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Are distinctive risk indicators associated with different stages of caries in children? A cross-sectional study

Are distinctive risk indicators associated with different stages of caries in children? A... Background: Actual caries figures emphasize the need to identify the risk indicators involved in the disease’s development. The hypothesis that certain risk indicators might affect the dynamic evolution of the caries process was assessed; to clarify this premise, a cross-sectional survey was performed in school children. Methods: A total of 390 subjects aged 6–8 years old were randomly selected. Caries was assessed, and the subjects were stratified as follows: i) highest caries score; ii) most prevalent caries score; and iii) number of affected teeth. Parents/guardians completed a questionnaire regarding vital statistics, socio-economic indicators, dietary habits, oral hygiene habits and oral health behaviours. Results: Caries was detected in 42.31% of the subjects. Maternal nationality, parental education level, use of a sweetened pacifier at night, intake of lactose-free milk and toothbrushing frequency were statistically significant associated (p < 0.05) with subjects stratified according to the highest caries score. Parental educational level, maternal occupational status and use of a sweetened pacifier at night were associated (p < 0.05) with affected children stratified according to the most prevalent caries score. Maternal educational level and intake of lactose-free milk were associated with subjects with moderate caries stages compared to being caries-free (p =0.01 and p = 0.02, respectively). Maternal nationality (p < 0.01) andtoothbrushingfrequency (p = 0.01) were associated with subjects affected by extensive lesions compared to caries-free children. In subjects affected by initial lesions as the most prevalent figure, gender (male) and paternal occupation status (unemployed) were statistically significant associated (p =0.03 and p = 0.04, respectively) compared to those affected by highest prevalence of extensive caries lesions. In children with the highest prevalence of moderate caries lesions, maternal education level (p < 0.01), paternal occupational status (p = 0.03) and use of a sweetened pacifier at night (p < 0.01) were statistically significantly associated. Conclusions: Maternal nationality, maternal low level of education, intake of lactose-free milk and low toothbrushing frequency were involved in the change from caries-free status to different caries stages. Gender, paternal unemployment, maternal low educational level and use of a sweetened pacifier were correlated with caries progression, showing how distinctive risk indicators were associated with different caries stages. Keywords: Dental caries, Children, Risk indicators, Caries staging, Feeding practice, Socio-economic status * Correspondence: [email protected] WHO Collaboration Centre for Epidemiology and Community Dentistry, Milan, Italy Department of Surgery, Microsurgery and Medicine Sciences, School of Dentistry, University of Sassari, Viale San Pietro 43/C, I-07100, Sassari, Italy Full list of author information is available at the end of the article © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cagetti et al. BMC Public Health (2016) 16:1213 Page 2 of 10 Background support decision-making at both the individual and Although, in recent decades in Western countries, a community levels [14]. The ICDAS provides options for decreasing caries trend has been observed, especially in coding 6 different stages of caries lesions (0 sound, 1 first childhood [1, 2], dental caries remains a major public visual change in enamel, 2 distinct visual change in ena- health issue with impacts on the quality of life of children mel, 3 localized enamel breakdown, 4 underlying dentin and adults [3]. Despite continuous improvements in den- shadow, 5 distinct cavity with visible dentin, and 6 exten- tal health, children remain a primary disparity group [4]. sive cavity with visible dentin) [14]. Health risk evaluation is the comprehensive assessment of As mentioned above, the premise of this study was to risk factors in the general population or specific groups, determine whether specific risk indicators might affect such as children, the elderly, subjects with immigrant different stages of the caries disease process. To investi- backgrounds and so on, based on environmental, genetic, gate this issue, a cross-sectional survey was designed economic, social and behavioural health determinants [5]. and performed. The caries decrease has resulted in a polarization of the distribution of the disease, and today, high caries figures Methods are observed only in a small proportion of the population Sample selection and study design [1, 4]. When the mean number of decayed, missing and The study protocol was approved by the Ethics Committee filled teeth improves, the number of caries-free individuals of the University of Sassari (registration no. SS0421/2012). increases, and polarization becomes more pronounced [6]. The study was conducted in accordance with the tenets of This skewed distribution emphasizes the need to identify the Declaration of Helsinki. According to data derived caries risk indicators that are involved in the development from the Italian Institute of Statistics [15] in 2013, the of the disease to plan targeted preventive programmes that number of subjects aged 6–8 years old living in the Sassari consider that health is linked to health promotion, particu- area was 3095. The study used a cross-sectional design, larly when care resources are limited [7]. and a formula for estimating population proportions with Caries can be defined as a dietary-bacterial disease [8], high precision was used to calculate the sample size. Data with the interactions between the host and different risk derived from the recent literature [16] described a preva- factors derived from social inequalities, such as a low lence of caries in the same age group of approximately socio-economic level, recent immigrant status, a low 35%. A power analysis was performed with G*Power soft- educational degree and unemployment status [9, 10]. ware, version 3.1.9.2 for Apple, using logistic regression, Considering the complex aetiology of the disease, a with the prevalence ratio added to 40% to safeguard against crucial issue is to identify its potential determinants and the risk of disease spread, an error probability of 0.05 and predictors to determine the appropriate public health actual power of 0.95. The total sample size was set to 246. measures to prevent it. Because caries lesions have a In February 2014, schoolchildren were recruited at their dynamic evolution requiring a long period of time, schools using systematic cluster sampling; every class was usually many months or years [11], it might be specu- identified as a cluster, and the class list was compiled. The lated that different risk indicators might be involved in first cluster was randomly selected, while the others were several stages of the dynamic process, playing different systematically chosen at intervals of three classes. The roles at different times. This study began with the number of subjects was approximately the same in each hypothesis that specific risk indicators might manifest class (n = 20 subjects). Considering the possibility of a low their effects in specific caries stages, leading to distinct response rate [17], 520 children were invited to participate patterns that could be identified and studied. For ex- through an information leaflet distributed to parents at the ample, subjects, especially children with initial lesions, school, explaining the aim of the study and requesting their should be considered at high risk for caries because children’s participation. Only children with their parents’ these lesions are indicative of caries activity [12]. signed consent were enrolled. Consent was obtained for Another difficult issue is the complexity of the disease 427 children. Parents were asked to complete a stan- state because the different manifestations of caries can- dardized questionnaire regarding different variables re- not be quantified by a single metric. The progression of lated to caries. Twenty-two subjects (5.15% dropouts) the lesion cannot be assessed with the most commonly returned an incomplete questionnaire and were excluded used caries index, the DMFT/S index (the sum of decayed, from the survey; moreover, 15 (3.51%) children were ab- missed, filled teeth/surfaces) because it does not distin- sent from school on the day of the examination. The guish among the different stages of caries lesions [13, 14]. survey reported data from 390 children (Fig. 1). The International Caries Detection Assessment System (ICDAS), which is based on the best available evidence for Data collection detecting the early and late stages of caries severity, should The data collection methods consisted of a questionnaire lead to the acquisition of better quality information to and a clinical oral examination. A structured standardized Cagetti et al. BMC Public Health (2016) 16:1213 Page 3 of 10 Fig. 1 Flow diagram of the recruitment of children questionnaire [18] was submitted to the parents/guardians Data analysis before the examination. The questionnaire was based on All of the data were input into a spreadsheet (Microsoft the following domains: 1 - vital statistics: gender, parental Excel® 2011 for Mac, version 14.4.3). Statistical analyses nationality, and eruption timing of