Elevated blood lead levels in a riverside population in the Brazilian Amazon
Transcript of Elevated blood lead levels in a riverside population in the Brazilian Amazon
ARTICLE IN PRESS
Environmental Research 109 (2009) 594–599
Contents lists available at ScienceDirect
Environmental Research
0013-93
doi:10.1
$ Fun
Canadia
Center a
Ethica
and at U� Corr
E-m
journal homepage: www.elsevier.com/locate/envres
Elevated blood lead levels in a riverside population in the Brazilian Amazon$
Fernando Barbosa Jr.a,�, Myriam Fillion b, Melanie Lemire b, Carlos Jose Sousa Passos c,Jairo Lisboa Rodrigues a, Aline Philibert a, Jean-Remy Guimaraes d, Donna Mergler b
a Laboratorio de Toxicologia e Essencialidade de Metais, Departamento de Analises Clınicas, Toxicologicas e Bromatologicas, Faculdade de Ciencias Farmaceuticas de Ribeirao Preto,
Universidade de Sao Paulo, Avenida do cafe S/N Monte Alegre 14040-903, Ribeirao Preto-SP, Sao Paulo, Brazilb Centre de recherche interdisciplinaire sur la biologie, la sante, la societe et l’environnement (CINBIOSE), Universite du Quebec a Montreal, Montreal, Quebec, Canadac Faculdade UnB Planaltina, Universidade de Brasılia, Planaltina, DF, Brazild Laboratorio de Trac-adores, Instituto de Biofısica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil
a r t i c l e i n f o
Article history:
Received 14 August 2008
Received in revised form
7 March 2009
Accepted 23 March 2009Available online 22 April 2009
Keywords:
Lead
Amazon
Environmental exposure
Blood lead
Manioc
51/$ - see front matter & 2009 Elsevier Inc. A
016/j.envres.2009.03.005
ding sources and ethical considerations: This
n Institutes of Health Research, the Internat
nd by Fundac- ao de Apoio a Pesquisa do Esta
l approvals were obtained at Universite du
niversidade de Sao Paulo (Brazil).
esponding author. Fax: +5516 36331936.
ail address: [email protected] (F. Barbosa
a b s t r a c t
Lead (Pb) is recognized as one of the most toxic metals. Sources of Pb exposure have been widely
documented in North America, and the removal of Pb additives from gasoline was reflected in a
dramatic lowering of blood Pb concentration. In Latin America, the removal of Pb from gasoline resulted
in decreased exposure, but Pb levels in many areas remain high due to occupational and environmental
sources of exposure. While many of the Pb sources have been identified (mining, industries, battery
recycling, lead-based paint, ceramics), new ones occasionally crop up. Here we report on blood Pb (B-Pb)
levels in remote riverside communities of the Brazilian Amazon. Blood Pb (B-Pb) levels were determined
in 448 persons from 12 villages of the Lower Tapajos River Basin, Para, Brazil. Socio-demographic and
dietary information, as well as occupational, residential and medical history was collected using an
interview-administered questionnaire. B-Pb, measured by ICP-MS, showed elevated concentrations.
Mean B-Pb was 13.1mg/dL78.5, median B-Pb was 11.2mg/dL and ranged from 0.59 to 48.3mg/dL. Men
had higher B-Pb compared to women (median: 15.3mg/dL vs 7.9mg/dL respectively). B-Pb increased
with age for women, while it decreased for men. For both genders, B-Pb decreased with education.
There were significant differences between villages. Exploratory analyses, using linear partition models,
showed that for men B-Pb was lower among those who were involved in cattle-raising, and higher
among those who hunted, farmed and fished. The distribution profile of B-Pb directed us towards
artisanal transformation of manioc to flour (farinha), which requires heating in a large metal pan, with
stirring primarily done by young men. In the village with the highest B-Pb, analysis of Pb concentrations
(dry weight) of manioc (prior to transformation) and farinha (following transformation) from 6 houses
showed a tenfold increase in Pb concentration (mean: 0.01770.016 to 0.1970.10mg/g). This was
confirmed in one of these villages where we sampled manioc paste (just before roasting) and the
roasted farinha (0.05mg/g vs 0.20mg/g). While there may be other sources (ammunition, sinkers for
fishing nets), the high concentrations in farinha, a dietary staple, assuredly makes an important
contribution. Further action needs to reduce Pb sources in this region.
& 2009 Elsevier Inc. All rights reserved.
1. Introduction
Lead (Pb) is recognized as one of the most toxic metals.Historically, there have been many reports of people sufferingfrom Pb toxicity throughout history, from the times of the RomanEmpire, through the Middle Ages and the Industrial Revolution
ll rights reserved.
study was supported by the
ional Development Research
do de Sao Paulo (FAPESP).
Quebec a Montreal (Canada)
Jr.).
