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Environmental Research 92 (2003) 232–244
Fish are central in the diet of Amazonian riparians: should we worry
about their mercury concentrations?
Jose G. Dorea
Faculdade de Ciências da Saúde, Universidade de Brası´lia, Nutrition C.P. 04322, 70910-970 Brası´lia, DF, Brazil
Received 4 April 2002; received in revised form 17 November 2002; accepted 18 December 2002
Abstract
The Amazon rain forest extends over an area of 7.8 106 km2 in nine countries. It harbors a diverse human population distributed
in dense cities and isolated communities with extreme levels of infrastructure. Amazonian forest people, either autochthons or
frontier riparians (ribeirinhos) living in isolated areas, share the same environment for survival and nutritional status. The
peculiarities of the hydrological cycle determine disease patterns, agricultural conditions, and food availability. Feeding strategies
depend heavily on cassava products and fish. These two foods carry toxic substances such as linamarin (naturally present in cassava)
and monomethyl mercury (MMHg) (bioconcentrated in fish flesh) that cause neurotoxic diseases in other parts of the world but not
in Amazonia, where neurotoxic cases of food origin are rare and not related to these staples. While cassava detoxification processes
may partly explain its safe consumption, the Hg concentrations in Amazonian fish are within traditionally safe limits for this
population and contribute to an important metabolic interaction with cassava. The gold rush of the 1970s and 1980s brought largescale environmental disruption and physical destruction of ecosystems at impact points, along with a heavy discharge of metallic Hg.
The discharged Hg has not yet impacted on MMHg concentrations in fish or in hair of fish consumers. Hair Hg concentration, used
as a biomarker of fish consumption, indicates that the Amazonian riparians are acquiring an excellent source of protein carrying
important nutrients, the lack of which could aggravate their existing health problems. Therefore, in a scenario of insufficient health
services and an unhealthy environment, food habits based on fish consumption are part of a successful survival strategy and
recommendations for changes are not yet justifiable.
r 2003 Elsevier Science (USA). All rights reserved.
Keywords: Amazon; Cassava; Methylmercury; Cyanide; Neuropathy; Amerindians
1. Introduction
The Amazon rain forest encompasses an area of
7.8 106 km2 extending over nine countries (Bolivia,
Brazil, Colombia, Ecuador, Peru, French Guyana,
Guyana, Surinam, and Venezuela), most of which is in
Brazilian territory. Its aquatic ecosystems vary dramatically in size, geographical location, catchment geochemistry, colonization, and human activities. Such
continental dimensions harbor native cultures (Amerindians), adapted riparians (locally called ‘‘ribeirinhos’’),
and large cities. More recently, free expansion of
agricultural areas and a gold rush in the 1970s attracted
small- to medium-sized human settlements. In Brazil,
densely populated cities such as Manaus, Belém, and
Fax: +55-61-368-5853.
E-mail address: [email protected].
other state capitals contrast with a population dispersed
throughout the forest or in small communities along the
riverbanks. The Amerindians and ribeirinhos, each with
distinct cultures, share the same forest environment.
Natural resources in the Amazon rain forest and its
surrounding environment directly affect human habitation. Nutritional ecology in the Amazon rain forest has
been described for Ameridians (Dufour, 1992), while
Murray and Sanchez-Choy (2001) described the livelihood strategies of Amazonian frontier communities.
These strategies involve synchronization with a constantly changing flood plain and upland forests to
guarantee survival and health, through nutritional
status and food security.
The Amazonian rivers have a hydrological cycle
controlled by the rainy season that extends from
October to April and can raise the water level from 8
to 15 m in parts of western Amazonia. This monumental
0013-9351/03/$ - see front matter r 2003 Elsevier Science (USA). All rights reserved.
doi:10.1016/S0013-9351(02)00092-0
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J.G. Dorea / Environmental Research 92 (2003) 232–244
landscape change dictates availability of forest foods
and pattern of diseases. Dietary and migratory patterns
of fish and other animals and agricultural cycles require
a successful food-securing strategy. The bulk of the
riparian population’s diet is provided by starchy roots,
mainly cassava (Manihot spp). The cassava tuber is
made into many food items, especially easily stored
flour. Its starch is a potential cariogen (Rosalen et al.,
1997) and has been associated with a high incidence of
dental cavities (Normando and de Araujo, 1990), but its
content of linamarin has never been a health problem in
Amazonia. The protein that complements the lowcalorie starchy foods is derived mainly from fish that
naturally accumulates monomethyl mercury (MMHg).
After the gold rush of the last 30 years, fish have been
considered impacted by Hg discharges and therefore a
toxic risk. In keeping with current scientific opinion and
as a consequence of monitoring Hg in the fish-eating
riparians, there are constant warnings of potential
health problems and suggestions that Hg contamination
could be reduced by changing the pattern of fish
consumption in these communities.
For indigenous populations of Alaska, Egeland and
Middaugh (1997) called attention to balancing the
benefits and risks of fish consumption in those latitudes.