primary teeth; 2 - were performed using Stata/SE® software, version 13.1 socio-economic indicators: parental educational level and for Mac (64-bit Intel®)(for raw data consultation please parental occupational status; 3 - dietary habits: breast- check Additional file 1). feeding, bottle-feeding, sweet bottle-feeding at night, Data from the clinical examinations were grouped as use of a sweetened pacifier at night, sweetened drinks follows: No caries (ICDAS 0), Initial stage (ICDAS 1–2), before sleeping and use of lactose-free milk as the main Moderate stage (ICDAS 3–4) and Extensive stage diary product; 4 - oral hygiene habits: fluoride amount (ICDAS 5–6). Regarding the number of affected teeth in in toothpaste, frequency of toothbrushing, and fluoride each subject, the following categories were defined: 1–2 supplement intake; and 5 - oral health behaviours: affected teeth, 3–5 affected teeth, and six or more frequency of dental check-ups for the parents and affected teeth. children. As the clinical chart was printed in the other Subjects were stratified according to the following side of the sheet of questionnaire, the questionnaire three different procedures: i) the maximum caries form was collected directly by the examiner before the stage – subjects were coded according to the highest examination. caries score (ICDAS) recorded; ii) the most prevalent Children were examined at their schools using a cali- caries stage – subjects were coded according to the brated examiner (GiC) from September to November of most prevalent caries score (ICDAS) recorded; and iii) 2014. An author (GC) acted as a benchmark, training the number of affected teeth – subjects were coded and calibrating the examiner (GiC). Fifty subjects, not according to the number of affected teeth recorded. included in the sample, were examined and re-examined Responses to questionnaire items were treated as cate- after 72 h. Intra-examiner reproducibility was evaluated gorical or ordinal variables. through percentage agreement and Cohen’s kappa statis- Associations between background variables and sub- tics. The percentage agreement was high at both the jects, stratified as reported above, were assessed using subject and tooth surface levels (Cohen’s kappa = 0.86 the chi-squared test; for values less than five, Fisher’s and 0.77, respectively). Clinical examinations were per- exact test was performed. formed under standardized conditions using a portable Multinomial logit models were performed following air-drier device, a plain mirror and a WHO Community the stratifying procedures to assess the associations with Periodontal Index probe. Dental caries was assessed background variables. The multinomial logit model as- using the ICDAS II criteria and visual and tactile exami- sumed that the data were case specific; each independent nations (using only a ball-ended probe) [19, 20]; no variable had a single value for each case. The model with radiographs were obtained [21]. the most severe caries grade as the dependent variable Cagetti et al. BMC Public Health (2016) 16:1213 Page 4 of 10 included the whole sample, using the caries-free subjects No statistically significant associations between the as the base outcome, while for the two other models, only stratification number of affected teeth and background caries-affected subjects were included, using the subjects variables were found (data not in table). with the most prevalent caries scores and the greatest The multinomial analysis is presented in Tables 4 number of affected teeth as the base outcome. An inter- and 5. The process of assessing the model showed no action model (likelihood statistics) tested the possible statistically significant effect modifiers on the dependent effects of modifiers of several background variables on the variables of the interaction between background covariates. dependent variables. The use of the most severe caries stage as a dependent Statistical significance was set as α < 0.05. variable showed that, in children with initial caries stages compared to those who were caries-free (con- sidered as the base outcome), a frequency of tooth- Results brushing of more than two times per day was near the Three hundred ninety children were examined (51.45% significance level. male and 48.55% female). Caries lesions were detected In subjects with moderate caries stages, maternal edu- in 42.31% of the subjects, while the caries experience cational level (compulsory level) and the use of lactose- (sum of decayed, filled and missing teeth due to caries) free milk as the principal dairy drink were associated was 44.06%. According to the most severe caries lesion with caries-free subjects (coef = 0.40 and p = 0.01 and stage, the affected children were divided into 2.56% coef = 1.09, p = 0.02, respectively). Maternal nationality with initial stage, 13.33% with moderate stage and from outside the European Union (coef = 1.39, p < 0.01) 26.42% with extensive stage. According to the most and toothbrushing frequency (1 time/day) (coef = −0.52, prevalent caries lesion stage, the affected children were p = 0.01) were associated in subjects with extensive lesions divided into 4.10% with a prevalence of initial stage, with regard to the base outcome (Table 4). In affected sub- 14.36% with a prevalence of moderate stage and the jects (42.31% of the total sample examined), the most remaining 23.85% with a prevalence of extensive stage. prevalent caries stage was used as the dependent variable. According to the number of affected teeth, the children In this model, the subjects with prevalence of extensive were divided into 18.21% with 1–2 affected teeth, caries stages were used as the base outcome (Table 5). In 13.33% with 3–5 affected teeth and 10.77% with six or subjects with prevalence of initial lesions, gender (male) more affected teeth. and paternal occupational status (unemployed) were The sample distribution of the questionnaire items by statistically significant associated (coef = 1.77, p =0.03 and gender is displayed in Table 1. Children with parents coef = 0.89, p = 0.04, respectively) among the subjects with from countries of the European Union, a medium/low the prevalence of extensive caries stages. In the com- educational level and an occupational status as an em- parison between subjects with prevalence of moderate ployee accounted for most of the sample. More than caries lesions and the base outcome (subjects with ex- 80% of the children appeared to have been breastfed, a tensive caries stages), maternal education level (coef = few of them used fluoride supplements, and a non- 0.60, p < 0.01), paternal occupational status (coef = −0.71, negligible percentage (approximately 30%) does not use p = 0.03) and the use of a sweetened pacifier at night fluoride in their toothpaste either. Approximately one- (coef = −1.16, p < 0.01) were statistically significantly third of the sample went to the dentist only in cases of associated. Because no statistical associations were ob- pain, regarding both the children and parents. served between the stratification number of affected The associations among background variables derived teeth and the background variables, it was decided not from the questionnaires and the different stratifying to run a multinomial model. procedures are reported in Tables 2 and 3. The most severe caries stage was statistically associated with a Discussion non-European Union maternal birthplace (p =0.02), The purpose of this study was to determine whether distinct with the educational levels of both parents (p < 0.01) caries risk indicators were associated with different stages of and with some behavioural habits, such as the use of a the caries disease process in a sample of schoolchildren in a sweetened pacifier at night (p = 0.03), the use of cross-sectional survey. The results showed that several risk lactose-free milk (p = 0.046) and the frequency of tooth- indicators interacted with disease evolution, mainly paren- brushing (p = 0.046). The distribution of affected chil- tal socio-economic and child behavioural indicators. dren, according to the most prevalent caries lesion stages, In this survey, caries distribution indicated a highly showed statistically significant associations with parental skewed figure with a large proportion of caries-free sub- educational level (p =0.02 mother and p <0.01 father), jects, a small proportion of subjects with caries at the initial with the occupational status of the mother (p = 0.03) and or moderate stage and a very large proportion of children with the use of a sweetened pacifier at night (p = 0.02). with caries at extensive stages. A skewed distribution of Cagetti et al. BMC Public Health (2016) 16:1213 Page 5 of 10 Table 1 Distribution of the sample across questionnaire variables and gender Male n (%) Female n (%) Total n (%) Parental nationality European Union 177 (45.85) 175 (45.34) 352 (91.19) Not European Union 22 (5.70) 12 (2.11) 34 (8.81) Maternal nationality European Union 185 (47.56) 180 (46.27) 365 (92.90) Not European Union 15 (3.86) 9 (2.31) 24 (7.10) Paternal nationality European Union 189 (48.96) 181 (46.90) 370 (95.86) Not European Union 10 (2.59) 6 (1.55) 16 (4.14) Eruption timing of primary teeth <6 months 58 (15.22) 57 (14.96) 115 (30.18) 6-9 months 124 (32.55) 117 (30.71) 241 (63.26) >9 months 16 (4.20) 9 (2.36) 25 (6.56) Maternal educational level Compulsory education 64 (16.45) 85 (21.85) 149 (28.30) Secondary school 104 (26.73) 82 (21.08) 186 (47.81) University 32 (8.23) 22 (5.66) 54 (13.89) Paternal educational level Compulsory