(Nriagu, 1983; Woolley, 1984). With the increasing industrializa-tion in the 19th century, scientific studies documented high levelsof occupational exposure to Pb in workers, who presentedsymptoms of acute and chronic disease (Hernberg, 2000). Overthe past three decades, studies focussing on low-level environ-mental exposures to Pb have shown its harmful effects onchildren’s neurodevelopment and behaviour, as well as its long-lasting effects on many target organs in both children andadults (Hernberg, 2000; Kosnett et al., 2007; Needleman, 2004).The Centers for the Disease Control and Prevention (CDC) ofthe United States established the screening action guideline inchildren at 10mg/dL in whole blood, but there is increasingconcern about the absence of a threshold at which deleteriouseffects occur (Barbosa et al., 2005; Bellinger, 2004; Lanphear et al.,
ARTICLE IN PRESS
F. Barbosa Jr. et al. / Environmental Research 109 (2009) 594–599 595
2003) and it has been suggested that this limit should be loweredto 2mg/dL (Gilbert and Weiss, 2006).
Sources of Pb have been widely studied in North America(Bellinger and Bellinger, 2006; Schwartz and Hu, 2007) and therehave been many initiatives to reduce exposures notably throughthe introduction of unleaded gasoline (Landrigan, 2002; Schwartzand Hu, 2007), but also through the removal of Pb-based paintand an increased vigilance of Pb-containing objects, such asceramics, jewellery and children’s toys (Goldman et al., 2004). Inthe United States and other industrialized countries, thesemeasures have resulted in a significant decrease in concentrationsof biomarkers of Pb exposure (Landrigan, 2002; Schwartz and Hu,2007). However, in many less-industrialized countries, althoughthe removal of Pb from gasoline is reflected in decreased blood Pb(B-Pb) levels, concentrations have, for the most part, remainedhigher than in the industrialized countries (Fewtrell et al., 2004;Landrigan et al., 2000; Olivero-Verbel et al., 2007).
In Latin America, Pb exposure has been reported primarily forindustrial workers and communities living around urban indus-trial facilities (Barbosa et al., 2006a; Gomes et al., 2004; Paolielloand De Capitani, 2005, 2007; Romieu, 2003; Romieu et al., 1990,1997), as well as in mining areas in the Andes (Cooke et al.,2007; Rojas and Vandecasteele, 2006). In Mexico, there have beenconsiderable efforts to document environmental exposure, andseveral studies were carried out over the last decade (Rothenberget al., 2000; Schnaas et al., 2004; Tellez-Rojo et al., 2002; Wrightet al., 2003). In 1991, Mexico introduced unleaded gasoline (PNUE,2006), resulting in an important decrease in B-Pb (Schnaas et al.,2004). However, B-Pb levels are still high in this country, due tothe numerous industrial activities in Mexico city or due to folkceramic manufacturing in other areas of the country (Hernandez-Serrato et al., 2003).
In Brazil, Pb exposure has been documented since the 1970s,mainly in industrial and mining areas (Barbosa et al., 2006b, c;Paoliello and De Capitani, 2007; Paoliello et al., 2002). Now thatPb mining has ceased in Brazil, industrial activities like batteryrecycling are considered the main sources of Pb emission in theenvironment (Paoliello and De Capitani, 2007). A study in thestate of Sao Paulo among men and women with a history of Pbexposure from a nearby battery plant showed B-Pb concentrationsranging from 1.0 to 42.8mg/dL (mean 7.6mg/dL) (Barbosa et al.,2006b). On the other hand, no information is available on Pbexposure in remote populations in Brazil. The objective of thepresent study was to determine B-Pb levels in riverside commu-nities of the Tapajos River in the Brazilian Amazon.
Table 1Socio-demographic characteristics.
n (%) Mean7SD Range
Women 232 (52.0)
Men 214 (48.0)
Age (years) 41.4716.6 15–87
Education (years) 4.8973.41 0–16
Smokers 113 (74.7)
Drinks alcohol 234 (52.3)
Body mass index 24.674.1 16–87
Born in the region 396 (88.6)
Village directly on the river 304 (67.6)
Number of fish meals (last 7 days) 6.0274.09 0–15
Subsistence activities
Fishing 295 (67.4)
Farming 267 (59.1)
Cattle-raising 156 (35.1)
Hunting 122 (27.3)
Raising pigs and/or chickens 342 (76.7)
2. Materials and methods
2.1. Study population
As part of a cross-sectional study on factors that affect human mercury (Hg)
exposure and its health effects, blood samples were taken from 448 persons
(216 men and 232 women) from 12 communities on the Lower Tapajos River Basin,
State of Para, Brazil. Recruitment was carried out in each village through house-to-
house visits and at village meetings, during which the research project was
explained, and villagers were invited to participate on a voluntary basis. Persons
who accepted to participate were scheduled for testing and then brought by boat
to a technical college in a nearby city, where biological samples were taken.
Trained interviewers administered questionnaires on socio-demographic informa-
tion, occupational, residential and medical history and dietary information.
