Global Approach to Reducing Lead Exposure and Poisoning

This article appeared in a journal published by Elsevier. The attached
copy is furnished to the author for internal non-commercial research
and education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Author's personal copy
Mutation Research 659 (2008) 166–175
Contents lists available at ScienceDirect
Mutation Research/Reviews in Mutation Research
journal homepage: www.elsevier.com/locate/reviewsmr
Community address: www.elsevier.com/locate/mutres
Review
Global approach to reducing lead exposure and poisoning
Pamela A. Meyer a,*, Mary Jean Brown b, Henry Falk a
a
Centers for Disease Control and Prevention, Coordinating Center for Environmental Health and Injury Prevention, 1600 Clifton Road, NE, Mailstop F-64,
Atlanta, GA 30333, United States
b
Centers for Disease Control and Prevention, National Center for Environmental Health, Division of Emergency and Environmental Services,
Lead Poisoning Prevention Branch, Mailstop F40, Chamblee, GA 30341-3717, United States
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 10 January 2008
Received in revised form 3 March 2008
Accepted 4 March 2008
Available online 20 March 2008
Lead poisoning is an important environmental disease that can have life-long adverse health effects. Most
susceptible are children, and most commonly exposed are those who are poor and live in developing
countries. Studies of children’s blood-lead levels (BLLs) are showing cognitive impairment at increasingly
lower BLLs. Lead is dangerous at all levels in children.
The sources of lead exposure vary among and within countries depending on past and current uses.
Sources of lead may be from historic contamination, recycling old lead products, or from manufacturing
new products. In all countries that have banned leaded gasoline, average population BLLs have declined
rapidly. In many developing countries where leaded gasoline is no longer used, many children and
workers are exposed to fugitive emissions and mining wastes. Unexpected lead threats, such as improper
disposal of electronics and children’s toys contaminated with lead, continue to emerge.
The only medical treatment available is chelation, which can save lives of persons with very high BLLs.
However, chelating drugs are not always available in developing countries and have limited value in
reducing the sequelae of chronic low dose lead exposure. Therefore, the best approach is to prevent
exposure to lead. Because a key strategy for preventing lead poisoning is to identify and control or
eliminate lead sources, this article highlights several major sources of lead poisoning worldwide. In
addition, we recommend three primary prevention strategies for lead poisoning: identify sources,
eliminate or control sources, and monitor environmental exposures and hazards.
Published by Elsevier B.V.
Keywords:
Lead poisoning
Primary prevention
Hazard control
Environmental health
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Adverse health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Leaded gasoline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Smelters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3.
Battery recycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4.
Paint . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.
Traditional remedies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.6.
Electronics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Prevention strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Identify sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Eliminate or control sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3.
Monitor environmental exposures and hazards . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* Corresponding author. Tel.: +1 770 488 0548; fax: +1 770 488 0701.
E-mail address: [email protected] (P.A. Meyer).
1383-5742/$ – see front matter . Published by Elsevier B.V.
doi:10.1016/j.mrrev.2008.03.003
167
167
168
168
169
169
169
170
170
170
171
173
174
174
174
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
1. Introduction
Lead has been mined, smelted, and used in cosmetics, internal
and topical medicinal preparations, and paint pigments and glazes
since early recorded history [1]. As early as the second century B.C.,
the symptoms of lead poisoning were described by the Greek
physician, Nikander [2]. The harmful effects of lead poisoning in
workers and children were described in the 19th century [3]. By
the mid-1920s, studies detailed the dangers of cumulative doses of
lead, the vulnerability of children, and the harm to the nervous
system [3]. For years it was generally believed that children who
did not die during the acute stage of lead poisoning suffered no
long-term adverse health effects [4,5]. However, evidence of
adverse health effects that did not meet the diagnostic criteria for
neurologic disease but were associated with lower intellectual
functioning began to emerge in population-based epidemiologic
studies in the 1970s [6].
Despite growing evidence of adverse health effects related to
lead, it is still widely used in consumer products and released into
the air through combustion of coals and oil, waste incineration, and
fugitive emissions during mining and smelting. Many countries
have taken steps to control the use of lead. For example, lead in
household paint was banned in Australia in 1920 and by
international convention in 1925 [4]. The phase-out of lead in
gasoline began in the mid-1970s in the United States; many other
countries have also banned leaded gasoline. However, more must
be done to protect people in all nations. Worldwide a large number
of people are exposed, especially those in developing countries.
This article will highlight adverse health effects and several
sources of lead exposure reported internationally in the scientific
literature since 2000. We recommend three strategies to prevent
people worldwide from ever being lead poisoned.
2. Adverse health effects
Lead is a potent and pervasive neurotoxicant. The toxic effects
of lead are the same regardless of the route of entry into the body,
which are primarily ingestion and inhalation. Once absorbed, lead
binds to erythrocytes and travels in the blood to soft tissues, such
as the liver, kidneys, lungs, brain, spleen, muscles and heart. After
several weeks, most of the lead moves into bones and teeth. In
adults about 94% of the total amount of lead in the body is
contained in the bones and teeth. About 73% of the lead in
children’s bodies is stored in their bones. Lead can stay in bones for
decades [7].
Lead affects virtually every organ or system in the body, and the
proposed mechanisms of lead toxicity involve fundamental
biochemical processes. These proposed mechanisms include lead’s
ability to inhibit or mimic the action of calcium and to interact with
proteins. One of the best documented mechanisms is impairment
of heme sysnthesis which results in adverse effects not limited to
the hematopoietic system. Most of the lead in blood is bound to
erythrocytes [8] but plasma is the biologically active compartment
from which lead is available to cross cell membranes [9]. Bloodlead levels (BLLs) are related to diverse health effects, presumably
because it is related to plasma lead, which exchanges with lead in
critical target tissues, such as the brain, bone, erythroblasts and
kidney.
The adverse health effects range from death [7] (Fig. 1) to
impaired cognitive and behavioral development that can have
lifelong consequences for children. Children are more susceptible
than adults to the effects of lead exposure because a proportionately greater amount of the lead they ingest is absorbed, more
circulating lead enters their brain, and their developing nervous
system is more vulnerable to lead’s toxic effects [10]. In 1991, the
167
Centers for Disease Control and Prevention (CDC) responded to the
increasing number of studies that found adverse health effects in
children at blood-lead levels as low as 10 mg/dL by issuing new
guidelines. These included compiling an environmental history,
educating parents about lead, and conducting follow-up for
children with BLLs 10 mg/dL [11].
Recent research demonstrates that cognitive impairment is
associated with BLLs <10 mg/dL among children [12–18]. Lanphear
et al. [12] analyzed data collected in NHANES III, a nationally
representative sample of the US civilian population. They observed
cognitive effects in children aged 6–16 years with BLLs <5 mg/dL.
Two other cross-sectional studies, one conducted in Detroit [13]
and the other in Mexico City [14] tested children at age 7 years and
also found an inverse relationship with BLLs <10 mg/dL and
cognitive development. In the Rochester Longitudinal Study,
Canfield [15] found that children’s intellectual functioning at ages
3 and 5 years was inversely related to BLLs even when their peak
BLL was <10 mg/dL. Bellinger and Needleman [16] re-analyzed
data on a cohort of children in Boston whose BLLs never exceeded
10 mg/dL and found similar findings. Tellez-Rojo et al. followed a
cohort of children in Mexico City and tested them at ages 12 and 24
months. The children’s BLLs did not exceed 10 mg/dL and there was
a significant inverse relationship between BLL and mental and
psychomotor development [17]. Lanphear et al. [18] pooled data
from 7 international population-based longitudinal cohort studies
that included 1333 children who were followed from birth or
infancy until ages 5–10 years and found intellectual deficits in
children whose BLLs never exceeded 7.5 mg/dL. Importantly,
studies identified no threshold for cognitive impairment due to
lead exposure in children.
