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Page 1: Author's personal copy - Harvard University · Author's personal copy Review Global approach to reducing lead exposure and poisoning Pamela A. Meyera,*, Mary Jean Brownb, Henry Falka

This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/copyright

Page 2: Author's personal copy - Harvard University · Author's personal copy Review Global approach to reducing lead exposure and poisoning Pamela A. Meyera,*, Mary Jean Brownb, Henry Falka

Author's personal copy

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 Statesb 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

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167

2. Adverse health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167

3. Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

3.1. Leaded gasoline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168

3.2. Smelters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169

3.3. Battery recycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169

3.4. Paint . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169

3.5. Traditional remedies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

3.6. Electronics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

4. Prevention strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

4.1. Identify sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171

4.2. Eliminate or control sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173

4.3. Monitor environmental exposures and hazards . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174

5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174

Mutation Research 659 (2008) 166–175

A R T I C L E I N F O

Article history:

Received 10 January 2008

Received in revised form 3 March 2008

Accepted 4 March 2008

Available online 20 March 2008

Keywords:

Lead poisoning

Primary prevention

Hazard control

Environmental health

A B S T R A C T

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.

* Corresponding author. Tel.: +1 770 488 0548; fax: +1 770 488 0701.

E-mail address: [email protected] (P.A. Meyer).

Contents lists available at ScienceDirect

Mutation Research/Reviews in Mutation Research

journal homepage: www.e lsev ier .com/ locate / rev iewsmrCommuni ty address : www.e lsevier .com/ locate /mutres

1383-5742/$ – see front matter . Published by Elsevier B.V.

doi:10.1016/j.mrrev.2008.03.003

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1. Introduction

Lead has been mined, smelted, and used in cosmetics, internaland topical medicinal preparations, and paint pigments and glazessince early recorded history [1]. As early as the second century B.C.,the symptoms of lead poisoning were described by the Greekphysician, Nikander [2]. The harmful effects of lead poisoning inworkers and children were described in the 19th century [3]. Bythe mid-1920s, studies detailed the dangers of cumulative doses oflead, the vulnerability of children, and the harm to the nervoussystem [3]. For years it was generally believed that children whodid not die during the acute stage of lead poisoning suffered nolong-term adverse health effects [4,5]. However, evidence ofadverse health effects that did not meet the diagnostic criteria forneurologic disease but were associated with lower intellectualfunctioning began to emerge in population-based epidemiologicstudies in the 1970s [6].

Despite growing evidence of adverse health effects related tolead, it is still widely used in consumer products and released intothe air through combustion of coals and oil, waste incineration, andfugitive emissions during mining and smelting. Many countrieshave taken steps to control the use of lead. For example, lead inhousehold paint was banned in Australia in 1920 and byinternational convention in 1925 [4]. The phase-out of lead ingasoline began in the mid-1970s in the United States; many othercountries have also banned leaded gasoline. However, more mustbe done to protect people in all nations. Worldwide a large numberof people are exposed, especially those in developing countries.This article will highlight adverse health effects and severalsources of lead exposure reported internationally in the scientificliterature since 2000. We recommend three strategies to preventpeople worldwide from ever being lead poisoned.

2. Adverse health effects

Lead is a potent and pervasive neurotoxicant. The toxic effectsof lead are the same regardless of the route of entry into the body,which are primarily ingestion and inhalation. Once absorbed, leadbinds to erythrocytes and travels in the blood to soft tissues, suchas the liver, kidneys, lungs, brain, spleen, muscles and heart. Afterseveral weeks, most of the lead moves into bones and teeth. Inadults about 94% of the total amount of lead in the body iscontained in the bones and teeth. About 73% of the lead inchildren’s bodies is stored in their bones. Lead can stay in bones fordecades [7].

Lead affects virtually every organ or system in the body, and theproposed mechanisms of lead toxicity involve fundamentalbiochemical processes. These proposed mechanisms include lead’sability to inhibit or mimic the action of calcium and to interact withproteins. One of the best documented mechanisms is impairmentof heme sysnthesis which results in adverse effects not limited tothe hematopoietic system. Most of the lead in blood is bound toerythrocytes [8] but plasma is the biologically active compartmentfrom which lead is available to cross cell membranes [9]. Blood-lead levels (BLLs) are related to diverse health effects, presumablybecause it is related to plasma lead, which exchanges with lead incritical target tissues, such as the brain, bone, erythroblasts andkidney.

