Human health risk assessment of metals and metalloids in mining areas of the Northeast Andean foothills of the Ecuadorian Amazon

Gold mining (GM) is a major source of metals and metalloids in rivers, causing severe environmental pollution and increasing the exposure risks to the residents of surrounding areas. Mining in Ecuadorian Amazonia has dramatically increased in recent years, but its impacts on Indigenous local populations that make use of rivers are still unknown. The aim of this study was to assess the risks to adults and children caused by the exposure to metals and metalloids in freshwater ecosystems contaminated with tailings released by GM activities in 11 sites of the upper Napo River basin, Ecuador. We selected a carcinogenic and a noncarcinogenic risk assessment method to estimate the hazard index (HI) and total cancer risk (TCR). The concentration of Ag, Al, As, Cd, Cu, Fe, Mn, Pb, Zn, B, and V in water and sediment samples was considered to assess the risks to human health. The calculated HI was 23–352 times greater than the acceptable limits in all sites for both children and adults. Mn and Fe were the main contributors (75% in water and 99% in sediment) to the total calculated risk based on the HI. The calculated TCR for children and adults exceeded approximately one to three times the permissible threshold in all sites. As and Pb contributed up to 93% of the total calculated risk based on TCR for both children and adults. This study demonstrates that the emission and mobilization of metals and metalloids caused by mining activities increase the risk to human health, to which we recommend further monitoring of freshwater contamination in the area and the implementation of preventive health management measures. Integr Environ Assess Manag 2023;19:706–716. © 2022 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).


INTRODUCTION
Gold mining (GM) has historically affected riverine areas of the Amazon basin (Pan et al., 2018;Rehman et al., 2020;Saha et al., 2017). Intensive gold exploitation results in landuse modifications (Guzmán-Martínez et al., 2020), causes freshwater contamination (Capparelli et al., 2020, and endangers human health . In the eastern Andes of Ecuador, at the transitions with Amazonia lowland, concessioned and illegal GM have caused severe environmental pollution problems  and negative social impacts (Guayasamin et al., 2021). New GM concessions were awarded in the Napo province during the previous decade (Roy et al., 2018). Although artisanal smallscale GM (mining without heavy machinery and granted to small companies or local communities) is the most common authorized concession, industrial GM accounts for 98% of the total territory for gold exploitation in the Napo province (33 718 ha). Nevertheless, illegal GM in Amazonia has increased sharply in recent years (Mestanza-Ramón et al., 2022a). Given the proliferation of mining concessions, and the substantial increase in illegal mining activities (Mestanza-Ramón et al., 2022b), gathering information on the risks to human health caused by this activity is crucial.
Metals and metalloids are commonly released as byproducts of GM and are persistent compounds with a high bioaccumulative capacity (Saha et al., 2017). They can cause neurotoxic and carcinogenic effects in humans when inhaled, ingested, or through dermal contact (Guzmán-Martínez et al., 2020;Ogola et al., 2002;Wang et al., 2014;Zheng et al., 2020). The toxic effects of the exposure to metals and metalloids have been widely reported using human health risk assessment (HHRA) methods (Li et al., 2013Sun et al., 2018). Human health risk assessments can be used to identify metals and metalloids that pose major human health hazards as well as to determine areas that require management and intervention (Castresana et al., 2019;Huang et al., 2018;Singh et al., 2019). In addition, HHRAs in mining areas may indicate whether residents are at risk caused by exposure to PTEs through multiple exposure routes and whether children have greater or less vulnerability than adults based on different exposure routes and their common behavior (Marrugo-Negrete et al., 2020;Rashid et al., 2019).
Artisanal and small-scale GM in the Ecuadorian Amazon is carried out on river margins and in small streams because gold deposits are often concentrated in the alluvial terraces. As a consequence of GM, concentrations of metals and metalloids greater than established environmental thresholds have been detected in rivers of the southern provinces of Sucumbios and Orellana (Carrillo et al., 2021;Escobar-Segovia et al., 2021;Rivera-Parra et al., 2021). In the Napo province, studies carried out in areas affected by GM have also detected metals and metalloids in environmental concentrations exceeding quality standards for both water and sediment (Capparelli et al., 2020Galarza et al., 2021). Based on the dataset of Capparelli et al. (2020), the HHRA made by Jiménez-Oyola et al. (2021) suggests that local populations in the Napo province are at risk through contact with multiple exposure routes (i.e., mining, urban pollution, fish farming, and lixiviate from dumping areas). However, no study has been dedicated to applying HHRAs exclusively to mining activities in this area. Given that GM has intensified, an HHRA using solely data from mining areas would help to understand the risks caused by metals and metalloids to local Indigenous populations inhabiting areas near GM exploitation. Thus, our study aims to assess the carcinogenic and noncarcinogenic risks posed by the exposure to metals and metalloids through water and sediment in GM areas of the Napo province of Ecuador.

