Abstract
Methylmercury (from fresh-water fish) and ethylmercury [from thimerosal-containing vaccines (TCVs)] are the most prevalent source of neurotoxic exposure during early life in families consuming fish and using these vaccines. But children living in Amazonian mining environments are exposed to additional toxic metals in waste materials. We studied mercury (Hg) exposure and neurodevelopment in 294 children (105 boys and 189 girls) from Bom Futuro (Rondonia, Brazil), the epicenter of a tin-ore open-pit mine. Hair-Hg (HHg) concentrations and total ethylmercury (from TCVs) were taken from infants and respective mothers during pregnancy. We used bivariate analysis to determine the effect of sex and linear mixed models to assess the association of prenatal and postnatal organic Hg exposures with children’s Bayley Scales of Infant Development (BSID) as psychomotor developmental index and mental developmental index (MDI) at 6 and 24 months of age as well as milestones achievements (age of walking and age of talking). Significant differences between boys and girls were observed for both MDI score (p = 0.0073) and MDI score (p = 0.0288) at 6 months but not at 24 months. Regression analysis showed that only in boys was there a significant interaction between MDI score with family income (β = 0.288, p = 0.018) and with birth weight (β = −0.216, p = 0.036) at 6 months; at 24 months, however, only boys showed a significant association of both MDI score (β = −0.222, p = 0.045) and MDI score (β = −0.222, p = 0.045) with neonatal HHg. In boys, age of walking was associated with HHg (β = 0.188, p = 0.019) and breastfeeding (β = −0.282, p = 0.000), whereas for girls, age of walking was only associated with breastfeeding (β = −0.275, p = 0.001). In this mining environment, with only a weak association for prenatal Hg exposure, there was a significant sex difference in neurodevelopment, with boys showing more sensitivity related to BSID delays.
Similar content being viewed by others
References
Ashraf MA, Maah MJ, Yusoff I (2012) Chemical speciation and potential mobility of heavy metals in the soil of former tin mining catchment. Sci World J 2012:125608
Barbieri FL, Cournil A, Sarkis JES, Bénéfice E, Gardon J (2011) Hair trace elements concentration to describe polymetallic mining waste exposure in Bolivian Altiplano. Biol Trace Elem Res 139:10–23
Barbosa AC, Silva SR, Dórea JG (1998) Concentration of mercury in hair of indigenous mothers and infants from the Amazon basin. Arch Environ Contam Toxicol 34:100–105
Bayley N (1993) Bayley scales of infant development II. Harcourt Brace, Antonio
Caravanos J, Ericson B, Ponce-Canchihuamán J, Hanrahan D, Block M, Susilorini B et al (2013) Rapid assessment of environmental health risks posed by mining operations in low- and middle-income countries: selected case studies. Environ Sci Pollut Res Int 20:7711–7718
Cernichiari E, Brewer R, Myers GJ, Marsh DO, Lapham LW, Cox C et al (1995) Monitoring methylmercury during pregnancy: maternal hair predicts fetal brain exposure. Neurotoxicology 16:705–710
Cernichiari E, Myers GJ, Ballatori N, Zareba G, Vyas J, Clarkson T (2007) The biological monitoring of prenatal exposure to methylmercury. Neurotoxicology 28:1015–1022
Chevrier C, Sullivan K, White RF, Comtois C, Cordier S, Grandjean P (2009) Qualitative assessment of visuospatial errors in mercury-exposed Amazonian children. Neurotoxicology 30:37–46
Choi AL, Cordier S, Weihe P, Grandjean P (2008) Negative confounding in the evaluation of toxicity: the case of methylmercury in fish and seafood. Crit Rev Toxicol 38:877–893
Counter SA (2003) Neurophysiological anomalies in brainstem responses of mercury-exposed children of Andean gold miners. J Occup Environ Med 45:87–95
Counter SA, Buchanan LH, Ortega F, Laurell G (2002) Elevated blood mercury and neuro-otological observations in children of the Ecuadorian gold mines. J Toxicol Environ Health A 65:149–163
Counter SA, Buchanan LH, Ortega F (2006) Neurocognitive screening of mercury-exposed children of Andean gold miners. Int J Occup Environ Health 12(3):209–214
Davidson PW, Myers GJ, Cox C, Axtell C, Shamlaye C, Sloane-Reeves J et al (1998) Effects of prenatal and postnatal methylmercury exposure from fish consumption on neurodevelopment: outcomes at 66 months of age in the Seychelles Child Development Study. JAMA 280:701–707