The adverse health effects range from death [7] (Fig. 1) toimpaired cognitive and behavioral development that can havelifelong consequences for children. Children are more susceptiblethan adults to the effects of lead exposure because a proportio-nately greater amount of the lead they ingest is absorbed, morecirculating lead enters their brain, and their developing nervoussystem is more vulnerable to lead’s toxic effects [10]. In 1991, the

Centers for Disease Control and Prevention (CDC) responded to theincreasing number of studies that found adverse health effects inchildren at blood-lead levels as low as 10 mg/dL by issuing newguidelines. These included compiling an environmental history,educating parents about lead, and conducting follow-up forchildren with BLLs �10 mg/dL [11].

Recent research demonstrates that cognitive impairment isassociated with BLLs<10 mg/dL among children [12–18]. Lanphearet al. [12] analyzed data collected in NHANES III, a nationallyrepresentative sample of the US civilian population. They observedcognitive 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 andalso found an inverse relationship with BLLs <10 mg/dL andcognitive development. In the Rochester Longitudinal Study,Canfield [15] found that children’s intellectual functioning at ages3 and 5 years was inversely related to BLLs even when their peakBLL was <10 mg/dL. Bellinger and Needleman [16] re-analyzeddata on a cohort of children in Boston whose BLLs never exceeded10 mg/dL and found similar findings. Tellez-Rojo et al. followed acohort of children in Mexico City and tested them at ages 12 and 24months. The children’s BLLs did not exceed 10 mg/dL and there wasa significant inverse relationship between BLL and mental andpsychomotor development [17]. Lanphear et al. [18] pooled datafrom 7 international population-based longitudinal cohort studiesthat included 1333 children who were followed from birth orinfancy until ages 5–10 years and found intellectual deficits inchildren whose BLLs never exceeded 7.5 mg/dL. Importantly,studies identified no threshold for cognitive impairment due tolead exposure in children.

One expanding area of study is the effect of maternal leadburden on fetal and child development. Because more than 90% oflead in human adults is stored in the bone [19] it can be releasedinto the blood during times of bone resorption. One such time isduring pregnancy when mobilization of maternal bone into theblood stream can expose the developing fetus [20]. Evidence thatmaternal bone lead can be mobilized during pregnancy has beenprovided by isotopic studies [21,22]. In addition, there is a strongcorrelation between maternal and umbilical cord blood-lead levelsthat indicates the transfer of lead from mother to fetus [23].

Several cohort studies have provided more evidence thatprenatal exposure is associated with child cognitive development.Gomaa et al. [24] measured umbilical cord blood lead and infantbone lead and compared lead levels with this cohort’s scores on theMental Development Index (MDI) on the Bayley scales at age 2years. Infants with the lowest patella lead levels had higher MDIscores than infants with higher patella lead levels [24]. Because theeffects produced by a neurotoxic agent depend on the timing of theexposure [25], three of the cohort studies examined timing of leadexposure during pregnancy. Hu et al. [26] studied fetal lead toxicityduring each trimester of pregnancy as predictors of infantneurodevelopment. They found that fetal exposure to lead duringthe first trimester before the pregnancy is recognized may have agreater impact on adverse neurodevelopment later in life thanexposures during the second or third trimester [26]. The MexicoCity Prospective Lead Study [27] assessed the relationship of BLLscollected during the second and third trimester of pregnancy, atdelivery, and at multiple points throughout childhood with IQmeasured at 6–10 years of age. Higher maternal BLL at thirdtrimester of pregnancy, especially around week 28, was associatedwith decreased intellectual child development, even after con-trolling for other prenatal and postnatal lead measurements.Wasserman et al. [28] investigated the contribution of prenatal andpostnatal lead exposure to early intelligence. Blood samples werecollected from pregnant women living in Kosovo from 1985 to

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1986 at mid-pregnancy, delivery, and at subsequent 6-monthintervals for their prospective lead study. The study participants’infants were tested at ages 3, 4, 5, or 7 years to determineintellectual function. The findings suggested that prenatal andpostnatal exposures that occur at any time during the first 7 yearsof life are likely to be independently associated with smalldecrements in later IQ scores, even after controlling for socialfactors [28].

Cognitive function and lead levels among adults have also beenexamined. Shih et al. [29] reviewed 21 studies published from1996 to 2006 that compared markers of both recent (blood lead)and cumulative (bone lead) dose and their association withcognitive function. The association between cognitive function andbone-lead levels was consistently stronger than for BLLs amongenvironmentally exposed older adults. In contrast, among workerswith current lead exposure the association between cognitivefunction and BLLs was stronger than for bone levels.

