Bull Environ Contam Toxicol (2014) 93:42–46 DOI 10.1007/s00128-014-1279-5
Monitoring Mercury Exposure in Reproductive Aged Women Inhabiting the Tapajo´s River Basin, Amazon ´ rika Abdon Fiquene Oliveira • Tereza Cristina de Oliveira Corvelo • E Amanda Magno de Parijo´s • Claudia Simone Baltazar de Oliveira • Rosane do Socorro Pompeu de Loiola • Ame´lia A. de Arau´jo • Carlos Arau´jo da Costa Luiz Carlos de Lima Silveira • Maria da Conceic¸a˜o Nascimento Pinheiro
•
Received: 14 October 2013 / Accepted: 8 April 2014 / Published online: 1 May 2014 Ó Springer Science+Business Media New York 2014
Abstract Among Amazonian communities, exposure to methylmercury is associated mainly with fish consumption that may affect fetal development in pregnant women. Therefore a temporal assessment was performed to assess the exposure of reproductive aged women to mercury who reside in the riparian communities of Sa˜o Luı´s do Tapajo´s and Barreiras located in the Tapajo´s basin of the Brazilian Amazon from 1999 to 2012. The total mercury concentration in the 519 hair samples was assessed by cold vapor atomic absorption spectrometry. Data analysis showed that the average total mercury concentration decreased from 1.066 to 0.743 lg/g in those years. In 1999 the proportion of volunteers with mercury levels C10 lg/g was approximately 68 %. In general, exposure to mercury decreased among women of reproductive age, but the potential risks to reproduction and human health is still an issue as 22 % of the woman continued showing high mercury levels (C10 lg/g) in 2012. Keywords Exposure to mercury Women of reproductive age Tapajo´s River Fish consumption Mercury is an environmental pollutant arising from natural and anthropogenic sources. Methylation is particularly relevant in the transformation of mercury into its organic form, i.e., methylmercury. The primary source of mercury exposure for most humans is through the consumption of T. C. de Oliveira Corvelo (&) E´. A. F. Oliveira A. M. de Parijo´s C. S. B. de Oliveira R. do Socorro Pompeu de Loiola A. A. de Arau´jo C. A. da Costa L. C. de Lima Silveira M. da Conceic¸a˜o Nascimento Pinheiro Nu´cleo de Medicina Tropical, Universidade Federal do Para´, Av. Generalı´ssimo Deodoro, 92, Bele´m, Para´ CEP 66055-240, Brazil e-mail: [email protected]
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contaminated fish. Approximately, 95 % of the total mercury in fish is in the form of methylmercury (Malm et al. 1995). Mercury is a neurotoxin that causes irreversible damage to the human nervous system, partly due to its chemical speciation and interactions with other metals in the environment and diet (Lombardi et al. 2012). The greatest damaging potential of methylmercury is associated with intrauterine development because it crosses the placenta and can reach levels in the fetal blood up to 25 % higher than in the maternal blood (Amin-Zaki et al. 1976). In the Amazonian ecosystem, contamination by mercury is associated with occupational exposure. However, the main source of exposure is organic mercury, which is acquired through food consumption (Lebel et al. 1997). The main food source of Amazonian communities is fish. In those communities, the average daily fish intake per individual is 340 g/day, which increases to more than 600 g/day in periods of abundance (Fre´ry et al. 2001). The average mercury levels in Amazonian predator fish vary from 0.04 to 3.77 lg/g per wet weight (revised in Nevado et al. 2010). Because methylmercury is excreted in human hair, and 80 % to 98 % of the mercury in the hair is in the form of methylmercury (Mahaffey 2005), hair is an excellent biological indicator for assessing and monitoring chronic exposure to mercury. Samples of hair collected in riparian communities in the Tapajo´s River area exhibit high mercury levels that can exceed the safety levels established by the World Health Organization (WHO). According to the latter, levels above 10 lg/g methylmercury in the mother’s hair are associated with a 5 % risk of neurological damage in newborns (WHO 1990). Although no typical case of Minamata disease has been reported yet in the Amazon area, mild clinical and/or
Bull Environ Contam Toxicol (2014) 93:42–46
neurophysiological changes are found in communities located along the Tapajo´s River, which can be associated with exposure to methylmercury through the consumption of fish (Lebel et al. 1998; Pinheiro et al. 2003). This situation is a source of concern, and the methylmercury levels of riparian women of reproductive age should be monitored to maintain the level of exposure below the tolerance limits and to avoid fetal exposure during pregnancy. This monitoring is recommended particularly because the upper tolerance limit of 10 lg/g is based on episodes of acute intoxication, in disagreement with to the long-term exposure to relatively low levels of mercury found in areas of the Tapajo´s basin. In these conditions, the likely toxic effects of mercury on the development of the central nervous system have not yet been fully elucidated (Amorim et al. 2000; Crespo-Lo´pez et al. 2009). Thus, these and other factors suggest the need to reassess the tolerance limits of mercury in human beings. The present study assessed the exposure level and accumulation of mercury in women of reproductive age as a potential risk to fetus during pregnancy from two communities in the Tapajo´s River area from 1999 to 2012.