The study was approved by the Federal University of Rio de Janeiro, which
has a mandate from the Ethics Review Board of the Conselho Nacional de
Desenvolvimento Cientıfico e Tecnologico (CNPq) of Brazil, the internal review
boards of the University of Sao Paulo in Ribeirao Preto and of the University of
Quebec at Montreal. All participants signed an informed consent form, which was
read to them.
2.2. Blood collection and analysis
For each participant, a trained Brazilian nurse collected 6-ml blood
samples. Blood samples were collected in ‘‘trace metals free’’ evacuated tubes
(BD Vacutainers) containing heparin. Then, the blood was transferred using a
pipette into cryogenic tubes previously cleaned in a class 100 clean room and
immediately frozen at �20 1C before analysis.
Pb levels in whole blood were determined at the Laboratory of Metals
Toxicology, University of Sao Paulo in Ribeirao Preto (Brazil), by Inductively
Coupled Plasma-Mass Spectrometry (ICP-MS), using the method published by
Palmer et al. (2006). The detection limit was 0.05mg/L Pb.
Quality control (QC) for Pb determination was assured by analyzing Standard
Reference Materials from the US National Institute of Standards and Technologies
(NIST 955c). In addition, various secondary reference materials provided either by
the New York State Department of Health (NYS DOH PT program for trace elements
in whole blood) or by the Institut National de Sante Publique du Quebec, Canada
(INSP-external quality assessment scheme (EQAS) for trace elements in whole
blood) were analyzed. Reference samples were analyzed before and after ten
ordinary samples. Experimental values were always in good agreement with the
provided reference or certified ranges.
2.3. Pb determination in manioc and flour samples
Raw manioc paste and roasted flour (farinha) samples were taken from
artisanal manioc transformation installations at 6 houses in the village with the
highest mean B-Pb concentration. Samples were collected in 10 ml screw cap tubes
and frozen at �201C until analyses. The samples were digested in closed vessels
with a microwave digestion system. Samples (0.20 g) were accurately weighed in a
PFA digestion vessel, and then 4 ml of nitric acid 14 mol/L+2 mL of 30% (v/v) H2O2
was added. The bomb was placed inside the microwave oven, and decomposition
was carried out according to the program described by Nardi et al. (2009). After
that, the digestate was left to cool and then the volume made up to 50 mL with
Milli-Q water. Digested samples were analyzed for Pb determination by using an
ICP-MS according to the procedure proposed by Nardi et al. (2009).
2.4. Statistical analyses
Descriptive statistics were used to characterize the population. Correlations,
simple and multiple regression analyses were used to explore the relations
between B-Pb and independent variables. Logistic regression models were used to
characterize Pb exposure among different groups. Recursive partition modeling
was used to explore how to best split with respect to age, education, village
location, and subsistence activities (fishing, farming, hunting, raising cattle). Non-
parametric paired analyses were used to examine differences in Pb concentration
in manioc and farinha from the same house. Statistical analyses were performed
using the JMP software, version 5.0.1 (SAS Institute Inc.).
3. Results
Table 1 presents the socio-demographic characteristics of thestudy population. Age ranged from 15 to 87 years and they hadlimited formal education; 37.8% had less than 4 years of schooling.
ARTICLE IN PRESS
Blood Pb (µg/dL)
25
50
75
0 10 20 30 40 50
Freq
uenc
y
Fig. 1. Distribution of B-Pb.
0.00
0.25
0.50
0.75
1.00
Perc
entil
e
0 10 20 30 40 50
Blood Pb (µg/dL)
womenmen
Fig. 2. Percentile distribution of B-Pb in women and men.
Table 2B-Pb (mg/dL) by village for women and men.
Village Women Men Wilcoxon signed rank
n Median Range n Median Range p
Ac 11 16.0 8.1–27.3 17 22.0 11.7–45.5 0.005
C-Ti 13 14.4 3.6–23.2 11 13.7 3.9–48.3 0.95
NCa 15 13.7 6.0–35.6 19 16.8 8.1–38.4 0.21
VA 18 12.2 1.5–29.9 25 17.3 5.6–31.8 0.05
SLTa 15 10.3 4.6–31.5 19 16.8 4.0–30.1 0.07
C-Te 15 9.1 3.7–28.5 9 16.7 7.8–29.1 0.01
SA 23 9.0 0.6–24.5 29 14.0 5.1–27.3 0.001
NP 6 7.7 3.2–18.9 7 17.0 8.2–22.4 0.10
Ipa 34 6.7 0.7–23.2 17 12.8 7.2–42.2 o0.001
Mua 15 6.2 1.3–15.8 8 13.6 7.5–17.9 0.01
BLa 49 5.8 0.9–22.0 35 13.0 4.1–36.4 o0.001
SCa 17 5.4 1.0–15.5 16 9.2 5.6–35.9 0.001
a Village located directly on the Tapajos River.
