Community Dent Oral Epidemiol 2014; 42; 553–562 All rights reserved
Ó 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental caries and fluorosis experience of 8–12-year-old children by early-life exposure to fluoride
Loc G. Do1, Jenifer Miller1, Claire Phelan2, Shanti Sivaneswaran2, A. John Spencer1 and Clive Wright2 1 Australian Research Centre for Population Oral Health, The University of Adelaide, Adelaide, SA, Australia, 2The Centre for Oral Health Strategy, Sydney, NSW, Australia
Do LG, Miller J, Phelan C, Sivaneswaran S, Spencer AJ, Wright C. Dental caries and fluorosis experience of 8–12-year-old children by early life exposure to fluoride. Community Dent Oral Epidemiol 2014; 42: 553–562. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Abstract – Background: It is important to evaluate concurrently the benefit for dental caries and the risk for dental fluorosis from early exposure to fluoride among children. Aim: To evaluate associations of different levels of exposure to fluoride in early childhood with dental caries and dental fluorosis experience in school children. Methods: A Child Dental Health Survey (CDHS) was conducted among school children in the Australian state of New South Wales (NSW) in 2007. Trained and calibrated examination teams conducted oral epidemiologic examinations to assess caries experience as decayed, missing or filled tooth surfaces of the primary and permanent dentitions (dmfs/DMFS) and fluorosis using the Thylstrup & Fejerskov (TF) index on the maxillary central incisors only. A parental questionnaire collected information on residential histories and tap water usage to enable calculation of percentage of 3-year lifetime exposure to fluoride in water. Use of dietary fluoride supplements was also collected. Dental caries and fluorosis experience were compared among groups by levels of exposure to fluoride from water and fluoride supplements in bivariate and multivariable analysis, controlling for socioeconomic factors. Results: Exposure to different fluoride sources varied in the group of 2611 children aged 8–12 years. Lower household income was significantly associated in both bivariate and multivariable analyses with the greater prevalence and severity of primary tooth caries among 8–10-year-old children and permanent tooth caries among 8–12 year old. Exposure to fluoride in water during the first 3 years of life was associated with both caries and fluorosis experience observed at age 8–12 years. Having higher percentage of 3-year lifetime exposure to fluoride in water was associated with higher prevalence of mostly mild fluorosis, but significantly lower prevalence and severity of caries in the primary and permanent dentitions. Conclusion: There were significant associations of dental caries and fluorosis experience with sources of early childhood fluoride exposure among children aged 8–12 years in New South Wales. Exposure to fluoridated water during the first 3 years of life was associated with better oral health of school-age children.
Fluoride use has been considered as one of the main contributing factors in improving the oral health status of child populations in many western doi: 10.1111/cdoe.12106
Key words: children; dental caries; dental fluorosis; fluoride Loc G. Do, ARCPOH, School of Dentistry, The University of Adelaide, Adelaide, SA 5005, Australia. Tel.: +61 8 8313 3964 Fax: +61 8 8313 3070 e-mail: [email protected] Submitted 30 December 2012; accepted 12 March 2014
countries (1, 2). Two main vehicles of fluoride delivery are water fluoridation and use of fluoridated toothpaste for toothbrushing. Water fluoridation
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is an effective and equitable programme that affords passive exposure to a low concentration of fluoride, while toothpaste use requires more active user participation. While exposure to fluoride in either water or toothpaste during early childhood is necessary to protect teeth, that exposure is associated with a certain level of risk of dental fluorosis, a developmental condition of tooth enamel (3, 4). Intake of fluoride during the first 3 years of life can increase the risk of having dental fluorosis on permanent incisors, the most aesthetically important teeth. The risk period for all permanent teeth, except third molars, can be up to 8 years of age. The best use of fluorides involves a balance between protection against dental caries and risk of dental fluorosis. The risks of having dental caries and fluorosis in a population can change over time, depending on the patterns of use of different fluoride sources. There is always a need to monitor the balance between risk and benefit of all early exposures to fluoride. Contemporary and relevant data would assist in the promotion, maintenance and regulation of water fluoridation, as well as guidance on the use of other forms of fluoride. There have been previous attempts to evaluate the trade-off of risk and benefit with early fluoride use (5–7). The recent large-scale population-based study of child oral health in the largest Australian state of New South Wales (NSW) (8) has provided an opportunity to further contribute to the scientific evidence on this issue. This study aimed to evaluate associations of different levels of exposure to fluoride in early childhood with dental caries and fluorosis experience in NSW school children. We hypothesized that early childhood exposure to fluoride was associated with both dental fluorosis and caries among school-aged children.
Methods Study design and sample selection Data for this analysis were collected in a cross-sectional population-based study. The NSW Child Dental Health Survey 2007 (NSW CDHS) covered a population representative sample of children aged 5–12 years from NSW (8). A two-stage sampling design was employed, with schools defined as the primary sampling units. Schools were stratified by NSW health service regions and a sample of schools was randomly selected from each region to
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ensure adequate regional representation. The school selection was conducted with probability of selection proportional to size. The Australian Research Centre for Population Oral Health (ARCPOH) at the University of Adelaide developed the study design, sampling strategy and examination manual and assisted in examiner training, calibration and data capture. Prior to selection, schools within each region were sorted by the Index of Relative Socio-Economic Disadvantage, which is one of the Australian Bureau for Statistics (ABS) Socio-Economic Indexes for Areas (SEIFA) (9), to ensure a spread of schools from regions with various socioeconomic backgrounds. A stratified random sample of children enrolled at each of these schools was selected based on age and sex distribution. Selected children’s families were sent an invitation package with a parental consent form. Children whose consent for participation was received were examined at schools by specially trained and calibrated examination teams comprised of an examiner and a data recorder. Ethical clearance was given by the University of Adelaide Human Research Ethics Committee, the NSW Population and Health Services Research Committee and the NSW Department of Education and Training.
Examination for oral health outcomes Twenty teams of calibrated dental examiners and recorders collected the oral health outcome data during the 2007 calendar year. Standard equipment, including portable air syringe compressors, lighting and blunt periodontal probes, were used. An examination protocol was developed based on the standard oral epidemiological indices for assessment of caries experience (10, 11) and dental fluorosis (12). The oral assessment was conducted primarily with visual criteria under two sources of light: an external portable dental light and an intraoral light. The blunted periodontal probe was mostly used to clean debris and to ‘feel’ surface roughness when distinguishing tooth colour restoration from enamel. Examiners were instructed to clean teeth with gauze and continually dry teeth with compressed air to ensure good vision. No X-ray was used. A dentist, acting as a principal survey examiner, jointly conducted the training and calibration of examination teams and also completed interexaminer reliability sessions with the field examiners on a subsample of children. A principal trainer, LGD,
Dental caries and fluorosis experience in children
also accompanied the principal examiner during the first two of her repeated examination sessions with each of the field examiners. The reliability of each of the examiners relative to the principal survey examiner was determined by calculating the intraclass correlation coefficient (ICC) of count data for each replicate pair and the Kappa values for categorical coding of individual tooth and surface status. Interexaminer reliability of examinations at tooth level for dental caries and individual level for dental fluorosis was reported elsewhere (8), with kappa scores ranging from 0.83 to 0.99.
Main oral health outcomes Two oral health outcome variables were used in this study, which represent two sides of the balance of exposure to fluoride in early childhood: dental caries and dental fluorosis. The history of dental caries in an individual was recorded at the tooth surface level. Dental caries was recorded when carious cavitation including enamel cavitation and/or dentinal involvement was observed. Noncavitated carious lesions were also recorded but not used in this analysis. Primary reasons for restorations were identified to distinguish fillings because of dental caries versus fillings for any other reasons. Causes of missing teeth were also distinguished between dental caries and other reasons. The average number of decayed, missing or filled tooth surfaces (dmfs/DMFS) is an expression of the extent of the disease in the population. The prevalence of dental caries experience on either primary or permanent dentition was estimated. Presence of dental fluorosis was assessed only on the two maxillary central incisors. Although the prevalence of dental fluorosis would be higher if other posterior teeth were assessed for dental fluorosis, the central incisors were used because they are most aesthetically important. If a tooth had a tooth-coloured filling or less than half of its crown erupted, or the child had fixed orthodontic band, the tooth was excluded from fluorosis examination. Fluorosis was differentiated from nonfluorotic opacities using the Russell differential diagnostic criteria (13). Severity of fluorosis was evaluated after air dry using a modified Thylsrup and Fejerskov (T-F) Index (12). The modified index has all scores from 0 to 4 identical to the original TF index. The TF scores 5 to 9 are collapsed to a single score 5 because very few children in the population were expected to have severe fluorosis that results in loss of enamel, based on fluorosis observed in another similar Australian population (14). For this
analysis, a case of fluorosis was defined as having a TF score of 2 + on one or both the maxillary central incisors.
