Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Toenail manganese as biomarker of drinking water exposure: a reliability study from a US pregnancy cohort

Abstract

Manganese (Mn) is an essential nutrient; however, overexposure can be neurotoxic. Recent evidence suggests that exposure to Mn from drinking water could be neurotoxic; however, research is hampered by the lack of consensus on a reliable biomarker of Mn exposure. Naturally high concentrations of Mn can occur in groundwater, particularly for private, unregulated water systems. This study aimed to investigate the association between exposure to Mn from drinking water with a relatively low Mn content (median of 2.9 μg/L; range, undetectable–8,340 μg/L) and Mn in toenails from women collected at two time points: during and after pregnancy. Mn concentrations in the paired toenail samples gathered during the second to third trimester of pregnancy and 2 weeks postpartum were correlated (r = 0.47, p < 0.001, n= 596). Among women consuming drinking water Mn in the highest tertile (i.e., > 9.8 μg/L) significant positive correlations were found between water Mn and toenails Mn (r = 0.31 and r = 0.38, for toenail samples collected during pregnancy and postpartum, respectively), whereas little to no correlation was observed at lower water concentrations. Overall, our data suggest that maternal toenail samples are a reliable environmental Mn exposure biomarker and reflect exposure from drinking water.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. ATSDR. Toxicological profile for manganese. 2012; available from: https://www.atsdr.cdc.gov/toxprofiles/tp151.pdf.

  2. Freeland-Graves JH, Mousa TY, Kim S. International variability in diet and requirements of manganese: causes and consequences. J Trace Elem Med Biol. 2016;38:24–32.

    Article  CAS  Google Scholar 

  3. Chung SE, Cheong H-KK, Ha E-HH, Kim B-NN, Ha M, Kim Y, et al. Maternal blood manganese and early neurodevelopment: The mothers and children’s environmental health (MOCEH) study. Environ Health Perspect. 2015;123:717–22.

    Article  CAS  Google Scholar 

  4. Keen CL, Ensunsa JL, Watson MH, Baly DL, Donovan SM, Monaco MH, et al. Nutritional aspects of manganese from experimental studies. Neurotoxicology. 1999;20:213–23.

    CAS  PubMed  Google Scholar 

  5. Takser L, Lafond J, Bouchard M, St-Amour G, Mergler D. Manganese levels during pregnancy and at birth: relation to environmental factors and smoking in a Southwest Quebec population. Environ Res. 2004;95:119–25.

    Article  CAS  Google Scholar 

  6. Claus Henn B, Austin C, Coull BA, Schnaas L, Gennings C, Horton MK, et al. Uncovering neurodevelopmental windows of susceptibility to manganese exposure using dentine microspatial analyses. Environ Res. 2018;161:588–98.

    Article  CAS  Google Scholar 

  7. Henn BC, Ettinger AS, Schwartz J, Téllez-Rojo MM, Lamadrid-Figueroa H, Hernández-Avila M, et al. Early postnatal blood manganese levels and children’s neurodevelopment. Epidemiology. 2010;21:433–9.

    Article  Google Scholar 

  8. Takeda A. Manganese action in brain function. Brain Res Brain Res Rev. 2003;41:79–87.

    Article  CAS  Google Scholar 

  9. Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Asp Med. 2005;26:353–62.

    Article  CAS  Google Scholar 

  10. Chen P, Bornhorst J, Aschner M. Manganese metabolism in humans. Front Biosci. 2018;23:1655–79.

    Article  CAS  Google Scholar 

  11. Federal-Provincial-Territorial Commitee on Drinking water. Manganese in drinking water [Internet]. 2016. Available from: http://publications.gc.ca/collections/collection_2017/sc-hc/H144-44-2016-eng.pdf.

  12. Chang Y, Kim Y, Woo S-T, Song H-J, Kim SH, Lee H, et al. High signal intensity on magnetic resonance imaging is a better predictor of neurobehavioral performances than blood manganese in asymptomatic welders. Neurotoxicology. 2009;30:555–63.

