Hair mercury (signature of fish consumption) and cardiovascular risk in Munduruku and Kayabi Indians of Amazonia
Introduction
Fish is a nutritious and important dietary staple of the people of the Amazonian rain forest. It is an abundant natural resource that is rich in high-quality protein, lysine, iodine, sulfur-containing amino acids, copper, calcium, zinc, iron, manganese, selenium, and omega-3 polyunsaturated fatty acids, among others. In the Amazonian rain forest, fish supply much needed protein and provide a balance to starchy food-staples such as yam, cassava, and plantain (Araújo et al., 1975). Fish is high in lysine in amounts comparable to milk protein (Batterham et al., 1979) and is an ideal complement to lysine-poor cereal grains. In cassava-based diets, fish consumption is associated with high bioavailability of iodine (Toure et al., 2001) and is positively correlated with the iodine status of women (Zollner et al., 2001). In tropical rain forests where soils and foods are iodine poor, fish provide much need iodine. Moreover, fish is a good source of sulfur-containing amino acids. Both sulfur and iodine may counteract goitrogens found in cassava (Tor-Agbidye et al., 1999). Compared to powdered skim milk, small fish have fivefold more Cu, twofold higher Ca, and two orders of magnitudes more Zn, Fe, and Mn (Larsen et al., 2000). It is known that zinc levels are significantly higher in protein-rich food like 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 of selenium (Dórea et al., 1998), a nutritional element known to counteract the toxic effects of Hg. It was recently observed that S-containing amino acids in fish are central to detoxification of high concentrations of neurotoxins in cassava (linamarin), the dominant source of energy for Amazonians (Dórea, 2004). Besides all of their nutritional uses, fish are used medicinally by inhabitants of the Amazon (Begossi et al., 2000).
In addition to protein, minerals, and vitamins, fish provide beneficial fats. Fish is an important source of omega-3 polyunsaturated fatty acids (e.g., PUFA; decosahexanoic [22:6] acid (DHA), eicosapentaenoic [20:5] acid), which have been proven to play an important role in the prevention of coronary heart diseases (Albert et al., 2002). In adults reporting high fish intake, erythrocyte Hg (a biomarker of fish intake) and plasma PUFA were found in high levels and were associated with decreased risk of the occurrence of a first myocardial infarction (Hallgren et al., 2001). Fish and omega-3 PUFA were associated with reduced risk of cardiovascular disease (Mizushima et al., 1997) and thrombotic infarction in women (Isso et al., 2001). Marckmann and Gronbaek (1999) concluded that fish consumption of 40–60 g daily is associated with markedly reduced coronary heart disease mortality in high-risk populations. There is a lack of data on omega-3 polyunsaturated fatty acids composition of freshwater fish of the Amazon. According to Inhamuns and Bueno Franco (2001), omega-3 polyunsaturated fatty acids were found in mapara (Hypophthalmus spp.). However, the beneficial effects of fish consumption on the cardiovascular system are not only due to the omega-3 fatty 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 challenged because fish contains mercury, which is known to adversely affect the cardiovascular system (NRC, 2000). Salonen et al. (1995) demonstrated a negative association between Hg (derived from fish consumption) and the risk of acute myocardial infarction (AMI). The adverse effects of Hg on the cardiovascular system may occur 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 also suggested that high Hg content might diminish the cardioprotective effect of fish intake.
Despite undisputable health benefits of fish consumption, there are legitimate concerns regarding the ingestion of monomethyl mercury (MMHg), which is contained in certain types of large fish and seafood. In the Amazon environment, without industrial discharges of preformed organic Hg, fish MMHg accumulation depends on complex biochemical factors such as metal methylation and MMHg acquisition by organisms in the aquatic food web. It is generally accepted that there is a predictive association between fish-feeding strategies, age/size within a particular species, and fish Hg concentration. Preformed MMHg is well absorbed and complexed in proteinaceous matrices of aquatic animals. In humans, fish is the main source of MMHg. MMHg levels can be traced through Hg concentrations found in hair and blood. Indeed, within the same Amazon rainforest environment, riparians (Rio Madeira Basin) were demonstrated to consume more fish than indigenous people of Eastern Amazonia by virtue of having higher hair Hg concentrations (Barbosa et al., 1995).
