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Grossklaus, R.; Liesenkötter, K.; Doubek, K.; Völzke, H.; Gaertner, R. Iodine Deficiency Affecting Fetal Brain Development. Encyclopedia. Available online: https://encyclopedia.pub/entry/47661 (accessed on 03 July 2024).
Grossklaus R, Liesenkötter K, Doubek K, Völzke H, Gaertner R. Iodine Deficiency Affecting Fetal Brain Development. Encyclopedia. Available at: https://encyclopedia.pub/entry/47661. Accessed July 03, 2024.
Grossklaus, Rolf, Klaus-Peter Liesenkötter, Klaus Doubek, Henry Völzke, Roland Gaertner. "Iodine Deficiency Affecting Fetal Brain Development" Encyclopedia, https://encyclopedia.pub/entry/47661 (accessed July 03, 2024).
Grossklaus, R., Liesenkötter, K., Doubek, K., Völzke, H., & Gaertner, R. (2023, August 04). Iodine Deficiency Affecting Fetal Brain Development. In Encyclopedia. https://encyclopedia.pub/entry/47661
Grossklaus, Rolf, et al. "Iodine Deficiency Affecting Fetal Brain Development." Encyclopedia. Web. 04 August, 2023.
Iodine Deficiency Affecting Fetal Brain Development
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This entry is adapted from the peer-reviewed paper 10.3390/nu15102249

An asymptomatic mild to moderate iodine deficiency and/or isolated maternal hypothyroxinemia might affect the development of the embryonal/fetal brain. There is sufficient evidence underlining the importance of an adequate iodine supply for all women of childbearing age in order to prevent negative mental and social consequences for their children. An additional threat to the thyroid hormone system is the ubiquitous exposure to endocrine disrupters, which might exacerbate the effects of iodine deficiency in pregnant women on the neurocognitive development of their offspring. 

iodine deficiency pregnancy hypothyroxinemia neurocognitive development

1. Introduction

Thyroid hormones are particularly important for normal embryonal/fetal and early postnatal neurocognitive development. Depending on the severity, duration and timing of iodine deficiency in certain life stages, iodine deficiency disorders (IDDs) may be associated with physical, neurological and intellectual deficits in humans. Severe iodine deficiency during pregnancy can lead to a number of adverse effects on maternal and child health, including goiter, hypothyroidism, stillbirth, increased neonatal mortality, neurological damage, and mental impairment [1]. In addition, global exposure to endocrine-disrupting chemicals (EDC) is increasing [2][3][4]. Exposure to these chemicals in the presence of inadequate iodine supply might be additionally harmful to the embryonal/fetal and neonatal brain development, growth, differentiation, as well as metabolic processes in adulthood [5][6][7][8][9][10][11][12].
Both iodine deficiency and exposure to EDCs have a negative impact on general health and on socio-economic systems. Annual costs for seven categories of EDCs with the highest causality have been estimated to be at least €33.1 billion in Europe. The largest proportion of costs is related to the loss of IQ points and neurocognitive diseases [13][14][15][16][17]. In addition, there is growing evidence that exposure to EDCs, including air pollution, affects not only the development of brain function [10][18][19][20][21] but also the outcomes of pregnancy and childbirth [22][23][24][25][26].
The “endemic goiter” has long been a synonym for iodine deficiency, and the aim has always been to prevent the enlargement of the thyroid gland and overt thyroid dysfunction. Within the last decades, however, the consequences of mild to moderate iodine deficiency on the cognitive development of the embryo/fetus have also come into focus [27].
Epidemiological and experimental studies of mild to moderate iodine deficiency over the past two decades have shown that embryonal/fetal brain development can be impaired not only in hypothyroid mothers but also in hypothyroxinemic mothers in the early stages of pregnancy [28][29][30][31][32]. Subtle changes in fetal brain development were observed even with maternal thyroid hormone levels within the lower reference range, although the results are not homogeneous, and, therefore, isolated maternal hypothyroxinemia (IMH) is not yet generally accepted as an independent thyroid disease. Instead, it is assumed to be the result of iodine deficiency and/or EDC contamination or of other factors, as extensively summarized and discussed by others [6][33][34][35].

