Lead exposure in indigenous communities of the Amazon basin, Peru

International Journal of Hygiene and Environmental Health 215 (2011) 59–63

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Lead exposure in indigenous communities of the Amazon basin, Peru Cynthia Anticona a,∗ , Ingvar A. Bergdahl b , Thomas Lundh c , Yuri Alegre d , Miguel San Sebastian a a

Department of Public Health and Clinical Medicine, Epidemiology and Global Health Umea University, SE-901 85 Umeå, Sweden Department of Public Health and Clinical Medicine, Occupational and Environmental Medicine, Umea University, SE-901 85 Umeå, Sweden c Department of Occupational and Environmental Medicine, Lund University Hospital S- 22185 Lund, Sweden d Regional Directorate of Health in Loreto, Av. 28 de Julio S/N Punchana, Iquitos, Peru b

a r t i c l e

i n f o

Article history: Received 2 February 2011 Received in revised form 17 June 2011 Accepted 17 July 2011 Keywords: Lead exposure Corrientes river Peru Oil exploitation

a b s t r a c t Since 2006, three studies have reported elevated levels of lead (Pb) among the indigenous population of the Corrientes river, in the Amazon basin of Peru. Due to the large evidence of environmental pollution related to oil exploitation in the area, this activity has been suggested as the source of exposure. This study aimed to evaluate Pb levels in the population and environment of two communities exposed and one community non-exposed to the oil exploitation activity. Blood lead levels (BLL) were determined by the instrument Leadcare. A comparison with the graphite furnace atomic absorption technique was performed in order to validate the Leadcare results. Environmental samples were analyzed by inductively coupled plasma atomic emission spectroscopy. Among 361 capillary samples, the mean BLL was 9.4 ␮g/dl. Mean BLL of the communities exposed (n = 171, x¯ = 9.5 ␮g/dl) and non-exposed (n = 190, x¯ = 9.2 ␮g/dl) to the oil activity were not significantly different. Pb levels in environmental samples were below the maximum permissible levels. The sources of exposure could not be identified. Elevated levels of Pb in the oil-non-exposed community pointed out at other sources not yet clarified. © 2011 Elsevier GmbH. All rights reserved.

Introduction The Corrientes river basin is located in the Peruvian Amazon basin. This territory has a 40 years history of oil exploitation, linked to a large environmental impact (Orta et al., 2007). In 2006, a governmental evaluation revealed elevated levels of lead (Pb) among a sample of 125 adults and 74 children from 7 indigenous communities of this river, 66.2% of the children were found with blood lead levels (BLL) ≥10 ␮g/dl. A simultaneous assessment of water and sediments indicated low concentrations of heavy metals in surface water. In five samples of sediments the Pb concentrations were 18–23 mg/kg (DIGESA, 2006). Two more evaluations conducted in 2006 (CENSOPAS, 2007) and 2007 (ERI et al., 2007) in two and five communities respectively, indicated elevated BLL mainly in the group aged 0–17 years. Additional analysis of surface water and sediments reported elevated concentrations of various contaminants (barium and polycyclic aromatic hydrocarbons) in water and sediments, but not Pb (ERI et al., 2007). The elevated BLL in these remote communities were surprising due to the absence of classical sources of exposure such as the proximity to lead-using industries or the automobile exhaust (leaded gasoline). Reports from public health officials (MINSA, 2006) and

∗ Corresponding author. Tel.: +46 90 785 13 28; fax: +46 90 13 89 77. E-mail address: [email protected] (C. Anticona). 1438-4639/$ – see front matter © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.ijheh.2011.07.003

other authors (ERI et al., 2007; Orta et al., 2007) suggested that the oil related pollution (the dumping of produced waters containing heavy metals into the river) might be the main source of Pb exposure. However, the lack of both, a comprehensive environmental assessment and ‘control’ communities made this suggested association uncertain. In order to overcome the previous limitations, this study aimed to determine and compare Pb levels in the population and the environment of two communities exposed and one community non-exposed to the oil exploitation activity and related pollution. In addition, the use of the portable Pb analysis instrument Leadcare was evaluated in order to validate its application as an screening tool in this kind of setting (tropical forest). Previous studies have indicated that critical factors such as the distance, the amount of human and material resources as well as the population acceptance (influenced by cultural beliefs) make the analysis of venous blood samples with the graphite furnace atomic absorption (GFAAS) method difficult and unsustainable.