43
for Tropical Medicine, and all of the volunteers signed an informed consent form. The data related to measuring the hair mercury concentrations of the investigated women were analyzed following logarithmic transformation to fit the data to a normal distribution. The data corresponding to the Sa˜o Luiz do Tapajo´s and Barreiras communities were analyzed separately and then combined because no difference was found between them. Descriptive statistics were used to analyze the distributions of the mercury exposure biomarker and the subjects’ ages. Fish consumption was included as a categorical variable. The chi- squared test was used to investigate the proportion of women with high levels of mercury in their hair using the WHO reference level as the threshold ([10 lg/g) (WHO 1990). The one-way analysis of variance (ANOVA) was applied to compare the means and standard errors of the total mercury concentrations in the volunteers’ hair over time from 1999 to 2012. All of the analyses were performed using the BioEstat 5.0 software (Ayres et al. 2007). The significance level was established at p \ 0.05.
Results Materials and Methods The present cross-sectional observational study assessed women of reproductive age, i.e., 12–46 years old, residing in two communities in the Tapajo´s River basin, Sa˜o Luı´s do Tapajo´s and Barreiras, which belong to the Itaituba district (04° 160 3400 S and 55° 590 0100 W), State of Para´Brazil. From 1999 to 2012, a total of 519 hair samples varying from 0.1 to 1 g were collected from the scalp at the occipital area. The total mercury (THg) concentration in hair was assessed by cold vapor atomic absorption spectrometry according to Akagi’s method, described in the Handbook of the Japanese Ministry of the Environment (Suzuki 2004). Quality control, including the precision and accuracy of these measurements, was investigated using the international reference standard IAEA 086 ([95 %). The laboratory of Environmental and Human Toxicology of the Center for Tropical Medicine of the Federal University of Para´ performed the hair analysis using an SP-3D mercury analyzer (Nippon Corporation, Tokyo, Japan). The subjects’ age, time of residence in the investigated locations, investigated year, dietary habits, and total hair mercury concentrations were collected from epidemiological questionnaires administered to each individual by researchers from the Center for Tropical Medicine in their annual visits to the investigated area. The study was approved by the research ethics committee of the Center
The average age of the reproductive age women residing at the investigated riparian communities of the Tapajo´s River ranged from 26 years in 1999 to 31 years in 2012. The average of the logarithm of the total mercury concentration in hair varied from 1.066 lg/g in 1999 to 0.743 lg/g in 2012, which represent the maximum and minimum mean values, respectively, for the investigated period (Table 1). Therefore, the average total mercury concentration significantly decreased (F(regression) = 21.5815; p = 0.0063) during the investigated period from 1999 to 2012 (Fig. 1). The differential variation of this decrease occurred between the estimate corresponding to 1999 and the estimates corresponding to the period from 2005 and 2009 as well as between the estimates corresponding to 1999/2009 and the estimate corresponding to 2012 (one-way ANOVA; LSD test; F = 6.9410; p \ 0.0001). The above-mentioned data were also assessed relative to the tolerance limit of total mercury in the hair established by the WHO (1990) for human beings ([10 lg/g). The temporal distribution of the exposure of women to mercury from 1999 to 2012 expressed as the percentage of hair samples with total mercury concentrations C10 lg/g is displayed in Fig. 2. On the other hand, a reference dose for MeHg of 0.1 lg/kg per day has been established by the US Environmental Protection Agency and has been reviewed by the National Academy of Sciences (NRC 2000). In the way, hair concentrations \1 lg/g represent minimal risk to
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44 Table 1 Descriptive statistics of the age and total mercury (THg) concentration (log units) variables in the hair of women in the Tapajo´s River area/PA, 1999–2012
Bull Environ Contam Toxicol (2014) 93:42–46
Year
Number of cases
Age (years) X ± SE (min–max)
THg (lg/g) X ± SE (min–max)
1999
75
26.07 ± 1.06 (13–46)
1.07 ± 0.034 (0.39 to 1.63)
2001
90
28.81 ± 0.89 (13–46)
1.00 ± 0.035 (-0.17 to 1.89)
2003
85
28.79 ± 0.94 (12–46)