Davidson PW, Leste A, Benstrong E, Burns CM, Valentin J, Sloane-Reeves J et al (2010) Fish consumption, mercury exposure, and their associations with scholastic achievement in the Seychelles Child Development Study. Neurotoxicology 31:439–447
Dórea JG (2009) Comparing fish-mercury exposed Amazonian children: should not we consider thimerosal-preserved vaccines? Neurotoxicology 30:485–486
Dórea JG (2011) Integrating experimental (in vitro and in vivo) neurotoxicity studies of low-dose thimerosal relevant to vaccines. Neurochem Res 36(6):927–938
Dórea JG (2013) Low-dose mercury exposure in early life: relevance of thimerosal to fetuses, newborns and infants. Curr Med Chem 20:4060–4069
Dórea JG, Marques RC (2010) Infants’ exposure to aluminum from vaccines and breast milk during the first 6 months. J Expo Sci Environ Epidemiol 20:598–601
Dórea JG, Marques RC, Isejima C (2012) Neurodevelopment of Amazonian infants: antenatal and postnatal exposure to methyl- and ethylmercury. J Biomed Biotechnol 2012:132876
Dórea JG, Farina M, Rocha JB (2013) Toxicity of ethylmercury (and Thimerosal): a comparison with methylmercury. J Appl Toxicol 33:700–711
Dórea JG, Marques RC, Abreu L (2014) Milestone achievement and neurodevelopment of rural Amazonian toddlers (12 to 24 months) with different methylmercury and ethylmercury exposure. J Toxicol Environ Health A 77:1–13
Grandjean P, Landrigan PJ (2006) Developmental neurotoxicity of industrial chemicals. Lancet 368(9553):2167–2178
Heron J, Golding J, ALSPAC Study Team (2004) Thimerosal exposure in infants and developmental disorders: a prospective cohort study in the United Kingdom does not support a causal association. Pediatrics 114:577–613
Hibbeln JR, Davis JM, Steer C, Emmett P, Rogers I, Williams C et al (2007) Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 369:578–615
Jedrychowski W, Perera F, Jankowskic J, Rauh V, Flaka E, Caldwell KL et al (2007) Fish consumption in pregnancy, cord blood mercury level and cognitive and psychomotor development of infants followed over the first three years of life: Krakow epidemiologic study. Environ Int 33:1057–1062
Krupskaya LT, Derbentseva AM, Nesterova OV, Nazarkina AV, Shchapova LN, Morin VA (2013) Soil contamination in the zone affected by waste products of tin ore processing in the Khabarovsk region. Eur Soil Sci 46:337–340
Lederman SA, Jones RL, Caldwell KL, Rauh V, Sheets SE, Tang D et al (2008) Relation between cord blood mercury levels and early child development in a World Trade Center cohort. Environ Health Perspect 116(8):1085–1091
Lee BE, Ha EH (2012) Response to commentary ‘‘Co-exposure and confounders during neurodevelopmentt: we need them in the bigger picture of secondhand smoke exposure during pregnancy”. Environ Res 112:235
Marques RC, Dórea JG, Fonseca MF, Bastos WR, Malm O (2007a) Hair mercury in breast-fed infants exposed to thimerosal-preserved vaccines. Eur J Pediatr 166:935–941
Marques RC, Dórea JG, Manzatto AG, Bastos WR, Bernardi JV, Malm O (2007b) Time of perinatal immunization, thimerosal exposure and neurodevelopment at 6 months in breastfed infants. Acta Paediatr 96:864–868
Marques RC, Dórea JG, Bernardi JV, Bastos WR, Malm O (2009) Prenatal and postnatal mercury exposure, breastfeeding and neurodevelopment during the first 5 years. Cogn Behav Neurol 22(2):134–141
Marques RC, Dórea JG, Bernardi JV (2010) Thimerosal exposure (from tetanus-diphtheria vaccine) during pregnancy and neurodevelopment of breastfed infants at six months. Acta Paediatr 99:934–939
Marques RC, Dórea JG, McManus C, Leão RS, Brandão KG, Marques RC et al (2011) Hydroelectric reservoir inundation (Rio Madeira Basin, Amazon) and changes in traditional lifestyle: impact on growth and neurodevelopment of pre-school children. Public Health Nutr 14:661–669
Marques RC, Dórea JG, Leão RS, Dos Santos VG, Bueno L, Marques RC et al (2012) Role of methylmercury exposure (from fish consumption) on growth and neurodevelopment of children under 5 years of age living in a transitioning (tin-mining) area of the western Amazon, Brazil. Arch Environ Contam Toxicol 62:341–350
