Exposure to organochlorine pesticides and the risk of type 2 diabetes in the population of East China

https://doi.org/10.1016/j.ecoenv.2019.110125Get rights and content

Highlights

  • OCP exposure was positively associated with the prevalence of type 2 diabetes.

  • β-HCH and p,p’-DDE were associated with higher levels of FPG in nondiabetics.

  • OCP exposure can disrupt lipid metabolism among participants without diabetes.

Abstract

Organochlorine pesticides (OCPs) have been reported to be associated with an elevated risk of type 2 diabetes, although no study has focused on such associations in Chinese populations. In this case-control study, we aimed to explore the associations between OCPs and type 2 diabetes and their potential mechanisms in a population from East China. Participants diagnosed with type 2 diabetes and nondiabetic participants from Shandong Province, East China, were enrolled in this case-control study. Six OCPs (β-HCH, trans-chlordane, trans-nonachlor, p,p’-DDE, p,p’-DDT and mirex/kepone) were detected in more than 75% of serum samples. Logistic regression analysis and multiple linear regression analysis were used to assess the associations between OCP exposure and the outcomes. After adjusting for potential confounding factors such as age, sex and body mass index, all six OCPs showed positive associations with type 2 diabetes in a linear dose-response manner. Serum concentrations of β-HCH and p,p’-DDE were associated with higher levels of fasting plasma glucose in participants without diabetes, although no OCPs showed significant associations with hemoglobin A1c. In addition, certain OCPs showed significantly positive associations with triglycerides, total cholesterol, and low-density lipoprotein cholesterol and negative relationships with high-density lipoprotein cholesterol in nondiabetics, indicating that OCP exposure may disrupt lipid metabolism. Findings in the current study indicated that OCPs may be a diabetogenic factor in the population of this study. To our knowledge, this is the first study to investigate the associations between OCP exposure and type 2 diabetes in a Chinese population.

Introduction

Organochlorine pesticides (OCPs) are group of persistent organic pollutants (POPs) that have been widely used for pest control in agriculture and disease vector control. Since the 1970s, developed countries began to prohibit the use of OCPs for agricultural purposes due to their environmental persistence, ecotoxicity, and potential human health effects (Voldner and Li, 1995). Nine OCPs (aldrin, chlordane, dichlorodiphenyltrichloroethane [DDT], dieldrin, endrin, heptachlor, hexachlorobenzene [HCB], mirex and toxaphene) were among the “dirty dozen” identified by the Stockholm Convention in 2001, followed by six others (α-hexachlorocyclohexane [HCH], β-HCH, lindane, pentachlorophenol and its salts and esters, and technical endosulfan and its related isomers) (UNEP, 2008). At present, OCPs are still being manufactured and used in some countries.

As a large agricultural country, China produced and used large quantities of OCPs in the past (Li et al., 1998; Wei et al., 2007). By 2003, the accumulated productions of DDT, HCH, HCB (1988–2003) and toxaphene were 459,000, 141,366, 79,278, and 20,660 tons, respectively (Hu et al., 2007). Although the use of OCPs for agriculture was banned in China since the 1980s, they have continued to be detected in the environment and humans in the country (Qin et al., 2011; Wang et al., 2017). Concentrations of p,p’-dichlorodiphenyldichloroethylene (DDE), HCB, and HCH in body fat and sera of the Chinese population were higher than those found in many other parts of the world (Ali et al., 2016; Hu et al., 2007; Qin et al., 2011).

Exposure to OCPs has been reported to be associated with several adverse health conditions such as diabetes, metabolic syndrome, and insulin resistance (Lee et al., 2007; Lee et al., 2011; Turyk et al., 2009a). In particular, a growing number of studies have indicated that OCP exposure may be a diabetogenic factor (Evangelou et al., 2016; Son et al., 2010; Turyk et al., 2009a; Zong et al., 2018). In recent years, the prevalence of diabetes has increased dramatically all over the world. In 2017, 425 million people were estimated to have diabetes worldwide, accounting for 8.8% of adults aged 20–79 years. The number of people with diabetes is expected to reach 629 million by 2045 (IDF, 2017).

A large number of recent epidemiological studies have investigated the effect of OCPs on type 2 diabetes (Aminov et al., 2016; Gasull et al., 2012; Park et al., 2019; Turyk et al., 2009b). However, no study has focused on such associations in Chinese populations. In addition, the pathogenesis of type 2 diabetes affected by OCPs remains largely unclear. Type 2 diabetes is characterized by abnormal insulin secretion caused by pancreatic β-cell dysfunction and/or insulin resistance (Chatterjee et al., 2017; Zimmet et al., 2001). As standard glycemic markers, fasting plasma glucose (FPG) and hemoglobin A1c (HbA1c) have been used to diagnosis diabetes. Thus, knowledge on how OCP exposure influence the levels of diabetes biomarkers could offer insight on mechanisms linking OCP exposure with the risk of diabetes. In addition, previous studies found a direct relation between elevated levels of cholesterol and reduced insulin secretion (Hao et al., 2007), indicating that levels of lipid fractions in human serum may be associated with the development of diabetes. However, the mediation effects of lipids on the associations between OCPs and diabetes have not yet been clarified.

In the present study, we conducted a case-control study to explore the associations between OCP exposure and the prevalence of type 2 diabetes among a Chinese population. To further clarify the potential mechanisms of OCP exposure with the development of type 2 diabetes, we analyzed the associations between OCPs and FPG, HbA1c, as well as lipid factions in nondiabetic participants.

Section snippets

Study cohort

A hospital-based case-control study was conducted during 2016–2017 in Shandong Province in East China. Details about the population have been described previously (Han et al., 2020). Briefly, 507 participants aged 25–74 years were enrolled in this study initially, including 265 participants diagnosed with diabetes and 242 participants without diabetes. All participants were recruited at Shandong Provincial Qianfoshan Hospital, and participants without diabetes were selected from people who went

Baseline characteristics

Fig. 1 shows the comparison of clinical chemistry parameters in serum samples between case and control groups. It was not surprising that participants with diabetes had higher BMI, FPG, and HbA1c and lower levels of HDL-C than nondiabetics. As we know, overweight or obesity is a risk factor for diabetes (Hu et al., 2001; Lee, 2012). In addition, type 2 diabetes is often accompanied by dyslipidemia and characterized by high levels of triglyceride and small dense LDL particles and a low level of

Conclusion

In conclusion, results of this case-control study suggest that OCP exposure is significantly associated with elevated risk of type 2 diabetes in the population of this study. In addition, OCP exposure may disrupt glucose homeostasis and lipid metabolism in participants without diabetes, and this may contribute to the development of type 2 diabetes. Future research is necessary to confirm the effects of OCPs on the pathogenesis of type 2 diabetes.

Competing financial interests

All authors declare they have no actual or potential competing financial interest.

CRediT authorship contribution statement

Xu Han: Conceptualization, Methodology, Software, Writing - original draft. Feng Zhang: Resources. Lingling Meng: Resources. Yuedong Xu: Resources. Yingming Li: Conceptualization, Writing - review & editing, Funding acquisition. An Li: Writing - review & editing. Mary E. Turyk: Writing - review & editing. Ruiqiang Yang: Writing - review & editing. Pu Wang: Writing - review & editing. Jianqing Zhang: Writing - review & editing. Guibin Jiang: Writing - review & editing.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (91743206, 21777186 and 41676183), the Eco-environmental Excellent Innovation projects of Research Center for Eco-Environmental Science (RCEES-EEI-2019-01), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14010100), and the Sanming Project of Medicine in Shenzhen (No. SZSM201811070).

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