Artisanal and small-scale gold mining (ASGM), which uses liquid elemental mercury in the gold extraction process, has emerged as the leading anthropogenic source of mercury emissions globally and accounts for 37% of human related atmospheric emissions and an additional 800 tons of mercury are released to land and water annually [1
]. Mercury is also released into the environment by other processes that include soil release from natural erosion, as well deforestation related to agricultural practices [3
]. Environmental contamination poses a human health risk due to the potential for mercury to be transformed into the highly toxic and bioavailable form, monomethylmercury (MeHg), which is responsible for the majority of dietary human exposures [6
]. MeHg is a potent neurotoxin with recognized impacts on child cognitive development [7
]. Despite knowledge of these health impacts, ASGM continues to expand and has increased 200–500% since 1998 in some hotspots in Southeast Asia, Africa, and the Amazon, in response to the global demand for gold [10
]. This rapid expansion raises concern for adverse human health impacts from elevated and chronic exposure in nearby non-ASGM communities.
Adverse health impacts result from both acute and chronic exposures; however, chronic exposures are a serious health concern because they are not only associated with the developmental, renal, and neurological impacts observed with acute exposure, but also with cardiovascular and immunological impairments [17
]. Additionally, chronic exposures could induce these health impacts at lower doses compared to acute exposures [23
]. In regions impacted by ASGM, chronic mercury exposure is often presumed from occupational exposure or dietary consumption [8
]; however, the majority of these studies use cross-sectional assessments of mercury content in hair, urine, or blood and only assess mercury exposure at one time-point [28
]. In fact, we are aware of only a handful of studies that evaluated the variation in mercury exposure over time in ASGM regions [29
]. Two of these studies, Dolbec et al. (2001) and Lebel et al. (1997), evaluated exposure seasonality in communities impacted by ASGM by using a segmented hair analysis. Both studies observed seasonality in hair mercury content that was correlated with fish consumption and fish species availability during different seasons [29
]. More studies of this nature are needed to appropriately define the temporal aspect of exposure risk.
Furthermore, to properly predict human health outcomes in regions impacted by ASGM, understanding mercury exposure routes is critical. Currently, assessments of human exposure risk factors have primarily focused on general fish consumption and spatial relation to mining activities; however, methodological constraints of previous work have limited broader interpretation of the data. For example, when considering dietary exposure, only in a few studies has the focus been on some specific species, in combination with consumption frequency. The focus on fish is understandable, given the strong association with mercury exposure; however, this focus has led to a paucity of knowledge concerning other potential dietary associations. In two studies that evaluated other food groups [29
], only one reported their observations of an association of reduced hair mercury with certain tropical fruits [31
]. This reduction in hair mercury may relate to decreased MeHg bioaccessibility observed in vitro with certain phytochemicals in tea extracts and grains [32
]. Laboratory-based studies also indicate that reduced mercury exposures could associate with dietary items rich in certain antioxidants, as antioxidants such as glutathione (GSH) and N-acetylcysteine (NAC) have been associated with increased mercury elimination [34
]. Dietary selenium is another factor postulated to reduce mercury exposure, but observed outcomes in laboratory and epidemiological studies have not been consistent [37
]. These findings warrant the consideration of other phytochemical and antioxidant-rich dietary items at the population level. In addition to dietary considerations, the prediction of human exposure risk requires knowledge of the spatial extent of environmental mercury contamination. In studies measuring both mercury content in fish and human hair, elevated exposures compared to a USEPA (U.S. Environmental Protection Agency) benchmark dose (1.2 µg/g) have been observed near and downstream of ASGM [30
]. However, these studies fall short at describing the spatial extent of ASGM-related contamination as their mercury measurements were only made at one or two locations. A more extensive survey that measures exposure at different distances and directions from mining is necessary to better describe the extent of environmental contamination and identify where the risk of exposure is high.
Building on previous work, this study provides the largest mercury exposure assessment to date in communities impacted by ASGM in the Peruvian Amazon. We focus on exposure risks related to diet, spatial location, and proximity to ASGM activities to elucidate the relationship between environmental and human mercury exposure, evaluate chronic human exposure, and identify important risk factors for exposure in a region where ASGM has expanded rapidly over the past decades, Madre de Dios (MDD), Peru. In MDD, the potential for human exposure has been reported in two studies that describe a range of human exposure in six non-randomly selected communities [44
]. While these studies indicate that human exposure is possible in some ASGM and non-ASGM communities in MDD, they have significant limitations connecting mining to fish contamination and human exposure because they: (1) did not assess human exposure in a systematic manner where communities and households were randomly selected; (2) only addressed fish consumption generally, not taking into account the importance of trophic level; and (3) measured levels of fish contamination in aquaculture farms, which are not a predominant source of fish for most households and could be less impacted by ASGM. Our study addresses these gaps, connecting human exposure and ASGM-related contamination by building on our previously published environmental study relating human exposure at different distances from mining to mercury content in water, sediment, and river fish [46
]. The human exposure assessment presented in this study was conducted in the same communities and in a similar timeframe as our environmental study, and therefore enabled for the first time a direct comparison between environmental and human exposure in a population-representative cohort of communities located along a 560 km segment of the MDD River.