education 99 (25.65) 110 (28.50) 209 (54.15) Secondary school 78 (20.20) 66 (17.10) 144 (37.30) University 22 (5.70) 11 (2.85) 33 (8.55) Maternal occupational status Housewife 69 (17.78) 78 (20.10) 147 (37.88) Unemployed 22 (5.67) 26 (6.70) 48 (12.37) Employed 89 (22.94) 59 (15.21) 148 (38.15) Self-employed 21 (5.41) 24 (6.19) 45 (11.60) Paternal occupational status Unemployed 29 (7.63) 25 (6.58) 54 (14.21) Employed 118 (31.05) 106 (27.90) 224 (58.95) Self-employed 52 (13.68) 50 (13.16) 102 (26.84) Breast-feeding at least for 3 months Yes 167 (42.93) 159 (40.87) 326 (83.80) No 34 (8.74) 29 (7.46) 63 (16.20) Bottle-feeding at least for 3 months Yes 164 (42.27) 152 (39.17) 316 (81.44) No 37 (9.54) 35 (9.02) 72 (18.56) Sweet bottle-feeding at night Yes 25 (6.63) 33 (8.75) 58 (15.38) No 167 (44.30) 152 (40.32) 319 (84.32) Sweetened pacifier at night Yes 57 (14.65) 73 (18.77) 130 (33.42) No 143 (36.76) 116 (29.82) 259 (66.58) Sweetened drink before sleeping No 70 (18.09) 67 (17.30) 137 (27.12) Yes 129 (33.33) 123 (31.26) 250 (64.60) Lactose-free milk Yes 23 (5.96) 16 (4.14) 39 (10.10) No 176 (45.60) 171 (44.30) 347 (89.90) Fluoride content in toothpaste Yes 142 (36.50) 125 (32.14) 267 (68.64) No 58 (14.91) 64 (16.45) 122 (31.36) Frequency of toothbrushing 1/day 41 (10.54) 31 (7.97) 72 (18.51) 2/day 110 (28.28) 116 (29.82) 226 (58.10) >2/day 50 (12.85) 41 (10.54) 91 (23.39) Fluoride supplement Yes 11 (2.87) 17 (4.44) 28 (7.31) No 185 (48.30) 170 (44.39) 355 (92.69) Cagetti et al. BMC Public Health (2016) 16:1213 Page 6 of 10 Table 1 Distribution of the sample across questionnaire variables and gender (Continued) Frequency of dental check-ups, parents 6 months 31 (8.20) 20 (5.29) 51 (13.49) Once per year 63 (16.67) 67 (17.72) 130 (34.39) Once every 2 years 33 (8.73) 29 (7.67) 62 (16.40) When in pain 68 (17.99) 67 (17.73) 135 (35.72) Frequency of dental check-ups, children 6 months 34 (12.27) 23 (8.30) 57 (20.57) Once per year 51 (18.41) 49 (17.69) 100 (36.10) Once every 2 years 8 (2.89) 14 (5.06) 22 (7.95) When in pain 51 (18.41) 47 (16.97) 98 (35.38) the disease in young populations from Western coun- Several questionnaire items were associated with the tries indicates the actual caries figures [1, 2], and in stratifications of children with regard to the dynamic Sardinia too [16], the prevalence of the disease was evolution of the caries process. Considering the entire reported as quite low with a high percentage of sample and according to the highest caries score, paren- caries-free children (64.5%). tal educational level was shown to be highly significantly Table 2 The distribution of the population across background variables according to the most severe caries stages Questionnaire Items Highest caries score (ICDAS) Healthy n (%) Initial n (%) Moderate n (%) Extensive n (%) p-value Maternal nationality European Union 217 (59.45) 9 (2.46) 47 (12.88) 92 (25.21) Not European Union 7 (29.17) 1 (4.17) 5 (20.83) 11 (45.83) 0.02 Parental educational level Mother Compulsory education 86 (57.72) 2 (1.34) 12 (8.05) 49 (32.89) Secondary school 107 (57.53) 5 (2.69) 30 (16.13) 44 (23.65) University 31 (57.41) 3 (5.55) 10 (18.52) 10 (18.52) <0.01 Father Compulsory education 114 (54.55) 3 (1.44) 27 (12.92) 65 (31.09) Secondary school 89 (61.81) 3 (2.08) 22 (15.28) 30 (20.83) University 19 (57.58) 4 (12.12) 3 (9.09) 7 (21.21) <0.01 Maternal occupational status Housewife 89 (60.54) 1 (0.69) 15 (10.20) 42 (28.57) Unemployed 24 (50.00) 2 (4.17) 6 (12.50) 16 (33.33) Employed 88 (59.46) 4 (2.70) 27 (18.24) 29 (19.60) Self-employed 24 (53.33) 3 (6.67) 3 (6.67) 15 (33.33) 0.06 Sweetened pacifier at night Yes 71 (54.61) 3 (2.31) 11 (8.46) 45 (34.62) No 153 (59.08) 7 (2.70) 41 (15.83) 58 (22.39) 0.03 Lactose-free milk Yes 16 (41.03) 1 (2.56) 10 (25.64) 12 (30.77) No 207 (59.65) 9 (2.59) 41 (11.82) 90 (25.94) 0.046 Frequency of toothbrushing 1/day 37 (51.39) 3 (4.17) 7 (9.72) 25 (34.72) 2/day 122 (53.98) 6 (2.65) 35 (15.49) 63 (27.88) > 2/day 65 (71.43) 1 (1.10) 10 (10.99) 15 (16.48) 0.046 The chi-square test was performed, and when a cell had a value less than five, Fisher’s exact test was performed Cagetti et al. BMC Public Health (2016) 16:1213 Page 7 of 10 Table 3 The distribution of affected subjects, according to the most prevalent caries stages (initial/moderate/extensive) and background variables Questionnaire items Most prevalent caries stage Initial n (%) Moderate n (%) Extensive n (%) p-value Maternal educational level Compulsory education 2 (3.17) 12 (19.05) 49 (77.78) 0.02 Secondary school 5 (6.33) 30 (37.97) 44 (55.70) University 3 (13.04) 10 (43.48) 10 (43.48) Paternal educational level Compulsory education 3 (3.16) 27 (28.42) 65 (68.42) <0.01 Secondary school 3 (5.46) 22 (40.00) 30 (54.54) University 4 (28.57) 3 (21.43) 7 (50.00) Maternal occupational status Housewife 1 (1.73) 15 (25.86) 42 (72.41) 0.03 Unemployed 2 (8.33) 6 (25.00) 16 (66.67) Employed 4 (6.67) 27 (45.00) 29 (48.33) Self-employed 3 (14.29) 3 (14.29) 15 (71.43) Sweetened pacifier at night Yes 3 (5.08) 11 (18.64) 45 (76.28) 0.02 No 7 (6.60) 41 (38.68) 58 (54.72) The chi-squared test was performed, and when a cell had a value less than five, Fisher’s exact test was performed Table 4 Multinomial logistic regression Number of observations = 390 log likelihood = −363.04 p < 0.01 Coef (SE) p > |z| 95% Conf. interval Caries-free (ICDAS = 0) Base outcome Initial lesions (ICDS =1/2) Maternal nationality (Not European Union) 1.05 (1.15) 0.36 −1.19/3.29 Maternal educational level (Compulsory) 0.59 (0.36) 0.11 −1.14/1.26 Paternal occupational status (Unemployed) 0.66 (0.56) 0.24 −0.45/1.77 Toothbrushing frequency (1/day) −1.12 (0.56) 0.05 −2.22/−0.01 Lactose-free milk (Yes) 0.27 (1.13) 0.81 −1.95/2.49 Sweetened pacifier at night (Yes) 0.16 (0.70) 0.83 −1.31/1.63 Moderate lesions (ICDS = 3/4) Maternal nationality (Not European Union) 0.93 (0.63) 0.14 −0.30/2.15 Maternal educational level (Compulsory) 0.40 (016) 0.01 0.08/0.72 Paternal occupational status (Unemployed) −0.55 (0.28) 0.05 −1.08/−0.01 Toothbrushing frequency (1/day) −0.27 (0.25) 0.28 −0.77/0.22 Lactose-free milk (Yes) 1.09 (0.46) 0.02 0.19/2.00 Sweetened pacifier at night (Yes) 0.63 (0.39) 0.10 −1.40/0.13 Extensive lesions (ICDS = 5/6) Maternal nationality (Not European Union) 1.39 (0.51) <0.01 0.39/2.41 Maternal educational level (Compulsory) −0.10 (0.12) 0.39 −0.33/0.13 Paternal occupational status (Unemployed) 0.03 (0.20) 0.86 −0.36/0.43 Toothbrushing frequency (1/day) −0.52 (0.20) 0.01 −0.91/−0.13 Lactose-free milk (Yes) 0.49 (0.42) 0.24 −0.33/1.31 Sweetened pacifier at night (Yes) 0.40 (0.26) 0.13 −0.11/0.91 The most severe caries stage (caries-free, initial, moderate, extensive) was used as the dependent variable Cagetti et al. BMC Public Health (2016) 16:1213 Page 8 of 10 Table 5 Multinomial logistic regression in affected subjects Number of observations = 165 log likelihood = −117.77 p < 0.01 Coef (SE) p > |z| 95% Conf. Interval Initial lesions (ICDS =1/2) Maternal educational level (Compulsory) 0.16 (0.41) 0.70 −0.64/0.95 Paternal educational level (Compulsory) 0.77 (0.62) 0.22 −0.45/1.98 Gender (Male) 1.77 (0.82) 0.03 0.16/3.39 Paternal occupational status (Unemployed) 0.89 (0.45) 0.04 0.03/1.77 Sweetened pacifier at night (Yes) 0.12 (0.84) 0.88 −1.52/1.76 Moderate lesions (ICDS = 3/4) Maternal educational level (Compulsory) 0.60 (0.21) <0.01 0.19/1.02 Paternal educational level (Compulsory) −0.19 (0.19) 0.34 −0.58/0.20 Gender (Male) −0.15 (0.38) 0.69 −0.89/0.59 Paternal occupational status (Unemployed) −0.71 (0.32) 0.03 −1.35/−0.08 Sweetened pacifier at night (Yes) −1.16 (0.43) <0.01 −2.01/−0.31 Extensive lesions (ICDS = 5/6) Base outcome The most prevalent caries stage (initial, moderate, extensive) was used as the dependent variable associated. The socio-economic level of the family in- affected by initial caries, no variables played roles in the fluences the health of all family members [22]. The change of status, while in those with moderate caries, a knowledge and personal and social skills provided low level of education of the mother and the intake of through education can better endow individuals to lactose-free milk as the primary dairy product were the access, maintain and improve their own and their covariates involved in the process. In children with the families’ health [23]. Higher levels of mothers’ educa- highest caries stage, maternal nationality outside the tion seemed to have a positive impact on children’s European Union and a low frequency of toothbrushing health [24] and on future health in adulthood [25]. habits were involved. All of these findings emphasize the Educational level remains quite stable after the school links between causal risk factors (intake of sugars and years and during adulthood, so it has a stable impact plaque) and socio-economic factors, mainly related to on health [25]. Considering the other socio-economic the mother (level of education and nationality). indicators, parental nationality and occupational status, Considering the caries-affected children stratified ac- only those factors related to the mother showed signifi- cording to the most prevalent caries lesions stage, paren- cant associations with the different caries stages. The tal educational level, maternal occupational status and mother’s educational level and occupational status were use of a sweetened pacifier at night were associated with associated with both the highest caries score and the this stratification. In the multinomial model, the base most prevalent score. As reported above, the educa- outcome was the subjects