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Low-mineral direct drinking water in school may retard height growth and increase dental caries in schoolchildren in China
Environment International 115 (2018) 104–109
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Low-mineral direct drinking water in school may retard height growth and increase dental caries in schoolchildren in China
T
Yujing Huanga, Jia Wanga, Yao Tana, Lingqiao Wanga, Hui Linb, Lan Lanc, Yu Xiongd, ⁎ Wei Huangd, Weiqun Shua, a
Department of Environmental Hygiene, College of Preventive Medicine, Army Medical University (Third Military Medical University), Chongqing 400038, PR China Department of Tropical Epidemiology, College of Preventive Medicine, Army Medical University (Third Military Medical University), Chongqing 400038, PR China c Health Supervision Institute of Nan'an, Health and Family Planning Commission of Nan'an, Chongqing 400060, PR China d Department of Stomatology, Southwest Hospital, Army Medical University (Third Military Medical University), Chongqing 400038, PR China b
A R T I C LE I N FO
A B S T R A C T
Handling Editor: Yong Guan Zhu
Although direct drinking water (DDW) systems that utilize a reverse-osmosis technique are thought to be harmful to children's development by reducing their daily mineral intake, few population data are available regarding this topic. We conducted an eco-epidemiological study to investigate the influence of low-mineral DDW on the development of schoolchildren. We collected developmental parameters of 13,723 girls and 16,161 boys before and after the introduction of DDW systems in 25 schools and measured the mineral levels in the DDW of each school. The DDW in 22 schools had lower-than-recommended levels of magnesium and calcium (magnesium, 10 mg/L and calcium, 20 mg/L, WHO). We found that children exposed to low-mineral DDW exhibited reduced height and diminished height increases as well as higher prevalences and incidences of hypoevolutism and dental caries (p < 0.01). This exposure was a risk factor for a greater incidence of both hypoevolutism and dental caries in children (RR = 7.110 (1.688, 29.953) and 1.813 (1.309, 2.509), respectively; p < 0.01). Our results suggest that low-mineral DDW may retard height growth and promote the incidence of dental caries in schoolchildren; thus, schools should choose DDW treatment systems that retain the minerals in water.
Keywords: Direct drinking water systems Mineral content Children Height Dental caries
1. Introduction Schoolchildren nearing puberty are in an important period of bone growth and mineral acquisition (Sowinska-Przepiera et al., 2011; Ward et al., 2014). A sufficient supply of mineral compounds, including calcium, is important for their development. Unfortunately, many studies have shown that the recommended daily intake of minerals is not satisfied via food consumption in children, including in China (Zhang et al., 2013; Zhou et al., 2015). In Chongqing, the calcium intake of children from their diets was only 480 mg ( ± 80 mg) per day (Gu et al., 2012), much lower than the recommendations of Chinese children (1000–1200 mg/d in 7–11 years old children) (Chinese Nutrition Society, 2014). Thus, other sources of calcium are essential to prevent adverse effects induced by a low-calcium diet (Bruvo et al., 2008; Centeno et al., 2009; Joyce et al., 2005; Lee et al., 2008; Madej et al., 2011; Martinez-Ferrer et al., 2008; Rylander, 2008). The calcium present in drinking water should be considered an important means of mineral supplementation for these children, as its bioavailability is
similar to that from dairy products. However, in many area of China, to ensure the quality of classically produced tap water, the government has widely implemented direct drinking water (DDW) systems on school campuses. DDW, also known as fine drinking water, is obtained from municipal tap water using a series of advanced water treatment technologies and can be consumed safely without another treatment. According to our preliminary investigation, reverse-osmosis technology, which almost completely removes minerals as well as harmful substances, is adopted in the majority of DDW systems (Huang et al., 2015). Our study also demonstrated a significant reduction in the mineral levels of DDW, including calcium, in schools that introduced DDW systems (Huang et al., 2015). Drinking low-mineral water can lead to various health risks, including osteopenia (Frantisek, 2005). Our previous study also indicated that low-mineral water was associated skeletal degradation in female rats (Qiu et al., 2015). Since schoolchildren in China spend most of their time at school (> 10 h per day), the DDW they drink at school accounts for a significant proportion of their water consumption. The lack of
Abbreviations:DDW, direct drinking water ⁎ Corresponding author. E-mail address: [email protected] (W. Shu). https://doi.org/10.1016/j.envint.2018.02.021 Received 18 October 2017; Received in revised form 19 January 2018; Accepted 10 February 2018 0160-4120/ © 2018 Elsevier Ltd. All rights reserved.
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Table 1 Distribution of the study subjects. Year recruited
Age (years)
2008
10 11 12 Total 10 11 12 Total 10 11 12 Total 10 11 12 Total
2009
2011
2012
Girls
(n)
Boys
(n)
Total
(n)
Group 1
Group 2
Group 1
Group 2
Group 1
Group 2
89 115 74 278 572 492 71 1135 506 175 179 860 514 469 102 1085
508 571 327 1406 1492 1287 254 3033 1388 531 575 2494 1473 1525 434 3432
119 107 91 317 562 556 142 1260 575 273 310 1158 630 497 188 1315
558 634 450 1642 1593 1421 396 3410 1527 796 793 3116 1577 1689 677 3943
208 222 165 595 1134 1048 213 2395 1081 448 489 2018 1144 966 290 2400
1066 1205 777 3048 3085 2708 650 6443 2915 1327 1368 5610 3050 3214 1111 7375
Table 2 Mineral contents of DDW. Analyte
Group 1 (3 schools) Mean ± SD
Group 2 (22 schools) Mean ± SD (n = 22)
p
Tap water
Calcium (mg/L) Magnesium (mg/L) Sodium (mg/L) Potassium (mg/L) Chlorides (mg/L) Sulfates (mg/L) Fluorides (mg/L) Bicarbonate (mg/L) Hardness (CaCO3, mg/L) Conductivity (μS/cm)a pHb
46.33 ± 6.78 10.09 ± 0.80 12.87 ± 3.81 0.91 ± 0.11 18.00 ± 1.81 50.18 ± 15.11 0.23 ± 0.04 102.03 ± 4.84 145.13 ± 7.43 355.63 ± 84.09 7.65 ± 0.33
3.41 ± 2.38 0.85 ± 0.46 2.27 ± 2.44 0.31 ± 0.31 4.56 ± 4.74 8.47 ± 14.42 0.10 ± 0.07 19.58 ± 12.28 24.49 ± 8.76 53.12 ± 26.64 7.34 ± 0.22
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.035
52.20 12.50 12.70 2.50 16.00 48.20 0.20 161.04 200.30 409 7.57
a b
From 2009 to 2013. From 2009 to 2012.
