American Journal erf Epidemiology
Copyright © 1999 by The Johns Hopkins University School of Hygiene and Public Health
All rights reserved
Vol.149, No. 8
Printed in USA.
Lifetime Low-Level Exposure to Environmental Lead and Children's
Emotional and Behavioral Development at Ages 11-13 Years
The Port Pirie Cohort Study
J. M. Burns,1 P. A. Baghurst,1 M. G. Sawyer,2 A. J. McMichael,3 and Shi-lu Tong4
The Port Pirie Cohort Study is the first study to monitor prospectivety the association between lifetime blood
lead exposure and the prevalence of emotional and behavioral problems experienced by children. Lead
exposure data along with ratings on the Child Behavior Checklist were obtained for 322 11-13-year-old children
from the lead smelting community of Port Pirie, Australia. Mean total behavior problem score (95% confidence
interval (Cl)) for boys whose lifetime average blood lead concentration was above 15 u.g/dl was 28.7 (24.6-32.8)
compared with 21.1 (17.5-24.8) in boys with lower exposure levels. The corresponding mean scores (95% Cl)
for girls were 29.7 (25.3-34.2) and 18.0 (14.7-21.3). After controlling for a number of confounding variables,
including the quality of the child's HOME environment (assessed by Home Observation for Measurement of the
Environment), maternal psychopathology, and the child's IQ, regression modeling predicted that for a
hypothetical increase in lifetime blood lead exposure from 10 to 30 u.g/dl, the externalizing behavior problem
score would increase by 3.5 in boys (95% Cl 1.6-5.4), and by 1.8 (95% Cl -0.1 to 11.1) in girls. Internalizing
behavior problem scores were predicted to rise by 2.1 (95% Cl 0.0-4.2) in girls but by only 0.8 (95% Cl -0.9 to
2.4) in boys. Am J Epidemiol 1999;149:740-9.
affective symptoms; child; child behavior; lead; prospective studies
In 1979, Needleman et al. (1) identified a positive
association between dentine lead levels and teacherrated childhood behavior problems in a large-scale
study of children in first and second grade at school.
Subsequently, similar findings were reported in studies
conducted in Europe, New Zealand, and the United
States (2-9). Bellinger et al. (10, 11) found that tooth
lead levels were positively associated with behavior
problems reported by the teachers of 8-year-old US
children, while Fergusson et al. (12) reported that higher tooth lead levels at 6-8 years were associated with an
increased prevalence of emotional and behavioral problems in New Zealand children at age 8 years and again
at 12-13 years.
Previous studies have suffered from a number of
important limitations. In particular, the reliance on
cross-sectional study designs excluded the possibility
of examining the temporal relations between lead exposure and childhood behavior, and the opportunistic
nature of many early studies rendered them vulnerable
to criticisms with respect to statistical power, selection
bias, and inadequate adjustment for confounding factors (13). The aspects of lead exposure which are
reflected in a single dentine lead level are also unclear.
To our knowledge, the Port Pirie Cohort Study is the
largest prospective study of children exposed to environmental lead. Since the study commenced, information has been collected on both the prenatal and postnatal blood lead exposure of participating children, and
on a range of other factors that have the potential to
influence the prevalence of childhood emotional and
behavioral problems. This paper describes the relation
between lifetime blood lead exposure and the prevalence of emotional and behavioral problems when the
children were aged 11-13 years.
Received for publication September 26, 1997, and accepted for
publication August 25, 1998.
Abbreviations: Cl, confidence interval; HOME, Home Observation
for Measurement of the Environment; OR, odds ratio; PbB, Wood
lead concentration.
' Division of Human Nutrition, Commonwealth Scientific Industrial
Research Organisation, Adelaide, SA, Australia.
2
Department of Psychiatry, University of Adelaide, Adelaide, SA,
Australia.
3
Department of Epidemiology and Population Health Sciences,
London School of Hygiene and Tropical Medicine, London, England.
4
Department of Public Health, Queensland University of
Technology, Brisbane, Old, Australia.
