Elsevier

NeuroToxicology

Volume 64, January 2018, Pages 118-125
NeuroToxicology

Full length article
Changes in water manganese levels and longitudinal assessment of intellectual function in children exposed through drinking water

https://doi.org/10.1016/j.neuro.2017.08.015Get rights and content

Highlights

  • Longitudinal assessment of relations between Mn exposure from tap water and IQ.

  • Higher water Mn levels are associated with lower IQ in girls.

  • Higher water Mn levels are associated with higher IQ in boys at adolescence.

  • Decreased IQ scores in participants whose water Mn increased between examinations.

Abstract

Background

Manganese is commonly found in water but potential neurotoxic effects from exposure through drinking water are poorly understood. We previously reported a cross-sectional study showing that drinking water Mn concentration was associated with lower IQ in children aged 6 to 13 years.

Objective

For this follow-up study, we aimed to re-assess the relation between exposure to Mn from drinking water and IQ at adolescence. In addition, we aimed to examine whether changes in drinking water Mn concentration was associated with changes in IQ scores.

Methods

From the 380 children enrolled in the baseline study, 287 participated to this follow-up study conducted in average 4.4 years after. Mn concentration was measured in home tap water and children's hair. The relationships between these Mn exposure indicators and IQ scores (Weschsler Abbreviated Scale of Intelligence) at follow-up were assessed with linear regression analysis, adjusting for potential confounders. Intra-individual differences in IQ scores between the two examinations were compared for children whose Mn concentration in water remained stable between examinations, increased or decreased.

Results

The mean age at follow-up was 13.7 years (range, 10.5 to 18.0 years). Geometric mean of Mn concentration in water at follow-up was 14.5 μg/L. Higher Mn concentration in water measured at follow-up was associated with lower Performance IQ in girls (β for a 10-fold increase = −2.8, 95% confidence intervals [CI] −4.8 to −0.8) and higher Performance IQ in boys (β = 3.9, 95% CI 1.4 to 6.4). IQ scores were not significantly associated with Mn concentration in hair, although similar trends as for concentration in water were observed. For children whose Mn concentration in water increased between baseline and follow-up, Performance IQ scores decreased significantly (intra-individual difference, −2.4 points).

Conclusion

Higher levels of Mn in drinking water were associated with lower Performance IQ in girls, whereas the opposite was observed in boys. These findings suggest long-term exposure to Mn through drinking water is associated differently with cognition in boys and girls.

Introduction

Manganese (Mn) is an essential element that occurs naturally in soil, air, as well as in all living organisms. This metal is also commonly present in groundwater, sometimes in high concentrations, due to local geological characteristics. High Mn concentration have been reported in drinking water in many countries around the world where groundwater is used for human consumption (Frisbie et al., 2012), including Canada (Barbeau et al., 2011). Mn is an essential nutrient, but in large dose can also be a potent neurotoxicant, with effects on cognition, behavior, and neuromotor function (Dobson et al., 2004). Early studies depicting the neurotoxic effects of Mn were conducted in occupationally exposed groups (Mergler et al., 1994, Rodier, 1955, Roels et al., 1987), and more recently increased efforts were made to investigate Mn neurotoxicity in environmentally exposed children (O'Neal and Zheng, 2015).

Epidemiological evidence suggests that Mn exposure from drinking water could be associated with lower intelligence quotient (IQ) scores in children (Bouchard et al., 2011, Wasserman et al., 2006). Drinking water Mn concentrations has also been associated with poorer memory, attention, motor functions (Oulhote et al., 2014a), mathematics achievement scores (Khan et al., 2012), perceptual reasoning, working memory (Nascimento et al., 2016, Rahman et al., 2016, Wasserman et al., 2011, Wasserman et al., 2016), as well as behavior problems (Bouchard et al., 2007, Khan et al., 2011, Rahman et al., 2016). Although these studies vary greatly in terms of levels of exposure, they support the hypothesis that Mn exposure might adversely affect the developing brain.