1.03 ± 0.031 (0.12 to 1.52)
2005
85
28.31 ± 0.88 (14–46)
0.94 ± 0.04 (-0.15 to 1.46)
2007
65
29.52 ± 0.97 (13–46)
0.89 ± 0.06 (-0.69 to 1.62)
2009
45
33.91 ± 0.75 (21–45)
0.94 ± 0.04 (0.29 to 1.43)
2012
74
31.12 ± 0.94 (14–46)
0.74 ± 0.05 (-1.69 to 1.55)
Fig. 1 Progression of the average total mercury (THg) concentration (log units) in hair samples of women in the Tapajo´s River area/PA over time (1999–2012)
The proportion of volunteers with mercury levels above the recommended levels (i.e., C10 lg/g) from 1999 to 2003 was approximately 61 %. That level decreased, on average, to 47 % from 2005 to 2010. The proportion of volunteers with high levels of exposure was 22 % in 2012, and this reduction over the 13 years of assessment was statistically significant (v2 = 39.6262; df = 6; p(w) \ 0.0001). The proportion of volunteers with high levels of exposure in 2012 was significantly different compared with previous years, whereas the results of the remainder of the comparisons were not significant. Between 2003 and 2006, the concentration of total mercury significantly (p \ 0.05) declined in the hair of women who consumed more than 10 meals per week of fish (Fig. 3). The average total hair mercury concentration of women, who included fish in more than 10 meals per week was 1.184 ± 0.342 lg/g in 2003, varying from 0.638 to 1.631 lg/g, and in 2006 it dropped to 0.918 ± 0.505 lg/ g, varying from 0.176 to 1.544 lg/g.
Discussion
Fig. 2 Temporal distribution of the number of women of reproductive age relative to the tolerance limit of total mercury (THg) concentration (10 lg/g) in hair samples, Tapajo´s River area/PA (1999–2012)
pregnant women. Hair concentrations between 1 and 10 lg/g are within the margin of safety, but for some fetuses may be above minimal risk. Hair concentrations above 10 lg/g include acute and chronic risks.
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The present study was conducted in women of reproductive age from two riparian communities in the Tapajo´s River area, which is characterized by active gold extraction and a population that uses fish as its main dietary resource. The average total hair mercury concentration was calculated for the period from 1999 to 2012 and showed a progressive reduction over time. Nevertheless, the levels of exposure to mercury remain high and are above the tolerance limit in approximately 22 % of the women assessed in 2012. These high averages might be due to increased mercury contamination of the Tapajo´s River fishes because in addition to the natural sources of contamination, additional mercury derived from the gold-digging activity in the area. Approximately 500 tons of gold have been extracted in the Tapajo´s River area since 1980 (Veiga 1997). For that reason, a decrease in mercury levels has been observed since 1999, possibly due to a significant reduction in the gold-digging activity following the exhaustion of the
Bull Environ Contam Toxicol (2014) 93:42–46
45
Fig. 3 Proportions of women according to their weekly fish consumption in 2003 and 2006
known alluvial deposits and to technological difficulties in the exploitation of primary gold deposits. Gold production in the Tapajo´s River basin decreased from 98.2 tons in 1990 to 49 tons in 1998 (DNPM 1999). As has been observed in other studies (Pinheiro et al. 2000, 2003, 2006, 2012) conducted in riparian communities in the Tapajo´s River area, the present study also found high average mercury concentrations in the hair of volunteers from Barreiras and Sa˜o Luiz do Tapajo´s. The mercury concentrations in volunteers’ hair exceeded the tolerance limit established by the WHO despite the tendency for these concentrations to decrease over time. These findings are corroborated by the results of a meta-analysis of studies conducted in these same communities from 1996 to 2001, which showed that the highest average hair mercury concentration were identified in Sa˜o Luiz de Tapajo´s in 1996 (25 lg/g), which was followed by progressive reduction over time until reaching an average of 15.13 lg/g in 2001 (Sa´ et al. 2006). Such a significant reduction in the mercury levels in the Tapajo´s River area seems to represent a gradual tendency that will persist over time. This assumption is supported by the results of the present study, which showed that the average mercury concentration in the studied population was lower in 2012 compared with previous years. Nevertheless, the average total mercury concentration was still above the recommended upper limit in a significant proportion of women of reproductive age (22 %), with potential risk of fetal exposure if these women become pregnant. For this reason, monitoring mercury levels in women of reproductive age is of paramount importance, particularly for women with higher susceptibility due to the significant consumption of fish with high methylmercury content (Bjornberg et al. 2005; NRC 2000; WHO 1991). This is especially important due to dietary preferences for top predator fish species which generally bioaccumulate high levels of mercury and have been identified as the main