with prevalence of the highest tional level indicator has great stability and a large in- caries stage; in children with a majority of initial lesions, fluence on behaviours and habits related to health. The gender (male) and the unemployment status of the father’seducationallevel wasalsodemonstratedtobe father were embodied in this stage. In subjects with associated because both maternal knowledge and pa- prevalence of moderate lesions, a low educational level ternal knowledge affect children’s oral health. Among of the mother, paternal unemployment status and use of dietary habits and hygiene behaviours, only the use of a sweetened pacifier at night were the distinguishing a sweetened pacifier at night, the regular intake of factors. Socio-economic indicators and casual factors lactose-free milk and the frequency of toothbrushing acted in synergy also in affected subjects, and as the le- were significantly associated. Although the relationship sions progressed, diet became increasingly important in between sugar and dental caries has become weaker in the process. fluoridated societies, fermentable carbohydrates remain a No statistically significant associations of the cate- primary factor in the development of caries, especially in gorization of the number of affected teeth and back- children [26]. Sugar consumption among children has ground variables were found, probably owing to the been associated with the mother’s level of education and highly skewed caries distribution. household income [27]. The results of this study must consider its weaknesses A multinomial model in which caries-free subjects and strengths. Firstly, the cross-sectional nature of the were used as the base outcome was used to evaluate the data used in this analysis did not allow for the investiga- roles of diverse risk indicators able to change the status tion of the directionality of the associations or the clarifi- from caries-free to different caries stages. In subjects cation of the time frames of the exposures. Nevertheless Cagetti et al. BMC Public Health (2016) 16:1213 Page 9 of 10 because some unalterable risk factors are involved in Acknowledgements The authors thank everyone who helped carry out this study, particularly the caries development, such as educational level in adult- manager of the Sassari school district and all of the teaching staff at the schools hood, as well as factors that are immutable over short involved in the study. periods of time, such as occupational status [10], these risk factors or “indicators” might also be investigated in Funding No sources of funding for the research were received. cross-sectional studies. Secondly, caries is a continuous disease process, and the timing or the exposure time Availability of data and materials was not considered in the analysis. Otherwise, socio- The raw data was added as Additional file 1 (data set raw data). economic risk indicators act beginning at birth and tooth eruption, while causal factors might act at every Authors’ contributions MGC, GM and SS conceived the study and participated in its design; MGC moment of the subject’s life. Thirdly, the study considered participated in the design of the study and the drafting of the manuscript; GiC only the associations between caries indicators and the and SS collected data; FC and GC organized the dental examination actual disease (caries lesions) without considering caries appointments and administered and collected the questionnaires; GC and FC performed the statistical analysis; MGC, FC and GC were involved in the drafting consequences, such as filled and missing teeth due to of the manuscript. All of the authors read and approved the final manuscript. caries. This limitation might have affected the associations with risk indicators; otherwise, the weight of the filled and Competing interests missing component of caries experience in these age The authors declare that they have no competing interests. groups was quite low, as reported in the Results section. Consent for publication Regarding strengths, this survey started from the premise Consent to publish is not applicable, as no personal data (i.e., name etc.) was of evaluating risk indicator from a different point of view; included in the paper. usually, their roles are considered as a whole and not with consideration of the disease as a continuous process. In Ethics approval and consent to participate the literature, only one paper applied a similar approach, The study protocol was approved by the Ethics Committee of the University of Sassari (registration no. SS0421/2012). The study was conducted in accordance investigating the association between cavitated or non- with the tenets of the Declaration of Helsinki. cavitated caries lesions and background factors [28]. The Subjects were invited to participate through an information leaflet distributed sample examined was quite large and representative of the to parents at the school, explaining the aim of the study and requesting their children’s participation. Only children with their parents’ signed consent were study population with the same age range, although the enrolled. generalization of study results is limited to similar popula- tions living in areas of Western countries with a medium/ Author details Department of Biomedical, Surgical and Dental Sciences, University of Milan, low per capita income, such as Sardinia. Milan, Italy. WHO Collaboration Centre for Epidemiology and Community Dentistry, Milan, Italy. Department of Surgery, Microsurgery and Medicine Sciences, School of Dentistry, University of Sassari, Viale San Pietro 43/C, Conclusions I-07100, Sassari, Italy. The results of the present paper, within the limitations Received: 9 February 2016 Accepted: 23 November 2016 described above, provided information about how dis- tinctive risk indicators were associated with different caries stages. Maternal socio-economic indicators and References children’s behaviours were involved in the changes from 1. Campus G, Sacco G, Cagetti MG, Abati S. Changing trend of caries from 1989 to 2004 among 12-year old Sardinian children. BMC Public Health. caries-free status to different caries stages. In the differen- 2007;7:28. tiation of initial from moderate and to severe caries stages, 2. Campus G, Solinas G, Strohmenger L, Cagetti MG, Senna A, Minelli L, et al. parental socio-economic indicators and oral health be- National pathfinder survey on children’s oral health in Italy: pattern and severity of caries disease in 4-year-olds. Caries Res. 2009;43(2):155–62. haviours were embodied in caries progression. Socio- 3. Gerritsen AE, Allen PF, Witter DJ, Bronkhorst EM, Creugers NH. Tooth loss economic indicators and casual factors acted in synergy, and oral health-related quality of life: a systematic review and meta-analysis. and as the lesion progressed, diet became increasingly Health Qual Life Outcomes. 2010;8:126. 4. Nunes AM, da Silva AA, Alves CM, Hugo FN, Ribeiro CC. Factors underlying important in the process. the polarization of early childhood caries within a high-risk population. BMC Public Health. 2014;14:988. 5. Sheiham A. Oral health, general health, and quality of life Bulletin of World Additional file Health. Organization. 2005;83(9):641–720. 6. Sheiham A, Sabbah W. Using universal patterns of caries for planning and Additional file 1: Data set raw data. (XLSX 82 kb) evaluating dental care. Caries Res. 2010;44(2):141–50. 7. Mejia GC. Measuring the oral health of populations. Community Dent Oral Epidemiol. 2012;40(S2):95–101. Abbreviations 8. Tanzer JM, Livingston J, Thompson AM. The microbiology of primary dental Coef: Coefficient; GC: Guglielmo Campus, the author who acted as caries in humans. J Dent Educ. 2001;65(10):1028–37. benchmark for the calibration of the examiner; GiC: Giovanna Congiu, the 9. Piovesan C, Mendes FM, Antunes JL, Ardenghi TM. Inequalities in the author who was involved in the clinical examination; ICDAS: International distribution of dental caries among 12-year-old Brazilian schoolchildren. Braz Caries Detection Assessment System; WHO: World Health Organization Oral Res. 2011;25(1):69–75. Cagetti et al. BMC Public Health (2016) 16:1213 Page 10 of 10 10. Costa SM, Martins CC, Bonfim Mde L, Zina LG, Paiva SM, Pordeus IA, et al. A systematic review of socioeconomic indicators and dental caries in adults. Int J Environ Res Public Health. 2012;9(10):3540–74. 11. Takahashi N, Nyvad B. Caries ecology revisited: microbial dynamics and the caries process. Caries Res. 2008;42(6):409–18. 12. Vadiakas G. Case definition, aetiology and risk assessment of early childhood caries (ECC): a revisited review. European Arch Paed Dent. 2008;9(9):114–25. 13. Clara J, Bourgeois D, Muller-Bolla M. DMF from WHO basic methods to ICDAS II advanced methods: a systematic review of literature. Odontol Trop. 2012;35(139):5–11. 14. Iranzo-Cortés JE, Montiel-Company JM, Almerich-Silla JM. Caries diagnosis: agreement between WHO and ICDAS II criteria in epidemiological surveys. Community Dent Health. 2013;30(2):108–11. 15. Italian Institute for Statistic 2013. http://demo.istat.it/pop2013/index_e.html. Accessed 13 Jan 2014. 16. Carta G, Cagetti MG, Sale S, Congiu G, Strohmenger L, Oleari F, et al. Oral health inequalities in Italian schoolchildren–a cross-sectional evaluation. Community Dent Health. 2014;31(2):123–8. 17. Ofstedal MB, Weir DR. The recruitment and retention of minority participants in the Health and Retirement Study. Gerontologist. 2011;51:S8–20. 