Timing of Permanent Tooth Emergence is Associated with Overweight/Obesity in Children from the Amazon Region

Abstract

The aim of this study was to evaluate the association between timing of permanent tooth emergence with overweight and obesity in children from Brazilian Amazon region. The studied population consisted of 192 children, 09 to 12 year-old, from public schools at Manaus, Amazonas-Brazil. Clinical examination was performed and the tooth emergence was evaluated according to the number of permanent erupted teeth. Body mass index z-score was calculated. For the statistical analysis ‘Overweight/obese’ group was compared with ‘Normal weight’ group in a case to control ratio 1:2. The t-test based on age was used for means comparison between the groups. A linear regression analysis using age and gender as co-variants was used. The established alpha was 5%. One hundred twenty-seven children were classified as normal weight and 65 were classified as overweight/obese (49 were overweight and 16 were obese). Overweight/obesity condition was associated with the gender, in which boys had a higher chance to present higher weight conditions (OR=1.84; CI 95% 1.06-3.37; p=0.04). The mean number of permanent teeth was higher in the overweight/obesity group (p<0.001). Linear regression analysis demonstrated that nutritional status, gender and age were strongly associated with number of permanent erupted teeth (p<0.05). In conclusion, our study demonstrated that timing of permanent tooth emergence is associated with overweigh/obesity in children from Manaus, Brazil.

Key Words:
tooth emergence; nutritional status; children

Resumo

O objetivo deste estudo foi avaliar se a erupção dentária está associada com sobrepeso/obesidade em crianças da região Amazônica brasileira. A população estudada foi composta por 192 crianças, de 9 a 12 anos, de escolas públicas de Manaus, Amazonas-Brasil. O exame clínico foi realizado e a erupção dentária foi avaliada de acordo com o número de dentes permanentes irrompidos. O índice de massa corporal escore-z foi calculado. Para a análise estatística, comparou-se o grupo "sobrepeso / obesidade" com o grupo "peso normal" em uma proporção de controle 1: 2. O teste t baseado na idade foi utilizado para comparação das médias entre os grupos. Uma análise de regressão linear usando idade e sexo como co-variáveis foi utilizada. O alfa estabelecido foi de 5%. Cento e vinte e sete crianças foram classificadas com peso normal e 65 foram classificados com sobrepeso / obesidade (49 com sobrepeso e 16 com obesidade). A condição de sobrepeso / obesidade associou-se ao gênero, no qual os meninos tiveram maior chance de apresentar condições de maior peso (OR = 1,84; IC 95% 1,06-3,37; p = 0,04). O número médio de dentes permanentes irrompidos foi maior no grupo sobrepeso / obesidade (p <0,001). A análise de regressão linear demonstrou que o estado nutricional, sexo e idade foram fortemente associados ao número de dentes permanentes irrompidos (p <0,05). Concluindo, nosso estudo demonstrou que o momento da erupção dos dentes permanentes é associado com sobrepeso / obesidade em crianças de Manaus, Brasil.

INTRODUCTION

Childhood overweight/obesity is one of the most serious public health challenges of the 21st century and has been increasing during the past years. According to the World Health Organization (WHO) over 42 million children are considered overweight or obese. It is well known that obesity is associated to adversely health issues, including earlier puberty ¹. Overweight children are taller than non-overweight children at the same age ².

Tooth emergence is the result of an intricate process, characterized by the movement of the tooth, during odontogenesis, through the alveolar bone and gingival mucosa until the tooth emergence in the proper position in the dental arches1. The mechanisms involved in the timing of tooth emergence are not completely understood and are influenced by many regulatory aspects ^1,2.

Several studies have already shown that the timing of tooth emergence can be influenced by the nutritional status, such as malnourished, overweight and obesity ^{3,4,5,6,7,8,9,10,1)}. Although previous studies in different populations demonstrated that obese and overweight children have more permanent erupted teeth when compared with their controls ^{3,5,6,7 9,10,11}, none of these studies were performed in a population of children from the Amazon forest region, which has a completely different genetic, environmental and cultural background. Thus, the aim of this study was to evaluate if overweight and obesity is associated with timing of permanent tooth emergence in children from the Brazilian amazon region.

MATERIAL AND METHODS

Participants

The study was approved by The Human Ethics Committee of Amazon State University (Nº 923.569). Informed written consent was obtained from the parents and age appropriate assent document were used for all children.

