You are on page 1of 5

Journal of Hazardous Materials 186 (2011) 19421946

Contents lists available at ScienceDirect

Journal of Hazardous Materials


journal homepage: www.elsevier.com/locate/jhazmat

The relationships between low levels of urine uoride on childrens intelligence,


dental uorosis in endemic uorosis areas in Hulunbuir, Inner Mongolia, China
Yunpeng Ding a,1 , YanhuiGao a,1 , Huixin Sun a , Hepeng Han a , Wei Wang a , Xiaohong Ji a ,
Xuehui Liu b , Dianjun Sun a,
a
Center for Endemic Disease Control, Chinese Center for Disease Control and Prevention, Harbin Medical University, Harbin 150081, Heilongjiang, China
b
Hulunbuir City Institute for Endemic Disease Control, Zalantun 162650, China

a r t i c l e i n f o a b s t r a c t

Article history: There has been public concern about childrens intellectual performance at high levels of uoride expo-
Received 28 October 2010 sure, but few studies provide data directly to the question of whether low uoride exposure levels less
Received in revised form than 3.0 mg/L in drinking water adversely associated with childrens intelligence. In this survey, we inves-
18 December 2010
tigated the effects of low uoride exposure on childrens intelligence and dental uorosis. 331 children
Accepted 20 December 2010
aged from 7 to 14 were randomly recruited from four sites in Hulunbuir City, China. Intelligence was
Available online 25 December 2010
assessed using Combined Raven Test-The Rural in China while dental uorosis was diagnosed with Deans
index. Mean value of uoride in drinking water was 1.31 1.05 mg/L (range 0.242.84). Urine uoride
Keywords:
Urine uoride
was inversely associated with IQ in the multiple linear regression model when childrens age as a covari-
IQ ate variable was taken into account (P < 0.0001). Each increase in 1 mg/L of urine uoride associated with
Dental uorosis 0.59-point decrease in IQ (P = 0.0226). Meanwhile, there was a doseresponse relationship between urine
Children uoride and dental uorosis (P < 0.0001). In conclusion, our study suggested that low levels of uoride
exposure in drinking water had negative effects on childrens intelligence and dental health and con-
rmed the doseresponse relationships between urine uoride and IQ scores as well as dental uorosis.

2010 Elsevier B.V. All rights reserved.

1. Introduction 5749-2006) [12]. However, most studies examining the effects on


the damages to childrens intellectual ability and other aspects were
Many animal experiments document that exposure to high lev- conducted in regions where residents were exposed to relatively
els of uoride in drinking water may have certain structural and high uoride levels (more than 3 mg/L) [5,6,13,14] while the major-
functional damages to nervous system [13] as well as cumula- ity of residents living in endemic uorosis areas have been exposed
tive toxic symptoms like dental uorosis and skeletal uorosis [4]. to lower uoride levels in their daily life. Although some studies
Epidemiological studies have consistently conrmed that excessive [15,16] in which the uoride exposure levels were relatively low
exposure to uoride in drinking water may lead to the decrease of had reported associations between low uoride exposure and the
childrens intellectual ability [5,6] and the rise in the prevalence negative effects among children, the analysis focused specically
of dental uorosis [79]. Meta-analyses focusing on the effect of on childrens dental uorosis condition rather than intellectual per-
uoride exposure in drinking water to childrens intelligence also formance.
suggest a strong negative relation of uoride exposure on IQ perfor- Fluoride concentration in drinking water is long-term stable in
mance [10,11]. These ndings provided evidences and references years in a certain region [17]; kidney as a site of active metabolism
for the health administrative departments in some countries to excretes 5080% of uoride intake from drinking water and other
revise their screening guidelines of uoride concentration in drink- sources [18]. Therefore, urine uoride concentration as an internal
ing water to safe levels. For instance, the uoride concentration in exposure index can systematically reect the burden of uoride
drinking water has been set to no more than 1 mg/L in China (GB exposure in drinking water. In the present ecologic study, we
explored the doseresponse relationships between urine uoride
levels and childrens intelligence quotient (IQ) as well as den-
tal uorosis condition using multiple linear regression model and
CochranArmitage test for trend respectively to estimate the possi-
Corresponding author. Tel.: +86 451 8661 2695; fax: +86 451 8665 7674.
ble negative effects of long-term low uoride exposure in drinking
E-mail address: hrbmusdj@163.com (D. Sun).
1
These authors contributed the same to this work. water to young children.