18. Congiu G, Campus G, Sale S, Spano G, Cagetti MG, Lugliè PF. Early childhood caries and associated determinants: a cross-sectional study on Italian preschool children. J Public Health Dent. 2014;74(2):147–52. 19. Braga MM, Ekstrand KR, Martignon S, Imparato JCP, Ricketts DNJ, Mendes FM. Clinical performance of Two visual scoring systems in detecting and assessing activity status of occlusal caries in primary teeth. Caries Res. 2010; 44(3):300–8. 20. Honkala E, Runnel R, Honkala S, Olak J, Vahlberg T, Saag M, et al. Measuring dental caries in the mixed dentition by ICDAS. Int J Dent. 2011;1504:24. 21. Espelid I, Mejàre I, Weerheijm K, EAPD. EAPD guidelines for use of radiographs in children. Eur J Paediatr Dent. 2003;4(1):40–8. 22. Vargas CM, Ronzio CR. Disparities in early childhood caries. BMC Oral Health. 2006;6 Suppl 1:S3. 23. Case A, Fertig A, Paxson C. The lasting impact of childhood health and circumstance. J Health Econ. 2005;24(2):365–89. 24. van Doorslaer E, Masseria C, Koolman X. Inequalities in access to medical care by income in developed countries. CMAJ. 2006;174(2):177–83. 25. Currie J, Moretti E. Mother’s education and the intergenerational transmission of human capital: evidence from college openings. Quart J Econ. 2003;118(4): 1495–532. 26. Moynihan P. Sugars and dental caries. Evidence for setting a recommended threshold for intake. Adv Nutr. 2016;7(1):149–56. 27. Johansson I, Holgerson PL, Kressin NR, Nunn ME, Tanner AC. Snacking habits and caries in young children. Caries Res. 2010;44(5):421–30. 28. Mendes FM, Braga MM, Oliveira LB, Antunes JLF, Ardenghi TM, Bönecker M. Discriminant validity of the International Caries Detection and Assessment System (ICDAS) and comparability with World Health Organization criteria in a cross-sectional study. Community Dent Oral Epidemiol. 2010;38(5):398–407. Submit your next manuscript to BioMed Central and we will help you at every step: • We accept pre-submission inquiries � Our selector tool helps you to find the most relevant journal � We provide round the clock customer support � Convenient online submission � Thorough peer review � Inclusion in PubMed and all major indexing services � Maximum visibility for your research Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Public Health Springer Journals

Are distinctive risk indicators associated with different stages of caries in children? A cross-sectional study

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Springer Journals
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2016 The Author(s).
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10.1186/s12889-016-3865-4
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Abstract

Background: Actual caries figures emphasize the need to identify the risk indicators involved in the disease’s development. The hypothesis that certain risk indicators might affect the dynamic evolution of the caries process was assessed; to clarify this premise, a cross-sectional survey was performed in school children. Methods: A total of 390 subjects aged 6–8 years old were randomly selected. Caries was assessed, and the subjects were stratified as follows: i) highest caries score; ii) most prevalent caries score; and iii) number of affected teeth. Parents/guardians completed a questionnaire regarding vital statistics, socio-economic indicators, dietary habits, oral hygiene habits and oral health behaviours. Results: Caries was detected in 42.31% of the subjects. Maternal nationality, parental education level, use of a sweetened pacifier at night, intake of lactose-free milk and toothbrushing frequency were statistically significant associated (p < 0.05) with subjects stratified according to the highest caries score. Parental educational level, maternal occupational status and use of a sweetened pacifier at night were associated (p < 0.05) with affected children stratified according to the most prevalent caries score. Maternal educational level and intake of lactose-free milk were associated with subjects with moderate caries stages compared to being caries-free (p =0.01 and p = 0.02, respectively). Maternal nationality (p < 0.01) andtoothbrushingfrequency (p = 0.01) were associated with subjects affected by extensive lesions compared to caries-free children. In subjects affected by initial lesions as the most prevalent figure, gender (male) and paternal occupation status (unemployed) were statistically significant associated (p =0.03 and p = 0.04, respectively) compared to those affected by highest prevalence of extensive caries lesions. In children with the highest prevalence of moderate caries lesions, maternal education level (p < 0.01), paternal occupational status (p = 0.03) and use of a sweetened pacifier at night (p < 0.01) were statistically significantly associated. Conclusions: Maternal nationality, maternal low level of education, intake of lactose-free milk and low toothbrushing frequency were involved in the change from caries-free status to different caries stages. Gender, paternal unemployment, maternal low educational level and use of a sweetened pacifier were correlated with caries progression, showing how distinctive risk indicators were associated with different caries stages. Keywords: Dental caries, Children, Risk indicators, Caries staging, Feeding practice, Socio-economic status * Correspondence: [email protected] WHO Collaboration Centre for Epidemiology and Community Dentistry, Milan, Italy Department of Surgery, Microsurgery and Medicine Sciences, School of Dentistry, University of Sassari, Viale San Pietro 43/C, I-07100, Sassari, Italy Full list of author information is available at the end of the article © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cagetti et al. BMC Public Health (2016) 16:1213 Page 2 of 10 Background support decision-making at both the individual and Although, in recent decades in Western countries, a community levels [14]. The ICDAS provides options for decreasing caries trend has been observed, especially in coding 6 different stages of caries lesions (0 sound, 1 first childhood [1, 2], dental caries remains a major public visual change in enamel, 2 distinct visual change in ena- health issue with impacts on the quality of life of children mel, 3 localized enamel breakdown, 4 underlying dentin and adults [3]. Despite continuous improvements in den- shadow, 5 distinct cavity with visible dentin, and 6 exten- tal health, children remain a primary disparity group [4]. sive cavity with visible dentin) [14]. Health risk evaluation is the comprehensive assessment of As mentioned above, the premise of this study was to risk factors in the general population or specific groups, determine whether specific risk indicators might affect such as children, the elderly, subjects with immigrant different stages of the caries disease process. To investi- backgrounds and so on, based on environmental, genetic, gate this issue, a cross-sectional survey was designed economic, social and behavioural health determinants [5]. and performed. The caries decrease has resulted in a polarization of the distribution of the disease, and today, high caries figures Methods are observed only in a small proportion of the population Sample selection and study design [1, 4]. When the mean number of decayed, missing and The study protocol was approved by the Ethics Committee filled teeth improves, the number of caries-free individuals of the University of Sassari (registration no. SS0421/2012). increases, and polarization becomes more pronounced [6]. The study was conducted in accordance with the tenets of This skewed distribution emphasizes the need to identify the Declaration of Helsinki. According to data derived caries risk indicators that are involved in the development from the Italian Institute of Statistics [15] in 2013, the of the disease to plan targeted preventive programmes that number of subjects aged 6–8 years old living in the Sassari consider that health is linked to health promotion, particu- area was 3095. The study used a cross-sectional design, larly when care resources are limited [7]. and a formula for estimating population proportions with Caries can be defined as a dietary-bacterial disease [8], high precision was used to calculate the sample size. Data with the interactions between the host and different risk derived from the recent literature [16] described a preva- factors derived from social inequalities, such as a low lence of caries in the same age group of approximately socio-economic level, recent immigrant status, a low 35%. A power analysis was performed with G*Power soft- educational degree and unemployment status [9, 10]. ware, version 3.1.9.2 for Apple, using logistic regression, Considering the complex aetiology of the disease, a with the prevalence ratio added to 40% to safeguard against crucial issue is to identify its potential determinants and the risk of disease spread, an error probability of 0.05 and predictors to determine the appropriate public health actual power of 0.95. The total sample size was set to 246. measures to prevent it. Because caries lesions have a In February 2014, schoolchildren were recruited at their dynamic evolution requiring a long period of time, schools using systematic cluster sampling; every class was usually many months or years [11], it might be specu- identified as a cluster, and the class list was compiled. The lated that different risk indicators might be involved in first cluster was randomly selected, while the others were several stages of the dynamic process, playing different systematically chosen at intervals of three classes. The roles at different times. This