Sleep and its association with dental caries or myopia in first graders

Abstract

Aim

First grade is a transition from pre-school to school-age. The change in lifestyle behaviours such as sleep may have a physiological response, which contributes to the presence or absence of two highly incident diseases: dental caries or myopia. The aim of the study was to examine the association between sleep and myopia as well as sleep and dental caries in first graders.

Design

It is a cross-sectional study.

Methods

This was a recruitment phase of an interventional study. A total of 338 children whose caregivers completed a Children's Sleep Habits Questionnaire. Caregivers also provided information regarding myopia and caries status of children and their parents. Binary logistic regression was applied to analyse the potential risk factors.

Results

Dental caries and myopia rates were 45.9% and 9.5%, respectively. After adjusting for children's gender, children's age, fathers with caries and mothers with caries, the odds ratio for dental caries in children who slept less than 9 h when compared to those who slept for nine and more hours was 1.94. Mothers with caries were 3.37 times more likely to have children with caries than mothers without caries. However, sleep was not associated with myopia in first graders.

Conclusion

Sleeping less than 9 h and maternal caries were risk factors of children developing dental caries. Future sleep and myopia studies can be conducted on higher graders who may present prolonged exposure and accumulations of myopic risk factors.

Implications

Screening of children with insufficient sleep is needed for nurses to enable the early identification of high-risk groups for dental caries in school settings. Family nurses are encouraged to work with family members to implement tailored sleep interventions, in order to facilitate better sleep and oral health practices in both school and home settings.

Registration

This study protocol was registered on ClinicalTrials.gov (Registration number: Redacted).

INTRODUCTION

Dental caries and myopia are two highly prevalent public health concerns that arise from family–lifestyle interactions. According to a systematic review from 1995 to 2019, the prevalence of caries in deciduous teeth and permanent teeth were 46.2% and 53.8%, respectively (Kazeminia et al., 2020). The American Academy of Ophthalmology had announced that the onset and the progression of myopia have become a global burden especially in East Asia (Modjtahedi et al., 2021). Family lifestyle like parental behaviours and sleep habits are modifiable factors that can predict susceptibility to human diseases, including dental caries and myopia (Enthoven et al., 2019; Shungin et al., 2019; Zhang et al., 2020).

Later or inadequate sleep contributes to poor oral conditions. The function of saliva contains remineralization, clearance, buffering, and lubrication. The salivary flow rate declines during sleep. With a low bacteria clearance rate, the bacteria in oral capacity may proliferate (Carlson-Jones et al., 2020). Moreover, when sleep deprivation occurs, the amount of saliva secretion innervated by the sympathetic nerves is relatively low compared to the production of saliva dominated by the parasympathetic nerves (Edgar et al., 2012). As a result of salivary hypofunction, the abundance of bacteria in the oral cavity becomes more than normal status. The risk of dental caries may increase (Carlson-Jones et al., 2020). Another explanation is that with insufficient sleep, the activation of leptin-sympathetic nerve systems dysregulates alveolar bone metabolism. The leptin-mediated sympathetic nerve system elevates the bone resorption markers and disturbs bone turnover through osteoblasts and osteoclast differentiation (Kuriyama et al., 2017). Inadequate sleep duration may also lower the host immunity in human beings as shorter sleep or sleep deprivation elevates cortisol levels. High cortisol levels compromise the immune response and thus induce low-grade inflammation (Besedovsky et al., 2019). However, salivary melatonin, a sleep hormone, was exploited to rival oxidative stress in the process of oral inflammation. With appropriate sleep durations, the production of salivary melatonin can mitigate carcinogenesis and generate osteoblast (Saeralaathan et al., 2021).

In addition to dental caries, internal and external cues have supported the correlation between sleep and myopia; however, it is still controversial that abnormal sleep patterns are associated with the risk of myopia. In terms of internal cues, dopamine is a hormone that prevents eye axial elongation. Melatonin is a sleep-promoting hormone. These two hormones have antagonist effects. As sleep–wake patterns are delayed, the delayed secretion of melatonin interacts with dopamine in the retina cells during the daytime. As a result, the suppression of dopamine release may weaken its effect on myopia prevention (Kearney et al., 2017). Moreover, external cues such as light and vision input entrain through activating melanopsin on the retinohypothalamic tract and connecting the pathway to the suprachiasmatic nucleus. Dopamine can also be produced by amacrine cells and interplexiform cells in the eyes. When the external cues enter the retina, the complex interaction of these neuromodulators influences retinal circadian rhythm as well as eye growth (Chakraborty et al., 2018). Some studies indicated that child myopia was associated with poor sleep quality, later bedtime and shorter sleep duration (Gong et al., 2014; Liu et al., 2020), whereas another study found that the significant association between sleep duration and myopia did not exist (Tsai et al., 2021).