Materials and methods Setting and study population The Corrientes river basin is located at 200 km west of the city of Iquitos, at 1–3 days’ travel by riverboat or 45 min by plane. With an area of 15 000 km2 of lowland tropical forests, it holds 36 communities and various oil installations (Perrault-Archambault and

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Coomes, 2008). The indigenous population (approximately 8000) from the Achuar, Quichua and Urarina ethnic groups is considered young (52% aged under 15) and poor (85% has at least one unsatisfied basic need like potable water) (MINSA, 2006). The great majority (85.8%) consumes ground water (Caritas del Peru, 2006) from wells operated by solar panels, in addition to river water. The provision of health care is delivered in 4 medical establishments in the largest communities and through outreach campaigns. Each community has a health promoter, trained to diagnose and give medication for prevalent diseases like malaria (MINSA, 2006). Their subsistence based activities are agriculture, hunting, fishing, and gathering of edible forest products (MINSA, 2006). Men are usually employed by the oil company for short periods. This study was set in three communities: San Cristobal, Peruanito and Santa Isabel de Copal (Fig. 1) with similar life style and/or cultural characteristics. San Cristobal (population = 37) and Peruanito (population = 154) are located in the margin of the Corrientes river, close to oil wells and many of their inhabitants have been employees in the oil company. Santa Isabel de Copal (population = 235) lies on the margin of a Corrientes tributary river (at a distance of 42 km from the Corrientes river) where no oil exploitation has been conducted (PEPISCO, 2008). Blood samples collection and analysis The communities were visited between January and February 2008. In each community, introductory meetings were held to explain the study objectives and invite the whole population to participate on a voluntary basis. A trained medical technician undertook the capillary blood sampling (finger stick) and conducted the analysis for Pb concentration using the portable instrument Leadcare Analyzer II (ESA Biosciences, Inc., USA) in the field, as described by Taylor et al. (2001). The detectable concentrations ranged between 3.33 and 65 ␮g/dl Pb. The equipment had an electronic calibration predetermined for the lot of electrodes used. A new calibration was performed with every batch. Analytical quality control (QC) was monitored by running the two standard QC materials available from the vendor (level 1 and level 2) with every change in test kit batch. For level 1 (Lot 1001A) the results obtained were 7.6 ± 2.1 ␮g/dl (mean ± SD, n = 9) vs. recommended range 4.2–10.2 ␮g/dl. For level 2, (Lot 1001A) the results obtained were 21.3 ± 2.0 ␮g/dl (n = 9) vs. recommended range 18.2–26.2 ␮g/dl. In order to validate the Leadcare analysis, the participants aged 0–17 years, who showed Leadcare BLL ≥ 10 ␮g/dl and the participants aged >17 years with Leadcare BLL ≥ 20 ␮g/dl were asked for a venous blood sample. Twelve samples from young children (0–6 years old) with BLL < 10 ␮g/dl were also included by indication of the local physician, as a safety measure. Six millilitre blood samples were collected in evacuated plastic tubes (Vacutainer green cap, heparin lithium) and frozen (−20 ◦ C) until analysis. Pb levels in whole blood were determined at the private laboratory Blufstein (Lima) by GFAAS (Graphite furnace HGA 900 and Spectrophotometer Aanalyst 400, PerkinElmer, Inc., USA) with Zeeman background correction method (Bosnak et al., 1993). The samples were diluted 1:9 with a solution containing 0.2% ammonium dihydrogen phosphate and 0.1% Triton-X-100. All the samples were prepared once and the concentration was determined in duplicate. The limit of detection (LOD) was 0.21 ␮g/dl, calculated as 3 standard deviations (SD) of the blank (10 repetitive measurements of the lowest sample concentration detected by the instrument). The calibration range for the laboratory GFAAS method was 1,0–40 ␮g/dl. To evaluate the precision, the coefficients of variation (CV) for 10 repetitive measurements of 3 standard concentrations were obtained. For 10, 20 and 40 ␮g/dl, the CV were 2.2%, 0.7% and 0.7%, respectively. To ensure accuracy and confiability, quality control samples Lyphochek Whole Blood Metals (Bio-Rad