One expanding area of study is the effect of maternal lead
burden on fetal and child development. Because more than 90% of
lead in human adults is stored in the bone [19] it can be released
into the blood during times of bone resorption. One such time is
during pregnancy when mobilization of maternal bone into the
blood stream can expose the developing fetus [20]. Evidence that
maternal bone lead can be mobilized during pregnancy has been
provided by isotopic studies [21,22]. In addition, there is a strong
correlation between maternal and umbilical cord blood-lead levels
that indicates the transfer of lead from mother to fetus [23].
Several cohort studies have provided more evidence that
prenatal exposure is associated with child cognitive development.
Gomaa et al. [24] measured umbilical cord blood lead and infant
bone lead and compared lead levels with this cohort’s scores on the
Mental Development Index (MDI) on the Bayley scales at age 2
years. Infants with the lowest patella lead levels had higher MDI
scores than infants with higher patella lead levels [24]. Because the
effects produced by a neurotoxic agent depend on the timing of the
exposure [25], three of the cohort studies examined timing of lead
exposure during pregnancy. Hu et al. [26] studied fetal lead toxicity
during each trimester of pregnancy as predictors of infant
neurodevelopment. They found that fetal exposure to lead during
the first trimester before the pregnancy is recognized may have a
greater impact on adverse neurodevelopment later in life than
exposures during the second or third trimester [26]. The Mexico
City Prospective Lead Study [27] assessed the relationship of BLLs
collected during the second and third trimester of pregnancy, at
delivery, and at multiple points throughout childhood with IQ
measured at 6–10 years of age. Higher maternal BLL at third
trimester of pregnancy, especially around week 28, was associated
with decreased intellectual child development, even after controlling for other prenatal and postnatal lead measurements.
Wasserman et al. [28] investigated the contribution of prenatal and
postnatal lead exposure to early intelligence. Blood samples were
collected from pregnant women living in Kosovo from 1985 to
Author's personal copy
168
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
Fig. 1. Blood-lead levels associated with adverse health effects.
1986 at mid-pregnancy, delivery, and at subsequent 6-month
intervals for their prospective lead study. The study participants’
infants were tested at ages 3, 4, 5, or 7 years to determine
intellectual function. The findings suggested that prenatal and
postnatal exposures that occur at any time during the first 7 years
of life are likely to be independently associated with small
decrements in later IQ scores, even after controlling for social
factors [28].
Cognitive function and lead levels among adults have also been
examined. Shih et al. [29] reviewed 21 studies published from
1996 to 2006 that compared markers of both recent (blood lead)
and cumulative (bone lead) dose and their association with
cognitive function. The association between cognitive function and
bone-lead levels was consistently stronger than for BLLs among
environmentally exposed older adults. In contrast, among workers
with current lead exposure the association between cognitive
function and BLLs was stronger than for bone levels.
Another area that has been associated with adult lead levels is
cardiovascular disease. Navas-Acien et al. [30] conducted a
systematic review of all observational studies through August
2006 regarding lead and cardiovascular end points. They
summarized findings from seven previous reviews of lead and
blood pressure, all of which reported a positive association, albeit
modest, between lead exposure and blood pressure. They reviewed
30 studies that examined lead levels and clinical cardiovascular
endpoints (cardiovascular, coronary heart disease, stroke mortality, and peripheral arterial disease) in both general and occupa-
tional populations. Although positive associations between lead
exposure and cardiovascular disease were observed, several
methodologic limitations existed.
3. Sources
The sources of lead exposures vary among and within countries
depending on historic and current uses. The following section
presents several sources that have been described in the recent
scientific literature.
3.1. Leaded gasoline
Leaded gasoline accounted for 80–90% of airborne lead
pollution in large cities where it was used worldwide [31].
Countries that have phased lead out of gasoline have reported
corresponding decreases in lead concentrations in air and human
blood. The decreases in population BLLs have been dramatic. For
example, mean BLLs in the United States, Ontario, Canada, and the
United Kingdom were reduced by >70% as lead in gasoline was
reduced [32]. As more countries phase lead out of gasoline, similar
findings are reported. For example, Singh and Singh [33] reviewed
15 research studies all of which measured lead in the environment
and some measured human blood during different periods. The
reviewers categorized the studies according to three stages of their
leaded gasoline phase-out: before (before 1996), during (1996–
2000), and after (2000 and after). Reductions in lead concentra-
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
tions were observed in tree leaves, water, air, and children’s blood
as lead was removed from gasoline [33]. In another study, Nichani
et al. [34] assessed children’s BLLs in Bombay, India, 2–3 years after
the phase-out of leaded gasoline and compared their findings with
results from BLLs in a study conducted by the George Foundation in
1997 (when leaded gasoline was still used in Bombay). Using
similar blood-collection procedures, the study conducted before
leaded gasoline was banned showed that 61.8% of children had
BLLs 10 mg/dL compared with 33.2% after the phase-out [34].
3.2. Smelters
Metal smelters are another potential source of contamination
for air and soil and can contribute to lead poisoning. Concerns
about the health effects for people living near smelters can prompt
investigations such as the study of children’s BLLs and risk factors
conducted in Torreón, Mexico, in March 2001 [35]. The Met-Mex
Peñoles metal-processing plant, the largest in Latin America and
fourth largest in the world, is located in Torreón. The mean BLL of
children living there was 6.0 mg/dL and 20% had BLLs 10 mg/dL in
2001. BLLs and soil–lead levels increased in a dose–response
fashion as the distance from their homes to the smelter decreased.
Leaded gasoline was not considered a significant contributor to the
lead levels observed in Torreón because lead had been completely
phased-out from gasoline in Mexico in 1997 [36].
After smelter emissions stop, historic soil contamination can
pose an ongoing threat. In June 2005, reports of symptomatic lead
poisoning among refugee children in Kosovo reached the US CDC.
The children most affected by the lead contamination in Mitrovica,
Kosovo, were the Roma whose homes were destroyed during the
war. They were relocated to refugee camps situated on land
contaminated with lead and other heavy metal mining wastes near
the Trepca smelter in Mitrovica. Considerable historic contamination remains in the areas from the mining and smelting operations
that occurred there for centuries. The current facility dates to the
1930s and had been the economic base for the region. Operations
ceased in 1999 when routine testing of United Nations peacekeeping forces identified soldiers with elevated BLLs. This finding
motivated testing of children living in the nearby refugee camps.
All children had blood-lead levels >10 mg/dL, the level of concern
for young children. The mean BLL was 47 mg/dL in the camps as
compared to 29 mg/dL in the non-Roma children in the area [37].
3.3. Battery recycling
Informal lead-smelting operations, often operated at or near the
home, can be a source of lead exposure for nearby residents.