The first objective of this study was to determine how well human exposure can be predicted from environmental mercury levels and residential proximity to ASGM. We hypothesized human exposure would be related to environmental levels: low exposure would occur upstream where there are minimal mining impacts, the highest exposures would be in communities closer to ASGM, and slightly lower exposure would be observed downstream of mining. Secondly, because regional ASGM has been expanding in MDD, we also evaluated chronic exposure that was measured using sequential hair samples from women of child-bearing age (WCBA). Temporal mercury exposure was examined in WCBA as they are a sensitive population whose exposure directly influences child health. The Peruvian Ministry of Health recognizes the potential for adverse health impacts from increased mercury exposure in the region and is interested in better understanding exposure risk factors to facilitate the reduction in total mercury body burden in MDD communities. Finally, we sought to evaluate intra-household correlations of mercury exposure among children, parents, and other family members and determine whether other dietary items, including high antioxidant and selenium-rich foods, and diversity in food consumption are positively or negatively associated with hair mercury level. While it is suspected that the consumption of high trophic level fish species is a risk for mercury exposure, limited scientific evidence exists to define what other dietary items may be positively or negatively associated with mercury exposure.
This is the first study to provide a spatially-resolved assessment of local environment, diet, and mercury exposure across a large geographic region of substantial ASGM activity with a large study population. Results from our studies demonstrate extensive environmental mercury contamination near and far downstream of ASGM activities are directly correlated with elevated human exposure across all age-sex groups. In addition, we identify a population far upstream (more than 100 km) of mining where environmental mercury contamination is low, but human mercury exposure is high. Lastly, we have determined that temporal variability in mercury exposure is low, yet considerable variability in mean levels exist across communities. The disparity between low environmental mercury and elevated human exposure persisted after accounting for household fish consumption and indicates that environmental sampling alone is insufficient to evaluate human mercury exposure. Fish consumption was strongly associated with increased hair mercury content; however, this study also observed lower hair mercury associations with frequent fruit and grain consumption. Although directionality of the inverse associations could not be addressed in this cross-sectional study, these results provide additional support that certain nutrients, such as omega-3 fatty acids [67
], have an influence on mediating mercury exposure and toxicity, which may account for the conflicting results concerning mercury related child neurotoxicity in two prospective studies performed in the Faroe Islands, where neurotoxicity was observed, and the Seychelles, where significant neurotoxicity was not observed.
Mercury levels detected among residents living in the MDD watershed were elevated over the year timeframe assessed in this study. The observed levels were greater than those reported in a previous study in Puerto Maldonado [44
], but lower than other studies of high fish-consuming communities of the Brazilian Amazon [69
]. In Brazil, along the Rio Tapajós, observed mercury content in hair ranges 4–9 µg/g in areas not impacted by mining [72
] and 13–24 µg/g in areas impacted by gold mining [71
]. In MDD, more than 80% of WCBA exceeded the USEPA threshold of 1.2 µg/g at the time of sampling and for the majority of the prior year. These results, combined with the model of child-predicted hair mercury imply that children who currently exceed 1.2 µg/g have an 85% probability of exceeding 1.2 µg/g for 8 of the past 12 months. These exposure levels have been associated with neurological deficits including child cognition and visual recognition, as well as verbal performance, visual recognition, language, attention, and memory deficiencies later in childhood in multiple longitudinal studies [7
] and a cross-sectional study in an Amazonian population [8
]. In MDD, the estimated neurotoxicity effects could include reduced infant visual recognition memory (VRM) score by 19.9 points (up to 70.9) and child IQ by 1.2 points (up to 4.4) based on reduced visual recognition memory scores in US infants [74
] and an estimated IQ point reduction from an assumed linear dose-response from neuropsychological exams administered to the Faroe Islands study cohort at age 7 [75
]. Moreover, a more recent evaluation of the Faroe Island cohort at age 22 years provides evidence that these deficits may persist beyond childhood [77
]. Child exposure and developmental outcomes are areas that should be pursued further as mercury exposure in these communities is chronic, which could produce long-term disease risk and loss in economic productivity [78
Over the timeframe evaluated, we observed high exposure over the previous year throughout all study communities, though temporal exposure varied between individual WCBA. In addition, we observed exposure seasonality, with higher hair mercury during the dry season and lower hair mercury during the rainy season. Although we were unable to assess seasonal availability of fish in each community, the lower exposure during the rainy season and could be reflective of an overall reduced fish availability or altered species availability, as mercury content in fish has not been observed to vary between the wet and dry seasons [46
]. A comparable pattern of lower exposures around the February–March rainy season was observed in another Amazonian population that had increased herbivorous fish consumption during the period of lower hair mercury, although the seasonality was more pronounced in that study [29
]. Interestingly, our observed changes in hair mercury over time did not show evidence of a continual increase in mercury exposure that could be expected in a region where mining has been readily expanding. However, the lack of an apparent increase in hair mercury may relate to the short timeframe examined.