Aspects of the interaction between toxin-bearing foods
(cassava and fish) are reviewed here to demonstrate the
compelling evidence for the importance of fish for health
benefits in the ecology of food and nutrition of
Amazonian riparians.
2. Neurotoxins in cassava and fish
Cassava has a low protein content (Nassar and
Dorea, 1982) but substantial amounts of cyanogenic
glucosides such as lotaustralin and, mainly, linamarin.
These naturally occurring substances are hydrolyzed to
hydrogen cyanide (CN), a potent neurotoxin, and have
to be destroyed by processing before consumption. The
content of linamarin in the roots and leaves depends on
the cassava species/variety, but in their by-products it
depends on the thoroughness of detoxification. Dufour
(1989) gives a brief description of these processes, which
consist of soaking the roots in the river for approximately 3 days, followed by grating or peeling. After
peeling, the soft, water-soaked roots are squeezed in
cloth or left to dewater in basketry sleeves. The
enzymatic action of the linamarinase present naturally
in the plant and the hydrolysis occurring after manipulations form CN. Depending on the final product, the
cassava dough is dried, fermented, or pan-baked. In
animals, residual CN is converted into thiocyanate, a
potent goitrogen that requires cysteine- and sulfurcontaining amino acids in its detoxification mechanisms
(Tor-Agbidye et al., 1999). Chronic CN poisoning is
233
responsible for endemic tropical ataxic neuropathy
(TAN) and aggravation of iodine-deficiency disorders
(IDD) (Onabolu et al., 2001).
Cassava linamarin can be greatly reduced by plant
variety choice and detoxification processes (Dufour,
1989). Depending on the plant variety, total CN
concentrations can range from 230 to 1609 ppm dry
matter (Dufour, 1988a). On the other hand, MMHg is
bioaccumulated in fish along with other substances
present in the aquatic environment (Lewis et al., 2002).
Predatory fish from lakes in industrial regions and
large oceanic fish tend to accumulate other toxic
metals such as As and lipophillic organochlorine (OC)
pollutants including dichlorodiphenyldichloroethylene,
polychlorinated biphenyls, polychlorinated dibenzo-pdioxins, and polychlorinated dibenzofurans (Svensson
et al., 1995). Industrial activities in Amazonia are
restricted to specific urban locations and there are
no studies of OC concentrations in Amazonian fish.
With regard to the impact of neurotoxic metals on
cassava, Amonoo-Neizer et al. (1996) determined Hg
and As in both cassava and fish in an area of Ghana
impacted by a mining plant using As in gold extraction. A trend of decreasing concentration of As in
cassava with increasing distance from the gold-processing plant was observed. The authors concluded that
cassava appeared to be an excluder of arsenic and
mercury.
Mercury occurs naturally in the environment in three
oxidation states (Hg0, Hg1+, Hg2+) and is widespread
due to a series of complex chemical transformations.
Methylation by microorganisms forms MMHg, the
most important step for Hg entry in the aquatic food
chain. As MMHg, it is bioconcentrated in the trophic
food chain of fish and other aquatic organisms. Natural
Hg release and methylation potential of ecosystems are
associated with geochemistry and complex human
activities, especially deforestation, agricultural land use
(Roulet et al., 1999), and gold mining activities (as
discussed below). Mercury acquisition, accumulation,
and biomagnification by fish are associated with the Hg
chemical form and fish physiology. Organic Hg in fish
constitutes an important contaminant that causes human neuromotor disturbances and neuropathies under
special circumstances. As summarized by Clarkson
(1998), the episodes of Minamata and Niigata represent
the most dramatic form of MMHg poisoning through
contaminated fish caught in a industrially polluted area
of Japan. Acetaldehyde plants were the source of
preformed MMHg that accumulated in fish in excess
of 20 mg/g (Clarkson, 1998).
Summing up, two potent neurotoxins are naturally
present in the Amazonian diet. However, while traditional technologies are effective in eliminating linamarin
(Dufour, 1989), detoxification of MMHg by industrial
(Aizpurua et al., 1997) or common (Armbruster et al.,
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J.G. Dorea / Environmental Research 92 (2003) 232–244
1988; Chicourel et al., 2001) cooking methods has been
proven ineffective.
3. Mercury accumulation in Amazonian fish
The inorganic Hg discharged during alluvial goldmining activities raised a legitimate interest in environmental damage and Hg pollution. Although the
environmental damage is enormous, with disruption
and destruction of aquatic ecosystems (Kligerman et al.,
2001), the Hg balance showed that the metal discharge
from gold-mining activities accounts for less than 1%
(Fadini and Jardim, 2001). The mercury pool in the top
layer of the Rio Negro’s basin surface soil is nearly
126 103 tons (Fadini and Jardim, 2001). Furthermore,
agricultural developments (which also occurred in the
1970s and 1980s) with deforestation, equally environmentally disruptive, may indeed have impacted on the
release of Hg from soil (Roulet et al., 1999). However,
studies of fish Hg concentrations indicate that Hg
released from gold-mining activities have not yet
impacted on fish MMHg (secondary or tertiary consumers) concentrations (Table 1). So far, there have
been no studies attempting to disentangle the role of Hg
released during gold-mining activities (inorganic) or
from soil (organic and inorganic) on Hg methylation
and its travel through the Amazonian food chain.
