The relationship between children's body mass index and periodontal status.

BACKGROUND: Childhood obesity is a serious medical condition that affects children and adolescents. Being overweight and obese are important risk factors for various adult diseases including diabetes, cardiovascular, and cerebrovascular disease, hypertension, and periodontal diseases. This study aimed to compare the periodontal findings in obese children with those exhibiting normal body mass.
MATERIALS AND METHODS: In the present retrospective cohort study, 108 children, 12 years of age, were randomly assigned to the two groups with equal gender distribution, selected from the schools in Yazd, Iran: obese (body mass index [BMI] ≥25) and nonobese (BMI <25). After obtaining informed consent forms from their parents, each participant's demographic data and BMI were recorded, and periodontal indices were determined including plaque index (PI), bleeding on probing (BOP), pocket depth (PD), and clinical attachment loss (CAL). Then, a questionnaire on dietary and oral hygiene habits was completed by the participants. The data were collected and analyzed with a Chi-square test and t-test.
RESULTS: The results showed statistically significantly higher mean PI, BOP, and PD in obese participants than nonobese participants (P < 0.05), with no statistically significant difference in CAL between the two groups (P > 0.05).
CONCLUSIONS: The periodontal indices of PI, BOP, and PD in obese children were significantly higher than in children with a normal weight. However, there was no statistically significant difference in CAL between the two groups. Copyright:

INTRODUCTION

Obesity has reached epidemic levels in developed as well as in developing countries.[1] Obesity is defined as excess body weight relative to the body mass without fat, which endangers health.[2] Obesity is considered a chronic, complicated, and multifactorial condition, and it is believed that various genetic, metabolic, behavioral, environmental, cultural, and socioeconomic factors contribute to its development.[3]

Obesity is an ever-increasing problem in children due to changes in lifestyle and dietary habits.[4] The prevalence of obesity in Iranian children is increasing, leading to various problems in these children.[5] The persistence of obesity is a significant risk factor for hypertension, cardiovascular diseases, pulmonary conditions, and Type II diabetes. Obesity increases disease incidence throughout life and decreases the quality of life, especially in young adults and groups with lower socioeconomic status.[6]

The most commonly used index to measure body fat is body mass index (BMI), which is defined as the body mass in kilograms divided by the squared body height in meters.[7]

Obesity creates a systemic proinflammatory condition, through which it exerts metabolic and immunologic effects on the body; therefore, it can increase the susceptibility to periodontal disease, considered a chronic infectious disease.[38]

The biological mechanism to establish a relationship between obesity and periodontitis includes hormones and cytokines derived from the adipose tissue, collectively called adipokines. An increase in adipokines derived from visceral fat leads to blood agglutination in the microvasculature, decreasing the gingival blood supply and promoting the progression of periodontitis.[9] Recent studies have shown that adipocytokines can directly affect periodontal tissues.[1011]

Palle et al. carried out a cross-sectional study and reported a significant correlation between visceral and general obesity and periodontal diseases, indicating that obesity might be considered a definitive risk factor for the progression of periodontitis.[12]

Suresh and Mahendra reviewed the relationship between adipose tissue-derived cytokines and periodontal disease and reported that an excessive reservoir of adipose tissue in obese individuals is associated with the release of adipokines, and dentists should inform the patients that obesity is associated with the risk of periodontal diseases.[13]

Tumor necrosis factor-alpha (TNF-α), which mediates tissue injuries due to endotoxins in various organs, including periodontal tissues, is secreted by the adipose tissue and can increase periodontal degradation.[8]

A study by Lundin et al. on young adults showed that TNF-α in the gingival crevicular fluid is related to a BMI of ≥40. A positive correlation between the gingival crevicular fluid TNF-α and BMI in individuals without periodontal disease shows that TNF-α is related to the finding that obesity is a low-grade systemic inflammatory condition.[14]

Considering the high prevalence of obesity and the reports on the relationship between periodontal diseases and other systemic conditions, the present study aimed to evaluate and compare periodontal indices between obese children and children with normal body mass.

