Impact of Oral Health Behaviors on Dental Caries in Children with Intellectual Disabilities in Guangzhou, China

Dental care is consistently reported as one of the primary medical needs of children with disabilities (IDC). The aim of the present study was to explore the influence of oral health behaviors on the caries experience in children with intellectual disabilities in Guangzhou, China. A cross-sectional study was carried out in 477 intellectually disabled children, 12 to 17 years old, who were randomly selected from special educational schools in Guangzhou. A self-administered parental questionnaire was used to collect data on socio-demographic characteristics and oral health behavior variables, and 450 valid questionnaires were returned. Multiple regression analysis was used to examine the factors associated with dental caries. The average age of those in the sample was 14.6 years (SD = 1.3), 68.4% of whom were male, and the caries prevalence rate was 53.5% (DMFT = 1.5 ± 2.0). The factors significantly affecting the development of dental caries in IDC included gender, the presence or absence of cerebral palsy, and the frequency of dental visits and toothbrushing. In conclusion, the presence of cerebral palsy contributed to an increase risk of caries experience in intellectually disabled children, while toothbrushing more than twice a day and routine dental visits were caries-protective factors. Oral health promotion action may lead to a reduction in dental caries levels in IDC.


Introduction
Children with disabilities are at high risk for health problems [1]. In particular, children with intellectual disabilities (IDC) usually need support to carry out daily self-care. The level of self-care may be said to be directly related to the degree of learning disability and children with more profound impairments may need greater levels of support [2,3]. So, IDC usually require extra help and rely on their parents or guardians to achieve and maintain good health. Oral health is no exception. Dental care is consistently reported as one of the primary medical needs of children with disabilities [4]. Difficulties in communicating oral health needs and concomitant diseases (cerebral palsy, Down syndrome, etc.) can be barriers to adequate oral care and put the IDC at greater risk for developing oral health problems [5]. Several studies have reported a greater prevalence of caries in children with disabilities compared with that in the general population [6][7][8]; therefore, these children should obtain special preventive care in the dental office [9]. According to the latest report, there are 2.46 million children with an intellectual or physical disability in China, 30.9% of whom are IDC, which ranks first [10]. However, little attention has been paid to the oral health status of IDC, and still less information on their prevalence of dental caries and DMFT (Decayed, Missing due to caries, and Filled Teeth) scores is available in Mainland China. Thus, studies on the dental health of IDC are urgently needed.
Factors related to the dental health of IDC have been discussed in previous literature. Socio-demographic characteristics (age, gender, and disability), socio-economic indicators [11], and oral health behaviors may be related to the development of dental caries. A study by Moreira et al. indicated that children with both cerebral palsy (CP) and intellectual disabilities presented more dental cavities than controls, and that intellectual disability affected the development of dental caries [12]. Bakry and Alaki reported that age, gender, and parents' education did not have a profound impact on caries experience in either children with intellectual disability or healthy children, while in IDC, the nature of diet and the severity of intellectual disability were significant risk factors associated with dental caries experience [13]. In Mainland China, however, the influence of risk/protective factors on the oral health of IDC has not yet been investigated. Because of significant differences in living habits and geographic location, whether the same factors in other regions would have the same effect on Chinese IDC is questionable. Therefore, we conducted this cross-sectional survey on the prevalence of caries and DMFT scores in IDC in Guangzhou city, aiming to explore the relationship between oral health behaviors and dental caries in IDC.

Study Design, Population and Sample
This study conservatively estimated caries prevalence in IDC to be 50.0%. Standard error was set at 5.0%, and the response rate was assumed to be 90.0%. At least 427 children were needed for study validity.
Our study was reviewed and approved by the Ethical Review Committee of the Institute of Stomatological Research, Sun Yat-Sen University, before the study began. The approval number is ERC-2012-028.
The present cross-sectional study was conducted among individuals from special educational schools in Guangzhou in March and April of 2013. Stratified by the numbers of schools and of the IDC enrolled, a representative sample of 6 special educational schools with 551 children was randomly selected. Schoolchildren were selected if they met the inclusion and didn't have any exclusion criteria. They were included if they were aged between 12 and 17 years old and had a clinical diagnosis of intellectual disability based on the criteria and classification established by Standardization Administration of the People's Republic of China [14], as registered in their medical records. We excluded children from the study for the reason that their parents refused to allow them to undergo the dental examination. The parents of each child were contacted and informed in writing about the study design and dental examination proposed for their children. If they agreed to have their children participate in the survey, a document of informed consent was voluntarily signed by the parents. In total, 477 IDC were recruited in the final sample.