Assumptions made on ‘‘Hg pollution’’ due to goldmining activity and a gradient of fish Hg concentration
were proposed for the Rio Tapajós (Uryu et al., 2001),
which has a 420-year history of intense gold-mining
activity. Table 1 summarizes fish Hg concentrations
from all over Amazonia. The ranges of mean Hg
concentrations in fish from the Rio Tapajós are not
systematically higher than those in fish from other rivers
(Table 1). The range of fish Hg means categorized by
fish food strategies from rivers with no history of gold
mining (i.e., Rio Negro) are even higher than those from
intensely mined rivers (i.e., Rio Tapajós, Rio Madeira).
The Hg concentrations of fish species caught in
Amazonian rivers are comparable to Hg concentrations
in oceanic fish caught and sold in southern Brazil. In
oceanic species of secondary and tertiary consumers, the
Hg concentrations ranged from 19 to 1493 ng/g
(Chicourel et al., 1995). Barbosa et al. (2003) showed
that fish Hg is highest in the Rio Negro (not impacted
by gold mining) and is modulated primarily by the food
chain structure. Also, hair Hg in fish-eating riparians of
the Rio Tapajós (which had the most intense goldmining activities) are within comparable ranges for
other Amazonian locations (Lodenius and Malm, 1998;
Barbosa et al., 2001). Furthermore, Tsugane and Kondo
(1987) compared hair Hg of Japanese immigrants living
in various countries of South America and reported that
they maintained their fish-eating habits in their new
countries and showed comparable hair Hg in all
countries studied, even in Bolivia where they consumed
fish from the head waters of the Madeira River. SilvaForsberg et al. (1999) found that the levels of hair Hg of
Negro River riparians were positively correlated with
river-dissolved organic carbon.
4. Dietary neuropathies in Amazonia: cyanide and
mercury
Cassava is implicated in certain types of nutritional
disorders all over the world. In Africa TAN reaches
epidemic proportions due to cassava cyanogenic substances or to its incomplete detoxification (Onabolu
et al., 2001). In protein-deficient populations of Africa,
neurological disorders attributed to CN exposure due to
eating cassava are exacerbated by a lack of sulfur amino
acids (Tor-Agbidye et al., 1999). IDD and congenital
cretinism are endemic nutritional diseases in Africa and
are aggravated by high intakes of cassava goitrogens
and by selenium deficiency. Indeed, different patterns
of thyroid function and goiter were observed in two
populations with a minute difference in iodine deficiency. The dietary differences involved milk consumption and lower ingestion of cassava in the population
with the lower incidence of IDD (Biassoni et al., 1998).
Thiocyanate overload originating from the consumption
of poorly detoxified cassava is considered a contributing
factor in increased rate of goiter (Abuye et al., 1998) and
growth retardation in children (Banea-Mayambu et al.,
1997). In southeast Asia, the goitrogenic effect of
cassava consumption was overcome by iodine supplementation (Hershman et al., 1983). Also in Reunion
Island cassava consumption was associated with goiter
incidence and distance from coast (Jaffiol et al., 1991).
Thilly et al. (1992) reported that a severe selenium
deficiency was associated with IDD. In a poor area of
southeast Nigeria there was an association between
impaired glucose tolerance and dietary cyanogens
(Akpan and Gingerich, 1991). However, Dufour
(1992), citing secondary sources, emphasized that goiter
has not been reported in any Amazonian Amerindians
living on cassava-based diets.
Cassava and other starchy roots are important staples
in Amazonia, but disastrous effects of its consumption
on the central nervous system (CNS) and the thyroid,
such as those reported for Africa (Roman et al., 1985),
have not been detected in the region. The potential harm
from thiocyanate exists in many parts of the world, and
neuropathies of dietary origin other than fish or cassava
consumption are demonstrable in Amazonia. Myelopathies due to thiamin deficiencies were found among the
Noir-Marron, a community in French Guyana where
cassava is a staple food (Sainte-Foie et al., 1997).