F. Barbosa Jr. et al. / Environmental Research 109 (2009) 594–599596
The large majority were born in the region, while the others weremostly immigrants from the north-eastern States of Brazil. In thispopulation, 25.6% smoked and their mean number of cigaretteswas 7/day. For 86%, body mass index (BMI) was in the normalrange between 18.5 and 30 kg/m2, with 3% consideredunderweight, with a BMI below 18.5 kg/m2, and 11% consideredobese with a BMI above 30 kg/m2. Over half of the populationcarried out subsistence fishing and farming.
Fig. 1 presents the distribution of B-Pb. Mean B-Pb is13.1mg/dL78.5, with a median of 11.2mg/dL, ranging from 0.59to 48.3mg/dL. Overall, men presented significantly higher B-Pbcompared to women, median: 15.33 and 7.86mg/dL, respectively.Their percentile distributions are presented in Fig. 2. A total of 79%of men and 35.8% of women had B-Pb X10mg/dL; 32.6% of womenof child-bearing age (15–45 years) presented B-Pb concentrationsX10mg/dL. A total of 30.4% of men and 8.2% of women presentedconcentrations X20mg/dL.
There were highly significant differences in B-Pb by village(ANOVA; po0.0001). Table 2 presents the results for menand women from the 12 villages. A threefold difference wasobserved between the village with the least and highest medianconcentrations of B-Pb. It is interesting to note that the genderdifferences, observed in the entire group, are not present in allof the villages. When the villages are grouped by whether they aredirectly on the Tapajos River or not, persons from the 6 villagesthat were not directly on the Tapajos River displayed signifi-cantly higher levels (median 13.1mg/dL vs 10.9mg/dL; Wilcoxonpo0.001), but these differences were much more pronounced inwomen (10.3mg/dL vs 6.9mg/dL; Wilcoxon po0.001) than in men(16.9mg/dL vs 13.7mg/dL; Wilcoxon p ¼ 0.13).
In simple regression models, there was an increase in B-Pbwith age for women (B ¼ 0.06; r2
¼ 0.02; p ¼ 0.02), while for menit was the contrary: B-Pb decreased with age (B ¼ �0.08;r2¼ 0.02; p ¼ 0.02). For women whose age was X40 years,
43.0% had B-Pb X10mg/dL compared to 29.6% for those who wereyounger (Chi square: p ¼ 0.03). However, for men X40 years22.2% had B-Pb X20mg/dL compared to 40.2% for the younger(Chi sq: p ¼ 0.004).
For both genders, B-Pb decreased with education, but while itwas highly significant for women (B ¼ 0.52; r2
¼ 0.08; po0.0001),for men it showed only a tendency (p ¼ 0.10). A total of 40.8%of women with 6 years or less of schooling presented B-PbX10mg/dL compared to 24.3% of the more educated (Chi sq:p ¼ 0.01). For men, these differences were 82.6% vs 67.3% for thosewith more schooling (Chi sq: p ¼ 0.02).
In a logistic regression model for B-Pb X10mg/dL with thecovariables, age and education, for women, only educationentered significantly into the model; the OR for B-Pb X10mg/gfor women with less education is 1.99 [95% CI: 1.04–1.72]. Formen, it was both age and education; for younger men (p40 years)to have B-Pb X10mg/dL, the OR is 2.46 [95% CI: 1.18–5.44], whilefor men with less education, the OR is 3.24 [95% CI: 1.47–7.21]. Noassociation was observed between B-Pb and smoking, drinkingor BMI.
Recursive partition modeling was used to explore how to bestsplit with respect to age, education, village location, andsubsistence activities (fishing, farming, hunting, raising cattle).The results of the decision tree are presented in Fig. 3. After theinitial separation on gender, for women, the second cut was oneducational level with those with less education presentinghigher B-Pb concentrations. On the next level, among themore poorly educated, those who live on the tributaries of theTapajos present higher Pb compared to those who live directlyon the Tapajos. For the more educated women, it is interestingto note that like the men (see below), those who hunt havehigher Pb levels, but only 3 women report being involved in thisactivity.
For men, the first division is on hunting with hunterspresenting higher Pb. Among the hunters, those that are involvedin cattle-raising have lower Pb, while for those that are notinvolved in cattle-raising, the subsequent division is for farmingactivities (although in this group only 5 are not also farming).Almost all of these are also involved in fishing activities. A similardistribution is seen with those who do not hunt: those who raisecattle have lower B-Pb and for those who do not raise cattle,fishers have higher Pb. The highest B-Pb is observed for those thathunt, are not involved in cattle-raising, but farm and fish.