MATERIALS AND METHODS

The present study has been approved by the ethics committee of Shahid Sadoughi University of Medical Sciences of Yazd with the number IR.SSU.REC.1398.220. The present parallel-design study evaluated the two groups of obese and nonobese with equal gender distribution 12-year-old children in Yazd, Iran, in 2019–2020. The 108 adolescents in this study were selected based on BMI records in the health files of the participants in school (54 participants with BMI <25 in the nonobese group and 54 with BMI ≥25 as the obese group). All the participants’ parents were signed an informed consent form to be included in the study.

Adolescents with systemic conditions, those taking antibiotics or local or systemic anti-inflammatory medications or having taken these medications in the past month, those with fixed orthodontic appliances, those with unerupted permanent teeth, or teeth with nonrestorable crowns, and girls who had menarche were excluded in this study.

To record BMI, the participants were asked to take off their shoes and heavy clothes. Then, they were weighed with a standard weighing machine. Their height was measured from the calvarium to the heel with a tape measure fixed on the wall, with an 0.05 cm accuracy. Then, each participant's BMI was calculated. The participants were clinically examined to determine the periodontal variables including plaque index (PI), bleeding on probing (BOP), probing depth (PD), and clinical attachment loss (CAL). The teeth selected for the study were maxillary right first molars, maxillary left first molars, maxillary right central incisors, mandibular left first molars, mandibular right first molars, and mandibular left central incisors. If any of these was absent or missing, one of the teeth mesial or distal to the missing tooth was selected.[15] The clinical examinations were carried out with Williams's periodontal probe and a dental mirror, and then indices were recorded.

O’Leary plaque index

This precise index is based on the presence of supragingival plaque on all four tooth surfaces. The test was done by disclosing the plaque, if there is a plaque, the positive mark was recorded on the specific simple chart, and if there is no plaque, the negative mark was recorded, and the percentage of plaque incidence in the oral cavity was calculated.[16]

Bleeding on probing

As in the PI, all four surfaces of included teeth were reexamined for the presence or absence of bleeding 30 s after they were probed, and the positive and negative results were recorded for each participant.[17]

Probing depths

A periodontal probe (William’s) was used to measure the distance between the gingival margin and the base of the periodontal pocket or gingival sulcus. The distance was determined by measuring six areas including the mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual, and distolingual surface. Then, the mean of the measured values for each tooth was used as the representative value.[18]

Clinical attachment loss

The distance between the cementoenamel junction and the pocket depth (PD) was measured in each included teeth with William's periodontal probe.[19]

Then, the operator helped the participants complete a questionnaire on dietary and oral hygienic habits. The questionnaire consisted of questions on the frequency of toothbrushing in 24 h, daily, and regular use of dental floss, the number of meals in 24 h, the use of fluoridated mouth rinses, and gingival bleeding during toothbrushing. Each participant's data were recorded separately after the clinical examinations and completion of the questionnaire. The means of the data were calculated for both groups and analyzed and compared with the Chi-square test and t-test, using SPSS Version 21.0 (IBM, Chicago, United States of America) at a significance level of P < 0.05.

RESULTS

In the present study, 108 children, 12 years of age, were evaluated in two groups of 54 participants with BMI <25 in the nonobese group and 54 with BMI ≥25 in the obese group. Each group had 27 boys and 27 girls with the same gender distribution.

Table 1 presents the mean BMI of obese (27.55) and nonobese (18.40) groups (P < 0.05).

Table 1

Mean body mass index in the two groups

BMI*	n*	Mean	SD*
Nonobese	54	18.40	2.09
Obese	54	27.55	2.20

T-test, P=0.001, P<0.05 – Statistically significant. BMI – Body mass index; n – numbers; SD – Standard deviation; P – Probability value; T – Test value

The results of clinical examinations based on the t-test on the periodontal findings showed statistically significant differences between the normal and obese groups in all the indices evaluated except for the CAL (P < 0.05) [Table 2]. No CAL was observed in the nonobese group, and in the obese group, only two participants exhibited 1 and 2 mm of CAL, which was not statistically significant (P > 0.05).