Changes in dietary patterns of Amazonian autochthons
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235
Table 1
Summary of reported mean Hg concentrations (ng/g) in muscle of fish caught in fresh waters of the Amazon rain forest
River basins/references
Piscivorous species
Nonpiscivorous species
Range
Local name
Range
Local name
510–1390
Tucunaré, Pescada
100
Acará
110–610
Tucunaré, Traı́ra
30–210
Acará, Cachorrinho de Padre,
Traı́ra, Pacú, Piaba
(240–650)
130–700
320
410–2600
Tucunaré, Traı́ra, Piranha,
Tucunaré, Cachorro, Piranha
Tucunaré, Cachorro, Piranha, Traı́ra
Tucunaré, Piranha, Pescada
60
60
60–390
Acará-Tinga
Acará
Piau, Curimata, Piaba
230–1340
Cara-Acú, Filhote, Piranha,
Cachorro, Pescada, Jacundá, Apapa,
Surubim, Barba Chata, Tucunaré,
Bico de Pato, Jejú, Piramitaba,
Dourada, Jandirá, Capararı́, Traı́ra,
Pirarucu
ND–1440
Boischio et al. (1995)
220–740
Piranha, Barba-Chata, Dourada,
Tucunaré
100–1900
Kehrig and Malm (1999)
570
150–180
Lechler et al. (2000)
Malm et al. (1995)
Maurice-Bourgoin et al. (1999)
Maurice-Bourgoin et al. (2000)
280–420
700
(806–1819)
49–1522
130
(8–31)
9–94
NG
Pacu, Tucunare
Jatará, Tambaqui, Pacu
Pfeiffer et al. (1989)
Pfeiffer et al. (1991)
70–2,700
70–2700
210
80–210
Curimata
Curimata, Jaturarama
Reuther (1994)
320–1330
Tucunaré, Cachorro, Piranha,
Mapara,
Matrixa
NG
Cachoro, Pintado, Bagre
Cachorro, Bagre, Dourado, Pintado,
Surubim
Pintado, Pirarucu, Dourado, Filhote
Pintado, Pirarucu, Dourado,
Filhote, Tucunaré
Tucunare, Pintado, Piranha, Peixe
Cachorro, Apapa, Traira, Dourado,
Filhote
Tamoatá, Cascudo, Jaraquı́,
Curimatã, Bodo, branquinha,
Ubarana, Mapara, Cubiu, Mandi,
Cara, Cuiu-cuiu, Sardinha, Aruana,
Pintadinho, Pirarara, Aracu,
Matrinxã, Pacu, Bacu, Pirapitinga,
Jatuarana, Tambaqui
Aruanã, Mandi, sardinha, Aracú,
Cará, Jatuarana, Pacú, Pirapitinga,
Tambaquı́, Curimatã, Jaraquı́,
Cascudo, Branquinha
Pacu, Sardinha, Piau, Branquinha
80–490
Mapara, Acara, Mandi, Cascudo,
Curimata
Amazon river
Eve et al. (1996)
Gurupi/Macaco/Piriá
Palheta and Taylor (1995)
Lakes and reservoirs
Guimaraes et al. (1999)a
Kehrig et al. (1998)b
Kehrig and Malm (1999)b
Porvari (1995)c
Madeira river
Boischio and Henshel, 2000
Negro
Kehrig and Malm (1999)
Pantanal
Alho and Vieira (1997)
Hylander et al. (1994)
Hylander et al. (2000)
Kehrig and Malm (1999)
Paraná
Moraes et al. (1997)
Tapajós river
Akagi et al. (1995)
610
Tucunaré, Aruanã, Cachorro,
Piranha
90
Branquinha, Cará, Aracú
1040–
12,310
120 540
76–813
70–120
Piranha, Surubim, Pescada, Traı́ra
7780
Mandi
Pintado
Surubim, Pintado, Piranha
Piranha, Bagre, Traı́ra
68–189
Surubim
—
—
80–3820
Dourada, Jaú, Piraı́ba, Mandubé,
Cachorro, Traı́ra, Apapa, Pescada,
Tucunaré, Filhote, Pirarucú
Tucunaré, Piranha, Cachorro,
Surubim, Jacundá, Mandi, Pescada,
Traı́ra, Piracmuntaba
Barbado, Surubim, Traı́ra,
Tucunaré, Aruana
Apapá, Cachorro, Dourada, Filhote,
Jacundá, Mandi, Pescada,
Piramutaba, Saranha, Piranha,
Surubim, Traı́ra, Tucunaré
Piraiba Jau, Pescada, Pintado,
Dourada, Traı́ra, Piranha, Tucunaré
100–280
Acará, Aruana, Pacú
37–100
Acaratinga, Aracu, Matrinxã, Pacu,
Jaraqui
93–120
12–149
Caratinga, Jaraqui, Aracu, Mandiá,
Jandiá, Pacú
Acará-A,cu, Acará-Tinga, Aracú,
Curimatã, Jaraqui, Mapara,
Matrinxã, Pacu, Tambaqui
80–80
Pacu, Curimata
Bidone et al. (1997a)
100–690
Brabo et al. (2000)
174–419
Castilhos et al. (1998)
60–690
Hacon et al. (1997)
280–2750
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J.G. Dorea / Environmental Research 92 (2003) 232–244
Table 1 (continued)
River basins/references
Piscivorous species
Nonpiscivorous species
Range
Local name
Range
Local name
Hacon et al. (2000)
Kehrig and Malm (1999)
Lebel et al. (1997)
300–1000
140–810
90–800
10–170
50
40–400
Pacú, Matrinxã, Curimatã
Aracú
Aracú, Caratinga, Pacú, Caraucu,
Mandubé, Saranha, Sardinha
Santos et al. (2000b)
375–839
51–121
Curimatã, Aracú, Pacú, Tambaqui
Santos et al. (2000c)
Souza Lima et al. (2000)
529
125–306
106
30–69
NG
Pacú, Pirapitinga, Tambaquı́, Aracu
Uryu et al. (2001)
92–2348
Tucunaré, Jaú, Pintado
Tucunaré, Traı́ra
Apapá, Barbado, Filhote, Mandi,
Pescada, Piracatinga, Piranha,
Sarda, Surubim, Jiju, Tucunaré,
Jacunda, Dourada, Cachorro,
Traı́ra, Pirarucu
Dourada, Filhote, Surubim,
Pescada, Tucunaré, Sarda
NG
Dourada, Cachorro, Pescada,
Piranha, Sarda, Surubim, Tucunaré
Apapa, Peixe-cachorro, Traira,
Pescada, Piranha, Piramutaba,
Barbado, |Piraiba, Pirarucu, Jau,
Tucunaré, Dourado, Mandube,
Pintado
8–930
Caratinga, Cabeca-gorda, Piau,
Curvina, Mapara, Aruana, Acari,
Jaraqui, Pacu, Tambaqui,
Branquinha, Aracu, Curimata
Tartarugalzinho
Bidone et al. (1997b)
305–742
Tucunaré, Piranha, Pirarucu,
Aruanã, Ituı́, Jacunda, Jeju, Uena
35–1225
Aracu, Cachorro de Pedra, Cara,
Manduba, Matrinxã, Pacu Branco,
Taumatá
Tocantins
Lacerda et al. (1994)
130–1560
Traı́ra, Cachorro, Jaú, Piranha
10–160
Matrinxã, Pacú Branco
( ), Individual values.
