Skip to main content
Log in

Heterogeneity of Multimedia Exposures to Neurotoxic Elements (Al, As, Cd, Pb, Mn, and Hg) in Breastfed Infants from Porto Velho, Brazil

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Infant exposure to neurotoxic elements is a public health issue that needs monitoring with regard to breast milk composition. We studied six neurotoxic elements in breast milk samples at different stages of lactation in mothers from Porto Velho, Brazil. We used a flow-injection mercury system (FIMS) to determine total Hg concentrations and an inductively coupled plasma optical emission spectrometer (ICP-OES) to determine the concentrations of Al, As, Cd, Pb, and Mn in 106 donors of a human milk bank. Association rules analyses were applied to determine the pattern of binary and ternary mixtures of the measured exposants. The metal concentration was mostly below the limit of detection (LOD) for Cd (99%), Pb (84%), and Hg (72%), and it was above the LOD for As (53%), Mn (60%), and Al (82%), respectively. Median concentrations (dry weight) of Al, As, Hg, Mn, and Pb were 1.81 μg/g, 13.8 ng/g, 7.1 ng/g, 51.1 ng/g, and 0.43 μg/g, respectively. Al is singly the most frequent element to which infants are exposed. Occurring binary combination (> LOD) was 56% for Al-Mn, 41% for Al-As, 22% for Al-Hg, and 13% for Al-Pb. In 100% of neonates, exposure to Al-ethylmercury (EtHg) occurred through immunization with thimerosal-containing vaccines (TCV). Association rules analysis revealed that Al was present in all of the multilevel combinations and hierarchical levels and that it showed a strong link with other neurotoxic elements (especially with Mn, As, and Hg). (a) Nursing infants are exposed to combinations of neurotoxicants by different routes, dosages, and at different stages of development; (b) In breastfed infants, the binary exposures to Al and total Hg can occur through breast milk and additionally through TCV (EtHg and Al); (c) The measured neurotoxic elements were found at low frequencies in breast milk and at concentrations that pose no public health concerns for milk banking.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. WHO (2003) World Health Organisation, Global strategy for infant and young child feeding. WHO, Geneva

    Google Scholar 

  2. Almeida SG, Dórea JG (2006) Quality control of banked milk in Brasilia, Brazil. J Hum Lact 2:335–339

    Article  Google Scholar 

  3. Vahter M, Berglund M, Akesson A, Lidén C (2002) Metals and women’s health. Environ Res 88:145–155

    Article  CAS  PubMed  Google Scholar 

  4. Esteban M, Castano A (2009) Non-invasive matrices in human biomonitoring: a review. Environ Int 35:438–449

    Article  CAS  PubMed  Google Scholar 

  5. Callan AC, Winters M, Barton C, Boyce M, Hinwood AL (2012) Children's exposure to metals: a community-initiated study. Arch Environ Contam Toxicol 62:714–722

    Article  CAS  PubMed  Google Scholar 

  6. Weidenhamer JD, Fitzpatrick MP, Biro AM, Kobunski PA, Hudson MR, Corbin RW, Gottesfeld P (2017) Metal exposures from aluminum cookware: an unrecognized public health risk in developing countries. Sci Total Environ 579:805–813

    Article  CAS  PubMed  Google Scholar 

  7. Concha G, Vogler G, Lezcano D, Nermell B, Vahter M (1998a) Exposure to inorganic arsenic metabolites during early human development. Toxicol Sci 44:185–190

    Article  CAS  PubMed  Google Scholar 

  8. Iyengar GV, Rapp A (2001) Human placenta as a ‘dual’ biomarker for monitoring fetal and maternal environment with special reference to potentially toxic trace elements. Part 3: toxic trace elements in placenta and placenta as a biomarker for these elements. Sci Total Environ 280:221–238

    Article  CAS  PubMed  Google Scholar 

  9. Rudge CV, Röllin HB, Nogueira CM, Thomassen Y, Rudge MC, Odland JØ (2009) The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J Environ Monit 11:1322–1330

    Article  CAS  PubMed  Google Scholar 

  10. Marques RC, Bernardi JV, Dórea JG, de Fatima R, Moreira M, 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

    Article  CAS  PubMed  Google Scholar 

  11. Bansa DK, Awua AK, Boatin R, Adom T, Brown-Appiah EC, Amewosina KK, Diaba A, Datoghe D, Okwabi W (2017) Cross-sectional assessment of infants’ exposure to toxic metals through breast milk in a prospective cohort study of mining communities in Ghana. BMC Public Health 17:505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kostial K, Kello D, Jugo S, Rabar I, Maljković T (1978) Influence of age on metal metabolism and toxicity. Environ Health Perspect 25:81–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Marchitti SA, LaKind JS, Naiman DQ, Berlin CM, Kenneke JF (2013) Improving infant exposure and health risk estimates: using serum data to predict polybrominated diphenyl ether concentrations in breast milk. Environ Sci Technol 47:4787–4795

