Prenatal fluoride exposure, offspring visual acuity and autonomic nervous system function in 6-month-old infants

Abstract

Background

Prenatal fluoride exposure can have adverse effects on children’s development; however, associations with visual and cardiac autonomic nervous system functioning are unknown. We examined associations between prenatal fluoride exposure and visual acuity and heart rate variability (HRV) in 6-month-old infants.

Methods

We used data from Canadian mother-infant pairs participating in the Maternal-Infant Research on Environmental Chemicals (MIREC) cohort. We estimated prenatal fluoride exposure using: i) fluoride concentration in drinking water (mg/L), ii) maternal urinary fluoride adjusted for specific gravity (MUF_SG; mg/L) and averaged across pregnancy, and iii) maternal fluoride intake (µg/kg/day) from consumption of water, tea, and coffee, adjusted for maternal body weight (kg). We used multivariable linear regression to examine associations between each measure of fluoride exposure and Teller Acuity Card visual acuity scores (n=435) and assessed HRV (n=400) using two measures: root mean square of successive differences (RMSSD) and the standard deviation of N-N intervals (SDNN) measured at 6-months of age.

Results

Median (IQR) values for water fluoride, MUF_SG, and daily fluoride intake were 0.20 (IQR: 0.13-0.56) mg/L; 0.44 (0.28-0.70) mg/L and 4.82 (2.58-10.83) µg/kg/day, respectively. After adjustment for confounding variables, water fluoride concentration was associated with poorer infant visual acuity (B = –1.51; 95% CI: -2.14,-0.88) and HRV as indicated by lower RMSSD (B = -1.60; 95% CI: -2.74,-0.46) but not SDNN. Maternal fluoride intake was also associated with poorer visual acuity (B = -0.82; 95% CI: -1.35,-0.29) and lower RMSSD (B = -1.22; 95% CI: -2.15,-0.30). No significant associations were observed between MUF_SG and visual acuity or HRV.

Conclusion

Fluoride in drinking water was associated with reduced visual acuity and alterations in cardiac autonomic function in infancy, adding to the growing body of evidence suggesting fluoride’s developmental neurotoxicity.

Graphical Abstract

EXCERPTS:1. Introduction

Approximately 73 % of Americans and 39 % of Canadians have fluoride added to municipal drinking water supplies at a concentration of 0.7 mg/L to prevent tooth decay (The State of Community Water Fluoridation across Canada. 2022 Report, (2022), Water fluoridation Data & Statistics, 2023). While the benefits of water fluoridation are cited widely, a growing body of evidence has linked early-life exposure to fluoride with adverse neurodevelopmental outcomes, even at optimal exposure levels (i.e., 0.7 mg/L) (Dewey et al., 2023, Farmus et al., 2021, Grandjean, 2019, Grandjean et al., 2023, Green et al., 2019, National Toxicology Program, 2022). However, some of the findings are mixed (Do et al., 2023, Ibarluzea et al., 2022), possibly reflecting differences in sources, cofactors, doses, and timing of exposure.

The fetus is particularly vulnerable to neurotoxicants, which can cross the placenta and interfere with the developing nervous system (Lanphear, 2015). To date, five pregnancy cohort studies have examined the impact prenatal fluoride exposure on offspring neurodevelopmental outcomes in populations receiving optimally fluoridated water or salt (Bashash et al., 2017, Cantoral et al., 2021, Dewey et al., 2023, Green et al., 2019, Ibarluzea et al., 2022). One study conducted in Mexico, where salt is fluoridated, showed that higher dietary fluoride intake in pregnancy was associated with lower nonverbal abilities in offspring at 24-months of age, but only in boys (Cantoral et al., 2021). Among preschool-aged children, studies conducted in Mexico City (Bashash et al., 2017) and Canada (Green et al., 2019) found that children born to women with higher levels of urinary fluoride in pregnancy had lower intelligence quotient (IQ) scores; this association was only significant among boys in the Canadian study (Green et al., 2019). Another Canadian cohort study reported links between exposure to fluoridated drinking water and lower cognitive flexibility at 3–5 years of age, particularly in girls (Dewey et al., 2023). In contrast, a study conducted in Spain found that higher urinary fluoride levels in pregnancy were positively associated with IQ in boys at age 4; however, this association was driven by those living in non-fluoridated communities and was attenuated when adjusting for other neurotoxicants (Ibarluzea et al., 2022).

