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Environmental Research 97 (2005) 209–219

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Hair mercury (signature of fish consumption) and cardiovascular riskin Munduruku and Kayabi Indians of Amazonia

Jose G. Dorea,a,� Jurandir R. de Souza,b Patricia Rodrigues,c Iris Ferrari,a andAntonio C. Barbosad

aFaculdade de Ciencias da Saude, Universidade de Brasılia, C.P. 04322, 70919-970 Brasılia, DF, BrazilbInstituto de Quımica, Universidade de Brasılia, Brasılia, Brazil

cFUNAI (Fundacao Nacional do Indio), Brasılia, BrazildIBAMA (Brazilian Environmental Agency), Brasılia, Brazil

Received 16 December 2003; received in revised form 9 April 2004; accepted 12 April 2004

Available online 17 June 2004

Abstract

Fish is an important natural resource in the diet of inhabitants of the Amazon rain forest and a marker of its consumption (hair

Hg) was used to compare selected cardiovascular risk parameters between tribes of Eastern Amazonia. Three Munduruku (Terra

Preta, Kaburua, Cururu) villages and one Kayabi village at the banks of head rivers (Tapajos, Tropas, Kabitutu, Cururu,

Curuzinho, Teles Pires) of the Tapajos Basin were studied in relation to fish Hg concentrations, mercury in hair (fish consumption)

and erythrocytes, body mass index (height/weight, kg/cm2), and blood pressure. The mean fish Hg concentrations were higher in

predatory (578.6 ng/g) than in nonpredatory species (52.8 ng/g). Overall only 26% of fish Hg concentrations were above 500 ng/g,

and only 11% were above 1000 ng/g. There was no systematic trend in fish Hg concentrations from rivers with a history of gold-

mining activities. The biomarker of fish consumption (hair Hg) was significantly associated with erythrocyte-Hg (r ¼ 0:5181;P ¼ 0:0001) and was significantly higher in Kayabi (12.7 mg/g) than in the Munduruku (3.4 mg/g). Biomarker-assessed fish

consumption rate was higher in the Kayabi (110 g/day) than in the Munduruku villages (30 g/day). Although no significant

differences in body mass index (BMI) were observed between tribes, there was a trend of lower increase in blood pressure with age

among the higher fish consumers (Kayabi). Summary clinical evaluation did not detect neurologic complaints compatible with Hg

intoxication (paraparesis, numbness, tremor, balancing failure), but endemic tropical diseases such as clinical history of malaria

showed a high prevalence (55.4%). Fish is an abundant natural resource, important in the Indian diet, that has been historically

consumed without perceived problems and can easily be traced through hair Hg. The exposure to freshwater fish monomethyl

mercury is less of an issue than endemic infectious diseases such as malaria and lack of basic medical services.

r 2004 Elsevier Inc. All rights reserved.

Keywords: Indians; Rio tapajos; Amazon; Mercury; Hair; Fish; Malaria

1. Introduction

Fish is a nutritious and important dietary staple of thepeople of the Amazonian rain forest. It is an abundantnatural resource that is rich in high-quality protein,lysine, iodine, sulfur-containing amino acids, copper,calcium, zinc, iron, manganese, selenium, and omega-3

e front matter r 2004 Elsevier Inc. All rights reserved.

vres.2004.04.007

ng author. Fax: +55-61-368-5853.

ss: dorea@rudah.com.br (J.G. Dorea).

polyunsaturated fatty acids, among others. In theAmazonian rain forest, fish supply much needed proteinand provide a balance to starchy food-staples such asyam, cassava, and plantain (Araujo et al., 1975). Fish ishigh in lysine in amounts comparable to milk protein(Batterham et al., 1979) and is an ideal complement tolysine-poor cereal grains. In cassava-based diets, fishconsumption is associated with high bioavailability ofiodine (Toure et al., 2001) and is positively correlatedwith the iodine status of women (Zollner et al., 2001). In

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tropical rain forests where soils and foods are iodinepoor, fish provide much need iodine. Moreover, fish is agood source of sulfur-containing amino acids. Bothsulfur and iodine may counteract goitrogens found incassava (Tor-Agbidye et al., 1999). Compared topowdered skim milk, small fish have fivefold more Cu,twofold higher Ca, and two orders of magnitudes moreZn, Fe, and Mn (Larsen et al., 2000). It is known thatzinc levels are significantly higher in protein-rich foodlike fish than in low-protein food (Terres et al., 2001).Fish is also known to enhance zinc (Garcia-Arias et al.,1993) and vegetable-iron absorption (Layrisse et al.,1968). Moreover, Amazonian fish is a good source ofselenium (Dorea et al., 1998), a nutritional elementknown to counteract the toxic effects of Hg. It wasrecently observed that S-containing amino acids in fishare central to detoxification of high concentrations ofneurotoxins in cassava (linamarin), the dominant sourceof energy for Amazonians (Dorea, 2004). Besides all oftheir nutritional uses, fish are used medicinally byinhabitants of the Amazon (Begossi et al., 2000).In addition to protein, minerals, and vitamins, fish

provide beneficial fats. Fish is an important source ofomega-3 polyunsaturated fatty acids (e.g., PUFA;decosahexanoic [22:6] acid (DHA), eicosapentaenoic[20:5] acid), which have been proven to play animportant role in the prevention of coronary heartdiseases (Albert et al., 2002). In adults reporting highfish intake, erythrocyte Hg (a biomarker of fish intake)and plasma PUFA were found in high levels and wereassociated with decreased risk of the occurrence of a firstmyocardial infarction (Hallgren et al., 2001). Fish andomega-3 PUFA were associated with reduced risk ofcardiovascular disease (Mizushima et al., 1997) andthrombotic infarction in women (Isso et al., 2001).Marckmann and Gronbaek (1999) concluded that fishconsumption of 40–60 g daily is associated with mark-edly reduced coronary heart disease mortality in high-risk populations. There is a lack of data on omega-3polyunsaturated fatty acids composition of freshwaterfish of the Amazon. According to Inhamuns and BuenoFranco (2001), omega-3 polyunsaturated fatty acidswere found in mapara (Hypophthalmus spp.). However,the beneficial effects of fish consumption on thecardiovascular system are not only due to the omega-3fatty acids but also to fish protein (Yahia et al., 2003).Despite all of the nutrients found in fish, the beneficial

aspects of fish consumption have been challengedbecause fish contains mercury, which is known toadversely affect the cardiovascular system (NRC,2000). Salonen et al. (1995) demonstrated a negativeassociation between Hg (derived from fish consumption)and the risk of acute myocardial infarction (AMI). Theadverse effects of Hg on the cardiovascular system mayoccur during prenatal exposure (Sorensen et al., 1999).Recently, Guallar et al. (2002) suggested that toenail Hg