2. Influence of TDCs, Including Air Pollution on Embryonic/Fetal Neurodevelopment in Iodine-Deficient Areas

So far, studies investigating maternal hypothyroxinemia due to mild to moderate iodine deficiency have not considered additional prenatal exposure to TDCs. However, retrospective case-control and cohort and population studies linking TDC exposure with epidemiological data on thyroid hormone-related (dys-)functions provide clear evidence that the development of the embryonal/fetal and neonatal brain as well as growth, differentiation and metabolic processes are at risk of suffering adverse TDCs effects [6][36]. In recent years, there has been a significant increase in neurodevelopmental disorders, including autism and ADHD [2][12][37][38][39][40].
Public health concern exists for mildly iodide-deficient pregnant women who are exposed to perchlorate, thiocyanate, nitrate or other environmental antithyroid agents [4][8][11][16][41][42][43][44][45][46][47]. In a dose-response model between iodide and perchlorate exposure in food, it was shown that a low iodide intake of 75 μg/day and a perchlorate daily dose of 4.2 μg/kg are sufficient to induce hypothyroxinemia, while an adequate iodine intake of 250 μg/day a higher perchlorate daily dose of around 34 μg/kg is required [48]. Iodine supplementation would be sufficient to prevent the goitrogenic effects of perchlorate exposure at current regulatory limits among at-risk individuals [43]. Iodine deficiency could therefore deteriorate the effects of TDCs exposure, especially during pregnancy [4][8][11][16][49][50].
Certain phthalates, including di-(2-ethylhexyl) phthalate (DEHP) and di-n-butylphthalate (DnBP), have antithyroid activity occurring through several possible mechanisms, such as down-regulation of NIS and interacting with hormone synthesis-related proteins, deiodinases, TTR, receptors, and hepatic enzymes [6][9][51][52]. Because phthalates may have multiple and possibly overlapping targets in the HPT axis, sometimes acting as an agonist or antagonist, the outcome from a given phthalate blend may not be predictable. For example, it had been shown in the Norwegian mother, child and father cohort study (MoBa) that exposure to certain phthalates in pregnant women increased TT3 and FT3, but only when iodine intake was low (<150 µg/d), whereas in those women with high iodine intake (>150 µg/d), TSH increased, and TT4 and FT4 decreased [53].
Furthermore, epidemiologic evidence suggests that prenatal exposure to phthalates is associated with emotional and behavioral difficulties in children [9][54][55][56][57][58][59][60]. However, a recent literature review including 17 epidemiological studies reveals no clear pattern of association between maternal exposures to phthalates during pregnancy and offspring neurodevelopment. This, again, might be caused by inconsistent study protocols, test systems and confounders [61][62].
A prospective pregnancy and birth cohort study examined BPA interaction with thyroid hormones in pregnant women and newborns. Higher BPA exposure is associated with decreased TSH in umbilical cord serum in girls. BPAs have the greatest negative effects on girls born to mothers with iodine deficiency [63]. A birth cohort study in China showed that the concentration of BPA in urine in the prenatal period was associated with low TSH in overweight mothers, but there was no association with fT4, fT3 and TSH in umbilical cord serum [64]. The disturbance of thyroid hormone (TH) levels as a result of prenatal exposure to BPA may be associated with long-term neurobehavioral changes at a later age [65][66][67]. It should be noted that there are various kinds of test batteries for child neurodevelopmental assessment at different ages whose findings have been inconsistent among studies. In addition, the timing and number of exposure assessments have varied. However, ADHD symptoms, especially among boys, constantly suggested an association with both prenatal and concurrent exposure to BPA [68]. Although there is limited evidence on the adverse effects of prenatal and postnatal BPA exposures, pregnant women and young children should be protected from exposure based on a precautionary approach [69][70].
Furthermore, a pilot study suggests that 2,3′,4,4′,5-pentachlorobiphenyl (PCB 118) has a negative impact on neurocognitive development and probably reduces the benefits of iodine supplementation in areas with borderline iodine deficiency. Therefore, TDC exposure should be considered when designing studies on the benefits of iodine supplementation during pregnancy [71].
Air pollution is a leading risk factor for the global disease burden, but the negative effects of exposure to particulate matter <2.5 μm (PM2.5) during pregnancy have not been considered in the past [72][73][74]. However, there is growing evidence of the negative effects of exposure to burn-related air pollution on the neurological development of fetuses and childhood behavior [20][75][76][77]. Air pollution may interfere with maternal thyroid function during early pregnancy, as shown in cohort studies from four European cohorts [10] and in Shanghai [78]. A 10 mcg/m3 increase in PM2.5 exposure in both the first and second trimester was associated with 28% (OR = 1.28, 95% CI, 1.05–1.57) and 23% (OR = 1.23, 95% CI, 1.00–1.51) increases in the odds of maternal hypothyroxinemia, respectively [78]. However, both studies have some limitations. Neither the iodine concentration in the urine of the pregnant women [79] nor the exposure to other environmental chemicals was considered [80].
The available evidence suggests that intrauterine PM2.5 exposure can alter prenatal brain development through oxidative stress and systemic inflammation, leading to chronic neuroinflammation, microglial activation, and neuronal micturition disorder [18][81][82]. It has been shown that particulate matter exposure during fetal lifetime was associated with structural changes in the child’s cerebral cortex, as well as with impairment of essential executive functions, such as inhibitory control [83][84].
Studies that focused on exposures to air pollution, especially PM and NO2, during the prenatal period and the first years of life found associations with reduced psychomotor development [85][86] and impairment in cognitive development [19][87][88], as well as with autism-spectrum disorders [39][89][90][91]. However, these results could not be confirmed by others [20][21][92][93][94].