Laboratories, Inc.) were analyzed along with the collected samples. For Lyphochek Whole Blood Metals level 1 (Lot 3670) the results obtained were 9.37 ± 0.51 ␮g/dl (mean ± SD, n = 7) vs. recommended range 7.1–11.2 ␮g/dl. For level 2, (Lot 36702) the results obtained were 25.43 ± 1.19 ␮g/dl (n = 7) vs. recommended range 21–31 ␮g/dl. An interlaboratory comparison was conducted by analyzing 10% of the venous blood samples in the Laboratory of Lund University Hospital, Sweden, by inductively coupled plasma mass spectrometry (ICP-MS; Thermo X7, Thermo Elemental, Winsford, UK). The LOD was 0.04 ␮g/l for BLL. Almost a perfect correlation (y = 0.8x + 2.1, r2 = 0.94) was found between BLL results from the local and reference laboratory (n = 10). All the sampling materials used for the study were pre-tested for their Pb content at the Laboratory of Lund University Hospital and were found to be free from disturbing contamination. Environmental samples collection and analyses In order to investigate potential sources of exposure in the selected communities, environmental samples in the communities and in dwellings were collected at the same time as the blood samples. In the communities, the collection included 4 samples of superficial water from the river bathing sites (at least two water samples per community) and 9 samples of soil from the sporting facilities, the community house, the port area and/or some classrooms from the school of each community (at least two soil samples per community). For the samples collection in dwellings, the authors used the BLL results obtained by the Leadcare to classify children (0–17 years) according to the Centers for Disease Control (CDC) reference value 10 ␮g/dl. In each community, two families including at least two children with BLL ≥ 10 ␮g/dl and two families including all children with BLL < 10 ␮g/dl were selected by random (all the families had at least 3 children). The samples collection in the dwellings included: 17 samples of drinking water (at least one sample per dwelling) and 29 samples of soil from the surface floor of the kitchen and/or the patio (at least one sample per dwelling). Water samples were collected in polyethylene containers and preserved in the field with nitric acid added until a pH < 2 was reached. Top to soil samples 5–10 cm depth from an area of 1 m2 were collected with aluminum spoons and placed in Ziploc plastic bags. The environmental samples analysis was conducted in the private laboratory Envirolab, Lima, by inductively coupled plasma atomic emission spectroscopy (PerkinElmer, Inc., USA). Lead was measured in water samples using EPA method 200.7 (EPA, 2001) with LOD of 1.0 ␮g/l. Accu TraceTM M-200.7-05-5 (AccuStandards Inc. Newhaven, USA) was analyzed to check the accuracy of the method, which was ±0.5% of the certified value (0.1 ␮g/l). In the soil samples, Pb was measured using EPA method 6010B (EPA, 1996) with LOD of 0.8 mg/kg (wet weight). Trace Metals- RTC Loamy Sand 1 (RTC, Laramie, USA) was analyzed to check the accuracy of the method, which was accepted between 85% and 115% of the recommended range (15.7 ± 1.43 mg/kg). Ethics The study protocol was approved by the Ethics Review Board of the Universidad Peruana Cayetano Heredia, Lima. All adult participants signed an informed consent form for themselves and their children. This was read to them in Spanish and in their native language. Medical care was provided whenever was needed. Final explanation of the findings and individual results were given to the communities in coordination with the Federation of Native

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Fig. 1. Location of the study communities in the Corrientes river basin.