Study area
This study was carried out in the tributaries of the Anzu, Jatunyacu, and Napo rivers in the Napo province in northern Ecuadorian Amazonia. This area is a geodiversity hot spot because of the diverse content of high-value minerals in alluvial deposits. Important local urban centers are Puerto Napo, Misahualli, Ahuano, and Carlos Julio Arosemena Tola ( Figure 1). More than half of the 18 200 inhabitants are selfidentified as Indigenous people, distributed in either urban or rural areas (INEC, 2010). The region is characterized by annual precipitation greater than 4000 mm and by the presence of an extensive hydrographic network.

Sampling collection and analyses
Data on metal and metalloids concentration in surface water and sediments were obtained from Capparelli et al. (2021). The water samples were collected at the center of the stream at mid-depth (according to the possibilities of each stream), and superficial sediment samples were collected at the riverbank at a depth of 15 cm. Samples were taken from 11 sites downstream from GM areas located within or right at the limits of the federal mining concessions. From the 44 compounds analyzed in Capparelli et al. (2021), we selected 12 (Ag, Al, As, B, Ba, Cd, Cu, Fe, Mn, Pb, V, and Zn) because of their potential toxicity to human health. Nine of these compounds (Ag, Al, As, Cd, Cu, Fe, Mn, Pb, and Zn) exceeded national or international regulatory standards for water and two (B and V) for sediments (Tables 1 and 2).

Human health risk assessment
The exposure pathways included in the HHRA were water ingestion, dermal contact via water, and dermal contact via sediment, based on the sum of the risk across all metals and metalloids in each site following the methodology described by Lee et al. (2005). For the HHRA calculations, we estimated the chronic daily intake (CDI) according to the proposed USEPA (2004) equations. The parameter values used in the exposure assessment are presented in Table 3.

Carcinogenic and noncarcinogenic risks
Clinical and epidemiological studies have related metals and metalloids with increased cancer risk and/or mortality caused by poisoning in human populations exposed to those substances (Cao et al., 2010;Dooyema et al., 2012). Noncarcinogenic risks were calculated using hazard quotients (HQs) measured for each metal and metalloid (Table 4, Equations 5 and 6). The human health HQs for noncarcinogenic risk were characterized by a threshold dose of toxicity, which is expressed by the reference dose (RfD). The RfD values are different for each metal and metalloid, and they were obtained from the Risk Assessment Information System (RAIS) website (https:// rais.ornl.gov; Supporting Information: Table S1). Then, the cumulative hazard index (HI) was calculated by the sum of all calculated HQs (Table 4, Equation 7). Hazard index values lower than 1 indicated the absence of risk, and HI values greater than 1 indicated risk (USEPA, 2001).
As there is no toxicological threshold for carcinogenic substances, the total carcinogenic risk (TCR) for each site was calculated as the sum of the carcinogenic risk (CR) values for water ingestion multiplied by the cancer slope factor (CSF) of all metals and metalloids found in the same site (Table 4, Equations 7 and 8). CSF values were available only for the PTEs As, B, Cd, and Pb in the RAIS (Supporting Information: Table S1). Then, TRC values were compared with the permissible reference values (USEPA, 2001). We decided to use a single model for each element, avoiding the use of metal-specific models in order to obtain results comparable with previously published studies (Covre et al., 2021;E. S. de Souza et al., 2017). Calculated TCR values greater than 1 × 10 −4 were considered to pose unacceptable risks (with high certainty), whereas values lower than 1 × 10 −6 were considered to pose insignificant risks (with high certainty), and values ranging between 1 × 10 −4 and 1 × 10 −6 were considered to pose potential risks (Fryer et al., 2006;Hu et al., 2012).