0304-3894/$ see front matter 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.jhazmat.2010.12.097
Y. Ding et al. / Journal of Hazardous Materials 186 (2011) 19421946 1943

Fig. 1. Distribution of four study sites in Hulunbuir City.

2. Materials and methods mixed 5 ml urine samples with 5 ml total ionic strength adjustment
buffer (TISAB) at PH 5, then used F-ion selective electrode (Yingke
2.1. Sample selection Crystal Materials Company) to detect those samples. All the sam-
ples were analyzed in twice (independent aliquots), and the means
Hulunbuir is a region that is governed as a prefecture-level of two aliquots were calculated to derive the urine uoride concen-
city in northeastern Inner Mongolia, China. Until October 10, 2001, tration. Recovery rate of this method was in the range of 95105%.
Hulunbuir was administered as a League. Hulunbuir is divided into The quantitation limit of this method is 0.05 mg/L.
13 different country-level jurisdictions: one district, ve country- Water samples were collected from small-scale central water
level cities, four banners and three autonomous banners [19]. Many supply system and tube wells with handy pump respectively and
cross-sectional studies [2022] showed that uoride concentration kept in 4 C until used for analysis. The Institute for Endemic Fluoro-
in drinking water in this area had been higher than the upper limit sis Control, Center for Endemic Disease Control, China CDC, using a
of 1 mg/L prescribed in Chinese Standards for Drinking Water Qual- national standardized method in China (WS/T 106-1999) [26], car-
ity [12] for a long period. Meanwhile, studies related to uoride ried out all analytical measurements for uoride in drinking water.
exposure in drinking water have found large number of children In the analysis, we mixed 5 ml water samples with 5 ml TISAB at
accompanied by dental uorosis in this region. In accordance with PH 5, using the F-ion selective electrode (Yingke Crystal Materials
the principles of matching such social and natural factors like eco- Company) to detect those samples. All the samples were analyzed
nomic situation, educational standard and geological environments in twice (independent aliquots), and the means of two aliquots
as much as possible, we conducted our investigation by randomly were calculated to derive the uoride concentration in drinking
identifying 340 subjects who were aged from 7 to 14 from four ele- water. Quality assurance validation was obtained through periodic
mentary schools among four nearby sites-Mianduhe Town, Donghu analysis of National Institute for Environmental Reference Mate-
District, Nan District and Zhalainuoer Country in Manzhouli City in rials (IERM, Beijing) Standard Reference Material of water-based
Hulunbuir according to the Inner Mongolia Statistical Yearbook in uoride (3.47 0.21 mg/L). The quantitation limit of this method is
2009 [23] (Fig. 1). These four elementary schools chosen to carry out 0.2 mg/L.
our investigation appear to be very similar in teaching quality based
on the information provided by local educational bureau. None of
these four sites was exposed to potential neurotoxic that are recog- 2.3. Standards for detection of dental uorosis
nized as contaminates inuencing IQ value, like arsenic in drinking
water [13], nor delimitated into endemic areas of iodine deciency Our investigation adopted Deans index [27] recommended by
disorders. For the current study, we nally excluded ve children WHO to diagnose dental uorosis. An individuals uorosis condi-
who had lived in these areas for less than 1 year and four children tion is based on the most severe form of uorosis found on two or
who did not consent to take IQ test, resulting in 331 subjects eligi- more teeth. An individuals dental status can be classied into six
ble for our study. The institutional review board of Harbin Medical parts: normal, questionable, very mild, mild, moderate and severe.
University approved the study, and all the parents or guardians The same professional examiner who was unaware of childrens
provided written informed consent. uoride exposure status was specied to conduct all the testing
measurements to guarantee the accuracy and consistency for diag-
nostic criteria.
2.2. Collection and analysis of water and urine samples