Children from four public schools from Manaus city were evaluated. Manaus is the capital city of the state of Amazonas state that is locate in the Northern Region of Brazil. Manaus is situated in the middle of the Amazon rainforest and the total population comprises 2,094,391 inhabitants. The ancestry of the inhabitants of Manaus is composed mainly by European and Native American, and the remaining of African descendant ¹².

The parents or legal guardians answered a questionnaire about information regarding their child’s medical history and actual health condition on order to evaluate if the weight deviation were associated with any comorbity. Non-syndromic children aged from 9 to 12 years old were included. Underweight/malnourished children were not included.

Determination of Timing of Tooth Emergence

Two specialists in pediatric dentistry (KRFV and SSE) performed the oral examination. The examination was performed in the schoolyard with sunlight as a direct light source. After brushing their teeth, the students were placed in a supine position. Tooth emergence was evaluated according to the number of permanent teeth erupted, which was defined as having occurred if any tooth surface had emerged the alveolar mucosa8.

Determination of the Nutritional Status

Heights were determined in meters and weights in kilograms with a weighing machine. The children were wearing light clothes and no shoes.

The nutritional status were calculated using the Body Mass Index (BMI) z-score calculator (http://zscore.research.chop.edu/index.php) and individual height, weight, age and gender as variables.

The classification was performed according to the World Health Organization12, as follow:

Overweight/obese group: BMI z-score >85th percentile;

Normal weight children: BMI z-score ≥ 3 and ≤85th percentile.

Statistical AnalysIs

For the statistical analysis ‘Overweight/obese’ group was compared with ‘Normal weight’ group were compared with normal weight children in a case to control ratio 1:2.

Data were analyzed using Epi Info 7. The Shapiro-Wilk test was used to verify the normality of the data. The t-test based on age was used for means comparison between the groups. A linear regression analysis using age and gender as co-variants was used. The established alpha was 5% for all comparisons.

The power was calculated using clinical.com (http://clincalc.com/stats/Power.aspx) to calculate the power for comparison of means from independent samples.

RESULTS

Normal weight group had 127 children and overweight/obese group had 65 children (49 were overweight, and 16 were obese). The characteristics distribution according to the groups is presented in Table 1. Overweight/obesity were associated with the gender, in which boys had a greater chance to present higher weight conditions (OR=1.84; CI 95% 1.06-3.37; p=0.04).

Table 1
Sample characteristics distribution between the groups.

Characteristics		Groups		p-value
		Normal weight	Overweight/obesity
Sex	Male	N=55 (43.31%)	N=38 (40.9%)	0.04*
	Female	N=72 (56.69%)	N=27 (27.3%)
Mean age (SD)		10.40 (+8.18)	10.22 (+0.94)	0.21

• SD: standard deviation; *statistically significant difference (p<0.05).

In the normal weight group, 1 child had a medical history of severe premature birth, one child had iron deficiency anemia, one child had high triglycerides, 7 children had allergies condition, 4 children had asthma, and one has attention deficit hyperactivity disorder-ADHD. In the overweight/obesity, 1child had high triglycerides, 2 children had allergies conditions and 2 children had asthma. There was no association between the medical history and overweight/obese (p>0.05).

The mean number of permanent teeth was higher in the overweight/obesity group. An association was observed when the analysis was performed in both genders, in males only and in females only (p<0.001). The mean distribution according to the nutritional status and stratified according to the gender is presented in the Table 2.

Table 2
Range and mean number of permanent erupted teeth according to the groups and stratified according to the sex.

Groups/Nutritional status	Number of erupted teeth		p-value
	Minimum-maximum	Mean (SD)
Both sexes
Normal Weight	10-28	20.36 (5.25)	<0.001*
Overweight/obesity	12-28	22.63 (4.89)
Males
Normal Weight	10-28	18.86 (4.78)	<0.001*
Overweight/obesity	12-28	21.48 (4.98)
Females
Normal Weight	10-28	21.47 (5.31)	<0.001*
Overweight/obesity	14-28	24.21 (4.30)

• SD: standard deviation; * statistically significant difference (p<0.05)

Table 3 shows the linear regression analysis results of the factors involved in the number of permanent erupted teeth. Nutritional status, gender and age were strongly associated with number of permanent erupted teeth (p<0.05).

Table 3
Factors influencing the number of permanent erupted teeth.

R2	0.43
Independent variables	SE	p-value
Nutritional status	0.62	0.001*
Sex	0.59	0.025*
Age	0.32	<0.001*

• SE means standard error. *statistically significant difference (p<0.05)

The power calculation using the actual sample sizes for normal weight and overweight/obese groups show that the power is 84.3% to detect the difference between groups.

