DB 6 Environmental and Biological Effects on Intelligence and Achievement Intelligence tests are controversial, partly because they sometimes determi

DB 6 Environmental and Biological Effects on Intelligence and Achievement
Intelligence tests are controversial, partly because they sometimes determine important aspects of peoples lives. For example, intelligence test scores have factored into determining school placement, identifying giftedness, and diagnosing mental retardation and learning disabilities. Even when an intelligence test shows that a child has normal intelligence, there might be speculation of a learning disability due to him or her falling behind in academic achievement. A childs biology and environment influences his or her academic achievement, as well. Children from different cultures and socioeconomic status have diverse experiences, beliefs, and attitudes that affect their academic achievement. There are also differences in skills that caregivers emphasize during a childs development that contribute to a childs school readiness, which influences intelligence and academic achievement.
Intelligence and academic achievement are often used to determine many aspects of a persons life, including the diagnosis of a learning disability. Most identifiers of learning disabilities are seen within the realm of intelligence and achievement. The Individuals with Disabilities Education Improvement Act of 2004 is an example of a federal mandate that allows for identification of indicators of learning disabilities, such as limited response to intervention or a meaningful discrepancy between a students intelligence and achievement scores. When diagnosing a learning disability in determining a childs intelligence, a combination of indicators is more accurate than a single test score.
For this Discussion, you will explore the differences between intelligence and academic achievement (as opposed to other types of achievement). You also will examine environmental and/or biological influences on intelligence and academic achievement.
To prepare for this Discussion:

Review this weeks Learning Resources related to intelligence and academic achievement and consider environmental and biological influences.
Select two influences: environmental and/or biological (you can select two of either category or one of each) that have been associated with intelligence and academic achievement.

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Post an explanation of the difference between intelligence and academic achievement. Then, briefly describe the two environmental and/or biological influences you selected. Explain the effects of each influence on intelligence and academic achievement. Be specific and provide examples from your Learning Resources. Use proper APA format and citations.
Resources
Berk, L. E. (2018). Development through the lifespan (7th ed.). Upper Saddle River, NJ: Pearson Education.

Chapter 7, Physical and Cognitive Development in Early Childhood (pp. 214253)
Chapter 9, Physical and Cognitive Development in Middle Childhood (pp. 292-331)

http://webapp1.dlib.indiana.edu/virtual_disk_library/index.cgi/4273355/FID840/eqtyres/erg/111564/1564.htm
Christoffersen, M. N. (2012). A study of adopted children, their environment, and development: A systematic review. Adoption Quarterly, 15(3), 220237.
Welsh, J. A., Nix, R. L., Blair, C., Bierman, K. L., & Nelson, K. E. (2010). The development of cognitive skills and gains in academic school readiness for children from low-income families. Journal of Educational Psychology, 102(1), 4353.

Impact of Low Blood Lead Concentrations on IQ and
School Performance in Chinese Children
Jianghong Liu1*, Linda Li1, Yingjie Wang1, Chonghuai Yan2, Xianchen Liu3,4

1 University of Pennsylvania, School of Nursing and School of Medicine, Philadelphia, Pennsylvania, United States of America, 2 Xinhua Hospital, MOE-Shanghai Key

Laboratory of Childrens Environmental Health, Shanghai Jiaotong University School of Medicine, Shanghai, China, 3 Indiana University, School of Medicine, Indianapolis,

Indiana, United States of America, 4 Shandong University, School of Public Health, Jinan, China

Abstract

Objectives: Examine the relationships between blood lead concentrations and childrens intelligence quotient (IQ) and
school performance.

Participants and Methods: Participants were 1341 children (738 boys and 603 girls) from Jintan, China. Blood lead
concentrations were measured when children were 35 years old. IQ was assessed using the Chinese version and norms of
the Wechsler Preschool and Primary Scale of Intelligence Revised when children were 6 years old. School performance was
assessed by standardized city tests on 3 major subjects (Chinese, Math, and English [as a foreign language]) when children
were age 810 years.