Data collection covariates
of
main
exposure
and
Parents of the children who underwent examination were sent a written questionnaire to collect basic demographic, socioeconomic, dental behaviour and fluoride data, history of residential movement, Indigenous status, household income, parental education, and use of other forms of fluoride. The questionnaire had a 76% response rate. These questionnaire data allowed for evaluation of two forms of fluoride exposure in early childhood: exposure to fluoride in water during the first 3 years of life and use of dietary fluoride supplements. The main exposure variable was the measurement of exposure to fluoride in water which was converted to percentage of lifetime exposure to fluoridated water during the first 3 years of life. The calculation was based on a method described elsewhere (5, 14, 15). Briefly, the questionnaire asked parents to list all locations where the child had lived and the time period for each location. Those locations were linked with a database of fluoride levels in Australian public water supplies. Other nonpublic waters were assumed to have negligible fluoride levels. Parents were also asked to estimate the child’s proportion of public water usage as part of all drinking water consumption for each period of residency listed. The categories of this estimate were ‘Almost none’; ‘About half’; and ‘Almost all’. The responses to this question were used to adjust the 3-year lifetime exposure to fluoride in water using three values: 0 was used if the response was ‘Almost none’; 0.5 was used for ‘About half’ response; and 1 was used if the parent responded that ‘Almost all’ fluid consumption of the child was from public water supply. The formula used in the calculation of percentage of 3-year lifetime exposure E was as below. E ¼ R(time(in months) at a residency during age periodiÞ fluoride level in public water percentage of public water usage age (in months) 100: The present paper used the life period from birth to age 3 years (total age included in the above for-
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mula equal to 36 months). The estimate of 3-year lifetime exposure was used to classify children into three groups: having 0% lifetime exposure, having >0 & ≤99% lifetime exposure, and having 100% lifetime exposure. The period from birth to age 3 years was used because it is the peak risk period for fluorosis on the permanent upper central incisors (1, 12, 16). Parents of the children were asked to indicate if the child used dietary fluoride supplements (in the form of fluoride tablet or drop) and number of times it was used per day. Because of the low number of children who reportedly used fluoride supplements, the responses were used to dichotomize children into never-used or ever-used groups. The covariates in the analysis were age at examination, sex, and two indicators of socioeconomic status: household income and highest educational attainment of each parent. Household income in Australian dollars was collected as income ranges. Highest level of educational attainment of parents was used to group children into three groups. Low education was assigned to children whose parents had only secondary school education or lower, medium was assigned if at least one parent had both school and vocational (trade, apprenticeship) training, and high was assigned when at least one parent had any university education or higher.
Data preparation and analysis For the analysis in this report, only children aged 8–12 years were included because not all younger children had their maxillary central incisors erupted sufficiently for fluorosis examination. Data analysis was performed in SAS for Windows version 9.3 (SAS Institute Inc., Cary, NC, USA) and SUDAAN for Windows version 10.0 (RTI International, Research Triangle Park, NC, USA). The sample was re-weighted to adjust for different sampling ratios and response rates to produce estimates representative of the NSW child population. A total sample of 2611 children (76% of children aged 8–12 years) who had both clinical and complete questionnaire data was included in the analysis. Percentages and mean scores were weighted estimates. The analysis was conducted progressively from bivariate to multivariable analysis. Analysis was conducted separately for the experience of dental caries and fluorosis. The prevalence of caries and fluorosis was compared among the groups by different levels of fluoride exposures and socioeconomic variables. Adjusted prevalence ratios (PR)
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for both caries and fluorosis between the exposure groups and the respective reference groups were calculated using Poisson regression models with robust variance estimation (SUDAAN Procedure LOGLINK) to adjust for complex sampling procedures (17, 18). This procedure is a standard method for estimating prevalence ratios for data collected with stratified, multistaged sampling procedures. The associations between the prevalence of dental caries and fluorosis and different levels of fluoride exposures in early childhood were evaluated, with adjustment for other factors. Two-way interactions between different factors were tested. However, none of the interactions were statistically significant and were not included in the final models. The mean decayed, missing or filled tooth surfaces (dmfs) scores were calculated as a measure of caries experience in the primary dentition for children aged 8–10 years while the similar measure of caries in the permanent dentition (DMFS) was calculated for all 8–12-year-old children. Adjusted rate ratios (RR) were calculated for mean dmfs/ DMFS between the exposure groups and the respective reference groups using multivariable regression models. Negative binomial distribution was specified in the models using SAS procedure GLIMMIX to address the complex sample design of the data (19). It is well known that dmf/DMF indices are count variables with over-dispersion that justifies the use of negative binomial distribution in the models (8, 20, 21). Zero-inflated models can also be suitable (21). However, fitting a zeroinflated model for data with complex sample design is computationally complex. Negative binomial regression for count of dental caries teeth or surfaces is closely comparable to zero-inflated regression model (20). The associations between caries with the available fluoride exposures were evaluated. Two-way interactions between factors were also tested but not included in the final models because of lack of statistical significance. In tables, where indicated, numbers of children are un-weighted, while percentages and mean values are weighted. Therefore, multiplying the estimates by the number of subjects may not yield integers of individuals.
Results A total of 2611 children aged 8–12 years were included in the analysis (Table 1). The distribution by age and sex reflected population benchmarks.
Dental caries and fluorosis experience in children Table 1. Study sample sociodemographic characteristics and exposure to fluoride in early childhood N (total 2611)
W%
95% CI
Age at examination 8 years 473 20.2 18.9–21.5 9 years 450 20.5 19.2–21.8 10 years 483 20.1 19.0–21.2 11 years 716 19.7 18.8–20.7 12 years 489 19.5 17.9–21.2 Sex Male 1319 51.2 48.3–54.1 Female 1292 48.8 45.9–51.7 Percentage of life exposure to F in water (birth to 3 years) 100% lifetime 1498 64.0 60.3–67.8 >0–99% lifetime 557 21.3 19.0–23.7 0% lifetime 386 14.6 11.4–17.9 Household income ≤40 000 AUD 548 22.2 19.0–25.4 >40–80 000 AUD 810 32.7 29.9–35.5 >80–120 000 AUD 642 25.7 23.0–28.4 >120 000 AUD 437 19.4 15.6–23.2 Parental education Low 624 24.1 20.9–27.3 Medium 1490 57.4 54.7–60.2 High 472 18.5 15.6–21.4 Dietary fluoride supplement use Never used 2419 94.2 92.7–95.6 Ever used 186 5.8 4.4–7.3 W%, weighted per cent; 95% CI, 95% Confidence Intervals. Data were weighted to represent population estimates. Some variables have missing data.
More than 60% of the children had almost all of their first 3 years of life exposed to fluoride from water, while just fewer than 15% had almost no exposure to fluoridated water during that age period. Some 21% of the children had some but less than 100% of their first 3 years of life exposed to fluoride in water. Just over a fifth of the sample was in the lowest income category while slightly less than a fifth was in the highest (over AU$120 000/year) category. The large majority of the children had never used dietary fluoride supplements. Approximately 25% of the sample had some level of dental fluorosis on maxillary central incisors. About 10% had at least one maxillary central incisor with fluorosis at TF score of 2 or higher. Most of the children (22% from those 24.6%) who had fluorosis on their maxillary central incisors had very mild or mild fluorosis (TF scores of 1 or 2) (Table 2). Some 2.6% of the total sample had a TF score of 3 or 4, while there were no cases of more severe fluorosis (data not shown). The prevalence of fluorosis was lowest among those who had 0% lifetime exposure to fluoride in water. The two groups with at least some exposure to fluoride in water had similar prevalence of fluorosis on their maxillary central incisors. There was some variation in the prevalence of dental fluorosis by household income and parental education.
Table 2. Distribution of maxillary central incisor fluorosis scores by sample characteristics–bivariate analysis Fluorosis experience (unadjusted) Total
TF 1 row% (SE)
Total 24.6 14.7 (0.8) Percentage of life exposure to F in water (birth to 3 years) 100% 26.2 15.0 (1.0) >0–99% 28.0 18.8 (2.0) 0% 16.9 10.2 (1.5) Household income ≤40 000 AUD 20.1 11.6 (1.5) >40–80 000 AUD 22.5 13.5 (1.3) >80–120 000 AUD 27.8 16.7 (1.6) >120 000 AUD 28.1 17.9 (2.1) Parental education Low 23.4 12.8 (1.5) Medium 24.8 15.2 (1.0) High 25.1 15.4 (1.9) Dietary fluoride supplement use Never used 24.8 14.7 (1.1) Ever used 19.6 14.7 (2.8)
TF 2 + row% (SE)
Multivariable modela Prevalence of TF 2 + PR (95% CI)
9.9 (0.7) 11.2 (0.9) 9.2 (1.5) 6.7 (1.4)
1.86 (1.14–3.05) 1.33 (0.71–2.50) Ref
8.5 (1.3) 9.0 (1.1) 11.1 (1.4) 10.2 (1.7)
0.78 (0.46–1.34) 0.89 (0.52–1.51) 0.97 (0.64–1.46) Ref
10.6 (1.4) 9.6 (0.9) 9.7 (1.6)
1.30 (0.72–2.32) 1.02 (0.63–1.63) Ref
10.1 (0.7) 4.9 (1.87)
1.46 (0.91–2.34) Ref
SE, standard error of the percentage; PR, prevalence ratios, estimated using multivariable regression models for Poisson distribution with robust variance estimation; CI, Confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. a Multivariable model for the prevalence of cases with TF score 2+ on maxillary central incisors, all variables, age and sex were included in the models.
