Elsevier

NeuroToxicology

Volume 82, January 2021, Pages 177-185
NeuroToxicology

Impact of Lead Exposure on Thyroid Status and IQ Performance among School-age Children Living Nearby a Lead-Zinc Mine in China

https://doi.org/10.1016/j.neuro.2020.10.010Get rights and content

Highlights

  • Lead intoxication decreased serum TSH level in school- age children.

  • Lead intoxication increased serum GABA level in school- age girls.

  • BLL and serum Glu level were negatively correlated with school- aged children's IQ.

  • The frequency of mother smoking and drinking un-boiled stagnant tap water were risk factors of lead intoxication.

  • Eating fresh fruits, vegetables and soy products regularly may protect against lead intoxication.

Abstract

Background

Lead exposure is one of the most concerning public health problems worldwide, particularly among children. Yet the impact of chronic lead exposure on the thyroid status and related intelligence quotient performance among school-age children remained elusive.

Objective

The aim of this study was to evaluate the influence of lead exposure on the thyroid hormones, amino acid neurotransmitters balances, and intelligence quotient (IQ) among school-age children living nearby a lead-zinc mining site. Other factors such as rice lead levels, mothers’ smoking behavior, and diet intake were also investigated.

Methods

A total of 255 children aged 7-12 years old were recruited in this study. Blood lead level (BLL), thyroid hormones including free triiodothyronine (FT3), free thyroxine (FT4) and thyroid stimulating hormone (TSH), and amino acid neurotransmitters such as glutamate (Glu), glutamine (Gln), and γ-aminobutyric acid (GABA) were measured using graphite furnace atomic absorption spectroscopy (GFAAS), chemiluminescence immunoassay, high performance liquid chromatography (HPLC). Raven's standard progressive matrices (SPM) and the questionnaire were used to determine IQ and collect related influence factors.

Results

The average BLL of children was 84.8 μg/L. The occurrence of lead intoxication (defined as the BLL ≥ 100 μg/L) was 31.8%. Serum TSH levels and IQ of lead-intoxicated children were significantly lower than those without lead toxicity. The GABA level of girls with the lead intoxication was higher than those with no lead-exposed group. Correlation analyses revealed that BLL were inversely associated with the serum TSH levels (R= -0.186, p < 0.05), but positively related with IQ grades (R = 0.147, p < 0.05). Moreover, BLL and Glu were inversely correlated with IQ. In addition, this study revealed four factors that may contribute to the incidence of lead intoxication among children, including the frequency of mother smoking (OR = 3.587, p < 0.05) and drinking un-boiled stagnant tap water (OR = 3.716, p < 0.05); eating fresh fruits and vegetables (OR = 0.323, p < 0.05) and soy products regularly (OR = 0.181, p < 0.05) may protect against lead intoxication.

Conclusion

Lead exposure affects the serum TSH, GABA levels and IQ of school-aged children. Developing good living habits, improving environment, increasing the intake of high-quality protein and fresh vegetable and fruit may improve the condition of lead intoxication.

Introduction

In developing countries, lead pollution is one of the most concerned public health problems(Li et al., 2015; Olympio et al., 2018; Shen et al., 2018; Yabe et al., 2018). Fast development of the manufacturing industry that utilizes lead has rendered the metal to be widely emitting into the sounding environment (da Rocha Silva et al., 2018; Han et al., 2018; Qu et al., 2018; Shen et al., 2018; Yabe et al., 2018; Ying et al., 2018). Lead-contained materials could enter the human body through the digestive, respiratory and dermal system, resulting in lead neurotoxicity (Bijoor et al., 2012; Warniment et al., 2010; Zhang et al., 2012) characterized by psychological and behavioral alterations, leading to impaired learning and memory function (Hornung et al., 2009; Hou et al., 2013; Warniment et al., 2010; Yang et al., 2018; Zhu et al., 2016) and other lead toxicities such as cardiovascular toxicity, reproductive toxicity and hepatorenal toxicity(Sachdeva et al., 2018). Children are particularly susceptible to lead toxicity, due to their unique growth and developmental stage when the absorption rate of lead in children is about four to five times higher than those in adults, while their rate of lead excretion is only about two-thirds of those in the adults (Advisory Committee on Childhood Lead Poisoning, 2000). In addition, the blood-brain barrier in children is more easily to be compromised by lead exposure (Shi and Zheng, 2007; Wang et al., 2012; Zheng et al., 2003a). Therefore, children are susceptible to lead (Advisory Committee on Childhood Lead Poisoning, 2000; Iriani et al., 2012; Mason et al., 2014; Wang et al., 2012).

