Open Access

Hair mercury levels in Amazonian populations: spatial distribution and trends

International Journal of Health Geographics20098:71

https://doi.org/10.1186/1476-072X-8-71

Received: 1 September 2009

Accepted: 21 December 2009

Published: 21 December 2009

Abstract

Background

Mercury is present in the Amazonian aquatic environments from both natural and anthropogenic sources. As a consequence, many riverside populations are exposed to methylmercury, a highly toxic organic form of mercury, because of their intense fish consumption. Many studies have analysed this exposure from different approaches since the early nineties. This review aims to systematize the information in spatial distribution, comparing hair mercury levels by studied population and Amazonian river basin, looking for exposure trends.

Methods

The reviewed papers were selected from scientific databases and online libraries. We included studies with a direct measure of hair mercury concentrations in a sample size larger than 10 people, without considering the objectives, approach of the study or mercury speciation. The results are presented in tables and maps by river basin, displaying hair mercury levels and specifying the studied population and health impact, if any.

Results

The majority of the studies have been carried out in communities from the central Amazonian regions, particularly on the Tapajós River basin. The results seem quite variable; hair mercury means range from 1.1 to 34.2 μg/g. Most studies did not show any significant difference in hair mercury levels by gender or age. Overall, authors emphasized fish consumption frequency as the main risk factor of exposure. The most studied adverse health effect is by far the neurological performance, especially motricity. However, it is not possible to conclude on the relation between hair mercury levels and health impact in the Amazonian situation because of the relatively small number of studies.

Conclusions

Hair mercury levels in the Amazonian regions seem to be very heterogenic, depending on several factors. There is no obvious spatial trend and there are many areas that have never been studied. Taking into account the low mercury levels currently handled as acceptable, the majority of the Amazonian populations can be considered exposed to methylmercury contamination. The situation for many of these traditional communities is very complex because of their high dependence on fish nutrients. It remains difficult to conclude on the Public Health implication of mercury exposure in this context.

Background

Since the Minamata tragedy as well as the Basra incident, methylmercury contamination has been a source of concern worldwide. There has been extensive work attempting to assess the human health impact of mercury contamination through fish, seafood or marine mammal consumption, such as the Seychelles and Faroe Islands birth cohorts and the New Zealand study [18].

In the Amazonian aquatic environments, mercury is present in soils, water and food chains from complex sources [916]. On one hand, these soils have accumulated mercury naturally through time [9]. Human activities such as deforestation and agricultural land use can mobilize mercury from soils and vegetation [14, 15, 17, 18]. Also, the use of metallic mercury in the gold mining process can contribute to mercury contamination in these areas [1013, 16].

According to specific methylation rates, mercury compounds in certain aquatic environments can be transformed into methylmercury, the most toxic mercury compound. This organic form of mercury is easily assimilated and accumulated into the food chains, with biomagnification along the trophic levels [10]. This is the main pathway for human exposure via fish consumption.

The most deleterious and studied health effects of methylmercury are neurological dysfunctions [1922], especially from in utero exposure [4, 19, 2329]. Also, immunotoxic and citotoxic damages have been shown [3033], as well as cardiovascular deleterious effects [5, 3437]. It was not easy to reach a consensus regarding safe values for methylmercury exposure [38]. Overall, the tendency through time has been to lower the recommended level as much as possible, in order to minimize the health risk [39, 40]. Based on in utero neurological development, the Joint FAO/WHO Expert Committee on Food Additives suggested a Benchmark Dose Limit (BMDL) of 14 μg/g of mercury in maternal hair, recommending a daily mercury intake lower than 1.5 μg/kg of body weight [41]. The Environmental Protection Agency (EPA) stated the Reference Dose (RfD) at 0.1 μg/kg/day, expecting no more than 11 μg/g of mercury in maternal hair [42]. Most researchers have handled for Amazonian populations a BMDL of 10 μg/g of hair mercury [36, 43].

Amazonian riverside populations, which are amongst the highest fish consumers in the world, are exposed to mercury because of their alimentary habits. This situation has been widely studied in Brazil and French Guyana since the late eighties, showing quite complete information about the determinants of mercury exposure in these riverside populations [38, 4451]. However, there is an evident lack of data in the rest of the Amazonian countries, where there have been a few isolated studies.

We aimed to systematize the available data and extract relevant information regarding hair mercury levels and observed health effects in Amazonian populations. We focused on the spatial distribution trends, in order to compare hair mercury levels by river basin and studied population.

Methods

We used scientific databases and online libraries such as PubMed, ISI Web of Knowledge, ScienceDirect, SpringerLink, SciELO, Horizon, selecting articles with "Mercury, methylmercury, Amazon, hair, human exposure, fish consumption" as main keywords. We included the websites of international public institutions such as the Environmental Protection Agency (EPA), the Agency for Toxic Substances and Disease Registry (ATSDR), the World Health Organization (WHO) and the Food and Agriculture Organization (FAO).

The articles were included in this review if a measure of the hair mercury concentration was presented from the general population or a target group of an Amazonian region. We also considered similar basins in Brazil such as the Tocantins River and Guyana Plateau, because of their geographic and ecological interfaces with the Amazon regions.