    Article  CAS  PubMed  Google Scholar 

  14. Rebelo FM, Caldas ED (2016) Arsenic, lead, mercury and cadmium: toxicity, levels in breast milk and the risks for breastfed infants. Environ Res 151:671–688

    Article  CAS  PubMed  Google Scholar 

  15. Walker SP, Wachs TD, Grantham-McGregor S, Black M, Nelson CA, Huffman SL, Baker-Henningham H, Chang SM, Hamadani JD, Lozoff B, Gardner JM, Powell CA, Rahman A, Richter L (2011) Inequality in early childhood: risk and protective factors for early child development. Lancet 378:1325–1338

    Article  PubMed  Google Scholar 

  16. Claus-Henn B, Coull BA, Wright RO (2014) Chemical mixtures and children’s health. Curr Opin Pediatr 26:223–229

    Article  CAS  PubMed  Google Scholar 

  17. Dórea JG (2017) Low-dose thimerosal in pediatric vaccines: adverse effects in perspective. Environ Res 152:280–293

    Article  CAS  PubMed  Google Scholar 

  18. Dórea JG (2017) Abating mercury exposure in young children should include thimerosal-free vaccines. Neurochem Res. https://doi.org/10.1007/s11064-017-2277-x

  19. Dórea JG (2015) Exposure to mercury and aluminum in early life: developmental vulnerability as a modifying factor in neurologic and immunologic effects. Int J Environ Res Public Health 12:1295–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. von Stackelberg K, Guzy E, Chu T, Claus Henn B (2015) Exposure to mixtures of metals and neurodevelopmental outcomes: a multidisciplinary review using an adverse outcome pathway framework. Risk Anal 35:971–1016

    Article  Google Scholar 

  21. Silva PR, Dorea JG, Boaventura GR (1997) Multielement determination in small samples of human milk by inductively coupled plasma atomic emission spectrometry. Biol Trace Elem Res 59:57–62

    Article  CAS  PubMed  Google Scholar 

  22. Kira CS, Maihara VA (2007) Determination of major and minor elements in dairy products through inductively coupled plasma optical emission spectrometry after wet partial digestion and neutron activation analysis. Food Chem 100:390–395

    Article  CAS  Google Scholar 

  23. Birghila S, Dobrinas S, Stanciu G, Soceanu A (2008) Determination of major and minor elements in milk through ICP-AES. Environ Eng Manag J 7:805–808

    Article  CAS  Google Scholar 

  24. Vieira SM, de Almeida R, Holanda IB, Mussy MH, Galvão RC, Crispim PT, Dórea JG, Bastos WR (2013) Total and methyl-mercury in hair and milk of mothers living in the city of Porto Velho and in villages along the Rio Madeira, Amazon, Brazil. Int J Hyg Environ Health 216:682–689

    Article  CAS  PubMed  Google Scholar 

  25. Malm O, Pfeiffer WC, Bastos WR, Souza CMM (1989) Utilização do Acessório de Geração de Vapor Frio para Análise de Mercúrio em Investigações Ambientais por Espectrofotometria de Absorção Atômica. Ciênc Cult 41:88–92

    CAS  Google Scholar 

  26. Bastos WR, Malm O, Pfeiffer WC, Cleary D (1998) Establishment and analytical quality control of laboratories for Hg determination in biological and geological samples in the Amazon, Brasil. Ciênc Cult 50:255–260

    CAS  Google Scholar 

  27. Agrawal R, Srikant R (1994) Fast algorithms for mining association rules. In Proceedings of the 20th int. conf. very large data bases, (VLDB). 1215:487-499

  28. Han J, Fu Y (1999) Mining multiple-level association rules in large databases. IEEE Trans Knowl Data Eng 11:798–805

    Article  Google Scholar 

  29. Dórea JG, Marques RC (2010) Infants’ exposure to aluminium from vaccines and breast milk during the first 6 months. J Expo Sci Environ Epidemiol 20:598–601

    Article  CAS  PubMed  Google Scholar 

  30. Santoro W, Martinez FE, Ricco RG, Jorge SM (2010) Colostrum ingested during the first day of life by exclusively breastfed healthy newborn infants. J Pediatr 156:29–32

    Article  PubMed  Google Scholar 

  31. Dórea JG, Marques RC, Brandão KG (2009) Brandão, Neonate exposure to thimerosal mercury from hepatitis B vaccines. Am J Perinatol 26:523–527