‘‘Backyard’’ or ‘‘cottage’’ lead smelting has been described in the
scientific literature for decades [38–40]. Reports of backyard
smelters as a cause of lead poisoning worldwide continue. These
smelters are usually unregulated and the magnitude of the
problem is not documented. A 1991 Jamaica study estimated that
about one third of spent lead-acid batteries in Jamaica were
recycled by backyard smelting operations or by small battery
repair shops scattered over the island [40]. These can be especially
dangerous to workers’ families and neighbors because the work
areas rarely have proper ventilation or control of worker exposure
or lead release. These operations create lead air emissions that then
settle and contaminate nearby soil, water, and food and can result
in high levels of lead exposure for families.
Other countries have also reported small secondary smelters as
sources of high dose lead exposure. Paoliello and DeCapitani [41]
reviewed published studies of environmental contamination in
Brazil and reported that, even though leaded gasoline is banned
and lead mining and primary smelting plants have closed,
169
hundreds of small secondary battery recycling plants that create
local contamination still operate. A Middle Eastern study found
BLLs >10 mg/dL among 2.2% of young children in Israel, <1% in
Jordan, 5.2% in West Bank, and 17.2% in Gaza. All of the children in
Gaza with BLLs >10 mg/dL lived near local small smelters engaged
in secondary recycling, smelting, and battery manufacture [42].
Melting lead to make fishing sinkers has also been reported as a
source of lead exposure. In Cartagena, Colombia, the parents of all
children with BLLs 10 mg/dL worked in and lived near small
metal smelting factories with poor indoor air quality, or were
fishers who made lead sinkers for their fishing nets. The highest
BLLs were in children from a neighborhood near a shoreline
where many family incomes were derived from fishing [43].
Similarly, Brown et al. conducted a study in Chuuk, Federated
States of Micronesia, and found that 61% of elevated BLLs among
children could be attributed to parents who made lead fishing
weights [44].
3.4. Paint
The most common source of lead poisoning for the majority of
young children in the United States is deteriorated, leaded
residential paint and lead-contaminated house dust and soil. Lead
was commonly used in residential paint before 1950; in the 1960s
the paint industry voluntarily began to limit lead in residential
paint. Although regulations limiting lead content in paint for
residential use were enacted in the United States in 1978, leaded
paint remains in many old homes. A wide distribution of housing
built before 1950 exists across the United States (Fig. 2) and poses a
potential health threat. The need for ongoing vigilance was
highlighted by the death of a 2-year-old Sudanese refugee girl who,
on 21 April 2000, became the first child in the United States known
to die from lead poisoning in the 10 previous years [45]. The
exposure occurred in the United States and was caused by lead
paint in the home.
In response to her death, the state where the death occurred
revised its testing recommendations to include two tests for
immigrants, upon arrival, and 6 months after resettlement, to
monitor changes in BLLs. The state found that BLLs for nearly 30% of
the refugee children became elevated after resettlement, which
suggested that the lead exposure occurred in the United States.
Investigations showed that elevated BLLs were associated with
living in old homes, the presence of lead hazards, behaviors that
increased the chance of ingesting lead, and chronic and acute
malnutrition [46]. Malnutrition is common in refugee populations
[47]. Anemia is a particular concern for children exposed to lead
because iron deficiency can enhance lead absorption and, thus,
increase risk for elevated BLLs.
Reports from Portugal, India, and South Africa indicate that
children in other countries are also being exposed to residential
lead paint. In Portugal’s Oporto Historical Center, a residential area
characterized by houses with deteriorating lead paint that were
built in the 1900s, children aged 1–5 years were tested for lead
poisoning [48]. BLLs ranged from 4.7 mg/dL to 42.5 mg/dL with a
mean of 13.9 mg/dL; 85.8% of children had BLLs 10 mg/dL.
Qualitative lead-paint tests of the walls of the homes were positive
for 91% of children with BLLs 20 mg/dL and 14% for children with
BLLs <10 mg/dL. In India, studies conducted in Mangalore and
Karnataka found lead-based paint in the homes of 3 of the 10
children with BLLs of at least 40 mg/dL. These 10 children were part
of a blood-lead study of 107 school children who were randomly
selected [49]. In Johannesburg, South Africa, lead was found in the
paint of 17% of the homes sampled in old and new suburbs that
represented a variety of socioeconomic backgrounds. The percentage of lead by weight in some samples reached 29% [50]. Clark
Author's personal copy
170
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
Fig. 2. States with pre-1950 housing, 2000.
et al. conducted a study of lead content in paint samples in India,
China and Malaysia and found that 66% of new paint samples
contained 5000 ppm (0.5%) of lead, the US definition of leadbased paint in existing housing, and 78% contained 600 ppm
(0.06%), the limit for new paints [51].
3.5. Traditional remedies
Complementary or alternative medicine has become widespread in Western countries. Because the remedies are ‘‘natural’’
they are believed to be free of toxic effects and health risks.
However, ethnic remedies may contain lead and other metals and
toxic substances. For example, certain branches of ayurvedic
medicines contain heavy metals because the metals are thought to
have therapeutic benefits for particular ailments. Several cases of
lead poisoning from ingesting medicinal products that contain lead
in New Zealand [52], Italy [53], and the United States [54] have
been reported in recent scientific literature. Traditional remedies
that contain lead have been reported to CDC for decades [52–64]. In
2004, three cases of lead poisoning by ayurvedic medicines were
reported to CDC. Subsequently, CDC posted an alert on the
Epidemic Information Exchange (Epi-X), a web-based communication that allows public health professionals to share preliminary surveillance information. In response to this posting, nine
additional adult cases of lead poisoning associated with ayurvedic
medicines were reported to CDC [54].
A traditional remedy imported from the Dominican Republic
and sold in botanicas (i.e., shops that sell herbs) in the United
States was associated with elevated BLLs in two children, twin
boys, in Rhode Island [64]. When the boys were identified with
elevated BLLs, an investigation for the lead source was conducted
promptly because investigators knew their home had been
remediated for lead. During the home inspection, litargirio was
found in a jar in the boys’ bedroom. Litargirio has been used by
Dominicans, particularly those from rural areas, as an antiperspirant/deodorant and as a traditional remedy for burns and fungal
infections of the feet. The boys had used the substance as an
antiperspirant/deodorant. The litargirio was tested and contained
790,000 ppm (79%) lead. When the children stopped using
litargirio, their BLLs decreased [64].
3.6. Electronics
Most electronic devices contain lead and may represent another
source of lead when discarded [65]. A study sponsored by the US
Environmental Protection Agency (US EPA) reported that electronic items in landfills leached lead at levels exceeding the threshold
for hazardous waste. The European Union recognized this potential
threat to human health and the environment and acted by banning
certain electronic items from landfills. However, the US EPAs most
recent estimate is that more than 2 million tons of electronic waste
is dumped in US landfills each year. EPA estimates that only about
10% of all obsolete consumer electronics are recycled. The rest are
stored somewhere, passed on to second users, or simply tossed in
the trash. US recyclers and watchdog groups estimate that 50% of
the used US computers, cellphones, and TVs that are sent to
recyclers are shipped overseas for recycling in facilities in Taizhou,
China, or Lagos, Nigeria, as permitted by federal law. Much of this
obsolete equipment ends up as toxic waste with hazardous
components exposed, burned, or allowed to degrade in landfills.
Waste by-products produced during informal recycling are heavily
contaminated with lead.
4. Prevention strategies
The striking aspect of these recent studies and reports is that
most lead sources have been reported previously in the scientific
literature. Although this article does not represent an exhaustive
search of all lead sources reported in the scientific literature, many
other sources such as children’s toys, jewelry, and candy are
identified and also tend to reappear (Table 1). These sources may
appear in new places and poison new populations and all were
potentially preventable.