Table 3 BMI (kg/m2, means ± SD (n)) of children in 2008, 2009, 2011, and 2012. Girls
Boys
Year
Age
Group 1
2008
10 11 12 10 11 12 10 11 12 10 11 12
18.3 18.4 17.6 18.4 18.6 17.7 18.2 17.9 18.5 18.2 18.1 17.8
2009
2011
2012
± ± ± ± ± ± ± ± ± ± ± ±
Group 2 3.3(89) 3.1(115) 3.1(74) 3.2(572) 3.1(492) 2.7(71) 3.2(506) 2.3(175) 3.0(179) 3.0(514) 2.9(469) 2.5(102)
18.6 18.2 18.3 18.6 18.6 18.3 18.2 18.2 18.5 18.1 18.4 18.8
± ± ± ± ± ± ± ± ± ± ± ±
3.2(508) 2.9(571) 3.2(327) 3.2(1492) 3.1(1287) 3.0(254) 3.1(1388) 3.2(531) 3.3(575) 2.9(1473) 3.1(1525) 9.1(434)
p
Group 1
0.330 0.512 0.105 0.270 0.867 0.111 0.897 0.101 0.926 0.715 0.098 0.274
18.4 17.6 18.4 18.6 17.7 18.4 17.9 18.5 18.1 18.1 17.8 18.2
± ± ± ± ± ± ± ± ± ± ± ±
Group 2 3.1(115) 3.1(74) 3.4(119) 3.1(492) 2.7(71) 3.2(562) 2.3(175) 3.0(179) 2.8(575) 2.9(469) 2.5(102) 2.9(630)
18.2 18.3 18.8 18.6 18.3 18.7 18.2 18.5 18.4 18.4 18.8 18.0
± ± ± ± ± ± ± ± ± ± ± ±
p 2.9(571) 3.2(327) 3.3(558) 3.1(1287) 3.0(254) 3.4(1593) 3.2(531) 3.3(575) 3.1(1527) 3.1(1525) 9.1(434) 3.0(1577)
0.512 0.105 0.244 0.867 0.111 0.088 0.101 0.926 0.028 0.098 0.274 0.217
usually is not self-limiting if without proper care. As caries will progress until the tooth is destroyed (Selwitz et al., 2007), it is necessary to clarify its causes. This disease may results from interactions between bacteria and many host factors, including insufficient mineral exposure (Riyat and Sharma, 2010; Selwitz et al., 2007). In DDW, the lack of calcium, which is the major constituent of teeth, and other minerals such as fluoride that are beneficial to dental caries prevention may increase the incidence of dental caries. To investigate the effect of low-mineral DDW on the physical development and dental health of schoolchildren, we selected 25 schools
minerals such as calcium in DDW may result in the loss of minerals obtained from drinking and affect the development of children. Dental caries is one of the most prevalent chronic diseases worldwide. Although people are susceptible to the disease throughout their lifetime, dental caries often arises in childhood as aggressive tooth decay (Selwitz et al., 2007). Dental caries is the primary cause of oral pain and eating difficulty and can even lead to inflammation of the tissue around the tooth, tooth loss, and infection or abscess formation (Laudenbach and Simon, 2014). However, the disease can be arrested and potentially reversed in its early stages (i.e., in childhood) and 105
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2.2. Study design The present study was a five-year eco-epidemiological study aiming to compare the difference in height development and tooth health between children exposed and not exposed to low-mineral DDW. A total of 29,882 Han children (13,723 girls and 16,161 boys) aged 10–12 years were recruited from 25 schools in 2008 (one year before the introduction of DDW system), 2009 (the year the DDW system had been introduced), and 2011 and 2012 (two and three years after the introduction of DDW system) in a district in Chongqing, China (Table 1). These schools had introduced the DDW systems in 2009 and did not change them until September 2013, and their DDW showed small fluctuations in conductivity during these years (2009–2012). All of the studied children were living in an urban area. The children were divided into two groups. In group 1, the children (3558 girls and 4050 boys) were not exposed to low-mineral DDW (from three schools in which the DDW systems did not use reverse osmosis membrane treatment technologies: one used an ultrafiltration membrane (pore size: 0.01 μm) (FY3AUF, Shenzheng water Equipment Co., Ltd., Fuoshan, China) combined with an activated carbon filter, and the other two used an ultrafiltration membrane (pore size: 0.02 μm) (J0-2A, Bili water Equipment Co., Ltd., Fuoshan, China) and the DDW of which was close to municipal tap water in mineral composition). In group 2, the children (10,365 girls and 12,111 boys) were exposed to low-mineral DDW (from 22 schools in which the DDW systems used reverse osmosis membrane treatment technologies: all of them used a reverse osmosis membrane (minimum desalination rate: 99%) (YQS-8040, Hydranautics- A Nitto Group Company, 401 Jones Road, Oceanside, CA, USA) combined with an activated carbon filter), with the mineral content of the DDW being sharply reduced compared to municipal tap water and lower than the levels recommended by the WHO: magnesium, 10 mg/L and calcium, 20 mg/L (World Health Organization, 2005). Developmental parameters, including height, weight, body mass index (BMI) and dental caries in permanent teeth, were collected in the year they had been recruited from the database of children's annual health examinations performed during September to November by the local health inspection bureau. Those data were evaluated by different people in different years and schools. However, all the investigators had undergone uniform training, used the uniform measurement tools which are adjusted annually, and followed the same diagnostic criteria (dental caries). A total of 5601 children (462 and 915 ten-year-old girls, 414 and 875 eleven-year-old girls, 547 and 949 ten-year-old boys, and 439 and 1000 eleven-year-old boys in group 1 and group 2, respectively) had health records for both 2009 and 2012, and their developmental parameters were collected twice (in 2009 and 2012) to evaluate the effect of DDW on their height development and incidence of dental caries and hypoevolutism. Study subjects who had a record of alcohol or tobacco use, bone fracture, development-associated diseases (including rickets, poliomyelitis, digestive system disease and metabolic syndrome), or a family history of these diseases in the annual health examination data were excluded. Height and weight were evaluated by using standard mechanical height and weight scales. The presence of dental caries was determined using a Community Periodontal Index probe according to the caries diagnosis criteria of the WHO Oral Health Surveys Basic Methods 4th edition (World Health Organization, 1997). Growth retardation was identified by hypoevolutism, which was assessed by height (lower than 125.2 cm (boy) and 123.9 cm (girl) for 10year-old children, lower than 129.1 cm (boy) and 128.6 cm (girl) for 11year-old children, and lower than 133.1 cm (boy) and 133.6 cm (girl) for 12-year-old children), according to the screening standard for malnutrition of school-age children and adolescents (National Health and Family Planning Commision of the People's Republic of China, 2014).