Results: Mean blood lead concentration was 6.43 mg/dL (SD = 2.64). For blood lead concentrations, 7.8% of children
(n = 105) had $10.0 mg/dL, 13.8% (n = 185) had 8.0 to ,10.0 mg/dL, and 78.4% (n = 1051) had ,8.0 mg/dL. Compared to
children with blood lead concentrations ,8 mg/dL, those with blood lead concentrations $8 mg/dL scored 23 points lower
in IQ and 56 points lower in school tests. There were no significant differences in IQ or school tests between children with
blood lead concentrations groups 810 and $10 mg/dL. After adjustment for child and family characteristics and IQ, blood
lead concentrations $10 mg/dL vs ,8 mg/dL at ages 35 years was associated with reduced scores on school tests at age 8
10 years (Chinese, b = 23.54, 95%CI = 26.46, 20.63; Math, b = 24.63, 95%CI = 27.86, 21.40; English, b = 24.66,
95%CI = 28.09, 21.23). IQ partially mediated the relationship between elevated blood lead concentrations and later
school performance.

Conclusions: Findings support that blood lead concentrations in early childhood, even ,10 mg/dL, have a long-term
negative impact on cognitive development. The association between blood lead concentrations 810 mg/dL and cognitive
development needs further study in Chinese children and children from other developing countries.

Citation: Liu J, Li L, Wang Y, Yan C, Liu X (2013) Impact of Low Blood Lead Concentrations on IQ and School Performance in Chinese Children. PLoS ONE 8(5):
e65230. doi:10.1371/journal.pone.0065230

Editor: Qinghua Sun, The Ohio State University, United States of America

Received September 24, 2012; Accepted April 23, 2013; Published May 29, 2013

Copyright: 2013 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: Funding was provided by the National Institute of Environment Health Sciences (NIEHS, R01-ES018858; K01-ES015 877; K02-ES019878-01); UPenn CEET
P30 ES013508; The Wacker Foundation US; Jintan City Government; Jintan Hospital, China. The funders had no role in study design, data collection and
analysis,decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

* E-mail: [emailprotected]

Introduction

Childhood lead exposure is still an important public health

problem in the world, predisposing children at risk of cognitive

deficits and behavioral problems [13]. Emerging evidence has

also suggested that even children with blood lead concentra-

tions,10 mg/dL are at significant risk for reduced cognitive
development and functioning, including intelligence quotient (IQ)

deficits [410] and poor academic performance [11,12]. Alarm-

ingly, deficits in intellectual abilities and elevated risks for

behavioral problems may persist into adolescence and even

adulthood [1317]. Despite increasing attention given to the

importance of both elevated ($10 mg/dL) and lower (,10 mg/dL)
blood lead concentrations on childrens cognitive development,

however, several questions remain. Although previous studies have

revealed that blood lead concentrations ,10 mg/dL were related

to poorer neurocognitive outcomes in children (e.g. [3,5,18]),

studies in this area are still limited. Even more recently, the US

Centers for Disease Control (CDC) eliminated the terminology

level of concern. Children with elevated blood lead concentra-

tions will instead be identified using a reference value based on the

97.5th percentile of the National Health and Nutrition Examina-

tion Survey (NHANES)-generated blood lead concentration

distribution in children aged 15 years old; currently, this value

is 5 mg/dl [19]. Since most studies have used cohorts from
Western countries, it is unclear whether their findings are

replicable in other developing countries, such as China, where

lead concentrations and prevalence of lead exposure are much

higher [3,20]. In areas of high lead exposure, effects of lower

concentrations of lead on childrens developmental function may

differ. In addition, the effects of lead on both IQ and school

performance have rarely been examined together. Although

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Surkan et al. [10] demonstrated significantly reduced IQ and

academic performance in 610 year old children, it is still unclear

whether IQ deficits due to lead exposure subsequently results in

poor academic achievement. Finally, regarding the effects of low

lead exposure on the specific type of IQ (e.g., Performance IQ

[PIQ]), some have argued that Verbal IQ (VIQ) (verbal skills) is

more negatively affected [10,21] while others have found only

significantly lowered PIQ (visual-spatial skills) [5]. More data

would be beneficial for understanding the impact of early lead

exposure on specific types of cognitive deficits to further investigate

the neurotoxicity of low blood lead on brain function as reflected

by cognitive outcomes.