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The multivariable model for the prevalence of dental fluorosis defined as having a TF score of 2 + confirmed the association between exposure to fluoride in water in the first 3 years of life and the prevalence of dental fluorosis. Children who had 100% of the period from birth to age 3 years exposed to fluoridated water had 1.86 times the prevalence of dental fluorosis compared to those who did not have any exposure. Those who had partial water fluoride exposure had higher prevalence of dental fluorosis compared with the reference group but the difference was not statistically significant. The associations between dental fluorosis and the socioeconomic variables were not statistically significant in the model. Over 34% of the children aged 8–10 years had a history of caries experience in their primary dentition, with an average of 2.69 surfaces per child (Table 3). It was clear that children who had exposure to fluoridated water during most of their first 3 years of life were less likely to have caries on their primary dentition. The intensity of caries experience measured by mean dmfs scores was also significantly lower in children who had exposure to fluoride in water. Children whose parents had only school education attainment had higher prevalence and extent of dental caries than those
whose parents had at least some university education. The association between exposure to fluoridated water and dental caries in the primary dentition was confirmed in the multivariable models for both the prevalence and extent of dental caries (Table 3). Having 100% of the first 3 years of life exposed to fluoridated water was significantly associated with 0.83 times the prevalence of dental caries and 0.65 times the count of dmfs score compared with having 0% exposure. Having some but less than 100% water fluoride exposure was also associated with significantly lower primary teeth caries experience. Children whose parents had low level of education had statistically significantly higher count of dmfs score than those with parents with high education. About a quarter of the children aged 8–12 years had experience of dental caries in the permanent dentition with the mean DMFS of 0.67 affected surfaces (Table 4). Similar to that observed in the primary teeth dentition, exposure to fluoridated water in the first 3 years of life was associated with significantly lower dental caries experience in the permanent dentition. After adjusting for other factors in the model, having 100% exposure to fluoridated water in the first 3 years of life was
Table 3. Prevalence and extent of dental caries in the primary dentition (aged 8–10 years) Caries experience (unadjusted)
Multivariable models
% (SE)1
% With caries a PR (95%CI)
Mean dmfsb RR (95% CI)
0.83 (0.70–0.99) 0.81 (0.65–1.01) Ref
0.65 (0.54–0.78) 0.66 (0.53–0.82) Ref
1.13 (0.91–1.40) 1.08 (0.88–1.33) 0.98 (0.78–1.23) Ref
1.24 (0.98–1.58) 1.21 (0.98–1.50) 0.95 (0.77–1.19) Ref
1.14 (0.90–1.40) 1.07 (0.85–1.34) Ref
1.35 (1.07–1.71) 1.04 (0.85–1.27) Ref
0.90 (0.65–1.25) Ref
0.86 (0.65–1.15) Ref
dmfs (SE)2
Total 34.1 (1.0) 2.69 (0.14) Percentage of life exposure to F in water (birth to 3 years) 100% 32.6 (1.4) 2.38 (0.18) >0–99% 31.5 (2.3) 2.30 (0.31) 0% 39.0 (2.6) 3.82 (0.43) Household income ≤40 000 AUD 39.4 (2.3) 3.70 (0.37) >40–80 000 AUD 35.3 (1.9) 2.97 (0.28) >80–120 000 AUD 30.7 (2.0) 2.12 (0.25) >120 000 AUD 30.3 (2.4) 1.95 (0.29) Parental education Low 37.9 (2.1) 3.63 (0.36) Medium 33.5 (1.4) 2.40 (0.17) High 30.7 (2.3) 2.36 (0.33) Dietary fluoride supplement use Never used 33.8 (1.1) 2.64 (0.15) Ever used 37.6 (3.8) 3.30 (0.54)
SE, standard error of estimates; CI, confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. Caries experience; 1: Prevalence of dental caries; 2: Mean dmfs. a Multivariable regression model for Poisson distribution with robust variance estimation for the prevalence of dental caries, controlling for all variable and age and sex. PR, Prevalence Ratio. b Multivariable regression model for negative binomial distribution with robust variance estimation for mean dmfs score, adjusting for all other variables and age and sex.
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Dental caries and fluorosis experience in children Table 4. Prevalence and extent of dental caries in the permanent dentition (aged 8–12 years) Caries experience (unadjusted)
Multivariable models
% With caries (SE)
% With caries a PR (95%CI)
Mean DMFSb RR (95% CI)
0.84 (0.67–1.07) 0.81 (0.62–1.06) Ref
0.76 (0.62–0.94) 0.84 (0.66–1.07) Ref
1.44 (1.02–2.04) 1.22 (0.89–1.67) 0.84 (0.67–1.07) Ref
1.39 (1.07–1.81) 1.17 (0.92–1.49) 0.75 (0.58–1.01) Ref
1.34 (1.00–1.82) 1.08 (0.83–1.40) Ref
1.93 (1.44–2.58) 1.54 (1.19–1.99) Ref
1.09 (0.81–1.46) Ref
0.97 (0.71–1.33) Ref
Mean DMFS (SE)
Total 23.8 (0.9) 0.67 (0.04) Percentage of life exposure to F in water (birth to 3 years) 100% 22.6 (1.2) 0.59 (0.04) >0–99% 22.6 (2.0) 0.63 (0.09) 0% 28.0 (2.3) 0.91 (0.10) Household income ≤40 000 AUD 31.7 (2.2) 1.04 (0.10) >40–80 000 AUD 24.3 (1.6) 0.69 (0.06) >80–120 000 AUD 18.3 (1.6) 0.45 (0.05) >120 000 AUD 20.5 (2.1) 0.53 (0.08) Parental education Low 30.4 (2.0) 0.94 (0.09) Medium 21.9 (1.1) 0.64 (0.05) High 21.0 (2.1) 0.40 (0.05) Dietary fluoride supplements use Never used 23.8 (0.9) 0.66 (0.04) Ever used 24.1 (3.4) 0.79 (0.15)
SE, standard error of estimates; CI: confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. a Multivariable regression model for Poisson distribution with robust variance estimation for the prevalence of dental caries, controlling for all variable and age and sex. PR, prevalence ratio. b Multivariable regression model for Negative Binomial distribution with robust variance estimation for mean DMFS score, adjusting for all other variables and age and sex.
associated with 0.76 times the count of DMFS score compared with having 0% exposure. The prevalence of dental caries was also lower but the difference was not statistically significant. Children whose parents had obtained only school education had significantly higher prevalence and count of dental caries experience than those whose parents had at least some tertiary education. Similarly, those children from household in the lowest income bracket had significantly higher prevalence and count of dental caries than those from the highest income households.