Fig. 1. Height (cm, means ± SD (n)) of children in 2008, 2009, 2011, and 2012.
that implemented DDW systems, collected the children's developmental and dental health records (including height, weight and dental caries) before and after the introduction of DDW, and evaluated the health risk of low-mineral DDW exposure in schoolchildren.
2. Materials and methods 2.1. Ethical approval This study was approved by the Ethics Committee of the Third Military Medical University, Chongqing, China. All methods were performed in accordance with the relevant guidelines and regulations of the Third Military Medical University. Informed consent was obtained from all subjects. 106
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The conductivity was detected with a Benchtop Conductivity Meter (hi9932, Hanna Instruments, Inc., Woonsocket, RI, USA). Annual conductivity and pH value data for the DDW were obtained from the routine monitoring records (twice per semester); the conductivity and pH values were determined using a pure water tester (hi98308, Hanna Instruments, Inc., Woonsocket, RI, USA) and pH tester (hi98108, Hanna Instruments, Inc., Woonsocket, RI, USA), respectively. 2.4. Statistical analysis All statistical analyses were performed with SPSS (SPSS Inc. Released 2009. PASW Statistics for Windows, Version 18.0. Chicago: SPSS Inc.). The independent-sample t-test was used to analyze differences in the minerals in the DDW in the two groups of schools and to compare the height and height increase in children between the two groups. Differences in the incidence (during 2009 to 2012) of dental caries and hypoevolutism in children between the two groups were analyzed using the chi-square test. Binary logistic regression was adopted to identify the effect of low-mineral DDW exposure on the incidence (during 2009 to 2012) of dental caries and hypoevolutism. Normal distribution was confirmed by all tests performed with a onesample Kolmogorov-Smirnov test.
Fig. 2. Height increase (mean ± SD) of children during 2009 to 2012.
3. Results 3.1. Minerals in water The water analysis showed that the municipal tap water was abundant in minerals, particularly calcium, magnesium, and bicarbonate, and total hardness (Table 2). However, after treatment with a DDW system, the water showed different mineral levels. The mineral content of DDW in the schools of group 1 was close to that of municipal tap water (Table 2). However, the mineral content of the DDW in the schools of group 2 was sharply decreased compared with tap water (Table 2).
Fig. 3. Prevalence of hypoevolutism in the two groups in 2008, 2009, 2011 and 2012.
3.2. Comparison of height and height increase between the groups There was no significant difference in BMI between the two groups in these years (p > 0.05, Table 3). There was no significant difference in average height between the two groups in 2008 or 2009 (p > 0.05, Fig. 1), but group 2 showed a significantly lower average height than group 1 in 2011 and 2012 (p < 0.01, Fig. 1). Furthermore, the height increase during 2009–2012 was significantly less in group 2 than in group 1 (p < 0.01, Fig. 2). 3.3. Comparison of prevalence and incidence of hypoevolutism and dental caries between the groups Fig. 4. Prevalence of dental caries in the two groups in 2008, 2009, 2011 and 2012.
Regarding the prevalence of hypoevolutism and dental caries, there was no significant difference between the two groups in 2008, 2009 or 2011 (p > 0.05, Figs. 3 and 4). However, group 2 showed a significantly higher prevalence of dental caries than group 1 in 2012 (p < 0.01, Figs. 3 and 4). In addition, the incidence of hypoevolutism and of dental caries during 2009 to 2012 was significantly higher in group 2 than in group 1 (p < 0.01, Fig. 5). Furthermore, the incidence of hypoevolutism and dental caries in these children was positively associated with lower mineral DDW exposure (p < 0.01, Table 4).
2.3. Analysis of minerals in water We collected water samples (including tap water and DDW from 25 primary schools) twice (in October 2012 and May 2013), stored the samples in glass containers at 4 °C, and measured the minerals contained according to standard examination methods for drinking water in China as in our previous studies (Huang et al., 2015; Qiu et al., 2015). Briefly, potassium and sodium were tested using a flame atomic absorption spectrophotometer (TAS-986, Purkinje General Instrument Co., Ltd., Beijing, China), and calcium and magnesium were tested using a flame atomic fluorescence spectrometer (APS-2202E, Haiguang Instrument Co., Ltd., Beijing, China). Bicarbonate was tested using indicator titration; hardness was tested using edetate disodium salt titration; and fluoride, chlorides and sulfates were tested using the ion chromatographic method (SPD-20A, Shimadzu Co., Ltd., Kyoto, Japan).
4. Discussion Although many studies have investigated minerals and childhood development, the majority of these studies have focused on food minerals (World Health Organization, 2013). Thus, few studies have been performed on water minerals, and of these, nearly all focus on highmineral drinking water and its impact on development or the 107
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population was not sufficient (Gu et al., 2012). Although medical calcium supplements are thought to compensate for shortages in daily calcium intake (Huang et al., 2014), these supplements are usually taken once or twice a day, and their administration may inhibit parathyroid hormone and bone resorption more intensely over a short period of time due to the corresponding intake of a large quantity of calcium (Guillemant et al., 2000; Vitoria et al., 2014). Thus, the water consumed throughout the day can be a significant alternative to food to satisfy requirements for this mineral because it results in a more sustained inhibition of bone resorption (Galan et al., 2002; Vitoria et al., 2014). In addition, its deficiency in drinking water may be associated with high risk of fracture in children (Verd Vallespir et al., 1992). Therefore, the shortage of the minerals in drinking water due to a DDW system may aggravate the adverse effects of low daily calcium intake on height growth and dental health in children (Gaucheron, 2011; Madej et al., 2011; Prentice et al., 2012; Ward et al., 2014; Winzenberg et al., 2006). Compared with the acute calcium and magnesium deficiency symptoms induced by drinking pure water in adults (Frantisek, 2005), these adverse effects in children are not as obvious but may be more widespread and serious. There were some limitations to this study. First, other minerals that affect bone development, such as metasilicate and strontium, were not measured, which may have influenced the results. Second, we did not consider pollution of ions such as lead, copper, iron, which can leach from plumbing and affect development because all DDW systems in these schools used a polypropylene materials pipework and the conductivity of the terminal water was much lower. This was our regret and negligence in this study. Third, the personal daily mineral intake from food and water in the study populations was lacking, so the food interaction could not be adequately evaluated. Considering that those students lived in the same area and shared similar daily habits of living, drinking and eating, we assume that their dietary mineral intakes were about the same, and the study by Gu et al. (2012) may confirm this hypothesis to some degree. Nevertheless, this study may provide data to support the adverse effects of drinking low-mineral water in children.