MATERIALS AND METHODS
Study population
The original Port Pirie Cohort study population consisted of 723 subjects recruited during the 3-year period from May 1979 to May 1982, and included approx740
Lead Exposure and Behavior in Children Aged 11-13 Years
imately 90 percent of all live births in the study area
during this period (14). Subjects were periodically
assessed from birth until age 7 years, and detailed
reports have been published elsewhere (15-21).
The base population for the present study comprised
494 children who were assessed at age 7 years. No
attempt was made to evaluate 21 children for whom
more than two previous blood lead measurements were
missing, and one child was excluded from the study
because of a head injury. Of the 472 eligible children,
55 (11.7 percent) could not be located; 42 families (8.9
percent) refused to participate; and a further 5 families
(1.0 percent) lived too far outside the study area. The
parents of two children failed to return a useable
checklist of behavioral/emotional problems; and difficulties in obtaining a sample of venous blood reduced
the number of children with analyzable data from 370
to 322.
The 353 children born into the cohort but subsequently lost to follow-up were not significantly different from die 370 who remained in the study at age
11-13 years with respect to 20 out of 23 variables chosen for comparison. Children lost to follow-up were
more likely to have a lower birth weight (3,286 g vs.
3,398 g, p = 0.05), to have a younger mother (25.3
years vs. 26.4 years, p = 0.01), and to have a fadier
who had been at secondary school for longer (3.6 years
vs. 3.4 years, p - 0.05), but otherwise were similar to
die study children (21). The mean umbilical-cord
blood lead concentrations for the two groups were very
close (8.4 vs. 8.1 |ig/dl).
Lead exposure measures
Cumulative blood lead exposure was estimated
using exposure measures collected throughout each
child's involvement in the cohort. An umbilical cord
sample was collected from each child at birth, and
postnatal blood samples were obtained by finger prick
(capillary) at ages 6, 15, and 24 months and each year
thereafter until the child was 7 years of age. In the
most recent assessment, a venous blood sample was
collected at age 11-13 years. A rigorous cleansing and
strict collection protocol was employed at every blood
sampling (14).
Blood lead concentrations were estimated using electrothermal atomization atomic absorption spectrometry
(22). Analytical techniques were subject to both internal and external (inter-laboratory) quality-control procedures with consistently satisfactory results (23).
Estimates of blood lead concentration were standardized to a packed-cell volume of 50 percent for cord
blood and 35 percent for all other samples.
Average lifetime blood lead concentration (lifetime
PbB) for each child was estimated by trapezoidal inteAm J Epidemiol
Vol. 149, No. 8, 1999
741
gration under his/her profile of blood lead concentration by age. To prevent a few extremely high exposure
values from exerting too great an influence on estimation procedures, the logarithm of die blood lead concentration was used routinely in all statistical analyses.
Assessment of childhood behavior problems
Emotional and behavioral problems of children who
participated in the study were assessed using the Child
Behavior Checklist, which was completed by their
mothers (24). The checklist was chosen because it is
designed to collect data in a standardized way and it
provides ratings of emotional and behavioral problems
in a range of areas. For each of 118 items comprising
the behavior problem section of the questionnaire, parents were asked to rate their child's behavior "now or
within the past 6 months" using a 3-point scale (0 = not
true (as far as you know); 1 = somewhat or sometimes
true, 2 = very true or often true). A total behavior problem score comprising the sum of all the scores on the
behavior items was obtained from the checklist. In
addition, two broadly based scales labeled "internalizing" and "externalizing" were also scored. The internalizing score rates fearful, inhibited, or overcontrolled behavior, while the externalizing score rates
aggressive, antisocial, or under-controlled behavior.
Eight "narrowband" factors, labeled "withdrawn,"
"somatic complaints," "anxious/depressed," "social
problems," "thought problems," "attention problems,"
"delinquent behavior," and "aggressive behavior," rate
more specific areas of children's emotional and behavioral functioning. The checklist has been widely used
in US, Dutch, and Australian studies of bodi community and clinic-referred children and there are extensive data that support its reliability and validity (24).
Other variables that influence children's
development
During die course of die study, a number of factors
which may influence the development of children were
also assessed. These included parental smoking habits,
years of parental secondary education, birth weight,
duration of breastfeeding, die quality of die children's
HOME environment (assessed by Home Observation
for Measurement of die Environment (25)), and maternal intelligence quotient (IQ) (26).
