Elevated blood lead levels in a riverside population in the Brazilian Amazon

6
Elevated blood lead levels in a riverside population in the Brazilian Amazon $ Fernando Barbosa Jr. a, , Myriam Fillion b , Me ´ lanie Lemire b , Carlos Jose ´ Sousa Passos c , Jairo Lisboa Rodrigues a , Aline Philibert a , Jean-Re ´ my Guimara ˜es d , Donna Mergler b a Laborato ´rio de Toxicologia e Essencialidade de Metais, Departamento de Ana ´lises Clı ´nicas, Toxicolo ´gicas e Bromatolo ´gicas, Faculdade de Cie ˆncias Farmace ˆuticas de Ribeira ˜o Preto, Universidade de Sa ˜o Paulo, Avenida do cafe ´ S/N Monte Alegre 14040-903, Ribeira ˜o Preto-SP, Sa ˜o Paulo, Brazil b Centre de recherche interdisciplinaire sur la biologie, la sante´, la socie´te ´ et l’environnement (CINBIOSE), Universite´ du Que ´bec a ` Montre ´al, Montre ´al, Que ´bec, Canada c Faculdade UnB Planaltina, Universidade de Brası ´lia, Planaltina, DF, Brazil d Laborato ´rio de Trac - adores, Instituto de Biofı ´sica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil article info Article history: Received 14 August 2008 Received in revised form 7 March 2009 Accepted 23 March 2009 Available online 22 April 2009 Keywords: Lead Amazon Environmental exposure Blood lead Manioc abstract 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 Tapajo ´ s 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 13.1 mg/dL78.5, median B-Pb was 11.2 mg/dL and ranged from 0.59 to 48.3 mg/dL. Men had higher B-Pb compared to women (median: 15.3 mg/dL vs 7.9 mg/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 0.1970.10 mg/g). This was confirmed in one of these villages where we sampled manioc paste (just before roasting) and the roasted farinha (0.05 mg/g vs 0.20 mg/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 suffering from Pb toxicity throughout history, from the times of the Roman Empire, through the Middle Ages and the Industrial Revolution (Nriagu, 1983; Woolley, 1984). With the increasing industrializa- tion in the 19th century, scientific studies documented high levels of occupational exposure to Pb in workers, who presented symptoms of acute and chronic disease (Hernberg, 2000). Over the past three decades, studies focussing on low-level environ- mental exposures to Pb have shown its harmful effects on children’s neurodevelopment and behaviour, as well as its long- lasting effects on many target organs in both children and adults (Hernberg, 2000; Kosnett et al., 2007; Needleman, 2004). The Centers for the Disease Control and Prevention (CDC) of the United States established the screening action guideline in children at 10 mg/dL in whole blood, but there is increasing concern about the absence of a threshold at which deleterious effects occur (Barbosa et al., 2005; Bellinger, 2004; Lanphear et al., ARTICLE IN PRESS Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/envres Environmental Research 0013-9351/$ - see front matter & 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.envres.2009.03.005 $ Funding sources and ethical considerations: This study was supported by the Canadian Institutes of Health Research, the International Development Research Center and by Fundac - a ˜o de Apoio a Pesquisa do Estado de Sa ˜o Paulo (FAPESP). Ethical approvals were obtained at Universite ´ du Que ´bec a ` Montre ´ al (Canada) and at Universidade de Sa ˜o Paulo (Brazil). Corresponding author. Fax: +551636331936. E-mail address: [email protected] (F. Barbosa Jr.). Environmental Research 109 (2009) 594–599

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.,

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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.

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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.

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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

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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).

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