cause underlying the high levels of human exposure to mercury in Amazonian riparian communities (Akagi et al. 1995; Barbosa et al. 2000; Bidone et al. 1997). There was also a significant temporal reduction in fish consumption. While 62.97 % of the volunteers ate fish more than 10 times per week in 2003, this percentage had decreased to 52.18 % by 2006. Furthermore, even among women who still consumed fish more than 10 times per week, there was a significant reduction in the average total mercury concentration between 2003 and 2006 from 1.184 to 0.918 lg/g. In general, these findings indicated that both the diversification of their diets as well as a change in the pattern of dietary fish consumption to include more planktivorous species. Such species generally exhibit reduced mercury bioaccumulation relative to top predator species and thus contribute to lower levels of dietary exposure. Indeed, the last mentioned alteration from predatory to planktivorous fish was stimulated by the application of educational measures in the region. Therefore, we concluded that the exposure of riparian women of reproductive age to mercury in the Tapajo´s River area decreased from 1999 to 2012. However, despite a change in volunteers’ patterns of fish consumption, the average mercury levels found might still pose potential risks to reproduction and human health.
References Akagi H, Kinjo Y, Branches F, Malm O, Harada M, Pfeiffer W, Kato H (1995) Methylmercury pollution in Tapajo´s River Basin Amazon. Environ Sci 3:25–32 Amin-Zaki L, Elhassani S, Majeed MA, Clarkson TW, Doherty RA, Greenwood MR, Giovanoli-Jakubczak T (1976) Perinatal methylmercury poisoning in Iraq. Am J Dis Child 130:1070–1076 Amorim MIM, Mergler D, Bahia MO, Dubeau H, Miranda D, Lebel J, Burbano RR, Lucotte M (2000) Cytogenetic damage related to low levels of methylmercury contamination in the Brazilian Amazon. An Acad Bras Cieˆnc 72:497–507
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46 Ayres M, Ayres JRM, Ayres DL, Santos AS (2007) BioEstat 5,0— ´ reas das Cieˆncias Biolo´gicas e Aplicac¸o˜es Estatı´sticas nas A Me´dicas [Bioestat 5,0—Statistical Applications in the Biological and Medical Sciences]. Mamiraua´, Bele´m Barbosa AC, Souza J, Ferrari I, Dorea JG, Barretto F (2000) Mercury concentrations in fish of the Negro River Basin, Amazon, Brazil. International conference on heavy metals in the environment, Ann Arbor Bidone ED, Castilhos ZC, Santos TJS, Souza TMC, Lacerda LD (1997) Fish contamination and human exposure to mercury in Tartarugalzinho River. Amapa´ State Northern Amazon, Brazil: a screening approach. Water Air Soil Pollut 97:9–15 Bjornberg KA, Vahter M, Berglund B, Niklasson B, Blennow M, Sandborgh-Englund G (2005) Transport of methylmercury and inorganic mercury to the fetus and breast-fed infant. Environ Health Perspect 113:1381–1385 Crespo-Lo´pez ME, Maceˆdo GL, Pereira SI, Arrifano GP, Picanc¸oDiniz DL, Nascimento JL, Herculano AM (2009) Mercury and human genotoxicity: critical considerations and possible molecular mechanisms. Pharmacol Res 60:212–220 Fre´ry N, Maury-Brachet R, Maillot E, Deheeger M, Merona B, Boudou A (2001) Gold mining activities and mercury contamination of native Amerindian communities in French Guiana: key role of fish in dietary uptake. Environ Health Perspect 109:449–456 Lebel J, Roulet M, Mergler D, Lucotte M, Larribe F (1997) Fish diet and mercury exposure in a riparian Amazonian population. Water Air Soil Pollut 97:31–44 Lebel J, Mergler D, Branches F, Lucotte M, Amorim M, Larribe F, Dolbec J (1998) Neurotoxic effects of low-level methylmercury contamination in the Amazonian Basin. Environ Res 79:20–32 Lombardi G, Lanzirotti A, Qualls C, Socola F, Ali AM, Appenzeller O (2012) Five hundred years of mercury exposure and adaptation. J Biomed Biotechnol 2012:472858. doi:10.1155/2012/ 472858 Mahaffey KR (2005) Mercury exposure: medical and public health issues. Trans Am Clin Climatol Assoc 116:127–154 Malm O, Branches FJ, Akagi H, Castro MB, Pfeiffer WC, Harada M, Bastos WR, Kato H (1995) Mercury and methylmercury in fish and human hair from the Tapajo´s River Basin Brazil. Sci Total Environ 175:141–150 National Department of Mineral Production and Executive Secretariat of Industry, Commerce and Mining (1999) Mineral summary DNPM and SEICOM Bele´m Para´
