Ó 2014 Eur J Oral Sci
Eur J Oral Sci 2014; 122: 210–215 DOI: 10.1111/eos.12124 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Food insecurity and dental caries in schoolchildren: a cross-sectional survey in the western Brazilian Amazon
~o1, Maria H. D. Benicio2, Paulo Fraza Paulo C. Narvai1, Marly A. Cardoso2,3 1
Department of Public Health Practice, School ~o Paulo, Sa ~o of Public Health, University of Sa Paulo; 2Department of Nutrition, School of ~o Paulo, Sa ~o Public Health, University of Sa Paulo, Brazil; 3David Rockefeller Center for Latin American Studies, Harvard University, Cambridge, MA, USA
Fraz~ ao P, Benicio MHD, Narvai PC, Cardoso MA. Food insecurity and dental caries in schoolchildren: a cross-sectional survey in the western Brazilian Amazon. Eur J Oral Sci 2014; 122: 210–215. © 2014 Eur J Oral Sci We analyzed the association between food insecurity and dental caries in 7- to 9-yrold schoolchildren. We performed a cross-sectional survey nested in a populationbased cohort study of 203 schoolchildren. The participants lived in the urban area of a small town within the western Brazilian Amazon. Dental examinations were performed according to criteria recommended by the World Health Organization. The number of decayed deciduous and permanent teeth as a count variable was the outcome measure. Socio–economic status, food security, behavioral variables, and child nutritional status, measured by Z-score for body mass index (BMI), were investigated, and robust Poisson regression models were used. The results showed a mean (SD) of 3.63 (3.26) teeth affected by untreated caries. Approximately 80% of schoolchildren had at least one untreated decayed tooth, and nearly 60% lived in food-insecure households. Sex, household wealth index, mother’s education level, and food-insecurity scores were associated with dental caries in the crude analysis. Dental caries was 1.5 times more likely to be associated with high food-insecurity scores after adjusting for socio–economic status and sex. A significant dose– response relationship was observed. In conclusion, food insecurity is highly associated with dental caries in 7- to 9-yr-old children and may be seen as a risk factor. These findings suggest that food-security policies could reduce dental caries.
Dental caries remains the primary oral health problem in several industrialized countries, affecting 60–90% of schoolchildren and most adults. The disease is a major cause of tooth loss and pain that restricts activities in school and at work, and impacts overall quality of life (1). In Brazil, the prevalence rate for caries in 12-yr-old children decreased from 96.3% in 1980 to 68.9% in 2003, probably because of increased access to fluoridated water and toothpaste and changes to public oral health programs to include the use of several forms of topical fluoride. As a result of these improvements, caries is unevenly distributed, with a small proportion of schoolchildren carrying most of the disease burden (2). Most of these children live in underdeveloped, nonfluoridated areas where the poverty rate is high. Many of these areas are located in the Brazilian Amazon, a vast territory of northern Brazil where the population’s oral health has seldom been investigated. Although access to adequate food has been listed in the Universal Declaration of Human Rights since 1948, worldwide more than 150 million preschool children and almost one billion people of all ages experience
~o, Universidade de Sa ~o Paulo, Paulo Fraza de Pu blica, Av Dr Arnaldo, Faculdade de Sau ~o Paulo, Brazil 715, Cep: 01246-904, Sa E-mail: [email protected] Key words: food supply; health policy; oral health; socio–economic factors; vulnerable populations Accepted for publication February 2014
chronic hunger (3). Despite declines in the poverty rate, in 2008, more than 30 million Brazilians were still below the poverty line and exposed to the daily threat of infant malnutrition (4). The 2009 National Household Sample Survey indicated that 40.3% of households in the northern Brazilian region experienced some level of food insecurity. Children living in households with food insecurity have lower nutrition and health indicators (5). Household food security can be defined as access to a diet of sufficient quantity and quality for all household members at all times, linked to socially acceptable ways of maximizing chances for a healthy and active life (6). Food security entails basic human rights to eating habits that respect local cultures and to sanitary standards and nutritional components that enable a long, active, and healthy life. Food insecurity has been considered a marker of economic hardship and of social and health vulnerability. Individuals in food-insecure households are more likely to report multiple chronic conditions, such as nutritional deficiencies, diabetes, hypertension, and heart disease (7).
Food insecurity and dental caries
Measuring food insecurity per se is important for monitoring inequality. However, no research has explored the association between food insecurity and dental caries in schoolchildren. This study aimed to assess whether food insecurity is an associated factor for dental caries in 7- to 9-yr-old children living in the western Brazilian Amazon.