Communities of the Corrientes River (FECONACO) and the Regional Directorate of Health (DIRESA) in Loreto. Statistical analyses Data were entered and checked with Epi-Info 3.5. Statistical analysis was performed with STATA 10 (StataCorp LP, USA). Descriptive statistics, tabulations, and distribution plots were determined to assess the BLL distribution. Due to the positively skewed distribution of BLL, values were transformed to a logarithmic scale. One-way analysis of variance (ANOVA) was conducted to test for significant differences among groups’ means (using the antilog BLL). Simple regression analyses and a pair-wise t-test were conducted to compare the Leadcare and GFAAS BLL results. Results Demographic characteristics Overall, there were 361 participants (34 from San Cristobal, 137 from Peruanito and 190 from Santa Isabel de Copal) with a slight majority of women (54.0%). The age group distribution indicated 29.8% for the group 0-6years; 31.3% for the group 7–17 years and 38.8% for the group older than 17 years (Table 1). Characteristics of lead exposure From 361 capillary blood samples, the BLL mean was 9.4 ␮g/dl (range: 3–31.6 ␮g/dl). The BLL mean was significantly lower for women (7.7 ␮g/dl) than for men (11.2 ␮g/dl) (p < 0.01) and it increased significantly by age (p < 0.05), ranging from 7.6 ␮g/dl in the young children (0–6 years old) to 10.7 ␮g/dl in the adults (>17 years old) (Table 2). There was not significant difference of BLL among communities exposed (n = 171, x¯ = 9.5 ␮g/dl) and nonexposed (n = 190, x¯ = 9.2 ␮g/dl) to the oil activity. In the group aged 0–17 years, 25.7% of the communities exposed to oil activity and 25.8% of the community non-exposed had BLL ≥ 10 ␮g/dl. In the group aged 18 years and older, 8.6% of the communities exposed and 4.3% of the community non-exposed to oil activity had BLL ≥ 20 ␮g/dl (Table 2). When reporting results to the population, our reference values for elevated BLL were 10 ␮g/dl for the group aged 0–17 years (CDC, 2005) and 20 ␮g/dl for the group aged > 17 years (CENSOPAS, 2007). Concerning the environmental evaluation, all the superficial river water samples (n = 4) and the drinking water samples (n = 17) showed levels of Pb < 10 ␮g/l (reference value = 15 ␮g/l) (EPA, 2009). Similarly, all the soil samples (n = 38) showed levels of Pb < 0.8 mg/kg (reference value = 200 mg/kg) (EPA, 2004).

Fig. 2. Regression plot of Leadcare versus GFAAS results. The solid line trough the data points (69 observations including 3 outliers) represents the fit regression line, the 95% CI is represented by the grey area.

Validity of Leadcare technique BLL in 66 capillary blood samples analyzed by the Leadcare system were compared with the GFAAS results from venous blood samples of the same individuals (Fig. 2). A simple linear regression detected a statistically significant association (p < 0.05) and good correlation between the two methods results (y = 0.92x + 1.47, r2 = 0.84). Three pair of Leadcare/GFAAS results exhibited a difference >3 standard deviations and were excluded as statistical outliers. The mean difference between the two methods for paired data was 0.53 ␮g/dl; (SD = 2.9, p < 0.05). Taking into account the 3 outliers, there was still a good correlation (y = 0.83x + 2.9, r2 = 0.7) between the results of the two methods. Discussion The population of the three study communities is affected by a chronic Pb exposure, at levels that have been associated with adverse health effects such as impaired cognitive development, subtle deficit of hearing acuity, and reduced height in children (Landrigan, 1998), as well as cardiovascular problems in adults (Navas-Acien, 2004; Park et al., 2006). Compared to previous studies in the same area, overall BLL means (14.3 ␮g/dl in 2005, 12.5 ␮g/dl in 2006 and 9.4 ␮g/dl in 2009) and the proportion of the population 0–17 years old with BLL ≥ 10 ␮g/dl (66.2% in 2005, 55.8% in 2006 and 27.5% in 2009) seem to have decreased over time. Nevertheless, certain diver-

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Table 1 Demographic distribution of participants in the communities exposed and non-exposed to oil activity, by age and gender.