Despite well-promoted school health programmes in the prevention of myopia and dental caries, these two diseases remain highly incident in primary grade and highly prevalent in school-age children. First grade is a transition from preschool to school age. A study in Asia also revealed that more than two-thirds of first graders had sleep disturbances (Amaerjiang et al., 2021). It is unknown whether sleep is associated with children's myopia and dental caries during this transition period. Understanding the application of sleep physiology in clinical practice is needed because the more sufficient sleep children receive, the fewer adverse health-related outcomes they may suffer from. Therefore, we initially analyse the data in our recruitment stage of a sleep interventional study to examine the relationship between sleep and dental caries, and also sleep and myopia in Taiwanese first-graders. We hypothesized that (a) problematic sleep would be positively associated with the presence of dental caries in first graders and (b) problematic sleep would be positively associated with myopia in first graders. The problematic sleep includes children with disturbed sleep behaviours, late bedtimes and less than 9 h of sleep.

METHODS Study design

This cross-sectional screening data was from the baseline of an ongoing sleep interventional study. We recruited first graders aged six to eight as our study participants. These participants were from 8 out of 20 public elementary schools in Taipei City, Taiwan using convenience sampling. Inclusion criteria were (1) children who were in the first grade of primary school and (2) children who were communicative and studied in normal classes. Exclusion criteria were (1) children who had congenital eye diseases; (2) children who attended school less than 15 days in the past month and (3) children who were taking medications that may influence sleep. The survey period was from 13 March 2021 to 30 April 2021. A total of 421 parents of first graders filled in the questionnaires, among them 374 provided complete data. Of those 374 children, 25 children had congenital eye diseases. Seven children took medication that may influence sleep, including antihistamine, anti-epileptic drugs, and medications of attention deficit and hyperkinetic disorders. Four children went to school less than 15 days per month due to diseases or semi-homeschooling. Figure 1 shows a flow chart of data collection. Therefore, we analysed the rest of the 338 participants. The response rate in this study was 88.8%.

FIGURE 1. Flow chart of data collection.

Data collection

Researchers contacted school nurses or teachers of first graders to distribute survey questionnaires. Faculties who agreed to assist with this study attached the questionnaire in children's family contact books. Informed consent of this study was provided on the first page of the questionnaire. Parents who were willing to participate in this survey completed the questionnaires and sent them back to school to school nurses. This survey was approved by the Research Ethics Committee of a university's full board review.

Instrument

Participants answer a brief questionnaire consisting two parts. The first part is sociodemographic data including children's birthdays, children's gender, and the marital status of the parents. The first section also covers whether the children had dental caries (yes/no), whether fathers had dental caries (yes/no/unknown), whether mothers had dental caries (yes/no/unknown), whether the children had myopia (yes/no), whether fathers had myopia (yes/no/unknown) and whether mothers had myopia (yes/no/unknown). Every semester, children receive a health examination in schools, including untreated caries and visual acuity. Dentists record children's untreated caries. School nurses assess children's visual acuity with a Tumbling E eye chart. Children whose visual acuity is less than 0.9 or who have untreated caries may receive a notice for further clinic visits. Therefore, parents can self-report their children's eye and oral health statuses according to the result of health checkups from schools. If they were uncertain of children's vision and dental health condition, we received a parental permission to obtain the data from school nurses. As for parental myopia and dental caries, we added an additional ‘unknown’ option since some parents may not have a regular health examination.