Material and methods The study protocol was approved by the Institutional Review Board of the School of Public Health, University of S~ao Paulo, Brazil (297/2009). It links to a larger research project on health and nutrition conditions at Acre State developed by Sao Paulo University and Acre Federal University whose field activities began with populationbased cross-sectional surveys in 2003 (8). Acrel^andia is more than 100 km from Rio Branco, the capital of Acre State, and borders two Brazilian states (Rond^ onia and Amazonas) and Bolivia. According to the Brazilian Institute for Geography and Statistics, the population in 2009 was estimated to be 11,520 inhabitants, 44.2% of whom lived in urban areas. The main economic activity was agriculture, followed by timber and Brazil nuts. The illiteracy rate was 24.3%, and the Human Development Index score was 0.680, a lower-than-average value compared with that for the country as a whole (0.766) (9). Infant mortality, estimated at 32.96 per 1,000 live births in 2008, was substantially higher than the country average (15.03 per 1,000 live births). Only 30% of the urban population lived in households connected to non-fluoridated public water networks. In the 2003 survey, 332 (99.4%) households, involving a total of 489 children 5 yr of age (15), Z-scores for BMI were calculated, and children were classified in quintiles. The sample size should comprise at least 185 participants in order to detect a difference in rate ratios from 1.26 to 1.54 with exposure frequencies ranging from 10% to 50% at 80% power and a two-tailed level of significance of 0.05. Mean, SD, median, and interquartile values for the number of decayed deciduous and permanent teeth were calculated, and Kruskal–Wallis and Mann–Whitney U-tests were used to identify differences between groups. Crude analyses between the dependent variable and each independent variable were performed, and rate ratios with 95% CI were calculated. Robust Poisson regression with a hierarchical approach was used for entry and selection of variables. The authors assumed four levels of dental-caries determinants: sex, socio–economic status, food insecurity, and nutritional status. We hypothesized that the variables in each level would influence the outcome and that the first level would exert influence on the second, and so on. Variables with P > 0.20 were not included in the adjusted models. Missing values were included as missing-value categories. P-values for trend were calculated for exploring a possible dose–response relationship. The analyses were performed using STATA/SE for Windows, Version 12.1 (Stata, College Station, TX, USA).
Results From the 218 school children examined, 15 were excluded because data on specific variables were missing. Therefore, the final study group was composed of 108 (53.2%) girls and 95 (46.8%) boys. Sixty-seven (33.0%) were 7 yr of age, 76 (37.4%) were 8 yr of age,
212
Fraz~ ao et al. Table 1
A
Descriptive statistics for dental caries*, according to study variables, in a population of 7- to 9-yr-old children from the western Brazilian Amazon (2010) Variables
B
Fig. 1. Percentage distribution of 7- to 9-yr-old children from the Western Brazilian Amazon, 2010, according to untreated decayed deciduous and permanent teeth (dt+DT) score (A) and food-insecurity score (B). (The food-insecurity score is a scale in which a score of zero means a food-secure household and a scale from 1 to 15 corresponds to a family’s experience in the last 3 months related to insufficient access to food: from worrying about running out of food to the possibility of going without food for a whole day. Increasing values mean worsening access).
and 60 (29.6%) were 9 yr of age. The distribution of children according to untreated caries and food-security scores is presented in Fig. 1. The percentage of cariesfree children was 20.7%. Approximately 80% of schoolchildren had at least one untreated decayed tooth, and nearly 60% lived in households that registered one or more issues with food insecurity. A mean (SD) of 3.63 (3.26) deciduous and permanent teeth were affected by untreated caries, with no apparent statistically significant differences among ages (Table 1). In our study population, 26.1% of the children had mothers with fewer than 4 yr of education. Approximately 20% of the children brushed their teeth less than twice per day and lived in families whose food insecurity score was >4. Wealth Index is presented in terciles, and child nutritional status (measured using the Z-score for BMI) is presented in quintiles (Table 1). Except for age and toothbrushing frequency, the P-value was ≤0.20 for all explanatory variables. Table 2 shows group stratified crude and adjusted effects of various independent variables. Boys presented a higher caries rate than did girls (P = 0.032). In crude analysis, having a score of >4 for food insecurity (P = 0.002) was positively associated with untreated caries, whereas the upper tertile of wealth index (P = 0.038), mother’s education >7 yr (P = 0.049), and upper quintile of Z-scores for BMI were negatively
n
%
Sex Female 108 53.2 Male 95 46.8 Age (yr) 7 yr 67 33.0 8 yr 76 37.4 9 yr 60 29.6 Wealth Index (terciles) Lower tercile 66 34.2 Second 63 32.6 Upper tercile 64 33.2 Mother schooling (yr) 7 yr 80 42.6 Food insecurity score 0 85 45.9 1–4 60 32.4 >4 40 21.6 Toothbrushing per day 2 58 31.9 Z-score for BMI (in quintiles) Lower quintile 38 19.9 Second quintile 38 19.9 Third quintile 39 20.4 Fourth quintile 38 19.9 Upper quintile 38 19.9
Mean (SD)
Median
IQV
P
3.18 (2.92) 4.15 (3.55)
3.0 3.0
1–5 1–6
0.036†
3.82 (3.64) 3.25 (2.79) 3.90 (3.36)
3.0 3.0 3.5
1–6 1–5 1–6
0.629‡
4.09 (3.86) 3.94 (2.71) 2.80 (3.19)
4.0 4.0 2.0
1–6 2–5 0–5
0.016‡
4.33 (3.45) 3.49 (3.79) 3.21 (2.89)
4.0 3.0 3.0
2–7 0–5 1–5
0.157‡
2.98 (2.86) 3.40 (3.38) 4.85 (3.61)
3.0 3.0 5.0
0–5 1–5 2–7
0.015‡
3.74 (3.60) 3.69 (3.22) 3.41 (3.24)
3.0 3.0 3.0
1–5 0–6 1–5
0.841‡
4.53 3.32 3.82 3.66 2.84
4.0 3.0 3.0 3.0 1.5
2–6 1–6 1–6 1–5 0–4
0.205‡
(3.70) (2.90) (3.29) (3.49) (3.20)
IQV, interquartile values. *Untreated decayed deciduous and permanent teeth. †Mann–Whitney U-test. ‡Kruskall–Wallis test.