Data Collection and Study Variables
The children's DMFT scores were based on clinical examinations performed by two well-trained and calibrated dental practitioners (kappa = 0.87) [15]. The DMFT score has been well established as the key measure of caries experience in dental epidemiology, reflecting the degree of caries experience, and is calculated by adding results for Decayed, Missing due to caries, and Filled Teeth in the permanent dentition. Visual examination by means of an artificial white light source and plane mouth mirror was combined with probing diagnosis in caries examination, with codes and criteria as established by the WHO [16]. The information on grade of intellectual disability and the presence or absence of cerebral palsy was supplied by the special education school. Every child with a disability had been examined and assessed by the designated and qualified hospital. The results of the assessment were registered in the school's medical records.
A self-administered parental questionnaire (11 items) was used to collect data on socio-demographic characteristics and oral health behavior variables. Socio-demographic variables included the gender of the children, parental education level, registered residence, and school district. The parental education level was categorized into "lower education" (1-12 years), "'medium education" (13-15 years), and "higher education" (16 or more years) [17]. Grade of intellectual disability and the presence/absence of cerebral palsy were based on the criteria established by Standardization Administration of the People's Republic of China and WHO respectively [14,18]. Oral health behavior variables, as used in previous research, included gargling habits after meals, dental visits in the preceding 12 months, frequency of toothbrushing, eating snacks, and eating sweet foods before sleeping [17,[19][20][21]. In total, 477 questionnaires were delivered, and 450 valid questionnaires were returned, for a return rate of 94.3%.

Statistical Analysis
Statistical analysis was conducted with SPSS 13.0 for Windows, with the level of significance set at 5.0% (p-value < 0.05). Frequencies, means, standard deviations (SD), and percentages were computed for descriptive purposes. We used the Kolmogorov-Smirnov (KS) test to determine the distribution of DMFT scores. Since non-normal distribution was found, non-parametric tests (Wilcoxon rank sum test and Kruskal-Wallis H test) were used. Pearson's chi-square test was used to analyze the differences in the distribution of socio-demographic and oral health behavior variables (independent variables) between the case group (DMFT > 0) and the control group (DMFT = 0), and crude odds ratios (OR's) and 95% confidence intervals (95% CI) were estimated. Unordered categorical variable (school districts) is defined as dummy viable with the method of reference cell coding. For the lowest prevalence rate of caries experience in our survey, Liwan was chosen as the reference cell, which is compared with all other districts. Variables that were significantly associated with DMFT scores were selected in the final model. Multivariate logistic regression analysis (Forward LR procedure) was conducted to investigate which independent variables were significant for explaining the dental condition.

Description of the Study Sample
The average age of the children was 14.6 years (SD = 1.3), and 68.4% were male. The sample consisted of 450 children (241 DMFT > 0, 209 DMFT = 0), and the caries prevalence rate was 53.5% (DMFT = 1.5 ± 2.0). Table 1 displays the distribution of socio-demographic characteristics, oral health behavior variables, and DMFT scores (mean ± SD). A statistically significant difference in DMFT scores was detected between subgroups stratified by gender, the presence/absence of cerebral palsy, dental visit in the preceding 12 months, and frequency of toothbrushing, respectively (p < 0.05).  Table 2 shows the socio-demographic results of single-factor analysis. No differences were observed in the variables of parents' education, domestic economic status, registered residence, grade of intellectual disability, and school district between children with DMFT > 0 and those with DMFT = 0 (p > 0.05). Crude OR's show that being female (OR = 1.8, p < 0.05, 95% CI = 1.2-2.7) and having cerebral palsy (OR = 1.6, p < 0.05, 95% CI = 1.1-2.4) were associated with an increased likelihood of caries experience. Table 3 shows the oral health behavior results of single-factor analysis. No differences were observed in the variables of gargling after dinner, eating snacks, and eating sweet foods before sleeping. Crude OR's show that children who had visited a dentist in the preceding 12 months (OR = 0.4, p < 0.05, 95% CI = 0.3-0.6) and had a higher frequency of toothbrushing (OR = 0.5, p < 0.05, 95% CI = 0.4-0.8) had a decreased likelihood of caries. Table 2. Single-factor analysis of the relationship between sociodemographic characteristics and caries experience in children with intellectual disabilities.

Results of the Multivariate Analysis
Results of the multivariate logistic regression analysis are shown in Table 4, which presented an adequate fit (goodness of fit, Hosmer and Lemeshow: χ 2 (7) = 6.28, p = 0.508). The prevalence of caries was significantly related to some socio-demographic characteristics and oral health behaviors. The odds for girls having caries (DMFT > 0) were 1.9 times more than for boys. The odds for children with cerebral palsy having caries were 1.6 times more than for those without cerebral palsy. Having dental visits in the preceding 12 months (adjusted OR = 0.4, p < 0.05, 95% CI = 0.2-0.6) and toothbrushing at least twice a day (adjusted OR = 0.5, p < 0.05, 95% CI = 0.3-0.8) were caries-protective factors.