Using a large, community-based, longitudinal cohort sample of

Chinese children for whom blood lead concentrations were

measured at 3, 4, or 5 years of age, IQ was assessed at 6 years

of age, and academic achievement in 3 major subjects (Chinese,

Math, and English) was assessed at 810 years of age, the present

study aims to: 1) assess whether elevated blood lead concentrations

are related to preschool childrens IQ and later academic

achievement in Chinese children; 2) examine whether and the

extent to which the relationship between blood lead concentra-

tions and school performance is mediated by IQ; 3) determine

which specific components of these aforementioned outcomes are

affected to delineate specificity of leads effect on verbal and

performance skills; and 4) identify at what blood lead concentra-

tions ,10 mg/dL are reduced cognitive outcomes observed for
potential public health implications.

Participants and Methods

Subjects
The current study is part of an ongoing longitudinal project, the

China Jintan Child Cohort Study, which consists of 1,656

preschool children accounting for 24.3% of all children aged 3

5 years in Jintan city, Jiangsu province, China. Participants were

drawn from four preschools chosen to represent the entire citys

geographical, social, and economic profiles. Between Fall 2004

and Spring 2005, children aged 35 years attending the preschools

were invited to participate in this study; signed consent forms were

obtained from the parents. Detailed information on this cohort,

including subjects, recruitment, and procedures, is reported

elsewhere [2225]. Institutional Review Board approval was

obtained from the University of Pennsylvania and the ethical

committee for research at Jintan Hospital in China.

Measures
Blood lead concentrations in preschool (35 years). Blood

specimens were collected only once for each child, when they

were 3, 4, or 5 years old, during November 2004 and March

2005 by trained pediatric nurses using a strict research protocol

to avoid lead contamination. Samples were frozen and shipped

to the Research Center for Environmental Medicine of Children

at Shanghai Jiaotong University for the analysis of lead using

graphite furnace atomic absorption spectrophotometer [2527].

This laboratory has participated successfully in a CDC-

administered quality-control program (Blood Lead Proficiency

Testing Program) for the measurement of lead in whole blood.

Analysis of each specimen was conducted using a replication

procedure, and the mean of the repeated measurements was

taken as the final measure. Blood lead reference materials for

quality control (QC) were provided by Kaulson Laboratories,

New Jersey. QC samples were inserted blindly among the study

samples (one QC sample in every 10 study samples. Limit of

detection (LOD) of blood lead concentration was 1.8 mg/dL and

half of LOD was imputed for 3 (0.2%) samples under LOD,

which was among multiple runs (mean LOD).

IQ at age 6 years. IQ was assessed by the Chinese version

and norms of the Wechsler Preschool and Primary Scale of

Intelligence Revised (WPPSIR) during childrens last year of

preschool. The test was constructed by Wechsler [28] to assess the

intelligence of children aged 37 years and consists of 5 verbal and

5 performance subtests [28]. Verbal subtests are combined to

produce a VIQ reflecting verbal skills and crystallized intelligence.

Performance subtests combine to produce a PIQ indicative of

visual-spatial skills and fluid intelligence. All 10 subtests are

combined to produce a Full Scale IQ (FIQ), which is widely

recognized as a good measure of general intelligence defined as an

average of all cognitive abilities. The Chinese WPPSI was

standardized in 1984 and has shown good reliability in Chinese

children [2932]. The test was administered by two research

assistants trained by a cognitive psychologist. Research assistants

who administered the WPPSI were blind to the blood lead

concentrations. Children were assessed in a quiet room at their

preschool. Detailed procedures and reliability are given in Liu &

Lynn [33] and Liu et al. [34].

School performance at age 810 years. School perfor-

mance was assessed by standardized city tests on 3 major subjects

in Chinese elementary schools: Chinese, Math, and English (as a

foreign language). The tests were administered to all children on

the same day during the final month of the Fall 2009 semester,

when children were in grades 35 (aged 810 years old). Each test

consists mainly of multiple-choice questions and is scored ranging

from 0100. A higher score indicates better performance on the

test.

Sociodemographic and other Confounding variables. Parents

completed a socio-demographic questionnaire to assess family

environment at the time of childrens IQ testing. Potential

confounding variables considered include parent educational

and occupational status, fathers smoking history and frequency,

and mothers smoking during pregnancy. Blood iron was also

analyzed at Nanjing Medical University using the same protocol

and at the same time as blood lead collection. Whole blood

concentrations of iron were determined by atomic absorption

spectrophotometry (BH model 5.100 manufactured by Beijing

Bohu Innovative Electronic Technology Corporation), with

duplicate readings taken with an integration time of two

seconds. Further details are provided elsewhere [35].