study began with the number of subjects was approximately the same in each hypothesis that specific risk indicators might manifest class (n = 20 subjects). Considering the possibility of a low their effects in specific caries stages, leading to distinct response rate [17], 520 children were invited to participate patterns that could be identified and studied. For ex- through an information leaflet distributed to parents at the ample, subjects, especially children with initial lesions, school, explaining the aim of the study and requesting their should be considered at high risk for caries because children’s participation. Only children with their parents’ these lesions are indicative of caries activity [12]. signed consent were enrolled. Consent was obtained for Another difficult issue is the complexity of the disease 427 children. Parents were asked to complete a stan- state because the different manifestations of caries can- dardized questionnaire regarding different variables re- not be quantified by a single metric. The progression of lated to caries. Twenty-two subjects (5.15% dropouts) the lesion cannot be assessed with the most commonly returned an incomplete questionnaire and were excluded used caries index, the DMFT/S index (the sum of decayed, from the survey; moreover, 15 (3.51%) children were ab- missed, filled teeth/surfaces) because it does not distin- sent from school on the day of the examination. The guish among the different stages of caries lesions [13, 14]. survey reported data from 390 children (Fig. 1). The International Caries Detection Assessment System (ICDAS), which is based on the best available evidence for Data collection detecting the early and late stages of caries severity, should The data collection methods consisted of a questionnaire lead to the acquisition of better quality information to and a clinical oral examination. A structured standardized Cagetti et al. BMC Public Health (2016) 16:1213 Page 3 of 10 Fig. 1 Flow diagram of the recruitment of children questionnaire [18] was submitted to the parents/guardians Data analysis before the examination. The questionnaire was based on All of the data were input into a spreadsheet (Microsoft the following domains: 1 - vital statistics: gender, parental Excel® 2011 for Mac, version 14.4.3). Statistical analyses nationality, and eruption timing of primary teeth; 2 - were performed using Stata/SE® software, version 13.1 socio-economic indicators: parental educational level and for Mac (64-bit Intel®)(for raw data consultation please parental occupational status; 3 - dietary habits: breast- check Additional file 1). feeding, bottle-feeding, sweet bottle-feeding at night, Data from the clinical examinations were grouped as use of a sweetened pacifier at night, sweetened drinks follows: No caries (ICDAS 0), Initial stage (ICDAS 1–2), before sleeping and use of lactose-free milk as the main Moderate stage (ICDAS 3–4) and Extensive stage diary product; 4 - oral hygiene habits: fluoride amount (ICDAS 5–6). Regarding the number of affected teeth in in toothpaste, frequency of toothbrushing, and fluoride each subject, the following categories were defined: 1–2 supplement intake; and 5 - oral health behaviours: affected teeth, 3–5 affected teeth, and six or more frequency of dental check-ups for the parents and affected teeth. children. As the clinical chart was printed in the other Subjects were stratified according to the following side of the sheet of questionnaire, the questionnaire three different procedures: i) the maximum caries form was collected directly by the examiner before the stage – subjects were coded according to the highest examination. caries score (ICDAS) recorded; ii) the most prevalent Children were examined at their schools using a cali- caries stage – subjects were coded according to the brated examiner (GiC) from September to November of most prevalent caries score (ICDAS) recorded; and iii) 2014. An author (GC) acted as a benchmark, training the number of affected teeth – subjects were coded and calibrating the examiner (GiC). Fifty subjects, not according to the number of affected teeth recorded. included in the sample, were examined and re-examined Responses to questionnaire items were treated as cate- after 72 h. Intra-examiner reproducibility was evaluated gorical or ordinal variables. through percentage agreement and Cohen’s kappa statis- Associations between background variables and sub- tics. The percentage agreement was high at both the jects, stratified as reported above, were assessed using subject and tooth surface levels (Cohen’s kappa = 0.86 the chi-squared test; for values less than five, Fisher’s and 0.77, respectively). Clinical examinations were per- exact test was performed. formed under standardized conditions using a portable Multinomial logit models were performed following air-drier device, a plain mirror and a WHO Community the stratifying procedures to assess the associations with Periodontal Index probe. Dental caries was assessed background variables. The multinomial logit model as- using the ICDAS II criteria and visual and tactile exami- sumed that the data were case specific; each independent nations (using only a ball-ended probe) [19, 20]; no variable had a single value for each case. The model with radiographs were obtained [21]. the most severe caries grade as the dependent variable Cagetti et al. BMC Public Health (2016) 16:1213 Page 4 of 10 included the whole sample, using the caries-free subjects No statistically significant associations between the as the base outcome, while for the two other models, only stratification number of affected teeth and background caries-affected subjects were included, using the subjects variables were found (data not in table). with the most prevalent caries scores and the greatest The multinomial analysis is presented in Tables 4 number of affected teeth as the base outcome. An inter- and 5. The process of assessing the model showed no action model (likelihood statistics) tested the possible statistically significant effect modifiers on the dependent effects of modifiers of several background variables on the variables of the interaction between background covariates. dependent variables. The use of the most severe caries stage as a dependent Statistical significance was set as α < 0.05. variable showed that, in children with initial caries stages compared to those who were caries-free (con- sidered as the base outcome), a frequency of tooth- Results brushing of more than two times per day was near the Three hundred ninety children were examined (51.45% significance level. male and 48.55% female). Caries lesions were detected In subjects with moderate caries stages, maternal edu- in 42.31% of the subjects, while the caries experience cational level (compulsory level) and the use of lactose- (sum of decayed, filled and missing teeth due to caries) free milk as the principal dairy drink were associated was 44.06%. According to the most severe caries lesion with caries-free subjects (coef = 0.40 and p = 0.01 and stage, the affected children were divided into 2.56% coef = 1.09, p = 0.02, respectively). Maternal nationality with initial stage, 13.33% with moderate stage and from outside the European Union (coef = 1.39, p < 0.01) 26.42% with extensive stage. According to the most and toothbrushing frequency (1 time/day) (coef = −0.52, prevalent caries lesion stage, the affected children were p = 0.01) were associated in subjects with extensive lesions divided into 4.10% with a prevalence of initial stage, with regard to the base outcome (Table 4). In affected sub- 14.36% with a prevalence of moderate stage and the jects (42.31% of the total sample examined), the most remaining 23.85% with a prevalence of extensive stage. prevalent caries stage was used as the dependent variable. According to the number of affected teeth, the children In this model, the subjects with prevalence of extensive were divided into 18.21% with 1–2 affected teeth, caries stages were used as the base outcome (Table 5). In 13.33% with 3–5 affected teeth and 10.77% with six or subjects with prevalence of initial lesions, gender (male) more affected teeth. and paternal occupational status (unemployed) were The sample distribution of the questionnaire items by statistically significant associated (coef = 1.77, p =0.03 and gender is displayed in Table 1. Children with parents coef = 0.89, p = 0.04, respectively) among the subjects with from countries of the European Union, a medium/low the prevalence of extensive caries stages. In the com- educational level and an occupational status as an em- parison between subjects with prevalence of moderate ployee accounted for most of the sample. More than caries lesions and the base outcome (subjects with ex- 80% of the children appeared to have been breastfed, a tensive caries stages), maternal education level (coef = few of them used fluoride supplements, and a non- 0.60, p < 0.01), paternal occupational status (coef = −0.71, negligible percentage (approximately 30%) does not use p = 0.03) and the use of a sweetened pacifier at night fluoride in their toothpaste either. Approximately one- (coef = −1.16, p < 0.01) were statistically significantly third of the sample went to the dentist only in cases of associated. Because no statistical associations were ob- pain, regarding both the children and parents. served between the stratification number of affected The associations among background variables derived teeth and the background variables, it was decided not from the questionnaires