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Bull Environ Contam Toxicol (2014) 93:42–46 National Reserch Council (NRC) (2000) Toxicological effects of methylmercury. National Academy Press, Washington, DC Nevado JJB, Rodrı´guez Martı´n-Doimeadios RC, Guzma´n Bernardo FJ, Jime´nez Moreno M, Herculano AM, Nascimento JL, CrespoLo´pez ME (2010) Mercury in the Tapajo´s River Basin Brazilian Amazon: a review. Environ Int 36:593–608 Pinheiro MCN, Guimaraes GA, Nakanishi J, Oikawa T, Vieira JL, Quaresma M, Cardoso B, Amoras W (2000) Assessment of mercury contamination through analysis of the total mercury content of samples of hair in riparian communities in the Tapajo´s River area Para´, Brazil. Rev Soc Bras Med Trop 33:181–184 Pinheiro MCN, Harada M, Yasoda E, Nakanishi J, Oikawa T, Vieira JFV, Costa SM, Guimaraes GA, Bacelar MDR, Almeida SS, Silveiras LCL (2003) Toxicological and epidemiological data on human exposure to mercury in the Tapajo´s River Basin: 1994–1998. Environ Sci 10:99–105 Pinheiro MC, Oikawa T, Vieira JL, Gomes MS, Guimara˜es GA, Crespo-Lo´pez ME, Mu¨ller RC, Amoras WW, Ribeiro DR, Rodrigues AR, Coˆrtes MI, Silveira LC (2006) Comparative study of human exposure to mercury in riverside communities in the Amazon Region. Braz J Med Biol Res 39:411–414 Pinheiro MC, Farripas SS, Oikawa T, Costa CA, Amoras WW, Vieira JL, Silveira AJ, Lima AC, Souza GS, Silveira LC (2012) Temporal evolution of exposure to mercury in riverside communities in the Tapajo´s Basin from 1994 to 2010. Bull Environ Contam Toxicol 89:119–124 Sa´ AL, Herculano AM, Pinheiro MC, Silveiras LCL, Nascimento JLM, Crespo-Lopez ME (2006) Human exposure to mercury in the western area of the state of Para´. Rev Para Med 20:19–25 Suzuki T (2004) Mercury analysis manual. Ministry of the Environment Japan, Tokyo Veiga MM (1997) Introducing new technologies for abatement of global mercury pollution in Latin America—Rio de Janeiro: UNIDO/UBC/CETEM/CNPq World Health Organization (WHO) and International Program in Chemical Safety (IPCS) (1990) Environmental health criteria 101: methylmercury. WHO, Geneva World Health Organization (WHO) and International Program in Chemical Safety (IPCS) (1991) Environmental health criteria 118: inorganic mercury. WHO, Geneva
Monitoring Mercury Exposure in Reproductive Aged Women Inhabiting the Tapajo´s River Basin, Amazon ´ rika Abdon Fiquene Oliveira • Tereza Cristina de Oliveira Corvelo • E Amanda Magno de Parijo´s • Claudia Simone Baltazar de Oliveira • Rosane do Socorro Pompeu de Loiola • Ame´lia A. de Arau´jo • Carlos Arau´jo da Costa Luiz Carlos de Lima Silveira • Maria da Conceic¸a˜o Nascimento Pinheiro
•
Received: 14 October 2013 / Accepted: 8 April 2014 / Published online: 1 May 2014 Ó Springer Science+Business Media New York 2014
Abstract Among Amazonian communities, exposure to methylmercury is associated mainly with fish consumption that may affect fetal development in pregnant women. Therefore a temporal assessment was performed to assess the exposure of reproductive aged women to mercury who reside in the riparian communities of Sa˜o Luı´s do Tapajo´s and Barreiras located in the Tapajo´s basin of the Brazilian Amazon from 1999 to 2012. The total mercury concentration in the 519 hair samples was assessed by cold vapor atomic absorption spectrometry. Data analysis showed that the average total mercury concentration decreased from 1.066 to 0.743 lg/g in those years. In 1999 the proportion of volunteers with mercury levels C10 lg/g was approximately 68 %. In general, exposure to mercury decreased among women of reproductive age, but the potential risks to reproduction and human health is still an issue as 22 % of the woman continued showing high mercury levels (C10 lg/g) in 2012. Keywords Exposure to mercury Women of reproductive age Tapajo´s River Fish consumption Mercury is an environmental pollutant arising from natural and anthropogenic sources. Methylation is particularly relevant in the transformation of mercury into its organic form, i.e., methylmercury. The primary source of mercury exposure for most humans is through the consumption of T. C. de Oliveira Corvelo (&) E´. A. F. Oliveira A. M. de Parijo´s C. S. B. de Oliveira R. do Socorro Pompeu de Loiola A. A. de Arau´jo C. A. da Costa L. C. de Lima Silveira M. da Conceic¸a˜o Nascimento Pinheiro Nu´cleo de Medicina Tropical, Universidade Federal do Para´, Av. Generalı´ssimo Deodoro, 92, Bele´m, Para´ CEP 66055-240, Brazil e-mail: [email protected]