Representativeness of Groups
The current study used a sample of 1,341 children (603 girls,

738 boys) for whom blood lead was measured at age 3 years, 4

years, or 5 years, which accounts for 81% of our original cohort.

The remaining 19% of the data was either not collected (e.g.:

children either moved to other schools or did not respond or

refused to participate in follow up) or was unavailable (e.g.: blood

samples were not available) for this statistical analysis. Character-

istics of the children and their families are summarized in Table 1.

There were no significant differences in demographics between

children with and without blood lead data [25]. For those children

who participated in follow-up for IQ and school performance

compared to those who did not participate in follow-up, blood lead

concentrations did not differ (t = 1.56; P = 0.120). Meanwhile,

complete data on both the IQ and school performance variables

were available on 561 subjects. Those with and without complete

data were compared on gender, age and grow-place, variables that

were available on all subjects at age 6. There was no significant

difference between those with complete data and those without

complete data on gender, age and grow-place. Therefore, the

Low Lead Levels and IQ and School Performance

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subjects with complete data are able to represent those without

complete data.

Statistical Analysis
Sample characteristics were summarized by descriptive statistics

such as mean, standard deviation (SD), and percentage. To

examine the association between blood lead concentration and

cognitive function and school performance, we computed bivariate

correlations between blood lead concentration and IQ (VIQ, PIQ,

and FIQ) and scores on Chinese, Math, and English. We used a

nonlinear approach to model the relationship between blood lead

concentration and IQ by a locally weighted polynomial regression

LOESS model, with estimated 95% confidence band. We

identified 8.0 mg/dl, equal to the 80th percentile, as the blood
lead concentration at which IQ started to decline. We then divided

children into 4 groups according to their blood lead concentration:

,6.0 (median), 6.08.0 (median to 80
th

percentile), 8.010.0, and

$10.0 mg/dl. Because the first 2 groups had no significant
differences in both IQ and school performance (data available

upon request), we merged them and included 3 categories for this

report: blood lead concentration ,8.0, 8.0 to ,10 (810), and

$10 mg/dl.
A series of analysis of variance (ANOVA) were performed to

examine the association between different concentrations of blood

lead and mean scores of IQ and school performance. General

linear models (GLM) were performed to examine the adjusted

associations between blood lead concentration and IQ and school

performance while controlling for child age at blood lead test,

child gender, residence as defined as school location, blood iron

level, parent education, parent occupation, and fathers smoking.

Maternal smoking was not included for analysis as only 3 mothers

reported smoking. These demographic variables were selected on

the basis of our previous study [25] and/or our preliminary

analyses indicating these variables were associated with either or

both blood lead concentration and IQ or school performance.

Finally, we examined if PIQ mediated the association between

blood lead concentration and school performance. We chose PIQ

as the potential mediating variable because PIQ is significantly

correlated with both the predictor (blood lead concentration) and

outcome measure (school performance), and PIQ was measured

before school performance data was collected. These two criteria

meet the conditions established by Baron and Kenny for potential

mediator variable [36]. A p-value,.05 was considered significant.

A nonlinear relationship between blood lead concentration and IQ

was done using R(2.14.0) loess model. All other analyses were

performed using SPSS, Version 17 (Chicago, IL).

Results

Sample characteristics
The sample consisted of 603 girls (45.0%) and 738 boys (55.0%),

with a mean age of 4.84 years (SD = 0.86) at blood lead testing.

Child and family characteristics of the sample are summarized in

Table 1. Mean blood lead concentration was 6.43 mg/dL
(SD = 2.64). Blood lead concentration was distributed as follows:

7.8% of children were $10.0 (N = 105), 13.8% were 8.010.0

(N = 185), 32.8% were 6.08.0 (N = 440), and 45.6% were ,6 mg/
dL (N = 611).

Bivariate correlations between blood lead concentration,
IQ, and school performance

Mean IQ and standardized test scores and their bivariate

correlations are shown in Table 2. Blood lead concentration was

significantly and negatively related to PIQ and scores of Chinese,

Math, and English. FIQ was highly correlated with VIQ and PIQ;

the correlation between VIQ and PIQ was moderate. Chinese,

Math and English were moderately correlated. The correlations

between FIQ, VIQ, and PIQ and Chinese, Math, or English were

low to moderate.