NG, not given.
a
Duas Bocas and Pracaúba.
b
Balbina Reservoir.
c
Tucuruı́ Reservoir.
resulting in polyneuropathy were reported by Vieira
Filho et al. (1997). Ecological factors seem to protect the
Brazilian Amazonians consuming cassava. In addition
to the effectiveness of cassava detoxification, the
abundance of animal protein (fish included) may protect
Amazonians against residual CN. In Africa, CN load
due to cassava consumption is more health threatening
(Onabolu et al., 2001).
With regard to fish consumption and Hg toxicity,
Clarkson (1995) suggested that raising plasma amino
acids from digestible fish protein increases levels of
leucine, methionine, phenylalanine, and other large
neutral amino acids that might inhibit MMHg entry
into the brain. He argues that in chronic exposure of
naturally bioaccumulated fish MMHg, defense mechanisms involving the enterohepatic cycle favors MMHg
conversion to inorganic Hg, thus facilitating its depuration.
The lack of Minamata-like symptoms in the Amazonian riparians (Boischio and Barbosa, 1993; Santos
et al., 1999, 2000a, 2002), challenged by a large daily
intake of Hg naturally present in fish consumed over a
lifetime, is compatible with Clarkson’s (1995) observation that fish-eating populations around the world
shows no clear-cut case of MMHg poisoning. Contrary
to this, Harada et al. (2001) claimed that in an
Amazonian region impacted by gold-mining activity
(Rio Tapajós), three of 132 subjects were diagnosed with
‘‘mild Minamata disease (tremor, failure in two-point
discrimination, slight balancing failure, and especially
glove-and-stocking-type sensory disturbance).’’ One of
the three subjects was occupationally exposed to
inorganic Hg in the 1960s. Fish-eating communities of
the Rio Tapajós were studied previously by others. No
clinical symptoms associated with MMHg poisoning
(Minamata disease) were observed in subjects with mean
hair Hg of 13.76 mg/g (Santos et al., 1999) or even
20.96 mg/g (Santos et al., 2000a) acquired from fish
consumption. However, this group of investigators
(Santos et al., 1995) reported that among occupationally
Hg-exposed subjects (in gold-mining settlements), 22
of 25 patients with urinary Hg above 10 mg/L showed
symptoms compatible with Hg poisoning. Riparians
of the Rio Madeira showed a prevalence of 3% of hair
Hg above 50 ppm (Boischio and Barbosa, 1993) but no
signs of Minamata disease.
Kligerman et al. (2001) reported that in gold-mining
settlements fish is not consumed due to the belief that
it is ‘‘Hg-contaminated.’’ In these communities, there
was also a high incidence of hepatitis, malaria, syphilis
(which can cause neurologic disorders), and other
sexually transmittable diseases (Santos et al., 1995).
Therefore, fish as an Se-rich food is not consumed and
vulnerability to inorganic Hg toxicity could increase.
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Indeed, symptoms of Hg toxicity were found among
those working in or living near the mining and refining
industry (Aks et al., 1995).
5. Safety of cassava and fish consumption in Amazonia
The Amazonian riparians depend heavily on cassava
and fish to meet their nutritional needs and are exposed
to naturally occurring cyanogenic glucoside (in cassava)
and MMHg (in fish). Although potentially harmful,
cassava consumption in Brazil was never associated with
neuropathies or thyroid diseases, except for an isolated
case of paraparesis (Carod-Artal et al., 1999). However,
endemic beriberi in a well-nourished community of
Ecuadorian Amazonians was suspected as being related
to cassava consumption (San Sebastian and Jativa,
1998). Although there are no reports of CN or
thiocyanate surveys in Brazilian riparians, there are
several surveys of Hg body load. After the gold rush of
the 1970s and 1980s, the interest in Hg contamination
resulted in studies of hair Hg due to occupational
exposure (inorganic Hg) and fish consumption (organic
Hg).