Use of multimethod approaches to assess the developing nervous system may provide the sensitivity needed to detect subtle yet important effects of prenatal fluoride exposure on the developing infant brain. Past fluoride studies conducted in human infants assessed cognitive and motor skills using the Bayley Scales of Infant Development (Cantoral et al., 2021; Valdez-Jimenz et al., 2017; Ibarluzea et al., 2022). Examining markers of both central and peripheral nervous system development, such as visual acuity and cardiac autonomic nervous system (ANS) function, could expand our understanding of the impact of prenatal fluoride exposure on offspring neurodevelopment beyond cognitive and behavioural outcomes. Indeed, markers of sensory system development and ANS function have been used to index aspects of infant neurodevelopment following exposure to prenatal adversity (Gilman et al., 2017). Additionally, assessing infants in the first 6-months of life is advantageous given that postnatal exposure to fluoride sources is limited, especially among breastfed infants. Breastmilk contains extremely low concentrations of fluoride (<0.02 µg/L) due to the limited transfer of plasma fluoride into breastmilk (Dabeka et al., 1986, Ekstrand et al., 1981, Ekstrand et al., 1984, Zohoori et al., 2019). Exposure to fluoride in the first 6-months of life is mainly limited to intake from infant formula, especially if fluoridated water is used to reconstitute formula (Zohoori et al., 2014). Exposure from other sources, such as fluoridated toothpaste and fluoride-containing foods, does not typically occur until after 6-months of age.

Visual acuity, which refers to the ability to detect small visual details with precision (Teller et al., 1986), can be reliably assessed within the first postnatal year and can be used to detect toxicity to the developing central nervous system (Brémond-Gignac et al., 2011). Indeed, prenatal exposure to various toxic chemicals, such as methylmercury (Murata et al., 2006, Yorifuji et al., 2013), chlorpyrifos (Silver et al., 2018), lead (Silver et al., 2016), molybdenum (Wang et al., 2023) and organic solvents (Till et al., 2005, Till et al., 2001) during gestation have been linked to poorer offspring visual acuity. Poorer visual acuity early in life has been associated with cognitive dysfunction and may be linked to further visual problems over the lifespan (Brémond-Gignac et al., 2011). To our knowledge, no studies have examined links between prenatal fluoride exposure and visual acuity in infancy.

The ANS, which plays a critical role in maintaining homeostasis across organ systems (Thayer & Sternberg, 2006), can be reliably assessed during the first postnatal year using measures of heart rate variability (HRV) (Laborde et al., 2017). Lower HRV is thought to reflect poorer ANS capacity to coordinate adaptive responses to situational demands/environmental challenges. Exposure to environmental toxins, including Bisphenol A (Bae et al., 2012) and particulate matter (Gold et al., 2000, Saenen et al., 2019) are inversely associated with HRV in adults and children. Prenatal environmental toxicant exposures may also adversely impact offspring HRV. For instance, some studies have reported lower HRV in offspring prenatally exposed to methylmercury (Chan et al., 2021, Grandjean et al., 2004, Murata et al., 2006, Sørensen et al., 1999), however, two other studies did not report links (Periard et al., 2015, Zareba et al., 2019). Prenatal exposure to nicotine, opioids, cocaine, and alcohol have also been linked to adverse ANS function in offspring (Fifer et al., 2009, Nordenstam et al., 2017, Sania et al., 2023, Schlatterer and du Plessis, 2021, Schuetze et al., 2007). Despite links to neurotoxicants and substances, as well as evidence suggesting that infant ANS function is sensitive to exposure to prenatal adversity (Chiera et al., 2020, Schlatterer and du Plessis, 2021, Van den Bergh et al., 2020), no studies have investigated associations between prenatal fluoride exposure and offspring HRV. Investigating these links is critical given that adverse ANS development is associated with poorer socioemotional functioning (Porges & Furman, 2011), psychiatric risk (Beauchaine & Thayer, 2015) and risk for adverse cardiometabolic outcomes (Thayer et al., 2010) across the lifespan.