Another area that has been associated with adult lead levels iscardiovascular disease. Navas-Acien et al. [30] conducted asystematic review of all observational studies through August2006 regarding lead and cardiovascular end points. Theysummarized findings from seven previous reviews of lead andblood pressure, all of which reported a positive association, albeitmodest, between lead exposure and blood pressure. They reviewed30 studies that examined lead levels and clinical cardiovascularendpoints (cardiovascular, coronary heart disease, stroke mortal-ity, and peripheral arterial disease) in both general and occupa-

tional populations. Although positive associations between leadexposure and cardiovascular disease were observed, severalmethodologic limitations existed.

3. Sources

The sources of lead exposures vary among and within countriesdepending on historic and current uses. The following sectionpresents several sources that have been described in the recentscientific literature.

3.1. Leaded gasoline

Leaded gasoline accounted for 80–90% of airborne leadpollution in large cities where it was used worldwide [31].Countries that have phased lead out of gasoline have reportedcorresponding decreases in lead concentrations in air and humanblood. The decreases in population BLLs have been dramatic. Forexample, mean BLLs in the United States, Ontario, Canada, and theUnited Kingdom were reduced by >70% as lead in gasoline wasreduced [32]. As more countries phase lead out of gasoline, similarfindings are reported. For example, Singh and Singh [33] reviewed15 research studies all of which measured lead in the environmentand some measured human blood during different periods. Thereviewers categorized the studies according to three stages of theirleaded gasoline phase-out: before (before 1996), during (1996–2000), and after (2000 and after). Reductions in lead concentra-

Fig. 1. Blood-lead levels associated with adverse health effects.

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tions were observed in tree leaves, water, air, and children’s bloodas lead was removed from gasoline [33]. In another study, Nichaniet al. [34] assessed children’s BLLs in Bombay, India, 2–3 years afterthe phase-out of leaded gasoline and compared their findings withresults from BLLs in a study conducted by the George Foundation in1997 (when leaded gasoline was still used in Bombay). Usingsimilar blood-collection procedures, the study conducted beforeleaded gasoline was banned showed that 61.8% of children hadBLLs �10 mg/dL compared with 33.2% after the phase-out [34].

3.2. Smelters

Metal smelters are another potential source of contaminationfor air and soil and can contribute to lead poisoning. Concernsabout the health effects for people living near smelters can promptinvestigations such as the study of children’s BLLs and risk factorsconducted in Torreon, Mexico, in March 2001 [35]. The Met-MexPenoles metal-processing plant, the largest in Latin America andfourth largest in the world, is located in Torreon. The mean BLL ofchildren living there was 6.0 mg/dL and 20% had BLLs�10 mg/dL in2001. BLLs and soil–lead levels increased in a dose–responsefashion as the distance from their homes to the smelter decreased.Leaded gasoline was not considered a significant contributor to thelead levels observed in Torreon because lead had been completelyphased-out from gasoline in Mexico in 1997 [36].

After smelter emissions stop, historic soil contamination canpose an ongoing threat. In June 2005, reports of symptomatic leadpoisoning 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 thewar. They were relocated to refugee camps situated on landcontaminated with lead and other heavy metal mining wastes nearthe Trepca smelter in Mitrovica. Considerable historic contamina-tion remains in the areas from the mining and smelting operationsthat occurred there for centuries. The current facility dates to the1930s and had been the economic base for the region. Operationsceased in 1999 when routine testing of United Nations peace-keeping forces identified soldiers with elevated BLLs. This findingmotivated testing of children living in the nearby refugee camps.All children had blood-lead levels >10 mg/dL, the level of concernfor young children. The mean BLL was 47 mg/dL in the camps ascompared 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 thehome, can be a source of lead exposure for nearby residents.‘‘Backyard’’ or ‘‘cottage’’ lead smelting has been described in thescientific literature for decades [38–40]. Reports of backyardsmelters as a cause of lead poisoning worldwide continue. Thesesmelters are usually unregulated and the magnitude of theproblem is not documented. A 1991 Jamaica study estimated thatabout one third of spent lead-acid batteries in Jamaica wererecycled by backyard smelting operations or by small batteryrepair shops scattered over the island [40]. These can be especiallydangerous to workers’ families and neighbors because the workareas rarely have proper ventilation or control of worker exposureor lead release. These operations create lead air emissions that thensettle and contaminate nearby soil, water, and food and can resultin high levels of lead exposure for families.

Other countries have also reported small secondary smelters assources of high dose lead exposure. Paoliello and DeCapitani [41]reviewed published studies of environmental contamination inBrazil and reported that, even though leaded gasoline is bannedand lead mining and primary smelting plants have closed,

hundreds of small secondary battery recycling plants that createlocal contamination still operate. A Middle Eastern study foundBLLs >10 mg/dL among 2.2% of young children in Israel, <1% inJordan, 5.2% in West Bank, and 17.2% in Gaza. All of the children inGaza with BLLs >10 mg/dL lived near local small smelters engagedin secondary recycling, smelting, and battery manufacture [42].