At die 11-13-year assessment, die psychological
adjustment of die parent who completed die Child
Behavior Checklist was assessed widi die use of the
12-item version of die General Healdi Questionnaire
(GHQ) (27). The GHQ is a self-administered questionnaire designed to identify individuals with nonpsychotic psychological impairment. It has been widely
742
Burns et al.
used in Australian populations, and appropriate normative data are available (28). Family adjustment was
assessed using the 12-item general functioning (FADGF) scale of the McMaster Family Assessment Device
(29). Scores on the FAD-GF range from 1 to 4, with
higher scores indicating less healthy functioning.
Finally, the Wechsler Intelligence Scale for
Children-Revised was used to assess each child's
intelligence (30), and Daniel's Scale of Prestige of
Occupations in Australia (31) was used as a measure of
socioeconomic status.
Procedure
In the current assessment, a nurse-interviewer contacted each child's mother and arranged a home visit.
During the visit, a blood sample was taken for lead
determination, the Child Behavior Checklist was completed, and information was collected on other variables which might influence behavioral and emotional
development (24, 32). At all times, members of the
research team were blind to each child's blood lead
exposure history.
Statistical analyses
Simple associations between lifetime PbB and
behavior problem scores were examined separately for
boys and girls. Stratified analyses were conducted,
because it was anticipated that there might be genderspecific relations between lead exposure and specific
types of behavior problems (33, 34).
In multiple regression analyses, a change-inestimate criterion was used to identify confounding
variables; i.e., if inclusion of a variable produced a
change of more than 10 percent in the regression coefficient of blood lead concentration, it was deemed to
be a confounder.
RESULTS
Lifetime blood lead exposure and behavior
problems
Lifetime PbB was similar for both sexes (geometric
means: boys, 14.3 Hg/dl (95 percent confidence interval (CI) 13.5-15.1); girls, 13.9 ng/dl (95 percent CI
13.2-14.6)). Mean behavior scores (95 percent CIs) on
the total, internalizing, and externalizing scales of the
Child Behavior Checklist were, respectively: boys,
24.8 (22.2-27.4), 6.7 (5.8-7.5), and 9.4 (8.3-10.5);
girls, 23.6 (21.0-26.2), 7.7 (6.7-8.7), and 7.8
(6.8-8.7). These scores are very similar to those which
have been reported for children who live in the community (24).
The mean total behavior problem score together
with the externalizing and internalizing scores for
children above and below 15 (ig/dl are shown in table
1. The cutoff score of 15 |lg/dl was chosen for three
reasons. First, it corresponded closely to the median
of lifetime PbB. Second, it corresponds to the
Australian National Health and Medical Research
Council's current level above which actions to prevent
exposure should take place at the individual level
(35). Third, its use facilitated direct comparison with
other studies (5). Both boys and girls with higher lifetime blood lead concentrations had higher total behavior problem scores than children with lower lead levels. However, across the two groups, the difference in
the scores on the total behavior problem scale and the
externalizing scale were relatively small, and children
with higher lead concentrations had scores which
were substantially lower than those reported for children who attended mental health clinics (24). This
suggests that while children with higher lead concentrations may experience increased emotional and
behavioral problems, the size of this increase is relatively small and the scope of the children's problems
is less than that of children with clinically significant
disorders.
Mean narrow band behavior problem scores for
boys and girls with lifetime PbB above and below 15
Hg/dl are shown in figures 1 and 2, respectively.
Consistent with the pattern reported for the internalizing and externalizing scores, it can be seen that the
differences between the groups occur in boys primarily on the scales labeled, "attention problems," "delinquent behavior," and "aggressive behavior," while for
girls differences are evident in scores on several of the
narrow band scales including those labeled "withdrawn," "anxious/depressed," "social problems,"
"attention problems," "delinquent behavior," "aggressive behavior."