Using data from the Maternal-Infant Research on Environmental Chemicals (MIREC) cohort, we examined associations between prenatal fluoride exposure and infant visual acuity and ANS function measured in 6-month-old infants. Considering findings from previous studies showing sex-specific associations related to prenatal fluoride exposure (Dewey et al., 2023, Green et al., 2019, Malin and Till, 2015), and the importance of examining sex-specific effects at different developmental stages (Bellinger et al., 2016, Gade et al., 2021, Goodman, (In Press)), we also explored the potential for sex-specific associations in this study…

3. Results

Table 1 shows the demographic characteristics of participants with fluoride exposure and complete covariate data who were included in adjusted models for mother-infant pairs with visual acuity and HRV data. Women were, on average, 31.6 (SD = 4.81) years at enrollment; the majority were married (94.6 %), had a bachelor’s degree or higher (66.1 %), and reported being White (91.3 %). At the time of testing, infants were, on average, 6.81 months of age (SD = 0.89; range: 4.93 to 10.09), and 48 % were female; 22 of 424 (5.2 %) infants were born moderately-to-late preterm (i.e., <37 weeks of gestation), and 26 (6.1 %) had a low birth weight (<2500 g)…

4. Discussion

In this Canadian prospective birth cohort study, we examined whether prenatal fluoride exposure was associated with grating visual acuity and cardiac autonomic function in infants using two time domain measures of heart rate variability, RMSSD and SDNN. We found that higher levels of fluoride in drinking water during pregnancy were associated with lower infant visual acuity and risk for ANS problems indexed by lower RMSSD. Relative to the findings with water fluoride concentration, similar, but weaker associations were observed with maternal fluoride intake (which accounts for exposure from water and additional dietary sources of fluoride, such as black tea) and offspring visual acuity and RMSSD. Taken together, these results suggest that water fluoride levels and maternal fluoride intake may be associated with poorer central (visual acuity) and peripheral (cardiac ANS) markers of nervous system functioning in infant offspring. These results are novel given that prior human studies examining prenatal exposure to fluoride have only assessed offspring outcomes using measures of cognitive and behavioral development.

In contrast, maternal urinary fluoride levels were not associated with any of our infant outcomes, consistent with past studies conducted in this cohort (Hall et al., 2023) as well as other samples (Malin et al., 2018, Riddell et al., 2019) showing stronger exposure-outcome associations with water fluoride compared with urinary fluoride levels. The moderate correlation between our fluoride exposure measures suggests that these metrics are capturing different aspects of fluoride exposure and are therefore considered complementary to each other. We consider water fluoride concentration to be a more representative measure of long-term exposure to fluoride, given that levels are relatively stable over months (Castiblanco-Rubio et al., 2022, Till et al., 2018). However, we acknowledge that this exposure metric is also prone to measurement error since a concentration of fluoride in drinking water does not reflect consumption habits, particularly amount of water consumed. We attempted to address an individual’s consumption habits by estimating maternal fluoride intake using questionnaire data reported by women at two time-points during pregnancy. Maternal fluoride intake is therefore thought to reflect a more individualized metric of exposure relative to water fluoride level because it takes into consideration overall volume of water, tea, and coffee consumed as well as additional exposure to fluoride from black tea consumption.

In contrast to our estimated fluoride exposure measures (i.e., water fluoride and fluoride intake), MUF_SG measured from urine spot samples captures recent systemic fluoride exposure from all sources and is more likely to exhibit variability over time. Our past work comparing MUF_SG levels across each trimester found an intraclass correlation coefficient of 0.37 (Till et al., 2018). This moderate consistency across trimesters in the MIREC cohort is likely due to the short (?6 hr) half-life of fluoride in the body (Whitford, 1994) and differences in amount of fluoride that is absorbed and released from long-term accumulation in bones due to continuous bone remodeling (Villa et al., 2010). While we attempted to minimize variability in urinary fluoride by averaging MUF_SG across three trimesters, the measure remains impacted by variability in day-to-day fluoride exposures (Castiblanco-Rubio et al., 2022), which may have contributed to null associations.