DISCUSSION

The childhood overweight and obesity is a serious public health problem. This problem is global and is progressively affecting many low- and middle-income countries, mainly in urban areas ¹². This study was performed in the capital of the Amazonas state- Brazil. Manaus is an urban area and is the largest city in northern of Brazil and represents the sixth largest economy of the country ¹³.

The health burden from overweight and obesity is the driving factor behind several research studies regarding the impact of nutritional status conditions on oral health. It is known that nutritional status plays a role in children’s oral health and development ¹⁴, but some aspects and the nature of this relationship remain unclear.

The BMI z-score analysis is a useful tool to evaluate children’s health and can be used to analyze the association between nutritional status with many aspects, such as dental, skeletal and motor development ^15,16. In our study, we also used this method to classify children’s nutritional status and evaluate if an association between higher BMI and tooth development exists.

Our study evaluated a singular population of children from the Brazilian Amazon Region, and we were able to note that our results were in agreement with previous studies performed in different populations, in which higher weight, mainly obesity, are associated with alterations in timing of tooth eruption ^3,5,6,7,9,10. We observed that overweight/obese children had a statistical significant higher mean number of permanent teeth. This finding could be explained by the fact that overweight and obese children have hormonal metabolism alterations ⁵ and earlier puberty. So, it is possible that these are the mechanisms related to the alteration in the timing of tooth eruption.

It is well established that the gender is involved in the timing of tooth eruption ^{17,18,19,20,21,22}. The analysis performed here also observed that girls had more erupted permanent teeth than boys. It is well established that girls mature earlier than boys, including the dental development ^23,24. For this reason, our analysis stratified the sample according to the gender, in which, overweight/obese children in both genders had more erupted permanent teeth.

Comorbidities of pediatric obesity may be grouped under physical and psychosocial categories. Childhood obesity can adversely affect nearly every organ system and often has serious consequences, including hypertension, dyslipidemia, insulin resistance, prediabetes, type 2 diabetes mellitus, fatty liver disease and psychosocial complications ²⁵. In the present study, we were not able to observe an association between overweight/obesity and health conditions. These could be explained by the fact that the medical history information was collected through a questionnaire, in which the parents/legal guardians failed to report some conditions. Other explanation could be the fact that obese children represent only 16 cases. Weight that is higher than what is considered as a healthy weight for a given height is described as overweight or obese, however, it is possible that only the severer phenotype (obesity) is associated with comorbidities in childhood.

The sample recruitment ended in 65 overweight/obese and almost a twice of normal weight children. Although a sample size calculation was not performed during the study design, we provided a post-hoc power calculation, which demonstrated that this sample was sufficient to maintain the power of the cross-sectional study.

Some previous studies have shown that the time of tooth emergence varies according to the origin of the population ^{17,18,19,21,22,26,27}. To the best of our knowledge, this is the first study to evaluate the impact of the overweight and obesity in the timing of tooth eruption in a population from the Amazon region, which presents a particular genetic background, with a mixture of Europeans descendants and Native South Americans, and indeed our study suggests that nutritional status are associated with dental development and time of tooth eruption in Amazon children.

Timing of permanent tooth emergence is associated with overweight and obesity in children from Manaus, Brazil.

Acknowledgements

This work was supported by the São Paulo Research Foundation (FAPESP) (funding number: 2015/06866-5) and individual scholarships (FAPESP and CAPES).