Data in literature have suggested that cell apoptosis and oxidative stress in the central nervous system may contribute to the learning and memory dysfunction induced by lead (Khodamoradi et al., 2015). More recent studies have shown that lead exposure may disrupt the balance of neurotransmitters system (Lasley and Gilbert, 2002; Neal et al., 2010). The dyshomeostasis of glutamate (Glu), glutamine (Gln), and γ-aminobutyric acid (GABA) is known to affect the long-term potentiation (LTP) (Albrecht et al., 2010; Lasley and Gilbert, 2002); an impaired LTP can lead to the learning impairment (Hu et al., 2018; Katauskis et al., 2018). It is worth noting that the level of amino acid neurotransmitter Gln and GABA has been shown to be closely correlated with thyroid hormone levels including T3 and T4 in neurodegenerative diseases induced by exogenous chemicals including manganese (Manzano et al., 2007; Ou et al., 2019). It is well known that thyroid hormones levels are closely related with the intellectual development of children (Bassett and Williams, 2016; Konig and Moura Neto, 2002; Kopp, 2001; Moog et al., 2017). Animal studies have demonstrated that lead exposure decreases thyroid hormone T3 levels and promotes the feedback increase of TSH levels (Ge et al., 2012). Moreover, the epidemiologic study among lead-exposed workers has established that lead exposure adversely affects workers’ thyroid function (Dundar et al., 2006; Yilmaz et al., 2012). It is well known that thyroid hormones levels are closely related with the intellectual development of children (Bassett and Williams, 2016; Konig and Moura Neto, 2002; Kopp, 2001; Moog et al., 2017). Animal studies have demonstrated that lead exposure decreases thyroid hormone T3 levels and promotes the feedback increase of TSH levels (Ge et al., 2012). Moreover, the epidemiologic study among lead-exposed workers has established that lead exposure adversely affects workers’ thyroid function (Dundar et al., 2006; Yilmaz et al., 2012). In contrast, a study have shown that the blood lead level of workers occupationally exposed to lead, cadmium and arsenic does not affect the thyroid hormone concentration (Jurdziak et al., 2018).

While the existing evidence support a relationship between lead exposure and alterations in amino acid neurotransmitters and thyroid function (Barysheva, 2018; Lasley and Gilbert, 2002; Neal et al., 2010; Ou et al., 2019; Zheng et al., 2003b; Zheng et al., 2001), such a relationship has never been explored among school-age children living nearby lead mining sites. Lead-zinc mines produce a variety of heavy metal pollutants, typically including lead, cadmium and other non-metallic contaminants (Hesami et al., 2018; Luo et al., 2018; Yabe et al., 2018). The presence of high levels of toxic metals in air, soil, and water renders it much easier for children living nearby to be exposed to lead, resulting in lead-associated health problems. Additionally, toys, household painting, ceramic tiles, and folk medicines are also important sources of lead exposure for children (da Rocha Silva et al., 2018; Shen et al., 2018; Ying et al., 2018).

The current sectional study was conducted in a lead-zinc mine in the north region of Guangxi Province in China, among school children from Grade1 to Grade 6. In addition to determine the effect of lead exposure on thyroid hormones (FT3, FT4, and TSH) and amino acid neurotransmitters (Glu, Gln, GABA) among these school-age children, we also measured levels of lead in rice (a common food source there) in the local area in order to understand the relationship between environmental lead exposure and the changes in serum thyroid hormones and amino acid neurotransmitters, and ensuing IQ testing outcomes. Other interfering factors such as mother’s smoking and eating habit were also explored.

Section snippets

Study population

The research has been approved by Institutional Review Boards of Guangxi Medical University in Nanning, China. All of the voluntarily participated children and their guardians signed the informed consent prior to their participation in this study. After excluding students with severe organic diseases or psychiatric diseases including ADHD or mental retardation, age-inconsistent, or children of the right age but their parents who failed to sign the informed consent, a total of 255 children aged

Socio-demographic characteristics of research objects

The average age of children in several tests ranged from 9.2 to 9.5 years old. There were no significant differences in the composition of gender and age among students involved in different tests (p>0.05). Based on the results of questionnaire survey, 20.5% of children in this study lived in poverty, and 7.5% of the children were from the well-to-do families. About 80% of their parents graduated from lower than high school and work as miners or farmers. The proportion of miners in fathers and

Discussion

The results of present research showed that the school-age children who have been living nearby the lead mining area with environmental lead exposure had the high blood lead level, and some has shown the lead intoxication with BLL over 100 μg/L. Moreover, lead intoxication adversely affected levels of TSH and GABA in school-age children. BLL, Glu level were inversely correlated with children's IQ. In addition, the influence factors in lead intoxication cases, while relatively complex, included

Conclusions

Overall, the lead pollution condition nearby the lead-zinc mine area is serious, and the lead exposure has significantly affected the serum TSH, GABA levels and the IQ performance of school-aged children. The foodstuff of high quality protein and fresh vegetables and fruits may play an important role in preventing children from lead intoxication. Therefore, the results of the study call on the public to pay attention to school-age children's physical and intellectual development, and make great

CRediT authorship contribution statement

Qiu-ling Cai: Formal analysis, Investigation, Data curation, Writing - original draft, Writing - review & editing. Dong-jie Peng: Writing - original draft, Visualization, Writing - review & editing. Lin-Zhao: Writing - original draft, Visualization. Jing-wen Chen: Formal analysis, Investigation. Yong-Li: Formal analysis, Investigation. Hai-lan Luo: Investigation. Shi-yan Ou: Investigation. Ming-li Huang: Resources. Yue-ming Jiang: Conceptualization, Supervision, Project administration, Funding

Declaration of Competing Interest

None declared.

Acknowledgement

This study was supported by National key basic research development plan -973 plan (2012CB525001) and the National Natural Science Foundation of China (NSFC 81773476). We thank Dr. Sherleen Xue-Fu Adamson from the Procter and Gamble Company for her critical reading and revision of the manuscript before submission. Meanwhile, we thank all the participating subjects of school age children for completing a series of testing and investigation work and their parents (guardians).

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