Skip to main content
SpringerLink
Log in

Postnatal exposure to mercury and neuropsychological development among preschooler children

  • DEVELOPMENTAL EPIDEMIOLOGY
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

The objective of this study was to describe the postnatal exposure to Hg and to evaluate its association with neuropsychological development among preschool children. The study population are 4–5 years old children (n = 1252) participant in the Spanish INMA Project. Total Hg was measured in cord blood and in hair samples taken at 4 years of age (2008–2012). Neuropsychological development was assessed using the McCarthy Scales of Children’s Abilities (MSCA). Information on covariates and possible confounders was obtained by questionnaires during pregnancy and childhood. Generalized additive and linear regression models were built in order to assess the relationship between MSCA scores and Hg exposure. We also evaluated the magnitude of the possible bias generated from measurement error in seafood intake estimate from questionnaire and Hg determination. The geometric mean of hair Hg was 0.98 µg/g [95% confidence interval (CI) 0.94, 1.03]. In the regression analysis, the association between Hg and the MSCA scores was positive for all the scales and statistically significant for the verbal (β = 0.89; 95%CI 0.38, 1.39), memory (β = 0.42; 95%CI 0.09, 0.76) and general cognitive scales (β = 1.35; 95%CI 0.45, 2.25). However, these associations were clearly attenuated when we adjusted by the children’s fish intake variables or when took into account theoretical scenarios of low precision in fish intake and Hg measurements. Hg levels in this Spanish population were high in comparison with other European countries; however, we did not observe adverse effects on child neuropsychological development associated with this postnatal exposure to Hg.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368:2167–78.

    CAS  PubMed  Google Scholar 

  2. Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108(Suppl 3):511–33.

    PubMed  PubMed Central  Google Scholar 

  3. Ginsberg G, Hattis D, Sonawane B. Incorporating pharmacokinetic differences between children and adults in assessing children’s risks to environmental toxicants. Toxicol Appl Pharmacol. 2004;198:164–83.

    CAS  PubMed  Google Scholar 

  4. Grandjean P, Landrigan PJ. Neurobehavioural effects of developmental toxicity. Lancet Neurol. 2014;13:330–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Domingo JL, Bocio A, Falcó G, Llobet JM. Benefits and risks of fish consumption Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology. 2007;230:219–26.

    CAS  PubMed  Google Scholar 

  6. Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. 2006;296:1885–99.

    CAS  PubMed  Google Scholar 

  7. Bjornberg KA, Vahter M, Petersson-Grawe K, Glynn A, Cnattingius S, Darnerud PO, et al. Methyl mercury and inorganic mercury in Swedish pregnant women and in cord blood: influence of fish consumption. Environ Health Perspect. 2003;111:637–41.

    PubMed  PubMed Central  Google Scholar 

  8. Freire C, Ramos R, Lopez-Espinosa MJ, Diez S, Vioque J, Ballester F, et al. Hair mercury levels, fish consumption, and cognitive development in preschool children from Granada, Spain. Environ Res. 2010;110:96–104.

    CAS  PubMed  Google Scholar 

  9. Miklavcic A, Casetta A, Snoj TJ, Mazej D, Krsnik M, Mariuz M, et al. Mercury, arsenic and selenium exposure levels in relation to fish consumption in the Mediterranean area. Environ Res. 2013;120:7–17.

    CAS  PubMed  Google Scholar 

  10. Ramon R, Murcia M, Aguinagalde X, Amurrio A, Llop S, Ibarluzea J, et al. Prenatal mercury exposure in a multicenter cohort study in Spain. Environ Int. 2011;37:597–604.

    CAS  PubMed  Google Scholar 

  11. Schoeman K, Tanaka T, Bend JR, Koren G. Hair mercury levels of women of reproductive age in Ontario, Canada: implications to fetal safety and fish consumption. J Pediatr. 2010;157:127–31.