Instant urine samples were collected using 15 ml tubes and kept 2.4. Assessments of intelligence
in 18 C until used for analysis. All collection tubes were carefully
washed with detergent before immersing in 10% aqueous nitric Children were administered to take the Combined Ravens Test-
acid solution for 8 h and then washed in distilled water for 3 times The Rural in China (CRT-RC3) [28] to evaluate their intellectual
in accordance with the national standard of China (GB/T 5750.2- ability. The seven categories of this test scores are as follows:
2006) [24]. The Institute for Endemic Fluorosis Control, Center for 69 retarded (low); 7079 borderline (below average); 8089 dull
Endemic Disease Control, China CDC, using a national standard- normal (low average); 90109 normal (average); 110119 high
ized method in China (WS/T 89-1996) [25], carried out all analytical normal (high average); 120129 superior (good); 130 very supe-
measurements for urine uoride. In the procedure of analysis, we rior (excellent).
1944 Y. Ding et al. / Journal of Hazardous Materials 186 (2011) 19421946

Table 1 the doseresponse associations of urine uoride with IQ as well as


Fluoride concentration (mg/L) in drinking water among four study sites in Hulunbuir
dental uorosis condition.
City.
Of total 331 eligible children selected in our investigation, Mian-
Number Mean SD Min Max duhe Town had 75, Nan District had 74, Donghu District had 79
Mianduhe town 3 0.28 0.03 0.24 0.31 and Zhalainuoer Country had 103. Nearly half of these subjects
Nan district 4 0.79 0.33 0.47 1.32 (165/331) were female. Children were aged from 7 to 14 years,
Donghu district 3 1.78 0.60 1.14 2.58 over 90% of children (303/331) were distributed from 8 to 12 years
Zhalainuoer country 6 1.82 1.00 0.32 2.84
old. We compared age, sex, IQ scores and urine uoride concentra-
tions of children with different dental uorosis condition (Table 2).
2.5. Statistical analysis Except for mean value of urine uoride concentrations, general
characteristics among the ve groups divided by dental uorosis
We estimated the association between urine uoride levels condition were similar.
and IQ scores with two progressive methods. First, children were We assigned all the 331 children into four groups by the quar-
classied into 10 groups based on the full range of urine uo- tiles of full range of urine uoride concentrations to examine
ride concentrations to demonstrate difference in mean IQ scores the doseresponse relationship of urine uoride against den-
across different level of urine uoride exposure. In addition, we tal uorosis. The distribution of urine uoride concentrations of
performed a multiple linear regression model that included full these four groups were 0.1000.552 mg/L (as the control group),
range of urine uoride concentrations as independent variable 0.5540.810 mg/L (as the low exposure group), 0.8181.301 mg/L
and age as covariate variable to analyze the association of urine (as the medium exposure group) and 1.3173.550 mg/L (as the
uoride with IQ scores which was seen as the dependent vari- high exposure group) respectively. From the results in Table 3,
able. CochranArmitage test for trend was used to evaluate the we found the value of risk ratio (OR) in different levels raised
doseresponse relationship between urine uoride and dental u- with the increasing of urine uoride concentrations. This possible
orosis. By use of ANOVA, we analyzed the signicance of age, IQ tendency between urine uoride and dental uorosis was fur-
and urine uoride concentration against different dental uorosis ther conrmed by the result of CochranArmitage test for trend
condition; 2 test was used to compare the signicance of percent- (Z = 4.099, P < 0.0001), which probably indicated that the risk of suf-
age of children with IQ 89 in different dental uorosis condition. fering dental uorosis was gradually increased along with the rise
Data were analyzed by Statistical Analysis System software (Ver- of urine uoride exposure.
sion 9.1, SAS Institute, Cary, North Carolina). A difference at P < 0.05 Evidence developed by Wu and Li [29] and Xiang et al. [30] in
was considered statistically signicant. high uoride exposure areas reinforced our results and revealed
that urine uoride concentrations were positively associated with
3. Results and discussion dental uorosis. It should be pointed out that the correlation of
urine uoride levels and dental uorosis condition are more likely
Most regions in Hulunbuir City, Inner Mongolia are identied to be observed in those relatively high uoride exposure areas
as drinking water type of uorosis areas. Four sites in Hulunbuir where the prevalence of dental uorosis as well as urine uoride
City were involved in our investigation. Mean, min and max value concentrations are much higher than normal regions. Heintzes
of uoride concentrations in drinking water of the four sites are research [31] that was conducted in low uoride areas was failed to
given in Table 1. Mean value of uoride in drinking water was nd signicant association between urine uoride levels and dental
1.31 1.05 mg/L (range 0.242.84). In the present study, uoride uorosis. This may be attributable to the low dental uorosis preva-
concentrations in Mianduhe Town and Nan District approximately lence caused by the relatively low uoride exposure in drinking
reached the Standards for Drinking Water Quality in China of water to approximately below 1 mg/L.
1 mg/L. Donghu District and Zhalainuoer Country had signicantly To examine the doseresponse relationship of urine uoride
higher uoride concentrations than the screening guideline of with IQ scores, the children were ordered by their urine uoride
1 mg/L, which illustrated that residents in these two sites had concentrations and put into 10 groups of about 33 in each. The
been exposed to higher uoride levels. However, none of these mean value of urine uoride concentration of the lowest group
four sites had uoride concentrations in drinking water more than was 0.262 mg/L and of the highest group was 2.956 mg/L. For each
3 mg/L in our survey. These results on uoride exposure levels group, the IQ difference from mean value was plotted against the
ensured the implementation of our study that required both rel- urine uoride concentrations (Fig. 2). From the rst group to tenth,
atively low uoride exposure circumstances and different uoride mean IQ score declined about 4.877 points. Besides, there was a
exposure levels to stratify children into several groups to estimate decrease of 3.261 points between the rst and third quartiles of

