Relation of urinary bisphenol concentration and diabetes or prediabetes in French adults: A cross-sectional study

PLOS ONE RESEARCH ARTICLE Relation of urinary bisphenol concentration and diabetes or prediabetes in French adults: A cross-sectional study Julie Delepierre, Sandrine Fosse-Edorh, Clémence Fillol, Clara Piffaretti ID* Santé Publique France, The French National Public Health Agency, Saint Maurice, France * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 Abstract Background OPEN ACCESS Citation: Delepierre J, Fosse-Edorh S, Fillol C, Piffaretti C (2023) Relation of urinary bisphenol concentration and diabetes or prediabetes in French adults: A cross-sectional study. PLoS ONE 18(3): e0283444. https://doi.org/10.1371/journal. pone.0283444 Editor: Iman Al-Saleh, King Faisal Specialist Hospital and Research Center, SAUDI ARABIA Received: August 12, 2022 Accepted: March 8, 2023 International research has recently shown an association between exposure to bisphenol A (BPA) and the risk of diabetes, although limited results are available for exposure to bisphenol S (BPS) and bisphenol F (BPF). The aim of this study was to examine the relationships between impregnation with BPA, BPS, and BPF and the prevalence of diabetes or prediabetes in the French adult population. Methods Based on the Esteban cross-sectional study, 852 adults aged 18 to 74 years living in France were included. To assess the link between urinary concentration of BPA, BPS and BPF and a state of dysglycemia (diabetes or prediabetes), logistic regression multivariable models were performed and adjusted for known risk factors for diabetes and urine creatinine concentration. Published: March 30, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0283444 Copyright: © 2023 Delepierre et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Due to legal and ethical concerns, the data underlying the results presented in the study are available on justified request from Santé publique France, the French Results The percentage of included individuals with diabetes or prediabetes was 17.8% (95% CI = [15.3–20.4]). Urinary BPA concentration was significantly higher in people with diabetes or prediabetes, independent of the known risk factors for diabetes (OR for an increase of 0.1 units in log-transformed concentration of BPA (μg/L) = 1.12; 95%CI = [1.05–1.19], p < 0.001). However, we did not find any significant independent association between urinary BPS and BPF levels and the prevalence of diabetes or prediabetes. Conclusions In this sample, considering the diabetes risk factors, diabetes or prediabetes was positively associated with higher urinary BPA concentration but not with urinary BPS and BPF concentrations. However, analysis of prospective longitudinal studies are still necessary to demonstrate a causal link between bisphenol exposure and the risk of diabetes or prediabetes. PLOS ONE | https://doi.org/10.1371/journal.pone.0283444 March 30, 2023 1 / 11 PLOS ONE national public health agency (https://www. santepubliquefrance.fr/). Funding: The French National Public Health Agency runs the French human biomonitoring programme, which is funded by the French Ministries of Health and Environment. The funders were part of a steering committee but had no role in data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Exposure to bisphenols and diabetes or prediabetes Introduction Type 2 diabetes is a chronic disease caused by the insufficient secretion of insulin by the pancreas or the reduced action of the insulin produced. The burden of diabetes-associated mortality and morbidity as well as the cost of the disease make it a major public health challenge. The prevalence of diabetes among adults has increased worldwide from 4.7% in 1980 to 8.5% in 2014 according to the World Health Organization (WHO) [1]. It was estimated to be 10.5% in 2021, rising to 12.2% in 2045, according to the International Diabetes Federation [2]. Age, sex, obesity, sedentary lifestyle, and family history are known risk factors for type 2 diabetes, but the unfavorable development of the disease has prompted the search for new factors likely to induce dysglycemia [3, 4]. Prediabetes is a high-risk state of diabetes and cardiovascular diseases, but effective strategies implemented at this stage can delay or prevent the development of diabetes [5]. In France, according to data from the French Nutrition and Health Survey (ENNS) in 2006–2007, the prevalence of diabetes and prediabetes was estimated at 5.1% and 5.6%, respectively, while it reached 7.4% and 9.9% in the Esteban survey in 2014–2016 [6]. Recently, international research on the potential contribution of exposure to environmental chemicals in the etiology of diabetes has rapidly expanded. Although causality has not yet been demonstrated, an overall positive association has been found between certain chemical substances present in the environment and diabetes. Therefore, it is necessary to continue research to improve our understanding of the role played by environmental exposures and facilitate the implementation of prevention strategies [7]. Certain environmental chemicals are endocrine-disrupting chemicals, that is, substances capable of interfering with the hormones present in the blood and acting on the organs regulating blood sugar and lipemia. Observational studies have shown a positive relationship between endocrine-disrupting chemicals and the diabetes epidemic [8–11]. Bisphenol A (BPA) is a known endocrine-disrupting chemical, meaning that it may be a risk factor for diabetes. The ubiquity of BPA in the environment, especially in food packaging, drinking water, dental materials, thermal paper, household dust, and tobacco smoke, makes its urinary concentration detectable in more than 90% of individuals [8–11]. Experimental studies have shown that BPA plays a role in the development of insulin resistance, adipogenesis, and dysfunction of β cells in the pancreas [12, 13]. In mice, research showed that long-term BPA exposure resulted in increased adipose tissue mass and hyperglycemia [12]. In humans, according to two meta-analyses mainly based on cross-sectional studies, urinary BPA concentrations are significantly associated with the risk of diabetes [14, 15]. To our knowledge, only one study has examined the relationship between prediabetes and BPA: the authors observed a positive independent association between higher levels of urinary BPA and prediabetes [16]. Li (...truncated)