TABLE 1. Mean behavior problem scores (standard error)
obtained with the Child Behavior Checklist for boys and girls
with lifetime average blood lead concentrations at ages 11-13
years above and below 15 p.g/dl: the Port Pirle Cohort Study,
1979-1995*
Lifetime average Mood lead concentration, by sex
Type of
behavior
problem
Total
Internalizing
Externalizing
Girls
Boys
£15ng/dl
(n = 83)
21.1(1.9)
6.4 (0.6)
7.4(0.8)
= 76)
28.1(2.1)
7.1 (0.7)
11.4(0.8)
= 90)
18.0(1.7)
6.1 (0.7)
5.8(0.6)
29.7(2.3)
9.0 (0.8)
10.4(0.8)
* The differences in mean scores between high and low exposure groups are significant, in all comparisons, at p < 0.008 (or less)
with the exception of internalizing behavior problems for boys (p =
0.45).
Am J Epidemiol Vol. 149, No. 8, 1999
Lead Exposure and Behavior in Children Aged 11-13 Years
9
743
V
Lead Exposure Status
8
l<=15yg/dl •>15«ig/dl
7
6
Behavior 5
Problem
Score 4
•
3
2
1
FIGURE 1. Mean Child Behavior Checklist scores for boys aged 11-13 years according to lifetime blood lead exposure: the Port Pirie Cohort
Study, 1979-1995. Note: in figures 1 and 2, the number of Herns comprising the scales vary, e.g., aggressive behavior consists of 20 behavior
problems while thought problems consist of only seven behavior problems.
8
7•
> - « • • '
6
.
l
r
-
t
Lead Exposure Status
<=15Mg/dl •>15pg/dl
>
Behavior 5 •
Problem
Score
4•
3 •
2•
1•
0•
•
witr
r|
1 mUh
-l 1
s
a
i
9
t
3
,
3
i'
sr
FIGURE 2. Mean Child Behavior Checklist scores for girts aged 11-13 years according to lifetime Wood lead exposure: the Port Pirie Cohort
Study, 1979-1995.
Many characteristics of the family (i.e., HOME
environment and family functioning), the mother
(including age at child's birth, intelligence and psychopathology), and the father (including occupation
Am J Epidemiol
Vol. 149, No. 8, 1999
and years of secondary education) were strongly associated with behavior problems for boys and girls (table
2). Obstetric factors and neonatal characteristics were
not significantly related to behavior problems.
744
Burns et al.
TABLE 2. Association of selected variables with total behavior probtem scores on the Child Behavior
Checklist: the Port Plrte Cohort Study, 1979-1995*
Variable
Lifetime
Hood lead
concentration
Mean
SEt
n
Mean
14.9
14.0
26.0
22.2
2.1
1.8
83
70
24.5
20.3
1.9
1.7
87
82
16.3
14.1
14.3
29.8
24.4
21.1
2.8
1.8
2.5
50
74
50
26.7
23.2
17.1
2.0
2.1
2.2
68
81
41
16.5
14.2
30.3
23.0
3.4
1.4
41
132
28.7
20.6
2.6
1.3
55
131
16.3
14.8
14.8
16.5
26.4
24.0
5.0
2.1
1.9
6
88
77
31.3
21.5
24.4
5.3
1.8
2.1
11
98
80
15.1
14.8
14.5
27.4
26.8
17.2
2.2
2.2
2.4
71
64
41
25.9
23.6
19.1
1.9
2.6
2.3
89
57
45
14.7
15.8
14.7
23.2
30.2
36.4
1.3
4.5
7.8
136
29
22.9
24.2
30.4
1.5
2.7
10.5
156
25
20.2
18.4
14.9
12.5
42.0
32.6
20.7
22.4
5.9
4.3
1.8
2.1
9
26
70
31.2
29.4
23.2
17.6
3.6
3.3
2.1
1.8
17.3
15.5
14.8
12.3
31.3
28.2
22.3
23.6
7.4
2.8
2.6
3.4
13
32
45
29
23.9
30.6
21.5
15.9
3.0
3.1
2.1
2.9
17
42
43
30
13.0
15.5
20.7
27.0
1.6
2.3
72
74
19.7
23.6
1.8
1.7
67
105
14.3
17.9
23.7
30.5
1.4
3.5
147
29
21.7
36.1
1.2
5.3
164
26
14.3
15.5
20.9
29.1
1.7
2.1
90
83
20.2
27.9
1.4
2.3
105
84
14.3
15.5
22.9
27.3
1.7
2.2
99
76
21.2
26.4
1.6
2.2
98
89
17.5
15.8
13.6
24.5
28.4
21.8
3.4
3.4
1.6
16
36
104
30.4
25.5
19.2
4.1
2.3
1.5
16
53
105
18.0
15.9
13.6
34.2
24.7
24.3
6.1
2.3
6
82
88
33.9
26.6
19.5
5.7
9
83
89
Girls
Boys
SE
n
Father's education level (years)}
£3
>3
Mother's age (years) at child's birth
<22
23-28
>28
Mother smoked during pregnancy
Yes
No