Fig. 5. Incidence of hypoevolutism and dental caries during 2009 to 2012. a Among the children who did not have hypoevolutism in 2009 (822 girls and 892 boys in group 1, 1676 girls and 1749 boys in group 2).
Table 4 Correlations (RR (95% Cl))a between low-mineral DDW exposure and the incidences of hypoevolutism and dental caries in children (2009–2012).
Hypoevolutism Dental caries a
Group 1
Group 2
p
Ref. Ref.
7.110 (1.688, 29.953) 1.813 (1.309, 2.509)
0.008 < 0.001
The rate ratio was analyzed by binary logistic regression and adjusted by gender and
age.
prevention and treatment of disease (Leurs et al., 2010; Poursafa et al., 2014; World Health Organization, 2005). This study reports an association between low-mineral DDW and children's development. Considering that DDW is increasing in popularity, it may become a new public health threat. The majority of DDW samples showed significant decreases in mineral composition compared with tap water. Although only two investigations on mineral content were conducted because the DDW systems were replaced in 2013 and 2014 after we reported a significant decrease in the mineral content in the DDW, the stable annual conductivity records from 2009 to 2012 partially reflected the slight variation in the mineral content in the DDW. Children in the low-mineral group (group 2) showed a marked drop in height and a marked rise in the prevalence of hypoevolutism and dental caries after the introduction of DDW (in 2011 and 2012), which was not found before the introduction of DDW (in 2008 and 2009). Moreover, children in the low-mineral group (group 2) had a lower height increase and higher incidence of hypoevolutism and dental caries after the introduction of DDW (2009–2012). Furthermore, lowmineral DDW exposure was a risk factor for hypoevolutism and dental caries incidence and lower height increase in children after the introduction of DDW systems (2009–2012). These results indicate that the low mineral content of the DDW may retard height development and promote dental caries in children. Considering that DDW accounted for the vast majority of water consumption in schoolchildren, the contribution of minerals from daily water consumption and daily mineral intake may have decreased in the low-mineral group. Although the contribution of minerals from water consumption is only a small proportion of daily mineral intake, it is important for the maintenance of health, especially when its deficiency in food is prevalent (Grandjean and Bartram, 2011). For example, calcium, the major element of hydroxyapatite, which is the inorganic mineral compound of bone, is essential to height growth and dental health (Martin-Bautista et al., 2011), and its intake in our study
5. Conclusions In summary, this study provides independent epidemiological evidence that drinking low-mineral water may retard height development and promote dental caries in schoolchildren. Our results indicate that we should not only consider the protection afforded by DDW in terms of drinking water safety but also monitor its potential adverse effects on the development of children when schools use DDW systems that remove too much of the necessary minerals, such as by reverse-osmosis technology. Campus DDW systems should utilize treatment systems that do not remove the minerals in water, such as acticarbon, ultrafiltration membranes, and disinfection by silver, ozone or ultraviolet radiation. If the reverse-osmosis technology is necessary, a subsequent remineralization, such as filtering through dolomite, should be considered. Acknowledgments This work was supported by the Project of Chongqing Municipal Health Bureau (Grant No. 2012-2-447). Author contributions W.Q.S. conceived the investigation and designed the exposure estimates. Y.J.H. designed the exposure estimates, performed the experiment and statistical analyses, and drafted the manuscript. L.L. and Q.B.Y. made substantial contributions to the data collection. W.H., Y.X. made substantial contributions to the interpretation of the data. Y.T. and L.Q.W. made substantial contributions to performing the experiments. H.L. assisted with and checked the statistical analyses. J.W. assisted with and checked the statistical analyses and modified the manuscript. 108
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Additional informationCompeting interests
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The authors do not have any competing interests to declare. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.envint.2018.02.021. References Bruvo, M., Ekstrand, K., Arvin, E., Spliid, H., Moe, D., Kirkeby, S., Bardow, A., 2008. Optimal drinking water composition for caries control in populations. J. Dent. Res. 87, 340–343. Centeno, V., de Barboza, G.D., Marchionatti, A., Rodriguez, V., Tolosa de Talamoni, N., 2009. Molecular mechanisms triggered by low-calcium diets. Nutr. Res. Rev. 22, 163–174. Chinese Nutrition Society, 2014. Chinese DRIs Handbook (Chinese Edition). Standards Press of China, Beijing. Frantisek, K., 2005. Health risks from drinking demineralised water. In: Water Sanitation and Health Programme (Ed.), Nutrients in Drinking Water. World Health Organization, Geneva, Switzerland, pp. 148–158. Galan, P., Arnaud, M.J., Czernichow, S., Delabroise, A.M., Preziosi, P., Bertrais, S., Franchisseur, C., Maurel, M., Favier, A., Hercberg, S., 2002. Contribution of mineral waters to dietary calcium and magnesium intake in a French adult population. J. Am. Diet. Assoc. 