Pergamon

PII: S0003-9969(97)00012-5

Archs oral Biol. Vol. 42, No. 5, pp. 401-406, 1997 ~ 1997 Elsevier Science Ltd. All rights reserved

Printed in Great Britain 0003-9969/97 $1;7.00 + 0.00

SEQUENCE OF ERUPTION OF DECIDUOUS DENTITION IN A CHILEAN SAMPLE WITH DOWN'S SYNDROME

A. ONDARZA, ~'* L. JARA, 2 P. MUNOZ ~ and R. BLANCO 2

'Department of Experimental Morphology, Faculty of Medicine, University of Chile, Casilla 70079, Santiago 7, Chile and -~Department of Cell Biology and Genetics, Faculty of Medicine, University of

Chile, Casilla 70079, Santiago 7, Chile

(Accepted 14 January 1997)

Summary--The eruption of the deciduous teeth in Down's individuals is reportedly delayed, but the extent of delay in comparison to normal children has been little studied. The eruption characteristics of the deciduous teeth in a sample of Chilean individuals with Down's syndrome were compared with those of the normal Chilean population. The sample consisted of 255 Down's individuals (all with tris- omy 21), 127 males and 128 females. Boys with Down's syndrome showed significantly delayed eruption in six teeth: in the maxilla the right central incisor and right and left lateral incisors, and in the mand- ible the right central incisor and right and left canines. Girls with Down's syndrome showed significant delays in the eruption of 11 teeth: in the maxilla the right and left lateral incisors, right and left canines and first left molar, and in the mandible the left central incisor, right and left lateral incisors and canines and second right molar. The chronological sequence of eruption in Down's children was not completely different from that of normal individuals. With a few exceptions no significant departures from Gaussian distribution were found in the age of eruption among both normal and Down's individ- uals. The variance was significantly larger in cases of Down's syndrome. © 1997 Elsevier Science Ltd

Key words: deciduous teeth, sequence of eruption, Down's syndrome.

INTRODUCTION

Tooth eruption is a process that exhibits precise timing and bilateral symmetry. Genetic, systemic and environmental factors are implicated in the control of the morphogens that carry out the com- plex sequence involved in normal odontogenesis and, therefore, in dental eruption (Stewart and Poole, 1982). Biochemical studies show that during eruption, cells, proteins and enzymes change in the dental follicle, and several growth factors and pro- teins known to accelerate or retard eruption have been identified (Marks, Gorski and Wise, 1995).

Delayed eruption of systemic origin is associated with many genetics conditions such as Down's and Turner's syndromes, cleidocranial dysplasia, hemifa- cial atrophy and mucopolysaccharidosis (Smith, 1976). In Down's syndrome, eruption of the decid- uous and permanenl dentitions is delayed as com- pared with the general population (Brousseau, 1928, as cited by Cohen and Cohen, 1971; Oster, 1953; Levinson, Friedman and Stamps, 1955; Spitzer and Quilian, 1958; Cohen and Winer, 1965; Barkla, 1966; Otero and Sznadjer, 1966, Roche and Barkla, 1964, 1967; Spitzer, 1967; Orner, 1971, 1973, 1975; Cohen and Cohen, 1971; Molina, Vifias and

*To whom all correspondence should be addressed.

Garcia-Godoy, 1982; Garcia and P6rez, 1985; Fischer-Brandies, 1989; Jara et al., 1993; Roger and Coleman, 1994). Several studies report a delay in the timing and sequence of eruption of the decid- uous dentition in Down's syndrome. Levinson et al.

(1955) found that in the deciduous dentition the eruption of the molars precedes that of the incisors in these individuals up to the age of 5 years. Roche and Barkla (1967), in a study of 48 Australian Down's children, found that the time of eruption of the deciduous teeth was retarded as compared to the general population, with the exception of the upper first and second molars and lower second molars. Fischer-Brandies (1989) studied the erup- tion of the deciduous dentition in 93 trisomics, ana- lysing the eruption of 842 teeth, and concluded that on average there was a delay of 6 months, the first molars being the first or second teeth to erupt. The sequence of eruption was very variable and it was impossible to establish differences between sexes or between right and left hemiarches.