Melting lead to make fishing sinkers has also been reported as asource of lead exposure. In Cartagena, Colombia, the parents of allchildren with BLLs �10 mg/dL worked in and lived near smallmetal smelting factories with poor indoor air quality, or werefishers who made lead sinkers for their fishing nets. The highestBLLs were in children from a neighborhood near a shorelinewhere many family incomes were derived from fishing [43].Similarly, Brown et al. conducted a study in Chuuk, FederatedStates of Micronesia, and found that 61% of elevated BLLs amongchildren could be attributed to parents who made lead fishingweights [44].

3.4. Paint

The most common source of lead poisoning for the majority ofyoung children in the United States is deteriorated, leadedresidential paint and lead-contaminated house dust and soil. Leadwas commonly used in residential paint before 1950; in the 1960sthe paint industry voluntarily began to limit lead in residentialpaint. Although regulations limiting lead content in paint forresidential use were enacted in the United States in 1978, leadedpaint remains in many old homes. A wide distribution of housingbuilt before 1950 exists across the United States (Fig. 2) and poses apotential health threat. The need for ongoing vigilance washighlighted by the death of a 2-year-old Sudanese refugee girl who,on 21 April 2000, became the first child in the United States knownto die from lead poisoning in the 10 previous years [45]. Theexposure occurred in the United States and was caused by leadpaint in the home.

In response to her death, the state where the death occurredrevised its testing recommendations to include two tests forimmigrants, upon arrival, and 6 months after resettlement, tomonitor changes in BLLs. The state found that BLLs for nearly 30% ofthe refugee children became elevated after resettlement, whichsuggested that the lead exposure occurred in the United States.Investigations showed that elevated BLLs were associated withliving in old homes, the presence of lead hazards, behaviors thatincreased the chance of ingesting lead, and chronic and acutemalnutrition [46]. Malnutrition is common in refugee populations[47]. Anemia is a particular concern for children exposed to leadbecause iron deficiency can enhance lead absorption and, thus,increase risk for elevated BLLs.

Reports from Portugal, India, and South Africa indicate thatchildren in other countries are also being exposed to residentiallead paint. In Portugal’s Oporto Historical Center, a residential areacharacterized by houses with deteriorating lead paint that werebuilt in the 1900s, children aged 1–5 years were tested for leadpoisoning [48]. BLLs ranged from 4.7 mg/dL to 42.5 mg/dL with amean 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 positivefor 91% of children with BLLs �20 mg/dL and 14% for children withBLLs <10 mg/dL. In India, studies conducted in Mangalore andKarnataka found lead-based paint in the homes of 3 of the 10children with BLLs of at least 40 mg/dL. These 10 children were partof a blood-lead study of 107 school children who were randomlyselected [49]. In Johannesburg, South Africa, lead was found in thepaint of 17% of the homes sampled in old and new suburbs thatrepresented a variety of socioeconomic backgrounds. The percen-tage of lead by weight in some samples reached 29% [50]. Clark

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et al. conducted a study of lead content in paint samples in India,China and Malaysia and found that 66% of new paint samplescontained �5000 ppm (0.5%) of lead, the US definition of lead-based 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 wide-spread 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 andtoxic substances. For example, certain branches of ayurvedicmedicines contain heavy metals because the metals are thought tohave therapeutic benefits for particular ailments. Several cases oflead poisoning from ingesting medicinal products that contain leadin New Zealand [52], Italy [53], and the United States [54] havebeen reported in recent scientific literature. Traditional remediesthat contain lead have been reported to CDC for decades [52–64]. In2004, three cases of lead poisoning by ayurvedic medicines werereported to CDC. Subsequently, CDC posted an alert on theEpidemic Information Exchange (Epi-X), a web-based commu-nication that allows public health professionals to share pre-liminary surveillance information. In response to this posting, nineadditional adult cases of lead poisoning associated with ayurvedicmedicines were reported to CDC [54].

A traditional remedy imported from the Dominican Republicand sold in botanicas (i.e., shops that sell herbs) in the UnitedStates was associated with elevated BLLs in two children, twinboys, in Rhode Island [64]. When the boys were identified withelevated BLLs, an investigation for the lead source was conductedpromptly because investigators knew their home had beenremediated for lead. During the home inspection, litargirio wasfound in a jar in the boys’ bedroom. Litargirio has been used byDominicans, particularly those from rural areas, as an antiper-spirant/deodorant and as a traditional remedy for burns and fungalinfections of the feet. The boys had used the substance as anantiperspirant/deodorant. The litargirio was tested and contained790,000 ppm (79%) lead. When the children stopped usinglitargirio, their BLLs decreased [64].