was directly associated with the risk of AMI. They alsosuggested that high Hg content might diminish thecardioprotective effect of fish intake.Despite undisputable health benefits of fish consump-

tion, there are legitimate concerns regarding the inges-tion of monomethyl mercury (MMHg), which iscontained in certain types of large fish and seafood. Inthe Amazon environment, without industrial dischargesof preformed organic Hg, fish MMHg accumulationdepends on complex biochemical factors such as metalmethylation and MMHg acquisition by organisms in theaquatic food web. It is generally accepted that there is apredictive association between fish-feeding strategies,age/size within a particular species, and fish Hgconcentration. Preformed MMHg is well absorbed andcomplexed in proteinaceous matrices of aquatic animals.In humans, fish is the main source of MMHg. MMHglevels can be traced through Hg concentrations found inhair and blood. Indeed, within the same Amazonrainforest environment, riparians (Rio Madeira Basin)were demonstrated to consume more fish than indigen-ous people of Eastern Amazonia by virtue of havinghigher hair Hg concentrations (Barbosa et al., 1995).Milton (1991) studied the dietary ecology of indigen-

ous people of Eastern Amazonia (Rio Xingu Basin) andshowed that intergroup dietary differences appear torepresent a type of cultural character displacement.These dietary differences aid in distinguishing membersof one group from another. The dietary importance offishing varies among Indian groups and, for some, itmay be regarded as an activity of little value (Milton,1991). The Amondavans of Western Amazonia (Pavanet al., 1999) and the Yanomami of Venezuela (Holmes,1984) rarely eat fish, while the Munduruku (Sai Cinzavillage) are reported to consume fish three times a day(Brabo et al., 2000). Among the Makuxi (Roraima,Brazil, Northern Amazon), depending on the village,consumption is frequent to rare (Sing et al., 1996). Forsome indigenous populations, language, isolation, andcultural differences are formidable obstacles in obtain-ing dietary information (Milton, 1991; Sing et al., 1996).However, in Amerindians of French Guiana, it has beenpossible to estimate fish consumption (Frery et al.,2001).It is recognized that lifestyle choices affect the risk of

developing cardiovascular diseases (CVD). This isespecially true in populations with body-mass indices(BMI) that have been associated with all major CVDrisk factors (Lamon-Fava et al., 1996). Due to theisolation of native inhabitants of the Amazon forest,studies of CVD risk factors associated with diets andlifestyle have grown of interest of late. These studiesfocused on unacultured Yanomami Indians with a no-salt diet and showed a very low incidence of cardiovas-cular disease (Carneiro and Jardim, 1993). Also, littlevariation of BMI and blood pressure with age was found

ARTICLE IN PRESSJ.G. Dorea et al. / Environmental Research 97 (2005) 209–219 211

(Carvalho et al., 1989). Early work on the aculturedMunduruku (Rio Cururu), consumers of salt, showedthat they have low blood pressure and that it tends toincrease with age (Lowenstein, 1961).The Munduruku and Kayabi inhabit the Tapajos

Basin. Devoid of large cities and industrial activity, thesole source of mercury acquisition is through fish.However, some of the rivers used as fishing grounds(Tapajos, Teles Pires, Tropas) have had recent gold-mining activity.In our study on Eastern Amazon indigenous people,

we assessed the impact of environmental disruption(gold mining) on fish Hg and the putative role of fishconsumption on CVD risk factors. This was done byusing standard markers of Hg exposure in the biota (fishHg) and fish consumption (hair Hg).

2. Materials and methods

The study is part of the Projeto Integrado de Protecaoa Populacoes Indıgenas da Amazonia Legal–PPTAL(Project for Integration and Protection of AmazonianIndians) of the Deutsche Gesellschaft fur TechnischeZusammenarbeit–GTZ. The study was approved andauthorized by the FUNAI (Fundacao Nacional doIndio, the Brazilian Bureau of Indian Affairs). At eachvillage, the leader of the community gave his or herpermission after the purpose of the research wasexplained. The area occupied by the Munduruku andKayabi groups living in the south of Para is shown inthe map of Fig. 1. These villages lack water treatmentand basic medical services. They have minimal externalresources. In each village there is a pharmacy precar-iously maintained because of interrupted provision ofbasic medications. There is a radio communicationsystem connected to the nearest town with hospital andFUNAI headquarters for emergencies.In the Munduruku reservation we clinically examined

the villages of Terra Preta (site 1: Rio das Tropas),Kaburua (site 2: Rio Kabitutu), Missao Cururu (site 3:Rio Cururu). Only one village was sampled for theKayabi group (site 4: Kayabi village; Rio Teles Piresand Rio Cururuzinho). Six hundred twenty-one indivi-duals (men, women, and children) were clinicallyexamined by a trained physician (I.F.) with the aid ofa local interpreter. The examination was followed bybiotic measurements of height, weight, blood pressure,and heart rate. Blood pressure was measured with astandard sphygmomanometer by one of us (I.F.), withthe subject resting for 5min in a sitting position.Particular attention was paid to perceived neurologiccomplaints compatible with mercury intoxication (para-paresis, numbness, tremor, balancing failure), and majorhealth problems. Body mass index (BMI) was calculatedfrom the weight (kg) divided by height (m2). Samples of

hair and blood were taken at the time of the medicalexamination. Hair was cut from the occipital area, closeto the scalp with stainless steel scissors, bundled togetherwith cotton thread, and placed in a properly identifiedenvelope. Blood samples were taken by venipuncture(3mL) in Vacutainer tubes containing anticoagulant.The samples were stored in ice and taken to theLaboratory of Environmental Chemistry of the Uni-versity of Brasilia for analysis.Fish samples were collected by fishhook or net at

fishing areas used by the communities. The Indians ofthe Kaburua village more frequently use ichthyotoxicplants, locally known as ‘‘timbo.’’ The fish caught werephotographed for identification, weighed, and measuredfor total and standard length. After that, they were cutin pieces of circa 20 g, packed and labeled in plasticsacks, and stored in refrigerated boxes to be analyzed inthe Laboratory of Environmental Chemistry of theUniversity of Brasılia.Sample preparation and mercury determination were

