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Blackwell Publishing Ltd

Developmental Impacts of Heavy Metals and Undernutrition

Gail A. Wasserman1,2, Xinhua Liu3, Pam Factor-Litvak3, Julie Meeks Gardner4 and Joseph H. Graziano3
1
Division of Child and Adolescent Psychiatry, Columbia University, New York, NY, 2New York State Psychiatric Institute,
New York, NY, 3Mailman School of Public Health, Columbia University, New York, NY, USA, and
4
Caribbean Child Development Centre, University of the West Indies, Kingston, Jamaica
(Received April 12, 2007; Accepted September 21, 2007)

Abstract: A recent Lancet series highlighted enormous loss to young children’s developmental potential in developing
countries, from exposure to sociocultural and health risks. The possibility that nutritional deficiencies might exacerbate the
adverse impact of environmental exposures to developmental toxicants such as heavy metals and pesticides has not been
explored. While both arsenic and manganese exposures have known neurotoxicity in adults, systematic investigation in
young children has only recently begun. Five hundred and ninety 6- and 10-year-old Bangladeshi children participated in
three overlapping studies. Well-water arsenic and manganese were measured from home wells; urine and blood samples
were provided; and sociodemographic and household characteristics obtained. For new analyses, ‘stunting’ was defined as
2 or more standard deviations below the Centers for Disease Control and Prevention gender-specific height-for-age norms.
Developmental assessments employed culturally adapted variants of the WISC-III (age 10) or WPPSI-III (age 6). In prior
analyses, after adjusting for social factors, well-water arsenic and manganese were both significantly associated with poorer
developmental scores at age 10; associations for water arsenic at 6 years were significant, but attenuated. Negative associations
with metal exposures held up in newer analyses, and stunting was significantly associated with lower intellectual functioning
in analyses considering either metal. There were no significant stunting-by-metal interactions. Developmental risks often
co-occur. Millions in South Asia are exposed to naturally occurring arsenic and manganese through household wells.
Stunting affects more than 25% of young children in developing countries. The combined neurocognitive loss from both
risks, although rarely jointly studied, represents a substantial loss of global potential.

Several excellent reviews have considered the global impact
of environmental exposure to developmental neurotoxicants
[1,2]. A recent Lancet series [3–5] on risks for severely
compromised development in young children in developing
nations reviewed the evidence linking compromised develop-
ment with modifiable biological and psychosocial risks
encountered by children from birth to age 5 years.
The Lancet papers [3–5] focused on impact on children
from developing nations, in order to estimate global risk from
a wide range of adverse nutritional, social and environmental
factors. On the assumption that risks might operate differently,
or cumulatively, in children growing up in more marginalized
environments, the Lancet review panel identified a series
of research gaps. Beyond metals exposure, which has been
well-studied globally, there are several additional environ-
mental exposures for which solid evidence of neurotoxic
impact exists from studies in developed nations, but these
have either not been tested or have not been well-tested in
developing nations. These include studies of polychlorinated
Author for correspondence: Gail A Wasserman, New York State
Psychiatric Institute, 1051 Riverside Drive, Unit 78, New York,
NY 10032, USA (fax +1 (212) 543 1000, e-mail wassermg@
childpsych.columbia.edu).
biphenyl exposure, for which there are consistent reports of
infant psychomotor deficits in developed nations [6], but
which have not been examined in developing nations. Other
examples include methyl mercury exposure, with well-
documented adverse impact in developed nations [7] but
with a single study in a developing nation [8], and pesticides
[9]. Features that strongly limit scientific rigor in many other
studies in developing nations include the use of ecological
designs that do not measure individual exposure, and the
failure to adjust for social and individual covariates that are
likely to confound the exposure/outcome relationship.
One of the Lancet review papers [5] identified four key
risks with urgent need for intervention: stunting, inadequate
cognitive stimulation, iodine deficiency and iron deficiency
anemia. The authors also concluded that evidence was
sufficient to warrant public health interventions for five other
factors: heavy metals, malaria, intrauterine growth retardation,
maternal depression and exposure to violence. Collectively,
these risk factors affect millions of children around the
world. They also commonly co-occur, although the impact
of exposure to multiple risks has rarely been investigated in
children from developing nations.
Our group has been engaged for a number of years in the
study of developmental consequences of metals for young
children in developing countries. We examined intellectual