Table 2
Age, sex, IQ and urine uoride levels against dental uorosis condition among children in Hulunbuir, China.

Normal (N = 136) Questionable (N = 54) Very mild (N = 74) Mild (N = 39) Moderate (N = 28)

Female sex (%) 52.9 48.1 43.2 56.4 50


Age (yr)
Mean SD 9.67 1.60 9.41 1.47 9.54 1.31 9.44 1.05 9.64 1.39
Min value 7 7 7 7 7
Max value 14 13 13 11 12
Intelligence quotient
Mean SD 104.07 12.30 103.00 16.10 102.11 15.05 106.03 12.33 103.54 13.59
Min value 78 54 58 82 83
Max value 138 139 143 133 132
Urine uoride (mg/L)
Mean SDa 0.80 0.55 1.13 0.73 1.11 0.74 1.31 0.78 1.46 0.79
Min value 0.10 0.19 0.16 0.25 0.22
Max value 3.44 3.41 3.55 3.32 3.22
a
P < 0.05 for comparison between children in different dental uorosis condition.
Y. Ding et al. / Journal of Hazardous Materials 186 (2011) 19421946 1945

Table 3
The relationship between dental uorosis and urine uoride levels.a

Quartiles of urine uoride (mg/L)

Q1 Q2 Q3 Q4
0.389 0.12 0.676 0.07 1.035 0.15 2.058 0.62

Sample number
Dental uorosis 22 32 40 47
Normalb 61 50 43 36
OR value 1.77 2.58 3.62
95% CI 0.923.43 1.354.94 1.886.95
a
CochranArmitage test for trend was used to evaluate the association between dental uorosis and urine uoride levels (Z = 4.099, P < 0.0001).
b
Normal group included normal and questionable status of dental uorosis..

IQ Differences
from Mean Value
10

-5

-10
0 0.5 1 1.5 2 2.5 3
Urine Fluoride Concentration (mg/L)

Fig. 2. The relationship between IQ differences and urine uoride concentrations. Multiple linear regression model was carried out to conrm the association of urine uoride
exposure with IQ scores (F = 9.85, P < 0.0001).