The patterns in exposure over time varied among women, though the range between the maximum and minimum hair mercury for most women was modest (less than 5 µg/g). This was not the case for all women, as a larger range (of up to 17 µg/g) was noted in several women with the highest exposures. The highest hair mercury contents (above 10 µg/g) were recorded during July–November 2013 in three Boca Manu (BMA) women with similar temporal exposure patterns. Hair mercury content in these individuals rapidly decreased to a lower level (5 µg/g) over 6–8 months. This attenuation of hair mercury was similar to the log-linear elimination rate observed in animal and human models recorded following a single exposure [79
]. All three women were from households that reported seasonal fish consumption and our observations could relate to attenuated mercury exposure following a high dietary exposure event related to season.
Spatial location relative to mining was an important determinant of both environmental and human mercury exposure, with the lowest exposures occurring more than 100 km upstream from ASGM and increased exposures occurring in near and far downstream of active mining. The correlation between human exposure and our environmental data that was collected in a similar timeframe with human biomarkers was high for communities near and downstream of ASGM. However, our results suggest that environmental mercury level (fish contamination) is not an adequate predictor in some communities. For example, communities near mining may have unexpected dietary sources or be exposed to other mercury species. Because the mercury in hair is typically dominated by monomethylmercury species [80
], diet is often presumed to be the dominant exposure route; however, a fraction of mercury in hair could be the inorganic form caused by other dietary and non-dietary routes (e.g., inorganic mercury exposure from gold amalgamation) [81
]. Unexpectedly, the highest measurements of hair mercury were identified in Boca Manu, a community located ~75 km upstream of active mining (Figure 2
). In communities upstream of mining, the high human exposure may relate to migration patterns to areas with higher mercury exposure risk, an unmeasured genetics factor causing slower clearance of mercury, or a difference in natural geology that results in increased local mercury release. These observed variations in predicted mercury levels underscore the importance of evaluating more information to predict human exposure.
In accordance with other studies, fish consumption was a strong predictor of increased mercury exposure [82
]. While general fish consumption at the household level did not predict hair mercury content, the consumption of higher trophic level fish including doncella and chambira, was associated with a 57–168% increase in hair mercury. Environmental data from the region also support that these fish could pose a risk as the average fish filet mercury level of doncella and carnivorous fish was above the USEPA recommended value (0.3 mg/kg), with many fish above the higher United States Food and Drug Administration (USFDA) action level (1.0 mg/kg) [46
Other household dietary variables were found to be strong predictors of mercury exposure, including the frequent consumption of grains and fruits native to Peru, which were associated with decreased hair mercury. The influence of two grains, quinoa and kiwicha, on mercury exposure have not been previously examined and frequent household consumption of these grains was associated with 61–95% and 45–88% lower hair mercury contents, respectively. The correlation of frequent grain consumption with decreased exposure may be related to increased mercury elimination. Both quinoa and kiwicha have health benefits that are suggested to originate from being high in fiber, dietary minerals (calcium, magnesium, manganese, and phosphorus), antioxidants, and flavonoids [86
Reduced hair mercury was also correlated with frequent fruit consumption, and the strongest associations were observed with tomatoes and bananas. Increased tomato and banana consumption were associated with 29–41% reductions in hair mercury. Protective effects related to tomato consumption has been observed in other studies [90
]. In young children, tomato consumption has been associated with lower blood mercury levels [90
]. In laboratory studies, tomato and tomato extracts mitigated the impacts of inorganic mercury exposure on intercellular communication and cytokine concentrations [92
] and reduced mercury accumulation in liver [91
]. Mechanisms related to this inverse relationship have not been identified but are likely related to the nutritional value of tomatoes and increased mercury elimination as tomatoes are known to contain antioxidants (the carotenoid lycopene, ascorbic acid, and beta-carotene); flavonoids; and metal chelating proteins, peptides, phytochelatins, and other heavy metal binding complexes that are analogous to metallothioneins [93
]. Mechanisms for mercury reductions observed with banana consumption are likely similar to that of tomatoes, as bananas also have high levels of antioxidants (β
-carotene, vitamin C, and vitamin E) [96
]. Our observations of reduced mercury exposure associated with consumption of certain dietary items should be further investigated with mechanistic studies and dietary interventions to validate these findings as they have the potential to mediate mercury exposure in communities where exposure is elevated. Considering diet as a factor that contributes to health status is not new; however, it is increasingly important to consider when determining mercury exposure impacts. Certain nutritional factors, like selenium, are hypothesized to alter mercury exposure by reducing bioavailable mercury and increasing antioxidant function [37
], while others, such as omega-3 fatty acids and vitamin B, have been associated with modifying child neurological [67
] and immunological outcomes [104