ARTICLE IN PRESS
Riversiden = 111
10.0 ± 7.7 µg/dL
Tributaryn = 47
12.4 ± 6.3 µg/dL
Education <6yn = 158
10.7 ± 7.0 µg/dL
Doesn't huntn = 71
6.8 ± 4.5 µg/dL
Huntsn = 3
13.8 ± 7.7 µg/dL
Education ³ 6yn= 74
7.1 ± 4.8 µg/dL
Womenn = 232
9.6 ± 6.6 µg/dL
Huntsn = 106
19.5 ± 9.3
Raises cattlen = 49
16.4 ± 7.0 µg/dL
Doesn't raise cattlen = 57
22.1 ± 10.2 µg/dL
Doesn't farmn = 5
15.4 ± 3.7µg/dL
Farmsn = 52
22.8 ± 10.4 µg/dL
Doesn't huntn = 108
14.5 ± 7.3 µg/dL
Raises Cattlen = 40
11.6 ± 5.1µg/dL
Doesn't raise catten = 68
16.1 ± 7.9 µg/dL
Doesn't fishn = 18
13.9 ± 6.3 µg/dL
Fishesn = 50
16.9 ± 8.3 µg/dL
Menn = 214
17.0 µg/dL ± 8.7 µg/dL
Total groupn = 446
13.1± 8.1 µg/dL
Fig. 3. Recursive partition modeling.
0
0.1
0.2
0.3
0.4
manioc farinha
F
E
DC
B
A
Pb (
µg/g
)
Fig. 4. Manioc and farinha Pb concentrations for 6 houses.
F. Barbosa Jr. et al. / Environmental Research 109 (2009) 594–599 597
The socio-demographic and occupational distributions of B-Pblead us to examine the various activities that could be sourcesof Pb exposure. A large percentage of families in the village withthe highest Pb levels were involved in the artisanal productionof flour (farinha) from manioc. The process involves roasting themanioc pulp in a large metal plate and requires constant stirring.Although family members participate, the stirring activity overthe hot fire is generally carried out by young men. Since the metalplate could be a potential source of Pb, we took samples of maniocand farinha from 6 homes where family members were involvedin the production of farinha. Mean Pb concentration (dry weight)for manioc was 0.017mg/g70.016 (median: 0.012mg/g, range:0.003–0.04mg/g) while for farinha it was 0.19mg/g70.10 (median:0.19; range: 0.09–0.38mg/g). The increase is significant (pairedt-test: po0.008); Fig. 4 shows the data from each of the houses.Increases range from 4- to 33-fold. To confirm these findings,at a later date and in one of the villages, we took samples ofmanioc paste, just before it was roasted and roasted farinha. Pbconcentration in manioc paste was 0.05mg/g, while in the roastedfarinha it was 0.20mg/g.
4. Discussion
The results of this study show elevated B-Pb concentrations inthis Amazonian population, where there is no documented sourceof occupational or environmental Pb. Fifty-seven percent (57%) ofparticipants had B-Pb levels equal to or higher than 10mg/dL, with19% presenting levels above 20mg/dL. Three men had levelsX40mg/dL. In comparison, today in North America, B-Pb variesbetween 1 and 10mg/dL in non-exposed population, and between20 and 40mg/dL in occupationally exposed population (Lanphearet al., 2002). The mean B-Pb (13.1mg/dL) observed in the presentstudy is also considerably higher than 7.56mg/dL, reported byBarbosa et al. (2006b) in the region of Sao Paulo State for personswho had lived for at least 3 years in the vicinity of a battery plant.
The elevated concentrations of B-Pb were surprising for theseremote villages and we examined the possibility of exposure fromknown sources. Recent studies in Latin America continue toidentify populations with high Pb concentrations associated withthe use and/or manufacture of lead-glazed ceramics. ElevatedPb exposure (mean 43.5mg/dL) was reported in a population studyof the city of Oaxaca, Mexico; use of ceramic pottery andoccupational exposure and smoking were identified as the majorrisk factors (Hernandez-Serrato et al., 2003). In Ecuador, childrenliving in an area with a local ceramic glazing cottage industrypresented a mean B-Pb of 18.0mg/dL (Counter et al., 2008). Inthe area of the present study, ceramic pottery is not used ormanufactured in these villages. Brazil banned Pb additives ingasoline in the 1970s and replaced it with 22% ethanol (Paolielloand De Capitani, 2007), and in most of the villages in this study,there are no roads or vehicles, although fuel is used for motorizedboats.
The variations in B-Pb with respect to gender, age, education,community and subsistence activities proved useful to directfurther investigation to determine possible sources of Pbexposure. Certain villages have significantly higher exposurecompared to others and young men with less education andwomen of all ages with less education presented higher exposurescompared to others. We thus examined men and women’sactivities, particularly in the village with the highest exposures.In this village, many families are involved in the productionof farinha. The process requires soaking manioc in the river for afew days, taking off the skin, grating the white root, draining the
ARTICLE IN PRESS
F. Barbosa Jr. et al. / Environmental Research 109 (2009) 594–599598
pulp, and roasting the pulp on a large metal plate. The metal plateis commercially manufactured and was purchased in Itaituba, thenearby urban center. While the pulp is roasting over a hot fire,persons, most often young men, spend several hours stirring thepulp. The large increase in Pb concentration between the rawmanioc paste and the roasted flour points to the metal plate as apossible important source of Pb exposure. Exposure may occurthrough inhalation of Pb vapours as well as through consumptionof farinha. While in this village, farinha is mostly consumed by thevillagers themselves, other villages produce farinha for sale in themarkets of local towns.