123
contaminated fish. Approximately, 95 % of the total mercury in fish is in the form of methylmercury (Malm et al. 1995). Mercury is a neurotoxin that causes irreversible damage to the human nervous system, partly due to its chemical speciation and interactions with other metals in the environment and diet (Lombardi et al. 2012). The greatest damaging potential of methylmercury is associated with intrauterine development because it crosses the placenta and can reach levels in the fetal blood up to 25 % higher than in the maternal blood (Amin-Zaki et al. 1976). In the Amazonian ecosystem, contamination by mercury is associated with occupational exposure. However, the main source of exposure is organic mercury, which is acquired through food consumption (Lebel et al. 1997). The main food source of Amazonian communities is fish. In those communities, the average daily fish intake per individual is 340 g/day, which increases to more than 600 g/day in periods of abundance (Fre´ry et al. 2001). The average mercury levels in Amazonian predator fish vary from 0.04 to 3.77 lg/g per wet weight (revised in Nevado et al. 2010). Because methylmercury is excreted in human hair, and 80 % to 98 % of the mercury in the hair is in the form of methylmercury (Mahaffey 2005), hair is an excellent biological indicator for assessing and monitoring chronic exposure to mercury. Samples of hair collected in riparian communities in the Tapajo´s River area exhibit high mercury levels that can exceed the safety levels established by the World Health Organization (WHO). According to the latter, levels above 10 lg/g methylmercury in the mother’s hair are associated with a 5 % risk of neurological damage in newborns (WHO 1990). Although no typical case of Minamata disease has been reported yet in the Amazon area, mild clinical and/or
Bull Environ Contam Toxicol (2014) 93:42–46
neurophysiological changes are found in communities located along the Tapajo´s River, which can be associated with exposure to methylmercury through the consumption of fish (Lebel et al. 1998; Pinheiro et al. 2003). This situation is a source of concern, and the methylmercury levels of riparian women of reproductive age should be monitored to maintain the level of exposure below the tolerance limits and to avoid fetal exposure during pregnancy. This monitoring is recommended particularly because the upper tolerance limit of 10 lg/g is based on episodes of acute intoxication, in disagreement with to the long-term exposure to relatively low levels of mercury found in areas of the Tapajo´s basin. In these conditions, the likely toxic effects of mercury on the development of the central nervous system have not yet been fully elucidated (Amorim et al. 2000; Crespo-Lo´pez et al. 2009). Thus, these and other factors suggest the need to reassess the tolerance limits of mercury in human beings. The present study assessed the exposure level and accumulation of mercury in women of reproductive age as a potential risk to fetus during pregnancy from two communities in the Tapajo´s River area from 1999 to 2012.
43
for Tropical Medicine, and all of the volunteers signed an informed consent form. The data related to measuring the hair mercury concentrations of the investigated women were analyzed following logarithmic transformation to fit the data to a normal distribution. The data corresponding to the Sa˜o Luiz do Tapajo´s and Barreiras communities were analyzed separately and then combined because no difference was found between them. Descriptive statistics were used to analyze the distributions of the mercury exposure biomarker and the subjects’ ages. Fish consumption was included as a categorical variable. The chi- squared test was used to investigate the proportion of women with high levels of mercury in their hair using the WHO reference level as the threshold ([10 lg/g) (WHO 1990). The one-way analysis of variance (ANOVA) was applied to compare the means and standard errors of the total mercury concentrations in the volunteers’ hair over time from 1999 to 2012. All of the analyses were performed using the BioEstat 5.0 software (Ayres et al. 2007). The significance level was established at p \ 0.05.