Birth weight (g)
<2,500
2,500-3,500
>3,500
Birth order
1st
2nd
£3rd
Feeding style
Breast
Bottle
Mixed
HOMEt score
<35 (worse)
35-^0
40-45
>45 (better)
Mother's IQf
£80 (tower)
81-90
91-100
>100 (higher)
Father's occupation
545.5 (better)
>45.5 (worse)
Marital status (1993)
Married
Not married
Maternal psychological impairment
59 (better)
>9 (worse)
Family functioning
51.83 (better)
>1.83 (worse)
No. of parents smoking
Both
One
None
Child's IQ
580 (lower)
81-100
> 100 (higher)
1.6
7
61
2.2
1.5
7
9
30
75
67
* To convert values from micrograms per deciliter to micromoles per liter, divide by 20.7.
t SE, standard error; HOME, Home Observation for Measurement of the Environment; IQ, intelligence quotient.
t Number of years of high school completed.
Am J Epidemiol
Vol. 149, No. 8, 1999
Lead Exposure and Behavior in Children Aged 11-13 Years
Regression analyses
Regression coefficients of (log) blood lead concentration were used to calculate expected increases in
behavior problem scores for hypothetical increases in
lifetime PbB (table 3). Thus, if lifetime PbB were to
rise from 10 |i.g/dl to 30 (ig/dl, such an increase would
be expected (ignoring other covariates) to be associated with an increase in total behavior problem scores of
5.0 for boys and 10.6 points for girls. After adjustment
for confounding, the predicted increase in total behavior problem scores would be 5.2 points for boys and
6.2 points for girls.
The relation between lifetime PbB and behavior
problem scores appeared to differ for boys and girls.
After adjustment for the covariates, the estimated
increase in the internalizing score was 2.1 points for
girls but only 0.8 points for boys. The estimated
increase in externalizing scores was 3.5 points for boys
and 1.8 points for girls.
To identify more specifically the nature of the emotional and behavioral problems associated with
increased lifetime PbB, regression analyses were also
conducted with scores from the narrow band scales,
with adjustment for the same set of confounding variables and covariates. Significant relations between lifetime PbB and behavior scores on the delinquent and
aggressive narrow band scales were observed for boys.
For girls, significant associations between lifetime PbB
and behavior scores were observed with scores on the
withdrawn, anxious/depressed, thought problem, attention problem, and aggressive behavior scales.
745
In order to ensure that the results of the multiple linear regression analyses were not unduly affected by
non-compliance with the underlying distributional
assumptions, multiple logistic regression analyses
were also performed on a binary outcome variable
indicating whether an individual's behavioral score
was above or below the median. The estimated regression coefficients were used to calculate adjusted odds
ratios associated with a hypothetical increase in lifetime PbB from 10 to 30 ng/dl (table 4). The relations
between lifetime PbB and behavior problem scores for
boys and girls were qualitatively similar to those
observed in multiple linear regression analyses.
Significant relations between lifetime PbB and total
behavior problem scores were observed for both boys
and girls. The risk of scoring above the median on the
total behavior problem scale increased 3.2-fold (95
percent CI 1.4-6.6) for boys and 2.8-fold (95 percent
CI 1.0-6.8) for girls when all covariates were entered
into the regression equation.
Total behavior problem scores and age-specific
lead exposure.