associated with untreated caries (P = 0.037). Mother’s education was highly correlated with wealth index, which is why the two multiple models were separately adjusted. A dose–response relationship was indicated between untreated caries and level of wealth index (P for trend = 0.037) and food insecurity (P for trend = 0.037). Mother’s education reached a borderline value (P = 0.057). Various adjustments did not significantly affect these results (Table 2). Adjusting for sex, a high level of maternal education was negatively associated with dental caries [relative risk (RR) = 0.74; P = 0.045] in Model 1 and children living in households from the upper tertile of the wealth index had less caries experience compared with the lower tertile (RR = 0.66, P = 0.024) in Model 2. In both models, high food-insecurity scores increased, by 1.5-times, the probability for dental caries adjusted by sex and variables related to socio–economic status. In the Model 1, weighted for earlier variables, caries experience was 37% lower for the upper quintile compared with the lower quintile of the Z-score for BMI (P = 0.050). P-values for trend were statistically significant for mother schooling (P = 0.053), for wealth index (P = 0.022), and for food insecurity (P = 0.043).
Food insecurity and dental caries
213
Table 2 Sex, socio–economic status, household access to food, and child nutritional status: crude and adjusted hierarchical analysis for dental caries* in a sample of 203, 7- to 9-yr-old children from the western Brazilian Amazon (2010) according to robust Poisson regression Model 1†
Crude values
Model 2†
Exposure
RR
95% CI
P
RR
95% CI
RR
95% CI
Sex (girls as reference) Wealth Index‡ Lower tercile Second tercile Upper tercile Mother schooling (yr)§ 7 yr Food-insecurity score** 0 1–4 >4 Z-score for BMI Lower quintile Second quintile Third quintile Fourth quintile Upper quintile
1.31
1.02–1.67
0.032
1.31
1.02–1.67
1.31
1.02–1.67
0.032
Ref. 0.96 0.68
0.72–1.28 0.48–0.98
0.790 0.038
Ref. 0.94 0.66
0.71–1.25 0.46–0.95
0.684 0.024¶
Ref. 0.81 0.74
0.57–1.15 0.55–0.99
0.234 0.049
Ref. 0.80 0.74
0.57–1.13 0.56–0.99
0.211 0.045¶
Ref. 1.14 1.63
0.83–1.58 1.20–2.21
0.419 0.002
Ref. 1.13 1.53
0.82–1.55 1.07–2.21
0.447 0.021††
Ref. 1.10 1.48
0.81–1.50 1.05–2.08
0.548 0.024‡‡
Ref. 0.73 0.84 0.81 0.63
0.50–1.07 0.58–1.22 0.54–1.20 0.41–0.97
0.105 0.370 0.290 0.037
Ref. 0.71 0.82 0.77 0.63
0.48–1.04 0.54–1.24 0.53–1.13 0.40–1.13
0.080 0.338 0.179 0.050§§
Ref. 0.70 0.82 0.77 0.65
0.48–1.02 0.56–1.21 0.53–1.12 0.41–1.02
0.067 0.319 0.172 0.059§§
P 0.032
P
BMI, body mass index; Ref., reference; RR, relative risk. *Untreated decayed deciduous and permanent teeth. †Adjusted values of rate ratio. ‡ To indicate that the variable Wealth Index was not included in the model 1. § To indicate that the variable Mother Schooling was not included in the model 2. ¶ Adjusted by sex. **Index related to household access to food – increasing values mean worsening access. ††Adjusted by sex and mother schooling. ‡‡Adjusted by sex and wealth index. §§Adjusted by earlier variables.
Discussion The association between food insecurity and dental caries was investigated. Boys presented a higher caries burden compared with girls, a difference also observed in other areas of Brazil (16). A high level of maternal education was a protective factor after adjustment for sex. The main finding was the association between high scores of food insecurity and caries rates after adjustment for variables related to socio-economic status and sex. Some investigations identified inequalities in caries experience according to socio–economic status (17, 18). ANTUNES et al. (19) reported correlations between caries and household factors, such as income and number of dwellers per bedroom. PERES et al. (20) and WIGEN & WANG (21) observed the effect of low parental education. This is the first study of dental caries and food security in 7- to 9-yr-old schoolchildren within a nonfluoridated area in which the value of Human Development Index is medium (e.g. higher than 0.49 but lower than 0.80). Earlier research in this subject investigated the use of dental services by children from New Zealand and self-reported oral health measures for members of the working poor Canadians (7, 22–24).
A main finding in the present study was the association between high scores of food insecurity and caries rates. Thus, dental caries scores were 1.5-times higher when associated with high scores of food insecurity, controlling for differences related to socio–economic status and sex. One possible explanation is that households with one or more issues of food insecurity are associated with reduced quality and variety of diet (7). As food-insecurity scores increased, individuals would typically consume fewer dairy products and fruits and vegetables, and higher levels of carbohydrate-based foods containing large amounts of added sugars. Food insecurity can also be connected to lack of availability of healthy food stores in rural and poor neighborhoods, increasing the risk for consumption of cariesassociated items (25). Other possible explanations are connected to poverty. The relationship between food insecurity and income/ poverty is well documented in the literature (5), and poverty is an acknowledged determinant of dental caries (1). We observed a high correlation between maternal education and wealth index, a composite measure related to the family’s accumulated income. According to many reports in the literature, variables related to socio–economic status remain major predictors for dental caries.