MiniReview METALS AND UNDERNUTRITION
development in a cohort of children whose mothers were
enrolled during pregnancy, through 12 years of age, some of
whom were exposed to high levels of lead from a smelter
and mining operation in Kosovo [10,11]. More recently, we
have examined intellectual development in cross-sectional
samples of 6- and 10-year-old Bangladeshi children exposed
to high concentrations of arsenic and manganese from
drinking water [12–14].
Here, we review the impact of growth deficiencies and
of metals exposure (lead, arsenic and manganese) on early
development. In new secondary analyses, we then consider
the joint impact of growth deficiency and metals exposure in
each of these cohorts.
Undernutrition
Early childhood undernutrition has been consistently asso-
ciated with continuing deficits in intellectual and school
functioning [15]. In developing countries, a third of children
below age 5 years (156 million) experience stunting [16].
Stunting is defined as height 2 standard deviations or more
below age standards, reflecting chronic undernutrition and
disease, rather than genetic differences. In young children,
patterns of growth are similar across countries [17]. Growth
problems generally begin before or soon after birth, and are
pronounced in the first 1.5 years of life. If not ameliorated
by approximately 40 months, stunting is likely to persist
through to adulthood [4]; there are almost no new incident
cases after early childhood. Stunted children show poorer
school progress or cognitive development in cross-sectional
studies in 17 developing nations around the globe. In six
other national studies, stunting between 1 and 3 years
predicted later measures of intellectual function or school
progress [4].
When food supplements are provided in randomized
trials, children show concurrent benefits to mental develop-
ment [18]. Studies that provide supplementation to children
before obvious signs of undernutrition have appeared gener-
ally report better outcomes than those supplemented after
malnourishment has occurred [5].
Metal exposures
Worldwide prevalence levels of elevated blood lead in
children are estimated to be approximately 40%, with children
in developing countries being at greater risk of exposure to
environmental lead than those in developed countries [19].
In both developing and developed nations, lead exposure is
associated with decrements in the range of 2–5 IQ points
that persist after adjustment for social confounders [11]. In
a longitudinal study of children living near a lead smelter in
Kosovo, modest deficits in intellectual, motor, visual-motor
and behavioural development appeared from age 2 through
10 years, even adjusting for social confounders [10]. Similar
results have appeared in other prospective studies of lead
exposure in the USA and in Australia, and have been
confirmed in a recent pooled analysis of the consequences of
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213
lead exposure [11], that considered studies of 1333 children
from seven sites in four countries.
In Bangladesh, we have examined the impact of naturally
occurring arsenic and manganese exposures from well-
water. While both arsenic and manganese exposures are
known to elicit neurotoxicity in adults, their systematic
investigation in young children has only recently begun. For
example, in a study in Mexico [20], urinary arsenic has been
associated with children’s lower verbal intelligence scores,
and in an ecological study in Taiwan [21] adolescents from
high exposure regions scored more poorly than those
from low exposure regions in some aspects of intellectual
function. In a study in Paris [22], preschoolers with high
manganese exposure from drinking water showed poorer
attention, non-verbal memory and hand skill, while in an
ecological study in China [23,24], 11–13-year-old from a region
with high exposure due to sewage scored poorly on similar
tests. Much of this work relies on ecological study, rather
than individual measures of exposure, and most such studies
provide little statistical adjustment for the social charac-
teristics that confound the exposure–outcome relationship.
A total of 590, 6- and 10-year-old children in Araihazar,
Bangladesh, were recruited for three overlapping studies. In
Bangladesh, 30–40 million people are exposed to high levels
of arsenic from household wells; in our study area, roughly
75% of wells exceed the WHO standard for arsenic of 10 µg/l
and 80% of wells exceed the WHO standard for manganese
(400 µg/l). All children were the offspring of adults from a
cohort of approximately 12,000 being studied by a multi-
disciplinary team; all participants receive regular medical
care at our clinic.
In Study 1 (table 1), we examined a random sample of
201 10-year-old children, nearly all of whom (n = 196)
used their own household wells. Children were assessed on a
culturally adapted variant of the WISC-III [12]. While
Study 1 children had a range of exposures to arsenic, we had
not selected them on the basis of their water manganese
exposure. Accordingly, for Study 2 we included the 54
children whose home wells were very low in arsenic (<10 µg/l)
and supplemented the sample with 88 newly recruited 10-
year-old children with similarly low arsenic exposure and a
range of manganese exposures [13]. Study 3 examined
intellectual function on an adaptation of the WPPSI-III in a
random sample of 6-year-old children in relation to arsenic
exposure [14].
For all studies, well-water arsenic and manganese were
measured from children’s household wells; urine and blood
samples were provided; and sociodemographic and house-
hold characteristics obtained. Water samples were analysed
by graphite furnace atomic absorption (GFAA) method;
samples whose water arsenic was less than the GFAA detec-
tion limit of 5 µg/l were subsequently analysed by mass
spectrometry (ICP-MS) [25] whose detection criterion was
0.1 µg/l. Children came for developmental assessments to
our local clinic. Because these tests were not standardized
for Bangladesh, and because cultural adaptation had
resulted in item deletions and substitutions, we examined
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214 GAIL A. WASSERMAN ET AL. MiniReview