3.6. Electronics

Most electronic devices contain lead and may represent anothersource of lead when discarded [65]. A study sponsored by the USEnvironmental Protection Agency (US EPA) reported that electro-nic items in landfills leached lead at levels exceeding the thresholdfor hazardous waste. The European Union recognized this potentialthreat to human health and the environment and acted by banningcertain electronic items from landfills. However, the US EPAs mostrecent estimate is that more than 2 million tons of electronic wasteis dumped in US landfills each year. EPA estimates that only about10% of all obsolete consumer electronics are recycled. The rest arestored somewhere, passed on to second users, or simply tossed inthe trash. US recyclers and watchdog groups estimate that 50% ofthe used US computers, cellphones, and TVs that are sent torecyclers are shipped overseas for recycling in facilities in Taizhou,China, or Lagos, Nigeria, as permitted by federal law. Much of thisobsolete equipment ends up as toxic waste with hazardouscomponents exposed, burned, or allowed to degrade in landfills.Waste by-products produced during informal recycling are heavilycontaminated with lead.

4. Prevention strategies

The striking aspect of these recent studies and reports is thatmost lead sources have been reported previously in the scientificliterature. Although this article does not represent an exhaustivesearch of all lead sources reported in the scientific literature, manyother sources such as children’s toys, jewelry, and candy areidentified and also tend to reappear (Table 1). These sources mayappear in new places and poison new populations and all werepotentially preventable.

The traditional approach to preventing lead poisoning hasbeen to act after exposure has occurred. The only medicaltreatment available is chelation, which can save lives in personswith very high BLLs. However, chelating drugs are not alwaysavailable in developing countries and have limited value inreducing the sequelae of lead poisoning [66,67]. Children aged 12–33 months with referral BLLs ranging from 22 to 44 mg/dL wereenrolled in a randomized clinical trial and received either placebo

Fig. 2. States with pre-1950 housing, 2000.

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or succimer. Neuropsychological tests at 3 years after randomiza-tion [66] and at age 7 years [67] revealed no developmentalbenefit in the group that received succimer. These findingshighlight the importance of implementing environmental mea-sures to prevent lead exposure. The best protection for all people isto control lead sources on a global scale. We recommend three keystrategies to prevent lead poisoning: identify sources, eliminate orcontrol sources, and monitor environmental exposures andhazards.

4.1. Identify sources

Sources of lead may be historic contamination, recycling oldlead products, or manufacturing new products. Vast reservoirs oflead remain in our environments and could emerge as healththreats. For example, old lead pipes in Washington, DC, did not

pose a serious health risk to local residents until a change in watertreatment [68] caused the lead to become more available indrinking water. Another potential hazard is lead paint in oldhomes. In the United States, an estimated 38 million homescontain lead-based paint. Although this represents a substantialreduction from 64 million homes with lead paint in 1990, there arestill 24 million that have significant lead hazards [69]. Whenhomes with lead paint deteriorate or are remodeled without takingproper lead-control precautions, the lead can become available indust and soil and result in human exposure.

Products imported from countries that do not adequately limitthe use of lead and enforce those regulations may also containharmful levels of lead. The United States has issued many recalls oftoys and children’s products in 2007 because they have been foundto contain lead (Table 2). In 2003, it was determined that a youngchild with a BLL of 123 mg/dL had swallowed a toy medallion [70].

Table 1Examples 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 Lead leaches from pots and wrappers 1998, 2002

Ceramic glaze Lead in ceramic glaze leached into stored beverages 1989, 2004, 2006

Traditional remedies Lead containing remedies, and traditional herbal medicines 1981, 1982,1983, 1984, 1989, 1993, 1999, 2002, 2004, 2005, 2005

Toy jewelry Ingestion of a necklace and a metallic charm 2004, 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].