Exclusion criteria were sample sizes less than 10 people, and the absence of a measure of central tendency (mean, geometric mean or median). Also, we excluded studies where the hair mercury concentration presented was an estimate calculated from the mercury concentration in fish tissue and the frequency and amount of fish consumption. In the cases where we found two or more articles corresponding to the same study and in the same population, we chose one to be represented on the maps.

We presented the results from all the selected articles in tables, showing author, study sites, sample sizes, hair mercury levels and fish consumption measures when available. The tables were organized by regions and using the same continuity given by the maps, starting with studies from Andean Amazonian countries (Table 1) and French Guyana (Table 2). Brazilian studies are presented in the following tables, divided according to the studied population or group (Tables 3, 4, 5). The studies conducted in the Tapajós River basins were presented in independent tables, also separated according to the studied population or group (Tables 6, 7, 8, 9). Finally, the studies from the Madeira River basin were displayed separately in the last table (Table 10).
Table 1

Hair mercury levels in Andean Amazonian Countries

Studied population

Study

N

Hg mean μg/g

Range

> 10 μg/ga

Fish

Country, River Basin

  

(median) [SD]

μg/g

  

General population

      

Barbieri et al. 2009

Cachuela Esperanza

150

3.76 (3.01) [2.52]

0.42-15.65

3%

10.5 meals/week

   Bolivia, Beni River

      

Monrroy et al. 2008

Upper Beni River

556

5.3 (4.0) [4.3]

0.08-34.

≈ 14.0%

 

   Bolivia, Beni River

   Children

393

5.2 (3.9) [4.4]

0.08-34.1

  
 

   Mothers

163

5.5 (4.4) [4.1]

0.15-20.0

  
 

   Pregnant women

18

3.2 (3.3) [2.1]

0.2-7.8

  
 

   Breastfeeding (BF)

57

6.2 (5.5) [4.1]

0.5-18.3

  
 

   Non pregnant, non BF

93

5.4 (4.1) [4.1]

0.15-20.0

  

Maurice-Bourgoin et al. 2000

Rurrenabaque

80

    

   Bolivia, Beni River

   Esse-Ejjas indigenous

37

9.8

4.3-19.5

  

Webb et al. 2004

Coca

45

1.9(1.5)

0.03-10.0

 

7.5 meals/month

   Ecuador, Napo River

Añangu

27

8.7 (7.8)

2.2-20.5

 

17.2 meals/month

 

Pañacocha

27

5.3 (5.0)

1.5-13.6

 

33.9 meals/month

Children

      

Counter et al. 2005

Nambija gold-mining

80

2.8b (2.0) [17.5]

1.0-135.0

<10%

 

   Ecuador, Nambija River

settlement

     

aPercentage of the population with hair mercury levels higher than 10 μg/g. bGeometric mean.

Table 2

Hair mercury levels in French Guyana

Studied

population

River

basin

Location

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

General

population

       

BASAG

2007

Maroni

River

Sinnamary

285

1.8

 

5%

 
 

Oyapok

River

Lower Maroni River

740

1.7-3.6

 

2.4%

 
  

Lower Oyapok

144

1.5-3.4

 

1 person

 
  

River

181

4.6-7.2

 

7.6-18.2%

 
  

Upper Oyapok River

     

Cordier

et al. 1998

Maroni

River

Oyapok

River

11 health centers

     
  

   Adults

255

3.4b

0.2-22.0

12.2%

 
  

   Pregnant women

109

1.6b

0.2-13.0

4.6%

 
  

   Children

136

2.5b

0.2-31.0

11.8

 

Fréry

et al. 2001

Maroni

River

Cayodé, Twenké,

Taluhen and

Antécume-Pata

235

11.4 [4.2]

1.9-27.2

57.4%

20-317 g/day

Mothers and their infants

       

Cordier

et al. 2002

Maroni

River

Oyapok

River

Upper

Maroni River

     
  

   Children

156

10.2b

 

79%

2 meals/day

  

   Mothers

90

12.7b

   
  

Oyapok River

     
  

   Children

69

6.5b

   
  

   Mothers

63

6.7b

   
  

Lower Maroni River

     
  

   Children

153

1.4b

   
  

   Mothers

77

2.8b

   

aPercentage of the population with hair mercury levels higher than 10 μg/g. bGeometric mean.

Table 3

Hair mercury levels in Brazilian River Basins, General Population

Study

River Basin

Location

N

Hg mean μg/g

(median) [SD]

Range μ

g/g

> 10 μg/ga

Fish

consumption

Akagi

et al. 1995

Três Bocas

11

28.1

8.4-54.0

  

   Araguari River

      

Castro et al. 1991

Surucucus,

Paapiu and

Mujacai areas

162

3.61

1.4-8.1

  

   Branco River

      

Forsberg et al. 1995

Various sites

between Marie

and Paduari Rivers

154

75.5 [35.2]

5.8-171.2

  

   Negro River

      

Kehrig et al. 1998

Balbina Reservoir

53

6.5 [5.4]

1.2-22.0

 

110 g

   Negro River

      

Leino & Lodenius 1995

Tucuruí area

125

35.0 (29.0)

0.9-240.0

 

11 meals/week

   Tocantins River

      

Pinheiro, Nakanishi

et al. 2000

Belém

13

2.0

   

   Tocantins River

      

Santos, Camara

et al. 2002

Caxiuanã

214

8.6 [6.3]

0.6-46.0

 

12.3 meals/week

   Amazon River

      