    CAS  PubMed  Google Scholar 

  12. Steuerwald U, Weihe P, Jorgensen PJ, Bjerve K, Brock J, Heinzow B, et al. Maternal seafood diet, methylmercury exposure, and neonatal neurologic function. J Pediatr. 2000;136:599–605.

    CAS  PubMed  Google Scholar 

  13. Institute of Medicine (IOM). Seafood choices, balancing benefits and risks. Committee on nutrient relationships in seafood: selections to balance benefits and risks. 2006.

  14. Llop S, Murcia M, Aguinagalde X, Vioque J, Rebagliato M, Cases A, et al. Exposure to mercury among Spanish preschool children: trend from birth to age four. Environ Res. 2014;132C:83–92.

    Google Scholar 

  15. Llop S, Guxens M, Murcia M, Lertxundi A, Ramon R, Riano I, et al. Prenatal exposure to mercury and infant neurodevelopment in a multicenter cohort in Spain: study of potential modifiers. Am J Epidemiol. 2012;175:451–65.

    PubMed  Google Scholar 

  16. Llop S, Ballester F, Murcia M, Forns J, Tardon A, Andiarena A, et al. Prenatal exposure to mercury and neuropsychological development in young children: the role of fish consumption. Int J Epidemiol. 2016;46:827–38.

    Google Scholar 

  17. Guxens M, Ballester F, Espada M, Fernandez MF, Grimalt JO, Ibarluzea J, et al. Cohort profile: the INMA—Infancia y Medio Ambiente—(Environment and Childhood) Project. Int J Epidemiol. 2012;41:930–40.

    PubMed  Google Scholar 

  18. McCarthy D. MSCA. Escalas McCarthy de Aptitudes y Psicomotricidad para Niños. Madrid: TEA Ediciones; 2009.

    Google Scholar 

  19. Vioque J, Navarrete-Munoz EM, Gimenez-Monzo D, Garcia-de-la-Hera M, Granado F, Young IS, et al. Reproducibility and validity of a food frequency questionnaire among pregnant women in a Mediterranean area. Nutr J. 2013;12:26.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Vioque J, Gimenez-Monzo D, Navarrete-Muñoz EM, Garcia-de-la-Hera M, Gonzalez-Palacios S, Rebagliato M, et al. Reproducibility and validity of a food frequency questionnaire designed to assess diet in children aged 4–5 years. PLoS ONE. 2016;11:e0167338.

    PubMed  PubMed Central  Google Scholar 

  21. World Health Organization (WHO). Evaluation of certain food additives and contaminants. Sixty-first of the joint FAO/WHO experte committee on food additives. 2004.

  22. Budtz-Jorgensen E, Grandjean P, Weihe P. Separation of risks and benefits of seafood intake. Environ Health Perspect. 2007;115:323–7.

    PubMed  Google Scholar 

  23. Grandjean P, Budtz-Jorgensen E, Jorgensen PJ, Weihe P. Umbilical cord mercury concentration as biomarker of prenatal exposure to methylmercury. Environ Health Perspect. 2005;113:905–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Grandjean P, Budtz-Jorgensen E. Total imprecision of exposure biomarkers: implications for calculating exposure limits. Am J Ind Med. 2007;50:712–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Rosseel Y. Lavaan: an R package for structural equation modelling. J Stat Softw. 2012;48:1–36.

    Google Scholar 

  26. Budtz-Jorgensen E, Grandjean P, Keiding N, White RF, Weihe P. Benchmark dose calculations of methylmercury-associated neurobehavioural deficits. Toxicol Lett. 2000;112–113:193–9.

    PubMed  Google Scholar 

  27. US Environmental Protection Agency. Mercury. Human Exposure. 2007.

  28. United Nations Environment Programme. Mercury programme. 2007.

  29. Gari M, Grimalt JO, Torrent M, Sunyer J. Influence of socio-demographic and diet determinants on the levels of mercury in preschool children from a Mediterranean island. Environ Pollut. 2013;182C:291–8.

