Persistent organic pollutants in young adults and changes in glucose related metabolism over a 23-year follow-up
Introduction
There is substantial in-vitro and in-vivo evidence that persistent organic pollutants (POPs) can act as endocrine disruptors and promote metabolic dysregulation (Lee et al., 2014). Recent studies showed that rats fed high-fat diets with POPs-contaminated salmon oils (compared to decontaminated salmon oil) (Ruzzin et al., 2010), and mice fed commercially farmed salmon filets contaminated with background POPs (compared to salmon specially raised to avoid POPs exposure) (Ibrahim et al., 2011) developed greater insulin resistance, abdominal obesity, and hepatosteatosis. In various population-based cross-sectional studies worldwide, exposure to several POPs at background concentrations (particularly polychlorinated biphenyls (PCB) and organochlorine pesticides) has been found to have strong positive associations with insulin resistance, pre-diabetes and diabetes after adjustment for confounders (Codru et al., 2007; Gasull et al., 2012; Lee et al., 2006, Lee et al., 2007a, Lee et al., 2007b; Uemura et al., 2008). Longitudinal studies in the USA, Sweden, Taiwan and Italy have also reported significant associations of organochlorine pesticides and PCBs with incidence of diabetes (Lee et al., 2011a, Turyk et al., 2009, Vasiliu et al., 2006, Wang et al., 2008) and diabetes-related deaths (Bertazzi et al., 2001). Nevertheless, longitudinal studies with repeated measures are scarce. Such studies could greatly contribute to establish the temporal sequence of metabolic events following POPs exposure.
We previously described non-monotonic (specifically, inverted U-shaped) associations of organochlorine pesticide and PCB blood concentrations with diabetes in a case (diabetes)-control study nested within the Coronary Artery Risk Development in Young Adults (CARDIA) study (n=180) (Lee et al., 2010). Among controls, organochlorine pesticides and PCBs also had positive quadratic associations with BMI, triglycerides and insulin resistance, and negative associations with HDL-cholesterol 18 years after the measurement of POPs (Lee et al., 2011b). The reported inverted U-shaped associations of organochlorine pesticides and PCBs with diabetes support the hypothesis that high body burdens of endocrine disrupting chemicals can exert inhibitory effects on processes that are stimulated at much lower doses.
The present investigation further characterizes the associations between blood concentrations of POPs from background exposures in 1987–1988 and glucose dysregulation over the following 23 years among participants with and without diabetes of the CARDIA nested case-control study. Given the possibility of varying associations between POP exposures and glucose dysregulation at different stages of life (Lee et al., 2014), and considering increasing accumulation of POPs in tissues and higher prevalence of cardiovascular and endocrine alterations with age (particularly, after age 40) (National Center for Health Statistics, 2013), we tested the hypothesis that the associations between POPs and glucose dysregulation would be strongest among older individuals.
Section snippets
Participant selection
In 1985–1986 (CARDIA year 0), CARDIA examined 5115 black and white participants 18–30 years of age, recruited from the general populations of Birmingham, AL, Minneapolis, MN, and Chicago, IL and from the Kaiser Permanente Medical Care Plan in Oakland, CA (Friedman et al., 1988, Hughes et al., 1987). Since year 0, there have been 7 follow-up examinations at years 2, 5, 7, 10, 15, 20 and 25 (2010–2011). The study was approved by the institutional review boards of the University of Minnesota,
Participant characteristics
Characteristics of participants with and without diabetes by quartiles of the 32 POP summary score are listed in Table 1. In both groups, participants with higher scores of the 32 POP summary were older, had higher fasting glucose and HbA1c values at year 25, and had higher year 2 cholesterol concentrations than participants with lower scores (unadjusted associations). The prevalences of glucose lowering medication use among diabetics were 78% and 70% for years 20 and 25, respectively.
POPs, HbA1c and fasting glucose
We
Discussion
Our present longitudinal analyses show that serum concentrations of organochlorine pesticides and PCBs in early adulthood were positively associated with measures of decreased insulin sensitivity independently of BMI, after participants reached 40 years of age (and particularly at ≥48 years of age). These findings were observed in normoglycemic controls and among treated people with diabetes.
While many POPs have been banned in most countries, they are still detected in the food supply (
Role of funding source
None.
Competing financial interests
None.
Institutional review board approval for research
The study was approved by the institutional review boards of the University of Minnesota, University of Alabama at Birmingham, Northwestern University, and the Division of Research at Kaiser Permanente Health Care Plan. Participants signed informed consent at every examination.
Acknowledgement
The Coronary Artery Risk Development in Young Adults Study (CARDIA) is supported by Contracts HHSN268201300025C, HHSN268201300026C, HHSN268201300027C, HHSN268201300028C, HHSN268201300029C, and HHSN268200900041C from the National Heart, Lung, and Blood Institute (NHLBI), the Intramural Research Program of the National Institute on Aging (NIA), and an intra-agency agreement between NIA and NHLBI (AG0005). The YALTA study is supported by R01HL53560. This investigation was further supported by the
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