Human health risk assessment
Overall, the HHRA indicated toxicological risks to human health in all sites. The HI exceeded the permissible thresholds for children and adults to be considered noncarcinogenic risk in all sites by at least one-to threefold. The HI values for children and adults were ranked as: The P6 site had the highest value exceeding the permissible limit for both children and adults, 352 and 154, respectively (Supporting Information: Table S6), and they would experience the highest noncarcinogenic effects caused by exposure to metals and metalloids at this site. The P8 site had the lowest value for both children and adults, whereas the risk to children was double that for adults (55 and 24, respectively). Higher HI values were obtained for children than for adults in all sites, meaning that children are more susceptible to toxicological risks due to water ingestion and water and sediment dermal contact (Figure 2A).
The TCR values for children and adults were ranked as: Sites P3, P10, and P11 had the highest values for both children and adults, exceeding by almost three times the limit to be considered a risk, 1 × 10 −6 , whereas P4 had the lowest risk value (Supporting Information: Table S6). However, none of the TCR values exceeded the threshold value of 1 × 10 −4 , above which unacceptable risks are expected with high certainty. According to our calculations, children were more susceptible to cancer risks than adults at all sites ( Figure 2B). The spatial distribution of HI and TCR across the study area is shown in Figure 3. Overall, the sites located in the western part of the study area had higher HI and TCR values than the eastern parts.
The presence of Mn and Fe in water and sediments contributed more than 75% and 99%, respectively, to the HI ( Figure 4A,B). In almost all sites, the contribution of Mn to the HI in water was greater than 60% for children and adults; whereas in sites P7 and P8 the contributions of Mn and Fe were very similar, approximately 40% each. As for sediments, Fe contributed up to 71% to the HI for children and adults. The HI results suggested that, for both adults and children, the HI risk for Mn and Fe from sediment dermal contact was the primary exposure pathway ( Figure 4A,B; Supporting Information: Tables S2, S3, S7). Regarding the TCR, in both adults and children, the exposure to As and Pb contributed up to 93%. Total cancer risk indicated that the primary pathway of exposure was derived from water ingestion ( Figure   Notes: Data were retrieved from Capparelli et al. (2021). Elements that exceed regulatory standards determined by the Ecuadorian (TULSMA) or the Canadian Environmental legislation (CCME) are indicated with an asterisk. Abbreviation: HHRA, human health risk assessment.

Potential impacts of PTEs on human health
This study was motivated by the high levels of metals and metalloids reported in the Napo province by Capparelli et al. (2021) and the concern these authors raised for the health of local freshwater ecosystems and Indigenous populations. The study suggests chronic toxicological risks in all sites evaluated and potential carcinogenic risks in most of the sites. Similar findings were reported by Castilhos et al. (2015) and E. S. de Souza et al. (2017) in GM areas of the Brazilian Amazonia. In our study, the maximum HI was up to 352 times greater than the established threshold for children and 153 times greater for adults. The TCR for adults and children was approximately three times greater than the established threshold for risk. The calculated TCR's highest values were for water ingestion for daily activities such as drinking, cooking, and human hygiene, corroborating the results of Jiménez-Oyola et al. (2021).
The elevated TRC was caused by the high concentration of As and Pb in the water. Our results are in line with those of Carvalho l Ferreira et al. (2016), who also reported elevated HI and TCR values in areas that had been affected by mining tailings in Portugal. In both cases, As exposure was related to incidental ingestion of water. Chronic and acute As toxicities have been associated with negative health effects (Chen et al., 2019), and high concentrations of As in areas close to mining sites may expose human populations to an endemic contamination risk (Souza Neto et al., 2020). Exposure to Pb is of great concern because between 8% and 57% of total Pb exposure is associated with drinking water. The risk of the exposure to Pb has been reported before (Jennings & Duncan, 2017). Regarding Cd, the high concentration of this metal has been linked to diarrhea, dermatitis, allergy, asthma, cancers, and other dysfunctions (Fallahzadeh et al., 2018;Satarug & Moore, 2004).
Human populations that are in constant contact with the above-mentioned metals are at elevated risk of developing acute and chronic diseases caused by long-term exposure. Additionally, given the high contribution of As, Cd, Pb, and Cr to the HI and TCR, local people should be informed and protected from exposure to contaminated water and sediments. Therefore, we advocate the provision of alternative water sources, the incentivizing of information campaigns, the facilitation of medical care, and the monitoring of the food chain supply, because metals can be easily transferred to edible plant parts (Gerson et al., 2021;Romero-Estévez et al., 2019), to invertebrates , and to   (3) Note: The exposure factors considered in the CDI are described in Table 3 (USEPA, 2011). Abbreviations: ABS, dermal absorption factor; AF, adherence factor; AT, averaging time; BW, body weight; CDI, chronic daily intake; CF, conversion factor; ED, exposure duration; EF, exposure frequency; ET, exposure time; K p , permeability constant; SA, skin surface area.
Sampling sites located at the outlets of the downstream basin (sites P6, P9, P10, and P11; Figure 3) had HIs and TCRs limits greater than the threshold for both adults and children. Human settlements are frequently located a short distance from river meanders, floodplains, and basin outlets, where washed mining sediments and mining tailings are immediately transported and deposited. For instance, sites P6 and P11 are located less than 1 km away from approximately 50 Indigenous communities that depend on rivers to obtain water for daily use. Moreover, the intensive flood regimes in the upper Napo basin rivers can lead to the storage of contaminated sediments along riverbanks near human settlements (Appleton et al., 2001;Lucas-Solis et al., 2021). The   degree of contamination of both water and sediments ) and the HI and TCR calculated for these sites suggest that it might be possible that local communities have been consuming water with metal and metalloid levels greater than the recommended for a relatively long time. Thus, further examination of the temporal and spatial extensions of contamination and their impacts on the health of local Indigenous communities is recommended.