urine uoride levels. Moreover, mean IQ scores of the last ve The results in our investigation were derived from full range of
groups were primarily below the mean value of total IQ scores. urine uoride concentrations based on individual exposure con-
Obviously, the data showed a negative doseresponse relationship ditions and the usage of multiple linear regression model was
between urine uoride levels and IQ scores. Multiple linear regres- very accurate to estimate the doseresponse relationship between
sion model that included age as covariate variable was carried childrens IQ and urine uoride exposure levels. In addition, the
out to further conrm the association of urine uoride exposure majority of children involved in this investigation were boarding
with IQ scores. Adjusted estimate (95% condence interval) of the students that balanced educational background and ordinary learn-
effect of urine uoride exposure on IQ test scores is a decrease ing behavior well between participants. Nevertheless, it should be
of 0.59 (1.09, 0.08) points in 1 mg/L increase of urine uoride recognized that the limitation of this study was its disability to
concentration (P < 0.0001). In other words, an increase in the urine describe the inuence of confoundings related to parents on chil-
uoride concentration of 1 mg/L associated with a decrease of 0.59 drens intelligence. The present investigation was initially carried
IQ scores. out to investigate intellectual ability of children exposed to low
Many literatures [5,13,32] have shown that exposure to high uoride levels in drinking water. We will study carefully the corre-
levels of uoride in drinking water associate with decits towards lation of childrens IQ with urine uoride exposure including other
childrens intelligence. These results were mainly illustrated by covariates, especially the ones related to parents, such as parents
comparing mean IQ scores in different exposure groups that were educational attainment, mothers age at delivery, mothers intelli-
selected based on uoride concentrations in drinking water. Com- gence and household income [3436] in future works.
pared to external exposure that is distinct in person due to The association of dental uorosis with childrens IQ scores is
individual difference in the absorption rate, urine uoride con- presented in Table 4. Number of children with IQ 89 did not have
sidered as internal exposure can truly reect the exposure levels signicant differences (2 = 2.362, df = 2, P = 0.307) among normal,
and preventing some negative inuences from external exposure. very mild and mild group of dental uorosis. Actually, the mean
Meanwhile, the association between levels of internal exposure IQ score in the mild group was higher and the number of chil-
and specic effect is more stable and consistent [33]. Our study dren with IQ 89 was less than the two of normal and very mild
demonstrated clearly that, across the full range of urine uoride groups. Despite the mean value of IQ in moderate dental uoro-
and using a measure to focus on individuals IQ scores, higher urine sis group had no signicant difference against the other groups
uoride levels were associated with decits of intellectual perfor- (F = 0.71, P = 0.548), percentage of childrens number with IQ 89
mance, even when the external exposure levels were not relatively was much higher.
high.
The characteristic of ecological investigation makes it unavoid- Table 4
able to select subjects in different regions for possession of the The association of dental uorosis condition with IQ scores.
different exposure levels of uoride in drinking water. From a Dental uorosis Number IQ scores
general standpoint, childrens intelligence is very susceptible to
many social and natural factors like economic situation, culture Mean SD IQ 89 (%)

and geological environments. Therefore, it seems difcult to deter- Normala 190 103.77 13.61 23 (12.11)
mine whether the difference of childrens IQ scores in two different Very mild 74 101.70 13.68 12 (16.22)
Mild 39 107.36 13.62 2 (5.13)
regions is caused by the uoride exposure or other factors. To
Moderate 28 103.27 13.68 6 (21.43)
reduce the possibility of interruption of intellectual confounding
a
factors, we limited this survey in only one region-Hulunbuir City. Normal group included normal and questionable status of dental uorosis.
1946 Y. Ding et al. / Journal of Hazardous Materials 186 (2011) 19421946