Santos

et al. 2003

Lower Mamoré:

Pakaás Novos Indigenous

Areas

910

8.4 (6.9) [6.4]

0.5-83.9

  

   Mamoré River

      

Soares et al. 2002

Doutor Tanajura

13

(6.1)

1.4-11.7

  

   Mamoré River

      

Vasconcellos et al. 1994

Indigenous Xingu Park

27

18.5 (18) [5.9]

6.9-34.0

  

   Xingu River

Billings Dam

28

0.9 (0.7) [0.7]

0.3-3.0

  
 

Controls

25

1.1 (1.0) [0.6]

0.3-2.5

  

Vasconcellos

et al. 2000

Xingu Park

(13 groups)

  

1.2-57.3

  

   Xingu River

   Highest values

 

21.8 (20.8) [6.1]

   
 

   Lowest values

 

3.6 (2.6) [2.4]

   

The Tapajós and Madeira Rivers basins are not displayed in this table (see Tables 5, 6, 7, 8, 9, 10). aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 4

Mercury levels in Brazilian River Basins, Target Groups

Studied population

River Basin

Location

N

Hg mean μg/g

(median) [SD]

Range

μg/g

> 10 μg/ga

Fish

consumption

Adults

      

Barbosa

et al. 2001

Negro River

shores

76

21.4 (17.8) [12.7]

1.7-59.0

79%

 

Negro River

   Men

17

26.2 [13.7]

   
 

   Women

31

18.3 [11.1]

   

Pinheiro

et al. 2006

Panacauera

22

≈ 7.0

   

Tocantins

River

Pindobal Grande

43

≈ 3.0

   

Silva

et al. 2004

Tabatinga

98

(6.4)

1.2-17.0

  

Amazon River, lakes

      

Yokoo

et al. 2003

Pantanal region

129

4.2 (3.7) [2.4]

0.6-13.6

  

Cuiabá River

      

Children

      

Barbosa

et al. 2001

Negro River

shores

73

18.5 (16.4) [10.0]

0.5-45.9

79%

 

Negro River

      

Pinheiro

et al. 2006

Pindobal Grande

88

≈ 3.0

   

Tocantins River

      

Pinheiro

et al. 2007

Panacauera

36

2.3

0.4-9.5

0%

 

Tocantins River

      

Santos-Filho

et al. 1993

Cubatão

Municipality

217

0.8 [0.5]

0.2-3.0

0%

 

Cubatão

River

      

Tavares

et al. 2005

Barão de Melgaço

114

2.1 (1.8) [1.4]

0.4-7.6

0%

4.6 meals/week

Cuiabá River

Riverside

communities

72

5.4 (4.7) [3.4]

0.6-17.1

 

7.8 meals/week

Women

      

Pinheiro

et al. 2008

Panacauera

20

3.3

1.3-6.0

0%

 

Tocantins River

      

Mothers and

their infants

      

Barbosa

et al. 1998

Garimpo

Maria Bonita

     

Fresco River

(Xingu basin)

   Mothers

28

8.1 (8.3) [3.2]

0.8-13.7

  
 

   Infants

54

7.3 (6.6) [3.5]

2.0-20.4

  

The Tapajós and Madeira Rivers basins are not displayed in this table (see Tables 5, 6, 7, 8, 9, 10). aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 5

Hair mercury levels in Brazilian River Basins, Occupational Groups

Study

Location

N

Hg mean μg/g

Range

> 10 μg/ga

Fish

consumption

River Basin

  

(median) [SD]

   

Guimarães et al 1999

Pracuúba Lake

15

16.7

   

   Tartarugal Grande River (Fishermen)

Duas Bocas Lake

15

28.0

 

87%

14 meals/week (200 g per day)

 

Groups

     

Palheta & Taylor 1995

Garimpeiros

20

 

0.4-32.

  

   Gurupi River

Cachoeira Villagers

5

 

0.8-4.6

  
 

River dwellers

10

 

0.2-15

  

The Tapajos and Madeira Rivers basins are not displayed in this table (see Tables 5, 6, 7, 8, 9, 10). aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 6

Hair mercury levels in the Tapajós River Basin, General Population

Study

Location

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

Akagi et al. 1995

Rainha

11

15.8

2.4-31.0

  
 

Brasília Legal

56

22.6

3.5-151.0

  
 

Ponta de Pedra

10

10.2

6.2-12.6

  
 

Jacareacanga

48

16.6

1.5-46.0

  

Barbosa et al. 1997

Apiacás Reservation

55

34.2 (42.8)

?-128

93%

≈ 6 times/week

Crompton et al. 2002

Jacareacanga

205

8.6

0.3-83.2

  

Dorea et al. 2005

Kaburuá

89

2.5 [1.4]

  

22 g/day

 

Cururu Mission

138

3.7 [1.6]

  

32 g/day

 

Terra Preta

22

6.0 [2.9]

  

52 g/day

 

Kayabi

47

12.8 [7.0]

  

110 g/day

Malm et al. 1995

Jacareacanga

10

25.0

5.7-52.0

  
 

Brasília Legal

13-29

26.0

4.7-151.0

  
 

Ponta de Pedra

4-26

12.0

   
 

Santarem

11

2.7

   

Pinheiro, Guimarães et al. 2000

Rainha

29

17.2

   
 