Perspectives on an Ecuadorian Amazonian scenario
Human health risk assessments are crucial to the design of further monitoring campaigns and to the establishment of corrective actions to areas affected by mining (De Miguel et al., 2014). Here, we based our HHRA estimates on the framework established by the USEPA, which includes a set of predefined exposure equations and parameter values. The calculation of risks to children and adults via water and sediment exposure was based on an exposure frequency of 350 (a value often used in other studies for Amazonian regions; Covre et al., 2021;J. J. de Souza et al., 2018) days per year, older than 6 years (for children) or 24 years (for adults; Table 3). However, contact with the aquatic ecosystem of Indigenous communities is expected to be greater than this, which could increase the risk of developing diseases related to metal and metalloid skin contact. Further research should be dedicated to refining the risk calculations by collecting a larger number of environmental samples for the critical elements defined in this study, adjusting water and sediment exposure calculations based on data that represent the habits of the Indigenous population of the Ecuadorian Amazonia.
The interaction of Amazonian communities with the rivers is the basis of their livelihood and cultural activities. If unable to use the river, these communities are forced to rely solely on accumulated rainwater for their daily needs. However, this is not enough for all the necessities, so the communities will still have to use river water for crop irrigation and watering cattle.
Because of the risk of cancer caused by the exposure to metals and metalloids, long-term strategic policies for reducing the exposure of local inhabitants are needed, as metal contamination can persist for decades in the ecosystem. The current policies of the Ecuadorian government aim to facilitate the legal mechanisms that allow mining concessions and other economic activities near or inside protected areas and Indigenous lands (Guayasamin et al., 2021). These policies are responsible for the highest rate of deforestation in the past 10 years, weakening the environmental protection legislation and human rights of traditional and Indigenous populations (Roy et al., 2018). With proper regulation, GM might represent economic gains to the country. However, it may harm the health of the communities and generate environmental problems (Mainville et al., 2006). In the past two years and during the COVID-19 pandemic, both legal and illegal mining activity has increased in Ecuador after the rise in the international price of gold (Mestanza-Ramón et al., 2022b). The data presented here were obtained in 2021, before the last expansion phase of GM activities in the upper Napo River basin. This study suggests that the human health risks were unacceptable before the mining increase in the region and calls for continued monitoring of metal and metalloid exposure and risk in the study region.

CONCLUSIONS
This study demonstrates that water and sediment exposure to metals and metalloids in the northeast Andean foothills of the Ecuadorian Amazon is greater than the established thresholds for producing carcinogenic and noncarcinogenic risks to the local population despite using exposure parameters that may slightly underestimate risk. Spatial analysis reveals that the rivers located at the end of the river basins (P2, P3, P6, P9, P10) are the most contaminated and, therefore,  pose the greatest risk to the health of local communities. Although total concentrations of metals and metalloids can be used to quantify health risks, it is also advisable to assess bioavailable concentrations to obtain more reliable results. Policies to reduce exposure are necessary to avoid harmful effects on the health of local populations and should be accompanied by epidemiological studies to identify the occurrence of diseases associated with heavy metals(loids) through different exposure routes, that is, the consumption of contaminated water and food.

DATA AVAILABILITY STATEMENT
Data, associated metadata, and calculation tools are available from corresponding author Mariana V. Capparelli (marivcap@gmail.com). Table S1. Reference doses (oral and dermal), cancer slope factor and permeability constant for some metals. NA, not available at the time of the study. Table S2. Total hazard quotient (HQ) and hazard index (HI) in water for children and adults. Table S3. Total hazard quotient (HQ) and hazard index (HI) in sediment for children and adults. Table S4. Carcinogenic risk (CR) in water for children and adults. Table S5. Cumulative hazard index (HI) and total cancer risk (TCR) to children and adults from all metals in each site classification by children and adults.