done according to our laboratory routine as in previousstudies of fish (Barbosa et al., 1995) and hair matrices(Barbosa et al., 2001). Briefly, the hair samples werecomminuted with stainless steel scissors, weighed, anddigested before analysis. Fish samples were digestedwith concentrated HNO3 and H2SO4 using a microwavesystem DGT-100 (Provecto Sistemas Analıticos, SaoPaulo, Brazil) with potencies varying from 0 to 800W,for 20min. The determination of total Hg in sampleswas performed by cold vapor atomic absorptionspectrometry (CV-AAS). The instrument used was aModel 1255 mercury monitor LDC analytical (LDC,Riviera Beach, FL) connected to a HP Model 3435multimeter (Hewlett Packard, Palo Alto, CA) and aNeptune Dyna Pump (Magnetek Universal Electric). Allglassware used in the analytical protocol was washed,rinsed with KOH and double distilled water, and left torest in 50% HNO3 for 24 h. It was then rinsed again indouble distilled water and dried at 100 1C for 12 h. Theharvested erythrocytes were washed three times inphosphate buffer solution (pH 7.1) and treated withacid solutions according to our laboratory routine formercury determination in blood (Barbosa et al., 1995).Precision and accuracy of mercury determinations

were ensured by the use of internal standards of fishmuscle prepared in our laboratory and used in theMercury Quality Assurance Program for Fish (Cana-dian Food Inspection Agency, Winnipeg, Canada),and in the Hair Mercury-Interlaboratory ComparisonProgram, Ottawa, Canada, that started in 1992.Our performance was considered acceptable with94%o2SD (n ¼ 16) for fish and 86%o2SD (n ¼ 14)for hair.The rate of fish consumption for adults was estimated

based on assumptions and equations described byRichardson and Currie (1993). The assumptions are

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Fig. 1. Map locating Indian villages and respective fish sampling sites.

J.G. Dorea et al. / Environmental Research 97 (2005) 209–219212

that hair Hg is a linear function of rate of Hg ingestion(i.e., at steady state the hair Hg concentrations is a linearfunction of fish Hg), and the rate of fish consumption.The equation

Fish consumption rate ðg=dayÞ ¼ hair ½Hg�=ðfish ½Hg�n an bÞ:

ð1Þ

We used overall mean fish Hg concentration of396.1 ng/g (w.w.) and individual hair Hg concentrations.Values for a and b represent the ratio of steady state[Hg] and daily intake of Hg, and the ratio of hair Hg toblood-Hg, respectively. Richardson and Currie (1993)used values for a (0.0010) and b (292) after studies

described by WHO (1976) (cited by Richardson andCurrie, 1993) and Kershaw et al. (1980).Summarized data (mean, SD, and ranges), Pearson

correlation between variables, and analysis of variancewere performed using a SAS (SAS Institute, Cary, NC).Statistical analysis with a P value less than 0.05 wasconsidered statistically significant.

3. Results

The Hg concentrations in fish are presented in Table 1and illustrate differences in trophic levels and riversfished by the Indians. Piscivorous species showed the

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Table 1

Mean (SD) of fish total-Hg concentrations (ng/g) as a function of fish feeding rank

Sampling

sites/rivers

Predators (P) Nonpredators (N-P) Local names

n [Hg] n [Hg]

Kabitutu 6 199.6 (99.9) 4 28.0 (15.4) P=Agulha, jacunda, mandi, traıra. N-P=Piau, cara, matrinxa.

Cururu 7 196.5 (177.7) 62 51.6 (52.5) P=Piranha, tucunare, tucunare-pitanga. N-P=Matrinxa, Pacu

pintado, piau-aracu.

Cururuzinho 101 777.0 (667.0) 11 44.3 (63.8) P=Cachorra, jacunda, piranha branca, piranha preta, pintado,

tucunare pitanga, trairao. N-P=Acari bodo, pacu-acu, pacu prata,

matrinxa.

Tapajosa 20 324.0 (327.2) 11 103.0 (26.9) P=Piranha branca, pescada, tucunare-acu, bico-de-pato, surubim,

mandi. N-P=Jaraqui, matrinxa.

Teles Piresa 56 673.1 (563.9) 13 68.6 (44.9) P=Tucunare-acu, tucunare-pitanga, piranha preta, pintado, Piranha

branca, cachorra, trairao, filhote, jau, dourado cachorro, surubim,

bicuda, barbado. N-P=Pacu-acu, pacu prata, piau, piau-aracu,

jundia.

Tropasa 49 259.5 (240.8) 25 33.9 (25.1) P=Piranha branca, tucunare-acu, tucunare-pitanga, tucunare-paca,

charroqui cabeca-de-pedra, piranha preta, barbado. N-P=Aracu,

pacu, acari-bodo, jaraqui, piau.

Overall

mean

239 578.6 126 52.8

aRivers with history of gold-mining activities.

0 500 1000 1500 2000 2500 3000 3500 4000

0

25

50

75

100

Fish [Hg], ng/g

Dis

tribu

tion,

%

Fig. 2. Percentage distribution of fish Hg concentrations for all

sampling sites.

Table 2

Mean (and SD) hair mercury concentrations and fish consumption

rates of Amerindian adults of Eastern Amazon

Tribe/

villages

n [Hg, mg/g] Fish consumption

(g/day)a

Munduruku

Kaburua 89 2.5 (1.4) 22.1 (12.2)

Cururu 138 3.7 (1.6) 32.0 (13.9)

Terra Preta 22 6.0 (2.9) 51.7 (25.1)

Total 249 3.4 (1.9) 30.0 (16.6)

Kayabi

Kayabi 47 12.8 (7.0) 110.4 (60.6)

aEstimated according to Richardson and Currie (1993).

J.G. Dorea et al. / Environmental Research 97 (2005) 209–219 213

highest Hg concentrations. The range of means of fishHg concentrations in piscivorous (196–777 ng/g) speciesfrom rivers not impacted by gold mining (Kabitutu,Cururu, and Curuzinho rivers) was comparable to therange (259–673 ng/g) seen for impacted rivers (Tapajos,Teles Pires, Tropas). Distribution of Hg in all fishsamples is illustrated in Fig. 2. Overall, most samples(74%) were below 500 ng/g and only 11% were above1000 ng/g. The chosen fishing ground at the RioKabitutu produced only 10 samples as a result ofoverfishing with ichthiotoxic ‘‘timbo.’’Hair Hg concentrations and fish consumption rate are

shown in Table 2. There was a statistically significantdifference (Po 0:0001) in the gradient of fish consump-tion (hair Hg) among the villages. The Kayabi showedthe highest hair Hg concentrations. Assessment of fishconsumption rate showed a marked difference betweenMunduruku and Kayabi. The Munduruku villages(Kaburua, Cururu, Terra Preta) had a fish consumptionrate of 22.10, 31.96, 51.67 g/day, respectively. Differ-ences in mean consumption rate were statisticallysignificant (Po 0:0001). Hair Hg was significantlycorrelated with erythrocyte (r ¼ 0:5181; P ¼ 0:0001) inadult Kayabi (Fig. 3). In this group of Indians, the EryHg concentrations ranged from 0.3 to 251.4 ng Hg/gEry. A summary of comparative aspects related tofish consumption rate, hair Hg, and fish Hg concentra-tions of natives of the Amazon rain forest is shown inTable 3.During clinical examination there were no complaints

or signs compatible with Hg intoxication (paraparesis,

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numbness, tremor, balancing failure). However, lack ofmedical services was perceived as their major healthconcern. Malaria is endemic in the Amazon rain forestand both tribes showed high incidence (55.4%) ofclinical history of malaria. Multiple episodes of malariawere registered varying from 1 to >10.Although no significant differences in BMI were seen

between Indian groups (Fig. 4), there were salientfeatures in trends related to blood pressure and fish