Table 1.
Characteristics of participants in three studies of exposure in Bangladesh.
Study 1 Study 2 Study 3
Arsenic age 10 Manganese age 10 Arsenic age 6
Measure n = 201 n = 141* n = 301
Male (%) 48.8 50.3 49.8
Child height (cm) 125.6 126.5 108.5
Paternal education (years) 3.7 3.9 3.7
Maternal education (years) 2.9 3.1 3.3
Father is a labourer/farmer 23.5% 34.5% 18.3%
Father is a factory worker 33.3% 34.5% 35.6%
House type
Thatched roof or poorer 10% 13.5% 13.6%
Corrugated tin 74.1% 71.6% 78.1%
Concrete construction 15.2% 14.8% 8.3%
Maternal Raven score (intelligence) 14.4 14.1 14.2
Water arsenic (µg/l) 117.8 3.0 120.1
Urinary arsenic (µg/l) 116.6 57.5 110.7
Water manganese (µg/l) 1386 797 1302
*One child from the original 142 was missing information on height, and was dropped from these analyses.

raw item totals for scores from WISC-III or WPPSI-III
tests. We used multiple regression analyses to predict test
scores from exposure, adjusting for potential confounders.
Table 2 presents unadjusted and adjusted associations
with intellectual function for both metals exposure. Before
adjustment, in Study 1, arsenic exposure was significantly
associated with all aspects of intellectual function. Before
adjustment, in Study 2, manganese exposure was signifi-
cantly associated with all aspects of intellectual function. In
Study 1, after adjusting for maternal education, maternal
intelligence, quality of house construction (as a marker for
socio-economic status: concrete, tin, thatched roof), child
stunting and television access (as a marker of stimulation),
well-water arsenic was significantly associated with
poorer scores on the Performance and Full Scale measures
of intellectual function. In Study 2, in which water arsenic
was exceeding low (mean = 3 µg/l), well-water manganese
was negatively associated with children’s Verbal, Perform-
ance and Full Scale scores, even after adjustment for
maternal education and intelligence, house type, television
access, stunting, and water arsenic. In Study 3, well-water
arsenic was negatively associated with children’s Perform-
ance and Processing Speed scores, even after adjustment for
maternal education and intelligence, child school attend-
ance, stunting, water manganese and childrearing qualities
of the home. The prevalence of undernutrition is very high in

Table 2.
Predicting WISC-III raw scores from arsenic and manganese exposure and stunting.
Study 1 Study 2
Full Scale Performance Verbal Full Scale Performance Verbal
Variable raw score B raw score B raw score B raw score B raw score B raw score B
Unadjusted analyses
Water arsenic (log) –2.16*** –1.84*** –0.32* – – –
Stunting –7.67* –6.57* –1.09 –17.90*** –15.31*** –2.50**
Water manganese (log) – – – –5.20*** –4.43*** –0.80*
Adjusted analyses
Maternal education
None –10.92* –7.98* –2.95** –8.59 –5.08 –3.10*
1–5 years –3.54 –2.68 –0.86 –3.84 –2.46 –1.07
5–13 years – – – – – –
Maternal Raven score 0.37 0.40 –0.03 0.68 0.58 0.43
House type
Thatched roof or poorer –7.69 –6.16 –1.53 –1.36 –2.21 0.79
Corrugated tin –0.89 –0.72 –0.17 3.54 2.90 0.65
Concrete – – – – – –
Television access 5.92* 4.12 1.80* 3.72 3.07 0.41
Water arsenic (log) –1.79*** –1.57*** –0.22 – – –
Stunting –7.79* –6.67* –1.12 –16.20*** –13.72*** –2.36*
Water manganese (log) – – – –4.26** –3.70*** –0.60****
*P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.10.

© 2008 The Authors

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MiniReview METALS AND UNDERNUTRITION 215

Fig. 1. Raw scores by quartile of (A) water arsenic (As) for children who are stunted; (B) water As for children who are not stunted;
(C) water manganese (Mn) for children who are stunted; and (D) water Mn for children who are not stunted.