Our exploratory analyses of the profile of B-Pb concentrationslikewise indicate that hunters have high Pb levels comparedto others, suggesting that ammunition may contain Pb. It isinteresting to note that although there are only 3 women whoreport hunting, their B-Pb concentrations are much higher thanother women. The higher levels in fishers and farmers comparedto those who raise cattle may reflect that persons involved in thelatter subsistence activities may be those who are also involved inthe production of farinha, or that other objects may contain Pb,notably sinkers used for fishing nets.
The surprisingly high B-Pb concentrations found in thesecommunities of the Brazilian Amazon reveal, as pointed out in theBrescia Declaration (Landrigan et al., 2000), that we should notlose our vigilance with respect to Pb exposure. The levels observedhere have been associated with lowered intellectual facultiesin children (Bellinger et al., 1992; Tellez-Rojo et al., 2006) andwith cardiovascular problems in adults (Navas-Acien et al., 2004;Park et al., 2006). We do not know for how long this situation hasexisted. Action needs to be taken to identify and reduce thesources of Pb exposure.
A further concern is that this population is likewise exposed tomercury through fish consumption (Dolbec et al., 2001; Doreaet al., 2003; Harada et al., 2001; Lebel et al., 1998; Pinheiro et al.,2006; Santos et al., 2000) and gold–Hg amalgam burning (SantaRosa et al., 2000). Experimental studies in rats showed that, whencombined with Hg, low doses of Pb had effects on the weightof the thymus, kidney and adrenals (Institoris et al., 2006) andon development (Belles et al., 2002). Likewise, the concomitantexposure to Pb and Hg may have important consequences onfoetal development, child and adult health, but there is littleinformation available about these multiple exposures (Bellinger,2007). Further analyses of the data from this study will examinethe concomitant effects of environmental exposure to Hg and Pbon several health outcomes.
Acknowledgments
This study was made possible through the participation of allvillagers and Brazilian field assistants. We are grateful to Marie-Eve Thibault for her amazing help through all the steps of thisproject. Funding was provided by the Canadian Institutes forHealth Research (CIHR) and by Fundac- ao de Amparo a Pesquisa doEstado de Sao Paulo (FAPESP).
References
Barbosa Jr., F., Tanus-Santos, J.E., Gerlach, R.F., Parsons, P.J., 2005. A critical reviewof biomarkers used for monitoring human exposure to lead: advantages,limitations, and future needs. Environ. Health Perspect. 113, 1669–1674.
Barbosa Jr., F., Correa Rodrigues, M.H., Buzalaf, M.R., Krug, F.J., Gerlach, R.F., Tanus-Santos, J.E., 2006a. Evaluation of the use of salivary lead levels as a surrogate ofblood lead or plasma lead levels in lead exposed subjects. Arch. Toxicol. 80(10), 633–637.
Barbosa Jr., F., Ramires, I., Rodrigues, M.H., Saint’ Pierre, T.D., Curtius, A.J., Buzalaf,M.R., et al., 2006b. Contrasting effects of age on the plasma/whole blood lead
ratio in men and women with a history of lead exposure. Environ. Res. 102 (1),90–95.
Barbosa Jr., F., Sertorio, J.T., Gerlach, R.F., Tanus-Santos, J.E., 2006c. Clinical evidencefor lead-induced inhibition of nitric oxide formation. Arch. Toxicol 80 (12),811–816.
Belles, M., Albina, M.L., Sanchez, D.J., Corbella, J., Domingo, J.L., 2002. Interactionsin developmental toxicology: effects of concurrent exposure to lead, organicmercury, and arsenic in pregnant mice. Arch. Environ. Contam. Toxicol. 42 (1),93–98.
Bellinger, D.C., 2004. Lead. Pediatrics 113 (4 Suppl), 1016–1022.Bellinger, D.C., 2007. Lead neurotoxicity in children: decomposing the variability in
dose–effect relationships. Am. J. Ind. Med. 50 (10), 720–728.Bellinger, D.C., Bellinger, A.M., 2006. Childhood lead poisoning: the torturous path
from science to policy. J. Clin. Invest. 116 (4), 853–857.Bellinger, D.C., Stiles, K.M., Needleman, H.L., 1992. Low-level lead exposure,
intelligence and academic achievement: a long-term follow-up study.Pediatrics 90 (6), 855–861.
Cooke, C.A., Abbott, M.B., Wolfe, A.P., Kittleson, J.L., 2007. A millennium ofmetallurgy recorded by lake sediments from Morococha, Peruvian Andes.Environ. Sci. Technol. 41 (10), 3469–3474.
Counter, S.A., Buchanan, L.H., Ortega, F., 2008. Zinc protoporphyrin levels, bloodlead levels and neurocognitive deficits in Andean children with chronic leadexposure. Clin. Biochem. 41 (1-2), 41–47.