The second part of the survey process is the Children's Sleep Habits Questionnaire (CSHQ). The CSHQ was a screening instrument designed by Owens et al. (2000). This questionnaire was a primary screening for children aged between 4 to 12 with sleep problems. Children who received higher scores in CSHQ indicated that they may have more disturbed sleep behaviours. The internal consistency for the community sample was 0.68. The sensitivity of the CSHQ was 0.80 and the specificity was 0.72 (Owens et al., 2000). The Cronbach's α of the CSHQ Chinese version was 0.72 and the test–retest reliability ranged from 0.54 to 0.76 (Liu et al., 2014). Cronbach's α of the CSHQ in our study was 0.76. In this questionnaire, the respondents were asked to fill in the children's bedtime time, waking time and total sleep duration (including nighttime sleep and naps).

Data analysis

Statistical Program for Social Sciences Version 22.0 (SPSS™, IBM Inc., Armonk, NY, USA) was applied to statistically analyse the data. Descriptive statistics included frequencies, the mean and the standard deviation. The rising time and the total score of the CSHQ underwent natural log transformation for normality for inferential statistics, yet we reported the original data of mean and standard deviation. We also used the chi-square test and compared means between children with and without myopia as well as children with and without caries. For those whose parental caries status was unknown, we used multiple imputation methods to achieve less than 20.0% of cells with numbers less than 5. We selected children with caries, fathers with caries, and mothers with caries into the model to be analysed. Finally, binary logistic regression was used to further evaluate the association between sleep variables and children with dental caries. We chose children's age and children's gender as covariates and put the variables that were statistically significant in the chi-square test, including fathers with caries, mothers with caries and sleep duration for data analysis. According to the recommendation of the National Sleep Foundation, school-age children should sleep nine to 11 h per day (Hirshkowitz et al., 2015). Therefore, we divided total sleep time into a dichotomous variable: <9 h and ≧9 h.

RESULTS

In this study, the dental caries rate was 45.9% and the myopia rate was 9.5%. Table S1 shows the characteristics of first-graders and their parents. The mean age of first-graders was 6.68 ± 0.53 years old. Approximately two-thirds of parents had myopia and dental caries. Fathers with caries and mothers with caries were significantly associated with children with caries (both p = 0.01).

Table S2 shows the average total sleep duration, bedtime, rising time, and total CSHQ score of children with and without myopia or dental caries. The average total sleep duration was 9 h and 12 min ±50 min per night, the average bedtime was 21:37 ± 00:40, and the average rising time was 06:50 ± 00:20. The mean total CSHQ score was 47.43 ± 6.65. Children with dental caries slept significantly less than children without caries (F = 8.58; p = 0.004). After adjusting for fathers with caries, mothers with caries, gender and age, total sleep duration less than 9 h has 1.94 (95% CI = 1.32–2.84, p = 0.001) times higher risk of dental caries than children sleep ≧9 h. The odds ratio of mothers with caries compared to the reference of mothers without caries was 3.37 (95% CI = 2.10–5.48, p < 0.001) (Table 1).

TABLE 1 Binary logistic regression of children with caries (N = 338).

[Table omitted. See PDF]

Abbreviations: CI, confidence interval; OR, odds ratio; Ref, reference; SE, standard error.

^*p < 0.05.

DISCUSSION

Sleep duration of fewer than 9 h was a significant risk factor of children with dental caries. This result was consistent with another Japanese study conducted in children aged 3–6 (Ogawa et al., 2021), and can be supported by biological and behavioural evidence. First, a decrease in the bacteria clearance rate during sleep increases the number of bacteria, and thus contributes to the risk of dental caries (Arvidsson et al., 2015; Edgar et al., 2012). Studies in Kuwait and Australia both found a considerable increase in oral bacteria during sleep (Alqaderi et al., 2020; Carlson-Jones et al., 2020). Furthermore, with abnormal sleep patterns, the interaction of the leptin-sympathetic system may contribute to bone dysregulation (Kuriyama et al., 2017). Lower salivary leptin was observed in Kuwait children with caries (Alqaderi et al., 2020). Last, short sleep duration may dysregulate immunity, resulting in chronic inflammation (Besedovsky et al., 2019). Another cross-sectional study in Japanese school-age children also suggested this hypothesis (Asaka et al., 2020). However, different from our finding, the Kuwaiti study showed that sleep duration acted as a modifier between children's bedtime and dental caries (Alqaderi et al., 2020). In our study, bedtime found no associations with dental caries, yet sleep duration was found to be a potential risk factor for dental caries.