In spite of the available literature, few investi- gators have documented case control observations involving rigorous statistical procedures analysing the chronology and sequence of eruption of the deciduous dentition in children with Down's syn- drome. Our objective now was to determine the pat- tern of eruption of the deciduous dentition in a

401

402 A. Ondarza et al.

sample of Chilean individuals with Down's syn- drome and to compare it with that of the normal Chilean population.

MATERIAL AND METHODS

Down's individuals were randomly selected from the population attending Escuelas Especiales E-497, F-86 and F-296, Escuela Diferencial E-469 (state schools for mentally retarded individuals located in the South Metropolitan Area of Santiago), and Cindy College and Coocendes (private schools for handicapped children). The individuals from state schools comprised 94.12% of the sample and belonged to the same socioeconomic level; individ- uals from Cindy College and Coocendes represented 5.88% of the sample and belonged to a somewhat different socioeconomic level, but no significant statistical differences were found between the two groups.

The Down's sample consisted of 255 individuals with trisomy 21, 127 males and 128 females, with ages ranging between 4 and 84 months. The date of birth of each child was obtained from the personal records of the respective schools. The data for the normal population were obtained from a previous report by Palomino, Blanco and Cisternas (1980) which used the same clinical and statistical methods described in the present study. This sample con- sisted of 445 children (220 males and 225 females) selected from the population attending the Center for Growth and Development, North Health Area, Santiago, Chile, whose ages ranged between 1 and 72 months. The sample was divided into 14 age groups with an interval of 6 months between groups, beginning at 4 months and ending at 84 months. This division was made to enable compari- son with previous studies, especially those on the normal eruption times of the deciduous dentition in the Chilean population.

A single investigator examined the entire sample (P.M.). The examination procedure for all partici- pants was uniform: it entailed the use of a dental mirror and probe with the patient seated in a dental chair facing a window with good natural light. The survey recorded the presence or absence of teeth. A tooth was considered erupted when any portion of its crown had pierced the gum. This criterion is commonly used in tooth eruption and gives a yes- no answer which facilitates statistical analysis.

A preliminary record was made of the number of boys and girls in each group. The number of erupted teeth in each group was then recorded for each tooth, The proportion of erupted teeth in each age group was computed from these data and trans- formed into probit values by a computer program. Probit analysis is basically an iterative technique involving successive approximations to give a line of best fit as tested by least-square methods for a given series of plotted values. The program also

gives the median emergence age (the age at which eruption has occurred in 50% of the population), the SD and the SE of the estimate (Finney, 1952). The effective number needed to perform statistical anaylses was obtained by dividing the variance (SD 2) by the square of SE. The actual number of individuals in each age group cannot necessarily be used because the number must be weighted accord- ing to the amount of information. Irregular distri- butions in the proportions of erupted teeth produced very large variances and unreliable esti- mates of variables. The program identifies these as non-Gaussian distributions after a xZ-test for good- ness of fit to a normal distribution. This occurs mainly when the proportions are close to 100 or 0%. Irregular distributions were not considered further in the analysis.

The age of eruption for each tooth was compared with that of a normal population studied in the same way (Table 4). The Student t-test with Welch's correction was calculated by the difference between both means divided by the pooled SE (unknown and unequal variances). We have used Welch's correction in order to reduce the estimation errors of the degrees of freedom (Remington and Schork, 1970). The degrees of freedom were calcu- lated with the effective number.

The Student t-test was used to compare the mean for the age of eruption of each tooth between Down's and normal individuals and the F-test to compare variances between both samples; we chose significance at the 5% level.

RESULTS

Table 1 shows the age and sex distribution of the sample of Down's children. Table 2 shows the mean age of eruption (in months), with its SD and SE for each decidual tooth for boys and girls. The means with very large SEs were not considered in subsequent analyses.