Discussion The NSW CDHS 2007 aimed to document the distribution of dental caries experience and fluorosis in the NSW child population. This has been achieved by a complex and sophisticated study design allowing for a representative sample of the state child population to be drawn. The estimates of the study were representative for the NSW child population in 2007. The survey has a large sample size further enabling more detailed analysis. Another significant strength of the study lies in the special training and calibration of examination teams. Further, the data items used in the question-
naire to collect fluoride exposure data have been extensively used in previous studies (5, 14). There are several issues with the investigation of the association between fluoride exposure and dental caries and fluorosis. Recall bias is an inherent limitation of retrospective research. The questionnaire was designed to minimize the issue. Collecting residential history in the preceding maximum of 12 years from parents of the children is considered simple and reliable. Hence, no systematic bias is expected in associations between fluoride exposures and dental diseases and conditions. Another issue lies in different timing of exposure. Fluorosis on maxillary central incisors is a developmental condition as a result of excess fluoride intake primarily during the first 3 years of life (12). Hence, mainly fluoride exposures during that age period can potentially have an effect on fluorosis experience of the permanent incisors. This NSW CDHS collected information on toothbrushing practice at the time of the study when children were already 8–12 years old. Therefore, patterns of toothbrushing practice could not be used in the analysis for this study. This study cannot provide evidence of risk for fluorosis attributable to the use of fluoridated toothpaste in this population. Fluoridated toothpaste use by young children has always been considered a major risk factor for fluorosis (5,
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22–24) in both children who used low concentration F toothpaste and the standard concentration F toothpaste. While caries experience was assessed when children were 8–12 years old, exposure to fluoride in water during the first 3 years of life was specifically used for this analysis. This age period is more critical in evaluating the balance in fluoride use as fluoride ingestion after the tooth development period does not cause dental fluorosis on most teeth in the permanent dentition. Fluoride exposure during the first 3 years of life may cause dental fluorosis on early erupting teeth while contributing to preventing dental caries in the primary dentition as well as permanent dentition. The study is the first to report on the prevalence and severity of dental fluorosis in a representative sample of the NSW child population. The prevalence of dental fluorosis in this population was similar to that reported in other Australian studies (14, 25). The vast majority of the observed fluorosis was very mild to mild (TF score 1 or 2). There was 2.4% of all children with a TF score of 3 (moderate) and further 0.3% with a TF score of 4. This level of fluorosis was found to not have any negative impact on children or their parents (7, 26). The children and their parents with very mild to mild dental fluorosis were more likely than those without dental fluorosis to report positive perception of dental appearance and oral health-related quality of life in a study conducted by us in South Australia (26). This finding can be partially explained by the phenomenon that trade-off was made, with some people accepting the occurrences of mild fluorosis in return for caries prevention. We also reported that children who had dental fluorosis had significantly lower dental caries experience (27). There has also been report of actual preferences for slight whiteness of tooth surface (28). A recent review concluded that very mild to mild dental fluorosis was not associated with negative impact on perception of oral health (29). The number of children with a TF score of 3 + , which can potentially have some negative aesthetic impact, was small (2.6% of the whole study sample). Therefore, a multivariable model was not useful with that more definitive case definition of fluorosis. The difference in the prevalence of any dental fluorosis (defined as having a TF score of 1 +) between children having 0% exposure and children who had exposure to fluoridated water during the first 3 years of life was roughly 10 percentage points (16.9% in those with 0% exposure versus
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26.2% in those with 100% exposure). This absolute difference was similar to the difference between areas with 0.9 ppm fluoride and areas with negligible fluoride in water reported by Dean in his classic studies when other forms of fluoride were not available (30). It should be noted that fluorosis at level of TF 1 is difficult to discern and may not be fully comparable to fluorosis at ‘very mild’ level in Dean’s studies. A review in the 1980s (31), comparing the earlier Dean’s studies with more recent North American studies after introduction of other forms of fluoride, reported that a stable absolute difference of 10% to 15% in the prevalence of dental fluorosis existed between fluoridated and nonfluoridated areas. This similarity between studies indicates that the recent increase in the prevalence of fluorosis is most likely attributable to other forms of fluoride. While the oral health of the child population in Australia has been improving since the 1970s, this study indicated that a significant proportion of the children still had decay experience on their primary or permanent dentition. Some 15% of the children had four or more primary tooth surfaces with dental caries experience, and some 5% of the children had 4+ permanent tooth surfaces with dental caries (data not shown). This level of dental caries experience is expected to have significant negative impact on the children and the dental health care system. Preventive measures are still needed to further reduce the prevalence and severity of dental caries in this population. The absolute levels and relationship between dental caries and fluorosis is a valuable in informing policy on acceptable levels of fluoride over time. With consideration of its strength and limitations, this study has provided high-level evidence of the risk-benefit trade-off of the use of fluoride from water in the NSW child population. There was a greater risk of mild fluorosis associated with higher per cent cumulative exposure to fluoridated water during the first 3 years of life. On the other hand, having such exposure was associated with a significantly lower prevalence and severity of dental caries in both permanent and primary dentitions. The significant effect of water fluoridation on the primary dentition has been widely reported. However, the effect on the permanent dentition of children has been reported as relatively small and inconsistent (32). This inconsistency is often attributed to relatively low level of caries extent in the permanent dentition. Despite that this study has provided strong evidence of the association of
Dental caries and fluorosis experience in children
water fluoridation and oral health in both dentitions. To conclude, this study has contributed evidence to assess the current preventive programmes using fluoride for young children. It has confirmed that water fluoridation is highly effective in preventing dental caries while poses certain level of risk for having dental fluorosis in young children. Dental caries continues to have negative impact on individuals and the health care system while dental fluorosis at the observed level is not associated with negative impact. Therefore, water fluoridation and use of fluoride toothpaste must remain the key population-based preventive programmes.
8.
9. 10.
11.
12.
Acknowledgements The examination data collection was funded by the Centre for Oral Health Strategy, NSW Health. Funding support from the Australian Dental Research Foundation and University of Adelaide School of Dentistry is also gratefully acknowledged. Loc Do is supported by NHMRC Career Development Fellowship # 1025045. Study participants and their families, the examination teams and support staff are gratefully acknowledged. Three anonymous reviewers are gratefully acknowledged for their constructive comments.
13. 14. 15.
16.
17.
References 1. CDC. Recommendations for using fluoride to prevent and control dental caries in the United States. Atlanta: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2001. 2. NHMRC. A systematic review of the efficacy and safety of fluoridation. Canberra: National Health and Medical Research Council; 2007. 3. Burt BA, Eklund SA. Dentistry, dental practice and the community, 5th edn. Philadelphia: WB Saunders; 1999. 4. Levy SM. An update on fluorides and fluorosis. J Can Dent Assoc 2003;69:286–91. 5. Do LG, Spencer AJ. Risk-benefit balance in the use of fluoride among young children. J Dent Res 2007; 86:723–8. 6. Kumar JV, Swango PA, Lininger LL, Leske GS, Green EL, Haley VB. Changes in dental fluorosis and dental caries in Newburgh and Kingston, New York. Am J Public Health 1998;88:1866–70. 7. Warren JJ, Levy SM, Broffitt B, Cavanaugh JE, Kanellis MJ, Weber-Gasparoni K. Considerations on optimal fluoride intake using dental fluorosis and
18.
19.
20.
21.
22. 23.
dental caries outcomes–a longitudinal study. J Public Health Dent 2009;69:111–5. Albert JM, Wang W, Nelson S. Estimating overall exposure effects for zero-inflated regression models with application to dental caries. Stat Methods Med Res 2011. doi: 10.1177/0962280211407800. ABS. Socio-economic Indexes For Areas (SEIFA). Canberra: Australian Bureau for Statistics; 2006. Ismail AI, Sohn W, Tellez M et al. The International Caries Detection and Assessment System (ICDAS): an integrated system for measuring dental caries. Community Dent Oral Epidemiol 2007;35:170–8. NIDCR. National Health and Nutrition Examination Survey dental examiners procedures manual. US Department of Health and Human Services CfDCaP, National Center for Health Statistics., Editor. 2002, Viewed 14 February 2007, available at: http://www. cdc.gov/nchs/data/nhanes/nhanes_03_04/DentalExaminers-2004.pdf. Hyattsville, MD. Fejerskov O, Manji F, Baelum V. Dental fluorosis: a handbook for health workers. Copenhagen: Munksgaard. 123; 1988. Russell AL. The differential diagnosis of fluoride and nonfluoride enamel opacities. J Public Health Dent 1961;21:143–6. Do LG, Spencer AJ. Decline in the prevalence of dental fluorosis among South Australian children. Community Dent Oral Epidemiol 2007;35:282–91. Slade GD, Spencer AJ, Davies MJ, Stewart JF. Influence of exposure to fluoridated water on socioeconomic inequalities in children’s caries experience. Community Dent Oral Epidemiol 1995;24:89– 100. Hong L, Levy SM, Broffitt B et al. Timing of fluoride intake in relation to development of fluorosis on maxillary central incisors. Community Dent Oral Epidemiol 2006;34:299–309. Barros AJ, Hirakata VN. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003;3:21. Greenland S. Model-based estimation of relative risks and other epidemiologic measures in studies of common outcomes and in case-control studies. Am J Epidemiol 2004;160:301–5. Wei R, Parsons V (2009) Model-based methods in analyzing complex survey data: a case study with National Health Interview Survey Data. Hyattsville, MD: Section on Survey Research Methods–JSM, NCHS, CDC; 2009. Lu HX, Wong MC, Lo EC, McGrath C. Risk indicators of oral health status among young adults aged 18 years analyzed by negative binomial regression. BMC Oral Health 2013;13:40. Preisser JS, Stamm JW, Long DL, Kincade ME. Review and recommendations for zero-inflated count regression modeling of dental caries indices in epidemiological studies. Caries Res 2012;46:413–23. Mascarenhas AK, Burt BA. Fluorosis risk from early exposure to fluoride toothpaste. Community Dent Oral Epidemiol 1998;26:241–8. Pendrys DG, Katz RV, Morse DE. Risk factors for enamel fluorosis in a fluoridated population. Am J Epidemiol 1994;140:461–71.
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Do et al. 24. Pendrys DG, Katz RV, Morse DE. Risk factors for enamel fluorosis in a nonfluoridated population. Am J Epidemiol 1996;143:808–15. 25. Riordan PJ. Dental fluorosis decline after changes to supplement and toothpaste regimens. Community Dent Oral Epidemiol 2002;30:233–40. 26. Do LG, Spencer A. Oral health-related quality of life of children by dental caries and fluorosis experience. J Public Health Dent 2007;67:132–9. 27. Do LG, Spencer AJ, Ha DH. Association between dental caries and fluorosis among South Australian children. Caries Res 2009;43:366–73. 28. McGrady MG, Ellwood RP, Goodwin M, Boothman N, Pretty IA. Adolescents’ perceptions of the aesthetic impact of dental fluorosis vs. other dental conditions in areas with and without water fluoridation. BMC Oral Health 2012;12:4.
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29. Chankanka O, Levy SM, Warren JJ, Chalmers JM. A literature review of aesthetic perceptions of dental fluorosis and relationships with psychosocial aspects/oral health-related quality of life. Community Dent Oral Epidemiol 2010;38:97–109. 30. Dean HT. The investigation of physiological effects by the epidemiological method. In: Moulton F, editors. Fluorine and dental health. Washington, DC: American Association for the Advancement of Science, 1942; p. 23. 31. Rozier RG. The prevalence and severity of enamel fluorosis in North American children. J Public Health Dent 1999;59:239–46. 32. McDonagh MS, Whiting PF, Wilson PM et al. Systematic review of water fluoridation. BMJ 2000;321: 855–9.