Milton (1991) studied the dietary ecology of indigenous people of Eastern Amazonia (Rio Xingu Basin) and showed that intergroup dietary differences appear to represent a type of cultural character displacement. These dietary differences aid in distinguishing members of one group from another. The dietary importance of fishing varies among Indian groups and, for some, it may be regarded as an activity of little value (Milton, 1991). The Amondavans of Western Amazonia (Pavan et al., 1999) and the Yanomami of Venezuela (Holmes, 1984) rarely eat fish, while the Munduruku (Sai Cinza village) 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). For some indigenous populations, language, isolation, and cultural differences are formidable obstacles in obtaining dietary information (Milton, 1991; Sing et al., 1996). However, in Amerindians of French Guiana, it has been possible to estimate fish consumption (Frery et al., 2001).
It is recognized that lifestyle choices affect the risk of developing cardiovascular diseases (CVD). This is especially true in populations with body-mass indices (BMI) that have been associated with all major CVD risk factors (Lamon-Fava et al., 1996). Due to the isolation of native inhabitants of the Amazon forest, studies of CVD risk factors associated with diets and lifestyle have grown of interest of late. These studies focused on unacultured Yanomami Indians with a no-salt diet and showed a very low incidence of cardiovascular disease (Carneiro and Jardim, 1993). Also, little variation of BMI and blood pressure with age was found (Carvalho et al., 1989). Early work on the acultured Munduruku (Rio Cururu), consumers of salt, showed that they have low blood pressure and that it tends to increase with age (Lowenstein, 1961).
The Munduruku and Kayabi inhabit the Tapajós Basin. Devoid of large cities and industrial activity, the sole source of mercury acquisition is through fish. However, some of the rivers used as fishing grounds (Tapajós, 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 fish consumption on CVD risk factors. This was done by using standard markers of Hg exposure in the biota (fish Hg) and fish consumption (hair Hg).
Section snippets
Materials and methods
The study is part of the Projeto Integrado de Proteção à Populações Indígenas da Amazonia Legal–PPTAL (Project for Integration and Protection of Amazonian Indians) of the Deutsche Gesellschaft fur Technische Zusammenarbeit–GTZ. The study was approved and authorized by the FUNAI (Fundação Nacional do Indio, the Brazilian Bureau of Indian Affairs). At each village, the leader of the community gave his or her permission after the purpose of the research was explained. The area occupied by the
Results
The Hg concentrations in fish are presented in Table 1 and illustrate differences in trophic levels and rivers fished by the Indians. Piscivorous species showed the highest Hg concentrations. The range of means of fish Hg concentrations in piscivorous (196–777 ng/g) species from rivers not impacted by gold mining (Kabitutu, Cururu, and Curuzinho rivers) was comparable to the range (259–673 ng/g) seen for impacted rivers (Tapajós, Teles Pires, Tropas). Distribution of Hg in all fish samples is
Discussion
In the Curuzinho (Kayabi fishing area) and Cururu rivers, there is no history of gold mining. Yet, the fish Hg concentrations are comparable to other sampling sites with a history of intense gold-mining activity (Rio Teles Pires, Rio das Tropas, Rio Tapajós). Overall, mean fish Hg concentrations are consistent with previously reported values for the Tapajós Basin (Barbosa et al., 2003). Part of this observed variation could be due to the random nature of opportunity fishing. Indeed, in fish
Conclusions
In spite of substantial amounts of metallic Hg released due to gold-mining activity, there is no evidence that this Hg has impacted fish Hg in the head tributaries of Rio Tapajós. Fish consumption is the only source of MMHg exposure for native people who do not have access to commodity foods. For these people, to reduce dietary MMHg means reducing the consumption of fish, a dietary staple and a source of many important nutrients. No evidence exists that shows that freshwater Amazonian fish
Acknowledgments
We thank the Fundação Nacional do Indio–FUNAI, Deutsche Gesellschaft fur Technische Zusammenarbeit–GTZ, Projeto Integrado de Proteção à Populações Indígenas da Amazonia Legal–PPTAL, and the Munduruku and Kayabi populations for participation in this study.
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