The traditional approach to preventing lead poisoning has
been to act after exposure has occurred. The only medical
treatment available is chelation, which can save lives in persons
with very high BLLs. However, chelating drugs are not always
available in developing countries and have limited value in
reducing the sequelae of lead poisoning [66,67]. Children aged 12–
33 months with referral BLLs ranging from 22 to 44 mg/dL were
enrolled in a randomized clinical trial and received either placebo
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
171
Table 1
Examples of published reports of elevated blood lead levels associated with imported products containing lead by exposure source
Exposure source
Description/exposure pathway
Year report published
Tamarind candy
Ceramic glaze
Traditional remedies
Toy jewelry
Lead leaches from pots and wrappers
Lead in ceramic glaze leached into stored beverages
Lead containing remedies, and traditional herbal medicines
Ingestion of a necklace and a metallic charm
1998,
1989,
1981,
2004,
2002
2004, 2006
1982,1983, 1984, 1989, 1993, 1999, 2002, 2004, 2005, 2005
2006
Tamarind candy: CDC, Lead poisoning associated with imported candy and powdered food coloring—California and Michigan, MMWR Morb. Mortal. Weekly Rep. 47 (1998)
1041–1043; Ref. [63]. Ceramics: CDC, Lead poisoning following ingestion of homemade beverage stored in a ceramic jug—New York, MMWR Morb. Mortal. Weekly Rep. 38
(1989) 379–380; CDC, Childhood lead poisoning from commercially manufactured french ceramic dinnerware—New York City, 2003, MMWR Morb. Mortal. Weekly Rep. 53
(2004) 584–586; D. Hellstrom-Lindberg, A. Bjorklund, C. Karlson-Stiber, P. Harper, A.I. Selden, Lead poisoning from souvenir earthenware, Int. Arch. Occup. Environ. Health 79
(2006) 165–168. Traditional remedies: Refs. [55–63,54,64]; A. Roche, C. Florkowski, T. Walmsley, Lead poisoning due to ingestion of Indian herbal remedies, NZ Med. J. 118
(2005) 1219. Toy Jewelry: Refs. [70,71].
or succimer. Neuropsychological tests at 3 years after randomization [66] and at age 7 years [67] revealed no developmental
benefit in the group that received succimer. These findings
highlight the importance of implementing environmental measures to prevent lead exposure. The best protection for all people is
to control lead sources on a global scale. We recommend three key
strategies to prevent lead poisoning: identify sources, eliminate or
control sources, and monitor environmental exposures and
hazards.
4.1. Identify sources
Sources of lead may be historic contamination, recycling old
lead products, or manufacturing new products. Vast reservoirs of
lead remain in our environments and could emerge as health
threats. For example, old lead pipes in Washington, DC, did not
pose a serious health risk to local residents until a change in water
treatment [68] caused the lead to become more available in
drinking water. Another potential hazard is lead paint in old
homes. In the United States, an estimated 38 million homes
contain lead-based paint. Although this represents a substantial
reduction from 64 million homes with lead paint in 1990, there are
still 24 million that have significant lead hazards [69]. When
homes with lead paint deteriorate or are remodeled without taking
proper lead-control precautions, the lead can become available in
dust and soil and result in human exposure.
Products imported from countries that do not adequately limit
the use of lead and enforce those regulations may also contain
harmful levels of lead. The United States has issued many recalls of
toys and children’s products in 2007 because they have been found
to contain lead (Table 2). In 2003, it was determined that a young
child with a BLL of 123 mg/dL had swallowed a toy medallion [70].
Table 2
US Consumer Product Safety Commission recalls of lead containing toysa and Children’s Productsb—1 January 2007–1 March 2008
Product description
Lead source
Units recalled
Date of recall
Country of manufacture
Children’s Metal Necklaces
Children’s Memory Testing Cards
Children’s Table and Chair
Pendants and Candle Charms
Children’s Sketchbooks and Colored Spirals
Toy Gardening Hand Rakes
Toy Wooden Block and Train Sets
Classroom Reading and Math Aids
Educational Assessment Blocks
Big Wooden Blocks and Wooden Train Sets
Toy Racing Cars
Cranium Cadoo Board Games
Play Mats
Toy Wrestler Figures
Toy Wagons
Soldier Bear Toys
Duck Water Globes
Princess Children’s Metal Jewelry
Baby Toy and Speed Racer Cars
Fishing Games
Children’s Sunglasses
Potty Seats
Mini Racing Helmets
Children’s Metal Necklaces and Bracelets
Assorted Metal Jewelry
Children’s Necklace and Earring Sets
Children’s Metal Jewelry
Children’s Pencil Pouches
Curious George Dolls
Toy Robot
Dizzy Ducks Music Box
Winnie-the-Pooh Spinning Top Toys
Big Red Wagons
Duck Family Toys
Toy Cars
Dragster and Funny Car
Galaxy Warriors Toy Figures
Metals contain lead
Surface paint
Surface paint
Metals contain lead
Paint on spiraled metal bindings
Paint on toy
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Surface paint
Painted base
Metal contains lead
Toys contain lead
Parts contain lead
Surface paint
Decorative plaque in back of seat
Surface paints
Jewelry contains lead
Jewelry contains lead
Jewelry contains lead
Jewelry contains lead
Paint of pouch zipper pulls
Surface paint and hat
Surface paints
Surface paints
Surface paints
Surface paints
Surface paints
Surface paint
Surface paint
Surface paint
2900
5300
50
460,000
80,000
400
30,000
185,000
18,000
15,000
2000
38,000
60
5400
15,000
11,400
60
1000
300,000
14,000
260,000
160,000
1400
10,400
205,000
4500
43,000
84,200
175,000
2600
1300
3600
7200
3500
380,000
75,000
380,000
2/22/2008
2/22/2008
2/8/2008
2/7/2008
2/6/2007
2/5/2008
2/12/2008
1/31/2008
1/24/2008
1/24/2008
1/23/2008
1/17/2008
1/16/2008
1/15/2008
1/3/2008
12/19/2007
12/13/2007
12/13/2007
12/13/2007
12/12/2007
12/7;2007
12/6/2007
12/5/2007
11/21/2007
11/21/2007
11/21/2007
11/21/2007
11/21/2007
11/8/2007
11/7/2007
11/7/2007
11/7/2007
11/7/2007
11/7/2007
11/7/2007
11/7/2007
10/31/2007
China
China
China
Korea
China
China
China
China
China
Hong Kong
China
China
Taiwan
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
172
Table 2 (Continued)
Product description
Lead source
Units recalled
Date of recall
Country of manufacture
Elite Operations Toys
Ribbit Board Games
Halloween Pails and Decorations
Children’s Metal Jewelry
WeGlow Children’s Metal Jewelry
Toy Gardening Toys
Princess Travel Art Set Lap Desks
Decorative Packaging Sold with Girl’s Gift Sets
Toy Garden Rakes
Toy Watering Cans
Go Diego Go Animal Rescue Boats
Children’s Puppet Theaters
Halloween Skull Pails
Winnie-the-PoohPlay Sets
Mini Racing Helmets
Dinosaur Toys
Toy Decorating Sets
Toy Flashlights
Baby Einstein Color Blocks
Wooden Toys
Children’s Metal Necklaces
Children’s Metal Jewelry Sets
Puppet Theaters
Knights of the Sword
Toy Gardening Tools and Chairs
Thomas & Friends Wooden Railway Toys
Thomas & Friends Railway Toys
Bongo Band Toys
Locomotive Toys
Barbie Accessory Toys
Wooden Coloring Cases