Ó 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental caries and fluorosis experience of 8–12-year-old children by early-life exposure to fluoride
Loc G. Do1, Jenifer Miller1, Claire Phelan2, Shanti Sivaneswaran2, A. John Spencer1 and Clive Wright2 1 Australian Research Centre for Population Oral Health, The University of Adelaide, Adelaide, SA, Australia, 2The Centre for Oral Health Strategy, Sydney, NSW, Australia
Do LG, Miller J, Phelan C, Sivaneswaran S, Spencer AJ, Wright C. Dental caries and fluorosis experience of 8–12-year-old children by early life exposure to fluoride. Community Dent Oral Epidemiol 2014; 42: 553–562. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Abstract – Background: It is important to evaluate concurrently the benefit for dental caries and the risk for dental fluorosis from early exposure to fluoride among children. Aim: To evaluate associations of different levels of exposure to fluoride in early childhood with dental caries and dental fluorosis experience in school children. Methods: A Child Dental Health Survey (CDHS) was conducted among school children in the Australian state of New South Wales (NSW) in 2007. Trained and calibrated examination teams conducted oral epidemiologic examinations to assess caries experience as decayed, missing or filled tooth surfaces of the primary and permanent dentitions (dmfs/DMFS) and fluorosis using the Thylstrup & Fejerskov (TF) index on the maxillary central incisors only. A parental questionnaire collected information on residential histories and tap water usage to enable calculation of percentage of 3-year lifetime exposure to fluoride in water. Use of dietary fluoride supplements was also collected. Dental caries and fluorosis experience were compared among groups by levels of exposure to fluoride from water and fluoride supplements in bivariate and multivariable analysis, controlling for socioeconomic factors. Results: Exposure to different fluoride sources varied in the group of 2611 children aged 8–12 years. Lower household income was significantly associated in both bivariate and multivariable analyses with the greater prevalence and severity of primary tooth caries among 8–10-year-old children and permanent tooth caries among 8–12 year old. Exposure to fluoride in water during the first 3 years of life was associated with both caries and fluorosis experience observed at age 8–12 years. Having higher percentage of 3-year lifetime exposure to fluoride in water was associated with higher prevalence of mostly mild fluorosis, but significantly lower prevalence and severity of caries in the primary and permanent dentitions. Conclusion: There were significant associations of dental caries and fluorosis experience with sources of early childhood fluoride exposure among children aged 8–12 years in New South Wales. Exposure to fluoridated water during the first 3 years of life was associated with better oral health of school-age children.
Fluoride use has been considered as one of the main contributing factors in improving the oral health status of child populations in many western doi: 10.1111/cdoe.12106
Key words: children; dental caries; dental fluorosis; fluoride Loc G. Do, ARCPOH, School of Dentistry, The University of Adelaide, Adelaide, SA 5005, Australia. Tel.: +61 8 8313 3964 Fax: +61 8 8313 3070 e-mail: [email protected] Submitted 30 December 2012; accepted 12 March 2014
countries (1, 2). Two main vehicles of fluoride delivery are water fluoridation and use of fluoridated toothpaste for toothbrushing. Water fluoridation
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is an effective and equitable programme that affords passive exposure to a low concentration of fluoride, while toothpaste use requires more active user participation. While exposure to fluoride in either water or toothpaste during early childhood is necessary to protect teeth, that exposure is associated with a certain level of risk of dental fluorosis, a developmental condition of tooth enamel (3, 4). Intake of fluoride during the first 3 years of life can increase the risk of having dental fluorosis on permanent incisors, the most aesthetically important teeth. The risk period for all permanent teeth, except third molars, can be up to 8 years of age. The best use of fluorides involves a balance between protection against dental caries and risk of dental fluorosis. The risks of having dental caries and fluorosis in a population can change over time, depending on the patterns of use of different fluoride sources. There is always a need to monitor the balance between risk and benefit of all early exposures to fluoride. Contemporary and relevant data would assist in the promotion, maintenance and regulation of water fluoridation, as well as guidance on the use of other forms of fluoride. There have been previous attempts to evaluate the trade-off of risk and benefit with early fluoride use (5–7). The recent large-scale population-based study of child oral health in the largest Australian state of New South Wales (NSW) (8) has provided an opportunity to further contribute to the scientific evidence on this issue. This study aimed to evaluate associations of different levels of exposure to fluoride in early childhood with dental caries and fluorosis experience in NSW school children. We hypothesized that early childhood exposure to fluoride was associated with both dental fluorosis and caries among school-aged children.
Methods Study design and sample selection Data for this analysis were collected in a cross-sectional population-based study. The NSW Child Dental Health Survey 2007 (NSW CDHS) covered a population representative sample of children aged 5–12 years from NSW (8). A two-stage sampling design was employed, with schools defined as the primary sampling units. Schools were stratified by NSW health service regions and a sample of schools was randomly selected from each region to
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ensure adequate regional representation. The school selection was conducted with probability of selection proportional to size. The Australian Research Centre for Population Oral Health (ARCPOH) at the University of Adelaide developed the study design, sampling strategy and examination manual and assisted in examiner training, calibration and data capture. Prior to selection, schools within each region were sorted by the Index of Relative Socio-Economic Disadvantage, which is one of the Australian Bureau for Statistics (ABS) Socio-Economic Indexes for Areas (SEIFA) (9), to ensure a spread of schools from regions with various socioeconomic backgrounds. A stratified random sample of children enrolled at each of these schools was selected based on age and sex distribution. Selected children’s families were sent an invitation package with a parental consent form. Children whose consent for participation was received were examined at schools by specially trained and calibrated examination teams comprised of an examiner and a data recorder. Ethical clearance was given by the University of Adelaide Human Research Ethics Committee, the NSW Population and Health Services Research Committee and the NSW Department of Education and Training.
Examination for oral health outcomes Twenty teams of calibrated dental examiners and recorders collected the oral health outcome data during the 2007 calendar year. Standard equipment, including portable air syringe compressors, lighting and blunt periodontal probes, were used. An examination protocol was developed based on the standard oral epidemiological indices for assessment of caries experience (10, 11) and dental fluorosis (12). The oral assessment was conducted primarily with visual criteria under two sources of light: an external portable dental light and an intraoral light. The blunted periodontal probe was mostly used to clean debris and to ‘feel’ surface roughness when distinguishing tooth colour restoration from enamel. Examiners were instructed to clean teeth with gauze and continually dry teeth with compressed air to ensure good vision. No X-ray was used. A dentist, acting as a principal survey examiner, jointly conducted the training and calibration of examination teams and also completed interexaminer reliability sessions with the field examiners on a subsample of children. A principal trainer, LGD,
Dental caries and fluorosis experience in children
also accompanied the principal examiner during the first two of her repeated examination sessions with each of the field examiners. The reliability of each of the examiners relative to the principal survey examiner was determined by calculating the intraclass correlation coefficient (ICC) of count data for each replicate pair and the Kappa values for categorical coding of individual tooth and surface status. Interexaminer reliability of examinations at tooth level for dental caries and individual level for dental fluorosis was reported elsewhere (8), with kappa scores ranging from 0.83 to 0.99.
Main oral health outcomes Two oral health outcome variables were used in this study, which represent two sides of the balance of exposure to fluoride in early childhood: dental caries and dental fluorosis. The history of dental caries in an individual was recorded at the tooth surface level. Dental caries was recorded when carious cavitation including enamel cavitation and/or dentinal involvement was observed. Noncavitated carious lesions were also recorded but not used in this analysis. Primary reasons for restorations were identified to distinguish fillings because of dental caries versus fillings for any other reasons. Causes of missing teeth were also distinguished between dental caries and other reasons. The average number of decayed, missing or filled tooth surfaces (dmfs/DMFS) is an expression of the extent of the disease in the population. The prevalence of dental caries experience on either primary or permanent dentition was estimated. Presence of dental fluorosis was assessed only on the two maxillary central incisors. Although the prevalence of dental fluorosis would be higher if other posterior teeth were assessed for dental fluorosis, the central incisors were used because they are most aesthetically important. If a tooth had a tooth-coloured filling or less than half of its crown erupted, or the child had fixed orthodontic band, the tooth was excluded from fluorosis examination. Fluorosis was differentiated from nonfluorotic opacities using the Russell differential diagnostic criteria (13). Severity of fluorosis was evaluated after air dry using a modified Thylsrup and Fejerskov (T-F) Index (12). The modified index has all scores from 0 to 4 identical to the original TF index. The TF scores 5 to 9 are collapsed to a single score 5 because very few children in the population were expected to have severe fluorosis that results in loss of enamel, based on fluorosis observed in another similar Australian population (14). For this
analysis, a case of fluorosis was defined as having a TF score of 2 + on one or both the maxillary central incisors.