Overall Sex Women Men Age 0–6 7–17 18 and >

Communitites exposed n (%)

Community non-exposed n (%)

Overall n (%)

171(47.4)

190(52.6)

361(100)

91 (53.2) 80 (46.8)

104 (53.3) 86 (51.8)

195(100) 166(100)

49 (45.4) 52 (56.0) 70(50)

59 (54.6) 61 (54.0) 70(50)

108(100) 113(100) 140(100)

Table 2 Distribution of BLL (␮g/dl) as measured by Leadcare technique in the communities exposed and non-exposed to oil activity, by age and gender. Communities exposed n = 171 Mean (SD) (range) Overall

Community non-exposed n = 190 Mean (SD) (range)

Overall n = 361 Mean (SD) (range)

9.5 (4.9) (3.3–31.6)

9.2 (4.3) (3.3–27.9)

Women Men

7.9 (3.6) (3.3–22.6) 11.3 (5.6) (3.3–31.6)

7.6 (2.8) (3.3–17.8) 11.2 (5.0) (4–27.9)

7.7 (3.2) (3.3–22.6) 11.2 (5.3) (3.3–31.6)**

0–6 7–17 18 and >

7.6 (3.1) (3.3–17.7) 9.5 (4.7) (3.3–22.6) 10.8 (5.7) (3.3–31.6)

7.6(2.9) (3.3–17.8) 9.2(4.5) (3.4–26.8) 10.7(4.6) (4.1–27.9)

7.6 (3.0) (3.3–17.8) 9.3 (4.6) (3.3–26.8)* 10.7 (5.1) (3.3–31.6)*

Elevated BLL n (%) 0–17 yearsa 18 years and >b

26 (25.7) 6 (8.6)

31 (25.8) 3 (4.3)

57 (25.8) 9 (6.4)

9.4 (4.6) (3.3–31.6)

Note: ANOVA analysis was conducted in the overall study population using the antilog BLL. * p-Value < 0.05. ** p-Value < 0.01 a Reference value = 10 ␮g/dl. b Reference value = 20 ␮g/dl.

gences in the characteristics of the three studies’ participants do not allow to conclude about a downward tendency. The subjects selected in each study belonged to different communities, which could variate in their sources and levels of Pb exposure. On another side, individuals younger than 1-year old were excluded from the studies in 2005 and 2006. According to our results, the younger children (0–1-year old) had the lowest BLL and their inclusion might have decreased the average of the whole studied population. On another hand, the three studies have concurred that the most affected group is formed by men between 7 and 17 years old, which does not represent a classical Pb age distribution where children 0–6 years of age have the highest BLL (Levin et al., 2008). To this respect, previous studies have described that particular activities of this group such as battery recycling, wire burning and the manufacture of Pb fishing sinkers at home might be risky for Pb exposure (Brown et al., 2008). The BLL mean in the children of these remote communities, 7.6 ␮g/dl for the group 0–6 years and 9.3 ␮g/dl for the group 7–17 years, was similar to the mean reported in other places in Peru. Some examples include the large depositary of minerals in el Callao and the exposure to Pb gasoline in Lima, where BLL means among children aged 0–11 years were found to be 9.6 ␮g/dl in El Callao and 7.1 ␮g/dl in Lima (Espinoza et al., 2003). The comparison of the BLL determined by the Leadcare system and the reference method GFAAS indicated that the portable instrument well estimated the true blood Pb value in the studied population. A recent article supported the use of this device for the clinical evaluation and monitoring of BLL among individual children, though not for investigating neurotoxic effect thresholds associated with BLL below 10 ␮g/dl (Sobin et al., 2011). Furthermore, CDC considers acceptable both the use of capillary blood samples (if collected by staff specially trained in the technique using devices certified as “lead-free.”) and the analysis with the Leadcare system (CDC, 2005), as conducted in this study.