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Fraz~ ao et al.
Socio–economic status, maternal education, toothbrushing frequency, and nutritional status were considered in the study design. The fact that our study was nested in a population-based cohort allowed us to use data obtained during the children’s lives, controlling for memory bias. Moreover, the study was undertaken in a county in the Brazilian Amazon, a vast territory in which the population’s oral health has been little investigated. The choice of the sum of untreated decayed deciduous and permanent teeth as the primary outcome allowed a stable parameter to be obtained (i.e. not dependent on age) and the avoidance of many observations with zero-value caries, a common pattern in the permanent dentition of 7- to 9-yr-old children. A limitation involves the population size, which is unlikely to identify statistically significant rate ratios lower than 1.26. Another restriction refers to the assumption that food insecurity had existed over the same time period as caries developed. Thus, as foodinsecurity data were obtained 2 yr before caries scoring, neither an overlap in time nor a causal relationship can be assured, but it is highly unlikely that the food-security situation had changed over such a short period of time. In addition, caries development is a process that normally does not lead to open cavities in a short period of time. Reduced caries experience was observed in children from the upper quintile of Z-scores for BMI in the crude analysis and in Model 2. The relationship between nutritional status and dental caries is controversial. Some claim that being overweight is linked to caries (26), whereas others report that caries is more common in underweight children (27, 28). These associations may not be contradictory, as both under- and over-nutrition in children generally result in inappropriate feeding practices and dietary behaviors associated with limited access to fresh, nutrient-dense foods, with intake rather of high-energy, low-cost and nutrientpoor sugary and fatty foods (25). In addition, other factors, such as an imbalance between energy intake and energy used/physical activity, also play a major role. Although obesity has become a major public health problem worldwide, it seems important to acknowledge within-country inequities affecting child populations from low- to middle-income countries (29), in spite of their overall emergent economic development. In conclusion, after adjusting for socio–economic status and sex, food insecurity was found to be an associated factor for dental caries. These findings can help policymakers plan further interventions to control dental caries in Amazonian children and in children in numerous other areas in the world. Food-security policies could reduce dental caries. Acknowledgements – We are grateful to the National Council for Research and Scientific Technological Development (CNPq-Brazil Grant 402260/2008-2). We also thank Prof. Jaime A. Cury from the State University of Campinas who coordinated the laboratory responsible for fluoride testing of samples from public water networks, and Doroti Elisabete D’Aquino Benicio who performed
the dental examinations. The first author is a researcher from CNPq-Brazil (Grant 304251/2012-7) . Conflicts of interest – The authors declare no conflicts of interest.
References 1. PETERSEN PE. The World Oral Health Report 2003: continuous improvement of oral health in the 21st century — the approach of the WHO Global Oral Health Programme. Community Dent Oral Epidemiol 2003; 31: 3–24. ~ P, RONCALLI AG, ANTUNES JL. [Dental 2. NARVAI PC, FRAZAO caries in Brazil: decline, polarization, inequality and social exclusion]. Rev Panam Salud Publica 2006; 19: 385–393. [Portuguese]. 3. FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS. 925 million in chronic hungry worldwide. 14 September 2010, Rome. Available at: http://www.fao.org/news/ story/en/item/45210/icode/ Accessed: Oct-15-2012. 4. ROCHA C. Developments in national policies for food and nutrition security in Brazil. Dev Policy Rev 2009; 27: 51–66. 5. REIS M. Food insecurity and the relationship between household income and children’s health and nutrition in Brazil. Health Econ 2012; 21: 405–427. ^ -ESCAMILLA R, SEGALL-CORREA AM, MARANHA LK, 6. PEREZ L, PANIGASSI G. An adapted verSAMPAIO MFA, MARIN-LEON sion of the U.S. Department of Agriculture Food Insecurity module is a valid tool for assessing household food insecurity in Campinas, Brazil. J Nutr 2004; 134: 1923–1928. ~ C, FIGUEIREDO R, LOCKER D. Oral 7. MUIRHEAD V, QUINONEZ health disparities and food insecurity in working poor Canadians. Community Dent Oral Epidemiol 2009; 37: 294– 304. 8. MUNIZ PT, CASTRO TG, ARAUJO TS, NUNES NB, DA SILVANUNES M, HOFFMANN EH, FERREIRA MU, CARDOSO MA. Child health and nutrition in the Western Brazilian Amazon: population-based surveys in two counties in Acre State. Cad Sa ude P ublica 2007; 23: 1283–1293. ~ es Unidas para o Desenvolvi9. [PNUD] Programa das Nacßo mento. http://www.pnud.org.br/atlas/ranking/IDH-M%2091% 2000%20Ranking%20decrescente%20(pelos%20dados%20de% 202000).htm Accessed on July 28, 2009. 10. CARDOSO MA, SCOPEL KK, MUNIZ PT, VILLAMOR E, FERREIRA MU. Underlying factors associated with anemia in Amazonian children: a population-based, cross-sectional study. PLoS One 2012; 7: e36341. 11. LOURENCß O BH, VILLAMOR E, AUGUSTO RA, CARDOSO MA. Determinants of linear growth from infancy to school-aged years: a population-based follow-up study in urban Amazonian children. BMC Public Health 2012; 12: 265. 12. WORLD HEALTH ORGANIZATION. Oral health surveys. Geneva: WHO; 1997. 13. FILMER D, PRITCHETT LH. Estimating wealth effects without expenditure data-or tear: an application to educational enrolments in states of India. Demography 2001; 38: 115–132. 14. LOURENCß O BH, VILLAMOR E, AUGUSTO RA, CARDOSO MA. Influence of early life factors on body mass index trajectory during childhood: a population-based longitudinal analysis in the Western Brazilian Amazon. Matern Child Nutr 2012; 1. doi: 10.1111/mcn.12005. [Epub ahead of print] 15. DE ONIS M, ONYANGO AW, BORGHI E, SIYAM A, NISHIDA C, SIEKMANN J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007; 85: 660–667. ~ P. Effectiveness of the bucco-lingual technique within 16. FRAZAO a school-based supervised toothbrushing program on preventing caries: a randomized controlled trial. BMC Oral Health 2011; 11: 11. 17. DO LG, SPENCER AJ, SLADE GD, HA DH, HOBERT-THOMSON KF, LIU P. Trend of income-related inequality of child oral health in Australia. J Dent Res 2010; 89: 959–964.