Results Materials and Methods The present cross-sectional observational study assessed women of reproductive age, i.e., 12–46 years old, residing in two communities in the Tapajo´s River basin, Sa˜o Luı´s do Tapajo´s and Barreiras, which belong to the Itaituba district (04° 160 3400 S and 55° 590 0100 W), State of Para´Brazil. From 1999 to 2012, a total of 519 hair samples varying from 0.1 to 1 g were collected from the scalp at the occipital area. The total mercury (THg) concentration in hair was assessed by cold vapor atomic absorption spectrometry according to Akagi’s method, described in the Handbook of the Japanese Ministry of the Environment (Suzuki 2004). Quality control, including the precision and accuracy of these measurements, was investigated using the international reference standard IAEA 086 ([95 %). The laboratory of Environmental and Human Toxicology of the Center for Tropical Medicine of the Federal University of Para´ performed the hair analysis using an SP-3D mercury analyzer (Nippon Corporation, Tokyo, Japan). The subjects’ age, time of residence in the investigated locations, investigated year, dietary habits, and total hair mercury concentrations were collected from epidemiological questionnaires administered to each individual by researchers from the Center for Tropical Medicine in their annual visits to the investigated area. The study was approved by the research ethics committee of the Center
The average age of the reproductive age women residing at the investigated riparian communities of the Tapajo´s River ranged from 26 years in 1999 to 31 years in 2012. The average of the logarithm of the total mercury concentration in hair varied from 1.066 lg/g in 1999 to 0.743 lg/g in 2012, which represent the maximum and minimum mean values, respectively, for the investigated period (Table 1). Therefore, the average total mercury concentration significantly decreased (F(regression) = 21.5815; p = 0.0063) during the investigated period from 1999 to 2012 (Fig. 1). The differential variation of this decrease occurred between the estimate corresponding to 1999 and the estimates corresponding to the period from 2005 and 2009 as well as between the estimates corresponding to 1999/2009 and the estimate corresponding to 2012 (one-way ANOVA; LSD test; F = 6.9410; p \ 0.0001). The above-mentioned data were also assessed relative to the tolerance limit of total mercury in the hair established by the WHO (1990) for human beings ([10 lg/g). The temporal distribution of the exposure of women to mercury from 1999 to 2012 expressed as the percentage of hair samples with total mercury concentrations C10 lg/g is displayed in Fig. 2. On the other hand, a reference dose for MeHg of 0.1 lg/kg per day has been established by the US Environmental Protection Agency and has been reviewed by the National Academy of Sciences (NRC 2000). In the way, hair concentrations \1 lg/g represent minimal risk to
123
44 Table 1 Descriptive statistics of the age and total mercury (THg) concentration (log units) variables in the hair of women in the Tapajo´s River area/PA, 1999–2012
Bull Environ Contam Toxicol (2014) 93:42–46
Year
Number of cases
Age (years) X ± SE (min–max)
THg (lg/g) X ± SE (min–max)
1999
75
26.07 ± 1.06 (13–46)
1.07 ± 0.034 (0.39 to 1.63)
2001
90
28.81 ± 0.89 (13–46)
1.00 ± 0.035 (-0.17 to 1.89)
2003
85
28.79 ± 0.94 (12–46)
1.03 ± 0.031 (0.12 to 1.52)
2005
85
28.31 ± 0.88 (14–46)
0.94 ± 0.04 (-0.15 to 1.46)
2007
65
29.52 ± 0.97 (13–46)
0.89 ± 0.06 (-0.69 to 1.62)
2009
45
33.91 ± 0.75 (21–45)
0.94 ± 0.04 (0.29 to 1.43)
2012
74
31.12 ± 0.94 (14–46)
0.74 ± 0.05 (-1.69 to 1.55)
Fig. 1 Progression of the average total mercury (THg) concentration (log units) in hair samples of women in the Tapajo´s River area/PA over time (1999–2012)
The proportion of volunteers with mercury levels above the recommended levels (i.e., C10 lg/g) from 1999 to 2003 was approximately 61 %. That level decreased, on average, to 47 % from 2005 to 2010. The proportion of volunteers with high levels of exposure was 22 % in 2012, and this reduction over the 13 years of assessment was statistically significant (v2 = 39.6262; df = 6; p(w) \ 0.0001). The proportion of volunteers with high levels of exposure in 2012 was significantly different compared with previous years, whereas the results of the remainder of the comparisons were not significant. Between 2003 and 2006, the concentration of total mercury significantly (p \ 0.05) declined in the hair of women who consumed more than 10 meals per week of fish (Fig. 3). The average total hair mercury concentration of women, who included fish in more than 10 meals per week was 1.184 ± 0.342 lg/g in 2003, varying from 0.638 to 1.631 lg/g, and in 2006 it dropped to 0.918 ± 0.505 lg/ g, varying from 0.176 to 1.544 lg/g.