The utilization of this instrument in indigenous communities of the Peruvian Amazon had shown important benefits in terms of coverage and costs. While the previous evaluations were not able to test children aged 0–1 years old because of their parents reluctancy, the use of capillary blood from a finger puncture in this study permitted to test BLL in the youngest children and motivated the interest among parents for future monitoring test. Furthermore, the use of the Leadcare in the field allowed to save great human and financial resources, necessary to transport biological samples from this setting to clinical laboratories in the capital city (12–24 h by motorized boat). For the purpose of this research, the local medical technician was trained in the Regional Directorate of Health in El Callao to conduct the collection and analysis of the blood samples. Therefore, we consider that the Leadcare instrument can be used as an effective and sustainable tool for Pb screening in these communities and others with similar characteristics. An environmental assessment including water and soil was undertaken in order to identify sources of exposure. Given the evidence of the oil related environmental contamination, some authors have suggested that the human Pb exposure might come from the produced waters dumped into the river (Orta et al., 2007). In fact, the first assessments in the Corrientes (1984–1987) indicated that the river waters contained high concentrations of Pb, cadmium, mercury, chromium, arsenic, and total petroleum hydrocarbons (TPH). In 1998, another evaluation recorded high concentrations of oils, fats and mercury in all the rivers receiving production waters, including the Corrientes, and elevated levels of Pb in some tributary streams (Orta et al., 2007). In 2005, the Regional Environmental Health Department (DESA) reported elevated Pb levels (>0.03 mg/l, which is the national accepted limit for ‘Waters of areas for the preservation of aquatic fauna and recreational or commercial fishing’) in 2 of 37 water samples taken from different locations in the Corrientes river (DESA, 2005). All the samples of surface waters taken in this study showed concentrations below the standards for Pb, suggesting a different

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situation today. Although we did not include sediments analysis, our findings are similar to the ones reported in more recent studies conducted by DIRESA Loreto during 2008 and 2009, as part of a Water Quality Monitoring project throughout the Corrientes river basin. The results showed that water and sediments had elevated levels of oil, fats, TPH and iron but no Pb. Analysis of water from the public treated-water system from all communities in the Corrientes river revealed high levels of iron but no Pb (DIRESA Loreto, 2009; DIRESA Loreto, 2010). The low concentration of Pb in our samples of soil reinforces the idea of a non-classical source of exposure. Studies conducted in indigenous populations of United States, Greenland and Canada (Brown et al., 2005; Hunt et al., 2009; Iqbal et al., 2008) have highlighted that traditional activities such as hunting as well as the consumption of meat with fragments of Pb ammunitions could be an important source of Pb exposure. A recent study from Brazil has pointed out the use of contaminated pans for farinha preparation as a potential source of Pb exposure (Barbosa et al., 2009). All these activities are commonly practiced among the indigenous people of the Corrientes communities. In conclusion, our data did not allow us to determine the sources of the Pb exposure documented in the studied population. While the environmental pollution in the area due to oil exploitation is evident, elevated BLL in the control community does not support its possible association with the oil extractive activity. The fact that young men were the most affected group points out to a potential exposure related to outdoor male activities such as hunting and fishing, rather than to water or soil. Further research (focused on indigenous traditional activities) to identify the sources and pathways of exposure will be conducted as a prior action, followed by monitoring of the affected individuals and the assessment of other communities in the Corrientes river basin. Funding The field work was financed by the Comprehensive health care plan for the Corrientes native communities (PEPISCO). This work was also supported by the Umeå Centre for Global Health Research, funded by FAS, the Swedish Council for Working Life and Social Research (Grant no. 2006-1512). Competing interests None. Acknowledgements This study was developed through a collaboration agreement between Umea University; FECONACO and DIRESA Loreto. We thank the communities and their leaders for their active participation. References Barbosa Jr., F., Fillion, M., Lemire, M., Sousa, C., 2009. Elevated blood lead levels in a riverside population in the Brazilian Amazon. Environ. Res. 109, 594–599. Bosnak, C., Bradshaw, D., Hergenreder, R., Kingston, K., 1993. Graphite furnace analysis of Pb in blood using continuum source background correction. At. Spectrosc. 14, 80–82. Brown, L., Kim, D., Yomai, A., Meyer, P.A., Noonan, G.P., Huff, D., et al., 2008. Blood lead levels and risk factors for lead poisoning in children and caregivers in Chuuk State, Micronesia. Int. J. Hyg. Environ. Health 4, 231–236. Brown, L., Kim, B., Yomai, A., Pamela, A., Noonan, G., Huffa, D., Flanders, W., Blood, 2005. Pb levels and risk factors for Pb poisoning in children and caregivers in Chuuk State, Micronesia. Int. J. Hyg. Environ. Health 208, 231–236.

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