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24. JAMIESON LM, KOOPU PI. Child use of dental services and receipt of dental care in New Zealand. J Paediatr Child Health 2007; 43: 732–739. 25. CONNIE MOBLEY C, MARSHALL TA, MILGROM P, COLDWELL SE. The contribution of dietary factors to dental caries and disparities in caries. Acad Pediatr 2009; 9: 410–414. 26. MARSHALL TA, EICHENBERGER-GILMORE JM, BROFFITT BA, WARREN JJ, LEVY SM. Dental caries and childhood obesity: roles of diet and socioeconomic status. Community Dent Oral Epidemiol 2007; 35: 449–458. € STALIN U, MATSSON L, THORNGREN27. NORBERG C, HALLSTROM JERNECK K, KLINGBERG G. Body mass index (BMI) and dental caries in 5-year-old children from southern Sweden. Community Dent Oral Epidemiol 2012; 40: 315–322. 28. MISHU MP, HOBDELL M, KHAN MH, HUBBARD RM, SABBAH W. Relationship between untreated dental caries and weight and height of 6- to 12-year-old primary school children in Bangladesh. Int J Dent 2013; 2013: 629675. 29. BARROS FC, VICTORA CG, SCHERPBIER R, GWATKIN D. Socioeconomic inequities in the health and nutrition of children in low/middle income countries. Rev Saude Publica 2010; 44: 1–16.
Eur J Oral Sci 2014; 122: 210–215 DOI: 10.1111/eos.12124 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Food insecurity and dental caries in schoolchildren: a cross-sectional survey in the western Brazilian Amazon
~o1, Maria H. D. Benicio2, Paulo Fraza Paulo C. Narvai1, Marly A. Cardoso2,3 1
Department of Public Health Practice, School ~o Paulo, Sa ~o of Public Health, University of Sa Paulo; 2Department of Nutrition, School of ~o Paulo, Sa ~o Public Health, University of Sa Paulo, Brazil; 3David Rockefeller Center for Latin American Studies, Harvard University, Cambridge, MA, USA
Fraz~ ao P, Benicio MHD, Narvai PC, Cardoso MA. Food insecurity and dental caries in schoolchildren: a cross-sectional survey in the western Brazilian Amazon. Eur J Oral Sci 2014; 122: 210–215. © 2014 Eur J Oral Sci We analyzed the association between food insecurity and dental caries in 7- to 9-yrold schoolchildren. We performed a cross-sectional survey nested in a populationbased cohort study of 203 schoolchildren. The participants lived in the urban area of a small town within the western Brazilian Amazon. Dental examinations were performed according to criteria recommended by the World Health Organization. The number of decayed deciduous and permanent teeth as a count variable was the outcome measure. Socio–economic status, food security, behavioral variables, and child nutritional status, measured by Z-score for body mass index (BMI), were investigated, and robust Poisson regression models were used. The results showed a mean (SD) of 3.63 (3.26) teeth affected by untreated caries. Approximately 80% of schoolchildren had at least one untreated decayed tooth, and nearly 60% lived in food-insecure households. Sex, household wealth index, mother’s education level, and food-insecurity scores were associated with dental caries in the crude analysis. Dental caries was 1.5 times more likely to be associated with high food-insecurity scores after adjusting for socio–economic status and sex. A significant dose– response relationship was observed. In conclusion, food insecurity is highly associated with dental caries in 7- to 9-yr-old children and may be seen as a risk factor. These findings suggest that food-security policies could reduce dental caries.
