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
Subscribe to this journal
Receive 6 print issues and online access
$259.00 per year
only $43.17 per issue
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
Similar content being viewed by others
References
ATSDR. Toxicological profile for manganese. 2012; available from: https://www.atsdr.cdc.gov/toxprofiles/tp151.pdf.
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.
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.
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.
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.
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.
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.
Takeda A. Manganese action in brain function. Brain Res Brain Res Rev. 2003;41:79–87.
Aschner JL, Aschner M. Nutritional aspects of manganese homeostasis. Mol Asp Med. 2005;26:353–62.
Chen P, Bornhorst J, Aschner M. Manganese metabolism in humans. Front Biosci. 2018;23:1655–79.
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.
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.
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.
Olanow CW. Manganese-induced parkinsonism and Parkinson’s disease. Ann N Y Acad Sci. 2004;1012:209–23.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Esteban M, Castaño A. Non-invasive matrices in human biomonitoring: a review. Environ Int. 2009;35:438–49.
Michalke B, Fernsebner K. New insights into manganese toxicity and speciation. J Trace Elem Med Biol. 2014;28:106–16.
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.
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.
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.
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.
R Core Team. R: A Language and Enrionment for Statistical Computing, R Foundation for Statisical Computing. Vienna; 2014.
EPA US. Drinking Water Regulations and Contaminant [Internet]. Available from: https://www.epa.gov/dwregdev/drinking-water-regulations-and-contaminants.
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.
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.
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.
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
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41370-018-0108-z
Keywords
This article is cited by
-
Periconceptional and Prenatal Exposure to Metals and Extracellular Vesicle and Particle miRNAs in Human Milk: A Pilot Study
Exposure and Health (2023)
-
A State-of-the-Science Review on Metal Biomarkers
Current Environmental Health Reports (2023)
-
Metal-mixtures in toenails of children living near an active industrial facility in Los Angeles County, California
Journal of Exposure Science & Environmental Epidemiology (2021)
-
Exposure to a Mixture of Metals and Growth Indicators in 6–11-Year-Old Children from the 2013–2016 NHANES
Exposure and Health (2021)