Table 2

Mean periodontal variables in the two groups

Periodontal variables	Study groups	Mean
Plaque index (%)	Nonobese	84
	Obese	96
Pocket depth (mm)	Nonobese	1.50
	Obese	2.25
Bleeding on probing (%)	Nonobese	24.1
	Obese	87

Chi-squared test, P=0.00, P<0.05 – Statistically significant. P – Probability value

Other analyses evaluated whether, after neutralizing the effect of dental plaque as an established factor for periodontal destruction, BMI will affect the periodontal indices or not. After eliminating the effect of PI by binary logistic regression, the effect of BMI on BOP became statistically significant (R2: 0.475, P < 0.05). In addition, after eliminating the effect of PI using linear regression, the effect of BMI on PD became statistically significant too (R2: 0.655, P < 0.05).

The data collected from the questionnaire on oral hygienic and dietary habits were analyzed [Table 3]. The results showed a statistically significant difference in the observance of oral hygiene between the normal and obese children groups, with the obese participants paying less attention to their oral hygiene.

Table 3

Data frequency of oral hygiene and dietary habits

Variables frequency	Study group (%)		P
	Nonobese	Obese
Tooth brushing
No times a day	31.5	74.1	<0.05
Once a day	46.3	20.4
Twice a day	13	5.6
Thrice a day and more	9.3	0
Food meals
Once or twice a day	27.8	3.7	<0.05
Thrice a day	53.7	24.1
More than thrice a day	18.5	72.2
Flossing
Yes	25.9	5.6	<0.05
No	74.1	94.4
Fluoride mouthwash
Yes	53.7	37	>0.05
No	46.3	63
Gingival bleeding during tooth brushing
Yes	14.8	74.1	<0.05
No	85.2	25.9

Chi-squared test, P=0.00, P<0.05: Statistically significant. P – Probability value

The results of the questions on the frequency of toothbrushing in 24 h showed that the obese participants brushed their teeth less frequently. Besides, there was a statistically significant difference in gingival bleeding during toothbrushing between the two groups (P < 0.05).

However, there was not a statistically significant difference between the two groups in the use of fluoride mouthwash (P > 0.05).

Concerning the use of dental floss, there was a statistically significant difference between the two groups, with statistically significantly less frequent dental floss use by the obese participants (P < 0.05).

The data on the food snacks and their frequency of use showed a statistically significant difference between the two groups, with a higher frequency of meals and snacks in the obese participants (P < 0.05).

DISCUSSION

Obesity is considered to be an epidemic given that its prevalence and severity in both adults, and children is rising at alarming rates.[20] However, limited studies are available on obesity in Iran, and most studies in Iran have been limited to one region.[21] On the other hand, obese children who remain obese in adolescence might become very obese in adulthood; 80% of obese adolescents remain obese in adulthood.[22]

Diet and oral health have a reciprocal effect on each other. On the one hand, the daily diet affects oral health, and on the other hand, oral health can significantly affect the diet and general health.[23] Recent studies have shown that obesity participates in a general systematic inflammatory process, affecting metabolic parameters, and increasing susceptibility to periodontal diseases.[89] Other studies have shown that age and gender (boys) are covariates that have a positive impact on the risk of periodontal disease in obese/overweight children.[424] Therefore, the present study was undertaken to evaluate the periodontal parameters in obese and nonobese children in Yazd, Iran, in 2019–2020.

In the present study, obese and nonobese children were comparatively evaluated in terms of PD, BOP, PI, and CAL parameters for assessing their periodontal status. The nonobese children were normal in terms of BMI and were matched with obese children in terms of gender.