Children’s Watering Cans
Character Address Books and Journals
Children’s Metal Jewelry Sets
Children’s Charm Bracelets
Spinning Tops and Tin Pails
Toy Train Sets
Sarge’’ Die Cast Toy Cars
Character Toys
Soldier Bear
Children’s Earring Sets
Children’s Metal Jewelry Sets
Solder Bear
Children’s Metal Jewelry
Children’s Gardening Gloves
Children’s Necklaces, Bracelets and Rings
Children’s Rings
Toy Drums
Children’s Religious Fish Necklaces
Children’s Rings
Anima-Bamboo Collection Games
Children’s Bracelets and Necklaces
Children’s Bracelets
Stuffed Fun Balls
Childrenr’s Necklaces
Children’s Mood Necklaces
Children’s Mood Necklaces
Elite Operations Toys
Children’s Easels
Children’s Necklace and Earring Sets
Children’s Rings
Boys’ Jackets
Children’s Bracelets
Children’s Rings
Children’s Necklaces
Children’s Clothing
Surface coatings
Surface paint
Surface paint
Jewelry contains lead
Jewelry contains lead
Surface paint
Surface paint on zipper pull of lap desk
Surface coating on bead packaging
Surface paint
Surface paint
Surface paints
Surface paints
Surface paints
Surface paints
Surface paints
Not specified
Surface paint
Surface paint
Surface paint
Surface paint
Clasps on necklaces contain lead
Metal jewelry contains lead
Surface paint
Surface paints
Surface paint
Surface paints
Surface paints
Surface paints
Surface paints
Surface paints
Ink on outer packaging of cases
Beak of watering can contains lead
Paint on metal spiral bindings
Metal jewelry sets contain lead
Jewelry contain lead
Surface paints
Surface paints
Surface paints
Surface paints
Surface paints
Metal earring sets contain lead
Metal jewelry sets contain lead
Surface paints
Jewelry contains lead
Painted logo on gloves contains lead
Jewelry contains lead
Rings contain lead
Surface paints
Necklaces contain lead
Rings contain lead
Toys
Surface paint
Paint on metallic band
Surface paints
Necklaces contain lead
Jewelry contains lead
Jewelry contains lead
Surface coatings
Paint on chalkboard side of easels
Jewelry contains lead
Jewelry contains lead
Snap closures on jackets contain lead
Jewelry contains lead
Jewelry contains lead
Pendant on necklace contains lead
Coatings on snaps in overalls and shirt
16,000
1500
142,000
198,000
110,000
97,000
7800
4000
16,000
6000
38,000
5400
55,000
49,000
2500
10,000
15,000
79,000
35,000
10,000
850
23,500
10,000
800
350,000
200,000
1.5 million
8900
90,000
675,000
27,000
6000
250,000
14,000
7900
66,000 tops; 4700 pails
27,000
253,000
967,000
13,000
220
20,000
3000
103,000
80
200,000
300,000
4500
132,000
200
5000
900,000
4 million
7200
58,000
47,000
3600
128,700
2500
6000
115,000
8000
86,000
280,000
113,800
200
10/31/2007
10/31/2007
10/25/2007
10/25/2007
10/25/2007
10/25/2007
10/11/2007
11/1/2007
9/26/2007
8/28/2007
10/25/2007
10/17/2007
10/17/2007
10/11/2007
10/11/2007
10/11/2007
10/4/2007
10/4/2007
10/4/2007
10/4/2007
9/26/2007
9/26/2007
9/26/2007
9/26/2007
9/26/2007
9/26/2007
6/13/2007
9/4/2007
9/4/2007
9/4/2007
8/30/2007
8/28/2007
8/22/2007
8/22/2007
8/22/2007
8/22/2007
8/21/2007
8/14/2008
9/2/2007
7/18/2007
7/17/2007
7/5/2007
5/23/2007
5/31/2007
5/16/2007
5/15/2007
5/15/2007
5/30/2007
5/2/2007
5/2/2007
5/2/2007
4/17/2007
4/3/2007
3/28/2007
3/15/2007
3/15/2007
3/13/2007
3/13/2007
3/7/2007
2/23/2007
2/23/2007
2/13/2007
2/7/2007
2/7/2007
1/18/2007
1/5/2007
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
China
Hong Kong
China
China
Hong Kong
China
China
China
China
China
China
India
China
India
China
China
China
China
China
China
China
China
China
China
China
China
China
China
a
b
Toy recalls posted on the Consumer Product Safety Commission website. Available at: http://www.cpsc.gov/cpscpub/prerel/category/toy.html.
Lead recalls posted on the Consumer Product Safety Commission website. Available at: http://www.cpsc.gov/cgi-bin/haz.aspx.
The medallion was removed from his abdomen, tested, and found
to contain 38.8% lead. It had been purchased in a US vending
machine and a recall was issued for 150 million of the necklaces.
The child survived, however, the recall did not adequately protect
all children.
In 2006, a child aged 4 years died of acute lead poisoning [71].
This was the first child lead-poisoning death since 2000 in the
United States. The autopsy revealed a heart-shaped metallic charm
in the abdomen that was found to have a lead content of 99.1%. The
charms were recalled; this was the 15th recall of leaded toys in
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
2 years. In 2007, a series of recalls of children’s toys that were
suspected of containing lead was issued in the United States. Other
products that children can access also have been recalled over
several decades.
4.2. Eliminate or control sources
Controlling potential sources of lead requires targeted and often
multiple approaches. These should include developing, implementing, and enforcing effective lead-control policies to reduce
lead emissions, clean contaminated sites, offer incentives to
encourage safer practices, and restrict nonessential uses of lead.
In many cases, effective technology exists to reduce lead emissions.
For example, there are technological solutions that can reduce
dangerous lead emissions from smelting facilities [72–76]. Soil
remediation can lower lead concentrations [77–79] that remain
long after lead-smelting emissions are reduced. Without reduction
of air emissions and remediation of soil, home hygiene and clean
neighborhood campaigns are of little value in decreasing elevated
BLLs.
The importance of regulations in lead-control efforts to prevent
re-emergence of known hazardous products is illustrated by the
availability of leaded house paint in countries without existing
laws [51]. A study that sampled house paint from four Asian
countries and tested their lead content found that some brands of
paint sold in China, India and Malaysia had high lead content. In
contrast those same brands marketed in countries such as
Singapore that had regulatory limits on lead in house paint either
had markedly lower or no detectable levels of lead [51].
Implementation and enforcement of safe worksite practices is
another lead-control strategy. Ye and Wong reviewed lead studies
reported in the Chinese scientific literature from 1990 to 2005 [80].
173
The authors compared workplace lead concentrations and the
prevalence of lead poisoning among workers before and after
passage of the 2002 Occupational Diseases Prevention Act that
included provisions for regulatory enforcement. Lead concentrations in both lead-battery and lead-smelter industries far exceeded
the occupational exposure limits for lead before and after passage
of the law. After passage of the law, the prevalence of lead
poisoning decreased significantly in lead-battery factories (45.5%
vs. 36.8%) and slightly in lead smelters (33.8% vs. 31.4%). However,
the high prevalence of lead poisoning among workers indicates the
need for stronger control measures and enforcement. Safe worksite
practices are also important to protect the workers’ family
members from exposure to contaminated work clothes [81,82].