and the different stratifying to run a multinomial model. procedures are reported in Tables 2 and 3. The most severe caries stage was statistically associated with a Discussion non-European Union maternal birthplace (p =0.02), The purpose of this study was to determine whether distinct with the educational levels of both parents (p < 0.01) caries risk indicators were associated with different stages of and with some behavioural habits, such as the use of a the caries disease process in a sample of schoolchildren in a sweetened pacifier at night (p = 0.03), the use of cross-sectional survey. The results showed that several risk lactose-free milk (p = 0.046) and the frequency of tooth- indicators interacted with disease evolution, mainly paren- brushing (p = 0.046). The distribution of affected chil- tal socio-economic and child behavioural indicators. dren, according to the most prevalent caries lesion stages, In this survey, caries distribution indicated a highly showed statistically significant associations with parental skewed figure with a large proportion of caries-free sub- educational level (p =0.02 mother and p <0.01 father), jects, a small proportion of subjects with caries at the initial with the occupational status of the mother (p = 0.03) and or moderate stage and a very large proportion of children with the use of a sweetened pacifier at night (p = 0.02). with caries at extensive stages. A skewed distribution of Cagetti et al. BMC Public Health (2016) 16:1213 Page 5 of 10 Table 1 Distribution of the sample across questionnaire variables and gender Male n (%) Female n (%) Total n (%) Parental nationality European Union 177 (45.85) 175 (45.34) 352 (91.19) Not European Union 22 (5.70) 12 (2.11) 34 (8.81) Maternal nationality European Union 185 (47.56) 180 (46.27) 365 (92.90) Not European Union 15 (3.86) 9 (2.31) 24 (7.10) Paternal nationality European Union 189 (48.96) 181 (46.90) 370 (95.86) Not European Union 10 (2.59) 6 (1.55) 16 (4.14) Eruption timing of primary teeth <6 months 58 (15.22) 57 (14.96) 115 (30.18) 6-9 months 124 (32.55) 117 (30.71) 241 (63.26) >9 months 16 (4.20) 9 (2.36) 25 (6.56) Maternal educational level Compulsory education 64 (16.45) 85 (21.85) 149 (28.30) Secondary school 104 (26.73) 82 (21.08) 186 (47.81) University 32 (8.23) 22 (5.66) 54 (13.89) Paternal educational level Compulsory education 99 (25.65) 110 (28.50) 209 (54.15) Secondary school 78 (20.20) 66 (17.10) 144 (37.30) University 22 (5.70) 11 (2.85) 33 (8.55) Maternal occupational status Housewife 69 (17.78) 78 (20.10) 147 (37.88) Unemployed 22 (5.67) 26 (6.70) 48 (12.37) Employed 89 (22.94) 59 (15.21) 148 (38.15) Self-employed 21 (5.41) 24 (6.19) 45 (11.60) Paternal occupational status Unemployed 29 (7.63) 25 (6.58) 54 (14.21) Employed 118 (31.05) 106 (27.90) 224 (58.95) Self-employed 52 (13.68) 50 (13.16) 102 (26.84) Breast-feeding at least for 3 months Yes 167 (42.93) 159 (40.87) 326 (83.80) No 34 (8.74) 29 (7.46) 63 (16.20) Bottle-feeding at least for 3 months Yes 164 (42.27) 152 (39.17) 316 (81.44) No 37 (9.54) 35 (9.02) 72 (18.56) Sweet bottle-feeding at night Yes 25 (6.63) 33 (8.75) 58 (15.38) No 167 (44.30) 152 (40.32) 319 (84.32) Sweetened pacifier at night Yes 57 (14.65) 73 (18.77) 130 (33.42) No 143 (36.76) 116 (29.82) 259 (66.58) Sweetened drink before sleeping No 70 (18.09) 67 (17.30) 137 (27.12) Yes 129 (33.33) 123 (31.26) 250 (64.60) Lactose-free milk Yes 23 (5.96) 16 (4.14) 39 (10.10) No 176 (45.60) 171 (44.30) 347 (89.90) Fluoride content in toothpaste Yes 142 (36.50) 125 (32.14) 267 (68.64) No 58 (14.91) 64 (16.45) 122 (31.36) Frequency of toothbrushing 1/day 41 (10.54) 31 (7.97) 72 (18.51) 2/day 110 (28.28) 116 (29.82) 226 (58.10) >2/day 50 (12.85) 41 (10.54) 91 (23.39) Fluoride supplement Yes 11 (2.87) 17 (4.44) 28 (7.31) No 185 (48.30) 170 (44.39) 355 (92.69) Cagetti et al. BMC Public Health (2016) 16:1213 Page 6 of 10 Table 1 Distribution of the sample across questionnaire variables and gender (Continued) Frequency of dental check-ups, parents 6 months 31 (8.20) 20 (5.29) 51 (13.49) Once per year 63 (16.67) 67 (17.72) 130 (34.39) Once every 2 years 33 (8.73) 29 (7.67) 62 (16.40) When in pain 68 (17.99) 67 (17.73) 135 (35.72) Frequency of dental check-ups, children 6 months 34 (12.27) 23 (8.30) 57 (20.57) Once per year 51 (18.41) 49 (17.69) 100 (36.10) Once every 2 years 8 (2.89) 14 (5.06) 22 (7.95) When in pain 51 (18.41) 47 (16.97) 98 (35.38) the disease in young populations from Western coun- Several questionnaire items were associated with the tries indicates the actual caries figures [1, 2], and in stratifications of children with regard to the dynamic Sardinia too [16], the prevalence of the disease was evolution of the caries process. Considering the entire reported as quite low with a high percentage of sample and according to the highest caries score, paren- caries-free children (64.5%). tal educational level was shown to be highly significantly Table 2 The distribution of the population across background variables according to the most severe caries stages Questionnaire Items Highest caries score (ICDAS) Healthy n (%) Initial n (%) Moderate n (%) Extensive n (%) p-value Maternal nationality European Union 217 (59.45) 9 (2.46) 47 (12.88) 92 (25.21) Not European Union 7 (29.17) 1 (4.17) 5 (20.83) 11 (45.83) 0.02 Parental educational level Mother Compulsory education 86 (57.72) 2 (1.34) 12 (8.05) 49 (32.89) Secondary school 107 (57.53) 5 (2.69) 30 (16.13) 44 (23.65) University 31 (57.41) 3 (5.55) 10 (18.52) 10 (18.52) <0.01 Father Compulsory education 114 (54.55) 3 (1.44) 27 (12.92) 65 (31.09) Secondary school 89 (61.81) 3 (2.08) 22 (15.28) 30 (20.83) University 19 (57.58) 4 (12.12) 3 (9.09) 7 (21.21) <0.01 Maternal occupational status Housewife 89 (60.54) 1 (0.69) 15 (10.20) 42 (28.57) Unemployed 24 (50.00) 2 (4.17) 6 (12.50) 16 (33.33) Employed 88 (59.46) 4 (2.70) 27 (18.24) 29 (19.60) Self-employed 24 (53.33) 3 (6.67) 3 (6.67) 15 (33.33) 0.06 Sweetened pacifier at night Yes 71 (54.61) 3 (2.31) 11 (8.46) 45 (34.62) No 153 (59.08) 7 (2.70) 41 (15.83) 58 (22.39) 0.03 Lactose-free milk Yes 16 (41.03) 1 (2.56) 10 (25.64) 12 (30.77) No 207 (59.65) 9 (2.59) 41 (11.82) 90 (25.94) 0.046 Frequency of toothbrushing 1/day 37 (51.39) 3 (4.17) 7 (9.72) 25 (34.72) 2/day 122 (53.98) 6 (2.65) 35 (15.49) 63 (27.88) > 2/day 65 (71.43) 1 (1.10) 10 (10.99) 15 (16.48) 0.046 The chi-square test was performed, and when a cell had a value less than five, Fisher’s exact test was performed Cagetti et al. BMC Public Health (2016) 16:1213 Page 7 of 10 Table 3 The distribution of affected subjects, according to the most prevalent caries stages (initial/moderate/extensive) and background variables Questionnaire items Most prevalent caries stage Initial n (%) Moderate n (%) Extensive n (%) p-value Maternal educational level Compulsory education 2 (3.17) 12 (19.05) 49 (77.78) 0.02 Secondary school 5 (6.33) 30 (37.97) 44 (55.70) University 3 (13.04) 10 (43.48) 10 (43.48) Paternal educational level Compulsory education 3 (3.16) 27 (28.42) 65 (68.42) <0.01 Secondary school 3 (5.46) 22 (40.00) 30 (54.54) University 4 (28.57) 3 (21.43) 7 (50.00) Maternal occupational status Housewife 1 (1.73) 15 (25.86) 42 (72.41) 0.03 Unemployed 2 (8.33) 6 (25.00) 16 (66.67) Employed 4 (6.67) 27 (45.00) 29 (48.33) Self-employed 3 (14.29) 3 (14.29) 15 (71.43) Sweetened pacifier at night Yes 3 (5.08) 11 (18.64) 45 (76.28) 0.02 No 7 (6.60) 41 (38.68) 58 (54.72) The chi-squared test was performed, and when a cell had a value less than five, Fisher’s exact test was performed Table 4 Multinomial logistic regression Number of observations = 390 log likelihood = −363.04 p < 0.01 Coef (SE) p > |z| 95% Conf. interval Caries-free (ICDAS = 0) Base outcome Initial lesions (ICDS =1/2) Maternal nationality (Not European Union) 1.05 (1.15) 0.36 −1.19/3.29 Maternal educational level (Compulsory) 0.59 (0.36) 0.11 −1.14/1.26 Paternal occupational status (Unemployed) 0.66 (0.56) 0.24 −0.45/1.77 Toothbrushing frequency (1/day) −1.12 (0.56) 0.05 −2.22/−0.01 Lactose-free milk (Yes) 0.27 (1.13) 0.81 −1.95/2.49 Sweetened pacifier at night (Yes) 0.16 (0.70) 0.83 −1.31/1.63 Moderate lesions (ICDS = 3/4) Maternal nationality (Not European Union) 0.93 (0.63) 0.14 −0.30/2.15 Maternal educational level (Compulsory) 0.40 (016) 0.01 0.08/0.72 Paternal occupational status (Unemployed) −0.55 (0.28) 0.05 −1.08/−0.01 Toothbrushing frequency (1/day) −0.27 (0.25) 0.28 −0.77/0.22 Lactose-free milk (Yes) 1.09 (0.46) 0.02 0.19/2.00 Sweetened pacifier at night (Yes) 0.63 (0.39) 0.10 −1.40/0.13 Extensive lesions (ICDS = 5/6) Maternal nationality (Not European Union) 1.39 (0.51) <0.01 0.39/2.41 Maternal educational level (Compulsory) −0.10 (0.12) 0.39 −0.33/0.13 Paternal occupational status (Unemployed) 0.03 (0.20) 0.86 −0.36/0.43 Toothbrushing frequency (1/day) −0.52 (0.20) 0.01 −0.91/−0.13 Lactose-free milk (Yes) 0.49 (0.42) 0.24 −0.33/1.31 Sweetened pacifier at night (Yes) 0.40 (0.26) 0.13 −0.11/0.91 The most severe caries stage (caries-free, initial, moderate, extensive) was used as the dependent variable Cagetti et al. BMC Public Health (2016) 16:1213 Page 8 of 10 Table 5 Multinomial logistic regression in affected subjects Number of observations = 165 log likelihood = −117.77 p < 0.01 Coef (SE) p > |z| 95% Conf. Interval Initial lesions (ICDS =1/2) Maternal educational level (Compulsory) 0.16 (0.41) 0.70 −0.64/0.95 Paternal educational level (Compulsory) 0.77 (0.62) 0.22 −0.45/1.98 Gender (Male) 1.77 (0.82) 0.03 0.16/3.39 Paternal occupational status (Unemployed) 0.89 (0.45) 0.04 0.03/1.77 Sweetened pacifier