While it has often been argued that a strength of
prospective studies is their potential to identify timepoints at which a child is maximally sensitive to lead
exposure, it is apparent from the unadjusted mean
behavior problem scores presented in table 5 that it
was not possible to identify from the Port Pirie Cohort
Study data any age at which the effects of lead were
more obviously severe. This is almost certainly a con-
TABLE 3. Estimated changes in behavior problem scores from the Child Behavior Checklist which would accompany a hypothetical Increase In lifetime blood lead concentration at age 11-13 years from 10 to 30 u.g/dl: the Port Plrie Cohort Study,
1979-1995*
Estimated change in problem score
Boys (n = 159)
ChBd Behavior
Checklist
problem scales
Simple
regression
Change
"
Total problems
Internalizing problems
Externalizing problems
Withdrawn
Somatic complaints
Anxious/depressed
Social problems
Thought problems
Attention problems
Delinquent behavior
Aggressive behavior
5.0
0.2
3.1
0.1
-0.2
0.3
0.5
0.1
0.6
0.8
2.4
95%Clt
1.1
-1.1
1.6
-0.3
-0.6
-0.5
0.0
0.0
-0.1
0.3
1.2
Girts (n = 163)
Multiple
regression
to
to
to
to
to
to
to
to
to
to
to
8.8
1.5
4.7
0.6
0.2
1.0
0.9
0.3
1.4
1.2
3.6
Change
5.2
0.8
3.5
0.1
-0.1
0.8
0.4
0.0
0.3
0.9
2.7
Simple
regression
Multiple
regression
95% CI
Change
95% CI
Change
0.4 to 10.1
-0.9 to 2.4
1.6 to 5.4
-0.4 to 0.7
-0.7 to 0.4
-0.2 to 1.8
-0.2 to 1.1
-0.2 to 0.3
-0.6 to 1.3
0.3 to 1.4
1.3 to 4.1
10.6
2.8
3.9
0.8
0.7
1.4
1.0
0.4
1.4
0.7
3.2
6.9 to 14.4
1.4 to 4.2
2.6 to 5.2
0.4 to 1.1
0.2 to 1.1
0.6 to 2.3
0.6 to 1.5
0.2 to 0.6
0.9 to 2.0
0.4 to 0.9
2.1 to 4.4
6.2
2.1
1.8
0.6
0.3
1.3
0.3
0.3
1.1
0.2
1.6
95% CI
1.3
0.0
-0.1
0.0
-0.4
0.1
-0.3
0.1
0.3
-0.1
0.0
to
to
to
to
to
to
to
to
to
to
to
11.1
4.2
3.7
1.1
0.9
2.5
0.8
0.5
1.8
0.6
3.2
* The estimates are derived from multiple regression models containing terms in maternal age, smoking during pregnancy, birth weight,
type of feeding, length of breastfeeding, maternal education, maternal IQ,t father's education, maternal psychopathology, birth order, family
functioning, father's occupation, parents' smoking habits, marital status, HOMEt environment, and child's IQ.
t CI, confidence interval; IQ, intelligence quotient; HOME, Home Observation for Measurement of the Environment
Am J Epidemiol Vol. 149, No. 8, 1999
746
Burns et al.
TABLE 4. Estimated odds ratios (OR)*,t associated with an Increase In lifetime blood concentration from 10 to 30 ng/dl at age
11-13 years: the Port Pirle Cohort Study, 1979-1995
Boys (n = 159)
Simple
regression
problem
Total problems
Internalizing problems
Externalizing problems
Withdrawn
Somatic complaints
Anxious/depressed
Social problems
Thought problems
Attention problems
Delinquent behavior
Aggressive behavior
Girls (n = 183)
Multiple
regression
Multiple
regression
Simple
regression
OR
95% at
OR
95% Cl
OR
95% Cl
OR
95% Cl
1.7
0.9
1.6
1.0
0.7
1.0
1.3
1.8
1.5
1.7
1.6
1.0-2.6
0.6-1.4
1.0-2.5
0.7-1.6
0.5-1.2
0.6-1.5
0.8-2.1
1.1-3.0
0.9-2.3
1.2-3.0
1.0-2.6
3.2
1.2
1.7
1.5
0.8
1.9
1.7
1.8
1.2
2.8
1.9
1.4-6.6
0.6-2.2
0.8-3.3
0.7-3.1
0.3-1.6
0.9-4.0
0.8-3.0
0.8-4.0
0.6-2.3
1.4-5.8
1.0-4.3
2.8
1.9
2.5
2.7
1.9
1.9
3.1
2.3
2.0
2.0
2.3
1.7-4.6
1.2-3.0
1.5-4.1
1.7-4.5
1.2-3.0
1.2-3.1
1.8-5.3
1.3-4.0
1.2-3.3
1.2-3.1
1.4-3.6
2.8
3.8
2.0
2.6
1.5
3.1
3.3
§
2.0
2.3
1.9
1.0-6.8
1.4-11.0
0.^4.6
1.0-6.5
0.6-3.3
1.2-7.9
1.2-9.3
0.8-4.9
1.0-5.7
0.8-4.5
* Odds of having behavior scores on the Child Behavior Checklist above the median.