Table 3

Fish consumption and hair-Hg concentrations in adult Amerindians of the A

Tribe Hair-Hg Fishing waters

Basin Gold mining

Munduruku 3.4 Tapajos Yes

Munduruku 3.4 Tapajos Yes

Kayabi 12.7 Tapajos No

Wari (1.4–11.7) Madeira Yes

Wayana 12.7 Maroni Yes

Wayampi 6.7 Oyapock NG

Galibi 2.8 Awala NG

Wayana 11.4a Maroni Yes

Suia 10.0 Xingu No

Uaura 12.6 Xingu No

Krem-Akrore 8.7 Xingu No

Coicuro 13.2 Xingu No

Matipu 10.6 Xingu No

Pavuru 20.6 Xingu No

Juruna 16.5 Xingu No

Kayabi 12.2 Xingu No

Munduruku 15.7 Tapajos Yes

Wayana 11.7 Maroni No

Kayapo 8.11 Xingu No

Kayapo 8.0 Madeira Yes

Yanomami 3.6 NG NG

Yanomami 1.0 Ocamo NG

Note: Range in parentheses; NG, not given.aGeometric mean.bSub-sample of Barbosa et al. (1995).

0 50 100 150 200 2500

10

20

30

40

50

Erythrocyte [Hg], ng/g

Hai

r [H

g],

µg/g

Fig. 3. Correlation between mercury in hair and in erythrocytes of

adult Kayabi Indians.

consumption. Parameters related to cardiovascular riskare illustrated in Figs. 5 and 6. Hair Hg per se was notsignificantly related to blood pressure all ages consid-ered. However, as a function of age, adult individuals ofthe Munduruku group had a tendency towardhigher blood pressure (systolic: r2 ¼ 0:044, P ¼ 0:0017;

mazon rain forest

Fish consumption rate Reference

30 g/d This study

30 g/day This study

110 g/day This study

NG Campos et al. (2002)

NG Cordier et al. (2002)

NG Cordier et al. (2002

NG Cordier et al. (2002

282 g/day Frery et al. (2001)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

NG Vasconcellos et al. (2000)

3 times/day Brabo et al. (2000), Santos et al. (1998)

6.5 times/week Cordier et al. (1998)

NG Barbosa et al. (1998)b

NG Barbosa et al. (1995)

NG Castro et al. (1991)

NG Hecker et al. (1974)

Fig. 4. Body mass index (body weight/height) of Munduruku

(Kaburua, Cururu, and Terra Preta villages) and Kayabi Indians.

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0 5 10 15 20 25 30 3550

100

150

200

Hair-Hg, µg/h

Hair-Hg, µg/h

Sys

tolic

pre

ssur

e, m

mH

g

0 5 10 15 20 25 30 350

50

100

150

200

Munduruku

Kayabi

Munduruku

Kayabi

Dia

stol

ic p

ress

ure,

mm

Hg

Fig. 6. Scatter plots of blood pressure as a function of hair Hg

concentrations in Munduruku and Kayabi.

15 25 35 45 55 65 75 8550

100

150

200

Kayabi

Munduruku

Kayabi

Munduruku

Age, years

Age, years

Sys

tolic

pre

ssur

e, m

mH

g

15 25 35 45 55 65 75 850

50

100

150

200

Dia

stol

ic p

ress

ure,

mm

Hg

Fig. 5. Scatter plots of blood pressure as a function of age in

Mundurukus (systolic, r2: 0.008, P: 0.3368; diastolic, r2: 0.0002, P:

0.8234) and Kayabi (systolic, r2: 0.025, P: 0.2841; diastolic, r2: 0.001,

P: 0.799).

J.G. Dorea et al. / Environmental Research 97 (2005) 209–219 215

diastolic: r2 ¼ 0:158, Po 0:001), which was not shownfor the Kayabi (systolic: r2 ¼ 0:014, P ¼ 0:4268; diasto-lic: r2 ¼ 0:086, P ¼ 0:045).

4. Discussion

In the Curuzinho (Kayabi fishing area) and Curururivers, there is no history of gold mining. Yet, the fishHg concentrations are comparable to other samplingsites with a history of intense gold-mining activity (RioTeles Pires, Rio das Tropas, Rio Tapajos). Overall,mean fish Hg concentrations are consistent withpreviously reported values for the Tapajos Basin(Barbosa et al., 2003). Part of this observed variationcould be due to the random nature of opportunityfishing. Indeed, in fish catches, not only did sample sizediffer among rivers, but also among species composition(Table 1). The distinction between piranha species S.

rhombeus and S. eigenamanni may be due to size (age)differences. We showed that differences in Hg concen-trations in piranhas of the Rio Negro were due to size(age) variations rather than to physiological traits of thespecies (Dorea et al., in press). Earlier researchersbelieved that mercury contamination of the biotaoccurred because of mining activities on some headrivers of the Tapajos Basin. Recent work in the RioNegro, an area with no history of gold-mining activities,demonstrated that fish Hg concentrations were thehighest among those reviewed (Barbosa et al., 2003).Furthermore, its fish-eating population (‘‘ribeirinhos’’)has the highest hair Hg concentrations (Dorea et al.,2003). Therefore, exposure from gold amalgamation innative Amazonians may be overestimated by otherresearchers.In fish, mercury acquisition and retention are not well

understood. It is known that fish MMHg bioaccumula-tion is dependent on aquatic food-chain structure andlength. Additionally, within a food trophic category, fishspecies present a variety of feeding strategies thatdifferentially influence MMHg acquisition. In short,plankton, at the bottom of the food chain, is consumedby zooplankton (primary consumers) and then by smallforage fishes (secondary consumers), which, in turn, areconsumed by piscivorous fish (tertiary consumers) wherehigh MMHg concentrations are expected (Nichols et al.,1999). Especially in these species, the older (or larger)the fish, the higher the Hg concentration. In the complexAmazonian ecosystem, little is known about mercury-trophic transport through the food chain. Studies onthis topic require knowledge of fish species diversity andenvironmental interactions. This area of study is furthercomplicated by the need to understand hydrologicalcycle and to have knowledge of recent human activitiessuch as agriculture and deforestation by fire. Fadini andJardim (2001) showed that, in the Amazon Basin waters,Hg is mainly released via nature. In the lower Tapajoshead rivers, early assumptions that gold-mining activityleads to Hg pollution and that this affected fish Hgconcentration gradients (Uryu et al., 2001) have notbeen confirmed. Indeed, predatory fish species in the Rio