We previously reported that elevated water Mn concentration (MnW) was associated with lower IQ in a group of school-age children aged 6–13 years (Bouchard et al., 2011). In this study, children in the highest quintile of Mn concentration had IQ scores 6 points lower than those in the lowest quintile. The association between MnW and IQ was stronger for girls than for boys. Hair Mn concentrations were also associated with lower IQ scores. Importantly, these results were observed at levels of exposure currently considered low and safe since and only 3% of participants had drinking water exceeding the World Health Organization guideline of 400 μg Mn/L (World Health Organization, 2004) (before this guideline it was discontinued altogether in 2011; World Health Organization, 2011).

The present study follows up the above cohort, and was conducted approximately four years after the initial study, depending on participants. The first objective was to re-assess the relation between water Mn concentration and cognition in this cohort around adolescence. The second objective was to monitor changes in Mn concentration in participants’ drinking water and to investigate how it might relate to change in IQ scores.

Section snippets

Study design and recruitment

Participants of the baseline epidemiological study in southern Quebec (Canada) carried out by Bouchard et al. in 2007–2009 were contacted for the present follow-up study, conducted in 2012–2013. Details on selection and recruitment of the baseline study participants are reported elsewhere (Bouchard et al., 2011). Of the initial 380 participants (mean age, 9.3 years; standard deviation [SD], 1.8), 287 children (mean age, 13.7 years; SD, 1.8) participated in the follow-up study. Mean time elapse

Descriptive statistics

Participants' characteristics and Mn levels in water and hair, as well as TAWMn are shown in Table 1. Seventy-eight percent of mothers had at least some college education, 64% had family income above $50,000, and 99% of children were white. More details on the characteristics of the initial cohort are available in Bouchard et al. (2011).

At follow-up examination, tap water Mn ranged from 0.2 to 961 μg/L (arithmetic mean, 57.6; geometric mean [GM], 14.5). Forty percent of children were exposed to

Discussion

The results from this follow-up study suggest that Mn concentration in drinking water is negatively associated with IQ during childhood, and that this negative association remains present at adolescence among girls. Higher water Mn concentration was rather associated with higher IQ in boys at the follow-up examination. Similar results were observed for MnH levels, i.e., lower Performance IQ scores in girls and opposite findings in boys, although associations were not significant. It is

Conclusion

Exposure to Mn from drinking water was associated with lower IQ in girls, whereas it was rather associated with higher IQ in boys. This adds to the mounting number of studies reporting sex-related differences in Mn toxicity. Also, for participants whose water Mn increased at follow-up, IQ scores decreased significantly compared with scores at baseline examination. Further studies are needed to better understand underlying mechanisms for sex differences in Mn neurotoxicity.

Competing financial interests’ declaration

We have no financial interests to declare.

Acknowledgments

We wish to acknowledge participants and families of participants who gave their time and help us carry out the study. We would like to thank Marie-Eve Brodeur for recruiting participants; her experience with this cohort was of great help. We are grateful for the SickKids Foundation for funding this study (grant #NI12-065). The Canadian Institutes of Health Research (CIHR) funded the original epidemiological study (NRF-82899).

References (37)

  • H.A. Roels et al.

    Manganese exposure and cognitive deficits: a growing concern for manganese neurotoxicity

    Neurotoxicology

    (2012)
  • R. Torres-Agustín et al.

    Effect of environmental manganese exposure on verbal learning and memory in mexican children

    Environ. Res.

    (2013)
  • G.A. Wasserman et al.

    Arsenic and manganese exposure and children's intellectual function

    Neurotoxicology

    (2011)
  • R.O. Wright et al.

    Neuropsychological correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site

    Neurotoxicology

    (2006)
  • M.F. Bouchard et al.

    Hair manganese and hyperactive behaviors: pilot study of school-age children exposed through tap water

    Environ. Health Perspect.

    (2007)
  • M.F. Bouchard et al.

    Intellectual impairment in school-age children exposed to manganese from drinking water

    Environ. Health Perspect.

    (2011)
  • P. Chen et al.

    Genetic factors and manganese-induced neurotoxicity

    Front. Genet.

    (2014)
  • A.W. Dobson et al.

    Manganese neurotoxicity

    Ann. N. Y. Acad. Sci.

    (2004)
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