102, 1658–1662. Gaucheron, F., 2011. Milk and dairy products: a unique micronutrient combination. J. Am. Coll. Nutr. 30, 400S–4009S. Grandjean, A.C., Bartram, J.K., 2011. Essential nature of water for health: water as part of the dietary intake for nutrients and the role of water in hygiene. In: Nriagu, J.O. (Ed.), Encyclopedia of Environmental Health. Elsevier, Burlington, pp. 594–604. Gu, Z., Mi, M., Gong, L., Zhang, Q., Zheng, H., Chen, Y., Wu, W., Lang, H., 2012. The food consumption and intake of nutrients in primary and middle school students in Chongqing City. Chin. J. Health Insp. 19, 548–551. Guillemant, J., Le, H.T., Accarie, C., du Montcel, S.T., Delabroise, A.M., Arnaud, M.J., Guillemant, S., 2000. Mineral water as a source of dietary calcium: acute effects on parathyroid function and bone resorption in young men. Am. J. Clin. Nutr. 71, 999–1002. Huang, J., Ou, H.Y., Chiu, K.C., 2014. Calcium supplements and fracture prevention. N. Engl. J. Med. 370, 387. Huang, Y., Lan, L., Yan, Q., Tang, W., Tan, Y., Wang, L., Shu, W., 2015. A survey on the mineral contents and potential renal acid loads in primary and secondary schoolsupplied drinking water in Chongqing. Zhonghua Yu Fang Yi Xue Za Zhi 49, 930–932. Joyce, M., Charles, O., Peter, L., George, H., 2005. The contribution of drinking water to total daily dietary intakes of selected trace mineral nutrients in the United States. In: Water Sanitation and Health Programme (Ed.), Nutrients in Drinking Water. World Health Organization, Geneva, Switzerland, pp. 75–88. Laudenbach, J.M., Simon, Z., 2014. Common dental and periodontal diseases: evaluation and management. Med. Clin. North Am. 98, 1239–1260. Lee, G.S., Byun, H.S., Kim, M.H., Lee, B.M., Ko, S.H., Jung, E.M., Gwak, K.S., Choi, I.G., Kang, H.Y., Jo, H.J., Lee, H.J., Jeung, E.B., 2008. The beneficial effect of the sap of Acer mono in an animal with low-calcium diet-induced osteoporosis-like symptoms. Br. J. Nutr. 100, 1011–1018. Leurs, L.J., Schouten, L.J., Mons, M.N., Goldbohm, R.A., van den Brandt, P.A., 2010. Relationship between tap water hardness, magnesium, and calcium concentration and mortality due to ischemic heart disease or stroke in The Netherlands. Environ.
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Low-mineral direct drinking water in school may retard height growth and increase dental caries in schoolchildren in China
T
Yujing Huanga, Jia Wanga, Yao Tana, Lingqiao Wanga, Hui Linb, Lan Lanc, Yu Xiongd, ⁎ Wei Huangd, Weiqun Shua, a
Department of Environmental Hygiene, College of Preventive Medicine, Army Medical University (Third Military Medical University), Chongqing 400038, PR China Department of Tropical Epidemiology, College of Preventive Medicine, Army Medical University (Third Military Medical University), Chongqing 400038, PR China c Health Supervision Institute of Nan'an, Health and Family Planning Commission of Nan'an, Chongqing 400060, PR China d Department of Stomatology, Southwest Hospital, Army Medical University (Third Military Medical University), Chongqing 400038, PR China b
A R T I C LE I N FO
A B S T R A C T
Handling Editor: Yong Guan Zhu
Although direct drinking water (DDW) systems that utilize a reverse-osmosis technique are thought to be harmful to children's development by reducing their daily mineral intake, few population data are available regarding this topic. We conducted an eco-epidemiological study to investigate the influence of low-mineral DDW on the development of schoolchildren. We collected developmental parameters of 13,723 girls and 16,161 boys before and after the introduction of DDW systems in 25 schools and measured the mineral levels in the DDW of each school. The DDW in 22 schools had lower-than-recommended levels of magnesium and calcium (magnesium, 10 mg/L and calcium, 20 mg/L, WHO). We found that children exposed to low-mineral DDW exhibited reduced height and diminished height increases as well as higher prevalences and incidences of hypoevolutism and dental caries (p < 0.01). This exposure was a risk factor for a greater incidence of both hypoevolutism and dental caries in children (RR = 7.110 (1.688, 29.953) and 1.813 (1.309, 2.509), respectively; p < 0.01). Our results suggest that low-mineral DDW may retard height growth and promote the incidence of dental caries in schoolchildren; thus, schools should choose DDW treatment systems that retain the minerals in water.
Keywords: Direct drinking water systems Mineral content Children Height Dental caries
1. Introduction Schoolchildren nearing puberty are in an important period of bone growth and mineral acquisition (Sowinska-Przepiera et al., 2011; Ward et al., 2014). A sufficient supply of mineral compounds, including calcium, is important for their development. Unfortunately, many studies have shown that the recommended daily intake of minerals is not satisfied via food consumption in children, including in China (Zhang et al., 2013; Zhou et al., 2015). In Chongqing, the calcium intake of children from their diets was only 480 mg ( ± 80 mg) per day (Gu et al., 2012), much lower than the recommendations of Chinese children (1000–1200 mg/d in 7–11 years old children) (Chinese Nutrition Society, 2014). Thus, other sources of calcium are essential to prevent adverse effects induced by a low-calcium diet (Bruvo et al., 2008; Centeno et al., 2009; Joyce et al., 2005; Lee et al., 2008; Madej et al., 2011; Martinez-Ferrer et al., 2008; Rylander, 2008). The calcium present in drinking water should be considered an important means of mineral supplementation for these children, as its bioavailability is
similar to that from dairy products. However, in many area of China, to ensure the quality of classically produced tap water, the government has widely implemented direct drinking water (DDW) systems on school campuses. DDW, also known as fine drinking water, is obtained from municipal tap water using a series of advanced water treatment technologies and can be consumed safely without another treatment. According to our preliminary investigation, reverse-osmosis technology, which almost completely removes minerals as well as harmful substances, is adopted in the majority of DDW systems (Huang et al., 2015). Our study also demonstrated a significant reduction in the mineral levels of DDW, including calcium, in schools that introduced DDW systems (Huang et al., 2015). Drinking low-mineral water can lead to various health risks, including osteopenia (Frantisek, 2005). Our previous study also indicated that low-mineral water was associated skeletal degradation in female rats (Qiu et al., 2015). Since schoolchildren in China spend most of their time at school (> 10 h per day), the DDW they drink at school accounts for a significant proportion of their water consumption. The lack of
Abbreviations:DDW, direct drinking water ⁎ Corresponding author. E-mail address: [email protected] (W. Shu). https://doi.org/10.1016/j.envint.2018.02.021 Received 18 October 2017; Received in revised form 19 January 2018; Accepted 10 February 2018 0160-4120/ © 2018 Elsevier Ltd. All rights reserved.