3. Prevention and Treatment of IMH

Since studies on the effects of IMH on cognitive and motor development, as well as on the risk of neuropsychiatric diseases in children, show a clear connection to early pregnancy; the central clinical question remains whether these complications can be prevented by early iodine supplementation or L-Thyroxine substitution [29][33].
Treatment of IMH or subclinical hypothyroidism with L-Thyroxine during early pregnancy revealed no benefit concerning the neurodevelopment of the children at the age of 6 and 9 years. However, L-Thyroxine supplementation started at the mean of the 12th week of pregnancy, which is too late [95][96]. This is why the ATA guidelines do not recommend L-Thyroxine supplementation [97]. However, based on new epidemiological data, ETA guidelines are considering L-Thyroxine supplementation during the first trimester rather than later [98]. The results of a recent study showed that early L-Thyroxine supplementation in women with TSH levels of >2.5 mU/L and fT4 < 7.5 pg/mL at or before the ninth gestational week (GW9) is safe and improves the progress of gestation. Whether the neurodevelopment of these offspring also improved, however, has not been studied so far. These data support the recommendation to adopt these cut-off levels for L-Thyroxine supplementation, which should be started as early as possible, ideally before the end of the first trimester of gestation, and TSH suppression should be avoided [99].
In regions with mild to moderate iodine deficiency, iodized salt intake, regularly used at least 24 months before pregnancy, can significantly improve maternal thyroid economy and reduce the risk of maternal thyroid insufficiency during pregnancy. This is probably due to a restoration of intrathyroidal iodine stores [100][101][102][103][104][105][106]. The importance of this finding is supported by the results of a large prospective cohort, including mothers and offspring. A positive association between preconception maternal iodine status and the cognitive function of the offspring at the age of 6–7 years could be demonstrated [103]. In contrast, meta-analyses of iodine supplementation starting during pregnancy found no effect on child neurodevelopment [102][107][108][109][110][111]. The lack of beneficial effects of iodine supplementation, typically after the first trimester, bypasses the critical period of development early in gestation.
There is some concern that over-the-counter iodine-containing supplements might contain high doses that temporarily disturb thyroid hormone production and/or release. Therefore, moderate iodine deficiency should be prevented already before conception [112][113]. Well-designed randomized controlled trials investigating a daily supplementation with 150–200 µg iodine in preconception, pregnancy, and lactation are underway to investigate children’s neuropsychological development [114][115][116][117]. Also, more data are needed to determine optimal and safe upper limits of iodine supplementation in pregnant women and assess the potential risks of chronic high iodine intake during pregnancy [109][118].
The Krakow Declaration of Iodine, published by the EU thyroid consortium and other organizations, raised major points about how iodine deficiency can be efficiently eradicated in Europe. It was demanded that (1) universal salt iodization should be harmonized across European countries, (2) regular monitoring and evaluation studies have to be established to continuously measure the benefits and potential harms of iodine fortification programs and (3) societal engagement is needed to warrant sustainability of IDD prevention programs [119].

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