Table 2US 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 Metals contain lead 2900 2/22/2008 China

Children’s Memory Testing Cards Surface paint 5300 2/22/2008 China

Children’s Table and Chair Surface paint 50 2/8/2008 China

Pendants and Candle Charms Metals contain lead 460,000 2/7/2008 Korea

Children’s Sketchbooks and Colored Spirals Paint on spiraled metal bindings 80,000 2/6/2007 China

Toy Gardening Hand Rakes Paint on toy 400 2/5/2008 China

Toy Wooden Block and Train Sets Surface paint 30,000 2/12/2008 China

Classroom Reading and Math Aids Surface paint 185,000 1/31/2008 China

Educational Assessment Blocks Surface paint 18,000 1/24/2008 China

Big Wooden Blocks and Wooden Train Sets Surface paint 15,000 1/24/2008 Hong Kong

Toy Racing Cars Surface paint 2000 1/23/2008 China

Cranium Cadoo Board Games Surface paint 38,000 1/17/2008 China

Play Mats Surface paint 60 1/16/2008 Taiwan

Toy Wrestler Figures Surface paint 5400 1/15/2008 China

Toy Wagons Surface paint 15,000 1/3/2008 China

Soldier Bear Toys Surface paint 11,400 12/19/2007 China

Duck Water Globes Painted base 60 12/13/2007 China

Princess Children’s Metal Jewelry Metal contains lead 1000 12/13/2007 China

Baby Toy and Speed Racer Cars Toys contain lead 300,000 12/13/2007 China

Fishing Games Parts contain lead 14,000 12/12/2007 China

Children’s Sunglasses Surface paint 260,000 12/7;2007 China

Potty Seats Decorative plaque in back of seat 160,000 12/6/2007 China

Mini Racing Helmets Surface paints 1400 12/5/2007 China

Children’s Metal Necklaces and Bracelets Jewelry contains lead 10,400 11/21/2007 China

Assorted Metal Jewelry Jewelry contains lead 205,000 11/21/2007 China

Children’s Necklace and Earring Sets Jewelry contains lead 4500 11/21/2007 China

Children’s Metal Jewelry Jewelry contains lead 43,000 11/21/2007 China

Children’s Pencil Pouches Paint of pouch zipper pulls 84,200 11/21/2007 China

Curious George Dolls Surface paint and hat 175,000 11/8/2007 China

Toy Robot Surface paints 2600 11/7/2007 China

Dizzy Ducks Music Box Surface paints 1300 11/7/2007 China

Winnie-the-Pooh Spinning Top Toys Surface paints 3600 11/7/2007 China

Big Red Wagons Surface paints 7200 11/7/2007 China

Duck Family Toys Surface paints 3500 11/7/2007 China

Toy Cars Surface paint 380,000 11/7/2007 China

Dragster and Funny Car Surface paint 75,000 11/7/2007 China

Galaxy Warriors Toy Figures Surface paint 380,000 10/31/2007 China

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The medallion was removed from his abdomen, tested, and foundto contain 38.8% lead. It had been purchased in a US vendingmachine and a recall was issued for 150 million of the necklaces.The child survived, however, the recall did not adequately protectall 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 theUnited States. The autopsy revealed a heart-shaped metallic charmin the abdomen that was found to have a lead content of 99.1%. Thecharms were recalled; this was the 15th recall of leaded toys in

Table 2 (Continued)

Product description Lead source Units recalled Date of recall Country of manufacture

Elite Operations Toys Surface coatings 16,000 10/31/2007 China

Ribbit Board Games Surface paint 1500 10/31/2007 China

Halloween Pails and Decorations Surface paint 142,000 10/25/2007 China

Children’s Metal Jewelry Jewelry contains lead 198,000 10/25/2007 China

WeGlow Children’s Metal Jewelry Jewelry contains lead 110,000 10/25/2007 China

Toy Gardening Toys Surface paint 97,000 10/25/2007 China

Princess Travel Art Set Lap Desks Surface paint on zipper pull of lap desk 7800 10/11/2007 China

Decorative Packaging Sold with Girl’s Gift Sets Surface coating on bead packaging 4000 11/1/2007 China