Fomons study [37] suggested that the occurrence of dental u- [9] S. Suthar, V.K. Garg, S. Jangir, et al., Fluoride contamination in drinking water
orosis was very sensitive to uoride toxicity, which made people in rural habitations of Northern Rajasthan, India, Environ. Monit. Assess. 145
(2008) 16.
exposed to lower dose of uoride got dental uorosis in their early [10] Q.Q. Tang, J. Du, H.H. Ma, et al., Fluoride and childrens intelligence: a meta-
childhood. On the other hand, the pace of development of childrens analysis, Biol. Trace Elem. Res. 126 (2008) 115120.
intelligence is comparatively slow and factors affecting intellectual [11] M. Liu, C. Qian, Effect of endemic uorosis on childrens intelligence develop-
ment: a meta analysis, Chin. J. Contemp. Pediatr. 10 (2008) 723725.
ability are much more than dental uorosis. Therefore, children [12] Ministry of Health of the Peoples Republic of China, Standards for Drinking
with very mild or mild dental uorosis probably have no difference Water Quality (GB 5749-2006), 2006.
on intellectual performance against normal children. Although we [13] S.X. Wang, Z.H. Wang, X.T. Cheng, et al., Arsenic and uoride exposure in drink-
ing water: childrens IQ and growth in shanyin county, shanxi province, China,
did not explore the biological mechanisms of this nding, there was Environ. Health Perspect. 115 (2007) 643647.
an animal experiment [3] suggesting that a relatively low level of [14] S.S. Liu, Y. Lu, Z.R. Sun, L.N. Wu, et al., The investigation of childrens intelligence
uoride exposure (100 mg/L in drinking water for 6 weeks) which in high uoride area, Chin. J. Control End. Dis. 15 (2000) 231232.
[15] J.P. Ruan, A. Brdsen, A.N. strm, et al., Dental uorosis in children in areas
could cause dental uorosis had little impact to weaning rats on
with uoride-polluted air, high-uoride water, and low-uoride water as well
their behavior disruption. However, the situation is quite different as low-uoride air: a study of deciduous and permanent teeth in the Shanxi
in children with moderate dental uorosis condition, because the province, China, Acta Odontol. Scand. 65 (2007) 6571.
severer condition of dental uorosis is, the higher exposure to u- [16] J. Narbutaite, M.M. Vehkalahti, S. Milciuviene, Dental uorosis and dental caries
among 12-yr-old children from high- and low-uoride areas in Lithuania, Eur.
oride in environment it means to children that can cause decits J. Oral Sci. 115 (2007) 137142.
in the development of intelligence. Hence, the explanation seems [17] G.S. Li (Ed.), Pathogenesis of Endemic Disease, Science Press, Beijing, 2004, pp.
logical and coherent that the proportion of children with severer 165173.
[18] H. Spencer, I. Lewin, E. Wistrowski, et al., Fluoride metabolism in man, Am. J.
dental uorosis condition in relatively low IQ scores is much more Med. 49 (1970) 807813.
likely to be larger than that of normal children. [19] Q.T. Hu (Ed.), Inner Mongolia Today: Hulun Buir, Inner Mongolia Peoples Pub-
lishing House, Hohhot, 1997, pp. 128129.
[20] Z.Y. Liu, S. Liu, S.Y. Guo, The analysis of the rusults of rural drinking water quality
4. Conclusions monitoring in zhalainuoer district, Manzhouli city, Chin. Prev. Med. 10 (2009)
427428.
Overall, our study suggested that low levels of uoride exposure [21] Q.B. Liu, Z.J. Wang, X.H. Liu, et al., The radiological difence of drinking brick-
tea type uorosis and drinking water type uorosis in Hulunber city, inner
in drinking water had negative effects on childrens intelligence and Mongolia, Chin, J. Control End. Dis. 22 (2007) 89.
dental health. The results also conrmed the doseresponse rela- [22] H.R. Li, Q.B. Liu, W.Y. Wang, et al., Fluoride in drinking water, brick tea infusion
tionships between urine uoride concentrations and IQ scores as and human urine in two counties in Inner Mongolia, China, J. Hazard. Mater.
167 (2009) 892895.
well as dental uorosis condition. Either a small decline in IQ scores [23] National Bureau of Statistical of China, Inner Mongolia Statistical Yearbook,
or the sickness of dental uorosis can lead a profound inuence for 2009.