    Article  CAS  Google Scholar 

  13. Bouchard M, Mergler D, Baldwin M, Panisset M, Roels HA. Neuropsychiatric symptoms and past manganese exposure in a ferro-alloy plant. Neurotoxicology. 2007;28:290–7.

    Article  CAS  Google Scholar 

  14. Olanow CW. Manganese-induced parkinsonism and Parkinson’s disease. Ann N Y Acad Sci. 2004;1012:209–23.

    Article  CAS  Google Scholar 

  15. Laohaudomchok W, Lin X, Herrick RF, Fang SC, Cavallari JM, Christiani DC, et al. Toenail, blood, and urine as biomarkers of manganese exposure. J Occup Environ Med. 2011;53:506–10.

    Article  CAS  Google Scholar 

  16. Ward EJ, Edmondson DA, Nour MM, Snyder S, Rosenthal FS, Dydak U. Toenail manganese: a sensitive and specific biomarker of exposure to manganese in career welders. Ann Work Expo Heal. 2017;62:101–11.

    Article  Google Scholar 

  17. Bouchard MF, Sauvé S, Barbeau B, Legrand M, Brodeur M-ÈÈ, Bouffard T, et al. Intellectual impairment in school-age children exposed to manganese from drinking water. Environ Health Perspect. 2011;119:138–43.

    Article  CAS  Google Scholar 

  18. Khan K, Factor-Litvak P, Wasserman GA, Liu X, Ahmed E, Parvez F, et al. Manganese exposure from drinking water and children’s classroom behavior in bangladesh. Environ Health Perspect. 2011;119:1501–6.

    Article  CAS  Google Scholar 

  19. Khan K, Wasserman GA, Liu X, Ahmed E, Parvez F, Slavkovich V, et al. Manganese exposure from drinking water and children’s academic achievement. Neurotoxicology. 2012;33:91–7.

    Article  CAS  Google Scholar 

  20. Oulhote Y, Mergler D, Barbeau B, Bellinger DC, Bouffard T, Brodeur M-È, et al. Neurobehavioral function in school-age children exposed to manganese in drinking water. Environ Health Perspect. 2014;122:1343–50.

    Article  CAS  Google Scholar 

  21. Kondakis XG, Makris N, Leotsinidis M, Prinou M, Papapetropoulos T. Possible health effects of high manganese concentration in drinking water. arch environ heal. Arch Environ Health. 1989;44:175–8.

    Article  CAS  Google Scholar 

  22. Wasserman GA, Liu X, Parvez F, Ahsan H, Levy D, Factor-Litvak P, et al. Water manganese exposure and children’s intellectual function in Araihazar, Bangladesh. Environ Health Perspect. 2006;114:124–9.

    Article  CAS  Google Scholar 

  23. Bouchard M, Laforest F, Vandelac L, Bellinger D, Mergler D. Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water. Environ Health Perspect. 2007;115:122–7.

    Article  CAS  Google Scholar 

  24. Frisbie SH, Mitchell EJ, Dustin H, Maynard DM, Sarkar B. World health organization discontinues its drinking-water guideline for manganese. Environ Health Perspect. 2012;120:775–8.

    Article  CAS  Google Scholar 

  25. EPA. 2012 Edition of the Drinking Water Standards and Health Advisories (EPA 822-S-12-001). Available from: https://www.epa.gov/sites/production/files/2015-09/documents/dwstandards2012.pdf.

  26. Smith D, Gwiazda R, Bowler R, Roels H, Park R, Taicher C, et al. Biomarkers of Mn exposure in humans. Am J Ind Med. 2007;50:801–11.

    Article  CAS  Google Scholar 

  27. Ntihabose R, Surette C, Foucher D, Clarisse O, Bouchard MF Assessment of saliva, hair and toenails as biomarkers of low level exposure to manganese from drinking water in children. Neurotoxicology. 2017;64:126–33.

    Article  CAS  Google Scholar 

  28. Agusa T, Kunito T, Fujihara J, Kubota R, Minh TB, Kim Trang PT, et al. Contamination by arsenic and other trace elements in tube-well water and its risk assessment to humans in Hanoi, Vietnam. Environ Pollut. 2006;139:95–106.