Marques RC, Bernardi JV, Dórea JG, Leão RS, Malm O (2013a) Mercury transfer during pregnancy and breastfeeding: hair mercury concentrations as biomarker. Biol Trace Elem Res 154:326–332
Marques RC, Moreira Mde F, Bernardi JV, Dórea JG (2013b) Breast milk lead concentrations of mothers living near tin smelters. Bull Environ Contam Toxicol 91:549–554
Marques RC, Bernardi JV, Dórea JG, Brandão KG, Bueno L, Leão RS et al (2013c) Fish consumption during pregnancy, mercury transfer, and birth weight along the Madeira River Basin in Amazonia. Int J Environ Res Public Health 10:2150–2163
Marques RC, Bernardi JV, Dórea JG, Moreira MF, Malm O (2014) Perinatal multiple exposure to neurotoxic (lead, methylmercury, ethylmercury, and aluminum) substances and neurodevelopment at six and 24 months of age. Environ Pollut 187:130–135
Mergler D (2012) Neurotoxic exposures and effects: gender and sex matter! Hänninen Lecture 2011. Neurotoxicology 33:644–651
Mrozek-Budzyn D, Majewska R, Kieltyka A, Augustyniak M (2012) Neonatal exposure to Thimerosal from vaccines and child development in the first 3 years of life. Neurotoxicol Teratol 34:592–597
Oken E, Østerdal ML, Gillman MW, Knudsen VK, Halldorsson TI, Strøm M et al (2008) Associations of maternal fish intake during pregnancy and breastfeeding duration with attainment of developmental milestones in early childhood: a study from the Danish National Birth Cohort. Am J Clin Nutr 88:789–796
Oliveira RC, Dórea JG, Bernardi JV, Bastos WR, Almeida R, Manzatto AG (2010) Fish consumption by traditional subsistence villagers of the Rio Madeira (Amazon): impact on hair mercury. Ann Hum Biol 37:629–642
Plumlee GS, Durant JT, Morman SA, Neri A, Wolf RE, Dooyema CA et al (2013) Linking geological and health sciences to assess childhood lead poisoning from artisanal gold mining in Nigeria. Environ Health Perspect 121:744–750
Plusquellec P, Muckle G, Dewailly E, Ayotte P, Bégin G, Desrosiers C et al (2010) The relation of environmental contaminants exposure to behavioral indicators in Inuit preschoolers in Arctic Quebec. Neurotoxicology 31:17–25
Riojas-Rodríguez H, Solís-Vivanco R, Schilmann A, Montes S, Rodríguez S, Ríos C et al (2010) Intellectual function in Mexican children living in a mining area and environmentally exposed to manganese. Environ Health Perspect 118:1465–1470
Rooney JP (2014) The retention time of inorganic mercury in the brain—a systematic review of the evidence. Toxicol Appl Pharmacol 274:425–435
Ruiz-Castell M, Paco P, Barbieri FL, Duprey JL, Forns J, Carsin AE et al (2012) Child neurodevelopment in a Bolivian mining city. Environ Res 112:147–154
Sagiv SK, Thurston SW, Bellinger DC, Amarasiriwardena C, Korrick SA (2012) Prenatal exposure to mercury and fish consumption during pregnancy and attention-deficit/hyperactivity disorder-related behavior in children. Arch Pediatr Adolesc Med 166:1123–1131
Sanfeliu C, Sebastià J, Cristòfol R, Rodríguez-Farré E (2003) Neurotoxicity of organomercurial compounds. Neurotoxicol Res 5:283–305
Santos EJ, Herrmann AB, Santos AB, Baika LM, Sato CS, Tormen L et al (2010) Determination of thimerosal in human and veterinarian vaccines by photochemical vapor generation coupled to ICP OES. J Anal Atmos Spectrom 25:1627–1632
Tang D, Li TY, Liu JJ, Zhou ZJ, Yuan T, Chen YH et al (2008) Effects of prenatal exposure to coal-burning pollutants on children’s development in China. Environ Health Perspect 116:674–679
Weiss B (2011) Same sex, no sex, and unaware sex in neurotoxicology. Neurotoxicology 32:509–517
Acknowledgments
This study was supported by a CNPq/MCT grant (Project Nos. 555516/2006-7, 575573/2008-2, and 478575/2009-2). We greatly appreciate the participation of the mothers. We also thank the students and staff of the University of Rondonia. We are grateful to the staff, especially the community health staff, of the Health Secretariat of the State of Rondonia.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marques, R.C., Bernardi, J.V.E., Abreu, L. et al. Neurodevelopment Outcomes in Children Exposed to Organic Mercury from Multiple Sources in a Tin-Ore Mine Environment in Brazil. Arch Environ Contam Toxicol 68, 432–441 (2015). https://doi.org/10.1007/s00244-014-0103-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-014-0103-x