Discussion
Fig. 2 Temporal distribution of the number of women of reproductive age relative to the tolerance limit of total mercury (THg) concentration (10 lg/g) in hair samples, Tapajo´s River area/PA (1999–2012)
pregnant women. Hair concentrations between 1 and 10 lg/g are within the margin of safety, but for some fetuses may be above minimal risk. Hair concentrations above 10 lg/g include acute and chronic risks.
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The present study was conducted in women of reproductive age from two riparian communities in the Tapajo´s River area, which is characterized by active gold extraction and a population that uses fish as its main dietary resource. The average total hair mercury concentration was calculated for the period from 1999 to 2012 and showed a progressive reduction over time. Nevertheless, the levels of exposure to mercury remain high and are above the tolerance limit in approximately 22 % of the women assessed in 2012. These high averages might be due to increased mercury contamination of the Tapajo´s River fishes because in addition to the natural sources of contamination, additional mercury derived from the gold-digging activity in the area. Approximately 500 tons of gold have been extracted in the Tapajo´s River area since 1980 (Veiga 1997). For that reason, a decrease in mercury levels has been observed since 1999, possibly due to a significant reduction in the gold-digging activity following the exhaustion of the
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Fig. 3 Proportions of women according to their weekly fish consumption in 2003 and 2006
known alluvial deposits and to technological difficulties in the exploitation of primary gold deposits. Gold production in the Tapajo´s River basin decreased from 98.2 tons in 1990 to 49 tons in 1998 (DNPM 1999). As has been observed in other studies (Pinheiro et al. 2000, 2003, 2006, 2012) conducted in riparian communities in the Tapajo´s River area, the present study also found high average mercury concentrations in the hair of volunteers from Barreiras and Sa˜o Luiz do Tapajo´s. The mercury concentrations in volunteers’ hair exceeded the tolerance limit established by the WHO despite the tendency for these concentrations to decrease over time. These findings are corroborated by the results of a meta-analysis of studies conducted in these same communities from 1996 to 2001, which showed that the highest average hair mercury concentration were identified in Sa˜o Luiz de Tapajo´s in 1996 (25 lg/g), which was followed by progressive reduction over time until reaching an average of 15.13 lg/g in 2001 (Sa´ et al. 2006). Such a significant reduction in the mercury levels in the Tapajo´s River area seems to represent a gradual tendency that will persist over time. This assumption is supported by the results of the present study, which showed that the average mercury concentration in the studied population was lower in 2012 compared with previous years. Nevertheless, the average total mercury concentration was still above the recommended upper limit in a significant proportion of women of reproductive age (22 %), with potential risk of fetal exposure if these women become pregnant. For this reason, monitoring mercury levels in women of reproductive age is of paramount importance, particularly for women with higher susceptibility due to the significant consumption of fish with high methylmercury content (Bjornberg et al. 2005; NRC 2000; WHO 1991). This is especially important due to dietary preferences for top predator fish species which generally bioaccumulate high levels of mercury and have been identified as the main
cause underlying the high levels of human exposure to mercury in Amazonian riparian communities (Akagi et al. 1995; Barbosa et al. 2000; Bidone et al. 1997). There was also a significant temporal reduction in fish consumption. While 62.97 % of the volunteers ate fish more than 10 times per week in 2003, this percentage had decreased to 52.18 % by 2006. Furthermore, even among women who still consumed fish more than 10 times per week, there was a significant reduction in the average total mercury concentration between 2003 and 2006 from 1.184 to 0.918 lg/g. In general, these findings indicated that both the diversification of their diets as well as a change in the pattern of dietary fish consumption to include more planktivorous species. Such species generally exhibit reduced mercury bioaccumulation relative to top predator species and thus contribute to lower levels of dietary exposure. Indeed, the last mentioned alteration from predatory to planktivorous fish was stimulated by the application of educational measures in the region. Therefore, we concluded that the exposure of riparian women of reproductive age to mercury in the Tapajo´s River area decreased from 1999 to 2012. However, despite a change in volunteers’ patterns of fish consumption, the average mercury levels found might still pose potential risks to reproduction and human health.
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