    Google Scholar 

  30. Forysová K, Pinkr-Grafnetterová A, Malý M, Krsková A, Mráz J, Kašparová L, et al. Urinary cadmium and cotinine levels and hair mercury levels in czech children and their mothers within the framework of the COPHES/DEMOCOPHES projects. Arch Environ Contam Toxicol. 2017;73:421–30.

    PubMed  Google Scholar 

  31. Mørck TA, Nielsen F, Nielsen JKS, Jensen JF, Hansen PW, Hansen AK, et al. The Danish contribution to the European DEMOCOPHES project: a description of cadmium, cotinine and mercury levels in Danish mother–child pairs and the perspectives of supplementary sampling and measurements. Environ Res. 2015;141:96–105.

    PubMed  Google Scholar 

  32. Deroma L, Parpinel M, Tognin V, Channoufi L, Tratnik J, Horvat M, et al. Neuropsychological assessment at school-age and prenatal low-level exposure to mercury through fish consumption in an Italian birth cohort living near a contaminated site. Int J Hyg Environ Health. 2013;216:486–93.

    CAS  PubMed  Google Scholar 

  33. Evrenoglou L, Partsinevelou SA, Stamatis P, Lazaris A, Patsouris E, Kotampasi C, et al. Children exposure to trace levels of heavy metals at the north zone of Kifissos River. Sci Total Environ. 2013;443C:650–61.

    Google Scholar 

  34. Welch AA, Lund E, Amiano P, Dorronsoro M, Brustad M, Kumle M, et al. Variability of fish consumption within the 10 European countries participating in the European Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2002;5:1273–85.

    CAS  PubMed  Google Scholar 

  35. Davidson PW, Myers GJ, Cox C, Axtell C, Shamlaye C, Sloane-Reeves J, et al. 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. 1998;280:701–7.

    CAS  PubMed  Google Scholar 

  36. Grandjean P, Weihe P, Debes F, Choi AL, Budtz-Jorgensen E. Neurotoxicity from prenatal and postnatal exposure to methylmercury. Neurotoxicol Teratol. 2014;43:39–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Choi AL, Cordier S, Weihe P, Grandjean P. Negative confounding in the evaluation of toxicity: the case of methylmercury in fish and seafood. Crit Rev Toxicol. 2008;38:877–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Julvez J, Mendez M, Fernandez-Barres S, Romaguera D, Vioque J, Llop S, et al. Maternal consumption of seafood in pregnancy and child neuropsychological development: a longitudinal study based on a population with high consumption levels. Am J Epidemiol. 2016;183:169–82.

    PubMed  Google Scholar 

  39. Debes F, Budtz-Jorgensen E, Weihe P, White RF, Grandjean P. Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicol Teratol. 2006;28:363–75.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Murata K, Weihe P, Budtz-Jorgensen E, Jorgensen PJ, Grandjean P. Delayed brainstem auditory evoked potential latencies in 14-year-old children exposed to methylmercury. J Pediatr. 2004;144:177–83.

    CAS  PubMed  Google Scholar 

  41. Selevan SG, Kimmel CA, Mendola P. Identifying critical windows of exposure for children’s health. Environ Health Perspect. 2000;108(Suppl 3):451–5.

    PubMed  PubMed Central  Google Scholar 

  42. González L, Cortés-Sancho R, Murcia M, Ballester F, Rebagliato M, Rodríguez-Bernal CL. The role of parental social class, education and unemployment on child cognitive development. Gac Sanit. 2020;34:51–60.

    PubMed  Google Scholar 

  43. Clarkson TW, Strain JJ. Nutritional factors may modify the toxic action of methyl mercury in fish-eating populations. J Nutr. 2003;133:1539S–43S.