t The odds ratios are from analyses adjusting for maternal age, mother smoking during pregnancy, birth weight, feeding style, maternal
education, maternal IQ,t father's education, maternal psychopathology, length of breastfeeding, birth order, family functioning, father's occupation, parents' smoking, marital status, HOMEt- environment, and child's IQ.
$ Cl, confidence interval; IQ, intelligence quotient; HOME, Home Observation for Measurement of the Environment.
§ Insufficient data.
TABLE 5. Unadjusted, mean total behavior problem scores at age 11-13 years by quartile of agespecific blood lead concentration: the Port Plrle Cohort Study, 1979-1995
Blood lead exposure category, by sex and quartile
Boys
Maternal blood
Antenatal
At delivery
Child blood
At birth (cord)
6 months
15 months
2 years
3 years
4 years
5 years
6 years
7 years
11-13 years
Girls
I
II
III
IV
I
II
III
IV
21.0
21.3
24.0
27.4
28.9
27.2
25.9
25.8
16.5
18.4
20.9
25.2
23.2
25.2
29.6
26.4
23.2
22.7
21.1
22.2
22.3
21.4
21.2
22.0
23.8
22.0
26.3
23.4
24.7
21.1
22.0
22.9
23.4
22.1
21.6
24.8
23.2
26.3
23.9
25.7
27.9
28.7
23.1
22.8
21.8
22.3
28.1
26.7
30.6
29.3
27.3
26.4
30.7
31.8
33.3
31.2
17.3
16.5
17.0
15.5
14.7
14.1
16.6
16.9
16.1
17.8
25.3
23.6
20.2
19.4
23.8
24.3
19.3
20.2
20.9
26.3
25.1
23.7
23.8
26.1
29.2
24.3
27.2
24.2
24.0
20.5
25.7
30.2
32.3
35.0
29.2
30.9
31.4
35.7
33.7
35.1
sequence of the phenomenon referred to as "tracking,"
in which a child whose exposure rating is high at one
age is likely to remain relatively high at an older age
unless differential action is undertaken to influence
that child's environment. While only the crude scores
have been presented in table 5, regression analyses
which took into account the other factors shown in
table 2 yielded results for all postnatal exposure measures which were qualitatively similar to those that we
report for lifetime average exposures (not shown).
DISCUSSION
The results from this study suggest that there is a
significant relation between exposure to environmental lead and later childhood emotional and behavioral
problems. Lifetime PbB was significantly associated
with total behavior problem scores for both boys and
girls aged 11-13 years. For boys, this association
appeared to be largely due to behavior problems of an
externalizing nature. For girls, the association did not
Am J Epidemiol Vol. 149, No. 8, 1999
Lead Exposure and Behavior in Children Aged 11-13 Years
appear to be confined to either externalizing or internalizing behaviors but was present in both problem
areas. In stratified analyses, girls appeared to be more
susceptible to the effects of lead. However, when other
factors that may influence the association between lead
exposure and behavior problems were taken into consideration, the differences between boys and girls were
less apparent. These results are consistent with the
findings obtained by SciariJlo et al. (5) and Bellinger et
al. (10), who reported that increased lead exposure
resulted in a greater number of both internalizing and
externalizing behavior problems, but with no apparent
difference between the boys and girls.