Barreiras

111

18.9

   
 

São Luís do Tapajós

30

25.3

   
 

Paranα-Mirim

21

9.2

   

Pinheiro, Nakanishi et al. 2000

Rainha

29

17.6

   
 

Barreiras

78

19.1

   

Santos et al. 2000

Brasília Legal

220

11.8 [8.0]

0.5-50.0

 

10 meals/week

 

São Luís do Tapajós

327

19.9 [12.0]

0.1-94.5

 

13 meals/week

 

Santana do Ituquí

321

4.3 [1.9]

0.4-11.6

 

13 meals/week

Santos, Camara et al 2002

Santana do Ituquí

321

4.3 [2.2]

0.4-12.0

 

12.7 meals/week

 

Aldeia do Lago Grande

316

4.0 [2.1]

0.4-12.0

 

12.0 meals/week

 

Vila do Tabatinga

499

5.4 [3.1]

0.4-17.0

 

10.5 meals/week

Santos, de Jesus et al. 2002

Sai Cinza

324

16.0 [18.9]

4,5-90,4

  

Silva et al. 2004

Jacareacanga

140

(8.0)

0.3-58.5

  
 

Rio-Rato

98

 

0.01-81.4

  

a Percentage of the population with hair mercury levels higher than 10 μg/g.

Table 7

Hair mercury levels in the Tapajós River Basin, Adults

Study

Location

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

Amorim et al. 2000

Brasília Legal

98

(13.5)

0.6-71.8

>50%

 
 

   Women

 

(10.8)

   
 

   Men

 

(17.1)

   

Dolbec et al. 2000

Cametá

68

10.8 (9.0) [6.1]

  

61.8% of total meals

 

   Women

41

9.9 (8.0) [5.6]

 

>25%

 
 

   Men

27

12.2 (10.8) [6.8]

 

>50%

 

Fillion et al. 2006

São Luís do Tapajós,

Nova Canaã, Santo Antônio,

Mussum, Vista Alegre and Açaituba

251

17.8

0.2-77.2

69.7%

6.8 meals/week

Lebel et al. 1997

Brasília Legal

96

(12.9)

 

>50%

 
 

   Women

 

(11.2)

  

44.7% of total meals

 

   Men

 

(15.7)

  

43.9% of total meals

Lebel et al. 1998

Brasília Legal

     
 

   Men

34

14.3 [9.4]

   
 

   Women

46

12.6 [7.0]

   

Passos et al. 2007

SLTapajós, Nova Canaã,

Santo Antônio, Ipaupixuna, Novo Paraíso,

Teça, Timbu, Açaituba, Campo Alegre,

Samauma, Mussum, Vista Alegre and Santa Cruz

457

16.8 (15.7) [10.3]

0.2-58.3

>50%

6.6 meals/week

Pinheiro et al. 2006

São Luís do Tapajós

32

≈ 15.0

   
 

Barreiras

37

≈ 15.5

   

Silva et al. 2004

Vila do Tabatinga

98

(6.4)

1.2-17.0

  

aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 8

Hair mercury levels in the Tapajós River Basin Women and Children

Studied

population

Location

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

Mothers and

their Children

      

   Grandjean et al. 1999

Mothers

114

11.6 (14.0)

   
 

Children

 

11.0 (12.8)

0.5-83.5

 

2 meals/day

 

   Brasilia Legal

76

11.9

0.7-35.8

76%

 
 

   São Luís do Tapajós

71

25.4

0.6-83.5

91%

 
 

   Sai-Cinza

87

17.7

7.3-63.8

92%

 
 

   Santana do Ituquí

105

3.8

0.5-12.4

2%

 

Children

      

   Barbosa et al. 1997

Apiacás Reservation

28

29

 

86%

 

   Dorea, Barbosa et al. 2005

Kaburuá

77

2.9 [2.1]

   
 

Cururu Mission

86

4.8 [2.1]

   
 

Kayabi

40

16.6 [11.4]

   

   Pinheiro et al. 2007

São Luís do Tapajós

48

10.9

1.3-53.8

52%

 
 

Barreiras

84

6.1

1.4-23.6

21%

 

Women

      

   Barbosa et al. 1997

Apiacás Reservation

13

41.2

 

100%

 

   Dolbec et al. 2001

Cametá

98

(12.5)

2.9-27.0

>50%

 

   Hacon et al. 2000

Alta Floresta

75

1.12 [1.2]

0,05-8,2

0%

8-20 g/day

   Passos et al. 2003

Brasília Legal

26

10.0 (9.1)

4.0-20.0

≈ 50%

8 meals/week

   Pinheiro et al. 2007

São Luís do Tapajós

    

5-14 meals/week

 

Rainha, and Barreiras

     
 

   Pregnant

19

8.2

1.5-19.4

37%

 
 

   Non-pregnant

21

9.4

5.2-21.0

28%

 

   Pinheiro et al. 2005

São Luís do Tapajós

28

13.7

3.2-30.04

36%

 
 

Barreiras

39

12.1

3.04-33.4

38%

 

aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 9

Hair mercury levels in the Tapajós River Basin, Occupational Groups

Study

Locations

and groups

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

Harada et al. 2001

Fishermen and families

     
 

   Barreiras

76

16.4 [10.6]

1.8-53.8

75%

 
 

   Rainha

12

14.1 [9.3]