The impact of enforcing strong laws for the remediation of
homes in which a child with an elevated BLL had been identified
was assessed. The assessment compared the number of properties
that had multiple children with elevated BLLs in two US states in
1992–1993 with the number of these same properties that had
children with elevated BLLs 5 years later [83]. Both states had wellestablished, lead poisoning-prevention programs with nearly
universal testing of children and widespread public education.
Both states had laws to remediate a home if a child with an
elevated BLL was identified. The addresses of houses where a child
with a BLL 25 mg/dL lived between 1992 and 1993 were
identified. A 5-year follow-up ascertained BLLs of children who
subsequently lived at those addresses. There was a fourfold
increased chance of a subsequent child tenant being identified
with a BLL 10 mg/dL for a house in the state with limited laws and
enforcement compared with a house in the state with strict laws
and enforcement.
Another lead-control strategy is to develop practices that
promote the use of commercially available and technically well-
Fig. 3. Leaded petrol phase-out: global status.
Author's personal copy
174
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
understood, safer alternatives to lead. The successful reduction in
leaded gasoline use in many developing countries is attributed in
part to the World Bank’s practice of requiring that countries
include strategies to replace leaded gasoline with unleaded
gasoline in their development plans. The World Bank supports
governments in adopting appropriate policies and developing
strategies, facilitating policies, and implementing lead phase-out
strategies [31]. These efforts have contributed to widespread
phase-out of leaded gasoline (Fig. 3). A similar approach could be
adopted to control unregulated battery smelting by offering buyback programs and ‘cradle to cradle’ registration of lead–zinc
batteries that allows tracking them from manufacture, though use,
recycling and re-marketing.
4.3. Monitor environmental exposures and hazards
Testing children’s BLLs has been a key prevention strategy for
decades. Results of blood-lead testing can be used to identify
populations at high risk and define risk factors for elevated BLLs,
which can be used to target interventions. However, not all
countries have the resources to conduct population-based leadpoisoning surveillance. Targeted and episodic lead testing of
populations that may be at risk for lead poisoning can be a costeffective way to identify and monitor population exposures [42].
Case management of individuals with elevated BLLs has
involved identifying and removing lead sources after exposure
has occurred. Ideally, we should monitor lead hazards to protect
people before they are exposed. Lead levels in air are monitored in
many countries to ensure that the public’s health is protected.
Businesses involving lead should routinely test their workers to
monitor BLLs. More can be done to track recycling of batteries and
electronic goods to ensure that emissions are properly contained to
protect families from exposure to lead and prevent contamination
of the environment. Testing of imported products that children
may use should be increased and tracked. The manufacture of
products, such as leaded paint and traditional medicines, in
countries without strong lead-control laws and enforcement can
result in exposing people in many countries. Often, these
exposures are identified after a person with lead poisoning has
been diagnosed. Electronic health communication systems such as
listservs can alert public health practitioners to emerging threats.
These systems disseminate information quickly across large
geographic areas and highlight issues that could be missed by
routine surveillance systems.
5. Conclusion
Even in countries where lead control has been vigilant, vast
reservoirs of lead still exist in soil, dust, and house paint; these
sources will continue to contribute to the population lead burden
for many years to come. In addition, lead is stored in bone,
therefore, it can result in adverse health outcomes in adults many
years after exposure. Further, maternal bone lead can be mobilized
during pregnancy and serve as an endogeous source of lead
exposure to the developing fetus [20]. In recognizing that there is
no safe BLL for children and that chelating agents have limited
value in reducing the sequelae of lead poisoning, all nations should
control or eliminate lead hazards in children’s environments
before they are exposed. Primary prevention, i.e., preventing
people from being exposed to lead is the only solution.
References
[1] J.O. Nriagu, Lead exposure and lead poisoning, in: Lead and Lead Poisoning in
Antiquity, John Wiley and Sons, New York, NY, 1983, pp. 309.
[2] R.H. Major, Classic Descriptions of Disease, 3rd ed., Charles C. Thomas, Springfield,
IL, 1945, 312 pp.
[3] G. Markowitz, D. Rosner, Cater to the children: the role of the lead industry in a
public health tragedy, 1900–1955, Am. J. Public Health 90 (2000) 36–46.
[4] H.L. Needleman, Childhood lead poisoning: the promise and abandonment of
primary prevention, Am. J. Public Health 88 (1998) 1871–1877.
[5] E. Silbergeld, Preventing lead poisoning in children, Annu. Rev. Public Health 18
(1997) 187–210.
[6] Agency for Toxic Substances and Disease Registry, Toxicological Profile for Lead,
ATSDR, Atlanta, GA, 1999.
[7] P.E. de Silva, Determination of lead in plasma and studies on its relationship to
lead in erythrocytes, Br. J. Ind. Med. 38 (1981) 209–217.
[8] A. Cavalleri, C. Minoia, L. Pozzoli, F. Polatti, P.F. Bolis, Lead in red blood cells and in
plasma of pregnant women and their offspring, Environ. Res. 17 (1978) 403–408.
[9] D.C. Bellinger, A.M. Bellinger, Childhood lead poisoning: the torturous path from
science to policy, J. Clin. Invest. 116 (2006) 853–857.
[10] T.I. Lidsky, J.S. Schneider, Lead neurotoxicity in children: basic mechanisms and
clinical correlates, Brain 126 (2003) 5–19.
[11] Centers for Disease Control and Prevention, Preventing lead poisoning in young
children: a statement by the Centers for Disease Control, 1991 Atlanta, GA, CDC
website (accessed on November 27, 2007) available at http://www.cdc.gov/nceh/
lead/publications/books/plpyc/contents.htm.
[12] B.P. Lanphear, K. Dietrich, P. Auinger, C. Cox, Cognitive deficits associated with
blood lead concentrations <10 mg/dL in US children and adolescents, Public
Health Rep. 115 (2000) 521–529.
[13] L.M. Chiodo, S.W. Jacobson, J.L. Jacobson, Neurodevelopmental effects of postnatal
lead exposure at very low levels, Neurotoxicol. Teratol. 26 (2004) 359–371.
[14] K. Kordas, R.L. Canfield, P. Lopez, J.L. Rosado, G.G. Vargas, M.E. Cebrian, et al.,
Deficits in cognitive function and achievement in Mexican first-graders with low
blood lead concentrations, Environ. Res. 100 (2006) 371–386.
[15] R.L. Canfield, C.R. Henderson, D.A. Cory-Slechta, C. Cox, T.A. Jusko, B.P. Lanphear,
Intellectual impairment in children with blood lead concentrations below 10 mg
per deciliter, N. Engl. J. Med. 348 (2003) 1517–1526.
[16] D.C. Bellinger, H.L. Needleman, Intellectual impairment and blood lead levels, N.
Engl. J. Med. 349 (2003) 500–502.
[17] M.M. Tellez-Rojo, D.C. Bellinger, C. Arroyo-Quiroz, H. Lamadrid-Figueroa, A.
Mercado-Garcia, L. Schnaas-Arrieta, et al., Longitudinal associations between
blood lead concentrations lower than 10 mg/dL and neurobehavioral development in environmentally exposed children in Mexico City, Pediatrics 118 (2006)
e323–e330.