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Table 1 Distribution of the study subjects. Year recruited
Age (years)
2008
10 11 12 Total 10 11 12 Total 10 11 12 Total 10 11 12 Total
2009
2011
2012
Girls
(n)
Boys
(n)
Total
(n)
Group 1
Group 2
Group 1
Group 2
Group 1
Group 2
89 115 74 278 572 492 71 1135 506 175 179 860 514 469 102 1085
508 571 327 1406 1492 1287 254 3033 1388 531 575 2494 1473 1525 434 3432
119 107 91 317 562 556 142 1260 575 273 310 1158 630 497 188 1315
558 634 450 1642 1593 1421 396 3410 1527 796 793 3116 1577 1689 677 3943
208 222 165 595 1134 1048 213 2395 1081 448 489 2018 1144 966 290 2400
1066 1205 777 3048 3085 2708 650 6443 2915 1327 1368 5610 3050 3214 1111 7375
Table 2 Mineral contents of DDW. Analyte
Group 1 (3 schools) Mean ± SD
Group 2 (22 schools) Mean ± SD (n = 22)
p
Tap water
Calcium (mg/L) Magnesium (mg/L) Sodium (mg/L) Potassium (mg/L) Chlorides (mg/L) Sulfates (mg/L) Fluorides (mg/L) Bicarbonate (mg/L) Hardness (CaCO3, mg/L) Conductivity (μS/cm)a pHb
46.33 ± 6.78 10.09 ± 0.80 12.87 ± 3.81 0.91 ± 0.11 18.00 ± 1.81 50.18 ± 15.11 0.23 ± 0.04 102.03 ± 4.84 145.13 ± 7.43 355.63 ± 84.09 7.65 ± 0.33
3.41 ± 2.38 0.85 ± 0.46 2.27 ± 2.44 0.31 ± 0.31 4.56 ± 4.74 8.47 ± 14.42 0.10 ± 0.07 19.58 ± 12.28 24.49 ± 8.76 53.12 ± 26.64 7.34 ± 0.22
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.035
52.20 12.50 12.70 2.50 16.00 48.20 0.20 161.04 200.30 409 7.57
a b
From 2009 to 2013. From 2009 to 2012.
Table 3 BMI (kg/m2, means ± SD (n)) of children in 2008, 2009, 2011, and 2012. Girls
Boys
Year
Age
Group 1
2008
10 11 12 10 11 12 10 11 12 10 11 12
18.3 18.4 17.6 18.4 18.6 17.7 18.2 17.9 18.5 18.2 18.1 17.8
2009
2011
2012
± ± ± ± ± ± ± ± ± ± ± ±
Group 2 3.3(89) 3.1(115) 3.1(74) 3.2(572) 3.1(492) 2.7(71) 3.2(506) 2.3(175) 3.0(179) 3.0(514) 2.9(469) 2.5(102)
18.6 18.2 18.3 18.6 18.6 18.3 18.2 18.2 18.5 18.1 18.4 18.8
± ± ± ± ± ± ± ± ± ± ± ±
3.2(508) 2.9(571) 3.2(327) 3.2(1492) 3.1(1287) 3.0(254) 3.1(1388) 3.2(531) 3.3(575) 2.9(1473) 3.1(1525) 9.1(434)
p
Group 1
0.330 0.512 0.105 0.270 0.867 0.111 0.897 0.101 0.926 0.715 0.098 0.274
18.4 17.6 18.4 18.6 17.7 18.4 17.9 18.5 18.1 18.1 17.8 18.2
± ± ± ± ± ± ± ± ± ± ± ±
Group 2 3.1(115) 3.1(74) 3.4(119) 3.1(492) 2.7(71) 3.2(562) 2.3(175) 3.0(179) 2.8(575) 2.9(469) 2.5(102) 2.9(630)
18.2 18.3 18.8 18.6 18.3 18.7 18.2 18.5 18.4 18.4 18.8 18.0
± ± ± ± ± ± ± ± ± ± ± ±
p 2.9(571) 3.2(327) 3.3(558) 3.1(1287) 3.0(254) 3.4(1593) 3.2(531) 3.3(575) 3.1(1527) 3.1(1525) 9.1(434) 3.0(1577)
0.512 0.105 0.244 0.867 0.111 0.088 0.101 0.926 0.028 0.098 0.274 0.217
usually is not self-limiting if without proper care. As caries will progress until the tooth is destroyed (Selwitz et al., 2007), it is necessary to clarify its causes. This disease may results from interactions between bacteria and many host factors, including insufficient mineral exposure (Riyat and Sharma, 2010; Selwitz et al., 2007). In DDW, the lack of calcium, which is the major constituent of teeth, and other minerals such as fluoride that are beneficial to dental caries prevention may increase the incidence of dental caries. To investigate the effect of low-mineral DDW on the physical development and dental health of schoolchildren, we selected 25 schools
minerals such as calcium in DDW may result in the loss of minerals obtained from drinking and affect the development of children. Dental caries is one of the most prevalent chronic diseases worldwide. Although people are susceptible to the disease throughout their lifetime, dental caries often arises in childhood as aggressive tooth decay (Selwitz et al., 2007). Dental caries is the primary cause of oral pain and eating difficulty and can even lead to inflammation of the tissue around the tooth, tooth loss, and infection or abscess formation (Laudenbach and Simon, 2014). However, the disease can be arrested and potentially reversed in its early stages (i.e., in childhood) and 105
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2.2. Study design The present study was a five-year eco-epidemiological study aiming to compare the difference in height development and tooth health between children exposed and not exposed to low-mineral DDW. A total of 29,882 Han children (13,723 girls and 16,161 boys) aged 10–12 years were recruited from 25 schools in 2008 (one year before the introduction of DDW system), 2009 (the year the DDW system had been introduced), and 2011 and 2012 (two and three years after the introduction of DDW system) in a district in Chongqing, China (Table 1). These schools had introduced the DDW systems in 2009 and did not change them until September 2013, and their DDW showed small fluctuations in conductivity during these years (2009–2012). All of the studied children were living in an urban area. The children were divided into two groups. In group 1, the children (3558 girls and 4050 boys) were not exposed to low-mineral DDW (from three schools in which the DDW systems did not use reverse osmosis membrane treatment technologies: one used an ultrafiltration membrane (pore size: 0.01 μm) (FY3AUF, Shenzheng water Equipment Co., Ltd., Fuoshan, China) combined with an activated carbon filter, and the other two used an ultrafiltration membrane (pore size: 0.02 μm) (J0-2A, Bili water Equipment Co., Ltd., Fuoshan, China) and the DDW of which was close to municipal tap water in mineral composition). In group 2, the children (10,365 girls and 12,111 boys) were exposed to low-mineral DDW (from 22 schools in which the DDW systems used reverse osmosis membrane treatment technologies: all of them used a reverse osmosis membrane (minimum desalination rate: 99%) (YQS-8040, Hydranautics- A Nitto Group Company, 401 Jones Road, Oceanside, CA, USA) combined with an activated carbon filter), with the mineral content of the DDW being sharply reduced compared to municipal tap water and lower than the levels recommended by the WHO: magnesium, 10 mg/L and calcium, 20 mg/L (World Health Organization, 2005). Developmental