Dolbec, J., Mergler, D., Larribe, F., Roulet, M., Lebel, J., Lucotte, M., 2001. Sequentialanalysis of hair mercury levels in relation to fish diet of an Amazonianpopulation, Brazil. Sci. Total Environ. 271 (1–3), 87–97.
Dorea, J., Barbosa, A.C., Ferrari, I., de Souza, J.R., 2003. Mercury in hair and in fishconsumed by Riparian women of the Rio Negro, Amazon, Brazil. Int. J. Environ.Health Res. 13 (3), 239–248.
Fewtrell, L.J., Pruss-Ustun, A., Landrigan, P., Ayuso-Mateos, J.L., 2004. Estimatingthe global burden of disease of mild mental retardation and cardiovasculardiseases from environmental lead exposure. Environ. Res. 94 (2), 120–133.
Gilbert, S.G., Weiss, B., 2006. A rationale for lowering the blood lead action levelfrom 10 to 2 microg/dL. Neurotoxicology 27 (5), 693–701.
Goldman, L., Falk, H., Landrigan, P.J., Balk, S.J., Reigart, J.R., Etzel, R.A., 2004.Environmental pediatrics and its impact on government health policy.Pediatrics 113 (4 Suppl.), 1146–1157.
Gomes, V.E., Rosario de Sousa Mda, L., Barbosa Jr., F., Krug, F.J., Pereira Saraiva Mda,C., Cury, J.A., Gerlach, R.F., 2004. In vivo studies on lead content of deciduousteeth superficial enamel of preschool children. Sci. Total Environ. 320 (1),25–35.
Harada, M., Nakanishi, J., Yasoda, E., Pinheiro, M.C., Oikawa, T., de Assis Guimaraes,G., et al., 2001. Mercury pollution in the Tapajos River basin, Amazon: mercurylevel of head hair and health effects. Environ. Int. 27 (4), 285–290.
Hernandez-Serrato, M.I., Mendoza-Alvarado, L.R., Rojas-Martinez, R., Gonzalez-Garza, C., Hulme, J.M., Olaiz-Fernandez, G., 2003. Factors associated with leadexposure in Oaxaca, Mexico. J. Expo Anal. Environ. Epidemiol. 13 (5), 341–347.
Hernberg, S., 2000. Lead poisoning in a historical perspective. Am. J. Ind. Med. 38(3), 244–254.
Institoris, L., Kovacs, D., Kecskemeti-Kovacs, I., Lukacs, A., Szabo, A., Lengyel, Z.,et al., 2006. Immunotoxicological investigation of subacute combinedexposure with low doses of Pb, Hg and Cd in rats. Acta Biol. Hung. 57 (4),433–439.
Kosnett, M.J., Wedeen, R.P., Rothenberg, S.J., Hipkins, K.L., Materna, B.L., Schwartz,B.S., et al., 2007. Recommendations for medical management of adult leadexposure. Environ. Health Perspect. 115 (3), 463–471.
Landrigan, P.J., 2002. The worldwide problem of lead in petrol. Bull. World HealthOrgan. 80 (10), 768.
Landrigan, P.J., Boffetta, P., Apostoli, P., 2000. The reproductive toxicity andcarcinogenicity of lead: a critical review. Am. J. Ind. Med. 38 (3), 231–243.
Lanphear, B.P., Dietrich, K.N., Berger, O., 2003. Prevention of lead toxicity in USchildren. Ambul. Pediatr. 3 (1), 27–36.
Lanphear, B.P., Hornung, R., Ho, M., Howard, C.R., Eberly, S., Knauf, K., 2002.Environmental lead exposure during early childhood. J. Pediatr. 140 (1), 40–47.
Lebel, J., Mergler, D., Branches, F., Lucotte, M., Amorim, M., Larribe, F., et al., 1998.Neurotoxic effects of low-level methylmercury contamination in the Amazo-nian Basin. Environ. Res. 79 (1), 20–32.
Nardi, E.P., Evangelista, F.S., Tormen, L., Saint’Pierre, T.D., Curtius, A.J., Souza, S.S.,et al., 2009. The use of inductively coupled plasma mass spectrometry(ICP-MS) for the determination of toxic and essential elements in differenttypes of food samples. Food Chem. 112 (3), 727–732.
Navas-Acien, A., Selvin, E., Sharrett, A.R., Calderon-Aranda, E., Silbergeld, E., Guallar,E., 2004. Lead, cadmium, smoking, and increased risk of peripheral arterialdisease. Circulation 109 (25), 3196–3201.
Needleman, H., 2004. Lead poisoning. Annu. Rev. Med. 55, 209–222.Nriagu, J.O., 1983. Lead and Lead Poisoning in Antiquity. Wiley, New York.Olivero-Verbel, J., Duarte, D., Echenique, M., Guette, J., Johnson-Restrepo, B.,
Parsons, P.J., 2007. Blood lead levels in children aged 5–9 years living inCartagena, Colombia. Sci. Total Environ. 372 (2–3), 707–716.
