Levels of Arsenic, Cadmium, and Mercury in Urine of Indigenous People Living Close to Oil Extraction Areas in the Peruvian Amazon

Cristina O’Callaghan-Gordo,1,2,3,4 Jaime Rosales,5 Pilar Lizárraga,5 Frederica Barclay,6 Tami Okamoto,7 Diana M. Papoulias,8 Ana Espinosa,2,3,4,9 Martí Orta-Martinez,10 Manolis Kogevinas,2,3,4,9 and John Astete5 Faculty of Health Sciences, Universitat Oberta de Catalunya, Barcelona, Spain ISGlobal, Barcelona, Spain Universitat Pompeu Fabra, Barcelona, Spain CIBER Epidemiología y Salud Pública, Spain Centro Nacional de Salud Ocupacional y Protección del Ambiente para la Salud, Instituto Nacional de Salud, Lima, Peru Centro de Políticas Públicas y Derechos Humanos–Perú Equidad, Lima, Peru Department of Geography, University of Cambridge, Cambridge, UK E-Tech International, El Sobrante, California, USA Hospital del Mar Medical Research Institute, Barcelona, Spain Department of Evolutionary Biology, Ecology and Environmental Sciences, Faculty of Biology, University of Barcelona, Barcelona, Spain


Introduction
Oil extraction can lead to long-term harm to the environment and human communities. 1 In the 1970's, oil extraction started in the northern Peruvian Amazon, in the Corrientes, Pastaza, and Tigre river basins, all major tributaries of the Marañón River, leading to high levels of environmental contamination in these four river basins. The oil concessions of this area, which are currently among of the most contaminated areas of the country [see reports on oil Blocks 8 and 192 (formerly 1AB)], overlap with the territories of the Achuar, Quechua, Kichwa, and Kukama Peoples. These Indigenous groups belong to the Jivaro, Quechua, and Tupi linguistic families, respectively. They live in the northern Amazon, on the border between Peru and Ecuador. According to the 2017 Peruvian National Census (indigenous communities module), it is estimated that ∼ 7,944 Achuar, 11,347 Quechua, 4,742 Kichwa, and 9,532 Kukama Peoples live in these four river basins. 2 These groups were mostly nomadic-hunter gatherers until the 1960s when they settled in small communities. Nowadays, they continue to rely on subsistence agriculture and on hunting and fishing for their daily protein intake. Since the arrival of the oil companies to the area, the inhabitants of the area have shown concerns about the potential health effects of the environmental contamination caused in the area. High blood lead levels (>5 lg=dL in 49% of children and in 60% of adults) were reported among the population of these river basins, 3 but there is no information on other metals. The primary aim of this study was to estimate concentrations of metals in urine of Indigenous People residing in four major river basins in oil concessions areas in Peru. Associations were then explored between previously reported urinary metal concentrations and sociodemographic, environmental, occupational, and lifestyle factors.

Methods
We conducted a cross-sectional study and assessed urinary concentrations of total arsenic (U-As), cadmium (U-Cd) and total mercury (U-Hg) in the populations of the Corrientes, Pastaza, Tigre, and Marañón River basins ( Figure 1) in collaboration with indigenous federations from the northern Peruvian Amazon (ACODECOSPAT, FECONACOR, OPIKAFPE, FEDIQUEP, PUINAMUDT) in May-June 2016. The study design was described in detail elsewhere. 3 Briefly, we followed a two-stage stratified random strategy to select study participants. Thirty-nine communities were selected and between 14% and 15% of families were randomly selected in each community. Participation was offered to all members of the selected families, excluding infants under 6 months of age. The study protocol was reviewed and accepted by the Ethics and Research Committee of the National Institute of Health (NIH), Peru. Written informed consent was given from traditional leaders to conduct the study in each of the communities. Participants ≥18 years of age provided written informed consent, and participants between ≥7 and <18 years of age provided personal verbal consent and their parents provided informed written consent. For participants <7 years of age parents provided informed written consent.
Face-to-face questionnaires were administered to the heads of households to collect information on dwelling and to all family members to collect information on individual risk factors. Urine samples were collected, preserved, and analyzed by atomic absorption spectrophotometry following protocols validated by the Peruvian NIH. 4 The limits of detection (LODs) were 2:5 lg=L for U-As and U-Hg and 0:5 lg=L for U-Cd. We replaced metal values below the LOD by the LOD divided by 2. Thirty-two percent (266), 31% (259), and 50% (408) of measurements were below the LOD for U-As, U-Hg, and U-Cd, respectively.
We used linear regression models of log-transformed variables, taking into account the multilevel study design. 3 Results were back-transformed and presented as geometric mean ratios with 95% confidence intervals [GMR (95% CI)], stratified by age using a threshold of 12 years of age. Associations were tested using the Wald test, and variables associated in individual models (p < 0:1) were considered in multiple regression models. If multicollinearity was observed (variable inflation factors >5), we dropped one of the correlated variables from the model. All analyses were made using Stata (version 14; StataCorp). The map in Figure 1 was elaborated using ArcGIS Pro (version 2.5.0; ESRI) and open-access spatial data on oil concessions and infrastructure, indigenous communities, and natural protected areas.

Results and Discussion
Creatinine-corrected concentrations of metals were available for 824 participants, of which 230 were children (<12 years of age) and 594 were adults (≥12 years of age). Characteristics are presented in Table 1. Average concentrations of U-Hg were 4:1 lg=g for children and 4:4 lg=g for adults. Corresponding concentrations for U-As were 27:7 lg=g and 15 lg=g, and for U-Cd 0:8 lg=g and 1:1 lg=g. Twenty-five percent (n = 57) of children and 28% (164) of adults had U-Hg levels above reference values (RVs) established by the Peruvian Ministry of Health (MINSA) (5 lg=g). For U-As, the corresponding percentages (RV = 20 lg=g) above the RV were 48% (110) for children and 23% (135) for adults, and for U-Cd (RV = 2 lg=g), 2% (6) and 13% (76), respectively. U-Hg concentration (Table 1) increased with age among adults and were higher in the Kukama, mestizo (i.e., peoples that do not identify as belonging to an indigenous group themselves, often mixed-blood people) and other peoples, and among those living around the Marañón basin. Elevated U-Hg was also associated with increased fish consumption, which was higher in the