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Cururuzinho, where there has been no gold-miningactivity, had the highest fish Hg concentrations observed(Table 1). Furthermore, there is no indication of anysystematic association of fish Hg concentrations withalluvial gold mining in the Amazon rain forest (Barbosaet al., 2003). These results concur with recent work inthe Rio Negro Basin, an area with no history of gold-mining activity (Barbosa et al., 2003).Hair Hg concentrations indicate varying levels of fish

consumption among villages. The range of mean hairHg agrees with previous studies (Table 3) on Indiansfrom Eastern (Castro et al., 1991 cited by Lodenius andMalm, 1998; Campos et al., 2002) and WesternAmazonia (Vasconcellos et al., 2000). Our earlier workin the Rio Xingu (Barbosa et al., 1995) showed that hairHg was higher in fish-eating ribeirinhos than in gold-mining workers who were occupationally exposed toHg. In people of the same forest environment, but withdifferent dietary habits, we also showed that ribeirinhos

had higher hair Hg than Kayapo Indians (Barbosa et al.,1998). Cultural differences in data summarized byGragson (1992) showed that in Kuikuru, 4–17% ofdietary protein came from fish while in Uanano, up to85% came from fish.Estimated fish consumption for the Kayabi is half of

that reported for the Wayana (Frery et al., 2001).However, hair Hg (a fish consumption signature) indi-cated that the Kayabi had hair Hg (12.4 mg/g) compar-able to that of the Wayana (11.4 mg/g) (Table 3). Thisdiscrepancy can be explained by methodological differ-ences in food intake assessment. Estimation of fishconsumption through dietary methods is susceptible tounder- and overestimation. The recall method wasfound to overestimate fish consumption by 30% whencompared to test weighing (Yokoo et al., 2001).Assumptions made on fish consumption through bio-marker-based methods can also present shortcomings.Nevertheless, this method has the advantage of allowingaccurate individual measurements, thereby strengthen-ing statistical analysis. This biomarker method proveduseful in categorizing individuals, villages, and groupsinto fish intake levels. This permitted us to makecorrelations between fish intake and clinical andbiochemical outcomes. In fact, we found a strongcorrelation between hair Hg and erythrocyte Hg andcould detect trends in blood pressure measurements.In these indigenous peoples, traditional practices

remain. Thus, health characteristics that are associatedwith BMI and cardiovascular parameters have beenpreserved. Though analysis of a single parameter islimiting, we chose to examine fish consumption rate anddiscovered a distinct pattern among these groups. Also,gathering food consumption data in native Amazonianpopulations is a rather complex task (Milton, 1991).This is due not only to difficulties imposed by culturaldifferences, but also to methodological problems in-

herent to food data collection. Despite these challengingconditions, the use of a biomarker rendered theestimates of fish consumption less uncertain for statis-tical analysis.The Munduruku consumed less fish than the Kayabis,

but adult BMI was similar within genders and betweenvillages. Values ranged between 22 and 26 kg/cm2.Therefore, the significant difference in fish consumptionwas compared to blood pressure data. Although nosignificant correlation between blood pressure para-meters and hair Hg was seen, the Kayabi were shown tobe less susceptible to age-related increases in bloodpressure. These results support the hypothesis that fishconsumption is beneficial since it affects factors that areknown to play a role in coronary-artery diseaseprevention (Figs. 2–4). Blood pressure studies amongAmazonian Indians were revised by Fleming-Moranand Coimbra Jr. (1990). Due to the complexity of suchstudies in isolated communities, blood pressure data aredifficult to interpret. Furthermore, recognizable factorsin lifestyle due to rapid culture changes were notconsidered here.The health implications of any diet are determined by

the balance between essential nutrients and toxicsubstances that are naturally present in the foodconsumed. In the traditional diet of Amerindians,cassava (Manhitot esculenta Crantz) is the main sourceof carbohydrates (Milton, 1991) and, in many cases, fishis an important source of animal protein. These twofoods carry toxic substances, such as linamarin (natu-rally present in cassava) and MMHg (naturally acquiredand retained in fish flesh), which caused neurotoxicdiseases in Minamata (Japan) but not in Amazonia(Dorea, 2003). Neurotoxic cases of food origin are rarein Amazonia. Those few reported cases were due tothiamin deficiency (Vieira Filho et al., 1997). The largestneuropathy epidemic outbreak in the 20th centuryoccurred in Cuba and is currently suspected to be ofnutritional origin, with riboflavin and carotenoidmetabolism to be central in the etiological process(Barnouin et al., 2001). There is evidence of fishingvillages in Amazon dating back eight millennia (Roo-sevelt et al., 1991). In Brazilian times, there are no casesof required medical attention due to health problemscaused by fish consumption. Regarding neurobehavioralchanges, the special fishing skills of some Amazoniannative people do not support the existence of acompromising problem. Some Amazonian tribes fishwith bow and arrow in turbid waters where they have toremain still for hours, apparently demonstrating goodperipheral vision and outstanding motor coordination.Nevertheless, in recent Amazonian environmental stu-dies, fish is frequently depicted as a toxic risk and rarelyas a health asset.The importance of weighing the risks and benefits of

fish consumption for indigenous populations was called

ARTICLE IN PRESSJ.G. Dorea et al. / Environmental Research 97 (2005) 209–219 217

to attention by Egeland and Middaugh (1997). Clarkson(1995) casts doubt on the use of advised safe upper limitsto consuming naturally bioaccumulated MMHg in fish.However, neurological symptoms seen in children ofpoisoned (pesticide Hg) Iraqi mothers (hair Hg con-centrations as low as 20 ppm) were absent in ocean fisheaters of Peru (hair Hg between 1.2 and 30 ppm) whosehair Hg levels are comparable. Marsh et al. (1995)attributed these differences to the presence of protectivenutrients in the fish diet of Peruvian mothers and to theabsence of these protective nutrients in the Hg-poisonedgrain consumed by Iraqi mothers. It is worth mention-ing that a benchmark dose (BMD) of hair Hg may rangebetween 11 and 22 mg/g, depending on the advisorycommittee and data used (Dourson et al., 2001). ABMD value of 11 mg/g was based on toxocokinetic datafrom seafood eaters (mainly pilot whale) from the FaroeIslands. A higher benchmark value (21 mg/g) wasdetermined for ocean fish eaters of the SeychellesIslands. In this population recent data do not supportthe hypothesis that there is a neurodevelopmentalrisk from prenatal MeHg exposure resulting solelyfrom ocean fish consumption (Myers et al., 2003).Curiously, variables in environmental toxicology indi-cate not only that mercury is higher in seafood than infreshwater fish (Clarkson, 1998), but also that seafoodcontains higher concentrations of other neurotoxicsubstances such as organochlorine pollutants andarsenic (Gebel, 2000).An emerging body of research is unveiling immuno-