Table 1. Distribution by age and sex of a sample of the Chilean population with Down's syndrome

Age (months) Boys Girls Both sexes

0 6 3 2 5 7-12 6 7 13 13-18 6 6 12 19-24 8 7 15 25-30 12 11 23 31 36 9 13 22 37-42 11 11 22 43 48 8 14 22 49 54 18 13 31 55 60 11 10 21 61-66 7 8 15 67-72 10 6 16 73 78 11 10 21 79 84 7 10 17 Total 127 128 255

Down's children and deciduous teeth eruption 403

Table 2. Means, SDs and SEs (by age in months) of erup- tion of the deciduous ~:eeth in a sample of Chilean children

with Down's syndrome

Tooth Sex x SD SE

5.5 M 127.66 5.645 2.042 F 129.12 6.067 1.838

5,4 M 17.21 3.611 1.499 F 13.28 ** **

5.3 M 12.02 32.10 19.48 F 30.70 6.454 1.447

5.2 M [ 8.44 9.652 2.424 F 17.31 14.42 3.625

5.1 M 15.27 5.515 1.797 F !5.16 9.340 4.778

6.5 M 27.66 5.645 2.042 F 29.60 5.649 1.637

6.4 M 17.21 3.611 1.499 F 25.87 14.34 5.253

6.3 M 22.16 13.85 8.260 F 30.60 7.249 1.586

6.2 M 18.13 10.01 3.422 F 17.31 14.42 3.625

6.1 M 9.77 30.62 10.25 F 15.16 9.340 4.778

8.1 M 14.15 11.82 3.909 F 7.515 17.75 16.02

8.2 M 7.569 35.24 13.75 F 27.59 19.01 3.976

8.3 M 25.87 7.667 2.046 F 27.83 11.25 2.633

8.4 M 17.21 3.611 1.498 F 57.38 -32.74 146.18"

8.5 M 27.71 5.562 1.487 F 28.83 3.454 1.127

7.1 M 11.07 10.76 4.288 F 12.02 7.286 2.699

7.2 M 9.313 30.61 11.57 F 24.66 23.86 5.447

7.3 M 2,5.65 7.431 1.906 F 23.80 10.60 2.360

7.4 M 1'7.88 5.166 1.930 F -322.4 262.17 2939.2*

7.5 M 2'7.71 5.562 1.487 F 32.31 13.43 4.382

*Not considered for further analysis due to large SE. **Data did not fit the Gaussian distribution

Down ' s girls began the eruptive sequence of decidual teeth as fol)ows: first the lower right cen- tral incisor at 7.51 months , second the lower left

cont ra l incisor at 12.02 months , third the upper

r ight first mola r at 13.28 months , and four th bo th upper r ight and upper left central incisors at 15.16 months .

The eruptive process of deciduous teeth in

Down ' s boys began at 7.57 m o n t h s with the lower r ight lateral incisor followed by the lower left lateral incisor at 9.31 months . Next came the upper left central incisor at 9.77 m o n t h s and the lower left

central incisor at 11.07 months .

Table 3 shows the complete chronological

sequence of e rupt ion of the deciduous teeth in D o w n ' s children. Table 4 presents the same sequence for the normal Chi lean popula t ion.

Figures 1 and 2 allow bet ter visualization of the sequence and symmetry of the pa t te rn of e rupt ion in normal and D o w n ' s individuals.

In normal Chilean boys the erupt ion pa t te rn on the r ight -and lef t -hand sides was symmetrical

bo th in the mandib le and maxilla. In Down ' s boys the erupt ion of teeth on the two sides was

asymmetr ical in the maxilla, with the only excep-

t ion being the second molar , while in the mand- ible all the teeth presented a symmetrical pa t te rn

(Fig. 1).

Figure 2 shows that no rmal Chilean girls had a symmetrical e rupt ion pa t te rn in the maxilla and

mandible . In D o w n ' s girls the pa t te rn of e rupt ion was asymmetr ical in the maxil la for the central and lateral incisors and for the first molar . In the mand- ible the erupt ion pa t te rn was symmetrical.