The results showed statistically significantly higher mean PI in nonobese children than obese children, consistent with a study by Scorzetti et al. and Sfasciotti et al.[2526] This higher PI in obese participants might be attributed to the higher frequency of meals, consumption of carbohydrate-rich foodstuff, and poor oral hygiene. However, this difference in a study by Zuza et al. with a smaller sample size was not statistically significant.[27]

Furthermore, obese participants had a statistically significantly higher relative frequency of BOP than the nonobese participants, consistent with studies by Zuza et al. and Scorzetti et al. and Sfascioti,[252627] which might be attributed to an increase in the pro-inflammatory cytokine levels in the gingival crevicular fluid of obese participants.[28] An increase in the levels of pro-inflammatory cytokines, such as interleukin (IL)-1, IL-6, TNF-α, and adipokines such as leptin in individuals with a high BMI, might increase gingival inflammation and periodontal destruction, leading to periodontal disease.[14]

In the present study, obese participants had higher mean PD than the nonobese participants, which was statistically significant, but from the point of clinical view, it was not significant because the higher rates in obese participants were not considered a periodontal disease. In the study by Scorzetti et al., the deepest pockets were recorded in both groups in each participant. The obese group participants had statistically significantly more numerous pockets with probing depth ≥ 4 mm than the nonobese participants (P < 0.05).[25]

In addition, in the study by Zuza et al., the periodontal status was evaluated in terms of the CPI, which was more prevalent with a code of zero in participants with the normal BMI.[27] However, in the study by Sfasciotti et al., none of the participants in any of the study groups exhibited PD values of >3 mm (P > 0.05).[26]

A study by Vallogini et al. on 204 participants with an age range of 10–16 years yielded results contrary to those of the studies above. The obese group exhibited lower visible PI and gingival bleeding index than the nonobese group. Besides, they had a better periodontal status in terms of PDs. The participants were selected from the obese patients in a pediatric hospital, and the nonobese participants were selected from a school. Therefore, the discrepancy in the results of studies might be attributed to the difference in sampling procedures because the participants selected from the hospital might have received dietary and hygiene counseling, resulting in an improvement in periodontal parameters.[29]

In the present study, similar to the Scorzetti et al. study, there was not a statistically significant difference between the two groups in loss of clinical attachment; however, this was worse in obese children.[25]

Data collected from the questionnaire on dietary and oral hygiene habits showed that the obese participants paid less attention to oral hygiene. In general, obese children exhibited a lower periodontal status than children with normal weight.

Most studies on the relationship between obesity and periodontitis are considered immunologic and metabolic changes as predisposing factors for periodontitis; however, some studies have reported that the composition of saliva in obese individuals is different from that in individuals with a normal weight and have considered oral bacteria as a factor for the prevalence of obesity. In this context, periodontal disease has been associated with a change in oral bacteria composition in obese individuals,[30] consistent with a study by DiBaise et al.[31]

In general, obesity is a complicated and multifactorial condition associated with many chronic conditions and periodontal disease; however, its principal mechanism is still under investigation.

Dahiya et al. suggest that dentists should encourage obese children and adolescents to lose weight by changing their diet and behavioral interventions to control inflammatory periodontal diseases during routine examinations of patients.[20]

From the limitations of the study, for a more accurate evaluation, it was advisable that both groups had already received health education and had the same average PI to evaluate the relationship between BMI and periodontal indices without confounding factors. Another limitation of the present study was the inability to match the participants from a socioeconomic perspective as a factor affecting the periodontal status.

Finally, it is suggested that prospective cohort studies be designed to evaluate the relationship between obesity and periodontal disease more accurately to determine confounding factors, including measuring the waist circumference for evaluating the periodontal parameters in patients with abdominal obesity.

CONCLUSIONS

The present study showed that obese children had lower periodontal status compared to children with normal BMI. It is recommended that parents pay more attention to the prevention of gingival diseases in addition to supervising unhealthy dietary and nutritional behaviors. Oral hygiene education should be provided including correct toothbrushing and the use of dental floss to promote knowledge and awareness about children's oral health.

Financial support and sponsorship

We would like to thank Faculty of Dentistry, Shahid Sadoughi University of Medical Science, Yazd, Iran.

Conflicts of interest

There are no conflicts of interest.