar to these, although they are somewhat earlier. The upper central and lateral incisors, the upper first premolars and the lower lateral incisors erupt approximately 0.25 years earlier. The difference in the case of the lower and upper canines is half a year.

In comparison with the AAPD standards [18], it can be seen that in the case of Hungarian children, the eruption of the upper central and lateral incisors, the lower first and second premolars and the lower and upper second molars is 0.5-1 year earlier. In the case of the upper canine and first premolar, not only is the eruption earlier, but the defined 1-year emergence interval is also narrow. Eruption is likely at the age of 10–12 in the case of the upper canine, and between 9 and 11 years in the case of the upper first premolar, as opposed to 11–12 and 10–11 years given by the AAPD.

Reference tables usually give the time interval between the 25th and 75th percentile as the standard eruption time and define the physiological range in plus/minus 1 year. Examining the eruption probability curves, it can be seen that it is important to modify the commonly used standards, since the eruption of individual teeth does not occur in the same time interval. Ekstrand et al. [50] also showed that the length of the emergence period of the first molar is shorter than that of the second molar, the difference between them being at least 1 year. In the case of second premolars and second molars, instead of the generally applied plus/minus 1 year, we have to count plus/minus 1.5 years to cover the time interval between the 5th and 95th percentiles.

There are some limitations of our study, most of which originate from the cross-sectional design. First, there was a lack of radiographic examination to confirm dental agenesis. The protocol of school screening examinations does not require routine X-ray to be taken, so we could not verify the origin of the missing teeth in some of the studied cases. It is possible, that occasionally congenitally missing teeth may have been registered as unerupted. As statistical methods assume that all teeth will erupt at some point, if we do not exclude congenitally missing teeth with radiological examination it may lead to an overestimation of the time of eruption [25]. Extracted teeth or teeth lost in an accident could also be mistakenly registered as not erupted, if no information was found about the previous events in the available retrospective data. Fortunately, we found all anamnestic data in the patients’ files, except for children newly arrived at educational institutions. We can assume that incorrectly coded cases did not bias our results, since the agenesis of permanent teeth is only 2.06% in Hungary [51] and our sample size was reasonably large.

Another limitation is that different recorders carried out the examinations and filled out the examination sheets without intra- or interexaminer reliability tests. The examined kindergartens and elementary schools belonged to four paediatric dentists who had the same education and several years of clinical experience. In addition, the binary type of examination outcomes and the routinely used method of recording minimised the possibility of error. Being a retrospective study, we saw no point in carrying out the reliability tests afterwards.

The third limitation is the urban nature of the study population. Hungarians are ethnically relatively homogenous, but in lifestyle the difference between urban and rural residents still exists. Urban residents still have an advantage in terms of caries frequency and intensity and there are significant differences in the available dental services, although the difference has somewhat decreased in recent decades [24]. Our study sample does not represent the entire Hungarian population. Since our data were obtained on urban children, these can only be cautiously applied to rural people.

Finally, due to the cross-sectional design we could not investigate the effect of early deciduous tooth extractions on eruption.

The data presented in this paper provide the first standards for permanent tooth emergence specific to Hungarian children. Permanent teeth were found to emerge earlier in girls, than in boys. The difference was statistically significant for all teeth, except the mandibular central incisor. The emergence of mandibular teeth preceded maxillary ones, except premolars. The emergence sequence of permanent teeth was different for the two sexes. The provided sex-specific standards by 5th, 25th, 50th, 75th and 95th percentiles may help in assessing children with delayed emergence time and may help to decide when it is necessary to take an X-ray due to suspicion of agenesis.

The measured eruption times also draw attention to the fact that a significant number of children have their first permanent teeth before they start elementary school, so unlike the practice in Hungary so far, group prevention programs must start in kindergarten.

The findings of this survey seem to correspond to earlier studies performed in Caucasian child populations, but we experienced deviations compared to international standards. In the future, it would seem appropriate to use this population-specific data set in patient care, education and forensic age determination of Hungarian children and adolescents.

Acknowledgement The authors would like to express their gratitude to Gabriella Kovalecz for her constructive criticism and helpful suggestions.

Author contribution The study was conceived and designed by Judit A. Nemes. Data collection was performed by Zsuzsa Kapusi-Papp and Judit A. Nemes. Statistical analysis was performed by János Máth. All authors interpreted the data. The first draft of the manuscript was written by Zsuzsa Kapusi-Papp and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding Open access funding was provided by the University of Debrecen.

Data Availability Data are available upon request.

Ethical approval This retrospective chart review study involving human participants was in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Access to and use of the data was approved by the Regional and Institutional Research Ethics Committee of the University of Debrecen (permit number: 5613-2020.).

Conflict of interest The authors declare no competing interests.

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Timing and sequence of permanent tooth emergence in Hungarian children

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