Dental caries remains the primary oral health problem in several industrialized countries, affecting 60–90% of schoolchildren and most adults. The disease is a major cause of tooth loss and pain that restricts activities in school and at work, and impacts overall quality of life (1). In Brazil, the prevalence rate for caries in 12-yr-old children decreased from 96.3% in 1980 to 68.9% in 2003, probably because of increased access to fluoridated water and toothpaste and changes to public oral health programs to include the use of several forms of topical fluoride. As a result of these improvements, caries is unevenly distributed, with a small proportion of schoolchildren carrying most of the disease burden (2). Most of these children live in underdeveloped, nonfluoridated areas where the poverty rate is high. Many of these areas are located in the Brazilian Amazon, a vast territory of northern Brazil where the population’s oral health has seldom been investigated. Although access to adequate food has been listed in the Universal Declaration of Human Rights since 1948, worldwide more than 150 million preschool children and almost one billion people of all ages experience
~o, Universidade de Sa ~o Paulo, Paulo Fraza de Pu blica, Av Dr Arnaldo, Faculdade de Sau ~o Paulo, Brazil 715, Cep: 01246-904, Sa E-mail: [email protected] Key words: food supply; health policy; oral health; socio–economic factors; vulnerable populations Accepted for publication February 2014
chronic hunger (3). Despite declines in the poverty rate, in 2008, more than 30 million Brazilians were still below the poverty line and exposed to the daily threat of infant malnutrition (4). The 2009 National Household Sample Survey indicated that 40.3% of households in the northern Brazilian region experienced some level of food insecurity. Children living in households with food insecurity have lower nutrition and health indicators (5). Household food security can be defined as access to a diet of sufficient quantity and quality for all household members at all times, linked to socially acceptable ways of maximizing chances for a healthy and active life (6). Food security entails basic human rights to eating habits that respect local cultures and to sanitary standards and nutritional components that enable a long, active, and healthy life. Food insecurity has been considered a marker of economic hardship and of social and health vulnerability. Individuals in food-insecure households are more likely to report multiple chronic conditions, such as nutritional deficiencies, diabetes, hypertension, and heart disease (7).
Food insecurity and dental caries
Measuring food insecurity per se is important for monitoring inequality. However, no research has explored the association between food insecurity and dental caries in schoolchildren. This study aimed to assess whether food insecurity is an associated factor for dental caries in 7- to 9-yr-old children living in the western Brazilian Amazon.
Material and methods The study protocol was approved by the Institutional Review Board of the School of Public Health, University of S~ao Paulo, Brazil (297/2009). It links to a larger research project on health and nutrition conditions at Acre State developed by Sao Paulo University and Acre Federal University whose field activities began with populationbased cross-sectional surveys in 2003 (8). Acrel^andia is more than 100 km from Rio Branco, the capital of Acre State, and borders two Brazilian states (Rond^ onia and Amazonas) and Bolivia. According to the Brazilian Institute for Geography and Statistics, the population in 2009 was estimated to be 11,520 inhabitants, 44.2% of whom lived in urban areas. The main economic activity was agriculture, followed by timber and Brazil nuts. The illiteracy rate was 24.3%, and the Human Development Index score was 0.680, a lower-than-average value compared with that for the country as a whole (0.766) (9). Infant mortality, estimated at 32.96 per 1,000 live births in 2008, was substantially higher than the country average (15.03 per 1,000 live births). Only 30% of the urban population lived in households connected to non-fluoridated public water networks. In the 2003 survey, 332 (99.4%) households, involving a total of 489 children 5 yr of age (15), Z-scores for BMI were calculated, and children were classified in quintiles. The sample size should comprise at least 185 participants in order to detect a difference in rate ratios from 1.26 to 1.54 with exposure frequencies ranging from 10% to 50% at 80% power and a two-tailed level of significance of 0.05. Mean, SD, median, and interquartile values for the number of decayed deciduous and permanent teeth were calculated, and Kruskal–Wallis and Mann–Whitney U-tests were used to identify differences between groups. Crude analyses between the dependent variable and each independent variable were performed, and rate ratios with 95% CI were calculated. Robust Poisson regression with a hierarchical approach was used for entry and selection of variables. The authors assumed four levels of dental-caries determinants: sex, socio–economic status, food insecurity, and nutritional status. We hypothesized that the variables in each level would influence the outcome and that the first level would exert influence on the second, and so on. Variables with P > 0.20 were not included in the adjusted models. Missing values were included as missing-value categories. P-values for trend were calculated for exploring a possible dose–response relationship. The analyses were performed using STATA/SE for Windows, Version 12.1 (Stata, College Station, TX, USA).
Results From the 218 school children examined, 15 were excluded because data on specific variables were missing. Therefore, the final study group was composed of 108 (53.2%) girls and 95 (46.8%) boys. Sixty-seven (33.0%) were 7 yr of age, 76 (37.4%) were 8 yr of age,
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Fraz~ ao et al. Table 1
A
Descriptive statistics for dental caries*, according to study variables, in a population of 7- to 9-yr-old children from the western Brazilian Amazon (2010) Variables
B
Fig. 1. Percentage distribution of 7- to 9-yr-old children from the Western Brazilian Amazon, 2010, according to untreated decayed deciduous and permanent teeth (dt+DT) score (A) and food-insecurity score (B). (The food-insecurity score is a scale in which a score of zero means a food-secure household and a scale from 1 to 15 corresponds to a family’s experience in the last 3 months related to insufficient access to food: from worrying about running out of food to the possibility of going without food for a whole day. Increasing values mean worsening access).