3.1-34.5

67%

 
 

   São Luís do Tapajós

44

20.8 [10.6]

5.1-42.2

86%

 

Lebel et al. 1997

Brasília Legal

     
 

   Fishermen

14

(27.3)

 

> 50%

68.8% of total meals

Lebel et al. 1998

Brasília Legal

     
 

   Fishermen

11

23.9 [9.3]

   

Santos, de Jesus et al. 2002

Sai Cinza

324

16.0 [18.9]

4,5-90,4

  
 

   Agriculture

127

17.3

6.8-90.4

  
 

   Gold mining

6

13.8

10.7-18.5

  
 

   Both of the above

25

13.8

6.9-25.7

  
 

   Others

11

12.3

6.6-20.6

  
 

   Children up to 6 y/o

93

16.8

4.5-66.6

  
 

   Students

38

15.1

9.0-38.7

  
 

   Without information

24

17.0

9.6-30.8

  

aPercentage of the population with hair mercury levels higher than 10 μg/g.

Table 10

Hair mercury levels in the Madeira River Basin

Studied population

Location

N

Hg mean μg/g

(median) [SD]

Range μg/g

> 10 μg/ga

Fish

consumption

General population

      

   Bastos et al. 2006

Various populations along the Madeira River

713

15.2 (12.5) [9.6]

0.36-150.0

>50%

7 meals/week

   Boischio & Barbosa 1993

Near Porto Velho

311

≈ (10)

?-303.1

51%

200 g/dayb

Mothers and their infants

      

   Barbosa & Dorea 1998

Near Porto Velho

     
 

   Mothers

98

14.1 (12.8) [10.7]

2.6-94.7

>50%

 
 

   Infants

71

10.8 (7.8) [8.5]

0.8-44.4

  

   Boschio & Cernichiari 1998

Near Porto Velho

     
 

   Mothers

12

 

4.0-41.0

  
 

   Infants

12

 

8.2-50.4

  

Boischio & Henshel 2000

Near Porto Velho

     
 

   Mothers

90

12.6 [6.5]

15.0-45.0

  
 

   Infants

89

10.2 [7.2]

1.0-34.2

  

Marques et al. 2007

Porto Velho city

     
 

   Mothers

82

(5.4)

0.4-62.4

 

1 meal/week

 

   Infants

82

(1.8)

0.02-32.9

  

aPercentage of the population with hair mercury levels higher than 10 μg/g. bFrom the Letter to the Editor Boischio Environ Research 2000; 82:91-92

In the cases when an article studied populations from different river basins, we presented them separately, in the corresponding basin tables.

For the design of the maps, we located each Amazonian study site using their longitude and latitude data when available in the article. Otherwise, we searched longitude and latitude data in geographic databases and using Google Earth, which allowed us to find and successfully locate the majority of the study sites. When it was not possible to identify the coordinates, we used the maps and/or site descriptions presented by the authors. We marked and named each study site on the map displaying a representation of the hair mercury levels found in this population in a six colour scale. Each individual square on the map represents a hair mercury measure and the target group used for the study, as well as the reference number. We prepared separated maps for the Madeira River, the Tapajós River and French Guiana. We also designed a map illustrating the studies that assessed health outcomes in relation to hair mercury levels in the studied populations, using a three colour scale for the different results.

Results and Discussion

We found 58 articles meeting our criteria for the elaboration of the maps. The majority of the studies were carried out in Brazil (86%), while there are only 3 studies in French Guyana, 3 in Bolivia and 2 in Ecuador (Figures 1, 2). In Brazil, 30 studies are focused on the Tapajós River basin (Figure 3), 10 on the Madeira River basin (Figure 4) and the remaining 20% of these Brazilian studies are from other basins, such as the Negro River, the Tocantins River or the Xingu River (Figure 1).
Figure 1

Hair mercury levels in the Amazon River basin.

Figure 2

Hair mercury levels in French Guyana.

Figure 3

Hair mercury levels in the Tapajós River basin, Brazil.

Figure 4

Hair mercury levels in the Madeira River basin, Brazil.

The approaches and strategies are quite variable between studies. Several studies have used a large sample size, selected randomly from the general population (Tables 1, 2, 3, 6, 10), and usually comparing two or three sites from the same basin. Some of them used smaller sample sizes, accepting the variability induced by the sampling fluctuation in order to extend to several populations geographically close to each other. In the Madeira River (Figure 4; Table 10), the study by Bastos et al. (2006) covered from the upper basin (near the Bolivian border) to a point downstream on the Amazon River [52]. Even if some of the populations had sample sizes of less than 10 people, the locations evaluated were 44, distributed along the largest part of the Madeira basin (Figure 4).

In French Guiana the studies have used both approaches, covering almost the totality of the Maroni and Oyapok River basins, with large sample sizes from the general population (Figure 2; Table 2) [47, 53, 54].

Hair mercury levels in the Amazon

In the Andean Amazonian regions (Figure 1; Table 1), mercury levels were found below 10 μg/g in Ecuador [55, 56] and Bolivia [5759].

In French Guiana (Figure 2; Table 2), most study sites showed hair mercury levels below 10 μg/g in the Oyapok River and the lower Maroni River basins [53, 60]. The only populations with mercury levels above 10 μg/g were located in an Amerindian reservation in the upper Maroni River basin [47, 53, 54].