Another explanation for why we observed associations with our water-based measures, but not with urinary fluoride, may be due to unmeasured confounding. It is possible that differences in water fluoride levels and intake levels (which differ by city) could serve as a proxy for other relevant characteristics that may differ between people living in fluoridated versus non-fluoridated communities. However, comparison of mother–child dyads by CWF status did not reveal any differences that could explain the observed associations over and above the covariates that were used in our models (Table S3). Finally, we note that we do not control for “city” in the models that used water-based fluoride measures due to collinearity between city and water fluoride concentration. To check whether controlling for “city” controls for community characteristics that are associated with the decision to fluoridate water supplies, we removed ‘city’ from the MUF_SG model. Results remained non-significant, meaning that the difference in the association between the urine biomarker versus our other fluoride measures are not due to differences in covariate adjustment.

Previous studies have reported poorer visual acuity following prenatal exposure to a variety of neurotoxicants, including methylmercury, lead, chlorpyrifos, and organic solvents (Silver et al., 2018, Till et al., 2005, Till et al., 2001, Yorifuji et al., 2013), reflecting the exquisite sensitivity of the developing visual system to early-life exposure to neurotoxicants (Grandjean and Landrigan, 2014, Lanphear, 2015). Furthermore, poorer visual acuity in infancy is an important outcome because it may have prognostic value for potential adverse outcomes later in life, including lower IQ and poorer reading comprehension (Brémond-Gignac et al., 2011).

Studies have also shown that toxins can impact heart rate variability in exposed adults and children (Bae et al., 2012, Gold et al., 2000, Halabicky et al., 2022, Saenen et al., 2019). Prenatal exposures, including methylmercury, nicotine, and alcohol, may also adversely affect offspring ANS development (Chan et al., 2021, Grandjean et al., 2004, Murata et al., 2006, Sørensen et al., 1999). We extend this evidence to prenatal fluoride exposure, albeit only with RMSSD, perhaps suggesting that prenatal fluoride exposure may disrupt the development of HRV mediated by the parasympathetic branch of the ANS, thereby indicating risk for adverse ANS function (Laborde et al., 2017, Shaffer and Ginsberg, 2017). Indeed, the ANS consists of two major branches, the parasympathetic (PSNS) and sympathetic (SNS) branch which work in concert to balance energy mobilization (SNS), and relaxed, restorative functions (PSNS) (Thayer & Sternberg, 2006). Therefore, adverse PSNS development can lead to ANS dysfunction, thereby increasing disease risk across multiple organ systems (Quigley and Moore, 2018, Thayer and Sternberg, 2006, Thayer et al., 2010). Other studies have also found that early adversity, including exposure to neurotoxicants, can negatively impact the PSNS branch of the ANS (Schlatterer & du Plessis, 2021). For instance, lead and methylmercury exposure have been linked to greater sympathetic dominance (i.e., poorer PSNS influence on the heart) (Halabicky et al., 2022) and lower PSNS activity (Gribble et al., 2015). Furthermore, prenatal methylmercury exposure was linked to lower PSNS activity and greater SNS dominance (Chan et al., 2021, Murata et al., 2006). Disruptions in parasympathetic function can impact development of socioemotional functioning (Porges & Furman, 2011), including self-regulation (Holzman & Bridgett, 2017), and increase risk for psychopathology (Beauchaine & Thayer, 2015).

While the mechanisms underlying the current findings are unclear, observing effects across both central (i.e., visual system development) and peripheral (i.e., ANS function) nervous system levels suggest that prenatal fluoride exposure may be associated with more diffuse, rather than focal effects on the developing nervous system. Fluoride readily crosses the blood–brain barrier and can accumulate in multiple brain areas, resulting in damage to myelin and neurons as well as decreases in dendritic arborization (Wang et al., 2018, Whitford et al., 2009). Furthermore, its effects on myelin could adversely impact third trimester myelination of the vague nerve, which is particularly important for parasympathetic influence on the heart (Cerritelli et al., 2021, Porges and Furman, 2011). This may also impact emerging connectivity pathways within the visual system that begin development prenatally and continue into childhood (Dayan et al., 2015).