References

• ¹
  Shiyan H, Nanquan R, Shuhao X, Xiaobing L. Research progress on the cellular and molecular mechanisms of tooth eruption. Hua Xi Kou Qiang Yi Xue Za Zhi 2016;34:317-321.
• ²
  Kjær I. Mechanism of human tooth eruption: review article including a new theory for future studies on the eruption process. Scientifica 2014;2014:341905.
• ³
  Hilgers KK, Akridge M, Scheetz JP, Kinane DE. Childhood obesity and dental development. Pediatr Dent 2006;28:18-22.
• ⁴
  Psoter W, Gebrian B, Prophete S, Reid B, Katz R. Effect of early childhood malnutrition on tooth eruption in Haitian adolescents. Community Dent Oral Epidemiol 2008;36:179-189.
• ⁵
  Sánchez-Pérez L, Irigoyen ME, Zepeda M. Dental caries, tooth eruption timing and obesity: a longitudinal study in a group of Mexican schoolchildren. Acta Odontol Scand 2010;68:57-64.
• ⁶
  Costacurta M, Sicuro L, Di Renzo L, Condò R, De Lorenzo A, Docimo R. Childhood obesity and skeletal-dental maturity. Eur J Paediatr Dent 2012;13:128-132.
• ⁷
  Must A, Phillips SM, Tybor DJ, Lividini K, Hayes C. The association between childhood obesity and tooth eruption. Obesity (Silver Spring) 2012;20:2070-2074.
• ⁸
  Heinrich-Weltzien R, Zorn C, Monse B, Kromeyer-Hauschild K. Relationship between malnutrition and the number of permanent teeth in Filipino 10- to 13-year-olds. Biomed Res Int 2013;2013:205950.
• ⁹
  Mack KB, Phillips C, Jain N, Koroluk LD. Relationship between body mass index percentile and skeletal maturation and dental development in orthodontic patients. Am J Orthod Dentofacial Orthop 2013;143:228-234.
• ¹⁰
  Hedayati Z, Khalafinejad F. Relationship between body mass index, skeletal maturation and dental development in 6- to 15- year old orthodontic patients in a sample of iranian population. J Dent 2014;15:180-186.
• ¹¹
  Arid, J, Vitiello MC, Silva RAB, Silva LAB, Queiroz AM, Kuchler EC, et al. Nutricional status is associated with permanent tooth eruption chronology. Brazilian Journal of Oral Sciences 2017;16:1-4.
• ¹²
  WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index- for-age: Methods and development. Geneva: World Health Organization, 2006.
• ¹³
  Instituto Brasileiro de Geografia e Estatística (IBGE). Censo Brasileiro de 2010. Rio de Janeiro: IBGE, 2010.
• ¹⁴
  Fonseca MA. Malnutrition and Oral Health in Children. Current Oral Health Reports. 2017;4:92-96.
• ¹⁵
  DuPlessis EA, Araujo EA, Behrents RG, Kim KB. Relationship between body mass and dental and skeletal development in children and adolescents. Am J Orthod Dentofacial Orthop 2016;150:268-273.
• ¹⁶
  Amouian S, Abbasi Shaye Z, Mohammadian S, Bakhtiari M, Parsianmehr B. Assessment of the Relationship between Body Mass Index and Gross Motor Development in Children. Iran J Child Neurol 2017;11:7-14.
• ¹⁷
  Diamanti J, Townsend GC. New standards for permanent tooth emergence in Australian children. Aust Dent J 2003;48:39-42.
• ¹⁸
  Leroy R, Bogaerts K, Lesaffre E, Declerck D. The emergence of permanent teeth in Flemish children. Community Dent Oral Epidemiol 2003;31:30-39.
• ¹⁹
  Moslemi M. An epidemiological survey of the time and sequence of eruption of permanent teeth in 4-15-year-olds in Tehran, Iran. Int J Paediatr Dent 2004;14:432-438.
• ²⁰
  Khan N. Eruption time of permanent teeth in pakistani children. Iran J Public Health 2011;40:63-73.
• ²¹
  Lakshmappa A, Guledgud MV, Patil K. Eruption times and patterns of permanent teeth in school children of India. Indian J Dent Res. 2011;22:755-763.
• ²²
  Oziegbe EO, Esan TA, Oyedele TA. Brief communication: Emergence chronology of permanent teeth in Nigerian children. Am J Phys Anthropol 2014;153:506-511.
• ²³
  Eskeli R, Lösönen M, Ikävalko T, Myllykangas R, Lakka T, Laine-Alava MT. Secular trends affect timing of emergence of permanent teeth. Angle Orthod 2016;86:53-58.
• ²⁴
  Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW, Dinov ID, Worthman CM, et al Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex 2011;21:636-646.
• ²⁵
  Güngör NK. Overweight and Obesity in Children and Adolescents. J Clin Res Pediatr Endocrinol 2014;6:129-143.
• ²⁶
  Marceau K, Ram N, Houts RM, Grimm KJ, Susman EJ. Individual differences in boys’ and girls’ timing and tempo of puberty: modeling development with nonlinear growth models. Dev Psychol 2011;47:1389-1409.
• ²⁷
  Almonaitiene R, Balciuniene I, Tutkuviene J. Standards for permanent teeth emergence time and sequence in Lithuanian children, residents of Vilnius city. 2012;14:93-100.

Publication Dates

• Publication in this collection
  Sep-Oct 2018

History

• Received
  22 Jan 2018
• Accepted
  11 May 2018