    CAS  PubMed  Google Scholar 

  44. Davidson PW, Cory-Slechta DA, Thurston SW, Huang L-S, Shamlaye CF, Gunzler D, et al. Fish consumption and prenatal methylmercury exposure: cognitive and behavioral outcomes in the main cohort at 17 years from the Seychelles child development study. Neurotoxicology. 2011;32:711–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Golding J, Hibbeln JR, Gregory SM, Iles-Caven Y, Emond A, Taylor CM. Maternal prenatal blood mercury is not adversely associated with offspring IQ at 8 years provided the mother eats fish: a British prebirth cohort study. Int J Hyg Environ Health. 2017;220:1161–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Ralston NV, Raymond LJ. Dietary selenium’s protective effects against methylmercury toxicity. Toxicology. 2010;278:112–23.

    CAS  PubMed  Google Scholar 

  47. Després C, Beuter A, Richer F, Poitras K, Veilleux A, Ayotte P, et al. Neuromotor functions in Inuit preschool children exposed to Pb, PCBs, and Hg. Neurotoxicol Teratol. 2005;27:245–57.

    PubMed  Google Scholar 

  48. Saint-Amour D, Roy M-S, Bastien C, Ayotte P, Dewailly E, Després C, et al. Alterations of visual evoked potentials in preschool Inuit children exposed to methylmercury and polychlorinated biphenyls from a marine diet. Neurotoxicology. 2006;27:567–78.

    CAS  PubMed  Google Scholar 

  49. Plusquellec P, Muckle G, Dewailly E, Ayotte P, Begin G, Desrosiers C, et al. The relation of environmental contaminants exposure to behavioral indicators in Inuit preschoolers in Arctic Quebec. Neurotoxicology. 2010;31:17–25.

    CAS  PubMed  Google Scholar 

  50. Gustin K, Tofail F, Mehrin F, Levi M, Vahter M, Kippler M. Methylmercury exposure and cognitive abilities and behavior at 10 years of age. Environ Int. 2017;102:97–105.

    CAS  PubMed  Google Scholar 

  51. Tavares LMB, Câmara VM, Malm O, Santos EC. Performance on neurological development tests by riverine children with moderate mercury exposure in Amazonia, Brazil. Cad Saude Publica. 2005;21:1160–7.

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors would particularly like to thank all the participants for their generous collaboration. A full roster of the INMA Project Investigators can be found at http://www.proyectoinma.org/proyecto-inma/investigadores/.

Funding

This study was funded by grants from European Union (FP7-ENV-2011 cod 282957 and HEALTH.2010.2.4.5-1), Spain: Instituto Carlos III (Red INMA G03/176; CB06/02/0041; FIS-FEDER: PI03/1615, PI04/1509, PI04/1436, PI04/1112, PI04/1931, PI05/1079, PI05/1052, PI06/0867, PI06/1213, PI07/0314, PI081151, PI09/00090, PI09/02647, PI11/01007, PI11/02591, PI11/02038, PI12/00610, PI13/02187, PI13/1944, PI13/2032, PI14/00108, PI14/00891, PI14/01687, PI16/00261, PI16/1288, PI17/00663, and PI19/1338; Miguel Servet-FSE: MS11/0178, MS15/0025, MSII16/0051, MSII19/00015; Miguel Servet-FEDER: CP11/0178 and CP15/0025, co-funded by European Regional Development Fund ‘A way to make Europe’), CIBERESP, Generalitat de Catalunya (CIRIT 1999SGR 00241 and AGAUR 2009 SGR 501), Fundació La marató de TV3 (090430), EU Commission (261357), Generalitat Valenciana, FISABIO (UGP 15-230, UGP-15-244, and UGP-15-249), Department of Health of the Basque Government (2005111093, 2009111069, 2013111089 and 2015111065), the Provincial Government of Gipuzkoa (DFG06/002, DFG08/001 and DFG15/221), annual agreements with the municipalities of the study area (Zumarraga, Urretxu, Legazpi, Azkoitia y Azpeitia y Beasain), and Alicia Koplowitz Foundation 2017. ISGlobal is a member of the CERCA Programme, Generalitat de Catalunya.