parameters, including height, weight, body mass index (BMI) and dental caries in permanent teeth, were collected in the year they had been recruited from the database of children's annual health examinations performed during September to November by the local health inspection bureau. Those data were evaluated by different people in different years and schools. However, all the investigators had undergone uniform training, used the uniform measurement tools which are adjusted annually, and followed the same diagnostic criteria (dental caries). A total of 5601 children (462 and 915 ten-year-old girls, 414 and 875 eleven-year-old girls, 547 and 949 ten-year-old boys, and 439 and 1000 eleven-year-old boys in group 1 and group 2, respectively) had health records for both 2009 and 2012, and their developmental parameters were collected twice (in 2009 and 2012) to evaluate the effect of DDW on their height development and incidence of dental caries and hypoevolutism. Study subjects who had a record of alcohol or tobacco use, bone fracture, development-associated diseases (including rickets, poliomyelitis, digestive system disease and metabolic syndrome), or a family history of these diseases in the annual health examination data were excluded. Height and weight were evaluated by using standard mechanical height and weight scales. The presence of dental caries was determined using a Community Periodontal Index probe according to the caries diagnosis criteria of the WHO Oral Health Surveys Basic Methods 4th edition (World Health Organization, 1997). Growth retardation was identified by hypoevolutism, which was assessed by height (lower than 125.2 cm (boy) and 123.9 cm (girl) for 10year-old children, lower than 129.1 cm (boy) and 128.6 cm (girl) for 11year-old children, and lower than 133.1 cm (boy) and 133.6 cm (girl) for 12-year-old children), according to the screening standard for malnutrition of school-age children and adolescents (National Health and Family Planning Commision of the People's Republic of China, 2014).
Fig. 1. Height (cm, means ± SD (n)) of children in 2008, 2009, 2011, and 2012.
that implemented DDW systems, collected the children's developmental and dental health records (including height, weight and dental caries) before and after the introduction of DDW, and evaluated the health risk of low-mineral DDW exposure in schoolchildren.
2. Materials and methods 2.1. Ethical approval This study was approved by the Ethics Committee of the Third Military Medical University, Chongqing, China. All methods were performed in accordance with the relevant guidelines and regulations of the Third Military Medical University. Informed consent was obtained from all subjects. 106
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The conductivity was detected with a Benchtop Conductivity Meter (hi9932, Hanna Instruments, Inc., Woonsocket, RI, USA). Annual conductivity and pH value data for the DDW were obtained from the routine monitoring records (twice per semester); the conductivity and pH values were determined using a pure water tester (hi98308, Hanna Instruments, Inc., Woonsocket, RI, USA) and pH tester (hi98108, Hanna Instruments, Inc., Woonsocket, RI, USA), respectively. 2.4. Statistical analysis All statistical analyses were performed with SPSS (SPSS Inc. Released 2009. PASW Statistics for Windows, Version 18.0. Chicago: SPSS Inc.). The independent-sample t-test was used to analyze differences in the minerals in the DDW in the two groups of schools and to compare the height and height increase in children between the two groups. Differences in the incidence (during 2009 to 2012) of dental caries and hypoevolutism in children between the two groups were analyzed using the chi-square test. Binary logistic regression was adopted to identify the effect of low-mineral DDW exposure on the incidence (during 2009 to 2012) of dental caries and hypoevolutism. Normal distribution was confirmed by all tests performed with a onesample Kolmogorov-Smirnov test.
Fig. 2. Height increase (mean ± SD) of children during 2009 to 2012.
3. Results 3.1. Minerals in water The water analysis showed that the municipal tap water was abundant in minerals, particularly calcium, magnesium, and bicarbonate, and total hardness (Table 2). However, after treatment with a DDW system, the water showed different mineral levels. The mineral content of DDW in the schools of group 1 was close to that of municipal tap water (Table 2). However, the mineral content of the DDW in the schools of group 2 was sharply decreased compared with tap water (Table 2).
Fig. 3. Prevalence of hypoevolutism in the two groups in 2008, 2009, 2011 and 2012.
3.2. Comparison of height and height increase between the groups There was no significant difference in BMI between the two groups in these years (p > 0.05, Table 3). There was no significant difference in average height between the two groups in 2008 or 2009 (p > 0.05, Fig. 1), but group 2 showed a significantly lower average height than group 1 in 2011 and 2012 (p < 0.01, Fig. 1). Furthermore, the height increase during 2009–2012 was significantly less in group 2 than in group 1 (p < 0.01, Fig. 2). 3.3. Comparison of prevalence and incidence of hypoevolutism and dental caries between the groups Fig. 4. Prevalence of dental caries in the two groups in 2008, 2009, 2011 and 2012.
Regarding the prevalence of hypoevolutism and dental caries, there was no significant difference between the two groups in 2008, 2009 or 2011 (p > 0.05, Figs. 3 and 4). However, group 2 showed a significantly higher prevalence of dental caries than group 1 in 2012 (p < 0.01, Figs. 3 and 4). In addition, the incidence of hypoevolutism and of dental caries during 2009 to 2012 was significantly higher in group 2 than in group 1 (p < 0.01, Fig. 5). Furthermore, the incidence of hypoevolutism and dental caries in these children was positively associated with lower mineral DDW exposure (p < 0.01, Table 4).