Toy Garden Rakes Surface paint 16,000 9/26/2007 China

Toy Watering Cans Surface paint 6000 8/28/2007 China

Go Diego Go Animal Rescue Boats Surface paints 38,000 10/25/2007 China

Children’s Puppet Theaters Surface paints 5400 10/17/2007 China

Halloween Skull Pails Surface paints 55,000 10/17/2007 China

Winnie-the-PoohPlay Sets Surface paints 49,000 10/11/2007 China

Mini Racing Helmets Surface paints 2500 10/11/2007 China

Dinosaur Toys Not specified 10,000 10/11/2007 China

Toy Decorating Sets Surface paint 15,000 10/4/2007 China

Toy Flashlights Surface paint 79,000 10/4/2007 China

Baby Einstein Color Blocks Surface paint 35,000 10/4/2007 China

Wooden Toys Surface paint 10,000 10/4/2007 China

Children’s Metal Necklaces Clasps on necklaces contain lead 850 9/26/2007 China

Children’s Metal Jewelry Sets Metal jewelry contains lead 23,500 9/26/2007 China

Puppet Theaters Surface paint 10,000 9/26/2007 China

Knights of the Sword Surface paints 800 9/26/2007 China

Toy Gardening Tools and Chairs Surface paint 350,000 9/26/2007 China

Thomas & Friends Wooden Railway Toys Surface paints 200,000 9/26/2007 China

Thomas & Friends Railway Toys Surface paints 1.5 million 6/13/2007 China

Bongo Band Toys Surface paints 8900 9/4/2007 China

Locomotive Toys Surface paints 90,000 9/4/2007 China

Barbie Accessory Toys Surface paints 675,000 9/4/2007 China

Wooden Coloring Cases Ink on outer packaging of cases 27,000 8/30/2007 China

Children’s Watering Cans Beak of watering can contains lead 6000 8/28/2007 China

Character Address Books and Journals Paint on metal spiral bindings 250,000 8/22/2007 China

Children’s Metal Jewelry Sets Metal jewelry sets contain lead 14,000 8/22/2007 China

Children’s Charm Bracelets Jewelry contain lead 7900 8/22/2007 China

Spinning Tops and Tin Pails Surface paints 66,000 tops; 4700 pails 8/22/2007 China

Toy Train Sets Surface paints 27,000 8/21/2007 China

Sarge’’ Die Cast Toy Cars Surface paints 253,000 8/14/2008 China

Character Toys Surface paints 967,000 9/2/2007 China

Soldier Bear Surface paints 13,000 7/18/2007 Hong Kong

Children’s Earring Sets Metal earring sets contain lead 220 7/17/2007 China

Children’s Metal Jewelry Sets Metal jewelry sets contain lead 20,000 7/5/2007 China

Solder Bear Surface paints 3000 5/23/2007 Hong Kong

Children’s Metal Jewelry Jewelry contains lead 103,000 5/31/2007 China

Children’s Gardening Gloves Painted logo on gloves contains lead 80 5/16/2007 China

Children’s Necklaces, Bracelets and Rings Jewelry contains lead 200,000 5/15/2007 China

Children’s Rings Rings contain lead 300,000 5/15/2007 China

Toy Drums Surface paints 4500 5/30/2007 China

Children’s Religious Fish Necklaces Necklaces contain lead 132,000 5/2/2007 China

Children’s Rings Rings contain lead 200 5/2/2007 India

Anima-Bamboo Collection Games Toys 5000 5/2/2007 China

Children’s Bracelets and Necklaces Surface paint 900,000 4/17/2007 India

Children’s Bracelets Paint on metallic band 4 million 4/3/2007 China

Stuffed Fun Balls Surface paints 7200 3/28/2007 China

Childrenr’s Necklaces Necklaces contain lead 58,000 3/15/2007 China

Children’s Mood Necklaces Jewelry contains lead 47,000 3/15/2007 China

Children’s Mood Necklaces Jewelry contains lead 3600 3/13/2007 China

Elite Operations Toys Surface coatings 128,700 3/13/2007 China

Children’s Easels Paint on chalkboard side of easels 2500 3/7/2007 China

Children’s Necklace and Earring Sets Jewelry contains lead 6000 2/23/2007 China

Children’s Rings Jewelry contains lead 115,000 2/23/2007 China

Boys’ Jackets Snap closures on jackets contain lead 8000 2/13/2007 China

Children’s Bracelets Jewelry contains lead 86,000 2/7/2007 China

Children’s Rings Jewelry contains lead 280,000 2/7/2007 China

Children’s Necklaces Pendant on necklace contains lead 113,800 1/18/2007 China

Children’s Clothing Coatings on snaps in overalls and shirt 200 1/5/2007 China

a Toy recalls posted on the Consumer Product Safety Commission website. Available at: http://www.cpsc.gov/cpscpub/prerel/category/toy.html.b Lead recalls posted on the Consumer Product Safety Commission website. Available at: http://www.cpsc.gov/cgi-bin/haz.aspx.

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2 years. In 2007, a series of recalls of children’s toys that weresuspected of containing lead was issued in the United States. Otherproducts that children can access also have been recalled overseveral decades.

4.2. Eliminate or control sources

Controlling potential sources of lead requires targeted and oftenmultiple approaches. These should include developing, imple-menting, and enforcing effective lead-control policies to reducelead emissions, clean contaminated sites, offer incentives toencourage 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 reducedangerous lead emissions from smelting facilities [72–76]. Soilremediation can lower lead concentrations [77–79] that remainlong after lead-smelting emissions are reduced. Without reductionof air emissions and remediation of soil, home hygiene and cleanneighborhood campaigns are of little value in decreasing elevatedBLLs.