Data collection covariates
of
main
exposure
and
Parents of the children who underwent examination were sent a written questionnaire to collect basic demographic, socioeconomic, dental behaviour and fluoride data, history of residential movement, Indigenous status, household income, parental education, and use of other forms of fluoride. The questionnaire had a 76% response rate. These questionnaire data allowed for evaluation of two forms of fluoride exposure in early childhood: exposure to fluoride in water during the first 3 years of life and use of dietary fluoride supplements. The main exposure variable was the measurement of exposure to fluoride in water which was converted to percentage of lifetime exposure to fluoridated water during the first 3 years of life. The calculation was based on a method described elsewhere (5, 14, 15). Briefly, the questionnaire asked parents to list all locations where the child had lived and the time period for each location. Those locations were linked with a database of fluoride levels in Australian public water supplies. Other nonpublic waters were assumed to have negligible fluoride levels. Parents were also asked to estimate the child’s proportion of public water usage as part of all drinking water consumption for each period of residency listed. The categories of this estimate were ‘Almost none’; ‘About half’; and ‘Almost all’. The responses to this question were used to adjust the 3-year lifetime exposure to fluoride in water using three values: 0 was used if the response was ‘Almost none’; 0.5 was used for ‘About half’ response; and 1 was used if the parent responded that ‘Almost all’ fluid consumption of the child was from public water supply. The formula used in the calculation of percentage of 3-year lifetime exposure E was as below. E ¼ R(time(in months) at a residency during age periodiÞ fluoride level in public water percentage of public water usage age (in months) 100: The present paper used the life period from birth to age 3 years (total age included in the above for-
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mula equal to 36 months). The estimate of 3-year lifetime exposure was used to classify children into three groups: having 0% lifetime exposure, having >0 & ≤99% lifetime exposure, and having 100% lifetime exposure. The period from birth to age 3 years was used because it is the peak risk period for fluorosis on the permanent upper central incisors (1, 12, 16). Parents of the children were asked to indicate if the child used dietary fluoride supplements (in the form of fluoride tablet or drop) and number of times it was used per day. Because of the low number of children who reportedly used fluoride supplements, the responses were used to dichotomize children into never-used or ever-used groups. The covariates in the analysis were age at examination, sex, and two indicators of socioeconomic status: household income and highest educational attainment of each parent. Household income in Australian dollars was collected as income ranges. Highest level of educational attainment of parents was used to group children into three groups. Low education was assigned to children whose parents had only secondary school education or lower, medium was assigned if at least one parent had both school and vocational (trade, apprenticeship) training, and high was assigned when at least one parent had any university education or higher.
Data preparation and analysis For the analysis in this report, only children aged 8–12 years were included because not all younger children had their maxillary central incisors erupted sufficiently for fluorosis examination. Data analysis was performed in SAS for Windows version 9.3 (SAS Institute Inc., Cary, NC, USA) and SUDAAN for Windows version 10.0 (RTI International, Research Triangle Park, NC, USA). The sample was re-weighted to adjust for different sampling ratios and response rates to produce estimates representative of the NSW child population. A total sample of 2611 children (76% of children aged 8–12 years) who had both clinical and complete questionnaire data was included in the analysis. Percentages and mean scores were weighted estimates. The analysis was conducted progressively from bivariate to multivariable analysis. Analysis was conducted separately for the experience of dental caries and fluorosis. The prevalence of caries and fluorosis was compared among the groups by different levels of fluoride exposures and socioeconomic variables. Adjusted prevalence ratios (PR)
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for both caries and fluorosis between the exposure groups and the respective reference groups were calculated using Poisson regression models with robust variance estimation (SUDAAN Procedure LOGLINK) to adjust for complex sampling procedures (17, 18). This procedure is a standard method for estimating prevalence ratios for data collected with stratified, multistaged sampling procedures. The associations between the prevalence of dental caries and fluorosis and different levels of fluoride exposures in early childhood were evaluated, with adjustment for other factors. Two-way interactions between different factors were tested. However, none of the interactions were statistically significant and were not included in the final models. The mean decayed, missing or filled tooth surfaces (dmfs) scores were calculated as a measure of caries experience in the primary dentition for children aged 8–10 years while the similar measure of caries in the permanent dentition (DMFS) was calculated for all 8–12-year-old children. Adjusted rate ratios (RR) were calculated for mean dmfs/ DMFS between the exposure groups and the respective reference groups using multivariable regression models. Negative binomial distribution was specified in the models using SAS procedure GLIMMIX to address the complex sample design of the data (19). It is well known that dmf/DMF indices are count variables with over-dispersion that justifies the use of negative binomial distribution in the models (8, 20, 21). Zero-inflated models can also be suitable (21). However, fitting a zeroinflated model for data with complex sample design is computationally complex. Negative binomial regression for count of dental caries teeth or surfaces is closely comparable to zero-inflated regression model (20). The associations between caries with the available fluoride exposures were evaluated. Two-way interactions between factors were also tested but not included in the final models because of lack of statistical significance. In tables, where indicated, numbers of children are un-weighted, while percentages and mean values are weighted. Therefore, multiplying the estimates by the number of subjects may not yield integers of individuals.
Results A total of 2611 children aged 8–12 years were included in the analysis (Table 1). The distribution by age and sex reflected population benchmarks.
Dental caries and fluorosis experience in children Table 1. Study sample sociodemographic characteristics and exposure to fluoride in early childhood N (total 2611)
W%
95% CI
Age at examination 8 years 473 20.2 18.9–21.5 9 years 450 20.5 19.2–21.8 10 years 483 20.1 19.0–21.2 11 years 716 19.7 18.8–20.7 12 years 489 19.5 17.9–21.2 Sex Male 1319 51.2 48.3–54.1 Female 1292 48.8 45.9–51.7 Percentage of life exposure to F in water (birth to 3 years) 100% lifetime 1498 64.0 60.3–67.8 >0–99% lifetime 557 21.3 19.0–23.7 0% lifetime 386 14.6 11.4–17.9 Household income ≤40 000 AUD 548 22.2 19.0–25.4 >40–80 000 AUD 810 32.7 29.9–35.5 >80–120 000 AUD 642 25.7 23.0–28.4 >120 000 AUD 437 19.4 15.6–23.2 Parental education Low 624 24.1 20.9–27.3 Medium 1490 57.4 54.7–60.2 High 472 18.5 15.6–21.4 Dietary fluoride supplement use Never used 2419 94.2 92.7–95.6 Ever used 186 5.8 4.4–7.3 W%, weighted per cent; 95% CI, 95% Confidence Intervals. Data were weighted to represent population estimates. Some variables have missing data.
More than 60% of the children had almost all of their first 3 years of life exposed to fluoride from water, while just fewer than 15% had almost no exposure to fluoridated water during that age period. Some 21% of the children had some but less than 100% of their first 3 years of life exposed to fluoride in water. Just over a fifth of the sample was in the lowest income category while slightly less than a fifth was in the highest (over AU$120 000/year) category. The large majority of the children had never used dietary fluoride supplements. Approximately 25% of the sample had some level of dental fluorosis on maxillary central incisors. About 10% had at least one maxillary central incisor with fluorosis at TF score of 2 or higher. Most of the children (22% from those 24.6%) who had fluorosis on their maxillary central incisors had very mild or mild fluorosis (TF scores of 1 or 2) (Table 2). Some 2.6% of the total sample had a TF score of 3 or 4, while there were no cases of more severe fluorosis (data not shown). The prevalence of fluorosis was lowest among those who had 0% lifetime exposure to fluoride in water. The two groups with at least some exposure to fluoride in water had similar prevalence of fluorosis on their maxillary central incisors. There was some variation in the prevalence of dental fluorosis by household income and parental education.
Table 2. Distribution of maxillary central incisor fluorosis scores by sample characteristics–bivariate analysis Fluorosis experience (unadjusted) Total
TF 1 row% (SE)
Total 24.6 14.7 (0.8) Percentage of life exposure to F in water (birth to 3 years) 100% 26.2 15.0 (1.0) >0–99% 28.0 18.8 (2.0) 0% 16.9 10.2 (1.5) Household income ≤40 000 AUD 20.1 11.6 (1.5) >40–80 000 AUD 22.5 13.5 (1.3) >80–120 000 AUD 27.8 16.7 (1.6) >120 000 AUD 28.1 17.9 (2.1) Parental education Low 23.4 12.8 (1.5) Medium 24.8 15.2 (1.0) High 25.1 15.4 (1.9) Dietary fluoride supplement use Never used 24.8 14.7 (1.1) Ever used 19.6 14.7 (2.8)
TF 2 + row% (SE)
Multivariable modela Prevalence of TF 2 + PR (95% CI)
9.9 (0.7) 11.2 (0.9) 9.2 (1.5) 6.7 (1.4)
1.86 (1.14–3.05) 1.33 (0.71–2.50) Ref
8.5 (1.3) 9.0 (1.1) 11.1 (1.4) 10.2 (1.7)
0.78 (0.46–1.34) 0.89 (0.52–1.51) 0.97 (0.64–1.46) Ref
10.6 (1.4) 9.6 (0.9) 9.7 (1.6)
1.30 (0.72–2.32) 1.02 (0.63–1.63) Ref
10.1 (0.7) 4.9 (1.87)
1.46 (0.91–2.34) Ref
SE, standard error of the percentage; PR, prevalence ratios, estimated using multivariable regression models for Poisson distribution with robust variance estimation; CI, Confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. a Multivariable model for the prevalence of cases with TF score 2+ on maxillary central incisors, all variables, age and sex were included in the models.