Bangladesh, and many of our participants were quite small
by Western standards. While each study had adjusted for
markers of growth (current height and head circumference),
we did not explicitly examine the role of stunting. In order
to examine the role of undernutrition in explaining these
results, and to consider whether grossly undernourished
children might have a particular vulnerability to the
impact of metals exposure, we conducted an additional set
of analyses of the children in Studies 1 and 2. International
growth standards exist for children only through 5 years,
and they have been found to apply adequately to children of
both high-resource and low-resource countries [17,26].
Therefore, following the procedures undertaken in the
Lancet papers, we relied on US norms for 10-year-old
children, defining children as ‘stunted’ if they were 2
standard deviations or more below the Centers for Disease
Control and Prevention gender-specific height-for-age
norms [27]. By this procedure, 45 children in Study 1 and
48 in Study 2 were characterized as stunted (respectively,
22% and 34%).
We repeated our regression analyses, adjusting for the
same variables as in the original studies, but in each case
replacing the terms for child height and head circumference
with a term for stunting, and then adding another for the
metal-by-stunting interaction. As table 2 shows, there was a
significant negative association between stunting and both
Full Scale and Performance Raw scores in Study 1, and for
all three measures of intellectual function in Study 2.
Including stunting in models did not alter the contribution
of other variables. In each case for which we had earlier
found a metals effect, we retained that effect even with
stunting in the model (except for a slight reduction in signifi-
cance for the impact of water manganese on Verbal score).
The stunting-by-water arsenic interaction was consistently
negative for all three measures of intellectual function in
both Study 1 and Study 2 (data not shown), although none
of these interactions was significant.
Figure 1A–D presents dose–response associations for
stunted and non-stunted children, between both arsenic and
manganese exposure and intellectual function in 10-year-old
children. Examining the figure provides some insight into
the relative impact of metal exposures and stunting on intel-
lectual function. For example, at each level of stunting, as
arsenic exposure increases from the lowest to the highest
quartile, Full Scale scores decreased by 11.5 points. At each
level of stunting, as manganese exposure increases from the
lowest to the highest quartile, Full Scale scores decreased by
approximately 20 points. On the other hand, as compared
to not stunted children, stunted children from Study 1
(fig. 1A,B) received Full Scale scores that were lower by 7.9

© 2008 The Authors

Journal compilation © 2008 Nordic Pharmacological Society. Basic & Clinical Pharmacology & Toxicology, 102, 212–217

216 GAIL A. WASSERMAN ET AL.
points; in Study 2, stunted children received Full Scale
scores that were 15.8 points lower than those received by
not stunted children (fig. 1C,D). The relatively greater loss
resulting from stunting in Study 2 reflects the higher
functioning of Study 2 non-stunted children relative to
those in Study 1; stunted children have similar scores across
both studies. The greater impact of stunting in Study 2 may
be due to removing the effect of arsenic exposure by design.
Similar analyses considering our younger sample (Study
3) revealed essentially the same results for younger children
(data not shown). Finally, similar analyses considering lead
exposure and moderate stunting in our Kosovo data (data
not shown) also revealed no significant interactions in
predicting 4-year (in Kosovo) intelligence.
Conclusions
In re-analyses of data from our Bangladesh studies, we
found that exposure to well-water arsenic and manganese
and severe stunting were independently associated with
poorer children’s intellectual functioning. We found no
evidence of an interaction between stunting and either
exposure. On the other hand, the small sample size in all
these analyses would have made detecting interactions
difficult. In addition, the present cross-sectional design does
not rule out the possibility that metals exposure might have
direct impact on growth. Larger, longitudinal investigations
should consider these issues. However, calculations suggest
that increasing the n in Study 1 to 770 children would be
necessary if we were to reduce the standard error for the
arsenic by stunting interaction enough to reach a significant
effect (P < 0.05) for Performance scores and 1000 children
would be necessary to do so for Full Scale scores; even at
this sample size, the interaction term for Verbal scores
would remain non-significant.
Perspectives
Based on global estimates of the prevalence of early childhood
stunting and of children living in absolute poverty, the Lancet
paper [4] estimated that over 200 million children under the
age of 5 years are far from fulfilling their developmental
potential, with proportions largest in sub-Saharan Africa
and absolute numbers largest in South Asia. Unfortunately,
these numbers are likely to increase in the near future, with
increases in the use of pesticides and the transition from
agricultural to industrial economies, with often absent or
insufficient regulation of use.
A third paper in the Lancet series [3] addressed strategies
to prevent or remediate these problems. If risk factors inter-
act synergistically to increase young children’s vulnerability,
interventions that target and prioritize cumulative risk will
need to be developed. On the other hand, if we consistently
look for, and fail to find interactions among risk factors that
predict poor outcome, this would suggest that we can draw
solid inferences from existing research on developmental
impact, so that the way may be clearer for systematic
© 2008 The Authors
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MiniReview
programmes intended to mitigate risk. As a final caution,
we should underscore that policy decisions must be based
on analyses of risk factors and their interactions that are
adequately powered.
Acknowledgements
This work was supported in part by two grants from the
National Institute of Environmental Health Sciences (P42
ES 10349, and P30 ES 09089).
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