In impacted and nonimpacted areas of Amazonia,
hair Hg is always higher in fish eaters than in
occupationally exposed workers (Barbosa et al., 1995).
However, despite several reports showing mean hair Hg
above threshold levels of 10 gm/g hair (Lodenius and
Malm, 1998; Barbosa et al., 2001), the typical symptoms
of Minamata disease were never diagnosed in fish-eating
riparians even with extreme values of 303.1 mg/g hair
(Boischio and Barbosa, 1993). Nevertheless, almost all
papers warn of potential risk of Hg contamination
through fish consumption. Because of the public outcry
caused by physical destruction of ecosystems and huge
discharges of metallic Hg, it was perceived that the
discharged metal would find its way into the aquatic
food web, ultimately posing toxic risks for the fisheating riparians.
Reports testing psychomotor-impairment effects suggested an association with hair Hg (o50 mg/g) due to
fish consumption in adults from the Tapajós Basin
(Lebel et al., 1996, 1998; Dolbec et al., 2001). Behavioral
and neurophysiological tests consisted of color discrimination capacity, nonvisual contrast-sensitivity profiles, peripheral visual field profiles, and grip strength
(Lebel et al., 1996, 1998; Dolbec et al., 2001). In the
same region (Tapajós Basin), Grandjean et al. (1999)
examined visiospatial domain, attention, and motor
function in 252 children (7–12 years old) and found a
significant association between the measurements of
neurobehavioral performance and the hair Hg concentration.
Subtle disturbances of neuromotor development,
performance, and cognition have been extensively
237
studied in populations consuming seafood. Associations
of prenatal MMHg exposure with neuromotor disturbances were found in some studies, whereas others have
found none (Myers and Davidson, 2000). Myers et al.
(2000) summarized studies carried out in Samoa, Peru,
and the Seychelles showing no evidence that consuming
large quantities of fish is associated with adverse effects
on adults or children. The advantages of breast feeding
have outweighed any possible adverse effect of breast
milk Hg in fish eaters of developed societies (Grandjean
et al., 1995) and it is likely to be of more benefit in these
isolated communities of Amazonia living in unsanitary
conditions, with high levels of intestinal parasites and
malnutrition.
Kosatsky and Foran (1996) discussed the lowest
observable effect level for MMHg in adults of fisheating populations. They concluded that no clear-cut
case of Minamata disease had been described and that
there was no demonstrable threshold tissue level above
which any form of neurologic dysfunction occurred.
Neurological effects were seen in children of poisoned
Iraqi mothers with hair-Hg concentrations as low as
20 ppm while in ocean fish eaters of Peru maternal hair
levels of methyl mercury between 1.2 and 30 ppm
showed no effect on infant neurological assessment.
Marsh et al. (1995) attributed these differences to
protective nutrients in the fish diet of Peruvian mothers
that were absent in the Hg-poisoned grain consumed by
Iraqi mothers.
The cassava processing techniques traditionally used
by Amazonian forest people are sophisticated and
effective in reducing cyanohydrin concentrations
(Dufour, 1988b, 1989). The residual CN content of
prepared cassava can range from 0 to 50 ppm in
cultivars of bitter (brava) cassava (Manhitot esculenta
Crantz). Studies indicate that the processing of cassava
products is more effective in Amazonia (0.4–14.6% of
residual CN) than in Africa (Dufour, 1989). Cyanide
intake by Tukanoans (northwest Amazonia) exceeds
20 mg/day and the high levels of its exposure biomarker
(serum thiocyanate; 180 mmol/L) are not associated with
neurologic or thyroid disorders (Dufour, 1988b). However, in hot and humid climates dietary contamination
with aflatoxins produced by A. flavus and A. parasiticus
is ubiquitous. Indeed hepatocarcinogenicity by aflatoxin
has been established in a case report attributed to
consumption of moldy cassava elsewhere (IARC-WHO,
1993; Crews et al., 2001). In Amazonia (French Guyana)
moldy cassava was speculated as being linked to the
unknown etiology of ‘‘fievre noire Amazonienne’’ (Le
Pelletier et al., 1970). Vis-a-vis with fish, cassava is by far
potentially more harmful. Nevertheless, Amazonian fish
is starting to appear in some environmental studies as a
toxic risk (Kazantzis, 2002; Fields, 2001; Yallouz et al.,
2002), although without evidence to support such
claims. In the absence of evidence of toxic risks, there
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J.G. Dorea / Environmental Research 92 (2003) 232–244
is compelling evidence that fish are important to
counteract possible CN residues in cassava and as a
wholesome nutritional complement to starchy foods.