    Article  CAS  Google Scholar 

  29. Bader M, Dietz MC, Ihrig A, Triebig G. Biomonitoring of manganese in blood, urine and axillary hair following low-dose exposure during the manufacture of dry cell batteries. Int Arch Occup Environ Health. 1999;72:521–7.

    Article  CAS  Google Scholar 

  30. He P, Liu DH, Zhang GQ. Effects of high-level-manganese sewage irrigation on children’s neurobehavior. Zhonghua Yu Fang Yi Xue Za Zhi. 1994;28:216–8.

    CAS  PubMed  Google Scholar 

  31. Coetzee DJ, McGovern PM, Rao R, Harnack LJ, Georgieff MK, Stepanov I. Measuring the impact of manganese exposure on children’s neurodevelopment: advances and research gaps in biomarker-based approaches. Environ Health. 2016;15:1–20.

    Article  Google Scholar 

  32. Esteban M, Castaño A. Non-invasive matrices in human biomonitoring: a review. Environ Int. 2009;35:438–49.

    Article  CAS  Google Scholar 

  33. Michalke B, Fernsebner K. New insights into manganese toxicity and speciation. J Trace Elem Med Biol. 2014;28:106–16.

    Article  CAS  Google Scholar 

  34. Viana GF, de S, Carvalho CF, de, Nunes LS, Rodrigues JLG, Ribeiro NS, et al. Noninvasive biomarkers of manganese exposure and neuropsychological effects in environmentally exposed adults in Brazil. Toxicol Lett. 2014;231:169–78.

    Article  CAS  Google Scholar 

  35. Sriram K, Lin GX, Jefferson AM, Roberts JR, Andrews RN, Kashon ML, et al. Manganese accumulation in nail clippings as a biomarker of welding fume exposure and neurotoxicity. Toxicology. 2012;291:73–82.

    Article  CAS  Google Scholar 

  36. Farzan SF, Korrick S, Li Z, Enelow R, Gandolfi AJ, Madan J, et al. In utero arsenic exposure and infant infection in a United States cohort: a prospective study. Environ Res. 2013;126:24–30.

    Article  CAS  Google Scholar 

  37. Gilbert-Diamond D, Cottingham KL, Gruber JF, Punshon T, Sayarath V, Gandolfi AJ, et al. Rice consumption contributes to arsenic exposure in US women. Proc Natl Acad Sci USA. 2011;108:20656–60.

    Article  CAS  Google Scholar 

  38. R Core Team. R: A Language and Enrionment for Statistical Computing, R Foundation for Statisical Computing. Vienna; 2014.

  39. EPA US. Drinking Water Regulations and Contaminant [Internet]. Available from: https://www.epa.gov/dwregdev/drinking-water-regulations-and-contaminants.

  40. Ayotte JD, Belaval M, Olson SA, Burow KR, Flanagan SM, Hinkle SR, et al. Factors affecting temporal variability of arsenic in groundwater used for drinking water supply in the United States. Sci Total Environ. 2015;505:1370–9.

    Article  CAS  Google Scholar 

  41. Claus Henn B, Schnaas L, Ettinger AS, Schwartz J, Lamadrid-Figueroa H, Hernández-Avila M, et al. Associations of early childhood manganese and lead coexposure with neurodevelopment. Environ Health Perspect. 2011;120:126–31.

    Article  Google Scholar 

  42. Takser L, Mergler D, Hellier G, Sahuquillo J, Huel G. Manganese, onoamine metabolite levels at birth, and child Psychomotor development. Neurotoxicology. 2003;24:667–74.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded in part by the US National Institutes of Environmental Health Sciences grant P01ES022832 and P42ES007373 and the RD83544201 from the US EPA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonio J. Signes-Pastor.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Signes-Pastor, A.J., Bouchard, M.F., Baker, E. et al. Toenail manganese as biomarker of drinking water exposure: a reliability study from a US pregnancy cohort. J Expo Sci Environ Epidemiol 29, 648–654 (2019). https://doi.org/10.1038/s41370-018-0108-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41370-018-0108-z

Keywords

This article is cited by

Search

Quick links