[18] B.P. Lanphear, R. Hornung, J. Khoury, K. Yolton, P. Baghurst, D.C. Bellinger, et al.,
Low-level environmental lead exposure and children’s intellectual function: an
international pooled analysis, Environ. Health Perspect. 113 (2005) 894–899.
[19] H.A. Schroeder, I.H. Tipton, The human body burden of lead, Arch. Environ. Health
17 (1968) 965–978.
[20] D.C. Bellinger, Teratogen update: lead and pregnancy, Birth Defects Res. 73 (2005)
409–420.
[21] B.L. Gulson, K.J. Mizon, M.J. Korsch, et al., Mobilization of lead from human bone
tissue during pregnancy and lactation—a summary of long-term research, Sci.
Total Environ. 303 (2003) 79–104.
[22] W.I. Manton, C.R. Angle, K.L. Stanek, et al., Release of lead from bone in pregnancy
and lactation, Environ. Res. 92 (2003) 139–151.
[23] L.M. Schell, M. Denham, A.D. Start, M. Gomez, J. Ravenscroft, P.J. Parsons, A.
Aydermir, R. Samelson, Maternal blood lead concentration, diet during pregnancy
and anthropometry predict neonatal blood lead in a socioeconomically disadvantaged population, Environ. Health Perspect. 111 (2003) 195–200.
[24] A. Gomaa, H. Hu, D. Bellinger, et al., Maternal bone lead as an independent risk
factor for fetal neurotoxicity: a prospective study, Pediatrics 110 (2002) 110–118.
[25] P. Mendola, S.G. Selevan, S. Gutter, D. Rice, Environmental factors associated with
a spectrum of neurodevelopmental deficits, Ment. Retard. Dev. Disabl. Res. Rev. 8
(2002) 188–197.
[26] H. Hu, M.M. Tellez-Rojo, D. Bellinger, D. Smith, A.E. Ettinger, H. LamadridFigueroa, J. Schwartz, L. Schnaas, A. Mercado-Garcia, M. Hernandez-Avila, Fetal
lead exposure at each stage of pregnancy as a predictor of infant mental development, Environ. Health Perspect. 114 (2006) 1730–1735.
[27] L. Schnaas, S.J. Rothenberg, M.F. Flores, S. Martinez, C. Hernandez, E. Osorio, et al.,
Reduced intellectual development in children with prenatal lead exposure,
Environ. Health Perspect. 111 (2006) 791–797.
[28] G.A. Wasserman, X. Liu, D. Popovac, P. Factor-Litvak, J. Kline, C. Waternaux, N.
Lolacono, J.H. Graziano, The Yugoslavia prospective lead study: contributions of
prenatal and postnatal lead exposure to early intelligence, Neurotoxicol. Teratol.
22 (2000) 811–818.
[29] R.A. Shih, H. Hu, M.G. Weisskopf, B.S. Schwartz, Cumulative lead dose and
cognitive function in adults: a review of studies that measured both blood lead
and bone lead, Environ. Health Perspect. 115 (2007) 483–492.
[30] A. Navas-Acien, E. Guallar, E.K. Silbergeld, S.J. Rothenberg, Lead exposure and
cardiovascular disease—a systematic review, Environ. Health Perspect. 115
(2007) 472–482.
[31] M. Lovei, Eliminating a silent threat: World Bank support for the global phase out
of lead from gasoline, in: A.M. George (Ed.), Lead Poisoning Prevention and
Treatment: Implementing a National Program in Developing Countries, The
George Foundation, Bangalore, India, 1999, pp. 169–180.
[32] World Resources Institute, Laden with Lead Earth Trends, The environmental
Information Portal (accessed on May 16, 2007) available at http://earthtrends.
wri.org/features/view_feature.php?fid=30&theme=6.
Author's personal copy
P.A. Meyer et al. / Mutation Research 659 (2008) 166–175
[33] A.K. Singh, M. Singh, Lead decline in the Indian environment resulting from the
petrol–lead phase-out programme, Sci. Total Environ. 368 (2006) 686–694.
[34] V. Nichani, L. Wan-I, M.A. Smith, G. Noonan, M. Kulkarni, M. Kodavor, L.P. Naeher,
Blood lead levels in children after phase-out of leaded gasoline in Bombay, India,
Sci. Total Environ. 363 (2006) 95–106.
[35] R. Albalak, R. Hart McElroy, G. Noonan, S. Buchanan, R.L. Jones, W.D. Flanders, C.
Gotway-Crawford, D. Kim, T. Dignam, W.R. Daley, J. Jarrett, E. Eduardo, M.A.
McGeehin, Blood lead levels and risk factors for lead poisoning among children in
a Mexican smelting community, Arch. Environ. Health 58 (2003) 172–183.
[36] I. Romieu, E. Palazuelos, M. Hernandez-Avila, et al., Sources of lead exposure in
Mexico City, Environ. Health Perspect. 102 (1994) 384–389.
[37] World Health Organization, Mission Report: Lead Crisis in the United Nations
Administered Province of Kosovo, WHO Bonn, Germany, 2005.
[38] J.P. Koplan, A.V. Wells, H.J. Diggory, E.L. Baker, J. Liddle, Lead absorption in a
community of potters in Barbados, Int. J. Epidemiol. 6 (1977) 225–229.
[39] M. Kawai, H. Toriumi, Y. Katagiri, Y. Maruyama, Home lead work as a potential
source of lead exposure for children, Int. Arch. Occup. Environ. Health 53 (1983)
37–46.
[40] T.D. Matte, J.P. Figueroa, S. Ostrowski, G. Burr, L. Jackson-Hunt, E.L. Baker, Lead
exposure from conventional and cottage lead smelting in Jamaica, Arch. Environ.
Contam. Toxicol. 21 (1991) 65–71.
[41] M.M.B. Paoliello, E.M. DeCapitani, Environmental contamination and human
exposure to lead in Brazil, Rev. Environ. Contam. Toxicol. 184 (2005) 59–96.
[42] J. Safi, A. Fischbein, S. ElHaj, R. Sansour, M. Jaghabir, M.A. Hashish, H. Suleiman, N.
Safi, A. Abu-Hamda, J.K. Witt, E. Platkov, S. Reingold, A. Alayyan, T. Berman, M.
Bercovitch, Y. Choudhri, E.D. Richter, Childhood lead exposure in the Palestinian
Authority, Israel, and Jordan: results from the Middle Eastern Regional Cooperation Project, 1996–2000, Environ. Health Perspect. 114 (2006) 917–922.
[43] J. Olivero-Verbel, D. Duarte, M. Echenique, J. Guette, B. Johnson-Restrepo, P.J.
Parsons, Blood lead levels in children aged 5–9 years living in Cartagena, Colombia, Sci. Total Environ. 372 (2007) 707–716.
[44] L.M. Brown, D. Kim, A. Youmai, P.A. Meyer, G.P. Noonan, D. Huff, W.D. Flanders,
Blood lead levels and risk factors for lead poisoning in children and caregivers in
Chuuk State, Micronesia, Int. J. Hyg. Environ. Health 208 (2005) 231–236.
[45] CDC, Fatal pediatric lead poisoning–New Hampshire, 2000, MMWR Morb. Mortal.
Weekly Rep. 50 (2001) 457–459.
[46] CDC, Elevated blood lead levels in refugee children, New Hampshire, 2003–2004,
MMWR Morb. Mortal. Weekly Rep. 54 (2005) 42–46.