Discussion
Nationwide oral epidemiology investigations were conducted in 1983, 1995, and 2005, but they included little, if any, information about the oral health status of IDC in China. The present study demonstrated that caries prevalence rates and DMFT in IDC are 53.5% and 1.5, respectively, in Guangzhou, which are well above the national index for 12-year-old children without disabilities (28.9% and 0.5) [22] and higher than those of teenagers with CP in Hong Kong (43% and 1.2) [23] . Our conclusion supported previous results [5,12,13,24] showing that the status of dental health in patients with disabilities was poorer compared with that of the general population, but is in contrast to the study done by Sagheri [25], which demonstrated that the prevalence of dental caries among preschool children with disabilities in Ireland is lower than that of the comparable general population. Well-established oral health preventive practices in Ireland may be related to the reduction in the prevalence of dental caries in children with disabilities. In addition, the prevalence of caries and DMFT varied among different types of disabilities. For example, Reddy and Sharma [26] reported the prevalence of caries and DMFT/dmft to be 40.0% and 1.1/0.2, respectively, in visually impaired children, and 11.5% and 0.9/0.5 in children without visual impairment. Jaber [8] reported that children with autism exhibited a higher caries prevalence (77.0%) and DMFT (1.6) than did children in a non-autistic healthy control group (caries prevalence = 46%, DMFT = 0.6).
This study also demonstrated that the odds ratios for IDC with CP were significantly higher than for those without CP, supporting the results of previous studies [12]. The increased risk of caries experience in IDC with CP might be related to complications (visual impairments, hearing impairment, seizures, and motor impairment, etc.), that could lower their physical abilities and be barriers to adequate oral care [5]. Researchers also reported that CP would lead to abnormal movements of the tongue and facial muscles [27] as well as low salivary flow, pH, and buffering capacity [28], which might increase the risk for dental caries. In addition, medication may contribute to complications. For example, there can be various neurologic and metabolic syndromes in children with CP, some involving seizures [29] and the medication administered to control seizures in children is frequently laced with sugars to make it more palatable. The medication then reduces salivary flow, making the child more vulnerable to dental decay [30]. Moreover, children with CP may have reduced control of gastrointestinal mobility, which reduces food intake and may result in malnutrition [31]. These children often require high calorie supplementary feeding to maintain body weight, and these supplements are high in extrinsic sugars which have a deleterious effect on oral health [32]. It is not surprising therefore that children with CP may have reduced levels of oral health.
Routinely visiting the dentist and toothbrushing are considered to be caries-preventive measures [33][34][35]. In our study, only 23.6% of IDC had visited a dentist in the preceding 12 months and 32% of IDC brush their teeth more than once a day; their prevalence rates for caries and DMFT scores were significantly lower in comparison with those of other children (p < 0.01). In China, because of a lack of dentists [36] and insufficient programs for public information and education about oral health, many parents have little access to information on dental health [37], and parental lack of scientific understanding can result in low rates of dental consultation for IDC faced with caries lesions [9,38]. Further, IDC always have difficulties in self-cleaning and communicating oral health needs [39]. They also cannot understand the significance of oral cleanliness, and tend not to cooperate and even resist toothbrushing, which is another barrier to parental success in helping their children with oral hygiene [5]. Toothbrushing as an effective method for the mechanical removal of bacterial biofilm [40] is even more important for these children [41]. The results of our study concluded that brushing twice a day helps to lower the prevalence of dental caries. The odds ratios for children who brushed their teeth twice a day were significantly lower than for those who brushed their teeth daily or less often, with an odds ratio of 0.5 (95% CI = 0.3-0.8). We recommend that the likelihood of dental caries prevention be strengthened by improving the frequency of toothbrushing to at least twice a day for IDC. Therefore, there is an urgent need for the government to take actively oral health promotion measures, intervening in the oral health of IDC. According to the WHO [42], building healthy public policy is important for policy-makers. In the early 21st century, the American Academy of Pediatrics developed the concept of a "dental home", which means "an ongoing relationship between the dentist and the patient, inclusive of all aspects of oral health care delivered in a comprehensive, continuously accessible, coordinated, and family-centered way" [25]. Chinese policy makers may learn from this concept to establish a "Chinese dental home". Due to the lack of dentists, the cultivation of a communitybased dentist is now a top priority for the government, which can improve the children's access to dental care and address the above barriers to dental services for IDC. In addition, a supportive environment and comprehensive oral health educational programs for parents are also imperative, to improve parental skills in maintaining the oral health of their children and provide an important basis for enhancing the role of parents in preventing dental caries among IDC.
Fewer DMFT scores were found for males than for females in this study, which was similar to the study done by Yee and Altun [5,43], while in contrast to findings of Sachin [44]. Chinese patriarchal traditions might be a reason that parents with male children were likely to pay more attention to their health compared with that of their female children. This requires further study.

Conclusions
The results of this study show poorer dental health status in IDC, who have higher caries prevalence rates and DMFT scores, and enhance our understanding of the role that oral health behaviors play in the dental health status of IDC in Guangzhou, China. IDC with CP have a higher risk of caries experience than IDC without CP, while toothbrushing more than twice a day and routine dental visits are cariesprotective factors. These results indicate that improving the IDC's access to dental care and comprehensive oral health educational programs for parents are urgently needed, which may lead to a reduction in dental caries levels in IDC.