6. The role of fish in the Amazonia’s diet
Fish are not only natural bioconcentrators of MMHg
but are also good sources of nutrients. As a staple food,
fish are the main providers of nutrients that in the
Amazonian forest environment can ameliorate nutritional deficiencies. Fish constitute a fundamental
complement for natives consuming 70–80% of dietary
energy from cassava (Dufour, 1988c; Wilson and
Dufour, 1999). The high protein content of fish is well
digested and has a high biological value, thus balancing
the protein-poor starchy food (Araujo et al., 1975).
The highly available lysine of fish is comparable to
milk protein (Batterham et al., 1979) and is ideal to
complement lysine-poor cereal grains (Costa et al.,
1990). In fact, compared to powdered skim milk, small
fish have five times more Cu, twofold higher Ca content,
and two orders of magnitude more Zn, Fe, and Mn
(Larsen et al., 2000). Fish flesh can enhance absorption
of Zn (Garcia-Arias et al., 1993) and Fe (Glahn et al.,
1996). Indeed, human absorption studies have shown
that fish promotes the absorption of nonheme Fe in
food (Bjorn-Rasmussen and Hallberg, 1979). Human
studies have shown also that small fish Ca is absorbed as
well as milk Ca (Hansen et al., 1998) and its frequent
consumption by Japanese women is associated with
greater bone mineral density (Ishikawa et al., 2000) and
higher levels of vitamin D (Nakamura et al., 2000).
According to Inhamuns and Franco (2001), Amazonian
fish contain omega-3 polyunsaturated fatty acids
(PUFA; decosahexanoic [22:6] acid (DHA) and eicosapentaenoic [20:5] acid).
In typical western diets, daily iodine intake is supplied
mainly by dairy products (37%), meat (27%), and bread
and cereals (18%), with fish accounting for 9% (Jahreis
et al., 2001). Neither dairy nor wheat products are part
of the riparians’ diet. Consumption of game and
domestic animals is frequent but given the indices of
hair Hg (signature of fish consumption), fish may be an
important source of iodine. In addition to being good
sources of sulfur amino acids, fish are associated with a
higher bioavailability of iodine in cassava-based diets
(Toure et al., 2001). Both nutrients may counterbalance
goitrogens (in cassava) and low iodine of foods
produced in iodine-depleted soils of tropical rain forests.
Indeed, fish consumption is positively correlated with
women’s iodine status (Zollner et al., 2001).
Fish are also important sources of omega-3 PUFA
which are important in the maternal diet during
pregnancy and lactation (Rice, 1996). An increased
intake of marine fats appears to prolong the duration of
gestation (Grandjean et al., 2001), and Olsen and Secher
(2002) reported that low consumption of fish in
Denmark was a strong risk for preterm delivery and
low birth weight. Fish intake was correlated positively
with the DHA level in breast milk in Sweden (Jorgensen
et al., 2001) and in Congolese mothers (Rocquelin et al.,
1998). Maternal supplementation with dietary fish oil
significantly increased the PUFA content of breast milk
(Moya et al., 2000) which affects stereopsis and
stereoscopic vision in breast-fed children (Williams
et al., 2001). In adults reporting high fish intake,
erythrocyte Hg (biomarker of fish intake) and plasma
PUFA were high and associated with decreased risk of
a first myocardial infarction (Hallgren et al., 2001).
Reduced cardiovascular risk (Mizushima et al., 1997)
and thrombotic infarction (Isso et al., 2001) in women
were associated with intake of fish and omega-3 PUFA.
However, studies in Finland indicate that Hg in fish may
cancel such effects by accelerating lipid peroxidation
(Salonen et al., 1995; Rissanen et al., 2000). The
traditional life-style of Amazonian Amondavas, compared with Africans, Italians, and Polish, seems to
protect them against the development of hypertension,
hypercholesterolemia, and diabetes (Pavan et al., 1999).
Furthermore, transition from a rural to an urbanized
life-style is accompanied by a rise in cardiovascular risk
factors (Pavan et al., 1997).
As dietary components fish are superior to other
animal products (meat, dairy products, eggs) and
vegetables in providing Se intake (Klapec et al., 1998).
Plasma Se is also correlated with fish intake (Svensson
et al., 1992) and Amazonian fish are good sources of
selenium (Dorea et al., 1998), known to counteract the
toxic effects of Hg. Experimental results show that
toxicity of Hg is reduced by administration of Se,
thereby forming a complex between plasma protein and
these two elements (Yoneda and Suzuki, 1997; Gailer
et al., 2000). As reflected in Se concentrations of Brazil
nuts, there are substantial differences in soil Se
concentrations that can vary from west (3 ppm) to east
(36 ppm) of Brazilian Amazonia (Chang et al., 1995) and
hence fish can be a stable source of dietary Se. Recently,
a significant correlation between Hg and Se in hair
was reported in Amazonians (Vasconcellos et al., 2000;
Campos et al., 2002).
Reports from several parts of the world emphasize the
role of fish in maternal diets to provide good-quality
protein (essential amino acids) and essential nutrients.