toxic interactions between mercury and tropical dis-eases, such as malaria (Crompton et al., 2002; Silbergeldet al., 2000, 2002) and leishmaniasis (Bagenstose et al.,2001). Experimental (Silbergeld et al., 2000) and fieldresearch (Crompton et al., 2002; Silbergeld et al., 2002)suggests that mercury exposure may play a role in theprevalence of malaria infection.

5. Conclusions

In spite of substantial amounts of metallic Hgreleased due to gold-mining activity, there is no evidencethat this Hg has impacted fish Hg in the head tributariesof Rio Tapajos. Fish consumption is the only source ofMMHg exposure for native people who do not haveaccess to commodity foods. For these people, to reducedietary MMHg means reducing the consumption of fish,a dietary staple and a source of many importantnutrients. No evidence exists that shows that freshwaterAmazonian fish cause neuropathies. As an abundantnatural resource, fish has been consumed for generationsin large amounts by Amazonian people without anyperceived problems. For these people, exposure to fishMMHg from the forest environment (nonindustrial

sources) is less of an issue than endemic infectiousdiseases such as malaria.

Acknowledgments

We thank the Fundacao Nacional do Indio–FUNAI,Deutsche Gesellschaft fur Technische Zusammenar-beit–GTZ, Projeto Integrado de Protecao a PopulacoesIndıgenas da Amazonia Legal–PPTAL, and the Mun-duruku and Kayabi populations for participation inthis study.

References

Albert, C.M., Campos, H., Stampfer, M.J., Ridker, P.M., Manson,

J.E., Willett, W.C., Ma, J., 2002. Blood levels of long-chain n-3

fatty acids and the risk of sudden death. N. Engl. J. Med. 11 (346),

1113–1118.

Araujo, T.M., Lago, E.S., Bion, F.M., Nascimento, J.S., Costa, L.P.,

Antunes, N.L., Chaves, N., Mello, A.V., 1975. Biological value of

manihot flour enriched with fish flour and soybean isolated protein,

and casein. Rev. Bras. Pesqui. Med. Biol. 8, 139–142.

Bagenstose, L.M., Mentink-Kane, M.M., Brittingham, A., Mosser,

D.M., Monestier, M., 2001. Mercury enhances susceptibility to

murine leishmaniasis. Parasite Immunol. 23, 633–640.

Batterham, E.S., Murison, R.D., Lewis, C.E., 1979. Availability of

lysine in protein concentrates as determined by the slope-ratio

assay with growing pigs and rats and by chemical techniques. Br.

J. Nutr. 41, 383–391.

Barbosa, A.C., Dorea, J.G., 1998. Indices of mercury contamination

during breast feeding in the Amazon Basin. Environ. Toxicol.

Pharmacol. 6, 71–79.

Barbosa, A.C., Boischio, A.A., East, G.A., Ferrari, I., Goncalves, A.,

Silva, P.R.M., Cruz, T.M.E., 1995. Mercury contamination in the

Brazilian Amazon. Environmental and occupational aspects.

Water Air Soil Pollut. 80, 109–121.

Barbosa, A.C., Silva, S.R.L., Dorea, J.G., 1998. Concentration

of mercury in hair of indigenous mothers and infants from

the Amazon Basin. Arch. Environ. Contam. Toxicol. 34,

100–105.

Barbosa, A.C., Jardim, W.F., Dorea, J.G., Fosberg, B., Souza, J.R.,

2001. Hair mercury speciation as a function of gender, age, and

body mass index in inhabitants of the Negro River Basin, Brazil.

Arch. Environ. Contam. Toxicol. 40, 435–444.

Barbosa, A.C., Souza, J., Dorea, J.G., Jardim, W.F., Fadini, P.S.,

2003. Mercury biomagnification in a tropical black water,

Rio Negro, Brazil. Arch. Environ. Contam. Toxicol. 45,

235–246.

Barnouin, J., Verdura, Barrios, T., Chassagne, M., Perez Cristia, R.,

Arnaud, J., Fleites Mestre, P., Montoya, M.E., Favier, A., 2001.

Nutritional and food protection against epidemic emerging

neuropathy. Epidemiological findings in the unique disease-free

urban area of Cuba. Int. J. Vitam. Nutr. Res. 71, 274–285.

Begossi, A., Hanazaki, N., Peroni, N., 2000. Knowledge and use of

biodiversity in Brazilian hot spots. Environ. Dev. Sustain. 2,

177–193.

Brabo, E.S., Santos, E.D., de Jesus, I.M., Mascarenhas, A.F.S., Faial,

K.D., 2000. Mercury contamination of fish and exposures of an

indigenous community in Para State, Brazil. Environ. Res. 84,

197–203.

Campos, M.S., Sarkis, J.E.S., Muller, R.C.S., Brabo, E.D., Santos,

E.D., 2002. Correlation between mercury and selenium concentrations

ARTICLE IN PRESSJ.G. Dorea et al. / Environmental Research 97 (2005) 209–219218

in Indian hair from Rondonia State, Amazon region, Brazil. Sci.

Total Environ. 287, 155–161.

Carneiro, O., Jardim, P.C., 1993. Blood pressure in a Xavante tribe.

Comparison after 15 years. Arq. Bras. Cardiol. 61, 279–282.

Carvalho, J.J., Baruzzi, R.G., Howard, P.F., Poulter, N., Alpers,

M.P., Franco, L.J., Marcopito, L.F., Spooner, V.J., Dyer, A.R.,

Elliott, P., et al., 1989. Blood pressure in four remote populations

in the INTERSALT study. Hypertension 14, 238–246.

Castro, M.B., Albert, B., Pfeiffer, W.C., 1991. Mercury levels in

Yanomami Indians hair from Roraima, Brazil. In: Proceedings of

the Eighth International Conference on Heavy Metals in the

Environment, vol. 1, pp. 367–370.

Clarkson, T.W., 1995. Environmental contaminants in the food chain.

Am. J. Clin. Nutr. 61, 682S–686S.