Figure 3 presents the significant delays in too th erupt ion in D o w n ' s chi ldren as compared with nor-

mal Chilean individuals. Down ' s girls had a larger n u m b e r of teeth with significant e rupt ion delays

than Down ' s boys. D o w n ' s girls presented sym- metrical delays in the upper and lower lateral inci-

sors and canines with respect to the right- and left- hand sides in the maxilla and the mandible . Down ' s boys had a symmetrical pa t te rn of delay only for lateral incisors in the maxil la and canines in the

mandible .

Table 3, Chronological sequence of eruption of the deciduous teeth in a sample of Chilean children with Down's syn- drome*

Boys - Girls

Tooth X SD Tooth k SD Tooth k SD Tooth ,~ SD

5.3 12.02 32.10 6.1 9.77 30.62 5.4 13.28 20.44 6.1 15.16 9.340 5.1 15.27 5.515 6.4 17.21 3.61l 5.1 15.16 9.340 6.2 17.31 14.42 5.4 17.21 3.611 6.2 18.13 10.01 5.2 17.31 14.42 6.4 25.87 14.34 5.2 18.44 9.652 6.3 22.16 13.85 5.5 29.12 6.067 6.5 29.60 5.649 5.5 27.66 5.645 6.5 27.66 5.645 5.3 30.70 6.454 6.3 30.60 7.249 8.2 7.569 35.24 7.2 9.313 30.61 8.1 7.515 17.75 7.1 12.02 7.286 8.1 14.15 11.82 7.1 11.07 10.76 8.2 27.59 19.01 7.2 24.66 23.86 8.4 17.21 3.611 7.4 17.88 5.166 8.3 27.83 11.25 7.3 28.80 10.60 8.3 25.87 7.667 7.3 26.65 7.431 8.5 28.83 3.454 7.5 32.31 13.43 8.5 27.71 5.562 7.5 27.71 5.562 8.4 57.38 -32.74 7.4 -322.4 262.17

*Age in months

404 A. Ondarza et al.

Table 4. Chronological sequence of eruption of the deciduous teeth in normal Chilean population*,t

Boys Girls

Tooth J( SD Tooth J( SD Tooth J( SD Tooth J( SD

5.1 9.499 2.546 6.1 9.305 2.410 5.1 9.359 3.114 6.1 9.340 2.854 5.2 10.51 2.430 6.2 9.86 3.587 5.2 10.40 3.178 6.2 10.30 3.192 5.4 15.43 1.961 6.4 15.29 2.033 5.4 15.52 2.042 6.4 15.89 2.210 5.3 18.36 3.215 6.3 18.14 3.272 5.3 18.67 3.105 6.3 18.70 3.099 5.5 26.87 3.931 6.5 26.63 3.952 5.5 26.98 3.614 6.5 27.05 3.502 8.1 6.37 1.180 7.1 6.37 1.180 8.1 6.39 1.460 7.1 6.39 1.460 8.2 12.51 3.439 7.2 12.90 3.982 8.2 12.77 3.412 7.2 12.49 3.450 8.4 15.88 2.078 7.4 15.86 2.160 8.4 15.95 2.033 7.4 16.07 2.394 8.3 19.04 3.377 7.3 18.98 3.337 8.3 19.23 3.153 7.3 19.08 3.373 8.5 26.14 3.588 7.5 26.11 3.724 8.5 26.28 3.725 7.5 26.28 3.529

*Age in months. tData from Palomino et al. (1980) Odontologia Chilena 28(123-124), 73 77]

According to the F-test, 39 out of 40 variances were significantly larger in the Down's sample. With the exception of the upper first right molar in girls, no significant departures from the Gaussian distribution were found in the age of eruption in normal and Down's individuals.

DISCUSSION Our results for the timing and sequence of the

pattern of eruption of the deciduous teeth in Down's children differ from those of other investi- gators.

According to Roche and Barkla (1967) the process of eruption in Down's children rarely begins before the age of 9 months and on average the first teeth erupt between 12 and 20 months. Fischer-Brandies (1989) states that the first molar is the first or second tooth to erupt. In our Chilean Down's populat ion the process of eruption in girls begins with the cen- tral incisors at 7.51 months and in boys at 7.57 months with the eruption of the lateral incisors.