The nonlinear relationship between blood lead concentration

and FIQ, PIQ, and VIQ, with estimated 95% confidence bands is

shown in Figure 1. FIQ started to decline at blood lead

concentration 8 mg/dl. Although both PIQ and VIQ declined at
blood lead concentration 8 mg/dl, PIQ and VIQ at blood lead
concentration ,8 mg/dL showed different patterns.

Table 1. Sample characteristics.

N` %

Sex 1341

Male 738 55.0

Female 603 45.0

Age at blood lead
test, Mean (SD)

1341 4.84(0.86)

3 years 316 23.6

4 years 415 30.9

5 years 610 45.5

Residence/schools 1341

City (Jianshe) 538 40.1

Suburban
(Huacheng)

521 38.9

Rural (Xuebu) 282 21.0

Fathers education 1304

#Middle school 503 38.6

High school 420 32.2

College or higher 381 29.2

Fathers occupation 1262

Unemployed 52 4.1

Physical worker 718 56.9

Professional worker 492 39.0

Mothers education 1305

#Middle school 657 50.3

High school 384 29.4

College or higher 264 20.2

Father smoking 1273

No 563 44.2

Occasionally 454 35.7

Several times/wk 41 3.2

,10 cigarettes/wk 127 10.0

1020 cigarettes/wk 71 5.6

.20 cigarettes/wk 17 1.3

Iron Status Mean (SD) 1341 8.13 (0.83)

Blood lead (mg/dL) Mean (SD) 1341 6.43(2.64)

,6.0 611 45.6

6.0 to ,8.0 440 32.8

8.0 to ,10.0 185 13.8

$10.0 105 7.8

`
Number of children differs across sample characteristics due to missing values.

doi:10.1371/journal.pone.0065230.t001

Low Lead Levels and IQ and School Performance

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Differences in IQ and school performance across blood
lead concentrations

IQ and school performance means (SD) by 3 categories of blood

lead concentration ($10.0, 8.010.0, and ,8 mg/dl) is presented
in Table 3. All scores declined with increased blood lead

concentration. Compared to the blood lead concentration

,8 mg/dL group, the blood lead concentration 8.010.0 mg/dL
group showed a significant 3.71 point PIQ decline and a 2.69

point FIQ decline. The change of VIQ was minor, about 1 point

decline.

Compared to the blood lead concentration ,8 mg/dL group,
the blood lead concentration 8.010.0 mg/dL group also had
significantly lower scores in Chinese, Math, and English. The

mean scores significantly declined by 56 points in the blood lead

concentration 8.010.0 mg/dL group compared to blood lead
concentration ,8 mg/dl. Mean scores did not significantly differ
between blood lead concentration 8.010.0 and $10.0 mg/dL
groups.

Multivariate analysis of blood lead concentration on IQ
and school performance

The independent effects of blood lead concentration on IQ and

school performance were examined using GLM analyses to adjust

for child and family factors. Children with blood lead concentra-

tion $10.0 mg/dL scored approximately 2 points lower on PIQ
and VIQ than those children with blood lead concentration

,8 mg/dl (Table 4). However, associations were not significant
after adjusting for potential confounders. All Chinese, Math, and

English scores significantly declined with elevated blood lead

concentration. Math scores declined the most, followed by English

and Chinese. Illustratively, compared to children with blood lead

concentration ,8 mg/dl, those with blood lead concentration 8.0
10.0 mg/dL scored 35 points lower on Chinese (b = 23.20,
95%CI = 25.78, 20.63), Math (b = 25.25, 95%CI = 28.14,
22.36), or English (b = 24.33, 95%CI = 27.32, 21.34). Mean-
while those with blood lead concentration $10.0 mg/dL scored
much lower (Chinese, b = 24.02, 95%CI = 27.11, 20.93; Math,
b = 25.27, 95%CI = 28.73, 21,81; English, b = 25.18,
95%CI = 28.76, 21.59) compared to children with blood lead

concentration ,8 mg/dl.