Clarkson, T.W., 1998. Human toxicology of mercury. J. Trace

Elements Exp. Med. 11, 303–317.

Cordier, S., Grasmick, C., Paquier-Passelaigue, M., Mandereau, L.,

Weber, J.P., Jouan, M., 1998. Mercury exposure in French Guiana:

levels and determinants. Arch. Environ. Health 53, 299–303.

Cordier, S., Garel, M., Mandereau, L., Morcel, H., Doineau, P.,

Gosme-Seguret, S., Josse, D., White, R., Amiel-Tison, C., 2002.

Neurodevelopmental investigations among methylmercury-ex-

posed children in French Guiana. Environ. Res. 89, 1–11.

Crompton, P., Ventura, A.M., de Souza, J.M., Santos, E., Strickland,

G.T., Silbergeld, E., 2002. Assessment of mercury exposure and

malaria in a Brazilian Amazon riverine community. Environ. Res.

90, 69–75.

Dorea, J.G., 2003. Fish are central in the diet of the Amazonian

riparians: should we worry about their mercury concentrations?.

Environ. Res. 92, 232–244.

Dorea, J.G., 2004. Cassava cyanogens and fish mercury are high but

safely consumed in the diet of native Amazonians. Ecotoxicol.

Environ. Saf. 57, 248–256.

Dorea, J.G., Moreira, M.B., East, G., Barbosa, A.C., 1998. Selenium

and mercury concentrations in some fish species of the Madeira

River, Amazon Basin, Brazil. Biol. Trace Elements Res. 65,

211–220.

Dorea, J.G., Barbosa, A.C., Ferrari, I., Souza, J.R., 2003. Mercury in

hair and in fish consumed by riparian women of the Rio Negro,

Amazon, Brazil. Int. J. Environ. Health Res. 13, 239–248.

Dorea, J.G., Barbosa, A.C., Souza, J., Fadini, P., Jardim, W.F., in

press. Piranhas (Serrasalmus spp) as markers of mercury biomag-

nification in the Amazonian ecosystem. Ecotox. Env. Saf.

doi:10.1016/j.ecoenv.2003.07.012.

Dourson, M.L., Wullenweber, A.E., Poirier, K.A., 2001. Uncertainties

in the reference dose for methylmercury. NeuroToxicology 22,

677–689.

Egeland, G.M., Middaugh, J.P., 1997. Balancing fish consumption

benefits with mercury exposure. Science 278, 1904–1905.

Fadini, P.S., Jardim, W.F., 2001. Is the Negro River Basin (Amazon)

impacted by naturally occurring mercury?. Sci. Total Environ. 275,

71–82.

Fleming-Moran, M., Coimbra Jr., C.E., 1990. Blood pressure studies

among Amazonian native populations: a review from an epide-

miological perspective. Soc. Sci. Med. 31, 593–601.

Frery, N., Maury-Brachet, R., Maillot, E., Deheeger, M., de Merona,

B., Boudou, A., 2001. Gold-mining activities and mercury

contamination of native Amerindian communities in French

Guiana: key role of fish in dietary uptake. Environ. Health

Perspect. 109, 449–456.

Garcia-Arias, M.T., Castrillon, A.M., Navarro, M.P., 1993. Bioavail-

ability of zinc in rats fed on tuna as a protein source in the diet.

J. Trace Elements Electrol. Health Dis. 7, 29–36.

Gebel, T., 2000. Confounding variables in the environmental

toxicology of arsenic. Toxicology 144, 155–162.

Gragson, T.L., 1992. Fishing the waters of Amazonia: native

subsistence economies in a tropical rain forest. Am. Anthropol.

94, 428–440.

Guallar, E., Sanz-Gallardo, M.I., van’t Veer, P., Bode, P., Aro, A.,

Gomez-Aracena, J., Kark, J.D., Riemersma, R.A., Martin-

Moreno, J.M., Kok, F.J., 2002. Heavy metals and myocardial

infarction study group: mercury, fish oils, and the risk of

myocardial infarction. N. Engl. J. Med. 347, 1747–1754.

Hallgren, C.G., Hallmans, G., Jansson, J.H., Marklund, S.L.,

Huhtasaari, F., Schutz, A., Stromberg, U., Vessby, B., Skerfving,

S., 2001. Markers of high fish intake are associated with decreased

risk of a first myocardial infarction. Br. J. Nutr. 86, 397–404.

Hecker, L.H., Allen, H.E., Dinman, B.D., 1974. Heavy metal levels in

acculturated and unacculturated populations. Arch. Environ.

Health 29, 181–185.

Holmes, R., 1984. Non-dietary modifiers of nutritional status in

tropical forest populations of Venezuela. Interciencia 9, 386–391.

Inhamuns, A.J., Bueno Franco, M.R., 2001. Composition of total,

neutral and phospholipids in mapara (Hypophtalmus sp.) from the

Brazilian Amazonian area. J. Agric. Food Chem. 49, 4859–4863.

Isso, H., Rexrode, K.M., Stampfer, M.J., Manson, J.E., Colditz, G.A.,

Speizer, F.E., Hennekens, C.H., Willett, W.C., 2001. Intake of fish

and omega-3 fatty acids and risk of stroke in women. J. Am. Med.

Assoc. 285, 304–312.

Kershaw, T.G., Clarkson, T.W., Dhahir, P.H., 1980. Interrelationships

of blood and hair mercury concentrations in a North American

population exposed to methylmercury. Arch. Environ. Health 35,

161–168.

Lamon-Fava, S., Wilson, P.W., Schaefer, E.J., 1996. Impact of body

mass index on coronary heart disease risk factors in men and

women. The Framingham Offspring Study. Arterioscler. Thromb.

Vasc. Biol. 16, 1509–1515.

Larsen, T., Thilsted, S.H., Kongsbak, K., Hansen, M., 2000. Whole

small fish as a rich calcium source. Br. J. Nutr. 83, 191–196.

Layrisse, M., Martinez-Torres, C., Roche, M., 1968. Effect of

interaction of various foods on iron absorption. Am. J. Clin.

Nutr. 21, 1175–1183.

Lodenius, M., Malm, O., 1998. Mercury in the Amazon. Rev. Environ.

Contam. Toxicol. 157, 25–52.

Lowenstein, F.W., 1961. Blood pressure in relation to age in the

tropics and subtropics. A preview of literature and an investigation

in two tribes of Brazil Indians. Lancet 1, 389–392.

Marckmann, P., Gronbaek, M., 1999. Fish consumption and coronary

heart disease mortality. A systematic review of prospective cohort

studies. Eur. J. Clin. Nutr. 53, 585–590.

Marsh, D.O., Turner, M.D., Smith, J.C., Allen, P., Richdale, N., 1995.