Fish have a positive impact on the quality and nutrient
enhancement of a family’s diet, especially in women and
children. Neumann et al. (2002) reviewed studies
showing that maternal intake of animal products during
pregnancy predicted gestational age and pregnancy
weight gain and were positively associated with infant
growth beginning in utero, birth weight, and birth
length. Children also greatly benefit from inclusion of
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J.G. Dorea / Environmental Research 92 (2003) 232–244
animal products in their diet. Intakes of available iron,
zinc, and iodized salt were statistically significant
predictors of growth. Intake of animal protein (meat,
fish) showed a positive and statistically significant
relationship to height in studies in New Guinea and in
South and Central America (Neumann et al., 2002). In a
community of indigenous Malay that depended on fish
and cassava, goiterous women had significantly lower
protein and energy intake compared with nongoiterous
counterparts (Cuthbertson et al., 2000).
The beneficial effects of fish consumption also impacts
on the health of an affluent population. Fernandez et al.
(1999, 2000) speculated that degenerative diseases such as
cancer (certain types) and Alzeimer’s disease were inversely
associated with fish consumption. Studies suggest that the
risk of prostate cancer is reduced with the intake of
long-chain n-3 polyunsaturated fatty acids derived from
fish (Norrish et al., 1999; Kobayashi et al., 1999).
Bartram et al. (1995) reported that fish oil in a low-fat
diet caused a decrease in rectal cell proliferation. Bosetti
et al. (2001) reanalyzed data from studies conducted
in the United States, Japan, China, and Europe. The
combined analysis indicated that elevated fish consumption
did not appreciably increase thyroid cancer risk, but may
have had a favorable influence in areas where iodine
deficiency was common. Biomarkers of fish intake by
immigrant Japanese in Brazil and the United States are
candidates for the prevention of chronic noncommunicable
diseases (Yamori et al., 2001). There are also studies
showing beneficial effects of fish consumption on mood,
low depressive episodes, and suicide rates (Tanskanen
et al., 2001) and a lack of seasonal mood (Cott and
Hibbeln, 2001).
In summary, minimizing MMHg exposure in riparians is equivalent to curtailing fish consumption, thereby
indicating that such a procedure is neither practical nor
beneficial. Fish are an abundant natural resource in
Amazonia with no dietary substitute.
7. Should we worry about Hg concentrations in
Amazonian fish?
Exposure to environmental chemicals does not occur
in isolation in industrially polluted areas. In the case
of Amazonia, artisanal gold extraction from alluvial
deposits is carried out after amalgamation with metallic
Hg which has not yet been shown to systematically
increase fish Hg concentrations (Table 1). The methods
used for alluvial gold mining in Amazonia involve the
hydraulic dismounting of river terraces and dredging
work on watercourses. In hydraulic dismount, the
miners use water jets to remove land strips, while in
watercourses, pumps are used to suck up the river sand
bedding. Mercury is used to improve gold recovery by
amalgamation and all discarded material goes into
239
rivers, causing turbidity and shoaling (Kligerman et al.,
2001). In other areas of South America, gold extraction
is also carried out with NaCN, which is showing a
devastating toxic effect on river biota and signs of
toxicity in the human population living along impacted
rivers (Tarras-Wahlberg et al., 2001).
Access to medical services is restricted in the
continental extensions of the Brazilian Amazonia as
such services are located in urban centers often a few
days journey away. Seasonal flooding isolates vast areas,
thus making its inhabitants vulnerable to gastrointestinal parasites and endemic tropical diseases (Santos
et al., 1992). For Amazonian riparians, nutritional
status depends on the family’s ability to secure food
during the hydrological cycle. This is guaranteed
mainly by starchy roots making up the bulk of diet,
with fish as the main source of protein and essential
nutrients. Consumption advisories for fish Hg must be
part of our constant effort to maintain high standards of
food safety. However, in this context of human
ecology, there are more urgent medical needs and public
health problems than possible risks of asymptomatic
neuromotor deficits which to date are from nonspecific
causes.
A successful interaction between food and nutrition in
the adaptive survival strategy of riparians is exemplified
by cassava and fish. Therefore, in this scenario of
insufficient health services and unhealthy environment,
food habits based on fish consumption are part of a
successful survival strategy and recommendations for
changes are not yet justifiable.
8. Conclusions
Eating fish certainly increases hair Hg concentrations,
but there is no hard evidence that in the last 20 years
there has been an increase in fish Hg or in hair Hg of
Amazonian riparians.
For the Amazonian riparians there is no proven
predisposition for degenerative CNS diseases associated
with lifetime consumption of naturally occurring toxins
in either cassava or fish.
The susceptibility of TAN and the aggravation of
IDD (due to cassava consumption) reported in other
parts of the world seem to be associated with undernutrition or lack of essential nutrients that in Amazonia
are provided by fish.
Biomarkers of exposures, to CN (serum thiocyanate)
from cassava or to MMHg (hair Hg) from fish, have
not yet been shown to predict clinically recognized
neuropathies in Amazonian riparians.
Fish per se are the best sources of essential nutrients
and are an abundant natural resource for the Amazonian riparians.
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Dietary changes in fish consumption that might
disrupt the metabolic adaptation through macro- and
micronutrient acquisitions are inappropriate.
Acknowledgments
I thank Dr. Connie McManus for redactorial suggestions.
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