Although we found no statistically significant evidence of effect modification by sex in the association between fluoride exposure and infant visual acuity and ANS functioning, effects were generally stronger among male infants, especially for RMSSD, which is consistent with some previous studies showing stronger effects of prenatal fluoride exposure on males (Cantoral et al., 2021, Farmus et al., 2021, Green et al., 2019). However, a recent study reported adverse cognitive development in females whose mothers were exposed to optimally fluoridated water in pregnancy (Dewey et al., 2023). Sex specific effects are complex and depend on multiple factors including the functional outcome assessed and developmental stage that offspring are assessed (Joel & McCarthy, 2017). Indeed, male and female fetuses use different strategies to respond to placental perturbations, with the male placenta investing more resources in growth relative to females (Sandman et al., 2013). This emphasis on growth is thought to reduce the male fetus’s ability to respond flexibly to prenatal adversities (Sandman et al., 2013), which could explain why males may be at greater risk for poorer PSNS development, a system which mediates adaptation and flexibility in response to internal/external demands (Thayer & Sternberg, 2006). Research also suggests that there is an interaction between sex and thyroid hormones and that certain neurotoxicants, including fluoride, may change thyroid physiology in a sex-specific manner ?(Batista & Hensch, 2019; Hall et al., 2023)?, which in turn may disrupt ANS functioning (Brusseau et al., 2022). However, while important to acknowledge mechanisms underlying sex differences following fetal exposure to neurotoxicants, further research is needed to elucidate the role of offspring sex in these links.

Our study must be examined in the context of the following limitations. First, we were unable to assess the magnitude of fluoride that reaches the fetal brain. While fluoride is commonly measured in spot urine or water samples, these exposure metrics do not account for variability in placental transport and metabolism and thus may not accurately reflect fetal exposure. Moreover, our archived data did not have information about day-to-day behaviors that may have occurred, such as morning fasting or use of fluoridated dental products or consumption of distilled bottled water prior to urine sampling. These behaviors would influence urine-fluoride levels given the short half-life of fluoride (?6 h) and contribute measurement error, which would be more likely to negatively bias our effect estimates towards the null. However, we attempted to mitigate the potential for exposure misclassification by taking the average urinary fluoride concentration across all three trimesters. Future studies should consider alternate biomarkers that can capture chronic fluoride exposure, such as tooth dentin and toenails (Nayak et al., 2021, Vidyadharan et al., 2020)). Tooth dentin can measure serial and cumulative prenatal and postnatal systemic exposure to fluoride (Yu et al., 2021). It is an optimal biomarker because the week-by-week history of fluoride exposure beginning at approximately 14 weeks gestation and continuing through the first 2 to 3 years of life can be reconstructed to test for critical windows of exposure (Davis et al., 2020). This type of biomarker would have the advantage of assessing fluoride exposures occurring in early infancy through formula-feeding and introduction of solid foods, which we were unable to do in the current study. To focus our analysis on fetal fluoride exposure, we conducted a sensitivity analysis controlling for exclusive breastfeeding. Results remained consistent, suggesting that the fetal period may be a critical exposure window, though this analysis was limited because we were missing infant feeding information at 6-months of age for almost 25 % of the sample. Third, while the TAC is considered a reliable measure of grating acuity, it is a behavioral assessment that is based on preferential looking and may not generalize to other aspects of vision. Finally, future studies could also aim to examine other measures of ANS activity using additional HRV measures, including frequency domain and non-linear assessments.

5. Conclusions

This study is the first to report associations between prenatal fluoride exposure and offspring visual acuity and HRV as assessed by RMSSD in 6-month-old infants. Our findings that prenatal fluoride exposure may adversely affect visual acuity and ANS functioning in infants highlights the gestational period as a critical period of susceptibility to fluoride. This work contributes to the growing body of evidence on the potential toxicity of fluoride to the developing brain.

Funding Source

This research was funded by the National Institute of Environmental Health Science, grant number R01ES030365, 2020–2025. The Maternal-Infant Research on Environmental Chemicals Study was funded by the Chemicals Management Plan at Health Canada, the Ontario Ministry of the Environment, and the Canadian Institutes for Health Research (grant MOP-81285). The funding source had no involvement in any aspect of the study.

Appendix A. Supplementary material

The following are the Supplementary data to this article:

Download: Download Word document (49KB)Supplementary data 1.

Data availability

Data will be made available on request.

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Prenatal fluoride exposure, offspring visual acuity and autonomic nervous system function in 6-month-old infants

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