at night (Yes) 0.12 (0.84) 0.88 −1.52/1.76 Moderate lesions (ICDS = 3/4) Maternal educational level (Compulsory) 0.60 (0.21) <0.01 0.19/1.02 Paternal educational level (Compulsory) −0.19 (0.19) 0.34 −0.58/0.20 Gender (Male) −0.15 (0.38) 0.69 −0.89/0.59 Paternal occupational status (Unemployed) −0.71 (0.32) 0.03 −1.35/−0.08 Sweetened pacifier at night (Yes) −1.16 (0.43) <0.01 −2.01/−0.31 Extensive lesions (ICDS = 5/6) Base outcome The most prevalent caries stage (initial, moderate, extensive) was used as the dependent variable associated. The socio-economic level of the family in- affected by initial caries, no variables played roles in the fluences the health of all family members [22]. The change of status, while in those with moderate caries, a knowledge and personal and social skills provided low level of education of the mother and the intake of through education can better endow individuals to lactose-free milk as the primary dairy product were the access, maintain and improve their own and their covariates involved in the process. In children with the families’ health [23]. Higher levels of mothers’ educa- highest caries stage, maternal nationality outside the tion seemed to have a positive impact on children’s European Union and a low frequency of toothbrushing health [24] and on future health in adulthood [25]. habits were involved. All of these findings emphasize the Educational level remains quite stable after the school links between causal risk factors (intake of sugars and years and during adulthood, so it has a stable impact plaque) and socio-economic factors, mainly related to on health [25]. Considering the other socio-economic the mother (level of education and nationality). indicators, parental nationality and occupational status, Considering the caries-affected children stratified ac- only those factors related to the mother showed signifi- cording to the most prevalent caries lesions stage, paren- cant associations with the different caries stages. The tal educational level, maternal occupational status and mother’s educational level and occupational status were use of a sweetened pacifier at night were associated with associated with both the highest caries score and the this stratification. In the multinomial model, the base most prevalent score. As reported above, the educa- outcome was the subjects with prevalence of the highest tional level indicator has great stability and a large in- caries stage; in children with a majority of initial lesions, fluence on behaviours and habits related to health. The gender (male) and the unemployment status of the father’seducationallevel wasalsodemonstratedtobe father were embodied in this stage. In subjects with associated because both maternal knowledge and pa- prevalence of moderate lesions, a low educational level ternal knowledge affect children’s oral health. Among of the mother, paternal unemployment status and use of dietary habits and hygiene behaviours, only the use of a sweetened pacifier at night were the distinguishing a sweetened pacifier at night, the regular intake of factors. Socio-economic indicators and casual factors lactose-free milk and the frequency of toothbrushing acted in synergy also in affected subjects, and as the le- were significantly associated. Although the relationship sions progressed, diet became increasingly important in between sugar and dental caries has become weaker in the process. fluoridated societies, fermentable carbohydrates remain a No statistically significant associations of the cate- primary factor in the development of caries, especially in gorization of the number of affected teeth and back- children [26]. Sugar consumption among children has ground variables were found, probably owing to the been associated with the mother’s level of education and highly skewed caries distribution. household income [27]. The results of this study must consider its weaknesses A multinomial model in which caries-free subjects and strengths. Firstly, the cross-sectional nature of the were used as the base outcome was used to evaluate the data used in this analysis did not allow for the investiga- roles of diverse risk indicators able to change the status tion of the directionality of the associations or the clarifi- from caries-free to different caries stages. In subjects cation of the time frames of the exposures. Nevertheless Cagetti et al. BMC Public Health (2016) 16:1213 Page 9 of 10 because some unalterable risk factors are involved in Acknowledgements The authors thank everyone who helped carry out this study, particularly the caries development, such as educational level in adult- manager of the Sassari school district and all of the teaching staff at the schools hood, as well as factors that are immutable over short involved in the study. periods of time, such as occupational status [10], these risk factors or “indicators” might also be investigated in Funding No sources of funding for the research were received. cross-sectional studies. Secondly, caries is a continuous disease process, and the timing or the exposure time Availability of data and materials was not considered in the analysis. Otherwise, socio- The raw data was added as Additional file 1 (data set raw data). economic risk indicators act beginning at birth and tooth eruption, while causal factors might act at every Authors’ contributions MGC, GM and SS conceived the study and participated in its design; MGC moment of the subject’s life. Thirdly, the study considered participated in the design of the study and the drafting of the manuscript; GiC only the associations between caries indicators and the and SS collected data; FC and GC organized the dental examination actual disease (caries lesions) without considering caries appointments and administered and collected the questionnaires; GC and FC performed the statistical analysis; MGC, FC and GC were involved in the drafting consequences, such as filled and missing teeth due to of the manuscript. All of the authors read and approved the final manuscript. caries. This limitation might have affected the associations with risk indicators; otherwise, the weight of the filled and Competing interests missing component of caries experience in these age The authors declare that they have no competing interests. groups was quite low, as reported in the Results section. Consent for publication Regarding strengths, this survey started from the premise Consent to publish is not applicable, as no personal data (i.e., name etc.) was of evaluating risk indicator from a different point of view; included in the paper. usually, their roles are considered as a whole and not with consideration of the disease as a continuous process. In Ethics approval and consent to participate the literature, only one paper applied a similar approach, The study protocol was approved by the Ethics Committee of the University of Sassari (registration no. SS0421/2012). The study was conducted in accordance investigating the association between cavitated or non- with the tenets of the Declaration of Helsinki. cavitated caries lesions and background factors [28]. The Subjects were invited to participate through an information leaflet distributed sample examined was quite large and representative of the to parents at the school, explaining the aim of the study and requesting their children’s participation. Only children with their parents’ signed consent were study population with the same age range, although the enrolled. generalization of study results is limited to similar popula- tions living in areas of Western countries with a medium/ Author details Department of Biomedical, Surgical and Dental Sciences, University of Milan, low per capita income, such as Sardinia. Milan, Italy. WHO Collaboration Centre for Epidemiology and Community Dentistry, Milan, Italy. Department of Surgery, Microsurgery and Medicine Sciences, School of Dentistry, University of Sassari, Viale San Pietro 43/C, Conclusions I-07100, Sassari, Italy. The results of the present paper, within the limitations Received: 9 February 2016 Accepted: 23 November 2016 described above, provided information about how dis- tinctive risk indicators were associated with different caries stages. Maternal socio-economic indicators and References children’s behaviours were involved in the changes from 1. Campus G, Sacco G, Cagetti MG, Abati S. Changing trend of caries from 1989 to 2004 among 12-year old Sardinian children. BMC Public Health. caries-free status to different caries stages. In the differen- 2007;7:28. tiation of initial from moderate and to severe caries stages, 2. 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Discriminant validity of the International Caries Detection and Assessment System (ICDAS) and comparability with World Health Organization criteria in a cross-sectional study. Community Dent Oral Epidemiol. 2010;38(5):398–407. Submit your next manuscript to BioMed Central and we will help you at every step: • We accept pre-submission inquiries � Our selector tool helps you to find the most relevant journal � We provide round the clock customer support � Convenient online submission � Thorough peer review � Inclusion in PubMed and all major indexing services � Maximum visibility for your research Submit your manuscript at www.biomedcentral.com/submit

Journal

BMC Public Health – Springer Journals

Published: Dec 1, 2016

Keywords: public health; medicine/public health, general; epidemiology; environmental health; biostatistics; vaccine

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