[47] United Nations System/Standing Committee on Nutrition, Nutrition information
in crisis situations, Secretariat of the UNS/SCN, Geneva, Switzerland, May 2004,
Report no. 2.
[48] O.N. Mayan, A.T. Henriques, J.M. Calheiros, Childhood lead exposure in Oporto,
Portugal, Int. J. Occup. Environ. Health 7 (2001) 209–216.
[49] A. Kuruvilla, V.V. Pillay, T. Venkatesh, et al., Portable lead analyzer to locate
sources of lead, Indian J. Pediat. 41 (2004) 495–499.
[50] M. Montgomery, A. Mathee, A preliminary study of residential paint lead concentrations in Johannesburg, Environ. Res. 98 (2005) 279–283.
[51] C.S. Clark, K.G. Rampal, V. Thuppil, C.K. Chen, R. Clark, S. Roda, The lead content of
currently available new residential paint in several Asian countries, Environ. Res.
102 (2006) 9–12.
[52] A. Roche, C. Florkowski, T. Walmsley, Lead poisoning due to ingestion of Indian
herbal remedies, NZ Med. J. 118 (2005) U1578.
[53] G. Muzi, M. Dell’Omo, N. Murgia, A. Curina, S. Ciabatta, G. Abbritti, Lead poisoning
caused by Indian ethnic remedies in Italy, Med. del Lavoro 96 (2005) 126–133.
[54] CDC, Lead poisoning associated with ayurvedic medications—five states, 2000–
2003, MMWR Morb. Mortal. Weekly Rep. 53 (2004) 582–584.
[55] CDC, Lead poisoning from lead tetroxide used as a folk remedy—Colorado, MMWR
Morb. Mortal. Weekly Rep. 30 (1981) 546–547.
[56] CDC, Use of lead tetroxide as a folk remedy for gastrointestinal illness, MMWR
Morb. Mortal. Weekly Rep. 30 (1982) 647–648.
[57] CDC, Folk remedy-associated lead poisoning in Hmong children—Minnesota,
MMWR Morb. Mortal. Weekly Rep. 32 (1983) 555–556.
[58] CDC, Lead poisoning from Mexican folk remedies—California, MMWR Morb.
Mortal. Weekly Rep. 32 (1983) 554–555.
175
[59] CDC, Lead poisoning associated death from Asian Indian folk remedies—Florida,
MMWR Morb. Mortal. Weekly Rep. 33 (1984) 643–645.
[60] CDC, Epidemiologic notes and reports cadmium and lead exposure associated
with pharmaceuticals imported from Asia—Texas, MMWR Morb. Mortal. Weekly
Rep. 38 (1989) 612–614.
[61] CDC, Lead poisoning associated with use of traditional ethnic remedies—
California, 1991–1992, MMWR Morb. Mortal. Weekly Rep. 42 (1993) 521–524.
[62] CDC, Adult lead poisoning from an Asian remedy for menstrual cramps—Connecticut, 1997, MMWR Morb. Mortal. Weekly Rep. 53 (1999) 27–29.
[63] CDC, Childhood lead poisoning associated with tamarind candy and folk remedies—California, 1999–2000, MMWR Morb. Mortal. Weekly Rep. 51 (2002) 684–
686.
[64] CDC, Lead poisoning associated with use of litargirio—Rhode Island, 2003, MMWR
Morb. Mortal. Weekly Rep. 54 (2005) 227–229.
[65] V.J. Brown, Electronics, lead and landfills, Environ. Health Perspect. 112 (2004)
A734.
[66] W.J. Rogan, et al., The effect of chelation therapy with succimer on neuropsychological development in children exposed to lead, N. Engl. J. Med. 344 (2001)
1421–1426.
[67] K.N. Dietrich, J.H. Ware, M. Salganik, J. Radcliff, W.J. Rogan, G.G. Rhoads, et al.,
Effect of chelation therapy on the neuropsychological and behavioral development of lead-exposed children after school entry, Pediatrics 114 (2004) 19–26.
[68] CDC, Blood lead levels in residents of homes with elevated lead in tap water—
District of Columbia, MMWR Morb. Mortal. Weekly Rep. 53 (2004) 268–270.
[69] D.E. Jacobs, R.P. Clickner, J.Y. Zhou, S.M. Viet, D.A. Marker, J.W. Rogers, et al., The
prevalence of lead-based paint hazards in US housing, Environ. Health Perspect.
110 (2002) A599–A606.
[70] J.L. VanArsdale, R.D. Leiker, M. Kohn, T. Merritt, B.Z. Howowitz, Lead poisoning
from a toy necklace, Pediatrics 114 (2004) 1096–1099.
[71] CDC, Death of a child after ingestion of a metallic charm—Minnesota, 2006,
MMWR Morb. Mortal. Weekly Rep. 55 (2006) 340–341.
[72] D. Prpic-Majic, J. Pongracid, J. Hrsak, A. Pizent, A follow-up study in a lead smelter
community following the introduction of an effective pollution control system,
Isr. J. Med. Sci. 28 (1992) 548–556.
[73] S.R. Hilts, F. Goodarzi, H. Sanei, M. Labonte, W.F. Duncan, S.E. Bock, Effect of
smelter emission reductions on children’s blood lead levels, Sci. Total Environ.
303 (2003) 51–58.
[74] K. Louekari, U. Mroueh, L. Maidell-Munter, S. Valkonen, T. Tuomi, K. Savolainen,
Reducing the risks of children living near the site of a former lead smelter, Sci.
Total Environ. 319 (2004) 65–75.
[75] F. Diaz-Barriga, A. Bates, J. Calderon, A. Lugo, L. Galvao, I. Lara, et al., The El Paso
smelter 20 years later: residual impact on Mexican children, Environ. Res. 74
(1997) 11–16.
[76] D. Morse, P. Landrigan, B. Rosenblum, J. Hubert, J. Housworth, El Paso revisited:
epidemiologic follow-up of an environmental lead problem, JAMA 242 (1979)
739–741.
[77] D. Gagne, Blood lead levels in Noranda children following removal of smeltercontaminated yard soil, Can. J. Public Health 85 (1994) 163–166.
[78] B. Lanphear, P. Succop, S. Roda, G. Henningsen, The effect of soil abatement on
blood lead levels in children living near a former smelting and milling operation,
Public Health Rep. 118 (2003) 83–91.
[79] I. Von Lindern, S. Spalinger, B. Bero, V. Petrosyan, M. Von Braun, The influence
of soil remediation on lead in house dust, Sci. Total Environ. 303 (2003) 59–
78.
[80] X. Ye, O. Wong, Lead exposure, lead poisoning, and lead regulatory standards in
China, 1990–2005, Regul. Toxicol. Pharm. 46 (2006) 157–162.
[81] R.J. Roscoe, J.L. Gittleman, J.A. Deddens, M.R. Petersen, W.E. Halperin, Blood lead
levels among children of lead-exposed workers: a meta-analysis, Am. J. Ind. Med.
36 (1999) 475–481.
[82] K.L. Hipkins, B.L. Materna, S. Payne, L. Kirsch, Family lead poisoning due to
occupation, Clin. Pediatr. 43 (2004) 845–849.
[83] M.J. Brown, J. Gardner, J.D. Sargent, K. Swartz, H. Hu, R. Timperi, The effectiveness
of housing policies in reducing children’s lead exposure, Am. J. Public Health 91
(2001) 621–624.