individuals on their developments. Thus, these ndings may have [24] Ministry of Health of the Peoples Republic of China, Standard Examination
Methods for Drinking Water-Collection and Preservation of Water Samples
policy implications for a country like China to put more effort on
(GB/T 5750.2-2006), 2006.
the water improving and deuoridation projects to alleviate toxic- [25] Ministry of Health of the Peoples Republic of China, Determination of Fluoride
ity of long-term effects of uoride exposure to local residents and in Urine-ion Selective Electrode Method (WS/T 89-1996), 1996.
their offspring. [26] Ministry of Health of the Peoples Republic of China, Method for Determination
of Fluoride in Drinking Water of Endemic Fluorosis Areas (WS/T 106-1999),
1999.
Acknowledgements [27] H.T. Dean, The investigation of physiological effects by the epidemiological
method, in: F.R. Moulton (Ed.), Fluoride and Dental Health, American Asso-
ciation for the Advancement of Science, Washington, DC, 1942, pp. 2331.
This research was supported by National Natural Science Foun- [28] D. Wang, M. Di, M. Qian, A Report on the third revision of combined Ravens
dation of China (Project Nos. 3057161and 30800956). The authors Test (CRTC3) for Children in China, Chin. J. Clin. Psychol. 15 (2007) 559568.
declare they have no competing nancial interests. [29] D.L. Wu, Y.L. Li, The investigation of the total amount of fIuoride intake with cor-
relative dental uorosis polluted by burn coal in the epidemic fIuorosis districts,
Chin. J. Prev. Med. 24 (1990) 15.
References [30] Q.Y. Xiang, L.S. Chen, C.S. Wang, Study on the bench mark dose of urine uoride
in children and its relaonship to the prevalence of dental urosis, Chin. J.
[1] C.X. Wu, X.L. Gu, Y.M. Ge, J.H. Zhang, et al., Effect of high uoride and arsenic Control End. Dis. 20 (2005) 6871.
on brain biochemical indexes and learning-memory in rats, Fluoride 39 (2006) [31] S.D. Heintze, J.R.D.M. Bastos, R. Bastos, Urinary uoride levels and prevalence of
274279. dental uorosis in three Brazilian cities with different uoride concentrations
[2] Y.M. Shivarajashankara, A.R. Shivashankara, P.G. Bhat, et al., Histological in the drinking water, Commun. Dent. Oral Epidemiol. 26 (1998) 316323.
changes in the brain of young uoride-intoxicated rats, Fluoride 35 (2002) [32] L.B. Zhao, G.H. Liang, D.N. Zhang, et al., Effect of a high uoride water supply on
1221. childrens intelligence, Fluoride 29 (1996) 190192.
[3] P.J. Mullenix, P.K. Denbesten, Ann Schunior, et al., Neurotoxicity of sodium [33] L.M. Li, The Epidemiology, fth ed., Peoples Medical Publishing House, Beijing,
uoride in rats, Neurotoxicol. Teratol. 17 (1995) 169177. 2003.
[4] WHO, Fluorides, Environmental Health Criteria, vol. 227, WHO, Geneva, 2002. [34] M. Fulton, G. Thomson, R. Hunter, et al., Inuence of blood lead on the ability
[5] M.H. Trivedi, R.J. Verma, N.J. Chinoy, et al., Effect of high uoride water on and attainment of children in edinburge, Lancet 329 (1987) 12211226.
intelligence of school children in india, Fluoride 40 (2007) 178183. [35] R.L. Caneld, C.R. Hederson Jr., et al., Intellectual impairment in children with
[6] Y.X. Chen, F.L. Han, Z.L. Zhou, et al., Research on the intellectual development blood lead concentrations below 10 g per deciliter, New Engl. J. Med. 348
of children in high uoride areas, Fluoride 41 (2008) 120124. (2003) 15171526.
[7] D.J. Sun, Surveillance on endemic uorosis of drinking water type in China: [36] T.A. Jusko, C.R. Henderson Jr., B.P. Lanphear, et al., Blood lead concentra-
a two-year report of 2003 and 2004, Chin. J. Epidemiol. 26 (2007) 161 tions<10 g/dL and child intelligence at 6 years of age, Environ. Health Perspect.
164. 116 (2008) 243248.
[8] V. Shitumbanuma, F. Tembo, J.M. Tembo, et al., Dental uorosis associated [37] S.J. Fomon, J. Ekstrand, E.E. Ziegler, Fluoride intake and prevalence of dental
with drinking water from hot springs in Choma district in southern province, uorosis: trends in uoride intake with special attention to infants: review
Zambia, Environ. Geochem. Health. 29 (2007) 5158. and Commentory, J. Public Health Dent. 60 (2000) 131139.

You might also like