In Brazilian Amazonia (Figures 1, 3, 4; Tables 3, 4, 5) hair mercury levels are very variable between basins and study sites. Without considering the studies from the Tapajós and Madeira Rivers, which will be explained in detail below, the highest mercury levels can be found in the Negro River basin [61, 62] and at the lakes from the Amapá State (Figure 1; Tables 3, 4, 5) [63], with means above 20 μg/g and even higher than 25 μg/g. These high values can also be found in two other sites from the Xingu and Tocantins Rivers, both from Amerindian reservations (Figure 1) [51, 6468]. These levels can be considered of a high risk for the populations and would merit further investigations about the health impact of this exposure. The rest of these study sites show hair mercury levels below 10 μg/g, with the exception of an Amerindian reservation on the Mamoré River (13.1 μg/g) [69].

Tapajós River basin

In the Tapajós River basin (Figure 3; Tables 6, 7, 8, 9) there is a wide difference in mercury levels between the various populations. Most locations present hair mercury levels above 10 μg/g, especially in some populations such as Rainha, Barreiras, Brasília Legal or São Luís do Tapajós [34, 7073], where exposure levels seem to be alarming, even reaching a mean over 30 μg/g in the Apiacás Reservation study [74]. In very few sites the hair mercury levels remained below 5 μg/g [75, 76]. The populations living in urban or suburban areas (Santarém and Santana do Ituquí) were used as control populations by the authors and showed lower exposure levels attributed to their food diversification [33, 7779]. In the same way, some authors used study sites from different river basins to compare their exposure levels, such as Panacuera or the city of Belém (Figure 1) [65, 73].

Unexpectedly, studies carried out in the same site and target group obtained quite different results. For example, in Jacareacanga the studies on the general population published in 1995 [77, 80] showed much higher levels (means of 16.6 and 25.0 μg/g) than those carried out in the following decade (mean = 8.6 μg/g and median = 8.0 μg/g) [33, 81]. The sample sizes and study designs were very different. In 1995, Jacareacanga was a village with approximately 3000 inhabitants, and the two studies published that year took samples of 10 and 48 people. In 2002, the population of Jacareacanga was around 2000 inhabitants, and the studies published in 2002 and 2004 took samples of 140 and 205 people. Other than that, there is not enough information to explain the observed difference in hair mercury levels. There is no evidence of a change in the fish consumption frequency, deforestation, colonization, agricultural land use or gold mining activities.

Madeira River basin

In the Madeira River basin (Figure 4; Table 10) most study sites showed hair mercury levels between 11 μg/g and 15 μg/g [52, 8285]. A couple of sites (very close to each other) presented hair mercury levels above 20 μg/g [52]. A few sites showed levels between 16 μg/g and 20 μg/g and the others presented hair mercury levels under 10 μg/g [52, 82, 83, 85]. This shows a mercury exposure distribution that appears to be less heterogenic than the Tapajós River basin. The higher mercury levels seem to be found in small isolated villages on the middle of the basin, downstream from Humaitá, near Manicoré (Figure 4).

Mercury levels and fish consumption

In the Brazilian Amazon, many studies include especially fish consumption in the population, even though not all of them show these results (Tables 1, 2, 3, 4, 5, 6, 7, 8, 9, 10). Fish consumption is not measured in a uniform manner in all the studies. Each research team chose their indicators according to their objectives, so this measure can be found in grams per day, percentage of meals composed by fish, meals per week or per day and/or times per week. No matter which indicator for fish consumption the authors chose, there was always a positive relation between fish consumption and hair mercury levels [19, 46, 47, 49, 64, 75, 76]. Most of these study sites are usually small and traditional riverside villages, some of them Amerindian reservations, without the proper roads connecting them to larger villages and cities. It is possible to hypothesize that this situation makes those populations more dependent on fish as source of protein intake.

In spite of those considerations, some populations with high fish consumption showed hair mercury levels below 10 μg/g, even if there was a significant relation with fish consumption frequency [5557, 59, 78, 79]. In those particular six studies, it is important to consider the different geographical and socio-economic situation those populations are in: three of those studies were conducted in the Andean piedmont Amazonian regions, the two Ecuadorian studies [55, 56] and one of the Bolivian studies [57]. Also, those populations are not solely dependent on fish because they are also farmers or hunters, even if fish remains the most important source of nutrients. The Bolivian population of Cachuela Esperanza, located near the Brazilian border, consumes large amounts of fish (10 fish meals per week), but only during the dry season, preferring game meat during the rainy season, which lasts from October to April [57].

The other two cases with intense fish consumption and low hair mercury levels are the studies conducted in Aldeia do Lago Grande, Santana do Ituquí and Vila to Tabatinga. These communities are located on the Amazon River shore, near the confluence with the Tapajós River. They are small but not isolated because they are connected by roads to the cities of Monte Alegre, Santarém and Juruti. The low hair mercury levels cannot be explained by food diversification, because these populations consume 10 to 13 fish meals per week. However, the fish they consume is collected from local lakes and minor rivers, and the mercury concentrations in fish tissue was found to be much lower than in other exposed populations [52, 78, 79].

On the Madeira River basin, where most hair mercury levels remained under 10 μg/g, the fish consumption in the majority of the populations was around seven meals per week (Table 10). On the contrary, on the Tapajós River basin the fish consumption in the majority of the populations was higher than 10 meals per week (Table 6).