Palmer, C.D., Lewis, M.E., Geraghty, C.M., Barbosa, F., Parsons, P.J., 2006.Determination of lead, cadmium and mercury in blood for assessment ofenvironmental exposure: A comparison between inductively coupled plasma-mass spectrometry an atomic absorption spectrometry. Spectrochim. Acta PartB 61, 980–990.
Paoliello, M.M., De Capitani, E.M., 2005. Environmental contamination and humanexposure to lead in Brazil. Rev. Environ. Contam. Toxicol. 184, 59–96.
ARTICLE IN PRESS
F. Barbosa Jr. et al. / Environmental Research 109 (2009) 594–599 599
Paoliello, M.M., De Capitani, E.M., 2007. Occupational and environmental humanlead exposure in Brazil. Environ. Res. 103 (2), 288–297.
Paoliello, M.M., De Capitani, E.M., da Cunha, F.G., Matsuo, T., Carvalho Mde, F.,Sakuma, A., et al., 2002. Exposure of children to lead and cadmium from amining area of Brazil. Environ. Res. 88 (2), 120–128.
Park, S.K., Schwartz, J., Weisskopf, M., Sparrow, D., Vokonas, P.S., Wright, R.O.,et al., 2006. Low-level lead exposure, metabolic syndrome, and heart ratevariability: the VA Normative Aging Study. Environ. Health Perspect. 114 (11),1718–1724.
Pinheiro, M.C., Oikawa, T., Vieira, J.L., Gomes, M.S., Guimaraes, G.A., Crespo-Lopez,M.E., et al., 2006. Comparative study of human exposure to mercury inriverside communities in the Amazon region. Braz. J. Med. Biol. Res. 39 (3),411–414.
PNUE UNEP, 2006. Partnership for Clean Fuels and Vehicles. Nairobi, Kenya:-Available: /http://unep.org/pcfv/regions/LAC.aspS [accessed 28 juillet 2007].
Rojas, J.C., Vandecasteele, C., 2006. Influence of Mining Activities in the North ofPotosi, Bolivia on the Water Quality of the Chayanta River, and itsConsequences. Environ Monit Assess.
Romieu, I., 2003. [Use of blood lead data to evaluate and prevent child-hood lead poisoning in Latin America]. Salud Publica Mex 45 (Suppl. 2),S244–S251.
Romieu, I., Lacasana, M., McConnell, R., 1997. Lead exposure in Latin America andthe Caribbean. Lead Research Group of the Pan-American Health Organization.Environ Health Perspect 105 (4), 398–405.
Romieu, I., Weitzenfeld, H., Finkelman, J., 1990. Urban air pollution in LatinAmerica and the Caribbean: health perspectives. World Health Stat. Q 43 (3),153–167.
Rothenberg, S.J., Schnaas, L., Perroni, E., Hernandez, R.M., Ortega, J.F., 2000. Bloodlead secular trend in a cohort of children in Mexico City. II. 1990–1995. Arch.Environ. Health 55 (4), 245–249.
Santa Rosa, R., Muller, R.C., Alves, C.N., Sarkis, J.E., Bentes, M.H., Brabo, E., et al.,2000. Determination of total mercury in workers’ urine in gold shops ofItaituba, Para State, Brazil. Sci. Total Environ. 261 (1–3), 169–176.
Santos, E.C., Jesus, I.M., Brabo, E.S., Loureiro, E.C., Mascarenhas, A.F., Weirich, J., etal., 2000. Mercury exposures in riverside Amazon communities in Para, Brazil.Environ. Res. 84 (2), 100–107.
Schnaas, L., Rothenberg, S.J., Flores, M.F., Martinez, S., Hernandez, C., Osorio, E., etal., 2004. Blood lead secular trend in a cohort of children in Mexico City(1987–2002). Environ. Health Perspect. 112 (10), 1110–1115.
Schwartz, B.S., Hu, H., 2007. Adult lead exposure: time for change. Environ. HealthPerspect. 115 (3), 451–454.
Tellez-Rojo, M.M., Bellinger, D.C., Arroyo-Quiroz, C., Lamadrid-Figueroa, H.,Mercado-Garcia, A., Schnaas-Arrieta, L., et al., 2006. Longitudinal associationsbetween blood lead concentrations lower than 10 microg/dL and neurobeha-vioral development in environmentally exposed children in Mexico City.Pediatrics 118 (2), e323–e330.
Tellez-Rojo, M.M., Hernandez-Avila, M., Gonzalez-Cossio, T., Romieu, I., Aro, A.,Palazuelos, E., et al., 2002. Impact of breastfeeding on the mobilization of leadfrom bone. Am. J. Epidemiol. 155 (5), 420–428.
Woolley, D.E., 1984. A perspective of lead poisoning in antiquity and the present.Neurotoxicology 5 (3), 353–361.
Wright, R.O., Hawai, H., Silverman, E.K., Tsaih, S.W., Schwartz, J., Bellinger, D., et al.,2003. Apolipoprotein E genotype predicts 24-month bayley scales infantdevelopment score. Pediatr. Res. 54 (6), 819–825.