The delay in eruption in our Chilean Down's children is statistically different only for certain teeth; results which differ from those of Shroff (1959), Roche and Barkla (1967) and Fischer- Brandies (1989), who reported a delay in all teeth. Nevertheless, in Roche and Barkla's study the teeth most affected were the canines and incisors, a find- ing rather similar to ours.

Shroff (1959) and Roche and Barkla (1967) reported that the eruption of the deciduous teeth ends at 4 or 5 years of age or later. In our study it ends at 27.71 months in boys and at 32.31 months in girls, given that the time of eruption of teeth 7.4 and 8.4 in girls is not reliable because of the large SE.

The aforementioned differences may reflect the multifactorial (genetic, epigenetic, environmental) and probably polygenic control of dental eruption. Eruption involves resorption and formation of bone on opposite sides of the erupting tooth and these activities depend on the dental follicle, a thin con- nective tissue investment of the developing and erupting crown. Proteins and enzymes change in the

Boys Girls N ~ l i 1 ~ ~6... 1 ~ T.n. ,~ T.n. axillar ~ Maxillary

T.n. T.n.

Fig. 1. Order of eruption (in roman numerals) of the Fig. 2. Order of eruption (in roman numerals) of the deciduous dentition by oral quadrant in normal and deciduous dentition by oral quadrant in normal and Down's boys. Tn, tooth number; N, normal individuals; Down's girls. Tn, tooth number; N, normal individuals;

D~ individuals with Down's syndrome. D, individuals with Down's syndrome.

Down's children and deciduous teeth eruption 405

Boys Girls

RIGHT LEFT RIGHT LEFT

Mandible

Fig. 3. Deciduous teeth with a significant delay in time of eruption in Chilean Down's children as compared to nor- mal individuals. *, delay significant at p < 0.05; **, delay

significant at p < 0.01.

in Down's children (Roche and Barkla, 1967). There is suggestive evidence that the rate of erup- tion is influenced by the vascularity of the periradi- cular connective tissue (Roche and Barkla, 1967). The poor peripheral circulation in Down's syn- drome could be a factor leading to delayed erup- tion. The delay may be a part of the delay in growth and development that characterizes this syn- drome; the growth of both the maxilla and mand- ible is retarded. Some have correlated the low weight at birth with the delayed dental eruption (Pindborg, 1970; Billewicz, 1973; Infante and Owen, 1973; Trupkin, 1974; Delgado et al., 1975).

dental follicle during eruption, and several growth factors and proteins known to accelerate or retard eruption have been identified (Marks et al., 1995). The gene products involved are probably coded by genes localized in different chromosomes.

The sequence of tooth eruption did not differ sig- nificantly between normal and Down's boys. In quadrants 2, 3 and 4 the sequence of eruption was similar in Down's and normal individuals, whereas in quadrant 1 a higher number of changes was observed. The differences in the sequence of erup- tion between Down's girls and normal individuals are more pronounced, especially in quadrant 1.

I f the sequence of tooth eruption in boys and girls is jointly analysed, in the mandible there is total symmetry in eruption between antimeric teeth, a situation that is not observed in the maxilla, where the largest alterations in sequence were found.

It seems that the alteration of the sequence is not necessarily a consequence of the alteration in the time of eruption. If the results on sequence and tim- ing of eruption are jointly analysed, then quadrants 1 and 4 show the greatest delay in Down's boys, and quadrants 2, 3 and 4 in Down's girls. These quadrants do not correspond with that which has the greatest alteration in eruption sequence (quad- rant 1) in Down's boys and girls. This implies that some teeth will erupt with some delay but will maintain a sequence of eruption which will be rather similar to that of normal individuals.

Levinson et al. (1955) describe how the eruption o f the molars precedes that of incisors, and Fischer- Brandies (1989) reports that the first molar is the first or second tooth to erupt, These characteristics of the sequence of eruption were not observed here.

The causes of delayed eruption in Down's chil- dren are unknown, Clue to lack of information on the factors intervening in the process of normal eruption. Nevertheless, the delayed eruption in Down's children seems to be dependent on the tri- somic state. Bone resorption occurs during eruption in normal children; this process may be depressed

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