Some studies measured mercury concentrations in fish tissue, finding positive relations between fish mercury concentrations, fish consumption and human hair mercury levels [13, 75, 77, 80, 86].

Studied populations

Due to the importance of mercury exposure and its health effects in children, as well as in utero exposure, many studies have chosen fertile age women and children as target groups (Tables 1, 2, 4, 8, 10). These studies are generally consistent with studies on the general population, with comparable hair mercury levels. When studied together as mother-infant pairs, there was always a strong relation between maternal hair mercury and the exposure in their infants; the mothers always had higher mercury levels than their infants [26, 60, 82, 83, 85, 87].

The majority of the studies did not find any significant relationship between age and hair mercury levels [13, 30, 33, 44, 48, 61, 66, 77, 78, 85, 8892]. Some studies found that hair mercury levels increase with age [74, 78, 79, 81, 84]. Nevertheless, a couple of studies found the opposite results, showing higher hair mercury levels in younger people, children and infants [58, 69].

Several studies found that men have higher hair mercury levels than women [19, 30, 34, 61, 65, 69, 71, 74, 84, 87]. In two articles from the Tapajós River basin, only the fishermen had hair mercury levels significantly higher than the women, while the other men from the same village presented hair mercury levels similar to those of the women (Tables 7, 8). Those differences corresponded to their fish consumption, which was also significantly higher for the fishermen [20, 49]. Only one study found women to have higher mercury levels than men [69].

No study revealed physiological basis that could lead to hypothesize a difference between female and male mercury metabolism. In fact, most studies (78%) did not find any significant relation between mercury exposure and gender.

A few studies focused their attention on fishermen, because of their obvious access to fish as main nutrient [49, 63, 70]. Their hair mercury means ranged from 16 to more than 25 μg/g, regardless of the river basin. For instance, the studies conducted by Lebel et al. (1997, 1998) compared fishermen and other adults from the Brasilia Legal population. Both men and women had mercury levels lower than 15 μg/g, while fishermen presented levels of 27.3 μg/g and 23.9 μg/g (Figure 3; Tables 7, 8) [20, 49].

The particular case of gold miners (called garimpeiros in Brazil and Bolivia) has been documented in a couple of studies. It is important to remark that occupational mercury exposure is very different from the environmental exposure. Artisanal garimpeiros are occupationally exposed to metallic mercury vapours, which are rapidly transformed in the human body into inorganic mercury, best measured in urine or plasma, while total hair mercury corresponds mainly to methylmercury exposure in high fish eating populations [36, 93]. Generally, the authors found that garimpeiros had lower hair mercury levels than the ribeirinhos [58, 94], concluding that because of their better economical situation, they were able to diversify their food, consuming less fish than the rest of the population[13]. However, in a few studies the garimpeiros or gold miners had higher total mercury levels in hair than the general population, without apparent relation with fish consumption frequency [45, 57, 95, 96]. Consistently, in those three studies the hair mercury means in the general population were lower than those found in most central Amazonian studies. In both the Bolivian study and the Colombian study, hair mercury means remained below 6 μg/g, even in the most exposed groups [57, 95]. It would be possible to assume that metallic mercury exposure can acquire significance in hair mercury levels in some specific situations of low methylmercury exposure. However, considering the differences between those studies and regions, and without hair mercury speciation, it is not possible to reach valid conclusions.

Multidisciplinary studies

Five studies carried out a multidisciplinary approach, measuring as well mercury in air, water, sediments, fish and human samples [13, 52, 58, 63, 96]. In those studies, human exposure seemed to be considered as a part of the totality of the environmental contamination. Therefore, those hair mercury levels were useful as a reference value for those specific study sites, and need to be interpreted in the whole context rather than as a Public Health assessment. These studies showed in a precise manner the interactions within various environmental components, showing a direct relation between mercury concentrations at different levels of the ecosystem and the food chains, including the human being as the last receptor of this pollution.

An example of an ecosystem approach is the CARUSO project [14, 15, 1720, 30, 34, 49, 71, 88, 97100]. This project started in 1994, and consists on a series of studies conducted by research teams of different disciplines, attempting to assess the various aspects of mercury pollution and human exposure in the Tapajós River basin.

Hair mercury levels and health impact

There were 15 studies conducted in Brazil and one in French Guyana (Figure 5). Most of them (73%) focused on neurological effects.
Figure 5

Hair mercury levels and health impact in the Amazon River basin.

In the Amazonian context it is not easy to identify a clear relation between hair mercury levels and patent neurological abnormalities. Observing the spatial distribution of the studies, we can see that in populations with low hair mercury levels, such as Santana do Ituquí, Vila do Tabatinga or the city of Porto Velho, it was not possible to confirm a relation between mercury levels and neurological performance [26, 78, 79, 101]. Also, in the populations with higher mercury exposure, the authors found an impact on the nervous system, especially motricity [19, 20, 60].

However, in São Luís do Tapajós or Brasília Legal the information is difficult to interpret. There were two studies assessing neurotoxicity in the general population and one in adults. While one of those studies documented cases of mild Minamata disease [70], the other did not find any relation between hair mercury levels and neurological outcomes [79]. On the contrary, the study conducted in adults found a dose-dependent relation between hair mercury levels and motor abnormalities [20]. There was also a study that found an association between exposure and psychomotor performance in children, but the authors concluded that the outcomes observed were also influenced by socioeconomic factors, such as maternal educational level or nutritional status [87].