Mediating effect of PIQ on blood lead concentration and
school performance

Blood lead concentration and IQ were both significantly

correlated with the three school tests, and blood lead concentra-

tion was significantly correlated with only PIQ (Table 2).

Consequently, it is possible that reduced PIQ could mediate the

main effect of blood lead concentration on school performance.

This possibility was tested by adding PIQ to Model 1 while

adjusting for child, school, and family factors (Table 4). As shown

in Model 2, blood lead concentration 8.010.0 mg/dL and
$10.0 mg/dL were still significantly associated with reduced

Table 2. Pearson correlations between blood lead concentrations and IQ and school performance.

Mean (SD) N`
Blood lead
concentration VIQ PIQ FIQ Chinese Math

Blood lead concentrations (mg/dL) 6.43(2.64) 1341 1.00

IQ VIQ 103.95(14.84) 1331 .011 1.00

PIQ 104.06(15.07) 1331 2.056* .498*** 1.00

FIQ 104.19(14.38) 1331 2.026 .869*** .857*** 1.00

School Performance Chinese 87.87(11.11) 561 2.234*** .241*** .344*** .305*** 1.00

Math 88.80(11.67) 561 2.200*** .242*** .391*** .375*** .511*** 1.00

English 89.58(13.22) 562 2.207*** .153*** .334*** .294*** .666*** .696***

*p,.05;
**p,.01,
***p,.001.
`
Number of children differs across sample characteristics due to missing values.

doi:10.1371/journal.pone.0065230.t002

Figure 1. FIQ, VIQ, and PIQ test scores by blood lead
concentration (mg/dl) with estimated 95% confidence bands.
Note: The dotted lines y-intercept is at the mean IQ test score.
doi:10.1371/journal.pone.0065230.g001

Low Lead Levels and IQ and School Performance

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scores on Chinese, Math, and English except for Chinese in

children with blood lead concentration 8.010.0 mg/dl. Compared
with blood lead concentration ,8 mg/dL at ages 35 years, blood
lead concentration $10 mg/dL was associated with 35 points
reduction on school tests at age 810 years (Chinese, b = 23.60,
95%CI = 26.58, 20.62; Math, b = 24.64, 95%CI = 27.91,
21.34; English, b = 24.62, 95%CI = 28.05, 21.18). However,
the effect as measured by regression coefficient was reduced,

indicating that the associations between blood lead concentration

and school tests were partially mediated by PIQ.

Discussion

Lead exposure is an important public health concern, especially

in countries that are developing or undergoing rapid economic

growth with limited environmental regulations [3739]. However,

little is known about the negative impact of low blood lead

concentration on later cognitive function in these developing

countries, where lead levels may be six-fold higher than in the US

[3840]. This study examined the association between blood lead

concentration in children at 35 years, their IQ at 6 years, and

school performance at age 810 years. We report several key

findings. First, elevated blood lead concentration in early

childhood was associated with reduced IQ at age 6 years,

particularly for PIQ (visual-spatial skills). Second, even after

adjusting for potential confounding variables, including prenatal

smoke exposure (exposed to fathers smoking) and iron deficiency

in childhood, elevated blood lead concentrations were also

significantly associated with reduced scores on standardized school

tests at age 10 years. Third, IQ partially mediated the blood lead

concentration and school performance relationship. Finally and

importantly, significant impairments were identified at even 8

10 mg/dL, supporting the view that lead exposure, even ,10 mg/
dL, is a risk factor for long-term cognitive impairment in children

and from a preventative perspective suggests that reduced early

childhood lead exposure could promote childrens long-term

cognitive development and school performance.

Our findings extend previous evidence for an inverse relation-

ship between blood lead concentration and IQ (e.g.: [3,5]). Our

results confirm previous findings by Chandramouli et al. [11] that

blood lead concentration ,10 mg/dL in early childhood my affect
later academic achievement. The present study importantly

reports on both childrens early IQ and later academic achieve-

ment, two different indicators of childrens cognitive performance

which both have important late-life health and quality-of-life

outcomes [4143].