The importance of regulations in lead-control efforts to preventre-emergence of known hazardous products is illustrated by theavailability of leaded house paint in countries without existinglaws [51]. A study that sampled house paint from four Asiancountries and tested their lead content found that some brands ofpaint sold in China, India and Malaysia had high lead content. Incontrast those same brands marketed in countries such asSingapore that had regulatory limits on lead in house paint eitherhad markedly lower or no detectable levels of lead [51].

Implementation and enforcement of safe worksite practices isanother lead-control strategy. Ye and Wong reviewed lead studiesreported in the Chinese scientific literature from 1990 to 2005 [80].

The authors compared workplace lead concentrations and theprevalence of lead poisoning among workers before and afterpassage of the 2002 Occupational Diseases Prevention Act thatincluded provisions for regulatory enforcement. Lead concentra-tions in both lead-battery and lead-smelter industries far exceededthe occupational exposure limits for lead before and after passageof the law. After passage of the law, the prevalence of leadpoisoning 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 theneed for stronger control measures and enforcement. Safe worksitepractices are also important to protect the workers’ familymembers from exposure to contaminated work clothes [81,82].

The impact of enforcing strong laws for the remediation ofhomes in which a child with an elevated BLL had been identifiedwas assessed. The assessment compared the number of propertiesthat had multiple children with elevated BLLs in two US states in1992–1993 with the number of these same properties that hadchildren with elevated BLLs 5 years later [83]. Both states had well-established, lead poisoning-prevention programs with nearlyuniversal testing of children and widespread public education.Both states had laws to remediate a home if a child with anelevated BLL was identified. The addresses of houses where a childwith a BLL �25 mg/dL lived between 1992 and 1993 wereidentified. A 5-year follow-up ascertained BLLs of children whosubsequently lived at those addresses. There was a fourfoldincreased chance of a subsequent child tenant being identifiedwith a BLL�10 mg/dL for a house in the state with limited laws andenforcement compared with a house in the state with strict lawsand enforcement.

Another lead-control strategy is to develop practices thatpromote the use of commercially available and technically well-

Fig. 3. Leaded petrol phase-out: global status.

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understood, safer alternatives to lead. The successful reduction inleaded gasoline use in many developing countries is attributed inpart to the World Bank’s practice of requiring that countriesinclude strategies to replace leaded gasoline with unleadedgasoline in their development plans. The World Bank supportsgovernments in adopting appropriate policies and developingstrategies, facilitating policies, and implementing lead phase-outstrategies [31]. These efforts have contributed to widespreadphase-out of leaded gasoline (Fig. 3). A similar approach could beadopted to control unregulated battery smelting by offering buy-back programs and ‘cradle to cradle’ registration of lead–zincbatteries 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 fordecades. Results of blood-lead testing can be used to identifypopulations at high risk and define risk factors for elevated BLLs,which can be used to target interventions. However, not allcountries have the resources to conduct population-based lead-poisoning surveillance. Targeted and episodic lead testing ofpopulations that may be at risk for lead poisoning can be a cost-effective way to identify and monitor population exposures [42].

Case management of individuals with elevated BLLs hasinvolved identifying and removing lead sources after exposurehas occurred. Ideally, we should monitor lead hazards to protectpeople before they are exposed. Lead levels in air are monitored inmany countries to ensure that the public’s health is protected.Businesses involving lead should routinely test their workers tomonitor BLLs. More can be done to track recycling of batteries andelectronic goods to ensure that emissions are properly contained toprotect families from exposure to lead and prevent contaminationof the environment. Testing of imported products that childrenmay use should be increased and tracked. The manufacture ofproducts, such as leaded paint and traditional medicines, incountries without strong lead-control laws and enforcement canresult in exposing people in many countries. Often, theseexposures are identified after a person with lead poisoning hasbeen diagnosed. Electronic health communication systems such aslistservs can alert public health practitioners to emerging threats.These systems disseminate information quickly across largegeographic areas and highlight issues that could be missed byroutine surveillance systems.

5. Conclusion

Even in countries where lead control has been vigilant, vastreservoirs of lead still exist in soil, dust, and house paint; thesesources will continue to contribute to the population lead burdenfor many years to come. In addition, lead is stored in bone,therefore, it can result in adverse health outcomes in adults manyyears after exposure. Further, maternal bone lead can be mobilizedduring pregnancy and serve as an endogeous source of leadexposure to the developing fetus [20]. In recognizing that there isno safe BLL for children and that chelating agents have limitedvalue in reducing the sequelae of lead poisoning, all nations shouldcontrol or eliminate lead hazards in children’s environmentsbefore they are exposed. Primary prevention, i.e., preventingpeople from being exposed to lead is the only solution.

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