Because this study cannot be used to infer causal
associations, it is useful to consider the evidence both
for and against the hypothesis that lifetime blood lead
exposure has long term effects on the prevalence of
behavioral and emotional problems that children experience.
There are a number of arguments in favor of this
hypothesis. First, the neurotoxic effects of exposure to
high levels of lead are well known and documented
(36-39), and case reports together with early clinical
studies of lead exposure have suggested a causal Link
between exposure and psychiatric status (40—44).
Second, adults exposed to lead in the work environment have been found to report a greater severity of
affective mood disturbances than do controls (45-47).
Third, animal experiments that have examined the
effect of lead exposure have found adverse effects on
both early mother-infant interaction and social play,
and have reported increased aggression and hyperactivity in exposed offspring (48). Fourth, meta-analytic
techniques suggest that chronic exposure to low lead
levels are associated with modest decrements in IQ in
children (38). The Port Pine Cohort Study has reported a consistent relation between lead exposure and
cognitive functioning in children at ages 2, 4, 7, and
11-13 years. Finally, several cross-sectional and
prospective studies (2-8, 10-12, 49) have reported
associations between increased lead exposure and the
prevalence of behavioral and emotional problems
experienced by children after adjustment for confounding variables. In the present study, the associations between lead levels and later outcomes persisted
after fairly extensive statistical adjustment for potential confounders. This adjustment was made for known
correlates and antecedents of lead exposure as well as
child's IQ.
Several arguments have been proposed in favor of
a non-causal association between lead exposure and
higher emotional/behavioral problems in children.
First, an association may be observed because children with higher problem scores also exhibit behavAm J Epidemiol
Vol. 149, No. 8, 1999
747
iors that result in increased lead absorption (e.g.,
playing in dust, thumb sucking, pica). To explore this
possibility, a measure of pica was entered into the
regression equation following the addition of lead
exposure. The regression coefficient for lifetime
exposure from birth to age 11-13 years actually
increased. In addition, the temporal relations between
developmental scores at ages 2, 4, and 7 years were
examined in relation to blood lead exposure at age
11-13 years. These early developmental scores were
not predictive of blood lead concentration later in
life. Second, the possibility cannot be eliminated that
we did not completely control for confounding variables and subsequently overestimated the true effect
of lead exposure. However, by the same token, it
might also be argued that some of the variables
included in the regression model may have influenced behavior through their effect on exposure, in
which case our analysis would have underestimated
the true effect of lead.
The fact that parents were aware of their child's
blood lead exposure is a potential concern. This
knowledge may have influenced parents' reports in
several ways. For example, some parents who were
aware that their children had been exposed to higher
levels of environmental lead may have tended to overreport behavior problems because they were anticipating the adverse effects of lead exposure. Alternatively,
parents who were aware that their child had been
exposed to higher levels of environmental lead may
have denied the existence of problems because of a
sense of guilt or responsibility for allowing their child
to be exposed to an adverse environmental influence.
Finally, many families have lived in Port Pirie for several generations without exhibiting "obvious" adverse
health affects of lead exposure, and parents from some
of these families may have experienced difficulties in
acknowledging that their children were exhibiting
emotional and behavioral problems.
Overall, the results indicate that any deleterious
effect of environmental lead is not likely to be large,
and that only a small fraction of the overall variation
in childhood emotional and behavioral problems can
be attributed to past lead exposure. Nevertheless, the
social consequences of such an effect are not negligible. Health authorities in the United States have
recently estimated that for each reduction of 1 (Xg/dl
(0.05 \imol per liter) in blood lead concentration due
to lead-exposure abatement programs, there would be
a net saving to society of approximately $2,000 US
per child (50, 51); and until such time as compelling
evidence to the contrary is available, policy makers
should treat low level lead exposure as a potential
source of harm to children.
748
Burns et al.
ACKNOWLEDGMENTS
This research was supported by a series of grants from the
National Health and Medical Research Council, the Channel
7 Children's Research Foundation, and the University of
Adelaide.
The authors thank Maureen Wauchope for blood sampling and interviews, Jim Lyster for supervising psychological assessments, Charles Greeneklee for assessing packedcell volume of blood samples, and Elaine Whitham for
blood lead analyses.
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