Because of the time gap between IQ and academic achievement

assessment and because PIQ was significantly correlated with both

blood lead concentration and school performance, we were able to

observe a partial mediating effect of PIQ for the blood lead

concentration -academic achievement relationship. We hypothe-

size that lead exposure negatively effects brain growth and

development, and that brain alterations are linked to school

performance. The exact mechanism between lead exposure and

school performance is unclear. Lead is a neurotoxicant, and

animal studies suggest that lead exposure may lead to altered brain

biochemistry [44], which in turn may result in a disorder of

Table 3. Mean IQ and 2009 school performance by blood concentrations of lead in preschool children.

Blood concentrations of lead (mg/dL) ANOVA Post-hoc analysis, LSD (p)

,8 (A) 8- ,10(B) $10 (C) F p A vs. B A vs. C B vs. C

IQ N = 1016 N = 182 N = 103

PIQ 104.46(14.93) 103.32(15.58) 100.75(16.03) 3.04 .048 .349 .018 .168

VIQ 104.23(14.80) 103.65(15.03) 103.08(14.65) 0.36 .696 .627 .453 .755

FIQ 104.55(14.36) 103.66(14.22) 101.86(15.25) 1.78 .169 .442 .072 .313

School performance N = 421 N = 79 N = 49

Chinese 89.33(9.20) 83.44(13.97) 82.12(16.67) 17.30 .000 .000 ,.001 .503

Math 90.32(9.20) 84.29(14.66) 83.04(19.42) 16.32 .000 .000 ,.001 .545

English 91.29(10.41) 84.16(18.10) 83.37(19.71) 16.59 .000 .000 ,.001 .732

doi:10.1371/journal.pone.0065230.t003

Table 4. Impact of blood concentrations of lead on IQ and
school performance in Chinese preschool children (n = 1341).

Blood concentrations of lead (mg/dL)

,8.0 8.0 ,10.0 $10.0

IQ (Model 1)

PIQ Ref 20.96 (23.28, 1.36) 21.90 (24.89, 1.09)

VIQ Ref 20.48 (23.36, 2.40) 21.77 (24.01, 0.46)

FIQ Ref 21.28 (24.01, 1.46) 21.45 (23.50, 0.67)

School
performance

Chinese: Model 1 Ref 23.20 (25.78, 20.63)* 24.02 (27.11,
20.93)*

Model 2 Ref 22.67 (25.16, 0.18)* 23.60 (26.58,
20.62)*

Math: Model 1 Ref 25.25 (28.14, 22.36)** 25.27(28.73,
21,81)**

Model 2 Ref 24.46(27.20, 21.72)** 24.64(27.91,
21.36)**

English: Model 1 Ref 24.33 (27.32, 21.34)* 25.18 (28.76,
21.59)**

Model 2 Ref 23.62 (26., 20.75)* 24.62 (28.05,
21.18)*

*p,.05,
**p,.01.
Model 1: Adjusting for age at blood lead test, sex, blood iron, school, fathers
education, mothers education, fathers occupation and smoking.
Model 2: Adjusting covariates in model 1 plus PIQ.
doi:10.1371/journal.pone.0065230.t004

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plasticity [45] and learning impairments. Our findings suggest that

lead may first alter brain development in children [4649] that

subsequently impede further school achievement. This hypothesis

is further supported by a functional neuroimaging study demon-

strating an inverse correlation between childhood blood lead

concentration and activation of the left frontal cortex and middle

temporal gyrus, brain regions undergoing rapid development to

support language capabilities, during young adulthood [49]. While

Yuan et al. also found that dormant circuits in the right

hemisphere appeared to be recruited to compensate for these

brain deficits circuitry, such a compensatory pathway may not

necessarily produce equivalent performance to that achieved by

the normative cortical circuitry, and may thus still lead to poorer

long-term academic achievement [49].The impairing effects of

lead exposure on the brain also extends to adults: structural

imaging shows that accumulated occupational lead exposure in

adults is associated with changes in cerebral white matter which

further affects motor performance [50]. Since PIQ was observed

to have a partial mediating effect, our findings also suggest that

blood lead concentration may negatively impact other facets of

development, such as behavior, that also contribute to reduced

school performance. Furthermore, cognitive deficits which were

not directly measured, such as poor motivation and self-discipline,

may also lead to poor academic achievement [51].

In our sample, blood lead concentration was more strongly

associated with PIQ than VIQ. Poorer performance on visual-

spatial and visual-motor functioning tests are reported in previous

studies of lead exposure [5256]. Notably, by using a large sample

size

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