and 60 (29.6%) were 9 yr of age. The distribution of children according to untreated caries and food-security scores is presented in Fig. 1. The percentage of cariesfree children was 20.7%. Approximately 80% of schoolchildren had at least one untreated decayed tooth, and nearly 60% lived in households that registered one or more issues with food insecurity. A mean (SD) of 3.63 (3.26) deciduous and permanent teeth were affected by untreated caries, with no apparent statistically significant differences among ages (Table 1). In our study population, 26.1% of the children had mothers with fewer than 4 yr of education. Approximately 20% of the children brushed their teeth less than twice per day and lived in families whose food insecurity score was >4. Wealth Index is presented in terciles, and child nutritional status (measured using the Z-score for BMI) is presented in quintiles (Table 1). Except for age and toothbrushing frequency, the P-value was ≤0.20 for all explanatory variables. Table 2 shows group stratified crude and adjusted effects of various independent variables. Boys presented a higher caries rate than did girls (P = 0.032). In crude analysis, having a score of >4 for food insecurity (P = 0.002) was positively associated with untreated caries, whereas the upper tertile of wealth index (P = 0.038), mother’s education >7 yr (P = 0.049), and upper quintile of Z-scores for BMI were negatively
n
%
Sex Female 108 53.2 Male 95 46.8 Age (yr) 7 yr 67 33.0 8 yr 76 37.4 9 yr 60 29.6 Wealth Index (terciles) Lower tercile 66 34.2 Second 63 32.6 Upper tercile 64 33.2 Mother schooling (yr) 7 yr 80 42.6 Food insecurity score 0 85 45.9 1–4 60 32.4 >4 40 21.6 Toothbrushing per day 2 58 31.9 Z-score for BMI (in quintiles) Lower quintile 38 19.9 Second quintile 38 19.9 Third quintile 39 20.4 Fourth quintile 38 19.9 Upper quintile 38 19.9
Mean (SD)
Median
IQV
P
3.18 (2.92) 4.15 (3.55)
3.0 3.0
1–5 1–6
0.036†
3.82 (3.64) 3.25 (2.79) 3.90 (3.36)
3.0 3.0 3.5
1–6 1–5 1–6
0.629‡
4.09 (3.86) 3.94 (2.71) 2.80 (3.19)
4.0 4.0 2.0
1–6 2–5 0–5
0.016‡
4.33 (3.45) 3.49 (3.79) 3.21 (2.89)
4.0 3.0 3.0
2–7 0–5 1–5
0.157‡
2.98 (2.86) 3.40 (3.38) 4.85 (3.61)
3.0 3.0 5.0
0–5 1–5 2–7
0.015‡
3.74 (3.60) 3.69 (3.22) 3.41 (3.24)
3.0 3.0 3.0
1–5 0–6 1–5
0.841‡
4.53 3.32 3.82 3.66 2.84
4.0 3.0 3.0 3.0 1.5
2–6 1–6 1–6 1–5 0–4
0.205‡
(3.70) (2.90) (3.29) (3.49) (3.20)
IQV, interquartile values. *Untreated decayed deciduous and permanent teeth. †Mann–Whitney U-test. ‡Kruskall–Wallis test.
associated with untreated caries (P = 0.037). Mother’s education was highly correlated with wealth index, which is why the two multiple models were separately adjusted. A dose–response relationship was indicated between untreated caries and level of wealth index (P for trend = 0.037) and food insecurity (P for trend = 0.037). Mother’s education reached a borderline value (P = 0.057). Various adjustments did not significantly affect these results (Table 2). Adjusting for sex, a high level of maternal education was negatively associated with dental caries [relative risk (RR) = 0.74; P = 0.045] in Model 1 and children living in households from the upper tertile of the wealth index had less caries experience compared with the lower tertile (RR = 0.66, P = 0.024) in Model 2. In both models, high food-insecurity scores increased, by 1.5-times, the probability for dental caries adjusted by sex and variables related to socio–economic status. In the Model 1, weighted for earlier variables, caries experience was 37% lower for the upper quintile compared with the lower quintile of the Z-score for BMI (P = 0.050). P-values for trend were statistically significant for mother schooling (P = 0.053), for wealth index (P = 0.022), and for food insecurity (P = 0.043).
Food insecurity and dental caries
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Table 2 Sex, socio–economic status, household access to food, and child nutritional status: crude and adjusted hierarchical analysis for dental caries* in a sample of 203, 7- to 9-yr-old children from the western Brazilian Amazon (2010) according to robust Poisson regression Model 1†
Crude values
Model 2†
Exposure
RR
95% CI
P
RR
95% CI
RR
95% CI
Sex (girls as reference) Wealth Index‡ Lower tercile Second tercile Upper tercile Mother schooling (yr)§ 7 yr Food-insecurity score** 0 1–4 >4 Z-score for BMI Lower quintile Second quintile Third quintile Fourth quintile Upper quintile
1.31
1.02–1.67
0.032
1.31
1.02–1.67
1.31
1.02–1.67
0.032
Ref. 0.96 0.68
0.72–1.28 0.48–0.98
0.790 0.038
Ref. 0.94 0.66
0.71–1.25 0.46–0.95
0.684 0.024¶
Ref. 0.81 0.74
0.57–1.15 0.55–0.99
0.234 0.049
Ref. 0.80 0.74
0.57–1.13 0.56–0.99
0.211 0.045¶
Ref. 1.14 1.63
0.83–1.58 1.20–2.21
0.419 0.002
Ref. 1.13 1.53
0.82–1.55 1.07–2.21
0.447 0.021††
Ref. 1.10 1.48
0.81–1.50 1.05–2.08
0.548 0.024‡‡
Ref. 0.73 0.84 0.81 0.63
0.50–1.07 0.58–1.22 0.54–1.20 0.41–0.97
0.105 0.370 0.290 0.037
Ref. 0.71 0.82 0.77 0.63
0.48–1.04 0.54–1.24 0.53–1.13 0.40–1.13
0.080 0.338 0.179 0.050§§
Ref. 0.70 0.82 0.77 0.65
0.48–1.02 0.56–1.21 0.53–1.12 0.41–1.02
0.067 0.319 0.172 0.059§§
P 0.032
P
BMI, body mass index; Ref., reference; RR, relative risk. *Untreated decayed deciduous and permanent teeth. †Adjusted values of rate ratio. ‡ To indicate that the variable Wealth Index was not included in the model 1. § To indicate that the variable Mother Schooling was not included in the model 2. ¶ Adjusted by sex. **Index related to household access to food – increasing values mean worsening access. ††Adjusted by sex and mother schooling. ‡‡Adjusted by sex and wealth index. §§Adjusted by earlier variables.