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The multivariable model for the prevalence of dental fluorosis defined as having a TF score of 2 + confirmed the association between exposure to fluoride in water in the first 3 years of life and the prevalence of dental fluorosis. Children who had 100% of the period from birth to age 3 years exposed to fluoridated water had 1.86 times the prevalence of dental fluorosis compared to those who did not have any exposure. Those who had partial water fluoride exposure had higher prevalence of dental fluorosis compared with the reference group but the difference was not statistically significant. The associations between dental fluorosis and the socioeconomic variables were not statistically significant in the model. Over 34% of the children aged 8–10 years had a history of caries experience in their primary dentition, with an average of 2.69 surfaces per child (Table 3). It was clear that children who had exposure to fluoridated water during most of their first 3 years of life were less likely to have caries on their primary dentition. The intensity of caries experience measured by mean dmfs scores was also significantly lower in children who had exposure to fluoride in water. Children whose parents had only school education attainment had higher prevalence and extent of dental caries than those
whose parents had at least some university education. The association between exposure to fluoridated water and dental caries in the primary dentition was confirmed in the multivariable models for both the prevalence and extent of dental caries (Table 3). Having 100% of the first 3 years of life exposed to fluoridated water was significantly associated with 0.83 times the prevalence of dental caries and 0.65 times the count of dmfs score compared with having 0% exposure. Having some but less than 100% water fluoride exposure was also associated with significantly lower primary teeth caries experience. Children whose parents had low level of education had statistically significantly higher count of dmfs score than those with parents with high education. About a quarter of the children aged 8–12 years had experience of dental caries in the permanent dentition with the mean DMFS of 0.67 affected surfaces (Table 4). Similar to that observed in the primary teeth dentition, exposure to fluoridated water in the first 3 years of life was associated with significantly lower dental caries experience in the permanent dentition. After adjusting for other factors in the model, having 100% exposure to fluoridated water in the first 3 years of life was
Table 3. Prevalence and extent of dental caries in the primary dentition (aged 8–10 years) Caries experience (unadjusted)
Multivariable models
% (SE)1
% With caries a PR (95%CI)
Mean dmfsb RR (95% CI)
0.83 (0.70–0.99) 0.81 (0.65–1.01) Ref
0.65 (0.54–0.78) 0.66 (0.53–0.82) Ref
1.13 (0.91–1.40) 1.08 (0.88–1.33) 0.98 (0.78–1.23) Ref
1.24 (0.98–1.58) 1.21 (0.98–1.50) 0.95 (0.77–1.19) Ref
1.14 (0.90–1.40) 1.07 (0.85–1.34) Ref
1.35 (1.07–1.71) 1.04 (0.85–1.27) Ref
0.90 (0.65–1.25) Ref
0.86 (0.65–1.15) Ref
dmfs (SE)2
Total 34.1 (1.0) 2.69 (0.14) Percentage of life exposure to F in water (birth to 3 years) 100% 32.6 (1.4) 2.38 (0.18) >0–99% 31.5 (2.3) 2.30 (0.31) 0% 39.0 (2.6) 3.82 (0.43) Household income ≤40 000 AUD 39.4 (2.3) 3.70 (0.37) >40–80 000 AUD 35.3 (1.9) 2.97 (0.28) >80–120 000 AUD 30.7 (2.0) 2.12 (0.25) >120 000 AUD 30.3 (2.4) 1.95 (0.29) Parental education Low 37.9 (2.1) 3.63 (0.36) Medium 33.5 (1.4) 2.40 (0.17) High 30.7 (2.3) 2.36 (0.33) Dietary fluoride supplement use Never used 33.8 (1.1) 2.64 (0.15) Ever used 37.6 (3.8) 3.30 (0.54)
SE, standard error of estimates; CI, confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. Caries experience; 1: Prevalence of dental caries; 2: Mean dmfs. a Multivariable regression model for Poisson distribution with robust variance estimation for the prevalence of dental caries, controlling for all variable and age and sex. PR, Prevalence Ratio. b Multivariable regression model for negative binomial distribution with robust variance estimation for mean dmfs score, adjusting for all other variables and age and sex.
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Dental caries and fluorosis experience in children Table 4. Prevalence and extent of dental caries in the permanent dentition (aged 8–12 years) Caries experience (unadjusted)
Multivariable models
% With caries (SE)
% With caries a PR (95%CI)
Mean DMFSb RR (95% CI)
0.84 (0.67–1.07) 0.81 (0.62–1.06) Ref
0.76 (0.62–0.94) 0.84 (0.66–1.07) Ref
1.44 (1.02–2.04) 1.22 (0.89–1.67) 0.84 (0.67–1.07) Ref
1.39 (1.07–1.81) 1.17 (0.92–1.49) 0.75 (0.58–1.01) Ref
1.34 (1.00–1.82) 1.08 (0.83–1.40) Ref
1.93 (1.44–2.58) 1.54 (1.19–1.99) Ref
1.09 (0.81–1.46) Ref
0.97 (0.71–1.33) Ref
Mean DMFS (SE)
Total 23.8 (0.9) 0.67 (0.04) Percentage of life exposure to F in water (birth to 3 years) 100% 22.6 (1.2) 0.59 (0.04) >0–99% 22.6 (2.0) 0.63 (0.09) 0% 28.0 (2.3) 0.91 (0.10) Household income ≤40 000 AUD 31.7 (2.2) 1.04 (0.10) >40–80 000 AUD 24.3 (1.6) 0.69 (0.06) >80–120 000 AUD 18.3 (1.6) 0.45 (0.05) >120 000 AUD 20.5 (2.1) 0.53 (0.08) Parental education Low 30.4 (2.0) 0.94 (0.09) Medium 21.9 (1.1) 0.64 (0.05) High 21.0 (2.1) 0.40 (0.05) Dietary fluoride supplements use Never used 23.8 (0.9) 0.66 (0.04) Ever used 24.1 (3.4) 0.79 (0.15)
SE, standard error of estimates; CI: confidence intervals. Estimates are statistically significant if their CIs do not include 1.0. a Multivariable regression model for Poisson distribution with robust variance estimation for the prevalence of dental caries, controlling for all variable and age and sex. PR, prevalence ratio. b Multivariable regression model for Negative Binomial distribution with robust variance estimation for mean DMFS score, adjusting for all other variables and age and sex.
associated with 0.76 times the count of DMFS score compared with having 0% exposure. The prevalence of dental caries was also lower but the difference was not statistically significant. Children whose parents had obtained only school education had significantly higher prevalence and count of dental caries experience than those whose parents had at least some tertiary education. Similarly, those children from household in the lowest income bracket had significantly higher prevalence and count of dental caries than those from the highest income households.