Fetal methylmercury study in a Peruvian fish-eating population.

Neurotoxicology 16, 717–726.

Milton, K., 1991. Comparative aspects of diet in Amazonian forest-

dwellers. Philos. Trans. R. Soc. London B: Biol. Sci. 334, 253–263.

Mizushima, S., Moriguchi, E.H., Ishikawa, P., Hekman, P., Nara, Y.,

Mimura, G., Moriguchi, Y., Yamori, Y., 1997. Fish intake and

cardiovascular risk among middle-aged Japanese in Japan and

Brazil. J. Cardiovasc. Risk 4, 191–199.

Myers, G.J., Davidson, P.W., Cox, C., Shamlaye, C.F., Palumbo, D.,

Cernichiari, E., Sloane-Reeves, J., Wilding, G.E., Kost, J., Huang,

L.S., Clarkson, T.W., 2003. Prenatal methylmercury exposure from

ocean fish consumption in the Seychelles child development study.

Lancet 17, 1686–1692.

National Research Council, 2000. Toxicological Effects of Methyl-

mercury. National Academy Press, Washington, DC pp. 1–344.

Nichols, J., Bradbury, S., Swartout, J., 1999. Derivation of wildlife

values for mercury. J. Toxicol. Environ. Health B: Crit. Rev. 2,

325–355.

Pavan, L., Casiglia, E., Braga, L.M., Winnicki, M., Puato, M.,

Pauletto, P., Pessina, A.C., 1999. Effects of a traditional lifestyle on

ARTICLE IN PRESSJ.G. Dorea et al. / Environmental Research 97 (2005) 209–219 219

the cardiovascular risk profile: the Amondava population of the

Brazilian Amazon. Comparison with matched African, Italian and

Polish populations. J. Hypertens. 17, 749–756.

Richardson, G.M., Currie, D.J., 1993. Estimating fish consumption

rates for Ontario Amerindians. J. Exp. Anal. Environ. Epidem. 3,

23–37.

Roosevelt, A.C., Housley, R.A., Dasilveira, M.I., Maranca, S.,

Jonson, R., 1991. 8th millennium pottery from a prehistoric

shell midden in the Brazilian Amazon. Science 254 (5038),

1621–1624.

Salonen, J.T., Seppanen, K., Nyyssonen, K., Korpela, H., Kauhanen,

J., Kantola, M., Tuomilehto, J., Esterbauer, H., Tatzber, F.,

Salonen, R., 1995. Intake of mercury from fish, lipid peroxidation,

and the risk of myocardial infarction and coronary, cardiovascular,

and any death in eastern Finnish men. Circulation 9, 645–655.

Santos, E.C.O., Jesus, I.M., Brabo, E.S., Loureiro, E.C.B., Weirich,

J., Mascarenhas, A.F.S., 1998. Nıveis de Hg em tecido capilar

na comunidade de indıgena de Sai-Cinza, reserva

Munduruku, Jacareacanga-Para. Rev. Soc. Bras. Med. Trop. 31,

40 (abstract).

Silbergeld, E.K., Sacci Jr., J.B., Azad, A.F., 2000. Mercury

exposure and murine response to Plasmodium yoelii infection and

immunization. Immunopharmacol. Immunotoxicol. 22 (4),

685–695.

Silbergeld, E.K., Nash, D., Trevant, C., Strickland, G.T., de Souza,

J.M., da Silva, R.S., 2002. Mercury exposure and malaria

prevalence among gold miners in Para, Brazil. Rev. Soc. Bras.

Med. Trop. 35, 421–429.

Sing, K.A., Hryhorczuk, D.O., Saffirio, G., Sinks, T., Paschal, D.C.,

Chen, E.H., 1996. Environmental exposure to organic mercury

among the Makuxi in the Amazon Basin. Int. J. Occup. Environ.

Health 2, 165–171.

Sorensen, N., Murata, K., Budtz-Jorgensen, E., Weihe, P.,

Grandjean, P., 1999. Prenatal methylmercury exposure as a

cardiovascular risk factor at seven years of age. Epidemiology 10,

370–375.

Terres, C., Navarro, M., Martin-Lagos, F., Gimenez, R., Lopez, H.,

Lopez, M.C., 2001. Zinc levels in foods from Southeastern Spain:

relationship to daily dietary intake. Food Addit. Contam. 18,

687–695.

Tor-Agbidye, J., Palmer, V.S., Lasarev, M.R., Craig, A.M., Blythe,

L.L., Sabri, M.I., Spencer, P.S., 1999. Bioactivation of cyanide

to cyanate in sulfur amino acid deficiency: relevance to neurolo-

gical disease in humans subsisting on cassava. Toxicol. Sci. 50,

228–235.

Toure, F., stoecker, B.J., Lucas, E., 2001. Fish and shrimp provided

bioavailable iodine for rats fed cassava/millet-based diets. FASEB

J. (abstract).

Uryu, Y., Malm, O., Thornton, I., Payne, I., Cleary, D., 2001.

Mercury contamination of fish and its implications for other

wildlife of the Tapajos Basin, Brazilian Amazon. Conserv. Biol. 15,

438–446.

Vieira Filho, J.P., Oliveira, A.S., da Silva, M.R., Amaral, A.L.,

Schultz, R.R., 1997. Polyneuropathy deficiency among Xavante

Indians. Rev. Assoc. Med. Bras. 43, 82–88.

Vasconcellos, M.B.A., Bode, P., Paletti, G., Catharino, M.G.M.,

Ammerlaan, A.K., Saiki, M., Favaro, D.I.T., Byrne, A.R., Baruzzi,

R., Rodrigues, D.A., 2000. Determination of mercury and selenium

in hair samples of Brazilian Indian populations living in the

Amazonic region by NAA. J. Radioanal. Nucl. Chem. 244, 81–85.

WHO-World Health Organization, 1976. Mercury, vol. 1. WHO,

Environmental Health Criteria, Geneva.

Yahia, D.A., Madani, S., Prost, E., Prost, J., Bouchenak, M.,

Belleville, J., 2003. Tissue antioxidant status differs in sponta-

neously hypertensive rats fed fish protein or casein. J. Nutr. 133,

479–482.

Yokoo, E.M., Valente, J.G., Sichieri, R., Silva, E.C., 2001. Validation

and calibration of mercury intake through self-referred fish

consumption in riverine populations in Pantanal Mato-grossense,

Brazil. Environ. Res. 86, 88–93.

Zollner, H., Below, H., Franke, G., Piek, M., Kramer, A., 2001.

Present alimentary supply of iodine in Western Pomerania. Dtsch.

Lebensm.-Rundsch. 97, 376–380.