Parental dental caries, especially for mothers, were associated with children's caries. This association can be explained by mother–child oral microbial similarities, lifestyle behaviours, and hereditary factors (Bretz et al., 2013; Shungin et al., 2019). Mothers and children share oral microbial similarities, which was reported in several oral microbial studies. Maternal–infant transmission shaped such identical oral microbial and could persist into early childhood (Bretz et al., 2013). Bretz et al. (2013) showed that 91.0% of mothers or children had at least one kind of oral risk factors, such as Streptococcus mutans (MS) and plaques. Mothers' caries was significantly associated with the transmission of MS. Moreover, maternal health literacy and behaviours tend to influence children's health behaviours (Lee et al., 2018; Ono et al., 2021). In terms of genetic factors, taste genes and immunity are influencers in caries aetiopathogenesis. Taste genes determine food preferences in human. Sweet receptor families like Taste 1 Receptor Member 2 (TAS1R2) and Taste 1 Receptor Member 3 (TAS1R3) are sensitive to sucrose, which may influence sweet preferences in children. Major histocompatibility complex (MHC) molecules controlled by chromosome 6 may incite various immune responses in oral microbial populations and enhance the susceptibility to caries (Opal et al., 2015).

In this study, there was no association between children's sleep and the risk of myopia. This finding is consistent with another Taiwanese national survey (Tsai et al., 2021). In Tsai's 2005 study, even in multivariate analysis of the survey, sleeping more than 9 h was a protective factor against myopia, but this significant finding no longer existed in the year 2016. However, we should generalize this result with caution since there may be other unpredicted but crucial factors that contribute to myopia more than sleep, such as screen time. Another possibility is that sleep phase delay was barely found in school-age children. Our biopathological assumption from previous studies was that sleep phase delay may also delay melatonin release and thus interact with the dopaminergic effect in the retina (Kearney et al., 2017). However, the included participants were children who attended school more than 15 days per month. Following school routines, they may receive a regular sleep–wake pattern on weekdays. Hence, as the release of dopamine in the retina during daytime is hard to be inhibited by the effect of melatonin, the antagonist effects of melatonin and dopamine may be weakened.

Children's myopia is unrelated to parental myopia. This result is inconsistent with previous studies (Enthoven et al., 2019; Zhang et al., 2020). One possible reason is that there were few myopic children in our first-grade samples, which implies the occurrence of myopia may require more time to accumulate exposure to potential risk factors. Further studies should be conducted longitudinally or aim at middle or high grades of primary schools. Another possibility is that most of the research that discussed the gene–lifestyle interaction focused on early childhood (Enthoven et al., 2019). Our study excluded children with congenital eye diseases. This exclusion may weaken the genetic effect in children with myopia. Although the previous study indicated that heredity accounted for approximately 12.0% of the predictors, the percentage was still lower than the effect of lifestyle behaviours that contribute to more than 50.0% (Zhang et al., 2020). As children were in the process of socialization, the effect of lifestyle behaviours may far surpass the unchanged genetic effect. Protective factors like outdoor activities could counteract and override the adverse effect of myopic genes.

Implications of nursing education and clinical practice

Sleep, being a relatively new area of nursing, is infrequently mentioned in most nursing education curricula. Therefore, there is a need to encourage nursing students and nurses to undertake continuing education courses on sleep. Moreover, nurses in clinical settings can enhance their skill in caring for paediatric patients by gaining a more comprehensive understanding of sleep. For example, a decrease in sleep duration is likely to indicate certain physical discomfort.

Implications of school nursing

School nurses can improve the coordination of healthcare in the context of students' families and communities. These nurses play an important role in screening, prevention, and intervention in health-risk behaviours such as insufficient sleep. Screening for insufficient sleep is essential for school nurses to quickly assess children's sleep problems, and for early detection of high-risk groups for dental health issues. However, there is a lack of school health curricula promoting paediatric sleep hygiene. Thus, sleep hygiene principles should be integrated into health-related programmes, for instance, adequate sleep duration should be promoted as a facilitator of better oral hygiene. Moreover, during the implementation of health educational programmes, school nurses can encourage parents, especially mothers, to participate. This is essential as this study shows that maternal caries are strongly associated with children's caries; moreover, most mothers are the primary caregivers of children. Their behaviours can have the greatest impact on their children.