Discussion The NSW CDHS 2007 aimed to document the distribution of dental caries experience and fluorosis in the NSW child population. This has been achieved by a complex and sophisticated study design allowing for a representative sample of the state child population to be drawn. The estimates of the study were representative for the NSW child population in 2007. The survey has a large sample size further enabling more detailed analysis. Another significant strength of the study lies in the special training and calibration of examination teams. Further, the data items used in the question-
naire to collect fluoride exposure data have been extensively used in previous studies (5, 14). There are several issues with the investigation of the association between fluoride exposure and dental caries and fluorosis. Recall bias is an inherent limitation of retrospective research. The questionnaire was designed to minimize the issue. Collecting residential history in the preceding maximum of 12 years from parents of the children is considered simple and reliable. Hence, no systematic bias is expected in associations between fluoride exposures and dental diseases and conditions. Another issue lies in different timing of exposure. Fluorosis on maxillary central incisors is a developmental condition as a result of excess fluoride intake primarily during the first 3 years of life (12). Hence, mainly fluoride exposures during that age period can potentially have an effect on fluorosis experience of the permanent incisors. This NSW CDHS collected information on toothbrushing practice at the time of the study when children were already 8–12 years old. Therefore, patterns of toothbrushing practice could not be used in the analysis for this study. This study cannot provide evidence of risk for fluorosis attributable to the use of fluoridated toothpaste in this population. Fluoridated toothpaste use by young children has always been considered a major risk factor for fluorosis (5,
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22–24) in both children who used low concentration F toothpaste and the standard concentration F toothpaste. While caries experience was assessed when children were 8–12 years old, exposure to fluoride in water during the first 3 years of life was specifically used for this analysis. This age period is more critical in evaluating the balance in fluoride use as fluoride ingestion after the tooth development period does not cause dental fluorosis on most teeth in the permanent dentition. Fluoride exposure during the first 3 years of life may cause dental fluorosis on early erupting teeth while contributing to preventing dental caries in the primary dentition as well as permanent dentition. The study is the first to report on the prevalence and severity of dental fluorosis in a representative sample of the NSW child population. The prevalence of dental fluorosis in this population was similar to that reported in other Australian studies (14, 25). The vast majority of the observed fluorosis was very mild to mild (TF score 1 or 2). There was 2.4% of all children with a TF score of 3 (moderate) and further 0.3% with a TF score of 4. This level of fluorosis was found to not have any negative impact on children or their parents (7, 26). The children and their parents with very mild to mild dental fluorosis were more likely than those without dental fluorosis to report positive perception of dental appearance and oral health-related quality of life in a study conducted by us in South Australia (26). This finding can be partially explained by the phenomenon that trade-off was made, with some people accepting the occurrences of mild fluorosis in return for caries prevention. We also reported that children who had dental fluorosis had significantly lower dental caries experience (27). There has also been report of actual preferences for slight whiteness of tooth surface (28). A recent review concluded that very mild to mild dental fluorosis was not associated with negative impact on perception of oral health (29). The number of children with a TF score of 3 + , which can potentially have some negative aesthetic impact, was small (2.6% of the whole study sample). Therefore, a multivariable model was not useful with that more definitive case definition of fluorosis. The difference in the prevalence of any dental fluorosis (defined as having a TF score of 1 +) between children having 0% exposure and children who had exposure to fluoridated water during the first 3 years of life was roughly 10 percentage points (16.9% in those with 0% exposure versus
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26.2% in those with 100% exposure). This absolute difference was similar to the difference between areas with 0.9 ppm fluoride and areas with negligible fluoride in water reported by Dean in his classic studies when other forms of fluoride were not available (30). It should be noted that fluorosis at level of TF 1 is difficult to discern and may not be fully comparable to fluorosis at ‘very mild’ level in Dean’s studies. A review in the 1980s (31), comparing the earlier Dean’s studies with more recent North American studies after introduction of other forms of fluoride, reported that a stable absolute difference of 10% to 15% in the prevalence of dental fluorosis existed between fluoridated and nonfluoridated areas. This similarity between studies indicates that the recent increase in the prevalence of fluorosis is most likely attributable to other forms of fluoride. While the oral health of the child population in Australia has been improving since the 1970s, this study indicated that a significant proportion of the children still had decay experience on their primary or permanent dentition. Some 15% of the children had four or more primary tooth surfaces with dental caries experience, and some 5% of the children had 4+ permanent tooth surfaces with dental caries (data not shown). This level of dental caries experience is expected to have significant negative impact on the children and the dental health care system. Preventive measures are still needed to further reduce the prevalence and severity of dental caries in this population. The absolute levels and relationship between dental caries and fluorosis is a valuable in informing policy on acceptable levels of fluoride over time. With consideration of its strength and limitations, this study has provided high-level evidence of the risk-benefit trade-off of the use of fluoride from water in the NSW child population. There was a greater risk of mild fluorosis associated with higher per cent cumulative exposure to fluoridated water during the first 3 years of life. On the other hand, having such exposure was associated with a significantly lower prevalence and severity of dental caries in both permanent and primary dentitions. The significant effect of water fluoridation on the primary dentition has been widely reported. However, the effect on the permanent dentition of children has been reported as relatively small and inconsistent (32). This inconsistency is often attributed to relatively low level of caries extent in the permanent dentition. Despite that this study has provided strong evidence of the association of
Dental caries and fluorosis experience in children
water fluoridation and oral health in both dentitions. To conclude, this study has contributed evidence to assess the current preventive programmes using fluoride for young children. It has confirmed that water fluoridation is highly effective in preventing dental caries while poses certain level of risk for having dental fluorosis in young children. Dental caries continues to have negative impact on individuals and the health care system while dental fluorosis at the observed level is not associated with negative impact. Therefore, water fluoridation and use of fluoride toothpaste must remain the key population-based preventive programmes.
8.
9. 10.
11.
12.
Acknowledgements The examination data collection was funded by the Centre for Oral Health Strategy, NSW Health. Funding support from the Australian Dental Research Foundation and University of Adelaide School of Dentistry is also gratefully acknowledged. Loc Do is supported by NHMRC Career Development Fellowship # 1025045. Study participants and their families, the examination teams and support staff are gratefully acknowledged. Three anonymous reviewers are gratefully acknowledged for their constructive comments.
13. 14. 15.
16.
17.
References 1. CDC. Recommendations for using fluoride to prevent and control dental caries in the United States. Atlanta: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2001. 2. NHMRC. A systematic review of the efficacy and safety of fluoridation. Canberra: National Health and Medical Research Council; 2007. 3. Burt BA, Eklund SA. Dentistry, dental practice and the community, 5th edn. Philadelphia: WB Saunders; 1999. 4. Levy SM. An update on fluorides and fluorosis. J Can Dent Assoc 2003;69:286–91. 5. Do LG, Spencer AJ. Risk-benefit balance in the use of fluoride among young children. J Dent Res 2007; 86:723–8. 6. Kumar JV, Swango PA, Lininger LL, Leske GS, Green EL, Haley VB. Changes in dental fluorosis and dental caries in Newburgh and Kingston, New York. Am J Public Health 1998;88:1866–70. 7. Warren JJ, Levy SM, Broffitt B, Cavanaugh JE, Kanellis MJ, Weber-Gasparoni K. Considerations on optimal fluoride intake using dental fluorosis and
18.
19.
20.
21.
22. 23.
dental caries outcomes–a longitudinal study. J Public Health Dent 2009;69:111–5. Albert JM, Wang W, Nelson S. Estimating overall exposure effects for zero-inflated regression models with application to dental caries. Stat Methods Med Res 2011. doi: 10.1177/0962280211407800. ABS. Socio-economic Indexes For Areas (SEIFA). Canberra: Australian Bureau for Statistics; 2006. Ismail AI, Sohn W, Tellez M et al. The International Caries Detection and Assessment System (ICDAS): an integrated system for measuring dental caries. Community Dent Oral Epidemiol 2007;35:170–8. NIDCR. National Health and Nutrition Examination Survey dental examiners procedures manual. US Department of Health and Human Services CfDCaP, National Center for Health Statistics., Editor. 2002, Viewed 14 February 2007, available at: http://www. cdc.gov/nchs/data/nhanes/nhanes_03_04/DentalExaminers-2004.pdf. Hyattsville, MD. Fejerskov O, Manji F, Baelum V. Dental fluorosis: a handbook for health workers. Copenhagen: Munksgaard. 123; 1988. Russell AL. The differential diagnosis of fluoride and nonfluoride enamel opacities. J Public Health Dent 1961;21:143–6. Do LG, Spencer AJ. Decline in the prevalence of dental fluorosis among South Australian children. Community Dent Oral Epidemiol 2007;35:282–91. Slade GD, Spencer AJ, Davies MJ, Stewart JF. Influence of exposure to fluoridated water on socioeconomic inequalities in children’s caries experience. Community Dent Oral Epidemiol 1995;24:89– 100. Hong L, Levy SM, Broffitt B et al. Timing of fluoride intake in relation to development of fluorosis on maxillary central incisors. Community Dent Oral Epidemiol 2006;34:299–309. Barros AJ, Hirakata VN. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003;3:21. Greenland S. Model-based estimation of relative risks and other epidemiologic measures in studies of common outcomes and in case-control studies. Am J Epidemiol 2004;160:301–5. Wei R, Parsons V (2009) Model-based methods in analyzing complex survey data: a case study with National Health Interview Survey Data. Hyattsville, MD: Section on Survey Research Methods–JSM, NCHS, CDC; 2009. Lu HX, Wong MC, Lo EC, McGrath C. Risk indicators of oral health status among young adults aged 18 years analyzed by negative binomial regression. BMC Oral Health 2013;13:40. Preisser JS, Stamm JW, Long DL, Kincade ME. Review and recommendations for zero-inflated count regression modeling of dental caries indices in epidemiological studies. Caries Res 2012;46:413–23. Mascarenhas AK, Burt BA. Fluorosis risk from early exposure to fluoride toothpaste. Community Dent Oral Epidemiol 1998;26:241–8. Pendrys DG, Katz RV, Morse DE. Risk factors for enamel fluorosis in a fluoridated population. Am J Epidemiol 1994;140:461–71.
561
Do et al. 24. Pendrys DG, Katz RV, Morse DE. Risk factors for enamel fluorosis in a nonfluoridated population. Am J Epidemiol 1996;143:808–15. 25. Riordan PJ. Dental fluorosis decline after changes to supplement and toothpaste regimens. Community Dent Oral Epidemiol 2002;30:233–40. 26. Do LG, Spencer A. Oral health-related quality of life of children by dental caries and fluorosis experience. J Public Health Dent 2007;67:132–9. 27. Do LG, Spencer AJ, Ha DH. Association between dental caries and fluorosis among South Australian children. Caries Res 2009;43:366–73. 28. McGrady MG, Ellwood RP, Goodwin M, Boothman N, Pretty IA. Adolescents’ perceptions of the aesthetic impact of dental fluorosis vs. other dental conditions in areas with and without water fluoridation. BMC Oral Health 2012;12:4.
562
29. Chankanka O, Levy SM, Warren JJ, Chalmers JM. A literature review of aesthetic perceptions of dental fluorosis and relationships with psychosocial aspects/oral health-related quality of life. Community Dent Oral Epidemiol 2010;38:97–109. 30. Dean HT. The investigation of physiological effects by the epidemiological method. In: Moulton F, editors. Fluorine and dental health. Washington, DC: American Association for the Advancement of Science, 1942; p. 23. 31. Rozier RG. The prevalence and severity of enamel fluorosis in North American children. J Public Health Dent 1999;59:239–46. 32. McDonagh MS, Whiting PF, Wilson PM et al. Systematic review of water fluoridation. BMJ 2000;321: 855–9.