2.3. Analysis of minerals in water We collected water samples (including tap water and DDW from 25 primary schools) twice (in October 2012 and May 2013), stored the samples in glass containers at 4 °C, and measured the minerals contained according to standard examination methods for drinking water in China as in our previous studies (Huang et al., 2015; Qiu et al., 2015). Briefly, potassium and sodium were tested using a flame atomic absorption spectrophotometer (TAS-986, Purkinje General Instrument Co., Ltd., Beijing, China), and calcium and magnesium were tested using a flame atomic fluorescence spectrometer (APS-2202E, Haiguang Instrument Co., Ltd., Beijing, China). Bicarbonate was tested using indicator titration; hardness was tested using edetate disodium salt titration; and fluoride, chlorides and sulfates were tested using the ion chromatographic method (SPD-20A, Shimadzu Co., Ltd., Kyoto, Japan).
4. Discussion Although many studies have investigated minerals and childhood development, the majority of these studies have focused on food minerals (World Health Organization, 2013). Thus, few studies have been performed on water minerals, and of these, nearly all focus on highmineral drinking water and its impact on development or the 107
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population was not sufficient (Gu et al., 2012). Although medical calcium supplements are thought to compensate for shortages in daily calcium intake (Huang et al., 2014), these supplements are usually taken once or twice a day, and their administration may inhibit parathyroid hormone and bone resorption more intensely over a short period of time due to the corresponding intake of a large quantity of calcium (Guillemant et al., 2000; Vitoria et al., 2014). Thus, the water consumed throughout the day can be a significant alternative to food to satisfy requirements for this mineral because it results in a more sustained inhibition of bone resorption (Galan et al., 2002; Vitoria et al., 2014). In addition, its deficiency in drinking water may be associated with high risk of fracture in children (Verd Vallespir et al., 1992). Therefore, the shortage of the minerals in drinking water due to a DDW system may aggravate the adverse effects of low daily calcium intake on height growth and dental health in children (Gaucheron, 2011; Madej et al., 2011; Prentice et al., 2012; Ward et al., 2014; Winzenberg et al., 2006). Compared with the acute calcium and magnesium deficiency symptoms induced by drinking pure water in adults (Frantisek, 2005), these adverse effects in children are not as obvious but may be more widespread and serious. There were some limitations to this study. First, other minerals that affect bone development, such as metasilicate and strontium, were not measured, which may have influenced the results. Second, we did not consider pollution of ions such as lead, copper, iron, which can leach from plumbing and affect development because all DDW systems in these schools used a polypropylene materials pipework and the conductivity of the terminal water was much lower. This was our regret and negligence in this study. Third, the personal daily mineral intake from food and water in the study populations was lacking, so the food interaction could not be adequately evaluated. Considering that those students lived in the same area and shared similar daily habits of living, drinking and eating, we assume that their dietary mineral intakes were about the same, and the study by Gu et al. (2012) may confirm this hypothesis to some degree. Nevertheless, this study may provide data to support the adverse effects of drinking low-mineral water in children.
Fig. 5. Incidence of hypoevolutism and dental caries during 2009 to 2012. a Among the children who did not have hypoevolutism in 2009 (822 girls and 892 boys in group 1, 1676 girls and 1749 boys in group 2).
Table 4 Correlations (RR (95% Cl))a between low-mineral DDW exposure and the incidences of hypoevolutism and dental caries in children (2009–2012).
Hypoevolutism Dental caries a
Group 1
Group 2
p
Ref. Ref.
7.110 (1.688, 29.953) 1.813 (1.309, 2.509)
0.008 < 0.001
The rate ratio was analyzed by binary logistic regression and adjusted by gender and
age.
prevention and treatment of disease (Leurs et al., 2010; Poursafa et al., 2014; World Health Organization, 2005). This study reports an association between low-mineral DDW and children's development. Considering that DDW is increasing in popularity, it may become a new public health threat. The majority of DDW samples showed significant decreases in mineral composition compared with tap water. Although only two investigations on mineral content were conducted because the DDW systems were replaced in 2013 and 2014 after we reported a significant decrease in the mineral content in the DDW, the stable annual conductivity records from 2009 to 2012 partially reflected the slight variation in the mineral content in the DDW. Children in the low-mineral group (group 2) showed a marked drop in height and a marked rise in the prevalence of hypoevolutism and dental caries after the introduction of DDW (in 2011 and 2012), which was not found before the introduction of DDW (in 2008 and 2009). Moreover, children in the low-mineral group (group 2) had a lower height increase and higher incidence of hypoevolutism and dental caries after the introduction of DDW (2009–2012). Furthermore, lowmineral DDW exposure was a risk factor for hypoevolutism and dental caries incidence and lower height increase in children after the introduction of DDW systems (2009–2012). These results indicate that the low mineral content of the DDW may retard height development and promote dental caries in children. Considering that DDW accounted for the vast majority of water consumption in schoolchildren, the contribution of minerals from daily water consumption and daily mineral intake may have decreased in the low-mineral group. Although the contribution of minerals from water consumption is only a small proportion of daily mineral intake, it is important for the maintenance of health, especially when its deficiency in food is prevalent (Grandjean and Bartram, 2011). For example, calcium, the major element of hydroxyapatite, which is the inorganic mineral compound of bone, is essential to height growth and dental health (Martin-Bautista et al., 2011), and its intake in our study
5. Conclusions In summary, this study provides independent epidemiological evidence that drinking low-mineral water may retard height development and promote dental caries in schoolchildren. Our results indicate that we should not only consider the protection afforded by DDW in terms of drinking water safety but also monitor its potential adverse effects on the development of children when schools use DDW systems that remove too much of the necessary minerals, such as by reverse-osmosis technology. Campus DDW systems should utilize treatment systems that do not remove the minerals in water, such as acticarbon, ultrafiltration membranes, and disinfection by silver, ozone or ultraviolet radiation. If the reverse-osmosis technology is necessary, a subsequent remineralization, such as filtering through dolomite, should be considered. Acknowledgments This work was supported by the Project of Chongqing Municipal Health Bureau (Grant No. 2012-2-447). Author contributions W.Q.S. conceived the investigation and designed the exposure estimates. Y.J.H. designed the exposure estimates, performed the experiment and statistical analyses, and drafted the manuscript. L.L. and Q.B.Y. made substantial contributions to the data collection. W.H., Y.X. made substantial contributions to the interpretation of the data. Y.T. and L.Q.W. made substantial contributions to performing the experiments. H.L. assisted with and checked the statistical analyses. J.W. assisted with and checked the statistical analyses and modified the manuscript. 108
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Additional informationCompeting interests
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