    Article  PubMed  Google Scholar 

  32. Marques RC, Dórea JG, Fonseca MF, Bastos WR, Malm O (2007) Hair mercury in breast-fed infants exposed to thimerosal-preserved vaccines. Eur J Pediatr 166:935–941

    Article  CAS  PubMed  Google Scholar 

  33. Rahbar MH, Samms-Vaughan M, Dickerson AS, Hessabi M, Bressler J, Desai CC, Shakespeare-Pellington S, Reece JA, Morgan R, Loveland KA, Grove ML, Boerwinkle E (2015) Concentration of lead, mercury, cadmium, aluminum, arsenic and manganese in umbilical cord blood of Jamaican newborns. Int J Environ Res Public Health 12:4481–4501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Björnberg 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kopp RS, Kumbartski M, Harth V, Brüning T, Käfferlein HU (2012) Partition of metals in the maternal/fetal unit and lead-associated decreases of fetal iron and manganese: an observational biomonitoring approach. Arch Toxicol 86:1571–1581

    Article  CAS  PubMed  Google Scholar 

  36. Concha G, Vogler G, Nermell B, Vahter M (1998b) Low-level arsenic excretion in breast milk of native Andean woman exposed to high levels of arsenic in drinking water. Int Arch Environ Health 71:42–46

    Article  CAS  Google Scholar 

  37. Rossipal E, Krachler M, Li F, Micetic-Turk D (2000) Investigation of the transport of trace elements across barriers in humans: studies of placental and mammary transfer. Acta Paediatr 89:1190–1195

    Article  CAS  PubMed  Google Scholar 

  38. Sharma R, Pervez S (2005) Toxic metals status in human blood and breast milk samples in an integrated steel plant environment in Central India. Environ Geochem Health 27:39–45

    Article  CAS  PubMed  Google Scholar 

  39. Gibson MA, Sarpong-Kumankomah S, Nehzati S, George GN, Gailer J (2017) Remarkable differences in the biochemical fate of Cd(2+), Hg(2+), CH(3)Hg(+) and thimerosal in red blood cell lysate. Metallomics. https://doi.org/10.1039/c7mt00069c

  40. Prato E, Biandolino F (2007) Combined toxicity of mercury, copper and cadmium on embryogenesis and early larval stages of the Mytilus galloprovincialis. Environ Technol 28:915–920

    Article  CAS  PubMed  Google Scholar 

  41. Björklund KL, Vahter M, Palm B, Grandér M, Lignell S, Berglund M (2012) Metals and trace element concentrations in breast milk of first time healthy mothers: a biological monitoring study. Environ Health 11:92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Matos C, Moutinho C, Almeida C, Guerra A, Balcão V (2014) Trace element compositional changes in human milk during the first four months of lactation. Int J Food Sci Nutr 65:547–551

    Article  CAS  PubMed  Google Scholar 

  43. Chao HH, Guo CH, Huang CB, Chen PC, Li HC, Hsiung DY, Chou YK (2014) Arsenic, cadmium, lead, and aluminium concentrations in human milk at early stages of lactation. Pediatr Neonatol 55:127–134

    Article  PubMed  Google Scholar 

  44. Sun Z, Yue B, Yang Z, Li X, Wu Y, Yin S (2013) Determination of 24 minerals inhuman milk by inductively coupled plasma mass spectrometry with microwave digestion. Wei Sheng Yan Jiu 42:504–509

    CAS  PubMed  Google Scholar 

  45. Bellés M, Albina ML, Sánchez DJ, Corbella J, Domingo JL (2002) Interactions in developmental toxicology: effects of concurrent exposure to lead, organic mercury, and arsenic in pregnant mice. Arch Environ Contam Toxicol 42:93–98

    Article  CAS  PubMed  Google Scholar 

  46. Gibson MA, Sarpong-Kumankomah S, Nehzati S, George GN, Gailer J (2017) Remarkable differences in the biochemical fate of Cd(2+), Hg(2+), CH(3)Hg(+) and thimerosal in red blood cell lysate. Metallomics 9:1060–1072

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank CT-Universal and INCT-INPeTAm/CNPq/MCT for the support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José G. Dórea.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bastos, W.R., Vieira, S.M., Manzatto, Â.G. et al. Heterogeneity of Multimedia Exposures to Neurotoxic Elements (Al, As, Cd, Pb, Mn, and Hg) in Breastfed Infants from Porto Velho, Brazil. Biol Trace Elem Res 184, 7–15 (2018). https://doi.org/10.1007/s12011-017-1165-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-017-1165-1

Keywords

Navigation