Implications of family nursing

This study provides additional evidence indicating that short sleep duration is a risk factor for dental caries in children. Because first-graders spend the majority of their time at home, the family environment emerges as another crucial setting for promoting optimal sleep practices for children's health, in addition to schools. By embracing the principles of family-centred care, health care providers can forge collaborative partnerships with family members (Kuo et al., 2012). Moreover, nurses, whether in schools or healthcare facilities, can lead health educational initiatives, as well as motivate primary caregivers to become actively engaged. These caregivers can thus gain invaluable insights into the impact of sleep duration on children's oral health through interactions. Furthermore, family nurses have the acumen to identify existing family routines that require refinement, provide carefully tailored sleep interventions, and to gradually establish children's bedtime routines. For example, reduction in children's sugar or caffeine intake before bedtime is recommended. With the collaboration and involvement of nurses and primary caregivers, sleep hygiene for children's health and wellbeing, including both the school and home environment, could be thoroughly implemented.

Implications of future studies

Nearly half of the first-graders (45.9%) in this study already had dental caries. Further, we found a correlation between sleep duration in first-graders and the presence of dental caries. These results suggest that implementation of preventive measures could potentially begin at pre-school ages. As for the association between myopia and sleep, the different found may require an investigation in higher grade students. Nevertheless, as most previous studies indicate myopia is highly prevalent in school age children, implementation of sleep and myopia intervention programmes should be considered for immediate application in lower-grade students (Grzybowski et al., 2020).

Limitations

There were several limitations in this study. First, some lifestyle behaviours before bedtime were not included in this preliminary survey. For example, bedtime sugar consumption may be a risk factor for dental caries. Second, this questionnaire was self-reported and distributed by school faculties. It is possible that more socially desirable answers are given. As technologies advances, future studies can provide online questionnaires instead or examine the association with objective instruments to measure the exact sleep duration. Third, the study was suspended due to the coronavirus pandemic and the school closure in May 2020, yet we still find some significant predictors in this study. Fourth, this was a cross-sectional study; therefore, the results cannot explain the causal relationship between sleep and dental caries. Future studies can conduct interventional research to examine the cause and effect. Last, for the purpose of intervening in our ongoing interventional study, we selected first graders as our study participants in terms of early prevention. However, few children with myopia were enrolled. As children age, total sleep duration becomes less. It is more likely to have significant findings in sleep variables. Further studies could focus on higher grades. Older students may present the effect of prolonged exposure and accumulation of lifestyle risk factors in children's myopia.

CONCLUSION

Children's sleep duration of fewer than 9 h was a risk factor for dental caries. Parents especially mothers who commonly act as primary caregivers play crucial roles in maintaining children's sleep and oral health. Sleep educational programmes may be needed for nurses as well as families. Nurses in school settings can screen for children with insufficient sleep and early prevent children from adverse health outcomes such as dental caries. Meanwhile, family nurses can promote sleep health and design tailored bedtime interventions based on different family backgrounds. Future studies can explore the causality of sleep and dental caries by using objective measurements to validate sleep quantity. Further sleep and myopia research can be conducted on higher graders since it may take more time to accumulate those myopic risk factors.

AUTHOR CONTRIBUTIONS

Han-Yi Tsai: Study design, data collection, data analysis, interpretation of the results and preparation of the manuscript. Tzu-I Tsai, Yin-Lin Wang and Hung-Chi Chen: Study design, interpretation of the results and revision of the manuscript. Chien-Chang Lee: Study design and revision of the manuscript. Shao-Yu Tsai: Study design, data analysis, interpretation of the results and revision of the manuscript.

ACKNOWLEDGEMENTS

The authors thank all the caregivers, school nurses and teachers whose assistance and participation made this study possible.

FUNDING INFORMATION

This study was supported by a Foxconn Education Foundation Scholarship. This article was subsidized for English editing by National Taiwan University under the Excellence Improvement Programme for Doctoral Students (grant number 108-2926-I-002-002-MY4), sponsored by the National Science and Technology Council, Taiwan.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

DATA AVAILABILITY STATEMENT

Data are available from the corresponding author on reasonable request.

PATIENT OR PUBLIC CONTRIBUTION

Parents of first graders contributed to this investigation.

INSTITUTIONAL REVIEW BOARD APPROVAL

This study is approved by the Institutional Review Board of National Taiwan University (Institutional Review Board approval number: NTU-REC No.: 202007HM010).