Author information

Authors and Affiliations

  1. Epidemiology and Environmental Health Joint Research Unit, Foundation for the Promotion of Health and Biomedical Research in the Valencian Region, FISABIO-Public Health, FISABIO–Universitat Jaume I–Universitat de València, Av. Catalunya 21, 46020, Valencia, Spain

    Sabrina Llop, Mario Murcia, Raquel Soler-Blasco, Marisa Rebagliato, Carmen Iñiguez, Maria-Jose Lopez-Espinosa, Llúcia Gonzalez & Ferran Ballester

  2. Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Av. Monforte de Lemos, 3-5. Pabellón 11, 28029, Madrid, Spain

    Sabrina Llop, Mario Murcia, Jordi Julvez, Loreto Santa-Marina, Marisa Rebagliato, Carmen Iñiguez, Maria-Jose Lopez-Espinosa, Llúcia Gonzalez, Jesús Vioque, Jordi Sunyer & Ferran Ballester

  3. School of Mathematics, University of Edinburgh, Peter Guthrie Tait Road, Edinburgh, EH9 3FD, UK

    Rubén Amorós

  4. Institut d’Investigació Sanitària Pere Virgili (IISPV), Hospital Universitari Sant Joan de Reus, Reus, Spain

    Jordi Julvez

  5. Barcelona Institute for Global Health (ISGlobal), Dr. Aiguader 88, 08003, Barcelona, Spain

    Jordi Julvez & Jordi Sunyer

  6. Municipal Institute of Medical Research, IMIM-Hospital del Mar, Dr. Aiguader 88, 08003, Barcelona, Spain

    Jordi Julvez & Jordi Sunyer

  7. Universitat Pompeu Fabra (UPF), Plaça de la Mercè 10-12, 08002, Barcelona, Spain

    Jordi Julvez & Jordi Sunyer

  8. Health Department of Basque Government, Sub-directorate of Public Health of Gipuzkoa, 20013, San Sebastián, Spain

    Loreto Santa-Marina

  9. Biodonostia Health Research Institute, Group of Environmental Epidemiology and Child Development, Doctor Begiristain, s/n, 20014, San Sebastián, Spain

    Loreto Santa-Marina & Ainara Andiarena

  10. Department of Medicine, Universitat Jaume I, Avenida de Vicent Sos Baynat s/n, 12071, Castellón de la Plana, Spain

    Marisa Rebagliato

  11. Laboratorio de Salud Pública de Alava, Santiago 11, 01002, Vitoria Gasteiz, Spain

    Xabier Aguinagalde & Gorka Iriarte

  12. Nursing School, Universitat de València, C/Jaume Roig s/n, 46010, Valencia, Spain

    Maria-Jose Lopez-Espinosa & Ferran Ballester

  13. Faculty of Psychology, University of the Basque Country, Tolosa Hiribidea 70, 20018, San Sebastián, Spain

    Ainara Andiarena

  14. Universidad Miguel Hernandez, Avenida de Alicante KM 87, 03550, Sant Joan d’Alacant, Spain

    Jesús Vioque

Authors
  1. Sabrina Llop
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mario Murcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rubén Amorós
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jordi Julvez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loreto Santa-Marina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raquel Soler-Blasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marisa Rebagliato
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carmen Iñiguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xabier Aguinagalde
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gorka Iriarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maria-Jose Lopez-Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ainara Andiarena
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Llúcia Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jesús Vioque
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jordi Sunyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Ferran Ballester
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sabrina Llop.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Hospital La Fe in Valencia, the Institut Municipal d’Assistència Sanitaria in Barcelona, Comité Ético de Investigación Clínica del Hospital Donostia, and Comité Ético de Investigación Clínica del Área Sanitaria de Gipuzkoa) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 415 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Llop, S., Murcia, M., Amorós, R. et al. Postnatal exposure to mercury and neuropsychological development among preschooler children. Eur J Epidemiol 35, 259–271 (2020). https://doi.org/10.1007/s10654-020-00620-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-020-00620-9

Keywords

Search

Navigation