Discussion The association between food insecurity and dental caries was investigated. Boys presented a higher caries burden compared with girls, a difference also observed in other areas of Brazil (16). A high level of maternal education was a protective factor after adjustment for sex. The main finding was the association between high scores of food insecurity and caries rates after adjustment for variables related to socio-economic status and sex. Some investigations identified inequalities in caries experience according to socio–economic status (17, 18). ANTUNES et al. (19) reported correlations between caries and household factors, such as income and number of dwellers per bedroom. PERES et al. (20) and WIGEN & WANG (21) observed the effect of low parental education. This is the first study of dental caries and food security in 7- to 9-yr-old schoolchildren within a nonfluoridated area in which the value of Human Development Index is medium (e.g. higher than 0.49 but lower than 0.80). Earlier research in this subject investigated the use of dental services by children from New Zealand and self-reported oral health measures for members of the working poor Canadians (7, 22–24).
A main finding in the present study was the association between high scores of food insecurity and caries rates. Thus, dental caries scores were 1.5-times higher when associated with high scores of food insecurity, controlling for differences related to socio–economic status and sex. One possible explanation is that households with one or more issues of food insecurity are associated with reduced quality and variety of diet (7). As food-insecurity scores increased, individuals would typically consume fewer dairy products and fruits and vegetables, and higher levels of carbohydrate-based foods containing large amounts of added sugars. Food insecurity can also be connected to lack of availability of healthy food stores in rural and poor neighborhoods, increasing the risk for consumption of cariesassociated items (25). Other possible explanations are connected to poverty. The relationship between food insecurity and income/ poverty is well documented in the literature (5), and poverty is an acknowledged determinant of dental caries (1). We observed a high correlation between maternal education and wealth index, a composite measure related to the family’s accumulated income. According to many reports in the literature, variables related to socio–economic status remain major predictors for dental caries.
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Fraz~ ao et al.
Socio–economic status, maternal education, toothbrushing frequency, and nutritional status were considered in the study design. The fact that our study was nested in a population-based cohort allowed us to use data obtained during the children’s lives, controlling for memory bias. Moreover, the study was undertaken in a county in the Brazilian Amazon, a vast territory in which the population’s oral health has been little investigated. The choice of the sum of untreated decayed deciduous and permanent teeth as the primary outcome allowed a stable parameter to be obtained (i.e. not dependent on age) and the avoidance of many observations with zero-value caries, a common pattern in the permanent dentition of 7- to 9-yr-old children. A limitation involves the population size, which is unlikely to identify statistically significant rate ratios lower than 1.26. Another restriction refers to the assumption that food insecurity had existed over the same time period as caries developed. Thus, as foodinsecurity data were obtained 2 yr before caries scoring, neither an overlap in time nor a causal relationship can be assured, but it is highly unlikely that the food-security situation had changed over such a short period of time. In addition, caries development is a process that normally does not lead to open cavities in a short period of time. Reduced caries experience was observed in children from the upper quintile of Z-scores for BMI in the crude analysis and in Model 2. The relationship between nutritional status and dental caries is controversial. Some claim that being overweight is linked to caries (26), whereas others report that caries is more common in underweight children (27, 28). These associations may not be contradictory, as both under- and over-nutrition in children generally result in inappropriate feeding practices and dietary behaviors associated with limited access to fresh, nutrient-dense foods, with intake rather of high-energy, low-cost and nutrientpoor sugary and fatty foods (25). In addition, other factors, such as an imbalance between energy intake and energy used/physical activity, also play a major role. Although obesity has become a major public health problem worldwide, it seems important to acknowledge within-country inequities affecting child populations from low- to middle-income countries (29), in spite of their overall emergent economic development. In conclusion, after adjusting for socio–economic status and sex, food insecurity was found to be an associated factor for dental caries. These findings can help policymakers plan further interventions to control dental caries in Amazonian children and in children in numerous other areas in the world. Food-security policies could reduce dental caries. Acknowledgements – We are grateful to the National Council for Research and Scientific Technological Development (CNPq-Brazil Grant 402260/2008-2). We also thank Prof. Jaime A. Cury from the State University of Campinas who coordinated the laboratory responsible for fluoride testing of samples from public water networks, and Doroti Elisabete D’Aquino Benicio who performed
the dental examinations. The first author is a researcher from CNPq-Brazil (Grant 304251/2012-7) . Conflicts of interest – The authors declare no conflicts of interest.
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