Two studies have evaluated the impact of mercury exposure on the immune system in vitro. The authors found positive relations between mercury levels and the presentation of auto-antibodies [33] and cytogenetic abnormalities in peripheral lymphocytes [30], especially in the most exposed Amazonian populations.

There are a couple of studies about mercury exposure and blood pressure on the Tapajós River basin. One of them supports a negative impact of mercury exposure on the cardiovascular system [34], while the other did not find a significant relation between mercury levels and blood pressure [76]. This second study was conducted in four Amerindian populations located on rivers tributaries to the Tapajós, with low hair mercury levels. The authors found that the community with higher hair mercury levels (12.8 μg/g) seemed to be protected against age-related increase of blood pressure, because of their intense fish consumption [76].

Two studies were focused on children's growth. One of these studies was carried out in an Amerindian community from the Tapajós River [75]. No significant correlation was found between growth or nutritional status and hair mercury levels. On the contrary, a study in the Bolivian Amazonia found a positive relation between hair mercury levels and a better nutritional status in children ranging from 5 to 10 years of age [102]. Considering the characteristics of that population, the authors hypothesized that the relation observed was caused by the nutritional contents in fish, mostly important at that age group. Furthermore, the same study found the opposite result in the mothers, with worse nutritional indices in the women with higher mercury levels. In fact, while some authors worry about the health impact of mercury exposure in high fish eating populations [38, 99, 103], others consider that the nutritional value of fish probably compensate an exposure to low mercury levels [46, 75, 102, 104, 105]. In absence of large cohort studies, as the ones developed in the Faeroe Islands and Seychelles, the issue of health impact in the Amazonian context still remains open for debate.

Other interactions

Interest has recently been focused on the relation between mercury exposure and antioxidant defences, suggesting that long term mercury exposure induced a depletion in the antioxidant enzymatic activity [67].

Interactions between fish and fruit consumption were studied in a population from the Tapajós River, finding an inverse relationship between fruit consumption and Hg levels [71, 100]. The authors recommended further investigation to establish new nutritional strategies aiming to limit mercury exposure while maintaining fish consumption.

Recently, some studies also emphasized the interactions between mercury and selenium from dietary sources, especially fish consumption [68, 90, 92, 98]. The authors generally found high concentrations of selenium in the populations exposed to methylmercury, with molar ratios consistently close to 1. Based on their observations, the authors suggest the need of further research regarding the protective role of selenium against mercury toxicity.

Variability in exposure assessment

As seen on the maps and tables, there is a considerable spatial and temporal variability in the measure of mercury exposure. Fish consumption frequency alone does not explain the differences in hair mercury levels in some study sites. There are several factors involved: the characteristics of the soils, methylation rates in different aquatic environments, the food chain structures, specific human habits and diets, social and economic characteristics, mercury interactions with other elements, and also strong local variations without a clear explanation. Moreover, many of these small populations are subjects to intense changes through time. Human migration, land use and deforestation are usually associated with erosion peaks, which could temporarily mobilize mercury from the soils [14, 15, 17, 18].

It is also possible to attribute some of the variations observed to the use of hair as biomarker. It has been stated that methylmercury corresponds to more than 90% of total hair mercury [19, 93, 106]. Therefore, total mercury in hair has been widely accepted as a well-validated methylmercury exposure marker, reflecting non-occupational exposure by seafood or fish consumption. Nevertheless, a study by Barbosa et al. (2001) in a Negro River basin population found important variations in the percentage of methylmercury in total hair mercury, ranging from 34% to 100% [61]. This variation did not seem to be influenced by age, gender, body mass index, frequency of fish consumption or total hair mercury levels. Besides, it is worth mentioning that the use of this biomarker for toxicological purposes has been criticized for its lack of reproducibility [107, 108].

That sum of factors makes it difficult to assess a certain situation with exactitude in a determined population. Also, it is important to consider the variability induced by the different sampling, target populations and methodologies used by the researchers according to their objectives. Therefore, we assume that not every hair mercury value represented on the maps and tables can be completely or accurately comparable to each other for epidemiological purposes.

Conclusions

Considering the current recommendations from the environmental agencies, it is patent that almost all the Amazonian riverside populations are exposed to mercury contamination through alimentary habits. There is no evident spatial trend, even if the highest hair mercury levels were found in the central Amazonian regions, especially the Tapajós River basin. Small and isolated communities with traditional lifestyles seem to be the most exposed to mercury, regardless of the river basin. This situation is very complex for these populations, given that many of them depend on fish for economic support as well as almost unique source of dietary protein.

The available information about the health impact of this situation is not conclusive. Therefore, it becomes difficult to assess accurately the Public Health implication of mercury exposure in this particular context.

Besides, there are numerous Amazonian regions with lacking data and also with discordant results. Thus, a harmonized assessment of mercury human exposure based on a standardized approach would be valuable in order to spatially identify the most contaminated populations. This assessment would also allow prospective follow-ups of exposed populations, especially considering that these small communities are in constant evolution and subject of global changes.

Declarations

Authors’ Affiliations

(1)
IRD - SELADIS
(2)
IRD - HSM

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